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Bacteriology

The Clinical Urine Culture: Enhanced Techniques Improve Detection of Clinically Relevant Microorganisms

Travis K. Price, Tanaka Dune, Evann E. Hilt, Krystal J. Thomas-White, Stephanie Kliethermes, Cynthia Brincat, Linda Brubaker, Alan J. Wolfe, Elizabeth R. Mueller, Paul C. Schreckenberger
B. A. Forbes, Editor
Travis K. Price
aDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University, Chicago, Illinois, USA
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Tanaka Dune
bDepartment of Obstetrics & Gynecology and Urology, Loyola University Medical Center, Maywood, Illinois, USA
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Evann E. Hilt
aDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University, Chicago, Illinois, USA
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Krystal J. Thomas-White
aDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University, Chicago, Illinois, USA
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Stephanie Kliethermes
cDepartments of Medicine and Public Health Sciences, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA
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Cynthia Brincat
bDepartment of Obstetrics & Gynecology and Urology, Loyola University Medical Center, Maywood, Illinois, USA
dDepartment of Obstetrics & Gynecology and Urology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA
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Linda Brubaker
bDepartment of Obstetrics & Gynecology and Urology, Loyola University Medical Center, Maywood, Illinois, USA
dDepartment of Obstetrics & Gynecology and Urology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA
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Alan J. Wolfe
aDepartment of Microbiology and Immunology, Stritch School of Medicine, Loyola University, Chicago, Illinois, USA
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Elizabeth R. Mueller
bDepartment of Obstetrics & Gynecology and Urology, Loyola University Medical Center, Maywood, Illinois, USA
dDepartment of Obstetrics & Gynecology and Urology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA
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Paul C. Schreckenberger
eDepartment of Pathology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA
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B. A. Forbes
Roles: Editor
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DOI: 10.1128/JCM.00044-16
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    FIG 1

    Average CFU per milliliter of uropathogens between the UTI and no-UTI cohorts. Depicted are the average CFU per milliliter with which the various uropathogens were cultured for both cohorts: UTI (blue bars) and no-UTI (red bars). Average CFU of Klebsiella pneumoniae (P = 0.04) and Streptococcus agalactiae (P = 0.02) are significantly higher in the UTI cohort (*). Several uropathogens had substantially lower average CFU-per-milliliter values in the no-UTI cohort than in the UTI cohort: Aerococcus urinae (P = 0.12), Enterococcus faecalis (P = 0.09), Escherichia coli (P = 0.08), Staphylococcus aureus (P = 0.06), and Streptococcus anginosus (P = 0.06). Independent t test (*, P < 0.05). Black bars depict common UTI thresholds (≥105 CFU/ml and ≥103 CFU/ml).

Tables

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  • TABLE 1

    Summary of urine cultivation protocols for catheterized urine specimens

    ProtocolVol (μl) of urineMedium or mediaConditionsIncubation(s) (h) for microbial identificationPatient sample identifiera
    Standard urine culture1BAP, MacConkey agarAerobic, 35°C241–107
    Modified urine culture1BAP, MacConkey agar5% CO2, 35°C24, 48108–150
    Expanded-spectrum EQUC1, 10, and 100BAP, MacConkey agarAerobic, 35°C24, 481–150
    BAP, chocolate agar, CNA agar5% CO2, 35°C24, 48
    CDC anaerobic BAPAnaerobic, 35°C48
    CDC anaerobic BAPbMicroaerophilic gas mixture (5% O2, 10% CO2, 85% N), 35°C48
    Streamlined EQUC100BAP, MacConkey agar,c CNA agar5% CO2, 35°C481–150d
    • ↵a Refers to the patient samples on which the corresponding protocol assessed the urinary microbiota. For diagnosis, the standard urine culture protocol was used on patient samples 1 to 107; the modified standard urine culture was used on patient samples 108 to 150. For research, all patient samples were assessed by expanded-spectrum EQUC.

    • ↵b The CDC anaerobic BAP microaerophilic gas mixture condition was used only for samples 10 to 150.

    • ↵c The MacConkey 5% CO2 condition was not part of the expanded-spectrum EQUC protocol.

    • ↵d The streamlined EQUC protocol was performed using a subgroup of agars/conditions from the expanded-spectrum EQUC protocol; therefore, it was used on all patient samples.

  • TABLE 2

    Demographic characteristics and symptoms

    Clinical variableEntire cohort (n = 150)No-UTI cohort (n = 75)UTI cohort (n = 75)P valued
    Age (yr), mean (SD)62.3 (14.9)60.6 (12.3)64.0 (17.1)0.16a
    BMI (kg/m2), mean (SD)29.3 (6.3)28.8 (5.9)29.9 (6.6)0.27a
    Race/ethnicity, no. (%)
        White121 (81)59 (79)62 (83)
        Hispanic15 (10)9 (12)6 (8)
        Black9 (6)5 (7)4 (5)0.90c
        Asian4 (3)2 (3)2 (3)
        Other1 (1)0 (0)1 (1)
    No. of vaginal deliveries, median (IQR)2 (0–11)2 (0–6)2 (0–11)0.80b
    Sexually active, no. (%)58 (39)37 (49)21 (28)0.01
    Previous antibiotic treatment, no. (%)45 (30)20 (27)25 (33)0.37
    Current anticholinergic treatment, no. (%)26 (17)9 (12)17 (23)0.08
    Type of anticholinergic used, no. (%)
        Oxybutynin9 (6)3 (4)6 (8)
        Solifenacin8 (5)3 (4)5 (7)
        Fesoterodine4 (3)2 (3)2 (3)
        Tolterodine2 (1)1 (1)1 (1)0.75c
        Oxybutynin patch1 (1)0 (0)1 (1)
        Trospium chloride1 (1)0 (0)1 (1)
        Mirabegron (Myrbetriq)1 (1)0 (0)1 (1)
    Previous vaginal estrogen use, no. (%)32 (21)11 (15)21 (28)0.05
    Current vaginal estrogen use, no. (%)29 (19)10 (13)19 (25)0.06
    Prior urogynecologic surgery, no. (%)40 (27)13 (17)27 (36)0.01
    Symptoms of incontinence, no. (%)
        Stress urinary incontinence17 (11)10 (13)7 (9)0.44
        Urgency urinary incontinence26 (17)11 (15)15 (20)0.39
        Mixed urinary incontinence42 (28)27 (36)15 (20)0.03
    Urgency-frequency syndrome, no. (%)18 (12)9 (12)9 (12)0.99
    Myofascial pain, no. (%)55 (37)20 (27)35 (47)0.01
    Painful bladder syndrome, pelvic pain, and dyspareunia, no. (%)4 (3)0 (0)4 (5)0.06c
    UTISA score, mean (SD)e
        Urination regularity6.6 (4.3)5.4 (4.3)7.9 (3.9)<0.001a
        Problems with urination3.4 (3.6)2.0 (2.5)5.4 (3.7)<0.001a
        Pain associated with UTI3.2 (3.6)2.1 (3.1)4.3 (3.8)<0.001a
        Blood in the urine0.2 (0.8)0.1 (0.4)0.4 (1.1)0.08a
    • ↵a Independent t test.

    • ↵b Wilcoxon rank sum test.

    • ↵c Fisher's exact test.

    • ↵d Chi-square test used unless otherwise indicated. Boldface indicates P values that are significant at ≤0.05.

    • ↵e UTISA scores for urinary regularity, problems with urination, and pain associated with UTI range from 0 to 12. UTISA scores for blood in the urine range from 0 to 6.

  • TABLE 3

    Optimal detection of specific uropathogens by the expanded-spectrum EQUC protocola

    TABLE 3
    • ↵a Listed are the uropathogens and the number of times that each was cultured under each expanded-spectrum EQUC plating condition. The condition(s) that best detected each uropathogen is shaded.

  • TABLE 4

    Detection of uropathogens in UTI cohort without symptom improvementa

    Postenrollment questionnaire response (sample identifier)Antibiotic prescribedUropathogen(s) detected by protocol(s):
    Standard urine culture and expanded-spectrum EQUCExpanded-spectrum EQUC onlyd
    Same (145)SMZ-TMPbEscherichia coliStreptococcus anginosus
    Same (048)NitrofurantoinEscherichia coliStreptococcus anginosus
    Same (134)SMZ-TMPEscherichia coliAerococcus urinae, Corynebacterium riegelii
    Same (033)CiprofloxacinKlebsiella pneumoniae
    Same (060)NitrofurantoinEscherichia coli
    Same (109)NitrofurantoinEscherichia coli
    Same (122)CiprofloxacinEscherichia coli
    Same (135)NitrofurantoinEscherichia coli
    Same (136)NitrofurantoinEscherichia coli
    Worse (082)NitrofurantoinEscherichia coli
    Same (140)Staphylococcus lugdunensis
    Same (116)Escherichia coli
    Worse (128)Escherichia coli
    Same (126)Lactobacillus speciescStaphylococcus lugdunensis, Streptococcus anginosus
    Same (121)Proteus mirabilis
    Same (029)Aerococcus urinae, Klebsiella pneumoniae
    Same (139)Alloscardovia omnicolens, Oligella urethralis, Morganella morganii
    Same (052)Streptococcus anginosus
    Same (067)Streptococcus anginosus
    Worse (025)Candida albicans
    Worse (112)Streptococcus agalactiae, Streptococcus anginosus
    Worse (142)Escherichia coli
    Same (084)
    Same (108)
    • ↵a Uropathogens detected and missed by the standard urine culture in urine samples obtained by catheter from the UTI cohort patients who reported feeling the same or worse for the postenrollment questionnaire. Antibiotics were prescribed based on the reporting of the standard urine culture results.

    • ↵b SMZ-TMP, sulfamethoxazole-trimethoprim.

    • ↵c Lactobacillus species is not considered a uropathogen, but it was detected at >100,000 CFU/ml by standard urine culture.

    • ↵d All of the uropathogens detected by the expanded-spectrum EQUC protocol would have been detected using the streamlined EQUC protocol.

Additional Files

  • Figures
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  • Supplemental material

    • Supplemental file 1 -

      Fig. S1 (Species accumulation curves for UTI and no-UTI cohorts), S2 (Frequency of detection of genera in UTI and no-UTI cohorts), S3 (Species significantly different between UTI and no-UTI cohorts), and S4 (Detection of uropathogens in urine volumes by expanded-spectrum EQUC) and Tables S1 (Urinary microbiota characteristics), S2 (Detection of Gram-positive and Gram-negative uropathogens), and S3 (Detection of microorganisms of unknown pathogenicity in UTI cohort patients without symptom improvement)

      PDF, 1.7M

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The Clinical Urine Culture: Enhanced Techniques Improve Detection of Clinically Relevant Microorganisms
Travis K. Price, Tanaka Dune, Evann E. Hilt, Krystal J. Thomas-White, Stephanie Kliethermes, Cynthia Brincat, Linda Brubaker, Alan J. Wolfe, Elizabeth R. Mueller, Paul C. Schreckenberger
Journal of Clinical Microbiology Apr 2016, 54 (5) 1216-1222; DOI: 10.1128/JCM.00044-16

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The Clinical Urine Culture: Enhanced Techniques Improve Detection of Clinically Relevant Microorganisms
Travis K. Price, Tanaka Dune, Evann E. Hilt, Krystal J. Thomas-White, Stephanie Kliethermes, Cynthia Brincat, Linda Brubaker, Alan J. Wolfe, Elizabeth R. Mueller, Paul C. Schreckenberger
Journal of Clinical Microbiology Apr 2016, 54 (5) 1216-1222; DOI: 10.1128/JCM.00044-16
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