Bio-behavioral survey of syphilis in homeless men in Central Brazil : a cross-sectional study

The objective of this study was to investigate the prevalence and factors associated with syphilis in homeless men in Central Brazil. It is a cross-sectional study conducted with 481 individuals attending four therapeutic communities between October and December 2015. A structured interview was conducted to collect sociodemographic data and risk factors for syphilis. Rapid/point-ofcare and VDRL tests were performed to determine exposure to syphilis and the presence of active syphilis, respectively. Poisson regression analysis was used to verify the risk factors associated with the outcomes investigated. Of the study participants, 10.2% were reactive to the rapid test, and 5.4% had active syphilis. At the multiple regression analysis, schooling (adjusted prevalence ratio – APR: 0.89; p = 0.005), history of genital ulcer (APR: 2.59; p = 0.002), STI history (APR: 1.97; p = 0.042), and sexual intercourse under drug effects (APR: 1.60; p = 0.022) were independent factors associated with lifetime syphilis. Also, history of genital ulcer (APR: 2.19; p = 0.019), STI history (APR: 1.74; p = 0.033) and number of sexual partners in the last year (APR: 1.02; p = 0.044) were associated with active syphilis. The prevalence of syphilis among homeless men was rather high, confirming the vulnerability of this group to this infection. These results emphasize the need for educational intervention, improvement of risk reduction programs, availability of diagnostic tests, especially the rapid test, and treatment. Syphilis; Homeless Persons; Risk Behavior This article is published in Open Access under the Creative Commons Attribution license, which allows use, distribution, and reproduction in any medium, without restrictions, as long as the original work is correctly cited. ARTIGO ARTICLE


Background
Syphilis is a major public health problem around the world.It is associated with several severe outcomes, including maternal-fetal complications, infertility, and death 1 .This infection is highly endemic in developing countries, and in recent decades it has considerably reemerged in several developed countries.The World Health Organization 2 estimated about 36.4 million prevalent cases of syphilis and an incidence of 10.6 million infections every year, of which 90% are concentrated in low-and middle-income countries.In the Americas, it is estimated that 6.7 million people are infected with Treponema pallidum, and that 2.8 million new cases of syphilis occur per year 3 .
In particular, congenital syphilis is generally devastating worldwide, being associated with high morbidity and mortality 4 .In 2012, it was estimated that 350,000 adverse pregnancy outcomes were associated with syphilis, with 143,000 early fetal deaths/stillbirths, 62,000 neonatal deaths, 44,000 preterm/low birth weight babies and 102,000 infected infants 5 .In the Region of the Americas, approximately 22,800 cases of congenital syphilis were estimated in 2015 in 37 countries and territories 6 .In Brazil, despite the advances in congenital syphilis policies and interventions, the epidemic has worsened, resulting in substantial fetal and neonatal mortality 7 .In 2015, 19,228 cases of congenital syphilis in children under one year of age were recorded in the Notifiable Diseases Information System (SINAN, acronym in Portuguese), resulting in an incidence rate of 5.4/1,000 live births.Also, the infant mortality rate for syphilis has increased from 2.4/100,000 live births to 7.4/100,000 live births from 2005 to 2015 8 .
Syphilis has predominantly sexual transmission and less frequent parenteral and vertical transmission 9 .Thus, this infection is predominant among individuals with high risk behaviors, such as alcohol and illicit drug use, injection drug use, inconsistent condom use, multiple sexual partners, and sex for money and/or drugs 10,11 .In addition, investigations have shown that individuals with low income and education level and with difficulties of access to health services are more vulnerable to syphilis 12 .In this context, the infection is more common among certain key populations, such as individuals deprived of their liberty, illicit drug users, men who have sex with men, sex workers, and homeless persons 9 .
Homeless populations represent one of the groups that is most affected by epidemics of sexually transmitted infections (STIs) including syphilis 13,14,15 .It is estimated that approximately 100 million people are homeless at the global level, and most are male 16 .Studies have shown a high frequency of risk behaviors among this population, such as consumption of psychoactive substances and inconsistent condom use 17,18,19,20 .In addition, they are more susceptible to social and environmental risk factors related to STIs when compared with the general population 13 .The few studies conducted with homeless men have shown syphilis prevalence from 4.4% to 6.9% 10,21 .
In developing countries, such as Brazil, the real prevalence of syphilis in homeless men is still unknown.The only studies conducted in the country found prevalence ranging from 5.2 to 6.6% in this population 12,22 .However, these studies included residents of only one city (São Paulo, Southeast region).In this context, epidemiological studies on infections such as syphilis in homeless men are important tools for the knowledge on this disease in this population, providing subsidies for the planning and implementation of measures of prevention, control, and treatment of the infection.This study aimed to investigate the prevalence and factors associated with syphilis in homeless men in Central Brazil.

Methods
A cross-sectional study was conducted using a non-probabilistic sample of homeless men between August and November 2015.Participants were recruited in four therapeutic communities for homeless people in the cities of Aparecida de Goiânia, Anápolis and Cocalzinho, located in the Goiás State, Central region of Brazil.We included all homeless men aged 18 or over who attended the institutions during the study period.Individuals with psychotic outbreak, severe mental illness or apparent psychomotor agitation were excluded from the study.No financial incentive was given for participation in this study.
The sample needed to perform the study was 285, considering a 80% statistical power (β = 20%), 95% significance level (α = 0.05), 3.0 design effect used to increase the sample and obtain a narrower 95% confidence interval (95%CI) 23 , and 6.6% 12 prevalence of active syphilis in homeless men.To achieve this value, 30% of eventual losses were added, totaling a minimum required sample of 370 homeless men.
Data were collected at the participating institutions by previously trained health professionals.After clarifying the objectives, methods, benefits and potential risks, all subjects who agreed to participate in the study answered a structured questionnaire about sociodemographic characteristics, psychoactive substance use, and risk factors for syphilis.The instrument was based on previously validated studies conducted on vulnerable populations and tested in a pilot study.After the interview, a digital puncture was performed for conducting the rapid/point-of-care test (treponemal test).Then, 5mL of blood were collected through venipuncture, to perform the venereal diseases research laboraty (VDRL) test (non-treponemal test).All participants received pre-test counseling.
In this investigation, two dependent variables were considered: (i) exposure to syphilis, defined as positive in the rapid test 24 , and active syphilis, defined as positive in the rapid test and VRDL (any titre) 25 .The following independents variables were considered: age (years); education level (years), length of stay on the street (days); marital status (married/consensual vs. single/separated/widowed), family cohabitation (yes vs. no); tattoo (yes vs. no); body piercing (yes vs. no); previous blood transfusion (yes vs. no); alcohol use (yes vs. no); marijuana use (yes vs. no); crack use (yes vs. no); use of intranasal cocaine (yes vs. no); injecting drug use (yes vs. no); previous HIV testing (yes vs. no); history of urethral discharge (yes vs. no); history of genital ulcer (yes vs. no); STIs history (yes vs. no); condom use (always vs. sometimes/never); condom use in the last sexual intercourse (yes vs. no); alcohol use before and/or during sexual intercourse (always vs. sometimes/never); use of illicit drugs before and/or during sexual intercourse (always vs. sometimes/never); sexual intercourse with STI carriers (yes vs. no); sex with sex workers (yes vs. no); sexual relations with illicit drug users (yes vs. no); homosexual sexual relation (yes vs. no) and number of sexual partners.The consumption of psychoactive substances was measured for the last 30 days, except for injection drugs which were measured for the participant's lifetime.Sexual behavior information was restricted to the last year.
The data were analyzed using the statistical program Stata (StataCorp LP, College Station, USA) version 12.0.Initially, the quantitative variables were verified through the Anderson-Darling test 26 .Descriptive analysis of the variables was performed.The quantitative variables were presented as median and interquartile range (IQR) and the qualitative variables, as absolute and relative frequencies.Lifetime and active syphilis prevalence was estimated with 95%CI.Poisson regression with robust variance estimation 27,28 was used to analyze the independent contribution of each risk factor to the investigated outcomes.In the multivariable analysis, the inclusion criterion adopted was p-value < 0.20 in the bivariate analysis for potential confounders, and the variables which had significance lower than 0.05 remained in the final model.The multivariable analysis results are presented as adjusted prevalence ratio (APR) and with a respective 95%CI.Variables with values of p < 0.05 were considered statistically significant.

Ethical aspects
This study was approved by the Ethics Committee of the Federal University of Goiás' University Hospital, under number 1236774.Consent was obtained from all participants.The results of the rapid test were delivered to the participants, immediately after the post-test counseling.Next, they were referred to the health unit closest to the interview site for clinical follow-up and treatment.

Characteristics of the participants
Of the total number of potentially eligible participants attending the institutions during the study period (n = 511), 481 agreed to participate (94.1% response rate).Table 1 1).

summarizes the
Antecedents of urethral discharge and genital ulcer were reported by 29.1% and 15.4% of the participants, respectively.STIs history was reported by 33.9% of the sample.Only 16.6% of the men reported previous HIV testing.Inconsistent condom use (sometimes/never) was reported by most participants (82.6%).Of the total, 89.4% and 60.3% reported use of alcohol and illicit drugs before and/ or during sexual intercourse, respectively.In addition, 72% reported having had sex with illicit drug users; 71.5% with sex workers; 30% with people of the same sex; 16.6% with STI carriers.The median number of sexual partners in the last year was two (IQR: 1.0-5.0)(Table 1).

Factors associated with syphilis
Table 2 shows the factors associated with exposure to and active syphilis in the bivariate Poisson analysis.History of genital ulcer (p = 0.010), and STIs history (p = 0.001) were predictors of exposure to syphilis in this analysis.Also, alcohol use (p = 0.016), crack use (p = 0.046), history of genital ulcer (p = 0.010) and STIs history (p = 0.008) were factors associated with active syphilis in this analysis.
Table 3 presents the results of the multiple regression model of factors associated with exposure to syphilis.Education level (APR: 0.89; p = 0.005), history of genital ulcer (APR: 2.59; p = 0.002), STIs history (APR: 1.97; p = 0.042), and use of illicit drugs before and/or during sexual intercourse (APR: 1.60; p = 0.022) were independent factors associated with this outcome.Table 4 presents the results of the multiple regression model of factors associated with active syphilis.The following factors were predictors of active syphilis: history of genital ulcer (APR: 2.19; p = 0.019), STIs history (APR: 1.74; p = 0.033), and number of sexual partners in the last year (APR: 1.02; p = 0.044).

Discussion
This study investigated the prevalence and factors associated with syphilis in homeless men in Central Brazil.Consistently with existing literature 10,22,29 , the results of this research show high rates of risk behavior, including use of alcohol and/or illicit drugs, multiple sexual partners, inconsistent use of condoms, sexual practices under the influence of alcohol, and/or illicit drugs, and with groups (illicit drug users, sex workers and STI carriers).In addition, a high prevalence of syphilis was observed in the study population, and an association was found with important predictors (low education level, number of sexual partners, sexual intercourse under illicit drug use, history of STI, and genital ulcer).These results suggest a high vulnerability of homeless men to syphilis in Brazil, and the potential risk of acquiring other STIs, including infection by HIV.
In the multivariable analysis, low education level, sexual intercourse under effects of illicit drugs and history of genital ulcer and STIs history were variables associated with exposure to syphilis.Moreover, history of genital ulcer, STIs history, and number of sexual partners were predictors of active syphilis.These factors have also been associated with syphilis in studies previously conducted with vulnerable populations in Brazil and in other countries 12,32,33 .
In this study, the prevalence of exposure to syphilis decreased by 11% for each year of formal education.In fact, structural factors (e.g., low income and educaton level) are related to the increased risk acquisition of STIs in several key populations, including homeless men 34,35 .Some evidence suggests that low education level, used as a proximal socioeconomic variable, is associated with higher prevalence of certain STIs, involvement in high-risk behaviors (e.g., inconsistent condom use), low level of knowledge on preventive methods and access to health services and protection 36,37 , which explains the relationship between this factor and infection by T. pallidum.
Our results show a high frequency of sexual intercourse under effects of illicit drugs in the study sample (60.3%), which is associated with exposure to syphilis.Also, many participants reported the use of substances such as crack, cocaine, and marijuana, and three-quarters of the men reported    alcohol consumption.There is a strong relationship between the use of alcohol and/or illicit drugs and STIs 25,38 .Consumption of alcohol and illicit drugs lowers the perception of risk, reduces the user's ability to convince their partner to use a condom, and induces other risk behaviors (eg., sex for money and/or drugs and number of sexual partners), increasing the risk of acquiring syphilis and other STIs 39,40 .In this context, strengthening harm reduction strategies could contribute to reduce the burden of syphilis in homeless men 12 .
Approximately one-third of the homeless men reported a history of medical diagnosis of STIs, and 15.4% reported a history of genital ulcer.These variables were predictors of exposure to and active syphilis.The presence of STIs, especially ulcerative infections, increases the chance of transmission and acquisition of HIV 18 .Ulcerative lesions facilitate the virus' access to cells under the epithelial surface and contact with blood, increasing the likelihood of systemic HIV infection 41 .It is estimated that the risk of HIV infection through sexual intercourse is increased 3-5 times in individuals infected with T. pallidum 42 .
This study has some limitations.The cross-sectional nature of the study design does not allow the establishment of a cause and effect relationship between syphilis and the variables investigated 33 .Longitudinal studies should be implemented to verify the risk or protective factors associated with syphilis in homeless men.The non-probabilistic sample used in the investigation and the inclusion of individuals attending therapeutic communities limits the generalization of the results to the population of homeless men from other localities in Brazil 29 .Individuals treated in therapeutic communities may have different risk behaviors when compared to men with no link to these services 43 .However, the sociodemographic characteristics of the study participants were similar to other studies conducted in Brazil 12,22,29 .Data related to risk factors were self-reported, liable to memory and response bias, especially due to the nature of the interview (face-to-face).Finally, potential false negative results due to the effect of prozone in the VDRL test are considered, and the positive results in the treponemal and non-treponemal tests may not necessarily indicate active syphilis, as there are possibilities of false-positive reactions.Despite the limitations, the results of this study add important information on the epidemiology of syphilis in homeless men in Brazil, indicating the need to control this infection and for educational actions focused on this population.

Sífilis; Personas Sin Hogar; Conducta de Riesgo
Contributors C. V. L. Barros contributed in the conception and design, acquisition of data, interpretation of results, drafting and approval of the final version for publication.H. Galdino Júnior participated in the Iinterpretation of results, drafting and approval of the final version for publication.G. Rezza participated on the interpretation of results, drafting, critical revision of the intellectual content and approval of the final version for publication.R. A. Guimarães contributed in the analysis of data, interpretation of results, drafting and approval of the final version for publication.P. M. Ferreira participated in the conception and design, acquisition of data, drafting and approval of the final version for publication.C. M. Souza, L. C. C. Guimarães and D. A. C. Barros contributed in the acquisition of data, drafting and approval of the final version for publication.S. M. Brunini contributed in the conception and design; acquisition of data; interpretation of results; drafting; critical revision of the intellectual content; approval of the final version for publication Cad.Saúde Pública 2018; 34(6):e00033317

Table 1
Sociodemographic characteristics, substance use, and risk behaviors of homeless men in Central Brazil.

Table 1 (continued)
Note: quantitative variables presented as median and interquartile range (IQR).

Table 2
Bivariate analysis of factors associated with lifetime and active syphilis in homeless men in Central Brazil.

Table 3
Multiple regression of factors associated with lifetime syphilis in homeless men in Central Brazil.

Table 4
Multiple regression of factors associated with active syphilis in homeless men in Central Brazil.
* Adjusted for all variables with p-value < 0.20 in the bivariate analysis; ** Wald chi-square test.