**Table A1.** Search strategies. **Search Strategies**







**Table A3.** *Cont.*


### **References**


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International Journal of *Environmental Research and Public Health*

### *Commentary* **Patient and Public Involvement in Sexual and Reproductive Health: Time to Properly Integrate Citizen's Input into Science**

**Miguel García-Martín 1,2,3, Carmen Amezcua-Prieto 1,2,3,\*, Bassel H Al Wattar 4,5, Jan Stener Jørgensen 6, Aurora Bueno-Cavanillas 1,2,3 and Khalid Saeed Khan 1,2**


Received: 21 September 2020; Accepted: 28 October 2020; Published: 31 October 2020

**Abstract:** Evidence-based sexual and reproductive health is a global endeavor without borders. Inter-sectorial collaboration is essential for identifying and addressing gaps in evidence. Health research funders and regulators are promoting patient and public involvement in research, but there is a lack of quality tools for involving patients. Partnerships with patients are necessary to produce and promote robust, relevant and timely research. Without the active participation of women as stakeholders, not just as research subjects, the societal benefits of research cannot be realized. Creating and developing platforms and opportunities for public involvement in sexual and reproductive health research should be a key international objective. Cooperation between healthcare professionals, academic institutions and the community is essential to promote quality research and significant developments in women's health. This cooperation will be improved when involvement of citizens in the research process becomes standard.

**Keywords:** patient and public involvement; women; health; research; international collaboration

### **1. Introduction**

Evidence-based sexual and reproductive health requires a global effort, with political and societal actions. A comprehensive paradigm shift is needed, where not only health professionals and researchers are ready to implement citizen participation, but also where political and administrative control of the health system allows and supports it [1]. Public and patient involvement is a field where policy has tended to outpace evidence. Exploring the impact of citizens in research is limited to investigating researchers' and public and patient contributors' reports of their views and experiences. Objective techniques for evaluating the impact and its influences remain hard to reach in a process that is inherently relational, subjective and socially constructed [2]. Public and patient involvement is as an expression of a democratization of healthcare, and a political and managerial tool to ensure quality, documentation, and equal treatment, thereby governing and controlling a public healthcare system. For example, the Danish public healthcare system is increasingly influenced by politicians. The use of standardized schemes and checklists used for documentation and quality assurance underlines this development, and patient and public involvement might be seen as adding to this movement [1].

The future worldwide vision is focused on building healthier lives, driven by the evidence-based provision of evidence-based healthcare to improve citizen's quality of life [3] However, evidence-based medicine faces challenges due to: lack of proper patient and public involvement or public and participant involvement (PPI) in research, leading to poor buy-in [4]; lack of incorporation of patients' lived experiences in research outcomes, reducing the relevance of evidence [5]; and lack of recommendations for shared decision-making in guidelines leading to ineffective communication between health workers and patients [6].

In the last decade, the incorporation of public participation initiatives has shown the potential to improve the quality and the object of research, allow a wide dissemination of the findings found, and promote a better integration of the results in clinical practice [7–9]. Public participation also allows an approach to sensitive phenomena such as sexual and reproductive health, or ethical aspects that arise during the development of the study [7].

Significant development of women's health requires international collaborations and participation of women in the research process. To improve sexual and reproductive health research, our objective should be to establish the importance of creating and developing the platforms and tools for public involvement. In this sense, creation of new tools and platforms involving a combination of traditional outreach and online strategies. Face-to-face invitations, training meetings, local civil society organizations (CSO) and family medicine health center support can be combined with online tools, such as online announcements, use of google meet, hangout or zoom, and social media platforms (Facebook, Twitter). These tools offer opportunities for community members to engage in interactive ways and can bring new input from the patient and participant involvement process.

### **2. Evidence-Based Sexual and Reproductive Health**

Reproductive health (RH) was defined in 1994 at the International Conference on Population and Development as a "state of complete physical, mental and social well-being and not merely the absence of disease or infirmity, in all matters relating to the reproductive system, and to its functions and processes" [7]. Sexual and reproductive health (SRH) includes a number of health problems, such as (1) family planning; (2) maternal and newborn health care; (3) prevention, diagnosis and treatment of sexually transmitted infections (STIs) [8]; (4) adolescent sexual and reproductive health; (5) cervical cancer detection; and (6) prevention and management of infertility [9]. The World Health Organization include the Sexual and reproductive health in the health topics and highlighted that 'Sexual and reproductive health is a very personal subject, so people may have trouble finding or asking for accurate information about it. This may also help explain why these issues are still not addressed openly, and services are inadequate, fragmented and unfriendly in some countries in the European Region' [10]. Sexual and reproductive health services aim to prevent poor sexual and reproductive health, such as complications of pregnancy and childbirth, unwanted pregnancies, unsafe abortions, complications caused by STIs, sexual violence, and women dying from preventable cancer [10].

Reproductive health, including sexual health, and reproductive rights, as well as gender equality and women's empowerment, are relevant to improving the quality of life for everyone [7] as affirmed at various international forums, such as the International Conference on Population and Development (ICPD) and The Fourth World Conference on Women: Action for Equality, Development and Peace [11,12]. The Millennium Development Goals related to maternal and child health have still not been achieved in many countries; considering 35 countries, less than 30 percent of women of reproductive age use modern contraceptive methods. The method choice is still limited in many countries, due to lack of access or provider biases. Although there are good options for safe abortion, these services remain unavailable in many countries due to legal barriers, lack of training, and stigma. However, significant progress has been made in improving reproductive health. For example, family planning has expanded around the world, spurring a broader coverage of services with greater emphasis on quality and human rights; adolescent sexual health has been addressed with effective

messages and services and new approaches try to reduce gender-based violence and clinical and policy guidelines have been incorporated [11].

The 2020 Sustainable Development Goals Report in goal five (gender equality) highlighting that there is still a lack of decision-making power for women, extending to their own reproductive health and that slightly more than half of all women (55%) make their own decisions when it comes to sexual and reproductive health and rights, based on 2007–2018 data from 57 countries on women aged 15 to 49, who are either married or in union. The analysis also found that only three in four women are making their own decisions regarding health care or on whether or not to have sex [12]. United Nations Member States have moved on to confirm their commitment to Sustainable Development Goals (SDG) including its targets designed to "ensure universal access to sexual and reproductive health (SRH) care services, including for family planning, information and education, and the integration of reproductive health into national strategies and programs by 2030" and to "ensure universal access to sexual and reproductive health and reproductive rights" [9].

Patient and public involvement in research could be an approach to effectively address poor sexual and reproductive health outcomes among women [13]. This enables researchers to identify better strategies, focusing, for example, on culturally and contextually appropriate research and prevention, equitable access to effective sexual health information, or quality education and training for public health professionals. The health, demographic change and well-being programs [14] are committed to the implementation of research to improve maternal and child health. Public participation and involvement in the investigation of pregnancy and childbirth differ from those under chronic diseases, especially because motherhood is a transitory health experience in the life of women and their families [4]. Women can have a variety of experiences in their pregnancy and delivery, ranging from low-risk, home birth without intervention to prolonged hospitalization with long-lasting morbidity [15]. Their own experience will influence your attitudes and inevitably your contribution to research. Their participation should guide the priority areas for users of health services. Moreover, the Faculty of Sexual and Reproductive Healthcare of the Royal College of Obstetrician and Gynaecologists values patient and public involvement in the development of clinical guidelines. It actively considers patient and public involvement across all stages of the guideline development process, from consulting with individuals on the proposed scope of the clinical guideline through to getting feedback on patient summaries. In order to facilitate patient and public involvement, a variety of methodologies (e.g., questionnaires, focus groups, interviews) across different settings (e.g., clinics, online, community) are considered [16].

### **3. Patient and Public Involvement**

Effective patient and public involvement can be defined as where research is "being carried out "with" or "by" members of the public" not just "to", "about" or "for" them" [17]. The involvement process needs to change from an ad-hoc informal consultation into an established partnership underpinned by dedicated systems and infrastructure [18]. It must be implemented throughout the research lifecycle from idea generation, prioritization and commissioning into research conduct, publication and implementation in clinical practice [4,19].

It has been known for some time now that patient and public involvement has an important role in the identification of specific research questions [20,21], and that subsequent requests for research funding are more successful. Furthermore, it may be that public participation reverses in the reformulation of research questions [22], or even in the abandonment of a research project request if the involvement suggests that the research questions are not meaningful to the patient, public or citizens [23]. Additionally, patient and public involvement improves trial design [24], by ensuring that the design is acceptable to potential participants [25], facilitates recruitment for studies [26] and allows access to underserved and rarely heard populations, and patient and public involvement helps to disseminate the research results [27]. In short, patient and public involvement increases researchers' confidence in their studies [24] and promotes a greater understanding of the patient's perspective [28].

Internationally, there is increasing recognition of the importance of involving patients and the public in health-care governance and research [29]. Policymakers give the relevance to patient and public involvement as characterized by the phrase 'nothing about me without me' [30]. Thus, local [31] and international organizations, such as 'The European Patient's Forum' or 'The International Association for Public Participation' [32,33] are beginning to harness the power of participation by health service users, promoting public participation in research planning and the development of resources and information to support citizen participation and patient engagement. Promoting the role of patients in health research lifecycle has been at the heart of various international efforts including the European Network for Health Technology Assessment [34] and the Innovative Medicines Initiative which have called for better patient and public involvement in research synthesis projects across Europe [35]. Recently, the European Patients' Academy (EUPATI), a pan-European project was established as a collaborative public–private multi-stakeholder partnership of pharmaceutical industry, academia, and not-for-profit patient organizations [36]. These initiatives have developed various tools, platforms, and training resources for patient advocates to improve their participation in research with focus on four areas: pharmaceutical industry-led medical research, ethics committees, regulatory authorities, and health technology assessment. In turn, prestigious journals such as the British Medical Journal (BMJ) have also emphasized the use of patients and citizens as editors and emphasize the need for patients to participate as co-authors in the articles that are published [37].

Involving lay volunteers for problem-solving provided insights enhanced research design and served to identify weaknesses and barriers. Tensions and barriers have been generated with patient and public involvement in research [38]. On one hand, shared tensions usually are due to unclear roles, absent reporting guidelines, exclusion, framework limitations, resource allocation, and administrative boundaries. For example: active public involvement in the decision-making process of designing trials is less common than consultation on what has already been decided. Volunteers report needing early involvement to propose constructive changes. Researchers' worries about aggressive patients and those without respect for rules of confidentiality or data protection held up the research. Researchers may feel overwhelmed when they cannot fulfill the expectations they have over patients and public involvement [39]. On the other hand, shared barriers include those imposed by cultures, values, and power hierarchies. Limited involvement of the health community may occur through coalitions, collaborations, and partnerships [38].

Because research literacy could be an inconvenience in the process of patients and public involvement, some suggestions for getting the best from public involvement have been published [38]: ongoing support and implementation; training/capacity building; inclusion process; building trust and community and reinforcing patients' value and validity. In the second suggestion, capacity building, it is necessary to (1) provide training in research literacy and ethics, drawing on the many training programs that are available, (2) at every meeting have a jargon bin, when an unfamiliar term comes up, define it and use this to build glossaries, (3) promote a reciprocal learning relationship, letting volunteers know that researchers have made a long-term commitment to the patient and public partnership in research, and (4) encourage realistic expectations in volunteers and researchers and manage relationships with respect. Moreover, the use of patient and public involvement in dissemination planning, design, implementation, and distribution could increase public involvement, contribute to health literacy, and expand knowledge for patient values and preferences. The addition of patient reviewers by journals may contribute to health literacy and provide insights for future participatory research practice [38].

### **4. Public Involvement in Research to Address Gaps in Evidence**

There is growing recognition of the importance of experiential knowledge being approached alongside scientific knowledge [40]. Patient and public involvement throughout the research lifecycle and in research syntheses, such as systematic reviews and clinical practice guidelines, is being demanded by funders, but there is often an intrinsic resistance in the field of biomedical research [41]. For example, the chief investigator who expressed skepticism about patient and public involvement, focused mainly on using public engagement to meet funding requirements or by including them on trial steering committees, whereas those who valued patient and public involvement often described in detail how it was of benefit within their trials [2]. Translation and effective implementation of evidence into practice through requires careful planning in consultation with patients as key stakeholders. When involving patients, it is imperative to take the perspective of the patient and their way of life as a starting point. Patient participation is achieved by inviting them to participate in their treatment and care, and in the research that surrounds them. It requires health professionals to be involved in the daily life of their patients, but it also requires organization and shared decisions that promote patient participation in daily clinical practice [1]. Then, establishing patients as a stakeholder group in a true partnership with researchers is the key to addressing these challenges [42,43]. Health research funders and regulators are promoting patient and public involvement in research and research syntheses [29]. However, many clinicians, researchers, systematic reviewers and guideline makers still do not have the tools required to involve patients. It is not always recognized that through their lived experiences and social background, patients can positively be involved in research with their unique perspectives, increasing its impact on society [44].

Another aspect of interest that must be taken into account is that, in the past, the choice of results in research studies was driven by researchers who did not consider the participation of patients or citizens [6]. This practice has often led to heterogeneity, making it difficult to synthesize research, replicating the same studies, and increasing research waste [5]. The implementation of core (standardized) sets of important outcomes for each health condition has been suggested as a possible novel solution to this problem [45]. A core outcome set (COS) is a minimum consensus-based set of results that should be measured and reported in all clinical trials for a specific health condition or intervention [46]. Issues related to outcome assessments, such as selective reporting and inconsistency between studies, can be addressed by developing a core set. Development requires reaching a consensus on: (1) core outcome domains and (2) core outcome measurement instruments. Besides, methods used to reach consensus include systematic reviews of the literature to inform the process, qualitative research with physicians and patients, group discussions (for example, using the nominal group technique), and structured surveys (for example, using the Delphi technique). Multiple stakeholders must be involved in the process, and particular attention must be paid to patients [47]. Traditionally, the guidelines promoted by leading health experts have generated subjective recommendations that correspond to the provision of local, regional or national clinical care [48]. This has produced a limited effect on health outcomes and has promoted high and unjustified variation in the provision of care and services to users.

We have to adopt a novel approach by involving a wide range of key stakeholders of different disciplines with direct involvement in healthcare planning and provision for women and children. A strong level of cooperation is necessary via effective communication channels between healthcare professionals, academic institutions and the community [49]. Stakeholders and activities for participant involvement in research are shown in Figure 1. We suggest that these developments include clinicians (e.g., gynaecologists and paediatricians), methodologists (e.g., statisticians and systematic reviewers) and lay consumers (e.g., patients with lived experiences and civil society organization (CSO) representatives and related to sexual and reproductive health). Clinicians and professional bodies should promote patient and public participation in research helping to develop know-how in participants engagement. Methodologists—researchers, guideline makers and systematic reviewers included—will help in the scientific training of lay research enablers, to develop the local know–how on participant involvement in research. Lay consumers will provide the voice of lay sexual and reproductive health participants of all backgrounds to engage in the research process and to be involved in the dissemination of the research. The patient perspective is valuable to ensure quality in healthcare. However, the patient perspective is only one perspective, similar to the ones of other important groups (e.g., health professionals, leaders, administrators, politicians). A selected coordinator for patient and

public involvement is key to facilitating interactions. We agree with other authors, the coordinator should be experienced in the potential challenges of public and patient involvement, including power and control issues, and the consequences of public and patient contributors lacking knowledge of research processes, terminology, and ethical constraints [39].

**Figure 1.** Key stakeholders and activities in public and participant involvement (PPI).

Furthermore, patient and public involvement recruitment strategies are necessary, ensuring that we apply fair and transparent processes, that there is a shared understanding of the roles, offering support and learning for public participation in the research. For example: (1) women participating in actives randomized controlled trials; (2) women and men contacted from midwives who collaborate closely with the clinical institutions; (3) women and men with a disability or belonging to disadvantaged social classes; (4) social media, web sites and banners in health centers and nurseries to recruit participants and (5) civil society organizations (CSO).

The patient and public involvement should be made up of citizens and the public. They should receive advanced training on citizen participation in research, such as has been carried out within individual projects [4]. This training should include some important topics: (1) Introduction to health research; (2) Different types of research and study designs; (3) Perspective of the research from the citizen's point of view; (4) Research life cycle; (5) Different roles for the audience (participation, engagement); (6) Why involve the public in research (including diversity and inclusion in research); (7) Case studies: examples and public impact on research; (8) How to do research with the commitment of citizens; (9) How can the public do "citizen science"?; (10) How to maximize the impact of "citizen science"; (11) Solution of practical problems in the field; (12) Research dissemination and beyond; and (13) Measurement of the value and impact of citizen research. Developing these initiatives further, more citizens should receive basic training in citizen participation and the relevance of the investigation through dedicated training sessions. Patient and public involvement aims are varied depending on the research subject. Therefore, it is less common to involve patients and the public in the research process, than in other areas such as genetics, biobank research, cancer research, clinical trial research or decision-making [50]. The methodology mainly used for patient and public involvement in researching is information sharing, questionnaires, interviews or focus groups. Importantly, conducting a focus group at the beginning of the study and another at the end, you can identify the needs, barriers and feedback of the patient and public participations, trying to respond to how diversity impacts innovation, how to act to promote the inclusion of people with disabilities or from more disadvantaged communities, relationships between citizens, researchers and institutions, the type of language used to communicate and whether there have been unexpected opportunities. On the other hand, the research team is focused on the public and patient involvement of consultation, deliberation and participation [50].

To achieve quality results in the process of patient and public involvement in research, the Guidance for Reporting Involvement of Patients and the Public (GRIPP2) can be useful, the first international evidence-based, consensus informed guidance for reporting patient and public involvement in research [51]. There is a short and a long version of GRIPP2, that aims to improve the quality, transparency of the international patient and public involvement. The short form has five sections or topics: (1) Aim of patient and public involvement in the study; (2) Methods used in the public involvement in the study; (3) Study results: positive and negative; (4) Discussion, describing the positive and negative effects on the extent to which patient and public involvement influenced the study, and conclusions; and (5) Reflections/critical perspective, comment critically the things that went well and those that did not. On the other hand, the long form includes eight sections: (1) Abstract of the paper; (2) Background to the paper; (3) Aims of the paper; (4) Methods of the paper; (5) Measurement of the patient and public involvement: methods used to qualitatively and quantitatively measure or assess the impact of public involvement and methods used to capture or measure its impact; (6) Economic assessment of public involvement in the study; (7) Study results; and (8) Discussion and conclusions. This last section incorporates the reflections and critical perspective of the study. In order to improve current public involvement practice in the sexual health field, a recently published study carried out audits on patients and public involvement plans in the local sexual health service (*n* = 18), and a refined audit tool was completed in research projects (*n* = 5). The responses of the tools used in the audit showed a wide variability in practice. Problems included the combination of patient participation work and qualitative research, lack of goals in patient participation in research and lack of responsiveness around patient needs, and insufficient resources to work with patient and public involvement. Specific research problems included late participation of patients after key decisions had already been made [52].

At present, there are still some limitations about the evidence of the patient and public involvement research outcomes. In a systematic review, mapping the impact of the patient and public involvement in health and social care research [42], authors aimed to examine the conceptualization, measurement, impact and outcomes of patient and public involvement in health and social care research. This study provides the first international evidence of patient and public involvement impact that has emerged in the research process, however, much of the evidence concerning the impact remains weak.

It is important to remark that the "ReseArch with Patient and Public invOlvement: a RealisT evaluation" study (RAPPORT study) [53] aimed to determine the types of patient and public involvement in funded research, analyze the contextual and dynamics of patient and public involvement and explore the experience of patient and public involvement in research. They found that six striking actions were required for effective patient and public involvement: (1) A clear purpose, role and structure for patient and public involvement; (2) a key individual co-ordinating patient and public involvement ensuring diversity; (3) whole research team engagement with patient and public involvement, this is a research team positive about patient and public involvement input and engaged with it; (4) mutual understanding and trust between the researchers and lay representatives; (5) ensuring opportunities for patient and public involvement throughout the research process; and (6) and evaluating patient and public involvement in a proactive and systematic approach. Future work is required, exploring the impact of virtual patient and public involvement, economic evaluation of patient and public involvement, and a longer-term follow-up study of the outcomes of patient and public involvement on research findings and impact on services and clinical practice.

### **5. Clinical Relevance and Goals of Patient and Public Involvement in Research**

The most documented benefits of patient and public involvement in research are the involvement of the patient and public groups at all stages of the trial [39], utility in randomized controlled trials [2], contribution in the design of clinical trials [38], and perceptions of patient involvement in research and clinical practice [1].

In a qualitative study of patients and researchers from a cohort of randomized trials [2], 21 chief investigators, 10 trial managers and 17 patient and public involvement contributors were interviewed from 28 trials. The conclusions were that to enhance patient and public involvement in trials is crucial to develop goals for patient and public involvement at an early stage that fits the needs of the trial, plan patient and public involvement implementation in accordance with these goals, invest in developing good relationships between patient and public involvement contributors and researchers, and favor responsive and managerial roles for contributors. A systematic overview of public and patient involvement in clinical trials design included 27 reviews [38]. Public involvement roles were primarily based on agenda setting, steering committees, ethical review, protocol development, and piloting. Public involvement was reported to have increased the quantity and quality of patient relevant priorities and outcomes, enrolment, funding, design, implementation, and dissemination.

We would like to mention a couple of examples were patients and the public were involved in research. The first is a 3D study [39], where fourteen people living with multiple long-term conditions (multimorbidity) were included as patient and public involvement contributors to a randomized controlled trial to improve care for people with multimorbidity. Meetings took place approximately four times a year throughout the trial, beginning at the grant application phase. Their experience also supports the findings of the RAPPORT study [53] in four of the six conditions most influential in establishing effective patient and public involvement: (1) a research team positive about patient and public involvement, (2) a key individual to co-ordinate, ensuring diversity, and relationships that are established and maintained over time, (3) a shared understanding of moral and methodological purposes of patient and public involvement and (4) proactive and systematic evaluation of patient and public involvement. The second example is a secondary analysis of women's perceptions and experiences of egg aspiration in fertility treatment [1]. This secondary analysis was initially inserted in a randomized controlled study where the aim was to gain insight into perceptions and experiences within a group of women undergoing fertility treatment through two focus group interviews. They pointed out that knowledge and awareness of the difference in perspectives is important when healthcare professionals seek to involve patients both in clinical practice and in research.

Secondly, patient and public involvement in research has doubled the impact in trials: focused and diffuse [2]. Focused impact comprises patient and public contributors' input that, from the perspective of the informant, changed or influenced an aspect of the trial, whereas diffuse impacts comprise patient and public contributions that influenced the way researchers thought or felt about the trial. Focused impacts included patient and public contributors helping to choose the primary outcome for the trial and to increase recruitment through their contacts and networks. Diffuse impacts largely entailed interactions between researchers and patients and public contributors that helped to reassure the research team and increase or maintain their confidence and motivation for the trial.

Specific examples of the impact of patient and public involvement in researchers' professional lives are those where patients become co-authors in publications, co-applicants in projects call and trainers [4,54–56] or even becoming new editors in a prestigious journal, such as the BMJ Sexual and Reproductive Health [57], who wrote: 'Patient involvement is an important piece of cultural change in healthcare, and will require commitment, time and sensitivity, and a willingness to experiment and learn from mistakes'.

### **6. Conclusions**

Without the active participation of citizens, sexual and reproductive health research risks losing relevance and validity. Health research funders and regulators are promoting patient and public involvement in research but there is a lack of quality tools for involving patients. International collaborations, and the cooperation between healthcare professionals, academic institutions and the community are essential to promote quality research in sexual and reproductive women's health. A significant development in women's health will be achieved when the involvement of citizens in the research process becomes standard.

**Author Contributions:** Conceptualization, K.K.S., G.-M.M., B.-C.A.; original draft preparation, A.-P.C.; writing—review and editing, B.-C.A., G.-M.M., H.A.W.B., J.J.S. and K.K.S. All authors have read and agreed to the published version of the manuscript.

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

**Acknowledgments:** Professor Khan is Distinguished Investigator at University of Granada funded by the Beatriz Galindo (senior modality) program of the Spanish Ministry of Education. We would like to thank all women involved in health researching and those taking part in the development of the research process.

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

### **References**


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

© 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/).

International Journal of *Environmental Research and Public Health*

### *Brief Report* **Association between Sexual Habits and Sexually Transmitted Infections at a Specialised Centre in Granada (Spain)**

**Raquel Casado Santa-Bárbara 1, César Hueso-Montoro 2,\*, Adelina Martín-Salvador 3,\*, María Adelaida Álvarez-Serrano 4, María Gázquez-López <sup>4</sup> and María Ángeles Pérez-Morente <sup>5</sup>**


Received: 8 August 2020; Accepted: 19 September 2020; Published: 21 September 2020

**Abstract:** Sexually transmitted infections are an important public health issue. The purpose of this study is to analyse the association between different sexual habits and the prevalence of sexually transmitted infections in the population of Granada who consult with a specialised centre. An observational, cross-sectional study was conducted based on the medical records of 678 people from the Sexually Transmitted Diseases and Sexual Orientation Centre of Granada, who were diagnosed positively or negatively with a sexually transmitted infection, during the 2000−2014 period. Sociodemographic and clinical data, as well as data on frequency and type of sexual habits, frequency of condom use and sexually transmitted infection positive or negative diagnosis were collected. Univariate and bivariate analyses were conducted. The most popular sexual habits were vaginal intercourse, oral sex (mouth–vagina and mouth–penis) and the least popular were anus–mouth and anal sex. The use of condom is frequent in vaginal and anal sex and less frequent in oral sex. Sexually transmitted infection is associated with mouth–penis (*p* = 0.004) and mouth–vagina (*p* = 0.023) oral sex and anal sex (*p* = 0.031). It is observed that there is a relationship between the presence of STIs and oral sex practices, people having such practices being the ones who use condoms less frequently. There is also a relationship between anal sex and the prevalence of STIs, although in such sexual practice the use of condom does prevail.

**Keywords:** sexually transmitted infections; sexual behaviour; sexual health

### **1. Introduction**

Risky sexual habits and behaviour strongly affect public health. According to the WHO, more than one million people acquire a sexually transmitted infection (STI) every day. The most recent averaged data indicate that one out of 25 people has at least one STI, maybe being infected with several of them at the same time [1].

Complications derived from an STI have a great impact on children's, teenagers', and adults' health and life on a worldwide basis, thus compromising their quality of life. Furthermore, they facilitate indirectly the transmission of HIV and cause cellular changes that lead to some types of cancer. They also impact on domestic economy and national health systems [2].

STIs are more common in people having high-risk sexual behaviour and attitude such as having sexual intercourse without using condoms, having contact without buccal–genital protection, having multiple sex partners, having a high-risk partner (someone having many sex partners or other risk factors), having anal sex or a partner who has an STI, having sexual intercourse with sex workers, or having sexual intercourse with someone who injects or has injected drugs before [3,4]. Moreover, an increase in the use of the Internet and mobile applications to easily meet sexual partners, thus increasing high-risk sexual practices, should be highlighted [5,6].

Hence, it is important to know the population's sexual habits in order to prioritise sexual health strategies that shall reduce the incidence of STIs, and therefore reduce the morbidity and mortality load worldwide derived from sexually transmitted pathogens.

Research has focused on studying the use of condom and its effectiveness in people with high-risk sexual contact [7–9], however, there are only a few studies on general population, which show that they are less aware of risks and motivation for condom use decreases [10,11]. In the United States, among 15−44-year-old people, prevalence of anal intercourse slightly increased from 2002 to 2015 both in women (30–33%) and men (34–38%), condoms being used in 32% in women and 46% in men, and only 7% during oral sex; such low percentages regarding condom use in high-risk sexual practices lead to an increase in the likelihood of getting an STI [12].

In Spain, a Blanc et al.'s study [13] revealed that the use of condom is higher in vaginal intercourse, and diminishes in anal sex and it is used in a lower percentage during oral sex (29.2%, 17.0%, and 2.0%, respectively). These results support the idea that young people use condoms more to avoid pregnancy than to prevent STIs.

Most published studies address sexual habits, condom use, and prevalence of STIs independently [14–16]; therefore, the purpose of this study is to analyse the association between different sexual practices and an STI diagnosis in people consulting with the Sexually Transmitted Diseases and Sexual Orientation Centre of Granada (Spain).

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

An observational, retrospective and cross-sectional study was conducted based on the medical records of people consulting with the Sexually Transmitted Diseases and Sexual Orientation Centre of Granada, attached to the Andalusian Health Service (Spain). It is the STI reference centre in the Granada province, it belongs to the public health system and it carries out preventive, diagnoses-related and therapeutic activities.

The sample was taken from a database composed of 1437 medical records of subjects attending for consultation associated with the presence or suspicion of an STI between 2000–2014. The sampling and data collection process may be checked in detail in a previous publication [17]. From said database, 678 medical records were taken for this research, which records complied with the criterion of having a test made to confirm or rule out the presence of an STI. Each history corresponds to one subject, so that there is no duplicate information in the final case selection. Every history was reviewed by a member of the research team, who took out data to include them in a data collection sheet created to that effect for this study. One of the disadvantages of this process was related to missing data, so the sample sizes defined for every analysis performed are specified in the data results.

The STI diagnosis was considered a dependent variable, collected as a binary qualitative variable (Yes, No). Sexual habits were established as an independent variable, identifying five practices: vaginal intercourse, oral (mouth–vagina), oral (mouth–penile), oral (anus–mouth), anal (penile–anus) intercourse. Subjects were asked about the frequency of such practices, so every habit was collected as a binary qualitative variable (Never or sporadic, Frequent or always). Additionally, data on condom use were collected for each and every described practice, following the same categorization in answers. To classify the sample, sociodemographic variables (age, sex, nationality, occupation, working status, education level, marital status, and sexual orientation), medical variables (reason for consultation) and risk indicators (age of first sexual intercourse, last time having sex without a condom, number of partners in the last month and in the past 12 months, use of drugs, and prior STI) were collected.

A univariate analysis was conducted by calculating the median (Me), interquartile range (IQR), frequency (*n*), and percentage (%), according to the variable type. The bivariate analysis was performed in order to analyse the association between STIs (dependent variable) and sexual habits (independent variable), via the chi-square test, by calculating the effect size through the Cramer's V (V), plus the Odds ration (OR) (Confidence Interval (CI) 95%).

In every case, a significant association was considered with *p* < 0.05. Univariate and bivariate analyses were conducted using the Statistical Package for the Social Sciences (SPSS) program, version 22, (IBM, New York, NY, USA).

The study protocol was approved by the Biomedical Research Ethics Committee of the province of Granada (research protocol approved on 12 February 2012, and 1 April 2015), as well as by the Management Directorate of the Granada-Metropolitan Health District, to which the centre where data were collected is attached.

### **3. Results**

Table 1 shows results corresponding to sociodemographic variables, medical care, and risk indicators. The general profile of the sample was a young subject, Spanish, with higher-level education, employed, mostly single, and heterosexual. The sample included a similar proportion of men and women, although with a slightly higher percentage of men. They consulted with the STI centre for some reason related to STI contagion or suspicion, highlighting the presence of symptoms as the reason for consultation.


**Table 1.** Sociodemographic features, medical care and risk indicators.


**Table 1.** *Cont.*

\* HIV: Human Immunodeficiency Virus; STI: Sexually Transmitted Infections; Control: people going to the centre for an STI control; Follow-up of contacts: people who go to the centre because they have had a risky contact.

Out of 678 analysed cases, 65.5% (*n* = 444) got an STI positive diagnosis, as opposed to 34.5% (*n* = 234) of negative cases. Table 2 shows the results of sexual habits and condom use variables in such sexual practices.


**Table 2.** Sexual habits and condom use.

\* H = habit; U.C. = use of condom.

Table 3 shows the results corresponding to the association between STIs and sexual habits. STI diagnosis was significantly associated with the practice (frequent-always) of mouth–penile oral sex (*p* = 0.004), mouth–vagina oral sex (*p* = 0.023), and anal sex (*p* = 0.031). In the three cases, the effect size was low.

**Table 3.** Sexual habits and STI diagnosis.


\* n.s.: not significant; n.a.: not applicable.

### **4. Discussion**

From among the results of this research, it is worth mentioning the association observed between the STI diagnosis and the frequency of oral sex (mouth–penile and mouth–vagina) and anal sex. Before describing such finding more deeply, there are aspects of the sample features that should be pointed out.

The age of the first sexual intercourse was around 17 years old, which approximates to other studies which establish the commencement of sexual intercourse between 17 and 18 years old [6,18], unlike other studies which point out slightly lower figures, reporting median ages between 15 and

16 years old [19,20]. It has been shown that a reduction in the age of the first sexual intercourse is a factor contributing to an increase in STIs [21,22].

As regards other risk indicators, subjects stated they had one sexual partner or no sexual partner during the last month and approximately 50% stated they had two or fewer partners during the last year, which results are similar to the ones observed in another study [4]. Although our study does not observe an elevated number of sexual partners, an increase in the number of sexual partners is known to be related to an increase in STIs [21,23]. With respect to the use of drugs, most of them stated they did not use or used them sporadically, which findings also coincide with another research [6]. As regards such finding, it should be noted that factors leading to a higher risk of acquiring HIV and STIs include not only early sexual intercourse and a higher number of sexual partners, but also drug use during said intercourse [22,23]. In Europe, an earlier initiation of sexual intercourse is observed, as well as an increase in the number of sexual partners, which would contribute to an increase in the incidence of STIs [21,23].

Regarding the sexual habits analysed, vaginal intercourse stands out as to frequency, followed by mouth–penis and mouth–vagina oral sex. In contrast, there were very few reported cases of mouth–anus oral sex as well as anal sex. Such data are similar to data from another study where higher percentages were found for vaginal intercourse [24], or where oral sex was more frequent than anal sex [18]. Our findings with respect to a higher frequency of vaginal sex as opposed to anal sex may be conditioned by mostly heterosexual subjects in our sample. The importance of anal intercourse as opposed to vaginal intercourse resides in the fact that the former constitutes a higher-risk sexual practice regarding transmission of HIV both for men and women [25].

In relation to condom use, results show an inconsistent use when asking subjects about the time elapsed from the last time they had sex without using a condom, which could increase contagion and transmission of STIs. It is worth mentioning that evidence is firm when relating the low use of condom to a higher risk of getting an STI [13,24,26,27]. In general, the epidemiological studies available has shown that, when condoms are used constantly and correctly, they are highly effective to prevent HIV infection and they reduce the risk of other STIs [28,29].

Upon analysing the use of condom in different sexual practices in detail, it is observed that its use in vaginal intercourse occurs always or frequently, closely followed by its use in anal sex. However, in mouth–vagina and mouth–penis oral sex, the use of condom is non-existent or sporadic. Previous studies consulted have varied results; some of them agree on the use of condom in vaginal intercourse and its non-frequent use in oral sex [13,30], and others report a lower use than the one observed in our study regarding anal sex [13]. Specifically, in the "Encuesta nacional sobre sexualidad y anticoncepción entre los jóvenes españoles" [19] ("National survey on sexuality and contraception among Spanish young people"), the main reason for not always using contraception methods, like condom, resides in the number of occasions in which oral sex is practised (59.1%). A possible explanation for the low use of condom in oral sex could be the fact that people practising it are less aware of the risk of acquiring an STI during oral sex or because they see condoms as a barrier that adversely affects sexual pleasure in the couple.

Our study shows a significant association between mouth–penis and mouth–vagina oral sex and an STI positive diagnosis. As observed, in such sexual practices, the frequency of condom use is low, which could be one of the causes explaining such association. Coincidences with another study were found, which study suggests that many young people are still unaware of the ways in which STIs may be transmitted in oral–genital contact [13] and, although some studies have demonstrated that the risk of getting HIV in oral sex with an infected partner (whether by giving or by receiving it) is much lower than the risk of getting this virus in anal or vaginal intercourse with an infected partner, it is possible that this may not be the case for other STIs [31]; hence, the importance of condom use in oral sex as well.

Furthermore, a significant association between anal sex and an STI positive diagnosis was found; although, it is worth recalling that descriptive data showed this practice is not frequent in the sample

studied. Anal intercourse is the riskiest sexual practice as regards transmission of STIs such as HIV, chlamydia, or gonorrhea [32], the risk being higher when a passive role is adopted [33,34], with a probability of infection 13 times higher than for the sexually active partner, due to the fact that the lining of the rectum is thin and may allow HIV to enter the body during anal sex [25].

This study has some limitations, one of them being related to the high percentage of values lost in some variables, since not in all of them data on the same number of subjects were registered; when working with medical records, not all variables are completed. In addition, another limitation is the fact that it is a single-centre and single-province study, which, when extrapolating the results obtained, would limit their external validity. Nevertheless, the WHO has emphasized, in its latest reports, the availability of local data to improve the approach to STIs [2]. Finally, the methodological design used does not allow for the establishment of causal relations, so the associations observed must be considered as hypotheses to be supported by more complex designs and analyses.

### **5. Conclusions**

In conclusion, the most frequent sexual practices reported in this research were vaginal and oral (mouth–vagina and mouth–penis) sex, unlike the low frequency of anal sex. Likewise, the use of condom was frequent in vaginal and anal sex, as opposed to the figures observed in oral sex. A statistically significant relationship is established between the presence of STIs and oral and anal sex.

The results obtained in this study may contribute to the design of sex education policies aimed at reducing the risk of certain sexual practices through strategies oriented to an improvement in sexual health and a minimization of exposure to and contagion of STIs. As previously mentioned, the findings of this study are in line with the WHO's proposal [2] of worldwide strategies to prevent sexually transmitted infections, where disparity in reports among different regions and countries, as well as within every region and every country, is worth mentioning because of the difficulty derived from the lack of local data to globally address STIs, in order to measure the advance towards their control.

**Author Contributions:** Conceptualization, R.C.S.-B. and A.M.-S.; methodology R.C.S.-B. and C.H.-M.; software, C.H.-M; investigation, R.C.S.-B., C.H.-M., and M.Á.P.-M.; data curation, R.C.S.-B., C.H.-M., and M.Á.P.-M.; writing—original draft preparation, R.C.S.-B., C.H.-M., A.M.-S., M.A.Á.-S., M.G.-L., and M.Á.P.-M.; writing—review and editing, R.C.S.-B., C.H.-M., A.M.-S., M.A.Á.-S., M.G.-L., and M.Á.P.-M.; and supervision, C.H.-M. and M.Á.P.-M. 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**


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