Circulation of extended-spectrum β-lactamase and plasmid-borne cephalosporinase-producing Escherichia coli from a One Health perspective
a narrative review
Guillaume Miltgen (Universite de la Reunion (UR), Centre Régional en Antibiothérapie (CRAtb) de La Réunion, CHU Félix Guyon)
Valentine Berti (AP-HP Nord, Université Paris Cité)
Milen Milenkov (Fondation Mérieux)
Heike Schmitt (TU Delft - BT/Environmental Biotechnology, Rijksinstituut voor Volksgezondheid en Milieu (RIVM))
Jaap A. Wagenaar (Wageningen University & Research, Universiteit Utrecht, WHO Collaborating Centre for Reference and Research on Campylobacter and Antimicrobial Resistance from a One Health Perspective/WOAH Reference Laboratory for Campylobacteriosis)
Laurence Armand-Lefevre (AP-HP Nord, Université Paris Cité)
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Abstract
Background
The global rise of extended-spectrum β-lactamase (ESBL) and plasmid-borne cephalosporinase (pAmpC) producing Enterobacterales is a major health concern. Their increasing prevalence in both humans and animals underscores the need for One Health surveillance, for which Escherichia coli has been recognized as a key indicator. While many studies have investigated the circulation of ESBL/pAmpC-producing E. coli (ESBL/pAmpC-Ec) across human, animal, and environmental sectors, the extent to which animals contribute to human acquisition remains unclear.
Objectives
This review provides an overview of the intersectoral circulation of ESBL/pAmpC-Ec and evaluates the potential role of animals as a reservoir for human colonization.
Sources
Publications (2010–2024) identified through PubMed, Scopus, and Google Scholar, on ESBL/pAmpC-Ec circulation across human, animal, and environmental sectors (excluding studies on human-environment, animal-environment, and human-food only) were reviewed considering the included sectors, comparison methods, and geographical context.
Content
Surveillance approaches varied widely between studies, shaped by sampling strategies, geographical context, and isolated comparison methods. Advances in genomic methods have refined our understanding of ESBL/pAmpC-Ec circulation between sectors. Early studies, mostly conducted in high-income countries (HICs), suggested human-animal transmission based on comparisons of ESBL/pAmpC-Ec sequence types, resistance genes, and plasmid replicons. However, these findings were challenged by the introduction of more discriminating comparison methods such as whole-genome sequencing, which revealed a largely compartmentalized circulation of ESBL/pAmpC-Ec in HICs. Similar studies in low- and middle-income countries (LMICs) shifted this paradigm, demonstrating frequent cross-sectoral transmission across humans, animals, and the environment. Many authors also highlighted the likely underestimated role of plasmids in the circulation of ESBL/pAmpC genes.
Implications
Despite the heterogeneity of the studies, two distinct scenarios emerged: predominantly intrasectoral ESBL/pAmpC-Ec circulation in HICs and significant intersectoral circulation in LMICs. These findings underscore the need for region-specific antimicrobial resistance control strategies, focusing on limiting human-to-human transmission in HICs and enhancing sanitation and biosecurity in LMICs.
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