FROM THE DEPARTMENTS OF RADIOLOGY AND MEDICINE, AARHUS KOMMUNEHOSPITAL, DK-8000 AARHUS, DENMARK.
BONE MATURATION IN CHILDREN WITH CHRONIC RENAL FAILURE Effect of let - hydroxy vitamin D, and renal transplantation A. JOHANNSEN, H. E. NIELSEN and H. E. HANSEN Bone age is often retarded in children with chronic renal failure (SCHARER et coIl. 1976, STICKLER 1976). As the kidney is the sole site of C - I hydroxylation, the transformation of vitamin D to the biologically active metabolite 1.25 (OH)2 vitamin D, is reduced in these patients (FRASER & KODICEK 1970). Increased growth and healing of bone lesions have previously been reported to occur in children with renal osteodystrophy when treated with 1.25 (OH)2 vitamin D, (CHESNEY et colI. 1978) and healing of bone lesions has been demonstrated in children treated with let - OH vitamin D, (NIELSEN et coIl. 1977). However, no report concerning the effect of 1.25 (OH)2 vitamin D, and 1et-OH vitamin D, on bone maturation in children with chronic renal failure has appeared in the literature. The effects of treatment with let - OH vitamin D, on bone maturation in children during hemodialysis were analysed and compared with the effect of successful renal transplantation. The results are now reported.
Material and Methods The material comprised II children aged 2 to 17 years treated at this hospital for chronic renal failure during 1968 to 1977. Submitted for publication 14 June 1978. Acta Radiologica Diagnosis 20 (1979) Fasc. 1 B
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A. JOHANNSEN, H. E. NIELSEN AND H. E. HANSEN
Table 1 Clinical data on 11 children with chronic renal failure
Case No.
1 2 3
4 5 6 7 8
9 10 11
Age on admission (years)
Clinical diagnosis
Period of dialysis (months)
10
CPN CPN CGN CGN CPN CRD CGN CRD CPN CGN CGN
64 64 76 56 40 0 3 4
10 8 10 8
1 15 15 13 13 12
0 2 3
Period of immunosuppressive therapy (months)
9 0 1 0 1
Bilateral Successful nephrectomy renal transplantation
+ + + +
0
43 27 51 69 30
+ + + + +
+ + + + +
CPN = Chronic pyelonephritis. CRD = Congenital renal disease. CGN = Chronic glomerulonephritis.
The patients were classified into two groups: (1) Patients treated with l z - OR vitamin D a, and (2) patients with a well functioning renal transplant. All children except 2 were treated with hemodialysis for 2 to 76 months (Table 1). The duration of dialysis was 6 hours 3 times per week, using a 1 m 2 13.5,um thick couprophane membrane (Rhone-Poulenc, RP5). The dialysis unit was supplied with distilled water and the dialysate contained 3.0 mEqjl of calcium and 1.3 mEqjl of magnesium. The patients' diet contained 40 to 70 g protein, 20 to 30 mEq sodium and 500 to 600 mg calcium per day. The patients in group 1 (5 hemodialysed and 1 non-dialysed) were treated with loc-OR vitamin D, for 2 to 22 months (mean 10.7 months). loc-OR vitamin D 3 was given initially in an oral dose of 1 ,ug per day for maintaining the level of serum calcium within the upper normal range. Serum phosphorus was regulated by aluminium aminoacetate (1.2-3.6 g orally per day) during the period of 10:~OR vitamin D 3 treatment. Three patients in this group received a renal transplant before the 10: ~ OR vitamin D 3 treatment (Figure). The renal transplant never functioned or was rejected in these patients. All 5 patients in group 2 had well functioning renal transplants. They were treated with hemodialysis for 0 to 4 months before the transplantation (Table 1). Films of the skeleton were obtained in most patients every 6 to 12 months. Children treated with l « - OR vitamin D 3 were examined both before and after the treatment. The bone age was evaluated by comparing the size and shape of the ossification
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BONE MATURATION IN CHILDREN WITH CHRONIC RENAL FAILURE bone age
start of 1Cl'-OH-Oa treatment
195
renal transplantation
220 200 180 160 140 120 11'
100 80 60 50 40 30 20 10 50 40 30 20 10 0 10 20 30
30 20 10 0 10 20 30 40 50 60 observation period Bone maturation (in months) in hemodialysed children before and after treatment with I« - OH vitamin D 3 (Nos 1-6) and in children after successful renal transplantation (Nos 7-11). In case 7 (female) and case 8 (male) the epiphyseal plates closed at the end of observation period (in months). T Renal transplant before 1a - OH - D 3 •
centres and epiphyseal cartilage in the hands and wrists with the standards given in the atlas of GREULICH & PYLE (1959). The figures were related to healthy Danish children, who are retarded 6 to 12 months in relation to the North American standard (ANDERSEN 1968, MATHIASEN 1973). Moreover all films of the skeleton were reviewed with regard to renal osteodystrophy. Results At the first radiography open epiphyseal plates were found in all patients. In 5 patients in group 1 (Nos 1-5), aged 8 to 10 years, bone maturation was retarded from 6 to 27 months, while normal bone age was found in a one-year-old child (No.6). Initially this child had marked osteodystrophy, while the other patients in the
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A. JOHANNSEN, H. E. NIELSEN AND H. E. HANSEN
Table 2 Radiologic bone abnormalities in 11 children with chronic renal failure
Case No.
Age at first radiography (months)
Bone age retardation (months)
Radiographic renal osteodystrophy At first examination
In relation to IGl:-OH D, treatment or successful renal transplant Rickets
1 2 3 4 5 6 7
8 9 10 11
130 120 102 121 104 13 198 190 166 166 154
15 6 9
27 10 0 0 0 23 25 36
Ostitis fibrosa
Before
After
Before
After
++
+
+ ++ +++
+ +
++ ++ ++ ++ +++
+ + + ++ + +
+ +
group only had varying degrees of halisteresis but no characteristics indicating renal osteodystrophy (Table 2). In the period of hemodialysis before lot:-OH vitamin D 3 treatment, bone retardation became more marked in all patients in group 1 (Figure). The bone maturation rate expressed as bone age/chronologie age was found to be 0.36 to 0.75 (Table 3). Five of the 6 patients developed renal osteodystrophy during this period. No relation was found between the severity of the renal osteodystrophy and the bone maturation rate. The bone disease was no more prominent in patients in whom bilateral nephrectomy was performed than in children with the kidneys in situ. During the period of treatment with lot:-OH vitamin D 3 the bone maturation rate was normal (Figure, Table 3). Moreover, the bone lesions markedly improved in the 5 patients with renal osteodystrophy both with regard to the rickets and the ostitis fibrosa. However, in the patient without evidence of renal osteodystrophy before administration of lot: - OH vitamin D 3 , slight abnormalities indicating ostitis fibrosa were apparent at the examination following treatment (Table 2). In group 2, normal bone age was observed in 2 patients (Nos 7, 8), aged about 16 years at the first radiography, while bone age in the other children (Nos 9-11), aged 12 to 13 years, was retarded 23 to 31 months (Table 2). All the patients had a slight degree of halisteresis. The patients received a well functioning renal transplant shortly after the first radiography; therefore, only few data concerning bone age before surgery are available (Figure).
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Table 3 Bone maturation rate expressed as the ratio increase in bone age (monthsilincrease in chronologie age (months) in hemodialysis patients before and during treatment with ICY. - 0 H-vitamin D3 Case No.
Before lCY.-OH-D 3 treatment
During lCY.-OH-D 3 treatment
Period of ICY. - OH - D 3 treatment (months)
1 2 3
1.27
22
5 6
0.43 0.36 0.44 0.75 0.47 0.57
1.11 LSO 1.00 0.50 0.70
11 2 7 8 14
Mean Range
0.50 0.36-0.75
1.01 0.50-LSO
10.7
4
2-22
Following transplantation a normal bone maturation rate was attained in all patients (Figure). None of these patients developed radiographic abnormalities suggestive of osteodystrophy. Discussion
A retarded bone maturation and radiologic signs of renal osteodystrophy were found in children with chronic renal disease, as in previous investigations (SCHARER et colI., STICKLER). Although the present results indicate that retarded bone age may occur without radiographic evidence of renal osteodystrophy, abnormal calcium and phosphorus metabolism is probably an important cause of growth failure and renal osteodystrophy in these patients. During treatment with the biologically active 1.25 (OH)2 vitamin D, or the synthetic 1ex-OH vitamin D a, the calcium and phosphorus metabolism may become normalized (NIELSEN et colI., CHESNEY et colI.) with subsequent healing of the uremic bone lesions and acceleration of the growth. However, the effect of these vitamin D metabolites on bone maturation has not previously been described. During the period of hemodialysis the bone maturation rate was reduced and renal osteodystrophy developed. In the period of 1ex - OH vitamin D, treatment the bone maturation rate was normalized and a marked improvement in the uremic bone lesions-rickets as well as ostitis fibrosa-occurred, as in the series reported by NIELSEN et colI. Opinions differ about the growth rate in children with renal transplants. GRUSHKIN & FINE(1973) have suggested that growth was poor in transplanted children with bone age corresponding to more than 12 years. However, CHANTLER et colI. (1977) could not confirm this suggestion. In the present series a normal bone maturation rate was found in all patients following successful renal transplantation. The bone age at the first examination indicated that the bone maturation rate had been abnormally low
Downloaded from acr.sagepub.com at UNIV OF MICHIGAN on July 22, 2015
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A. JOHANNSEN, H. E. NIELSEN AND H. E. HANSEN
in the period before transplantation in the younger but not in the older patients. The normal bone maturation following renal transplantation might be due to improved renal function with production of 1.25 (OH)2 vitamin D 3 , the kidney being the sole place of C - 1 hydroxylation necessary for the transformation of vitamin D into the active metabolite (FRASER & KODICEK). It is concluded that loc:-OH vitamin D 3 treatment as well as successful renal transplantation may normalize the bone maturation rate in children with chronic renal failure.
Acknowledgements 1IX - OH vitamin DB was kindly supplied by Leo Pharmaceutical Products, Copenhagen, Denmark.
SUMMARY In 8 of 11 children with terminal chronic renal failure, bone age was retarded 6 months to 3 years. During hemodialysis the bone maturation rate decreased. 1IX - OH vitamin DB treatment and renal transplantation normalized the bone maturation rate.
ZUSAMMENFASSUNG Bei 8 von 11 Kindem mit herabgesetzter Nierenfunktion war das Knochenalter 6 Monate bis 3 Jahre verspatet. Wahrend Hamodialyse sank die Knochenreifungsrate. Mit 1IX - OH Vitamen Ds-Behandlung und Nierentransplantation normalisierte sich die Knochenreifungsrate.
RESUME Chez 8 enfants sur 11 atteints d'insuffisance renale chronique terminale, l'age osseux etait en retard de 6 mois it 3 ans. Pendant l'hemodialyse la vitesse de maturation osseuse diminue. Le traitement par la vitamine D. 1IX - OH et la transplantation renale ont normaIises la vitesse de maturation osseuse.
REFERENCES ANDERSEN E.: Skeletal maturation of Danish school children in relation to height, sexual development and social conditions. Thesis, University of Aarhus 1968. CHANTLER c., DONCKERWOLCKE R. A., BRUNNER F. P., GURLAND H. J., HATHWAY R. A, JACOBS c., SELWOOD N. H. and WING A J.: Combined report on regular dialysis and transplantation of children in Europe, 1976. In: Proceedings of the XIVth European Dialysis and Transplant Association, p. 70. EdIted by B. H. B. Robinson. Pitman Medical Publishing Co., Kent, England 1977. CHESNEY R. W., MOORTHY A V., EISMAN J. A, JAX D. K., MAZESS R. B. and DELUCA H. F.: Increased growth after long-term oral 1IX,25-vitamin D. in childhood renal osteodystrophy. New Engl. J. Med. 298 (1978), 238. FRASER D. R. and KODICEK E.: Unique biosynthesis by kidney of a biologically active vitamin D metabolite. Nature 228 (1970), 764.
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GREULICH W. W. and PYLE S. J.: Radiographic atlas of skeletal development of the hand and wrist. Second edition. Stanford University Press, Stanford, California, 1959. GRUSHKIN C M. and FINE R. N.: Growth in children following renal transplantation. Amer. J. Dis. Child. 125 (1973), 514. MATHIASEN M. S.: Determination of bone age and recording of minor skeletal hand abnormalities in normal children. Dan. med. Bull. 20 (1973), 80. NIELSEN H. E., MELSEN F., CHRISTENSEN M. S., HANSEN H. E., RODBRO P. and JOHANNSEN A.: 1IX hydroxycholecalciferol treatment of long-term hemodialyzed patients. Effects on mineral metabolism, bone mineral content and bone morphometry. Clin. Nephrology 8 (1977), 429. . SCHARER K., CHANTLER C, BRUNNER F. P., GURLAND H. J., JACOBS C, SELWOOD N. H., SPIES G. and WING A. J.: Combined report on regular dialysis and transplantation of children in Europe, 1975. In: Proceedings of the XIIlth Congress of European Dialysis and Transplant Association, p. 60. Edited by B. H. B. Robinson. Pitman Medical Publishing Co., Kent, England 1976. STICKLER G. B.: Growth failure in renal disease. Pediat. Clin. N. Amer. 23 (1976), 885.
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BONE MATURATION IN CHILDREN WITH CHRONIC RENAL FAILURE Effect of let - hydroxy vitamin D, and renal transplantation A. JOHANNSEN, H. E. NIELSEN and H. E. HANSEN Bone age is often retarded in children with chronic renal failure (SCHARER et coIl. 1976, STICKLER 1976). As the kidney is the sole site of C - I hydroxylation, the transformation of vitamin D to the biologically active metabolite 1.25 (OH)2 vitamin D, is reduced in these patients (FRASER & KODICEK 1970). Increased growth and healing of bone lesions have previously been reported to occur in children with renal osteodystrophy when treated with 1.25 (OH)2 vitamin D, (CHESNEY et colI. 1978) and healing of bone lesions has been demonstrated in children treated with let - OH vitamin D, (NIELSEN et coIl. 1977). However, no report concerning the effect of 1.25 (OH)2 vitamin D, and 1et-OH vitamin D, on bone maturation in children with chronic renal failure has appeared in the literature. The effects of treatment with let - OH vitamin D, on bone maturation in children during hemodialysis were analysed and compared with the effect of successful renal transplantation. The results are now reported.
Material and Methods The material comprised II children aged 2 to 17 years treated at this hospital for chronic renal failure during 1968 to 1977. Submitted for publication 14 June 1978. Acta Radiologica Diagnosis 20 (1979) Fasc. 1 B
13 -795844
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A. JOHANNSEN, H. E. NIELSEN AND H. E. HANSEN
Table 1 Clinical data on 11 children with chronic renal failure
Case No.
1 2 3
4 5 6 7 8
9 10 11
Age on admission (years)
Clinical diagnosis
Period of dialysis (months)
10
CPN CPN CGN CGN CPN CRD CGN CRD CPN CGN CGN
64 64 76 56 40 0 3 4
10 8 10 8
1 15 15 13 13 12
0 2 3
Period of immunosuppressive therapy (months)
9 0 1 0 1
Bilateral Successful nephrectomy renal transplantation
+ + + +
0
43 27 51 69 30
+ + + + +
+ + + + +
CPN = Chronic pyelonephritis. CRD = Congenital renal disease. CGN = Chronic glomerulonephritis.
The patients were classified into two groups: (1) Patients treated with l z - OR vitamin D a, and (2) patients with a well functioning renal transplant. All children except 2 were treated with hemodialysis for 2 to 76 months (Table 1). The duration of dialysis was 6 hours 3 times per week, using a 1 m 2 13.5,um thick couprophane membrane (Rhone-Poulenc, RP5). The dialysis unit was supplied with distilled water and the dialysate contained 3.0 mEqjl of calcium and 1.3 mEqjl of magnesium. The patients' diet contained 40 to 70 g protein, 20 to 30 mEq sodium and 500 to 600 mg calcium per day. The patients in group 1 (5 hemodialysed and 1 non-dialysed) were treated with loc-OR vitamin D, for 2 to 22 months (mean 10.7 months). loc-OR vitamin D 3 was given initially in an oral dose of 1 ,ug per day for maintaining the level of serum calcium within the upper normal range. Serum phosphorus was regulated by aluminium aminoacetate (1.2-3.6 g orally per day) during the period of 10:~OR vitamin D 3 treatment. Three patients in this group received a renal transplant before the 10: ~ OR vitamin D 3 treatment (Figure). The renal transplant never functioned or was rejected in these patients. All 5 patients in group 2 had well functioning renal transplants. They were treated with hemodialysis for 0 to 4 months before the transplantation (Table 1). Films of the skeleton were obtained in most patients every 6 to 12 months. Children treated with l « - OR vitamin D 3 were examined both before and after the treatment. The bone age was evaluated by comparing the size and shape of the ossification
Downloaded from acr.sagepub.com at UNIV OF MICHIGAN on July 22, 2015
BONE MATURATION IN CHILDREN WITH CHRONIC RENAL FAILURE bone age
start of 1Cl'-OH-Oa treatment
195
renal transplantation
220 200 180 160 140 120 11'
100 80 60 50 40 30 20 10 50 40 30 20 10 0 10 20 30
30 20 10 0 10 20 30 40 50 60 observation period Bone maturation (in months) in hemodialysed children before and after treatment with I« - OH vitamin D 3 (Nos 1-6) and in children after successful renal transplantation (Nos 7-11). In case 7 (female) and case 8 (male) the epiphyseal plates closed at the end of observation period (in months). T Renal transplant before 1a - OH - D 3 •
centres and epiphyseal cartilage in the hands and wrists with the standards given in the atlas of GREULICH & PYLE (1959). The figures were related to healthy Danish children, who are retarded 6 to 12 months in relation to the North American standard (ANDERSEN 1968, MATHIASEN 1973). Moreover all films of the skeleton were reviewed with regard to renal osteodystrophy. Results At the first radiography open epiphyseal plates were found in all patients. In 5 patients in group 1 (Nos 1-5), aged 8 to 10 years, bone maturation was retarded from 6 to 27 months, while normal bone age was found in a one-year-old child (No.6). Initially this child had marked osteodystrophy, while the other patients in the
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A. JOHANNSEN, H. E. NIELSEN AND H. E. HANSEN
Table 2 Radiologic bone abnormalities in 11 children with chronic renal failure
Case No.
Age at first radiography (months)
Bone age retardation (months)
Radiographic renal osteodystrophy At first examination
In relation to IGl:-OH D, treatment or successful renal transplant Rickets
1 2 3 4 5 6 7
8 9 10 11
130 120 102 121 104 13 198 190 166 166 154
15 6 9
27 10 0 0 0 23 25 36
Ostitis fibrosa
Before
After
Before
After
++
+
+ ++ +++
+ +
++ ++ ++ ++ +++
+ + + ++ + +
+ +
group only had varying degrees of halisteresis but no characteristics indicating renal osteodystrophy (Table 2). In the period of hemodialysis before lot:-OH vitamin D 3 treatment, bone retardation became more marked in all patients in group 1 (Figure). The bone maturation rate expressed as bone age/chronologie age was found to be 0.36 to 0.75 (Table 3). Five of the 6 patients developed renal osteodystrophy during this period. No relation was found between the severity of the renal osteodystrophy and the bone maturation rate. The bone disease was no more prominent in patients in whom bilateral nephrectomy was performed than in children with the kidneys in situ. During the period of treatment with lot:-OH vitamin D 3 the bone maturation rate was normal (Figure, Table 3). Moreover, the bone lesions markedly improved in the 5 patients with renal osteodystrophy both with regard to the rickets and the ostitis fibrosa. However, in the patient without evidence of renal osteodystrophy before administration of lot: - OH vitamin D 3 , slight abnormalities indicating ostitis fibrosa were apparent at the examination following treatment (Table 2). In group 2, normal bone age was observed in 2 patients (Nos 7, 8), aged about 16 years at the first radiography, while bone age in the other children (Nos 9-11), aged 12 to 13 years, was retarded 23 to 31 months (Table 2). All the patients had a slight degree of halisteresis. The patients received a well functioning renal transplant shortly after the first radiography; therefore, only few data concerning bone age before surgery are available (Figure).
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Table 3 Bone maturation rate expressed as the ratio increase in bone age (monthsilincrease in chronologie age (months) in hemodialysis patients before and during treatment with ICY. - 0 H-vitamin D3 Case No.
Before lCY.-OH-D 3 treatment
During lCY.-OH-D 3 treatment
Period of ICY. - OH - D 3 treatment (months)
1 2 3
1.27
22
5 6
0.43 0.36 0.44 0.75 0.47 0.57
1.11 LSO 1.00 0.50 0.70
11 2 7 8 14
Mean Range
0.50 0.36-0.75
1.01 0.50-LSO
10.7
4
2-22
Following transplantation a normal bone maturation rate was attained in all patients (Figure). None of these patients developed radiographic abnormalities suggestive of osteodystrophy. Discussion
A retarded bone maturation and radiologic signs of renal osteodystrophy were found in children with chronic renal disease, as in previous investigations (SCHARER et colI., STICKLER). Although the present results indicate that retarded bone age may occur without radiographic evidence of renal osteodystrophy, abnormal calcium and phosphorus metabolism is probably an important cause of growth failure and renal osteodystrophy in these patients. During treatment with the biologically active 1.25 (OH)2 vitamin D, or the synthetic 1ex-OH vitamin D a, the calcium and phosphorus metabolism may become normalized (NIELSEN et colI., CHESNEY et colI.) with subsequent healing of the uremic bone lesions and acceleration of the growth. However, the effect of these vitamin D metabolites on bone maturation has not previously been described. During the period of hemodialysis the bone maturation rate was reduced and renal osteodystrophy developed. In the period of 1ex - OH vitamin D, treatment the bone maturation rate was normalized and a marked improvement in the uremic bone lesions-rickets as well as ostitis fibrosa-occurred, as in the series reported by NIELSEN et colI. Opinions differ about the growth rate in children with renal transplants. GRUSHKIN & FINE(1973) have suggested that growth was poor in transplanted children with bone age corresponding to more than 12 years. However, CHANTLER et colI. (1977) could not confirm this suggestion. In the present series a normal bone maturation rate was found in all patients following successful renal transplantation. The bone age at the first examination indicated that the bone maturation rate had been abnormally low
Downloaded from acr.sagepub.com at UNIV OF MICHIGAN on July 22, 2015
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in the period before transplantation in the younger but not in the older patients. The normal bone maturation following renal transplantation might be due to improved renal function with production of 1.25 (OH)2 vitamin D 3 , the kidney being the sole place of C - 1 hydroxylation necessary for the transformation of vitamin D into the active metabolite (FRASER & KODICEK). It is concluded that loc:-OH vitamin D 3 treatment as well as successful renal transplantation may normalize the bone maturation rate in children with chronic renal failure.
Acknowledgements 1IX - OH vitamin DB was kindly supplied by Leo Pharmaceutical Products, Copenhagen, Denmark.
SUMMARY In 8 of 11 children with terminal chronic renal failure, bone age was retarded 6 months to 3 years. During hemodialysis the bone maturation rate decreased. 1IX - OH vitamin DB treatment and renal transplantation normalized the bone maturation rate.
ZUSAMMENFASSUNG Bei 8 von 11 Kindem mit herabgesetzter Nierenfunktion war das Knochenalter 6 Monate bis 3 Jahre verspatet. Wahrend Hamodialyse sank die Knochenreifungsrate. Mit 1IX - OH Vitamen Ds-Behandlung und Nierentransplantation normalisierte sich die Knochenreifungsrate.
RESUME Chez 8 enfants sur 11 atteints d'insuffisance renale chronique terminale, l'age osseux etait en retard de 6 mois it 3 ans. Pendant l'hemodialyse la vitesse de maturation osseuse diminue. Le traitement par la vitamine D. 1IX - OH et la transplantation renale ont normaIises la vitesse de maturation osseuse.
REFERENCES ANDERSEN E.: Skeletal maturation of Danish school children in relation to height, sexual development and social conditions. Thesis, University of Aarhus 1968. CHANTLER c., DONCKERWOLCKE R. A., BRUNNER F. P., GURLAND H. J., HATHWAY R. A, JACOBS c., SELWOOD N. H. and WING A J.: Combined report on regular dialysis and transplantation of children in Europe, 1976. In: Proceedings of the XIVth European Dialysis and Transplant Association, p. 70. EdIted by B. H. B. Robinson. Pitman Medical Publishing Co., Kent, England 1977. CHESNEY R. W., MOORTHY A V., EISMAN J. A, JAX D. K., MAZESS R. B. and DELUCA H. F.: Increased growth after long-term oral 1IX,25-vitamin D. in childhood renal osteodystrophy. New Engl. J. Med. 298 (1978), 238. FRASER D. R. and KODICEK E.: Unique biosynthesis by kidney of a biologically active vitamin D metabolite. Nature 228 (1970), 764.
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GREULICH W. W. and PYLE S. J.: Radiographic atlas of skeletal development of the hand and wrist. Second edition. Stanford University Press, Stanford, California, 1959. GRUSHKIN C M. and FINE R. N.: Growth in children following renal transplantation. Amer. J. Dis. Child. 125 (1973), 514. MATHIASEN M. S.: Determination of bone age and recording of minor skeletal hand abnormalities in normal children. Dan. med. Bull. 20 (1973), 80. NIELSEN H. E., MELSEN F., CHRISTENSEN M. S., HANSEN H. E., RODBRO P. and JOHANNSEN A.: 1IX hydroxycholecalciferol treatment of long-term hemodialyzed patients. Effects on mineral metabolism, bone mineral content and bone morphometry. Clin. Nephrology 8 (1977), 429. . SCHARER K., CHANTLER C, BRUNNER F. P., GURLAND H. J., JACOBS C, SELWOOD N. H., SPIES G. and WING A. J.: Combined report on regular dialysis and transplantation of children in Europe, 1975. In: Proceedings of the XIIlth Congress of European Dialysis and Transplant Association, p. 60. Edited by B. H. B. Robinson. Pitman Medical Publishing Co., Kent, England 1976. STICKLER G. B.: Growth failure in renal disease. Pediat. Clin. N. Amer. 23 (1976), 885.
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