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

OBJECTIVES: In May 2024, the World Health Organization classified carbapenem (CARB)- and third-generation cephalosporin (3GC) resistance (R) in Escherichia coli 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 CARBR, COLR, and 3GCR in E. coli 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 E. coli, and antimicrobial susceptibility to CARB, COL and 3GC in E. coli 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 E. coli genomes, respectively. RESULTS: Of the 5,034 identified articles, 64 studies were deemed eligible. The overall PPs of 3GCR, CARBR, and COLR E. coli 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 3GCR-, COLR- and CARBR E. coli significantly varied by hosts, continent, and year of studies (p<0.05). Diverse E. coli lineages were found, including 13 high-risk E. coli sequence types (STs), within which ST10 predominated. Phylogenomic analyses produced 4 clusters of related CARBR- and COLR E. coli strains (<25 single nucleotide polymorphism): ST940-blaOXA-181 from humans in Lebanon, ST617-mcr-1 from pigs in China, ST46-mcr-1 from poultry in Tanzania, and ST1720-mcr-1 from goats in France. CONCLUSIONS: COLR and 3GCR are more frequent than CARBR in gut E. coli. These 10-year epidemiological data highlight the persistence and transmission of critical priority and high-risk E. coli strains in healthy humans and animals, raising significant One Health concerns.