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Papillary Thyroid Carcinoma
1. ORIGINAL ARTICLE Papillary Thyroid Carcinoma Modified Radical Neck Dissection Improves Prognosis Shiro Noguchi, MD, PhD; Nobuo Murakami, MD; Hiroto Yamashita, MD, PhD; Masakatsu Toda, MD, PhD; Hitoshi Kawamoto, PhD Objective: To ascertain whether modified radical neck section, 8.5% underwent partial node excision, and 19.4% dissection offers a survival advantage for some subsets underwent no node excision. of patients with papillary cancer of the thyroid. Results: A univariate analysis revealed a subset of pa- Design: A retrospective cohort study of 2966 patients tients who benefited from modified radical neck dissec- curatively treated at the Noguchi Thyroid Clinic and tion. A multivariate analysis revealed that sex (P .001), Hospital Foundation, Oita, Japan, between 1946 and age at the time of the operation (P .001), size of the pri- 1991. mary tumor (P .001), extrathyroidal invasion (P .001), and the presence of nodal metastasis (P .01) are sig- Setting: A center for the treatment of thyroid disease, nificant risk factors. where about 1400 thyroid operations are performed per year. Conclusion: Patients with nodal metastasis, patients in whom the primary tumor invades beyond the thyroid cap- Patients: Between 1946 and 1991, patients with pap- sule, and women older than 60 years can benefit from illary cancer whose primary tumor was 1 cm or larger modified radical neck dissection. and who were curatively treated were studied. Of the 2859 patients, 72.1% underwent modified radical neck dis- Arch Surg. 1998;133:276-280 I N THE surgical management of recurrence rate,1,2 its influence on the sur- papillary cancer, controversy ex- vival rate still remains unclear. In this ar- ists not only about thyroidec- ticle, we report a survival advantage of tomy but also about the extent of modified radical neck dissection in some lymph node excision. While there subgroups of patients with papillary thy- are well-accepted risk factors, such as the roid cancer, despite the fact that these pa- patient’s age at the time of surgery, the size tients had more advanced disease. of the primary tumor, and invasion of the tumor beyond the thyroid capsule, the in- RESULTS fluence of lymph node metastasis on sur- vival is controversial. In this study, we at- PRIMARY TUMOR tempted to address these issues. A randomized trial is believed to be The mean (±SD) diameter of the primary the most reliable and scientific way of com- tumor was 27.1±14.5 mm. The smallest tu- paring 2 therapeutic methods. However, mor was 10 mm in diameter by defini- when a randomized trial is not feasible, an- tion, and the largest was 150 mm in di- other approach is to determine whether a ameter. The tumor was confined within the group of patients with advanced disease thyroid capsule in 912 patients. has a better prognosis after undergoing one METASTASIS surgical procedure than another group of patients with less advanced disease who Gross nodal metastasis was found in 1160 has undergone a less extensive surgical (39.1%) of the patients. procedure. If so, the more extensive sur- In 638 (21.5%) of the patients, nodal From the Noguchi Thyroid gical procedure would be justified. metastasis was not examined or counted; Clinic and Hospital Foundation (Drs Noguchi, Murakami, We elected to use subtotal thyroidec- in 323 (10.9% of the patients, metastasis Toda, and Kawamoto) and the tomy and to perform modified radical neck was histologically confirmed not to be pres- Department of Pathology, Oita dissection in most of our patients. Al- ent; and in 2005 (67.6%) of the patients, Medical University though it is unquestionably established that metastasis was histologically confirmed to (Dr Yamashita), Oita, Japan. modified radical neck dissection reduces the be present. ARCH SURG/ VOL 133, MAR 1998 276 Downloaded from www.archsurg.com on October 21, 2010 ©1998 American Medical Association. All rights reserved.
Table 1. Lymph Node Excision PATIENTS AND METHODS in Relation to Thyroidectomy* Modified Between 1946 and 1991, 3994 patients seen at the Radical Partial Noguchi Thyroid Clinic and Hospital Foundation, Neck Node No Node Oita, Japan, had papillary cancer. The following 2 Type of Procedure Dissection Excision Excision groups of patients were excluded from the study: 124 Total thyroidectomy 68 (90.7) 6 (8.0) 1 (1.3) patients who were not surgically treated or who un- (n = 75) derwent noncurative surgery (including 17 patients Subtotal thyroidectomy 1022 (82.9) 90 (7.3) 121 (9.8) who had pulmonary metastases when they were ini- (n = 1233) tially seen and 92 who underwent incomplete resec- Lobectomy 971 (79.8) 87 (7.1) 159 (13.1) tion) and 904 patients whose primary tumor had a (n = 1217) maximum diameter of less than 10 mm. Therefore, Partial lobectomy 78 (17.7) 69 (15.6) 294 (66.7) (n = 441) 2966 patients were included in this study. Information about living patients was obtained *All data are given as the number (percentage) of patients who underwent by periodic correspondence with the patients them- each type of procedure. selves, family members, referring physicians, and mu- nicipal records. For the deceased patients, the cause of death was confirmed by death certificates or con- Table 2. Characteristics of Patients Who Underwent tact with family members and hospitals. The mean Modified Radical Neck Dissection (MRND) Compared follow-up interval in the patients last known to be With Patients Who Did Not Undergo MRND* alive was 15.6 years. Twelve (0.4%) of the patients were unavailable for follow-up, 170 died of thyroid Patients Who Patients cancer, and 333 died of unrelated causes. Underwent Who Did Not The cause-specific survival rates were calcu- MRND Undergo MRND lated according to the Kaplan-Meier method. Risk fac- Characteristics (n = 2139) (n = 827) tor analysis was performed using the Cox propor- Preoperative diagnosis of cancer 1839 (86.0) 292 (35.3) tional hazards regression model. 2 Analysis was Extrathyroidal invasion 814 (38.1) 98 (11.8) applied for comparisons between 2 groups with a simi- Adhesion lar distribution, and the Wilcoxon rank sum test– Recurrent nerve 628 (29.4) 35 (4.2) Kruskal-Wallis test was applied for groups with an To the esophagus 354 (16.5) 22 (2.7) irregular distribution. To the larynx 116 (5.4) 8 (1.0) To the jugular vein 255 (11.9) 23 (2.8) Mean diameter, mm 27.5 26.7 *All data are given as the number (percentage) of patients in each group. TYPES OF THYROIDECTOMY AND Except for mean diameter ( P .22), all differences between groups were LYMPH NODE EXCISION significant ( P .001). Total thyroidectomy was performed in 75 (2.5%) of the internal carotid artery to the trapezius muscle, and from patients; subtotal thyroidectomy, 1233 (41.6%) of the the subclavian vein to the hypoglosseal nerve (lateral patients; lobectomy, 1217 (41.0%) of the patients; and compartment). partial lobectomy, 441 (14.9%) of the patients. Our Patients who underwent modified radical neck dis- routine method of subtotal thyroidectomy is to leave section had macroscopic metastasis, invasion of the pri- behind 1 or 2 g of the upper pole of the unaffected lobe, mary tumor to surrounding tissue, or a preoperative di- with the parathyroid gland left in situ. When intraglan- agnosis of cancer. Further analysis was performed by dular dissemination is present on the contralateral dividing the patients into 2 groups, those treated with modi- upper pole, we try to leave behind 1.0 or 1.5 g of the fied radical neck dissection and those not treated with modi- upper pole of any side that looks normal. Lobectomy is fied radical neck dissection, because of the few patients almost always accompanied by isthmectomy. A special in the central compartment excision group. Table 1 shows explanation is required regarding patients who under- the number and percentage of patients treated with each went partial lobectomy. Of the 441 patients, 71 had type of thyroidectomy and lymph node excision. concomitant benign disease; of these 71 patients, 66 Patients who did not undergo this dissection had no underwent the operation for that reason. The remaining macroscopic metastasis and minimal or no invasion to patients had a small tumor. Of the 441 patients, 78 surrounding tissue. The differences between the 2 groups underwent modified radical neck dissection, 69 under- are summarized in Table 2. went central compartment node dissection, and the remaining 294 underwent no node excision. This pro- INVASION OR ADHESION cedure was mostly performed between 1970 and 1975. The modified radical neck dissection encompassed dis- In this type of retrospective study, adhesion and inva- section of the fat and lymph node tissues around the sion of the primary tumor to the surrounding tissues were trachea (central compartment) and those around the hard to differentiate strictly; therefore, they were grouped jugular vein extending from the common carotid artery together. The incidence of invasion or adhesion of the up to the bifurcation, superior to the bifurcation the primary tumor to surrounding tissues increased with age ARCH SURG/ VOL 133, MAR 1998 277 Downloaded from www.archsurg.com on October 21, 2010 ©1998 American Medical Association. All rights reserved.
1.0 1.0 0.9 Patients Who 0.9 Patients Who Underwent MRND Underwent MRND 0.8 0.8 0.7 0.7 Patients Who Did Not Undergo MRND Patients Who Did Not 0.6 0.6 Undergo MRND Survival Rate Survival Rate 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 10 20 30 40 50 0 10 20 30 40 50 Years After Surgery Years After Surgery Figure 1. Modified radical neck dissection (MRND) improves the Figure 2. Modified radical neck dissection (MRND) improves the cause-specific survival rate in patients whose primary tumor had cause-specific survival rate in patients who had gross nodal metastasis extrathyroidal invasion (n=912, 30.7% of the total) ( P .02, log-rank test, (n=1157, 39.0% of the total) ( P .009, log-rank test, and P .005, Wilcoxon and P .01, Wilcoxon rank sum test). rank sum test). (P .001). The incidence of nodal metastasis in male and in 1 patient. Among these patients, 83 were successfully female patients was 92.1% and 85.5%, respectively. The treated by a second operation and 1 survived with disease; difference was significant (P .009). of the remaining 13 (0.4%) of the patients, 11 (0.37%) died The patients in whom there was invasion or adhesion of distant metastasis and 2 (0.07%) died of local disease. of the primary tumor to surrounding tissue and who ex- perienced gross nodal involvement had a better survival MULTIVARIATE ANALYSIS OF RISK FACTORS rate after a modified radical neck dissection was performed, as shown in Figure 1 and Figure 2, respectively. The significant risk factors were sex (P .001), age at the Although the overall survival rates in the group that time of the operation (P .001), maximum diameter of underwent modified radical neck dissection and in the the primary tumor (P .001), extrathyroidal invasion group that did not undergo modified radical neck dis- (P .001), and presence of metastasis regardless of the section were not statistically different, among patients with size of the tumor (P .04). any metastases, the group that underwent modified radi- cal neck dissection had a survival advantage (Figure 3). COMMENT AGE Since 1970, when we first noted the extremely high in- cidence of nodal metastases in patients with papillary can- Patients were classified into 4 age groups: younger than cer of the thyroid, we have advocated modified radical 20 years, between 20 and 50 years, between 51 and 60 neck dissection for these patients.3,4 Recently, Simon and years, and older than 60 years. Older age was a signifi- Goretzki1 noticed a high nodal recurrence rate and sug- cant (P .001) risk factor. In women older than 60 years, gested the usefulness of a modified radical neck dissec- who composed 17.7% of the patients, modified radical tion. Scheumann et al2 reported improvement of the re- neck dissection conferred a significant (P .02, log- currence rate and the survival rate after a modified radical rank test, and P .007, Wilcoxon rank sum test) sur- neck dissection; however, the indication criteria were not vival advantage regardless of the risk factors (Figure 4). clarified. Although many had failed to find improve- The 10- and 20-year cause-specific survival rates for the ment of the survival rate after modified radical neck dis- group that underwent modified radical neck dissection section,5-8 we were able to demonstrate the beneficial ef- (n=373) were 92.4% and 73.2% compared with 80.3% fect of modified radical neck dissection on survival in some and 56.7%, respectively, for the group that did not un- subsets of female patients with papillary cancer of the thy- dergo modified radical neck dissection (n=130). roid by univariate and multivariate analyses. There are several possible reasons why previous studies have failed RECURRENCE FROM REMNANT THYROID to demonstrate any benefit of modified radical neck dis- section. This form of surgery has often been applied ex- Recurrence in the remnant thyroid tissue was observed in clusively for advanced disease: the percentage of pa- 97 (3.3%) of the patients. The contralateral lobe was af- tients with papillary cancer of the thyroid who underwent fected in 74 patients, the ipsilateral thyroid bed was af- radical or modified radical neck dissection ranged from fected in 22 patients, and the bilateral lobes were affected 12.3% to 30.0% in institutions in which the procedure ARCH SURG/ VOL 133, MAR 1998 278 Downloaded from www.archsurg.com on October 21, 2010 ©1998 American Medical Association. All rights reserved.
1.0 1.0 Patients Who 0.9 Underwent MRND 0.9 Patients Who Did Not 0.8 Undergo MRND 0.8 Patients Who Underwent MRND 0.7 0.7 0.6 0.6 Survival Rate Survival Rate 0.5 0.5 Patients Who Did Not Undergo MRND 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 10 20 30 40 50 0 5 10 15 20 25 30 Years After Surgery Years After Surgery Figure 3. Modified radical neck dissection (MRND) improves the Figure 4. Modified radical neck dissection (MRND) improves the cause-specific survival rate in patients who had nodal metastasis of any size cause-specific survival rate in female patients older than 60 years, regardless (n=2005, 67.6% of the total) ( P .04, log-rank test, and P .007, Wilcoxon of other risk factors (n=468, 15.8% of the total) ( P .02, log-rank test, and rank sum test). P .007, Wilcoxon rank sum test). is reserved only for patients with gross nodal metasta- ing system by excluding histological grading and includ- sis.6-12 Moreover, because recurrence in cervical nodes can ing completeness of the resection, invasion of the pri- be treated easily and successfully by a second surgery, mary tumor to surrounding tissues, and size of the primary such recurrence may not have affected the survival in tumor.25 None of these scoring systems but ours singu- many instances.5,6,13-15 Because of the indolent nature of larly ignored nodal involvement, despite the fact that mul- papillary cancer, the probability of differences of disease- tivariate analysis clearly proved that gross nodal involve- specific survival rates among groups given different treat- ment is one of the risk factors. ments is small and, therefore, an analysis of many cases Routine or frequent use of radioactive iodine with is necessary before any significant difference will emerge.16 the objective of ablating microscopic cancer foci is rec- Finally, not all patients benefit from modified radical neck ommended by those who advocate total thyroidec- dissection, and there are no criteria for identifying pa- tomy.5,6,26-28 Those who do not perform total thyroidec- tients who are, and who are not, likely to benefit. tomy routinely use radioactive iodine in selected Recent advances of statistical models and com- patients.29,30 We employ radioactive iodine only when re- puter technology enabled us to analyze many patients with mote metastasis is evident and when the metastasis can multiple risk factors.2,9,17-20 With the use of multivariate accumulate radioactive iodine, not only because of the analysis, the age of the patients at the time of the opera- strict regulation of radioisotopes in Japan but because we tion, the size of the primary tumor, the presence of gross also believe that calcitonin secretion must be preserved. nodal involvement, and the presence of remote metas- In our series, male patients had a higher incidence tasis when they were specifically mentioned have been of nodal metastasis. This observation agreed with the ob- agreed on as the risk factors in the literature we exam- servations of Tisell et al,12 Tscholl and Hedinger,31 and ined.13,17,21-23 However, a scoring system or a classifica- Ahuja et al.32 tion of patients based on prognosis, inclusive of nodal Although we are aware that total thyroidectomy is metastasis, is only given in the article that we previ- a safe procedure when it is performed by skilled and well- ously published.20 experienced surgeons,33-35 we still try to avoid total thy- Aside from these rather sophisticated mathematical roidectomy for the simple reason that it does not seem methods of analysis, Cady et al24 made a simple and prac- to improve the survival rate. Because of this policy, we tical rating system named AMES, which is essentially based paid particular attention to recurrence at the remnant thy- on the age of the patient, the presence of remote metas- roid. Of the 2966 patients who we observed on average tasis, the extension of the primary tumor beyond the thy- for 15.6 years, only 13 (0.4%) died of causes related to roid capsule, and the size of the primary tumor. They fur- recurrence in the remnant thyroid or thyroid bed; among ther developed the concept of risk group definition. With these patients, only 2 (0.07%) died with neck disease. the use of multivariate analysis, as well as histological grad- Many other researchers are also unable to find any sur- ing, Hay et al25 proposed a new scoring system inclusive vival advantage of total thyroidectomy.7,14,36-40 Samaan et of histological grading, known as AGES, which denotes al26 indicated that total thyroidectomy was associated with age of the patient, histological grade of the tumor, exten- a longer disease-free interval and less recurrence. How- sion beyond the thyroid capsule, and size of the primary ever, in their more recent article,41 a higher survival rate tumor. They further developed and improved their scor- was reported.42 We wonder whether the total thyroidec- ARCH SURG/ VOL 133, MAR 1998 279 Downloaded from www.archsurg.com on October 21, 2010 ©1998 American Medical Association. All rights reserved.
tomies were performed by more experienced surgeons 9. Salvensen H, Njolstad PR, Akslen LA, et al. Thyroid carcinoma: results from sur- gical treatment in 211 consecutive patients. Eur J Surg. 1991;157:521-526. compared with the less extensive thyroidectomies. The 10. McHenry CR. Prospective management of nodal metastases in differentiated thy- bone mineral content is reduced after total thyroidec- roid cancer. Am J Surg. 1991;162:353-356. tomy.42 Therefore, if there is no benefit associated with 11. Proye C, Carnaille B, Vix M, et al. Recidives ganglionaires des cancers thyroı- ´ ¨ diens opere: de l’inutilite du curage ganglionaire de principe (carcinomes medul- ´ ´ ´ total thyroidectomy in appropriately selected patients, then laires ecclus). Chirurgie. 1992;118:448-452. the increased risk of osteoporosis should be avoided. 12. Tisell L-E, Nilsson B, Molne J, et al. Improved survival of patients with papillary ¨ Most researchers agree that older patients with dif- thyroid cancer after surgical microdissection. World J Surg. 1996;20:854-859. 13. Simpson WJ, McKinney SE, Carruthers JS, et al. Papillary and follicular thyroid ferentiated thyroid cancer have a relatively poorer prog- cancer: prognostic factors in 1578 patients. Am J Med. 1987;83:479-488. nosis. In the men and women in our study, age was one 14. Rossi RD, Cady B, Silverman ML, et al. Current results of conservative surgery for differentiated thyroid carcinoma. World J Surg. 1986;10:612-622. of the most important risk factors. Women older than 15. Vickery AJ, Wang CA, Walker AM. Treatment of intrathyroidal papillary carci- 60 years accrue a survival advantage when they un- noma of the thyroid. Cancer. 1987;60:2587-2595. dergo modified radical neck dissection, regardless of other 16. Udelsman R, Lakatos E, Landenson P. Optimal surgery for papillary thyroid car- cinoma. World J Surg. 1996;20:88-93. risk factors. 17. Tubiana M, Schlumberger M, Rougier P. Long-term results and prognostic fac- Univariate and multivariate analyses of modified radi- tors in patients with differentiated thyroid cancer. Cancer. 1985;55:794-804. cal neck dissection indicated a survival advantage in older 18. Bacourt F, Asselain B, Savoie JC, et al. Multifactorial study of prognostic factors in differentiated thyroid carcinoma and a re-evaluation of importance of age. Br women. However, women younger than 55 years, those J Surg. 1986;73:274-277. without gross metastasis, and those without extrathy- 19. Kerr DJ, Burt AD, Boyle P, MacFarlane GJ, Storer AM, Brewin TB. Prognostic roidal invasion seemed to derive no benefit from this pro- factors in thyroid tumours. Br J Cancer. 1986;54:475-482. 20. Noguchi S, Murakami N, Kawamoto H. Classification of papillary cancer of the cedure. thyroid based on prognosis. World J Surg. 1994;18:552-557. 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