Participant number. \* Participants were asked to rate how RA has impacted their life on a scale of 1–7, from "no impact" to "extreme impact".

### *3.2. Healthy Appearance as a Myth*

3.2.1. Invisibility and Lack of Validation

A common struggle highlighted by participants was others' inability to comprehend that the participants were sick. Many endured physical impediments regularly but showed no discernible signs of disease. People often did not believe that the participants were experiencing pain or take the condition seriously, making it difficult for participants to feel supported and validated.

*"It's one of those things you can't see it: I look fine, I look completely fine* . . . *. It's kind of like the silent suffering* . . . *because you don't look any different, you don't act any different, and I kind of learned to just deal with it." (Participant #25)*

*"I've wondered a lot like is this all just in my head* . . . *and how much of this is real?" (#24)*

Relationships were strained by their friends' and family's incapacity to see the symptoms and consequently, to believe the participants or show sympathy. Friendships dissolved as people took offense when the participants had to cancel plans due to flare-ups or fatigue. This further loss of socialization brought participants to feel a sense of deprivation and resentment toward the disease.

*"A lot of friends think you just don't want to hang out with them. I can plan and whatever I want to plan but, on the day, when it's time to do it, if I can't do it, I can't do it." (#2)*

*"You have to cancel a lot on people, and that's really depressing." (#8)*

### 3.2.2. Preference to Hide RA from Others

Although several participants were frustrated by RA's invisibility, others reported purposefully hiding their symptoms or not mentioning they had the disease; some felt both sentiments simultaneously. Participants intended to minimize being perceived as ailing to achieve a desired sense of normalcy. They also attempted to disguise or counter (sometimes unsuccessfully) the anguish they experienced inside.

*"(Acquaintances' response) is what I hate, they're like, 'Oh my God, I can't believe that you're so sick'* . . . *'You look so healthy! How?'* . . . *I feel like sometimes they think differently of me so I don't like sharing it with people." (#24)*

*"Every semester, I've had a moment where an advisor is like, 'hey, do you maybe not wanna do this semester?' And I'm like, 'No, I wanna do it!'* . . . *maybe more of a fear than a hope is being able to hold a full-time job and just live a normal life in that respect." (#30)*

*"Some days my husband comes home and I'm with full makeup and full jewelry everything— I'm looking great—and he's like 'what's going on here? You feel really bad today, don't you?' and I'm like 'yep.'" (#2)*

### 3.2.3. Embarrassment from Physical Symptoms

Adding to their predicament of preferring to hide the disease yet desiring to be understood, participants also described discomfiture with apparent physical symptoms. More prominent disease manifestations were indicative of sickness. Such visible signs could cause embarrassment and disappointment.

*"Your knees will look swollen, or your hands. And it was kind of embarrassing to go into dating because you tried to hide your twisted fingers." (#9)*

*"I want to go walking but I can't. It's like excruciating pain. It's embarrassing sometimes, because I want to do things but can't move." (#6)*

### *3.3. Identity Crisis*

Participants, moreover, indicated their dismayed realization that they were no longer the same person after diagnosis. Unable to perform daily tasks or forced to relinquish what they formerly enjoyed, many struggled to maintain their self-identity and described having difficulty recognizing themselves. The common misconception that RA only occurs at old age added to the confusion for both participants and others.

*"I couldn't hold the book, I couldn't do anything. I just felt so helpless, useless and that's not my mode. I'm a very independent person, I don't like to ask anyone for help, and so having to do that was really problematic. It was even problematic—and I'm just going to be blunt—to go to the bathroom." (#27)*

*"It was hard to think of myself as chronically ill." (#26)*

*"I am way too young to be ending up with RA because I thought of it as an older person's disorder." (#18)*

The perpetual exertion of managing or suppressing symptoms took a toll both mentally and physiologically. Many participants experienced self-doubt, frequent mood-swings, and long-term changes to their personalities or worldview.

*"I feel like I'm not as happy-go-lucky as I would like to be because it nags at you, distracts your mind." (#31)*

*"I was losing my mind. This is not like me." (#7)*

*"I was a very social person. I don't go out anymore...except for going to the doctors. I stopped any social engagement* . . . *it affects EVERY part of life. I was living in a black-and-white world (with no color)." (#21)*

RA also impacted fulfillment of responsibilities, which participants found upsetting and frustrating. They felt that their functionality as a parent, spouse, or employee was inadequate, and their performance of their roles within the household, office, or society seemed unsatisfactory. Some were confounded by the reversed role from caregiver to care-receiver.

*"The days I can't are the days my kids want to do everything, like 'mom I want to do this, ride bikes,' and I'm like 'talk to your dad.'* . . . *that for me, is hurtful." (#5)*

*"I couldn't have kids. And that's really sad when you come from a Latino family, and the family is the nucleus of everything." (#9)*

*"I left a really good job. I just couldn't handle the pressure and the stress with the RA symptoms." (#20)*

### *3.4. Occupying the Mindset*

RA became the determinant of all activities and plans. Many participants reported constantly thinking about RA, and that the fluctuating severity of symptoms dictated continuously how their day went. Even on a "good day" with minimal symptoms, the continuous dread or anticipation of pain or incapacity remained a burden.

*"I think about it every morning when I put my feet on the floor. Like when I get up, I know what kind of day it's going to be based on how I get up out of bed." (#12)*

*"I get nervous, I know I will have pain even before I can feel it." (#22)*

Participants also discussed the malevolent effects of RA on maintaining a sense of consistency in their lives and on their schedule. They regularly had to arrange for an alternative, bothersome plan. Many also shared nuisances due to the unpredictability of each day, whether simply getting out of bed, running errands, going to work, or taking a trip.

*"I would get up and leave for work earlier so that I could go and sleep in my car for an extra hour before going into the office. Even the driving, I would get fatigued* . . . *some days are just absolutely horrible." (#15)*

*"I might have a day when I'm feeling pretty good* . . . *but then there's a day when I don't* . . . *so then I get very frustrated because there are things I want to do or plan to do." (#17)*

*"It's really difficult to make plans living like that. I just committed myself to a 3-day trip with several friends and I'm wondering am I going to be able to go? And if I go, am I going to end up in the hotel the whole time?" (#13)*

### *3.5. Chronic Nature of the Disease*

The chronic nature of RA led to fear and despair, especially in the early stages of diagnosis. Participants expressed annoyance with the unknown of the disease and worried about their future, even with effective treatment or minor symptoms.

*"It started in my forties, and so does that mean that when I'm in my sixties, is it going to be really bad? And how long can it be maintained at a reasonable level? What happens when something isn't working and it hurts? And how bad can it be?" (#14)* ried about their future, even with effective treatment or minor symptoms. *"It started in my forties, and so does that mean that when I'm in my sixties, is it going to be really bad? And how long can it be maintained at a reasonable level? What happens when something isn't working and it hurts? And how bad can it be? (#14)* 

The chronic nature of RA led to fear and despair, especially in the early stages of diagnosis. Participants expressed annoyance with the unknown of the disease and wor-

*"I might have a day when I'm feeling pretty good…but then there's a day when I don't …so then I get very frustrated because there are things I want to do or plan to do."* 

*"It's really difficult to make plans living like that. I just committed myself to a 3-day trip with several friends and I'm wondering am I going to be able to go? And if I go,* 

*"The whole frustrating part is I have no idea what to expect moving forward." (#26) "The whole frustrating part is I have no idea what to expect moving forward". (#26)* 

As participants reluctantly adapted to an altered life, many found ways to improve their conditions by modifying their exercise routines, diets, or perspectives through positive thinking. Some had reached a neutral sense of acceptance or became at peace with RA. Through their experience battling the disease, participants described a sense of personal growth, gaining control and confidence in being able to persevere. As participants reluctantly adapted to an altered life, many found ways to improve their conditions by modifying their exercise routines, diets, or perspectives through positive thinking. Some had reached a neutral sense of acceptance or became at peace with RA. Through their experience battling the disease, participants described a sense of personal growth, gaining control and confidence in being able to persevere.

*"I know I would have to take the medication for life, there is no cure. What can I do? It happens to me and I will just face it." (#29) "I know I would have to take the medication for life, there is no cure. What can I do? It happens to me and I will just face it." (#29)* 

*"I'm the kind of person that says other people have it worse. So I find someone who has it worse than me and I say I can do it, I can survive." (#27) "I'm the kind of person that says other people have it worse. So I find someone who has it worse than me and I say I can do it, I can survive." (#27)* 

We further synthesized the themes and findings in Figure 1. We further synthesized the themes and findings in Figure 1.

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 11

*am I going to end up in the hotel the whole time?" (#13)*

*(#17)* 

*3.5. Chronic Nature of the Disease* 

**Figure 1. Figure 1.**Identified themes and struggles from RA patient interviews. Identified themes and struggles from RA patient interviews.

### **4. Discussion**

We identified four interconnected themes illustrating the imprints of RA on participants' lives and identities through in-depth focus groups and interviews. Their narrated experiences conveyed vivid accounts of the common mental and physical dilemmas patients regularly face. Participants expressed an overarching sense of frustration, apprehension, and lack of control in both managing RA symptoms and dealing with related social and psychological consequences. However, many were able to eventually come to terms with the illness and adapt, albeit reluctantly, to their new normal.

Earlier studies examined patients' preference for hiding symptoms and a desire for validation separately [4,37]. We uncovered the RA patients' concurrent intentions to conceal the disease and its manifestations while still seeking recognition to escape the disease's isolating effects. The suppression of knowledge about their illness might have made the disease feel even more confining and their experience invalidated. Other diseases have also been described as invisible, including fibromyalgia [38], chronic fatigue [39], and inflammatory bowel disease [40]. Our participants' qualitative reflections shed light on the seemingly contradictory inclinations encountered by RA and other patient populations.

These clashing sentiments are analogous to previous findings of RA's social impact, wherein patients described "illness-related shame" in being perceived as sickly and incapable [18]. Although the literature did not indicate whether this stigmatization was actualized or self-promulgated, our findings suggest a combination of both. Some participants were teased or treated differently by friends and family, but others tended to place guilt on themselves for not living up to expected roles. This self-disappointment was especially hurtful in a family context; such experiences were similar to that of mothers pervaded with guilt due to limited involvement in or forced exclusion from enjoyable family moments [41,42].

Moreover, our participants echoed an identity crisis pertaining to losing independence or self-esteem and feeling useless, which may contribute to personality change or depression. Participants were perceived differently by others, and came to (not) recognize themselves internally. These observations build upon existing understandings of RA-related identity conflict, where patients describe poor body-self unity in a physical sense [34,43]. Some felt uncomfortable in their own skin due to pain and bodily changes [5]. Others saw themselves as increasingly disabled and ineffective, propagating low selfconfidence [7,8]. These findings highlight the far-reaching effect of RA on self-perception and altering identity. Both providers and support systems need to address these emotional hardships of RA patients, as psychological distress could lead to worsened disease and related mental health outcomes [16,44]. This is where patient-centered, integrative care involving a multidisciplinary consultation could be most beneficial [21,23].

Adding to the literature of disease-associated anxiety [6,16], our results underlined how RA remained prominent in the participants' minds. The ever-presence of the disease amended all plans and routines, and thereby minimized any sense of consistency. The participants further disclosed sentiments ranging from anxiety and concern about their future to neutrality and acceptance of the disease being part of their lives with the unending need for maintenance. However, even with effective treatment or absence of pain, the chronic nature of RA was nevertheless frustrating and worrisome for both new and seasoned patients. Many participants not only feared and actively avoided potentially distressing circumstances, but lived in a perpetual state of anticipation of symptom manifestation and a terror of possible disability. Personalized medicine needs to account for these non-somatic factors that could influence how patients take or react to medication, disease progression, and health outcomes.

Previous research has connected behavior modifications to the disease's conditions with positive results, such as decreased intensity of depression, reduced feelings of guilt and hopelessness, and improved physical functions [8,14,42]. Although no action may entirely remove the afflictions patients face, we also found encouraging evidence of patients turning illness impediments into motivation for self-improvement in other areas of their lives. Future exploration of this transformative change of mindset could offer valuable lessons for personalized therapies.

Analysis of patient perspectives from their own narratives is critical for supporting this population and understanding their reality. Yet the clinical practices necessary to recognize and validate these psychological symptoms and forced alterations remain sparse [20,45,46]. Instead, treatment strategies have primarily focused on the pharmacologic and physical aspects. Healthcare professionals tend not to probe for cognitive and emotional problems beyond the more frequent diagnoses of anxiety and depression [12,14]. Patients have indicated a desire for discussing social and emotional issues with their care team but less than a quarter of them receive such support [47]. Studies concur that this exclusion of psychologi-

cal signs or inquiries is not a reflection of poor healthcare quality, but rather demonstrates the need for a greater understanding of the far-reaching impact of patients' struggles and multifaceted approaches to communication and treatment techniques [4,12,48]. The results of our qualitative investigation provided deeper insights into the complexity of psychological burdens in the RA population and informed education for both patients and providers for more holistic care. Future research into personalized medicine could explore the feasibility and effect of incorporating mental support in designing and evaluating treatment programs.

Numerous techniques have been proposed to better meet the psychological needs of RA patients, including encouraging patient involvement in medical decisions [15] and creating long-term goals [28], asking open-ended questions about the psychological impacts to allow for emotional venting [12,49], cognitive behavioral therapy [50], and the use of support groups [15,51]. These recommendations can help patients better address disease uncertainty and feelings of invalidation and uselessness. However, the effectiveness of these strategies on lesser-understood struggles has not been directly studied [47,48]. In addition, research is needed to determine if and how such therapies are actively sought by patients, or if physicians and nurses must encourage psychological counseling options as a complement to medications. Educational programs should also target the public so that families and communities can adequately offer support.

The current study has several limitations. First, the sample size was small. Different from quantitative studies, it is customary for qualitative studies to have a few dozen participants. A large majority of the participants were women, despite attention being paid to specifically recruit males as well, reflective of the doubly high incidence of RA in females (male−female ratio of RA prevalence is about 1:3) [2]. Future studies could incorporate more male perspectives, as existing findings are inconsistent as to whether men experience fewer, or perhaps differently expressed, psychological symptoms [28,34,48]. The heterogeneity of our participants in their demographic and disease-related characteristics ensured that the diverse perspectives of RA patients were represented. The subjective nature of qualitative coding could have introduced biases in the selection of themes and quotes. Other key ideas may have been overlooked due to confirmation or experimenter bias. Efforts were taken to reduce biases through consultation of the literature in developing the codebook and the utilization of multiple coders. Lastly, the volunteer-based sampling, though practical and common for similar observational studies, may have excluded patients who had different opinions or experiences but were unwilling or unable to participate.

### **5. Conclusions**

There is a lack of qualitative research in rheumatic diseases and healthcare in general [30,52], signaling a gap in the literature. Future research should incorporate more in-depth examinations into patients' needs as well as investigate illness-induced cognitive and emotional processes that influence health outcomes. Our study provides a novel, comprehensive perspective of RA patients' experiences beyond somatic functionality and across a variety of contexts. Highlighting and connecting the sociopsychological burdens resulting from physical limitations adds to the knowledge of the impact of a chronic disease. These insights demonstrate the persistent need and the patients' desire for more personalized care that includes psychological support. This need has also been recognized in treatment guidelines but the demand has not been met, leaving care provision incomplete for many patients. In addition to providing pharmaceutical therapies, healthcare professionals must acknowledge and address these struggles when discussing and planning treatment strategies to both validate and ameliorate patients' experiences.

**Author Contributions:** Conceptualization C.L., R.T. and P.T.; data acquisition C.L. and P.T.; data analysis and interpretation C.L., R.T., B.B. and P.T.; manuscript drafting C.L. and B.B.; critical revisions C.L., R.T., B.B. and P.T. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was partially supported by Duke University Bass Connections.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by Duke University Institutional Review Board.

**Informed Consent Statement:** Informed consent was obtained from all participants involved in the study.

**Data Availability Statement:** The portion of the de-identified transcript directly pertaining to this paper is available from the corresponding author for one year from the date of publication upon reasonable request with a methodically sound proposal.

**Acknowledgments:** The authors would like to thank their research team's assistance in the data collection process and The Link Group's support in facilitating the focus groups and interviews. The authors are grateful for the study participants candidly sharing their experiences.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


### *Review* **Moving towards Integrated and Personalized Care in Parkinson's Disease: A Framework Proposal for Training Parkinson Nurses**

**Marlena van Munster 1,\* , Johanne Stümpel 2,3 , Franziska Thieken <sup>1</sup> , David J. Pedrosa <sup>1</sup> , Angelo Antonini <sup>4</sup> , Diane Côté 5 , Margherita Fabbri <sup>6</sup> , Joaquim J. Ferreira 7,8,9, Evžen R ˚užiˇcka <sup>10</sup>, David Grimes <sup>11</sup> and Tiago A. Mestre <sup>11</sup>**


**Abstract:** Delivering healthcare to people living with Parkinson's disease (PD) may be challenging in face of differentiated care needs during a PD journey and a growing complexity. In this regard, integrative care models may foster flexible solutions on patients' care needs whereas Parkinson Nurses (PN) may be pivotal facilitators. However, at present hardly any training opportunities tailored to the care priorities of PD-patients are to be found for nurses. Following a conceptual approach, this article aims at setting a framework for training PN by reviewing existing literature on care priorities for PD. As a result, six prerequisites were formulated concerning a framework for training PN. The proposed training framework consist of three modules covering topics of PD: (i) comprehensive care, (ii) self-management support and (iii) health coaching. A fourth module on telemedicine may be added if applicable. The framework streamlines important theoretical concepts of professional PD management and may enable the development of novel, personalized care approaches.

**Keywords:** Parkinson's disease; nursing training; integrated care; Parkinson nurse; personalized care; multidisciplinary care

### **1. Introduction**

Parkinson's disease (PD) is a progressive non-curable neurodegenerative disorder with an age of onset usually over 60 and presenting with complex motor and non-motor features such as cognitive impairment, mood and sleep disorders, autonomic dysfunction, and pain. In Europe, 1.2 million people are living with PD [1] with an increasing incidence

**Citation:** van Munster, M.; Stümpel, J.; Thieken, F.; Pedrosa, D.J.; Antonini, A.; Côté, D.; Fabbri, M.; Ferreira, J.J.; R ˚užiˇcka, E.; Grimes, D.; et al. Moving towards Integrated and Personalized Care in Parkinson's Disease: A Framework Proposal for Training Parkinson Nurses. *J. Pers. Med.* **2021**, *11*, 623. https://doi.org/10.3390/ jpm11070623

Academic Editors: Riitta Suhonen, Minna Stolt and David Edvardsson

Received: 30 April 2021 Accepted: 25 June 2021 Published: 30 June 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

in the elderly, so that the number of affected patients worldwide is expected to double by 2030 [2]. PD ranges among the top ten most resource intensive brain disorders in Europe [1] so that the need for PD services is expected to build up and consequently the burden on healthcare systems. This reality warrants the development and implementation of a care delivery model that conforms with society resources to guarantee its sustainability, while promoting better public policies, and reducing the overwhelming societal impact of PD [3]. The complexity of PD implies specific requirements for the design and delivery of care. Nevertheless, to date personalized care delivery models are rare [4]. While it has been shown that integrated and multidisciplinary care delivery models following a personalized care approach have positive implications for persons living with PD (PwPs), care partner and care providers, their implementation is difficult due to several reasons [3–5]. A key aspect for personalizing care services, is the availability of specialized staff [3]. Among these healthcare professionals, Parkinson Nurses (PN) can accomplish important tasks in the care process, such as providing mental health support, monitoring symptom progression and promoting patient navigation through the local healthcare system [3,6,7]. There has not been a consensus on defining the PN, but following Parkinsons UK, a PN can " . . . provide expert care because they only work with people with the condition." They describe the major role of a PN in providing care as whilst " . . . helping people to manage their medication" [8], the provided care by a PN will result in less side effects. Generally, PN help patients to manage their illness through making, for example by giving information and support to people with Parkinson's.

However, there are various definitions and descriptions not only of the role in the care team but there are also multiple approaches on the training of PNs as highlighted in Table 1.


**Table 1.** Existing Training Opportunities for Parkinson Nurses in different Countries.


**Table 1.** *Cont.*

1 In the United States and Canada, a variety of different forms of nurse education exist, and the nomenclature also holds a wide range of designations in both countries. The role and education of APNs (Advanced Practice Nurses) will be discussed here as an example. An explicit training as an advanced practice nurse for Parkinson's disease is not currently available in the United States and Canada.

Even though specialized training for PN on the delivery of personalized care services has been recommended [17], no framework has been proposed yet and existing curricular do not explicitly in cooperate it. By reviewing the specific requirements for the design and delivery of care in PD, we aim to propose a training framework for PN to facilitate the personalization and integration of care delivery.

### **2. Materials and Methods**

We adopted a conceptual research approach to synthesize different perspectives on the theme of PD care and role of nurses. [18]. We entertained various conceptual streams from health care design, care delivery and medical prerequisites of PD. We considered the following questions to be essential to PN training: What are the care priorities for people living with PD (PwPs)? What type of PD-specific skills should a PN be equipped with in order to meet these needs?

The conceptualization of a training framework, may thus be seen a synthesis from various theoretical concepts which address care priorities for PD. We followed the structure of a line of reasoning to model this novel concept [19]. In this approach different hypothesis are formulated which then are integrated into a proposed model [19]. Following Lynham's Growth Cycle of Applied Theory-Building, the conceptualization of the training framework was informed by research, theory and practice [20]. A scoping literature review was conducted in order to identify relevant literature on care for PD. We chose The methodological approach of a scoping review, as it has been recommended to be particularly useful for categorizing the existing scientific literature in a defined research area in terms of its type, characteristics, and scope [21].The literature review was conducted in March 2020, (with an update in April 2021) by searching MEDLINE and Web of Knowledge (Figure 1), using the terms Parkinson's disease, concept and care. The search was not restricted in terms of the publication year. Studies were included if they described or theorized care models or concepts, relevant to PD and were either published in English or German. If a paper referred to another theory which was not focusing on PD but still relevant for the research aim (developing a PN training framework), the paper and theory reported also included. Opinion papers, literature reviews not proposing a new care model or studies testing short term interventions (i.e., physical therapy) were excluded. Publications focusing on palliative care were excluded, because this was seen as a different topic, where PwPs and care partners develop unique needs and concepts become relevant, which distinguish from other PD care literature. The search strategies, as well as a detailed list of in- and exclusion criteria can be accessed in the Supplementary Material (Table S1).

As a first step, publications retrieved from the literature review were grouped into 3 categories: intervention, practical care concept or theoretical concepts. Next, practical care concepts, guidelines and interventions were reviewed to identify care priorities for PD. Consecutively, a code was invented, whenever a new guiding care principle was mentioned following the approach of an undirected content analysis [22]. Thirdly, the identified care priorities informed the formulation of two hypothesis regarding a PN training framework. Fourth, the content of theoretical concepts was analyzed according to the previously identified care priorities. Finally, the content was used to construct a line of reasoning and to propose a framework for training PN. The literature research and coding, following the guidelines of PRISMA-ScR [23], was independently performed by two researchers (M.vM; J.S.). Discrepancies in coding and grouping were solved via discussion with a third researcher (F.T.). The final framework was commented by a range of PD experts for the iCARE-PD consortium (http://icare-pd.ca/, 1 June 2021), including PN, neurologists and scientists.

**Figure 1.** PRISMA flow diagram for the conducted scoping review. **Figure 1.** PRISMA flow diagram for the conducted scoping review.

### **3. Results**

rologists and scientists.

As a first step, publications retrieved from the literature review were grouped into 3 Fifty-six publications were included for final synthesis. (Figure 1).

categories: intervention, practical care concept or theoretical concepts. Next, practical care concepts, guidelines and interventions were reviewed to identify care priorities for PD. Consecutively, a code was invented, whenever a new guiding care principle was mentioned following the approach of an undirected content analysis [22]. Thirdly, the identified care priorities informed the formulation of two hypothesis regarding a PN training framework. Fourth, the content of theoretical concepts was analyzed according to the previously identified care priorities. Finally, the content was used to construct a line of reasoning and to propose a framework for training PN. The literature research and coding, The analysis included nine interventions implementing and evaluating a care model for PD, two guidelines for organizing PD care, 29 publications describing an implemented care model and 18 conceptual papers. Few publications described the same practical care model [24–27] whereas two reported the same care concept [28,29]. Consequently, 35 publications informed the definition of care priorities for PD care and 18 models informed the conceptualization of a PN training framework. Based on the implemented care models and recommendations, nine priorities for the organization and delivery of PD care were identified. The priorities and the frequency with which they were mentioned are summarized in Table 2.

following the guidelines of PRISMA-ScR [23], was independently performed by two researchers (M.vM; J.S.). Discrepancies in coding and grouping were solved via discussion with a third researcher (F.T.). The final framework was commented by a range of PD ex-


**Table 2.** Care Priorities for Parkinson's Disease in Practical Care Concepts.

The conceptual models covered the same care priorities as the practical care concepts. In addition to these priorities, the priority *personalized care* was observable in the conceptual models. The priorities and the frequency with which they were mentioned are summarized in Table 3. A content summary of the included models can be found in the Supplementary Material (Table S2).

**Table 3.** Care Priorities for Parkinson's Disease in Conceptual Models.


Based on the identified care priorities for PD patients and their conceptualization in various care models, we present two hypotheses on the training requirements for PN, followed by relevant question(s) related to each hypothesis and their implication to the development of a PN training framework.

**Hypothesis 1 (H1).** *Parkinson Nurses should be trained to deliver comprehensive care for people living with parkinson's Disease and their care partner.*

Given the heterogeneous and progressive nature of PD, treatments require a high degree of personalization, as this enables the adjustment of the multiple existing management options to the clinical presentation, the individual symptoms and their progression, and the care needs of PwPs [81]. Based on the analyzed concepts of PD care, two models described personalized care management as important aspect [70,75] whereas two other models included the provision of tailored information [69,80].

What is personalized care? Personalizing care means adapting the care process to the patients' needs and preferences [78] (813) (p.813). Van Halteren et al. described five essential aspects of personalized care: providing information, proactively monitoring early detection signs and symptoms and the care process, coordinating care and navigating the patient in the healthcare system [78].

Implications for a PN curriculum: In reference to the conceptualization of a training framework, a PN ought to be competent to identify care needs and preferences for each individual. Additionally, they must be able to decide their implications for the care plan.

Personalizing care approaches means, that patients' perspective plays a central role in decision-making processes and leads to another frequently mentioned care priority: patient-centered care. Two models incorporated patient-centeredness as a pivotal aspect for care delivery [66,70] and three models highlighted the patients perspective as central component [65,68,71].

What is patient-centered care? Implementing a patient-centered perspective means '*[* . . . *] ensuring that patient values guide all clinical decisions*.' ([69], p. 360). Good communication is needed in order to identify these values [64,67]. PN must be able to meet patients and care partner with respect and empathy [64,67,69,72]. Providing emotional support and creating a trustful relationship has been mentioned as important element for implementing patient-centered care across all three identified concepts [67,69].

Implications for a PN curriculum: In reference to the conceptualization of a training framework, a PN ought to be trained in communicating with PwPs and care partner to enhance patient-centeredness.

What is integrated care? Integrated care is a form of multidisciplinary care. A multidisciplinary care approach can be described as an approach '[ . . . ] with contributions by experts from multiple complementary disciplines.' [49] (p.167). Bringing together these professions is what Goodwin described as professional integration [74]. Other concepts referred to this by highlighting the importance of incorporating physicians' perspectives in the care process; coordinating care across professions and implementing a clinical information system [64,68,77].

While there is a wide range of definitions, integrated care can be described as a care approach that aims '[ . . . ] bringing together key aspects in the design and delivery of care systems that are fragmented' [74] (p 1) (p.1). Three conceptual models described components that an integrated care approach should consider [66,74,76]. The Rainbow defines four primary domains of integration: clinical, professional, organizational, and systems integration, whereby functional and normative enablers play a role [76]. The Development Model of Integrated Care (DMIC) presents a nine-cluster model for organizational development in four phases with an emphasis on actual co-operation and commitment [66]. The DMIC also focuses on conditions for achieving effective collaboration, such as patient engagement, clarity of roles and responsibilities within the care delivery team [66]. Goodwin's work [74] distinguishes not only in the form in which integrated care should be designed (horizontal, vertical, sectoral, people-centered and whole-system), but also by how it is classified (by type, level, process, breadth and degree/intensity) [74].

An important aspect that was identifiable across the three integrated care concepts is care organization [66,74,76]. For PD, the inclusion of multiple healthcare professionals and the coordination of their care actions is of utmost importance [3]. Delivering integrated care has been described as central aspect for meeting PwPs complex care needs, reducing the burden of care partner and improving health care professional satisfaction [4].

Two of the conceptual models in integrated care services as important aspect for care delivery [73,75] and three models referred indirectly to the integration of care by mentioning a continuous collaboration of care providers, the organization of care and the selection of combined helping methods as important aspects of care organization [68,77].

Implications for a PN curriculum: PN fulfill important roles as clinical care integrators, navigators, support person and supervisor [4,75,82]. PNs, as part of the professional care team, should be able to design and implement a flexible routine network of service provider to support PwPs and their care partner in inpatient and outpatient settings.

What is home-based and community-centered care? Home-based care '*[* . . . *] refers to clinical practices that provide physician- or nurse practitioner led, longitudinal interdisciplinary care [* . . . *]*' at home ([79], p. 1). According to the Quality of Care Framework for Home-Based Medical Care [79], the essential elements are: assessment, care-coordination, patient and care partner education, provider competency, safety, provider competency and shared decision-making [79]. Additionally, factors such as patient and care partner experience, financial aspects and quality of life should be considered [79]. According to the model, patient-centered care can be promoted through the use of quality indicators that assess patients' access to care services, as well as their satisfaction with the expertise of care providers [79]. From the reviewed conceptual models, two referred indirectly to the organization of home-based care by mentioning the support of autonomy as important aspect for organizing patient-centered care [55,56]. Three models highlighted the need to assess available community resources [58,68], one model referred to the importance of assessing the personal lifestyle [59], one model defined quality criteria for the implementation of home-based telemedicine [19,20] and five models mentioned the navigation of the patient towards these resources and the reduction of barriers as important aspect for the organization of care and the selection of combined support methods as important aspects of care organization [59,60,62,68,69].

Delivering community-centered care means bringing '*[* . . . *] care directly to the patients in the local community setting [* . . . *].*' ([30], p. 1). Consequently, knowledge about the community and available resources is required. Based on the literature review, no model exclusively focusing on community-centered care was identified, however several concepts included available community resources as important quality aspects of care [67,77] as further detailed above.

Delivering care at home and within the community is important for PwPs and their care partners in order to enable access to care [3,73,83]. Additionally, home-based care for PwPs is becoming increasingly important from a demographic (e.g., aging, immobile population) and social (e.g., patients having a pronounced desire to continue living in their own homes) point of view [68].

Implications for a PN curriculum: Based on the concepts of home-based and communitycentered care, we propose that the quality of care provided by PN may be influenced by level of coordination skills of different stakeholders in the healthcare system and knowledge about local healthcare resources. Thus, PN should be trained to map available community resources and navigate PwPs towards them.

**Hypothesis 2 (H2).** *Parkinson Nurses should be trained to deliver self-management support to persons with Parkinson's Disease and their care partner.*

Self-management support (SMS) and patient-education are critical elements of effective PD management [4,84], and key component of integrated care. SMS is a top priority for PwPs when asked about their care requirements [85]. SMS and patient-education help to reduce disease progression, complications and costs [4,84,85].

What is patient and care partner education? Based on Graham's concept, patient and care partner education are a form of knowledge translation [80]. The ability of lifelong learning is an important aspect of healthy aging and may be jeopardized by PD [70]. Implementing learning processes and empowering patients and care partner through education characterize integrated care concepts that were included in the analysis [66,69,75,77]. According to the Knowledge Translation Framework, patient education should be based on identified problems and adapted knowledge based on these problems. Patients and care partner should be motivated to use the delivered knowledge. Additionally, the identification of barriers and the use of knowledge should be evaluated continuously [80].

What is self-management support? Self-management support '*[* . . . *] aims to empower patients with the skills and confidence necessary to manage their clinical disease*.' ([73], p. 25). Activities include patient education, monitoring changes in symptoms and abilities, goal setting, and problem-solving [73]. Based on Orem's Self Deficit Theory, self-management support is needed, when the client's self-care demand exceeds the available self-care agency [68]. From the literature review, four conceptual models were identified that included self-management support as important aspect of care [65,70,73,77]. The Glasgow model (or 5-A's approach) describes five important actions that should be taken by the health-care professional when delivering SMS to the patient, namely: assessing, agreeing, advising, arranging and assisting. Another model, which is often referred to by SMS interventions for PwPs is the Chronic Care Model [77]. The model does not exclusively

focus on SMS, but describes SMS as one of six dimensions, which should be addressed to improve care for patients with a chronic disease. According to the model, all dimensions affect each other, which is why all dimensions should be considered when aiming to improve care. The Chronic Disease Self-Management Model [77] is another model, which does not explicitly address PwPs but informed SMS approaches for PD [86]. Similar to the Glasgow model, it focuses on the relationship between the healthcare professional and the patient, however, a stronger focus is placed on the motivational aspect. According to the model, a good SMS-program pays attention to emotional and role management in addition to medical management and incorporates techniques to improve the patients' confidence.

Implications for a PN curriculum: PN play an important role in delivering SMS to PwPs [4,87,88], as good SMS relies on support from educated health professionals [88]. PN have a have a close patient contact and thus, are ideal professionals for delivering SMS [88]. In order to advise and assist PwPs properly, an understanding of the disease and its complexity is required, making it an essential part of a PN training framework. Considering the Knowledge Translation Framework, we propose that a PN training should include aspects of motivational interviewing in order to facilitate knowledge use by PwPs and their care partners [89].

Finally, one of the identified theoretical concepts considered telemedicine [28,29]. Telemedical applications can improve PwPs access to care, enhance quality of life and reduce the burden of care partner [90]. However, their purpose can vary greatly [28], which is why we propose to add a fourth module to the PN training framework when applicable, specifically focusing on the available technology.

### *Proposing a Framework for Training Parkinson Nurses to Deliver a Personalized Care Approach*

In the previous section, we have formulated two hypotheses: (1) PN should be trained to deliver comprehensive care for PwPs and their care partner and (2) PD Nurses should be trained to deliver self-management support to PwPs and their care partner. Based on the review of conceptual models, we identified the following requirements to a framework for training PN:


Understanding the disease is a fundamental prerequisite for delivering care and, consequently, a foundational knowledge and skills for PN training [6,17,82]. PN must be able to adapt care delivery to the care requirements of PwPs and care partner, which change across the course of the disease. After completing the first module, PN are equipped with skills, that are important for integrating, personalizing and centering care around the patient. Besides a sound medical knowledge, PN must be able to understand and

conduct clinical assessments [91]. These assessments may help the PN to evaluate patient needs as a starting point for discussion about care plans. Additionally, aspects of patient education and self-management support come into play when the PN discusses tests results or care plans with the patients. Consequently, we propose training on clinical assessments. And obtaining clinical conversation skills as central goal for the second training module: health coaching. Optimal care of PD should promote general health and wellbeing and care priorities should be defined together with PwPs and care partner [3]. Also, PwPs and care partner require a reference person that can be embodied by the PN through the empathic assessment of their care needs and the nurse's role as a care coordinator [3]. After the completion of this second training module, PN will have acquired the skills to assess personal care requirements of PwPs. The understanding of PD and health coaching skills merge, in line with the care priorities of home-based and community centered care, into a third and last module: delivering comprehensive tailored care. PwPs and care partner have to be navigated throughout the local healthcare system; multiple professions have to be incorporated in the care process and PwPs and care partner need motivation to use these resources. Consequently, we propose that PN should be trained to identify relevant local resources for PwPs and care partner, understand their living situation and motivate them to utilize available resources. Finally, a fourth module regarding available technologies can be added if applicable. This module will be discussed in greater detail in the following section.

**Table 4.** Conceptual framework for training Parkinson-Nurses to deliver a personalized care approach.


### **4. Discussion**

This paper proposes a framework for a novel PN training in the context of integrated care. There is a scientific consensus that PNs will take a significant and prominent role in integrated, patient-centered home-/and community-based care in the future [92]. The PN is widely considered to be an important primary point of contact for PwPs and care partner alike. PNs are also recognized to be very helpful in the role of a multidisciplinary care team coordinator [93]. When PNs are available to provide home-based care, it has been shown that patients' quality of life improves [54,94]. The importance of professional education can be identified in both theoretical and intervention-based models [55,65].

When it comes to educating PN, a variety of training pathways exist in the various countries. Also, the recognition of nurses as important care coordinators differs. As it has been stated elsewhere, funding mechanisms and the structure of healthcare systems play an important task for defining a nurse's role [95]. This is also reflected in different education programs. Therefore, it is necessary to address country specific requirements when implementing the framework. Also, the structure of healthcare systems affects the availability of resources, which is why a sound understanding of the overall context is essential for implementing the framework presented here. We emphasize that module 3 of the framework should be adjusted to the country-specific context. Further research may aim to further defining this module and adapting it to a country-specific context. For countries with extensive training opportunities and high resources, such as the United States [95], we suggest, that single modules of the proposed training framework could be implemented in the basic training of nurses as prerequisite for a later specialization in the field. This would enable nurse students to better understand PD and prepare them to be empowered nursing advocates for PwPs in inpatient and outpatient settings. For countries, where the profession of PN is less well developed, such as Germany [7,95] the framework may be fully implemented and also be utilized to build an agenda for future research on how the role of PN can be strengthened.

When implementing the framework into pratice, one might face challenges and barriers. In some countries, the PN has been an integral part of the multidisciplinary care team for a long time [96], while in others PN are not present in every care team [7,17]. Also, it is necessary to clarify funding issues for implementing the framework and hire staff, such as experienced PN, to deliver the framework. Additionally the lack in certification of such training could be another barrier [7]. However, the framework introduced here may represent an crucial step towards a universal consensus on certification.

Concerning the fourth module, the framework is deliberately kept open. Telemedicine represents an increasingly studied and apparently beneficial instrument for the provision of medical care to the chronically ill [29,97,98]. However, telemedicine must always be evaluated in the context of its application, i.e., the technical prerequisites for widespread use must also be accessible to the individual patients [99]. Therefore, telemedicine is not yet part of this framework, but we strongly encourage its future integration. Due to the emerging possibility of remote patient monitoring (i.e., smart glasses, smart beds or wearables [83,100]), we emphasize future research on up-to-date tech-based home-based care solutions and the future role a PN may hold in this scenario of increasingly techbased medical and social care delivery. This demand would also meet the need of care approaches to not only being responsive to specific care situations, but to incorporate proactive elements, such as the utilization of telemedicine [92,93].

For the future, the model being proposed here should configure a practical care concept that addresses effectively the identified care priorities for PD. One important aspect is the validation of the role of the PN and its training across cultures and societal contexts. Further research may focus on evaluating the implementation of the framework into a practical care concept and the development of a toolkit, which allows a flexible and streamlined adaptation of the training curriculum into different settings. Also, the model may be extended by reviewing care priorities for palliatve care.

### **5. Limitations**

This review holds potential limitations. The quality of evidence, which was included in the review was not assessed, since the purpose was to review existing concepts as widely as possible. Further, the curriculum has not been implemented or evaluated in practice, which is why no claims about its feasibility can be made. Rather, it should be understood as stimulating and inspiring source of information for developing future PN curricula. Finally, the framework does not include country-specific differences of PN, which may affect its applicability.

### **6. Conclusions**

A training framework for PN introduced here marks a pivotal contribution to increase the quality of care delivery for PwPs and their care partner following a care priority adapted approach. This framework is intended as an invitation to other researchers and practitioners to aid supporting the role of PNs and to move towards a standardized training. A shift towards a proactive role of a PN amongst healthcare providers is necessary and should be encouraged by legislation.

**Supplementary Materials:** The following are available online at https://www.mdpi.com/article/10 .3390/jpm11070623/s1, Table S1: Search Strategy and In- and Exclusion Criteria, Table S2: Overview of Theoretical Concepts.

**Author Contributions:** Conceptualization, M.v.M., J.S., F.T., D.C. and T.A.M.; methodology, M.v.M., J.S.; formal analysis, M.v.M. and J.S.; investigation, M.v.M. and J.S.; resources, M.v.M., J.S., F.T. and T.A.M.; writing—original draft preparation, M.v.M., J.S.; writing—review and editing, F.T., D.J.P. and T.A.M.; visualization, M.v.M.; supervision, T.A.M.; funding acquisition, T.A.M., D.C., D.J.P., A.A., M.F., J.J.F., D.G., E.R. contributed with professional expertise and provided critical revisions of the intellectual content. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by the Canadian Institutes of Health Research/EU Joint Programme—Neurodegenerative Disease Research, grant number 01789-000/HESOCARE-329-073.

**Conflicts of Interest:** M.v.M. declares no C.o.I. J.S. declares no C.o.I. F.T. declares no C.o.I. D.P. declares no C.o.I. A.A. has received compensation for consultancy and speaker related activities from UCB, Boehringer Ingelheim, General Electric, Britannia, AbbVie, Kyowa Kirin, Zambon, Bial, Neuroderm, Theravance Biopharma, Roche, Medscape; he receives research support from Bial, Lundbeck, Roche, Angelini Pharmaceuticals, Horizon 2020—Grant 825785, Horizon2020 Grant 101016902, Ministry of Education University and Research (MIUR) Grant ARS01\_01081, Cariparo Foundation. He serves as consultant for Boehringer–Ingelheim for legal cases on pathological gambling. D.C. declares no C.o.I. M.F. declares no C.o.I. J.J.F. has held consultancy functions with GlaxoSmithKline, Novartis, TEVA, Lundbeck, Solvay, Abbott, Abbvie, BIAL, Merck-Serono, Merz, Ipsen, Biogen, NeuroDerm, Zambon, Sunovion, Affiris, ONO; has received lecture fees from Biogen, BIAL, Sunovion, ONO, Zambon, Abbvie; has received grants from GlaxoSmithKline, Grunenthal, MSD, Allergan, Novartis, Fundação MSD (Portugal), Medtronic and Teva; has been employed by Faculdade de Medicina de Lisboa and CNS—Campus Neurológico. D.G. received honorarium for speaking and consulting from Sunovion, Paladin Labs Inc, Clinical trials funding from Canadian Institutes of Health Research, Genzyme Corporation/Sanofi Canada, Eli Lilly and Company and grants from Canadian Institutes of Health Research, Parkinson Canada, Brain Canada, Ontario Brain Institute, PSI Foundation, Parkinson Research Consortium, EU Joint Programme—Neurodegenerative Disease Research, uOBMRI E. R. has been employed by First Faculty of Medicine, Charles University and General University Hospital in Prague, Czechia; received research funding form Czech Health Research Council and Michael J Fox Foundation; has no other relationships that present a potential conflict of interest. T.M. has received personal compensation for serving as a Consultant for CHDI, Sunovion, Valeo Pharma, Roche, Biogen and nQ, received personal compensation serving on a Speakers Bureau for Abbvie, Valeo Pharma, and has received research support from the Canadian Institutes of Health Research, EU Joint Programme—Neurodegenerative Disease Research, the Ontario Research Fund, Michael J Fox Foundation, Parkinson Canada, uOBMRI/Parkinson Research Consortium, Parkinson Canada, Brain Canada, Ontario Brain Institute, and PSI Foundation.

### **References**


### *Article* **Individualized Health Care for Older Diabetes Patients from the Perspective of Health Professionals and Service Consumers**

**Birute Bartkeviciute \* , Vita Lesauskaite and Olga Riklikiene**

Faculty of Nursing, Lithuanian University of Health Sciences, LT 44307 Kaunas, Lithuania; vita.lesauskaite@lsmuni.lt (V.L.); olga.riklikiene@lsmuni.lt (O.R.)

**\*** Correspondence: birute.bartkeviciute@lsmuni.lt

**Abstract:** Background: Individualized nursing care as a form of person-centered care delivery is a well-known approach in the health care context and is accepted as best practice by organizations and professionals, yet its implementation in everyday practice creates serious challenges. The aim was to assess and compare the perceptions of health professionals and older diabetes patients on their individual care in regard to the patient's clinical situation, personal life situation, and decisional control. Methods: The quantitative study with a cross-sectional survey design was conducted from March 2019 until January 2021. The Individualized Care Scale was applied for the data collection. Health professionals (nurses and physicians, *n* = 70) and older diabetes patients (*n* = 145) participated in the study. The average duration of diabetes was 15.8 years (SD = 10.0) and type 2 diabetes was the most common (89.0%). The current glucose-lowering therapy for 51.0% of the patients was oral medications, 37.9% used injected insulin, and 11.1% were treated by combined therapy. Results: The highest-rated aspects of individualized care on both dimensions of the scale from the health professionals' perspective related to the clinical situation, and the scores for provision were significantly higher than those for support. The highest means of patients' ratings on the support dimension related to the clinical situation and the decisions over care sub-scale; for the care provision dimension, the highest individuality in care was assigned to the decisions over care sub-scale. The lowest ratings of individualized care, both in the health professionals' and patients' samples, related to the personal life situation sub-scale. Conclusions: Health professionals are more positive in regard to individualized care support and provisions for older diabetes patients than the patients themselves. Patient characteristics, such as the type of glucose-lowering therapy, education, and nutritional status, make a difference in patients' understanding and experience of individuality in care.

**Keywords:** individual care; nurses; older diabetes patients; physicians; support

### **1. Introduction**

Patient-centered care is a well-known and widely used approach in the health care context, as well as in education, management, and scientific investigations. The WHO global strategy on people-centered and integrated health services (2015) highlighted the importance of placing people and communities at the center of health services, which makes health services more comprehensive and responsive, more integrated, accessible, coordinated, safe, more focused on health needs and preferences, and more humane and holistic. Patient-centered care is understood as health services throughout the course of life that respond to the consumers' values and preferences, and are 'organized around the health needs and expectations of people rather than diseases' [1], p. 7.

A particular advantage of patient centralization in care, as mentioned by the WHO strategy, is an improved ability to respond to health care crises. Now, health care systems and societies, still guided by the global pandemic, have never been more clearly aware of the importance of patient-centered care for individuals' positive health outcomes and highquality and continuity of care. As it was stated in the WHO document, a well-organized

**Citation:** Bartkeviciute, B.; Lesauskaite, V.; Riklikiene, O. Individualized Health Care for Older Diabetes Patients from the Perspective of Health Professionals and Service Consumers. *J. Pers. Med.* **2021**, *11*, 608. https://doi.org/ 10.3390/jpm11070608

Academic Editor: Riitta Suhonen

Received: 29 May 2021 Accepted: 25 June 2021 Published: 27 June 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

health system that is 'able to adapt to the needs of the people it serves is not only better positioned to respond to emerging threats, but is also more resilient to tackling the myriad of chronic diseases which plague our populations' [1], p. 5.

Several studies and reviews addressed care individuality, a form of person-centered care delivery, for chronic disease patients. The evidence was created on preferences for decision-making among chronic neurodegenerative disease (Parkinson's) patients [2] and the benefits of nurse-led patient education for adults with heart failure [3,4]. Nurse-led case management was tested on adults with cancer [5] and other chronic illnesses [6]. The effectiveness of community-based case management among adults who abuse substances [7] and nurse-led primary health care coordination were investigated for patients with complex needs [8]. The results of these studies indicated multidisciplinary teamwork, the delivery of personalized, integrated, and coordinated care, patient education, and self-management skill improvement as suitable strategies in solving complex patients' health and social care needs in the primary health care of chronic illnesses, including diabetes mellitus.

The number of new diabetes cases has been increasing globally, with a projected increase to 26.6 million cases of incidence, 570.9 million cases of prevalence, and 1.59 million deaths in 2025 without effective interventions [9]. There were 109,162 diabetes mellitus cases (0.8% were children) in Lithuania in 2018, that is, 1 in every 28 men and 1 in every 23 women. Complications of the illness were prevalent in 80.5% of patients with type 1, and in 46.1% of type 2 diabetes patients; 528 patients die annually from this disease or its complications. In 2019, the number of patients with diabetes increased to 110,136 (396.3/1000 pop.); 6421 (2.3/1000 pop.) had type 1 diabetes and 104,659 (37.46/1000) were ill with type 2 diabetes [10].

Health care service for patients with diabetes, besides the physical, psychological, and social consequences, brings remarkable financial expenses, creating an economical burden for national health care systems. In 2011, estimates of global health care expenditures due to diabetes were USD 376 billion, and for the whole European region, it was USD 105 billion (10% of total health care expenditures; USD 2046 per person), with expectations for it to increase to USD 490 billion by 2030 [11]. A study conducted by Domeikiene et al. (2014) calculated the direct health care costs needed for patients with type 2 diabetes mellitus (non-complicated and complicated cases) in Lithuania. The results revealed that costs, adjusted for the average annual cost per person with diabetes, increased gradually with the number of complications from USD 814.73 (95% CI, 697.22–932.24) in patients without complications to USD 1926.64 (95% CI, 1275.66–2577.61) in patients with three or more complications [12].

There is evidence that patient-centered care positively relates to reduced pain and discomfort, faster physical and emotional recovery, improved outcomes and quality of life [5,13], enhanced respect for persons and autonomy [2], increased adherence to the care plan [14], reduced hospital readmissions [3,13], and decreased health care utilization [15]. Similar patient health and care issues are intrinsic to older diabetes patients.

Various care strategies were suggested to improve the care and quality of life for patients with diabetes. In nursing, traditional nursing theoretical frameworks with patient education strategies were utilized for improving the care and self-care behaviors of people with diabetes [16–19]. To improve care for diabetes patients, an order of the Health Ministry on the requirements for the provision of nursing services for patients with diabetes mellitus was issued in Lithuania. The order states the right for diabetes nurses to provide primary and continuous consultations, and perform foot and leg ulcer care for patients independently or with a team [20]. Patient education becomes an important part of diabetes nurse service, as it encourages behavior changes in people with diabetes, which, in turn, may improve their chances for diabetes control. The clinical trial on continual diabetes education confirmed that values and achievement of the type 2 diabetes mellitus control improved after face-to-face individualized education sessions for patients [21]. During individual and group education, general information is provided, trying to correspond to the basic needs of the patients, enabling them to be active participants and creating a

possibility to learn from the experiences of others. However, diabetes patients, particularly those of older age, are not always prepared to take an active role when discussing their care with health care professionals as they are lacking skills [22] or are not familiar with what their exact role in that discussion should be.

Even if the approach of patient-centered care is familiar to health care organizations and health professionals, the implementation of such care commonly creates challenges. The obstacles are related to the differences in the comprehension of the phenomenon, a necessary physical change of health facilities, a serious cultural shift of the paradigm in traditional care practices (e.g., a paternalistic approach vs a consumer-oriented approach to care), organizational initiatives, leadership capacities, and health care professionals' knowledge and skills [23,24]. To tackle the situation, it is important to analyze the providers' perspectives on the support and provision for individual care for patients. In addition, the consumers' feedback of their experiences in patient-centered care may be of great benefit for the improvement of the work at health care organizations [25].

To our knowledge, there is a lack of studies that explore older diabetes patients' perspectives on individualized care and compare the experiences of patients with those of health professionals (nurses and physicians). For the Republic of Lithuania and similar post-soviet states that began to transform the national health care system in the early 1990s by adopting the Western countries' principles of health service provision and modern nursing developments, the individualized approach to the care of older patients with chronic disease is a new practical reality where more evidence is needed. The results of this study highlight the need for more active involvement of older diabetes patients in care planning and provisions by communicating their preferences and making individual decisions. We also expect that increasing the data on Lithuanian nurses' perspectives on individualized care for diabetes patients will facilitate change by fostering the development of the independent role and expanding the competence of diabetes nurses in other countries where such specialty has not been introduced yet.

The aim of this study was to assess and compare the perceptions of health professionals and older diabetes patients on their individual care in regard to their patient clinical situation, personal life situation, and decisional control.

### **2. Materials and Methods**

### *2.1. Design and Setting*

A quantitative study with a cross-sectional survey design was conducted. The study was performed from March 2019 until January 2021.

The study was conducted at the primary health care institutions (*n* = 10) of the Kaunas region (i.e., the second largest city of Lithuania), where diabetes care for patients is provided by primary care physicians, physician endocrinologists, diabetes nurses, and general practice nurses. All institutions are funded by the national compulsory health insurance fund. Before the pandemic, questionnaires were distributed by the investigator when she met nurse managers at the study field, introduced the study, and asked for help in distributing and collecting the questionnaires to health professionals and patients. Patients, in most cases, picked up the questionnaire with a stamped envelope during their regular check-up, completed it at home, and returned it during the next visit or by mail. At the time of the pandemic and quarantine, health professionals were addressed through their work emails and were sent an e-questionnaire. The patients were not surveyed by e-mail.

### *2.2. Instruments*

For this study, 2 versions of the Individualized Care Scale (ICS) [26–29] were applied for the data collection. The Nurse Version (ICS–Nurse) was filled in by the nurses and physicians who take care of older diabetes patients, and the Patient Version (ICS–Patient) of the instrument was delivered to older patients with either type 1 or type 2 diabetes mellitus.

The Individualized Care Scale–Nurse Version (ICS–Nurse) is a bipartite questionnaire designed to explore nurses' views about individualized care in two dimensions (A-ICS–

Nurse and B-ICS–Nurse) [29]. The current version of the scale includes 17 (A) and 17 (B) items, for a total of 34. The A-ICS–Nurse is a 17-item 5-point Likert-type scale (1 = strongly disagree, 2 = disagree to some extent, 3 = neither agree nor disagree, 4 = agree to some extent, 5 = strongly agree) designed to explore nurses' views on how they support patient individuality through nursing activities in general. For example, the nurse is asked to rate the items 'I talk with patients about their fears and anxieties' or 'I help patients take part in decisions concerning their care'. The B-ICS–Nurse is also a 17-item 5-point Likert-type scale exploring the extent to which nurses perceive that the care they provide is individualized (e.g., 'I took into account their needs that require care and attention') [30,31]. Both scales consist of 3 sub-scales: (1) clinical situation (Clin A and B), (2) personal life situation (Pers A and B), and (3) decisional control over care (Dec A and B).

The Individualized Care Scale–Patient Version (ICS–Patient) is a 34-item self-reporting measure that was developed for the purposes of exploring patients' views on how patient individuality was supported through specific nursing activities (A-ICS–Patient) and the extent to which patients perceived their care as individualized (B-ICS–Patient) [27].

Both dimensions consist of 3 sub-scales eliciting information on the following: (1) patient characteristics in the clinical situation caused by hospitalization (or, for this study, a visit to an outpatient clinic) (Clin A and B), (2) the patient's personal life situation (Pers A and B), and (3) decisional control over care (Dec A and B). Both dimensions, that is, A and B-ICS–Patient, share the same structure in terms of their content. The questions are differently worded in that some A-ICS–Patient items ask the patients how nurses' activities have facilitated their individual existence in care, whereas some B-ICS–Patient items present the question as to how individual or individualized the care for the patients has been. The following response categories were used: 1 = fully disagree, 2 = disagree to some extent, 3 = neither disagree nor agree, 4 = agree to some extent, and 5 = fully agree. Higher scores indicated higher individuality in care from the patient perspective.

The ICS–Nurse and ICS–Patient versions have been previously translated and validated in various European countries with nurses of different specialties (e.g., general surgery, orthopedic surgery, maternity ward, geriatric, rehabilitation) and patients (e.g., patients from surgical, internal medicine, oncological, and gynecological wards) [28–33]. For this study, the Individualized Care Scale (ICS) was forward-translated into the Lithuanian language and back-translated into English following the methodological considerations for double translation and reconciliation [34].

To assess the psychometric properties, Cronbach's alpha was calculated for internal consistency for both scales (ICS-A and ICS-B) and 6 sub-scales of both instruments, for nurses and patients. In this study, 1 item from the sub-scales A and B (No. 17) that related to the patient's preference of washing time in a day was excluded from the Lithuanian version of the Individualized Care Scale (ICS) in the Nurse and Patient Versions, as it was not relevant for the primary health care service profile.

The 2 scales and 6 sub-scales of the Individualized Care Scale–Nurse Version (ICS– Nurse) had Cronbach's alpha (α) values ranging from 0.79 to 0.92; the Cronbach's alpha (α) for the Individualized Care Scale–Patient Version (ICS–Patient) ranged from 0.77 to 0.96, indicating appropriate (from satisfactory to excellent) internal consistency of the instrument for both samples (Table 1). When compared with the Dutch validation study, we observed that the internal consistency of the Lithuanian version of the ICS was weaker [33].


**Table 1.** Reliability statistics for the Lithuanian version of the Individualized Care Scale–Nurse Version (ICS–Nurse) and Patient Version (ICS–Patient).

The Individualized Care Scale–Nurse Version (ICS–Nurse) was used for health care professionals that provide care for older diabetes patients. Even if the ICS is primarily aimed at nurses' support and provision of individualized care, we used this scale for physicians as well. By not separating physician and nurse contributions to individualized care, we argue that nurses and physicians work as a team while providing care for older patients with diabetes. Thus, the team is responsible for finding the means to assure that their care plan implements each patient's preferences and enables him/her to actively participate in their care by making decisions about their own care. Moreover, the scale items appear to be generic (not specific to only nursing activities) and ask patients to respond about general features of an individual approach to care. It is also expected that the study results will help to detect the weakest points of patient-centered care implementation for the specific population of our study, that is, older diabetes patients, and will serve as a basis for further joint educational initiatives for both physicians and nurses.

The following background data about the nurses' and physicians' characteristics were requested from the participants: age, gender, education, occupation/job title (nurse/physician), and years of professional experience. In addition, the patients were asked to provide their age, gender, education level, height and weight, type of diabetes, most recent HbA1c, and duration of illness.

### *2.3. Participants*

Nurses and physicians (*n* = 126, response rate—96.9%), as well as older patients with diabetes (*n* = 145, response rate—72.5%), participated in the anonymous survey. The enrollment criteria for the study for nurses and physicians was the provision of care for older diabetes patients for more than one year. Every nurse and physician from the institutions involved in the study that suited the inclusion criteria were invited to participate in the study.

Among the health care professionals (N = 70), the majority were nurses (81.4%, 57) and the others were physicians (28.6%, 13). Regarding gender, all the respondents were female. The mean age of the respondents (nurses and physicians) was 48.57 ± 9.33 years (range of 24–65, median of 49.5 y.). More than half of the health care professionals (65.7%, 46) had completed higher education (university or college), and the others (34.3%, 24) had received a vocational education (nursing school with a diploma). The average duration of professional experience was 24.37 ± 10.96 years (range of 1–43); 34.3% worked in their professional practice for fewer than 20 years, and the others (65.7%, 46) for 20 years or more.

Patients were consecutively enrolled based on the following criteria: age of 65+, with a confirmed diagnosis of type 1 or type 2 diabetes mellitus, with more than 1 year of the disease's duration, having Lithuanian language reading and writing skills, and being able to comprehend the questions. Each older diabetes patient that visited a primary health care center or outpatient unit of the hospital during the study period (23 months in total) was invited to participate in the study. Those who declined to answer the questionnaire

explained being busy at the time, not being interested in the study, or having vision or Lithuanian language problems. The characteristics of the patient sample are presented in Table 2.


**Table 2.** Characteristics of the patient sample (N = 145).

### *2.4. Ethical Considerations*

Permission to conduct the study was obtained from the Kaunas Regional Biomedical Research Ethics Committee on 13 March 2019, No. BE-2-29.

### *2.5. Statistical Data Analysis*

The data were analyzed using the Statistical Package for Social Sciences (IBM SPSS Statistics) version 25.0. To assess the psychometric properties of the scale, Cronbach's alpha was calculated for the internal consistency of the individual items and the sub-scales; the internal consistency of α > 0.6 was considered to be acceptable [35].

The results were presented in percentages for the qualitative variables and the means with standard deviation (SD) were calculated for the quantitative variables. For the ICS, the higher the mean scores, the better patient individuality was supported (ICS-A–Nurse) and the higher the perceptions were of the maintenance of individuality in care (ICS-B–Nurse).

The nonparametric Kolmogorov–Smirnov normality test was used to test the normal distribution of the data. As normality was absent, the nonparametric Mann–Whitney U test was used to compare the distributions of the quantitative variables for the independent groups. The Wilcoxon signed-ranks test was applied to compare the results from the 2 ICS dimensions. The significance of the differences was defined by a *p*-value of <0.05.

### **3. Results**

At the sub-scale level, health professionals scored the perception of individual care provided to the patient (B-ICS–Clinical) (mean 4.17) and views on support to the patient (A-ICS–Clinical) (mean 4.13) at clinical situations as the highest. The lowest professionals' and patients' scores in both domains (support and provision) of individualized care were associated with the patient's personal life situation (Table 3). Accordingly, the highest means of patients' ratings of individualized care in the support dimension related to the clinical situation (mean of 3.55) and decisions related to care (mean of 5.54) sub-scales. For the care provision dimension, the highest individuality in care from the patients' perspective was related to the decisions over care domain (mean of 3.65). Moreover, the ratings of support for individualized care and such care provision were significantly higher for the health professionals than for the patients in each sub-scale of the ICS (Table 3).

**Table 3.** Health professionals' and patients' assessments of individualized care at the ICS dimension and sub-scale level.


At the ICS item level, significant differences between the health professionals' and patients' perspectives towards the support of individuality in care were determined for the majority of the items (Part A); the scores of the health professionals were higher than those of the patients (Table 4). In contrast, no differences were revealed in the answers about previous experiences of hospitalization and patients' participation in decision making.

Regarding the support scorings, the health professionals' and patients' perspectives on the provision of individual care for older patients also varied significantly; the professionals were more positive in their answers than the patients were (Table 5). The nurses and physicians thought similarly to the patients only in the cases of the patients' chance to take responsibility as far as possible and their knowledge preferences (what they want to know about illness/health condition).

A comparative analysis of ratings among health professionals revealed statistically significant differences between the two dimensions of the ICS, that is, the professionals' views on support to the patient through care activities and the professionals' perception of individual care provided to the patients. The differences were related to the personal life situation and the decisional control over care sub-scales; the health professionals' ratings of provision were significantly higher than those for support (*p* = 0.046 and *p* = 0.037, respectively, based on the Wilcoxon test).

Within the health professionals' sample, there were no differences in the scores (neither at the dimension nor at the sub-scale level) of individualized care between physicians and nurses. The sociodemographic characteristics in the total sample of health professionals did not make any differences for individualized care scores as well.

As all the physicians (N = 13) had a higher university education, we separately analyzed the nurses' (N = 57) ratings on the ICS sub-scales in relation to their education.

Nurses who take care of older diabetes patients and who have had vocational education scored support for individual care (Part A) with significantly higher scores than nurses with a college education (the means were 4.11 and 3.68, *p* = 0.039, respectively,). In addition, it was observed that the tendency for nurses with a university education rated provision (Part B) higher than nurses with a college education; the means were 4.16 and 3.66, *p* = 0.052, respectively.

Several factors made a difference in the perception of individual care in older patients with diabetes. The highest differences in diabetes patients' assessments of individualized care dimensions and sub-scales were observed in relation to the current type of glucose-lowering therapy. Patients with combined therapy rated each sub-scale of the provision dimension and particular sub-scales of the support dimension of individual care significantly higher than those with oral or injectable medications (Table 6).


**Table 4.** Health professionals' and patients' assessments of the support of patient individuality: item-level analysis.


**Table 5.** Health professionals and patients' assessments of the provision of individualized care: item-level analysis.

In addition, patients with lower than a degree education level rated the support dimension (Part A) higher than those with a college or university education; the means were 3.60 and 3.12, *p* = 0.032, respectively.

Body mass index (BMI) was also a variable that resulted in variations in the patients' perceptions of support for individual care. Older diabetes patients with a BMI of <30 rated the support dimension significantly lower than patients with a BMI of ≥30; the means for Part A of the ICS were 3.34 and 3.68 respectively (*p* = 0.032).

Moreover, a tendency was observed in relation to the patients' ages and their opinions on individual care; patients of 71 years and over rated the support for their personal life situation (A-ICS–Personal) higher than those who were 70 years old or below (*p* = 0.054).


**Table 6.** Patients' assessments of individualized care at the ICS dimension and sub-scale levels in relation to the current type of glucose-lowering therapy.

\* Mann–Whitney U test; 1—tablets (*n* = 74), 2—insulin injections (*n* = 55), 3—combined (*n* = 16).

### **4. Discussion**

A patient-centered approach to care sees individuals as active recipients of health care provision. Patients are expected to collaborate with medical professionals, discuss their clinical and life situations, and make decisions related to their care plan. Health professionals (nurses and physicians) taking care of older diabetes patients in the Lithuanian primary health care organization had an opinion that they support patient individuality, in general, and provide care that takes into account the particular patient's situation. The highest scores from the professionals' perspective were for the support and provision of individual care in regard to the clinical situation of the patient. These results generally correspond to the comparative cross-cultural study on individualized nursing care in seven countries [31]. Very similar nurses' positive perceptions of individualized care, especially for the clinical situation and patients' decisional control over care, were also found by Finnish researchers [36].

Notably, patients in our study rated the support for individual care higher than patients from internal medicine and surgical units of teaching hospitals in Turkey, although the results of both studies correspond in regard to the patients' ratings of the personal life situation aspect of the support dimension, where the mean was the lowest [32]. Similar to a study on orthopedic and trauma patients [37], the personal life preferences of the patient were also at least discussed during care provision for the Lithuanian older diabetes patients from both patients' and health professionals' points of view.

In all cases, the ratings of support for individualized care and such care provision through care activities were significantly higher for the health professionals than for the patients. An international study among five European countries revealed similar differences in patients' and nurses' assessments of individualized nursing, where nurses, compared with patients, assessed that they supported patient individuality more often [30]. In Lithuania, the data about chronically ill patients' preferences and readiness for active participation in care and in decision-making, particularly, is scarce and creates difficulties for a valid interpretation of the current results. The arguments for a lower rating of individual care support and provision in the patient sample might be twofold: either they wish but lack actual possibilities to participate, discuss, and make decisions, or their understanding and knowledge about such possibilities is incomplete and they are not even motivated to be an active participant in their care. Such an interpretation is consistent with the findings of du Pon et al. (2019), in which patients with diabetes were found to have limited necessary skills to be adequately prepared for a consultation and achieve an active role [22]. In prior research on the preferences and participation in decision-making among patients with Parkinson's disease, the authors suggest that in some contexts or situations, patients prefer less autonomy in medical decision-making and choose shared decisions, or

even find it acceptable to be excluded from decision-making as their illness worsens. Some patients preferred to make the final decision, some wanted the decision-making process to be evenly shared, while others preferred to delegate final decisions to the doctor [2]. Further research applying a rigorous quantitative and qualitative design to larger populations of diabetes patients is recommended. Future work should also address how different groups of patients understand and prefer individuality in care, and how this care is linked with other relevant factors.

The ratings of individual care for the ICS dimensions and sub-scales did not vary among health professionals in regard to their qualification, that is, being a nurse or physician. Although, education level made a difference in how nurses comprehend and practice their individual approach in the care of older diabetes patients, as the nurses with a vocational education were more positive and rated higher individual care proposed and provided for the older diabetes patients than the college degree nurses. These results are in contrast with those of Suhonen et al., (2009) who found that higher scores supporting the delivery of individualized care could have been expected from nurses with higher education [38]. Such results may be explained by the differences that were introduced in the nursing curriculum in the last decade, when nursing education was elevated from a diploma to a college or university-based system. As a condition for membership in the European Union (EU), nursing programs were harmonized with the EU requirements, which caused remarkable transitions of nursing education from a strongly biomedical, technical approach toward a more sensitive, patient-centered, holistic approach to care [39]. We propose that higher educated nurses are well equipped with the knowledge of modern nursing and have a clearer vision of what care should be in relation to safeguarding the patient's individuality. This is the reason they are more critical in assessing the current situation, which is lacking a full integration of the patient-centered approach in older diabetes patient care practice.

Our results revealed that patients with combined glucose-lowering therapy rated some aspects of support and all the aspects of the provision of individuality in their care higher than those patients who were treated by oral or injectable medications. We propose that a complex type of treatment requires the physicians and nurses to give more attention to an individual patient0 s case through collecting health information, assessing health status, instructing, and educating. In addition, the integration and monitoring of patient-reported outcomes facilitates holistic interdisciplinary care and takes into account patient-relevant endpoints [40]. Such a relatively prolonged communication and going into the situation creates for the patient an impression of greater consideration for his or her particular case. A similar interpretation might be true in regard to the body mass index, as diabetes patients with a BMI of ≥30 had more positive opinions about individual care support than those patients with a lower BMI.

Patients' perceptions of individualized nursing care are related to their education level. In our study, older diabetes patients with a lower than degree education level rated the support dimension (Part A) higher than those with a college or university education. Other researchers similarly reported that a lower educational level is associated with a perception of more individualized care in patients [36,41].

The findings of this study provide the initial evidence of the perception and provision of the individualized care approach to the care of older diabetes patients. For improvements in clinical practice and fostering the actual implementation of a patient-centered approach of care, complex means would be the most effective for unifying professional, organizational, and policy development. The research showed that older patients' perceptions of individuality in care were associated with the care environment, especially a patient-centered care climate [42]. In order to be responsible in personal care decisions and adhere to health recommendations (e.g., medications, nutrition, and physical activity), patients require adequate 'education and support they need to make decisions and participate in their own care' [1], p. 7. It might be assumed that continuous patient–provider communication, regular contact, and careful consideration of individual values, knowl-

edge, habits, and behaviors motivate and empower older and chronically ill patients to change. Further continuing education of physicians and nurses, joining them in one class and with the same teaching content, would help to expand their unified understanding of patient-centered care components, principles, and practical implementation in caring for older diabetes patients.

This study was one of the first attempts to study individual patient care in our country. For further research, physicians' and nurses' work environment characteristics that can also affect the provision of individualized have to be considered [43]. There are more factors of the professional practice environment found that correlate with the nurses' perceptions about the support of individuality and their views on the individual care provided [44]. This means that for a real shift toward an individual approach to care, health care institutions need to expand their philosophy of service to support the new roles of care providers and consumers at an organizational level.

This study has several limitations. Firstly, the Individualized Care Scale–Nurse Version (ICS–Nurse) was initially developed and validated to assess nurses' points of view about individual care support and the provision of such care through nursing activities, particularly. The evidence for the validation of this scale among other health care professionals is lacking and should be separately addressed in further studies. Secondly, the construct of the scale (a bipartite structure with a rather similar wording of items for both dimensions) may influence the clear comprehension and accuracy of the responses when applying it to older persons with chronic illnesses. Specific considerations would be important during the selection of an appropriate data collection method (e.g., a structural face-to-face interview instead of a survey). Thirdly, the sample size of patients was small and has a limited representation of only the institutions involved in the study. The study is lacking generalizability across settings and countries; wider studies are recommended for the future, including older diabetes patients with experiences of inpatient settings as well. Finally, half of the data collection was conducted during the pandemic period when a rather large extent of routine health care services for chronically ill patients were suspended or provided by different means (e.g., phone calls). This fact should be taken into consideration when interpreting and comparing the results of this study with any other sources.

### **5. Conclusions**

Health professionals have a more positive perception in regard to individualized care support and provision for older diabetes patients than the patients themselves. Individual personal life preferences of the patient are at least discussed during care provisions for the older diabetes patients from both health professionals' and patients0 points of view. Patient characteristics, such as the type of glucose-lowering therapy, education, and body mass index, make a difference for older diabetes patients in their understanding and experience of individuality in care.

A change needs to be made to provide better individualized care for older diabetes patients, and the next steps would be to interview patients to see how the care can be improved and what will motivate patients to be more active in their care planning and implementation. Careful consideration of individual patients' values, knowledge, habits, and behaviors would assist and assure that their personal life situation is taken into account during care processes.

**Author Contributions:** Conceptualization, B.B., V.L. and O.R.; methodology, B.B. and O.R.; software, B.B.; formal analysis, B.B.; investigation, B.B.; data curation, B.B.; writing—original draft preparation, B.B.; writing—review and editing, V.L. and O.R.; visualization, B.B.; supervision, V.L. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Kaunas Regional Biomedical Research Ethics Committee on 13 March 2019, No. BE-2-29.

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Acknowledgments:** The authors acknowledge Patti Hamilton, Texas Woman's University for her valuable critical comments on the manuscript and her help with English language editing.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


### *Article* **Validation of the Patient-Centred Care Competency Scale Instrument for Finnish Nurses**

**Riitta Suhonen 1,2,3,\* , Katja Lahtinen 1,4, Minna Stolt <sup>1</sup> , Miko Pasanen <sup>1</sup> and Terhi Lemetti 1,5**


**Abstract:** Patient-centredness in care is a core healthcare value and an effective healthcare delivery design requiring specific nurse competences. The aim of this study was to assess (1) the reliability, validity, and sensitivity of the Finnish version of the Patient-centred Care Competency (PCC) scale and (2) Finnish nurses' self-assessed level of patient-centred care competency. The PCC was translated to Finnish (PCC-Fin) before data collection and analyses: descriptive statistics; Cronbach's alpha coefficients; item analysis; exploratory and confirmatory factor analyses; inter-scale correlational analysis; and sensitivity. Cronbach's alpha coefficients were acceptable, high for the total scale, and satisfactory for the four sub-scales. Item analysis supported the internal homogeneity of the itemsto-total and inter-items within the sub-scales. Explorative factor analysis suggested a three-factor solution, but the confirmatory factor analysis confirmed the four-factor structure (Tucker–Lewis index (TLI) 0.92, goodness-of-fit index (GFI) 0.99, root mean square error of approximation (RMSEA) 0.065, standardized root mean square residual (SRMR) 0.045) with 61.2% explained variance. Analysis of the secondary data detected no differences in nurses' self-evaluations of contextual competence, so the inter-scale correlations were high. The PCC-Fin was found to be a reliable and valid instrument for the measurement of nurses' patient-centred care competence. Rasch model analysis would provide some further information about the item level functioning within the instrument.

**Keywords:** patient-centred care; competence; assessment; instrument; measurement; validity; reliability

### **1. Introduction**

Patient-centeredness in care has been reported to be a core health care value [1,2], and the optimal design for the delivery of healthcare [3,4] requiring specific competences from healthcare professionals [5,6]. Patient-centred care has also been found to be a healthcare core competency [7]. This core competency describes the professionals' ability to identify patient expectations, preferences, and values, facilitating joint decision making, and acting with individual patients to deliver safe, effective, and compassionate care [8]. Patientcentred care is, therefore, a care approach which considers individual patient's specific care needs [4,9,10] and is regarded as patients' preferred care delivery process [11,12]. Importantly, patient-centeredness in care has been used as an attribute and indicator of quality [2,13] and patient safety [6], especially in the interaction between the patient and care provider [14].

The concept of patient-centred care is multidimensional, and includes domains at the individual, human level and at organizational levels [2,4,15–17]. The concepts of patientcentred care and person-centred care have been used interchangeably in the literature,

**Citation:** Suhonen, R.; Lahtinen, K.; Stolt, M.; Pasanen, M.; Lemetti, T. Validation of the Patient-Centred Care Competency Scale Instrument for Finnish Nurses. *J. Pers. Med.* **2021**, *11*, 583. https://doi.org/10.3390/ jpm11060583

Academic Editor: Chun-Jen Huang

Received: 10 May 2021 Accepted: 17 June 2021 Published: 21 June 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

e.g., [18], and defined in many ways. However, regardless of the particular title, the concepts include very similar core elements, with elements specific to professional groups in healthcare. Scholl and colleagues [18] (p. 1), in their model of patient-centredness in professionals and healthcare, identified 15 dimensions: "essential characteristics of the clinician; the clinician-patient relationship; clinician-patient communication; the patient as a unique person; the biopsychosocial perspective; patient information; patient involvement in care; involvement of family and friends; patient empowerment; physical support; emotional support; the integration of medical and non-medical care; teamwork and teambuilding; access to care; and the coordination and continuity of care".

The difference between the concepts may be the intent of the focus on or viewpoint to ill-health issues or patient as a person, or the balance on these. However, the approach, typical in nursing is bringing the person to the centre of care, seeing the individual, trying to maintain their personhood, and valuing their personal experiences of life in relations with others in their social environment [19,20].

Competence has typically been defined in terms of "complex combinations of knowledge, skills, performance, attitudes and values" [20,21]. However, there seems to be no consensus about the meaning of these terms within the nursing profession [21–23]. Demonstrating this complexity further, both subjective (self-assessment) and objective (knowledge test and simulations) evaluations of competence have been used to assess competence. This complexity and lack of consensus is not surprising as assessing competence is many-sided, and rarely comprehensive [24].

Competence has been assessed and measured as a behavioural objective, within a psychological construct which includes decision-making and justifications for actions. In these assessments the self-assessing individuals justify their preferences and activities against defined, predetermined criteria. Measuring competence using self-assessment and standard instruments in this behavioural context has been criticized as reductionism, simplifying the assessed issues, dividing the complex processes of healthcare activities into single tasks, or sets of tasks, activities, and targets [24]. Helpfully, competence has also been divided into professional competence [25,26] and clinical competence, e.g., [27,28]. In a similarly helpful way, patient-centred care has also been separated into care competence needed by all professionals and specific competence, being context specific [29] and possibly varying between individual professionals [26]. As with general competence, the patientcentered care competence has been found to be multidimensional and can be conceptualised and operationalised in multiple ways [6].

Although the concept of patient-centred care has been used for many years and is considered widely to be fundamental for individualised healthcare [30,31], the competence requirements for such care provision remain largely undefined. Although empirical studies about patient-centred care competence are limited [6] these studies have pointed out the clear need for a special competence required for the provision of patient-centred care [5,6]. It follows that the assessment of patient-centred care competence forms the basis of support for the development and enhancement of patient-centred clinical care provision by nurses for patients [6]. The Patient-centred Care Competency (PCC) instrument was developed for measuring professional nurses' competence in the delivery of patient-centred care in hospitals [6]. Within the PCC instrument, patient-centred care competence is defined in terms of knowledge, skills, and attitudes [6] (p. 45) and applies components from the Quality and Safety Education for Nurses (QSEN) faculty study [32]. The QSEN study [32] included the following components of competence for nurses: patient-centred care, advance event management, contributions to patient safety culture, effective communication, optimisation of human and environmental factors, risk management, and teamwork. The results of this study and the work of Hwang [6], formulating the PCC instrument, suggests that assessment could be based around the use of core competencies for nursing professionals including patient-centred care, as defined in terms of earlier literature, e.g., [11,19,33–36]. Thus, the PCC instrument includes assessment of the knowledge, skills and attitudes

required in terms of respecting patients' perspectives; promoting patient involvement in care processes; providing for patient comfort; and advocating for patients [6].

The aim of this current study was to assess (1) the reliability, validity, and sensitivity of the Finnish version of the PCC scale and (2) the self-assessed level of patient-centred care competency in two samples of Finnish nurses.

### **2. Materials and Methods**

### *2.1. Design, Setting and Sampling*

The assessment of the PCC uses the data from two earlier studies as secondary data where the PCC was used. These two studies employed cross-sectional survey designs and used the PCC instrument [6] (with permission from Hwang, also from Elsevier) as part of them. These separate datasets, labelled Dataset 1 and Dataset 2, were used to analyse the psychometric properties of the PCC, not fully reported previously.

Dataset 1 was collected electronically, between October 2016 and January 2017, from registered nurses working in one major university hospital in Southern Finland using self-administered questionnaires. Digitally delivered questionnaires were used in one organisation, with the assistance of the member of the organisation. Nurses were recruited with the help of nurse managers, who emailed the information letter and a link to the survey to potential participants. Inclusion criteria for participation were that respondents would: (1) be a registered nurse (RN) and (2) work in an acute hospital in-patient unit that cares for older patients. The researcher, together with the nurse managers, identified the units where older people form most of the patients cared for in the unit, including internal medicine units. In total 770 invitations were sent to a convenience sample of RNs working in 14 in-patient units, 223 nurses responded giving the response rate of 29%. The respondents' mean age was 38.9 (standard deviation (SD) 11.6, range 23–64) and most of the respondents were female (n = 206). The highest level of nurse education was registered nurse (college or baccalaureate, n = 210). A few of the respondents had a master's degree in nursing (n = 4) or had taken postgraduate classes in nursing (n = 9). The mean length of the work experience in the nurses' current employment was 7.6 years (SD 7.3, range 0.1–35).

Dataset 2 was collected in written form, between October 2017 and June 2018 from nurses working in a University hospital and in primary health care units in Southern Finland. Paper-pencil format was the only useful technique as many organisations participated and access to study sites was demanding due to many participating organisations. A cluster sampling approach was used to recruit nurses from one university hospital (hospital) and two major cities (primary health care) offering care for older people in Finland. Respondents were informed about the study verbally and in writing. If the respondents were interested in participating in the study, they completed the paper questionnaire by hand, sealed it in an envelope and sent it to the researcher by mail. A total of 1435 questionnaires were delivered to potential respondents from 41 units in the university hospital and 19 units in primary health care: health centres: (n = 13); long-term care units (n = 2); home care (n = 2); and city hospitals (n = 2).

A total of 443 completed questionnaires (response rate 30.9%) were returned by hospital nurses (n = 240) and primary health care nurses (n = 203). The respondents mean age was 43.2 (SD 11.2, range 22–67) and most of the respondents were female (n = 426). The highest level of nurse education was that of Registered Nurse (college or polytechnic, n = 385). However, some of respondents' highest level of nurse education was master of healthcare (polytechnic, n = 14), bachelor of healthcare (university, n = 19) or Master of healthcare (university, n = 14). The mean length of the work experience in their current unit was for nurses working in the university hospital, 8.6 years (SD 9.0, range 0.6–37.2) and for nurses working in primary health care, 6.2 (SD 6.3, range 0.8–32.0).

### *2.2. Instrument*

The PCC scale [6] was used in both Finnish studies. The PCC was originally developed in Korea for the measurement of patient-centred competence of nurses in hospital settings. The competence was defined in terms of knowledge, skills and attitudes related to patient-centred care. The PCC consists of four sub-scales including Respecting patients' perspectives (6 items), Promoting patient involvement in care processes (5 items), Providing for patient comfort (3 items) and Advocating for patients (3 items). The instrument uses a five-point Likert scale (1 minimal, 2 below average, 3 average, 4 good, 5 excellent) which the respondents used to rate their competencies. (subjective, self-assessment).

The 41 PCC items were developed, based on earlier literature and the QSEN faculty framework of competence in patient-centred care [32]. The items were then analyzed by experts who reduced the preliminary 41 items, to 25 after using the Content Validity Index (CVI) and cut off criterion of 0.70, and psychometric testing [6]. The expert panel members were eight members of the board of directors (Korean Quality Improvement Nurses Society) and three nursing professors, and they assessed the relevance of the proposed 41 items. The first version of the PCC was pretested in the sample of two head nurses and two registered nurses to verify the comprehensibility and clarity of the items. The PCC was then tested with a sample of 577 hospital nurses. Explorative factor analysis supported a four-factor solution explaining 64.7% of the variance and suggesting the final 17 items for the PCC [6]. The overall Cronbach's alpha coefficients for the 17-item instrument was 0.92, and for the sub-scales, 0.80–0.85. Concurrent validity was assessed using the single item on patient-centred care performance using VAS (0–100), with Pearson's correlation coefficient of 0.60 (*p* < 0.001).

### *2.3. Translation of the Instrument*

The PCC with 17 items created by Hwang [6] was used, and the English language items were used. A standard forward-back translation method [37] was used to translate the PCC from the English version to the Finnish version by an official translator, whose work was analysed by two researchers, mainly interested in ensuring nursing terminology was well matched. Secondly, the translated version was back-translated into English by another official translator. Thirdly, the back translated version was compared with the original English language instrument. Finally, all three instrument versions were analysed at the same time by two experienced researchers. The final Finnish version included some minor changes of terms (professional terminology and most suitable term from two suggested) and the deletion of some redundant words. As languages differ from each other, the semantic, cultural, conceptual equivalence, and linguistic terminology were ensured [37].

### *2.4. Data Analysis*

Data were analysed statistically using the SPSS for Windows (IBM SPSS, Chicago, IL, USA) version 22.0/24.0 and lavaan (0.6–7) package from R (version 4.0.2) statistical software. Firstly, descriptive statistics were calculated which described the two samples and study variables at the total scale and sum-variable level for the four sub-scales. The sumvariables were formed based on the theoretical background of the original instrument, see [6]. Secondly, the internal consistency reliability was examined using the Cronbach's alpha coefficients and item analysis in both data sets (criterion ≥ 0.70) [38,39]. Item analysis included item-to-total correlations (criterion ≥ 0.30) and the percentage of the appropriate inter-item correlations (criterion 0.30 ≤ r ≤ 0.70). Thirdly, an explorative factor analysis (EFA) was conducted in the sample of 233 respondents (Dataset I). The Kaiser–Meyer–Olkin measure of sampling adequacy was 0.895, (acceptable value > 0.5) [40] and Bartlett's test of sphericity (<0.001; where a *p* value less than 0.05 indicates that a factor analysis may be useful with the data) [41]. These two measures were used to assess the preconditions for factor analysis. An EFA, with principal axis factoring as the extraction method, and Promax with Kaiser Normalization for rotation method was computed. Fourthly, a confirmatory

factor analysis (CFA) with maximum likelihood estimation was used to investigate the conceptualised four-dimensional structure (KMO = 0.92, Bartlett's test < 0.001). Several indices with criteria were used to examine the goodness-of-fit of the model with Dataset 2: goodness-of-fit index (GFI); adjusted goodness-of-fit index (AGFI); Tucker–Lewis index (TLI) and the comparative fit index (CFI) (criterion >0.90 threshold for all mentioned fit indices [42,43], root mean square error of approximation (RMSEA <0.08) [42], and standardized root mean square residual (SRMR <0.08) [42]. Fifthly, to examine whether the PCC sub-scales measure distinct dimensions, inter-scale correlations between the PCC sub-scales were analysed. Finally, analysis of the sensitivity of the PCC was assessed comparing the PCC total and sub-scale scores within the two different facilities (contrasting groups), university hospital care (n = 233) and primary health care (n = 201) in Dataset 2 (n = 434). The distributions were non-normal and therefore, the Mann–Whitney U-test was used.

### *2.5. Ethical Considerations*

Permissions for data collection were obtained from the participating organisations according to their specific ethical procedures. The studies using Dataset 1 and Dataset 2 were approved by the Ethics Committee of the University (34/2016/6 June 2016 and 4/2016/15 February 2016 respectively). Permission to use the PCC instrument was granted by the developer Jee-In Hwang (email) and Elsevier (reprint of the items). The respondents gave their voluntary informed consent for the studies by completing the questionnaires sent to them and posting them to the researcher, after having all information about the study in an introductory letter. Respondents were informed that they could withdraw from the study at any time.

### **3. Results**

### *3.1. Descriptive Statistics on the Patient-Centred Care Competency (PCC) and Sub-Scales*

In total, patient-centred care competence in Dataset I was rated in the 'good', level 4.04 (SD 0.46) and was higher compared to Dataset 2 (3.90, SD 0.42). At the sub-scale level (dataset 2 in parenthesis), competence providing for patient comfort was evaluated the highest in both data sets 4.31, SD 0.56 (4.13, SD 0.55) at the 'good' level. Competence in respecting patients' perspectives 4.12 SD 0.49 (3.99, SD 0.42) and advocating for patients 4.03 SD 0.56 (3.84, SD 0.56) was also rated 'good'. Competence promoting patient involvement in care processes was assessed the lowest at 3.78 SD 0.56 (3.70, SD 0.49).

### *3.2. Psychometric Properties of the PCC*

### 3.2.1. Internal Consistency Reliability

The internal consistency measured using Cronbach's alpha coefficients (Dataset 2 in parenthesis) was α = 0.93 (0.91) for the total scale and ranged from α = 0.78 (0.74) to α = 0.85 (0.83) for the sub-scales (Table 1). Item analysis (Dataset I) provided some evidence about the internal consistency of the items within the total scale and its four sub-scales. All items were closely tied to its construct as all item-to-total correlations reached an acceptable level (≥0.40). Correlations between the items in the given sub-scale (inter-item correlations) were acceptable in three sub-scales (PCC2–4), as was 87% of the inter-item correlations within the PCC total and the sub-scale PCC1 (Table 1).


**Table 1.** Descriptive statistics of the Patient-centred Care Competency (PCC) total and sub-scales, Cronbach's alpha and item analysis.

\* α Cronbach's alpha coefficient. § item to total correlation r > 0.3. # inter item correlation 0.30 < r < 0.70.

### 3.2.2. Construct Validity

Firstly, the exploratory factor analysis of Dataset I suggested a three-factor solution based on scree plot and eigen values (criterion eigen value ≥ 1). The Pattern matrix showed a clear structure for three sub-scales (Factors 3, 2 and 1) which explained 57.7% of the variance. However, the fourth sub-scale was not independent as the items loaded on the first sub-scale (Factor 1, item 15) and the third sub-scale (Factor 3, item 16 and item 17). A four-factor model was also examined, with a 61.2% explained variance, and an eigen value range of 8.04–0.87, and a last factor with an eigen value of less than 1.0. (Table 2).




**Table 2.** *Cont*.

Extraction Method: principal axis factoring; Rotation method: Promax with Kaiser normalization. Bold: representing original structure. Items reprinted from *Nursing Outlook* 55(1), Cronenwett et al. Quality and safety education for nurses 122–131, Table 1. Copyright (2007), with permission from Elsevier.

> Secondly, a Confirmatory Factor Analysis was conducted using the Dataset 2 (n = 421 valid cases). The Chi-square test did not show a model fit (χ <sup>2</sup> = 283.70, df = 113, *p* < 0.01) possibly due to the large sample size. Other goodness-of-fit indices were as follows: CFI 0.93, TLI 0.92, GFI 0.99 and adjusted AGFI 0.99, all at an acceptable level (criterion >0.90). The RMSEA was 0.065 (criterion <0.08) and the SRMR of 0.045 (criterion <0.08) was also a good fit to the model. The Item loadings ranged were: PCC1 (0.584–0.729), PCC2 (0.612– 0.681), PCC3 (0.726–0.824) and PCC4 (0.699–0.707), all of which were acceptable (criterion >0.40) (Figure 1).

**Figure 1.** Construct validity of the Patient-centred Care (PCC) instrument based on confirmatory factor analysis (CFA) and inter-scale correlations PCC1–PCC4. q refers to items, numbers refer to factor loadings within each sub-scale. Model fit statistics: comparative fit index (CFI) 0.93, Tucker– Lewis index (TLI) 0.92, goodness-of-fit index (GFI) 0.99, adjusted goodness-of-fit index (AGFI) 0.99, root mean square error of approximation (RMSEA) 0.065, standardized root mean square residual (SRMR) 0.045.

The average variance extracted (AVE), the amount of variance captured by a construct in relation to the amount of variance due to measurement error) [44] was 0.44 (PCC1), 0.41 (PCC2), 0.49 (PCC3) and 0.47 (PCC4) implying that the discriminant validity may not be ideal but includes variance based on measurement bias. However, the factor loadings were as follows, PCC1 (0.584–0.729, composite reliability (CR) 0.82), PCC2 (0.612–0.681, CR 0.77), PCC3 (0.726–0.824, CR 0.83) and PCC4 (0.699–0.707, 0.82), some being lower than 0.70.

### 3.2.3. Inter Scale Correlations

The correlations between the PCC sub-scales ranged from 0.57 to 0.88 showing the scales are related to each other and to the latent variable, PSS (Figure 1).

### *3.3. Sensitivity to Context/Contrasting Groups*

The competence assessments by nurses working in specialised hospital care and those working in primary health care were not statistically significantly different in the total scale or any of the sub-scales (total PCC, Mann–Whitney U =20,804, *p* = 0.659), PCC1 (U = 22,484, *p* = 0.628), PCC2 (U = 21,763, *p* = 0.519), PCC3 (U = 23,620, *p* = 0.745) or PCC4 (U = 20,110, *p* = 0.980).

### **4. Discussion**

Two datasets (1 and 2) were used to validate the PCC instrument in the Finnish healthcare context. The psychometric properties computed suggest acceptable reliability, content and construct validity and sensitivity. The PCC was developed and tested in the hospital environment in Korea by Hwang [6] to measure patient-centred care competency, and the findings in this current study are similar to those of Hwang [6]. The purpose of the PCC instrument is clearly defined, has meaningful content in the Finnish context and has acceptable internal consistency, face validity and construct validity [45]. These results demonstrate that the instrument is a useful measure of patient-centred care competency. In the Finnish studies the nurses assessed their overall patient-centred care competency higher 4.04 (Dataset I), 3.90 (Dataset 2) compared to the Korean studies, 3.58 [6] and 3.61 [46] respectively. The sub-scale "providing for patient comfort" was assessed the highest and the sub-scale "promoting patient involvement" was assessed the lowest in all four studies, increasing the inter-rater reliability of the instrument.

This current study also shows that the instrument is suitable for use in different health care environments, for example, home care and long-term care units (Dataset 2) as the findings are comparable between Dataset I and Dataset 2. However, because the data from home care and long-term care units, Dataset 2, is limited, and the staffing profiles differ from those in hospital environments, more research is needed to be more certain of this.

The sub-scales contain items related to general patient relations, patient involvement, safety, and teamwork [6,46] which are shared goals of all health care workers, for example clinicians and practical nurses. Therefore, it can be argued that although the instrument was originally developed for use in nursing studies, it could be used, with minor adaptations, to measure the patient-centred care competency of other healthcare workers such as physiotherapists and public health nurses.

Translating instruments for nursing studies is necessary [47] for researchers to have access to the many valid and reliable instruments available [37]. The standard forward-back translation method [37] for the Finnish version of the PCC achieved equivalence [47] with the original English and also Korean version. The Likert-type response options of the PCC are sensitive, and the instrument is comprehensible to the healthcare respondents as it suits their demographic and educational backgrounds [48]. The PCC is easy to complete taking a short time only, making it a useful research tool [48]. However, more research is needed to further validate the instrument, for example in diverse healthcare environments and among different professionals working in health care.

Patient-centred care competence is a multidimensional concept which can be defined and measured from different perspectives and multiple ways. This study provides more

information about the validation of one instrument, the PCC instrument [6], used for measuring nurses' patient-centred care competence. The results of this study suggest that the PCC instrument is a valid, reliable, and sensitive instrument that could be used to measure Finnish nurses' patient-centred care competence and may be adapted to measure the patient-centred competence of other health care workers. Cowan et al. [24] suggests that the self-assessed instrument oversimplifies a complex process, applying also to PCC. However, this instrument provides important information about nurses' own views of their patient-centred care competence. Combining this information with other measurements, for example, peer, co-workers' and patients' perspectives, can provide a more comprehensive understanding of patient-centred care competence in the workplace.

### *Methodological Considerations, Validity and Limitations*

Some of the methodological considerations of the study, relate to data collection, sample size and instrumentation, and warrant further discussion. The data in this study were taken from two independent studies, using same instrument, the PCC [6]. Due to the secondary nature of the data, it was not possible to increase the sample size. However, the recommended sample size for a study like this, is at least five respondents per item in cross-sectional survey studies [38,39] which was realized in both studies. The PCC was translated to Finnish following the recommended forward-back translation process and semantic and linguistic equivalence were confirmed. As the PCC is a self-assessment instrument, the results may be affected by social desirability bias [49], as the participants may have evaluated their competence higher than in reality. This is to be expected as patientcenteredness in care, strongly rooted in the value-based healthcare, and often discussed in policy and strategic documents is a pillar of professional nurse education. There is no method available to evaluate competence in such value-laden activities, including the knowledge, skills, and attitudes objectively [21,24]. The PCC items self-assess knowledge, skills, and attitudes of the practicing nurse. The next step could be the development of a more objective assessment method. However, it might be very challenging objectively to measure all the aforementioned dimensions of competence. This may possibly lead to behavioural level assessment. It has been criticized that the competence of healthcare professionals is multidimensional, demanding several assessment methods.

Cronbach's alpha coefficients, indicating the level of internal consistency homogeneity of the total scale, in both datasets were (0.91–0.93). This high value suggests some scale items have similar meaning, requiring item deletion. However, the Cronbach's alpha coefficients are lower and more acceptable at the sub-scale level in both datasets (0.78–0.85 and 0.74–0.83). The correlation coefficients (also in the CFA) between the factors, especially between PCC4 and the other factors PCC1, PCC2 and PCC3, are high, suggesting there may be some overlap within the scales. The chi-square statistics did not show a model fit with a *p* value less than 0.05. However, this statistic is known to be sensitive to sample size [50] and is, therefore, insufficient in this study for the assessment of goodness-of-fit. The other goodness-of-fit indices were all acceptable.

The average variance extracted (AVE 0.41–0.49 within the sub-scales) implied that the discriminant validity may not be ideal and includes variance based on measurement bias. The factor loadings were mostly acceptable PCC1 (0.584–0.729), composite reliability CR 0.82), PCC2 (0.612–0.681, CR 0.77), PCC3 (0.726–0.824, CR 0.83) and PCC4 (0.699–0.707, 0.82). The criteria given (0.5 > AVE > 0.4) [44] if the composite reliability CR >0.6, is acceptable (here all CR > 0.7), but may suggest revision for the total scale, by deleting some possibly redundant items. The PCC scale could benefit from a Rasch analysis which would further analyse item-level reliability and provide information about how participants response patterns relate to the difficulty of the items. For the known-group validity testing, the findings regarding the total scale or its sub-scales indicate that competence was assessed in the hospital care context and in primary health care context in similar ways, even though there was a variety of service provision.

### **5. Conclusions**

Patient-centred care has a central role in healthcare worldwide [30,31] and has been found to improve health literacy and patient engagement, be effective and cost-effective [31] and can be used as an important indicator of care quality [2,13] and patient safety [6]. In nursing, patient-centred care competence has been identified as a core competency for nurses [7,32] and is needed to guide the development of care. The PCC instrument measures nurses' patient-centred care competence in terms of knowledge, skills, and attitudes through self-assessment. In this current study, the PCC was validated in the Finnish healthcare system by registered nurses using self-assessment. The PCC has proven reliability, construct validity and sensitivity for the measurement of non-contextual, specific competence. Further research into the analysis of item-level discrimination with, for example, Rasch modelling, will identify any overlapping items and person fit in evaluations, including the identification of nurse-related characteristics. The results of this study showed there is some room for improvement in the promotion of patient involvement in their care.

**Author Contributions:** Conceptualization, R.S., T.L., K.L.; methodology, R.S., M.S., M.P.; formal analysis, M.P.; investigation, T.L., K.L.; data curation, T.L., K.L.; writing—original draft preparation, R.S., K.L., T.L.; writing—review and editing, R.S., M.S., T.L., K.L., M.P.; visualization, M.P.; supervision, R.S., M.S., T.L.; project administration, R.S., T.L.; funding acquisition, R.S. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by The Turku University Hospital, special grant-in aid VTR, grant number 13238.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Ethics Committee of the University of Turku (34/2016/6 June 2016; dataset I) as well as the study with dataset 2 (4/2016/15 February 2016).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study as advised by returning of the anonymous questionnaires to the researchers.

**Data Availability Statement:** No new data were created or analyzed in this study. Data sharing is not applicable to this article.

**Acknowledgments:** We acknowledge Norman Rickard for the language edition. We would like to thank Statistician Pauli Puukka and Jouko Katajisto for their expertise in the earlier steps with the statistics, as this was the secondary analysis.

**Conflicts of Interest:** The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

### **References**


### *Article* **Older Adults' Perceived Barriers to Participation in a Falls Prevention Strategy**

**Júlio Belo Fernandes 1,\* , Sónia Belo Fernandes 2,\*, Ana Silva Almeida <sup>3</sup> , Diana Alves Vareta <sup>3</sup> and Carol A. Miller <sup>4</sup>**


**Abstract:** There is a need to increase older adults' access and adherence to falls prevention strategies. This study aims to explore older adults' perceived barriers to participation in a fall prevention strategy. A qualitative descriptive approach was used. Semi-structured interviews were conducted with 18 older adult users of a Day Care Unit from a Private Institution of Social Solidarity in the region of Lisbon and Tagus Valley in Portugal. The recruitment was made in September 2019. The interviews were recorded transcribed verbatim and analysed thematically using the method of constant comparisons. The barriers to participation in a fall prevention strategy are healthcare system gaps, social context, economic context, health status, psychological capability, and lack of knowledge to demystify myths and misconceptions about falls. There are different barriers to participate in a fall prevention strategy. It is urgent to eliminate or reduce the effect of these barriers to increase older adults' participation in fall prevention strategies.

**Keywords:** accidental falls; fall prevention; older adults; barriers; patient compliance

### **1. Introduction**

Every year, one out of three older adults falls. It is estimated that each year, more than 640,000 people die as a result of falls [1]. Falls are the second leading cause of non-fatal and fatal injuries among older adults [2–4]. Older adults with a high risk of falls are in the high-risk group for fall injury [5] and fall-related death [6]. Fall related injury can range from minor trauma to severe injuries requiring hospitalization. The most common severe injuries include fractured bones and soft tissue injuries [7,8].

Preventing falls and fall-related injuries is challenging because of its multifactorial nature [9]. Several studies have identified more than 400 potential risk factors for falling [10]. Results from numerous researches have suggested that multidimensional falls prevention strategies can be effective in reducing the number of falls [11–13]. Furthermore, several guidelines have been developed to summarise the best evidence and guide healthcare professionals in their clinical practice [14,15]. Despite these facts, many fallers do not seek any type of help to prevent further falls [16], as well as many older adults, do not engage in fall prevention strategies even after referrals are made [17].

To improve access and adherence to falls prevention strategies, health care policymakers and health administrators should contemplate older adults' perspectives when developing these strategies [18]. Little is known about the barriers to engage in a fall prevention strategy in the Portuguese population, therefore this research seeks to fill this evidence gap by exploring barriers to participation in a fall prevention strategy from the perspective of Portuguese older adults with a high risk of falling. By seeking this evidence

**Citation:** Fernandes, J.B.; Fernandes, S.B.; Almeida, A.S.; Vareta, D.A.; Miller, C.A. Older Adults' Perceived Barriers to Participation in a Falls Prevention Strategy. *J. Pers. Med.* **2021**, *11*, 450. https://doi.org/ 10.3390/jpm11060450

Academic Editors: Riitta Suhonen, Minna Stolt and David Edvardsson

Received: 25 April 2021 Accepted: 20 May 2021 Published: 23 May 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

we can provide insight into developing a more effective fall prevention strategy and take measures to minimise those obstacles and therefore increasing enrolment and participation.

### **2. Methods**

### *2.1. Study Design*

A qualitative descriptive study was conducted using semi-structured interviews, which enabled an in-depth exploration of older adults' perceived barriers to participation in a fall prevention strategy. To ensure quality in the research report we followed the con-solidated criteria for reporting qualitative research (COREQ) [19].

### *2.2. Setting*

The study setting was a Day Care Unit from a Private Institution of Social Solidarity in the region of Lisbon and Vale do Tejo in Portugal that caters to a population of over 80,000 people.

### *2.3. Sampling and Recruitment*

The study population consists of older adults who are users of the Day Care Unit. The sampling method selection was non-probabilistic by convenience. The inclusion criteria included: (1) have a high risk of falling; (2) have participated in a falls prevention strategy.

Researchers used the fall risk test developed by VeiligheidNL [20] to screen older adults. The test contains three simple questions: 'Did you fall during the past twelve months?', 'Do you experience problems with movement and balance?', and 'Are you afraid of falling?' When participants answer "yes" to the first question or two of the overall questions, they are considered at high risk of falling.

The recruitment was made in September 2019. Eligible participants were invited by telephone to participate in the interviews. All older adults available at the time of data collection that met the inclusion criteria were included in the study.

### *2.4. Participants*

Of the 26 older adults who agreed to participate in the study, 8 were excluded based on not meeting the inclusion criteria. We conducted 18 interviews, the participants were mostly male (61.1%). The mean age of participants was 76.2 (range 69–83 years) and the standard deviation was 4.16215 years.

### *2.5. Data Collection*

The interviews were conducted by the first author at the Day Care Unit facilities and lasted approximately 20 min. All interviews were audiotaped, transcribed verbatim into written data, anonymised, and analysed.

The semi-structured interview guide was developed based on data gathered from previous studies and with contributions from experts. Examples of questions used in the guide are: 'Were there any factors that limit you to participate in a falls prevention program?' 'Tell me about a particular example of a barrier to undertake a falls prevention program?' 'What do you think could difficult people to participate in a falls prevention program?' 'Do you have any suggestions for how services could improve its contributions for older adults to engage in a falls prevention program?'

### *2.6. Data Analyses*

In the process of analysis, Braun, Clarke, Hayfield, and Terry's [21] procedures were followed. Researchers listened to the audio records to obtain an overall sense and then transcribed verbatim into written data. The data was separated into meaning units, based on similarity. Meaning unit codes were developed based on participants' own words. Initially, the transcribed verbatim was reviewed independently by two study team members and manually coded using inductive content analysis to identify common themes. To ensure credibility, the researchers discussed and compared the emergent themes and

categories. Afterward, the other study team member reviewed the participant quotes and matched each quote to one of the identified themes.

### *2.7. Ethics and Procedures*

Before conducting the study, a research protocol was analysed and approved by the Institutional Review Board. Prior to the interviews, all participants sign a written informed consent to record, anonymously report and publish the research data.

### **3. Results**

Six themes emerged from the analysis of focus group data. These themes included several categories as showed in Table 1, and examples are provided in the following section.


**Table 1.** Barriers to undertaking a fall prevention strategy.

### *3.1. Healthcare System Gaps*

### 3.1.1. Access Shortage

Participants highlighted a shortage of program offers. Hence, they were unable to engage in a fall prevention program.

'There are not many offers of these types of programs. While I was in the hospital, I participated in an exercise program to prevent falls, but after discharged I questioned everyone and nobody was able to refer me to a community-based program. There is a real shortage.' (P11)

### 3.1.2. Lack of Personalised Interventions

In addition to the offer shortage, participants reported that the ones they attended lack personalised interventions. They felt that to solve their problem, they should have been targets of tailored programs. Program participants had different problems, so they should receive interventions personalised to their different needs.

'There's no personalised intervention. There were around ten or twelve people in a room doing the same thing. My problem was not the same as the others, so how does the same intervention solve different problems.' (P3)

### *3.2. Social Context*

### 3.2.1. Stigma Associated with Fall

Participants described stigma as a barrier to engage in a fall prevention strategy because they associate falls with the need to receive institutional care. They fear that by participating in a falls prevention strategy, their families might assume they lack the physical capacity to take care of themselves and therefore institutionalize them to nursing homes.

'It is unlikely for me to assume the need to undertake a fall prevention program because as soon as they feel that I lack capabilities to take care of me, they will search for a nursing home.' (P4)

### 3.2.2. Social Awkwardness

The group environment made participants state social awkwardness as they felt uncomfortable and unease in a group-based exercise program.

'At this age, it isn't normal for us to do training exercises in a gym. You look around and realise everybody feels uncomfortable. Life is full of awkward and uncomfortable situations. We can avoid them. You have a lot of say-so in how you feel as you grow older.' (P8)

### *3.3. Economic Context*

### Financial Capacity

Participants referred that their financial capacity is a major barrier to undertaking a falls prevention strategy. Even considering the offer of free programs, in some cases, the costs associated with travel in itself harm their family budget.

'Even if there was a greater offer of fall prevention programs, they are not free and you have to add travel costs. As you grow older, the money you spend on our health increases a lot.' (P10)

### *3.4. Health Status*

### 3.4.1. Lack of Physical Fitness

Participants reported their experience of facing physical challenges. They consider that despite thinking that they were able to perform the physical component of the fall prevention program, they lacked physical fitness.

'It was a bit more than I could manage. I thought I was capable to perform the exercises without any problems, but the reality was different. I felt short of breath and tired. I went there once and gave up.' (P7)

### 3.4.2. Impaired Mobility

Besides their lack of physical fitness, participants also reported their inability to face physical challenges due to impaired mobility. This impairment has an impact not only on the ability to perform exercises but also on the ability to travel from home to the facilities where the training program takes place.

'There were several problems. First, my impaired mobility has a tremendous impact on my ability to travel to the clinic. Then I was unable to do more than half of the exercise because of my mobility.' (P2)

### *3.5. Psychological Capability*

### Fear of Falling and Injuries

Participants referred to the fear of falling and injuries as a barrier. They stated that after several falls, even if they did not sustain any injuries, they become afraid of falling and this leads them to feel more and more limited in terms of their autonomy and physical independence.

'Who wants to participate in any exercise program if they have to leave their house and risk falling again. It's a big problem because you fall, and fall again and then you became afraid. Fear sets in and you don't want to do any daily activities.' (P12)

### *3.6. Lack of Knowledge*

3.6.1. Falls Perceived as Inevitable and Not Preventable

Participants referred that their lack of knowledge about falls led them to think that this was an issue that only affected frail older adults and that falls are accidental and, therefore, inevitable and not preventable.

'There is a belief that falls only happen to frail older adults. I thought they were an inevitable event associated with ageing. It wasn't just me who thought that. My sons also thought the same. Lack of knowledge leads to these common misconceptions.' (P12)

### 3.6.2. Underestimation of Risk

Participants reported that some older adults refused to admit that they are at risk of falling and thus underestimate the consequences of certain behaviours to increase the risk of fall.

'Sometimes people do not want to admit their weakness and they are careless, underestimate the consequences of their behaviours and then fall and sustain injuries.' (P1)

### **4. Discussion**

Understanding the barriers to undertaking a falls prevention strategy may influence the guideline to change the process of selecting and more appropriately target the person at risk of falling.

It is well known from information gathered in other researches that before choosing the program interventions, decision-makers need to understand the target group, setting, and barriers to change [18].

This research found that access shortage and lack of personalised interventions are healthcare system gaps that could act as barriers for older adults to undertake a falls prevention strategy. Participants described difficulties with accessing any type of fall prevention programs due to access shortage. Older adults require opportunities within their environment to attend these types of programs. There must be a variety of offers so that the person can choose a program that best suits one's personhood [22].

It seems clear, that for the successful implementation of a fall prevention strategy in community settings, it requires an approach involving a greater program offers. Given the limited resources in Portugal, it is likely that potential users will become unmotivated after realising that the resources are scarce and scattered.

A theme articulated amongst participants was the lack of personalised interventions. The identification of this barrier may reflect the value attributed by participants in maintaining their personhood and usual routines. Further, previous studies have shown that older adults may value the affective characteristics of care as much as achieving better health outcomes [23]. It has been known for a long time that intervention strategies should be tailored to the cultural and socioeconomic context. There are no strategies that have universal applicability [24]. There is a growing body of evidence demonstrating that personalised interventions should be applied to each person to achieve positive clinical outcomes and increase their satisfaction [25]. This type of care can be the path to include the person at the centre of care and improve older adults' adherence to falls prevention strategies. Despite this acknowledgment, reports from participants revealed that in the programs they engaged in, this did not happen.

Another barrier highlighted in this study is the social context, namely the stigma associated with falls and social awkwardness. According to participants, older adults perceived falling as a stigma as they related falls with declining capabilities and loss of independence and consequently with the need to be admitted in a residential or nursing home. Many older adults feel embarrassed and stigmatised about their falls, and consequently choose not to show their weakness [26].

Similar findings have been identified among older adults in Eastern Culture. In older Chinese people, there was a refusal to use walking aids as they perceived them as a bad omen and carried stigma [27].

It is necessary to remove the stigma associated with falling so that older adults can get the help they need to promote healthy and active aging. Therefore, fall prevention strategies should convey the message of positive health and social benefits, such as improving muscle strength and body balance rather than focusing on reducing falls [28].

Participation in group programs can lead to social benefits and often act as an enabler for continued participation, although the transition to new groups could be challenging [29]. In this study, the participants considered the group environment as socially awkward because they felt out of place in that environment. This barrier can be linked closely to an individual's preference as in other researches the group environment was appointed either as an enabler or a barrier to continuing with a fall prevention program [29].

Another identified barrier is the economic context. This barrier has a crucial preponderance for older adults' participation in falls prevention strategies, because if they do not have the financial capacity to support their daily expenses, they will not consider undertaking any other activities. Other studies also identified the financial situation as a barrier to participate in a fall prevention strategy [30,31]. However, there seems to be a consensus in the literature that the cost associated with intervention may not be perceived as a barrier, as long as the cost is fair and reasonable enough [26].

Regarding the health status, participants reported their experience of facing physical challenges. Other researchers also identified the lack of physical fitness and impaired mobility as major barriers to undertake a falls prevention strategy [32,33]. In addition, they identified that previous habits and perceived value of physical activity can be an important factor to older adults' participation in exercise programs [32].

To undertake a falls prevention strategy participants must change their behaviour in the same manner as a sedentary person needs to be supported and encouraged to take an exercise program [34]. Physical training must be a progressive and adaptive process to allow the body to adapt to the stress of exercise with greater fitness [33]. Apparently, in the programs attended by participants, the exercise routines were not tailored to their needs and health status, and, therefore, they were not able to perform well. As mentioned previously, fall prevention strategies must be tailored to the context and the participants in order to increase their adherence. Furthermore, fall prevention programs must be multidimensional, combining a wide range of specific interventions that go beyond physical exercise [18,33].

The fear of falling was perceived as a barrier that leads older adults to feel physically limited and consequently have to protect themselves against dangers, by delegating their care to others, and ultimately denying their own autonomy and physical independence. In other researches, older adults with previous falls were more prone to undertake a falls prevention strategy, and those who were afraid of falling were four times more likely to enrol in these types of strategies [18].

The underestimation of risk and falls being perceived as inevitable and not preventable are lined up with the conviction that falls are part of ageing. These findings may suggest that falls prevention strategy are not effective and emphasise the vital need that older adults have to acquire more knowledge to demystify myths and misconceptions about falls. Educational or awareness strategies must be part of a multidimensional falls preventions strategy to counteract the common misconception that falls are simply an issue for older and frail adults as a result of accidents and, therefore, not preventable [18,33].

### *Limitations and Trustworthiness*

Researchers carried out 18 interviews, which is considered sufficient for data saturation to occur. Data were collected by semi-structured interview during which participants described their experiences. The overall results illuminate variations in older adults' perspectives on barriers to undertake a falls prevention strategy.

In this study, participants' mental and physical status were not assessed. This is a limitation as active depression and sever physical illness could potentially influence the participants' answers. Additionally, similar to previous studies that depend on data collected from interviews, actual reports may diverge from what participants revealed due to biases such as lack of confidence in guaranteeing anonymity or protection of identity, values, or beliefs. We collected data from the reports of various participants to reduce this bias.

The study's trustworthiness was confirmed through credibility, transferability, dependability, and confirmability as described by Nowell, Norris, White, and Moules [35]. To increase credibility researchers debated each phase of analysis. Disagreements were solved by discussion until achieving consensus. To ensure its transferability, the researchers provide descriptions with appropriate quotations so that those who seek to transfer the findings to different sittings can judge transferability. To achieve dependability, researchers detailed every phase of the decision-making process so that others can follow the research. To ensure confirmability, external observers search for inconsistencies by comparing the similarity of their perceptions with the ones from the researchers.

### **5. Conclusions**

In conclusion, this research has shown that older adults identify different key barriers to engage in a fall prevention strategy. According to participants' narratives, we identified six categories of barriers, namely healthcare system gaps, social context, economic context, health status, psychological capability, and lack of knowledge.

From our point of view, some barriers need urgently to be addressed for older adults to participate in a falls prevention strategy. The healthcare system gaps and social context are major barriers that highlight the critical need to develop and disseminate fall prevention strategies through public and private partnerships and social marketing.

These programs should be structured based on personalised interventions for each person, as scientific evidence shows that tailored interventions can lead to positive clinical outcomes and increase personal satisfaction.

Another barrier and perhaps the most important is the economic context because if the person does not have the financial capacity to support the fees to carry out the program, they will certainly not engage in these activities. Falls prevention strategies must be low cost because falls are a public health problem, with impact on economic costs for healthcare systems worldwide, so prevention must be a priority. Thus, fall prevention strategies should have a minimal cost for users and ultimately be supported by the healthcare systems.

Further research is needed to better understand the relationships and impact of these barriers, also it would be valuable to study which barriers are the drives of success to participation in a falls prevention strategy.

**Author Contributions:** J.B.F.: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Project administration; Writing—Reviewing and Editing. S.B.F.: Conceptualization; Formal analysis; Investigation; Methodology; Writing and Reviewing. A.S.A.: Conceptualization; Formal analysis; Investigation; Writing and Reviewing. D.A.V.: Formal analysis; Investigation; Methodology; Writing and Reviewing. C.A.M.: Conceptualization; Methodology; Writing and Reviewing. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of CAS (ID/02-06.19, approved on 10 June 2019).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** The data presented in this study are available on request from the corresponding author. The data are not publicly available due to participants´privacy.

**Acknowledgments:** This work is financed by national funds through the FCT—Foundation for Science and Technology, I.P., under the project UIDB/04585/2020. The researchers would like to thank the Centro de Investigação Interdisciplinar Egas Moniz (CiiEM) for the support provided for the publication of this article.

**Conflicts of Interest:** The authors declare that they have no conflict of interests.

**Ethical Approval:** Before conducting the study, a research protocol was analysed and approved by the CAS Institutional Review Board (Date: 10 June 2019; ID/02-06.19).

### **References**


### *Article* **Effect of a Music Therapy Intervention Using Gerdner and Colleagues' Protocol for Caregivers and Elderly Patients with Dementia: A Single-Blind Randomized Controlled Study**

**Guido Edoardo D'Aniello 1,\*, Davide Maria Cammisuli <sup>2</sup> , Alice Cattaneo <sup>1</sup> , Gian Mauro Manzoni 1,3 , Enrico Molinari 1,2 and Gianluca Castelnuovo 1,2**


**Citation:** D'Aniello, G.E.; Cammisuli, D.M.; Cattaneo, A.; Manzoni, G.M.; Molinari, E.; Castelnuovo, G. Effect of a Music Therapy Intervention Using Gerdner and Colleagues' Protocol for Caregivers and Elderly Patients with Dementia: A Single-Blind Randomized Controlled Study. *J. Pers. Med.* **2021**, *11*, 455. https://doi.org/ 10.3390/jpm11060455

Academic Editors: Riitta Suhonen, Minna Stolt and David Edvardsson

Received: 11 April 2021 Accepted: 20 May 2021 Published: 23 May 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

**Abstract:** Music therapy (MT) is considered one of the complementary strategies to pharmacological treatment for behavioral and psychological symptoms (BPSD) of dementia. However, studies adopting MT protocols tailored for institutionalized people with dementia are limited and their usefulness for supporting caregivers is under investigated to date. Our study aimed at evaluating the effects of an MT intervention according to Gerdner and colleagues' protocol in a sample of 60 elderly people with moderate-to-severe dementia of the Auxologico Institute (Milan, Italy) and associated caregivers, randomly assigned to an Experimental Group (EG) (*n* = 30) undergoing 30 min of MT two times a week for 8 weeks and to a Control Group (*n* = 30) (CG) receiving standard care. Before and after the intervention, residents-associated caregivers were administered the Caregiver Burden Inventory (CBI) and the Neuropsychiatric Inventory (NPI). Depression and worry were also assessed in caregivers prior to the intervention, by the Beck Depression Inventory-II and the Penn State Worry Questionnaire, respectively. A mixed model ANCOVA revealed a Time\*Group effect (*p* = 0.006) with regard to CBI decreasing after the intervention for the EG and Time\*Group effects (*p* = 0.001) with regard to NPI\_frequencyXseverity and NPI\_distress, with a greater effect for the EG than the CG. Implications for MT protocols implementations are discussed.

**Keywords:** music therapy; dementia; caregiver; RCT

### **1. Introduction**

Behavioral and psychological symptoms of dementia (BPSD) refer to the spectrum of non-cognitive and non-neurological features significantly impacting on prognosis and patient management and constitute a major component of the disease, irrespective of its subtypes [1]. As dementia is a progressive disease, BPSD worsen over time, requiring higher support and increased sanitary and care costs [2]. The BPSD improve caregivers' burden and distress [3] and are related to an increased level of dependence according to the progression of the disease [4]. Indeed, many studies have focused on the stressors associated with caregivers' support. Remarkably, caregivers' coping strategies and personality factors seem to play a critical role towards controlling BPSD [5]. Further, BPSD increasing causes higher caregiver distress [3].

It has been estimated that the prevalence of BPSD in people with dementia living in institutional settings is approximately 91–96% [1] and the majority of patients mainly present with an outcome of neuropsychiatric symptoms such as depression, apathy, irritability, anxiety, euphoria, hallucination and disinhibition [6]. One of the most extensively used instruments to assess BPSD is the Neuropsychiatric Inventory (NPI) [7]. Validity

and reliability of the NPI have been established in different languages; it can evaluate 12 symptoms based on a caregiver's interview about patient (i.e., delusions, hallucinations, agitation, depression, anxiety, apathy, irritability, euphoria, disinhibition, aberrant motor behavior, night-time behavior disturbances, and eating behavior abnormalities) covering a wide range of symptoms associated with progressive dementia states. Treatment of BPSD currently represents a relevant therapeutic challenge for patients with moderate-tosevere dementia because of their difficulty in explaining feeling and emotions and agitation reported in the course of the disease [8]. Particularly, people with moderate-to-severe dementia are at higher risk of developing aggression [9], in terms of violent behavior and physically/verbally inappropriate responses to environmental stimuli [10].

Pharmacological treatment usually constitutes the primary approach to excessive behaviors but adverse effects of medication (e.g., speech inhibition, diminished language skills, altered gait and falls, and even a more severe cognitive deterioration) may occur in the treatment course [11], with negative consequences on patients' global status. Nonspecific experiences such as music listening, touch therapy, and hand massage may be beneficial for calming neuropsychiatric symptoms presented by patients with moderate-tosevere dementia [12]. Specifically, Music Therapy (MT) represents a non-pharmacological complementary strategy to pharmacological treatment for dealing with neuropsychiatric symptoms of people with dementia [13]. Recent advancements improving personalized medicine in research, diagnosis and treatment of dementia have sustained a more comprehensive approach for patients, with the aim of better finalizing scientific knowledge to tailored interventions starting from data integration about an individual's specific pattern of genetic variability, environment and lifestyle factors [14].

Through non-verbal behavior and sound-music performances, MT allows participants to convey their emotions and feelings, establish a contact with significant others and modify their affective status and interpersonal communication, with a positive adaptation to their social environment. In particular, Gerdner and colleagues' protocol [15,16] supports the fact that archaic expressive and relational non-verbal abilities persist across a person's life span and may be reactivated by MT as interpersonal modalities of relationship. More specifically, Gerdner outlined a specific theoretical framework in order to formalize and refine an individualized music listening for patients with dementia through the "*Mid-range theory of individualized music intervention for agitation*" (IMIA) [17]. The first factor on which IMIA is based concerns the perception of music by the person with dementia. Although the pathology may drastically reduce the ability to understand and produce language, the receptive and expressive skills concerning music are generally preserved much longer and beyond the severity of cognitive decline. For this reason, although the literature has not yet come to a univocal and solid explanation, we tend to consider music processing as partially independent from cognitive efficiency [18]. The second factor concerns the ability of music to elicit memories. As a powerful means of reminiscence, music can produce both pleasant and unpleasant memories, depending on the type of evoked stimuli, images and sensations linked to the person's private experience [19]. In order to avoid the possibility that music may elicit negative memories, it must be selected (i.e., an "*individualized approach*"). It has to be part of the patient's positive experience and should be based on his/her personal preferences (for example, popular music at the time of patient's adulthood, or songs offered during religious or other services followed, etc.). As specified by Gerdner [16], the assessment must cover individual songs as well as preferred instruments and genres; if cognitive impairment affects the ability of the person to select music, it is possible to interview the caregiver to find this information.

Given these characteristics, such a kind of protocol seems to be promising as a complementary strategy to pharmacological treatment for people with dementia living in institutional settings. Starting from this assumption, the aim of our study was to evaluate the effect of an MT intervention adopting Gerdner and colleagues' protocol in reducing neuropsychiatric symptoms reported by dementia patients and in ameliorating the caregiver's burden.

### **2. Materials and Methods**

### *2.1. Participants*

A randomized controlled trial (RCT) was conducted at the RSA *Monsignor Bicchierai* in the Istituto Auxologico (Milan, Italy). A total of 60 residents and associated caregivers were randomly assigned to the Experimental Group (EG) (*n* = 30) and to the Control Group (CG) (*n* = 30). The residents underwent a complete psychogeriatric and neurological examination at the Institute, including the administration of the Mini Mental State Examination (MMSE). Inclusion criteria to the study for residents encompassed: (i) a diagnosis of dementia, according to the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition; (ii) age over 80 years; (iii) an MMSE score < 20, ranging from moderate to severe dementia [20]. The residents were excluded if they report: (i) a severe psychiatric condition; (ii) a hearing impairment; (iii) any other inability that may interfere in attending a 20-minute MT intervention; (iv) absence of a reliable informant caregiver. No restriction was applied for residents-associated caregivers. Eligible participants and their caregivers were provided with a detailed explanation of the study. All the patients signed an informed consent and for those with a severe cognitive deterioration, the consent was provided by the caregivers who were reassured of confidentiality and anonymity of the data collected during the study. Participants could withdraw from the study at any time without any effect on their usual care at the Facility.

### *2.2. Clinical Measures and Outcomes*

Caregivers were administered the Caregiver Burden Inventory (CBI) [21] by a trained clinical psychologist dedicated to elderly care in the Facility. In addition, the Beck Depression Inventory-II [22] and the Penn State Worry Questionnaire [23] were used prior to the intervention. The caregivers were also interviewed about associated residents' neuropsychiatric symptoms by the Neuropsychiatric Inventory (NPI) (Cummings et al., 1994) [7] reporting two main scores (NPI\_aXb = frequency for severity; NPI\_distress = caregiver's distress). The effectiveness of the MT was expected as an improvement in the following outcome measures after the intervention: CBI total score, NPI\_aXb and NPI\_distress scores.

### *2.3. MT Intervention*

The residents and associated caregivers were allocated to the EG and the CG using a predetermined list of randomization, with 1:1 allocation ratio and they were blinded towards the intervention (Figure 1). All the participants completed the study protocol. In both cases, caregivers were considered part of the Facility staff signing the *Individualized Care Plan* designed by the multidisciplinary group (i.e., geriatrician, nursing coordinator, educator, social assistant, and clinical psychologist) for each resident and agreed to attend the Facility activities program during the intervention. While residents and associated caregivers of the CG followed the usual care provided by the Assisted Healthcare Residence staff (i.e., educational support and entertainment activities), residents and associated caregivers of the EG underwent an intervention of music listening strictly respecting Gerdner and colleagues' protocol [24], as follows: (1) music selection according to patient's preference by caregivers [25]; (2) music material file (i.e., Mp3) preparation for each resident, as a result of the collaboration between caregiver and psychologist; (3) MT intervention on residents' room at the Facility as a quiet and comfortable environment (i.e., 30 min 2 times a week for 8 weeks, for a total of 16 sessions); (4) information provided to caregivers by the psychologist on patient's monitoring during sessions (in case of agitation, music listening was interrupted).

**Figure 1.** The study flow chart.

#### **Figure 1.** The study flow chart. *2.4. Statistical Analysis*

*2.4. Statistical Analysis*  The collected data passed the Shapiro–Wilk test for normality distribution and Levene test for variances homogeneity. The comparability of the two study groups was first determined using T-tests for independent samples for continuous variables. Then, The collected data passed the Shapiro–Wilk test for normality distribution and Levene test for variances homogeneity. The comparability of the two study groups was first determined using T-tests for independent samples for continuous variables. Then, changes between groups after the intervention were compared by a mixed model ANCOVA by controlling for significant differences that resulted after the T-tests at baseline (Dependent variables: CBI; NPI\_aXb; NPI distress; Factors: Time and Groups, EG vs. CG; Covariates: BDI; PSWQ). The effect size was calculated by the eta squared.

#### changes between groups after the intervention were compared by a mixed model AN-**3. Results**

*3.1. Descriptive Analysis of the Whole Sample* 

tics of clinical measures are shown in Table 1.

**3. Results** 

#### COVA by controlling for significant differences that resulted after the T-tests at baseline *3.1. Descriptive Analysis of the Whole Sample*

(Dependent variables: CBI; NPI\_aXb; NPI distress; Factors: Time and Groups, EG vs. CG; Covariates: BDI; PSWQ). The effect size was calculated by the eta squared. Age and education of the residents were 89.50(±6.96) and 9.68(±5.20) years, respectively, 41.7% male and 58.3% female, with an MMSE of 9.45 ± 6.66. Age and education of the caregivers were of 61.7(±7.67) and of 11.5(±7.66) years, respectively. Descriptive statistics of clinical measures are shown in Table 1.

> **CG (***n* **= 30)**

**EG (***n* **= 30)** 

BDI-II 9.23 ± 1.68 6.15 ± 1.12 PSWQ 49.80 ± 12.44 40.10 ± 15.39

CBI (baseline) 27.26 ± 13.37 24.06 ± 10.51 CBI (follow-up) 19.53 ± 10.40 30.53 ± 11.69 NPI\_aXb (baseline) 20.46 ± 9.00 22.46 ± 12.96 NPI\_aXb (follow-up) 6.70 ± 5.17 18.70 ± 8.65 NPI\_distress (baseline) 10.66 ± 6.07 12.96 ± 6.21

Age and education of the residents were 89.50(±6.96) and 9.68(±5.20) years, respec-

tively, 41.7% male and 58.3% female, with an MMSE of 9.45 ± 6.66. Age and education of the caregivers were of 61.7(±7.67) and of 11.5(±7.66) years, respectively. Descriptive statis-


NPI\_distress (follow-up) 2.46 ± 2.06 10.66 ± 5.31

**Table 1.** Clinical measures of the EG and the CG prior and after the intervention. Data are expressed as mean ± standard deviation; EG: Experimental Groups; CG: Control Group;

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 5 of 9

Data are expressed as mean ± standard deviation; EG: Experimental Groups; CG: Control Group; BDI-II: Beck Depression Inventory-II; PSWQ: Penn State Worry Questionnaire; CBI: Caregiver Burden Inventory; NPI\_aXb: Neuropsychiatric Inventory\_frequency for serverity; NPI\_distress: Neuropsychiatric Inventory\_distress. 0.025, *p* = 0.156) dimensions at baseline. Conversely, significant differences were found in terms of depression severity (BDI-II) (t(58) = 3.768, *p* = 0.044), and worry (PSWQ) (t(58) =

#### *3.2. Comparison of the EG and the CG* 0.678, *p* = 0.009).

The T-tests for independent samples revealed that groups did not differ in terms of CBI (t(58) = 1.019, *p* = 0.313), NPI\_aXb (t(58) = 1.715, *p* = 0.490) and NPI\_distress (t(58) = 0.025, *p* = 0.156) dimensions at baseline. Conversely, significant differences were found in terms of depression severity (BDI-II) (t(58) = 3.768, *p* = 0.044), and worry (PSWQ) (t(58) = 0.678, *p* = 0.009). *3.3. CBI Results*  As shown in Figure 2, a Time\*Group effect (λ = 0.872; F(1,56) = 8.038; *p* = 0.006; η2 =

#### *3.3. CBI Results* 0.128) was found with regard to CBI that decreases after the intervention in the EG while

As shown in Figure 2, a Time\*Group effect (λ = 0.872; F(1,56) = 8.038; *p* = 0.006; η <sup>2</sup> = 0.128) was found with regard to CBI that decreases after the intervention in the EG while this trend was not shown for the CG. this trend was not shown for the CG.

**Figure 2.** Comparison of the average CBI global scores in the EG (purple line) and in the CG over time (green line).

was found with regard to NPI\_distress, with a greater effect for the EG.

**Figure 2.** Comparison of the average CBI global scores in the EG (purple line) and in the

As shown in Figure 3, a Time\*Group effect (λ = 0.740; F(1,56) = 20.343, *p* = 0.001; η2 =

0.260) was also found with regard to NPI\_aXb, with a greater effect for the EG. Likewise, as shown in Figure 4, a Time\*Group effect (λ = 0.779; F(1,56) = 16,165, *p* = 0.001; η2 = 0.221)

CG over time (green line).

*3.4. NPI Results* 

### *3.4. NPI Results*

As shown in Figure 3, a Time\*Group effect (λ = 0.740; F(1,56) = 20.343, *p* = 0.001; η <sup>2</sup> = 0.260) was also found with regard to NPI\_aXb, with a greater effect for the EG. Likewise, as shown in Figure 4, a Time\*Group effect (λ = 0.779; F(1,56) = 16,165, *p* = 0.001; η <sup>2</sup> = 0.221) was found with regard to NPI\_distress, with a greater effect for the EG. *J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 9

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 9

**Figure 3.** Comparison of the average NPI\_aXb in the EG (purple line) and in the CG (green line) over time. line) over time*.* 

**Figure 3***.* Comparison of the average NPI\_aXb in the EG (purple line) and in the CG (green

**Figure 4.** Comparison of the average NPI\_distress in the EG (purple line) and in the CG over time (green line).

**Figure 4.** Comparison of the average NPI\_distress in the EG (purple line) and in the CG

**Figure 4.** Comparison of the average NPI\_distress in the EG (purple line) and in the CG

We demonstrated that a structured MT intervention (i.e., 30 min two times a week

We demonstrated that a structured MT intervention (i.e., 30 min two times a week

for 8 weeks) based on Gerdner and colleagues' protocol [24] ameliorates caregivers' burden and reduces neuropsychiatric symptoms reported in assisted elderly residents with dementia better than usual care, both for their frequency/severity and perceived distress by caregivers. According to a recent 12-year longitudinal cohort study [26], understanding the natural course of neuropsychiatric symptoms in dementia is important for patient care planning and trial design. Remarkably, starting from a previous systematic literature review [27] highlighting how depression, agitation/aggression and apathy are the most distressing symptoms for caregivers assisting people with dementia, the MT intervention adopted reported an effect on neuropsychiatric symptoms as a whole, suggesting how it

for 8 weeks) based on Gerdner and colleagues' protocol [24] ameliorates caregivers' burden and reduces neuropsychiatric symptoms reported in assisted elderly residents with dementia better than usual care, both for their frequency/severity and perceived distress by caregivers. According to a recent 12-year longitudinal cohort study [26], understanding the natural course of neuropsychiatric symptoms in dementia is important for patient care planning and trial design. Remarkably, starting from a previous systematic literature review [27] highlighting how depression, agitation/aggression and apathy are the most distressing symptoms for caregivers assisting people with dementia, the MT intervention adopted reported an effect on neuropsychiatric symptoms as a whole, suggesting how it

over time (green line).

over time (green line).

**4. Discussion** 

**4. Discussion** 

### **4. Discussion**

We demonstrated that a structured MT intervention (i.e., 30 min two times a week for 8 weeks) based on Gerdner and colleagues' protocol [24] ameliorates caregivers' burden and reduces neuropsychiatric symptoms reported in assisted elderly residents with dementia better than usual care, both for their frequency/severity and perceived distress by caregivers. According to a recent 12-year longitudinal cohort study [26], understanding the natural course of neuropsychiatric symptoms in dementia is important for patient care planning and trial design. Remarkably, starting from a previous systematic literature review [27] highlighting how depression, agitation/aggression and apathy are the most distressing symptoms for caregivers assisting people with dementia, the MT intervention adopted reported an effect on neuropsychiatric symptoms as a whole, suggesting how it may be beneficial for a large spectrum of dimensions potentially impacting on patients' behavior and caregivers' health.

Other investigations have already shown a reduction in some neuropsychiatric symptoms associated with dementia after MT interventions. In detail, Garland et al. [28] showed that both listening to audiotapes with a conversation about positive experiences from the past and the exposure to a selection of songs that the individual used to enjoy in their youth are effective in reducing agitation. Holmes et al. [29] revealed that live interactive music is more effective than pre-recorded music in reducing apathy in moderate and severe dementia. Moreover, a case–control study [30] concluded that MT sessions consisting of singing songs chosen by the group accompanied by instruments significantly reduce agitation and anxiety in a sample of people suffering from moderate-to-severe Alzheimer's dementia. More recently, Raglio and colleagues [31] completed a Randomized Controlled Trial (RCT) reporting that consecutive cycles of 12 active MT sessions three times a week is sufficient for observing a significant reduction in behavioral disorders in severely impaired patients with dementia. Finally, Sung et al. [32] investigated the effects of group music sessions of 30 min, twice a week for 6 weeks in institutionalized elders with dementia (i.e., five-minute warm-up session with movements and breathing; 20-minute session of active participation using percussion instruments; five minutes of soft music listening) founding that such a type of intervention is effective for anxiety reduction. Our study added a few thoughts on MT protocols highlighting the potential role of music in evoking emotional response associated with personal memories (i.e., autobiographical events) thanks to an individualized approach able to bypass cognitive impairment severity.

Further, our findings are in line with the latest published Cochrane review [33] reporting that providing people with dementia with at least five sessions of a music-based therapeutic intervention improves overall behavioral and psychological problems at the end of treatment. According to the guidelines of the *Italian Psychogeriatric Association* [34] highlighting the necessity to produce RCTs based on structured evidence-based music protocols for people with dementia, we would stress that Gerdner and colleagues' schema represents an effective way to improve wellbeing both for people with dementia living in institutional settings and for their caregivers. Gerdner and colleagues' protocol for the usage of personal music materials to evoke past memories of the patients may represent an original application of personalized medicine in dementia, even if more efforts are necessary to meet the clinical complexity of the disease and to build stronger evidence able to address rehabilitation practice.

However, our study had some limitations. In order to reach a better generalizability of results, larger randomized *double-blind* controlled trials with follow-up measuring maintenance effects are encouraged in the future. Indeed, interventions based on listening to the music usually present the greatest effect at the end of the intervention, without maintenance effect [35]. It is also necessary to develop clinical trials aiming to design standardized protocols depending on etiology and stage of dementia so they can be applied alongside psychological intervention (e.g., cognitive-behavioral therapy) or pharmacological treatment. In addition, the CBI includes items referred to daily living and it does not fulfil criteria to specifically evaluate residents at institutional settings. In order to

implement future RCTs, researchers should also assume measures such as the Revised Scale for Caregiving Self Efficacy [36] with the scope of facilitating the development of improved caregiver strategies for dealing with stressors form care. Potential effects of medication received by patients with dementia that may influence results were also not taken into account.

### **5. Conclusions**

We documented that a structured MT intervention administered for 8 weeks (20 min a day) in a relaxing way for patients with moderate-to-severe dementia living in institutional settings is able to reduce BPSD and ameliorate caregivers' burden. Such an intervention was brief, safe, low-cost and can be replicated in similar contexts, without spending in excessive sanitary and human resources. A caregiver's efficacy for managing BPSD is an important determinant of familiar stress and plays a pivotal role with regard to patients' management. Implementing MT interventions with a more comprehensive assessment of caregivers' profile may be advantageous in supporting institutionalized elderly people with dementia.

**Author Contributions:** Conceptualization, G.E.D. and G.C.; methodology, G.E.D. and G.M.M.; formal analysis, D.M.C.; investigation, G.E.D.; resources, G.E.D.; data curation, A.C.; writing original draft preparation, D.M.C.; writing—review and editing, E.M. and G.C.; visualization, A.C.; supervision, E.M. and G.C.; project administration, G.C. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Ethics Committee of the Istituto Auxologico Italiano, (Milan, Italy) (Protocol number: "Interventions for Dementia 04/2018").

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** Details regarding data supporting results can be found at: http:// tesionline.unicatt.it/handle/10280/59475, Accessed date: 11 April 2021.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


### *Article* **Complexity of Nurse Practitioners' Role in Facilitating a Dignified Death for Long-Term Care Home Residents during the COVID-19 Pandemic**

**Shirin Vellani 1,2 , Veronique Boscart 1,3, Astrid Escrig-Pinol 1,4 , Alexia Cumal 1,2 , Alexandra Krassikova 1,5 , Souraya Sidani <sup>6</sup> , Nancy Zheng <sup>1</sup> , Lydia Yeung <sup>1</sup> and Katherine S. McGilton 1,2,\***


**Abstract:** Due to the interplay of multiple complex and interrelated factors, long-term care (LTC) home residents are increasingly vulnerable to sustaining poor outcomes in crisis situations such as the COVID-19 pandemic. While death is considered an unavoidable end for LTC home residents, the importance of facilitating a good death is one of the primary goals of palliative and end-of-life care. Nurse practitioners (NPs) are well-situated to optimize the palliative and end-of-life care needs of LTC home residents. This study explores the role of NPs in facilitating a dignified death for LTC home residents while also facing increased pressures related to the COVID-19 pandemic. The current exploratory qualitative study employed a phenomenological approach. A purposive sample of 14 NPs working in LTC homes was recruited. Data were generated using semi-structured interviews and examined using thematic analysis. Three categories were derived: (a) advance care planning and goals of care discussions; (b) pain and symptom management at the end-of-life; and (c) care after death. The findings suggest that further implementation of the NP role in LTC homes in collaboration with LTC home team and external partners will promote a good death and optimize the experiences of residents and their care partners during the end-of-life journey.

**Keywords:** nurse practitioners; nursing home; COVID-19; palliative care; end-of-life; dignified death; older adults

### **1. Introduction**

Individuals transition into long-term care (LTC) homes closer to the end of their life, often with multiple comorbid conditions, higher levels of frailty and complex care needs [1,2]. Within two years of admittance to LTC homes, most residents die [3,4]. As such, integrating a palliative approach to care would be the best practice, yet this approach is not implemented in the majority of LTC homes [5]. A palliative approach consists of four central components: advance care planning (ACP); optimization of pain and symptom management; psychosocial and spiritual support for patients and their care partners such as friends and relatives; as well as shared decision-making [6]. While death is an unavoidable ending for LTC residents, promoting a good death is an important goal of palliative and end-of-life (EOL) care [7,8]. This has become even more pressing during the SARS Coronavirus Disease-2019 (COVID-19) pandemic, where a large percentage of deaths were among LTC home residents, ranging from 8% in South Korea, 39% in the

**Citation:** Vellani, S.; Boscart, V.; Escrig-Pinol, A.; Cumal, A.; Krassikova, A.; Sidani, S.; Zheng, N.; Yeung, L.; McGilton, K.S. Complexity of Nurse Practitioners' Role in Facilitating a Dignified Death for Long-Term Care Home Residents during the COVID-19 Pandemic. *J. Pers. Med.* **2021**, *11*, 433. https:// doi.org/10.3390/jpm11050433

Academic Editors: David Edvardsson, Minna Stolt and Riitta Suhonen

Received: 30 April 2021 Accepted: 17 May 2021 Published: 19 May 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

United States [9] to 69% in Canada [10]. A good death is characterized by freedom from preventable distress in a dying person, their care partners, and healthcare providers; being in harmony with the wishes of the dying person and their family; and following clinical, cultural, and ethical principles [8].

Sufficient staffing is critical for integrating a palliative approach to care and to achieve a good death in LTC settings [11]. However, the LTC sector continues to suffer from chronic staff shortages. Furthermore, to optimize the infection prevention and control measures, LTC home residents have been forced to isolate in their own spaces with visitation restrictions from informal care partners [12]. Traditionally, care partners served as a means for socialization and comfort for residents and also assisted them with activities of daily living [13] and EOL care. During the pandemic, there was also a shift in physicians' presence in LTC homes, where many only worked virtually because of their multiple responsibilities across different sites [14], limiting the planning and implementation of palliative care. In contrast, nurse practitioners (NPs) in Ontario were able to work on-site [15] and provide palliative and EOL care by functioning closely with the registered nurses, registered practical nurses, and personal support workers in LTC homes [16]. In Ontario, Canada, NPs are advanced practice registered nurses, who can autonomously assess, diagnose, and treat patients [17,18] and are well situated to optimize the palliative and EOL care needs of LTC home residents. Empirical evidence demonstrates that palliative care provided by NPs in various settings was effective in improving persons' emotional and mental wellbeing as well as their quality of life [19]. NPs also increase ACP [20–22] and provide effective management of EOL symptoms [23,24].

There is limited knowledge of the role of NPs in delivering and coordinating EOL care and facilitating a "dignified death" for LTC home residents during the COVID-19 pandemic. The term "dignified death" is used in this study as the pandemic has hampered the staff's ability to ensure a good death by exposing the entire LTC sector to a myriad of challenges such as understaffing, limited family contacts and a lack of palliative care supplies in some LTC homes [25,26]. In this study, we focused on NPs' perspectives and aimed to explore their role and experiences in facilitating a dignified death for LTC home residents, while also facing the increased pressures related to the COVID-19 pandemic. The findings will provide more insight and understanding into the roles NPs can play in integrating a palliative approach to care in LTC settings. Additionally, they will highlight knowledge gaps in optimizing resident-centered palliative care in LTC homes and yield implications for policy makers, researchers and clinicians.

### **2. Methods**

### *2.1. Study Design and Participants*

We designed an exploratory qualitative study to examine the role and experiences of NPs in supporting a dignified death during the COVID-19 pandemic, as the phenomenon is not yet well-observed or understood [27]. The study used a phenomenological approach, which is valuable in revealing shared and divergent experiences among participants [28]. We conducted telephone-based semi-structured interviews with NPs providing care to LTC home residents during the pandemic. Recruitment of NPs was assisted by the Nurse Practitioners Association of Ontario (npao.org). An email with information about the project, inclusion criteria, and an invitation to connect with the Research Coordinator (RC) was sent out to all NPAO members by their Practice and Policy Manager. The inclusion criteria were NPs who worked at least three days a week in an LTC home that had experienced positive cases of COVID-19.

The final sample included 14 NPs from 14 separate LTC homes, representing approximately 13% of all NPs working in the province of Ontario LTC home sector. The recruited NPs worked in both rural and urban settings, as well as in an even mix of profit and not-for-profit homes. This sample size was determined by reaching data saturation, i.e., information became repetitious from one interview to the next [29]. The characteristics of the participating NPs and their respective LTC homes are summarized in Table 1.


**Table 1.** Characteristics of study participants and their workplace.

Most participants were employed full-time and experienced an increase in work hours during the pandemic. Most NPs were females, with an average of nine years of experience in the NP role. Eight were attending NPs and six were outreach NPs. Attending NPs provide direct primary health care to residents, work to increase the knowledge and skills of LTC staff and participate in administrative and leadership activities to improve resident outcomes and reduce pressures on acute care services [30]. The outreach NP role was created to provide comprehensive acute and episodic care to LTC home residents in order to avoid transfers to the emergency department, facilitate hospital transfers where necessary and reduce hospital stays through early repatriation back to LTC homes [31].

### *2.2. Procedures*

After receiving approval from the Research Ethics Board at the participating institution, we obtained informed written consent from participants. In order to maintain their privacy, each participant was assigned a unique identification number and all their identifying information (e.g., name of the LTC home) was anonymized in the interview transcripts. Furthermore, the research team had considered potential emotional distress for the participants with sharing their experiences during the pandemic. Therefore, participants were offered breaks, opportunity to reschedule or drop-out and resources for emotional support during the interview, when appropriate. Telephone interviews were conducted by the RC (AK), while a note-taker (LY or AC) recorded the topics conversed and other relevant information. We audio-recorded the interviews, which, on average, lasted 50 min and took place between August and October 2020. Participants were provided a CAD 50 gift card as an honorarium serving as a token of appreciation for their time and effort to participate during these extremely busy and challenging times imposed by the pandemic. Most NPs participated in the study after their regular work hours to prevent any work-time lost deserving recognition from the research team and the honorarium may have served as an incentive to participate. However, gift card was only introduced after NPs had expressed desire to participate to prevent the risk of undue inducement as suggested by other authors [32]. Additionally, participants had the option of leaving the study at any time.

Semi-structured interviews were designed to prompt NPs to elaborate and reflect on their experiences [33] related to EOL care before and during the pandemic, their thoughts on their roles and responsibilities, and how they adapted in the context of the crisis. The interview guide was piloted for clarity and relevance with an NP experienced in LTC homes, but this was not included as a part of the study. The interview guide is in Supplementary Material Table S1.

### *2.3. Data Analysis*

The RC reviewed and anonymized the professionally transcribed interviews by using participant ID numbers, guaranteeing confidentiality. Data were exported into NVIVO12 to be managed, organized, and coded. This provided the research team a greater degree of transparency and integrity as members were able to create notes on their thoughts alongside the participant data. It also allowed for tracking the analysis process efficiently and mapping the relationship between data. However, some team members had no prior experience of using the NVIVO software, which required more time to train members on its features before starting the analysis process. There were also issues with software compatibility with different operating systems.

We employed an inductive thematic analysis strategy adapted from Braun and Clark [34]. The analysis was conducted in five steps. The first step involved familiarization with the data, which involved the research team reading the interview transcripts multiple times and writing down ideas as they arose in the due process. Debrief sessions were held after each interview to discuss and record emerging topics. In the second step, the initial themes were generated in a systematic manner across all the interviews. Two analysts (a primary analyst (AK) and a secondary analyst (either SV/AC/LY/NZ)) independently coded each transcript into initial themes and met regularly to compare and reconcile coding divergences. The third step involved the identification of broader categories by collating the codes and gathering data appropriate to each category. Preliminary themes were used as a point of departure and evolved as analysts generated additional themes during the coding stage. We organized these topics into 10 preliminary themes. Initial themes were grouped into three broad categories. In the fourth stage, broader categories were reviewed by the full research team to reach a consensus on these categories. Once the consensus was reached, the analysis team verified the coherence of categories and themes by reading all collated extracts for each theme, while also confirming that they were sufficiently and meaningfully different from each other [34]. This strategy allowed for refinement of the themes and categories. In the final step, the research team generated clear definitions and names of the categories and themes [34,35], as presented in Table 2 below.


**Table 2.** Categories and themes related to the Nurse Practitioners' role in facilitating a dignified death in long-term care homes during the COVID-19 pandemic using Thematic Analysis [34].


**Table 2.** *Cont.*

Credibility was ensured by conducting systematic peer debriefing sessions, incorporating researcher reflexivity and triangulation, keeping an exhaustive record of the process and decisions made, managing data systematically, and analyzing opposing accounts [33,36]. Discussions during these peer debriefing sessions resulted in adjustments in the order and phrasing of questions to improve the flow and clarity during subsequent interviews, and in a list of preliminary themes appearing on each interview. For example, while we initially thought there was a sub-category related to how NPs partnered with families to ensure a dignified death, with more debriefing sessions and subsequent interviews, we realized that NPs reached out to family members for different purposes along the journey. Thus, the specific reasons for reaching out to families were included as themes within each category to better represent the important role NPs had related to connecting with families in all aspects of EOL care. The Standards for Reporting Qualitative Research guidelines were followed [37].

### **3. Results**

Three categories were derived in relation to the NPs' roles and responsibilities in facilitating a dignified death for LTC home residents under their care: (a) ACP and goals of care discussions; (b) pain and symptom management at the EOL; and (c) care after death. The categories are presented in Table 2 and detailed below.

### *3.1. ACP and Goals of Care Discussions*

NPs described this responsibility as engaging with residents and more frequently with their health care proxies, who were often care partners, by taking a proactive approach to facilitate ACP and goals of care conversations. They connected with care partners for difficult, yet critical, discussions when the residents appeared to be nearing the EOL. During the pandemic, these conversations with care partners usually happened virtually over the telephone or through video calls. NPs attested to the importance of implementing a palliative approach to care where the focus is on the residents' quality of life, while also adhering to the safety requirements necessitated by the COVID-19 pandemic. Many highlighted the complexity of these discussions in light of care partners' inability to see firsthand the residents' decline due to the physical distancing restrictions. One NP explained:

*This was time-consuming, but we were very successful in bringing families into sort of an understanding of reality and acceptance of end-of-life issues* . . . *advance-care planning was a huge, huge part of my time–helping families to move along that continuum.* (NP 13)

NPs explained that, generally, ACP and goals of care conversations are carried out with care partners and residents at the time of admission to the LTC home, and regularly thereafter, particularly when any acute changes in condition arise. However, during the pandemic, the need and frequency of these conversations increased markedly, as explained by this NP:

*If there's a change in the resident's condition, I would be the one in touch with the families. It was a bit more fast-forwarded (during the pandemic). I just had so many of them. So, I would have daily conversations with probably five to 10 families about goals of care.* (NP 3)

Some LTC homes did not have the resources to tackle these discussions in a timely way. Therefore, several NP participants were specifically assigned by their LTC home management to support LTC staff in holding ACP and goals of care discussions with families, given the constant risk of a sudden decline in residents' condition. In addition, several NPs organized and chaired virtual care conferences linking families with the care team and physicians, involving residents whenever possible. One NP (*NP 8*) noted that their team was called "palliative rescue", alluding to the fact that when there was a COVID-19 outbreak, several residents became sick very fast, potentially needing life-sustaining treatments and goals of care discussions. This NP explained:

*One of my homes I was supporting virtually and via telephone had a COVID outbreak. They started with 10 cases, and then within three days, they had 30, and then it was escalating, and then by the end of the week, they had over 77 cases. So, at that point, we spoke with the DOC [director of care] and were asked to support goals of care discussions with the families because the home had not done them and so the entire outreach team started calling families to discuss goals of care.* (NP 8)

Many NPs noted that communication with families was a responsibility that frequently fell upon them during the pandemic. Several NPs indicated that although these conversations were lengthy, they were gratifying. NPs engaged in difficult conversations with care partners regarding prior requests for life-sustaining treatments, such as resuscitation, in light of the inherent risk of aerosolizing COVID-19 viral particles during such interventions, and the impact of these treatments on residents' quality of life and wellbeing. These interactions provided care partners the opportunity for shared decision-making to devise a plan of care, whether that involved comfort care in the LTC home or transfer to a hospital, which was not always possible due to the pandemic and restrictions imposed by the acute care hospitals, making these conversations even more difficult. In terms of restrictions, some NPs indicated that in order to prepare for the surge of patients with COVID-19 in acute care, some administrators within LTC homes were informed to avoid hospital transfers by managing their residents' acute changes in condition within their homes. As

such, NPs needed to make decisions on how to balance the needs of the residents and potential outcomes of life-sustaining treatments. Some NPs made these difficult decisions in consultation with emergency department physicians, which was often made possible based on a history of working together.

NPs were sensitive to the fact that care partners could not be present physically due to the social distancing measures when the residents were dying. As such, in many cases, NPs helped family members appreciate the inevitable nearing of the EOL and also provided much needed emotional support. One participant explained:

*Yes, communicating with families was my big responsibility really. It sort of just fell upon me, explaining to the families what was happening and if it looked like the person was at the end-of-life, then I would be talking to them about palliative care and what things we could do for the person in the home in order for them to have a dignified death in the home.* (NP 12)

Overall, NPs made it their duty to keep the families abreast of the residents' condition, such as how COVID-19 was affecting them and what the care options were for the day, which served as a lifeline for the families given their inability to be physically present with the resident. They served as a link between the family and the residents, listened to the families' fears and concerns, and answered their questions.

### *3.2. Pain and Symptom Management at the EOL*

The NPs' second responsibility consisted of optimizing comfort for residents who were at the EOL and where death was imminent, through pain and symptom management. This involved working closely with LTC home staff and management teams in optimizing emergency supplies and planning ahead for emergencies; prescribing anticipatory medications to aid EOL symptom management; consulting with expert clinicians where needed; and addressing the psychosocial needs of residents and families. Some NPs played an instrumental role in creating the EOL order sets with input from palliative care physicians in their local hospital. They also updated these order sets regularly to include relevant symptom management for residents dying of COVID-19 infection due to its unique symptom profile because the appearance and progression of symptoms such as respiratory distress can be rapid and fulminant, intensifying over a short period of time; and shared them with clinicians at other LTC homes. Additionally, NPs led educational initiatives to prepare and guide staff on interventions pertaining to intravenous therapy and hypodermoclysis. Moreover, NPs became involved in sourcing an optimal stock of emergency supplies such as oxygen, parenteral antibiotics and analgesics in the event that they were needed after hours. One NP explained:

*We had a lot more End-of-Life meds in the building. We had more oxygen concentrators. We had more IM antibiotics, more Hydromorphone* . . . *we did increase our emergency stock med, so that we could* . . . *like at 2:00 a.m. if we needed to. So, I guess that's the other thing we did plan.* (NP 6)

In general, NPs were instrumental in ensuring that analgesics and other medications were available when needed for palliative and EOL care needs. Many NPs stressed the importance of collaborative teamwork involving LTC home nurses and other staff to optimize residents' care given the scarcity of resources and shortage of staff.

NPs expressed that it was difficult to complete timely in-person assessments given the challenges associated with insufficient staffing and the time required to don and doff the personal protective equipment (PPE) with each resident interaction. Despite this, they tried their best and worked with other staff for ongoing identification of distressing symptoms, prescribing anticipatory and emergent treatments to address them, specifically in cases where EOL order sets had not been implemented. Many referred to the fact that LTC home physicians were generally not present in person during the pandemic, requiring NPs to manage this limitation in medical management. Therefore, NPs also assisted staff in the safe and timely delivery and assessment of prescribed therapies, including opioids. Ultimately, together, the teams ensured that residents died peacefully. Several NPs expressed that EOL care was most challenging because of the physical/social isolation, whereby direct contact with residents was more limited, in addition to family and friends not being able to visit. Many NPs found that working closely with the LTC staff and connecting with other NPs working in the LTC sector served as sources of strength to deal with challenges they experienced during these times. NPs ensured that staff and residents' care partners had their direct numbers to reach out any time of the day. Moreover, they worked hard to identify residents close to the EOL and ensured that symptom management was provided, as this quote exemplifies:

*We just really wanted to identify the residents who were unfortunately really sick or passing away from COVID. Because we didn't want them to die uncomfortably and alone and without any support and care. And that was probably the most emotional because you find residents with a respiratory rate of 50 and they're diaphoretic and they're struggling to breathe and they're alone. And so, we did provide our assessments and we tried to give the residents the treatment that they needed to die comfortably.* (NP 10)

NPs talked about the complexity of LTC home resident care associated with their advanced age and multimorbidities, sometimes requiring consultation with expert clinicians and services to optimize pain and symptom management at the EOL. NPs consulted physicians with expertise in nephrology, palliative care, and geriatrics mostly virtually when they were unable to visit in-person. Furthermore, to address situations when they were not available, NPs developed algorithms for LTC home staff on how to consult with specialists. In some LTC homes, palliative care physicians provided expert consultations to NPs in order to facilitate a dignified death for residents with more complex needs, as is highlighted in this quote:

*So, the ten residents that died, I provided their palliative care, their end-of-life symptom management. And if there was a resident that I was having difficulty managing their symptoms, I would call and consult with a palliative care physician to get those symptoms under control.* (NP 1)

Therefore, NPs' resourcefulness in consulting with clinical experts helped to ensure the better control of symptoms for residents who were nearing death.

Many NPs also addressed the psychosocial needs of residents and their families, particularly when the residents were nearing the EOL. They expressed that sitting vigil at the time of death is considered a norm in LTC homes; however, this was challenging during the pandemic. They felt a sense of responsibility to promote human connection in these difficult circumstances as best as possible, through creative means, with support from LTC home staff. Several NPs pointed out that compassionate visits were offered to care partners when their residents were imminently dying, allowing them to stay as long as possible while making sure that their PPE remained safely usable. This was illustrated by NPs in the following quotes:

*When we were talking about comfort or end-of-life, then we were offering compassionate visits. So essentially once I was in contact with the families, then I would put them on the list of allowed visitors.* (NP 3)

*As soon as we possibly could, if people were dying, knowing they were clearly at the end-of-life, then families could come in–one person at a time with full PPE.* (NP 13)

In cases where families could come but were unable to be at the bedside due to the active risk of exposure to the aerosolized virus, NPs and LTC home staff tried unprecedented and creative ways to allow families and residents to see and hear each other through a window or virtual means. One NP shared her experience with a resident that involved juggling with safety procedures while also enabling family connection in the last moments of life:

*I feel at peace at least with what we were able to do for her* . . . *her oxygen requirements were going up fast* . . . *potentially aerosolizing the COVID virus.* . . . *we knew she was* *going to pass away from COVID* . . . *and she was on the main floor so the family was able to come to her window. We were able to sort of set up the phone on our end and then call their cell phone on the other side, so it kind of looked like you were talking to each other* . . . *it was very sad but it was also, you know, the quote "good death" if you will.* (NP 5)

Finding creative ways to promote connection and support the psychological needs of the resident and care partners at the last moments of life highlights the critical role the NPs played.

Moreover, in many cases, NPs collaborated with LTC home staff such as personal support workers to keep vigil at the time of residents' death so that they would not die alone. They held residents' hands or played a musical instrument when the care partner could not be at their bedside. This was believed to be a source of comfort for residents as well as staff, and in line with enabling a dignified death given the restrictions imposed by the COVID-19 pandemic.

### *3.3. Care after Death*

The third NP role responsibility involved being present with the staff for the dignified performance of last offices and providing emotional support to staff and care partners upon residents' death. Care after death also included informing the care partners of the death, upholding the pandemic-related policy of allowing only one grieving care partner at a time, and completing death certificates, sometimes after hours. Several NPs expressed feeling significant moral distress as the pandemic led to losing several residents under their care in a short period of time, in addition to seeing care partners lose time for genuine human connections that will not be replaced. One NP explained:

*It was very difficult to watch families come in one at a time and try to manage their grieving by themselves, with their other family in the parking lot. That's what's changed at end-of-life; that's what made it so difficult. Calling a resident's family to say that they passed away, and they weren't there.* (NP 1)

Despite their own high emotional burden, NPs worked hard to provide emotional support to grieving care partners.

NPs also worked closely with LTC home nurses and the administrators in devising and implementing new policies related to the care after death. To contain the potential spread of the COVID-19 virus, they had a very restricted amount of time to pronounce death, inform the family, perform the last offices (previously performed by the funeral homes), and hand over the body to the funeral home staff, who were not allowed to come into the building; all of this while avoiding the omnipresent media. NPs identified that they were under a great deal of pressure to prevent the accumulation of bodies in LTC homes. NPs took on the leadership role in identifying the best practices in performing the last offices with dignity and care as well as instituting specific considerations for those who died with COVID-19 infection. They educated staff on COVID-19-focused care after death through demonstrations and hands-on help. As, many unregistered staff had no previous experience of performing last offices. One NP describes their post-death experience as follows:

*The other thing that we had a lot of policy around, this sounds horrible, but on pronouncing death and removing bodies from the home. This was a nightmare. We got this thing that said nobody could come in the home to take them out—I'm going to cry* . . . *but we had to do all of the post-mortem care and the nurses found that so hard. So again, we needed to look at how it was done, how do you transport people out. How do we keep the media from photographing people that died as they're being taken out of the home? It was brutal.* (NP 13)

Given that NPs in the province of Ontario have the ability to complete the death certificates if they had the primary responsibility of the patient, they were responsible for completing them as soon as the residents passed. This NP describes her experience below: *All the death certificates were completed online. I would often get a phone call in the middle of the night to do a death certificate, like at 2:00 a.m. to complete one, where those could have waited 'till the next morning, previously.* (NP 6)

As such, NPs worked beyond normal hours to fulfill their duties that also involved administrative tasks post residents' death, highlighting the significance of their role and the added stress.

NPs described challenges encountered by the LTC home staff after any resident's death due to experiencing pandemic-based disenfranchised grief. For example, novel and continuously changing COVID-19 policies affected how LTC home staff would traditionally perform care after death. As a result, NPs had to meet the pandemic-imposed demands while also mindfully allocating large amounts of time and effort in working closely with nurses and other staff to adapt new policies and providing them emotional support to recognize and process the losses. One participant stated:

*Because normally the way nursing homes deal with resident death is the funeral home would come and prepare the body and whatnot. And there's actually a ceremony, not a real ceremony, but all the staff lines up at the front entrance and it's more of a respectful send-off to the resident, whereas this is kind of like "OK, let's just get the body ready and take them outside." And no one was allowed to be there to witness all of this stuff. So, it just doesn't feel as humanistic as how it was done pre-COVID.* (NP 2)

NPs provided emotional support to staff, especially after the changes to the processes after death were made, which often left little room for staff's own grieving. As one NP noted:

*What I learned very quickly is she [staff] just needed to be listened to, and just needed to have someone who could validate her fears and say yeah, we don't know all the answers but we're going to get through this, and we're going to do it together* . . . *mostly it was listening, listening, listening, and modeling. And trying–and not appearing fearful yourself.* (NP 13)

Many NPs expressed that given the challenges associated with working during the pandemic, they had minimal time to focus on in their own self-care; however, they found communication exchanges with other staff helpful. NPs relayed a sense of accomplishment and gratitude to be a part of the healthcare workforce during this pandemic. They highlighted that their work was complemented by the LTC home staff and administrators, all of whom were devoted to doing their best to provide person-centered care during this time of crisis when much was unknown. It appears that NPs served as a binding force that played a crucial role in holding together the staff and residents in facilitating a dignified death for the residents.

### **4. Discussion**

SARS COVID-19-related adverse events and mortality have been the highest in the LTC sector globally [38,39]. This is because of a complex interplay of multiple intricate and inextricably connected factors that increase the vulnerability of LTC home residents to not only contract COVID-19 infection but also to sustain poor outcomes, including death [40,41]. Amidst this unprecedented crisis, there has been a further decline in already limited human and material resources in LTC homes to optimally provide for the needs of the residents and the workforce, who continued to care for their residents with threadbare resources [42].

Residents admitted to LTC homes are increasingly complex, with high care needs [1,2]. Death is a critical juncture for not only the residents but also their care partners and LTC home staff [3,4]. However, the COVID-19 pandemic brought a variety of challenges in the achievement of a good death. This study demonstrated that NPs, along with staff within LTC home teams, collaborated and worked tirelessly to support a dignified death experience for residents. NPs and staff assisted in ACP and goals of care discussions with residents and care partners, both proactively and when residents showed signs of

acute changes in condition. This, in turn, helped care partners move forward in accepting the impending EOL. Findings from our study correlate with other studies that demonstrated an increase in ACP discussion where NPs were involved in the residents' care team [20–22], with one study showing a 300% increase in the number of residents with ACP discussions [20]. Similar to the findings in our study, Campbell and colleagues also found that NPs were part of the collective approach in ensuring residents were frequently assessed, especially those in the last stage of their life [43]. NPs worked hard so that residents' distressing symptoms were addressed, that they were comfortable, and died in their familiar surroundings rather than a hospital, when appropriate. NPs helped LTC home staff and administrators implement new policies and procedures related to post-death care, such as dignified care of the deceased, while maintaining the infection prevention and control measures, in addition to catering to the emotional needs of the staff and grieving care partners.

Our study demonstrated that NPs played a vital role in promoting a dignified death for LTC home residents while navigating the challenges of the COVID-19 pandemic. Based on previous studies, a good death is a broad construct where multiple factors can play a role to achieve it [44]. These factors can be related to the individual experiencing the death, their care partners as well as healthcare providers. Allison and O'Connor describe a 6-step framework used by clinical nurse specialists to facilitate a good death in residential aged care facilities [45]. The framework involved (1) responding within 24–48 h of a referral; (2) visiting the residential aged care setting to assess the resident and train the staff; (3) developing a care plan; (4) encouraging staff to proactively request medications for pain, respiratory secretion, and nausea from the general practitioner; (5) liaising with management and ensuring support for staff; and (6) involving the family in care planning and preparing them for death. The findings from our study suggest that NPs were able to faciliate a dignified death which appeared to be aligned with the 6-step framework provided by Allison and O'Connor, but also did more due to their expanded scope of practice. For example, some NPs were available 24 h a day either in person or over the phone, not only to staff but also to residents' care partners. Additionally, they were able to prescribe medications including opioids in order to maximize comfort in the last moments of life.

In addition to pain control, peace, and dignity, the presence of care partners, and being surrounded by familiar people and things have also been identified as sources promoting a good death in those dying with dementia [46]. Though people's preferences for the presence of others may vary, having someone present at the time of death can serve to address the primal need for companionship and is seen as a closing chance to display comfort and affection to the resident [47]. Whereas COVID-19 stripped the care partners of these opportunities, NPs collaborated with LTC home staff in identifying ways to connect them through virtual and other creative means. NPs or the staff also sat vigil by the residents' bedside of those who were in the last moments of their life. However, there remains a need for further initiatives and research on how to best care for residents' spiritual and cultural needs as well as the needs of the bereaved in light of the strange circumstances imposed by the COVID-19 pandemic [48].

This study highlights several research, policy, and clinical implications. NPs fostered interdisciplinary collaboration for in-house care that embraced an integrated palliative approach with chronic disease management. However, a palliative approach to care is not a norm in the LTC sector and regular ACP discussions are not a standard of practice [49]. ACP discussions are generally held in the form of level of care documentation to identify residents' and their proxy's wishes related to hospital admission and resuscitation at the time of admission to the LTC home and do not necessarily identify their values and wishes such as for their EOL care. Furthermore, previous research has identified that non-palliative specialist NPs who have provided palliative care to people under their care have also expressed the need for education in palliative care [50], highlighting a gap in relevant training and education. A recent work commissioned by the Alzheimer

Society of Canada on Improving End-of-Life Care for People with Dementia in LTC homes during the COVID-19 pandemic and beyond proposes three strategies to implement a palliative approach [49]. These include (a) adopting it in the whole home; (b) education and training of all staff on a palliative approach to care; and (c) implementing policies and tools that assist staff to use their knowledge about a palliative approach to enhance resident care [49]. Some LTC homes have successfully implemented a palliative approach through initiatives such as the Strengthening a Palliative Approach in Long Term Care Model (SPA-LTC) [51,52]. Hence, there is much to learn from their experiences in order to successfully implement this approach in other homes and to increase the capacity of LTC home staff, including the NPs as well as external consultants. Additionally, there is a need to implement the same palliative care standards of practice across all practice settings, appreciating the highly complex resident population served by LTC homes.

NPs working collaboratively with their team members have demonstrated the ability to provide high quality palliative and EOL care [19,23,53]. Countries and regions where the role of NPs is either non-existent or in infancy can learn from the experiences of various regions in Canada, the USA and the UK, where the role of the NP has been successfully implemented [18] to be able to autonomously assess, diagnose, order, and interpret diagnostic tests and treat their patients with full prescriptive authority. In addition, they are able to collaborate with other healthcare practitioners including primary care physicians and palliative care specialists and seek further advice when required. Furthermore, they embrace shared decision-making and serve as a link bringing the healthcare team, residents and their care partners together for coordinated care planning [43,54]. As a result, NPs globally can be in a better position to deliver timely and person-centered care to LTC home residents, which includes the provision of a dignified death.

Although this study provides new insights into the evidence involving the role of NPs in the integration of a palliative approach, it has limitations. It is an exploratory study involving a small sample of NPs; hence, the findings may not be transferable to other regions. However, the NPs included in our study worked in geographically diverse regions of Ontario, including both private and not-for-profit homes serving a wide range in the number of residents. In addition, we did not compare the experiences of NPs working in different models, i.e., attending or outreach and in different types of LTC homes. This was due to them all having performed similar functions and conveying the same sense of duty in caring for their residents who are experiencing the EOL. However, future research should explore the differences between the roles, responsibilities, and outcomes associated with the two groups of NPs working in LTC settings. Finally, the study did not include other LTC home staff such as nurses and administrators. This results in missing insights into their role in implementing an integrated palliative approach and supporting a dignified death to their residents during the pandemic.

### **5. Conclusions**

Despite numerous challenges, the NPs played a critical role in facilitating a dignified death for LTC residents through ACP and goals of care discussions, EOL pain and symptom management and care measures after the death of residents. A dignified death for residents was accomplished in close collaboration with LTC home staff. The COVID-19 pandemic has emphasized the need to take an upstream approach in implementing an integrated palliative approach to care for residents and their care partners that focuses on the needs of the whole person while acknowledging their mortality. While LTC homes need to implement this approach, in light of the exceptional circumstances imposed by the pandemic, it is critical that interventions are in place to address complicated bereavement in care partners and moral distress in LTC home staff.

**Supplementary Materials:** The following are available online at https://www.mdpi.com/article/10 .3390/jpm11050433/s1, Table S1: Semi-Structured Interview Guide with Nurse Practitioners.

**Author Contributions:** All authors have contributed substantially to the work reported. Conceptualization, K.S.M. and S.V.; methodology, A.E.-P., and K.S.M.; validation, K.S.M., A.E.-P., S.V. and A.K.; formal analysis, S.V., A.K., A.C., N.Z., L.Y., A.E.-P. and K.S.M.; investigation, A.K., A.C. and L.Y.; resources, K.S.M.; data curation, A.K., K.S.M. and S.V.; writing—original draft preparation, S.V.; writing—review and editing, S.V., K.S.M., V.B., A.E.-P., A.C., S.S., A.K., L.Y., N.Z.; visualization, A.K.; supervision, K.S.M.; project administration, L.Y. and A.K.; funding acquisition, K.S.M. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by Maria and Walter Schroeder Institute for Brain Innovation and Recovery.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Research Ethics Board of the Toronto Rehabilitation Institute-University Health Network (protocol code: 20-5652; date of approval: 20 July 2020).

**Informed Consent Statement:** Informed consent was obtained from all participants involved in the study.

**Data Availability Statement:** Not applicable.

**Acknowledgments:** We would like to acknowledge the NPs who took time to participate in the study.

**Conflicts of Interest:** The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

### **References**


### *Article* **The Development of a Personalized Symptom Management Mobile Health Application for Persons Living with HIV in China**

**Shuyu Han <sup>1</sup> , Yaolin Pei <sup>2</sup> , Lina Wang <sup>3</sup> , Yan Hu 1,4,\* , Xiang Qi <sup>2</sup> , Rui Zhao 1,5, Lin Zhang <sup>6</sup> , Wenxiu Sun <sup>6</sup> , Zheng Zhu 1,4 and Bei Wu 2,\***


**Abstract:** Persons living with HIV (PLWH) continuously experience symptom burdens. Their symptom prevalence and severity are also quite different. Mobile health (mHealth) applications (apps) offer exceptional opportunities for using personalized interventions when and where PLWH are needed. This study aimed to demonstrate the development process of the symptom management (SM) app and the structure and content of it. Our research team systematically searched for evidence-based resources and summarized up-to-date evidence for symptom management and health education. Our multidisciplinary research team that included physicians, nurses, software engineers, and nursing professors, evaluated the structure and content of the drafted app. Both quantitative data and qualitative results were collected at a group discussion meeting. Quantitative data were scores of sufficient evidence, situational suitability, practicability, cost-effectiveness, and understandability (ranged from one to four) for 119 items of the app contents, including the health tracking module, the self-assessment module, coping strategies for 18 symptoms (80 items), medication management, complementary therapy, diet management, exercise, relaxation techniques, and the obtaining support module. The SM app was comprised of eight modules and provided several personalized symptom management functions, including assessing symptoms and receiving different symptom management strategies, tracking health indicators, and communicating with medical staff. The SM app was a promising and flexible tool for HIV symptom management. It provided PLWH with personalized symptom management strategies and facilitated the case management for medical staff. Future studies are needed to further test the app's usability among PLWH users and its effects on symptom management.

**Keywords:** HIV; mobile health; smartphone application; symptom management

### **1. Introduction**

Since the development of antiretroviral therapy (ART), persons living with HIV (PLWH) can achieve a relatively satisfying life expectancy [1]. However, symptoms and related health outcomes have brought significant challenges and distress to the quality of life for PLWH. Many factors such as HIV infection, opportunistic infections and comorbidities,

**Citation:** Han, S.; Pei, Y.; Wang, L.; Hu, Y.; Qi, X.; Zhao, R.; Zhang, L.; Sun, W.; Zhu, Z.; Wu, B. The Development of a Personalized Symptom Management Mobile Health Application for Persons Living with HIV in China. *J. Pers. Med.* **2021**, *11*, 346. https://doi.org/ 10.3390/jpm11050346

Academic Editor: Riitta Suhonen

Received: 28 March 2021 Accepted: 23 April 2021 Published: 25 April 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

ART toxicity, and social discrimination contribute to the onset and progression of symptoms among PLWH [2,3]. Although ART helps to decrease symptom intensity [4], it also brings on additional symptoms such as lipodystrophy, insomnia, and rash [3]. Evidence showed that both the number and frequency of symptoms were not associated with CD4 count levels, which indicated that those symptoms persisted throughout the HIV infection trajectory in PLWH [4]. PLWH usually suffer from physical and psychological symptoms simultaneously [5]. Common symptoms of PLWH include fatigue, depression, pain, rash, and insomnia. The average symptom counts can be as high as 8–17 [6–8]. Previous studies reported a different but high prevalence of these common symptoms, with a range of 43–78% [6–8]. PLWH are burdened with multiple symptoms. They also have different symptoms of distress and unmet needs further exacerbate their situations. Therefore, the long-term and complexity of HIV symptoms call for more personalized and sustainable symptoms management strategies.

Chinese PLWH receive free ART based on the National Strategies of Four Frees and One Care for HIV/AIDS [9]. However, only publicly-funded domestic antiretroviral medications are free of charge. The integrase strand transfer inhibitors (INSTIs), which are the internationally recommended first-line treatment medication for PLWH [10], by contrast, are imported and needed to be paid out-of-pocket. Therefore, due to the issue of affordability, instead of taking these imported INSTIs, most Chinese PLWH choose to take free ART medications, e.g., efavirenz (EFV) or lopinavir/ritonavir (LPV/r). These medications may increase their risks for medication toxicity and symptoms of distress (EFV may lead to rash and sleep disorders, LPV/r may lead to diarrhea [11]). Evidence also showed that PLWH in developing countries were disproportionally affected by mental symptoms compared to their counterparts in developed countries [12]. The prevalence of depression and anxiety symptoms among Chinese PLWH is 61% and 43%, respectively [13]. The symptom burden may seriously affect PLWH's ART medication adherence, clinical prognosis, and quality of life [3,8,14]. Furthermore, Chinese PLWH's needs for symptom management are unmet due to their severe symptom burden, fear of asking for help because of HIV-related stigma, and difficulties in getting timely assistance for symptom management from medical staff [15,16]. Therefore, the development of symptom management for Chinese PLWH is urgently needed.

Smartphone use has been increasing and popularizing rapidly in the last two decades [17]. The health education and self-management strategies provided by the mobile health (mHealth) applications (apps) benefit both PLWH and medical professionals [18]. Several mHealth apps designed for PLWH provide functionalities, including medication reminders, communication to peers or providers, medical information searching engine and resources, and laboratory reports [19]. Although one app was previously developed to facilitate symptom management among PLWH [20], culturally tailored symptom management tools and suitable strategies for Chinese PLWH are still limited. Our research team developed a mHealth app to provide PLWH with a more convenient tool for personalized symptom management. This study aimed to demonstrate the development process of the symptom management (SM) app and its structure and content.

### **2. Framework**

Our study was guided by a framework (Figure 1) informed by the University of California, San Francisco (UCSF) Symptom Management Model [21] and the Self-regulatory HIV/AIDS Symptom Management Model (SSMM-HIV) [14]. Three key components of symptom management are symptom experience, management strategies, and outcomes. Symptom experience focuses on symptom occurrence (the cognitive pathway) and symptom distress (the emotional pathway). Symptom management strategies consider who, what (the nature of the strategy), when, where, how (delivered), to whom (the recipient of intervention), how much (the intervention dose) and why. Outcomes involve symptom outcomes and clinical outcomes. Social support, ART medication adherence, and quality of

life are equally essential components of HIV/AIDS symptom management. Guided by this framework, we designed the main functions and content of the SM app. outcomes and clinical outcomes. Social support, ART medication adherence, and quality of life are equally essential components of HIV/AIDS symptom management. Guided by this framework, we designed the main functions and content of the SM app.

**Figure 1.** Symptom Management Framework. **Figure 1.** Symptom Management Framework.

#### **3. Materials and Methods 3. Materials and Methods**

According to the Good Practice Guidelines on Health Apps and Smart Devices [22], it was important to collect health content information from evidence-based resources and the opinions from multidisciplinary experts (healthcare professionals, engineers, professional bodies, patient or consumer associations, etc.). Therefore, the development of the SM app included two phrases. Nursing researchers first systematically searched for evidence-based resources to summarize up-to-date evidence for symptom management and health education and then completed the app's first draft. At the next step, the multidisciplinary research team including physicians, nurses, software engineers, and nursing researchers, evaluated the quality of the app through a group meeting. According to the Good Practice Guidelines on Health Apps and Smart Devices [22], it was important to collect health content information from evidence-based resources and the opinions from multidisciplinary experts (healthcare professionals, engineers, professional bodies, patient or consumer associations, etc.). Therefore, the development of the SM app included two phrases. Nursing researchers first systematically searched for evidencebased resources to summarize up-to-date evidence for symptom management and health education and then completed the app's first draft. At the next step, the multidisciplinary research team including physicians, nurses, software engineers, and nursing researchers, evaluated the quality of the app through a group meeting.

#### *3.1. Drafting the Structure and Content of the App 3.1. Drafting the Structure and Content of the App*

Our research team designed the overall structure of the SM app according to the symptom management framework and determined the symptoms based on the modified sign and symptom checklist for HIV (SSC-HIV rev) [23] and self-completed HIV symptom index [24]. These two tools reflected common symptoms of PLWH and had been applied among Chinese PLWH in previous studies [16,25]. Then nursing researchers searched health education and coping strategies for each symptom. Our research team designed the overall structure of the SM app according to the symptom management framework and determined the symptoms based on the modified sign and symptom checklist for HIV (SSC-HIV rev) [23] and self-completed HIV symptom index [24]. These two tools reflected common symptoms of PLWH and had been applied among Chinese PLWH in previous studies [16,25]. Then nursing researchers searched health education and coping strategies for each symptom.

Our research team developed the Chinese culturally adapted AIDS Clinical Nursing Practice Guidelines in 2014, which contained comprehensive evidence for common symptoms [26]. Given this important previous work, we only searched for literature that stood in the high hierarchy of the evidence pyramid, i.e., guidelines rather than original studies and systematic reviews. We also included clinical manuals and books in both English and Chinese concerning PLWH treatment and care that focused on symptom evaluation, symptom treatment, and symptom management strategies. We thoroughly searched evidence-based resources at various websites, including the World Health Organization, UNAIDS, the Centers for Disease Control and Prevention, Association of Nurses in AIDS Care, European AIDS Clinical Society Department of Health and Human Services, U.S. Department of Health and Human Services, International Association of Providers of AIDS Care, British HIV Association, New York State Department of Health AIDS Institute, Our research team developed the Chinese culturally adapted AIDS Clinical Nursing Practice Guidelines in 2014, which contained comprehensive evidence for common symptoms [26]. Given this important previous work, we only searched for literature that stood in the high hierarchy of the evidence pyramid, i.e., guidelines rather than original studies and systematic reviews. We also included clinical manuals and books in both English and Chinese concerning PLWH treatment and care that focused on symptom evaluation, symptom treatment, and symptom management strategies. We thoroughly searched evidence-based resources at various websites, including the World Health Organization, UNAIDS, the Centers for Disease Control and Prevention, Association of Nurses in AIDS Care, European AIDS Clinical Society Department of Health and Human Services, U.S. Department of Health and Human Services, International Association of Providers of AIDS Care, British HIV Association, New York State Department of Health AIDS Institute,

Office of the AIDS Research Advisory Council (OARAC), and Canadian AIDS Treatment Information Exchange (CATIE).

### *3.2. Group Discussion and Written Feedback from the Multidisciplinary Research Team*

We drafted the structure and content of the app from the review of the evidencebased resource. A group discussion meeting with the multidisciplinary research team was conducted in November 2017 in a conference room at the Shanghai Public Health Center (SPHC) affiliated with Fudan University. The handbook and checklist that quantitatively evaluated the quality of the app were sent to each expert by email in advance. During this 150 min group discussion meeting, a researcher (the sixth author) introduced the framework and contents of the app, and experts individually gave their suggestions and feedback. A total of 119 items, including the health tracking module, the self-assessment module, coping strategies for 18 symptoms (80 items), medication management, complementary therapy, diet management, exercise, relaxation techniques, and the obtaining support module were evaluated in terms of sufficient evidence, situational suitability, practicability, cost-effectiveness, and understandability (scores from 1 to 4). The group discussion was recorded and analyzed within 24 h. Members could also communicate with the researcher staff for additional suggestions after the meeting. Informed consent was obtained from all group members.

### **4. Results**

### *4.1. Suggestions and Feedback from the Group Discussion*

After systematically searching and summarizing evidence-based resources for symptom management (Supplementary Material Table S1 presents the detailed sources), we drafted the structure and content of the app and then conducted the multidisciplinary group meeting. Ten experts, including hospital managers, nursing professors, physicians, nurses, and software engineers, gave their suggestions and feedback. Among them, three had Ph.D. degrees, three had master's degrees, and six had bachelor's degrees. All experts completed the evaluation checklist. They generally agreed with the framework and content of the app and gave high scores on the questionnaire. Supplementary Material Table S2 presents the detailed scores for each item. The qualitative suggestions were as follows:

The health tracking module operated convenient and attractive functions of checking laboratory tests. However, this model needed to be enhanced with data visualization. Tables or trend charts were recommended to help users track their health indicators. According to this suggestion, the revised app added the indicator trend submodule in the health tracking module. When an indicator had more than two times of data, this submodule could generate a trend chart.

Experts strongly recommended simplifying the assessment tools in the self-assessment module. For instance, we could apply the two-item Patient Health Questionnaire (PHQ-2) instead of the nine-item Patient Health Questionnaire (PHQ-9) to assess depression. According to this suggestion, all symptom assessment tools were simplified to less than four items (Supplementary Material Table S3).

We revised or deleted some details of the symptom management coping strategies according to the experts' suggestions to make the strategies applicable in the local context. For example, (a) the experts thought that some complementary therapies for fatigue and diet therapies for depression were not suitable for the recommendation. Therefore, we deleted the following: "Taking vitamin or mineral supplements, such as vitamin B12, can help relieve fatigue. Some traditional Chinese medicines, such as rhodiola, ginseng, and licorice, may also help relieve fatigue." and "We suggest consuming more vitamin-D-rich foods, such as eggs, and vitamin B, such as blueberries and bamboo shoots to ameliorate depressive symptoms. Additionally, food rich in Omega-3 and tryptophan may help improve moods." (b) Symptom diaries (sleep diary and emotion diary) were recommended for deletion. One expert (E8) thought they were complicated and increased the amount of reading for users. (c) The deletion of some medication advice for symptom management

was suggested. For example, some listed medicines for diarrhea were not available in China and should be deleted (E1 and E3). Medication for perianal neoplasms should be used under particular conditions. The listing of these medications in the app, which might be misleading and cause clinical risks, was suggested to be deleted (E10). One of the headache management strategies was as follows: "Herbal short-toned chrysanthemum may be effective in relieving headache. It is recommended to take it more than two hours apart from the ART medication and under the guidance of medical staff." Short-toned chrysanthemum was not commonly prescribed clinically and ought to be deleted (E2). (d) One item for fever management was as follows: "Fever may occur at any stage of the disease. It is an indicator of the disease and a process by which the immune system reacts to outside pathogens. When experiencing a fever, you should focus on cooling down, identifying the cause of your fever, preventing chills, and consuming enough water." The experts suggested revising and adding the following expression: "When experiencing a fever, you should visit a doctor as soon as possible." (E3)

In order to provide more comprehensive medication guidance, experts recommended adding a table of ART medication interactions with other medications in the app. We accepted this suggestion and added the table in the medication management submodule in the coping strategies module.

Stigma might discourage PLWH from downloading and using this app. Logo and homepage should not show HIV. In addition, data security and confidentiality should be strengthened to reduce patients' concerns. The following measures were conducted to address these issues: (a) We removed all HIV-related information in the app logo and homepage. (b) To ensure internal network security, we could use virtual local area network (VLAN) technology and logical isolation strategies. Using the latest firewall technology and packet filtering or proxy technologies could allow data to pass through selectively, making it possible to effectively monitor any activity between the internal network and the external network and prevent malicious and illegal access. (c) All data were recommended to be transmitted on the Web API (application programming interface) to ensure data transmission security. Encrypting sensitive data during the transmission process was recommended. An application authentication and authorization mechanism were also established. (d) Users could set a login password and/or gesture password. The screen would be locked if no operations were performed in the last 5 min. (e) To prevent data leakage, we transmitted the patient's laboratory test data directly from the hospital's health information system (HIS) to the mobile terminal of the app. The web-based administration portal could not acquire any user's medical or identity information.

It would be user-friendly to provide a communication platform between medical staff and PLWH. Thus, medical staff could give personalized information support according to the patients' questions. We accepted this suggestion and designed a question and answers (Q&As) submodule in the obtaining support module (the staff answered questions from users on the web-based administration portal). Medical staff should answer users' questions on the web-based administration portal within 48 h.

In order to strengthen the sustainability of the SM app, experts recommended designing neat and aesthetically pleasing app interfaces and providing various forms of information, including text, pictures, audio, and videos, to attract more users. They also recommended embedding the app into the routine process of clinical follow-ups, such as case management in SPHC.

### *4.2. Structure and Key Functions of the App*

Based on all our previous work, the final app structure and functions in the mobile terminal include eight modules. Users see the home page as Figure 3a after opening the SM app (Figure 2). Four major modules are shown on the home page, including health tracking, self-assessment, coping strategies, and obtaining support. Other modules with smaller logos are newly registered user, regular user, symptom history, and reminders and settings. By clicking the round blue button at the top left of the home page, users can connect their

(**a**) Home page (Chinese)

personal information with the HIS of SPHC through the Certification Information button (Figure 3c). Technicians check users' ID numbers and names within 48 h and give user's permission to browse their medical reports in the web-based administration portal. If users have had visits in SPHC, they can see all the information, including their prescriptions and laboratory reports, in the SM app. mation button (Figure 3c). Technicians check users' ID numbers and names within 48 h and give user's permission to browse their medical reports in the web-based administration portal. If users have had visits in SPHC, they can see all the information, including their prescriptions and laboratory reports, in the SM app. *J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 12 and settings. By clicking the round blue button at the top left of the home page, users can connect their personal information with the HIS of SPHC through the Certification Infor-

and settings. By clicking the round blue button at the top left of the home page, users can connect their personal information with the HIS of SPHC through the Certification Infor-

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 12

**Figure 2.** Logo of the SM app. **Figure 2.** Logo of the SM app. **Figure 2.** Logo of the SM app.

**Figure 3.** Screenshot of the home page and information settings. **Figure 3.** Screenshot of the home page and information settings.

#### 4.2.1. Self-Assessment Module 4.2.1. Self-Assessment Module

 (**b**) Home page (English) (**c**) Information settings (Chinese) (**d**) Information settings **Figure 3.** Screenshot of the home page and information settings. 4.2.1. Self-Assessment Module By clicking the self-assessment module on the home page, users can see symptom assessment options as in Figure 4a. Symptom assessment includes two mental symptoms (depression and anxiety) and 16 physical symptoms (fatigue, headache, muscle and joint pain, fever, sleep disorder, diarrhea, nausea or vomiting, shortness of breath or cough, By clicking the self-assessment module on the home page, users can see symptom assessment options as in Figure 4a. Symptom assessment includes two mental symptoms (depression and anxiety) and 16 physical symptoms (fatigue, headache, muscle and joint pain, fever, sleep disorder, diarrhea, nausea or vomiting, shortness of breath or cough, numbness/tingling of hands or feet, perianal neoplasms, fat redistribution, weight loss, rash, oral leukoplakia or ulcers, memory loss, and blurred vision). By clicking on one of the symptom buttons (such as depression), users can see the assessment tools as in Figure 4c. We applied PHQ-2 to screen depression [27] and the Generalized Anxiety Disorder scale (GAD-2) to screen anxiety [28]. Both PHQ-2 and GAD-2 are widely used valid screening tools. There were no available validated and widely-used screening tools for each physical symptom. Therefore, we designed screening tools for 16 physical symptoms. According to the symptom management framework, symptom experience focuses on symptom occurrence (the cognitive pathway) and symptom distress (the emotional pathway), i.e., symptom severity and symptom distress. Therefore, all the physical symp-By clicking the self-assessment module on the home page, users can see symptom assessment options as in Figure 4a. Symptom assessment includes two mental symptoms (depression and anxiety) and 16 physical symptoms (fatigue, headache, muscle and joint pain, fever, sleep disorder, diarrhea, nausea or vomiting, shortness of breath or cough, numbness/tingling of hands or feet, perianal neoplasms, fat redistribution, weight loss, rash, oral leukoplakia or ulcers, memory loss, and blurred vision). By clicking on one of the symptom buttons (such as depression), users can see the assessment tools as in Figure 4c. We applied PHQ-2 to screen depression [27] and the Generalized Anxiety Disorder scale (GAD-2) to screen anxiety [28]. Both PHQ-2 and GAD-2 are widely used valid screening tools. There were no available validated and widely-used screening tools for each physical symptom. Therefore, we designed screening tools for 16 physical symptoms. According to the symptom management framework, symptom experience focuses on symptom occurrence (the cognitive pathway) and symptom distress (the emotional pathway), i.e.,

toms were assessed from these two aspects. For example, the two items for fatigue: (1) If

numbness/tingling of hands or feet, perianal neoplasms, fat redistribution, weight loss,

the symptom buttons (such as depression), users can see the assessment tools as in Figure 4c. We applied PHQ-2 to screen depression [27] and the Generalized Anxiety Disorder scale (GAD-2) to screen anxiety [28]. Both PHQ-2 and GAD-2 are widely used valid screening tools. There were no available validated and widely-used screening tools for each physical symptom. Therefore, we designed screening tools for 16 physical symptoms. According to the symptom management framework, symptom experience focuses on symptom occurrence (the cognitive pathway) and symptom distress (the emotional pathway), i.e., symptom severity and symptom distress. Therefore, all the physical symptoms were assessed from these two aspects. For example, the two items for fatigue: (1) If

(English)

symptom severity and symptom distress. Therefore, all the physical symptoms were assessed from these two aspects. For example, the two items for fatigue: (1) If a score of 0 means no fatigue at all, and a score of 10 means the worst fatigue you can imagine, how much do you rate your fatigue over the past 2 weeks? (2) How much does fatigue affect your daily life (0 = not at all, 1 = a little, 2 = a moderate amount, 3 = very much, 4 = extremely)? All the brief self-reported tools that assess each symptom are available in Supplementary Material Table S3. *J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 7 of 12 a score of 0 means no fatigue at all, and a score of 10 means the worst fatigue you can imagine, how much do you rate your fatigue over the past 2 weeks? (2) How much does fatigue affect your daily life (0 = not at all, 1 = a little, 2 = a moderate amount, 3 = very much, 4 = extremely)? All the brief self-reported tools that assess each symptom are available in Supplementary Material 3. *J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 7 of 12 a score of 0 means no fatigue at all, and a score of 10 means the worst fatigue you can imagine, how much do you rate your fatigue over the past 2 weeks? (2) How much does fatigue affect your daily life (0 = not at all, 1 = a little, 2 = a moderate amount, 3 = very much, 4 = extremely)? All the brief self-reported tools that assess each symptom are available in Supplementary Material 3.


**Figure 4.** Screenshot of symptom assessment options and symptom assessment tools. **Figure 4.** Screenshot of symptom assessment options and symptom assessment tools. **Figure 4.** Screenshot of symptom assessment options and symptom assessment tools.

> A total of 80 symptom management strategies are available in the SM app. Users receive personalized result interpretations and strategies (Figure 5a) according to their assessment submission and cutoffs. Appendix 3 also presents all the cutoffs for each assessment tool. A total of 80 symptom management strategies are available in the SM app. Users receive personalized result interpretations and strategies (Figure 5a) according to their assessment submission and cutoffs. Appendix 3 also presents all the cutoffs for each assessment tool. A total of 80 symptom management strategies are available in the SM app. Users receive personalized result interpretations and strategies (Figure 5a) according to their assessment submission and cutoffs. Appendix 3 also presents all the cutoffs for each assessment tool.


**Figure 5.** Personalized results explanation and strategies, and the health tracking module. **Figure 5.** Personalized results explanation and strategies, and the health tracking module. **Figure 5.** Personalized results explanation and strategies, and the health tracking module.

#### 4.2.2. Health Tracking Module 4.2.2. Health Tracking Module

By clicking the health tracking module on the home page, users can see their latest prescription and four submodules on the screen, i.e., laboratory report, indicator trend, medication list, and symptoms results (Figure 5c). By clicking the laboratory report button, users can see their lab report results transferred from the HIS system (Figure 6a). If they have not visited SHPC before, they can input blood test results themselves. The indicator trend button in the health tracking module can generate tables and trend charts to help users track their health indicators, including their viral load, CD4+ T cell count, body temperature, body weight, pain, fatigue, and ART medication adherence (Figure 6c). By clicking the health tracking module on the home page, users can see their latest prescription and four submodules on the screen, i.e., laboratory report, indicator trend, medication list, and symptoms results (Figure 5c). By clicking the laboratory report button, users can see their lab report results transferred from the HIS system (Figure 6a). If they have not visited SHPC before, they can input blood test results themselves. The indicator trend button in the health tracking module can generate tables and trend charts to help users track their health indicators, including their viral load, CD4+ T cell count, body temperature, body weight, pain, fatigue, and ART medication adherence (Figure 6c).

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 8 of 12

**Figure 6.** Screenshot of laboratory report and indicator trend. **Figure 6.** Screenshot of laboratory report and indicator trend.

#### 4.2.3. Coping Strategy Module 4.2.3. Coping Strategy Module

The coping strategy module on the home page provides basic knowledge and coping strategies, including medication management (ART medication introduction, the principles of taking ART medication, taking medicine under particular circumstances, the interaction of ART medication with other medication, and coping strategies for the side effects of ART medication), the principles of using a complementary therapy, diet adjustment (balanced diet, safe diet, and diet under special circumstances), exercise (exercise principles, exercise choice, exercise plan, and precautions), and relaxation training (mindfulness, deep breathing, image guidance, body scan, and activating events–beliefs–consequences (ABC) rational-emotive behavior therapy). The coping strategy module on the home page provides basic knowledge and coping strategies, including medication management (ART medication introduction, the principles of taking ART medication, taking medicine under particular circumstances, the interaction of ART medication with other medication, and coping strategies for the side effects of ART medication), the principles of using a complementary therapy, diet adjustment (balanced diet, safe diet, and diet under special circumstances), exercise (exercise principles, exercise choice, exercise plan, and precautions), and relaxation training (mindfulness, deep breathing, image guidance, body scan, and activating events–beliefs–consequences (ABC) rational-emotive behavior therapy).

#### 4.2.4. Obtaining Support Module 4.2.4. Obtaining Support Module

The obtaining support module on the home page has four submodules including, health care support, peer support, information support, and Q&As. Any questions left on the Q&As submodule are answered by medical staff within 48 h. The obtaining support module on the home page has four submodules including, health care support, peer support, information support, and Q&As. Any questions left on the Q&As submodule are answered by medical staff within 48 h.

#### 4.2.5. Other Modules 4.2.5. Other Modules

The newly registered user module on the home page provides knowledge patients who took ART medication for less than six months needed to know, including an introduction to HIV, an introduction to ART, ART medication adherence, timely follow-up, safety measures, and a healthy lifestyle. The regular user module on the home page provides knowledge and topics designed for patients who have taken ART medication for The newly registered user module on the home page provides knowledge patients who took ART medication for less than six months needed to know, including an introduction to HIV, an introduction to ART, ART medication adherence, timely follow-up, safety measures, and a healthy lifestyle. The regular user module on the home page provides knowledge and topics designed for patients who have taken ART medication for more than six months, including treatment goals, treatment progress, medication resistance, medication side effects, healthy lifestyle, and fertility options.

### 4.2.6. Web-Based Administration Portal Functions

The web-based administration portal for medical staff and technical staff includes five functions:


### *4.3. Privacy and Confidentiality*

The following design helps users understand that the SM app protects users' privacy and confidentiality. Firstly, people cannot distinguish from the logo (Figure 2) and homepage (Figure 3a) that the SM app was designed for PLWH. Secondly, it is not mandatory for users to provide their personal information. If they do not provide their ID number, they can still use all the functions of the app. The only advantage for connecting their ID number with our hospital is that they can check and look up all the medical prescriptions, laboratory tests through the app as Figures 5c and 6a. If users do not provide personal information but still want to see the generated trend of their health status based on the health indicators, such as CD4 + T cell count (Figure 6c), they can input data by themselves. Thirdly, users can set a login password and/or guest password. The screen is locked if no operations are performed in the last 5 min.

### **5. Discussion**

To our knowledge, the SM app was the first attempt to develop a mHealth app for personalized symptom management for PLWH in China. It was developed based on evidence-based resource reviews and input from our multidisciplinary research team. The SM app can be operated on both Android and iOS systems. It also has a web-based administration portal managed by medical staff and technicians.

mHealth technology has been developing rapidly in recent years. Given the potential to improve access to care by reducing geographical and financial barriers, mHealth apps provide feasible, accessible, and effective platforms for self-management of many chronic diseases, including hypertension [29], diabetes [30], and cancer [31]. They are also increasingly being used for the care of PLWH [19]. HIV infection is a lifelong chronic disease. After HIV infection, symptom management is a long-term task for PLWH. PLWH also have different symptom prevalence and severity. Therefore, mHealth apps are promising choices for expanding the HIV personalized symptom management interventions.

The SM app provides reliable symptom management knowledge from evidence-based resources that are recommended by researchers. The multidisciplinary group discussion was an efficient way to collect opinions from different areas and perspectives and played an important role in ensuring the accuracy and cultural adaptability of the app's content and promoting the app's acceptability. After the input from the multidisciplinary research group, the app could meet PLWH's personalized needs for symptom management and became a promising tool to promote case management for medical professionals.

One symptom management app for PLWH in the United States of America (mVIP) provides symptom management strategies for 13 symptoms [20]. Our app has a bigger symptom pool (18 symptoms), which may cover more PLWH's symptom issues. Guided by a symptom management framework, the SM app also includes health contents and functions about improving medication adherence and social support. General health

contents are provided for newly registered users and regular users and may improve the quality of life outcome. Particularly, the SM app has several personalized symptom management functions. Firstly, PLWH can assess their symptoms and receive different symptom management strategies according to their assessment results. Secondly, the health tracking module provides PLWH with a convenient tool to track their health indicators. Thirdly, PLWH can communicate with medical staff to gain support through the SM app. These personalized functions can meet personalized needs and may encourage more usage.

Several limitations of this study should be noted. Firstly, the SM app currently only connects with the HIS of the SPHC, and users can only check prescriptions and laboratory tests from SPHC. Secondly, PLWH did not participate in the development process of the app. Future research is needed to examine whether the SM app meets the expectations of PLWH and medical staff and evaluate the app's usability. The app will be revised and updated according to the user feedback. When the SM app is determined to be userfriendly and suitable to be promoted to a larger group of PLWH, its effects on symptom management for PLWH will be tested and open access to HIS in other hospitals.

### **6. Conclusions**

The SM app was developed based on evidence-based resource reviews and the input from our multidisciplinary research team. It provided PLWH with reliable symptom management knowledge and personalized symptom management functions. The web-based administration portal also provided the medical staff with convenient functions for case management. Future studies are needed to further test the app's usability and effectiveness on symptom management. We will refine the SM app based on users' experience and the collected data.

### **7. Patents**

The SM app, which was developed for both iOS and Android, applied for a patent (National Copyright Administration of the People's Republic of China: No.02700189).

**Supplementary Materials:** The following are available online at https://www.mdpi.com/article/10 .3390/jpm11050346/s1, Table S1: Symptom management app content source; Table S2: Scores in terms of evidence-based, situational suitability, practicability, cost-effectiveness, and understandability in the group discussion; Table S3: Assessment tool and cutoff in the symptom management app.

**Author Contributions:** Conceptualization, Y.H.; methodology, Y.H.; software, S.H.; validation, S.H.; formal analysis, R.Z.; investigation, R.Z.; resources, L.Z. and W.S.; data curation, R.Z.; writing– original draft preparation, S.H.; writing–review & editing, Y.P., L.W., X.Q., and B.W.; visualization, S.H.; supervision, Z.Z.; project administration, R.Z. and W.S.; funding acquisition, Y.H. and Z.Z. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by the National Natural Science Foundation of China (Grant Number 71673057) and the China Scholarship Council (No. 201906100135).

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Research Ethical Committee of the School of Nursing, Fudan University (IRB#TYSA2016-3-1) and the Shanghai Public Health Center (SPHC) affiliated with Fudan University (2019-S036-02).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** All the raw data are available in the Supplementary Materials.

**Acknowledgments:** The authors would like to appreciate all the staff who helped us complete this project. They are: Hongzhou Lu, Yinzhong Shen, Renfang Zhang, Jiangrong Wang, the physicians at the Shanghai Public Health Center Affiliated with Fudan University; Meijuan Bao, Lijun Zha, Yanjuan Gan, the nurses at the Shanghai Public Health Center Affiliated with Fudan University; Mingcheng Zhu, software engineer at the Shanghai Public Health Center affiliated with Fudan University.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


### *Article* **Personalized Healthcare: The Importance of Patients' Rights in Clinical Practice from the Perspective of Nursing Students in Poland, Spain and Slovakia—A Cross-Sectional Study**

**Ewa Kupcewicz 1,\* , Elzbieta Grochans ˙ 2 , Helena Kaduˇcáková 3 , Marzena Mikla 4,5, Aleksandra Bentkowska <sup>6</sup> , Adam Kupcewicz <sup>7</sup> , Anna Andruszkiewicz <sup>8</sup> and Marcin Jó´zwik <sup>9</sup>**


**Abstract:** Background: This study aimed to define the role and importance of patients' rights in personalized healthcare from the perspective of nursing students in Poland, Spain and Slovakia. Methods: The research was carried out by means of a diagnostic survey, using the survey technique, with the participation of 1002 nursing students attending a full-time undergraduate study program at three European countries. The "Patients' rights" questionnaire was used as a research tool. The average age of students was 21.6 years (±3.4). The empirical material collected was subjected to a statistical analysis. Results: The study demonstrated that 72.1% of nursing students from Spain, 51.2% from Poland and 38.5% from Slovakia believe that patients' rights are respected at a good level in their country. Significant intergroup differences (F = 67.43; *p* < 0.0001) were observed in the self-assessment of students' knowledge of patients' rights. The highest average values were obtained by students from Spain (3.54 ± 0.92), while 35.9% of students from Slovakia and 25.5% from Poland were quite critical and pointed to their low level of knowledge of patients' rights in their self-assessment. When ranking patients' rights related to respecting dignity, students from Spain obtained much higher average values (4.37 ± 0.92) than students from the other two countries. Conclusions: The level of students' knowledge of patients' rights and the respect for patients' rights by medical personnel is, in the opinion of the respondents, quite diverse and requires in-depth educational activities among nursing students at the university level in respective countries.

**Keywords:** patients' rights; student; nursing; personalized medicine

### **1. Introduction**

Personalized medicine is a model in which disease prevention and treatment is based on the patient's unique clinical, genetic and environmental characteristics [1–3]. Personalized healthcare, providing opportunities for a more precise approach to individual medical

**Citation:** Kupcewicz, E.; Grochans, E.; Kaduˇcáková, H.; Mikla, M.; Bentkowska, A.; Kupcewicz, A.; Andruszkiewicz, A.; Jó´zwik, M. Personalized Healthcare: The Importance of Patients' Rights in Clinical Practice from the Perspective of Nursing Students in Poland, Spain and Slovakia—A Cross-Sectional Study. *J. Pers. Med.* **2021**, *11*, 191. https://doi.org/10.3390/ jpm11030191

Academic Editors: Riitta Suhonen and Ari VanderWalde

Received: 24 January 2021 Accepted: 9 March 2021 Published: 11 March 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

care, is of particular benefit to the patients. It also poses a unique challenge in terms of its holistic approach to health and sickness. This approach assumes that it is a person who should be treated, not just an illness, since a strong link exists among body, soul and mind; they form one entity and only a balance among them can ensure the state of health [4].

Personalized healthcare involves the important issue of patients' rights, which determine the status of the patient during the provision of health services and the obligations of the medical personnel towards the patients as well as towards their relatives [5]. Consequently, the observance of patients' rights by medical personnel in clinical practice is regarded as an ethical obligation and a legal obligation [6]. The concept of patients' rights was developed on the basis of the Universal Declaration of Human Rights adopted in 1948 by the United Nations (UN) General Assembly, which explicitly states that every human being has an inherent right to life, freedom, privacy, free development in society and respect for their dignity [6–8]. The aim of the concept of patients' rights is to protect the autonomy of the patient from interference by others, as well as the right to demand the rightful conditions for the exercise of those rights [6].

According to the World Health Organization (WHO), patients' rights vary from country to country, and it is often the prevailing cultural and social norms that determine the catalogue of patients' rights applicable in a given country [7]. However, there is international consensus that all patients have a fundamental right to privacy, to the confidentiality of their medical data, to consent or refuse treatment and to information about the risks associated with medical procedures [7].

In Europe, the observance of patients' rights is guaranteed, among others, by the Convention on Human Rights and Biomedicine of 1997 (also referred to as the European Bioethics Convention or the Oviedo Convention) [9]. Another document is the European Charter of Patients' Rights, issued in 2002 by the Active Citizenship Network, which governs basic issues concerning patients' rights [10]. The charter mentions, among others, the right of access to health services and the right to respect of patients' time, regardless of the phase or place of treatment, which states that every person has the right to receive the necessary treatment within a swift, predetermined period [10]. Such a guarantee has been introduced in selected European countries, e.g., Sweden, Denmark, Finland, Norway, England, Scotland, Wales, Ireland, Portugal, Spain and the Netherlands [11]. The European Parliament and the Council of the European Union have played a significant role in protecting patients' rights, recognizing that the Member States of the European Union have a responsibility to provide citizens in their territory with safe, efficient, high-quality and quantitatively adequate medical care. The undertaken actions resulted in the introduction of Directive 2011/24/EU of the European Parliament and of the Council of 9 March 2011 on the application of patients' rights in cross-border healthcare [12–16]. As numerous studies have shown, the management of patient care with regard to personal needs, rights and duties requires a certain degree of personalization [17,18]. It is connected with the theoretical and clinical preparation of students of nursing studies for future work related to patient care [19]. Nursing program curricula provide students with the opportunity to achieve learning outcomes in terms of knowledge of human rights, children's rights and patients' rights [19,20]. In the process of socialization under the guidance of academic teachers, nursing students, as future nurses, acquire social competences to be guided in their future work by professional values when making decisions in the face of emerging, healthcare-related ethical challenges [21]. In terms of social competence, a graduate of nursing studies is ready to respect the rights of the patient, to respect the dignity and autonomy of the persons under their care, to be guided by the welfare of the patient and to show understanding for differences in worldview and culture and empathy in relation to the patient and their family [19,20].

The aim of this study was to define the role and importance of patients' rights in personalized healthcare from the perspective of nursing students in Poland, Spain and Slovakia.

The following research problems were formulated:


### **2. Materials and Methods**

### *2.1. Settings and Design*

The study was carried out between May 2018 and April 2019 by means of a diagnostic survey, using the survey technique, with the participation of 1002 nursing students, studying in first degree (bachelor's degree) programs in a full-time system at the University of Warmia and Mazury in Olsztyn and the Pomeranian Medical University in Szczecin (Poland), the University of Murcia in Murcia (Spain) and the Catholic University in Ružomberok (Slovakia). The surveys were carried out at the place where the didactic classes for students were conducted, and the distribution of the prepared sets of paper questionnaires to a given university was handled by one of the researchers. Upon obtaining permission from the academic teacher to conduct the survey, students were informed of the purpose and the scope of the study and provided with instructions on how to complete the questionnaire. Students had the opportunity to ask questions and receive comprehensive explanations. The survey was anonymous and voluntary; the time taken to complete the questionnaires in person was approximately 20 min. The inclusion criterion for the students in the study was the age of the subjects up to 30 years, while the exclusion criterion was the absence of informed consent to participate in the study. Students could also opt-out of the study at any time without providing a reason. In total, 1017 survey forms were distributed among students. After collecting data and eliminating defective questionnaires, 1002 (i.e., 98.5%) correctly completed paper version questionnaires were accepted for the final statistical analysis. The collected data were entered into a spreadsheet in Excel software and the results were analyzed collectively.

### *2.2. Participants*

The investigated group included 404 (40.3%) students from Poland, 208 students (20.8%) from Spain and 390 students (38.9%) from Slovakia. The mean age for all subjects was 21.6 years (±3.4). Among the students, women accounted for 91.3% (*n* = 915), men for 8.7% (*n* = 87). The distribution of first-, second- and third-year students across the universities was similar. The most numerous group were second-year students (*n* = 458; 45.71%), while 329 (32.83%) studied in the first year and 215 (21.46%) in the third year. The age of the students was analyzed in three age groups, assuming the following ranges: ≤20 years (*n* = 401; 40.02%), 21–22 years (*n* = 410; 40.92%) and ≥23 years (*n* = 191; 19.06%). The presented data are part of a larger international project and detailed sociodemographic characteristics are also included in other publications [22,23].

### *2.3. Research Instruments*

A structured survey questionnaire created by the authors, entitled "Patients' Rights", was used to measure the variables of the study. The questionnaire consisted of two parts. The first part contained subjective questions to determine the structure of the surveyed group of students in terms of sociodemographic variables such as place of residence (country), gender, age, level of education and mode and year of studies. These questions included five closed questions, including all possible answer options, and one open question to determine the age of the respondents. The second part of the questionnaire contained 14 questions of an objective or subjective nature, which made it possible to determine the level of students' knowledge of patients' rights and selected aspects related to their observance in personalized healthcare addressed to sick and healthy people. The questions included two so-called "ranking" questions, to self-assess students' level of

knowledge of patients' rights and to prioritize the patient's right to dignity. In the first ranked question, the respondent could choose from a rating scale from 2 to 5, reflecting the level of their current knowledge of patients' rights, where "2" and "3" indicated a low level of knowledge, "4" an average level and "5" a high level. Similarly, in the second question concerning the ranking of the importance of the patient's right to respect for dignity, the respondent indicated on a rating scale from 2 to 5, the rank given to the patients' right, where "2" and "3" indicated a low rank, "4" an average rank and "5" a high rank. In the remaining questions, the respondent was asked to mark one of four or five possible answers for each question.

The process of constructing the applied tool involved the development of a set of statements concerning the studied variables using information retrieved from the literature on the subject. Once the final set of questions in the Polish language was established, it was translated into the Spanish and Slovak languages. The research tool in equivalent language versions was subjected to a psychometric assessment. The reliability of the questionnaire was assessed through the internal consistency estimation, which was established based on Cronbach's alpha coefficients. When estimating the internal consistency degree, two of the questions from the second part of the questionnaire were rejected due to only slight thematic coherence. The reliability of all the other questions, measured by the value of the Cronbach's alpha coefficient, ranged from 0.60 to 0.71 [24].

### *2.4. Statistical Analysis*

Statistical analyses were performed using the Polish version of STATISTICA 13 (TIBCO, Palo Alto, CA, USA). The mean, standard deviation and confidence interval for the mean ±95%, median, minimum and maximum were used to describe some of the analyzed variables. The ANOVA analysis of variance (F-test) comparing multiple samples of independent groups was used to investigate the significance of differences in the ranking of the subjective assessment of students' level of knowledge and in the ranking of the patients' right to respect for dignity. The significance of variation in the knowledge of patients' rights was assessed with the chi-square test (χ 2 ). For all tests, a significance level of *p* < 0.05 was assumed. The analyses of the results are presented in descriptive, tabular and graphical forms [24]. The research meets the criteria for a cross-sectional study [25].

### **3. Results**

Students participating in the survey were given the opportunity to express their opinion on selected patients' rights in personalized healthcare based on their own experience of staying in a healthcare facility as a patient and as a nursing student, deepening their knowledge during clinical activities. The majority of nursing students (79.8%; *n* = 800) had used medical services as a patient in a hospital or clinic/outpatient clinic in the last three years preceding the survey. Their level of satisfaction with the quality of the medical services provided at that time significantly varied (χ <sup>2</sup> = 45.53; *p <* 0.0001). The majority of students expressed a positive opinion on the overall quality of the medical services provided. However, only 33.9% of respondents reported that they had been informed about their rights and that information about patients' rights and the Patient Ombudsman was posted in a publicly accessible place. Taking into account the cultural background and the organization of the healthcare system in the different countries, a significant variation in results was observed (χ <sup>2</sup> = 124.26; *p <* 0.0001) as regards the provision of information to patients concerning their rights. As analyses show, significantly more respondents in Poland (62.4%) than in Slovakia (37.7%) and Spain (16.5%) were informed about their rights when using medical services. When assessing the observance of patients' rights in personalized medical care, the results of the answers to the question concerning the provision of a sufficient level of intimacy to the patient during the provision of medical services were also sought. As indicated by the data, 60.5% of respondents confirmed that they were ensured good conditions when receiving medical services that minimized the feeling of embarrassment and reduced privacy.

### *3.1. Observance of Patients' Rights in Personalized Healthcare as Perceived by Nursing Students*

In the opinion of nursing students, respect for the patients' right to receive comprehensive information about their own health condition and planned medical treatment in personalized healthcare significantly varied (χ <sup>2</sup> = 315.61; *p <* 0.0001) in the analyzed subgroups. A high percentage (92.8%) of nursing students from Spain indicated that the right in question is respected in their country. However, around half of the respondents (51%) in the Slovak group and only 28.5% in the Polish group were of the same opinion. Further analysis involving the issue of compliance with the patients' right to receive pastoral care during the hospital stay showed statistically significant differences (χ <sup>2</sup> = 122.24; *p <* 0.0001). More than half of the respondents confirmed this possibility and one in three Spanish students had no opinion about it, while in the Polish group 16.6% (*n* = 67) and in the Slovak group 13.6% (*n* = 68) of nursing students declared that they had no knowledge about it (Table 1).



Obligation to provide the pa-


**Table 1.** *Cont.* No 30 (7.4) 18 (8.7) 53 (13.6)

Never 40 (9.9) 10 (4.8) 26 (6.7)

of the court 80 (19.8) 37 (17.8) 95 (24.4)

Yes 289 (71.5) 156 (75.0) 264 (67.7)

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 6 of 14

could contribute to a risk to the health and life of others

At the request

Explanations: \* *p* < 0.05; \*\* *p* < 0.01; \*\*\* *p* < 0.001. Explanations: \* *p* < 0.05; \*\* *p* < 0.01; \*\*\* *p* < 0.001.

In the following analyses, an attempt was made to find a subjective assessment by the nursing students concerning the extent to which patients' rights were respected in healthcare facilities in Poland, Spain and Slovakia. The distribution of the results was significantly different (χ <sup>2</sup> = 75.26; *p <* 0.0001). It was found that 72.1% of nursing students from Spain, 51.2% from Poland and 38.5% of students from Slovakia rated the respect of patients' rights as good (Figure 1). On the other hand, one in five students from the Slovak group (20.8%) also indicated a disadvantageous situation for the patient, indicating that the level of respect for patients' rights was rather low or definitely low (Figure 1). In the following analyses, an attempt was made to find a subjective assessment by the nursing students concerning the extent to which patients' rights were respected in healthcare facilities in Poland, Spain and Slovakia. The distribution of the results was significantly different (χ2 = 75.26; *p <* 0.0001). It was found that 72.1% of nursing students from Spain, 51.2% from Poland and 38.5% of students from Slovakia rated the respect of patients' rights as good (Figure 1). On the other hand, one in five students from the Slovak group (20.8%) also indicated a disadvantageous situation for the patient, indicating that the level of respect for patients' rights was rather low or definitely low (Figure 1).

**Figure 1.** Observance of patients' rights as perceived by nursing students.

### *3.2. Differences in Nursing Students' Knowledge of Selected Patients' Rights in Personalized Healthcare*

Further analyses involved investigating students' knowledge of a patients' rights in personalized healthcare to deposit valuable items to a hospital depository during inpatient treatment in a healthcare facility. The analysis demonstrated statistically significant differences (χ <sup>2</sup> = 121.64; *p <* 0.0001). It was found that the vast majority of Slovak students

(91.3%; *n* = 356) positively responded to the question of whether a patient in healthcare facilities has the right to use a depository for the period of hospitalization. One of the most important patients' rights in personalized healthcare concerns the confidentiality of patient-related information. The data obtained show that 86.5% (*n* = 867) of nursing students confirm that the patient has the right to data protection and confidentiality concerning the information on the patient by the medical staff. This means that all information about the patient's health condition, the diagnostic, therapeutic, rehabilitation and nursing activities carried out and any other information obtained in connection with the exercise of the medical profession must not be disclosed to any unauthorized persons and should be treated as confidential. The data in Table 1 allow us to conclude that there is a statistically significant variation in the results among students across countries (χ <sup>2</sup> = 66.13; *p <* 0.0001) in terms of knowledge of the patients' right to the confidentiality of information. A higher percentage of students from Slovakia (91.3%; *n* = 356) than students from Spain (79.3%; *n* = 165) indicated their knowledge of this right. In certain situations, medical practitioners are obliged to disclose information covered by professional secrecy. It was found that more than half of the nursing students (54.5%; *n* = 546) felt that medical staff could be exempted from professional confidentiality if the information covered could contribute to a risk to the health and life of others. The analysis of opinions concerning the issuance of copies of inpatient/ambulatory treatment records by the medical facility to the patient demonstrated statistically significant differences (χ <sup>2</sup> = 51.14; *p <* 0.0001). It was found (Table 1) that 75% of the students (*n* = 156) from Spain confirmed that a medical facility is obliged to provide the patient with the records of inpatient or outpatient treatment, while a slightly lower percentage of students from Poland (71.5%; *n* = 289) and Slovakia (67.7%; *n* = 264) were of the same opinion. The situation was slightly different as regards knowledge declared by the students of the patient's right to be discharged from a hospital at their own request. The data presented show significant variation in responses among students (χ <sup>2</sup> = 86.00; *p* < 0.0001). The vast majority of respondents from Poland (79.5%; *n* = 321) and Slovakia (75.9%; *n* = 296) stated that a patient has the right to be discharged from hospital on their own request. In contrast, a significant proportion (35.1%; *n* = 73) of Spanish students stated that a patient can only be discharged upon their own request from a hospital if their life is not in danger. Patients' rights also include the right to withdraw their objection to the donation of organs and tissues. Data analysis (Table 1) showed significant differences among nursing students (χ <sup>2</sup> = 15.17; *p <* 0.004); the vast majority of students (72.1%; *n* = 150) from Spain confirmed the patient's right to withdraw their objection to organ and tissue donation, while 29.5% (*n* = 115) of students from Slovakia, 27.0% (*n* = 109) from Poland and 17.3% (*n* = 36) from Spain stated that they had no knowledge of this issue.

In the course of the study, students were asked to make a subjective assessment of their level of knowledge in the field of patients' rights, using a rating scale from 2 to 5. In a statistical analysis, significant differences in the level of knowledge (F = 67.43; *p <* 0.0001) were observed between students from Poland, Spain and Slovakia. The highest mean values were obtained by students from Spain (3.54 ± 0.92), while significantly lower scores were found for students from Poland (3.00 ± 0.73) and Slovakia (Table 2).

**Table 2.** Variation in students' self-assessed knowledge of patients' rights.


Explanations: \* *p <* 0.05; \*\* *p <* 0.01; \*\*\* *p* < 0.001. *n*, subgroup size; M, arithmetic mean; SD, standard deviation; Me, median; Min., minimum; Max, maximum; 95% CI, confidence interval.

**Variables** 

Self-assessment of students' knowledge of patients' rights (rating

> After establishing low, average and high scores, special attention was paid to the proportion of the surveyed students who rated their competence in the area of patients' rights as low. As it turned out, as many as 35.9% of students from Slovakia, 26.5% from Poland and 14.9% from Spain were quite critical and indicated in the self-assessment a low level of knowledge of patients' rights (Figure 2). After establishing low, average and high scores, special attention was paid to the proportion of the surveyed students who rated their competence in the area of patients' rights as low. As it turned out, as many as 35.9% of students from Slovakia, 26.5% from Poland and 14.9% from Spain were quite critical and indicated in the self-assessment a low level of knowledge of patients' rights (Figure 2).

**Slovakia**  *n* **= 390 (38.9%)** 

**M ± SD, Me, Min.–Max., 95% CI** 

2.79 ± 0.69, 3.00, 2.00–5.00, 2.72 ± 2.86

**ANOVA** 

**(F)** *p* **Value** 

F = 67.43 0.0001 \*\*\*

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 8 of 14

**Table 2.** Variation in students' self-assessed knowledge of patients' rights.

**Country of Origin** 

**Spain**  *n* **= 208 (20.8%)** 

**M ± SD, Me, Min.–Max., 95% CI** 

3.54 ± 0.92, 4.00, 2.00–5.00, 3.42 ± 3.67

Explanations*:* \* *p <* 0.05; \*\* *p <* 0.01; \*\*\* *p < 0.001. n*, subgroup size; M, arithmetic mean; SD, standard deviation; Me, median;

**Poland**  *n* **= 404 (40.3%)** 

**M ± SD, Me, Min.–Max., 95% CI** 

3.00 ± 0.73, 3.00, 2.00–5.00, 2.93 ± 3.07

Min., minimum; Max, maximum; 95% CI, confidence interval.

**Figure 2.** Self-assessment of the level of the students' knowledge of patients' rights—distribution of answers. **Figure 2.** Self-assessment of the level of the students' knowledge of patients' rights—distribution of answers.

Subsequent analyses reported statistically significant differences (F = 3.44; *p <* 0.03) in self-reported knowledge of patients' rights among the age groups of Slovak students. It was proven that students aged 23 years and older received significantly higher mean values in the assessment (3.0 ± 0.68) than students in the ≤20 years age group (2.7 ± 0.67). This is probably linked to the implementation of educational content on the topic of patients' rights in classes in subsequent years. However, no statistically significant differences in self-assessed knowledge were found among Polish and Spanish students (F = 0.11; *p <* 0.89 vs. F = 0.18; *p <* 0.83) in the respective age groups. Analyses demonstrated that, in the Spanish group, the year of study significantly determined the level of students' knowledge of patients' rights (F = 14.68; *p <* 0.0001). Second-year students received higher Subsequent analyses reported statistically significant differences (F = 3.44; *p <* 0.03) in self-reported knowledge of patients' rights among the age groups of Slovak students. It was proven that students aged 23 years and older received significantly higher mean values in the assessment (3.0 ± 0.68) than students in the ≤20 years age group (2.7 ± 0.67). This is probably linked to the implementation of educational content on the topic of patients' rights in classes in subsequent years. However, no statistically significant differences in self-assessed knowledge were found among Polish and Spanish students (F = 0.11; *p <* 0.89 vs. F = 0.18; *p <* 0.83) in the respective age groups. Analyses demonstrated that, in the Spanish group, the year of study significantly determined the level of students' knowledge of patients' rights (F = 14.68; *p <* 0.0001). Second-year students received higher mean values in the self-assessment (3.8 ± 0.85) than first-year students. Taking into account the year of study in the analyses, no significant differences in self-assessed knowledge of patients' rights were found among students from Poland (F = 0.16; *p <* 0.85) and Slovakia (F = 0.81; *p <* 0.44).

### *3.3. Assessing the Importance of the Patient's Right to Dignity in Personalized Healthcare*

In further analyses, an attempt was made to rank, in the opinion of nursing students, the importance of the patient's right to respect their dignity, since the care of people in health and illness should always be based on respect for their dignity, subjectivity and ensuring intimacy when health services are provided by medical personnel. The right to respect for dignity also includes the right to die in peace. When asked what rank on a 2–5 rating scale the students would give to the patients' right to dignity, significantly different results (F = 133.56; *p <* 0.0001) were obtained, depending on the surveyed students' country of origin (Table 3).


**Table 3.** Patients' right to dignity—comparison of rankings.

Explanations: \* *p* < 0.05; \*\* *p* < 0.01; \*\*\* *p* < 0.001. *n*, subgroup size; M, arithmetic mean; SD, standard deviation; Me, median; Min., minimum; Max., maximum; 95% CI—confidence interval.

> The analyses showed that Spanish students obtained significantly higher mean values (4.37 ± 0.92) in the ranking of the patient's right to dignity than students from the other two countries. Subsequent analyses explored the influence of selected sociodemographic characteristics such as age and year of study within the country on the ratings indicated by students regarding the patient's right to dignity. The analysis found no statistically significant differences in the rank given to the patient's right to dignity across age groups in any of the analyzed countries. However, in Spain, the year of study was found to significantly (F = 3.72; *p <* 0.03) influence the level of students' ranking of the patient's right to dignity. Spanish first-year students gave a significantly higher ranking to the patient's right to dignity (4.6 ± 0.73) than third-year students (4.1 ± 1.08; *p <* 0.02). In contrast, there were no statistically significant differences in the ranking given to the patient's right in students from different years of study in Poland and Slovakia. Therefore, it may be concluded that the results of the studies conducted in Poland, Spain and Slovakia confirm the differences in the knowledge of patients' rights among nursing students, but they require further scientific consideration.

### **4. Discussion**

We attempted to determine the role and importance of patients' rights in personalized healthcare from the perspective of nursing students in Poland, Spain and Slovakia. It was recognized that the individualized nature of medical services involves respecting the rights of the patient, which protect the patient's autonomy (freedom) from interference by other parties and provides the basis for claiming the legitimate conditions for the exercise of those rights. According to the procedures applicable in a given healthcare facility, the patient should be informed of their rights, which should be recorded in an understandable and legible manner and available in the patients' areas.

The results of the authors' own research show that only one-third of the respondents were informed about their rights before admission to hospital or during the provision of health services and that the information on patients' rights and the Patients' Ombudsman was posted in a publicly accessible place. The analyses of research results obtained by many other authors quite often reveal an unfavorable situation of the patient concerning their rights in various medical entities operating in the medical services market. For example, a study conducted by Ansari et al. among 500 Iranian patients in inpatient and outpatient care found that 93.5% of them did not receive any information on patients' rights [26]. Moreover, a study conducted by Egyptian researchers on a group of 514 patients hospitalized at the Minia University Hospital found that about 76% of patients did not know about the existence of the patients' rights charter and 98.1% of those surveyed said that the medical team did not inform them of the treatment options available [27]. This means that healthcare providers should place greater emphasis on raising patients' awareness of their rights and involving them in decisions about their treatment choices. Abedi et al. also indicated the need to increase patients' awareness of their rights during the

delivery of healthcare services [28]. As stated by Agrawal et al., to take effective educational measures to improve general awareness not only among patients but also among various stakeholders in the healthcare system, it is important to assess the awareness of hospitalized patients of their rights [29]. As shown by the results of a study conducted by Tabassum et al. in two hospitals in Lahore (Pakistan) from the public and the private sectors, most patients (64%) were not aware of their rights. However, the level of awareness of patients' rights was higher in patients receiving medical care in a private hospital than in a public hospital [30]. It is also worth referring to the findings of Mohammadi et al. who, in their study, indicated the need to inform patients about ethical and legal issues related to privacy and confidentiality, before and during admission to hospital [31].

As shown by an analysis of the authors' own study results, significantly more patients in Poland (62.4%) than in Slovakia (37.7%) or Spain (16.5%) were informed about their rights. Other researchers have also attempted to assess existing barriers to compliance with patients' rights on the basis of a meta-analysis. The most important factors cited as obstacles to respecting patients' rights included, among others: excessive workload of nurses, staff shortage, organizational factors and a lack of awareness of the patients' rights charter among patients, nurses, doctors and students [32]. In the current study, the degree of observing patients' rights in healthcare institutions in the opinion of nursing students in Poland, Spain and Slovakia is significantly different. Almost 75% of Spanish students rated the level of observing patients' rights in their country as good. The respect for patients' rights in Polish and Slovak healthcare institutions was rated much lower by the students. Undoubtedly, there is a need to search for subjective and objective factors affecting the level of respecting patients' rights in medical facilities.

Interesting results were also presented by Mousavi et al. who showed that the rights of patients admitted to the Intensive Care Unit are more affected than those of patients admitted to other hospital wards. They pointed to inadequate nurse-to-patient ratios, socio-economic problems, working hours and high workload in a limited time as the main factors affecting the quality of nursing practice in terms of respecting patients' rights, among others [33]. In contrast, Waddington and Mesherry raise the important issue of informed consent for the treatment of people with psychosocial disabilities in Europe [34]. In other studies conducted by Sabzevari et al. among medical staff of the hospitals affiliated with the Mashhad University of Medical Sciences, the highest level of respect for patients' rights was found in the area of respect for patients' privacy and confidentiality, which was assessed as excellent by all respondents (100%). The lowest value of compliance with patients' rights was associated with the presentation of adequate and appropriate information addressed to patients, which was rated excellent by 48.1% respondents [35].

Human dignity and subjectivity require that medical personnel observe the highest standards of ethical conduct and respect the intimacy of the patient. In the authors' own study, Spanish nursing students ranked the patient's right to respect for dignity with the highest mean values, demonstrating the importance of this right in personalized medical care.

Of all the staff caring for patients, it is nurses who spend the most time with the patients, see their behavior and recognize their needs. Thus, the quality of nursing care depends on the knowledge and experience of nurses. As Sheikhtaheri et al. proved in their study on a group of Iranian nurses, the mean score of nurses' knowledge of patients' rights was acceptable, while more experienced and educated nurses showed more knowledge about patients' rights. However, compliance with patients' rights by the nurses involved in the study was questionable [36]. In the current study, the level of nursing students' knowledge of patients' rights significantly varied. The highest average values were obtained by students from Spain, while the most critical in self-evaluation were those from Slovakia.

An attempt to determine the extent to which doctors and nurses in Oman were aware of the importance of patients' rights and their observance was undertaken by Al-Saadi et al. Their research showed that overall awareness of the importance of patients' rights

among medical staff was high (91.5%), although compliance with these rights in practice was much lower (63.8%) [37].

Nurses often take on the role of the patient's spokesperson, yet daily nursing practice also includes certain shortcomings with regard to respecting patients' rights [38]. During their studies, nursing students acquire knowledge, clinical skills and social competences in order to fulfill their duties towards patients and their families with due diligence in their professional work.

Aydin Er et al. presented the results of a study involving 238 nursing students from the West Black Sea Universities in Turkey in which the majority of the nursing students held desirable attitudes toward patient information, truth-telling and protection of patients' privacy and medical records. The authors proposed that ethics education, covering both patient's rights and the obligations of nurses to defend these rights, be introduced to the study curriculum [39]. Based on a review of the literature on the topic, genuine contacts of nursing students with patients during clinical classes are of key importance in the development of the skills necessary for students working with patients. The concept of learning from patients has emerged recently, thus transferring the emphasis of learning from professionals as the example to follow to relations created between the student and the patient [40]. This development is particularly important in the domain of social competences, where nursing students should always see to the patient's welfare, respect patient's dignity and autonomy, display understanding for ideological and cultural differences and respond with empathy in contacts with patients and their families [20].

As indicated by Kim, in order for future nurses to be well prepared for their professional roles, it is desirable to revise the curriculum in the nursing program to strengthen interpersonal care behaviors, biomedical ethics and students' sensitivity to human rights [41]. Moreover, mentors involved in clinical nursing education are expected to provide the optimal educational environment for achieving and demonstrating the desired level of competence in conjunction with professional ethics and patients' rights [42]. Finally, it should be added that modern nursing entails an ethical responsibility to respect and protect patients' rights. The presented results of the authors' own research reflect a certain fragment of reality and provide a contribution to further scientific investigations.

### **5. Limitations and Implications for Professional Practice**

The results of this study help to outline implications for professional practice. Firstly, they point to a need to analyze study programs in conjunction with assessing the effectiveness of clinical teaching in the nursing program, with particular emphasis on the courses that involve learning outcomes related to professional ethics and patients' rights. Secondly, there is a need to disseminate the information on patients' rights among the population in a given country. Thirdly, medical practitioners, as part of their postgraduate training, should deepen their knowledge, improve their professional skills and develop their social skills throughout their careers. This will ensure a sufficiently high level of medical care for the patient, which will translate into therapeutic safety and patient satisfaction with the medical services provided. The presented study is the first one of this type conducted on the international scale in selected European countries, i.e., Poland, Spain and Slovakia, but it has its limitations, such as the size of the surveyed group, and needs to be replicated with a larger number of respondents.

### **6. Conclusions**


**Author Contributions:** Conceptualization, E.K. and A.B.; methodology, E.K., M.J. and E.G.; software, E.K.; validation, E.K., H.K. and M.M.; formal analysis, E.K.; investigation, E.K.; resources, E.K. and A.K.; data curation, E.K.; writing—original draft preparation, E.K.; writing—review and editing, E.K. and E.G.; visualization, E.K.; supervision, E.K. and A.A.; project administration, E.K. and A.K.; funding acquisition, E.K. All authors have read and agreed to the published version of the manuscript.

**Funding:** This work was a part of a research project, financed by the University of Warmia and Mazury in Olsztyn (No 63-610-001), Poland.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Senate Committee on Ethics of Scientific Research at the Higher School in Olsztyn, Poland. (protocol code No. 4/2020, on 12.03.2020).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** The data presented in this study are available on request from the corresponding author.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


### *Article* **Maternal Psychological and Biological Factors Associated to Gestational Complications**

**David Ramiro-Cortijo 1,2,† , Maria de la Calle 3,†, Vanesa Benitez <sup>4</sup> , Andrea Gila-Diaz 2,5 , Bernardo Moreno-Jiménez <sup>6</sup> , Silvia M. Arribas 2,\* and Eva Garrosa 6,\***


**Abstract:** Early detection of gestational complications is a priority in obstetrics. In our social context, this is linked to maternity age. Most studies are focused on biological factors. However, pregnancy is also influenced by social and psychological factors, which have not been deeply explored. We aimed to identify biopsychosocial risk and protective factors associated with the development of maternal and fetal complications. We enrolled 182 healthy pregnant women, and plasma melatonin and cortisol levels were measured in the first trimester by chemiluminescent immunoassays. At different time points along gestation, women answered several questionnaires (positive and negative affect schedule, hospital anxiety and depression scale, pregnancy concerns scale, life orientation test, resilience scale, life satisfaction scale and life–work conflicts scale). They were followed up until delivery and categorized as normal pregnancy, maternal or fetal complications. Maternal complications were associated with low melatonin (OR = 0.99 [0.98; 1.00]; *p*-value = 0.08) and life satisfaction (OR = 0.64 [0.41; 0.93]; *p*-value = 0.03) and fetal complications were associated with high cortisol (OR = 1.06 [1.02; 1.13]; *p*-value = 0.04), anxiety (OR = 2.21 [1.10; 4.55]; *p*-value = 0.03) and life–work conflicts (OR = 1.92 [1.04; 3.75]; *p*-value = 0.05). We conclude that psychological factors influence pregnancy outcomes in association with melatonin and cortisol alterations. High maternal melatonin and life satisfaction levels could be potential protective factors against the development of maternal complications during pregnancy. Low anxiety and cortisol levels and reduced work–life conflicts could prevent fetal complications.

**Keywords:** anxiety; life satisfaction; life–work concerns; melatonin; cortisol; biopsychosocial model; obstetric complications

### **1. Introduction**

Maternity is highly influenced by social factors, including education, economic or racial aspects. In industrialized societies, a key social determinant is the delay of maternity age [1], related to the gradual access of the women to higher education, employment and pregnancy control. The use of assisted reproduction techniques (ART) has made possible maternity beyond biological limits [2]. Pregnancy at an age over the optimum childbearing age has biological consequences, including higher rate of pregnancy complications and

**Citation:** Ramiro-Cortijo, D.; de la Calle, M.; Benitez, V.; Gila-Diaz, A.; Moreno-Jiménez, B.; Arribas, S.M.; Garrosa, E. Maternal Psychological and Biological Factors Associated to Gestational Complications. *J. Pers. Med.* **2021**, *11*, 183. https://doi.org/ 10.3390/jpm11030183

Academic Editors: Riitta Suhonen, Minna Stolt and David Edvardsson

Received: 17 January 2021 Accepted: 2 March 2021 Published: 5 March 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

infertility. In addition, the use of ART increases the rates of multiple pregnancies [3], which are also a risk factor for complications, including preterm delivery (labor before 37 weeks of gestation) and fetal growth restriction (FGR) [4].

Almost 17% of pregnant women experience some type of pregnancy complication, which affects maternal and infant's health [5]. Detecting women at risk as early as possible is a priority in obstetrics. Despite intensive research, there are still unknown causes that increase the risk of pregnancy complications. The majority of studies have focused on biological factors, some of which have been identified. However, pregnancy is influenced not only by biological determinants, but also by other factors. The biopsychosocial approach is ingrained in the "general systems theory", which states that a system is characterized by the complex interactions of its components [6]. In the obstetric field, there is a psychological and social domain that should be incorporated into clinical practice to improve healthcare. Therefore, insight into pregnancy complications should be approached from a biopsychosocial point of view.

The psychological sphere likely exerts an important influence on pregnancy. Getting pregnant at an advanced age, the need of ART and a multiple pregnancy represent important stress factors which may negatively influence pregnancy outcome. There is evidence that individuals under high stress take poorer care of themselves and are more likely to engage in health-impairing behaviors, which may affect maternofetal health [7,8]. The importance of psychological factors on maternal health also is evidenced by the fact that antenatal optimism is the most protective factor against maternal postnatal adverse outcomes, e.g., depression or other mood disorders [9]. Maternal psychological factors may also influence long-term offspring health. For example, psychological stress in pregnancy, specifically in early stages, has been associated with higher risk of mental disorders in the offspring [10]. Life concerns, anxiety or problems in concealing work and personal life exert an influence on the biological environment of pregnant mothers and could be the link between psychological responses and negative influences on maternofetal health.

The interaction between psychological and biological factors and their impact on pregnancy outcomes have not been sufficiently explored [8]. Melatonin and cortisol are important hormones in gestation and can be potential biological factors implicated in this relationship. Melatonin is synthesized by the pineal gland with a peak at night [11], and during pregnancy it is also produced by the placenta [12]. Melatonin is a key hormone for pregnancy maintenance due to its pleiotropic roles [13], including its remarkable effects as an antioxidant [14]. We have evidence that, in the first trimester of pregnancy, a poor antioxidant status is linked with the development of pregnancy complications, and melatonin is an important contributor protecting against oxidative damage [3]. Our data indicate that maternal plasma melatonin is lower in women with preterm birth [15]. Daytime melatonin levels have been demonstrated to be influenced by anxiety and depression [16], perhaps due to the reduction in the number of sleep hours, which are directly proportional to melatonin circulating levels [17]. Therefore, it is possible that the dysregulation of this hormone under stressful conditions will influence pregnancy outcome.

Cortisol is another important hormone that may influence pregnancy outcome. Cortisol is synthesized by the hypothalamus–pituitary–adrenal axis and has cell catabolic and immune system suppression effects [18]. Cortisol secretion is closely linked to stress conditions, and it has been related to maternal mood, showing associations with psychological stress [19] and anxiety [20]. The maternal psychological stress and the associated increase in cortisol levels have been linked with adverse neonatal outcomes [21]. In this sense, we have evidence from twin pregnancies that the levels of maternal cortisol in early pregnancy are negatively associated with birth weight [15].

We hypothesize that social and psychological spheres exert an impact on obstetric outcome, influencing biological factors. We aimed to identify biopsychosocial risk and protective factors associated with the development of maternal and fetal complications in our social context, characterized by an advanced maternity age. We also explored the relationship between psychological variables and melatonin and cortisol, key hormones implicated in pregnancy and stress.

### **2. Materials and Methods**

### *2.1. Cohort Selection*

This is a retrospective, non-interventional and observational study from the Hospital Universitario La Paz (HULP, Madrid, Spain). Pregnant women were enrolled at 8 weeks of gestation at Obstetrics and Gynecology service. Women were first informed about the study proposal, and those who accepted anonymously and voluntarily to participate in the study signed a consent. The exclusion criterion was women who had previous diseases (hypertension, obesity, diabetes mellitus, inflammatory or immune deficiency diseases or record of previous pregnancy complications). The inclusion criterion was good comprehension of the Spanish language. Finally, 182 healthy pregnant women were enrolled. The study flow-chart is shown in Figure 1.

**Figure 1.** Flow-chart of study participants. Exclusion criteria: chronic maternal disease (i.e., hypertension, obesity, diabetes mellitus, inflammatory or immune deficiency diseases previous pregnancy) and diagnoses of obstetrical complications before. Sample size (*n*) is shown between brackets.

This study was performed in accordance with the Declaration of Helsinki regarding studies in human subjects and it was approved by HULP and Universidad Autónoma de Madrid Ethical Committees (PI-1490 and CEMU/2013-10, respectively).

### *2.2. Maternal and Neonatal Data Collection and Group Classification*

Maternal and neonatal data were collected from the medical record. Maternal data collected were maternal age (years), civil status (single/married), educational level (undergraduate/university degree), employment situation (working/unemployment, of herself and, in the case of having a partner, also of the partner), family core-economic income (euros/month), smoking habits (yes/no) and alcohol intake during pregnancy (yes/no), gestational age (weeks of gestation), twin gestation (binary variable) and assisted reproduction techniques (ART, binary variable). In addition, obstetric adverse outcomes (diagnosed by the obstetrician staff based on hospital guidelines) were also recorded and included: *hyperemesis gravidarum* (defined as more than 3 episodes of vomiting/day, weight loss of 5% and ketones in the urine), pregnancy-induced hypertension (defined as blood pressure ≥ 140/110 mmHg without preeclampsia alterations before 20 weeks of gestation), gestational diabetes mellitus (defined as blood glucose levels > 140 mg/dL in the glucose tolerance test), preeclampsia (defined as pregnancy-induced hypertension and

protein in the urine), pregnancy anemia (defined as hemoglobin < 11 g/dL in the first trimester or < 10.5 g/dL in the second or third trimester) and intrahepatic cholestasis of pregnancy (defined as pruritus and alterations in the blood/liver function tests including serum bile acids levels). Women who developed any of these complications during pregnancy were included in the "maternal complications" group.

Neonatal data recorded were infant sex and the following fetal adverse clinical outcome: any alterations in the physiologic systems reported by echography during pregnancy follow-up, FGR (defined as intrauterine growth below the third percentile or below the tenth percentile with hemodynamic alterations by Doppler echography; binary variable) and preterm labor (defined as gestational age low than 37 weeks; binary variable). Pregnancies with any of these fetal outcomes were included in the "fetal complications" group.

### *2.3. Maternal Plasma Variables in the First Trimester*

At 9–11 weeks of gestation, blood samples were extracted from 8:00 to 9:00 am, by venipuncture in Vacutainer® lithium heparin gel tubes for plasma separation (Becton Dickinson comp., Madrid; Spain), following the protocols established by the medical staff. Plasma was obtained by centrifugation (2100× *g*, 15 min at 4 ◦C), within a maximum of 2 h after extraction and stored at −80 ◦C to assay melatonin and cortisol.

To determine melatonin levels, plasma was evaporated to dryness with an evaporator centrifuge (Speed Vac SC 200; Savant; Hyannis, MA, USA). The residues were dissolved in distilled water and melatonin levels were determined by a competitive enzyme immunoassay kit (Melatonin ELISA; IBL International, Hamburg; Germany) according to the manufacturer's instructions. The kit is characterized by an analytical sensitivity of 1.6 pg/mL and high analytical specificity (low cross-reactivity). Melatonin was expressed as pg/mL. This method was extensively described in Aguilera et al. [22].

To assess plasma cortisol, a competitive immunoassay using direct chemiluminescent technology was used, being analyzed with an Advia Centaur instrument (Siemens Healthineers, Madrid; Spain). Cortisol was expressed as µg/dL.

### *2.4. Maternal Psychological Variables during Pregnancy*

Women answered psychological applications in each trimester of pregnancy at Weeks 9–11 (first trimester), 24–25 (second trimester) and 36 (third trimester), during a programmed visit to the hospital. Missing data referred to women with miscarriage, preterm delivery or follow-up loss, coinciding with the visit of pregnant women to the hospital. Psychological applications are described below:

*Positive and Negative Affect Schedule* [23], Spanish version [24]. This standardized application scores the positive and negative affectivity using 20 items with a Likert answer of 5 points ranging from "nothing" (1) to "extremely" (5). Some of the positive items were "active" or "strong" and some of the negative items were "restless" or "distressed".

*Hospital Anxiety and Depression Scale* [25], Spanish version [26]. This standardized application scores the anxiety using a questionnaire with seven items with a Likert answer of 4 points ranging from "no anxiety" (0) to "high anxiety" (3).

*Pregnancy concerns scale*. It is an ad-hoc scale, which was elaborated according to the recommended phases for the creation of psychological scales [27] and was previously used by our research group [28]. This scale evaluates personal concerns about gestation worries. It is a scale with 10 items with a Likert answer of 4 points ranging from "none" (0) to "many" (3). Some items were "the health of my newborn" or "the effect of the drugs on the fetus".

*Life Orientation Test* [29], Spanish version [30]. This application scores personal optimism. We used a short scale of five items with a Likert answer of 5 points ranging from "completely agree" (1, low optimism) to "completely disagree" (5, high optimism). Some examples of the items are "I am always optimistic about my future" and "I usually think the things are not going right".

*Resilience scale* [31], Spanish version [32]. This application scores the ability to cope with daily difficulties/problems. We used a short scale of six items with a Likert answer of 7 points ranging from "completely disagree" (1, low resiliency) to "completely agree" (7, high resiliency). Some items in the scale were "In any situation, I can be efficient" and "When I believe in myself, I can go through difficult times".

*Life Satisfaction scale* [33], Spanish pregnancy version [34]. This application scores subjective satisfaction with your own life. The scale has five items with a Likert answer of 5 points ranging from "completely disagree" (1, low life satisfaction) to "completely agree" (7, high life satisfaction). Some items in the scale were "In general, my real life is close to my ideal life" or "If I were born again, I don't think I'd change anything in my life".

*Life–work conflicts scale*. It is an ad-hoc scale, which was elaborated according to the phases for the construction of psychological scales [27] and was previously used by our research group [28]. This application scores the association between work and family life difficulties. It is a scale with six items with a Likert answer of 4 points ranging from "never" (0, minimum conflicts) to "always" (3, maximum conflicts). Some items were "I am irritable at home because my work is exhausting" and "I have to cancel plans with my partner/family/friends due to work commitments".

The points of data collection and reliability of psychological applications are summarized in Table 1.


**Table 1.** Timing for data collection and reliability of the psychological application.

First trimester (1T), second trimester (2T) and third trimester (3T) of pregnancy. Cronbach's α was used to assess the reliability of psychological applications in this study.

### *2.5. Statistical Analysis*

Statistical analysis was performed using R software (version 3.6.0, R Core Team, 2018, Vienna; Austria) within R Studio interface, using MASS, pscl, oddsratio, ggplot2, ggpubr and cowplot packages. Continuous variables were expressed as median and interquartile range (IQR) and qualitative variables as relative frequency. The univariate analysis for the maternal characteristics, plasma and psychological variables were compared using the Mann–Whitney test. The correlation between hormonal levels and psychological factors was analyzed by the rho-Spearmen test. The association between quantitative variables was assessed by the Chi-squared test. Those variables that showed a *p*-value < 0.10 in the univariate analysis were considered as modulatory variables in the regression models. This criterion was proved as the most parsimonious analysis in the models [35].

Regression models were created through stepwise procedures to estimate the major contribution of maternal/neonatal characteristics, maternal plasma and psychological variables to maternal and fetal complications. We conducted a stepwise analysis of potential confounders in five sequential categories: (1) maternal characteristics: maternal age, gestational age, twin gestation, ART, infant sex, FGR and preterm labor; (2) maternal plasma variables at first trimester: melatonin and cortisol; (3) psychological variables at first trimester; (4) psychological variables at second trimester; and (5) psychological variables at third trimester. The regression models show adjusted odds ratios (OR) with 95% of

confidence interval (CI) and determination coefficients (R<sup>2</sup> ). In the regression models, the collinearity variables were discharged. The *p*-value < 0.05 was considered significant. In addition, *p*-value < 0.10 was reported as a quasi-significant trend.

### **3. Results**

The prevalence of maternal complications in the cohort was 46.2% (84/182) and the prevalence of fetal complications was 25.0% (45/182). There was no statistical association between maternal and fetal complications (*χ* <sup>2</sup> = 0.759; *p*-value = 0.38).

### *3.1. Maternal Characteristics and Development of Obstetric Complications*

Overall, 67.5% (123/182) of the women in the study had graduate degree, being the rest undergraduate degree. There were no women with less than an undergraduate education. Overall, 67.0% (122/182) had a partner; and the partner was employed for 95.1% (116/122). Overall, 86.2% (157/182) of the women were employed during the study period. Regarding the economic level of the family core, 74.1% (135/182) of the cohort earned more than 2000 euros/month.

We did not find statistical differences in any of the socioeconomic parameters analyzed (civil status, educational level, economic status and alcohol or tobacco consumption) between women with and without maternal complications. No differences were found in relation to either infant sex or maternal age. The group of women with maternal complications showed a significantly lower gestational age and higher use of ART, twin pregnancies and preterm labor, compared to women without maternal complications (Table 2).


**Table 2.** Maternal characteristics according to maternal and fetal complications.

Data show median and interquartile range (IQR) in quantitative variables and relative frequency (*n*) in qualitative variables. <sup>1</sup> Sex in single and first newborn in twin pregnancies. <sup>2</sup> Sex of the second newborn in twin pregnancies. Assisted reproduction techniques (ART). The *p*-value was obtained by Mann–Whitney U and Chi-squared tests, for quantitative or qualitative variables, respectively.

> Regarding differences between women who developed or not fetal complications, no statistical differences were found in socioeconomic parameters or infant sex. However, women with fetal complications had significantly higher age, use of ART, twin pregnancies, preterm labor and FGR, compared to women without fetal complications (Table 2).

In our cohort, ART and twin pregnancy were significantly associated (*χ* <sup>2</sup> = 79.512; *p*-value = 0.001), as well as preterm labor and FGR (*χ* <sup>2</sup> = 4.391; *p*-value = 0.036). Based on

2B).

these collinearities, the variables twin pregnancy and preterm labor were included in the logistic regression models. 16.0 (27.3) pg/mL. Melatonin levels tended to be lower in women who developed a maternal complication compared to those who did not develop a maternal complication, it

In pregnancies without any obstetric adverse outcome, plasma melatonin levels were

#### *3.2. Maternal Plasma Variables in the First Trimester* but did not reach statistical significance (*p*-value = 0.09; Figure 2A). Melatonin levels were not significantly different between women with and without fetal complications (Figure

*J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 7 of 16

Male 1 52.3% (46) 60.8% (48) 0.27 57.6% (68) 51.3% (20) 0.49 Male 2 41.9% (13) 52.9% (27) 0.33 54.2% (26) 42.9% (12) 0.34 Preterm labor 17% (16) 32.9% (26) 0.015 0% (0) 52.4% (22) 0.001 Fetal growth restriction 4.3% (4) 12.2% (9) 0.060 0% (0) 33.3% (15) 0.001 Data show median and interquartile range (IQR) in quantitative variables and relative frequency (*n*) in qualitative variables. 1 Sex in single and first newborn in twin pregnancies. 2 Sex of the second newborn in twin pregnancies. Assisted reproduction techniques (ART). The *p*-value was obtained by Mann–Whitney U and Chi-squared tests, for quantitative or

*3.2. Maternal Plasma Variables in the First Trimester* 

In pregnancies without any obstetric adverse outcome, plasma melatonin levels were 16.0 (27.3) pg/mL. Melatonin levels tended to be lower in women who developed a maternal complication compared to those who did not develop a maternal complication, it but did not reach statistical significance (*p*-value = 0.09; Figure 2A). Melatonin levels were not significantly different between women with and without fetal complications (Figure 2B). In pregnancies without any obstetric adverse outcomes, plasma cortisol levels were 19.2 (8.7) µg/dL. Cortisol levels did not show statistical differences between women with and without maternal complications (Figure 2A). Cortisol tended to be higher in the group who developed fetal complications but did not reach statistical significance (*p*-value = 0.07) (Figure 2B).

**Figure 2.** Maternal plasma melatonin and cortisol levels according to maternal (**A**) and fetal (**B**) complications. Data show median and interquartile range (IQR). The *p*-value was obtained by **Figure 2.** Maternal plasma melatonin and cortisol levels according to maternal (**A**) and fetal (**B**) complications. Data show median and interquartile range (IQR). The *p*-value was obtained by Mann–Whitney U test.

Mann–Whitney U test. *3.3. Psychological Variables during Pregnancy*  Psychological variables were reported according to the gestational trimester. Table 3 shows the scores of the study groups and mothers without any obstetric adverse outcome (maternal or fetal complications). In pregnancies without any obstetric adverse outcomes, plasma cortisol levels were 19.2 (8.7) µg/dL. Cortisol levels did not show statistical differences between women with and without maternal complications (Figure 2A). Cortisol tended to be higher in the group who developed fetal complications but did not reach statistical significance (*p*-value = 0.07) (Figure 2B).

### *3.3. Psychological Variables during Pregnancy*

Psychological variables were reported according to the gestational trimester. Table 3 shows the scores of the study groups and mothers without any obstetric adverse outcome (maternal or fetal complications).

Regarding maternal complications, in the first trimester, we did not detect statistical differences between groups in any of the parameters evaluated. In the second trimester, women who developed maternal complications showed significantly lower scores in life satisfaction compared to those without maternal complications. In the third trimester, the group of maternal complications scored statistically lower in both life satisfaction and resilience than women without maternal complications (Table 3).

Regarding the group of fetal complications, in the first trimester, women with fetal complications showed a significantly higher score in anxiety compared to women without fetal complications. In the second and third trimesters, no statistical differences in the psychological variables were detected between mothers with and without fetal complications (Table 3).


**Table 3.** Psychological variables according to maternal (*n* = 84) and fetal (*n* = 45) complications.

*p*-value was obtained by Mann–Whitney U test.

In the cohort (n = 182), we found in the first trimester a significant and positive correlation between resilience and melatonin levels (rho = 0.18; *p*-value = 0.021). Although without significant differences, in the second trimester, we found a negative correlation among negative affect (rho = −0.15; *p*-value = 0.09), pregnancy concerns (rho = −0.15; *p*-value = 0.07) and melatonin levels. Furthermore, in pregnant women with maternal and fetal complications, we found in the second trimester a significant and positive correlation between positive affect and melatonin levels (rho = 0.55; *p*-value = 0.033). However, we did not find a statistical correlation between cortisol levels and any of the psychological scores.

Since a high proportion of women in the study had pregnancies derived from ART (*n* = 66), we also analyzed differences in psychological variables according to use of ART. In the first trimester, ART had significantly higher scores of negative affect (ART = 2.1 (1.0); non-ART = 1.7 (0.8), *p*-value = 0.026) and anxiety (ART = 1.1 (0.6); non-ART = 0.7 (0.4), *p*-value = 0.006). In the third trimester, ART also had significantly higher scores of negative affect (ART = 2.3 (1.1); non-ART = 2.0 (1.0), *p*-value = 0.010) and anxiety (ART = 1.3 (0.8), non-ART = 1.0 (0.7), *p*-value = 0.007). Furthermore, ART had significantly lower scores of positive affect (ART = 3.4 (0.7); non-ART = 3.5 (0.8), *p*-value = 0.033) and life satisfaction (ART = 5.4 (1.6); non-ART = 5.8 (1.0), *p*-value = 0.017). *J. Pers. Med.* **2021**, *11*, x FOR PEER REVIEW 9 of 16 non-ART = 1.0 (0.7), *p*-value = 0.007). Furthermore, ART had significantly lower scores of positive affect (ART = 3.4 (0.7); non-ART = 3.5 (0.8), *p*-value = 0.033) and life satisfaction (ART = 5.4 (1.6); non-ART = 5.8 (1.0), *p*-value = 0.017). *3.4. Logistic Regression Models Associated with Maternal and Fetal Complications* 

#### *3.4. Logistic Regression Models Associated with Maternal and Fetal Complications* indicating that maternal complications are a risk factor for prematurity. Data also evidence that melatonin levels in the first trimester and the psychological variable "life sat-

The models showed that maternal complications were associated with preterm labor, indicating that maternal complications are a risk factor for prematurity. Data also evidence that melatonin levels in the first trimester and the psychological variable "life satisfaction" in the third trimester were negatively associated with maternal complications and, therefore, could be considered protective factors (Figure 3A). isfaction" in the third trimester were negatively associated with maternal complications and, therefore, could be considered protective factors (Figure 3A). In the models of fetal complications, preterm labor was a risk factor associated with fetal complications. Other risk factors for fetal complications were maternal cortisol levels and anxiety in the first trimester, and life–work concerns in the second trimester (Figure 3B).

The models showed that maternal complications were associated with preterm labor,

**Figure 3.** Logistic regression models, obtained by stepwise procedures, for maternal (**A**) and fetal (**B**) complications. Data show odds ratio (OR) [95% confidence interval (CI)] and determination coefficients (R2). **4. Discussion Figure 3.** Logistic regression models, obtained by stepwise procedures, for maternal (**A**) and fetal (**B**) complications. Data show odds ratio (OR) [95% confidence interval (CI)] and determination coefficients (R<sup>2</sup> ).

The objective of this study was to identify biopsychosocial risk and protective factors associated with the development of adverse obstetric outcomes. Our data show that

In the models of fetal complications, preterm labor was a risk factor associated with fetal complications. Other risk factors for fetal complications were maternal cor-tisol levels and anxiety in the first trimester, and life–work concerns in the second tri-mester (Figure 3B).

### **4. Discussion**

The objective of this study was to identify biopsychosocial risk and protective factors associated with the development of adverse obstetric outcomes. Our data show that maternal psychological features exert an influence on pregnancy outcomes; in particular, high scores in life satisfaction could be a protective factor to prevent maternal complications, while anxiety and life–work conflicts may be risk factors of fetal complications. The present study also points out the relationship between maternal melatonin and cortisol levels in early pregnancy and obstetric outcomes. We explored the association between maternal psychological parameters and these plasma hormones. Although we did not find a significant correlation with cortisol, we found some associations between psychological variables and melatonin. Melatonin levels were positively associated with resilience in the first trimester and with positive affect in the second trimester, while a negative association was found with pregnancy concerns. In summary, our data reveal the relationship between social, psychological and biological spheres, which can exert an influence on pregnancy outcomes. Our data point out the need to study pregnancy from a more global biopsychosocial approach.

Pregnancy complications are increasing in our society due to several factors and represent an important health problem. Thus far, they have been studied mainly from a clinical point of view. The incorporation of the psychological and social domain into clinical practice may help to understand their origin and to improve healthcare. The relevance of considering multiple spheres to predict the clinical outcomes has been demonstrated in perinatology [36]. In this work, we considered this global approach, analyzing the social, psychological and biological spheres. These different aspects are discussed below.

*Social factors.* Regarding the social sphere, poverty and racial disparities have usually been explored as key determinants of health. In the studied population, these factors do not seem to play an important influence on the obstetric and neonatal outcome, since the population studied is of middle-high socioeconomic level. A relevant characteristic in our population was the age, which was above the optimum for maternity. This fact reflects a key aspect in high-income countries: the delay in the maternity age. In our social context, there has been a gradual access of the women to higher education and employment, as well as in pregnancy control [37]. These sociocultural determinants may be some of the factors implicated in the continuing rise in the age of childbearing observed from the second half of the twentieth century [38]. High-income countries enacted comprehensive maternity legislation providing women with rights, such as a period of employment protection for childbirth [39]. Legislation can help solving the problem of work–family conflicts; however, delayed maternity age and its impact on women's health remains a problem. In fact, in our population, we found that maternity age was associated with adverse fetal outcomes.

The association between advanced maternity age and adverse outcome may have biological grounds. On the one hand, it is linked to infertility. ART has made possible maternity beyond biological limits. However, the main consequence is an increased rate of twin pregnancies, which are a risk factor for obstetric complications, particularly preterm labor [38,40]. This was confirmed in the present study, evidencing that twin pregnancies were nearly seven times more likely to develop a complication compared to singletons. It is important to note that obstetric adverse outcomes are not a direct effect of ART, but rather of the fact that the use of ART is associated with twin pregnancies. In fact, it has been found that the rate of obstetric complications in twin pregnancies derived from ART is not higher than in spontaneous twin pregnancies, even at 45 years old [41]. In addition, an important aspect to explore would be the relationship of particular ART techniques and obstetrical outcomes, which we did not collect it.

In addition to the biological influence on pregnancy outcome, psychological factors were considered. Getting pregnant at an advanced age, the process of repetitive ART cycles and a multiple pregnancy represent important stress factors for the mother, which may exert negative influences. Therefore, the psychological sphere should be considered.

*Psychological factors*. Psychological stress during pregnancy affects the maternal–fetal binomial health and is known to have effects on pregnancy hypertension, fetal programming and gestational timing [42]. According to the literature, pregnancy is a period of significant life change for a woman and her partner, and it can be perceived as a stressful situation. Research has found that negative life events were associated with an increased risk of fetal complications and emotional distress in the mother [43]. Our data support that pregnant women with high negative affect scores are associated with maternal and fetal complications. In the same line, other studies have found that psychological optimism, pessimism or anxiety are associated with birth outcomes [44]. Our data show that maternal anxiety in the first trimester is a risk factor for later development of fetal complications.

Pregnancy represents a challenge, and, for many women, it may be a stressful period, particularly if there are insufficient psychosocial resources or additional stressors. One of them is the use of ART, which implies a high level of uncertainty. We therefore explored the possible influence on psychological factors and pregnancy outcomes. As expected, we found higher scores of negative affect and anxiety and lower positive affect and life satisfaction in pregnancies derived from ART. If the response to a stressor is inadequate, it may lead to a negative influence on health. Our data show that ART-derive pregnancies were at higher risk of maternal and fetal complications. This has been proposed to be directly linked to advanced maternity age and the association with twin pregnancies; however, our data reveal high levels of anxiety, which may also contribute to the worse outcome and could be taken into consideration.

According to the Commission on the Social Determinants of Health from the World Health Organization [45], a stressful workplace is considered one of the most important psychological stressors, while stable family core and social behaviors are key positive aspects for mental health [46]. Our data support that pregnant women with maternal and fetal complications scored low in life satisfaction and high in life–work concerns. Today, health professionals should be aware of the influence of psychological processes and social behavior disadvantage on disease; in fact, sociodemographic disadvantages are also postulated as independent risk factors for adverse pregnancy outcomes [47].

It is important to note that the psychological scores in the second and third trimesters may be biased because pregnancy problems have already been diagnosed and maternal behaviors could be affected.

*Biological factors*. Pregnancy is a period of biological changes, which interacts with the psychological sphere. A stressful job, the problems associated with the pressure of getting pregnant at an advanced age, the use of ART and twin pregnancies are important psychological factors which may influence the biological domain [43]. Even though the biological milieu has been thoroughly studied in relation to obstetric complications, the relationship between psychological and biological spheres has not been fully addressed before. In our study, we assessed two key hormones, melatonin and cortisol, since they are relevant in pregnancy and have been previously shown to be affected by psychological conditions.

Melatonin has been associated with the psychological alterations, and it has been proposed that low levels of this hormone may underlie the pathophysiology of depression and other mood disorders, which are also relatively frequent the context of pregnancy. In addition, this hormone is relevant in the maintenance of a normal pregnancy. Therefore, we hypothesized that melatonin could be a keystone between psychological processes and pregnancy disorders. Our data show a negative correlation between melatonin levels and pregnancy concerns. In addition, we demonstrated that women with maternal complications tended to have lower melatonin levels. This association may be related to poorer antioxidant defenses, since oxidative stress is a key mechanism in pregnancy complications [48] and the role of melatonin as protective hormone in pregnancy is related

to its powerful antioxidant actions [14]. In fact, previous data of our group demonstrate that low plasma melatonin was associated with low levels of antioxidants and development of maternal complications [3] and with preterm delivery in twin gestation [15]. We suggest that low melatonin can contribute to a poor antioxidant balance in early pregnancy and participate in pregnancy complications later on. Melatonin is a hormone with a circadian rhythm and its highest levels occur during sleep. Therefore, the reasons for low melatonin levels can be directly related to sleep deficiency. Sleep disturbances can be linked to psychological factors. For example, it has been shown that life–work conflicts and pregnancy concerns are key factors influencing sleep [48]. According to our data, pregnancy concerns tended to be increased in women with maternal complications. Therefore, it is possible that the association between low melatonin and poor pregnancy outcome could be partially related to a reduction of the number of sleep hours. Additionally, the effects of job-related stressors on work–family conflict are most often viewed from the perspective of conservation of resources theory [49]. According to the theory, individuals have a finite amount of time, attention and energy, and, therefore, higher time commitment or demand from one role puts pressure on other roles [50,51]. We analyzed the possible relationship between melatonin and resilience in the first trimester and found a positive association. We propose that melatonin can be a hormone affected by psychological variables, being associated with positive and negative mood in pregnancy. This hypothesis needs to be studied further since the present work had some limitations, such as assessing melatonin at daytime and at a single and point. It would be desirable to analyze also night levels along pregnancy, together with evaluation of sleep quality and psychological variables.

Cortisol is a hormone with multiple physiological roles and well known to be secreted in stressful situations. In pregnancy, maternal cortisol passage to the fetus is limited by the placental barrier 11β-dehydrogenase enzyme (11β-HSD-2), which transforms cortisol into cortisone, an inactive glucocorticoid [52,53]. It has been demonstrated that 11β-HSD-2 is inhibited as a consequence of maternal psychological stress, affecting fetal growth [54,55]. There is also evidence that pregnant women who had anxiety showed a reduction of uterine blood flow [56] which is related to FGR. These studies are in accordance with our data showing high anxiety scores in women who developed fetal complications together with a trend towards high levels of cortisol in the first trimester. Our data add evidence to the link between maternal stress during early pregnancy and adverse maternal-fetal outcome, through alterations in the hormonal milieu. However, although we analyzed the possible association between cortisol levels and the psychological variables, such as anxiety, we did not find any potential relationship. Our study had some limitations regarding cortisol measurements, which could account for this. Firstly, the assessment at a single time point in the morning; evaluation of the hormone at different time points would have been more informative, allowing analyzing other parameters such as the diurnal cortisol slope and cumulative cortisol output across the day. It is also possible that venipuncture could have caused additional stress and cortisol release; this effect has been mainly observed in children related to fear of pain and is likely minimized in our population of adults with a programmed intervention. Cortisol measurements in saliva could avoid this possible problem.

### *Strengths and Limitations*

The main strength of this study was the longitudinal approach in the psychological variables. This condition adds power to the design compared to cross-sectional studies, by virtue of observing the temporal order of events. The second strength of the study was the exploration of multiple spheres in the pregnancy context. The new methodological approaches to research in human biomedicine must consider the biological, psychological and social points of view. Thirdly, the logistic regression models with the stepwise method allow estimating the contribution of biological, psychological and social areas sequentially.

Regarding limitations, the first is the assessment of the biochemical variables only at a one-time point since cortisol and melatonin exhibit circadian rhythms. This was due to

ethical limitations, which restricted the blood collection only in the morning and in the first trimester, coincident with a routine analysis. Although blood samples were extracted in the same conditions and the levels were determinate under the same protocols for all women, this aspect needs to be taken into account in future studies. The second limitation is the sample size, which is smaller in the third trimester than in the first one, related to prematurity, stillbirths or loss to follow-up, resulting in fewer women completing the psychological applications at the end of pregnancy. It would also be desirable to have a more heterogeneous population reflecting other social environments, since the present sample is homogeneous in terms of age, education and income. Thirdly, the analysis of the biological markers at different time points along gestation, and the inclusion of other molecules such as inflammatory mediators, oxidative stress markers or placental and vascular growth factors, known to be related to pregnancy disorders would help to complete the relationship between biological and psychological variables and their role in pregnancy outcomes.

In addition, it would be necessary to carry out new studies to check whether the results are maintained in other cohorts with another methodologies (i.e., Monte Carlo simulation analysis). However, the key element is to start from a theoretical model that justifies the analyses performed, not only focus on the method [57]. Gaining knowledge on factors from these three spheres would help building up the biopsychosocial model of pregnancy, which would aid maternal counseling to improve pregnancy outcomes.

### **5. Conclusions**

In this work, using logistic regression models, we detected a relationship between some maternal psychological and biological factors (melatonin and cortisol) and the development of complications.

To help preventing maternal complications, high melatonin levels at the beginning of gestation and life satisfaction in mid-pregnancy could be protective factors. Our results also suggest that low anxiety and cortisol levels at the beginning of pregnancy and reducing problems of work–life conciliation could help prevent fetal complications. Considering these data, it may be interesting to promote health public guidelines to support resources, which will improve life satisfaction and life–work conciliation during pregnancy. In addition, to know the social-reality of each pregnant women, intervening from primary care to specialized clinical psychology would help humanize pregnancy. These policies contribute to the decline in the rate of adverse obstetric outcomes with a direct impact on the healthcare cost, particularly in societies with advanced maternity age.

**Author Contributions:** Conceptualization, B.M.-J., S.M.A. and E.G.; methodology, B.M.-J. and E.G.; software, D.R.-C. and E.G.; validation, B.M.-J., S.M.A. and E.G.; formal analysis, D.R.-C. and E.G.; investigation, D.R.-C., M.d.l.C., V.B. and A.G.-D.; data curation, D.R.-C. and A.G.-D.; writing original draft preparation, D.R.-C., M.d.l.C., V.B. and A.G.-D.; writing—review and editing, B.M.-J., S.M.A. and E.G.; and supervision, S.M.A. and E.G. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Human Research Ethical Committee of Hospital Universitario La Paz and Institutional Review Board of Universidad Autónoma de Madrid (protocol code PI-1490 and CEMU/2013-10, respectively; October 2013).

**Informed Consent Statement:** Informed consent was obtained from all subjects involved in the study.

**Data Availability Statement:** The raw datasets used for this study contained health personal information and the Ethical Committee requirements has forbidden the data transfer. However, a particular report could be sent to the corresponding authors by email.

**Acknowledgments:** The authors would to thank all study pregnant and nursing research staff.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


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