Microbiota of female genital tract - functional overview of microbial flora from vagina to uterine tubes and placenta

. 2022 Dec 27 ; 71 (Suppl 1) : S21-S33.

Jazyk angličtina Země Česko Médium print

Typ dokumentu přehledy, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36592438

Microorganisms and eukaryotic human cells coexist in synergistic relationships in nearly every niche of the human body. The female genital tract consisting of the vagina, uterus with its cervix and endometrium, uterine tubes and ovaries - harbors its own typical microbiota, which accounts for 9 % of the total bacterial population in females. To this organ system, we also assigned the microbiome of the placenta, which has not been studied much until now. Among the spectrum of microbial species, the female genital tract is mainly dominated by Lactobacillus species, which are considered to be one of the simplest yet most important microbial communities. However, this relationship between macro- and micro-organisms seems to have a number of physiological functions, e.g., the vaginal and cervical microbiota have unique impact on reproductive health. The aim of this review was to provide current view on female genital tract microbiota and its role in reproductive health. We describe in detail the association of vaginal or tubal epithelium with microbiota or the role of microbiota in normal placental function.

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Young VB. The Role of the microbiome in human health and disease: an introduction for clinicians. BMJ. 2017;356:j831. doi: 10.1136/bmj.j831. PubMed DOI

Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214. doi: 10.1038/nature11234. PubMed DOI PMC

Liptáková A, Predný J, Buc M, Slobodníková L, Jalili N, Krčméry V, Koreň J, et al. Medical Microbiology. 1st Edition. Bratislava, Herba: 2019. p. 952. (in Slovak)

Chen C, Song X, Wei W, Zhong H, Dai J, Lan Z, Li F, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017;8:875. doi: 10.1038/s41467-017-00901-0. PubMed DOI PMC

Moreno I, Simon C. Deciphering the effect of reproductive tract microbiota on human reproduction. Reprod Med Biol. 2018;18(1):40–50. doi: 10.1002/rmb2.12249. PubMed DOI PMC

Punzón-Jiménez P, Labarta E. The impact of the female genital tract microbiome in women health and reproduction: a review. J Assist Reprod Genet. 2021;38(10):2519–2541. doi: 10.1007/s10815-021-02247-5. PubMed DOI PMC

Witkin SS, Linhares IM. Why do lactobacilli dominate the human vaginal microbiota? BJOG. 2017;124(4):606–611. doi: 10.1111/1471-0528.14390. PubMed DOI

Boris S, Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000;2(5):543–546. doi: 10.1016/S1286-4579(00)00313-0. PubMed DOI

White BA, Creedon DJ, Nelson KE, Wilson BA. The vaginal microbiome in health and disease. Trends Endocrinol Metab. 2011;22(10):389–393. doi: 10.1016/j.tem.2011.06.001. PubMed DOI PMC

Greenbaum S, Greenbaum G, Moran-Gilad J, Weintraub AY. Ecological dynamics of the vaginal microbiome in relation to health and disease. Am J Obstet Gynecol. 2019;220(4):324–335. doi: 10.1016/j.ajog.2018.11.1089. PubMed DOI

Vitale SG, Carugno J, D'Alterio MN, Mikuš M, Patrizio P, Angioni S. A New Methodology to Assess Fallopian Tubes Microbiota and Its Impact on Female Fertility. Diagnostics. 2022;12(6):1375. doi: 10.3390/diagnostics12061375. PubMed DOI PMC

Amegashie CP, Gilbert NM, Peipert JF, Allsworth JE, Lewis WG, Lewis AL. Relationship between nugent score and vaginal epithelial exfoliation. PLOS ONE. 2017;12(5):e0177797. doi: 10.1371/journal.pone.0177797. PubMed DOI PMC

Sharma M, Chopra C, Mehta M, Sharma V, Mallubhotla S, Sistla S, Sistla JC, et al. An Insight into Vaginal Microbiome Techniques. Life. 2021;11(11):1229. doi: 10.3390/life11111229. PubMed DOI PMC

Sirota I, Zarek SM, Segars JH. Potential influence of the microbiome on infertility and assisted reproductive technology. Semin Reprod Med. 2014;32(1):35–42. doi: 10.1055/s-0033-1361821. PubMed DOI PMC

Cui L, Morris A, Ghedin E. The human mycobiome in health and disease. Genome Med. 2013;5:63. doi: 10.1186/gm467. PubMed DOI PMC

Johnson JS, Spakowicz DJ, Hong BY, Petersen LM, Demkowicz P, Chen L, Leopold SR, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10(1):5029. doi: 10.1038/s41467-019-13036-1. PubMed DOI PMC

Pekmezovic M, Mogavero S, Naglik JR, Hube B. Host-Pathogen Interactions during Female Genital Tract Infections. Trends Microbiol. 2019;27(12):982–996. doi: 10.1016/j.tim.2019.07.006. PubMed DOI

Łaniewski P, Ilhan ZE, Herbst-Kralovetz MM. The microbiome and gynaecological cancer development, prevention and therapy. Nat Rev Urol. 2020;17(4):232–250. doi: 10.1038/s41585-020-0286-z. PubMed DOI PMC

Farage MA, Miller KW, Sobel JD. Dynamics of the vaginal ecosystem-hormonal influences. Infectious Diseases: Research and Treatment. 2010;3:IDRT-S3903. doi: 10.4137/IDRT.S3903. DOI

Chen X, Lu Y, Chen T, Li R. The female vaginal microbiome in health and bacterial vaginosis. Front Cell Infect Microbiol. 2021;11:631972. doi: 10.3389/fcimb.2021.631972. PubMed DOI PMC

Petrova MI, Lievens E, Malik S, Imholz N, Lebeer S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 2015;6:81. doi: 10.3389/fphys.2015.00081. PubMed DOI PMC

Brown SE, Robinson CK, Shardell MD, Holm JB, Ravel J, Ghanem KG, Brotman RM. Assessing the concordance between urogenital and vaginal microbiota: can urine specimens be used as a proxy for vaginal samples? Front Cell Infection Microbiol. 2021;11:671413. doi: 10.3389/fcimb.2021.671413. PubMed DOI PMC

Martin DH. The microbiota of the vagina and its influence on women's health and disease. Am J Med Sci. 2012;343(1):2–9. doi: 10.1097/MAJ.0b013e31823ea228. PubMed DOI PMC

Aldunate M, Srbinovski D, Hearps AC, Latham CF, Ramsland PA, Gugasyan R, Cone RA, et al. Antimicrobial and immune modulatory effects of lactic acid and short chain fatty acids produced by vaginal microbiota associated with eubiosis and bacterial vaginosis. Front Physiol. 2015;6:164. doi: 10.3389/fphys.2015.00164. PubMed DOI PMC

Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, Padavattan N, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity. 2017;46(1):29–37. doi: 10.1016/j.immuni.2016.12.013. PubMed DOI PMC

Klatt NR, Cheu R, Birse K, Zevin AS, Perner M, Noel-Romas L, Grobler A, et al. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science. 2017;356(6341):938–945. doi: 10.1126/science.aai9383. PubMed DOI

Elovitz MA, Gajer P, Riis V, Brown AG, Humphrys MS, Holm JB, Ravel J. Cervicovaginal microbiota and local immune response modulate the risk of spontaneous preterm delivery. Nat Commun. 2019;10(1):1305. doi: 10.1038/s41467-019-09285-9. PubMed DOI PMC

Al-Memar M, Bobdiwala S, Fourie H, Mannino R, Lee YS, Smith A, Marchesi JR, et al. The association between vaginal bacterial composition and miscarriage: a nested case-control study. BJOG. 2020;127(2):264–274. doi: 10.1111/1471-0528.15972. PubMed DOI PMC

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. 200;16(9):1809–1813. doi: 10.1093/humrep/16.9.1809. PubMed DOI

Aldunate M, Tyssen D, Johnson A, Zakir T, Sonza S, Moench T, Cone R, et al. Vaginal concentrations of lactic acid potently inactivate HIV. J Antimicrob Chemother. 2013;68(9):2015–2025. doi: 10.1093/jac/dkt156. PubMed DOI PMC

Edwards VL, Smith SB, McComb EJ, Tamarelle J, Ma B, Humphrys MS, Cajer P, et al. The cervicovaginal microbiota-host interaction modulates chlamydia trachomatis infection. mBio. 2019;10(4):e01548–19. doi: 10.1128/mBio.01548-19. PubMed DOI PMC

Ravel J, Gajer P, Abdo Z, Frney LJ. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4680–4687. doi: 10.1073/pnas.1002611107. PubMed DOI PMC

Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UME, Zhong X, Koenig SSK, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 2012;4(132):132ra52. doi: 10.1126/scitranslmed.3003605. PubMed DOI PMC

Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, Hall RW, Ross FJ, et al. Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One. 2012;7(6):e37818. doi: 10.1371/journal.pone.0037818. PubMed DOI PMC

Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver M, Viscidi R, et al. Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause. 2014;21(5):450–458. doi: 10.1097/GME.0b013e3182a4690b. PubMed DOI PMC

Pacha-Herrera D, Vasco G, Cruz-Betancourt C, Galarza JM, Barragán V, Machado A. Vaginal microbiota evaluation and lactobacilli quantification by qPCR in pregnant and non-pregnant women: a pilot study. Front Cell Infect Microbiol. 2020;10:303. doi: 10.3389/fcimb.2020.00303. PubMed DOI PMC

Brown JM, Poirot E, Hess KL, Brown S, Vertucci M, Hezareh M. Motivations for intravaginal product use among a cohort of Women in Los Angeles. PLoS One. 2016;11(3):e0151378. doi: 10.1371/journal.pone.0151378. PubMed DOI PMC

Lokken EM, Manguro GO, Abdallah A, Ngacha C, Shafi J, Kiarie J, Jaoko W, et al. Association between vaginal washing and detection of Lactobacillus by culture and quantitative PCR in HIV-seronegative Kenyan women: a cross-sectional analysis. Sex Transm Infect. 2019;95(6):455–461. doi: 10.1136/sextrans-2018-053769. PubMed DOI PMC

Hesham H, Mitchell AJ, Bergerat A, Hung K, Mitchell CM. Impact of vaginal douching products on vaginal Lactobacillus, Escherichia coli and epithelial immune responses. Sci Rep. 2021;11(1):23069. doi: 10.1038/s41598-021-02426-5. PubMed DOI PMC

Alcaide ML, Rodriguez VJ, Brown MR, Pallikkuth S, Arheat K, Martinez O, Roach M, et al. High levels of inflammatory cytokines in the reproductive tract of women with BV and engaging in intravaginal douching: A cross-sectional study of participants in the women interagency HIV study. AIDS Res Hum Retrovir. 2017;33(4):309–317. doi: 10.1089/aid.2016.0187. PubMed DOI PMC

Barousse MM, Van Der Pol BJ, Fortenberry D, Orr D, Fidel PL., Jr Vaginal yeast colonisation, prevalence of vaginitis, and associated local immunity in adolescents. Sex Transm Infect. 2004;80(1):48–53. doi: 10.1136/sti.2002.003855. PubMed DOI PMC

Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspollu A, Saarma I, Salumets A, et al. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One. 2013;8(1):e54379. doi: 10.1371/journal.pone.0054379. PubMed DOI PMC

Noverr MC, Noggle RM, Toews GB, Huffnagle GB. Role of antibiotics and fungal microbiota in driving pulmonary allergic responses. Infect Immun. 2004;72(9):4996–5003. doi: 10.1128/IAI.72.9.4996-5003.2004. PubMed DOI PMC

Kalia N, Singh J, Kaur M. Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: a critical review. Ann Clin Microbiol Antimicrob. 2020;19(1):5. doi: 10.1186/s12941-020-0347-4. PubMed DOI PMC

Nelson DE, Van Der Pol B, Dong Q, Revanna KV, Fan B, Easwaran S, Sodergren E, et al. Characteristic male urine microbiomes associate with asymptomatic sexually transmitted infection. PLoS One. 2010;5(11):e14116. doi: 10.1371/journal.pone.0014116. PubMed DOI PMC

Dong Q, Nelson DE, Toh E, Diao L, Gao X, Fortenberry JD, Van Der Pol B. The microbial communities in male first catch urine are highly similar to those in paired urethral swab specimens. PLoS One. 2011;6(5):e19709. doi: 10.1371/journal.pone.0019709. PubMed DOI PMC

Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K, Fok C, Kliethermes S, et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. mBio. 2014;5(4):e01283–14. doi: 10.1128/mBio.01283-14. PubMed DOI PMC

Mueller ER, Wolfe AJ, Brubaker L. Female urinary microbiota. Curr Opin Urol. 2017;27(3):282–286. doi: 10.1097/MOU.0000000000000396. PubMed DOI PMC

Adebayo AS, Ackermann G, Bowyer RCE, Wells PM, Humphreys G, Knight R, Spector TD, et al. The urinary tract microbiome in older women exhibits host genetic and environmental influences. Cell Host Microbe. 2020;28(2):298–305.e3. doi: 10.1016/j.chom.2020.06.022. PubMed DOI

Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, Brubaker L, et al. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol. 2014;52(3):871–876. doi: 10.1128/JCM.02876-13. PubMed DOI PMC

Coorevits L, Heytens S, Boelens J, Claeys G. The resident microflora of voided midstream urine of healthy controls: standard versus expanded urine culture protocols. Eur J Clin Microbiol Infect Dis. 2017;36(4):635–639. doi: 10.1007/s10096-016-2839-x. PubMed DOI

Thomas-White KJ, Kliethermes S, Rickey L, Wolfe AJ, Brubaker L. Evaluation of the urinary microbiota of women with uncomplicated stress urinary incontinence. Am J Obstet Gynecol. 2017;216(1):55.e1–55.e16. doi: 10.1016/j.ajog.2016.07.049. PubMed DOI PMC

Thomas-White K, Forster SC, Kumar N, Van Kuiken M, Putonti C, Stares MD, Hilt EE, et al. Culturing of female bladder bacteria reveals an interconnected urogenital microbiota. Nat Commun. 2018;9(1):1557. doi: 10.1038/s41467-018-03968-5. PubMed DOI PMC

Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, FitzGerald MP, Mueller ER, et al. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50(4):1376–83. doi: 10.1128/JCM.05852-11. PubMed DOI PMC

Komesu YM, Dinwiddie DL, Richter HE, Carper B, Gantz MG. Defining the relationship between vaginal and urinary microbiomes. Am J Obstet Gynecol. 2020;222(2):154.e1–154.e10. doi: 10.1016/j.ajog.2019.08.011. PubMed DOI PMC

Brown SE, Robinson CK, Shardell MD, Holm JB, Ravel J, Ghanem KG, Brotman RM. Assessing the concordance between urogenital and vaginal microbiota: can urine specimens be used as a proxy for vaginal samples? Front Cell Infect Microbiol. 2021;11:671413. doi: 10.3389/fcimb.2021.671413. PubMed DOI PMC

Gliniewicz K, Schneider GM, Ridenhour BJ, Williams CJ, Song Y, Farage MA, Miller K, et al. Comparison of the vaginal microbiomes of premenopausal and postmenopausal women. Front Microbiol. 2019;10:193. doi: 10.3389/fmicb.2019.00193. PubMed DOI PMC

Shardell M, Gravitt PE, Burke AE, Ravel J, Brotman RM. Association of vaginal microbiota with signs and symptoms of the genitourinary syndrome of menopause across reproductive stages. J Gerontol A Biol Sci Med Sci. 2021;76(9):1542–1550. doi: 10.1093/gerona/glab120. PubMed DOI PMC

Ammitzb⊘ll N, Bau BPJ, Bundgaard-Nielsen C, Villadsen AB, Jensen AM, Leutscher PDC, Glavind K, et al. Pre- and postmenopausal women have different core urinary microbiota. Sci Rep. 2021;11(1):2212. doi: 10.1038/s41598-021-81790-8. PubMed DOI PMC

Holm JB, Humphrys MS, Robinson CK, Settles ML, Ott S, Fu L, Yang H, et al. Ultrahigh-throughput multiplexing and sequencing of >500-base-pair amplicon regions on the Illumina HiSeq 2500 platform. mSystems. 2019;4(1):e00029–19. doi: 10.1128/mSystems.00029-19. PubMed DOI PMC

Amin M, Moradi Choghakabodi P, Alhassan Hamidi M, Najafian M, Farajzadeh Sheikh A. In vitro antimicrobial activities of metabolites from vaginal Lactobacillus strains against Clostridium perfringens isolated from a woman's vagina. J Chin Med Assoc. 2017;80(1):29–33. doi: 10.1016/j.jcma.2016.04.009. PubMed DOI

Mendling W. Vaginal microbiota. Adv Exp Med Biol. 2016;902:83–93. doi: 10.1007/978-3-319-31248-4_6. PubMed DOI

France M, Alizadeh M, Brown S, Ma B, Ravel J. Towards a deeper understanding of the vaginal microbiota. Nat Microbiol. 2022;7:367–378. doi: 10.1038/s41564-022-01083-2. PubMed DOI PMC

Pendergrass PB, Belovicz MW, Reeves CA. Surface area of the human vagina as measured from vinyl polysiloxane casts. Gynecol Obstet Invest. 2003;55(2):110–113. doi: 10.1159/000070184. PubMed DOI

Balko J, Tonar Z, Varga I. Memorix Histology. 1st Edition. Prague, Czech Republic: Triton; 2018. p. 556.

Anderson DJ, Marathe J, Pudney J. The structure of the human vaginal stratum corneum and its role in immune defense. Am J Reprod Immunol. 2014;71(6):618–623. doi: 10.1111/aji.12230. PubMed DOI PMC

Younes JA, Klappe K, Kok JW, Busscher HJ, Reid G, van der Mei HC. Vaginal epithelial cells regulate membrane adhesiveness to co-ordinate bacterial adhesion. Cell Microbiol. 2016;18(4):605–614. doi: 10.1111/cmi.12537. PubMed DOI

Spear GT, McKenna M, Landay AL, Makinde H, Hamaker B, French AL, Lee BH. Effect of pH on cleavage of glycogen by vaginal enzymes. PLoS One. 2015;10(7):e0132646. doi: 10.1371/journal.pone.0132646. PubMed DOI PMC

Nunn KL, Clair GC, Adkins JN, Engbrecht K, Fillmore T, Forney LJ. Amylases in the human vagina. mSphere. 2020;5(6):e00943–20. doi: 10.1128/mSphere.00943-20. PubMed DOI PMC

Wu S, Hugerth LW, Schuppe-Koistinen I, Du J. The right bug in the right place: opportunities for bacterial vaginosis treatment. NPJ Biofilms Microbiomes. 2022;8(1):34. doi: 10.1038/s41522-022-00295-y. PubMed DOI PMC

Mohankumar B, Shandil RK, Narayanan S, Krishnan UM. Vaginosis: Advances in new therapeutic development and microbiome restoration. Microb Pathog. 2022;168:105606. doi: 10.1016/j.micpath.2022.105606. PubMed DOI

Wee BA, Thomas M, Sweeney EL, Frentiu FD, Samios M, Ravel J, Gajer G, et al. A retrospective pilot study to determine whether the reproductive tract microbiota differs between women with a history of infertility and fertile women. Aust N Z J Obstet Gynaecol. 2018;58(3):341–348. doi: 10.1111/ajo.12754. PubMed DOI

Miles SM, Hardy BL, Merrell DS. Investigation of the microbiota of the reproductive tract in women undergoing a total hysterectomy and bilateral salpingo-oopherectomy. Fertil Steril. 2017;107(3):813–820.e1. doi: 10.1016/j.fertnstert.2016.11.028. PubMed DOI

Pelzer ES, Willner D, Buttini M, Huygens F. A role for the endometrial microbiome in dysfunctional menstrual bleeding. Antonie van Leeuwenhoek. 2018;111:933–943. doi: 10.1007/s10482-017-0992-6. PubMed DOI

Winters AD, Romero R, Gervasi MT, Gomez-Lopez N, Tran MR, Garcia-Flores V, Pacora P, et al. Does the endometrial cavity have a molecular microbial signature? Sci Rep. 2019;9(1):9905. doi: 10.1038/s41598-019-46173-0. PubMed DOI PMC

Wang H, Jiang Y, Liang Y, Wei L, Zhang W, Li L. Observation of the cervical microbiome in the progression of cervical intraepithelial neoplasia. BMC Cancer. 2022;22(1):362. doi: 10.1186/s12885-017-3359-5. PubMed DOI PMC

Lin S, Zhang B, Lin Y, Lin Y, Zuo X. Dysbiosis of Cervical and Vaginal Microbiota Associated With Cervical Intraepithelial Neoplasia. Front Cell Infect Microbiol. 2022;12:767693. doi: 10.3389/fcimb.2022.767693. PubMed DOI PMC

Mitchell CM, Haick A, Nkwopara E, Garcia R, Rendi M, Agnew K, Fredricks DN, et al. Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women. Am J Obstet Gynecol. 2015;212(5):611.e1–9. doi: 10.1016/j.ajog.2014.11.043. PubMed DOI PMC

Moreno I, Codoñer FM, Vilella F, Valbuena D, Martinez-Blanch JF, Jimenez-Almazán J, Alonso R, et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am J Obstet Gynecol. 2016;215(6):684–703. doi: 10.1016/j.ajog.2016.09.075. PubMed DOI

Moreno I, Franasiak JM. Endometrial microbiota-new player in town. Fertil Steril. 2017;108(1):32–39. doi: 10.1016/j.fertnstert.2017.05.034. PubMed DOI

Franasiak JM, Werner MD, Juneau CR, Tao X, Landis J, Zhan Y, Treff NR, et al. Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit. J Assist Reprod Genet. 2016;33(1):129–136. doi: 10.1007/s10815-015-0614-z. PubMed DOI PMC

García-Velasco JA, Budding D, Campe H, Malfertheiner SF, Hamamah S, Santjohanser C, Schuppe-Koistinen I, et al. The reproductive microbiome - clinical practice recommendations for fertility specialists. Reprod Biomed Online. 2020;41(3):443–453. doi: 10.1016/j.rbmo.2020.06.014. PubMed DOI

Pelzer ES, Willner D, Buttini M, Hafner LM, Theodoropoulos C, Huygens F. The Fallopian tube microbiome: implications for reproductive health. Oncotarget. 2018;9(30):21541–21551. doi: 10.18632/oncotarget.25059. PubMed DOI PMC

Varga I, Miko M, Kachlík D, Žišková M, Danihel L’, Jr, Babál P. How many cell types form the epithelial lining of the human uterine tubes? Revision of the histological nomenclature of the human tubal epithelium. Ann Anat. 2019;224:73–80. doi: 10.1016/j.aanat.2019.03.012. PubMed DOI

Wira CR, Ghosh M, Smith JM, Shen L, Connor RI, Sundstrom P, Frechette GM, et al. Epithelial cell secretions from the human female reproductive tract inhibit sexually transmitted pathogens and Candida albicans but not Lactobacillus. Mucosal Immunol. 2011;4(3):335–342. doi: 10.1038/mi.2010.72. PubMed DOI PMC

Hunt JL, Lynn AA. Histologic features of surgically removed fallopian tubes. Arch Pathol Lab Med. 2002;126(8):951–955. doi: 10.5858/2002-126-0951-HFOSRT. PubMed DOI

Pelzer ES, Allan JA, Cunningham K, Mengersen K, Allan JM, Launchbury T, Beagley K, et al. Microbial colonization of follicular fluid: alterations in cytokine expression and adverse assisted reproduction technology outcomes. Hum Reprod. 2011;26:1799–1812. doi: 10.1093/humrep/der108. PubMed DOI

Zhou B, Sun C, Huang J, Xia M, Guo E, Li N, Lu H, et al. The biodiversity composition of microbiome in ovarian carcinoma patients. Sci Rep. 2019;9:1691. doi: 10.1038/s41598-018-38031-2. PubMed DOI PMC

Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6:237ra65. doi: 10.1126/scitranslmed.3008599. PubMed DOI PMC

Schoenmakers S, Steegers-Theunissen R, Faas M. The matter of the reproductive microbiome. Obstet Med. 2019;12(3):107–115. doi: 10.1177/1753495X18775899. PubMed DOI PMC

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