Evaluation of thyroid isthmusectomy as a potential treatment for papillary thyroid carcinoma limited to the isthmus: A clinical study of 73 patients

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1 ORIGINAL ARTICLE Evaluation of thyroid isthmusectomy as a potential treatment for papillary thyroid carcinoma limited to the isthmus: A clinical study of 73 patients Jianbiao Wang, MM, 1 Haili Sun, BM, 2 Li Gao, MD, 1 Lei Xie, PhD, 1 Xiujun Cai, MD, PhD 3 * 1 Department of Head and Neck Surgery, Institute of Micro-Invasive Surgery of Zhejiang University, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China, 2 Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China, 3 Department of General Surgery, Institute of Micro-Invasive Surgery of Zhejiang University, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China. Accepted 13 September 2015 Published online 11 November 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. There are no specific therapeutic guidelines for thyroid cancers confined to the isthmus. To determine whether isthmic papillary thyroid carcinoma (PTC) can be treated with thyroid isthmusectomy and limited neck dissection, we analyzed factors related to central lymph node (CLN) metastasis in patients with clinically nodenegative (cn0), solitary, isthmic PTC. Methods. We retrospectively reviewed 73 consecutive patients who underwent surgery for solitary isthmic, PTC. The frequency, pattern, and risk factors of CLN metastasis were analyzed. Results. Occult CLN metastasis and paratracheal lymph node (PTLN) metastasis were detected in 34 patients (46.6%) and 28 patients (38.4%), respectively. On multivariate logistic regression analysis, male sex and tumor size >0.7 cm were associated with CLN metastasis, and age 38 years, tumor size >0.6 cm, and pretracheal lymph node positivity were associated with PTLN metastasis. Conclusion. Thyroid isthmusectomy for solitary isthmic PTC may be insufficient in patients with tumors >0.6 cm, those aged 38 years, and male patients. VC 2015 Wiley Periodicals, Inc. Head Neck 38: E1510 E1514, 2016 KEY WORDS: papillary thyroid carcinoma, thyroid isthmus, central lymph node metastasis, thyroid isthmusectomy, risk factor *Corresponding author: X. Cai, Department of General Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, #3 East Qingchun Road, Hangzhou , China. cxjzju@sina.com Contract grant sponsor: This research was supported by grant no from the Health and Family Planning Commission of Zhejiang Province. INTRODUCTION Although the majority of thyroid nodules involve the thyroid lobes, a small minority are limited to the thyroid isthmus. Currently, there is no specific guideline for the management of thyroid cancers confined to the isthmus. A few authors have suggested that thyroid isthmusectomy alone or with limited neck dissection (including precricoid and pretracheal lymph node dissection) may be sufficient for the treatment of patients with papillary thyroid carcinoma (PTC) limited to the thyroid isthmus. 1,2 However, PTC has a propensity for regional lymphatic spread, and most frequently involves the central neck lymph nodes. 3 Subclinical nodal metastasis is found in a high proportion of patients with PTC at the time of surgery and in a high proportion of pathology specimens. 4,5 Furthermore, limited published data are available about the frequency and pattern of the nodal metastasis of solitary PTCs limited to the thyroid isthmus. Excision of the isthmus alone or combined with precricoid and pretracheal lymph node dissection for isthmic PTC may be insufficient, as this procedure retains the paratracheal lymph nodes (PTLNs), which are often involved in PTC. Therefore, in this study, we investigated the frequency, pattern, and predictive factors of occult central neck lymph node metastasis in clinically node-negative (cn0) patients with solitary PTC limited to the isthmus, and discuss appropriate surgical strategies for solitary isthmic PTC. PATIENTS AND METHODS Patients We conducted a retrospective analysis of prospectively collected data from the Head and Neck Surgery Department of Sir Run Run Shaw Hospital, Medical School of Zhejiang University. The study cohort was composed of 73 consecutive cn0 patients who had primary solitary isthmic PTC and were scheduled to undergo initial surgery between January 2006 and December This study was approved by the ethics committee of Sir Run Run Shaw Hospital, Medical School of Zhejiang University. Written informed consent was obtained from all patients before the study. The patients included in the study met the following criteria: solitary PTC limited to the median portion of the thyroid isthmus; clinically node-negative neck; no history of thyroid surgery; and availability of an adequate medical history. Patients found to have an incidental minute PTC limited to a thyroid lobe on frozensection or paraffin-section examinations and patients E1510 HEAD & NECK DOI /HED APRIL 2016

2 CENTRAL LYMPH NODE METASTASIS IN SOLITARY ISTHMIC PTC who underwent therapeutic neck dissection for clinically positive nodes in the lateral or central neck compartments were excluded. A clinically node-negative neck was defined as a neck with no palpable central lymph nodes (CLNs) and no suspicious metastatic nodes on imaging studies, such as ultrasonography and CT. Detailed preoperative evaluations were performed in each patient. The thyroid and the CLN and lateral neck lymph nodes were examined using ultrasonography and CT. Ultrasound-guided fine-needle aspiration was performed to confirm if the lesion was malignant or metastatic. Vocal cord function was assessed using direct or indirect laryngoscopy. In addition, the levels of thyroid hormones, parathyroid hormone, calcitonin, serum calcium, etc., were also measured. All patients underwent total thyroidectomy plus bilateral prophylactic central neck dissection (CND). Surgical approach for central neck dissection All operations were performed by the same panel of senior surgeons. Thyroidectomy was performed using a standard technique of fine capsular dissection. The recurrent laryngeal nerves (RLNs) and all parathyroid glands were routinely identified and preserved under direct vision. The blood supply of the parathyroid glands was confirmed using the fine-needle pricking test. Any devascularized parathyroid gland was excised in a piecemeal fashion and autotransplanted in the sternocleidomastoid muscle. The extent of CND specified in the American Thyroid Association guidelines was followed strictly. Bilateral CND included removal of the prelaryngeal, pretracheal, and both the right and left paratracheal nodal basins. 6 Follow-up All patients received thyroid-stimulating hormone-suppressive therapy after surgery. Postsurgical physical examinations were performed every 3 to 6 months. Radioactive iodine therapy was administered to patients who were found to have lymph node metastasis. During a follow-up of 24 to 96 month, all patients underwent ultrasonography of the neck. The levels of thyroglobulin and thyroglobulin antibody were routinely measured. A CT scan or an fine-needle aspiration was performed to evaluate suspected recurrences in the thyroid bed and lateral neck. Locoregional recurrence was diagnosed using ultrasonography or CT plus cytological examination when necessary. Clinicopathologic factors Clinicopathologic factors that could be associated with central or PTLN metastases were prospectively documented. They included the following: sex; age; concomitant thyroid diseases; maximum tumor size; extrathyroidal extension; and lymph node metastases in the prelaryngeal and pretracheal regions. Extrathyroidal extension was evaluated based on intraoperative findings or paraffin biopsy examination. Statistical analysis Statistical analyses were performed using SPSS version 16.0 (SPSS, Chicago, IL). The results were expressed as mean 6 SD. The statistical analyses were performed using the t test, chi-square test, or Mann Whitney U test, as appropriate. A receiver operating characteristic (ROC) curve analysis was used to identify the cutoff points of tumor size and patient age for defining the risk of CLN metastasis and PTLN metastasis. The odds ratio (OR) and 95% confidence interval (CI) of the association of each variable with lymph node metastasis (present or absent) were calculated using binary logistic regression. Any p <.05 was considered statistically significant. RESULTS Patient characteristics Between January 2006 and December 2012, a total of 3557 patients underwent primary treatment for PTC at our hospital. Of these patients, 86 (2.4%) were diagnosed with solitary PTC located in the median portion of the isthmus on preoperative ultrasonography, although 3 patients were excluded because of positive nodes in the central compartment, and 10 patients were excluded because a minute PTC was found in the body of the thyroid lobe on paraffin biopsy examination. Thus, a total of 73 patients (2.1%) who met the selection criteria were included in the study. The study patients consisted of 19 men and 54 women, with a mean age of 43.6 years (range, years) at the time of diagnosis. All patients were diagnosed with solitary PTC on paraffin biopsy examination after the surgery. Concomitant Hashimoto thyroiditis was found in 8 patients. All patients underwent total thyroidectomy plus bilateral prophylactic CND. None of the patients had received head and neck radiation before the surgery, and no patient had distant metastasis. The characteristics of the patients have been listed in Table 1. Frequency and distribution of central lymph node metastasis in clinically node-negative patients with solitary isthmic papillary thyroid carcinoma On postoperative pathology examination, 46.6% of all patients (34 of 73) had lymph node metastasis in the central neck compartment. The pretracheal, left paratracheal, and right PTLNs had similar positivity rates (26.0%, 27.4%, and 24.7%, respectively), whereas the prelaryngeal lymph nodes were the least likely to be involved (13.7%; Table 2). The prelaryngeal and pretracheal lymph nodes can easily be dissected during thyroid isthmusectomy without exploration of the tracheoesophageal groove; in contrast, bilateral PTLN dissection is more complicated and hazardous owing to the risk of injury to the RLN and parathyroid glands. We therefore determined the frequency of PTLN metastasis among patients with solitary isthmic PTC, and found that this rate was 38.4% (28 of 73). Prelaryngeal or pretracheal lymph node metastasis was encountered in 24 patients (32.9%; 24 of 73). HEAD & NECK DOI /HED APRIL 2016 E1511

3 WANG ET AL. TABLE 1. Clinicopathologic factors associated with central lymph node metastasis. Parameter Total (n 5 73) CLN metastasis1 (n 5 34) CLN metastasis- (n 5 39) p value Sex Male 19 (26.0%) 13 (38.2%) 6 (15.4%).026 Female 54 (74.0%) 21 (61.8%) 33 (84.6%) Age, y, mean 6 SD Concomitant thyroid disease Hashimoto thyroiditis 8 (11.0%) 3 (8.8%) 5 (12.8%).586 Absent 65 (89.0%) 31 (91.2%) 34 (87.2%) Primary tumor size, cm, mean 6 SD Extrathyroidal extension Present 8 (11.0%) 6 (17.6%) 2 (5.1%).088 Absent 65 (89.0%) 28 (82.4%) 37 (94.9%) Abbreviations: 1, positive; -, negative; CLN, central lymph node. Any p <.05 indicates statistically significant differences between the CLN1 group and the CLN- group. Risk factors for central lymph node metastasis in clinically node-negative patients with solitary isthmic papillary thyroid carcinoma We used ROC curve analysis to determine the cutoff point of primary tumor size ( cm) for predicting CLN metastasis. The analysis showed that a tumor size of 0.75 cm was the cutoff point for predicting CLN metastasis. However, on univariate logistic regression, a tumor size >0.80 cm was not significantly associated with CLN metastasis, whereas a size >0.70 cm was significantly associated with CLN metastasis. Among the other variables, only male sex was significantly associated with CLN metastasis on univariate logistic regression. Factors, such as young age (45 years), extrathyroidal extension, and concomitant Hashimoto thyroiditis, had no significant influence on CLN status. Multivariate logistic regression analysis confirmed that male sex and a primary tumor size >0.7 cm significantly predicted CLN metastasis (Table 3). Risk factors of paratracheal lymph node metastasis in clinically node-negative patients with solitary isthmic papillary thyroid carcinoma ROC curve analysis showed that the cutoff point of primary tumor size (range, cm) for predicting PTLN metastasis was cm. However, on univariate logistic regression, a tumor size >0.60 cm was significantly associated with PTLN metastasis, whereas a size >0.50 cm was not. PTLN metastasis is more likely among young patients. However, young age (45 years) was not significantly associated with PTLN metastasis on univariate logistic regression (data not shown). We therefore used ROC curve analysis to determine the cutoff age for predicting PTLN metastasis (range, years), and found that the cutoff age was 38.5 years. Age 38 years and <39 years were both significantly associated with PTLN metastasis on univariate logistic regression, but the former had a higher OR and 95% CI and a p value <.01. We therefore analyzed the risk of PTLN metastasis in patients aged 38 years, and found that this parameter was a statistically significant predictor of PTLN metastasis (Table 4). The results of the logistic regression for age <39 years are not shown. Other variables, such as male sex, prelaryngeal lymph node metastasis, and pretracheal lymph node metastasis, were also significantly associated with PTLN metastasis on univariate logistic regression. Conversely, factors, such as extrathyroidal extension and concomitant Hashimoto thyroiditis, had no significant influence on PTLN status. Of all the factors found to be significant on univariate analysis, young age (38 years), tumor size >0.6 cm, and positive pretracheal lymph nodes were confirmed to be significant predictors of PTLN metastasis on multivariate logistic regression analysis (Table 4). Surgical complications and follow-up Among the 73 patients, 3 (4.1%) developed transient hypoparathyroidism; no patient developed permanent hypoparathyroidism. RLN injury did not occur in any patient. During a follow-up period of 24 to 96 months, there were no cases of tumor recurrence or persistence. TABLE 2. Patterns and distribution of cervical lymph node metastasis in solitary isthmic papillary thyroid carcinoma. CLN Prelaryngeal Pretracheal Left paratracheal Right paratracheal No. of resected nodes, mean (95% CI) ( ) 1.19 ( ) 3.48 ( ) 4.18 ( ) 5.40 ( ) No. of positive nodes, mean (95% CI) 1.66 ( ) 0.19 ( ) 0.52 ( ) 0.58 ( ) 0.37 ( ) Overall lymph node metastasis, no. of patients (%) 34 (46.6) 10 (13.7) 19 (26.0) 20 (27.4) 18 (24.7) Abbreviations: CLN, central lymph node; 95% CI, 95% confidence interval. E1512 HEAD & NECK DOI /HED APRIL 2016

4 CENTRAL LYMPH NODE METASTASIS IN SOLITARY ISTHMIC PTC TABLE 3. Univariate and multivariate logistic regression for central lymph node metastasis in solitary isthmic papillary thyroid carcinoma. Independent variables Univariate Multivariate OR (95% CI) p value OR (95% CI) p value Sex, male vs female ( ) ( ).038 Age, 45 vs > ( ) ( ).610 Size, >0.7 vs 0.7 cm ( ) ( ).003 Extrathyroidal extension, positive vs negative ( ) ( ).098 Concomitant thyroid disease, thyroiditis vs absent ( ) ( ).489 Abbreviations: OR, odds ratio; 95% CI, 95% confidence interval. DISCUSSION Between 2006 and 2012, we treated 3557 patients with PTC in our hospital, of whom 73 (2.1%) were histologically diagnosed with solitary PTC limited to the thyroid isthmus, which is similar to previously reported value of 2.5%. 2 Lee et al 7 reported a higher frequency of isthmic PTC (9.2%), but their study included patients with multifocal tumors; the frequency of solitary isthmic PTCs was 4.7% in their study. Only 2 studies 7,8 have examined CLN metastasis in isthmic PTC; however, they did not separately analyze the risk factors for CLN metastasis and PTLN metastasis. One of these 2 studies had a small sample size (45 patients, including 35 patients with non-median isthmic tumors), and the other study included patients with multifocal tumors (48.6%) and patients who underwent only unilateral CND. Both studies enrolled heterogeneous populations, including patients who underwent prophylactic and therapeutic dissection of the central as well as lateral compartment. Our study had a homogenous population of patients with solitary PTC in the median portion of the isthmus and cn0 necks, all of whom were treated with total thyroidectomy plus bilateral prophylactic CND. The prevalence of occult CLN metastasis in our population was 46.6%, which is as high as the reported prevalence of PTCs located in the thyroid lobes (30% to 65%). 9,10 Song et al 8 reported a higher frequency (71.1%) rate of CLN metastasis among 45 patients with solitary, isthmic PTC, possibly because their study included 32 patients with cn1 disease and 35 patients with non-median isthmic tumors. The occult CLN metastasis rate reported by Song et al 8 was 52.2%, which is similar to our result. We also evaluated the CLN metastasis distribution at different sites in the neck. We found that the pretracheal and paratracheal nodes were most likely to be affected in patients with solitary isthmic PTC, with involvement rates of 26.0% and 38.4%, respectively. This finding is consistent with that reported by Song et al. 8 A possible explanation for this finding is that isthmic tumors are located in the connection between the 2 thyroid lobes, and more easily drain to the inferiorly located pretracheal and PTLNs, and subsequently to the inferior jugular lymphatics and superior mediastinal lymphatics, than to the superiorly located prelaryngeal lymph nodes. The role of CND in preventing the nodal recurrence of PTC has been an ongoing debate. 11 Residual metastatic nodes, after initial insufficient CND, are the most common cause of recurrence in PTC. 12 Thus, a thorough resection of the lymphatic tissue in the central compartment may reduce the risks of recurrent or persistent disease by eliminating residual subclinical lymph node metastasis. However, PTC located in the isthmus is a special situation, because the thyroid isthmus is located above the trachea, and can be easily excised without exploring the tracheoesophageal groove. Although there are recommendations for the treatment of differentiated thyroid carcinoma, there are no specific guidelines for the management of thyroid cancers confined to the thyroid isthmus. 13,14 Thyroid isthmusectomy with limited neck dissection (including precricoid and pretracheal lymph node dissection) does not require exploration of the tracheoesophageal groove or formal identification of the RLN, which may reduce the risk of iatrogenic injury to the parathyroid glands and RLN. Nixon et al 1 reported that among 19 patients with well-differentiated thyroid cancer isolated to the isthmus, thyroid isthmusectomy was associated with a 10-year disease-specific survival rate of 100% and a 10- year locoregional recurrence-free survival of 100%. TABLE 4. Univariate and multivariate logistic regression for paratracheal lymph node metastasis in solitary isthmic papillary thyroid carcinoma. Independent variables Univariate Multivariate OR (95% CI) p value OR (95% CI) p value Sex, male vs female ( ) ( ).441 Age, 38 vs >38 y ( ) ( ).003 Size, >0.6 vs 0.6 cm ( ) ( ).004 Extrathyroidal extension, positive vs negative ( ) ( ).815 Prelaryngeal metastasis, positive vs negative ( ) ( ).943 Pretracheal metastasis, positive vs negative ( ) ( ).001 Concomitant thyroid disease, thyroiditis vs absent ( ) ( ).944 Abbreviations: OR, odds ratio; 95% CI, 95% confidence interval. HEAD & NECK DOI /HED APRIL 2016 E1513

5 WANG ET AL. However, thyroid isthmusectomy with limited neck dissection for solitary isthmic PTC may be insufficient in patients with occult lymph node metastasis in the paratracheal basins. We therefore analyzed the lymph nodes in the paratracheal basins among patients with solitary cn0 PTC limited to the thyroid isthmus. There were a mean of 4.18 (95% CI: ) nodes in the left paratracheal basin and 5.40 (95% CI: ) nodes in the right paratracheal basin, of which a mean of 0.58 (95% CI: ) and 0.37 (95% CI: ) nodes, respectively, were metastatic. The risk factors for PTLN metastasis included young age (38 years), primary tumor size >0.6 cm, and positive pretracheal lymph nodes. The risk factors for CLN metastasis were male sex and primary tumor size >0.7 cm. In our cohort, 11.0% patients (8 of 73) had extrathyroidal extension of the primary tumor, including gross invasion beyond the thyroid and microscopic extracapsular spread. This rate is less than the previously reported values (51.1% to 70.2%). 7,8 A possible explanation for the lower extrathyroidal extension frequency in our study could be that only cn0 patients with solitary isthmic lesions were enrolled in this study. Extrathyroidal extension is a recognized risk factor for CLN metastasis in patients with PTC. 15,16 Although the incidence of extrathyroidal extension was higher in patients with PTLN metastasis or CLN metastasis than in patients without PTLN or CLN involvement (17.9% vs 6.7% and 17.6% vs 5.1%, respectively), extrathyroidal extension was not significantly associated with PTLN metastasis or CLN metastasis in our population on logistic regression analysis, possibly because of the small sample size of our study. CONCLUSION In our study of 73 patients with solitary isthmic PTC, 34 (46.6%) and 28 (38.4%) were found to have occult CLN metastasis and PTLN metastasis, respectively, on pathological examination after total thyroidectomy plus bilateral prophylactic CND. A maximum tumor diameter >0.7 cm and male sex independently predicted CLN metastasis. Pretracheal lymph node metastasis, primary tumor >0.6 cm, and age 38 years independently predicted PTLN metastasis. Thus, thyroid isthmusectomy for solitary isthmic PTC may be unsuitable in patients with tumors >0.6 cm, those aged 38 years, and in male patients. REFERENCES 1. Nixon IJ, Palmer FL, Whitcher MM, et al. Thyroid isthmusectomy for well-differentiated thyroid cancer. Ann Surg Oncol 2011;18: Sugenoya A, Shingu K, Kobayashi S, et al. Surgical strategies for differentiated carcinoma of the thyroid isthmus. Head Neck 1993;15: Shindo M, Wu JC, Park EE, Tanzella F. The importance of central compartment elective lymph node excision in the staging and treatment of papillary thyroid cancer. Arch Otolaryngol Head Neck Surg 2006;132: Mirallie E, Visset J, Sagan C, Hamy A, Le Bodic MF, Paineau J. Localization of cervical node metastasis of papillary thyroid carcinoma. World J Surg 1999;23: ; discussion Wada N, Duh QY, Sugino K, et al. Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg 2003;237: American Thyroid Association Surgery Working Group, American Association of Endocrine Surgeons, American Academy of Otolaryngology Head and Neck Surgery, et al. Consensus statement on the terminology and classification of central neck dissection for thyroid cancer. Thyroid 2009;19: Lee YS, Jeong JJ, Nam KH, Chung WY, Chang HS, Park CS. Papillary carcinoma located in the thyroid isthmus. World J Surg 2010;34: Song CM, Lee DW, Ji YB, Jeong JH, Park JH, Tae K. Frequency and pattern of central lymph node metastasis in papillary carcinoma of the thyroid isthmus. Head Neck [Epub ahead of print] 9. Hartl DM, Travagli JP. The updated American Thyroid Association Guidelines for management of thyroid nodules and differentiated thyroid cancer: a surgical perspective. Thyroid 2009;19: Koo BS, Choi EC, Yoon YH, Kim DH, Kim EH, Lim YC. Predictive factors for ipsilateral or contralateral central lymph node metastasis in unilateral papillary thyroid carcinoma. Ann Surg 2009;249: Forest VI, Clark JR, Ebrahimi A, et al. Central compartment dissection in thyroid papillary carcinoma. Ann Surg 2011;253: Pereira JA, Jimeno J, Miquel J, et al. Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery 2005;138: ; discussion American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19: Watkinson JC, British Thyroid Association. The British Thyroid Association guidelines for the management of thyroid cancer in adults. Nucl Med Commun 2004;25: Zhang L, Wei WJ, Ji QH, et al. Risk factors for neck nodal metastasis in papillary thyroid microcarcinoma: a study of 1066 patients. J Clin Endocrinol Metab 2012;97: Roh JL, Kim JM, Park CI. Central lymph node metastasis of unilateral papillary thyroid carcinoma: patterns and factors predictive of nodal metastasis, morbidity, and recurrence. Ann Surg Oncol 2011;18: E1514 HEAD & NECK DOI /HED APRIL 2016

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