Lesbian and bisexual women's health beliefs about performing the Papanicolaou’s test

Objective: to identify the health beliefs of lesbian and bi-sexual women about performing the Papanicolaou’s test. Methods: cross-sectional study developed exclusively on-line, with fifty-five participants. Google Forms ® were used for data collection, with sociodemographic and economic questions, as well as questions related to practices, intention, and beliefs about performing the Papanicolaou’s test. Data were organized in Google Sheets ® and analyzed in SPSS ® software. Results: it was found that bisexual women believe more in the benefit “when I do the preventive exam, I am relieved” (p=0.047). However, they have higher scores of ashamed for doing the preventive exam (p=0.005). Significant association was identified between having done the exam and perceived benefits (p=0.040); perceived se - verity and education level (p=0.006); having done the exam (p=0.039); and having fixed partnership (p=0.028). Conclu - sion: bisexual women believe that performing the exam generates relief, but feelings of shame may hinder adherence to the exam. Lesbian and bisexual women without access to higher education, who never had the exam, and who have multiple sexual partnerships are more vulnerable to cervical cancer. Contributions to practice: reflect on this sce - nario so that educational strategies are effective for cervical cancer prevention.


Introduction
Cervical cancer (CC) represents a relevant injury due to its high incidence and mortality (1) . Worldwide, it is responsible for 265 thousand deaths per year, being the fourth leading cause of female mortality. Its high incidence rates occur in sub-Saharan African and Southeast Asian countries (2) .
In Brazil, it is estimated of 17,010 cases between the years 2023 and 2025. These data become even more alarming when classified in order of importance and when distributed by regions. It is verified that, disregarding non-melanoma skin tumors, cervical cancer is the second type of cancer with higher incidence in the North and Northeast Regions (1) .
Although cervical cancer is preventable through screening (Papanicolaou's test) and vaccination against the human papillomavirus (HPV), it remains a public health problem worldwide (3) , since the rates of occurrence and morbidity and mortality still challenge the preventive measures adopted so far, showing deficiencies in supply, access, and quality of actions (4) .
The review of barriers to screening and early diagnosis of cervical cancer identified some major barriers to care for women: lack of support, community and social stigma, and spousal consent. Other barriers include individual factors such as accessibility, behaviors, attitudes, values, and practices of nonadherence to screening, namely: embarrassment, socioeconomic status, financial barriers, inability to take time off work, family responsibilities, and feelings of fear (5) .
Besides these factors, social vulnerability is highlighted, since there is a lower frequency of Papanicolaou's tests in lesbian and bisexual women, sexual and gender minorities, when compared to heterosexual women. This result suggests that health professionals make this population invisible, and that women do not always seek care, or only do so when symptoms appear. The reasons for the lower demand refer to discrimination, the fact that various lesbian or bisexual women do not find support to assume their sexual orientation, the non-perception of risk practi-ces, and the unpreparedness of professionals (6) .
Despite efforts to understand the factors that influence CC screening behavior, most studies structure their assessment into factors without the application of intrapersonal theories or behavior change frameworks. This is an opportunity, as the use of established theoretical frameworks has been crucial to the development of effective, evidence-based interventions to change health behavior (7) . The health belief model is a framework that has been commonly applied to explain methods of resolving interpersonal decisions involving a wide range of health behaviors and the psychological processes involved in these changes (8) , including cervical cancer (9) . Therefore, a similar effort is needed to study the beliefs of sexual minority women regarding the Papanicolaou's test, to understand how the constructs of the health belief model are associated with the intention and behavior of CC screening.
Given the gap evidenced in the national and international literature about studies involving the health belief model in lesbian and bisexual women regarding the performance of the Papanicolaou's test, this study becomes relevant because it aims to recognize the barriers to access of this population to services and create a favorable environment, considering the social, cultural, and structural aspects for the use of services, in addition to fostering interventions for behavior change. Thus, the objective was to identify the health beliefs of lesbian and bisexual women about performing the Papanicolaou's test.

Methods
Cross-sectional research, with a quantitative approach, developed exclusively online, with fifty-five lesbian and bisexual women from June to November 2022.
The following inclusion criteria were adopted: being Brazilian; self-declaring to be lesbian or bisexual; being in the age group recommended as priority for the Papanicolaou's test -age 25 to 64 years (10) ; and having started sexual activity. Women with a history of cervical cancer or hysterectomy; who were pregnant; and who had a any cognitive, visual, or hearing limitation that made it impossible to fill out the instruments were excluded.
To describe the population estimate, we adopted the formula used to calculate the sample for the description of quantitative variables in an infinite population. Given the impossibility of establishing the prevalence, we adopted a proportion of 50% (0.5) and the complement of the sample proportion of 50% (0.5). The sampling error adopted was 5% (0.05) and the confidence level was 95% (1.96). Thus, for this study, a minimum of 385 women were expected. However, this number of participants was not reached, and the sample was composed of fifty-five women.
The social network Instagram ® was used for dissemination and sample recruitment. The researchers created a post on the official page of the research group Sexual and Reproductive Health Promotion, to which the authors of this article are linked, with information about the study and with the electronic link to access the data collection instrument. The post was boosted weekly during the data collection period.
We conducted a convenience sampling of twenty-two participants initially (11) . These participants were referred to as seeds, with a diverse racial and regional composition. Seeds were recruited through posting on Instagram ® . Each seed referred the survey to their peers. These were women in the seed participant's social circle, to whom they had previously disclosed their sexual orientation. Peer recruitment was admitted by sharing a link, on media such as WhatsApp ® , Facebook ® or email (12) . Each contacted peer who participated in the study was also named seed and referred the research to others. It should be noted that there were no financial incentives for participation in the research.
To organize the data collection instruments, the free Google Forms ® tool was used. The instrument was programmed to record only the answers to the questionnaires that were completed by the partici-pants. The questionnaire was organized into three blocks: sociodemographic and economic issues; practices and intention to perform the Papanicolaou's test; and health beliefs about the Papanicolaou's test.
The first block included characteristics of the permanent private home, access to basic services and sanitation, access to radio, television, DVD, microcomputer, tablet and internet, widespread characteristics, nuptiality, education characteristics, work and income characteristics, practice of sports and physical activity.
In the second block, questions about the number of tests performed, time of performance, reason for performance and frequency were addressed (13) . The intention to perform cervical cancer screening was evaluated with the question: How likely are you to perform cervical cancer screening? This item was answered using an 11-point Likert scale from 0 (no intention) to 10 (strongest intention). The intention item was classified as "low" or "high" intention by the median score of the intention item as the cutoff point (14) .
The third block was composed of questions from the Health Belief Model, using a form validated and cross-culturally adapted to Brazil, Champion's Health Belief Model Scale (13) . This instrument is composed of twenty-nine questions distributed in four Likert-type scales that contemplate susceptibility, severity, benefits, and barriers. For each question, there are five alternative answers (strongly disagree, disagree, neither agree nor disagree, agree, and strongly agree) and each alternative has a value ranging from one to five. The value of each scale was obtained from the sum of the values of the marked items.
The higher scores on the susceptibility, severity, benefits, and barriers scales imply, respectively, in higher perception of risk, severity, benefits of the Papanicolaou's test and barriers related to cervical cancer prevention (13) . The data were organized in Google Sheets ® and Microsoft Office Excel ® version 2016 software. Subsequently, they were analyzed in SPSS software version 26.0. All results were expressed in tabulations.
To describe the variables, absolute and percentage frequencies were used. For the descriptive analysis, median calculations were applied, as measures of central tendency, and interquartile range, as a measure of dispersion. The Shapiro-Wilk normality test and Levene's homogeneity test were used for the quantitative variables. Since there was no normality of the data, the nonparametric Mann-Whitney test was used. It was considered statistically significant when p<0.05. Evaluating the association between the variables, Pearson's Chi-square test was used and was considered statistically significant p<0.05.
The study complied with the ethical and legal aspects of research with human beings and was approved by the Research Ethics Committee of the University of International Integration of the Afro-Brazilian Lusophony with opinion number 5,468,575/2022 and Certificate of Ethical Appreciation Submission: 56304421,9,0000,5576.

Results
Most women (61.8%; n=34) declared themselves bisexual and with a fixed sexual partnership (54.5%; n=30). All participants could read and write. The median age was 25 (interquartile range -IQR: 3) years. As for the practices and intentions for performing the Papanicolaou's test, the majority (56.3%; n=31) had already performed the exam. The main reason for performing it was screening (47.2%; n=26). Overall, the median, on a scale of 0 to 10, of interest in performing CC screening was 9 (IQR: 2).
Most participants resided in the state of Ceará (85.4%; n=47), followed by Bahia (5.4%; n=3), Amazonas (5.4%; n=3), Piauí (1.8%; n=1) and Espírito Santo (1.8%; n=1). The municipalities of residence of the women with the highest frequency were Baturité (25.4%; n=14), Redenção (20.0%; n=11) and Fortaleza (12.7%; n=7), all in the State of Ceará. The characterization of the profile of the women is presented in Table 1.   Table 2 exposes the comparison between the scores of each item of the health belief scales regarding the sexual orientation of the women. It was found that bisexual women believe more in the benefit of the exam (p=0.047). However, they have higher scores regarding shame in taking the exam (p=0.005). When relating the sociodemographic data to the classification of the belief scores, a significant association was identified between performing the exam and perceiving its benefits (p=0.040), with a hi-gher frequency of medium or high perception among women who had already undergone the exam (61.3%; n=19); severity and level of education (p=0.006), with women with higher education having medium or high perception (80.0%; n=24); severity and exam performance (p=0.039), with higher frequency of medium or high perception among women who had already taken the exam (77.4%; n=24); and fixed partnership and severity (p=0.028), with higher proportion of medium and high perception among those with fixed partnership (76.7%; n=23). Table 3 presents the comparison between the scores of health beliefs regarding women's sexual orientation. It was found that there was no statistical difference between the health belief scores of lesbian and bisexual women.

Discussion
It was observed that there are factors of direct responsibility of health services that are related to the desire to perform the exam, its benefits, and the perception of severity of CC. Thus, this research emphasizes the need for health teams to develop strategies for searching and welcoming lesbian and bisexual women, so that feelings of shame, for example, are mitigated, and that patients perceive the benefits of performing the exam with the recommended frequency.
It was found that among the study participants, there was a prevalence of bisexuals, with fixed part-nerships, and single women. The predominance of bisexual identity among the participants reveals a higher probability of exposure to sexual intercourse with penile penetration. The transmission of human papillomavirus (HPV) can occur in any type of sexual intercourse and can affect the anus, vulva, vagina, penis, and oropharynx; however, most women with CC were infected soon after sexarch, with progressive development of lesions (15) .
It is alerted, however, that lesbian women may also be vulnerable, since most have already had previous sexual experience with men and, considering that sexuality can change throughout life, even women who define themselves as lesbians can establish sexual intercourse with penile penetration (16) . Moreover, other forms of contamination, besides sexual contact with penile penetration, need to be considered.
The sexual relationship with a fixed partner may constitute a vulnerability factor, due to the false impression that not being exposed to multiple partners represents a lower risk. However, the development of cervical cancer is conditioned to HPV contamination and associated with individual factors. HPV, in turn, is a highly transmissible virus that can remain in latency for a prolonged period (17) . These characteristics reinforce the importance of the screening test and the vulnerability of all women who have established unprotected sexual intercourse, even with a fixed partnership.
Slightly more than half of the participants in this study stated that they had performed the exam and declared an interest in doing so. It is verified that the number of lesbian and bisexual women who have never undergone cervical cancer screening is still large, especially considering the goal of 80% coverage for the female population in general.
Women who have sex with women present a similar percentage of adherence to the Papanicolaou's test (52.7%), but it was highlighted that, among these women, most underwent the exam only once (18) . Given the low adherence to the exam, it is necessary that active search and welcoming strategies be implemented to ensure the inclusion of lesbians and bisexuals and increase the coverage of the Papanicolaou's test for these populations. Furthermore, lesbian, and bisexual women, when they manage to access health services, experience greater challenges regarding the prevention of cervical cancer (19)(20) .
It was identified the belief, for bisexual women, who performing the Papanicolaou's test generates relief, probably because it is a health care related to the verification that there is no development of cervical cancer. On the other hand, it was also found that the same public revealed to be embarrassed to undergo the exam, which may represent a reason for non--adherence. The Papanicolaou's test itself is considered a procedure that involves diverse feelings related to the embarrassment of exposing the body and sexual practices. The feeling of shame reported by the participants may be related to the reception of this public and/or the posture of the health professional in conducting the gynecological consultation, especially regarding sexual behavior.
In the health system, lesbian and bisexual women suffer prejudice related to religious judgment of sexual practice and negligence associated with the assumption that lesbians do not need to undergo the Papanicolaou's test because they have never had sexual intercourse with penetration (21)(22)(23) . These issues may impact access to care and, consequently, the development of cervical cancer, which requires urgency in training health professionals to offer inclusive care to vulnerable populations, such as lesbians and bisexuals.
The level of education of the participants is significantly related to the perception of severity, since women who entered higher education have medium or high perception. Access to formal education seems to positively influence not only obtaining health information, but the understanding of the message surrounding this information. Research developed with thirty-five university lesbians observed good adherence to gynecological consultation (77.1%), a fact that may be associated with the higher educational level (24) .
In fact, high incidence, and prevalence rates of CC are identified in underdeveloped and/or developing countries, which tend to present low socioeconomic and educational levels. In Brazil, for example, the estimated incidence rate for 2023 is 15.38%, a value that is much higher than the estimates of developed countries such as Australia and New Zealand, both with an estimated incidence rate of 5.6% (1)(2) .
The previous experience of the exam is related both to the perception of the benefits of the exam and the severity of the CC. This finding may result from information that patients acquired during gynecological consultations, since on this occasion there may be clarification about the disease and the importance of the Papanicolaou's test for secondary prevention of this disease. Health education during gynecological consultations can broaden knowledge and positively influence the adoption of healthy attitudes and practices, including the perception of the need to perform the Papanicolaou's test (25)(26) .
The fact of having a steady partner was also, in this study, significantly associated with the awareness of the severity of cervical cancer. About the relationship between sexual practices and health care, a research analyzing sexual practices of 231 women who have sex with women found that those who do not have a steady partnership were more vulnerable to sexual intercourse without using condoms, with higher chances of not using this protection method than women who do not have a steady partnership (27) .

Study limitations
The research had the limitation of collecting data online, which may imply in misinterpretations of the questions addressed in the questionnaire, since the interviewer was not present to clarify any doubts. However, we emphasize that because it is a previously validated instrument, the results obtained are dependable and offer important scientific contributions. Another weakness refers to the sample size, since the small number of participants may compromise the ge-neralizability of the study to the population. Furthermore, the data from this study provide the literature with information and gaps for future studies.

Contributions to practice
These findings arouse reflection about the multiple vulnerabilities of women who have relationships with women without a fixed partnership, since besides being more exposed due to sexual intercourse without condom use, they are still less aware of the seriousness of cervical cancer. This reality can favor the development of cervical cancer by the increased exposure to human papillomavirus and the eventual non-adherence to the Papanicolaou's test. It is necessary that educational strategies directed to this audience contemplate the importance of primary and secondary prevention of the disease.

Conclusion
Bisexual women have the belief that performing the Papanicolaou preventive exam generates a sense of relief; however, this public also revealed feeling ashamed to perform the exam, which may hinder adherence to secondary prevention with the necessary regularity. Higher education, previous exam performance, and/or the existence of a fixed sexual partnership were associated with greater perception about the severity of cervical cancer, which highlights the fact that lesbian and bisexual women without access to higher education, who have never undergone the Papanicolaou's test and/or have multiple sexual partnerships are more vulnerable to cervical cancer.

Authors' contribution
Conception and design or analysis and interpretation of data; Writing of the manuscript or relevant critical review of the intellectual content; Final approval of the version to be published; Agreement to be responsible for all aspects of the manuscript related to the accuracy or completeness of any part of the manuscript: Maciel NS, Nascimento ABJ, Castro GB, Bandeira BS, Alves JG, Sousa LB.