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Clinical Thyroidology / Original Paper

Free Access

A Prospective Study Showing an Excellent Response of Patients with Low-Risk Differentiated Thyroid Cancer Who Did Not Undergo Radioiodine Remnant Ablation after Total Thyroidectomy

Janovsky C.C.P.S.a, b · Maciel R.M.B.a, b · Camacho C.P.a, b · Padovani R.P.a, b · Nakabashi C.C.a, b · Yang J.H.a, b · Malouf E.Z.a, b · Ikejiri E.S.a, b · Mamone M.C.O.C.a, b · Wagner J.b · Andreoni D.M.a, b · Biscolla R.P.M.a, b

Author affiliations

aThyroid Diseases Center and Laboratory of Molecular and Translational Endocrinology, Division of Endocrinology, Department of Medicine, Escola Paulista de Medicina, Universidade Federal de São Paulo, and bThyroid Diseases Center, Instituto Israelita de Ensino e Pesquisa Albert Einstein, São Paulo, Brazil

Corresponding Author

Rui M.B. Maciel, MD, PhD, Laboratory of Molecular and Translational Endocrinology

Division of Endocrinology, Department of Medicine, Escola Paulista de Medicina

Universidade Federal de São Paulo

Rua Pedro de Toledo 669, 11th Floor, São Paulo, SP 04039-032 (Brazil)

E-Mail rui.maciel@unifesp.br

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Eur Thyroid J 2016;5:44-49

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Abstract

Objectives: To prospectively evaluate the outcome of patients with low-risk papillary thyroid carcinoma treated with total thyroidectomy (TT) who did not undergo radioiodine remnant ablation (RRA). Study Design: We prospectively followed up 57 patients; 3 months after TT, thyroglobulin (Tg) assessment and neck ultrasonography (US) were performed while patients were taking L-T4, presenting suppressed TSH. Six months after TT, patients underwent stimulated Tg testing and whole-body scan (WBS) after recombinant TSH (rhTSH). Then, 18 months after TT, the patients were evaluated by neck US and Tg under TSH between 0.5 and 2.0 mIU/ml. Two years after TT, we performed another rhTSH assessment, measuring Tg and making a WBS. The patients were then annually monitored with neck US and Tg measurement under TSH between 0.5 and 2.0 mIU/l for 36-84 months. Results: Neck US of all patients, 3 months after TT, presented no evidence of abnormal residual tissues or metastatic lymph nodes (negative neck US); at this time, the mean Tg level was 0.42 ng/ml. Six months after surgery, after rhTSH, the mean thyroid bed uptake was 1.82%, and Tg levels ranged from 0.10 to 22.30 ng/ml (mean, 2.89 ng/ml). The patients were followed up without any sign of recurrence (negative neck US and stable or decreasing Tg levels). During the ongoing follow-up, the Tg trend was stable or decreasing, independently of the initial suppressed or stimulated Tg level, or WBS uptake. Conclusions: In patients with low-risk differentiated thyroid cancer, who were operated by TT and who did not undergo RRA, an excellent response to treatment may be confirmed by annual neck US and Tg trend.

© 2015 European Thyroid Association Published by S. Karger AG, Basel


References

  1. Veiga LHS, Neta G, Aschebrook-Kilfoy B, Ron E, Devesa SS: Thyroid cancer incidence patterns in Sao Paulo, Brazil, and the US SEER Program, 1997-2008. Thyroid 2013;23:748-757.
  2. Ito Y, Nikiforov YE, Schlumberger M, Vigneri R: Increasing incidence of thyroid cancer: controversies explored. Nat Rev Endocrinol 2013;9:178-184.
  3. Davies L, Welch HG: Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 2006;295:2164-2167.
  4. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer; Cooper DS, Doherty GM, Haugen BR, Hauger BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM: Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167-1214.
  5. Brito JP, Morris JC, Montori VM: Thyroid cancer: zealous imaging has increased detection and treatment of low risk tumours. BMJ 2013;347:f4706-f4706.
  6. Ahn HS, Kim HJ, Welch G: Korea's Thyroid-Cancer ‘Epidemic' Screening and Overdiagnosis. N Engl J Med 2014;371:1765-1767.
  7. Brito JP, Hay ID, Morris JC: Low risk papillary thyroid cancer. BMJ 2014;348:g3045-g3045.
  8. Rosario PW, Ward LS, Carvalho GA, Graf H, Maciel RMB, Maciel LMZ, Maia AL, Vaisman M: Thyroid nodules and differentiated thyroid cancer: update on the Brazilian consensus. Arq Brasil Endocrinol Metab 2013;57:240-264.
  9. Tuttle RM, Sabra MM: Selective use of RAI for ablation and adjuvant therapy after total thyroidectomy for differentiated thyroid cancer: a practical approach to clinical decision making. Oral Oncol 2013;49:676-683.
  10. Tuttle RM, Tala H, Shah J, Leboeuf R, Ghossein R, Gonen M, Brokhin M, Omry G, Fagin JA, Shaha A: Estimating risk of recurrence in differentiated thyroid cancer after total thyroidectomy and radioactive iodine remnant ablation: using response to therapy variables to modify the initial risk estimates predicted by the New American Thyroid Association staging system. Thyroid 2010;20:1341-1349.
  11. Schlumberger M, Catargi B, Borget I, Deandreis D, Zerdoud S, Bridji B, Bardet S, Leenhardt L, Bastie D, Schvartz C, Vera P, Morel O, Benisvy D, Bournaud C, Bonichon F, Dejax C, Toubert M-E, Leboulleux S, Ricard M, Benhamou E; Tumeurs de la Thyroïde Refractaires Network for the Essai Stimulation Ablation Equivalence Trial: Strategies of radioiodine ablation in patients with low-risk thyroid cancer. N Engl J Med 2012;366:1663-1673.
  12. Cho YY, Lim J, Oh C-M, Ryu J, Jung K-W, Chung JH, Won Y-J, Kim SW: Elevated risks of subsequent primary malignancies in patients with thyroid cancer: a nationwide, population-based study in Korea. Cancer 2015;121:259-268.
  13. Sawka AM, Thabane L, Parlea L, Ibrahim-Zada I, Tsang RW, Brierley JD, Straus S, Ezzat S, Goldstein DP: Second primary malignancy risk after radioactive iodine treatment for thyroid cancer: a systematic review and meta-analysis. Thyroid 2009;19:451-457.
  14. Iyer NG, Morris LGT, Tuttle RM, Shaha AR, Ganly I: Rising incidence of second cancers in patients with low-risk (T1N0) thyroid cancer who receive radioactive iodine therapy. Cancer 2011;117:4439-4446.
  15. Almeida JP, Sanabria AE, Lima ENP, Kowalski LP: Late side effects of radioactive iodine on salivary gland function in patients with thyroid cancer. Head Neck 2011;33:686-690.
  16. Mandel SJ, Mandel L: Radioactive iodine and the salivary glands. Thyroid 2003;13:265-271.
  17. Roman BR, Feingold JH, Patel SG, Shaha AR, Shah JP, Tuttle RM, Epstein AJ: The 2009 American Thyroid Association guidelines modestly reduced radioactive iodine use for thyroid cancers less than 1 cm. Thyroid 2014;24:1549-1550.
  18. Lamartina L, Durante C, Filetti S, Cooper DS: Low-risk differentiated thyroid cancer and radioiodine remnant ablation: a systematic review of the literature. J Clin Endocrinol Metab 2015;100:1748-1761.
  19. Durante C, Montesano T, Attard M, Torlontano M, Monzani F, Costante G, Meringolo D, Ferdeghini M, Tumino S, Lamartina L, Paciaroni A, Massa M, Giacomelli L, Ronga G, Filetti S; on behalf of the PTC Study Group: Long-term surveillance of papillary thyroid cancer patients who do not undergo postoperative radioiodine remnant ablation: is there a role for serum thyroglobulin measurement? J Clin Endocrinol Metab 2012;97:2748-2753.
  20. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM: Management guidelines for patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association Guidelines Taskforce. Thyroid 2006;16:1-34.
  21. Durante C, Montesano T, Torlontano M, Attard M, Monzani F, Tumino S, Costante G, Meringolo D, Bruno R, Trulli F, Massa M, Maniglia A, D'Apollo R, Giacomelli L, Ronga G, Filetti S; PTC Study Group: Papillary thyroid cancer: time course of recurrences during postsurgery surveillance. J Clin Endocrinol Metab 2013;98:636-642.
  22. Cano-Palomares A, Castells I, Capel I, Bella MR, Barcons S, Serrano A, Guirao X, Rigla M: Response to initial therapy of differentiated thyroid cancer predicts the long-term outcome better than classical risk stratification systems. Int J Endocrinol 2014;6:1-6.
  23. Castagna MG, Maino F, Cipri C, Belardini V, Theodoropoulou A, Cevenini G, Pacini F: Delayed risk stratification, to include the response to initial treatment (surgery and radioiodine ablation), has better outcome predictivity in differentiated thyroid cancer patients. Eur J Endocrinol 2011;165:441-446.
  24. Pitoia F, Bueno F, Urciuoli C, Abelleira E, Cross G, Tuttle RM: Outcomes of patients with differentiated thyroid cancer risk stratified according to the American Thyroid Association and Latin American Thyroid Society risk of recurrence classification systems. Thyroid 2013;23:1401-1407.
  25. Momesso D, Tuttle RM: Update on differentiated thyroid cancer staging. Endocrinol Metab Clin North Am 2014;43:401-421.
  26. Matsuzu K, Sugino K, Masudo K, Nagahama M, Kitagawa W, Shibuya H, Ohkuwa K, Uruno T, Suzuki A, Magoshi S, Akaishi J, Masaki C, Kawano M, Suganuma N, Rino Y, Masuda M, Kameyama K, Takami H, Ito K: Thyroid lobectomy for papillary thyroid cancer: long-term follow-up study of 1,088 cases. World J Surg 2013;38:68-79.
  27. Ito Y, Miyauchi A: Is surgery necessary for papillary thyroid microcarcinomas? Nat Rev Endocrinol 2011;8:1-1.
  28. Blahd WH, Nordyke RA, Bauer FK: Radioactive iodine (131I) in the postoperative treatment of thyroid cancer. Cancer 1960;13:745-756.
  29. Mazzaferri EL, Jhiang SM: Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 194;97:418-428.
  30. DeGroot LJ: Long-term impact of initial and surgical therapy on papillary and follicular thyroid cancer. Am J Med 1994;97:499-500.
  31. Molinaro E, Giani C, Agate L, Biagini A, Pieruzzi L, Bianchi F, Brozzi F, Ceccarelli C, Viola D, Piaggi P, Vitti P, Pacini F, Elisei R: Patients with differentiated thyroid cancer who underwent radioiodine thyroid remnant ablation with low-activity 131I after either recombinant human TSH or thyroid hormone therapy withdrawal showed the same outcome after a 10-year follow-up. J Clin Endocrinol Metab 2013;98:2693-2700.
  32. Yamazaki CA, Padovani RP, Biscolla RPM, Ikejiri ES, Marchetti RR, Castiglioni MLV, Matsumura LK, Maciel RMB, Furlanetto RP: Lithium as an adjuvant in the postoperative ablation of remnant tissue in low-risk thyroid carcinoma. Thyroid 2012;22:1002-1006.
  33. Padovani RP, Robenshtok E, Brokhin M, Tuttle RM: Even without additional therapy, serum thyroglobulin concentrations often decline for years after total thyroidectomy and radioactive remnant ablation in patients with differentiated thyroid cancer. Thyroid 2012;22:778-783.
  34. Nakabashi CCD, Kasamatsu TS, Crispim F, Yamazaki CA, Camacho CP, Andreoni DM, Padovani RP, Ikejiri ES, Mamone MCOM, Aldighieri FC, Wagner J, Hidal JT, Vieira JGH, Biscolla RPM, Maciel RMB: Basal serum thyroglobulin measured by a second-generation assay is equivalent to stimulated thyroglobulin in identifying metastases in patients with differentiated thyroid cancer with low or intermediate risk of recurrence. Eur Thyroid J 2014;3:43-50.
    External Resources
  35. Brassard M, Borget I, Edet-Sanson A, Giraudet AL, Mundler O, Toubeau M, Bonichon F, Borson-Chazot F, Leenhardt L, Schvartz C, Dejax C, Brenot-Rossi I, Toubert ME, Torlontano M, Benhamou E, Schlumberger M; THYRDIAG Working Group: Long-term follow-up of patients with papillary and follicular thyroid cancer: a prospective study on 715 patients. J Clin Endocrinol Metab 2011;96:1352-1359.

Article / Publication Details

First-Page Preview
Abstract of Clinical Thyroidology / Original Paper

Received: August 13, 2015
Accepted: October 29, 2015
Published online: November 24, 2015
Issue release date: March 2016

Number of Print Pages: 6
Number of Figures: 2
Number of Tables: 2

ISSN: 2235-0640 (Print)
eISSN: 2235-0802 (Online)

For additional information: https://www.karger.com/ETJ

References

  1. Veiga LHS, Neta G, Aschebrook-Kilfoy B, Ron E, Devesa SS: Thyroid cancer incidence patterns in Sao Paulo, Brazil, and the US SEER Program, 1997-2008. Thyroid 2013;23:748-757.
  2. Ito Y, Nikiforov YE, Schlumberger M, Vigneri R: Increasing incidence of thyroid cancer: controversies explored. Nat Rev Endocrinol 2013;9:178-184.
  3. Davies L, Welch HG: Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 2006;295:2164-2167.
  4. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer; Cooper DS, Doherty GM, Haugen BR, Hauger BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM: Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167-1214.
  5. Brito JP, Morris JC, Montori VM: Thyroid cancer: zealous imaging has increased detection and treatment of low risk tumours. BMJ 2013;347:f4706-f4706.
  6. Ahn HS, Kim HJ, Welch G: Korea's Thyroid-Cancer ‘Epidemic' Screening and Overdiagnosis. N Engl J Med 2014;371:1765-1767.
  7. Brito JP, Hay ID, Morris JC: Low risk papillary thyroid cancer. BMJ 2014;348:g3045-g3045.
  8. Rosario PW, Ward LS, Carvalho GA, Graf H, Maciel RMB, Maciel LMZ, Maia AL, Vaisman M: Thyroid nodules and differentiated thyroid cancer: update on the Brazilian consensus. Arq Brasil Endocrinol Metab 2013;57:240-264.
  9. Tuttle RM, Sabra MM: Selective use of RAI for ablation and adjuvant therapy after total thyroidectomy for differentiated thyroid cancer: a practical approach to clinical decision making. Oral Oncol 2013;49:676-683.
  10. Tuttle RM, Tala H, Shah J, Leboeuf R, Ghossein R, Gonen M, Brokhin M, Omry G, Fagin JA, Shaha A: Estimating risk of recurrence in differentiated thyroid cancer after total thyroidectomy and radioactive iodine remnant ablation: using response to therapy variables to modify the initial risk estimates predicted by the New American Thyroid Association staging system. Thyroid 2010;20:1341-1349.
  11. Schlumberger M, Catargi B, Borget I, Deandreis D, Zerdoud S, Bridji B, Bardet S, Leenhardt L, Bastie D, Schvartz C, Vera P, Morel O, Benisvy D, Bournaud C, Bonichon F, Dejax C, Toubert M-E, Leboulleux S, Ricard M, Benhamou E; Tumeurs de la Thyroïde Refractaires Network for the Essai Stimulation Ablation Equivalence Trial: Strategies of radioiodine ablation in patients with low-risk thyroid cancer. N Engl J Med 2012;366:1663-1673.
  12. Cho YY, Lim J, Oh C-M, Ryu J, Jung K-W, Chung JH, Won Y-J, Kim SW: Elevated risks of subsequent primary malignancies in patients with thyroid cancer: a nationwide, population-based study in Korea. Cancer 2015;121:259-268.
  13. Sawka AM, Thabane L, Parlea L, Ibrahim-Zada I, Tsang RW, Brierley JD, Straus S, Ezzat S, Goldstein DP: Second primary malignancy risk after radioactive iodine treatment for thyroid cancer: a systematic review and meta-analysis. Thyroid 2009;19:451-457.
  14. Iyer NG, Morris LGT, Tuttle RM, Shaha AR, Ganly I: Rising incidence of second cancers in patients with low-risk (T1N0) thyroid cancer who receive radioactive iodine therapy. Cancer 2011;117:4439-4446.
  15. Almeida JP, Sanabria AE, Lima ENP, Kowalski LP: Late side effects of radioactive iodine on salivary gland function in patients with thyroid cancer. Head Neck 2011;33:686-690.
  16. Mandel SJ, Mandel L: Radioactive iodine and the salivary glands. Thyroid 2003;13:265-271.
  17. Roman BR, Feingold JH, Patel SG, Shaha AR, Shah JP, Tuttle RM, Epstein AJ: The 2009 American Thyroid Association guidelines modestly reduced radioactive iodine use for thyroid cancers less than 1 cm. Thyroid 2014;24:1549-1550.
  18. Lamartina L, Durante C, Filetti S, Cooper DS: Low-risk differentiated thyroid cancer and radioiodine remnant ablation: a systematic review of the literature. J Clin Endocrinol Metab 2015;100:1748-1761.
  19. Durante C, Montesano T, Attard M, Torlontano M, Monzani F, Costante G, Meringolo D, Ferdeghini M, Tumino S, Lamartina L, Paciaroni A, Massa M, Giacomelli L, Ronga G, Filetti S; on behalf of the PTC Study Group: Long-term surveillance of papillary thyroid cancer patients who do not undergo postoperative radioiodine remnant ablation: is there a role for serum thyroglobulin measurement? J Clin Endocrinol Metab 2012;97:2748-2753.
  20. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM: Management guidelines for patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association Guidelines Taskforce. Thyroid 2006;16:1-34.
  21. Durante C, Montesano T, Torlontano M, Attard M, Monzani F, Tumino S, Costante G, Meringolo D, Bruno R, Trulli F, Massa M, Maniglia A, D'Apollo R, Giacomelli L, Ronga G, Filetti S; PTC Study Group: Papillary thyroid cancer: time course of recurrences during postsurgery surveillance. J Clin Endocrinol Metab 2013;98:636-642.
  22. Cano-Palomares A, Castells I, Capel I, Bella MR, Barcons S, Serrano A, Guirao X, Rigla M: Response to initial therapy of differentiated thyroid cancer predicts the long-term outcome better than classical risk stratification systems. Int J Endocrinol 2014;6:1-6.
  23. Castagna MG, Maino F, Cipri C, Belardini V, Theodoropoulou A, Cevenini G, Pacini F: Delayed risk stratification, to include the response to initial treatment (surgery and radioiodine ablation), has better outcome predictivity in differentiated thyroid cancer patients. Eur J Endocrinol 2011;165:441-446.
  24. Pitoia F, Bueno F, Urciuoli C, Abelleira E, Cross G, Tuttle RM: Outcomes of patients with differentiated thyroid cancer risk stratified according to the American Thyroid Association and Latin American Thyroid Society risk of recurrence classification systems. Thyroid 2013;23:1401-1407.
  25. Momesso D, Tuttle RM: Update on differentiated thyroid cancer staging. Endocrinol Metab Clin North Am 2014;43:401-421.
  26. Matsuzu K, Sugino K, Masudo K, Nagahama M, Kitagawa W, Shibuya H, Ohkuwa K, Uruno T, Suzuki A, Magoshi S, Akaishi J, Masaki C, Kawano M, Suganuma N, Rino Y, Masuda M, Kameyama K, Takami H, Ito K: Thyroid lobectomy for papillary thyroid cancer: long-term follow-up study of 1,088 cases. World J Surg 2013;38:68-79.
  27. Ito Y, Miyauchi A: Is surgery necessary for papillary thyroid microcarcinomas? Nat Rev Endocrinol 2011;8:1-1.
  28. Blahd WH, Nordyke RA, Bauer FK: Radioactive iodine (131I) in the postoperative treatment of thyroid cancer. Cancer 1960;13:745-756.
  29. Mazzaferri EL, Jhiang SM: Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 194;97:418-428.
  30. DeGroot LJ: Long-term impact of initial and surgical therapy on papillary and follicular thyroid cancer. Am J Med 1994;97:499-500.
  31. Molinaro E, Giani C, Agate L, Biagini A, Pieruzzi L, Bianchi F, Brozzi F, Ceccarelli C, Viola D, Piaggi P, Vitti P, Pacini F, Elisei R: Patients with differentiated thyroid cancer who underwent radioiodine thyroid remnant ablation with low-activity 131I after either recombinant human TSH or thyroid hormone therapy withdrawal showed the same outcome after a 10-year follow-up. J Clin Endocrinol Metab 2013;98:2693-2700.
  32. Yamazaki CA, Padovani RP, Biscolla RPM, Ikejiri ES, Marchetti RR, Castiglioni MLV, Matsumura LK, Maciel RMB, Furlanetto RP: Lithium as an adjuvant in the postoperative ablation of remnant tissue in low-risk thyroid carcinoma. Thyroid 2012;22:1002-1006.
  33. Padovani RP, Robenshtok E, Brokhin M, Tuttle RM: Even without additional therapy, serum thyroglobulin concentrations often decline for years after total thyroidectomy and radioactive remnant ablation in patients with differentiated thyroid cancer. Thyroid 2012;22:778-783.
  34. Nakabashi CCD, Kasamatsu TS, Crispim F, Yamazaki CA, Camacho CP, Andreoni DM, Padovani RP, Ikejiri ES, Mamone MCOM, Aldighieri FC, Wagner J, Hidal JT, Vieira JGH, Biscolla RPM, Maciel RMB: Basal serum thyroglobulin measured by a second-generation assay is equivalent to stimulated thyroglobulin in identifying metastases in patients with differentiated thyroid cancer with low or intermediate risk of recurrence. Eur Thyroid J 2014;3:43-50.
    External Resources
  35. Brassard M, Borget I, Edet-Sanson A, Giraudet AL, Mundler O, Toubeau M, Bonichon F, Borson-Chazot F, Leenhardt L, Schvartz C, Dejax C, Brenot-Rossi I, Toubert ME, Torlontano M, Benhamou E, Schlumberger M; THYRDIAG Working Group: Long-term follow-up of patients with papillary and follicular thyroid cancer: a prospective study on 715 patients. J Clin Endocrinol Metab 2011;96:1352-1359.
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