Resumo (abstract):
Using datathe National Health Survey 2019, this cross-sectional study explored the association between sexual orientation and timing of the last Pap smear in Brazil. Robust Poisson regression was used to estimate crude and adjusted prevalence ratios (PR), with corresponding 95% confidence intervals (CI95%). A total of 45,307 women participated, including 720 (1.85%) non-heterosexual women, of whom 394 (0.97%) identified as lesbian and 326 (0.88%) as bisexual. A negative association between sexual orientation and time since last Pap smear less than three years was observed in both women aged ≥ 18 years and those aged 25-64 years (the target population for cervical cancer screening in the country), with prevalence rates that were 17% lower (PR = 0.83; CI95% 0.76-0.90) and 14% lower (PR = 0.86; CI95% 0.78-0.96), respectively, among non-heterosexual women. Therefore, homo and bissexuals women in Brazil are less likely to have had a Pap smear within three years compared with heterosexual women, highlighting the need for health services in the country to ensure that these women have access to this important screening.
Palavras-chave (keywords):
Sexual and gender minorities, Mass screening, Uterine cervical neoplasms, Health surveys, Brazil
Ler versão inglês (english version)
Conteúdo (article):
Sexual orientation and time since last Papanicolaou test in Brazil: the 2019 National Health Survey
Rafael Tavares Jomar
Instituto Nacional de Câncer
E-mail: rafaeljomar@yahoo.com.br
ORCID iD: https://orcid.org/0000-0002-4101-7138.
Lucivaldo Almeida Alves
Instituto Nacional de Câncer
E-mail: lucivaldoalvesdm@gmail.com
ORCID iD: https://orcid.org/0000-0001-6127-3828
Karina Cardoso Meira
Universidade Federal de São Paulo
E-mail: ninameira87@gmail.com
ORCID iD: https://orcid.org/0000-0002-1722-5703
Abstract
This cross-sectional study used data from the 2019 National Health Survey to explore the association between sexual orientation and time since last Papanicolaou test in Brazil, by means of Poisson regression with robust variance, to estimate crude and adjusted prevalence ratios (PRs) and respective 95% confidence intervals (95%CI). The participants were 45,307 women, of whom 720 (1.85%) were non-heterosexual, that is, 394 (0.97%) homosexual and 326 (0.88%) bisexual. A negative association was found between sexual orientation and time of less than three years since last Papanicolaou test, among both women aged ≥ 18 years and those 25-64 years old (the target-population for cervical cancer screening in Brazil), with prevalences of, respectively, 17% (PR = 0.83; 95%CI 0.76-0.90) and 14% (PR = 0.86; 95%CI 0.78-0.96) lower among non-heterosexuals. That is, in Brazil, homosexual and bisexual women are less likely to have had a Papanicolaou test in the prior three years than heterosexual women, which calls for efforts by health services in Brazil to offer those women this important test.
Key words Sexual and gender minorities, Mass screening, Uterine cervical neoplasms, Health surveys, Brazil
Introduction
In several developed countries, significant reduction in incidence of cervical cancer and related mortality has been attributed to the introduction of organised screening programmes based on the Papanicolaou (cytopathology) test1. In Brazil, this is the disease screening method that should be offered to women, or to any person with a cervix, in the 25-64 year age range who has been sexually active, for the purpose of identifying, confirming and treating precursor lesions2.
Launched in 1998, the National Plan to Combat Cervical Cancer introduced opportunistically-structured screening measures. Mortality from cervical cancer then trended downwards in Brazil, with annual negative variation of around 2% up to 2014, when the trend became stationary3. This was followed by decentralised implementation of a number of control measures, by way of health education, vaccination and screening in Primary Health Care, particularly since the Family Health Strategy was expanded and strengthened4.
Even though potentially preventable by means of early diagnosis of precursor lesions and vaccination against human papillomavirus (HPV)5, cervical cancer continues to be a severe public health problem in Brazil. The adjusted rate of new cases estimated for each year from 2023 to 2025 was 13.25 per 100,000 women, making it the third most incident form of cancer among women nationwide and second in the North and Northeast macro-regions (16.77/100,000 and 13.85/100,000, respectively)6. Note that, in Brazil, the national health system (Sistema Único de Saúde, SUS) has distributed the quadrivalent HPV vaccine, free of charge, for children and adolescents, since 2014, and the target population has been gradually extended to boys and girls aged nine to 14 years, persons living with HIV, solid organ or bone marrow transplantees and cancer patients aged nine to 45 years, victims of sexual abuse and users of HIV pre-exposure prophylaxis aged 15 to 45 years and those with recurrent respiratory papillomatosis from age two years7.
Although evidence has been shown that, in Brazil, the percentage of women, regardless of age, who have taken a Papanicolaou test in the past three years has increased and the percentage who never had one has decreased8, it is also known that among those from 25 to 64 years of age, prevalences of testing in the past three years are higher among those whose race/colour is white, who have more schooling and family income, private health insurance and reside in the South and Southeast macro-regions, particularly in state capitals and urban areas8. Meanwhile, among the target population, the highest prevalences of never having had a Papanicolaou test are found among those whose race/colour is black or mixed, who have less schooling and family income, high parity, no private health insurance and reside in the North and Northeast macro-regions, particularly outside state capitals8.
In that light, the authors stress that the role of sexual orientation in determining Papanicolaou testing in Brazil is unknown. That is because, not only was a national policy for lesbian, gay, bisexual, transvestite and transsexual health not introduced until 20119, but nationally representative surveys never collected data on sexual orientation, until the second national health survey (Pesquisa Nacional de Saúde, PNS) in 201910.
Specific aim 12 of the National Comprehensive LGBT Health Policy is to prevent new cases of cervical cancer among lesbians and bisexual women9, warranting research studies on the subject which can collaborate towards understanding the vulnerabilities of this population group and improve related screening measures in Brazil.
Accordingly, this study explored the association between sexual orientation and time since last Papanicolaou test in Brazil.
Methods
This cross-sectional study used data from the 2019 PNS, a representative population-based survey by the Ministry of Health, in partnership with the official bureau of statistics, of individuals 15 years old or more residing in private households in Brazil. On the basis of a complex sampling strategy, the 2019 PNS used a three-stage cluster plan, in which the primary units were census tracts, the secondary units, households and the tertiary units, residents aged 15 years or more11.
Data were collected, from March 2019 to March 2020, by appropriately trained interviewers using mobile devices. Residents (N = 88,531) selected randomly in each household answered questions on work and health after signing a declaration of free and informed consent, after execution of the 2019 PNS was duly approved by the National Research Ethics Committee (Opinion No. 3.529.376, of 23 August 2019)11.
The study reported here included women who responded ‘heterosexual’, ‘homosexual’ or ‘bisexual’ to the question ‘What is your sexual orientation?’, addressed only to interviewees ≥ 18 years old, who responded directly onto the mobile data collection device, so as to ensure privacy11. Excluded were those for whom no information was given on the variables colour/race (n = 3) and monthly per capita household income (n = 18).
In Brazil, a woman is defined as being heterosexual, homosexual or bisexual, respectively, as: a person of female gender identity who has relations with persons of male gender identity; a (lesbian) woman who has affective and sexual relations with other women, regardless of gender identity; and a person of female gender identity who has affective and sexual relations with persons of both sexes, regardless of gender identity12.
The exposure variable (sexual orientation) was transformed into only two categories: heterosexual and non-heterosexual, the latter comprising self-declared homosexuals and bisexuals. The outcome variable (time since last Papanicolaou test) was obtained by the question ‘When was the last time you had a cervical cancer prevention test?’ and was also transformed for the same purpose: those who responded ‘Less than a year ago’, ‘From one year to less than two years ago’ and ‘From two years to less than three years ago’ formed the ‘Less than three years’ category, while those who responded ‘Three years or more ago’ and ‘Never had one’ formed the ‘Three years or more’ category. The covariables used to control for confounders in the association of interest were age (in years), race/colour (white and non-white), schooling (none, incomplete lower secondary, complete lower secondary, incomplete upper secondary, complete upper secondary, incomplete higher and complete higher), monthly per capita household income (in minimum wages: up to ¼, from ¼ to ½, from ½ to 1, from 1 to 2, from 3 to 5 and 5 or more) and macro-region of residence (South, Southeast, Mid-west, Northeast and North).
All statistical analyses were performed on Stata 15.0 software, using procedures with the svyset command to contemplate the complex sampling of the 2019 PNS. First, the outcome was explored, in percentage terms, by sexual orientation and age ranges (18-24, 25-64 and ≥ 65 years), and the covariables, by sexual orientation. The association between sexual orientation and time since last Papanicolaou test was explored by Poisson regression with robust variance, which estimated prevalence ratios (PRs) and 95% confidence intervals (95%CIs). From that crude model, others were tested with adjustment for the covariables, which were introduced, one by one, in the following order: age, race/colour, schooling, monthly per capita household income and macro-region of residence. Covariables which then returned a p-value > 0.05 were excluded from the above sequence. The association of interest was explored in the whole study population (women aged ≥ 18 years) and in the 25-64 year age range, which is the target-population for cervical cancer screening in Brazil2.
Results
The study participants were 45,307 women: 44,587 (98.15%) of them heterosexual and 720 (1.85%) non-heterosexual; of the latter, 394 (0.97%) were homosexual and 326 (0.88%) bisexual. Most were in the 25-64 year age range (71.01%), non-white (55.91%), had complete upper secondary schooling (30.11%), monthly per capita household income from ½ to 1 minimum wage (29.54%) and resided in Southeast Brazil (43.70%). Table 1 shows the proportional distribution of these covariables, by sexual orientation.
Table 2 shows that 58% of the heterosexual women and 61.8% of the non-heterosexual women in the 25-64 year age range had had a Papanicolaou test less than three years earlier.
A negative association between sexual orientation and time since last Papanicolaou test was shown both among women aged ≥ 18 years (Table 3) and among those in the 25-64 year age range (Table 4), with respective prevalences of 17% (PR = 0.83; 95%CI 0.76-0.90) and 14% (PR = 0.86; 95%CI 0.78-0.96) lower among non-heterosexual women.
Discussion
The study reported here showed a negative association, in Brazil, between non-heterosexual sexual orientation and having had a Papanicolaou test less than three years previously, which was consistently confirmed in the crude and adjusted analyses among women aged ≥ 18 years and, in the adjusted analysis, among those in the 25-64 year age range. In other words, homosexual and bisexual women in Brazil are less likely to have had a Papanicolaou test in the past three years than heterosexual women.
A recent systematic review with meta-analysis13, which compared rates of Papanicolaou testing among heterosexual women and women belonging to sexual minorities, found that the latter were 42% less likely (odds ratio [OR]: 0.58; 95%CI 0.48-0.71) to have been tested than the former. Lesbians, in particular, were 54% less likely (OR: 0.46; 95%CI 0.37-0.56) to be tested routinely13.
Note that the association found in the study reported here is approximately a third as strong as in the above review, which to a point confirms the high level of cervical cancer screening achieved by Brazil in 20198. Nonetheless, Brazil’s health services, obviously supported by vigorous anti-discrimination policies for LGBT people, must direct efforts to identifying and attracting non-heterosexual women in order to offer them Papanicolaou testing, in that, otherwise, they are less likely to be tested.
The high rates of discrimination perceived or experienced by non-heterosexual women in health services14 are possible reasons for that likelihood. One nationwide online survey in Brazil15, which recruited 6,693 persons aged ≥ 50 years (1,332 of them LGBT) by snowball sampling, showed that 53% of the LGBT participants did not believe that doctors were prepared to deal with the particular health needs of this population and that 9% of those who had a doctor, on revealing their sexual orientation, perceived inappropriate reactions from these professionals. Incidentally, the same survey found that the percentage of homosexual and bisexual women who had had a Papanicolaou test at least once in their life was lower than for heterosexual women (39% vs. 73%; p value < 0.001)15.
It is thus indispensable that stronger action be taken in Brazil’s health services to promote respect for sexual diversity9. This follows from a study based on data from the first National Health Survey (2013 PNS), which showed that none of the characteristics surveyed (age, schooling, macro-region of residence, having private health insurance, the last doctor’s appointment and the last appointment through the national health service, the SUS) was capable, pragmatically, of influencing a person’s risk, whatever their sex and race/colour, of suffering discrimination for their sexual orientation in Brazil’s health services16.
Added to this, public health interventions directed to increasing homosexual and bisexual women’s access to cervical cancer screening must be planned – with the support and participation of civil society organisations – and, as soon as they are specified, be systematically practiced in health care establishments. The authors believe that these interventions should include education measures to make this population aware of cervical cancer, the exposures that increase the risk of developing it and the benefits of the Papanicolaou test. Other authors believe that simply using an instrument tailored to assessing the health of LGBT people is a significant strategy for surmounting this structural and organisational barrier to this population’s access to primary health care17, where the Papanicolaou test is mainly performed2.
One online survey18, using respondent-driven sampling, recruited 299 women who had sex with women in South Brazil: 31.8% of them had never had a Papanicolaou test. The main reasons given for not doing so included the fact that they only had sex with other women and were fearful of being mistreated by health personnel18. In that regard, it is important that health care personnel avoid the assumption that all patients are heterosexual, as such heteronormative behaviour discourages patients from declaring their sexual orientation19 21 and undermines their confidence in the health care professional22,23, making it less likely that they will follow his or her recommendations21,24. Prior studies have shown that, among lesbians, declaring sexual orientation to a health caregiver is associated with greater likelihood of having had a Papanicolaou test in the past three years25,26.
The findings of this study should be interpreted in the light of its limitations. The use of secondary data precluded assessment of the role of gender identity in the association of interest, given that the 2019 PNS did not collect that information. The cross-sectional design made it impossible to determine a causal relationship between sexual orientation and time since last Papanicolaou test. Classification of both outcome and exposure was based on self-reporting, which may have introduced, respectively, memory bias and prevarication bias. Even though the exposure variable was obtained in such a manner as to minimise such occurrences, the frequency of women self-declared homosexual and bisexual may be underestimated. As a result, and given the possibility of recall bias, the magnitude of the association of interest may also be underestimated.
Even given these limitations, this is the first study in Brazil to explore the association between sexual orientation and time since last Papanicolaou test in a nationally-representative sample, showing that, in comparison with heterosexual women, homosexual and bisexual women are less likely to have been tested in the prior three years. The study thus raises the hypothesis that women in Brazil are at greater risk of receiving a diagnosis of high-grade malignant or pre-malignant cervical lesions, a situation that deserves to be investigated in future prospective research.
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