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Frontiers in microbiology2022; 13; 884574; doi: 10.3389/fmicb.2022.884574

Endometrial and vaginal microbiome in donkeys with and without clinical endometritis.

Abstract: Endometrial and vaginal microbiomes are critical in the study of endometritis, which is an important cause of infertility in donkeys. Our objective was to investigate the difference of the endometrial and vaginal microbiomes between healthy donkey jennies (group C) and jennies with endometritis (group E). Endometrial and vaginal swab samples were collected, and the 16 s rRNA gene amplicon high-throughput sequencing technique was applied to identify the microbial composition in the samples. A similar microbial composition pattern was found between endometrial and vaginal samples, which indicated the impact of the vaginal microbiome on the endometrial microbial environment and health. There was a significant difference of endometrial and vaginal swab samples between the two groups. and were significantly more abundant in endometrial and vaginal microbiomes of group E than in group C. Their dominance was consistent with increased anaerobic bacterial taxa in the functional analysis, which might be associated with the pathogenesis of endometritis in donkeys. , a bacterial family reported in bovine semen, was statistically more abundant in endometrial microbiome of group E than in group C, which might suggest an association between high abundance of possibly due to uncleared semen and donkey endometritis. Our study revealed the composition of the vaginal and endometrial microbiomes in healthy and endometritis donkeys. These findings will provide more insights into the pathogenesis of donkey endometritis.
Publication Date: 2022-08-01 PubMed ID: 35979491PubMed Central: PMC9376452DOI: 10.3389/fmicb.2022.884574Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research aimed to study the differences in the vaginal and endometrial microbiomes (community of microorganisms) in healthy donkeys and those suffering from endometritis, a disease causing infertility.

Research Purpose and Methodology

  • The main purpose of this study was to analyze and compare the composition of the endometrial and vaginal microbiomes in healthy donkeys (group C) and those showing symptoms of endometritis (group E), a common cause of infertility in these animals.
  • For the research, the scientists used endometrial and vaginal swab samples collected from the donkeys.
  • To identify the microbial composition in these samples, they used a method known as the 16 s rRNA gene amplicon high-throughput sequencing technique.

Key Findings

  • The researchers noted a parallel microbial pattern in both the endometrial and vaginal samples, suggesting the important role of the vaginal microbiome in determining the microbial environment of the endometrium and in overall health.
  • There was a marked difference between the composition of the endometrial and vaginal samples taken from the two different groups (healthy donkeys and those affected by endometritis).
  • Particular types of anaerobic bacteria, which thrive without oxygen, were found significantly more in both the endometrial and vaginal microbiomes of group E (donkeys with endometritis) than in group C (healthy donkeys).
  • This dominance of anaerobic bacteria aligns with the functional analysis the researchers conducted, suggesting these bacteria might be linked to the pathogenesis, or development, of endometritis in donkeys.
  • The research also found that a particular type of bacteria, previously linked with bovine semen, was statistically more common in the endometrial microbiome of donkeys with endometritis. Researchers connected its presence to uncleared semen, hinting at potential causality between the bacteria and the condition.

Implications of the Research

  • This study offers a deeper understanding of the composition of both the vaginal and endometrial microbiomes in both healthy and diseased donkeys.
  • By identifying the potential link between the presence of certain bacteria and the development of endometritis, the findings pave the way for future research and investigation into the pathogenesis of the disease, as well as potential treatments for donkeys dealing with this form of infertility.

Cite This Article

APA
Li J, Zhu Y, Mi J, Zhao Y, Holyoak GR, Yi Z, Wu R, Wang Z, Zeng S. (2022). Endometrial and vaginal microbiome in donkeys with and without clinical endometritis. Front Microbiol, 13, 884574. https://doi.org/10.3389/fmicb.2022.884574

Publication

ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 13
Pages: 884574
PII: 884574

Researcher Affiliations

Li, Jing
  • Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
  • National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University, Beijing, China.
Zhu, Yiping
  • Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Mi, Junpeng
  • School of Veterinary Science, University of Sydney, Sydney, NSW, Australia.
Zhao, Yufei
  • Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Holyoak, Gilbert Reed
  • College of Veterinary Medicine, Oklahoma State University, Stillwater, OK, United States.
Yi, Ziwen
  • Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Wu, Rongzheng
  • Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, Beijing, China.
Wang, Zixuan
  • College of Veterinary Medicine, Kansas State University, Manhattan, KS, United States.
Zeng, Shenming
  • National Engineering Laboratory for Animal Breeding, Key Laboratory of Animal Genetics and Breeding of the Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University, Beijing, China.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 58 references
  1. Agerholm JS. Coxiella burnetii associated reproductive disorders in domestic animals--a critical review.. Acta Vet Scand 2013 Feb 18;55(1):13.
    doi: 10.1186/1751-0147-55-13pmc: PMC3577508pubmed: 23419216google scholar: lookup
  2. Albihn A, Båverud V, Magnusson U. Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems.. Acta Vet Scand 2003;44(3-4):121-9.
    doi: 10.1186/1751-0147-44-121pmc: PMC1831563pubmed: 15074625google scholar: lookup
  3. Amos MR, Healey GD, Goldstone RJ, Mahan SM, Düvel A, Schuberth HJ, Sandra O, Zieger P, Dieuzy-Labaye I, Smith DG, Sheldon IM. Differential endometrial cell sensitivity to a cholesterol-dependent cytolysin links Trueperella pyogenes to uterine disease in cattle.. Biol Reprod 2014 Mar;90(3):54.
    doi: 10.1095/biolreprod.113.115972pubmed: 24478394google scholar: lookup
  4. Ault TB, Clemmons BA, Reese ST, Dantas FG, Franco GA, Smith TPL, Edwards JL, Myer PR, Pohler KG. Bacterial taxonomic composition of the postpartum cow uterus and vagina prior to artificial insemination1.. J Anim Sci 2019 Oct 3;97(10):4305-4313.
    doi: 10.1093/jas/skz212pmc: PMC6776284pubmed: 31251804google scholar: lookup
  5. Barba M, Martínez-Boví R, Quereda JJ, Mocé ML, Plaza-Dávila M, Jiménez-Trigos E, Gómez-Martín Á, González-Torres P, Carbonetto B, García-Roselló E. Vaginal Microbiota Is Stable throughout the Estrous Cycle in Arabian Maress.. Animals (Basel) 2020 Nov 3;10(11).
    doi: 10.3390/ani10112020pmc: PMC7692283pubmed: 33153053google scholar: lookup
  6. Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5, 627–640.
    doi: 10.3390/d5030627google scholar: lookup
  7. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.. Nat Biotechnol 2019 Aug;37(8):852-857.
    doi: 10.1038/s41587-019-0209-9pmc: PMC7015180pubmed: 31341288google scholar: lookup
  8. 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 Jul;232(7):1681-1688.
    doi: 10.1002/jcp.25806pubmed: 28098358google scholar: lookup
  9. Chen H, Fu K, Pang B, Wang J, Li H, Jiang Z, Feng Y, Tian W, Cao R. Determination of uterine bacterial community in postpartum dairy cows with metritis based on 16S rDNA sequencing.. Vet Anim Sci 2020 Dec;10:100102.
    doi: 10.1016/j.vas.2020.100102pmc: PMC7386775pubmed: 32734024google scholar: lookup
  10. Christoffersen M, Brandis L, Samuelsson J, Bojesen AM, Troedsson MH, Petersen MR. Diagnostic double-guarded low-volume uterine lavage in mares.. Theriogenology 2015 Jan 15;83(2):222-7.
  11. Christoffersen M, Woodward E, Bojesen AM, Jacobsen S, Petersen MR, Troedsson MH, Lehn-Jensen H. Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis.. BMC Vet Res 2012 Mar 29;8:41.
    doi: 10.1186/1746-6148-8-41pmc: PMC3368729pubmed: 22458733google scholar: lookup
  12. Cocchia N, Paciello O, Auletta L, Uccello V, Silvestro L, Mallardo K, Paraggio G, Pasolini MP. Comparison of the cytobrush, cottonswab, and low-volume uterine flush techniques to evaluate endometrial cytology for diagnosing endometritis in chronically infertile mares.. Theriogenology 2012 Jan 1;77(1):89-98.
  13. de Amorim M D, Gartley C J, Foster R A, Hill A, Scholtz E L, Hayes A. Comparison of clinical signs, endometrial culture, endometrial cytology, uterine low-volume lavage, and uterine biopsy and combinations in the diagnosis of equine endometritis. J Equine Vet Sci 44, 54–61.
  14. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads.. Nat Methods 2013 Oct;10(10):996-8.
    doi: 10.1038/nmeth.2604pubmed: 23955772google scholar: lookup
  15. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection.. Bioinformatics 2011 Aug 15;27(16):2194-200.
  16. Elliott L, McMahon KJ, Gier HT, Marion GB. Uterus of the cow after parturition: bacterial content.. Am J Vet Res 1968 Jan;29(1):77-81.
    pubmed: 5688806
  17. Frontoso R, De Carlo E, Pasolini MP, van der Meulen K, Pagnini U, Iovane G, De Martino L. Retrospective study of bacterial isolates and their antimicrobial susceptibilities in equine uteri during fertility problems.. Res Vet Sci 2008 Feb;84(1):1-6.
    doi: 10.1016/j.rvsc.2007.02.008pubmed: 17434193google scholar: lookup
  18. Gao N, Du Y, Zheng X, Shu S, Suo J, Han M. Endometritis in donkeys associated with Streptococcus equi subspecies zooepidemicus infection. The Pakistan Veterinary Journal 40, 537–539.
    doi: 10.29261/pakvetj/2020.081google scholar: lookup
  19. Garber A, Hastie P, Murray JA. Factors Influencing Equine Gut Microbiota: Current Knowledge.. J Equine Vet Sci 2020 May;88:102943.
    doi: 10.1016/j.jevs.2020.102943pubmed: 32303307google scholar: lookup
  20. Heil B, Thompson S, Kearns T, Davolli G, King G, Sones J. Metagenetic characterization of the resident equine uterine microbiome using multiple techniques. J Equine Vet Sci 66, 111.
  21. Holyoak G R, Lyman C C, Wieneke X, DeSilva U. The equine endometrial microbiome. Clin. Theriogenol. 10, 273–278.
  22. Husso A, Jalanka J, Alipour MJ, Huhti P, Kareskoski M, Pessa-Morikawa T, Iivanainen A, Niku M. The composition of the perinatal intestinal microbiota in horse.. Sci Rep 2020 Jan 16;10(1):441.
    doi: 10.1038/s41598-019-57003-8pmc: PMC6965133pubmed: 31949191google scholar: lookup
  23. Jeon SJ, Vieira-Neto A, Gobikrushanth M, Daetz R, Mingoti RD, Parize AC, de Freitas SL, da Costa AN, Bicalho RC, Lima S, Jeong KC, Galvão KN. Uterine Microbiota Progression from Calving until Establishment of Metritis in Dairy Cows.. Appl Environ Microbiol 2015 Sep;81(18):6324-32.
    doi: 10.1128/aem.01753-15pmc: PMC4542247pubmed: 26150453google scholar: lookup
  24. Jones E. Characterization of the equine Microbiome during late Gestation and the Early Postpartum period, and at Various times during the Estrous cycle in mares Being bred with raw or Extended semen. .
  25. Katila T. Evaluation of diagnostic methods in equine endometritis.. Reprod Biol 2016 Sep;16(3):189-196.
    doi: 10.1016/j.repbio.2016.06.002pubmed: 27692361google scholar: lookup
  26. Kilburn C, Rooks DJ, McCarthy AJ, Murray RD. Antimicrobial resistance in some gram-negative bacteria isolated from the bovine ejaculate.. Reprod Domest Anim 2013 Jun;48(3):525-8.
    doi: 10.1111/rda.12127pubmed: 23331295google scholar: lookup
  27. Knudsen LR, Karstrup CC, Pedersen HG, Angen Ø, Agerholm JS, Rasmussen EL, Jensen TK, Klitgaard K. An investigation of the microbiota in uterine flush samples and endometrial biopsies from dairy cows during the first 7 weeks postpartum.. Theriogenology 2016 Jul 15;86(2):642-50.
  28. Koskinen R, Ali-Vehmas T, Kämpfer P, Laurikkala M, Tsitko I, Kostyal E, Atroshi F, Salkinoja-Salonen M. Characterization of Sphingomonas isolates from Finnish and Swedish drinking water distribution systems.. J Appl Microbiol 2000 Oct;89(4):687-96.
  29. LeBlanc MM. Advances in the diagnosis and treatment of chronic infectious and post-mating-induced endometritis in the mare.. Reprod Domest Anim 2010 Jun;45 Suppl 2:21-7.
  30. LeBlanc MM, Causey RC. Clinical and subclinical endometritis in the mare: both threats to fertility.. Reprod Domest Anim 2009 Sep;44 Suppl 3:10-22.
  31. LeBlanc MM, Magsig J, Stromberg AJ. Use of a low-volume uterine flush for diagnosing endometritis in chronically infertile mares.. Theriogenology 2007 Aug;68(3):403-12.
  32. Lietaer L, Bogado Pascottini O, Hernandez-Sanabria E, Kerckhof FM, Lacoere T, Boon N, Vlaminck L, Opsomer G, Van de Wiele T. Low microbial biomass within the reproductive tract of mid-lactation dairy cows: A study approach.. J Dairy Sci 2021 May;104(5):6159-6174.
    doi: 10.3168/jds.2020-19554pubmed: 33685679google scholar: lookup
  33. Lozano FM, Bernabeu A, Lledo B, Morales R, Diaz M, Aranda FI, Llacer J, Bernabeu R. Characterization of the vaginal and endometrial microbiome in patients with chronic endometritis.. Eur J Obstet Gynecol Reprod Biol 2021 Aug;263:25-32.
    doi: 10.1016/j.ejogrb.2021.05.045pubmed: 34144490google scholar: lookup
  34. Lyman CC, Holyoak GR, Meinkoth K, Wieneke X, Chillemi KA, DeSilva U. Canine endometrial and vaginal microbiomes reveal distinct and complex ecosystems.. PLoS One 2019;14(1):e0210157.
  35. Mahalingam S, Dharumadurai D, Archunan G. Vaginal microbiome analysis of buffalo (Bubalus bubalis) during estrous cycle using high-throughput amplicon sequence of 16S rRNA gene. Symbiosis 78, 97–106.
  36. Miller EA, Beasley DE, Dunn RR, Archie EA. Lactobacilli Dominance and Vaginal pH: Why Is the Human Vaginal Microbiome Unique?. Front Microbiol 2016;7:1936.
    doi: 10.3389/fmicb.2016.01936pmc: PMC5143676pubmed: 28008325google scholar: lookup
  37. Miranda-CasoLuengo R, Lu J, Williams EJ, Miranda-CasoLuengo AA, Carrington SD, Evans ACO, Meijer WG. Delayed differentiation of vaginal and uterine microbiomes in dairy cows developing postpartum endometritis.. PLoS One 2019;14(1):e0200974.
  38. Mitchell CM, Haick A, Nkwopara E, Garcia R, Rendi M, Agnew K, Fredricks DN, Eschenbach D. Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women.. Am J Obstet Gynecol 2015 May;212(5):611.e1-9.
    doi: 10.1016/j.ajog.2014.11.043pmc: PMC4754962pubmed: 25524398google scholar: lookup
  39. Moreno I, Franasiak JM. Endometrial microbiota-new player in town.. Fertil Steril 2017 Jul;108(1):32-39.
  40. Moreno I, Simon C. Relevance of assessing the uterine microbiota in infertility.. Fertil Steril 2018 Aug;110(3):337-343.
  41. H A Morris L, M McCue P, Aurich C. Equine endometritis: a review of challenges and new approaches.. Reproduction 2020 Nov;160(5):R95-R110.
    doi: 10.1530/rep-19-0478pubmed: 32805710google scholar: lookup
  42. Nielsen JM. Endometritis in the mare: a diagnostic study comparing cultures from swab and biopsy.. Theriogenology 2005 Aug;64(3):510-8.
  43. Nielsen J M, Troedsson M H, Pedersen M R, Bojesen A M, Lehn-Jensen H, Zent W W. Diagnosis of endometritis in the mare based on bacteriological and cytological examinations of the endometrium: comparison of results obtained by swabs and biopsies. J Equine Vet Sci 30, 27–30.
  44. Pascottini OB, Van Schyndel SJ, Spricigo JFW, Rousseau J, Weese JS, LeBlanc SJ. Dynamics of uterine microbiota in postpartum dairy cows with clinical or subclinical endometritis.. Sci Rep 2020 Jul 23;10(1):12353.
    doi: 10.1038/s41598-020-69317-zpmc: PMC7378066pubmed: 32704012google scholar: lookup
  45. Rantala M, Attia S, Koukila-Kähkölä P, de Hoog S, Anttila M, Katila T. Cladophialophora bantiana as an Emerging Pathogen in Animals: Case Report of Equine Endometritis and Review of the Literature.. J Clin Microbiol 2015 Sep;53(9):3047-53.
    doi: 10.1128/JCM.00728-15pmc: PMC4540934pubmed: 26085616google scholar: lookup
  46. Riddle WT, LeBlanc MM, Stromberg AJ. Relationships between uterine culture, cytology and pregnancy rates in a Thoroughbred practice.. Theriogenology 2007 Aug;68(3):395-402.
  47. Rota A, Panzani D, Sabatini C, Camillo F. Donkey jack (Equus asinus) semen cryopreservation: studies of seminal parameters, post breeding inflammatory response, and fertility in donkey jennies.. Theriogenology 2012 Nov;78(8):1846-54.
  48. Sanglard LP, Schmitz-Esser S, Gray KA, Linhares DCL, Yeoman CJ, Dekkers JCM, Niederwerder MC, Serão NVL. Investigating the relationship between vaginal microbiota and host genetics and their impact on immune response and farrowing traits in commercial gilts.. J Anim Breed Genet 2020 Jan;137(1):84-102.
    doi: 10.1111/jbg.12456pubmed: 31762123google scholar: lookup
  49. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation.. Genome Biol 2011 Jun 24;12(6):R60.
    doi: 10.1186/gb-2011-12-6-r60pmc: PMC3218848pubmed: 21702898google scholar: lookup
  50. Sheldon IM, Lewis GS, LeBlanc S, Gilbert RO. Defining postpartum uterine disease in cattle.. Theriogenology 2006 May;65(8):1516-30.
  51. Siddiqui H, Nederbragt AJ, Lagesen K, Jeansson SL, Jakobsen KS. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons.. BMC Microbiol 2011 Nov 2;11:244.
    doi: 10.1186/1471-2180-11-244pmc: PMC3228714pubmed: 22047020google scholar: lookup
  52. Troedsson MH. Uterine clearance and resistance to persistent endometritis in the mare.. Theriogenology 1999 Aug;52(3):461-71.
    doi: 10.1016/s0093-691x(99)00143-0pubmed: 10734380google scholar: lookup
  53. Wang J, Li C, Nesengani LT, Gong Y, Zhang S, Lu W. Characterization of vaginal microbiota of endometritis and healthy sows using high-throughput pyrosequencing of 16S rRNA gene.. Microb Pathog 2017 Oct;111:325-330.
    doi: 10.1016/j.micpath.2017.08.030pubmed: 28867636google scholar: lookup
  54. Wang ML, Liu MC, Xu J, An LG, Wang JF, Zhu YH. Uterine Microbiota of Dairy Cows With Clinical and Subclinical Endometritis.. Front Microbiol 2018;9:2691.
    doi: 10.3389/fmicb.2018.02691pmc: PMC6232309pubmed: 30459745google scholar: lookup
  55. Wang J, Sun C, Liu C, Yang Y, Lu W. Comparison of vaginal microbial community structure in healthy and endometritis dairy cows by PCR-DGGE and real-time PCR.. Anaerobe 2016 Apr;38:1-6.
  56. Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D. BugBase predicts organism-level microbiome phenotypes. BioRxiv 133462:441.
  57. Zhang L, Wang L, Dai Y, Tao T, Wang J, Wu Y, Zeng X, Zhang J. Effect of Sow Intestinal Flora on the Formation of Endometritis.. Front Vet Sci 2021;8:663956.
    doi: 10.3389/fvets.2021.663956pmc: PMC8249707pubmed: 34222396google scholar: lookup
  58. Zhu Y, Wang X, Deng L, Chen S, Zhu C, Li J. Effects of Pasture Grass, Silage, and Hay Diet on Equine Fecal Microbiota.. Animals (Basel) 2021 May 7;11(5).
    doi: 10.3390/ani11051330pmc: PMC8148540pubmed: 34066969google scholar: lookup

Citations

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  1. Tyrnenopoulou P, Fthenakis GC. Clinical Aspects of Bacterial Distribution and Antibiotic Resistance in the Reproductive System of Equids. Antibiotics (Basel) 2023 Mar 28;12(4).
    doi: 10.3390/antibiotics12040664pubmed: 37107026google scholar: lookup
  2. Poole RK, Soffa DR, McAnally BE, Smith MS, Hickman-Brown KJ, Stockland EL. Reproductive Microbiomes in Domestic Livestock: Insights Utilizing 16S rRNA Gene Amplicon Community Sequencing. Animals (Basel) 2023 Jan 31;13(3).
    doi: 10.3390/ani13030485pubmed: 36766374google scholar: lookup
  3. Guo L, Holyoak GR, DeSilva U. Endometrial microbiome in mares with and without clinical endometritis. Front Vet Sci 2025;12:1588432.
    doi: 10.3389/fvets.2025.1588432pubmed: 40822659google scholar: lookup
  4. Khan MZ, Li Y, Zhu M, Li M, Wang T, Zhang Z, Liu W, Ma Q, Wang C. Advances in Donkey Disease Surveillance and Microbiome Characterization in China. Microorganisms 2025 Mar 26;13(4).
  5. da Silva-Álvarez E, Gómez-Arrones V, Correa-Fiz F, Martín-Cano FE, Gaitskell-Phillips G, Carrasco JJ, Rey J, Aparicio IM, Peña FJ, Alonso JM, Ortega-Ferrusola C. Metagenomic and proteomic analyses reveal similar reproductive microbial profiles and shared functional pathways in uterine immune regulation in mares and jennies. PLoS One 2025;20(4):e0321389.
    doi: 10.1371/journal.pone.0321389pubmed: 40238748google scholar: lookup
  6. Wang Z, Zeng S, Wang Y, Wang T, Qu H, Zhu Y, Li J. Reproductive Disorders in Donkeys: Current Evidence and Update. Animals (Basel) 2024 Aug 28;14(17).
    doi: 10.3390/ani14172494pubmed: 39272279google scholar: lookup
  7. Gil-Miranda A, Macnicol J, Orellana-Guerrero D, Samper JC, Gomez DE. Reproductive Tract Microbiota of Mares. Vet Sci 2024 Jul 18;11(7).
    doi: 10.3390/vetsci11070324pubmed: 39058008google scholar: lookup
  8. Gil-Miranda A, Caddey B, Orellana-Guerrero D, Smith H, Samper JC, Gomez DE. Vaginal and Uterine Microbiota of Healthy Maiden Mares during Estrus. Vet Sci 2024 Jul 18;11(7).
    doi: 10.3390/vetsci11070323pubmed: 39058007google scholar: lookup
  9. Salman MM, Nawaz M, Yaqub T, Mushtaq MH. Milk microbiota of Holstein Friesian cattle reared in Lahore: Association with mastitis. Saudi J Biol Sci 2024 Jun;31(6):103984.
    doi: 10.1016/j.sjbs.2024.103984pubmed: 38633360google scholar: lookup
  10. Silva JA, Castañares M, Mouguelar H, Valenciano JA, Pellegrino MS. Isolation of lactic acid bacteria from the reproductive tract of mares as potentially beneficial strains to prevent equine endometritis. Vet Res Commun 2024 Jun;48(3):1353-1366.
    doi: 10.1007/s11259-024-10295-2pubmed: 38233700google scholar: lookup