Perspective on the relationship between reproductive tract microbiota eubiosis and dysbiosis and reproductive function
Nesrein M. Hashem![https://orcid.org/0000-0003-0058-9671](/media/client/orcid_16x16.png)
A Department of Animal and Fish Production, Faculty of Agriculture (El-Shatby), Alexandria University, Alexandria 21545, Egypt.
B Departamento 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.
Handling Editor: Graeme Martin
Reproduction, Fertility and Development 34(7) 531-539 https://doi.org/10.1071/RD21252
Published online: 15 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The role played by microbiota is attracting growing attention within the scientific and medical community, in both human and animal fields, in the last years. Most of the studies have been focused on the intestinal microbiome, whilst little attention has been paid to other systems, like the reproductive tract of both females and males. However, there is a growing body of information showing the interplay between reproductive tract dysbiosis, due to the action of pathogens and/or unhealthy lifestyle, and reproductive disease and disorders in many mammalian species. The present review aims to summarise current knowledge on the biodiversity of the microbiota of the reproductive tract, and the possible relationships between eubiosis or dysbiosis and reproductive health and function in both females and males.
Keywords: eubiosis, fertility, mammals, metritis, microbial biodiversity, prostatitis, reproductive disorders, vaginosis.
References
Ahmadi, MH, Mirsalehian, A, Gilani, MAS, Bahador, A, and Talebi, M (2017). Asymptomatic infection with Mycoplasma hominis negatively affects semen parameters and leads to male infertility as confirmed by improved semen parameters after antibiotic treatment. Urology 100, 97–102.| Asymptomatic infection with Mycoplasma hominis negatively affects semen parameters and leads to male infertility as confirmed by improved semen parameters after antibiotic treatment.Crossref | GoogleScholarGoogle Scholar | 27871827PubMed |
Altmäe, S, Franasiak, JM, and Mändar, R (2019). The seminal microbiome in health and disease. Nature Reviews Urology 16, 703–721.
| The seminal microbiome in health and disease.Crossref | GoogleScholarGoogle Scholar | 31732723PubMed |
Appiah, MO, Wang, J, and Lu, W (2020). Microflora in the reproductive tract of cattle: a review. Agriculture 10, 232.
| Microflora in the reproductive tract of cattle: a review.Crossref | GoogleScholarGoogle Scholar |
Bahaabadi, SJ, Moghadam, NM, Kheirkhah, B, Farsinejad, A, and Habibzadeh, V (2014). Isolation and molecular identification of Mycoplasma hominis in infertile female and male reproductive system. Nephro-Urology Monthly 6, e22390.
| Isolation and molecular identification of Mycoplasma hominis in infertile female and male reproductive system.Crossref | GoogleScholarGoogle Scholar |
Baud D, Pattaroni C, Vulliemoz N, Castella V, Marsland BJ, Stojanov M (2019) Sperm microbiota and its impact on semen parameters. Frontiers in Microbiology 10, 234.
| Crossref |
Bicalho, MLS, Lima, FS, Machado, VS, Meira, EB, Ganda, EK, Foditsch, C, Bicalho, RC, and Gilbert, RO (2016). Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology 85, 267–274.
| Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Bromfield, JJ, and Sheldon, IM (2013). Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biology of Reproduction 88, 98.
| Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo.Crossref | GoogleScholarGoogle Scholar | 23515670PubMed |
Chen, C, Song, X, Wei, W, et al. (2017). The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nature Communications 8, 875.
| The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases.Crossref | GoogleScholarGoogle Scholar | 29042534PubMed |
Deng, F, McClure, M, Rorie, R, Wang, X, Chai, J, Wei, X, Lai, S, and Zhao, J (2019). The vaginal and fecal microbiomes are related to pregnancy status in beef heifers. Journal of Animal Science and Biotechnology 10, 92.
| The vaginal and fecal microbiomes are related to pregnancy status in beef heifers.Crossref | GoogleScholarGoogle Scholar | 31857897PubMed |
Fang, R-L, Chen, L-X, Shu, W-S, Yao, S-Z, Wang, S-W, and Chen, Y-Q (2016). Barcoded sequencing reveals diverse intrauterine microbiomes in patients suffering with endometrial polyps. American Journal of Translational Research 8, 1581.
| 27186283PubMed |
Fergani, C, Saifullizam, AK, Routly, JE, Smith, RF, and Dobson, H (2012). Estrous behavior, luteinizing hormone and estradiol profiles of intact ewes treated with insulin or endotoxin. Physiology & Behavior 105, 757–765.
| Estrous behavior, luteinizing hormone and estradiol profiles of intact ewes treated with insulin or endotoxin.Crossref | GoogleScholarGoogle Scholar |
Fosch, SE, Ficoseco, CA, Marchesi, A, Cocucci, S, Nader-Macias, MEF, and Perazzi, BE (2018). Contraception: influence on vaginal microbiota and identification of vaginal lactobacilli using MALDI-TOF MS and 16S rDNA sequencing. The Open Microbiology Journal 12, 218.
| Contraception: influence on vaginal microbiota and identification of vaginal lactobacilli using MALDI-TOF MS and 16S rDNA sequencing.Crossref | GoogleScholarGoogle Scholar | 30069261PubMed |
Freitas, AC, Chaban, B, Bocking, A, Rocco, M, Yang, S, Hill, JE, and Money, DM (2017). The vaginal microbiome of pregnant women is less rich and diverse, with lower prevalence of Mollicutes, compared to non-pregnant women. Scientific Reports 7, 9212.
| The vaginal microbiome of pregnant women is less rich and diverse, with lower prevalence of Mollicutes, compared to non-pregnant women.Crossref | GoogleScholarGoogle Scholar | 28835692PubMed |
Gabidullina, RI, Galimyanova, EI, Sharapova, AM, and Bagirli, RR (2020). Effect of combined oral contraceptive containing 17β-estradiol on vaginal environment in women. Medical Alphabet 26, 53–56.
Galvão, KN, Bicalho, RC, and Jeon, SJ (2019). Symposium review: The uterine microbiome associated with the development of uterine disease in dairy cows. Journal of Dairy Science 102, 11786–11797.
| Symposium review: The uterine microbiome associated with the development of uterine disease in dairy cows.Crossref | GoogleScholarGoogle Scholar | 31587913PubMed |
Gdoura, R, Kchaou, W, Chaari, C, Znazen, A, Keskes, L, Rebai, T, and Hammami, A (2007). Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC Infectious Diseases 7, 129.
| Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men.Crossref | GoogleScholarGoogle Scholar | 17988404PubMed |
Gonzalez Moreno, C, Fontana, C, Cocconcelli, PS, Callegari, ML, and Otero, MC (2016). Vaginal microbial communities from synchronized heifers and cows with reproductive disorders. Journal of Applied Microbiology 121, 1232–1241.
| Vaginal microbial communities from synchronized heifers and cows with reproductive disorders.Crossref | GoogleScholarGoogle Scholar | 27442450PubMed |
Hashem, NM, Hassanein, EM, and Simal-Gandara, J (2021). Improving reproductive performance and health of mammals using honeybee products. Antioxidants 10, 336.
| Improving reproductive performance and health of mammals using honeybee products.Crossref | GoogleScholarGoogle Scholar | 33668287PubMed |
Heil, BA, Paccamonti, DL, and Sones, JL (2019). Role for the mammalian female reproductive tract microbiome in pregnancy outcomes. Physiological Genomics 51, 390–399.
| Role for the mammalian female reproductive tract microbiome in pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 31251700PubMed |
Herath, S, Williams, EJ, Lilly, ST, Gilbert, RO, Dobson, H, Bryant, CE, and Sheldon, IM (2007). Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134, 683–693.
| Ovarian follicular cells have innate immune capabilities that modulate their endocrine function.Crossref | GoogleScholarGoogle Scholar | 17965259PubMed |
Herman, AP, Krawczyńska, A, Bochenek, J, Haziak, K, Romanowicz, K, Misztal, T, Antushevich, H, Herman, A, and Tomaszewska-Zaremba, D (2013). The effect of rivastigmine on the LPS-induced suppression of GnRH/LH secretion during the follicular phase of the estrous cycle in ewes. Animal Reproduction Science 138, 203–212.
| The effect of rivastigmine on the LPS-induced suppression of GnRH/LH secretion during the follicular phase of the estrous cycle in ewes.Crossref | GoogleScholarGoogle Scholar | 23557940PubMed |
Hyman, RW, Herndon, CN, Jiang, H, Palm, C, Fukushima, M, Bernstein, D, Vo, KC, Zelenko, Z, Davis, RW, and Giudice, LC (2012). The dynamics of the vaginal microbiome during infertility therapy with in vitro fertilization-embryo transfer. Journal of Assisted Reproduction and Genetics 29, 105–115.
| The dynamics of the vaginal microbiome during infertility therapy with in vitro fertilization-embryo transfer.Crossref | GoogleScholarGoogle Scholar | 22222853PubMed |
Jašarević, E, Howard, CD, Morrison, K, Misic, A, Weinkopff, T, Scott, P, Hunter, C, Beiting, D, and Bale, TL (2018). The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus. Nature Neuroscience 21, 1061–1071.
| The maternal vaginal microbiome partially mediates the effects of prenatal stress on offspring gut and hypothalamus.Crossref | GoogleScholarGoogle Scholar | 29988069PubMed |
Javurek, AB, Spollen, WG, Johnson, SA, Bivens, NJ, Bromert, KH, Givan, SA, and Rosenfeld, CS (2017). Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice. Reproduction, Fertility and Development 29, 1602–1612.
| Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice.Crossref | GoogleScholarGoogle Scholar |
Jeon, SJ, Cunha, F, Vieira-Neto, A, Bicalho, RC, Lima, S, Bicalho, ML, and Galvão, KN (2017). Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome 5, 109.
| Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows.Crossref | GoogleScholarGoogle Scholar | 28841911PubMed |
Jespers, V, Menten, J, Smet, H, Poradosú, S, Abdellati, S, Verhelst, R, Hardy, L, Buvé, A, and Crucitti, T (2012). Quantification of bacterial species of the vaginal microbiome in different groups of women, using nucleic acid amplification tests. BMC Microbiology 12, 83.
| Quantification of bacterial species of the vaginal microbiome in different groups of women, using nucleic acid amplification tests.Crossref | GoogleScholarGoogle Scholar | 22647069PubMed |
Koedooder, R, Mackens, S, Budding, A, Fares, D, Blockeel, C, Laven, J, and Schoenmakers, S (2019). Identification and evaluation of the microbiome in the female and male reproductive tracts. Human Reproduction Update 25, 298–325.
| Identification and evaluation of the microbiome in the female and male reproductive tracts.Crossref | GoogleScholarGoogle Scholar | 30938752PubMed |
Laguardia-Nascimento, M, Branco, KMGR, Gasparini, MR, Giannattasio-Ferraz, S, Leite, LR, Araujo, FMG, Salim, ACM, Nicoli, JR, de Oliveira, GC, and Barbosa-Stancioli, EF (2015). Vaginal microbiome characterization of Nellore cattle using metagenomic analysis. PLoS ONE 10, e0143294.
| Vaginal microbiome characterization of Nellore cattle using metagenomic analysis.Crossref | GoogleScholarGoogle Scholar | 26599789PubMed |
Lavon, Y, Leitner, G, Goshen, T, Braw-Tal, R, Jacoby, S, and Wolfenson, D (2008). Exposure to endotoxin during estrus alters the timing of ovulation and hormonal concentrations in cows. Theriogenology 70, 956–967.
| Exposure to endotoxin during estrus alters the timing of ovulation and hormonal concentrations in cows.Crossref | GoogleScholarGoogle Scholar | 18602682PubMed |
Liu, CM, Osborne, BJW, Hungate, BA, Shahabi, K, Huibner, S, Lester, R, Dwan, MG, Kovacs, C, Contente-Cuomo, TL, Benko, E, Aziz, M, Price, LB, and Kaul, R (2014). The semen microbiome and its relationship with local immunology and viral load in HIV infection. PLoS Pathogens 10, e1004262.
| The semen microbiome and its relationship with local immunology and viral load in HIV infection.Crossref | GoogleScholarGoogle Scholar | 25058515PubMed |
Mahalingam, S, Dharumadurai, D, and Archunan, G (2019). Vaginal microbiome analysis of buffalo (Bubalus bubalis) during estrous cycle using high-throughput amplicon sequence of 16S rRNA gene. Symbiosis 78, 97–106.
| Vaginal microbiome analysis of buffalo (Bubalus bubalis) during estrous cycle using high-throughput amplicon sequence of 16S rRNA gene.Crossref | GoogleScholarGoogle Scholar |
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, and Truu, J (2015). Complementary seminovaginal microbiome in couples. Research in Microbiology 166, 440–447.
| Complementary seminovaginal microbiome in couples.Crossref | GoogleScholarGoogle Scholar | 25869222PubMed |
Mändar, R, Punab, M, Korrovits, P, Türk, S, Ausmees, K, Lapp, E, Preem, J-K, Oopkaup, K, Salumets, A, and Truu, J (2017). Seminal microbiome in men with and without prostatitis. International Journal of Urology 24, 211–216.
| Seminal microbiome in men with and without prostatitis.Crossref | GoogleScholarGoogle Scholar | 28147438PubMed |
Maretti, C, and 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 oligoasthenoteratospermia: a pilot study. Andrology 5, 439–444.
| 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.Crossref | GoogleScholarGoogle Scholar | 28245352PubMed |
Molina, NM, Sola-Leyva, A, Saez-Lara, MJ, Plaza-Diaz, J, Tubić-Pavlović, A, Romero, B, Clavero, A, Mozas-Moreno, J, Fontes, J, and Altmäe, S (2020). New opportunities for endometrial health by modifying uterine microbial composition: present or future? Biomolecules 10, 593.
| New opportunities for endometrial health by modifying uterine microbial composition: present or future?Crossref | GoogleScholarGoogle Scholar |
Monteiro, C, Marques, PI, Cavadas, B, Damião, I, Almeida, V, Barros, N, Barros, A, Carvalho, F, Gomes, S, and Seixas, S (2018). Characterization of microbiota in male infertility cases uncovers differences in seminal hyperviscosity and oligoasthenoteratozoospermia possibly correlated with increased prevalence of infectious bacteria. American Journal of Reproductive Immunology 79, e12838.
| Characterization of microbiota in male infertility cases uncovers differences in seminal hyperviscosity and oligoasthenoteratozoospermia possibly correlated with increased prevalence of infectious bacteria.Crossref | GoogleScholarGoogle Scholar | 29500854PubMed |
Moreno, I, and Franasiak, JM (2017). Endometrial microbiota – new player in town. Fertility and Sterility 108, 32–39.
| Endometrial microbiota – new player in town.Crossref | GoogleScholarGoogle Scholar | 28602480PubMed |
Moreno, I, and Simon, C (2019). Deciphering the effect of reproductive tract microbiota on human reproduction. Reproductive Medicine and Biology 18, 40–50.
| Deciphering the effect of reproductive tract microbiota on human reproduction.Crossref | GoogleScholarGoogle Scholar | 30655720PubMed |
Moreno, I, Codoñer, FM, Vilella, F, Valbuena, D, Martinez-Blanch, JF, Jimenez-Almazán, J, Alonso, R, Alamá, P, Remohí, J, Pellicer, A, Ramon, D, and Simon, C (2016). Evidence that the endometrial microbiota has an effect on implantation success or failure. American Journal of Obstetrics and Gynecology 215, 684–703.
| Evidence that the endometrial microbiota has an effect on implantation success or failure.Crossref | GoogleScholarGoogle Scholar | 27717732PubMed |
Pascottini, OB, Van Schyndel, SJ, Spricigo, JFW, Rousseau, J, Weese, JS, and LeBlanc, SJ (2020). Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis. Scientific Reports 10, 12353.
| Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis.Crossref | GoogleScholarGoogle Scholar | 32704012PubMed |
Pelzer, ES, Allan, JA, Waterhouse, MA, Ross, T, Beagley, KW, and Knox, CL (2013). Microorganisms within human follicular fluid: effects on IVF. PloS ONE 8, e59062.
| Microorganisms within human follicular fluid: effects on IVF.Crossref | GoogleScholarGoogle Scholar | 23554970PubMed |
Pelzer, ES, Willner, D, Buttini, M, and Huygens, F (2018). A role for the endometrial microbiome in dysfunctional menstrual bleeding. Antonie van Leeuwenhoek 111, 933–943.
| A role for the endometrial microbiome in dysfunctional menstrual bleeding.Crossref | GoogleScholarGoogle Scholar | 29299770PubMed |
Pereira, LC, Correia, AF, da Silva, ZDL, de Resende, CN, Brandão, F, Almeida, RM, and de Medeiros Nóbrega, YK (2021). Vulvovaginal candidiasis and current perspectives: new risk factors and laboratory diagnosis by using MALDI TOF for identifying species in primary infection and recurrence. European Journal of Clinical Microbiology & Infectious Diseases 40, 1681–1693.
| Vulvovaginal candidiasis and current perspectives: new risk factors and laboratory diagnosis by using MALDI TOF for identifying species in primary infection and recurrence.Crossref | GoogleScholarGoogle Scholar |
Peymani R, DeCherney A (2016) Microbiome, infection and inflammation in infertility. In ‘Genital infections and infertility’. (Ed. A Darwish) pp. 99–133. (IntechOpen)
Piersanti, RL, Horlock, AD, Block, J, Santos, JE, Sheldon, IM, and Bromfield, JJ (2019). Persistent effects on bovine granulosa cell transcriptome after resolution of uterine disease. Reproduction 158, 35–46.
| Persistent effects on bovine granulosa cell transcriptome after resolution of uterine disease.Crossref | GoogleScholarGoogle Scholar | 30933928PubMed |
Pino, A, Giunta, G, Randazzo, CL, Caruso, S, Caggia, C, and Cianci, A (2017). Bacterial biota of women with bacterial vaginosis treated with lactoferrin: an open prospective randomized trial. Microbial Ecology in Health and Disease 28, 1357417.
| Bacterial biota of women with bacterial vaginosis treated with lactoferrin: an open prospective randomized trial.Crossref | GoogleScholarGoogle Scholar | 28959181PubMed |
Pino, A, Bartolo, E, Caggia, C, Cianci, A, and Randazzo, CL (2019). Detection of vaginal lactobacilli as probiotic candidates. Scientific Reports 9, 3355.
| Detection of vaginal lactobacilli as probiotic candidates.Crossref | GoogleScholarGoogle Scholar | 30833631PubMed |
Price, JC, Bromfield, JJ, and Sheldon, IM (2013). Pathogen-associated molecular patterns initiate inflammation and perturb the endocrine function of bovine granulosa cells from ovarian dominant follicles via TLR2 and TLR4 pathways. Endocrinology 154, 3377–3386.
| Pathogen-associated molecular patterns initiate inflammation and perturb the endocrine function of bovine granulosa cells from ovarian dominant follicles via TLR2 and TLR4 pathways.Crossref | GoogleScholarGoogle Scholar | 23825132PubMed |
Qi, X, Yun, C, Pang, Y, and Qiao, J (2021). The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes 13, 1–21.
| The impact of the gut microbiota on the reproductive and metabolic endocrine system.Crossref | GoogleScholarGoogle Scholar | 33722164PubMed |
Ravel, J, Gajer, P, Abdo, Z, et al. (2011). Vaginal microbiome of reproductive-age women. Proceedings of the National Academy of Sciences of the United States of America 108, 4680–4687.
| Vaginal microbiome of reproductive-age women.Crossref | GoogleScholarGoogle Scholar | 20534435PubMed |
Rizzo, AE, Gordon, JC, Berard, AR, Burgener, AD, and Avril, S (2021). The female reproductive tract microbiome – implications for gynecologic cancers and personalized medicine. Journal of Personalized Medicine 11, 546.
| The female reproductive tract microbiome – implications for gynecologic cancers and personalized medicine.Crossref | GoogleScholarGoogle Scholar | 34208337PubMed |
Rodrigues, NF, Kästle, J, Coutinho, TJD, Amorim, AT, Campos, GB, Santos, VM, Marques, LM, Timenetsky, J, and de Farias, ST (2015). Qualitative analysis of the vaginal microbiota of healthy cattle and cattle with genital-tract disease. Genetics and Molecular Research 14, 6518–6528.
| Qualitative analysis of the vaginal microbiota of healthy cattle and cattle with genital-tract disease.Crossref | GoogleScholarGoogle Scholar | 26125856PubMed |
Rodríguez, C, Cofré, J, Sánchez, M, Fernández, P, Boggiano, G, and Castro, E (2011). Lactobacilli isolated from vaginal vault of dairy and meat cows during progesteronic stage of estrous cycle. Anaerobe 17, 15–18.
| Lactobacilli isolated from vaginal vault of dairy and meat cows during progesteronic stage of estrous cycle.Crossref | GoogleScholarGoogle Scholar | 21145403PubMed |
Salah, RM, Allam, AM, Magdy, AM, and Mohamed, AS (2013). Bacterial vaginosis and infertility: cause or association? European Journal of Obstetrics & Gynecology and Reproductive Biology 167, 59–63.
| Bacterial vaginosis and infertility: cause or association?Crossref | GoogleScholarGoogle Scholar |
Saleh, M, Haraki Nezhad, MT, and Salmani, V (2014). Detection of some bacterial causes of abortion in Afshari sheep using real time PCR detection and sensitivity assessment of campylobacter primers. Agricultural Biotechnology Journal 6, 107–120.
Schreiber, CA, Harwood, BJ, Switzer, GE, Creinin, MD, Reeves, MF, and Ness, RB (2006). Training and attitudes about contraceptive management across primary care specialties: a survey of graduating residents. Contraception 73, 618–622.
| Training and attitudes about contraceptive management across primary care specialties: a survey of graduating residents.Crossref | GoogleScholarGoogle Scholar | 16730495PubMed |
Sheldon, IM, Cronin, JG, Healey, GD, Gabler, C, Heuwieser, W, Streyl, D, Bromfield, JJ, Miyamoto, A, Fergani, C, and Dobson, H (2014). Innate immunity and inflammation of the bovine female reproductive tract in health and disease. Reproduction 148, R41–R51.
| Innate immunity and inflammation of the bovine female reproductive tract in health and disease.Crossref | GoogleScholarGoogle Scholar | 24890752PubMed |
Shpigel, NY, Adler-Ashkenazy, L, Scheinin, S, Goshen, T, Arazi, A, Pasternak, Z, and Gottlieb, Y (2017). Characterization and identification of microbial communities in bovine necrotic vulvovaginitis. The Veterinary Journal 219, 34–39.
| Characterization and identification of microbial communities in bovine necrotic vulvovaginitis.Crossref | GoogleScholarGoogle Scholar | 28093107PubMed |
Sirota, I, Zarek, SM, and Segars, JH (2014). Potential influence of the microbiome on infertility and assisted reproductive technology. Seminars in Reproductive Medicine 32, 35–42.
| Potential influence of the microbiome on infertility and assisted reproductive technology.Crossref | GoogleScholarGoogle Scholar | 24390919PubMed |
Stumpf, RM, Wilson, BA, Rivera, A, Yildirim, S, Yeoman, CJ, Polk, JD, White, BA, and Leigh, SR (2013). The primate vaginal microbiome: comparative context and implications for human health and disease. American Journal of Physical Anthropology 152, 119–134.
| The primate vaginal microbiome: comparative context and implications for human health and disease.Crossref | GoogleScholarGoogle Scholar | 24166771PubMed |
Suzuki, C, Yoshioka, K, Iwamura, S, and Hirose, H (2001). Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domestic Animal Endocrinology 20, 267–278.
| Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 11518620PubMed |
Swartz, JD, Lachman, M, Westveer, K, O’Neill, T, Geary, T, Kott, RW, Berardinelli, JG, Hatfield, PG, Thomson, JM, Roberts, A, and Yeoman, CJ (2014). 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 1, 19.
| Characterization of the vaginal microbiota of ewes and cows reveals a unique microbiota with low levels of lactobacilli and near-neutral pH.Crossref | GoogleScholarGoogle Scholar | 26664918PubMed |
Vander Borght, M, and Wyns, C (2018). Fertility and infertility: definition and epidemiology. Clinical Biochemistry 62, 2–10.
| Fertility and infertility: definition and epidemiology.Crossref | GoogleScholarGoogle Scholar | 29555319PubMed |
Verstraelen, H, Verhelst, R, Claeys, G, De Backer, E, Temmerman, M, and Vaneechoutte, M (2009). Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora. BMC Microbiology 9, 116.
| Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora.Crossref | GoogleScholarGoogle Scholar | 19490622PubMed |
Walsh, DM, Hokenstad, AN, Chen, J, Sung, J, Jenkins, GD, Chia, N, Nelson, H, Mariani, A, and Walther-Antonio, MRS (2019). Postmenopause as a key factor in the composition of the Endometrial Cancer Microbiome (ECbiome). Scientific Reports 9, 19213.
| Postmenopause as a key factor in the composition of the Endometrial Cancer Microbiome (ECbiome).Crossref | GoogleScholarGoogle Scholar | 31844128PubMed |
Walther-António, MRS, Chen, J, Multinu, F, Hokenstad, A, Distad, TJ, Cheek, EH, Keeney, GL, Creedon, DJ, Nelson, H, Mariani, A, and Chia, N (2016). Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Medicine 8, 122.
| Potential contribution of the uterine microbiome in the development of endometrial cancer.Crossref | GoogleScholarGoogle Scholar |
Wang, Y, Ametaj, BN, Ambrose, DJ, and Gänzle, MG (2013). Characterisation of the bacterial microbiota of the vagina of dairy cows and isolation of pediocin-producing Pediococcus acidilactici. BMC Microbiology 13, 19.
| Characterisation of the bacterial microbiota of the vagina of dairy cows and isolation of pediocin-producing Pediococcus acidilactici.Crossref | GoogleScholarGoogle Scholar | 23356904PubMed |
Wang, Y, Wang, J, Li, H, Fu, K, Pang, B, Yang, Y, Liu, Y, Tian, W, and Cao, R (2018). Characterization of the cervical bacterial community in dairy cows with metritis and during different physiological phases. Theriogenology 108, 306–313.
| Characterization of the cervical bacterial community in dairy cows with metritis and during different physiological phases.Crossref | GoogleScholarGoogle Scholar | 29284157PubMed |
Wee, BA, Thomas, M, Sweeney, EL, Frentiu, FD, Samios, M, Ravel, J, Gajer, P, Myers, G, Timms, P, Allan, JA, and Huston, WM (2018). A retrospective pilot study to determine whether the reproductive tract microbiota differs between women with a history of infertility and fertile women. Australian and New Zealand Journal of Obstetrics and Gynaecology 58, 341–348.
| A retrospective pilot study to determine whether the reproductive tract microbiota differs between women with a history of infertility and fertile women.Crossref | GoogleScholarGoogle Scholar | 29280134PubMed |
Weng, S-L, Chiu, C-M, Lin, F-M, et al. (2014). Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PloS ONE 9, e110152.
| Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality.Crossref | GoogleScholarGoogle Scholar | 25340531PubMed |
Yeoman, CJ, Ishaq, SL, Bichi, E, Olivo, SK, Lowe, J, and Aldridge, BM (2018). Biogeographical differences in the influence of maternal microbial sources on the early successional development of the bovine neonatal gastrointestinal tract. Scientific Reports 8, 3197.
| Biogeographical differences in the influence of maternal microbial sources on the early successional development of the bovine neonatal gastrointestinal tract.Crossref | GoogleScholarGoogle Scholar | 29453364PubMed |
Younge, N, McCann, JR, Ballard, J, Plunkett, C, Akhtar, S, Araújo-Pérez, F, Murtha, A, Brandon, D, and Seed, PC (2019). Fetal exposure to the maternal microbiota in humans and mice. JCI Insight 4, e127806.
| Fetal exposure to the maternal microbiota in humans and mice.Crossref | GoogleScholarGoogle Scholar |
Younis, N, and Mahasneh, A (2020). Probiotics and the envisaged role in treating human infertility. Middle East Fertility Society Journal 25, 33.
| Probiotics and the envisaged role in treating human infertility.Crossref | GoogleScholarGoogle Scholar |
Zinzendorf, N, Kouassi-Agbessi, B, Lathro, J, Don, C, Kouadio, L, and Loukou, Y (2008). Ureaplasma urealyticum or Mycoplasma hominis infections and semen quality of infertile men in Abidjan. Journal of Reproduction and Contraception 19, 65–72.
| Ureaplasma urealyticum or Mycoplasma hominis infections and semen quality of infertile men in Abidjan.Crossref | GoogleScholarGoogle Scholar |