T HE development of renal osteodystrophy in patients on maintenance
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1 OCTOBER, 1975 RENAL OSTEODYSTROPHY IN PATIENTS ON HEMODIALYSIS AS REFLECTED IN THE BONY PELVIS* By JOSEPH NORFRAY, M.D.,t LEONID CALENOFF, M.D., FRANCESCO DEL GRECO, M.D., and FRANK A. KRUMLOVSKY, M.D. ABSTRACT: CHICAGO, ILLINOIS Roentgen studies in a group of 131 patients on maintenance hemodialysis reveal renal osteodystrophy in 25 patients (19 per cent). In 24 patients of the latter group (98 per cent), the various manifestations of renal osteodystrophy appear in the bony pelvis. They include: osteomalacia; osteitis fibrosa; osteosclerosis; dialysis osteopenia; and extraosseous calcifications. Some of the changes, i.e., bending of bone, Looser s lines, metaphyseal fractures and dialysis osteopenia, are due, at least in part, to the weight bearing nature of the bony pelvis. These findings are rarely, if ever, seen in the digits or in other non-weight bearing bones. It is therefore proposed to evaluate the bony pelvis, together with the magnification digital roentgenogram, when a less costly and less time consuming skeletal survey is needed in hemodialized patients. T HE development of renal osteodystrophy in patients on maintenance The bony pelvis was chosen as the weight renal osteodystrophy. hemodialysis is not an unusual occurrence. bearing bone, because roentgenograms of A higher incidence has been noted in those the pelvis are readily available for every patients compared to non-hemodialized patients with similar chronic renal disease.4 9 The roentgen manifestations of renal osteodystrophy, namely, osteomalacia, osteitis fibrosa, osteosclerosis, dialysis osteopenia, and soft tissue calcifications, are well documented in the literature We have previously stressed the less costly and less time consuming value of direct magnification digital roentgenography4 in evaluating renal osteodystrophy in hemodialyzed patients. The digit, easily accessible for roentgenography, is a non-weight bearing cortical bone which readily shows changes of bone resorption. Changes due to stress, however, are not seen in the digit,7 and examination of a weight bearing bone is needed to complete an economical and rapid skeletal survey of patients suspected of having or being followed for hemodialyzed patient from urograms, cystograms, or complete skeletal surveys. The purpose of this communication is to describe the roentgen manifestations of renal osteodystrophy as they appear in the bony pelvis and to review briefly the current pathogenic concepts of skeletal changes in chronic renal insufficiency. CLINICAL MATERIAL During the period from January, 1963, through December, 1972, 131 patients with end-stage renal disease of varying etiology entered the program of hemodialysis at our institution. 8 As part of the initial evaluation, all patients had a complete skeletal survey, and most had intravenous or retrograde urography, or both, and cystography. Biopsy of the posterior iliac crest was performed in 45 patients. After the inception * From the Department of Radiology and the Section of Nephrology-Hypertension, Department of Medicine, Northwestern Memorial Hospital and the McGaw Medical Center of Northwestern University, Chicago, Illinois. Partially supported by Otho 5. A. Sprague Foundation, National Institutes of Health, Division of Research Resources, R. R. 48 and Training Grant AMO 05614, and the Kidney Research Fund of Passavant Pavilion, Northwestern Memorial Hospital. t Present Address: Department of Radiology, Henrotin Hospital, Chicago, Illinois. 352
2 VOL. 125, No. 2 Renal Osteodystrophy in Patients on Hemodialysis 353 of maintenance hemodialysis, skeletal survey roentgenography was repeated at intervals of from 6 to 12 months, or more frequently if indicated. The level of serum parathyroid hormone was determined serially in 15 patients observed during the latter part of this period. Renal osteodystrophy, verified by roentgen examination, bone biopsy, or both, developed during this period in 25 patients (19 per cent of the total). In 24 patients of the latter group (96 per cent), the manifestations of renal osteodystrophy were reflected in the bony pelvis. The specific findings are given in Table i. ROENTGEN MANIFESTATIONS Because of the weight bearing function of the pelvis and surrounding structures, the roentgen examination of the pelvis may reveal: Looser s lines, coxa vara deformities, Otto pelvis deformities, metaphyseal fractures, widening of the growth plates, and frank fractures. OSTEOMALACIA Decreased mineralization of osteoid is TABLE RENAL OSTEODYSTROPHY MAN! FESTATIONS IN PELVIC ROENTGENOGRAMS OF 24 PATIENTS Roentgen. Findings* I No. of. Patients Percentage Advanced osteomalacia Coxa vara Otto pelvis Wide growth plates Osteitis fibrosa ii 45.8 Metaphyseal fracture I 4. I Osteolysis at insertion of muscles and tendons 6 25 Wide joints 4 i6.6 Osteosclerosis Extraosseous calcifications Arterial calcifications Periarticular calcifications Dialysis osteopenia i 4. I Avascular necrosist 4 i6.6 * In most instances, there was more than i finding on each pelvic roentgenogram. t See explanations in text. the fundamental disorder underlying osteomalacia.2 5 J chronic renal failure, intestinal absorption of calcium is impaired, and there are hypocalcemia, hyperphosphatemia, and secondary hyperparathyroidism. 5 2 Resistance to the biological action of vitamin D on the intestinal mucosa comes about, with further decline of calcium absorption. Consequently, the ionized plasma pooi of calcium is even more decreased, causing additional stimulation ofparathyroid hormone secretion. It has been stated2 that the vitamin D resistance of uremia may also explain the depression of bone formation and apposition rate and the delay in the maturation of organic bone matrix. The nature of vitamin D resistance in uremia is yet to be fully elucidated. Many studies have shown that the patient with uremia requires a greater intake of vitamin D than the normal individual, and that the metabolism of vitamin D is altered in uremia. 5 2 It has been established that the loss of kidney cells interferes with the conversion of vitamin D to its active metabolite, lack of which is ultimately responsible for the defect in calcium absorption.5 The dietary intake of calcium may also be inadequate. Additionally, if the calcium content of the dialysate is below 3 mg. per cent, the plasma pool of ionized calcium can be further decreased.9 Hyperphosphatemia, the result of inability of the diseased kidney to excrete dietary phosphorus adequately, may also contribute to hypocalcemia. Osteomalacia in the adult will appear in the pelvis as decreased bone density, Looser s lines, and bending of bone. The decreased bone density can best be seen in the change in the clarity of the trabeculae in the pelvis and proximal femurs (Fig. i). There is osteoclastic osteolysis of both the secondary trabeculae which run perpendicular or oblique to major trabeculae, and also the major trabeculae, which run parallel to the lines of stress.7 The osteoblasts attempt to reform the trabeculae by producing osteoid. However, because of poor
3 354 Norfray, Caleno,ff, Del Greco and Krumlovsky OCTOBER, 1975 FIG. i. Pelvis of a 3! year old woman with chronic glomerulonephritis and roentgen signs of osteomalacia. The trabeculae in the femoral head and in the area above the acetabulum are indistinct. mineralization, excessive osteoid develops. This gives a hazy appearance to the remaining trabeculae. Looser s lines are thin, radiolucent lines perpendicular to the cortex at sites of stress, and composed of woven bone (nonlamellar bone formed by the abnormal collagen). 9 They are seen in the ischial and pubic rami, the medial margins of the femoral neck and shaft, and the lesser trochanter. 6 The poorly mineralized osteoid allows the bones surrounding the pelvis to bend, leading to development of coxa vara (Fig. 2)and Otto pelvis6 (Fig. 3; and ). FIG. 2. L vis of a 25 year old man with f a! vitamin D resistant rickets on hemodialysis after 2 unsuccessful renal transplants. Bilateral coxa vara has developed as a result of osteomalacia. Note the increase in thickness of the cortex on the medial aspect of the femoral neck, the result of realignment after bending had occurred. The bony trabeculae are covered by ground glass osteoid. Decreased bone density, Looser s lines, and bending of bone also occur in rickets; however, in this condition there are changes about the unfused epiphysis and metaphysis. Widening of the zone of provisional ossification between epiphysis and metaphysis by more than I mm. is the earliest sign of rickets. Later, cupping and fraying of the metaphysis are seen. 9 2#{176} The unfused femoral epiphysis allows one to observe these changes (Fig. 3). OSTEITIS FIBROSA Hypocalcemia, hyperphosphatemia, and vitamin D resistance associated with renal failure ultimately result in secondary hyperparathyroidism. The increase in serum parathyroid hormone level causes increased osteocytic and osteoclastic bone reabsorption, with resultant osteolysis. This occurs at the endosteal, Haversian, and subperiosteal surfaces. Reabsorptive activity is seen roentgenographically when resorption cavities are filled with woven bone or fibrous tissue (e.g., ostei tis fibrosa). Subperiosteal reabsorption is caused by osteocytes located in the lacunae and canaliculi of cortical 1 FIG. 3. Pelvis of a i6 year old boy L hereditary interstitial nephritis and unfused epiphyses. There is bilateral protrusion of the acetabulum (Otto pelvis). The zones of provisional ossification in the unfused femoral epiphyses, the cartilage of Y, and the sacroiliac joints are wide.
4 VOL. 125, No. 2 Renal Osteodystrophy in Patients on Hemodialysis 355 bone. 5 Endosteal and Haversian osteolysis is also caused by osteoclasts. Subperiosteal reabsorption is more readily identified roentgenologically because of greater osteocytic versus osteoclastic activity. Roentgenograms of the pelvis can permit identification of osteolysis in areas of increased remodelling. Metaphyseal fractures are caused by osteolysis in these areas. #{176} This explains the increased incidence of metaphyseal hip fractures in patients with renal osteodystrophy (Fig. 4). There also is increased osteolysis at sites of stress from tendon insertions and joints, such as the sacroiliac joint and the symphysis pubis (Fig. 5). Presumably, these sites of stress develop electrical potential differences at their surfaces, and osteolysis occurs at the surface with the positive charge.8 The widened joint spaces have been shown to be a combination of poorly mineralized woven bone and fibrous tissue which has replaced the lamellar bone in the subchondral region. OSTEOSCLEROSIS Osteosclerosis will appear in the pelvis as an area of increase in bone density. The disorder is thought to develop because of lii..... patient as in 1 1 3, 8 months later. There are fractures of both femoral metaphyses (arrows), resulting in slippage of the epiphyses. The fractures are a direct result of osteolysis occurring in areas of increased remodelling of bone. Fic.. Pelvis of a 50 year old woman with chronic pyelonephritis. There are signs of osteolysis in the anterior superior iliac spines, ischial tuberosities, and trochanters (open arrows), the sites of insertion of muscles. The osteolysis is identified as subperiosteal resorption. The wide symphysis pubis and sacroiliac joints (black arrows) are the result of osteolysis and replacement by woven bone and fibrous tissue (osteitis fibrosa). glomerulonephritis. 1 #{241}e increased density of the bony pelvis and femurs is characteristic of osteosclerosis, representing excessive but poorly mineralized osteoid.
5 356 Norfray, Calenoff, Del Greco and Krumlovsky OCTOBER, 1975 osteoid, there is such an excessive amount of osteoid that the bone appears dense (Fig. 6). FIG. 7. Pelvis of a 33 year old man with medullary cystic renal disease, who developed, while on hemodialysis, profuse arterial calcifications (a sign of M#{246}nckeberg s arteriosclerosis). The iliac and femoral arteries are calcified (arrows). Note clips from present working transplanted kidney. The transplant has not reversed the calcification. the direct effect of increased parathyroid hormone secretion on osteoblasts to enhance osteoid production, while there is only partial mineralization of the osteoid due to osteomalacia. 7 Thus, even though there is only partial mineralization of Pelvis of a 6 year old woman with nephrosclerosis. In addition to calcified arteries (black arrows), there are calcifications in the symphysis pubis (vertical black arrow), indicating chondrocalcinosis. Note also periarticular calcifications of the hips (white arrows). EXTRAOSSEOUS CALCIFICATIONS Extraosseous calcifications are more likely to occur when the product of the plasma calcium (in mg./ioo ml.) and plasma phosphorus (in mg./ioo ml.) is greater than 75,7.20 In renal osteodystrophy the product increases chiefly because the level of plasma phosphorus is elevated, due to inability of the diseased kidneys to excrete ingested dietary phosphorus. Hypercalcemia, secondary to tertiary ( autonomous ) hyperparathyroidism or to excessive vitamin D administration, may also contribute to an elevated calcium-phosphorus product. Extraosseous calcifications in the bony pelvis are most commonly seen as calcifications of the internal and external iliac arteries and superficial femoral arteries (Fig. 7; and 8). The calcifications are located in the tunica media, rather than in the intima as in arteriosclerosis. 4 Periarticular calcifications can also be FIG.. Tomogram of the left hip of an x8 year old girl with medullary cystic renal disease, who while on maintenance hemodialysis developed an undisplaced fracture of the femoral neck characteristic of dialysis osteopenia.
6 VOL. 125, No. 2 Renal Osteodystrophy in Patients on Hemodialysis 357 observed around the hip joints and the symphysis pubis. They present as chrondrocalcinosis or tumoral calcinosis 4 (Fig. 8). DIALYSIS OSTEOPENIA Recently a new presentation of bone disease in renal osteodystrophy has been described-dialysis osteopenia. 3 It is characterized primarily by a progressive reduction in bone mass (i.e., osteoporosis), but changes of osteomalacia and osteitis fibrosa are also present. Its roentgenographic manifestation is that of stress fractures which heal slowly, although with abundant callus (Fig. 9). In addition to the femoral neck, they can occur in the pubic and ischial rami. AVASCULAR NECROSIS Avascular necrosis is seen fairly frequently in renal transplant recipients, as well as in other patients receiving high doses of steroids. Avascular necrosis may occur in the course of maintenance hemodialysis without any demonstrable underlying etiological factor. Twenty-three patients with avascular necrosis were seen in a series of 350 patients on maintenance hemodialysis. In our series of 131 patients on hemodialysis, we did not observe avascular necrosis occurring in the femoral I FIG. 10. Pelvis of a 22 year old woman with chronic glomerulonephritis who had a transplant 2 years earlier. The transplanted kidney was rejected 2 months later following heavy doses of corticosteroids. While on hemodialysis she developed bilateral aseptic necrosis of the hips. Note the fragmentation, flattening, and sclerotic changes of the fernoral heads. head, except after renal transplantation and high doses of steroids (Fig. io). Leonid Calenoff, M.D. Department of Radiology Northwestern Memorial Hospital 303 East Superior Street Chicago, Illinois 6o6i i REFERENCES I. AGUS, Z. S., and GOLDBERG, M. Pathogenesis of uremic osteodystrophy. Radiol. Clin. North America, 1972, /0, AvioLl, L. V. Vitamin D metabolism in uremia. Kidney, 1975, 8, BAILEY, G. L., GItIFFITHS, H. J., MOCELIN, A. J., GUNDY, D. H., HAMPERS, C. L., and MERRILL, J. P. Avascular necrosis of femoral head in patients of chronic dialysis. Tr. Am. Soc. Artj,f. mt. Organs, 1972, z8, CALENOFF, L., and NORFRAY, J. Magnification digital roentgenography: method for evaluating renal osteodystrophy in hemodialyzed patients. AM. J. ROENTGENOL., RAD. THERAPY & NUCLEAR MED., 1973, ii8, DELUCA, H. F. Kidney as endocrine organ involved in calcium homeostasis. Kidney Internat., 1973, 4, EASTWOOD, J. B., BORDIER, P. J., and DE WARDENER, H. E. Some biochemical, histological, radiological and clinical features of renal osteod ystroph y. Kidney Internat., 1973, 4, EIST, J. H. Biological basis of radiologic findings in bone disease: recognition and interpretation of abnormal bone architecture. Radiol. C/in. North America, 1970, 8, FROST, H. M. The Bone Dynamics in Osteoporosis and Osteomalacia. Charles C Thomas, Publisher, Springfield, Ill., 1966, p GOLDSMITH, R. S., and JOHNSON, W. J. Role of phosphate depletion and high dialysate calcium in controlling dialytic renal osteodystrophy. Kidney Internat., 1973, 4, 154-I 6o. 10. KIRKw00D, J. R., OZONOFF, M. B., and STEIN- BACH, H. L. Epiphyseal displacement after metaph yseal fracture in renal osteod ystrophy. AM. J. ROENTGENOL., RAD. THERAPY & NUCLEAR MED., 1972, 115, ii. KREMPIEN, E. R., MEHLS, 0., and MALLUCH, H. Skeletal abnormalities in chronic renal insufficiency before and during maintenance hemodialysis. Kidney Internat., 1973, 4, MEEMA, H. E., RABINOVICH, S., MEEMA, S., LLOYD, G. J., and OREOPOULOS, D. G. Improved radiological diagnosis of azotemic osteodystrophy. Radiology, 1972, 102, 1-10.
7 358 Norfray, Calenoff, Del Greco and Krumlovsky OCTOBER, PARFITT, A. M., MASSRY, S. G., and WINFIELD, A. C. Osteopenia and fractures occurring during maintenance hemodialysis. C/in. Orthopedics, 1972,87, PARFITT, A. M. Soft tissue calcifications in uremia. A.M.A. Arch. mt. Med., 1969, /24, 15. RASMUSSEN, H., and BORDIER, P. The Physiological and Cellular Basis of Metabolic Bone Disease. Williams & Wilkins Company, Baltimore, 1974, pp. I9-5I i6. REYNOLDS, W. A., and KARO, J. J. Radiologic diagnosis of metabolic bone disease. Orthop. C/in. North America, 1972,3, RoBINSoN, R. A. Ultrastructural appearance of bone cells and bone matrix in renal osteodystrophy. A.M.A. Arch. mt. Med., 1969, /24, i8. ROGUSKA, J., SIMON, N. M., DEL GRECO, F., and KRUMLOVSKY, F. A. Ten year experience with maintenance hemodialysis for chronic uremia. Tr. Am. Soc. Artjf. mt. Organs, 1974, 20, SHAPIRO, R. Radiologic aspects of renal osteodystrophy. Radiol. Clin. North America, 1972, JO, SMITH, R. Pathophysiology and management of rickets. Orthop. C/in. North America, 1972, 3, 6oi STANBURY, S. W. Bone disease in uremia. Am. 7. Med., 1968, 44,
8 This article has been cited by: 1. Judith E. AdamsRadiology of Rickets and Osteomalacia [CrossRef] 2. J ADAMSRadiology of Rickets and Osteomalacia [CrossRef] 3. C. N. Griffin Symmetrical ilial pseudofractures: A complication of chronic renal failure. Skeletal Radiology 8:4, [CrossRef]
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