Authors:
Tanya Strateva Department of Medical Microbiology “Corr. Mem. Prof. Ivan Mitov, MD, DMSc”, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria

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Emma Keuleyan Department of Clinical Microbiology and Virology, University Hospital Lozenetz, Sofia, Bulgaria

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Slavil Peykov Department of Medical Microbiology “Corr. Mem. Prof. Ivan Mitov, MD, DMSc”, Faculty of Medicine, Medical University of Sofia, Sofia, Bulgaria
Department of Genetics, Faculty of Biology, Sofia University “St. Kliment Ohridski”, Sofia, Bulgaria
BioInfoTech Laboratory, Sofia Tech Park, Sofia, Bulgaria

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Abstract

The present study aimed to explore the genomic characteristics of eight New Delhi metallo-β-lactamase-1 (NDM-1)-producing carbapenem-resistant Pseudomonas aeruginosa (CRPA) isolates from a Bulgarian tertiary hospital (2021–2023) in comparison to blaNDM-1-positive strains originating from the Balkans. Antimicrobial susceptibility testing, phenotypic assays for carbapenemase activity, PCR screening, whole-genome sequencing (WGS), and phylogenomic analysis were performed. Seven of the CRPA isolates investigated (Minimum inhibitory concentration values of imipenem and meropenem >32 mg L−1) were also resistant to piperacillin-tazobactam, ceftazidime, ceftazidime-avibactam, cefepime, ceftolozane-tazobactam, amikacin, tobramycin, ciprofloxacin, and levofloxacin, but were susceptible to colistin (0.5–2 mg L−1) and cefiderocol (0.25–1 mg L−1). The P. aeruginosa Pae57 isolate (designated Pae57) remained susceptible to aminoglycosides as well. WGS uncovered the co-existence of blaNDM-1 and blaGES-1. The isolates belonged to the ST654 high-risk clone, except for Pae57 (ST611). Alignment against reference sequences revealed the presence of a Tn21 transposon harboring bleMBLblaNDM-1–ISAba125. It was similar to that found in the P. aeruginosa ST654 NDM1_1 strain (GCA_020404785.1) from Serbia. Phylogenomic analysis of our isolates indicated that seven of them (ST654) differed from each other in no more than 44 single-nucleotide polymorphisms (SNPs). Pae57 (ST611) was strikingly different (>21,700 SNPs) compared to all Balkan strains. In conclusion, to our knowledge this is the first report of blaNDM-1-positive P. aeruginosa ST611 isolation, which indicates the transmission dynamics of this determinant between high-risk and potentially high-risk P. aeruginosa clones. Obtained results unveil the dissemination of clonally related NDM-1-producing P. aeruginosa strains in the monitored hospital for approximately a 2-year period.

  • 1.

    De Oliveira DMP, Forde BM, Kidd TJ, Harris PNA, Schembri MA, Beatson SA, et al. Antimicrobial resistance in ESKAPE pathogens. Clin Microbiol Rev 2020; 33(3): e0018119. https://doi.org/10.1128/CMR.00181-19.

    • Search Google Scholar
    • Export Citation
  • 2.

    Reynolds D, Kollef M. The epidemiology and pathogenesis and treatment of Pseudomonas aeruginosa infections: an Update. Drugs 2021; 81(18): 211731. https://doi.org/10.1007/s40265-021-01635-6.

    • Search Google Scholar
    • Export Citation
  • 3.

    Behzadi P, Baráth Z, Gajdács M. It’s not easy being green: a narrative review on the microbiology, virulence and therapeutic prospects of multidrug-resistant Pseudomonas aeruginosa. Antibiotics 2021; 10(1): 42. https://doi.org/10.3390/antibiotics10010042.

    • Search Google Scholar
    • Export Citation
  • 4.

    Migiyama Y, Sakata S, Iyama S, Tokunaga K, Saruwatari K, Tomita Y, et al. Airway Pseudomonas aeruginosa density in mechanically ventilated patients: clinical impact and relation to therapeutic efficacy of antibiotics. Crit Care 2021; 25(1): 59. https://doi.org/10.1186/s13054-021-03488-7.

    • Search Google Scholar
    • Export Citation
  • 5.

    Mekonnen SA, El Husseini N, Turdiev A, Carter JA, Belew AT, El-Sayed NM, et al. Catheter-associated urinary tract infection by Pseudomonas aeruginosa progresses through acute and chronic phases of infection. Proc Natl Acad Sci USA 2022; 119(50): e2209383119. https://doi.org/10.1073/pnas.2209383119.

    • Search Google Scholar
    • Export Citation
  • 6.

    Gomersall J, Mortimer K, Hassan D, Whitehead KA, Slate AJ, Ryder SF, et al. Ten-year analysis of bacterial colonization and outcomes of major burn patients with a focus on Pseudomonas aeruginosa. Microorganisms 2023; 12(1): 42. https://doi.org/10.3390/microorganisms12010042.

    • Search Google Scholar
    • Export Citation
  • 7.

    Paprocka P, Durnaś B, Mańkowska A, Król G, Wollny T, Bucki R. Pseudomonas aeruginosa infections in cancer patients. Pathogens 2022; 11(6): 679. https://doi.org/10.3390/pathogens11060679.

    • Search Google Scholar
    • Export Citation
  • 8.

    Yakout MA, Abdelwahab IA. Diabetic foot ulcer infections and Pseudomonas aeruginosa biofilm production during the COVID-19 pandemic. J Pure Appl Microbiol 2022; 16(1): 13846. https://doi.org/10.22207/JPAM.16.1.02.

    • Search Google Scholar
    • Export Citation
  • 9.

    Rossi E, La Rosa R, Bartell JA, Marvig RL, Haagensen JAJ, Sommer LM, et al. Pseudomonas aeruginosa adaptation and evolution in patients with cystic fibrosis. Nat Rev Microbiol 2021; 19(5): 33142. https://doi.org/10.1038/s41579-020-00477-5.

    • Search Google Scholar
    • Export Citation
  • 10.

    Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 2022; 399(10325): 62955. https://doi.org/10.1016/S0140-6736(21)02724-0.

    • Search Google Scholar
    • Export Citation
  • 11.

    Jangra V, Sharma N, Chhillar AK. Therapeutic approaches for combating Pseudomonas aeruginosa infections. Microbes Infect 2022; 24(4): 104950. https://doi.org/10.1016/j.micinf.2022.104950.

    • Search Google Scholar
    • Export Citation
  • 12.

    CDC. Antibiotic resistance threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019. Available online: https://www.cdc.gov/drugresistance/biggest-threats.html [Accessed 4 May 2024].

    • Search Google Scholar
    • Export Citation
  • 13.

    Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18(3): 31827. https://doi.org/10.1016/S1473-3099(17)30753-3.

    • Search Google Scholar
    • Export Citation
  • 14.

    Peykov S, Strateva T. Whole-genome sequencing-based resistome analysis of nosocomial multidrug-resistant non-fermenting Gram-negative pathogens from the Balkans. Microorganisms 2023; 11(3): 651. https://doi.org/10.3390/microorganisms11030651.

    • Search Google Scholar
    • Export Citation
  • 15.

    WHO Regional Office for Europe/European Centre for Disease Prevention and Control. Antimicrobial resistance surveillance in Europe 2022 – 2020 data. Copenhagen: WHO Regional Office for Europe; 2022. Available online: https://www.ecdc.europa.eu/en/publications-data/antimicrobial-resistance-surveillance-europe-2022-2020-data [Accessed 3 May 2024].

    • Search Google Scholar
    • Export Citation
  • 16.

    European Centre for Disease Prevention and Control. Antimicrobial resistance in the EU/EEA (EARS-Net) – annual epidemiological report 2022. Stockholm: ECDC; 2023. Available online: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2022[Accessed 3 May 2024].

    • Search Google Scholar
    • Export Citation
  • 17.

    Glen KA, Lamont IL. β-lactam resistance in Pseudomonas aeruginosa: current status, future prospects. Pathogens 2021; 10(12): 1638. https://doi.org/10.3390/pathogens10121638.

    • Search Google Scholar
    • Export Citation
  • 18.

    Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-β-Lactamase Gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae Sequence Type 14 from India. Antimicrob Agents Chemother 2009; 53(12): 504654. https://doi.org/10.1128/AAC.00774-09.

    • Search Google Scholar
    • Export Citation
  • 19.

    Struelens MJ, Monnet DL, Magiorakos AP, Santos O’Connor F, Giesecke J, the European NDM-1 Survey Participants. New Delhi metallo-beta-lactamase 1–producing Enterobacteriaceae: emergence and response in Europe. Euro Surveill 2010; 15(46): 19716. https://doi.org/10.2807/ese.15.46.19716-en.

    • Search Google Scholar
    • Export Citation
  • 20.

    Jovcic B, Lepsanovic Z, Suljagic V, Rackov G, Begovic J, Topisirovic L, et al. Emergence of NDM-1 metallo-β-lactamase in Pseudomonas aeruginosa clinical isolates from Serbia. Antimicrob Agents Chemother 2011; 55(8): 392931. https://doi.org/10.1128/AAC.00226-11.

    • Search Google Scholar
    • Export Citation
  • 21.

    Tsilipounidaki K, Gkountinoudis CG, Florou Z, Fthenakis GC, Miriagou V, Petinaki E. First detection and molecular characterization of Pseudomonas aeruginosa blaNDM-1 ST308 in Greece. Microorganisms 2023; 11(9): 2159. https://doi.org/10.3390/microorganisms11092159.

    • Search Google Scholar
    • Export Citation
  • 22.

    Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, et al. The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 2018; 46(W1): W2828. https://doi.org/10.1093/nar/gky467.

    • Search Google Scholar
    • Export Citation
  • 23.

    The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, Version 14.0., 2024. Available online: https://eucast.org [Accessed 8 May 2024].

    • Search Google Scholar
    • Export Citation
  • 24.

    Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18(3): 26881. https://doi.org/10.1111/j.1469-0691.2011.03570.x.

    • Search Google Scholar
    • Export Citation
  • 25.

    Kadri SS, Adjemian J, Lai YL, Spaulding AB, Ricotta E, Prevots DR, et al. Difficult-to-treat resistance in Gram-negative bacteremia at 173 US hospitals: retrospective cohort analysis of prevalence, predictors, and outcome of resistance to all first-line agents. Clin Infect Dis 2018; 67(12): 180314. https://doi.org/10.1093/cid/ciy378.

    • Search Google Scholar
    • Export Citation
  • 26.

    Lixandru BE, Cotar AI, Straut M, Usein CR, Cristea D, Ciontea S, et al. Carbapenemase-producing Klebsiella pneumoniae in Romania: a six-month survey. PLoS ONE 2015; 10(11): e0143214. https://doi.org/10.1371/journal.pone.0143214.

    • Search Google Scholar
    • Export Citation
  • 27.

    Poirel L, Nordmann P. Acquired carbapenem-hydrolyzing beta-lactamases and their genetic support. Curr Pharm Biotechnol 2002; 3(2): 11727. https://doi.org/10.2174/1389201023378427.

    • Search Google Scholar
    • Export Citation
  • 28.

    Afgan E, Nekrutenko A, Grüning BA, Blankenberg D, Goecks J, Schatz MC, et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2022 update. Nucleic Acids Res 2022; 50(W1): W34551. https://doi.org/10.1093/nar/gkac247.

    • Search Google Scholar
    • Export Citation
  • 29.

    Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 2004; 42(12): 56449. https://doi.org/10.1128/JCM.42.12.5644-5649.2004.

    • Search Google Scholar
    • Export Citation
  • 30.

    Thrane SW, Taylor VL, Lund O, Lam JS, Jelsbak L. Application of whole-genome sequencing data for O-specific antigen analysis and in silico serotyping of Pseudomonas aeruginosa isolates. J Clin Microbiol 2016; 54(7): 17828. https://doi.org/10.1128/JCM.00349-16.

    • Search Google Scholar
    • Export Citation
  • 31.

    Russel J, Pinilla-Redondo R, Mayo-Muñoz D, Shah SA, Sørensen SJ. CRISPRCasTyper: automated identification, annotation, and classification of CRISPR-Cas loci. CRISPR J 2020; 3(6): 4629. https://doi.org/10.1089/crispr.2020.0059.

    • Search Google Scholar
    • Export Citation
  • 32.

    Tafaj S, Gona F, Rodrigues CF, Kapisyzi P, Caushi F, Rossen JW, et al. Whole-genome sequences of two NDM-1-producing Pseudomonas aeruginosa strains isolated in a clinical setting in Albania in 2018. Microbiol Resour Announc 2020; 9(1): e0129119. https://doi.org/10.1128/MRA.01291-19.

    • Search Google Scholar
    • Export Citation
  • 33.

    Kostyanev T, Nguyen MN, Markovska R, Stankova P, Xavier BB, Lammens C, et al. Emergence of ST654 Pseudomonas aeruginosa co-harbouring blaNDM-1 and blaGES-5 in novel class I integron In1884 from Bulgaria. J Glob Antimicrob Resist 2020; 22: 6723. https://doi.org/10.1016/j.jgar.2020.06.008.

    • Search Google Scholar
    • Export Citation
  • 34.

    Kabic J, Fortunato G, Vaz-Moreira I, Kekic D, Jovicevic M, Pesovic J, et al. Dissemination of metallo-β-lactamase-producing Pseudomonas aeruginosa in Serbian hospital settings: expansion of ST235 and ST654 clones. Int J Mol Sci 2023; 24(2): 1519. https://doi.org/10.3390/ijms24021519.

    • Search Google Scholar
    • Export Citation
  • 35.

    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30(14): 20689. https://doi.org/10.1093/bioinformatics/btu153.

    • Search Google Scholar
    • Export Citation
  • 36.

    Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31(22): 36913. https://doi.org/10.1093/bioinformatics/btv421.

    • Search Google Scholar
    • Export Citation
  • 37.

    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30(9): 13123. https://doi.org/10.1093/bioinformatics/btu033.

    • Search Google Scholar
    • Export Citation
  • 38.

    Letunic I, Bork P. Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49(W1): W2936. https://doi.org/10.1093/nar/gkab301.

    • Search Google Scholar
    • Export Citation
  • 39.

    European Centre for Disease Prevention and Control. Healthcare-associated infections acquired in intensive care units. In: ECDC. Annual epidemiological report for 2020. Stockholm: ECDC; 2024. Available online: https://www.ecdc.europa.eu/en/publications-data/healthcare-associated-infections-acquired-intensive-care-units-annual [Accessed 8 May 2024].

    • Search Google Scholar
    • Export Citation
  • 40.

    Malisova L, Vrbova I, Pomorska K, Jakubu V, Zemlickova H. In vitro activity of cefiderocol against carbapenem-resistant Enterobacterales and Pseudomonas aeruginosa. Microb Drug Resist 2023; 29(10): 48591. https://doi.org/10.1089/mdr.2023.0090.

    • Search Google Scholar
    • Export Citation
  • 41.

    Karakonstantis S, Rousaki M, Kritsotakis EI. Cefiderocol: systematic review of mechanisms of resistance, heteroresistance and in vivo emergence of resistance. Antibiotics 2022; 11(6): 723. https://doi.org/10.3390/antibiotics11060723.

    • Search Google Scholar
    • Export Citation
  • 42.

    Nurjadi D, Kocer K, Chanthalangsy Q, Klein S, Heeg K, Boutin S. New Delhi metallo-beta-lactamase facilitates the emergence of cefiderocol resistance in Enterobacter cloacae. Antimicrob Agents Chemother 2022; 66(2): e0201121. https://doi.org/10.1128/AAC.02011-21.

    • Search Google Scholar
    • Export Citation
  • 43.

    Schneider I, Keuleyan E, Rasshofer R, Markovska R, Queenan AM, Bauernfeind A. VIM-15 and VIM-16, two new VIM-2-Like metallo-β-lactamases in Pseudomonas aeruginosa isolates from Bulgaria and Germany. Antimicrob Agents Chemother 2008; 52(8): 29779. https://doi.org/10.1128/AAC.00175-08.

    • Search Google Scholar
    • Export Citation
  • 44.

    Strateva T, Setchanova L, Peykov S. Characterization of a Bulgarian VIM-2 metallo-β-lactamase-producing Pseudomonas aeruginosa clinical isolate belonging to the high-risk sequence type 111. Infect Dis (Lond) 2021; 53(11): 8837. https://doi.org/10.1080/23744235.2021.1934531.

    • Search Google Scholar
    • Export Citation
  • 45.

    Stoikov I, Ivanov IN, Donchev D, Teneva D, Dobreva E, Hristova R, et al. Genomic characterization of IMP-producing Pseudomonas aeruginosa in Bulgaria reveals the emergence of IMP-100, a novel plasmid-mediated variant coexisting with a chromosomal VIM-4. Microorganisms 2023; 11(9): 2270. https://doi.org/10.3390/microorganisms11092270.

    • Search Google Scholar
    • Export Citation
  • 46.

    Oliver A, Rojo-Molinero E, Arca-Suarez J, Beşli Y, Bogaerts P, Cantón R, et al. Pseudomonas aeruginosa antimicrobial susceptibility profiles, resistance mechanisms and international clonal lineages: update from ESGARS-ESCMID/ISARPAE Group. Clin Microbiol Infect 2024; 30(4): 46980. https://doi.org/10.1016/j.cmi.2023.12.026.

    • Search Google Scholar
    • Export Citation
  • 47.

    Opazo-Capurro A, Morales-León F, Jerez C, Olivares-Pacheco J, Alcalde-Rico M, González-Muñoz P, et al. Isolation of an extensively drug-resistant Pseudomonas aeruginosa exoS+/O4 strain belonging to the “high-risk” clone ST654 and coproducer of NDM-1 and the novel VIM-80. Microbiol Spectr 2022; 10(5): e0143922. https://doi.org/10.1128/spectrum.01439-22.

    • Search Google Scholar
    • Export Citation
  • 48.

    Bai Y, Gong Y e, Shen F, Li H, Cheng Y, Guo J, et al. Molecular epidemiological characteristics of carbapenem-resistant Pseudomonas aeruginosa clinical isolates in southeast Shanxi, China. J Glob Antimicrob Resist 2024; 36: 3016. https://doi.org/10.1016/j.jgar.2023.12.029.

    • Search Google Scholar
    • Export Citation
  • 49.

    Zhao Y, Chen D, Ji B, Zhang X, Anbo M, Jelsbak L. Whole-genome sequencing reveals high-risk clones of Pseudomonas aeruginosa in Guangdong, China. Front Microbiol 2023; 14: 1117017. https://doi.org/10.3389/fmicb.2023.1117017.

    • Search Google Scholar
    • Export Citation
  • 50.

    Botelho J, Tüffers L, Fuss J, Buchholz F, Utpatel C, Klockgether J, et al. Phylogroup-specific variation shapes the clustering of antimicrobial resistance genes and defence systems across regions of genome plasticity in Pseudomonas aeruginosa. EBioMedicine 2023; 90: 104532. https://doi.org/10.1016/j.ebiom.2023.104532.

    • Search Google Scholar
    • Export Citation
  • 51.

    Wheatley RM, MacLean RC. CRISPR-Cas systems restrict horizontal gene transfer in Pseudomonas aeruginosa. ISME J 2021; 15(5): 142033. https://doi.org/10.1038/s41396-020-00860-3.

    • Search Google Scholar
    • Export Citation
  • 52.

    Fortunato G, Vaz-Moreira I, Gajic I, Manaia CM. Insight into phylogenomic bias of blaVIM-2 or blaNDM-1 dissemination amongst carbapenem-resistant Pseudomonas aeruginosa. Int J Antimicrob Agents 2023; 61(5): 106788. https://doi.org/10.1016/j.ijantimicag.2023.106788.

    • Search Google Scholar
    • Export Citation
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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. 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.)

 

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Acta Microbiologica et Immunologica Hungarica
Language English
Size A4
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Foundation
1954
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per Year
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per Year
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Founder Magyar Tudományos Akadémia
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