Inter-host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals

Environ Health Perspect. 2019 Oct;127(10):107009. doi: 10.1289/EHP5251. Epub 2019 Oct 23.

Abstract

Background: The rapidly increasing dissemination of carbapenem-resistant Enterobacteriaceae (CRE) in both humans and animals poses a global threat to public health. However, the transmission of CRE between humans and animals has not yet been well studied.

Objectives: We investigated the prevalence, risk factors, and drivers of CRE transmission between humans and their backyard animals in rural China.

Methods: We conducted a comprehensive sampling strategy in 12 villages in Shandong, China. Using the household [residents and their backyard animals (farm and companion animals)] as a single surveillance unit, we assessed the prevalence of CRE at the household level and examined the factors associated with CRE carriage through a detailed questionnaire. Genetic relationships among human- and animal-derived CRE were assessed using whole-genome sequencing-based molecular methods.

Results: A total of 88 New Delhi metallo-β-lactamases-type carbapenem-resistant Escherichia coli (NDM-EC), including 17 from humans, 44 from pigs, 12 from chickens, 1 from cattle, and 2 from dogs, were isolated from 65 of the 746 households examined. The remaining 12 NDM-EC were from flies in the immediate backyard environment. The NDM-EC colonization in households was significantly associated with a) the number of species of backyard animals raised/kept in the same household, and b) the use of human and/or animal feces as fertilizer. Discriminant analysis of principal components (DAPC) revealed that a large proportion of the core genomes of the NDM-EC belonged to strains from hosts other than their own, and several human isolates shared closely related core single-nucleotide polymorphisms and blaNDM genetic contexts with isolates from backyard animals.

Conclusions: To our knowledge, we are the first to report evidence of direct transmission of NDM-EC between humans and animals. Given the rise of NDM-EC in community and hospital infections, combating NDM-EC transmission in backyard farm systems is needed. https://doi.org/10.1289/EHP5251.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Domestic
  • Bacterial Proteins*
  • Carbapenem-Resistant Enterobacteriaceae*
  • Cattle
  • China
  • Dogs
  • Drug Resistance, Multiple, Bacterial / genetics*
  • Escherichia coli*
  • Humans
  • Swine
  • Zoonoses / transmission
  • beta-Lactamases*

Substances

  • Bacterial Proteins
  • beta-Lactamases
  • carbapenemase