Extraintestinal pathogenic (ExPEC) lineages explain prolonged carriage of travel-acquired extended-spectrum β-lactamase-producing Escherichia coli
AbstractFecally carried extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (ESBL-Ec) are frequently acquired during international travel, contributing to global spread of AMR. However, determinants of long-term carriage of travel-acquired ESBL-Ec are unknown.From a prospective cohort study of 2001 international travelers, we selected all 28 who acquired ESBL-Ec during travel and subsequently carried ESBL-Ec for at least 12 months after return. We sequenced a total of 155 ESBL-Ec isolates from these long-term carriers and 54 age-, sex- and destination-matched short-term carriers (<1 month carriage). We confirmed persistence of ESBL-Ec in long-term carriers using SNP typing and compared ESBL-Ec from long-term and short-term carriers using in silico multi-locus sequence and phylogroup typing. We employed long-read sequencing to investigate ESBL plasmid dissemination.We show that extraintestinal pathogenic (ExPEC) lineages of Escherichia coli are significantly more likely to persist in healthy travelers than other E. coli lineages, in the absence of antibiotic usage, mainly driven by sequence type (ST) 131 and phylogroup D E. coli. Additionally, we identified two epidemiologically unrelated clonal lineages of ST38 carrying a range of ESBL- and carbapenemase-encoding genes. Using public datasets, we demonstrate the recent parallel emergence of these lineages and their subsequent rapid global dissemination, which has major implications for epidemiological tracking of ST38 strains.Our findings show that persistence of travel-acquired ESBL-Ec is mediated by a limited number of ExPEC lineages. These findings support recent insights suggesting ExPEC lineages have not necessarily evolved towards virulence, but rather towards efficient intestinal colonization.ImportanceIn 2018, an estimated 1.4 billion international trips were undertaken according to the World Tourism Organization. Antibiotic resistant Escherichia coli are frequently acquired during travel due to contact with contaminated foodstuff, or fecal-oral, environmental and human-to-human transmission. Resistant E. coli that can persist in the travelers’ gut for long periods of time after return from travel, are likely to contribute to further transmission. Using highly detailed genomic typing of resistant E. coli, isolated from a large prospective cohort of international travelers, we identified bacterial characteristics explaining long-term carriage. Our results provide important information that can be used to estimate the risk of long-term carriage when travelers return with acquired resistant E. coli.