Genomic Diversity and Virulence Potential of ESBL- and AmpC-β-Lactamase-Producing Escherichia coli Strains From Healthy Food Animals Across Europe
The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal Escherichia spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in vario...
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| Published in | Frontiers in microbiology Vol. 12; p. 626774 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
01.04.2021
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| Online Access | Get full text |
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| Abstract | The role of livestock animals as a putative source of ESBL/pAmpC
E. coli
for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal
Escherichia
spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred
Escherichia
spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST).
In silico
screening of WGS data of 99 isolates (98
E. coli
and 1
E. fergusonii
) revealed
bla
SHV
–
12
(32.3%),
bla
CTX
–
M
–
1
(24.2%), and
bla
CMY
–
2
(22.2%) as predominant ESBL/pAmpC types. Other types were
bla
SHV
–
2
(1.0%),
bla
CTX
–
M
–
2
/
–
14
/
–
15
(1.0/6.1/1.0%), and
bla
TEM
–
52
(5.1%). Six isolates revealed AmpC-promoter mutations (position −42 (C > T) and one carried
mcr-1
. The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The
bla
TEM
–
52
genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to
E
. clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic
E. coli
(ExPEC; 2.0%), avian pathogenic
E. coli
(APEC; 51.5%), and atypical enteropathogenic
E. coli
(EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health. |
|---|---|
| AbstractList | The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal Escherichia spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred Escherichia spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST). In silico screening of WGS data of 99 isolates (98 E. coli and 1 E. fergusonii) revealed blaSHV–12 (32.3%), blaCTX–M–1 (24.2%), and blaCMY–2 (22.2%) as predominant ESBL/pAmpC types. Other types were blaSHV–2 (1.0%), blaCTX–M–2/–14/–15 (1.0/6.1/1.0%), and blaTEM–52 (5.1%). Six isolates revealed AmpC-promoter mutations (position −42 (C > T) and one carried mcr-1. The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The blaTEM–52 genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to E. clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic E. coli (ExPEC; 2.0%), avian pathogenic E. coli (APEC; 51.5%), and atypical enteropathogenic E. coli (EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health. The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal Escherichia spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred Escherichia spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST). In silico screening of WGS data of 99 isolates (98 E. coli and 1 E. fergusonii ) revealed bla SHV – 12 (32.3%), bla CTX – M – 1 (24.2%), and bla CMY – 2 (22.2%) as predominant ESBL/pAmpC types. Other types were bla SHV – 2 (1.0%), bla CTX – M – 2 / – 14 / – 15 (1.0/6.1/1.0%), and bla TEM – 52 (5.1%). Six isolates revealed AmpC-promoter mutations (position −42 (C > T) and one carried mcr-1 . The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The bla TEM – 52 genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to E . clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic E. coli (ExPEC; 2.0%), avian pathogenic E. coli (APEC; 51.5%), and atypical enteropathogenic E. coli (EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health. The role of livestock animals as a putative source of ESBL/pAmpC for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST). screening of WGS data of 99 isolates (98 and 1 ) revealed (32.3%), (24.2%), and (22.2%) as predominant ESBL/pAmpC types. Other types were (1.0%), (1.0/6.1/1.0%), and (5.1%). Six isolates revealed AmpC-promoter mutations (position -42 (C > T) and one carried . The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to . clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic (ExPEC; 2.0%), avian pathogenic (APEC; 51.5%), and atypical enteropathogenic (EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health. The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal Escherichia spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred Escherichia spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST). In silico screening of WGS data of 99 isolates (98 E. coli and 1 E. fergusonii) revealed bla SHV - 12 (32.3%), bla CTX - M - 1 (24.2%), and bla CMY - 2 (22.2%) as predominant ESBL/pAmpC types. Other types were bla SHV - 2 (1.0%), bla CTX - M - 2 / - 14 / - 15 (1.0/6.1/1.0%), and bla TEM - 52 (5.1%). Six isolates revealed AmpC-promoter mutations (position -42 (C > T) and one carried mcr-1. The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The bla TEM - 52 genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to E. clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic E. coli (ExPEC; 2.0%), avian pathogenic E. coli (APEC; 51.5%), and atypical enteropathogenic E. coli (EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health.The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993 commensal Escherichia spp. isolates were recovered from randomly collected fecal samples of healthy cattle, pigs and chickens in various abattoirs. One-hundred Escherichia spp. isolates (0.5% from cattle, 1.3% pigs, 8.0% chickens) fulfilled the criteria for cefotaxime and ceftazidime non-wildtype (EUCAST). In silico screening of WGS data of 99 isolates (98 E. coli and 1 E. fergusonii) revealed bla SHV - 12 (32.3%), bla CTX - M - 1 (24.2%), and bla CMY - 2 (22.2%) as predominant ESBL/pAmpC types. Other types were bla SHV - 2 (1.0%), bla CTX - M - 2 / - 14 / - 15 (1.0/6.1/1.0%), and bla TEM - 52 (5.1%). Six isolates revealed AmpC-promoter mutations (position -42 (C > T) and one carried mcr-1. The majority (91.3%) of ESBL/pAmpC genes were located on plasmids. SHV-12 was mainly (50%) encoded on IncI1α plasmids (pST-3/-26/-95), followed by IncX3 (12.5%) and IncK2 (3.1%). The bla TEM - 52 genes were located on IncI1α-pST-36 (60%) and IncX1 plasmids (20%). The dominant plasmid lineage among CTX-M-1 isolates was IncI1α (pST-3/-295/-317) (87.5%), followed by IncN-pST-1 (8.3%). CMY-2 was mostly identified on IncI1α (pST-12/-2) (54.5%) and IncK2 (31.8%) plasmids. Several plasmids revealed high similarity to published plasmids from human and animal Enterobacteriaceae. The isolates were assigned to phylogroups A/C (34.7/7.1%), B1 (27.6%), B2 (3.1%), D/F (9.2/10.2%), E (5.1%), and to E. clades (3.0%). With 51 known and 2 novel MLST types, a wide variety of STs was found, including STs previously observed in human isolates (ST10/38/117/131/648). ESBL/AmpC types or STs were rarely correlated with the geographic origin of the isolates or animal species. Virulence gene typing identified extraintestinal pathogenic E. coli (ExPEC; 2.0%), avian pathogenic E. coli (APEC; 51.5%), and atypical enteropathogenic E. coli (EPEC; 6.1%). In conclusion, the high diversity of STs and phylogenetic groups provides hardly any hint for clonal spread of single lineages but hints toward the dissemination of cephalosporin resistance genes in livestock via distinct, globally successful plasmid lineages. Even though a number of isolates could not be assigned to a distinct pathotype, our finding of combined multidrug-resistance and virulence in this facultative pathogen should be considered an additional threat to public health. |
| Author | de Jong, Anno El Garch, Farid Ewers, Christa Tiwari, Sumeet K. Semmler, Torsten Prenger-Berninghoff, Ellen Leidner, Ursula |
| AuthorAffiliation | 1 Department of Veterinary Medicine, Institute of Hygiene and Infectious Diseases of Animals, Justus Liebig University Giessen , Giessen , Germany 3 NG1 Microbial Genomics, Robert Koch Institute , Berlin , Germany 2 European Antimicrobial Susceptibility Surveillance in Animals (EASSA) Study Group, Executive Animal Health Study Center (CEESA) , Brussels , Belgium |
| AuthorAffiliation_xml | – name: 3 NG1 Microbial Genomics, Robert Koch Institute , Berlin , Germany – name: 2 European Antimicrobial Susceptibility Surveillance in Animals (EASSA) Study Group, Executive Animal Health Study Center (CEESA) , Brussels , Belgium – name: 1 Department of Veterinary Medicine, Institute of Hygiene and Infectious Diseases of Animals, Justus Liebig University Giessen , Giessen , Germany |
| Author_xml | – sequence: 1 givenname: Christa surname: Ewers fullname: Ewers, Christa – sequence: 2 givenname: Anno surname: de Jong fullname: de Jong, Anno – sequence: 3 givenname: Ellen surname: Prenger-Berninghoff fullname: Prenger-Berninghoff, Ellen – sequence: 4 givenname: Farid surname: El Garch fullname: El Garch, Farid – sequence: 5 givenname: Ursula surname: Leidner fullname: Leidner, Ursula – sequence: 6 givenname: Sumeet K. surname: Tiwari fullname: Tiwari, Sumeet K. – sequence: 7 givenname: Torsten surname: Semmler fullname: Semmler, Torsten |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33868190$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler. Copyright © 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler. 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler |
| Copyright_xml | – notice: Copyright © 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler. – notice: Copyright © 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler. 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler |
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| Keywords | AmpC pathotype virulence Escherichia coli livestock ESBL plasmid sequence type |
| Language | English |
| License | Copyright © 2021 Ewers, de Jong, Prenger-Berninghoff, El Garch, Leidner, Tiwari and Semmler. 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. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Nilton Lincopan, University of São Paulo, Brazil; Mohamed Salah Abbassi, Tunis El Manar University, Tunisia; Jorge Blanco, University of Santiago de Compostela, Spain Edited by: Edward Feil, University of Bath, United Kingdom This article was submitted to Antimicrobials, Resistance and Chemotherapy, a section of the journal Frontiers in Microbiology |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.3389/fmicb.2021.626774 |
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| PublicationDateYYYYMMDD | 2021-04-01 |
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| PublicationTitle | Frontiers in microbiology |
| PublicationTitleAlternate | Front Microbiol |
| PublicationYear | 2021 |
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| Snippet | The role of livestock animals as a putative source of ESBL/pAmpC
E. coli
for humans is a central issue of research. In a large-scale pan-European surveillance,... The role of livestock animals as a putative source of ESBL/pAmpC for humans is a central issue of research. In a large-scale pan-European surveillance, 2,993... The role of livestock animals as a putative source of ESBL/pAmpC E. coli for humans is a central issue of research. In a large-scale pan-European surveillance,... |
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| SubjectTerms | AmpC ESBL Escherichia coli livestock Microbiology sequence type virulence |
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| Title | Genomic Diversity and Virulence Potential of ESBL- and AmpC-β-Lactamase-Producing Escherichia coli Strains From Healthy Food Animals Across Europe |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33868190 https://www.proquest.com/docview/2515066165 https://pubmed.ncbi.nlm.nih.gov/PMC8047082 https://doaj.org/article/8aa414ae7a5f452e98c9aaa3d11d3b30 |
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