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.
Copyright © 2024 Gravey, Sévin, Castagnet, Foucher, Maillard, Tapprest, Léon, Langlois, Le Hello and Petry.
Publication Date: 2024-01-11 PubMed ID: 38274763PubMed Central: PMC10808340DOI: 10.3389/fmicb.2023.1334555Google Scholar: Lookup
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- Journal Article
Summary
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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
Researcher Affiliations
- 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.
- ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
- 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.
- ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
- Research Department, LABÉO, Caen, France.
- ANSES, Normandy Laboratory for Animal Health, Physiopathology and Epidemiology of Equine Diseases Unit, Goustranville, France.
- 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.
- 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, Université de Caen Normandie, Université de Rouen Normandie, INSERM, DYNAMICURE UMR1311, CHU Caen, Caen, France.
- Department of Infectious Agents, Bacteriology, CHU Caen, Caen, France.
- 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
- 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.
- 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.
- Andrews S. FastQC: a quality control tool for high throughput sequence data. .
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- CASFM. Comité de l’Antibiogramme de la Société Française de Microbiologie - Recommandations 2013. .
- CASFM. Comité de l’Antibiogramme de la Société Française de Microbiologie - Recommandations Vétérinaires 2021. .
- CASFM/EUCAST. Comité de l’antibiogramme de la Société Française de Microbiologie – Recommandations 2021 V.1.0 Avril. .
- Clausen PTLC, Aarestrup FM, Lund O. Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinform 19:307.
- Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43, 4178–4182.
- Dong N, Yang X, Chan EW, Zhang R, Chen S. Klebsiella species: taxonomy, hypervirulence and multidrug resistance. EBioMedicine 79:103998.
- 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.
- 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.
- Follador R, Heinz E, Wyres KL, Ellington MJ, Kowarik M, Holt KE. The diversity of Klebsiella pneumoniae surface polysaccharides. Microb Genom 2:e000073.
- Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075.
- 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.
- 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.
- Jacoby GA. AmpC β-lactamases. Clin Microbiol Rev 22, 161–82, Table of Contents.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- Malaluang P, Wilén E, Lindahl J, Hansson I, Morrell JM. Antimicrobial resistance in equine reproduction. Animals 11:3035.
- Platt H, Atherton JG. Klebsiella and Enterobacter organisms isolated from horses. J Hyg Camb 77, 401–408.
- Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 32, e00001–e00019.
- 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.
- 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.
- 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.
- 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.
- Tang M, Kong X, Hao J, Liu J. Epidemiological characteristics and formation mechanisms of multidrug-resistant Hypervirulent Klebsiella pneumoniae. Front Microbiol 11:581543.
- 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.
- 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.
- 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.
- Wyres KL, Lam MMC, Holt KE. Population genomics of Klebsiella pneumoniae. Nat Rev Microbiol 18, 344–359.
- Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67, 2640–2644.
- 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.
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