Abstract
Sex steroids are central to regulation of the dual roles of the female reproductive tract: support of reproduction and protection against deleterious pathogen invasion. The mechanisms by which sex steroids orchestrate the balance between reproduction and protection against pathogenic microorganisms, however, are complex and poorly understood. Epidemiologic studies have revealed associations between sex steroids and diagnosis, shedding, transmission of sexually transmitted diseases and their clinical sequelae, as well as disruptions to the normal vaginal flora. Experimental approaches, including animal models, have provided some insight into the mechanism of these associations, though often with contradictory results. Inherent limitations in traditional approaches to understanding the physiology of sex steroid regulation of immunity in the female genital tract will require significant interdisciplinary collaboration.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Al-Harthi L, Wright DJ, Anderson D, Cohen M, Matity Ahu D, Cohn J, Cu-Unvin S, Burns D, Reichelderfer P, Lewis S, Beckner S, Kovacs A, Landay A (2000) The impact of the ovulatory cycle on cytokine production: evaluation of systemic, cervicovaginal, and salivary compartments. J Interferon Cytokine Res 20(8):719–724
Appleby P, Beral V, Berrington de Gonzalez A, Colin D, Franceschi S, Goodhill A, Green J, Peto J, Plummer M, Sweetland S (2007) Cervical cancer and hormonal contraceptives: collaborative reanalysis of individual data for 16, 573 women with cervical cancer and 35, 509 women without cervical cancer from 24 epidemiological studies. Lancet 370(9599):1609–1621
Asin SN, Heimberg AM, Eszterhas SK, Rollenhagen C, Howell AL (2008) Estradiol and progesterone regulate HIV type 1 replication in peripheral blood cells. AIDS Res Hum Retroviruses 24(5):701–716
Baeten JM, Benki S, Chohan V, Lavreys L, McClelland RS, Mandaliya K, Ndinya-Achola JO, Jaoko W, Overbaugh J (2007) Hormonal contraceptive use, herpes simplex virus infection, and risk of HIV-1 acquisition among Kenyan women. AIDS 21(13):1771–1777
Baeten JM, Nyange PM, Richardson BA, Lavreys L, Chohan B, Martin HL Jr, Mandaliya K, Ndinya-Achola JO, Bwayo JJ, Kreiss JK (2001) Hormonal contraception and risk of sexually transmitted disease acquisition: results from a prospective study. Am J Obstet Gynecol 185(2):380–385
Banura C, Franceschi S, Doorn LJ, Arslan A, Wabwire-Mangen F, Mbidde EK, Quint W, Weiderpass E (2008) Infection with human papillomavirus and HIV among young women in Kampala, Uganda. J Infect Dis 197(4):555–562
Bauters TG, Dhont MA, Temmerman MI, Nelis HJ (2002) Prevalence of vulvovaginal candidiasis and susceptibility to fluconazole in women. Am J Obstet Gynecol 187(3):569–574
Beigi RH, Meyn LA, Moore DM, Krohn MA, Hillier SL (2004) Vaginal yeast colonization in nonpregnant women: a longitudinal study. Obstet Gynecol 104(5 Pt 1):926–930
Benki S, Mostad SB, Richardson BA, Mandaliya K, Kreiss JK, Overbaugh J (2004) Cyclic shedding of HIV-1 RNA in cervical secretions during the menstrual cycle. J Infect Dis 189(12):2192–2201
Black CA, Rohan LC, Cost M, Watkins SC, Draviam R, Alber S, Edwards RP (2000) Vaginal mucosa serves as an inductive site for tolerance. J Immunol 165(9):5077–5083
Bose SK, Goswami PC (1986) Enhancement of adherence and growth of Chlamydia trachomatis by estrogen treatment of HeLa cells. Infect Immun 53(3):646–650
Brabin L, Fairbrother E, Mandal D, Roberts SA, Higgins SP, Chandiok S, Wood P, Barnard G, Kitchener HC (2005) Biological and hormonal markers of chlamydia, human papillomavirus, and bacterial vaginosis among adolescents attending genitourinary medicine clinics. Sex Transm Infect 81(2):128–132
Brake T, Lambert PF (2005) Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc Natl Acad Sci USA 102(7):2490–2495
Brunham RC, Martin DH, Hubbard TW, Kuo CC, Critchlow CW, Cles LD, Eschenbach DA, Holmes KK (1983) Depression of the lymphocyte transformation response to microbial antigens and to phytohemagglutinin during pregnancy. J Clin Invest 72(5):1629–1638
Castle PE, Hildesheim A, Bowman FP, Strickler HD, Walker JL, Pustilnik T, Edwards RP, Crowley-Nowick PA (2002) Cervical concentrations of interleukin-10 and interleukin-12 do not correlate with plasma levels. J Clin Immunol 22(1):23–27
Cauci S, Culhane JF (2007) Modulation of vaginal immune response among pregnant women with bacterial vaginosis by Trichomonas vaginalis, Chlamydia trachomatis, Neisseria gonorrhoeae, and yeast. Am J Obstet Gynecol 196(2):133 e1-7
Cetin M, Ocak S, Gungoren A, Hakverdi AU (2007) Distribution of Candida species in women with vulvovaginal symptoms and their association with different ages and contraceptive methods. Scand J Infect Dis 39(6–7):584–588
Chen YH, Huang LH, Chen TM (1996) Differential effects of progestins and estrogens on long control regions of human papillomavirus types 16 and 18. Biochem Biophys Res Commun 224(3):651–659
Chipperfield EJ, Evans BA (1975) Effect of local infection and oral contraception on immunoglobulin levels in cervical mucus. Infect Immun 11(2):215–221
Clemetson DB, Moss GB, Willerford DM, Hensel M, Emonyi W, Holmes KK, Plummer F, Ndinya-Achola J, Roberts PL, Hillier S et al (1993) Detection of HIV DNA in cervical and vaginal secretions. Prevalence and correlates among women in Nairobi, Kenya. JAMA 269(22):2860–2864
Cotch MF, Hillier SL, Gibbs RS, Eschenbach DA (1998) Epidemiology and outcomes associated with moderate to heavy Candida colonization during pregnancy. Vaginal Infections and Prematurity Study Group. Am J Obstet Gynecol 178(2):374–380
Critchlow CW, Wolner-Hanssen P, Eschenbach DA, Kiviat NB, Koutsky LA, Stevens CE, Holmes KK (1995) Determinants of cervical ectopia and of cervicitis: age, oral contraception, specific cervical infection, smoking, and douching. Am J Obstet Gynecol 173(2):534–543
Crowley T, Horner P, Hughes A, Berry J, Paul I, Caul O (1997) Hormonal factors and the laboratory detection of Chlamydia trachomatis in women: implications for screening? Int J STD AIDS 8(1):25–31
Cu-Uvin S (2005) Effect of the menstrual cycle on virological parameters. J Acquir Immune Defic Syndr 38(Suppl 1):S33–S34
Daniels W, Glover DD, Essmann M, Larsen B (2001) Candidiasis during pregnancy may result from isogenic commensal strains. Infect Dis Obstet Gynecol 9(2):65–73
de Roda Husman AM, Walboomers JM, Hopman E, Bleker OP, Helmerhorst TM, Rozendaal L, Voorhorst FJ, Meijer CJ (1995) HPV prevalence in cytomorphologically normal cervical scrapes of pregnant women as determined by PCR: the age-related pattern. J Med Virol 46(2):97–102
Demes P, Gombosova A, Valent M, Fabusova H, Janoska A (1988a) Fewer Trichomonas vaginalis organisms in vaginas of infected women during menstruation. Genitourin Med 64(1):22–24
Demes P, Gombosova A, Valent M, Janoska A, Fabusova H, Petrenko M (1988b) Differential susceptibility of fresh Trichomonas vaginalis isolates to complement in menstrual blood and cervical mucus. Genitourin Med 64(3):176–179
Donders GG, Vereecken A, Bosmans E, Spitz B (2003) Vaginal cytokines in normal pregnancy. Am J Obstet Gynecol 189(5):1433–1438
Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, Markowitz LE (2007) Prevalence of HPV infection among females in the United States. JAMA 297:813
Eschenbach DA, Thwin SS, Patton DL, Hooton TM, Stapleton AE, Agnew K, Winter C, Meier A, Stamm WE (2000) Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis 30(6):901–907
Fairley CK, Robinson PM, Chen S, Tabrizi SN, Garland SM (1994) The detection of HPV DNA, the size of tampon specimens and the menstrual cycle. Genitourin Med 70(3):171–174
Farzadegan H, Hoover DR, Astemborski J, Lyles CM, Margolick JB, Markham RB, Quinn TC, Vlahov D (1998) Sex differences in HIV-1 viral load and progression to AIDS. Lancet 352(9139):1510–1514
Fidel PL Jr, Cutright J, Steele C (2000) Effects of reproductive hormones on experimental vaginal candidiasis. Infect Immun 68(2):651–657
Fife KH, Katz BP, Brizendine EJ, Brown DR (1999) Cervical human papillomavirus deoxyribonucleic acid persists throughout pregnancy and decreases in the postpartum period. Am J Obstet Gynecol 180(5):1110–1114
Fox H (1988) Fewer Trichomonas vaginalis organisms in vaginas of infected women during menstruation. Genitourin Med 64(4):280
FUTURE II Study Group (2007) Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 356(19):1915–1927
Garland SM, Hernandez-Avila M, Wheeler CM, Perez G, Harper DM, Leodolter S, Tang GW, Ferris DG, Steben M, Bryan J, Taddeo FJ, Railkar R, Esser MT, Sings HL, Nelson M, Boslego J, Sattler C, Barr E, Koutsky LA (2007) Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 356(19):1928–1943
Geiger AM, Foxman B (1996) Risk factors for vulvovaginal candidiasis: a case-control study among university students. Epidemiology 7(2):182–187
Geisler WM, James AB (2008) Chlamydial and gonococcal infections in women seeking pregnancy testing at family-planning clinics. Am J Obstet Gynecol 198(5):502 e1-4
Ghanem KG, Shah N, Klein RS, Mayer KH, Sobel JD, Warren DL, Jamieson DJ, Duerr AC, Rompalo AM (2005) Influence of sex hormones, HIV status, and concomitant sexually transmitted infection on cervicovaginal inflammation. J Infect Dis 191(3):358–366
Gillgrass AE, Ashkar AA, Rosenthal KL, Kaushic C (2003) Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J Virol 77(18):9845–9851
Gillgrass AE, Fernandez SA, Rosenthal KL, Kaushic C (2005a) Estradiol regulates susceptibility following primary exposure to genital herpes simplex virus type 2, while progesterone induces inflammation. J Virol 79(5):3107–3116
Gillgrass AE, Tang VA, Towarnicki KM, Rosenthal KL, Kaushic C (2005b) Protection against genital herpes infection in mice immunized under different hormonal conditions correlates with induction of vagina-associated lymphoid tissue. J Virol 79(5):3117–3126
Gorgos L, Fine D, Marrazzo J (2008) Chlamydia positivity in American Indian/Alaska native women screened in family planning clinics, 1997–2004. Sex Transm Dis 35(8):753–757
Gravitt P, Hildesheim A, Herrero R, Schiffman M, Sherman M, Bratti M, Rodriguez A, Morera L, Cardenas F, Bowman F, Shah K, Crowley-Nowick P (2003) Correlates of IL-10 and IL-12 concentrations in cervical secretions. J Clin Immunol 23(3):175–183
Green J, Berrington de Gonzalez A, Smith JS, Franceschi S, Appleby P, Plummer M, Beral V (2003) Human papillomavirus infection and use of oral contraceptives. Br J Cancer 88(11):1713–1720
Grigoriou O, Baka S, Makrakis E, Hassiakos D, Kapparos G, Kouskouni E (2006) Prevalence of clinical vaginal candidiasis in a university hospital and possible risk factors. Eur J Obstet Gynecol Reprod Biol 126(1):121–125
Harlow SD, Ephross SA (1995) Epidemiology of menstruation and its relevance to women’s health. Epidemiol Rev 17(2):265–286
Harper DM, Longacre MR, Noll WW, Belloni DR, Cole BF (2003) Factors affecting the detection rate of human papillomavirus. Ann Fam Med 1(4):221–227
Henin Y, Mandelbrot L, Henrion R, Pradinaud R, Coulaud JP, Montagnier L (1993) Virus excretion in the cervicovaginal secretions of pregnant and nonpregnant HIV-infected women. J Acquir Immune Defic Syndr 6(1):72–75
Hernandez-Giron C, Smith JS, Lorincz A, Lazcano E, Hernandez-Avila M, Salmeron J (2005) High-risk human papillomavirus detection and related risk factors among pregnant and nonpregnant women in Mexico. Sex Transm Dis 32(10):613–618
Hildesheim A, Schiffman MH, Gravitt PE, Glass AG, Greer CE, Zhang T, Scott DR, Rush BB, Lawler P, Sherman ME et al (1994) Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis 169(2):235–240
Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338(7):423–428
International Collaboration of Epidemiological Studies of Cervical Cancer (2006) Cervical carcinoma and reproductive factors: collaborative reanalysis of individual data on 16, 563 women with cervical carcinoma and 33, 542 women without cervical carcinoma from 25 epidemiological studies. Int J Cancer 119(5):1108–1124
Jacobson DL, Peralta L, Farmer M, Graham NM, Gaydos C, Zenilman J (2000) Relationship of hormonal contraception and cervical ectopy as measured by computerized planimetry to chlamydial infection in adolescents. Sex Transm Dis 27(6):313–319
Johansson EL, Wassen L, Holmgren J, Jertborn M, Rudin A (2001) Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infect Immun 69(12):7481–7486
Johnson HL, Erbelding EJ, Zenilman JM, Ghanem KG (2007) Sexually transmitted diseases and risk behaviors among pregnant women attending inner city public sexually transmitted diseases clinics in Baltimore, MD, 1996–2002. Sex Transm Dis 34(12):991–994
Kaushic C, Ashkar AA, Reid LA, Rosenthal KL (2003) Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 77(8):4558–4565
Kemp EA, Hakenewerth AM, Laurent SL, Gravitt PE, Stoerker J (1992) Human papillomavirus prevalence in pregnancy. Obstet Gynecol 79(5 ( Pt 1)):649–656
Kortekangas-Savolainen O, Vuorinen T (2007) Trends in herpes simplex virus type 1 and 2 infections among patients diagnosed with genital herpes in a Finnish sexually transmitted disease clinic, 1994–2002. Sex Transm Dis 34(1):37–40
Kreiss J, Willerford DM, Hensel M, Emonyi W, Plummer F, Ndinya-Achola J, Roberts PL, Hoskyn J, Hillier S, Kiviat N (1994) Association between cervical inflammation and cervical shedding of human immunodeficiency virus DNA. J Infect Dis 170(6):1597–1601
Kutteh WH, Franklin RD (2001) Quantification of immunoglobulins and cytokines in human cervical mucus during each trimester of pregnancy. Am J Obstet Gynecol 184(5):865–872 discussion 872-4
Kutteh WH, Moldoveanu Z, Mestecky J (1998) Mucosal immunity in the female reproductive tract: correlation of immunoglobulins, cytokines, and reproductive hormones in human cervical mucus around the time of ovulation. AIDS Res Hum Retroviruses 14(Suppl 1):S51–S55
Larsen B, Galask RP (1984) Influence of estrogen and normal flora on vaginal candidiasis in the rat. J Reprod Med 29(12):863–868
Lavreys L, Chohan V, Overbaugh J, Hassan W, McClelland RS, Kreiss J, Mandaliya K, Ndinya-Achola J, Baeten JM (2004) Hormonal contraception and risk of cervical infections among HIV-1-seropositive Kenyan women. AIDS 18(16):2179–2184
Louv WC, Austin H, Perlman J, Alexander WJ (1989) Oral contraceptive use and the risk of chlamydial and gonococcal infections. Am J Obstet Gynecol 160(2):396–402
MacDonald EM, Savoy A, Gillgrass A, Fernandez S, Smieja M, Rosenthal KL, Ashkar AA, Kaushic C (2007) Susceptibility of human female primary genital epithelial cells to herpes simplex virus, type-2 and the effect of TLR3 ligand and sex hormones on infection. Biol Reprod 77(6):1049–1059
Maffei CM, Paula CR, Mazzocato TS, Franceschini S (1997) Phenotype and genotype of Candida albicans strains isolated from pregnant women with recurrent vaginitis. Mycopathologia 137(2):87–94
Mahmoud EA, Hamad EE, Olsson SE, Mardh PA (1994) Antichlamydial activity of cervical secretion in different phases of the menstrual cycle and influence of hormonal contraceptives. Contraception 49(3):265–274
Maslow AS, Davis CH, Choong J, Wyrick PB (1988) Estrogen enhances attachment of Chlamydia trachomatis to human endometrial epithelial cells in vitro. Am J Obstet Gynecol 159(4):1006–1014
McClelland RS (2005) Effect of exogenous hormones. J Acquir Immune Defic Syndr 38(Suppl 1):S38–S39
McClelland RS, Wang CC, Richardson BA, Corey L, Ashley RL, Mandaliya K, Ndinya-Achola J, Bwayo JJ, Kreiss JK (2002) 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 185(12):1822–1825
Mohllajee AP, Curtis KM, Martins SL, Peterson HB (2006) Hormonal contraceptive use and risk of sexually transmitted infections: a systematic review. Contraception 73(2):154–165
Molano M, Meijer CJ, Weiderpass E, Arslan A, Posso H, Franceschi S, Ronderos M, Munoz N, van den Brule AJ (2005) The natural course of Chlamydia trachomatis infection in asymptomatic Colombian women: a 5-year follow-up study. J Infect Dis 191(6):907–916
Morrison CS, Bright P, Wong EL, Kwok C, Yacobson I, Gaydos CA, Tucker HT, Blumenthal PD (2004) Hormonal contraceptive use, cervical ectopy, and the acquisition of cervical infections. Sex Transm Dis 31(9):561–567
Morrison CS, Richardson BA, Mmiro F, Chipato T, Celentano DD, Luoto J, Mugerwa R, Padian N, Rugpao S, Brown JM, Cornelisse P, Salata RA (2007a) Hormonal contraception and the risk of HIV acquisition. Aids 21(1):85–95
Morrison CS, Wang J, Van Der Pol B, Padian N, Salata RA, Richardson BA (2007b) Pregnancy and the risk of HIV-1 acquisition among women in Uganda and Zimbabwe. AIDS 21(8):1027–1034
Morrison EA, Gammon MD, Goldberg GL, Vermund SH, Burk RD (1996) Pregnancy and cervical infection with human papillomaviruses. Int J Gynaecol Obstet 54(2):125–130
Moscicki AB, Hills N, Shiboski S, Powell K, Jay N, Hanson E, Miller S, Clayton L, Farhat S, Broering J, Darragh T, Palefsky J (2001) Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA 285(23):2995–3002
Moscicki AB, Shiboski S, Broering J, Powell K, Clayton L, Jay N, Darragh TM, Brescia R, Kanowitz S, Miller SB, Stone J, Hanson E, Palefsky J (1998) The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr 132(2):277–284
Mostad SB (1998) Prevalence and correlates of HIV type 1 shedding in the female genital tract. AIDS Res Hum Retroviruses 14(Suppl 1):S11–S15
Mostad SB, Kreiss JK, Ryncarz AJ, Mandaliya K, Chohan B, Ndinya-Achola J, Bwayo JJ, Corey L (2000) Cervical shedding of herpes simplex virus in human immunodeficiency virus-infected women: effects of hormonal contraception, pregnancy, and vitamin A deficiency. J Infect Dis 181(1):58–63
Mostad SB, Overbaugh J, DeVange DM, Welch MJ, Chohan B, Mandaliya K, Nyange P, Martin HL Jr, Ndinya-Achola J, Bwayo JJ, Kreiss JK (1997) Hormonal contraception, vitamin A deficiency, and other risk factors for shedding of HIV-1 infected cells from the cervix and vagina. Lancet 350(9082):922–927
Nardelli-Haefliger D, Wirthner D, Schiller JT, Lowy DR, Hildesheim A, Ponci F, De Grandi P (2003) Specific antibody levels at the cervix during the menstrual cycle of women vaccinated with human papillomavirus 16 virus-like particles. J Natl Cancer Inst 95(15):1128–1137
Ness RB, Soper DE, Holley RL, Peipert J, Randall H, Sweet RL, Sondheimer SJ, Hendrix SL, Amortegui A, Trucco G, Bass DC, Kelsey SF (2001) Hormonal and barrier contraception and risk of upper genital tract disease in the PID Evaluation and Clinical Health (PEACH) study. Am J Obstet Gynecol 185(1):121–127
Nielsen A, Kjaer SK, Munk C, Iftner T (2008) Type-specific HPV infection and multiple HPV types: prevalence and risk factor profile in nearly 12, 000 younger and older Danish women. Sex Transm Dis 35(3):276–282
Nobbenhuis MA, Helmerhorst TJ, van den Brule AJ, Rozendaal L, Bezemer PD, Voorhorst FJ, Meijer CJ (2002) High-risk human papillomavirus clearance in pregnant women: trends for lower clearance during pregnancy with a catch-up postpartum. Br J Cancer 87(1):75–80
Nomelini RS, Pansani PL, Murta EF (2007) Frequency of cervical intraepithelial neoplasia and infectious agents for vaginitis in menstrual cycle phase. Eur J Gynaecol Oncol 28(5):389–393
Parazzini F, Di Cintio E, Chiantera V, Guaschino S (2000) Determinants of different Candida species infections of the genital tract in women. Sporachrom Study Geoup. Eur J Obstet Gynecol Reprod Biol 93(2):141–145
Pasley JN, Rank RG, Hough AJ Jr, Cohen C, Barron AL (1985) Absence of progesterone effects on chlamydial genital infection in female guinea pigs. Sex Transm Dis 12(3):155–158
Peddie BA, Bishop V, Bailey RR, McGill H (1984) Relationship between contraceptive method and vaginal flora. Aust N Z J Obstet Gynaecol 24(3):217–218
Putkonen T, Ebeling K (1950) Gonococci and the menstrual cycle. J Vener Dis Inf 31(10):263–267
Rahm VA, Odlind V, Pettersson R (1991) Chlamydia trachomatis in sexually active teenage girls. Factors related to genital chlamydial infection: a prospective study. Genitourin Med 67(4):317–321
Reichelderfer PS, Coombs RW, Wright DJ, Cohn J, Burns DN, Cu-Uvin S, Baron PA, Coheng MH, Landay AL, Beckner SK, Lewis SR, Kovacs AA (2000) Effect of menstrual cycle on HIV-1 levels in the peripheral blood and genital tract. WHS 001 Study Team. AIDS 14(14):2101–2107
Richardson H, Abrahamowicz M, Tellier PP, Kelsall G, du Berger R, Ferenczy A, Coutlee F, Franco EL (2005) Modifiable risk factors associated with clearance of type-specific cervical human papillomavirus infections in a cohort of university students. Cancer Epidemiol Biomarkers Prev 14(5):1149–1156
Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, Lowy DR, Schiller JT (2007) Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 13(7):857–861
Rosenthal GE, Landefeld CS (1990) The relation of chlamydial infection of the cervix to time elapsed from the onset of menses. J Clin Epidemiol 43(1):15–20
Rubin GL, Ory HW, Layde PM (1982) Oral contraceptives and pelvic inflammatory disease. Am J Obstet Gynecol 144(6):630–635
Rupp RE, Stanberry LR, Rosenthal SL (2005) Vaccines for sexually transmitted infections. Pediatr Ann 34(10):818–820 822-4
Schneider A, Kirchhoff T, Meinhardt G, Gissmann L (1992) Repeated evaluation of human papillomavirus 16 status in cervical swabs of young women with a history of normal Papanicolaou smears. Obstet Gynecol 79(5 ( Pt 1)):683–688
Selvakumar R, Schmitt A, Iftner T, Ahmed R, Wettstein FO (1997) Regression of papillomas induced by cottontail rabbit papillomavirus is associated with infiltration of CD8+ cells and persistence of viral DNA after regression. J Virol 71(7):5540–5548
Senanayake P, Kramer DG (1980) Contraception and the etiology of pelvic inflammatory disease: new perspectives. Am J Obstet Gynecol 138(7 Pt 2):852–860
Sherman ME, Carreon JD, Schiffman M (2006) Performance of cytology and human papillomavirus testing in relation to the menstrual cycle. Br J Cancer 94(11):1690–1696
Shrier LA, Bowman FP, Lin M, Crowley-Nowick PA (2003) Mucosal immunity of the adolescent female genital tract. J Adolesc Health 32(3):183–186
Simhan HN, Anderson BL, Krohn MA, Heine RP, Martinez de Tejada B, Landers DV, Hillier SL (2007) Host immune consequences of asymptomatic Trichomonas vaginalis infection in pregnancy. Am J Obstet Gynecol 196((1):59 e1-5
Sonnex C (1998) Influence of ovarian hormones on urogenital infection. Sex Transm Infect 74(1):11–19
Spacek J, Buchta V, Jilek P, Forstl M (2007) Clinical aspects and luteal phase assessment in patients with recurrent vulvovaginal candidiasis. Eur J Obstet Gynecol Reprod Biol 131(2):198–202
Spinillo A, Capuzzo E, Nicola S, Baltaro F, Ferrari A, Monaco A (1995) The impact of oral contraception on vulvovaginal candidiasis. Contraception 51(5):293–297
Stanberry LR, Spruance SL, Cunningham AL, Bernstein DI, Mindel A, Sacks S, Tyring S, Aoki FY, Slaoui M, Denis M, Vandepapeliere P, Dubin G (2002) Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N Engl J Med 347(21):1652–1661
Sterling TR, Vlahov D, Astemborski J, Hoover DR, Margolick JB, Quinn TC (2001) Initial plasma HIV-1 RNA levels and progression to AIDS in women and men. N Engl J Med 344(10):720–725
Straub RH (2007) The complex role of estrogens in inflammation. Endocr Rev 28(5):521–574
Sugarman B, Agbor P (1986) Estrogens and Chlamydia trachomatis. Proc Soc Exp Biol Med 183(1):125–131
Sweet RL, Blankfort-Doyle M, Robbie MO, Schacter J (1986) The occurrence of chlamydial and gonococcal salpingitis during the menstrual cycle. JAMA 255(15):2062–2064
Vaccarella S, Herrero R, Dai M, Snijders PJ, Meijer CJ, Thomas JO, Hoang Anh PT, Ferreccio C, Matos E, Posso H, de Sanjose S, Shin HR, Sukvirach S, Lazcano-Ponce E, Ronco G, Rajkumar R, Qiao YL, Munoz N, Franceschi S (2006) Reproductive factors, oral contraceptive use, and human papillomavirus infection: pooled analysis of the IARC HPV prevalence surveys. Cancer Epidemiol Biomarkers Prev 15(11):2148–2153
van Ham MA, Melchers WJ, Hanselaar AG, Bekkers RL, Boonstra H, Massuger LF (2002) Fluctuations in prevalence of cervical human papillomavirus in women frequently sampled during a single menstrual cycle. Br J Cancer 87(4):373–376
Wang CC, McClelland RS, Overbaugh J, Reilly M, Panteleeff DD, Mandaliya K, Chohan B, Lavreys L, Ndinya-Achola J, Kreiss JK (2004) The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 18(2):205–209
Watts DH (2005) Effect of pregnancy. J Acquir Immune Defic Syndr 38(Suppl 1):S36–S38
Wheeler CM, Greer CE, Becker TM, Hunt WC, Anderson SM, Manos MM (1996) Short-term fluctuations in the detection of cervical human papillomavirus DNA. Obstet Gynecol 88(2):261–268
White S, Larsen B (1997) Candida albicans morphogenesis is influenced by estrogen. Cell Mol Life Sci 53(9):744–749
Wilgenburg BJ, Budgeon LR, Lang CM, Griffith JW, Christensen ND (2005) Characterization of immune responses during regression of rabbit oral papillomavirus infections. Comp Med 55(5):431–439
Wilson ME, Dimayuga FO, Reed JL, Curry TE, Anderson CF, Nath A, Bruce-Keller AJ (2006) Immune modulation by estrogens: role in CNS HIV-1 infection. Endocrine 29(2):289–297
Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA (2003) Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol 157(3):218–226
Wira CR, Grant-Tschudy KS, Crane-Godreau MA (2005) Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am J Reprod Immunol 53(2):65–76
Wolner-Hanssen P (1986) Oral contraceptive use modifies the manifestations of pelvic inflammatory disease. Br J Obstet Gynaecol 93(6):619–624
Wolner-Hanssen P, Eschenbach DA, Paavonen J, Kiviat N, Stevens CE, Critchlow C, DeRouen T, Holmes KK (1990) Decreased risk of symptomatic chlamydial pelvic inflammatory disease associated with oral contraceptive use. JAMA 263(1):54–59
Woods JL, Shew ML, Tu W, Ofner S, Ott MA, Fortenberry JD (2006) Patterns of oral contraceptive pill-taking and condom use among adolescent contraceptive pill users. J Adolesc Health 39(3):381–387
Woodworth CD, Simpson S (1993) Comparative lymphokine secretion by cultured normal human cervical keratinocytes, papillomavirus-immortalized, and carcinoma cell lines. Am J Pathol 142(5):1544–1555
Workowski KA, Berman SM (2006) Sexually transmitted diseases treatment guidelines, 2006. MMWR Recomm Rep 55(RR-11):1–94
Wright TC Jr, Subbarao S, Ellerbrock TV, Lennox JL, Evans-Strickfaden T, Smith DG, Hart CE (2001) Human immunodeficiency virus 1 expression in the female genital tract in association with cervical inflammation and ulceration. Am J Obstet Gynecol 184(3):279–285
Xu F, Sternberg MR, Kottiri BJ, McQuillan GM, Lee FK, Nahmias AJ, Berman SM, Markowitz LE (2006) Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 296(8):964–973
Xu J, Sobel JD (2004) Candida Vulvovaginitis in Pregnancy. Curr Infect Dis Rep 6(6):445–449
Ziegler A, Kastner C, Chang-Claude J (2003) Analysis of pregnancy and other factors on detection of human papilloma virus (HPV) infection using weighted estimating equations for follow-up data. Stat Med 22(13):2217–2233
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2010 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Gravitt, P., Ghanem, K. (2010). Sex Steroids and Risk of Female Genital Tract Infection. In: Klein, S., Roberts, C. (eds) Sex Hormones and Immunity to Infection. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02155-8_10
Download citation
DOI: https://doi.org/10.1007/978-3-642-02155-8_10
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-02154-1
Online ISBN: 978-3-642-02155-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)