Hospitalized Pets as a Source of Carbapenem-Resistance

The massive and irrational use of antibiotics in livestock productions has fostered the occurrence and spread of resistance to “old class antimicrobials.” To cope with that phenomenon, some regulations have been already enforced in the member states of the European Union. However, a role of livestoc...

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Main Authors: Fabio Gentilini, Maria Elena Turba, Frederique Pasquali, Domenico Mion, Noemi Romagnoli, Elisa Zambon, Daniele Terni, Gisele Peirano, Johann Dawid Daniel Pitout, Antonio Parisi, Vittorio Sambri, Renato Giulio Zanoni
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02872/full
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author Fabio Gentilini
Maria Elena Turba
Frederique Pasquali
Domenico Mion
Noemi Romagnoli
Elisa Zambon
Daniele Terni
Gisele Peirano
Johann Dawid Daniel Pitout
Antonio Parisi
Vittorio Sambri
Vittorio Sambri
Renato Giulio Zanoni
author_facet Fabio Gentilini
Maria Elena Turba
Frederique Pasquali
Domenico Mion
Noemi Romagnoli
Elisa Zambon
Daniele Terni
Gisele Peirano
Johann Dawid Daniel Pitout
Antonio Parisi
Vittorio Sambri
Vittorio Sambri
Renato Giulio Zanoni
author_sort Fabio Gentilini
collection DOAJ
description The massive and irrational use of antibiotics in livestock productions has fostered the occurrence and spread of resistance to “old class antimicrobials.” To cope with that phenomenon, some regulations have been already enforced in the member states of the European Union. However, a role of livestock animals in the relatively recent alerts on the rapid worldwide increase of resistance to last-choice antimicrobials as carbapenems is very unlikely. Conversely, these antimicrobials are increasingly administered in veterinary hospitals whose role in spreading bacteria or mobile genetic elements has not adequately been addressed so far. A cross-sectional study was carried out on 105 hospitalized and 100 non-hospitalized pets with the aim of measuring the prevalence of carbapenem-resistant Gram-negative bacteria (GNB) colonizing dogs and cats, either hospitalized or not hospitalized and estimating the relative odds. Stool samples were inoculated on MacConkey agar plates containing 1 mg/L imipenem which were then incubated aerobically at 37°C ± 1 for 48 h. Isolated bacteria were identified first by Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and were confirmed by 16S rRNA sequencing. The genetic basis of resistance was investigated using PCR methods, gene or whole genome sequencing (WGS). The prevalence of pets harboring carbapenem-resistant bacteria was 11.4 and 1.0% in hospitalized and not-hospitalized animals, respectively, with an odds ratio of 12.8 (p < 0.01). One pet carried two diverse isolates. Overall, 14 gram-negative non-fermenting bacteria, specifically, one Acinetobacter radioresistens, five Acinetobacter baumannii, six Pseudomonas aeruginosa and two Stenotrophomonas maltophilia were isolated. The Acinetobacter species carried acquired carbapenemases genes encoded by blaNDM-1 and blaOXA-23. In contrast, Pseudomonas phenotypic resistance was associated with the presence of mutations in the oprD gene. Notably, inherent carbapenem-resistant isolates of S. maltophilia were also resistant to the first-line recommended chemotherapeutic trimethoprim/sulfamethoxazole. This study estimates the risk of colonization by carbapenem-resistant non-fermenting GNB in pets hospitalized in veterinary tertiary care centers and highlights their potential role in spreading resistance genes among the animal and human community. Public health authorities should consider extending surveillance systems and putting the release of critical antibiotics under more strict control in order to manage the infection/colonization of pets in veterinary settings.
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spelling doaj.art-65d3216fc808473b8332d7089b649edf2022-12-22T01:59:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-12-01910.3389/fmicb.2018.02872334579Hospitalized Pets as a Source of Carbapenem-ResistanceFabio Gentilini0Maria Elena Turba1Frederique Pasquali2Domenico Mion3Noemi Romagnoli4Elisa Zambon5Daniele Terni6Gisele Peirano7Johann Dawid Daniel Pitout8Antonio Parisi9Vittorio Sambri10Vittorio Sambri11Renato Giulio Zanoni12Department of Veterinary Medical Sciences, University of Bologna, Bologna, ItalyGenefast Srl, Forlì, ItalyDepartment of Agricultural and Food Sciences, University of Bologna, Bologna, ItalyDepartment of Veterinary Medical Sciences, University of Bologna, Bologna, ItalyDepartment of Veterinary Medical Sciences, University of Bologna, Bologna, ItalyOspedale: Veterinario I Portoni Rossi s.r.l., Bologna, ItalyOspedale: Veterinario I Portoni Rossi s.r.l., Bologna, ItalyUnit of Microbiology, University of Calgary and Calgary Laboratory Services, Calgary, AB, CanadaUnit of Microbiology, University of Calgary and Calgary Laboratory Services, Calgary, AB, CanadaIstituto Zooprofilattico Sperimentale della Puglia e della Basilicata, Foggia, ItalyThe Great Romagna Hub Laboratory, Pievesestina, ItalyDepartment of Experimental, Diagnostic and Specialty Medicine - DIMES, University of Bologna, Bologna, ItalyDepartment of Veterinary Medical Sciences, University of Bologna, Bologna, ItalyThe massive and irrational use of antibiotics in livestock productions has fostered the occurrence and spread of resistance to “old class antimicrobials.” To cope with that phenomenon, some regulations have been already enforced in the member states of the European Union. However, a role of livestock animals in the relatively recent alerts on the rapid worldwide increase of resistance to last-choice antimicrobials as carbapenems is very unlikely. Conversely, these antimicrobials are increasingly administered in veterinary hospitals whose role in spreading bacteria or mobile genetic elements has not adequately been addressed so far. A cross-sectional study was carried out on 105 hospitalized and 100 non-hospitalized pets with the aim of measuring the prevalence of carbapenem-resistant Gram-negative bacteria (GNB) colonizing dogs and cats, either hospitalized or not hospitalized and estimating the relative odds. Stool samples were inoculated on MacConkey agar plates containing 1 mg/L imipenem which were then incubated aerobically at 37°C ± 1 for 48 h. Isolated bacteria were identified first by Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and were confirmed by 16S rRNA sequencing. The genetic basis of resistance was investigated using PCR methods, gene or whole genome sequencing (WGS). The prevalence of pets harboring carbapenem-resistant bacteria was 11.4 and 1.0% in hospitalized and not-hospitalized animals, respectively, with an odds ratio of 12.8 (p < 0.01). One pet carried two diverse isolates. Overall, 14 gram-negative non-fermenting bacteria, specifically, one Acinetobacter radioresistens, five Acinetobacter baumannii, six Pseudomonas aeruginosa and two Stenotrophomonas maltophilia were isolated. The Acinetobacter species carried acquired carbapenemases genes encoded by blaNDM-1 and blaOXA-23. In contrast, Pseudomonas phenotypic resistance was associated with the presence of mutations in the oprD gene. Notably, inherent carbapenem-resistant isolates of S. maltophilia were also resistant to the first-line recommended chemotherapeutic trimethoprim/sulfamethoxazole. This study estimates the risk of colonization by carbapenem-resistant non-fermenting GNB in pets hospitalized in veterinary tertiary care centers and highlights their potential role in spreading resistance genes among the animal and human community. Public health authorities should consider extending surveillance systems and putting the release of critical antibiotics under more strict control in order to manage the infection/colonization of pets in veterinary settings.https://www.frontiersin.org/article/10.3389/fmicb.2018.02872/fullone healthcarbapenem resistanceAcinetobacter radioresistensdogs and catshospitalizationveterinary tertiary care facilities
spellingShingle Fabio Gentilini
Maria Elena Turba
Frederique Pasquali
Domenico Mion
Noemi Romagnoli
Elisa Zambon
Daniele Terni
Gisele Peirano
Johann Dawid Daniel Pitout
Antonio Parisi
Vittorio Sambri
Vittorio Sambri
Renato Giulio Zanoni
Hospitalized Pets as a Source of Carbapenem-Resistance
Frontiers in Microbiology
one health
carbapenem resistance
Acinetobacter radioresistens
dogs and cats
hospitalization
veterinary tertiary care facilities
title Hospitalized Pets as a Source of Carbapenem-Resistance
title_full Hospitalized Pets as a Source of Carbapenem-Resistance
title_fullStr Hospitalized Pets as a Source of Carbapenem-Resistance
title_full_unstemmed Hospitalized Pets as a Source of Carbapenem-Resistance
title_short Hospitalized Pets as a Source of Carbapenem-Resistance
title_sort hospitalized pets as a source of carbapenem resistance
topic one health
carbapenem resistance
Acinetobacter radioresistens
dogs and cats
hospitalization
veterinary tertiary care facilities
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02872/full
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