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Bone scan findings in patients with chronic renal failure having symptoms related to bone: correlation with parathyroid hormone levels
Bone Scan Findings in Patients With Chronic Renal Failure Having Symptoms Related to Bone: Correlation With Parathyroid Hormone Levels A. Aktas and N. Elahi
C
HRONIC renal failure leads to changes in bone metabolism known as renal osteodystrophy. The mechanisms involved in the development of renal osteodystrophy are complex and various factors influence the final expression of this disorder. Renal osteodystrophy may express itself in the form of osteomalacia, osteitis fibrosa, osteoporosis, osteosclerosis, or adynamic bone disease. None of these is specific for chronic renal failure. Metabolic bone disease encompasses a number of disorders that typically show involvement of the whole skeleton. Commonly encountered pathologies leading to metabolic bone disease include primary hyperparathyroidism, osteomalacia, and renal osteodystrophy. Many types of metabolic bone disease share similar scan appearances. Increased rates of bone turnover explain increased radiophosphate uptake on conventional bone scintigraphy. This increase may be diffuse or focal as in the case of pseudofractures. The most abnormal scans often occur in renal osteodystrophy and reflect the combined effects of osteomalacia and hyperparathyroidism. This study was planned to investigate the usefulness of bone scintigraphy in symptomatic patients with chronic renal failure and to correlate the findings with parathyroid hormone (PTH) levels. PATIENTS AND METHODS Thirty-seven patients (21 male, 16 female; age range: 14 to 70 with a mean age of 40) with chronic renal failure, 11 with normal and 26 with increased PTH levels, referred for the evaluation of generalized or local bone pain, were included for this study. Whole body images were acquired 3 hours after the intravenous (IV) administration of 740 MBq of Tc-99m MDP by using a single-headed camera (Siemens-Diacam) with a low energy all-purpose colimator. For the interpretation of the bone scans, the metabolic index suggested by Fogelman et al was used.1 Scintigraphic features of metabolic bone disease forming the basis of the Fogelman score include increased activity in the axial skeleton, increased activity in the long bones, increased activity in periarticular areas, prominent calvarium and mandible, beading of the costochondral junctions, increased activity in the sternum: (“tie sternum”), and faint or absent kidney images. Each feature was scored as follows: 0 ⫽ normal, 1 abnormal, 2 ⫽ markedly abnormal. The sum of the scores is defined as the metabolic index (Fogelman score) for that patient. Bone scans were also evaluated for the presence of soft tissue activity and the presence of focally increased activity, sug-
Table 1. Abnormalities Detected in Bone Scans of Patients With Elevated PTH Levels Number of Patients
Type of Abnormality
Increased activity in periarticular areas Generalized increased activity Prominent calvarium and mandible Beading of the costochondral junctions Increased activity in the sternum Visceral calcification Focally increased activity
13 11 3 6 4 3 3
gesting pseudofractures or Brown tumor. Parathormone levels were studied before scintigraphy by radioimmunoassay methods.
RESULTS
Among patients with elevated PTH levels, only two had normal bone scintigraphy. The remaining 24 (92%) had an abnormal metabolic index. Metabolic index of patients with elevated PTH levels were as follows: 1 ⫽ 13 patients, ⱖ2 ⫽ 11 patients. The correlation between elevated PTH levels and the presence of abnormal bone scan findings was high. Bone scan features of patients with elevated PTH levels are summarized in Table 1. Figures 1 and 2 show the bone scan appearance of patients with elevated PTH levels. Of 11 patients with normal PTH levels, 6 had normal scintigraphy, 2 had generalized increased activity, 2 had increased activity at one particular joint, and 1 had multiple periarticular increased activity. The percentage of abnormal bone scan findings was 45% in patients with normal PTH levels. Overall, pathologic bone scan findings suggesting metabolic bone disease have been observed in 78% of referred patients. Periarticular increased activity was the most frequent finding, with generalized increased activity being the second.
From the Department of Nuclear Medicine, Baskent University School of Medicine, Ankara, Turkey. Address reprint requests to Ayse Aktas, Baskent University School of Medicine, 10.sk No: 45, Bahcelievler 06490, AnkaraTurkiye. E-mail: melekk@Baskent 1.h.baskent.edu.tr.
© 1999 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
0041-1345/99/$–see front matter PII S0041-1345(99)00807-6
Transplantation Proceedings, 31, 3309–3311 (1999)
3309
3310
Fig 1. Bone scan of a patient with chronic renal failure having increased PTH levels. There is bilateral diffuse increased activity in the lung parenchyma and multiple focally increased activity, suggesting pseudofractures and bilateral increased activity of the patella.
DISCUSSION
The most common bone scan appearance in renal osteodystrophy is of generalized increased uptake throughout the skeleton with some or all of the typical metabolic features. This produces increased contrast between bone and soft tissues giving rise to the appearance of a super scan in more severe cases. In the case of diffuse involvement of the skeleton, the recognition of increased tracer uptake is subjective. Quantitative measurements improve the detec-
AKTAS AND ELAHI
Fig 2. Bone scan of another patient demonstrating prominent calvarium and mandible, generalized increased activity, and increased activity of the sternum.
tion of metabolic bone disease over visual evaluation of the studies.2 The 24-hour total body retention of radiophosphate is increased in patients with metabolic bone disease. In cases with increased bone turnover, this was due to skeletal uptake and not soft tissue. Several studies have shown that bone scintigraphy has a higher sensitivity than radiography to detect changes compatible with renal osteodystrophy. By using the semiquantitative scoring system with the incorporation of some of metabolic features, 83% to 93% of patients were found to have abnormalities on bone scintigraphy. Radiologic abnormalities related to hyperparathyroidism was seen in 33% to 46% subjects.3–5 By
BONE SCAN FINDINGS
using the metabolic index described by Fogelman, 29 patients with renal osteodystrophy had increased metabolic index. In another study, 24 patients with renal bone disease had increased metabolic index, whereas only 14 patients showed radiologic abnormalities compatible with renal osteodystrophy or hyperparathyroidism.6 Advanced hyperparathyroidism is often associated with uptake in the lungs and stomach, reflecting metastatic calcification. Although the frequency of pulmonary calcification in individuals with long-standing renal failure is 60% to 70% at autopsy, increased radiophosphate in the lungs is unusual.4,7 This is explained by the low affinity of the amorphous or microcrystalline compound seen in calcifications of uremic patients for the radiophosphate. In renal bone disease, focally increased activity can be observed in cases of pseudofracture, brown tumors, or ectopic calcifications. Periarticular increased uptake is a frequent finding. It may be due to crystal deposition, dialysis arthropathy,8 or bone resorption. In osteomalacia, it is probably related to bone changes caused by the disease itself. In conclusion, 78% of symptomatic patients with chronic renal failure had abnormal bone scans, with the sensitivity of bone scintigraphy increasing up to 92% in cases with
3311
elevated PTH levels. Periarticular increased uptake was the most frequently observed scintigraphic abnormality. Since bone scintigraphy is a safe and easily performed procedure which is more sensitive than radiography reflecting the general status of skeletal metabolism, it can be used in the routine diagnostic work-up of symptomatic patients with elevated PTH levels.
REFERENCES 1. Fogelman I, Citrin DL, Turner JG, et al: Eur J Nucl Med 4:287, 1979 2. Fogelman I, Bessent RG, Turner JG, et al: J Nucl Med 19:270, 1978 3. Sy WM, Mittal AK: Br J Radiol 48:878, 1975 4. DeGraaf P, Schicht IM, Pauwels EKJ, et al: J Nucl Med 19:1289, 1978 5. Olgaard K, Heerfordt J, Madsen S, et al: Nephron 17:325, 1976 6. Fogelman I, Carr D: Clin Radiol 31:321, 1980 7. Corger JD, Hammond WS, Alfrey AC, et al: Ann Intern Med 83:330, 1975 8. Grateau G, Zingraff J, Fauchet M, et al: J Kidney Dis 11:231, 1988
C
HRONIC renal failure leads to changes in bone metabolism known as renal osteodystrophy. The mechanisms involved in the development of renal osteodystrophy are complex and various factors influence the final expression of this disorder. Renal osteodystrophy may express itself in the form of osteomalacia, osteitis fibrosa, osteoporosis, osteosclerosis, or adynamic bone disease. None of these is specific for chronic renal failure. Metabolic bone disease encompasses a number of disorders that typically show involvement of the whole skeleton. Commonly encountered pathologies leading to metabolic bone disease include primary hyperparathyroidism, osteomalacia, and renal osteodystrophy. Many types of metabolic bone disease share similar scan appearances. Increased rates of bone turnover explain increased radiophosphate uptake on conventional bone scintigraphy. This increase may be diffuse or focal as in the case of pseudofractures. The most abnormal scans often occur in renal osteodystrophy and reflect the combined effects of osteomalacia and hyperparathyroidism. This study was planned to investigate the usefulness of bone scintigraphy in symptomatic patients with chronic renal failure and to correlate the findings with parathyroid hormone (PTH) levels. PATIENTS AND METHODS Thirty-seven patients (21 male, 16 female; age range: 14 to 70 with a mean age of 40) with chronic renal failure, 11 with normal and 26 with increased PTH levels, referred for the evaluation of generalized or local bone pain, were included for this study. Whole body images were acquired 3 hours after the intravenous (IV) administration of 740 MBq of Tc-99m MDP by using a single-headed camera (Siemens-Diacam) with a low energy all-purpose colimator. For the interpretation of the bone scans, the metabolic index suggested by Fogelman et al was used.1 Scintigraphic features of metabolic bone disease forming the basis of the Fogelman score include increased activity in the axial skeleton, increased activity in the long bones, increased activity in periarticular areas, prominent calvarium and mandible, beading of the costochondral junctions, increased activity in the sternum: (“tie sternum”), and faint or absent kidney images. Each feature was scored as follows: 0 ⫽ normal, 1 abnormal, 2 ⫽ markedly abnormal. The sum of the scores is defined as the metabolic index (Fogelman score) for that patient. Bone scans were also evaluated for the presence of soft tissue activity and the presence of focally increased activity, sug-
Table 1. Abnormalities Detected in Bone Scans of Patients With Elevated PTH Levels Number of Patients
Type of Abnormality
Increased activity in periarticular areas Generalized increased activity Prominent calvarium and mandible Beading of the costochondral junctions Increased activity in the sternum Visceral calcification Focally increased activity
13 11 3 6 4 3 3
gesting pseudofractures or Brown tumor. Parathormone levels were studied before scintigraphy by radioimmunoassay methods.
RESULTS
Among patients with elevated PTH levels, only two had normal bone scintigraphy. The remaining 24 (92%) had an abnormal metabolic index. Metabolic index of patients with elevated PTH levels were as follows: 1 ⫽ 13 patients, ⱖ2 ⫽ 11 patients. The correlation between elevated PTH levels and the presence of abnormal bone scan findings was high. Bone scan features of patients with elevated PTH levels are summarized in Table 1. Figures 1 and 2 show the bone scan appearance of patients with elevated PTH levels. Of 11 patients with normal PTH levels, 6 had normal scintigraphy, 2 had generalized increased activity, 2 had increased activity at one particular joint, and 1 had multiple periarticular increased activity. The percentage of abnormal bone scan findings was 45% in patients with normal PTH levels. Overall, pathologic bone scan findings suggesting metabolic bone disease have been observed in 78% of referred patients. Periarticular increased activity was the most frequent finding, with generalized increased activity being the second.
From the Department of Nuclear Medicine, Baskent University School of Medicine, Ankara, Turkey. Address reprint requests to Ayse Aktas, Baskent University School of Medicine, 10.sk No: 45, Bahcelievler 06490, AnkaraTurkiye. E-mail: melekk@Baskent 1.h.baskent.edu.tr.
© 1999 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
0041-1345/99/$–see front matter PII S0041-1345(99)00807-6
Transplantation Proceedings, 31, 3309–3311 (1999)
3309
3310
Fig 1. Bone scan of a patient with chronic renal failure having increased PTH levels. There is bilateral diffuse increased activity in the lung parenchyma and multiple focally increased activity, suggesting pseudofractures and bilateral increased activity of the patella.
DISCUSSION
The most common bone scan appearance in renal osteodystrophy is of generalized increased uptake throughout the skeleton with some or all of the typical metabolic features. This produces increased contrast between bone and soft tissues giving rise to the appearance of a super scan in more severe cases. In the case of diffuse involvement of the skeleton, the recognition of increased tracer uptake is subjective. Quantitative measurements improve the detec-
AKTAS AND ELAHI
Fig 2. Bone scan of another patient demonstrating prominent calvarium and mandible, generalized increased activity, and increased activity of the sternum.
tion of metabolic bone disease over visual evaluation of the studies.2 The 24-hour total body retention of radiophosphate is increased in patients with metabolic bone disease. In cases with increased bone turnover, this was due to skeletal uptake and not soft tissue. Several studies have shown that bone scintigraphy has a higher sensitivity than radiography to detect changes compatible with renal osteodystrophy. By using the semiquantitative scoring system with the incorporation of some of metabolic features, 83% to 93% of patients were found to have abnormalities on bone scintigraphy. Radiologic abnormalities related to hyperparathyroidism was seen in 33% to 46% subjects.3–5 By
BONE SCAN FINDINGS
using the metabolic index described by Fogelman, 29 patients with renal osteodystrophy had increased metabolic index. In another study, 24 patients with renal bone disease had increased metabolic index, whereas only 14 patients showed radiologic abnormalities compatible with renal osteodystrophy or hyperparathyroidism.6 Advanced hyperparathyroidism is often associated with uptake in the lungs and stomach, reflecting metastatic calcification. Although the frequency of pulmonary calcification in individuals with long-standing renal failure is 60% to 70% at autopsy, increased radiophosphate in the lungs is unusual.4,7 This is explained by the low affinity of the amorphous or microcrystalline compound seen in calcifications of uremic patients for the radiophosphate. In renal bone disease, focally increased activity can be observed in cases of pseudofracture, brown tumors, or ectopic calcifications. Periarticular increased uptake is a frequent finding. It may be due to crystal deposition, dialysis arthropathy,8 or bone resorption. In osteomalacia, it is probably related to bone changes caused by the disease itself. In conclusion, 78% of symptomatic patients with chronic renal failure had abnormal bone scans, with the sensitivity of bone scintigraphy increasing up to 92% in cases with
3311
elevated PTH levels. Periarticular increased uptake was the most frequently observed scintigraphic abnormality. Since bone scintigraphy is a safe and easily performed procedure which is more sensitive than radiography reflecting the general status of skeletal metabolism, it can be used in the routine diagnostic work-up of symptomatic patients with elevated PTH levels.
REFERENCES 1. Fogelman I, Citrin DL, Turner JG, et al: Eur J Nucl Med 4:287, 1979 2. Fogelman I, Bessent RG, Turner JG, et al: J Nucl Med 19:270, 1978 3. Sy WM, Mittal AK: Br J Radiol 48:878, 1975 4. DeGraaf P, Schicht IM, Pauwels EKJ, et al: J Nucl Med 19:1289, 1978 5. Olgaard K, Heerfordt J, Madsen S, et al: Nephron 17:325, 1976 6. Fogelman I, Carr D: Clin Radiol 31:321, 1980 7. Corger JD, Hammond WS, Alfrey AC, et al: Ann Intern Med 83:330, 1975 8. Grateau G, Zingraff J, Fauchet M, et al: J Kidney Dis 11:231, 1988