Original Article

Uropathogens and their antimicrobial resistance

patterns: Relationship with urinary tract infections
Syed Suhail Ahmed, ABSTRACT
Ali Shariq,
Abdulaziz Ajlan Alsalloom, Objectives: This study was performed to determine the prevalence of uropathogens
causing urinary tract infections (UTIs) and to determine their pattern of antimicrobial
Ibrahim H. Babikir, resistance.
Badr N. Alhomoud
Department of Pathology and Laboratory Methods: This study was conducted on 273 urine samples collected from outpatient
Medicine, College of Medicine, Qassim departments (OPDs) of Qassim University affiliated hospitals. Fully automated VITEK
University, Saudi Arabia 2 compact system was used in the identification and antimicrobial susceptibility testing
Address for correspondence: of causative microorganisms.
Dr. Syed Suhail Ahmed, Department of
Pathology and Laboratory Medicine, College Results: Of 273 urine samples, only 89 (32.6%) were found to show significant
of Medicine, Outpatient Department, Qassim growth for UTI, and overall, drug resistance was found in 92% (n = 82/89) of
University, Saudi Arabia.
E-mail: suhailahmed@qumed.edu.sa samples, with most (80%) being resistant to at least two drugs. Antibiotic resistance
was commonly observed in ampicillin (88.3%), piperacillin (72.7%), clindamycin
(66.7%), amoxicillin/clavulanic acid (66.2%), and trimethoprim/sulfamethoxazole
(50%). The commonly isolated microorganisms were Escherichia coli 24 (27%),
Klebsiella pneumoniae 11 (12.4%), Proteus mirabilis 4 (4.5%), Pseudomonas
aeruginosa 4 (4.5%), Enterobacter cloacae 5 (5.6%), Enterococcus faecalis 5 (5.6%),
and Staphylococcus saprophyticus 3 (3.4%).

Conclusions: This research work has shown that patients with UTI in Qassim are
at high risk of antibiotic resistance. The work also showed that multidrug-resistant
bacteria can lead to momentous therapeutic problems in OPD patients.

WEBSITE: ijhs.org.sa
ISSN: 1658-3639 Keywords: Antimicrobial resistance, Escherichia coli, Klebsiella, multidrug
PUBLISHER: Qassim University resistance, Pseudomonas aeruginosa, qassim, uropathogens, VITEK system

Introduction Klebsiella species, Enterobacter species, and Citrobacter

species. Among Gram-positive bacteria, Staphylococcus
Urinary tract infection (UTI) is a common health problem in saprophyticus, Enterococcus species, and Coagulase-negative
both community and nosocomial settings. UTI is among one of Staphylococcus are common predictable spectrum of bacteria
the most common infections occurring particularly in women. which are responsible for causing UTIs.[4,5]
As reported by the National Ambulatory Medical Care Survey,
UTI alone is responsible for nearly seven million patient visits As compared to non-pathogenic bacteria, the bacteria which are
in outpatient department (OPD) as well as up to one million responsible for causing UTIs have more aggressive virulence
visits in hospital emergency department, resulting in about factors which enhance their host cell attachment, colonization
100,000 hospitalizations.[1] Nearly 50–60% of all women suffer as well as invasion abilities. These bacteria avoid evasion of the
from an episode of UTI at least once in their lifetime.[2] If the immune system of host by the help of certain virulence factors
predisposing factors which are responsible for the occurrence which may be comprised of various cellular components such
of UTI are not timely diagnosed and treated, then it is also as pili, capsule, lipopolysaccharides, and various other cell
common for UTI episodes to reoccur.[3] Untreated UTI can result surface structures.[4] Certain human anatomical as well as
in serious complications such as kidney damage, renal scarring, physiological factors are also responsible for increasing the
and renal failure. UTI is commonly caused by bacteria mostly incidence of UTI, for example, length of the urethra is shorter
by Gram-negative bacteria such as Escherichia coli, Proteus in females as compared to males which leads to an increased
species, Pseudomonas aeruginosa, Acinetobacter species, chance of acquiring UTI. Similarly, incomplete emptying

International Journal of Health Sciences 48

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

of bladder particularly in old age results in accumulation of Measurements

residual urine remaining in the bladder and vesicoureteral
Colony count method is a technique by which the number
reflux which frequently occurs among pregnant women which
of viable bacterial colonies can be counted numerically in
is the vital factors that can predispose host to UTIs.[6]
milliliter of urine sample; it is a quantitative measurement
by which we can differentiate true bacteriuria from bacterial
UTI is treated often by broad-spectrum antibiotics, and
contamination that often occurs during improper collection of
treatment is started empirically without performing culture
mid-stream or “clean-catch” urine.[11] UTI occurs when there
and sensitivity. This inappropriate and non-judicious usage
is a presence of >105 colony-forming units (CFUs)/ml of mid-
of antibiotics has resulted in the development of worldwide
stream urine, which is diagnostic. UTI was defined as urine
antibiotic resistance in bacteria, leading to the emergence of
culture plates growing bacterial colonies of ≥105 CFU/mL in
multiresistant strains of bacterial pathogens.[7] According to a mid-stream urine sample.[11,12]
a survey conducted by the European Survey of Antibiotic
Consumption, multidrug-resistant (MDR) bacterial strains
Collection and process of urine samples
were accountable for a mortality rate nearly about 25,000
Europeans/year usually due to complications of UTIs.[8] Hence, Mid-stream urine samples were collected in a sterile container
it is necessary to circumvent non-judicious use of antibiotics and were processed within 2 h of collection time. Urine sample
that lead to the emergence of antimicrobial resistance and was inoculated on a standard culture media Cystine–Lactose–
most appropriate antibiotics should be opted for first-choice Electrolyte-Deficient (CLED) agar, using a calibrated (1 μL)
empiric treatment of UTI. The antimicrobial susceptibility loop. Culture plates were incubated at 35–37°C ambient air
pattern among bacteria varies from country to country.[9] The incubator for 18 h. After the allocated time period, the culture
Infectious Diseases Society of America recommends that plates were visualized for the presence of bacterial colonies.
regional surveillance should be conducted to monitor changes They were reported as significant or non-significant growth
in susceptibility of uropathogens in specific regions.[10] on the basis of colony count method. These urine samples
were also centrifuged, and urine sediment was used for
The main aim of this study was to determine the prevalence of direct microscopic examination of red blood cells (RBCs),
UTI causing pathogens according to age and sex at a medical leukocytes, epithelial cell, casts, crystals, and parasites. In
college hospital among OPD and their antibiotic susceptibility the normal urine sediment, a few count of RBCs, pus cells
pattern to provide a database for reference. Keeping this study (0–5/high power field), and epithelial cells may present.
in view, insufficient research work has been published on this Epithelial cell count reported as “few,” “moderate,” or “many”
particular topic. per low-power field.

In the current scenario, where the antimicrobial resistance Bacterial identification and susceptibility testing
pattern is changing very alarmingly and new MDR bacteria The identification and antimicrobial susceptibility of bacteria
are emerging frequently leading to enhance morbidity and isolated from urine samples were performed by VITEK 2
mortality. This study focuses on highlighting the guidelines Compact System. Initially, the urine samples are cultured
for the usage of appropriate antibiotics which can be used on CLED agar and were incubated at ambient temperature
in treating UTI. In addition, our study will assist concerned 35–37°C in 5% CO2, after 18 h of incubation; the bacterial
authorities in preparing antibiotic prescription policies and growth was preliminary identified by their colony morphology
evaluating their antibiotic formulary guidelines. Increase as well as gram staining. The culture plates showing growth
awareness and annual reporting for these findings will help of significant bacterial colonies were used to formulate a
in preventing the immerged strains from spread within the standardized saline inoculum recommended for VITEK
community. identification. For the identification of bacteria through
VITEK, we used special ID: Gram-negative ID card (GN
Methods Reference 21 341) and Gram-positive ID card (GP Reference
21 342).
Study design and setting
The antimicrobial susceptibility tests (AST) and the minimum
This is a cross-sectional study, and the retrospective analysis inhibitory concentrations were determined by special
was carried out at the College of Medicine OPD in Buraydah, sensitivity (AST) cards. Clinical and Laboratory Standards
Qassim area, Saudi Arabia. We included all urine sample results Institute criteria were used for the interpretation of AST results
submitted for urine culture and sensitivity in this study. We as per manufacturer’s instructions (BioMérieux, France) and
enrolled a total of 273 urine samples. The identification and the Advanced Expert System.
susceptibility of causative microorganisms were performed by
VITEK 2 compact system. Ethical approval was taken from Isolated Gram-negative uropathogens were tested against
the ethical committee of the Ministry of Health, KSA (Ethical different AST-N panels including ampicillin, cefepime,
approval number #20180314). norfloxacin, cefoxitin, amoxicillin/clavulanic acid, piperacillin,

49 International Journal of Health Sciences

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

piperacillin/tazobactam, cefalotin, amikacin, tobramycin, samples were showing significant growth for UTI, among
cefuroxime, cefuroxime, cefpodoxime, cefotaxime, whom, the females were 65 (73%) episodes. The average
meropenem, ceftazidime, nitrofurantoin, trimethoprim/ age (±SD) was 35.82±15.3 years. Frequency of gender
sulfamethoxazole, ciprofloxacin, and gentamicin [Figure 1]. distribution of UTI cases admitted to OPD of Qassim
University medical clinics, Buraydah, Qassim, Saudi Arabia
Whereas, Gram-positive uropathogens were tested against are summarized in Table 1.
AST-P which include benzylpenicillin, erythromycin,
tetracycline, oxacillin, moxifloxacin, trimethoprim/ The most common Gram-negative urinary pathogens isolated
sulfamethoxazole, cefalotin screen, gentamicin, tobramycin, were E. coli, Klebsiella pneumoniae, Proteus mirabilis,
levofloxacin, clindamycin, inducible clindamycin resistance, P. aeruginosa, Enterobacter cloacae, Enterobacter aerogenes,
linezolid, teicoplanin, vancomycin, fosfomycin, and and Morganella morganii [Table 2]. The frequency of
nitrofurantoin [Figure 1]. Acinetobacter, Citrobacter, and Pantoea agglomerans is
mentioned in Table 4 due to their clinical relevance.
Data collection and statistical analysis
The number (percentage) of common Gram-negative urinary
A structured questionnaire was designed to collect the
pathogens resistant (R) to antimicrobial agents is shown in
demographic and clinical data of the patients. On arrival of a
Table 2. The common urinary pathogens such as E. coli,
patient in the OPD, gender, age, medical history as well as vital
K. pneumoniae, and P. mirabilis showed high resistance
signs were noted. We performed descriptive statistical methods
when they were tested against amoxicillin/clavulanic acid
for the data analysis. The antimicrobial resistance prevalence
(66.2) and piperacillin (72.7). In comparison, low resistance
was calculated as the proportion of positive results over the
rates were found against cefoxitin, cefpodoxime, ceftazidime,
entire study sample. Those bacteria which showed resistance
meropenem, and amikacin [Table 2]. E. coli showed a
to two antimicrobial agents of different class of antibiotics
relatively low rate of resistance to nitrofurantoin (8.3% of
were termed as MDR.
the isolates) when compared with K. pneumoniae isolates
(90.9%), and only 4.2% of E. coli isolates were resistant
Data analysis was performed using SPSS software. Statistical
to gentamicin. In contrast, K. pneumoniae showed an 27%
tests of significance were performed using the Student’s t-test
resistance rates.
and Chi-square (χ2) test, and variables were compared using
cross-tabulation statistical methods. P < 0.05 was considered
statistically significant. Multiple resistances
Antimicrobial resistance was seen both in Gram-positive
Results and Gram-negative bacteria. Multiple resistances were high
among the isolated urinary pathogens. Particularly, E. coli
A total of 273 urine samples have been received in the had a ˃50% resistance rate to at least five of 20 antimicrobial
Microbiology Laboratory, College of Medicine OPD in agents [Table 3], while K. pneumoniae and P. mirabilis had
Qassim University, Saudi Arabia. Only 89 (32.6%) urine ˂50% and ˂30% resistance rates, respectively.

Figure 1: Frequency distribution of isolated microorganisms from patients with catheter-associated urinary tract infection

International Journal of Health Sciences 50

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

Discussion as it affects people all over the globe. Based on the results of the
urinary samples at the College of Medicine OPD in Buraidah,
UTI is listed among one of the most common infections caused Qassim area, Saudi Arabia, we have shown that approximately
by various Gram-positive and Gram-negative bacteria.[13] To 92% (n = 82/89) of samples were resistant to antibiotic drugs
successfully treat the patients who are suffering from UTI, it and ~80% (n = 72) were MDR.
is crucial to accurately identify the causative pathogen. Failure
to do so will not only prolong the disease and will render In our research study, the ratio of female patients with UTI
the patient to complications but will also promote negative was more than the males. This was inconsistent with the study
consequences of bacterial resistance due to a non-judicious by Kattel et al.[14] Higher prevalence of UTI among females is
use of inappropriate antibiotics. It is onerous to precisely due to various factors that predispose women to UTI.[15] The
measure the incidence and prevalence of UTIs because it is most prevalent urinary tract pathogen in both the genders in
not a reportable disease within Saudi Arabia. In addition, the our study was E. coli and K. pneumoniae in concordance with
diagnosis of UTI is dependent on both the presence of clinical other studies from Saudi Arabia conducted by Ahmed et al.
signs and symptoms along with a positive urine culture; and Al-Tawfiq and Anani.[16,17]
however, in majority of health-care settings on the scene, this
diagnosis is accomplished and treatment is started without In comparison to previous studies related to UTI since 1995,
performing the culture and antimicrobial sensitivity. the prevalence rate of UTIs and the antibiotic resistance pattern
in the Qassim area have enhanced over the past 20 years.[18]
The emergence of antimicrobial resistance is a global problem For example, in our study, the prevalence rate of UTI by
urinary pathogens is concluded to be 32%, and these results
Table 1: Frequency of gender distribution of UTI cases admitted are slightly higher than a study by Ahmad S, 1995 conducted
to OPD of Qassim University medical clinics, Buraydah, Qassim, in King Fahad Specialist Hospital in Buraidah, Qassim area,
Saudi Arabia, 2014
Saudi Arabia, who concluded a prevalence of 20.54%.[18]
Variables Frequency (%) Furthermore, we found that the distribution of the common
Female 65 (73) pathogens was slightly different from previous studies in
Male 24 (27) the same area. As shown in Table 4, the common isolated
Total 89 (100) pathogens were E. coli which was the most common organism
OPD: Outpatient department, UTI: Urinary tract infection (50.11%), followed by Klebsiella spp. (28.33%), Pseudomonas

Table 2: Number (%) of common Gram‑negative urinary pathogens resistant (R) to antimicrobial agents
Variables Escherichia Klebsiella Proteus Pseudomonas Enterobacter Enterobacter Morganella
coli pneumoniae mirabilis aeruginosa cloacae aerogenes morganii
Ampicillin 22 (91.7) 11 (100) 3 (75) IR IR IR IR
Amoxicillin/clavulanic acid 13 (54.2) 7 (63.6) 1 (25) IR IR IR IR
Piperacillin 21 (87.5) 10 (90.9) 1 (25) 4 (100) 3 (60) 3 (100) 3 (75)
Piperacillin/tazobactam 8 (33.3) 4 (36.4) 1 (25) 4 (100) 3 (60) 1 (33.3) 3 (75)
Cefalotin 17 (70.8) 4 (36.4) 2 (50) IR IR IR IR
Cefuroxime 6 (25) 3 (27.3) 2 (50) IR IR IR IR
Cefoxitin 2 (8.3) 1 (9.1) 1 (25) IR IR IR IR
Cefpodoxime 2 (8.3) 2 (18.2) 1 (25) IR IR IR IR
Cefotaxime 1 (4.2) 2 (18.2) 1 (25) IR 3 (60) 0 (0.0) 3 (75)
Ceftazidime 2 (8.3) 2 (18.2) 1 (25) 4 (100) 3 (60) 0 (0.0) 4 (100)
Cefepime 2 (8.3) 2 (18.2) 1 (25) 3 (75) 3 (60) 0 (0.0) 3 (75)
Meropenem 1 (4.2) 0 (0.0) 0 (0.0) 2 (50) 0 (0.0) 0 (0.0) 0 (0.0)
Amikacin 4 (16.7) 3 (27.3) 0 (0.0) 1 (25) 1 (20) 0 (0.0) 1 (25)
Gentamicin 1 (4.2) 3 (27.3) 0 (0.0) 1 (25) 2 (40) 0 (0.0) 2 (50)
Tobramycin 5 (20.8) 3 (27.3) 0 (0.0) 1 (25) 1 (20) 0 (0.0) 2 (50)
Ciprofloxacin 8 (33.3) 1 (9.1) 0 (0.0) 2 (50) 2 (40) 0 (0.0) 2 (50)
Norfloxacin 8 (33.3) 1 (9.1) 2 (50) 2 (50) 2 (40) 0 (0.0) 2 (50)
Nitrofurantoin 2 (8.3) 10 (90.9) IR ‑ 5 (100) 0 (0.0) IR
Trimethoprim/sulfamethoxazole 14 (58.3) 5 (45.5) 2 (50) IR 3 (60) 1 (33.3) 1 (25)
Total number of isolates 24 11 4 4 5 3 4
IR: Intrinsic resistance. ‑: Not tested

51 International Journal of Health Sciences

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

Table 3: Number (%) of common Gram‑positive urinary pathogens resistant (R) to antimicrobial agents*
Variables Enterococcus faecalis Enterococcus faecium Staphylococcus aureus Staphylococcus saprophyticus
Benzyl penicillin 5 (100) 2 (100) 2 (100) 3 (100)
Oxacillin ‑ ‑ 1 (50) 1 (33.3)
Gentamicin IR IR 0 (0.0) 0 (0.0)
Tobramycin IR IR 0 (0.0) 0 (0.0)
Levofloxacin 2 (40) 1 (50) 1 (50) 0 (0.0)
Clindamycin IR IR 0 (0.0) 1 (33.3)
Linezolid 1 (20) 0 (0.0) 0 (0.0) 0 (0.0)
Teicoplanin 0 (0.0) 0 (0.0) 0 (0.0) 1 (33.3)
Vancomycin 0 (0.0) 0 (0.0) 0 (0.0) 1 (33.3)
Fosfomycin 5 (100) 2 (100) 0 (0.0) IR
Nitrofurantoin 2 (40) 2 (100) 0 (0.0) 0 (0.0)
Rifampicin 5 (100) 2 (100) 0 (0.0) 1 (33.3)
Trimethoprim/Sulfamethoxazole IR IR 0 (0.0) 0 (0.0)
Total number of isolates 5 2 2 3
IR: Intrinsic resistance. ‑: Not tested

Table 4: Frequency distribution of microorganisms isolated from (5.6%), S. saprophyticus (3.3%), and Staphylococcus aureus
patients with CA‑UTIs admitted to OPD of Qassim University (2.2%). These data pointed out that there were decreased in
medical clinics, Buraydah, Qassim, Saudi Arabia, 2014 the prevalence of E. coli and increased of Enterococcus sp.
Organism isolated (n=89) Frequency (%) Total
Escherichia coli 24 (27.0) An alarming finding from this study showed a high degree
Klebsiella pneumoniae 11 (12.4) of drug resistance among pathogens. Our study showed a
Proteus mirabilis 4 (4.5)
very high rate of resistance (>70%) among E. coli isolates to
piperacillin. Among Klebsiella isolates, no resistance was found
Pseudomonas aeruginosa 4 (4.5) 56
for meropenem and low resistance was found for ciprofloxacin
Enterobacter cloacae 5 (5.6)
(9.1), norfloxacin (9.1), and cefotaxime (9.1) but high for
Morganella morganii 4 (4.5) nitrofurantoin and trimethoprim/sulfamethoxazole. Resistance
Pantoea agglomerans 4 (4.5) to piperacillin, piperacillin/tazobactam, and ceftazidime among
Citrobacter freundii 4 (4.5) P. aeruginosa, E. cloacae, and M. morganii goes in similar
Klebsiella oxytoca 3 (3.4) pattern consistently over 75%.[19] This resistance is most likely
Proteus vulgaris 2 (2.2) due to the massive use of third-generation cephalosporins and
Acinetobacter baumannii 3 (3.4) 21
fluoroquinolone antibiotics in UTIs patients. Therefore, they
were increasingly recognized as important causes of UTIs and
Enterobacter aerogenes 3 (3.4)
our study findings highlight the significance of this species
Acinetobacter lwoffii 3 (3.4)
as a leading cause of MDR infection in patients with UTIs.
Serratia marcescens 3 (3.4)
Enterococcus faecalis 5 (5.6) The etiology of bacteria causing UTI as well as their
Staphylococcus saprophyticus 3 (3.4) susceptibility to antimicrobials continue to vary over time
Enterococcus faecium 2 (2.2) 12 period and it is different among different countries.[10,20,21]
Staphylococcus aureus 2 (2.2) Sensitivity to cotrimoxazole is a crucial feature in choosing
Total 89 (100.0) 89
the empirical treatment for UTIs, as recommended by the
OPD: Outpatient department, CA‑UTIs: Catheter‑associated urinary tract infections
European Urology Association Guidelines, [22,23] which
suggest cotrimoxazole as the first-line antibiotic choice for
spp. (7.84%), and Proteus spp. (4.91%). Other bacterial empirical therapy in uncomplicated community-acquired
UTIs when the local rates of trimethoprim/sulfamethoxazole
pathogens were Enterococcus spp. (3.98%), Acinetobacter spp.
resistance in uropathogens are <10–20%. However, our
(1.84%), Staphylococcus aureus (1.63%), and Enterobacter
study revealed an overall resistance of trimethoprim/
spp. (0.35). However, in our study, the most common sulfamethoxazole of 49.4% and E. coli-specific resistance
pathogen was E. coli (26.9 %), K. pneumoniae (12.4%), E. of 58.3%. Similar results were obtained in a recent study
cloacae (5.6%), P. mirabilis (4.5%), P. aeruginosa (4.5%), E. of this nature conducted in Sultanate Oman by Sharef et
aerogenes (3.3%), M. morganii (4.5%), Citrobacter freundii al.,[24] which revealed an overall resistance of 47% and E.
(4.5%), Pantoea agglomerans (4.5%), Enterococcus faecalis coli specific resistance of 50%, to this antibiotic. This is in

International Journal of Health Sciences 52

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

contrast to various studies conducted in European countries We use a fully automated machine. The use of the VITEK 2
which revealed low resistance ranging from 28% to 30%[25,26] system enables the identity of broad spectrum of bacteria and
and other African countries where resistance is comparatively their susceptibility up to 20 different antimicrobials.
high ranging from 88.3% to 98.6% [27,28] The high resistance in
trimethoprim/sulfamethoxazole susceptibility pattern may be In the current study, the urinary pathogens of a relatively
due to non-judicious use and over-the-counter selling of this low prevalence or newly emerged uropathogens are
antibiotic; however, recently, steps have been taken by the described in Table 5. These included Citrobacter freundii,
Ministry of Health, KSA, to restrict over-the-counter selling Klebsiella oxytoca, Proteus vulgaris, Acinetobacter
of antibiotics without prescription of doctor; implantation baumannii, Acinetobacter lwoffii, Serratia marcescens,
of this rule will have a significant impact in controlling and Pantoea agglomerans. Information on Acinetobacter,
antibiotic resistance. Citrobacter, and Pantoea agglomerans are included in Table 5
die to their clinical importance. Mostly, Acinetobacter species
Only few researches have been conducted to reveal the latest are acquired from nosocomial infections, particularly, in
trends in etiological agents causing UTI among outpatients patients who are catheterized or having debilitating disease,
and community. In contrast, significant changes in the causes but, in our research, we isolated it from it in community-
of hospital-acquired UTIs have been reported since 1980.[29] acquired UTI.
The laboratory tests, especially urine culture and sensitivity,
are mandatory to establish an accurate diagnosis and antibiotic The antibiotic susceptibility of uropathogenic bacteria is
susceptibility pattern of pathogens causing UTI. known to change with time and is inconsistent in different
regions.[20] Here, we have described the impact of the best
As part of infection control, we use the VITEK System to antimicrobials with low resistance rate (overall resistance %)
detect and report uropathogenic etiology and to detect the against the uropathogens in this study. The best antimicrobials
antibiotic susceptibility to limit the therapeutic failures that for Gram-negative organisms (n = 77) were meropenem
may inherently be caused by the conventional methods used. (6.5%), amikacin (20.8%), gentamicin (20.8%), tobramycin
The phenotyping techniques which have been used to identify (27.3%), and cefepime (28.6%) and moderate resistance
uropathogenic bacteria and to confirm the antimicrobial rate were ciprofloxacin (31.2%), cefotaxime (32.5%),
resistance data profile find concurrently agreements to the cefoxitin (35.1%), norfloxacin (35.1%), ceftazidime (36.4%),
previously used molecular genotyping methods. cefpodoxime (41.6%), piperacillin/tazobactam (44.2%),

Table 5: Number (%) of less common Gram‑negative urinary pathogens resistant (R) to antimicrobial agents*
Variables Citrobacter Klebsiella Proteus Acinetobacter Acinetobacter Pantoea Serratia
freundii oxytoca vulgaris baumannii lwoffii agglomerans marcescens
Ampicillin IR IR IR IR IR IR IR
Amoxicillin/clavulanic acid IR 3 (100) 2 (100) IR IR IR IR
Piperacillin 4 (100) 3 (100) 2 (100) 1 (33.3) 2 (66.7) 0 (0.0) 0 (0.0)
Piperacillin/tazobactam 1 (25) 3 (100) 2 (100) 1 (33.3) 2 (66.7) 0 (0.0) 1 (33.3)
Cefalotin IR 3 (100) IR IR IR IR IR
Cefuroxime IR IR IR IR IR IR IR
Cefoxitin IR 2 (66.7) 2 (100) IR IR IR IR
Cefpodoxime IR 3 (100) 2 (100) ‑ ‑ IR 3 (100)
Cefotaxime 2 (50) 3 (100) 2 (100) 1 (33.3) 2 (66.7) 4 (100) 1 (33.3)
Ceftazidime 2 (50) 3 (100) 2 (100) 1 (33.3) 2 (66.7) 2 (50) 0 (0.0)
Cefepime 1 (25) 3 (100) 2 (100) 0 (0.0) 1 (33.3) 1 (25) 0 (0.0)
Meropenem 0 (0.0) 2 (66.7) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)
Amikacin 2 (50) 3 (100) 0 (0.0) 0 (0.0) 1 (33.3) 0 (0.0) 0 (0.0)
Gentamicin 2 (50) 2 (66.7) 0 (0.0) 0 (0.0) 1 (33.3) 2 (50) 0 (0.0)
Tobramycin 2 (50) 3 (100) 0 (0.0) 0 (0.0) 1 (33.3) 2 (50) 0 (0.0)
Ciprofloxacin 3 (75) 3 (100) 1 (50) 0 (0.0) 2 (66.7) 0 (0.0) 0 (0.0)
Norfloxacin 3 (75) 3 (100) 1 (50) 0 (0.0) 2 (66.7) 1 (25) 0 (0.0)
Nitrofurantoin 2 (50) 2 (66.7) IR ‑ ‑ 4 (100) IR
Trimethoprim/sulfamethoxazole 1 (25) 2 (66.7) 1 (50) 3 (100) 3 (100) 4 (100) 0 (0.0)
Total number of isolates 4 3 2 3 3 4 3
IR: Intrinsic resistance. ‑: Not tested

53 International Journal of Health Sciences

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

and cefuroxime (46.8%); however, the high resistance Availability of data and materials
rate was found to be against cefuroxime axetil (49.4%),
trimethoprim/sulfamethoxazole (49.4%), nitrofurantoin All the data which are supporting our research findings are
(50.6%), amoxicillin/clavulanic acid (66.2%), piperacillin present in this work.
(72.7%), and ampicillin (88.3%).
Competing Interests
In contrast, the sensitivity pattern of antimicrobials for Gram-
positive organisms (n = 12) was linezolid (8.3%), teicoplanin Authors mention that they do not have any competing interests
(8.3%), vancomycin (8.3%), cefalotin screen (16.7%), moxifloxacin in this research.
(25%), nitrofurantoin (33.3%), and levofloxacin (33.3%); however,
the high resistance rate was found to be against erythromycin Funding
(50%), trimethoprim/sulfamethoxazole (50%), gentamicin (58.3%),
tobramycin (58.3%), fosfomycin (58.3%), clindamycin (66.7%), There has been no funding for this research study.
oxacillin (75%), tetracycline (75%)m and benzylpenicillin (100%)
resistance rate. Among our Gram-positive isolated organisms, there References
was no inducible clindamycin resistance (0.0%).
1. Foxman B. Epidemiology of urinary tract infections: Incidence,
This research work will have an important impact in the treatment morbidity, and economic costs. Dis Mon 2003;49:53-70.
and management of patients with catheter-associated (CA)- 2. American College of Obstetricians and Gynecologists. ACOG practice
bulletin no 91: Treatment of urinary tract infections in nonpregnant
UTI, particularly those patients who are infected with MDR
women. Obstet Gynecol 2008;111:785-94.
uropathogens. It should be noted that MDR is gradually increasing
3. Foxman B, Gillespie B, Koopman J, Zhang L, Palin K, Tallman P, et al.
throughout the world and it is an alarming sign as with time we are Risk factors for second urinary tract infection among college women.
losing our therapeutic options for treating simple infections caused Am J Epidemiol 2000;151:1194-205.
by bacteria. Efforts should be done to make clinicians realize 4. Nguyen HT. Bacterial Infections of the Genitourinary Tract. Smith’s
the fact that there is a high possibility of multidrug resistance. General Urology. 16th ed New York (USA): Mcgraw-Hill Medical;
Second, the occurrence of MDR which we observed in this study 2004. p. 220.
is a serious threat in the management of patients with CA-UTI. It 5. Momoh A, Orhue P, Idonije O, Oaikhena A, Nwoke E, Momoh A. The
highlights the relevance of a more serious systematic approach to antibiogram types of Escherichia coli isolated from suspected urinary
tract infection samples. J Microbiol Biotech Res 2011;1:57-65.
decrease the antibiotic resistance rates. In this particular era, when
antibiotic resistance is growing with an alarming rate, more research 6. Schnarr J, Smaill F. Asymptomatic bacteriuria and symptomatic urinary
tract infections in pregnancy. Eur J Clin Invest 2008;38 Suppl 2:50-7.
work is highly needed on a priority basis for the development of
7. Spellberg B, Bartlett JG, Gilbert DN. The future of antibiotics and
rapid diagnostic test (point of care testing) for prompt targeted
resistance. N Engl J Med 2013;368:299-302.
therapy. The execution of a drug monitoring system that augments
8. McQuiston Haslund J, Rosborg Dinesen M, Sternhagen Nielsen AB,
drug administration and assists a more personalized methodology Llor C, Bjerrum L. Different recommendations for empiric first-
to recommended treatment is also needed. choice antibiotic treatment of uncomplicated urinary tract infections in
europe. Scand J Prim Health Care 2013;31:235-40.
Moreover, education programs should be conducted to reduce 9. Goossens H, Ferech M, Vander Stichele R, Elseviers M, ESAC Project
the prevalence of disease in the community as well as enlighten Group. Outpatient antibiotic use in Europe and association with
the quality of life for patients living in low- and middle-income resistance: A cross-national database study. Lancet 2005;365:579-87.
regions. In the near future, we aim to implement and weigh the 10. Warren JW, Abrutyn E, Hebel JR, Johnson JR, Schaeffer AJ,
Stamm WE, et al. Guidelines for antimicrobial treatment of
efficiency of such programming in improving health literacy
uncomplicated acute bacterial cystitis and acute pyelonephritis in
as well as decreasing infection rates. women. Infectious diseases society of America (IDSA). Clin Infect Dis
1999;29:745-58.
Conclusions 11. Hamdan HZ, Ziad AH, Ali SK, Adam I. Epidemiology of urinary
tract infections and antibiotics sensitivity among pregnant women at
This research work has shown that patients who presented Khartoum north hospital. Ann Clin Microbiol Antimicrob 2011;10:2.
with UTI in Qassim are at high risk of antibiotic resistance. 12. Hamdan HZ, Kubbara E, Adam AM, Hassan OS, Suliman SO, Adam I,
et al. Urinary tract infections and antimicrobial sensitivity among
The research also has shown that MDR bacteria can lead to
diabetic patients at Khartoum, Sudan. Ann Clin Microbiol Antimicrob
momentous therapeutic problems in OPD patients. 2015;14:26.
13. Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol
Declarations 2010;7:653-60.
14. Kattel HP, Acharya J, Mishra SK, Rijal BP, Pokhrel BM. Bacteriology
Ethics approval and consent to participate of urinary tract infection among patients attending Tribhuvan
university teaching hospital Kathmandu, Nepal. J Nepal Assoc Med
Taken. Lab Sci 2008;25:29.

International Journal of Health Sciences 54

Vol. 13, Issue 2 (March - April 2019)
 Ahmed, et al.: Uropathogens/antimicrobial susceptibility patterns

15. August SL, De Rosa MJ. Evaluation of the prevalence of urinary tract 23. Grabe M, Bartoletti R, Bjerklund-Johansen T. Guidelines on Urological
infection in rural panamanian women. PLoS One 2012;7:e47752. Infections. Netherlands: European Association of Urology; 2015.
16. Ahmad S, Al-Juaid NF, Alenzi FQ, Mattar EH, Bakheet Oel-S. 24. Sharef SW, El-Naggari M, Al-Nabhani D, Al Sawai A, Al Muharrmi Z,
Prevalence, antibiotic susceptibility pattern and production of Elnour I, et al. Incidence of antibiotics resistance among uropathogens
extended-spectrum beta-lactamases amongst clinical isolates of in Omani children presenting with a single episode of urinary tract
Klebsiella pneumoniae at armed forces hospital in Saudi Arabia. J Coll infection. J Infect Public Health 2015;8:458-65.
Physicians Surg Pak 2009;19:264-5. 25. De Francesco MA, Ravizzola G, Peroni L, Negrini R, Manca N.
17. Al-Tawfiq JA, Anani AA. Antimicrobial susceptibility pattern of Urinary tract infections in Brescia, Italy: Etiology of uropathogens
bacterial pathogens causing urinary tract infections in a Saudi Arabian and antimicrobial resistance of common uropathogens. Med Sci Monit
hospital. Chemotherapy 2009;55:127-31. 2007;13:BR136-44.

18. Ahmad S, Ahmad F. Urinary tract infection at a specialist hospital in 26. Miragliotta G, Di Pierro MN, Miragliotta L, Mosca A. Antimicrobial
Saudi Arabia. Bangladesh Med Res Counc Bull 1995;21:95-8. resistance among uropathogens responsible for community-acquired
urinary tract infections in an Italian community. J Chemother
19. Gupta K, Stamm WE. Outcomes associated with trimethoprim/ 2008;20:721-7.
sulphamethoxazole (TMP/SMX) therapy in TMP/SMX resistant
27. Ibrahim ME, Bilal NE, Hamid ME. Increased multi-drug resistant
community-acquired UTI. Int J Antimicrob Agents 2002;19:554-6.
Escherichia coli from hospitals in Khartoum state, Sudan. Afr Health
20. Livermore DM, Pearson A. Antibiotic resistance: Location, location, Sci 2012;12:368-75.
location. Clin Microbiol Infect 2007;13 Suppl 2:7-16.
28. Ibrahim ME, Bilal NE, Magzoub MA, Hamid ME. Prevalence of
21. Magliano E, Grazioli V, Deflorio L, Leuci AI, Mattina R, Romano P, extended-spectrum β-lactamases-producing Escherichia coli from
et al. Gender and age-dependent etiology of community-acquired hospitals in Khartoum state, Sudan. Oman Med J 2013;28:116-20.
urinary tract infections. ScientificWorldJournal 2012;2012:349597. 29. Bronsema DA, Adams JR, Pallares R, Wenzel RP. Secular trends in
22. European Association of Urology. Guidelines on Urological Infections. rates and etiology of nosocomial urinary tract infections at a university
Netherlands: European Association of Urology; 2014. hospital. J Urol 1993;150:414-6.

55 International Journal of Health Sciences

Vol. 13, Issue 2 (March - April 2019)