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Volume 20 / Issue 1 / April 2013
Original Article 
Antimicrobial resistance in pathogens causing urinary 
tract infections in a rural community of Odisha, India 
Muktikesh Dash, Sanghamitra Padhi, Indrani Mohanty, Pritilata Panda, Banojini Parida 
Department of Microbiology, Maharaja Krushna Chandra Gajapati Medical College and Hospital, Berhampur University, Odisha, India 
Address for correspondence: Dr. Muktikesh Dash, Department of Microbiology, Maharaja Krushna Chandra Gajapati Medical College and 
Hospital, Berhampur, Odisha ‑ 760 004, India. E‑mail: mukti_mic@yahoo.co.in 
ABSTRACT 
Background: Antimicrobial resistance of urinary tract pathogens has increased worldwide. Empiric treatment 
of community‑acquired urinary tract infection (CA‑UTI) is determined by antimicrobial resistance patterns 
of uropathogens in a population of specific geographical location. Objectives: This study was conducted to 
determine the prevalence of CA‑UTI in rural Odisha, India, and the effect of gender and age on its prevalence as 
well as etiologic agents and the resistance profile of the bacterial isolates. Materials and Methods: Consecutive 
clean‑catch mid‑stream urine samples were collected from 1670 adult patients. The urine samples were 
processed and microbial isolates were identified by conventional methods. Antimicrobial susceptibility testing 
was performed on all bacterial isolates by Kirby Bauer’s disc diffusion method. Results: The prevalence of 
UTI was significantly higher in females compared with males (females 45.2%, males 18.4%, OR = 2.041, 95% 
CI = 1.64‑2.52, P ≤ 0.0001). Young females within the age group of 18‑37 years and elderly males (≥68 years) 
showed high prevalence of UTI. Escherichia coli (68.8%) was the most prevalent isolate followed by Enterococcus 
spp. (9.7%). Amikacin and nitrofurantoin were the most active antimicrobial agents which showed low resistance 
rate of 5.8% and 9.8%, respectively. Conclusion: Our study revealed E. coli as the pre‑dominant bacterial 
pathogen. Nitrofurantoin should be used as empirical therapy for uncomplicated CA‑UTIs. In the Indian 
setting, routine urine cultures may be advisable, since treatment failure is likely to occur with commonly used 
antimicrobials. Therefore, development of regional surveillance programs is necessary for implementation 
of national CA‑UTI guidelines. 
Key words: Antimicrobial, community‑acquired urinary tract infection, Escherichia coli, prevalence, 
resistance 
INTRODUCTION 
Urinary tract infection (UTI) is most common infectious 
disease after respiratory tract infection in community 
practice. It remains a major public health problem in 
terms of morbidity and financial cost with an estimated 
150 million cases per annum worldwide, costing global 
economy in excess of 6 billion US dollars.[1] Although 
UTIs occur in all age groups including men and women, 
clinical studies suggest that the overall prevalence of UTI is 
higher in women. An estimated 50% of women experience 
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DOI: 
10.4103/2230-8229.108180 
at least one episode of UTI at some point of their lifetime 
and between 20% and 40% of women can have recurrent 
episodes.[2,3] Approximately 20% of all UTIs occur in men.[4] 
UTI is defined as bacteriuria along with urinary symptoms.[5] 
It may involve only the lower urinary tract or may involve 
both the upper and lower tract. The term cystitis has 
been used to describe lower UTI, which is characterized 
by a syndrome involving dysuria, frequency, urgency and 
occasionally suprapubic tenderness. However, the presence 
of symptoms of lower tract without upper tract symptoms 
does not exclude upper tract infection, which is also often 
present.[6] 
Malnutrition, poor hygiene, low socio‑economic status 
are associated with UTIs and these factors are usually 
found in rural settings.[7] Although Escherichia coli has been 
reported as the commonest isolate causing UTI, few 
authors have reported changing patterns in the prevalence 
of uropathogens.[8,9] 
20 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 | 20-26
Dash, et al.: Antimicrobial resistance in urinary tract infections 
The introduction of antimicrobial therapy has contributed 
significantly to the management of UTIs. In almost 
all cases of community‑acquired UTI (CA‑UTI), 
empirical antimicrobial treatment is initiated before the 
laboratory results of urine culture are available; thus 
resistance may increase in uropathogens due to frequent 
misuse of antimicrobials.[10] The resistance pattern 
of community‑acquired uropathogens has not been 
extensively studied in the eastern India.[11‑13] To the best of 
our knowledge, no data concerning resistance of bacteria 
isolated from UTIs from rural Odisha, India has been 
documented till date. Since most CA‑UTIs are treated 
empirically, the selection of appropriate antimicrobial 
agents should be determined by the most likely pathogen 
and its expected resistance pattern in a geographic area. 
Therefore there is need for periodic monitoring of 
etiologic agents of UTI, and their resistance pattern in 
the community. 
This study was undertaken in view of paucity of reports of 
UTIs in our adult community of Odisha state, India. The 
aim of the study is to determine the prevalence of UTI 
as well as the effect of gender and age on its prevalence. 
The etiologic agents and their susceptibility pattern will 
also be determined. 
MATERIALS AND METHODS 
Study area 
The present retrospective study was carried out in the 
central clinical microbiology laboratory of a tertiary care 
hospital which is located in southern Odisha, India and 
catering patients mostly from rural to tribal areas. The 
duration of the study was two and half year period from 
January 2010 to July 2012. 
Study population 
A total of 1670 adult patients from rural areas with 
signs to symptoms of UTI who attended the outpatient 
departments (OPDs) of our hospital were recruited for 
this study. They consisted of 1006 females and 664 males 
with age ranging from 18 to 85 years. Exclusion criteria 
included (a) patient’s age <18 years (b) patients with 
history of inpatient admission a week prior to their 
presentation in our OPDs to rule out hospital acquired 
infections (c) antibiotics usage within week and (d) patients 
from urban areas. Verbal informed consent was obtained 
from all patients prior to specimen collection. The study 
was conducted after due approval from institutional ethical 
committee. 
Sample collection and processing 
Freshly voided, clean‑catch midstream urine sample was 
collected from each patient into sterile screw‑capped 
universal container in the OPDs. The specimen was 
labeled and transported to the microbiology laboratory 
for processing within 2 h. 
Semi quantitative urine culture was done using a 
calibrated loop. A loopful (0.001 mL) of well mixed 
un‑centrifuged urine was inoculated onto the surface of 
cysteine lactose electrolyte deficient medium. The culture 
plates were incubated aerobically at 37°C for 18‑24 h 
and count were expressed as colony forming units (cfu) 
per milliliter (ml). For this study, significant bacteriuria 
was defined as culture of a single bacterial species 
from the urine sample at a concentration of 105 cfu/ml 
associated with microscopy findings of >10 white blood 
cells (WBCs) per high power field.[14] Only patients 
with significant bacteriuria (≥105 cfu/ml) were included 
for microbiological analysis. The culture isolates were 
identified by standard microbiological methods.[15] All 
culture media were procured from HiMedia Laboratories, 
Mumbai, India. 
Isolates were tested for antimicrobial susceptibility testing by 
the standard Kirby‑Bauer disc diffusion method according 
to Bauer et al.[16] Mueller‑Hinton agar plates were incubated 
for 24 h after inoculation with organisms and placement of 
discs. After 24 h the inhibition zones were measured. The 
following standard antibiotic discs for the isolates were used; 
ampicillin (10 mcg), augmentin i.e. amoxicillin + clavulinic 
acid (20/10 mcg), co‑trimoxazole (23.75/1.25 mcg), 
nitrofurantoin (300 mcg), ciprofloxacin (5 mcg), 
ofloxacin (5 mcg), cefaclor (30 mcg), cefpodoxime 
cefpodoxime proxetil (10 mcg), gentamicin (10 mcg) and 
amikacin (30 mcg). Antibiotic discs were obtained from 
HiMedia Laboratories, Mumbai, India. The results were 
interpreted according to Clinical and Laboratory Standards 
Institute guidelines.[17] The quality control strains used were 
E. coli American type culture collection (ATCC) 25922, 
Pseudomonas aeruginosa ATCC 27853, Enterococcus fecalis 
ATCC 29212 and Staphylococcus aureus ATCC 25923 for 
antimicrobial discs. 
Statistical analysis 
The data were analyzed using Chi‑square (χ2) test, 
confidence interval (CI), odds ratio (OR) analysis and 
P value by GraphPad® Software, Inc. 2236 Avenida de la 
Playa La Jolla, CA 92037 USA, InStat statistical software. 
Statistical significance was defined when P value is <0.05. 
RESULTS 
The age distribution of the patients in the sample set was 
18‑85 years (mean 43.6 years, standard deviation 16.2 years). 
A total of 1670 urine samples from clinically suspected 
patients were analyzed for CA‑UTI. Of these, 577 (34.5%) 
Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 21
Dash, et al.: Antimicrobial resistance in urinary tract infections 
samples were found to be culture positive showing 
significant bacteriuria and the remaining 1093 (65.5%) 
samples were either non‑significant bacteriuria or had 
sterile urine [Table 1]. 
From total 1670 patients, 1006 (60.2%) were female to 
among these 455 (45.2%) showed culture positive significant 
bacteriuria. Out of 664 male patients, only 122 (18.4%) had 
CA‑UTI. Female gender was a significant risk factor for 
acquiring CA‑UTI (OR = 2.041, 95% CI = 1.64‑2.52, and 
statistically significant P value of <0.0001, Table 1). 
The prevalence of CA‑UTI was highest within 18‑27 years 
of age group (29.2%), followed by 28‑37 years (26.2%), 
among the female patients. Whereas majority of the 
isolates (41.8%) were obtained from male patients 
aged ≥68 years [Table 2]. 
Table 3 illustrates the overall frequency of 
community‑acquired uropathogens. From total 577 
significant isolates, Gram‑negative aerobic rods accounted 
for 451 (78.2%), while Gram‑positive cocci accounted 
for 120 (20.8%) and Candida spp. in 6 (1%) cases. 
Escherichia coli was the most pre‑dominant isolate causing 
CA‑UTI, followed by Enterococcus spp., coagulase negative 
Staphylococci (CONS), Staphylococcus aureus, Klebsiella spp., 
Citrobacter spp. and Pseudomonas spp. (9.7, 6.2, 4.9, 2.9, 2.3, 
and 1.6%, respectively). 
Antimicrobial resistance profiles of the bacterial isolates 
are summarized in Table 4. Overall Gram‑negative 
isolates showed higher resistant pattern in comparison 
with Gram‑positive isolates. Gram‑positive isolates 
showed least resistant to nitrofurantoin, augmentin, 
ciprofloxacin, ofloxacin, gentamicin, and amikacin. 
Among all Gram‑negative isolates, E. coli showed highest 
resistance to most commonly used antimicrobials. E. coli 
isolates were least resistant to amikacin (5.8%), followed 
by nitrofurantoin (9.8%) and gentamicin (15.9%). 
Importantly for E. coli, the commonly recommended 
antimicrobials i.e. augmentin, co‑trimoxazole, ampicillin, 
cefaclor cefpodoxime, ciprofloxacin and ofloxacin 
showed high resistant rates (63.7, 51.9, 94.7, 66.7, 
58.2, 53.4, and 47.1%, respectively). The presence of 
Pseudomonas spp. i.e., 1.6% of all isolates was striking 
since it is considered to be a nosocomial pathogen. It 
showed highest sensitivity to ciprofloxacin, gentamicin 
and amikacin. 
DISCUSSION 
Against the background of paucity of reports of CA‑UTI 
in rural setting of India, this is the first study conducted 
to determine the prevalence of UTI, the effect of gender 
and age on its prevalence and their susceptibility profile 
in a rural community of Odisha state, India. This study 
provides valuable laboratory data to monitor the status 
of antimicrobial resistance among uropathogens and 
to improve treatment recommendations in a specific 
geographical region. The study also allows comparison 
of the situation in Odisha with other regions within and 
outside the country. Our data was restricted to patients 
who can afford laboratory analysis; therefore this study 
may not reflect the true prevalence of UTI among patients 
in Odisha as most patients are initially treated empirically 
for their symptoms of UTI. 
From total 1670 urine samples collected from CA‑UTI 
patients 577 (34.5%) yielded significant pathogens. The 
similar value of 39.7% was obtained by Oladeinde et al. 
in rural community of Nigeria.[18] The culture positive 
rate for CA‑UTI was higher in our study in comparison 
with studies conducted in Jaipur, India (17.19%) and 
Aligarh, India (10.86%).[12,19] Orrett in south Trinidad and 
Garcia‑Morŭa et al. in Mexican population had obtained 
higher significant uropathogens (49% and 97.3%, 
respectively).[20,21] Geographical location may be the reason 
for this wide difference. 
The finding showed that females (45.2%) had higher 
prevalence of UTI in comparison with males (18.4%) in 
agreement with earlier studies.[18,19,21,22] Close proximity of 
the female urethral meatus to anus, short urethra, and sexual 
intercourse have been reported as factors which influence 
the higher prevalence in women.[8] 
The age group analysis showed that young female patients 
in the range of 18‑37 years had highest prevalence 
rate (55.4%) of CA‑UTI. This result is in agreement 
with previous studies.[12,19,23] Among sexually active young 
Table 1: Effect of gender on prevalence of urinary tract infection in rural Odisha, India 
Gender Total no. of urine specimen Odds ratio 95% CI P value 
No. tested No. not infected (%) No. infected (%) 
Male 664 542 (81.6) 122 (18.4) 2.041 1.64‑2.52 P≤0.0001 (P<0.05, significant) 
Female 1006 551 (54.8) 455 (45.2) 
Total 1670 1093 577 
CI, Confidence interval 
22 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1
Dash, et al.: Antimicrobial resistance in urinary tract infections 
women the incidence of symptomatic UTI is high, and the 
risk is strongly associated with recent sexual intercourse, 
recent use of diaphragm with spermicide, and a history of 
recurrent UTIs.[24] Elderly males (≥68 years) had a higher 
incidence of CA‑UTI (41.8%) when compared with the 
elderly females (10.3%). This finding is similar to study 
conducted by Sood et al.[19] This is probably because with 
advancing age, the incidence of UTI increases among 
males due to prostate enlargement and neurogenic 
bladder.[25] 
In our study Gram‑negative aerobic rods (78.2%) 
pre‑dominated, among which E. coli was the commonest 
uropathogen responsible for CA‑UTI. It accounted for 
68.8% of all culture‑positive isolates, while Enterococcus 
spp. was the next most common organism, accounting for 
9.7% of isolates in the present study. The proportion of 
bacterial species isolated was similar to those described 
in previous studies.[19,26,27] Our study significantly differed 
from Garcia‑Morŭa et al., who found out that E. coli 
was the commonest organism in UTI (24.7%), followed 
by Candida albicans (23.7%) among Mexican population 
group.[21] The data collected from other places around 
the world, also showed that E. coli and Klebsiella spp. are 
still the commonest uropathogens isolated in CA‑UTI 
patients[12,13,28‑30] [Table 5]. Gram‑negative aerobic bacteria 
including Enterobacteriaceae have several factors 
responsible for their attachment to uroepithelium. They 
colonize in the urogenital mucosa with adhesins, pili, 
fimbriae, and P‑1 blood group phenotype receptor.[25] 
The infectious disease society of America guidelines 
consider co‑trimoxazole, fluoroquinolones, nitrofurantoin, 
and β‑lactams including augmentin, cefdinir, 
cefaclor, cephalexin, cefpodoxime‑proxetil as current 
standard empirical therapy for uncomplicated UTI in 
women.[31] However, the guidelines have a suggestion that 
local antimicrobial susceptibility patterns must be taken 
into account before choosing an agent. 
Generally, uncomplicated UTIs are treated empirically in 
the community with short courses of oral antibiotics. In 
most cases, microbiological evaluation of UTI cases were 
conducted only following treatment failure, recurrent or 
relapsing infection. Overall, Gram‑negative isolates showed 
higher resistant pattern in comparison to Gram‑positive 
isolates in the present study. 
Table 2: Effect of age on prevalence of urinary 
tract infection in rural Odisha, India 
Age 
groups 
in years 
No. of 
females 
infected (%) 
No. of 
males 
infected (%) 
P value 
18‑27 133 (29.2) 12 (9.8) Chi‑Square 
(χ2)=9.105 
P value=0.1049 
(P<0.05, 
Significant) 
28‑37 119 (26.2) 11 (9) 
38‑47 65 (14.3) 09 (7.4) 
48‑57 58 (12.7) 17 (13.9) 
58‑67 45 (9.9) 22 (18.1) 
≥68 35 (7.7) 51 (41.8) 
Total 455 (100) 122 (100) 
Table 3: Prevalence of uropathogens in rural 
Odisha, India 
Microorganisms Frequency Percentage 
Escherichia coli 397 68.8 
Klebsiella spp. 17 2.9 
Citrobacter spp. 13 2.3 
Pseudomonas spp. 09 1.6 
Proteus spp. 08 1.4 
Enterobacter spp. 07 1.2 
Total Gram‑negative organisms 
451 78.2 
isolated 
Enterococcus spp. 56 9.7 
Coagulase negative 
staphylococci (CONS) 
36 6.2 
Staphylococcus aureus 28 4.9 
Candida spp. 06 1 
Total Gram‑positive organisms 
isolated 
126 21.8 
Total organisms (Both Gram 
negative and positive) 
577 100 
Table 4: Resistance patterns of Escherichia coli, Gram‑negative isolates and Gram‑positive isolates 
Antimicrobial Number (%) of isolates 
resistant for Escherichia 
coli (N=397) 
Number (%) of isolates 
resistant for all Gram‑negative 
isolates (N=451) 
Number (%) of isolates 
resistant for all Gram‑positive 
isolates (N=120) 
Ampicillin 376 (94.7) 419 (92.9) 78 (65) 
Augmentin 253 (63.7) 274 (60.7) 23 (19.2) 
Co‑trimoxazole 206 (51.9) 241 (53.4) 46 (38.3) 
Nitrofurantoin 39 (9.8) 43 (9.5) 07 (5.8) 
Cefaclor 265 (66.7) 288 (63.8) 43 (35.8) 
Cefpodoxime 231 (58.2) 253 (56.1) 47 (39.2) 
Ciprofloxacin 212 (53.4) 231 (51.2) 16 (13.3) 
Ofloxacin 187 (47.1) 201 (44.6) 18 (15) 
Gentamicin 63 (15.9) 66 (14.6) 11 (9.2) 
Amikacin 23 (5.8) 24 (5.3) 12 (10) 
Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 23
Dash, et al.: Antimicrobial resistance in urinary tract infections 
Our study revealed that among Gram‑negative bacteria, 
the most common isolate E. coli showed high level 
of resistance to commonly used empirical antibiotics 
β‑lactams (ampicillin, augmentin, cefaclor, and cefpodoxime), 
fluoroquinolones (ciprofloxacin and ofloxacin) and 
co‑trimoxazole. This value is similar to previous community 
based studies in India[13,19,32] [Table 6]. These high resistant 
rates among uropathogenic isolates from a rural population 
with poor access to health care raises question about 
selection pressures that generate, maintain and spread 
resistant strains in the community. It is also possible that due 
to poor access to health care services, irrational prescription 
of antimicrobials which are available over‑the‑counter in 
India, has contributed to this alarming situation. Unqualified 
practitioners, untrained pharmacists and nurses all over 
the country use antimicrobials indiscriminately.[33] Similar 
practices have also been reported from other developing 
countries, including Nepal and Vietnam.[34,35] The widespread 
use of antimicrobials in veterinary practice may be another 
possible factor for the emergence of resistant strains. Our 
findings thus suggest that empirical treatment with these 
drugs should no longer be appropriate. 
Aminoglycosides i.e., gentamicin and amikacin showed low 
resistant rate of 15.9% and 5.8%, respectively for E. coli. 
Aminoglycosides being injectables are used less commonly 
in the community‑care setting and hence have shown better 
sensitivity rates. 
In our study, nitrofurantoin has shown better activity 
against most uropathogens with resistant rate of less 
than 10%. Similar results had been reported from 
studies conducted in different parts of India.[19,23,32] 
Nitrofurantoin should therefore be the ideal antibiotic of 
choice for uncomplicated UTI. The limitation of orally 
available Nitrofurantoin formulation is that it cannot be 
recommended for serious upper UTI or for those patients 
with systemic involvement.[3] 
Reference 
no 
Candida 
spp. 
Enterococcus 
spp. 
Akram et al. (2007) in Aligarh, India 61 22 ‑ 4 2 ‑ ‑ 7 1 ‑ [12] 
Selvakumar et al. (2007) in southern 
44 14.5 0.6 6.2 3.8 3 ‑ ‑ ‑ ‑ [28] 
India 
Kothari et al. (2008) in Delhi, India 68 16.9 5.5 ‑ ‑ 5.3 2.8 ‑ 1.5 ‑ [13] 
Khameneh et al. (2009) in Iran 78.6 5.5 3.4 1.6 1.5 2.2 5.2 1.7 ‑ ‑ [27] 
Garcia‑Morŭa et al. (2009) in Mexico 24.7 6.5 ‑ 6.1 ‑ ‑ ‑ 6.8 13.4 23.7 [21] 
Kashaf et al. (2010) in Tehran, Iran 68.8 9.6 12.4 3.3 0.2 0.4 1.1 0.6 1.3 ‑ [22] 
Sood et al. (2011) in Jaipur, india 61.8 6.6 1.4 4.6 2.3 3.7 0.9 5.5 9.2 0.3 [19] 
Oladeinde et al. (2011) in Nigeria 41.2 4.4 6.7 2.4 ‑ ‑ ‑ 32.3 ‑ 12.2 [18] 
Bahadin et al. (2011) in Singapore 74.5 8.7 3 1.5 2.7 0.6 1.2 3.9 2.4 0.6 [29] 
Sabharwal et al. (2012) in Rajasthan, 
63.3 8.3 3.4 1.7 ‑ ‑ 15 8.3 ‑ ‑ [32] 
India 
Shaifali et al. (2012) in Lucknow, India 33.1 7.9 0.7 ‑ ‑ ‑ ‑ 2.2 ‑ ‑ [23] 
Bano et al. (2012) in Pakistan 47 18.1 0.2 0.2 ‑ 0.1 3.6 13.2 3.6 4.8 [30] 
Present study in Odisha, India 68.8 2.9 1.4 1.6 2.3 1.2 6.2 4.9 9.7 1 
CONS: Coagulase negative staphylococci includes S.=saprophyticus and S.=epidermidis 
CONCLUSIONS 
The worldwide trend of empirically treating CA‑UTI 
may not apply for specific geographical regions, where 
decreased susceptibility rates are documented for 
common uropathogens. As more than two thirds of all 
pathogens are E. coli, local antimicrobial susceptibility 
patterns of E. coli in particular should be considered 
in antimicrobial selection for CA‑UTIs. In the Indian 
setting, routine urine cultures may be advisable, since 
treatment failure likely to occur with commonly used 
antimicrobials. Therefore, development of regional 
surveillance programs is necessary for implementation 
of Indian CA‑UTI guidelines. Table 5: Worldwide distribution of pathogens isolated among community‑acquired urinary tract infection patients 
Author, year and place of study Percentage (%) of bacterial species isolated 
CONS Staphylococcus 
aureus 
Enterobacter 
spp. 
Citrobacter 
spp. 
Pseudomonas 
spp. 
Proteus 
spp. 
Klebsiella 
spp. 
Escherichia 
coli 
24 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1
Dash, et al.: Antimicrobial resistance in urinary tract infections 
Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 25 
Table 6: Regional antimicrobial resistance patterns of Escherichia coli isolates 
Author, year 
and place of 
study 
Percentage of Escherichia coli isolates resistant to antimicrobials 
Ampicillin Augmentin Co‑trimoxazole Nitrofurantoin Ciprofloxacin Cefpodoxime Cefaclor Ofloxacin Gentamicin Amikacin Reference 
no. 
Akram 
et al. (2007) in 
Aligarh, India 
‑ ‑ 76 80 69 85 ‑ ‑ 64 51 [12] 
Selvakumar 
et al. (2007) 
in southern 
India 
96 72 71 62 92 ‑ ‑ 62 73 21 [28] 
Kothari 
et al. (2008) in 
Delhi, India 
‑ 59.2 74 24.4 72 ‑ ‑ ‑ ‑ 33 [13] 
Khameneh 
et al. (2009) 
in Iran 
‑ ‑ ‑ 69.8 83.2 ‑ ‑ ‑ 83.9 ‑ [27] 
Garcia‑Morŭa 
et al. (2009) in 
Mexico 
‑ ‑ ‑ 19.5 73.2 ‑ ‑ ‑ ‑ 14.7 [21] 
Kashaf 
et al. (2010) in 
Teheran, Iran 
96.4 ‑ 61.8 28.7 31.9 ‑ ‑ ‑ 50.7 ‑ [22] 
Sood 
et al. (2011) in 
Jaipur, India 
81.2 80.7 67.8 5.8 74.7 ‑ ‑ ‑ 28 8.2 [19] 
Oladeinde 
et al. (2011) in 
Nigeria 
‑ 87.1 75.3 81.2 9.5 ‑ ‑ 29.5 47.1 ‑ [18] 
Bahadin 
et al. (2011) in 
Singapore 
46.3 9.3 37.8 5.3 24.4 ‑ ‑ ‑ 8.5 ‑ [29] 
Sabharwal 
et al. (2012) 
in Rajasthan, 
India 
90 78 75 10 80 ‑ ‑ ‑ 15 00 [32] 
Shaifali 
et al. (2012) 
in Lucknow, 
India 
52.2 ‑ 39.2 13.1 60.9 ‑ 65.2 ‑ 54.4 95.7 [23] 
Bano 
et al. (2012) in 
Pakistan 
90 62 88 75 95 ‑ ‑ ‑ 77 44 [30] 
Present study 
in Odisha, 
India 
94.7 63.7 51.9 9.8 53.4 58.2 66.7 44.6 38.3 5.3
Dash, et al.: Antimicrobial resistance in urinary tract infections 
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et al. Antibiotic medication and bacterial resistance to antibiotics: 
A survey of children in a Vietnamese community. Trop Med Int 
Health 2000;5:711‑21. 
How to cite this article: Dash M, Padhi S, Mohanty I, Panda P, 
Parida B. Antimicrobial resistance in pathogens causing urinary tract 
infections in a rural community of Odisha, India. J Fam Community 
Med 2013;20:20-6. 
Source of Support: Nil, Conflict of Interest: Nil 
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26 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1

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Antimicrobial resistance in pathogens causing urinary tract infections in a rural community of Odisha, India

  • 1. Volume 20 / Issue 1 / April 2013
  • 2. Original Article Antimicrobial resistance in pathogens causing urinary tract infections in a rural community of Odisha, India Muktikesh Dash, Sanghamitra Padhi, Indrani Mohanty, Pritilata Panda, Banojini Parida Department of Microbiology, Maharaja Krushna Chandra Gajapati Medical College and Hospital, Berhampur University, Odisha, India Address for correspondence: Dr. Muktikesh Dash, Department of Microbiology, Maharaja Krushna Chandra Gajapati Medical College and Hospital, Berhampur, Odisha ‑ 760 004, India. E‑mail: mukti_mic@yahoo.co.in ABSTRACT Background: Antimicrobial resistance of urinary tract pathogens has increased worldwide. Empiric treatment of community‑acquired urinary tract infection (CA‑UTI) is determined by antimicrobial resistance patterns of uropathogens in a population of specific geographical location. Objectives: This study was conducted to determine the prevalence of CA‑UTI in rural Odisha, India, and the effect of gender and age on its prevalence as well as etiologic agents and the resistance profile of the bacterial isolates. Materials and Methods: Consecutive clean‑catch mid‑stream urine samples were collected from 1670 adult patients. The urine samples were processed and microbial isolates were identified by conventional methods. Antimicrobial susceptibility testing was performed on all bacterial isolates by Kirby Bauer’s disc diffusion method. Results: The prevalence of UTI was significantly higher in females compared with males (females 45.2%, males 18.4%, OR = 2.041, 95% CI = 1.64‑2.52, P ≤ 0.0001). Young females within the age group of 18‑37 years and elderly males (≥68 years) showed high prevalence of UTI. Escherichia coli (68.8%) was the most prevalent isolate followed by Enterococcus spp. (9.7%). Amikacin and nitrofurantoin were the most active antimicrobial agents which showed low resistance rate of 5.8% and 9.8%, respectively. Conclusion: Our study revealed E. coli as the pre‑dominant bacterial pathogen. Nitrofurantoin should be used as empirical therapy for uncomplicated CA‑UTIs. In the Indian setting, routine urine cultures may be advisable, since treatment failure is likely to occur with commonly used antimicrobials. Therefore, development of regional surveillance programs is necessary for implementation of national CA‑UTI guidelines. Key words: Antimicrobial, community‑acquired urinary tract infection, Escherichia coli, prevalence, resistance INTRODUCTION Urinary tract infection (UTI) is most common infectious disease after respiratory tract infection in community practice. It remains a major public health problem in terms of morbidity and financial cost with an estimated 150 million cases per annum worldwide, costing global economy in excess of 6 billion US dollars.[1] Although UTIs occur in all age groups including men and women, clinical studies suggest that the overall prevalence of UTI is higher in women. An estimated 50% of women experience Access this article online Quick Response Code: Website: www.jfcmonline.com DOI: 10.4103/2230-8229.108180 at least one episode of UTI at some point of their lifetime and between 20% and 40% of women can have recurrent episodes.[2,3] Approximately 20% of all UTIs occur in men.[4] UTI is defined as bacteriuria along with urinary symptoms.[5] It may involve only the lower urinary tract or may involve both the upper and lower tract. The term cystitis has been used to describe lower UTI, which is characterized by a syndrome involving dysuria, frequency, urgency and occasionally suprapubic tenderness. However, the presence of symptoms of lower tract without upper tract symptoms does not exclude upper tract infection, which is also often present.[6] Malnutrition, poor hygiene, low socio‑economic status are associated with UTIs and these factors are usually found in rural settings.[7] Although Escherichia coli has been reported as the commonest isolate causing UTI, few authors have reported changing patterns in the prevalence of uropathogens.[8,9] 20 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 | 20-26
  • 3. Dash, et al.: Antimicrobial resistance in urinary tract infections The introduction of antimicrobial therapy has contributed significantly to the management of UTIs. In almost all cases of community‑acquired UTI (CA‑UTI), empirical antimicrobial treatment is initiated before the laboratory results of urine culture are available; thus resistance may increase in uropathogens due to frequent misuse of antimicrobials.[10] The resistance pattern of community‑acquired uropathogens has not been extensively studied in the eastern India.[11‑13] To the best of our knowledge, no data concerning resistance of bacteria isolated from UTIs from rural Odisha, India has been documented till date. Since most CA‑UTIs are treated empirically, the selection of appropriate antimicrobial agents should be determined by the most likely pathogen and its expected resistance pattern in a geographic area. Therefore there is need for periodic monitoring of etiologic agents of UTI, and their resistance pattern in the community. This study was undertaken in view of paucity of reports of UTIs in our adult community of Odisha state, India. The aim of the study is to determine the prevalence of UTI as well as the effect of gender and age on its prevalence. The etiologic agents and their susceptibility pattern will also be determined. MATERIALS AND METHODS Study area The present retrospective study was carried out in the central clinical microbiology laboratory of a tertiary care hospital which is located in southern Odisha, India and catering patients mostly from rural to tribal areas. The duration of the study was two and half year period from January 2010 to July 2012. Study population A total of 1670 adult patients from rural areas with signs to symptoms of UTI who attended the outpatient departments (OPDs) of our hospital were recruited for this study. They consisted of 1006 females and 664 males with age ranging from 18 to 85 years. Exclusion criteria included (a) patient’s age <18 years (b) patients with history of inpatient admission a week prior to their presentation in our OPDs to rule out hospital acquired infections (c) antibiotics usage within week and (d) patients from urban areas. Verbal informed consent was obtained from all patients prior to specimen collection. The study was conducted after due approval from institutional ethical committee. Sample collection and processing Freshly voided, clean‑catch midstream urine sample was collected from each patient into sterile screw‑capped universal container in the OPDs. The specimen was labeled and transported to the microbiology laboratory for processing within 2 h. Semi quantitative urine culture was done using a calibrated loop. A loopful (0.001 mL) of well mixed un‑centrifuged urine was inoculated onto the surface of cysteine lactose electrolyte deficient medium. The culture plates were incubated aerobically at 37°C for 18‑24 h and count were expressed as colony forming units (cfu) per milliliter (ml). For this study, significant bacteriuria was defined as culture of a single bacterial species from the urine sample at a concentration of 105 cfu/ml associated with microscopy findings of >10 white blood cells (WBCs) per high power field.[14] Only patients with significant bacteriuria (≥105 cfu/ml) were included for microbiological analysis. The culture isolates were identified by standard microbiological methods.[15] All culture media were procured from HiMedia Laboratories, Mumbai, India. Isolates were tested for antimicrobial susceptibility testing by the standard Kirby‑Bauer disc diffusion method according to Bauer et al.[16] Mueller‑Hinton agar plates were incubated for 24 h after inoculation with organisms and placement of discs. After 24 h the inhibition zones were measured. The following standard antibiotic discs for the isolates were used; ampicillin (10 mcg), augmentin i.e. amoxicillin + clavulinic acid (20/10 mcg), co‑trimoxazole (23.75/1.25 mcg), nitrofurantoin (300 mcg), ciprofloxacin (5 mcg), ofloxacin (5 mcg), cefaclor (30 mcg), cefpodoxime cefpodoxime proxetil (10 mcg), gentamicin (10 mcg) and amikacin (30 mcg). Antibiotic discs were obtained from HiMedia Laboratories, Mumbai, India. The results were interpreted according to Clinical and Laboratory Standards Institute guidelines.[17] The quality control strains used were E. coli American type culture collection (ATCC) 25922, Pseudomonas aeruginosa ATCC 27853, Enterococcus fecalis ATCC 29212 and Staphylococcus aureus ATCC 25923 for antimicrobial discs. Statistical analysis The data were analyzed using Chi‑square (χ2) test, confidence interval (CI), odds ratio (OR) analysis and P value by GraphPad® Software, Inc. 2236 Avenida de la Playa La Jolla, CA 92037 USA, InStat statistical software. Statistical significance was defined when P value is <0.05. RESULTS The age distribution of the patients in the sample set was 18‑85 years (mean 43.6 years, standard deviation 16.2 years). A total of 1670 urine samples from clinically suspected patients were analyzed for CA‑UTI. Of these, 577 (34.5%) Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 21
  • 4. Dash, et al.: Antimicrobial resistance in urinary tract infections samples were found to be culture positive showing significant bacteriuria and the remaining 1093 (65.5%) samples were either non‑significant bacteriuria or had sterile urine [Table 1]. From total 1670 patients, 1006 (60.2%) were female to among these 455 (45.2%) showed culture positive significant bacteriuria. Out of 664 male patients, only 122 (18.4%) had CA‑UTI. Female gender was a significant risk factor for acquiring CA‑UTI (OR = 2.041, 95% CI = 1.64‑2.52, and statistically significant P value of <0.0001, Table 1). The prevalence of CA‑UTI was highest within 18‑27 years of age group (29.2%), followed by 28‑37 years (26.2%), among the female patients. Whereas majority of the isolates (41.8%) were obtained from male patients aged ≥68 years [Table 2]. Table 3 illustrates the overall frequency of community‑acquired uropathogens. From total 577 significant isolates, Gram‑negative aerobic rods accounted for 451 (78.2%), while Gram‑positive cocci accounted for 120 (20.8%) and Candida spp. in 6 (1%) cases. Escherichia coli was the most pre‑dominant isolate causing CA‑UTI, followed by Enterococcus spp., coagulase negative Staphylococci (CONS), Staphylococcus aureus, Klebsiella spp., Citrobacter spp. and Pseudomonas spp. (9.7, 6.2, 4.9, 2.9, 2.3, and 1.6%, respectively). Antimicrobial resistance profiles of the bacterial isolates are summarized in Table 4. Overall Gram‑negative isolates showed higher resistant pattern in comparison with Gram‑positive isolates. Gram‑positive isolates showed least resistant to nitrofurantoin, augmentin, ciprofloxacin, ofloxacin, gentamicin, and amikacin. Among all Gram‑negative isolates, E. coli showed highest resistance to most commonly used antimicrobials. E. coli isolates were least resistant to amikacin (5.8%), followed by nitrofurantoin (9.8%) and gentamicin (15.9%). Importantly for E. coli, the commonly recommended antimicrobials i.e. augmentin, co‑trimoxazole, ampicillin, cefaclor cefpodoxime, ciprofloxacin and ofloxacin showed high resistant rates (63.7, 51.9, 94.7, 66.7, 58.2, 53.4, and 47.1%, respectively). The presence of Pseudomonas spp. i.e., 1.6% of all isolates was striking since it is considered to be a nosocomial pathogen. It showed highest sensitivity to ciprofloxacin, gentamicin and amikacin. DISCUSSION Against the background of paucity of reports of CA‑UTI in rural setting of India, this is the first study conducted to determine the prevalence of UTI, the effect of gender and age on its prevalence and their susceptibility profile in a rural community of Odisha state, India. This study provides valuable laboratory data to monitor the status of antimicrobial resistance among uropathogens and to improve treatment recommendations in a specific geographical region. The study also allows comparison of the situation in Odisha with other regions within and outside the country. Our data was restricted to patients who can afford laboratory analysis; therefore this study may not reflect the true prevalence of UTI among patients in Odisha as most patients are initially treated empirically for their symptoms of UTI. From total 1670 urine samples collected from CA‑UTI patients 577 (34.5%) yielded significant pathogens. The similar value of 39.7% was obtained by Oladeinde et al. in rural community of Nigeria.[18] The culture positive rate for CA‑UTI was higher in our study in comparison with studies conducted in Jaipur, India (17.19%) and Aligarh, India (10.86%).[12,19] Orrett in south Trinidad and Garcia‑MorĹ­a et al. in Mexican population had obtained higher significant uropathogens (49% and 97.3%, respectively).[20,21] Geographical location may be the reason for this wide difference. The finding showed that females (45.2%) had higher prevalence of UTI in comparison with males (18.4%) in agreement with earlier studies.[18,19,21,22] Close proximity of the female urethral meatus to anus, short urethra, and sexual intercourse have been reported as factors which influence the higher prevalence in women.[8] The age group analysis showed that young female patients in the range of 18‑37 years had highest prevalence rate (55.4%) of CA‑UTI. This result is in agreement with previous studies.[12,19,23] Among sexually active young Table 1: Effect of gender on prevalence of urinary tract infection in rural Odisha, India Gender Total no. of urine specimen Odds ratio 95% CI P value No. tested No. not infected (%) No. infected (%) Male 664 542 (81.6) 122 (18.4) 2.041 1.64‑2.52 P≤0.0001 (P<0.05, significant) Female 1006 551 (54.8) 455 (45.2) Total 1670 1093 577 CI, Confidence interval 22 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1
  • 5. Dash, et al.: Antimicrobial resistance in urinary tract infections women the incidence of symptomatic UTI is high, and the risk is strongly associated with recent sexual intercourse, recent use of diaphragm with spermicide, and a history of recurrent UTIs.[24] Elderly males (≥68 years) had a higher incidence of CA‑UTI (41.8%) when compared with the elderly females (10.3%). This finding is similar to study conducted by Sood et al.[19] This is probably because with advancing age, the incidence of UTI increases among males due to prostate enlargement and neurogenic bladder.[25] In our study Gram‑negative aerobic rods (78.2%) pre‑dominated, among which E. coli was the commonest uropathogen responsible for CA‑UTI. It accounted for 68.8% of all culture‑positive isolates, while Enterococcus spp. was the next most common organism, accounting for 9.7% of isolates in the present study. The proportion of bacterial species isolated was similar to those described in previous studies.[19,26,27] Our study significantly differed from Garcia‑MorĹ­a et al., who found out that E. coli was the commonest organism in UTI (24.7%), followed by Candida albicans (23.7%) among Mexican population group.[21] The data collected from other places around the world, also showed that E. coli and Klebsiella spp. are still the commonest uropathogens isolated in CA‑UTI patients[12,13,28‑30] [Table 5]. Gram‑negative aerobic bacteria including Enterobacteriaceae have several factors responsible for their attachment to uroepithelium. They colonize in the urogenital mucosa with adhesins, pili, fimbriae, and P‑1 blood group phenotype receptor.[25] The infectious disease society of America guidelines consider co‑trimoxazole, fluoroquinolones, nitrofurantoin, and β‑lactams including augmentin, cefdinir, cefaclor, cephalexin, cefpodoxime‑proxetil as current standard empirical therapy for uncomplicated UTI in women.[31] However, the guidelines have a suggestion that local antimicrobial susceptibility patterns must be taken into account before choosing an agent. Generally, uncomplicated UTIs are treated empirically in the community with short courses of oral antibiotics. In most cases, microbiological evaluation of UTI cases were conducted only following treatment failure, recurrent or relapsing infection. Overall, Gram‑negative isolates showed higher resistant pattern in comparison to Gram‑positive isolates in the present study. Table 2: Effect of age on prevalence of urinary tract infection in rural Odisha, India Age groups in years No. of females infected (%) No. of males infected (%) P value 18‑27 133 (29.2) 12 (9.8) Chi‑Square (χ2)=9.105 P value=0.1049 (P<0.05, Significant) 28‑37 119 (26.2) 11 (9) 38‑47 65 (14.3) 09 (7.4) 48‑57 58 (12.7) 17 (13.9) 58‑67 45 (9.9) 22 (18.1) ≥68 35 (7.7) 51 (41.8) Total 455 (100) 122 (100) Table 3: Prevalence of uropathogens in rural Odisha, India Microorganisms Frequency Percentage Escherichia coli 397 68.8 Klebsiella spp. 17 2.9 Citrobacter spp. 13 2.3 Pseudomonas spp. 09 1.6 Proteus spp. 08 1.4 Enterobacter spp. 07 1.2 Total Gram‑negative organisms 451 78.2 isolated Enterococcus spp. 56 9.7 Coagulase negative staphylococci (CONS) 36 6.2 Staphylococcus aureus 28 4.9 Candida spp. 06 1 Total Gram‑positive organisms isolated 126 21.8 Total organisms (Both Gram negative and positive) 577 100 Table 4: Resistance patterns of Escherichia coli, Gram‑negative isolates and Gram‑positive isolates Antimicrobial Number (%) of isolates resistant for Escherichia coli (N=397) Number (%) of isolates resistant for all Gram‑negative isolates (N=451) Number (%) of isolates resistant for all Gram‑positive isolates (N=120) Ampicillin 376 (94.7) 419 (92.9) 78 (65) Augmentin 253 (63.7) 274 (60.7) 23 (19.2) Co‑trimoxazole 206 (51.9) 241 (53.4) 46 (38.3) Nitrofurantoin 39 (9.8) 43 (9.5) 07 (5.8) Cefaclor 265 (66.7) 288 (63.8) 43 (35.8) Cefpodoxime 231 (58.2) 253 (56.1) 47 (39.2) Ciprofloxacin 212 (53.4) 231 (51.2) 16 (13.3) Ofloxacin 187 (47.1) 201 (44.6) 18 (15) Gentamicin 63 (15.9) 66 (14.6) 11 (9.2) Amikacin 23 (5.8) 24 (5.3) 12 (10) Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 23
  • 6. Dash, et al.: Antimicrobial resistance in urinary tract infections Our study revealed that among Gram‑negative bacteria, the most common isolate E. coli showed high level of resistance to commonly used empirical antibiotics β‑lactams (ampicillin, augmentin, cefaclor, and cefpodoxime), fluoroquinolones (ciprofloxacin and ofloxacin) and co‑trimoxazole. This value is similar to previous community based studies in India[13,19,32] [Table 6]. These high resistant rates among uropathogenic isolates from a rural population with poor access to health care raises question about selection pressures that generate, maintain and spread resistant strains in the community. It is also possible that due to poor access to health care services, irrational prescription of antimicrobials which are available over‑the‑counter in India, has contributed to this alarming situation. Unqualified practitioners, untrained pharmacists and nurses all over the country use antimicrobials indiscriminately.[33] Similar practices have also been reported from other developing countries, including Nepal and Vietnam.[34,35] The widespread use of antimicrobials in veterinary practice may be another possible factor for the emergence of resistant strains. Our findings thus suggest that empirical treatment with these drugs should no longer be appropriate. Aminoglycosides i.e., gentamicin and amikacin showed low resistant rate of 15.9% and 5.8%, respectively for E. coli. Aminoglycosides being injectables are used less commonly in the community‑care setting and hence have shown better sensitivity rates. In our study, nitrofurantoin has shown better activity against most uropathogens with resistant rate of less than 10%. Similar results had been reported from studies conducted in different parts of India.[19,23,32] Nitrofurantoin should therefore be the ideal antibiotic of choice for uncomplicated UTI. The limitation of orally available Nitrofurantoin formulation is that it cannot be recommended for serious upper UTI or for those patients with systemic involvement.[3] Reference no Candida spp. Enterococcus spp. Akram et al. (2007) in Aligarh, India 61 22 ‑ 4 2 ‑ ‑ 7 1 ‑ [12] Selvakumar et al. (2007) in southern 44 14.5 0.6 6.2 3.8 3 ‑ ‑ ‑ ‑ [28] India Kothari et al. (2008) in Delhi, India 68 16.9 5.5 ‑ ‑ 5.3 2.8 ‑ 1.5 ‑ [13] Khameneh et al. (2009) in Iran 78.6 5.5 3.4 1.6 1.5 2.2 5.2 1.7 ‑ ‑ [27] Garcia‑MorĹ­a et al. (2009) in Mexico 24.7 6.5 ‑ 6.1 ‑ ‑ ‑ 6.8 13.4 23.7 [21] Kashaf et al. (2010) in Tehran, Iran 68.8 9.6 12.4 3.3 0.2 0.4 1.1 0.6 1.3 ‑ [22] Sood et al. (2011) in Jaipur, india 61.8 6.6 1.4 4.6 2.3 3.7 0.9 5.5 9.2 0.3 [19] Oladeinde et al. (2011) in Nigeria 41.2 4.4 6.7 2.4 ‑ ‑ ‑ 32.3 ‑ 12.2 [18] Bahadin et al. (2011) in Singapore 74.5 8.7 3 1.5 2.7 0.6 1.2 3.9 2.4 0.6 [29] Sabharwal et al. (2012) in Rajasthan, 63.3 8.3 3.4 1.7 ‑ ‑ 15 8.3 ‑ ‑ [32] India Shaifali et al. (2012) in Lucknow, India 33.1 7.9 0.7 ‑ ‑ ‑ ‑ 2.2 ‑ ‑ [23] Bano et al. (2012) in Pakistan 47 18.1 0.2 0.2 ‑ 0.1 3.6 13.2 3.6 4.8 [30] Present study in Odisha, India 68.8 2.9 1.4 1.6 2.3 1.2 6.2 4.9 9.7 1 CONS: Coagulase negative staphylococci includes S.=saprophyticus and S.=epidermidis CONCLUSIONS The worldwide trend of empirically treating CA‑UTI may not apply for specific geographical regions, where decreased susceptibility rates are documented for common uropathogens. As more than two thirds of all pathogens are E. coli, local antimicrobial susceptibility patterns of E. coli in particular should be considered in antimicrobial selection for CA‑UTIs. In the Indian setting, routine urine cultures may be advisable, since treatment failure likely to occur with commonly used antimicrobials. Therefore, development of regional surveillance programs is necessary for implementation of Indian CA‑UTI guidelines. Table 5: Worldwide distribution of pathogens isolated among community‑acquired urinary tract infection patients Author, year and place of study Percentage (%) of bacterial species isolated CONS Staphylococcus aureus Enterobacter spp. Citrobacter spp. Pseudomonas spp. Proteus spp. Klebsiella spp. Escherichia coli 24 Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1
  • 7. Dash, et al.: Antimicrobial resistance in urinary tract infections Journal of Family and Community Medicine | April 2013 | Vol 20 | Issue 1 25 Table 6: Regional antimicrobial resistance patterns of Escherichia coli isolates Author, year and place of study Percentage of Escherichia coli isolates resistant to antimicrobials Ampicillin Augmentin Co‑trimoxazole Nitrofurantoin Ciprofloxacin Cefpodoxime Cefaclor Ofloxacin Gentamicin Amikacin Reference no. Akram et al. (2007) in Aligarh, India ‑ ‑ 76 80 69 85 ‑ ‑ 64 51 [12] Selvakumar et al. (2007) in southern India 96 72 71 62 92 ‑ ‑ 62 73 21 [28] Kothari et al. (2008) in Delhi, India ‑ 59.2 74 24.4 72 ‑ ‑ ‑ ‑ 33 [13] Khameneh et al. (2009) in Iran ‑ ‑ ‑ 69.8 83.2 ‑ ‑ ‑ 83.9 ‑ [27] Garcia‑MorĹ­a et al. (2009) in Mexico ‑ ‑ ‑ 19.5 73.2 ‑ ‑ ‑ ‑ 14.7 [21] Kashaf et al. (2010) in Teheran, Iran 96.4 ‑ 61.8 28.7 31.9 ‑ ‑ ‑ 50.7 ‑ [22] Sood et al. (2011) in Jaipur, India 81.2 80.7 67.8 5.8 74.7 ‑ ‑ ‑ 28 8.2 [19] Oladeinde et al. (2011) in Nigeria ‑ 87.1 75.3 81.2 9.5 ‑ ‑ 29.5 47.1 ‑ [18] Bahadin et al. (2011) in Singapore 46.3 9.3 37.8 5.3 24.4 ‑ ‑ ‑ 8.5 ‑ [29] Sabharwal et al. (2012) in Rajasthan, India 90 78 75 10 80 ‑ ‑ ‑ 15 00 [32] Shaifali et al. (2012) in Lucknow, India 52.2 ‑ 39.2 13.1 60.9 ‑ 65.2 ‑ 54.4 95.7 [23] Bano et al. (2012) in Pakistan 90 62 88 75 95 ‑ ‑ ‑ 77 44 [30] Present study in Odisha, India 94.7 63.7 51.9 9.8 53.4 58.2 66.7 44.6 38.3 5.3
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