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Serotype distribution and β-lactam resistance in Haemophilus influenzae isolated from patients with respiratory infections in Korea

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Abstract

Haemophilus influenzae is a frequent causative bacterial pathogen of respiratory tract infections. Resistance to β-lactam antibiotics has been a significant clinical problem in treatment for H. influenzae respiratory infections. This study describes the serotype, antibiotic resistance and distribution of TEM-1 or ROB-1 β-lactamase in H. influenzae isolates from local private hospitals from 2002 to 2004. Among the 100 H. influenzae respiratory isolates, only 7% were identified as serotypes a, b, e, and f, with the remaining 93% being nontypeable. Resistance to ampicillin, cefaclor, and tetracycline was 57%, 46%, and 16%, respectively. All strains were susceptible to azithromycin and ciprofloxacin, whereas amoxicillin/clavulanate, cefotaxime, and imipenem exhibited reduced susceptibilities of 99%, 99%, and 91%, respectively. All 57 ampicillinresistant strains (minimum inhibitory concentration, MIC≥4 μg/ml) were β-lactamase-positive and possessed the TEM-1 type β-lactamase. One β-lactamase-positive amoxicillin/clavulanate-resistant isolate that was resistant to ampicillin (MIC>128 μg/ml) had the TEM-1 type β-lactamase and not susceptible to cefaclor and cefotaxime. Analysis of penicillin binding protein 3 revealed six residues (Asp-350, Met-377, Ala-502, Asn-526, Val-547, and Asn-569) that were substituted by Asn, Ile, Val, Lys, Ile, and Ser, respectively.

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References

  • Abdel-Rahman, E.M., N.A. Ismael, and R.A. Dixon. 2000. Antibiotic resistance and prevalence of β-lactamase in Haemophilus influenzae isolates — a surveillance study of patients with respiratory infection in Saudi Arabia. Diagn. Microbiol. Infect. Dis. 36, 203–208.

    Article  CAS  PubMed  Google Scholar 

  • Adderson, E.E., C.L. Byington, L. Spencer, A. Kimball, M. Hindiyeh, K. Carroll, S. Moiitce, E.K. Korgenski, J.C. Christenson, and A.T. Pavia. 2001. Invasive serotype a Haemophilus influenzae infections with a virulence genotype resembling Haemophilus influnenzae type b: emerging pathogen in the vaccine era? Pediatrics 108, 1–6.

    Article  Google Scholar 

  • Alpuche, C., J. Garau, and V. Lim. 2007. Global and local variations in antimicrobial susceptibilities and resistance development in the major respiratory pathogens. Int. J. Antimicrob. Agents 30, 135–138.

    Article  Google Scholar 

  • Bozdogan, B., S. Tristram, and P.C. Appelbaum. 2006. Combination of altered PBPs and expression of cloned extended-spectrum β-lactamases confer cefotaxime resistance in Haemophilus influenzae. J. Antimicrob. Chemother. 57, 747–749.

    Article  CAS  PubMed  Google Scholar 

  • Cao, L.D., I. Naruhiko, T. Nobue, and K. Yoichi. 2004. Antimicrobial susceptibility of respiratory Haemophilus influenzae strains isolated from pediatric respiratory tract infections. Pediatr. Int. 46, 419–424.

    Article  CAS  PubMed  Google Scholar 

  • Chong, Y.S., K.S. Song, C.H. Pai, E.C. Kim, and T.Y. Choi. 1992. Haemophilus influenzae isolated from sputum specimens: prevalence, biotypes and antimicrobial susceptibility. Korean J. Infect. Dis. 24, 107–113.

    Google Scholar 

  • Clinical and Laboratory Standards Institute (CLSI). 2008. Performance Standards for Antimicrobial Susceptibility Testing. Eighteenth Informational Supplement. Approved Standard, M100-S18. Clinical and Laboratory Standards Institute, Wayne, PA, USA.

    Google Scholar 

  • Dabernat, H., C. Delmas, M. Sequy, R. Pelisser, G. Faucon, S. Bennamani, and C. Pasquier. 2002. Diversity of beta-lactam resistance-conferring amino acid substitutions in penicillin-binding protein 3 of Haemophilus influenzae. Antimicrob. Agents Chemother. 46, 2208–2218.

    Article  CAS  PubMed  Google Scholar 

  • Doern, G.V., A.B. Brueggemann, G. Pierce, H.P. Holley, and A. Rauch. 1997. Antibiotic resistant among clinical isolates of Haemophilus influenzae in the United States in 1994 and 1995 and detection of β-lactamase-positive strains resistant to amoxicillinclavulanate: results of a national multicenter surveillance study. Antimicrob. Agents Chemother. 41, 292–297.

    CAS  PubMed  Google Scholar 

  • Falla, T.J., D.W.M. Crook, L.N. Brophy, D. Maskell, J.S. Kroll, and E.R. Moxon. 1994. PCR for capsular typing of Haemophilus influenzae. J. Clin. Microbiol. 32, 2382–2386.

    CAS  PubMed  Google Scholar 

  • Heath, P.T., R. Booy, H.J. Azzopardi, M.P. Slack, J. Fogarty, A.C. Moloney, M.E. Ramsay, and E.R. Moxon. 2001. Non-type b Haemophilus influenzae disease: clinical and epidemiologic characteristics in the Haemophilus influenzae type b vaccine era. Pediatr. Infect. Dis. J. 20, 300–305.

    Article  CAS  PubMed  Google Scholar 

  • Hoban, D. and D. Felmingham. 2002. The PROTEKT surveillance study: antimicrobial susceptibility of Haemophilus influenzae and Moraxella catarrhalis from community-acquired respiratory tract infections. J. Antimicrob. Chemother. 50, 49–59.

    CAS  PubMed  Google Scholar 

  • Kaczmarek, F.S., T.D. Gootz, F. Dib-Hajj, W. Shang, S. Hallowell, and M. Cronan. 2004. Genetic and molecular characterization of β-lactamase-negative ampicillin-resistant Haemophilus influenzae with unusually high resistance to ampicillin. Antimicrob. Agents Chemother. 48, 1630–1639.

    Article  CAS  PubMed  Google Scholar 

  • Karlowsky, J.A., I.A. Critchley, R.S. Blosser-Middleton, E.A. Karginova, M.E. Jones, C. Thornsberry, and D.F. Saham. 2002. Antimicrobial surveillance of Haemophilus influenzae in the United States during 2000–2001 leads to detection of clonal dissemination of a β-lactamase-negative and ampicillin-resistant strain. J. Clin. Microbiol. 40, 1063–1066.

    Article  CAS  PubMed  Google Scholar 

  • Kim, I.S., C.S. Ki, S.J. Kim, W.S. Oh, K.R. Peck, J.H. Song, K.W. Lee, and N.Y. Lee. 2007. Diversity of ampicillin resistance genes and antimicrobial susceptibility patterns in Haemophilus influenzae strains isolated in Korea. Antimicrob. Agents Chemother. 51, 453–460.

    Article  CAS  PubMed  Google Scholar 

  • Kwak, Y.H., H.S. Jung, S.E. Park, J.Y. Park, E.C. Kim, H.J. Lee, and M.R. Jacobs. 2000. Serotypes and antimicrobial susceptibility in clinical isolates of Haemophilus influenzae from Korean children in prevaccination era. J. Korean Med. Sci. 15, 616–622.

    CAS  PubMed  Google Scholar 

  • Luong, D.C., N. Ishiwada, N. Takeda, and Y. Kohno. 2004. Serotypes of Haemophilus influenzae strains isolated from pediatric patients with respiratory tract infections. Tohoku J. Exp. Med. 202, 245–254.

    Article  CAS  PubMed  Google Scholar 

  • Nissinen, A., E. Herva, M.L. Katila, S. Kontiainen, L. Iimatanen, S. Oinonen, A.K. Takala, and P. Huovinen. 1995. Antimicrobial resistance in Haemophilus influenzae isolated from blood, cerebrospinal fluid, middle ear fluid and throat samples of children. A nationwide study in Finland in 1988–1990. Scand. J. Infect. Dis. 27, 57–61.

    Article  CAS  PubMed  Google Scholar 

  • Pittman, M. 1931. Variation and type specificity in the bacterial species Haemophilus influenzae. J. Exp. Med. 53, 471–492.

    Article  PubMed  Google Scholar 

  • Tenover, F.C., M.B. Huang, J.K. Rasheed, and D.H. Fersing. 1994. Development of PCR assays to detect ampicillin resistance genes in cerebrospinal fluid samples containing Haemophilus influenzae. J. Clin. Microbiol. 32, 2729–2737.

    CAS  PubMed  Google Scholar 

  • Tristram, S., M.R. Jacobs, and P.C. Appelbaum. 2007. Antimicrobial resistance in Haemophilus influenzae. Clin. Microbiol. Rev. 20, 368–389.

    Article  CAS  PubMed  Google Scholar 

  • Waggoner-Fountain, L.A., J.O. Hendley, E.J. Cody, V.A. Perriello, and L.G. Donowitz. 1995. The emergence of Haemophilus influenzae types e and f as significant pathogens. Clin. Infect. Dis. 21, 1322–1324.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Bacterial Respiratory Infections, Center for Infectious Diseases, National Institute of Health, Korea Centers for Disease Control and Prevention, Seoul, 122-701, Republic of Korea

    Songmee Bae, Jaehoon Lee, Eunah Kim, Jaehwa Lee, Jaeyon Yu & Yeonho Kang

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  1. Songmee Bae
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  2. Jaehoon Lee
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  3. Eunah Kim
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  4. Jaehwa Lee
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  6. Yeonho Kang
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Correspondence to Songmee Bae.

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Bae, S., Lee, J., Kim, E. et al. Serotype distribution and β-lactam resistance in Haemophilus influenzae isolated from patients with respiratory infections in Korea. J Microbiol. 48, 84–88 (2010). https://doi.org/10.1007/s12275-009-0212-9

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  • DOI: https://doi.org/10.1007/s12275-009-0212-9

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