Original Article | J Adv Med Biomed Res. 2023; 31(148): 464-471
Journal of Advances in Medical and Biomedical Research | ISSN:2676-6264
Bacterial Urinary Tract Infections in North West of Iran: A Cross- Sectional
Study
Erfan Fakheri1
1.
2.
3.
4.
, Niloufar Kazemi1
, Narges Moradi1,2
, Bahman Mirzaei3,4*
Student Research Committee, Zanjan University of Medical Sciences, Zanjan, Iran
Dept. of Life Technologies, University of Turku, Turku, Finland
Dept. of Bacteriology, Pasteur Institute of Iran, Tehran, Iran
Dept. of Medical Microbiology and Virology, School of Medicine, Zanjan University of Medical Sciences, Zanjan,
Iran
Article Info
ABSTRACT
10.30699/jambs.31.148.464
Received: 2022/08/09;
Accepted: 2022/00/20;
Published Online: 29 Oct 2023;
Use your device to scan and read the
article online
Corresponding Information:
Bahman Mirzaei,
Dept. of Bacteriology, Pasteur Institute
of Iran, Tehran, Iran
E-Mail: dr.bahman.m@gmail.com
Background & Objective: Bacteria play a major role in urinary tract infections
(UTIs); therefore, it is necessary to be aware of their regional prevalence and the
causative pathogens for better prognosis and rapid treatment in clinical settings.
This study aims to evaluate the prevalence of bacterial isolates involved in UTI
samples and their antibiotics resistance pattern.
Materials & Methods: In this cross-sectional study, bacterial infections from 4214
urine samples were analyzed from December 2016 to December 2018. After
biochemical tests, disk diffusion susceptibility procedures were performed on all
positive clinical cultures, according to CLSI guidelines. The obtained data were sorted
and statistically analyzed by SPSS 26.
Results: Out of 3582 suspected UTIs samples, 2006 (56%) were females and 1576
(44%) males in the 0-99 years old age range and mainly consisting of middle-aged and
elderly patients (62.2%). Escherichia coli (53.43%) and Staphylococcus epidermidis
(15.99%) were the most frequent isolates. Among gram negative bacteria,
nitrofurantoin and among gram- positive, vancomycin represented the lowest
resistance rates at 25.27% and 26.74% respectively. Piperacillin showed the least
efficacy with a resistance rate of 76.04%, followed by cefazolin with a 74.94%
resistance rate. In gram positive bacteria, vancomycin and gentamicin showed more
promise with respective resistance rates of 19.34% and 27.34%. The highest resistance
was associated with ampicillin (68.61%) and Trimethoprim/Sulfamethoxazole
(66.06%).
Conclusion: Alarming resistance rates were observed in ampicillin and
piperacillin, which should be taken into account in therapy guidelines in this area.
Prevalence of resistant strains can be avoided by developing appropriate healthcare
policies and community awareness.
Keywords: Antimicrobial Resistance, Bacteria, Hospital-acquired Infection,
Urinary Tract Infection
Copyright © 2023, This is an original open-access article distributed under the terms of the Creative Commons Attribution-noncommercial 4.0 International License which permits
copy and redistribution of the material just in noncommercial usages with proper citation.
Introduction
Nosocomial infections or healthcare-associated
infections (HAIs) are infections that hospitalized patients
acquire throughout their period of stay. Symptoms of the
disease may appear during the hospitalization or after
discharge from the hospital (1). Infections that appear
after 48 to 72 hours are usually classified as nosocomial,
and if the infection occurs less than 48 hours of
hospitalization, it is likely that the patient might have
obtained the infection during the administration process
and may have been in the common phase of the disease
(2). A recent meta-analysis conducted by Mohammadi et
al., from 2001 to 2017, reported a 4.6% overall prevalence
rate of HIAs in Iranian hospitals (3). A 2014 CDC report
including 183 US hospitals and 11,282 hospitalized
Volume 31, September & October 2023
patients indicated that 4% of the patients suffered from
one or more HAIs (4). This results in a rise in costs, length
of recovery, disabilities and even death amongst patients
and attaches great importance to development of
regionally studied and validated diagnostic and
therapeutic guidelines for these infections.
Bacteria are microorganisms that are found in various
environments, especially in clinical settings. The ability of
bacteria to cause hospital outbreaks and epidemics is
indicative of the importance of these microorganisms.
Bacteria are mainly labeled as opportunistic pathogens
and can create various acquired infections in clinical
settings including bacteremia, meningitis, surgical wound
infections, urinary tract infections (UTIs), hospitalJournal of Advances in Medical and Biomedical Research
Erfan Fakheri et al. 465
acquired pneumonia, etc. (5). UTIs are bacterial infections
that affect various parts of the urinary tract. Physiologic
and anatomic differences have made UTIs more prevalent
among women than men; however, the prevalence rate is
similar in elderly males and females (6). Infections of the
lower urinary tract and the upper urinary tract are referred
to as cystitis (bladder infection) and pyelonephritis
(kidney infection), respectively (7). Symptoms of the
lower urinary tract infections include frequent urination
accompanied by pain (dysuria), while symptoms of
pyelonephritis include fever, shivering and flank pain in
addition to the symptoms of lower urinary tract infections
(8). The main cause of both types of infections is
uropathogenic Escherichia coli, a gram negative rodshaped bacterium from the Enterobacteriaceae family (9).
The increasing antibiotic resistance and the emergence of
multidrug-resistant (MDR) and extensively-drug resistant
(XDR) E. coli strains have led to a global health crisis. In
most of the infections, the hospital environment is the
source and reservoir and, in several studies, it has been
observed that environmental pollution has been the source
of sudden epidemics caused by bacterial infections (1).
Bacteria play an important role in UTIs; therefore, it is
necessary to be aware of their prevalence and the
causative pathogens for better prognosis, rapid treatment
and elimination of the infectious agents in clinical
settings. This study aims to evaluate the prevalence of
bacterial isolates involved in UTI samples and their
antibiotics resistance pattern.
Materials and Methods
Sample Collection and Culture
A cross-sectional study was designed to analyze
bacterial infections in a total number of 3582 urine
samples collected from ambulatory and hospitalized
patients in Valie-Asr hospital in Zanjan, Iran, from
December 2016 to December 2018. Samples were
initially cultured on MacConkey agar and blood agar
(Lioflchem, Italy), according to standard bacteriological
protocols and incubated at 37°C for 24 hours (10).
Identification of Bacterial Isolates
Bergeys̓ microbiology book guidelines were applied for
isolate identification (10). Gram staining and
conventional media and biochemical tests including
catalase, oxidase, Sulfide Indole Motility (SIM), Triple
Sugar Iron Agar (TSI), Methyl Red (MR)/VogesProskauer (VP), citrate, sensitivity to specific antibiotic
disks, Mannitol Salt Agar, urease, Dnase, etc. (Merck,
Germany) were used to confirm the growth of the
bacteria.
Antibiotic Susceptibility Testing
Disk diffusion susceptibility tests were performed on all
positive clinical cultures, according to Clinical Laboratory
Standard Institute (CLSI) guidelines (11) using the disks
(BD BBLTM Sensi DiscTM) containing amikacin (AN)
(30 μg), ceftazidime (CAZ) (30 μg), cephalexin (30 μg),
levofloxacin (LEV) (5 μg), piperacillin-tazobactam (PI
Volume 31, September & October 2023
10 μg) ciprofloxacin (CP) (5 μg), imipenem (IMP) (10
μg), meropenem (MEN) (10 μg), gentamycin (GM) (10
μg), ampicillin (10 µg), ceftriaxone (CRO) (30 µg),
cefotaxime
(CTX)
(30
µg),
trimethoprim/sulfamethoxazole (SXT) (25 [1.25/23.75]
µg), cefazolin (CZ), cefepime (FEP) (30 μg),
nitrofurantoin (FM) (300 µg), oxacillin (CX) (30 μg), and
vancomycin (30 µg) (only for gram positive bacteria)
(11). American Type Culture Collection (ATCC)
standard reference strains (Escherichia coli ATCC 25922
and Staphylococcus aureus ATCC 29213) were used as
controls.
Statistical Analysis
The obtained data were sorted and statistically analyzed
in SPSS 26 (SPSS Inc., Chicago, IL, USA). Pearson’s chisquare test was used for variable comparison in
independent groups and P-values less than 0.05 were
considered significant.
Ethics approval and consent to participate
This study complies with ethical principles and the
standards for conducting clinical research and is approved
by The Ethics Committee of Zanjan University of
Medical Sciences (IR.ZUMS.REC.1398.370).In the
current study, all ethical guidelines including Ethics and
Consent to participate from the parents have been
collected.
Results
From December 2016 to December 2018, a total
number of 6299 urinary, respiratory tract, blood, and
stool culture tests were performed for the patients who
referred to Valie-Asr Hospital Laboratory in Zanjan,
Iran, including 3168 (50.3%) males and 3131 (49.7%)
females. Urine culture was the most frequently requested
culture (n=3582, 56.87%), followed by sputum (n=1058,
16.8%), blood (n=854, 13.4%) and stool (n=182, 2.9%)
cultures. In this study, we analyzed microbial cultures of
patients with bacterial infections of the urinary tract and
the associated antimicrobial resistance patterns. The
study population consisted of a total number of 3582
patients with positive urine cultures (85%), including
2006 (56%) females and 1576 (44%) males in the 0-99
age range. The study population mainly consisted of
middle-aged and elderly patients (n=2228, 62.2%),
followed by young adults (n=1021, 28.5%). Positive
urine cultures were the least frequent among adolescents
and children (n=333, 9.3%). The average age of the
study population was 63.4 years. With 1275 positive
bacterial growth results, the emergency ward had the
highest positive culture ratio (35.6%), followed by the
following wards: internal (17.8%, n=638), neurosurgery
(16.9%, n=605), intensive care unit (11.8%, n=423),
infectious diseases (10.4%, n=373), cardiology (3.7%,
n=133), surgery (1.6%, n=57), coronary care unit (0.9%,
n=32) oncology (0.7%, n=25), and ophthalmology
(0.6%, n=21).
Journal of Advances in Medical and Biomedical Research
466 Bacterial Uropathogens
According to urine cultures results, E. coli and
Staphylococcus epidermidis were the most frequently
isolated gram negative and gram-positive bacteria from
the urine samples with isolation rates of 53.43% and
15.99%, respectively. Table 1 reveals information on the
prevalence of the isolated bacteria.
Table 1. Prevalence of isolated bacteria from the urine samples of a total number of 3582 patients with positive urine
cultures.
Isolation frequency (N=3582)
Gram Negative
Gram Positive
Escherichia coli
53.43% (n=1914)
Serratia marcescens
5.38% (n=193)
Pseudomonas aeruginosa
4.52% (n=162)
Klebsiella pneumoniae
4.15% (n=149)
Acinetobacter baumanni
0.3% (n=11)
Citrobacter freundii
0.16% (n=6)
Morganella morganii
0.11% (n=4)
Proteus mirabilis
0.08% (n=3)
Staphylococcus epidermidis
15.99% (n=537)
Group D Streptococci
7.7% (n=279)
Staphylococcus saprophyticus
6.19% (n=222)
Lactobacillus acidophilus
1.2% (n=44)
Viridans streptococci
1% (n=36)
Staphylococcus aureus
0.6% (n=22)
Among gram negative bacteria, nitrofurantoin and
vancomycin represented the lowest resistance rates at
25.27% and 26.74% respectively. Piperacillin showed
the least efficacy with a resistance rate of 76.04%,
followed by cefazolin which had a resistance rate of
74.94%. Antibiotic susceptibility results of the isolated
gram-negative bacteria are demonstrated in Table 2.
Table 2. Antibiotic susceptibility pattern of the gram-negative bacteria isolated from 2442 urine samples of the clinical
origin and the associated resistance rates.
Amikacin
Gentamycin
Imipenem
E.
coli
S.
marce
scens
P.
aerug
inosa
K.
pneu
monia
A.
bum
annii
C.
freu
ndii
M.
morg
anii
P.
mirab
ilis
Total
(N)
Number
(n)
1914
193
162
149
11
6
4
3
2442
Sensitive
1178
19
47
63
2
4
3
2
1318
Intermedia
te
353
3
2
24
2
1
1
1
387
Resistant
383
171
113
62
7
1
0
0
737
Sensitive
1187
15
50
49
6
3
0
3
1313
Intermedia
te
76
3
3
2
1
1
1
0
87
Resistant
651
175
109
98
4
2
3
0
1042
Sensitive
1417
19
36
83
2
0
4
2
1563
Intermedia
te
95
17
2
14
1
2
0
0
131
Resistant
402
157
124
52
8
4
0
1
748
Sensitive
1531
10
130
18
1
1
2
0
1693
Volume 31, September & October 2023
Resistan
ce Rate
(%)
30.18
42.67
30.63
25.27
Journal of Advances in Medical and Biomedical Research
Erfan Fakheri et al. 467
Nitrofurantoi
n
Trimethopri
m/Sulfameth
oxazole
Ciprofloxacin
Cefepime
Ceftriaxone
Piperacillin
Cefazolin
Ceftazidime
Levofloxacin
Ampicillin
Cefoxitin
E.
coli
S.
marce
scens
P.
aerug
inosa
K.
pneu
monia
A.
bum
annii
C.
freu
ndii
M.
morg
anii
P.
mirab
ilis
Total
(N)
Intermedia
te
115
2
3
12
0
0
0
0
132
Resistant
268
181
29
119
10
5
2
3
617
Sensitive
670
11
4
31
0
2
2
2
722
Intermedia
te
57
2
1
1
0
0
0
0
61
Resistant
1187
180
157
117
11
4
2
1
1659
Sensitive
804
19
36
32
0
4
4
3
902
Intermedia
te
4
2
5
1
0
0
0
0
12
Resistant
1106
172
121
116
11
2
0
0
1528
Sensitive
957
10
47
47
5
4
2
1
1073
Intermedia
te
57
2
7
11
0
0
2
1
80
Resistant
900
181
108
91
6
2
0
1
1289
Sensitive
756
10
17
38
1
2
2
2
828
Intermedia
te
17
2
11
3
3
0
0
0
36
Resistant
1141
181
134
108
7
4
2
1
1578
Sensitive
459
10
37
21
1
0
2
3
533
Intermedia
te
38
2
4
3
2
2
1
0
52
Resistant
1417
181
121
125
8
4
1
0
1857
Sensitive
511
4
14
19
0
2
1
2
553
Intermedia
te
54
1
0
2
0
1
0
1
59
Resistant
1349
188
148
128
11
3
3
0
1830
Sensitive
924
7
47
50
2
3
0
2
1035
Intermedia
te
118
3
11
12
0
1
0
0
145
Resistant
872
183
104
87
9
2
4
1
1262
Sensitive
840
14
39
61
2
2
4
2
964
Intermedi
ate
54
3
3
3
2
0
0
1
66
Resistant
1020
176
120
85
7
4
0
0
1412
Sensitive
717
19
41
47
6
2
2
3
837
Intermedi
ate
239
7
1
43
1
1
0
0
292
Resistant
958
167
120
59
4
3
2
0
1313
Sensitive
1311
8
21
89
5
5
2
2
1443
Intermedi
ate
19
3
5
2
1
1
1
0
32
Resistant
584
182
136
58
5
0
1
1
967
Volume 31, September & October 2023
Resistan
ce Rate
(%)
67.94
62.57
52.78
64.62
76.04
74.94
51.68
57.82
53.77
39.60
Journal of Advances in Medical and Biomedical Research
468 Bacterial Uropathogens
Among gram positive bacteria, vancomycin and
gentamicin showed more promise with respective
resistance rates of 19.34% and 27.34%. The highest
resistance was associated with ampicillin (68.61%) and
Trimethoprim/Sulfamethoxazole (66.06%). Antibiotic
susceptibility results of the isolated gram-positive
bacteria are demonstrated in Table 3.
Table 3. Antibiotic susceptibility pattern of the gram-positive bacteria isolated from 1096 urine samples of the clinical
origin and the associated resistance rates.
Amikacin
Gentamicin
Imipenem
Nitrofurant
oin
Trimethopr
im/
Sulfametho
xazole
Ciprofloxac
in
Piperacillin
Cefepime
Vancomyci
n
Cefazolin
S.
epidemidi
s
Group D
Streptococci
S.
saprohyti
cus
Viridans
streptococc
i
S.
aureus
Total
(N)
Number (n)
537
279
222
36
22
1096
Susceptible
326
93
57
5
8
489
Intermediate
74
10
7
1
0
92
Resistant
137
176
158
30
14
515
Susceptible
397
104
145
30
19
695
Intermediate
23
57
13
2
1
96
Resistant
117
118
64
4
2
305
Susceptible
254
80
109
24
12
479
Intermediate
4
40
8
6
1
59
Resistant
279
159
105
6
9
558
Susceptible
388
224
130
27
18
787
Intermediate
16
11
7
2
1
37
Resistant
133
44
85
7
3
272
Susceptible
191
84
43
20
12
350
Intermediate
12
1
8
1
0
22
Resistant
334
194
171
15
10
724
Susceptible
219
73
65
18
12
387
Intermediate
24
11
14
2
5
56
Resistant
294
195
143
16
5
653
Susceptible
260
78
147
4
5
494
Intermediate
8
16
7
3
3
37
Resistant
269
185
68
29
14
565
Susceptible
281
93
58
5
17
454
Intermediate
25
12
6
0
3
46
Resistant
231
174
158
31
2
596
Susceptible
517
176
119
31
19
862
Intermediate
12
6
3
0
1
22
Resistant
8
97
100
5
2
212
Susceptible
329
42
34
17
18
440
Intermediate
9
8
7
4
2
30
Resistant
199
229
181
15
2
626
Susceptible
134
164
22
12
15
347
Intermediate
11
33
4
6
1
55
Resistance
rate (%)
46.99
27.83
50.91
24.82
66.06
59.58
51.55
54.38
19.34
57.12
63.32
Oxacillin
Volume 31, September & October 2023
Journal of Advances in Medical and Biomedical Research
Erfan Fakheri et al. 469
Ampicillin
Levofloxaci
n
S.
epidemidi
s
Group D
Streptococci
S.
saprohyti
cus
Viridans
streptococc
i
S.
aureus
Total
(N)
Resistant
392
82
196
18
6
694
Susceptible
119
93
86
14
7
319
Intermediate
6
14
3
1
1
25
Resistant
412
172
133
21
14
752
Susceptible
253
159
93
4
9
518
Intermediate
10
2
4
2
1
19
Resistant
274
118
125
30
13
560
Resistance
rate (%)
68.61
51.09
Discussion
A total number of 3582 ambulatory and hospitalized
patients with bacterial UTI were included in our study.
The overall prevalence of UTI was significantly high
(85%, P<0.001) among the patients with a urine culture
request compared to several similar studies, which
reported overall UTI prevalence of 12.1% to 45.32%
(12-15). Even though this prevalence variation can be
due to geographical and environmental factors,
diagnostic methods applied in the study and the
characteristics of the included patients such as personal
hygiene standards and diet (15), high prevalence ratio
in our study raises the concern of sufficiency of the
quantity of microbiologic tests requested by the
physicians in this clinical setting in Zanjan, Iran from
2016 to 2018.
Similar to other studies in this timeframe and as
expected from the general epidemiology of UTIs (14),
the female patients consisted the majority of the
population in our study. Furthermore, a significant
increase was observed in the prevalence of UTI with
age, given that most of the patients were from the
middle-aged and the elderly group (P=0.016). This can
be explained by higher number of hospital admission,
longer duration of stay and previous antibiotic therapy
in the elderly. UTI incidence in women over 60 was 1.7
times higher than the overall incidence in females,
putting this group at the highest risk. This result is
similar to that of a study by Alós, which reported 20%
and 11% UTI prevalence rates in women over 65 years
and in the overall population, respectively (16).
marcescens usually accounts for 1-2% of HAIs;
however, its isolation rate was significantly higher in
this study (5.38%) (P<0.001) (18). This reveals that
even though S. marcescens rarely causes communityacquired infections, its importance should be taken into
account in healthcare settings and as a nosocomial
infection, which plays a critical role in hospital
outbreaks.
S. epidermidis and group D streptococci were the
most prevalent gram-positive bacteria in the patient
population with respective prevalence rates of 15.99%
and 7.7%. This result was consistent with previous
literature reporting Enterococcus spp., Staphylococcus
spp., and Streptococcus agalactiae as dominant grampositive uropathogens. Gram-positive bacteria
nevertheless, are more likely to be contaminants in the
urine cultures and should be analyzed along with other
factors including symptoms and urine analysis results
such as WBC count (19, 20). Lactobacilli-containing
samples were excluded from antibiotic susceptibility
tests since they are a part of vaginal bacterial flora and
commonly indicative of contamination while
collecting urine specimens (21).
Gram-negative bacteria were the most sensitive and
resistant to nitrofurantoin and piperacillin with
resistance rates of 25.27% and 76.04%, respectively.
Gram-positive bacteria were widely resistant to
ampicillin
(68.61%)
and
Trimethoprim/Sulfamethoxazole (66.06%).
Gram-negative bacteria were significantly more
prevalent (68%) than gram positive-bacteria (32%) in
this study (P<0.001) and E. coli was the pathogen
behind more than half of the infections. This is in
accordance with results from several other studies,
which reported the dominance of gram-negative
bacteria and especially E. coli in their study
populations (12). The second most common gramnegative bacteria -S. marcescens- nevertheless, was not
reported to be frequently isolated in UTIs in other
studies, as normally, E. coli, K. pneumoniae, P.
aeruginosa, Enterobacter, Citrobacter, P. mirabilis are
the most common bacterial uropathogens (17). S.
These results are in line with resistance patterns
reported from Iran and worldwide (3, 12, 17, 22, 23).
Vancomycin resistance was relatively low in both
gram-negative (26.74%) and gram-positive (19.34%)
bacteria. However, it is considered as a last-resort
antibiotic and should only be included in the antibiotic
therapy regimen according to regional guidelines and
only when needed. The vancomycin resistance result in
our study was higher compared to that of a UTI study
conducted by Mihankhah et al., in northern Iran, in the
same timeframe (11.7%) (22). Furthermore, in a study
by Khoshbakht et al., conducted in Karaj, Iran in 2013,
vancomycin resistance was reported 7.7% (24). This
rate was reported lower and under 5% in a ten-year
Volume 31, September & October 2023
Journal of Advances in Medical and Biomedical Research
470 Bacterial Uropathogens
surveillance European study conducted on the
prevalence and susceptibility patterns of UTIassociated bacteria, in 2013 (13).
The limitations of the study included exclusive
application
of
conventional
biochemical
microbiological tests for bacterial identification and
not determining resistance-associated genes.
Erfan Fakheri contributed to Conceptualization.
Narges Moradi and Niloufar Kazemi contributed to
data collection, writing and data curation.
Acknowledgments
The authors are grateful for the support of colleagues
in Bacteriology and virology Departments at Zanjan
University of Medical Sciences.
Conclusion
The overall prevalence of UTIs was relatively high
in this study, which emphasizes the importance of
proper quantity and quality of urine cultures and
susceptibility tests, as well as development of novel
efficient surveillance guidelines for each area. E.
coli and S. epidermidis were the most prevalently
isolated uropathogens and there was a notable S.
marcescens outbreak in the study timeframe. Alarming
resistance rates were observed in ampicillin and
piperacillin, which should be taken into account in
therapy guidelines in this area. Prevalence of resistant
strains can be avoided by developing appropriate
healthcare policies and community awareness. Further
studies should focus on regional and periodical
prevalence and susceptibility patterns of the UTIs,
globally.
Conflict of Interest
The authors declare that they have no competing
interests.
References
1.
Sikora A ZF. Nosocomial infections: StatPearls
Publishing; 2021. Available from:
[https://www.ncbi.nlm.nih.gov/books/NBK55931
2/]
2.
Horan TC, Andrus M, Dudeck MA. CDC/NHSN
surveillance definition of health care-associated
infection and criteria for specific types of
infections in the acute care setting. Am J Infect
Control. 2008;36(5):309-32.
[DOI:10.1016/j.ajic.2008.03.002] [PMID]
3.
Responsible genes to antibiotic resistance, genetic
relationship between the resistant strains, and
investigating
any correlations
with
patient
characteristics are not determined and these are the
limitations of this study. Moreover, identification of
isolates were merely performed taking advantage of
biochemical aspect.
Mohammadi M, Vaisi Raiegan A, Jalali R,
Ghobadi A, Salari N, Barati H. The prevalence of
nosocomial infections in Iranian hospitals. J Babol
Univ Med Sci. 2019;21(1):39-45.
4.
Magill SS, Edwards JR, Bamberg W,et al.
Multistate point-prevalence survey of health careassociated infections. N Engl J Med.2014;370(13):
1198-208. [DOI:10.1056/NEJMoa1306801]
[PMID] [PMCID]
Consent for publication
5.
Monegro AF MV, Regunath H. Hospital acquired
infections treasure island (FL): StatPearls
Publishing; 2021 [updated 2021 Aug 30; cited
2021 Aug 1]. Available from:
[https://www.ncbi.nlm.nih.gov/books/NBK44185
7/]
6.
Geerts N, Boonen KJM, Boer AK, Scharnhorst V.
Cut-off values to rule out urinary tract infection
should be gender-specific. Clinica Chimica Acta.
2016;452:173-6.
[DOI:10.1016/j.cca.2015.11.022] [PMID]
7.
Gupta S, Malakar M, Kalita P, Pandey F. Bacterial
profile and antibiograms in urinary tract
infection.Al Ameen J Me Sci.2019;12(4):192-96.
8.
Masajtis-Zagajewska A, Nowicki M. New
markers of urinary tract infection. Clin chim Acta.
2017;471:286-91.
[DOI:10.1016/j.cca.2017.06.003] [PMID]
9.
Flores-Mireles AL, Walker JN, Caparon M,
Hultgren
SJ.
Urinary
tract
infections:
Limitations
All named authors meet the International Committee
of Medical Journal Editors (ICMJE) criteria for
authorship for this article, take responsibility for the
integrity of the work as a whole, and have given their
approval for this version to be published.
Availability of Data and Materials
All data generated or analyzed during this study are
included
in
this
published
article/as
supplementary information files.
Funding
Not applicable.
Authors’ Contributions
Supervision, methodology, final editing and review
were done by Bahman Mirzaei. Bahman Mirzaei and
Volume 31, September & October 2023
Journal of Advances in Medical and Biomedical Research
Erfan Fakheri et al. 471
epidemiology, mechanisms of infection and
treatment options. Nat Rev Microbiol. 2015;13(5):
269-84. [DOI:10.1038/nrmicro3432] [PMID]
[PMCID]
10. Parte A, Whitman WB, Goodfellow M, et al.
Bergey's manual of systematic bacteriology:
volume 5: the Actinobacteria: Springer Science &
Business Media; 2012.
11. Wayne P. Clinical and laboratory standards
institute. Performance standards for antimicrobial
susceptibility testing.Research Gate. 2011.
12. Gessese YA, Damessa DL, Amare MM, et al.
Urinary pathogenic bacterial profile, antibiogram
of isolates and associated risk factors among
pregnant women in Ambo town, Central Ethiopia:
a cross-sectional study. Antimicrob Resist Infect
Control. 2017;6(1):132. [PMID] [PMCID]
[DOI:10.1186/s13756-017-0289-6]
13. Linhares I, Raposo T, Rodrigues A, Almeida A.
Frequency and antimicrobial resistance patterns of
bacteria implicated in community urinary tract
infections: a ten-year surveillance study (20002009). BMC Infect Dis. 2013;13(1):19. [PMID]
[DOI:10.1186/1471-2334-13-19] [PMCID]
14. Medina M, Castillo-Pino E. An introduction to the
epidemiology and burden of urinary tract
infections. Therapeut Adv Urol. 2019;11:
1756287219832172. [PMID] [PMCID]
[DOI:10.1177/1756287219832172]
15. Shaifali I, Gupta U, Mahmood SE, Ahmed J.
Antibiotic susceptibility patterns of urinary
pathogens in female outpatients. North Am J Med
Sci. 2012;4(4):163. [PMID] [PMCID]
[DOI:10.4103/1947-2714.94940]
16. Alós JI. Epidemiology and etiology of community
urinary infection. Antimicrobial susceptibility of
major pathogens and clinical significance of
resistance. Infect Dis Clin Microbiol. 2005; 23:38.
17. Ade-Ojo I, Oluyege A, Adegun P, Akintayo A,
Aduloju O, Olofinbiyi B. Prevalence and
antimicrobial susceptibility of asymptomatic
significant bacteriuria among new antenatal
enrollees in Southwest Nigeria. Int Res J
Microbiol. 2013;4(8):197-203
18. Khanna A, Khanna M, Aggarwal A. Serratia
marcescens- a rare opportunistic nosocomial
pathogen and measures to limit its spread in
hospitalized patients. J Clin Diagn Res. 2013;7(2):
243-6. [DOI:10.7860/JCDR/2013/5010.2737]
[PMID] [PMCID]
19. Kline
KA,
Lewis
AL.
Gram-positive
uropathogens, polymicrobial urinary tract
infection, and the emerging microbiota of the
urinary tract. Microbiol Spectr. 2016;4(2):10.
[DOI:10.1128/microbiolspec.UTI-0012-2012]
[PMID] [PMCID]
20. Kim SY, Park Y, Kim H, et al. Rapid screening of
urinary tract infection and discrimination of grampositive and gram-negative bacteria by automated
flow cytometric analysis using sysmex UF-5000. J
Clin Microbiol. 2018;56(8):e02004-17.
[DOI:10.1128/JCM.02004-17] [PMID] [PMCID]
21. Darbro BW, Petroelje BK, Doern GV.
Lactobacillus delbrueckii as the cause of urinary
tract infection. J Clin Microbiol. 2009;47(1):2757. [DOI:10.1128/JCM.01630-08] [PMID]
[PMCID]
22. Mihankhah A, Khoshbakht R, Raeisi M, Raeisi V.
Prevalence and antibiotic resistance pattern of
bacteria isolated from urinary tract infections in
Northern Iran. J Res Med Sci 2017;2:18.
23. Ghanbari F, Khademi F, Saberianpour S, et al. An
epidemiological study on the prevalence and
antibiotic resistance patterns of bacteria isolated
from urinary tract infections in central Iran.
Avicenna J Clin Microbiol Infect. 2017;4(3):
42214. [DOI:10.5812/ajcmi.42214]
24. Khoshbakht R, Salimi A, Shirzad Aski H,
Keshavarzi H. Antibiotic susceptibility of
bacterial strains isolated from urinary tract
infections in Karaj, Iran. Jundishapour J
Microbiol. 2013;6(1):86-90.
[DOI:10.5812/jjm.4830]
How to Cite This Article:
Fakheri E, Kazemi N, Moradi N, Mirzaei B. Bacterial Urinary Tract Infections in North West of Iran: A CrossSectional Study. J Adv Med Biomed Res. 2023; 31(138):464-71.
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