doi: 10.15389/agrobiology.2022.2.222eng
UDC: 636.018:579.2
MICROBIOTA AND REPRODUCTION IN AGRICULTURAL MAMMALS(review)
D.V. Popov✉
Afanas’ev Research Institute of Fur-Bearing Animal Breeding and Rabbit Breeding, 6, ul. Trudovaya, pos. Rodniki, Ramenskii Region, Moscow Province, 140143 Russia, e-mail popov.bio@gmail.com (✉ corresponding author)
ORCID:
Popov D.V. orcid.org/0000-0001-7422-5470
October 13, 2021
The use of specialized animal breeds of agricultural species is often accompanied by a decrease in reproductive success. In dairy cattle breeding, the number of service-period days, artificial insemination procedures per pregnancy, and the frequency of pregnancy losses are increasing (S.V. Guskova et al., 2014). Accumulated data on obtaining embryos by in vivo and in vitro methods and their transplantation indicate a significant level (30-60 %) of embryo losses (P.J. Hansen, 2020). The reasons for low rates in reproductive technologies are diverse and associated with both biotic and abiotic factors, and one of the key factors of embryo losses may be the imbalance of microbial communities in the reproductive system sections of both female donors and recipients. The study of the microbiota composition of various departments and systems of the multicellular organism has recently become an increasingly dominant topic in the scientific literature. Modern methods of microbial identification, e.g., metagenomic sequencing, reveals great microbial diversity in various anatomical departments of macroorganisms. The accumulated data show the microbial composition, dynamics in the organs of the reproductive system, and its relationship with the reproduction of mammals, reproductive success, the course of pregnancy, the prognosis of the possibilities of pathological processes. The review focuses on the impact of microbiota on the success of reproductive technologies, e.g., in vitro fertilization, embryo transplantation, and artificial insemination. For example, F. Marco-Jiménez et al. (2020) discuss the effect of symbiotic bacteria on fertility and semen quality. The understudied nature of this area for mammals and the extreme need for additional research on the microbiota of the reproductive tract of farm animals, the results of which will provide insight and insight into the unsuccessful and positive outcomes of reproduction, are noted. At the same time, the practical application of this information will increase the chances of success in reproductive biotechnology, reduce the costs associated with reproduction and therapeutic interventions in the treatment of pathological processes of the reproductive system, and open up the possibility of developing and implementing new methods such as microbial therapy. Thus, it can be concluded that the microbiota of mammalian reproductive system and organs influence the physiological processes of reproduction (R. Koedooder et al., 2019). It is clear that by being able to manage microbial communities, humans can increase the chances of reproductive success in the reproduction of highly specialized breeds of farm animals (P.J. Hansen, 2020; R.W. Hyman et. al., 2012; D.E. Moore et. al., 2000).
Keywords: endometrium, microbiota, microbiome, reproductive system, sperm, uterus, reproductive technology.
REFERENCES
- Gus'kova S.V., Turbina I.S., Eskin G.V., Kombarova N.A. Myasnoe i molochnoe skotovodstvo, 2014, 3: 10-13 (in Russ.).
- Hansen P.J. The incompletely fulfilled promise of embryo transfer in cattle-why aren’t pregnancy rates greater and what can we do about it? J. Anim. Sci., 2020, 98(11): skaa288 CrossRef
- 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. Human Reproduction Update, 2019, 25(3): 298-325 CrossRef
- Marchesi J.R., Ravel J. The vocabulary of microbiome research: a proposal. Microbiome, 2015, 3: 31 CrossRef
- Stoma I.O., Karpov I.A. Mikrobiom cheloveka [Human microbiome]. Minsk, 2018 (in Russ.).
- Lane D.J., Pace B., Olsen G.J., Stahl D.A., Sogin M.L., Pace N.R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci USA, 1985, 82(20): 6955-6959 CrossRef
- Gray M.W., Sankoff D., Cedergren R.J. On the evolutionary descent of organisms and organelles: a global phylogeny based on a highly conserved structural core in small subunit ribosomal RNA. Nucleic Acids Research, 1984, 12(14): 5837-5852 CrossRef
- Metzker M.L. Emerging technologies in DNA sequencing. Genome Res., 2005, 15: 1767-1776 CrossRef
- Margulies M., Egholm M., Altman W.E., Attiya S., Bader J.S., Bemben L.A., Berka J., Braverman M.S., Chen Y.-J., Chen Z. Genome sequencing in microfabricated highdensity picolitre reactors. Nature, 2005, 437(7057): 376-380 CrossRef
- Loman N.J., Misra R.V., Dallman T.J., Constantinidou C., Gharbia S.E., Wain J., Pallen M.J. Performance comparison of benchtop high-throughput sequencing platforms. Nat. Biotechnol., 2012, 30(5): 434-439 CrossRef
- Ranjan R., Rani A., Metwally A., McGee H.S., Perkins D.L. Analysis of the microbiome: advantages of whole genome shotgun versus 16S amplicon sequencing. Biochem. Biophys. Res. Commun., 2016, 469(4): 967-977 CrossRef
- Roumpeka D.D., Wallace R.J., Escalettes F., Fotheringham I., Watson M. A review of bioinformatics tools for bio-prospecting from metagenomic sequence data. Frontiers in Genetics, 2017, 8: 23 CrossRef
- Ott S.J., Musfeldt M., Ullmann U., Hampe J., Schreiber S. Quantification of intestinal bacterial populations by real-time PCR with a universal primer set and minor groove binder probes: a global approach to the enteric flora. Journal of Clinical Microbiology, 2004, 42(6): 2566-2572 CrossRef
- Malinen E., Kassinen A., Rinttila T., Palva A. Comparison of real-time PCR with SYBR Green I or 5´-nuclease assays and dot-blot hybridization with rDNA-targeted oligonucleotide probes in quantification of selected faecal bacteria. Microbiology, 2003, 149: 269-277 CrossRef
- Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Applied and Environmental Microbiology, 2009, 75(23): 7537-7541 CrossRef
- Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Pena A.G., Goodrich J.K., Gordon J.I. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods, 2010, 7: 335 CrossRef
- Edgar R.C. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics, 2018, 34: 2371-2375 CrossRef
- Westcott S.L., Schloss P.D. De novo clustering methods outperform reference based methods for assigning 16S rRNA gene sequences to operational taxonomic units. PeerJ, 2015, 3: e1487 CrossRef
- McDonald D., Price M.N., Goodrich J., Nawrocki E.P., DeSantis T.Z., Probst A., Andersen G.L., Knight R., Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J., 2012, 6: 610-618 CrossRef
- Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glöckner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research,2007, 35(21): 7188-7196 CrossRef
- Cole J.R., Wang Q., Cardenas E., Fish J., Chai B., Farris R.J., Kulam-Syed-Mohideen A.S., McGarrell D.M., Marsh T., Garrity G.M., Tiedje J.M. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research, 2009, 37(suppl_1): D141-D145 CrossRef
- Chen W., Zhang C.K., Cheng Y., Zhang S., Zhao H. A comparison of methods for clustering 16S rRNA sequences into OTUs. PLoS ONE, 2013, 8: e70837 CrossRef
- Nguyen N.P., Warnow T., Pop M., White B. A perspective on 16 S rRNA operational taxonomic unit clustering using sequence similarity. NPJ Biofilms Microbiomes, 2016, 2: 16004 CrossRef
- Haas B.J., Gevers D., Earl A.M., Feldgarden M., Ward D.V., Giannoukos G., Ciulla D., Tabbaa D., Highlander S.K., Sodergren E., Methé B., DeSantis T.Z., Human Microbiome Consortium, Petrosino J.F., Knight R., Birren B.W. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res., 2011, 21(3): 494-504 (doi: 10.1101/gr.112730.110">CrossRef
- D’Amore R., Ijaz U.Z., Schirmer M., Kenny J.G., Gregory R., Darby A.C., Shakya M., Podar M., Quince C., Hall N. A comprehensive benchmarking study of protocols and sequencing platforms for 16 S rRNA community profiling. BMC Genomics, 2016, 17: 55 CrossRef
- Glazko V.I., Zybaylov B.L., Kosovsky G.Yu., Glazko G.V., Glazko T.T. Domestication and microbiome The Holocene, 2021, 31(10): 1635-1645 CrossRef
- Wilkins A.S. A striking example of developmental bias in an evolutionary process: The “domestication syndrome”. Evolution & Development, 2020, 22(1-2): 143-153 CrossRef
- Glazko V., Zybailov B., Glazko T. Asking the right question about the genetic basis of domestication: what is the source of genetic diversity of domesticated species? Adv. Genet. Eng., 2015, 4(2): 1000125 CrossRef
- O’Hara A.M., Shanahan F. The gut flora as a forgotten organ. EMBO Rep., 2006, 7(7): 688-693 CrossRef
- Kolodny O., Callahan B.J., Douglas A.E. The role of the microbiome in host evolution. Phil. Trans. R. Soc. B, 2020, 375(1808): 20190588 CrossRef
- Zilber-Rosenberg I., Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev., 2008, 32(5): 723-735 CrossRef
- Ikeda-Ohtsubo W., Brugman S., Warden C.H., Rebel J.M.J., Folkerts G., Pieterse C.M.J. How can we define “optimal microbiota?”: a comparative review of structure and functions of microbiota of animals, fish, and plants in agriculture. Front. Nutr., 2018, 5: 90 ( doi: 10.3389/fnut.2018.00090">CrossRef
- Douglas-Escobar M., Elliott E., Neu J. Effect of intestinal microbial ecology on the developing brain. JAMA Pediatr., 2013, 167(4): 374-379 CrossRef
- Bercik P., Denou E., Collins J., The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology, 2011, 141(2): 599-609 CrossRef
- Knight R., Callewaert C., Marotz C., Hyde E.R., Debelius J.W., McDonald D., Sogin M.L. The microbiome and human biology. Annual Review of Genomics and Human Genetics, 2017, 18: 65-86 CrossRef
- Li J.V., Swann J., Marchesi J.R. Biology of the microbiome 2: metabolic role. Gastroenterol. Clin. North Am., 2017, 46(1): 37-47 CrossRef
- Doré J., Blottière H. The influence of diet on the gut microbiota and its consequences for health. Curr. Opin. Biotechnol., 2015, 32: 195-199 CrossRef
- NIH Human Microbiome Portfolio Analysis Team. A review of 10 years of human microbiome research activities at the US national institutes of health, fiscal years 2007-2016. Microbiome, 2019, 7: 31 CrossRef
- Peterson S.N., Snesrud E., Liu J., Ong A.C., Kilian M., Schork N.J., Bretz W. The dental plaque microbiome in health and disease. PLoS ONE, 2013, 8: e58487 CrossRef
- Yang F., Zeng X., Ning K., Liu K.L., Lo C.C., Wang W., Chen J., Wang D., Huang R., Chang X. Saliva microbiomes distinguish caries-active from healthy human populations. ISME J., 2012, 6: 1-10 CrossRef
- Fredricks D.N., Fiedler T.L., Marrazzo J.M. Molecular identification of bacteria associated with bacterial vaginosis. N. Engl. J. Med., 2005, 353(18):1899-1911 CrossRef
- Cotozzolo E., Cremonesi P., Curone G., Characterization of bacterial microbiota composition along the gastrointestinal tract in rabbits. Animals (Basel), 2020, 11(1): 31 CrossRef
- Chen C., Song X., Wei W., Zhong H., Dai J., Lan Z., Li F., Yu X., Feng Q., Wang Z. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat. Commun., 2017, 8: 875 CrossRef
- Mitchell C.M., Haick A., Nkwopara E., Garcia R., Rendi M., Agnew K., Fredricks D.N., Eschenbach D. Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women. Am. J. Obstet. Gynecol., 2015, 212(5): 611.e1-611.e9 CrossRef
- Hickey R.J., Zhou X., Pierson J.D., Ravel J., Forney L.J. Understanding vaginal microbiome complexity from an ecological perspective. Transl. Res., 2012, 160(4): 267-282 CrossRef
- Noyes N., Cho K.-C., Ravel J., Forney L.J., Abdo Z. Associations between sexual habits, menstrual hygiene practices, demographics and the vaginal microbiome as revealed by Bayesian network analysis. PLoS ONE, 2018, 13: e0191625 CrossRef
- Ravel J., Gajer P., Abdo Z., Schneider G.M., Koenig S.K., McCulle S.L., Karlebach S., Gorle R., Russell J., Tacket C.O., Brotman R.M., Davis C.C., Ault K., Peralta L., Forney L.J. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci., 2011, 108(supplement_1): 4680- 4687 CrossRef
- Gajer P., Brotman R.M., Bai G., Sakamoto J., Schütte U.M.E., Zhong X., Koenig S.S.K., Fu L., Ma Z.S., Zhou X., Abdo Z., Forney L.J., Ravel J. Temporal dynamics of the human vaginal microbiota. Sci. Transl. Med., 2012, 4(132): 132ra152 CrossRef
- Albert A.Y.K., Chaban B., Wagner E.C., Schellenberg J.J., Links M.G., Van Schalkwyk J., Reid G., Hemmingsen S.M., Hill J.E., Money D. A study of the vaginal microbiome in healthy Canadian women utilizing cpn60-based molecular profiling reveals distinct Gardnerella subgroup community state types. PLoS ONE, 2015, 10: e0135620 CrossRef
- O’Hanlon D.E., Moench T.R., Cone R.A. Vaginal pH and microbicidal lactic acid when Lactobacilli dominate the microbiota. PLoS ONE, 2013, 8(11): e80074 CrossRef
- Anahtar M.N., Byrne E.H., Doherty K.E., Bowman B.A., Yamamoto H.S., Soumillon M., Padavattan N., Ismail N., Moodley A., Sabatini M.E., Ghebremichael M.S., Nusbaum C., Huttenhower C., Virgin H.W., Ndung'u T., Dong K.L., Walker B.D., Fichorova R.N., Kwon D.S. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity,2015, 42(5): 965-976 CrossRef
- Anukam K.C., Osazuwa E.O., Ahonkhai I., Reid G. Lactobacillus vaginal microbiota of women attending a reproductive health care service in Benin city, Nigeria. Sexually Transmitted Diseases, 2006, 33(1): 59-62 CrossRef
- Pendharkar S., Magopane T., Larsson P.-G., de Bruyn G., Gray G.E., Hammarström L., Marcotte H. Identification and characterisation of vaginal Lactobacilli from South African women. BMC Infect. Dis., 2013, 13: 43 CrossRef
- MacIntyre D.A., Chandiramani M., Lee Y.S., Kindinger L., Smith A., Angelopoulos N., Lehne B., Arulkumaran S., Brown R., Teoh T.G., Holmes E., Nicoholson J.K., Marchesi J.R., Bennett P.R. The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci. Rep., 2015, 5: 8988 CrossRef
- Aagaard K., Riehle K., Ma J., Segata N., Mistretta T.A., Coarfa C., Raza S., Rosenbaum S., Van den Veyver I., Milosavljevic A. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE, 2012, 7: e36466 CrossRef
- Romero R., Hassan S.S., Gajer P., Tarca A.L., Fadrosh D.W., Nikita L., Galuppi M., Lamont R.F., Chaemsaithong P., Miranda J., Chaiworapongsa T., Ravel J. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of nonpregnant women. Microbiome, 2014, 2: 4 CrossRef
- Hyman R.W., Fukushima M., Jiang H., Fung E., Rand L., Johnson B., Vo K.C., Caughey A.B., Hilton J.F., Davis R.W., Giudice L.C. Diversity of the vaginal microbiome correlates with preterm birth. Reproductive Sciences, 2014, 21(1): 32-40 CrossRef
- Stout M.J., Zhou Y., Wylie K.M., Tarr P.I., Macones G.A., Tuuli M.G. Early pregnancy vaginal microbiome trends and preterm birth. Am. J. Obstet. Gynecol., 2017, 217(3): 356.e1-356.e18 CrossRef
- Mendes-Soares H., Suzuki H., Hickey R.J., Forney L.J. Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal Lactobacilli to their environment. Journal of Bacteriology, 2014, 196(7): 1458-1470 CrossRef
- Ojala T., Kankainen M., Castro J., Cerca N., Edelman S., Westerlund-Wikström B., Paulin L., Holm L., Auvinen P. Comparative genomics of Lactobacillus crispatus suggests novel mechanisms for the competitive exclusion of Gardnerella vaginalis. BMC Genomics, 2014, 15: 1070 CrossRef
- Graspeuntner S., Bohlmann M.K., Gillmann K., Speer R., Kuenzel S., Mark H., Hoellen F., Lettau R., Griesinger G., König I.R. Microbiota-based analysis reveals specific bacterial traits and a novel strategy for the diagnosis of infectious infertility. PLoS ONE, 2018, 13: e0191047 CrossRef
- Babu G., Singaravelu B.G., Srikumar R., Reddy S.V. Comparative study on the vaginal flora and incidence of asymptomatic vaginosis among healthy women and in women with infertility problems of reproductive age. Journal of Clinical and Diagnostic Research, 2017, 11(8): DC18-DC22 CrossRef
- 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., 2017, 232(7): 1681-1688 CrossRef
- Di M.P., Filardo S., Porpora M.G., Recine N., Latino M.A., Sessa R. HPV/Chlamydia trachomatis co-infection: metagenomic analysis of cervical microbiota in asymptomatic women. New Microbiologica, 2018, 41(1): 34-41.
- Van de Wijgert J.H.H.M, Borgdorff H., Verhelst R., Crucitti T., Francis S., Verstraelen H., Jespers V. The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS ONE, 2014, 9: e105998 CrossRef
- Workowski K.A., Bolan G.A. Sexually transmitted diseases treatment guidelines, 2015. Recommendations and Reports, 2015, 64(RR3): 1-137.
- Onderdonk A.B., Delaney M.L., Fichorova R.N. The human microbiome during bacterial vaginosis. Clinical Microbiology Reviews, 2016, 29(2): 223-238 CrossRef
- Gottschick C., Deng Z.-L., Vital M., Masur C., Abels C., Pieper D.H., Wagner-Döbler I. The urinary microbiota of men and women and its changes in women during bacterial vaginosis and antibiotic treatment. Microbiome, 2017, 5: 99 CrossRef
- Donders G.G., Van Calsteren K., Bellen G., Reybrouck R., Van den Bosch T., Riphagen I., Van Lierde S. Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. BJOG: An International Journal of Obstetrics & Gynaecology, 2009, 116(10): 1315-1324 CrossRef
- Işik G., Demirezen Ş., Dönmez H.G., Beksaç M.S. Bacterial vaginosis in association with spontaneous abortion and recurrent pregnancy losses. Journal of Cytology, 2016, 33(3): 135-140 CrossRef
- Karstrup C.C., Klitgaard K., Jensen T.K., Agerholm J.S., Pedersen H.G. Presence of bacteria in the endometrium and placentomes of pregnant cows. Theriogenology, 2017, 99: 41-47 CrossRef
- Bicalho M.L., Lima F.S., Machado V.S., Meira E.B. Jr., Ganda E.K., Foditsch C., Bicalho R.C., Gilbert R.O. Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology, 2016, 85(2): 267-274 CrossRef
- Galvão K.N., Bicalho R.C., Jeon S.J. Symposium review: The uterine microbiome associated with the development of uterine disease in dairy cows. Journal of Dairy Science, 2019, 102(12): 11786-11797 CrossRef
- Bicalho V.S., Machado C.H., Higgins F.S., Lima R.C. Genetic and functional analysis of the bovine uterine microbiota. Part I: Metritis versus healthy cows. Journal of Dairy Science, 2017, 100(5): 3850-3862 CrossRef
- Bicalho M.L.S., Lima S., Higgins C.H., Machado V.S., Lima F.S., Bicalho R.C. Genetic and functional analysis of the bovine uterine microbiota. Part II: Purulent vaginal discharge versus healthy cows. Journal of Dairy Science, 2017, 100(5): 3863-3874 CrossRef
- Umar T., Yin B., Umer S., Ma X., Jiang K., Umar Z., Akhtar M., Shaukat A., Deng G. MicroRNA: could it play a role in bovine endometritis? Inflammation, 2021, 44(5): 1683-1695 CrossRef
- Miller E.A., Beasley D.E., Dunn R.R., Archie E.A. Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique? Front. Microbiol., 2016, 7: 1936 CrossRef
- Swartz J.D., Lachman M., Westveer K., O'Neill T., Geary T., Kott R.W., Berardinelli J.G., Hatfield P.G., Thomson J.M., Roberts A., Yeoman C.J. Characterization of the vaginal microbiota of ewes and cows reveals a unique microbiota with low levels of Lactobacilli and Near-Neutral pH. Frontiers in Veterinary Science, 2014, 1: 19 CrossRef
- Hyman R.W., Herndon C.N., Jiang H., Palm C., Fukushima M., Bernstein D., Vo K.C., Zelenko Z., Davis R.W., Giudice L.C. The dynamics of the vaginal microbiome during infertility therapy with in vitro fertilization-embryo transfer. Journal of Assisted Reproduction and Genetics, 2012, 29(2): 105-115 CrossRef
- Moore D.E., Soules M.R., Klein N.A., Fujimoto V.Y., Agnew K.J., Eschenbach D.A. Bacteria in the transfer catheter tip influence the live-birth rate after in vitro fertilization. Fertility and Sterility, 2000, 74(6): 1118-1124 CrossRef
- Hillier S.L., Nugent R.P., Eschenbach D.A., Krohn M.A., Gibbs R.S., Martin D.H., Cotch M.F., Edelman R., Pastorek J.G., Rao A.V., McNellis D., Regan J.A., et all., for the Vaginal Infections and Prematurity Study Group. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. New England Journal of Medicine, 1995, 333: 1737-1742 CrossRef
- 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 Reproduction, 2016, 31(4): 795-803 CrossRef
- Mangot-Bertrand J., Fenollar F., Bretelle F., Gamerre M., Raoult D., Courbiere B. Molecular diagnosis of bacterial vaginosis: impact on IVF outcome. European Journal of Clinical Microbiology & Infectious Diseases, 2013, 32: 535-541 CrossRef
- Pelzer 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 CrossRef
- Petrova M., Lievens E., Malik S., Imholz N., Lebeer S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Frontiers in Physiology, 2015, 6: 81 CrossRef
- Moreno I., Codoñer F.M., Vilella F., Valbuena D., Martinez-Blanch J.F., Jimenez-Almazán J., Alonso R., Alamá P., Remohí J., Pellicer A. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am. J. Obstet. Gynecol., 2016, 215: 684-703 CrossRef
- Cicinelli E., Matteo M., Tinelli R., Lepera A., Alfonso R., Indraccolo U., Marrocchella S., Greco P., Resta L. Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy. Human Reproduction, 2015, 30(2): 323-330 CrossRef
- Cicinelli E., Matteo M., Tinelli R., Pinto V., Marinaccio M., Indraccolo U., De Ziegler D., Resta L. Chronic endometritis due to common bacteria is prevalent in women with recurrent miscarriage as confirmed by improved pregnancy outcome after antibiotic treatment. Reproductive Sciences,2014, 21(5): 640-647 CrossRef
- Khan K.N., Fujishita A., Kitajima M., Hiraki K., Nakashima M., Masuzaki H. Intra-uterine microbial colonization and occurrence of endometritis in women with endometriosis. Human Reproduction, 2014, 29(11): 2446-2456 CrossRef
- Fotouh I.A., Al-Inany M.G. The levels of bacterial contamination of the embryo transfer catheter relate negatively to the outcome of embryo transfer. Middle East Fertility Society Journal,2008, 13(1): 39-43.
- Franasiak J.M., Werner M.D., Juneau C.R., Tao X., Landis J., Zhan Y., Treff N.R., Scott R.T. Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit. Journal of Assisted Reproduction and Genetics, 2016, 33(1): 129-136 CrossRef
- Kroon B., Hart R.J., Wong B., Ford E., Yazdani A. Antibiotics prior to embryo transfer in ART. Cochrane Database of Systematic Reviews, 2012, 3: CD008995 CrossRef
- Brook N., Khalaf Y., Coomarasamy A., Edgeworth J., Braude P. A randomized controlled trial of prophylactic antibiotics (co-amoxiclav) prior to embryo transfer. Human Reproduction, 2006, 21(11): 2911-2915 CrossRef
- Schoenmakers S., Steegers-Theunissen R., Faas M. The matter of the reproductive microbiome. Obstetric Medicine, 2019, 12(3): 107-115 CrossRef
- Kim J.H., Yoo S.M., Sohn Y.H., Jin C.H., Yang Y.S., Hwang I.T., Oh K.Y. Predominant Lactobacillus species types of vaginal microbiota in pregnant Korean women: quantification of the five Lactobacillus species and two anaerobes. Journal of Maternal-Fetal & Neonatal Medicine, 2017, 30(19): 2329-2333 CrossRef
- Beckers K.F., Sones J.L. Maternal microbiome and the hypertensive disorder of pregnancy, preeclampsia. American Journal of Physiology-Heart and Circulatory Physiology, 2020, 318(1): H1-H10 CrossRef
- McElrath T.F., Hecht J.L., Dammann O., Boggess K., Onderdonk A., Markenson G., Harper M., Delpapa E., Allred E.N., Leviton A., ELGAN Study Investigators. Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification. American Journal of Epidemiology, 2008, 168(9): 980-989 CrossRef
- Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. The placenta harbors a unique microbiome. Sci. Transl. Med., 2014, 6(237): 237ra65 CrossRef
- Benner M., Ferwerda G., Joosten I., Van der Molen R.G. How uterine microbiota might be responsible for a receptive, fertile endometrium. Human Reproduction, 2018, 24(4): 393-415 CrossRef
- Weng S.-L., Chiu C.-M., Lin F.-M., Huang W.-C., Liang C., Yang T., Yang T.-L., Liu C.-Y., Wu W.-Y., Chang Y.-A., Chang T.-H., Huang H.-D. Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PLoS ONE,2014, 9(10): e110152 CrossRef
- Gdoura R., Kchaou W., Chaari C., Znazen A., Keskes L., Rebai T., Hammami A. Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC Infect. Dis., 2007, 7: 129 CrossRef
- Zinzendorf N.Y., Kouassi-Agbessi B.T., Lathro J.S., Don C., Kouadio L., Loukou Y.G. Ureaplasma urealyticum or Mycoplasma hominis infections and semen quality of infertile men in Abidjan. Journal of Reproduction and Contraception, 2008, 19(2): 65-72 CrossRef
- Ahmadi 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 CrossRef
- Mändar R., Punab M., Korrovits P., Türk S, Ausmees K., Lapp E., Preem J.K., Oopkaup K., Salumets A., Truu J. Seminal microbiome in men with and without prostatitis. Int. J. Urol.,2017, 24(3): 211-216 CrossRef
- Monteiro 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(6): e12838 CrossRef
- Marco-Jiménez F., Borrás S., Garcia-Dominguez X., D'Auria G., Vicente J.S., Marin C. Roles of host genetics and sperm microbiota in reproductive success in healthy rabbit Theriogenology, 2020, 158: 416-423 CrossRef
- Mändar R., Punab M., Borovkova N., Lapp E., Kiiker R., Korrovits P., Metspalu A., Krjutškov K., Nõlvak H., Preem J.K., Oopkaup K., Salumets A., Truu J. Complementary seminovaginal microbiome in couples. Research in Microbiology, 2015, 166(5): 440-447 CrossRef
- Borovkova N., Korrovits P., Ausmees K., Turk S., Joers K., Punab M., Mändar R. Influence of sexual intercourse on genital tract microbiota in infertile couples. Anaerobe, 2011, 17(6): 414-418 CrossRef
- Eschenbach D.A., Patton D.L., Hooton T.M., Meier A.S., Stapleton A., Aura J., Agnew K. Effects of vaginal intercourse with and without a condom on vaginal flora and vaginal epithelium. The Journal of Infectious Diseases, 2001, 183(6): 913-918 CrossRef
- Leppaluoto P.A. Bacterial vaginosis: what is physiological in vaginal bacteriology? An update and opinion. Acta Obstetricia et Gynecologica Scandinavica, 2011, 90(12): 1302-1306 CrossRef
- Robertson S.A., Sharkey D.J. Seminal fluid and fertility in women. Fertility and Sterility, 2016, 106(3): 511-519 CrossRef