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Abstract

Reproductive tract infections (RTIs) are of significant public health concern. The bulk of their long-term morbidity disproportionately affects women. Consequently, research and public health efforts have focused on trying to minimize the burden of these infections in women. In this chapter, we focus on two agents that cause RTIs: Neisseria gonorrhoeae, a curable bacterial infection, and herpes simplex virus (HSV), a viral pathogen for which no cure exists. We have chosen these pathogens to highlight intriguing differences in epidemiology, clinical manifestations, and immunological responses noted between men and women. We begin by summarizing what we know about these infections in women and any existing differences between the sexes. Potential mechanisms that may explain the sex-based differences observed for these and other RTIs are evaluated. Such mechanisms consist of both behavioral (gender) and biological (sex) factors. Consideration of the role of mucosal immune responses, sex hormones, and the vaginal microbiome in mediating sex-based differences are suggested.

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References

  • Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM (2000) Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 66:2001–2005

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aldunate M, Tyssen D, Johnson A, Zakir T, Sonza S, Moench T, Cone R, Tachedjian G (2013) Vaginal concentrations of lactic acid potently inactivate HIV. J Antimicrob Chemother 68:2015–2025

    CAS  PubMed Central  PubMed  Google Scholar 

  • Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, Holmes KK (1983) Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 74:14–22

    CAS  PubMed  Google Scholar 

  • Aroutcheva A, Gariti D, Simon M, Shott S, Faro J, Simoes JA, Gurguis A, Faro S (2001) Defense factors of vaginal lactobacilli. Am J Obstet Gynecol 185:375–379

    CAS  PubMed  Google Scholar 

  • 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 185:380–385

    CAS  PubMed  Google Scholar 

  • 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 21:1771–1777

    PubMed  Google Scholar 

  • Bahamondes L, Trevisan M, Andrade L, Marchi NM, Castro S, Diaz J, Faundes A (2000) The effect upon the human vaginal histology of the long-term use of the injectable contraceptive Depo-Provera. Contraception 62:23–27

    CAS  PubMed  Google Scholar 

  • Bakken LR (1985) Separation and purification of bacteria from soil. Appl Environ Microbiol 49:1482–1487

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balkus JE, Richardson BA, Rabe LK, Taha TE, Mgodi N, Kasaro MP, Ramjee G, Hoffman IF, Abdool Karim SS (2014) Bacterial vaginosis and the risk of trichomonas vaginalis acquisition among HIV-1–negative women. Sex Transm Dis 41:123–128

    PubMed Central  PubMed  Google Scholar 

  • Belkacem A, Caumes E, Ouanich J, Jarlier V, Dellion S, Cazenave B, Goursaud R, Lacassin F, Breuil J, Patey O, Working Group F-D (2013) Changing patterns of disseminated gonococcal infection in France: cross-sectional data 2009–2011. Sex Transm Infect 89:613–615

    PubMed  Google Scholar 

  • Belshe RB, Leone PA, Bernstein DI, Wald A, Levin MJ, Stapleton JT, Gorfinkel I, Morrow RLA, Ewell MG, Stokes-Riner A, Dubin G, Heineman TC, Schulte JM, Deal CD, Herpevac Trial for Women (2012) Efficacy results of a trial of a herpes simplex vaccine. N Engl J Med 366:34–43

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bernstein DI, Bellamy AR, Hook EW, Levin MJ, Wald A, Ewell MG, Wolff PA, Deal CD, Heineman TC, Dubin G, Belshe RB (2013) Epidemiology, clinical presentation, and antibody response to primary infection with herpes simplex virus type 1 and type 2 in young women. Clin Infect Dis 56:344–351

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 165:5077–5083

    CAS  PubMed  Google Scholar 

  • Black SR, Schmiege S, Bull S (2013) Actual versus perceived peer sexual risk behavior in online youth social networks. Transl Behav Med 3:312–319

    PubMed Central  PubMed  Google Scholar 

  • Boris S, Barbés C (2000) Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect 2:543–546

    CAS  PubMed  Google Scholar 

  • Boskey ER, Cone RA, Whaley KJ, Moench TR (2001) Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod 16:1809–1813

    CAS  PubMed  Google Scholar 

  • Bradshaw CS, Walker J, Fairley CK, Chen MY, Tabrizi SN, Donovan B, Kaldor JM, Mcnamee K, Urban E, Walker S, Currie M, Birden H, Bowden F, Garland S, Pirotta M, Gurrin L, Hocking JS (2013) Prevalent and incident bacterial vaginosis are associated with sexual and contraceptive behaviours in young Australian women. PLoS One 8:e57688

    CAS  PubMed Central  PubMed  Google Scholar 

  • Britigan BE, Cohen MS, Sparling PF (1985) Gonococcal infection: a model of molecular pathogenesis. N Engl J Med 312:1683–1694

    CAS  PubMed  Google Scholar 

  • Brotman RM (2011) Vaginal microbiome and sexually transmitted infections: an epidemiologic perspective. J Clin Invest 121:4610–4617

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J, Schwebke JR (2010) Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis 202:1907–1915

    PubMed Central  PubMed  Google Scholar 

  • Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver MI, Viscidi RP, Burke AE, Ravel J, Gravitt PE (2014a) Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause 21:450–458

    PubMed Central  PubMed  Google Scholar 

  • Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, Gravitt PE (2014b) Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis 210:1723–1733

    PubMed  Google Scholar 

  • Bryson Y, Dillon M, Bernstein DI, Radolf J, Zakowski P, Garratty E (1993) Risk of acquisition of genital herpes simplex virus type 2 in sex partners of persons with genital herpes: a prospective couple study. J Infect Dis 167:942–946

    CAS  PubMed  Google Scholar 

  • Buvé A, Jespers V, Crucitti T, Fichorova RN (2014) The vaginal microbiota and susceptibility to HIV. AIDS 28:2333–2344

    PubMed  Google Scholar 

  • Calabrese EJ (2001) Androgens: biphasic dose responses. Crit Rev Toxicol 31:517–522

    CAS  PubMed  Google Scholar 

  • Cherpes TL, Meyn LA, Krohn MA, Hillier SL (2003a) Risk factors for infection with herpes simplex virus type 2: role of smoking, douching, uncircumcised males, and vaginal flora. Sex Transm Dis 30:405–410

    PubMed  Google Scholar 

  • Cherpes TL, Meyn LA, Krohn MA, Lurie JG, Hillier SL (2003b) Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis 37:319–325

    PubMed  Google Scholar 

  • Cohen CR, Lingappa JR, Baeten JM, Ngayo MO, Spiegel CA, Hong T, Donnell D, Celum C, Kapiga S, Delany S, Bukusi EA (2012) Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS Med 9:e1001251

    PubMed Central  PubMed  Google Scholar 

  • Corey L, Wald A, Patel R, Sacks SL, Tyring SK, Warren T, Douglas JM, Paavonen J, Morrow RA, Beutner KR, Stratchounsky LS, Mertz G, Keene ON, Watson HA, Tait D, Vargas-Cortes M, Valacyclovir HSV Transmission Study Group (2004) Once-daily valacyclovir to reduce the risk of transmission of genital herpes. N Engl J Med 350:11–20

    CAS  PubMed  Google Scholar 

  • Cruickshank R (1934) The conversion of the glycogen of the vagina into lactic acid. J Pathol Bacteriol 39:213–219

    CAS  Google Scholar 

  • Datta SD, Sternberg M, Johnson RE, Berman S, Papp JR, Mcquillan G, Weinstock H (2007) Gonorrhea and chlamydia in the United States among persons 14 to 39 years of age, 1999 to 2002. Ann Intern Med 147:89–96

    PubMed  Google Scholar 

  • Devillard E, Burton JP, Hammond JA, Lam D, Reid G (2004) Novel insight into the vaginal microflora in postmenopausal women under hormone replacement therapy as analyzed by PCR-denaturing gradient gel electrophoresis. Eur J Obstet Gynecol Reprod Biol 117:76–81

    CAS  PubMed  Google Scholar 

  • Division of STD Prevention, C D C (2013) Sexually transmitted disease surveillance 2012, pp 1–174

    Google Scholar 

  • Faas M, Bouman A, Moesa H, Heineman MJ, De Leij L, Schuiling G (2000) The immune response during the luteal phase of the ovarian cycle: a Th2-type response? Fertil Steril 74:1008–1013

    CAS  PubMed  Google Scholar 

  • Ferris MJ, Masztal A, Martin DH (2004) Use of species-directed 16S rRNA gene PCR primers for detection of Atopobium vaginae in patients with bacterial vaginosis. J Clin Microbiol 42:5892–5894

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fichorova RN, Desai PJ, Gibson FC 3rd, Genco CA (2001) Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect Immun 69:5840–5848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fredricks DN, Fiedler TL, Marrazzo JM (2005) Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med 353:1899–1911

    CAS  PubMed  Google Scholar 

  • Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ (2006) Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 20:73–83

    PubMed  Google Scholar 

  • Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, Abdo Z, Forney LJ, Ravel J (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med 4:132ra52

    PubMed Central  PubMed  Google Scholar 

  • Gallo MF, Macaluso M, Warner L, Fleenor ME, Hook EW 3rd, Brill I, Weaver MA (2012) Bacterial vaginosis, gonorrhea, and chlamydial infection among women attending a sexually transmitted disease clinic: a longitudinal analysis of possible causal links. Ann Epidemiol 22:213–220

    PubMed  Google Scholar 

  • Ghartey JP, Smith BC, Chen Z, Buckley N, Lo Y, Ratner AJ, Herold BC, Burk RD (2014) Lactobacillus crispatus dominant vaginal microbiome is associated with inhibitory activity of female genital tract secretions against Escherichia coli. PLoS One 9:e96659

    PubMed Central  PubMed  Google Scholar 

  • 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 79:3107–3116

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 79:3117–3126

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goldacre MJ, Loudon N, Watt B, Grant G, Loudon JD, Mcpherson K, Vessey MP (1978) Epidemiology and clinical significance of cervical erosion in women attending a family planning clinic. Br Med J 1:748–750

    CAS  PubMed Central  PubMed  Google Scholar 

  • Graver MA, Wade JJ (2011) The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann Clin Microbiol Antimicrob 10:8

    PubMed Central  PubMed  Google Scholar 

  • Handsfield HH (1975) Disseminated gonococcal infection. Clin Obstet Gynecol 18:131–142

    CAS  PubMed  Google Scholar 

  • Harrison HR, Costin M, Meder JB, Bownds LM, Sim DA, Lewis M, Alexander ER (1985) Cervical Chlamydia trachomatis infection in university women: relationship to history, contraception, ectopy, and cervicitis. Am J Obstet Gynecol 153:244–251

    CAS  PubMed  Google Scholar 

  • Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner-Hanssen P, Holmes KK (1996) Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 174:1058–1063

    CAS  PubMed  Google Scholar 

  • Heinemann C, Reid G (2005) Vaginal microbial diversity among postmenopausal women with and without hormone replacement therapy. Can J Microbiol 51:777–781

    CAS  PubMed  Google Scholar 

  • Hel Z, Stringer E, Mestecky J (2010) Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 31:79–97

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hillier SL, Lau RJ (1997) Vaginal microflora in postmenopausal women who have not received estrogen replacement therapy. Clin Infect Dis 25(Suppl 2):S123–S126

    PubMed  Google Scholar 

  • Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA (1993) The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 16(Suppl 4):S273–S281

    PubMed  Google Scholar 

  • Hook EW (2012) Gender differences in risk for sexually transmitted diseases. Am J Med Sci 343:10–11

    PubMed  Google Scholar 

  • Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336:1268–1273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hummelen R, Macklaim JM, Bisanz JE, Hammond JA, Mcmillan A, Vongsa R, Koenig D, Gloor GB, Reid G (2011) Vaginal microbiome and epithelial gene array in post-menopausal women with moderate to severe dryness. PLoS One 6:e26602

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 27:313–319

    CAS  PubMed  Google Scholar 

  • Jakobsson T, Forsum U (2008) Changes in the predominant human Lactobacillus flora during in vitro fertilisation. Ann Clin Microbiol Antimicrob 7:14

    PubMed Central  PubMed  Google Scholar 

  • Johnson HL, Ghanem KG, Zenilman JM, Erbelding EJ (2011) Sexually transmitted infections and adverse pregnancy outcomes among women attending inner city public sexually transmitted diseases clinics. Sex Transm Dis 38:167–171

    PubMed  Google Scholar 

  • Keane FE, Ison CA, Taylor-Robinson D (1997) A longitudinal study of the vaginal flora over a menstrual cycle. Int J STD AIDS 8:489–494

    CAS  PubMed  Google Scholar 

  • Kenyon C, Colebunders R, Hens N (2013) Determinants of generalized herpes simplex virus-2 epidemics: the role of sexual partner concurrency. Int J STD AIDS 24:375–382

    CAS  PubMed  Google Scholar 

  • King CC, Jamieson DJ, Wiener J, Cu-Uvin S, Klein RS, Rompalo AM, Shah KV, Sobel JD (2011) Bacterial vaginosis and the natural history of human papillomavirus. Infect Dis Obstet Gynecol 2011:319460

    PubMed Central  PubMed  Google Scholar 

  • Koumans EH, Sternberg M, Bruce C, Mcquillan G, Kendrick J, Sutton M, Markowitz LE (2007) The prevalence of bacterial vaginosis in the United States, 2001–2004; associations with symptoms, sexual behaviors, and reproductive health. Sex Transm Dis 34:864–869

    PubMed  Google Scholar 

  • Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R, Hope TJ, Hanes J (2009) Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol 83:11196–11200

    CAS  PubMed Central  PubMed  Google Scholar 

  • Levine WC, Pope V, Bhoomkar A, Tambe P, Lewis JS, Zaidi AA, Farshy CE, Mitchell S, Talkington DF (1998) Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. J Infect Dis 177:167–174

    CAS  PubMed  Google Scholar 

  • Liu B, Roberts CL, Clarke M, Jorm L, Hunt J, Ward J (2013) Chlamydia and gonorrhoea infections and the risk of adverse obstetric outcomes: a retrospective cohort study. Sex Transm Infect 89:672–678

    PubMed  Google Scholar 

  • Looker KJ, Garnett GP (2005) A systematic review of the epidemiology and interaction of herpes simplex virus types 1 and 2. Sex Transm Infect 81:103–107

    CAS  PubMed Central  PubMed  Google Scholar 

  • Looker KJ, Garnett GP, Schmid GP (2008) An estimate of the global prevalence and incidence of herpes simplex virus type 2 infection. Bull World Health Organ 86:805–812 A

    Google Scholar 

  • Louv WC, Austin H, Perlman J, Alexander WJ (1989) Oral contraceptive use and the risk of chlamydial and gonococcal infections. Am J Obstet Gynecol 160:396–402

    CAS  PubMed  Google Scholar 

  • Martin DH (2012) The microbiota of the vagina and its influence on women’s health and disease. Am J Med Sci 343:2–9

    PubMed Central  PubMed  Google Scholar 

  • Martin H, Richardson B, Nyange P, Lavreys L, Hillier S, Chohan B, Mandaliya K, Ndinya-Achola J, Bwayo J, Kreiss J (1999) Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis 180:1863–1868

    CAS  PubMed  Google Scholar 

  • Martin DH, Zozaya M, Lillis RA, Myers L, Nsuami MJ, Ferris MJ (2013) Unique vaginal microbiota that includes an unknown Mycoplasma-like organism is associated with Trichomonas vaginalis infection. J Infect Dis 207:1922–1931

    PubMed Central  PubMed  Google Scholar 

  • Mauck CK, Callahan MM, Baker J, Arbogast K, Veazey R, Stock R, Pan Z, Morrison CS, Chen-Mok M, Archer DF, Gabelnick HL (1999) The effect of one injection of Depo-Provera on the human vaginal epithelium and cervical ectopy. Contraception 60:15–24

    CAS  PubMed  Google Scholar 

  • Mcgee ZA, Jensen RL, Clemens CM, Taylor-Robinson D, Johnson AP, Gregg CR (1999) Gonococcal infection of human fallopian tube mucosa in organ culture: relationship of mucosal tissue TNF-alpha concentration to sloughing of ciliated cells. Sex Transm Dis 26:160–165

    CAS  PubMed  Google Scholar 

  • Mcmillan A, Dell M, Zellar MP, Cribby S, Martz S, Hong E, Fu J, Abbas A, Dang T, Miller W, Reid G (2011) Disruption of urogenital biofilms by lactobacilli. Colloids Surf B: Biointerfaces 86:58–64

    CAS  PubMed  Google Scholar 

  • Miller WC, Ford CA, Morris M, Handcock MS, Schmitz JL, Hobbs MM, Cohen MS, Harris KM, Udry JR (2004) Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA 291:2229–2236

    CAS  PubMed  Google Scholar 

  • Mirmonsef P, Gilbert D, Zariffard MR, Hamaker BR, Kaur A, Landay AL, Spear GT (2011) The effects of commensal bacteria on innate immune responses in the female genital tract. Am J Reprod Immunol 65:190–195

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 31:561–567

    PubMed  Google Scholar 

  • Moscicki AB, Ma Y, Holland C, Vermund SH (2001) Cervical ectopy in adolescent girls with and without human immunodeficiency virus infection. J Infect Dis 183:865–870

    CAS  PubMed  Google Scholar 

  • 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 350:922–927

    CAS  PubMed  Google Scholar 

  • 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 181:58–63

    CAS  PubMed  Google Scholar 

  • Motevaseli E, Shirzad M, Akrami SM, Mousavi A-S, Mirsalehian A, Modarressi MH (2013) Normal and tumour cervical cells respond differently to vaginal lactobacilli, independent of pH and lactate. J Med Microbiol 62:1065–1072

    PubMed  Google Scholar 

  • Myer L, Denny L, Telerant R, Souza M, Wright TC Jr, Kuhn L (2005a) Bacterial vaginosis and susceptibility to HIV infection in South African women: a nested case-control study. J Infect Dis 192:1372–1380

    PubMed  Google Scholar 

  • Myer L, Kuhn L, Stein ZA, Wright TC Jr, Denny L (2005b) Intravaginal practices, bacterial vaginosis, and women’s susceptibility to HIV infection: epidemiological evidence and biological mechanisms. Lancet Infect Dis 5:786–794

    PubMed  Google Scholar 

  • Ness RB, Kip KE, Soper DE, Hillier S, Stamm CA, Sweet RL, Rice P, Richter HE (2005) Bacterial vaginosis (BV) and the risk of incident gonococcal or chlamydial genital infection in a predominantly black population. Sex Transm Dis 32:413–417

    PubMed  Google Scholar 

  • O’brien JP, Goldenberg DL, Rice PA (1983) Disseminated gonococcal infection: a prospective analysis of 49 patients and a review of pathophysiology and immune mechanisms. Medicine 62:395–406

    PubMed  Google Scholar 

  • Ocana VS, Pesce De Ruiz Holgado AA, Nader-Macias ME (1999) Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain. Appl Environ Microbiol 65:5631–5635

    CAS  PubMed Central  PubMed  Google Scholar 

  • O'hanlon DE, Moench TR, Cone RA (2011) In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 11:200

    PubMed Central  PubMed  Google Scholar 

  • Paavonen T (1994) Hormonal regulation of immune responses. Ann Med 26:255–258

    CAS  PubMed  Google Scholar 

  • Pabich WL, Fihn SD, Stamm WE (2003) Prevalence and determinants of vaginal flora alterations in postmenopausal women. J Infect Dis 188:1054–1058

    PubMed  Google Scholar 

  • Peipert JF, Lapane KL, Allsworth JE, Redding CA, Blume JD, Stein MD (2008) Bacterial vaginosis, race, and sexually transmitted infections: does race modify the association? Sex Transm Dis 35:363–367

    PubMed  Google Scholar 

  • Pennock JW, Stegall R, Bell B, Vargas G, Motamedi M, Milligan G, Bourne N (2009) Estradiol improves genital herpes vaccine efficacy in mice. Vaccine 27:5830–5836

    CAS  PubMed Central  PubMed  Google Scholar 

  • Petersen BH, Lee TJ, Snyderman R, Brooks GF (1979) Neisseria meningitidis and Neisseria gonorrhoeae bacteremia associated with C6, C7, or C8 deficiency. Ann Intern Med 90:917–920

    CAS  PubMed  Google Scholar 

  • Phukan N, Parsamand T, Brooks AE, Nguyen TN, Simoes-Barbosa A (2013) The adherence of Trichomonas vaginalis to host ectocervical cells is influenced by lactobacilli. Sex Transm Infect 89:455–459

    PubMed  Google Scholar 

  • Phupong V, Sittisomwong T, Wisawasukmongchol W (2005) Disseminated gonococcal infection during pregnancy. Arch Gynecol Obstet 273:185–186

    PubMed  Google Scholar 

  • Poonia B, Wang X, Veazey RS (2006) Distribution of simian immunodeficiency virus target cells in vaginal tissues of normal rhesus macaques: implications for virus transmission. J Reprod Immunol 72:74–84

    CAS  PubMed  Google Scholar 

  • Prabhala RH, Wira CR (1995) Sex hormone and IL-6 regulation of antigen presentation in the female reproductive tract mucosal tissues. J Immunol 155:5566–5573

    CAS  PubMed  Google Scholar 

  • Putkonen T, Ebeling K (1950) Gonococci and the menstrual cycle. J Vener Dis Inf 31:263–267

    CAS  PubMed  Google Scholar 

  • Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, Mcculle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108(Suppl 1):4680–4687

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ravel J, Brotman RM, Gajer P, Ma B, Nandy M, Fadrosh DW, Sakamoto J, Koenig SS, Fu L, Zhou X, Hickey RJ, Schwebke JR, Forney LJ (2013) Daily temporal dynamics of vaginal microbiota before, during and after episodes of bacterial vaginosis. Microbiome 1:29

    PubMed Central  PubMed  Google Scholar 

  • Reddy BS, Rastogi S, Das B, Salhan S, Verma S, Mittal A (2004) Cytokine expression pattern in the genital tract of Chlamydia trachomatis positive infertile women – implication for T-cell responses. Clin Exp Immunol 137:552–558

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reid G, Heinemann C, Velraeds M, Van Der Mei HC, Busscher HJ (1999) Biosurfactants produced by Lactobacillus. Methods Enzymol 310:426–433

    CAS  PubMed  Google Scholar 

  • Rice PA (2005) Gonococcal arthritis (disseminated gonococcal infection). Infect Dis Clin North Am 19:853–861

    PubMed  Google Scholar 

  • Robinson K, Cohen T, Colijn C (2012) The dynamics of sexual contact networks: effects on disease spread and control. Theor Popul Biol 81:89–96

    PubMed Central  PubMed  Google Scholar 

  • Rompalo AM, Hook EW 3rd, Roberts PL, Ramsey PG, Handsfield HH, Holmes KK (1987) The acute arthritis-dermatitis syndrome. The changing importance of Neisseria gonorrhoeae and Neisseria meningitidis. Arch Intern Med 147:281–283

    CAS  PubMed  Google Scholar 

  • Rosenthal GE, Landefeld CS (1990) The relation of chlamydial infection of the cervix to time elapsed from the onset of menses. J Clin Epidemiol 43:15–20

    CAS  PubMed  Google Scholar 

  • Røttingen JA, Cameron DW, Garnett GP (2001) A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known? Sex Transm Dis 28:579–597

    PubMed  Google Scholar 

  • Ryckman KK, Williams SM, Krohn MA, Simhan HN (2008) Racial differences in cervical cytokine concentrations between pregnant women with and without bacterial vaginosis. J Reprod Immunol 78:166–171

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schiffer JT, Magaret A, Selke S, Corey L, Wald A (2011) Detailed analysis of mucosal herpes simplex virus-2 replication kinetics with and without antiviral therapy. J Antimicrob Chemother 66:2593–2600

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sobel JD (2005) What’s new in bacterial vaginosis and trichomoniasis? Infect Dis Clin North Am 19:387–406

    PubMed  Google Scholar 

  • Sobel JD, Ferris D, Schwebke J, Nyirjesy P, Wiesenfeld HC, Peipert J, Soper D, Ohmit SE, Hillier SL (2006) Suppressive antibacterial therapy with 0.75 % metronidazole vaginal gel to prevent recurrent bacterial vaginosis. Am J Obstet Gynecol 194:1283–1289

    CAS  PubMed  Google Scholar 

  • Srinivasan S, Liu C, Mitchell CM, Fiedler TL, Thomas KK, Agnew KJ, Marrazzo JM, Fredricks DN (2010) Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PLoS One 5:e10197

    PubMed Central  PubMed  Google Scholar 

  • Stanberry LR, Spruance SL, Cunningham AL, Bernstein DI, Mindel A, Sacks S, Tyring S, Aoki FY, Slaoui M, Denis M, Vandepapeliere P, Dubin G, Glaxosmithkline Herpes Vaccine Efficacy Study Group (2002) Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N Engl J Med 347:1652–1661

    CAS  PubMed  Google Scholar 

  • Sturm-Ramirez K, Gaye-Diallo A, Eisen G, Mboup S, Kanki PJ (2000) High levels of tumor necrosis factor-alpha and interleukin-1beta in bacterial vaginosis may increase susceptibility to human immunodeficiency virus. J Infect Dis 182:467–473

    CAS  PubMed  Google Scholar 

  • Svanborg C, Godaly G, Hedlund M (1999) Cytokine responses during mucosal infections: role in disease pathogenesis and host defence. Curr Opin Microbiol 2:99–105

    CAS  PubMed  Google Scholar 

  • Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    CAS  PubMed  Google Scholar 

  • Trent M (2013) Pelvic inflammatory disease. Pediatr Rev/Am Acad Pediatr 34:163–172

    Google Scholar 

  • Tronstein E, Johnston C, Huang M-L, Selke S, Magaret A, Warren T, Corey L, Wald A (2011) Genital shedding of herpes simplex virus among symptomatic and asymptomatic persons with HSV-2 infection. JAMA 305:1441–1449

    CAS  PubMed Central  PubMed  Google Scholar 

  • Valente AM, Auerswald CL (2013) Gender differences in sexual risk and sexually transmitted infections correlate with gender differences in social networks among San Francisco homeless youth. J Adolesc Health 53:486–491

    PubMed  Google Scholar 

  • Vallor AC, Antonio MA, Hawes SE, Hillier SL (2001) Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production. J Infect Dis 184:1431–1436

    CAS  PubMed  Google Scholar 

  • 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 18:205–209

    PubMed  Google Scholar 

  • Wawer MJ, Sewankambo NK, Serwadda D, Quinn TC, Paxton LA, Kiwanuka N, Wabwire-Mangen F, Li C, Lutalo T, Nalugoda F, Gaydos CA, Moulton LH, Meehan MO, Ahmed S, Gray RH (1999) Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial. Rakai Project Study Group. Lancet 353:525–535

    CAS  PubMed  Google Scholar 

  • Wira CR, Rossoll RM (1995) Antigen-presenting cells in the female reproductive tract: influence of sex hormones on antigen presentation in the vagina. Immunology 84:505–508

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wira CR, Rossoll RM, Kaushic C (2000) Antigen-presenting cells in the female reproductive tract: influence of estradiol on antigen presentation by vaginal cells. Endocrinology 141:2877–2885

    CAS  PubMed  Google Scholar 

  • Wise CM, Morris CR, Wasilauskas BL, Salzer WL (1994) Gonococcal arthritis in an era of increasing penicillin resistance. Presentations and outcomes in 41 recent cases (1985–1991). Arch Intern Med 154:2690–2695

    CAS  PubMed  Google Scholar 

  • Witkin SS, Linhares IM, Giraldo P, Ledger WJ (2007) An altered immunity hypothesis for the development of symptomatic bacterial vaginosis. Clin Infect Dis 44:554–557

    CAS  PubMed  Google Scholar 

  • 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 263:54–59

    CAS  PubMed  Google Scholar 

  • Workowski K (2013) In the clinic. Chlamydia and gonorrhea. Ann Intern Med 158:ITC2-1

    PubMed  Google Scholar 

  • World Health Organization (2009) World health statistics, 2009. WHO Press, Geneva

    Google Scholar 

  • 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 296:964–973

    CAS  PubMed  Google Scholar 

  • Yudin MH, Landers DV, Meyn L, Hillier SL (2003) Clinical and cervical cytokine response to treatment with oral or vaginal metronidazole for bacterial vaginosis during pregnancy: a randomized trial. Obstet Gynecol 102:527–534

    CAS  PubMed  Google Scholar 

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Correspondence to Khalil G. Ghanem .

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Brotman, R.M., Ghanem, K.G. (2015). Reproductive Tract Infections in Women. In: Klein, S., Roberts, C. (eds) Sex and Gender Differences in Infection and Treatments for Infectious Diseases. Springer, Cham. https://doi.org/10.1007/978-3-319-16438-0_11

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