An Overview of Antibacterial Resistance Patterns of Pediatric Community-Acquired Urinary Infections

Abstract

Background:
Urinary tract infections (UTIs) are common infections affecting children. In this study, in order to determine a guide for the empirical antibiotic treatment of community-acquired UTIs, we aimed to investigate the etiology and antimicrobial resistance patterns of uropathogens and to evaluate epidemiological and clinical characteristics of patients.

Methods:
A total of 158 children with a positive urine culture were included in the study. Antibiotic susceptibility testing was performed by Vitek 2 Compact for twenty eight commonly used antimicrobials.

Results:
The mean age was 3.36 ± 3.38 years (45 days to 15 years). Escherichia coli (60.1%), and Klebsiella spp. (16.5%) were the most common uropathogens. For all Gram-negative isolates, a high level of resistance was found against ampicillin/sulbactam (60.1%), trimethoprim/sulfamethoxazole (44.2%), cefazolin (36.2%), cefuroxime sodium (33.5%), and amoxicillin/clavulanate (31.5%). A low level of resistance was found against cefepime (8.7%), ertapenem (4.6%), norfloxacin (1.3%), and meropenem (0.7%). There was no resistance against amikacin.

Conclusions:
The results represent a high antibiotic resistance among the children with UTI. The patterns of antimicrobial resistance of uropathogens vary in their susceptibility to antimicrobials depending on region and time. Thus, the trends of antibiotic susceptibility patterns should be detected periodically to select the appropriate regimen for the treatment of UTIs. This article is protected by copyright. All rights reserved.

Full text

Original Article
Antibacterial resistance patterns of pediatric community-acquired
urinary infection: Overview
Capan Konca,
1,2
Mehmet Tekin,
2
Fatih Uckardes,
3
Sadik Akgun,
4
Habip Almis,
2
Ibrahim Hakan Bucak,
2
Yeliz Genc
2
and
Mehmet Turgut
2
1
Division of Pediatric Intensive Care Unit and Departments of
2
Pediatrics,
3
Statistics and
4
Microbiology, School of
Medicine, Adiyaman University, Adiyaman, Turkey
Abstract Background:Urinary tract infection (UTI) is common in children. The aim of this study was therefor to construct
a guide for the empirical antibiotic treatment of community-acquired UTI by investigating the etiology and antimi-
crobial resistance patterns of uropathogens and analyzing the epidemiological and clinical patient characteristics.
Methods:A total of 158 children with positive urine culture were included in the study. Antibiotic susceptibility
testing was performed with Vitek 2 Compact for 28 commonly used antimicrobials.
Results:Mean age was 3.36 3.38 years (range, 45 days–15 years). Escherichia coli (60.1%), and Klebsiella spp.
(16.5%) were the most common uropathogens. For all Gram-negative isolates, a high level of resistance was found
against ampicillin/sulbactam (60.1%), trimethoprim/sulfamethoxazole (44.2%), cefazolin (36.2%), cefuroxime
sodium (33.5%), and amoxicillin/clavulanate (31.5%). A low level of resistance was noted against cefepime (8.7%),
ertapenem (4.6%), norfloxacin (1.3%), and meropenem (0.7%). There was no resistance against amikacin.
Conclusions:There is high antibiotic resistance in children with UTI. The patterns of uropathogen antimicrobial
resistance vary in susceptibility to antimicrobials depending on region and time. Thus, the trends of antibiotic sus-
ceptibility patterns should be analyzed periodically to select the appropriate regimen for UTI treatment.
Key words antibiotic resistance, child, urinary tract infection, uropathogen.
Urinary tract infection (UTI) is one of the most common
bacterial diseases in children. The prevalence of UTI varies
according to age, gender, and locality. The prevalence of UTI
is 1–3% in girls and 1% in boys.
1
Up to the age of 7, 8% of
girls and 2% of boys will have at least one episode of UTI.
2
The most frequently isolated pathogens in children are Escher-
ichia coli (75–90%), followed by Klebsiella spp., Proteus
spp., Enterococcus spp., and Enterobacter spp.
3–5
Pediatric
UTI are associated with high morbidity and long-term compli-
cations such as renal scarring, hypertension, and chronic renal
failure.
6
Early diagnosis and prompt antimicrobial treatment
are required to minimize these complications.
In patients with suspected UTI, antibiotic treatment is usu-
ally started empirically, before urine culture results are avail-
able. Inappropriate and frequent use of antibiotics may change
the intestinal flora and induce bacterial resistance.
7
Therefore,
knowledge of the pathogen types responsible for UTI and their
resistance patterns to antibiotics is very important in helping
clinicians to choose the right empirical treatment.
8
In this study, in order to determine a guide for the empirical
antibiotic treatment of community-acquired UTI, we
investigated the etiology and antimicrobial resistance patterns of
pathogens associated with community-acquired UTI in children.
Methods
Subjects
The present retrospective study was carried out at the Pediatric
Polyclinics of Adiyaman University Training and Research
Hospital, Adiyaman, Turkey. A total of 158 children with pos-
itive urine culture (age range, 45 days–15 years) were
included in the study. All cases were detected at the Pediatric
Polyclinics of Adiyaman University between August 2013 and
August 2014. Hospitalized or catheterized patients were
excluded. Patient files were retrospectively scanned. Age, gen-
der, date of admission, laboratory findings, radiological
findings, culture, and antibiogram results were recorded.
After standard cleaning, urine samples were obtained from
young patients without urine control via sterile urine bags or
bladder catheterization, and from patients with urine control
from mid-stream urine. Semi-quantitative urine samples were
introduced onto Eosin Methylene Blue (bioM
erieux, Marcy
l’Etoile, France) and 5% sheep blood agar via 4 mm caliber
loops in the laboratory, and were incubated at 37°C for an
average of 18–24 h. Diagnosis of UTI was then based on clin-
ical findings and significant bacteriuria in culture. For this
Correspondence: Capan Konca, MD, Department of Pediatrics,
School of Medicine, Adiyaman University, Adiyaman, Turkey.
Email: dr.capan@hotmail.com
Received 18 August 2015; revised 10 August 2016; accepted
17 August 2016.
©2016 Japan Pediatric Society
Pediatrics International (2016) 0, 1–7 doi: 10.1111/ped.13139

study, significant bacteriuria was defined as culture of single
bacterial species from the urine sample at a concentration of
10
5
c.f.u./mL for a urine specimen collected midstream or via
sterile urine bags, or concentration >10
4
c.f.u./mL in a urine
specimen collected via transurethral bladder catheterization.
9,10
A level <10
5
c.f.u./mL was defined as non-significant bacteri-
uria (negative) for a urine specimen collected mid-stream or
via sterile urine bag. Only a single positive culture per patient
was included in the analysis.
Conventional methods (colony morphology, Gram stain,
indole, methyl red, Voges-Proskauer, and citrate (IMViC)
tests) and Vitek 2 Compact fully automatic identification sys-
tem (bioM
erieux) were used to identify isolates. Antimicrobial
susceptibility testing was performed according to the recom-
mendations of the Clinical and Laboratory Standards Institute
(CLSI) using the automatic identification system against ami-
kacin, amoxicillin/clavulanate, aztreonam, benzylpenicillin,
cefazolin, cefixime, cefoxitin, ceftazidime, ceftriaxone,
cefuroxime sodium, ciprofloxacin, clindamycin, daptomycin,
ertapenem, erythromycin, gentamicin, imipenem, levofloxacin,
linezolid, oxacilin, meropenem, nitrofurantoin, piperacillin,
rifampin, teicoplanin, tetracycline, trimethoprim/sulfamethoxa-
zole, and vancomycin.
Extended spectrum b-lactamase (ESBL) identification was
carried out in two stages. Initially isolates were screened with
the automated identification system (Vitek 2); then ESBL-
positive isolates were confirmed on disk diffusion testing. To
detect ESBL, discs of ceftazidime and ceftriaxone were placed
30 mm from an amoxicillin/clavulanate (20/10 mg) disc. For
disk diffusion testing, >5 mm increase in zone diameter for
either antimicrobial agent in combination with clavulanic acid
versus its zone when tested alone confirmed an ESBL-
producing organism.
11,12
Multidrug resistance (MDR) was defined as resistance to
≥one agent in ≥three categories of antimicrobials.
13
The study was approved by the Adıyaman University
Ethics Committee.
Statistical analysis
Statistical analysis was performed using IBM SPSS statistics ver-
sion 20 for Windows (IBM Corporation, NY, USA). In this study,
patient age was used as continuous data. Normality of continuous
data was assessed with Kolmogorov–Smirnov test. Because the
data were not normally distributed, groups were compared using
Mann–Whitney U-test. Results are reported as mean SD and
median (range). Categorical variables were compared using chi-
squared test and are expressed as counts and percentages.
P<0.05 was considered statistically significant.
Results
Demographic data
A total of 158 children with positive urine culture were
included in the study. Among these, 99 (62.6%) were female
and 59 (37.4%), male. The female/male ratio was 1.68. The
number of girls was significantly higher than that of boys
(P<0.001). Mean age was 3.36 3.38 years and the age
range was from 45 days to 15 years. The mean age of girls
was 3.54 3.40 years and that of boys, 3.08 3.34 years.
The difference was not statistically significant (P=0.317).
The median age of girls was 2 years (range, 2 months–
14 years) and the median age of boys was 1.2 years (range,
45 days–15 years).
A total of 32.9% of subjects (n=52) were <12 months
old, 28.5% (n=45) aged 1–3 years, and 38.6% (n=61) aged
>3 years. A total of 45.7% (n=27) of boys were <12 months,
35.6% (n=21) aged 1–3 years, and 18.7% (n=11) aged
>3 years. In all, 25.3% (n=25) of girls were aged
<12 months, 24.2% (n=24) aged 1–3 years, and 50.5%
(n=50) aged >3 years (Fig. 1).
Urinary tract infection was most often seen in summer
(34.2%, n=54) and winter (31.6%, n=50), and less often in
spring (17.1%, n=27) and autumn (17.1%, n=27). There
was no significant difference according to season (P=0.177).
Isolated pathogens
Gram-negative bacteria constituted the largest group, with a
prevalence of 94.3% (149/158). E. coli (60.1%) was the com-
monest uropathogen, which was isolated in all age groups, fol-
lowed by Klebsiella species (16.5%) and Proteus mirabilis
(14.6%). Only 5.7% of the isolates were Gram positive: Sta-
phylococcus aureus (3.2%), Enterococcus faecalis (1.9%), and
Streptococcus agalactiae (0.6%; Table 1). The prevalence of
E. coli was 47.5% (n=28) in the boys and 67.7% (n=67) in
Fig. 1 Age distribution in (■) boys and (□) girls.
©2016 Japan Pediatric Society
2 C Konca et al.

the girls. The prevalence of Klebsiella spp.was 17.2%
(n=17) in the girls and 15.2% (n=9) in the boys. The
prevalence of P. mirabilis was 20.3% (n=12) in the boys
and 11.1% (n=11) in the girls. Female/male ratio was signifi-
cantly higher for E. coli and Klebsiella spp. (P<0.001).
E. coli infection was seen most often in summer (34.7%,
n=33) and least often in spring (16.8%, n=16). Similarly,
Klebsiella spp. infection was most often seen in summer
(34.6%, n=9) and less often in spring (11.5%, n=3). In
contrast, P. mirabilis infection was most often seen in winter
(47.8%, n=11). The most frequently isolated pathogen in all
age groups and seasons was E. coli. Additionally, E. coli
(32.63%), Klebsiella spp. (30.43%) and P. mirabilis (42.31%)
were the most commonly isolated pathogens in recurrent UTI.
Distribution of the uropathogens for the most common isolated
species is given in Table 2 according to season, age group,
and gender.
Antibiotic susceptibility
The antibiotic susceptibility patterns of the three Gram-nega-
tive bacilli that comprised 91.1% of the uropathogens are sum-
marized in Table 3. E. coli isolates were most susceptible to
amikacin (100%), meropenem (100%), imipenem (97.9%), and
nitrofurantoin (96.7%), followed by gentamicin (95.8%).
E. coli isolates had the highest resistance rate to ampicillin/
sulbactam (56.4%), cefazolin (44.4%), trimethoprim/sul-
famethoxazole (43.2%), cefixime (36.8%), and amoxicillin/
clavulanate (32.6%), respectively. The Klebsiella isolates had
a high susceptibility to imipenem (100%), amikacin (100%),
imipenem (100%), cefoxitin (90.5%), and nitrofurantoin
(90%). Klebsiella spp. had the highest resistance to ampicillin/
sulbactam (78.3%), cefazolin (66.7%), cefixime (53.8%),
cefuroxime sodium (47.6%), ceftriaxone (38.4%), and
trimethoprim/sulfamethoxazole (42.9%). Proteus spp. had the
highest sensitivity to amikacin (100%), cefepime (100%), mer-
openem (96.2%), and ceftazidime (96.2). Proteus spp. had the
highest resistance rate to nitrofurantoin (88%), trimethoprim/
sulfamethoxazole (65.4%), and ampicillin/sulbactam (42.3%).
Table 1 Uropathogen distribution
Uropathogens n%
Gram ()
Escherichia coli 95 60.1
Klebsiella spp. 26 16.5
Proteus mirabilis 23 14.6
Morganella morganii 4 2.5
Enterobacter cloacae 1 0.6
Gram (+)
S. aureus 5 3.2
Enterococcus faecalis 3 1.9
Streptococcus agalactiae 1 0.6
Table 2 Uropathogen distribution vs season, age group and gender
Parameters E. coli
n(%)
Klebsiella spp.
n(%)
Proteus spp.
n(%)
Others
n(%)
P-value
†
Age group
<1 year 27 (51.9) 19 (36.5) 5 (9.6) 1 (1.9) <0.001
1–3 years 24 (53.3) 3 (6.6) 14 (31.1) 4 (8.8) <0.001
>3 years 44 (72.2) 4 (6.5) 4 (6.5) 9 (14.8) <0.001
F/M ratio 2.39* 1.88* 0.86 0.55 0.819
Predisposing disease (%) 12.63 26.09 19.23 14.2 0.112
Recurrent UTI (%) 32.63 30.43 42.31 35.7 0.328
Seasons
Spring 16 (59.2) 3 (11.1) 2 (7.4) 6 (22.2) <0.001
Summer 33 (61.1) 9 (16.7) 7 (12.9) 5 (9.3) <0.001
Autumn 17 (62.9) 6 (22.2) 3 (11.1) 1 (3.7) <0.001
Winter 29 (58.0) 8 (16.0) 11 (22.0) 2 (4) <0.001
*P<0.05.
†
Chi-squared test. UTI, urinary tract infection.
Table 3 Uropathogen antibiotic resistance pattern
Antibiotics E. coli
(%)
Klebsiella
spp. (%)
Proteus
spp. (%)
All
Gram-negative
isolates (%)
Amikacin 0 0 0 0
TMP-SMX 43.2 30.4 65.4 44.2
Aztreonam 27.4 42.9 18.2 24.8
Cefazolin 44.4 66.7 22.2 36.2
Cefixime 36.8 53.8 11.1 20.8
Cefoxitin 6.6 9.5 4.5 10.6
Ceftazidime 22.1 36.4 3.8 20.8
Ceftriaxone 33.6 38.4 34.7 33.5
Cefuroxime
sodium
32.3 47.6 16 33.5
Ciprofloxacin 6.3 13.6 7.7 7.3
Ertapenem 5.4 0 4 4.6
Gentamicin 4.2 13 19.2 9.4
Imipenem 2.1 0 15.3 4.1
Meropenem 0 0 3.8 0.7
Nitrofurantoin 3.3 10 88 21.5
Piperacillin 18.5 26.1 3.8 16.1
Amoxicillin/
clavulanate
32.6 28.6 16.7 31.5
Ampicillin/
sulbactam
56.4 78.3 42.3 60.1
Norfloxacin 5.9 0 83.3 1.3
Cefepime 24.4 30 0 8.7
TMP-SMX, trimethoprim-sulfamethoxazole.
©2016 Japan Pediatric Society
UTI antibiotic resistance patterns 3

For all Gram-negative isolates, a high level of resistance
was noted against ampicillin/sulbactam (90/60.1%), trimetho-
prim/sulfamethoxazole (66/44.2%), cefazolin (54/36.2%),
cefuroxime sodium (50/33.5%), and amoxicillin/clavulanate
(47/31.5%). A low level of resistance was noted against cefe-
pime (13/8.7%), ertapenem (7/4.6%), norfloxacin (2/1.3%),
and meropenem (1/0.7%). There was no resistance to
amikacin.
ESBL producers
In all, 44 of the 149 Gram-negative isolates (29.5%) were pre-
sumptive ESBL producers. A total of 30.5% of E. coli, 34.6%
of Klebsiella spp. and 26.1% of P. mirabilis isolates were
ESBL producers. Risk factors for community-onset ESBL-pro-
ducing E. coli or MDR pathogens were previous renal scarring
(n=14, 31,8%), dilation of the pelvicalyceal system (n=10,
22.9%), vesicoureteral reflux (n=10, 22.9%), hydronephrosis
(n=5, 11.4%), kidney stones (n=4, 9.1%), and ureteropelvic
junction obstruction (n=1, 2.3%), respectively.
Discussion
The pattern of antimicrobial resistance of the microorganisms
causing UTI infection varies in susceptibility to antimicrobials
depending on region and time. Therefore, it is important to
know the status of antimicrobial resistance among uropatho-
gens to improve treatment recommendations. We conducted
this study to clarify the frequency and antimicrobial suscepti-
bility patterns of community-acquired uropathogens, and to
establish a guide for the empirical antibiotic treatment of com-
munity-acquired UTI.
Recent studies on antibiotic resistance in childhood UTI in
Turkey show that antibacterial resistance patterns have chan-
ged over time (Table 4). Amikacin, meropenem and imipenem
maintained their very high efficacy against urinary pathogens
in Turkey. Co-trimoxazole resistance rates have been gradu-
ally decreasing over time, but initial empirical treatment with
co-trimoxazole is no longer appropriate in this region. Ceftri-
axone resistance rates have been increasing. We concluded
that the appropriate choice of antibiotics, and prevention of
misuse or excessive use of antibiotics, will help to decrease
antibiotic resistance rates.
The frequency of UTI in children varies according to age
and sex. Although the incidence of UTI in male infants is
highest in the first 3 years of life, it significantly decreases
with age. The incidence of completely retractable prepuce
gradually increases from 0% at age 6 months to 62.9% by 11–
15 years of age, while that of a tight ring decreases with age
from 84.3% to 8.6%.
19
Phimosis is the inability to retract the
prepuce over the glans penis and could be defined as physio-
logical, as in infancy and childhood, or pathological. Tokg€
oz
et al. investigated the preputial flora in 32 boys, and noted
significant uropathogenic bacterial colonization in 100% of the
boys with phimosis, and in 48.1% of those without phimosis.
20
Therefore a high incidence of UTI in young boys may be
attributed to the presence of prepuce.
21
The incidence of UTI
is similar at all ages for girls.
21
It has been frequently reported
that UTI most commonly occurs in female subjects, and that
up to one-third of all women have a UTI at some point during
their lifetime.
21–24
This may be attributed to the high risk of
infection in female subjects due to the short urethra and its
proximity to the anal opening.
In the present study, consistent with previous studies, the
majority of patients (62.6%) were female and the incidence of
UTI in male infants was highest in the first 3 years of life.
Although the type of UTI pathogen may vary according to
gender and age, Gram-negative organisms are the most com-
monly isolated. For appropriate treatment, it is important to
identify the causal pathogens. The main etiological agents of
UTI have changed little during the last few decades:
9
E. coli
is still the principal etiological agent of UTI, accounting for
70–90% of infection.
25
Yolbaset al. reported that E. coli
(75.3%), Klebsiella spp. (20.7%), Proteus spp. (2.7%), and
Pseudomonas spp. (1.3%) were isolated from most of the sam-
ples.
21
Another study reported that E. coli (45.12%), followed
by Klebsiella spp. (18.71%), and Enterococcus spp. (9.23%)
were the causal pathogens.
26
The present findings are similar
to these previous studies.
High resistance to commonly used antimicrobial agents
was observed in the present study, but all of the Gram-nega-
tive isolates were mostly susceptible to amikacin, meropenem,
imipenem, nitrofurantoin, and gentamicin. The present results
were compared according to region in Turkey and with other
countries to obtain a more accurate view of antibiotic resis-
tance rates. The rates of antibiotic resistance were mostly
lower than those in developing countries, but higher than in
developed countries (Table 5). We considered that in the
underdeveloped and developing countries, due to inappropriate
use of antibiotics, antibiotic resistance is high.
In a recent study, ESBL positivity was 6% in E. coli and
Klebsiella spp.
26
Akram et al. reported that 42% of isolates
produced ESBL. Among the five most frequent UTI patho-
gens, E. coli (34.42%) and Klebsiella pneumoniae (27.3%)
were the most prevalent ESBL producers.
27
In another study,
29.1% of E. coli, 25.6% of Klebsiella spp. and 28.6% of
Enterobacter spp. were ESBL producers.
28
In the present
study, similar to these studies, 29.5% of all Gram-negative
isolates were ESBL producers; the proportion of ESBL-produ-
cing Klebsiella spp., however, was higher than in other studies
(34.6%).
The present study had some limitations. First, we were
unable to obtain data for a large number of countries. Another
limitation was the low number of patients and the heterogene-
ity of the subject group.
Although the most common oral antibiotics prescribed in
Turkey for UTI are ampicillin/sulbactam, amoxicillin/clavu-
lanate, first-generation cephalosporins and co-trimoxazole, the
most common parenteral treatment is aminoglycosides and
third-generation cephalosporins. For secondary prophylaxis
cephixim, co-trimoxazole and nitrofurantoin are commonly
prescribed. Prais et al. reported that empirical treatment with
©2016 Japan Pediatric Society
4 C Konca et al.

co-trimoxazole or cephalexin as the initial drug is inadequate
in approximately one-third of UTI cases, but that nitrofuran-
toin and nalidixic acid maintained their very high efficacy
against urinary pathogens in Israel.
24
Ghadage et al. reported
that resistance to ampicillin and co-trimoxazole, commonly
used for empirical therapy, has increased in India.
26
Also,
Kothari and Sagar reported extremely low susceptibility to the
first-line agents (amoxicillin, amoxicillin/clavulanate, cipro-
floxacin, co-trimoxazole) in uropathogens.
32
Initial empirical
treatment with trimethoprim-sulfamethoxazole is now no
longer appropriate in Tehran, but fluoroquinolones and nitrofu-
rantoin should be seriously reconsidered in Tehran.
29
The
Table 4 Antibiotic resistance patterns of E. coli strains isolated on urine culture in Turkey
Antibiotics Previous studies Present study
2002
14
2006
15
2008
16
2010
17
2012
18
Amikacin 9 11.5 3.8 0 3.2 0
Co-trimoxazole 61 82.2 43.6 52.7 54.8 43.2
Aztreonam 25 – – – – 27.4
Cefazolin – – 48.1 – – 44.4
Cefixime – – – – – 36.8
Cefoxitin 0 – – – – 6.6
Ceftazidime 8.2 – – – – 22.1
Ceftriaxone 21.7 6.8 12.8 6 20 33.6
Cefuroxime sodium 28 21.9 30.8 – – 32.3
Ciprofloxacin 10.2 – – 12 –6.3
Ertapenem – – – – – 5.4
Gentamicin –6.6 12 5.4 –4.2
Imipenem 1.2 –0.8 – – 2.1
Meropenem 1 – – – – 0
Nitrofurantoin – – 6.8 – – 3.3
Piperacillin 17.5 –44.4 – – 18.5
Amoxicillin/clavulanate 28 –28.6 23.4 43.5 32.6
Ampicillin/sulbactam 75 63.2 –37.1 69.3 56.4
Norfloxacin – – – – – 5.9
Cefepime 10.7 – – – – 24.4
Table 5 Comparison of antibiotic resistance rates
Antibiotics Escherichia coli Klebsiella spp.
India
27
Italy
28
Turkey
21
Iran
29
Brazil
30
England
31
Present
study
India
27
Turkey
21
Israel
24
Iran
29
Present
study
Amikacin 51 –3–0–0 35 0 – – 0
Co-trimoxazole 76 15 58 61.8 51 53.7 43.2 53 61 22 53.1 30.4
Aztreonam 75 –44 – – – 27.4 59 48 – – 42.9
Cefazolin – – 54 –10 –44.4 –71 – – 66.7
Cefixime – – – – – – 36.8 – – – – 53.8
Cefoxitin 69 –10 –5–6.6 53 27 – – 9.5
Ceftazidime 65 <1 37 31.8 5 –22.1 53 52 –17.4 36.4
Ceftriaxone 55 <1 46 36.5 5 –33.6 47 68 –52.7 38.4
Cefuroxime
sodium
– – 51 –10 –32.3 –74 – – 47.6
Ciprofloxacin 69 –21 31.9 4 5.9 6.3 47 11 –18.7 13.6
Ertapenem – – 7– – – 5.4 –14 – – 0
Gentamicin 64 <1 34 50.7 –3.6 4.2 53 48 –46.9 13
Imipenem 0 –0– – – 2.1 12 0 – – 0
Meropenem – – 0– – – 0–0– – 0
Nitrofurantoin 80 <1 9 28.7 6 3.8 3.3 76 37 27 72.8 10
Piperacillin 84 –83 – – – 18.5 82 55 – – 26.1
Amoxicillin/
clavulanate
–10 50 97.4 –12.9 32.6 –57 22 88.5 28.6
Ampicillin/
sulbactam
–52 65 96.4 55 62.3 56.4 –79 93 100 78.3
Norfloxacin 69 –17 38 – – 5.9 47 16 –8.3 0
Cefepime 67 –44 –5–24.4 53 52 – – 30
©2016 Japan Pediatric Society
UTI antibiotic resistance patterns 5

present study noted low susceptibility to the most common
oral antibiotics, but cefepime, cefoxitin and nitrofurantoin
maintained their very high efficacy against urinary pathogens.
In conclusion, uropathogens had low susceptibility to ampi-
cillin/sulbactam, trimethoprim/sulfamethoxazole, amoxicillin/
clavulanate, cefuroxime sodium, cefazolin, and ceftriaxone in
the present patients. Conversely, there was a high susceptibil-
ity to amikacin, fluoroquinolones, carbapenems, cefepime,
gentamicin, and cefoxitin. The present results may be of sig-
nificant value to determine trends in antimicrobial sensitivities,
to assist physicians in the appropriate choice of antibiotics,
and to prevent the misuse or excessive use of antibiotics.
There was also a significant increase in ESBL-producing Kleb-
siella spp., indicating that there may be difficulties in the near
future in the treatment of UTI caused by Klebsiella spp.
Disclosure
The authors declare no conflicts of interest.
Author contributions
C.K. designed the study and wrote the manuscript; H.A.,
_
I.H.B. and Y.G. collected and analyzed data; M.T., M.T., S.A.
and F.U. gave technical support and conceptual advice. M.T.
contributed to the conception and design of this study; F.U.
performed the statistical analysis; M.T. and C.K. critically
reviewed the manuscript and supervised the whole study pro-
cess. All authors read and approved the final manuscript.
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