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Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)

Guadeloupe (French West Indies), a Caribbean island, is an ideal place to study the reservoirs of the Klebsiella pneumoniae species complex (KpSC) and identify the routes of transmission between human and nonhuman sources due to its insularity, small population size, and small area. Here, we report...

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Autores principales: Dereeper, Alexis, Gruel, Gaëlle, Pot, Matthieu, Couvin, David, Barbier, Elodie, Bastian, Sylvaine, Bambou, Jean-Christophe, Gelu-Simeon, Moana, Ferdinand, Séverine, Guyomard-Rabenirina, Stéphanie, Passet, Virginie, Martino, Frederic, Piveteau, Pascal, Reynaud, Yann, Rodrigues, Carla, Roger, Pierre-Marie, Roy, Xavier, Talarmin, Antoine, Tressieres, Benoit, Valette, Marc, Brisse, Sylvain, Breurec, Sébastien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9603589/
https://www.ncbi.nlm.nih.gov/pubmed/36094181
http://dx.doi.org/10.1128/spectrum.01242-22
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author Dereeper, Alexis
Gruel, Gaëlle
Pot, Matthieu
Couvin, David
Barbier, Elodie
Bastian, Sylvaine
Bambou, Jean-Christophe
Gelu-Simeon, Moana
Ferdinand, Séverine
Guyomard-Rabenirina, Stéphanie
Passet, Virginie
Martino, Frederic
Piveteau, Pascal
Reynaud, Yann
Rodrigues, Carla
Roger, Pierre-Marie
Roy, Xavier
Talarmin, Antoine
Tressieres, Benoit
Valette, Marc
Brisse, Sylvain
Breurec, Sébastien
author_facet Dereeper, Alexis
Gruel, Gaëlle
Pot, Matthieu
Couvin, David
Barbier, Elodie
Bastian, Sylvaine
Bambou, Jean-Christophe
Gelu-Simeon, Moana
Ferdinand, Séverine
Guyomard-Rabenirina, Stéphanie
Passet, Virginie
Martino, Frederic
Piveteau, Pascal
Reynaud, Yann
Rodrigues, Carla
Roger, Pierre-Marie
Roy, Xavier
Talarmin, Antoine
Tressieres, Benoit
Valette, Marc
Brisse, Sylvain
Breurec, Sébastien
author_sort Dereeper, Alexis
collection PubMed
description Guadeloupe (French West Indies), a Caribbean island, is an ideal place to study the reservoirs of the Klebsiella pneumoniae species complex (KpSC) and identify the routes of transmission between human and nonhuman sources due to its insularity, small population size, and small area. Here, we report an analysis of 590 biological samples, 546 KpSC isolates, and 331 genome sequences collected between January 2018 and May 2019. The KpSC appears to be common whatever the source. Extended-spectrum-β-lactamase (ESBL)-producing isolates (21.4%) belonged to K. pneumoniae sensu stricto (phylogroup Kp1), and all but one were recovered from the hospital setting. The distribution of species and phylogroups across the different niches was clearly nonrandom, with a distinct separation of Kp1 and Klebsiella variicola (Kp3). The most frequent sequence types (STs) (≥5 isolates) were previously recognized as high-risk multidrug-resistant (MDR) clones, namely, ST17, ST307, ST11, ST147, ST152, and ST45. Only 8 out of the 63 STs (12.7%) associated with human isolates were also found in nonhuman sources. A total of 22 KpSC isolates were defined as hypervirulent: 15 associated with human infections (9.8% of all human isolates), 4 (8.9%) associated with dogs, and 3 (15%) associated with pigs. Most of the human isolates (33.3%) belonged to the globally successful sublineage CG23-I. ST86 was the only clone shared by a human and a nonhuman (dog) source. Our work shows the limited transmission of KpSC isolates between human and nonhuman sources and points to the hospital setting as a cornerstone of the spread of MDR clones and antibiotic resistance genes. IMPORTANCE In this study, we characterized the presence and genomic features of isolates of the Klebsiella pneumoniae species complex (KpSC) from human and nonhuman sources in Guadeloupe (French West Indies) in order to identify the reservoirs and routes of transmission. This is the first study in an island environment, an ideal setting that limits the contribution of external imports. Our data showed the limited transmission of KpSC isolates between the different compartments. In contrast, we identified the hospital setting as the epicenter of antibiotic resistance due to the nosocomial spread of successful multidrug-resistant (MDR) K. pneumoniae clones and antibiotic resistance genes. Ecological barriers and/or limited exposure may restrict spread from the hospital setting to other reservoirs and vice versa. These results highlight the need for control strategies focused on health care centers, using genomic surveillance to limit the spread, particularly of high-risk clones, of this important group of MDR pathogens.
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spelling pubmed-96035892022-10-27 Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies) Dereeper, Alexis Gruel, Gaëlle Pot, Matthieu Couvin, David Barbier, Elodie Bastian, Sylvaine Bambou, Jean-Christophe Gelu-Simeon, Moana Ferdinand, Séverine Guyomard-Rabenirina, Stéphanie Passet, Virginie Martino, Frederic Piveteau, Pascal Reynaud, Yann Rodrigues, Carla Roger, Pierre-Marie Roy, Xavier Talarmin, Antoine Tressieres, Benoit Valette, Marc Brisse, Sylvain Breurec, Sébastien Microbiol Spectr Research Article Guadeloupe (French West Indies), a Caribbean island, is an ideal place to study the reservoirs of the Klebsiella pneumoniae species complex (KpSC) and identify the routes of transmission between human and nonhuman sources due to its insularity, small population size, and small area. Here, we report an analysis of 590 biological samples, 546 KpSC isolates, and 331 genome sequences collected between January 2018 and May 2019. The KpSC appears to be common whatever the source. Extended-spectrum-β-lactamase (ESBL)-producing isolates (21.4%) belonged to K. pneumoniae sensu stricto (phylogroup Kp1), and all but one were recovered from the hospital setting. The distribution of species and phylogroups across the different niches was clearly nonrandom, with a distinct separation of Kp1 and Klebsiella variicola (Kp3). The most frequent sequence types (STs) (≥5 isolates) were previously recognized as high-risk multidrug-resistant (MDR) clones, namely, ST17, ST307, ST11, ST147, ST152, and ST45. Only 8 out of the 63 STs (12.7%) associated with human isolates were also found in nonhuman sources. A total of 22 KpSC isolates were defined as hypervirulent: 15 associated with human infections (9.8% of all human isolates), 4 (8.9%) associated with dogs, and 3 (15%) associated with pigs. Most of the human isolates (33.3%) belonged to the globally successful sublineage CG23-I. ST86 was the only clone shared by a human and a nonhuman (dog) source. Our work shows the limited transmission of KpSC isolates between human and nonhuman sources and points to the hospital setting as a cornerstone of the spread of MDR clones and antibiotic resistance genes. IMPORTANCE In this study, we characterized the presence and genomic features of isolates of the Klebsiella pneumoniae species complex (KpSC) from human and nonhuman sources in Guadeloupe (French West Indies) in order to identify the reservoirs and routes of transmission. This is the first study in an island environment, an ideal setting that limits the contribution of external imports. Our data showed the limited transmission of KpSC isolates between the different compartments. In contrast, we identified the hospital setting as the epicenter of antibiotic resistance due to the nosocomial spread of successful multidrug-resistant (MDR) K. pneumoniae clones and antibiotic resistance genes. Ecological barriers and/or limited exposure may restrict spread from the hospital setting to other reservoirs and vice versa. These results highlight the need for control strategies focused on health care centers, using genomic surveillance to limit the spread, particularly of high-risk clones, of this important group of MDR pathogens. American Society for Microbiology 2022-09-12 /pmc/articles/PMC9603589/ /pubmed/36094181 http://dx.doi.org/10.1128/spectrum.01242-22 Text en Copyright © 2022 Dereeper et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Dereeper, Alexis
Gruel, Gaëlle
Pot, Matthieu
Couvin, David
Barbier, Elodie
Bastian, Sylvaine
Bambou, Jean-Christophe
Gelu-Simeon, Moana
Ferdinand, Séverine
Guyomard-Rabenirina, Stéphanie
Passet, Virginie
Martino, Frederic
Piveteau, Pascal
Reynaud, Yann
Rodrigues, Carla
Roger, Pierre-Marie
Roy, Xavier
Talarmin, Antoine
Tressieres, Benoit
Valette, Marc
Brisse, Sylvain
Breurec, Sébastien
Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title_full Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title_fullStr Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title_full_unstemmed Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title_short Limited Transmission of Klebsiella pneumoniae among Humans, Animals, and the Environment in a Caribbean Island, Guadeloupe (French West Indies)
title_sort limited transmission of klebsiella pneumoniae among humans, animals, and the environment in a caribbean island, guadeloupe (french west indies)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9603589/
https://www.ncbi.nlm.nih.gov/pubmed/36094181
http://dx.doi.org/10.1128/spectrum.01242-22
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