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

Abstract

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.

Keywords: Caribbean; ESBL; Klebsiella pneumoniae; One Health; genomic.

FIG 1

Species and phylogroup distributions of 433 isolates of the K. pneumoniae species complex collected in Guadeloupe (French West Indies), according to source. Species were defined by real-time PCR.

FIG 2

Phylogenetic tree of 331 isolates of the K. pneumoniae species complex from Guadeloupe (French West Indies). A maximum likelihood tree was constructed using RAxML based on the core-genome alignment and drawn with iTOL. Leaves are colored according to the phylogroup (Kp1, Kp2, Kp3, and Kp4), and annotation tracks are displayed as follows: source (human/animal/environment), nosocomial/community origin, ESBL production, and hypervirulence.

FIG 3

Unrooted phylogenetic trees of the genomes of the six most represented sequence types (STs) recovered in Guadeloupe (French West Indies). All these STs belong to K. pneumoniae sensu stricto (Kp1). Isolates are colored according to their source (i.e., human in blue and animal in orange). Using a threshold of <10 SNPs, single strains are framed with dotted lines.