Molecular Evolution of Beta-lactam-resistant Haemophilus Influenzae: 9-year Surveillance of Penicillin-binding Protein 3 Mutations in Isolates from Japan

Overview

Journal Antimicrob Agents Chemother

Publisher American Society for Microbiology

Specialty Pharmacology

Date 2006 Jun 28

PMID 16801430

Citations 26

Authors

Yumiko Sanbongi

Takahisa Suzuki

Yumi Osaki

Nami Senju

Takashi Ida

Kimiko Ubukata

Affiliations

Soon will be listed here.

Abstract

A total of 621 clinical isolates of Haemophilus influenzae collected in Japan between 1995 and 2003 were studied for their susceptibilities to several antimicrobial agents, beta-lactamase production, and amino acid substitutions in penicillin-binding protein 3 (PBP 3). Over the four study periods (first period, 1995 to 1996; second period, 1997 to 1998; third period, 2000 to 2001; fourth period, 2002 to 2003), the susceptibilities to beta-lactam agents decreased and the incidence of isolates with substitutions at positions 377, 385, 389, 517, and/or 526 in PBP 3 increased from 28.8% to 52.0%. Five hundred seventy-one beta-lactamase-nonproducing isolates were grouped into 18 classes, based on the pattern of the five mutations in PBP 3. The Asp526Lys substitution led to 6.0-, 4.3-, 2.4-, and 5.4-fold increases in amoxicillin-clavulanic acid, cefdinir, cefditoren, and faropenem resistance, respectively. PBP 3 with multiple substitutions (Met377Ile, Ser385Thr, and/or Leu389Phe) together with Asp526Lys resulted in increased resistance compared to that for PBP 3 with the Asp526Lys substitution alone. These results indicate that mutations at these five positions increased resistance to most beta-lactams. Although a significant change in the prevalence of beta-lactamase-producing strains was not observed, the proportions of those possessing both PBP 3 alterations and beta-lactamase production have slightly increased (from 1.4% to 5.0%). The ROB-1 beta-lactamase was rare, but this is the first report of this beta-lactamase in Japan.

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References

Karlowsky J, Verma G, Zhanel G, Hoban D . Presence of ROB-1 beta-lactamase correlates with cefaclor resistance among recent isolates of Haemophilus influenzae. J Antimicrob Chemother. 2000; 45(6):871-5. DOI: 10.1093/jac/45.6.871. View

Fluit A, Florijn A, Verhoef J, Milatovic D . Susceptibility of European beta-lactamase-positive and -negative Haemophilus influenzae isolates from the periods 1997/1998 and 2002/2003. J Antimicrob Chemother. 2005; 56(1):133-8. DOI: 10.1093/jac/dki167. View

Dabernat H, Delmas C, Seguy M, Pelissier R, Faucon G, Bennamani S . Diversity of beta-lactam resistance-conferring amino acid substitutions in penicillin-binding protein 3 of Haemophilus influenzae. Antimicrob Agents Chemother. 2002; 46(7):2208-18. PMC: 127296. DOI: 10.1128/AAC.46.7.2208-2218.2002. View

Hoban D, Felmingham D . The PROTEKT surveillance study: antimicrobial susceptibility of Haemophilus influenzae and Moraxella catarrhalis from community-acquired respiratory tract infections. J Antimicrob Chemother. 2002; 50 Suppl S1:49-59. DOI: 10.1093/jac/dkf810. View

Straker K, Wootton M, Simm A, Bennett P, MacGowan A, Walsh T . Cefuroxime resistance in non-beta-lactamase Haemophilus influenzae is linked to mutations in ftsI. J Antimicrob Chemother. 2003; 51(3):523-30. DOI: 10.1093/jac/dkg107. View

Suzuki K, Nishimura T, Baba S . Current status of bacterial resistance in the otolaryngology field: results from the Second Nationwide Survey in Japan. J Infect Chemother. 2003; 9(1):46-52. DOI: 10.1007/s10156-002-0209-3. View

Hasegawa K, Yamamoto K, Chiba N, Kobayashi R, Nagai K, Jacobs M . Diversity of ampicillin-resistance genes in Haemophilus influenzae in Japan and the United States. Microb Drug Resist. 2003; 9(1):39-46. DOI: 10.1089/107662903764736337. View

Hiltke T, Schiffmacher A, Dagonese A, Sethi S, Murphy T . Horizontal transfer of the gene encoding outer membrane protein P2 of nontypeable Haemophilus influenzae, in a patient with chronic obstructive pulmonary disease. J Infect Dis. 2003; 188(1):114-7. DOI: 10.1086/375724. View

Jacobs M, Felmingham D, Appelbaum P, Gruneberg R . The Alexander Project 1998-2000: susceptibility of pathogens isolated from community-acquired respiratory tract infection to commonly used antimicrobial agents. J Antimicrob Chemother. 2003; 52(2):229-46. DOI: 10.1093/jac/dkg321. View

10.

Matic V, Bozdogan B, Jacobs M, Ubukata K, Appelbaum P . Contribution of beta-lactamase and PBP amino acid substitutions to amoxicillin/clavulanate resistance in beta-lactamase-positive, amoxicillin/clavulanate-resistant Haemophilus influenzae. J Antimicrob Chemother. 2003; 52(6):1018-21. DOI: 10.1093/jac/dkg474. View

11.

Ubukata K . Problems associated with high prevalence of multidrug-resistant bacteria in patients with community-acquired infections. J Infect Chemother. 2003; 9(4):285-91. DOI: 10.1007/s10156-003-0278-y. View

12.

Hasegawa K, Chiba N, Kobayashi R, Murayama S, Iwata S, Sunakawa K . Rapidly increasing prevalence of beta-lactamase-nonproducing, ampicillin-resistant Haemophilus influenzae type b in patients with meningitis. Antimicrob Agents Chemother. 2004; 48(5):1509-14. PMC: 400528. DOI: 10.1128/AAC.48.5.1509-1514.2004. View

13.

Nazir J, Urban C, Mariano N, Burns J, Tommasulo B, Rosenberg C . Quinolone-resistant Haemophilus influenzae in a long-term care facility: clinical and molecular epidemiology. Clin Infect Dis. 2004; 38(11):1564-9. DOI: 10.1086/420820. View

14.

Vega R, SADOFF H, Patterson M . Mechanisms of ampicillin resistance in Haemophilus influenzae type B. Antimicrob Agents Chemother. 1976; 9(1):164-8. PMC: 429493. DOI: 10.1128/AAC.9.1.164. View

15.

Medeiros A, Levesque R, Jacoby G . An animal source for the ROB-1 beta-lactamase of Haemophilus influenzae type b. Antimicrob Agents Chemother. 1986; 29(2):212-5. PMC: 176379. DOI: 10.1128/AAC.29.2.212. View

16.

Dowson C, Hutchison A, Brannigan J, George R, HANSMAN D, Linares J . Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci U S A. 1989; 86(22):8842-6. PMC: 298386. DOI: 10.1073/pnas.86.22.8842. View

17.

Scriver S, Walmsley S, Kau C, Hoban D, Brunton J, McGeer A . Determination of antimicrobial susceptibilities of Canadian isolates of Haemophilus influenzae and characterization of their beta-lactamases. Canadian Haemophilus Study Group. Antimicrob Agents Chemother. 1994; 38(7):1678-80. PMC: 284617. DOI: 10.1128/AAC.38.7.1678. View

18.

Fleischmann R, Adams M, White O, Clayton R, Kirkness E, Kerlavage A . Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995; 269(5223):496-512. DOI: 10.1126/science.7542800. View

19.

Smith-Vaughan H, Sriprakash K, Mathews J, Kemp D . Nonencapsulated Haemophilus influenzae in Aboriginal infants with otitis media: prolonged carriage of P2 porin variants and evidence for horizontal P2 gene transfer. Infect Immun. 1997; 65(4):1468-74. PMC: 175155. DOI: 10.1128/iai.65.4.1468-1474.1997. View

20.

Seki H, Kasahara Y, Ohta K, Saikawa Y, Sumita R, Yachie A . Increasing prevalence of ampicillin- resistant, non-beta-lactamase-producing strains of Haemophilus influenzae in children in Japan. Chemotherapy. 1999; 45(1):15-21. DOI: 10.1159/000007160. View