Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Gentilini, Fabio, Turba, Maria Elena, Pasquali, Frederique, Mion, Domenico, Romagnoli, Noemi, Zambon, Elisa, Terni, Daniele, Peirano, Gisele, Pitout, Johann Dawid Daniel, Parisi, Antonio, Sambri, Vittorio, Zanoni, Renato Giulio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6291488/
https://www.ncbi.nlm.nih.gov/pubmed/30574124
http://dx.doi.org/10.3389/fmicb.2018.02872
_version_ 1783380257734131712
author Gentilini, Fabio
Turba, Maria Elena
Pasquali, Frederique
Mion, Domenico
Romagnoli, Noemi
Zambon, Elisa
Terni, Daniele
Peirano, Gisele
Pitout, Johann Dawid Daniel
Parisi, Antonio
Sambri, Vittorio
Zanoni, Renato Giulio
author_facet Gentilini, Fabio
Turba, Maria Elena
Pasquali, Frederique
Mion, Domenico
Romagnoli, Noemi
Zambon, Elisa
Terni, Daniele
Peirano, Gisele
Pitout, Johann Dawid Daniel
Parisi, Antonio
Sambri, Vittorio
Zanoni, Renato Giulio
author_sort Gentilini, Fabio
collection PubMed
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 bla(NDM-1) and bla(OXA-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.
format Online
Article
Text
id pubmed-6291488
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-62914882018-12-20 Hospitalized Pets as a Source of Carbapenem-Resistance Gentilini, Fabio Turba, Maria Elena Pasquali, Frederique Mion, Domenico Romagnoli, Noemi Zambon, Elisa Terni, Daniele Peirano, Gisele Pitout, Johann Dawid Daniel Parisi, Antonio Sambri, Vittorio Zanoni, Renato Giulio Front Microbiol Microbiology 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 bla(NDM-1) and bla(OXA-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. Frontiers Media S.A. 2018-12-06 /pmc/articles/PMC6291488/ /pubmed/30574124 http://dx.doi.org/10.3389/fmicb.2018.02872 Text en Copyright © 2018 Gentilini, Turba, Pasquali, Mion, Romagnoli, Zambon, Terni, Peirano, Pitout, Parisi, Sambri and Zanoni. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Gentilini, Fabio
Turba, Maria Elena
Pasquali, Frederique
Mion, Domenico
Romagnoli, Noemi
Zambon, Elisa
Terni, Daniele
Peirano, Gisele
Pitout, Johann Dawid Daniel
Parisi, Antonio
Sambri, Vittorio
Zanoni, Renato Giulio
Hospitalized Pets as a Source of Carbapenem-Resistance
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 Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6291488/
https://www.ncbi.nlm.nih.gov/pubmed/30574124
http://dx.doi.org/10.3389/fmicb.2018.02872
work_keys_str_mv AT gentilinifabio hospitalizedpetsasasourceofcarbapenemresistance
AT turbamariaelena hospitalizedpetsasasourceofcarbapenemresistance
AT pasqualifrederique hospitalizedpetsasasourceofcarbapenemresistance
AT miondomenico hospitalizedpetsasasourceofcarbapenemresistance
AT romagnolinoemi hospitalizedpetsasasourceofcarbapenemresistance
AT zambonelisa hospitalizedpetsasasourceofcarbapenemresistance
AT ternidaniele hospitalizedpetsasasourceofcarbapenemresistance
AT peiranogisele hospitalizedpetsasasourceofcarbapenemresistance
AT pitoutjohanndawiddaniel hospitalizedpetsasasourceofcarbapenemresistance
AT parisiantonio hospitalizedpetsasasourceofcarbapenemresistance
AT sambrivittorio hospitalizedpetsasasourceofcarbapenemresistance
AT zanonirenatogiulio hospitalizedpetsasasourceofcarbapenemresistance