Original Article

Urinary Tract Infection in Children with Protein‑energy

Malnutrition in Aminu Kano Teaching Hospital Kano, Northwest
Nigeria
Umma Abdulsalam Ibrahim, Henry A. Aikhionbare1, Ibrahim Aliyu
Department of Paediatrics, Bayero University Kano/Aminu Kano Teaching Hospital, PMB 3452, Kano, 1Department of Child Health, University of Benin Teaching
Hospital, PMB 1111, Benin City, Nigeria

Abstract
Background: Determining the antimicrobial sensitivity pattern of urinary tract infection (UTI) in malnourished children in a community
will help the clinician in decision‑making regarding suitable first‑line antibiotics. Materials and Methods: We performed a prospective
cross‑sectional study from July to November 2011 at the Aminu Kano Teaching Hospital to determine the prevalence of UTI and evaluate the
antibiotic sensitivity pattern of organisms isolated from the urine of children with protein‑energy malnutrition (PEM) and normal controls. In
total, 169 children with PEM aged 6–59 months were enrolled consecutively as subjects and 169 well‑nourished age and sex‑matched children
as controls. Results: The prevalence of UTI was found to be 16.0% in the subjects; this was significantly higher than 2.4% in the controls.
The most common isolate was E. coli in both the subjects and controls. All isolates were sensitive to gentamycin and ciprofloxacin, whereas
about half of the isolates were resistant to commonly used antibiotics such as amoxicillin, cotrimoxazole, and cefuroxime. The antibiotic
sensitivity pattern of the organisms differs from other reports. Conclusion: There is high a prevalence of antibiotic resistance to the commonly
used antibiotics for UTI. It is recommended that ciprofloxacin or gentamycin be considered as empirical antibiotic of choice in children with
PEM and proven UTI. It is advised that regular surveillance of urinary tract pathogens should be carried out to evaluate antibiotic sensitivity
pattern to guide empirical treatment.

Keywords: Children, protein‑energy malnutrition, urinary tract infection

Introduction tract, which can predispose to UTI.[3]  If UTI is untreated, it

can lead to kidney damage; this includes kidney scars, poor
Urinary tract infection (UTI) is a common cause of childhood
kidney growth and function, which may predispose to high
morbidity and mortality in most developing countries.[1,2] It is
blood pressure, and end‑stage kidney disease. Therefore,
the second most common bacterial infection in children, and
children with UTI should receive prompt treatment and a
perhaps the most common disease of the urogenital tract, which
careful evaluation of the urinary tract for structural anomalies.
can lead to substantial morbidity that may not be limited to
UTI is more common in malnourished children than in their
the acute period of illness.[2] UTI is the most common occult
well‑nourished counterparts,[4] and the risk of UTI increases
bacterial cause of unexplained fever, especially in children
with the severity of malnutrition.[4] Therefore, understanding
less than 2 years.[3] Immaturity of the immune system in young
the relationship between PEM and UTI is of great public
children may predispose them to higher risk of septicemic and
health importance. Severe acute malnutrition is associated
bacteremic illnesses, and the urinary tract may become seeded
by these invasive organisms during such episodes.[3] UTI can
Address for correspondence: Dr. Umma Abdulsalam Ibrahim,
result in recognition of an important underlying structural or Department of Paediatrics, Aminu Kano Teaching Hospital,
neurogenic abnormality of the urinary tract. Another possible PMB 3452, Kano, Nigeria.
reason for the high prevalence of UTI in this age group is E‑mail: aummaibraheem@gmail.com
due to the presence of structural anomalies of the urinary
This is an open access journal, and articles are distributed under the terms of the Creative
Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to
Access this article online remix, tweak, and build upon the work non-commercially, as long as appropriate credit
Quick Response Code: is given and the new creations are licensed under the identical terms.
Website:
For reprints contact: reprints@medknow.com
www.njbcs.net

How to cite this article: Ibrahim UA, Aikhionbare HA, Aliyu I. Urinary
DOI: tract infection in children with protein-energy malnutrition in Aminu
10.4103/njbcs.njbcs_5_18 Kano Teaching Hospital Kano, Northwest Nigeria. Niger J Basic Clin Sci
2019;16:64-9.

64 © 2019 Nigerian Journal of Basic and Clinical Sciences | Published by Wolters Kluwer - Medknow
 Ibrahim, et al.: UTI in children with PEM
with immune deficiency, which expectedly renders affected
children more vulnerable to severe infections.[5‑7] The effect
of malnutrition on the immune system includes reduced
cell‑ mediated immunity, reduced level of complements,
diminished IgA response, reduced inflammatory response,
and migration of white cell to areas of tissue damage. UTI in
children with PEM may mimic other childhood illnesses.[8]
This study was designed to determine the prevalence of UTI
in children with PEM seen at the Aminu Kano Teaching
Hospital (AKTH) in northern Nigeria. To evaluate, the
antibiotic sensitivity pattern of organisms isolated with a view
to make appropriate recommendations regarding management
and choice of antimicrobials in this environment.
Materials and Methods
This hospital‑based prospective cross‑sectional study was
carried out from July to November 2011 at the AKTH, Kano.
Approval was obtained from the hospital’s ethical committee
for this study. The minimum sample size of 169 was calculated
using the standard formula and the documented prevalence of
11.3% of UTI in malnourished children in Maiduguri.[9]
In total, 169 children with various degrees of PEM aged
6–59 months were enrolled as subjects and 169 well‑nourished
age and sex matched children as controls. Both subjects
and controls were enrolled consecutively in the Paediatric
Outpatient Department (POPD) and Emergency Paediatric
Unit (EPU) of AKTH Kano, after a written informed consent
was obtained from the parents or guardian of the children,
followed with administration of proforma; a dietary history
and 24 h dietary recall were taken. Exclusion criteria for the
children included the history of treatment with antibiotics
during the preceding 2 weeks, those who have been on
steroids, and those whose parents declined consent to be part
of the study.
History was taken from each child, and a systemic physical
examination was performed looking for evidence of symptoms
and signs associated with renal lesion. Weight was measured
using the Bassinet weighing scale in children less than
2 years, and children who were too weak to stand. Infants
were all weighed naked; however, children more than 2 years
were weighed with light clothing after obtaining consent
from the parents using a well calibrated bathroom weighing
scale (Hanson, model 89G Ireland). The weighing scale
was adjusted and standardized to zero, then the weight was
measured to the nearest 50 g. The patients were categorized
into marasmus: Weight for age (WFA) less than 60% without
edema, marasmic kwashiorkor: WFA less than 60% with
edema, underweight kwashiorkor: WFA 60‑<80% with edema,
kwashiorkor: WFA 80–100% with edema and well nourished:
WFA 80–100% without edema according to the Modified
Wellcome classification.[10]
Urine sample was collected from each child into a sterile
universal container with 1.8% boric acid using percutaneous
Nigerian Journal of Basic and Clinical Sciences  ¦  Volume 16  ¦  Issue 1  ¦  January-June 2019
suprapubic aspiration in non‑toilet trained children (less than
3 years old), and midstream urine was collected in older
toilet trained children. Suprapubic aspiration is considered
the gold standard for collection of urine in non‑toilet trained
children (children below the age of 3 years), and it is the most
reliable and useful method of urine collection in non‑toilet
trained children.[11] Lidnocaine cream was applied to the
suprapubic area before the urine sample was collected. The
lower abdomen was then cleansed with savlon antiseptic before
the suprapubic aspiration. Before collecting the midstream
urine in females, the perineum was cleaned with sterile water
from anterior backwards, with the labia separated. In males,
the glans penis and the urethral orifice were also cleaned with
sterile water, with the prepuce retracted in the uncircumcised.
Urine was collected into two sterile universal bottles; urine
sample were collected at the same time of the day (early
morning urine) throughout the data collection. Urine samples
were examined immediately and where samples could not be
worked on immediately; they were stored in the refrigerator
at 4–8°C for not more than 12 h.
Each urine sample was examined with the Combur 10 test
strip (Boehringer Mannheim, Johannesburg) to determine
its protein, leucocyte esterase, and nitrite content. Positive
reactions were measured in accordance with the manufacturer’s
guidelines.
Urine for microscopy was centrifuged at 2000 rpm for 5 min,
the supernatant was discarded, and a wet preparation made
from the sediments and examined under a 40X objective of
a microscope, for pus cells, red cells, and casts. Greater than
10 pus cells per high power field was regarded as significant
pyuria.[2,11] A loop calibrated to deliver approximately 0.001 ml
urine was used for inoculation on cystine lactose electrolyte
deficient and MacConkey agar plates. All plates were incubated
at 37°C for 24 h for colony counts and reported as colony
forming units per ml.[8,11,12] Thereafter, bacterial identification
was done by standard laboratory methods.[8,11]
UTI was defined as pure growth of any single bacterial
organism in urine obtained by suprapubic tap and in case
of clean catch or midstream urine, equal to or greater than
105 colonies/ml of urine.[2,8,11] Antimicrobial sensitivity was
performed on significant isolates by the disc and diffusion
method of strokes,[13] using oxoids multi disc (oxoid Ltd,
Basingstoke, Hampshire England) with the following
antibiotics amoxicillin (20 mcg), cotrimoxazole (25 mcg),
nitrofurantoin (200 mcg), nalidixic acid (30 mcg),
ciprofloxacin (30 mcg), and gentamycin (10 mcg).
Statistical analysis
Data collected were entered into computer database and
analyzed using SSPS version 16.0 software package.
Quantitative variables were summarized using measures
of central tendency (mean and median) and measures of
dispersion (standard deviation). Categorical variables were
summarized using frequency and percentages. The means
were compared using Student’s t test, whereas Chi‑square
65
 Ibrahim, et al.: UTI in children with PEM

test and Fisher’s exact test were used for association between
Table 1: Prevalence of urinary tract infection in PEM and
categorical variables and to determine statistical significance.
control
A P–value of < 0.05 was considered statistically significant.
UTI n (%) No UTI n (%) Total
Results PEM
Control
27 (16.0%)
4 (2.4%)
142 (84.0%)
165 (97.6%)
169
169
Overall, 169 children with PEM and 169 well‑nourished age χ2=18.8, P=0.001 (significant)
and sex matched children were included in the study; there
were 105  (62.1%) males and 64  (37.9%) females, giving a
male: female ratio of 1.6:1 in each group. The mean age was Table 2: Prevalence of urinary tract infection in each
20.6 ± 9.2. More than half of the children with PEM had category of PEM
marasmus. Malnutrition categories Number Total in
with UTI group (%)
In total, 27  (16%) of the subjects and 4  (2.4%) of the
Marasmus 17 87 (19.5)
control group had UTI. The difference was statistically
Marasmic kwashiorkor 4 27 (14.8)
significant (χ2 = 17.19, P = 0.001) [Table 1]. Sixty‑four percent
Underweight kwashiorkor 4 26 (15.3)
of the cases of UTI occurred in the age groups 13–24 months.
Kwashiorkor 2 6 (33.3)
UTI was more common in girls 13  (20.3%) than in boys
Total 27 169 (16)
14 (13.3%), and this was statistical significant (P = 0.001). χ2=1.349, P=0.72 (not significant)
There was an apparently higher trend of UTI in children with
kwashiorkor [Table 2]. The most common isolates were Gram
negative organisms that constituted 89% of isolates with Table 3: Etiologic agents of UTI in PEM and control
Escherichia coli (E. coli) accounting for 51.9% of the cases Etiologic PEM Controls
in children with PEM and 75.0% in the controls  [Table 3]. agent
n % n %
There was no statistically significant difference in the bacterial
E. coli 14 51.9 3 75
etiologic agents and the type of malnutrition (P = 1.00).
Klebsiella 5 18.5 1 25
All the bacterial isolates in PEM were highly sensitive to
Proteus 4 14.8 ‑ ‑
gentamycin and ciprofloxacin, whereas in the control all the
S. aureus 3 11.1 ‑ ‑
isolates were highly sensitive to gentamycin, ceftazidime, and
Pseudomonas 1 3.7 ‑ ‑
ciprofloxacin. However, the isolates showed poor sensitivity
Total 27 100% 4 100%
to amoxicillin, cotrimoxazole, nitrofurantoin, cefuroxime,
and chloramphenicol in children with PEM, whereas poor
sensitivity to amoxicillin, cotrimoxazole, and chloramphenicol the incidence of UTI was significantly higher in severely
was observed in the control group [Tables 4 and 5]. malnourished children.[17,18] The increase susceptibility to UTI
in PEM can be attributable to immunosuppression resulting
Only five (18.5%) of the subjects and two (50%) of the controls from impairment in the cell‑mediated immunity, depressed
with positive urine cultures had significant leucocyturia opsonic activity, and decreased phagocytosis.[9,19] Vitamin A
(10 WBC/mm 3). Dipstick urinalysis did not detect an deficiency and breakdown of anatomic barriers also contribute
appreciable proportion of children with culture proven UTI. In to their increased susceptibility to infection.[20]
the subjects, leucocyte esterase test was positive in 12 (44.4%),
nitrite test was positive in 8  (29.6%), and 7  (25.9%) had There was a preponderance of girls with UTI in PEM. This
no abnormality in their urinalysis, whereas in the controls agrees with most report on UTI in childhood[2,3,4], and this is
leucocyte esterase and nitrite were positive in only one of the also in agreement with Musa et al.[3] who reported more cases
patients with culture proven UTI. of UTI in females. However, the female preponderance outside
the neonatal period was not revealed in both the studies by
Discussion Babaoye[21] in Zaria, Reed et al.[15] and Kala et al.[19] in South
Africa, no reasons were given for their finding. The female
In this study, the prevalence of UTI in children with PEM preponderance of UTI found in this study can be explained
was 16.0% which was significantly higher than 2.4% in
by the close proximity of the urethral orifice to the anus and
well‑nourished children. This observation is in support of
the short female urethra that facilitates the ascents of bacteria
previous reports which showed that significant bacteriuria was
in the urinary tract.[2]
higher in children with PEM than that in the normal children.[14‑16]
This is also in accord with the study of Arvind et al.[4] where Most cases of UTI occurred in children with kwashiorkor.
it was reported that the incidence of UTI in malnourished This observation compared favorably with the works of
children was 15.2%, and in the controls subjects it was 1.8%. Reed et al.[15] and Adamu et al.[9] who found most cases of
Adamu et al.[9]in Maiduguri also found that incidence of UTI UTI occurring in children with kwashiorkor and marasmic
was higher in children with PEM. Similarly, previous studies kwashiorkor, respectively. However, this was in disagreement
within and outside this environment also demonstrated that with the report by Babaoye et al.[21] who found a higher

66 Nigerian Journal of Basic and Clinical Sciences  ¦  Volume 16  ¦  Issue 1  ¦  January-June 2019
 Ibrahim, et al.: UTI in children with PEM

Table 4: Pathogens causing UTI in PEM and their antibiotic sensitivity pattern
Organisms Antibiotic sensitivity pattern
n GM AM AU CO ND NF CEF CFT CFD CIP CPC

E. coli 14 14 8 10 6 9 5 6 11 14 14 7
Klebsiella spp 5 5 2 4 2 3 1 5 5 5 5 4
Proteus spp 4 4 1 2 3 1 1 1 3 2 4 1
Pseudomonas spp 1 1 1 0 1 1 1 0 1 1 1 0
S. aureus 3 3 1 2 0 1 1 1 1 1 3 1
Total 27 27 13 18 12 15 9 13 21 23 27 13
Percentage Total 100 48.1 66.6 44.4 55.5 33.3 48.1 77.7 85.1 100 48.1
*n: Number of isolates, GM: Gentamicin, AM: Amoxicillin, AU: Augmentin, CO: Cotrimoxazole, ND: nalidixic acid, NF: Nitrofurantoin,
CEF: Cefuroxime, CFT: Ceftriaxone, CFD: Ceftazidime, CIP: Ciprofloxacin, CPC: Chloramphenicol

Table 5: Pathogens causing UTI in control subjects and their antibiotic sensitivity pattern
Organism Antibiotic sensitivity pattern
n GM AM AU CO ND NF CEF CFT CFD CIP CPC
E. coli 3 3 0 2 1 2 2 1 2 3 3 2
Klebsiella spp 1 1 1 1 1 1 1 0 1 1 1 0
Total 4 4 1 3 2 3 3 1 3 4 4 2
Percentage total 100 50 75 50 75 75 25 75 100 100 50
*n: Number of isolates, GM: Gentamicin, AM: Amoxicillin, AU: Augmentin, CO: Cotrimoxazole, ND: Nalidixic acid, NF: Nitrofurantoin,
CEF: Cefuroxime, CFT: Ceftriaxone, CFD: Ceftazidime, CIP: Ciprofloxacin, CPC: Chloramphenicol

percentage in children with marasmus. The higher trend among
children with kwashiorkor may be ascribed to the fact that they
are more prone to infection because they have higher level of
serum aflatoxins which have been found to reduce resistance
to infection, by impairment of cell mediated immunity
and depression of complement activity.[22] Children with
kwashiorkor also have intrarenal edema, which predisposes
them to UTI.[23]
Poor leucocyte response was observed in children with PEM as
only 18.5% of them had significant leucocyturia as opposed to
50% of the control. This observation is similar to findings in a
previous study by Adamu et al.[9] were there was poor leukocyte
response in children with PEM, but in contrast to the study
by Arvind et al.[4] that showed that all the PEM patients with
significant bacteriuria had leucocyturia. The poor leucocytes
response in malnourished children may be due to impairment
of both the process of phagocytises and bactericidal activities
of polymorphonuclear cells.
Leucocyte esterase test was defective in detecting UTI in the
children with PEM and in the controls. This may be ascribed
to the fact that most UTI occurred in the 13–24 months age
group, and dipstick test has been shown to have poor sensitivity
in younger children because they tend to have lower colony
count per positive culture.[24]
Nitrite test was not useful in detecting UTI in this study.
This could be explained by the fact that the diets of these
patients may be lacking in nitrate containing food such as
beans, spinach, and cabbage, which are necessary to provide
significant substrate for the enzyme nitrate reductase.[25]
These foods may be inadequate in the diets of these patients.
Another factor that could also contribute to the nitrite test
being defective in detecting UTI is the fact that random urine
sample was used in this study. The time of urine specimen
collection has been reported to affect the sensitivity of the
nitrite test. The use of first morning urine sample results
in a higher sensitivity of the nitrite test than that in the use
of randomly collected urine sample.[26] The Gram negative
organisms were the predominant organisms isolated,
and they all belonged to the family enterobacteriaceae.
Enterobacteriaceae are noted to be the most common
organism isolated from most uncomplicated UTI.[12] E. coli
was the predominant organism isolated in this study. E. coli
was isolated in 51.9% and 75% of the case in PEM and the
controls, respectively. This pattern is similar to that obtained
in studies performed in the United States of America, Europe,
and West Africa.[3,9,18,27‑29] In another study in Ibadan by
Adeyemo et al.[30] findings showed that Klebsiella species
were the most common isolates, Pseudomonas aeruginosa
was the most prevalent isolate among symptomless children,
and Staphylococcus epidermidis was the most prevalent
among symptomatic children. These differences may be
because mainly older children were recruited in the Ibadan
studies, whereas in this study most children with UTI were
less than 2 years of age.
The presence of bacterial pili or fimbriae on the surface
of E. coli determines its specific invasive property. E. coli
carrying the type I fimbriae are the ones commonly implicated
in UTI.[8] The receptor for type I fimbriae is present on the
uroepithelial cell membrane and these enables attachment of

Nigerian Journal of Basic and Clinical Sciences  ¦  Volume 16  ¦  Issue 1  ¦  January-June 2019 67
 Ibrahim, et al.: UTI in children with PEM
E. coli to the uroepithelium. This may partly be the reason for
the preponderance of E. coli found in this study.
All the urinary isolates were sensitive to gentamycin,
ceftazidime, and ciprofloxacin. This is similar to a report by
Adedoyin et al.[31] in Ilorin. The sensitivity of this urinary
isolates to these antibiotics is higher than that reported in
Benin[3] and Ibadan.[32] The high sensitivity of the organisms
to gentamycin and ceftazidime found in this study could be
explained by low rate of abuse of these drugs as they are present
only in injectable forms.
Poor sensitivity to nalidixic acid, amoxicillin, clavulanic
acid‑potentiated amoxicillin, cotrimoxazole, and
chloramphenicol were observed. The resistance of most urinary
isolates to these antibiotics has also been described in previous
studies in Nigeria[9,30‑32] and in South Africa.[15,33] However,
this finding differs from that of Arvind et al.[4] in India who
reported high sensitivity to amoxicillin, cotrimoxazole,
and chloramphenicol. The observed poor sensitivities to
the commonly used antibiotics in this environment may be
attributable to indiscriminate use of over the counter drugs
occasioned by wide spread practice of self‑ medication,
inappropriate dosing, substandard preparation of the drug, and
possibly non‑ compliance.
Conclusion and Recommendations
The prevalence of UTI was higher among children with PEM.
This study revealed high prevalence of antibiotic resistance
to the commonly used antibiotics for UTI. It is recommended
that UTI should be actively investigated for and treated in
children with PEM. The regular surveillance of UTI pathogens
and their antibiotic sensitivity pattern in children with PEM
were important. Dipstick screening tests may not detect a
significant proportion of malnourished children with UTI and
should, therefore, not replace traditional culture methods if
these are available.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
1. Bhat RG, Katy TA, Place FC. Paediatric urinary tract infection. Med
Clin N Am 2011;29:637‑53.
2. Owa JA. Urinary tract infection in children. In: Azubuike JC,
Nkanginieme KEO editors. Paediatrics and Child Health In a Tropical
Region. 3rd ed. Owerri, Nigeria: African Educational Services;
2016.p. 982‑9.
3. Musa AA, Ibadin OM, Ukoh G, Akepede GO. Prevalence and
antimicrobial sensitivity pattern in urinary tract infection in febrile
under 5s at a children emergency unit in Nigeria. Ann Trop Paediatr
2003;23:39‑45.
4. Bagga A, Tripathi P, Jatana V, Hari P, Kapil A, Srivastava RN, et al.
Bacteriuria and urinary tract infections in malnourished children.
PediatrNephrol 2003;18:366‑70.
5. Alcoba G, Kerac M, Breysse S, Salpeteur C, Galetto‑Lacour A, Briend A,
68 Nigerian Journal of Basic and Clinical Sciences  ¦  Volume 16  ¦  Issue 1  ¦  January-June 2019
et al. Do children with uncomplicated severe acute malnutrition
need antibiotics? A systematic review and meta‑analysis. PLOS One
2013;8:e53184.
6. Iyer SS, Chatraw JH, Tan WG, Wherry EJ, Becker TC, Ahmed R,
et al. Protein energy malnutrition impairs homeostatic proliferation of
memory CD8 T cells. J Immunol 2012;188:77‑84.
7. Ulasi TO, Joy E. Nutritional disorders in childhood. In: Azubuike JC,
Nkanginieme KEO editors. Paediatrics and Child Health in a
Tropical Region. 3rd ed. Owerri, Nigeria: Africa Educational Services;
2016.p. 701‑18.
8. Elder JS. Urologic disorders in infants and children. In: Behrman RE,
Kliegman RM, Jenson HB editors. Nelson Textbook of Paediatrics.
18th ed. Philadelphia: W. B Saunders Company; 2007.p. 1619‑58.
9. Adamu IR, Daniel S. Urinary tract infection in severely malnourished
children at the university of Maiduguri teaching hospital, Maiduguri
Nigeria. J Trop Pediatr 2002;48:359‑61.
10. Hendrickse RT. Protein energy malnutrition. In: Hendrickse RC.
Barr DGD, Mathews TS, editors. Paediatrics in the Tropics. London:
Blackwell Scientific Publications; 1991. p. 119‑31.
11. American Academy of Pediatrics Committee on Quality improvement
subcommittee on Urinary Tract Infection. Practice parameter: The
diagnosis, treatment and evaluation of initial urinary tract infection in
febrile infants and young children. Pediatrics 1999;103:843‑52.
12. Srivastava RN, Arvind B. Urinary tract infection. In: Paediatric
Nephrology. 4th ed. New Delhi: Jaypee Brother Medical Publishers (P)
LTD; 2005.p. 235‑63.
13. Winstanley TG, Limb DI, Egging R, Hancock F. A 10 year survey
of urinary tract isolates in the UK: The microbe base project.
J AntimicrobChemother 1997;40:591‑4.
14. Ojuawo A, Nwafor AC. Urinary tract infection in children with severe
protein energy malnutrition. Nig Med Pract 1994;28:6‑8.
15. Reed RP, Wegerhoff FO. Urinary tract infection in malnourished rural
African children. Ann Trop Paediatr 1995;15:21‑6.
16. Banapurmath CR, Jayamony S. Prevalence of urinary tract infection in
children in severely malnourished preschool children. Indian Paediatr
1994;31:679‑89.
17. Muzamil S, Imran RA, Huma Z. Clinical pattern of infections in
malnourished children. Pediatrics 2010;16:352‑56.
18. Uduak AO, Danlami G, Augustin EF, Secka O, Ikumapayi UN, Udo JJ,
et al. Bacterial isolates and antibiotic sensitivity among Gambian
children with severe acute malnutrition. Int J Pediatr 2011;2011:825123.
19. Kala UK, Jacobs DW. Evaluation of urinary tract infection in
malnourished black children. Ann Trop Paediatr 1992;12:75‑81.
20. Rytter MJ, Kolte L, Brind A, Friis H, Christen VB. The immune
system inchildren with malnutrition. A systematic review.PLoS One
2014;9:e105017.
21. Babaoye F, Ogala W. Dysuria in infancy and childhood an analysis of
42 children presenting in the Paediatric outpatient clinic. East Afr Med J
1991;68:860‑4.
22. Hendrickse RG. Infleunce of aflatoxins on child health in the tropics with
reference to kwashiorkor. Trans Roy Soc Med Hyg 1984;78:427‑35.
23. Ighogboja IS, Angyo I, Okolo AA, Szlachetka R. Morbidity and
mortality pattern of paediatric emergencies in Jos. Nig Med Pract
1995;30:15‑8.
24. Shaw KN, Hexter D, McGowan KL, Schwartz JS. Clinical evaluation of
a rapid screening test for UTI in children. J Pediatr 1991;118:733‑6.
25. Shelton IJ, Hogan MM, Stokes B, Hurst JA. Urinary tract infection in
childhood: The place of the nitrite test. Med J Aust 1977;1:882‑6.
26. Czerwinski AW, Wilkerson RG, Merril JA, Braden B, Colmore JP.
Further evaluation of the Greiss test to detect significant bacteriuria. Am
J Obstet Gynecol 1971;110:677‑81.
27. Riccabona M. Urinary tract infection in children. CurrOpinUrol
2003;13:59‑62.
28. Kozer E, Rosenbloom E, Goldman D.Pain in infants who are
younger than 2 months during suprapubic aspiration and transurethral
bladder catheterisation: A randomised controlled study. Pediatrics
2006;118:e51‑6.
29. Wammanda K. Urinary tract pathogens and their antimicrobial
sensitivity pattern in children. Ann Trop Paediatr 2002;22:197‑8.
30. Adeyomo AA, Gbadegesin RA, Onyemenem TN, Ekweozor CC.
 Ibrahim, et al.: UTI in children with PEM

Urinary tract pathogens and antimicrobial sensitivity pattern in Ibadan,
Nigeria. Ann Trop Paediatr 1994;14:271‑4.
31. Adedoyin OT, Oyeyemi BO, Aiyedehin O. Screening of febrile children
on admission for UTI. Afr J ClinExp microbial 2003;4:56‑62.
32. Elegbe IA, Elegbe I, Amuson K. Screening for urinary tract infection
in asymptomatic elementary schoolchildren in Ile‑ife Nigeria. J Trop
Paediatr 1993;20:84‑8.
33. Jeena, PM, Coovadia, HM, Adhikari, MA. A prospective study of
bacteriuria and pyuria in catheter specimens from hospitalised children,
Durban South Africa. Ann Trop Paediatr 1995;15:153‑8.

Nigerian Journal of Basic and Clinical Sciences  ¦  Volume 16  ¦  Issue 1  ¦  January-June 2019 69
Copyright of Nigerian Journal of Basic & Clinical Sciences is the property of Wolters Kluwer
India Pvt Ltd and its content may not be copied or emailed to multiple sites or posted to a
listserv without the copyright holder's express written permission. However, users may print,
download, or email articles for individual use.