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Annals of Surgical Oncology 8:856-860 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Minimally Invasive, Radioguided Surgery for Primary Hyperparathyroidism

G. McGreal, FRCSI, D.C. Winter, MD, FRCSI, S. Sookhai, FRCSI, D. Evoy, FRCSI, M. Ryan, FRCSI, G.C. O’Sullivan, MCh, FRCSI and H.P. Redmond, MCh, FRCSI

From the Academic Department of Surgery and Department of Surgical Oncology, National University of Ireland, Cork, at Cork University Hospital, and Mercy Hospital, Cork, Ireland.

Correspondence: Address correspondence and reprint requests to: Professor H. P. Redmond, MCh, FRCSI, Academic Department of Surgery, Cork University Hospital, Wilton, Cork, Ireland; Fax: 353-21-343307; E-mail: p.redmond{at}ucc.ie


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Primary hyperparathyroidism affects 1 in 700 individuals in the United States. A single adenoma is responsible in over 85% of cases. Surgery remains the most effective treatment. This study was designed to assess the feasibility of minimally invasive radioguided parathyroidectomy (MIRP) with confirmation of excision by ex vivo radioactivity alone.

Methods: Seventy-five consecutive patients with primary hyperparathyroidism were prospectively studied. Following sestamibi scan, patients underwent unilateral neck exploration guided by a handheld gamma probe, which was also used to measure ex vivo radioactivity of excised tissue.

Results: The sestamibi scan was positive in 88% of the patients. A small incision (mean, 3.2 ± 0.3 cm) was sufficient. Ectopic gland sites were localized in five patients with positive scans and single adenomas. Mean operative time was 48 minutes (range, 15–125 minutes), with shorter procedures after the initial 20 cases (mean, 24 vs. 72 minutes; P < .01). Radioguided parathyroidectomy was successful in 97%, with a mean follow-up of 11 months (range, 1–26 months). As noted previously, adenomatous parathyroid glands contained more than 20% of the background radioactivity.

Conclusions: MIRP is a feasible alternative to bilateral dissection with the advantages of guided dissection and rapid confirmation, and may become the procedure of choice for primary hyperparathyroidism.

Key Words: Hyperparathyroidism • Minimally invasive parathyroidectomy • Sestamibi


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Primary hyperparathyroidism affects 1 in 700 individuals, with an estimated 100,000 new cases diagnosed annually in the United States.1,2 A single adenoma is responsible for the elevated parathyroid hormone levels in approximately 85% to 90% of cases; removal of this gland is curative.1,2 Until recently, most surgeons recommended bilateral neck exploration for all cases of primary hyperparathyroidism.2–6 The rationale for this approach was the inability either to localize adenomas unilaterally preoperatively or to exclude the 15% of cases with multiple adenomas or gland hyperplasia. However, recent advances in scintigraphic mapping, alone or in combination with ultrasonography, have facilitated the localization of adenomas in single gland disease and in cases necessitating re-exploration for recurrent or persistent hyperparathyroidism.7–9 Specificity for identifying patients with a single adenoma approaches 100%, with sensitivity rates of up to 95%.7–9 The result has been an evolution in parathyroidectomy, with the result that unilateral neck exploration with the aid of 99mTc sestamibi tomographic imaging (MIBI) was developed.10 Several series have reported successful unilateral exploration guided by scintigraphic parathyroid mapping.11–16 Furthermore, unilateral exploration under local anesthesia or minimally invasive resection under cervical block anesthesia has been employed successfully.17,18

The use of a handheld gamma probe to localize radioactive parathyroid tissue following MIBI imaging has been able to facilitate further minimally invasive approaches or to isolate glands that lie in an ectopic position.14 Although it confers considerable advantages, some view it as superfluous gadgetry when rapid intraoperative parathyroid hormone (PTH) monitoring is available.14,15 However, a recent study of more than 1200 tissue specimens resected with the radioguided technique has demonstrated that radioactive ratios can confirm parathyroidectomy adequately.16 Excised tissue that contains over 20% of background radioactivity in a patient with a positive sestamibi scan is strong evidence for a solitary adenoma. Equivalent ratios for fat, lymph nodes, or normal parathyroids were <2.5%, and those of hyperplastic parathyroids were <16%. Thus, the technique of radioguided surgery not only facilitates parathyroidectomy, but also obviates intraoperative monitoring of PTH, frozen section, or identification of other glands in at least 85% of cases.16 Our experience with minimally invasive radioguided parathyroidectomy and ex vivo radioactive ratios using this 20% rule is presented here.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Seventy-five consecutive patients with primary hyperparathyroidism were prospectively studied with informed consent. On the morning of surgery, patients received 740 MBq of 99mTc–methoxyisobutylisonitrile (sestamibi). Fifteen minutes later, with the patient supine and the neck extended, a static image was acquired with a gamma camera. A further image was acquired 2 hours following injection. Early and late images were compared to identify high-uptake regions, and a dual phase technique was selected rather than subtraction scanning because the latter carries a higher false-positive rate.19 Focal areas of increased isotope uptake were marked on the skin.

Patients were transferred to the operating room within 3 hours of the initial injection. A handheld gamma probe (Navigator; United States Surgical Corp., Norwalk, CT) was used to map radioactivity within the quadrants of the neck before the incision was made. When the deep fascia in the neck was opened, the gamma probe was employed to direct dissection to the area of maximal radioactivity. Ex vivo radioactivity was recorded from all excised tissues (in counts per second of gamma radiation), and the equivalent background radioactivity from the operative field was determined. Radioactive ratios of ex vivo tissue versus background radioactivity were calculated and expressed as a percentage. Parathyroidectomy was considered successful if the excised tissue was morphologically consistent with a parathyroid gland, in particular an adenoma, and contained more than 20% of background radioactivity.16 The procedure was terminated if both criteria were met. Incisions were closed in layers in a standard fashion, and only cases of bilateral dissection were drained. Operative time from the time of incision to completion of skin closure was recorded in all cases. The serum calcium level was measured prior to discharge and at the 1-month postoperative clinic visit, at which time the parathyroid hormone levels were reassessed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Seventy-five consecutive patients presenting with primary hyperparathyroidism underwent sestamibi scanning and radioguided parathyroidectomy. The mean age was 61 ± 13 years (range, 28–86 years). Fifty-one patients were female (approximate female:male ratio of 2:1). The sestamibi scan was positive in 66 of 75 cases (88%), with a single high-uptake focus demonstrated. There was no focal uptake in the remaining 9 cases (12%). Patients with a positive scan underwent radio-guided parathyroidectomy via a minimally invasive approach with a transverse incision measuring <=4 cm (mean, 3.2 ± 0.3 cm). The operation was performed under local anesthesia (bupivacaine) and intravenous sedation (midazolam) in 13 patients in this group (20%). General anesthesia was employed in all other patients. A traditional bilateral dissection via a transverse cervical incision was performed in the nine cases in which no focal uptake was identified on sestamibi scanning. In these cases, all glands were identified, and abnormal glands (morphologically and with more than 20% background radioactivity) were excised. Therefore, the probe was used in all procedures irrespective of sestamibi scan findings.

Multigland disease (i.e., adenomas or hyperplasias involving more than one gland) was found in six patients (8%), all of whom had a negative sestamibi scan. Formal dissection assisted by probe guidance was performed in these patients. Ectopic parathyroid gland sites were identified in five patients with positive scans and single adenomas: in two, in the superior mediastinum, and in the other three, in an intrathyroidal position. The former were accessed by extending the dissection into the mediastinum; the latter were extirpated by lobectomy and histologically confirmed to be intrathyroidal (completely surrounded by thyroid tissue). Radioguidance facilitated the localization and identification of these aberrant glands. The 20% rule16 applied to the successful radio-guided parathyroidectomies for all adenomas. That is, if the excised tissue contained more than 20% of the background radioactivity, it was always confirmed histologically as an adenomatous parathyroid gland (Table 1). Meanwhile, lymph nodes, thyroid tissue, and normal or hyperplastic glands consistently were found to have less than 20% of the level of background radioactivity (Table 1).


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  		TABLE 1. Radioactive ratios (percentage of background radioactivity) of parathyroid adenomas and other excised tissue (confirmed histologically)
 
The mean operative time was 48 minutes (range, 15–125 minutes), with a tendency to shorter operative times after the first 20 cases (mean, 24 versus 72 minutes; P < .01). Radioguided parathyroidectomy was successful in 73 patients (97%), with return to normal serum parathyroid hormone levels. Two cases of persisting hyperparathyroidism occurred (one of which met the criteria for the 20% rule at initial operation), one due to four-gland hyperplasia and the other to a missed second adenoma. In this case of hyperplasia, which occurred early in the series, the gland removed was morphologically consistent with an adenoma. A second procedure was performed successfully by traditional exploration in both patients without undue difficulty, because only one quadrant of the neck had been explored at the first operation and scarring was minimal. In the first case, the complete dissection revealed all three remaining hyperplastic glands containing less than 20% of background radioactivity (Table 1). All glands were excised, and a portion of one was implanted in the left sternocleidomastoid muscle. In the other case, the second adenoma arose in the opposite quadrant (right superior) and also contained more than 20% of background radioactivity. Hypercalcemia was eliminated in all patients (Table 2). Three patients with multigland disease and three with single adenomas developed transient hypocalcemia that resolved with oral supplementation with activated vitamin D and calcium salts. These patients required admission for a total of 3 days, whereas all other patients were discharged within 48 hours. There were no recurrent laryngeal nerve injuries and no wound complications. All patients have remained free of hypercalcemia with a mean follow-up of 11 months (range, 1–26 months).


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  		TABLE 2. Pre- and postoperative biochemical parameters
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Most patients presenting with primary hyperparathyroidism have a solitary adenoma; a small proportion have four-gland hyperplasias or multiple adenomata, but carcinomas are rare.2,20,21 Surgical excision remains the standard of care, with low complication rates and excellent results.1,2,22,23 Patients enjoy a good quality of life and return to age- and sex-matched life spans following parathyroidectomy.24,25 The advent of minimally invasive surgery has led to a reevaluation of parathyroidectomy techniques. Preoperative localization with MIBI, which has higher sensitivity (>90%) than ultrasonography (70–80%), computed tomography (~75–83%), or magnetic resonance imaging (~85%),26,27 has revolutionized parathyroidectomy and permitted minimally invasive radioguided surgery (MIRP).14 Centers with experience in this technique report that it is successful, safe, and can be performed quickly through a small incision, even under local anesthesia or as an outpatient procedure.14,16–18,27,28 Patients who have undergone previous neck surgery also have had successful MIRP procedures.29

This study outlines our initial experience with MIRP using the 20% rule described previously for confirmation of adenoma excision.16 The 20% rule applied to parathyroid adenomata in all cases, and nonparathyroid tissue or normal glands consistently displayed < 10% of background radioactivity. A regression analysis revealed no correlation between the serum level of PTH and the radioactive counts of the removed adenomata (results not shown). This reflects the heterogeneity of gland size and isotope uptake, and of the serum hormone levels. A unilateral approach was undertaken in which scintigraphic mapping localized a single gland and bilateral exploration in the remaining cases. In either scenario, the handheld gamma probe was a useful adjunct for localizing glands, confirming parathyroid tissue ex vivo, and identifying a drop in the background radioactivity following excision. Furthermore, in our experience, probe guidance facilitated the identification of parathyroid adenomas in aberrant sites.

Accurate scintigraphy requires dedicated staff. There is a learning curve at inception, and the scan quality can be variable.7,8,14,30 This may adversely influence local perception of nuclear mapping if the quality of scan is not conducive to confident unilateral surgery.2,5,31–34 Furthermore, opponents to unilateral exploration cite potential injuries to the recurrent laryngeal nerve, incomplete parathyroid extirpation in multigland disease, and inability to assess the thyroid gland confidently for coexisting abnormalities, due to inadequate exposure.31–34 Early experience suggests that the arguments against unilateral surgery are largely invalid with regard to MIRP. It has comparable success rates and safety, may be used in the reoperative neck, and has been found to confer significant cost reductions when compared to a conventional approach13,14,16,28–30,35,36.

Rapid PTH assays have been developed and used to confirm successful excision of abnormal glands within minutes.14,37–39 They may be a useful adjunct in minimally invasive parathyroidectomy by improving accuracy, although the additional expense may limit their use in radioguided surgery due to cost-benefit imbalance. Nevertheless, the two cases of persisting hyperparathyroidism in the present series might not have occurred had a rapid PTH assay been used. The relative contributions of sestamibi scanning, intraoperative gamma probe localization, and the rapid PTH assay were outlined recently.40 In this series of 32 patients, 28 of whom had primary hyperparathyroidism, a directed operation was facilitated by all techniques, and it was concluded that a minimally invasive procedure may be performed in selected cases. Furthermore, the authors stated that the combination of techniques allows for successful reoperative parathyroidectomy. A controlled trial of MIRP alone versus minimally invasive parathyroidectomy using rapid PTH assay confirmation without probe radioguidance may be useful to compare efficacy and cost in order to establish which technique is superior.

Minimally invasive surgery for primary hyperparathyroidism recently was compared with the traditional approach by analysis of data (odds ratios) from published studies.41 Although confidence intervals were large, the analysis favored the unilateral technique for safety and efficacy.41 Recommendations with regard to a unilateral approach by these authors and others12,37,40,41 include preoperative identification of a presumed solitary adenoma and exclusion of patients with apparent multiple gland disease, multiple endocrine neoplasia, goiter, or previous surgery or irradiation to the neck. In conclusion, because MIRP is a feasible alternative to bilateral dissection in most cases, and has the advantages of guided dissection and rapid ex vivo confirmation, we believe that is should be the procedure of choice for primary hyperparathyroidism.

Received for publication November 28, 2000. Accepted for publication August 16, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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