The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women (original) (raw)
Ma B, Forney LJ, Ravel J: Vaginal microbiome: rethinking health and disease. Annu Rev Microbiol. 2012, 66: 371-389. 10.1146/annurev-micro-092611-150157. CASPubMedPubMed Central Google Scholar
Döderlein A: Das Scheidensekret und seine Bedeutung fuerdas Puerperalfieber. Die Arten des Scheidensekretes. 1892, 11: 699- Google Scholar
Thomas S: Döderlein Bacillus: lactobacillus acidophilus. J Infect Dis. 1928, 43: 218-227. 10.1093/infdis/43.3.218. Google Scholar
Rogosa M, Sharpe ME: Species differentiation of human vaginal lactobacilli. J Gen Microbiol. 1960, 23: 197-201. 10.1099/00221287-23-1-197. CASPubMed Google Scholar
Redondo-Lopez V, Cook RL, Sobel JD: Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial microflora. Rev Infect Dis. 1990, 12: 856-872. 10.1093/clinids/12.5.856. CASPubMed Google Scholar
Klebanoff SJ, Coombs RW: Viricidal effect of Lactobacillus acidophilus on human immunodeficiency virus type 1: possible role in heterosexual transmission. J Exp Med. 1991, 174: 289-292. 10.1084/jem.174.1.289. CASPubMed Google Scholar
Hillier SL, Krohn MA, Klebanoff SJ, Eschenbach DA: The relationship of hydrogen peroxide-producing lactobacilli to bacterial vaginosis and genital microflora in pregnant women. Obstet Gynecol. 1992, 79: 369-373. 10.1097/00006250-199203000-00008. CASPubMed Google Scholar
Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA: The normal vaginal flora, H2O2-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis. 1993, 16 (Suppl 4): S273-S281. PubMed Google Scholar
Sewankambo N, Gray RH, Wawer MJ, Paxton L, McNaim D, Wabwire-Mangen F: HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet. 1997, 350: 546-550. 10.1016/S0140-6736(97)01063-5. CASPubMed Google Scholar
Gupta K, Stapleton AE, Hooton TM, Roberts PL, Fennell CL, Stamm WE: Inverse association of H2O2-producing lactobacilli and vaginal Escherichia coli colonization in women with recurrent urinary tract infections. J Infect Dis. 1998, 178: 446-450. 10.1086/515635. CASPubMed Google Scholar
Sobel JD: Is there a protective role for vaginal flora?. Curr Infect Dis Rep. 1999, 1: 379-383. 10.1007/s11908-999-0045-z. PubMed Google Scholar
Pybus V, Onderdonk AB: Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect. 1999, 1: 285-292. 10.1016/S1286-4579(99)80024-0. CASPubMed Google Scholar
Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, Chohan B: Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis. 1999, 180: 1863-1868. 10.1086/315127. CASPubMed Google Scholar
Donders GG, Bosmans E, Dekeersmaecker A, Vereecken A, Van Bulck B, Spitz B: Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol. 2000, 182: 872-878. 10.1016/S0002-9378(00)70338-3. CASPubMed Google Scholar
van De Wijgert JH, Mason PR, Gwanzura L, Mbizvo MT, Chirenje ZM, Iliff V: Intravaginal practices, vaginal flora disturbances, and acquisition of sexually transmitted diseases in Zimbabwean women. J Infect Dis. 2000, 181: 587-594. 10.1086/315227. CASPubMed Google Scholar
Larsen B, Monif GR: Understanding the bacterial flora of the female genital tract. Clin Infect Dis. 2001, 32: e69-e77. 10.1086/318710. CASPubMed Google Scholar
Vasquez A, Jakobsson T, Ahrne S, Forsum U, Molin G: Vaginal lactobacillus flora of healthy Swedish women. J Clin Microbiol. 2002, 40: 2746-2749. 10.1128/JCM.40.8.2746-2749.2002. PubMedPubMed Central Google Scholar
Ocana VS, Nader-Macias ME: Vaginal lactobacilli: self- and co-aggregating ability. Br J Biomed Sci. 2002, 59: 183-190. PubMed Google Scholar
Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL: Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis. 2003, 36: 663-668. 10.1086/367658. PubMed Google Scholar
De Backer E, Verhelst R, Verstraelen H, Alqumber MA, Burton JP, Tagg JR: Quantitative determination by real-time PCR of four vaginal Lactobacillus species. Gardnerella vaginalis and Atopobium vaginae indicates an inverse relationship between L. gasseri and L. iners. BMC Microbiol. 2007, 7: 115-10.1186/1471-2180-7-115. PubMedPubMed Central Google Scholar
Lai SK, Hida K, Shukair S, Wang YY, Figueiredo A, Cone R: Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human cervicovaginal mucus. J Virol. 2009, 83: 11196-11200. 10.1128/JVI.01899-08. CASPubMedPubMed Central Google Scholar
Leppaluoto PA: Bacterial vaginosis: what is physiological in vaginal bacteriology? An update and opinion. Acta Obstetricia Et Gynecologica Scandinavica. 2011, 90: 1302-1306. 10.1111/j.1600-0412.2011.01279.x. PubMed Google Scholar
Linhares IM, Summers PR, Larsen B, Giraldo PC, Witkin SS: Contemporary perspectives on vaginal pH and lactobacilli. Am J Obstet Gynecol. 2011, 204 (120): e1-e5. PubMed Google Scholar
Mirmonsef P, Gilbert D, Zariffard MR, Hamaker BR, Kaur A, Landay AL: The effects of commensal bacteria on innate immune responses in the female genital tract. Am J Reprod Immunol. 2011, 65: 190-195. 10.1111/j.1600-0897.2010.00943.x. CASPubMedPubMed Central Google Scholar
Witkin SS, Ledger WJ: Complexities of the uniquely human vagina. Science Translational Medicine. 2012, 4: 132fs11- PubMed Google Scholar
Kashket ER: Bioenergitcs of lactic acid bacteria: cytoplasmic pH and osmotolerance. FEMS Microbiol. 1987, 46: 233-244. 10.1111/j.1574-6968.1987.tb02463.x. CAS Google Scholar
Russell JB, Diez-Gonzalez F: The effects of fermentation acids on bacterial growth. Adv Microb Physiol. 1998, 39: 205-234. CASPubMed Google Scholar
Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA: Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun. 1999, 67: 5170-5175. CASPubMedPubMed Central Google Scholar
Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM: Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol. 2000, 66: 2001-2005. 10.1128/AEM.66.5.2001-2005.2000. CASPubMedPubMed Central Google Scholar
Saling E, Schreiber M, al-Taie T: A simple, efficient and inexpensive program for preventing prematurity. J Perinat Med. 2001, 29: 199-211. CASPubMed Google Scholar
Boskey ER, Cone RA, Whaley KJ, Moench TR: Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum Reprod (Oxford, England). 2001, 16: 1809-1813. 10.1093/humrep/16.9.1809. CAS Google Scholar
Hoyme UB, Saling E: Efficient prematurity prevention is possible by pH-self measurement and immediate therapy of threatening ascending infection. Eur J Obstet Gyn R B. 2004, 115: 148-153. 10.1016/j.ejogrb.2004.02.038. CAS Google Scholar
O’Hanlon DE, Moench TR, Cone RA: In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis. 2011, 11: 200-10.1186/1471-2334-11-200. PubMedPubMed Central Google Scholar
Hammerschlag MR, Alpert S, Onderdonk AB, Thurston P, Drude E, McCormack WM: Anaerobic microflora of the vagina in children. Am J Obstet Gynecol. 1978, 131: 853-856. CASPubMed Google Scholar
Hillier SL, Lau RJ: Vaginal microflora in postmenopausal women who have not received estrogen replacement therapy. Clin Infect Dis. 1997, 25 (Suppl 2): S123-S126. PubMed Google Scholar
Alvarez-Olmos MI, Barousse MM, Rajan L, Van Der Pol BJ, Fortenberry D, Orr D: Vaginal lactobacilli in adolescents: presence and relationship to local and systemic immunity, and to bacterial vaginosis. Sex Transm Dis. 2004, 31: 393-400. 10.1097/01.OLQ.0000130454.83883.E9. PubMed Google Scholar
Farage M, Maibach H: Lifetime changes in the vulva and vagina. Arch Gynecol Obstet. 2006, 273: 195-202. 10.1007/s00404-005-0079-x. PubMed Google Scholar
Gupta S, Kumar N, Singhal N, Kaur R, Manektala U: Vaginal microflora in postmenopausal women on hormone replacement therapy. Indian J Pathol Microbiol. 2006, 49: 457-461. PubMed Google Scholar
Yamamoto T, Zhou X, Williams CJ, Hochwalt A, Forney LJ: Bacterial populations in the vaginas of healthy adolescent women. J Pediatr Adolesc Gynecol. 2009, 22: 11-18. 10.1016/j.jpag.2008.01.073. PubMed Google Scholar
Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ: Understanding vaginal microbiome complexity from an ecological perspective. Transl Res. 2012, 160: 267-282. 10.1016/j.trsl.2012.02.008. CASPubMedPubMed Central Google Scholar
Johnson SR, Petzold CR, Galask RP: Qualitative and quantitative changes of the vaginal microbial flora during the menstrual cycle. Am J Reprod Im Mic. 1985, 9: 1-5. CAS Google Scholar
Eschenbach DA, Thwin SS, Patton DL, Hooton TM, Stapleton AE, Agnew K: Influence of the normal menstrual cycle on vaginal tissue, discharge, and microflora. Clin Infect Dis. 2000, 30: 901-907. 10.1086/313818. CASPubMed Google Scholar
Devillard E, Burton JP, Hammond JA, Lam D, Reid G: Novel insight into the vaginal microflora in postmenopausal women under hormone replacement therapy as analyzed by PCR-denaturing gradient gel electrophoresis. Eur J Obstet Gyn R B. 2004, 117: 76-81. 10.1016/j.ejogrb.2004.02.001. CAS Google Scholar
Heinemann C, Reid G: Vaginal microbial diversity among postmenopausal women with and without hormone replacement therapy. Can J Microbiol. 2005, 51: 777-781. 10.1139/w05-070. CASPubMed Google Scholar
Bezirtzoglou E, Voidarou C, Papadaki A, Tsiotsias A, Kotsovolou O, Konstandi M: Hormone therapy alters the composition of the vaginal microflora in ovariectomized rats. Microb Ecol. 2008, 55: 751-759. 10.1007/s00248-007-9317-z. CASPubMed Google Scholar
Hyman RW, Herndon CN, Jiang H, Palm C, Fukushima M, Bernstein D: The dynamics of the vaginal microbiome during infertility therapy with in vitro fertilization-embryo transfer. J Assist Reprod Genet. 2012, 29: 105-115. 10.1007/s10815-011-9694-6. PubMedPubMed Central Google Scholar
Kazi YF, Saleem S, Kazi N: Investigation of vaginal microbiota in sexually active women using hormonal contraceptives in Pakistan. BMC Urol. 2012, 12: 22-10.1186/1471-2490-12-22. PubMedPubMed Central Google Scholar
Brotman RM, Ravel J, Bavoil PM, Gravitt PE, Ghanem KG: Microbiome, sex hormones, and immune responses in the reproductive tract: challenges for vaccine development against sexually transmitted infections. Vaccine. 2013, Epub 2013/10/19 Google Scholar
Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI: Host-bacterial mutualism in the human intestine. Science. 2005, 307: 1915-1920. 10.1126/science.1104816. PubMed Google Scholar
Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI: The human microbiome project. Nature. 2007, 449: 804-810. 10.1038/nature06244. CASPubMedPubMed Central Google Scholar
Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA: The NIH human microbiome project. Genome Res. 2009, 19: 2317-2323. PubMedPubMed Central Google Scholar
Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR: A catalog of reference genomes from the human microbiome. Science. 2010, 328: 994-999. CASPubMed Google Scholar
Conlan S, Kong HH, Segre JA: Species-level analysis of DNA sequence data from the NIH Human Microbiome Project. PloS one. 2012, 7: e47075-10.1371/journal.pone.0047075. CASPubMedPubMed Central Google Scholar
Cho I, Blaser MJ: The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012, 13: 260-270. CASPubMedPubMed Central Google Scholar
Relman DA: Microbiology: learning about who we are. Nature. 2012, 486: 194-195. 10.1038/486194a. CASPubMed Google Scholar
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C: A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010, 464: 59-65. 10.1038/nature08821. CASPubMedPubMed Central Google Scholar
Spiegel CA, Amsel R, Holmes KK: Diagnosis of bacterial vaginosis by direct gram stain of vaginal fluid. J Clin Microbiol. 1983, 18: 170-177. CASPubMedPubMed Central Google Scholar
Eschenbach DA, Hillier S, Critchlow C, Stevens C, DeRouen T, Holmes KK: Diagnosis and clinical manifestations of bacterial vaginosis. Am J Obstet Gynecol. 1988, 158: 819-828. 10.1016/0002-9378(88)90078-6. CASPubMed Google Scholar
Krohn MA, Hillier SL, Eschenbach DA: Comparison of methods for diagnosing bacterial vaginosis among pregnant women. J Clin Microbiol. 1989, 27: 1266-1271. CASPubMedPubMed Central Google Scholar
Nugent RP, Krohn MA, Hillier SL: Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. 1991, 29: 297-301. CASPubMedPubMed Central Google Scholar
Hillier SL, Krohn MA, Nugent RP, Gibbs RS: Characteristics of three vaginal flora patterns assessed by gram stain among pregnant women. Vaginal Infections and Prematurity Study Group. Am J Obstet Gynecol. 1992, 166: 938-944. CAS Google Scholar
Hay PE, Morgan DJ, Ison CA, Bhide SA, Romney M, McKenzie P: A longitudinal study of bacterial vaginosis during pregnancy. Br J Obstet Gynaecol. 1994, 101: 1048-1053. 10.1111/j.1471-0528.1994.tb13580.x. CASPubMed Google Scholar
Rosenstein IJ, Morgan DJ, Sheehan M, Lamont RF, Taylor-Robinson D: Bacterial vaginosis in pregnancy: distribution of bacterial species in different gram-stain categories of the vaginal flora. J Med Microbiol. 1996, 45: 120-126. 10.1099/00222615-45-2-120. CASPubMed Google Scholar
Schwebke JR, Hillier SL, Sobel JD, McGregor JA, Sweet RL: Validity of the vaginal gram stain for the diagnosis of bacterial vaginosis. Obstet Gynecol. 1996, 88: 573-576. 10.1016/0029-7844(96)00233-5. CASPubMed Google Scholar
Donders GG: Gram stain method shows better sensitivity than clinical criteria for detection of bacterial vaginosis in surveillance of pregnant, low-income women in a clinical setting. Infect Dis Obstet Gynecol. 1999, 7: 273-275. CASPubMedPubMed Central Google Scholar
Curzik D, Drazancic A, Hrgovic Z: Nonspecific aerobic vaginitis and pregnancy. Fetal Diagn Ther. 2001, 16: 187-192. 10.1159/000053906. CASPubMed Google Scholar
Marrazzo JM, Koutsky LA, Eschenbach DA, Agnew K, Stine K, Hillier SL: Characterization of vaginal flora and bacterial vaginosis in women who have sex with women. J Infect Dis. 2002, 185: 1307-1313. 10.1086/339884. PubMed Google Scholar
Wilson JD, Ralph SG, Rutherford AJ: Rates of bacterial vaginosis in women undergoing in vitro fertilisation for different types of infertility. BJOG. 2002, 109: 714-717. 10.1111/j.1471-0528.2002.01297.x. PubMed Google Scholar
Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B: Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG. 2002, 109: 34-43. 10.1111/j.1471-0528.2002.00432.x. PubMed Google Scholar
Brotman RM, Ravel J, Cone RA, Zenilman JM: Rapid fluctuation of the vaginal microbiota measured by Gram stain analysis. Sex Transm Infect. 2010, 86: 297-302. 10.1136/sti.2009.040592. PubMedPubMed Central Google Scholar
Hugenholtz P, Goebel BM, Pace NR: Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol. 1998, 180: 4765-4774. CASPubMedPubMed Central Google Scholar
Kalra A, Palcu CT, Sobel JD, Akins RA: Bacterial vaginosis: culture- and PCR-based characterizations of a complex polymicrobial disease’s pathobiology. Curr Infect Dis Rep. 2007, 9: 485-500. 10.1007/s11908-007-0074-4. PubMed Google Scholar
Amann RI, Ludwig W, Schleifer KH: Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995, 59: 143-169. CASPubMedPubMed Central Google Scholar
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M: Diversity of the human intestinal microbial flora. Science. 2005, 308: 1635-1638. 10.1126/science.1110591. PubMedPubMed Central Google Scholar
Pace NR: A molecular view of microbial diversity and the biosphere. Science. 1997, 276: 734-740. 10.1126/science.276.5313.734. CASPubMed Google Scholar
Torsvik V, Ovreas L: Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol. 2002, 5: 240-245. 10.1016/S1369-5274(02)00324-7. CASPubMed Google Scholar
Martin DH, Zozaya M, Lillis R, Miller J, Ferris MJ: The microbiota of the human genitourinary tract: trying to see the forest through the trees. Trans Am Clin Climatol Assoc. 2012, 123: 242-256. PubMedPubMed Central Google Scholar
Ward DM, Weller R, Bateson MM: 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature. 1990, 345: 63-65. 10.1038/345063a0. CASPubMed Google Scholar
Zoetendal EG, Akkermans AD, De Vos WM: Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998, 64: 3854-3859. CASPubMedPubMed Central Google Scholar
Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD: Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999, 65: 4799-4807. CASPubMedPubMed Central Google Scholar
Ye Y: Identification and Quantification of Abundant Species from Pyrosequences of 16S rRNA by Consensus Alignment. Proceedings (IEEE Int Conf Bioin Biomed). 2011, 2010: 153-157. Google Scholar
Handelsman J: Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol R. 2004, 68: 669-685. 10.1128/MMBR.68.4.669-685.2004. CAS Google Scholar
Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J: Metagenomic pyrosequencing and microbial identification. Clin Chem. 2009, 55: 856-866. 10.1373/clinchem.2008.107565. CASPubMedPubMed Central Google Scholar
Pallen MJ, Loman NJ, Penn CW: High-throughput sequencing and clinical microbiology: progress, opportunities and challenges. Curr Opin Microbiol. 2010, 13: 625-631. 10.1016/j.mib.2010.08.003. CASPubMed Google Scholar
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS: Metagenomic biomarker discovery and explanation. Genome Biol. 2011, 12: R60-10.1186/gb-2011-12-6-r60. PubMedPubMed Central Google Scholar
Gosalbes MJ, Abellan JJ, Durban A, Perez-Cobas AE, Latorre A, Moya A: Metagenomics of human microbiome: beyond 16s rDNA. Clin Microbiol Infec. 2012, 18 (Suppl 4): 47-49. CAS Google Scholar
Hugenholtz P, Pace NR: Identifying microbial diversity in the natural environment: a molecular phylogenetic approach. Trends Biotechnol. 1996, 14: 190-197. 10.1016/0167-7799(96)10025-1. CASPubMed Google Scholar
Baker GC, Smith JJ, Cowan DA: Review and re-analysis of domain-specific 16S primers. J Microbiol Meth. 2003, 55: 541-555. 10.1016/j.mimet.2003.08.009. CAS Google Scholar
Weng L, Rubin EM, Bristow J: Application of sequence-based methods in human microbial ecology. Genome Res. 2006, 16: 316-322. 10.1101/gr.3676406. CASPubMed Google Scholar
Pavlova SI, Kilic AO, Kilic SS, So JS, Nader-Macias ME, Simoes JA: Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences. J Appl Microbiol. 2002, 92: 451-459. 10.1046/j.1365-2672.2002.01547.x. CASPubMed Google Scholar
Zhou X, Bent SJ, Schneider MG, Davis CC, Islam MR, Forney LJ: Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology. 2004, 150: 2565-2573. 10.1099/mic.0.26905-0. CASPubMed Google Scholar
Ferris MJ, Masztal A, Martin DH: Use of species-directed 16S rRNA gene PCR primers for detection of Atopobium vaginae in patients with bacterial vaginosis. J Clin Microbiol. 2004, 42: 5892-5894. 10.1128/JCM.42.12.5892-5894.2004. CASPubMedPubMed Central Google Scholar
Verhelst R, Verstraelen H, Claeys G, Verschraegen G, Delanghe J, Van Simaey L: Cloning of 16S rRNA genes amplified from normal and disturbed vaginal microflora suggests a strong association between Atopobium vaginae. Gardnerella vaginalis and bacterial vaginosis. BMC Microbiol. 2004, 4: 16- PubMed Google Scholar
Fredricks DN, Fiedler TL, Marrazzo JM: Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med. 2005, 353: 1899-1911. 10.1056/NEJMoa043802. CASPubMed Google Scholar
Hyman RW, Fukushima M, Diamond L, Kumm J, Giudice LC, Davis RW: Microbes on the human vaginal epithelium. Proc Natl Acad Sci USA. 2005, 102: 7952-7957. 10.1073/pnas.0503236102. CASPubMedPubMed Central Google Scholar
Hill JE, Goh SH, Money DM, Doyle M, Li A, Crosby WL: Characterization of vaginal microflora of healthy, nonpregnant women by chaperonin-60 sequence-based methods. Am J Obstet Gynecol. 2005, 193: 682-692. 10.1016/j.ajog.2005.02.094. CASPubMed Google Scholar
Sha BE, Chen HY, Wang QJ, Zariffard MR, Cohen MH, Spear GT: Utility of Amsel criteria, Nugent score, and quantitative PCR for Gardnerella vaginalis, Mycoplasma hominis, and Lactobacillus spp. for diagnosis of bacterial vaginosis in human immunodeficiency virus-infected women. J Clin Microbiol. 2005, 43: 4607-4612. 10.1128/JCM.43.9.4607-4612.2005. PubMedPubMed Central Google Scholar
Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P: Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 2007, 1: 121-133. 10.1038/ismej.2007.12. CASPubMed Google Scholar
Witkin SS, Linhares IM, Giraldo P: Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol. 2007, 21: 347-354. 10.1016/j.bpobgyn.2006.12.004. PubMed Google Scholar
Fredricks DN, Fiedler TL, Thomas KK, Oakley BB, Marrazzo JM: Targeted PCR for detection of vaginal bacteria associated with bacterial vaginosis. J Clin Microbiol. 2007, 45: 3270-3276. 10.1128/JCM.01272-07. CASPubMedPubMed Central Google Scholar
Oakley BB, Fiedler TL, Marrazzo JM, Fredricks DN: Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl Environ Microbiol. 2008, 74: 4898-4909. 10.1128/AEM.02884-07. CASPubMedPubMed Central Google Scholar
Zozaya-Hinchliffe M, Martin DH, Ferris MJ: Prevalence and abundance of uncultivated Megasphaera-like bacteria in the human vaginal environment. Appl Environ Microbiol. 2008, 74: 1656-1659. 10.1128/AEM.02127-07. CASPubMedPubMed Central Google Scholar
Trama JP, Pascal KE, Zimmerman J, Self MJ, Mordechai E, Adelson ME: Rapid detection of Atopobium vaginae and association with organisms implicated in bacterial vaginosis. Mol Cell Probes. 2008, 22: 96-102. 10.1016/j.mcp.2007.08.002. CASPubMed Google Scholar
Brotman RM, Ravel J: Ready or not: the molecular diagnosis of bacterial vaginosis. Clin Infect Dis. 2008, 47: 44-46. 10.1086/588662. PubMed Google Scholar
Srinivasan S, Fredricks DN: The human vaginal bacterial biota and bacterial vaginosis. Interdiscip Perspect Infect Dis. 2008, 2008: 750479- PubMedPubMed Central Google Scholar
Lamont RF, Sobel JD, Akins RA, Hassan SS, Chaiworapongsa T, Kusanovic JP: The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG. 2011, 118: 533-549. 10.1111/j.1471-0528.2010.02840.x. CASPubMedPubMed Central Google Scholar
Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL: Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011, 108 (Suppl 1): 4680-4687. CASPubMedPubMed Central Google Scholar
Fettweis JM, Serrano MG, Girerd PH, Jefferson KK, Buck GA: A new era of the vaginal microbiome: advances using next-generation sequencing. Chem Biodivers. 2012, 9: 965-976. 10.1002/cbdv.201100359. CASPubMedPubMed Central Google Scholar
Srinivasan S, Liu C, Mitchell CM, Fiedler TL, Thomas KK, Agnew KJ: Temporal variability of human vaginal bacteria and relationship with bacterial vaginosis. PloS One. 2010, 5: e10197-10.1371/journal.pone.0010197. PubMedPubMed Central Google Scholar
Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, Zhong X: Temporal dynamics of the human vaginal microbiota. Science Translational Medicine. 2012, 4: 52-132. Google Scholar
Zhou X, Hansmann MA, Davis CC, Suzuki H, Brown CJ, Schutte U: The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol. 2010, 58: 169-181. 10.1111/j.1574-695X.2009.00618.x. CASPubMedPubMed Central Google Scholar
Pybus V, Onderdonk AB: Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella bivia involving ammonia: potential significance for bacterial vaginosis. J Infect Dis. 1997, 175: 406-413. 10.1093/infdis/175.2.406. CASPubMed Google Scholar
Pybus V, Onderdonk AB: A commensal symbiosis between Prevotella bivia and Peptostreptococcus anaerobius involves amino acids: potential significance to the pathogenesis of bacterial vaginosis. FEMS Immunol Med Microbiol. 1998, 22: 317-327. 10.1111/j.1574-695X.1998.tb01221.x. CASPubMed Google Scholar
Verstraelen H, Verhelst R, Claeys G, Temmerman M, Vaneechoutte M: Culture-independent analysis of vaginal microflora: the unrecognized association of Atopobium vaginae with bacterial vaginosis. Am J Obstet Gynecol. 2004, 191: 1130-1132. 10.1016/j.ajog.2004.04.013. PubMed Google Scholar
Burton JP, Devillard E, Cadieux PA, Hammond JA, Reid G: Detection of Atopobium vaginae in postmenopausal women by cultivation-independent methods warrants further investigation. J Clin Microbiol. 2004, 42: 1829-1831. 10.1128/JCM.42.4.1829-1831.2004. PubMedPubMed Central Google Scholar
Fredricks DN, Marrazzo JM: Molecular methodology in determining vaginal flora in health and disease: its time has come. Curr Infect Dis Rep. 2005, 7: 463-470. 10.1007/s11908-005-0049-2. PubMed Google Scholar
Bradshaw CS, Tabrizi SN, Fairley CK, Morton AN, Rudland E, Garland SM: The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J Infect Dis. 2006, 194: 828-836. 10.1086/506621. CASPubMed Google Scholar
Tamrakar R, Yamada T, Furuta I, Cho K, Morikawa M, Yamada H: Association between Lactobacillus species and bacterial vaginosis-related bacteria, and bacterial vaginosis scores in pregnant Japanese women. BMC Infect Dis. 2007, 7: 128-10.1186/1471-2334-7-128. PubMedPubMed Central Google Scholar
Menard JP, Fenollar F, Henry M, Bretelle F, Raoult D: Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis. 2008, 47: 33-43. 10.1086/588661. CASPubMed Google Scholar
Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y: Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genom. 2010, 11: 488-10.1186/1471-2164-11-488. Google Scholar
Jespers V, Menten J, Smet H, Poradosu S, Abdellati S, Verhelst R: Quantification of bacterial species of the vaginal microbiome in different groups of women, using nucleic acid amplification tests. BMC Microbiol. 2012, 12: 83-10.1186/1471-2180-12-83. PubMedPubMed Central Google Scholar
Joesoef MR, Hillier SL, Josodiwondo S, Linnan M: Reproducibility of a scoring system for gram stain diagnosis of bacterial vaginosis. J Clin Microbiol. 1991, 29: 1730-1731. CASPubMedPubMed Central Google Scholar
Delaney ML, Onderdonk AB: Nugent score related to vaginal culture in pregnant women. Obstet Gynecol. 2001, 98: 79-84. 10.1016/S0029-7844(01)01402-8. CASPubMed Google Scholar
Burton JP, Reid G: Evaluation of the bacterial vaginal flora of 20 postmenopausal women by direct (Nugent score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J Infect Dis. 2002, 186: 1770-1780. 10.1086/345761. CASPubMed Google Scholar
Peters SE, Beck-Sague CM, Farshy CE, Gibson I, Kubota KA, Solomon F: Behaviors associated with Neisseria gonorrhoeae and Chlamydia trachomatis: cervical infection among young women attending adolescent clinics. Clin Pediatr. 2000, 39: 173-177. 10.1177/000992280003900307. CAS Google Scholar
Cherpes TL, Meyn LA, Krohn MA, Lurie JG, Hillier SL: Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis. 2003, 37: 319-325. 10.1086/375819. PubMed Google Scholar
Schwebke JR: Gynecologic consequences of bacterial vaginosis. Obstet Gyn Clin N Am. 2003, 30: 685-694. 10.1016/S0889-8545(03)00086-X. Google Scholar
Plitt SS, Garfein RS, Gaydos CA, Strathdee SA, Sherman SG, Taha TE: Prevalence and correlates of chlamydia trachomatis, neisseria gonorrhoeae, trichomonas vaginalis infections, and bacterial vaginosis among a cohort of young injection drug users in Baltimore, Maryland. Sex Transm Dis. 2005, 32: 446-453. 10.1097/01.olq.0000154567.21291.59. PubMed Google Scholar
Kaul R, Nagelkerke NJ, Kimani J, Ngugi E, Bwayo JJ, Macdonald KS: Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis. 2007, 196: 1692-1697. 10.1086/522006. PubMed Google Scholar
Gibbs RS: Asymptomatic bacterial vaginosis: is it time to treat?. Am J Obstet Gynecol. 2007, 196: 495-496. 10.1016/j.ajog.2007.04.001. PubMed Google Scholar
Fichorova RN: Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J Reprod Immunol. 2009, 83: 185-189. 10.1016/j.jri.2009.08.007. CASPubMedPubMed Central Google Scholar
Yoshimura K, Yoshimura M, Kobayashi T, Kubo T, Hachisuga T, Kashimura M: Can bacterial vaginosis help to find sexually transmitted diseases, especially chlamydial cervicitis?. Int J Std Aids. 2009, 20: 108-111. 10.1258/ijsa.2008.008249. CASPubMed Google Scholar
Mania-Pramanik J, Kerkar SC, Salvi VS: Bacterial vaginosis: a cause of infertility?. Int J Std Aids. 2009, 20: 778-781. 10.1258/ijsa.2009.009193. CASPubMed Google Scholar
Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J: Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis. 2010, 202: 1907-1915. 10.1086/657320. PubMedPubMed Central Google Scholar
Allsworth JE, Peipert JF: Severity of bacterial vaginosis and the risk of sexually transmitted infection. Am J Obstet Gynecol. 2011, 205 (113): e1-e6. PubMed Google Scholar
Brotman RM, Bradford LL, Conrad M, Gajer P, Ault K, Peralta L: Association between Trichomonas vaginalis and vaginal bacterial community composition among reproductive-age women. Sex Transm Dis. 2012, 39: 807-812. 10.1097/OLQ.0b013e3182631c79. PubMedPubMed Central Google Scholar
Taha TE, Hoover DR, Dallabetta GA, Kumwenda NI, Mtimavalye LA, Yang LP: Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998, 12: 1699-1706. 10.1097/00002030-199813000-00019. CASPubMed Google Scholar
Cu-Uvin S, Hogan JW, Caliendo AM, Harwell J, Mayer KH, Carpenter CC: Association between bacterial vaginosis and expression of human immunodeficiency virus type 1 RNA in the female genital tract. Clin Infect Dis. 2001, 33: 894-896. 10.1086/322613. CASPubMed Google Scholar
Zariffard MR, Sha BE, Wang QJ, Chen HY, Bremer J, Cohen MH: Relationship of U1 cell HIV-stimulatory activity to bacterial vaginosis and HIV genital tract virus load. AIDS Res Hum Retrovir. 2005, 21: 945-948. 10.1089/aid.2005.21.945. CASPubMed Google Scholar
Myer L, Kuhn L, Stein ZA, Wright TC, Denny L: Intravaginal practices, bacterial vaginosis, and women’s susceptibility to HIV infection: epidemiological evidence and biological mechanisms. Lancet Infect Dis. 2005, 5: 786-794. 10.1016/S1473-3099(05)70298-X. PubMed Google Scholar
Watts DH, Fazzari M, Minkoff H, Hillier SL, Sha B, Glesby M: Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis. 2005, 191: 1129-1139. 10.1086/427777. PubMed Google Scholar
Watts DH, Springer G, Minkoff H, Hillier SL, Jacobson L, Moxley M: The occurrence of vaginal infections among HIV-infected and high-risk HIV-uninfected women: longitudinal findings of the women’s interagency HIV study. J Acquir Immune Defic Syndr. 2006, 43: 161-168. 10.1097/01.qai.0000242448.90026.13. PubMed Google Scholar
Spear GT, St John E, Zariffard MR:Bacterial vaginosis and human immunodeficiency virus infection. AIDS Res Ther. 2007, 4: 25-10.1186/1742-6405-4-25. PubMedPubMed Central Google Scholar
Coleman JS, Hitti J, Bukusi EA, Mwachari C, Muliro A, Nguti R: Infectious correlates of HIV-1 shedding in the female upper and lower genital tracts. AIDS. 2007, 21: 755-759. 10.1097/QAD.0b013e328012b838. PubMed Google Scholar
Rebbapragada A, Howe K, Wachihi C, Pettengell C, Sunderji S, Huibner S: Bacterial vaginosis in HIV-infected women induces reversible alterations in the cervical immune environment. J Acquir Immune Defic Syndr. 2008, 49: 520-522. 10.1097/QAI.0b013e318189a7ca. PubMed Google Scholar
Hummelen R, Changalucha J, Butamanya NL, Cook A, Habbema JD, Reid G: Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 to prevent or cure bacterial vaginosis among women with HIV. Int J Gynaecol Obstet. 2010, 111: 245-248. 10.1016/j.ijgo.2010.07.008. PubMed Google Scholar
Guedou FA, Van Damme L, Mirembe F, Solomon S, Becker M, Deese J: Intermediate vaginal flora is associated with HIV prevalence as strongly as bacterial vaginosis in a cross-sectional study of participants screened for a randomised controlled trial. Sex Transm Infect. 2012, 88: 545-551. 10.1136/sextrans-2011-050319. PubMed Google Scholar
Cohen CR, Lingappa JR, Baeten JM, Ngayo MO, Spiegel CA, Hong T: Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS Med. 2012, 9: e1001251-10.1371/journal.pmed.1001251. PubMedPubMed Central Google Scholar
Eschenbach DA, Gravett MG, Chen KC, Hoyme UB, Holmes KK: Bacterial vaginosis during pregnancy. An association with prematurity and postpartum complications. Scand J Urol Nephrol Suppl. 1984, 86: 213-222. CASPubMed Google Scholar
Hardy PH, Hardy JB, Nell EE, Graham DA, Spence MR, Rosenbaum RC: Prevalence of six sexually transmitted disease agents among pregnant inner-city adolescents and pregnancy outcome. Lancet. 1984, 2: 333-337. CASPubMed Google Scholar
Gravett MG, Nelson HP, DeRouen T, Critchlow C, Eschenbach DA, Holmes KK: Independent associations of bacterial vaginosis and Chlamydia trachomatis infection with adverse pregnancy outcome. JAMA. 1986, 256: 1899-1903. 10.1001/jama.1986.03380140069024. CASPubMed Google Scholar
Gravett MG, Hummel D, Eschenbach DA, Holmes KK: Preterm labor associated with subclinical amniotic fluid infection and with bacterial vaginosis. Obstet Gynecol. 1986, 67: 229-237. 10.1097/00006250-198602000-00013. CASPubMed Google Scholar
Minkoff H, Grunebaum A, Feldman J, Cummings M, McCormack WM: Relationship of vaginal pH and Papanicolaou smear results to vaginal flora and pregnancy outcome. Int J Gynaecol Obstet. 1987, 25: 17-23. 10.1016/0020-7292(87)90179-2. CASPubMed Google Scholar
McGregor JA: Prevention of preterm birth: new initiatives based on microbial-host interactions. Obstet Gynecol Surv. 1988, 43: 1-14. 10.1097/00006254-198843010-00001. CASPubMed Google Scholar
McGregor JA, French JI, Lawellin D, Todd JK: Preterm birth and infection: pathogenic possibilities. Am J Reprod Im Mic. 1988, 16: 123-132. CAS Google Scholar
Romero R, Mazor M, Wu YK, Sirtori M, Oyarzun E, Mitchell MD: Infection in the pathogenesis of preterm labor. Sem Perinatol. 1988, 12: 262-279. CAS Google Scholar
Silver HM, Sperling RS, St Clair PJ, Gibbs RS:Evidence relating bacterial vaginosis to intraamniotic infection. Am J Obstet Gynecol. 1989, 161: 808-812. 10.1016/0002-9378(89)90406-7. CASPubMed Google Scholar
Martius J, Eschenbach DA: The role of bacterial vaginosis as a cause of amniotic fluid infection, chorioamnionitis and prematurity – a review. Arch Gynecol Obstet. 1990, 247: 1-13. 10.1007/BF02390649. CASPubMed Google Scholar
Kurki T, Sivonen A, Renkonen OV, Savia E, Ylikorkala O: Bacterial vaginosis in early pregnancy and pregnancy outcome. Obstet Gynecol. 1992, 80: 173-177. CASPubMed Google Scholar
Riduan JM, Hillier SL, Utomo B, Wiknjosastro G, Linnan M, Kandun N: Bacterial vaginosis and prematurity in Indonesia: association in early and late pregnancy. Am J Obstet Gynecol. 1993, 169: 175-178. 10.1016/0002-9378(93)90157-E. CASPubMed Google Scholar
Eschenbach DA: Bacterial vaginosis and anaerobes in obstetric-gynecologic infection. Clin Infect Dis. 1993, 16 (Suppl 4): S282-S287. PubMed Google Scholar
Gibbs RS: Chorioamnionitis and bacterial vaginosis. Am J Obstet Gynecol. 1993, 169: 460-462. 10.1016/0002-9378(93)90341-F. CASPubMed Google Scholar
Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J: Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. Br Med J. 1994, 308: 295-298. 10.1136/bmj.308.6924.295. CAS Google Scholar
Holst E, Goffeng AR, Andersch B: Bacterial vaginosis and vaginal microorganisms in idiopathic premature labor and association with pregnancy outcome. J Clin Microbiol. 1994, 32: 176-186. CASPubMedPubMed Central Google Scholar
McGregor JA, French JI, Jones W, Milligan K, McKinney PJ, Patterson E: Bacterial vaginosis is associated with prematurity and vaginal fluid mucinase and sialidase: results of a controlled trial of topical clindamycin cream. Am J Obstet Gynecol. 1994, 170: 1048-1059. 10.1016/S0002-9378(94)70098-2. Discussion 59–60 CASPubMed Google Scholar
Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH: Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995, 333: 1737-1742. CAS Google Scholar
Meis PJ, Goldenberg RL, Mercer B, Moawad A, Das A, McNellis D: The preterm prediction study: significance of vaginal infections. National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Am J Obstet Gynecol. 1995, 173: 1231-1235. 10.1016/0002-9378(95)91360-2. CASPubMed Google Scholar
Krohn MA, Hillier SL, Nugent RP, Cotch MF, Carey JC, Gibbs RS: The genital flora of women with intraamniotic infection. Vaginal Infection and Prematurity Study Group. J Infect Dis. 1995, 171: 1475-1480. CAS Google Scholar
Goldenberg RL, Thom E, Moawad AH, Johnson F, Roberts J, Caritis SN:The preterm prediction study: fetal fibronectin, bacterial vaginosis, and peripartum infection. NICHD Maternal Fetal Medicine Units Network. Obstet Gynecol. 1996, 87: 656-660. CASPubMed Google Scholar
Wennerholm UB, Holm B, Mattsby-Baltzer I, Nielsen T, Platz-Christensen J, Sundell G: Fetal fibronectin, endotoxin, bacterial vaginosis and cervical length as predictors of preterm birth and neonatal morbidity in twin pregnancies. Br J Obstet Gynaecol. 1997, 104: 1398-1404. 10.1111/j.1471-0528.1997.tb11010.x. CASPubMed Google Scholar
Newton ER, Piper J, Peairs W: Bacterial vaginosis and intraamniotic infection. Am J Obstet Gynecol. 1997, 176: 672-677. 10.1016/S0002-9378(97)70568-4. CASPubMed Google Scholar
Chaim W, Mazor M, Leiberman JR: The relationship between bacterial vaginosis and preterm birth. A review. Arch Gynecol Obstet. 1997, 259: 51-58. 10.1007/BF02505309. CASPubMed Google Scholar
Cotch MF, Pastorek JG, Nugent RP, Hillier SL, Gibbs RS, Martin DH: Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis. 1997, 24: 353-360. CAS Google Scholar
Dammann O, Leviton A: Does prepregnancy bacterial vaginosis increase a mother’s risk of having a preterm infant with cerebral palsy?. Dev Med Child Neurol. 1997, 39: 836-840. CASPubMed Google Scholar
Sherman DJ, Tovbin J, Lazarovich T, Avrech O, Reif R, Hoffmann S: Chorioamnionitis caused by gram-negative bacteria as an etiologic factor in preterm birth. Eur J Clin Microbiol. 1997, 16: 417-423. 10.1007/BF02471905. CAS Google Scholar
Kimberlin DF, Andrews WW: Bacterial vaginosis: association with adverse pregnancy outcome. Semin Perinatol. 1998, 22: 242-250. 10.1016/S0146-0005(98)80012-8. CASPubMed Google Scholar
Gratacos E, Figueras F, Barranco M, Vila J, Cararach V, Alonso PL: Spontaneous recovery of bacterial vaginosis during pregnancy is not associated with an improved perinatal outcome. Acta Obstetricia Et Gynecologica Scandinavica. 1998, 77: 37-40. 10.1080/00016349808565808. CASPubMed Google Scholar
Flynn CA, Helwig AL, Meurer LN: Bacterial vaginosis in pregnancy and the risk of prematurity: a meta-analysis. J Fam Pract. 1999, 48: 885-892. CASPubMed Google Scholar
French JI, McGregor JA, Draper D, Parker R, McFee J: Gestational bleeding, bacterial vaginosis, and common reproductive tract infections: risk for preterm birth and benefit of treatment. Obstet Gynecol. 1999, 93: 715-724. 10.1016/S0029-7844(98)00557-2. CASPubMed Google Scholar
Andrews WW, Hauth JC, Goldenberg RL: Infection and preterm birth. Am J Perinatol. 2000, 17: 357-365. 10.1055/s-2000-13448. CASPubMed Google Scholar
Jacobsson B, Pernevi P, Chidekel L, Jorgen P-CJ: Bacterial vaginosis in early pregnancy may predispose for preterm birth and postpartum endometritis. Acta Obstetricia Et Gynecologica Scandinavica. 2002, 81: 1006-1010. 10.1034/j.1600-0412.2002.811103.x. PubMed Google Scholar
Subtil D, Denoit V, Le Goueff F, Husson MO, Trivier D, Puech F: The role of bacterial vaginosis in preterm labor and preterm birth: a case–control study. Eur J Obstet Gynecol Reprod Biol. 2002, 101: 41-46. 10.1016/S0301-2115(01)00515-2. PubMed Google Scholar
Goffinet F, Maillard F, Mihoubi N, Kayem G, Papiernik E, Cabrol D: Bacterial vaginosis: prevalence and predictive value for premature delivery and neonatal infection in women with preterm labour and intact membranes. Eur J Obstet Gynecol Reprod Biol. 2003, 108: 146-151. 10.1016/S0301-2115(02)00423-2. CASPubMed Google Scholar
Hauth JC, Macpherson C, Carey JC, Klebanoff MA, Hillier SL, Ernest JM: Early pregnancy threshold vaginal pH and Gram stain scores predictive of subsequent preterm birth in asymptomatic women. Am J Obstet Gynecol. 2003, 188: 831-835. 10.1067/mob.2003.184. PubMed Google Scholar
Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P: Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol. 2003, 189: 139-147. 10.1067/mob.2003.339. PubMed Google Scholar
Romero R, Chaiworapongsa T, Kuivaniemi H, Tromp G: Bacterial vaginosis, the inflammatory response and the risk of preterm birth: a role for genetic epidemiology in the prevention of preterm birth. Am J Obstet Gynecol. 2004, 190: 1509-1519. 10.1016/j.ajog.2004.01.002. PubMed Google Scholar
Goffinet F, Kayem G, Maillard F, Trebeden H, Cabrol D, Weill B: Detection of interleukin 6 mRNA by RT-PCR in vaginal secretions: association with preterm delivery and neonatal infection in women with preterm labour and intact membranes. Eur J Obstet Gynecol Reprod Biol. 2005, 123: 167-173. 10.1016/j.ejogrb.2005.03.015. CASPubMed Google Scholar
Larsson PG, Bergstrom M, Forsum U, Jacobsson B, Strand A, Wolner-Hanssen P: Bacterial vaginosis. Transmission, role in genital tract infection and pregnancy outcome: an enigma. APMIS. 2005, 113: 233-245. 10.1111/j.1600-0463.2005.apm_01.x. CASPubMed Google Scholar
Klebanoff MA, Hillier SL, Nugent RP, MacPherson CA, Hauth JC, Carey JC: Is bacterial vaginosis a stronger risk factor for preterm birth when it is diagnosed earlier in gestation?. Am J Obstet Gynecol. 2005, 192: 470-477. 10.1016/j.ajog.2004.07.017. PubMed Google Scholar
Goldenberg RL, Culhane JF, Johnson DC: Maternal infection and adverse fetal and neonatal outcomes. Clin Perinatol. 2005, 32: 523-559. 10.1016/j.clp.2005.04.006. PubMed Google Scholar
Jacobsson B, Mattsby-Baltzer I, Hagberg H: Interleukin-6 and interleukin-8 in cervical and amniotic fluid: relationship to microbial invasion of the chorioamniotic membranes. BJOG. 2005, 112: 719-724. 10.1111/j.1471-0528.2005.00536.x. CASPubMed Google Scholar
Guaschino S, De Seta F, Piccoli M, Maso G, Alberico S: Aetiology of preterm labour: bacterial vaginosis. BJOG. 2006, 113: 46-51. CASPubMed Google Scholar
Vogel I, Thorsen P, Hogan VK, Schieve LA, Jacobsson B, Ferre CD: The joint effect of vaginal Ureaplasma urealyticum and bacterial vaginosis on adverse pregnancy outcomes. Acta Obstetricia Et Gynecologica Scandinavica. 2006, 85: 778-785. 10.1080/00016340500442423. PubMed Google Scholar
Thorsen P, Vogel I, Olsen J, Jeune B, Westergaard JG, Jacobsson B: Bacterial vaginosis in early pregnancy is associated with low birth weight and small for gestational age, but not with spontaneous preterm birth: a population-based study on Danish women. J Matern-Fetal Neo M. 2006, 19: 1-7. Google Scholar
Azargoon A, Darvishzadeh S: Association of bacterial vaginosis, trichomonas vaginalis, and vaginal acidity with outcome of pregnancy. Arch Iran Med. 2006, 9: 213-217. PubMed Google Scholar
Holst RM, Jacobsson B, Hagberg H, Wennerholm UB: Cervical length in women in preterm labor with intact membranes: relationship to intra-amniotic inflammation/microbial invasion, cervical inflammation and preterm delivery. Ultrasound Obst Gyn. 2006, 28: 768-774. 10.1002/uog.3837. Google Scholar
Andrews WW, Klebanoff MA, Thom EA, Hauth JC, Carey JC, Meis PJ: Midpregnancy genitourinary tract infection with Chlamydia trachomatis: association with subsequent preterm delivery in women with bacterial vaginosis and Trichomonas vaginalis. Am J Obstet Gynecol. 2006, 194: 493-500. 10.1016/j.ajog.2005.08.054. PubMed Google Scholar
Leitich H, Kiss H: Asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol. 2007, 21: 375-390. 10.1016/j.bpobgyn.2006.12.005. PubMed Google Scholar
Donders GG, Van Calsteren K, Bellen G, Reybrouck R, Van den Bosch T, Riphagen I: Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG. 2009, 116: 1315-1324. 10.1111/j.1471-0528.2009.02237.x. CASPubMed Google Scholar
Denney JM, Culhane JF: Bacterial vaginosis: a problematic infection from both a perinatal and neonatal perspective. Semin Fetal Neonatal Med. 2009, 14: 200-203. 10.1016/j.siny.2009.01.008. PubMed Google Scholar
Lamont RF, Taylor-Robinson D: The role of bacterial vaginosis, aerobic vaginitis, abnormal vaginal flora and the risk of preterm birth. BJOG. 2010, 117: 119-120. Author reply 20–1 CASPubMed Google Scholar
Larsson PG, Platz-Christensen JJ, Dalaker K, Eriksson K, Fahraeus L, Irminger K: Treatment with 2% clindamycin vaginal cream prior to first trimester surgical abortion to reduce signs of postoperative infection: a prospective, double-blinded, placebo-controlled, multicenter study. Acta Obstetricia Et Gynecologica Scandinavica. 2000, 79: 390-396. 10.1080/j.1600-0412.2000.079005390.x. CASPubMed Google Scholar
Llahi-Camp JM, Rai R, Ison C, Regan L, Taylor-Robinson D: Association of bacterial vaginosis with a history of second trimester miscarriage. Hum Reprod (Oxford, England). 1996, 11: 1575-1578. 10.1093/oxfordjournals.humrep.a019440. CAS Google Scholar
Ralph SG, Rutherford AJ, Wilson JD: Influence of bacterial vaginosis on conception and miscarriage in the first trimester: cohort study. Br Med J. 1999, 319: 220-223. 10.1136/bmj.319.7204.220. CAS Google Scholar
Watts DH, Krohn MA, Hillier SL, Eschenbach DA: Bacterial vaginosis as a risk factor for post-cesarean endometritis. Obstet Gynecol. 1990, 75: 52-58. CASPubMed Google Scholar
Shiraishi T, Fukuda K, Morotomi N, Imamura Y, Mishima J, Imai S: Influence of menstruation on the microbiota of healthy women’s labia minora as analyzed using a 16S rRNA gene-based clone library method. Jpn J Infect Dis. 2011, 64: 76-80. PubMed Google Scholar
Kyongo JK, Jespers V, Goovaerts O, Michiels J, Menten J, Fichorova RN: Searching for lower female genital tract soluble and cellular biomarkers: defining levels and predictors in a cohort of healthy Caucasian women. PloS One. 2012, 7: e43951-10.1371/journal.pone.0043951. CASPubMedPubMed Central Google Scholar
Mitchell CM, Fredricks DN, Winer RL, Koutsky L: Effect of sexual debut on vaginal microbiota in a cohort of young women. Obstet Gynecol. 2012, 120: 1306-1313. PubMedPubMed Central Google Scholar
Verstraelen H, Verhelst R, Claeys G, De Backer E, Temmerman M, Vaneechoutte M:Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora. BMC Microbiol. 2009, 9: 116-10.1186/1471-2180-9-116. PubMedPubMed Central Google Scholar
Hernandez-Rodriguez C, Romero-Gonzalez R, Albani-Campanario M, Figueroa-Damian R, Meraz-Cruz N, Hernandez-Guerrero C: Vaginal microbiota of healthy pregnant Mexican women is constituted by four Lactobacillus species and several vaginosis-associated bacteria. Infect Dis Obstet Gynecol. 2011, 2011: 851485- PubMedPubMed Central Google Scholar
Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C: A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PloS One. 2012, 7: e36466-10.1371/journal.pone.0036466. CASPubMedPubMed Central Google Scholar
Relman DA: ‘Til death do us part’: coming to terms with symbiotic relationships. Forward. Nat Rev Microbiol. 2008, 6: 721-724. 10.1038/nrmicro1990. CASPubMed Google Scholar
Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA: The application of ecological theory toward an understanding of the human microbiome. Science. 2012, 336: 1255-1262. 10.1126/science.1224203. CASPubMedPubMed Central Google Scholar
Tremaroli V, Backhed F: Functional interactions between the gut microbiota and host metabolism. Nature. 2012, 489: 242-249. 10.1038/nature11552. CASPubMed Google Scholar
Maynard CL, Elson CO, Hatton RD, Weaver CT: Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012, 489: 231-241. 10.1038/nature11551. CASPubMedPubMed Central Google Scholar
Hooper LV, Littman DR, Macpherson AJ: Interactions between the microbiota and the immune system. Science. 2012, 336: 1268-1273. 10.1126/science.1223490. CASPubMedPubMed Central Google Scholar
Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK: Bacterial colonization factors control specificity and stability of the gut microbiota. Nature. 2013, 501: 426-429. 10.1038/nature12447. CASPubMedPubMed Central Google Scholar
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL: An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005, 122: 107-118. 10.1016/j.cell.2005.05.007. CASPubMed Google Scholar
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006, 444: 1027-1031. 10.1038/nature05414. PubMed Google Scholar
Ley RE, Turnbaugh PJ, Klein S, Gordon JI: Microbial ecology: human gut microbes associated with obesity. Nature. 2006, 444: 1022-1023. 10.1038/4441022a. CASPubMed Google Scholar
Dethlefsen L, McFall-Ngai M, Relman DA: An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007, 449: 811-818. 10.1038/nature06245. CASPubMed Google Scholar
Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC: Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008, 455: 1109-1113. 10.1038/nature07336. CASPubMedPubMed Central Google Scholar
Baker PI, Love DR, Ferguson LR: Role of gut microbiota in Crohn’s disease. Expet Rev Gastroenterol Hepatol. 2009, 3: 535-546. 10.1586/egh.09.47. CAS Google Scholar
Neuman MG, Nanau RM: Inflammatory bowel disease: role of diet, microbiota, life style. Transl Res. 2012, 160: 29-44. 10.1016/j.trsl.2011.09.001. PubMed Google Scholar
Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R: Diversity, stability and resilience of the human gut microbiota. Nature. 2012, 489: 220-230. 10.1038/nature11550. CASPubMedPubMed Central Google Scholar
Parfrey LW, Knight R: Spatial and temporal variability of the human microbiota. Clin Microbiol Infec. 2012, 18 (Suppl 4): 8-11. Google Scholar
Clemente JC, Ursell LK, Parfrey LW, Knight R: The impact of the gut microbiota on human health: an integrative view. Cell. 2012, 148: 1258-1270. 10.1016/j.cell.2012.01.035. CASPubMed Google Scholar
Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S: Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012, 488: 178-184. 10.1038/nature11319. CASPubMed Google Scholar
Aziz Q, Dore J, Emmanuel A, Guarner F, Quigley EM: Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroent Motil. 2013, 25: 4-15. 10.1111/nmo.12046. CAS Google Scholar
Forney LJ, Gajer P, Williams CJ, Schneider GM, Koenig SS, McCulle SL: Comparison of self-collected and physician-collected vaginal swabs for microbiome analysis. J Clin Microbiol. 2010, 48: 1741-1748. 10.1128/JCM.01710-09. CASPubMedPubMed Central Google Scholar
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R: UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011, 27: 2194-2200. 10.1093/bioinformatics/btr381. CASPubMedPubMed Central Google Scholar
Matsen FA, Kodner RB, Armbrust EV: pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics. 2010, 11: 538-10.1186/1471-2105-11-538. PubMedPubMed Central Google Scholar
Lin J: Divergence measures based on the shannon entropy. IEEE Trans Inf Theory. 1991, 37: 145-151. 10.1109/18.61115. Google Scholar
Højsgaard S, Halekoh U, Yan J: The R package geepack for generalized estimating equations. J Stat Softw. 2006, 15: 1-11. Google Scholar
Lambert D: Zero-inflated Poisson regression, with an application to defects in manufacturing. Technometrics. 1992, 34: 1-14. 10.2307/1269547. Google Scholar
Littell CA, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O: In SAS for Mixed Models. 2nd edition. Nonlinear Mixed Models. 2006, Cary, NY, USA: SAS Institute Inc: Edited by Littell CA, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O, 567-635. Google Scholar
Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol. 2010, 11: R106-10.1186/gb-2010-11-10-r106. CASPubMedPubMed Central Google Scholar
Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R: Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989, 161: 817-824. 10.1016/0002-9378(89)90409-2. CASPubMed Google Scholar
Romero R, Gomez R, Chaiworapongsa T, Conoscenti G, Kim JC, Kim YM: The role of infection in preterm labour and delivery. Paediatr Perinat Ep. 2001, 15 (Suppl 2): 41-56. Google Scholar
Goncalves LF, Chaiworapongsa T, Romero R: Intrauterine infection and prematurity. Ment Retard Dev D R. 2002, 8: 3-13. 10.1002/mrdd.10008. Google Scholar
Gomez R, Romero R, Nien JK, Chaiworapongsa T, Medina L, Kim YM: A short cervix in women with preterm labor and intact membranes: a risk factor for microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 2005, 192: 678-689. 10.1016/j.ajog.2004.10.624. PubMed Google Scholar
Hassan S, Romero R, Hendler I, Gomez R, Khalek N, Espinoza J: A sonographic short cervix as the only clinical manifestation of intra-amniotic infection. J Perinat Med. 2006, 34: 13-19. PubMedPubMed Central Google Scholar
Vaisbuch E, Hassan SS, Mazaki-Tovi S, Nhan-Chang CL, Kusanovic JP, Chaiworapongsa T: Patients with an asymptomatic short cervix (< or =15 mm) have a high rate of subclinical intraamniotic inflammation: implications for patient counseling. Am J Obstet Gynecol. 2010, 202 (433): e1-e8. Google Scholar
Romero R, Gonzalez R, Sepulveda W, Brandt F, Ramirez M, Sorokin Y: Infection and labor. VIII. Microbial invasion of the amniotic cavity in patients with suspected cervical incompetence: prevalence and clinical significance. Am J Obstet Gynecol. 1992, 167: 1086-1091. 10.1016/S0002-9378(12)80043-3. CASPubMed Google Scholar
Mays JK, Figueroa R, Shah J, Khakoo H, Kaminsky S, Tejani N: Amniocentesis for selection before rescue cerclage. Obstet Gynecol. 2000, 95: 652-655. 10.1016/S0029-7844(99)00633-X. CASPubMed Google Scholar
Lee SE, Romero R, Park CW, Jun JK, Yoon BH: The frequency and significance of intraamniotic inflammation in patients with cervical insufficiency. Am J Obstet Gynecol. 2008, 198 (633): e1-e8. Google Scholar
Bujold E, Morency AM, Rallu F, Ferland S, Tetu A, Duperron L: Bacteriology of amniotic fluid in women with suspected cervical insufficiency. J Obstet Gynaecol Can. 2008, 30: 882-887. PubMed Google Scholar
Oh KJ, Lee SE, Jung H, Kim G, Romero R, Yoon BH: Detection of ureaplasmas by the polymerase chain reaction in the amniotic fluid of patients with cervical insufficiency. J Perinat Med. 2010, 38: 261-268. CASPubMedPubMed Central Google Scholar
Romero R, Shamma F, Avila C, Jimenez C, Callahan R, Nores J: Infection and labor. VI. Prevalence, microbiology, and clinical significance of intraamniotic infection in twin gestations with preterm labor. Am J Obstet Gynecol. 1990, 163: 757-761. 10.1016/0002-9378(90)91063-I. CASPubMed Google Scholar
Mazor M, Hershkovitz R, Ghezzi F, Maymon E, Horowitz S, Leiberman JR: Intraamniotic infection in patients with preterm labor and twin pregnancies. Acta Obstetricia Et Gynecologica Scandinavica. 1996, 75: 624-627. 10.3109/00016349609054686. CASPubMed Google Scholar
Yoon BH, Park KH, Koo JN, Jun JK, Syn HC, Romero R: Intramniotic infection of twin pregnancies with preterm labor. Am J Obstet Gynecol. 1997, 176: S35- Google Scholar
Gomez R, Romero R, Nien JK, Medina L, Carstens M, Kim YM: Idiopathic vaginal bleeding during pregnancy as the only clinical manifestation of intrauterine infection. J Matern-Fetal Neo M. 2005, 18: 31-37. 10.1080/14767050500217863. Google Scholar
Park CW, Moon KC, Park JS, Jun JK, Yoon BH: The frequency and clinical significance of intra-uterine infection and inflammation in patients with placenta previa and preterm labor and intact membranes. Placenta. 2009, 30: 613-618. 10.1016/j.placenta.2009.04.005. CASPubMed Google Scholar
Madan I, Romero R, Kusanovic JP, Mittal P, Chaiworapongsa T, Dong Z: The frequency and clinical significance of intra-amniotic infection and/or inflammation in women with placenta previa and vaginal bleeding: an unexpected observation. J Perinat Med. 2010, 38: 275-279. PubMedPubMed Central Google Scholar
Thorp JM, Katz VL, Fowler LJ, Kurtzman JT, Bowes WA: Fetal death from chlamydial infection across intact amniotic membranes. Am J Obstet Gynecol. 1989, 161: 1245-1246. 10.1016/0002-9378(89)90675-3. PubMed Google Scholar
Goldenberg RL, Thompson C: The infectious origins of stillbirth. Am J Obstet Gynecol. 2003, 189: 861-873. 10.1067/S0002-9378(03)00470-8. PubMed Google Scholar
Blackwell S, Romero R, Chaiworapongsa T, Kim YM, Bujold E, Espinoza J: Maternal and fetal inflammatory responses in unexplained fetal death. J Matern-Fetal Neo M. 2003, 14: 151-157. 10.1080/jmf.14.3.151.157. CAS Google Scholar
Horvath B, Yang M, Manning FA: Intrauterine fetal death caused by Haemophilus influenzae infection: a case report. J Reprod Med. 2008, 53: 55-56. PubMed Google Scholar
Vigliani M: Chorioamnionitis and intrauterine fetal death after second-trimester amniocentesis. Fetal Diagn Ther. 2009, 26: 216-218. 10.1159/000257087. PubMed Google Scholar
Doh K, Barton PT, Korneeva I, Perni SC, Bongiovanni AM, Tuttle SL: Differential vaginal expression of interleukin-1 system cytokines in the presence of Mycoplasma hominis and Ureaplasma urealyticum in pregnant women. Infect Dis Obstet Gynecol. 2004, 12: 79-85. 10.1080/10647440400003667. CASPubMedPubMed Central Google Scholar
Paavonen J: Physiology and ecology of the vagina. Scand J Infect Dis Supplementum. 1983, 40: 31-35. CAS Google Scholar
Sjoberg I, Cajander S, Rylander E: Morphometric characteristics of the vaginal epithelium during the menstrual cycle. Gynecol Obstet Inves. 1988, 26: 136-144. 10.1159/000293685. CAS Google Scholar
Galask RP: Vaginal colonization by bacteria and yeast. Am J Obstet Gynecol. 1988, 158: 993-995. 10.1016/0002-9378(88)90111-1. CASPubMed Google Scholar
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: 431-439. 10.1016/S0029-7844(00)00906-6. CASPubMed Google Scholar