Dataset Information

Limited transmission of carbapenem-resistant Klebsiella pneumoniae between animals and humans: a study in Qingdao.

ABSTRACT: ABSTRACTDespite no carbapenem use in food animals, carbapenem-resistant Klebsiella pneumoniae (CRKP) perseveres within food animals, rising significant concerns regarding public health risks originating from these non-clinical reservoirs. To investigate the potential link between CRKP in food animals and its infections in humans, we conducted a cross-sectional study encompassing human clinical, meat products, and farm animals, in Qingdao city, Shandong province, China. We observed a relatively higher presence of CRKP among hospital inpatients (7.3%) compared to that in the meat products (2.7%) and farm animals (pig, 4.6%; chicken, 0.63%). Multilocus sequence typing and core-genome phylogenetic analyses confirm there is no evidence of farm animals and meat products in the clinical acquisition of K. pneumoniae isolates and carbapenem-resistant genes. However, potential transmission of K. pneumoniae of ST659 and IncX3 plasmid harbouring bla_NDM-5 gene from pigs to pork and farm workers was observed. Our findings suggest a limited role of farm animals and meat products in the human clinical acquisition of K. pneumoniae, and the transmission of K. pneumoniae is more common within settings, than between them.

SUBMITTER: Bai R

PROVIDER: S-EPMC11312996 | biostudies-literature | 2024 Dec

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Limited transmission of carbapenem-resistant Klebsiella pneumoniae between animals and humans: a study in Qingdao.

Bai Rina R Wang Xiao X Zou Zhiyu Z Zhou Wenjing W Tan Chang C Cao Yue Y Fu Bo B Zhai Weishuai W Hu Fupin F Wang Yang Y Wu Congming C Zhu Yuanqi Y Sun Chengtao C

Emerging microbes & infections 20240808 1

ABSTRACTDespite no carbapenem use in food animals, carbapenem-resistant Klebsiella pneumoniae (CRKP) perseveres within food animals, rising significant concerns regarding public health risks originating from these non-clinical reservoirs. To investigate the potential link between CRKP in food animals and its infections in humans, we conducted a cross-sectional study encompassing human clinical, meat products, and farm animals, in Qingdao city, Shandong province, China. We observed ...[more]

PMID: 39082402

Similar Datasets

Project 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.

Project description:The surveillance of mobile genetic elements facilitating the spread of antimicrobial resistance genes has been challenging. Here, we tracked both clonal and plasmid transmission in colistin- and carbapenem-resistant Klebsiella pneumoniae using short- and long-read sequencing technologies. We observed three clonal transmissions, all containing Incompatibility group (Inc) L plasmids and New Delhi metallo-beta-lactamase blaNDM-1, although not co-located on the same plasmid. One IncL-blaNDM-1 plasmid had been transferred between sequence type (ST) 392 and ST15, and the promiscuous IncL-blaOXA-48 plasmid was likely shared between a singleton and a clonal transmission of ST392. Plasmids within clonal outbreaks and between clusters and STs had 0-2 single nucleotide polymorphism (SNP) differences, showing high stability upon transfer to same or different STs. The simplest explanation, without a comprehensive analysis with long-read sequencing, would be the spread of a single common IncL-blaNDM-1 plasmid. However, here, we report blaNDM-1 in five different plasmids, emphasizing the need to investigate plasmid-mediated transmission for effective containment of outbreaks.IMPORTANCEAntimicrobial resistance occupies a central stage in global public health emergencies. Recently, efforts to track the genetic elements that facilitate the spread of resistance genes in plasmids outbreaks, utilizing short-read sequencing technologies, have been described. However, incomplete plasmid reconstruction from short-read sequencing data hinders full knowledge about plasmid structure, which makes the exploration very challenging. In this study, we used both short- and long-read sequencing in clinical Klebsiella pneumoniae from University Hospital Centre Zagreb, Croatia, which was resistant to both last-resort antibiotics colistin and carbapenem. Our results show complex transmission networks and sharing of plasmids, emphasizing multiple transmissions of plasmids harboring carbapenem and/or colistin resistance genes between and within K. pneumoniae clones. Only full-length sequencing plus a novel way of determining plasmid clusters resulted in the complete picture, showing how future active monitoring of plasmids as a vital tool for infection prevention and control could be implemented.

Project description:We conducted a 6-month prospective study in a newly opened ICU for high-resolution tracking of carbapenem-resistant Klebsiella pneumoniae (CRKP) through environmental surveillance, patient screening, and genome sequencing. Among all ICU patients (n = 348) screened, 3.5% carried CRKP on admission and 16.3% acquired CRKP thereafter. CRKP was not detected in the environment until 10 weeks and was then isolated from 98 of 2,989 environmental samples (3.3%). The first CRKP isolate from rectal swabs (n = 37) and the first clinical isolate (n = 8) of each patient as well as the 98 isolates from environmental were subjected to whole-genome sequencing. The 143 CRKP isolates from patients and environment samples were assigned to four sequence types, with ST11 dominating (95.8%) and further divided into 14 clones, suggesting introduction of multiple clones. Subsequent CRKP transmission was complex and dynamic with 10 clones found in multiple patients and seven also detected in the environment. Two particular ST11 clones caused extensive (≥5 rooms) and persistent (≥10 weeks) environmental contamination. Both clones were associated with patients who carried CRKP throughout their prolonged ICU stay. Such "super-contaminators" are a priority for isolation and environmental surveillance. IMPORTANCE Carbapenem-resistant Klebsiella pneumoniae (CRKP) is a global challenge for human health. In health care settings, patients have frequent interactions with other patients and the environment, rendering challenges for untangling the introduction and transmission of CRKP. We conducted a prospective surveillance study in a newly opened ICU for high-resolution tracking of CRKP. Our study demonstrated the dynamic, complicated transmission of CRKP and has important findings that may help to curb its spread in health care settings. First, compliance with basic measures such as routine environment cleaning and postdischarge terminal cleaning is needed to minimize the environmental contamination-driven spread. Second, active screening could demonstrate the scale of the problem, and room transfer of patients with CRKP should be prohibited whenever possible. Third, the priority for single-room isolation should be given to patients with prolonged carriage of CRKP, especially in resource-limited settings. Good infection control practice lays a foundation for tackling multidrug-resistant organisms like CRKP.

Project description:Carbapenem-resistantKlebsiella pneumoniae(CR-Kp) is significant threat to public health worldwide. The primary reservoir for CR-Kp is the intestinal tract, where the bacterium is usually present at low density, but can bloom following antibiotic treatment, mostly in hospital settings. The impact of disturbances in the intestinal environment on the fitness, survival, expansion, and drug susceptibility of this pathogen is not well-understood. Nevertheless, gaining such knowledge could lead to innovative intervention strategies for addressing colonization and infection. Here, we adopted anin vivomodel to examine the transcriptional adaptation of a CR-Kp clinical isolate to immune activation in the intestine. We report that as early as 6 hours following host treatment with anti-CD3 antibody, CR-Kp underwent rapid transcriptional changes including downregulation of genes involved in sugar utilization and amino acid biosynthesis, and upregulation of genes involved in amino acid uptake and catabolism, antibiotic resistance, and stress response. In agreement with these findings, the concentration of oxidative species and amino acids was increased in the mouse intestine following treatment. Genes encoding for proteins containing the domain of unknown function (DUF) 1471 were particularly upregulated, however their deletion did not impair CR-Kp fitness in vivoupon immune activation. Transcription factor enrichment analysis identified the global regulator cAMP-Receptor Protein CRP as a potential orchestrator of the observed transcriptional signature. In keeping with the recognized role of CRP in regulating utilization of alternative carbon sources, CRP deletion in CR-Kp resulted in strongly impaired gut colonization, but this effect was not amplified by immune activation. Thus, following intestinal colonization, which occurs in a CRP-dependent manner, CR-Kp can rapidly respond to immune cues by implementing a well-defined and complex transcriptional program whose direct relevance towards bacterial fitness remains cryptic. Further analyses utilizing this model may identify key factors to tackle the intestinal stage of CR-Kp colonization.

Project description:Carbapenem-resistant Klebsiella pneumoniae (CRKP) has become a critical public health threat. However, the association between intestinal colonization and parenteral infection among pediatric patients has not been elucidated. We collected 8 fecal CRKP strains and 10 corresponding CRKP strains responsible for extraintestinal infection from eight patients who did not manifest infection upon admission to the hospital. Paired isolates showed identical resistance to antimicrobials and identical virulence in vitro and in vivo. wzi capsule typing, multilocus sequence typing, and whole-genome sequencing (WGS) indicated high similarity between paired colonizing and infecting isolates. Mutations between colonizing and infecting isolate pairs found by WGS had a distinctive molecular signature of a high proportion of complex structural variants. The mutated genes were involved in pathways associated with infection-related physiological and pathogenic functions, including antibiotic resistance, virulence, and response to the extracellular environment. The latter is important for bacterial infection of environmental niches. Various mutations related to antibiotic resistance, virulence, and colonization that were not associated with any particular mutational hot spot correlated with an increased risk of extraintestinal infection. Notably, novel subclone carbapenem-resistant hypervirulent K. pneumoniae (CR-hvKP) KL19-ST15 exhibited hypervirulence in experimental assays that reflected the severe clinical symptoms of two patients infected with the clonal strains. Taken together, our findings indicate the association between CRKP intestinal colonization and extraintestinal infection, suggesting that active screening for colonization on admission could decrease infection risk in children. IMPORTANCE Carbapenem-resistant Klebsiella pneumoniae (CRKP) causes an increasing number of nosocomial infections, which can be life-threatening, as carbapenems are last-resort antibiotics. K. pneumoniae is part of the healthy human microbiome, and this provides a potential advantage for infection. This study demonstrated that CRKP intestinal colonization is strongly linked to extraintestinal infection, based on the evidence given by whole-genome sequencing data and phenotypic assays of antimicrobial resistance and virulence. Apart from these findings, our in-depth analysis of point mutations and chromosome structural variants in patient-specific infecting isolates compared with colonizing isolates may contribute insights into bacterial adaptation underlying CRKP infection. In addition, a novel subclone of carbapenem-resistant hypervirulent K. pneumoniae (CR-hvKP) was observed in the study. This finding highlights the importance of CRKP active surveillance among children, targeting in particular the novel high-risk CR-hvKP clone.

Dataset Information

Limited transmission of carbapenem-resistant Klebsiella pneumoniae between animals and humans: a study in Qingdao.

Publications

Limited transmission of carbapenem-resistant <i>Klebsiella pneumoniae</i> between animals and humans: a study in Qingdao.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets

Dataset Information

Limited transmission of carbapenem-resistant Klebsiella pneumoniae between animals and humans: a study in Qingdao.

Publications

Limited transmission of carbapenem-resistant &lt;i&gt;Klebsiella pneumoniae&lt;/i&gt; between animals and humans: a study in Qingdao.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets

Limited transmission of carbapenem-resistant <i>Klebsiella pneumoniae</i> between animals and humans: a study in Qingdao.