Original Article

Virulence and antimicrobial resistance of

common urinary bacteria from asymptomatic
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students of Niger Delta University,

Amassoma, Bayelsa State, Nigeria
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 03/05/2024

Adebola Onanuga, Tamaradobra Laurretta Selekere

Department of ABSTRACT
Pharmaceutical
Background: Asymptomatic bacteriuria frequently occurs among all ages with the possibility of developing into urinary
Microbiology and
Biotechnology,
tract infections, and the antimicrobial resistance patterns of the etiologic organisms are essential for appropriate
Faculty of Pharmacy, therapy. Thus, we investigated the virulence and antimicrobial resistance patterns of common urinary bacteria in
Niger Delta University, asymptomatic students of Niger Delta University, Amassoma, Bayelsa State, Nigeria in a cross‑sectional study.
Wilberforce Island, Materials and Methods: Clean catch mid‑stream early morning urine samples collected from 200 asymptomatic
Bayelsa State, Nigeria University students of aged ranges 15–30 years were cultured, screened and common bacteria were identified using
standard microbiological procedures. The isolates were screened for hemolysin production and their susceptibility to
Address for correspondence: antibiotics was determined using standard disc assay method. Results: A total prevalence rate of 52.0% significant
Dr. Adebola Onanuga,
E‑mail: adebola.onanuga@
bacteriuria was detected and it was significantly higher among the female with a weak association (2 = 6.01,
ndu.edu.ng phi = 0.173, P = 0.014). The Klebsiella pneumoniae and Staphylococcus aureus isolates were most frequently
encountered among the isolated bacteria and 18 (12.7%) of all the bacterial isolates produced hemolysins. All the
bacterial isolates exhibited 50–100% resistance to the tested beta‑lactam antibiotics, tetracycline and co-trimoxazole.
The isolated bacteria were 85-100% multi-drug resistant. However, most of the isolates were generally susceptible
to gentamicin and ofloxacin. The phenotypic detection of extended‑spectrum beta‑lactamases was 9 (9.6%) among
the tested Gram‑negative bacterial isolates. Conclusions: The observed high proportions of multidrug resistant urinary
bacteria among asymptomatic University students call for the need of greater control of antibiotic use in this study area.
Received : 14‑03‑15
Review completed : 16‑05‑15 KEY WORDS: Antimicrobial resistance, asymptomatic bacteriuria, Bayelsa State, Nigeria, students,
Accepted : 16‑06‑15 urinary pathogens

U rinary tract infections (UTIs) are one of the most common

bacterial infections which affect the human population of
all ages regardless of their sex in both community and hospital
settings.[1,2] It is the second most common type of infection
that accounts for about 8.3 million doctor visit every year and
it occurs far more frequently in women than in men because
of the female’s short urethra, which is adjacent to the genital
and intestinal tracts openings.[3,4]
Asymptomatic bacteriuria is a condition that refers to the
presence of bacteria in two consecutive clear‑voided urine
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specimens with both yielding positive cultures of at least 105
cfu/ml of the same uropathogen in a patient without urinary
symptoms.[4,5] Asymptomatic bacteriuria commonly occurs at
varying prevalence by age, sex, sexual activity, and the presence
of genitourinary abnormalities with the prevalence of bacteriuria
usually increases with age especially in females living in the
community.[5]
Asymptomatic bacteriuria is known to be highly prevalent
among the elderly, pregnant women and people with diabetes
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How to cite this article: Onanuga A, Selekere TL. Virulence and antimicrobial
DOI: resistance of common urinary bacteria from asymptomatic students of
10.4103/0975-7406.171684 Niger Delta University, Amassoma, Bayelsa State, Nigeria. J Pharm Bioall
Sci 2016;8:29-33.

© 2016 Journal of Pharmacy And Bioallied Sciences | Published by Wolters Kluwer - Medknow 29 
 Onanuga and Selekere: Virulence and antibiotic resistance of uropathogen
and bladder catheters who are more likely to experience
systematic UTI. Hence, the volume of reports on these groups
of people than the general healthy individuals living in the
community.[6] Notwithstanding, the screening of young sexually
active individuals in a particular community for significant
asymptomatic bacteriuria and the patterns of antibiotic
resistance of the isolated uropathogens will be a very useful
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guide for the empirical treatment of UTIs, since UTIs affects
humans of all ages and not a selected group.[7] The frequently
encountered bacteria in patients with UTIs include Escherichia
coli, Klebsiella species, Pseudomonas aeruginosa, Proteus spp.,
Streptococcus faecalis, Staphylococcus aureus, Staphylococcus
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saprophyticus and Enterobacter species, but Gram‑negative
bacteria especially E. coli and Klebsiella species have been
reported by several researchers to be the most predominant
organisms in UTIs cases.[8,9]
Antibiotic resistance has become a problem of global proportions
affecting virtually all bacteria that commonly cause human
illness.[10] The clinical management of UTIs has been hampered
by the increasing speed at which some urinary bacteria develop
resistance to frequently used antimicrobial agents.[11] The
incidence of multidrug resistance among common uropathogens
has been associated with unregulated use of antibiotics in most
developing countries including Nigeria which favor the huge
use and misuse of antibiotics within the hospital, agricultural
and community settings.[12,13]
The study of asymptomatic bacteriuria among University
students and other healthy individuals in the community have
been very few in Nigeria, with reports from Ibadan (South West),
Keffi (North Central) and Port Harcourt (South‑South) while
there is none from Bayelsa State.[14‑16] Thus, this study of
determining the bacterial profile and antibiotic resistance
patterns of uropathogens among asymptomatic students of
Niger Delta University in Amassoma, Bayelsa state, Nigeria
will both contribute to the knowledge in this field and serve as
a means of providing guideline for the empirical treatment of
UTIs in this area of Nigeria.
Materials and Methods
Study design
A cross‑sectional study was carried out among 200 healthy
undergraduate students of Niger Delta University, Amassoma,
Bayelsa State, as a representative of healthy young sexually
active individuals in the community. The objective of the
study was to investigate the level of carriage of common
urinary pathogens by these healthy individuals, their virulence
potentials, and antibiotic resistance rate. A study questionnaire
was used to recruit those who claimed not to have symptoms
associated with UTIs and to obtain their basic demographic
data.
Setting
The asymptomatic students were drafted from various faculties
of learning in the University from April to August 2012
 30 Journal of Pharmacy and Bioallied Sciences January-March 2016 Vol 8 Issue 1
(5 months) and only students who had not used antibiotics
within the last 2 weeks prior to this survey were admitted into
the study.
Ethical approval and consent
A written informed consent was signed by all the participants
before enrollment, and the study was approved by the ethical
committee of the institution before the commencement of
the study.
Collection of samples and bacteriology
Each study participant collected the clean catch midstream
urine into the sterile and wide mouthed glass bottles following
the prescribed instructions for the urine collection. The urine
samples were processed in the laboratory within 2 h of collection.
Each of the urine samples was mixed and a calibrated sterile
wire loop of 4.0 mm diameter designed to deliver 0.01 ml was
used to inoculate Cysteine Lactose Electron Deficient agar and
MacConkey agar (Oxoid, UK) plates and streaked for discrete
colonies before being incubated at 37°C for 24 h for bacterial
growth. The samples that gave bacterial count ≥105 colonies per
ml (after multiplying the plate count by 100) were considered
as significant bacteriuria while those that gave <105 colonies
per ml were considered as insignificant bacteriuria.[17] The
characteristic discrete colonies on the plates were identified
using microbiological techniques which include colony
morphology on selective media, hemolytic pattern on blood
agar, Gram’s stain reaction and biochemical characteristics for
both Gram‑positive and Gram‑negative bacteria.
Antimicrobial susceptibility testing
Antimicrobial susceptibility tests of all the pure bacterial
isolates were performed with 12 antibiotic discs from
Oxoid, UK using the modified Kirby‑Bauer disc diffusion
technique as specified by Clinical Laboratory Standard
Institute.[18] The standard suspension of each isolate was
prepared using its overnight colony culture, which was adjusted
to the turbidity of 0.5 McFarland standard before being
used to swab the surface of a dried Mueller‑Hinton (MH)
agar (Oxoid, UK) plate. The following antimicrobial discs
were placed on the MH agar (in duplicates) after 20 min of
inoculation: Ampicillin (AMP 10 µg), tetracycline (TET 30 µg),
co‑trimoxazole (SXT 25 µg), ofloxacin (OFX 5 µg), ciprofloxacin
(CIP 5 µg), chloramphenicol (C 30 µg), gentamicin (CN
10 µg), ceftazidime (CAZ 30 µg), cefotaxime (CTX 30 µg) and
nitrofurantoin (F 30 µg) for Gram‑negative bacteria. The third
generation cephalosporins (ceftazidime and cefotaxime) were
replaced with cefoxitin (FOX 30 µg) for Gram‑positive bacteria
and these isolates were subjected to vancomycin 2–16 µg/ml
using agar dilution method. The plates containing enterobacteria
were incubated at 37°C while those for Staphylococcus species
were incubated at 35°C for 24 h. The zone diameter of inhibition
around each antimicrobial disc was measured and interpreted
using the Clinical and Laboratory Standards Institute chart while
the Staphylococcus isolates that were resistant to vancomycin at
2 µg/ml were subjected to 4–16 µg/ml concentrations.
 Onanuga and Selekere: Virulence and antibiotic resistance of uropathogen

Detection of extended spectrum beta‑lactamase Table 1: Age and gender distribution of students with
producing organisms significant bacteriuria
Age Number Number with significant Chi-square Ф P
The Gram‑negative bacteria that were resistant to the third group of sample bacteriuria
generation cephalosporins (cefotaxime and ceftazidime) were Male (%) Female (%)
subjected to combination discs of cefotaxime/clavulanic acid, (n=107) (n=93)
ceftazidime/clavulanic acid, single disc of cefotaxime and 15-19 35 5 16 1.414 0.201 0.234
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ceftazidime on the same MH agar plates and incubated at 37°C 20-24 141 35 36 2.099 0.122 0.147
25-29 24 7 5 3.556 0.385 0.059
for 24 h for the phenotypic detection of extended spectrum
Total 200 47 (43.9%) 57 (61.3%) 6.011 0.173 0.014*
beta‑lactamase (ESBL) enzymes. The bacteria is said to be
an ESBL producing organism, if the zone diameter difference *Statistically significant (P<0.05)
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between each combination disc and its single disc on the

organism’s plate is ≥ 5 mm.[18] Table 2: Common UTI bacteria and their virulence trait
(haemolysin production)
Statistical analysis Urinary bacteria Number Number (%) of
of isolates haemolysin producers
The groups differences were tested using the Chi‑square test Escherichia coli 10 (7.0) 1 (5.6)
(or Fisher’s exact test when expected frequencies were too low), Pseudomonas aeruginosa 29 (20.4) 3 (10.3)
with the assumed level of statistical significance at a P < 0.05 Klebsiella pneumoniae 55 (38.7) 9 (16.4)
Staphylococcus aureus 48 (33.8) 5 (10.4)
while the strength and direction association or relationship
Total 142 18 (12.7)
was measured using the phi coefficient/Cramer’s V tests where
applicable. Data was performed with SPSS for Windows, version UTI: Urinary tract infection
15.0 (SPSS Inc., Chicago, IL).
Table 3: The antimicrobial resistance profile of common
Results urinary isolates from asymptomatic subjects
Antimicrobial Number of resistant urinary isolates (%)
Of all the 200 University students which comprised 107 (53.3%) agent Escherichia Klebsiella Pseudomonas Staphylococcus
females and 93 (46.5%) males recruited for this study, coli pneumoniae aeruginosa aureus
155 (77.5%) of their urine samples yielded positive bacterial (n=10) (n=55) (n=29) (n=48)
growth with 104 (52.0%) of them having significant bacteriuria. Ampicillin 10 (100) 55 (100) 29 (100) 48 (100)
The prevalence of significant bacteriuria among the students Ceftazidime 5 (50) 30 (54.5) 29 (100) NT
was significantly higher with a weak association among female Cefotaxime 9 (90) 23 (41.8) 29 (100) NT
Chloramphenicol 3 (30) 41 (74.5) 18 (62) 25 (52.1)
than the male (2 = 6.01, phi = 0.173, P = 0.014) but the Gentamicin 3 (30) 25 (45.5) 9 (31) 7 (14.6)
observed differences among the different age groups were not Ciprofloxacin 5 (50) 23 (41.8) 8 (27.6) 20 (41.7)
statistically significant [Table 1]. Ofloxacin 4 (40) 14 (25.5) 7 (24.1) 19 (39.6)
Nitrofurantoin 3 (30) 39 (70.9) 20 (68.9) 13 (27.1)
A total of 142 isolates of common UTI bacteria were identified Tetracycline 10 (100) 55 (100) 29 (100) 43(89.6)
Co-trimoxazole 10 (100) 37 (67.3) 18 (62) 28 (58.3)
from all the 155 samples with positive growths. Multiple bacteria Cefoxitin NT NT NT 48 (100)
of different species were recovered from 18 (11.6%) of the Vancomycin NT NT NT 3 (6.3)
samples, and the number of isolates with hemolysin production
NT: Not tested
was 18 (12.7%) as shown in [Table 2].

All the tested Gram‑positive and Gram‑negative bacteria
exhibited 50–100% resistance to beta‑lactam antibiotics,
tetracycline, and co‑trimoxazole. Klebsiella pneumoniae was
found to be generally resistant to all the tested agents whilst
P. aeruginosa was totally insensitive to the tested beta‑lactam
antibiotics and tetracycline. All the isolates of S. aureus were
phenotypic methicillin‑resistant strains. The most effective
agents against all the isolated bacteria, although with moderate
levels of resistance were gentamicin and ofloxacin [Table 3].
Multiple antibiotic resistance in this study was defined as the
resistance of an isolate to at least one antimicrobial agent in at
least three classes of antimicrobial agents used.[19] The isolates
of the common urinary bacteria from asymptomatic University
students exhibited a multiple antibiotic resistance of 85–100%
as shown in Table 4.
A total of 9 (9.6%) Gram‑negative bacteria isolates showed a
phenotypic production of ESBLs enzymes and the distribution
of the producers among the bacteria is shown in Table 5.
Discussion
Our study found a total prevalence of 52.0% significant
bacteriuria among the young asymptomatic University
students with a significantly higher level among the females
than the males (P = 0.014). This observed rate of significant
bacteriuria is higher than the findings of Ngwai et al.[14] in Keffi
(North Central) and Olowe et al.[15] in Oshogbo (South West)
Nigeria, among similar individuals without overt clinical
symptoms. The high prevalence among the subjects might be
due to contaminants from procedural error or perennial skin.
However, significantly higher level of bacteriuria observed

Journal of Pharmacy and Bioallied Sciences January-March 2016 Vol 8 Issue 1 31 

 Onanuga and Selekere: Virulence and antibiotic resistance of uropathogen

Table 4: Multi-drug resistance of the isolated bacteria its consequences could be an increased cost of treatments and
Resistance to Number of resistant urinary isolates (%) long hospital visits when the empirical treatments are targeted
class of agent Escherichia Pseudomonas Klebsiella Staphylococcus at a particular class of bacteria.
coli aeruginosa pneumoniae aureus (n=48)
(n=10) (n=29) (n=55) Antimicrobial resistance has been known to be a global health
Fully susceptible 0 0 0 0 problem affecting the treatment of patients with UTIs and
1 0 0 0 3 the situation is alarming in developing countries where there
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2 0 5 4 4 is little or no control of antimicrobial use. This study’s results

3 4 6 7 14
of antimicrobial resistance showed all the tested bacteria to
4 2 7 8 12
5 1 4 12 8 be 60–100% resistant to ampicillin and co‑trimoxazole. These
6 2 2 14 4 agents were not only among the older antimicrobial agents but
7 1 3 10 2 were also among the recommended first line drugs of choice for
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8 0 0 0 1 the treatment of UTIs.[30] This, therefore, suggests that their

≥3 10 (100) 24 (88.8) 51 (92.7) 41 (85.4) usefulness for the empiric therapy of UTIs is limited. The high
resistance of these bacteria to ampicillin, co‑trimoxazole and
tetracycline has been attributed to their frequent uses in the
Table 5: The frequency of ESBL producers among the hospital, community, and agricultural settings since they are
enterobacteria older antibiotics with cheaper prices.[11] The observation of total
Urinary enterobacteria Number Number (%) of resistance of P. aeruginosa isolates to the tested third generation
of isolates ESBL producers
cephalosporin suggests the ineffectiveness of these agents to
Escherichia coli 10 1 (10) this organism and thus, they might not be suitable for empiric
Pseudomonas aeruginosa 29 4 (13.8)
treatment of UTIs especially with the emerging prevalence of
Klebsiella pneumoniae 55 4 (7.3)
Total 94 9 (9.6) multiple co‑infections. Of all the tested agents, gentamicin and
ofloxacin were observed to be the most effective agents against
ESBL: Extended spectrum beta-lactamase
the isolated bacteria although with some moderate levels of
resistance. Thus, these agents may be suitable for the empiric
among the females is in agreement with the findings of several treatment of mixed infections. The observed moderate levels
earlier studies[6,14,15,20] and it might be related to the short of resistance to these agents which are not frequently being
course of the female urethra and its proximity to the anorectal used like the older drugs show the increasing rate at which the
region.[21,22] treatment of UTIs is becoming a difficult task.

The prevalence of common UTI bacteria among the samples
from the asymptomatic young adults revealed K. pneumoniae
and S. aureus as the most frequently recovered organisms
whilst E. coli was the least. This observation is in contrast to
several reports, which identified E. coli as the most common
uropathogen causing asymptomatic bacteriuria.[15,23,24] However,
this study aligns with the findings of Dada‑Adegbola and
Muili[25] who reported K. pneumoniae as the leading urinary
pathogen. Furthermore, the increasing isolation of S. aureus
as one of the major causes of UTI has also been reported,
thereby suggesting the importance of these bacteria in UTIs.
This observation might be due to these organisms increasing
virulence and prevalence in the gastrointestinal tract.[16,26,27]
The presence of virulence markers in bacteria measures the
organism’s degree of pathogenicity, and hemolysin production
is one of the common virulence traits in bacteria. Hemolysin
is the bacterial toxin that liberates hemoglobin from red
blood cells by destroying their structural integrity. Our study’s
prevalence of hemolysins production among all the isolates
was low (12.7%), suggesting the reason why the volunteers
were not having any overt clinical symptoms. However, the risk
of tissue pathology of the renal system could be high among
those harboring the hemolysin producing bacteria, and such
injury could facilitate bacterial entry into the bloodstream.[28,29]
The detection of 18 (12.7%) samples with different species of
bacteria among the study asymptomatic subjects suggests the
possibility of multiple infections among people with UTIs, and
All the isolates of S. aureus were observed to be phenotypic
methicillin‑resistant strains which had 40% resistance to the
fluoroquinolones but were highly susceptible to vancomycin.
These strains of methicillin‑resistant S. aureus (MRSA) have
been known to have very limited treatment options and their
presence in healthy young adults suggests the possibility of
increasing prevalence of UTIs with very limited treatment
options because MRSA is a potential transmitter of its resistance
genes to susceptible pathogens of the same or different species.
The common urinary bacteria isolated in this study were found
to exhibit 85–100% multiple antibiotic resistance indicating
that the isolates have been widely exposed to various classes of
antimicrobial agents and thus they possess varying antibiotic
resistance genes that could be transferred across species. ESBLs
are enzymes produced by some Gram‑negative bacteria that
mediate resistance to extended spectrum third generation
cephalosporins. Consequently, the ESBL producing bacteria
possess resistance determinants to many other important
groups of antibiotics.[31‑33] This study’s phenotypic detection
of ESBLs among Gram‑negative isolates revealed a prevalence
rate of 9.6%, which suggests that the observed high multidrug
resistance among these isolates might not be fully due to ESBLs
enzymes but to other factors, which were not examined in this
study. However, its detection among isolates of asymptomatic
students even though low, is worrisome because it indicates
the increasing rate at which these bacteria transmit resistance
genes to same or different species. Thus, proper and regular

 32 Journal of Pharmacy and Bioallied Sciences January-March 2016 Vol 8 Issue 1


hand washing techniques can help control its spread to the
healthy population.
Conclusion
The results of this study revealed a high proportion of significant
bacteriuria with high multi‑drug resistant bacteria among the
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asymptomatic students of Niger Delta University, Bayelsa State.
These findings, therefore, highlight the need for constant
monitoring of antimicrobial susceptibility patterns of common
pathogens among the healthy population as a necessary tool
nYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 03/05/2024
in adopting measures to control their spread to vulnerable
individuals in the population.
Acknowledgments
The authors are grateful to the students of Niger Delta
University, Amassoma, Bayelsa State for their voluntary
participation and the staff of Pharmaceutical Microbiology and
Biotechnology Laboratory for their technical assistance during
the period of the study.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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