Hormonal contraceptive use and female-to-male HIV transmission: A systematic review of the epidemiologic evidence

AIDS

Volumn 27, Issue 4, 2013, Pages 493-505

  Polis, Chelsea B ^a   Phillips, Sharon J ^b   Curtis, Kathryn M ^c  

^a UNITED STATES AGENCY FOR INTERNATIONAL DEVELOPMENT   (United States)

^b WORLD HEALTH ORGANIZATION   (Switzerland)

^c NATIONAL CENTER FOR CHRONIC DISEASE PREVENTION AND HEALTH PROMOTION   (United States)

Author keywords

contraception; female to male HIV transmission; HIV; hormonal; prevention of mother to child transmission

Indexed keywords

CONTRACEPTIVE AGENT; INJECTABLE CONTRACEPTIVE AGENT; LEVONORGESTREL; ORAL CONTRACEPTIVE AGENT; VIRUS RNA;

CONDOM; EVIDENCE BASED MEDICINE; FEMALE GENITAL SYSTEM; HORMONAL CONTRACEPTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; ORAL CONTRACEPTION; PRIORITY JOURNAL; REVIEW; SEROCONVERSION; SEXUAL TRANSMISSION; SYSTEMATIC REVIEW; UTERINE CERVIX CYTOLOGY; VAGINA SMEAR; VIRUS DETECTION; VIRUS LOAD; VIRUS SHEDDING; VIRUS TRANSMISSION;

ADULT; ANTI-HIV AGENTS; CONTRACEPTIVES, ORAL, HORMONAL; DRUG INTERACTIONS; EVIDENCE-BASED MEDICINE; FEMALE; HIV SERONEGATIVITY; HIV SEROPOSITIVITY; HUMANS; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; MALE; ODDS RATIO; PREGNANCY; REPRODUCTIVE BEHAVIOR; REPRODUCTIVE HEALTH; UNITED STATES; VIRAL LOAD; VIRUS SHEDDING;

EID: 84873411250     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835ad539     Document Type: Review

References (83)

1. World Health Organization. Review of Priorities in Research on Hormonal Contraception and IUDs and HIV Infection: Report of a Technical Meeting. 13-15 March 2007. Geneva, Switzerland.
2. Curtis KM, Nanda K, Kapp N. Safety of hormonal and intrauterine methods of contraception for women with HIV/AIDS: a systematic review. AIDS 2009; 23:S55-S67.
3. Morrison CS, TurnerAN, Jones LB. Highly effective contraception and acquisition of HIV and other sexually transmitted infections. Best Pract Res Clin Obstet Gynaecol 2009; 23:263-284.
4. El-Ibiary SY, Cocohoba JM. Effects of HIV antiretrovirals on the pharmacokinetics of hormonal contraceptives. Eur J Contracept Reprod Healthcare 2008; 13:123-132.
5. Kancheva Landolt NT, Lakhonphon S, Ananworanich J. Contraception in HIV-positive female adolescents. AIDS Res Ther 2011; 8:19.
6. Blish CA, Baeten JM. Hormonal contraception and HIV-1 transmission. Am J Reprod Immunol 2011; 65:302-307.
7. Baeten JM, Kahle E, Lingappa JR, Coombs RW, Delany-Moretlwe S, Nakku-Joloba E, et al. Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med 2011; 3:77ra29.
8. Hel Z, Stringer E, Mestecky J. Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 2010; 31:79-97.
9. Mati JK, Hunter DJ, Maggwa BN, Tukei PM. Contraceptive use and the risk of HIV infection in Nairobi, Kenya. Int J Gynaecol Obstet 1995; 48:61-67.
10. Critchlow CW, Wolner-Hanssen P, Eschenbach DA, Kiviat NB, Koutsky LA, Stevens CE, et al. Determinants of cervical ectopia and of cervicitis: age, oral contraception, specific cervical infection, smoking, and douching. Am J Obstet Gynecol 1995; 173:534-543.
11. Clemetson DB, Moss GB, Willerford DM, Hensel M, Emonyi W, Holmes KK, et al. Detection of HIVDNAin cervical and vaginal secretions. Prevalence and correlates among women in Nairobi, Kenya. JAMA 1993; 269:2860-2864.
12. Tanton C, Weiss HA, Le Goff J, Changalucha J, Rusizoka M, Baisley K, et al. Correlates of HIV-1 genital shedding in Tanzanian women. PLoS One 2011; 6:e17480.
13. Mostad SB, Overbaugh J, DeVange DM, Welch MJ, Chohan B, Mandaliya K, 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; 350:922-927.
14. Ghys PD, Fransen K, Diallo MO, Ettiegne-Traore V, Coulibaly IM, Yeboue KM, et al. The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Cote d'Ivoire. AIDS 1997; 11:F85-F93.
15. Kovacs A, Wasserman SS, Burns D, Wright DJ, Cohn J, Landay A, et al. Determinants of HIV-1 shedding in the genital tract of women. Lancet 2001; 358:1593-1601.
16. Kreiss J, Willerford DM, Hensel M, Emonyi W, Plummer F, Ndinya-Achola J, et al. Association between cervical inflammation and cervical shedding of human immunodeficiency virus DNA. J Infect Dis 1994; 170:1597-1601.
17. Morrison CS, Demers K, Kwok C, Bulime S, Rinaldi A, Munjoma M, et al. Plasma and cervical viral loads among Ugandan and Zimbabwean women during acute and early HIV-1 infection. AIDS 2010; 24:573-582.
18. Henin Y, Mandelbrot L, Henrion R, Pradinaud R, Coulaud JP, Montagnier L. Virus excretion in the cervicovaginal secretions of pregnant and nonpregnant HIV-infected women. J Acquir Immune Defic Syndr 1993; 6:72-75.
19. Gardella B, Roccio M, Maccabruni A, Mariani B, Panzeri L, Zara F, et al. HIV shedding in cervico-vaginal secretions in pregnant women. Curr HIV Res 2011; 9:313-320.
20. Mugo NR, Heffron R, Donnell D, Wald A, Were EO, Rees H, et al. Increased risk of HIV-1 transmission in pregnancy: a prospective study among African HIV-1-serodiscordant couples. AIDS 2011; 25:1887-1895.
21. Ghanem KG, Shah N, Klein RS, Mayer KH, Sobel JD, Warren DL, et al. Influence of sex hormones, HIV status, and concomitant sexually transmitted infection on cervicovaginal inflammation. J Infect Dis 2005; 191:358-366.
22. Johnson LF, Lewis DA. The effect of genital tract infections on HIV-1 shedding in the genital tract: a systematic review and meta-analysis. Sex Transm Dis 2008; 35:946-959.
23. Rotchford K, Strum AW, Wilkinson D. Effect of coinfection with STDs and of STD treatment on HIV shedding in genital-tract secretions: systematic review and data synthesis. Sex Transm Dis 2000; 27:243-248.
24. Ward H, Ronn M. Contribution of sexually transmitted infections to the sexual transmission of HIV. Curr Opin HIV AIDS 2010; 5:305-310.
25. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000; 342:921-929.
26. Attia S, Egger M, Muller M, Zwahlen M, Low N. Sexual transmission of HIV according to viral load and antiretroviral therapy: systematic review and meta-analysis. AIDS 2009; 23:1397-1404.
27. Glujovsky D, Bardach A, García Martí S, Comandé D, Ciapponi A. EROS: A new software for early stage of systematic reviews. Value in Health 2011; 14:A564.
28. Egger M, Smith GD, Schneider M. Systematic reviews of observational studies. In: Egger M, Smith GD, Altman DG, editors. Systematic reviews in healthcare: meta-analysis in context. London: BMJ Publishing Group; 2001. pp. 211-227.
29. Cushman LF, Romero D, Kalmuss D, Davidson AR, Heartwell S, Rulin M. Condom use among women choosing longterm hormonal contraception. Fam Plann Persp 1998; 30: 240-243.
30. Sangi-Haghpeykar H, Posner SF, Poindexter AN 3rd. Consistency of condom use among low-income hormonal contraceptive users. Perspect Sex Reprod Health 2005; 37:184-191.
31. Polis CB, Gray RH, Lutalo T, Nalugoda F, Kagaayi J, Kigozi G, et al. Trends and correlates of hormonal contraceptive use among HIV-infected women in Rakai, Uganda, 1994-2006. Contraception 2011; 83:549-555.
32. Morrison CS, Richardson BA, Mmiro F, Chipato T, Celentano DD, Luoto J, et al. Hormonal contraception and the risk of HIV acquisition. AIDS 2007; 21:85-95.
33. Robins JM, Hernan MA, Brumback B. Marginal structural models and causal inference in epidemiology. Epidemiology 2000; 11:550-560.
34. Hernan MA, Brumback B, Robins JM. Marginal structural models to estimate the causal effect of zidovudine on the survival of HIV-positive men. Epidemiology 2000; 11:561-570.
35. Cole SR, Hernan MA, Robins JM, Anastos K, Chmiel J, Detels R, et al. Effect of highly active antiretroviral therapy on time to acquired immunodeficiency syndrome or death using marginal structural models. Am J Epidemiol 2003; 158:687-694.
36. Gallo MF, Sobel JD, Rompalo AM, Cu-Uvin S, Schoenbaum E, Jamieson DJ. Discordance between spermatozoa detection and self-reported semen exposure. Sex Transm Dis 2011; 38:909- 912.
37. Minnis AM, Steiner MJ, Gallo MF, Warner L, Hobbs MM, van der Straten A, et al. Biomarker validation of reports of recent sexual activity: results of a randomized controlled study in Zimbabwe. Am J Epidemiol 2009; 170:918-924.
38. Catania JA, Gibson DR, Chitwood DD, Coates TJ. Methodological problems in AIDS behavioral research: influences on measurement error and participation bias in studies of sexual behavior. Psychol Bull 1990; 108:339-362.
39. Magwali TL, Steiner MJ, Toms H, Brown JM. How are condoms used in a family planning setting: evidence from Zimbabwe. Cent Afr J Med 2005; 51:79-84.
40. Aklilu M,Messele T, Tsegaye A, Biru T,MariamDH, van Benthem B, et al. Factors associated with HIV-1 infection among sex workers of Addis Ababa, Ethiopia. AIDS 2001; 15:87-96.
41. Callegari L, Harper CC, van der Straten A, Kamba M, Chipato T, Padian NS. Consistent condom use in married Zimbabwean women after a condom intervention. Sex Transm Dis 2008; 35:624-630.
42. Van Rossem R, Meekers D, Akinyemi Z. Consistent condom use with different types of partners: evidence from two Nigerian surveys. AIDS Educ Prev 2001; 13:252-267.
43. Goodman SN. Toward evidence-based medical statistics. 1: The P value fallacy. Ann Intern Med 1999; 130:995-1004.
44. Anderson BL, Cu-Uvin S. Determinants of HIV shedding in the lower genital tract of women. Curr Infect Dis Rep 2008; 10:505-511.
45. Coombs RW, Reichelderfer PS, Landay AL. Recent observations on HIV type-1 infection in the genital tract of men and women. AIDS 2003; 17:455-480.
46. Cu-Uvin S, Delong AK, Venkatesh KK, Hogan JW, Ingersoll J, Kurpewski J, et al. Genital tract HIV-1 RNA shedding among women with below detectable plasma viral load. AIDS 2010; 24:2489-2497.
47. Larke NL, Weiss HA, Mayaud P, Van de Perre P, Clayton T, Ouedraogo A, et al. Design of epidemiological studies measuring genital and plasma HIV-1 outcomes: lessons from a randomised controlled trial. Trop Med Int Health 2009; 14:267-275.
48. Coombs RW, Wright DJ, Reichelderfer PS, Burns DN, Cohn J, Cu-Uvin S, et al. Variation of human immunodeficiency virus type 1 viral RNA levels in the female genital tract: implications for applying measurements to individual women. J Infect Dis 2001; 184:1187-1191.
49. Duerr A, Curtis K, Shelton JD, Meirik O. Hormonal contraception and genital-tract shedding of HIV-1-infected cells. Lancet 1998; 351:294-295.
50. Mitchell C, Paul K, Agnew K, Gaussman R, Coombs RW, Hitti J. Estimating volume of cervicovaginal secretions in cervicovaginal lavage fluid collected for measurement of genital HIV-1 RNA levels in women. J Clin Microbiol 2011; 49:735-736.
51. Dezzutti CS, Hendrix CW, Marrazzo JM, Pan Z, Wang L, Louissaint N, et al. Performance of swabs, lavage, and diluents to quantify biomarkers of female genital tract soluble mucosal mediators. PLoS One 2011; 6:e23136.
52. Delany S, Rosas R, Mlaba N, Clayton T, Akpomiemie G, LeGoff J, et al. Comparison of cervicovaginal lavage, cervicovaginal lavage enriched with cervical swab, and vaginal tampon for the detection of HIV-1 RNA and HSV-2DNAin genital secretions. J Acquir Immune Defic Syndr 2008; 49:406-409.
53. Baeten JM, Overbaugh J. Measuring the infectiousness of persons with HIV-1: opportunities for preventing sexual HIV-1 transmission. Current HIV Res 2003; 1:69-86.
54. 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.
55. European Study Group on Heterosexual Transmission of HIV. Comparison of female to male and male to female transmission of HIV in 563 stable couples. European Study Group on Heterosexual Transmission of HIV. BMJ 1992; 304:809-813.
56. Wang CC, McClelland RS, Overbaugh J, Reilly M, Panteleeff DD, Mandaliya K, et al. The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 2004; 18:205-209.
57. Heikinheimo O, Lehtovirta P, Suni J, Paavonen J. The levonorgestrel- releasing intrauterine system (LNG-IUS) in HIV-infected women-effects on bleeding patterns, ovarian function and genital shedding of HIV. Hum Reprod 2006; 21:2857- 2861.
58. Heikinheimo O, Lehtovirta P, Aho I, Ristola M, Paavonen J. The levonorgestrel-releasing intrauterine system in human immunodeficiency virus-infected women: a 5-year follow-up study. Am J Obstet Gynecol 2011; 204:126e121-126e124.
59. Richardson BA, Morrison CS, Sekadde-Kigondu C, Sinei SK, Overbaugh J, Panteleeff DD, et al. Effect of intrauterine device use on cervical shedding of HIV-1 DNA. AIDS 1999; 13:2091- 2097.
60. Heffron R, Donnell D, Rees H, Celum C, Mugo N, Were E, et al. Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect Dis 2012; 12:19-26.
61. Seck K, Samb N, Tempesta S, Mulanga-Kabeya C, Henzel D, Sow PS, et al. Prevalence and risk factors of cervicovaginal HIV shedding among HIV-1 and HIV-2 infected women in Dakar, Senegal. Sex Transm Infect 2001; 77:190-193.
62. Clark RA, Theall KP, Amedee AM, Dumestre J, Wenthold L, Kissinger PJ. Lack of association between genital tract HIV-1 RNA shedding and hormonal contraceptive use in a cohort of Louisiana women. Sex Transm Dis 2007; 34:870-872.
63. Graham SM, Masese L, Gitau R, Jalalian-Lechak Z, Richardson BA, Peshu N, et al. Antiretroviral adherence and development of drug resistance are the strongest predictors of genital HIV-1 shedding among women initiating treatment. J Infect Dis 2010; 202:1538-1542.
64. Roccio M, Gardella B, Maserati R, Zara F, Iacobone D, Spinillo A. Low-dose combined oral contraceptive and cervicovaginal shedding of human immunodeficiency virus. Contraception 2011; 83:564-570.
65. Cejtin HE, Lisa JB, Springer C, Watts DH, Levine A, Greenblatt R, et al. Effect of hormonal contraceptive use on plasma HIV-1- RNA levels among HIV-infected women. AIDS 2003; 17:1702- 1704.
66. Richardson BA, Otieno PA, Mbori-Ngacha D, Overbaugh J, Farquhar C, John-Stewart GC. Hormonal contraception and HIV-1 disease progression among postpartum Kenyan women. AIDS 2007; 21:749-753.
67. Sagar M, Lavreys L, Baeten JM, Richardson BA, Mandaliya K, Ndinya-Achola JO, et al. Identification of modifiable factors that affect the genetic diversity of the transmitted HIV-1 population. AIDS 2004; 18:615-619.
68. Polis CB, Gray RH, Bwanika JB, Kigozi G, Kiwanuka N, Nalugoda F, et al. Effect of hormonal contraceptive use before HIV seroconversion on viral load setpoint among women in Rakai, Uganda. J Acquir Immune Defic Syndr 2011; 56:125-130.
69. Kumwenda JJ, Makanani B, Taulo F, Nkhoma C, Kafulafula G, Li Q, et al. Natural history and risk factors associated with early and established HIV type 1 infection among reproductive-age women in Malawi. Clin Infect Dis 2008; 46:1913-1920.
70. Lavreys L, Baeten JM, Kreiss JK, Richardson BA, Chohan BH, Hassan W, 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; 189:303-311.
71. McNutt LA, Wu C, Xue X, Hafner JP. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am J Epidemiol 2003; 157:940-943.
72. Singh SD, J.E. Adding it up: costs and benefits of contraceptive services - Estimates for 2012. New York: Guttmacher Institute and United Nations Population Fund (UNFPA); 2012.
73. Shulman LP. The state of hormonal contraception today: benefits and risks of hormonal contraceptives: combined estrogen and progestin contraceptives. Am J Obstet Gynecol 2011; 205:S9-13.
74. Burke AE. The state of hormonal contraception today: benefits and risks of hormonal contraceptives: progestin-only contraceptives. Am J Obstet Gynecol 2011; 205:S14-S17.
75. Johnson KB, Akwara P, Rutstein SO, Bernstein S. Fertility preferences and the need for contraception among women living with HIV: the basis for a joint action agenda. AIDS 2009; 23 (Suppl 1):S7-S17.
76. Reynolds HW, Janowitz B, Homan R, Johnson L. The value of contraception to prevent perinatal HIV transmission. Sex Transm Dis 2006; 33:350-356.
77. Reynolds HW, Janowitz B, Wilcher R, Cates W. Contraception to prevent HIV-positive births: current contribution and potential cost savings in PEPFAR countries. Sex Transm Infect 2008; 84 (Suppl 2):ii49-ii53.
78. Reynolds HW, Steiner MJ, Cates W Jr. Contraception's proved potential to fight HIV. Sex Trans Infect 2005; 81:184-185.
79. Halperin DT, Stover J, Reynolds HW. Benefits and costs of expanding access to family planning programs to women living with HIV. AIDS 2009; 23 (Suppl 1):S123-S130.
80. Hladik W, Stover J, Esiru G, Harper M, Tappero J. The contribution of family planning towards the prevention of vertical HIV transmission in Uganda. PLoS One 2009; 4:e7691.
81. Mahy M, Stover J, Kiragu K, Hayashi C, Akwara P, Luo C, et al. What will it take to achieve virtual elimination of mother-tochildtransmission ofHIV?Anassessment of current progress and future needs. Sex Transm Infect 2010; 86 (Suppl 2):ii48-ii55.
82. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med 2011; 365:493-505.
83. Anglemyer A, Rutherford GW, Baggaley RC, Egger M, Siegfried N. Antiretroviral therapy for prevention of HIV transmission in HIV-discordant couples. Cochrane Database Syst Rev 2011: CD009153.