Barriers to syphilis testing among men who have sex with men: a systematic review of the literature
Rodman Turpin
A C , Andre D. Rosario B and Typhanye Dyer A
+ Author Affiliations
- Author Affiliations
A University of Maryland, College Park, School of Public Health, Department of Epidemiology and Biostatistics, 4200 Valley Drive #2242, College Park, MD 20742, USA.
B Howard University Hospital, Psychiatry and Behavioral Sciences, 2041 Georgia Avenue NW, Washington, D.C. 20060, USA.
C Corresponding author. Email: RTurpin@umd.edu
Sexual Health 17(3) 201-213 https://doi.org/10.1071/SH19044
Submitted: 9 March 2019 Accepted: 11 April 2020 Published: 26 June 2020
Abstract
Men who have sex with men (MSM) represent the highest risk group for syphilis in the United States and several other countries. Improving uptake of syphilis testing among MSM requires understanding key barriers to testing in this population. Using preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines, a systematic review to assess proportions of syphilis testing among MSM and identify social, structural, and individual barriers to syphilis testing was conducted. All searches were conducted through the University of Maryland world catalogue search engine. Studies that measured syphilis testing in a sample of MSM were included. All studies were assessed for bias using JBI-MAStARI instruments. Studies were synthesised based on sample size, years of data collection, study selection method (e.g. hospital or clinic-based, community/venue-based), location (e.g. USA-based, other countries) and results of the bias assessment. For studies measuring barriers associated with testing, the measure of association, point estimate and statistical significance was assessed. Of 848 studies found in the initial search, 24 were included in the final review. The largest difference in syphilis testing proportions was based on hospital or clinic-based sampling (50–87%) compared with venue/community-based and online sampling (31–38%). Socioeconomic factors (four items, four studies, OR 0.23 to 0.68), healthcare interactions six items, five studies, OR 0.09 to 0.69) and community/interpersonal factors (seven items, five studies, OR 0.07 to 0.58) were identified as barriers to testing. Barriers to syphilis testing among MSM include socioeconomic factors, healthcare-related factors and community/interpersonal factors. Improving overall routine utilisation of healthcare services is an especially important focal point in testing promotion.
Additional keywords: gay men, health services, public health.
References
[1] Centers for Disease Control and Prevention (CDC). 2016 HIV surveillance report. Atlanta, GA: CDC; 2017.[2] Branger J, van der Meer JT, van Ketel RJ, Jurriaans S, Prins JM. High incidence of asymptomatic syphilis in HIV-infected MSM justifies routine screening. Sex Transm Dis 2009; 36 84–5.
| High incidence of asymptomatic syphilis in HIV-infected MSM justifies routine screening.Crossref | GoogleScholarGoogle Scholar | 18971797PubMed |
[3] 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 Saude Publica 2015; 31 1035–48.
| 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.Crossref | GoogleScholarGoogle Scholar | 26083178PubMed |
[4] Hakre S, Arteaga GB, Nunez AE, Arambu N, Aumakhan B, Liu M, et al. Prevalence of HIV, syphilis, and other sexually transmitted infections among MSM from three cities in Panama. J Urban Health 2014; 91 793–808.
| Prevalence of HIV, syphilis, and other sexually transmitted infections among MSM from three cities in Panama.Crossref | GoogleScholarGoogle Scholar | 24927712PubMed |
[5] Hernandez I, Johnson A, Reina-Ortiz M, Rosas C, Sharma V, Teran S, et al. Syphilis and HIV/syphilis co-infection among men who have sex with men (MSM) in Ecuador. Am J Men’s Health 2017; 11 823–33.
| Syphilis and HIV/syphilis co-infection among men who have sex with men (MSM) in Ecuador.Crossref | GoogleScholarGoogle Scholar |
[6] Huang YF, Nelson KE, Lin YT, Yang CH, Chang FY, Lew-Ting CY. Syphilis among men who have sex with men (MSM) in Taiwan: its association with HIV prevalence, awareness of HIV status, and use of antiretroviral therapy. AIDS Behav 2013; 17 1406–14.
| Syphilis among men who have sex with men (MSM) in Taiwan: its association with HIV prevalence, awareness of HIV status, and use of antiretroviral therapy.Crossref | GoogleScholarGoogle Scholar | 23297086PubMed |
[7] Liu G, Lu H, Wang J, Xia D, Sun Y, Mi G, et al. Incidence of HIV and syphilis among men who have sex with men (MSM) in Beijing: an open cohort study. PLoS One 2015; 10 e0138232
| Incidence of HIV and syphilis among men who have sex with men (MSM) in Beijing: an open cohort study.Crossref | GoogleScholarGoogle Scholar | 26642208PubMed |
[8] Ning Z, Fu J, Zhuang M, Park JA, Ibragimov U, He N, et al. HIV and syphilis epidemic among MSM and non-MSM aged 50 and above in Shanghai, China: a yearly cross-sectional study, 2008–2014. Glob Public Health 2018; 13 1625–33.
| HIV and syphilis epidemic among MSM and non-MSM aged 50 and above in Shanghai, China: a yearly cross-sectional study, 2008–2014.Crossref | GoogleScholarGoogle Scholar | 29419357PubMed |
[9] Spornraft-Ragaller P. Ein Klassiker, den auch der Hausarzt gut kennen sollte. MMW Fortschr Med 2014; 156 38–45. [Syphilis: the new epidemic among MSM.]
| Ein Klassiker, den auch der Hausarzt gut kennen sollte.Crossref | GoogleScholarGoogle Scholar | 25026856PubMed |
[10] Taylor MM, Aynalem G, Olea LM, He P, Smith LV, Kerndt PR. A consequence of the syphilis epidemic among men who have sex with men (MSM): neurosyphilis in Los Angeles, 2001–2004. Sex Transm Dis 2008; 35 430–4.
| A consequence of the syphilis epidemic among men who have sex with men (MSM): neurosyphilis in Los Angeles, 2001–2004.Crossref | GoogleScholarGoogle Scholar | 18446083PubMed |
[11] Li Y, Xu J, Reilly KH, Zhang J, Wei H, Jiang Y, et al. Prevalence of HIV and syphilis infection among high school and college student MSM in China: a systematic review and meta-analysis. PLoS One 2013; 8 e69137
| Prevalence of HIV and syphilis infection among high school and college student MSM in China: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 24391964PubMed |
[12] Zuger A. HIV continues to target young black MSM…and syphilis isn’t far behind. J Watch AIDS Clin Care. 2012; 24 4
| 26223040PubMed |
[13] Spornraft-Ragaller P, Boashie U, Stephan V, Schmitt J. Analysis of risk factors for late presentation in a cohort of HIV-infected patients in Dresden: positive serology for syphilis in MSM is a determinant for earlier HIV diagnosis. Infection 2013; 41 1145–55.
| Analysis of risk factors for late presentation in a cohort of HIV-infected patients in Dresden: positive serology for syphilis in MSM is a determinant for earlier HIV diagnosis.Crossref | GoogleScholarGoogle Scholar | 23728772PubMed |
[14] Zhang TP, Liu C, Han L, Tang W, Mao J, Wong T, et al. Community engagement in sexual health and uptake of HIV testing and syphilis testing among MSM in China: a cross-sectional online survey. J Int AIDS Soc 2017; 20 21372
| Community engagement in sexual health and uptake of HIV testing and syphilis testing among MSM in China: a cross-sectional online survey.Crossref | GoogleScholarGoogle Scholar | 28406270PubMed |
[15] Xu JJ, Reilly KH, Lu CM, Ma N, Zhang M, Chu ZX, et al. A cross-sectional study of HIV and syphilis infections among male students who have sex with men (MSM) in northeast China: implications for implementing HIV screening and intervention programs. BMC Public Health 2011; 11 287
| A cross-sectional study of HIV and syphilis infections among male students who have sex with men (MSM) in northeast China: implications for implementing HIV screening and intervention programs.Crossref | GoogleScholarGoogle Scholar | 21554742PubMed |
[16] Fairley CK, Law M, Chen MY. Eradicating syphilis, hepatitis C and HIV in MSM through frequent testing strategies. Curr Opin Infect Dis 2014; 27 56–61.
| Eradicating syphilis, hepatitis C and HIV in MSM through frequent testing strategies.Crossref | GoogleScholarGoogle Scholar | 24275695PubMed |
[17] Tilchin C, Schumacher CM, Psoter KJ, Humes E, Muvva R, Chaulk P, et al. HIV diagnosis following a syphilis, gonorrhea, or repeat diagnosis among males including non-MSM: what is the incidence? Sex Transm Dis 2018; 46 271–77.
[18] Yu D, Hatala AR, Reimer J, Lorway R. ‘I’m more aware of my HIV risk than anything else’: syndemics of syphilis and HIV among gay men in Winnipeg. Cult Health Sex 2018; 20 1036–48.
| 29268658PubMed |
[19] Centers for Disease Control and Prevention (CDC). 2016 Sexually transmitted diseases surveillance report. Atlanta, GA: CDC; 2017.
[20] Bowers KA. Explaining health behavior: the health belief model. Nurs Adm Q 1980; 4 41–6.
| 6898872PubMed |
[21] Andersen R, Newman JF. Societal and individual determinants of medical care utilization in the United States. Milbank Mem Fund Q Health Soc 1973; 51 95–124.
| Societal and individual determinants of medical care utilization in the United States.Crossref | GoogleScholarGoogle Scholar | 4198894PubMed |
[22] Johnston LG, Vaillant TC, Dolores Y, Vales HM. HIV, hepatitis B/C and syphilis prevalence and risk behaviors among gay, transsexuals and men who have sex with men, Dominican Republic. Int J STD AIDS 2013; 24 313–21.
| HIV, hepatitis B/C and syphilis prevalence and risk behaviors among gay, transsexuals and men who have sex with men, Dominican Republic.Crossref | GoogleScholarGoogle Scholar | 23970664PubMed |
[23] Ross C, Shaw S, Marshall S, Stephen S, Bailey K, Cole R, et al. Impact of a social media campaign targeting men who have sex with men during an outbreak of syphilis in Winnipeg, Canada. Can Commun Dis Rep 2016; 42 45–9.
| Impact of a social media campaign targeting men who have sex with men during an outbreak of syphilis in Winnipeg, Canada.Crossref | GoogleScholarGoogle Scholar | 29770003PubMed |
[24] Tucker JD. The social and policy context of curing syphilis: commentary on Francis (2013). Arch Sex Behav 2013; 42 1381
| The social and policy context of curing syphilis: commentary on Francis (2013).Crossref | GoogleScholarGoogle Scholar | 23857520PubMed |
[25] Fujimoto K, Flash CA, Kuhns LM, Kim JY, Schneider JA. Social networks as drivers of syphilis and HIV infection among young men who have sex with men. Sex Transm Infect 2018; 94 365–71.
| Social networks as drivers of syphilis and HIV infection among young men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 29440465PubMed |
[26] Taylor MM, Frasure-Williams J, Burnett P, Park IU. Interventions to improve sexually transmitted disease screening in clinic-based settings. Sex Transm Dis 2016; 43 S28–41.
| Interventions to improve sexually transmitted disease screening in clinic-based settings.Crossref | GoogleScholarGoogle Scholar | 26779685PubMed |
[27] Moher D, Liberati A, Tetzlaff J, Altman DG, the PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. PLoS Med 2009; 6 e1000097
| Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.Crossref | GoogleScholarGoogle Scholar | 19753108PubMed |
[28] The Joanna Briggs Institute. The Joanna Briggs Institute reviewers’ manual: the systematic review of economic evaluation evidence. 2014 edn. Adelaide: The Joanna Briggs Institute; 2014.
[29] An Q, Wejnert C, Bernstein K, Paz-Bailey G. Syphilis screening and diagnosis among men who have sex with men, 2008–2014, 20 U.S. cities. J Acquir Immune Defic Syndr 2017; 75 S363–9.
| Syphilis screening and diagnosis among men who have sex with men, 2008–2014, 20 U.S. cities.Crossref | GoogleScholarGoogle Scholar | 28604440PubMed |
[30] Barbee LA, Tat S, Dhanireddy S, Marrazzo JM. Implementation and operational research: effectiveness and patient acceptability of a sexually transmitted infection self-testing program in an HIV care setting. J Acquir Immune Defic Syndr 2016; 72 e26–31.
| Implementation and operational research: effectiveness and patient acceptability of a sexually transmitted infection self-testing program in an HIV care setting.Crossref | GoogleScholarGoogle Scholar | 26959189PubMed |
[31] Barbee LA, Dhanireddy S, Tat SA, Marrazzo JM. Barriers to bacterial sexually transmitted infection testing of HIV-infected men who have sex with men engaged in HIV primary care. Sex Transm Dis 2015; 42 590–4.
| Barriers to bacterial sexually transmitted infection testing of HIV-infected men who have sex with men engaged in HIV primary care.Crossref | GoogleScholarGoogle Scholar | 26372931PubMed |
[32] Best J, Tang W, Zhang Y, Han L, Liu F, Huang S, et al. Sexual behaviors and HIV/syphilis testing among transgender individuals in China: implications for expanding HIV testing services. Sex Transm Dis 2015; 42 281–5.
| Sexual behaviors and HIV/syphilis testing among transgender individuals in China: implications for expanding HIV testing services.Crossref | GoogleScholarGoogle Scholar | 25868142PubMed |
[33] Chow EPF, Callander D, Fairley CK, Zhang L, Donovan B, Guy R, et al. Increased syphilis testing of men who have sex with men: greater detection of asymptomatic early syphilis and relative reduction in secondary syphilis. Clin Infect Dis 2017; 65 389–95.
| Increased syphilis testing of men who have sex with men: greater detection of asymptomatic early syphilis and relative reduction in secondary syphilis.Crossref | GoogleScholarGoogle Scholar | 28419198PubMed |
[34] Dean BB, Scott M, Hart R, Battalora L, Novak RM, Durham MD, et al. Sexually transmitted disease testing of human immunodeficiency virus-infected men who have sex with men: room for improvement. Sex Transm Dis 2017; 44 678–84.
| Sexually transmitted disease testing of human immunodeficiency virus-infected men who have sex with men: room for improvement.Crossref | GoogleScholarGoogle Scholar | 28876305PubMed |
[35] Dearing N, Lamont C. P222 Bisexual men – twice the fun or double the risk? Sex Transm Infect 2017; 93 A89.
[36] Gulov K, Coulter RW, Matthews DD, Uzzi M, Stall R. HIV and STIs among MSM in Tajikistan: laboratory-confirmed diagnoses and self-reported testing behaviors. AIDS Behav 2016; 20 341–49.
| HIV and STIs among MSM in Tajikistan: laboratory-confirmed diagnoses and self-reported testing behaviors.Crossref | GoogleScholarGoogle Scholar | 27307182PubMed |
[37] Mattson CL, Bradley H, Beer L, Johnson C, Pearson WS, Shouse RL. Increased sexually transmitted disease testing among sexually active persons receiving medical care for human immunodeficiency virus infection in the United States, 2009–2013. Clin Infect Dis 2017; 64 629–34.
| 27940947PubMed |
[38] McKenney J, Sullivan PS, Bowles KE, Oraka E, Sanchez TH, DiNenno E. HIV risk behaviors and utilization of prevention services, urban and rural men who have sex with men in the United States: results from a national online survey. AIDS Behav 2018; 22 2127–36.
| HIV risk behaviors and utilization of prevention services, urban and rural men who have sex with men in the United States: results from a national online survey.Crossref | GoogleScholarGoogle Scholar | 28986669PubMed |
[39] Ong JJ, Fu H, Pan S, Smith MK, Wu D, Wei C, et al. Missed opportunities for human immunodeficiency virus and syphilis testing among men who have sex with men in China: a cross-sectional study. Sex Transm Dis 2018; 45 382–6.
| Missed opportunities for human immunodeficiency virus and syphilis testing among men who have sex with men in China: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 29750773PubMed |
[40] Park I, Schapiro J, Hurley L, Hare CB, Slome S, Flamm J, et al. LB 2.59 Improving STD screening in HIV care through implementation of self-collected extragenital swabs. Sex Transm Infect 2017; 93 A92
[41] Rüütel K, Parker RD, Lõhmus L, Valk A, Aavik T. HIV and STI testing and related factors among men who have sex with men in Estonia. AIDS Behav 2016; 20 2275–85.
| HIV and STI testing and related factors among men who have sex with men in Estonia.Crossref | GoogleScholarGoogle Scholar | 26852032PubMed |
[42] Said MA, German D, Flynn C, Linton SL, Blythe D, Cooley LA, et al. Uptake of testing for HIV and syphilis among men who have sex with men in Baltimore, Maryland: 2004–2011. AIDS Behav 2015; 19 2036–43.
| Uptake of testing for HIV and syphilis among men who have sex with men in Baltimore, Maryland: 2004–2011.Crossref | GoogleScholarGoogle Scholar | 26078117PubMed |
[43] Tao G, Peterman T, Nye MB, Gift TL, Body BA. P3.88 Frequency of syphilis testing among men who have had rectal tests for chlamydia and gonorrhoea, United States. Sex Transm Infect 2017; 93 A125–6.
[44] Trubiano JA, Hoy JF. Taming the great: enhanced syphilis screening in HIV-positive men who have sex with men in a hospital clinic setting. Sex Health 2015; 12 176–8.
| Taming the great: enhanced syphilis screening in HIV-positive men who have sex with men in a hospital clinic setting.Crossref | GoogleScholarGoogle Scholar | 25528423PubMed |
[45] Zhang TP, Liu C, Han L, Tang W, Mao J, Wong T, et al. Community engagement in sexual health and uptake of HIV testing and syphilis testing among MSM in China: a cross-sectional online survey. J Int AIDS Soc 2017; 20 21372
| Community engagement in sexual health and uptake of HIV testing and syphilis testing among MSM in China: a cross-sectional online survey.Crossref | GoogleScholarGoogle Scholar | 28406270PubMed |
[46] Goodman SH, Grosso AL, Ketende SC, Ouedraogo GH, Kouanda S, Ky-Zerbo O, et al. Examining the correlates of sexually transmitted infection testing among men who have sex with men in Ouagadougou and Bobo-Dioulasso, Burkina Faso. Sex Transm Dis 2016; 43 302–9.
| Examining the correlates of sexually transmitted infection testing among men who have sex with men in Ouagadougou and Bobo-Dioulasso, Burkina Faso.Crossref | GoogleScholarGoogle Scholar | 27100767PubMed |
[47] Ong JJ, Liao M, Lee A, Fu H, Pan SW, Tang W, et al. Bridging the HIV-syphilis testing gap: dual testing among men who have sex with men living in China. Sex Transm Infect 2018; 45 382–86.
| Bridging the HIV-syphilis testing gap: dual testing among men who have sex with men living in China.Crossref | GoogleScholarGoogle Scholar |
[48] de Voux A, Bernstein K, Bradley H, Kirkcaldy RD, Tie Y, Shouse RL, et al. Syphilis testing among sexually active men who have sex with men and who are receiving medical care for HIV in the United States-Medical Monitoring Project, 2013–2014. Nephrol Dial Transplant 2018; 68 934–39.
[49] Logie CH, Kenny KS, Lacombe-Duncan A, Wang Y, Levermore K, Jones N, et al. Factors associated with sexually transmissible infection testing practices among men who have sex with men in Jamaica: results from a cross-sectional, tablet-based survey. Sex Health 2018; 15 325–34.
| Factors associated with sexually transmissible infection testing practices among men who have sex with men in Jamaica: results from a cross-sectional, tablet-based survey.Crossref | GoogleScholarGoogle Scholar | 29925463PubMed |
[50] Singh V, Crosby RA, Gratzer B, Gorbach PM, Markowitz LE, Meites E. Disclosure of sexual behavior is significantly associated with receiving a panel of health care services recommended for men who have sex with men. Sex Transm Dis 2018; 45 803–7.
| Disclosure of sexual behavior is significantly associated with receiving a panel of health care services recommended for men who have sex with men.Crossref | GoogleScholarGoogle Scholar | 29944645PubMed |
[51] Mebrahtu H, Furegato M, Sile B, Were J, Mohammed H, Hughes G. Access of non-specialist sexual health services by men who have sex with men: do they differ from those attending specialist services? Sex Transm Infect 2018; 94 72–74.
| Access of non-specialist sexual health services by men who have sex with men: do they differ from those attending specialist services?Crossref | GoogleScholarGoogle Scholar | 27888206PubMed |
[52] Wu D, Tang W, Lu H, Zhang TP, Cao B, Ong JJ, et al. Leading by example: web-based sexual health influencers among men who have sex with men have higher HIV and syphilis testing rates in China. J Med Internet Res 2019; 21 e10171
| Leading by example: web-based sexual health influencers among men who have sex with men have higher HIV and syphilis testing rates in China.Crossref | GoogleScholarGoogle Scholar | 30664490PubMed |
[53] Petroll AE, DiFranceisco W, McAuliffe TL, Seal DW, Kelly JA, Pinkerton SD. HIV testing rates, testing locations, and healthcare utilization among urban African-American men. J Urban Health 2009; 86 119
| HIV testing rates, testing locations, and healthcare utilization among urban African-American men.Crossref | GoogleScholarGoogle Scholar | 19067176PubMed |
[54] Ober AJ, Martino SC, Ewing B, Tucker JS. If you provide the test, they will take it: factors associated with HIV/STI testing in a representative sample of homeless youth in Los Angeles. AIDS Educ Prev 2012; 24 350–62.
| If you provide the test, they will take it: factors associated with HIV/STI testing in a representative sample of homeless youth in Los Angeles.Crossref | GoogleScholarGoogle Scholar | 22827904PubMed |
[55] Arnold EA, Sterrett-Hong E, Jonas A, Pollack LM. Social networks and social support among ball-attending African American men who have sex with men and transgender women are associated with HIV-related outcomes. Glob Public Health 2018; 13 144–58.
| Social networks and social support among ball-attending African American men who have sex with men and transgender women are associated with HIV-related outcomes.Crossref | GoogleScholarGoogle Scholar | 27169632PubMed |
[56] Neary J, Wagner AD, Mugo C, Mutiti PM, Bukusi D, John-Stewart GC, et al. Influence and involvement of support people in adolescent and young adult HIV testing. AIDS Care 2019; 31 105–12.
| Influence and involvement of support people in adolescent and young adult HIV testing.Crossref | GoogleScholarGoogle Scholar | 30261747PubMed |
[57] Regan S, Losina E, Chetty S, Giddy J, Walensky RP, Ross D, et al. Factors associated with self-reported repeat HIV testing after a negative result in Durban, South Africa. PLoS One 2013; 8 e62362
| Factors associated with self-reported repeat HIV testing after a negative result in Durban, South Africa.Crossref | GoogleScholarGoogle Scholar | 23626808PubMed |
