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Derivation of an HIV Risk Score for African Women Who Engage in Sex Work

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Abstract

No tool exists to stratify HIV risk in contemporary African female sex worker (FSW) populations. Data from a cohort of HIV-negative FSWs in Mombasa, Kenya from 2010 to 2017 were used to conduct a survival analysis assessing predictors of HIV infection. Stepwise regression was used to construct a multivariable model that formed the basis for the score. Seventeen HIV infections occurred over 1247 person-years of follow-up contributed by 670 women. Using depot medroxyprogesterone acetate (DMPA), having a curable sexually transmitted infection (STI), and being married contributed points to the score. HIV incidence was 0.85/100 person-years in a lower-risk group and 3.10/100 person-years in a higher-risk group. In a cohort with overall HIV incidence < 1.50/100 person-years, this risk score identified a subgroup of FSWs with HIV incidence > 3.00/100 person-years, which is the threshold used by the World Health Organization for initiating pre-exposure prophylaxis (PrEP). If validated in an external population, this tool could be useful for targeted PrEP promotion among higher-risk FSWs.

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References

  1. Kreiss J, Koech D, Plummer F, et al. AIDS virus infection in Nairobi prostitutes. Spread of the epidemic to East Africa. N Engl J Med. 1986;314(7):414–8.

    Article  CAS  PubMed  Google Scholar 

  2. UNAIDS. Fact Sheet—World AIDS Day 2020. https://www.unaids.org/en/resources/documents/2020/UNAIDS_FactSheet

  3. Shannon K, Crago AL, Baral SD, et al. The global response and unmet actions for HIV and sex workers. Lancet. 2018;392(10148):698–710.

    Article  PubMed  PubMed Central  Google Scholar 

  4. UNAIDS. Miles to go—closing gaps, breaking barriers, righting injustices. 2018. https://www.unaids.org/en/resources/documents/2018/global-aids-update

  5. Eakle R, Gomez GB, Naicker N, et al. HIV pre-exposure prophylaxis and early antiretroviral treatment among female sex workers in South Africa: results from a prospective observational demonstration project. PLoS Med. 2017;14(11):e1002444.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Koss CA, Charlebois ED, Ayieko J, et al. Uptake, engagement, and adherence to pre-exposure prophylaxis offered after population HIV testing in rural Kenya and Uganda: 72-week interim analysis of observational data from the SEARCH study. Lancet HIV. 2020;7(4):e249–61.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Glick JL, Russo R, Jivapong B, et al. The PrEP care continuum among cisgender women who sell sex and/or use drugs globally: a systematic review. AIDS Behav. 2020;24(5):1312–33.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Restar AJ, Tocco JU, Mantell JE, et al. Perspectives on HIV pre- and post- exposure prophylaxes (PrEP and PEP) among female and male sex workers in Mombasa, Kenya: implications for integrating biomedical prevention into sexual health services. AIDS Educ Prev. 2017;29(2):141–53.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Eakle R, Bothma R, Bourne A, et al. “I am still negative”: female sex workers’ perspectives on uptake and use of daily pre-exposure prophylaxis for HIV prevention in South Africa. PLoS ONE. 2019;14(4):e0212271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Shea J, Bula A, Dunda W, et al. “The drug will help protect my tomorrow”: perceptions of integrating PrEP into HIV prevention behaviors among female sex workers in Lilongwe, Malawi. AIDS Educ Prev. 2019;31(5):421–32.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Pillay D, Stankevitz K, Lanham M, et al. Factors influencing uptake, continuation, and discontinuation of oral PrEP among clients at sex worker and MSM facilities in South Africa. PLoS ONE. 2020;15(4):e0228620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Haberer JE, Kidoguchi L, Heffron R, et al. Alignment of adherence and risk for HIV acquisition in a demonstration project of pre-exposure prophylaxis among HIV serodiscordant couples in Kenya and Uganda: a prospective analysis of prevention-effective adherence. J Int AIDS Soc. 2017;20(1):21842.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Pyra M, Brown ER, Haberer JE, et al. Patterns of oral PrEP adherence and HIV risk among eastern African women in HIV serodiscordant partnerships. AIDS Behav. 2018;22(11):3718–25.

    Article  PubMed  PubMed Central  Google Scholar 

  14. World Health Organization. Report on key populations in African HIV/AIDS: National Strategic Plans. 2018. https://www.who.int/hiv/pub/toolkits/key-population-report-afro/en/

  15. World Health Organization. Guideline on when to start antiretroviral therapy and on pre-exposure prophylaxis for HIV. 2015. https://www.who.int/hiv/pub/guidelines/earlyrelease-arv/en/

  16. McClelland RS, Richardson BA, Cherutich P, et al. A 15-year study of the impact of community antiretroviral therapy coverage on HIV incidence in Kenyan female sex workers. AIDS. 2015;29(17):2279–86.

    Article  PubMed  Google Scholar 

  17. Diabaté S, Chamberland A, Geraldo N, et al. Gonorrhea, chlamydia and HIV incidence among female sex workers in Cotonou, Benin: a longitudinal study. PLoS ONE. 2018;13(5):e0197251.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Bazzi AR, Rangel G, Martinez G, et al. Incidence and predictors of HIV and sexually transmitted infections among female sex workers and their intimate male partners in northern Mexico: a longitudinal, multilevel study. Am J Epidemiol. 2015;181(9):723–31.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Li J, Zhang H, Shen Z, et al. Screening for acute HIV infections and estimating HIV incidence among female sex workers from low-grade venues in Guangxi, China. PLoS ONE. 2014;9(6):e99522.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Sharifi H, Mirzazadeh A, Shokoohi M, et al. Estimation of HIV incidence and its trend in three key populations in Iran. PLoS ONE. 2018;13(11):e0207681.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Wang H, Reilly KH, Brown K, et al. HIV incidence and associated risk factors among female sex workers in a high HIV-prevalence area of China. Sex Transm Dis. 2012;39(11):835–41.

    Article  PubMed  Google Scholar 

  22. Haukoos JS, Lyons MS, Lindsell CJ, et al. Derivation and validation of the Denver human immunodeficiency virus (HIV) risk score for targeted HIV screening. Am J Epidemiol. 2012;175(8):838–46.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Smith DK, Pals SL, Herbst JH, et al. Development of a clinical screening index predictive of incident HIV infection among men who have sex with men in the United States. J Acquir Immune Defic Syndr. 2012;60(4):421–7.

    Article  PubMed  Google Scholar 

  24. Menza TW, Hughes JP, Celum CL, et al. Prediction of HIV acquisition among men who have sex with men. Sex Transm Dis. 2009;36(9):547–55.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Hoenigl M, Weibel N, Mehta SR, et al. Development and validation of the San Diego early test score to predict acute and early HIV infection risk in men who have sex with men. Clin Infect Dis. 2015;61(3):468–75.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Wahome E, Thiong’o AN, Mwashigadi G, et al. An empiric risk score to guide PrEP targeting among MSM in coastal Kenya. AIDS Behav. 2018;22(Suppl 1):35–44.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kahle EM, Hughes JP, Lingappa JR, et al. An empiric risk scoring tool for identifying high-risk heterosexual HIV-1-serodiscordant couples for targeted HIV-1 prevention. J Acquir Immune Defic Syndr. 2013;62(3):339–47.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kagaayi J, Gray RH, Whalen C, et al. Indices to measure risk of HIV acquisition in Rakai, Uganda. PLoS ONE. 2014;9(4):e92015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Pintye J, Drake AL, Kinuthia J, et al. A risk assessment tool for identifying pregnant and postpartum women who may benefit from preexposure prophylaxis. Clin Infect Dis. 2017;64(6):751–8.

    PubMed  Google Scholar 

  30. Balkus JE, Brown E, Palanee T, et al. An empiric HIV risk scoring tool to predict HIV-1 acquisition in African women. J Acquir Immune Defic Syndr. 2016;72(3):333–43.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Baeten JM, Richardson BA, Martin HL Jr, et al. Trends in HIV-1 incidence in a cohort of prostitutes in Kenya: implications for HIV-1 vaccine efficacy trials. J Acquir Immune Defic Syndr. 2000;24(5):458–64.

    Article  CAS  PubMed  Google Scholar 

  32. Sabo MC, Richardson BA, Lavreys L, et al. Does bacterial vaginosis modify the effect of hormonal contraception on HIV seroconversion. AIDS. 2019;33(7):1225–30.

    Article  PubMed  Google Scholar 

  33. Masese L, Baeten JM, Richardson BA, et al. Incident herpes simplex virus type 2 infection increases the risk of subsequent episodes of bacterial vaginosis. J Infect Dis. 2014;209(7):1023–7.

    Article  PubMed  Google Scholar 

  34. Lavreys L, Baeten JM, Kreiss JK, et al. Injectable contraceptive use and genital ulcer disease during the early phase of HIV-1 infection increase plasma virus load in women. J Infect Dis. 2004;189(2):303–11.

    Article  PubMed  Google Scholar 

  35. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J Clin Microbiol. 1991;29(2):297–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Richardson BA, Mbori-Ngacha D, Lavreys L, et al. Comparison of human immunodeficiency virus type 1 viral loads in Kenyan women, men, and infants during primary and early infection. J Virol. 2003;77(12):7120–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Busch MP, Lee LL, Satten GA, et al. Time course of detection of viral and serologic markers preceding human immunodeficiency virus type 1 seroconversion: implications for screening of blood and tissue donors. Transfusion. 1995;35(2):91–7.

    Article  CAS  PubMed  Google Scholar 

  38. Penn State Eberly College of Science. STAT 501—regression methods—stepwise regression. https://online.stat.psu.edu/stat501/lesson/10/10.2

  39. Dean AG, Sullivan KM, Soe MM. Open Epi: Open Source Epidemiologic Statistics for Public Health, Version 3.01. www.openepi.com

  40. Odek WO, Githuka GN, Avery L, et al. Estimating the size of the female sex worker population in Kenya to inform HIV prevention programming. PLoS ONE. 2014;9(3):e89180.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Murray L, Moreno L, Rosario S, et al. The role of relationship intimacy in consistent condom use among female sex workers and their regular paying partners in the Dominican Republic. AIDS Behav. 2007;11(3):463–70.

    Article  PubMed  Google Scholar 

  42. Deering KN, Bhattacharjee P, Bradley J, et al. Condom use within non-commercial partnerships of female sex workers in southern India. BMC Public Health. 2011;11(Suppl 6):S11.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Voeten HACM, Egesah OB, Varkevisser CM, et al. Female sex workers and unsafe sex in urban and rural Nyanza, Kenya: regular partners may contribute more to HIV transmission than clients. Trop Med Int Heal. 2007;12(2):174–82.

    CAS  Google Scholar 

  44. Luchters S, Richter ML, Bosire W, et al. The contribution of emotional partners to sexual risk taking and violence among female sex workers in Mombasa, Kenya: a cohort study. PLoS ONE. 2013;8(8):e68855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Goldenberg SM, Gallardo Cruz M, Strathdee SA, et al. Correlates of unprotected sex with female sex workers among male clients in Tijuana, Mexico. Sex Transm Dis. 2010;37(5):319–24.

    Article  PubMed  PubMed Central  Google Scholar 

  46. McClelland L, Wanje G, Kashonga F, et al. Understanding the context of HIV risk behavior among HIV-positive and HIV-negative female sex workers and male bar clients following antiretroviral therapy rollout in Mombasa, Kenya. AIDS Educ Prev. 2011;23(4):299–312.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Lowndes CM, Alary M, Gnintoungbé CA, et al. Management of sexually transmitted diseases and HIV prevention in men at high risk: targeting clients and non-paying sexual partners of female sex workers in Benin. AIDS. 2000;14(16):2523–34.

    Article  CAS  PubMed  Google Scholar 

  48. Côté AM, Sobela F, Dzokoto A, et al. Transactional sex is the driving force in the dynamics of HIV in Accra, Ghana. AIDS. 2004;18(6):917–25.

    Article  PubMed  Google Scholar 

  49. Martin HL Jr, Nyange PM, Richardson BA, et al. Hormonal contraception, sexually transmitted diseases, and risk of heterosexual transmission of human immunodeficiency virus type 1. J Infect Dis. 1998;178(4):1053–9.

    Article  PubMed  Google Scholar 

  50. Baeten JM, Benki S, Chohan V, et al. Hormonal contraceptive use, herpes simplex virus infection, and risk of HIV-1 acquisition among Kenyan women. AIDS. 2007;21(13):1771–7.

    Article  PubMed  Google Scholar 

  51. Lavreys L, Baeten JM, Martin HL Jr, et al. Hormonal contraception and risk of HIV-1 acquisition: results of a 10-year prospective study. AIDS. 2004;18(4):695–7.

    Article  PubMed  Google Scholar 

  52. Polis CB, Curtis KM, Hannaford PC, et al. An updated systematic review of epidemiological evidence on hormonal contraceptive methods and HIV acquisition in women. AIDS. 2016;30(17):2665–83.

    Article  CAS  PubMed  Google Scholar 

  53. Ahmed K, Baeten JM, Beksinska M, et al. HIV incidence among women using intramuscular depot medroxyprogesterone acetate, a copper intrauterine device, or a levonorgestrel implant for contraception: a randomised, multicentre, open-label trial. Lancet. 2019;394(10195):303–13.

    Article  Google Scholar 

  54. Masha SC, Cools P, Sanders EJ, et al. Trichomonas vaginalis and HIV infection acquisition: a systematic review and meta-analysis. Sex Transm Infect. 2019;95(1):36–42.

    Article  PubMed  Google Scholar 

  55. Ward H, Rönn M. Contribution of sexually transmitted infections to the sexual transmission of HIV. Curr Opin HIV AIDS. 2010;5(4):305–10.

    Article  PubMed  PubMed Central  Google Scholar 

  56. 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 Transm Infect. 1999;75(1):3–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol. 2004;2(1):33–42.

    Article  CAS  PubMed  Google Scholar 

  58. World Health Organization. Report on global sexually transmitted infection surveillance. 2018. https://www.who.int/reproductivehealth/publications/stis-surveillance-2018/en/

  59. Boyadzhyan B, Yashina T, Yatabe JH, et al. Comparison of the APTIMA CT and GC assays with the APTIMA Combo 2 assay, the Abbott LCx assay, and direct fluorescent-antibody and culture assays for detection of Chlamydia trachomatis and Neisseria gonorrhoeae. J Clin Microbiol. 2004;42(7):3089–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Smith G. Step away from stepwise. J Big Data. 2018;5:32.

    Article  Google Scholar 

  61. Verguet S, Stalcup M, Walsh JA. Where to deploy pre-exposure prophylaxis (PrEP) in sub-Saharan Africa? Sex Transm Infect. 2013;89(8):628–34.

    Article  PubMed  Google Scholar 

  62. McGillen JB, Anderson SJ, Hallett TB. PrEP as a feature in the optimal landscape of combination HIV prevention in sub-Saharan Africa. J Int AIDS Soc. 2016;19(7(Suppl 6)):21104.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Gomez GB, Borquez A, Case KK, et al. The cost and impact of scaling up pre-exposure prophylaxis for HIV prevention: a systematic review of cost-effectiveness modelling studies. PLoS Med. 2013;10(3):e1001401.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Bowring AL, Ketende S, Rao A, et al. Characterising unmet HIV prevention and treatment needs among young female sex workers and young men who have sex with men in Cameroon: a cross-sectional analysis. Lancet Child Adolesc Heal. 2019;3(7):482–91.

    Article  Google Scholar 

  65. Napierala S, Chabata ST, Fearon E, et al. Engagement in HIV care among young female sex workers in Zimbabwe. J Acquir Immune Defic Syndr. 2018;79(3):358–66.

    Article  PubMed  Google Scholar 

  66. UN Women. Facts and figures: HIV and AIDS. 2018. https://www.unwomen.org/en/what-we-do/hiv-and-aids/facts-and-figures

  67. McClelland RS, Lavreys L, Hassan WM, et al. Vaginal washing and increased risk of HIV-1 acquisition among African women: A 10-year prospective study. AIDS. 2006;20(2):269–73.

    Article  PubMed  Google Scholar 

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Acknowledgements

We acknowledge the time and commitment of the women of the Mombasa Cohort, without whom this work would not have been possible. We are grateful for the clinical, laboratory, and administrative staff in Mombasa and Seattle for their daily efforts to maintain the cohort and study site. We thank Caroline Mwalimu for time spent cleaning and organizing data and Jennifer Balkus for helpful discussions concerning methods for this analysis.

Funding

This study was funded by a grant from the NIH/NIAID (R37 AI38518/HD103571). RSM receives support for mentoring through NICHD K24 HD88229. Infrastructure support for the research site in Mombasa was provided by the University of Washington’s Center for AIDS Research (CFAR), an NIH funded program (P30 AI027757) that is supported by the following centers: NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NCCAM. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Authors and Affiliations

  1. University of Washington School of Medicine, Seattle, WA, USA

    Alexandra C. Willcox

  2. Medical Scientist Training Program, University of Washington, Seattle, WA, USA

    Alexandra C. Willcox

  3. Department of Biostatistics, University of Washington, Seattle, WA, USA

    Barbra A. Richardson

  4. Department of Global Health, University of Washington, 325 9th Avenue, Box 359909, Seattle, WA, 98104, USA

    Barbra A. Richardson, Kishorchandra Mandaliya & R. Scott McClelland

  5. Department of Medicine, University of Washington, Seattle, WA, USA

    Juma Shafi, Emmanuel Kabare & R. Scott McClelland

  6. Department of Epidemiology, University of Washington, Seattle, WA, USA

    R. Scott McClelland

  7. Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Barbra A. Richardson

  8. Human Biology Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Julie Overbaugh

  9. Department of Medical Microbiology, University of Nairobi, Nairobi, Kenya

    Juma Shafi, Emmanuel Kabare, Walter Jaoko & R. Scott McClelland

  10. Kenyatta National Hospital, University of Nairobi, Nairobi, Kenya

    John Kinuthia

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Contributions

Conceptualization: RSM; Methodology: ACW, BAR, RSM; Formal analysis and investigation: ACW; Writing—original draft preparation: ACW, RSM; Writing—review and editing: BAR, JS, EK, JK, WJ, KM, JO, RSM; Funding acquisition: JO, RSM; Resources: RSM; Supervision: RSM.

Corresponding author

Correspondence to R. Scott McClelland.

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Conflict of interest

RSM receives research funding, paid to the University of Washington, from Hologic Corporation, and has received honoraria for consulting from Lupin Pharmaceuticals.

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All participants provided written informed consent to participate in the research.

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No identifiable information links individual participants to this work.

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This study was approved by the Institutional Review Boards at Kenyatta National Hospital and the University of Washington.

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Willcox, A.C., Richardson, B.A., Shafi, J. et al. Derivation of an HIV Risk Score for African Women Who Engage in Sex Work. AIDS Behav 25, 3292–3302 (2021). https://doi.org/10.1007/s10461-021-03235-7

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