Analyze Diet
Veterinary sciences2022; 9(2); 67; doi: 10.3390/vetsci9020067

Antimicrobial Susceptibility of Bacterial Isolates from Donkey Uterine Infections, 2018-2021.

Abstract: Endometritis is a common reproductive disease in equine animals. No investigation about the bacterial characteristics and antimicrobial susceptibility pattern of donkeys with endometritis has thus far been reported. Objective: To determine the common uterine bacterial isolates from donkeys with endometritis and to evaluate their susceptibility to antimicrobials used for the treatment thereof. Methods: Retrospective case-series. Methods: Medical records at an equine clinical diagnostic center were retrospectively reviewed to identify submissions from donkeys with bacterial endometritis between 2018 and 2021. Data were extracted and analyzed descriptively in terms of the frequency of bacterial species, susceptibility to antimicrobials and multidrug resistance. Results: A total of 73 isolates were identified from 30 donkeys, of which 92% of the isolates were Gram-negative bacteria. Mixed cultures were found in 90% of the donkeys. The most common isolates were (31.5%) and spp. (21.9%). Susceptibility testing revealed that amikacin (98%), cefoxitin (95%), trimethoprim-sulfamethoxazole (78%) and gentamicin (74%) were the most efficient agents for donkeys. Multidrug resistance (MDR) was found in 20% of all bacterial isolates, of which all isolates showed a multidrug resistance profile. Main limitations: The sample size was relatively small, which means a bias of selection may exist. The antimicrobial resistance and MDR of agents without break points were not calculated, which means the relative results may be underestimated in our study. Conclusions: Severe infections were detected in donkeys with endometritis. Antimicrobial resistance and MDR bacteria are not rare in our study. This study demonstrated that bacteria identification and antimicrobial susceptibility testing are highly recommended before the treatment of uterine infections in donkeys. Further studies, including the epidemiological investigation of bacterial endometritis of donkeys, should be conducted to provide a better understanding of this critical problem.
Publication Date: 2022-02-05 PubMed ID: 35202320PubMed Central: PMC8875120DOI: 10.3390/vetsci9020067Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • 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.

The research paper examines the types of bacteria common in donkey uterine infections and their resistance to various antimicrobials. The study showed that antimicrobial resistance and multi-drug resistance bacteria are prevalent in donkey uterine bacteria and recommended further tests before treatment.

Study Objective and Methodology

  • The primary objective was to identify prevalent bacterial species causing endometritis, a common reproductive disease, in donkeys and assess their resistance to commonly used antibiotics.
  • The study adopted a retrospective case-series methodology where medical records from an equine clinical diagnostic center were curated to note submissions related to endometritis in donkeys from 2018-2021.
  • The data compiled included the frequency of various bacterial species, their resistance to antimicrobial medications, and instances of multidrug resistance.

Findings of the Study

  • The analysis identified 73 bacterial isolates sourced from 30 donkeys. An overwhelmingly large proportion, about 92%, of these isolates were Gram-negative bacteria.
  • Mixed cultures were present in around 90% of the affected donkeys. The most commonly isolated bacteria were Escherichia coli (31.5%) and Klebsiella spp. (21.9%).
  • The study found that amongst antibiotics, amikacin (98% efficacy), cefoxitin (95% efficacy), trimethoprim-sulfamethoxazole (78% efficacy), and gentamicin (74% efficacy) were the most beneficial in treating these infections.
  • Insights revealed that 20% of all bacterial isolates showcased multidrug resistance, including all the Escherichia coli isolates.

Study Limitations and Implications

  • The limited sample size was a significant limitation, raising the possibility of selection bias. Additionally, the study did not calculate the resistance and multidrug resistance of agents without break points, potentially underestimating the relative results.
  • The study found substantial prevalence of severe infections, antimicrobial resistance, and multidrug-resistant bacteria in donkeys suffering from endometritis. This highlights the importance of bacterial identification and antimicrobial susceptibility testing before treatment commencement.

Recommendations for Future Research

  • The researchers suggested that more comprehensive studies, including the epidemiological investigation of bacterial endometritis in donkeys, should be conducted. This would help broaden the understanding of this prominent issue and possibly assist in effective treatment and prevention strategies.

Cite This Article

APA
Zhao Y, Zhu Y, Liu B, Mi J, Li N, Zhao W, Wu R, Holyoak GR, Li J, Liu D, Zeng S, Wang Y. (2022). Antimicrobial Susceptibility of Bacterial Isolates from Donkey Uterine Infections, 2018-2021. Vet Sci, 9(2), 67. https://doi.org/10.3390/vetsci9020067

Publication

ISSN: 2306-7381
NlmUniqueID: 101680127
Country: Switzerland
Language: English
Volume: 9
Issue: 2
PII: 67

Researcher Affiliations

Zhao, Yufei
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Zhu, Yiping
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Liu, Bo
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Mi, Junpeng
  • School of Veterinary Science, University of Sydney, Sydney, NSW 2000, Australia.
Li, Nan
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Zhao, Weisen
  • College of Animal Science and Technology, China Agriculture University, Beijing 100193, China.
Wu, Rongzheng
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Holyoak, Gilbert Reed
  • College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078, USA.
Li, Jing
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Liu, Dejun
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.
Zeng, Shenming
  • College of Animal Science and Technology, China Agriculture University, Beijing 100193, China.
Wang, Yang
  • College of Veterinary Medicine, China Agriculture University, Beijing 100193, China.

Grant Funding

  • 81991531 / National Natural Science Foundation of China

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 53 references
  1. Beja-Pereira A, England PR, Ferrand N, Jordan S, Bakhiet AO, Abdalla MA, Mashkour M, Jordana J, Taberlet P, Luikart G. African origins of the domestic donkey.. Science 2004 Jun 18;304(5678):1781.
    doi: 10.1126/science.1096008pubmed: 15205528google scholar: lookup
  2. Canisso IF, Panzani D, Miró J, Ellerbrock RE. Key Aspects of Donkey and Mule Reproduction.. Vet Clin North Am Equine Pract 2019 Dec;35(3):607-642.
    doi: 10.1016/j.cveq.2019.08.014pubmed: 31672204google scholar: lookup
  3. 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
  4. Troedsson MH, Woodward EM. Our current understanding of the pathophysiology of equine endometritis with an emphasis on breeding-induced endometritis.. Reprod Biol 2016 Mar;16(1):8-12.
    doi: 10.1016/j.repbio.2016.01.003pubmed: 26952748google scholar: lookup
  5. Rasmusse CD, Petersen MR, Bojesen AM, Pedersen HG, Lehn-Jensen H, Christoffersen M. Equine infectious endometritis—Cinical and subclinical cases.. J. Equine Vet. Sci. 2015;35:95–104.
  6. Casagrande Proietti P, Bietta A, Coppola G, Felicetti M, Cook RF, Coletti M, Marenzoni ML, Passamonti F. Isolation and characterization of β-haemolytic-Streptococci from endometritis in mares.. Vet Microbiol 2011 Aug 26;152(1-2):126-30.
    doi: 10.1016/j.vetmic.2011.04.009pubmed: 21570219google scholar: lookup
  7. Causey RC. Making sense of equine uterine infections: the many faces of physical clearance.. Vet J 2006 Nov;172(3):405-21.
    doi: 10.1016/j.tvjl.2005.08.005pubmed: 16169264google scholar: lookup
  8. Benko T, Boldizar M, Novotny F, Hura V, Valocky 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.. Vet. Med. 2016;60:613–620.
    doi: 10.17221/8529-VETMEDgoogle scholar: lookup
  9. 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
  10. 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.
  11. Holyoak GR, Lyman CC. The equine endometrial microbiome: A brief review.. Am. J. Biomed. Sci. Res. 2021;11:532–534.
  12. Rock KS, Love BC, DeSilva U, Rezabek GB, Meijer WG, Carrington SD, Holyoak GR. Detectable differences in the endometrial microbiome between normal and susceptible mares using metagenomic profiling and conventional bacterial culture.. Clin. Theriogenol. 2011;3:376.
  13. Holyoak GR, Lyman CC, Wieneke X, DeSilva U. The equine endometrial microbiome.. Clin. Theriogenol. 2018;10:273–278.
  14. Causey RC. Uterine therapy for mares with bacterial infections. Elsevier; Amsterdam, The Netherlands: 2007. pp. 105–115.
  15. Troedsson MH. Breeding-induced endometritis in mares.. Vet Clin North Am Equine Pract 2006 Dec;22(3):705-12.
    doi: 10.1016/j.cveq.2006.07.003pubmed: 17129798google scholar: lookup
  16. Li J, Zhao Y, Gao Y, Zhu Y, Holyoak GR, Zeng S. Treatments for Endometritis in Mares Caused by Streptococcus equi Subspecies zooepidemicus: A Structured Literature Review.. J Equine Vet Sci 2021 Jul;102:103430.
    doi: 10.1016/j.jevs.2021.103430pubmed: 34119209google scholar: lookup
  17. Rogan D, Fumuso E, Rodríguez E, Wade J, Sánchez Bruni SF. Use of a mycobacterial cell wall extract (MCWE) in susceptible mares to clear experimentally induced endometritis with streptococcus zooepidemicus.. J. Equine Vet. Sci. 2007;27:112–117.
  18. Morley PS, Apley MD, Besser TE, Burney DP, Fedorka-Cray PJ, Papich MG, Traub-Dargatz JL, Weese JS. Antimicrobial drug use in veterinary medicine.. J Vet Intern Med 2005 Jul-Aug;19(4):617-29.
  19. 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
  20. Ricketts S. The barren mare: Diagnosis, prognosis, prophylaxis and treatment for genital abnormality.. Practice 1989;11:156–164.
    doi: 10.1136/inpract.11.4.156google scholar: lookup
  21. Davis HA, Stanton MB, Thungrat K, Boothe DM. Uterine bacterial isolates from mares and their resistance to antimicrobials: 8,296 cases (2003-2008).. J Am Vet Med Assoc 2013 Apr 1;242(7):977-83.
    doi: 10.2460/javma.242.7.977pubmed: 23517211google scholar: lookup
  22. Ferrer MS, Palomares R. Aerobic uterine isolates and antimicrobial susceptibility in mares with post-partum metritis.. Equine Vet J 2018 Mar;50(2):202-207.
    doi: 10.1111/evj.12738pubmed: 28796905google scholar: lookup
  23. Pisello L, Rampacci E, Stefanetti V, Beccati F, Hyatt DR, Coletti M, Passamonti F. Temporal efficacy of antimicrobials against aerobic bacteria isolated from equine endometritis: an Italian retrospective analysis (2010-2017).. Vet Rec 2019 Nov 16;185(19):598.
    doi: 10.1136/vr.105413pubmed: 31409748google scholar: lookup
  24. Díaz-Bertrana ML, Deleuze S, Pitti Rios L, Yeste M, Morales Fariña I, Rivera Del Alamo MM. Microbial Prevalence and Antimicrobial Sensitivity in Equine Endometritis in Field Conditions.. Animals (Basel) 2021 May 20;11(5).
    doi: 10.3390/ani11051476pmc: PMC8160901pubmed: 34065566google scholar: lookup
  25. Canisso IF, Segabinazzi LGTM, Fedorka CE. Persistent Breeding-Induced Endometritis in Mares - a Multifaceted Challenge: From Clinical Aspects to Immunopathogenesis and Pathobiology.. Int J Mol Sci 2020 Feb 20;21(4).
    doi: 10.3390/ijms21041432pmc: PMC7073041pubmed: 32093296google scholar: lookup
  26. 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
  27. CLSI. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals.. 4th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2013.
  28. CLSI. Performance Standards for Antimicrobial Susceptibility Testing.. 30th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2020.
  29. Patel R. MALDI-TOF MS for the diagnosis of infectious diseases.. Clin Chem 2015 Jan;61(1):100-11.
    doi: 10.1373/clinchem.2014.221770pubmed: 25278500google scholar: lookup
  30. Johnston GCA, Lumsden JM. Antimicrobial susceptibility of bacterial isolates from 33 thoroughbred horses with arytenoid chondropathy (2005-2019).. Vet Surg 2020 Oct;49(7):1283-1291.
    doi: 10.1111/vsu.13474pubmed: 32767594google scholar: lookup
  31. Leclercq R, Cantón R, Brown DF, Giske CG, Heisig P, MacGowan AP, Mouton JW, Nordmann P, Rodloff AC, Rossolini GM, Soussy CJ, Steinbakk M, Winstanley TG, Kahlmeter G. EUCAST expert rules in antimicrobial susceptibility testing.. Clin Microbiol Infect 2013 Feb;19(2):141-60.
  32. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.. Clin Microbiol Infect 2012 Mar;18(3):268-81.
  33. Høiby N, Bjarnsholt T, Moser C, Bassi GL, Coenye T, Donelli G, Hall-Stoodley L, Holá V, Imbert C, Kirketerp-Møller K, Lebeaux D, Oliver A, Ullmann AJ, Williams C. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014.. Clin Microbiol Infect 2015 May;21 Suppl 1:S1-25.
    doi: 10.1016/j.cmi.2014.10.024pubmed: 25596784google scholar: lookup
  34. Ferris RA, McCue PM, Borlee GI, Loncar KD, Hennet ML, Borlee BR. In Vitro Efficacy of Nonantibiotic Treatments on Biofilm Disruption of Gram-Negative Pathogens and an In Vivo Model of Infectious Endometritis Utilizing Isolates from the Equine Uterus.. J Clin Microbiol 2016 Mar;54(3):631-9.
    doi: 10.1128/JCM.02861-15pmc: PMC4768000pubmed: 26719448google scholar: lookup
  35. Ferris RA, McCue PM, Borlee GI, Glapa KE, Martin KH, Mangalea MR, Hennet ML, Wolfe LM, Broeckling CD, Borlee BR. Model of Chronic Equine Endometritis Involving a Pseudomonas aeruginosa Biofilm.. Infect Immun 2017 Dec;85(12).
    doi: 10.1128/IAI.00332-17pmc: PMC5695105pubmed: 28970274google scholar: lookup
  36. Maboni G, Seguel M, Lorton A, Sanchez S. Antimicrobial resistance patterns of Acinetobacter spp. of animal origin reveal high rate of multidrug resistance.. Vet Microbiol 2020 Jun;245:108702.
    doi: 10.1016/j.vetmic.2020.108702pubmed: 32456823google scholar: lookup
  37. Smet A, Cools P, Krizova L, Maixnerova M, Sedo O, Haesebrouck F, Kempf M, Nemec A, Vaneechoutte M. Acinetobacter gandensis sp. nov. isolated from horse and cattle.. Int J Syst Evol Microbiol 2014 Dec;64(Pt 12):4007-4015.
    doi: 10.1099/ijs.0.068791-0pubmed: 25225259google scholar: lookup
  38. Weese JS. Antimicrobial therapy for multidrug resistant pathogens.. Equine Vet. Educ. 2009;21:328–334.
    doi: 10.2746/095777308X334293google scholar: lookup
  39. Ebert MA, Riese RL. Infertility in the mare.. Iowa State Univ. Vet. 1986;48:4.
  40. Gao N, Du Y, Zheng X, Shu S, Suo J, Han M, Ma X, Huang R, Peng W, Fu C. Endometritis in donkeys associated with Streptococcus equi subspecies zooepidemicus infection.. Pak. Vet. J. 2020;40:537–539.
    doi: 10.29261/pakvetj/2020.081google scholar: lookup
  41. Carvalho S, Marinho C, Gonçalves A, Sousa M, Nóvoa M, Quaresma M, Igrejas G, Poeta P. Vaginal bacterial microbiota of an endangered donkey breed: A comparison between Miranda donkey breed (Equus asinus) jennies with and without reproductive problems.. J. Integr. OMICS. 2016;6:193.
  42. Christoffersen M, Söderlind M, Rí»ºlk SR, Pedersen HG, Allen J, Krekeler N. Risk factors associated with uterine fluid after breeding caused by Streptococcus zooepidemicus.. Theriogenology 2015 Nov;84(8):1283-90.
  43. Bourély C, Cazeau G, Jarrige N, Haenni M, Gay E, Leblond A. Antimicrobial resistance in bacteria isolated from diseased horses in France.. Equine Vet J 2020 Jan;52(1):112-119.
    doi: 10.1111/evj.13133pubmed: 31033041google scholar: lookup
  44. Schmiedel J, Falgenhauer L, Domann E, Bauerfeind R, Prenger-Berninghoff E, Imirzalioglu C, Chakraborty T. Multiresistant extended-spectrum β-lactamase-producing Enterobacteriaceae from humans, companion animals and horses in central Hesse, Germany.. BMC Microbiol 2014 Jul 12;14:187.
    doi: 10.1186/1471-2180-14-187pmc: PMC4105247pubmed: 25014994google scholar: lookup
  45. Robinson TP, Bu DP, Carrique-Mas J, Fèvre EM, Gilbert M, Grace D, Hay SI, Jiwakanon J, Kakkar M, Kariuki S, Laxminarayan R, Lubroth J, Magnusson U, Thi Ngoc P, Van Boeckel TP, Woolhouse ME. Antibiotic resistance: mitigation opportunities in livestock sector development.. Animal 2017 Jan;11(1):1-3.
    doi: 10.1017/S1751731116001828pubmed: 27549404google scholar: lookup
  46. Patel HB, Lusk KA, Cota JM. The Role of Cefepime in the Treatment of Extended-Spectrum Beta-Lactamase Infections.. J Pharm Pract 2019 Aug;32(4):458-463.
    doi: 10.1177/0897190017743134pubmed: 29166830google scholar: lookup
  47. Salmon-Rousseau A, Martins C, Blot M, Buisson M, Mahy S, Chavanet P, Piroth L. Comparative review of imipenem/cilastatin versus meropenem.. Med Mal Infect 2020 Jun;50(4):316-322.
    doi: 10.1016/j.medmal.2020.01.001pubmed: 32035719google scholar: lookup
  48. Guglick MA, MacAllister CG, Clarke CR, Pollet R, Hague C, Clarke JM. Pharmacokinetics of cefepime and comparison with those of ceftiofur in horses.. Am J Vet Res 1998 Apr;59(4):458-63.
    pubmed: 9563631
  49. Langston VC, Fontenot RL, Byers JA, Andrews CM, Mochal-King CA. Plasma and synovial fluid pharmacokinetics of a single intravenous dose of meropenem in adult horses.. J Vet Pharmacol Ther 2019 Sep;42(5):525-529.
    doi: 10.1111/jvp.12770pubmed: 31222751google scholar: lookup
  50. Petry S, Sévin C, Kozak S, Foucher N, Laugier C, Linster M, Breuil MF, Dupuis MC, Hans A, Duquesne F, Tapprest J. Relationship between rifampicin resistance and RpoB substitutions of Rhodococcus equi strains isolated in France.. J Glob Antimicrob Resist 2020 Dec;23:137-144.
    doi: 10.1016/j.jgar.2020.08.006pubmed: 32992034google scholar: lookup
  51. Goldstein BP. Resistance to rifampicin: a review.. J Antibiot (Tokyo) 2014 Sep;67(9):625-30.
    doi: 10.1038/ja.2014.107pubmed: 25118103google scholar: lookup
  52. Lin YW, Han ML, Zhao J, Zhu Y, Rao G, Forrest A, Song J, Kaye KS, Hertzog P, Purcell A, Creek D, Zhou QT, Velkov T, Li J. Synergistic Combination of Polymyxin B and Enrofloxacin Induced Metabolic Perturbations in Extensive Drug-Resistant Pseudomonas aeruginosa.. Front Pharmacol 2019;10:1146.
    doi: 10.3389/fphar.2019.01146pmc: PMC6785843pubmed: 31632279google scholar: lookup
  53. Johns IC, Adams EL. Trends in antimicrobial resistance in equine bacterial isolates: 1999-2012.. Vet Rec 2015 Mar 28;176(13):334.
    doi: 10.1136/vr.102708pubmed: 25628448google scholar: lookup

Citations

This article has been cited 1 times.
  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