doi:10.1111/j.1440-1754.2007.01167.

ORIGINAL ARTICLE

Body composition of children with chronic and end-stage renal failure

Andreas Nydegger,1 Boyd JG Strauss,5 Ralf G Heine,1,3,4 Ninik Asmaningsih,2 Colin L Jones2,3 and Julie E Bines1,3,4
1 Departments of Gastroenterology and Clinical Nutrition, 2Department of Renal Medicine, Royal Childrens Hospital, Parkville, 3Department of Paediatrics, University of Melbourne, Melbourne, 4Murdoch Childrens Research Institute, Parkville and 5Body Composition Laboratory, Department of Medicine, Monash University, Clayton, Victoria, Australia

Aim: Protein energy malnutrition is common in children with chronic renal failure (CRF) and may negatively impact on clinical outcome. Although the aetiology of malnutrition is multifactorial, descriptive information on body composition may guide nutritional interventions aimed at optimising nutritional status. Methods: This prospective cohort study in children with CRF was conducted from April 1999 to November 2000. Patients were categorised according to their glomerular ltration rate (GFR) into CRF and end-stage renal failure (ESRF). Body composition was assessed based on anthropometry, total body potassium (TBK), total body protein (TBP) and dual X-ray absorptiometry (DEXA). Results: Fifteen patients (10 male, 5 female; mean age: 13.4 4.3 years) were studied, including eight patients with CRF (mean GFR: 17.0 7.2 mL/min/1.73 m2) and seven patients with ESRF (mean GFR: 6.4 1.7 mL/min/1.73 m2). Patients in both groups (n = 15) had decits in height and TBP (mean z-score height-for-age: 1.19 1.05, P < 0.01; mean z-score TBP: 0.71 0.71, P < 0.05). There were no signicant differences in weight, height, fat-free mass, TBK and TBP between patients with CRF and ESRF. Conclusions: Linear growth impairment and decreased TBP are common in children with chronic and ESRF. TBK and DEXA may underestimate the degree of malnutrition in these patients. Key words: anthropometry; dual energy X-ray absorptiometry; growth failure; malnutrition; total body potassium; total body protein.

Despite signicant advances in dialysis technique, proteinenergy malnutrition remains a common problem in patients with advanced renal failure. Alterations of the nutritional, metabolic and uid homeostasis in patients with CRF may negatively impact on their long-term clinical outcome and quality of life.1 Malnutrition has been demonstrated in up to 50% of patients on chronic haemodialysis.25 Several studies have indicated that malnutrition represents a major factor contributing to morbidity and mortality in patients receiving renal replacement therapy.3,6

Key Points 1 Linear growth impairment and decreased total body protein are common in children with chronic and ESRF. 2 Total body potassium and DEXA measurements may underestimate the degree of malnutrition in children chronic and ESRF. 3 Early detection of nutritional decits in children with chronic renal disease may help target nutritional interventions aimed at ameliorating deciency states and growth failure.
Correspondence: Professor Julie E Bines, Department of Paediatrics, University of Melbourne, Flemington Road, Parkville, Vic. 3052, Australia. Fax: +61 39345 6240; email: julie.bines@rch.org.au Accepted for publication 7 May 2007.

Malnutrition in patients receiving dialysis is multifactorial. It may result from insufcient energy intake owing to anorexia, adverse drug effects or uid restriction. In addition, haemodialysis and peritoneal dialysis are associated with loss of amino acids, peptides and proteins, as well as an increase in resting energy expenditure.7 The average daily protein loss during peritoneal dialysis may amount to 10 g and signicantly deplete essential amino acid stores.8,9 Patients on peritoneal dialysis seem to be less affected by malnutrition than those receiving haemodialysis, perhaps owing to the peritoneal absorption of carbohydrate calories provided with each intraperitoneal exchange.10 Malnutrition is usually established before the initiation of renal replacement therapy. Pre-dialysis nutritional status correlates with the clinical outcome of these patients.11 Furthermore, malnutrition may progress despite regular dialysis.5,12,13 Metabolic consequences of renal failure, such as uraemia, catabolic stress during infective episodes, and endocrine disorders may also contribute to poor nutritional status.14 In prepubertal children, abnormalities in parathyroid and growth hormone levels contribute to renal osteodystrophy and poor growth.15,16 Few data are available on the nutritional consequences of CRF and ESRF in childhood. Previous studies have demonstrated signicantly decreased total body potassium (TBK) and fat-free mass (FFM) in children with CRF and ESRF, consistent with a reduction in body cell and skeletal muscle mass.17,18 The aim of this study was to compare changes in anthropometric

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measurements and other markers of body composition in children with advanced renal failure.

Patients and Methods

This prospective cohort study was conducted at the Renal Clinic, Royal Childrens Hospital and Monash Medical Centre, Melbourne, from April 1999 to November 2000. Patients were eligible for inclusion in the study if they were aged between 5 and 20 years and had advanced renal failure, as assessed by a paediatric nephrologist (CLJ). Patients were categorised according to their glomerular ltration rate (GFR) into chronic renal failure (CRF; GRF 1075 mL/min/1.73 m2) or end-stage renal failure (ESRF; GFR < 10 mL/min/1.73 m2). Patients on peritoneal dialysis were studied before commencing the next dialysis cycle. Similarly, patients on haemodialysis had measurements performed before dialysis. The hydration status of all children at time of measurement was clinically assessed as normal. None of the patients were receiving growth hormone replacement therapy, enteral supplements or tube feeding at the time of assessment. All body composition measurements were performed at the Body Composition Laboratory located at Monash Medical Centre. The study was approved by the Human Ethics Research Committee of the Royal Childrens Hospital, Melbourne. Informed written consent was obtained from adolescent patients, or from their parents before entry into the study.

Patients lay supine on a movable bed which was positioned to centre the trunk section in a collimated neutron beam measuring 40 cm 20 cm at a bed level 35 cm above a 10 g 252Cf neutron source. Induced rays characteristic of body nitrogen were measured over a 1000 s exposure by two 10 cm 10 cm 15 cm NaI(Tl) detectors, positioned on each side of the patient. Subject measurements were calibrated against a phantom, and a correction factor was applied to account for variation in body width and thickness. The effective whole body radiation dose was 0.32 mSv (Q = 20), and the intra- and inter-assay accuracy and precision established in phantoms were >97% and <4% (coefcient of variation), and >98% and <5%, respectively.26 Measurements of TBN standardised for age, gender and height were used as an index of protein status, assuming that 1 g nitrogen = 6.25 g protein.

DEXA bone mineral content, fat mass and fat-free soft tissue mass
A total body dual energy X-ray absorptiometry (DEXA) scan was performed (Lunar Corp. Software version 3.6z, Madison, WI, USA). Each patient was required to lie supine on a 60 cm 200 cm padded table while X-rays of two distinct energies scanned the patient from head to foot. Scans were performed in the medium scan speed mode over a 20-min period. The manufacturers software was then used to resolve body composition into three distinct compartments, that is, bone mineral, fat and fat-free soft tissue. The total body skin entrance dose was <0.01 mSv, and the precision of measurement 2% (coefcient of variation) for soft tissue and 1% for bone mass and density.27 FFM-DEXA was estimated as the sum of total body bone mineral and fat-free soft tissue. The precision of measurement was 3% (coefcient of variation).27

Anthropometry
Weight was measured to the nearest 0.1 kg using calibrated digital scales. Height was measured to the nearest 0.1 cm using a stadiometer. Triceps skin fold thickness measurements were obtained using Harpenden callipers. All anthropometric measurements were performed using the standardised procedures of Lohman19 by a single trained observer.

Statistical Analysis
Calculation of standard deviation scores (z-scores)
Anthropometric measurements were expressed as age- and gender-specic z-scores, using the epidemiological software package Epi Info 2002 (Centres for Disease Control and Prevention, Atlanta, GA, USA). TBK, TBP and DEXA measurements were transformed into z-scores using the reference child and adolescent models of body composition (matched for age, gender and ethnicity).28 Statistical analysis was performed using Graph Pad InStat (V3.05 for Windows 95/NT, Graph Pad Software, San Diego, CA, USA). Data were summarised as mean standard deviation. Group comparisons were made by two-tailed Students t-test. Statistical signicance was accepted for P < 0.05.

Total body potassium

Total body potassium was determined by whole body counting of 1.46 MeV -ray emissions from 40K, using a purpose-built shadow shield counter. A total body scan was performed with the patient positioned supine on a moveable stretcher. Patients passed through a symmetric array of four 40 cm 10 cm 10 cm NaI(Tl) detectors shielded within an open ended chamber. Subject measurements were calibrated against an anthropomorphic phantom, and a correction factor was applied to account for variation in body thickness and width. Inter- and intra-assay accuracy and precision for repeated 30 min scans of a standard phantom were >7% and <8% (coefcient of variation), and >97% and <4%, respectively.20 FFM-TBK was calculated using the age and gender-specic constants for conversion of TBK to FFM in children.2123

Results
Of 15 patients (10 male, 5 female; mean age 13.4 4.3 years; range 6.120.8), there were eight patients with CRF (mean age 14.9 4.3 years) and seven patients with ESRF (mean age 11.6 3.8 years). Of the seven children with ESRF, ve were managed with haemodialysis, and two with peritoneal dialysis.
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Total body protein

Total body protein (TBP) was calculated from the direct measurement of total body nitrogen (TBN) by prompt- in vivo neutron activation analysis (1 g nitrogen = 6.25 g protein).24,25

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Table 1 Characteristics of patient cohort Type of renal failure CRF Treatment modality Conservative Primary disease and number of patients (n) Hypoplastic or dysplastic kidney (n = 3) Glomerulonephritis (n = 1) Reux nephropathy (n = 2) Bilateral renal vein thrombosis (n = 1) Neurogenic bladder (n = 1) Hypoplastic or dysplastic kidney (n = 2) Glomerulonephritis (n = 2) HenochSchnlein purpura (n = 1) Reux nephropathy (n = 1) Medullary cystic disease (n = 1) Total number of patients 8 Gender Age in years (mean range) 14.9 (9.220.8) GFR (mean range) 17.0 (10.332.3)

6M:2F

ESRF

HD

4M:1F

12.7 (8.617.2)

6.0 (4.48.4)

PD

2F

8.9 (6.111.6)

7.3 (5.78.9)

CRF, chronic renal failure; ESRF, end-stage renal failure; F, female; GFR, glomerular ltration rate (mL/min/1.73 m2); HD, haemodialysis; M, male; PD, peritoneal dialysis.

Table 1 summarises patient characteristics, underlying disease and type of treatment. Children with CRF and ESRF displayed signicant decits in height (mean height-for-age z-score: 1.19 1.05; 95% CI: 1.77, 0.61; P < 0.01) and TBP (mean z-score: 0.71 0.71; 95% CI: 1.10, 0.32; P < 0.05); Figure 1. Weight (mean weight-for-age z-score: 0.34 0.69; 95% CI: 0.72, 0.04, not signicant) and triceps skin fold thickness (mean z-score: 0.51 0.95; 95% CI: 1.03, 0.02, not signicant) were also decreased in both groups, compared with normal controls, but these differences did not reach statistical signicance. TBK was signicantly increased (TBK mean z-score: 0.74 0.81; 95% CI: 0.29, 1.19; P < 0.05). This increase was observed independent of dialysis technique, as shown in Figure 2. FFM estimated by DEXA was increased in patients with CRF and ESRF but did not reach statistical signicance (DEXA mean z-score: 0.55 1.22; 95% CI: 0.13, 1.23, not signicant). The body mass index (BMI) for study patients was similar to controls (BMI 0.06 0.96; 95% CI: 0.47, 0.59, not signicant). There were no signicant differences in any of the parameters measured when comparing patients with CRF and ESRF (Table 2).

Discussion
Our study demonstrated signicant linear growth impairment and depletion of TBP stores in children with advanced renal failure. Although we observed higher levels of TBK and DEXAFFM in children with CRF and ESRF, these were not signicantly different from controls. These descriptive data may help to improve our understanding of the impact of malnutrition and may guide nutritional interventions aimed at improving nutritional status in children with renal failure. Height, weight and BMI are considered useful markers of nutritional status, but may be too insensitive to detect subtle changes in fat-free mass.10 Patients with renal impairment frequently experience uctuations in body weight and body composition owing to rapid changes in body water and electrolyte balance during dialysis.10 In addition, secondary endocrinological disorders (i.e. growth hormone deciency,
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hyperparathyroidism) may affect the accuracy of anthropometric measurements.29 Anthropometry has been previously shown to underestimate body protein depletion in haemodialysis patients.30 In the present study, children with CRF and ESRF had evidence of depleted protein stores, compared with healthy control subjects. In adults dialysis patients, low TBP stores have been shown to be predictive of increased mortality.31 Although ESRF represents a more advanced phase of renal dysfunction, patients with ESRF had similar protein decits compared with those with CRF. This may reect the small sample size in this study and may be explored in larger studies in this population in the future. Reduced levels of plasma proteins such as albumin, transferrin, retinol-binding protein, and prealbumin have been proposed as markers of moderate to severe malnutrition.32 However, they need to be interpreted with caution in patients with renal insufciency as serum protein concentrations may be reduced in the setting of extracellular volume excess.10 Prealbumin is cleared by glomerular ltration. In patients with renal impairment, normal levels may occur despite malnutrition. However, low prealbumin levels in the setting of a low GFRs are more reliable in predicting malnutrition.10 In view of these difculties, TBN may be the most accurate marker of TBP stores, particularly in patients with chronic renal insufciency. However, it is costly and not widely available.33,34 Substantial loss of TBP stores may occur in other chronic diseases and in ageing. Such losses may negatively impact on immune function and quality of life, as well as on growth velocity in children.35 Losses of specic amino acids, peptides and proteins during dialysis may lead to changes in plasma and intracellular amino acid proles and loss of essential amino acids. In order to avoid malnutrition in CRF, a daily protein intake of at least 1.2 g per kilogram body weight with at least 5060% of protein with high biological value is recommended.36,37 The Clinical Practice Guidelines for Chronic Kidney Disease recommend for adult patients with CRF a low-protein diet providing between 0.60 and 0.75 g protein/kg/day.38 However, evidence to support the use of oral protein and energy supplements to improve the nutritional status of children with a range of chronic diseases,

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CRF
2

ESRF
2

including CRF, is not available.39 The measurement of TBK provides an estimation of body cell mass and is derived from measurement of the intracellular uid compartment. This approach is based on the assumption that >96% of TBK is found in intracellular water.22 This is the energy-using, workperforming, nitrogen-rich component of the body.40 When the energy demands of the body are not met, proteins that full structural or functional roles are metabolised and inadequate accretion or depletion of the body cell mass will result from unmet protein-energy requirements.41 It is therefore not surprising that TBK is decreased in malnourished patients, compared with healthy control subjects.42 By contrast, we observed an increase in TBK in our paediatric cohort with CRF and ESRF. Intracellular accumulation of uid as a manifestation of renal insufciency and/or dialysis treatment may explain these ndings. To minimise systematic errors, measurements were performed between peritoneal dialysis cycles, that is, without dialysis uid in the abdominal cavity, and before haemodialysis. Contrary to our results, El-Bishti et al. found that the intracellular water compartment of children on haemodialysis was signicantly smaller than expected, in the presence of normal total body water levels.43

z-scores z-scores

3
0

z-scores

1 0 1 2 3 Peritoneal dialysis Haemodialysis

2
Fig. 1 Comparison of CRF and ESRF, using child and adolescent body composition reference data (matched for age, gender and ethnicity).28 ( ) Weight z-score, ( ) height z-score, ( ) TSF z-score, ( ) BMI z-score, ( ) TBK z-score, ( ) TBP z-score, ( ) DEXA-FFM z-score. BMI, body mass index; CRF, chronic renal failure; DEXA-FFM, dual X-ray absorptiometry fat-free mass; ERSF, end-stage renal failure; TBK, total body potassium; TBP, total body protein; TSF, triceps skin fold thickness.

Fig. 2 Comparison of total body potassium levels for patients receiving peritoneal dialysis or haemodialysis.

Table 2 Body composition of children with CRF and ESRF (z-scores; mean SD) CRF Number (%) Weight-for-age z-score Height-for-age z-score Triceps skin fold thickness z-score Body mass index z-score Total body potassium z-score Total body protein z-score DEXA fat-free mass z-score 8 (53%) 0.30 0.87 0.97 0.98 0.71 1.07 0.31 1.13 0.52 0.81 0.72 0.83 0.68 1.51 ESRF 7 (47%) 0.39 0.49 1.45 1.14 0.28 0.83 0.31 0.73 0.99 0.81 0.71 0.62 0.40 0.87 P-value 0.823 0.397 0.404 0.357 0.279 0.981 0.674

CRF, chronic renal failure; DEXA, dual X-ray absorptiometry; ESRF, end-stage renal failure.

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Dual X-ray absorptiometry is traditionally considered the gold-standard for measuring bone mineral content44 and FFM.45,46 However, DEXA-FFM may be unreliably in dialysis patients as it depends on the assumption that there is uniform tissue hydration; this may not be the case in patients with uid retention owing to renal disease.47 Woodrow et al. found no correlation between total body water and FFM by DEXA in patients with ESRF.48 Patients on peritoneal dialysis may carry up to 40 mL/kg body weight of excess uid in their peritoneal cavity.49 In summary, patients with CRF and ESRF exhibit linear growth impairment and depletion of TBP stores. Our data suggest that TBK measurements as a marker of nutritional status in children with advanced renal failure should be interpreted with caution. Owing to abnormalities in uid distribution and tissue hydration, TBK and DEXA may underestimate the degree of malnutrition. Early detection of nutritional decits in children with chronic renal disease may help target nutritional interventions aimed at ameliorating nutritional deciency states and growth failure in these patients.

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