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Renal abnormalities among HIV infected children at Muhimbili National Hospital (MNH)—Dar es Salaam, Tanzania

  • Francis Fredrick1, 2Email author,
  • Joel M. Francis3,
  • Paschal J. Ruggajo2, 4 and
  • Eden E. Maro4
BMC NephrologyBMC series – open, inclusive and trusted201617:30

https://doi.org/10.1186/s12882-016-0242-6

Received: 29 January 2015

Accepted: 16 March 2016

Published: 21 March 2016

Abstract

Background

Human Immunodeficiency Virus infection is a multisystem disease that contributes to significant morbidity. Renal involvement is reported to be common among patients with HIV. This study was carried out to determine renal involvement using simple bedside tests combined with ultrasonography examination.

Methods

We recruited 240 children from the HIV clinic at Muhimbili National Hospital. Data were collected using structured questionnaires and included demographic, clinical information, radiological tests; renal ultrasound and laboratory tests; serum creatinine, white blood cells, CD4+ counts and percent, urine for microalbuminuria and proteinuria.

Results

Microalbuminuria and proteinuria were present in 20.4 % and 7.1 % respectively. Significantly higher prevalence of microalbuminuria (p < 0.01) and proteinuria p < 0.01) were noted with low CD4 percent (<25 %). Lower mean CD4+ count were noted among children with microalbuminuria [937.4 ± 595.3 cells/μL vs 1164.7 ± 664.3 cell/μL, (p < 0.05)] and proteinuria [675.5 ± 352.3 cells/μL vs 1152 ± 662 cells/μL (p < 0.001)]. Fourteen (5.8 %) HIV infected children had estimated glomerular filtration rate (eGFR of 30–59) consistent with severe renal impairment. Increased cortical echogenicity was noted in 69/153 (39.2 %) of participants who had ultrasound examination.

Conclusion

Microalbuminuria, proteinuria and renal dysfunction were noted to be prevalent among HIV infected children indicating the need to consider routine screening of renal complications in these children.

Background

About 2.3 million children under the age of 15 years were estimated to be living with HIV globally 90 % of which were in sub-Saharan Africa [1]. In Tanzania 150,000 children aged between 0 and 14 years were estimated to require anti-retroviral therapy (ART) in 2011 [2]. Deaths in the first two years of life were attributed mainly to diarrhoeal diseases and respiratory infections before ART programs. [3] Improved survival with ART programs has paved way for long term HIV complications including renal complications [4]. ART drugs have been reported to contribute to renal complications [5].

Dondo et al. reported renal impairment in 34.6 % and proteinuria in 16 % among ART naïve HIV infected children in Zimbabwe [6]. In Nigeria proteinuria was reported in 20.8 % of HIV infected children by Esezobor et al. [7] In a study of ten children with HIV nephropathy in Nigeria Anochie et al. described proteinuria in all participants and impaired renal function in 90 % [8]. These findings highlight the contribution of renal complications in morbidity and possible mortality in HIV infected African children.

HIV related complications in HIV infected children include proteinuria, electrolyte disturbances, urinary tract infections, impaired renal function and end stage renal disease (ESRD) [9, 10]. Proteinuria is a marker of HIV nephropathy and has been correlated with decreased renal function and progression to ESRD. [1113] HIV infected patients with advanced AIDS stage, severe malnutrition, low CD4 count and high viral load have been reported to be more likely to present with proteinuria [5, 6, 13, 14].

Despite proteinuria being the early marker of HIV nephropathy, microalbuminuria has been reported to predict its occurrence [15]. In a study which was conducted in Bethesda, USA in a cohort of HIV infected children 15 % were noted to have microalbuminuria which correlated significantly with low CD4 count [16]. HIV infected patients with microalbuminuria have been reported to have kidney abnormalities, Han et al reported biopsy proven HIV nephropathy in majority (86 %) of HIV infected patients who had microalbuminuria in South Africa [11].

HIV renal complications results from direct infection of renal epithelial and mesangial cells and deposition of immune complexes into renal tissues [17, 18]. Anti-retroviral medications have also been reported to cause renal complications [1921]. This study aimed to determine renal complications and associated factors among HIV infected children attending HIV clinic at Muhimbili National Hospital (MNH).

Methods

This was a hospital based cross-sectional study of HIV infected children attending HIV clinic at MNH. Muhimbili University of Health and Allied Sciences Research Ethical Committee approved this study. We obtained informed written consents from parents/guardians and assent from participants aged ≥10 years prior to recruitment.

HIV infected children aged 1–14 years were consecutively recruited between January and March, 2011. We estimated a minimum sample size of 250 to determine proteinuria using Epi info version 6 statistical package assuming prevalence of microalbuminuria of 15 % based on the findings of a study conducted in a cohort of children infected with HIV acquired vertically in Bethesda [16].

Standardized questionnaires were used to obtain information on socio-demographic information including age and sex of participants. Other information was obtained from case notes. Clean catch urine specimen from each participant was tested for proteinuria and microalbuminuria using URiSCAN® dipstick and Microalbumin 2-1 test strips (which determine albumin to creatinine ratio) respectively. Proteinuria was defined as positive dipstick test of ≥ +1 corresponding to ≥ 30 mg/dL and microalbuminuria was defined as urinary albumin/creatinine ratio of ≥30 mg/g. Five milliliters of blood samples were drawn from each participant and tested for CD4 count and percentage, white blood cell count and serum creatinine using Architect Chemistry analyzer (Abbot®) and Cell-dyn 3500R analyzer respectively.

Each participant had weight measurement taken using a calibrated standard beam balance (SECA®) with the child putting on light clothing and no shoes, weight measures were approximated to the nearest 10 g. We calibrated the weighing scale to zero each day of recruitment. Length of children was measured with a length board, parents/guardians assisted in removing shoes and gently laying the child in supine position on the board, with their heads placed at 90° to the fixed headpiece, the sliding foot piece was brought into contact to the child’s heels. Height of participants was measured with the child standing at right angle in front of height board and sliding head piece was brought into contact with the head. Height/length was recorded to the nearest 10 mm. Body Mass Index (BMI) was calculated for each participant and was used to determine nutrition status using BMI for age z-score according to World Health Organization (WHO) standard charts.

Estimated GFR (eGFR) was calculated using modified bedside Schwartz equation validated for children with and without CKD [2225]. Recruited participants were given appointments for renal ultrasound examination scheduled one week after recruitment. Two certified radiologists reviewed the images and reached an agreement. Renal size was determined by comparison with age matched norms. Cortical echogenicity of the sonograms were graded relative to the liver or spleen. Cortical echogenicity was compared with liver and spleen and children who had higher echogenicity as compared to liver and spleen were considered to have abnormally increased echogenicity.

Stata version 12 was used for data analysis, proportions were calculated for microalbuminuria, proteinuria, t-test was used to compare continuous variables while association between categorical variables was determined using Chi-square and Fisher’s exact tests. Univariable logistic regression and multivariable logistic models were performed to determine predictors of microalbuminuria and proteinuria. Crude and adjusted odds ratio (OR) were reported, p value of < 0.05 was considered statistically significant.

Results

Demographic and clinical characteristics of study participants

Two hundred and forty children were recruited into this study as described in Table 1, out of which 133 (55.4 %) were males. Participants were aged between 1 and 14 years with mean age of 7.6 ± 3.7 years. Majority of study participants 219 (91.2 %) were using anti-retroviral drugs (ARV), of those using ARV 53 % (129/219) were using stavudine, lamivudine and nevirapine combination regimen. Sixty four (27.6 %) participants had immunosuppression (CD4 < 25 %), 44 (20.4 %) participants had microalbuminuria and 17 (7.1 %) had proteinuria.

Glomerular filtration rate and renal ultrasound findings

Fourteen (5.8 %) participants had eGFR between 30 and 59 ml/min/m2 which is consistent with renal impairment, 83 (34.6 %) had eGFR of ≥ 90 ml/min/m2 and 143 (59.6 %) participants had eGFR between 60 and 89 ml/min/m2. All participants were given appointments for renal ultrasound examination but only 153 (63.8 %) out of all participants attended for this evaluation. Sixty participants (39.2 %) out of 153 who were examined had normal kidney size and increased echogenicity.

Factors associated with microalbuminuria

Presence of haematuria and low CD4 percent were noted to influence occurrence of microalbuminuria. We observed that children with lower CD4 percent (<25 %) to more likely to have microalbuminuria [39.5 % vs. 14.8 % (p < 0.01)] as compared to those with CD4 percent ≥ 25 %, similarly higher proportion of participants with microalbuminuria had haematuria as compared to those without [50.0 % vs. 19.0 % (p = 0.02)] Table 2.
Table 1

Demographic characteristics of study participants

Variable

N (%)/N (±SD)

Age

  < 5 years

66 (27.5)

 5 up to 10 years

94 (39.2)

  ≥ 10 years

80 (33.3)

Sex

 Male

133 (55.4)

 Female

107 (44.6)

Using anti-retroviral therapy

 Yes

219 (91.2)

 No

21 (8.8)

Types of ARV

 d4T, 3TC, NVP

129 (53.8)

 d4T, 3TC, EFV

33 (13.8)

 AZT, 3TC, NVP

28 (11.7)

 AZT, 3TC, EFV

24 (10.0)

 ABC, ddI, Kaletra

5 (2.1)

CD4 percent

  ≥ 25 %

64 (27.6)

  < 25 %

176 (73.3)

Laboratory values

 Mean serum creatinine

51.3 ± 6.8 μmol/L

 Mean blood urea nitrogen

2.8 ± 0.9 mmol/L

 Mean eGFR

84 ± 14.7 mL/min/1.73 m2

 Mean white blood cell count

6.7 ± 2.8 x 103 cells/μL

 Mean CD4 percent

31.1 ± 10 %

 Mean haemoglobin level

10.9 ± 1.4 g/dL

Table 2

Factors associated with microalbuminuria

Variable

n

Microalbuminuria present n (%)

P value

Age (years)

 1 up to 5

63

12 (18.2)

 

 5 up to 10

91

18 (19.1)

 

 10 and above

86

19 (23. 8)

0.669

Sex

 Male

133

30 (22.6)

 

 Female

107

19 (17.8)

0.359

Use of ART

 Yes

219

45 (20.5)

 

 No

21

4 (19.0)

1.000

CD4 percent

  < 25 %

64

23 (35.9)

 

  ≥ 25 %

176

26 (14.8)

0.001

Haematuria

 Present

10

5 (50.0)

 

 Absent

230

44 (19.1)

0.018

BMI z–score

 Median- -1SD

164

39 (23.8)

 

  < -1 SD

76

10 (13.2)

0.061

Renal echogenicitya

 Normal

93

14 (23.3)

 

 Increased

60

20 (21.5)

0.843

an = 153

Table 3

Factors associated with Proteinuria (n = 240)

Variable

n

Proteinuria present n (%)

P value

Age (years)

 1 up to 5

63

4 (6.1)

 

 5 up to 10

91

2 (2.1)

 

 10 and above

86

11 (13.8)

0.012

Sex

 Male

133

9 (6.8)

 

 Female

107

8 (7.5)

0.831

Use of ART

 Yes

119

16 (7.3)

 

 No

21

1 (4.8)

1.000

CD4 percent

  < 25 %

64

10 (15.6)

 

  ≥ 25 %

176

7 (4.0)

0.004

Haematuria

 Present

10

1 (10.0)

 

 Absent

230

16 (7.0)

0.527a

BMI Z –score

 Median- -1SD

164

11 (6.7)

 

  < -1 SD

76

6 (7.9)

0.739

Renal echogenicityb

 Normal

93

6 (10.0)

 

 Increased

60

9 (9.7)

1.0

aFischer’s exact test, bn = 153

Children with haematuria had four folds increased likelihood of having microalbuminuria as compared to those without haematuria. Children with low CD4 percent (<25 %) had five fold increased likelihood of having microalbuminuria as compared to those with CD4 ≥ 25 %, Table 4.
Table 4

Univariate and multivariate logistic regression for factors associated with microalbuminuria

Variable

Crude OR (95 % CI)

p-value

Adjusted OR (95 % CI)

p-value

Age

  < 5 years

Ref

 

Ref

 

 5–10 years

1.166 (0.508–2.673)

0.717

2.242 (2.396–11.124)

0.116

  > 10 years

1.432 (0.630–3.254)

0.391

3.020 (1.0345–8.820)

0.043

Sex

 Male

Ref

 

Ref

 

 Female

0.741 (0.390–1.407)

0.360

0 .656 (0.309–1.393)

0.273

CD4 percent

  ≥ 25 %

Ref

 

Ref

 

  < 25 %

3.236 (1.675–6.254)

<0.0001

5.134 (2.369–11.125)

<0.0001

Haematuria

 Absent

Ref

 

Ref

 

 Present

4.227 (1.172–15.240)

0.028

3.844 (0.975–15.153)

0.054

Factors associated with proteinuria

The proportion of children with proteinuria was higher among children aged ten years and above as compared to younger children (p = 0.01). Children with lower CD4 percent (< 25 %) were likely to present with proteinuria [15.6 % vs. 4.0 % (p < 0.01)] as compared to those with CD4 percent ≥ 25 %, Table 3. Participants with proteinuria had significantly lower mean CD4 count as compared to those without proteinuria [675.5 ± 352.3 cell/μL vs. 1152 ± 662 cells/μL (p < 0.01)]. Participants with CD4 < 25 % were four fold more likely to have proteinuria as compared to those with CD4 ≥ 25 %, Table 5. No association was noted between haematuria or severe renal impairment with microalbuminuria or proteinuria.
Table 5

Univariate and multivariate logistic regression for factors associated with proteinuria

Variable

Crude OR (95 % CI)

p-value

Adjusted OR (95 % CI)

p-value

Age

  < 5 years

Ref

 

Ref

 

 5–10 years

0.331(0.059–1.868)

0.211

0.539(0.081–3.593)

0.523

  > 10 years

2.163(0.655–7.140)

0.205

3.538(0.728–17.190)

0.117

CD4 percent

  < 25 %

Ref

 

Ref

 

  ≥ 25 %

4.471(1.623–12.316)

<0.004

4.416(1.409–13.845)

0.011

Haematuria

 Present

Ref

 

Ref

 

 Absent

1.486(0.177–12.474)

0.715

0.978(0.104–9.175)

0.984

Discussion

We found microalbuminuria and proteinuria to be common among HIV infected children in our setting. Microalbuminuria was noted in 20.4 % while proteinuria was present in 7.1 % of the recruited participants in this study. This findings were presumed to represent HIVAN.

Microalbuminuria has been reported as a common renal manifestation in HIV infected people, several studies have reported microalbuminuria in HIV infected children both in developed countries and sub-Saharan Africa. Dimock et al reported 15 % among HIV infected youth and children in Bethesda, USA [16]. Two other studies conducted among HIV infected Nigerian children reported prevalence of microalbuminuria of 11.1 % and 12 % [26, 27]. Microalbuminuria present earlier than proteinuria and has been reported to predict proteinuria in HIV infected patients [15].

A study conducted among HIV infected Zimbabwean children reported a prevalence of proteinuria to be 5 %, this is comparable to our findings of 7.1 % [6]. Esezobor et al. [7] reported a prevalence of proteinuria determined using urine protein to creatinine ratio, to be 20.5 % in a study conducted among HIV infected Nigerian children [7].

Older children had significantly higher prevalence of proteinuria in our study; with no difference being noted in occurrence of microalbuminuria with age. Therefore it may be advantageous to screen children with both tests in order to detect earlier renal complications. Microalbuminuria has been reported as a presentation of HIV associated nephropathy, in South Africa Han et al reported microalbuminuria in 24 % of patients who had biopsy proven HIV associated nephropathy [11].

Participants with immunosuppression (CD4 percent < 25 %) had higher prevalence of both microalbuminuria and proteinuria in this study. This is consistent with reports from other studies, Esezobor et al. in a study conducted in Nigerian children reported proteinuria in 11 (37.9 %) out of 29 children who had severe immunosuppression as compared to 7 (11.9 %) out of 59 with milder immunosuppression [4]. Chaparro et al reported similar association between proteinuria and low CD4 count and high viral load in a landmark study of proteinuria in HIV infected children conducted in Miami, USA [13].

Participants with microalbuminuria and proteinuria had significantly lower mean CD4 count which is in consistence with noted trend for CD4 percent. Similar findings have been reported among HIV infected patients with immunosuppression and advanced disease [6, 7, 1315, 26, 27]. It is evident from our findings that it is important for clinician to make close follow up on the progress of patients receiving ART, to ensure immune competency is attained and maintained to prevent or delay occurrence of HIV associated renal complications. Fifteen participants (0.06 %) had haematuria which had no significant association with mircroalbuminuria or proteinuria; this finding may be attributed to urinary tract infection.

Severe renal impairment (defined as eGFR <60 ml/min/1.73 m2) was noted in 5.8 % of study participants, this is lower than 13.3 % reported by Esezobor et al. from a study conducted among HIV infected children in Nigeria [28]. In our study eGFR was estimated using serum creatinine which is different from cystatin C method utilized by Esezobor et al. Dondo et al in study conducted among HIV infected children in Zimbabwe reported renal dysfunction (defined by eGFR of 30 to ≤ 90 ml/min/1.73 m2) in 34.6 % of participants [6]. These findings justify initial renal function screening at recruitment and regular monitoring in HIV infected children.

Renal ultrasound examination of 153 participants revealed normal sized kidneys with increased cortical echogenicity in 39.2 % (60/153) which was attributed to HIVAN. Similar findings were reported by Steel-Duncan et al. in a study which was conducted in HIV infected Jamaican children which revealed normal sized kidneys with increased echogenicity [29]. Anochie et al reported grossly enlarged kidneys in 30 % and normal sized kidneys and increased echogenicity in 70 % of children with HIVAN in Nigeria [8]. No correlation was noted between occurrence of microalbuminuria or proteinuria and increased echogenicity in our study. It may be important to performing renal ultrasound examination at recruitment and regularly thereafter to complement urinalysis and renal function tests.

Study limitations

Microalbuminuria and proteinuria were tested only once in this study this could have underestimated the true magnitude of these two entities. The modified Schwartz formula utilized for estimating eGFR could have resulted in over/underestimation of GFR in the study population particularly for children below two years. Only 63.8 % of participants had renal ultrasound examination performed, this is because participants were given appointment for the examination on a different day from the visit on which they were recruited, this may be due to lack of reimbursement for transport which could not be provided in this study.

Conclusions

This study has documented existence of renal abnormalities in HIV infected children at MNH in the form of microalbuminuria, proteinuria and renal dysfunction. Immunosuppression was positively linked to occurrence of both microalbuminuria and proteinuria indicating the importance of attaining immune-competency among HIV infected children who are ART naïve and those on ART. Findings of this study may justify the role of screening HIV infected children for renal complications before starting ART and annually thereafter. This will facilitate earlier detection of affected children and making proper follow up including seeking care from kidney care specialists.

Abbreviations

AIDS: 

acquired immunodeficiency syndrome

ART: 

anti-retroviral therapy

BMI: 

body mass index

CD: 

cluster of differentiation

CKD: 

chronic kidney disease

eGFR: 

estimated glomerular filtration rate

ESRD: 

end stage renal disease

HIV: 

human immunodeficiency virus

HIVAN: 

human immunodeficiency virus associated nephropathy

MNH: 

Muhimbili National Hospital

MUHAS: 

Muhimbili University of Health and Allied Sciences

NIMR: 

National Institute of Medical Research

OR: 

odds ratio

USA: 

United States of America

WHO: 

World Health Organization

Declarations

Acknowledgements

We are grateful to contribution and guidance provided by the late Prof. Bjarne Magnus Iversen in study design and preliminary report writing. We acknowledge nurses in paediatric HIV clinic and Mrs Mlalasi, laboratory technicians at MNH who assisted in conducting this study. Special thanks to MNH radiologists; Dr Joel Bwemero and Dr Ramadhani Kabala, and sonographer-Mr Maulid Kikondo for performing ultrasound examinations in this study. This study was funded by Norwegian Master’s program (NOMA program) and Ministry of Health and Social Welfare of Tanzania.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Paediatrics and Child Health, School of Medicine, Muhimbili University of Health and Allied Sciences (MUHAS)
(2)
Renal Unit, Muhimbili National Hospital (MNH)
(3)
National Institute of Medical Research (NIMR), Mwanza-Centre
(4)
Department of Internal Medicine, School of Medicine, Muhimbili University of Health and Allied Sciences (MUHAS)

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Copyright

© Fredrick et al. 2016