Changing the operative strategy for thyroid cancer by node sampling

Changing the operative strategy for thyroid cancer by node sampling

Changing the Operative Strategy for Thyroid Cancer By Node Sampling Irving B. Rosen, MD, Toronto, Ontario, Canada Andrew Maitland, MB, Toronto, Ontar...

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Changing the Operative Strategy for Thyroid Cancer By Node Sampling

Irving B. Rosen, MD, Toronto, Ontario, Canada Andrew Maitland, MB, Toronto, Ontario, Canada

The advent of radioiodine therapy for hyperthyroidism made thyroid surgery progressively infrequent. The resultant conservatism was reinforced by the perception of thyroid cancer as infrequent and biologically unimportant where excisional treatment could be casual and limited with the invariable expectation of long-term survival and cure. Perhaps more than any other worker in this field, Crile [I] exerted a great moderating influence on the extent of surgery for thyroid cancer. Current strategy consists of an appropriate thyroidectomy (the extent of which has not been standardized) and a nodal dissection for obvious proven metastatic thyroid cancer of cervical lymph nodes. Although the outcome of treatment for thyroid cancer usually is successful (a pleasant contrast to malignancies elsewhere), the experienced observer invariably encounters instances where thyroid cancer demonstrates its more aggressive and lethal behavior. To scrutinize the completeness of cancer clearance using commonly accepted guidelines for surgical treatment of thyroid cancer, a retrospective study of our recent experience was carried out. Material and Methods In a 2 year period (from 1979 to 1981), 150 patients, 124 of whom were women and 26 men, who ranged from 30 to 72 years of age, underwent thyroid surgical procedures primarily to exclude malignant disease. All patients had undergone clinical assessment, thyroid scintiscanning, needle aspiration biopsy, routine thyroid function tests, and thyroid antibody estimation. Patients selected for surgical treatment had fulfilled one or more of the following criteria: (1) presence of clinical cancer, (2) positive or cellular cytologic findings by needle aspiration, (3) presence of a solitary cold nodule on scintiscan, (4) persistence of nodular irregularity after prolonged thyroid feeding, (5) history of radiation exposure. The standard operative procedure for a lateralized lesion consisted of total ipsilateral lobectomy and a subtotal lobectomy of the contralateral side. A near-total thyroidectomy was carried out for From the Department of Surgery, University of Toronto, Toronto, Ontario. Reauests for reprints should be addressed to Irving 6. Rosen, MD, 600 Univeisity Avenue, Suite 445, Toronto, Ontario, M5G 1X5, Canada. Presented at the 29th Annual Meeting of the Society of Head and Neck Surgeons, New Orleans, Louisiana, May 4-7, 1963.

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malignant disease or thyroid nodular disease occuring after radiation exposure, which comprised six patients or 13 percent of the series. In the cancer cases, a search was made for metastatic cancer to cervical lymph nodes of the neck. If present, it was managed by a modified neck dissection in which the thyroidectomy incision was extended laterally and a skin flap was mobilized to the upper neck. The nodal mass was then dissected out from the neck, preserving the internal jugular vein, the spinal accessory nerve, and the sternomastoid muscle which was mobilized and retracted or, on occasion, transected through its clavicular head and subsequently resutured. The submandibular triangle, unless involved, was not dissected. The wound was then closed without tracheostomy and healed with the use of suction catheter drainage (Figure 1). In cancer patients without apparent nodal involvement of Delphian regional superior mediastinal areas, a node sampling procedure of the ipsilateral lower internal jugular node chain was carried out without extending the thyroidectomy incision. The strap muscles and sternomastoid muscle were mobilized and retracted superiorally. The carotid sheath was identified. Dissection of areolar tissue and sternomastoid muscle from off the internal jugular vein was carried out gently. The internal jugular vein was identified, and a right angle retractor was inserted along its posterior border, retracting the entire carotid sheath centrally. In the absence of any obvious node, the node bearing fatty tissue was locally excised taking care not to injure the underlying phrenic nerve. Hemostasis was obtained, and the fatty tissue was then submitted for both quick and paraffin sections. Three to seven nodes were usually seen on microscopic examination. The presence of metastatic cancer in the jugular nodes was usually followed by a modified neck dissection as described.

Results Of the 150 patients who underwent thyroidectomy, 48 were found to have cancer (incidence 32 percent), including 40 women and 8 men who ranged in age from 21 to 72 years. Of the remaining 102 patients, 72 adenomas were demonstrated, which yielded 120 tumors, or a 80 percent neoplasia rate, for our entire experience. Four false-negative needle biopsy results were recorded for a 2.5 percent false-negative rate for the entire patient study group. There was also one false-positive result for a less than 1 percent rate for

The American Journal of Surgery

Operative

Strategy

for Thyroid

Cancer

Figure 7. Left, usual operative field of modified neck dissection with preservation of infemal]uguiar vein, sternomastoid muscle, and spinal accessory nerve thtwgh extension of the thyroidectomy incision (courtesy of J. Palmer). Right, appearance of patient with modified neck dissection.

the entire 150 patients. This gave us a sensitivity of 97 percent, a specificity of 97 percent, and an accuracy of 96 percent. Histologic malignancies included papillary cancer in 12, patients, mixed papillar-follicular cancer in 12, follicular cancer in 14, medullary cancer in 5, Hurthle cell tumors in 4, and anaplastic cancer in one. In the 48 cancer patients, there were 3 associated hyperfunctioning parathyroid adenomas which were adequately treated. In 8 of 48 cancer patients or 16 percent of the group, obvious clinical or macroscopic nodal enlargement at the time of operation was identified and verified, and a modified neck dissection was then carried out. Of the remaining 40 cancer patients with a clinically negative neck, 6 did not undergo node sampling because of false-negative pathologic findings at quick section examination. Thus, 12 percent of the pathologic findings were false-negative for the cancer group and 4 percent were false-negative for the entire patient study. There was one additional cancer patient in whom it was thought that node sampling was precluded because of infirmity. Of the remaining 33 patients, node sampling of the internal jugular vein was performed and showed 12 patients with microscopic metastatic thyroid cancer. This gave a 36 percent yield of occult metastatic cancer for the 33 patients studied, and a 36 percent yield for the 33 patients who had apparent negative necks. The results from the node sampling more than doubled

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the yield of metastatic thyroid cancer from 8 of 48 cancer patients (16 percent of the group) to 20 of 48 for a 42 percent incidence of nodal metastases (Table I). Of further anecdotal interest is the history of one patient who presented, a decade after undergoing hemithyroidectomy for cancer, with recurrent disease at the stump site. He subsequently underwent completion thyroidectomy and node sampling which was positive and which lead to nodal dissection. Palpation was only carried out on the original side and was thought to reveal no abnormalities; however, that determination was shown to be fallacious by the emergence of clinical neck cancer on the original side 6 months after dissection.

TABLE I

Cancer Incidence in 150 Patients Who Underwent Thyroidectomy n

%

481150

32

Nodal metastases Macroscopic Microscopic (sampling)

8148 12133

16 36

Total

20148

42

Thyroidectomy

l

Number and percent of patients in whom metastatic thyroid cancer was detected due to macroscopic and microscopic examination. l

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There was no operative mortality, hypoparathyroidism, or accidental injury of the recurrent laryngeal nerve, phrenic nerve or spinal accessory nerve. One recurrent laryngeal nerve involved by cancer was deliberately sacrificed. One postoperative neck recurrence of medullary carcinoma was recognized 8 months after surgery and was treated with wide local excision and postoperative radiation. Apparent control was achieved 18 months after the second operation. There has been no evidence of systemic cancer or death due to malignancy. All patients were placed on thyroid suppressive feeding. Twenty patients (42 percent) received radioiodine ablation of residual thyroid neck tissue detected on postoperative scintiscanning, and 7 (14 percent) received external radiation for what was conceived to be extrathyroidal spread, usually involving strap muscle. Four of the 12 positive nodal samples showed additional tumor at neck dissection (Figure 2). Comments The thyroid gland enjoys a rich lymphatic system [2,3] verified by early anatomists. The rich capillary network that encircles the follicles makes its way to a position below the capsule of the gland giving rise to collecting trunks. These collecting trunks are closely associated with the blood supply to the gland. Six collecting trunks are usually identified, although a variation is seen. Main lymphatic trunks run in superior, lateral, and inferior directions and follow the branches of the blood supply. Superior pathways drain the anterior and posterior portions of the thyroid, including the isthmus, and continue to the superior subdigastric nodes. The posterior portion of the upper lobe terminates in the superior and anterior internal jugular nodes. The lateral pathways drain frequently into the inferior lateral nodes of the internal jugular chain and usually come from the lateral lower half of the lobe, the inferior pathway draining the lower portion of the isthmus and the medial and posterior lower half of the lobe and the inferior pole going into the pretracheal and paratracheal lymph nodes, as well as the recurrent laryngeal chain of nodes. Free communication of retropharyngeal and retroesophageal nodes with the recurrent and paratracheal nodes is frequently demonstrated [2]. In a study of the distribution of positive nodes in 111 specimens from patients with thyroid cancer, Feind [2] noted that the majority of positive nodes can be seen in the midjugular and lower jugular sites. Five hundred thirteen positive nodes of a total of 778 demonstrated throughout the affected necks, were in the mid and lower jugular positions. The recognition of the frequency of occult metastatic nodal disease in thyroid cancer is well established. Attie et al [4], advocated elective neck dis-

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section in treatment of papillary carcinoma of the thyroid. Of 212 patients without palpable lymph nodes, 115 were selected for elective neck dissection of whom 79 (68.7 percent) demonstrated metastatic cancer. Since histologic study of the specimen was considered to be routine without the node clearing technique, it was presumed that a higher incidence of metastatic involvement was likely. In no patient who had this form of treatment did neck recurrence or death due to cancer develop. Attie et al [4] cited other surgeons in their paper who had observed the occurrence of positive neck disease as a result of elective neck dissection for thyroid cancer in a range of from 21 to 82 percent of patients. Block et al [5] has noted that “the presence of palpable cervical lymph nodes preoperatively nearly always indicates the presence of metastasis from an existing thyroid cancer but absence of clinically palpable cervical nodes does not preclude the existence of metastasis.” He also reported that 54 percent of patients undergoing elective cervical node dissection were found to have microscopic evidence of metastasis to nodes. Feind [2] indicated that “only when one cleans out the area from hyoid bone to the thoracic inlet and laterally to include the jugular chain can the pathologist ascertain the extent of lymphatic spread,” noting that in every case where a positive periglandular node biopsy indicates lateral spread, metastatic tumor was found in neck dissection specimens. Cody and Shah [6], in dealing with locally invasive thyroid cancer, recommended that elective neck dissection be considered in patients with this type of malignant disease since the incidence of nodal metastases is high. They further reported a good experience with the operative management of occult metastatic cancer and recorded the development of clinical metastatic disease in 50 percent of their observedonly group. Although the prevalence of occult disease seems unquestioned, its biologic implication remains unclarified. Cady [7] has indicated that metastatic lymph nodes are currently a greater cause of failure in low-risk thyroid cancer patients as a result of conservative surgery but without an adverse influence on survival. Although neck metastases were less frequently found in his older high-risk group, Cady found that this disease was more life threatening in these patients than in younger patients. Mazzaferri and Young [B] noted that the cancer recurrence rate was twice as high in patients initially observed to have cervical lymph node metastases and even fivefold greater in patients over 4p years of age, but that survival did not appear to be adversely affected. They further found that the extent of lymph node surgery did not appear important to survival and advocated simple excision of metastatic cervical nodes at the time of initial surgery. Simpson and Carruthers [9] described their experience with 137 patients with

The American Journal of Surgery

Operative Strategy for Thyroid Cancer

low-grade thyroid cancer, referred usually for radiation therapy management after primary treatment, Thirty-eight of these patients eventually died from disease and 28 patients with papillary tumors and 31 with follicular tumors presented with infiltrating neck masses, distant metastasis, or both as evidence of advanced disease. Occult but widespread nodal involvement by metastatic thyroid cancer is well recognized in the established literature [4,6,7], but survival appears unaffected by nodal involvement or the extent of its treatment [6,7]. Other workers have advanced evidence indicating that nodal disease can be a serious factor in survival [2,4,7-g]. Elective neck dissection in the treatment of thyroid cancer [4] has never been accepted as standard therapy which may reflect the legitimate medical and legal concerns of any postoperative problem in a negative neck, the widely observed unaggressive nature of thyroid cancer, even in its nodal metastatic form, and the general disrepute of elective neck dissection and its debatable influence on survival. However, the idea of ignoring residual cancer which may, for the infrequent individual, be pertinent to survival or well-being seems unpalatable. In our view, it appears that the optimal treatment for thyroid cancer should not only consist of a near-total thyroidectomy, but in the presence of apparent negative nodal involvement of central or lateral regions of the neck, a bilateral lower internal jugular node chain sampling should be carried out as described in this paper. If positive, it provides a rational basis for selecting patients for a modified neck dissection which can be carried out with low morbidity and no mortality, and provides a good cosmetic and functional result and a reasonable method of cancer clearance. Jugular node sampling, permitting the intelligent use of modified neck dissection, increased the yield of metastatic cancer in our experience from 16 to 42 percent, thus permitting us to afford the patients surgical treatment in one hospitalization while preventing the emergence of future malignant disease in at least some patients and providing the possibility of complete cancer clearance. In view of the relative freedom from significant morbidity, node sampling seems to be eminently sensible. Summary One hundred fifty patients underwent thyroid surgery from 1979 to 1981, of whom 48 showed cancer for a 32 percent rate. In eight patients (16 percent), obvious clinical nodal disease was treated with modified neck dissection. Of the remaining 40 patients, internal jugular node sampling was carried out in 33, and revealed microscopic metastatic cancer in 12 patients who then underwent appropriate neck dissection. Node sampling increased our yield of nodal metastases from 16 to 42 percent, permitted

Volume 146, October 1963

Figure 2. Low-power (top) and high-power (middle) nodal samfMngs of occult nodal metastasis in a 35 year old woman wfth a contralateral neck mass stmulatlng a carotid body tumor. Bottom, primarylesion of occult primary thyroid cancer. Furt&r malignancy detected in superior jugular nodes at neck dissection (courtesy of the Department of Pathology, h4t. Slnai Hospital, Toronto.). (Rfagnlrrcat/ons X 700, reduced by 64 percent.)

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one-hospitalization treatment, and afforded our patients the possibility of complete cancer control and prevention of the emergence of future recurrent disease. It is recommended that node sampling be incorporated into the operative strategy for thyroid cancer to permit intelligent selection of patients for modified neck dissection.

References 1. Crile G Jr. Treatment of patients after exposure to radiation of the thyroid. In: Degroot L, Frohman L, Kaplan E, Refetoff S, eds. Radiation associated thyroid carcinoma. New York: tine and Stratton, 1976:409- 11. 2. Feind C. The head and neck. In: Haagensen C, Feind C, Herter F, Slanetz C, Weinberg G, eds. The lymphatics in cancer.

Toronto: WB Saunders, 1972; 174-64. 3. Clark R, Cole W, Fuller L, et al. Thyroid. In: Maccomb WS, Fletcher GH, eds. Cancer of the head and neck. Baltimore: Williams and Wilkins, 1967:293-329. 4. Attie J, Khafif R, Steckler R. Elective neck dissection in papillary carcinoma of the thyroid. Am J Surg 1971;122:464-72. 5. Block M, Miller M, Horn R. Thyroid carcinoma with cervical lymph node metastases effectiveness of total thyroidectomy and node dissection. Am J Surg 1971;122:456-64. 6. Cody HS Ill, Shah J. Locally invasive well differentiated thyroid cancer. Am J Surg 1961;142:460-3. 7. Cady B. Surgery of thyroid cancer. World J Surg 1961;5:315. 6. Mazzaferri E,Young R. Papillary thyroid carcinoma. A ten year follow-up report of the impact of therapy in five-hundred and seventy-six patients. Am J Med 1961;70:511-7. 9. Simpson J, Carruthers J. Their role of external radiation in the management of papillary follicular thyroid cancer. Am J Surg 1976;136:457-61.

See page 537 for a corresponding

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