Logo of straninfSexually Transmitted InfectionsVisit this articleSubmit a manuscriptReceive email alertsContact usBMJ
Sex Transm Infect. 1999 Feb; 75(1): 3–17.
PMCID: PMC1758168

From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection


OBJECTIVES: To review the scientific data on the role of sexually transmitted diseases (STDs) in sexual transmission of HIV infection and discuss the implications of these findings for HIV and STD prevention policy and practice. METHODS: Articles were selected from a review of Medline, accessed with the OVID search engine. The search covered articles from January 1987 to September 1998 and yielded 2101 articles. Methods used to uncover articles which might have been missed included searching for related articles by author, and combing literature reviews. In addition, all abstracts under the category "sexually transmitted diseases" from the XI and XII International Conferences on AIDS (Vancouver 1996 and Geneva 1998) and other relevant scientific meetings were reviewed. Efforts were made to locate journal articles which resulted from the research reported in the identified abstracts. All original journal articles and abstracts which met one of the following criteria were included: (1) studies of the biological plausibility or mechanism of facilitation of HIV infectiousness or susceptibility by STDs, (2) prospective cohort studies (longitudinal or nested case-control) which estimate the risk of HIV infection associated with specific STDs or STD syndromes, or (3) intervention studies which quantitate the effect which STD treatment can have on HIV incidence. RESULTS: Strong evidence indicates that both ulcerative and non-ulcerative STDs promote HIV transmission by augmenting HIV infectiousness and HIV susceptibility via a variety of biological mechanisms. These effects are reflected in the risk estimates found in numerous prospective studies from four continents which range from 2.0 to 23.5, with most clustering between 2 and 5. The relative importance of ulcerative and non-ulcerative STDs appears to be complex. Owing to the greater frequency of non-ulcerative STDs in many populations, these infections may be responsible for more HIV transmission than genital ulcers. However, the limited reciprocal impact of HIV infection on non-ulcerative STDs and the evidence that non-ulcerative STDs may increase risk primarily for the receptive partner (rather than bidirectionally) may modulate the impact of these diseases. The results of two community level randomised, controlled intervention trials conducted in Africa suggest that timely provision of STD services can substantially reduce HIV incidence, but raise additional questions about the optimal way to target and implement these services to achieve the greatest effect on HIV transmission. CONCLUSIONS: Available data leave little doubt that other STDs facilitate HIV transmission through direct, biological mechanisms and that early STD treatment should be part of a high quality, comprehensive HIV prevention strategy. Policy makers, HIV prevention programme managers, and providers should focus initial implementation efforts on three key areas: (i) improving access to and quality of STD clinical services; (ii) promoting early and effective STD related healthcare behaviours; and (iii) establishing surveillance systems to monitor STD and HIV trends and their interrelations.

Full Text

The Full Text of this article is available as a PDF (157K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Landry DJ, Forrest JD. Public health departments providing sexually transmitted disease services. Fam Plann Perspect. 1996 Nov-Dec;28(6):261–266. [PubMed]
  • Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis. 1992 Mar-Apr;19(2):61–77. [PubMed]
  • Clottey C, Dallabetta G. Sexually transmitted diseases and human immunodeficiency virus. Epidemiologic synergy? Infect Dis Clin North Am. 1993 Dec;7(4):753–770. [PubMed]
  • Kreiss JK, Coombs R, Plummer F, Holmes KK, Nikora B, Cameron W, Ngugi E, Ndinya Achola JO, Corey L. Isolation of human immunodeficiency virus from genital ulcers in Nairobi prostitutes. J Infect Dis. 1989 Sep;160(3):380–384. [PubMed]
  • Plummer FA, Wainberg MA, Plourde P, Jessamine P, D'Costa LJ, Wamola IA, Ronald AR. Detection of human immunodeficiency virus type 1 (HIV-1) in genital ulcer exudate of HIV-1-infected men by culture and gene amplification. J Infect Dis. 1990 Apr;161(4):810–811. [PubMed]
  • Ghys PD, Fransen K, Diallo MO, Ettiègne-Traoré V, Coulibaly IM, Yeboué KM, Kalish ML, Maurice C, Whitaker JP, Greenberg AE, et al. The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Côte d'Ivoire. AIDS. 1997 Oct;11(12):F85–F93. [PubMed]
  • Dyer JR, Eron JJ, Hoffman IF, Kazembe P, Vernazza PL, Nkata E, Costello Daly C, Fiscus SA, Cohen MS. Association of CD4 cell depletion and elevated blood and seminal plasma human immunodeficiency virus type 1 (HIV-1) RNA concentrations with genital ulcer disease in HIV-1-infected men in Malawi. J Infect Dis. 1998 Jan;177(1):224–227. [PubMed]
  • Schacker T, Ryncarz AJ, Goddard J, Diem K, Shaughnessy M, Corey L. Frequent recovery of HIV-1 from genital herpes simplex virus lesions in HIV-1-infected men. JAMA. 1998 Jul 1;280(1):61–66. [PubMed]
  • Mole L, Ripich S, Margolis D, Holodniy M. The impact of active herpes simplex virus infection on human immunodeficiency virus load. J Infect Dis. 1997 Sep;176(3):766–770. [PubMed]
  • Spinola SM, Orazi A, Arno JN, Fortney K, Kotylo P, Chen CY, Campagnari AA, Hood AF. Haemophilus ducreyi elicits a cutaneous infiltrate of CD4 cells during experimental human infection. J Infect Dis. 1996 Feb;173(2):394–402. [PubMed]
  • Stamm WE, Handsfield HH, Rompalo AM, Ashley RL, Roberts PL, Corey L. The association between genital ulcer disease and acquisition of HIV infection in homosexual men. JAMA. 1988 Sep 9;260(10):1429–1433. [PubMed]
  • Magro CM, Crowson AN, Alfa M, Nath A, Ronald A, Ndinya-Achola JO, Nasio J. A morphological study of penile chancroid lesions in human immunodeficiency virus (HIV)-positive and -negative African men with a hypothesis concerning the role of chancroid in HIV transmission. Hum Pathol. 1996 Oct;27(10):1066–1070. [PubMed]
  • Van Laer L, Vingerhoets J, Vanham G, Kestens L, Bwayo J, Otido J, Piot P, Roggen E. In vitro stimulation of peripheral blood mononuclear cells (PBMC) from HIV- and HIV+ chancroid patients by Haemophilus ducreyi antigens. Clin Exp Immunol. 1995 Nov;102(2):243–250. [PMC free article] [PubMed]
  • Heng MC, Heng SY, Allen SG. Co-infection and synergy of human immunodeficiency virus-1 and herpes simplex virus-1. Lancet. 1994 Jan 29;343(8892):255–258. [PubMed]
  • Pleskoff O, Tréboute C, Brelot A, Heveker N, Seman M, Alizon M. Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-1 entry. Science. 1997 Jun 20;276(5320):1874–1878. [PubMed]
  • Moss GB, Overbaugh J, Welch M, Reilly M, Bwayo J, Plummer FA, Ndinya-Achola JO, Malisa MA, Kreiss JK. Human immunodeficiency virus DNA in urethral secretions in men: association with gonococcal urethritis and CD4 cell depletion. J Infect Dis. 1995 Dec;172(6):1469–1474. [PubMed]
  • Anderson DJ, O'Brien TR, Politch JA, Martinez A, Seage GR, 3rd, Padian N, Horsburgh CR, Jr, Mayer KH. Effects of disease stage and zidovudine therapy on the detection of human immunodeficiency virus type 1 in semen. JAMA. 1992 May 27;267(20):2769–2774. [PubMed]
  • Atkins MC, Carlin EM, Emery VC, Griffiths PD, Boag F. Fluctuations of HIV load in semen of HIV positive patients with newly acquired sexually transmitted diseases. BMJ. 1996 Aug 10;313(7053):341–342. [PMC free article] [PubMed]
  • Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC, Zimba D, Vernazza PL, Maida M, Fiscus SA, et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet. 1997 Jun 28;349(9069):1868–1873. [PubMed]
  • Mostad SB, Overbaugh J, DeVange DM, Welch MJ, Chohan B, Mandaliya K, Nyange P, Martin HL, Jr, Ndinya-Achola J, Bwayo JJ, et al. Hormonal contraception, vitamin A deficiency, and other risk factors for shedding of HIV-1 infected cells from the cervix and vagina. Lancet. 1997 Sep 27;350(9082):922–927. [PubMed]
  • Clemetson DB, Moss GB, Willerford DM, Hensel M, Emonyi W, Holmes KK, Plummer F, Ndinya-Achola J, Roberts PL, Hillier S, et al. Detection of HIV DNA in cervical and vaginal secretions. Prevalence and correlates among women in Nairobi, Kenya. JAMA. 1993 Jun 9;269(22):2860–2864. [PubMed]
  • Kreiss J, Willerford DM, Hensel M, Emonyi W, Plummer F, Ndinya-Achola J, Roberts PL, Hoskyn J, Hillier S, Kiviat N. Association between cervical inflammation and cervical shedding of human immunodeficiency virus DNA. J Infect Dis. 1994 Dec;170(6):1597–1601. [PubMed]
  • John GC, Nduati RW, Mbori-Ngacha D, Overbaugh J, Welch M, Richardson BA, Ndinya-Achola J, Bwayo J, Krieger J, Onyango F, et al. Genital shedding of human immunodeficiency virus type 1 DNA during pregnancy: association with immunosuppression, abnormal cervical or vaginal discharge, and severe vitamin A deficiency. J Infect Dis. 1997 Jan;175(1):57–62. [PMC free article] [PubMed]
  • Levine WC, Pope V, Bhoomkar A, Tambe P, Lewis JS, Zaidi AA, Farshy CE, Mitchell S, Talkington DF. Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. J Infect Dis. 1998 Jan;177(1):167–174. [PubMed]
  • Ho JL, He S, Hu A, Geng J, Basile FG, Almeida MG, Saito AY, Laurence J, Johnson WD., Jr Neutrophils from human immunodeficiency virus (HIV)-seronegative donors induce HIV replication from HIV-infected patients' mononuclear cells and cell lines: an in vitro model of HIV transmission facilitated by Chlamydia trachomatis. J Exp Med. 1995 Apr 1;181(4):1493–1505. [PMC free article] [PubMed]
  • Dallabetta GA, Miotti PG, Chiphangwi JD, Liomba G, Canner JK, Saah AJ. Traditional vaginal agents: use and association with HIV infection in Malawian women. AIDS. 1995 Mar;9(3):293–297. [PubMed]
  • 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 Sep-Oct;23(5):429–440. [PubMed]
  • Cameron DW, Simonsen JN, D'Costa LJ, Ronald AR, Maitha GM, Gakinya MN, Cheang M, Ndinya-Achola JO, Piot P, Brunham RC, et al. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet. 1989 Aug 19;2(8660):403–407. [PubMed]
  • Mbizvo MT, Machekano R, McFarland W, Ray S, Bassett M, Latif A, Katzenstein D. HIV seroincidence and correlates of seroconversion in a cohort of male factory workers in Harare, Zimbabwe. AIDS. 1996 Jul;10(8):895–901. [PubMed]
  • Nopkesorn T, Mock PA, Mastro TD, Sangkharomya S, Sweat M, Limpakarnjanarat K, Laosakkitiboran J, Young NL, Morse SA, Schmid S, et al. HIV-1 subtype E incidence and sexually transmitted diseases in a cohort of military conscripts in northern Thailand. J Acquir Immune Defic Syndr Hum Retrovirol. 1998 Aug 1;18(4):372–379. [PubMed]
  • Nelson KE, Eiumtrakul S, Celentano D, Maclean I, Ronald A, Suprasert S, Hoover DR, Kuntolbutra S, Zenilman JM. The association of herpes simplex virus type 2 (HSV-2), Haemophilus ducreyi, and syphilis with HIV infection in young men in northern Thailand. J Acquir Immune Defic Syndr Hum Retrovirol. 1997 Dec 1;16(4):293–300. [PubMed]
  • Telzak EE, Chiasson MA, Bevier PJ, Stoneburner RL, Castro KG, Jaffe HW. HIV-1 seroconversion in patients with and without genital ulcer disease. A prospective study. Ann Intern Med. 1993 Dec 15;119(12):1181–1186. [PubMed]
  • Plummer FA, Simonsen JN, Cameron DW, Ndinya-Achola JO, Kreiss JK, Gakinya MN, Waiyaki P, Cheang M, Piot P, Ronald AR, et al. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J Infect Dis. 1991 Feb;163(2):233–239. [PubMed]
  • de Vincenzi I. A longitudinal study of human immunodeficiency virus transmission by heterosexual partners. European Study Group on Heterosexual Transmission of HIV. N Engl J Med. 1994 Aug 11;331(6):341–346. [PubMed]
  • Kassler WJ, Zenilman JM, Erickson B, Fox R, Peterman TA, Hook EW., 3rd Seroconversion in patients attending sexually transmitted disease clinics. AIDS. 1994 Mar;8(3):351–355. [PubMed]
  • Mehendale SM, Rodrigues JJ, Brookmeyer RS, Gangakhedkar RR, Divekar AD, Gokhale MR, Risbud AR, Paranjape RS, Shepherd ME, Rompalo AE, et al. Incidence and predictors of human immunodeficiency virus type 1 seroconversion in patients attending sexually transmitted disease clinics in India. J Infect Dis. 1995 Dec;172(6):1486–1491. [PubMed]
  • Holmberg SD, Stewart JA, Gerber AR, Byers RH, Lee FK, O'Malley PM, Nahmias AJ. Prior herpes simplex virus type 2 infection as a risk factor for HIV infection. JAMA. 1988 Feb 19;259(7):1048–1050. [PubMed]
  • Keet IP, Lee FK, van Griensven GJ, Lange JM, Nahmias A, Coutinho RA. Herpes simplex virus type 2 and other genital ulcerative infections as a risk factor for HIV-1 acquisition. Genitourin Med. 1990 Oct;66(5):330–333. [PMC free article] [PubMed]
  • Kingsley LA, Armstrong J, Rahman A, Ho M, Rinaldo CR., Jr No association between herpes simplex virus type-2 seropositivity or anogenital lesions and HIV seroconversion among homosexual men. J Acquir Immune Defic Syndr. 1990;3(8):773–779. [PubMed]
  • Kuiken CL, van Griensven GJ, de Vroome EM, Coutinho RA. Risk factors and changes in sexual behavior in male homosexuals who seroconverted for human immunodeficiency virus antibodies. Am J Epidemiol. 1990 Sep;132(3):523–530. [PubMed]
  • Craib KJ, Meddings DR, Strathdee SA, Hogg RS, Montaner JS, O'Shaughnessy MV, Schechter MT. Rectal gonorrhoea as an independent risk factor for HIV infection in a cohort of homosexual men. Genitourin Med. 1995 Jun;71(3):150–154. [PMC free article] [PubMed]
  • Darrow WW, Echenberg DF, Jaffe HW, O'Malley PM, Byers RH, Getchell JP, Curran JW. Risk factors for human immunodeficiency virus (HIV) infections in homosexual men. Am J Public Health. 1987 Apr;77(4):479–483. [PMC free article] [PubMed]
  • Otten MW, Jr, Zaidi AA, Peterman TA, Rolfs RT, Witte JJ. High rate of HIV seroconversion among patients attending urban sexually transmitted disease clinics. AIDS. 1994 Apr;8(4):549–553. [PubMed]
  • Plourde PJ, Pepin J, Agoki E, Ronald AR, Ombette J, Tyndall M, Cheang M, Ndinya-Achola JO, D'Costa LJ, Plummer FA. Human immunodeficiency virus type 1 seroconversion in women with genital ulcers. J Infect Dis. 1994 Aug;170(2):313–317. [PubMed]
  • Laga M, Manoka A, Kivuvu M, Malele B, Tuliza M, Nzila N, Goeman J, Behets F, Batter V, Alary M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS. 1993 Jan;7(1):95–102. [PubMed]
  • Kapiga SH, Lyamuya EF, Lwihula GK, Hunter DJ. The incidence of HIV infection among women using family planning methods in Dar es Salaam, Tanzania. AIDS. 1998 Jan 1;12(1):75–84. [PubMed]
  • Taha TE, Hoover DR, Dallabetta GA, Kumwenda NI, Mtimavalye LA, Yang LP, Liomba GN, Broadhead RL, Chiphangwi JD, Miotti PG. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998 Sep 10;12(13):1699–1706. [PubMed]
  • Weir SS, Feldblum PJ, Roddy RE, Zekeng L. Gonorrhea as a risk factor for HIV acquisition. AIDS. 1994 Nov;8(11):1605–1608. [PubMed]
  • Sewankambo N, Gray RH, Wawer MJ, Paxton L, McNaim D, Wabwire-Mangen F, Serwadda D, Li C, Kiwanuka N, Hillier SL, et al. HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet. 1997 Aug 23;350(9077):546–550. [PubMed]
  • Miettinen OS. Proportion of disease caused or prevented by a given exposure, trait or intervention. Am J Epidemiol. 1974 May;99(5):325–332. [PubMed]
  • Vittinghoff E, Padian NS. Attributable risk of exposures associated with sexually transmitted disease. J Infect Dis. 1996 Oct;174 (Suppl 2):S182–S187. [PubMed]
  • Boily MC, Anderson RM. Human immunodeficiency virus transmission and the role of other sexually transmitted diseases. Measures of association and study design. Sex Transm Dis. 1996 Jul-Aug;23(4):312–332. [PubMed]
  • May RM, Anderson RM. Transmission dynamics of HIV infection. Nature. 1987 Mar 12;326(6109):137–142. [PubMed]
  • Boily MC, Brunham RC. The impact of HIV and other STDs on human populations. Are predictions possible? Infect Dis Clin North Am. 1993 Dec;7(4):771–792. [PubMed]
  • Robinson NJ, Mulder DW, Auvert B, Hayes RJ. Proportion of HIV infections attributable to other sexually transmitted diseases in a rural Ugandan population: simulation model estimates. Int J Epidemiol. 1997 Feb;26(1):180–189. [PubMed]
  • Garnett GP, Anderson RM. Strategies for limiting the spread of HIV in developing countries: conclusions based on studies of the transmission dynamics of the virus. J Acquir Immune Defic Syndr Hum Retrovirol. 1995 Aug 15;9(5):500–513. [PubMed]
  • Mertens TE, Hayes RJ, Smith PG. Epidemiological methods to study the interaction between HIV infection and other sexually transmitted diseases. AIDS. 1990 Jan;4(1):57–65. [PubMed]
  • Hayes R, Wawer M, Gray R, Whitworth J, Grosskurth H, Mabey D. Randomised trials of STD treatment for HIV prevention: report of an international workshop. HIV/STD Trials Workshop Group. Genitourin Med. 1997 Dec;73(6):432–443. [PMC free article] [PubMed]
  • Nkowane BM, Lwanga SK. HIV and design of intervention studies for control of sexually transmitted diseases. AIDS. 1990;4 (Suppl 1):S123–S126. [PubMed]
  • Laga M, Alary M, Nzila N, Manoka AT, Tuliza M, Behets F, Goeman J, St Louis M, Piot P. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers. Lancet. 1994 Jul 23;344(8917):246–248. [PubMed]
  • Levine WC, Revollo R, Kaune V, Vega J, Tinajeros F, Garnica M, Estenssoro M, Lewis JS, Higueras G, Zurita R, et al. Decline in sexually transmitted disease prevalence in female Bolivian sex workers: impact of an HIV prevention project. AIDS. 1998 Oct 1;12(14):1899–1906. [PubMed]
  • Grosskurth H, Mosha F, Todd J, Mwijarubi E, Klokke A, Senkoro K, Mayaud P, Changalucha J, Nicoll A, ka-Gina G, et al. Impact of improved treatment of sexually transmitted diseases on HIV infection in rural Tanzania: randomised controlled trial. Lancet. 1995 Aug 26;346(8974):530–536. [PubMed]
  • Mayaud P, Mosha F, Todd J, Balira R, Mgara J, West B, Rusizoka M, Mwijarubi E, Gabone R, Gavyole A, et al. Improved treatment services significantly reduce the prevalence of sexually transmitted diseases in rural Tanzania: results of a randomized controlled trial. AIDS. 1997 Dec;11(15):1873–1880. [PubMed]
  • Gilson L, Mkanje R, Grosskurth H, Mosha F, Picard J, Gavyole A, Todd J, Mayaud P, Swai R, Fransen L, et al. Cost-effectiveness of improved treatment services for sexually transmitted diseases in preventing HIV-1 infection in Mwanza Region, Tanzania. Lancet. 1997 Dec 20;350(9094):1805–1809. [PubMed]
  • Cohen MS. Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet. 1998;351 (Suppl 3):5–7. [PubMed]
  • Dallabetta GA, Gerbase AC, Holmes KK. Problems, solutions, and challenges in syndromic management of sexually transmitted diseases. Sex Transm Infect. 1998 Jun;74 (Suppl 1):S1–11. [PubMed]

Articles from Sexually Transmitted Infections are provided here courtesy of BMJ Group


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • Cited in Books
    Cited in Books
    PubMed Central articles cited in books
  • MedGen
    Related information in MedGen
  • PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...