|Year : 2019 | Volume
| Issue : 4 | Page : 843-852
|Prevalence and Pattern of Human Immunodeficiency Virus-Associated Nephropathy among Human Immunodeficiency Virus-Positive Children at the University of Maiduguri Teaching Hospital, Nigeria
Halima Umar Ibrahim1, Hassan Abdullahi Elechi2, Adamu Ibrahim Rabasa2, Garba Mohammed Ashir2, Abubakar Garba Farouk2, Mohammed Saad Yauba2, Bello Abdullahi Ibrahim2
1 Department of Pediatrics, Federal Medical Center, Birnin-Kudu, Jagawa State, Nigeria
2 Department of Pediatrics, College of Medical Sciences, University of Maiduguri, Maiduguri, Nigeria
Click here for correspondence address and email
|Date of Submission||10-Apr-2018|
|Date of Acceptance||09-May-2018|
|Date of Web Publication||27-Aug-2019|
| Abstract|| |
The kidney is an important target organ in human immunodeficiency virus (HIV) infection, and a variety of renal disorders could occur throughout the course of the disease. HIV- associated nephropathy (HIVAN) is the most common form of kidney disease resulting directly from HIV infection. The true prevalence of HIVAN among infected African children is unknown largely due to lack of surveillance and reporting. We thus aimed to determine the prevalence of HIVAN and associated factors among HIV-infected children at the University of Maiduguri Teaching Hospital. This was a cross-sectional study carried out at the Pediatric Infectious Clinic. Children aged ≤15 years were recruited through systematic random sampling. Relevant sociodemographic and clinical information were obtained. Spot urine sample was analyzed using a multistix (Combi-Screen 10SL Analyticon Biotechnologies AG, Germany), and proteinuria of ≥2+ was considered significant. The CD4+ count and CD4+% (for those <5 years) were obtained using a PARTEC™ CD4+ easy count kit. The obtained data were entered and analyzed using Statistical Package for the Social Sciences version 16.0. A total of 250 children were recruited. Eighty-five (34%) of them had HIVAN. Sex, social class, and mode of transmission were not significantly associated with HIVAN (P >0.05). However, age, medication status (highly active antiretroviral therapy [HAART]), duration on HAART, and disease severity (both clinical and immunological) all had a significant association to HIVAN (p = 0.005, 0.004, 0.008, and <0.001, respectively). These factors also showed a positive but weak correlation to HIVAN; while age had the least correlation coefficient (0.157), immunological class had the highest r = 0.458. However, these relationships were all significant (P <0.5). HIVAN is highly prevalent among children living with HIV in Maiduguri. Routine screening through urina-lysis and early commencement of HAART is recommended.
|How to cite this article:|
Ibrahim HU, Elechi HA, Rabasa AI, Ashir GM, Farouk AG, Yauba MS, Ibrahim BA. Prevalence and Pattern of Human Immunodeficiency Virus-Associated Nephropathy among Human Immunodeficiency Virus-Positive Children at the University of Maiduguri Teaching Hospital, Nigeria. Saudi J Kidney Dis Transpl 2019;30:843-52
|How to cite this URL:|
Ibrahim HU, Elechi HA, Rabasa AI, Ashir GM, Farouk AG, Yauba MS, Ibrahim BA. Prevalence and Pattern of Human Immunodeficiency Virus-Associated Nephropathy among Human Immunodeficiency Virus-Positive Children at the University of Maiduguri Teaching Hospital, Nigeria. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2020 Nov 26];30:843-52. Available from: https://www.sjkdt.org/text.asp?2019/30/4/843/265460
| Introduction|| |
Human immunodeficiency virus (HIV) pandemic has remained an important public health issue globally with the sub-Saharan Africa subcontinent being the greatest hit. Nigeria is known to have the largest number of HIV positive children in the world. Prior to improved access to standard therapy of HIV disease, African children frequently died early from diarrhea-induced dehydration or respiratory infections. However, with more patients having access to diagnosis and treatment with (highly active antiretroviral therapy [HAART]), in addition to other supporting managements, there is a concomitant increase of survival of African children with HIV. Thus, HIV-infected children who would have succumbed to the disease now run a chronic course of the illness with long-term multisystem complications such as renal disease and cardiomyopathy.
The kidney is an important target organ in HIV infection, and a variety of renal disorders could occur through the course of the disease. HIV-associated nephropathy (HIVAN), the most common form of kidney disease resulting directly from HIV infection, is characterized by proteinuria, normal blood pressure (BP), elevated serum creatinine, normal to large echogenic kidneys on ultrasound imaging, and collapsing focal and segmental glomerulo-sclerosis on renal biopsy. This disorder may relentlessly progress to end-stage renal disease within 8–16 weeks with mortality approaching 100% within six months of onset of uremia. The mechanism underlying renal involvement in HIV-infected patients is still poorly understood, but both genetic factors,,, and direct viral invasion,,, are known to play significant roles in the pathogenesis of the disease.
The true prevalence of HIVAN among infected African children is unknown, largely due to lack of surveillance and reporting. In Nigeria, Esezobor et al, using the presence of proteinuria, reported a prevalence of 20.5% among HIV-infected children from Lagos, South West Nigeria, while Ikpeme et al found a higher prevalence of 31.6% using a more sensitive microalbuminuria from Uyo, South South Nigeria. A prevalence of 24% was reported from South Africa among 615 HIV infected children. Previous studies from the USA and Asia have reported a lower prevalence of 15% and 10.7%, respectively, using the presence of significant proteinuria. The higher prevalence from African studies may be partly due to race. The black race has been found in several studies to be an important risk factor for the development of HIVAN.,,,
HIVAN is the most widely recognized cause of proteinuria in HIV-infected African-American children., Proteinuria is believed to be the earliest and most consistent clinical finding for the diagnosis of HIVAN. Renal ultrasound scan (USS) and renal biopsy are other means of diagnosing HIVAN, but both are more expensive and require more expertise. Biopsy in addition is quite invasive, and the desired structural changes might not be picked in early cases with both USS and biopsy. Hence, protei-nuria remains the most feasible screening tool in a poor setting like ours.
We thus undertook this study to determine the prevalence of HIVAN and associated factors among HIV-infected children receiving care at the University of Maiduguri Teaching Hospital, Nigeria.
| Materials and Methods|| |
This cross-sectional study was conducted over a period of eight months between February and October 2014 at the Pediatric Infectious Disease Clinic of the University of Maiduguri Teaching Hospital, Borno State, located in the northeastern region of Nigeria. The Infectious Disease Clinic runs twice a week, Tuesdays and Fridays, with an average patient load of 50–60 patients per week.
The study population was HIV-infected children aged 15 years and below attending the Pediatric Infectious Disease Clinic of the University of Maiduguri Teaching Hospital. The minimum sample size was determined using Taylor’s formula (n = Z2pq/d2). The prevalence of proteinuria was taken at 20.5% from a previous study. The calculated minimum sample size was 250 participants.
The participants were selected using systematic random sampling. The sampling interval “K = 4” was determined by dividing total number of registered HIV-positive children (n = 1012) by the minimum sample size (n = 250). On each clinic day, patients were numbered as they registered; the first participant was selected by simple balloting of the first four participants to register and subsequently every 4th participant. In case of noneligibility, the next patient who fulfilled the eligibility criteria was selected. Age of ≤15 years with verifiable positive HIV test result defined as two positive DNA polymerase chain reaction for those aged <18 months and two positive antibody test for those aged >18 months were eligible. Those with sickle cell anemia or hepatitis B and C virus infections or whose parents declined consent were excluded.
The study protocol was reviewed and approved by the Research and Ethics Committee of our institution. A signed informed consent form was obtained from the parents/caregivers after passing adequate information regarding the research. Each parent/caregiver had unlimited liberty to decline without any consequence. The research material and information obtained were treated with utmost confidentiality; the result of the urinalysis was discussed with parents, and those with proteinuria or other abnormal findings were referred to the pediatric nephrology unit for further evaluation.
On the day of enrollment, information on biodata, sociodemographic features, detailed clinical features, and anthropometric measurements were obtained and recorded in a structured questionnaire. Information obtained included patient age, sex, parents’ educational attainment, and occupation. Others included age at diagnosis, mode of transmission, duration on HAART, and the HAART regimen and clinical features at enrollment such as fever, skin rashes, cough, wasting, ear discharge, oral thrush, lymphadenopathy, difficulty in breathing, pallor, facial puffiness, and edema. The weight and height were measured to the nearest 0.05 kg and 0.5 cm, respectively, using Wunder’s stadio- meter fitted with a weighing scale. The weighing scale was adjusted to zero reading before each weighing, and a standard weight of 10 kg was used every day to recalibrate the scale. The height was measured with the child standing erect, and the head was positioned such that the Frankfurt plane was horizontal. Arms were hanging loosely at the side with palms facing the thigh. The movable headboard was then gently lowered until it could touch the crown of the head. The height measurement was taken with the examiner’s eyes leveled with the headboard to avoid parallax error. For younger children or very ill ones who could not stand erect, a measuring board was used with the help of an assistant. Socioeconomic status of the children was determined from the parents’ educational attainment and occupation using Oyedeji ‘s model. BP (mm Hg) was measured using Accuson’s mercury sphygmomanometer with appropriate cuffs. Systolic and diastolic BP was indicated by the 1st and 5th Korotkoff sounds, respectively. Two measurements were taken and the average of the two was recorded as the BP. BP was categorized using appropriate nomogram for age, sex, and height, into normal, high, or low.
The clinical features and anthropometry were used in staging the patients as per the World Health Organization (WHO) clinical staging for infants and children. The WHO clinical Stages 1 and 2 were defined as nonadvanced disease, while Stages 3 and 4 were advanced disease. Age categorization was based on the WHO immunological classification of HIV infection in children.
On the day of recruitment into the study, 2.5 mL of venous blood was collected using aseptic technique into ethylenediaminetetraacetic acid (EDTA) bottle for hepatitis B surface antigen (HBsAg) and hepatitis C virus antibody (HCVAb) screening as well as CD4+ count and CD4+% enumeration.
Hepatitis B surface antigen and hepatitis C virus antibody screening
Screening for HBsAg and HCVAb was carried out using micropoint HBsAg and HCVAb gold rapid screen test for the qualitative detection of the viruses. A drop of blood was added onto the sample pad strip. After the blood was completely absorbed, a drop of whole blood diluent was added. Results were read in 5–20 min as per manufacturer’s instructions. Patients found to be positive for either HBsAg or HCVAb were excluded from further analysis and the study.
CD4+ count and CD4+ percentage estimation
The CD4+ count and CD4+% (for children <5 years) were obtained using a PARTEC™ CD4+ easy count kit. Twenty microliters (μL) of blood (EDTA as anticoagulant) was dropped into a PARTEC™ easy count test tube using pipette. Twenty μL of CD4+ mouse antibody (mAb) PE was added to the blood and gently mixed and allowed to incubate for 15 min at room temperature. Eight hundred μL of no lyse buffer was added and mixed thoroughly. The mixed sample was analyzed on a PARTEC™ (GmbH Gorlitz Germany) flow cytometer, with an excitation light source of 488 nM or 532 nM. Enumeration of CD4+ count and percentage was done as per manufacturer’s instruction in the presence of the investigator. Using the WHO age-related CD4 count and CD4% values, the children were stratified into four groups: no significant immunosuppression, mild immuno-suppression, advanced immunosuppression, and severe immunosuppression. However, for this study, both no significant and mild immunosup- pression were grouped as nonsevere immuno- suppression, while both advanced and severe suppression were grouped together as severe immunosuppression.
Spot urine sample was collected in a universal bottle. The urine was analyzed by the investigator using a multistix (Combi-screen 10SL Analyticon Biotechnologies AG, Germany). The test strip was immersed into the freshly voided urine for approximately 2–3 s, making sure that all the color pads on the strip were completely immersed in the urine as recommended by the manufacturers. It was drawn across the rim of the container to remove excess urine. It was then read after 60 s to allow reaction of embedded chemicals with urine for semi-quantitative analysis as appropriate. This was done under optimum light conditions by aligning the strip to the standard color-coded guide. Proteinuria which was more specific to albumin on dipstick was reported as negative, 1+ (30 mg/dL), 2+ (100 mg/dL), 3+ (300 mg/ dL), or 4+ (1000 mg/dL). Significant protei-nuria (defined as the presence of 2+ or more of protein in urine), urine specific gravity, glucose, blood, pH, and nitrite were checked. All urine samples were analyzed within 2 h of collection as recommended by the manufacturer.
| Statistical Analysis|| |
The data were collected, entered, and cleaned in a computer. Analysis was done using Statistical Package for the Social Sciences (SPSS) version 16.0 (SPSS, Chicago, IL, USA). Values were expressed as mean ± standard deviation (mean ± SD). Both numerical and categorical variables were generated. Student’s t-test was used to test differences between means of continuous variable, and Chi-square and Fisher’s exact tests were used where applicable for categorical variables. Correlation between immunological status (CD4+ count and CD4+%), WHO clinical stage, and HIVAN were performed using Spearman’s rank correlation. Logistic regression was performed to assess the relationship between study variables and HIVAN. P <0.05 was considered significant. Tables and Figure were used for illustrations as appropriate.
| Results|| |
A total of 250 patients were recruited for the study. The children were aged between five months and 180 months, with a mean ± SD age of 89.02 ± 47.95 months. Majority [163 (65.2%)] were aged ≥60 months, and infants were the least in number 18 (7.2%). There were 116 (46.4%) males and 134 (53.6%) females, with a male-to-female ratio (M:F) of approximately 1:1.1. One hundred and thirty-seven (54.8%) were of low social class, while 40 (16.0%) were of upper social class [Table 1].
Treatment modalities, mode of disease transmission, and clinical and immunological disease severity are shown in [Table 2]. One hundred and fifty-seven children (62.8%) were on HAART for a period ranging from 1 to 168 months, with a mean duration of 66.06 ± 46.47 months. One hundred and forty-three children (91.1%) on HAART were on a regimen consisting of zidovudine, lamivudine, and nevirapine. The remaining 14 patients (8.9%) were on other regimens including either abacavir or efavirenz in place of nevirapine. Twenty of the 250 participants (8%) were on antituberculous treatment; of these, six were on HAART. Majority of the study population [231 (92.4%)] acquired the infection through vertical transmission. Mode of transmission could not be ascertained in 14 patients who were mostly adolescents. A total of 93 participants (37.2%) had advanced disease comprising WHO clinical Stages 3 and 4. One hundred and three (41.2%) had advanced or severe immunosuppression.
|Table 2: Frequency distribution of the use of medications, modes of transmission, disease severity, and immunosuppression among human immunodeficiency virus-infected patients.|
Click here to view
A total of 85 (34%) of the study population had HIVAN based on significant proteinuria ≥2+; of these, 27 (31.8%) had nephrotic-range proteinuria ≥3+ [Figure 1].
Among the group with proteinuria, 67 participants (78.8%) were aged ≥60 months, 51 (60%) were of low socioeconomic class, 50 (58.8%) had advanced HIV disease, and 63 (74.1%) had severe immunosuppression, while 57 (67.1%) were either HAART naive or <1 year on HAART. Gender, social class, and mode of transmission were not significantly associated with significant proteinuria (P >0.05). However, age, medication (HAART) status, duration on HAART, and disease severity (both clinical and immunological) were significantly associated with significant protei- nuria (P = 0.005, 0.004, 0.008, and <0.001, respectively; [Table 3]).
|Table 3: Human immunodeficiency virus disease and occurrence of proteinuria.|
Click here to view
The mean ± SD systolic and diastolic BP among those with significant proteinuria was 103.06 ± 13.00 and 61.71 ± 9.49, respectively. Children without significant proteinuria had mean ± SD systolic and diastolic BP of 95.30 ± 11.66 and 57.30 ± 8.84, respectively. Although the mean ± SD BP of both groups were within normal limits, those with significant proteinuria had significantly higher BP, t = -4.79 and -3.64 for systolic and diastolic BP, respectively; P <0.001 in both.
[Table 4] shows the strength and direction of relationship between HIVAN and some of the factors with a significant association. All the factors showed a positive but weak correlation to HIVAN, while age had the least correlation coefficient (0.157) and immunological class had the highest r = 0.458. However, these relationships were all significant (P <0.5).
|Table 4: Spearman correlation between human immunodeficiency virus-associated nephropathy and selected factors.|
Click here to view
The effect of various factors on the prevalence of HIVAN is depicted in the binary logistic regression in [Table 5]. While infants were 0.5 times less likely to have HIVAN, children aged 13–59 months were 1.2 times more likely when compared to those aged ≥60 months. These effects of age were, however, not significant; P values are 0.555 and 0.709, respectively. Similarly, sex and social class had no significant effect on the prevalence of HIVAN. In contrast, children who were on HAART had nonsevere immunosuppression and nonadvanced clinical diseases and were less likely to have HIVAN when compared to those who were not on HAART, who had severe immunosuppres- sion and advanced disease.
|Table 5: Effect of various factors on human immunodeficiency virus-associated nephropathy.|
Click here to view
| Discussion|| |
The prevalence of 34.0% for HIVAN recorded in this study is quite high underscoring the need for routine screening of all HIV-positive children. It is similar to the findings of Ikpeme et al from Uyo but higher than that reported in the studies by Esezobor et al from Lagos and Iduoriyekemwen et al from Benin. The difference between the finding of the present study and that from Lagos may be due to the differences in the definition of proteinuria. While proteinuria of 2+ on dipstick was considered significant proteinuria in this study, the Lagos study used urine protein–creatinine ratio which is more specific than dipstick in diagnosing renal disorder. In addition, more than one-third of the study population had advanced HIV/AIDS disease, and it has been demonstrated in this study and others,,,,, that HIVAN occurs in a setting of severe immuno-suppression. The lower prevalence reported by Benin could be because all the studied patients were on HAART with relatively higher CD4 count compared to this study where 57 (67.1%) of those with significant proteinuria were either HAART naive or recently commenced therapy. Similarly, the lower prevalence documented by Strauss et al and Ray et al from America may be due to the racial differences between this study and theirs. It is known that black race is an important risk factor for HIVAN, which constitutes 100% of the present study population. The American studies included both blacks and Caucasians.
Similar to previous studies,,,, age had a significant association and positive correlation to HIVAN. The reason for this predilection could be because older children have supposedly longer duration of exposure to HIV. The natural course of HIV infection is such that with increasing duration of exposure, there is disease progression.
Although advanced disease and older age were significantly associated with a higher prevalence of HIVAN in this study, people living with HIV may present with HIVAN before developing other symptoms of AIDS or even during acute seroconversion illness. This was corroborated in this study as age failed to demonstrate a significant effect on logistic regression. This is in conformity with the findings of Anochie et al where duration from HIV infection to development of HIVAN ranged from five months to 10 years, and renal disease was the first manifestation of HIV infection in 60% of patients with HIVAN. It is possible that acquisition of HIV at a time when the kidneys are still developing may predispose to renal disease earlier in children compared to adults.
There was a significantly lower prevalence of HIVAN among patients using HAART. In addition, the prevalence further reduced with increasing duration of HAART use. This finding, however, is in contrast to that reported by Ikpeme et al and Esezobor et al who did not find any significant relationship between HAART use and prevalence of HIVAN. This difference may not be unconnected to the fact that the median duration of HAART use in this study was much higher than the Lagos and Uyo studies., Similar to our findings, other authors, have reported a significant remission in renal disease by both clinical and histopathological criteria following commencement on HAART. It is known that the use of HAART over time suppresses viral load and direct viral inversion of the kidney plays an important role in the pathogenesis of HIVAN.,,, Hence, suppression of viral load may explain the pattern observed among those on HAART in this study.
The mean systolic and diastolic BP was within normal limit for age, sex, and height in patients with HIVAN in this study. This is in tandem with findings of other studies that hypertension is not a feature of HIVAN., BP in HIVAN has been described as normal, and if raised, it is recommended that other causes of hypertension including other nephropathies should be excluded., This finding is thought to result from the propensity of the kidneys in HIVAN to lose salt and water., The observed higher mean BP among those with HIVAN in comparison to those without significant proteinuria may be due to the significantly higher age of those with HIVAN demonstrated in this study.
| Conclusion|| |
HIVAN is highly prevalent among children living with HIV in Maiduguri. Routine screening of all HIV-positive children using dipstick and early initiation of therapy with HAART would go a long way in reducing the burden of renal disease among these children.
| References|| |
Pantaleo G, Graziosi C, Fauci AS. The immuno-pathogenesis of human immunodeficiency virus infection. N Engl J Med 1993;328:327-35.
McCulloch MI. Introduction to paediatric HIV disease. Paediatr Nephrol 2007;22:298.
Seney FD Jr., Burns DK, Silva FG. Acquired immunodeficiency syndrome and the kidney. Am J Kidney Dis 1990;16:1-3.
Weiner NJ, Goodman JW, Kimmel PL. The HIV-associated renal diseases: Current insight into pathogenesis and treatment. Kidney Int 2003;63:1618-31.
Herman ES, Klotman PE. HIV-associated nephropathy: Epidemiology, pathogenesis, and treatment. Semin Nephrol 2003;23:200-8.
Winston JA, Burns GC, Klotman PE. The human immunodeficiency virus (HIV) epidemic and HIV-associated nephropathy. Semin Nephrol 1998;18:373-7.
Ahuja TS, Grady J, Khan S. Changing trends in the survival of dialysis patients with human immunodeficiency virus in the United States. J Am Soc Nephrol 2002;13:1889-93.
Bourgoignie JJ, Ortiz-Interian C, Green DF, Roth D. Race, a cofactor in HIV-1-associated nephropathy. Transplant Proc 1989;21:3899- 901.
Cantor ES, Kimmel PL, Bosch JP. Effect of race on expression of acquired immunodeficiency syndrome-associated nephropathy. Arch Intern Med 1991;151:125-8.
Abbott KC, Hypolite I, Welch PG, Agodoa LY. Human immunodeficiency virus/acquired immunodeficiency syndrome-associated nephro-pathy at end-stage renal disease in the United States: Patient characteristics and survival in the pre highly active antiretroviral therapy era. J Nephrol 2001;14:377-83.
Kopp JB, Smith MW, Nelson GW, et al. MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat Genet 2008;40:1175- 84.
Klotman PE. HIV-associated nephropathy. Kidney Int 1999;56:1161-76.
Kimmel PL, Barisoni L, Kopp JB. Pathogenesis and treatment of HIV-associated renal diseases: Lessons from clinical and animal studies, molecular pathologic correlations, and genetic investigations. Ann Intern Med 2003;139:214- 26.
Winston JA, Bruggeman LA, Ross MD, et al. Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection. N Engl J Med 2001;344:1979-84.
Peters PJ, Moore DM, Mermin J, et al. Anti-retroviral therapy improves renal function among HIV-infected Ugandans. Kidney Int 2008;74:925-9.
Ikpeme EE, Ekrikpo UE, Akpan MU, Ekaidem SI. Determining the prevalence of human immunodeficiency virus-associated nephropathy (HIVAN) using proteinuria and ultrasound findings in a Nigerian paediatric HIV population. Pan Afr Med J 2012;11:13.
Esezobor CI, Iroha E, Onifade E, Akinsulie AO, Temiye EO, Ezeaka C. Prevalence of protei-nuria among HIV-infected children attending a tertiary hospital in Lagos, Nigeria. J Trop Pediatr 2010;56:187-90.
Han TM, Naicker S, Ramdial PK, Assounga AG. A cross-sectional study of HIV-sero-positive patients with varying degrees of proteinuria in South Africa. Kidney Int 2006;69: 2243-50.
Ray PE, Rakusan T, Loechelt BJ, Selby DM, Liu XH, Chandra RS. Human immunodeficiency virus (HIV)-associated nephropathy in children from the Washington, D.C. Area: 12 years’ experience. Semin Nephrol 1998;18:396- 405.
Shah I, Gupta S, Shah DM, Dhabe H, Lala M. Renal manifestations of HIV infected highly active antiretroviral therapy naive children in India. World J Pediatr 2012;8:252-5.
National Institute of Diabetes and Digestive and Kidney Diseases. United States Renal Data System: USRDS 2008 Annual Data Report: Atlas of End-Stage Renal Disease in the United States. Bethesda, MD, Bethesda, Maryland: National Institute of Diabetes and Digestive and Kidney Diseases; 2008.
Strauss J, Abitbol C, Zilleruelo G, et al. Renal disease in children with the acquired immunodeficiency syndrome. N Engl J Med 1989;321: 625-30.
Andiman WA, Chernoff MC, Mitchell C, et al. Incidence of persistent renal dysfunction in human immunodeficiency virus-infected children: Associations with the use of antiretro-virals, and other nephrotoxic medications and risk factors. Pediatr Infect Dis J 2009;28:619- 25.
Araoye MO. Research Methology with Statistics for Health and Social Sciences. Ilorin: Nathadex; 2003. p. 115-8.
Oyedeji GA. Socio-economic and cultural background of hospitalized children in Ilesha. Nig J Paediatr 1985;12:111-7.
Daniel B. Evaluation of the cardiovascular system. In: Behrman RE, Kleigman RM, Ann MA, editors. Nelson Textbook of Paediatrics. 18th
ed. Philadelphia: Saunders Co.; 2007. p. 1988-9.
National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 2004;114:555-76.
WHO Interim WHO Clinical Staging of HIV/AIDS & HIV/AIDS Case Definitions for Surveillance in African Region; 2005. p. 2-41. Available from: www.who.int/hiv/pub/ guidelines/casedefinitions/en/inndex.html. [Last accessed on 2012 Nov 12].
Beth A, Vogt E, Avner D. Conditions particularly associated with proteinuria In: Behrman RE, Kleigman RM, Ann MA, edotors. Nelson Textbook of Paediatrics. 18th
ed. Philadelphia: Saunders Co.; 2007. p. 2188-9.
Iduoriyekemwen NJ, Sadoh WE, Sadoh AE. Prevalence of renal disease in Nigerian children infected with the human immunodeficiency virus and on highly active anti-retroviral therapy. Saudi J Kidney Dis Transpl 2013;24:172- 7.
] [Full text]
Park JI, Baek H, Kim BR, Jung HH. Comparison of urine dipstick and albumin: Creatinine ratio for chronic kidney disease screening: A population-based study. PLoS One 2017;12:e0171106.
Connor E, Gupta S, Joshi V, et al. Acquired immunodeficiency syndrome-associated renal disease in children. J Pediatr 1988;113:39-44.
Ademola AD, Asinobi OO, Oladokun RE, Ogunkunle OO, Okoloz CA, Ogbole GE. Kidney disease in hospitalised HIV positive children in Ibadan, South West Nigeria. Afr J Med Med Sci 2012;41:221-30.
Anochie IC, Eke FU, Okpere AN. Human immunodeficiency virus-associated nephropathy (HIVAN) in Nigerian children. Pediatr Nephrol 2008;23:117-22.
Ezeonwu BU, Oguonu T, Okafor HU, Ikefuna AN. The use of estimated glomerular filtration rate in the evaluation of renal function in HIV-positive children in Enugu. Ann Trop Med Public Health 2013;6:206-10. [Full text]
Carbone L, D’Agati V, Cheng JT, Appel GB. Course and prognosis of human immunodeficiency virus-associated nephropathy. Am J Med 1989;87:389-95.
Wali RK, Drachenberg CI, Papadimitriou JC, Keay S, Ramos E. HIV-1-associated nephro-pathy and response to highly-active antiretro- viral therapy. Lancet 1998;352:783-4.
Ray PE, Xu L, Rakusan T, Liu XH. A 20-year history of childhood HIV-associated nephro-pathy. Pediatr Nephrol 2004;19:1075-92.
Bourgoignie JJ, Meneses R, Ortiz C, Jaffe D, Pardo V. The clinical spectrum of renal disease associated with human immunodeficiency virus. Am J Kidney Dis 1988;12:131-7.
Hassan Abdullahi Elechi
Department of Pediatrics, University of Maiduguri, Maiduguri
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
| Article Access Statistics|
| Viewed||1401 |
| Printed||22 |
| Emailed||0 |
| PDF Downloaded||113 |
| Comments ||[Add] |