Unilateral versus bilateral neck exploration in parathyroid surgery: An assessment of 55 cases.
We retrospectively evaluated the cases of 55 patients who had undergone surgery for primary hyperparathyroidism at our institution to determine whether their parathyroid glands were abnormal on both sides. Thirty-six of these patients had undergone a bilateral neck exploration, and 19 had had a unilateral investigation. Of the 36 bilaterally explored patients, 30 had a solitary adenoma and no parathy raid pathology on the opposite side, five patients had hyperplastic glands with more than one gland involved, and one patient had two adenomas. In the unilaterally explored group, all 19 patients had a solitary adenoma. There were no failures in the way of persistent hypercalcemia in either group. Based on ourfindings, we conclude that a unilateral neck exploration should be performed during surgery for primary hyperparathyroidism whenever a large parathyroidadenoma and a normal parathyroid gland are found on the same side. Bilateral exploration should be reserved for patients in whom pathology cannot be found on the initially explored side during surgery and for patients who have obvious parathyroid hyperplasia.
Surgical approaches to the treatment of patients with primary nonsyndromal hyperparathyroidism are designed to find and remove the abnormal parathyroid tissue and re-establish normocalcemia. Surgery should limit complications such as hypocalcemia, nerve injury, and persistent hypercalcemia.  Some head and neck surgeons explore both sides and identify all parathyroid glands. Their rationale is that the incidence of multiple gland disease is high and the complication rate of bilateral exploration is low in experienced hands. [2,3] Other surgeons advocate unilateral neck exploration when there is a reliable preoperative localization study and both an abnormal and normal gland on the initially explored side.  Their preference is based on the fact that in 85% of all cases, primary hyperpararthyroidism is caused by a single adenoma and that the presence of microscopic hyperplasia is not clinically significant.
To determine the true incidence of bilateral disease, we reviewed the findings in 55 patients who had been explored during surgery for primary hyperparathyroidism. We paid particular attention to the incidence of pathology on both sides of the neck and to the value of preoperative localization studies. We found that the incidence of bilateral neck disease was low and that the preoperative localization studies were generally accurate.
Materials and methods
We retrospectively reviewed the records of 62 patients who had undergone parathyroid exploration for hyperparathyroidism at our institution between 1985 and 1993. Our study included a review of the operative and pathology reports to determine if there was pathology on both sides of the neck, the type of pathology, and the number of glands found during bilateral exploration. The results of preoperative localization studies were compared with pathologic findings when possible. All patients had undergone some type of neck imaging for parathyroid mass localization--either ultrasonography, computed tomography (CT), magnetic resonance imaging (MRI), or radioisotope scanning. Most patients who had undergone surgery before 1992 routinely had a bilateral neck exploration. Subsequent patients were routinely scheduled for a unilateral exploration, and the decision to expand to a bilateral exploration was not made until the intraoperative pathology was evaluated.
Of the 62 patients whose cases we reviewed, 55 had had primary hyperparathyroidism. Thirty-six of them had undergone a bilateral neck exploration and 19 had had a unilateral procedure.
Bilateral exploration. Among the 36 patients who underwent a bilateral neck exploration, 30(83.3%) had a solitary adenoma with pathology confined to one side of the neck. Five patients (13.9%) had parathyroid hyperplasia with more than one gland involved, and one patient (2.8%) had two adenomas. In all, six of the 36 patients (16.7%) had bilateral pathology.
We were unable to identify at least one parathyroid gland in 18 patients (50%); three glands were not identified in three patients, two glands were not found in five patients, and one gland was not identified in 10 patients. In 15 patients (41.7%), we were unable to identify either one or two glands on the side opposite the pathologic side, and in five patients (13.9%) we could not find the second parathyroid gland on the same side as a pathologically enlarged gland.
Unilateral exploration. All 19 patients who had undergone unilateral exploration had had a solitary adenoma and a normal parathyroid gland on the explored side. However, the normal gland was not always confirmed histologically.
Localization. Preoperative localization studies were accurate in all 19 patients who had undergone a unilateral exploration. Among the 36 patients who had had a bilateral exploration, three patients (8.3%) had lesions that could not be localized by imaging studies and three had incorrect localizing studies. There were no failures in the way of persistent hypercalcemia in either group.
Proponents of unilateral exploration. Selective unilateral neck exploration was first advocated by Roth et al  and subsequent]y supported by Tibblin et al. [6-8] The rationale for this approach is based on the fact that in 85% of cases, primary nonsyndromal hyperpararthyroidism is caused by a single adenoma. These authors reported that unilateral exploration produced a lower incidence of morbid postoperative hypocalcemia and recurrent nerve injury, caused less destruction of tissue planes, and required a shorter operating time. They also pointed out that the incidence of persistent or recurrent disease was not any higher than it is when a bilateral exploration is performed.
Wang reviewed the records of 1,300 patients with hyperparathyroidism who were seen over a 60-year period.  Some 564 of these patients had undergone a unilateral exploration based on the results of preoperative studies and based on the detection of both an adenoma and a normal gland on the explored side. The failure rate in this group was only 4%. Wang reported that unilateral exploration produced less morbidity and shortened the duration of both operating times and hospital stays.
Lucas et al studied 19 patients who had undergone unilateral exploration for primary hyperparathyroidism on the basis of positive ultrasound findings and found no failures.  Duh et al developed a mathematical model for the surgical treatment of primary hyperparathyroidism and reported that the risk of missing an adenoma on unilateral exploration is only 2% when the surgeon uses a preoperative localization study that has a sensitivity of at least 80%.  They wrote that the probability of missing a double adenoma during a unilateral approach is equal to the actual incidence of multiple adenomas--that is, approximately 2.2%.
Worsey et al reported their findings over 15 years in 371 patients who had been explored for primary hyperparathyroidism.  It was their practice to routinely explore the right side of the neck and stop there whenever they found both an adenoma and a histologically confirmed normal gland. They began their exploration on the left side of the neck only when preoperative localization studies favored that side. Under these criteria, 125 of the 371 patients had undergone a unilateral exploration, and 122 of them (97.6%) had had a single adenoma. There were no complications in this group. The remaining 246 patients required a bilateral exploration. The failure rate in this group was 7%, and the complication rate was 1.5%. Worsey et al concluded that unilateral exploration in primary hyperparathyroidism is safe and cost-effective and avoids obliterative scarring of the contralateral neck. Petti also advocated performing a unilateral exploration when the preoperative localization tests are correct and the remaini ng gland is normal on histologic examination. 
The overall cure and morbidity rates in our 19 patients who underwent unilateral exploration were comparable to those reported in several large series of patients who underwent routine bilateral neck dissection.
Proponents of bilateral exploration. Bilateral exploration has many advocates as well. Their reasons include the unreliability of localization studies, the variability of disease in more than one gland, and variables such as the skill of the surgeon and the age of the patient.
Attie et al stressed the need to perform bilateral exploration because most of the cases of multiple adenoma seen in their series were bilateral.  However, Attie et al believed that the only criterion for removal in primary hyperparathyroidism is an enlargement of the parathyroid glands. They felt that microscopic hyperplasia is not clinically significant; moreover, the removal of only enlarged glands at surgery resulted in normocalcemia for many years. Of note was their statement that they sometimes could not find a fourth gland during exploration.
Nottingham et al reported the results of bilateral exploration in 73 patients with primary hyperparathyroidism.  The failure rate with preoperative ultrasonographic localization was 37%. A total of 38 of their patients (52%) underwent removal of an adenoma and biopsy of one gland. Eighteen patients (25%) had a subtotal parathyroidectomy to remove microscopic hyperplasia. Five patients (7%) had two adenomas, and ten patients (14%) had transient hypocalcemia. Nottingham et al reported that 72 of the 73 patients (99%) were cured. The incidence of multiple gland abnormality in this series was 41%. Because of the high incidence of multiple gland involvement, the authors concluded that these patients would not have been cured with unilateral exploration.
Thompson et al also advocated bilateral exploration for parathyroid disease, arguing that the incidence of multiple gland disease approaches 20%.  Paloyan et al advocated a subtotal parathyroidectomy for primary hyperparathyroidism because the disease is multifocal.  Roses et al found that the failure to remove even a slightly enlarged parathyroid gland resulted in clinical failure; they suggested that any enlargement found on surgical exploration, even just a slight one, might be clinically significant, and therefore they believed that all glands should be explored at surgery. 
Localizing studies. Gaz found that a reliance on preoperative localization studies had its drawbacks.  Among them were the facts that adenomas and multiple enlarged glands were often missed and that surgeons were misled by false-positive results. The added cost of the localization studies had to be weighed against the cost of re-exploration if there was a failure. Gaz felt that in skilled hands, bilateral exploration is safe and rapid, results in low morbidity, and does not significantly increase cost.
Obtaining a sensitive preoperative study increases the probability that a patient will undergo a unilateral exploration and decreases the probability that a tumor on the opposite side will be missed. A sensitive localization study also improves outcomes by identifying multiple adenomas. The sensitivities of the available localization studies--ultrasonography, CT, MRI, thallium 201 scanning, and technetium-99m sestamibi scanning--are all in the range of approximately 80%.  Without a preoperative localization study, the probability that a tumor on the unexplored side will be missed is 8%. When the prevalence of double adenomas is 2%, as it was in our series, the risk of missing a second adenoma is 3.6%. The mean incidence of multiple adenomas is 2.2% (range: 0 to 10%), but it is more common in patients with multiple endocrine neoplasia and familial hyperparathyroidism.
We were not able to determine which preoperative localizing modality was the most sensitive because we used a number of combination studies; we did find that the thallium/sestamibi study was particularly effective.
Another effective tool is the quick parathyroid hormone (PTH) level measurement by immunochemiluminometric assay. This assay provides measurements in only 10 minutes, which makes it practical during a parathyroidectomy. The PTH assay is easy to obtain, it obviates the need for radioisotope scanning, and it provides an objective endpoint of surgery.
Our recommendations. First, we recommend a unilateral approach for neck exploration in primary hyperparathyroidism when both a large parathyroid adenoma and normal parathyroid gland are found at surgery. Limiting the extent of neck exploration reduces the incidence of trauma to the normal parathyroids and recurrent nerves and lowers the incidence of permanent hypoparathyroidsm to near zero. Unilateral exploration performed by an experienced surgeon also results in shorter operating times and lengths of hospital stay.
Second, bilateral neck exploration should be reserved for patients who have parathyroid hyperplasia and for those in whom the preoperative localization study is incorrect.
Finally, a controlled multicenter study should be undertaken to realistically assess the comparative value of the different localization studies and the cost-effectiveness and resultant morbidity associated with both surgical approaches.
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|Comment:||Unilateral versus bilateral neck exploration in parathyroid surgery: An assessment of 55 cases.|
|Publication:||Ear, Nose and Throat Journal|
|Article Type:||Brief Article|
|Date:||Aug 1, 2001|
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