352155512022030120220301
2072-66431442022Feb21NutrientsNutrientsThe Use of Probiotics for Management and Improvement of Reproductive Eubiosis and Function.90210.3390/nu14040902Reproductive tract dysbiosis, due to the action of pathogens and/or unhealthy lifestyle, has been related to many reproductive diseases and disorders in mammalian species. Classically, such a problem has been confronted by the administration of antibiotics. Despite their effectiveness for controlling disease, treatments with antibiotics may negatively affect the fertility of males and females and, mainly, may induce antibiotic resistance. Accordingly, safer alternatives for maintaining reproductive system eubiosis, such as probiotics, are required. The present review summarizes the current knowledge on the biodiversity of the microbiota at the reproductive tract, possible changes in the case of dysbiosis, and their relationships with adequate reproductive health and functioning in both females and males. Afterwards, mechanisms of action and benefits of different probiotics are weighed since the biological activities of probiotics may provide a promising alternative to antibiotics for maintaining and restoring reproductive eubiosis and function. However, at present, it is still necessary for further research to focus on: (a) identifying mechanisms by which probiotics can affect reproductive processes; (b) the safety of probiotics to the host, specifically when consumed during sensitive reproductive windows such as pregnancy; and (c) the hazards instructions and regulatory rules required for marketing these biological-based therapies with sufficient safety. Thus, in this review, to draw a comprehensive overview with a relatively low number of clinical studies in this field, we showed the findings of studies performed either on human or animal models. This review strategy may help provide concrete facts on the eligible probiotic strains, probiotics colonization and transfer route, and prophylactic and/or therapeutic effects of different probiotic strains.HashemNesrein MNM0000-0003-0058-9671Department of Animal and Fish Production, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria 21545, Egypt.Gonzalez-BulnesAntonioA0000-0002-0917-4475Departamento de Produccion y Sanidad Animal, Facultad de Veterinaria, Universidad Cardenal Herrera-CEU, CEU Universities, C/Tirant lo Blanc, 7, Alfara del Patriarca, 46115 Valencia, Spain.engJournal ArticleReview20220221
SwitzerlandNutrients1015215952072-66430Anti-Bacterial AgentsIMAnimalsAnti-Bacterial Agentstherapeutic useDysbiosisdrug therapyFemaleHumansMicrobiotaPregnancyProbioticstherapeutic useReproductioneubiosisfertilitymammalsprobioticsThe authors declare no conflict of interest.20221142022282022215202222616202222760202233602022221epublish35215551PMC887819010.3390/nu14040902nu14040902Molina N.M., Sola-Leyva A., Saez-Lara M.J., Plaza-Diaz J., Tubic-Pavlovic A., Romero B., Clavero A., Mozas-Moreno J., Fontes J., Altmae S. New Opportunities for Endometrial Health by Modifying Uterine Microbial Composition: Present or Future. Biomolecules. 2020;10:593. doi: 10.3390/biom10040593.10.3390/biom10040593PMC722603432290428Pereira N., Hutchinson A.P., Lekovich J.P., Hobeika E., Elias R.T. Antibiotic prophylaxis for gynecologic procedures prior to and during the utilization of assisted reproductive technologies: A systematic review. J. Pathog. 2016;2016:4698314. doi: 10.1155/2016/4698314.10.1155/2016/4698314PMC480010327047692Silla A.J., Keogh L.M., Byrne P.G. Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered booroolong frog, Litoria booroolongensis. Reprod. Fertil. Dev. 2015;27:1147–1153. doi: 10.1071/RD14062.10.1071/RD1406224965921Rosenfeld C.S., Javurek A.B., Johnson S.A., Lei Z., Sumner L.W., Hess R.A. Seminal fluid metabolome and epididymal changes after antibiotic treatment in mice. Reproduction. 2018;156:1–10. doi: 10.1530/REP-18-0072.10.1530/REP-18-0072PMC666801929692359Moreno I., Simon C. Deciphering the effect of reproductive tract microbiota on human reproduction. Reprod. Med. Biol. 2019;18:40–50. doi: 10.1002/rmb2.12249.10.1002/rmb2.12249PMC633275230655720Dhanasekar K.R., Shilpa B., Gomathy N., Kundavi S. Prenatal Probiotics: The Way Forward in Prevention of Preterm Birth. J. Clin. Gynecol. Obstet. 2019;8:63–69. doi: 10.14740/jcgo571.10.14740/jcgo571Chen Y., Li Z., Tye K.D., Luo H., Tang X., Liao Y., Wang D., Zhou J., Yang P., Li Y., et al. Probiotic Supplementation During Human Pregnancy Affects the Gut Microbiota and Immune Status. Front. Cell. Infect. Microbiol. 2019;9:254. doi: 10.3389/fcimb.2019.00254.10.3389/fcimb.2019.00254PMC664651331380297Helli B., Kavianpour M., Ghaedi E., Dadfar M., Haghighian H.K. Probiotic effects on sperm parameters, oxidative stress index, inflammatory factors and sex hormones in infertile men. Hum. Fertil. 2020:1–9. doi: 10.1080/14647273.2020.1824080.10.1080/14647273.2020.182408032985280Maretti C., Cavallini G. The association of a probiotic with a prebiotic (Flortec, Bracco) to improve the quality/quantity of spermatozoa in infertile patients with idiopathic oligoasthenoteratospermia: A pilot study. Andrology. 2017;5:439–444. doi: 10.1111/andr.12336.10.1111/andr.1233628245352Quereda J.J., Garcia-Rosello E., Barba M., Moce M.L., Gomis J., Jimenez-Trigos E., Bataller E., Martinez-Bovi R., Garcia-Munoz A., Gomez-Martin A. Use of Probiotics in Intravaginal Sponges in Sheep: A Pilot Study. Animals. 2020;10:719. doi: 10.3390/ani10040719.10.3390/ani10040719PMC722276032326046Gu X.L., Li H., Song Z.H., Ding Y.N., He X., Fan Z.Y. Effects of isomaltooligosaccharide and Bacillus supplementation on sow performance, serum metabolites, and serum and placental oxidative status. Anim. Reprod. Sci. 2019;207:52–60. doi: 10.1016/j.anireprosci.2019.05.015.10.1016/j.anireprosci.2019.05.01531208846Mastromarino P., Macchia S., Meggiorini L., Trinchieri V., Mosca L., Perluigi M., Midulla C. Effectiveness of Lactobacillus-containing vaginal tablets in the treatment of symptomatic bacterial vaginosis. Clin. Microbiol. Infect. 2009;15:67–74. doi: 10.1111/j.1469-0691.2008.02112.x.10.1111/j.1469-0691.2008.02112.x19046169Bradshaw C.S., Pirotta M., De Guingand D., Hocking J.S., Morton A.N., Garland S.M., Fehler G., Morrow A., Walker S., Vodstrcil L.A. Efficacy of oral metronidazole with vaginal clindamycin or vaginal probiotic for bacterial vaginosis: Randomised placebo-controlled double-blind trial. PLoS ONE. 2012;7:e34540. doi: 10.1371/journal.pone.0034540.10.1371/journal.pone.0034540PMC331799822509319Peter S., Gartner M.A., Michel G., Ibrahim M., Klopfleisch R., Lubke-Becker A., Jung M., Einspanier R., Gabler C. Influence of intrauterine administration of Lactobacillus buchneri on reproductive performance and pro-inflammatory endometrial mRNA expression of cows with subclinical endometritis. Sci. Rep. 2018;8:5473. doi: 10.1038/s41598-018-22856-y.10.1038/s41598-018-22856-yPMC588302629615632Younge N., McCann J.R., Ballard J., Plunkett C., Akhtar S., Araújo-Pérez F., Murtha A., Brandon D., Seed P.C. Fetal exposure to the maternal microbiota in humans and mice. JCI Insight. 2019;4:e127806. doi: 10.1172/jci.insight.127806.10.1172/jci.insight.127806PMC679539831479427Sheldon I.M., Cronin J.G., Healey G.D., Gabler C., Heuwieser W., Streyl D., Bromfield J.J., Miyamoto A., Fergani C., Dobson H. Innate immunity and inflammation of the bovine female reproductive tract in health and disease. Reproduction. 2014;148:R41–R51. doi: 10.1530/REP-14-0163.10.1530/REP-14-016324890752Wee B.A., Thomas M., Sweeney E.L., Frentiu F.D., Samios M., Ravel J., Gajer P., Myers G., Timms P., Allan J.A. 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;58:341–348. doi: 10.1111/ajo.12754.10.1111/ajo.1275429280134Herath S., Williams E.J., Lilly S.T., Gilbert R.O., Dobson H., Bryant C.E., Sheldon I.M. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction. 2007;134:683–693. doi: 10.1530/REP-07-0229.10.1530/REP-07-0229PMC273581217965259Moreno I., Franasiak J.M. Endometrial microbiota—New player in town. Fertil. Steril. 2017;108:32–39. doi: 10.1016/j.fertnstert.2017.05.034.10.1016/j.fertnstert.2017.05.03428602480Pelzer E.S., 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/s10482-017-0992-6.10.1007/s10482-017-0992-629299770Fang R.-L., Chen L.-X., Shu W.-S., Yao S.-Z., Wang S.-W., Chen Y.-Q. Barcoded sequencing reveals diverse intrauterine microbiomes in patients suffering with endometrial polyps. Am. J. Transl. Res. 2016;8:1581.PMC485964227186283Rizzo A.E., Gordon J.C., Berard A.R., Burgener A.D., Avril S. The Female Reproductive Tract Microbiome—Implications for Gynecologic Cancers and Personalized Medicine. J. Pers. Med. 2021;11:546. doi: 10.3390/jpm11060546.10.3390/jpm11060546PMC823121234208337Walther-António M.R., Chen J., Multinu F., Hokenstad A., Distad T.J., Cheek E.H., Keeney G.L., Creedon D.J., Nelson H., Mariani A. Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Med. 2016;8:1–15. doi: 10.1186/s13073-016-0368-y.10.1186/s13073-016-0368-yPMC512333027884207Walsh D.M., Hokenstad A.N., Chen J., Sung J., Jenkins G.D., Chia N., Nelson H., Mariani A., Walther-Antonio M.R. Postmenopause as a key factor in the composition of the Endometrial Cancer Microbiome (ECbiome) Sci. Rep. 2019;9:19213. doi: 10.1038/s41598-019-55720-8.10.1038/s41598-019-55720-8PMC691577831844128Koedooder 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. Update. 2019;25:298–325. doi: 10.1093/humupd/dmy048.10.1093/humupd/dmy04830938752Pelzer E.S., Allan J.A., Waterhouse M.A., Ross T., Beagley K.W., Knox C.L. Microorganisms within human follicular fluid: Effects on IVF. PLoS ONE. 2013;8:e59062. doi: 10.1371/journal.pone.0059062.10.1371/journal.pone.0059062PMC359521923554970Halis G., Arici A. Endometriosis and inflammation in infertility. Ann. N. Y. Acad. Sci. 2004;1034:300–315. doi: 10.1196/annals.1335.032.10.1196/annals.1335.03215731321López-Moreno A., Aguilera M. Vaginal probiotics for reproductive health and related dysbiosis: Systematic review and meta-analysis. J. Clin. Med. 2021;10:1461. doi: 10.3390/jcm10071461.10.3390/jcm10071461PMC803756733918150Fuochi V., Li Volti G., Furneri P.M. Commentary: Lactobacilli dominance and vaginal pH: Why is the human vaginal microbiome unique? Front. Microbiol. 2017;8:1815. doi: 10.3389/fmicb.2017.01815.10.3389/fmicb.2017.01815PMC562218928993762Russo R., Karadja E., De Seta F. Evidence-based mixture containing Lactobacillus strains and lactoferrin to prevent recurrent bacterial vaginosis: A double blind, placebo controlled, randomised clinical trial. Benef. Microbes. 2019;10:19–26. doi: 10.3920/BM2018.0075.10.3920/BM2018.007530525953Altmäe S., Franasiak J.M., Mändar R. The seminal microbiome in health and disease. Nat. Rev. Urol. 2019;16:703–721. doi: 10.1038/s41585-019-0250-y.10.1038/s41585-019-0250-y31732723Ahmadi M.H., Mirsalehian A., Gilani M.A.S., Bahador A., Talebi M. Asymptomatic infection with Mycoplasma hominis negatively affects semen parameters and leads to male infertility as confirmed by improved semen parameters after antibiotic treatment. Urology. 2017;100:97–102. doi: 10.1016/j.urology.2016.11.018.10.1016/j.urology.2016.11.01827871827Monteiro C., Marques P.I., Cavadas B., Damião I., Almeida V., Barros N., Barros A., Carvalho F., Gomes S., Seixas S. Characterization of microbiota in male infertility cases uncovers differences in seminal hyperviscosity and oligoasthenoteratozoospermia possibly correlated with increased prevalence of infectious bacteria. Am. J. Reprod. Immunol. 2018;79:e12838. doi: 10.1111/aji.12838.10.1111/aji.1283829500854Mändar R., Punab M., Borovkova N., Lapp E., Kiiker R., Korrovits P., Metspalu A., Krjutškov K., Nolvak H., Preem J.-K. Complementary seminovaginal microbiome in couples. Res. Microbiol. 2015;166:440–447. doi: 10.1016/j.resmic.2015.03.009.10.1016/j.resmic.2015.03.00925869222Rodrigues N., Kästle J., Coutinho T., Amorim A., Campos G., Santos V., Marques L., Timenetsky J., De Farias S. Qualitative analysis of the vaginal microbiota of healthy cattle and cattle with genital-tract. Gen. Mol. Res. 2015;14:6518–6528. doi: 10.4238/2015.June.12.4.10.4238/2015.June.12.426125856Shpigel N., Adler-Ashkenazy L., Scheinin S., Goshen T., Arazi A., Pasternak Z., Gottlieb Y. Characterization and identification of microbial communities in bovine necrotic vulvovaginitis. Vet. J. 2017;219:34–39. doi: 10.1016/j.tvjl.2016.12.002.10.1016/j.tvjl.2016.12.00228093107Wang Y., Wang J., Li H., Fu K., Pang B., Yang Y., Liu Y., Tian W., Cao R. Characterization of the cervical bacterial community in dairy cows with metritis and during different physiological phases. Theriogenology. 2018;108:306–313. doi: 10.1016/j.theriogenology.2017.12.028.10.1016/j.theriogenology.2017.12.02829284157Saleh M., Haraki Nezhad M.T., Salmani V. Detection of some bacterial causes of abortion in Afshari sheep using real time PCR detection and sensitivity assessment of campylobacter primers. Agric. Biotechnol. J. 2014;6:107–120.Younis N., Mahasneh A. Probiotics and the envisaged role in treating human infertility. Middle East Fertil. Soc. J. 2020;25:33. doi: 10.1186/s43043-020-00039-y.10.1186/s43043-020-00039-yLopez-Moreno A., Aguilera M. Probiotics Dietary Supplementation for Modulating Endocrine and Fertility Microbiota Dysbiosis. Nutrients. 2020;12:757. doi: 10.3390/nu12030757.10.3390/nu12030757PMC714645132182980Cao M., Li Y., Wu Q.J., Zhang P., Li W.T., Mao Z.Y., Wu D.M., Jiang X.M., Zhuo Y., Fang Z.F. Effects of dietary Clostridium butyricum addition to sows in late gestation and lactation on reproductive performance and intestinal microbiota. J. Anim. Sci. 2019;97:3426–3439. doi: 10.1093/jas/skz186.10.1093/jas/skz186PMC666726831233597Kitaya K., Matsubayashi H., Takaya Y., Nishiyama R., Yamaguchi K., Takeuchi T., Ishikawa T. Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. Am. J. Reprod. Immunol. 2017;78:e12719. doi: 10.1111/aji.12719.10.1111/aji.1271928608596McQueen D.B., Bernardi L.A., Stephenson M.D. Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil. Steril. 2014;101:1026–1030. doi: 10.1016/j.fertnstert.2013.12.031.10.1016/j.fertnstert.2013.12.03124462055Cicinelli E., Matteo M., Trojano G., Mitola P.C., Tinelli R., Vitagliano A., Crupano F.M., Lepera A., Miragliotta G., Resta L. Chronic endometritis in patients with unexplained infertility: Prevalence and effects of antibiotic treatment on spontaneous conception. Am. J. Reprod. Immunol. 2018;79:e12782. doi: 10.1111/aji.12782.10.1111/aji.1278229135053Zhang Y., Xu H., Liu Y., Zheng S., Zhao W., Wu D., Lei L., Chen G. Confirmation of chronic endometritis in repeated implantation failure and success outcome in IVF-ET after intrauterine delivery of the combined administration of antibiotic and dexamethasone. Am. J. Reprod. Immunol. 2019;82:e13177. doi: 10.1111/aji.13177.10.1111/aji.1317731373128Weinreb E.B., Cholst I.N., Ledger W.J., Danis R.B., Rosenwaks Z. Should all oocyte donors receive prophylactic antibiotics for retrieval? Fertil. Steril. 2010;94:2935–2937. doi: 10.1016/j.fertnstert.2010.05.054.10.1016/j.fertnstert.2010.05.05420633881Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014;17:506–514. doi: 10.1038/nrgastro.2014.66.10.1038/nrgastro.2014.6624912386Khalesi S., Bellissimo N., Vandelanotte C., Williams S., Stanley D., Irwin C. A review of probiotic supplementation in healthy adults: Helpful or hype? Eur. J. Clin. Nutr. 2019;73:24–37. doi: 10.1038/s41430-018-0135-9.10.1038/s41430-018-0135-929581563Trush E.A., Poluektova E.A., Beniashvilli A.G., Shifrin O.S., Poluektov Y.M., Ivashkin V.T. The evolution of human probiotics: Challenges and prospects. Probiotics Antimicrob. Proteins. 2020;12:1291–1299. doi: 10.1007/s12602-019-09628-4.10.1007/s12602-019-09628-431907861Pino A., Bartolo E., Caggia C., Cianci A., Randazzo C.L. Detection of vaginal lactobacilli as probiotic candidates. Sci. Rep. 2019;9:3355. doi: 10.1038/s41598-019-40304-3.10.1038/s41598-019-40304-3PMC639933630833631Niu C., Cheng C., Liu Y., Huang S., Fu Y., Li P. Transcriptome profiling analysis of bovine vaginal epithelial cell response to an isolated lactobacillus strain. Msystems. 2019;4:e00268-19. doi: 10.1128/mSystems.00268-19.10.1128/mSystems.00268-19PMC673909931506261Chenoll E., Moreno I., Sanchez M., Garcia-Grau I., Silva A., Gonzalez-Monfort M., Genoves S., Vilella F., Seco-Durban C., Simon C., et al. Selection of New Probiotics for Endometrial Health. Front. Cell. Infect. Microbiol. 2019;9:114. doi: 10.3389/fcimb.2019.00114.10.3389/fcimb.2019.00114PMC648127931058101Ametaj B., Iqbal S., Selami F., Odhiambo J., Wang Y., Gänzle M., Dunn S., Zebeli Q. Intravaginal administration of lactic acid bacteria modulated the incidence of purulent vaginal discharges, plasma haptoglobin concentrations, and milk production in dairy cows. Res. Vet. Sci. 2014;96:365–370. doi: 10.1016/j.rvsc.2014.02.007.10.1016/j.rvsc.2014.02.00724612560Poutahidis T., Springer A., Levkovich T., Qi P., Varian B.J., Lakritz J.R., Ibrahim Y.M., Chatzigiagkos A., Alm E.J., Erdman S.E. Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS ONE. 2014;9:e84877. doi: 10.1371/journal.pone.0084877.10.1371/journal.pone.0084877PMC387936524392159Zhou Z., Wang W., Liu W., Gatlin III D.M., Zhang Y., Yao B., Ringø E. Identification of highly-adhesive gut Lactobacillus strains in zebrafish (Danio rerio) by partial rpoB gene sequence analysis. Aquaculture. 2012;370:150–157. doi: 10.1016/j.aquaculture.2012.10.018.10.1016/j.aquaculture.2012.10.018Valcarce D., Genovés S., Riesco M., Martorell P., Herráez M., Ramón D., Robles V. Probiotic administration improves sperm quality in asthenozoospermic human donors. Benef. Microbes. 2017;8:193–206. doi: 10.3920/BM2016.0122.10.3920/BM2016.012228343402Sashihara T., Sueki N., Furuichi K., Ikegami S. Effect of growth conditions of Lactobacillus gasseri OLL2809 on the immunostimulatory activity for production of interleukin-12 (p70) by murine splenocytes. Int. J. Food Microbiol. 2007;120:274–281. doi: 10.1016/j.ijfoodmicro.2007.09.003.10.1016/j.ijfoodmicro.2007.09.00317936392Inatomi T., Otomaru K. Effect of dietary probiotics on the semen traits and antioxidative activity of male broiler breeders. Sci. Rep. 2018;8:5874. doi: 10.1038/s41598-018-24345-8.10.1038/s41598-018-24345-8PMC589734429651158Jeżewska-Frąckowiak J., Seroczyńska K., Banaszczyk J., Jedrzejczak G., Żylicz-Stachula A., Skowron P.M. The promises and risks of probiotic Bacillus species. Acta Biochim. Pol. 2018;65:509–519. doi: 10.18388/abp.2018_2652.10.18388/abp.2018_265230521647Gaziano R., Sabbatini S., Roselletti E., Perito S., Monari C. Saccharomyces cerevisiae-Based Probiotics as Novel Antimicrobial Agents to Prevent and Treat Vaginal Infections. Front. Microbiol. 2020;11:718. doi: 10.3389/fmicb.2020.00718.10.3389/fmicb.2020.00718PMC718637932373104Pericolini E., Gabrielli E., Ballet N., Sabbatini S., Roselletti E., Cayzeele Decherf A., Pélerin F., Luciano E., Perito S., Jüsten P. Therapeutic activity of a Saccharomyces cerevisiae-based probiotic and inactivated whole yeast on vaginal candidiasis. Virulence. 2017;8:74–90. doi: 10.1080/21505594.2016.1213937.10.1080/21505594.2016.1213937PMC596321227435998Buggio L., Somigliana E., Borghi A., Vercellini P. Probiotics and vaginal microecology: Fact or fancy? BMC Womens Health. 2019;19:25. doi: 10.1186/s12905-019-0723-4.10.1186/s12905-019-0723-4PMC635746430704451Bohbot J., Cardot J. Vaginal impact of the oral administration of total freeze-dried culture of LCR 35 in healthy women. Infect. Dis. Obstet. Gynecol. 2012;2012:503648. doi: 10.1155/2012/503648.10.1155/2012/503648PMC337306222701297Antonio M.A., Meyn L.A., Murray P.J., Busse B., Hillier S.L. Vaginal colonization by probiotic Lactobacillus crispatus CTV-05 is decreased by sexual activity and endogenous Lactobacilli. J. Infect. Dis. 2009;199:1506–1513. doi: 10.1086/598686.10.1086/59868619331578Hemmerling A., Harrison W., Schroeder A., Park J., Korn A., Shiboski S., Foster-Rosales A., Cohen C.R. Phase 2a study assessing colonization efficiency, safety, and acceptability of Lactobacillus crispatus CTV-05 in women with bacterial vaginosis. Sex. Transm. Dis. 2010;37:745–750. doi: 10.1097/OLQ.0b013e3181e50026.10.1097/OLQ.0b013e3181e5002620644497El-Deeb W.M., Fayez M., Elsohaby I., Ghoneim I., Al-Marri T., Kandeel M., ElGioushy M. Isolation and characterization of vaginal Lactobacillus spp. in dromedary camels (Camelus dromedarius): In vitro evaluation of probiotic potential of selected isolates. PeerJ. 2020;8:e8500. doi: 10.7717/peerj.8500.10.7717/peerj.8500PMC700773232071813Kim J.-M., Park Y.J. Probiotics in the prevention and treatment of postmenopausal vaginal infections. J. Menopausal Med. 2017;23:139–145. doi: 10.6118/jmm.2017.23.3.139.10.6118/jmm.2017.23.3.139PMC577052229354612Srinivasan S., Hoffman N.G., Morgan M.T., Matsen F.A., Fiedler T.L., Hall R.W., Ross F.J., McCoy C.O., Bumgarner R., Marrazzo J.M. Bacterial communities in women with bacterial vaginosis: High resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS ONE. 2012;7:e37818. doi: 10.1371/journal.pone.0037818.10.1371/journal.pone.0037818PMC337771222719852Coudeyras S., Jugie G., Vermerie M., Forestier C. Adhesion of human probiotic Lactobacillus rhamnosus to cervical and vaginal cells and interaction with vaginosis-associated pathogens. Infect. Dis. Obstet. Gynecol. 2008;2008:549640. doi: 10.1155/2008/549640.10.1155/2008/549640PMC263164919190778Wang Y., Wu Y., Wang Y., Xu H., Mei X., Yu D., Wang Y., Li W. Antioxidant properties of probiotic bacteria. Nutrients. 2017;9:521. doi: 10.3390/nu9050521.10.3390/nu9050521PMC545225128534820Cani P.D., Knauf C. How gut microbes talk to organs: The role of endocrine and nervous routes. Mol. Metab. 2016;5:743–752. doi: 10.1016/j.molmet.2016.05.011.10.1016/j.molmet.2016.05.011PMC500414227617197Sudo N., Chida Y., Aiba Y., Sonoda J., Oyama N., Yu X.N., Kubo C., Koga Y. Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J. Physiol. 2004;558:263–275. doi: 10.1113/jphysiol.2004.063388.10.1113/jphysiol.2004.063388PMC166492515133062Marcone V., Calzolari E., Bertini M. Effectiveness of vaginal administration of Lactobacillus rhamnosus following conventional metronidazole therapy: How to lower the rate of bacterial vaginosis recurrences. New Microbiol. 2008;31:429.18843900Barthow C., Wickens K., Stanley T., Mitchell E.A., Maude R., Abels P., Purdie G., Murphy R., Stone P., Kang J. The Probiotics in Pregnancy Study (PiP Study): Rationale and design of a double-blind randomised controlled trial to improve maternal health during pregnancy and prevent infant eczema and allergy. BMC Pregnancy Childbirth. 2016;16:133. doi: 10.1186/s12884-016-0923-y.10.1186/s12884-016-0923-yPMC489189827255079Cayzeele-Decherf A., Pélerin F., Jüsten P. Saccharomyces cerevisiae CNCM I-3856 as a natural breakthrough for vaginal health: A clinical study. Med. J. Obstet. Gynecol. 2017;5:1112.Ahmadzadeh L., Hosseinkhani A., Kia H.D. Effect of supplementing a diet with monensin sodium and Saccharomyces Cerevisiae on reproductive performance of Ghezel ewes. Anim. Reprod. Sci. 2018;188:93–100. doi: 10.1016/j.anireprosci.2017.11.013.10.1016/j.anireprosci.2017.11.01329137911Genis S., Sanchez-Chardi A., Bach A., Fabregas F., Aris A. A combination of lactic acid bacteria regulates Escherichia coli infection and inflammation of the bovine endometrium. J. Dairy Sci. 2017;100:479–492. doi: 10.3168/jds.2016-11671.10.3168/jds.2016-1167127837977Deng Q., Odhiambo J., Farooq U., Lam T., Dunn S., Ametaj B. Intravaginal probiotics modulated metabolic status and improved milk production and composition of transition dairy cows. J. Anim. Sci. 2016;94:760–770. doi: 10.2527/jas.2015-9650.10.2527/jas.2015-965027065146Kritas S., Marubashi T., Filioussis G., Petridou E., Christodoulopoulos G., Burriel A., Tzivara A., Theodoridis A., Pískoriková M. Reproductive performance of sows was improved by administration of a sporing bacillary probiotic (Bacillus subtilis C-3102) J. Anim. Sci. 2015;93:405–413. doi: 10.2527/jas.2014-7651.10.2527/jas.2014-765125568382Hashem N.M., Gonzalez-Bulnes A. Nanotechnology and Reproductive Management of Farm Animals: Challenges and Advances. Animals. 2021;11:1932. doi: 10.3390/ani11071932.10.3390/ani11071932PMC830031334209536Deng F., McClure M., Rorie R., Wang X., Chai J., Wei X., Lai S., Zhao J. The vaginal and fecal microbiomes are related to pregnancy status in beef heifers. J. Anim. Sci. Biotechnol. 2019;10:92. doi: 10.1186/s40104-019-0401-2.10.1186/s40104-019-0401-2PMC690951831857897Mizubuchi H., Yajima T., Aoi N., Tomita T., Yoshikai Y. Isomalto-oligosaccharides polarize Th1-like responses in intestinal and systemic immunity in mice. J. Nutr. 2005;135:2857–2861. doi: 10.1093/jn/135.12.2857.10.1093/jn/135.12.285716317132Mao K., Liu L., Mo T., Pan H., Liu H. Preparation, characterization, and antioxidant activity of an isomaltooligosaccharide–iron complex (IIC) J. Carbohydr. Chem. 2015;34:430–443. doi: 10.1080/07328303.2015.1085551.10.1080/07328303.2015.1085551Guo Y., Du X., Bian Y., Wang S. Chronic unpredictable stress-induced reproductive deficits were prevented by probiotics. Reprod. Biol. 2020;20:175–183. doi: 10.1016/j.repbio.2020.03.005.10.1016/j.repbio.2020.03.00532265160Dardmeh F., Alipour H., Gazerani P., Van der Horst G., Brandsborg E., Nielsen H.I. Lactobacillus rhamnosus PB01 (DSM 14870) supplementation affects markers of sperm kinematic parameters in a diet-induced obesity mice model. PLoS ONE. 2017;12:e0185964. doi: 10.1371/journal.pone.0185964.10.1371/journal.pone.0185964PMC563462529016685Yang J., Wen M., Pan K., Shen K., Yang R., Liu Z. Protective effects of dietary co-administration of probiotic Lactobacillus casei on CP-induced reproductive dysfunction in adult male Kunming mice. Vet. Res. 2012;5:110–119.Tremellen K., Pearce K. Probiotics to improve testicular function (Andrology 5: 439–444, 2017)—A comment on mechanism of action and therapeutic potential of probiotics beyond reproduction. Andrology. 2017;5:1052–1053. doi: 10.1111/andr.12400.10.1111/andr.1240028914502Ommati M.M., Li H., Jamshidzadeh A., Khoshghadam F., Retana-Márquez S., Lu Y., Farshad O., Nategh Ahmadi M.H., Gholami A., Heidari R. The crucial role of oxidative stress in non-alcoholic fatty liver disease-induced male reproductive toxicity: The ameliorative effects of Iranian indigenous probiotics. Naunyn-Schmiedebergs Arch. Pharmacol. 2022;395:247–265. doi: 10.1007/s00210-021-02177-0.10.1007/s00210-021-02177-034994824Javurek A.B., Spollen W.G., Johnson S.A., Bivens N.J., Bromert K.H., Givan S.A., Rosenfeld C.S. Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice. Reprod. Fertil. Dev. 2017;29:1602–1612. doi: 10.1071/RD16119.10.1071/RD1611927569192Nader-Macías M.E.F., De Gregorio P.R., Silva J.A. Probiotic lactobacilli in formulas and hygiene products for the health of the urogenital tract. Pharmacol. Res. Perspect. 2021;9:e00787. doi: 10.1002/prp2.787.10.1002/prp2.787PMC849145634609059Mattia A., Merker R. Regulation of probiotic substances as ingredients in foods: Premarket approval or “generally recognized as safe” notification. Clin. Infect. Dis. 2008;46:S115–S118. doi: 10.1086/523329.10.1086/52332918181714Baldassarre M.E., Palladino V., Amoruso A., Pindinelli S., Mastromarino P., Fanelli M., Di Mauro A., Laforgia N. Rationale of Probiotic Supplementation during Pregnancy and Neonatal Period. Nutrients. 2018;10:1693. doi: 10.3390/nu10111693.10.3390/nu10111693PMC626757930404227Kuitunen M., Kukkonen K., Savilahti E. Pro-and prebiotic supplementation induces a transient reduction in hemoglobin concentration in infants. J. Pediatr. Gastroenterol. Nutr. 2009;49:626–630. doi: 10.1097/MPG.0b013e31819de849.10.1097/MPG.0b013e31819de84919644396Czarnecki-Maulden G.L. Effect of dietary modulation of intestinal microbiota on reproduction and early growth. Theriogenology. 2008;70:286–290. doi: 10.1016/j.theriogenology.2008.05.041.10.1016/j.theriogenology.2008.05.04118533245Hoffmann D.E., Fraser C.M., Palumbo F., Ravel J., Rowthorn V., Schwartz J. Probiotics: Achieving a better regulatory fit. Food Drug Law J. 2014;69:237.PMC611417025163211Cordaillat-Simmons M., Rouanet A., Pot B. Live biotherapeutic products: The importance of a defined regulatory framework. Exp. Mol. Med. 2020;52:1397–1406. doi: 10.1038/s12276-020-0437-6.10.1038/s12276-020-0437-6PMC808058332908212Nagy Z.K., Wagner I., Suhajda Á., Tobak T., Harasztos A.H., Vigh T., Sóti P.L., Pataki H., Molnár K., Marosi G. Nanofibrous solid dosage form of living bacteria prepared by electrospinning. eXPRESS Polym. Lett. 2014;8:352–361. doi: 10.3144/expresspolymlett.2014.39.10.3144/expresspolymlett.2014.39Li T., Zhang Y., Song J., Chen L., Du M., Mao X. Yogurt Enriched with Inulin Ameliorated Reproductive Functions and Regulated Gut Microbiota in Dehydroepiandrosterone-Induced Polycystic Ovary Syndrome Mice. Nutrients. 2022;14:279. doi: 10.3390/nu14020279.10.3390/nu14020279PMC878181235057459Zakariaee H., Sudagar M., Hosseini S.S., Paknejad H., Baruah K. In vitro Selection of Synbiotics and in vivo Investigation of Growth Indices, Reproduction Performance, Survival, and Ovarian Cyp19α Gene Expression in Zebrafish Danio rerio. Front. Microbiol. 2021;12:758758. doi: 10.3389/fmicb.2021.758758.10.3389/fmicb.2021.758758PMC852110434671338Nataraj B.H., Ali S.A., Behare P.V., Yadav H. Postbiotics-parabiotics: The new horizons in microbial biotherapy and functional foods. Microb. Cell Factories. 2020;19:168. doi: 10.1186/s12934-020-01426-w.10.1186/s12934-020-01426-wPMC744167932819443