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Virulence and Resistance of Klebsiella pneumoniae

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Medical Microbiology".

Deadline for manuscript submissions: closed (30 November 2021) | Viewed by 28642

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Dr. Aida Duarte

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1. Faculdade de Farmacia, Universidade de Lisboa, Department of Microbiology and Immunology, Lisbon, Portugal
2. Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Instituto Universitário Egas Moniz (IUEM), Caparica, Portugal
Interests: biochemistry, environmental exposures; microbiology; antibiotics; bacterial virulence
Special Issues, Collections and Topics in MDPI journals

Dr. Cátia Caneiras

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1. Microbiology Research Laboratory in Environmental Health (EnviHealthMicro Lab), Institute of Environmental Health (ISAMB), Faculty of Medicine, University of Lisboa, 1649-026 Lisboa, Portugal
2. Institute of Preventive Medicine and Public Health (IMP&SP), University of Lisboa, 1649-026 Lisboa, Portugal
3. Microbiology and Immunology Department, Faculty of Pharmacy, University of Lisboa, 1649-033 Lisboa, Portugal
4. Centro de Investigação Interdisciplinar Egas Moniz (CiiEM), Instituto Universitário Egas Moniz (IUEM), Caparica, Portugal
Interests: klebsiella pneumoniae complex; gram-negative pathogens; enterobacteriacea; virulence factors; antimicrobial resistance; extended-spectrum β-lactamases (ESBL); carbapenemases; home care services; quality of health care; respiratory diseases; pulmonary rehabilitation; oxygen; non-invasive ventilation; sleep care; e-health
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Klebsiella pneumoniae is an important opportunistic Gram-negative pathogen that belongs to the Enterobacteriaceae family, which is frequently associated with severe healthcare-associated infections (HAI) as well as community-acquired infections. It can cause different types of infection such as pneumonia, urinary tract infection, skin or soft tissue infection, meningitis, pyogenic liver abscess, and bacteremia potentially developing into sepsis. It is believed that the gastrointestinal tract is the most important reservoir for the transmission of K. pneumoniae. However, in contrast to many other bacterial pathogens, K. pneumoniae is ubiquitous in nature, and environmental reservoirs can also have a relevant role in human infections. Infections resulting from multidrug-resistant (MDR), extended-spectrum beta-lactamase (ESBL), and/or carbapenemase-producing K. pneumoniae strains are a challenge due to the lack of vaccines and therapeutic options. Several virulence factors, such as adherence and invasion factors, toxins, capsules, and siderophores, can be involved in the pathogenic mechanisms, namely, invasion of the host, disease induction, and the evasion of host defenses. The coexistence of antimicrobial resistance genes with other advantageous determinants such as virulence factors can have a significant impact on bacterial pathogenicity. Moreover, recent population diversity studies have shown that K. pneumoniae is in fact part of a complex of species. The aim of this Special Issue is to give an updated insight into K. pneumonia-complex resistance and virulence determinants, and the interplay of these factors. For this purpose, we welcome the submission of research articles, review articles, and short communications related to the various aspects of K. pneumonia-complex infection, with particular emphasis on antimicrobial resistance, its transmissibility, molecular pathways, the coexistence of virulence factors, biomarkers, clinical and environmental reservoirs, high-risk clones, whole genome sequencing characterization, in vivo infection models, and bacterial pathogenicity.

Prof. Dr. Aida Duarte
Prof. Dr. Cátia Caneiras
Guest Editors

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Keywords

Klebsiella pneumoniae complex
virulence factors
antimicrobial resistance
extended-spectrum β-lactamases (ESBL)
carbapenemase producers
molecular epidemiology
bacterial pathogenicity

Published Papers (8 papers)

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Research

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13 pages, 726 KiB

Open AccessArticle

Correlation between Polymerase Chain Reaction Identification of Iron Acquisition Genes and an Iron-Deficient Incubation Test for Klebsiella pneumoniae Isolates from Bovine Mastitis

by Takeshi Tsuka, Soma Kumashiro, Tsubasa Kihara and Toshiko Iida

Microorganisms 2022, 10(6), 1138; https://doi.org/10.3390/microorganisms10061138 - 31 May 2022

Viewed by 1823

Abstract

We investigated the correlation between the polymerase chain reaction (PCR) identification of six virulence genes associated with siderophore activation and the iron-uptake system (iron-acquisition genes; iucA, entB, fepA, ybtS, psn, and kfu) in mastitis-associated Klebsiella pneumoniae (K. pneumoniae). The growth of 37 K. pneumoniae isolates from the milk of cows with mild mastitis reared on Japanese dairy farms between October 2012 and December 2014 was examined by incubation in an iron-deficient medium. entB-, fepA-, or ybtS-positive isolates grew significantly better than entB-, fepA-, or ybtS-negative isolates after incubating in an iron-deficient medium for three days. Interestingly, the growth of isolates with 0 and ≥4 PCR-positive iron-acquisition genes in the iron-deficient medium were significantly different by day 2, while isolates with 2, 3, and ≥4 PCR-positive iron-acquisition genes grew significantly better than those with no PCR-positive iron-acquisition genes by day 3. Based on the correlation between the results of PCR and iron-deficient incubation tests, iron-deficient incubation for three days can be used to estimate the presence or absence of iron-acquisition genes in mastitis-associated K. pneumoniae. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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17 pages, 1272 KiB

Open AccessArticle

Whole-Genome Sequencing Enables Molecular Characterization of Non-Clonal Group 258 High-Risk Clones (ST13, ST17, ST147 and ST307) among Carbapenem-Resistant Klebsiella pneumoniae from a Tertiary University Hospital Centre in Portugal

by Gabriel Mendes, João F. Ramalho, Ana Bruschy-Fonseca, Luís Lito, Aida Duarte, José Melo-Cristino and Cátia Caneiras

Microorganisms 2022, 10(2), 416; https://doi.org/10.3390/microorganisms10020416 - 11 Feb 2022

Cited by 10 | Viewed by 2162

Abstract

The carbapenem-resistant Enterobacterales (CRE) strains have been identified by the World Health Organization as critical priority pathogens in research and development of diagnostics, treatments, and vaccines. However, recent molecular information about carbapenem-resistant K. pneumoniae (CRK) epidemiology in Portugal is still scarce. Thus, this study aimed to provide the molecular epidemiology, resistome, and virulome of CRK clinical strains recovered from a tertiary care hospital centre (2019–2021) using polymerase chain reaction (PCR) and the advanced molecular technique whole-genome sequencing (WGS). PCR amplification of carbapenemase genes was performed in 437 carbapenem-resistant K. pneumoniae strains. The most frequent carbapenemases were: KPC-3 (42%), followed by OXA-181 (20%), GES-5 (0.2%), and NDM-1 (0.2%). Additionally, 10 strains (2%) coproduced KPC-3 and OXA-181, and 1 strain coproduced KPC-3 and OXA-48 (0.2%). The genomic population structure of 68 strains characterized by WGS demonstrated the ongoing dissemination of four main high-risk clones: ST13, ST17, ST147, and ST307, while no clones belonging to the European predominant clonal groups (CG15 and CG258) were found. Moreover, we describe one K. pneumoniae ST39-KL62 that coproduced the NDM-1 carbapenemase and the extended-spectrum beta-lactamase CTX-M-15, and one K. pneumoniae ST29-KL54 GES-5 and BEL-1 coproducer. Furthermore, a high prevalence of iron siderophores were present in all CRK strains, with several strains presenting both colibactin and the hypermucoviscosity phenotype. Thus, the data presented here highlight an uncommon molecular epidemiology pattern in Portugal when compared with most European countries, further supporting the emergence and dissemination of nonclonal group 258 hypervirulent multidrug high-risk clones and the need to promote in-depth hospital molecular surveillance studies. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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13 pages, 1660 KiB

Open AccessArticle

Hypervirulent Klebsiella pneumoniae Strains Modulate Human Dendritic Cell Functions and Affect T_H1/T_H17 Response

by Sabrina Nicolò, Giorgio Mattiuz, Alberto Antonelli, Fabio Arena, Vincenzo Di Pilato, Tommaso Giani, Ilaria Baccani, Ann Maria Clemente, Giuseppe Castronovo, Michele Tanturli, Federico Cozzolino, Gian Maria Rossolini and Maria Gabriella Torcia

Microorganisms 2022, 10(2), 384; https://doi.org/10.3390/microorganisms10020384 - 07 Feb 2022

Cited by 6 | Viewed by 2379

Abstract

Hypervirulent Klebsiella pneumoniae (Hv-Kp) strains have emerged as pathogens causing life-threatening, invasive disease even in immunocompetent hosts. Systemic dissemination usually occurs following perturbations of the gut microbiota and is facilitated by Hv-Kp resistance to phagocytosis and complement activity. Hv-Kp are usually associated with K1 or K2 capsular types, produce several iron uptake systems (e.g., aerobactin and salmochelin) and are often but not invariably, capsular material hyper-producers (hypermucoviscous phenotype: HMV). Whether Hv-Kp escape the immune response at mucosal site is unknown. In this work, we studied the effects of Hv-Kp on human dendritic cells (DCs), central players of the IL-23/IL-17 and IL-12/IFN-γ axis at mucosal sites, essential for pathogen clearance. Four Hv-Kp and HMV strains were selected and their activity on DC maturation and cytokine production was compared to that of non-virulent Kp strains with classic or HMV phenotypes. While the maturation process was equally induced by all Kp strains, significant differences between virulent and non-virulent strains were found in the expression of genes for cytokines involved in T-cell activation and differentiation. The non-virulent KP04C62 and the classic Kp, KPC157 induced high expression of T_H1 (IL-12p70 and TNFα) and T_H17 cytokines (IL-23, IL-1β and IL-6), while Hv-Kp poorly activated these cytokine genes. Moreover, conditioned media from DCs cultured with non-virulent Kp, either classical or hypercapsulated, induced the activation of IL-17 and IFN-γ genes in preactivated CD4⁺-cells suggesting their T_H17/T_H1 differentiation. Conditioned media from Hv-Kp poorly activated IL-17 and IFN-γ genes. In summary, our data indicate that Hv-Kp interfere with DC functions and T-cell differentiation and suggest that the escape from the IL-23/IL-17 and IL-12/IFN-γ axes may contribute to pathogen dissemination in immunocompetent hosts. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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14 pages, 789 KiB

Open AccessArticle

First Outbreak of NDM-1-Producing Klebsiella pneumoniae ST11 in a Portuguese Hospital Centre during the COVID-19 Pandemic

by Gabriel Mendes, João F. Ramalho, Aida Duarte, Adriana Pedrosa, Ana Cristina Silva, Lucía Méndez and Cátia Caneiras

Microorganisms 2022, 10(2), 251; https://doi.org/10.3390/microorganisms10020251 - 23 Jan 2022

Cited by 19 | Viewed by 4114

Abstract

New Delhi metallo-β-lactamase (NDM) carbapenemase has been considered a global threat due to its worldwide widespread in recent years. In Portugal, a very low number of infections with NDM-producing Enterobacterales has been reported. A total of 52 strains from 40 patients and 1 environmental sample isolated during COVID-19 pandemic were included in this study. Wholegenome sequencing (WGS) was performed on 20 carbapenemase-producing strains, including 17 NDM-1-producing Klebsiella pneumoniae ST11-KL105 lineage strains, one NDM-1-producing Escherichia coli ST58 strain and one KPC-3-producing K. pneumoniae ST147 strain, recovered from a total of 19 patients. Of interest, also one NDM-1-producing K. pneumoniae ST11-KL105 was collected from the hospital environment. Genome-wide phylogenetic analysis revealed an ongoing dissemination of NDM-1-producing K. pneumoniae ST11 strains (n = 18) with the same genetic features seen across multiple wards. Furthermore, the ST58 E. coli strain, collected from a patient rectal swab that was also colonised with a K. pneumoniae strain, also showed the IncFIA plasmid replicon and the bla_NDM-1 gene (preceded by IS30 and followed by genes ble_MBL, trpF, dsbC, cutA, groES and groEL). The bla_NDM-1 is part of Tn125-like identical to those reported in Poland, Italy and India. The bla_KPC-3 K. pneumoniae ST147-KL64 strain has the genetic environment Tn4401d isoform. In conclusion, herein we report the molecular epidemiology, resistome, virulome and mobilome of the first NDM-1 carbapenemase outbreak caused by K. pneumoniae ST11-KL105 lineage during the COVID-19 pandemic in Portugal. Moreover, the outbreak strains characterised included seventeen different patients (infected and colonised) and one environmental sample which also emphasises the role of commensal and hospital environment strains in the dissemination of the outbreak. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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9 pages, 8769 KiB

Open AccessFeature PaperArticle

Colistin Dependency among Colistin-Heteroresistant Acinetobacter baumannii Isolates

by Hadas Kon, Amichay Hameir, Elizabeth Temkin, Alona Keren-Paz, David Schwartz, Vered Schechner and Yehuda Carmeli

Microorganisms 2022, 10(1), 58; https://doi.org/10.3390/microorganisms10010058 - 28 Dec 2021

Cited by 4 | Viewed by 1617

Abstract

Colistin dependent (CD) isolates are dependent on colistin for optimal growth. Here we aimed to systematically determine the emergence of CD among colistin-heteroresistant carbapenem-resistant Acinetobacter baumannii (CRAB) isolates. We also examined the phenotypic characteristics of CD and the evolution of CD strains to overt resistance. Additionally, we examined whether detection of growth in blood cultures was impaired by CD. Heteroresistant isolates, as determined by population analysis profiling, were exposed to colistin; when the colony count with colistin was significantly higher than without, isolates were suspected to be CD. CD was confirmed by Etest and growth curves. CD strains with colistin minimum inhibitory concentrations > 2 mg/L after growth in colistin-free media were considered colistin-resistant. Of the 65 heteroresistant strains tested, eight became CD after colistin exposure. These strains attained higher colony counts and growth rates with colistin vs. without, and grew adjacent to the colistin Etest strip. CD strains exhibited increased susceptibilities to multiple antibiotics compared to their parent heteroresistant strains. All CD strains tested became colistin-resistant following growth without colistin. CD strains were detected in blood culture bottles, but time to detection was significantly prolonged compared with parent strains, suggesting that CD may lead to delay in detection of CRAB bacteremia. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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18 pages, 1088 KiB

Open AccessArticle

Genomic Epidemiology of Carbapenemase Producing Klebsiella pneumoniae Strains at a Northern Portuguese Hospital Enables the Detection of a Misidentified Klebsiella variicola KPC-3 Producing Strain

by João Perdigão, Cátia Caneiras, Rita Elias, Ana Modesto, Anton Spadar, Jody Phelan, Susana Campino, Taane G. Clark, Eliana Costa, Maria José Saavedra and Aida Duarte

Microorganisms 2020, 8(12), 1986; https://doi.org/10.3390/microorganisms8121986 - 13 Dec 2020

Cited by 15 | Viewed by 2774

Abstract

The evolutionary epidemiology, resistome, virulome and mobilome of thirty-one multidrug resistant Klebsiella pneumoniae clinical isolates from the northern Vila Real region of Portugal were characterized using whole-genome sequencing and bioinformatic analysis. The genomic population structure was dominated by two main sequence types (STs): ST147 (n = 17; 54.8%) and ST15 (n = 6; 19.4%) comprising four distinct genomic clusters. Two main carbapenemase coding genes were detected (bla_KPC-3 and bla_OXA-48) along with additional extended-spectrum β-lactamase coding loci (bla_CTX-M-15, bla_SHV-12, bla_SHV-27, and bla_SHV-187). Moreover, whole genome sequencing enabled the identification of one Klebsiella variicola KPC-3 producer isolate previously misidentified as K. pneumoniae, which in addition to the bla_KPC-3 carbapenemase gene, bore the chromosomal broad spectrum β-lactamase bla_LEN-2 coding gene, oqxAB and fosA resistance loci. The bla_KPC-3 genes were located in a Tn4401b transposon (K. variicolan = 1; K. pneumoniaen = 2) and Tn4401d isoform (K. pneumoniaen = 28). Overall, our work describes the first report of a bla_KPC-3 producing K. variicola, as well as the detection of this species during infection control measures in surveillance cultures from infected patients. It also highlights the importance of additional control measures to overcome the clonal dissemination of carbapenemase producing clones. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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Review

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29 pages, 2390 KiB

Open AccessReview

From Klebsiella pneumoniae Colonization to Dissemination: An Overview of Studies Implementing Murine Models

by Laura Joseph, Thomas Merciecca, Christiane Forestier, Damien Balestrino and Sylvie Miquel

Microorganisms 2021, 9(6), 1282; https://doi.org/10.3390/microorganisms9061282 - 12 Jun 2021

Cited by 22 | Viewed by 8701

Abstract

Klebsiella pneumoniae is a Gram-negative pathogen responsible for community-acquired and nosocomial infections. The strains of this species belong to the opportunistic group, which is comprised of the multidrug-resistant strains, or the hypervirulent group, depending on their accessory genome, which determines bacterial pathogenicity and the host immune response. The aim of this survey is to present an overview of the murine models mimicking K. pneumoniae infectious processes (i.e., gastrointestinal colonization, urinary, pulmonary, and systemic infections), and the bacterial functions deployed to colonize and disseminate into the host. These in vivo approaches are pivotal to develop new therapeutics to limit K. pneumoniae infections via a modulation of the immune responses and/or microbiota. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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6 pages, 1180 KiB

Open AccessCase Report

Hypervirulent Klebsiella pneumoniae of Lineage ST66-K2 Caused Tonsillopharyngitis in a German Patient

by Kathleen Klaper, Sebastian Wendt, Christoph Lübbert, Norman Lippmann, Yvonne Pfeifer and Guido Werner

Microorganisms 2021, 9(1), 133; https://doi.org/10.3390/microorganisms9010133 - 08 Jan 2021

Cited by 14 | Viewed by 3138

Abstract

Hypervirulent Klebsiella pneumoniae (hvKp) is a novel pathotype that has been rarely described in Europe. This study characterizes a hvKp isolate that caused a community-acquired infection. The hypermucoviscous Klebsiella pneumoniae (K. pneumoniae) strain 18-0005 was obtained from a German patient with tonsillopharyngitis in 2017. Antibiotic susceptibility testing was performed and the genome was sequenced by Illumina and Nanopore technology. Whole genome data were analyzed by conducting core genome multilocus sequence typing (cgMLST) and single nucleotide polymorphism (SNP) analysis. Virulence genes were predicted by applying Kleborate. Phenotypic and whole genome analyses revealed a high similarity of the study isolate 18-0005 to the recently reported antibiotic-susceptible hvKp isolate SB5881 from France and the “ancestral” strain Kp52.145; both were assigned to the ST66-K2 lineage. Comparative genomic analysis of the three plasmids showed that the 18-0005 plasmid II differs from SB5881 plasmid II by an additional 3 kb integrated fragment of plasmid I. Our findings demonstrate the genetic flexibility of hvKp and the occurrence of a strain of the clonal group CG66-K2 in Germany. Hence, it emphasizes the need to improve clinical awareness and infection monitoring of hvKp. Full article

(This article belongs to the Special Issue Virulence and Resistance of Klebsiella pneumoniae)

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