Acta Microbiologica et Immunologica Hungarica
Volume/Issue:
Volume 70: Issue 4
Molecular epidemiology and antimicrobial resistance of Haemophilus influenzae isolates from otitis media in Bulgaria
Authors:
Alexandra Sashova Alexandrova Department of Medical Microbiology, Medical Faculty, Medical University of Sofia, 1, G.Sofiiski Boul., 1431-Sofia, Bulgaria

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https://orcid.org/0000-0001-5944-961X
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Ivo Nikolaev Sirakov Department of Medical Microbiology, Medical Faculty, Medical University of Sofia, 1, G.Sofiiski Boul., 1431-Sofia, Bulgaria

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Lena Petrova Setchanova Laboratory of Clinical Microbiology, UMBAL St. “Ivan Rilski” - Sofia, 15, Acad. Ivan Geshov boul., 1431-Sofia, Bulgaria

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Kalina Ionkova Mihova Department of Medical Chemistry and Biochemistry, Molecular Medicine Center, Medical Faculty, Medical University of Sofia, 2, Zdrave str., 1431-Sofia, Bulgaria

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Daniela Rosenova Pencheva Department of Medical Chemistry and Biochemistry, Molecular Medicine Center, Medical Faculty, Medical University of Sofia, 2, Zdrave str., 1431-Sofia, Bulgaria

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Raina Tsvetanova Gergova Department of Medical Microbiology, Medical Faculty, Medical University of Sofia, 1, G.Sofiiski Boul., 1431-Sofia, Bulgaria

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Pages:
318–324
Online Publication Date:
08 Nov 2023
Publication Date:
07 Dec 2023
Article Category:
Research Article
DOI:
https://doi.org/10.1556/030.2023.02126
Keywords:
Haemophilus influenzae; otitis media; clonal structure; antimicrobial resistance
Restricted access

Abstract

Haemophilus influenzae is one of the main bacteria responsible for otitis media (OM) among children worldwide. We aimed to estimate the distribution of encapsulated and non-capsulated variants (NTHi), biotypes, antibiotic susceptibility, and molecular epidemiology of H. influenzae isolates recovered from pediatric OM cases in Bulgaria.

Capsule detection was done by PCR for bexB gene, absent in NTHi. All encapsulated strains were subjected to PCR serotyping. MIC susceptibility testing was performed according to the criteria of EUCAST. MLST was conducted for all 71 OM isolates.

The capsule detection and PCR – serotyping disclosed a predominance of NTHi (90.1%) and a few “a”, “f”, and “c” types. Biotype I was the most widespread (42.3%). β-lactam resistance was found in 35.2% of the isolates. MLST represented heterogenic population structure, whereas the most represented clonal complexes belonged to ST-3, ST-57, ST-105, and ST-1426. 42.3% of the STs showed relatedness to globally represented clones, and 11.3% displayed affiliation to international type 2.

Most of the H. influenzae isolates recovered from children with otitis media were non-typable strains from biotype I. The examined population structure was genetically diverse, with a predominance of international type 2 isolates.

  • 1.

    Morgan S, Yoder-Himes D, Jackson D, Naber J, Berry R, Cash E, et al. Bactericidal effects of high-energy visible light on common otitis media pathogens. J Appl Microbiol 2022; 3: 1856–65. https://doi.org/10.1111/jam.15366.

    • Search Google Scholar
    • Export Citation
  • 2.

    Cunningham M, Guardiani E, Kim H, Brook I. Otitis media. Future Microbiol 2012; 6: 733–53. https://doi.org/10.2217/fmb.12.38.2.

  • 3.

    Kroll S, Loynds B, Brophy L, Moxon ER. The bex locus in encapsulated Haemophilus influenzae: a chromosomal region involved in capsule polysaccharide export. Mol Microbiol 1990; 4: 1853–62. https://doi.org/10.1111/j.1365-2958.1990.tb02034.x.

    • Search Google Scholar
    • Export Citation
  • 4.

    Slack M, Esposito S, Haas H, Mihalyi A, Nissen M, Mukherjee P, et al. Haemophilus influenzae type b disease in the era of conjugate vaccines: critical factors for successful eradication. Expert Rev Vaccin 2020; 10: 903–17. https://doi.org/10.1080/14760584.2020.1825948.

    • Search Google Scholar
    • Export Citation
  • 5.

    Reilly AS, McElligott M, Mac Dermott Casement C, Drew R. Haemophilus influenzae type f in the post-Haemophilus influenzae type b vaccination era: a systematic review. J Med Microbiol 2022; 71(10). https://doi.org/10.1099/jmm.0.001606.

    • Search Google Scholar
    • Export Citation
  • 6.

    Bakaletz LO, Novotny LA. Nontypeable Haemophilus influenzae (NTHi). Trends Microbiol 2018; 8: 727–8. https://doi.org/10.1016/j.tim.2018.05.001.

    • Search Google Scholar
    • Export Citation
  • 7.

    Tristram S, Jacobs MR, Appelbaum PC. Antimicrobial resistance in Haemophilus influenzae. Clin Microbiol Rev, 2007; 2: 368–89. https://doi.org/10.1128/CMR.00040-06.

    • Search Google Scholar
    • Export Citation
  • 8.

    Khurana P, Shenoy S. Occurrence of blaTEM and blaROB in Haemophilus species causing respiratory tract infections. Infect Disord Drug Targets 2020; 3: 385–388. https://doi.org/10.2174/1871526519666190118103148.

    • Search Google Scholar
    • Export Citation
  • 9.

    Straker K, Wootton M, Simm A, Bennett PM, MacGowan AP, Walsh TR, et al. Cefuroxime resistance in non-beta-lactamase Haemophilus influenzae is linked to mutations in ftsI. J Antimicrob Chemother 2003; 51: 523–530 https://doi.org/10.1093/jac/dkg107.

    • Search Google Scholar
    • Export Citation
  • 10.

    Harper JJ, Tilse MH. Biotypes of Haemophilus influenzae that are associated with noninvasive infections. J Clin Microbiol. 1991; 11: 2539–42. https://doi.org/10.1128/jcm.29.11.2539-2542.1991.

    • Search Google Scholar
    • Export Citation
  • 11.

    Davis GS, Sandstedt SA, Patel M, Marrs CF, Gilsdorf JR. Use of bexB to detect the capsule locus in Haemophilus influenzae. J Clin Microbiol 2011; 7: 2594–601 https://doi.org/10.1128/JCM.02509-10.

    • Search Google Scholar
    • Export Citation
  • 12.

    Falla TJ, Crook D, Brophy L, Maskell D, Kroll JS, Moxon ER. PCR for capsular typing of Haemophilus influenzae. J Clin Microbiol. 1994; 32: 2382–6. https://doi.org/10.1128/jcm.32.10.2382-2386.1994.

    • Search Google Scholar
    • Export Citation
  • 13.

    Hasegawa K, Yamamoto K, Chiba N, Kobayashi R, Nagai K, Jacobs MR, et al. Diversity of ampicillin-resistance genes in Haemophilus influenzae in Japan and the United States. Microb Drug Resist 2003; 9: 39–46. https://doi.org/10.1089/107662903764736337.

    • Search Google Scholar
    • Export Citation
  • 14.

    Harmes KM, Blackwood RA, Burrows HL, Cooke JM, Van Harrison R, Passamani PP. Otitis media: diagnosis and treatment. Am Fam Physician 2013; 88(7): 435–40.

    • Search Google Scholar
    • Export Citation
  • 15.

    Gilsdorf JR. What the pediatrician should know about non-typeable Haemophilus influenzae. J Infect 2015; 1: S10–4. https://doi.org/10.1016/j.jinf.2015.04.014.

    • Search Google Scholar
    • Export Citation
  • 16.

    Ubukata K, Shibasaki Y, Yamamoto K, Chiba N, Hasegawa K, Takeuchi Y, et al. Association of amino acid substitutions in penicillin-binding protein 3 with beta-lactam resistance in beta-lactamase-negative ampicillin-resistant Haemophilus influenzae. Antimicrob Agents Chemother 2001; 45: 1693–9. https://doi.org/10.1128/AAC.45.6.1693-1699.2001.

    • Search Google Scholar
    • Export Citation
  • 17.

    Skaare D, Lia A, Hannisdal A, Tveten Y, Matuschek E, Kahlmeter G, et al. Haemophilus influenzae with non-beta-lactamase-mediated beta-lactam resistance: easy to find but hard to categorize. J Clin Microbiol 2015; 11: 3589–95. https://doi.org/10.1128/JCM.01630-15.

    • Search Google Scholar
    • Export Citation
  • 18.

    Honda H, Sato T, Shinagawa M, Fukushima Y, Nakajima C, Suzuki Y, et al. Multiclonal expansion and high prevalence of β-lactamase-negative Haemophilus influenzae with high-level ampicillin resistance in Japan and susceptibility to quinolones. Antimicrob Agents Chemother 2018; 62(9): e00851–18. https://doi.org/10.1128/AAC.00851-18.

    • Search Google Scholar
    • Export Citation
  • 19.

    Lacross NC, Marrs CF, Patel M, Sandstedt SA, Gilsdorf JR. High genetic diversity of nontypeable Haemophilus influenzae isolates from two children attending a day care center. J Clin Microbiol 2008; 46: 3817–21. https://doi.org/10.1128/JCM.00940-08.

    • Search Google Scholar
    • Export Citation
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Cover Acta Microbiologica et Immunologica Hungarica
Acta Microbiologica et Immunologica Hungarica A Quarterly of the Hungarian Academy of Sciences
Print ISSN:
1217-8950
Online ISSN:
1588-2640

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
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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