Osteoarticular Changes in Wilson s Disease
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1 Osteoarticular Changes in Wilson s Disease Edward R. Feller and H. Ralph Schumacher The musculoskeletal system of 17 patients with known Wilson s disease was studied clinically and radiographically. Major abnormalities were seen only in 5 patients over 21 years of age. Multiple calcified loose bodies at the wrists were present in 4, premature degenerative arthritis at the knees with chondromalacia patellae in 4 and chondrocalcinosis at the knees in 2. Mild demineralization was seen at all ages and was present in 9 patients. These unusual wrist and knee changes are infrequently recognized manifestations of Wilson s disease in the adult. Wilson s disease (hepatolenticular degeneration) is an uncommon, recessively inherited disease characterized by excessive retention of copper with degenerative changes in the brain, particularly the basal ganglia and cirrhosis of the liver. The brown or greenishbrown Kayser-Fleischer rings at the limbus of the cornea are pathognomonic of the disease. The onset of clinical illness usually is during childhood or adolescence (1). Presenting manifestations rarely may include renal tubular disease, psychiatric disturbances or hemolytic anemia (2). Radiographic evidence of osteoarticular changes has also been described, but most reviews of Wilson s disease give little mention of bone or joint disease (1-3). Some patients have definite rickets (4, 5) or osteomalacia (6) which has occasionally been attributed to renal tubu- From the Arthritis Section, Department of Medicine, Hospital of the University of Pennsylvania and Veterans Administration Hospital, Philadelphia, Pa. H. RALPH SCHUMACHER, MD: Assistant Professor of Medicine and Director, Arthritis Research, University of Pennsylvania School of Medicine, Chief, Arthritis Section, VA Hospital, Philadelphia, Pa; EDWARD FELLER: Medical Student, University of Pijon, Dijon, France. Reprint requests should be addressed to: Dr. Schumacher, 26 Maloney Building, Hospital of the University of Pennsylvania, 36th and Spruce Streets, Philadelphia, Pa Submitted for publication Sept 2, 1971; accepted Jan 26,1912. lar dysfunction (6,7). Other changes, described mainly in the radiologic literature, include scattered subchondral bone fragmentation (6, 8-1 ), osteoarthritis (6-8), osteochondritis dissecans (2, 4, 8, 9), osteochondritis of the spine (8), paraarticular calcifications (lo), subchondral cysts (9), Milkman pseudofractures (6), pathologic fractures (6-9, 1 l), and possible chondrocalcinosis (11). Demineralization has been reported in as many as 33 of 38 patients in one study (9). This report describes a clinical and radiographic study of 17 patients with Wilson s disease. Our results suggest that bony fragmentation or ossicles at the wrists, premature degenerative arthritis particularly with chondromalacia patellae, and chondrocalcinosis, may be characteristic findings in adults surviving with Wilson s disease. MATERIALS AND METHODS Seventeen patients with known Wilson s disease were studied by clinical and radiographic examination of the musculoskeletal system. Five were asymptomatic siblings of patients with overt Wilson s disease. In all 17, serum ceruloplasmin was less than 2mg/1ml (normal: 2 to 4 mg/1ml) and hepatic copper exceeded 2rg/g of dry liver (normal: less than 5&g of dry liver) (12). Calcium, phosphorous and alkaline phosphatase determinations were obtained from hospital records or repeated at the time of study. Urinary amino acids were measured in 12 patients. A Parker-Pearson needle synovial biopsy of a knee joint Arthritis and Rheumatism, Vol. 15, No. 3 (MayJune 1972) 259
2 FELLER AND SCHUMACHER Fig 1. Bone fragments or accesory bones in the region of the radial-ulnar articulation in this 26-year-old woman with neurologic and hepatic symptoms for 11 years who had been treated with penicillamine for 4 years (Case 14). The left wrist showed similar changes. was performed on 1 patient (Case 1) and examined by light microscopy, using hematoxylin and eosin and the rubeanic acid stain for copper, and by electron microscopy. Radiographic abnormalities were summarized and correlated with clinical assessment of hepatic, renal and central nervous system disease. RESULTS Clinical Aspects Four patients had signs Or symptoms of osteoarthropathy. A 31-year-old woman Fig 2. Wrist showing several distinct bony ossicles adjacent to the medial aspect of the distal radius with a smaller less-defined density at the radial-navicular joint. There are also small cysts in the distal ulna (anow). Thirty-one-year-old woman with hepatic and neurologic symptoms for 2 years who had been treated with penicillarnine for 11 years (Case 16). 26 Arthritis and Rheumatism, Vol. 15, No. 3 (May-June 1972)
3 WILSON'S DISEASE Fig 3. Small loose fragment adjacent to the distal ulna in a 21-year-old woman with hepatic and neurologic abnormalities for ll years and who had been treated with penicillamine for 6 years (Case 13). (Case 16), presented with a history Of sporadic pain and swelling of the knees for several years. Sharp, diffuse pain was elicited by movement of the left patella and knee joint. There was some retropatellar crepitus in the left knee. A 26- year-old woman (Case 14) had rough, painless crepitus of the right wrist on flexion and extension. Retropatellar crepitus was present bilaterally. There was clicking at the lateral menis- Fig4. Small calcified fragment at the base of the middle phalanx of the long finger of the left hand. A similar fragment was also seen about the radius in the left wrist. Thirty-five-year-old man with neurologic and hepatic symptoms for 11 years treated with penicillamine for 7 years (Case 17). cus of the right knee on the McMurray test. A 1" flexion deformity was present at both knees. A 29-year-old woman (Case 15) complained of swelling of the knees with pain on walking for 3 Fig 5A (left). Irregularity of the posterior surface of the patella compatible with chondromalacia patellae. The articular surface of the femoral condyle is also irregular. Note the spurring on the posterior surface of the patella. There are illdefined calcified densities near the tibiofibular joint. Same patient as in Figure 2. B (right). Chondromalacia patellae in a 29-year-old woman who had hepatic and neurologic symptoms for 12 years and who was treated with penicillamine for 5 years (Case 15). Arthritis and Rheumatism, Vol. 15, No. 3 (May-June 1972) 261
4 FELLER AND SCHUMACHER months. She had mild crepitus but no swelling when examined. A fourth patient, a 19-year-old boy (Case 1) presented a 1-day history of dull, steady pain and nontender swelling of the right knee. The proximal interphalangeal joints were slightly enlarged and firm. X-rays of the hands and knees were normal in this patient. Joint aspiration and needle synovial biopsy of the right knee were performed. Synovial fluid was viscous with few cells and no crystals. The synovium was negative for copper by the rubeanic acid stain. There was only equivocal focal lining cell proliferation and subsynovial fibrosis. Sedimentation rate, latex fixation test for rheumatoid factor, and antinuclear factor were done on this patient only and were all normal or negative. Pain and swelling did not recur after the aspiration. He was asymptomatic 1 year later. X-ray Findings The first 3 symptomatic patients and 2 others over age 21 without symptoms or abnormal physical findings had joint x-ray changes. All 4 21-year-old or older patients for whom bone surveys of the wrists were available showed multiple ossified or calcified loose bodies in or about the wrist joints (Figures 1-4) and, in 1 patient each, at the hands and at the knees. These apparent bony fragmentations were not associated with osteoarthritic changes-ie, the joint space was not narrowed nor was there major subchondral sclerosis or irregularity. Four patients (Table) showed premature osteoarthritic changes about the knees with hypertrophic spurring. In each case, this included bilateral chondromalacia patellae (Figures 5A and B). Two of these patients had linear densities in the,joint space compatible with chondrocalcinosis (Figure 6). Mild demineralization characterized by cortical thinning and prominence of the trabecular pattern was seen in 9 patients. Four young subjects had demineralization of long bones or spine. Two other children had slight periarticular demineralization as did 3 older patients with arthropathy. All demineralization was mild and no compression fractures were seen. Other less frequent skeletal changes are de- Fig 6. Degenerative changes at the knee with hypertrophic spurring and mild localized demineralization involving the medial femoral condyle and upper tibia. There is a linear density in the medial joint space (arrow) compatible with chondrocalcinosis. Another irregular density is seen in the lateral joint space. Same patient as in Figure Arthritis and Rheumatism, Vol. 15, No. 3 (MayJune 1972)
5 -. Table 1. Radiographic Abnormalities of Bones and Joints Related to Clinical Manifestations of Wilson's Disease E n Clinical manifestations Radiographic manifestations m B a Duration Osteo- 9 m 5 of arthritis F E Duration Peni- of knee with UJ 2 m of cillamine Articular chondroc. Case Age, symptoms therapy* Deminer- calcified malacia -3 No. sex (Yr) (yr) Hepatic$ CNSS alization bodies patellae Other changes 4 p 1 5M - 1 w - CII 2 8F F - 2? 4 9M - 2 Retarded skeletal w maturation m E 5 9M 2 z 6 12M - Benign cortical E a defect (femur) - A m N M 18M 18M 19M 19M 19M 21 F 26F 29F 31F 35M * Wrists Wrists, knee * Wrists Wrists, hands Periosteal proliferation (femur) Subchondral cysts (hip) Osteochondritis (spine): scoliosis Chondrocalcinosis (knee) Subchondral cysts (ulna) chondrocalcinosis (knee) Subchondral cysts (carpal) N ~~ ~ "Wrist, hand x-rays not available +Hepatic criteria: = absent: + = abnormal liver function tests: + + = cirrhosis: = hepatic failure SCNS (central nervous system) criteria: = absent: + = minor changes (dysarthria. mild tremor): + + = intermediate changes: = disabling rigidity with or without tremor
6 FELLER AND SCHUMACHER scribed in Table 1. Osteochondritis dissecans, Milkman pseudofractures or pathologic fractures were not encountered. Four of the children had prominent growth recovery lines of doubtful significance. Results of all serum calcium, phosphorous and alkaline phosphatase determinations were within normal range. Renal tubular dysfunction manifested by mild aminoaciduria was present in 3 children, 1 of whom had mild demineralization. DISCUSSION The calcified or ossified bodies at the wrists of 4 of our adult patients are similar to changes described by others as part of a process of bone fragmentation (6, 8-1) or osteoarthritis (6-8). These interpretations suggest that we are dealing with a predominantly noninflammatory destructive and degenerative process. This would seem to be a good possibility in light of other degenerative changes in cartilage seen elsewhere, but we were unable to conclusively visualize irregularities of articular cortex characteristic of fragmentation at the wrist. Mindelzun et al(9) reported subchondral cysts in 9 patients. Similar bone cysts in 3 of our patients were often near the loose bodies but not clearly enough related to be certain of an association. Thus, it remains conceivable that the calcified bodies might also represent accessory skeletal elements or calcifications of bursae or tendons (1 3). Whatever their explanation, their uniform presence in the adults studied and their rarity in others in this age group suggests some relationship to their Wilson s disease. Chondromalacia patellae has not been previously described in association with Wilson s disease but this was an unusually prominent aspect of the premature degenerative arthritis seen in several knees in our series. Boudin and others (11) reported a case of possible chondrocalcinosis in the shoulder and knee joints of one of their patients. Our finding of 2 cases compatible with chondrocalcinosis at the knee joint in patients with Wilson s disease suggests a similarity with the arthropathy of other metabolic diseases, such as hemochromatosis (14, 15), hyperparathyroidism ( 1 6), and ochronosis (17) in which chondrocalcinosis can also be seen. We have not yet been able to obtain cartilage biopsies or crystals from the synovial fluid to determine the type of calcium crystal in any patients with Wilson s disease. Symptoms when present seemed most consistent with mechanical or degenerative type disease. There was never morning stiffness or clinical evidence of inflammation. The effusion in the 19-year-old boy (Case 1) was noninflammatory. This patient has remained well since the joint aspiration, so whether his effusion was related to the degenerative disease seen in older patients is not yet known. Symptoms when mentioned in other series have also been predominantly mild arthralgias. Radiographic evaluation of demineralization is difficult, and, of necessity, approximate. We made no systematic attempt to measure bone density because films were taken at a variety of hospitals with varying views and technics. None of our patients developed the severe rickets or osteomalacia seen by others (4-6). The most severe changes have been described from India (5) and China (7) so that nutritional factors may have also contributed. Our findings support the previous statements that many patients with Wilson s disease have apparent skeletal demineralization, but this appears to be of minor clinical importance. In one series of 9 patients no evidence of either osteomalacia or osteoporosis (1 8) was reported. Quantitative study of bone density should be of interest. The mechanism of most osteoarticular changes in Wilson s disease is not clear. Shortterm experimental copper loading has not been shown to produce bone or joint changes (19), but copper-deficient dogs do develop skeletal malformations (2). Some patients with Wilson s disease and renal tubular dysfunction develop rickets and osteomalacia (6); however, most of our patients did not have demonstrable 264 Arthritis and Rheumatism, Vol. 15, No. 3 (May-June 1972)
7 WILSON S DISEASE renal tubular abnormalities. In 3 patients with aminoaciduria, only 1 had mild demineralization. Finby and Bearn (6) noted that, because of their tremor and spasticity, patients with Wilson s disease are more susceptible to minor injuries than normal persons. Thus, chronic trauma could be responsible for cartilage damage and bone fragmentation. However, these authors point out that osteoarthritic changes have not been seen in patients with other tremulous neurologic diseases, such as Parkinson s disease or multiple sclerosis. A recent report has implicated dyskinesias in the production of cervical spondylosis (21), and Rosenoer and Michell reported severe cervical spondylosis in 1 patient with Wilson s disease marked by tremor (8). In our series, major bone or joint changes occurred in patients with minimal neurologic involvement, while several patients with severe neurologic illness had little or no evidence of bone or joint disease. Some patients with cirrhosis of the liver have osteoporosis and pseudocysts associated with hepatic dysfunction (22), but again in our series there was no correlation between osteoarticular changes and severity of liver involvement. Harpey et a1 (23) have reported a lupus-like syndrome possibly induced by a penicillamine. We saw no evidence of any similar reactions. Although the degenerative joint involvement in Wilson s disease seems generally milder, an analogy is possible with that of hemochromatosis. The prominent metacarpal phalangeal and hip involvement seen in hemochromatosis was not seen in our patients with Wilson s disease although involvement of these joints has occasionally been described. The calcified bodies and chondromalacia patellae seen in our patients with Wilson s disease have not been characteristic of hemochromatosis. Despite these differences in sites involved, the process seems to be degenerative in both. In both diseases, the metal excess is a possible mechanism for direct or indirect production of the arthropathy. In vitro inhibition of pyrophosphatase by cupric and ferrous ions has been shown. This has been suggested as a possible mechanism allowing deposition of calcium pyrophosphate producing chondrocalcinosis in Wilson s disease and hemochromatosis (24). In our series, younger patients showed only occasional demineralization. The more severe bone and joint lesions were present only in older patients. No direct relation between total disease severity, spasticity and tremors, liver or renal disease and the production of osteoarthropathy has been established. Acute or chronic trauma was not considered a factor in any case. All our patients with major bone and joint disease had been observed at least 4 years with symptomatic Wilson s disease before penicillamine therapy was started. Since early reports of osteoarthritis and bone fragmentation were before the advent of penicillamine therapy, it is unlikely that penicillamine causes these osteoarticular changes. Whether earlier detection and treatment will prevent or minimize bone and joint damage remains to be determined. ACKNOWLEDGMENTS The authors gratefully acknowledge the assistance of Drs. Wallace Miller and John Kirkpatrick in the interpretation of the x-rays. We also thank Drs. Geraldine King, John Bryfogle, Philip Holtzapple, and Warren Grover for permission to study their patients. REFERENCES 1. Bearn AG: Wilson s disease, The Metabolic Basis of Inherited Disease. Edited by JB Stanbury, JB Wyngaarden, DS Frederickson. New York, McGraw-Hill Book Co, 1966, pp Walshe JM: Wilson s disease, the presenting symptoms. Arch Dis Child 37: , Slovis TL, Dubois RS, Rodgerson DO, et al: The varied manifestations of Wilson s disease. J Pediat 78: , Cavallino R, Grossman H: Wilson s disease presenting with rickets. Radiology 9: , Mehta RS, Shinde VA: Wilson s disease with rickets. Neurology (India) 13:67-73, 1965 Arthritis and Rheumatism, Vol. 15. No. 3 (May-June 1972) 265
8 FELLER AND SCHUMACHER 6. Finby N, Beam AG: Roentgenographic abnormalities of the skeletal system in Wilson s disease (hepatolenticular degeneration). Am J Roentgenol79:63-611, Feng YK, Sun Y, Tang HF: Calcium and phosphorous metabolism in Wilson s disease. Chinese Med J 81 :23-29, Rosenoer VM, Michell RC: Skeletal changes in Wilson s disease (hepatolenticular degeneration). Br J Radio1 32:85-89, Mindelzun R, Elkin M, Scheinberg IH, et al: Skeletal changes in Wilson s disease: A radiological study. Radiology 94: , Charbonnel A, Vercelleto P, Lemouroux P, et al: Les arthropathies de la maladie de Wilson (The arthropathies of Wilson s disease). J Med Nantes 5: , Boudin G, Pepin B, Hubault A: Les arthropathies de la maladie de Wilson (The arthropathies of Wilson s disease). SOC Med Hop Paris 114: , Sternlieb I, Scheinberg IH: The diagnosis of Wilson s disease in asymptomatic patients. JAMA 183:747-75, Kohler A: Borderlands of the Normal and Early Pathologic in Skeletal Roentgenology. Third American edition. Edited by EA Zimmer. New York, Grune and Stratton, 1968, pp 59-63, Schumacher HR: Hemochromatosis and arthritis; Arthritis Rheum 7:41-5, Dymock IW, Hamilton EBD, Laws JW, et al: Arthropathy of hemochromatosis. Ann Rheum Dis 29: , McCarty DJ, Gatter RA: Pseudogout syndrome (articular chondrocalcinosis). Bull Rheum Dis 14: , Bywaters EGL, Dorling J, Sutor J: Ochronotic densification. Ann Rheum Dis 29:563, Randall RV, Goldstein NP, Gross JB, et al: Hypercalcuria in hepatolenticular degeneration (Wilson s disease). Am J Med Sci 252:715-72, Wolff SM: Copper deposition in the rat. Arch Pathol69: , Baxter JH, Van Wyk JJ: Bone disorder associated with copper deficiency; gross morphological, roentgenological and chemical observations. Bull John Hopkins Hosp 93:l-23, Levine RA, Rosenbaum AE, Waltz JM, et al: Cervical spondylosis and dyskinesias. Neurology 2: , Balabanski L, Hadzhidekov G: Modifications osseuses dans la cirrhose du foie (Bone changes in cirrhosis of the liver). Rev Int Hepat 14:81-91, Harpey JP, Caille B, Moulias R, et al: Lupuslike syndrome induced by D-penicillamine in Wilson s disease. Lancet 1 :292, McCarty DJ, Pepe PF, Solomon SD, et al: Inhibition of human erythrocyte pyrophosphatase activity by calcium, cupric and ferrous ions. Arthritis Rheum 13:336, Arthritis and Rheumatism, Vol. 15, No. 3 (MayJune 1972)
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