El microbioma y su relación con la fisiología de la reproducción: Influencia de los antibióticos y probióticos

  1. 1 Universidad Complutense de Madrid

    Universidad Complutense de Madrid

    Madrid, España

    ROR 02p0gd045

  2. 2 Universidad Politécnica de Madrid

    Universidad Politécnica de Madrid

    Madrid, España

    ROR https://ror.org/03n6nwv02

Anales de la Real Academia de Ciencias Veterinarias

Year of publication: 2020

Volume: 28

Issue: 28

Pages: 127-162

Type: Article


In recent years, there has been a huge revolution in the scientific world with the discovery of the role of the microbiome in practically all areas of physiology, and of course also, in the physiology of reproduc-tion. The finding of communities of microorganisms in the female and male reproductive systems, leads to the hypothesis of the possible role of a reproductive microbiome (together with that of other locations, such as the gastrointestinal system), in the quality of sperm, oocytes or embryos and in reproductive mechanisms, such as fertilization, embryo implanta-tion, or gestation, which ultimately affect the success of reproduction. Therefore, it is essential to maintain the homeostasis of the microbiota to positively influence the reproductive health and reproductive success of the individual, and even the health of their offspring. The use of antibio-tics and other alternative substances, such as probiotics, can affect the microbiome. It can lead to changes that are harmful or beneficial to the animal's health and its reproduction. In this sense, resistance to antibio-tics is a growing global concern in human and veterinary medicine. It is necessary to eliminate or reduce the use of antibiotics and to replace them with other alternative compounds, although it is important to know how they affect the original microbiome of individuals and how its changes modify physiological mechanisms and then productive traits. In this work, the role of the microbiome will be reviewed as well as the use of antibiotics and probiotics, in the physiology of reproduction and its ef-fects on animal production.

Bibliographic References

  • Dai Z, Wu Z, Hang S, Zhu W, Wu G. 2014. Amino acid metabo-lism in intestinal bacteria and its potential implications for mam-malian reproduction. Mol Hum Reprod. 21:389–409. https://doi.org/10.1093/molehr/gav003.
  • Nuriel-Ohayon M, Neuman H, Koren O. 2016. Microbial changes during pregnancy, birth, and infancy. Front Microbiol. 7:1–13. https://doi.org/10.3389/fmicb.2016.01031.
  • Cho I, Blaser MJ. 2012. The Human Microbiome: at the interface of health and disease. Nat Rev Genet. 13:260–70. https://doi.org/10.1038/nrg3182.The.
  • Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J. 2016. The Microbiome of Animals: Implications for Conservation Biology. Int J Genomics. https://doi.org/10.1155/2016/5304028.
  • O’Callaghan TF, Ross RP, Stanton C, Clarke G. 2016. The gut microbiome as a virtual endocrine organ with implications for farm and domestic animal endocrinology. Domest Anim Endocri-nol. 56:S44–55. https://doi.org/10.1016/j.domaniend.2016.05.003.
  • Berg G, Rybakova D, Fischer D, Cernava T, Vergès MCC, Char-les T, Chen X, Cocolin L, Eversole K, Herrero Corral G, Kazou M, Kinkel L, Lange L, Lima N, Loy A, Macklin JA, Maguin E, Mauchline T, McClure R, Mitter B, Ryan M, Sarand I, Smidt H, Schelkle B, Roume H, Kiran GS, Selvin J, Soares R, de Souza C, van Overbeek L, Singh BK, Wagner M, Walsh A, Sessitsch A, Schloter M. 2020. Microbiome definition re-visited: old concepts and new challenges. Microbiome. 8(1):1–22. Doi: 10.1186/ s40168-020-00875-0.
  • Power ML, Quaglieri C, Schulkin J. 2017. Reproductive Micro-biomes: A New Thread in the Microbial Network. Reprod Sci. 24:1482–92. https://doi.org/10.1177/1933719117698577.
  • Mills S, Stanton C, Lane JA, Smith GJ, Ross RP. 2019. Precision nutrition and the microbiome, part I: Current state of the science. Nutrients. 11:1–45. https://doi.org/10.3390/nu11040923.
  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with in-creased capacity for energy harvest. Nature. 444:1027–31. https://doi.org/10.1038/nature05414.
  • Dibner JJ, Richards JD. 2005. Antibiotic growth promoters in agri-culture: History and mode of action. Poult Sci. 84:634–43. https://doi.org/10.1093/ps/84.4.634.
  • Mingmongkolchai S, Panbangred W. 2018. Bacillus probiotics: an alternative to antibiotics for livestock production. J Appl Micro-biol. 124:1334–46. Doi: 10.1111/jam.13690.
  • Da Costa PM, Loureiro L, Matos AJF. 2013. Transfer of multi-drug-resistant bacteria between intermingled ecological niches: The interface between humans, animals and the environment. Int J Environ Res Public Health. 10:278–94. https://doi.org/10.3390/ijerph10010278.
  • Marshall BM, Levy SB. 2011. Food animals and antimicrobials: Impacts on human health. Clin Microbiol Rev. 24:718–33. https://doi.org/10.1128/CMR.00002-11.
  • OMS. Antimicrobial resistance n.d. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance.
  • Al-Nasiry S, Ambrosino E, Schlaepfer M, Morré SA, Wieten L, Voncken JW, Voncken W, Spinelli M, Mueller M, Kramer BW. 2020. The Interplay Between Reproductive Tract Microbiota and Immunological System in Human Reproduction. Front Immunol. 11:1–20. https://doi.org/10.3389/fimmu.2020.00378.
  • Ikeda-Ohtsubo W, Brugman S, Warden CH, Rebel JMJ, Folkerts G, Pieterse CMJ. 2018. How Can We Define “Optimal Micro-biota?”: A Comparative Review of Structure and Functions of Mi-crobiota of Animals, Fish, and Plants in Agriculture. Front Nutr. 5:1–18. https://doi.org/10.3389/fnut.2018.00090.
  • Matějková T, Hájková P, Stopková R, Stanko M, Martin JF, Krei-singer J, Stopka P. 2020. Oral and vaginal microbiota in selected field mice of the genus Apodemus: a wild population study. Sci Rep. 10:1–11. https://doi.org/10.1038/s41598-020-70249-x.
  • Comizzoli P, Power ML. 2019. Reproductive Microbiomes in Wild Animal Species: A New Dimension in Conservation Bio-logy. Adv Exp Med Biol. Pp. 225–40. Doi: 10.1007/978-3-030-23633-5_8.
  • Grenham S, Clarke G, Cryan JF, Dinan TG. 2011. Brain-gut-mi-crobe communication in health and disease. Front Physiol. 2:1–15. https://doi.org/10.3389/fphys.2011.00094.
  • Rowe M, Veerus L, Trosvik P, Buckling A, Pizzari T. 2020. The Reproductive Microbiome: An Emerging Driver of Sexual Selec-tion, Sexual Conflict, Mating Systems, and Reproductive Isola-tion. Trends Ecol Evol. 35:220–34. https://doi.org/10.1016/j.tree.2019.11.004.
  • Einenkel R, Zygmunt M, Muzzio DO. 2019. Microorganisms in the healthy upper reproductive tract: from denial to beneficial as-signments for reproductive biology. Reprod Biol. 19:113–8. https://doi.org/10.1016/j.repbio.2019.04.001.
  • Tomaiuolo R, Veneruso I, Cariati F, D’argenio V. 2020. Micro-biota and human reproduction: The case of female infertility. High-Throughput. 9:1–15. https://doi.org/10.3390/ht9020012.
  • Heil BA, Paccamonti DL, Sones JL. 2019. Role for the mamma-lian female reproductive tract microbiome in pregnancy outcomes. Physiol Genomics. 51:390–9. https://doi.org/10.1152/physiolgenomics.00045.2019.
  • Baud D, Pattaroni C, Vulliemoz N, Castella V, Marsland BJ, Sto-janov M. 2019. Sperm microbiota and its impact on semen para-meters. Front Microbiol. 10:1–9. https://doi.org/10.3389/fmicb.2019.00234.
  • Chen C, Song X, Wei W, Zhong H, Dai J, Lan Z, Li F, Yu X, Feng Q, Wang Z, Xie H, Chen X, Zeng C, Wen B, Zeng L, Du H, Tang H, Xu C, Xia Y, Xia H, Yang H, Wang J, Wang J, Madsen L, Brix S, Kristiansen K, Xu X, Li J, Wu R, Jia H. 2017. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 8. https://doi.org/10.1038/s41467-017-00901-0.
  • Pelzer ES, Allan JA, Cunningham K, Mengersen K, Allan JM, Launchbury T, Beagley K, Knox CL. 2011. Microbial coloniza-tion of follicular fluid: Alterations in cytokine expression and ad-verse assisted reproduction technology outcomes. Hum Reprod. 26:1799–812. https://doi.org/10.1093/humrep/der108.
  • Baker JM, Chase DM, Herbst-Kralovetz MM. 2018. Uterine mi-crobiota: Residents, tourists, or invaders? Front Immunol. 9. https://doi.org/10.3389/fimmu.2018.00208.
  • Moreno I, Simon C. 2018. Relevance of assessing the uterine mi-crobiota in infertility. Fertil Steril. 110:337–43. https://doi.org/10.1016/j.fertnstert.2018.04.041.
  • Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J VJ. 2014. The placenta harbors a unique microbiome. Sci Transl Med. 6: 237. Doi: 10.1126/scitranslmed.3008599.
  • Moore SG, Ericsson AC, Poock SE, Melendez P, Lucy MC. 2017. Hot topic: 16S rRNA gene sequencing reveals the microbiome of the virgin and pregnant bovine uterus. J Dairy Sci. 100: 4953–60. https://doi.org/10.3168/jds.2017-12592.
  • Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q, Roehl KA, Nelson DM, Macones GA, Mysorekar IU. 2013. Identifica-tion of intracellular bacteria in the basal plate of the human pla-centa in term and preterm gestations. Am J Obstet Gynecol. 208:226.e1-226.e7. https://doi.org/10.1016/j.ajog.2013.01.018.
  • de Goffau MC, Lager S, Sovio U, Gaccioli F, Cook E, Peacock SJ, Parkhill J, Charnock-Jones DS, Smith GCS. 2019. Human pla-centa has no microbiome but can contain potential pathogens. Na-ture. 572:329–34. https://doi.org/10.1038/s41586-019-1451-5.
  • Alfano M, Ferrarese R, Locatelli I, Ventimiglia E, Ippolito S, Ga-llina P, Cesana D, Canducci F, Pagliardini L, Viganò P, Clementi M, Nebuloni M, Montorsi F, Salonia A. 2018. Testicular micro-biome in azoospermic men’first evidence of the impact of an alte-red microenvironment. Hum Reprod. 33:1212–7. https://doi.org/10.1093/humrep/dey116.
  • Hou D, Zhou X, Zhong X, Settles ML, Herring J, Wang L, Abdo Z, Forney LJ, Xu C. 2013. Microbiota of the seminal fluid from healthy and infertile men. Fertil Steril. 100:1261–9. https://doi.org/10.1016/j.fertnstert.2013.07.1991.
  • Javurek AB, Spollen WG, Ali AMM, Johnson SA, Lubahn DB, Bivens NJ, Bromert KH, Ellersieck MR, Givan SA, Rosenfeld CS. 2016. Discovery of a Novel Seminal Fluid Microbiome and In-fluence of Estrogen Receptor Alpha Genetic Status. Sci Rep. 6:1–14. https://doi.org/10.1038/srep23027.
  • Schulze M, Schäfer J, Simmet C, Jung M, Gabler C. 2018. Detec-tion and characterization of Lactobacillus spp. In the porcine se-minal plasma and their influence on boar semen quality. PLoS One. 13:1–16. https://doi.org/10.1371/journal.pone.0202699.
  • Marco-Jiménez F, Borrás S, Garcia-Dominguez X, D’Auria G, Vi-cente JS, Marin C. 2020. Roles of host genetics and sperm micro-biota in reproductive success in healthy rabbit. Theriogenology. 158:416–23. https://doi.org/10.1016/j.theriogenology.2020.09.028.
  • Krajmalnik-Brown R, Ilhan ZE, Kang DW, DiBaise JK. 2012. Ef-fects of gut microbes on nutrient absorption and energy regulation. Nutr Clin Pract. 27:201–14. https://doi.org/10.1177/0884533611436116.
  • LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. 2013. Bacteria as vitamin suppliers to their host: A gut microbiota perspective. Curr Opin Biotechnol. 24:160–8. https://doi.org/10.1016/j.copbio.2012.08.005.
  • Buntyn J, TB S, Nisbet D, Callaway T. 2015. The Role of Direct-Fed Microbials in Conventional Livestock. Annu Rev Anim Biosci. 4:335–55. Doi: 10.1146/annurev-animal-022114-111123
  • Evans JM, Morris LS, Marchesi JR. 2013. The gut microbiome: The role of a virtual organ in the endocrinology of the host. J En-docrinol. 218. https://doi.org/10.1530/JOE-13-0131.
  • Neuman H, Debelius JW, Knight R, Koren O. 2015. Microbial en-docrinology: The interplay between the microbiota and the endo-crine system. FEMS Microbiol Rev. 39:509–21. https://doi.org/10.1093/femsre/fuu010.
  • Blaser MJ, Dominguez-Bello MG. 2016. The Human Microbiome before Birth. Cell Host Microbe. 20:558–60. https://doi.org/10.1016/j.chom.2016.10.014.
  • Al-Asmakh M, Stukenborg JB, Reda A, Anuar F, Strand ML, He-din L, Pettersson S, Söder O. 2014. The gut microbiota and deve-lopmental programming of the testis in mice. PLoS One. 9. https://doi.org/10.1371/journal.pone.0103809.
  • Gérard P. 2016. Gut microbiota and obesity. Cell Mol Life Sci. 73:147–62. https://doi.org/10.1007/s00018-015-2061-5.
  • Zhuo Y, Cao M, Gong Y, Tang L, Jiang X, Li Y, Yang M, Yu S, Li J, Che L, Lin Y, Feng B, Fang Z, Wu D. 2020. Gut microbial metabolism of dietary fiber protects against high-energy feeding induced ovarian follicular atresia in a pig model. Br J Nutr. https://doi.org/10.1017/S0007114520002378.
  • Kunc M, Gabrych A, Witkowski JM. 2016. Microbiome impact on metabolism and function of sex, thyroid, growth and parathy-roid hormones. Acta Biochim Pol. 63:189–201. https://doi.org/10.18388/abp.2015_1093.
  • Flak MB, Neves JF, Blumberg RS. 2013. Welcome to the micro-genderome. Science (80-). 339:1044–5. https://doi.org/10.1126/science.1236226.
  • Plottel CS, Blaser MJ. 2011. Microbiome and malignancy. Cell Host Microbe. 10:324–35. https://doi.org/10.1016/j.chom.2011.10.003.
  • Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. 2017. Estrogen–gut microbiome axis: Physiological and clinical implications. Ma-turitas. 103:45–53.
  • López-Moreno A, Aguilera M. 2020. Probiotics dietary supple-mentation for modulating endocrine and fertility microbiota dys-biosis. Nutrients. 12:1–15. https://doi.org/10.3390/nu12030757.
  • Komiya S, Naito Y, Okada H, Matsuo Y, Hirota K, Takagi T, Mizushima K, Inoue R, Abe A, Morimoto Y. 2020. Characterizing the gut microbiota in females with infertility and preliminary re-sults of a water- soluble dietary fiber intervention study. J Clin Biochem Nutr. 67:105–11. https://doi.org/10.3164/jcbn.20-53.
  • Antwis RE, Edwards KL, Unwin B, Walker SL, Shultz S. 2019. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome. 7:1–12. https://doi.org/10.1186/s40168-019-0639-0.
  • Dunlop AL, Mulle JG, Ferranti EP, Edwards S, Dunn AB, Corwin EJ. 2015. Maternal Microbiome and Pregnancy Outcomes That Impact Infant Health: A Review. Adv Neonatal Care. 15: 377–85. https://doi.org/10.1097/ANC.0000000000000218.
  • Jašarević E, Bale TL. 2019. Prenatal and postnatal contributions of the maternal microbiome on offspring programming. Front Neuroendocrinol. 55. https://doi.org/10.1016/j.yfrne.2019.100797.
  • Lv Y, Yan Z, Zhao X, Gang X, He G, Sun L, Li Z, Wang G. 2018. The effects of gut microbiota on metabolic outcomes in pregnant women and their offspring. Food Funct. 9:4537–47. Doi: 10.1039/c8fo00601f.
  • Jašarević E, Morrison KE, Bale TL. 2016. Sex differences in the gut microbiome – Brain axis across the lifespan. Philos Trans R Soc B Biol Sci. 371:12–7. https://doi.org/10.1098/rstb.2015.0122.
  • Dong L, Han L, Duan T, Lin S, Li J, Liu X. 2020. Integrated mi-crobiome-metabolome analysis reveals novel associations bet-ween fecal microbiota and hyperglycemia - related changes of plasma metabolome in gestational diabetes mellitus. RSC Adv. 10:2027–36. https://doi.org/10.1039/c9ra07799e.
  • Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UME, Zhong X, Koenig SSK, Fu L, Ma Z, Zhou X, Abdo Z, Forney LJ, Ravel J. 2012. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 4. https://doi.org/10.1126/scitranslmed.3003605.
  • Miller EA, Livermore JA, Alberts SC, Tung J, Archie EA. 2017. Ovarian cycling and reproductive state shape the vaginal micro-biota in wild baboons. Microbiome. 5:1–14. https://doi.org/10.1186/s40168-017-0228-z.
  • Štšepetova J, Baranova J, Simm J, Parm Ü, Rööp T, Sokmann S, Korrovits P, Jaagura M, Rosenstein K, Salumets A, Mändar R. 2020. The complex microbiome from native semen to embryo cul-ture environment in human in vitro fertilization procedure. Reprod Biol Endocrinol. 18:1–13. https://doi.org/10.1186/s12958-019-0562-z.
  • Pelzer ES, Allan JA, Waterhouse MA, Ross T, Beagley KW, Knox CL. 2013. Microorganisms within Human Follicular Fluid: Effects on IVF. PLoS One. 8. https://doi.org/10.1371/journal.pone.0059062.
  • Pelzer ES, Harris JE, Allan JA, Waterhouse MA, Ross T, Beagley KW, Knoxa CL. 2013. TUNEL analysis of DNA fragmentation in mouse unfertilized oocytes: The effect of microorganisms within human follicular fluid collected during IVF cycles. J Reprod Im-munol. 99:69–79. https://doi.org/10.1016/j.jri.2013.07.004.
  • [64] Moreno I, Codoñer FM, Vilella F, Valbuena D, Martinez-Blanch JF, Jimenez- Almazán J, Alonso R, Alamá P, Remohí J, Pellicer A, Ramon D, Simon C. 2016. Evidence that the endometrial mi-crobiota has an effect on implantation success or failure. Am J Obstet Gynecol. 215:684–703. https://doi.org/10.1016/j.ajog.2016.09.075.
  • Franasiak JM, Werner MD, Juneau CR, Tao X, Landis J, Zhan Y, Treff NR, Scott RT. 2016. Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit. J Assist Reprod Genet. 33:129–36. https://doi.org/10.1007/s10815-015-0614-z.
  • Hashimoto T, Kyono K. 2019. Does dysbiotic endometrium affect blastocyst implantation in IVF patients? J Assist Reprod Genet. 36:2471–9. https://doi.org/10.1007/s10815-019-01630-7.
  • Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Kling Bäckhed H, Gonzalez A, Werner JJ, Angenent LT, Knight R, Bäckhed F, Isolauri E, Salminen S, Ley RE. 2012. Host remode-ling of the gut microbiome and metabolic changes during preg-nancy. Cell. 150:470–80. https://doi.org/10.1016/j.cell.2012.07.008.
  • Tissier H. 1900. Recherches sur la flore intestinale normale et pathologique du nourrisson. Thès de Paris n°529. https://www.biusante.parisdescartes.fr/histmed/me-dica/cote?TPAR1900x529.
  • Jašarević E, Howard C, Morrison K, Misic A, Weinkopff T, Scott P, Hunter C, Beiting D, Bale T. 2018. The maternal vaginal mi-crobiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus. Nat Neurosci. 21:1061–1071. Doi: 10.1038/s41593-018-0182-5.
  • Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hi-dalgo G, Fierer N, Knight R. 2010. Delivery mode shapes the ac-quisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 107:11971–5. https://doi.org/10.1073/pnas.1002601107.
  • Han YW, Shen T, Chung P, Buhimschi IA, Buhimschi CS. 2009. Uncultivated bacteria as etiologic agents of intra-amniotic inflam-mation leading to preterm birth. J Clin Microbiol. 47:38–47. https://doi.org/10.1128/JCM.01206-08.
  • Jiménez E, Marín ML, Martín R, Odriozola JM, Olivares M, Xaus J, Fernández L, Rodríguez JM. 2008. Is meconium from healthy newborns actually sterile? Res Microbiol. 159:187–93. https://doi.org/10.1016/j.resmic.2007.12.007.
  • Hu J, Nomura Y, Bashir A, Fernandez-Hernandez H, Itzkowitz S, Pei Z, Stone J, Loudon H, Peter I. 2013. Diversified microbiota of meconium is affected by maternal diabetes status. PLoS One. 8. https://doi.org/10.1371/journal.pone.0078257.
  • McDonald B, McCoy KD. 2019. Maternal microbiota in preg-nancy and early life. Science (80-). 365:984–5. https://doi.org/10.1126/science.aay0618.
  • De Agüero MG, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchi-mura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, McCoy KD, Macpherson AJ. 2016. The maternal microbiota drives early postnatal innate immune development. Science (80-). 351:1296–302. https://doi.org/10.1126/science.aad2571.
  • Thaper D, Rahi D, Prabha V. 2019. Amelioration of sperm immo-bilisation factor-induced infertility by bacterial antigenic determi-nants cross-reacting with spermatozoa. Reprod Fertil Dev. 31:602–12. Doi:10.1186/s12958-020-00654-4.
  • Zan Bar T, Yehuda R, Hacham T, Krupnik S, Bartoov B. Influence of Campylobacter fetus subsp. fetus on ram sperm cell quality. J Med Microbiol. 57:1405–10. https://doi.org/10.1099/jmm.0.2008/001057-0.
  • Altmae S. 2018. Commentary: Uterine Microbiota: Residents, Tourists, or Invaders? Front Immunol. 9. Doi:10.1007/s00265-006-0178-0.
  • Poiani A. 2006. Complexity of seminal fluid: A review. Behav Ecol Sociobiol. 60:289–310. https://doi.org/10.1007/s00265-006-0178-0.
  • Weng SL, Chiu CM, Lin FM, Huang WC, Liang C, Yang T, Yang TL, Liu CY, Wu WY, Chang YA, Chang TH, Huang H Da. 2014. Bacterial communities in semen from men of infertile couples: Metagenomic sequencing reveals relationships of seminal micro-biota to semen quality. PLoS One. 9. https://doi.org/10.1371/journal.pone.0110152.
  • Gòdia M, Ramayo-Caldas Y, Zingaretti LM, Darwich L, López S, Rodríguez-Gil JE, Yeste M, Sánchez A, Clop A. 2020. A pilot RNA-seq study in 40 pietrain ejaculates to characterize the porcine sperm microbiome. Theriogenology. 157:525–33. https://doi.org/10.1016/j.theriogenology.2020.08.001
  • Santos TMA, Gilbert R, Bicalho RC. 2011. Metagenomic analysis of the uterine bacterial microbiota in healthy and metritic postpar-tum dairy cows. J Dairy Sci. 94:291–302. https://doi.org/10.3168/jds.2010-3668.
  • Heil BA, Thompson SK, Kearns TA, Davolli GM, King G, Sones JL. 2018. Metagenetic Characterization of the Resident Equine Uterine Microbiome Using Multiple Techniques. J Equine Vet Sci. 66:111. https://doi.org/10.1016/j.jevs.2018.05.156.
  • Wu Y, Jiang H, Tan M, Lu X. 2020. Screening for chronic prosta-titis pathogens using high-throughput next-generation sequencing. Prostate. 80:577–87. https://doi.org/10.1002/pros.23971.
  • Chenoll E, Moreno I, Sánchez M, Garcia-Grau I, Silva Á, Gonzá-lez-Monfort M, Genovés S, Vilella F, Seco-Durban C, Simón C, Ramón D. 2019. Selection of new probiotics for endometrial health. Front Cell Infect Microbiol. 9:1–13. https://doi.org/10.3389/fcimb.2019.00114.
  • Cicinelli E, Matteo M, Tinelli R, Pinto V, Marinaccio M, Indrac-colo U, De Ziegler D, Resta L. 2014. Chronic endometritis due to common bacteria is prevalent in women with recurrent misca-rriage as confirmed by improved pregnancy outcome after antibio-tic treatment. Reprod Sci. 21:640–7. https://doi.org/10.1177/1933719113508817.
  • Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Tei-tler I, Chung J, Sohn J, Barber CM, Goldfarb DS, Raju K, Abubu-cker S, Zhou Y, Ruiz VE, Li H, Mitreva M, Alekseyenko A V., Weinstock GM, Sodergren E, Blaser MJ. 2015. Metabolic and me-tagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun. 6:1–15. https://doi.org/10.1038/ncomms8486.
  • [88] Vitagliano A, Saccardi C, Noventa M, Di Spiezio Sardo A, Sac-cone G, Cicinelli E, Pizzi S, Andrisani A, Litta PS. 2018. Effects of chronic endometritis therapy on in vitro fertilization outcome in women with repeated implantation failure: a systematic review and meta-analysis. Fertil Steril. 110:103-112.e1. https://doi.org/10.1016/j.fertnstert.2018.03.017
  • Borges ED, Berteli TS, Reis TF, Silva AS, Vireque AA. 2020. Mi-crobial contamination in assisted reproductive technology: source, prevalence, and cost. J Assist Reprod Genet. 37:53–61. https://doi.org/10.1007/s10815-019-01640-5.
  • Swain J. 2015. Optimal human embryo culture. Semin Reprod Med. 33:103–17. Doi: 10.1055/s-0035-1546423.
  • Schulze M, Nitsche-Melkus E, Hensel B, Jung M, Jakop U. 2020. Antibiotics and their alternatives in Artificial Breeding in lives-tock. Anim Reprod Sci. 106284. https://doi.org/10.1016/j.anireprosci.2020.106284.
  • Fuller R. 1989. Probiotics in man and animals. J Appl Bacteriol. 66:365–78. https://doi.org/10.1111/jam.1989.66.issue-5.
  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Mo-relli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. 2014. Expert consensus document: The international scientific as-sociation for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastro-enterol Hepatol. 11:506–14. https://doi.org/10.1038/nrgastro.2014.66.
  • Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Gancel F, Kempf I, Drider D. 2019. Benefits and inputs from lactic acid bac-teria and their bacteriocins as alternatives to antibiotic growth pro-moters during food-animal production. Front Microbiol. 10:1–17. https://doi.org/10.3389/fmicb.2019.00057.
  • Azas-Braesco V, Bresson JL, Guarner F, Corthier G. 2010. Not all lactic acid bacteria are probiotics, but some are. Br J Nutr. 103:1079–81. https://doi.org/10.1017/S0007114510000723.
  • Gibson GR, Probert HM, Loo J Van, Rastall RA, Roberfroid MB. 2004. Dietary modulation of the human colonic microbiota: upda-ting the concept of prebiotics. Nutr Res Rev. 17:259–75. https://doi.org/10.1079/nrr200479.
  • Chaucheyras-Durand F, Durand H. 2010. Probiotics in animal nu-trition and health. Benef Microbes. 1:3–9. https://doi.org/10.3920/BM2008.1002.
  • Yeoman C, White B. 2014. Gastrointestinal tract microbiota and probiotics in production animals. Annu Rev Anim Biosci. 2:469–86. Doi: 10.1146/annurev-animal-022513-114149.
  • Ballou MA, Davis EM, Kasl BA. 2019. Nutraceuticals: An Alter-native Strategy for the Use of Antimicrobials. Vet Clin North Am - Food Anim Pract. 35:507–34. https://doi.org/10.1016/j.cvfa.2019.08.004.
  • Mohammed AA, Jacobs JA, Murugesan GR, Cheng HW. 2018. Animal well-being and behavior: Effect of dietary synbiotic supplement on behavioral patterns and growth performance of broiler chickens reared under heat stress. Poult Sci. 97:1101–8. https://doi.org/10.3382/ps/pex421.
  • Abd El-Hack ME, El-Saadony MT, Shafi ME, Qattan SYA, Ba-tiha GE, Khafaga AF, Abdel-Moneim AME, Alagawany M. 2020. Probiotics in poultry feed: A comprehensive review. J Anim Phy-siol Anim Nutr (Berl). Pp. 1–16. https://doi.org/10.1111/jpn.13454.
  • Soroko M, Zaborski D. 2020. Investigation of the effects of pro-biotic, bacillus subtilis on stress reactions in laying hens using in-frared thermography. PLoS One. 15:1–12. https://doi.org/10.1371/journal.pone.0234117.
  • Hegab I, Eman A, Rania A, El-Azzazi F. 2019. Effect of Probiotics on Productive, Physiological and Microbiological Parameters of New Zealand White Rabbits Reared Under Hot Summer Condi-tions. Egypt Poult Sci J. 39:599–614. https://doi.org/10.21608/epsj.2019.46933.
  • Gioacchini G, Maradonna F, Lombardo F, Bizzaro D, Olivotto I, Carnevali O. 2010. Increase of fecundity by probiotic administra-tion in zebrafish (Danio rerio). Reproduction. 140:953–9. https://doi.org/10.1530/REP-10-0145.
  • Amdekar S, Singh V. 2016. Lactobacillus acidophilus maintained oxidative stress from reproductive organs in collagen-induced arthritic rats. J Hum Reprod Sci. 9:41–6. Doi: 10.4103/0974-1208.178638.
  • Mikulski D, Jankowski J, Naczmanski J, Mikulska M, Demey V. 2012. Effects of dietary probiotic (Pediococcus acidilactici) supplementation on performance, nutrient digestibility, egg traits, egg yolk cholesterol, and fatty acid profile in laying hens. Poult Sci. 91:2691–700. https://doi.org/10.3382/ps.2012-02370.
  • Siwek M, Slawinska A, Stadnicka K, Bogucka J, Dunislawska A, Bednarczyk M. 2018. Prebiotics and synbiotics - In ovo delivery for improved lifespan condition in chicken. BMC Vet Res. 14:1–17. https://doi.org/10.1186/s12917-018-1738-z.
  • Rautava S, Kainonen E, Salminen S, Isolauri E. 2012. Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol. 130:1355–60. https://doi.org/10.1016/j.jaci.2012.09.003.
  • Azagra-Boronat I, Tres A, Massot-Cladera M, Franch À, Castell M, Guardiola F, Pérez-Cano FJ, Rodríguez-Lagunas MJ. 2020. Lactobacillus fermentum CECT5716 Supplementation in Rats du-ring Pregnancy and Lactation Impacts Maternal and Offspring Li-pid Profile, Immune System and Microbiota. Cells. 9:575. https://doi.org/10.3390/cells9030575.
  • Gu XL, Li H, Song ZH, Ding YN, He X, Fan ZY. 2019. Effects of isomaltooligosaccharide and Bacillus supplementation on sow performance, serum metabolites, and serum and placental oxida-tive status. Anim Reprod Sci. 207:52–60. https://doi.org/10.1016/j.anireprosci.2019.05.015.
  • Kritas SK, Marubashi T, Filioussis G, Petridou E, Christodoulo-poulos G, Burriel AR, Tzivara A, Theodoridis A, Pískoriková M. 2015. Reproductive performance of sows was improved by admi-nistration of a sporing bacillary probiotic (Bacillus subtilis C-3102). J Anim Sci. 93:405–13. https://doi.org/10.2527/jas.2014-7651.
  • Hayakawa T, Masuda T, Kurosawa D, Tsukahara T. 2016. Dietary administration of probiotics to sows and/or their neonates impro-ves the reproductive performance, incidence of post-weaning dia-rrhea and histopathological parameters in the intestine of weaned piglets. Anim Sci J. 87:1501–10. Doi: 10.1111/asj. 12565.
  • Nasiri AH, Towhidi A, Shakeri M, Zhandi M, Dehghan-Banadaky M, Colazo MG. 2018. Effects of live yeast dietary supplementa-tion on hormonal profile, ovarian folicular dynamics, and repro-ductive performance in dairy cows exposed to high ambient tem-perature. Theriogenology. 122:41–6. https://doi.org/10.1016/j.theriogenology.2018.08.013.
  • Francisco CC, Chamberlain CS, Waldner DN, Wettemann RP, Spicer LJ. 2002. Propionibacteria fed to dairy cows: Effects on energy balance, plasma metabolites and hormones, and reproduc-tion. J Dairy Sci. 85:1738–51. https://doi.org/10.3168/jds.S0022-0302(02)74248-3.
  • Nicodemus N, Carabaño R, García J, Blas JD. 2004. Performance response of doe rabbits to Toyocerin(R) (Bacillus cereus var. To-yoi) supplementation. World Rabbit Science. 12(2):109-118. Doi:10.4995/wrs.2004.577.
  • Maertens L., Van Renterghem R., De Groote G. 2010. Effects of Dietary Inclusion of Paciflor® (Bacillus Cip 5832) on the Milk Composition and Performances of Does and on Caecal and Growth Parameters of Their Weanlings. World Rabbit Sci. 2. https://doi.org/10.4995/wrs.1994.220.
  • Fernández L, Cárdenas N, Arroyo R, Manzano S, Jiménez E, Mar-tín V, Rodríguez JM. 2016. Prevention of Infectious Mastitis by Oral Administration of Lactobacillus salivarius PS2 during Late Pregnancy. Clin Infect Dis. 62:568–73. https://doi.org/10.1093/cid/civ974.
  • Falcão-e-Cunha L, Castro-Solla L, Maertens L, Marounek M, Pin-heiro V, Freire J, Mourão JL. 2007. Alternatives to antibiotic growth promoters in rabbit feeding: A review. World Rabbit Sci. 15:127–40. https://doi.org/10.4995/wrs.2007.597.
  • Quesnel H, Farmer C. 2019. Review: Nutritional and endocrine control of colostrogenesis in swine. Animal. 13:S26–34. https://doi.org/10.1017/S1751731118003555.
  • Gilboa Y, Bar-Hava I, Fisch B, Ashkenazi J, Voliovitch I, Bor-kowski T, Orvieto R. 2005. Does intravaginal probiotic supple-mentation increase the pregnacy rate in IVF-embryo transfer cy-cles? Reprod Biomed Online. 11:71–5. https://doi.org/10.1016/S1472-6483(10)61301-6.
  • Quereda JJ, García-Roselló E, Barba M, Mocé ML, Gomis J, Ji-ménez-Trigos E, Bataller E, Martínez-Boví R, García-Muñoz Á, Gómez-Martín Á. 2020. Use of probiotics in intravaginal sponges in sheep: A pilot study. Animals. 10. https://doi.org/10.3390/ani10040719.
  • Deng Q, Odhiambo JF, Farooq U, Lam T, Dunn SM, Ametaj BN. 2016. Intravaginal probiotics modulated metabolic status and im-proved milk production and composition of transition dairy cows. J Anim Sci. 94:760–70. https://doi.org/10.2527/jas.2015-9650.
  • Marques TM, Wall R, Ross RP, Fitzgerald GF, Ryan CA, Stanton C. 2010. Programming infant gut microbiota: Influence of dietary and environmental factors. Curr Opin Biotechnol. 21: 149–56. https://doi.org/10.1016/j.copbio.2010.03.020.
  • Surzenko N, Pjetri E, Munson CA, Friday WB, Hauser J, Mitchel ES. 2020. Prenatal exposure to the probiotic Lactococcus lactis decreases anxiety-like behavior and modulates cortical cytoarchi-tecture in a sex specific manner. PLoS One. 15:1–15. https://doi.org/10.1371/journal.pone.0223395.
  • [125] Guo Y, Wang Z, Chen L, Tang L, Wen S, Liu Y, Yuan J. 2018. Diet induced maternal obesity affects offspring gut microbiota and persists into young adulthood. Food Funct. 9:4317–27. Doi: 10.1039/c8fo00444g.
  • Valcarce DG, Riesco MF, Martínez-Vázquez JM, Robles V. 2019. Long exposure to a diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality and progeny sur-vival in the zebrafish model. Biomolecules. 9. https://doi.org/10.3390/biom9080338.
  • Maretti C, Cavallini G. 2017. The association of a probiotic with a prebiotic (Flortec, Bracco) to improve the quality/quantity of spermatozoa in infertile patients with idiopathic oligoasthenotera-tospermia: a pilot study. Andrology. 5:439–44. https://doi.org/10.1111/andr.12336.
  • Mandour AS, Samir H, El-Beltagy MA, Abdel-Daim MM, Izumi W, Ma D, Matsuura K, Tanaka R, Watanabe G. 2020. Effect of supra-nutritional selenium-enriched probiotics on hematobioche-mical, hormonal, and Doppler hemodynamic changes in male goats. Environ Sci Pollut Res. 27:19447–60. https://doi.org/10.1007/s11356-020-08294-2.
  • Poutahidis T, Springer A, Levkovich T, Qi P, Varian BJ, Lakritz JR, Ibrahim YM, Chatzigiagkos A, Alm EJ, Erdman SE. 2014. Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS One. 9. https://doi.org/10.1371/journal.pone.0084877.
  • Emmanuel DC, Amaka AE, Okezie ES, Sunday UP, Ethelbert OC. 2019. Epididymal sperm characteristics, testicular morphometric traits and growth parameters of rabbit bucks fed dietary saccha-romyces cerevisiae and/or zinc oxide. Rev Bras Cienc Avic. 21. https://doi.org/10.1590/1806-9061-2018-0803.
  • García-Galán A, De La Fe C, Gomis J, Bataller E, Sánchez A, Quereda JJ, García-Roselló E, Gómez-Martín A. 2020. The addi-tion of Lactobacillus spp. negatively affects Mycoplasma bovis viability in bovine cervical mucus. BMC Vet Res. 16. https://doi.org/10.1186/s12917-020-02454-9.