Using source-associated mobile genetic elements to identify zoonotic extraintestinal infections

Cindy M. Liu, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Maliha Aziz, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Daniel E. Park, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Zhenke Wu, Department of Biostatistics, University of Michigan School of Public Health, 1415 Washington Heights, Ann Arbor, MI 48109, USA.
Marc Stegger, Department of Bacteria, Parasites and Fungi, Statens Serum Institut, 5 Artillerivej, DK-2300 Copenhagen, Denmark.
Mengbing Li, Department of Biostatistics, University of Michigan School of Public Health, 1415 Washington Heights, Ann Arbor, MI 48109, USA.
Yashan Wang, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Kara Schmidlin, Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), 3051 W Shamrell Blvd, Flagstaff, AZ 86005, USA.
Timothy J. Johnson, Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, 1365 Gortner Ave, St Paul, MN 55108, USA.
Benjamin J. Koch, Center for Ecosystem Science and Society, Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA.
Bruce A. Hungate, Center for Ecosystem Science and Society, Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, USA.
Lora Nordstrom, Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), 3051 W Shamrell Blvd, Flagstaff, AZ 86005, USA.
Lori Gauld, Flagstaff Medical Center, 1200 N. Beaver St. Flagstaff, AZ 86001, USA.
Brett Weaver, Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), 3051 W Shamrell Blvd, Flagstaff, AZ 86005, USA.
Diana Rolland, Flagstaff Medical Center, 1200 N. Beaver St. Flagstaff, AZ 86001, USA.
Sally Statham, Division of Pathogen Genomics, Translational Genomics Research Institute (TGen), 3051 W Shamrell Blvd, Flagstaff, AZ 86005, USA.
Brantley Hall, Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742, USA.
Sanjeev Sariya, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Gregg S. Davis, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.
Paul S. Keim, The Pathogen and Microbiome Institute, Department of Biological Sciences, Northern Arizona University, Room 210 Building 56, Applied Research & Development, 1395 S Knoles Drive, Flagstaff, AZ 86011, USA.
James R. Johnson, Minneapolis Veterans Affairs Health Care System, 1 Veterans Dr, Minneapolis, MN 55417, USA.
Lance B. Price, Antibiotic Resistance Action Center, Department of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, 800 22nd Street NW, Washington, DC 20052, USA.

Document Type

Journal Article

Publication Date

6-1-2023

Journal

One health (Amsterdam, Netherlands)

Volume

16

DOI

10.1016/j.onehlt.2023.100518

Keywords

Bayesian latent class model; Escherichia coli; Food-animal production; Foodborne; Host adaptation; Infectious diseases; Mobile genetic element; Public health; Urinary tract infection; Zoonosis

Abstract

A one-health perspective may provide new and actionable information about transmission. colonizes a broad range of vertebrates, including humans and food-production animals, and is a leading cause of bladder, kidney, and bloodstream infections in humans. Substantial evidence supports foodborne transmission of pathogenic strains from food animals to humans. However, the relative contribution of foodborne zoonotic (FZEC) to the human extraintestinal disease burden and the distinguishing characteristics of such strains remain undefined. Using a comparative genomic analysis of a large collection of contemporaneous, geographically-matched clinical and meat-source isolates ( = 3111), we identified 17 source-associated mobile genetic elements - predominantly plasmids and bacteriophages - and integrated them into a novel Bayesian latent class model to predict the origins of clinical isolates. We estimated that approximately 8 % of human extraintestinal infections (mostly urinary tract infections) in our study population were caused by FZEC. FZEC strains were equally likely to cause symptomatic disease as non-FZEC strains. Two FZEC lineages, ST131-22 and ST58, appeared to have particularly high virulence potential. Our findings imply that FZEC strains collectively cause more urinary tract infections than does any single non- uropathogenic species (e.g., ). Our novel approach can be applied in other settings to identify the highest-risk FZEC strains, determine their sources, and inform new one-health strategies to decrease the heavy public health burden imposed by extraintestinal infections.

Department

Environmental and Occupational Health

Link to Full Text

Share

COinS