Advertisement
AJOG Review| Volume 191, ISSUE 4, P1103-1112, October 2004

Managing the sexually transmitted disease pandemic: A time for reevaluation

      Abstract

      The serious implications of the sexually transmitted disease (STD) pandemic that currently challenges educators, medical practitioners and governments suggest that prevention strategies, which primarily focus on barrier protection and the management of infection, must be reevaluated and that initiatives focusing on primary prevention of behaviors predisposing individuals to STD risk must be adopted. Human immunodeficiency virus/acquired immunodeficiency syndrome, human papillomavirus, genital herpes, and Chlamydia are used to illustrate the pervasive presence of STDs and their serious consequences for individuals and national infrastructures. Long-term sequelae are discussed, including the emerging link between various sexually transmitted infections and cancer, and the psychosexual and psychosocial factors which impact infected individuals. Although risk reduction and treatment of existing infection is critical, the promotion of optimal life-long health can be achieved most effectively through delayed sexual debut, partner reduction, and the avoidance of risky sexual behaviors.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Obstetrics & Gynecology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Piot P.
        Introduction.
        Br Med Bull. 2001; 58: 3-5
        • Michaud C.M.
        • Murray C.J.
        • Bloom B.R.
        Burden of disease—implications for future research.
        JAMA. 2001; 285: 535-539
      1. Short C. Secretary of State for International Development. Presentation at the International Conference on HIV/AIDS Prevention, London, February 2002.

        • Lamptey P.R.
        Reducing heterosexual transmission of HIV in poor countries.
        BMJ. 2002; 324: 207-211
        • Gayle H.D.
        • Hill G.L.
        Global impact of human immunodeficiency virus and AIDS.
        Clin Microbiol Rev. 2001; 14: 327-335
        • Centers for Disease Control
        The global HIV and AIDS epidemic, 2001.
        MMWR Morb Mortal Wkly Rep. 2001; 50: 434-439
        • Cernescu C.
        Romanian HIV-AIDS epidemic after a decade of evolution.
        Rom J Virol. 1999; 50: 5-15
        • Ghys P.D.
        • Bazant W.
        • Monteiro M.G.
        • Calvani S.
        • Lazzari S.
        The epidemics of injecting drug use and HIV in Asia.
        AIDS. 2001; 15: S91-S99
        • Kalichman S.C.
        • Kelly J.A.
        • Sikkema K.J.
        • Koslov A.P.
        • Shaboltas A.
        • Granskaya J.
        The emerging AIDS crisis in Russia: review of enabling factors and prevention needs.
        Int J STD AIDS. 2000; 11: 71-75
      2. Fears of an Eastern European explosion of HIV epidemic are being realized.
        Aids Alert. 2002; 17 (3): 19-20
        • Chen X.S.
        • Gong X.D.
        • Liang G.J.
        • Zhang G.C.
        Epidemiologic trends of sexually transmitted diseases in China.
        Sex Transm Dis. 2000; 27: 138-142
        • Cohen M.S.
        • Ping G.
        • Fox K.
        • Henderson G.E.
        Sexually transmitted diseases in the People's Republic of China in Y2K: back to the future.
        Sex Transm Dis. 2000; 27: 143-145
        • Eberstadt N.
        The future of AIDS. American Enterprise Institute for Public Policy Research.
        Foreign Affairs, Council on Foreign Relations, Washington (DC)Nov/Dec 2002
        • Lemke D.
        Man no be God: Bushdoctor in Cameroon.
        Writers Club Press, Lincoln (NE)2001
      3. Genital HPV infection. 2001. In CDC: STD Prevention [Government website]. [cited 14 December 2002]. Available at: URL: http://www.cdc.gov/nchstp/dstd/Fact_Sheets/FactsHPV.htm.

      4. Health Canada. Population and Public Health Branch. STD Epi Update, Bureau of HIV/AIDS, STD and TB Update Series 2000.

        • Sellors J.W.
        • Karwalajtys T.L.
        • Kaczorowski J.
        • Mahony J.B.
        • Lytwyn A.
        • Chong S.
        • et al.
        Incidence, clearance and predictors of human papillomavirus infection in women.
        CMAJ. 2003; 168: 421-425
        • Collins S.
        • Mazloomzadeh S.
        • Winter H.
        • Blomfield P.
        • Bailey A.
        • Young L.S.
        • et al.
        High incidence of cervical human papillomavirus infection in women during their first sexual relationship.
        BJOG. 2002; 109: 96-98
        • Rosenfeld W.D.
        • Vermund S.H.
        • Wentz S.J.
        • Burk R.D.
        High prevalence rate of human papillomavirus infection and association with abnormal papanicolaou smears in sexually active adolescents.
        Arch Pediatr Adolesc Med. 1989; 143: 1443-1447
        • Rosenfeld W.D.
        Sexually transmitted diseases in adolescents: update 1991.
        Pediatr Ann. 1991; 20: 303-312
        • Beutner R.R.
        Human papillomavirus infection.
        J Am Acad Dermatol. 1989; 20: 113-123
        • Campion M.J.
        • Singer A.
        • Clarkson P.K.
        • McCance D.J.
        Increased risk of cervical neoplasia in consorts of men with penile condylomata acuminata.
        Lancet. 1985; 1: 943-946
        • Oriel J.D.
        Natural history of genital warts.
        Br J Vener Dis. 1971; 47: 1-13
        • Ho G.Y.
        • Bierman R.
        • Beardsley L.
        • Chang C.J.
        • Burk R.D.
        Natural history of cervicovaginal papillomavirus infection in young women.
        N Engl J Med. 1998; 338: 423-428
        • Crum C.P.
        The beginning of the end for cervical cancer?.
        N Engl J Med. 2002; 347: 1703-1705
        • Franceschi S.
        Human papillomavirus: a vaccine against cervical carcinoma uterine.
        Epidemiol Prev. 2002; 26: 140-144
      5. Human papillomaviruses and cancer. 2001. In: Cancer Information Services [a National Cancer Institute website]. [cited 25 March 2002]. Available at: URL:http://cis.nci.nih.gov/fact/3_20.htm.

        • Rice P.S.
        • Cason J.
        • Best J.M.
        • Banatvala J.E.
        High risk genital papillomavirus infections are spread vertically.
        Rev Med Virol. 1999; 9: 15-21
        • Munoz N.
        • Bosch F.X.
        • de Sanjose S.
        • Herrero R.
        • Castellsague X.
        • Shah K.V.
        • et al.
        Epidemiologic classification of human papillomavirus types associated with cervical cancer.
        N Engl J Med. 2003; 348: 518-527
        • Piketty C.
        • Darragh T.M.
        • Da Costa M.
        • Bruneval P.
        • Heard I.
        • Kazatchkine M.D.
        • et al.
        High prevalence of anal human papillomavirus infection and anal cancer precursors among HIV-infected persons in the absence of anal intercourse.
        Ann Intern Med. 2003; 138: 453-459
        • Chang J.Y.
        • Lin M.C.
        • Chiang C.P.
        High-risk human papillomaviruses may have an important role in non-oral habits-associated oral squamous cell carcinomas in Taiwan.
        Am J Clin Pathol. 2003; 120: 909-916
        • Centers for Disease Control
        Genital HPV Infection.
        National Center for HIV, STI and TB Prevention, Division of Sexually Transmitted Diseases Prevention, Atlanta (GA)2001
        • Hemminki K.
        • Dong C.
        Cancer in husbands of cervical cancer patients.
        Epidemiology. 2000; 11: 347-349
        • Picconi M.A.
        • Eijan A.M.
        • Distefano A.L.
        • Pueyo S.
        • Alonio L.V.
        • Gorostidi S.
        • et al.
        Human papillomavirus (HPV) DNA in penile carcinomas in Argentina: analysis of primary tumors and lymph nodes.
        J Med Virol. 2000; 61: 65-69
        • Rusk D.
        • Sutton G.P.
        • Look K.Y.
        • Roman A.
        Analysis of invasive squamous cell carcinoma of the vulva and vulvar intraepithelial neoplasia for the presence of human papillomavirus DNA.
        Obstet Gynecol. 1991; 77: 918-922
        • Gillison M.L.
        • Koch W.M.
        • Capone R.B.
        • Spafford M.
        • Westra W.H.
        • Wu L.
        • et al.
        Evidence for a causal association between human papillomavirus and a subset of head and neck cancers.
        J Natl Cancer Inst. 2000; 92: 709-720
        • Mork J.
        • Lie A.K.
        • Glattre E.
        • Hallmans G.
        • Jellum E.
        • Koskela P.
        • et al.
        Human papillomavirus infection as a risk factor for squamous-cell carcinoma of the head and neck.
        N Engl J Med. 2001; 344: 1125-1131
        • Frisch M.
        • Glimelius B.
        • van den Brule A.J.
        • Wohlfahrt J.
        • Meijer C.J.
        • Walboomers J.M.
        • et al.
        Sexually transmitted infection as a cause of anal cancer.
        N Engl J Med. 1997; 337: 1350-1358
        • Orjuela M.
        • Castaneda V.P.
        • Ridaura C.
        • Lecona E.
        • Leal C.
        • Abramson D.H.
        • et al.
        Presence of human papilloma virus in tumor tissue from children with retinoblastoma: an alternative mechanism for tumor development.
        Clin Cancer Res. 2000; 6: 4010-4016
        • Hughes J.P.
        • Garnett G.P.
        • Koutsky L.
        The theoretical population-level impact of a prophylactic human papilloma virus vaccine.
        Epidemiology. 2002; 13: 631-639
        • Sharma D.C.
        HPV vaccine trial may take place in India.
        Lancet Oncol. 2002; 3: 649
        • Koutsky L.A.
        • Ault K.A.
        • Wheeler C.M.
        • Brown D.R.
        • Barr E.
        • Alvarez F.B.
        • et al.
        A controlled trial of a human papillomavirus type 16 vaccine.
        N Engl J Med. 2002; 347: 1645-1651
        • Corey L.
        • Handsfield H.H.
        Genital herpes and public health: addressing a global problem.
        JAMA. 2000; 283: 791-794
        • Nahmias A.J.
        • Lee F.K.
        • Beckman-Nahmias S.
        Sero-epidemiological and -sociological patterns of herpes simplex virus infection in the world.
        Scand J Infect Dis Suppl. 1990; 69: 19-36
        • Fleming D.T.
        • McQuillan G.M.
        • Johnson R.E.
        • Nahmias A.J.
        • Aral S.O.
        • Lee F.K.
        • et al.
        Herpes simplex virus type 2 in the United States, 1976 to 1994.
        N Engl J Med. 1997; 337: 1105-1111
        • Anagrius C.
        • Hallen A.
        • Moi H.
        • Persson E.
        Prevention of sexually transmitted diseases and abortions–the present situation for medical care of sexually transmitted diseases in Sweden.
        Semin Dermatol. 1990; 9: 190-193
        • Corbett E.L.
        • Steketee R.W.
        • ter Kuile F.O.
        • Latif A.S.
        • Kamali A.
        • Hayes R.J.
        HIV-1/AIDS and the control of other infectious diseases in Africa.
        Lancet. 2002; 359: 2177-2187
        • Wald A.
        • Link K.
        Risk of human immunodeficiency virus infection in herpes simplex virus type 2-seropositive persons: a meta-analysis.
        J Infect Dis. 2002; 185: 45-52
        • Smith J.S.
        • Herrero R.
        • Bosetti C.
        • Munoz N.
        • Bosch F.X.
        • Eluf-Neto J.
        • et al.
        Herpes simplex virus-2 as a human papillomavirus cofactor in the etiology of invasive cervical cancer.
        J Natl Cancer Inst. 2002; 94: 1604-1613
        • Brown Z.A.
        • Benedetti J.
        • Ashley R.
        • Burchett S.
        • Selke S.
        • Berry S.
        • et al.
        Neonatal herpes simplex virus infection in relation to asymptomatic maternal infection at the time of labor.
        N Engl J Med. 1991; 324: 1247-1252
        • Stanberry L.R.
        • Spruance S.L.
        • Cunningham A.L.
        • Bernstein D.I.
        • Mindel A.
        • Sacks S.
        • et al.
        Glycoprotein-D-adjuvant vaccine to prevent genital herpes.
        N Engl J Med. 2002; 347: 1652-1661
        • Navarro C.
        • Jolly A.
        • Nair R.
        • Chen Y.
        Risk factors for genital chlamydial infection.
        Can J Infect Dis. 2002; 13: 195-207
        • Gaydos C.A.
        • Howell M.R.
        • Pare B.
        • Clark K.L.
        • Ellis D.A.
        • Hendrix R.M.
        • et al.
        Chlamydia trachomatis infections in female military recruits.
        N Engl J Med. 1998; 339: 739-744
        • Buve A.
        • Weiss H.A.
        • Laga M.
        • Van Dyck E.
        • Musonda R.
        • Zekeng L.
        • et al.
        The epidemiology of gonorrhoea, chlamydial infection and syphilis in four African cities.
        AIDS. 2001; 15: S79-S88
        • Wallin K.L.
        • Wiklund F.
        • Luostarinen T.
        • Angstrom T.
        • Anttila T.
        • Bergman F.
        • et al.
        A population-based prospective study of Chlamydia trachomatis infection and cervical carcinoma.
        Int J Cancer. 2002; 101: 371-374
        • Turner C.F.
        • Roger S.M.
        • Miller H.G.
        • Miller W.C.
        • Gribble J.N.
        • Chromy J.R.
        • et al.
        Untreated gonococcal and chlamydial infection in a probability sample of adults.
        JAMA. 2002; 287: 726-733
        • Workowski K.A.
        • Levine W.C.
        Sexually transmitted diseases treatment guidelines 2002. Centers for Disease Control and Prevention.
        MMWR Recomm Rep. 2002; 51: 1-78
        • Wiesenfeld H.C.
        • Lowry D.L.
        • Heine R.P.
        • Krohn M.A.
        • Bittner H.
        • Kellinger K.
        • et al.
        Self-collection of vaginal swabs for the detection of Chlamydia, gonorrhea, and trichomoniasis: opportunity to encourage sexually transmitted disease testing among adolescents.
        Sex Transm Dis. 2001; 28: 321-325
        • Schachter J.
        Chlamydial infections.
        West J Med. 1990; 153: 523-534
        • Patrick D.M.
        Chlamydia control: components of an effective control strategy to reduce the incidence of Chlamydia trachomatis.
        Can J Human Sex. 1997; 6: 143-149
        • Genuis S.J.
        Risky sex: the onslaught of sexually transmitted disease.
        KEG Publishing, Edmonton (Canada)1992
        • Meeker M.
        Epidemic: how teen sex is killing our kids.
        Lifeline Press, Washington (DC)2002
        • Munger K.
        The role of human papillomaviruses in human cancers.
        Front Biosci. 2002; 7: d641-d649
        • Kadow J.F.
        • Regueiro-Ren A.
        • Weinheimer S.P.
        The role of viruses in human cancer development and antiviral approaches for intervention.
        Curr Opin Investig Drugs. 2002; 3: 1574-1579
        • Anttila T.
        • Saikku P.
        • Koskela P.
        • Bloigu A.
        • Dillner J.
        • Ikaheimo I.
        • et al.
        Serotypes of Chlamydia trachomatis and risk for development of cervical squamous cell carcinoma.
        JAMA. 2001; 285: 47-51
        • Mayor S.
        Human papilloma-virus classified as carcinogenic.
        BMJ. 1996; 313: 70
        • Moscicki A.B.
        • Hills N.
        • Shiboski S.
        • Powell K.
        • Jay N.
        • Hanson E.
        • et al.
        Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females.
        JAMA. 2001; 285: 2995-3002
        • Vezina C.
        • Steben M.
        Genital herpes: psychosexual impacts and counselling.
        Can J Cont Med Ed. 2001; 13: 125-137
        • Silber T.J.
        Mental health aspects of sexually transmitted diseases in adolescents.
        in: Greydanus D.E. Wolraich M.L. Behavior pediatrics. Springer-Verlag, New York1992: 381-386
        • Clarke P.
        • Ebel C.
        • Catotti D.N.
        • Stewart S.
        The psychosocial impact of human papillomavirus infection: implications for health care providers.
        Int J STD AIDS. 1996; 7: 197-200
        • Rosemberg S.K.
        Sexually transmitted papillomaviral infection in men: an update.
        Dermatol Clin. 1991; 9: 317-331
        • Campion M.J.
        • Brown J.R.
        • McCance D.J.
        • Atia W.
        • Edwards R.
        • Cuzick J.
        • et al.
        Psychosexual trauma of an abnormal cervical smear.
        BJOG. 1988; 95: 175-181
        • Voog E.
        • Lowhagen G.B.
        Follow-up of men with genital papilloma virus infection: psychosexual aspects.
        Acta Derm Venereol. 1992; 72: 185-186
        • VanderPlate C.
        • Aral S.O.
        Psychosocial aspects of genital herpes virus infection.
        Health Psychol. 1987; 6: 57-72
        • Vezina C.
        • Steben M.
        Psychosexual impacts of human papillomavirus.
        Can J Cont Med Ed. 2001; 13: 139-153
      6. Health Canada. Population and Public Health Branch. Infectious syphilis in Canada. STD Epi Update, Bureau of HIV/AIDS, STD and TB Update Series 2002.

        • Centers for Disease Control
        Congenital syphilis—New York City, 1986-1988.
        MMWR Morb Mortal Wkly Rep. 1989; 38: 825-829
        • Kaul D.
        • Patel J.A.
        Clinical manifestations and management of pediatric HIV infection.
        Indian J Pediatr. 2001; 68: 623-631
        • Walker N.
        • Schwartlander B.
        • Bryce J.
        Meeting international goals in child survival and HIV/AIDS.
        Lancet. 2002; 360: 284-289
        • Meyers T.M.
        • Pettifor J.M.
        • Gray G.E.
        • Crewe-Brown H.
        • Galpin J.S.
        Pediatric admissions with human immunodeficiency virus infection at a regional hospital in Soweto, South Africa.
        J Trop Pediatr. 2000; 46: 224-230
        • Whitley R.J.
        • Arvin A.M.
        Herpes simplex infections.
        in: Remington J.S. Klein J.O. Infectious diseases of the fetus and newborn infant. 4th ed. WB Saunders, Philadelphia1995: 354-376
        • Puranen M.
        • Yliskoski M.
        • Saarikoski S.
        • Syrjanen K.
        • Syrjanen S.
        Vertical transmission of human papillomavirus from infected mothers to their newborn babies and persistence of the virus in childhood.
        Am J Obstet Gynecol. 1996; 174: 694-699
        • Rice P.S.
        • Mant C.
        • Cason J.
        • Bible J.M.
        • Muir P.
        • Kell B.
        • et al.
        High prevalence of human papillomavirus type 16 infection among children.
        J Med Virol. 2000; 61: 70-75
        • Tseng C.J.
        • Liang C.C.
        • Soong Y.K.
        • Pao C.C.
        Perinatal transmission of human papillomavirus in infants: relationship between infection rate and mode of delivery.
        Obstet Gynecol. 1998; 91: 92-96
        • Armbruster-Moraes E.
        • Ioshimoto L.M.
        • Leao E.
        • Zugaib M.
        Detection of human papillomavirus deoxyribonucleic acid sequences in amniotic fluid during different periods of pregnancy.
        Am J Obstet Gynecol. 1993; 169: 1074
        • Armbruster-Moraes E.
        • Ioshimoto L.M.
        • Leao E.
        • Zugaib M.
        Presence of human papillomavirus DNA in amniotic fluids of pregnant women with cervical lesions.
        Gynecol Oncol. 1994; 54: 152-158
        • Cordon-Cardo C.
        Virus linked to pediatric eye tumor.
        National Cervical Cancer Coalition, Van Nuys (CA)2001 (Research bulletin)
        • Buka S.L.
        • Tsuang M.T.
        • Torrey E.F.
        • Klebanoff M.A.
        • Bernstein D.
        • Yolken R.H.
        Maternal infections and subsequent psychosis among offspring.
        Arch Gen Psychiatry. 2001; 58: 1032-1037
        • Low-Beer D.
        • Stoneburner R.L.
        • Mukulu A.
        Empirical evidence for the severe but localized impact of AIDS on population structure.
        Nat Med. 1997; 3: 553-557
        • McIlhaney Jr., J.S.
        Sexually transmitted infection and teenage sexuality.
        Am J Obstet Gynecol. 2000; 183: 334-339
        • Genuis S.J.
        • Genuis S.K.
        The dilemma of adolescent sexuality, I: the onslaught of sexually transmitted diseases.
        J Soc Obstet Gynecol Can. 1993; 15: 552-565
        • Wald A.
        • Langenberg A.G.
        • Link K.
        • Izu A.E.
        • Ashley R.
        • Warren T.
        • et al.
        Effect of condoms on reducing the transmission of herpes simplex virus type 2 from men to women.
        JAMA. 2001; 285: 3100-3106
        • Genuis S.J.
        • Genuis S.K.
        Orgasm without organisms: science or propaganda?.
        Clin Pediatr. 1996; 35: 10-17
        • Giovannelli L.
        • Campisi G.
        • Lama A.
        • Giambalvo O.
        • Osborn J.
        • Margiotta V.
        • et al.
        Human papillomavirus DNA in oral mucosal lesions.
        J Infect Dis. 2002; 185: 833-836
        • Edwards S.
        • Carne C.
        Oral sex and the transmission of viral STIs.
        Sex Transm Infect. 1998; 74: 6-10
        • Oncale R.M.
        • King B.M.
        Comparison of men's and women's attempts to dissuade sexual partners from the couple using condoms.
        Arch Sex Behav. 2001; 30: 379-391
        • Macaluso M.
        • Kelaghan J.
        • Artz L.
        • Austin H.
        • Fleenor M.
        • Hook 3rd, E.W.
        • et al.
        Mechanical failure of the latex condom in a cohort of women at high STD risk.
        Sex Transm Dis. 1999; 26: 450-458
        • Warner L.
        • Clay-Warner J.
        • Boles J.
        • Williamson J.
        Assessing condom use practices: implications for evaluating method and user effectiveness.
        Sex Transm Dis. 1998; 25: 273-277
        • 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; 331: 341-346
        • Hausser D.
        • Michaud P.A.
        Does a condom-promoting strategy (the Swiss STOP-AIDS campaign) modify sexual behavior among adolescents?.
        Pediatrics. 1994; 93: 580-585
        • Catania J.A.
        • Coates T.J.
        • Stall R.
        • Turner H.
        • Peterson J.
        • Hearst N.
        • et al.
        Prevalence of AIDS-related risk factors and condom use in the United States.
        Science. 1992; 258: 1101-1106
        • Weisman C.S.
        • Plichta S.
        • Nathanson C.A.
        • Ensminger M.
        • Robinson J.C.
        Consistency of condom use for disease prevention among adolescent users of oral contraceptives.
        Fam Plann Perspect. 1991; 23: 71-74
        • Kegeles S.M.
        • Adler N.E.
        • Irwin Jr., C.E.
        Sexually active adolescents and condoms: changes over one year in knowledge, attitudes and use.
        Am J Public Health. 1988; 78: 460-461
        • Genuis S.J.
        • Genuis S.K.
        Dealing with the AIDS epidemic: quo vadis?.
        J Soc Obstet Gyncol Can. 1995; 17: 219-223
        • Madhok R.
        • McCallum A.K.
        • McEwan R.
        • Bhopal R.S.
        Students' knowledge and behavior concerning safer sex: a UK study.
        J Am Coll Health. 1993; 42: 121-125
        • Tyden T.
        • Olsson S.
        • Bjorkelund-Ylander C.
        Female university students in Sweden: sex, contraception and STDs.
        Adv Contracept. 1991; 7: 165-171
        • Herlitz C.
        Condom use due to the risk of AIDS: trends in the general population of Sweden.
        Scand J Soc Med. 1992; 20: 102-109
        • Catania J.A.
        • Binson D.
        • Docini M.M.
        • Stall R.
        • Choi K.H.
        • Pollack L.M.
        • et al.
        Risk factors for HIV and other sexually transmitted diseases and prevention practices among US heterosexual adults: changes from 1990 to 1992.
        Am J Public Health. 1995; 85: 1492-1499
        • Bankole A.
        • Darroch J.E.
        • Singh S.
        Determinants of trends in condom use in the United States, 1988-1995.
        Fam Plann Perspect. 1999; 31: 264-271
        • Ahmed S.
        • Lutalo T.
        • Wawer M.
        • Serwadda D.
        • Sewankambo N.K.
        • Nalugoda F.
        • et al.
        HIV incidence and sexually transmitted disease prevalence associated with condom use: a population study in Rakai, Uganda.
        AIDS. 2001; 15: 2171-2179
        • Rojanapithayakorn W.
        • Hanenberg R.
        The 100% condom program in Thailand.
        AIDS. 1996; 10: 1-7
        • Hanenberg R.S.
        • Rojanapithayakorn W.
        • Kunasol P.
        • Sokal D.C.
        Impact of Thailand's HIV-control programme as indicated by the decline of sexually transmitted diseases.
        Lancet. 1994; 344: 243-245
        • Pisani E.
        • Garnett G.P.
        • Grassly N.C.
        • Brown T.
        • Stover J.
        • Hankins C.
        • et al.
        Back to basics in HIV prevention: focus on exposure.
        BMJ. 2003; 326: 1384-1387
        • Alary M.
        • Mukenge-Tshibaka L.
        • Bernier F.
        • Geraldo N.
        • Lowndes C.M.
        • Meda H.
        • et al.
        Decline in the prevalence of HIV and sexually transmitted diseases among female sex workers in Cotonou, Benin, 1993-1999.
        AIDS. 2002; 16: 463-470
        • Shelton A.J.
        • Halperin D.T.
        • Nantulya V.
        • Potts M.
        • Gayle H.D.
        • Holmes K.K.
        Partner reduction is crucial for balanced “ABC” approach to HIV prevention.
        BMJ. 2004; 328: 891-894
        • Green E.C.
        • Conde A.
        Sexual partner reduction and HIV infection.
        Sex Transm Infect. 2000; 76: 145
        • Kilmarx P.H.
        • Palanuvej T.
        • Limpakarnjanarat K.
        • Chitvarakorn A.
        • St Louis M.E.
        • Mastro T.D.
        Seroprevalence of HIV among female sex workers in Bangkok: evidence of ongoing infection risk after the “100% condom program” was implemented.
        J Acquir Immune Defic Syndr. 1999; 21: 313-316
        • Nelson K.E.
        • Celentano D.D.
        • Eiumtrakol S.
        • Hoover D.R.
        • Beyrer C.
        • Suprasert S.
        • et al.
        Changes in sexual behavior and a decline in HIV infection among young men in Thailand.
        N Engl J Med. 1996; 335: 297-303
        • Paz-Bailey G.
        • Kilmarx P.H.
        • Supawitkul S.
        • Chaowanachan T.
        • Jeeyapant S.
        • Sternberg M.
        • et al.
        Risk factors for sexually transmitted diseases in northern Thai adolescents: an audio-computer-assisted self-interview with noninvasive specimen collection.
        Sex Transm Dis. 2003; 30: 320-326
        • Thato S.
        • Charron-Prochownik D.
        • Dorn L.D.
        • Albrecht S.A.
        • Stone C.A.
        Predictors of condom use among adolescent Thai vocational students.
        J Nurs Scholarsh. 2003; 35: 157-163
        • Lertpiriyasuwat C.
        • Plipat T.
        • Jenkins R.A.
        A survey of sexual risk behavior for HIV infection in Nakhonsawan, Thailand, 2001.
        AIDS. 2003; 17: 1969-1976
        • Stammers T.
        • Ingham R.
        For and against: doctors should advise adolescents to abstain from sex.
        BMJ. 2000; 321: 1520-1522
        • Stuart-Smith S.
        Teenage sex.
        BMJ. 1996; 312: 390-391
        • Kay L.E.
        Adolescent sexual intercourse: strategies for promoting abstinence in teens.
        Postgrad Med. 1995; 97 (132-4): 121-127
        • Genuis S.J.
        • Genuis S.K.
        Adolescent sexual involvement: time for primary prevention.
        Lancet. 1995; 345: 240-241
        • Genuis S.J.
        • Genuis S.K.
        The dilemma of adolescent sexuality: part IV—dealing with the challenge.
        J Soc Obstet Gyncol Can. 1994; 16: 1343-1359
        • Sonenstein F.L.
        • Pleck J.H.
        • Ku L.C.
        Levels of sexual activity among adolescent males in the United States.
        Fam Plann Perspect. 1991; 23: 162-167
        • Wasserheit J.N.
        Effect of changes in human ecology and behavior on patterns of sexually transmitted diseases, including human immunodeficiency virus infection.
        Proc Natl Acad Sci U S A. 1994; 91: 2430-2435
        • Santelli J.S.
        • Brener N.D.
        • Lowry R.
        • Bhatt A.
        • Zabin L.S.
        Multiple sexual partners among U.S. adolescents and young adults.
        Fam Plann Perspect. 1998; 30: 271-275
        • Greenberg J.
        • Magder L.
        • Aral S.
        Age at first coitus: a marker for risky sexual behavior in women.
        Sex Transm Dis. 1992; 19: 331-334
        • Genuis S.J.
        • Genuis S.K.
        Teen sex: reality check.
        Winfield House Publishing, Edmonton (Canada)2002
        • Cohen M.W.
        Adolescent sexual activity as an expression of nonsexual needs.
        Pediatr Ann. 1995; 24: 324-329
        • Hawkins J.D.
        • Catalano R.F.
        • Kosterman R.
        • Abbott R.
        • Hill K.G.
        Preventing adolescent health-risk behaviors by strengthening protection during childhood.
        Arch Pediatr Adolesc Med. 1999; 153: 226-234
        • Jorgensen S.R.
        • Potts V.
        • Camp B.
        Project taking charge: six month follow-up of a pregnancy prevention program for early adolescents.
        Fam Relations. 1993; 42: 401-406
        • Weinstein M.
        • Thornton A.
        Mother-child relations and adolescent sexual attitudes and behavior.
        Demography. 1989; 26: 563-577
        • Santelli J.S.
        • DiClemente R.J.
        • Miller K.S.
        • Kirby D.
        Sexually transmitted diseases, unintended pregnancy, and adolescent health promotion.
        Adolesc Med. 1999; 10: 87-108
        • Small S.A.
        • Luster T.
        Adolescent sexual activity: an ecological risk-factor approach.
        J Marriage Fam. 1994; 56: 181-192
        • Hillis S.D.
        • Anda R.F.
        • Felitti V.J.
        • Marchbanks P.A.
        Adverse childhood experiences and sexual risk behaviors in women: a retrospective cohort study.
        Fam Plann Perspect. 2001; 33: 206-211
        • Santelli J.S.
        • Lowry R.
        • Brener N.D.
        • Robin L.
        The association of sexual behaviors with socioeconomic status, family structure, and race/ethnicity among US adolescents.
        Am J Public Health. 2000; 90: 1582-1588
        • Blum R.W.
        • Beuhring T.
        • Shew M.L.
        • Bearinger L.H.
        • Sieving R.E.
        • Resnick M.D.
        The effects of race/ethnicity, income, and family structure on adolescent risk behaviors.
        Am J Public Health. 2000; 90: 1879-1884
        • Resnick M.D.
        • Bearman P.S.
        • Blum R.W.
        • Bauman K.E.
        • Harris K.M.
        • Jones J.
        • et al.
        Protecting adolescents from harm: findings from the National Longitudinal Study on Adolescent Health.
        JAMA. 1997; 278: 823-832
        • Rosenthal S.L.
        • Von Ranson K.M.
        • Cotton S.
        • Biro F.M.
        • Mills L.
        • Succop P.A.
        Sexual initiation: predictors and developmental trends.
        Sex Transm Dis. 2001; 28: 527-532
        • Ellen J.M.
        • Adler N.
        Sexual initiation and developmental changes.
        Sex Transm Dis. 2001; 28: 533-534
        • Young E.W.
        • Jensen L.C.
        • Olsen J.A.
        • Cundick B.P.
        The effects of family structure on the sexual behavior of adolescents.
        Adolescence. 1991; 26: 977-986
        • Fergusson D.M.
        • Lynskey M.T.
        Alcohol misuse and adolescent sexual behaviors and risk taking.
        Pediatrics. 1996; 98: 91-96
        • Halpern-Felsher B.L.
        • Millstein S.G.
        • Ellen J.M.
        Relationship of alcohol use and risky sexual behavior: a review and analysis of findings.
        J Adolesc Health. 1996; 19: 331-336
        • Strunin L.
        • Hingson R.
        Alcohol, drugs, and adolescent sexual behavior.
        Int J Addict. 1992; 27: 129-146
        • Shafer M.A.
        • Boyer C.B.
        Psychosocial and behavioral factors associated with risk of sexually transmitted diseases, including human immunodeficiency virus infection, among urban high school students.
        J Pediatr. 1991; 119: 826-833
        • Ammann A.J.
        Preventing HIV.
        BMJ. 2003; 326: 1342-1343
        • Vincent M.L.
        • Clearie A.F.
        • Schluchter M.D.
        Reducing adolescent pregnancy through school and community-based education.
        JAMA. 1987; 257: 3382-3386
        • Blake S.M.
        • Simkin L.
        • Ledsky R.
        • Perkins C.
        • Calabrese J.M.
        Effects of a parent-child communications intervention on young adolescents' risk for early onset of sexual intercourse.
        Fam Plann Perspect. 2001; 33: 52-61
        • Sieving R.E.
        • McNeely C.S.
        • Blum R.W.
        Maternal expectations, mother-child connectedness, and adolescent sexual debut.
        Arch Pediatr Adolesc Med. 2000; 154: 809-816
        • Griffin G.C.
        Condoms and contraceptives in junior high and high school clinics: what do you think?.
        Postgrad Med. 1993; 93 (26-8, 37-8): 21-23
        • Howard M.
        • McCabe J.B.
        Helping teenagers postpone sexual involvement.
        Fam Plann Perspect. 1990; 22: 21-26
        • Hubbard B.M.
        • Giese M.L.
        • Rainey J.
        A replication study of reducing the risk, a theory-based sexuality curriculum for adolescents.
        J Sch Health. 1998; 68: 243-247
        • Kirby D.
        • Barth R.P.
        • Leland N.
        • Fetro J.V.
        Reducing the risk: impact of a new curriculum on sexual risk-taking.
        Fam Plann Perspect. 1991; 23: 253-263
        • Centers for Disease Control
        Trends in sexual risk behaviors among high school students—United States, 1991-2001.
        MMWR Morb Mortal Wkly Rep. 2002; 51: 856-859
        • Centers for Disease Control
        Trends in sexual risk behaviors among high school students—United States, 1991-1997.
        MMWR Morb Mortal Wkly Rep. 1998; 47: 749-752
        • Ford K.
        • Sohn W.
        • Lepkowski J.
        American adolescents: sexual mixing patterns, bridge partners, and concurrency.
        Sex Transm Dis. 2002; 29: 13-19
        • Hogle J.
        • Green E.C.
        • Nantulya V.
        • Stoneburner R.
        • Stover J.
        What happened in Uganda? Declining HIV prevalence, behavior change, and the national response.
        US Agency for International Development, Office of HIV/AIDS, Bureau of Global Health, Washington (DC)2002
        • Allen A.
        Sex change.
        New Republic. 2002; 226: 14-15
      7. Uganda tackles AIDS from the very top down.
        AIDS Alert. 1999; 14: 3-4
        • Kilian A.H.
        • Gregson S.
        • Ndyanabangi B.
        • Walusaga K.
        • Kipp W.
        • Sahlmuller G.
        • et al.
        Reductions in risk behaviour provide the most consistent explanation for declining HIV-1 prevalence in Uganda.
        AIDS. 1999; 13: 391-398
        • Whitworth J.A.
        • Mahe C.
        • Mbulaiteye S.M.
        • Nakiyingi J.
        • Ruberantwari A.
        • Ojwiya A.
        • et al.
        HIV-1 epidemic trends in rural south-west Uganda over a 10-year period.
        Trop Med Int Health. 2002; 7: 1047-1052
        • Grulich A.E.
        • Kaldor J.M.
        Evidence of success in HIV prevention in Africa.
        Lancet. 2002; 360: 3-4
        • Mbulaiteye S.M.
        • Mahe C.
        • Whitworth J.A.
        • Ruberantwari A.
        • Nakiyingi J.S.
        • Ojwiya A.
        • et al.
        Declining HIV-1 incidence and associated prevalence over 10 years in a rural population in south-west Uganda: a cohort study.
        Lancet. 2002; 360: 41-46
        • Okware S.
        • Opio A.
        • Musinguzi J.
        • Waibale P.
        Fighting HIV/AIDS: is success possible?.
        Bull World Health Organ. 2001; 79: 1113-1120
        • Buve A.
        • Bishikwabo-Nsarhaza K.
        • Mutangadura G.
        The spread and effect of HIV-1 infection in sub-Saharan Africa.
        Lancet. 2002; 359: 2011-2017
      8. Nantulya VN. HIV/AIDS prevention: policy and program context of Uganda's success story. Presentation to USAID, Washington, DC, February 5, 2002.

        • Adetunji J.
        • Meekers D.
        Consistency in condom use in the context of HIV/AIDS in Zimbabwe.
        J Biosoc Sci. 2001; 33: 121-138
      9. Fact list. AIDS: Focus on Africa.
        CMAJ. 2002; 167: 529