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Mechanisms of Resistance

Genetic Characteristics and Clonal Dissemination of β-Lactamase-Negative Ampicillin-Resistant Haemophilus influenzae Strains Isolated from the Upper Respiratory Tract of Patients in Japan

Muneki Hotomi, Keiji Fujihara, Dewan S. Billal, Kenji Suzuki, Tadao Nishimura, Shunkichi Baba, Noboru Yamanaka
Muneki Hotomi
1Department of Otolaryngology-Head and Neck Surgery, Wakayama Medical University, Wakayama, Japan
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Keiji Fujihara
1Department of Otolaryngology-Head and Neck Surgery, Wakayama Medical University, Wakayama, Japan
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Dewan S. Billal
1Department of Otolaryngology-Head and Neck Surgery, Wakayama Medical University, Wakayama, Japan
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Kenji Suzuki
2Surveillance Subcommittee, Japan Society for Infectious Diseases in Otolaryngology
3Department of Otolaryngology, Second Affiliated Hospital, Fujita Health University, Nagoya, Japan
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Tadao Nishimura
2Surveillance Subcommittee, Japan Society for Infectious Diseases in Otolaryngology
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Shunkichi Baba
2Surveillance Subcommittee, Japan Society for Infectious Diseases in Otolaryngology
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Noboru Yamanaka
1Department of Otolaryngology-Head and Neck Surgery, Wakayama Medical University, Wakayama, Japan
2Surveillance Subcommittee, Japan Society for Infectious Diseases in Otolaryngology
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  • For correspondence: ynobi@wakayama-med.ac.jp
DOI: 10.1128/AAC.00422-07
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  • FIG. 1.
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    FIG. 1.

    PCR-based genotypes of H. influenzae. Lane 1, P6 gene encoding outer membrane protein P6; lane 2, bla; lane 3, pbp3-S; lane 4, pbp3-BLN; lane *, cps b encoding type b capsular polysaccharides. MM, molecular weight marker.

  • FIG. 2.
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    FIG. 2.

    Genetic identity and/or high relatedness among BLNAR isolates. PFGE dendrogram (unweighted pair group method with arithmetic means) of 61 BLNAR strains (MIC ≥ 4 μg/ml). Dice coefficients are shown above the dendrogram. Isolates with ≥80% relatedness on the dendrogram are considered highly genetically related.

Tables

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  • TABLE 1.

    Oligonucleotide primers used in this study

    PrimerGeneSequenceProduct size (bp)
    PBP3-S ftsI Forward 5′-GATACTACGTCCTTTAAATTAAG-3′551
    Reverse 5′-GCAGTAAATGCCACATACTTA-3′
    PBP3-BLN ftsI Forward 5′-TTCAAGTAACCGTGGTGTGAC-3′465
    Reverse 5′-GCAGTAAATGCCACATATTTC-3′
    BLP bla Forward 5′-TAAGAGAATTATGCAGTGCTGCC-3′458
    Reverse 5′-TCCATAGTTGCCTGACTCCCC-3′
    P6 p6 Forward 5′-ACGATGCTGCAGGCAATGGT-3′198
    Reverse 5′-TCCATAGTTGCCTGACTCCCC-3′
    CPSB cps bForward 5′-ACGATGCGCAGGCAATGGT-3′224
    Reverse 5′-CATCAGTATTACCTTCTACTAAT-3′
  • TABLE 2.

    Sources of clinical isolates of H. influenzae

    CharacteristicTotal no. (%) of isolatesNo. (%) with susceptibility to AMPP valuea
    SusceptibleIntermediateResistant
    Total264161 (61.0)37 (14.0)66 (25.0)
    Gender
        Male143 (54.2)91 (63.6)16 (11.2)36 (25.2)NS
        Female121 (45.8)70 (57.9)21 (17.4)30 (24.8)
    Age (yr)
        0-2108 (40.9)56 (51.9)19 (17.6)33 (30.6)NS
        3-538 (14.4)27 (71.1)5 (13.2)6 (15.8)NS
        6-1219 (7.2)12 (63.2)1 (5.3)6 (31.6)NS
        13-2015 (5.7)10 (66.7)1 (6.7)4 (26.7)NS
        21-5072 (27.3)48 (66.7)9 (12.5)15 (20.8)NS
        ≥5112 (4.5)8 (66.7)2 (16.7)2 (16.7)NS
    Specimens type
        Middle ear fluid66 (25.0)34 (51.5)14 (21.2)18 (27.3)
        Nasopharyngeal secretion77 (29.2)46 (59.7)10 (13.0)21 (27.3)NS
        Nasal discharge/sinus aspirate63 (23.9)38 (60.3)9 (14.3)16 (25.4)NS
        Tonsil swab58 (22.0)43 (74.1)4 (6.9)7 (19.0)NS
    Type of clinic
        University medical center37 (14.0)23 (62.2)7 (18.9)11 (18.9)NS
        General hospital84 (31.8)49 (58.3)14 (16.7)21 (25.0)NS
        Private clinic143 (54.2)89 (62.2)16 (11.2)38 (26.6)NS
    • ↵ a NS, nonsignificant.

  • TABLE 3.

    Correlation between PCR-based genotyping and susceptibility to AMP

    PCR-based genotypeNo. of isolatesNo. of isolates with MIC to AMP (μg/ml) of:MIC (μg/ml)Susceptibility (%)a
    ≤0.120.250.512481632≥64MIC50MIC90RangeSIR
    gBLNAS873354630.50.50.12-110000
    Group I/II gBLNAR98523211823620.520.12-868.423.58.1
    Group III gBLNAR7471418241014161-329.518.971.6
    Group I/II gBLPACR1112812812800100
    Group III gBLPACR22>128>128>12800100
    gBLPAR2264>12864->12800100
    Total264858672837242610150.580.12->128
    • ↵ a S, susceptible; I, intermediate; R, resistant.

  • TABLE 4.

    Antimicrobial susceptibilities of H. influenzae isolates to other antibiotics according to PCR-based genotypes

    Antimicrobial agentPCR-based genotypeNo. of isolatesMIC (μg/ml)Susceptibility (%)a
    MIC50MIC90RangeSIR
    Clavulanate-amoxicillingBLNAS870.510.25-210000
    Group I/II gBLNAR98140.25-1692.9NA7.1
    Group III gBLNAR748322-3226.7NA73.3
    Total2591160.25-32
    CefpodoximegBLNAS870.120.12≤0.06-0.12100NA0
    Group I/II gBLNAR980.252≤0.06-890.8NA9.2
    Group III gBLNAR74816≤0.06-649.1NA91.9
    Total2590.258≤0.06-64
    CefditorengBLNAS87≤0.06≤0.06≤0.06-0.12NANANA
    Group I/II gBLNAR98≤0.060.12≤0.06-0.5NANANA
    Group III gBLNAR740.250.5≤0.06-8NANANA
    Total259≤0.060.5≤0.06-8
    CefuroximegBLNAS87120.25-1697.71.11.2
    Group I/II gBLNAR982160.25-6466.312.321.4
    Group III gBLNAR74641280.25->1281.44.194.6
    Total25921280.12->128
    ClarithromycingBLNAS878162-3279.317.23.5
    Group I/II gBLNAR988162-3275.522.52.0
    Group III gBLNAR748164-1660.839.20
    Total2598162-32
    AzithromycingBLNAS87240.25-898.8NA1.2
    Group I/II gBLNAR98240.5-1695.9NA4.1
    Group III gBLNAR74240.5-897.3NA2.7
    Total259240.25-16
    TelithromycingBLNAS87240.5-897.72.30
    Group I/II gBLNAR98240.5-893.96.10
    Group III gBLNAR74241-887.812.20
    Total259240.5-8
    LevofloxacingBLNAS87≤0.06≤0.06≤0.0610000
    Group I/II gBLNAR98≤0.06≤0.06≤0.06-0.1210000
    Group III gBLNAR74≤0.06≤0.06≤0.06-0.510000
    Total259≤0.06≤0.06≤0.06-0.5
    MeropenemgBLNAS87≤0.06≤0.06≤0.06-0.1210000
    Group I/II gBLNAR980.120.25≤0.06-0.510000
    Group III gBLNAR740.250.5≤0.06-290.509.5
    Total2590.120.5≤0.06-2
    • ↵ a S, susceptible; I, intermediate; R, resistant; NA, not available.

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Genetic Characteristics and Clonal Dissemination of β-Lactamase-Negative Ampicillin-Resistant Haemophilus influenzae Strains Isolated from the Upper Respiratory Tract of Patients in Japan
Muneki Hotomi, Keiji Fujihara, Dewan S. Billal, Kenji Suzuki, Tadao Nishimura, Shunkichi Baba, Noboru Yamanaka
Antimicrobial Agents and Chemotherapy Oct 2007, 51 (11) 3969-3976; DOI: 10.1128/AAC.00422-07

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Genetic Characteristics and Clonal Dissemination of β-Lactamase-Negative Ampicillin-Resistant Haemophilus influenzae Strains Isolated from the Upper Respiratory Tract of Patients in Japan
Muneki Hotomi, Keiji Fujihara, Dewan S. Billal, Kenji Suzuki, Tadao Nishimura, Shunkichi Baba, Noboru Yamanaka
Antimicrobial Agents and Chemotherapy Oct 2007, 51 (11) 3969-3976; DOI: 10.1128/AAC.00422-07
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KEYWORDS

ampicillin
Haemophilus influenzae
respiratory tract infections

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