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
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
settings.[1,2] It is the second most common type of infection varying prevalence by age, sex, sexual activity, and the presence
that accounts for about 8.3 million doctor visit every year and of genitourinary abnormalities with the prevalence of bacteriuria
it occurs far more frequently in women than in men because usually increases with age especially in females living in the
of the female’s short urethra, which is adjacent to the genital community.[5]
and intestinal tracts openings.[3,4]
Asymptomatic bacteriuria is known to be highly prevalent
Asymptomatic bacteriuria is a condition that refers to the among the elderly, pregnant women and people with diabetes
presence of bacteria in two consecutive clear‑voided urine
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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 (5 months) and only students who had not used antibiotics
systematic UTI. Hence, the volume of reports on these groups within the last 2 weeks prior to this survey were admitted into
of people than the general healthy individuals living in the the study.
community.[6] Notwithstanding, the screening of young sexually
active individuals in a particular community for significant Ethical approval and consent
asymptomatic bacteriuria and the patterns of antibiotic
resistance of the isolated uropathogens will be a very useful A written informed consent was signed by all the participants
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guide for the empirical treatment of UTIs, since UTIs affects before enrollment, and the study was approved by the ethical
humans of all ages and not a selected group.[7] The frequently committee of the institution before the commencement of
encountered bacteria in patients with UTIs include Escherichia the study.
coli, Klebsiella species, Pseudomonas aeruginosa, Proteus spp.,
Streptococcus faecalis, Staphylococcus aureus, Staphylococcus
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Collection of samples and bacteriology

saprophyticus and Enterobacter species, but Gram‑negative
bacteria especially E. coli and Klebsiella species have been Each study participant collected the clean catch midstream
reported by several researchers to be the most predominant urine into the sterile and wide mouthed glass bottles following
organisms in UTIs cases.[8,9] the prescribed instructions for the urine collection. The urine
samples were processed in the laboratory within 2 h of collection.
Antibiotic resistance has become a problem of global proportions Each of the urine samples was mixed and a calibrated sterile
affecting virtually all bacteria that commonly cause human wire loop of 4.0 mm diameter designed to deliver 0.01 ml was
illness.[10] The clinical management of UTIs has been hampered used to inoculate Cysteine Lactose Electron Deficient agar and
by the increasing speed at which some urinary bacteria develop MacConkey agar (Oxoid, UK) plates and streaked for discrete
resistance to frequently used antimicrobial agents.[11] The colonies before being incubated at 37°C for 24 h for bacterial
incidence of multidrug resistance among common uropathogens growth. The samples that gave bacterial count ≥105 colonies per
has been associated with unregulated use of antibiotics in most ml (after multiplying the plate count by 100) were considered
developing countries including Nigeria which favor the huge as significant bacteriuria while those that gave <105 colonies
use and misuse of antibiotics within the hospital, agricultural per ml were considered as insignificant bacteriuria.[17] The
and community settings.[12,13] characteristic discrete colonies on the plates were identified
using microbiological techniques which include colony
The study of asymptomatic bacteriuria among University morphology on selective media, hemolytic pattern on blood
students and other healthy individuals in the community have agar, Gram’s stain reaction and biochemical characteristics for
been very few in Nigeria, with reports from Ibadan (South West), both Gram‑positive and Gram‑negative bacteria.
Keffi (North Central) and Port Harcourt (South‑South) while
there is none from Bayelsa State.[14‑16] Thus, this study of Antimicrobial susceptibility testing
determining the bacterial profile and antibiotic resistance
patterns of uropathogens among asymptomatic students of Antimicrobial susceptibility tests of all the pure bacterial
Niger Delta University in Amassoma, Bayelsa state, Nigeria isolates were performed with 12 antibiotic discs from
will both contribute to the knowledge in this field and serve as Oxoid, UK using the modified Kirby‑Bauer disc diffusion
a means of providing guideline for the empirical treatment of technique as specified by Clinical Laboratory Standard
UTIs in this area of Nigeria. Institute.[18] The standard suspension of each isolate was
prepared using its overnight colony culture, which was adjusted
Materials and Methods to the turbidity of 0.5 McFarland standard before being
used to swab the surface of a dried Mueller‑Hinton (MH)
Study design agar (Oxoid, UK) plate. The following antimicrobial discs
were placed on the MH agar (in duplicates) after 20 min of
A cross‑sectional study was carried out among 200 healthy inoculation: Ampicillin (AMP 10 µg), tetracycline (TET 30 µg),
undergraduate students of Niger Delta University, Amassoma, co‑trimoxazole (SXT 25 µg), ofloxacin (OFX 5 µg), ciprofloxacin
Bayelsa State, as a representative of healthy young sexually (CIP 5 µg), chloramphenicol (C 30 µg), gentamicin (CN
active individuals in the community. The objective of the 10 µg), ceftazidime (CAZ 30 µg), cefotaxime (CTX 30 µg) and
study was to investigate the level of carriage of common nitrofurantoin (F 30 µg) for Gram‑negative bacteria. The third
urinary pathogens by these healthy individuals, their virulence generation cephalosporins (ceftazidime and cefotaxime) were
potentials, and antibiotic resistance rate. A study questionnaire replaced with cefoxitin (FOX 30 µg) for Gram‑positive bacteria
was used to recruit those who claimed not to have symptoms and these isolates were subjected to vancomycin 2–16 µg/ml
associated with UTIs and to obtain their basic demographic using agar dilution method. The plates containing enterobacteria
data. were incubated at 37°C while those for Staphylococcus species
were incubated at 35°C for 24 h. The zone diameter of inhibition
Setting around each antimicrobial disc was measured and interpreted
using the Clinical and Laboratory Standards Institute chart while
The asymptomatic students were drafted from various faculties the Staphylococcus isolates that were resistant to vancomycin at
of learning in the University from April to August 2012 2 µg/ml were subjected to 4–16 µg/ml concentrations.
 30 Journal of Pharmacy and Bioallied Sciences January-March 2016 Vol 8 Issue 1
 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 A total of 9 (9.6%) Gram‑negative bacteria isolates showed a
exhibited 50–100% resistance to beta‑lactam antibiotics, phenotypic production of ESBLs enzymes and the distribution
tetracycline, and co‑trimoxazole. Klebsiella pneumoniae was of the producers among the bacteria is shown in Table 5.
found to be generally resistant to all the tested agents whilst
P. aeruginosa was totally insensitive to the tested beta‑lactam Discussion
antibiotics and tetracycline. All the isolates of S. aureus were
phenotypic methicillin‑resistant strains. The most effective Our study found a total prevalence of 52.0% significant
agents against all the isolated bacteria, although with moderate bacteriuria among the young asymptomatic University
levels of resistance were gentamicin and ofloxacin [Table 3]. students with a significantly higher level among the females
than the males (P = 0.014). This observed rate of significant
Multiple antibiotic resistance in this study was defined as the bacteriuria is higher than the findings of Ngwai et al.[14] in Keffi
resistance of an isolate to at least one antimicrobial agent in at (North Central) and Olowe et al.[15] in Oshogbo (South West)
least three classes of antimicrobial agents used.[19] The isolates Nigeria, among similar individuals without overt clinical
of the common urinary bacteria from asymptomatic University symptoms. The high prevalence among the subjects might be
students exhibited a multiple antibiotic resistance of 85–100% due to contaminants from procedural error or perennial skin.
as shown in Table 4. 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 All the isolates of S. aureus were observed to be phenotypic
from the asymptomatic young adults revealed K. pneumoniae methicillin‑resistant strains which had 40% resistance to the
and S. aureus as the most frequently recovered organisms fluoroquinolones but were highly susceptible to vancomycin.
whilst E. coli was the least. This observation is in contrast to These strains of methicillin‑resistant S. aureus (MRSA) have
several reports, which identified E. coli as the most common been known to have very limited treatment options and their
uropathogen causing asymptomatic bacteriuria.[15,23,24] However, presence in healthy young adults suggests the possibility of
this study aligns with the findings of Dada‑Adegbola and increasing prevalence of UTIs with very limited treatment
Muili[25] who reported K. pneumoniae as the leading urinary options because MRSA is a potential transmitter of its resistance
pathogen. Furthermore, the increasing isolation of S. aureus genes to susceptible pathogens of the same or different species.
as one of the major causes of UTI has also been reported,
thereby suggesting the importance of these bacteria in UTIs. The common urinary bacteria isolated in this study were found
This observation might be due to these organisms increasing to exhibit 85–100% multiple antibiotic resistance indicating
virulence and prevalence in the gastrointestinal tract.[16,26,27] that the isolates have been widely exposed to various classes of
antimicrobial agents and thus they possess varying antibiotic
The presence of virulence markers in bacteria measures the resistance genes that could be transferred across species. ESBLs
organism’s degree of pathogenicity, and hemolysin production are enzymes produced by some Gram‑negative bacteria that
is one of the common virulence traits in bacteria. Hemolysin mediate resistance to extended spectrum third generation
is the bacterial toxin that liberates hemoglobin from red cephalosporins. Consequently, the ESBL producing bacteria
blood cells by destroying their structural integrity. Our study’s possess resistance determinants to many other important
prevalence of hemolysins production among all the isolates groups of antibiotics.[31‑33] This study’s phenotypic detection
was low (12.7%), suggesting the reason why the volunteers of ESBLs among Gram‑negative isolates revealed a prevalence
were not having any overt clinical symptoms. However, the risk rate of 9.6%, which suggests that the observed high multidrug
of tissue pathology of the renal system could be high among resistance among these isolates might not be fully due to ESBLs
those harboring the hemolysin producing bacteria, and such enzymes but to other factors, which were not examined in this
injury could facilitate bacterial entry into the bloodstream.[28,29] study. However, its detection among isolates of asymptomatic
The detection of 18 (12.7%) samples with different species of students even though low, is worrisome because it indicates
bacteria among the study asymptomatic subjects suggests the the increasing rate at which these bacteria transmit resistance
possibility of multiple infections among people with UTIs, and genes to same or different species. Thus, proper and regular

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

 Onanuga and Selekere: Virulence and antibiotic resistance of uropathogen

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Journal of Pharmacy and Bioallied Sciences January-March 2016 Vol 8 Issue 1 33 