Exploring the bacteriome and resistome of humans and food-producing animals in Brazil
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , , , , , , , , , , , , , , , , , , |
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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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 |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
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 |
eu_rights_str_mv |
openAccess |
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) instname:Instituto Evandro Chagas (IEC) instacron:IEC |
instname_str |
Instituto Evandro Chagas (IEC) |
instacron_str |
IEC |
institution |
IEC |
reponame_str |
Repositório Digital do Instituto Evandro Chagas (Patuá) |
collection |
Repositório Digital do Instituto Evandro Chagas (Patuá) |
bitstream.url.fl_str_mv |
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bitstream.checksum.fl_str_mv |
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bitstream.checksumAlgorithm.fl_str_mv |
MD5 MD5 MD5 MD5 |
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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1787533072110977024 |