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Research Article | Applied and Environmental Science

A Population-Based Surveillance Study of Shared Genotypes of Escherichia coli Isolates from Retail Meat and Suspected Cases of Urinary Tract Infections

Reina Yamaji, Cindy R. Friedman, Julia Rubin, Joy Suh, Erika Thys, Patrick McDermott, Melody Hung-Fan, Lee W. Riley
Patricia A. Bradford, Editor
Reina Yamaji
aSchool of Public Health, Division of Infectious Diseases and Vaccinology, University of California, Berkeley, California, USA
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Cindy R. Friedman
bEnteric Diseases Epidemiology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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Julia Rubin
aSchool of Public Health, Division of Infectious Diseases and Vaccinology, University of California, Berkeley, California, USA
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Joy Suh
aSchool of Public Health, Division of Infectious Diseases and Vaccinology, University of California, Berkeley, California, USA
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Erika Thys
aSchool of Public Health, Division of Infectious Diseases and Vaccinology, University of California, Berkeley, California, USA
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Patrick McDermott
cNARMS at U.S. Department of Health & Human Services/FDA, Laurel, Maryland, USA
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Melody Hung-Fan
dPublic Health Laboratory Services, Contra Costa Public Health Lab, Martinez, California, USA
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Lee W. Riley
aSchool of Public Health, Division of Infectious Diseases and Vaccinology, University of California, Berkeley, California, USA
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Patricia A. Bradford
Antimicrobial Development Specialists, LLC
Roles: Editor
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DOI: 10.1128/mSphere.00179-18
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Figures

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  • FIG 1 
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    FIG 1 

    Geographic distribution of local retail markets in Northern California, where retail meat product sampling was performed in 2016 to 2017. The light-green circle shows the location of the Contra Costa County Public Health Laboratory. The blue circle represents the location of the university-affiliated health care service. Red circles represent the locations of local markets where meat samples were purchased.

  • FIG 2 
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    FIG 2 

    Distribution of multilocus sequence types of E. coli isolates obtained in Northern California from patients suspected to have UTI seen at the university health service (A) and from retail meat products (B).

  • FIG 3 
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    FIG 3 

    Venn diagram of the multilocus sequence genotypes of E. coli isolates obtained in Northern California from retail meat products and patients with urinary tract infections.

  • FIG 4 
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    FIG 4 

    Population snapshot of E. coli isolates obtained in Northern California from patients suspected to have UTIs seen at the university health service and retail meat products. Genetic relationships among 395 E. coli isolates from human urine samples and retail meat products were visualized by the goeBURST algorithm based on the PHYLOViZ software (http://www.phyloviz.net/). Each circle represents a distinct genotype; the size of a circle is proportional to the number of isolates. Representative STs are shown as numbers without the ST prefix. The numbers in squares represent the shared genotypes (sequence type without the ST prefix) between urine and meat E. coli isolates. STs that are single-locus variants are connected with thick black lines. STs that are double-locus variants are connected with thin black lines. STs that are different at three or more loci are connected with dotted lines. Gray shading indicates that more than two STs belong to one clonal complex. (A) Isolates from three source groups (human urine samples, poultry meat samples, and pork and beef samples). (B) Isolates from two source groups (human urine samples and poultry meat samples).

Tables

  • Figures
  • Supplemental Material
  • TABLE 1 

    E. coli isolates belonging to the 12 MLST genotypes found in both human urine and retail meat samples

    Sequence
    type
    No. of E. coli isolates belonging to the MLST genotype
    Retail meat samplesaHuman
    urine
    samples
    TurkeyChickenPorkBeefAll meat
    ST1174810131
    ST10222176
    ST695200722
    ST101032051
    ST38020021
    ST1310200212
    ST1844110021
    ST80100011
    ST88100012
    ST569010012
    ST906001011
    ST2562001011
    Total14 (32.6)21 (48.8)7 (16.3)1 (2.3)43 (100)51
    • ↵a Numbers in parentheses represent the percentage of isolates from each type of meat.

  • TABLE 2 

    Antimicrobial drug susceptibility of E. coli isolates of the 12 genotypes shared by human urine and retail meat samplesa

    Genotype
    (total no. of
    isolates typed)
    Human urine samplesRetail meat samplesP value
    No. of pan-
    susceptible
    isolatesb
    Drug resistancec
    (no. of isolates)
    No. of pan-
    susceptible
    isolates
    Drug resistance
    (no. of isolates)
    ST117 (14)109AMP (1)
    GEN (2)
    TMP-SMZ+GEN (1)1.00
    ST10 (13)2AMP (2)5AMP (1)
    AMP+TMP-SMZ (1)TMP-SMZ (1)0.29
    AMP+CTX+TMP-SMZ+GEN (1)
    ST69 (29)4AMP (3)1AMP (6)
    TMP-SMZ (1)
    AMP+TMP-SMZ (11)
    AMP+TMP-SMZ+GEN (1)1.00
    AMP+TMP-SMZ+FOS (1)
    AMP+TMP-SMZ+GEN+CTX+CIP (1)
    ST101 (6)0AMP (1)500.17
    ST38 (3)0AMP+CTX+TMP-SMZ+NIT (1)0AMP (1)
    NIT (1)1.00
    ST131 (14)3AMP+CIP (2)1GEN (1)
    AMP+GEN (1)
    AMP+TMP-SMZ+GEN (1)0.51
    AMP+TMP-SMZ+CIP (1)
    AMP+CIP+GEN+CTX+CAZ (3)
    AMP+CIP+GEN+CTX+CAZ+TMP-SMZ (1)
    ST1844 (3)10201.00
    ST80 (2)10101.00
    ST88 (3)0AMP (2)0AMP+GEN (1)1.00
    ST569 (3)1AMP (1)101.00
    ST906 (2)10101.00
    ST2562 (2)10101.00
    Total153627160.002
    • ↵a Antimicrobial drug abbreviations: AMP, ampicillin; CAZ, ceftazidime; CIP, ciprofloxacin; CTX, cefotaxime; GEN, gentamicin; NIT, nitrofurantoin; TMP-SMZ, trimethoprim-sulfamethoxazole.

    • ↵b Pan-susceptible isolates were defined as those susceptible to all nine antimicrobial agents tested: AMP, TMP-SMZ, CIP, CTX, FOX, CAZ, NIT, FOS, and GEN. 

    • ↵c Resistant isolates contain those resistant to at least one antimicrobial agent of nine antimicrobial agents tested: AMP, TMP-SMZ, CIP, CTX, FOX, CAZ, NIT, FOS, and GEN. Resistance to specific antimicrobial agents is indicated.

  • TABLE 3 

    β-Lactamase gene types identified among ampicillin-resistant E. coli isolates of the 12 shared genotypes

    Sequence typeβ-Lactamase gene type (no. of isolates)a
    Human urine samplesRetail meat products
    ST117NAblaTEM type (1)
    ST10blaTEM type (2)blaTEM type (1)
    ST69blaTEM type (14)blaTEM type (6)
    blaTEM type + blaCTX-M group 1 (1)
    Other (2)
    ST101blaTEM type + blaCTX-M group 1 (1)NA
    ST38Other (1)Other (1)
    ST131blaCTX-M group 1 + blaOXA type (4)NA
    blaTEM type + blaCTX-M group 9 (1)
    blaOXA type (1)
    blaTEM type (3)
    ST88blaTEM type (1)Other (1)
    Other (1)
    ST569blaTEM type (1)NA
    • ↵a NA, not applicable. Other denotes ampicillin-resistant isolates that did not have any blaTEM-type, blaCTX-M-type, blaOXA-type, blaSHV-type, or blaAmpC-type genes. The bla types and genes included in the bla types follow: blaTEM type, blaTEM-1 and blaTEM-2; blaSHV type, blaSHV-1; blaCTX-M group 1, blaCTX-M-1, blaCTX-M-3, and blaCTX-M-15; blaCTX-M group 2, blaCTX-M-2; blaCTX-M group 9, blaCTX-M-9 and blaCTX-M-14; blaCTX-M group 8/25, blaCTX-M-8, blaCTX-M-25, blaCTX-M-26, and blaCTX-M-39 to blaCTX-M-41; blaOXA type, blaOXA-1, blaOXA-4, and blaOXA-30.

Supplemental Material

  • Figures
  • Tables
  • DATA SET S1 

    Number of E. coli isolates with designated genotype from patients with UTIs and retail meat products in Northern California in 2016 to 2017. Among E. coli isolates from retail meat samples, seven isolates, including two from turkey, three from chicken, and two from pork could not be assigned an ST designation. Among E. coli isolates from human urine samples, eight isolates could not be assigned an ST designation. The isolates with no ST designation are not contained in the data set. Download DATA SET S1, XLSX file, 0.01 MB.

    Copyright © 2018 Yamaji et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • DATA SET S2 

    Number of genotypes of E. coli isolates contained in a single sample for each type of meat. Download DATA SET S2, XLSX file, 0.01 MB.

    Copyright © 2018 Yamaji et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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A Population-Based Surveillance Study of Shared Genotypes of Escherichia coli Isolates from Retail Meat and Suspected Cases of Urinary Tract Infections
Reina Yamaji, Cindy R. Friedman, Julia Rubin, Joy Suh, Erika Thys, Patrick McDermott, Melody Hung-Fan, Lee W. Riley
mSphere Aug 2018, 3 (4) e00179-18; DOI: 10.1128/mSphere.00179-18

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A Population-Based Surveillance Study of Shared Genotypes of Escherichia coli Isolates from Retail Meat and Suspected Cases of Urinary Tract Infections
Reina Yamaji, Cindy R. Friedman, Julia Rubin, Joy Suh, Erika Thys, Patrick McDermott, Melody Hung-Fan, Lee W. Riley
mSphere Aug 2018, 3 (4) e00179-18; DOI: 10.1128/mSphere.00179-18
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    • ABSTRACT
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KEYWORDS

Escherichia coli
extraintestinal diseases
molecular epidemiology
multidrug resistance
multilocus sequence typing
urinary tract infection
uropathogenic E. coli

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