o r i g i n a l c o m m u n i c a t i o n

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

Introduction

U
Background: An increase in resistance against many differ-
rinary tract infections (UTIs) have been report-
ent drugs among urinary tract infection (UTI) E coli isolates
ed to affect up to 150 million individuals annu-
has been observed in the last 2 decades. This study deter-
ally worldwide.1 They are the most common
mined the trends of antimicrobial resistance in E coli to com-
bacterial infection in women and account for signifi-
monly used antibiotics.
cant morbidity and health care costs.2 In the United
Methods: The study was conducted in Ile-Ife, southwest States, UTIs result in approximately 8 million physi-
Nigeria. Patients with features suggestive of UTI were inves- cian visits and more than 100 000 hospital admissions
tigated for presence of significant bacteriuria. Urine isolates per year3 with young, otherwise apparently healthy,
were identified. Antimicrobial susceptibility was evaluated in sexually active women being at highest risk for com-
accordance with standard bacteriological methods. munity-acquired UTIs. The main risk factors that have
Results: Of 442 urine specimens, 158 (35.8%) yielded signifi- been identified for this infection are sexual intercourse,
cant growth, including 41 (25.6%) with E coli. Among the E spermicide-based contraception, and a history of UTIs.4
coli isolates, antimicrobial susceptibility varied in prevalence Infections, including cystitis and pyelonephritis, are
by agent in descending order as follows: nitrofurantoin common both in community and hospital settings with
(80%), ofloxacin (24%), ciprofloxacin (15%), nalidixic acid Escherichia coli being the predominant pathogen. 5
(10%), cotrimoxazole (5%), and amoxicillin/clavulanic acid There is increasing evidence that some E coli strains
(2%). No isolate was susceptible to amoxicillin, gentamicin, that cause UTIs and other extraintestinal infections are
or tetracycline. All were also found to be resistant to at least responsible for community-wide epidemics.6-8
3 commonly used drugs. All 25 isolates tested for extended- Up to 95% of UTI cases, including even some of
spectrum ß-lactamase (ESBC) production were found to be those with severe symptoms, are treated without bacte-
presumptive ESBCs producers. riological investigation, with the empirically selected
antibiotic treatment varying according to the patient’s
Conclusion: The results demonstrate the continued suscep-
age, sex, and the infecting agent.9 A short course of tri-
tibility of E coli to nitrofurantoin and their widespread and
methoprim-sulfamethoxazole (cotrimoxazole) is the
increasing resistance to amoxicillin, gentamicin, cotrimoxa-
recommended empirical antimicrobial agent for treating
zole, ciprofloxacin, ofloxacin, and tetracycline. Nitrofuran-
acute uncomplicated bacterial cystitis in settings where
toin is a—and, in this locale, perhaps the only—rational drug
the prevalence of resistance to cotrimoxazole in E coli is
for empiric treatment of uncomplicated UTI. There is a need
less than 20%.2,3 However, the changing spectrum of
for a comprehensive study of the involvement of ESBC-pro-
microorganisms involved in UTIs and the emergence of
ducing E coli in UTI in this environment.
acquired microbial resistance dictate the need for con-
Keywords: urinary tract infection n bacteria n Nigeria tinuous surveillance to guide empirical therapy.10 This
being the case, the World Health Organization and the
J Natl Med Assoc. 2009;101:1268-1273 European Commission have recognized the importance
of studying the emergence and determinants of acquired
Author Affiliations: Department of Medical Microbiology and Parasitology, antimicrobial resistance and the need to devise appropri-
College of Health Sciences (Messers Aboderin and Odetoyin)and Depart-
ment of Pharmaceutics, Faculty of Pharmacy (Dr Lamikanra), Obafemi
ate strategies for their control.11 Over the last 2 decades,
Awolowo University, Ile-Ife, Osun-State, Nigeria; and Department of Medi- the proportion of community-acquired strains with
cal Microbiology and Parasitology, College of Health Sciences, Niger Delta resistance to first-line agents such as ampicillin, nitrofu-
University, Wilberforce Island, Bayelsa-State, Nigeria (Mr Abdu). rantoin, and cotrimoxazole have been shown to be on the
Corresponding Author: Adebayo Lamikanra, PhD, Department of Pharma- increase.12-15 More recently, resistance to fluoroquino-
ceutics, Faculty of Pharmacy, Obafemi Awolowo University, Ile-Ife, Osun-
State, Nigeria ([email protected]).
lones such as ciprofloxacin and levofloxacin has been on
the increase too,16,17 thus further complicating the man-

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 Resistance E coli in Urinary Tract Infection

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

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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
 Resistance E coli in Urinary Tract Infection

Results UTIs, accounting for 75% to 90% of UTIs as earlier

During the study period (September 2004 through observed in the Central African Republic (55.6%),33
April 2005), a total of 442 urine specimens were investi- Madagascar (67.2%),34 and Turkey (73.6%).35 However,
gated by microscopy, culture, and (if culture positive) sus- in agreement with the low recovery rate of E coli from
ceptibility testing to 9 antimicrobial agents. Nearly two- UTIs, the present result closely mirrors what was
thirds (ie, 284 [64.2%]) of the specimens were culture observed in the earlier study29 and 36% observed by
negative, whereas 158 (35.8%) yielded significant growth Kariuki et al36 in Nairobi, Kenya. Reasons that might
of 1 or more organisms, for a total of 160 isolates. Table 1 have been attributed to the observed variance may
shows the pathogens recovered. Of the 158 positive cul- include (1) differences in the study design and patient
tures, 152 (96%) yielded the growth of a single organism, selection, and (2) differing environmental conditions in
whereas 6 yielded 2 or more different pathogens. various study centers.
Of the 160 isolates, more than 60% were Enterobac- Antimicrobial resistance is recognized as an increas-
teriaceae, with Klebsiella spp being the most commonly ing global problem.37 In this study, all of the E coli iso-
isolated organism (49 [30.6%]). E coli (41 [25.6%]), lates were resistant to amoxicillin, gentamicin, and tetra-
whereas Proteus spp and other gram-negative bacteria cycline, while 95% were resistant to cotrimoxazole. To
(Pseudomonas spp) accounted for 13 (8.1%) and 18 our knowledge, this will be the highest report so far for
(11.3%), respectively. Only 27 (16.9%) of the isolates these agents. The prevalence of antibiotic resistances in
were gram positive, and all of these were identified as our study environment is considerably higher than what
Staphylococcus aureus. Candida albicans was isolated was reported within the same location in 1988 by Lami-
from 6 individuals. kanra and Ndep.29 Their observed resistance prevalences
Of the 41 patients from whom E coli was isolated, 23 were 85.9%, 72.6%, 68.7%, 21.1%, 18.7%, and 1.6% to
were male and 18 were female. The mean age of all the ampicillin, tetracycline, streptomycin, gentamicin,
patients was 47.7 years (range, 1-80 years). Twenty-two cephalotin, and nalidixic acid, respectively. Though
(10 males, 12 females) were hospitalized, while 19 (13 higher proportions of resistant strains have been reported
males, 6 females) were outpatients. Of the hospitalized in various parts of the developing world,34,38,39 none has
patients, 10 of 23 (43.5%) men and 12 of 18 (66.7%) reported resistance rates higher than what is now
women were identified in the study. reported for these agents and confirms the observation
As illustrated in Figure 1, the E coli isolates exhib- by Okeke, Fayinka, and Lamikanra28 that the prevalence
ited a high prevalence of resistance to the 9 antibiotics of antibiotic resistances within the study environment
tested except nitrofurantoin, to which 20% were resis- was increasing with time. The extensive multidrug anti-
tant. Overall, 8 patterns of antibiotic resistance were biotic resistance patterns to amoxicillin, amoxicillin-
observed among the E coli isolates, and further analysis clavulanic acid, fluoroquinolones, and trimethoprim-
revealed that 56% of them exhibited coresistance to as sulfamethoxazole observed among E coli clinical
many as 8 of the 9 drugs used in the study. The predomi- isolates in these studies, and the continuous increase in
nant resistance pattern is that which involved 8 antibiot- prevalence of infections caused by antibiotic-resistant E
ics—namely, amoxicillin, amoxicillin/clavulanic acid, coli makes the effective empirical treatment of UTIs dif-
ciprofloxacin, cotrimoxazole, gentamicin, nalidixic acid, ficult in these environments.9,40
ofloxacin, and tetracycline. Other resistance patterns are The prevalence of cotrimoxazole resistance among
illustrated in Table 2. All the isolates were resistant to at urinary E coli varies considerably among different geo-
least 3 different classes of antibiotics. graphical locations, with current estimates from devel-
We carried out presumptive ESBC detection tests on oped countries being 20% to 40%.4,5 In North America,
25 isolates, and all were found to be presumptive ESBC cotrimoxazole resistance ranges from 18% to 25%,40
producers. having increased from 7% to 9% in 1989-1992 to 17%
to 18% in 1995-1999.2 The 1998 SENTRY surveillance
DISCUSSION program, reporting on isolates of E coli collected from
This study demonstrates that E coli strains that are 26 US centers, found the overall prevalence of cotrimox-
simultaneously resistant to several antimicrobial agents azole to be 23.3%.2 In developing countries, especially
normally used in the empirical treatment of UTI are a those in Africa, rates of resistance are higher, being
prominent cause of UTI in Ile-Ife. Reports of other stud- 67%, 68.1%, 80%, and 85% in Sudan,38 Senegal, 39 Mad-
ies have shown that the vast majority of uncomplicated agascar, 34 and the Central African Republic,33 respec-
UTIs within the study environment and other environ- tively. In like manner, between 30% and 45% E coli iso-
ments are caused by E coli.29,33-35 In contrast, in the pres- lates in more developed countries are resistant to
ent study, Klebsiella spp outnumbered E coli for overall amoxicillin.5 This is in contrast to higher rates from the
prevalence, and other pathogens encountered. The recov- developing countries being 46% to 80%.34,36,39-40 The
ery rate of 25.6% E coli in our study is in contrast to pre- extensive use and easy availability of antimicrobial
vious reports that E coli is considered a major cause of drugs over the counter has been a contributing factor for

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 101, NO. 12, DECEMBER 2009 1271
Resistance E coli in Urinary Tract Infection

the high selection pressure for resistant bacteria.28,29,41 acknowledged, and all 25 isolates screened for ESBC
Reports of antimicrobial resistance trends in uro- production demonstrated the ability to produce ESBCs.
pathogenic E coli isolates from other countries raise the Although, this is the first report from our community,
specter of wider resistance to fluoroquinolones. Resis- community-associated ESBC-producing uropathogenic
tance to the fluoroquinolones (ofloxacin and ciprofloxa- E coli have previously been reported in other parts of the
cin) in this study was strikingly prevalent, at 76% and world.19,26,27,42
85%, respectively. Many studies worldwide have In the present study, nitrofurantoin was the only drug
reported a sharp increase in ciprofloxacin resistance that was found to be active against a majority of the E
among E coli isolates from UTIs. For example, a study coli isolates, the prevalence of resistance being only
in China revealed that the prevalence of ciprofloxacin 20%. It is thus, the only one of the study drugs that can
resistance increased steadily from 46.6% to 59.4%.9 In be regarded as being useful for the empirical treatment
Senegal,39 a significant increase of resistance to quino- of UTI in this environment. However, it is worth noting
lones was observed between 2004 and 2006, with cur- that this figure is still considerably higher than what has
rent estimates being 23.9% to nalidixic acid, 15.5% to been reported by Sire et al (10.1%),39 Arredondo-Garcia,
ciprofloxacin, and 16.4% to norfloxacin. In a recent and Amabile-Cuevas (7.4%).42 As the large majority of E
study conducted in Mexico, Arredondo-Garcia and coli isolates obtained in this study are resistant to cotri-
Amabile-Cuevas42 reported that 44% (11.4% intermedi- moxazole and fluoroquinolones, we suggest that nitrofu-
ate) of the organisms isolated were resistant to ciproflox- rantoin be an important alternative oral agent for the
acin. However, in sharp contrast to this, ciprofloxacin treatment of uncomplicated UTIs in Ile-Ife as earlier
remains very active in the United States and Canada, reported by Odetoyin et al.50
where the resistance prevalence has been reported as The primary factor responsible for the development
2%43 and 4%,4 respectively. The high prevalence of resis- and spread of bacterial resistance has been identified as
tance to the fluoroquinolones documented in the present the injudicious use of antimicrobial agents.51 Thus, strat-
study may be ascribed to high selective pressure preva- egies to improve prescription practices that use surveil-
lent in an environment in which antibiotics are freely lance data to rationally guide more judicious antibiotic
available without restriction.44 Furthermore, Davidson et use warrant consideration in this locality.
al45 had suggested that chloroquine might be an added
selective pressure for quinolones resistance. We think References
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