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Home / Equine Research Bank / Animals (Basel) / Antimicrobial Resistance in Equine Reproduction.
Animals : an open access journal from MDPI2021; 11(11); doi: 10.3390/ani11113035

Antimicrobial Resistance in Equine Reproduction.

Abstract: Bacteria develop resistance to antibiotics following low-level "background" exposure to antimicrobial agents as well as from exposure at therapeutic levels during treatment for bacterial infections. In this review, we look specifically at antimicrobial resistance (AMR) in the equine reproductive tract and its possible origin, focusing particularly on antibiotics in semen extenders used in preparing semen doses for artificial insemination. Our review of the literature indicated that AMR in the equine uterus and vagina were reported worldwide in the last 20 years, in locations as diverse as Europe, India, and the United States. Bacteria colonizing the mucosa of the reproductive tract are transferred to semen during collection; further contamination of the semen may occur during processing, despite strict attention to hygiene at critical control points. These bacteria compete with spermatozoa for nutrients in the semen extender, producing metabolic byproducts and toxins that have a detrimental effect on sperm quality. Potential pathogens such as Klebsiella pneumoniae, Escherichia coli, and Pseudomonas aeruginosa may occasionally cause fertility issues in inseminated mares. Antibiotics are added during semen processing, according to legislation, to impede the growth of these microorganisms but may have a detrimental effect on sperm quality, depending on the antimicrobial agent and concentration used. However, this addition of antibiotics is counter to current recommendations on the prudent use of antibiotics, which recommend that antibiotics should be used only for therapeutic purposes and after establishing bacterial sensitivity. There is some evidence of resistance among bacteria found in semen samples. Potential alternatives to the addition of antibiotics are considered, especially physical removal separation of spermatozoa from bacteria. Suggestions for further research with colloid centrifugation are provided.
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Publication Date: 2021-10-22 PubMed ID: 34827768PubMed Central: PMC8614435DOI: 10.3390/ani11113035Google Scholar: Lookup
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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 investigates the growing issue of antimicrobial resistance (AMR) in horse reproduction, exploring how bacteria in the reproductive organs resist antibiotics used in artificial insemination. The authors examine the effects of these antibiotic-resistant bacteria, alternatives to using antibiotics, and areas for future research.

Understanding Antimicrobial Resistance in Equine Reproduction

The researchers focused their study on antibiotic resistance in the reproductive tract of horses. Their main area of interest was to understand the effects of the antibiotics used in semen extenders – a substance used to prepare semen for artificial insemination.

  • The study found that antibiotic-resistant bacteria were present in the uterus and vagina of horses worldwide. These findings were based on literature reports from various locations spanning the last two decades.
  • The bacteria reside on the mucosal surfaces of the reproductive tract, enabling their transfer to the semen during collection. The authors note that additional contamination may occur during processing, even when strict hygiene measures are followed.
  • These bacteria compete with the sperm for nutrients in the semen extender, a process that can generate toxins harmful to sperm quality.

Effects of Antibiotics and Potential Pathogens

The study observed the effects of antibiotics added during semen processing and their impact on sperm quality, as well as the role of potential pathogens that may affect fertility.

  • The researchers highlighted the common practice of adding antibiotics during semen processing to curb the growth of bacteria, despite its potential negative effect on sperm.
  • However, the authors discussed the current recommendations that advocate for prudent use of antibiotics. These guidelines state that antibiotics should be used for therapeutic purposes only and that bacterial sensitivity should first be established.
  • The study identified potential pathogens such as E.coli, Klebsiella, and Pseudomonas that can occasionally contribute to fertility issues in horses.

Alternatives to Antibiotics and Further Research

In closing, the researchers evaluated potential alternatives to using antibiotics during semen processing and suggested potential areas for further research.

  • They explored the possibility of physically removing the bacteria from the semen as an alternative to using antibiotics during processing.
  • The authors identified the need for further research into the use of colloid centrifugation, a technique potentially useful for separating bacteria from sperm during processing.

Cite This Article

APA
Malaluang P, Wilén E, Lindahl J, Hansson I, Morrell JM. (2021). Antimicrobial Resistance in Equine Reproduction. Animals (Basel), 11(11). https://doi.org/10.3390/ani11113035

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 11

Researcher Affiliations

Malaluang, Pongpreecha
  • Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE-75007 Uppsala, Sweden.
Wilén, Elin
  • Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE-75007 Uppsala, Sweden.
Lindahl, Johanna
  • Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE-75007 Uppsala, Sweden.
  • Department of Biosciences, International Livestock Research Institute, P.O. Box 30709, Nairobi 00100, Kenya.
  • Department of Medical Biochemistry and Microbiology, Uppsala University, Box 582, 75123 Uppsala, Sweden.
Hansson, Ingrid
  • Biomedical Science and Veterinary Public Health, Swedish University of Agricultural Sciences (SLU), Box 7036, SE-75007 Uppsala, Sweden.
Morrell, Jane M
  • Clinical Sciences, Swedish University of Agricultural Sciences (SLU), Box 7054, SE-75007 Uppsala, Sweden.

Conflict of Interest Statement

J.M. is the inventor and patent holder of the colloid mentioned in the last section of this article, on alternatives to antibiotics. However, this did not in any way influence the writing of the review.

References

This article includes 82 references
  1. WHO. Antimicrobial resistance.. 2020.
  2. WHO. Antibiotic resistance.. 2020.
  3. Plackett B. Why big pharma has abandoned antibiotics.. Nature 2020;586:S50–S52.
    doi: 10.1038/d41586-020-02884-3google scholar: lookup
  4. American Veterinary Medical Association. [(accessed on 13 June 2021)]. Available online: https://www.avma.org/Policies/Pages/Judicious-Therapeutic-Use-of-Antimicrobials.aspx.
  5. Wright G.D.. Antibiotic resistance in the environment: A link to the clinic?. Curr. Opin. Microbiol. 2010;13:589–594.
    doi: 10.1016/j.mib.2010.08.005pubmed: 20850375google scholar: lookup
  6. Johansson A., Greko C., Engström B.E., Karlsson M.. Antimicrobial susceptibility of Swedish, Norwegian and Danish isolates of Clostridium perfringens from poultry, and distribution of tetracycline resistance genes.. Vet. Microbiol. 2004;99:251–257.
    doi: 10.1016/j.vetmic.2004.01.009pubmed: 15066727google scholar: lookup
  7. Divala T.H., Corbett E.L., Stagg H.R., Nliwasa M., Sloan D.J., French N., Fielding K.L.. Effect of the duration of antimicrobial exposure on the development of antimicrobial resistance (AMR) for macrolide antibiotics: Protocol for a systematic review with a network meta-analysis.. Sys. Rev. 2018;7:246.
    doi: 10.1186/s13643-018-0917-0pmc: PMC6304229pubmed: 30580758google scholar: lookup
  8. Martinez J.L., Rojo F.. Metabolic regulation of antibiotic resistance.. FEMS Microbiol. Rev. 2011;35:768–789.
    doi: 10.1111/j.1574-6976.2011.00282.xpubmed: 21645016google scholar: lookup
  9. Martínez J.L.. Bottlenecks in the Transferability of Antibiotic Resistance from Natural Ecosystems to Human Bacterial Pathogens.. Front. Microbiol. 2012;2:256.
    doi: 10.3389/fmicb.2011.00265pmc: PMC3249888pubmed: 22319513google scholar: lookup
  10. Davies J., Webb V.. Antibiotic resistance in bacteria.. Biomedical Research Reports: Emerging Infections 1998. pp. 239–273.
  11. Palmer K.L., Kos V.N., Gilmore M.S.. Horizontal Gene Transfer and the Genomics of Enterococcal Antibiotic Resistance.. Curr. Opin. Microbiol. 2010;13:632–639.
    doi: 10.1016/j.mib.2010.08.004pmc: PMC2955785pubmed: 20837397google scholar: lookup
  12. Bello-López J.M., Cabrero-Martínez O.A., Ibáñez-Cervantes G., Hernández-Cortez C., Pelcastre-Rodríguez L.I., Luis U., Gonzalez-Avila L.U., Castro-Escarpulli G.. Horizontal Gene Transfer and Its Association with Antibiotic Resistance in the Genus Aeromonas spp.. Microorganisms 2019;7:363.
    doi: 10.3390/microorganisms7090363pmc: PMC6780555pubmed: 31540466google scholar: lookup
  13. Sørum H., L’Abée-Lund T.M.. Antibiotic resistance in food-related bacteria—A result of interfering with the global web of bacterial genetics.. Int. J. Food Microbiol. 2002;78:43–56.
    doi: 10.1016/S0168-1605(02)00241-6pubmed: 12222637google scholar: lookup
  14. Andersson D.I., Levin B.R.. The biological cost of antibiotic resistance.. Curr. Opin. Microbiol. 1999;2:489–493.
    doi: 10.1016/S1369-5274(99)00005-3pubmed: 10508723google scholar: lookup
  15. Martínez J.L., Coque T.M., Baquero F.. What is a resistance gene? Ranking risk in resistomes.. Nat. Rev. Microbiol. 2015;13:116–123.
    doi: 10.1038/nrmicro3399pubmed: 25534811google scholar: lookup
  16. Magiorakos A.P., Srinivasan A., Carey R.B., Carmeli Y., Falagas M.E., Giske C.G., Harbarth S., Hindler J.F., Kahlmeter G., Olsson-Liljequist B.. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance.. Clin. Microbiol. Infect. 2012;18:268–281.
    doi: 10.1111/j.1469-0691.2011.03570.xpubmed: 21793988google scholar: lookup
  17. Singh B.R.. Occurrence of multiple drug Resistant (MDR) Aerobic Bacteria in Vaginal Swabs of Mares and Their Association with Infertility.. Indian J. Comp. Micobiol. Immunol. Infect. Dis. 2009;30:105–112.
  18. Kenney R.M., Bergman R.V., Cooper W.L., Morse G.W.. Minimal contamination techniques for breeding mares: Techniques and preliminary findings. Proceedings of the 21st Annual Convention of the American Association of Equine Practitioners Boston, MA, USA. 1–3 December 1975; pp. 327–335.
  19. Albihn A., Baverud V., Magnusson U.. Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems.. Acta Vet. Scand. 2003;44:121–129.
    doi: 10.1186/1751-0147-44-121pmc: PMC1831563pubmed: 15074625google scholar: lookup
  20. Rota A., Calicchio E., Nardoni S., Fratini F., Ebani V.V., Sgorbini M., Panzani D., Camillo F., Mancianti F.. Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions.. Theriogenology 2011;76:464–470.
    doi: 10.1016/j.theriogenology.2011.02.023pubmed: 21529914google scholar: lookup
  21. European Council Directive 92/65/EEC. 1992. [(accessed on 21 October 2021)]. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A01992L0065-20190716&qid=1634831824015.
  22. Klug E.. Routine AI application in the Hannoverian Sport Horse Breeding Association.. Anim. Reprod. Sci. 1992;28:39–44.
    doi: 10.1016/0378-4320(92)90089-Vgoogle scholar: lookup
  23. Holyoak G., Lyman C.C.. The Equine Endometrial Microbiome: A Brief Review.. Am. J. Biomed. Sci. Res. 2021;11:532–534.
    doi: 10.34297/AJBSR.2021.11.001689google scholar: lookup
  24. Al-Kass Z., Guo Y., Vinnere Pettersson O., Niazi A., Morrell J.M.. Metagenomic analysis of bacteria in stallion semen.. Anim. Reprod. Sci. 2020;221:106568.
    doi: 10.1016/j.anireprosci.2020.106568pubmed: 32861118google scholar: lookup
  25. Leblanc M.M., Causey R.C.. Clinical and Subclinical Endometritis in the Mare: Both Threats to Fertility.. Reprod. Domest. Anim. 2009;44((Suppl. S3)):10–22.
    doi: 10.1111/j.1439-0531.2009.01485.xpubmed: 19660076google scholar: lookup
  26. Davis H.A., Stanton M.B., Thungrat K., Boothe D.M.. Uterine bacterial isolates from mares and their resistance to antimicrobials: 8,296 cases (2003–2008). J. Am. Vet. Med. Assoc. 2013;242:977–983.
    doi: 10.2460/javma.242.7.977pubmed: 23517211google scholar: lookup
  27. Cerny K.L., Little T.V., Scoggin C.F., Coleman R.J., Troedsson M.H.T.. Presence of Bacteria on the External Genitalia of Healthy Stallions and its Transmission to the Mare at the Time of Breeding by Live Cover.. J. Eq. Vet. Sci. 2014;34:369–374.
    doi: 10.1016/j.jevs.2013.07.008google scholar: lookup
  28. Christoffersen M., Troedsson M.. Inflammation and fertility in the mare.. Reprod. Domest. Anim. 2017;52((Suppl. S3)):14–20.
    doi: 10.1111/rda.13013pubmed: 28815848google scholar: lookup
  29. Blanchard T.L., Kenny R.M., Timony P.J.. Venereal disease.. Vet. Clin. North. Amer. Eq. Pract. 1992;8:191–203.
    doi: 10.1016/S0749-0739(17)30475-3pubmed: 1315616google scholar: lookup
  30. Parlevliet J.M., Samper J.C.. Equine Breeding Management and Artificial Insemination. Disease transmission through semen. W.B. Saunders Co. Philadelphia, PA, USA: 2000; pp. 133–140.
  31. Samper J.C., Tibary A.. Disease transmission in horses.. Theriogenology 2006;66:551–559.
    doi: 10.1016/j.theriogenology.2006.04.019pubmed: 16837034google scholar: lookup
  32. Heitmann J., Kirchhoff H., Petzoldt K., Sonnenschein B.. Isolation of acholeplasmas and mycoplasmas from aborted horse fetuses.. Vet. Rec. 1979;104:350.
    doi: 10.1136/vr.104.15.350-apubmed: 473533google scholar: lookup
  33. Kirchhoff H., Heitmann J., Bisping W.. Mycoplasmas isolated from the genital tract of mares.. Zbl. Bakt. Mikrobiol. Hyg. 1980;246:228–235.
    pubmed: 6999784
  34. Pasolini M., Prete C., Del Fabbri S., Auletta L.. Bacterial endometritis that is refractory to traditional antimicrobial treatment is a significant challenge in the equine breeding industry.. Genital Infections and Infertility 2016. Chapter 15.
  35. Morris L., McCue P.M., Aurich C.. Equine endometritis: A review of challenges and new approaches.. Reproduction 2020;160:R95–R110.
    doi: 10.1530/REP-19-0478pubmed: 32805710google scholar: lookup
  36. Witte T.S., Bergwerff A.A., Scherpenisse P., Drillich M., Heuwieser W.. Ceftiofur derivates in serum and endometrial tissue after intramuscular administration in healthy mares.. Theriogenology 2010;74:466–472.
    doi: 10.1016/j.theriogenology.2010.02.030pubmed: 20494421google scholar: lookup
  37. Davolli G.M., Beavers K.N., Medina V., Sones J., Pinto C.R., Paccamonti D.L., Causey R.C.. Concentrations of sulfadiazine and trimethoprim in blood and endometrium of mares after administration of an oral suspension.. J. Equine Vet. Sci. 2018;67:27–30.
    doi: 10.1016/j.jevs.2018.02.022google scholar: lookup
  38. González C., Moreno L., Fumuso E., García J., Rivulgo M., Confalonieri A., Sparo M., Sánchez Bruni S.. Enrofloxacin-based therapeutic strategy for the prevention of endometritis in susceptible mares.. J. Vet. Pharmacol. Ther. 2010;33:287–294.
    doi: 10.1111/j.1365-2885.2009.01135.xpubmed: 20557446google scholar: lookup
  39. Rodriguez J.S., Han S., Nielsen S., Pearson L.K., Gay J.M., Tibary A.. Consequences of intrauterine enrofloxacin infusion on mare endometrium.. J. Equine Vet. Sci. 2012;32:106–111.
    doi: 10.1016/j.jevs.2011.08.003google scholar: lookup
  40. Trundell D.A., Ferris R.A., Hennet M.R., Wittenburg L.A., Gustafson D.L., Borlee B.R., McCue P.M.. Pharmacokinetics of Intrauterine Ciprofloxacin in the Mare and Establishment of Minimum Inhibitory Concentrations for Equine Uterine Bacterial Isolates.. J. Equine Vet. Sci. 2017;54:54–59.
    doi: 10.1016/j.jevs.2016.12.013google scholar: lookup
  41. Boyd B.E., Allen W.E.. Absorption of neomycin from the equine uterus: Effect of bacterial and chemical endometritis.. Vet. Rec. 1988;122:37–39.
    doi: 10.1136/vr.122.2.37pubmed: 3284159google scholar: lookup
  42. Jeremejeva J., Orro T., Waldmann A., Arend A., Kask K.. Treatment of dairy cows with PGF2α or NSAID, in combination with antibiotics, in cases of postpartum uterine inflammation.. Acta Vet. Scand. 2012;54:45–53.
    doi: 10.1186/1751-0147-54-45pmc: PMC3502358pubmed: 22883439google scholar: lookup
  43. Mileva R., Karadaev M., Fasulkov I., Petkova T., Rusenova N., Vasilev N., Milanova A.. Oxytetracycline Pharmacokinetics After Intramuscular Administration in Cows with Clinical Metritis Associated with Trueperella Pyogenes Infection.. Antibiotics 2020;9:392.
    doi: 10.3390/antibiotics9070392pmc: PMC7400317pubmed: 32659893google scholar: lookup
  44. Pisello L., Rampacci E., Stefanetti V., Beccati F., Hyatt D.R., Passamonti F.. Temporal efficacy of antimicrobials against aerobic bacteria isolated from equine endometritis: An Italian retrospective analysis (2010–2017). Vet. Rec. 2019;185:105413.
    doi: 10.1136/vr.105413pubmed: 31409748google scholar: lookup
  45. Dabernat H.J., Delmas C.F., Tainturier D.J., Lareng M.B.. In vitro susceptibility of Haemophilus equigenitalis, the causative organism of contagious equine metritis 1977, to antimicrobial agents.. Antimicrob. Agents Chemother. 1980;18:841–843.
    doi: 10.1128/AAC.18.6.841pmc: PMC352975pubmed: 7195184google scholar: lookup
  46. Berwal S.S., Bugalia N.S., Kapoor P.K., Garg D.N., Monga D.P., Batra M.. Cytological and microbiological evaluation of uterine flush of fertile and repeat breeder mares and post-treatment fertility.. Haryana Vet. 2006;45:15–17.
  47. Frontoso R., De Carlo E., Pasolini M.P., 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;84:1–6.
    doi: 10.1016/j.rvsc.2007.02.008pubmed: 17434193google scholar: lookup
  48. Goncagül G., Seyrek-İntas K.. Antimicrobial Susceptibility of Bacteria Isolated from Uteri of Thoroughbred Mares with Fertility Problems.. Kafkas Univ. Vet. Fak. Derg. 2013;19:A105–A109.
    doi: 10.9775/kvfd.2012.8094google scholar: lookup
  49. Benko T., Boldizar M., Novotny F., Hura V., Valocki I., Dudrikova K., Karamanova M., Petrovic V.. Incidence of bacterial pathogens in equine uterine swabs, their antibiotic resistance patterns, and selected reproductive indices in English thoroughbred mares during the foal heat cycle.. Veterinární Med. 2015;60:613–620.
    doi: 10.17221/8529-VETMEDgoogle scholar: lookup
  50. Goncagul G., Gocmen H., Yendim S.K., Yilmaz K., Intas K.S.. Bacteriologic and cytologic examination results of mares with pneumovagina in bursa region.. Inter. J. Vet. Sci. 2016;5:295–298.
  51. Nocera F.P., Papulino C., Del Prete C., Palumbo V., Pasolini M.P., De Martino L.. Endometritis associated with Enterococcus casseliflavus in a mare: A case report.. Asian Pac. J. Trop. Biomed. 2017;7:760–762.
    doi: 10.1016/j.apjtb.2017.07.016google scholar: lookup
  52. Ferrer M.S., Palomares R.. Aerobic uterine isolates and antimicrobial susceptibility in mares with post-partum metritis.. Equine Vet. J. 2018;50:202–207.
    doi: 10.1111/evj.12738pubmed: 28796905google scholar: lookup
  53. Balamurugan K., Subapriya S., Dinesh N.M., Partheban P.. Antibiotic sensitivity test on pathogens causing reproductive tract infection in thoroughbred mares.. J. Entomol. Zool. Stud. 2020;8:913–915.
  54. Picket B.W., Voss J.L., Jones R.L.. Control of bacteria in stallions and their semen.. J. Equine vet. Sci. 1999;19:424–441.
    doi: 10.1016/S0737-0806(99)80254-8google scholar: lookup
  55. Clement F., Vidament M., Guerin B.. Microbial contamination of stallion semen.. Biol. Reprod. 1995;1:779–786.
    doi: 10.1093/biolreprod/52.monograph_series1.779google scholar: lookup
  56. Neto C.R., da Silva Y.F.R.S., Resende H.L., Guasti P.N., Monteiro G.A., Papa P.M., Dell’aqua Júnior J.A., Filho J.N.P.P., Alvarena M.A., Papa F.O.. Control Methods and Evaluation of Bacterial Growth on Fresh and Cooled Stallion Semen.. J. Equine Vet. Sci. 2015;35:277–282.
    doi: 10.1016/j.jevs.2015.01.014google scholar: lookup
  57. Pasing S., Aurich C., von Lewinski M., Wulf M., Kruger M., Aurich J.E.. Development of the genital microflora in stallions used for artificial insemination throughout the breeding season.. Anim. Reprod. Sci. 2013;139:53–61.
    doi: 10.1016/j.anireprosci.2013.03.009pubmed: 23602488google scholar: lookup
  58. Aurich J., Aurich C.. Developments in European horse breeding and consequences for veterinarians in equine reproduction.. Reprod. Domest. Anim. 2006;41:275–279.
    doi: 10.1111/j.1439-0531.2006.00719.xpubmed: 16869881google scholar: lookup
  59. Bennett D.G.. Therapy of Endometritis in Mares.. J. Am. Vet. Med. Assoc. 1986;188:1390–1392.
    pubmed: 3528094
  60. Ortega-Ferrusola C., González-Fernández L., Muriel A., Macías-García B., Rodríguez-Martínez H., Tapia J.A., Peña F.J.. Does the microbial flora in the ejaculate affect the freezeability of stallion sperm?. Reprod. Domest. Anim. 2009;44:518–522.
    doi: 10.1111/j.1439-0531.2008.01267.xpubmed: 19655428google scholar: lookup
  61. Yaniz J.L., Marco-Aguado M.A., Mateos J.A., Santolaria P.. Bacterial contamination of ram semen, antibiotic sensitivities, and effects on sperm quality during storage at 15 degrees C.. Anim. Reprod. Sci. 2010;122:142–149.
    doi: 10.1016/j.anireprosci.2010.08.006pubmed: 20832206google scholar: lookup
  62. Onemu S.O., Ibeh I.N.. Studies on the significance of positive bacterial semen cultures in male infertility in Nigeria.. Int. J. Fertil. Womens Med. 2001;46:210–214.
    pubmed: 11563831
  63. Hernández-Avilés C., Serafini R., Love C.C., Teague S.R., LaCaze K.A., Lawhon S.D., Wu J., Blanchard T.L., Varner D.D.. The effects of antibiotic type and extender storage method on sperm quality and antibacterial effectiveness in fresh and cooled-stored stallion semen.. Theriogenology 2018;122:23–29.
    doi: 10.1016/j.theriogenology.2018.08.022pubmed: 30219312google scholar: lookup
  64. Santos C.S., Silva A.R.. Current and alternative trends in antibacterial agents used in mammalian semen technology.. Anim. Reprod. 2020;17:e20190111.
    doi: 10.21451/1984-3143-AR2019-0111pmc: PMC7212743pubmed: 32399069google scholar: lookup
  65. Varner D.D., Scanlan C.M., Thompson J.A., Brumbaugh G.W., Blanchard T.L., Carlton C.M., Johnson L.. Bacteriology of preserved stallion semen and antibiotics in semen extenders.. Theriogenology 1998;50:559–573.
    doi: 10.1016/S0093-691X(98)00161-7pubmed: 10732147google scholar: lookup
  66. Aurich C., Spergser J.. Influence of bacteria and gentamicin on cooled-stored stallion spermatozoa.. Theriogenology 2007;67:912–918.
    doi: 10.1016/j.theriogenology.2006.11.004pubmed: 17141306google scholar: lookup
  67. Al-Kass Z., Spergser J., Aurich C., Kuhl J., Schmidt K., Morrell J.M.. Effect of presence or absence of antibiotics and use of modified single layer centrifugation on bacteria in pony stallion semen.. Reprod. Domest. Anim. 2018;54:342–349.
    doi: 10.1111/rda.13366pubmed: 30351456google scholar: lookup
  68. Hernández-Avilés C., Love C.C., Serafini R., Ramírez-Agámez L., Kelley D.E., de Andino E.M., Teague S.R., LaCaze K.A., Brinsko S.P., Varner D.D.. Inclusion of supplemental antibiotics (amikacin—penicillin) in a commercial extender for stallion semen: Effects on sperm quality, bacterial growth, and fertility following cooled storage.. Theriogenology 2020;158:209–217.
    doi: 10.1016/j.theriogenology.2020.09.018pubmed: 32971438google scholar: lookup
  69. Malaluang P., Wilén E., Hansson I., Lindahl J., Morrell J.M.. Antibiotic resistance in vaginal flora of inseminated mares.. 2021. in press.
    pmc: PMC10058017pubmed: 36986297
  70. Anwar M., Iqbal Q., Saleem F.. Improper disposal of unused antibiotics: An often overlooked driver of antimicrobial resistance.. Expert Rev. Antibiot. Ther. 2020;18:697–699.
    doi: 10.1080/14787210.2020.1754797pubmed: 32281427google scholar: lookup
  71. Vickram A.S., Kuldeep D., Archana K., Parameswari R., Ramesh Pathy M., Iqbal H.M.N., Sridharan T.B.. Antimicrobial peptides in semen extenders: A valuable replacement option for antibiotics in cryopreservation—a prospective review.. J. Exp. Biol. Agric. Sci. 2017;5:578–588.
  72. Hall-Stoodley L., Stoodley P., Kathju S., Hoiby N., Moser C., Costerton W.J., Bjarnsholt T.. Towards diagnostic guidelines for biofilm-associated infections.. FEMS Immunol. Medic. Microbiol. 2012;65:127–145.
    doi: 10.1111/j.1574-695X.2012.00968.xpubmed: 22469292google scholar: lookup
  73. Coelho M.L., Duarte A.F.S., Bastos M.C.F.. Bacterial labionin-containing peptides and sactibiotics: Unusual types of antimicrobial peptides with potential use in clinical settings (a review). Curr. Top. Med. Chem. 2017;17:1–22.
    pubmed: 27697045
  74. Bourgeon F., Evrard B., Brillard-Bourdet M., Colleu D., Jegou B., Pineau C.. Involvement of semenogelin-derived peptides in the antibacterial activity of human seminal plasma.. Biol. Reprod. 2004;70:768–774.
    doi: 10.1095/biolreprod.103.022533pubmed: 14613901google scholar: lookup
  75. Hirt H., Gorr S.U.. Antimicrobial peptide GL13K is effective in reducing biofilms of Pseudomonas aeruginosa.. Antimicrob. Agents Chemother. 2013;57:4903–4910.
    doi: 10.1128/AAC.00311-13pmc: PMC3811403pubmed: 23917321google scholar: lookup
  76. Schulze M., Junkes C., Müller P., Speck S., Rüdiger K., Dathe M., Müller K.. Effects of cationic antimicrobial peptides on liquid-preserved boar spermatozoa.. PLoS ONE 2014;9:e100490.
    doi: 10.1371/journal.pone.0100490pmc: PMC4062521pubmed: 24940997google scholar: lookup
  77. Schulze M., Dathe M., Waberski D., Müller K.. Liquid storage of boar semen: Current and future perspectives on the use of cationic antimicrobial peptides to replace antibiotics in semen extenders.. Theriogenology 2016;85:39–46.
    doi: 10.1016/j.theriogenology.2015.07.016pubmed: 26264695google scholar: lookup
  78. Tsakmakidis I.A., Samaras T., Anastasiadou S., Basioura A., Ntemka A., Michos I., Simeonidis K., Karagiannis I., Tsousis G., Angelakeris M.. Iron Oxide Nanoparticles as an Alternative to Antibiotics Additive on Extended Boar Semen.. Nanomaterials 2020;10:1568.
    doi: 10.3390/nano10081568pmc: PMC7466471pubmed: 32784995google scholar: lookup
  79. Barone F., Ventrella D., Zannoni A., Forni M., Bacci M.L.. Can microfiltered seminal plasma preserve the morphofunctional characteristics of porcine spermatozoa in the absence of antibiotics? A preliminary study.. Reprod. Domest. Anim. 2016;51:604–610.
    doi: 10.1111/rda.12699pubmed: 27174664google scholar: lookup
  80. Morrell J.M., Klein C., Lundeheim N., Erol E., Troedsson M.H.T.. Removal of bacteria from stallion semen by colloid centrifugation.. Anim. Reprod. Sci. 2014;145:47–53.
    doi: 10.1016/j.anireprosci.2014.01.005pubmed: 24485764google scholar: lookup
  81. Morrell J.M., Nunes M.M.. Practical guide to Single Layer Centrifugation of stallion semen.. Equine Vet. Educ. 2018;30:392–398.
    doi: 10.1111/eve.12658google scholar: lookup
  82. Morrell J.M., Nunez-Gonzalez A., Crespo-Felez I., Martinez-Martinez S., Martinez Alborcia M.J., Fernandez-Alegre E., Dominguez J.C., Gutierrez-Martin C.B., Martinez-Pastor F.. Removal of bacteria from boar semen using a low-density colloid.. Theriogenology 2019;126:272–278.
    doi: 10.1016/j.theriogenology.2018.12.028pubmed: 30594102google scholar: lookup

Citations

This article has been cited 16 times.
  1. Alfatlawy HJ. Microbial profile of post-breeding endometritis in Arabian mares from the Al-Hira District, Iraq. Open Vet J 2025;15(8):3670-3676.
    doi: 10.5455/OVJ.2025.v15.i8.30pubmed: 41035988google scholar: lookup
  2. Ullah A, Chen W, Shi L, Wang M, Geng M, Na J, Akhtar MF, Khan MZ, Wang C. Challenges and Enhancing Strategies of Equine Semen Preservation: Nutritional and Genetic Perspectives. Vet Sci 2025 Aug 25;12(9).
    doi: 10.3390/vetsci12090807pubmed: 41012733google scholar: lookup
  3. Zabala SM, Serres C, Montero N, Crespo F, Lorenzo PL, Pérez-Aguilera V, Oliet A, Hijón V, Moreno S, González-Zorn B, Gutiérrez-Cepeda L. Innovative Approaches to Avoid Antibiotic Use in Equine Semen Cryopreservation: Advancing Sustainable Reproductive Technologies. Animals (Basel) 2025 May 9;15(10).
    doi: 10.3390/ani15101368pubmed: 40427246google scholar: lookup
  4. Carvalho IB, Branco S, Laranjo M, Queiroga MC, Bettencourt E. Characteristics of the Mare-Uterine-Culture-Based Bacterial Composition Using Practical Clinical Evaluation Methods. Pathogens 2025 Apr 7;14(4).
    doi: 10.3390/pathogens14040357pubmed: 40333165google scholar: lookup
  5. Cutarelli A, Passantino G, Razzuoli E, Serpe F, Leonardi L, Zizzo N, Roperto S. Digital droplet PCR-based detection and quantification of ovine papillomavirus DNA from the vaginal virobiota of healthy mares. Sci Rep 2025 Mar 22;15(1):9951.
    doi: 10.1038/s41598-025-94279-5pubmed: 40121289google scholar: lookup
  6. Hardefeldt LY, Thomas K, Begg L. Antimicrobial use and prescribing practices by equine veterinarians in Australia: Insights into reproduction, dentistry, compounding and use for nonbactericidal effects. Aust Vet J 2025 Jun;103(6):307-313.
    doi: 10.1111/avj.13428pubmed: 40000246google scholar: lookup
  7. Mazzuchini MP, Lisboa FP, de Castro JI, Alvarenga MA, Segabinazzi LGTM, Canisso IF. In vitro antimicrobial activity of non-traditional therapies for infectious endometritis in mares. Equine Vet J 2025 Jul;57(4):1118-1126.
    doi: 10.1111/evj.14423pubmed: 39431554google scholar: lookup
  8. Kabir A, Lamichhane B, Habib T, Adams A, El-Sheikh Ali H, Slovis NM, Troedsson MHT, Helmy YA. Antimicrobial Resistance in Equines: A Growing Threat to Horse Health and Beyond-A Comprehensive Review. Antibiotics (Basel) 2024 Jul 29;13(8).
    doi: 10.3390/antibiotics13080713pubmed: 39200013google scholar: lookup
  9. Mouncey R, Arango-Sabogal JC, Rathbone P, Scott CJ, de Mestre AM. Prevalence of Microbial Isolates Cultured from Endometrial Swab Samples Collected from United Kingdom Thoroughbred Mares from 2014 to 2020. Vet Sci 2024 Feb 9;11(2).
    doi: 10.3390/vetsci11020082pubmed: 38393100google scholar: lookup
  10. Gravey F, Sévin C, Castagnet S, Foucher N, Maillard K, Tapprest J, Léon A, Langlois B, Le Hello S, Petry S. Antimicrobial resistance and genetic diversity of Klebsiella pneumoniae strains from different clinical sources in horses. Front Microbiol 2023;14:1334555.
    doi: 10.3389/fmicb.2023.1334555pubmed: 38274763google scholar: lookup
  11. Zabala SM, Serres C, Montero N, Crespo F, Lorenzo PL, Pérez-Aguilera V, Galán C, Domínguez-Gimbernat M, Oliet A, Moreno S, González-Zorn B, Gutiérrez-Cepeda L. Strategies to Reduce the Use of Antibiotics in Fresh and Chilled Equine Semen. Animals (Basel) 2024 Jan 5;14(2).
    doi: 10.3390/ani14020179pubmed: 38254348google scholar: lookup
  12. Thomson P, García P, Río CD, Castro R, Núñez A, Miranda C. Antimicrobial Resistance and Extended-Spectrum Beta-Lactamase Genes in Enterobacterales, Pseudomonas and Acinetobacter Isolates from the Uterus of Healthy Mares. Pathogens 2023 Sep 8;12(9).
    doi: 10.3390/pathogens12091145pubmed: 37764953google scholar: lookup
  13. 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
  14. Malaluang P, Wilén E, Frosth S, Lindahl JF, Hansson I, Morrell JM. Antimicrobial Resistance in Vaginal Bacteria in Inseminated Mares. Pathogens 2023 Feb 24;12(3).
    doi: 10.3390/pathogens12030375pubmed: 36986297google scholar: lookup
  15. Thomson P, Pareja J, Núñez A, Santibáñez R, Castro R. Characterization of microbial communities and predicted metabolic pathways in the uterus of healthy mares. Open Vet J 2022 Nov-Dec;12(6):797-805.
    doi: 10.5455/OVJ.2022.v12.i6.3pubmed: 36650865google scholar: lookup
  16. Malaluang P, Wilén E, Frosth S, Lindahl J, Hansson I, Morrell JM. Vaginal Bacteria in Mares and the Occurrence of Antimicrobial Resistance. Microorganisms 2022 Nov 8;10(11).
    doi: 10.3390/microorganisms10112204pubmed: 36363796google scholar: lookup
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