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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 11 3867-3871
Copyright © 1998 by The Endocrine Society

Original Studies

Parathyroid Detection in Secondary Hyperparathyroidism with 123I/99mTc-Sestamibi Subtraction Single Photon Emission Computed Tomography

Donald R. Neumann, Caldwell B. Esselstyn, Jr., Arelis Madera, C. Oliver Wong and Michael Lieber

Departments of Nuclear Medicine (D.R.N., C.O.W.), General Surgery (C.B.E.), and Endocrinology (A.M.), Division of Radiology (M.L.), Cleveland Clinic Foundation, Cleveland, Ohio 44195

Address all correspondence and requests for reprints to: Dr. Donald R. Neumann, Department of Nuclear Medicine, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, Ohio 44195.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
123I/99mTc-sestamibi subtraction single photon emission computed tomography (SPECT) has been proposed to detect hyperplastic parathyroid tissue, but the clinical usefulness of this technique in secondary hyperparathyroidism is uncertain. The purpose of this study was to evaluate preoperative parathyroid localization using 123I/99mTc-sestamibi subtraction SPECT in patients with renal failure and secondary hyperparathyroidism. Nineteen patients with chronic renal failure and secondary hyperparathyroidism underwent 123I/99mTc-sestamibi subtraction SPECT imaging preoperatively. None of these patients had undergone previous neck surgery. The location, weight, and histopathological results of all identified parathyroid glands were recorded. Surgery was considered successful in all patients, with resection of a total of 74 hyperplastic parathyroid glands. 123I/99mTc-sestamibi subtraction SPECT correctly identified 57 of these parathyroid glands (77% sensitivity). The mean weight among the true positive glands (n = 57) was 1031 mg (range, 45–7900 mg), and that among the false negative glands (n = 17) was 465 mg (range, 20–1800 mg). This difference between the mean weights was statistically significant (P = 0.018). There was a positive correlation between parathyroid weight and detectability with 123I/99mTc-sestamibi subtraction SPECT (Spearman correlation = 0.28; P = 0.0167). 123I/99mTc-sestamibi subtraction SPECT is able to correctly localize hyperplastic parathyroid glands in patients with renal failure and secondary hyperparathyroidism, but there is a fairly weak relationship between preoperative detection rate and anatomical parathyroid gland size.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
THE LOCALIZATION of abnormal parathyroid glands can be helpful in planning surgical strategy before neck exploration. For this purpose, several invasive and noninvasive procedures have been tried, mostly in patients with primary hyperparathyroidism, including high resolution ultrasonography, computed tomography, venous sampling, and magnetic resonance imaging (1). Radionuclide procedures have also been used for this purpose. Previously, the most commonly used scintigraphic approach has been a dual isotope procedure combining 201Tl-thallous chloride with either 99mTc-pertechnetate or 123I-labeled sodium iodide (2).

More recently, 99mTc-sestamibi has become a popular substitute for thallium-201 in scintigraphic parathyroid localization studies. As 99mTc-sestamibi was first described for this use by Coakley et al. (3), the so-called double phase method proposed by Taillefer et al. (4) has gained considerable attention. This method involves imaging at two points in time; initially at 15 min and later at 2–3 h after iv injection of 99mTc-sestamibi. A positive finding is an area of increased focal uptake that persists on late planar imaging. Sestamibi accumulation in normal thyroid tissue progressively decreases over time, allowing differentiation from abnormal parathyroid tissue. In an initial report of 23 patients by Taillefer et al. (4), 19 of 21 parathyroid adenomas were successfully identified using this double phase sestamibi technique.

The value of 99mTc-sestamibi imaging in primary hyperparathyroidism for preoperative localization of parathyroid adenomas is becoming increasingly well documented. Reports have demonstrated sensitivities ranging between 59–94% in such patients (5, 6, 7, 8, 9). Although 99mTc-sestamibi appears to be fairly sensitive for the detection of parathyroid adenomas in primary hyperparathyroidism, data accumulated to date in other hyperparathyroid conditions are limited.

The localization of hyperplastic parathyroid glands in patients with renal failure and secondary hyperparathyroidism is more technically demanding, and results with 99mTc-sestamibi have been correspondingly less impressive. O’Doherty et al. detected 32 of 60 hyperplastic parathyroid glands from a total of 15 patients with 99mTc-sestamibi imaging, compared with 28 of 60 hyperplastic glands using thallium/pertechnetate subtraction scintigraphy (10).

Although these results are comparable to localization of hyperplastic parathyroid lesions by ultrasonography or computed tomography, they are inferior to the detection of parathyroid adenomas by 99mTc-sestamibi scintigraphy (11).

The reason for the inferior results for 99mTc-sestamibi imaging for multiglandular parathyroid hyperplasia is uncertain. It may be partly related to size, with the general tendency of hyperplastic parathyroid glands to be smaller in size than parathyroid adenomas (11, 12, 13). In addition, it has been speculated that, along with parathyroid gland size, vascularity, and pathology, the concentration of several extracellular ions in chronic renal failure may alter the biokinetics of radiotracers, such as thallium and pertechnetate, and, therefore, the detectability of hyperplastic parathyroid glands (7, 14, 15, 16).

A relatively new and promising technique is subtraction scintigraphy using 123I and 99mTc-sestamibi in conjunction with SPECT tomographic imaging. In our initial experience with 15 patients with primary hyperparathyroidism, the sensitivity of the simultaneous 99mTc-sestamibi subtraction SPECT for the detection of parathyroid adenomas was 88%, which was significantly better than the 53% sensitivity of the double phase 99mTc-sestamibi technique (17). Encouraged by these results, the goal of our present study was to assess the role of 123I/99mTc-sestamibi subtraction SPECT in the detection of parathyroid glands in uremic hyperparathyroidism.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Nineteen consecutive patients with chronic renal failure and secondary hyperparathyroidism who were scheduled for parathyroid surgery were included in this study. Only those patients without a history of previous neck surgery were enrolled in this study. The group included 13 women and 6 men, with a mean age of 43 yr (range, 27–61 yr), a mean serum calcium level of 10.3 mg/dL (range, 8.4–12.5 mg/dL), and a mean serum intact PTH level of 1017 pg/mL (range, 99–3975 pg/mL; normal range, 10–60 pg/mL).

Ten minutes after the sestamibi injection, simultaneous dual isotope SPECT of the neck and chest was acquired using two photopeaks: one with a 15% energy window centered over the 140-keV photopeak of 99mTc, and the other with a 10% energy window centered over the 159-keV photopeak of 123I. Measurements performed in our laboratory indicate that with the energy windows used in this study, the expected cross-talk contribution from a 99mTc source in the 159-keV energy window is less than 4.5% of the counts detected in the 140-keV energy window.

A single 60-s anterior image of the neck was acquired before sestamibi injection using the same two energy windows as during the dual isotope SPECT acquisition. These two digital images were used to determine the cross-over factor of 123I into the 140-keV (99mTc) energy window.

A large field of view, double headed SPECT camera system (BIAD, Trionix Research Laboratory, Twinsburg, OH) was used for image acquisition. Projection images were acquired in a 128 x 128 matrix, with a pixel width of 5.28 mm, providing an axial field of view of 338 mm. For the SPECT portions of the study, projections were acquired for 30 s at each of 45 angular positions, sampling a 360° noncircular orbit every 4°.

After applying correction of estimated 123I cross-talk into the paired 140-keV projection images using the measured cross-over factor, tomographic reconstruction was performed for each of the two energy window datasets using a Hamming filter (cut-off frequency of 0.74 cycles/cm) before convolution-backprojection.

Two experienced nuclear medicine physicians interpreted all scintigraphic studies in this series, unaware of the results of any other localization studies. The SPECT studies were all interpreted prospectively before surgery. Digital tomographic images were displayed on a computer workstation (SPARC station 10, Sun Microsystems, Mountain View, CA) with the observers having individual control of the window display settings.

Bilateral surgical neck exploration was performed on each patient by an experienced parathyroid surgeon. In all patients, total parathyroidectomy combined with heterotopic placement of parathyroid autografts into the sternocleidomastoid muscle was performed. An attempt was made during surgery to identify all parathyroid glands. The appearance, size, and location of every parathyroid gland were documented. Histopathological examination and weights of all resected surgical specimens was obtained. Postoperative serum calcium levels were determined in each patient. Surgical success in each patient was defined by the identification of at least three parathyroid glands and a significant reduction in serum calcium levels postoperatively.

Interactive software was used for normalization and subtraction of the 123I data from the corresponding tomographic early 99mTc-sestamibi tomograms, and data were displayed for interpretation. During an interpretation session, each observer displayed a registered pair (99mTc-sestamibi, 123I) of images in any of three available planes (transverse, sagittal, or coronal). The software automatically determines a preliminary normalization factor based on the inverse of the ratio of the maximum pixel value in the 123I tomogram to the value of the corresponding pixel in the 99mTc-sestamibi image. Each pixel in the 123I tomogram is multiplied by this normalization factor before subtraction from the corresponding 99mTc-sestamibi tomogram to yield the resultant image. In an interactive fashion, the operator is able to adjust this normalization factor and choose other paired tomograms until subjectively satisfactorily subtraction images are obtained. Using a normalization factor determined in this manner, the observers then evaluated the remainder of the dual isotope tomographic study, which was displayed on the computer workstation.

For the dual isotope subtraction SPECT, a positive finding was defined as a focus of residual sestamibi activity after normalization and subtraction of the corresponding tomographic 123I image data. Preliminary interpretation of the location and number of abnormalities identified was rendered by each observer independently. After completion of interpretations, the two sets of interpretations were compared, and final interpretations were derived by consensus in case of observer disagreement.

Sensitivity was defined as the ratio of true positive results to the sum of true positives plus false negatives. Specificity was defined as the ratio of true negative results to the sum of true negatives plus false positives.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Surgical findings

All 19 patients underwent successful bilateral surgical neck exploration for hyperparathyroidism. Four hyperplastic parathyroid glands were found in orthotopic sites in each of 16 patients. In 1 patient, 3 orthotopic hyperplastic glands and 1 hyperplastic gland in the right carotid sheath were found. The preoperative imaging results aided in the detection of this heterotopic parathyroid gland at surgery. In 1 patient, 3 orthotopic hyperplastic glands and 1 histologically normal parathyroid gland were found. In the remaining patient, 3 orthotopic hyperplastic parathyroid glands were found. The mean weight of the 74 hyperplastic parathyroid glands was 901 mg (range, 20–7900 mg).

Postoperatively, serum calcium levels fell in all patients to a mean value of 8.2 mg/dL. This represented a significant change from preoperative serum calcium levels, which had a mean value of 10.3 mg/dL (P < 0.005, by paired Student’s t test).

Imaging results

Compared with the surgical results, the simultaneous 123I/99mTc-sestamibi subtraction SPECT correctly localized 57 of 74 hyperplastic parathyroid glands, including the 1 undescended parathyroid gland, resulting in a sensitivity of 77%. No false positive findings were identified in this series, and the 1 normal parathyroid gland was associated with negative imaging findings. In one patient, multiple colloid thyroid nodules were found, which were associated with negative imaging findings. Using the SE reported by Rao and Scott (18) to account for intrapatient correlation among parathyroid glands, the 95% confidence interval for the true sensitivity of simultaneous 123I/99mTc-sestamibi subtraction SPECT to detect hyperplastic parathyroid glands in secondary hyperparathyroidism is 66.6%, 85.4%.

The mean weight among the true positive hyperplastic parathyroid glands (n = 57) was 1031 mg (range, 45–7900 mg). Among the false negative hyperplastic parathyroid glands (n = 17), the mean weight was 465 mg (range, 20–1800 mg). This difference between the mean weights was statistically significant (P = 0.018, by Wilcoxon test).

There was a positive correlation between hyperplastic parathyroid gland weight and the likelihood of a true positive finding on the 123I/99mTc-sestamibi subtraction SPECT (Spearman correlation = 0.28; P = 0.0167).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Secondary hyperparathyroidism is a well known complication of chronic renal failure. As a result from hypocalcemia, an increase in the serum phosphorus level and reduced synthesis of 1,25-dihydroxycholecalciferol (19), hyperplasia of the parathyroid glands is stimulated, with subsequent elevation of PTH levels. Conservative measures aim to prevent the development of renal osteodystrophy, calcium deposition, and hypercalcemia associated with secondary hyperparathyroidism (20).

Most patients with secondary hyperparathyroidism may be controlled medically by phosphate binders, calcium supplements and appropriately concentrated dialysates, and synthetic calcitriol (21). Despite aggressive medical management, however, up to nearly 30% of chronic renal failure patients with secondary hyperparathyroidism will not be adequately controlled (19, 22), with indications for surgical intervention including hypercalcemia metastatic calcification, intractable pruritis, muscle weakness, and late complications of renal osteodystrophy, such as bone pain and pathological fractures (23, 24, 25, 26, 27, 28).

The goal of surgery is to resect an adequate mass of parathyroid tissue to lower PTH levels, yet leave enough functioning parathyroid tissue to avoid permanent hypocalcemia. Total parathyroidectomy with autotransplantation of fragments of parathyroid tissue into skeletal muscle has rapidly become an established surgical procedure. The hopes are to avoid the need for surgical neck reexploration, prevent osteomalacia associated with PTH deficiency, and retain the prospect of regaining normal parathyroid function in the event of successful renal transplantation (29, 30, 31).

The benefit of preoperative imaging in secondary hyperparathyroidism, however, has yet to be established. Although the reported sensitivities for the detection of parathyroid adenomas in primary hyperparathyroidism using 123I/99mTc-sestamibi subtraction imaging have ranged from 70–100% (5, 17, 32, 33, 34, 35, 36, 37, 38), a completely different clinicopathological setting is associated with secondary hyperparathyroidism. In this disease, as opposed to primary hyperparathyroidism, it is more common for all parathyroid glands to become hyperplastically involved. Furthermore, as with the detection of parathyroid adenomas, the reported success rates for the scintigraphic detection of hyperplastic parathyroid glands have also been variable, with a majority of reported sensitivities below 50% (15).

The reason for the generally inferior results for scintigraphic detection for hyperplastic parathyroid glands is uncertain. In our present study, however, there was a positive correlation between hyperplastic parathyroid lesion size and delectability by simultaneous 123I/99mTc-sestamibi subtraction SPECT, with larger hyperplastic parathyroid glands more likely to be detected (Spearman correlation = 0.28; P = 0.0167). It should be emphasized, however, that this is a fairly weak correlation, and parathyroid gland weight alone does not adequately account for the likelihood of detection by 123I/99mTc-sestamibi subtraction SPECT.

These findings support the contention, suggested by others (15), that a combination of other variables may be implicated as factors in hyperplastic parathyroid gland detection by scintigraphic techniques using 99mTc-sestamibi. Some factors that might be considered include parathyroid gland shape, location, uptake biokinetics, vascularity and altered cellularity, as well as parathyroid gland size.

The double phase technique with use of 99mTc-sestamibi as a single agent was first reported in 1992 (4), with a sensitivity of 90% for the detection of parathyroid adenomas. The single agent, double phase 99mTc-sestamibi technique takes advantage of the slower release of sestamibi by abnormal parathyroid tissue than by normal thyroid tissue. Since that time, other studies using the double phase sestamibi technique have reported sensitivities ranging from 59–94% for parathyroid adenoma detection (5, 6, 7, 8, 9). There have been a few reports on the use of this technique for hyperplastic parathyroid gland detection. A survey of the literature over the last few years reveals that the reported success of double phase 99mTc-sestamibi for the detection of hyperplastic parathyroid glands has been fairly low, with most sensitivities below 50% (16, 39, 40, 41).

In our present series of patients, the sensitivity of 123I/99mTc-sestamibi subtraction SPECT for the detection of hyperplastic parathyroid lesions in secondary hyperparathyroidism is 77%. Our results are comparable to those of other recent studies using the dual isotope approach in secondary hyperparathyroidism, each reporting sensitivities of about 82% (13, 42). Combined, these results suggest an improvement of the dual isotope approach over the use of the double phase 99mTc-sestamibi technique for the detection of hyperplastic parathyroid glands.

Although we are unaware of any reports that directly compare the double phase sestamibi technique to the 123I/99mTc-sestamibi subtraction method in patients with secondary hyperparathyroidism, the results of our present study are consistent with our previous experience in patients with primary hyperparathyroidism. We previously compared double phase sestamibi SPECT and simultaneous 123I/99mTc-sestamibi subtraction SPECT in a series of patients with primary hyperparathyroidism. The sensitivity for the detection of parathyroid adenomas was 88% for 123I/99mTc-sestamibi subtraction SPECT and 53% for double phase 99mTc-sestamibi SPECT (17). The difference in sensitivity for the detection of hyperplastic parathyroid glands with simultaneous 123I/99mTc-sestamibi subtraction SPECT in the present study compared to reported sensitivities for the double phase sestamibi technique is similar to that reported in our previous study.

Although the results of our present study are encouraging, they must be considered preliminary because of the relatively small size of our patient series. In addition, our present study included only those patients who had not undergone neck surgery previously. The rate of recurrent hyperparathyroidism after total parathyroidectomy with autotransplantation has been reported to be as high as 19% of cases (43). Although usually caused by hyperplasia of the parathyroid autotransplant in these patients, recurrent postoperative hyperparathyroidism may be a source of considerable clinical frustration due to the possibility of supernumerary parathyroid glands. In addition, supernumerary parathyroid glands are relatively common and can act as a source of confusion over the site of PTH hypersecretion when recurrent hyperparathyroidism occurs (44). It has been suggested that a search for supernumerary parathyroid glands should be carried out in every hyperparathyroid patient, particularly in those with diffuse hyperplasia associated with chronic renal disease (45).

The need for preoperative parathyroid imaging in cases of persistent or recurrent postoperative secondary hyperparathyroidism is more established, partly because of the increased morbidity and reduced surgical success rates encountered. Not only is it technically more difficult to perform subsequent operations because of the presence of scar tissue and obscuration of normal tissue planes, but residual abnormal parathyroid tissue is more likely to be present in aberrant or ectopic locations (46). Conceivably, a thyroid marker such as 123I may not be as beneficial in these patients to distinguish thyroid from parathyroid uptake of 99mTc-sestamibi, although further investigations are required to demonstrate this contention.



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  		Figure 1. 30-yr-old man with secondary hyperparathyroidism. A, Coronal 99mTc-sestamibi tomogram of neck and chest; B, Corresponding control 123I tomogram; C, After subtraction of B and A, resultant image shows four areas of residual 99mTc-sestamibi subtraction activity in the neck (arrows). At surgery, sour hyperplastic parathyroid glands weighing 400 (right upper), 200 (right lower), 600 (left upper), and 430 mg (left lower) were resected from the neck.

 


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  		Figure 2. Distribution of hyperplastic parathyroid gland weights and detection by 123I 99mTc-sestamibi substraction SPECT. TP, true positive. FN, false negative.

 
Received March 25, 1998.

Revised July 21, 1998.

Accepted July 28, 1998.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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