The conditions experienced by incarcerated populations around the world, including covert risk behaviors and precarious health programs and policies, make prison systems potential amplifiers of infectious diseases, including sexually transmitted infections (STIs).1 For women, imprisonment can affect the prevalence and incidence of chronic and infectious diseases, including STI.2
Syphilis is one the world's most common STI.1 Low- and middle-income countries account for most infections, and women within these regions are disproportionately affected compared with men. Among women in low- and middle-income countries, evidence of past and current syphilis infection is high among female sex workers. Syphilis has also been associated with incarceration, among other factors that include multiple sex partners, use of illicit drugs during sexual intercourse, and finding sex partners on the Internet or through social media.1,3
Epidemiological data on syphilis in Brazil originate mainly from mandatory case reporting of diagnoses made in clinical settings. Between 2010 and 2017, a total of 626,738 syphilis diagnoses were reported to the national surveillance unit.4,5 Of these, 60.1% were women, with 55.1% of these cases reported among pregnant women for whom testing is mandatory and routine. Very little information on the prevalence of syphilis in populations at risk outside clinical care exists.
To better understand the epidemiology of syphilis in Brazil, studies directly measuring prevalence need to be conducted in populations at risk independently of screening practices in clinical settings and the potential biases of case reporting. Incarcerated women present a population at potentially high risk of syphilis infection who can serve as a sentinel for emerging trends within institutions of detention as well as within the communities from which they come.6 Women are at greater risk of entering prison with an STI, such as syphilis and HIV, because they are members of groups most vulnerable to acquiring these infections outside a prison.7 Among women in the largest penitentiary system in the country, in São Paulo state, lifetime prevalence of syphilis was found to be 7.0% and that of HIV infection was 2.8%, in 2013.8 Brazil ranks fourth among countries with the largest numbers of incarcerated persons.9 In 2016, around 42,000 women were incarcerated in Brazil. Furthermore, this figure represents an increase of 656% from 2000 for women and 293% for men in prison.10 The incarcerated population may circulate between their communities and prison. The prevalence of syphilis and its correlates in this population can therefore provide critical data to guide public policies of prevention and control inside and outside prisons in the country.11 Such data can help determine the needs for syphilis screening and treatment within the public and prison health systems as well as point to factors driving syphilis transmission outside prison. We therefore conducted a nationally representative, cross-sectional survey of incarcerated women in Brazil with the objectives of determining the prevalence of antibodies against syphilis infection and identifying demographic and behavioral factors associated with infection.
This was a cross-sectional study designed to be nationally representative of the incarcerated female population of Brazil. The sample originated from 15 female prison units located in the 5 major regions of Brazil. This included units in the states of Ceará in the Northeast Region, the Federal District and Mato Grosso in the Center-West, São Paulo and Minas Gerais in the Southeast, Pará and Rondônia in the North, and Paraná and Rio Grande do Sul in the South. The study was carried out from January 2014 to December 2015. All prison units in the study had to have prison health services on location to be included in the sampling fame.
Study Population and Sampling Methods
The target population included women under the authority of the Brazilian penitentiary system at all administrative levels. The study excluded women who were sentenced to an open (i.e., under house arrest) or semiopen regime (i.e., they can leave the prison during daytime but have to return to the prison at night). Those who could not be visited by the research team due to reasons of health, safety, administrative discipline, away to receive external care, or not being fluent in Portuguese were also not included.
The sample was constructed in several steps. First, all Brazilian women's prison units were listed according to the Brazilian Institute of Geography and Statistics, based on DEPEN data from 2012.12 Second, a purposive selection of the states to be included was done based on regional diversity (i.e., including the 5 regions of Brazil), the size of the prison population, the diversity of the types of detention facilities, and the willingness of the prison to participate. This stage intentionally included, for example, the 2 states with the highest number of prisoners. Third, the female prisons were stratified by state, number of detainees (i.e., 75–150, 151–500, and >500), and location (e.g., state capital or large metropolitan area or interior location) to apportion the total sample to ensure inclusion of these strata. Once the apportioned number of women from each facility was determined, a random selection of women from a list of all prisoners provided by each prison unit was drawn using a random number generator (Intemodino Group). This final random selection was made at the time of the investigators' arrival at the prison unit. The randomly selected women were offered participation into the study. The sample size calculation was based on an expected 30% prevalence of STI as reported in the literature,13 a desired margin of error (±3%, accounting for the study design), a 95% level of significance, and also a 90% power to detect associations with lifetime syphilis prevalence of odds ratios (ORs) at 1.5 or greater over a wide range of prevalence of exposures. The sample size calculation was 2503 women. In the field, because of financial and operational limitations, the final sample recruited was 1327 women, corresponding to a lower power of 67% to detect an OR of 1.5 or greater. Nonetheless, this sample size produced acceptable precision on point estimates and detected significant associations with lifetime syphilis prevalence on the order of an OR of 1.5 or greater.
Data collection took place in 2 separate rooms, one for completing the questionnaire and one for drawing specimens and providing counseling. To comply with institutional safety procedures and operational standards, women were brought from their cells together as a group. In the first room, women completed a structured questionnaire in private by audio computer-assisted self-interview (ACASI). The questionnaire included sections on socioeconomic characteristics, incarceration history, sexual behavior, use of legal and illegal drugs, interpersonal violence, and sexual, reproductive, and other health history. Data were automatically entered into a database with built-in error checks. To address any problems that might arise, a researcher was available at all times.
The second room was used for one-on-one counseling and fingerprick collection for syphilis testing. A rapid treponemal antibody test approved by the Ministry of Health (Rapid Test DPP Sífilis Bio-Manguinhos) was used to determine syphilis seropositivity (i.e., lifetime history of infection) following the manufacturer's instructions.14 Posttest counseling was provided when delivering the result. If the rapid test result was positive, the prisoner was referred to the prison health team for necessary follow-up, including testing for current infection, treatment, and partner services.
The database was exported to Excel for management and later imported into STATA v.15.0 software for analysis. Analysis was weighted to reflect the complex sampling design, based on the inverse of the product of the probabilities of the sampling units in each of the stages. The analysis used the complex survey analysis module in STATA. Bivariate logistic regression analysis was used to test associations between the outcome variable, syphilis antibody seropositivity, and independent variables of interest. Variables with P < 0.1 in bivariate analysis were considered for inclusion in multivariate analysis. The Wald statistic was used to test the significant effects in the logistic regression model, and variables testing at P < 0.05 were retained in the final model and considered significant. Potential confounding and effects of collinearity between factors and covariates were analyzed. In case of collinearity, only one of the variables remained in the model.
The procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation, and the protocol was reviewed by the Brazilian National Health Council (approval no. 188.211) and with the Declaration of Helsinki 1975, as revised in 2000. Informed consent was obtained in writing from all participants; no incentives or special privileges were given for participation.
A total of 1518 randomly selected female prisoners were offered participation; of these, 114 were determined ineligible. The most common reasons for ineligibility were health problems, exhibiting dangerous or threatening behavior, and not speaking Portuguese as their main language. Among eligible women, 77 (5.5%) declined to participate, for a total sample of 1327 women.
Table 1 describes female prisoners, weighted to represent the target population in Brazil, with respect to demographic characteristics, incarceration-related factors, sexual and reproductive health history, other health-related variables, alcohol and drug use, and prior syphilis testing. A largest proportion of the women were older than 30 years (52.3%; 95% CI, 49.7%–55.5%), had incomplete elementary education (48.3%; 95% CI, 45.4%–51.2%), and were black/Afro-Brazilian (65.7%; 95% CI, 62.9%–70.4%). Nearly half (47.2%; 95% CI, 44.4%–50.1%) earned minimum wage or less before incarceration; 14.2% (95% CI, 12.3%–16.3%) had ever been homeless. Two-thirds (67.7%; 95% CI, 64.9%–70.3%) received visitors while in prison. Most women were arrested for drug trafficking (65.6%; 95% CI, 62.9%–68.3%), followed by theft (17.5%; 95% CI, 15.5%–19.8%), with drug possession the reason for arrest for 3.0% (95% CI, 2.1%–4.3%). Nonetheless, 72.3% (95% CI, 69.7%–74.8%) had a history of drug use. More than two-thirds (69.4%; 95% CI, 66.6%–72.0%) of women reported sexual debut by age 15 years or younger. More than one-third (33.3%; 95% CI, 31.1%–36.6%) reported having had an abortion, and nearly one-third (29.9%; 95% CI, 27.3%–32.6%) reported ever experiencing sexual violence in a relationship. Few (8.4%; 95% CI, 6.9%–10.3%) reported receiving condoms in school (a marker for exposure to school-based sexual education and reproductive health services). Approximately half (49.2%; 95% CI, 46.2%–52.1%) recalled having a prior syphilis test. Of note, receiving money for sex, reported by 3.4% of women, is not a crime in Brazil.
Table 2 shows syphilis antibody prevalence by variables hypothesized to be associated with elevated risk of infection, also weighted for the sampling design. Overall prevalence of syphilis seropositivity among female prisoners in Brazil was 11.6% (95% CI, 9.2%–14.6%) and did not differ by age above or below 30 years. Syphilis seropositivity was elevated among black/Afro-Brazilian or mixed race women (13.6%; 95% CI, 11.2%–16.4%) compared with white and Asian women, and among those who had been homeless (33.2%; 95% CI, 25.3%–42.1%), had a history of abortion (15.3%; 95% CI, 11.7%–19.0%), and experienced sexual violence (19.4%; 95% CI, 10.4%–33.2%). Syphilis seropositivity was lower among women who reported receiving a condom in school (3.2%; 95% CI, 0.9%–10.4%).
Table 3 shows significant correlates of syphilis seropositivity in bivariate and multivariate analyses, adjusted for the sample design. In multivariate analysis, independent correlates of syphilis seropositivity were black/Afro-Brazilian and mixed race/ethnicity (adjusted OR [aOR], 1.78; 95% CI, 1.10–2.87), ever being homeless (AOR, 4.58; 95% CI, 2.78–7.56), ever having an abortion (AOR, 1.56; 95% CI, 1.02–2.38), and ever experiencing sexual violence (AOR, 1.59; 95% CI, 1.01–2.49). Lower odds of syphilis seropositivity was found with ever receiving condoms in school (AOR, 0.28; 95% CI, 0.08–1.00).
In a large, nationally representative sample of female prisoners in Brazil, we measured syphilis antibody prevalence and associated factors. More than 1 (11.6%) in 9 incarcerated women had serological evidence of past syphilis infection. Prevalence in our study was higher than that in populations of incarcerated women in other countries, ranging from 0.7% to 8.5%,15,16 yet falls below the prevalence found in one study among female prisoners in the Center-West region of Brazil at 17%.17 Our data therefore corroborate the high risk of syphilis among women who enter the Brazilian prison system and likely in their communities.
Our data also highlight strong demographic associations with syphilis. Black/Afro-Brazilian (locally “preta”) and mixed race (locally “parda”) women imprisoned in Brazil had higher and similar rates of syphilis seropositivity compared with white and Asian women, who had similar and lower prevalence. In Brazilian society, black/Afro-Brazilian women have less power and are more vulnerable compared with whites, compounding and intersecting inequalities in gender relations, social status, and socioeconomic situation. These factors in turn may be associated with sexual risk behavior and present barriers to the access of prevention and care services. The finding may be analogous to the higher prevalence of syphilis among black/African Americans and the pervasive racial/ethnic disparities for other diseases they experience in the United States.18 A study among female prisoners in the Northeast of Brazil in 2013 showed risks of syphilis related to socioeconomic factors linked to race, such as low education and family income levels, independently of condom use and knowledge of STI transmission.19 In fact, low socioeconomic status, encapsulated by history of homelessness, was the single strongest association with syphilis seropositivity among female Brazilian prisoners in our study. Other studies that include homeless women confirm high vulnerability to STI including syphilis and hepatitis in London, the southern United States, San Francisco, and New York.20–23
We found that incarcerated women with a history of abortion were more likely to test antibody positive for syphilis. The association may be partly explained because unwanted pregnancy is the result of condomless sexual behavior, as is syphilis infection.24 Despite a context of highly restrictive laws against abortion in Brazil, studies demonstrate that it is a common practice. One national survey estimated that 1 in 5 women up to the age of 40 years had at least one abortion.25 Our data suggest that the figure is closer to 1 in 3 among incarcerated women.
A striking observation of this study was the significant risk of syphilis associated with sexual violence in a relationship experienced by incarcerated women. Although history of sexual violence may be a marker for other vulnerabilities to STI, the finding calls attention to this underaddressed problem, acknowledged by nearly one-third of women in our study. Nonetheless, the events of sexual assault do present significant risks of STI.26 The incidence of STI in situations of sexual violence depends on several factors, such as type and frequency of exposure, occurrence of genital lesions, age of the victim, and presence of inflammatory STI or genital ulcer at the time of the violence. Meanwhile, vaginal penetration is the most frequent act among crimes committed against women of reproductive age.27 Screening for STI in the context of assessing sexual violence is therefore of paramount importance.28
Finally, we noted the protective effect of having received condoms in school for syphilis seropositivity. The encouraging finding supports sexual education and access to prevention within the Brazilian school system. However, we recognize that the association does not prove a causal relationship in this cross-sectional survey.
In addition to causality, we recognize other limitations of our study. The questions were on highly sensitive topics, including sexual and illegal behaviors, some occurring while in prison, and therefore vulnerable to response bias. We believe that such bias would likely result in underreporting of such behaviors. We attempted to mitigate these biases by using a self-administered questionnaire in ACASI. However, some women had difficulty using the tablet during the interview. As a result, an unknown number of questionnaires had to be completed in face-to-face interviews with study staff, which may have generated underestimation for some respondents. In some locations, the interview rooms and space available were limited, sometimes resulting in interviewers in close proximity to participants using ACASI. Another limitation was the difficulty of accessing 2 of the prisons we had initially selected. The state most affected by inability to recruit prisons and prisoners was São Paulo. This state conducted a major study 1 year before our study involving female prisoners. Lastly, caution is needed when comparing our results with that of studies using both treponemal and nontreponemal tests, thereby presenting a lower current prevalence compared with the lifetime prevalence in the present report. The present study was limited in resources to measure lifetime prevalence rather than current infection.
Despite limitations, our data can help advocate for improved STI screening and other health programs for women prisoners in Brazil, who receive relatively little attention compared with other populations in Brazil despite greater exposure to risks and health problems. Women deprived of their liberty may particularly suffer from sexual violence, with subsequent STI.29 In addition, the gap of low testing rates for STI among the most vulnerable populations who are not accessing clinical care might be addressed by improved services in prisons. The benefits of enhanced care further accrue to the partners and families of incarcerated women and the communities to which these women will return. Enhanced attention to prison populations can be an important influence on and indicator of society-wide health.
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