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Anna VenturaDepartment of Diagnostics and Public Health, University of Verona, Verona, Italy

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Elena AddisDepartment of Diagnostics and Public Health, University of Verona, Verona, Italy

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Anna BertoncelliDepartment of Diagnostics and Public Health, University of Verona, Verona, Italy

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Annarita MazzariolDepartment of Diagnostics and Public Health, University of Verona, Verona, Italy

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https://orcid.org/0000-0003-2729-1007
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Abstract

This study focused on the characterization of 19 hypermucoviscous Klebsiella pneumoniae strains, that were identified from 26 hypermucosal strains. In order to identify hypermucoviscous strains of K. pneumoniae, the string test was applied. This phenotype is known in the literature as one of the virulence factors of this species together with the production of biofilm and other hypervirulence factor genes such as: rmpA, rmpA2, iucA, iroB, peg-344. We also investigated presence of magA gene that correlates with the hyper-production of capsule of K1 serotype. Of the strains under study, 13 out of 19 harboured at least one virulence factor.

Sequence type (ST) was determined in order to identify known high-risk clones or new emerging high-risk clones and their variability in a single clinical setting. Important STs found among these strains were ST65 and ST29. Carbapenem resistance was also investigated and 4 out of 19 strains harboured at least a carbapenemase: one strain harboured a KPC enzyme alone, one strain carried a KPC and an OXA-48 like, one strain produced OXA-48-like alone, and the last strain harboured two metallo-β-lactamases (VIM-1 and NDM-5) plus OXA-48-like. In particular, this latter strain belongs to ST383, which was recently reported in Northern Italy as a hypervirulent and XDR strain.

The global spread of hypervirulent K. pneumoniae is an important epidemiological issue that should be considered in diagnostic and therapeutic managements of patients with K. pneumoniae infections.

Abstract

This study focused on the characterization of 19 hypermucoviscous Klebsiella pneumoniae strains, that were identified from 26 hypermucosal strains. In order to identify hypermucoviscous strains of K. pneumoniae, the string test was applied. This phenotype is known in the literature as one of the virulence factors of this species together with the production of biofilm and other hypervirulence factor genes such as: rmpA, rmpA2, iucA, iroB, peg-344. We also investigated presence of magA gene that correlates with the hyper-production of capsule of K1 serotype. Of the strains under study, 13 out of 19 harboured at least one virulence factor.

Sequence type (ST) was determined in order to identify known high-risk clones or new emerging high-risk clones and their variability in a single clinical setting. Important STs found among these strains were ST65 and ST29. Carbapenem resistance was also investigated and 4 out of 19 strains harboured at least a carbapenemase: one strain harboured a KPC enzyme alone, one strain carried a KPC and an OXA-48 like, one strain produced OXA-48-like alone, and the last strain harboured two metallo-β-lactamases (VIM-1 and NDM-5) plus OXA-48-like. In particular, this latter strain belongs to ST383, which was recently reported in Northern Italy as a hypervirulent and XDR strain.

The global spread of hypervirulent K. pneumoniae is an important epidemiological issue that should be considered in diagnostic and therapeutic managements of patients with K. pneumoniae infections.

Introduction

In recent years, Klebsiella pneumoniae has gained notoriety as an infectious agent due to its increase in number of serious infections and its increasing resistance to antibiotic therapy. Furthermore, additional genetic traits associated with hypervirulence, and antibiotic resistance have recently been identified that make K. pneumoniae infection an increasingly emergency problem [1].

It is important to differentiate between classical K. pneumoniae (cKp) strains that typically cause nosocomial infections, now found worldwide and hypervirulent (hvKp) strains that cause severe, community-acquired systemic infections in otherwise healthy individuals, an emergency that initially worried only Asian countries but it is now rapidly expanding [2].

In 1986, Liu et al. [3] reported the first seven clinical cases of invasive K. pneumoniae infection in community individuals who presented with a liver abscess in the absence of biliary tract disease and these K. pneumoniae strains were defined as hypervirulent. Notably, hvKp strains cause primary liver abscesses in patient populations that do not appear to have any underlying liver disease. In turn, liver abscesses can give rise to a number of other secondary infections due to hematogenous spread from the liver [4].

To date, there are four major classes of virulence factors that have been characterized well in K. pneumoniae: capsule, including the production of hypercapsule in hvKp strains; lipopolysaccharide (LPS); siderophores; and type 1 and 3 fimbriae. Siderophores play an important role in virulence, and hv K. pneumoniae encodes for salmochelin, aerobactin, other than enterobactin, and yersiniabactin, the last of which is also produced by cKp strains. Salmochelin is a form of c-glucosylated enterobactin encoded by the iroA gene. It is present in only about 2–4% of nosocomial K. pneumoniae strains but is much more prevalent in hv K. pneumoniae strains. Aerobactin is a citrate-hydroxamate siderophore encoded by the iucA gene; it is expressed rarely by classical nosocomial clinical isolates of K. pneumoniae but it is present in 93–100% of hvKp isolates [2].

Currently, magA is defined as an essential gene for the formation of the biosynthesis of K1 capsular polysaccharides but it is not an independent specific virulence gene in strains of K. pneumoniae that cause liver abscesses [5].

Clinical laboratories are currently still in the midst of studying the differentiation between hvKp and cKp. Increased capsule production and aerobactin production have been identified as specific virulence factors for the hypermucoviscous phenotype; in addition to these elements, it has been shown that several biomarkers and quantitative production of siderophores accurately predict hvKp strains [6].

Klebsiella pneumoniae is known for its propensity to collect resistance plasmids. Extensive use of carbapenems has led to the emergence and rapid spread of carbapenemase-producing strains. The types of carbapenemases prevalent in K. pneumoniae are: K. pneumoniae carbapenemase (KPC)-type enzymes; New Delhi metallo-β-lactamase (NDM)-type enzymes; and oxacillinase (OXA)-type enzymes, mainly OXA-48 [7].

The aim of this study is the identification of hypermucoviscous and hypervirulent strains through the molecular and phenotypic characterization of 19 isolates of multidrug-resistant (MDR) and non-MDR K. pneumoniae. This work stems from an ongoing health emergency, since the failure to recognize the increasingly dangerous factors of hypervirulence and resistance could lead to underestimate the risky circulation of these strains.

Materials and methods

Bacterial strains

The study included a collection of 26 strains of K. pneumoniae that have been isolated at Microbiology and Virology Hospital Service in Verona, Italy in the year 2021 and collected from blood cultures and abscesses during routine clinical analysis. All strains were identified by Maldi-tof Vitek MS (BioMérieux, France).

Antimicrobial susceptibility determination

Antimicrobial susceptibility tests for carbapenems were performed by disc diffusion method following the EUCAST (European Committee on Antimicrobial Susceptibility Testing) guideline. The results were interpreted using the breakpoints table of Enterobacterales on EUCAST's website [8].

String test

The string test is a simple, rapid, and readily available screening method that confirms a known virulence factor of K. pneumoniae, the hypermucoviscous phenotype. Furthermore, not all mucoid strains of K. pneumoniae show a positive string test, therefore a colonial mucoid appearance does not equate to a hypermucoviscous phenotype [9]. This phenomenon highlights a clear difference between the classic capsular mucoid strains and the hypermucoviscous variants [10]. The test is positive when there is formation of a viscous string of in > 5 mm in length when a loop is used to stretch the colony on an agar plate [11].

Hypervirulence factor detection

Hypervirulence factors of hypermucoviscous strains were detected by Polymerase Chain Reaction (PCR) using primers and thermal profiles reported earlier [12]. The marker genes used to distinguish hvKp from cKp are: rmpA/rmpA2 encoding regulator of mucoid phenotype (hypermucoid); iucA gene in the locus of aerobactin siderophore; iroB gene in the locus of salmochelin siderophore; and peg-344, which is a putative transporter. To determine the presence of magA gene, a PCR was performed using primers and conditions already reported [13].

Carbapenemase detection

The CARBA NP phenotypic test [14] was used for the rapid detection of carbapenemase production in Enterobacterales. Molecular characterization of carbapenemase genes (blaVIM, blaIMP, blaNDM, blaKPC and blaOXA-48) was performed by PCR [15].

Multilocus Sequence Typing (MLST)

MLST analysis was conducted through simplex PCRs for seven different housekeeping genes as described on the Institute Pasteur website [16, 17]. The MLST PCR products were purified through the QIAquick PCR Purification Kit and then sequenced at Eurofins Genomics (Germany, Ebersberg) in order to obtain sequence-typing (ST).

In vitro biofilm production

The production of biofilm was also analysed through the crystal violet test performed on a microtiter plate, and the optical density was measured in the plate at 550 nm through a fluorescence microplate reader. The results obtained were then subjected to the analysis described by Stepanovic et al. [18].

Results and discussion

To date K. pneumoniae is recognized as an urgent threat to human health due to the emergence of multidrug-resistant strains associated with hospital outbreaks as well as due to hypervirulent strains associated with severe community-acquired infections. Therefore, the convergence of virulence and resistance genes could potentially soon lead to the emergence of invasive, untreatable infections caused by K. pneumoniae [1–4].

All 26 K. pneumoniae isolates were selected in this study on the basis of their hypermucosal aspect and were analysed through the string test screening method. Strains with a string >5 mm were classified as a hypermucoviscous (hmv) phenotype; this was shown in 19 out of the 26 strains. The incorporation of the string test into the daily practice of microbiological surveillance could lead to more appropriate diagnostic tools. At the same time, we must remember that non-hmvKp positive strains can also be highly virulent when organisms possess hypervirulence genes [19].

These 19 hypermucoviscous strains were further investigated for virulence factors, and MLST was performed in order to check for high-risk clones; all data are summarized in Table 1.

Table 1.

Virulence factors, antimicrobial susceptibility, carbapenemases and sequence types of the 19 hypermucoviscous strains under study

StrainsString testCarba NPCarbapenemasesSTHypervirulence factorsmagABiofilmKirby-Bauer

Disk Diffusion Susceptibility
ImipenemMeropenemErtapenem
AMP 3291+ND65iucA, iroB, peg-344, rmpA, rmpA2StrongSSS
AMP 3678+ND86iucA, iroB, peg-344, rmpA, rmpA2StrongSSS
AMP 3679+ND65iucA, iroB, peg-344, rmpA, rmpA2StrongSSS
AMP 3680+ND1,224NoneStrongSSS
AMP 3681+ND45None+StrongSSS
AMP 3682+NDNDNone+StrongSSS
AMP 3683+ND380iucA, iroB, peg-344, rmpA, rmpA2+StrongSSS
AMP 3866+ND29iucA, iroB, rmpA, rmpA2StrongSSS
AMP 3872+ND17NoneStrongSSS
AMP 3875++KPC35NoneStrongRIR
AMP 3876+ND86NoneStrongSSS
AMP 3877+ND29iucA, iroB, peg-344, rmpA, rmpA2StrongSSS
AMP 3878+ND10None+StrongSSS
AMP 3880+ND65iucA, iroB, peg-344, rmpA, rmpA2StrongSSS
AMP 3881+ND111NoneStrongSSS
MDR 444++OXA-48-like395None+StrongSIR
MDR 1682++VIM-1

NDM-5

OXA-505
383rmpA2StrongRRR
MDR 2145++KPC

OXA-48-like
101NoneStrongRRR
MDR 3605+ND307rmpA2+StrongSSS

ND = Not Determined; S = Susceptible; R = Resistant; I = Susceptible at increase dosage

ST = sequence type

All 19 strains, following the Stepanovic criteria for classification [18], resulted in strong biofilm producers. This factor will contribute to these strains' tolerance of antibiotics [2].

The five main loci, namely iroB, iucA, peg-344, rmpA, and rmpA2, which according to the literature can differentiate and therefore define a hypervirulent strain with respect to the classical forms of K. pneumoniae, have been selected. Through molecular characterization, it was found that seven strains of the study displayed at least 4 hypervirulence genes. According to what is reported in the literature, a K. pneumoniae strain is defined as hypervirulent if it has at least four of the aforementioned genes [12]. Figure 1 reports the distribution of virulence genes in the strains under study.

Fig. 1.
Fig. 1.

Virulence factor distribution among the strains in this study

Citation: Acta Microbiologica et Immunologica Hungarica 2022; 10.1556/030.2022.01908

However, it should also be taken into account that the strains MDR 1682 and MDR 3605 carry the rmpA2 gene alone, which according to the ECDC risk assessment [1] is one of the major factors of hypervirulence.

According to the PCR results for the magA gene, which is responsible for the capsular serotype K1, 6 out of 19 strains (31.6%) resulted positive. This result is consistent with literature, which reports that K1 capsular serotype together with K2 are the two types of capsule mostly related to hypervirulence [10], since capsule serotyping is a very long procedure that includes different type K and type O antigens, these strains cannot be defined with certainty as K1 serotype. However, this test can still be a good start in the K. pneumoniae capsule serotyping procedure.

Carbapenemase-producing strains were screened through the CarbaNP test, and only 4 out of 19 strains resulted positive (21.05%). All CarbaNP-positive strains were subjected to molecular analysis through various PCRs. Carbapenemases were detected in different combinations: KPC alone; OXA-48 alone; KPC and OXA-48 together; and one strain harboured VIM-1, NDM-5, and OXA-48-like. The last is considered also a potential pathotype since it harbours the rmpA2 gene, while the other three strains harbouring carbapenemases did not carry rmpA2. The three carbapenemases harboured by the MDR 1682 strain were sequenced and found to be VIM-1, NDM-5, and OXA-505 enzymes. NDM-5 is a variant recently found in Italy, in Escherichia coli strains isolated in Tuscany [20].

MLST was performed in order to identify ST linked to the hmv Kp pattern, and to check if ST43 was present as indicated by the ECDC [1]. We have not found ST43; however, we were able to detect other STs present in our hospital setting that can act as emerging clones. Noteworthy also are the multiple STs that we found among hmv strains and harbouring hypervirulence factors. Three strains were characterized as ST65, which, according to the literature, is precisely linked to the hypervirulence of the K2 capsular serotype strains and has caused severe and fatal infections in clinical setting in China [21]. Two strains, on the other hand, belong to ST29, which is commonly associated with extended-spectrum β-lactamase-encoding genes (in particular, blaCTX−M−15), but rarely has carbapenemase genes [22]. The AMP 3678 strain was identified as ST86, which corresponds to the ST found in the first case of community-acquired pneumonia due to an hmv strain of K. pneumoniae [23]. The strain AMP 3683 showed ST380, which is considered an emerging ST in severe community-acquired infections [24].

Among seven strains with five or four hypervirulence genes, we found four STs, most of them already correlated with hypervirulence and considered as emerging clones. This was a surprising and worrying result, since these strains are more widespread than is generally believed and they can easily combine with multidrug resistance.

Another important finding is that the strain harbouring the three carbapenemases belong to ST383. At the beginning of 2022, NDM-1/5- and OXA-48-co-producing, extensively drug-resistant hypervirulent K. pneumoniae strains were detected in Northern Italy, more specifically at the San Raffaele hospital in Milan, and these strains were ST383 [25].

Among the strains that do not harbour the virulence factors taken into consideration, we find ST101 and ST307. These STs have been identified in Southern Italy in serious bloodstream infections and are emerging high-risk carbapenems-resistant clones of K. pneumoniae. Furthermore, these clones appear to be potentially extremely virulent [26].

In conclusion, the global spread of hvKp is an important epidemiological change that should be considered in the diagnostic and therapeutic management of patients with K. pneumoniae infections. Unfortunately, there is high concern about the possibility of a further combination of virulence and resistance, thus leading to severe and untreatable infections in healthy individuals, which would be extremely difficult to manage.

The emergence of these high-risk clones and the global spread of these strains has left physicians with very few treatment options. Therefore, it is essential to have new protocols for strengthened screening control in order to limit the spread of multidrug-resistant and hypervirulent K. pneumoniae strains. New strategies need to be further explored as therapeutic options in the treatment of infections caused by both classical and hypervirulent strains of K. pneumoniae.

Conflict of interests

None.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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  • 1.

    European Centre for Disease Prevention and Control. Risk assessment: emergence of hypervirulent Klebsiella pneumoniae ST23 carrying carbapenemase genes in EU/EEA countries. ECDC website; March 2021.

    • Search Google Scholar
    • Export Citation
  • 2.

    Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Clin Microbiol Rev 2016; 80: 62961.

  • 3.

    Liu YC, Cheng DL, Lin CL. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med 1986; 146: 191316.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 2019; 32: e0000119.

  • 5.

    Yeh KM, Chang FY, Fung CF, Lin JC, Siu LK. magA is not a specific virulence gene for Klebsiella pneumoniae strains causing liver abscess but is part of the capsular polysaccharide gene cluster of K. pneumoniae serotype K1. J Med Microbiol 2006; 55: 8034.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Russo TA, Olson R, MacDonald U, Beanan J, Davidson BA. Aerobactin, but not yersiniabactin, salmochelin, or enterobactin, enables the growth/survival of hypervirulent (hypermucoviscous) Klebsiella pneumoniae ex vivo and in vivo. Infect Imm 2015; 83: 332533.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Piperaki ET, Syrogiannopoulos GA, Tzouvelekis LS, Daikos GL. Klebsiella pneumoniae: virulence, biofilm and antimicrobial resistance. Ped Infec Dis J 2017; 36: 10025.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Pomakova DK, Hsiao CB, Beanan JM, Olson R, MacDonald U, Keynan Y, et al. Clinical and phenotypic differences between classic and hypervirulent Klebsiella pneumoniae: an emerging and under-recognized pathogenic variant. Eur J Clin Microbiol Infect Dis 2012; 31: 9819.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Catalán-Nájera JC, Garza-Ramos U, Barrios-Camacho H. Hypervirulence and hypermucoviscosity: two different but complementary Klebsiella spp. Phenotypes? Virulence 2017; 8: 111123.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Walker KA, Miller VL. The intersection of capsule gene expression, hypermucoviscosity and hypervirulence in Klebsiella pneumoniae. Curr Opin Microbiol 2020; 54: 95102.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Patro LPP, Sudhakar KU, Rathinavelan T. K-PAM: a unified platform to distinguish Klebsiella species K- and O-antigen types, model antigen structures and identify hypervirulent strains. Sci Rep 2020; 10: 16372.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Yeh KM, Kurup A, Siu LK, Koh YL, Fung CP, Lin JC, et al. Capsular serotype K1 or K2, rather than magA and rmpA, is a major virulence determinant for Klebsiella pneumoniae liver abscess in Singapore and Taiwan. J Clin Microbiol 2007; 45: 46671.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Nordmann P, Poirel L, Dortet L. Rapid detection of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis 2012; 18: 15037.

  • 15.

    Dallenne C, Da Costa A, Decre D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important b-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 4905.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    http://www.pasteur.fr/mlst

    Genotyping of pathogens and public health, Institute Pasteur, Paris, France.

  • 17.

    Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 2005; 43: 417882.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Cirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. J Pathol Microbiol Immunol 2007; 115: 8919.

    • Search Google Scholar
    • Export Citation
  • 19.

    Hagiya H, Watanabe N, Maki M, Murase T, Otsuka F. Clinical utility of string test as a screening method for hypermucoviscosity-phenotype Klebsiella pneumoniae. Acute Med Surg 2014; 1: 2456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Bibbolino G, Di Lella FM, Oliva A, Lichtner M, Del Borgo C, Raponi G, et al. Molecular epidemiology of NDM-5-producing Escherichia coli high-risk clones identified in two Italian hospitals in 2017-2019. Diagn Microbiol Infec Dis 2021; 100: 115399.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Zhang Y, Wang X, Wang Q, Chen H, Li H, Wang S, et al. Emergence of tigecycline nonsusceptible and IMP-4 carbapenemase-producing K2-ST65 hypervirulent Klebsiella pneumoniae in China. Microbiol Spectr 2021; 9: e01305-21.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Liu L, Feng L, Wei L, Xiao Y, Zong Z. KPC-2-producing carbapenem-resistant Klebsiella pneumoniae of the uncommon ST29 type carrying OXA-926, a novel narrow-spectrum OXA β-lactamase. Front Microbiol 2021; 12: 701513.

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  • 23.

    Hirai J, Sakanashi D, Kinjo T, Haranaga S, Fujita J. The first case of community-acquired pneumonia due to capsular genotype K2-ST86 hypervirulent Klebsiella pneumoniae in Okinawa, Japan: a case report and literature review. Infec Drug Res 2020; 13: 223743.

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    Hentzien M, Rosman J, Decré D, Brenkle K, Mendes-Martins L, Mateu P. Seven hypervirulent ST380 Klebsiella pneumoniae septic localizations. Med Mal Infec 2017; 47: 1713.

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  • 25.

    Lorenzin G, Gona F, Battaglia S, Spitaleri A, Saluzzo F, Trovato A, et al. Detection of NDM-1/5 and OXA-48 co-producing extensively drug-resistant hypervirulent Klebsiella pneumoniae in Northern Italy. J Glob Antimicrob Resist 2022; 28: 14650.

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  • 26.

    Loconsole D, Accogli M, De Robertis AL, Capozzi L, Bianco A, Morea A, et al. Emerging high-risk ST101 and ST307 carbapenem-resistant Klebsiella pneumoniae clones from bloodstream infections in Southern Italy. Ann Clin Microbiol and Antimicrob 2020; 19: 24.

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The author instruction is available in PDF.
Please, download the file from HERE

Senior editors

Editor-in-Chief: Prof. Dóra Szabó (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Managing Editor: Dr. Béla Kocsis (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Co-editor: Dr. Andrea Horváth (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)

Editorial Board

  • Prof. Éva ÁDÁM (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Sebastian AMYES (Department of Medical Microbiology, University of Edinburgh, Edinburgh, UK.)
  • Dr. Katalin BURIÁN (Institute of Clinical Microbiology University of Szeged, Szeged, Hungary; Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary.)
  • Dr. Orsolya DOBAY (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Ildikó Rita DUNAY (Institute of Inflammation and Neurodegeneration, Medical Faculty, Otto-von-Guericke University, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany)
  • Prof. Levente EMŐDY(Department of Medical Microbiology and Immunology, University of Pécs, Pécs, Hungary.)
  • Prof. Anna ERDEI (Department of Immunology, Eötvös Loránd University, Budapest, Hungary, MTA-ELTE Immunology Research Group, Eötvös Loránd University, Budapest, Hungary.)
  • Prof. Éva Mária FENYŐ (Division of Medical Microbiology, University of Lund, Lund, Sweden)
  • Prof. László FODOR (Department of Microbiology and Infectious Diseases, University of Veterinary Medicine, Budapest, Hungary)
  • Prof. József KÓNYA (Department of Medical Microbiology, University of Debrecen, Debrecen, Hungary)
  • Prof. Yvette MÁNDI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Károly MÁRIALIGETI (Department of Microbiology, Eötvös Loránd University, Budapest, Hungary)
  • Prof. János MINÁROVITS (Department of Oral Biology and Experimental Dental Research, University of Szeged, Szeged, Hungary)
  • Prof. Béla NAGY (Centre for Agricultural Research, Institute for Veterinary Medical Research, Budapest, Hungary.)
  • Prof. István NÁSZ (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Kristóf NÉKÁM (Hospital of the Hospitaller Brothers in Buda, Budapest, Hungary.)
  • Dr. Eszter OSTORHÁZI (Institute of Medical Microbiology, Semmelweis University, Budapest, Hungary)
  • Prof. Rozália PUSZTAI (Department of Medical Microbiology and Immunobiology, University of Szeged, Szeged, Hungary)
  • Prof. Peter L. RÁDY (Department of Dermatology, University of Texas, Houston, Texas, USA)
  • Prof. Éva RAJNAVÖLGYI (Department of Immunology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary)
  • Prof. Ferenc ROZGONYI (Institute of Laboratory Medicine, Semmelweis University, Budapest, Hungary)
  • Prof. Zsuzsanna SCHAFF (2nd Department of Pathology, Semmelweis University, Budapest, Hungary)
  • Prof. Joseph G. SINKOVICS (The Cancer Institute, St. Joseph’s Hospital, Tampa, Florida, USA)
  • Prof. Júlia SZEKERES (Department of Medical Biology, University of Pécs, Pécs, Hungary.)
  • Prof. Mária TAKÁCS (National Reference Laboratory for Viral Zoonoses, National Public Health Center, Budapest, Hungary.)
  • Prof. Edit URBÁN (Department of Medical Microbiology and Immunology University of Pécs, Pécs, Hungary; Institute of Translational Medicine, University of Pécs, Pécs, Hungary.)

 

Editorial Office:
Akadémiai Kiadó Zrt.
Budafoki út 187-187, A/3, H-1117 Budapest, Hungary

Editorial Correspondence:
Acta Microbiologica et Immunologica Hungarica
Institute of Medical Microbiology
Semmelweis University
P.O. Box 370
H-1445 Budapest, Hungary
Phone: + 36 1 459 1500 ext. 56101
Fax: (36 1) 210 2959
E-mail: amih@med.semmelweis-univ.hu

 Indexing and Abstracting Services:

  • Biological Abstracts
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  • Chemical Abstracts
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Referativnyi Zhurnal
  • SCOPUS
  • Science Citation Index Expanded

2021  
Web of Science  
Total Cites
WoS
696
Journal Impact Factor 2,298
Rank by Impact Factor Immunology 141/161
Microbiology 118/136
Impact Factor
without
Journal Self Cites
2,143
5 Year
Impact Factor
1,925
Journal Citation Indicator 0,39
Rank by Journal Citation Indicator Immunology 146/177
Microbiology 129/157
Scimago  
Scimago
H-index
29
Scimago
Journal Rank
0,362
Scimago Quartile Score Immunology and Microbiology (miscellaneous) (Q3)
Medicine (miscellaneous) (Q3)
Scopus  
Scopus
Cite Score
3,6
Scopus
CIte Score Rank
General Immunology and Microbiology 26/56 (Q2)
Infectious Diseases 149/295 (Q3)
Microbiology (medical) 66/118 (Q3)
Scopus
SNIP
0,598

2020  
Total Cites 662
WoS
Journal
Impact Factor
2,048
Rank by Immunology 145/162(Q4)
Impact Factor Microbiology 118/137 (Q4)
Impact Factor 1,904
without
Journal Self Cites
5 Year 0,671
Impact Factor
Journal  0,38
Citation Indicator  
Rank by Journal  Immunology 146/174 (Q4)
Citation Indicator  Microbiology 120/142 (Q4)
Citable 42
Items
Total 40
Articles
Total 2
Reviews
Scimago 28
H-index
Scimago 0,439
Journal Rank
Scimago Immunology and Microbiology (miscellaneous) Q4
Quartile Score Medicine (miscellaneous) Q3
Scopus 438/167=2,6
Scite Score  
Scopus General Immunology and Microbiology 31/45 (Q3)
Scite Score Rank  
Scopus 0,760
SNIP
Days from  225
submission
to acceptance
Days from  118
acceptance
to publication
Acceptance 19%
Rate

2019  
Total Cites
WoS
485
Impact Factor 1,086
Impact Factor
without
Journal Self Cites
0,864
5 Year
Impact Factor
1,233
Immediacy
Index
0,286
Citable
Items
42
Total
Articles
40
Total
Reviews
2
Cited
Half-Life
5,8
Citing
Half-Life
7,7
Eigenfactor
Score
0,00059
Article Influence
Score
0,246
% Articles
in
Citable Items
95,24
Normalized
Eigenfactor
0,07317
Average
IF
Percentile
7,690
Scimago
H-index
27
Scimago
Journal Rank
0,352
Scopus
Scite Score
320/161=2
Scopus
Scite Score Rank
General Immunology and Microbiology 35/45 (Q4)
Scopus
SNIP
0,492
Acceptance
Rate
16%

 

Acta Microbiologica et Immunologica Hungarica
Publication Model Online only Hybrid
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Article Processing Charge 1100 EUR/article
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Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription fee 2022 Online subsscription: 662 EUR / 832 USD
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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
Year of
Foundation
1954
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 1217-8950 (Print)
ISSN 1588-2640 (Online)

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