Active syphilis and its association with HIV and sexual risk behaviours in a multicity sample of men who have sex with men and transgender women in Peru
Lia N. Pizzicato A , Panagiotis Vagenas B , Pedro Gonzales C , Javier R. Lama C E , Monica Pun D , Jorge Sanchez C E F and Frederick L. Altice A B G
+ Author Affiliations
- Author Affiliations
A Yale School of Public Health, Department of Epidemiology of Microbial Diseases, 60 College Street, New Haven, CT 06520, USA.
B Yale School of Medicine, Section of Infectious Diseases, AIDS Program, 135 College Street, Suite 323, New Haven, CT 06510, USA.
C Asociación Civil Impacta Salud y Educación, Av Almte Miguel Grau 1010, Barranco 15063, Peru.
D Dirección General de Epidemiología, Ministerio de Salud, Av. Salaverry 801, Jesús María 15072, Peru.
E University of Washington, Department of Global Health Seattle, WA 98195, USA.
F Centro de Investigaciones Tecnológicas, Biomédicas y Medioambientales, Ca José Santos Chocano 199, Lima 15081, Peru.
G Corresponding author. Email: frederick.altice@yale.edu
Sexual Health 14(4) 304-312 https://doi.org/10.1071/SH16149
Submitted: 25 July 2016 Accepted: 20 February 2017 Published: 18 May 2017
Abstract
Background: Syphilis in Peru is heavily concentrated in men who have sex with men (MSM) and transgender women (TGW). The aim of the present study was to understand the risk factors for active syphilis infection among MSM and TGW in Peru. Methods: Independent correlates suggestive of active syphilis infection were examined to better understand risk factors for syphilis in MSM and TGW, with separate analyses conducted based on location and among TGW. In 2011, 5101 MSM and TGW completed both self-report surveys and HIV and syphilis testing in five Peruvian cities. Results: Overall, 261 (5.1%) MSM and TGW met the criteria for active syphilis, with higher prevalence in Lima than elsewhere (7.0% vs 3.0%) and in TGW than in MSM (10.7% vs 4.2%). Significant independent correlates of active syphilis infection differed greatly by location. In Lima, they included being HIV-infected (aware or unaware of status), being a TGW, being a high school graduate, engaging in receptive anal intercourse, no recent sex with a female partner and having had any symptomatic sexually transmissible infection, including syphilis, in the previous 6 months. Outside Lima, the independent correlates included being HIV-infected and unaware of status, engaging in recent sex work, no recent sex with a female partner and age 35–44 years. Among TGW, independent correlates of active syphilis included being HIV-infected (aware or unaware of status), a recent syphilis diagnosis in the previous 6 months and recent drug use. Conclusion: The findings of the present study support the need not only for combined HIV and syphilis screening, but also for increased screening and treatment of syphilis in MSM and TGW populations. Stratified analyses suggest different syphilis epidemics throughout the country and in TGW, yet being HIV-infected and aware were consistently associated with active syphilis, suggesting higher syphilis risk in HIV-infected MSM and TGW.
Additional keyword: South America.
References
[1] World Health Organization. Global incidence and prevalence of selected curable sexually transmitted infections – 2008. Geneva: World Health Organization; 2012.[2] Ruan Y, Li D, Li X, et al Relationship between syphilis and HIV infections among men who have sex with men in Beijing, China. Sex Transm Dis 2007; 34 592–7.
[3] Koblin BA, Husnik MJ, Colfax G, et al Risk factors for HIV infection among men who have sex with men. AIDS 2006; 20 731–9.
| Risk factors for HIV infection among men who have sex with men.Crossref | GoogleScholarGoogle Scholar |
[4] Stolte IG, Dukers NH, de Wit JB, Fennema JS, Coutinho RA. Increase in sexually transmitted infections among homosexual men in Amsterdam in relation to HAART. Sex Transm Infect 2001; 77 184–6.
| Increase in sexually transmitted infections among homosexual men in Amsterdam in relation to HAART.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzmsFylug%3D%3D&md5=bc0ef75cfb90333f20ae232f9ebf2b02CAS |
[5] Paz-Bailey G, Meyers A, Blank S, et al A case–control study of syphilis among men who have sex with men in New York City: association with HIV infection. Sex Transm Dis 2004; 31 581–7.
| A case–control study of syphilis among men who have sex with men in New York City: association with HIV infection.Crossref | GoogleScholarGoogle Scholar |
[6] Lynn WA, Lightman S. Syphilis and HIV: a dangerous combination. Lancet Infect Dis 2004; 4 456–66.
| Syphilis and HIV: a dangerous combination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czhvFGhtg%3D%3D&md5=ca09ba668ad61f668f2cb08c10254bcaCAS |
[7] Karp G, Schlaeffer F, Jotkowitz A, Riesenberg K. Syphilis and HIV co-infection. Eur J Intern Med 2009; 20 9–13.
| Syphilis and HIV co-infection.Crossref | GoogleScholarGoogle Scholar |
[8] Kuiken CL, van Griensven GJ, de Vroome EM, Coutinho RA. Risk factors and changes in sexual behavior in male homosexuals who seroconverted for human immunodeficiency virus antibodies. Am J Epidemiol 1990; 132 523–30.
| Risk factors and changes in sexual behavior in male homosexuals who seroconverted for human immunodeficiency virus antibodies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3czlvVWqsg%3D%3D&md5=33a0cad2ee86c463cf3ddf62b7ea6390CAS |
[9] Solomon MM, Mayer KH, Glidden DV, et al Syphilis predicts HIV incidence among men and transgender women who have sex with men in a preexposure prophylaxis trial. Clin Infect Dis 2014; 59 1020–6.
| Syphilis predicts HIV incidence among men and transgender women who have sex with men in a preexposure prophylaxis trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvFWlsL7M&md5=3cb98e145f455a75d65b8fdc0301154bCAS |
[10] Sanchez J, Lama JR, Peinado J, et al High HIV and ulcerative sexually transmitted infection incidence estimates among men who have sex with men in Peru: awaiting for an effective preventive intervention. J Acquir Immune Defic Syndr 2009; 51 S47–51.
| High HIV and ulcerative sexually transmitted infection incidence estimates among men who have sex with men in Peru: awaiting for an effective preventive intervention.Crossref | GoogleScholarGoogle Scholar |
[11] Lama JR, Lucchetti A, Suarez L, et al Association of herpes simplex virus type 2 infection and syphilis with human immunodeficiency virus infection among men who have sex with men in Peru. J Infect Dis 2006; 194 1459–66.
| Association of herpes simplex virus type 2 infection and syphilis with human immunodeficiency virus infection among men who have sex with men in Peru.Crossref | GoogleScholarGoogle Scholar |
[12] Silva-Santisteban A, Raymond HF, Salazar X, et al Understanding the HIV/AIDS epidemic in transgender women of Lima, Peru: results from a sero-epidemiologic study using respondent driven sampling. AIDS Behav 2012; 16 872–81.
| Understanding the HIV/AIDS epidemic in transgender women of Lima, Peru: results from a sero-epidemiologic study using respondent driven sampling.Crossref | GoogleScholarGoogle Scholar |
[13] Carcamo CP, Campos PE, Garcia PJ, et al Prevalences of sexually transmitted infections in young adults and female sex workers in Peru: a national population-based survey. Lancet Infect Dis 2012; 12 765–73.
| Prevalences of sexually transmitted infections in young adults and female sex workers in Peru: a national population-based survey.Crossref | GoogleScholarGoogle Scholar |
[14] The Joint United Nations Programme on HIV/AIDS. Global Report: UNAIDS report on the global AIDS epidemic 2013. Geneva: Joint United Nations Programme on HIV/AIDS; 2013.
[15] Goodreau SM, Peinado J, Goicochea P, et al Role versatility among men who have sex with men in urban Peru. J Sex Res 2007; 44 233–9.
| Role versatility among men who have sex with men in urban Peru.Crossref | GoogleScholarGoogle Scholar |
[16] Tabet S, Sanchez J, Lama J, et al HIV, syphilis and heterosexual bridging among Peruvian men who have sex with men. AIDS 2002; 16 1271–7.
| HIV, syphilis and heterosexual bridging among Peruvian men who have sex with men.Crossref | GoogleScholarGoogle Scholar |
[17] Nelson A, Press N, Bautista CT, et al Prevalence of sexually transmitted infections and high-risk sexual behaviors in heterosexual couples attending sexually transmitted disease clinics in Peru. Sex Transm Dis 2007; 34 344–61.
[18] Ludford KT, Vagenas P, Lama JR, et al Screening for drug and alcohol use disorders and their association with HIV-related sexual risk behaviors among men who have sex with men in Peru. PLoS One 2013; 8 e69966
| Screening for drug and alcohol use disorders and their association with HIV-related sexual risk behaviors among men who have sex with men in Peru.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlajs7vE&md5=1febd9b191a29bc075d609b91962a33dCAS |
[19] Clark JL, Konda KA, Segura ER, et al Risk factors for the spread of HIV and other sexually transmitted infections among HIV-infected men who have sex with men in Lima, Peru. Sex Transm Infect 2008; 84 449–54.
| Risk factors for the spread of HIV and other sexually transmitted infections among HIV-infected men who have sex with men in Lima, Peru.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjmtFCjtA%3D%3D&md5=5eae3e677d3ac6a999b9d275d78f5f2aCAS |
[20] Bautista CT, Sanchez JL, Montano SM, et al Seroprevalence of and risk factors for HIV-1 infection among South American men who have sex with men. Sex Transm Infect 2004; 80 498–504.
| Seroprevalence of and risk factors for HIV-1 infection among South American men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2crpvFGrsg%3D%3D&md5=9c47a460f046c91a53d92feeb24b67b0CAS |
[21] Larsen SA, Steiner BM, Rudolph AH. Laboratory diagnosis and interpretation of tests for syphilis. Clin Microbiol Rev 1995; 8 1–21.
| 1:STN:280:DyaK2M3hvFyhtg%3D%3D&md5=e0ff2c929df79d13e51dce604c359b02CAS |
[22] Barbor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG. AUDIT: the Alcohol Use Disorders Identification Test: guidelines for use in primary care, 2nd edn. Geneva: World Health Organization; 2001.
[23] Vagenas P, Ludford KT, Gonzales P, et al Being unaware of being HIV-infected is associated with alcohol use disorders and high-risk sexual behaviors among men who have sex with men in Peru. AIDS Behav 2014; 18 120–7.
| Being unaware of being HIV-infected is associated with alcohol use disorders and high-risk sexual behaviors among men who have sex with men in Peru.Crossref | GoogleScholarGoogle Scholar |
[24] Snowden JM, Konda KA, Leon SR, et al Recent syphilis infection prevalence and risk factors among male low-income populations in coastal Peruvian cities. Sex Transm Dis 2010; 37 75–80.
| Recent syphilis infection prevalence and risk factors among male low-income populations in coastal Peruvian cities.Crossref | GoogleScholarGoogle Scholar |
[25] Verre M, Peinado J, Segura E, et al Socialization patterns and their associations with unprotected anal intercourse, HIV, and syphilis among high-risk men who have sex with men and transgender women in Peru. AIDS Behav 2014; 18 2030–9.
| Socialization patterns and their associations with unprotected anal intercourse, HIV, and syphilis among high-risk men who have sex with men and transgender women in Peru.Crossref | GoogleScholarGoogle Scholar |
[26] Jarzebowski W, Caumes E, Dupin N, et al Effect of early syphilis infection on plasma viral load and CD4 cell count in human immunodeficiency virus-infected men: results from the FHDH-ANRS CO4 cohort. Arch Intern Med 2012; 172 1237–43.
| Effect of early syphilis infection on plasma viral load and CD4 cell count in human immunodeficiency virus-infected men: results from the FHDH-ANRS CO4 cohort.Crossref | GoogleScholarGoogle Scholar |
[27] Kofoed K, Gerstoft J, Mathiesen LR, Benfield T. Syphilis and human immunodeficiency virus (HIV)-1 coinfection: influence on CD4 T-cell count, HIV-1 viral load, and treatment response. Sex Transm Dis 2006; 33 143–8.
| Syphilis and human immunodeficiency virus (HIV)-1 coinfection: influence on CD4 T-cell count, HIV-1 viral load, and treatment response.Crossref | GoogleScholarGoogle Scholar |
[28] Dougan S, Evans BG, Elford J. Sexually transmitted infections in Western Europe among HIV-positive men who have sex with men. Sex Transm Dis 2007; 34 783–90.
[29] Chang YH, Liu WC, Chang SY, et al Associated factors with syphilis among human immunodeficiency virus-infected men who have sex with men in Taiwan in the era of combination antiretroviral therapy. J Microbiol Immunol Infect 2014; 47 533–41.
| Associated factors with syphilis among human immunodeficiency virus-infected men who have sex with men in Taiwan in the era of combination antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar |
[30] van Kesteren NMC, Hospers HJ, Kok G. Sexual risk behavior among HIV-positive men who have sex with men: a literature review. Patient Educ Couns 2007; 65 5–20.
| Sexual risk behavior among HIV-positive men who have sex with men: a literature review.Crossref | GoogleScholarGoogle Scholar |
[31] Perez-Brumer AG, Konda KA, Salvatierra HJ, et al Prevalence of HIV, STIs, and risk behaviors in a cross-sectional community- and clinic-based sample of men who have sex with men (MSM) in Lima, Peru. PLoS One 2013; 8 e59072
| Prevalence of HIV, STIs, and risk behaviors in a cross-sectional community- and clinic-based sample of men who have sex with men (MSM) in Lima, Peru.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFaqsr8%3D&md5=5412e012d9ba6faccbdda941f3797d58CAS |
[32] Baggaley RF, White RG, Boily MC. HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention. Int J Epidemiol 2010; 39 1048–63.
| HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention.Crossref | GoogleScholarGoogle Scholar |
[33] Boily M-C, Baggaley RF, Wang L, et al Heterosexual risk of HIV-1 infection per sexual act: a systematic review and meta-analysis of observational studies. Lancet Infect Dis 2009; 9 118–29.
| Heterosexual risk of HIV-1 infection per sexual act: a systematic review and meta-analysis of observational studies.Crossref | GoogleScholarGoogle Scholar |
[34] Clark J, Salvatierra J, Segura E, et al Moderno love: sexual role-based identities and HIV/STI prevention among men who have sex with men in Lima, Peru. AIDS Behav 2013; 17 1313–28.
| Moderno love: sexual role-based identities and HIV/STI prevention among men who have sex with men in Lima, Peru.Crossref | GoogleScholarGoogle Scholar |
[35] Galea JT, Kinsler JJ, Galan DB, et al Factors associated with visible anogenital warts among HIV-uninfected Peruvian men who have sex with men and transwomen: a cross-sectional study. Sex Transm Dis 2015; 42 202–7.
| Factors associated with visible anogenital warts among HIV-uninfected Peruvian men who have sex with men and transwomen: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar |
[36] Tang EC, Segura ER, Clark JL, Sanchez J, Lama JR. The syphilis care cascade: tracking the course of care after screening positive among men and transgender women who have sex with men in Lima, Peru. BMJ Open 2015; 5 e008552
| The syphilis care cascade: tracking the course of care after screening positive among men and transgender women who have sex with men in Lima, Peru.Crossref | GoogleScholarGoogle Scholar |
