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RESEARCH ARTICLE

Could implementation of Australia’s National Gay Men’s Syphilis Action Plan have an indirect effect on the HIV epidemic?

Alexander Hoare A , Richard T. Gray A and David P. Wilson A B
+ Author Affiliations
- Author Affiliations

A National Centre in HIV Epidemiology and Clinical Research, The University of New South Wales, Sydney, NSW 2010, Australia.

B Corresponding author. Email: dwilson@nchecr.unsw.edu.au

Sexual Health 9(2) 144-151 https://doi.org/10.1071/SH10145
Submitted: 21 November 2010  Accepted: 19 May 2011   Published: 24 August 2011

Abstract

Objectives: The number of incident infections of syphilis and HIV have increased over the past decade across Australia, particularly among gay men. In other industrialised settings, syphilis epidemics have also resurged coincidentally with increases in HIV diagnoses. Sexually transmissible infections (STI) are a biologically plausible cofactor for increasing HIV transmission. We pose the question: could strategies purely targeting syphilis also have an indirect impact on HIV incidence? Methods: We developed an agent-based computer model that simulates the transmission and disease progression of HIV and syphilis among a population of sexually active gay men, calibrated to reflect the epidemics in Victoria, Australia. The model was informed by detailed behavioural data from a variety of sources and was used to investigate the potential epidemiological impact of different public health interventions. Results: Assuming that syphilis could act as a biological cofactor for HIV transmission, from no effect to increasing risk by five-fold, our model indicates that if Australia’s syphilis action plan is effectively implemented then the number of HIV infections could decrease by up to 48% over the next decade in the absence of any specific HIV interventions. Conclusion: It is plausible that effective implementation of interventions targeting syphilis epidemics can have an indirect effect of mitigating the spread of HIV. The possible effects of STI should be considered in the design, implementation and evaluation of public health strategies and programs.

Additional keywords: HIV, mathematical model, men who have sex with men, syphilis.


References

[1]  Branger J, van der Meer JTM, 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 |

[2]  Chen SY, Gibson S, Katz MH, Klausner JD, Dilley JW, Schwarcz SK, et al Continuing increases in sexual risk behavior and sexually transmitted diseases among men who have sex with men: San Francisco, California, 1999–2001, USA. Am J Public Health 2002; 92 1387–8.
Continuing increases in sexual risk behavior and sexually transmitted diseases among men who have sex with men: San Francisco, California, 1999–2001, USA.Crossref | GoogleScholarGoogle Scholar | 12197957PubMed |

[3]  Fenton KA, Imrie J. Increasing rates of sexually transmitted diseases in homosexual men in Western Europe and the United States: why? Infect Dis Clin North Am 2005; 19 311–31.
Increasing rates of sexually transmitted diseases in homosexual men in Western Europe and the United States: why?Crossref | GoogleScholarGoogle Scholar | 15963874PubMed |

[4]  Lee DM, Chen MY. The re-emergence of syphilis among homosexually active men in Melbourne. Aust N Z J Public Health 2005; 29 390–1.
The re-emergence of syphilis among homosexually active men in Melbourne.Crossref | GoogleScholarGoogle Scholar | 16222942PubMed |

[5]  National Centre in HIV Epidemiology and Clinical Research (NCHECR). HIV/AIDS, viral hepatitis and sexually transmissible infections in Australia Annual Surveillance Report 2009. Sydney: NCHECR; 2009.

[6]  Fisher M, Pao D, Murphy G, Dean G, McElborough D, Homer G, et al Serological testing algorithm shows rising HIV incidence in a UK cohort of men who have sex with men: 10 years application. AIDS 2007; 21 2309–14.
Serological testing algorithm shows rising HIV incidence in a UK cohort of men who have sex with men: 10 years application.Crossref | GoogleScholarGoogle Scholar | 18090279PubMed |

[7]  Grulich AE, Kaldor J. Trends in HIV incidence in homosexual men in developed countries. Sex Health 2008; 5 113–18.
Trends in HIV incidence in homosexual men in developed countries.Crossref | GoogleScholarGoogle Scholar | 18588775PubMed |

[8]  Zablotska I, Prestage G, Hull P, Crawford J, Kippax S, Sutherland, et al. Sydney Gay Periodic Survey February 1996 to February 2006. Sydney: National Centre in HIV Social Research, University of New South Wales; 2006.

[9]  Lee E, Holt M, Zablotska I, Prestage G, Staunton S, Scott K, et al. Gay Community Periodic Survey Queensland 2009. Sydney: National Centre in HIV Social Research, University of New South Wales; 2010.

[10]  Frankland A, Lee E, Zablotska I, Prestage G, Down I, Holt M, et al. Gay Community Periodic Survey: Sydney, February 2009. Sydney: National Centre in HIV Social Research, University of New South Wales; 2009

[11]  Zablotska I, Prestage G, Batrouney C, Kennedy M, Clift P, Dixon M, et al. Gay Community Periodic Survey: Melbourne 2009. Sydney: National Centre in HIV Social Research, University of New South Wales; 2009.

[12]  Bautista CT, Sanchez JL, Montano SM, Laguna-Torres VA, Lama JR, Sanchez JL, 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=15eef5659a162b7a7704089805f67ff6CAS | 15572623PubMed |

[13]  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 3–17.
From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MznslCntg%3D%3D&md5=8966cdb09ad76e2c41e281d5b0f31535CAS | 10448335PubMed |

[14]  Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2004; 2 33–42.
The role of sexually transmitted diseases in HIV transmission.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1KrsL8%3D&md5=e2cab824e73330eecb989e7fb82728aaCAS | 15035007PubMed |

[15]  Piot P, Laga M. Genital ulcers, other sexually transmitted diseases, and the sexual transmission of HIV. BMJ 1989; 298 623–4.
Genital ulcers, other sexually transmitted diseases, and the sexual transmission of HIV.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M3ivFGntg%3D%3D&md5=9faf5dad817a308da57c346082265112CAS | 2496785PubMed |

[16]  Read TRH, Hocking J, Sinnott V, Hellard M. Risk factors for incident HIV infection in men having sex with men: a case–control study. Sex Health 2007; 4 35–9.
Risk factors for incident HIV infection in men having sex with men: a case–control study.Crossref | GoogleScholarGoogle Scholar |

[17]  Rottingen JA, Cameron DW, Garnett GP. A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known? Sex Transm Dis 2001; 28 579–97.
A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnjsFejsQ%3D%3D&md5=4c3c628fbb1df84c2665867f447123e6CAS | 11689757PubMed |

[18]  Simonsen JN, Cameron DW, Gaykinya MN, Ndinya-Achola JO, D’Costa LJ, Karasira P, et al Human immunodeficiency virus infection among men with sexually transmitted diseases. Experience from a center in Africa. N Engl J Med 1988; 319 274–8.
Human immunodeficiency virus infection among men with sexually transmitted diseases. Experience from a center in Africa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3ns1Slsg%3D%3D&md5=4c4d66aa63697bed78776ff3ca2d4c06CAS | 3393182PubMed |

[19]  Dickerson MC, Johnston J, Delea TE, White A, Andrews E. The causal role for genital ulcer disease as a risk factor for transmission of human immunodeficiency virus. An application of the Bradford Hill criteria. Sex Transm Dis 1996; 23 429–40.
The causal role for genital ulcer disease as a risk factor for transmission of human immunodeficiency virus. An application of the Bradford Hill criteria.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FjvFGhtw%3D%3D&md5=184993b89ade6c3163ba133b9a5074deCAS | 8885077PubMed |

[20]  Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19 61–77.
Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383nvFymsA%3D%3D&md5=6abee7240d367d4ae28674b62b705ff6CAS | 1595015PubMed |

[21]  Holmberg SD, Stewart JA, Gerber AR, Byers RH, Lee FK, O’Malley PM, et al Prior herpes simplex virus type 2 infection as a risk factor for HIV infection. JAMA 1988; 259 1048–50.
Prior herpes simplex virus type 2 infection as a risk factor for HIV infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvFekug%3D%3D&md5=773e70babd23d095bae1109aeec554b6CAS | 2828700PubMed |

[22]  Plummer FA, Simonsen JN, Cameron DW, Ndinya-Achola JO, Kreiss JK, Gakinya MN, et al Cofactors in male–female sexual transmission of human immunodeficiency virus type 1. J Infect Dis 1991; 163 233–9.
Cofactors in male–female sexual transmission of human immunodeficiency virus type 1.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7gvVWntw%3D%3D&md5=30b1cc3ae6af3e14282cc34758e04b9cCAS | 1988508PubMed |

[23]  Sellati TJ, Wilkinson DA, Sheffield JS, Koup RA, Radolf JD, Norgard MV. Virulent Treponema pallidum, lipoprotein, and synthetic lipopeptides induce CCR5 on human monocytes and enhance their susceptibility to infection by human immunodeficiency virus type 1. J Infect Dis 2000; 181 283–93.
Virulent Treponema pallidum, lipoprotein, and synthetic lipopeptides induce CCR5 on human monocytes and enhance their susceptibility to infection by human immunodeficiency virus type 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslagsQ%3D%3D&md5=f60b51a9422474fabfc7ab42a921015dCAS | 10608777PubMed |

[24]  Kamali A, Quigley M, Nakiyingi J, Kinsman J, Kengeya-Kayondo J, Gopal R, et al Syndromic management of sexually-transmitted infections and behaviour change interventions on transmission of HIV-1 in rural Uganda: a community randomised trial. Lancet 2003; 361 645–52.
Syndromic management of sexually-transmitted infections and behaviour change interventions on transmission of HIV-1 in rural Uganda: a community randomised trial.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FpsFSrtw%3D%3D&md5=57801d0429a9e8e93708b75ec063e1f5CAS | 12606175PubMed |

[25]  Kaul R, Kimani J, Nagelkerke NJ, Fonck K, Ngugi EN, Keli F, et al Monthly antibiotic chemoprophylaxis and incidence of sexually transmitted infections and HIV-1 infection in Kenyan sex workers: a randomized controlled trial. JAMA 2004; 291 2555–62.
Monthly antibiotic chemoprophylaxis and incidence of sexually transmitted infections and HIV-1 infection in Kenyan sex workers: a randomized controlled trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkslWgtro%3D&md5=ae3faada5042df8871c943e126a66527CAS | 15173146PubMed |

[26]  Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Paxton L, Berkley S, et al A randomized, community trial of intensive sexually transmitted disease control for AIDS prevention, Rakai, Uganda. AIDS 1998; 12 1211–25.
A randomized, community trial of intensive sexually transmitted disease control for AIDS prevention, Rakai, Uganda.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czjvFyhtw%3D%3D&md5=3f4d9eacbf9096407e986d5f5193e0c8CAS | 9677171PubMed |

[27]  Wawer MJ, Sewankambo NK, Serwadda D, Quinn TC, Paxton LA, Kiwanuka N, et al Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial. Rakai Project Study Group. Lancet 1999; 353 525–35.
Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial. Rakai Project Study Group.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7ltFCgug%3D%3D&md5=8dd7b930bb91142003e99b7f9eefc91bCAS | 10028980PubMed |

[28]  Gray RT, Wilson DP. Acyclovir and transmission of HIV-1 from persons infected with HIV-1 and HSV-2. N Engl J Med 2010; 362 1740–42.
Acyclovir and transmission of HIV-1 from persons infected with HIV-1 and HSV-2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXls1ylsL0%3D&md5=5c4d2c5010605023d6317f789e0096d7CAS |

[29]  Wilson DP. Interpreting sexually transmissible infection prevention trials by adjusting for the magnitude of exposure. Clin Trials 2010; 7 36–43.
Interpreting sexually transmissible infection prevention trials by adjusting for the magnitude of exposure.Crossref | GoogleScholarGoogle Scholar | 20007407PubMed |

[30]  Wilson DP, Prestage G, Donovan B, Gray RT, Hoare A, McCann PD, et al. Phase A of the National Gay Men’s Syphilis Action Plan: modelling evidence and research on acceptability of interventions for controlling syphilis in Australia. Sydney: National Centre in HIV Epidemiology and Clinical Research; 2009.

[31]  Gray RT, Hoare A, Prestage G, Donovan B, Kaldor JK, Wilson DP, et al Frequent testing of highly sexually active gay men is required to control syphilis. Sex Transm Dis 2010; 37 298–305.
| 20393383PubMed |

[32]  Prestage G, Ferris J, Grierson J, Thorpe R, Zablotska I, Imrie J, et al Homosexual men in Australia: population, distribution and HIV prevalence. Sex Health 2008; 5 97–102.
Homosexual men in Australia: population, distribution and HIV prevalence.Crossref | GoogleScholarGoogle Scholar | 18588772PubMed |

[33]  Fogarty A, Mao L, Zablotska I, Salter M, Prestage G, Rule J, et al. The Health in Men and Positive Health cohorts: a comparison of trends in the health and sexual behaviour of HIV-negative and HIV-positive gay men, 2002–2005. Sydney: National Centre in HIV Social Research; 2006.

[34]  Prestage G, Hudson J, Bradley J, Down I, Sutherland R, Corrigan N, et al. TOMS: Three or More Study. Sydney: National Centre in HIV Epidemiology and Clinical Research; 2008.

[35]  Garnett GP, Aral SO, Hoyle DV, Cates W. Garnett GP, Aral SO, Hoyle DV, Cates W. The natural history of syphilis. Implications for the transmission dynamics and control of infection. Sex Transm Dis 1997; 24 185–200.
The natural history of syphilis. Implications for the transmission dynamics and control of infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3ls1aqug%3D%3D&md5=5cc706242de1cf010e2a909062d990daCAS | 9101629PubMed |

[36]  White RG, Orroth KK, Korenromp EL, Bakker R, Wambura M, Sewankambo NK, et al Can population differences explain the contrasting results of the Mwanza, Rakai, and Masaka HIV/sexually transmitted disease intervention trials? A modeling study. J Acquir Immune Defic Syndr 2004; 37 1500–13.
Can population differences explain the contrasting results of the Mwanza, Rakai, and Masaka HIV/sexually transmitted disease intervention trials? A modeling study.Crossref | GoogleScholarGoogle Scholar | 15602129PubMed |

[37]  Fitch TJ, Stine C, Hager WD, Mann J, Adam MB, Mcilhaney J. Condom effectiveness: factors that influence risk reduction. Sex Transm Dis 2002; 29 811–7.
Condom effectiveness: factors that influence risk reduction.Crossref | GoogleScholarGoogle Scholar |

[38]  Tramont EC. Treponema pallidum. In: Mandell GL, Bennett JE, Dolm R, editors. Principles and practice of infectious disease, 4th edn . New York: Churchill Livingstone; 1995. pp. 2117–2132.

[39]  Schrijvers D, Josse R, Trebucq A, Dupont A, Cheringou H, Larouze B. Transmission of syphilis between sexual partners in Gabon. Genitourin Med 1989; 65 84–5.
Transmission of syphilis between sexual partners in Gabon.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1Mzis1Clug%3D%3D&md5=1873468012a51503ca1eccd784d043a7CAS | 2753517PubMed |

[40]  Clark EG, Danbolt N. The Oslo study of the natural course of untreated syphilis. An epidemiologic investigation based on a re-study of the Boeck-Bruusgaard material. Med Clin North Am 1964; 48 613–23.

[41]  Brunham RC, Plummer FA. A general model of sexually transmitted disease epidemiology and its implications for control. Med Clin North Am 1990; 74 1339–52.
| 1:STN:280:DyaK3M%2FmtFGhtg%3D%3D&md5=8634ebfcb3efe5870dee5c3a468ef134CAS | 2246943PubMed |

[42]  Lossick JG, Kraus SJ. Syphilis. In: Evans AS, editor. Bacterial infections of humans: epidemiology and control. New York: Plenum; 1991. pp. 675–695.

[43]  Moore MB, Price EV, Knox JM, Elgin LW. Epidemiologic treatment of contacts to infectious syphilis. Public Health Rep 1963; 78 966–70.
Epidemiologic treatment of contacts to infectious syphilis.Crossref | GoogleScholarGoogle Scholar | 14084872PubMed |

[44]  Pourbohloul B, Rekart ML, Brunham RC. Impact of mass treatment on syphilis transmission: a mathematical modeling approach. Sex Transm Dis 2003; 30 297–305.
Impact of mass treatment on syphilis transmission: a mathematical modeling approach.Crossref | GoogleScholarGoogle Scholar | 12671548PubMed |

[45]  Rottingen JA, Garnett GP. The epidemiological and control implications of HIV transmission probabilities within partnerships. Sex Transm Dis 2002; 29 818–27.
The epidemiological and control implications of HIV transmission probabilities within partnerships.Crossref | GoogleScholarGoogle Scholar | 12466726PubMed |

[46]  Schober PC, Gabriel G, White P, Felton WF, Thin R. How infectious is syphilis? Br J Vener Dis 1983; 59 217–9.
| 1:STN:280:DyaL3s3lvVClsg%3D%3D&md5=edc922684abbc101907aab6589e5b25aCAS | 6871650PubMed |

[47]  Schroeter AL, Turner RH, Lucas JB, Brown WJ. Therapy for incubation syphilis. JAMA 1971; 218 711–3.
Therapy for incubation syphilis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE38%2FmtlGltQ%3D%3D&md5=c399e4dd132d92a7aa2efce303c48acaCAS | 5171497PubMed |

[48]  Stamm LV. Biology of Treponema pallidum. In: Holmes KK, Sparling PR, Mardh P-A, editors. Sexually transmitted diseases, 3rd edn. New York: McGraw-Hill; 1998. pp. 467–472.

[49]  Jin F, Prestage GP, Kippax SC, Pell CM, Donovan BJ, Kaldor JM, et al Epidemic syphilis among homosexually active men in Sydney. Med J Aust 2005; 183 179–83.
| 16097913PubMed |

[50]  Mao L, Crawford J, Hospers H, Prestage G, Grulich A, Kaldor J, et al “Serosorting” in casual anal sex of HIV-negative gay men is noteworthy and is increasing in Sydney, Australia. AIDS 2006; 20 1204–6.
“Serosorting” in casual anal sex of HIV-negative gay men is noteworthy and is increasing in Sydney, Australia.Crossref | GoogleScholarGoogle Scholar | 16691075PubMed |

[51]  Prestage GP, Hudson J, Down I, Bradley J, Corrigan N, Hurley M, et al Gay men who engage in group sex are at increased risk of HIV infection and onward transmission. AIDS Behavior 2009; 13 724–30.
Gay men who engage in group sex are at increased risk of HIV infection and onward transmission.Crossref | GoogleScholarGoogle Scholar |

[52]  Martin IE, Lau A, Sawatzky P, Tsang RS, Cuff W, Lee C, et al Serological diagnosis of syphilis: enzyme-linked immunosorbent assay to measure antibodies to individual recombinant Treponema pallidum antigens. J Immunoassay Immunochem 2008; 29 143–51.
Serological diagnosis of syphilis: enzyme-linked immunosorbent assay to measure antibodies to individual recombinant Treponema pallidum antigens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFCltbk%3D&md5=afedf1ad7b9d5cf7cc9aa02aa2e70d05CAS | 18360809PubMed |

[53]  Nessa K, Alam A, Arif Hasan Chawdhury F, Huq M, Nahar S, Salauddin G, et al Field evaluation of simple rapid tests in the diagnosis of syphilis. Int J STD AIDS 2008; 19 316–20.
Field evaluation of simple rapid tests in the diagnosis of syphilis.Crossref | GoogleScholarGoogle Scholar | 18482961PubMed |