Exploring the bacteriome and resistome of humans and food-producing animals in Brazil

Detalhes bibliográficos
Autor(a) principal: Carvalho, Fabíola Marques de
Data de Publicação: 2022
Outros Autores: Valiatti, Tiago Barcelos, Santos, Fernanda Fernandes, Silveira, Alessandro Conrado de Oliveira, Guimarães, Ana Paula C, Gerber, Alexandra Lehmkuhl, Souza, Cintya de Oliveira, Corsi, Dandara Cassu, Brasiliense, Danielle Murici, Castelo-Branco, Débora de Souza Collares Maia, Anzai, Eleine Kuroki, Bessa Neto, Francisco Ozório, Guedes, Glaucia Morgana de Mello, Souza, Gleyce Hellen de Almeida de, Lemos, Leandro Nascimento, Ferraz, Lúcio Fábio Caldas, Bahia, Márcia de Nazaré Miranda, Vaz, Márcia Soares Mattos, Silva, Ramon Giovani Brandão da, Veiga, Ruanita, Simionatto, Simone, Monteiro, Walter Aparecido Pimentel, Lima, William Alencar de Oliveira, Kiffer, Carlos Roberto Veiga, Pignatari, Antonio Carlos Campos, Cayô, Rodrigo, Vasconcelos, Ana Tereza Ribeiro de, Gales, Ana Cristina
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/4662
Resumo: The epidemiology of antimicrobial resistance (AMR) is complex, with multiple interfaces (human-animal-environment). In this context, One Health surveillance is essential for understanding the distribution of microorganisms and antimicrobial resistance genes (ARGs). This report describes a multicentric study undertaken to evaluate the bacterial communities and resistomes of food-producing animals (cattle, poultry, and swine) and healthy humans sampled simultaneously from five Brazilian regions. Metagenomic analysis showed that a total of 21,029 unique species were identified in 107 rectal swabs collected from distinct hosts, the highest numbers of which belonged to the domain Bacteria, mainly Ruminiclostridium spp. and Bacteroides spp., and the order Enterobacterales. We detected 405 ARGs for 12 distinct antimicrobial classes. Genes encoding antibiotic-modifying enzymes were the most frequent, followed by genes related to target alteration and efflux systems. Interestingly, carbapenemase-encoding genes such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1 were identified in distinct hosts. Our results revealed that, in general, the bacterial communities from humans were present in isolated clusters, except for the Northeastern region, where an overlap of the bacterial species from humans and food-producing animals was observed. Additionally, a large resistome was observed among all analyzed hosts, with emphasis on the presence of carbapenemase-encoding genes not previously reported in Latin America. IMPORTANCE Humans and food production animals have been reported to be important reservoirs of antimicrobial resistance (AMR) genes (ARGs). The frequency of these multidrug-resistant (MDR) bacteria tends to be higher in low- and middle-income countries (LMICs), due mainly to a lack of public health policies. Although studies on AMR in humans or animals have been carried out in Brazil, this is the first multicenter study that simultaneously collected rectal swabs from humans and food-producing animals for metagenomics. Our results indicate high microbial diversity among all analyzed hosts, and several ARGs for different antimicrobial classes were also found. As far as we know, we have detected for the first time ARGs encoding carbapenemases, such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1, in Latin America. Thus, our results support the importance of metagenomics as a tool to track the colonization of food-producing animals and humans by antimicrobial-resistant bacteria. In addition, a network surveillance system called GUARANI, created for this study, is ready to be expanded and to collect additional data.
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spelling Carvalho, Fabíola Marques deValiatti, Tiago BarcelosSantos, Fernanda FernandesSilveira, Alessandro Conrado de OliveiraGuimarães, Ana Paula CGerber, Alexandra LehmkuhlSouza, Cintya de OliveiraCorsi, Dandara CassuBrasiliense, Danielle MuriciCastelo-Branco, Débora de Souza Collares MaiaAnzai, Eleine KurokiBessa Neto, Francisco OzórioGuedes, Glaucia Morgana de MelloSouza, Gleyce Hellen de Almeida deLemos, Leandro NascimentoFerraz, Lúcio Fábio CaldasBahia, Márcia de Nazaré MirandaVaz, Márcia Soares MattosSilva, Ramon Giovani Brandão daVeiga, RuanitaSimionatto, SimoneMonteiro, Walter Aparecido PimentelLima, William Alencar de OliveiraKiffer, Carlos Roberto VeigaPignatari, Antonio Carlos CamposCayô, RodrigoVasconcelos, Ana Tereza Ribeiro deGales, Ana Cristina2022-09-13T11:17:35Z2022-09-13T11:17:35Z2022CARVALHO, Fabíola Marques de et al. Exploring the bacteriome and resistome of humans and food-producing animals in Brazil. Microbiology Spectrum, v. xx, n. e0056522, 2022. DOI: https://doi.org/10.1128/spectrum.00565-22. Disponível em: http://patua.iec.gov.br/handle/iec/46622165-0497https://patua.iec.gov.br/handle/iec/466210.1128/spectrum.00565-22The epidemiology of antimicrobial resistance (AMR) is complex, with multiple interfaces (human-animal-environment). In this context, One Health surveillance is essential for understanding the distribution of microorganisms and antimicrobial resistance genes (ARGs). This report describes a multicentric study undertaken to evaluate the bacterial communities and resistomes of food-producing animals (cattle, poultry, and swine) and healthy humans sampled simultaneously from five Brazilian regions. Metagenomic analysis showed that a total of 21,029 unique species were identified in 107 rectal swabs collected from distinct hosts, the highest numbers of which belonged to the domain Bacteria, mainly Ruminiclostridium spp. and Bacteroides spp., and the order Enterobacterales. We detected 405 ARGs for 12 distinct antimicrobial classes. Genes encoding antibiotic-modifying enzymes were the most frequent, followed by genes related to target alteration and efflux systems. Interestingly, carbapenemase-encoding genes such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1 were identified in distinct hosts. Our results revealed that, in general, the bacterial communities from humans were present in isolated clusters, except for the Northeastern region, where an overlap of the bacterial species from humans and food-producing animals was observed. Additionally, a large resistome was observed among all analyzed hosts, with emphasis on the presence of carbapenemase-encoding genes not previously reported in Latin America. IMPORTANCE Humans and food production animals have been reported to be important reservoirs of antimicrobial resistance (AMR) genes (ARGs). The frequency of these multidrug-resistant (MDR) bacteria tends to be higher in low- and middle-income countries (LMICs), due mainly to a lack of public health policies. Although studies on AMR in humans or animals have been carried out in Brazil, this is the first multicenter study that simultaneously collected rectal swabs from humans and food-producing animals for metagenomics. Our results indicate high microbial diversity among all analyzed hosts, and several ARGs for different antimicrobial classes were also found. As far as we know, we have detected for the first time ARGs encoding carbapenemases, such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1, in Latin America. Thus, our results support the importance of metagenomics as a tool to track the colonization of food-producing animals and humans by antimicrobial-resistant bacteria. In addition, a network surveillance system called GUARANI, created for this study, is ready to be expanded and to collect additional data.National Council for Science and Technological Development (CNPq) and the Bill & Melinda Gates Foundation (process numbers 402659/2018-0, 443805/2018-0, and OPP1193112); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); CNPq (process number 312066/2019-8), CNPq (307145/2021-2); FAPERJ (E-26/201.046/2022)National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Regional University of Blumenau. Blumenau, SC, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Federal University of Ceará. Postgraduate Program in Medical Microbiology. Group of Applied Medical Microbiology. Fortaleza, CE, Brazil.Regional University of Blumenau. Blumenau, SC, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.Federal University of Ceará. Postgraduate Program in Medical Microbiology. Group of Applied Medical Microbiology. Fortaleza, CE, Brazil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.University São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.University São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. 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dc.title.pt_BR.fl_str_mv Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
title Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
spellingShingle Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
Carvalho, Fabíola Marques de
Análise de Alimentos
Antibacterianos / análise
Produção de Alimentos
Alimentos Industrializados
Genes MDR
Metagenômica
Vigilância Sanitária de Produtos
Estudo Multicêntrico
title_short Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
title_full Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
title_fullStr Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
title_full_unstemmed Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
title_sort Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
author Carvalho, Fabíola Marques de
author_facet Carvalho, Fabíola Marques de
Valiatti, Tiago Barcelos
Santos, Fernanda Fernandes
Silveira, Alessandro Conrado de Oliveira
Guimarães, Ana Paula C
Gerber, Alexandra Lehmkuhl
Souza, Cintya de Oliveira
Corsi, Dandara Cassu
Brasiliense, Danielle Murici
Castelo-Branco, Débora de Souza Collares Maia
Anzai, Eleine Kuroki
Bessa Neto, Francisco Ozório
Guedes, Glaucia Morgana de Mello
Souza, Gleyce Hellen de Almeida de
Lemos, Leandro Nascimento
Ferraz, Lúcio Fábio Caldas
Bahia, Márcia de Nazaré Miranda
Vaz, Márcia Soares Mattos
Silva, Ramon Giovani Brandão da
Veiga, Ruanita
Simionatto, Simone
Monteiro, Walter Aparecido Pimentel
Lima, William Alencar de Oliveira
Kiffer, Carlos Roberto Veiga
Pignatari, Antonio Carlos Campos
Cayô, Rodrigo
Vasconcelos, Ana Tereza Ribeiro de
Gales, Ana Cristina
author_role author
author2 Valiatti, Tiago Barcelos
Santos, Fernanda Fernandes
Silveira, Alessandro Conrado de Oliveira
Guimarães, Ana Paula C
Gerber, Alexandra Lehmkuhl
Souza, Cintya de Oliveira
Corsi, Dandara Cassu
Brasiliense, Danielle Murici
Castelo-Branco, Débora de Souza Collares Maia
Anzai, Eleine Kuroki
Bessa Neto, Francisco Ozório
Guedes, Glaucia Morgana de Mello
Souza, Gleyce Hellen de Almeida de
Lemos, Leandro Nascimento
Ferraz, Lúcio Fábio Caldas
Bahia, Márcia de Nazaré Miranda
Vaz, Márcia Soares Mattos
Silva, Ramon Giovani Brandão da
Veiga, Ruanita
Simionatto, Simone
Monteiro, Walter Aparecido Pimentel
Lima, William Alencar de Oliveira
Kiffer, Carlos Roberto Veiga
Pignatari, Antonio Carlos Campos
Cayô, Rodrigo
Vasconcelos, Ana Tereza Ribeiro de
Gales, Ana Cristina
author2_role author
author
author
author
author
author
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 Carvalho, Fabíola Marques de
Valiatti, Tiago Barcelos
Santos, Fernanda Fernandes
Silveira, Alessandro Conrado de Oliveira
Guimarães, Ana Paula C
Gerber, Alexandra Lehmkuhl
Souza, Cintya de Oliveira
Corsi, Dandara Cassu
Brasiliense, Danielle Murici
Castelo-Branco, Débora de Souza Collares Maia
Anzai, Eleine Kuroki
Bessa Neto, Francisco Ozório
Guedes, Glaucia Morgana de Mello
Souza, Gleyce Hellen de Almeida de
Lemos, Leandro Nascimento
Ferraz, Lúcio Fábio Caldas
Bahia, Márcia de Nazaré Miranda
Vaz, Márcia Soares Mattos
Silva, Ramon Giovani Brandão da
Veiga, Ruanita
Simionatto, Simone
Monteiro, Walter Aparecido Pimentel
Lima, William Alencar de Oliveira
Kiffer, Carlos Roberto Veiga
Pignatari, Antonio Carlos Campos
Cayô, Rodrigo
Vasconcelos, Ana Tereza Ribeiro de
Gales, Ana Cristina
dc.subject.decsPrimary.pt_BR.fl_str_mv Análise de Alimentos
Antibacterianos / análise
Produção de Alimentos
Alimentos Industrializados
Genes MDR
Metagenômica
Vigilância Sanitária de Produtos
Estudo Multicêntrico
topic Análise de Alimentos
Antibacterianos / análise
Produção de Alimentos
Alimentos Industrializados
Genes MDR
Metagenômica
Vigilância Sanitária de Produtos
Estudo Multicêntrico
description The epidemiology of antimicrobial resistance (AMR) is complex, with multiple interfaces (human-animal-environment). In this context, One Health surveillance is essential for understanding the distribution of microorganisms and antimicrobial resistance genes (ARGs). This report describes a multicentric study undertaken to evaluate the bacterial communities and resistomes of food-producing animals (cattle, poultry, and swine) and healthy humans sampled simultaneously from five Brazilian regions. Metagenomic analysis showed that a total of 21,029 unique species were identified in 107 rectal swabs collected from distinct hosts, the highest numbers of which belonged to the domain Bacteria, mainly Ruminiclostridium spp. and Bacteroides spp., and the order Enterobacterales. We detected 405 ARGs for 12 distinct antimicrobial classes. Genes encoding antibiotic-modifying enzymes were the most frequent, followed by genes related to target alteration and efflux systems. Interestingly, carbapenemase-encoding genes such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1 were identified in distinct hosts. Our results revealed that, in general, the bacterial communities from humans were present in isolated clusters, except for the Northeastern region, where an overlap of the bacterial species from humans and food-producing animals was observed. Additionally, a large resistome was observed among all analyzed hosts, with emphasis on the presence of carbapenemase-encoding genes not previously reported in Latin America. IMPORTANCE Humans and food production animals have been reported to be important reservoirs of antimicrobial resistance (AMR) genes (ARGs). The frequency of these multidrug-resistant (MDR) bacteria tends to be higher in low- and middle-income countries (LMICs), due mainly to a lack of public health policies. Although studies on AMR in humans or animals have been carried out in Brazil, this is the first multicenter study that simultaneously collected rectal swabs from humans and food-producing animals for metagenomics. Our results indicate high microbial diversity among all analyzed hosts, and several ARGs for different antimicrobial classes were also found. As far as we know, we have detected for the first time ARGs encoding carbapenemases, such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1, in Latin America. Thus, our results support the importance of metagenomics as a tool to track the colonization of food-producing animals and humans by antimicrobial-resistant bacteria. In addition, a network surveillance system called GUARANI, created for this study, is ready to be expanded and to collect additional data.
publishDate 2022
dc.date.accessioned.fl_str_mv 2022-09-13T11:17:35Z
dc.date.available.fl_str_mv 2022-09-13T11:17:35Z
dc.date.issued.fl_str_mv 2022
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
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dc.identifier.citation.fl_str_mv CARVALHO, Fabíola Marques de et al. Exploring the bacteriome and resistome of humans and food-producing animals in Brazil. Microbiology Spectrum, v. xx, n. e0056522, 2022. DOI: https://doi.org/10.1128/spectrum.00565-22. Disponível em: http://patua.iec.gov.br/handle/iec/4662
dc.identifier.uri.fl_str_mv https://patua.iec.gov.br/handle/iec/4662
dc.identifier.issn.-.fl_str_mv 2165-0497
dc.identifier.doi.pt_BR.fl_str_mv 10.1128/spectrum.00565-22
identifier_str_mv CARVALHO, Fabíola Marques de et al. Exploring the bacteriome and resistome of humans and food-producing animals in Brazil. Microbiology Spectrum, v. xx, n. e0056522, 2022. DOI: https://doi.org/10.1128/spectrum.00565-22. Disponível em: http://patua.iec.gov.br/handle/iec/4662
2165-0497
10.1128/spectrum.00565-22
url https://patua.iec.gov.br/handle/iec/4662
dc.language.iso.fl_str_mv eng
language eng
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
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dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositório Digital do Instituto Evandro Chagas (Patuá)
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institution IEC
reponame_str Repositório Digital do Instituto Evandro Chagas (Patuá)
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