Abstract

Objective:

to describe sociodemographic and behavioral characteristics and to identify factors associated with human immunodeficiency virus (HIV) co-infection in cases of acquired syphilis reported in a Reference Center for Sexually Transmitted Diseases (STD) and AIDS.

Methods:

cross-sectional study with secondary data from a Reference Center for STD and AIDS in the municipality of São Paulo, Brazil, in 2014; the Poisson regression was used to estimate prevalence ratios (PR) and 95% confidence intervals (95%CI).

Results:

648 cases of acquired syphilis were reported, and 98% were male; 88% were men who have sex with men (MSM) and 57% had HIV co-infection; male sex (PR=1.95; 95%CI 1.05;3.61) and MSM (PR=1.87; 95%CI 1.38;2.53) were factors independently associated with HIV co-infection.

Conclusion:

there was a high prevalence of HIV co-infection in the service analyzed, disproportionately affecting MSM who were notified with acquired syphilis.

Keywords:
Epidemiological Surveillance; Syphilis; Sexually Transmitted Diseases; HIV Infections; Cross-Sectional Studies

Introduction

Syphilis still constitutes a serious public health problem for its magnitude and transcendence, despite the existence of effective prevention and control measures.¹1. World Health Organization. 138th session provisional agenda item 9.2. Draft global health sector strategies. Sexually transmitted infections, 2016-2021 [internet]. Geneva: World Health Organization; 2015 [cited 2017 Aug 10]. 11 p. Available in: Available in: http://apps.who.int/gb/ebwha/pdf_files/EB138/B138_31-en.pdf .
http://apps.who.int/gb/ebwha/pdf_files/E... The predominant form of this disease transmission is via sex.²2. Ho EL, Lukehart SA. Syphilis: using modern approaches to understand an old disease. J Clin Invest. 2011 Dec;121(12):4584-92. Among the main consequences of untreated infection are the vertical transmission of Treponema pallidum - which causes the congenital syphilis - and the association with human immunodeficiency virus (HIV) infection.¹1. World Health Organization. 138th session provisional agenda item 9.2. Draft global health sector strategies. Sexually transmitted infections, 2016-2021 [internet]. Geneva: World Health Organization; 2015 [cited 2017 Aug 10]. 11 p. Available in: Available in: http://apps.who.int/gb/ebwha/pdf_files/EB138/B138_31-en.pdf .
http://apps.who.int/gb/ebwha/pdf_files/E...

2. Ho EL, Lukehart SA. Syphilis: using modern approaches to understand an old disease. J Clin Invest. 2011 Dec;121(12):4584-92.^-33. Secretaria de Estado de Saúde (SP). Coordenadoria de Controle de Doenças. Centro de Referência e Treinamento DST/Aids. Guia de referências técnicas e programáticas para as ações do plano de eliminação da sífilis congênita [internet]. São Paulo: Secretaria de Estado de Saúde; 2010 [citado 2017 ago 10]. 196 p. Disponível em: Disponível em: http://www3.crt.saude.sp.gov.br/tvhivsifilis/guia_versao_digital/Guia_Integrado_versao_digital.pdf .
http://www3.crt.saude.sp.gov.br/tvhivsif... HIV and syphilis co-infection has a synergistic effect, characterized by both the elevation of HIV transmissibility and the atypical evolution of treponemic infection.²2. Ho EL, Lukehart SA. Syphilis: using modern approaches to understand an old disease. J Clin Invest. 2011 Dec;121(12):4584-92.^,44. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Trans Infect. 1999 Feb;75(1):3-17.

Actions for the prevention and control of syphilis are available and have a low cost: use of condom, early detection and proper treatment of infected people and their sexual partners.²2. Ho EL, Lukehart SA. Syphilis: using modern approaches to understand an old disease. J Clin Invest. 2011 Dec;121(12):4584-92.^,33. Secretaria de Estado de Saúde (SP). Coordenadoria de Controle de Doenças. Centro de Referência e Treinamento DST/Aids. Guia de referências técnicas e programáticas para as ações do plano de eliminação da sífilis congênita [internet]. São Paulo: Secretaria de Estado de Saúde; 2010 [citado 2017 ago 10]. 196 p. Disponível em: Disponível em: http://www3.crt.saude.sp.gov.br/tvhivsifilis/guia_versao_digital/Guia_Integrado_versao_digital.pdf .
http://www3.crt.saude.sp.gov.br/tvhivsif... It is important to highlight that these actions have an extremely favorable cost-effectiveness relation.¹1. World Health Organization. 138th session provisional agenda item 9.2. Draft global health sector strategies. Sexually transmitted infections, 2016-2021 [internet]. Geneva: World Health Organization; 2015 [cited 2017 Aug 10]. 11 p. Available in: Available in: http://apps.who.int/gb/ebwha/pdf_files/EB138/B138_31-en.pdf .
http://apps.who.int/gb/ebwha/pdf_files/E...

According to estimates from the World Health Organization (WHO), in 2012, approximately 18 million adults had syphilis worldwide, with 5.6 million new cases per year.⁵5. Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One. 2015 Dec;10(12):e0143304. WHO has established syphilis as one of priorities for implementation of actions to prevent and control sexually transmitted infections (STI) from 2016 to 2021.¹1. World Health Organization. 138th session provisional agenda item 9.2. Draft global health sector strategies. Sexually transmitted infections, 2016-2021 [internet]. Geneva: World Health Organization; 2015 [cited 2017 Aug 10]. 11 p. Available in: Available in: http://apps.who.int/gb/ebwha/pdf_files/EB138/B138_31-en.pdf .
http://apps.who.int/gb/ebwha/pdf_files/E... In order to achieve the goal defined by WHO to reduce 90% of the cases until 2030, several strategies have been proposed, among which we highlight the strengthening of surveillance activities in order to enable the monitoring and planning of the actions to be organized.¹1. World Health Organization. 138th session provisional agenda item 9.2. Draft global health sector strategies. Sexually transmitted infections, 2016-2021 [internet]. Geneva: World Health Organization; 2015 [cited 2017 Aug 10]. 11 p. Available in: Available in: http://apps.who.int/gb/ebwha/pdf_files/EB138/B138_31-en.pdf .
http://apps.who.int/gb/ebwha/pdf_files/E...

In Brazil, congenital syphilis has been a notifiable disease since 1986. However, syphilis in pregnant women and acquired syphilis became notifiable diseases only in 2005 and 2010, respectively.⁶6. Secretaria de Estado de Saúde (SP). Centro de Referência e Treinamento em DST/Aids de São Paulo. Programa Estadual de DST/Aids. Bol Epidemiológico [internet]. 2016 jul [citado 2017 ago 10];33(1):1-126. Disponível em: Disponível em: http://www.saude.sp.gov.br/resources/crt/vig.epidemiologica/boletim-epidemiologico-crt/boletim_epidemiologico_2016.pdf?attach=true .
http://www.saude.sp.gov.br/resources/crt...

From 2010 to June 2016, 227,663 cases of acquired syphilis in adults were reported in the country. São Paulo state accounted for 44% of this total, with 9,976 and 25,909 cases of acquired syphilis reported in 2011 and 2015, respectively.⁷7. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Sífilis 2016. Bol Epidemiológico [Internet]. 2016 out [citado 2017 ago 10];47(35):1-32. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2016/boletim-epidemiologico-de-sifilis-2016 .
http://www.aids.gov.br/pt-br/pub/2016/bo...

In the Brazilian context, the increase in the number of acquired syphilis cases may have occurred due to the reduction of underreporting cases; it can also be attributed to the influence of changes in the scenario of sexual practices and behaviors that could favor people's vulnerability to STI. According to a systematic review of the literature on the use of condoms in Brazil, studies indicate the stabilization or reduction in the frequency of male condom use, mainly since 2005.⁸8. Dourado I, MacCarthy S, Reddy M, Calazans G, Gruskin S. Revisitando o uso de preservativo no Brasil. Rev Bras Epidemiol. 2015 set;18(supl 1):63-88.

In the country, data available in the Information System for Notifiable Diseases (Sinan) referring to syphilis are about personal identification: sex, age, ethnicity/skin color, education level and place of residence. Data related to laboratory confirmation, disease phase, sexual behaviors, treatment prescription and presence of HIV co-infection are not yet available for all national territory.⁶6. Secretaria de Estado de Saúde (SP). Centro de Referência e Treinamento em DST/Aids de São Paulo. Programa Estadual de DST/Aids. Bol Epidemiológico [internet]. 2016 jul [citado 2017 ago 10];33(1):1-126. Disponível em: Disponível em: http://www.saude.sp.gov.br/resources/crt/vig.epidemiologica/boletim-epidemiologico-crt/boletim_epidemiologico_2016.pdf?attach=true .
http://www.saude.sp.gov.br/resources/crt... ^,77. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Sífilis 2016. Bol Epidemiológico [Internet]. 2016 out [citado 2017 ago 10];47(35):1-32. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2016/boletim-epidemiologico-de-sifilis-2016 .
http://www.aids.gov.br/pt-br/pub/2016/bo... Without the systematic collection of information related to the main exposures and the presence of HIV co-infection, it is not possible to carry out an adequate evaluation of the trends of this disease. In the United States (USA)⁹9. U.S. Department of Health and Human Services. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2015 [internet]. Atlanta (GA): Centers for Disease Control and Prevention; 2016 [cited 2017 Aug 10]. 176 p. Available in: Available in: https://www.cdc.gov/std/stats15/std-surveillance-2015-print.pdf .
https://www.cdc.gov/std/stats15/std-surv... and Europe,¹⁰10. European Centre for Disease Prevention and Control. Sexually transmitted infections in Europe 2013 [internet]. Stockholm: ECDC; 2015 [cited 2017 Aug 10]. 124 p. Available in: Available in: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/sexual-transmitted-infections-europe-surveillance-report-2013.pdf .
https://ecdc.europa.eu/sites/portal/file... the epidemiological surveillance systems recommend the syphilis notification in adults with data regarding the disease phase, monitoring of main exposures, and HIV co-infection.

According to data available in Sinan,⁷7. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Sífilis 2016. Bol Epidemiológico [Internet]. 2016 out [citado 2017 ago 10];47(35):1-32. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2016/boletim-epidemiologico-de-sifilis-2016 .
http://www.aids.gov.br/pt-br/pub/2016/bo... it is not possible to know the prevalence of HIV/syphilis co-infection, since there is no co-infection data in the notification and investigation records of acquired syphilis or HIV/AIDS. To obtain this information, it would be necessary to establish relationships between databases referring to each of the diseases, using nominal data - which are not publicly available. Thus, we can justify the investigation of the prevalence of HIV/syphilis co-infection in a specialized care service, as well as the study of associated factors, in order to contribute to the proposal of prevention and control measures of these diseases at local level.

The objective of this study was to describe sociodemographic and behavioral characteristics and to identify factors associated with HIV co-infection in cases of acquired syphilis reported at a Reference Center for Sexually Transmitted Diseases (STD) and AIDS.

Methods

This is a cross-sectional study with secondary data from the Information System for Notifiable Diseases - Sinan.

The Reference Center for Sexually Transmissible Diseases (STD) and AIDS where the research was conducted is a specialized public assistance service that meets spontaneous and referenced demand from other state management services. This service is located in the southeast region of São Paulo city, state capital. It is organized into specialized outpatient clinics, which have different characteristics according to the populations assisted: an outpatient clinic for people living with HIV/AIDS (PLHA), predominantly with referenced demand; and an STD outpatient clinic, with a testing and counseling center (TCC), for diagnosis of HIV infection and STI, predominantly with spontaneous demand.

We included all cases of acquired syphilis diagnosed at the STD and AIDS Reference Center aged 18 years or older at the time of diagnosis, reported at Sinan in 2014.

We analyzed the following variables:

The definition of acquired syphilis case adopted at the STD and AIDS Reference Center was the following: asymptomatic individual, with non-treponemic reactive serology with titration above 1/16 and reagent treponemic test; or individual with clinical evidence of primary or secondary syphilis (presence of hard cancer or lesions compatible with secondary syphilis), with non-treponemal serology reagent with any titration and reagent treponemic test. The case definition of HIV infection followed the laboratory flow chart defined by the Brazilian Ministry of Health.¹¹11. Ministério da Saúde (BR). Secretaria de Vigilância em saúde. Departamento de DST, Aids e Hepatites Virais. Manual técnico para diagnóstico da infecção pelo HIV [internet]. Brasília: Ministério da Saúde; 2013 [citado 2017 ago 10]. 56 p. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/publicacoes/manual_tecnico_diagnostico_infeccao_hiv.pdf .
http://bvsms.saude.gov.br/bvs/publicacoe... All results of the serological and dark-field microscopy were obtained from laboratory reports performed at the same center.

We utilized data from Sinan and from syphilis investigation and notification forms. Sinan is a nationwide information system, managed by the Ministry of Health, and used for epidemiological surveillance in the country. Data entry in this system is under local responsibility; these data are extracted from specific investigation and notification forms on each disease or illness, and then consolidated and analyzed by municipal and state levels.¹²12. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Sistema de informação de agravos de notificação - Sinan: normas e rotinas [Internet]. Brasília: Ministério da Saúde ; 2006 [citado 2017 ago 10]. 80 p. Disponível em: Disponível em: http://bvsms.saude.gov.br/bvs/publicacoes/sistema_informacao_agravos_notificacao_sinan.pdf .
http://bvsms.saude.gov.br/bvs/publicacoe... Sinan's data on acquired syphilis do not incorporate the clinical, laboratory and epidemiological preceding, neither the status in relation to HIV infection; only sociodemographic characteristics are recorded in the system. In order to complete the missing information, a complementary form was used in the service routine of the unit's epidemiological surveillance. Identification data were typed in Sinan; and the other data, in an Excel® spreadsheet.

All information regarding serology results for syphilis and HIV were confirmed with the laboratory source, to ensure the data reliability. We evaluated the duplicity of cases in Sinan database, withdrawing the identified cases. The possibly confounding variables were controlled through multivariate analysis.

All cases of acquired syphilis reported in 2014 were included.

In the analysis, the relative and absolute frequencies of the variables were calculated, as well as the prevalence of HIV co-infection and the respective prevalence ratios (PR) and 95% confidence intervals (95%CI). The Stata® statistical package (version 11.0) was used in the analyses. The Poisson regression model with robust variance estimation was used for multivariate analysis.¹³13. Coutinho LMS, Scazufca M, Menezes PR. Métodos para estimar razão de prevalência em estudos de corte transversal. Rev Saúde Pública. 2008 dez;42(6):992-8. The multivariate model was organized with the inclusion of all analyzed variables that showed p<0.20 in the crude prevalence ratio, by the Wald test. We adopted the significance level of 5% for the maintenance of variables in the final model; the selection of the variables was performed using the stepwise backward technique. The variables that remained in the model were those that presented a level of significance lower than 0.05 by the Wald test. We organized two intermediate models (model 1 and model 2) to test the potential confounding effect of the variable outpatient clinic type. In model 1, we tested the variables sex, age group, education level and sexual behavior; an exception was made for the outpatient clinic type, which was included in model 2; model 3 resulted from the inclusion of better adjusted variables.

The study was approved by the Research Ethics Committee of the institution on April 28^th, 2015 - CAAE: 43705715.2.0000.5375 -, in accordance with the Resolution of the National Health Council No. 466, dated December 12^th, 2012. Only secondary data, registered by the local epidemiological surveillance system were used; thus, the signing of the Free and Informed Term of Consent was not necessary.

Results

A total of 648 cases of acquired syphilis were reported, with a predominance of males (97.8%), from 25 to 34 years old (40.3%), complete or incomplete higher education (47.5%) and self-declared white (59.9%) (Table 1); 56.9% were asymptomatic and 90.6% presented a non-treponemal test result higher than or equal to 1/32 dilution (Table 2). Among the characteristics of sexual behavior and other vulnerabilities, of the total reported cases, we observed: 8.2% transvestite/transsexual gender identity, 60.6% with multiple sexual partnerships in the prior year, 88.1% of MSM, 44.1% of non-injecting drug use and 1.5% of injecting drug use in the prior year (Table 2). The prevalence of HIV co-infection was of 56.5% (n=366) (Table 3).

There were differences among patients, according to the care provided at each of the two outpatient clinics located in the STD and AIDS Reference Center, especially regarding socio-demographic characteristics, sexual behavior and HIV seropositivity: higher frequency of cases over 35 years old (55.6%) in the PLHA outpatient clinic; higher frequency of heterosexuals (14.6%); and higher frequency of non-injectable drug use (50%) in the STD/ TCC outpatient clinic. As expected, the prevalence of HIV co-infection was much higher in the PLHA outpatient clinic (99.3%), and this prevalence was of 22.7% (82) in the STD/TCC outpatient clinic (Table 3).

The highest prevalence ratios on HIV co-infection found in reported cases of acquired syphilis were the following: male sex, PR=2.68 (95%CI 1.30; 5.50); age of 45 years and over, PR=2.26 (95%CI 1.74; 2.92); education level of eight years or more of schooling, PR=1.52 (95%CI 1.09; 2.12); MSM, PR=2.52 (95%CI 1.77; 3.59); clinical classification of asymptomatic syphilis, PR=1.34 (CI95% 1.03; 1.72); and STD/CTA outpatient type, PR=0.23 (95%CI 0.19; 0.26) (Table 3).

In the multivariate analysis, there was a difference between the models: in model 1, there were associations related to age group and MSM exposure category. In models 2 and 3, the associated variables were sex, education level, MSM exposure category and outpatient clinic type. There was a confounding effect of the variables age group and outpatient clinic type. The inclusion of outpatient clinic type in model 2 made visible the confounding effect of age group, considering the reduction of more than 20% in the association measure, since the age group of PLHA outpatient clinic cases was higher than the STD/TCC outpatient clinic. In model 3, the variables independently associated to HIV infection were the following: male (PR=1.95; 95%CI 1.05;3.61); education level comprising eight or more of schooling (PR=0.96; 95%CI 0.93;0.99); MSM (PR=1.87; 95%CI 1.38;2.53); and outpatient clinic type (PR=0.24; 95%CI 0.19; 0.29) (Table 4).

Discussion

In the considered STD and AIDS Reference Center, the cases of acquired syphilis diagnosed and notified were predominantly of young men, with higher education level, self-declared white, with multiple sexual partners in the prior year, MSM, with preceding of non-injecting drug use, and with reagent serology to HIV.

Of the reported cases of acquired syphilis in the service in 2014, almost half were from 25 to 34 years old, a result that is similar to the most frequent age group among cases reported in the state of São Paulo in the same year.⁶6. Secretaria de Estado de Saúde (SP). Centro de Referência e Treinamento em DST/Aids de São Paulo. Programa Estadual de DST/Aids. Bol Epidemiológico [internet]. 2016 jul [citado 2017 ago 10];33(1):1-126. Disponível em: Disponível em: http://www.saude.sp.gov.br/resources/crt/vig.epidemiologica/boletim-epidemiologico-crt/boletim_epidemiologico_2016.pdf?attach=true .
http://www.saude.sp.gov.br/resources/crt... In Brazil, according to data from cases of acquired syphilis reported in 2015, 33% refer to individuals in the age group from 20 to 29 years old.⁷7. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Sífilis 2016. Bol Epidemiológico [Internet]. 2016 out [citado 2017 ago 10];47(35):1-32. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2016/boletim-epidemiologico-de-sifilis-2016 .
http://www.aids.gov.br/pt-br/pub/2016/bo... In the USA, among the reported cases of syphilis in 2015, the highest incidence rate of primary and secondary syphilis in adults occurred in the age group from 25 to 29 years old (23.5 cases per 100,000 population).⁹9. U.S. Department of Health and Human Services. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2015 [internet]. Atlanta (GA): Centers for Disease Control and Prevention; 2016 [cited 2017 Aug 10]. 176 p. Available in: Available in: https://www.cdc.gov/std/stats15/std-surveillance-2015-print.pdf .
https://www.cdc.gov/std/stats15/std-surv...

Results related to education level and skin color reflect, in part, the characteristics of the territory where the STD and AIDS Reference Center in question is located, in the southeastern region of São Paulo city. In 2010 this region presented a very low index of social vulnerability.¹⁴14. Assembleia Legislativa (SP). Secretaria de Planejamento e Desenvolvimento Regional (SP). Fundação Sistema Estadual de Análise de Dados. Índice paulista de vulnerabilidade social - versão 2010 [internet]. São Paulo: Assembleia Legislativa; 2010 [citado 2017 ago 10]. 20 p. Disponível em: Disponível em: http://indices-ilp.al.sp.gov.br/view/pdf/ipvs/principais_resultados.pdf .
http://indices-ilp.al.sp.gov.br/view/pdf...

The high frequency of MSM, multiple sexual partners and the use of non-injectable drugs were also reported by another study conducted in 2006, in a similar service located in the central region of the same municipality, where more than 50% of cases of syphilis were found in MSM,¹⁵15. Deienno MCV, Farias N, Chencinscki J, Simões RN. Perfil dos usuários do serviço de aconselhamento no Serviço de Assistência Especializadas em DST/Aids Campos Elíseos, Município de São Paulo, Brasil. Bepa. 2010 fev;7(74):13-22. pointing the need to intensify STI prevention actions in those more vulnerable groups.

In studies to estimate the prevalence of syphilis and HIV infection in MSM conducted in Brazil in 2008 and 2009, there was a high prevalence of syphilis in Bahia (8.8%)¹⁶16. Brignol S, Dourado I, Amorim LD, Kerr LR. Vulnerability in the context of HIV and syphilis infection in a population of men who have sex with men (MSM) in Salvador, Bahia State, Brazil. Cad Saúde Pública. 2015 May;31(5):1035-48. and Minas Gerais (14%).¹⁷17. Guimarães MDC, Ceccato MGB, Gomes RRFM, Rocha GM, Camelo LV, Carmo RA, et al. Vulnerabilidade e fatores associados a HIV e sífilis em homens que fazem sexo com homens, Belo Horizonte, MG. Rev Med Minas Gerais. 2013; 23(4):412-26. These results are well above the prevalence of syphilis in puerperal women with hospital delivery, corresponding to 1%,¹⁸18. Domingues RMSM, Szwarcwald CL, Souza-Junior PRB, Leal MC. Prevalência de sífilis na gestação e testagem pré-natal: Estudo Nascer no Brasil. Rev Saúde Pública. 2014 out;48(5):766-74. indicating an increased risk in the MSM population. In the USA, among the 23,872 reported cases of primary and secondary syphilis in adults in 2015, 60% were of MSM.⁹9. U.S. Department of Health and Human Services. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2015 [internet]. Atlanta (GA): Centers for Disease Control and Prevention; 2016 [cited 2017 Aug 10]. 176 p. Available in: Available in: https://www.cdc.gov/std/stats15/std-surveillance-2015-print.pdf .
https://www.cdc.gov/std/stats15/std-surv...

We should emphasize that the high prevalence of HIV co-infection among the cases of acquired syphilis in the service studied herein is due to the fact that many of them were being followed up at the PLHA outpatient clinic. In spite of the purpose of this outpatient clinic, the high frequency of co-infection that was found may represent possible failures in adherence to prevention measures and, potentially, occurrence of new exposures to the etiologic agent of syphilis.

About one-quarter of acquired syphilis cases treated at the STD/TCC outpatient clinic presented HIV co-infection. This high frequency, much higher than that estimated for the Brazilian population, is also due to the service characteristics. We should point out the fact of being a TCC, where recently exposed people are looking for the service for testing. In a study about personal characteristics and factors associated with HIV seropositivity in TCC service users, for the period from 2000 to 2007, 7.5% of HIV infection was found, and an HIV prevalence of 11.6% among those who had syphilis.¹⁹19. Farias N, Tancredi MV, Wolffenbuttel K, Tayra A. Características dos usuários e fatores associados à soropositividade para o HIV em usuários de Centro de Testagem e Aconselhamento (CTA) no estado de São Paulo, 2000 a 2007. Bepa. 2008;5(60):9-18.

The variables independently associated with HIV co-infection in cases of acquired syphilis were males and MSM. Associations found among male sex, MSM and HIV co-infection, independently of outpatient clinic type, corroborate the results of other studies that showed an increased risk of HIV co-infection in MSM. A study carried out in 2013 with 391 MSM in Rio de Janeiro revealed a prevalence of HIV and syphilis co-infection of 10.8%.²⁰20. Cunha CB, Firedman RK, Boni RB, Gaydos C, Guimarães MRC, Siqueira BH et al. Chlamydia trachomatis, neisseria gonorrhoeae and syphilis among men who have sex with men in Brazil. BMC Public Health. 2015 Jul;15:686. Another study, carried out from 2008 to 2009 in Salvador, with 383 MSM, found 44 of them with syphilis diagnosed, and 22.7% with HIV co-infection.¹⁶16. Brignol S, Dourado I, Amorim LD, Kerr LR. Vulnerability in the context of HIV and syphilis infection in a population of men who have sex with men (MSM) in Salvador, Bahia State, Brazil. Cad Saúde Pública. 2015 May;31(5):1035-48. Surveillance data in England from 2009 to 2013 showed that the chance of MSM with HIV infection to be affected by syphilis was four times higher than in other exposure category.²¹21. Malek R, Mitchell H, Furegato M, Simms I, Mohammed H, Nardone A, et al. Contribution of transmission in HIV-positive men who have sex with men to envolving epidemics of sexually transmitted infections in England: an analysis using multiple data sources, 2009-2013. Euro Surveill. 2015 Apr;20(15):pil=21093. In the USA, in 2015, 50% of notified cases of primary and secondary syphilis involving MSM presented HIV co-infection.⁹9. U.S. Department of Health and Human Services. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2015 [internet]. Atlanta (GA): Centers for Disease Control and Prevention; 2016 [cited 2017 Aug 10]. 176 p. Available in: Available in: https://www.cdc.gov/std/stats15/std-surveillance-2015-print.pdf .
https://www.cdc.gov/std/stats15/std-surv...

The present study has some limitations. Data quality could be compromised due to incompleteness and inconsistency - quite present when secondary data are utilized. To reduce possible losses, the information was checked with those from other sources. In order to minimize underreporting of cases, all service users who presented reagent results to serological tests for syphilis were investigated and notified.

Results of this research point the need to strengthen the offer of HIV prevention and control actions on MSM category for those that seek health care during the diagnosis of syphilis. Several prevention strategies available should be offered in accordance with the exposures and vulnerabilities of the population, in an articulated way. Among these strategies, we highlight the behavioral (condom distribution), educational (counseling) and biomedical (antiretroviral therapy pre-exposure [PrEP] and post-exposure [PEP] to HIV.²¹21. Malek R, Mitchell H, Furegato M, Simms I, Mohammed H, Nardone A, et al. Contribution of transmission in HIV-positive men who have sex with men to envolving epidemics of sexually transmitted infections in England: an analysis using multiple data sources, 2009-2013. Euro Surveill. 2015 Apr;20(15):pil=21093.

22. Wit JB, Aggleton P, Myers T, Crewe M. The rapidly changing paradigm of HIV prevention: time to strengthening social and behavioral approaches. Health Educ Res. 2011 Jun;26(3):381-92.

23. Terto Júnior V. Diferentes prevenções geram diferentes escolhas? Reflexões para a prevenção de HIV/AIDS em homens que fazem sexo com homens e outras populações vulneráveis. Rev Bras Epidemiol. 2015 set;19(supl 1):156-68.

24. Abara WE, Hess KL, Neblett Fanfair N, Bernstein KT, Paz-Bailey G. Syphilis trends among men who have sex with men in the United States and Western Europe: a systematic review of trend studies published between 2004 and 2015. PLoS One. 2016 Jul;11(7):e0159309.^-2525. Grant RM, Lama JR, Anderson PL, McMahan V, Liu AY, Vargas L, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med. 2010 Dec;363(27):2587-99.

Brazilian policy to tackle HIV and AIDS adopts the combined prevention strategy, because it understands that different prevention strategies can offer the choice opportunity of the prevention tool considered more appropriate.²⁶26. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância, Prevenção e Controle das Infecções Sexualmente Transmissíveis, do HIV/Aids e das Hepatites Virais. Protocolo clínico e diretrizes terapêuticas para profilaxia pré-exposição (PrEP) de risco à infecção pelo HIV [internet]. Brasília: Ministério da Saúde ; 2017 [citado 2017 ago 10]. 52 p. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2017/protocolo-clinico-e-diretrizes-terapeuticas-para-profilaxia-pre-exposicao-prep-de-risco .
http://www.aids.gov.br/pt-br/pub/2017/pr...

In this service studied in 2014, MSM notified with acquired syphilis were disproportionately affected by HIV co-infection. The possibility of offering combined prevention actions, as recommended by the Brazilian policy to tackle HIV and AIDS for specialized care services to STI and AIDS, would enable the vulnerability reduction of this population.

In the recommendations of the 'Clinical Protocol and Therapeutic Guidelines for Pre-Exposure Prophylaxis (PrEP) of Risk to HIV Infection’²⁶26. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância, Prevenção e Controle das Infecções Sexualmente Transmissíveis, do HIV/Aids e das Hepatites Virais. Protocolo clínico e diretrizes terapêuticas para profilaxia pré-exposição (PrEP) de risco à infecção pelo HIV [internet]. Brasília: Ministério da Saúde ; 2017 [citado 2017 ago 10]. 52 p. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2017/protocolo-clinico-e-diretrizes-terapeuticas-para-profilaxia-pre-exposicao-prep-de-risco .
http://www.aids.gov.br/pt-br/pub/2017/pr... the indication of PrEP is mentioned as one of the components of combined prevention actions. The presence of recurrent STI in MSM constitutes one of the criteria for offering this prevention strategy in Brazil²⁶26. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância, Prevenção e Controle das Infecções Sexualmente Transmissíveis, do HIV/Aids e das Hepatites Virais. Protocolo clínico e diretrizes terapêuticas para profilaxia pré-exposição (PrEP) de risco à infecção pelo HIV [internet]. Brasília: Ministério da Saúde ; 2017 [citado 2017 ago 10]. 52 p. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2017/protocolo-clinico-e-diretrizes-terapeuticas-para-profilaxia-pre-exposicao-prep-de-risco .
http://www.aids.gov.br/pt-br/pub/2017/pr... and in the USA.²⁷27. U.S. Public Health Service. Centers for Diseases Control and Prevention. Preexposure prophylaxis for the prevention of HIV infection in the United States - 2014: a clinical practice guideline [internet]. Atlanta (GA): CDC; 2014 [cited 2017 Aug 10]. 67 p. Available in: Available in: https://www.cdc.gov/hiv/pdf/guidelines/PrEPguidelines2014.pdf .
https://www.cdc.gov/hiv/pdf/guidelines/P... Therefore, we recommend to be one of the criteria for choosing PrEP²⁶26. Ministério da Saúde (BR). Secretaria de Vigilância em Saúde. Departamento de Vigilância, Prevenção e Controle das Infecções Sexualmente Transmissíveis, do HIV/Aids e das Hepatites Virais. Protocolo clínico e diretrizes terapêuticas para profilaxia pré-exposição (PrEP) de risco à infecção pelo HIV [internet]. Brasília: Ministério da Saúde ; 2017 [citado 2017 ago 10]. 52 p. Disponível em: Disponível em: http://www.aids.gov.br/pt-br/pub/2017/protocolo-clinico-e-diretrizes-terapeuticas-para-profilaxia-pre-exposicao-prep-de-risco .
http://www.aids.gov.br/pt-br/pub/2017/pr... the presence of bacterial sexually infections in MSM, as well as in other populations at increased risk.

In conclusion, the analysis of HIV co-infection prevalence in patients with acquired syphilis and its associated factors can contribute to the formulation of prevention measures on HIV infection in populations that attend specialized services of STI and AIDS. Future studies should deepen the knowledge of different profiles on the co-infection between HIV and syphilis in other scenarios of assistance to STI and AIDS.

Acknowledgments

To Mariza V. Tancredi, for the important contributions in the discussion of analysis procedures in this article.To Wong Kuen Alencar, in memoriam, for his tireless work in the conception of this project and commitment with the epidemiological surveillance. To Beatriz Suter and Letícia dos Santos Cesário, for important contribution in the data collection.

References

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