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(Radiology. 2001;218:783-790.)
© RSNA, 2001

Head and Neck Imaging

Comparison between MR Imaging and 99mTc MIBI Scintigraphy in the Evaluation of Recurrent or Persistent Hyperparathyroidism1

Michael B. Gotway, MD, Gautham P. Reddy, MD, MPH, W. Richard Webb, MD, Eugene T. Morita, MD, Orlo H. Clark, MD and Charles B. Higgins, MD

1 From the Thoracic Imaging Section, Department of Radiology, University of California, San Francisco General Hospital, 1001 Potrero Ave, Rm 1X 55A, Box 1325, San Francisco, CA 94110 (M.B.G.); the Department of Radiology, University of California, San Francisco (M.B.G., G.P.R., W.R.W., E.T.M., C.B.H.); and the Department of Surgery, University of California, Mt Zion Medical Center, San Francisco (O.H.C.). Received April 28, 2000; revision requested June 17; revision received July 14; accepted July 25. Address correspondence to M.B.G. (e-mail: michael.gotway@radiology.ucsf.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To compare the sensitivity and positive predictive value of magnetic resonance (MR) imaging and technetium 99m 2-methoxyisobutyl-isonitrile (MIBI) scintigraphy for the detection of hyperfunctioning parathyroid tissue when used alone and in combination in a large patient population with recurrent or persistent hyperparathyroidism (HPT).

MATERIALS AND METHODS: In 98 consecutive patients with biochemically proved recurrent or persistent HPT after surgery, MR imaging and 99mTc MIBI study findings were retrospectively reviewed and compared with surgical and histopathologic findings. The sensitivity and positive predictive value of MR imaging and 99mTc MIBI scintigraphy were compared with each other and in combination.

RESULTS: In these patients, 130 abnormal parathyroid glands were identified at surgery. The sensitivity and positive predictive value of MR imaging were 82% (95% CI: 75%, 89%) and 89%, respectively; those for 99mTc MIBI scintigraphy were 85% (95% CI: 79%, 91%) and 89%. No significant difference was found between MR imaging and 99mTc MIBI scintigraphy for sensitivity (P = .7). The sensitivity and positive predictive value for the detection of abnormal parathyroid tissue on a per-gland basis increased to 94% (95% CI: 90%, 98%) and 98%, respectively, when only one of the two tests was required to be positive.

CONCLUSION: MR imaging and 99mTc MIBI scintigraphy have similarly good sensitivity and positive predictive value for the detection of hyperfunctioning parathyroid tissue in patients after surgery. The combination of the two tests provided a substantial increase in sensitivity and positive predictive value.

Index terms: Parathyroid, hyperparathyroidism, 274.531 • Parathyroid, MR, 274.121411, 274.121415 • Parathyroid, neoplasms, 274.363 • Parathyroid, radionuclide studies, 274.12175 • Parathyroid, SPECT, 274.12162


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Hyperparathyroidism (HPT) is a common clinical condition that affects nearly one in 700 patients (1,2). Ninety-five percent of patients may be cured with cervical exploration without preoperative imaging studies for localization of abnormal glands (1,3–6). Because the success rate in patients undergoing repeat cervical exploration after an initial failed surgery may be as low as 60% (7,8), preoperative localization studies are often used in patients with recurrent or persistent HPT. These studies include ultrasonography (US), computed tomography (CT), technetium 99m pertechnetate–thallium 201 scintigraphy, magnetic resonance (MR) imaging, selective venous sampling, selective arteriography, and, more recently, 99mTc 2-methoxyisobutyl-isonitrile (MIBI) scintigraphy. Use of preoperative imaging provides a directed surgical approach, the success rate of subsequent surgery is improved, and surgical morbidity is decreased when such techniques are used (1,3,6,9–11).

Preoperative imaging studies have been compared in several investigations (7,9,12–22), and tailored approaches for preoperative imaging have been suggested. MR imaging has consistently been shown to be useful in the preoperative assessment of recurrent or persistent HPT (2,7,10,12,19,23–34). Recently, 99mTc MIBI scintigraphy has been shown to have a high sensitivity and specificity for the detection of abnormal glands in patients with primary and/or recurrent or persistent HPT (12,15,17,35–39). Both MR imaging and 99mTc MIBI scintigraphy have demonstrated improvements in sensitivity for the detection of abnormal parathyroid glands in recent data compared with that in earlier investigations (2,23,27,29–31,33,40). Results of a prior investigation (7) that included a smaller number of patients examined with MR imaging and 99mTc MIBI scintigraphy suggested that the combination of the two techniques provided successful preoperative localization of abnormal parathyroid tissue in more than 90% of cases. Other investigators (3,16,17,19,24–26,31) have also observed that the combination of these two studies provides an optimal approach for the preoperative localization of hyperfunctioning parathyroid tissue.

The purpose of the current study was to compare the sensitivity and positive predictive value of MR imaging and 99mTc MIBI scintigraphy for the detection of hyperfunctioning parathyroid tissue when used alone and in combination in a large patient population with recurrent or persistent HPT.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Patients
One hundred nineteen patients with initial failed cervical neck explorations and biochemical evidence of recurrent or persistent HPT were examined with MR imaging and 99mTc MIBI scintigraphy between June 1992 and December 1999 at our institutions. All patients had hypercalcemia and elevated levels of parathyroid hormone. All patients had at least one prior failed neck exploration for HPT. Both MR imaging and 99mTc MIBI scintigraphy were performed during the course of the clinical investigation of recurrent or persistent HPT. For the purposes of this study, MR images were retrospectively reviewed and compared with the reports of the 99mTc MIBI scintigraphic scans. In 14 patients, 99mTc MIBI scintigraphic reports were not available, and in another seven patients, surgical and/or histopathologic confirmation of abnormal parathyroid tissue was lacking. Surgical and histopathologic confirmation of the abnormal parathyroid glands were obtained in the remaining 98 patients (32 male and 66 female patients; age range, 11–89 years; mean age, 54.2 years) that constituted the study group.

One hundred two MR imaging and 99mTc MIBI scintigraphic examinations were performed in the 98 patients. Four patients each underwent examination on two separate occasions; in all four patients, the two examinations occurred at least 1 year apart. MR imaging and 99mTc MIBI scintigraphy were performed within 12 months after surgical reexploration in all patients (mean, 38 days; range, 0–365 days). MR imaging and 99mTc MIBI scintigraphy were performed within 6 months of each other (mean, 12.6 days; range, 0–172 days).

MR Imaging
Spin-echo images of the neck were obtained with a 1.5-T magnet (Signa; GE Medical Systems, Milwaukee, Wis) in all patients by using an anterior neck coil. Images of the chest were obtained by using a torso coil. Three- to 5-mm-thick transverse images were obtained through the neck from the hyoid bone to the cervicothoracic junction by using T1-weighted sequences (700/20 [repetition time msec/echo time msec]) and fast spin-echo T2-weighted sequences (3,000/85–102). A 20% intersection gap was used. For neck imaging, the matrix size was 256 x 192, and the field of view was 16 cm.

Peripheral or electrocardiographically gated spin-echo T1-weighted images (R-R interval/20) with a 5-mm section thickness were acquired through the chest from the cervicothoracic junction through the base of the heart. The field of view for the thoracic images was 32 cm, with a matrix size of 256 x 192. T1-weighted (700/20) transverse images through the neck with 5-mm section thickness and a 20% intersection gap were also obtained after the intravenous administration of 0.1 mmol of gadolinium chelate (Magnevist, Berlex Imaging, Wayne, NJ; or Omniscan, Nycomed Amersham, Princeton, NJ) per kilogram of body weight. Contrast material was not administered in two patients: one because of patient refusal and the other because of inability to obtain intravenous access. Fat-saturation techniques were used in 70% of cases for the imaging sequences used after the administration of contrast material.

99mTc MIBI Scintigraphy
Three minutes after the intravenous administration of 10–25 mCi (370–925 MBq) of MIBI (Cardiolite; Dupont-Merck Pharmaceutical, Billerica, Mass), 16 images of the neck were obtained in the anterior projection by using a pinhole collimator and a mobile camera (Technicare Mobile Camera; GE Medical Systems). Each image was obtained during 1 minute. Images of the neck from the right and left anterior oblique views were obtained for 5 minutes per view by using a 128 x 128 matrix. Subsequently, by using a high-resolution collimator and 128 x 128 matrix, additional 5-minute images of the neck in the anterior projection and of the chest in anterior, posterior, and right and left oblique projections were obtained after placement of a marker on the sternal notch, surgical scar, and cricoid cartilage. Planar imaging of the neck and chest was also performed with a pinhole collimator at 2 hours after injection of the tracer. When activity within the neck was inseparable from thyroid gland activity, 10 mCi (370 MBq) of 99mTc pertechnetate was administered to localize the thyroid gland.

Single photon emission CT (SPECT) (Sopha DSX camera; Sopha Medical Systems, Columbia, Md) was occasionally used for potential chest lesions or in cases in which no potentially abnormal parathyroid tissue was found in the neck with routine imaging. SPECT imaging was performed by using an elliptic orbit and a 64 x 64 digital matrix. SPECT images were acquired for 30 seconds at 64 stops. A single experienced observer (E.T.M.) without knowledge of the surgical findings or the MR imaging results interpreted the 99mTc MIBI scintigraphic studies. The diagnosis of an abnormal parathyroid gland was made when a dominant focus of 99mTc MIBI scintigraphic activity was observed on early and delayed images.

Image Analysis
MR images were reviewed retrospectively by four radiologists. In any given case, three of the four radiologists (M.B.G., G.P.R., W.R.W., and C.B.H.) participated in the review. In all cases, two radiologists (M.B.G., C.B.H.) participated in the review. MR images were interpreted by means of consensus of three radiologists (M.B.G. and C.B.H., and either G.P.R. or W.R.W.). MR images were interpreted without knowledge of either the result of the 99mTc MIBI scintigraphic study or the findings at surgery. The interpreters were aware of the clinical context in which the imaging was performed. MR images were evaluated for the presence of abnormal parathyroid glands, with primary emphasis placed on the typical locations (adjacent to the posterior aspects of the thyroid gland) and known ectopic locations (thymus, intrathyroidal, parapharyngeal, tracheoesophageal groove, and anterior mediastinum) of such glands. The signal intensity and presence or lack of contrast enhancement of suspect nodular structures, particularly those in any of these locations, were noted. These results were recorded and compared with the findings at surgery and the findings of the 99mTc MIBI scintigraphic studies.

Correlation of Surgical and Histopathologic Findings
The number of abnormal glands identified at surgery and the location of these glands were recorded. The same surgeon (O.H.C.), using the information from both MR images and 99mTc MIBI scintigraphic scans, performed surgery in all patients. The locations of normally situated abnormal parathyroid glands were specified at surgery in relation to the thyroid gland (ie, right or left, related to the upper or lower poles of the thyroid gland). The location of ectopic glands was specified in relation to adjacent anatomic structures (ie, within the thymus, intrathyroidal). With either MR imaging or 99mTc MIBI scintigraphy, no attempt was made to distinguish parathyroid adenoma from parathyroid gland hyperplasia, although hyperplasia was considered likely if more than one abnormal parathyroid gland was detected. These results were used to determine the number of true-positive, false-positive, and false-negative MR images and 99mTc MIBI scintigraphic scans.

The total number and relative percentages of adenomas, hyperplastic glands, and parathyroid carcinomas was recorded by one author (M.B.G.) who reviewed the pathology reports. In multiple instances, the histopathologic analyses of the resected glands were read only as hypercellular. In such cases, the pathologist was unable to distinguish adenoma from hyperplasia because biopsy samples of the remaining parathyroid glands were not provided, or a rim of normocellular parathyroid tissue surrounding the hypercellular glandular tissue, characteristic of adenoma, was not present. Therefore, a direct comparison of the performance of MR imaging and 99mTc MIBI scintigraphy in the detection of adenomas versus hyperplastic glands was not possible. Instead, the individual true-positive rates for the detection of adenomas, hyperplastic glands, hypercellular glands, and carcinomas for both MR imaging and 99mTc MIBI scintigraphy were noted and compared.

Although correlation of the imaging findings and performance with resected gland weight and size was desired, it was not feasible because many of the histopathologic specimens were fragmented or such information was otherwise unavailable. False-positive MR imaging and/or 99mTc MIBI scintigraphic examination results were reviewed by one author (M.B.G.) and compared with findings at surgery and histopathologic examination to determine the cause of such findings. An attempt to determine the cause of false-negative MR imaging examinations was also performed.

Statistical Analysis
The sensitivity and positive predictive values of the two tests were calculated. The McNemar test was used to assess the difference in performance between MR imaging and 99mTc MIBI scintigraphy for abnormal parathyroid gland detection. Because all patients were expected to have at least one abnormal gland, a true-negative fraction was considered impossible; thus, specificity and negative predictive value could not be calculated (7,24).

The sensitivity of the combination of MR imaging and 99mTc MIBI scintigraphy for the detection of abnormal parathyroid tissue was also calculated on both a per-abnormal-gland and per-patient basis. For the latter, a true-positive result was recorded when either MR imaging or 99mTc MIBI scintigraphy helped correctly identify a proved abnormal parathyroid gland.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Identification of Abnormal Glands
MR imaging versus 99mTc MIBI scintigraphy.—At surgery, 130 abnormal glands were identified. MR imaging was used successfully to identify 107 (82%) of the 130 abnormal parathyroid glands, whereas 99mTc MIBI scintigraphy was used to correctly identify 110 (85%). Among the 99 normally positioned abnormal parathyroid glands, 35 (35%) and 14 (14%) were located along the posteroinferior border of the right and left lobes of the thyroid gland, respectively. Twenty-nine (29%) and 21 (21%) of the 99 normally located abnormal parathyroid glands (22%) were found along the posterosuperior border of the right and left lobes of the thyroid gland, respectively.

Of 130 abnormal parathyroid glands, 31 (24%) were ectopic (Table). MR imaging was used successfully to identify 29 (94%) of the 31 ectopic glands, and 99mTc MIBI scintigraphy was used successfully to identify 27 (87%). The sensitivity and positive predictive value of an abnormal MR imaging test were 82% (95% CI: 75%, 89%) and 89%, respectively. The sensitivity and positive predictive value for 99mTc MIBI scintigraphy were 85% (95% CI: 79%, 91%) and 89%, respectively. One test did not perform significantly better than the other for the detection of hyperfunctioning parathyroid tissue (P = .7).


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  		Locations of the 31 Ectopic Glands: MR Imaging and Scintigraphic Sensitivity
 
Among the abnormal parathyroid glands, 60 (46%) were adenomas, 39 (30%) were hyperplastic, and nine (7%) were parathyroid carcinomas. The remaining 22 (17%) of the resected abnormal glands were read as hypercellular. MR imaging depicted 53 (88%) and 99mTc MIBI scintigraphy depicted 54 (90%) of 60 adenomas. For hypercellular glands, MR imaging was used to correctly localize 17 (77%) and 99mTc MIBI scintigraphy, 14 (64%) of 22. Among the 39 glands read as hyperplastic, MR imaging depicted 32 (82%), whereas 99mTc MIBI scintigraphy depicted 35 (90%). MR imaging was used to correctly localize four (44%) of nine glands with parathyroid carcinoma, and 99mTc MIBI scintigraphy revealed seven (78%), including one left supraclavicular nodal metastasis that was not seen at MR imaging.

Combination of MR imaging and 99mTc MIBI scintigraphy.—The combination of MR imaging and 99mTc MIBI scintigraphy was used successfully to localize hyperfunctioning parathyroid tissue in 122 of 130 surgically proved abnormal glands, which yielded a sensitivity of 94% (95% CI: 90%, 98%). The positive predictive value of the combination of the two tests was 98%. One of the two tests was positive in 95 (97%) of 98 patients.

MR imaging.—In most cases, abnormal parathyroid tissue demonstrated isointense to low signal intensity relative to muscle on T1-weighted images, with increased signal intensity typically present on T2-weighted images. Intense contrast enhancement was frequently observed (Figs 1, 2).



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  		Figure 1a. True-positive MR and 99mTc MIBI scintigraphic images for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (4,000/105), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrowhead) is found in a common nonectopic location just inferior to the right lobe of the thyroid gland and demonstrates the characteristic pattern of low signal intensity on T1-weighted images and increased signal intensity on T2-weighted images, with strong contrast enhancement. (d) Planar 99mTc MIBI scintigraphic image obtained 2 hours after tracer injection demonstrates increased tracer uptake in the same location (arrow), which is consistent with parathyroid adenoma.

 


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  		Figure 1b. True-positive MR and 99mTc MIBI scintigraphic images for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (4,000/105), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrowhead) is found in a common nonectopic location just inferior to the right lobe of the thyroid gland and demonstrates the characteristic pattern of low signal intensity on T1-weighted images and increased signal intensity on T2-weighted images, with strong contrast enhancement. (d) Planar 99mTc MIBI scintigraphic image obtained 2 hours after tracer injection demonstrates increased tracer uptake in the same location (arrow), which is consistent with parathyroid adenoma.

 


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  		Figure 1c. True-positive MR and 99mTc MIBI scintigraphic images for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (4,000/105), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrowhead) is found in a common nonectopic location just inferior to the right lobe of the thyroid gland and demonstrates the characteristic pattern of low signal intensity on T1-weighted images and increased signal intensity on T2-weighted images, with strong contrast enhancement. (d) Planar 99mTc MIBI scintigraphic image obtained 2 hours after tracer injection demonstrates increased tracer uptake in the same location (arrow), which is consistent with parathyroid adenoma.

 


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  		Figure 1d. True-positive MR and 99mTc MIBI scintigraphic images for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (4,000/105), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrowhead) is found in a common nonectopic location just inferior to the right lobe of the thyroid gland and demonstrates the characteristic pattern of low signal intensity on T1-weighted images and increased signal intensity on T2-weighted images, with strong contrast enhancement. (d) Planar 99mTc MIBI scintigraphic image obtained 2 hours after tracer injection demonstrates increased tracer uptake in the same location (arrow), which is consistent with parathyroid adenoma.

 


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  		Figure 2a. True-positive MR images for ectopic parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/14), (b) T2-weighted (4,000/80), and (c) postcontrast T1-weighted (500/8) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrow) is in a location typical for parapharyngeal parathyroid adenomas and demonstrates characteristic signal intensity patterns on all three images. 99mTc MIBI scintigraphic images (not shown) were also used to correctly identify this lesion.

 


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  		Figure 2b. True-positive MR images for ectopic parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/14), (b) T2-weighted (4,000/80), and (c) postcontrast T1-weighted (500/8) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrow) is in a location typical for parapharyngeal parathyroid adenomas and demonstrates characteristic signal intensity patterns on all three images. 99mTc MIBI scintigraphic images (not shown) were also used to correctly identify this lesion.

 


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  		Figure 2c. True-positive MR images for ectopic parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/14), (b) T2-weighted (4,000/80), and (c) postcontrast T1-weighted (500/8) MR images with fat saturation in a patient with recurrent HPT after neck exploration. The adenoma (arrow) is in a location typical for parapharyngeal parathyroid adenomas and demonstrates characteristic signal intensity patterns on all three images. 99mTc MIBI scintigraphic images (not shown) were also used to correctly identify this lesion.

 
Ten (8%) of the 130 surgically proved abnormal parathyroid glands demonstrated atypical signal intensity characteristics at MR imaging. Four (3%) glands revealed increased T1 signal intensity; two of these lesions also had increased T2 signal intensity relative to muscle (Fig 3), and the other two demonstrated T2 signal intensity isointense to that of muscle. Hypercellular parathyroid tissue with an associated benign cyst was seen histopathologically in one of the two lesions that showed increased T1 and T2 signal intensity. This cyst contained lipid material and necrosis. The other lesion demonstrating increased T1 and T2 signal intensity was read only as hypercellular (Fig 3); no specific histopathologic correlate for the unusual signal intensities was noted.



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  		Figure 3a. Atypical signal intensity characteristics for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,416/90), and (c) postcontrast T1-weighted (483/20) MR images with fat saturation through the lower neck in a patient after transplantation of parathyroid tissue into the left sternocleidomastoid muscle. Parathyroid tissue was transplanted into the sternocleidomastoid muscle to prevent hypoparathyroidism after resection of native hyperplastic glands in the neck. This patient later developed symptoms of recurrent HPT. In a, increased signal intensity of the lesion (arrow) is revealed, a pattern atypical for hyperfunctioning parathyroid tissue. High T2 signal intensity (b) and strong enhancement (c), typical for parathyroid adenoma, are observed. No specific histologic correlate for the increased signal intensity on T1-weighted images was found.

 


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  		Figure 3b. Atypical signal intensity characteristics for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,416/90), and (c) postcontrast T1-weighted (483/20) MR images with fat saturation through the lower neck in a patient after transplantation of parathyroid tissue into the left sternocleidomastoid muscle. Parathyroid tissue was transplanted into the sternocleidomastoid muscle to prevent hypoparathyroidism after resection of native hyperplastic glands in the neck. This patient later developed symptoms of recurrent HPT. In a, increased signal intensity of the lesion (arrow) is revealed, a pattern atypical for hyperfunctioning parathyroid tissue. High T2 signal intensity (b) and strong enhancement (c), typical for parathyroid adenoma, are observed. No specific histologic correlate for the increased signal intensity on T1-weighted images was found.

 


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  		Figure 3c. Atypical signal intensity characteristics for parathyroid adenoma. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,416/90), and (c) postcontrast T1-weighted (483/20) MR images with fat saturation through the lower neck in a patient after transplantation of parathyroid tissue into the left sternocleidomastoid muscle. Parathyroid tissue was transplanted into the sternocleidomastoid muscle to prevent hypoparathyroidism after resection of native hyperplastic glands in the neck. This patient later developed symptoms of recurrent HPT. In a, increased signal intensity of the lesion (arrow) is revealed, a pattern atypical for hyperfunctioning parathyroid tissue. High T2 signal intensity (b) and strong enhancement (c), typical for parathyroid adenoma, are observed. No specific histologic correlate for the increased signal intensity on T1-weighted images was found.

 
The two lesions with increased signal intensity on T1-weighted images and signal intensity isointense to that of muscle on T2-weighted images were parathyroid carcinomas that were surrounded by dense fibrous tissue. In most cases, abnormal parathyroid tissue that demonstrated signal intensity isointense to or lower than that of muscle revealed no specific histopathologic correlate accounting for this signal intensity pattern. Eight (6%) glands were isointense to or lower in intensity than muscle on T2 weighted images. All but five (4%) of the resected abnormal glands demonstrated some degree of enhancement in the 100 cases in which contrast material was administered, although such enhancement was not always intense.

Histopathologic Correlation in False-Positive or False-Negative MR Imaging and 99mTc MIBI Scintigraphic Studies
In five of 13 false-positive MR imaging examinations, coexistent thyroid abnormalities, particularly exophytic thyroid nodules (Fig 4), resulted in false-positive MR imaging studies. Other surgically proved causes of false-positive MR imaging examinations included one case each of normal lymph nodes and follicular lymphadenitis. The cause of a false-positive MR imaging examination was uncertain in the six remaining false-positive studies. The most common causes of false-negative MR imaging interpretations included two cases of abnormal parathyroid glands adjacent to thyroid goiters, four cases of parathyroid hyperplasia, and five glands with parathyroid carcinoma.



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  		Figure 4a. False-positive MR images. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,600/90), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. A lesion (arrow) with signal intensity characteristics typical of hyperfunctioning parathyroid tissue is seen along the posterior aspect of the thyroid gland. These images were interpreted as suspect for parathyroid adenoma at this location. Histopathologic analysis of this lesion revealed that it was an exophytic thyroid adenoma. 99mTc MIBI scintigraphic images (not shown) were also used to correctly localize this lesion.

 


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  		Figure 4b. False-positive MR images. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,600/90), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. A lesion (arrow) with signal intensity characteristics typical of hyperfunctioning parathyroid tissue is seen along the posterior aspect of the thyroid gland. These images were interpreted as suspect for parathyroid adenoma at this location. Histopathologic analysis of this lesion revealed that it was an exophytic thyroid adenoma. 99mTc MIBI scintigraphic images (not shown) were also used to correctly localize this lesion.

 


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  		Figure 4c. False-positive MR images. Transverse (a) precontrast T1-weighted (500/20), (b) T2-weighted (3,600/90), and (c) postcontrast T1-weighted (500/20) MR images with fat saturation in a patient with recurrent HPT after neck exploration. A lesion (arrow) with signal intensity characteristics typical of hyperfunctioning parathyroid tissue is seen along the posterior aspect of the thyroid gland. These images were interpreted as suspect for parathyroid adenoma at this location. Histopathologic analysis of this lesion revealed that it was an exophytic thyroid adenoma. 99mTc MIBI scintigraphic images (not shown) were also used to correctly localize this lesion.

 
Causes of false-positive 99mTc MIBI scintigraphic studies included one case of thyroid tissue entrapped by dense surrounding fibrous tissue; two cases of exophytic thyroid nodules; one case each of lymph nodes with follicular hyperplasia, nodes with chronic inflammation, fibrosis, and anthracotic pigment (Fig 5); and one case of lymph nodes with sinus histiocytosis and hemosiderosis. False-negative 99mTc MIBI scintigraphic interpretations occurred in nine cases of parathyroid hyperplasia and two cases of parathyroid carcinoma.



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  		Figure 5. False-positive planar 99mTc MIBI scintigraphic image obtained 15 minutes after tracer injection reveals increased uptake in the mediastinum, which suggests ectopic, hyperfunctioning parathyroid tissue (straight arrow). This lesion was resected and was found to represent an enlarged lymph node containing anthracotic pigment. The 99mTc MIBI scintigraphic image also led to correct localization of the hyperfunctioning parathyroid tissue along the posteroinferior aspect of the left lobe of the thyroid gland (curved arrow). MR images (not shown) were also used to correctly localize this lesion.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
Initial surgical neck exploration in patients with primary HPT is successful in more than 95% of cases; in such circumstances, preoperative imaging has not proved necessary (22,26,41). However, the success rate of subsequent cervical explorations may approach only 60% (2,7,8,10). The lower success rate of subsequent surgical procedures may be related to anatomic distortion from scarring, an increased likelihood of ectopic adenomas or multiple abnormal glands in patients with initial failed explorations, supernumerary glands, surgical inexperience, or regrowth of abnormal parathyroid tissue (1,6,10,27,42). When HPT persists or recurs after neck exploration, preoperative imaging localization has been shown to improve the surgical success rate and decrease surgical morbidity (1,3,9–11,18,42–44).

Invasive preoperative imaging modalities include selective venous sampling and selective arteriography; both are expensive and technically difficult (45). Invasive techniques are frequently reserved for cases of recurrent or persistent HPT in which noninvasive techniques yield conflicting results or are inconclusive (9,12, 16,17,26,41,43,45).

Noninvasive imaging tests include US, CT, MR imaging, and scintigraphic methods, such as 99mTc pertechnetate–201Tl scintigraphy, 201Tl–iodine 123 subtraction scintigraphy, and 99mTc MIBI scintigraphy. The reported sensitivities for these techniques in the setting of recurrent or persistent HPT vary. The sensitivity for the identification of abnormal parathyroid glands by means of US is 34%–78% (3,7,10,12, 23,24,30,31,38,46,47). Disadvantages of US include operator dependence and limited fields of view; the latter is particularly troublesome when ectopic glands in the mediastinum are considered (7,26,28). US is often used as a preoperative imaging technique in patients with primary HPT and no history of prior neck surgery (1,21).

The sensitivity of CT for the detection of abnormal parathyroid glands is 46%–87% (10,12,17,24,26,40,46,48), depending on the size of the lesion. Disadvantages of CT include the use of ionizing radiation and iodinated contrast materials, as well as the possibility that streak artifacts from surgical clips in the neck from prior neck explorations may obscure abnormal parathyroid glands (7, 26,46).

MR imaging evaluation in patients with recurrent or persistent HPT has been examined extensively. The reported sensitivities of MR imaging, including both patients who have undergone surgery and patients who have not, is 42%–88% (2,3,7,10,12,17,19,23–28,30,32–34,38). Refinement in MR imaging equipment and techniques, as well as increased investigator experience, are likely responsible for the improved sensitivities in recent studies (7,19,25,26) compared with older data (2,23,24,30). Although CT and MR imaging both provide excellent anatomic detail, superior tissue contrast, ability to image vasculature without the need for contrast material, lack of ionizing radiation, multiplanar capability, and relatively minimal artifact surrounding surgical clips in the neck make MR imaging preferable to CT scanning in this patient population.

99mTc MIBI scintigraphy recently demonstrated a relatively high sensitivity and specificity for the detection of abnormal parathyroid glands in patients with recurrent or persistent HPT (7,12,17, 19,26,36–38). 99mTc MIBI scintigraphy has essentially supplanted other scintigraphic methods in this regard (7,15, 17,36). The 99mTc MIBI scintigraphic technique generally requires the use of only one tracer and also has the favorable photon energy of the 99mTc label; the latter allows improved depiction of lesions deep within the neck or chest relative to methods in which 201Tl is used. The 99mTc MIBI scintigraphic technique also allows dual-phase acquisitions, and SPECT may be performed. Reported sensitivities for the detection of abnormal parathyroid glands range from 50% to greater than 90% (4,7,12,15,17,19,25, 26,36,38). As with MR imaging, results of more recent reports (15,17,36,38) suggest that the sensitivity of the 99mTc MIBI scintigraphic technique is improving, perhaps owing to more extensive investigator experience, improvements in equipment and technique, and, importantly, the more widespread application of SPECT in these cases.

Consequently, a major purpose of this study was to reassess the value of MR imaging compared with that of 99mTc MIBI scintigraphy as a preoperative localization technique in patients with recurrent or persistent HPT, particularly in light of recent data suggesting that 99mTc MIBI scintigraphy may be the method of choice for the examination of such patients (15,17,38). In the current study, both MR imaging and 99mTc MIBI scintigraphy performed with high sensitivities (82% vs 85%, respectively) and positive predictive values (89% for both) for the identification of abnormal parathyroid tissue in patients with recurrent or persistent HPT after neck exploration. When combining the two examinations, the sensitivity for the detection of abnormal parathyroid tissue rose to 94%. Thus, combining a technique with superior anatomic resolution with a functional imaging study appears to maximize the detection of hyperfunctioning parathyroid glands; this phenomenon has also been noted previously (3,7,13,16,19,22,25,26).

Because all patients had hypercalcemia and elevated blood levels of parathyroid hormone, it is likely that all patients had HPT. Thus, because a true-negative fraction could not be defined, the specificity and negative predictive value of MR imaging and 99mTc MIBI scintigraphy could not be calculated. Other investigators (19) suggested that the specificity of 99mTc MIBI scintigraphy may exceed that of MR imaging, although false-positive results may occur with 99mTc MIBI scintigraphy (36).

Ectopic Glands
Approximately 5%–20% of parathyroid glands are ectopic (26,28,49), a situation that is even more frequent in patients with recurrent or persistent HPT after failed neck explorations. Abnormal ectopic parathyroid tissue was found as the cause of recurrent or persistent HPT in our series in 31 (32%) of 98 of patients, or in 31 (24%) of all 130 resected glands. MR imaging demonstrated excellent sensitivity for the detection of these lesions and helped identify 94% (29 of 31) of such glands (Fig 2). 99mTc MIBI scintigraphy also demonstrated good sensitivity (87%) for the detection of ectopic parathyroid tissue. Most important is that the combination of MR imaging and 99mTc MIBI scintigraphy led to accurate localization of all ectopic glands.

Correlation of Histopathologic Findings and MR Imaging Characteristics of Abnormal Glands
Abnormal parathyroid tissue typically demonstrates isointense to low signal intensity with sequences with short repetition and echo times and high signal intensity with sequences with long repetition and echo times (Figs 1, 2). Parathyroid adenomas demonstrated atypical signal intensity characteristics, such as increased T1 or decreased T2 signal intensity, in nearly 30% of cases in one series (23). Overall, 10 (8%) of the 130 glands in our series demonstrated signal intensity characteristics considered atypical for parathyroid adenomas.

Histopathologic Correlation in False-Negative and False-Positive Studies
The most frequent surgically proved cause of false-positive MR imaging examinations in our study was concomitant thyroid abnormalities (Fig 4), in particular exophytic thyroid nodules. This is not surprising, given that coexistent thyroid abnormalities have been noted in more than 40% of patients with HPT (50,51).

The most common discernable causes for false-negative MR imaging studies were adenomas situated closely adjacent to a thyroid goiter and cases of parathyroid hyperplasia and carcinoma. Other investigators (2,25,31,33,38,41,48,51,52) have also observed the increased prevalence of false-negative imaging studies in cases of parathyroid hyperplasia, as opposed to adenoma, although not all authors (32,34) agree. This observation may be the result of the relatively smaller size of hyperplastic glands as opposed to adenoma, although no discrete size threshold for the detection of abnormal parathyroid tissue has been firmly established (34). Alternatively, the lower sensitivity of imaging studies for hyperplasia as opposed to adenoma could reflect a satisfaction-of-search phenomenon (25,32).

False-negative 99mTc MIBI scintigraphic interpretations were observed in several cases of parathyroid hyperplasia and carcinoma, even with the use of SPECT. As with MR imaging, in several instances, the cause of false-negative 99mTc MIBI scintigraphic examination results was unclear.

In conclusion, MR imaging and 99mTc MIBI scintigraphy demonstrate high sensitivity and positive predictive value for the detection of abnormal parathyroid glands in patients with recurrent or persistent HPT after failed cervical explorations. There was no statistically significant difference in either sensitivity or positive predictive value between the two modalities. The combination of the two studies depicted more abnormal glands than either test alone. The superior anatomic resolution achieved with MR imaging combined with the physiologic information gained from 99mTc MIBI scintigraphy provided the most effective approach for the preoperative localization of hyperfunctioning parathyroid tissue in this patient population.


   FOOTNOTES
 
Abbreviations: HPT = hyperparathyroidism, MIBI = 2-methoxyisobutyl-isonitrile

Author contributions: Guarantor of integrity of entire study, M.B.G.; study concepts and design, C.B.H., M.B.G.; definition of intellectual content, C.B.H., M.B.G.; literature research, M.B.G.; clinical studies, E.T.M., O.H.C.; data acquisition, W.R.W., G.P.R., M.B.G., C.B.H.; data analysis, C.B.H., M.B.G.; statistical analysis, M.B.G.; manuscript preparation, M.B.G., C.B.H.; manuscript editing, M.B.G., C.B.H., E.T.M.; manuscript review, M.B.G., C.B.H., W.R.W., G.P.R., E.T.M.; manuscript final version approval, M.B.G.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 

  1. Clark OH, Duh QY. Primary hyperparathyroidism: a surgical perspective. Endocrinol Metab Clin North Am 1989; 18:701-714.[Medline]
  2. Peck WW, Higgins CB, Fisher MR, Ling M, Okerlund MD, Clark OH. Hyperparathyroidism: comparison of MR imaging with radionuclide scanning. Radiology 1987; 163:415-420.[Abstract/Free Full Text]
  3. Billingsley KG, Fraker DL, Doppman JL, et al. Localization and operative management of undescended parathyroid adenomas in patients with persistent primary hyperparathyroidism. Surgery 1994; 116:982-990.[Medline]
  4. Summers GW. Parathyroid update: a review of 220 cases. Ear Nose Throat J 1996; 75:434-439.[Medline]
  5. Rafferty MA, Hill AD, Zbar AP, et al. Cervical exploration for primary hyperparathyroidism: a 25 year experience. Ir Med J 1997; 90:188-189.[Medline]
  6. Shen W, Duren M, Morita E, et al. Reoperation for persistent or recurrent primary hyperparathyroidism. Arch Surg 1996; 131:861-869.[Abstract/Free Full Text]
  7. Numerow LM, Morita ET, Clark OH, Higgins CB. Persistent/recurrent hyperparathyroidism: a comparison of sestamibi scintigraphy, MRI, and ultrasonography. J Magn Reson Imaging 1995; 5:702-708.[Medline]
  8. Satava RM, Jr, Beahrs OH, Scholz DA. Success rate of cervical exploration for hyperparathyroidism. Arch Surg 1975; 110:625- 628.[Abstract/Free Full Text]
  9. Duh QY, Sancho JJ, Clark OH. Parathyroid localization: clinical review. Acta Chir Scand 1987; 153:241-254.[Medline]
  10. Flickinger FW, Sathyanarayana , White JE, McWhirt EB. MRI in hyperparathyroidism requiring reoperation. Clin Imaging 1991; 15:210-212.[Medline]
  11. Levin KE, Clark OH. Localization of parathyroid glands. Annu Rev Med 1988; 39:29-40.[Medline]
  12. Peeler BB, Martin WH, Sandler MP, Goldstein RE. Sestamibi parathyroid scanning and preoperative localization studies for patients with recurrent/persistent hyperparathyroidism or significant comorbid conditions: development of an optimal localization strategy. Am Surg 1997; 63:37-46.[Medline]
  13. Yousem DM. Parathyroid and thyroid imaging. Neuroimaging Clin N Am 1996; 6:435-459.[Medline]
  14. Yousem DM, Scheff AM. Thyroid and parathyroid gland pathology: role of imaging. Otolaryngol Clin North Am 1995; 28:621-649.[Medline]
  15. Udelsman R. Parathyroid imaging: the myth and the reality (editorial). Radiology 1996; 201:317-318.[Free Full Text]
  16. Rodriquez JM, Tezelman S, Siperstein AE, et al. Localization procedures in patients with persistent or recurrent hyperparathyroidism. Arch Surg 1994; 129:870- 875.[Abstract/Free Full Text]
  17. Moinuddin M, Whynott C. Ectopic parathyroid adenomas: multi-imaging modalities and its management. Clin Nucl Med 1996; 21:27-32.[Medline]
  18. Mitchell BK, Merrell RC, Kinder BK. Localization studies in patients with hyperparathyroidism. Surg Clin North Am 1995; 75:483-498.[Medline]
  19. Lee VS, Spritzer CE, Coleman RE, et al. The complementary roles of fast spin-echo MR imaging and double-phase 99m Tc-sestamibi scintigraphy for localization of hyperfunctioning parathyroid glands. AJR Am J Roentgenol 1996; 167:1555-1562.[Abstract/Free Full Text]
  20. Kebebew E, Clark OH. Parathyroid adenoma, hyperplasia, and carcinoma: localization, technical details of primary neck exploration, and treatment of hypercalcemic crisis. Surg Oncol Clin N Am 1998; 7:721-748.[Medline]
  21. Hopkins CR, Reading CC. Thyroid and parathyroid imaging. Semin Ultrasound CT MR 1995; 16:279-295.[Medline]
  22. Freitas JE, Freitas AE. Thyroid and parathyroid imaging. Semin Nucl Med 1994; 24:234-245.[Medline]
  23. Auffermann W, Gooding GA, Okerlund MD, et al. Diagnosis of recurrent hyperparathyroidism: comparison of MR imaging and other imaging techniques. AJR Am J Roentgenol 1988; 150:1027-1033.[Abstract/Free Full Text]
  24. Erdman WA, Breslau NA, Weinreb JC, et al. Noninvasive localization of parathyroid adenomas: a comparison of x-ray computerized tomography, ultrasound, scintigraphy and MRI. Magn Reson Imaging 1989; 7:187-194.[Medline]
  25. Fayet P, Hoeffel C, Fulla Y, et al. Technetium-99m sestamibi scintigraphy, magnetic resonance imaging and venous blood sampling in persistent and recurrent hyperparathyroidism. Br J Radiol 1997; 70:459-464.[Abstract]
  26. Giron J, Ouhayoun E, Dahan M, et al. Imaging of hyperparathyroidism: US, CT, MRI and MIBI scintigraphy. Eur J Radiol 1996; 21:167-173.[Medline]
  27. Higgins CB, Auffermann W. MR imaging of thyroid and parathyroid glands: a review of current status. AJR Am J Roentgenol 1988; 151:1095-1106.[Free Full Text]
  28. Kang YS, Rosen K, Clark OH, Higgins CB. Localization of abnormal parathyroid glands of the mediastinum with MR imaging. Radiology 1993; 189:137-141.[Abstract/Free Full Text]
  29. Kier R, Blinder RA, Herfkens RJ, et al. MR imaging with surface coils in primary hyperparathyroidism. J Comput Assist Tomogr 1987; 11:863-868.[Medline]
  30. Kneeland JB, Krubsack AJ, Lawson TL, et al. Enlarged parathyroid glands: high-resolution local coil MR imaging. Radiology 1987; 162:143-146[Erratum: Radiology 1987; 164:586.].[Abstract/Free Full Text]
  31. Krubsack AJ, Wilson SD, Lawson TL, et al. Prospective comparison of radionuclide,computed tomographic, sonographic, and magnetic resonance localization of parathyroid tumors. Surgery 1989; 106:639-646.[Medline]
  32. McDermott VG, Fernandez RJM, Meakem TJ, 3rd, et al. Preoperative MR imaging in hyperparathyroidism: results and factors affecting parathyroid detection. AJR Am J Roentgenol 1996; 166:705-710.[Abstract/Free Full Text]
  33. Spritzer CE, Gefter WB, Hamilton R, et al. Abnormal parathyroid glands: high-resolution MR imaging. Radiology 1987; 162:487-491.[Abstract/Free Full Text]
  34. Stevens SK, Chang JM, Clark OH, Chang PJ, Higgins CB. Detection of abnormal parathyroid glands in postoperative patients with recurrent hyperparathyroidism: sensitivity of MR imaging. AJR Am J Roentgenol 1993; 160:607-612.[Abstract/Free Full Text]
  35. Okuda I, Murata H, Ozawa Y, Kokubo T, Maruno T. Usefulness and limitations of 99mTc-MIBI scintigraphy for detection of parathyroid lesions. Nippon Igaku Hoshasen Gakkai Zasshi 1997; 57:668-674[Japanese].[Medline]
  36. Nguyen BD. Parathyroid imaging with Tc-99m sestamibi planar and SPECT scintigraphy. RadioGraphics 1999; 19:601- 616.[Abstract/Free Full Text]
  37. Ishibashi M, Nishida H, Okuda S, Suekane S, Hayabuchi N. Localization of parathyroid glands in hemodialysis patients using Tc-99m sestamibi imaging. Nephron 1998; 78:48-53.[Medline]
  38. Ishibashi M, Nishida H, Hiromatsu Y, Kojima K, Tabuchi E, Hayubuchi N. Comparison of technetium-99m-MIBI, technetium-99m-tetrofosmin, ultrasound and MRI for localization of abnormal parathyroid glands. J Nucl Med 1998; 39:320-324.[Abstract/Free Full Text]
  39. Ishibashi M, Nishida H, Hiromatsu Y, et al. Localization of ectopic parathyroid glands using technetium-99m sestamibi imaging: comparison with magnetic resonance and computed tomographic imaging. Eur J Nucl Med 1997; 24:197-201.[Medline]
  40. Von Schulthess GK, Weder W, Goebel N, et al. 1.5 T MRI, CT, ultrasonography and scintigraphy in hyperparathyroidism. Eur J Radiol 1988; 8:157-164.[Medline]
  41. Miller DL. Pre-operative localization and interventional treatment of parathyroid tumors: when and how?. World J Surg 1991; 15:706-715/LAST-PAGE>.[Medline]
  42. Levin KE, Clark OH. The reasons for failure in parathyroid operations. Arch Surg 1989; 124:911-915.[Abstract/Free Full Text]
  43. Clark OH, Okerlund MD, Moss AA, et al. Localization studies in patients with persistent or recurrent hyperparathyroidism. Surgery 1985; 98:1083-1094.[Medline]
  44. Clark OH. Current management of patients with hyperparathyroidism. Adv Surg 1996; 30:179-187.[Medline]
  45. Miller DL. Endocrine angiography and venous sampling. Radiol Clin North Am 1993; 31:1051-1067.[Medline]
  46. Miller DL, Doppman JL, Shawker TH, et al. Localization of parathyroid adenomas in patients who have undergone surgery. I. Noninvasive imaging methods. Radiology 1987; 162:133-137.[Abstract/Free Full Text]
  47. Gooding GA, Okerlund MD, Stark DD, Clark OH. Parathyroid imaging: comparison of double-tracer (T1-201, Tc-99m) scintigraphy and high-resolution US. Radiology 1986; 161:57-64.[Abstract/Free Full Text]
  48. Stark DD, Moss AA, Gooding GA, Clark OH. Parathyroid scanning by computed tomography. Radiology 1983; 148:297-299.[Abstract/Free Full Text]
  49. Akerstrom G, Malmaeus J, Bergstrom R. Surgical anatomy of human parathyroid glands. Surgery 1984; 95:14-21.[Medline]
  50. Lever EG, Refetoff S, Straus FHD, Nguyen M, Kaplan EL. Coexisting thyroid and parathyroid disease: are they related?. Surgery 1983; 94:893-900.[Medline]
  51. Lee VS, Spritzer CE. MR imaging of abnormal parathyroid glands. AJR Am J Roentgenol 1998; 170:1097-1103.[Free Full Text]
  52. De Feo ML, Colagrande S, Biagini C, et al. Parathyroid glands: combination of (99m)Tc MIBI scintigraphy and US for demonstration of parathyroid glands and nodules. Radiology 2000; 214:393-402.[Abstract/Free Full Text]



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