The influence of hormonal contraceptive use on HIV-1 transmission and disease progression

Clinical Infectious Diseases

Volumn 45, Issue 3, 2007, Pages 360-369

  Baeten, Jared M ^a,c   Lavreys, Ludo ^a   Overbaugh, Julie ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c Seattle HIV Prevention Trials Unit   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRACEPTIVE AGENT; LEVONORGESTREL; MEDROXYPROGESTERONE ACETATE; ORAL CONTRACEPTIVE AGENT;

AFRICA; CHLAMYDIASIS; CONDOM; DISEASE COURSE; DOSE RESPONSE; GENITAL HERPES; HORMONAL CONTRACEPTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INCIDENCE; INFECTION RISK; INFECTION SENSITIVITY; INTRAUTERINE CONTRACEPTIVE DEVICE; PRIORITY JOURNAL; PUBLIC HEALTH SERVICE; REVIEW; SEXUALLY TRANSMITTED DISEASE; SIDE EFFECT; UTERINE CERVICITIS; VAGINITIS; VIRUS TRANSMISSION;

CONTRACEPTIVES, ORAL, HORMONAL; DISEASE PROGRESSION; DISEASE SUSCEPTIBILITY; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MALE; WORLD HEALTH;

EID: 34547103232     PISSN: 10584838     EISSN: None     Source Type: Journal    
DOI: 10.1086/519432     Document Type: Review

References (89)

1. Joint United Nations Programme on HIV/AIDS. Report on the global AIDS epidemic 2006. Available at: http://www.unaids.org/en/HIV_ data/ 2006GlobalReport/default.asp. Accessed 14 September 2006.
2. Population Division, United Nations Department of Economic and Social Affairs. World Contraceptive Use 2003. Available at: http:// www.un.org/esa/population/publications/contraceptive2003/WallChart_ CP2003.pdf. Accessed 14 September 2006.
3. Burkman RT Jr. Noncontraceptive effects of hormonal contraceptives: bone mass, sexually transmitted disease and pelvic inflammatory disease, cardiovascular disease, menstrual function, and future fertility. Am J Obstet Gynecol 1994; 170:1569-75.
4. Food and Drug Administration. Black box warning added concerning long-term use of Depo-Provera Contraceptive Injection. Available at: http://www.fda.gov/bbs/topics/ANSWERS/2004/ANS01325.html. Accessed 7 February 2006.
5. Marx PA, Spira AI, Gettie A, et al. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat Med 1996; 2:1084-9.
6. Smith SM, Baskin GB, Marx PA. Estrogen protects against vaginal transmission of simian immunodeficiency virus. J Infect Dis 2000; 182: 708-15.
7. Smith SM, Mefford M, Sodora D, et al. Topical estrogen protects against SIV vaginal transmission without evidence of systemic effect. AIDS 2004; 18:1637-43.
8. Abel K, Rourke T, Lu D, Bost K, McChesney MB, Miller CJ. Abrogation of attenuated lentivirus-induced protection in rhesus macaques by administration of Depo-Provera before intravaginal challenge with simian immunodeficiency virus mac239. J Infect Dis 2004; 190:1697-705.
9. Veazey RS, Klasse PJ, Schader SM, et al. Protection of macaques from vaginal SHIV challenge by vaginally delivered inhibitors of virus-cell fusion. Nature 2005; 438:99-102.
10. Mauck CK, Callahan MM, Baker J, et al. The effect of one injection of Depo-Provera on the human vaginal epithelium and cervical ectopy. Contraception 1999; 60:15-24.
11. Bahamondes L, Trevisan M, Andrade L, et al. The effect upon the human vaginal histology of the long-term use of the injectable contraceptive Depo-Provera. Contraception 2000; 62:23-7.
12. Miller L, Patton DL, Meier A, Thwin SS, Hooton TM, Eschenbach DA. Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol 2000; 96:431-9.
13. Critchlow CW, Wolner-Hanssen P, Eschenbach DA, et al. Determinants of cervical ectopia and of cervicitis: age, oral contraception, specific cervical infection, smoking, and douching. Am J Obstet Gynecol 1995; 173:534-43.
14. Baeten JM, Nyange PM, Richardson BA, et al. Hormonal contraception and risk of sexually transmitted disease acquisition: results from a prospective study. Am J Obstet Gynecol 2001; 185:380-5.
15. Moss GB, Clemetson D, D'Costa L, et al. Association of cervical ectopy with heterosexual transmission of human immunodeficiency virus: results of a study of couples in Nairobi, Kenya. J Infect Dis 1991; 164: 588-91.
16. Kapiga SH, Lyamuya EF, Kwihula GK, Hunter DJ. The incidence of HIV infection among women using family planning methods in Dar es Salaam, Tanzania. AIDS 1998; 12:75-84.
17. Cottingham J, Hunter D. Chlamydia trachomatis and oral contraceptive use: a quantitative review. Genitourin Med 1992; 68:209-16.
18. Avonts D, Sercu M, Heyerick P, Vandermeeren I, Meheus A, Piot P. Incidence of uncomplicated genital infections in women using oral contraception or an intrauterine device: a prospective study. Sex Transm Dis 1990; 17:23-9.
19. Louv WC, Austin H, Perlman J, Alexander WJ. Oral contraceptive use and the risk of chlamydial and gonococcal infections. Am J Obstet Gynecol 1989; 160:396-402.
20. Morrison CS, Bright P, Wong EL, et al. Hormonal contraceptive use, cervical ectopy, and the acquisition of cervical infections. Sex Transm Dis 2004; 31:561-7.
21. Washington AE, Gove S, Schachter J, Sweet RL. Oral contraceptives, Chlamydia trachomatis infection, and pelvic inflammatory disease: a word of caution about protection. JAMA 1985; 253:2246-50.
22. Kaushic C, Ashkar AA, Reid LA, Rosenthal KL. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 2003; 77:4558-65.
23. Smith JS, Herrero R, Munoz N, et al. Prevalence and risk factors for herpes simplex virus type 2 infection among middle-age women in Brazil and the Philippines. Sex Transm Dis 2001; 28:187-94.
24. Martin HL, Richardson BA, Nyange PM, et al. Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis 1999; 180:1863-8.
25. Ghanem KG, Shah N, Klein RS, et al. Influence of sex hormones, HIV status, and concomitant sexually transmitted infection on cervicovaginal inflammation. J Infect Dis 2005; 191:358-66.
26. Prakash M, Kapembwa MS, Gotch F, Patterson S. Oral contraceptive use induces upregulation of the CCR5 chemokine receptor on CD4(+) T cells in the cervical epithelium of healthy women. J Reprod Immunol 2002; 54:117-31.
27. Prakash M, Patterson S, Gotch F, Kapembwa MS. Ex vivo analysis of HIV-1 co-receptors at the endocervical mucosa of women using oral contraceptives. BJOG 2004; 111:1468-70.
28. Hunt JS, Miller L, Piatt JS. Hormonal regulation of uterine macrophages. Dev Immunol 1998; 6:105-10.
29. Zang YC, Halder JB, Hong J, Rivera VM, Zhang JZ. Regulatory effects of estriol on T cell migration and cytokine profile: inhibition of transcription factor NF-kappa B. J Neuroimmunol 2002; 124:106-14.
30. Gillgrass AE, Ashkar AA, Rosenthal KL, Kaushic C. Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J Virol 2003; 77:9845-51.
31. Furth PA, Westphal H, Hennighausen L. Expression from the HIV-LTR is stimulated by glucocorticoids and pregnancy. AIDS Res Hum Retroviruses 1990; 6:553-60.
32. Plummer FA, Simonsen JN, Cameron DW, et al. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J Infect Dis 1991; 163:233-9.
33. Laga M, Manoka A, Kivuvu M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS 1993; 7:95-102.
34. Saracco A, Musicco M, Nicolosi A, et al. Man-to-woman sexual transmission of HIV: longitudinal study of 343 steady partners of infected men. J Acquir Immune Defic Syndr 1993; 6:497-502.
35. Plourde PJ, Pepin J, Agoki E, et al. Human immunodeficiency virus type 1 seroconversion in women with genital ulcers. J Infect Dis 1994; 170:313-7.
36. 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; 331:341-6.
37. Bulterys M, Chao A, Habimana P, Dushimimana A, Nawrocki P, Saah A. Incident HIV-1 infection in a cohort of young women in Butare, Rwanda. AIDS 1994; 8:1585-91.
38. Weir SS, Feldblum PJ, Roddy RE, Zekeng L. Gonorrhea as a risk factor for HIV acquisition. AIDS 1994; 8:1605-8.
39. Sinei SKA, Fortney JA, Kigondu CS, et al. Contraceptive use and HIV infection in Kenyan family planning clinic attenders. Int J STD AIDS 1996; 7:65-70.
40. Ungchusak K, Rehle T, Thammapornpilap P, Spiegelman D, Brinkmann U, Siraprapasiri T. Determinants of HIV infection among female commercial sex workers in northeastern Thailand: results from a longitudinal study. J Acquir Immune Defic Syndr Hum Retrovirol 1996; 12: 500-7.
41. Martin HL Jr, Nyange PM, Richardson BA, et al. Hormonal contraception, sexually transmitted diseases, and risk of heterosexual transmission of human immunodeficiency virus type 1. J Infect Dis 1998; 178:1053-9.
42. Kilmarx PH, Limpakarnjanarat K, Mastro TD, et al. HIV-1 seroconversion in a prospective study of female sex workers in northern Thailand: continued high incidence among brothel-based women. AIDS 1998; 12:1889-98.
43. Kiddugavu M, Makumbi F, Wawer MJ, et al. Hormonal contraceptive use and HIV-1 infection in a population-based cohort in Rakai, Uganda. AIDS 2003; 17:233-40.
44. Lavreys L, Baeten JM, Martin HL Jr, et al. Hormonal contraception and risk of HIV-1 acquisition: results of a 10-year prospective study. AIDS 2004; 18:695-7.
45. Morrison CS, Richardson BA, Mmiro F, et al. Hormonal contraception and the risk of HIV acquisition. The Hormonal Contraception and the Risk of HIV (HC-HIV) Study Group. AIDS 2007; 21:85-95.
46. Wang CC, Reilly M, Kreiss JK. Risk of HIV infection in oral contraceptive pill users: a meta-analysis. J Acquir Immune Defic Syndr 1999; 21:51-8.
47. Wawer MJ, Sweankambo NK, Serwadda D, et al. Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial. Lancet 1999; 353:525-35.
48. Martin HL Jr, Jackson DJ, Mandaliya K, et al. Preparation for AIDS vaccine evaluation in Mombasa, Kenya: establishment of seronegative cohorts of commercial sex workers and trucking company employees. AIDS Res Hum Retroviruses 1994; 10(Suppl 2):S235-7.
49. Stephenson JM. Systematic review of hormonal contraception and risk of HIV transmission: when to resist meta-analysis. AIDS 1998; 12: 545-53.
50. White E, Hunt JR, Casso D. Exposure measurement in cohort studies: the challenges of prospective data collection. Epidemiol Rev 1998; 20: 43-56.
51. Sangi-Haghpeykar H, Posner SF, Poindexter AN 3rd. Consistency of condom use among low-income hormonal contraceptive users. Perspect Sex Reprod Health 2005; 37:184-91.
52. Downs AM, de Vincenzi I. Probability of heterosexual transmission of HIV: relationship to the number of unprotected sexual contacts. European Study Group in Heterosexual Transmission of HIV. J Acquir Immune Defic Syndr Hum Retrovirol 1996; 11:388-95.
53. Baeten JM, Richardson BA, Lavreys L, et al. Female-to-male infectivity of HIV-1 among circumcised and uncircumcised Kenyan men. J Infect Dis 2005; 191:546-53.
54. Kapiga SH, Shao JF, Lwihula GK, Hunter DJ. Risk factors for HIV infection among women in Dar-es-Salaam, Tanzania. J Acquir Immune Defic Syndr 1994; 7:301-9.
55. Morrison CS, Richardson BA, Celentano DD, et al. Prospective clinical trials designed to assess the use of hormonal contraceptives and risk of HIV acquisition. J Acquir Immune Defic Syndr 2005; 38:S17-8.
56. Lavreys L, Baeten JM, Kreiss JK, et al. Injectable contraceptive use and genital ulcer disease during the early phase of HIV-1 infection increase plasma virus load in women. J Infect Dis 2004; 189:303-11.
57. Schacker TW, Hughes JP, Shea T, Coombs RW, Corey L. Biological and virologic characteristics of primary HIV infection. Ann Intern Med 1998; 128:613-20.
58. Henrard DR, Phillips JF, Muenz LR, et al. Natural history of HIV-1 cell-free viremia. JAMA 1995; 274:554-8.
59. Lavreys L, Baeten JM, Chohan V, et al. Higher set point plasma viral load and more-severe acute HIV type 1 (HIV-1) illness predict mortality among high-risk HIV-1 - infected African women. Clin Infect Dis 2006; 42:1333-9.
60. Sagar M, Lavreys L, Baeten JM, et al. Identification of modifiable factors that affect the genetic diversity of the transmitted HIV-1 population. AIDS 2004; 18:615-9.
61. Sagar M, Lavreys L, Baeten JM, et al. Infection with multiple human immunodeficiency virus type 1 variants is associated with faster disease progression. J Virol 2003; 77:12921-6.
62. Gottlieb GS, Nickle DC, Jensen MA, et al. Dual HIV-1 infection associated with rapid disease progression. Lancet 2004; 363:619-22.
63. Cejtin HE, Jacobson L, Springer G, et al. Effect of hormonal contraceptive use on plasma HIV-1-RNA levels among HIV-infected women. AIDS 2003; 17:1702-4.
64. Lavreys L, Chohan V, Overbaugh J, et al. Hormonal contraception and risk of cervical infections among HIV-1-seropositive Kenyan women. AIDS 2004; 18:2179-84.
65. Anzala AO, Simonsen JN, Kimani J, et al. Acute sexually transmitted infections increase human immunodeficiency virus type 1 plasma viremia, increase plasma type 2 cytokines, and decrease CD4 cell counts. J Infect Dis 2000; 182:459-66.
66. Anzala OA, Nagelkerke NJ, Bwayo JJ, et al. Rapid progression to disease in African sex workers with human immunodeficiency virus type 1 infection. J Infect Dis 1995; 171:686-9.
67. Kilmarx PH, Limpakarnjanarat K, Kaewkungwal J, et al. Disease progression and survival with human immunodeficiency virus type 1 subtype E infection among female sex workers in Thailand. J Infect Dis 2000; 181:1598-606.
68. European Study Group on Heterosexual Transmission of HIV. Comparison of female to male and male to female transmission of HIV in 563 stable couples. BMJ 1992; 304:809-13.
69. Pedraza MA, del Romero J, Roldan F, et al. Heterosexual transmission of HIV-1 is associated with high plasma viral load levels and a positive viral isolation in the infected partner. J Acquir Immune Defic Syndr 1999; 21:120-5.
70. Baeten JM, Overbaugh J. Measuring the infectiousness of persons with HIV-1: opportunities for preventing sexual HIV-1 transmission. Curr HIV Res 2003; 1:69-86.
71. Clemetson DB, Moss GB, Willerford DM, et al. Detection of HIV DNA in cervical and vaginal secretions: prevalence and correlates among women in Nairobi, Kenya. JAMA 1993; 269:2860-4.
72. Mostad SB, Overbaugh J, DeVange DM, 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; 350:922-7.
73. Kovacs A, Wasserman SS, Burns D, et al. Determinants of HIV-1 shedding in the genital tract of women. Lancet 2001; 358:1593-601.
74. Wang CC, McClelland RS, Overbaugh J, et al. The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 2004; 18:205-9.
75. Benki S, Mostad SB, Richardson BA, Mandaliya K, Kreiss JK, Overbaugh J. Cyclic shedding of HIV-1 RNA in cervical secretions during the menstrual cycle. J Infect Dis 2004; 189:2192-201.
76. Reichelderfer PS, Coombs RW, Wright DJ, et al. Effect of menstrual cycle on HIV-1 levels in the peripheral blood and genital tract. WHS 001 Study Team. AIDS 2000; 14:2101-7.
77. McClelland RS, Wang CC, Mandaliya K, et al. Treatment of cervicitis is associated with decreased cervical shedding of HIV-1. AIDS 2001; 15:105-10.
78. Baeten JM, McClelland RS, Corey L, et al. Vitamin A supplementation and genital shedding of herpes simplex virus among HIV-1-infected women: a randomized clinical trial. J Infect Dis 2004; 189:1466-71.
79. Mbopi-Keou FX, Gresenguet G, Mayaud P, et al. Interactions between herpes simplex virus type 2 and human immunodeficiency virus type 1 infection in African women: opportunities for intervention. J Infect Dis 2000; 182:1090-6.
80. McClelland RS, Wang CC, Overbaugh J, et al. Association between cervical shedding of herpes simplex virus and HIV-1. AIDS 2002; 16: 2425-30.
81. Mostad SB, Kreiss JK, Ryncarz AJ, et al. Cervical shedding of herpes simplex virus in human immunodeficiency virus-infected women: effects of hormonal contraception, pregnancy, and vitamin A deficiency. J Infect Dis 2000; 181:58-63.
82. Cherpes TL, Melan MA, Kant JA, Cosentino LA, Meyn LA, Hillier SL. Genital tract shedding of herpes simplex virus type 2 in women: effects of hormonal contraception, bacterial vaginosis, and vaginal group B Streptococcus colonization. Clin Infect Dis 2005; 40:1422-8.
83. McClelland RS, Wang CC, Richardson BA, et al. A prospective study of hormonal contraceptive use and cervical shedding of herpes simplex virus in human immunodeficiency virus type 1 - seropositive women. J Infect Dis 2002; 185:1822-5.
84. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20:73-83.
85. Mingjia L, Short R. How oestrogen or progesterone might change a woman's susceptibility to HIV-1 infection. Aust N Z J Obstet Gynaecol 2002; 42:472-5.
86. World Health Organization (WHO). Hormonal contraception and HIV: science and policy. Available at: http://www.who.int/reproductive-health/stis/hc_hiv/ nairobi_statement.pdf. Accessed 1 May 2006.
87. Balkus J, Bosire R, John-Stewart G, et al. High uptake of postpartum hormonal contraception among HIV-1-seropositive women in Kenya. Sex Transm Dis 2007; 34:25-9.
88. World Health Organization (WHO). Prevention of HIV in infants and young children: review of evidence and WHO's activities. Available at: http://www.who.int/hiv/mtct/ReviewofEvidence.pdf. Accessed 13 September 2006.
89. World Health Organization (WHO). Medical eligibility criteria for contraceptive use: Available at: http://www.who.int/reproductive-health/ publications/mec/mec.pdf. Accessed 14 September 2006.