doi:10.2967/jnmt.107.039743
Journal of Nuclear Medicine Technology Volume 35, Number 3, 2007 135-139
© 2007 by Society of Nuclear Medicine
Tomoscintigraphy Improves the Determination of the Embryologic Origin of Parathyroid Adenomas, Especially in Apparently Inferior Glands: Imaging Features and Surgical Implications
David Taïeb1,
Rim Hassad1,
Frédéric Sebag2,
Cécile Colavolpe1,
Eric Guedj1,
Elif Hindié3,
Jean-François Henry2 and
Olivier Mundler1
1 Service Central de Biophysique et de Médecine Nucléaire, Centre Hospitalo-Universitaire de la Timone, Marseille, France; 2 Service de Chirurgie Générale et Endocrinienne, Centre Hospitalo-Universitaire de la Timone, Marseille, France; and 3 Service de Médecine Nucléaire, Centre Hospitalo-Universitaire Saint Louis, Paris, France
Correspondence: For correspondence or reprints contact: David Taïeb, Service Central de Biophysique et de Médecine Nucléaire, Centre Hospitalo-Universitaire de la Timone, 264 Rue Saint-Pierre, 13385 Marseille Cedex 5, France. E-mail: david.taieb{at}ap-hm.fr
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ABSTRACT
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Identification of the embryologic origin of hyperfunctioning parathyroid adenomas in primary hyperparathyroidism (PHPT) could determine the most suitable approach for minimally invasive surgery. The aim of this study was to prospectively evaluate the reliability of a new, combined protocol for the preoperative localization and determination of the embryologic origin of parathyroid adenomas. Methods: Anterior dual-isotope (123I/99mTc-sestamibi) static planar imaging followed by tomoscintigraphy (SPECT acquisition) centered over the 140-keV photopeak (combined protocol) was performed on 35 consecutive patients with sporadic PHPT. On the basis of anatomic considerations, adenomas were classified as superior (P4 derived) if they were located above the isthmus or posterior to the thyroid on SPECT images, despite their apparently middle to inferior position, and as inferior (P3 derived) if the foci were located in inferior and anterior positions or along the thyrothymic tract. Parathyroid ultrasonography was performed on all patients. Results: A total of 36 adenomas were removed: 34 solitary adenomas and 1 double adenoma (for totals of 19 P3-derived and 17 P4-derived adenomas). Pinhole subtraction imaging, SPECT, and ultrasonography sensitivities for detecting adenomas were 86%, 78%, and 77%, respectively. False-positive contralateral images were observed only with ultrasonography (3 cases). Positive SPECT results were associated with higher gland weights. Thirteen glands were identified by SPECT as posterior glands, despite their apparently inferior position, and were removed through an appropriate lateral endoscopic approach. Eleven (85%) of these glands had a P4 origin. Only 2 corresponded to large P3-derived adenomas (>2 g). Conclusion: By reclassifying apparently inferior adenomas as P4-derived adenomas prolapsed behind the thyroid gland, SPECT provides information about the most suitable surgical approach for avoiding recurrent laryngeal nerve injury. Additional pinhole images should increase the detection of small adenomas. The combined protocol offers both advantages.
Key Words: hyperparathyroidism; subtraction imaging; SPECT; minimally invasive surgery
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INTRODUCTION
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The diagnosis of primary hyperparathyroidism (PHPT) is based on laboratory criteria, including hypercalcemia, normal to elevated urinary calcium excretion, and inappropriately normal to elevated parathyroid hormone (PTH) levels. Surgery is the first-line therapy for PHPT despite the controversies that still exist regarding asymptomatic patients. A solitary parathyroid eutopic adenoma is the most common cause of PHPT, and preoperative imaging studies have only limited impact on bilateral cervicotomy (conventional open surgery) results (1). In contrast, identifying uniglandular disease has become crucial in selecting patients for minimally invasive surgery (MIS) (2). Parathyroid scintigraphy and neck ultrasonography are not reliable for identifying multiglandular disease, but their negative predictive value for multiglandular disease is high (3). Another aim of preoperative imaging is to localize as precisely as possible a hyperfunctioning gland. This is particularly true for parathyroid MIS, for which the accurate anatomic localization of a gland should also determine the most suitable surgical route for gland removal. At our institutions, the choice of the minimally invasive technique depends on the risk of recurrent laryngeal nerve injury during the dissection, which is dependent on the embryologic origin of the gland. Because the nerve runs posteriorly to the thyroid lobes, resections of P4-derived and, less frequently, posterior P3-derived adenomas are risky and should be performed via a lateral endoscopic route (4). In contrast, inferior glands should be removed via a small anterior incision.
Many studies have demonstrated the high sensitivity of parathyroid planar scintigraphy with 1 radiolabeled tracer (dual-phase protocol) or 2 radiolabeled tracers (subtraction method) for precisely locating the side and position of hyperfunctioning glands. The pinhole subtraction method seems to have better sensitivity than the dual-phase protocol for detecting small lesions or adenomas in patients with concomitant nodular thyroid disease. However, information provided by planar images is often insufficient to describe the embryologic origin of the involved glands. Such data are obtained by oblique pinhole imaging or SPECT acquisition. SPECT provides information on the neck and mediastinum. To our knowledge, the specific combination of dual-tracer pinhole subtraction imaging and SPECT has never been evaluated. The aim of this study was to evaluate a protocol involving high-resolution planar pinhole imaging followed by SPECT acquisition (combined protocol) for 35 consecutive patients who were good candidates for MIS.
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MATERIALS AND METHODS
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Patients
Between May 2006 and September 2006, 35 consecutive patients with laboratory evidence of PHPT were enrolled in the study. Inclusion criteria were as follows: apparent sporadic disease (absence of other endocrine tumor, negative family history), absence of a previous history of thyroidectomy, and absence of thyroid disease that warranted a transverse cervicotomy approach. Thyroid disease was excluded on the basis of clinical history, palpation, and available imaging data.
Preoperative imaging included neck ultrasonography and parathyroid scintigraphy. According to the results of the imaging workup, patients underwent surgery via a minimally invasive approach or a conventional bilateral cervicotomy. For patients undergoing MIS, the success of the surgery was validated by measurement of intraoperative PTH levels (50% decrease compared with the highest preexcision value). Cure was defined as normalization of serum calcium and PTH levels after gland removal.
Parathyroid Scintigraphy Combined Protocol
All patients underwent dual-isotope (123I/99mTc-sestamibi) static planar pinhole imaging followed by 99mTc-sestamibi SPECT on the same day. The same camera (Siemens ECAM) was used for both image acquisitions, but equipped, respectively, with pinhole and parallel-hole, low-energy, high-resolution collimators. The steps of the protocol were as follows.
First, the patients received 12 MBq of 123I. Two hours later, 740 MBq of 99mTc-sestamibi were injected. Pinhole acquisition was started 3 min after 99mTc-sestamibi injection; static anterior cervical views were obtained for 20 min with 2 photopeaks of 7% energy windows, centered, respectively, over the 140-keV photopeak of 99mTc and over the 159-keV photopeak of 123I (128 x 128 matrix, zoom of 2.67). Interactive software was used for image normalization and subtraction.
The tomographic study was started after the collimators were changed (at 30–45 min after sestamibi injection), with the following parameters: 128 x 128 matrix, zoom of 1.45, 45 s per projection at each of 32 angular steps, and sampling of a 360° orbit every 24°. The photopeak was centered over 140 keV only, and iterative reconstruction was performed with a gaussian filter (full width at half maximum, 10 mm). The neck and the mediastinum (from the angle of the mandible to the heart) were included in the field of view.
Image Interpretation
Two independent nuclear medicine physicians reviewed pinhole subtraction and SPECT images separately.
A positive finding on pinhole images was defined as residual 99mTc activity after normalization and subtraction. On SPECT images, a positive finding was defined as focal uptake in an ectopic position (posterior or inferior to the thyroid lobe, mediastinal) or as focal tracer retention in an area of the thyroid distinct from the remaining thyroid tissue. Lesions were classified as superior (P4 derived) if they were located above the isthmus or behind the thyroid on SPECT images, despite their apparently inferior position, and as inferior (P3 derived) if they were located in inferior and anterior glands (at the tip of the inferior pole of the thyroid lobe or along the thyrothymic tract).
Finally, a finding was designated as positive if both reviewers were in agreement. In case of disagreement, a third reviewer was used to reach a consensus.
Additional Imaging Techniques
The same trained radiologist performed neck ultrasonography on all patients (Philips-ATL HDI 5000 system with a 12-MHz linear transducer).
Statistical Analysis
To identify factors that could influence imaging results, distributions of age, serum calcium levels, PTH levels, and gland weight in patients with positive and negative results were compared with a Mann–Whitney–Wilcoxon test. In patients with a solitary adenoma, the correlation among preoperative serum calcium levels, PTH levels, and gland weight was calculated with the Pearson correlation coefficient.
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RESULTS
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Patient and Tumor Characteristics
Thirty of the 35 patients were women, with a mean age of 61 y (mean ± SD, 61 ± 11 y). Preoperative median serum calcium and PTH levels were 2.65 mmol/L (2.69 ± 0.13) and 79 ng/mL (97 ± 71), respectively. A total of 36 adenomas were removed: 34 solitary adenomas and 1 double adenoma (left and right P4-derived adenomas). The median gland weight was 880 mg (1,095 ± 880). Gland weight was significantly correlated with preoperative PTH levels (P = 0.047, r2 = 0.34) but not with hypercalcemia. Only one supernumerary ectopic gland, located in the thymus, was identified (130 mg). No major ectopia was found. Adenomas developed from P3 glands in 19 patients (6 right P3-derived and 13 left P3-derived adenomas) and P4 glands in 16 patients (17 adenomas: 11 right P4-derived and 6 left P4-derived adenomas, including 1 P4-derived double adenoma).
Imaging Results and Surgical Considerations
Diagnostic Accuracy of Parathyroid Scintigraphy and Intrapatient Comparison of Protocols.
Planar pinhole imaging results were positive for 31 of 36 adenomas (86%). SPECT results were positive for 28 of 36 adenomas (78%). No false-positive lesion was reported. In 3 cases, adenomas were visualized only on pinhole images (130, 200, and 580 mg). No lesion was localized by SPECT alone. The double adenoma was visualized by both scintigraphy protocols. In 2 cases, the localization of adenomas was doubtful only on SPECT images and required a third reviewer to reach a consensus. Gland weight was significantly higher in patients with positive SPECT results (P = 0.0078) than in those with negative results. Age, serum calcium levels, and PTH levels were not statistically different for positive and negative pinhole subtraction imaging and SPECT results.
Comparison of Parathyroid Scintigraphy and Ultrasonography.
Parathyroid ultrasonography correctly identified 28 adenomas (78%) but produced contralateral false-positive results in 3 cases. Ultrasonography provided the sole positive results in 2 cases (350 and 680 mg). It missed one lesion in the patient with a double adenoma.
Value of SPECT Used with Planar Imaging for Determination of Embryologic Origin of Involved Glands and Surgical Implications.
As shown in Figure 1, P4-derived adenomas seen on planar images were widely distributed throughout the inner part of the thyroid lobe. Half of the P4-derived adenomas were located in the middle portion of the thyroid lobe, at the medial margin, close to the isthmus. In contrast, 95% of P3-derived adenomas were located at the tip of the inferior lobe or along the thyrothymic tract. Thirteen glands were identified by SPECT as posterior glands, despite their apparently inferior position, and were removed through an appropriate lateral endoscopic approach. Eleven (85%) of these glands had a P4 origin. Only 2 corresponded to large P3-derived adenomas (>2 g). By reclassifying apparently inferior adenomas as P4-derived adenomas prolapsed behind the thyroid gland, SPECT provided information about the most suitable surgical approach for avoiding recurrent laryngeal nerve injury (Figs. 2–4
). Anterior P3-derived adenomas were removed via a small cervical incision (mini-opening approach). Patients with negative preoperative imaging results, discordant imaging results, or multiglandular disease underwent conventional bilateral cervical surgery. Thus, 29 patients underwent surgery via a focused approach, and 6 underwent conventional bilateral cervical surgery. No surgical conversion was performed. Only one patient had persistent hyperparathyroidism because of partial gland removal. Other patients had normal serum calcium and PTH levels. No hypoparathyroidism or recurrent nerve palsy was observed.
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ABSTRACT
INTRODUCTION
