**Managing the Oral Health of Cancer Patients during the COVID-19 Pandemic: Perspective of a Dental Clinic in a Cancer Center**

**Sunita Manuballa 1, Marym Abdelmaseh 1, Nirmala Tasgaonkar 1, Vladimir Frias 1, Michael Hess 1, Heidi Crow 1,2, Sebastiano Andreana 1,3, Vishal Gupta 4, Kimberly E. Wooten 4, Michael R. Markiewicz 4,5, Anurag K. Singh 6, Wesley L. Hicks Jr. <sup>4</sup> and Mukund Seshadri 1,7,\***


Received: 11 August 2020; Accepted: 24 September 2020; Published: 28 September 2020

**Abstract:** The practice of dentistry has been dramatically altered by the coronavirus disease 2019 (COVID-19) pandemic. Given the close person-to-person contact involved in delivering dental care and treatment procedures that produce aerosols, dental healthcare professionals including dentists, dental assistants and dental hygienists are at high risk of exposure. As a dental clinic in a comprehensive cancer center, we have continued to safely provide medically necessary and urgent/emergent dental care to ensure that patients can adhere to their planned cancer treatment. This was accomplished through timely adaptation of clinical workflows and implementation of practice modification measures in compliance with state, national and federal guidelines to ensure that risk of transmission remained low and the health of both immunocompromised cancer patients and clinical staff remained protected. In this narrative review, we share our experience and measures that were implemented in our clinic to ensure that the oral health needs of cancer patients were met in a timely manner and in a safe environment. Given that the pandemic is still on-going, the impact of our modified oral healthcare delivery model in cancer patients warrants continued monitoring and assessment.

**Keywords:** COVID-19; oral oncology; dental; oral surgery; head and neck cancer; cancer patients

#### **1. Introduction**

The outbreak of coronavirus disease 2019 (COVID-19) [1] has dramatically changed the practice of dentistry worldwide, given the close "person-to-person" contact involved in delivering dental care and treatment procedures that produce aerosols, often resulting in dental providers being exposed to blood, saliva and respiratory droplets [2,3]. Given the mode of transmission of COVID-19, dental healthcare professionals including dentists, dental assistants and dental hygienists are at high risk of exposure among all healthcare personnel [4,5]. In this regard, studies from multiple groups around the globe have reported on critical infection control measures [5–7] and guidelines for modifications to dental clinic workflows that were implemented during the pandemic [8,9]. Reports have also described the impact of COVID-19 on the practice of dental specialties, including oral medicine [10] oral and maxillofacial surgery [11–13], orthodontics [14] and endodontics [4,15].

Oral oncology (sometimes referred to as "Dental Oncology") is a branch of dentistry/oral medicine that provides specialized care to address the complex dental and oral health needs of cancer patients [16,17]. The division of Dentistry and Maxillofacial Prosthetics (DMFP) is a clinical service within the Department of Oral Oncology at Roswell Park, a National Cancer Institute (NCI)-designated Comprehensive Cancer Center located in Buffalo, New York. The center provides comprehensive cancer care to patients in the Buffalo–Niagara metropolitan area, surrounding counties in Western New York (WNY) and patients from New York State (NYS). The center also provides cancer care for patients from other states within the U.S. and Canada. The mission of DMFP is to provide high-quality oral healthcare to cancer patients. Specialized services provided by DMFP include management of existing dental conditions prior to the start of cancer therapy, prevention and management of oral complications from cancer treatment (radiation, chemotherapy and hematopoietic stem cell transplantation) and functional rehabilitation of patients after invasive cancer surgery [18–20]. Cancer patients are immunocompromised and, as a result, susceptible to oral and respiratory infections, including COVID-19 [21]. Given this "double whammy" (increased risk for cancer patients and dental providers), the pandemic has necessitated rapid implementation of changes to our oral healthcare delivery model, including adaptation of clinical workflows and diagnostic and treatment paradigms. Kochhar et al. have recently described recommendations for provision of dental care to cancer patients during the pandemic [22]. As a dental clinic in a comprehensive cancer center, we have continued to safely deliver dental care to cancer patients during this pandemic. This was accomplished through adaptation of clinical workflows to ensure that cancer patients can adhere to their planned cancer treatment. Timely implementation of practice modification measures was critical to ensure that patients and dental clinic staff remained protected and the risk of transmission remained minimal.

#### **2. Overview of DMFP Clinic Responsiveness to COVID-19**

The overview of the DMFP clinic response to COVID-19 is shown schematically in Figure 1. In response to the pandemic, a DMFP clinic task force was created in early March 2020 to implement clinic-centric measures that were in compliance with Centers for Disease Control and Prevention (CDC), the American Dental Association (ADA), NYS and institutional guidelines and develop protocols for safely providing dental care for cancer patients. The taskforce included the department chair, the clinical chief, a general dentist, the lead dental assistant and the clinic administrator. Such a composition of the task force ensured that all administrative and operational needs of the clinic and staff concerns were addressed. Given the relatively fluid nature of the situation, daily virtual meetings of the taskforce were conducted (via WebEx) to monitor the regional situation and to appraise team members of any updates to institutional policies regarding patient care and staff. The goals of the task force and the strategic approach undertaken to implement clinic-centric measures that complemented institutional measures are summarized in Figure 1.

**Overview of DMFP Clinical Responsiveness to COVID-19**

**Figure 1.** Schematic overview of the responsiveness of the Dentistry and Maxillofacial Prosthetics (DMFP) clinic at Roswell Park Comprehensive Center to the pandemic. (CDC—Centers for Disease Control and Prevention; ADA—American Dental Association; NYS—New York State).

The following measures were implemented in our clinic to limit traffic in clinical areas and ensure that the oral health needs of cancer patients were met in a timely manner and in a safe environment.

#### *2.1. Identifying Critical Services Provided by the Dental Clinic*

With the evolution of the pandemic in NYS and around the United States, the ADA, CDC and the New York State Dental Association (NYSDA) issued guidance on March 16, 2020, that all dental offices provide only emergency dental care for patients. A minimum of 3 weeks of postponement was recommended for all elective and non-emergent services. By mid-March 2020, the dental clinic taskforce had decided to scale down clinical operations to essential critical functions. In compliance with NYS, ADA and CDC guidelines, clinic visits were restricted to management of active cancer patients that needed medically necessary oral health evaluations (e.g., patients requiring dental clearance prior to start of radiation therapy, bone marrow transplant patients, patients scheduled for surgery) and urgent/emergent dental treatment.

#### *2.2. Modifying Clinic Schedules*

All clinic providers were asked to review their schedules for the months of March and April. Consistent with the framework [23] suggested by the Centers for Medicare and Medicaid Services (CMS), a three-tiered classification of patients was developed to modify clinic schedules as shown in Figure 2. Patients with scheduled appointments were immediately contacted and their health status assessed over the phone to determine the urgency of their treatment. The immune status of patients (undergoing active chemo/RT or immunotherapy, recent organ transplant; on immunosuppressive therapy) was also taken into consideration while determining the tier and type of appointment. Patients with appointments for elective dental procedures (e.g., routine follow-up appointments, prosthetic or routine oral hygiene maintenance patients that could wait) that could be safely deferred were rescheduled (on an average of 4–6 weeks from the initial appointment date). Patients were notified of their rescheduled appointments by the clinic receptionist along with the communication regarding the availability of all dentists and specialists for telephone consults.


**Figure 2.** Three-tiered classification of patients based on their oral health needs for optimal scheduling of appointments during the pandemic.

#### *2.3. Rotational Scheduling of Clinic Faculty and Sta*ff

In alignment with the institutional "directed to leave campus" (DLC) policy, non-critical clinic staff, including personnel in administrative and research arms of the department, were scheduled to work remotely. Secure remote access (email, virtual desktop) was provided to staff members, which allowed them to continue their daily tasks from home. For essential clinic staff, a rotational schedule was implemented wherein one dentist and two dental assistants were assigned on a weekly basis. The providers and the assistants were on-site two days of the week to attend to patients requiring medically necessary dental procedures, but all providers were available for teleconsultation during the week. Additional emergent/urgent appointments were also handled by the same dentist /dental assistant team scheduled to be "on call" for the week. This arrangement also ensured a two-week window before the same provider/assistant team was scheduled to be back on-site (i.e., Week 1: Team A; Week 2: Team B; Week 3: Team C; Week 4: Team A). This temporal spacing of provider/staff schedules minimized overlap between faculty and staff from individual teams and allowed for a potential 14-day period of isolation or quarantine in the unfortunate event that one of the team members became symptomatic. All staff were instructed to continue self-monitoring and advised to stay home if they experienced flu-like symptoms.

#### *2.4. Transitioning to a 'Virtual' Tumor Board*

Another COVID-related modification in our clinical workflow involved a change in the conduct of a multidisciplinary head and neck conference ("tumor board"). The multidisciplinary conference serves as a valuable forum for discussions among team members regarding diagnosis and treatment planning of head and neck cancer patients. Roswell Park conducts a weekly head and neck tumor board meeting that is attended by faculty from the above-mentioned specialties along with nurse practitioners, physician assistants, physical therapists, palliative care and social workers. These weekly meetings are quintessential to ensure adequate work up for correct diagnosis, staging, discuss treatment strategies (surgery versus radiation), surgical reconstruction approaches for best quality of life and survivorship issues. In a pre-COVID-19 world, this involved an in-person meeting of about 25–30 specialists in a packed conference room. With the onset of the pandemic and the restrictions that followed, such a gathering was no longer possible. Given the large number of participants at these weekly meetings, a decision was made in March 2020 to move the tumor board to an online platform ("virtual" tumor board). We transitioned to weekly virtual tumor board meetings utilizing the WebEx platform developed by Citrix systems. The WebEx platform allowed both video and audio presentation,

including a screen sharing ability. The platform was approved by Roswell IT and was compliant with the Health Insurance Portability and Accountability Act (HIPAA) regulations. Email invitations for these sessions were sent out to participants along with the pertinent WebEx information. Participation required a valid attendee name and a Roswell Park email login. The virtual format allowed for efficient participation of a large number of attendees with case presentations made in Microsoft Power Point format by the head and neck fellow, along with review of histology slides by a pathologist and imaging by the radiologist. Although not a new concept, we had no previous experience with virtual multidisciplinary conferences. Our experience to date with the virtual tumor board format has been positive, and the format has encouraged greater and timely participation from a large group of participants. In addition, since most of the attendees participated in the virtual meeting from their workstations, it provided them with the ability to instantly access not just patient records, but also published literature to clarify any points if needed. The biggest limitation of the virtual format is the lack of personal interaction and interactive conversations between multiple speakers. Despite a few initial technical glitches, this approach continues to be effective, allowing the entire team to engage in thoughtful discussions regarding treatment plans for individual patients without increasing the risk of exposure and potential members between clinic staff.

#### *2.5. Screening of Patients Prior to Visits*

Multiple measures were put in place for screening patients with scheduled appointments at our clinic. These included inquiry of symptoms over the phone ("tele-triage") 24 h prior to their appointment. Patients were screened (symptom checks, temperature measurements) at the main entrance to our cancer center and then at the clinic front desk at check-in. The duration of appointments for patients requiring medically necessary or emergency dental procedures was also lengthened (approximately 90 min) with adequate time (30–45 min) between appointments to allow clinic staff to perform all infection control procedures according to CDC guidelines.

#### *2.6. Infection Control Training and Operatory Preparation*

Recognizing the need for stringent infection control protocols, several institutional and clinic-centric training measures were implemented to train all clinical faculty and staff. In addition to the mandatory annual in-services routinely completed by all hospital staff, refresher training on infection control procedures was provided in the form of training videos, instruction sheets, flyers as well as presentations and group discussions (via WebEx). Topics covered in these training sessions included but were not limited to the basics of COVID-19, hand hygiene, respiratory etiquette, personal protective equipment (PPE), donning and doffing, sterilization and disinfection procedures, protection of all equipment (e.g., computer screens, monitors), proper disposal of single-use instruments and minimizing clutter (e.g., leaving all paperwork outside the operatory; removal of any potential sources of contamination, such as pictures from the walls) within the operatories. All providers, including assistants, wore full surgical garb (shoe covers, head covers, surgical gowns, gloves, N95 masks and face shields) while examining patients.

#### *2.7. Clinical Care Guidelines for Dental Management of Cancer Patients*

Given the unprecedented nature of events, guidelines for managing oral care of cancer patients were developed. Due to the known risk of COVID-19 transmission via respiratory droplets, a decision was made to avoid high aerosol-generating procedures including the use of high-speed hand pieces, ultrasonic scalers and air-water syringe. A prophylactic hydrogen peroxide mouth rinse was provided to all patients prior to their clinical examination. Aerosol-generating procedures were avoided in severely immunocompromised patients, and clinical evaluation of these patients was performed in dedicated operatories. Consideration was given and plans put in place for performing low aerosol-generating procedures in the operating room (OR) to these patients if clinically warranted. Conservative treatment for asymptomatic carious restorations and minimal debridement were provided without the use of

ultrasonic equipment to reduce the microbial load prior to their treatments. Restorative procedures were performed following the principles of atraumatic restorative therapy [24]. Based on the depth of invasion and the presence/absence of symptoms, caries excavation and temporary restorations were placed. Alternatively, caries arresting measures, through the use of silver diamine fluoride (SDF 38% Advantage Arrest), were performed. Hand scaling was performed, and no ultrasonic scaling or polishing was done. Procedures were performed under rubber dam isolation, and radiography was limited to extra-oral radiographs. Extractions of non-restorable teeth were performed following the recommended PPE protocols. Extractions of teeth were only done when the teeth had significant mobility, poor bone support or a root morphology that was amenable to a simple extraction. For head and neck patients undergoing surgical procedures, dental extractions were performed in the operating room (OR) in close coordination with the head and neck surgeons. Contingency plans were also made for providing dental care in peri-operative surgical suites as alternatives to dental operatories, if needed. Emergency floor consultations were provided for in-patients and treatments provided as needed. During this time, the dental faculty maintained crucial communication with patients, their treating physicians (medical and radiation oncologists) and surgeons to maintain continuity of care.

#### *2.8. Maxillofacial Rehabilitation of Cancer Patients during COVID-19*

Maxillofacial prosthetics is the sub-specialty of prosthodontics that deals with the rehabilitation of head and neck defects beyond the immediate oral region. The most common procedures performed by a maxillofacial prosthodontist at a cancer center are the obturation or restoration of missing maxillary and mandibular structures and the replacement of missing orbital, nasal, auricular and cranial structures [16,17,25]. Other procedures performed include surgical placement of implants to support or retain prostheses or the creation of devices to aid the delivery of surgical or radiation treatment. The decision-making process during COVID-19 was complicated by the fact that, although many non-emergent prosthetic procedures could be postponed, the delay in adequate rehabilitation has major consequences, including deficient speech, swallowing as well as the psychosocial issues for patients due to a visibly missing body part. The treatment protocol at Roswell Park considered both the patient's medical status as well as the urgency of the procedure involved and attempted to provide treatment with the fewest number of visits and procedures to prevent exposure to the virus. Medically necessary surgical obturations that could be inserted with sutures or ligation were performed in the operating room. Removal of the surgical prosthetic and replacement with an interim prosthesis were evaluated on a case-by-case basis, and all adjustments were carried out under a laboratory hood. Since the creation of definitive prosthetics often requires multiple aerosol-generating procedures, these treatments were postponed. Conventional prosthodontic procedures and surgical implant placement also generate a large amount of aerosol and were delayed in order to limit the exposure of severely medically compromised patients. Fabrication of facial or somatic prostheses also requires multiple visits and would increase patient and provider risk of exposure (asymptomatic carriers) and was postponed.

#### *2.9. Telemonitoring and Follow-Up*

All phone consultations were documented in the electronic health record (EHR). The temporal scheduling of clinical faculty and staff enabled providers that were off-site to monitor requests for clinic appointments. Concerns and requests from patients seeking emergency appointments were reviewed by a dental provider to understand the nature of their emergency and the appropriate course of management. Phone consults were also performed for patients receiving radiation to follow up for dysphagia, mucositis or candidiasis. Individual prescription requests (e.g., fluoride toothpaste, chlorhexidine) were managed by the providers. Appropriate prescriptions were called into their pharmacies. All patient concerns were initially addressed with a phone call, and if a clinic visit was deemed necessary, the patient was scheduled for a visit.

#### *2.10. Modifications to a General Practice Dental Residency Training Program*

The DMFP department serves as a home to a 1-year General Practice Residency (GPR) program that is administered jointly with the State University of New York, University at Buffalo, School of Dental Medicine. The program has an annual intake of two residents who spend approximately 70 percent of their time in the clinical care of patients. The didactic portion consists of treatment-planning seminars and literature reviews, as well as lectures in diagnosis, prosthodontics, endodontics and practice management. When the directive to leave campus (DLC) for all non-essential staff was implemented at our cancer center, a distance education model based on an online learning curriculum and continuing education (CE) credits covering all areas of general dentistry was implemented. Subsequently, following the implementation of several risk reduction measures and enhanced infection controls, residents were allowed to return on a rotating basis and observe patient care, to minimize contact and exposure for an already vulnerable patient population. PPE donning/doffing procedures were extensively reviewed. Modifications to dental practice and clinical decision making in the context of a pandemic were thoroughly explained. Differences in risk–benefit considerations between ideal treatment plans versus minimally acceptable treatment to "clear" patients for oncologic care were discussed. Residents also participated in care by conducting assessment phone calls with patients calling the clinic with dental concerns. Residents learned to triage and classify dental emergencies and urgent care cases based on ADA interim guidelines. Emphasis was placed on gathering pertinent patient information to come up with working diagnoses before scheduling patients to minimize appointment times and overall exposure. Residents were tasked with leading virtual weekly case reviews. A thorough medical and dental history was presented for each patient that was seen in the clinic that week. Dental treatment that was proposed or completed to clear them to proceed with their cancer care was outlined and discussed with the faculty. Detailed discussions took place surrounding the modifications that had to be made in their oncologic and dental care as a result of COVID-19. Although not ideal, these modifications enabled the residents to effectively continue their dental and oral oncology training during the pandemic.

#### **3. Conclusions**

#### *3.1. Teamwork Is Integral to Ensure Timely and Optimal Coordination of Care*

Managing the oral health of cancer patients requires timely coordination of care between surgeons, radiation oncologists, medical oncologists, radiologists, pathologists, dentists and maxillofacial prosthodontists. For example, we have previously documented that stem cell transplant patients may have a narrow window of adequate disease control for successful transplantation [26]. Similarly, the time from a head and neck cancer diagnosis to the initiation of radiation therapy correlates with survival [27]. As a result, timely dental clearance of cancer patients is integral to their overall cancer care. While such coordination of care was routinely performed prior to the pandemic, the unprecedented outbreak of COVID-19 posed several logistical challenges and uncertainties in dental and oral healthcare delivery models. Therefore, the importance and the value of teamwork and communication between dentists and medical professionals cannot be understated.

#### *3.2. The Road Ahead*

We have recently begun resuming our clinical services in a phased manner with modified clinical workflow while maintaining social distancing guidelines in our clinic waiting rooms and continued incorporation of infection control procedures in our clinic areas. At the present time, clinical care is provided with staggered appointments while simultaneously managing unscheduled consultation requests and emergencies. Roswell Park currently offers COVID testing on-site by scheduled appointment, drive-up or in an expedited manner at point-of-care for cancer patients based on clinical need. As a result, we have routinely begun COVID testing our dental clinic patients. These modifications have enabled us to safely provide dental care to cancer patients while ensuring

that they adhere to their planned cancer treatment. However, it is now being increasingly recognized that the impact of COVID-19 is likely to be long-standing (several months to years) with a possibility of a second wave of infections in the fall. As we gradually progress to a "new normal", evaluating the impact of these optimized practices and processes within the dental clinic will be important. Given the planned scale-down of our clinic operations, the number of patients seen by our clinic during this time was reduced. We are currently reviewing our clinic volume data (number of appointments, number and type of procedures performed) during March–September 2020 and comparing it to our "pre-COVID" (March–September 2019) metrics. Such a comparative assessment would have to take additional variables into consideration, including number of active providers (dentists and specialists) on staff, number of residents and so on., to recognize the true impact of COVID-19 on our practice. Equally important is measuring the impact of these practice modifications on patient outcomes and evaluating the overall impact of these changes to clinical workflows on patient experience. The impact of COVID-19 on healthcare economics for dentistry and oral medicine also warrants further investigation. In this regard, we have recently begun examining the financial consequences of COVID-19 on our clinical practice through a review of our billing records. We continue to closely monitor the impact of our clinic measures on treatment-related oral health complications and outcomes in cancer patients and hope to report our findings in the future.

**Author Contributions:** S.M., N.T., H.C. and M.S.: Contributed to conception or design, drafted and critically revised the manuscript. M.A., V.F., M.H., S.A., V.G., K.E.W., M.R.M., A.K.S. and W.L.H.J.: Contributed to conception or design and drafted the manuscript. All authors gave their final approval and agree to be accountable for all aspects of the work. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by Roswell Park's Cancer Center Support Grant from the National Cancer Institute P30CA016056 and 3R01DE024595-05S1 from the National Institute of Dental and Craniofacial Research.

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

#### **References**


© 2020 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 (http://creativecommons.org/licenses/by/4.0/).

### *Article* **Children's Dental Anxiety during the COVID-19 Pandemic: Polish Experience**

**Aneta Olszewska 1,\* and Piotr Rzymski 2,3,\***


Received: 14 July 2020; Accepted: 25 August 2020; Published: 25 August 2020

**Abstract:** Dental fear and anxiety is a significant issue that affects pediatric patients and creates challenges in oral health management. Considering that the coronavirus disease 2019 (COVID-19) pandemic, along with its associated sanitary regime, social distancing measures and nationwide quarantines, could itself induce public fears, including in children, it is of great interest to explore whether this situation and the necessity of reorganizing dental care could potentially affect the emotional state of pediatric patients facing a need for urgent dental intervention. The present study assessed the emotional state of children ≤ seven years old (*n* = 25) requiring dental healthcare during a nationwide quarantine in Poland, as well as the anxiety levels of their caregivers. The Faces Anxiety Scale was adopted, and the evaluation was independently performed by the dentist, caregivers and children themselves. The level of anxiety in caregivers was also measured. As demonstrated, children requiring dental intervention during the nationwide quarantine did not reveal a significantly higher anxiety level as compared to the age- and indication-matched pre-pandemic control group (*n* = 20), regardless of whether their emotional state was evaluated by the dentist, caregivers, or by themselves. However, the share of children scoring the lowest anxiety level in all assessments was smaller in the pandemic group. Boys in the pandemic group had a higher anxiety level, as indicated by a caregiver assessment, and displayed a negative correlation with age in all three types of evaluation. Moreover, caregiver anxiety levels were higher in the pandemic group as compared to the pre-pandemic subset and revealed stronger correlations with the dental anxiety in children. The results suggest that the reorganization of oral healthcare under the pandemic scenario did not have a profound effect on children's dental anxiety. Nevertheless, findings in young boys highlight that they may be more vulnerable and require special care to mitigate their anxiety and decrease the risk of dentophobia in the future—these observations must be, however, treated with caution due to the small sample size and require further confirmation. Moreover, it is important to reassure caregivers of the safety of the dental visit during the pandemic to minimize the effect of their own anxiety on dental fears in children.

**Keywords:** COVID-19; SARS-CoV-2; dental care; children; dentist-patient relation; pandemic

#### **1. Introduction**

The outbreak of the novel coronavirus disease COVID-19 in December 2019 that spread across the Asian continent and eventually turned into a pandemic [1,2] created numerous challenges in health care sectors unrelated to the management of infectious diseases, including dentistry [3–7]. Following the confirmation of the first case in an increasing number of countries, the physical infrastructure, including entire hospitals, hospital wards, beds and technical equipment, had to be repurposed. The workforce resources in health care have also undergone reorganization and

reallocation to support the response to the pandemic. This has led to the limitation or postponing of non-emergency health care appointments and treatments. In the meantime, the rapidly evolving epidemiological situation has forced numerous countries to implement strict sanitary regimes and social distancing measures, and eventually impose nationwide quarantines to decrease transmission rates. Under such circumstances, and particularly lockdown-associated isolation, significant public distress can be seen, further magnified by mass media coverage, often based on sensational, panic promoting headlines, as well as by online social media through which the spread of unsupported claims and fake news could be seen [8–10]. This stress is not only related to a fear of contracting the disease but also to significant and rapid changes to lifestyle and work [11]. As already demonstrated, all of these factors can be so profoundly affecting that a relevant percentage of individuals are put at risk of less or more severe mental health issues [12], including children and their parents [13–16]. Moreover, one study in adults has already reported that the introduction of the pandemic caused anxiety in 25% of dental patients [17]. However, no research has specifically addressed dental anxiety levels during COVID-19, including that in children.

During the COVID-19 pandemic, children suffer from not going to kindergartens and schools, not having real contact with their friends and some family members and having to live at home with decreased ability to practice physical activity and carry out some of their hobbies. As shown in an Italian survey, a significant percentage of children become nervous when hearing about the pandemic (e.g., on television) [18]. To protect them from distress, parents might often avoid discussing the pandemic, although the research supports that sensitive communication during the crisis has benefits for children's wellbeing [19,20]. In addition, their emotional state can closely reflect that of caregivers, further adding to anxiety level [21].

Providing children with dental care during the COVID-19 pandemic, and in particular during the increased social restrictions, can be a challenging task. It is known that appointments are often met with dental fear and anxiety, while 7–8% of children in pre- and early school age display it at a level which might interfere with dental procedures [22,23]. This primarily originates from fears of procedure and pain [24–27], but under pandemic-related lockdown these emotions and feelings can potentially be further exacerbated by the new stressors present in their environment as well as by the psychological tension resonating from the caregivers who need to take a decision to leave home and potentially risk contracting SARS-CoV-2. Moreover, in the regular setting, there is a possibility of the effective management of children's fear, anxiety and phobia with the support of caregivers and through desensitization, tell-show-do, positive reinforcement, and other behavioral techniques [26,28]. As the main route of SARS-CoV-2 transmission is via airborne droplets, dental staff are required to use personal protective equipment (PPE), i.e., suits, goggles, face visors, and face masks. The PPE affects the voice tone, makes it more difficult for children to understand what a dentist is communicating, does not allow children to read facial expressions which are important for building their trust with a dentist, adds to white coat syndrome, and overall hinders interaction with the patient [7]. Although some techniques to manage the anxiety level are still possible and still performed, the additional safety measures may effectively worsen the relationship between pediatric patients and personnel.

Survey studies reported that 50–70% of dental professionals admit to experiencing higher stress and anxiety levels as a result of the COVID-19 pandemic [29,30], an effect that may, in turn, alter their relationship with the pediatric patient. All of this, along with empty dental clinics and the smell of ozone disinfectant, can affect the children's trust in and perception of the oral healthcare provider, particularly in patients with a high fear level, and potentially aggravate the possibility of reassuring and de-stressing them in the waiting room and dental office, and eventually this may reinforce dental anxiety.

The present study aimed to explore the level of anxiety in children and their caregivers during dental visits at the time of the nationwide quarantine in Poland. The first COVID-19 case in the country was confirmed on 4 March 2020. Following this, schools and universities were closed on 11 March and a nationwide quarantine was imposed on 24 March. The lockdown lasted till 4 May when hotels and shopping centers were permitted to reopen while on 6 May daycare centers and kindergartens were allowed to resume their activities. Despite the easing of social distancing rules, dental care will continue to be provided with new sanitary regimes. Evaluation of the emotional state of young patients and their caregivers during the pandemic and related nationwide lockdown is important to understand whether the additional safety measures can affect dental fear and to discuss the strategies that could effectively decrease this.

#### **2. Experimental Section**

#### *2.1. Study Design*

The study was designed to explore the emotional state of 25 children aged four–seven who required intervention at the Pediatric Dentistry Clinic at Poznan University of Medical Sciences, Pozna ´n, Poland, during the nationwide quarantine in Poland (pandemic group), and to compare it to an age- and an indication-matched group of pediatric patients before the COVID-19 pandemic (pre-pandemic group). The pre-pandemic group used for comparison consisted of 20 children aged four–seven requiring dental intervention between January and June 2018. The level of anxiety related to the dental visit was also assessed in caregivers in both groups, as they remain in a close emotional relationship with their children and can affect each other. The following medical indications for dental appointments were considered in both groups of pediatric patients: tooth extraction, abscess, dental trauma (traumatic injury to orofacial tissues), mucosal lesion, and necessity of performing pulp treatment. All children enrolled in the study had a dental history of no more than three appointments, no history of chronic disease and no mental disorder. The following descriptive variables of the studied children were collected: age, sex, and medical indication for dental intervention.

The anxiety levels in the pandemic group was evaluated between 24 March and 30 April 2020 (pandemic group). At the time the study was initiated, COVID-19 infections were active in 195 countries and territories, including Poland, with 425,675 cases and 19,195 deaths confirmed globally. During the time the study was conducted, the total number of confirmed infections and fatal cases in Poland increased from 901 to 12,877 and from 10 to 644, respectively. This period represents the strictest national lockdown, which was imposed from 24 March with some restrictions lifted at the beginning of May when hotels, shopping centers, daycare centers, and kindergartens were permitted to reopen. During this period, the following modifications to dental healthcare procedures were undertaken:


All caregivers and children in the pandemic group adhered to the above-mentioned rules.

The purpose and protocol of the study were explained to every child and their supervisor. Participation in the research was entirely voluntary. Prior to participation, all supervisors were asked to give their written informed consent. The supervisor accompanied the child during the emotional assessment. The study protocol was submitted to the Bioethical Committee at Poznan University of Medical Sciences - according to the performed evaluation, it lacked the characteristics of a medical

experiment and, in line with Polish law and the Good Clinical Practice, it did not require specific approval by the Bioethics Committee.

#### *2.2. Emotional State Evaluation*

The emotional state of children was evaluated in the waiting room prior to dental procedures by a caregiver, dentist and by the child. The whole procedure took max. 15 min. Dentists and caregivers independently assessed the children's emotional state using the faces mood scale (Figure 1). The scale was prepared by a graphic artist according to the facial muscle changes involved in a fearful expression and based on photographs of faces showing increased fear [31]. The evaluating individual selected one of the six drawn faces that suited the child's emotional state. The drawings were numbered as follows: 1—calm; 2—uncertain; 3—reserved, closed and uncooperative; 4—avoiding; 5—loud; 6—crying. The pediatric patients, given the paper with a blank face (Figure 1), were asked to complete the drawing by adding the facial elements: eyes, nose and lips. Prior to this, all children were instructed that a drawing should express their own emotions before the dental appointment. The dentist then categorized the children's drawings to the corresponding faces 1–6, mostly by matching eye and lip expressions. Such a graphical approach in the evaluation of the emotional state of children appears to be advantageous compared to the numerical scale assessment - it only requires simplified verbal instructions and is more accessible for children to understand than a translation of their inner state to a particular numerical score [32]. It has also been demonstrated that children and their caregivers tend to prefer the faces scale over other evaluation methods [33,34]. The numbers associated with each drawing were operationalized by transforming them into 1–6 Likert scales, where 1 and 6 indicated the lowest and highest level of anxiety, respectively.

**Figure 1.** The graphical scale used to assess the emotional state of pediatric patients before the dental appointment (**A**) and a blank face (**B**) used by children to express their own emotional state by drawing missing elements: eyes, nose and lips.

Additionally, the caregivers were asked to assess their own level of anxiety related to the dental visit by using a Likert scale 0–10, where 0 corresponded to lack of fear, 5 indicated medium anxiety, while 10 represented a very high level of anxiety.

#### *2.3. Statistical Analysis*

The statistical analyses were performed using Statistica v.13.1 (StatSoft Inc., Tulsa, OK, USA). Because age did not meet the assumption of Gaussian distribution (Shapiro–Wilk test; *p* < 0.05) and the emotional state of children was measured in the ordinal scale, non-parametric methods were employed. The differences in the emotional state scores in pandemic and pre-pandemic groups, as well as between boys and girls, were assessed with the Mann-Whitney U test. The association between children's age

and the scores were evaluated using Spearman's rank correlation coefficient (Rs). The differences in the prevalence of medical indications for dental intervention in the pandemic and the pre-pandemic group were assessed by Pearson's χ<sup>2</sup> test. A value of *p* < 0.05 was considered statistically significant.

#### **3. Results**

The pandemic group consisted of 25 children: 15 boys (mean ± SD age 5.1 ± 1.1 years) and 10 girls (mean ± SD age 5.3 ± 0.9 years). The pre-pandemic group consisted of 10 boys (mean ± SD age 4.5 ± 0.8 years) and 10 girls (mean ± SD age 5.6 ± 1.1 years). The comparative age of the two groups did not differ (*p* > 0.05, Mann-Whitney U test). The demographic breakdown of medical indications for a dental visit in both groups is summarized in Table 1. The prevalence of these indications did not differ between the studied groups (*p* > 0.05, χ<sup>2</sup> test in all cases); tooth extraction was the most frequent procedure (Table 2).

**Table 1.** Spearman's rank correlation coefficient calculated for the level of anxiety in the pre-pandemic (*n* = 20) and pandemic group of children (*n* = 25) before the dental appointment assessed by the dentist, caregivers and children themselves. All values are statistically significant.




The emotional state of children in the pandemic group did not differ from that in the pre-pandemic group, either when assessed by the dentist [median (interquartile range, IQR): 3 (2–5) vs. 2 (1–4)], caregiver [3 (2–5) vs. 3 (2–5)], or the children themselves [3 (2–4) vs. 2 (1–3)] (*p* > 0.05 in all cases, Mann-Whitney U test). However, the percentage of children for whom the highest anxiety score of 6 in the pre-pandemic and pandemic groups was 20.0 and 12.0% (dentist's evaluation), 20.0 and 16.0% (caregiver's evaluation) and 10.0 and 24.0% (self-evaluation by children), respectively In turn, the lowest anxiety score of 1 in these groups was 30.0 and 16% (dentist's evaluation), 15.0 and 12.0% (caregiver's evaluation) and 40.0 and 24.0% (self-evaluation by children), respectively The summary of scores in each group given by dentists, caregivers and children is presented in Figure 2. The scores given by the dentist, caregivers, and self-reported by the children were all highly correlated in both studied groups of children (Table 2).

Moreover, the gender of children did not differentiate the level of their anxiety in either pre- or pandemic groups (*p* > 0.05 in all cases, Mann-Whitney U test) (Figure 3). The only exception was the assessment of children's anxiety performed by parents in the pandemic group, with a higher score given for boys than girls [median (IQR): 4 (3–5) vs. 2 (2–3)] (*p* < 0.05, Mann-Whitney U test). The comparison of each gender across the two groups yielded no differences in anxiety level (*p* > 0.05 in both cases, Mann-Whitney U test).

**Figure 2.** The emotional state of pediatric patients before the dental appointment in the pre-pandemic (*n* = 20) and pandemic group (*n* = 25) as assessed by dentists, caregivers and children themselves.

**Figure 3.** The emotional state of boys and girls before the dental appointment in the pre-pandemic (*n* = 20) and pandemic group (*n* = 25) as assessed by dentists, caregivers and children themselves. The bars represent median, the whiskers represent interquartile range.

However, as presented in Table 3, the percentage of boys in the pandemic group having the lowest and highest anxiety levels was respectively decreased and increased compared to the pre-pandemic subset in all three evaluations—such a phenomenon was not seen in the case of girls.

As shown in Table 4, a number of negative correlations were found between children's age in the pandemic group and the scores they were given, including their own assessment of emotional state. However, when differentiated by gender, these correlations were only significant for the subset of boys (Table 4). When evaluated by the dentist, caregivers and children themselves, the median (IQR) scores of anxiety in boys aged four from the pandemic group were 5 (5–6), 5 (5–6) and 4 (3–6), respectively, while for those aged seven, these scores were 1 (1–2), 2 (1–4) ad 2 (1–4), respectively.

A significant difference in the anxiety of caregivers accompanying children before and during the pandemic was observed with a median (IQR) level of 6 (4–8) and 3 (2–4), respectively (*p* < 0.01, Mann-Whitney U test). The number of caregivers indicating a score >5 (above the level of anxiety defined as 'medium') in pre-pandemic and pandemic groups was 1/20 (5%) and 13/25 (52%), respectively. The parental anxiety level in the pandemic group was positively correlated with children's dental anxiety as assessed by the dentist (Rs = 0.80, *p* < 0.05), the caregiver (Rs = 0.76, *p* < 0.05) and

self-evaluated by the children (0.74, *p* < 0.05). In the pre-pandemic group, positive correlations with the children's anxiety evaluated by caregivers (Rs = 0.57, *p* < 0.05) and children themselves (Rs = 0.72 *p* < 0.05) were observed.

**Table 3.** The percentage of boys and girls with the lowest and highest anxiety levels before the dental appointment in the pre-pandemic (*n* = 20) and pandemic group (*n* = 25) as assessed by dentists, caregivers and children themselves.


**Table 4.** Relationship between the age of pediatric patients and their fear as evaluated by dentists, caregivers and self-reported by children (Spearman's rank correlation coefficient).


\* *p* < 0.05; ns—not significant (*p* > 0.05).

#### **4. Discussion**

The present study is the first to report on the emotional state of children ≤ seven years during the COVID-19 pandemic. Its unique aspect is that it was specifically conducted during the strictest form of the nationwide quarantine. The previous research in adults has shown that dental patients reported feeling anxious about the pandemic, although this finding cannot be attributed directly to dental anxiety, and, contrary to our study, it did not investigate anxiety levels during the dental appointment [17]. In turn, dental fear and anxiety in children represent an important issue in dental management, and as hypothesized, fears related to the ongoing epidemiological situation and associated changes in the dental service organization could further potentiate them. This could be particularly expected given the fact that the emotional state of children is often influenced by that of their parents [35,36], and during the pandemic-related lockdown the fear of contracting SARS-CoV-2 during different activities, e.g., while shopping in the grocery store, were frequently reported [11]. On the other hand, the additional measures undertaken to shorten dental appointments via applying telemedicine, i.e., video/phone consultation to take medical history and talk through the proposed treatment, as well as efforts to make children as familiar as possible with the new sanitary regime during the dental visit, could possibly mitigate, at least to some extent, fear and anxiety in children. The observations of the present study indicate that children requiring dental intervention during the COVID-19 pandemic-related nationwide quarantine may not experience significant changes in their emotional state, as compared to the pre-pandemic, age- and indication-matched group. It should be however noted that the share of patients with the lowest anxiety level in all assessments was smaller in the pandemic group.

The emotional state of pediatric patients was evaluated in the present study by children themselves, but also by their caregiver and the dentist. Such an approach allows for a broader assessment of the child's inner state. As previously suggested by studies on pain intensity, self-reporting tools can be inaccurate for children younger than seven years due to poor understanding of the method and the skills needed to express their experiences not yet being fully developed [37,38]. Therefore, in such groups, complementary observational measures should be employed. In such a case, caregivers can be used as a proxy for patients' reports, especially in situations in which some communication barriers may exist. Finally, the assessment of the child by the dentist is also valuable as it is based on professional experience and not biased by the strong emotional relationship that exists between a child and a parent [39]. One should, however, note that a survey conducted in 30 countries reported increased levels of anxiety in dentists during the COVID-19 pandemic [29], and this may potentially alter their perception and assessment of the patient's emotional state. Importantly though, the present study demonstrated that the results on children's emotional state obtained using the face scale from the dentist, caregivers and self-reported by the pediatric patients generally agree with each other.

Previous research has related dental anxiety in children to various factors such as personality traits, increased general fears, a history of painful dental experiences, parental dental fears and other family-related factors [22,40,41]. Some studies have also found that it tends to be higher in girls than boys, and in younger children. These age and gender-related differences were, however, not always confirmed [42]. In the present study, gender-differences, with a higher level of anxiety in boys, were observed only in the group undergoing a dental procedure during the pandemic-related nationwide quarantine, and only when the assessment was performed by a caregiver. One should note that the percentage of boys in the pandemic group who displayed the highest and lowest level of anxiety increased and decreased, respectively, when compared to the pre-pandemic subset. Furthermore, the present study suggests that younger boys were the most vulnerable, as highlighted by the negative correlation of all anxiety assessments and their age, and the highest scores seen in patients aged 4. This is an interesting finding since general anxiety levels tend to be higher in girls during early childhood [43]. It can be hypothesized that under the pandemic scenario it may be more challenging to explain the nature of the situation to younger boys than girls, due to the difference in the development of their language skills [44–47]. As reported, four-year-old boys reveal a significantly lower expression of pivotal factors for human communication, such as FOXP2 protein [48]. Nevertheless, the present results highlight that special care may be needed for younger boys requiring a dental intervention during pandemic in order to mitigate their anxiety and decrease the induction of potential dentophobia in the future. One should however stress that implementation of any mitigation strategies in this regard should only be considered if the present results, based on small sample size, would find confirmation in future studies.

Importantly, the present study clearly shows that parental anxiety levels are correlated with the emotional state of children and that this association was stronger during the pandemic. The percentage of caregivers having anxiety above the medium level was over 10-fold higher in the pandemic group when compared to the pre-pandemic subset. Increased anxiety in adults during epidemiological events is not uncommon and has been observed previously, e.g., during the H1N1 pandemic in 2009–2010 [49–51]. Unsurprisingly, it has also been reported during the COVID-19 pandemic [52–54].

In turn, previous dental studies show that parents play a key role in children's anxiety and development [55–57]. Therefore, it is of high importance, particularly during the pandemic, to ensure that caregivers of pediatric patients are fully aware of these links and to educate them on how to make a dental visit a more comfortable event for children. Considering that parental anxiety levels in the pandemic group were higher than in the pre-pandemic group, it can be suggested that fears related to COVID-19 and contracting SARS-CoV-2 were responsible for this effect. It is, therefore, necessary for healthcare professionals to explain, prior to the appointment, all the measures undertaken to maximally limit the risk of infection in the dentist's surgery and to reassure patients of their safety. This can be achieved with a phone or video call preceding the dental visit during which medical history is also recorded.

Although the present study reports on the important issue of dental healthcare under a pandemic scenario, the study limitations must be emphasized. Firstly, the results represented a single-center experience and were obtained from a small population size. Moreover, dental anxiety in children is multifactorial, and this research did not explore the effect of personal traits and family-related issues, including socioeconomic status and level of education of caregivers [40,41,58–60]. Moreover, transforming the Faces Anxiety Scale into the Likert scale allowed for a more in-depth statistical elaboration of the results, although the study was not designed to delve into explaining the exact reasons for the observed anxiety levels in children. This would require additional questions, time spent in the dental clinic, and communication approaches that were challenging to apply during the dental clinical practice under the scenario of the most strict form of the COVID-19 related quarantine.

#### **5. Conclusions**

This is the first study to report on dental anxiety in children during the strictest form of the COVID-19 lockdown. In general, the present research indicates that, contrary to the concerns that pediatric children will be significantly more stressed due to dental appointments during a nationwide quarantine related to the COVID-19 pandemic, their anxiety levels, assessed by the dentist, caregivers and by themselves, did not differ from the pre-pandemic group of pediatric patients. Nevertheless, the percentage of children having the lowest level of anxiety in all employed assessments decreased in the pandemic group. The results suggest that younger boys may potentially be more vulnerable in this regard—this finding should be treated with caution and would require further confirmation in larger-scale studies. Moreover, parental anxiety levels were highly associated with the emotional state of children, particularly during the pandemic period. It seems reasonable to make parents aware of this association and, further, to reassure their safety by explaining that the risks of contracting an infectious agent during a dental visit are mitigated by appropriate measures.

**Author Contributions:** Conceptualization, A.O.; methodology, A.O.; validation, A.O. and P.R.; formal analysis, investigation, A.O. and P.R; writing—original draft preparation, A.O and P.R. All authors have read and agreed to the published version of the manuscript.

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

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

#### **References**


© 2020 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 (http://creativecommons.org/licenses/by/4.0/).

*Review*
