The Impact of Pre-exposure Prophylaxis for Human Immunodeficiency Virus on Gonorrhea Prevalence

Abstract

Pre-exposure prophylaxis (PrEP) has been shown to be highly effective in reducing the risk of HIV infection in gay and bisexual men who have sex with men (GbMSM). However, PrEP does not protect against other sexually transmitted infections (STIs). In some populations, PrEP has also led to riskier behavior such as reduced condom usage, with the result that the prevalence of bacterial STIs like gonorrhea has increased. Here, we develop a compartmental model of the transmission of HIV and gonorrhea and the impacts of PrEP, condom usage, STI testing frequency and potential changes in sexual risk behavior stemming from the introduction of PrEP in a population of GbMSM. We find that introducing PrEP causes an increase in gonorrhea prevalence for a wide range of parameter values, including at the currently recommended frequency of STI testing once every three months for individuals on PrEP. Moreover, the model predicts that a higher STI testing frequency alone is not enough to prevent a rise in gonorrhea prevalence, unless the testing frequency is increased to impractical levels. However, testing every 2 months in combination with a 10–25 % reduction in risky behavior by individuals on PrEP would maintain gonorrhea prevalence at pre-PrEP levels. The results emphasize that programs making PrEP more available should be accompanied by efforts to support condom usage and frequent STI testing, in order to avoid an increase in the prevalence of gonorrhea and other bacterial STIs.

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References

  1. Alaei K, Paynter CA, Juan S-C, Alaei A (2016) Using pre-exposure prophylaxis, losing condoms? Pre-exposure prophylaxis promotion may undermine safe sex. Aids 30(18):2753–2756

    Google Scholar 

  2. Alirol E, Wi TE, Bala M, Bazzo ML, Chen X-S, Deal C, Dillon J-AR, Kularatne R, Heim J, van Huijsduijnen RH et al (2017) Multidrug-resistant gonorrhea: a research and development roadmap to discover new medicines. PLoS Med 14(7):e1002366

    Google Scholar 

  3. Banks P, Marchand R, Robert W (2010) Gustafson R. Hogg R. Gilbert M. Trussler, T. and the ManCount Survey Team. Mancount sizes-up the gaps: a sexual health survey of gay men in Vancouver. Vancouver coastal health: Vancouver

  4. Bauch CT (2002) A versatile ODE approximation to a network model for the spread of sexually transmitted diseases. J Math Biol 45(5):375–395

    MathSciNet  MATH  Google Scholar 

  5. Bauch CT (2005) Imitation dynamics predict vaccinating behaviour. Proc R Soc B Biol Sci 272(1573):1669–1675

    Google Scholar 

  6. Bauch C, Rand DA (2000) A moment closure model for sexually transmitted disease transmission through a concurrent partnership network. Proc R Soc Lond Ser B Biol Sci 267(1456):2019–2027

    Google Scholar 

  7. Bérubé A (2003) The history of gay bathhouses. J Homosex 44(3–4):33–53

    Google Scholar 

  8. Beyrer C, Baral SD, Van Griensven F, Goodreau SM, Chariyalertsak S, Wirtz AL, Brookmeyer R (2012) Global epidemiology of HIV infection in men who have sex with men. Lancet 380(9839):367–377

    Google Scholar 

  9. Buonomo B, Carbone G, d’Onofrio A (2018) Effect of seasonality on the dynamics of an imitation-based vaccination model with public-health intervention. Math Biosci Eng 15(1):299–321

    MathSciNet  MATH  Google Scholar 

  10. Cates W Jr, Hunter Handsfield H (1988) HIV counseling and testing: does it work? Am J Public Health 78(12):1533–1534

    Google Scholar 

  11. Centre for Communicable Diseases, Infectious Disease Prevention Infection Control, and Public Health Agency of Canada Control Branch 92011) Public Health agency of canada. M-Track: Enhanced surveillance of HIV, sexually transmitted and blood-borne infections, and associated risk behaviours among men who have sex with men in Canada. phase 1 report

  12. Chow EPF, Medland NA, Denham I, Wright EJ, Fairley CK (2018) Decline in new HIV diagnoses among MSM in melbourne. Lancet HIV 5(9):e479–e481

    Google Scholar 

  13. Cihlar T, Fordyce M (2016) Current status and prospects of HIV treatment. Curr Opin Virol 18:50–56

    Google Scholar 

  14. Coffin JM, Hughes SH, Varmus HE (1997) Retroviral virions and genomes-retroviruses. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  15. Cunningham E, Chan Y-T, Aghaizu A, Bibby DF, Murphy G, Tosswill J, Harris RJ, Myers R, Field N, Delpech V et al. (2016) Enhanced surveillance of HIV-1 drug resistance in recently infected MSM in the UK. J Antimicrob Chemother, p dkw404

  16. Eames KTD, Keeling MJ (2002) Modeling dynamic and network heterogeneities in the spread of sexually transmitted diseases. Proc Nat Acad Sci 99(20):13330–13335

    Google Scholar 

  17. Fu F, Rosenbloom DI, Wang L, Nowak MA (2010) Imitation dynamics of vaccination behaviour on social networks. Proc R Soc B Biol Sci 278(1702):42–49

    Google Scholar 

  18. Gao L, Hethcote H (2006) Simulations of rubella vaccination strategies in China. Math Biosci 202(2):371–385

    MathSciNet  MATH  Google Scholar 

  19. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM et al (1999) Origin of HIV-1 in the chimpanzee pan troglodytes troglodytes. Nature 397(6718):436

    Google Scholar 

  20. Goedel WC, Mayer KH, Mimiaga MJ, Duncan DT (2017) Considerable interest in pre-exposure prophylaxis uptake among men who have sex with men recruited from a popular geosocial-networking smartphone application in London. Global public health, pp 1–10

  21. Ha S, Pogany L, Seto J, Wu J, Gale-Rowe M (2017) Sexually transmitted infections: what are Canadian primary care physicians prescribing for the treatment of Gonorrhea? Can Commun Dis Rep 43(2):33

    Google Scholar 

  22. Hammack PL, Meyer IH, Krueger EA, Marguerita L, Frost DM (2018) HIV testing and pre-exposure prophylaxis (PrEP) use, familiarity, and attitudes among gay and bisexual men in the United States: a national probability sample of three birth cohorts. PLoS One 13(9):e0202806

    Google Scholar 

  23. Hull M, Tan DHS (2017) Can we eliminate HIV?: setting the stage for expanding HIV pre-exposure prophylaxis use in Canada. Can Commun Dis Rep 43(12):272

    Google Scholar 

  24. Hurt CB, Eron JJ Jr, Cohen MS (2011) Pre-exposure prophylaxis and antiretroviral resistance: HIV prevention at a cost? Clin Infect Dis 53(12):1265–1270

    Google Scholar 

  25. Kalichman SC, Pellowski J, Turner C (2011) Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: systematic review with implications for using HIV treatments for prevention. Sex Trans Infect 87(3):183–190

    Google Scholar 

  26. Kent CK, Chaw JK, Wong W, Liska S, Gibson S, Hubbard G, Klausner JD (2005) Prevalence of rectal, urethral, and pharyngeal chlamydia and Gonorrhea detected in 2 clinical settings among men who have sex with men: San Francisco, California. Clin Infect Dis 41(1):67–74

    Google Scholar 

  27. Koechlin FM, Fonner VA, Dalglish SL, O’Reilly KR, Baggaley R, Grant RM, Rodolph M, Hodges-Mameletzis I, Kennedy CE (2017) Values and preferences on the use of oral pre-exposure prophylaxis (PrEP) for HIV prevention among multiple populations: a systematic review of the literature. AIDS Behav 21(5):1325–1335

    Google Scholar 

  28. Lotfi EM, Mahrouf M, Maziane M, Silva CJ, Torres DFM, Yousfi N (2018) A minimal HIV-AIDS infection model with general incidence rate and application to Morocco data. arXiv preprint arXiv:1812.06965

  29. Mansky LM (1998) Retrovirus mutation rates and their role in genetic variation. J Gen Virol 79(6):1337–1345

    Google Scholar 

  30. Martin I, Sawatzky P, Allen V, Lefebvre B, Hoang LMN, Naidu P, Minion J, Van Caeseele P, Haldane D, Gad RR et al. (2019) Multidrug-resistant and extensively drug-resistant gonorrhea in Canada, 2012–2016

  31. McCormack S, Dunn DT, Desai M, Dolling DI, Gafos M, Gilson R, Sullivan AK, Clarke A, Reeves I, Schembri G et al (2016) Pre-Exposure Prophylaxis to prevent the acquisition of HIV-1 infection (PROUD): effectiveness results from the pilot phase of a pragmatic open-label randomized trial. Lancet 387(10013):53–60

    Google Scholar 

  32. Mitchell JW, Horvath KJ (2013) Factors associated with regular HIV testing among a sample of US MSM with HIV-negative main partners. J Acquir Immune Defic Syndr 64(4):417

    Google Scholar 

  33. Montano MA, Dombrowski JC, Barbee LA, Golden MR, Khosropour CM (2017) Changes in sexual behavior and sti diagnoses among msm using prep in seattle, wa. Age 30(8):7

    Google Scholar 

  34. Morris M, Kretzschmar M (1997) Concurrent partnerships and the spread of HIV. Aids 11(5):641–648

    Google Scholar 

  35. Mosley T, Khaketla M, Armstrong HL, Cui Z, Sereda P, Lachowsky NJ, Hull MW, Olarewaju G, Jollimore J, Edward J et al (2018) Trends in awareness and use of HIV PrEP among gay, bisexual, and other men who have sex with men in Vancouver, Canada 2012–2016. AIDS Behav 22(11):3550–3565

    Google Scholar 

  36. Ndeffo Mbah ML, Liu J, Bauch CT, Tekel YI, Medlock J, Meyers LA, Galvani AP (2012) The impact of imitation on vaccination behavior in social contact networks. PLoS Comput Biol 8(4):e1002469

    MathSciNet  Google Scholar 

  37. Nwokolo N, Hill A, McOwan A, Pozniak A (2017) Rapidly declining HIV infection in MSM in central london. Lancet HIV 4(11):e482–e483

    Google Scholar 

  38. Pathela P, Braunstein SL, Braunstein SL, Blank S, Schillinger JA (2013) HIV incidence among men with and those without sexually transmitted rectal infections: estimates from matching against an HIV case registry. Clin Infect Dis 57(8):1203–1209

    Google Scholar 

  39. Patrick R, Forrest D, Cardenas G, Opoku J, Magnus M, Phillips IIG, Greenberg A, Metsch L, Kharfen M, LaLota M et al (2017) Awareness, willingness, and use of pre-exposure prophylaxis among men who have sex with men in Washington, DC and Miami-Dade county, FL: national HIV behavioral surveillance, 2011 and 2014. JAIDS J Acquir Immune Defic Syndr 75:S375–S382

    Google Scholar 

  40. Paxton LA, Hope T, Jaffe HW (2007) Pre-exposure prophylaxis for HIV infection: what if it works? Lancet 370(9581):89–93

    Google Scholar 

  41. Pinkerton SD, Abramson PR (1997) Effectiveness of condoms in preventing HIV transmission. Soc Sci Med 44(9):1303–1312

    Google Scholar 

  42. Poorolajal J, Molaeipoor L, Mohraz M, Mahjub H, Ardekani MT, Mirzapour P, Golchehregan H (2015) Predictors of progression to aids and mortality post-HIV infection: a long-term retrospective cohort study. AIDS Care 27(10):1205–1212

    Google Scholar 

  43. Prep use among gbmsm: What does it mean for sti prevention? https://www.catie.ca/en/pif/spring-2019/prep-use-among-gbmsm-what-does-it-mean-sti-prevention,author=Harrigan,Mallory,year=2019

  44. Punyacharoensin N, Edmunds WJ, De Angelis D, Delpech V, Hart G, Elford J, Brown A, Gill N, White RG (2015) Modelling the HIV epidemic among MSM in the United Kingdom: quantifying the contributions to HIV transmission to better inform prevention initiatives. Aids 29(3):339–349

    Google Scholar 

  45. Rambaut A, Robertson DL, Pybus OG, Peeters M, Holmes EC (2001) Phylogeny and the origin of HIV-1. Nature 410(6832):1047

    Google Scholar 

  46. Rana Jayoti, Wilton James, Fowler Shawn, Hart Trevor A, Bayoumi Ahmed M, and Tan Darrell HS (2018) Trends in the awareness, acceptability, and usage of HIV pre-exposure prophylaxis among at-risk men who have sex with men in Toronto. Can J Public Health, pp 1–11

  47. Rocheleau G, Franco-Villalobos C, Oliveira N, Brumme ZL, Rusch M, Shoveller J, Brumme CJ, Harrigan PR (2017) Sociodemographic correlates of HIV drug resistance and access to drug resistance testing in British Columbia, Canada. PLoS One 12(9):e0184848

    Google Scholar 

  48. Rodger AJ, Cambiano V, Bruun T, Vernazza P, Collins S, Degen O, Corbelli GM, Estrada V, Geretti AM, Beloukas A et al (2019) Risk of HIV transmission through condomless sex in serodifferent gay couples with the HIV-positive partner taking suppressive antiretroviral therapy (PARTNER): final results of a multicentre, prospective, observational study. Lancet 393(10189):2428–2438

    Google Scholar 

  49. Royce RA, Sena A, Cates W Jr, Cohen MS (1997) Sexual transmission of HIV. N Engl J Med 336(15):1072–1078

    Google Scholar 

  50. Sharomi O, Podder CN, Gumel AB, Elbasha EH, Watmough J (2007) Role of incidence function in vaccine-induced backward bifurcation in some hiv models. Math Biosci 210(2):436–463

    MathSciNet  MATH  Google Scholar 

  51. Sharomi O, Podder C, Gumel A, Gumel A, Song B (2008) Mathematical analysis of the transmission dynamics of HIV/TB coinfection in the presence of treatment. Math Biosci Eng 5(1):145

    MathSciNet  MATH  Google Scholar 

  52. Shuper PA, Joharchi N, Irving H, Fletcher D, Kovacs C, Loutfy M, Walmsley SL, Wong DKH, Rehm J (2016) Differential predictors of art adherence among HIV-monoinfected versus HIV/HCV-coinfected individuals. AIDS Care 28(8):954–962

    Google Scholar 

  53. Silva CJ, Torres DFM (2017) A SICA compartmental model in epidemiology with application to HIV/AIDS in Cape Verde. Ecol Complex 30:70–75

    Google Scholar 

  54. Singh AE, Gratrix J, Martin I, Friedman DS, Hoang L, Lester R, Metz G, Ogilvie G, Read R, Wong T (2015) Gonorrhea treatment failures with oral and injectable expanded spectrum Cephalosporin monotherapy versus dual therapy at 4 Canadian sexually transmitted infection clinics, 2010–2013. Sex Transm Dis 42(6):331–336

    Google Scholar 

  55. Smith M (1998) Social movements and equality seeking: the case of gay liberation in Canada. Can J Political Sci Rev 31(2):285–309

    MathSciNet  Google Scholar 

  56. Smith RJ, Blower SM (2004) Could disease-modifying HIV vaccines cause population-level perversity? Lancet Infect Dis 4(10):636–639

    Google Scholar 

  57. Spinner CD, Boesecke C, Zink A, Jessen H, Stellbrink H-J, Rockstroh JK, 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

    Google Scholar 

  58. Tan DHS, Hull MW, Yoong D, Tremblay C, O’byrne P et al, Thomas R, Kille J, Baril J-G, Cox J, Giguere P et al (2017) Canadian guideline on HIV pre-exposure prophylaxis and nonoccupational postexposure prophylaxis. Can Med Assoc J 189(47):E1448–E1458

  59. Tapsall J (2006) Antibiotic resistance in Neisseria Gonorrhoeae is diminishing available treatment options for Gonorrhea: some possible remedies. Expert Rev Anti-infect Ther 4(4):619–628

    Google Scholar 

  60. Tetteh RA, Yankey BA, Nartey ET, Lartey M, Leufkens HGM, Dodoo ANO (2017) Pre-exposure prophylaxis for HIV prevention: safety concerns. Drug Saf 40(4):273–283

    Google Scholar 

  61. Tomas K, Dhami P, Houston C, Ogunnaike-Cooke S, Rank C (2015) Good news on HIV: HIV in Canada: 2009–2014. Can Commun Dis Rep 41(12):292

    Google Scholar 

  62. Traeger MW, Schroeder SE, Wright EJ, Hellard ME, Cornelisse VJ, Doyle JS, Stoové MA (2018) Effects of pre-exposure prophylaxis for the prevention of human immunodeficiency virus infection on sexual risk behavior in men who have sex with men: a systematic review and meta-analysis. Clin Infect Dis 67(5):676–686

    Google Scholar 

  63. Tully S, Cojocaru M, Bauch CT (2015) Sexual behavior, risk perception, and HIV transmission can respond to HIV antiviral drugs and vaccines through multiple pathways. Sci Rep 5:15411

    Google Scholar 

  64. Tully S, Cojocaru M-G, Bauch CT (2017) Multiplayer games and HIV transmission via casual encounters. Math Biosci Eng 14(2):359–376

    MathSciNet  MATH  Google Scholar 

  65. Unemo Magnus, Golparian Daniel, Eyre David W (2019) Antimicrobial resistance in Neisseria Gonorrhoeae and treatment of Gonorrhea. Neisseria Gonorrhoeae. Springer, Berlin, pp 37–58

    Google Scholar 

  66. Van Laarhoven A, Hoornenborg E, Achterbergh R, De Vries H, Prins M, Van Der Loeff MS (2017) O09. 3 changes in sexual risk behaviour among daily PrEP users after 6 months of use in the Amsterdam prep project

  67. Weller SC (1993) A meta-analysis of condom effectiveness in reducing sexually transmitted HIV. Soc Sci Med 36(12):1635–1644

    Google Scholar 

  68. Williams BG, Lloyd-Smith JO, Gouws E, Hankins C, Getz WM, Hargrove J, De Zoysa I, Dye C, Auvert B (2006) The potential impact of male circumcision on HIV in sub-Saharan Africa. PLoS Med 3(7):e262

    Google Scholar 

  69. Workowski KA, Bolan GA, (2015) Sexually transmitted diseases treatment guidelines, (2015) MMWR. Recommendations and reports: morbidity and mortality weekly report. Recomm Rep 64(RR–03):1

  70. York A (2019) Undetectable equals untransmittable

  71. Zablotska I, Vaccher S, Bloch M et al. (2017) No hiv infections despite high-risk behaviour and sti incidence among gay/bisexual men taking daily pre-exposure prophylaxis (prep): the prelude demonstration project. In Program and abstracts of the 9th IAS Conference on HIV Science, Paris, France

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Pharaon, J., Bauch, C.T. The Impact of Pre-exposure Prophylaxis for Human Immunodeficiency Virus on Gonorrhea Prevalence. Bull Math Biol 82, 85 (2020). https://doi.org/10.1007/s11538-020-00762-7

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Keywords

  • Mathematical model
  • HIV
  • Gonorrhea
  • Prophylaxis
  • Infectious disease epidemiology
  • Compartmental model