YAJEM-57254; No of Pages 5

American Journal of Emergency Medicine xxx (2018) xxx–xxx

Contents lists available at ScienceDirect

American Journal of Emergency Medicine

journal homepage: www.elsevier.com/locate/ajem

Risk factors of urinary tract infection caused by extended spectrum β-lactamase-

producing Escherichia coli in emergency department☆
Hyeonseok Lee, Seung Baik Han, Ji Hye Kim, Soo Kang, Areum Durey ⁎
Department of Emergency Medicine, Inha University School of Medicine, Incheon, Republic of Korea

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: The incidence of urinary tract infection (UTI) due to extended-spectrum β-lactamase (ESBL)-producing
Received 27 December 2017 Escherichia coli has increased over recent years. Initial empirical therapy is often ineffective for these resistant iso-
Received in revised form 10 January 2018 lates resulting in prolonged hospitalization and increased mortality. This study was conducted to determine the
Accepted 12 January 2018 risk factors of UTI caused by ESBL E. coli in the emergency department (ED).
Available online xxxx
Methods: This is a retrospective case-control study at a university hospital in Korea with UTI patients who visited
ED between June 2015 and December 2016. We compared case patients with ESBL E. coli UTI (n = 50) to control
Keywords:
Extended-spectrum beta-lactamase
patients with non-ESBL-producing E. coli UTI (n = 100), which were matched for age and sex. Multivariate logistic
Urinary tract infection regression analysis was used to explore risk factors.
Risk factors Results: Our study showed that hospital-acquired infection (OR = 3.86; 95% CI = 1.26–11.8; p = .017), prior UTI
Emergency department within 1 year (OR = 3.26; 95% CI = 1.32–8.05; p = .010), and underlying cerebrovascular disease (OR = 3.24;
Escherichia coli 95% CI = 1.45–7.25; p = .004) were independent risk factors for acquisition of ESBL-producing E. coli. Notably,
Community-acquired infection 35 (70%) out of 50 case patients had community-acquired infection, and 68% and 54% of ESBL E. coli were resistance
to ciprofloxacin and trimethoprim-sulfamethoxazole, respectively. On the contrary, 98% of ESBL E. coli was suscep-
tible to amikacin.
Conclusion: The main risk factors identified in our study should be considered when treating UTI patients in ED.
Amikacin may improve the outcome of empirical treatment without increasing carbapenem utilization.
© 2018 Elsevier Inc. All rights reserved.

1. Introduction ineffective leading to prolonged hospitalization, rising medical costs

Urinary tract infection (UTI) is a very common disease encountered
in the emergency department (ED), and Escherichia coli is known to
account for 75–90% of bacterial isolates in community-onset UTI [1].
Recently, the incidence of UTI due to extended-spectrum β-lactamase
(ESBL)-producing E. coli in the United States has increased in both com-
munity and tertiary-care hospitals [2, 3], and the prevalence of ESBL-
producing E. coli was reported to range from 3.3% to 40.4% in Europe [4].
Increasing incidence of ESBL-producing E. coli is a clinical challenge
to emergency physicians in treating UTI patients because ESBL are
capable of degrading the β-lactam ring of most of the penicillins,
cephalosporins and aztreonam [5]. Moreover, some ESBL plasmids
carry additional genes that give resistance to aminoglycosides, sulfon-
amides, and fluoroquinolones [6]. Treatment options for UTI due to
ESBL E. coli are therefore limited, and initial empirical therapy is often
and increased mortality [7, 8].
Despite the clinical importance of the widespread emergence of
these multidrug-resistant uropathogen, there are few studies
concerning ESBL-producing E. coli UTI in the setting of ED [9]. Therefore,
we conducted a retrospective matched case-control study to determine
the risk factors of UTIs caused by ESBL-producing E. coli.
2. Material and methods
2.1. Study design
This was a single-center retrospective case-control study to investi-
gate the characteristics and risk factors of patient diagnosed as ESBL-
producing E. coli UTI in the ED from June 2015 to December 2016. This
study was conducted in a university hospital in Korea which is a tertiary
hospital with 56,000 patients according to an annual census of ED visits.

☆ Source of Support: This work was supported by INHA University Hospital Research
2.2. Study protocol and population
Grant.
⁎ Corresponding author at: Department of Emergency Medicine, Inha University
Hospital, 7-206, Shinheung-Dong, Jung-Gu, Incheon 400-711, Republic of Korea. A 1:2 matched case-control study was performed by a blinded ob-
E-mail address: arkim1202@inhauh.com (A. Durey). server who was unaware of the clinical outcomes. The records of all

https://doi.org/10.1016/j.ajem.2018.01.046
0735-6757/© 2018 Elsevier Inc. All rights reserved.

Please cite this article as: Lee H, et al, Risk factors of urinary tract infection caused by extended spectrum β-lactamase-producing Escherichia coli in
emergency department, American Journal of Emergency Medicine (2018), https://doi.org/10.1016/j.ajem.2018.01.046
2 H. Lee et al. / American Journal of Emergency Medicine xxx (2018) xxx–xxx
positive urine cultures (≥105 CFU/mL) collected from UTI patients who
visited ED over the 18 months were reviewed from the computer
database. We randomly enrolled 50 adult patients (age, ≥ 18 years),
who was clinically diagnosed UTI with urine cultures positive for ESBL-
producing E. coli as the case group. Patients with urine culture positive
for non-ESBL-producing E. coli in the same period were chosen as the
control group. Sex and age (±5 years) were matched for each patient.
UTI was defined as 2 or more following symptoms or signs: fever
(≥38 °C), urinary symptoms (dysuria, frequency, urgency, sensing of re-
sidual urine), or tenderness of costovertebral angle on physical exam.
UTI with multiple pathogens was excluded, and each patient was in-
cluded once in the study. In cases in which urine cultures were positive
for E. coli twice or more in this period in the same patients, we selected
the ESBL-producing isolate preferentially, then non-ESBL-producing
one at the time of initial isolation. Concurrent bacteremia was defined
as the presence of the E. coli with the same antibiogram in blood
cultures.
2.3. Variables and definition
The following variables were collected for UTI patients with ESBL
E. coli (case group) and non-ESBL isolates (control group) by reviewing
the medical charts: age, sex, comorbidities, presence of medical device
such as urinary catheter or colostomy, prior hospitalization and number
of outpatient visits within the year before index date, the site of acquisi-
tion, previous UTI episodes, and history of drug exposure. Vital signs and
results of laboratory tests including blood cultures and antimicrobial
susceptibility of E. coli isolates of enrolled patients were also recorded
upon ED arrival. Enrolled patients were followed up until discharge,
and clinical outcome variables such as vasopressor use, ICU admission,
hospital days, transfer or death were also documented.
2.3.1. Sites of acquisition
Each patient was classified as hospital-acquired, healthcare-associ-
ated, or community-acquired. Infections were considered to be hospi-
tal-acquired if (1) the patients were transferred from another hospital
after N48 h hospitalization; (2) the patients were discharged from a hos-
pital within 3 days; (3) the patients had surgery within 30 days.
Healthcare-associated infections were defined in accordance with the
definitions of Friedman et al. [10] (1) patients received intravenous
therapy, wound care, or specialized nursing care at home; (2) patients
attended a hemodialysis clinic in the 30 days before the infection; (3)
patients resided in a nursing home or long-term care facility.
2.3.2. Previous UTI
We defined an episode of previous UTI within the year before the
index date. We used a 30-day time window to distinguish the index
UTI episode from previous episodes, therefore any UTI observed within
30 days before the index UTI were regarded as belonging to the same
episode.
2.3.3. Previous drug exposure
We identified all prescriptions by reviewing medical records from
prior/current hospitalizations and hospital visits for PPI, immunosup-
pressant, chemotherapy, steroid and systemic antibiotics within three
months before the index UTI. We categorized antibiotics as penicillin,
cephalosporin, fluoroquinolone, carbapenem and other.
2.4. Bacteria identification and antimicrobial susceptibility
Fresh urine samples were placed on the eosin methylene blue agar,
and the isolated microorganisms were categorized by Gram staining.
Identification of E. coli was performed using the VITEK 2 system
(bioMérieux, Marcy l'Etoile, France).
Antibiotic susceptibilities were tested by the disk diffusion method
in accordance with the criteria from the Clinical and Laboratory
Please cite this article as: Lee H, et al, Risk factors of urinary tract infection caused by extended spectrum β-lactamase-producing Escherichia coli in
emergency department, American Journal of Emergency Medicine (2018), https://doi.org/10.1016/j.ajem.2018.01.046
Standards Institute. Drug disks tested for the isolated Gram-negative ba-
cilli included ampicillin, amoxacillin-clavulanic acid, piperacillin-tazo-
bactam, aztreonam, cefazolin, cefoxitin, cefotaxime, ceftazidime,
cefepime, gentamicin, amikacin, ciprofloxacin, and trimethoprim-sulfa-
methoxazole. The minimum inhibitory concentration was measured by
the broth microdilution method based on the CLSI recommendation.
2.5. Testing for ESBL phenotype
ESBL confirmatory test involved testing cefotaxime (CTX, 30 μg) and
ceftazidime (CAZ, 30 μg) alone and in combination with clavulanate
(CLA, 10 μg) on Mueller-Hinton agar. If the zone diameter increased
5 mm or more in the presence of CLA, the isolate was considered ESBL-
producing. Escherichia coli ATCC 25922 and Klebsiella pneumoniae ATCC
700603(700,603.18) were used as quality controls.
2.6. Statistical analyses
Patients were divided into two groups: the ESBL-positive E. coli
group and the ESBL-negative group, and characteristics of each group
were compared respectively. Data with a normal distribution were
expressed as mean ± standard deviation and were analyzed by
independent samples t-test. Data with a skewed distribution were
expressed as medians and interquartile ratios and were analyzed by
Mann–Whitney U test. Categorical variables were compared using χ2
test or Fisher exact test depending on the sample size. Univariate anal-
ysis followed by multivariable logistic regression analysis was per-
formed in this case–control study to identify independent risk factors
of UTI caused by ESBL E. coli at ED. Variables with a p value of b0.10 in
the univariate analysis were candidates for multivariate analysis using
a backward elimination method. A p value b .05 was considered statisti-
cally significant. All statistical analyses were performed using Medcalc
for Windows, version 17.6 (MedCalc software, Ostend, Belgium).
3. Results
3.1. Characteristics of the study population
The characteristics of the study population are showed in Table 1.
Fifty had UTI caused by ESBL-producing E. coli (cases) and 100 had
non-ESBL-producing E. coli UTI (controls). Among the case patients, 38
(75%) were women, with a median age of 71 years (range 63–77 years).
Compared to the control group, ESBL E. coli UTI group were more
likely to be bed-ridden status and have urinary catheter in place. They
more frequently had a cerebrovascular disease and previous episodes
of UTI. As for vital signs upon ED arrival, patients with non-ESBL E. coli
were presented with higher body temperature compared to the case
group (38.7 °C ± 1.19 vs. 38.1 °C ± 1.48 respectively; p 0.009) No asso-
ciation was found with respect to laboratory results. Associated bacter-
emia (blood culture with positive isolation of bacteria) was found in
about 40% in both groups.
Regarding clinical outcome, case patients had a higher rate of vaso-
pressor use and ICU care. Case group also had a longer hospital stay of
13.5 days (range 7–21 days) compared to control group (7 days, range
3–12 days) (p = .0001). There was no mortality reported in both
groups.
3.2. Site of acquisition
Site of acquisition of UTI caused by the ESBL-producing E. coli was
categorized to be community-acquired, healthcare-associated and hos-
pital-acquired in 35 (70%), 2 (4%) and 13 (26%) patients, respectively.
Most of the UTIs (91%) caused by non-ESBL E. coli were community-ac-
quired in origin. There was a statistically significant predominance for
hospital-acquired infection in the ESBL group compare to the non-
ESBL group (26% vs. 6% respectively; p b 0.001).
 H. Lee et al. / American Journal of Emergency Medicine xxx (2018) xxx–xxx 3

Table 1
Characteristics of patients with urinary tract infection in the emergency department caused by extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and non-ESBL producing
isolates.

Characteristics ESBL (n = 50) Non-ESBL (n = 100) P value

Bed-ridden, no. (%) 11 (22) 8 (8) 0.016⁎

Medical device, no. (%)
Urinary catheter 4 (8) 1 (1) 0.042⁎
Colostomy 1 (2) 0 (0) 0.33
Comorbid conditions, no. (%)
Diabetes mellitus 19 (38) 32 (32) 0.466
Cardiovascular disease 9 (18) 13 (13) 0.416
Respiratory disease 1 (2) 3 (3) 1.0
Chronic renal failure 2 (4) 7 (7) 0.718
Rheumatologic disease 1 (2) 5 (5) 0.664
Cerebrovascular disease 24 (48) 18 (18) 0.0001⁎⁎⁎
Malignancy 7 (14) 16 (16) 0.749
Prior hospitalization within 3 months, no. (%) 13 (26) 15 (15) 0.104
Outpatient visits within 1 year, no. (%) 4 (0–11) 4 (0–10) 0.655
Prior UTI within 1 year, no. (%) 17 (34) 12 (12) 0.0013⁎⁎
Infection type, no. (%)
Community-acquired 35 (70) 91 (91) 0.001⁎⁎
Healthcare-associated 2 (4) 3 (3) 1.0
Hospital-acquired 13 (26) 6 (6) 0.0005⁎⁎⁎
Vital signs on presentation
SBP, mm Hg 125 (108–144) 130 (119–148) 0.159
DBP, mm Hg 76.7 ± 15.1 78.7 ± 15.0 0.956
PR, beats/min 92 (82–106) 96 (84–107) 0.547
RR, breaths/min 18 (18–20) 18 (18–20) 0.859
Body temperature, °C 38.1 ± 1.48 38.7 ± 1.19 0.009⁎⁎
Saturation, % 95.6 (94.0–97.7) 96.6 (94.7–97.1) 0.590
Laboratory findings on presentation
Leukocyte count, x109cells/mL 11,395 (8170–14,510) 10,260 (7355–13,795) 0.091
Platelet, ×103/μl 217 (159–263) 199 (160–261) 0.500
CRP, mg/dL 8.11 (4.15–14.95) 9.11 (3.52–12.77) 0.908
Serum creatinine, mg/dL 0.94 (0.70–1.29) 0.94 (0.76–1.20) 0.754
Bacteremia 22 (44) 43 (43) 0.907
Antibiotics susceptibility, no. (%)
Ciprofloxacin 16 (32) 74 (74) b0.0001⁎⁎⁎
Amikacin 49 (98) 100 (100) 0.333
Trimethoprim-sulfamethoxazole 22 (44) 73 (73) 0.0005⁎⁎⁎
Use of vasopressor, no. (%) 8 (16) 6 (6) 0.047⁎
ICU care, no. (%) 12 (24) 10 (10) 0.022⁎
Hospital days 13.5 (7–21) 7 (3–12) 0.0001⁎⁎⁎
DNR order, no. (%) 0 2 (2) 0.552
Transfer, no. (%) 5 (10) 3 (3) 0.117
Death, no. (%) 0 2 (2) 0.552
⁎p b .05, ⁎⁎p b .01 ⁎⁎⁎p b .001: significant change from baseline values.
UTI = urinary tract infection; ICU = intensive care unit; DNR = Do not resuscitate.

3.3. Antimicrobial susceptibility 4. Discussion

Only 32% and 44% of ESBL-positive isolates were susceptible to cipro-
floxacin and trimethoprim-sulfamethoxazole, respectively. However,
N70% of ESBL-negative isolates were susceptible to both antibiotics.
98% of the ESBL-positive isolates and 100% of ESBL-negative isolates
were susceptible to amikacin.
Traditionally ESBL-producing organisms are considered to be hospi-
tal-acquired, and our study also identified hospital-acquired infection as
the independent risk factors for ESBL-producing E. coli UTI. The mecha-
nism was suggested that increased ESBL E. coli in gastrointestinal

3.4. Previous antimicrobial use Table 2

Previous drug exposure including antimicrobial agents in study population.

The proportion of patients who had prior antimicrobial exposure was ESBL (n = 50) Non-ESBL (n = 100) P value
significantly higher for the ESBL group compared with the non-ESBL Antimicrobial exposure within 21 (42) 19 (19) 0.002⁎⁎
group (42% vs. 19% respectively; p = .0028). Especially penicillin and 3 months, no. (%)
fluoroquinolone were more frequently used in ESBL group (Table 2). Penicillin 5 (10) 0 0.003⁎⁎
Cephalosporin 6 (12) 10 (10) 0.709
Fluoroquinolone 8 (13) 5 (5) 0.024⁎
3.5. Risk factors for ESBL E. coli UTI Carbapenem 1 (2) 0 0.333
Other 1 (2) 4 (4) 0.665
Results of the multivariate logistic regression analysis are presented Other drug use within 3 months,
no. (%)
in Table 3. Regression analysis showed that underlying cerebrovascular
PPI 4 (8) 8 (8) 1.0
disease (OR = 3.24; 95% CI = 1.45–7.25; p = .004), prior UTI within Immunosuppressant 1 (2) 5 (5) 0.664
1 year (OR = 3.26; 95% CI = 1.32–8.05; p = .010), and hospital-acquired Chemotherapy 0 3 (3) 0.551
infection (OR = 3.86; 95% CI = 1.26–11.8; p = .017) were the indepen- Steroid 3 (6) 5 (5) 1.0
dent risk factors for the acquisition of ESBL-producing E. coli in UTI pa- ⁎p b .05, ⁎⁎p b .01 ⁎⁎⁎p b .001: significant change from baseline values.
tients presenting to ED. UTI = urinary tract infection; PPI = proton pump inhibitor.

Please cite this article as: Lee H, et al, Risk factors of urinary tract infection caused by extended spectrum β-lactamase-producing Escherichia coli in
emergency department, American Journal of Emergency Medicine (2018), https://doi.org/10.1016/j.ajem.2018.01.046
4 H. Lee et al. / American Journal of Emergency Medicine xxx (2018) xxx–xxx
Table 3
Risk factors for extended-spectrum β-lactamase-producing Escherichia coli in patients with urinary tract infection (UTI) presenting to emergency department.
Characteristics Univariate analysis
OR (95% CI)
Bedridden 3.24 (1.21–8.68)
Medical device
Urinary catheter 8.60 (0.93–79.19)
Comorbid conditions,
Cerebrovascular disease 4.20 (1.97–8.93)
Prior UTI within 1 year 3.77 (1.63–8.75)
Antimicrobial exposure within 3monthsa 2.20 (0.96–5.03)
Fluoroquinolone 3.61 (1.11–11.71)
Infection type
Hospital-acquired 5.50 (1.94–15.56)
⁎p b .05, ⁎⁎p b .01 ⁎⁎⁎p b .001: significant change from baseline values.
CI = confidence interval; OR = odds ratio; UTI = urinary tract infection.
a
Not included in the multivariate analyses.
microflora during hospitalization could become pathogens of ascending
UTI [11, 12]. Therefore, ESBL E. coli should be considered as a pathogen
of UTI in ED not only with transferred patients from another hospital
after N48 h hospitalization, but also with the patients who were
discharged within 3 days or who had surgery within 30 days before
UTI. Furthermore, there were reports that ESBL-producer UTIs were
independently associated with nursing home residence or regularly
visiting dialysis centers [13, 14], which indicates healthcare-associated
infection should be taken into account as a risk factor as well even
though only two patients out of 50 ESBL-positive cases had
healthcare-associated infection in our study.
However, the problem of ESBL production is no longer limited to
hospital-acquired or healthcare-associated infections. It has been in-
creasingly identified as causes of community-onset infection, making
it less predictable [2, 6]. Therefore, identifying risk factors for acquiring
ESBL E. coli has become of critical importance in the setting of ED. Our
study revealed that cerebrovascular disease and previous episodes of
UTI within 1 year were risk factors. Bedridden status and indwelling
urinary catheter were more frequently associated with ESBL-positive
isolates, yet did not show statistically significance according to multi-
variate analysis. Additionally, previous studies have identified male
sex, age ≥ 65 years [15], diabetes mellitus [16], previous invasive proce-
dures of the urinary tract [6], and recent international travel history [17]
as risk factors for acquiring ESBL E. coli UTI.
Meanwhile, the association between recent antibiotic use and ESBL
E. coli infections has been well established in previous studies [15, 18].
Antibiotics may alter the normal flora by eliminating susceptible strains
and increasing the colonization of resistant organisms. Previous use of
penicillin and cephalosporin has been well-known to be associated
with ESBL positivity [19, 20]. Quinolone use was also found to be an in-
dependent risk factor in many studies, including one from Norway [21].
Interestingly, ESBL-positive bacteria show high rates of resistance non-
β-lactam antibiotics including quinolones. Ciprofloxacin resistance
was reported to be 31–84% among ESBL-positive E. coli isolates in previ-
ous studies [22]. Our study also showed that 68% and 54% of ESBL E. coli
were resistance to ciprofloxacin and trimethoprim-sulfamethoxazole,
respectively. It may be due to ESBL-encoding plasmids which frequently
bear resistance genes for additional antimicrobial classes, such as sul-
fonamide, aminoglycosides, and fluoroquinolones [23].
Consequently, treatment options for infections are limited in ED, and
initial empirical therapy is often ineffective resulting in prolonged hos-
pitalization [7, 8], rising medical costs, and increased mortality [24, 25].
Carbapenems, are now the recommended agents for cases with serious
ESBL-producing bacterial infection [19, 26], because of its very high rate
of susceptibility. However, these effective antibiotics are usually not
included in first-line empirical antimicrobial agents for ED patients.
Besides, there is concern that the increase in incidence of ESBL
Enterobacteriaceae infections in the community may increase carbapenem
Please cite this article as: Lee H, et al, Risk factors of urinary tract infection caused by extended spectrum β-lactamase-producing Escherichia coli in
emergency department, American Journal of Emergency Medicine (2018), https://doi.org/10.1016/j.ajem.2018.01.046
Multivariate analysis
P value OR (95% CI) P value
0.019
0.057
b0.001⁎⁎⁎ 3.24 (1.45–7.25) 0.004⁎⁎
0.001⁎⁎ 3.26 (1.32–8.05) 0.010⁎
0.060
0.031⁎
0.001⁎⁎ 3.86 (1.263–11.82) 0.017⁎
utilization, which may in turn contribute to the spread of carbapenem-
resistant Enterobacteriaceae (CRE) [27, 28]. Although β-lactam/β
-lactamase inhibitor combinations may be of value in treatment of
ESBL-producing bacteria, the therapeutic outcomes lack adequate
supporting evidence [29]. Notably, 98% of ESBL E. coli was susceptible
to amikacin in our study. Lin et al. also reported that Enterobacteriaceae
were highly susceptible to aminoglycosides [30]. Hence, amikacin could
also be used cautiously as antimicrobial empiric therapy for UTI in ED
with a consideration for kidney function.
There are several limitations to this study. First, this study is a retro-
spective case-control study, which carries the potential for recall bias
and selection bias. Second, some data may have been missing from
the medical records. The study population size could also be considered
a limitation in order to evaluate certain risk factors.
Given that there has been a sustained increase in community-
acquired UTI caused by ESBL E. coli over recent years, emergency physi-
cians should be aware of risk factors and empirical antimicrobial op-
tions for these isolates. The main risk factors identified in our study
(hospital-acquired infection, cerebrovascular disease, and prior UTI
within 1 year) should be considered when treating UTI patients in ED.
Based on our study, amikacin may improve the outcome of empirical
treatment without increasing carbapenem utilization for ESBL E. coli
UTI patients in ED. Considering the variability of distribution of bacterial
isolates and their susceptibility patterns, further study including differ-
ent geographical locations is required.
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