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Two artificial tears outbreak-associated cases of XDR Pseudomonas aeruginosa detected through whole genome sequencing-based surveillance.

ABSTRACT: We describe two cases of XDR Pseudomonas aeruginosa infection caused by a strain of public health concern recently associated with a nationwide outbreak of contaminated artificial tears. Both cases were detected through database review of genomes in the Enhanced Detection System for Hospital-Associated Transmission (EDS-HAT), a routine genome sequencing-based surveillance program. We generated a high-quality reference genome for the outbreak strain from one of the case isolates from our center and examined the mobile elements encoding bla _VIM-80 and bla _GES-9 carbapenemases. We then used publicly available P. aeruginosa genomes to explore the genetic relatedness and antimicrobial resistance genes of the outbreak strain.

SUBMITTER: Sundermann AJ

PROVIDER: S-EPMC10153325 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Two artificial tears outbreak-associated cases of XDR <i>Pseudomonas aeruginosa</i> detected through whole genome sequencing-based surveillance.

Sundermann Alexander J AJ Srinivasa Vatsala Rangachar VR Mills Emma G EG Griffith Marissa P MP Waggle Kady D KD Ayres Ashley M AM Pless Lora L Snyder Graham M GM Harrison Lee H LH Van Tyne Daria D

medRxiv : the preprint server for health sciences 20230417

We describe two cases of XDR <i>Pseudomonas aeruginosa</i> infection caused by a strain of public health concern recently associated with a nationwide outbreak of contaminated artificial tears. Both cases were detected through database review of genomes in the Enhanced Detection System for Hospital-Associated Transmission (EDS-HAT), a routine genome sequencing-based surveillance program. We generated a high-quality reference genome for the outbreak strain from one of the case isolates from our c ...[more]

PMID: 37131775

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Project description:In this study, we aimed to elucidate a prolonged outbreak of extensively drug-resistant (XDR) Pseudomonas aeruginosa, at two adjacent hospitals over a time course of 4 years. Since all strains exhibited a similar antibiotic susceptibility pattern and carried the carbapenemase gene blaVIM, a monoclonal outbreak was assumed. To shed light on the intra-hospital evolution of these strains over time, whole genome sequence (WGS) analysis of 100 clinical and environmental outbreak strains was employed. Phylogenetic analysis of the core genome revealed the outbreak to be polyclonal, rather than monoclonal as initially suggested. The vast majority of strains fell into one of two major clusters, composed of 27 and 59 strains, and their accessory genome each revealed over 400 and 600 accessory genes, respectively, thus indicating an unexpectedly high structural diversity among phylogenetically clustered strains. Further analyses focused on the cluster with 59 strains, representing the hospital from which both clinical and environmental strains were available. Our investigation clearly shows both accumulation and loss of genes occur very frequently over time, as reflected by analysis of protein enrichment as well as functional enrichment. In addition, we investigated adaptation through single nucleotide polymorphisms (SNPs). Among the genes affected by SNPs, there are a multidrug efflux pump (mexZ) and a mercury detoxification operon (merR) with deleterious mutations, potentially leading to loss of repression with resistance against antibiotics and disinfectants. Our results not only confirm WGS to be a powerful tool for epidemiologic analyses, but also provide insights into molecular evolution during an XDR P. aeruginosa hospital outbreak. Genome mutation unveiled a striking genetic plasticity on an unexpectedly high level, mostly driven by horizontal gene transfer. Our study adds valuable information to the molecular understanding of "real-world" Intra-hospital P. aeruginosa evolution and is a step forward toward more personalized medicine in infection control.

Project description:Most knowledge about Pseudomonas aeruginosa pathoadaptation is derived from studies on airway colonization in cystic fibrosis; little is known about adaptation in acute settings. P. aeruginosa frequently affects burned patients and the burn wound niche has distinct properties that likely influence pathoadaptation. This study aimed to genetically and phenotypically characterize P. aeruginosa isolates collected during an outbreak of infection in a burn intensive care unit (ICU). Sequencing reads from 58 isolates of ST1076 P. aeruginosa taken from 23 patients were independently mapped to a complete reference genome for the lineage (H25338); genetic differences were identified and were used to define the population structure. Comparative genomic analysis at single-nucleotide resolution identified pathoadaptive genes that evolved multiple, independent mutations. Three key phenotypic assays (growth performance, motility, carbapenem resistance) were performed to complement the genetic analysis for 47 unique isolates. Population structure for the ST1076 lineage revealed 11 evolutionary sublineages. Fifteen pathoadaptive genes evolved mutations in at least two sublineages. The most prominent functional classes affected were transcription/two-component regulatory systems, and chemotaxis/motility and attachment. The most frequently mutated gene was oprD, which codes for outer membrane porin involved in uptake of carbapenems. Reduced growth performance and motility were found to be adaptive phenotypic traits, as was high level of carbapenem resistance, which correlated with higher carbapenem consumption during the outbreak. Multiple prominent linages evolved each of the three traits in parallel providing evidence that they afford a fitness advantage for P. aeruginosa in the context of human burn infection. IMPORTANCE Pseudomonas aeruginosa is a Gram-negative pathogen causing infections in acutely burned patients. The precise mechanisms required for the establishment of infection in the burn setting, and adaptive traits underpinning prolonged outbreaks are not known. We have assessed genotypic data from 58 independent P. aeruginosa isolates taken from a single lineage that was responsible for an outbreak of infection in a burn ICU that lasted for almost 2.5 years and affected 23 patients. We identified a core set of 15 genes that we predict to control pathoadaptive traits in the burn infection based on the frequency with which independent mutations evolved. We combined the genotypic data with phenotypic data (growth performance, motility, antibiotic resistance) and clinical data (antibiotic consumption) to identify adaptive phenotypes that emerged in parallel. High-level carbapenem resistance evolved rapidly, and frequently, in response to high clinical demand for this antibiotic class during the outbreak.

Project description:BackgroundCarbapenem-resistant Pseudomonas aeruginosa (CRPA) are a serious cause of healthcare-associated infections. Part of the infection prevention and control measures are outbreak investigations (OI) of patients, healthcare workers (HCW), and the environment after identifying a CRPA in order to identify carriers and environmental reservoirs, so that targeted actions can be taken to prevent further transmission. However, little is known on when and how to perform such OI. Therefore, this systematic review aims to summarize OI performed after detection of CRPA in the endemic and epidemic hospital setting.Main textArticles related to our research question were identified through a literature research in multiple databases (Embase, Medline Ovid, Cochrane, Scopus, Cinahl, Web of Science, and Google Scholar) until January 12, 2022 (Prospero registration number CRD42020194165). Hundred-twenty-six studies were included. In both the endemic and the epidemic setting, a median number of two out of seven predefined components of OI were identified. In the endemic setting, the most frequent component of OI was screening of the environment (28 studies, 62.2%). In the epidemic setting, screening of the environment (72 studies, 88.9%), and screening of patients during hospitalization (30 studies, 37%) were most frequently performed. Only 19 out of 126 studies (15.1%) reported screening of contact patients, and 37 studies reported screening of healthcare workers (HCW, 29.4%).ConclusionDue to probable underreporting of OI in the literature, the available evidence for the usefulness of the individual components of OI is scarce. This could lead to inhomogeneous performance of OI after detection of CRPA in the healthcare setting, and with this, potential under- or overscreening. While we could show evidence for the usefulness for environmental screening in order to identify the mode of transmission, evidence for HCW screening is scarce and might not lead to the identification of modes of transmission. Further studies are needed to better understand CI in different settings and, finally, develop guidance on when and how to best perform OI.

Dataset Information

Two artificial tears outbreak-associated cases of XDR Pseudomonas aeruginosa detected through whole genome sequencing-based surveillance.

Publications

Two artificial tears outbreak-associated cases of XDR <i>Pseudomonas aeruginosa</i> detected through whole genome sequencing-based surveillance.

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