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

Miltgen Guillaume, Martak Daniel, Valot Benoît, Kamus Laure, Garrigos Thomas, Verchere Guillaume, Gbaguidi-Haore Houssein, Ben Cimon Céline, Ramiandrisoa Mahery, Picot Sandrine, Lignereux Anne, Masson Geoffrey, Jaffar-Bandjee Marie-Christine, Belmonte Olivier, Cardinale Eric, Hocquet Didier, Mavingui Patrick, Bertrand Xavier. 2022. One Health compartmental analysis of ESBL-producing Escherichia coli on Reunion Island reveals partitioning between humans and livestock. Journal of Antimicrobial Chemotherapy, 77 (5) : 1254-1262.

Résumé : 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 da:ta 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.

Mots-clés Agrovoc : bétail, genre humain, génétique des populations, variation génétique, Escherichia coli, transmission des maladies, Enquête pathologique, ovin, épidémiologie, zoonose

Mots-clés géographiques Agrovoc : France, La Réunion, Mayotte, Madagascar, océan Indien

Agences de financement hors UE : Agence Régionale de Santé de La Réunion, Commission de l'Océan Indien, Centre de Coopération Internationale en Recherche Agronomique pour le Développement, Centre Hospitalier Universitaire de Besançon, Université de La Réunion, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, Institut de Recherche pour le Développement

Auteurs et affiliations

• Miltgen Guillaume, Centre hospitalier universitaire Félix Guyon (REU) - auteur correspondant
• Martak Daniel, CHU Besançon (FRA)
• Valot Benoît, Université de Bourgogne (FRA)
• Kamus Laure, Centre hospitalier universitaire Félix Guyon (REU)
• Garrigos Thomas, Centre hospitalier universitaire Félix Guyon (REU)
• Verchere Guillaume, Université de la Réunion (REU)
• Gbaguidi-Haore Houssein, CHU Besançon (FRA)
• Ben Cimon Céline, Laboratoires Réunilab (REU)
• Ramiandrisoa Mahery, Laboratoires Cerballiance (REU)
• Picot Sandrine, CHU (REU)
• Lignereux Anne, Centre Hospitalier Ouest Réunion (REU)
• Masson Geoffrey, Groupe Hospitalier Est Réunion (REU)
• Jaffar-Bandjee Marie-Christine, Centre hospitalier universitaire Félix Guyon (REU)
• Belmonte Olivier, Centre hospitalier universitaire Félix Guyon (REU)
• Cardinale Eric, CIRAD-BIOS-UMR ASTRE (REU) ORCID: 0000-0002-3434-3541
• Hocquet Didier, CHU Besançon (FRA)
• Mavingui Patrick, Université de la Réunion (REU)
• Bertrand Xavier, Université de Bourgogne (FRA)

Source : Cirad-Agritrop (https://agritrop.cirad.fr/606397/)

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