Abstract
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.
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- Anderson D. J., O'Brien T. R., Politch J. A., Martinez A., Seage G. R., 3rd, Padian N., Horsburgh C. R., Jr, Mayer K. H. 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] [Google Scholar]
- Atkins M. C., Carlin E. M., Emery V. C., Griffiths P. D., 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. doi: 10.1136/bmj.313.7053.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boily M. C., Anderson R. M. 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. doi: 10.1097/00007435-199607000-00012. [DOI] [PubMed] [Google Scholar]
- Boily M. C., Brunham R. C. 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] [Google Scholar]
- Cameron D. W., Simonsen J. N., D'Costa L. J., Ronald A. R., Maitha G. M., Gakinya M. N., Cheang M., Ndinya-Achola J. O., Piot P., Brunham R. C. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet. 1989 Aug 19;2(8660):403–407. doi: 10.1016/s0140-6736(89)90589-8. [DOI] [PubMed] [Google Scholar]
- Clemetson D. B., Moss G. B., Willerford D. M., Hensel M., Emonyi W., Holmes K. K., Plummer F., Ndinya-Achola J., Roberts P. L., Hillier S. 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] [Google Scholar]
- 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] [Google Scholar]
- Cohen M. S., Hoffman I. F., Royce R. A., Kazembe P., Dyer J. R., Daly C. C., Zimba D., Vernazza P. L., Maida M., Fiscus S. A. 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. doi: 10.1016/s0140-6736(97)02190-9. [DOI] [PubMed] [Google Scholar]
- Cohen M. S. Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet. 1998;351 (Suppl 3):5–7. doi: 10.1016/s0140-6736(98)90002-2. [DOI] [PubMed] [Google Scholar]
- Craib K. J., Meddings D. R., Strathdee S. A., Hogg R. S., Montaner J. S., O'Shaughnessy M. V., Schechter M. T. Rectal gonorrhoea as an independent risk factor for HIV infection in a cohort of homosexual men. Genitourin Med. 1995 Jun;71(3):150–154. doi: 10.1136/sti.71.3.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dallabetta G. A., Gerbase A. C., Holmes K. K. Problems, solutions, and challenges in syndromic management of sexually transmitted diseases. Sex Transm Infect. 1998 Jun;74 (Suppl 1):S1–11. [PubMed] [Google Scholar]
- Dallabetta G. A., Miotti P. G., Chiphangwi J. D., Liomba G., Canner J. K., Saah A. J. Traditional vaginal agents: use and association with HIV infection in Malawian women. AIDS. 1995 Mar;9(3):293–297. [PubMed] [Google Scholar]
- Darrow W. W., Echenberg D. F., Jaffe H. W., O'Malley P. M., Byers R. H., Getchell J. P., Curran J. W. Risk factors for human immunodeficiency virus (HIV) infections in homosexual men. Am J Public Health. 1987 Apr;77(4):479–483. doi: 10.2105/ajph.77.4.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dickerson M. C., Johnston J., Delea T. E., 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. doi: 10.1097/00007435-199609000-00015. [DOI] [PubMed] [Google Scholar]
- Dyer J. R., Eron J. J., Hoffman I. F., Kazembe P., Vernazza P. L., Nkata E., Costello Daly C., Fiscus S. A., Cohen M. S. 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. doi: 10.1086/517359. [DOI] [PubMed] [Google Scholar]
- Garnett G. P., Anderson R. M. 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] [Google Scholar]
- Ghys P. D., Fransen K., Diallo M. O., Ettiègne-Traoré V., Coulibaly I. M., Yeboué K. M., Kalish M. L., Maurice C., Whitaker J. P., Greenberg A. E. 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. doi: 10.1097/00002030-199712000-00001. [DOI] [PubMed] [Google Scholar]
- Gilson L., Mkanje R., Grosskurth H., Mosha F., Picard J., Gavyole A., Todd J., Mayaud P., Swai R., Fransen L. 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. doi: 10.1016/S0140-6736(97)08222-6. [DOI] [PubMed] [Google Scholar]
- Grosskurth H., Mosha F., Todd J., Mwijarubi E., Klokke A., Senkoro K., Mayaud P., Changalucha J., Nicoll A., ka-Gina G. 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. doi: 10.1016/s0140-6736(95)91380-7. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1136/sti.73.6.432. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heng M. C., Heng S. Y., Allen S. G. Co-infection and synergy of human immunodeficiency virus-1 and herpes simplex virus-1. Lancet. 1994 Jan 29;343(8892):255–258. doi: 10.1016/s0140-6736(94)91110-x. [DOI] [PubMed] [Google Scholar]
- Ho J. L., He S., Hu A., Geng J., Basile F. G., Almeida M. G., Saito A. Y., Laurence J., Johnson W. D., 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] [Google Scholar]
- Holmberg S. D., Stewart J. A., Gerber A. R., Byers R. H., Lee F. K., O'Malley P. M., Nahmias A. J. Prior herpes simplex virus type 2 infection as a risk factor for HIV infection. JAMA. 1988 Feb 19;259(7):1048–1050. [PubMed] [Google Scholar]
- John G. C., Nduati R. W., Mbori-Ngacha D., Overbaugh J., Welch M., Richardson B. A., Ndinya-Achola J., Bwayo J., Krieger J., Onyango F. 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. doi: 10.1093/infdis/175.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kapiga S. H., Lyamuya E. F., Lwihula G. K., Hunter D. J. The incidence of HIV infection among women using family planning methods in Dar es Salaam, Tanzania. AIDS. 1998 Jan 1;12(1):75–84. doi: 10.1097/00002030-199801000-00009. [DOI] [PubMed] [Google Scholar]
- Kassler W. J., Zenilman J. M., Erickson B., Fox R., Peterman T. A., Hook E. W., 3rd Seroconversion in patients attending sexually transmitted disease clinics. AIDS. 1994 Mar;8(3):351–355. doi: 10.1097/00002030-199403000-00009. [DOI] [PubMed] [Google Scholar]
- Keet I. P., Lee F. K., van Griensven G. J., Lange J. M., Nahmias A., Coutinho R. A. 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. doi: 10.1136/sti.66.5.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kingsley L. A., Armstrong J., Rahman A., Ho M., Rinaldo C. R., 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] [Google Scholar]
- Kreiss J. K., Coombs R., Plummer F., Holmes K. K., Nikora B., Cameron W., Ngugi E., Ndinya Achola J. O., Corey L. Isolation of human immunodeficiency virus from genital ulcers in Nairobi prostitutes. J Infect Dis. 1989 Sep;160(3):380–384. doi: 10.1093/infdis/160.3.380. [DOI] [PubMed] [Google Scholar]
- Kreiss J., Willerford D. M., Hensel M., Emonyi W., Plummer F., Ndinya-Achola J., Roberts P. L., 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. doi: 10.1093/infdis/170.6.1597. [DOI] [PubMed] [Google Scholar]
- Kuiken C. L., van Griensven G. J., de Vroome E. M., Coutinho R. A. 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. doi: 10.1093/oxfordjournals.aje.a115688. [DOI] [PubMed] [Google Scholar]
- Laga M., Alary M., Nzila N., Manoka A. T., 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. doi: 10.1016/s0140-6736(94)93005-8. [DOI] [PubMed] [Google Scholar]
- Laga M., Manoka A., Kivuvu M., Malele B., Tuliza M., Nzila N., Goeman J., Behets F., Batter V., Alary M. 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. doi: 10.1097/00002030-199301000-00015. [DOI] [PubMed] [Google Scholar]
- Landry D. J., Forrest J. D. Public health departments providing sexually transmitted disease services. Fam Plann Perspect. 1996 Nov-Dec;28(6):261–266. [PubMed] [Google Scholar]
- Levine W. C., Pope V., Bhoomkar A., Tambe P., Lewis J. S., Zaidi A. A., Farshy C. E., Mitchell S., Talkington D. F. Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. J Infect Dis. 1998 Jan;177(1):167–174. doi: 10.1086/513820. [DOI] [PubMed] [Google Scholar]
- Levine W. C., Revollo R., Kaune V., Vega J., Tinajeros F., Garnica M., Estenssoro M., Lewis J. S., Higueras G., Zurita R. 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. doi: 10.1097/00002030-199814000-00022. [DOI] [PubMed] [Google Scholar]
- Magro C. M., Crowson A. N., Alfa M., Nath A., Ronald A., Ndinya-Achola J. O., 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. doi: 10.1016/s0046-8177(96)90285-3. [DOI] [PubMed] [Google Scholar]
- May R. M., Anderson R. M. Transmission dynamics of HIV infection. Nature. 1987 Mar 12;326(6109):137–142. doi: 10.1038/326137a0. [DOI] [PubMed] [Google Scholar]
- Mayaud P., Mosha F., Todd J., Balira R., Mgara J., West B., Rusizoka M., Mwijarubi E., Gabone R., Gavyole A. 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. doi: 10.1097/00002030-199715000-00013. [DOI] [PubMed] [Google Scholar]
- Mbizvo M. T., 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. doi: 10.1097/00002030-199607000-00013. [DOI] [PubMed] [Google Scholar]
- Mehendale S. M., Rodrigues J. J., Brookmeyer R. S., Gangakhedkar R. R., Divekar A. D., Gokhale M. R., Risbud A. R., Paranjape R. S., Shepherd M. E., Rompalo A. E. 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. doi: 10.1093/infdis/172.6.1486. [DOI] [PubMed] [Google Scholar]
- Mertens T. E., Hayes R. J., Smith P. G. Epidemiological methods to study the interaction between HIV infection and other sexually transmitted diseases. AIDS. 1990 Jan;4(1):57–65. doi: 10.1097/00002030-199001000-00008. [DOI] [PubMed] [Google Scholar]
- Miettinen O. S. Proportion of disease caused or prevented by a given exposure, trait or intervention. Am J Epidemiol. 1974 May;99(5):325–332. doi: 10.1093/oxfordjournals.aje.a121617. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1086/517297. [DOI] [PubMed] [Google Scholar]
- Moss G. B., Overbaugh J., Welch M., Reilly M., Bwayo J., Plummer F. A., Ndinya-Achola J. O., Malisa M. A., Kreiss J. K. 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. doi: 10.1093/infdis/172.6.1469. [DOI] [PubMed] [Google Scholar]
- Mostad S. B., Overbaugh J., DeVange D. M., Welch M. J., Chohan B., Mandaliya K., Nyange P., Martin H. L., Jr, Ndinya-Achola J., Bwayo J. J. 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. doi: 10.1016/S0140-6736(97)04240-2. [DOI] [PubMed] [Google Scholar]
- Nelson K. E., Eiumtrakul S., Celentano D., Maclean I., Ronald A., Suprasert S., Hoover D. R., Kuntolbutra S., Zenilman J. M. 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. doi: 10.1097/00042560-199712010-00011. [DOI] [PubMed] [Google Scholar]
- Nkowane B. M., Lwanga S. K. HIV and design of intervention studies for control of sexually transmitted diseases. AIDS. 1990;4 (Suppl 1):S123–S126. [PubMed] [Google Scholar]
- Nopkesorn T., Mock P. A., Mastro T. D., Sangkharomya S., Sweat M., Limpakarnjanarat K., Laosakkitiboran J., Young N. L., Morse S. A., Schmid S. 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. doi: 10.1097/00042560-199808010-00009. [DOI] [PubMed] [Google Scholar]
- Otten M. W., Jr, Zaidi A. A., Peterman T. A., Rolfs R. T., Witte J. J. High rate of HIV seroconversion among patients attending urban sexually transmitted disease clinics. AIDS. 1994 Apr;8(4):549–553. doi: 10.1097/00002030-199404000-00020. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1126/science.276.5320.1874. [DOI] [PubMed] [Google Scholar]
- Plourde P. J., Pepin J., Agoki E., Ronald A. R., Ombette J., Tyndall M., Cheang M., Ndinya-Achola J. O., D'Costa L. J., Plummer F. A. Human immunodeficiency virus type 1 seroconversion in women with genital ulcers. J Infect Dis. 1994 Aug;170(2):313–317. doi: 10.1093/infdis/170.2.313. [DOI] [PubMed] [Google Scholar]
- Plummer F. A., Simonsen J. N., Cameron D. W., Ndinya-Achola J. O., Kreiss J. K., Gakinya M. N., Waiyaki P., Cheang M., Piot P., Ronald A. R. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J Infect Dis. 1991 Feb;163(2):233–239. doi: 10.1093/infdis/163.2.233. [DOI] [PubMed] [Google Scholar]
- Plummer F. A., Wainberg M. A., Plourde P., Jessamine P., D'Costa L. J., Wamola I. A., Ronald A. R. 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. doi: 10.1093/infdis/161.4.810. [DOI] [PubMed] [Google Scholar]
- Robinson N. J., Mulder D. W., Auvert B., Hayes R. J. 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. doi: 10.1093/ije/26.1.180. [DOI] [PubMed] [Google Scholar]
- Schacker T., Ryncarz A. J., 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. doi: 10.1001/jama.280.1.61. [DOI] [PubMed] [Google Scholar]
- Sewankambo N., Gray R. H., Wawer M. J., Paxton L., McNaim D., Wabwire-Mangen F., Serwadda D., Li C., Kiwanuka N., Hillier S. L. HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet. 1997 Aug 23;350(9077):546–550. doi: 10.1016/s0140-6736(97)01063-5. [DOI] [PubMed] [Google Scholar]
- Spinola S. M., Orazi A., Arno J. N., Fortney K., Kotylo P., Chen C. Y., Campagnari A. A., Hood A. F. Haemophilus ducreyi elicits a cutaneous infiltrate of CD4 cells during experimental human infection. J Infect Dis. 1996 Feb;173(2):394–402. doi: 10.1093/infdis/173.2.394. [DOI] [PubMed] [Google Scholar]
- Stamm W. E., Handsfield H. H., Rompalo A. M., Ashley R. L., Roberts P. L., 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] [Google Scholar]
- Taha T. E., Hoover D. R., Dallabetta G. A., Kumwenda N. I., Mtimavalye L. A., Yang L. P., Liomba G. N., Broadhead R. L., Chiphangwi J. D., Miotti P. G. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998 Sep 10;12(13):1699–1706. doi: 10.1097/00002030-199813000-00019. [DOI] [PubMed] [Google Scholar]
- Telzak E. E., Chiasson M. A., Bevier P. J., Stoneburner R. L., Castro K. G., Jaffe H. W. HIV-1 seroconversion in patients with and without genital ulcer disease. A prospective study. Ann Intern Med. 1993 Dec 15;119(12):1181–1186. doi: 10.7326/0003-4819-119-12-199312150-00005. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1111/j.1365-2249.1995.tb03772.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vittinghoff E., Padian N. S. Attributable risk of exposures associated with sexually transmitted disease. J Infect Dis. 1996 Oct;174 (Suppl 2):S182–S187. doi: 10.1093/infdis/174.supplement_2.s182. [DOI] [PubMed] [Google Scholar]
- Wasserheit J. N. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis. 1992 Mar-Apr;19(2):61–77. [PubMed] [Google Scholar]
- Weir S. S., Feldblum P. J., Roddy R. E., Zekeng L. Gonorrhea as a risk factor for HIV acquisition. AIDS. 1994 Nov;8(11):1605–1608. doi: 10.1097/00002030-199411000-00013. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1056/NEJM199408113310601. [DOI] [PubMed] [Google Scholar]