o r i g i n a l c o m m
Antimicrobial Resistance in Escherichia coli
Strains From Urinary Tract Infections
Oladipo A. Aboderin, FMCPath; Abdul-Rasheed Abdu, MSc; Babatunde W. Odetoyin, MSc;
Adebayo Lamikanra, PhD
Background: An increase in resistance against many differ-
ent drugs among urinary tract infection (UTI) E coli isolates
has been observed in the last 2 decades. This study deter-
mined the trends of antimicrobial resistance in E coli to com-
monly used antibiotics.
Methods: The study was conducted in Ile-Ife, southwest
Nigeria. Patients with features suggestive of UTI were inves-
tigated for presence of significant bacteriuria. Urine isolates
were identified. Antimicrobial susceptibility was evaluated in
accordance with standard bacteriological methods.
Results: Of 442 urine specimens, 158 (35.8%) yielded signifi-
cant growth, including 41 (25.6%) with E coli. Among the E
coli isolates, antimicrobial susceptibility varied in prevalence
by agent in descending order as follows: nitrofurantoin
(80%), ofloxacin (24%), ciprofloxacin (15%), nalidixic acid
(10%), cotrimoxazole (5%), and amoxicillin/clavulanic acid
(2%). No isolate was susceptible to amoxicillin, gentamicin,
or tetracycline. All were also found to be resistant to at least
3 commonly used drugs. All 25 isolates tested for extended-
spectrum ß-lactamase (ESBC) production were found to be
presumptive ESBCs producers.
Conclusion: The results demonstrate the continued suscep-
tibility of E coli to nitrofurantoin and their widespread and
increasing resistance to amoxicillin, gentamicin, cotrimoxa-
zole, ciprofloxacin, ofloxacin, and tetracycline. Nitrofuran-
toin is a—and, in this locale, perhaps the only—rational drug
for empiric treatment of uncomplicated UTI. There is a need
for a comprehensive study of the involvement of ESBC-pro-
ducing E coli in UTI in this environment.
Keywords: urinary tract infection n bacteria n Nigeria
J Natl Med Assoc. 2009;101:1268-1273
Author Affiliations: Department of Medical Microbiology and Parasitology,
College of Health Sciences (Messers Aboderin and Odetoyin)and Depart-
ment of Pharmaceutics, Faculty of Pharmacy (Dr Lamikanra), Obafemi
Awolowo University, Ile-Ife, Osun-State, Nigeria; and Department of Medi-
cal Microbiology and Parasitology, College of Health Sciences, Niger Delta
University, Wilberforce Island, Bayelsa-State, Nigeria (Mr Abdu).
Corresponding Author: Adebayo Lamikanra, PhD, Department of Pharma-
ceutics, Faculty of Pharmacy, Obafemi Awolowo University, Ile-Ife, Osun-
State, Nigeria (alamikanra@yahoo.com).
1268 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
u n i c a t i o n
Introduction
U
rinary tract infections (UTIs) have been report-
ed to affect up to 150 million individuals annu-
ally worldwide.1 They are the most common
bacterial infection in women and account for signifi-
cant morbidity and health care costs.2 In the United
States, UTIs result in approximately 8 million physi-
cian visits and more than 100 000 hospital admissions
per year3 with young, otherwise apparently healthy,
sexually active women being at highest risk for com-
munity-acquired UTIs. The main risk factors that have
been identified for this infection are sexual intercourse,
spermicide-based contraception, and a history of UTIs.4
Infections, including cystitis and pyelonephritis, are
common both in community and hospital settings with
Escherichia coli being the predominant pathogen. 5
There is increasing evidence that some E coli strains
that cause UTIs and other extraintestinal infections are
responsible for community-wide epidemics.6-8
Up to 95% of UTI cases, including even some of
those with severe symptoms, are treated without bacte-
riological investigation, with the empirically selected
antibiotic treatment varying according to the patient’s
age, sex, and the infecting agent.9 A short course of tri-
methoprim-sulfamethoxazole (cotrimoxazole) is the
recommended empirical antimicrobial agent for treating
acute uncomplicated bacterial cystitis in settings where
the prevalence of resistance to cotrimoxazole in E coli is
less than 20%.2,3 However, the changing spectrum of
microorganisms involved in UTIs and the emergence of
acquired microbial resistance dictate the need for con-
tinuous surveillance to guide empirical therapy.10 This
being the case, the World Health Organization and the
European Commission have recognized the importance
of studying the emergence and determinants of acquired
antimicrobial resistance and the need to devise appropri-
ate strategies for their control.11 Over the last 2 decades,
the proportion of community-acquired strains with
resistance to first-line agents such as ampicillin, nitrofu-
rantoin, and cotrimoxazole have been shown to be on the
increase.12-15 More recently, resistance to fluoroquino-
lones such as ciprofloxacin and levofloxacin has been on
the increase too,16,17 thus further complicating the man-
VOL. 101, NO. 12, DECEMBER 2009
 Resistance E coli in Urinary Tract Infection

agement of these infections.
Recent studies indicate that UTIs caused by extended-
spectrum ß-lactamase (ESBC)-producing E coli consti-
tute an emerging problem in outpatient settings in vari-
ous parts of the world.18,19 Possible community acquisition
of ESBCs-producing E coli was first reported in 1998,
when a nalidixic acid-resistant uropathogenic E coli pro-
ducing an ESBC was isolated from an elderly patient
who did not have a recent history of hospitalization in
Ireland.20 Since then, ESBC-producing E coli have been
increasingly reported in different communities.21-27
It is imperative that the prevalence of antimicrobial
resistance in organisms associated with UTI be the sub-
ject of regular study and that these studies be performed
at different geographic locations.28 Since the most recent
such work from Ile-Ife (a semiurban community in
southwest Nigeria) was published in 1988,29 we sought
to define the current trends of antimicrobial resistance in
our region. Moreover, since ESBC-producing strains
have emerged in other parts of the world in the interven-
ing period, we evaluated ESBC production in some of
the strains isolated.
Materials and Methods
Patients
All the patients recruited presented at the various
departments (outpatient clinics and wards) of the Ife
State Hospital unit of the Obafemi Awolowo University
Teaching Hospitals Complex (OAUTHC) between Sep-
tember 2004 and April 2005. They all complained of
symptoms associated with UTI and were thus referred to
the medical microbiology laboratory for investigation.
Sociodemographic information, including age, sex, and
status regarding hospitalization was obtained from each
patient. Mid-stream urine specimens were collected
from each of the patients into sterile bottles (Sterilin,
England) and immediately processed appropriately.
Bacterial Strains
Urine microscopy, isolation and identification of
organisms were carried out as part of the routine proce-
dures in the diagnostic microbiology laboratory of OAU-
THC, and cultures with a colony count of ≥105 colony-
forming unit (CFU/mL) were considered significant for
inclusion. Briefly, a semiquantitative technique was per-
formed by inoculating the urine specimens on a well-
dried cystine-lactose-electrolyte-deficient medium. The
plates were incubated overnight aerobically at 37ºC. The
identities of all the isolates with significant growth (≥105
CFU/mL) were determined by employing standard
microbiological techniques.30 Isolates that were gram
negative, lactose positive, indole positive, and citrate
negative were defined as E coli and were stored in tryp-
tone soya agar.
Antimicrobial Susceptibility Testing
Susceptibility to 9 antimicrobial agents was tested by
the disc diffusion technique according to the guidelines
by the Clinical and Laboratory Standards Institute
(CLSI, formerly National Committee for Clinical Labo-
ratory Standards).31 The antibiotic discs used were amox-
icillin, 25 μg; amoxicillin/clavulanic acid, 30 μg; cipro-
floxacin, 5 μg; cotrimoxazole, 25 μg; gentamicin, 10 μg;
nalidixic acid, 10 μg; nitrofurantoin, 300 μg; ofloxacin, 5
μg; and tetracycline, 30 μg (Remel, Lenexa, Kansas).
The discs were placed on to the surface of the agar by an
autodispenser (Remel) that is capable of placing 8 discs
equidistantly close to the periphery of the plate, leaving
the center for the ninth disc. Inhibition zone diameters
were measured to the nearest millimeter, and isolates
were classified as susceptible, intermediate, or resistant
according to CLSI-specified interpretive criteria.31 Inter-
mediate and resistant strains were further grouped
together in the resistant group for analysis. E coli K12
C600 was used as the control strain.
Extended-Spectrum
ß-Lactamase Tests
ESBC production was detected by disk diffusion
technique as described by CLSI.32 In brief, the test plates
were inoculated as for a standard disk diffusion test.
Disks containing expanded-spectrum cephalosporins
(ceftazidime, 30 μg; cefotaxime, 30μg) were then
applied. After overnight incubation at 37ºC, the pre-
sumptive production of ESBCs was detected by the

Table 1. Pathogens Recovered From 158 Urine Samples During the Period September 2004 to April 2005

Organism Category Specific Organism (Any Species) No. of Isolates (% of 160)

Gram-negative bacilli 121 (75%)
Klebsiella spp 49 (30.6)
Escherichia coli 41 (25.6)
Pseudomonas aeruginosa 18 (11.3)
Proteus spp 13 (8.1)
Gram-positive cocci Staphylococcus aureus 27 (16.9)
Yeast Candida spp 6 (3.8)
Other Mixed growth 6 (3.8)

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 101, NO. 12, DECEMBER 2009 1269
Resistance E coli in Urinary Tract Infection

presence of inhibition zones ≤22 mm and ≤27 mm for Data Handling

ceftazidime and cefotaxime, respectively. All data were entered into a Microsoft Excel data-
base (Microsoft Corp, Redmond, Washington). Data
obtained were analyzed using descriptive statistics.

Figure 1. Antimicrobial Resistance Patterns of Urinary Tract Infection E Coli

Abbreviations: AMX, amoxicillin; AUG, amoxicillin/clavulanic acid; CIP, ciprofloxacin; COT, cotrimoxazole; GEN, gentamicin; NAL,
nalidixic acid; NIT, nitrofurantoin; OFL, ofloxacin; TET, tetracycline.

Table 2. Antibiotic Resistance Patterns of 41 E coli Isolates

Resistance Pattern No. of Isolates (% of 41)

Resistance to 4 antibiotics
Amx Cot Gen Tet 1 (2.4%)
Amx Aug Gen Tet 1 (2.4)
Resistance to 5 antibiotics
Amx Aug Cot Gen Tet 2 (4.9)
Resistance to 6 antibiotics
Amx Aug Cot Gen Nal Tet 2 (4.9)
Resistance to 7 antibiotics
Amx Aug Cip Cot Gen Nal Tet 5 (12.2)
Amx Aug Cip Gen Nal Ofl Tet 1 (2.4)
Resistance to 8 antibiotics
Amx Aug Cip Cot Gen Nal Ofl Tet 23 (56.1)
Resistance to 9 antibiotics
Amx Aug Cip Cot Gen Nal Nit Ofl Tet 6 (14.6)
Abbreviations: AMX, amoxicillin; AUG, amoxicillin/clavulanic acid; CIP, ciprofloxacin; COT, cotrimoxazole; GEN, gentamicin; NAL,
nalidixic acid; NIT, nitrofurantoin; OFL, ofloxacin; TET, tetracycline.

1270 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 101, NO. 12, DECEMBER 2009

Results
During the study period (September 2004 through
April 2005), a total of 442 urine specimens were investi-
gated by microscopy, culture, and (if culture positive) sus-
ceptibility testing to 9 antimicrobial agents. Nearly two-
thirds (ie, 284 [64.2%]) of the specimens were culture
negative, whereas 158 (35.8%) yielded significant growth
of 1 or more organisms, for a total of 160 isolates. Table 1
shows the pathogens recovered. Of the 158 positive cul-
tures, 152 (96%) yielded the growth of a single organism,
whereas 6 yielded 2 or more different pathogens.
Of the 160 isolates, more than 60% were Enterobac-
teriaceae, with Klebsiella spp being the most commonly
isolated organism (49 [30.6%]). E coli (41 [25.6%]),
whereas Proteus spp and other gram-negative bacteria
(Pseudomonas spp) accounted for 13 (8.1%) and 18
(11.3%), respectively. Only 27 (16.9%) of the isolates
were gram positive, and all of these were identified as
Staphylococcus aureus. Candida albicans was isolated
from 6 individuals.
Of the 41 patients from whom E coli was isolated, 23
were male and 18 were female. The mean age of all the
patients was 47.7 years (range, 1-80 years). Twenty-two
(10 males, 12 females) were hospitalized, while 19 (13
males, 6 females) were outpatients. Of the hospitalized
patients, 10 of 23 (43.5%) men and 12 of 18 (66.7%)
women were identified in the study.
As illustrated in Figure 1, the E coli isolates exhib-
ited a high prevalence of resistance to the 9 antibiotics
tested except nitrofurantoin, to which 20% were resis-
tant. Overall, 8 patterns of antibiotic resistance were
observed among the E coli isolates, and further analysis
revealed that 56% of them exhibited coresistance to as
many as 8 of the 9 drugs used in the study. The predomi-
nant resistance pattern is that which involved 8 antibiot-
ics—namely, amoxicillin, amoxicillin/clavulanic acid,
ciprofloxacin, cotrimoxazole, gentamicin, nalidixic acid,
ofloxacin, and tetracycline. Other resistance patterns are
illustrated in Table 2. All the isolates were resistant to at
least 3 different classes of antibiotics.
We carried out presumptive ESBC detection tests on
25 isolates, and all were found to be presumptive ESBC
producers.
DISCUSSION
This study demonstrates that E coli strains that are
simultaneously resistant to several antimicrobial agents
normally used in the empirical treatment of UTI are a
prominent cause of UTI in Ile-Ife. Reports of other stud-
ies have shown that the vast majority of uncomplicated
UTIs within the study environment and other environ-
ments are caused by E coli.29,33-35 In contrast, in the pres-
ent study, Klebsiella spp outnumbered E coli for overall
prevalence, and other pathogens encountered. The recov-
ery rate of 25.6% E coli in our study is in contrast to pre-
vious reports that E coli is considered a major cause of
JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
Resistance E coli in Urinary Tract Infection
UTIs, accounting for 75% to 90% of UTIs as earlier
observed in the Central African Republic (55.6%),33
Madagascar (67.2%),34 and Turkey (73.6%).35 However,
in agreement with the low recovery rate of E coli from
UTIs, the present result closely mirrors what was
observed in the earlier study29 and 36% observed by
Kariuki et al36 in Nairobi, Kenya. Reasons that might
have been attributed to the observed variance may
include (1) differences in the study design and patient
selection, and (2) differing environmental conditions in
various study centers.
Antimicrobial resistance is recognized as an increas-
ing global problem.37 In this study, all of the E coli iso-
lates were resistant to amoxicillin, gentamicin, and tetra-
cycline, while 95% were resistant to cotrimoxazole. To
our knowledge, this will be the highest report so far for
these agents. The prevalence of antibiotic resistances in
our study environment is considerably higher than what
was reported within the same location in 1988 by Lami-
kanra and Ndep.29 Their observed resistance prevalences
were 85.9%, 72.6%, 68.7%, 21.1%, 18.7%, and 1.6% to
ampicillin, tetracycline, streptomycin, gentamicin,
cephalotin, and nalidixic acid, respectively. Though
higher proportions of resistant strains have been reported
in various parts of the developing world,34,38,39 none has
reported resistance rates higher than what is now
reported for these agents and confirms the observation
by Okeke, Fayinka, and Lamikanra28 that the prevalence
of antibiotic resistances within the study environment
was increasing with time. The extensive multidrug anti-
biotic resistance patterns to amoxicillin, amoxicillin-
clavulanic acid, fluoroquinolones, and trimethoprim-
sulfamethoxazole observed among E coli clinical
isolates in these studies, and the continuous increase in
prevalence of infections caused by antibiotic-resistant E
coli makes the effective empirical treatment of UTIs dif-
ficult in these environments.9,40
The prevalence of cotrimoxazole resistance among
urinary E coli varies considerably among different geo-
graphical locations, with current estimates from devel-
oped countries being 20% to 40%.4,5 In North America,
cotrimoxazole resistance ranges from 18% to 25%,40
having increased from 7% to 9% in 1989-1992 to 17%
to 18% in 1995-1999.2 The 1998 SENTRY surveillance
program, reporting on isolates of E coli collected from
26 US centers, found the overall prevalence of cotrimox-
azole to be 23.3%.2 In developing countries, especially
those in Africa, rates of resistance are higher, being
67%, 68.1%, 80%, and 85% in Sudan,38 Senegal, 39 Mad-
agascar, 34 and the Central African Republic,33 respec-
tively. In like manner, between 30% and 45% E coli iso-
lates in more developed countries are resistant to
amoxicillin.5 This is in contrast to higher rates from the
developing countries being 46% to 80%.34,36,39-40 The
extensive use and easy availability of antimicrobial
drugs over the counter has been a contributing factor for
VOL. 101, NO. 12, DECEMBER 2009 1271
Resistance E coli in Urinary Tract Infection
the high selection pressure for resistant bacteria.28,29,41
Reports of antimicrobial resistance trends in uro-
pathogenic E coli isolates from other countries raise the
specter of wider resistance to fluoroquinolones. Resis-
tance to the fluoroquinolones (ofloxacin and ciprofloxa-
cin) in this study was strikingly prevalent, at 76% and
85%, respectively. Many studies worldwide have
reported a sharp increase in ciprofloxacin resistance
among E coli isolates from UTIs. For example, a study
in China revealed that the prevalence of ciprofloxacin
resistance increased steadily from 46.6% to 59.4%.9 In
Senegal,39 a significant increase of resistance to quino-
lones was observed between 2004 and 2006, with cur-
rent estimates being 23.9% to nalidixic acid, 15.5% to
ciprofloxacin, and 16.4% to norfloxacin. In a recent
study conducted in Mexico, Arredondo-Garcia and
Amabile-Cuevas42 reported that 44% (11.4% intermedi-
ate) of the organisms isolated were resistant to ciproflox-
acin. However, in sharp contrast to this, ciprofloxacin
remains very active in the United States and Canada,
where the resistance prevalence has been reported as
2%43 and 4%,4 respectively. The high prevalence of resis-
tance to the fluoroquinolones documented in the present
study may be ascribed to high selective pressure preva-
lent in an environment in which antibiotics are freely
available without restriction.44 Furthermore, Davidson et
al45 had suggested that chloroquine might be an added
selective pressure for quinolones resistance. We think
this claim could be relevant in our situation, as chloro-
quine was the cheapest and most widely used antimalar-
ial drug in our environment. In addition, the observed
resistant pattern results may also be attributable to a pre-
vious hypothesis that fluoroquinolone-resistant E coli
encountered in humans are likely transmitted from live-
stock, rather than having originated in humans by con-
version of susceptible human intestinal E coli to resis-
tant E coli under selective pressure from medical
fluoroquinolone use.46-48 These enormous differences
may be the result of administering antimicrobials in
poultry production.49
Unlike what has been observed in other parts of the
world11,35,39 and indeed what was observed in an earlier
study in this locality in which only 21%29 of the organ-
isms tested were found to be resistant to gentamicin, all
the isolates obtained in the course of the present study
were found to be resistant to this agent. This is not in
agreement with the reports observed in different parts of
the world.11,35,39 This observation suggests that there is
widespread use in this environment of gentamicin, an
injectable antibiotic, and further suggests that conditions
conducive to the spread of ESBC-producing organisms
are present within the study environment, since resis-
tance to gentamicin in E coli has been associated with
strains that have the capacity to produce ESBC.11,35
Because of the resistance of these isolates to several anti-
biotics, the need to perform an ESBC screening test was
1272 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
acknowledged, and all 25 isolates screened for ESBC
production demonstrated the ability to produce ESBCs.
Although, this is the first report from our community,
community-associated ESBC-producing uropathogenic
E coli have previously been reported in other parts of the
world.19,26,27,42
In the present study, nitrofurantoin was the only drug
that was found to be active against a majority of the E
coli isolates, the prevalence of resistance being only
20%. It is thus, the only one of the study drugs that can
be regarded as being useful for the empirical treatment
of UTI in this environment. However, it is worth noting
that this figure is still considerably higher than what has
been reported by Sire et al (10.1%),39 Arredondo-Garcia,
and Amabile-Cuevas (7.4%).42 As the large majority of E
coli isolates obtained in this study are resistant to cotri-
moxazole and fluoroquinolones, we suggest that nitrofu-
rantoin be an important alternative oral agent for the
treatment of uncomplicated UTIs in Ile-Ife as earlier
reported by Odetoyin et al.50
The primary factor responsible for the development
and spread of bacterial resistance has been identified as
the injudicious use of antimicrobial agents.51 Thus, strat-
egies to improve prescription practices that use surveil-
lance data to rationally guide more judicious antibiotic
use warrant consideration in this locality.
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