Genomic characterization of extended-spectrum β-lactamase-producing Escherichia coli spread among chickens and healthy residents in Lombok, Indonesia

TL;DR

This study explores how antibiotic-resistant E. coli spreads between chickens and people in Lombok, Indonesia, highlighting risks to public health.

Contribution

The study provides genomic evidence of zoonotic transmission and plasmid-mediated resistance spread in a poultry farming setting.

Findings

blaCTX-M-55 was the most common ESBL gene, often carried by an IncHI1A-type plasmid.

ESBL-Ec clones were detected in both chickens and farmers, indicating zoonotic transmission.

Multidrug resistance was observed due to the acquisition of resistance genes via plasmids.

Abstract

Extended-spectrum β-lactamase-producing Escherichia coli (ESBL-Ec) poses a substantial public health challenge, particularly in developing countries where antimicrobial resistance is a growing concern. Although extensive research has documented the prevalence and impact of ESBL-Ec in clinical settings and farm animals, the intricate relationship between poultry farming practices and human health remains unclear. To elucidate the genomic relationships between isolates from chickens and humans, we conducted a whole-genome sequencing analysis of 200 E. coli isolates derived from chickens, chicken farmers, and non-farmer volunteers in Lombok, Indonesia. The isolates exhibited considerable diversity, with 78 distinct sequence types (STs) identified by multilocus sequence typing. Of these, 35% (n = 70) and 6% (n = 12) were positive for ESBL and AmpC-type β-lactamase genes, respectively, with blaCTX-M-55 being the most prevalent (n = 41). The most prevalent STs among those carrying ESBL or AmpC genes were ST48, ST1485, ST1727, and ST2690. Phylogenetic analysis of publicly available data indicated that ST1485, ST1727, and ST2690 strains had an indigenous spread in this region, whereas the ST48 isolates originated from different sources. The blaCTX-M-55 gene was identified in 22 different STs, predominantly carried by an IncHI1A-type plasmid, suggesting horizontal transmission of the plasmid over the clonal barrier. Long-read sequencing analysis of representative isolates revealed the presence of additional resistance genes against different classes of antibiotics, suggesting that the acquisition of the IncHI1A-type plasmid contributes to multidrug resistance in recipient clones. Our analysis provides unique insights into the dissemination of multidrug-resistant ESBL-Ec strains in Lombok, where humans and chickens are in close proximity.

We performed a genomic comparison of ESBL-producing E. coli (ESBL-Ec) isolated from chickens, chicken farmers, and non-farmers on Lombok Island, where indigenous chicken farming, which involves close proximity of humans and chickens, is a major industry. The detection of the same ESBL-Ec clones in both chickens and farmers indicated the potential of a zoonotic transmission pathway for antibiotic-resistant bacteria. Moreover, the presence of a common plasmid carrying an ESBL gene along with other antimicrobial resistance genes in various E. coli clonal groups highlights the dissemination of resistance determinants within both poultry and human populations. This cross-species amplification of antimicrobial resistance poses a substantial risk to public health, as it can lead to the proliferation of multidrug-resistant bacterial infections, complicating treatment options and increasing the burden on healthcare systems. Addressing these issues is crucial for implementing effective antimicrobial stewardship and improving biosecurity practices in poultry farming.

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