The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals

Carbapenemase-producing Enterobacterales (CPE) are considered a major public health issue. In the frame of the EU Harmonized AMR Monitoring program conducted in Italy in 2021, 21 epidemiological units of fattening pigs (6.98%; 95% CI 4.37–10.47%; 21/301) and four epidemiological units of bovines &am...

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Main Authors: Virginia Carfora, Elena Lavinia Diaconu, Angela Ianzano, Paola Di Matteo, Roberta Amoruso, Elena Dell'Aira, Luigi Sorbara, Francesco Bottoni, Flavia Guarneri, Laura Campana, Alessia Franco, Patricia Alba, Antonio Battisti
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1016895/full
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author Virginia Carfora
Elena Lavinia Diaconu
Angela Ianzano
Paola Di Matteo
Roberta Amoruso
Elena Dell'Aira
Luigi Sorbara
Francesco Bottoni
Flavia Guarneri
Laura Campana
Alessia Franco
Patricia Alba
Antonio Battisti
author_facet Virginia Carfora
Elena Lavinia Diaconu
Angela Ianzano
Paola Di Matteo
Roberta Amoruso
Elena Dell'Aira
Luigi Sorbara
Francesco Bottoni
Flavia Guarneri
Laura Campana
Alessia Franco
Patricia Alba
Antonio Battisti
author_sort Virginia Carfora
collection DOAJ
description Carbapenemase-producing Enterobacterales (CPE) are considered a major public health issue. In the frame of the EU Harmonized AMR Monitoring program conducted in Italy in 2021, 21 epidemiological units of fattening pigs (6.98%; 95% CI 4.37–10.47%; 21/301) and four epidemiological units of bovines <12 months (1.29%; 95% CI 0.35–3.27%, 4/310) resulted positive to OXA-48-like-producing E. coli (n = 24 OXA-181, n = 1 OXA-48). Whole Genome Sequencing (WGS) for in-depth characterization, genomics and cluster analysis of OXA-181-(and one OXA-48) producing E. coli isolated, was performed. Tracing-back activities at: (a) the fattening holding of origin of one positive slaughter batch, (b) the breeding holding, and (c) one epidemiologically related dairy cattle holding, allowed detection of OXA-48-like-producing E. coli in different units and comparison of further human isolates from fecal samples of farm workers. The OXA-181-producing isolates were multidrug resistant (MDR), belonged to different Sequence Types (STs), harbored the IncX and IncF plasmid replicons and multiple virulence genes. Bioinformatics analysis of combined Oxford Nanopore Technologies (ONT) long reads and Illumina short reads identified blaOXA-181 as part of a transposon in IncX1, IncX3, and IncFII fully resolved plasmids from 16 selected E. coli, mostly belonging to ST5229, isolated during the survey at slaughter and tracing-back activities. Although human source could be the most likely cause for the introduction of the blaOXA-181-carrying IncX1 plasmid in the breeding holding, concerns arise from carbapenemase OXA-48-like-producing E. coli spreading in 2021 in Italian fattening pigs and, to a lesser extent, in veal calf holdings.
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spelling doaj.art-e52517b408f1465596cd9cc8ba7f4c942022-12-22T04:14:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-11-011310.3389/fmicb.2022.10168951016895The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animalsVirginia Carfora0Elena Lavinia Diaconu1Angela Ianzano2Paola Di Matteo3Roberta Amoruso4Elena Dell'Aira5Luigi Sorbara6Francesco Bottoni7Flavia Guarneri8Laura Campana9Alessia Franco10Patricia Alba11Antonio Battisti12Department of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalySede Territoriale di Brescia, Laboratorio Diagnostica Generale, Istituto Zooprofilattico Sperimentale Della Lombardia e Dell’Emilia-Romagna “Bruno Ubertini”, Brescia, ItalyAgenzia Tutela Della Salute, Brescia, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyDepartment of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, Rome, ItalyCarbapenemase-producing Enterobacterales (CPE) are considered a major public health issue. In the frame of the EU Harmonized AMR Monitoring program conducted in Italy in 2021, 21 epidemiological units of fattening pigs (6.98%; 95% CI 4.37–10.47%; 21/301) and four epidemiological units of bovines <12 months (1.29%; 95% CI 0.35–3.27%, 4/310) resulted positive to OXA-48-like-producing E. coli (n = 24 OXA-181, n = 1 OXA-48). Whole Genome Sequencing (WGS) for in-depth characterization, genomics and cluster analysis of OXA-181-(and one OXA-48) producing E. coli isolated, was performed. Tracing-back activities at: (a) the fattening holding of origin of one positive slaughter batch, (b) the breeding holding, and (c) one epidemiologically related dairy cattle holding, allowed detection of OXA-48-like-producing E. coli in different units and comparison of further human isolates from fecal samples of farm workers. The OXA-181-producing isolates were multidrug resistant (MDR), belonged to different Sequence Types (STs), harbored the IncX and IncF plasmid replicons and multiple virulence genes. Bioinformatics analysis of combined Oxford Nanopore Technologies (ONT) long reads and Illumina short reads identified blaOXA-181 as part of a transposon in IncX1, IncX3, and IncFII fully resolved plasmids from 16 selected E. coli, mostly belonging to ST5229, isolated during the survey at slaughter and tracing-back activities. Although human source could be the most likely cause for the introduction of the blaOXA-181-carrying IncX1 plasmid in the breeding holding, concerns arise from carbapenemase OXA-48-like-producing E. coli spreading in 2021 in Italian fattening pigs and, to a lesser extent, in veal calf holdings.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1016895/fullcarbapenem-resistant EnterobacteralesOXA-48-like carbapenemasesOXA-181 carbapenemaseslong-read sequencingWhole Genome Sequencingplasmids
spellingShingle Virginia Carfora
Elena Lavinia Diaconu
Angela Ianzano
Paola Di Matteo
Roberta Amoruso
Elena Dell'Aira
Luigi Sorbara
Francesco Bottoni
Flavia Guarneri
Laura Campana
Alessia Franco
Patricia Alba
Antonio Battisti
The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
Frontiers in Microbiology
carbapenem-resistant Enterobacterales
OXA-48-like carbapenemases
OXA-181 carbapenemases
long-read sequencing
Whole Genome Sequencing
plasmids
title The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
title_full The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
title_fullStr The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
title_full_unstemmed The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
title_short The hazard of carbapenemase (OXA-181)-producing Escherichia coli spreading in pig and veal calf holdings in Italy in the genomics era: Risk of spill over and spill back between humans and animals
title_sort hazard of carbapenemase oxa 181 producing escherichia coli spreading in pig and veal calf holdings in italy in the genomics era risk of spill over and spill back between humans and animals
topic carbapenem-resistant Enterobacterales
OXA-48-like carbapenemases
OXA-181 carbapenemases
long-read sequencing
Whole Genome Sequencing
plasmids
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1016895/full
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