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Title: Association of Diet and Antimicrobial Resistance in Healthy U.S. Adults

Abstract

Antimicrobial resistance (AMR) represents a significant source of morbidity and mortality worldwide, with expectations that AMR-associated consequences will continue to worsen throughout the coming decades. Since resistance to antibiotics is encoded in the microbiome, interventions aimed at altering the taxonomic composition of the gut might allow us to prophylactically engineer microbiomes that harbor fewer antibiotic resistant genes (ARGs). Diet is one method of intervention, and yet little is known about the association between diet and antimicrobial resistance. To address this knowledge gap, we examined diet using the food frequency questionnaire (FFQ; habitual diet) and 24-h dietary recalls (Automated Self-Administered 24-h [ASA24®] tool) coupled with an analysis of the microbiome using shotgun metagenome sequencing in 290 healthy adult participants of the United States Department of Agriculture (USDA) Nutritional Phenotyping Study. We found that aminoglycosides were the most abundant and prevalent mechanism of AMR in these healthy adults and that aminoglycoside-O-phosphotransferases (aph3-dprime) correlated negatively with total calories and soluble fiber intake. Individuals in the lowest quartile of ARGs (low-ARG) consumed significantly more fiber in their diets than medium- and high-ARG individuals, which was concomitant with increased abundances of obligate anaerobes, especially from the family Clostridiaceae, in their gut microbiota. Finally, we appliedmore » machine learning to examine 387 dietary, physiological, and lifestyle features for associations with antimicrobial resistance, finding that increased phylogenetic diversity of diet was associated with low-ARG individuals. These data suggest diet may be a potential method for reducing the burden of AMR.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [1]; ORCiD logo [3];  [4];  [3];  [2];  [2]; ORCiD logo [3];  [2]; ORCiD logo [2]
  1. US Dept. of Agriculture (USDA), Davis, CA (United States). ARS-Western Human Nutrition Research Center
  2. US Dept. of Agriculture (USDA), Davis, CA (United States). ARS-Western Human Nutrition Research Center; Univ. of California, Davis, CA (United States)
  3. Univ. of California, Davis, CA (United States)
  4. Nanjing Agricultural University (China)
Publication Date:
Research Org.:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USDA Agricultural Research Service
OSTI Identifier:
1982979
Grant/Contract Number:  
SC0014664; 2032-51530-026-00D; 2032-51530-022-00-D; 0426572
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 13; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; Antibiotic resistance; Bioinformatics; Diet; Diversity; Fiber; Food; Gut microbes; Human health; Machine learning; Metagenomes; Microbiome; Nutrition

Citation Formats

Oliver, Andrew, Xue, Zhengyao, Villanueva, Yirui T., Durbin-Johnson, Blythe, Alkan, Zeynep, Taft, Diana H., Liu, Jinxin, Korf, Ian, Laugero, Kevin D., Stephensen, Charles B., Mills, David A., Kable, Mary E., and Lemay, Danielle G. Association of Diet and Antimicrobial Resistance in Healthy U.S. Adults. United States: N. p., 2022. Web. doi:10.1128/mbio.00101-22.
Oliver, Andrew, Xue, Zhengyao, Villanueva, Yirui T., Durbin-Johnson, Blythe, Alkan, Zeynep, Taft, Diana H., Liu, Jinxin, Korf, Ian, Laugero, Kevin D., Stephensen, Charles B., Mills, David A., Kable, Mary E., & Lemay, Danielle G. Association of Diet and Antimicrobial Resistance in Healthy U.S. Adults. United States. https://doi.org/10.1128/mbio.00101-22
Oliver, Andrew, Xue, Zhengyao, Villanueva, Yirui T., Durbin-Johnson, Blythe, Alkan, Zeynep, Taft, Diana H., Liu, Jinxin, Korf, Ian, Laugero, Kevin D., Stephensen, Charles B., Mills, David A., Kable, Mary E., and Lemay, Danielle G. Tue . "Association of Diet and Antimicrobial Resistance in Healthy U.S. Adults". United States. https://doi.org/10.1128/mbio.00101-22. https://www.osti.gov/servlets/purl/1982979.
@article{osti_1982979,
title = {Association of Diet and Antimicrobial Resistance in Healthy U.S. Adults},
author = {Oliver, Andrew and Xue, Zhengyao and Villanueva, Yirui T. and Durbin-Johnson, Blythe and Alkan, Zeynep and Taft, Diana H. and Liu, Jinxin and Korf, Ian and Laugero, Kevin D. and Stephensen, Charles B. and Mills, David A. and Kable, Mary E. and Lemay, Danielle G.},
abstractNote = {Antimicrobial resistance (AMR) represents a significant source of morbidity and mortality worldwide, with expectations that AMR-associated consequences will continue to worsen throughout the coming decades. Since resistance to antibiotics is encoded in the microbiome, interventions aimed at altering the taxonomic composition of the gut might allow us to prophylactically engineer microbiomes that harbor fewer antibiotic resistant genes (ARGs). Diet is one method of intervention, and yet little is known about the association between diet and antimicrobial resistance. To address this knowledge gap, we examined diet using the food frequency questionnaire (FFQ; habitual diet) and 24-h dietary recalls (Automated Self-Administered 24-h [ASA24®] tool) coupled with an analysis of the microbiome using shotgun metagenome sequencing in 290 healthy adult participants of the United States Department of Agriculture (USDA) Nutritional Phenotyping Study. We found that aminoglycosides were the most abundant and prevalent mechanism of AMR in these healthy adults and that aminoglycoside-O-phosphotransferases (aph3-dprime) correlated negatively with total calories and soluble fiber intake. Individuals in the lowest quartile of ARGs (low-ARG) consumed significantly more fiber in their diets than medium- and high-ARG individuals, which was concomitant with increased abundances of obligate anaerobes, especially from the family Clostridiaceae, in their gut microbiota. Finally, we applied machine learning to examine 387 dietary, physiological, and lifestyle features for associations with antimicrobial resistance, finding that increased phylogenetic diversity of diet was associated with low-ARG individuals. These data suggest diet may be a potential method for reducing the burden of AMR.},
doi = {10.1128/mbio.00101-22},
journal = {mBio (Online)},
number = 3,
volume = 13,
place = {United States},
year = {Tue May 10 00:00:00 EDT 2022},
month = {Tue May 10 00:00:00 EDT 2022}
}

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