Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals

IntroductionHealthcare-associated infections (HCAIs) associated with extended-spectrum cephalosporin-resistant gram-negative (ESC-R GN) bacteria are an emerging concern in veterinary hospitals, especially in companion animal intensive care units (ICUs).MethodsTo understand the molecular epidemiology...

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Main Authors: Flavia Zendri, Cajsa M. Isgren, Jane Devaney, Vanessa Schmidt, Rachel Rankin, Dorina Timofte
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1252216/full
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author Flavia Zendri
Cajsa M. Isgren
Jane Devaney
Vanessa Schmidt
Rachel Rankin
Dorina Timofte
author_facet Flavia Zendri
Cajsa M. Isgren
Jane Devaney
Vanessa Schmidt
Rachel Rankin
Dorina Timofte
author_sort Flavia Zendri
collection DOAJ
description IntroductionHealthcare-associated infections (HCAIs) associated with extended-spectrum cephalosporin-resistant gram-negative (ESC-R GN) bacteria are an emerging concern in veterinary hospitals, especially in companion animal intensive care units (ICUs).MethodsTo understand the molecular epidemiology of ESC-R GN isolates in two veterinary hospitals (equine and small animal), a 6-month pilot study was performed during which fecal and environmental samples were obtained twice from selected patients, upon ICU admission and after 48 h of hospitalization. In total, 295 ESC-R GNs were analyzed using the Acuitas Resistome® Test (OpGen, Maryland, US), a PCR-based assay screening for 50 antimicrobial resistance gene families encoding for production of extended-spectrum beta-lactamase (ESBLs), TEM/SHV/OXA or AmpC beta-lactamases and carbapenemases. Combining organism identification and antimicrobial susceptibility data to genotyping results, unique “Acuitas profiles” were generated that can be used for fast typing the isolates and tracking transmission events.ResultsESKAPE GN pathogens were the most prevalent ESC-R GN isolates circulating in both the small animal and equine hospitals, consisting of Enterobacter cloacae complex (21.7%), Pseudomonas aeruginosa (20%), Klebsiella pneumoniae (15.9%), and Acinetobacter baumannii complex (13.6%) followed by Escherichia coli (12.2%), most harboring a combination of genes encoding for beta-lactamases and ESBLs. Some ESKAPE genotypes showed likely intra-hospital transmission, including E. cloacae (two genotypes, one carrying SHV4, SHV5, and TEM7 and the other TEM1, TEM3, and TEM7 enzymes) in the equine and K. pneumoniae (SHV1, SHV5, and DHA1-positive) in the small animal ICUs, respectively. Furthermore, P. aeruginosa (carrying OXA-50), A. baumannii complex (OXA-51), and E. coli (CTX-M-1) genotypes were isolated across both hospitals, suggesting possible transfer mediated via movement of staff and students. Importantly, isolates carrying transmissible resistance to last-resort antimicrobials (i.e. carbapenems) were identified within the hospital environments, consisting of three environmental Acinetobacter spp. harboring blaOXA − 23 and one clinical E. coli with blaOXA − 48.ConclusionWe describe the widespread occurrence of ESKAPE gram-negative organisms in veterinary ICU patients and hospital environments. Findings from this project provide baseline data on the epidemiology of ESKAPE pathogens in veterinary settings, which can inform infection control policies to aid in patient management and prevent transmission of nosocomial infections associated with these pathogens.
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spelling doaj.art-c148b62bd8654a7c9f5fffb24b38b3e22023-09-07T21:13:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12522161252216Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitalsFlavia Zendri0Cajsa M. Isgren1Jane Devaney2Vanessa Schmidt3Rachel Rankin4Dorina Timofte5Department of Veterinary Anatomy, Physiology and Pathology, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Neston, United KingdomWestern Counties Equine Hospital Ltd., Culmstock, United KingdomDepartment of Equine Clinical Science, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, United KingdomDepartment of Small Animal Clinical Science, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, United KingdomDepartment of Small Animal Clinical Science, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Leahurst Campus, Neston, United KingdomDepartment of Veterinary Anatomy, Physiology and Pathology, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Neston, United KingdomIntroductionHealthcare-associated infections (HCAIs) associated with extended-spectrum cephalosporin-resistant gram-negative (ESC-R GN) bacteria are an emerging concern in veterinary hospitals, especially in companion animal intensive care units (ICUs).MethodsTo understand the molecular epidemiology of ESC-R GN isolates in two veterinary hospitals (equine and small animal), a 6-month pilot study was performed during which fecal and environmental samples were obtained twice from selected patients, upon ICU admission and after 48 h of hospitalization. In total, 295 ESC-R GNs were analyzed using the Acuitas Resistome® Test (OpGen, Maryland, US), a PCR-based assay screening for 50 antimicrobial resistance gene families encoding for production of extended-spectrum beta-lactamase (ESBLs), TEM/SHV/OXA or AmpC beta-lactamases and carbapenemases. Combining organism identification and antimicrobial susceptibility data to genotyping results, unique “Acuitas profiles” were generated that can be used for fast typing the isolates and tracking transmission events.ResultsESKAPE GN pathogens were the most prevalent ESC-R GN isolates circulating in both the small animal and equine hospitals, consisting of Enterobacter cloacae complex (21.7%), Pseudomonas aeruginosa (20%), Klebsiella pneumoniae (15.9%), and Acinetobacter baumannii complex (13.6%) followed by Escherichia coli (12.2%), most harboring a combination of genes encoding for beta-lactamases and ESBLs. Some ESKAPE genotypes showed likely intra-hospital transmission, including E. cloacae (two genotypes, one carrying SHV4, SHV5, and TEM7 and the other TEM1, TEM3, and TEM7 enzymes) in the equine and K. pneumoniae (SHV1, SHV5, and DHA1-positive) in the small animal ICUs, respectively. Furthermore, P. aeruginosa (carrying OXA-50), A. baumannii complex (OXA-51), and E. coli (CTX-M-1) genotypes were isolated across both hospitals, suggesting possible transfer mediated via movement of staff and students. Importantly, isolates carrying transmissible resistance to last-resort antimicrobials (i.e. carbapenems) were identified within the hospital environments, consisting of three environmental Acinetobacter spp. harboring blaOXA − 23 and one clinical E. coli with blaOXA − 48.ConclusionWe describe the widespread occurrence of ESKAPE gram-negative organisms in veterinary ICU patients and hospital environments. Findings from this project provide baseline data on the epidemiology of ESKAPE pathogens in veterinary settings, which can inform infection control policies to aid in patient management and prevent transmission of nosocomial infections associated with these pathogens.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1252216/fullveterinaryinfection controlgram-negativeESKAPEcompanion animalssurveillance
spellingShingle Flavia Zendri
Cajsa M. Isgren
Jane Devaney
Vanessa Schmidt
Rachel Rankin
Dorina Timofte
Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
Frontiers in Microbiology
veterinary
infection control
gram-negative
ESKAPE
companion animals
surveillance
title Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
title_full Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
title_fullStr Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
title_full_unstemmed Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
title_short Resistome-based surveillance identifies ESKAPE pathogens as the predominant gram-negative organisms circulating in veterinary hospitals
title_sort resistome based surveillance identifies eskape pathogens as the predominant gram negative organisms circulating in veterinary hospitals
topic veterinary
infection control
gram-negative
ESKAPE
companion animals
surveillance
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1252216/full
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