Erosive Spondyloarthropathy in Primary Hyperparathyroidism Without Renal Failure Joshua Barzilay, MD, and Arturo R. Rolla, MD • A patient with erosive spondyloarthropathy (ESA) and primary hyperparathyroidism is described. In the past, ESA has been described exclusively in patients with chronic renal failure (CRF) and has been attributed to crystal deposition, amyloidosis, severe secondary hyperparathyroidism, or other abnormalities of chronic renal failure. This patient with normal renal function suggests that secondary hyperparathyroidism plays the major pathogenetic role in ESA in patients with renal failure. © 1992 by the National Kidney Foundation, Inc. INDEX WORDS: Hypercalcemia; hyperparathyroidism; spondyloarthropathy; arthritis; renal failure.
E
ROSIVE spondyloarthropathy (ESA) is a radiographic entity characterized by subchondral bone resorption, cavitation of vertebral bodies, and destruction of vertebral end-plates and disk spaces. 1. 16 Clinically, it is most often silent, but may present with rapidly progressive cervical or lumbar pain. Rarely, a more destructive form of this process leads to spinal cord compression. 2,lO To date, ESA has been reported exclusively in patients with chronic renal failure (CRF), most of whom have been on long-term dialysis. In a number of series, it is estimated to occur in 15% to 30% of dialysis patients. The pathogenesis has been variously attributed to crystal deposition,7,13,17 amyloidosis,2,4,9,lO,12,13,15 secondary hyperparathyroidism, 3,6,11 or other abnormalities related to CRF. 18 No clear consensus has been reached regarding this point. In the present report, we describe a patient with an early form of ESA and severe primary hyperparathyroidism who did not have renal failure or any of its associated sequelae. To the best of our knowledge, this is the first such reported case in primary hyperparathyroidism. From this case, it may be inferred that secondary hyperparathyroidism is the main pathogenetic factor for ESA in patients with renal failure. CASE REPORT A 59-year-old woman was admitted to the hospital because of increasing low back pain of I year's duration, and the recent
From the Departments of Medicine. New England Deaconess Hospital. and Harvard Medical School. Boston. MA, Received December 11. 1991; accepted in revised form F ebruary 4. 1992. No reprints available. © 1992 by the National Kidney Foundation, Inc. 0272-6386/92/2001-0013$3.00;0 90
onset of left-sided sciatic pain. The pain worsened over a 6week period to the point that it was difficult for her to walk. She felt otherwise well, and her weight and appetite were stable. On physical examination, she was an obese woman in distress even when lying in bed. Her vital signs were normal and her temperature was continuously normal. There was no lower back tenderness to percussion. The left ankle and knee jerks were present, but reduced when compared with the right. She had a positive straight-leg raising test at 40° on the left side. It was negative on the right. She was known to have elevated calcium levels, 2.74 to 2.99 mmolfL (11 to 12 mgjdL) for the preceding 2'12 years, with normal serum levels of phosphorus, proteins, and alkaline phosphatase. The patient had not been taking calcium or vitamin D preparations. She was found to have asymptomatic hyperglycemia 2 years before admission and was placed on a diet and g1yburide 10 mgjd. Hypertension was found I year before admission, and was treated with propranolol 40 mg twice daily and cardiazem 60 mg four times a day. Because of a past history of seizure disorder, she was taking carbamazepine 300 mgjd. There was no history of gout, kidney stones, or CRF. Anteroposterior and lateral lumbosacral spine x-rays showed a loss of the anterior-superior cortex of L5 and an indistinct inferior aspect of L3 and L4 (Fig I). The L4-L5 disk space was slightly narrowed and eroded. Computed tomography (CT) scanning of the same area (Fig 2) showed lytic changes throughout the body of L4. The erosive lesions were surrounded by zones of sclerosis. In addition, bilateral erosive changes of the facet joints of L3-L4 and L4-L5 were seen. There was moderate, diffuse disk bulging at L3-L4 and significant stenosis of the spinal canal at that level. X-rays of the hand and wrists demonstrated mild subperiosteal resorption. Ultrasound of the neck showed a 3- X 2.7-ern echogenic mass lateral to, but separate from, the right lobe of the thyroid. Localization was confirmed by a thallium-technetium substraction scan. A bone scan showed no abnormality, and there was no increased uptake over the lumbar spine. Laboratory tests showed serum calcium 3.09 mmollL (12.4 mgjdL), phosphorus 0.74 mmol/L (2.3 mgjdL), urea nitrogen 8.93 mmol/L urea (25 mgjdL), creatinine 110 mmollL (1.2 mgj dL), and uric acid 367 mmol/L (6.2 mgjdL). AIkaline phosphatase was elevated at 186 IV/L (normal, < I06 IVIL). Erythrocyte sedimentation rate (ESR) was 26 mm. Carboxyl-terminal parathyroid hormone (PTH) by radioimmunoassay (RIA) was 9,550 pg/mL (normal, 50 to 330 pg/mL), and amino-terminal PTH 95 pg/ mL (normal, 8 to 24 pg/mL), confirming the diagnosis of hy-
American Journal of Kidney Diseases, Vol XX, No 1 (July), 1992: pp 90-93
SPONDYLOARTHROPATHY AND HYPERPARATHYROIDISM
Fig 1. Lateral x-ray showing loss of the anterior-superior cortex of L5 and an indistinct inferior border of L4.
perparathyroidism. 1-25,di-OH vitamin D was 85 pmol/L (34 pg/mL) (normal, 40 to 160 pmol/ L). Owing to the previously unknown association of primary hyperparathyroidism with ESA and uncertainty of diagnosis, a CT-guided lumbar disk space aspiration to rule out infection was performed. The Gram stain and bacterial. mycobacterial, and fungal cultures were all negative. The patient underwent neck exploration. A 3.6- X 3.2- X 1.8cm adenoma, somewhat hemorrhagic, was removed from the posterior wall of the right parathyroid gland. Following surgery, the patient complained of tingling in her fingers, and there was a transient decrease in calcium to 2 mmol/L (8.0 mgjdL) and phosphorus to 0.65 mmo\jL (2.0 mgjdL), which required oral calcium replacement for a period of 3 weeks. The patient continued to have back and left pain, and 2 weeks later underwent a decompression laminectomy of L4-L5. Vertebral fragments showed focal increase of both osteoblastic and osteoclastic activity, with peritrabecular fibrosis consistent with hyperparathyroidism. There were no crystal deposition or amyloid in the specimen. Eighteen months following surgery, the patient is normocalcemic and symptom-free.
91
sence of renal failure suggests that ESA in association with CRF is most probably due to secondary hyperparathyroidism. Two recent studies support this conclusion. In the first, McCarthy et alii reported two dialysis patients with ESA who underwent subtotal parathyroidectomies and who attained rapid relief of symptoms and no further progression of radiographic findings. A third patient with ESA who refused surgery had progression of findings. In the second report, Alcalay et al 6 demonstrated the presence ofESA in two patients with CRF before the onset of dialysis, an observation consistent with an early role for secondary hyperparathyroidism. In addition to these reports, secondary hyperparathyroidism has been reported in association with ESA in many instances, and the incidence of parathyroidectomies performed in these patients is higher than that in the general dialysis population. 16 Moreover, erosive osteoarthropathy in peripheral joints due to subchondral bone resorption has also been associated with secondary hyperparathyroidism. 19 Primary hyperparathyroidism infrequently leads to articular complaints, but roentgenologic findings in the axial skeleton (acromioclavicular, sternoclavicular, sacroiliac and temporomandibular joints, and symphysis pubis) are common. 20•21 These findings are usually secondary to juxta-articular and/or subchondral bone resorp-
DISCUSSION
The demonstration in this case that ESA can occur in primary hyperparathyroidism in the ab-
Fig 2. CT scan of the body of L4 showing numerous lytic lesions.
92
BARZILAY AND ROLLA
tion, calcium pyrophosphate crystal deposition, and capsular and ligamentous laxity, which may be a direct effect of high PTH levels. 22 In the spine, partial disruption of cartilage plates and softening of underlying bone results in subluxation and disk protrusion. 23 In secondary hyperparathyroidism, this process in the spine results in Schmorl's nodes-the protrusion of disk material into the vertebral body through defective cartilaginous end-plates. 21 Recently, Sundarum et al 5 have drawn attention to ESA of the anterior corners of the vertebral bodies in up to 25% of dialysis patients and suggested that it too may be a vertebral manifestation of secondary hyperparathyroidism. With regard to other possible pathogenetic mechanisms, Kuntz et al,l in the original report ofESA, found hydroxyapatite crystals in the disk matrix of one patient. They postulated that these crystals played a pathogenetic role in the joint destruction by activating collagenases and proteases. However, this finding was not confirmed by others. Moreover, crystal-induced arthritis in CRF patients, as a consequence of secondary hyperparathyroidism, has been reported. 19,24 It is therefore more likely that in ESA the crystals are a consequence, rather than a cause, of the bony erosions. Another suggested cause of ESA is the deposition of amyloid. B2-microglobulin-related amyloid protein is recognized a,s a cause of dialysis arthropathy in large and medium joints,25-27 and a number of studies of ESA have shown deposits within disk material and peridisk ligaments. 2,4,9,10,12.13,15.28 However, a causal relation-
ship was never established in these cases. It is also known that amyloid deposits can be found in clinically unaffected joints of dialysis patients,27 making it likely that amyloid deposition in damaged vertebrae and disks is a secondary phenomenon, rather than a primary causative factor. Moreover, in many of the reported cases of amyloid in ESA, severe secondary hyperparathyroidism was present. It should be recognized that ESA occurs almost exclusively in the presence of CRF and that hyperparathyroidism alone (with the exception of this case) does not cause this syndrome. It follows that factors associated with renal failure most probably act synergistically with hyperparathyroidism or potentiate its effect to allow for the development of this finding. One additional point regarding the present case bears mentioning. The radiologic appearance of ESA simulates that of an infectious process, and in many cases ofESA, infection was the primary consideration. One noninvasive means of differentiating between these two conditions would be the use of bone scintigraphy. In the present case, as in other cases of ESA,6,24,29 no active uptake was demonstrated, an unusual finding were the lesion infectious. This most probably reflects the purely resorptive nature of this lesion. Further studies of bone scintigraphy in ESA will be needed to confirm the discriminatory value of this test. ACKNOWLEDGMENT The patient was referred to the authors by Michael K. Rees, MD.
REFERENCES 1. Kuntz D, Naveau B, Bardin T, et al: Destructive spondyloarthropathy in hemodialyzed patients: A new syndrome. Arthritis Rheum 27:369-375, 1984 2. Sebert J-L, Fardellone P, Marie A, et al: Destructive spondyloarthropathy in hemodialyzed patients: A possible role of amyloidosis. Arthritis Rheum 29:301-303, 1986 (letter) 3. Kaplan P, Resnick D, Murphey M, et al: Destructive noninfectious spondyloarthropathy in hemodialysis patients: A report of four cases. Radiology 162:241-244, 1987 4. Varga J, Fenves A: Destructive noninfectious spondyloarthropathy in hemodialysis patients. Radiology 164:584585, 1987 (letter) 5. Sundaram M, Seelig R, Pohl D: Vertebral erosions in patients undergoing maintenance hemodialysis for chronic renal failure. AJR 149:323-327 1987 6. Alcalay M, Goupy M-C, Azais J, et al: Hemodialysis is not essential for the development of destructive spondyloar-
thropathy in patients with chronic renal failure. Arthritis Rheum 30:1182-1186, 1987 7. Menard H-A, Langevin S, Levesque R-Y: Destructive spondyloarthropathy in short term chronic ambulatory peritoneal dialysis and hemodialysis. Rheumatology 15:644-647, 1988 8. Raftos S, Dalinka M, Schiebler M, et al: Spondyloarthropathy of the cervical spine in long-term hemodialysis. Radiology 166:201-204, 1988 9. Naidich J, Mossey R, McHeffey-Atkinson B, et al: Spondyloarthropathy from long-term hemodialysis. Radiology 167:761-764, 1988 10. Patel B, Mistry C, Kumar N, et al: Magnetic resonance imaging in non-infective destructive spondyloarthropathy. Br J RadioI61:511-514, 1988 11. McCarthy J, Dahlberg P, Kriegshauser J, et al: Erosive spondy1oarthropathy in long term dialysis patients: Relation-
SPONDYLOARTHROPATHY AND HYPERPARATHYROIDISM
ship to severe hyperparathyroidism. Mayo Clin Proc 63:446527, 1988 12. Kerr R, Bjorkengren A, Bielecki D, et al: Destructive spondyloarthropathy in hemodialysis patients: Report offour cases and prospective study. Skeletal Radiol 17: 176-180, 1988 13. Hurst N, Van den Berg R, Disney A, et al: Dialysis related arthropathy: A survey of95 patients receiving chronic hemodialysis with special reference to B2 microglobulin related amyloidosis. Ann Rheum Dis 48:409-420, 1989 14. Cruz A, Gonzalez T, Balsa A, et al: Destructive spondyloarthropathy in long term CAPD and hemodialysis. J Rheumatol 16: 1169-1170, 1989 (letter) 15. Orzincolo C, Bedani P-L, Scutellari P, et al: Destructive spondyloarthropathy and radiographic follow up in hemodialysis patients. Skeletal Radiol 19:483-487, 1990 16. Bindi P, Chanard J: Destructive spondyloarthropathy in dialysis patients: An overview. Nephron 55: 104-109, 1990 17. Benoist M, Bloch-Michel H, Kahn M, et al: Les manifestations vertebrales de la chondrocalcinose articularie. Nouv Presse Med 9:1827-1830, 1980 18. Cary N, Sethi D, Brown E, et al: Dialysis arthropathy: Amyloid or iron? Br Med J 293:1392-1394, 1986 19. Rubin L, Fam A, Rubenstein J, et al: Erosive azotemic osteoarthropathy. Arthritis Rheum 27:1086-1094,1984 20. Zvaifler N, Reefe W, Black R: Articular manifestations
93 in primary hyperparathyroidism. Arthritis Rheum 5:237-249, 1962 21. Resnick D, Niwayama G: Subchondral resorption of bone in renal osteodystrophy. Radiology 118:315-321, 1976 22. Lipson R, Williams L: The "connective tissue disorder" of hyperparthyroidism. Arthritis Rheum II: 198-203, 1968 23. Bywaters E, Dixon A, Scott J: Joint lesions of hyperparathyroidism. Ann Rheum Dis 22: 171-187, 1963 24. Schumacher H, Miller J, Ludivico C, et al: Erosive arthritis associated with appatite crystal deposition. Arthritis Rheum 24:31-37, 1981 25. Huaux J, Noel H, Malghem J, et al: Erosive azotemic osteoarthropathy: Possible role of amyloidosis. Arthritis Rheum 28:1075-1076, 1985 (letter) 26. Bardin T, Kuntz D, Zingraff J, et al: Synovial amyloidosis in patients undergoing long-term hemodialysis. Arthritis Rheum 28:1052-1058, 1985 27. Bardin T, Zingraff J, Shirahama T, et al: Hemodialysisassociated amyloidosis and beta-2 microglobulin: Clinical and immunohistochemical study. Am J Med 83:419-424, 1987 28. Deramond H, Sebert J, Rosat P, et al: Destructive spondyloarthropathy in chronic haemodialysis patients: Current data and radiological aspects. J Neuroradiol 14:27-38, 1987 29. Sundaram M: Renal osteodystrophy. Skeletal Radiol 18:415-426, 1989
E
ROSIVE spondyloarthropathy (ESA) is a radiographic entity characterized by subchondral bone resorption, cavitation of vertebral bodies, and destruction of vertebral end-plates and disk spaces. 1. 16 Clinically, it is most often silent, but may present with rapidly progressive cervical or lumbar pain. Rarely, a more destructive form of this process leads to spinal cord compression. 2,lO To date, ESA has been reported exclusively in patients with chronic renal failure (CRF), most of whom have been on long-term dialysis. In a number of series, it is estimated to occur in 15% to 30% of dialysis patients. The pathogenesis has been variously attributed to crystal deposition,7,13,17 amyloidosis,2,4,9,lO,12,13,15 secondary hyperparathyroidism, 3,6,11 or other abnormalities related to CRF. 18 No clear consensus has been reached regarding this point. In the present report, we describe a patient with an early form of ESA and severe primary hyperparathyroidism who did not have renal failure or any of its associated sequelae. To the best of our knowledge, this is the first such reported case in primary hyperparathyroidism. From this case, it may be inferred that secondary hyperparathyroidism is the main pathogenetic factor for ESA in patients with renal failure. CASE REPORT A 59-year-old woman was admitted to the hospital because of increasing low back pain of I year's duration, and the recent
From the Departments of Medicine. New England Deaconess Hospital. and Harvard Medical School. Boston. MA, Received December 11. 1991; accepted in revised form F ebruary 4. 1992. No reprints available. © 1992 by the National Kidney Foundation, Inc. 0272-6386/92/2001-0013$3.00;0 90
onset of left-sided sciatic pain. The pain worsened over a 6week period to the point that it was difficult for her to walk. She felt otherwise well, and her weight and appetite were stable. On physical examination, she was an obese woman in distress even when lying in bed. Her vital signs were normal and her temperature was continuously normal. There was no lower back tenderness to percussion. The left ankle and knee jerks were present, but reduced when compared with the right. She had a positive straight-leg raising test at 40° on the left side. It was negative on the right. She was known to have elevated calcium levels, 2.74 to 2.99 mmolfL (11 to 12 mgjdL) for the preceding 2'12 years, with normal serum levels of phosphorus, proteins, and alkaline phosphatase. The patient had not been taking calcium or vitamin D preparations. She was found to have asymptomatic hyperglycemia 2 years before admission and was placed on a diet and g1yburide 10 mgjd. Hypertension was found I year before admission, and was treated with propranolol 40 mg twice daily and cardiazem 60 mg four times a day. Because of a past history of seizure disorder, she was taking carbamazepine 300 mgjd. There was no history of gout, kidney stones, or CRF. Anteroposterior and lateral lumbosacral spine x-rays showed a loss of the anterior-superior cortex of L5 and an indistinct inferior aspect of L3 and L4 (Fig I). The L4-L5 disk space was slightly narrowed and eroded. Computed tomography (CT) scanning of the same area (Fig 2) showed lytic changes throughout the body of L4. The erosive lesions were surrounded by zones of sclerosis. In addition, bilateral erosive changes of the facet joints of L3-L4 and L4-L5 were seen. There was moderate, diffuse disk bulging at L3-L4 and significant stenosis of the spinal canal at that level. X-rays of the hand and wrists demonstrated mild subperiosteal resorption. Ultrasound of the neck showed a 3- X 2.7-ern echogenic mass lateral to, but separate from, the right lobe of the thyroid. Localization was confirmed by a thallium-technetium substraction scan. A bone scan showed no abnormality, and there was no increased uptake over the lumbar spine. Laboratory tests showed serum calcium 3.09 mmollL (12.4 mgjdL), phosphorus 0.74 mmol/L (2.3 mgjdL), urea nitrogen 8.93 mmol/L urea (25 mgjdL), creatinine 110 mmollL (1.2 mgj dL), and uric acid 367 mmol/L (6.2 mgjdL). AIkaline phosphatase was elevated at 186 IV/L (normal, < I06 IVIL). Erythrocyte sedimentation rate (ESR) was 26 mm. Carboxyl-terminal parathyroid hormone (PTH) by radioimmunoassay (RIA) was 9,550 pg/mL (normal, 50 to 330 pg/mL), and amino-terminal PTH 95 pg/ mL (normal, 8 to 24 pg/mL), confirming the diagnosis of hy-
American Journal of Kidney Diseases, Vol XX, No 1 (July), 1992: pp 90-93
SPONDYLOARTHROPATHY AND HYPERPARATHYROIDISM
Fig 1. Lateral x-ray showing loss of the anterior-superior cortex of L5 and an indistinct inferior border of L4.
perparathyroidism. 1-25,di-OH vitamin D was 85 pmol/L (34 pg/mL) (normal, 40 to 160 pmol/ L). Owing to the previously unknown association of primary hyperparathyroidism with ESA and uncertainty of diagnosis, a CT-guided lumbar disk space aspiration to rule out infection was performed. The Gram stain and bacterial. mycobacterial, and fungal cultures were all negative. The patient underwent neck exploration. A 3.6- X 3.2- X 1.8cm adenoma, somewhat hemorrhagic, was removed from the posterior wall of the right parathyroid gland. Following surgery, the patient complained of tingling in her fingers, and there was a transient decrease in calcium to 2 mmol/L (8.0 mgjdL) and phosphorus to 0.65 mmo\jL (2.0 mgjdL), which required oral calcium replacement for a period of 3 weeks. The patient continued to have back and left pain, and 2 weeks later underwent a decompression laminectomy of L4-L5. Vertebral fragments showed focal increase of both osteoblastic and osteoclastic activity, with peritrabecular fibrosis consistent with hyperparathyroidism. There were no crystal deposition or amyloid in the specimen. Eighteen months following surgery, the patient is normocalcemic and symptom-free.
91
sence of renal failure suggests that ESA in association with CRF is most probably due to secondary hyperparathyroidism. Two recent studies support this conclusion. In the first, McCarthy et alii reported two dialysis patients with ESA who underwent subtotal parathyroidectomies and who attained rapid relief of symptoms and no further progression of radiographic findings. A third patient with ESA who refused surgery had progression of findings. In the second report, Alcalay et al 6 demonstrated the presence ofESA in two patients with CRF before the onset of dialysis, an observation consistent with an early role for secondary hyperparathyroidism. In addition to these reports, secondary hyperparathyroidism has been reported in association with ESA in many instances, and the incidence of parathyroidectomies performed in these patients is higher than that in the general dialysis population. 16 Moreover, erosive osteoarthropathy in peripheral joints due to subchondral bone resorption has also been associated with secondary hyperparathyroidism. 19 Primary hyperparathyroidism infrequently leads to articular complaints, but roentgenologic findings in the axial skeleton (acromioclavicular, sternoclavicular, sacroiliac and temporomandibular joints, and symphysis pubis) are common. 20•21 These findings are usually secondary to juxta-articular and/or subchondral bone resorp-
DISCUSSION
The demonstration in this case that ESA can occur in primary hyperparathyroidism in the ab-
Fig 2. CT scan of the body of L4 showing numerous lytic lesions.
92
BARZILAY AND ROLLA
tion, calcium pyrophosphate crystal deposition, and capsular and ligamentous laxity, which may be a direct effect of high PTH levels. 22 In the spine, partial disruption of cartilage plates and softening of underlying bone results in subluxation and disk protrusion. 23 In secondary hyperparathyroidism, this process in the spine results in Schmorl's nodes-the protrusion of disk material into the vertebral body through defective cartilaginous end-plates. 21 Recently, Sundarum et al 5 have drawn attention to ESA of the anterior corners of the vertebral bodies in up to 25% of dialysis patients and suggested that it too may be a vertebral manifestation of secondary hyperparathyroidism. With regard to other possible pathogenetic mechanisms, Kuntz et al,l in the original report ofESA, found hydroxyapatite crystals in the disk matrix of one patient. They postulated that these crystals played a pathogenetic role in the joint destruction by activating collagenases and proteases. However, this finding was not confirmed by others. Moreover, crystal-induced arthritis in CRF patients, as a consequence of secondary hyperparathyroidism, has been reported. 19,24 It is therefore more likely that in ESA the crystals are a consequence, rather than a cause, of the bony erosions. Another suggested cause of ESA is the deposition of amyloid. B2-microglobulin-related amyloid protein is recognized a,s a cause of dialysis arthropathy in large and medium joints,25-27 and a number of studies of ESA have shown deposits within disk material and peridisk ligaments. 2,4,9,10,12.13,15.28 However, a causal relation-
ship was never established in these cases. It is also known that amyloid deposits can be found in clinically unaffected joints of dialysis patients,27 making it likely that amyloid deposition in damaged vertebrae and disks is a secondary phenomenon, rather than a primary causative factor. Moreover, in many of the reported cases of amyloid in ESA, severe secondary hyperparathyroidism was present. It should be recognized that ESA occurs almost exclusively in the presence of CRF and that hyperparathyroidism alone (with the exception of this case) does not cause this syndrome. It follows that factors associated with renal failure most probably act synergistically with hyperparathyroidism or potentiate its effect to allow for the development of this finding. One additional point regarding the present case bears mentioning. The radiologic appearance of ESA simulates that of an infectious process, and in many cases ofESA, infection was the primary consideration. One noninvasive means of differentiating between these two conditions would be the use of bone scintigraphy. In the present case, as in other cases of ESA,6,24,29 no active uptake was demonstrated, an unusual finding were the lesion infectious. This most probably reflects the purely resorptive nature of this lesion. Further studies of bone scintigraphy in ESA will be needed to confirm the discriminatory value of this test. ACKNOWLEDGMENT The patient was referred to the authors by Michael K. Rees, MD.
REFERENCES 1. Kuntz D, Naveau B, Bardin T, et al: Destructive spondyloarthropathy in hemodialyzed patients: A new syndrome. Arthritis Rheum 27:369-375, 1984 2. Sebert J-L, Fardellone P, Marie A, et al: Destructive spondyloarthropathy in hemodialyzed patients: A possible role of amyloidosis. Arthritis Rheum 29:301-303, 1986 (letter) 3. Kaplan P, Resnick D, Murphey M, et al: Destructive noninfectious spondyloarthropathy in hemodialysis patients: A report of four cases. Radiology 162:241-244, 1987 4. Varga J, Fenves A: Destructive noninfectious spondyloarthropathy in hemodialysis patients. Radiology 164:584585, 1987 (letter) 5. Sundaram M, Seelig R, Pohl D: Vertebral erosions in patients undergoing maintenance hemodialysis for chronic renal failure. AJR 149:323-327 1987 6. Alcalay M, Goupy M-C, Azais J, et al: Hemodialysis is not essential for the development of destructive spondyloar-
thropathy in patients with chronic renal failure. Arthritis Rheum 30:1182-1186, 1987 7. Menard H-A, Langevin S, Levesque R-Y: Destructive spondyloarthropathy in short term chronic ambulatory peritoneal dialysis and hemodialysis. Rheumatology 15:644-647, 1988 8. Raftos S, Dalinka M, Schiebler M, et al: Spondyloarthropathy of the cervical spine in long-term hemodialysis. Radiology 166:201-204, 1988 9. Naidich J, Mossey R, McHeffey-Atkinson B, et al: Spondyloarthropathy from long-term hemodialysis. Radiology 167:761-764, 1988 10. Patel B, Mistry C, Kumar N, et al: Magnetic resonance imaging in non-infective destructive spondyloarthropathy. Br J RadioI61:511-514, 1988 11. McCarthy J, Dahlberg P, Kriegshauser J, et al: Erosive spondy1oarthropathy in long term dialysis patients: Relation-
SPONDYLOARTHROPATHY AND HYPERPARATHYROIDISM
ship to severe hyperparathyroidism. Mayo Clin Proc 63:446527, 1988 12. Kerr R, Bjorkengren A, Bielecki D, et al: Destructive spondyloarthropathy in hemodialysis patients: Report offour cases and prospective study. Skeletal Radiol 17: 176-180, 1988 13. Hurst N, Van den Berg R, Disney A, et al: Dialysis related arthropathy: A survey of95 patients receiving chronic hemodialysis with special reference to B2 microglobulin related amyloidosis. Ann Rheum Dis 48:409-420, 1989 14. Cruz A, Gonzalez T, Balsa A, et al: Destructive spondyloarthropathy in long term CAPD and hemodialysis. J Rheumatol 16: 1169-1170, 1989 (letter) 15. Orzincolo C, Bedani P-L, Scutellari P, et al: Destructive spondyloarthropathy and radiographic follow up in hemodialysis patients. Skeletal Radiol 19:483-487, 1990 16. Bindi P, Chanard J: Destructive spondyloarthropathy in dialysis patients: An overview. Nephron 55: 104-109, 1990 17. Benoist M, Bloch-Michel H, Kahn M, et al: Les manifestations vertebrales de la chondrocalcinose articularie. Nouv Presse Med 9:1827-1830, 1980 18. Cary N, Sethi D, Brown E, et al: Dialysis arthropathy: Amyloid or iron? Br Med J 293:1392-1394, 1986 19. Rubin L, Fam A, Rubenstein J, et al: Erosive azotemic osteoarthropathy. Arthritis Rheum 27:1086-1094,1984 20. Zvaifler N, Reefe W, Black R: Articular manifestations
93 in primary hyperparathyroidism. Arthritis Rheum 5:237-249, 1962 21. Resnick D, Niwayama G: Subchondral resorption of bone in renal osteodystrophy. Radiology 118:315-321, 1976 22. Lipson R, Williams L: The "connective tissue disorder" of hyperparthyroidism. Arthritis Rheum II: 198-203, 1968 23. Bywaters E, Dixon A, Scott J: Joint lesions of hyperparathyroidism. Ann Rheum Dis 22: 171-187, 1963 24. Schumacher H, Miller J, Ludivico C, et al: Erosive arthritis associated with appatite crystal deposition. Arthritis Rheum 24:31-37, 1981 25. Huaux J, Noel H, Malghem J, et al: Erosive azotemic osteoarthropathy: Possible role of amyloidosis. Arthritis Rheum 28:1075-1076, 1985 (letter) 26. Bardin T, Kuntz D, Zingraff J, et al: Synovial amyloidosis in patients undergoing long-term hemodialysis. Arthritis Rheum 28:1052-1058, 1985 27. Bardin T, Zingraff J, Shirahama T, et al: Hemodialysisassociated amyloidosis and beta-2 microglobulin: Clinical and immunohistochemical study. Am J Med 83:419-424, 1987 28. Deramond H, Sebert J, Rosat P, et al: Destructive spondyloarthropathy in chronic haemodialysis patients: Current data and radiological aspects. J Neuroradiol 14:27-38, 1987 29. Sundaram M: Renal osteodystrophy. Skeletal Radiol 18:415-426, 1989
