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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2004.06.011 on March 15, 2004

Annals of Surgical Oncology 11:407-412 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Surgical Treatment of Thyroid Cancers With Concurrent Graves Disease

Tzu-Chieh Chao, MD, PhD, Jen-Der Lin, MD and Miin-Fu Chen, MD

From the Division of General Surgery, Department of Surgery (T-CC, M-FC), and Division of Metabolism and Endocrinology, Department of Internal Medicine (J-DL), Chang Gung University College of Medicine and Chang Gung Memorial Hospital, Taoyuan, Taiwan.

Correspondence: Address correspondence and reprint requests to: Tzu-Chieh Chao, MD, PhD, Department of Surgery, Chang Gung Memorial Hospital, 5 Fuhsing St., Kweishan, Taoyuan, Taiwan; Fax: 886-3328-5818; E-mail: tcchao{at}adm.cgmh.org.tw


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Thyroid cancers with concurrent Graves disease are relatively rare. Accordingly, the natural history and optimal surgical treatment of thyroid cancers with Graves disease are controversial.

Methods: Sixty-one thyroid cancers with concurrent Graves disease were retrospectively reviewed. Histopathologic diagnoses included 58 papillary thyroid carcinomas (95.1%), 1 follicular carcinoma (1.6%), 1 medullary carcinoma (1.6%), and 1 Hürthle cell carcinoma (1.6%).

Results: The sample included 54 females and seven males. Subjects’ ages ranged from 20 to 73 years (mean ± SD, 35.9 ± 10.6 years; median, 37 years). Average tumor size was 10.7 ± 15.9 mm (range, 1–70 mm). Forty-nine tumors (80.3%) were 10 mm or smaller. Surgical procedures included subtotal thyroidectomy (40 patients), total thyroidectomy (16 patients), total thyroidectomy plus neck dissection (2 patients), near-total thyroidectomy (1 patient), and lobectomy with contralateral subtotal lobectomy (1 patient). Thirty-seven patients (60.7%) underwent postoperative 131I ablation for thyroid remnant. Neck lymph node metastases occurred in three patients and lung metastases in two patients. Patients who developed metastases were younger and had significantly larger tumors and higher pretreatment serum T3 level than those who did not develop metastases. No deaths occurred during the 6.2 ± 4.1 year follow-up period (range, 1 year and 2 months to 18 years and 11 months).

Conclusions: Most thyroid cancers with concurrent Graves disease were 10 mm or smaller. Subtotal thyroidectomy is adequate for patients with Graves disease with concurrent carcinoma 10 mm or smaller.

Key Words: Carcinoma • Graves disease • Incidentaloma • Thyroid • Thyroidectomy • Thyrotoxicosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Thyroid cancers with concurrent Graves disease are relatively rare, occurring in 0.76% to 9.9% of glands removed in the treatment of Graves disease.1–8 Although the clinical behavior and management of papillary carcinoma and follicular carcinoma of the thyroid have been extensively studied during recent decades, controversy surrounds the natural history and optimal surgical treatment of thyroid cancer with Graves disease. Some investigators have reported an aggressive course for thyroid cancers associated with Graves disease.4,6,9,10 However, other investigators have found no evidence of aggression in the course of this condition.5,7,11,12 This discrepancy results partly from the relative rarity of the disease and the lack of a large data series. To better understand thyroid cancers concomitant with Graves disease, we retrospectively reviewed the data of patients with thyroid cancers with concurrent Graves disease. The present report presents clinical manifestations, treatment, outcome, and predictors of metastases.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
During the 18-year period of August 1983 to July 2001, a total of 1900 patients with primary thyroid cancers were treated at our institution. This sample included 1459 (76.8%) with papillary carcinomas, 265 (14.0%) with follicular carcinomas, 40 (2.1%) with medullary carcinomas, 80 (4.2%) with anaplastic carcinomas, and 56 (3.0%) with carcinomas of other histological types. During the same period, 3044 patients underwent thyroidectomy for Graves disease at our hospital. Graves disease was diagnosed by raised serum levels of triiodothyronine (T3) and thyroxine (T4), low thyroid-stimulating hormone (TSH) levels, presence of autoantibodies, and thyrotoxic clinical symptoms combined with histological features of diffuse hyperplasia of the thyroid gland.

Patients were treated with propylthiouracil, carbimazole, or methimazole before surgery. Moreover, patients also received Lugol solution for 7 to 10 days during the immediate preoperative period. The indications for surgery for patients with Graves disease included recurrent thyrotoxicosis; side effects of antithyroid medications; low likelihood of taking or inability to take medication; cold nodules within toxic glands on thyroid scanning; unusually large diffuse goiters; and malignancy or suspected cytological findings following fine-needle aspiration biopsy.

Sixty-one (2.0%) of 3112 patients with Graves disease had concurrent thyroid carcinoma. Thirty of these 61 patients were reviewed in our previous study.13 None of these patients had a history of previous neck irradiation or radioiodine therapy. Tumor size was the maximum dimension measured on pathological examination. In carcinomas with multiple foci, the maximum dimension of tumor foci was taken as the tumor size. Small tumors were defined as those 10 mm or smaller, whereas large tumors exceeded 10 mm.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The 61 thyroid cancers with concurrent Graves disease included the following histological types: 58 (95.1%), papillary thyroid carcinomas; 1 (1.6%), follicular carcinoma; 1 (1.6%), medullary carcinoma; and 1 (1.6%), Hürthle cell carcinoma. Thirty-one tumors (50.8%) were located in the right lobe, 19 (31.1%) in the left lobe, 2 (3.3%) in the isthmus, and 9 (14.8%) in both the right and left lobes. Table 1 lists the clinical characteristics of the thyroid cancer patients with concurrent Graves disease. Fifty-four of the patients were female and seven were male (female-to-male ratio, 7.7:1). The median age of the patients did not differ between the male and female groups (37 years vs. 36.0 years). However, the male patients had significantly larger median tumor size than the female patients (13.5 mm vs. 4.0 mm; Mann-Whitney U-test, P = .0485).


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  		TABLE 1. Clinical characteristics
 
Forty-nine patients (80.3%) had tumors 10 mm or smaller (small tumors) and 12 (19.7%) had tumors larger than 10 mm (large tumors). Forty-one patients (67.2%) had tumors incidentally found at surgery or by permanent section histological examination (incidentalomas) and 20 (32.8%) had clinically overt nodules. The data of the patients with small and large tumors were compared, revealing no difference between the two groups in terms of duration of thyrotoxic symptoms, serum levels of T3 and T4 before antithyroid medications, and 6-week postoperative serum thyroglobulin level. However, 6-week postoperative serum TSH level (median, 5.03 mIU/L) was significantly lower (P = .0271) in the small-tumor group than in the large-tumor group (median, 48.00 mIU/L). The patients with incidentalomas had symptoms of significantly shorter duration than did those with clinically overt nodules. Age, serum T3 and T4 levels before antithyroid medications, and postoperative serum thyroglobulin and TSH levels were not different between the two groups (Table 1).

Forty-two patients (68.9%) underwent technetium-99m (99mTc) sodium pertechnetate thyroid scanning before surgery, which revealed that 25 (59.5%) had toxic diffuse goiters, 10 (23.8%) had toxic diffuse goiters with a coexistent cold nodule, 6 (14.3%) had toxic multinodular goiters, and 1 (2.4%) had subacute thyroiditis. Thirty-three patients (54.1%) underwent preoperative thyroid ultrasonography with fine-needle aspiration cytology (FNAC) owing to the appearance of cold nodules on the thyroid scan or the presence of clinically palpable nodules.

FNAC revealed papillary carcinoma in three patients (9.1%) and revealed suspected malignancy in five (15.2%). Meanwhile, FNAC for the remaining patients yielded the following findings: 1 patient (3.0%), Hürthle cell tumor; 1 (3.0%), follicular neoplasm; 15 (45.5%), autoimmune thyroid diseases; and 8 (24.2%), benign thyroid lesions. That is, only 10 patients (30.3%) had FNAC findings indicating a need for surgical treatment. Twenty-one patients (34.4%) underwent intraoperative frozen-section examination for nodules. Frozen-section histology confirmed malignancy in 15 patients (71.4%) with papillary carcinoma and one (4.8%) with Hürthle cell carcinoma. Frozen-section analysis revealed no malignancy in the remaining five patients (23.8%).

Table 2 lists the surgical methods for thyroid cancer patients with concurrent Graves disease. Subtotal thyroidectomy was the most common surgical method, particularly for incidentalomas. Total thyroidectomy and near-total thyroidectomy were conducted following frozen-section diagnosis of malignancy. One patient with an incidentaloma and three with clinically overt tumors were initially treated by subtotal thyroidectomy followed by completion thyroidectomy after permanent section diagnosis of malignancy. Additionally, two patients who were initially treated by lobectomy and contralateral subtotal lobectomy on the basis of frozen section diagnoses of benign lesions declined subsequent completion thyroidectomy. Operative morbidity included transient hypoparathyroidism (one patient, 1.6%), permanent hypoparathyroidism (three patients, 4.9%), and transient recurrent laryngeal nerve palsy (two patients, 3.3%).


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  		TABLE 2. Operative methods
 
Thirty-seven patients (60.7%) underwent iodine-131 (131I) ablation of thyroid remnant 6 weeks following thyroidectomy. Among these patients, 18 (48.7%) were treated by subtotal thyroidectomy, 16 (43.2%) by total thyroidectomy, 1 (2.7%) by near-total thyroidectomy, and 2 (5.4%) by lobectomy and contralateral subtotal lobectomy. The dosage of 131I ranged from 1110 to 5550 MBq. These 37 patients also were given thyroxine supplement after 131I treatment.

The follow-up period ranged from 1 year and 2 months to 18 years and 11 months (median, 5.1 years; mean ± SD, 6.2 ± 4.1 years). No deaths occurred during follow-up. Five patients (8.2%) suffered metastases to the lungs or neck lymph nodes. Of these five patients, two patients with clinically overt nodules (one large papillary carcinoma and one small papillary carcinoma) had lung metastases 11 months and 2 years after near-total and total thyroidectomy. These two patients were treated with 3700 to 5550 MBq 131I and remained alive with persistent disease at final follow-up.

Two patients with incidentalomas had metastases to neck lymph nodes, at 11 months and at 2 years and 3 months after subtotal thyroidectomy. These two patients underwent neck dissection followed by either radioiodine treatment or external radiation and remained disease-free until final follow-up. Finally, one patient with large papillary carcinoma had neck lymph node metastases 11 months following total thyroidectomy. This patient declined repeat surgery for metastatic lymph nodes and subsequently was treated with radioiodine. This patient remained alive with the disease 4 years and 5 months after initial thyroidectomy.

Table 3 lists characteristics in patients with or without metastases. Patients with metastases were younger and had significantly larger tumors than did patients without metastases. Moreover, serum T3 levels before antithyroid medications in patients with metastases significantly exceeded those in patients without metastases. Age, premedication serum T4 level, and 6-week postoperative serum levels of thyroglobulin and TSH in patients with metastases did not differ between patients with and without metastases. Furthermore, postoperative 131I ablation and the extent of surgery were not associated with metastases.


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  		TABLE 3. Characteristics in thyroid cancer with and without metastases
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study revealed higher pretreatment serum T3 levels in patients who developed neck lymph node or lung metastases than in those without metastases. This finding is consistent with our previous work on thyroid cancers concomitant with Graves disease, toxic multinodular goiters, and toxic adenomas.13 The reason for higher pretreatment serum T3 levels in patients with metastases than in those without metastases is unclear and requires further study. The age of the patients in this study resembles that reported in the literature.5–7 However, this study showed that the patients with neck nodal or lung metastases were younger than those without metastases. This finding obviously differs from other reports of better outcomes for younger patients.14–16 However, because only five patients in the present study developed metastases, a larger series is necessary before any definite conclusions can be drawn.

Treatment options for Graves disease include antithyroid drugs, radioactive iodine therapy, and surgery.17–20 Although the policy for treating Graves disease varies markedly within and between different countries, the presence or otherwise of concomitant thyroid nodules might be considered when treatment is determined. In Graves disease, 10% to 17.1% of all nodules8,12,21 and 15.4% to 45.8% of scintigraphically cold nodules are malignant.4,9,12,22 Therefore, some investigators recommend surgical treatment for patients with Graves disease concomitant with nodules.9,18 However, nodules located deeply or in the context of a goiter often escape detection during physical examination by an experienced clinician.23 Nonpalpable nodules represent around 58.5% to 78.7% of the thyroid nodules identified by ultrasonography or thyroid scintigraphy in Graves disease.8,9,23,24

Accordingly, many authors recommend that patients with Graves disease should undergo examination of the thyroid gland not only by palpation but also by thyroid scintigraphy or ultrasonography.9,12,24–26 Thyroid scintigraphy revealed cold nodules in only 23.8% of the patients in the present study, a finding suggesting that nodules in Graves disease are rarely detected by this method. This suggestion is consistent with the literature reports that thyroid scintigraphy detects cold nodules in only 5.8% to 12.0% of cases of Graves disease.8,9,12 On the other hand, ultrasonography can detect nodules more frequently in Graves disease than can thyroid scintigraphy, with an incidence of 20.8% to 33.7%.8,24 FNAC is applied to differentiate benign from malignant nodules in Graves disease.24,27 However, this study did not show FNAC to be particularly useful for diagnosing malignancy in patients with Graves disease. The reason for this phenomenon is that the malignant nodules in Graves disease are generally small.5,6

FNAC is difficult for small nodules and carries the risk of hemorrhage in a Graves goiter. Additionally, the hyperplastic tissues associated with Graves disease may increase the cytological diagnosis of follicular neoplasm.12 Consequently, given the suggestion of an increased cancer risk in nodules concomitant with Graves disease, this study sets a low threshold for nodule referral for surgery, unless an expert cytologist concludes by means of FNAC that cancer is highly unlikely.

The extent of surgery for thyroid carcinoma concomitant with Graves disease has rarely been discussed. Some researchers have reported that thyroid cancers associated with Graves disease behave aggressively, with a tendency toward a high frequency of lymph node metastases, found both at surgery and as a cause of recurrent locoregional disease.4,6,9,10 Accordingly, total, near-total,10 or subtotal thyroidectomy9 plus central neck dissection was recommended for treating this disease. In contrast, most of the present group of patients underwent subtotal thyroidectomy, and, moreover, it was observed that the extent of thyroidectomy did not influence the incidence of metastases. In the present study, although three small tumors developed metastases, the median size of tumors developing metastases was larger than that of tumors that did not develop metastases (Table 3). The measured results are consistent with reports of others that, in Graves disease, larger thyroid cancers are more aggressive4,10 and smaller tumors have a more favorable prognosis.10

Most carcinomas associated with Graves disease in the present study and in the literature5,6,10 are small and found incidentally during postoperative pathological examination of the thyroid or during surgery. Noguchi et al.28 showed that carcinomas smaller than 10 mm concomitant with Graves disease can be treated by subtotal thyroidectomy with excellent outcomes. Similar results also have been noted in euthyroid patients. Although some authors have reported that thyroid papillary carcinomas 10 mm or smaller may follow an aggressive course,29,30 most researchers have found that most small thyroid carcinomas have an excellent prognosis and can be treated with surgery less extensive than total or near-total thyroidectomy.28,31–36

Ablation of thyroid remnant with 131I is generally performed in euthyroid patients with well differentiated thyroid carcinomas following total or near-total thyroidectomy,37,38 in response to the finding of a significant reduction in recurrence and cancer-related deaths in patients treated with 131I therapy.14,39 There have been few reports of postoperative 131I ablation for thyroid carcinomas concomitant with Graves disease.5,7 Most carcinomas in Graves disease are small tumors that were found incidentally following surgery. Patients with thyroid carcinomas concomitant with Graves disease are usually treated by subtotal thyroidectomy for Graves disease.

Accordingly, a key question is whether these patients should undergo 131I ablation following subtotal thyroidectomy or whether they should undergo other less extensive procedures. The present study found that 131I ablation of thyroid remnant did not influence the incidence of metastases. A recent study of 867 patients with thyroid carcinomas smaller than 10 mm included 541 patients (62.4%), including 414 with Graves disease, treated by subtotal thyroidectomy.28 Postoperative 131I ablation was not administered to these patients in the absence of metastases, and the sample group had a high recurrence-free survival rate. Similar findings were observed in euthyroid patients with papillary microcarcinoma of the thyroid.28,36,40,41 Consequently, routine 131I ablation is not necessary in patients with Graves disease with small thyroid carcinoma.

In conclusion, most thyroid cancers with concurrent Graves disease were 10 mm or smaller. Patients who developed metastases were younger and had larger tumors and higher pretreatment serum concentration of T3 than those who did not develop metastases. Cold nodules on thyroid scan suggest the possibility of thyroid carcinomas in Graves goiter, and these need to be treated surgically. Subtotal thyroidectomy is adequate for patients with Graves disease with concurrent carcinoma 10 mm or smaller. Moreover, postoperative 131I ablation of thyroid remnant generally is unnecessary for patients with small tumors.


   FOOTNOTES
 
Most thyroid cancers with concurrent Graves disease were 10 mm or smaller. Subtotal thyroidectomy is adequate for patients with Graves disease and concurrent carcinoma 10 mm or smaller.

Received for publication June 18, 2003. Accepted for publication December 21, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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