Nigerian Journal of Basic and Clinical Sciences

: 2019  |  Volume : 16  |  Issue : 1  |  Page : 64--69

Urinary tract infection in children with protein-energy malnutrition in Aminu Kano Teaching Hospital Kano, Northwest Nigeria

Umma Abdulsalam Ibrahim1, Henry A Aikhionbare2, Ibrahim Aliyu1,  
1 Department of Paediatrics, Bayero University Kano/Aminu Kano Teaching Hospital, PMB 3452, Kano, Nigeria
2 Department of Child Health, University of Benin Teaching Hospital, PMB 1111, Benin City, Nigeria

Correspondence Address:
Dr. Umma Abdulsalam Ibrahim
Department of Paediatrics, Aminu Kano Teaching Hospital, PMB 3452, Kano


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.

How to cite this article:
Ibrahim UA, Aikhionbare HA, Aliyu I. Urinary tract infection in children with protein-energy malnutrition in Aminu Kano Teaching Hospital Kano, Northwest Nigeria.Niger J Basic Clin Sci 2019;16:64-69

How to cite this URL:
Ibrahim UA, Aikhionbare HA, Aliyu I. Urinary tract infection in children with protein-energy malnutrition in Aminu Kano Teaching Hospital Kano, Northwest Nigeria. Niger J Basic Clin Sci [serial online] 2019 [cited 2020 Sep 27 ];16:64-69
Available from:

Full Text


Urinary tract infection (UTI) is a common cause of childhood morbidity and mortality in most developing countries.[1],[2] It is the second most common bacterial infection in children, and perhaps the most common disease of the urogenital tract, which can lead to substantial morbidity that may not be limited to the acute period of illness.[2] UTI is the most common occult bacterial cause of unexplained fever, especially in children less than 2 years.[3] Immaturity of the immune system in young children may predispose them to higher risk of septicemic and bacteremic illnesses, and the urinary tract may become seeded by these invasive organisms during such episodes.[3] UTI can result in recognition of an important underlying structural or neurogenic abnormality of the urinary tract. Another possible reason for the high prevalence of UTI in this age group is due to the presence of structural anomalies of the urinary tract, which can predispose to UTI.[3] If UTI is untreated, it can lead to kidney damage; this includes kidney scars, poor kidney growth and function, which may predispose to high blood pressure, and end-stage kidney disease. Therefore, children with UTI should receive prompt treatment and a careful evaluation of the urinary tract for structural anomalies. UTI is more common in malnourished children than in their well-nourished counterparts,[4] and the risk of UTI increases with the severity of malnutrition.[4] Therefore, understanding the relationship between PEM and UTI is of great public health importance. Severe acute malnutrition is associated with immune deficiency, which expectedly renders affected children more vulnerable to severe infections.[5],[6],[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-[10]

Urine sample was collected from each child into a sterile universal container with 1.8% boric acid using percutaneous 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 test and Fisher's exact test were used for association between categorical variables and to determine statistical significance. A P–value of < 0.05 was considered statistically significant.


Overall, 169 children with PEM and 169 well-nourished age 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 20.6 ± 9.2. More than half of the children with PEM had marasmus.

In total, 27 (16%) of the subjects and 4 (2.4%) of the control group had UTI. The difference was statistically significant (χ2 = 17.19, P = 0.001) [Table 1]. Sixty-four percent of the cases of UTI occurred in the age groups 13–24 months. UTI was more common in girls 13 (20.3%) than in boys 14 (13.3%), and this was statistical significant (P = 0.001). 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 Escherichia coli (E. coli) accounting for 51.9% of the cases in children with PEM and 75.0% in the controls [Table 3]. There was no statistically significant difference in the bacterial etiologic agents and the type of malnutrition (P = 1.00). All the bacterial isolates in PEM were highly sensitive to gentamycin and ciprofloxacin, whereas in the control all the isolates were highly sensitive to gentamycin, ceftazidime, and ciprofloxacin. However, the isolates showed poor sensitivity to amoxicillin, cotrimoxazole, nitrofurantoin, cefuroxime, and chloramphenicol in children with PEM, whereas poor sensitivity to amoxicillin, cotrimoxazole, and chloramphenicol was observed in the control group [Table 4] and [Table 5].{Table 1}{Table 2}{Table 3}{Table 4}{Table 5}

Only five (18.5%) of the subjects and two (50%) of the controls with positive urine cultures had significant leucocyturia (10 WBC/mm3). Dipstick urinalysis did not detect an appreciable proportion of children with culture proven UTI. In the subjects, leucocyte esterase test was positive in 12 (44.4%), nitrite test was positive in 8 (29.6%), and 7 (25.9%) had no abnormality in their urinalysis, whereas in the controls leucocyte esterase and nitrite were positive in only one of the patients with culture proven UTI.


In this study, the prevalence of UTI in children with PEM was 16.0% which was significantly higher than 2.4% in well-nourished children. This observation is in support of previous reports which showed that significant bacteriuria was higher in children with PEM than that in the normal children.[14],[15],[16] This is also in accord with the study of Arvind et al.[4] where it was reported that the incidence of UTI in malnourished children was 15.2%, and in the controls subjects it was 1.8%. Adamu et al.[9] in Maiduguri also found that incidence of UTI was higher in children with PEM. Similarly, previous studies within and outside this environment also demonstrated that the incidence of UTI was significantly higher in severely malnourished children.[17],[18] The increase susceptibility to UTI in PEM can be attributable to immunosuppression resulting from impairment in the cell-mediated immunity, depressed opsonic activity, and decreased phagocytosis.[9],[19] Vitamin A deficiency and breakdown of anatomic barriers also contribute to their increased susceptibility to infection.[20]

There was a preponderance of girls with UTI in PEM. This agrees with most report on UTI in childhood[2],[3],[4], and this is also in agreement with Musa et al.[3] who reported more cases of UTI in females. However, the female preponderance outside the neonatal period was not revealed in both the studies by 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 preponderance of UTI found in this study can be explained by the close proximity of the urethral orifice to the anus and the short female urethra that facilitates the ascents of bacteria in the urinary tract.[2]

Most cases of UTI occurred in children with kwashiorkor. This observation compared favorably with the works of Reed et al.[15] and Adamu et al.[9] who found most cases of UTI occurring in children with kwashiorkor and marasmic kwashiorkor, respectively. However, this was in disagreement with the report by Babaoye et al.[21] who found a higher 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],[28],[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 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],[31],[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


Conflicts of interest

There are no conflicts of interest.


1Bhat RG, Katy TA, Place FC. Paediatric urinary tract infection. Med Clin N Am 2011;29:637-53.
2Owa 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.
3Musa 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.
4Bagga 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.
5Alcoba G, Kerac M, Breysse S, Salpeteur C, Galetto-Lacour A, Briend A, et al. Do children with uncomplicated severe acute malnutrition need antibiotics? A systematic review and meta-analysis. PLOS One 2013;8:e53184.
6Iyer 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.
7Ulasi 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.
8Elder 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.
9Adamu 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.
10Hendrickse RT. Protein energy malnutrition. In: Hendrickse RC. Barr DGD, Mathews TS, editors. Paediatrics in the Tropics. London: Blackwell Scientific Publications; 1991. p. 119-31.
11American 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.
12Srivastava RN, Arvind B. Urinary tract infection. In: Paediatric Nephrology. 4th ed. New Delhi: Jaypee Brother Medical Publishers (P) LTD; 2005.p. 235-63.
13Winstanley 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.
14Ojuawo A, Nwafor AC. Urinary tract infection in children with severe protein energy malnutrition. Nig Med Pract 1994;28:6-8.
15Reed RP, Wegerhoff FO. Urinary tract infection in malnourished rural African children. Ann Trop Paediatr 1995;15:21-6.
16Banapurmath CR, Jayamony S. Prevalence of urinary tract infection in children in severely malnourished preschool children. Indian Paediatr 1994;31:679-89.
17Muzamil S, Imran RA, Huma Z. Clinical pattern of infections in malnourished children. Pediatrics 2010;16:352-56.
18Uduak 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.
19Kala UK, Jacobs DW. Evaluation of urinary tract infection in malnourished black children. Ann Trop Paediatr 1992;12:75-81.
20Rytter MJ, Kolte L, Brind A, Friis H, Christen VB. The immune system inchildren with malnutrition. A systematic review.PLoS One 2014;9:e105017.
21Babaoye 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.
22Hendrickse RG. Infleunce of aflatoxins on child health in the tropics with reference to kwashiorkor. Trans Roy Soc Med Hyg 1984;78:427-35.
23Ighogboja IS, Angyo I, Okolo AA, Szlachetka R. Morbidity and mortality pattern of paediatric emergencies in Jos. Nig Med Pract 1995;30:15-8.
24Shaw KN, Hexter D, McGowan KL, Schwartz JS. Clinical evaluation of a rapid screening test for UTI in children. J Pediatr 1991;118:733-6.
25Shelton 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.
26Czerwinski 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.
27Riccabona M. Urinary tract infection in children. CurrOpinUrol 2003;13:59-62.
28Kozer 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.
29Wammanda K. Urinary tract pathogens and their antimicrobial sensitivity pattern in children. Ann Trop Paediatr 2002;22:197-8.
30Adeyomo AA, Gbadegesin RA, Onyemenem TN, Ekweozor CC. Urinary tract pathogens and antimicrobial sensitivity pattern in Ibadan, Nigeria. Ann Trop Paediatr 1994;14:271-4.
31Adedoyin OT, Oyeyemi BO, Aiyedehin O. Screening of febrile children on admission for UTI. Afr J ClinExp microbial 2003;4:56-62.
32Elegbe 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.
33Jeena, 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.