Abstract
Pre-exposure prophylaxis (PrEP) use may be associated with risk compensation. We enrolled and provided PreP to sexual and gender minorities (SGM) in Abuja, Nigeria between April 2018 and May 2019. Behavioral information and samples for urogenital and anorectal Chlamydia trachomatis and Neisseria gonorrhoeae sexually transmitted infections (STIs) were collected at baseline. Blood samples for PrEP assay and self-reported adherence were collected at three-monthly follow-up visits. STIs were detected using Aptima Combo2 assay. We estimated the odds ratios (ORs) of PCR-diagnosed bacterial STIs and self-reported behavioral outcomes (condomless anal intercourse [CAI] and concurrent sexual relationships) with conditional logistic regression. Of 400 SGM who initiated PrEP, 206 were eligible for analysis, and had a median age of 24 years (IQR 22–27). In multivariable analysis, participants in the PrEP period had decreased odds of CAI (adjusted OR: 0.49, 95% CI 0.28, 0.84). PrEP use was not associated with risk compensation.
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Data, materials, and code cannot be shared publicly due to the institutionalized criminalization of same sex relationship in Nigeria (country of study). The study investigators are committed to protecting the privacy of all participants. However, the IRB protocol allows the publication of aggregated data that can be requested from implementationscienceunit@somumaryland.onmicrosoft.com.
References
Adeyemi, O. A., Nowak, R. G., Marzinke, M., Morgan, D., Sam-Agudu, N., Craddock, J., Zhan, M., Crowell, T. A., Baral, S., Ndembi, N., Adebajo, S., & Charurat, M. E. (2023). Correlates of self-reported and biomarker based adherence to daily oral HIV pre-exposure prophylaxis among a cohort of predominantly men who have sex with men in Nigeria. PLoS ONE, 18(3), e0282999. https://doi.org/10.1371/journal.pone.0282999
Baral, S. D., Ketende, S., Schwartz, S., Orazulike, I., Ugoh, K., Peel, S. A., Ake, J., Blattner, W., & Charurat, M. (2015). Evaluating respondent-driven sampling as an implementation tool for universal coverage of antiretroviral studies among men who have sex with men living with HIV. Journal of Acquired Immune Deficiency Syndromes, 68, S107–S113. https://doi.org/10.1097/QAI.0000000000000438
Battle, J. J., & Bennett, N. D. A. (2007). Striving for place: Lesbian, gay, bisexual, and transgender (LGBT) people. In A companion to African American history (pp. 412–445). Blackwell Publishing Ltd. https://doi.org/10.1002/9780470996720.ch26
Beyrer, C., Sullivan, P., Sanchez, J., Baral, S. D., Collins, C., Wirtz, A. L., Altman, D., Trapence, G., & Mayer, K. (2013). The increase in global HIV epidemics in MSM. AIDS, 27(17), 2665–2678. https://doi.org/10.1097/01.aids.0000432449.30239.fe
Buchbinder, S. P. (2018). Maximizing the benefits of HIV preexposure prophylaxis. Topics in Antiviral Medicine, 25(4), 138–142. http://www.ncbi.nlm.nih.gov/pubmed/29689539.
Cassell, M., Halperin, D. T., Shelton, J. D., & Stanton, D. (2006). Risk compensation: The Achilles’ heel of innovations in HIV prevention? British Medical Journal, 332(7541), 605–607. https://doi.org/10.1136/bmj.332.7541.605
Dean, L., Meyer, I. H., Robinson, K., Sell, R. L., Sember, R., Silenzio, V. M. B., Bowen, D. J., Bradford, J., Rothblum, E., White, J., Dunn, P., Lawrence, A., Wolfe, D., Xavier, J., Carter, D., Pittman, J., & Tierney, R. (2000). Lesbian, gay, bisexual, and transgender health: Findings and concerns. Journal of the Gay and Lesbian Medical Association, 4(3), 101–151.
FMOH. (2014). Guidelines for young persons’ participation in research and access to sexual and reproductive health services in Nigeria. https://www.popcouncil.org/uploads/pdfs/2014HIV_YoungPersonsSRH-Nigeria.pdf
Fonner, V. A., Dalglish, S. L., Kennedy, C. E., Baggaley, R., O’Reilly, K. R., Koechlin, F. M., Rodolph, M., Hodges-Mameletzis, I., & Grant, R. M. (2016). Effectiveness and safety of oral HIV preexposure prophylaxis for all populations. AIDS, 30(12), 1973–1983. https://doi.org/10.1097/QAD.0000000000001145
Golub, S A, Pena, S., Fikslin, R. A., Goldberg, M., & Radix, A. (2018). Partners, not condom use, drive STI rates among PrEP users in community health center. Topics in Antiviral Medicine, 26, 468s. https://www.embase.com/search/results?subaction=viewrecord&id=L621729406&from=export
Golub, S. A., Gamarel, K. E., Rendina, H. J., Surace, A., & Lelutiu-Weinberger, C. L. (2013). From efficacy to effectiveness: Facilitators and barriers to PrEP acceptability and motivations for adherence among MSM and transgender women in New York City. AIDS Patient Care and STDs, 27(4), 248–254. https://doi.org/10.1089/apc.2012.0419
Grant, R. M., Lama, J. R., Anderson, P. L., McMahan, V., Liu, A. Y., Vargas, L., Goicochea, P., Casapía, M., Guanira-Carranza, J. V., Ramirez-Cardich, M. E., Montoya-Herrera, O., Fernández, T., Veloso, V. G., Buchbinder, S. P., Chariyalertsak, S., Schechter, M., Bekker, L.-G., Mayer, K. H., Kallás, E. G., for the iPrEx Study Team. (2010). Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. New England Journal of Medicine, 363(27), 2587–2599. https://doi.org/10.1056/NEJMoa1011205
Hendrix, C. W., Andrade, A., Bumpus, N. N., Kashuba, A. D., Marzinke, M. A., Moore, A., Anderson, P. L., Bushman, L. R., Fuchs, E. J., Wiggins, I., Radebaugh, C., Prince, H. A., Bakshi, R. P., Wang, R., Richardson, P., Shieh, E., McKinstry, L., Li, X., Donnell, D., & Patterson, K. B. (2016). Dose frequency ranging pharmacokinetic study of tenofovir-emtricitabine after directly observed dosing in healthy volunteers to establish adherence benchmarks (HPTN 066). AIDS Research and Human Retroviruses, 32(1), 32–43. https://doi.org/10.1089/aid.2015.0182
Holt, M., & Murphy, D. A. (2017). Individual versus community-level risk compensation following preexposure prophylaxis of HIV. American Journal of Public Health, 107(10), 1568–1571. https://doi.org/10.2105/AJPH.2017.303930
Hoornenborg, E., Coyer, L., van Laarhoven, A., Achterbergh, R., de Vries, H., Prins, M., & van der Loeff, M. S. (2018). Change in sexual risk behaviour after 6 months of pre-exposure prophylaxis use. AIDS, 32(11), 1527–1532. https://doi.org/10.1097/QAD.0000000000001874
Jenness, S. M., Weiss, K. M., Goodreau, S. M., Gift, T., Chesson, H., Hoover, K. W., Smith, D. K., Liu, A. Y., Sullivan, P. S., & Rosenberg, E. S. (2017). Incidence of Gonorrhea and Chlamydia following human immunodeficiency virus preexposure prophylaxis among men who have sex with men: A modeling study. Clinical Infectious Diseases, 65(5), 712–718. https://doi.org/10.1093/cid/cix439
Kirkcaldy, R. D., Zaidi, A., Hook, E. W., Holmes, K. H., Soge, O., Del Rio, C., Hall, G., Papp, J., Bolan, G., & Weinstock, H. S. (2013). Neisseria gonorrhoeae antimicrobial resistance among men who have sex with men and men who have sex exclusively with women: The Gonococcal Isolate Surveillance Project, 2005–2010. Annals of Internal Medicine, 158(5 PART 1). https://doi.org/10.7326/0003-4819-158-5-201303050-00004.
Kumar, S., Haderxhanaj, L. T., & Spicknall, I. H. (2021). Reviewing PrEP’s effect on STI incidence among men who have sex with men—balancing increased STI screening and potential behavioral sexual risk compensation. AIDS and Behavior, 25(6), 1810–1818. https://doi.org/10.1007/s10461-020-03110-x
Lal, L., Audsley, J., Murphy, D. A., Fairley, C. K., Stoove, M., Roth, N., Moore, R., Tee, B. K., Puratmaja, N., Anderson, P. L., Leslie, D., Grant, R. M., De Wit, J., & Wright, E. (2017). Medication adherence, condom use and sexually transmitted infections in Australian preexposure prophylaxis users. AIDS, 31(12), 1709–1714. https://doi.org/10.1097/QAD.0000000000001519
Liu, A. Y., Vittinghoff, E., Chillag, K., Mayer, K., Thompson, M., Grohskopf, L., Colfax, G., Pathak, S., Gvetadze, R., O’Hara, B., Collins, B., Ackers, M., Paxton, L., & Buchbinder, S. P. (2013). Sexual risk behavior among HIV-uninfected men who have sex with men participating in a tenofovir preexposure prophylaxis randomized trial in the United States. Journal of Acquired Immune Deficiency Syndromes, 64, 87–94. https://doi.org/10.1097/QAI.0b013e31828f097a
Liu, A. Y., Vittinghoff, E., von Felten, P., Rivet Amico, K., Anderson, P. L., Lester, R., Andrew, E., Estes, I., Serrano, P., Brothers, J., Buchbinder, S., Hosek, S., & Fuchs, J. D. (2019). Randomized controlled trial of a mobile health intervention to promote retention and adherence to preexposure prophylaxis among young people at risk for human immunodeficiency virus: The EPIC Study. Clinical Infectious Diseases, 68(12), 2010–2017. https://doi.org/10.1093/cid/ciy810
Maljaars, L. P., Gill, K., Smith, P. J., Gray, G. E., Dietrich, J. J., Gomez, G. B., & Bekker, L. G. (2017). Condom migration after introduction of pre-exposure prophylaxis among HIV-uninfected adolescents in South Africa: A cohort analysis. Southern African Journal of HIV Medicine, 18(1). https://doi.org/10.4102/sajhivmed.v18i1.712
Marcus, J. L., Glidden, D. V., Mayer, K. H., Liu, A. Y., Buchbinder, S. P., Amico, K. R., McMahan, V., Kallas, E. G., Montoya-Herrera, O., Pilotto, J., & Grant, R. M. (2013). No evidence of sexual risk compensation in the iPrEx Trial of daily oral HIV preexposure prophylaxis. PLoS ONE, 8(12), e81997. https://doi.org/10.1371/journal.pone.0081997
Marcus, J. L., Katz, K. A., Krakower, D. S., & Calabrese, S. K. (celiac). Risk compensation and clinical decision making—the case of HIV preexposure prophylaxis. New England Journal of Medicine, 380(6), 510–512. https://doi.org/10.1056/NEJMp1810743
Montaño, M. A., Dombrowski, J. C., Dasgupta, S., Golden, M. R., Duerr, A., Manhart, L. E., Barbee, L. A., & Khosropour, C. M. (2019a). Changes in sexual behavior diagnoses among initiating clinic setting. AIDS and Behavior, 23, 548–555. https://doi.org/10.1007/s10461-018-2252-9.
Montaño, M. A., Dombrowski, J. C., Dasgupta, S., Golden, M. R., Duerr, A., Manhart, L. E., Barbee, L. A., & Khosropour, C. M. (2019b). Changes in sexual behavior and STI diagnoses among MSM initiating PrEP in a clinic setting. AIDS and Behavior, 23(2), 548–555. https://doi.org/10.1007/s10461-018-2252-9
Newcomb, M. E., Moran, K., Feinstein, B. A., Forscher, E., & Mustanski, B. (2018). Pre-exposure prophylaxis (PrEP) use and condomless anal sex: Evidence of risk compensation in a cohort of young men who have sex with men. Journal of Acquired Immune Deficiency Syndromes, 77, 358–364. https://doi.org/10.1097/QAI.0000000000001604
Nguyen, V.-K., Greenwald, Z. R., Trottier, H., Cadieux, M., Goyette, A., Beauchemin, M., Charest, L., Longpré, D., Lavoie, S., Tossa, H. G., & Thomas, R. (2018). Incidence of sexually transmitted infections before and after pre-exposure prophylaxis for HIV. AIDS, 32(4), 523–530. https://doi.org/10.1097/QAD.0000000000001718
Oldenburg, C. E., Nunn, A. S., Montgomery, M., Almonte, A., Mena, L., Patel, R. R., Mayer, K. H., & Chan, P. A. (2018). Behavioral changes following uptake of HIV pre-exposure prophylaxis among men who have sex with men in a clinical setting. AIDS and Behavior, 22(4), 1075–1079. https://doi.org/10.1007/s10461-017-1701-1
Sagaon-Teyssier, L., Suzan-Monti, M., Demoulin, B., Capitant, C., Lorente, N., Préau, M., Mora, M., Rojas Castro, D., Chidiac, C., Chas, J., Meyer, L., Molina, J. M., & Spire, B. (2016). Uptake of PrEP and condom and sexual risk behavior among MSM during the ANRS IPERGAY trial. AIDS Care—Psychological and Socio-Medical Aspects of AIDS/HIV, 28, 48–55. https://doi.org/10.1080/09540121.2016.1146653
Spinner, C. D., Boesecke, C., Zink, A., Jessen, H., Stellbrink, H. J., Rockstroh, J. K., & Esser, S. (2016). HIV pre-exposure prophylaxis (PrEP): A review of current knowledge of oral systemic HIV PrEP in humans. Infection, 44(2), 151–158. https://doi.org/10.1007/s15010-015-0850-2
Stahlman, S., Johnston, L. G., Yah, C., Ketende, S., Maziya, S., Trapence, G., Jumbe, V., Sithole, B., Mothopeng, T., Mnisi, Z., & Baral, S. (2016). Respondent-driven sampling as a recruitment method for men who have sex with men in southern sub-Saharan Africa: A cross-sectional analysis by wave. Sexually Transmitted Infections, 92, 292–298. https://doi.org/10.1136/sextrans-2015-052184
UNAIDS. (2018). UNAIDS Data 2018. 1–376. https://www.unaids.org/sites/default/files/media_asset/2019-global-AIDS-update_en.pdf.
UNAIDS. (2019). 2018 global HIV statistics.
U.S. Food and Drug Administration & Department of Health and Human Services. (2016). FDA approves first drug for reducing the risk of sexually acquired HIV infection. FDA Press Announcements. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm312210.htm
van Griensven, F., de Lind van Wijngaarden, J. W., Baral, S., & Grulich, A. (2009). The global epidemic of HIV infection among men who have sex with men. Current Opinion in HIV and AIDS, 4(4), 300–307. https://doi.org/10.1097/COH.0b013e32832c3bb3
Acknowledgements
We are grateful to all study participants and the staff of the TRUST/RV368 clinic for their participation and commitment to this study. In particular, we are grateful to Mr. Ruxton Adebiyi for his contributions to data management for this study.
Funding
This work was supported by Fogarty Epidemiology Research Training for Public Health Impact in Nigeria Program (D43TW010051) and the National Institutes of Health (R01 MH099001, R01 A120913, R01 MH110358). The views expressed in this manuscript are the authors and not the funders of the study.
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OAA conceptualized the study and drafted the initial manuscript. OAA analyzed the data under the guidance of MZ. RGN, DM, NASA, JC, MZ, TAC, SB, SA, and MEC reviewed and edited the manuscript. MEC was responsible for funding acquisition. RGN DM, NASA, JC, MZ, SA, and MEC supervised the study.
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Ethical clearance was obtained from the Federal Capital Territory Research Ethics Committee, Abuja (FHREC/2012/01/22/09-08-12), and the Institutional Review Board of the University of Maryland, Baltimore (HP-0052013).
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Adeyemi, O.A., Nowak, R.G., Morgan, D. et al. Risk Compensation After Initiation of Daily Oral Pre-exposure Prophylaxis Among Sexual and Gender Minorities in Nigeria. Arch Sex Behav (2024). https://doi.org/10.1007/s10508-024-02859-9
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DOI: https://doi.org/10.1007/s10508-024-02859-9