Antimicrobial Resistance in Wildlife in Guadeloupe (French West Indies): Distribution of a Singlebla(CTX-M-1)/IncI1/ST3 Plasmid Among Humans and Wild Animals

Type Article
Date 2020-07
Language English
Author(s) Guyomard-Rabenirina Stephanie1, Reynaud YannORCID1, Pot MatthieuORCID1, Albina EmmanuelORCID2, 3, Couvin DavidORCID1, Ducat Celia1, Gruel Gaelle1, Ferdinand Severine1, Legreneur Pierre4, Le Hello Simon5, 6, Malpote Edith7, Sadikalay Syndia1, Talarmin Antoine1, Breurec Sebastien1, 8, 9
Affiliation(s) 1 : Inst Pasteur Guadeloupe, Transmiss Reservoir & Divers Pathogens Unit, Pointe A Pitre, Guadeloupe, France.
2 : CIRAD, UMR ASTRE, Montpellier, France.
3 : Univ Montpellier, CIRAD, INRA, UMR ASTRE, F-34398 Montpellier, France.
4 : Univ Claude Bernard Lyon 1, Univ Lyon, Interuniv Lab Human Movement Biol E4 7424, Villeurbanne, France.
5 : Inst Pasteur, Enter Bacterial Pathogens Unit, Paris, France.
6 : Univ Caen Normandy, EA2656, GRAM 2 0, UNICAEN,Grp Rech Adaptat Microbienne, Caen, France.
7 : Univ Hosp Guadeloupe, Lab Clin Microbiol, Pointe A Pitre, Guadeloupe, France.
8 : Univ Antilles, Fac Med Hyacinthe Bastaraud, Pointe A Pitre, Guadeloupe, France.
9 : Ctr Clin Invest 1424, INSERM, Pointe A Pitre, Guadeloupe, France.
Source Frontiers In Microbiology (1664-302X) (Frontiers Media Sa), 2020-07 , Vol. 11 , P. 1524 (11p.)
DOI 10.3389/fmicb.2020.01524
WOS© Times Cited 21
Keyword(s) Escherichia coli, wild animals, antimicrobial resistance, extended-spectrum beta-lactamase, plasmid
Abstract Limited data are available on the contribution of wildlife to the spread of antibacterial resistance. We determined the prevalence of resistance to antibiotics inEscherichia coliisolates collected from wild animals in 2013 and 2014 and the genetic basis for resistance to third-generation cephalosporin in Guadeloupe. We recovered 52 antibiotic-resistant (AR)E. colistrains from 48 of the 884 (5.4%) wild animals tested (46 iguanas, 181 birds, 289 anoles, and 368 rodents at 163 sampling sites). Rodents had higher rates of carriage (n= 38, 10.3%) than reptiles and birds (2.4% and 1.1%, respectively,p< 0.001). A significant association (p< 0.001) was found between the degree of anthropization and the frequency of ARE. colicarriage for all species. The carriage rate of ciprofloxacin- and cefotaxime-resistant isolates was 0.7% (6/884) and 1.5% (13/884), respectively. Most (65.4%) ARE. coliwere multi-drug resistant, and the prevalence of extended-spectrum beta-lactamase (ESBL)-producingE. coliwas low (n= 7, 0.8%) in all species. Eight ESBL-producingE. coliwere recovered, two genetically unrelated isolates being found in one bird. These isolates and 20 human invasive ESBLE. coliisolates collected in Guadeloupe during the same period were investigated by whole genome sequencing.bla(CTX-M-1)was the only ESBL gene shared by three animal classes (humans,n= 2; birds,n= 2; rodents,n= 2). Thebla(CTX-M-1)gene and most of the antimicrobial resistance genes were present in a large conjugative IncI1 plasmid that was highly similar (>99% nucleotide identity) to ESBL-carrying plasmids found in several countries in Europe and in Australia. Although the prevalence of ESBL-producingE. coliisolates was very low in wild animals, it is of concern that the well-conserved IncI1 plasmid-carryingbla(CTX-M-1)is widespread and occurs in variousE. colistrains from animals and humans.
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FIGURE S1 | Maximum likelihood (ML) unrooted phylogenetic tree of extended-spectrum beta-lactamase-producing Escherichia coli isolates based on multiple sequence alignments of the 3082 core genome... 561 KB Open access
FIGURE S2 | Maximum likelihood (ML) phylogenetic tree of extended-spectrum beta-lactamase-producing Escherichia coli isolates based on multiple sequence alignments of the 3082 core genome loci ... 779 KB Open access
FIGURE S3 | Alignment of IncI1/blaCTX–M–1/ST3 plasmids from the PLSDB database listed in Supplementary Table S3, with the four plasmids sequenced in this study: pEC1, pEC7, pEC28, and pEC38. 1 MB Open access
TABLE S1 | Molecular characteristics of extended-spectrum beta-lactamase-producing Escherichia coli isolates from wild animals and humans in Guadeloupe (French West Indies). 18 KB Open access
TABLE S2 | Characteristics of extended-spectrum beta-lactamase-producing Escherichia coli isolates from wild animals and humans in Guadeloupe (French West Indies). 16 KB Open access
TABLE S3 | Metadata on IncI1/blaCTX–M–1/ST3 plasmids in the PLSDB database sharing >99% nucleotide identity with pESBL20150178 and having aadA5/dfrA17/sul2 resistance genes. 27 KB Open access
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Guyomard-Rabenirina Stephanie, Reynaud Yann, Pot Matthieu, Albina Emmanuel, Couvin David, Ducat Celia, Gruel Gaelle, Ferdinand Severine, Legreneur Pierre, Le Hello Simon, Malpote Edith, Sadikalay Syndia, Talarmin Antoine, Breurec Sebastien (2020). Antimicrobial Resistance in Wildlife in Guadeloupe (French West Indies): Distribution of a Singlebla(CTX-M-1)/IncI1/ST3 Plasmid Among Humans and Wild Animals. Frontiers In Microbiology, 11, 1524 (11p.). Publisher's official version : https://doi.org/10.3389/fmicb.2020.01524 , Open Access version : https://archimer.ifremer.fr/doc/00771/88293/