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Frontiers in microbiology2020; 11; 616032; doi: 10.3389/fmicb.2020.616032

Emergence and Spread of Different ESBL-Producing Salmonella enterica Serovars in Hospitalized Horses Sharing a Highly Transferable IncM2 CTX-M-3-Encoding Plasmid.

Abstract: is a major causative pathogen of human and animal gastroenteritis. Antibiotic resistant strains have emerged due to the production of extended-spectrum β-lactamases (ESBLs) posing a major health concern. With the increasing reports on ESBL-producing Enterobacterales that colonize companion animals, we aimed to investigate ESBL dissemination among ESBL-producing (ESBL-S) in hospitalized horses. We prospectively collected ESBL-S isolates from hospitalized horses in a Veterinary-Teaching Hospital during Dec 2015-Dec 2017. Selection criteria for ESBL-S were white colonies on CHROMagarESBL plates and an ESBL phenotypic confirmation. serovars were determined using the Kaufmann-White-Le-Minor serological scheme. ESBL-encoding plasmids were purified, transformed and compared using restriction fragment length polymorphism (RFLP). Whole genome sequencing (Illumina and MinION platforms) were performed for detailed phylogenetic and plasmid analyses. Twelve ESBL-S were included in this study. Molecular investigation and Sequence Read Archive (SRA) meta-analysis revealed the presence of three unique serovars, Cerro, Havana and Liverpool, all reported for the first time in horses. PFGE revealed the clonal spread of Cerro between seven horses. All twelve isolates carried and showed an identical multidrug resistance profile with co-resistance to trimethoprim/sulfamethoxazole and to aminoglycosides. Plasmid RFLP proved the inter-serovar horizontal spread of a single -encoding plasmid. Complete sequence of a representative plasmid (. Havana strain 373.3.1), designated pSEIL-3 was a -86.4 Kb IncM2 plasmid, that encoded nine antibiotic resistance genes. pSEIL-3 was virtually identical to pCTX-M3 from , and showed high identity (>95%) to six other or IncM2 broad host range plasmids from various Enterobacterales of human origin. Using a specific six gene-based multiplex PCR, we detected pSEIL-3 in various Enterobacterales species that co-colonized the horses' gut. Together, our findings show the alarming emergence of ESBL-S in hospitalized horses associated with gut shedding and foal morbidity and mortality. We demonstrated the dissemination of CTX-M-3 ESBL among different serovars due to transmission of a broad host range plasmid. This report highlights horses as a zoonotic reservoir for ESBL-S, including highly transmissible plasmids that may represent a 'One-Health' hazard. This risk calls for the implementation of infection control measures to monitor and control the spread of ESBL-S in hospitalized horses.
Copyright © 2020 Dor, Shnaiderman-Torban, Kondratyeva, Davidovich-Cohen, Rokney, Steinman and Navon-Venezia.
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Publication Date: 2020-12-17 PubMed ID: 33391248PubMed Central: PMC7773750DOI: 10.3389/fmicb.2020.616032Google 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.

The research study investigates the emergence and dissemination of antibiotic resistant strains of Salmonella enterica in hospitalized horses, triggered by the production of certain proteins called extended-spectrum β-lactamases (ESBLs). The study identified the presence of a highly transferable factor, an IncM2 CTX-M-3-encoding plasmid, that facilitated the spread of resistance across different Salmonella enterica serovars.

Objectives and Methodology

  • The research aimed to understand the spread of ESBL-producing Salmonella enterica (ESBL-S) in hospitalized horses. This was motivated by the rising incidents of ESBL-producing Enterobacterales colonizing companion animals.
  • ESBL-S samples were collected from horses in a Veterinary-Teaching Hospital over a period of two years. These samples were identified through the presence of white colonies on CHROMagarESBL plates and an ESBL phenotypic confirmation.
  • Different Salmonella enterica serovars were identified using the Kaufmann-White-Le-Minor serological scheme.
  • The ESBL-encoding plasmids, molecules of DNA that can exist and replicate independently of the chromosomes, in these samples were analyzed using restriction fragment length polymorphism (RFLP) and detailed phylogenetic and plasmid analyses were performed through whole genome sequencing.

Key Findings

  • The study identified twelve ESBL-S strains, with three unique Salmonella enterica serovars, Cerro, Havana and Liverpool, being reported in horses for the first time.
  • Investigations revealed the clonal spread of the Cerro serovar among seven horses, implying identical or highly similar genetic material, indicating a common source or transmission path.
  • All twelve isolates presented the same multidrug resistance profile and contained a CTX-M3 ESBL, suggesting a shared resistance mechanism and the presence of the same plasmid aiding the inter-serovar spread of antibiotic resistance.
  • The plasmid, named pSEIL-3, was found to be almost identical to pCTX-M3 from Escherichia coli, showcasing a high identity to six other CTX-M3 or CTX-M2 IncM2 plasmids of human origin, underlining the wide host range the plasmid can inhabit.
  • Through multiplex PCR, the researchers identified the presence of pSEIL-3 in various Enterobacterales species found in the horses’ gut.

Implications and Recommendations

  • With the emergence of ESBL-S in hospitalized horses linked to gut shedding and morbidity and mortality in foals, this study raises an alarm about a significant health hazard.
  • It underscores the risk posed by horses as a zoonotic reservoir for ESBL-S and emphasizes the need for strict infection control measures to monitor and control the spread of ESBL-S in hospitalized horses.

Cite This Article

APA
Dor Z, Shnaiderman-Torban A, Kondratyeva K, Davidovich-Cohen M, Rokney A, Steinman A, Navon-Venezia S. (2020). Emergence and Spread of Different ESBL-Producing Salmonella enterica Serovars in Hospitalized Horses Sharing a Highly Transferable IncM2 CTX-M-3-Encoding Plasmid. Front Microbiol, 11, 616032. https://doi.org/10.3389/fmicb.2020.616032

Publication

Frontiers in microbiology
ISSN: 1664-302X
NlmUniqueID: 101548977
Country: Switzerland
Language: English
Volume: 11
Pages: 616032
PII: 616032

Researcher Affiliations

Dor, Ziv
  • Department of Molecular Biology, Ariel University, Ariel, Israel.
Shnaiderman-Torban, Anat
  • Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
Kondratyeva, Kira
  • Department of Molecular Biology, Ariel University, Ariel, Israel.
Davidovich-Cohen, Maya
  • Government Central Laboratories, Ministry of Health, Jerusalem, Israel.
Rokney, Assaf
  • Government Central Laboratories, Ministry of Health, Jerusalem, Israel.
Steinman, Amir
  • Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
Navon-Venezia, Shiri
  • Department of Molecular Biology, Ariel University, Ariel, Israel.
  • The Dr. Miriam and Sheldon G. Adelson School of Medicine, Ariel University, Ariel, Israel.

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.

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