Original Article

Analysis of Antibiotic Sensitivity Profile of Biofilm‑Forming

Uropathogenic Escherichia coli
Kulkarni Ramesh Sudheendra, Peerapur V. Basavaraj1
Department of Microbiology, BLDEA’s Shri B M Patil Medical College, Bijapur, 1Department of Microbiology, Raichur Institute of Medical Sciences, Raichur, Karnataka,
India

Abstract
Introduction: Biofilms are group of microorganisms which are embedded within a self-produced matrix of extracellular polymeric substance
which adhere to each other. They are found to be involved in a wide range of infections in the body like urinary tract infections (UTIs). Biofilms
are considered to be highly resistant to antimicrobial agents. Escherichia coli (E. coli) is the most common organism causing both community
as well as hospital acquired UTI leading to serious health issues. Objectives: This study was conducted to analyse the antibiotic sensitivity
profile of biofilm forming Escherichia coli (E. coli) isolated from patients with suspected UTI attending a Teaching hospital of North Karnataka.
Materials And Methods: 388 E. coli isolates recovered from1000 suspected cases of UTI were tested for susceptibility to fourteen different
antibiotics. In vitro biofilm formation was detected by Tube adherence method, Congo red agar method and Tissue culture plate method.
Results: 277 isolates (71.39%) produced biofilm in-vitro by all the three methods. Biofilm forming E. coli developed significantly higher degree
of resistance towards antimicrobial drugs Ampicillin (87.36%), Cefuroxime (81.58%), Amoxicillin clavulanic acid (77.61%), Ciprofloxacin
(71.48%) and Ceftriaxone (71.48%). They were sensitive to higher antibiotics like Imipenem, Piperacillin-tazobactam, Nitrofurantoin, and
Amikacin. Conclusion: Detection of biofilm in E. coli and its resistance to commonly prescribed antibiotics in the clinical practice is essential
in improving the efficacy of empirical treatment. This study revealed the prevalence and antimicrobial susceptibility pattern of biofilm forming
E. coli which helps clinicians to treat UTI effectively.

Keywords: Antibiotic resistance, biofilm, Escherichia coli, urinary tract infection

Introduction colonization of the bacteria and help the organism overcome

host defenses and invade the urinary tract.[9]
Urinary tract infections (UTIs) are the major and most
important cause of serious health problems and morbidity. Biofilm formation is one of the most important virulence factors
UTIs account for more than 7 million visits to physicians per exhibited by E. coli among other virulence factors. Microbial
year[1‑3] affecting persons of all ages including children, women, biofilms are  community of bacteria and other microorganisms
and elderly but most predominant in women, especially in that are irreversibly attached to self‑produced extracellular
developing countries such as India.[4,5] Approximately 40% polymeric substances and adhere to a surface or each other.
of women have had a UTI in their lifetime and over 20% of Biofilms are ubiquitous and can be found in a variety of niches
young sexually active women who had previous UTIs have or sites or devices. They play an important role in medicine and
recurrent UTIs.[6] have been proven to cause a wide range of microbial infections
in the human body such as UTIs, catheter‑associated infections,
Escherichia coli is the most common organism causing both
or dental plaques.[10]
community and hospital‑acquired UTIs, leading to serious
secondary health issues worldwide.[7,8] Currently, recurrent
UTI is a serious health problem for many women despite our Address for correspondence: Mr. Kulkarni Ramesh Sudheendra,
Department of Microbiology, BLDEA’s Shri B M Patil Medical College,
broad array of very successful antimicrobial agents. Recurrent Bijapur, Karnataka, India.
and relapse UTIs may be due to bacterial virulence factors E‑mail: sudheekulkarni86@gmail.com
exhibited by uropathogenic E. coli (UPEC) which enable
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DOI: How to cite this article: Sudheendra KR, Basavaraj PV. Analysis of
10.4103/jnsbm.JNSBM_209_17 antibiotic sensitivity profile of biofilm-forming uropathogenic Escherichia
coli. J Nat Sc Biol Med 2018;9:175-9.

© 2018 Journal of Natural Science, Biology and Medicine | Published by Wolters Kluwer - Medknow 175
 Sudheendra and Basavaraj: Sensitivity profile of uropathogenic Escherichia coli

Biofilms decrease the susceptibility of organism to antimicrobial Tube adherence method

agents by enclosing them in an extracellular matrix.[11] A high This test described by Christensen et al. is a qualitative method for
content of polysaccharides in biofilm prevents the access of biofilm detection.[16] A loopful of test organisms was inoculated
antimicrobial agents. Limited penetration of antimicrobial in 10 ml of trypticase soy broth with 1% glucose in test tubes. The
agents into the biofilm and slow rate of cell multiplication of tubes were incubated at 37°C for 24 h. After incubation, tubes were
organisms in the biofilm may contribute to the development decanted and washed with phosphate‑buffered saline (pH 7.3) and
of chronic infections. Biofilm‑forming bacteria exhibit higher dried. Tubes were then stained with crystal violet (0.1%). Excess
resistance to antimicrobial drugs used for the treatment of stain was washed with deionized water and dried. The scoring
UTIs, which also lead to recurrent infections.[12] for tube method was done according to the results of the control
Our study aimed to unveil the association of biofilm‑forming strains. Biofilm formation was considered positive when a visible
E. coli and their antimicrobial susceptibility pattern. This study film lined the wall and the bottom of the tube.
would help the clinicians in choosing suitable antibiotics for
Congo red agar method
effective treatment of UTI.
Freeman et al.[17] have described a simple qualitative method to
detect biofilm production using CRA medium. CRA medium was
Materials and Methods prepared with brain–heart infusion broth 37 g/L, sucrose 50 g/L, agar
Sample collection and processing no. 1 10 g/L (HiMedia Laboratories, Mumbai, Maharashtra, India),
This study was conducted in the Department of Microbiology, and Congo red indicator 8 g/L (Nice chemicals, Cochin). Initially,
Bidar Institute of Medical Sciences (BRIMS), Bidar, after getting Congo red stain was prepared as a concentrated aqueous solution
approval from the Institutional Ethical Committee. One thousand and autoclaved (121°C for 15 min) separately from the other
patients of all age groups and both sexes complaining of burning medium constituents. It was then added to the autoclaved
micturition and other associated illness attending the outpatient brain–heart infusion agar with sucrose at 55°C. CRA plates were
department of BRIMS teaching hospital were included in this inoculated with test organisms and incubated at 37°C for 24 h
study. Informed consent was obtained from all the patients. aerobically. Black colonies with a dry crystalline consistency
Clean‑catch midstream urine samples were collected in a sterile indicated biofilm production.
widemouthed container along with information about their
age, sex, and brief clinical history. Samples were transported Tissue culture plate method
to the laboratory immediately and processed for culture and This quantitative test described by Christensen et al. is
antimicrobial drug susceptibility testing as per the routine considered the gold standard method for biofilm detection.[18]
microbiological techniques and recommendations of Kass.[13] Isolates were inoculated in 10 ml of trypticase soy broth with
Further, the isolates were identified by standard biochemical 1% glucose and incubated at 37°C for 24 h. The cultures were
tests, and a diagnosis of UTI was made when pathogens were then diluted 1:100 with fresh medium. Individual wells of
grown at least 105 colony forming unit/ml of urine. Only E. coli sterile TCPs were filled with 200 µL of the diluted cultures
isolates were included in this study. including control strains. Plates were incubated at 37°C for
24 h. After incubation, contents of each well were removed
Antibiotic sensitivity testing
by gentle tapping. The wells were washed with 0.2 mL of
Antibiotics (obtained from HiMedia Laboratories,
phosphate‑buffered saline (pH 7.2) four times. Biofilms
Mumbai, Maharashtra, India) such as ampicillin
formed by bacteria adherent to the wells were fixed by 2%
(AMP 10 µg), amikacin (AK 30 µg), amoxicillin‑clavulanic
sodium acetate and stained by crystal violet (0.1%). Excess
acid (AMC 30 µg), aztreonam (AT 30 µg), ceftriaxone
(CTR 30 µg), cefuroxime (CXM 30 µg), cefepime stain was removed by using deionized water and plates were
(CPM 30 µg), ciprofloxacin (CIP 5 µg), chloramphenicol dried. Optical density of stained adherent biofilms was obtained
(C 30 µg), gentamicin (GEN 10 µg), imipenem (IPM 10 µg), using micro ELISA autoreader (model 680, Biorad, UK) at a
nitrofurantoin (NIT 300 µg), norfloxacin (NX 10 µg), and wavelength of 570 nm. The interpretation of biofilm production
piperacillin‑tazobactam (PIT 100/10 µg) were tested according was done according to the criteria of Stepanovic et al.[19]
to Kirby–Bauer’s disc diffusion method[14] as per the Clinical Quality control
and Laboratory Standards Institute’s (CLSI) guidelines.[15] The biofilm producers such as Staphylococcus epidermidis
Quality control ATCC 35984 (positive control) and the nonbiofilm producers
The CLSI control strain of E. coli ATCC 25922 was used as a such as S. epidermidis ATCC 12228 (negative control) were
control for antimicrobial susceptibility testing. used as standard control strains.
Statistical analysis
In vitro Biofilm Detection Statistical software package SPSS version 22 (IBM SPSS
In vitro detection of biofilm was done by three different Statistics for Windows, IBM Corp., Released 2013, Armonk,
methods as follows: tube adherence method, Congo red agar NY, USA) was used to analyze the data. Chi‑square test was
method (CRA), and tissue culture plate method (TCP). applied. P ˂ 0.05 was considered statistically significant.

176 Journal of Natural Science, Biology and Medicine ¦ Volume 9 ¦ Issue 2 ¦ July-December 2018
Results
Of 1000 urine specimens processed from patients of suspected
UTI, 388 E. coli were isolated (38.8%). Infection was
predominant in females with a rate of 80.92% between the age
group of 20 and 29 years (39%). Among males, the infection
rate was 19.07%.
Among 388 E. coli strains subjected to in vitro biofilm
production, 277 isolates (71.39%) produced biofilm by all
the three methods. In vitro biofilm formation by different
methods was as follows: 40 (10.3%) strains showed
highly positive, 35 strains (9%) showed moderately
positive, and 91 strains (23.5%) showed weakly positive
by tube method [Figure 1]. Similarly, in CRA method, 254
strains (65.5%) showed highly positive [Figure 2], whereas in
TCP method, 284 (73.2%) strains showed strongly positive, Figure 1: Strong biofilm formation of Escherichia coli by tube adherence
23 strains (5.9%) showed moderately positive, and 81 method
strains (20.9%) showed weakly positive [Figure 3 and Table 1].
Biofilm‑producing isolates showed the highest resistance to the
antibiotics compared to nonbiofilm‑producing isolates. Biofilm
producers demonstrated resistance to AMP (87.36%) followed by
CXM (81.58%), AMC (77.61%), CIP (71.48%), CTR (54.6%),
and CPM (64.98%) [Table 2]. Significant association was
observed between biofilm formation and multidrug resistance
which was proved to be statistically significant regarding
antibiotics such as AK, AMC, AT, CTR, CXM, CPM, CIP,
and C [Table 3]. Isolates were sensitive to antibiotics such as
PIT (97.83%), IPM (97.14%), and NIT (92.41%).

Discussion
E. coli is the most prominent causative agent of both
symptomatic and asymptomatic UTIs, which accounts for
more than 80% of the infections.[20,21] In our study, we found Figure 2: Biofilm formation of Escherichia coli on Congo red agar
that the frequency of UTI was higher in females compared
to males, which concord with other studies conducted.[22,23]
This difference in frequency may be due to several clinical
factors, including anatomic differences and hormonal effects.
UTI is associated with an expression of different virulence
factors including biofilm formation. Biofilm formation is
closely related to the susceptibility pattern of E. coli toward
the antimicrobial drugs which are commonly used to treat
UTIs. The resistance pattern in UTI patients of this region is
not known. Understanding the resistance pattern will be helpful
for treatment. Resistance to antibiotics by biofilm‑producing
E. coli increases the chronicity and recurrence of UTI as
bacteria are enclosed within the biofilm and do not allow the
Figure 3: Positive biofilm formation of Escherichia coli by tissue culture
antibiotic access to the bacteria.
plate method
In this study, the incidence of in vitro biofilm formation by
UPEC was 71.39%, which was similar to the studies conducted and we classified them as highly positive (10.3%), moderately
by Subramanian et al.,[24] Sharma et al.,[25] and Suman et al.[26] positive (9%), and weakly positive (23.5%). In CRA method,
who reported biofilm formation at the rates of 63%, 67.5%, 65.5% isolates were found positive. In TCP method, again
and 92.0%, respectively. In our study, we analyzed the in vitro it was classified as strongly positive (73.2%), moderately
biofilm formation by three different methods. Nearly 42.78% positive (5.9%), and weakly positive (20.9%). These findings
of isolates were found positive by tube adherence method, were much closer to the study results reported by Tabasi et al.[27]

177
 Sudheendra and Basavaraj: Sensitivity profile of uropathogenic Escherichia coli

In our study, we detected biofilm formation in all the 388 nonbiofilm producers. Our study results revealed significant
E. coli isolates (100%) by TCP method which was similar to correlation between biofilm formation and multidrug
the findings reported by Fattahi et al.[28] who outlined biofilm resistance. There was an increase in resistance pattern of the
formation in 100% of isolates by TCP method. drugs such as AK, AMC, AT, CTR, CXM, CPM, CIP, and C
We studied antibiotic susceptibility pattern for all UPEC which were routinely used to treat UTIs from a long time. This
isolates. We analyzed the antibiotic resistance pattern pattern of resistance coincides with the study findings reported
of biofilm‑ and nonbiofilm‑forming E. coli isolates. by Mittal et al. and Ponnusamy et al.[29,30]
Biofilm‑forming isolates demonstrated increased resistance Bacterial biofilms are associated with long‑term persistence
to the commonly used antibiotics to treat UTI compared to of the organisms in various environments. Biofilms make the
organisms impermeable to antibiotics and bind the agents at
the outer surface of the matrix layer which protects the bacteria
Table 1: Screening of the Escherichia coli isolates for from penetration of the antibiotics. This causes recurrent
biofilm formation by tube adherence method, Congo Red infection and results in the organism developing multidrug
Agar method, and tissue culture plate method resistance. These strains respond poorly or not respond at all
Tube adherence CRA method (%) TCP method (%) to conventional and routine antimicrobial therapies.
method (%)
In the present study, the drugs PIT, IPM, and NIT were
Strong 40 (10.3) 254 (65.5) 284 (73.2)
Moderate 35 (9) 23 (5.9)
effective against biofilm‑producing UPEC isolates and these
Weak 91 (21.5) 81 (20.9) drugs can serve as useful reserved drugs for the treatment of
Negative 222 (57.2) 134 (34.5) UTI. Understanding biofilms in UTIs will help clinicians in
Total 388 388 388 decision‑making toward effective treatment guidelines for
CRA: Congo Red Agar, TCP: Tissue culture plate recurrent UTI in this geographical region.

Table 2: Antibiotic sensitivity profile of biofilm‑forming and nonbiofilm‑producing Escherichia coli isolates
Antibiotic Biofilm producers (n=277) Nonbiofilm producers (n=111)
Number of isolates showing Number of isolates showing Number of isolates showing Number of isolates showing
resistance (%) sensitive (%) resistance (%) sensitive (%)
AMP 242 (87.36) 35 (12.2) 88 (79.3) 23 (20.7)
AK 32 (11.55) 245 (88.4) 10 (9.1) 101 (90.9)
AMC 215 (77.61) 62 (22.3) 62 (55.9) 49 (44.1)
AT 139 (50.18) 138 (49.8) 37 (44.4) 74 (66.6)
CTR 198 (71.48) 79 (28.5) 57 (51.4) 54 (48.6)
CXM 226 (81.58) 51 (18.4) 61 (55) 50 (55)
CPM 180 (64.98) 97 (35) 47 (42.4) 64 (57.6)
CIP 198 (71.48) 79 (28.5) 56 (50.5) 55 (49.5)
C 33 (11.91) 244 (88) 19 (13.2) 92 (82.8)
GEN 128 (46.2) 149 (53.7) 34 (30.7) 77 (69.3)
IPM 8 (2.88) 269 (97.1) 5 (4.6) 106 (95.4)
NIT 21 (7.58) 256 (96) 6 (5.4) 105 (94.5)
NX 134 (48.37) 143 (51.6) 42 (37.9) 69 (62.1)
PIT 6 (2.16) 271 (97.8) 18 (12.3) 93 (83.7)
AMP: Ampicillin, AK: Amikacin, AMC: Amoxicillin‑clavulanic acid, AT: Aztreonam, CTR: Ceftriaxone, CXM: Cefuroxime, CPM: Cefepime,
CIP: Ciprofloxacin, C: Chloramphenicol, GEN: Gentamicin, IPM: Imipenem, NIT: Nitrofurantoin, NX: Norfloxacin, PIT: Piperacillin‑tazobactam

Table 3: Association between antimicrobial resistance and biofilm‑forming uropathogenic Escherichia coli isolates
Biofilm formation Antimicrobial drugs
AMP (%) AK (%) AMC (%) AT (%) CTR (%) CXM (%) CPM (%) CIP (%) C (%) GEN (%)
TCP method
Strong 6.1 11.9 6.6 8.7 6 6.6 7.1 5.6 12.5 7
Moderate 22.7 38.1 25.3 25.4 26.3 24.5 26.2 25 35.7 32.4
Weak 71.2 50 68.1 65.9 67.7 69 66.7 69.4 51.8 68.8
P NS 0.002* 0.002* 0.009* 0.002* 0.010* 0.003* 0.020* 0.001* NS
*Significant at P<0.05. TCP: Tissue culture plate, AMP: Ampicillin, AK: Amikacin, AMC: Amoxicillin‑clavulanic acid, AT: Aztreonam, CTR: Ceftriaxone,
CXM: Cefuroxime, CPM: Cefepime, CIP: Ciprofloxacin, C: Chloramphenicol, GEN: Gentamicin, NS: Not significant

178 Journal of Natural Science, Biology and Medicine ¦ Volume 9 ¦ Issue 2 ¦ July-December 2018
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