Guts of healthy humans, livestock, and pets harbor critical-priority and high-risk Escherichia coli clones

Abstract

OBJECTIVES: In May 2024, the World Health Organization classified carbapenem (CARB)- and third-generation cephalosporin (3GC) resistance (R) in <italic>Escherichia coli</italic> as a critical priority, whereas colistin (COL) is a “last resort” antibiotic for their treatment. This meta-analysis evaluated the pooled prevalence, high-risk lineages, genetic relatedness, and mechanisms of CARB^R, COL^R, and 3GC^R in <italic>E. coli</italic> from healthy humans and animals.METHODS: We conducted a systematic review and meta-analyses following the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) criteria on all eligible studies that reported the analysis of <italic>E. coli</italic>, and antimicrobial susceptibility to CARB, COL and 3GC in <italic>E. coli</italic> from gut samples of clinically healthy humans, livestock, and pets from June 2014 to June 2024. Random-effect models and conserved signature indels phylogeny 1.4 were used to determine pooled prevalence rates (PPs) and the relatedness of publicly available <italic>E. coli</italic> genomes, respectively.RESULTS: Of the 5,034 identified articles, 64 studies were deemed eligible. The overall PPs of 3GC^R, CARB^R, and COL^R <italic>E. coli</italic> were 22.5% (95% confidence interval [CI], 17.5 to 28.3), 2.2% (95% CI, 1.0 to 4.7), and 15.5% (95% CI, 10.8 to 21.8), respectively. The PPs of 3GC^R-, COL^R- and CARB^R <italic>E. coli</italic> significantly varied by hosts, continent, and year of studies (p<0.05). Diverse <italic>E. coli</italic> lineages were found, including 13 high-risk <italic>E. coli</italic> sequence types (STs), within which ST10 predominated. Phylogenomic analyses produced 4 clusters of related CARB^R- and COL^R <italic>E. coli</italic> strains (<25 single nucleotide polymorphism): ST940-<italic>bla</italic>_OXA-181 from humans in Lebanon, ST617-<italic>mcr</italic>-1 from pigs in China, ST46-<italic>mcr</italic>-1 from poultry in Tanzania, and ST1720-<italic>mcr</italic>-1 from goats in France.CONCLUSIONS: COL^R and 3GC^R are more frequent than CARB^R in gut <italic>E. coli</italic>. These 10-year epidemiological data highlight the persistence and transmission of critical priority and high-risk <italic>E. coli</italic> strains in healthy humans and animals, raising significant One Health concerns.