Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador

Liseth Salinas; Fernanda Loayza; Paúl Cárdenas; Carlos Saraiva; Timothy J. Johnson; Heather Amato; Jay P. Graham; Gabriel Trueba

doi:10.1289/EHP7729

Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador

Liseth Salinas, Fernanda Loayza, Paúl Cárdenas, Carlos Saraiva, Timothy J. Johnson, Heather Amato, Jay P. Graham, Gabriel Trueba

Veterinary and Biomedical Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

BACKGROUND: There is a significant gap in our understanding of the sources of multidrug-resistant bacteria and resistance genes in community set-tings where human–animal interfaces exist. OBJECTIVES: This study characterized the relationship of third-generation cephalosporin-resistant Escherichia coli (3GCR-EC) isolated from animal feces in the environment and child feces based on phenotypic antimicrobial resistance (AMR) and whole genome sequencing (WGS). METHODS: We examined 3GCR-EC isolated from environmental fecal samples of domestic animals and child fecal samples in Ecuador. We analyzed phenotypic and genotypic AMR, as well as clonal relationships (CRs) based on pairwise single-nucleotide polymorphisms (SNPs) analysis of 3GCR-EC core genomes. CRs were defined as isolates with fewer than 100 different SNPs. RESULTS: A total of 264 3GCR-EC isolates from children (n = 21), dogs (n = 20), and chickens (n = 18) living in the same region of Quito, Ecuador, were identified. We detected 16 CRs total, which were found between 7 children and 5 domestic animals (5 CRs) and between 19 domestic animals (11 CRs). We observed that several clonally related 3GCR-EC isolates had acquired different plasmids and AMR genes. Most CRs were observed in different homes (n = 14) at relatively large distances. Isolates from children and domestic animals shared the same bla_CTX-M allelic variants, and the most prevalent were bla_CTX-M-55 and bla_CTX-M-65, which were found in isolates from children, dogs, and chickens. DISCUSSION: This study provides evidence of highly dynamic horizontal transfer of AMR genes and mobile genetic elements (MGEs) in the E. coli community and shows that some 3GCR-EC and (extended-spectrum β-lactamase) ESBL genes may have moved relatively large distances among domestic animals and children in semirural communities near Quito, Ecuador. Child–animal contact and the presence of domestic animal feces in the environment potentially serve as important sources of drug-resistant bacteria and ESBL genes.

Original language	English (US)
Article number	027007
Pages (from-to)	1-10
Number of pages	10
Journal	Environmental health perspectives
Volume	129
Issue number	2
DOIs	https://doi.org/10.1289/EHP7729
State	Published - 2021

Bibliographical note

Funding Information:
Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (NIH) under Award Number R01AI135118. P.C. is funded by NIH FIC D43TW010540 Global Health Equity Scholars. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Publisher Copyright:
© 2021, Public Health Services, US Dept of Health and Human Services. All rights reserved.

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Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador. / Salinas, Liseth; Loayza, Fernanda; Cárdenas, Paúl; Saraiva, Carlos; Johnson, Timothy J.; Amato, Heather; Graham, Jay P.; Trueba, Gabriel.

In: Environmental health perspectives, Vol. 129, No. 2, 027007, 2021, p. 1-10.

Research output: Contribution to journal › Article › peer-review

Salinas, Liseth ; Loayza, Fernanda ; Cárdenas, Paúl ; Saraiva, Carlos ; Johnson, Timothy J. ; Amato, Heather ; Graham, Jay P. ; Trueba, Gabriel. / Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador. In: Environmental health perspectives. 2021 ; Vol. 129, No. 2. pp. 1-10.

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title = "Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador",

abstract = "BACKGROUND: There is a significant gap in our understanding of the sources of multidrug-resistant bacteria and resistance genes in community set-tings where human–animal interfaces exist. OBJECTIVES: This study characterized the relationship of third-generation cephalosporin-resistant Escherichia coli (3GCR-EC) isolated from animal feces in the environment and child feces based on phenotypic antimicrobial resistance (AMR) and whole genome sequencing (WGS). METHODS: We examined 3GCR-EC isolated from environmental fecal samples of domestic animals and child fecal samples in Ecuador. We analyzed phenotypic and genotypic AMR, as well as clonal relationships (CRs) based on pairwise single-nucleotide polymorphisms (SNPs) analysis of 3GCR-EC core genomes. CRs were defined as isolates with fewer than 100 different SNPs. RESULTS: A total of 264 3GCR-EC isolates from children (n = 21), dogs (n = 20), and chickens (n = 18) living in the same region of Quito, Ecuador, were identified. We detected 16 CRs total, which were found between 7 children and 5 domestic animals (5 CRs) and between 19 domestic animals (11 CRs). We observed that several clonally related 3GCR-EC isolates had acquired different plasmids and AMR genes. Most CRs were observed in different homes (n = 14) at relatively large distances. Isolates from children and domestic animals shared the same blaCTX-M allelic variants, and the most prevalent were blaCTX-M-55 and blaCTX-M-65, which were found in isolates from children, dogs, and chickens. DISCUSSION: This study provides evidence of highly dynamic horizontal transfer of AMR genes and mobile genetic elements (MGEs) in the E. coli community and shows that some 3GCR-EC and (extended-spectrum β-lactamase) ESBL genes may have moved relatively large distances among domestic animals and children in semirural communities near Quito, Ecuador. Child–animal contact and the presence of domestic animal feces in the environment potentially serve as important sources of drug-resistant bacteria and ESBL genes.",

author = "Liseth Salinas and Fernanda Loayza and Pa{\'u}l C{\'a}rdenas and Carlos Saraiva and Johnson, {Timothy J.} and Heather Amato and Graham, {Jay P.} and Gabriel Trueba",

note = "Funding Information: Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (NIH) under Award Number R01AI135118. P.C. is funded by NIH FIC D43TW010540 Global Health Equity Scholars. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} 2021, Public Health Services, US Dept of Health and Human Services. All rights reserved.",

year = "2021",

doi = "10.1289/EHP7729",

language = "English (US)",

volume = "129",

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AU - Salinas, Liseth

AU - Loayza, Fernanda

AU - Cárdenas, Paúl

AU - Saraiva, Carlos

AU - Johnson, Timothy J.

AU - Amato, Heather

AU - Graham, Jay P.

AU - Trueba, Gabriel

N1 - Funding Information: Research reported in this publication was supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (NIH) under Award Number R01AI135118. P.C. is funded by NIH FIC D43TW010540 Global Health Equity Scholars. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: © 2021, Public Health Services, US Dept of Health and Human Services. All rights reserved.

PY - 2021

Y1 - 2021

N2 - BACKGROUND: There is a significant gap in our understanding of the sources of multidrug-resistant bacteria and resistance genes in community set-tings where human–animal interfaces exist. OBJECTIVES: This study characterized the relationship of third-generation cephalosporin-resistant Escherichia coli (3GCR-EC) isolated from animal feces in the environment and child feces based on phenotypic antimicrobial resistance (AMR) and whole genome sequencing (WGS). METHODS: We examined 3GCR-EC isolated from environmental fecal samples of domestic animals and child fecal samples in Ecuador. We analyzed phenotypic and genotypic AMR, as well as clonal relationships (CRs) based on pairwise single-nucleotide polymorphisms (SNPs) analysis of 3GCR-EC core genomes. CRs were defined as isolates with fewer than 100 different SNPs. RESULTS: A total of 264 3GCR-EC isolates from children (n = 21), dogs (n = 20), and chickens (n = 18) living in the same region of Quito, Ecuador, were identified. We detected 16 CRs total, which were found between 7 children and 5 domestic animals (5 CRs) and between 19 domestic animals (11 CRs). We observed that several clonally related 3GCR-EC isolates had acquired different plasmids and AMR genes. Most CRs were observed in different homes (n = 14) at relatively large distances. Isolates from children and domestic animals shared the same blaCTX-M allelic variants, and the most prevalent were blaCTX-M-55 and blaCTX-M-65, which were found in isolates from children, dogs, and chickens. DISCUSSION: This study provides evidence of highly dynamic horizontal transfer of AMR genes and mobile genetic elements (MGEs) in the E. coli community and shows that some 3GCR-EC and (extended-spectrum β-lactamase) ESBL genes may have moved relatively large distances among domestic animals and children in semirural communities near Quito, Ecuador. Child–animal contact and the presence of domestic animal feces in the environment potentially serve as important sources of drug-resistant bacteria and ESBL genes.

AB - BACKGROUND: There is a significant gap in our understanding of the sources of multidrug-resistant bacteria and resistance genes in community set-tings where human–animal interfaces exist. OBJECTIVES: This study characterized the relationship of third-generation cephalosporin-resistant Escherichia coli (3GCR-EC) isolated from animal feces in the environment and child feces based on phenotypic antimicrobial resistance (AMR) and whole genome sequencing (WGS). METHODS: We examined 3GCR-EC isolated from environmental fecal samples of domestic animals and child fecal samples in Ecuador. We analyzed phenotypic and genotypic AMR, as well as clonal relationships (CRs) based on pairwise single-nucleotide polymorphisms (SNPs) analysis of 3GCR-EC core genomes. CRs were defined as isolates with fewer than 100 different SNPs. RESULTS: A total of 264 3GCR-EC isolates from children (n = 21), dogs (n = 20), and chickens (n = 18) living in the same region of Quito, Ecuador, were identified. We detected 16 CRs total, which were found between 7 children and 5 domestic animals (5 CRs) and between 19 domestic animals (11 CRs). We observed that several clonally related 3GCR-EC isolates had acquired different plasmids and AMR genes. Most CRs were observed in different homes (n = 14) at relatively large distances. Isolates from children and domestic animals shared the same blaCTX-M allelic variants, and the most prevalent were blaCTX-M-55 and blaCTX-M-65, which were found in isolates from children, dogs, and chickens. DISCUSSION: This study provides evidence of highly dynamic horizontal transfer of AMR genes and mobile genetic elements (MGEs) in the E. coli community and shows that some 3GCR-EC and (extended-spectrum β-lactamase) ESBL genes may have moved relatively large distances among domestic animals and children in semirural communities near Quito, Ecuador. Child–animal contact and the presence of domestic animal feces in the environment potentially serve as important sources of drug-resistant bacteria and ESBL genes.

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Environmental spread of extended spectrum beta-lactamase (Esbl) producing escherichia coli and esbl genes among children and domestic animals in Ecuador

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Bibliographical note

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