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Bacteriology

Genotypes of Klebsiella oxytoca Isolates from Patients with Nosocomial Pneumonia Are Distinct from Those of Isolates from Patients with Antibiotic-Associated Hemorrhagic Colitis

Kathrin A. T. Herzog, Georg Schneditz, Eva Leitner, Gebhard Feierl, Karl Martin Hoffmann, Ines Zollner-Schwetz, Robert Krause, Gregor Gorkiewicz, Ellen L. Zechner, Christoph Högenauer
W. M. Dunne Jr., Editor
Kathrin A. T. Herzog
aDivision of Gastroenterology and Hepatology, Department of Internal Medicine, Medical University of Graz, Graz, Austria
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Georg Schneditz
bInstitute of Molecular Biosciences, University of Graz, Graz, Austria
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Eva Leitner
cInstitute of Hygiene, Microbiology and Environmental Medicine, Medical University of Graz, Graz, Austria
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Gebhard Feierl
cInstitute of Hygiene, Microbiology and Environmental Medicine, Medical University of Graz, Graz, Austria
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Karl Martin Hoffmann
dDivision of General Pediatrics, Department of Pediatrics and Adolescent Medicine, Medical University of Graz, Graz, Austria
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Ines Zollner-Schwetz
eSection of Infectious Diseases and Tropical Medicine, Department of Internal Medicine, Medical University of Graz, Graz, Austria
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Robert Krause
eSection of Infectious Diseases and Tropical Medicine, Department of Internal Medicine, Medical University of Graz, Graz, Austria
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Gregor Gorkiewicz
fInstitute of Pathology, Medical University of Graz, Graz, Austria
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Ellen L. Zechner
bInstitute of Molecular Biosciences, University of Graz, Graz, Austria
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Christoph Högenauer
aDivision of Gastroenterology and Hepatology, Department of Internal Medicine, Medical University of Graz, Graz, Austria
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W. M. Dunne Jr.
Roles: Editor
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DOI: 10.1128/JCM.03373-13
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  • FIG 1
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    FIG 1

    Neighbor-joining tree showing the genetic relatedness of 74 clinical K. oxytoca isolates combined with clinical and phenotypic information. Stool isolates are indicated by green squares and respiratory isolates by orange squares, shown to the right of the isolate number. Bootstrap values, denoting the reliability of the given branches, are shown next to the tree nodes. Only values of >60% are shown. Clusters/subclusters are indicated in large letters on the tree. All the isolates were resistant to ampicillin. The scale bar represents 0.01 substitutions per site. CC, clonal complex; r.t., respiratory tract; u.t., urinary tract; AAHC, antibiotic-associated hemorrhagic colitis; COPD, chronic obstructive pulmonary disease; CSSTI, complicated skin and skin structure infection; DFS, diabetic foot syndrome; IBD, inflammatory bowel disease; UTI, urinary tract infection; VAP, ventilator-associated pneumonia; AUT, Austria; ESP, Spain; GER, Germany; HKG, Hong Kong; JPN, Japan; NED, Netherlands; ESBL, extended spectrum β-lactamase; CRE, carbapenem-resistant Enterobacteriaceae; N, nosocomial; O, outpatient; n/a, information not available.

  • FIG 2
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    FIG 2

    Clonal diversity of K. oxytoca isolates. eBURST (22) was used to calculate clonal complexes (CC) that contain single-locus variants (SLVs) that share 6 of 7 MLST alleles (STs connected by lines). The single-locus difference between SLVs is indicated by the gene name next to the connecting line. The relative positions and spacing between the STs are not related to genetic distance. Each ST is represented by a dot, the size of which varies directly with the frequency of the ST in the population.

  • FIG 3
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    FIG 3

    Split decomposition analysis for K. oxytoca strains. SplitsTree (23) was used for analysis of concatenated sequences of the seven MLST loci. Each K. oxytoca ST (included in Fig. 1), regardless of frequency within the population, was included once in the analysis.

Tables

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  • TABLE 1

    Clinical and phenotypical attributes of K. oxytoca isolatesa

    Isolation siteDiagnosisbN and/or OcToxindCountry of isolatione
    Stool (40)AAHC (16), diarrhea/colitis of other causes (11), IBD (3), asymptomatic carrier (7), follow-up/AAHC (1), asymptomatic carrier/UTI (1), NA (1)N (9), O (25), NA (6)Positive (31), Negative (9)JPN (1), USA (1), NED (2), AUT (30), ESP (1), HKG (3), GER (2)
    Respiratory tract (21)Nosocomial pneumonia/VAP (13), COPD (2), cystic fibrosis (1), pneumonia (2), pharyngitis (2), pneumothorax (1)N (15), O (6)Positive (3), Negative (18)AUT (21)
    Urinary tract (4)UTI (4)N (2), O (2)Negative (4)AUT (4)
    Blood (2)AAHC with bacteremia (1), bacteremia (1)O (2)Positive (1), Negative (1)AUT (2)
    Skin/mucous membranes (7)DFS (4), CSSTI (2), oral abscess (1)O (7)Positive (4), Negative (3)AUT (7)
    • ↵a The number of isolates within a given category is shown in parentheses.

    • ↵b AAHC, antibiotic-associated hemorrhagic colitis; IBD, inflammatory bowel disease; UTI, urinary tract infection; VAP, ventilator-associated pneumonia; COPD, chronic obstructive pulmonary disease; DFS, diabetic foot syndrome; CSSTI, complicated skin and skin structure infection.

    • ↵c Isolates were classified as nosocomial (N) when infection occurred 48 h after hospitalization. O, outpatient; NA, information not available.

    • ↵d Cytotoxicity was assessed via an MTT-based cell culture assay (6).

    • ↵e JPN, Japan; NED, Netherlands; AUT, Austria; ESP, Spain; HKG, Hong Kong; GER, Germany.

  • TABLE 2

    Nucleotide polymorphisms among K. oxytoca isolates and MLST target and PCR primer information

    GenePutative gene functionOligonucleotideOligonucleotide sequence (5′ to 3′)aSize of analyzed fragment (bp)No. of allelesbNo. of polymorphic sitesbMean % G+C contentVariation indicesb
    πcdN/dSd
    gapAGlyceraldehyde-3-phosphate dehydrogenasegapA_fwdGTTTTCCCAGTCACGACGTTGTATGAAGTATGACTCCACTCACGG4508 (9)15 (16)53.70.01340 (0.01335)0.000 (0.000)
    gapA_revTTGTGAGCGGATAACAATTTCAACGCCTTTCATTGCGCCTTCGGAA
    infBTranslation initiation factor 2infB_fwdGTTTTCCCAGTCACGACGTTGTACTCTCTGCTGGACTACATTCG31815 (17)48 (50)59.20.05615 (0.05625)0.139 (0.137)
    infB_revTTGTGAGCGGATAACAATTTCCGCTTTCAGCTCCAGAACTTC
    mdhMalate dehydrogenasemdh_fwdGTTTTCCCAGTCACGACGTTGTACCCAACTGCCTTCAGGTTCAG47725 (25)86 (86)52.10.05222 (0.05233)0.032 (0.031)
    mdh_revTTGTGAGCGGATAACAATTTCCCTTCCACGTAGGCGCATTCC
    pgiPhosphoglucose isomerasepgi_fwdGTTTTCCCAGTCACGACGTTGTAGAGAAAAACCTGCCGGTGCTGCTG43227 (29)45 (45)56.20.03008 (0.03023)0.008(0.008)
    pgi_revTTGTGAGCGGATAACAATTTCCGGTTAATCAGGCCGTTAGTGGAGC
    phoEPhosphoporine EphoE_fwdGTTTTCCCAGTCACGACGTTGTAACCTGGCGCAACACCGATTTCTTC42026 (28)52 (54)53.70.03315 (0.03337)0.020 (0.019)
    phoE_revTTGTGAGCGGATAACAATTTCTTCAGCTGGTTGATTTTGTAATCCAC
    rpoBRNA polymerase subunit βrpoB_fwdGTTTTCCCAGTCACGACGTTGTAGGCGAAATGGCGGAAAACCA50119 (21)40 (42)54.30.01777 (0.01812)0.001 (0.001)
    rpoB_revTTGTGAGCGGATAACAATTTCGAGTCTTCGAAGTTGTAACC
    tonBPeriplasmic energy transducertonB_fwdGTTTTCCCAGTCACGACGTTGTACTCTATACTTCGGTACATCAGGTT40525 (27)78 (79)61.90.05920 (0.06001)0.092 (0.095)
    tonB_revTTGTGAGCGGATAACAATTTCCCTGTTTGGCGGCCAGCACCTGGT
    Concatenated sequence3,00355.60.03607 (0.03631)
    • ↵a Specific oligonucleotides: bold-type sequence binds target gene, underlined sequence (overhang) serves as annealing site for sequencing primer (phoE was sequenced with distinct nested primers).

    • ↵b Publicly available K. oxytoca NCBI sequence data were combined with the Sanger sequences from clinical isolates to generate a separate alignment which yielded the values given in brackets.

    • ↵c Diversity index (π) is equal to the average number of nucleotide differences per site.

    • ↵d dN/dS, ratio of nonsynonymous to synonymous substitutions.

  • TABLE 3

    Primers used for Sanger sequencing in this study

    Primer nameSequence (5′ to 3′)
    MLST_seq_fwdGTTTTCCCAGTCACGACGTTGTA
    MLST_seq_revTTGTGAGCGGATAACAATTTC
    phoE_seq_fwdTTTCTTCGGCGTGGTAGATCC
    phoE_seq_revGTAATCCACAAAGGCATTC
  • TABLE 4

    Clinical, genetic, and phenotypic information of sequence types represented by more than one K. oxytoca isolate

    Sequence typeIsolateToxinaGeographic originbIsolation siteDiagnosiscIsolation date (mo/yr)Antibiotic resistance typedNosocomial (N)/outpatient (O)eClonal complexCluster
    134+AUT (Graz)StoolAAHC3/2004OA
    145+AUT (Graz)StoolFollow-up/AAHC4/2004OA
    256+AUT (Graz)StoolAAHC4/2004O2A
    2379+ESPStool/rectal swabNA5/2009CREN2A
    433−AUT (Styria)SkinCSSTI5/2004O8A
    473−AUT (Graz)StoolAsymptomatic carrier4/2004ESBLN8A
    481+AUT (Graz)StoolAsymptomatic carrier6/2005O8A
    4204+AUT (Graz)StoolAAHC8/2008ESBLO8A
    4231−AUT (Graz)Respiratory tractNosocomial pneumonia10/2010ESBL + CREN8A
    4402−AUT (Graz)Respiratory tractPneumonia6/2013O8A
    937+AUT (Graz)StoolAsymptomatic carrier4/2004ESBLNA
    9128+AUT (Styria)StoolIBD3/2007OA
    9188+AUT (Vienna)StoolAAHC1/2008NAA
    9222+AUT (Graz)StoolAAHC11/2009ESBLOA
    9232+AUT (Graz)BloodAAHC with bacteremia8/2010OA
    9382+AUT (Graz)StoolIBD8/2013OA
    9425+GERStoolDiarrhea2013OA
    1175−AUT (Graz)skinDFS4/2004O4B1
    11400−AUT (Graz)Respiratory tractVAP6/2013N4B1
    18113−AUT (Burgenland)StoolAsymptomatic carrier6/2005O2A
    18336+HKGStoolDiarrheaNANA2A
    33180−AUT (Graz)StoolAAHC12/2007O1A
    33227+AUT (Vienna)StoolAAHC6/2010O1A
    36195+AUT (Graz)StoolUTI1/2008NA
    36195-H−AUT (Graz)Urinary tractUTI1/2008NA
    38131−AUT (Styria)StoolAsymptomatic carrier4/2007OB2
    38333+AUT (Salzburg)StoolColitis3/2014OB2
    4021−AUT (Graz)Respiratory tractVAP11/2003NB1
    40284−AUT (Graz)Respiratory tractNosocomial pneumonia2/2012NB1
    4123−AUT (Graz)Respiratory tractVAP11/2003N3B1
    41389−AUT (Graz)Respiratory tractPneumothorax9/2013O3B1
    4440−AUT (Graz)Respiratory tractVAP5/2004ESBLNB1
    44179−AUT (Styria)Urinary tractUTI11/2007ESBLOB1
    • ↵a Cytotoxicity was assessed via an MTT-based cell culture assay (6).

    • ↵b AUT, Austria; ESP, Spain; GER, Germany; HKG, Hong Kong.

    • ↵c AAHC, antibiotic-associated hemorrhagic colitis; NA, information not available; CSSTI, complicated skin and skin structure infection; IBD, inflammatory bowel disease; DFS, diabetic foot syndrome; VAP, ventilator-associated pneumonia; UTI, urinary tract infection.

    • ↵d All isolates were resistant to ampicillin. ESBL, extended spectrum β-lactamase; CRE, carbapenem-resistant Enterobacteriaceae.

    • ↵e Isolates were classified as nosocomial when infection occurred after 48 h of hospitalization.

Additional Files

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  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 1 -

      Fig. S1 (Neighbor-joining tree showing the genetic relatedness of 54 clinical K. oxytoca isolates, including 7 isolates with published sequences), S2 (Similar phylogenetic clustering of K. oxytoca isolates is obtained based on concatenated MLST target sequences and results of whole-genome BLAST search results), and S3 (Neighbor-joining trees based on the individual genetic loci of the K. oxytoca MLST scheme) and Table S1 (Summary of genetic, typing, and clinical information for K. oxytoca isolates included in this study)

      PDF, 1.6M

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Genotypes of Klebsiella oxytoca Isolates from Patients with Nosocomial Pneumonia Are Distinct from Those of Isolates from Patients with Antibiotic-Associated Hemorrhagic Colitis
Kathrin A. T. Herzog, Georg Schneditz, Eva Leitner, Gebhard Feierl, Karl Martin Hoffmann, Ines Zollner-Schwetz, Robert Krause, Gregor Gorkiewicz, Ellen L. Zechner, Christoph Högenauer
Journal of Clinical Microbiology Apr 2014, 52 (5) 1607-1616; DOI: 10.1128/JCM.03373-13

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Genotypes of Klebsiella oxytoca Isolates from Patients with Nosocomial Pneumonia Are Distinct from Those of Isolates from Patients with Antibiotic-Associated Hemorrhagic Colitis
Kathrin A. T. Herzog, Georg Schneditz, Eva Leitner, Gebhard Feierl, Karl Martin Hoffmann, Ines Zollner-Schwetz, Robert Krause, Gregor Gorkiewicz, Ellen L. Zechner, Christoph Högenauer
Journal of Clinical Microbiology Apr 2014, 52 (5) 1607-1616; DOI: 10.1128/JCM.03373-13
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