hepatobiliary disease
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1 Archives of Disease in Childhood, 1974, 49, 641 Bone disease in infants and children with hepatobiliary disease AKIO KOBAYASHI, SAKAE KAWAI, TAKEKO UTSUNOMIYA, and YOSHIRO OHBE From the Section of Gastroenterology, Department of Paediatrics, National Children's Hospital, Tokyo Kobayashi, A, Kawai, S, Utsunomiya, T, and Ohbe, Y (1974) Archives of Disease in Childhood, 49, 641 Bone disease in infants and children with hepatobiliary disease Radiological studies of bone were performed in infants and children with hepatobiliary disease Rickets was found in 23 out of 39 patients (59%) with surgically unrepaired biliary atresia, in 4 out of 15 (27%) with surgically repaired biliary atresia, in 11 out of 21 (52%) with neonatal hepatitis, and in 2 out of 4 (5%) with intrahepatic cholestasis Osteoporosis was found in 23 out of 39 (59%) with unrepaired biliary atresia, in 3 out of 15 (2%) with repaired biliary atresia, in 5 out of 21 (24%) with neonatal hepatitis, and in 1 out of 4 (25%) with intrahepatic cholestasis 2 girls with Byler disease and 1 infant with choledochal cyst showed no radiological evidence of bone disease In unrepaired biliary atresia comparative studies of biochemical data in the groups with and without bone disease showed the following Serum calcium levels were reduced in the patients with bone disease compared with those in the group without it Serum magnesium levels were markedly reduced in the groups with and without bone disease The product of serum calcium and phosphorus was reduced in the group with osteoporosis compared with that in the group without it The raised levels of serum alkaline phosphatase were unrelated to the presence or absence of bone disease Bone disease has been described in association with chronic liver disease in adults (Atkinson, Nordin, and Sherlock, 1956; Kehayoglou et al, 1968) Atkinson et al (1956) reported 22 adult patients with obstructive jaundice, in 6 of whom a diagnosis of osteomalacia was made However, there have been conspicuously few reports on this subject in infants and children (Teng et al, 1961; Yu, WalkerSmith, and Burnard, 1971) This paper describes the incidence of bone disease in infants and children with hepatobiliary disease, the age of onset, and comparative biochemical studies between the groups with and without bone disease Materials and methods The subjects were 54 infants with biliary atresia, 15 of whom were successfully repaired by hepatic portojejunostomy and had no jaundice (Kobayashi et al, 1973), 21 infants with neonatal hepatitis, 4 infants and Received 28 January children with intrahepatic cholestasis, 2 girls with Byler disease (Kobayashi et al, 1975), and 1 infant with choledochal cyst All patients with biliary atresia had laparotomy and the diagnosis was confirmed Diagnosis of neonatal hepatitis was on clinical and laboratory grounds, excluding other diseases causing obstructive jaundice during infancy Of 4 patients with intrahepatic cholestasis, 3 had socalled intrahepatic biliary atresia shown by laparotomy and histological studies The other had intrahepatic cholestasis of unknown aetiology These 4 patients complained of severe pruritus, and 2 of 3 patients with intrahepatic biliary atresia had developed xanthoma Diagnosis of Byler disease was on clinical and laboratory grounds (Clayton et al, 1969), based on jaundice with intermittent exacerbations, severe pruritus, hepatosplenomegaly, dwarfing, mental retardation, raised serum alkaline phosphatase levels, normal or low serum cholesterol values, hypoprothrombinaemia, and biliary cirrhosis The state of the skeleton was assessed in each case by xrays of both wrist joints Xrays were made 1 to 6 times for each case with variable intervals A diagnosis of rickets was made by the rarefaction and irregular 641 Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from on 24 December 218 by guest Protected by copyright
2 642 fraying of the provisional zone of calcification ofthe distal end of the ulna was not considered significant because it is observed in some nonrachitic infants A diagnosis of osteoporosis was made on radiological grounds based on the thin cortex of the radius and reduced bone density In unrepaired biliary atresia comparative studies of biochemical data were performed in 2 groups The data in the group with bone disease were determined when bone disease was detected on xrays, and in the group without it at the latest examination of normal xrays Serum alkaline phosphatase levels were measured by the method of Kind and King (1954) Serum calcium was determined by a modification of the method of Connerty and Briggs (1966) using the metal complexing dye orthocresolphthalein complexone, and magnesium by the method of Schachter (1961) using a spectrofluorometer Serum phosphorus was determined by a modification of the method of Fiske and Subbarow (1925) In some cases of biliary atresia the heat stability of serum alkaline phosphatase was studied by the method of Posen, Neale, and Clubb (1965) A4) a L a Age (months) Kobayashi, Kawai, Utsunomiya, and Ohbe Cupping Results Incidence of rickets and osteoporosis in hepatobiliary disease (Fig 1 and 2) Rickets was found in 23 out of 39 patients (59%) with surgically unrepaired biliary atresia The lesion was observed in 4 out of 15 (27%) with surgically repaired biliary atresia Osteoporosis was diagnosed in 23 out of 39 patients (59%) with surgically unrepaired biliary atresia, and in 3 out of 15 (2%) with surgically 6 (>~~~~~~~~~~~~~~~~(F (> 9" * 4 a 4) 4)CL ~~~~~~~~~~~~~ 4 * 4_ 4 repaired biliary atresia Of 39 patients with biliary atresia, 17 had both rickets and osteoporosis Exact age of onset of these bone diseases was obscure in most cases because the diseases developed insidiously and because xrays were not made at regular intervals In our series of biliary atresia the age at which rickets developed ranged from 1 to 4 months, and that of osteoporosis 1 to 5 months In neonatal hepatitis the incidence of rickets was the same as in unrepaired biliary atresia It * Rickets o No rickets * Rickets during imvitamin D, No rickets during im vitamin D WO Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from A _ os o go ~~~~~~~ S ooo ~~~~~~ o o~~~~ o FIG 1Radiological studies of bone in 54 patients with biliary atresia _ o~~~~~~~~~~~~~~~~~~ on 24 December 218 by guest Protected by copyright
3 L_ 4) 4) c cu 4) cx Bone disease in infants and children with hepatobiliary disease 643 Age (months) 6 ** (1 4 * Osteoporosis o No osteoporosis * Osteoporosis during im vitamin D 4 No osteoporosis during im vitamin D v O oe ~ ~ ~ ~ ~ ~ * _ \P, ~~~~~~~~ * 4~~~~~~~~~ o CO o 4 o _ S FIG 2Radiological studies of bone in 54 patients with biliary atresia appeared in 11 of 21 cases (52 %) The lesions, however, disappeared in most cases by the age of 6 months Osteoporosis, on the other hand, developed in 5 of 21 (24%), and these 5 infants with osteoporosis also showed the signs of rickets Of 4 cases of intrahepatic cholestasis, 2 showed the radiological evidence of rickets and 1 showed osteoporosis 2 girls with Byler disease and 1 infant with choledochal cyst had no radiological signs of bone disease Comparative studies of biochemical data in the group with and without bone disease in unrepaired biliary atresia (Table and Fig 3) Serum alkaline phosphatase levels were high in most cases of biliary atresia and were higher in those with rickets and/or osteoporosis than in those without these lesions However, the difference was not significant In some cases of biliary atresia with and without rickets the heat stability of alkaline phosphatase was evaluated to assess these high values (Fig 3) The results showed that the greater contribution of liver alkaline phosphatase was responsible for these high values The mean concentration of serum calcium in the patients with rickets was 4 4 meq/l (SD 42, no = 15) with a range of 3 * 7 to 5 * In the group without rickets the value was 4 * 76 meq/l (SD 51, no = 16) with a range of 4 to 5 4, and the difference between these 2 groups was significant (P < * 5) The same relation was present between serum levels of calcium in the patients with and without osteoporosis (mean 4*37 meq/l, SD 49, no = 14, and range 37 to 54 in the patients with osteoporosis; mean 4 * 7 meq/l, SD * 43, no = 19, and range 4 to 5 4 in those without osteoporosis; P < *5) In biliary atresia serum magnesium levels were conspicuously reduced below the normal range The degree of reduction was greater than that of Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from on 24 December 218 by guest Protected by copyright
4 644 1, E,5 ~4 3 2 l 1 _tj Kobayashi, Kawai, Utsunomiya, and Ohbe 1% TAB Blood chemical data in the groups with and With bone disease (mean ± SD) (no) Rickets Without bone disease (mean ± SD) (no) Alkaline phosphatase (KindKing units) 59*7 21*7 (22) 492 ±2*5 (24) Calcium (meq/l) (15) (16) Magnesium (meq/l) 1 39± 27 (12) 153±19 (1) Ca (mg/1 ml) xp (mg/1 ml) 217±97 (15) 277±84 (15) The difference was not significant between these groups The value was, however, significantly reduced in the patients with osteoporosis compared with those without the lesion The mean value was 19 8 (SD 16, no = 13) in the patients with osteoporosis, and 28 (SD 85, no = 17) in those without the lesion Discussion The ~ present study showed a high incidence of bone disease in hepatobiliary disease in infancy and childhood In biliary atresia, in which bile flow into the gut was completely absent, more than half Biliary a tresia with rickets the patients studied had bone disease The Biliary atresia without rickets incidence of rickets was 6%, the same as that of Normal ccontrol osteoporosis Rickets developed about 3 months of agea little earlier than the osteoporosis In surgically repaired biliary atresia the incidence of M nutes at 56 C bone disease was conspicuously decreased, and the lesions were rarely seen after the age of 12 months FIG 3The heat stability test serum phosphatase in 1 normal In most of these cases the infan lesions were associated it and 4 infants with unwith ascending cholangitis after surgery (Kobayashi repaired biliary atresia In bili, cary atresia the main portion of serum alkaline phosphatase was heat stable and the et al, 1973) In neonatal hepatitis rickets was declining curves were unrelated tto the presence or absence of observed in half of the patients and cured rickets spontaneously by the age of 6 months On the other hand, osteoporosis was seen only in 25% of serum calcium, especially in the patients with bone cases of this disease All patients with osteoporosis disease The mean value was 1 39 meq/l (SD also had the radiological signs of rickets This low 27, no = 12) with a rant ge of (9 to 1 8 in the incidence of osteoporosis compared with that of patients with rickets, and 1l 53 meq/l (SD 19, rickets in neonatal hepatitis was due to the fact that no = 1) with a range of 1 2 to 1 8 in those without neonatal hepatitis had a favourable clinical course on the lesion The differencwe was, however, not followup and was cured in most cases by the age of significant between these 2 groups The mean 6 months In intrahepatic cholestasis the patients value was 1 41 meq/l (SD 26, no = 1) with a showed the same incidence of bone disease as in range of 9 to 1 8 in the paitients with osteoporosis, neonatal hepatitis In one case of choledochal cyst and 1 56 meq/l (SD 22, no = 13) with a range no bone disease was seen In Byler disease 2 of 1 1 to 18 in those withlout osteoporosis The patients had no rickets or osteoporosis, but had difference between these wals also not significant knock knees The mean value of the product of serum calcium The reported incidence of bone disease in hepatoand phosphorus concentratic)ns was 21 7 mg/1 ml biliary disease in infancy and childhood is variable (SD 9 7, no 15) in the = pcatients with rickets, and In the report of BastisMaounis, Matsaniotis, 27 7 (SD 8 4, no = 15) in t:hose without the lesion and Maounis (1973) 3 out of 7 patients with biliary Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from on 24 December 218 by guest Protected by copyright
5 LE without bone disease in unrepaired biliary atresia Difference Bone disease in infants and children with hepatobiliary disease Osteoporosis With bone disease Without bone disease (mean ± SD) (no) (mean ± SD) (no) Difference NS 62 *±24*9 (2) 5*9+17*8 (28) NS P < ± 49 (14) 47±43 (19) P < 5 NS 1 41± 26 (1) 1 56± 22 (13) NS NS 19*8+1*6 (13) 28+8*5 (17) P < *5 atresia showed radiological evidence of rickets, and 7 out of 11 with neonatal hepatitis In the paper entitled 'Rickets: a common complication of neonatal hepatitis' by Yu et al (1971), 4 out of 3 infants with the disease had rickets There has been, however, meagre information available on the incidence of osteoporosis in hepatobiliary disease in childhood except for the report by Teng et al (1961) The pathogenesis of bone disease in hepatobiliary disease has been poorly understood Bile is important for the intestinal absorption of calcium and magnesium because it is necessary for the absorption of vitamin D (Schachter, Finkelstein, and Kowarski, 1964), which enhances the absorption of both elements Bone disease may be attributable to the malabsorption of these elements in hepatobiliary disease in which bile flow into the intestines is deficient or absent (Kobayashi et al, 1974) Furthermore, vitamin D that is absorbed from the gastrointestinal tract via the lymphatics and is transported from there to the liver in the chylomicron of the plasma may be hydroxylated in the liver to a more potent metabolite, 25hydroxycholecalciferol (25HCC) (Lund and DeLuca, 1966; Ponchon, Kennan, and DeLuca, 1969), which is thought to be converted to more active forms, 1,25 or 21,25dihydroxycholecalciferol (1,25 or 21,25 DHCC) in the kidneys (Fraser and Kodicek, 197) Since the initial step of transformation of vitamin D to its active form may take place in the liver, there may be a failure to metabolize the vitamin adequately, and there is some evidence that this may occur in hepatic cirrhosis (Ponchon and DeLuca, 1969) Yu et al (1971) postulated that rickets associated with neonatal hepatitis was due to the impairment of the hepatic conversion of vitamin D to its biologically active form Conditions which are accompanied with intraand extrahepatic cholestasis may cause biliary cirrhosis These disorders include congenital biliary atresia, protracted neonatal hepatitis, Byler disease, etc Among these, surgically unrepaired 645 biliary atresia is rapidly progressive and patients who survive over 12 months show advanced biliary cirrhosis The cirrhotic patients show severe impairment of liver function and a systemic deficit of protein This protein deficit may be an important aetiological factor of osteoporosis in liver disease since osteoporosis is widely considered to be a disorder of the protein matrix of bone (Cooke, 1955) In neonatal hepatitis, fewer patients had osteoporosis than rickets, whereas in biliary atresia the incidence of osteoporosis was the same as that of rickets These observations accord better with the fact that deficient or absent bile flow into the gut is observed in both diseases, though biliary cirrhosis is a common feature of biliary atresia but not of neonatal hepatitis In biliary atresia serum concentrations of calcium were significantly reduced in the patients with bone disease compared with those without it Serum magnesium levels were conspicuously reduced in the groups with and without bone disease, and there was no significant difference in serum levels between these 2 groups The reduction of the product of serum calcium and phosphorus was significant in the group with osteoporosis compared with that in the group without the lesion, but not significant for rickets The serum levels of alkaline phosphatase were unrelated to the presence or absence of bone disease Its raised levels were of hepatic origin, shown by a heat inactivation procedure This observation was not in accord with that of Bastis Maounis et al (1973), who reported that the high values of serum alkaline phosphatase in association with hepatic disease in infants reflected, at least in part, a secondary vitamin D deficiency Out of 6 cases of unrepaired biliary atresia that had no signs of rickets over the age of 12 months, 2 had received vitamin D 3, IU weekly intramuscularly Kobayashi et al (1974) showed that in biliary atresia oral vitamin D had little, if any, effect on the absorption of calcium and magnesium, though the vitamin moderately increased absorption Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from on 24 December 218 by guest Protected by copyright
6 646 Kobayashi, Kawai, Utsunomiya, and Ohbe when given intramuscularly It is reasonable to conclude from these studies that vitamin D should be given intramuscularly to reduce the incidence and severity of rickets in this disorder In neonatal hepatitis oral vitamin D supplement in a dosage of 2 IU daily was recommended by some workers (Danks, 1965; Yu et al, 1971), but we found that rickets was spontaneously cured by the age of 6 months in this condition REFERENcES Atkinson, M, Nordin, B E C, and Sherlock, S (1956) Malabsorption and bone disease in prolonged obstructive jaundice Quarterly J3ournal of Medicine, 25, 299 BastisMaounis, B, Matsaniotis, N, and Maounis, F (1973) Serum alkaline phosphatase in infants with obstructive jaundice: relation to vitamin D supplementation Journal of Pediatrics, 82, 68 Clayton, R J, Iber, F L, Ruebner, B H, and McKusick, V A (1969) Byler disease Fatal familial intrahepatic cholestasis in an Amish kindred American Journal of Diseases of Children, 117, 112 Connerty, H V, and Briggs, A R (1966) Determination of serum calcium by means of orthocresolphthalein complexone American Journal of Clinical Pathology, 45, 29 Cooke, A M (1955) Osteoporosis Lancet, 1, 877, 929 Danks, D M (1965) Prolonged neonatal obstructive jaundice A survey of modem concepts Clinical Pediatrics, 4, 499 Fiske, C H, and Subbarow, Y (1925) The colorimetric determination of phosphorus Journal of Biological Chemistry, 66, 375 Fraser, D R, and Kodicek, E (197) Unique biosynthesis by kidney of a biologically active vitamin D metabolite Nature, 228, 764 Kehayoglou, A K, Holdsworth, C D, Agnew, J E, Whelton, M J, and Sherlock, S (1968) Bone disease and calcium absorption in primary biliary cirrhosis With special reference to vitamind therapy Lancet, 1, 715 Kind, P R N, and King, E J (1954) Estimation of plasma phosphatase by determination of hydrolyzed phenol with aminoantipyrine Journal of Clinical Pathology, 7, 322 Kobayashi, A, Kawai, S, Utsunomiya, T, and Ohbe, Y (1975) Byler disease in 2 Japanese girls (In preparation) Kobayashi, A, Utsunomiya, T, Ohbe, Y, and Nagashima, Y (1974) Intestinal absorption of calcium and magnesium in hepatobiliary disease in infancy Archives of Disease in Childhood, 49, 9 Kobayashi, A, Utsunomiya, T, Ohbe, Y, and Shimizu, K (1973) Ascending cholangitis after successful surgical repair of biliary atresia Archives of Disease in Childhood, 48, 697 Lund, J, and DeLuca, H F (1966) Biologically active metabolite of vitamin D3 from bone, liver, and blood serum journal of Lipid Research, 7, 739 Ponchon, G, and DeLuca, H F (1969) The role of the liver in the metabolism of vitamin D journal of Clinical Investigation, 48, 1273 Ponchon, G, Kennan, A L, and DeLuca, H F (1969) 'Activation' of vitamin D by the liver Journal of Clinical Investigation, 48, 232 Posen, S, Neale, F C, and Clubb, J S (1965) Heat inactivation in the study of human alkaline phosphatases Annals of Internal Medicine, 62, 1234 Schachter, D (1961) Fluorometric estimation of magnesium with 8hydroxy5quinolinesulfonate journal of Laboratory and Clinical Medicine, 58, 495 Schachter, D, Finkelstein, J D, and Kowarski, S (1964) Metabolism of vitamin D I Preparation of radioactive vitamin D and its intestinal absorption in the rat J7ournal of Clinical Investigation, 43, 787 Teng, C T, Daeschner, C W, Jr, Singleton, E B, Rosenberg, H S, Cole, V W, Hill, L L, and Brennan, J C (1961) Liver disease and osteoporosis in children I Clinical observations Journal of Pediatrics, 59, 684 Yu, J S, WalkerSmith, J A, and Burnard, E D (1971) Rickets: a common complication of neonatal hepatitis Medical Journal of Australia, 1, 79 Correspondence to Dr A Kobayashi, Department of Paediatrics, National Children's Hospital, Taishido 33531, Setagayaku, Tokyo, Japan Arch Dis Child: first published as 11136/adc on 1 August 1974 Downloaded from on 24 December 218 by guest Protected by copyright
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