WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil

Detalhes bibliográficos
Autor(a) principal: Fuga, Bruna
Data de Publicação: 2022
Outros Autores: Sellera, Fábio P, Cerdeira, Louise, Esposito, Fernanda, Cardoso, Brenda, Fontana, Herrison, Moura, Quézia, Arias, Adriana Cardenas, Sano, Elder, Ribas, Rosineide M, Carvalho, Albalúcia C, Tognim, Maria Cristina B, Morais, Marcia Maria C de, Quaresma, Ana Judith Pires Garcia, Santana, Ângela Patrícia, Reis, Joice N, Pilonetto, Marcelo, Vespero, Eliana Carolina, Bonelli, Raquel R, Cerqueira, Aloysio M. F, Sincero, Thaís C. M, Lincopan, Nilton
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Digital do Instituto Evandro Chagas (Patuá)
Texto Completo: https://patua.iec.gov.br/handle/iec/4551
Resumo: The dissemination of carbapenem-resistant and third generation cephalosporin-resistant pathogens is a critical issue that is no longer restricted to hospital settings. The rapid spread of critical priority pathogens in Brazil is notably worrying, considering its continental dimension, the diversity of international trade, livestock production, and human travel. We conducted a nationwide genomic investigation under a One Health perspective that included Escherichia coli strains isolated from humans and nonhuman sources, over 45 years (1974-2019). One hundred sixty-seven genomes were analyzed extracting clinically relevant information (i.e., resistome, virulome, mobilome, sequence types [STs], and phylogenomic). The endemic status of extended-spectrum b-lactamase (ESBL)-positive strains carrying a wide diversity of blaCTX-M variants, and the growing number of colistin-resistant isolates carrying mcr-type genes was associated with the successful expansion of international ST10, ST38, ST115, ST131, ST354, ST410, ST648, ST517, and ST711 clones; phylogenetically related and shared between human and nonhuman hosts, and polluted aquatic environments. Otherwise, carbapenem-resistant ST48, ST90, ST155, ST167, ST224, ST349, ST457, ST648, ST707, ST744, ST774, and ST2509 clones from human host harbored blaKPC-2 and blaNDM-1 genes. A broad resistome to other clinically relevant antibiotics, hazardous heavy metals, disinfectants, and pesticides was further predicted. Wide virulome associated with invasion/adherence, exotoxin and siderophore production was related to phylogroup B2. The convergence of wide resistome and virulome has contributed to the persistence and rapid spread of international high-risk clones of critical priority E. coli at the human-animal-environmental interface, which must be considered a One Health challenge for a post-pandemic scenario. IMPORTANCE A One Health approach for antimicrobial resistance must integrate whole-genome sequencing surveillance data of critical priority pathogens from human, animal and environmental sources to track hot spots and routes of transmission and developing effective prevention and control strategies. As part of the Grand Challenges Explorations: New Approaches to Characterize the Global Burden of Antimicrobial Resistance Program, we present genomic data of WHO critical priority carbapenemase-resistant, ESBL-producing, and/or colistin-resistant Escherichia coli strains isolated from humans and nonhuman sources in Brazil, a country with continental proportions and high levels of antimicrobial resistance. The present study provided evidence of epidemiological and clinical interest, highlighting that the convergence of wide virulome and resistome has contributed to the persistence and rapid spread of international high-risk clones of E. coli at the human-animal-environmental interface, which must be considered a One Health threat that requires coordinated actions to reduce its incidence in humans and nonhuman hosts.
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spelling Fuga, BrunaSellera, Fábio PCerdeira, LouiseEsposito, FernandaCardoso, BrendaFontana, HerrisonMoura, QuéziaArias, Adriana CardenasSano, ElderRibas, Rosineide MCarvalho, Albalúcia CTognim, Maria Cristina BMorais, Marcia Maria C deQuaresma, Ana Judith Pires GarciaSantana, Ângela PatríciaReis, Joice NPilonetto, MarceloVespero, Eliana CarolinaBonelli, Raquel RCerqueira, Aloysio M. FSincero, Thaís C. MLincopan, Nilton2022-06-06T11:41:12Z2022-06-06T11:41:12Z2022FUGA, Bruna et al. WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil. Microbiology Spectrum, v. 10, n. 2, p. 1-18, Apr. 2022. DOI: https://doi.org/10.1128/spectrum.01256-21. Disponível em: http://patua.iec.gov.br/handle/iec/45512165-0497https://patua.iec.gov.br/handle/iec/455110.1128/spectrum.01256-21The dissemination of carbapenem-resistant and third generation cephalosporin-resistant pathogens is a critical issue that is no longer restricted to hospital settings. The rapid spread of critical priority pathogens in Brazil is notably worrying, considering its continental dimension, the diversity of international trade, livestock production, and human travel. We conducted a nationwide genomic investigation under a One Health perspective that included Escherichia coli strains isolated from humans and nonhuman sources, over 45 years (1974-2019). One hundred sixty-seven genomes were analyzed extracting clinically relevant information (i.e., resistome, virulome, mobilome, sequence types [STs], and phylogenomic). The endemic status of extended-spectrum b-lactamase (ESBL)-positive strains carrying a wide diversity of blaCTX-M variants, and the growing number of colistin-resistant isolates carrying mcr-type genes was associated with the successful expansion of international ST10, ST38, ST115, ST131, ST354, ST410, ST648, ST517, and ST711 clones; phylogenetically related and shared between human and nonhuman hosts, and polluted aquatic environments. Otherwise, carbapenem-resistant ST48, ST90, ST155, ST167, ST224, ST349, ST457, ST648, ST707, ST744, ST774, and ST2509 clones from human host harbored blaKPC-2 and blaNDM-1 genes. A broad resistome to other clinically relevant antibiotics, hazardous heavy metals, disinfectants, and pesticides was further predicted. Wide virulome associated with invasion/adherence, exotoxin and siderophore production was related to phylogroup B2. The convergence of wide resistome and virulome has contributed to the persistence and rapid spread of international high-risk clones of critical priority E. coli at the human-animal-environmental interface, which must be considered a One Health challenge for a post-pandemic scenario. IMPORTANCE A One Health approach for antimicrobial resistance must integrate whole-genome sequencing surveillance data of critical priority pathogens from human, animal and environmental sources to track hot spots and routes of transmission and developing effective prevention and control strategies. As part of the Grand Challenges Explorations: New Approaches to Characterize the Global Burden of Antimicrobial Resistance Program, we present genomic data of WHO critical priority carbapenemase-resistant, ESBL-producing, and/or colistin-resistant Escherichia coli strains isolated from humans and nonhuman sources in Brazil, a country with continental proportions and high levels of antimicrobial resistance. The present study provided evidence of epidemiological and clinical interest, highlighting that the convergence of wide virulome and resistome has contributed to the persistence and rapid spread of international high-risk clones of E. coli at the human-animal-environmental interface, which must be considered a One Health threat that requires coordinated actions to reduce its incidence in humans and nonhuman hosts.Bill and Melinda Gates Foundation, Grand Challenges Explorations Brazil–New approaches to characterize the global burden of antimicrobial resistance [grant OPP1193112], Conselho Nacional de Desenvolvimento Científico e Tecnológico [grants AMR 443819/2018-1, 433128/ 2018-6, and 312249/2017-9], Fundação de Amparo à Pesquisa do Estado de São Paulo [grant 2020/08224-9 and 2019/15578-4], and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior [grants 88887.358057/2019-00 and 1794306] are gratefully acknowledged. N.L. is a research fellow of CNPq [grant 314336/2021-4].University of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / University of São Paulo. Faculty of Pharmaceutical Sciences. Department of Clinical Analysis. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilOne Health Brazilian Resistance Project. São Paulo, SP, Brazil / University of São Paulo. School of Veterinary Medicine and Animal Science. Department of Internal Medicine. São Paulo, SP, Brazil / Metropolitan University of Santos. School of Veterinary Medicine. Santos, SP, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / Monash University. Central Clinical School. Department of Infectious Diseases. Melbourne, Australia / Liverpool School of Tropical Medicine. Department of Vector Biology. Liverpool, UKUniversity of São Paulo. Faculty of Pharmaceutical Sciences. Department of Clinical Analysis. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilUniversity of São Paulo. Faculty of Pharmaceutical Sciences. Department of Clinical Analysis. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, Brazil / Federal University of Grande Dourados. Faculty of Health Sciences. Dourados, MS, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilFederal University of Uberlândia. Institute of Biomedical Sciences. Laboratory of Molecular Microbiology. Uberlândia, MG, BrazilFederal University of Paraiba. Clinical Laboratory. João Pessoa, PB, BrazilState University of Maringá. School of Pharmacy. Maringá, PR, BrazilFederal University of Uberlândia. Institute of Biomedical Sciences. Laboratory of Molecular Microbiology. Uberlândia, MG, BrazilMinistério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, BrasilUniversity of Brasília. Faculty of Agronomy and Veterinary Medicine. Brasília, DF, BrazilFederal University of Bahia. Faculty of Pharmacy. Salvador, BA, BrazilCentral Laboratory of the State of Paraná. São Jose dos Pinhais, PR, BrazilState University of Londrina. Microbiology Laboratory of the University Hospital of Londrina. Londrina, PR, BrazilFederal University of Rio de Janeiro. Paulo de Góes Institute of Microbiology. Medical Microbiology Research Laboratory. Rio de Janeiro, RJ, BrazilFluminense Federal University. Biomedical Institute. Laboratory of Enteropathogens, Veterinary and Food Microbiology. Niterói, RJ, BrazilFederal University of Santa Catarina. Department of Clinical Analysis. Laboratory of Applied Molecular Microbiology. Florianópolis, SC, BrazilUniversity of São Paulo. Instituto de Ciências Biomédicas. Department of Microbiology. São Paulo, SP, Brazil / University of São Paulo. Faculty of Pharmaceutical Sciences. Department of Clinical Analysis. São Paulo, SP, Brazil / One Health Brazilian Resistance Project. São Paulo, SP, BrazilengAmerican Society for MicrobiologyWHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazilinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleEscherichia coli / patogenicidadeEscherichia coli / efeitos dos fármacosVigilância em Saúde PúblicaSaúde ÚnicaEnterobacteriáceas Resistentes a Carbapenêmicosinfo:eu-repo/semantics/openAccessreponame:Repositório Digital do Instituto Evandro Chagas (Patuá)instname:Instituto Evandro Chagas (IEC)instacron:IECORIGINALWHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil.pdfWHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil.pdfapplication/pdf5455662https://patua.iec.gov.br/bitstreams/8e0d7c15-9d8b-4421-aa64-829fbe333a34/download38d5cb7160dcbc6d8c4bbfc2e7351185MD51LICENSElicense.txtlicense.txttext/plain; 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dc.title.pt_BR.fl_str_mv WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
title WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
spellingShingle WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
Fuga, Bruna
Escherichia coli / patogenicidade
Escherichia coli / efeitos dos fármacos
Vigilância em Saúde Pública
Saúde Única
Enterobacteriáceas Resistentes a Carbapenêmicos
title_short WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
title_full WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
title_fullStr WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
title_full_unstemmed WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
title_sort WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil
author Fuga, Bruna
author_facet Fuga, Bruna
Sellera, Fábio P
Cerdeira, Louise
Esposito, Fernanda
Cardoso, Brenda
Fontana, Herrison
Moura, Quézia
Arias, Adriana Cardenas
Sano, Elder
Ribas, Rosineide M
Carvalho, Albalúcia C
Tognim, Maria Cristina B
Morais, Marcia Maria C de
Quaresma, Ana Judith Pires Garcia
Santana, Ângela Patrícia
Reis, Joice N
Pilonetto, Marcelo
Vespero, Eliana Carolina
Bonelli, Raquel R
Cerqueira, Aloysio M. F
Sincero, Thaís C. M
Lincopan, Nilton
author_role author
author2 Sellera, Fábio P
Cerdeira, Louise
Esposito, Fernanda
Cardoso, Brenda
Fontana, Herrison
Moura, Quézia
Arias, Adriana Cardenas
Sano, Elder
Ribas, Rosineide M
Carvalho, Albalúcia C
Tognim, Maria Cristina B
Morais, Marcia Maria C de
Quaresma, Ana Judith Pires Garcia
Santana, Ângela Patrícia
Reis, Joice N
Pilonetto, Marcelo
Vespero, Eliana Carolina
Bonelli, Raquel R
Cerqueira, Aloysio M. F
Sincero, Thaís C. M
Lincopan, Nilton
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Fuga, Bruna
Sellera, Fábio P
Cerdeira, Louise
Esposito, Fernanda
Cardoso, Brenda
Fontana, Herrison
Moura, Quézia
Arias, Adriana Cardenas
Sano, Elder
Ribas, Rosineide M
Carvalho, Albalúcia C
Tognim, Maria Cristina B
Morais, Marcia Maria C de
Quaresma, Ana Judith Pires Garcia
Santana, Ângela Patrícia
Reis, Joice N
Pilonetto, Marcelo
Vespero, Eliana Carolina
Bonelli, Raquel R
Cerqueira, Aloysio M. F
Sincero, Thaís C. M
Lincopan, Nilton
dc.subject.decsPrimary.pt_BR.fl_str_mv Escherichia coli / patogenicidade
Escherichia coli / efeitos dos fármacos
Vigilância em Saúde Pública
Saúde Única
Enterobacteriáceas Resistentes a Carbapenêmicos
topic Escherichia coli / patogenicidade
Escherichia coli / efeitos dos fármacos
Vigilância em Saúde Pública
Saúde Única
Enterobacteriáceas Resistentes a Carbapenêmicos
description The dissemination of carbapenem-resistant and third generation cephalosporin-resistant pathogens is a critical issue that is no longer restricted to hospital settings. The rapid spread of critical priority pathogens in Brazil is notably worrying, considering its continental dimension, the diversity of international trade, livestock production, and human travel. We conducted a nationwide genomic investigation under a One Health perspective that included Escherichia coli strains isolated from humans and nonhuman sources, over 45 years (1974-2019). One hundred sixty-seven genomes were analyzed extracting clinically relevant information (i.e., resistome, virulome, mobilome, sequence types [STs], and phylogenomic). The endemic status of extended-spectrum b-lactamase (ESBL)-positive strains carrying a wide diversity of blaCTX-M variants, and the growing number of colistin-resistant isolates carrying mcr-type genes was associated with the successful expansion of international ST10, ST38, ST115, ST131, ST354, ST410, ST648, ST517, and ST711 clones; phylogenetically related and shared between human and nonhuman hosts, and polluted aquatic environments. Otherwise, carbapenem-resistant ST48, ST90, ST155, ST167, ST224, ST349, ST457, ST648, ST707, ST744, ST774, and ST2509 clones from human host harbored blaKPC-2 and blaNDM-1 genes. A broad resistome to other clinically relevant antibiotics, hazardous heavy metals, disinfectants, and pesticides was further predicted. Wide virulome associated with invasion/adherence, exotoxin and siderophore production was related to phylogroup B2. The convergence of wide resistome and virulome has contributed to the persistence and rapid spread of international high-risk clones of critical priority E. coli at the human-animal-environmental interface, which must be considered a One Health challenge for a post-pandemic scenario. IMPORTANCE A One Health approach for antimicrobial resistance must integrate whole-genome sequencing surveillance data of critical priority pathogens from human, animal and environmental sources to track hot spots and routes of transmission and developing effective prevention and control strategies. As part of the Grand Challenges Explorations: New Approaches to Characterize the Global Burden of Antimicrobial Resistance Program, we present genomic data of WHO critical priority carbapenemase-resistant, ESBL-producing, and/or colistin-resistant Escherichia coli strains isolated from humans and nonhuman sources in Brazil, a country with continental proportions and high levels of antimicrobial resistance. The present study provided evidence of epidemiological and clinical interest, highlighting that the convergence of wide virulome and resistome has contributed to the persistence and rapid spread of international high-risk clones of E. coli at the human-animal-environmental interface, which must be considered a One Health threat that requires coordinated actions to reduce its incidence in humans and nonhuman hosts.
publishDate 2022
dc.date.accessioned.fl_str_mv 2022-06-06T11:41:12Z
dc.date.available.fl_str_mv 2022-06-06T11:41:12Z
dc.date.issued.fl_str_mv 2022
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.citation.fl_str_mv FUGA, Bruna et al. WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil. Microbiology Spectrum, v. 10, n. 2, p. 1-18, Apr. 2022. DOI: https://doi.org/10.1128/spectrum.01256-21. Disponível em: http://patua.iec.gov.br/handle/iec/4551
dc.identifier.uri.fl_str_mv https://patua.iec.gov.br/handle/iec/4551
dc.identifier.issn.-.fl_str_mv 2165-0497
dc.identifier.doi.-.fl_str_mv 10.1128/spectrum.01256-21
identifier_str_mv FUGA, Bruna et al. WHO critical priority Escherichia coli as one health challenge for a post-pandemic scenario: genomic surveillance and analysis of current trends in Brazil. Microbiology Spectrum, v. 10, n. 2, p. 1-18, Apr. 2022. DOI: https://doi.org/10.1128/spectrum.01256-21. Disponível em: http://patua.iec.gov.br/handle/iec/4551
2165-0497
10.1128/spectrum.01256-21
url https://patua.iec.gov.br/handle/iec/4551
dc.language.iso.fl_str_mv eng
language eng
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eu_rights_str_mv openAccess
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repository.name.fl_str_mv Repositório Digital do Instituto Evandro Chagas (Patuá) - Instituto Evandro Chagas (IEC)
repository.mail.fl_str_mv clariceneta@iec.gov.br || Biblioteca@iec.gov.br
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