Analyze Diet
Frontiers in microbiology2024; 14; 1334555; doi: 10.3389/fmicb.2023.1334555

Antimicrobial resistance and genetic diversity of Klebsiella pneumoniae strains from different clinical sources in horses.

Abstract: Klebsiella pneumoniae is a major cause of infections and reproductive disorders among horses, ranked in recent French studies as the sixth most frequently isolated bacterial pathogen in equine clinical samples. The proportion of multidrug-resistant (MDR) K. pneumoniae is therefore significant in a context where MDR K. pneumoniae strains are considered a major global concern by the World Health Organization. Unassigned: In this study, we used a genomic approach to characterize a population of 119 equine K. pneumoniae strains collected by two laboratories specialized in animal health in Normandy (France). We describe the main antibiotic resistance profiles and acquired resistance genes, and specify the proportion of virulence-encoding genes carried by these strains. The originality of our panel of strains lies in the broad collection period covered, ranging from 1996 to 2020, and the variety of sample sources: necropsies, suspected bacterial infections (e.g., genital, wound, allantochorion, and umbilical artery samples), and contagious equine metritis analyses. Unassigned: Our results reveal a remarkable level of genomic diversity among the strains studied and we report the presence of 39% MDR and 9% hypervirulent strains (including 5% that are both MDR and hypervirulent). Unassigned: These findings clearly emphasize the importance of improving the surveillance of K. pneumoniae in routine equine diagnostic tests to detect high-risk MDR-hypervirulent Klebsiella pneumoniae strains. The circulation of these worrisome strains reveals that they are not being detected by the simple K1, K2, and K5 serotype approach currently implemented in the French horse-breeding sector.
Publication Date: 2024-01-11 PubMed ID: 38274763PubMed Central: PMC10808340DOI: 10.3389/fmicb.2023.1334555Google 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 researchers studied the genetic diversity and antimicrobial resistance of the Klebsiella pneumoniae bacteria in horses, revealing a high level of genomic diversity and a significant number of multidrug-resistant strains.

Methodology

  • The diverse population of 119 equine Klebsiella pneumoniae strains used in the study was collected by two specialized animal health laboratories in Normandy, France. The strains were gathered over a lengthy period, from 1996 to 2020.
  • This wide spectrum of samples came from various sources including necropsies, suspected bacterial infections (like genital, wound, allantochorion, and umbilical artery samples), and contagious equine metritis analyses.

Findings

  • The study established a high degree of genomic diversity among the Klebsiella pneumoniae strains.
  • The team found that there were considerable levels of multidrug-resistant strains, representing 39% of the total strains.
  • The study also revealed the presence of 9% hypervirulent strains, with 5% of the overall strains showing both multidrug resistance and hypervirulence.

Implications

  • The researchers emphasized the need to improve the surveillance and detection of Klebsiella pneumoniae in routine equine diagnostic tests. Increasing these measures could help detect high-risk, multidrug-resistant, and hypervirulent strains of the bacteria.
  • Interestingly, these problematic strains of Klebsiella pneumoniae are not currently being identified through the traditional K1, K2, and K5 serotype approach used in the French horse-breeding sector.

Conclusion

  • The study reveals an urgent need for developing alternative strategies for detecting problematic Klebsiella pneumoniae strains to curb the rising incident of multidrug-resistant infections in horses.

Cite This Article

APA
Gravey F, Sévin C, Castagnet S, Foucher N, Maillard K, Tapprest J, Léon A, Langlois B, Le Hello S, Petry S. (2024). Antimicrobial resistance and genetic diversity of Klebsiella pneumoniae strains from different clinical sources in horses. Front Microbiol, 14, 1334555. https://doi.org/10.3389/fmicb.2023.1334555

Publication

ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 14
Pages: 1334555

Researcher Affiliations

Gravey, Francois
  • Department of Infectious Agents, Bacteriology, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
  • Department of Infectious Agents, Bacteriology, CHU Caen, Caen, France.
Sévin, Corinne
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Castagnet, Sophie
  • Department of Infectious Agents, Bacteriology, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
  • Research Department, LABÉO, Caen, France.
Foucher, Nathalie
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Maillard, Karine
  • Research Department, LABÉO, Caen, France.
Tapprest, Jackie
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
Léon, Albertine
  • Department of Infectious Agents, Bacteriology, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
  • Research Department, LABÉO, Caen, France.
Langlois, Bénédicte
  • Department of Infectious Agents, Bacteriology, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
Le Hello, Simon
  • Department of Infectious Agents, Bacteriology, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
  • Department of Infectious Agents, Bacteriology, CHU Caen, Caen, France.
Petry, Sandrine
  • ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.

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 44 references
  1. Akter R, El-Hage CM, Sansom FM, Carrick J, Devlin JM, Legione AR. Metagenomic investigation of potential abortigenic pathogens in foetal tissues from Australian horses. BMC Genomics 22:713.
    doi: 10.1186/s12864-021-08010-5pmc: PMC8487468pubmed: 34600470google scholar: lookup
  2. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M, Edalatmand A. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 48, D517–D525.
    doi: 10.1093/nar/gkz935pmc: PMC7145624pubmed: 31665441google scholar: lookup
  3. Andrews S. FastQC: a quality control tool for high throughput sequence data. .
  4. Arcari G, Carattoli A. Global spread and evolutionary convergence of multidrug-resistant and hypervirulent Klebsiella pneumoniae high-risk clones. Pathog Glob Health 117, 328–341.
  5. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19, 455–477.
    doi: 10.1089/cmb.2012.0021pmc: PMC3342519pubmed: 22506599google scholar: lookup
  6. Bialek-Davenet S, Criscuolo A, Ailloud F, Passet V, Jones L, Delannoy-Vieillard AS. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 20, 1812–1820.
    doi: 10.3201/eid2011.140206pmc: PMC4214299pubmed: 25341126google scholar: lookup
  7. 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 52, 112–119.
    doi: 10.1111/evj.13133pubmed: 31033041google scholar: lookup
  8. Brisse S, Passet V, Haugaard AB, Babosan A, Kassis-Chikhani N, Struve C. Wzi gene sequencing, a rapid method for determination of capsular type for Klebsiella strains. J Clin Microbiol 51, 4073–4078.
    doi: 10.1128/JCM.01924-13pmc: PMC3838100pubmed: 24088853google scholar: lookup
  9. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58, 3895–3903.
    doi: 10.1128/AAC.02412-14pmc: PMC4068535pubmed: 24777092google scholar: lookup
  10. CASFM. Comité de l’Antibiogramme de la Société Française de Microbiologie - Recommandations 2013. .
  11. CASFM. Comité de l’Antibiogramme de la Société Française de Microbiologie - Recommandations Vétérinaires 2021. .
  12. CASFM/EUCAST. Comité de l’antibiogramme de la Société Française de Microbiologie – Recommandations 2021 V.1.0 Avril. .
  13. Clausen PTLC, Aarestrup FM, Lund O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinform 19:307.
    doi: 10.1186/s12859-018-2336-6pmc: PMC6116485pubmed: 30157759google scholar: lookup
  14. Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43, 4178–4182.
  15. Dong N, Yang X, Chan EW, Zhang R, Chen S. Klebsiella species: taxonomy, hypervirulence and multidrug resistance. EBioMedicine 79:103998.
    doi: 10.1016/j.ebiom.2022.103998pmc: PMC9010751pubmed: 35405387google scholar: lookup
  16. Duchesne R, Castagnet S, Maillard K, Petry S, Cattoir V, Giard JC. In vitro antimicrobial susceptibility of equine clinical isolates from France, 2006-2016. J Glob Antimicrob Resist 19, 144–153.
    doi: 10.1016/j.jgar.2019.03.006pubmed: 30880244google scholar: lookup
  17. Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048.
  18. Follador R, Heinz E, Wyres KL, Ellington MJ, Kowarik M, Holt KE. The diversity of Klebsiella pneumoniae surface polysaccharides. Microb Genom 2:e000073.
    doi: 10.1099/mgen.0.000073pmc: PMC5320592pubmed: 28348868google scholar: lookup
  19. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075.
  20. Hennart M, Guglielmini J, Bridel S, Maiden MCJ, Jolley KA, Criscuolo A. Dual barcoding approach to bacterial strain nomenclature: genomic taxonomy of Klebsiella pneumoniae strains. Mol Biol Evol 39:msac135.
    doi: 10.1093/molbev/msac135pmc: PMC9254007pubmed: 35700230google scholar: lookup
  21. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 112, E3574–E3581.
    doi: 10.1073/pnas.1501049112pmc: PMC4500264pubmed: 26100894google scholar: lookup
  22. Jacoby GA. AmpC β-lactamases. Clin Microbiol Rev 22, 161–82, Table of Contents.
    doi: 10.1128/cmr.00036-08pmc: PMC2620637pubmed: 19136439google scholar: lookup
  23. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158, 1005–1015.
    doi: 10.1099/mic.0.055459-0pmc: PMC3492749pubmed: 22282518google scholar: lookup
  24. Lam MMC, Wick RR, Watts SC, Cerdeira LT, Wyres KL, Holt KE. A genomic surveillance framework and genotyping tool for Klebsiella pneumoniae and its related species complex. Nat Commun 12:4188.
    doi: 10.1038/s41467-021-24448-3pmc: PMC8263825pubmed: 34234121google scholar: lookup
  25. Lam MMC, Wyres KL, Duchêne S, Wick RR, Judd LM, Gan HH. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat Commun 9:2703.
    doi: 10.1038/s41467-018-05114-7pmc: PMC6045662pubmed: 30006589google scholar: lookup
  26. Lam MMC, Wyres KL, Wick RR, Judd LM, Fostervold A, Holt KE. Convergence of virulence and MDR in a single plasmid vector in MDR Klebsiella pneumoniae ST15. J Antimicrob Chemother 74, 1218–1222.
    doi: 10.1093/jac/dkz028pmc: PMC6477991pubmed: 30770708google scholar: lookup
  27. Laugier C, Foucher N, Sevin C, Leon A, Tapprest J. A 24-year retrospective study of equine abortion in Normandy (France). J Equine Vet 31, 116–123.
  28. Léon A, Castagnet S, Maillard K, Paillot R, Giard JC. Evolution of in vitro antimicrobial susceptibility of equine clinical isolates in France between 2016 and 2019. Animals 10:812.
    doi: 10.3390/ani10050812pmc: PMC7278474pubmed: 32392891google scholar: lookup
  29. Loncaric I, Cabal Rosel A, Szostak MP, Licka T, Allerberger F, Ruppitsch W. Broad-spectrum cephalosporin-resistant Klebsiella spp. isolated from diseased horses in Austria. Animals 10:332.
    doi: 10.3390/ani10020332pmc: PMC7070950pubmed: 32093201google scholar: lookup
  30. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18, 268–281.
  31. Malaluang P, Wilén E, Lindahl J, Hansson I, Morrell JM. Antimicrobial resistance in equine reproduction. Animals 11:3035.
    doi: 10.3390/ani11113035pmc: PMC8614435pubmed: 34827768google scholar: lookup
  32. Platt H, Atherton JG. Klebsiella and Enterobacter organisms isolated from horses. J Hyg Camb 77, 401–408.
    doi: 10.1017/s0022172400055789pmc: PMC2129811pubmed: 794407google scholar: lookup
  33. Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 32, e00001–e00019.
    doi: 10.1128/CMR.00001-19pmc: PMC6589860pubmed: 31092506google scholar: lookup
  34. Russo TA, Olson R, Fang CT, Stoesser N, Miller M, MacDonald U. Identification of biomarkers for differentiation of Hypervirulent Klebsiella pneumoniae from Classical K. pneumoniae. J Clin Microbiol 56, e00776–e00718.
    doi: 10.1128/JCM.00776-18pmc: PMC6113484pubmed: 29925642google scholar: lookup
  35. Shnaiderman-Torban A, Marchaim D, Navon-Venezia S, Lubrani O, Paitan Y, Arielly H. Third generation cephalosporin resistant Enterobacterales infections in hospitalized horses and donkeys: a case–case–control analysis. Antibiotics 10:155.
    doi: 10.3390/antibiotics10020155pmc: PMC7913880pubmed: 33557061google scholar: lookup
  36. Silva M, Machado MP, Silva DN, Rossi M, Moran-Gilad J, Santos S. chewBBACA: a complete suite for gene-by-gene schema creation and strain identification. Microbial Genom 4:3.
    doi: 10.1099/mgen.0.000166pmc: PMC5885018pubmed: 29543149google scholar: lookup
  37. Srinivasan VB, Rajamohan G. KpnEF, a new member of the Klebsiella pneumoniae cell envelope stress response regulon, is an SMR-type efflux pump involved in broad-spectrum antimicrobial resistance. Antimicrob Agents Chemother 57, 4449–4462.
    doi: 10.1128/AAC.02284-12pmc: PMC3754300pubmed: 23836167google scholar: lookup
  38. Tang M, Kong X, Hao J, Liu J. Epidemiological characteristics and formation mechanisms of multidrug-resistant Hypervirulent Klebsiella pneumoniae. Front Microbiol 11:581543.
    doi: 10.3389/fmicb.2020.581543pmc: PMC7714786pubmed: 33329444google scholar: lookup
  39. Trigo da Roza F, Couto N, Carneiro C, Cunha E, Rosa T, Magalhães M. Commonality of multidrug-resistant Klebsiella pneumoniae ST348 isolates in horses and humans in Portugal. Front Microbiol 10:1657.
    doi: 10.3389/fmicb.2019.01657pmc: PMC6657530pubmed: 31379799google scholar: lookup
  40. Turton JF, Baklan H, Siu LK, Kaufmann ME, Pitt TL. Evaluation of a multiplex PCR for detection of serotypes K1, K2 and K5 in Klebsiella sp. and comparison of isolates within these serotypes. FEMS Microbiol Lett 284, 247–252.
  41. Wick RR, Heinz E, Holt KE, Wyres KL. Kaptive web: user-friendly capsule and lipopolysaccharide serotype prediction for Klebsiella genomes. J Clin Microbiol 56, e00197–e00118.
    doi: 10.1128/JCM.00197-18pmc: PMC5971559pubmed: 29618504google scholar: lookup
  42. Wyres KL, Lam MMC, Holt KE. Population genomics of Klebsiella pneumoniae. Nat Rev Microbiol 18, 344–359.
    doi: 10.1038/s41579-019-0315-1pubmed: 32055025google scholar: lookup
  43. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67, 2640–2644.
    doi: 10.1093/jac/dks261pmc: PMC3468078pubmed: 22782487google scholar: lookup
  44. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C, Francisco AP. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 28, 1395–1404.
    doi: 10.1101/gr.232397.117pmc: PMC6120633pubmed: 30049790google scholar: lookup