Childhood and Adolescent Thyroid Carcinoma
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1 724 Childhood and Adolescent Thyroid Carcinoma Perry W. Grigsby, M.D. 1 Anat Gal-or, B.Sc. 1 Jeff M. Michalski, M.D. 2 Gerard M. Doherty, M.D. 2 1 Department of Radiation Oncology, Mallinckrodt Institute of Radiology, Washington University Medical Center, St. Louis, Missouri. 2 Department of Surgery, Washington University Medical Center, St. Louis, Missouri. Address for reprints: Perry W. Grigsby, M.D., Department of Radiation Oncology, Washington University Medical Center, P.O. Box 8224, 4939 Children s Place, Suite 5500, St. Louis, MO 63110; Fax: (314) ; grigsbyp@ netscape.net Received December 13, 2001; revision received February 22, 2002; accepted February 25, OBJECTIVES. This analysis was performed to evaluate the influence of clinical and treatment factors on local tumor control, control of distant metastasis, survival, and complications in children and adolescents with thyroid carcinoma. METHODS. The records of 56 children and adolescents with papillary and follicular carcinoma of the thyroid were reviewed. They ranged in age from 4 to 20 years. There were 43 females and 13 males. At diagnosis, 15 (27%) patients had disease confined to the thyroid, 34 (60%) had additional lymph node metastasis to the neck or upper mediastinum, and 7 (13%) also had lung metastasis. Treatment consisted of a total thyroidectomy in 48 patients, a subtotal thyroidectomy in 4 patients, and a lobectomy in 4 patients. All 56 patients received postoperative thyroid hormone suppressive therapy. 131 I was administered to 82% (46 of 56) of patients after their initial surgery. RESULTS. The overall survival rate was 98% with a follow-up of years (with a median follow-up of 11.0 years). The one death that occurred in this patient population was the result of a congenital heart defect and was unrelated to thyroid carcinoma. The 10-year progression-free survival rate was 61%. Nineteen patients (34%) experienced a recurrence of their thyroid carcinoma. The time to first recurrence of disease ranged from 8 months to 14.8 years (mean, 5.3 years). None of those with disease confined to the thyroid developed recurrent disease. The recurrence rate was 50% (17 of 34) in patients with lymph node metastasis and 29% (2 of 7) in patients with lung metastasis (P 0.02). Tumor characteristics were evaluated for time to first recurrence utilizing the logistic likelihood ratio test to predict disease recurrence. Thyroid capsule invasion (P 0.02), soft tissue invasion (P 0.03), positive margins (P 0.006), and tumor location at diagnosis (thyroid only vs. thyroid and lymph nodes vs. thyroid, lymph nodes, and lung metastasis, P 0.02) were significant for developing recurrent disease. Patients younger than 15 years old at diagnosis were more likely to have more extensive tumor at diagnosis than patients who were 15 years and older (thyroid only vs. thyroid and lymph nodes vs. thyroid, lymph nodes, and lung metastasis, P 0.02). CONCLUSION. Carcinoma of the thyroid in children and adolescents has little risk of mortality but a high risk of recurrence. Younger patients present with a more advanced stage of disease and are more likely to have disease recurrence. Total thyroidectomy and lymph node dissection, followed by postoperative 131 I therapy, thyroid hormone replacement (suppressive) administration, and diligent surveillance are warranted. Cancer 2002;95: American Cancer Society. DOI /cncr KEYWORDS: thyroid carcinoma, childhood, adolescents, 131 I American Cancer Society
2 Childhood and Adolescent Thyroid Carcinoma/Grigsby et al. 725 Several studies have shown that thyroid carcinoma in pediatric patients differs from thyroid carcinoma in adults with respect to its presentation and its outcome. Although pediatric patients with thyroid carcinoma tend to present with disease at a more advanced stage than adults, namely, a higher incidence of lymph node and pulmonary metastasis, the prognosis for death from disease is much better for the pediatric patients. Because of the favorable course for survival with this disease in pediatric patients, many have argued for less aggressive treatment than for adults. 1 In particular, recommendations have been made to not perform a total thyroidectomy and lymph node dissection. Conversely,some investigators believe that the use of total thyroidectomy, lymph node dissection, and postoperative 131 I therapy is best to treat this condition. 2 To tailor treatment to best suit the individual patient, there have been attempts to classify the aggressiveness of thyroid carcinoma in pediatric patients by identifying prognostic factors for developing recurrent and metastatic disease. Many studies have evaluated patient, tumor, and treatment variables, but no specific factors have been identified that unequivocally predict the risk of developing recurrent disease in children. DNA content of tumor cells, patient age, tumor histology, and gender may be correlated with prognosis. However, these prognostic factors have not been substantiated by others. 3 In light of incomplete information, we sought to develop a treatment plan that can achieve the best results for the most patients. This current study is a report of a retrospective chart review of pediatric patients treated at our institution for thyroid carcinoma. MATERIALS AND METHODS This retrospective study consists of 56 children and adolescents with the diagnosis of carcinoma of the thyroid seen at the Mallinckrodt Institute of Radiology from 1970 through Data were obtained from the patients medical records and by direct communication with the patients. There were 43 females and 13 males. The age of the patients at the time of the diagnosis of thyroid carcinoma ranged from 4 to 20 years (mean, 15.8 years). Of the 56 children, 46 were white, 6 were black, 2 were Asian, and 2 were Hispanic. None of the patients had a history of head or neck irradiation. One patient had a history of a completely resected cerebellar astrocytoma treated solely with surgery. The two signs at presentation were a thyroid mass in 91% of the patients and palpable cervical adenopathy in 29% (16 of 56). Of those with a palpable thyroid mass, the mass ranged from 1 to 5 cm (mean, 2.3 cm). Cervical adenopathy was unilateral in 13 and bilateral in 3. A total thyroidectomy was performed in 48 patients, a subtotal thyroidectomy in 4 patients, and a lobectomy in 4 patients. The cervical lymph nodes were evaluated by biopsy only in 3 patients, excision was performed in 27 patients, a modified radical neck dissection was performed in 9 patients, and a radical neck dissection was performed in 3 patients. The initial chest X-ray was abnormal in two patients. Patient follow-up ranged from 0.6 to 30.7 years (median, 11.0 years). The Kaplan Meier estimate was used to evaluate tumor recurrence. 4 The test of equivalence of the estimates of recurrence was performed by the Mantel Cox log rank test. 5 The Yates corrected chi-square test was used to compare groups. Multivariate regression analysis was performed using the Cox proportional hazards model. 6 RESULTS Histologic Tumor Characteristics The histologic subtype of the tumor was pure papillary carcinoma in 66%, follicular variant of papillary carcinoma in 29%, and pure follicular carcinoma in 5% of patients. All tumors were well differentiated. Both lobes of the thyroid gland were involved with tumor in 30% of patients. There were multiple tumor foci in 57%, thyroid capsule invasion in 54%, vascular invasion in 52%, soft tissue involvement in 36%, positive margins in 29%, cervical lymph node metastasis in 73%, and pulmonary metastasis in 13% of patients. Cervical lymph node involvement was unilateral in 54% and bilateral in 46% of patients with histologic lymph node involvement. Postoperative Treatment 131 I was administered to 46 patients after their initial operation whereas 10 patients did not receive adjuvant 131 I. The initial amount of 131 I that was administered ranged from 25 to 200 mci (mean, 98 mci) and is related to patient age and size (Fig. 1). The cumulative 131 I administered for initial therapy ranged from 31 to 810 mci (mean, 194 mci). The patients received one to five 131 I doses after surgery; 24 received one treatment, 8 received two, 8 received three, 3 received four, and 3 received five treatments. External irradiation, in addition to 131 I, was used in one case. This
3 726 CANCER August 15, 2002 / Volume 95 / Number 4 FIGURE 1. Initial (n 46). 131 I administration activity according to patient age. FIGURE 3. Progression-free survival by extent of disease at diagnosis (thyroid only, n 15; thyroid plus lymph nodes, n 34; thyroid plus lymph nodes plus lung, n 7; P 0.02). FIGURE 2. Progression-free survival for all patients (n 56). patient received a tumor dose of 60 Gy in 30 fractions. All 56 patients received thyroid hormone replacement therapy. Recurrence At the time of last follow-up, 53 patients were alive and free of thyroid carcinoma, 2 patients were alive with persistent thyroid carcinoma, and 1 patient died of intercurrent disease. The overall survival rate was 98%. The 10 and 20-year progression-free survival rates were 61% and 46%, respectively (Fig. 2). Nineteen patients (34%) experienced a recurrence of their thyroid carcinoma. Recurrences occurred in 7 of 10 patients who did not receive initial postoperative 131 I and in 12 of 46 (26%) patients who did receive 131 I. The time to first recurrence ranged from 8 months to 14.8 years (mean, 5.3 years). None of the patients with disease confined to the thyroid developed recurrent disease. The recurrence rates were 50% (17 of 34) in patients with lymph node metastasis and 29% (2 of 7) in patients with lung metastasis (P 0.02; Fig. 3). The two lung recurrences were detected by chest X-ray (and both subsequently had 131 I uptake) and all neck recurrences were detected by physical examination. The five patients with lung metastasis at diagnosis who did not have disease recurrence in the lung had negative total body 131 I scintigrams. All neck recurrences were either histologically proven or had 131 I uptake or both. In our selected patient population, recurrence could not be correlated with the extent of the initial thyroidectomy or with the use of postoperative 131 I therapy. Treatment of Recurrences Of the 19 patients who had disease recurrence, 2 underwent surgery only, 5 received only 131 I, and 12 underwent surgery and received 131 I for treatment of their recurrent disease. All patients undergoing an operation for recurrent disease had a lymph node dissection. The cumulative 131 I dose administered to patients with recurrent disease ranged from 100 to 751 mci (mean, 288 mci).
4 Childhood and Adolescent Thyroid Carcinoma/Grigsby et al. 727 TABLE 1 Multivariate Analysis of Prognostic Factors Histologic Finding P value Positive margins Tumor location at diagnosis (thyroid, lymph nodes, lung) Capsular invasion Soft tissue invasion Multifocal Vascular invasion Age at diagnosis Tumor size Prognostic Factors Tumor characteristics were evaluated for time of first recurrence utilizing Cox multivariate analysis to predict disease recurrence. Capsular invasion (P 0.02), soft tissue invasion (P 0.03), positive margins (P 0.006), and tumor location at diagnosis (P 0.02) were significant for developing recurrent disease (Table 1). Patients younger than 15 years old at diagnosis were more likely to have more extensive tumor at diagnosis than patients who were 15 years and older (thyroid only vs. thyroid and lymph nodes vs. thyroid, lymph nodes, and lung metastasis, P 0.02). Complications Postoperative complications occurred in eight patients. Temporary vocal cord dysfunction (not paralysis) occurred in three, permanent hypoparathyroidism occurred in four, and one had facial nerve dysfunction. Complications from irradiation included neck fibrosis in the patient treated with external irradiation and temporary loss of taste occurred in one patient. No severe complications were noted as a result of 131 I administration. No secondary neoplasms were detected. DISCUSSION Carcinoma of the thyroid is relatively uncommon in the United States and accountsfor less than 1% of cancer-related deaths. Although most cases of thyroid carcinoma occur in adults, thyroid carcinoma may present in children. It is generally agreed that the clinical course of thyroid carcinoma in children and adolescents is different than the clinical course in adults. Namely, the prognosis for cancer death in children is markedly better than the prognosis in adults. 7 But, paradoxically, children present with larger tumors, a greater incidence of lymph node metastasis, and a greater incidence of lung metastasis than do adults. 8 The discrepancy between aggressive tumor presentation and excellent prognosis in children is not well explained. One suggestion is that this observation may be related to the nondiploid DNA content of the tumor. 3 Zimmerman et al. 8 found that 25% of tumors in adults had nondiploid DNA compared with only 10% of tumors in children. Another suggestion for the difference in prognosis between children and adults is that thyroid tumors in children have a larger dependence on thyroid-stimulating hormone (TSH). Therefore, TSH suppression with thyroid hormone replacement is a more effective treatment in children. In adults, over time, well differentiated thyroid carcinoma may dedifferentiate to poorly differentiated thyroid carcinoma, especially in the course of the development of metastatic disease. Children may have a better prognosis because of a lack of progression from well to poorly differentiated neoplasms. 9 The patient and tumor characteristics observed in our patient population are similar to those reported in other studies. None of our patients had a history of head or neck irradiation. Our female-to-male ratio was 3.31:1, which is within the range reported by Segal et al. 2 Tumor involvement in both lobes of the thyroid gland ranges from 22% 10 to 49%. 2 Pathologic evaluation of the thyroid gland in our patients revealed that 30% had involvement of both lobes. Cervical adenopathy is a common presenting sign in children and adolescents. McHenry et al. 11 reported a 62% incidence of cervical adenopathy in their patients and Zimmerman et al. 8 reported a 90% incidence. We report a 29% incidence of cervical adenopathy clinically, but pathologically, 73% of patients had cervical lymph node disease. Pathologic involvement of cervical lymph nodes was bilateral in 46% of our patients. Another common presenting sign is pulmonary metastasis. The incidence of lung metastasis at presentation is reported to range from 6% to 33% The incidence of lung metastasis at presentation was 13% in our patient population. None of the patients in our study who developed recurrent disease developed lung metastasis as a new finding. It is noteworthy that none of the patients in our study and no patients reported in the literature have bone metastasis at diagnosis. None of the children and adolescents in our group developed clinically evident bone metastasis on follow-up evaluation. This is in contrast to the frequent occurrence of lung and bone metastasis in adults.
5 728 CANCER August 15, 2002 / Volume 95 / Number 4 Our study indicated that when the initial disease was confined to the thyroid, none of the patients developed recurrent disease. This is in contrast to a 50% recurrence rate in patients with thyroid and lymph node disease at diagnosis and a 29% recurrence rate in patients with thyroid, lymph node, and lung metastasis at diagnosis. Our data indicate that there are four significant prognostic factors associated with the development of recurrent thyroid carcinoma. These are capsular invasion, soft tissue invasion, positive margins, and tumor location at diagnosis (thyroid only vs. thyroid and lymph nodes v.s thyroid, lymph nodes, and lung metastasis). Younger children tend to present with more locally advanced disease than older children. Low treatment morbidity is a critical requirement of a strategy for this group of patients with an excellent prognosis and long life expectancy. In particular, in this study group of patients who underwent surgical procedures at multiple institutions, the significant rate of permanent hypoparathyroidism (8%, 4 of 52 bilateral procedures) emphasizes the need for expert attention to the technical details of the operation. The parathyroid glands in children are small and have a fragile blood supply. However, with the liberal use of parathyroid autotransplantation, permanent hypoparathyroidism should be a relatively uncommon permanent complication in experienced hands. 15,16 The optimal management of children and adolescents is not well defined. Some investigators suggest that limited surgery and thyroid hormone suppressive therapy are the most effective means of controlling this disease. 1,8,10 The majority of investigators recommend a combination of total thyroidectomy, selective lymph node dissection, postoperative 131 I therapy, and thyroid hormone suppressive therapy ,17 21 Specific guidelines for 131 I dosage are not available for children. Our general guidelines for adults are to administer postoperative 131 I in amounts of 100 mci for routine ablation, 150 mci for regional spread of disease, and 250 mci for distant metastatic disease. Our recommendations for children are to administer these activities on a mci-to-kg ratio (assuming the standard adult weight of 70 kg). The initial doses for the patients in this studyare shown in Figure 1. No significant acute or long-term toxicities from 131 I therapy were noted in these children. CONCLUSION Carcinoma of the thyroid in children and adolescents has little risk of mortality but a high risk of recurrence. Younger patients tend to present with a more advanced stage of disease. Although many of the patients in our study developed recurrent disease, the overall survival rate was excellent. Our treatment recommendations are standard for all children and adolescents. We recommend a total thyroidectomy and selective lymph node dissection. In our patients, the disease was bilateral in 30% and 73% had cervical lymph node metastasis. If the disease is unilateral and no lymph node metastases are present, then adjuvant 131 I therapy can be avoided. Postoperative 131 I therapy and thyroid hormone suppressive therapy should be administered to all patients. Recurrence is common and lifelong follow-up is essential. Follow-up evaluation should rely on periodic physical examination, thyroglobulin measurements, and total body 131 I scintigrams. 22 REFERENCES 1. Massimino M, Gasparini M, Ballerini E, Del Bo R. Primary thyroid carcinoma in children: a retrospective study of 20 patients. Med Pediatr Oncol. 1995;24: Segal K, Hadar T, Lubin E, Abraham A, Levy R. Thyroid carcinoma in children and adolescents. Harefuah. 1992;122: Tallroth E, Backdahl M, Einhorn J, Lundell G, Lowhagen T, Silversward C. Thyroid carcinoma in children and adolescents. Cancer. 1986;58: Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Statistic Assoc. 1958;53: Mantel N. Evaluation of survival data and two new rank order statistics arising in its consideration. Can Chemother Rep. 1966;50: Cox DR. Regression models and life tables. J R Statist Soc. 1972;34: Goepfert H, Dichtel WJ, Samaan NA. Thyroid cancer in children and teenagers. Arch Otolaryngol. 1984;110: Zimmerman D, Hay ID, Gough IR, et al. Papillary thyroid carcinoma in children and adults: long-term follow-up of 1039 patients conservatively treated at one institution during three decades. Surgery. 1988;104: De Keyser LF, Van Herle AJ. Differentiated thyroid cancer in children. Head Neck Surg. 1985;8: La Quaglia MP, Corbally MT, Heller G, Exelby PR, Brennan MF. Recurrence and morbidity in differentiated thyroid carcinoma in children. Surgery. 1988;104: McHenry C, Smith M, Lawrence AM, Jarosz H, Paloyan E. Nodular thyroid disease in children and adolescents: a high incidence of cacinoma. Am Surg. 1988;54: Ceccarelli C, Pacini F, Lippi F, et al. Thyroid cancer in children and adolescents. Surgery. 1988;104: Zueras VMT, Blanco AM, Matarranz YR, Perez RP, Morante MC, Oses SJM. Differentiated thyroid carcinoma in childhood. An Esp Pediatr. 1992;37: Lamberg BA, Karkinen-Jaaskelainen M, Franssila KO. Differentiated follicle-derived thyroid carcinoma in children. 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6 Childhood and Adolescent Thyroid Carcinoma/Grigsby et al Olson JA, DeBenedetti MK, Baumann DS, Wells SA. Parathyroid autotransplantation during thyroidectomy. Results of long-term follow-up. Ann Surg. 1996;223: Jocham A, Joppich I, Hecker W, Knorr D, Schwarz HP. Thyroid carcinoma in childhood: management and follow up of 11 cases. Eur J Pediatr. 1994;153: Harness JK, Thompson NW, McLeod MK, Pasieka JL, Fukuuchi A. Differentiated thyroid carcinoma in children and adolescents. World J Surg. 1992;16: Zohar Y, Strauss M, Laurian N. Adolescent versus adult thyroid carcinoma. Laryngoscope. 1986;96: Jereb B, Lowhagen T. Carcinoma of the thyroid in children and young adults. A review of 32 patients. Acta Radiol Ther Phys Biol. 1972;11: Harness JK, Thompson NW, Nishiyama RH. Childhood thyroid carcinoma. Arch Surg. 1971;102: Grigsby PW, Baglan K, Siegel BA. Surveillance of patients to detect recurrent thyroid cancer. Cancer. 1999;85:
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