One Health compartmental analysis of ESBL-producing Escherichia coli on Reunion Island reveals partitioning between humans and livestock

Abstract

Background Extended-spectrum β-lactamase-producing Escherichia coli (ESBL-Ec) is a major cause of infections worldwide. An understanding of the reservoirs and modes of transmission of these pathogens is essential, to tackle their increasing frequency. Objectives We investigated the contributions of various compartments (humans, animals, environment), to human colonization or infection with ESBL-Ec over a 3 year period, on an island. Methods The study was performed on Reunion Island (Southwest Indian Ocean). We collected ESBL-Ec isolates prospectively from humans, wastewater and livestock between April 2015 and December 2018. Human specimens were recovered from a regional surveillance system representative of the island’s health facilities. These isolates were compared with those from livestock and urban/rural wastewater, by whole-genome sequencing. Results We collected 410 ESBL-Ec isolates: 161 from humans, 161 from wastewater and 88 from animals. Phylogenomic analysis demonstrated high diversity (100 STs), with different STs predominating among isolates from humans (ST131, ST38, ST10) and animals (ST57, ST156). The large majority (90%) of the STs, including ST131, were principally associated with a single compartment. The CTX-M-15, CTX-M-27 and CTX-M-14 enzymes were most common in humans/human wastewater, whereas CTX-M-1 predominated in animals. Isolates of human and animal origin had different plasmids carrying blaCTX-M genes, with the exception of a conserved IncI1-ST3 blaCTX-M-1 plasmid. Conclusions These molecular data suggest that, despite their high level of contamination, animals are not a major source of the ESBL-Ec found in humans living on this densely populated high-income island. Public health policies should therefore focus primarily on human-to-human transmission, to prevent human infections with ESBL-Ec.

ESBL‐producing Enterobacteriaceae in a rural Rwandan community: Carriage among community members, livestock, farm products and environment

“…We were expecting a role of animal husbandry in ESBL-PE transmission but did not observe it: livestock in less than half the proportion seen in humans were carriers, livestock ownership did not increase the odds of ESBL-PE carriage in humans, and this was also the case when animals were ESBL-PE carriers themselves. This accords with findings from Réunion, showing that animals are not a major source of the ESBL-E. coli found in humans [31]. Reasons for this lack of association in our study may include the villagers' almost complete preoccupation with livestock farming, and a respectively low statistical power, and a predominance of free roaming, particularly smaller, livestock with resulting broad rather than focused faecal contamination.…”

Tricycle surveillance in Antananarivo, Madagascar: circulation of both extended-spectrum beta-lactamase producingEscherichia colistrains and plasmids among humans, chickens and the environment

“…Most studies analysing the intersectoral circulation of ESBL-E. coli have identified rather genetically distinct populations of human, animal and environmental isolates, with inter-human transmission being the major source for community colonization. [24][25][26][27] However, these studies have rarely investigated isolates collected at the same temporo-spatial scale. 24,25,27 Moreover, they included human strains, isolated from invasive infections, and were mainly conducted in high-income countries, where E. coli strains from B2 and D phylogroups have progressively outpaced commensal phylogroups A and B1.…”

Faecal carriage of ESBL-producingEscherichia coliin a remote region of Niger

“…Fourth, careful genetic analysis of the bla CTX-M-15 gene in the ST46 and ST46 single locus variant clones (Figure 4) argues for mobilisation of the ESBL gene with variable numbers of flanking genes between plasmids and from plasmids to chromosome. This process has been recently suggested in A phylogroup strains isolated during a "One Health" study on Reunion island 63 .…”