Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique

ABSTRACT Increasing demand for poultry has spurred poultry production in low- and middle-income countries like Mozambique. Poultry may be an important source of foodborne, antimicrobial-resistant bacteria to consumers in settings with limited water, sanitation, and hygiene infrastructure. The Chicke...

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Main Authors: Natalie Olson, Frederica Lamar, Hermógenes Mucache, José Fafetine, Joaquim Saíde, Amélia Milisse, Denise R. A. Brito, Kelsey J. Jesser, Karen Levy, Matthew C. Freeman, Maya L. Nadimpalli
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mSystems
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Online Access:https://journals.asm.org/doi/10.1128/msystems.01037-24
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author Natalie Olson
Frederica Lamar
Hermógenes Mucache
José Fafetine
Joaquim Saíde
Amélia Milisse
Denise R. A. Brito
Kelsey J. Jesser
Karen Levy
Matthew C. Freeman
Maya L. Nadimpalli
author_facet Natalie Olson
Frederica Lamar
Hermógenes Mucache
José Fafetine
Joaquim Saíde
Amélia Milisse
Denise R. A. Brito
Kelsey J. Jesser
Karen Levy
Matthew C. Freeman
Maya L. Nadimpalli
author_sort Natalie Olson
collection DOAJ
description ABSTRACT Increasing demand for poultry has spurred poultry production in low- and middle-income countries like Mozambique. Poultry may be an important source of foodborne, antimicrobial-resistant bacteria to consumers in settings with limited water, sanitation, and hygiene infrastructure. The Chicken Exposures and Enteric Pathogens in Children Exposed through Environmental Pathways (ChEEP ChEEP) study was conducted in Maputo City, Mozambique from 2019 to 2021 to quantify enteric pathogen exposures along the supply chain for commercial and local (i.e., scavenger) chicken breeds. Here, we performed metagenomic sequencing of total DNA from banked ChEEP ChEEP samples to characterize fecal and carcass microbiomes and resistome diversity between chicken breeds and along the supply chain. Fecal samples (n = 26) were collected from commercial and local chickens at production sites and markets and carcass (n = 49) and rinse bucket samples (n = 26) from markets. We conducted taxonomic profiling and identified antimicrobial resistance genes (ARGs) from metagenomic sequence data, focusing especially on potential human pathogens and “high-risk” ARGs. We estimated alpha diversity for each sample and compared by site and breed. We estimated Bray–Curtis dissimilarity between samples and examined clustering. We found that commercial and local chickens harbored distinct fecal potential pathogens and resistomes at production and market sites. Many potentially pathogenic bacteria and ARGs present in chicken fecal samples are also present on carcasses sold to consumers. Finally, commercial chicken carcasses contain high-risk ARGs that are not necessarily introduced from chicken feces. These results indicate markets are an important site of exposure to potentially pathogenic bacteria and high-risk ARGs.IMPORTANCEWhile chicken eggs and meat are a critical protein source in low-income settings, antibiotics are routinely fed to chickens with consequences for selection of antimicrobial resistance. Evaluating how poultry gut bacterial communities, including potential human pathogens and high-risk antimicrobial resistance genes, differ from farm to market could help identify where to target interventions to minimize transmission risks to human populations. In this study in Maputo City, Mozambique, we found compositional differences between commercial and local chicken breeds at production and market sites. We also found that while all potentially pathogenic bacteria and many high-risk antimicrobial resistance genes persisted from production and market through processing, some resistance genes were detected on carcass samples only after processing, suggesting human or environmental contamination is occurring within markets. Overall, our findings indicate that open-air markets may represent a critical juncture for human exposures to pathogens and antimicrobial resistance genes from poultry and poultry products.
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spelling doaj-art-375a64da11e043c2be034fcd92344f062025-01-21T14:00:28ZengAmerican Society for MicrobiologymSystems2379-50772025-01-0110110.1128/msystems.01037-24Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, MozambiqueNatalie Olson0Frederica Lamar1Hermógenes Mucache2José Fafetine3Joaquim Saíde4Amélia Milisse5Denise R. A. Brito6Kelsey J. Jesser7Karen Levy8Matthew C. Freeman9Maya L. Nadimpalli10Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, USAGangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, USAVeterinary Faculty, Universidade Eduardo Mondlane, Maputo, MozambiqueVeterinary Faculty, Universidade Eduardo Mondlane, Maputo, MozambiqueBiotechnology Center, Universidade Eduardo Mondlane, Maputo, MozambiqueBiotechnology Center, Universidade Eduardo Mondlane, Maputo, MozambiqueBiotechnology Center, Universidade Eduardo Mondlane, Maputo, MozambiqueDepartment of Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington, USADepartment of Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington, USAGangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, USAGangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia, USAABSTRACT Increasing demand for poultry has spurred poultry production in low- and middle-income countries like Mozambique. Poultry may be an important source of foodborne, antimicrobial-resistant bacteria to consumers in settings with limited water, sanitation, and hygiene infrastructure. The Chicken Exposures and Enteric Pathogens in Children Exposed through Environmental Pathways (ChEEP ChEEP) study was conducted in Maputo City, Mozambique from 2019 to 2021 to quantify enteric pathogen exposures along the supply chain for commercial and local (i.e., scavenger) chicken breeds. Here, we performed metagenomic sequencing of total DNA from banked ChEEP ChEEP samples to characterize fecal and carcass microbiomes and resistome diversity between chicken breeds and along the supply chain. Fecal samples (n = 26) were collected from commercial and local chickens at production sites and markets and carcass (n = 49) and rinse bucket samples (n = 26) from markets. We conducted taxonomic profiling and identified antimicrobial resistance genes (ARGs) from metagenomic sequence data, focusing especially on potential human pathogens and “high-risk” ARGs. We estimated alpha diversity for each sample and compared by site and breed. We estimated Bray–Curtis dissimilarity between samples and examined clustering. We found that commercial and local chickens harbored distinct fecal potential pathogens and resistomes at production and market sites. Many potentially pathogenic bacteria and ARGs present in chicken fecal samples are also present on carcasses sold to consumers. Finally, commercial chicken carcasses contain high-risk ARGs that are not necessarily introduced from chicken feces. These results indicate markets are an important site of exposure to potentially pathogenic bacteria and high-risk ARGs.IMPORTANCEWhile chicken eggs and meat are a critical protein source in low-income settings, antibiotics are routinely fed to chickens with consequences for selection of antimicrobial resistance. Evaluating how poultry gut bacterial communities, including potential human pathogens and high-risk antimicrobial resistance genes, differ from farm to market could help identify where to target interventions to minimize transmission risks to human populations. In this study in Maputo City, Mozambique, we found compositional differences between commercial and local chicken breeds at production and market sites. We also found that while all potentially pathogenic bacteria and many high-risk antimicrobial resistance genes persisted from production and market through processing, some resistance genes were detected on carcass samples only after processing, suggesting human or environmental contamination is occurring within markets. Overall, our findings indicate that open-air markets may represent a critical juncture for human exposures to pathogens and antimicrobial resistance genes from poultry and poultry products.https://journals.asm.org/doi/10.1128/msystems.01037-24poultrymetagenomicsEast Africaantibiotic resistancemarkets
spellingShingle Natalie Olson
Frederica Lamar
Hermógenes Mucache
José Fafetine
Joaquim Saíde
Amélia Milisse
Denise R. A. Brito
Kelsey J. Jesser
Karen Levy
Matthew C. Freeman
Maya L. Nadimpalli
Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
mSystems
poultry
metagenomics
East Africa
antibiotic resistance
markets
title Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
title_full Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
title_fullStr Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
title_full_unstemmed Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
title_short Farm-to-fork changes in poultry microbiomes and resistomes in Maputo City, Mozambique
title_sort farm to fork changes in poultry microbiomes and resistomes in maputo city mozambique
topic poultry
metagenomics
East Africa
antibiotic resistance
markets
url https://journals.asm.org/doi/10.1128/msystems.01037-24
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