The Influence Of The Reproductive System Microbiota On Female And Male Fertility. The Role Of Lactobacillus Bacteria

Kiecka, Aneta; Macura, Barbara; Szczepanik, Marian

doi:10.21307/PM-2021.60.2.12

Abstract

It is well known, that vaginal microbiota is dominated by Lactobacillus genus. These bacteria protect a vaginal microenvironment against the invading pathogens. The presence of Lactobacillus communities was already confirmed in an upper female reproductive system, as well as in the male reproductive system and semen. In this paper we present the current state of knowledge about the influence of the Lactobacillus species on female and male fertility. We also discuss the possible role of the reproductive system microbiota in an idiopathic infertility, and the association between Lactobacillus species and effectiveness of assisted reproductive techniques. Further research on the relationship between the reproductive system microbiota and human fertility is needed.

References

Aldunate M., Tyssen D., Johnson A., Zakir T., Sonza S., Moench T., Cone R., Tachedjian G.: Vaginal concentrations of lactic acid potently inactivate HIV. J. Antimicrob. Chemother. 68, 2015–2025 (2013)
Search in Google Scholar Back to article
Alfano M., Salonia A. i wsp.: Testicular microbiome in azoospermic men-first evidence of the impact of an altered microenvironment. Hum. Reprod. 33, 1212–1217 (2018)
Search in Google Scholar Back to article
Altmäe S., Franasiak J.M., Mändar R.: The seminal microbiome in health and disease. Nat. Rev. Urol. 16, 703–721 (2019)
Search in Google Scholar Back to article
Amabebe E., Anumba DOC.: The vaginal microenvironment: The physiologic role of Lactobacilli. Front. Med. doi:10.3389/fmed.2018.00181 (2018)
Open DOI Search in Google Scholar Back to article
Amato V., Mancini N. i wsp.: Differential composition of vaginal microbiome, but not of seminal microbiome, is associated with successful intrauterine insemination in couples with idio pathic infertility: A Prospective observational study. Open Forum Infect. Dis. doi:10.1093/ofid/ofz525 (2020)
Open DOI Search in Google Scholar Back to article
Anahtar M.N., Gootenberg D.B., Mitchell C.M., Kwon D.S.: Cervicovaginal microbiota and reproductive health: The virtue of simplicity. Cell Host Microbe. 23,159–168 (2018)
Search in Google Scholar Back to article
Aroutcheva A., Gariti D., Simon M., Shott S., Faro J., Simoes J.A., Gurguis A., Faro S.: Defense factors of vaginal Lactobacilli. Am. J. Obstet. Gynecol. 185, 375–379 (2001)
Search in Google Scholar Back to article
Baud D., Pattaroni C., Vulliemoz N., Castella V., Marsland B.J., Stojanov M.: Sperm microbiota and its impact on semen parameters, Front Microbiol. doi: 10.3389/fmicb.2019.00234 (2019)
Open DOI Search in Google Scholar Back to article
Benner M., Ferwerda G., Joosten I., van der Molen R.G.: How uterine microbiota might be responsible for a receptive, fertile endometrium. Hum. Reprod. Update. 24, 393–415 (2018)
Search in Google Scholar Back to article
Bernabeu A., Bernabeu R. i wsp.: Effect of the vaginal microbiome on the pregnancy rate in women receiving assisted reproductive treatment. J. Assist. Reprod. Genet. 36, 2111–2119 (2019)
Search in Google Scholar Back to article
Bracewell-Milnes T., Saso S., Nikolaou D., Norman-Taylor J., Johnson M., Thum MY.: Investigating the effect of an abnormal cervico-vaginal and endometrial microbiome on assisted reproductive technologies: A systematic review. Am. J. Reprod. Immunol. 80, e13037 (2018)
Search in Google Scholar Back to article
Brandão P., Gonçalves-Henriques M.: The impact of female genital microbiota on fertility and assisted reproductive treatments. J. Fam. Reprod. Health. 14, 131–149 (2020)
Search in Google Scholar Back to article
Campisciano G., Florian F., D’Eustacchio A., Stanković D., Ricci G., De Seta F., Comar M.: Subclinical alteration of the cervical-vaginal microbiome in women with idiopathic infertility. J. Cell. Physiol. 232, 1681–1688 (2017)
Search in Google Scholar Back to article
Chen C., Jia H. i wsp.: The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat. Commun. doi: 10.1038/s41467-017-00901-0 (2017)
Open DOI Search in Google Scholar Back to article
Deplanche M., Berkova N. i wsp.: Staphylococcus aureus induces DNA damage in host cell. Sci. Rep. doi:10.1038/s41598-019-44213-3 (2019)
Open DOI Search in Google Scholar Back to article
Farahani L., Tharakan T., Yap T., Ramsay J.W., Jayasena C.N., Minhas S.: The semen microbiome and its impact on sperm function and male fertility: a systematic review and meta-analysis. Andrology. doi: 10.1111/andr.12886 (2020)
Open DOI Search in Google Scholar Back to article
France MT, Mendes-Soares H, Forney LJ. Genomic Comparisons of Lactobacillus crispatus and Lactobacillus iners Reveal Potential Ecological Drivers of Community Composition in the Vagina. Appl. Environ. Microbiol. 21, 24: 7063–7073 (2016)
Search in Google Scholar Back to article
Gajer P., Ravel J.: Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med. 4, 132ra52 (2012)
Search in Google Scholar Back to article
Garcia-Grau I., Perez-Villaroya D., Bau D., Gonzalez-Monfort M., Vilella F., Moreno I., Simon C.: Taxonomical and functional assessment of the endometrial microbiota in a context of recurrent reproductive failure: A case report. Pathogens, 8, 205 (2019)
Search in Google Scholar Back to article
García-Velasco J.A., Budding D., Campe H., Malfertheiner S.F., Hamamah S., Santjohanser C., Schuppe-Koistinen I., Nielsen H.S., Vieira-Silva S., Laven J.: The reproductive microbiome – clinical practice recommendations for fertility specialists. Reprod. Biomed. 41, 443–453 (2020)
Search in Google Scholar Back to article
Gerstner, G.J., Grünberger, W., Boschitsch, E., Rotter M.: Vaginal organisms in prepubertal children with and without vulvovaginitis. Arch. Gynecol. 231, 247–252 (1982)
Search in Google Scholar Back to article
Haahr T., Jensen J.S., Thomsen L., Duus L., Rygaard K., Humaidan P.: Abnormal vaginal microbiota may be associated with poor reproductive outcomes: a prospective study in IVF patients. Human Reprod. 31, 795–803 (2016)
Search in Google Scholar Back to article
Hammerschlag M.R., Alpert S., Rosner I. Microbiology of the vagina in children: normal and potentially pathogenic organisms. Pediatrics. 62 57–62 (1978)
Search in Google Scholar Back to article
Hou D., Zhou X., Zhong X., Settles M. L., Herring J., Wang L., Abdo Z., Forney L. J., Xu C.: Microbiota of the seminal fluid from healthy and infertile men. Fertil. Steril. 100, 1261–1269 (2013)
Search in Google Scholar Back to article
Javurek, A.B., Spollen W.G., Ali A.M., Johnson S.A., Lubahn D.B., Bivens N.J., Bromert K.H., Ellersieck M.R., Givan, S.A., Rosenfeld C.S.: Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status. Sci. Rep. 6, 23027 (2016)
Search in Google Scholar Back to article
Jungwirth A., Diemer T., Dohle G. R., Giwercman B. A., Kopa Z., Krausz C., Tournaye H. „Rekomendacje dotyczące postępowania w męskiej niepłodności”, Post. Androl. 3, 17–54 (2016)
Search in Google Scholar Back to article
Kacerovsky M., Vrbacky F., Kutova R., Pliskova L., Andrys C., Musilova I., Menon R., Lamont R., Nekvindova J.: Cervical microbiota in women with preterm prelabor rupture of membranes. PLoS One, 10, e0126884 (2015)
Search in Google Scholar Back to article
Karaoğlu Ş.: Antimicrobial activity and characteristics of bacteriocins produced by vaginal Lactobacilli. Turk. J. Med. Sci. 33, 7–13 (2003)
Search in Google Scholar Back to article
Koedooder R., Laven J.S.E. i wsp.: The vaginal microbiome as a predictor for outcome of in vitro fertilization with or without intracytoplasmic sperm injection: a prospective study. Hum. Reprod. 34, 1042–1054 (2019)
Search in Google Scholar Back to article
Koedooder R., Mackens S., Budding A., Fares D., Blockeel C., Laven J., Schoenmakers S.: Identification and evaluation of the microbiome in the female and male reproductive tracts. Hum. Reprod. 25, 298–325 (2019)
Search in Google Scholar Back to article
Kong Y., Liu Z., Shang Q., Gao Y., Li X., Zheng C., Deng X., Chen T.: The disordered vaginal microbiota is a potential indicator for a higher failure of invitro fertilization. Front. Med. 7, 217 (2020)
Search in Google Scholar Back to article
Kyono K., Hashimoto T., Kikuchi S., Nagai Y., Sakuraba Y.: A pilot study and case reports on endometrial microbiota and pregnancy outcome: An analysis using 16S rRNA gene sequencing among IVF patients, and trial therapeutic intervention for dysbiotic endometrium. Reprod. Med. Biol. 18, 72–82 (2018)
Search in Google Scholar Back to article
Lundy S., Eng C.: Functional and taxonomic dysbiosis of the gut, urine, and semen microbiome in male infertility. Fert. Steril. 114, e94 (2020)
Search in Google Scholar Back to article
Łepecka-Klusek C., Pilewska-Kozak A.B., Jakiel G.: Niepłodność w świetle definicji choroby podanej przez WHO, Med. Og. Nauk. Zdr. 18, 163–166 (2012)
Search in Google Scholar Back to article
Łukaszuk K., Wołczyński S. i wsp.: (2018) Diagnostyka i leczenie niepłodności – rekomendacje Polskiego Towarzystwa Medycyny Rozrodu i Embriologii (PTMRiE) oraz Polskiego Towarzystwa Ginekologów i Położników (PTGP). GiPP, 3, 112–140 (2018)
Search in Google Scholar Back to article
Macura B., Majewska-Szczepanik M., Strzępa A., Szczepanik M.: Wpływ mikrobioty macicy na zdrowie kobiety i jej potomstwa. Med. Og. Nauk. Zdr. 26, 230–239 (2020)
Search in Google Scholar Back to article
Mändar R. Microbiota of male genital tract: impact on the health of man and his partner. Pharmacol Res. 69, 32–41 (2013)
Search in Google Scholar Back to article
Mändar R., Truu J. i wsp.: Complementary seminovaginal microbiome in couples. Res. Microbiol. 166, 440–447 (2015)
Search in Google Scholar Back to article
Mändar R., Türk S., Korrovits P., Ausmees K., Punab M.: Impact of sexual debut on culturable human seminal microbiota. Andrology, 6, 510–512 (2018)
Search in Google Scholar Back to article
Moreno I., Garcia-Grau I., Bau D., Perez-Villaroya D., Gonzalez--Monfort M., Vilella F., Romero R., Simón C.: The first glimpse of the endometrial microbiota in early pregnancy. Am. J. Obstet. Gynecol. 222, 296–305 (2020)
Search in Google Scholar Back to article
Moreno, I.; Simon, C. Relevance of assessing the uterine microbiota in infertility. Fertil. Steril. 110, 337–343 (2018)
Search in Google Scholar Back to article
Moreno I., Simon C.: Deciphering the effect of reproductive tract microbiota on human reproduction. Reprod. Med. Biol. 18, 40–50 (2018)
Search in Google Scholar Back to article
Nardini P., Ñahui Palomino R.A., Parolin C., Laghi L., Foschi C., Cevenini R., Vitali B., Marangoni A.: Lactobacillus crispatus inhibits the infectivity of Chlamydiatrachomatis elementary bodies, in vitro study. Sci. Rep. 6, 29024 (2016)
Search in Google Scholar Back to article
Nunn K.L., Forney L.J.: Unraveling the dynamics of the human vaginal microbiome. Yale J. Biol. Med. 9, 331–337 (2016)
Search in Google Scholar Back to article
Nuriel-Ohayon M., Neuman H., Koren O.: Microbial changes during pregnancy, birth, and infancy. Front. Microbiol. 7, 1031 (2016)
Search in Google Scholar Back to article
Osadchiy V., Mills J. N., Mayer E. A., Eleswarapu S. V.: The seminal microbiome and male factor infertility. Curr. Sex. Health Rep. 12, 202–207 (2020)
Search in Google Scholar Back to article
Petricevic L., Domig K.J., Nierscher F.J., Sandhofer M.J., Fidesser M., Krondorfer I., Husslein P., Kneifel W., Kiss H.: Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci. Rep. 4, 5136 (2014)
Search in Google Scholar Back to article
Petrova M.I., Lievens E., Malik S., Imholz N., Lebeer S.: Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 6, 81 (2015)
Search in Google Scholar Back to article
Petrova M.I., Reid G., Vaneechoutte M., Lebeer S.: Lactobacillus iners: Friend or Foe? Trends Microbiol. 25, 182–191 (2017)
Search in Google Scholar Back to article
Pytka M., Kordowska-Wiater M., Jarocki P.: Mikrobiom układu płciowego kobiet. Post. Mikrobiol. 58, 227–236 (2019)
Search in Google Scholar Back to article
Ravel J., Forney LJ. i wsp.: Vaginal microbiome of reproductive--age women. Proc. Natl. Acad. Sci. 108, 4680–4687 (2011)
Search in Google Scholar Back to article
Schoenmakers S., Laven J.: The vaginal microbiome as a tool to predict IVF success. Curr. Opin. Obstet. Gynecol. 32, 169–178 (2020)
Search in Google Scholar Back to article
Singer M., Borg M., Ouburg S., Morré S.A.: The relation of the vaginal microbiota to early pregnancy development during in vitro fertilization treatment-A meta-analysis. J. Gynecol. Obstet. Hum. Reprod. 48, 223–229 (2019)
Search in Google Scholar Back to article
Stone L.: Infection: Vaginal microbiota and infectious infertility. Nat Rev Urol. 15, 136 (2018)
Search in Google Scholar Back to article
Štšepetova J.A., Mändar R.: The complex microbiome from native semen to embryo culture environment in human in vitro fertilization. Reprod. Biol. Endocrinol. 18, 3 (2020)
Search in Google Scholar Back to article
Swanson G.M., Moskovtsev S., Librach C., Pilsner J.R., Goodrich R., Stephen A., Krawetz S.A.: What human sperm RNA-Seq tells us about the microbiome. J. Assist. Reprod. Genet. 37, 359–368 (2020)
Search in Google Scholar Back to article
Tachedjian G., O’Hanlon D.E., Ravel J.: The implausible „in vivo” role of hydrogen peroxide as an antimicrobial factor produced by vaginal microbiota. Microbiome, 6, 29 (2018)
Search in Google Scholar Back to article
Tomaiuolo R., Veneruso I., Cariati F., D’Argenio V.: Microbiota and human reproduction: the case of female infertility. High Throughput, 9, 12 (2020)
Search in Google Scholar Back to article
Tomaiuolo R., Veneruso I., Cariati F., D’Argenio V.: Microbiota and human reproduction: the case of male infertility. High Throughput, 9, 10 (2020)
Search in Google Scholar Back to article
Valcarce D.G., Genovés S., Riesco M.F., Martorell P., Herráez M.P., Ramón D., Robles V.: Probiotic administration improves sperm quality in asthenozoospermic human donors. Benef. Microbes, 8, 193–206 (2017)
Search in Google Scholar Back to article
Valenti P., Rosa L., Capobianco D., Lepanto M.S., Schiavi E., Cutone A., Paesano R., Mastromarino P.: Role of Lactobacilli and Lactoferrin in the Mucosal Cervicovaginal Defense. Front. Immunol. 9, 376 (2018)
Search in Google Scholar Back to article
Vallor A.C., Antonio M.A., Hawes S.E., Hillier S.L.: Factors associated with acquisition of, or persistent colonization by, vaginal Lactobacilli: role of hydrogen peroxide production. J. Infect. Dis. 184, 1431–1436 (2001)
Search in Google Scholar Back to article
Verstraelen H., Vilchez-Vargas R., Desimpel F., Jauregui R., Vankeirsbilck N., Weyers S., Verhelst R., De Sutter P., Pieper D.H., Van De Wiele T.: Characterisation of the human uterine microbiome in non-pregnant women through deep sequencing of the V1-2 region of the 16S rRNA gene. Peer J. 4, e1602 (2016)
Search in Google Scholar Back to article
Wang H., Chen T., Chen Y., Luo T., Tan B., Chen H., Xin H.: Evaluation of the inhibitory effects of vaginal microorganisms on sperm motility invitro. Exp. Ther. Med. 19, 535–544 (2020)
Search in Google Scholar Back to article
Wee, B.A., Huston W.M. i wsp.: A retrospective pilot study to determine whether the reproductive tract microbiota differs between women with a history of infertility and fertile women. J. Obstet. Gynaecol. 58, 341–348 (2018)
Search in Google Scholar Back to article
Weng S.L., Huang H.D. i wsp.: Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PLoS One. 9, e110152 (2014)
Search in Google Scholar Back to article
Witkin S.S., Linhares I.M.: Why do Lactobacilli dominate the human vaginal microbiota? BJOG, 124, 606–611 (2017)
Search in Google Scholar Back to article
Zheng J., Lebeer S.A. i wsp.: Taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 70, 2782–2858 (2020)
Search in Google Scholar Back to article

The Influence Of The Reproductive System Microbiota On Female And Male Fertility. The Role Of Lactobacillus Bacteria

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