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Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Antimicrobial Agents and Resistance".

Deadline for manuscript submissions: closed (30 April 2023) | Viewed by 21486

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Dr. Dobroslava Bujňáková

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Institute of Animal Physiology, Centre of Biosciences of the Slovak Academy of Sciences, 040 01 Košice, Slovakia
Interests: Enterobacterales; virulence factors; antibiotic resistance; biofilm; quorum sensing
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Ivana Ćirković

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Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, dr Subotica 1, 11000 Belgrade, Serbia
Interests: Enterobacterales; antimicrobial resistance; biofilm; human medicine
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

This Special Issue is a continuation of our 2022 Special Issue "Virulence Factors and Antibiotic Resistance of Enterobacterales".

The heterogeneous group of Gram-negative bacteria such as Escherichia coli and non-Escherichia coli Enterobacterales (e.g., Klebsiella, Enterobacter, Citrobacter), which can colonize the gastrointestinal tract of humans and animals and persist as gut commensals without inducing any infections in the environment with balanced microbiota (colonization resistance), also harbor features responsible for virulence and pathogenicity, including “fitness factors” or phenotypes that may result in severe health concerns such as biofilm formation and/or multidrug resistance. Pathogenic Enterobacterales isolated from infected patients are the most often investigated, but fecal isolates from healthy subjects including food, companion, and wild animals and/or food or environmental strains should be a more frequent target, aiming to determine the pathogenic potential of a wider biodiversity reservoir.

This Special Issue invites researchers interested in Enterobacterales characterization concerning the presence of genes associated with virulence (adhesins; surface cellulose structures and curli; siderophores, e.g., enterobactin, aerobactin, and yersiniabactin; protectines; invasins or toxins), and bacterial-biofilm-associated phenotypes. Although not directly involved in pathogenicity, the acquisition of multiple antibiotic resistances strongly supports the success of opportunistic Enterobacterales pathogens in invasion, survival, and spread, and markedly complicates the treatment of infections. Not only pathogens but also commensal bacteria, considered harmless and part of the normal microbiota, are exposed to selection pressure and can be a reservoir of mobile genetic elements carrying antibiotic resistance genes. Therefore, the occurrence of drug-resistant bacteria within a commensal population and the possibility to exchange genetic material through horizontal gene transfer may represent a major health concern. Research papers, up-to-date review articles, and commentaries dealing with resistance, virulence, and biofilm in Enterobacterales are all welcome.

Dr. Dobroslava Bujňáková
Prof. Ivana Ćirković
Guest Editors

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Keywords

Enterobacterales
virulence factors
antibiotic resistance
biofilm
healthy and sick animals
commensal and pathogenic bacteria

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Published Papers (9 papers)

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Research

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22 pages, 7590 KiB

Open AccessArticle

Comparative De Novo and Pan-Genome Analysis of MDR Nosocomial Bacteria Isolated from Hospitals in Jeddah, Saudi Arabia

by Molook Alghamdi, Effat Al-Judaibi, Mohammed Al-Rashede and Awatif Al-Judaibi

Microorganisms 2023, 11(10), 2432; https://doi.org/10.3390/microorganisms11102432 - 28 Sep 2023

Viewed by 1699

Abstract

Multidrug-resistant (MDR) bacteria are one of the most serious threats to public health, and one of the most important types of MDR bacteria are those that are acquired in a hospital, known as nosocomial. This study aimed to isolate and identify MDR bacteria from selected hospitals in Jeddah and analyze their antibiotic-resistant genes. Bacteria were collected from different sources and wards of hospitals in Jeddah City. Phoenix BD was used to identify the strains and perform susceptibility testing. Identification of selected isolates showing MDR to more than three classes on antibiotics was based on 16S rRNA gene and whole genome sequencing. Genes conferring resistance were characterized using de novo and pan-genome analyses. In total, we isolated 108 bacterial strains, of which 75 (69.44%) were found to be MDR. Taxonomic identification revealed that 24 (32%) isolates were identified as Escherichia coli, 19 (25.3%) corresponded to Klebsiella pneumoniae, and 17 (22.67%) were methicillin-resistant Staphylococcus aureus (MRSA). Among the Gram-negative bacteria, K. pneumoniae isolates showed the highest resistance levels to most antibiotics. Of the Gram-positive bacteria, S. aureus (MRSA) strains were noticed to exhibit the uppermost degree of resistance to the tested antibiotics, which is higher than that observed for K. pneumoniae isolates. Taken together, our results illustrated that MDR Gram-negative bacteria are the most common cause of nosocomial infections, while MDR Gram-positive bacteria are characterized by a wider antibiotic resistance spectrum. Whole genome sequencing found the appearance of antibiotic resistance genes, including SHV, OXA, CTX-M, TEM-1, NDM-1, VIM-1, ere(A), ermA, ermB, ermC, msrA, qacA, qacB, and qacC. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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12 pages, 1677 KiB

Open AccessArticle

Detection of Plasmid-Mediated Resistance against Colistin in Multi-Drug-Resistant Gram-Negative Bacilli Isolated from a Tertiary Hospital

by Mario Galindo-Méndez, Humberto Navarrete-Salazar, Reinaldo Pacheco-Vásquez, Devanhí Quintas-de la Paz, Isabel Baltazar-Jiménez, José David Santiago-Luna and Laura Guadarrama-Monroy

Microorganisms 2023, 11(8), 1996; https://doi.org/10.3390/microorganisms11081996 - 3 Aug 2023

Cited by 2 | Viewed by 1450

Abstract

The aim of this study was to determine the prevalence of plasmid-mediated colistin resistance mcr-1 to mcr-5 genes among colistin and multi-drug-resistant Gram-negative bacilli strains isolated from patients in a tertiary hospital in Toluca, Mexico. The presence of mcr genes among the 241 strains collected was assessed by PCR. In the case of mcr-carrying E. coli, further PCR tests were performed to determine the presence of bla_CTX-M and whether the strains belonged to the O25b-ST131 clone. Conjugation experiments were also carried out to assess the horizontal transmission of colistin resistance. A total of twelve strains (5.0%), of which four were E. coli; four were P. aeruginosa; three were K. pneumoniae, and one E. cloacae, were found to be resistant to colistin. Of these strains, two E. coli isolates were found to carry mcr-1, and Southern blot hybridization demonstrated its presence on an approximately 60 kb plasmid. Both mcr-1-carrying E. coli strains were found to co-express bla_CTX-M, belong to the O25b-ST131 clone, and horizontally transmit their colistin resistance. The results of this study confirm the presence of plasmid-mediated colistin resistance in hospitalized patients in Mexico and demonstrated that the multi-drug-resistant O25b-ST131 E. coli clone can acquire mcr genes and transmit such resistance traits to other bacteria. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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17 pages, 946 KiB

Open AccessArticle

Occurrence and Molecular Study of Hypermucoviscous/Hypervirulence Trait in Gut Commensal K. pneumoniae from Healthy Subjects

by Dina M. Osama, Bishoy M. Zaki, Wafaa S. Khalaf, Marwa Yousry A. Mohamed, Mahmoud M. Tawfick and Heba M. Amin

Microorganisms 2023, 11(3), 704; https://doi.org/10.3390/microorganisms11030704 - 9 Mar 2023

Cited by 6 | Viewed by 2649

Abstract

Hypervirulent Klebsiella pneumoniae (hvKp) is emerging worldwide. Hypermucoviscousity is the characteristic trait that distinguishes it from classic K. pneumoniae (cKp), which enables Kp to cause severe invasive infections. This research aimed to investigate the hypermucoviscous Kp (hmvKp) phenotype among gut commensal Kp isolated from healthy individuals and attempted to characterize the genes encoding virulence factors that may regulate the hypermucoviscosity trait. Using the string test, 50 identified Kp isolates from healthy individuals’ stool samples were examined for hypermucoviscosity and investigated by transmission electron microscopy (TEM). Antimicrobial susceptibility profiles of Kp isolates were determined using the Kirby Bauer disc method. Kp isolates were tested for genes encoding different virulence factors by PCR. Biofilm formation was assayed by the microtiter plate method. All Kp isolates were multidrug-resistant (MDR). Phenotypically, 42% of isolates were hmvKp. PCR-based genotypic testing revealed the hmvKp isolates belonged to capsular serotype K2. All study Kp isolates harbored more than one virulence gene. The genes magA and rmpA were not detected, while the terW gene was present in all isolates. The siderophores encoding genes entB and irp2 were most prevalent in hmvKp isolates (90.5%) and non-hmvKp (96.6%), respectively. hmvKp isolates harbored the genes wabG and uge with rates of 90.5% and 85.7%, respectively. The outcomes of this research highlight the potential health risk of commensal Kp to cause severe invasive diseases, owing to being hmvKp and MDR, and harboring multiple virulence genes. The absence of essential genes related to hypermucoviscosity such as magA and rmpA in hmvKp phenotypes suggests the multifactorial complexity of the hypermucoviscosity or hypervirulence traits. Thus, further studies are warranted to verify the hypermucoviscosity-related virulence factors among pathogenic and commensal Kp in different colonization niches. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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11 pages, 1016 KiB

Open AccessCommunication

Colonization and Healthcare-Associated Infection of Carbapenem-Resistant Enterobacteriaceae, Data from Polish Hospital with High Incidence of Carbapenem-Resistant Enterobacteriaceae, Does Active Target Screening Matter?

by Iwona Pawłowska, Grzegorz Ziółkowski, Estera Jachowicz-Matczak, Michał Stasiowski, Mateusz Gajda and Jadwiga Wójkowska-Mach

Microorganisms 2023, 11(2), 437; https://doi.org/10.3390/microorganisms11020437 - 9 Feb 2023

Cited by 3 | Viewed by 2201

Abstract

The objective of the study was to analyse the incidence of carbapenem-resistant Enterobacteriaceae (CRE) at a provincial hospital from 2019–2021. Multiplex PCR was used to detect the presence of carbapenemase genes. There were 399 cases of CRE detected in total in the analysed period, including 104 healthcare-associated infections. Out of the isolated CRE, 97.7% were Klebsiella pneumoniae with OXA-48 or KPC genes. Overall, among the identified CRE genes, the most frequently present genes were the ones mediating oxacillinase OXA-48 (71%) and KPC (26%), and significantly less often New Delhi NDM metallo-β-lactamase (2.5%). Moreover, two isolates produced two carbapenemases, i.e., OXA-48 and KPC. The conducted research demonstrates that there is a constant need for continuous monitoring of the occurrence of CRE strains and the hospital antibiotic policy, as well as the implementation of procedures to prevent CRE transmission by medical personnel and hospital support staff. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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18 pages, 1657 KiB

Open AccessArticle

Susceptibility and Virulence of Enterobacteriaceae Isolated from Urinary Tract Infections in Benin

by Funkè F. Assouma, Haziz Sina, Tomabu Adjobimey, Agossou Damien Pacôme Noumavo, Akim Socohou, Bawa Boya, Ange D. Dossou, Lauriane Akpovo, Basile Boni Saka Konmy, Jacques F. Mavoungou, Adolphe Adjanohoun and Lamine Baba-Moussa

Microorganisms 2023, 11(1), 213; https://doi.org/10.3390/microorganisms11010213 - 14 Jan 2023

Cited by 9 | Viewed by 4208

Abstract

Enterobacteriaceae represent one of the main families of Gram-negative bacilli responsible for serious urinary tract infections (UTIs). The present study aimed to define the resistance profile and the virulence of Enterobacteriaceae strains isolated in urinary tract infections in Benin. A total of 390 urine samples were collected from patients with UTIs, and Enterobacteriaceae strains were isolated according to standard microbiology methods. The API 20E gallery was used for biochemical identification. All the isolated strains were subjected to antimicrobial susceptibility testing using the disc diffusion method. Extended-spectrum beta-lactamase (ESBL) production was investigated using a double-disc synergy test (DDST), and biofilm production was quantified using the microplate method. Multiplex PCR was used to detect uro-virulence genes, namely: PapG, IronB, Sfa, iucD, Hly, FocG, Sat, FyuA and Cnf, using commercially designed primers. More than 26% (103/390) of our samples were contaminated by Enterobacteriaceae strains at different levels. Thus, E. coli (31.07%, 32/103), Serratia marcescens (11.65%, 12/103), Klebsiella ornithinolytica (8.74%, 9/103), Serratia fonticola (7.77%, 8/103) and Enterobacter cloacae (6.80%, 7/103) were identified. Among the isolated strains, 39.81% (41/103) were biofilm-forming, while 5.83% (6/103) were ESBL-producing. Isolates were most resistant to erythromycin, cefixime, ceftriaxone and ampicillin (≥90%) followed by ciprofloxacin, gentamycin, doxycycline and levofloxacin (≥50%), and least resistant to imipenem (27.18%). In regard to virulence genes, Sfa was the most detected (28.15%), followed by IronB (22.23%), iucD (21.36%), Cnf (15.53%), PapG (9.71%), FocG (8.74%), Sat (6.79%), FyuA (5.82%) and Hyl (2.91%). These data may help improve the diagnosis of uropathogenic strains of Enterobacteriaceae, but also in designing effective strategies and measures for the prevention and management of severe, recurrent, or complicated urinary tract infections in Benin. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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13 pages, 866 KiB

Open AccessArticle

Whole Genome Sequencing Reveals Presence of High-Risk Global Clones of Klebsiella pneumoniae Harboring Multiple Antibiotic Resistance Genes in Multiple Plasmids in Mwanza, Tanzania

by Vitus Silago and Stephen E. Mshana

Microorganisms 2022, 10(12), 2396; https://doi.org/10.3390/microorganisms10122396 - 2 Dec 2022

Cited by 2 | Viewed by 2620

Abstract

Background: Klebsiella pneumoniae is an important multidrug-resistant (MDR) pathogen, causing both community- and healthcare-associated infections. The resistance is due to the continuous accumulation of multiple antibiotic-resistance-genes (ARGs) through spontaneous genomic mutations and the acquisition of conjugative plasmids. This study presents antibiotics resistance genes, plasmids replicons, and virulence genes of K. pneumoniae isolates from clinical specimens in a tertiary hospital, Mwanza, Tanzania. Methods: Whole genome sequencing (WGS) of 34 K. pneumoniae was performed, using an Illumina NextSeq 500, followed by in silco analysis. Results: A total of 34 extended-spectrum beta-lactamase-producing K. pneumoniae, isolated from blood samples from neonatal units were whole-genome sequenced. Of these, 28 (82.4%) had an identified sequence type (ST), with ST14 (39.3%, n = 11) being frequently identified. Moreover, 18 (52.9%) of the bacteria harbored at least one plasmid, from which a total of 25 plasmid replicons were identified with a predominance of IncFIB(K) 48.0% (n = 12). Out of 34 sequenced K. pneumoniae, 32 (94.1%) were harboring acquired antibiotic/biocides-resistance-genes (ARGs) with a predominance of bla_CTX-M-15 (90.6%), followed by oqxB (87.5%), oqxA (84.4%), bla_TEM-1B (84.4%) and sul2 (84.4%). Interestingly, we observed the ColRNAI plasmid-replicon (n = 1) and qacE gene (n = 4) for the first time in this setting. Conclusion: Global high-risk clones of K. pneumoniae isolates carry multiple ARGs in multiple plasmid-replicons. Findings from this study warrant genomic-based surveillance to monitor high-risk global clones, epidemic plasmids and ARGs in low- and middle-income countries. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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15 pages, 345 KiB

Open AccessArticle

Dissemination of High-Risk Clones Enterobacterales among Bulgarian Fecal Carriage Isolates

by Rumyana Markovska, Petya Stankova, Temenuga Stoeva, Marianna Murdjeva, Yulia Marteva-Proevska, Dobrinka Ivanova, Maryia Sredkova, Atanaska Petrova, Kalina Mihova and Lyudmila Boyanova

Microorganisms 2022, 10(11), 2144; https://doi.org/10.3390/microorganisms10112144 - 29 Oct 2022

Cited by 6 | Viewed by 1804

Abstract

The gastrointestinal tract is an important reservoir of high-risk Enterobacteria clones and a driver of antimicrobial resistance in hospitals. In this study, patients from six hospitals in four major Bulgarian towns were included in this study. Overall, 205 cefotaxime-resistant isolates (35.3%) of Enterobacterales order were detected in fecal samples among 580 patients during the period of 2017–2019. ESBL/carbapenemase/plasmidic AmpC producer rates were 28.8%, 2.4%, and 1.2%, respectively. A wide variety of ESBLs: CTX-M-15 (41%), CTX-M-3 (24%), CTX-M-27 (11%), and CTX-M-14 (4%) was found. The carbapenemases identified in this study were New Delhi metalo-β-lactamase (NDM)-1 (5.4%) and Klebsiella carbapenemase (KPC)-2 (1.5%). Most NDM-1 isolates also produced CTX-M-15/-3 and CMY-4 β-lactamases. They belonged to ST11 Klebsiella pneumoniae clone. The epidemiology typing revealed three main high-risk K. pneumoniae clones (26%)—ST11, ST258, and ST15 and five main Escherichia coli clones—ST131 (41.7%), ST38, ST95, ST405, and ST69. Sixty-one percent of ST131 isolates were from the highly virulent epidemic clone O25b:H4-ST131. Phylotyping revealed that 69% of E. coli isolates belonged to the virulent B2 and D groups. Almost all (15/16) Enterobacter isolates were identified as E. hormaechei and the most common ST type was ST90. Among all of the isolates, a high ESBL/carbapenemases/plasmid AmpC (32.4%) prevalence was observed. A significant proportion of the isolates (37%) were members of high-risk clones including two pan-drug-resistant K. pneumoniae ST11 NDM-1 producing isolates. Due to extensive antibiotic usage during COVID-19, the situation may worsen, so routine screenings and strict infection control measures should be widely implemented. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

18 pages, 529 KiB

Open AccessArticle

Antibiotic Susceptibility Profiles and Resistance Mechanisms to β-Lactams and Polymyxins of Escherichia coli from Broilers Raised under Intensive and Extensive Production Systems

by Mariana Ferreira, Célia Leão, Lurdes Clemente, Teresa Albuquerque and Ana Amaro

Microorganisms 2022, 10(10), 2044; https://doi.org/10.3390/microorganisms10102044 - 16 Oct 2022

Cited by 2 | Viewed by 2058

Abstract

The intensive and extensive broiler production systems imply different veterinary interventions, including the use of antimicrobials. This study aimed to compare the antimicrobial susceptibility profiles of Escherichia coli isolated from both systems, characterize resistance mechanisms to β-lactams and polymyxins, and identify genetic elements such as integrons. E. coli isolates recovered from broiler cecal samples were assayed for antimicrobial susceptibility through the broth microdilution technique. The molecular characterization of acquired resistance mechanisms to β-lactams and colistin and the detection of integrons was performed by a multiplex PCR. For most antibiotics tested, the prevalence of reduced susceptibility is higher in commensal and extended-spectrum β-lactamases (ESBL)/AmpC producers from broilers raised in the intensive system, compared with those raised under extensive conditions. SHV-12 was the most common ESBL enzyme found in both production systems. Other ESBL variants such as CTX-M-1, CTX-M-55, CTX-M-14, CTX-M-32, CTX-M-9, TEM-52, and plasmid-encoded AmpC enzyme CMY-2 were also present. MCR-1 was identified in a colistin-resistant isolate from broilers raised under the intensive system. This study highlights the differences in E. coli antibiotic susceptibility from both production types and emphasizes that a great deal of work remains to decrease consumption and antimicrobial resistance levels. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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Review

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15 pages, 696 KiB

Open AccessReview

Epidemiology of Cefotaxime-Hydrolysing β-Lactamase-Producing Escherichia coli in Children with Diarrhoea Reported Globally between 2012 and 2022

by Simbarashe Karambwe, Afsatou Ndama Traoré and Natasha Potgieter

Microorganisms 2024, 12(1), 171; https://doi.org/10.3390/microorganisms12010171 - 15 Jan 2024

Cited by 1 | Viewed by 1414

Abstract

The global spread of cefotaxime-hydrolysing β-lactamase (CTX-M)-producing Escherichia coli (E. coli) and its associated impact on paediatric diarrhoeal treatment and management has become a public health concern. This review assessed surveillance studies on CTX-M-producing E. coli associated with diarrhoea in children published between 2012 and 2022 globally. A total of thirty-eight studies were included for data analysis, categorised into continental regions, and tabulated. The majority (68%) of studies were conducted in Asian countries while few studies were conducted in Europe (11%) and Africa (18%), respectively. On the African continent, the majority (11%) of studies were conducted in Northern Africa while no studies were reported in East Africa. On the American continent, 3% of the studies were reported from South America. The studies included were classified into diarrheagenic E. coli (74%; 28/38) and faecal carriage (26%; 10/38). Of all the E. coli pathotypes associated with CTX-M production, EPEC was frequently reported. The prevalence of CTX-M-producing E. coli including the CTX-M-15-producing variants ranged between 1% and 94%. About 37% of the studies generalised the report as bla_CTX-M-positive E. coli. The use of sequencing in characterising the CTX-M-producing E. coli was reported in only 32% of all the studies. This review provides information on the epidemiology of CTX-M-15-producing E. coli in paediatric diarrhoea and the extent to which surveillance is being performed. This is relevant in informing clinical practice for the management of diarrhoea as well as the design of future surveillance studies. Full article

(This article belongs to the Special Issue Virulence Factors and Antibiotic Resistance of Enterobacterales 2.0)

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