This study analyzed urine samples collected from 2011-2013 at a hospital in Silchar, India to determine the antibiotic resistance patterns of bacteria causing urinary tract infections (UTIs). The main findings were:
1) Escherichia coli was the most common cause of UTIs, identified in 38.54% of samples. Resistance to oral antibiotics like fluoroquinolones and cephalosporins was high for E. coli isolates.
2) Extended spectrum beta-lactamase (ESBL) production was observed in 28.74% of E. coli and 40.74% of Klebsiella isolates.
3) Methicillin-resistant Staphylococcus aureus (
Antibiotic Resistance Pattern among Uropathogens in Silchar Hospital
1. International Journal of Advances in Health Sciences (IJHS)
ISSN 2349-7033
Vol-3, Issue-1, 2016, pp1-9
http://www.ijhsonline.com
Research Article
Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care
Hospital in Silchar
Nishanta Thakuria, Rohit Tigga and Gunamani Thakuria
Department of Pharmacology
Silchar Medical College and Hospital, India.
(Email: dr.nyshanta@yahoo.co.in)
[Received-19/12/2015, Accepted-29/12/2015, Published- 07/01/2016]
ABSTRACT
Urinary tract infections (UTIs) are amongst the most common infections encountered in clinical practice with an
estimated 150 million UTIs per annum worldwide. The introduction of antimicrobial therapy has contributed
significantly to the management of UTIs. However the main problem with current antibiotic therapies is the
rapid emergence of antimicrobial resistance in hospitals and the community.
Aims: To determine the frequency and pattern of antibiotic resistance among uropathogens in a Tertiary Care
Hospital in Silchar.
Settings and Design: Outdoor and indoor wards of Silchar Medical College & Hospital, Silchar/ Retrospective
study
Methods and Material: An analysis was done on all the urine samples (1799) sent for culture and sensitivity to
the department of Microbiology, SMCH, Silchar from 1st
January 2011 to 31st
December 2013. A total of 659
positive urinary isolates were detected from the 1799 samples. Antibiotic susceptibility was done on Mueller
Hinton Agar plate by Bauer-Kirby method. Extended spectrum beta lactamase (ESBL) production was
determined by the double disk approximation test and the Clinical and Laboratory Standards Institute (formerly
NCCLS) confirmatory method and Methicilin Resistant Staphylococcus aureus (MRSA) production was
determined by the oxacillin disc inhibition test and the Clinical and Laboratory Standards Institute (formerly
NCCLS) confirmatory method.
Statistical analysis used: Microsoft excel sheet was used to plot the data and prepare the graphs.
Results: During the study period, 1799 consecutive urine samples were processed from OPD and indoor
patients, 659 (36.63%) of these urine samples [OPD- 106 (16.08%) and Indoor- 553 (83.92%)] yielded
significant growth of pathogens. Escherichia coli was the most frequently isolated uropathogen accounting for
38.54% of the total isolates. ESBL production was observed in 28.74% of E. coli strains and 40.74% of
Klebsiella strains. MRSA producing organisms was found to be 28.40% of S. aureus strains. With the exception
of nitrofurantoin and amoxycillin/clavulinic acid for gram negative bacteria and linezolid for gram positive
cocci, resistance to agents commonly used as oral treatments for UTI was quite high.
Conclusions: The study revealed E. coli as the predominant bacterial pathogen, followed by S. aureus for UTIs
in Silchar Medical College & Hospital, Silchar, Assam. An increasing trend in the production ESBLs and
MRSAs among UTI pathogens were noted.
Key-words: Urinary tract infection, Antimicrobial resistance, Escherichia coli, Staphylococcus aureus
INTRODUCTION
Urinary tract infections (UTIs) are amongst the
most common infections encountered in clinical
practice with an estimated 150 million UTIs per
annum worldwide.[9,15] Although UTIs occur
in both men and women, clinical studies
suggest that the overall prevalence of UTI is
higher in women. Uncomplicated UTIs in
healthy women have an incidence of
50/1000/year.[6] An estimated 50% of women
experience at least one episode of UTI at some
point in their lifetime and between 20% and
40% of women have recurrent episodes.[23,28]
The introduction of antimicrobial therapy has
contributed significantly to the management of
2. Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care Hospital in Silchar
Nishanta Thakuria, et al. 2
UTIs. However the main problem with current
antibiotic therapies is the rapid emergence of
antimicrobial resistance in hospitals and the
community.[12] Antibiotics are usually given
empirically before the laboratory results of
urine culture are available. To ensure
appropriate therapy, current knowledge of the
organisms that cause UTI and their antibiotic
susceptibility is mandatory.[10] The resistance
pattern of community acquired uropathogens
has not been extensively studied in the Indian
subcontinent.[1,3,16]
No data concerning the antimicrobial resistance
of bacteria isolated from UTIs from this part of
the country (i.e. the southern part of the state of
Assam) has been documented till date. It is
important to realize that there may be marked
differences between various geographic areas
within a vast country like India.
Since most UTIs are treated empirically the
selection of antimicrobial agent should be
determined not only by the most likely
pathogen but also by its expected susceptibility
pattern. Thus, knowledge of local antimicrobial
susceptibility patterns of common uropathogens
is essential for prudent empiric therapy of
community acquired UTIs.
It was against this backdrop that the current
study was undertaken to assess the most
frequent pathogens responsible for UTIs in
outdoor and indoor patients and their
antimicrobial resistance pattern in Silchar
Medical College, Silchar, Assam, through
consecutive urine samples collected during
three year period from January 2011 to
December 2013. Additionally, the study also
aimed at identifying possible resistance trends.
AIMS AND OBJECTIVES
To determine the frequency and pattern of
antibiotic resistance among uropathogens in a
Tertiary Care Hospital in Silchar.
MATERIALS AND METHODS
Type of study: Retrospective study.
Place of study: Silchar Medical College and
Hospital.
Study period: One year, from August 2014 to
July 2015
An analysis was done on all the urine samples
(1799) sent for culture and sensitivity to the
department of Microbiology, SMCH, Silchar
from 1st January 2011 to 31st December 2013.
A total of 659 positive urinary isolates were
detected from the 1799 samples. Antibiotic
susceptibility was done on Mueller Hinton Agar
plate by Bauer-Kirby method. Freshly voided,
midstream urine samples collected in sterile
containers from OPD patients were received in
the Microbiology lab.
The sample was inoculated for semi-
quantitative culture on Mc-Conkey media and
blood agar from Jnauary 2011 to September
2012 and on Cystine Lactose Electrolyte
Deficient (CLED) media from October 2012 to
December 2013 using a calibrated loop. The
culture plate was incubated at 37°C for 18-24
hours under aerobic conditions. Identification
of bacterial growth was determined by Gram’s
staining and standard microbiology
techniques.[5]
Antibiotic Sensitivity Testing:
Antibiotic susceptibility was performed by the
Kirby-Bauer disc diffusion method on Mueller
Hinton agar or Nutrient agar.[4]
The following antibiotics were tested:
amoxiclav (20/10 mcg), amikacin (30 mcg),
norfloxacin (10 mcg), ciprofloxacin(5 mcg),
nitrofurantoin (300 mcg), gentamicin (10 mcg),
cefuroxime (30 mcg), ceftriaxone (30 mcg),
ceftazidime (30 mcg), cefotaxime (30 mcg),
piperacillin/tazobactam (100/10 mcg),
cefoperazone/sulbactam (75/30 mcg), and
vancomycin(30 mcg), imipenem(10 mcg),
cefoperazone (75 mcg), cefepime(30 mcg),
levofloxacin (5 mcg), cefexime (5 mcg),
aztreonam (30 mg), nitrofurantoin (300
mcg),ofloxacin (5 mcg),cefaclor(30 mcg),
linezolid (30 mcg), cefoxitin (30 mcg).
Dehydrated media and antibiotic discs were
procured from Himedia, India. The controls
strains used were E. coli ATCC 25922,
Pseudomonas aeruginosa ATCC 27853, and
Staphylococcus aureus 25922.
3. Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care Hospital in Silchar
Nishanta Thakuria, et al. 3
Tests for Extended Spectrum Beta
Lactamases (ESBL) production:
Double disc approximation test
The organism was swabbed on to a Mueller-
Hinton agar plate. Antibiotic discs of
amoxicillin/clavulanic acid (20/10 mcg) and a
cephalosporin disc (cefotaxime (30 mcg),
ceftriaxone (30 mcg), and ceftazidime (30
mcg)) were placed at a distance of 15 mm apart
and incubated. Organism that showed a clear
extension of any of the cephalosporin inhibition
zone towards the disc containing clavulanate
was considered as ESBL producer.[14]
National committee for clinical laboratory
standards confirmatory test
While performing antibiotic testing, ceftazidime
(30 mcg), and ceftazidime plus clavulanic acid
(30/10 mcg) were placed on Mueller-Hinton
agar and incubated. Organism was considered
as ESBL producer if there was a ≥5 mm
increase in the zone diameter of
ceftazidime/clavulanate disc and that of
ceftazidime disc alone. E. coli ATCC 25922
and a known in-house ESBL producer were
used as negative and positive controls,
respectively.[20]
Tests for Methicilin Resistant
Staphylococcus aureus (MRSA) production:
Disk Diffusion Method:
Staphylococcous aureus are tested for
methicillin resistance according to CLSI
guidelines. Here while performing antibiotic
sensitivity by Kirby Bauer disc diffusion
method in Mueller Hinton Agar, the diameter of
zone of inhibition around the Oxacillin(1 mcg)
disc is noted. If the zone diameter is <13mm
around oxacillin, then the strain is regarded as
MRSA.[21]
Statistics:
All data were entered in Microsoft Excel
2007and was used to plot the data and prepare
the graphs.
RESULTS
During the study period, 1799 consecutive urine
samples were processed from OPD and indoor
patients, 659 (36.63%) of these urine samples
[OPD- 106 (16.08%) and Indoor- 553
(83.92%)] yielded significant growth of
pathogens. Remaining 1140 samples had either
no significant bacteriuria or had a very low
bacterial count or were sterile urine.
Table 1 outlines the demographic profile of
patients with community acquired UTIs. The
patients were between the ages 1 month and 95
years with a mean age of 30.42 years. UTIs
were reported in 286 (43.39%) males and 373
(56.61%) females. Females of the reproductive
age group (between 21 and 50 years)
constituted 28.81% of the total patients with
UTI. However, elderly (61 years or more)
males had a higher incidence of UTI (6.36%)
compared to the elderly females (4.38%) of the
total patients with UTI.
Table 2 describes the year wise frequency and
distribution of various urinary pathogens
isolated from both indoor and OPD patients. E.
coli was the predominant uropathogen all
through the study period accounting for 38.54%
of the total isolates. These were followed by
Staphylococcus aureus (25.64%), Klebsiella
species (12.29%), Pseudomonas aeruginosa
(8.80%) and Enterococcus species (8.04%).
Table 3 depicts the antibiotic resistance pattern
of tested antimicrobials against the encountered
uropathogens. A high proportion of strains of E.
coli were resistant to orally administered drugs
such as fluoroquinolones: ofloxacin (18.5%),
ciprofloxacin (17.71%), levofloxacin (14.96%),
norfloxacin (12.59%) & moxifloxacin
(12.20%); and cephalosporins: cefixime
(15.35%), cefadroxil (11.41%) & cefaclor
(11.41%). Nitrofurantoin (5.1%) is the orally
administered drug with least resistance,
followed by amoxycillin/clavulinic acid
(7.08%) to E. coli throughout the 3 year study
period. However, oxacillin and
amoxycillin/clavulinic acid demonstrated a very
high resistance for Staphylococcus aureus
species of 29.54% and 45.45% respectively.
Out of the injectable drugs with highest
resistance to the strains of E. coli were
cefuroxime (30.31%), ceftazidime (28.74%),
ceftriaxone (26.37%) and
4. Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care Hospital in Silchar
Nishanta Thakuria, et al. 4
piperacillin/tazobactum(23.22%).
Aminoglycosides: amikacin and gentamicin
have shown a resistance trend against E. coli of
6.29% and 10.23% respectively. Linezolid
remains the drug with least resistance for gram
positive cocci showing a resistance of 0.86% (2
cases out of total 232 gram positive isolates),
followed by vancomycin (1.29%).
Table 4 depicts the frequency of isolation of
ESBL (Extended Spectrum Beta Lactamases)
producing organisms over the 3 year period.
Extended spectrum beta lactamases production
was observed in 28.74% of E. coli strains,
40.74% of Klebsiella species strains, 15.52% of
Pseudomonas aeruginosa strains and 29.17% of
Proteus species strains. The total number of
ESBL cases were highest in 2011 (46.82%),
followed by 2013 (44.35%) and lowest in the
year 2012 (4.79%).
Table 5 depicts the frequency of isolation of
MRSA (Methicillin Resistant Staphylococcus
aureus) producing organisms over the 3 year
period. An increasing trend in the isolation of
MRSA cases has been noticed over the study
period with 1.4% in 2011 to 40.9% in 2012 to
50.8% in 2013.
DISCUSSION
This is the first study to evaluate the
susceptibility patterns of bacterial strains
isolated from OPD and indoor patients with
UTIs in Silchar Medical College & Hospital
(SMCH), Silchar, Assam. This study provides
valuable laboratory data and allows comparison
of the situation in Assam with other parts of the
country. The results show that 36.63% of urine
samples from patients attending the outpatient
clinics and indoor patients at our hospital
yielded significant pathogens. The culture
positive rate for community acquired
uropathogens was higher in our study than that
reported at Aligarh, India (10.86%),[1] Tehran,
Iran (6.3%)[17] and Jaipur, India
(17.19%).[24]
The demographic data indicates that women of
the reproductive age group formed the main
group of adult patients with UTI presenting to
the OPD and wards of SMCH (28.83% of all
UTI detected in women of age 21-50 years).
UTIs were reported in 56.61% of females and
in 43.39% of males. It has been extensively
reported that adult women have a higher
prevalence of UTI than men, principally owing
to anatomic and physical factors.[1] Elderly (61
years or more) males had a higher incidence of
UTI (6.37%) compared to the elderly females
(4.40%). This is probably because with the
advancing age, the incidence of UTI increases
is men due to prostate enlargement and
neurogenic bladder.[7] The study demonstrates
that E. coli remain the leading uropathogen
being responsible for 38.54% of UTIs in
SMCH, and no change in its prevalence among
all uropathogens was observed over the 3 year
study period. This is in consistent with findings
of other studies around the globe in which E.
coli was the most frequently reported isolate
from patients with UTIs.[8,11,13,18,19]
Following E. coli, our study shows
Staphylococcus aureus (25.64%), Klebsiella
species (12.29%), Pseudomonas aeruginosa
(8.80%) and Enterococcus species (8.04%) as
the other common uropathogens in the setting
of SMCH.
Enterobacteriaceae have several factors
responsible for their attachment to the
uroepithelium. These gram negative aerobic
bacteria colonize the urogenital mucosa with
adhesion, pili, fimbriae, and P1-blood group
phenotype receptor.[7] In our study,
Enterobacteriaceae bacteria accounted for
54.93% of all the isolates, followed by gram
positive cocci (35.20%) and non-fermenting
gram-negative bacteria (9.86%).
Our study reveals 28.74% of the E. coli isolates
and 40.74% of Klebsiella species to be ESBL
producers. Pitout et al. have also highlighted the
emergence of Enterobacteriaceae producing
ESBLs in the community particularly from
UTIs.[25] Aggarwal et al. reported 40% of E.
coli and 54.54% of Klebsiella species to be
ESBL producers from Rohtak, Haryana.[2] In
another study from Nagpur, 18.5% of E. coli
isolates and 25.6% of Klebsiella isolates were
found to be ESBL producers.[26] This
geographical difference may be due to different
5. Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care Hospital in Silchar
Nishanta Thakuria, et al. 5
patterns of antibiotic usage. Our study confirms
the global trend towards increased resistance to
β-lactam antibiotics. ESBL producing bacteria
may not be detectable by routine disk diffusion
susceptibility test, leading to inappropriate use
of antibiotics and treatment failure. It is
emphasized that institutions should employ
appropriate tests for their detection and avoid
indiscriminate use of third-generation
cephalosporins.
Generally, uncomplicated UTIs are treated in
the community with short courses of empirical
antibiotics. In many cases, urine samples are
only sent for microbiological evaluation
following treatment failure, recurrent or
relapsing infection. Although the levels of
resistance we observed amongst community
isolates may therefore overestimate the true rate
of resistance in the community, the high levels
of resistance of gram negative uropathogens to
ampicillin, amoxiclav, and co-trimoxazole raise
concerns over the use of these agents. Our
findings are in consistence with the recent data
reported from other developing
countries.[25,27]
Our findings thus suggest that empirical
treatment with these drugs should no longer be
appropriate. Aminoglycosides: amikacin,
gentamicin have shown a resistance trend
against E. coli in the 3 year study period from
2011 to 2013 as 6.29% and 10.23%
respectively. Aminoglycosides being
injectables are used restrictively in the
community-care setting and hence have shown
better sensitivity rates. The overall resistance of
E. coli to the fluoroquinolones i.e.,
ciprofloxacin, norfloxacin, ofloxacin,
levofloxacin and moxifloxacin was 17.71%,
12.59%, 18.50%, 14.90% and 12.20%
respectively. Fluoroquinolones have a wide
variety of indications, permeate most body
compartments, and are ubiquitously prescribed,
accounting for the emergence of their
resistance. Our findings indicate that urgent
strategies to counteract increased resistance to
these drugs must be developed or their use in
uncomplicated infections should be strictly
curtailed. Nitrofurantoin (5.1%) has shown the
least resistance for E. coil. Our findings are
similar to other Indian studies which have also
demonstrated nitrofurantoin as an appropriate
agent for first-line treatment of community
acquired UTIs.[3,16] Given the fact that
nitrofurantoin has no role in the treatment of
other infections, it can be administered orally
and is highly concentrated in urine; it may
therefore be the most appropriate agent for
empirical use in uncomplicated UTI.
Fosfomycin is another oral antibiotic which is
commonly used for treatment of CA-UTI in
Europe with low resistance rates; however, it is
not marketed in India.[3] Linezolid (0.86%)
and vancomycin (1.29%) are the drug with least
resistance to gram positive cocci. An overall
1.88% resistance for vancomycin and no
resistance for linezolid was observed in gram
positive cocci belonging to the Enterococcus
species. Although, the frequency of isolation of
vancomycin-resistant Enterococci is not very
high in our setting as compared to West, this
may just be the beginning of the problem.
CONCLUSION
In our study, the culture positive rate for urinary
tract infections was high, with the majority
coming from female patients of reproductive
age group. As expected, E. coli was the most
common etiological agent identified and
remains susceptible to nitrofurantoin. This drug
should therefore be the ideal antibiotic to use
for uncomplicated UTI. Our findings suggest
the presence of ESBL and MRSA-producing
strains in the community as well as in the
hospital; therefore, monitoring of antibiotic
susceptibility of bacterial isolates should be
mandatory. International guidelines are no
longer applicable for treating community
acquired UTIs in India and development of
specific guidelines based on local susceptibility
patterns are necessary.
ACKNOWLEDGEMENT
We acknowledge the support of Dr. A. K.
Borthakur, Professor & Head, Department of
Microbiology, Silchar Medical College &
Hospital, Silchar, Assam in helping us conduct
and complete the study.
8. Antibiotic Resistance Pattern among Uropathogens in a Tertiary Care Hospital in Silchar
Nishanta Thakuria, et al. 8
Year
Total no.
of E. coli
isolated
ESBL
producing
E. coli No.
(%)
Total no. of
Klebsiela
spp.
isolated
ESBL
producing
Klebsiela spp.
No. (%)
Total no.
of P.
aeruginosa
isolated
ESBL
producing
P. aeruginosa
No. (%)
Total no.
of
Proteus
spp.
isolated
ESBL
producing
Proteus spp.
No. (%)
2011 77 40 (51.95) 23 12 (52.17) 21 6 (28.57) 5 1 (20)
2012 99 2 (2.02) 31 4 (12.09) 30 1 (3.33) 7 1 (14.24)
2013 78 31 (39.75) 27 17 (62.9) 7 2 (28.57) 12 5 (41.67)
Total 254 73 (28.74) 81 33 (40.74) 58 9 (15.52) 24 7 (29.17)
Table 4: Percentage distribution of extended spectrum beta-lactamase producing uropathogens isolated over the
study period
Year
Total no. of S.
aureus isolated
MRSA No. (%)
2011 68 1 (1.4)
2012 44 18 (40.9)
2013 57 29 (50.8)
Total 169 48 (28.40)
Table 5: Percentage distribution of MRSA producing uropathogens isolated over the study period
Abbreviations:
MRSA – Methicillin resistant Staphyloccous aureus
CA-UTI – Community acquired urinary tract
infection
ESBL – Extended spectrum Beta lactamase
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