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Langenbeck's Archives of Surgery

, Volume 403, Issue 3, pp 325–332 | Cite as

Risk of recurrence in a homogeneously managed pT3-differentiated thyroid carcinoma population

  • Nathalie Chereau
  • Etienne Dauzier
  • Gaëlle Godiris–Petit
  • Séverine Noullet
  • Isabelle Brocheriou
  • Laurence Leenhardt
  • Camille Buffet
  • Fabrice Menegaux
ORIGINAL ARTICLE
  • 86 Downloads

Abstract

Background

International guidelines for the management of differentiated thyroid cancers are based on the 7th TNM classification: pT3 tumors are defined as differentiated thyroid cancers (DTCs) measuring more than 4 cm in their greatest dimension that are limited to the thyroid or any tumor with minimal extrathyroidal extension (ETE; sternothyroid muscle or perithyroid soft tissues). Differences in clinicohistological features and prognosis among patients with pT3 tumors remain controversial, and studies regarding pT3 subgroups are lacking.

Objective

To analyze the prognosis of four subgroups of pT3 DTCs (papillary, PTC; or follicular, FTC).

Design and setting

The data of patients who underwent surgery for pT3 DTC between 1978 and 2015 in a surgical department specialized in endocrine surgery were reviewed. Patients were classified into four groups as follows: the pT3a (≤ 10 mm with ETE), pT3b (10–40 mm with ETE), pT3c (> 40 mm without ETE), and pT3d groups (> 40 mm with ETE). Recurrence-free survival (RFS) was analyzed using the Kaplan-Meier method.

Results

One thousand eighty-eight patients with pT3 DTC were included, of whom 311 (29%) had pT3a; 548 (50%), pT3b; 165 (15%), pT3c; and 64 (6%), pT3d. For the 916 patients with lymph node (LN) dissection, metastatic LNs were more frequent in the pT3b and pT3d groups (61 and 61%, respectively) than in the other groups (44% pT3a and 10% pT3c; p < 0.001). During the median follow-up period of 9 years (range, 2–38 years), recurrence occurred in 169 patients with T3 tumors (16%), including 18 with pT3a (6%), 100 with pT3b (18%), 20 with pT3c (12%), and 31 with pT3d (48%). In a multivariate analysis, LN metastases (< 0.0001), extranodal extension (p = 0.03), FTC (vs. PTC) (p = 0.006), pT3b (p = 0.016), and pT3d (p = 0.047) were associated with an increased risk of recurrence. The 5-year RFS rates were 94.5, 82.2, 91.1, and 50.3% for the pT3a, pT3b, pT3c, and pT3d groups, respectively (p < 0.01).

Conclusion

Except for microcarcinoma, the risk of LN involvement is high and similar for the DTC patients with minimal ETE, regardless of the size of the tumor. The association of a tumor size of > 4 cm and ETE are associated with a poor prognosis and should justify the classification of these cases as a high-risk group. Other pT3 patients with no LN metastases could be individualized as a low-risk group.

Keywords

Thyroid cancer, well differentiated, papillary, follicular Clinicopathological features Lymph node dissection Neoplasm recurrence, local Tumor staging 

Notes

Acknowledgments

We thank the following individuals for their assistance in this study: Romain Ducoudray (MD), Héloïse Bergeret-Cassagne (MD), Anna Carteaux-Taieb (MD), Benedetto Cali (MD), and Christophe Tresallet (MD, PhD).

Authors’ contributions

Study conception and design were performed by Chereau, Dauzier, Godiris Petit, Noullet, Leenhardt, Buffet, and Menegaux. Data acquisition was performed by Chereau, Dauzier, Godiris Petit, Noullet, Brocheriou, Leenhardt, Buffet, and Menegaux. Data analysis and interpretation were performed by Dauzier, Chereau, and Menegaux. Drafting of manuscript was performed by Chereau, Dauzier, and Menegaux. Critical revision of manuscript was performed by Buffet, Leenhardt, and Menegaux.

Compliance with ethical standards

For this type of study, formal consent is not required. Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Lim H, Devesa SS, Sosa JA, Check D, Kitahara CM (2017) Trends in thyroid cancer incidence and mortality in the United States, 1974–2013. JAMA 317(13):1338–1348.  https://doi.org/10.1001/jama.2017.2719 CrossRefPubMedGoogle Scholar
  2. 2.
    Tuttle RM, Tala H, Shah J, Leboeuf R, Ghossein R, Gonen M, Brokhin M, Omry G, Fagin JA, Shaha A (2010) 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 20(12):1341–1349.  https://doi.org/10.1089/thy.2010.0178 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Lang B, Lo C-Y, Chan W-F, Lam K-Y, Wan K-Y (2007) Restaging of differentiated thyroid carcinoma by the sixth edition AJCC/UICC TNM staging system: stage migration and predictability. Ann Surg Oncol 14(5):1551–1559.  https://doi.org/10.1245/s10434-006-9242-2 CrossRefPubMedGoogle Scholar
  4. 4.
    Edge SB, Compton CC (2010) The American joint committee on cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17(6):1471–1474.  https://doi.org/10.1245/s10434-010-0985-4 CrossRefPubMedGoogle Scholar
  5. 5.
    Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JWA, Wiersinga W, European Thyroid Cancer Taskforce (2006) European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol Eur Fed Endocr Soc 154(6):787–803.  https://doi.org/10.1530/eje.1.02158 CrossRefGoogle Scholar
  6. 6.
    Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L (2016) 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 26(1):1–133.  https://doi.org/10.1089/thy.2015.0020 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Moon HJ, Kim E-K, Chung WY, Yoon JH, Kwak JY (2011) Minimal extrathyroidal extension in patients with papillary thyroid microcarcinoma: is it a real prognostic factor? Ann Surg Oncol 18(7):1916–1923.  https://doi.org/10.1245/s10434-011-1556-z CrossRefPubMedGoogle Scholar
  8. 8.
    Chereau N, Buffet C, Trésallet C, Tissier F, Golmard J-L, Leenhardt L et al (2014) Does extracapsular extension impact the prognosis of papillary thyroid microcarcinoma? Ann Surg Oncol 21(5):1659–1664.  https://doi.org/10.1245/s10434-013-3447-y CrossRefPubMedGoogle Scholar
  9. 9.
    Youngwirth LM, Adam MA, Scheri RP, Roman SA, Sosa JA (2017) Extrathyroidal extension is associated with compromised survival in patients with thyroid cancer. Thyroid 27(5):626–631.  https://doi.org/10.1089/thy.2016.0132 CrossRefPubMedGoogle Scholar
  10. 10.
    Ito Y, Tomoda C, Uruno T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, Kuma K, Miyauchi A (2006) Prognostic significance of extrathyroid extension of papillary thyroid carcinoma: massive but not minimal extension affects the relapse-free survival. World J Surg 30(5):780–786.  https://doi.org/10.1007/s00268-005-0270-z CrossRefPubMedGoogle Scholar
  11. 11.
    Shin JH, Ha TK, Park HK, Ahn MS, Kim KH, Bae KB, Kim TH, Choi CS, Kim TK, Bae SK, Kim SH (2013) Implication of minimal extrathyroidal extension as a prognostic factor in papillary thyroid carcinoma. Int J Surg 11(9):944–947.  https://doi.org/10.1016/j.ijsu.2013.06.015 CrossRefPubMedGoogle Scholar
  12. 12.
    Al Afif A, Williams BA, Rigby MH, Bullock MJ, Taylor SM, Trites J, Hart RD (2015) Multifocal papillary thyroid cancer increases the risk of central lymph node metastasis. Thyroid 25(9):1008–1012.  https://doi.org/10.1089/thy.2015.0130 CrossRefPubMedGoogle Scholar
  13. 13.
    Tallini G, Tuttle RM, Ghossein RA (2016) The history of the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 102(1):15–22Google Scholar
  14. 14.
    Yu XM, Schneider DF, Leverson G, Chen H, Sippel RS (2013) Follicular variant of papillary thyroid carcinoma is a unique clinical entity: a population-based study of 10,740 cases. Thyroid 23(10):1263–1268.  https://doi.org/10.1089/thy.2012.0453 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Yang J, Gong Y, Yan S, Shi Q, Zhu J, Li Z, Gong R (2015) Comparison of the clinicopathological behavior of the follicular variant of papillary thyroid carcinoma and classical papillary thyroid carcinoma: a systematic review and meta-analysis. Mol Clin Oncol 3(4):753–764.  https://doi.org/10.3892/mco.2015.540 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    O’Neill CJ, Vaughan L, Learoyd DL, Sidhu SB, Delbridge LW, Sywak MS (2011) Management of follicular thyroid carcinoma should be individualised based on degree of capsular and vascular invasion. Eur J Surg Oncol 37(2):181–185.  https://doi.org/10.1016/j.ejso.2010.11.005 CrossRefPubMedGoogle Scholar
  17. 17.
    O’Connell K, Yen TW, Quiroz F, Evans DB, Wang TS (2013) The utility of routine preoperative cervical ultrasonography in patients undergoing thyroidectomy for differentiated thyroid cancer. Surgery 154(4):697–701-703.  https://doi.org/10.1016/j.surg.2013.06.040 CrossRefPubMedGoogle Scholar
  18. 18.
    Hartl DM, Leboulleux S, Al Ghuzlan A, Baudin E, Chami L, Schlumberger M, Travagli JP (2012) Optimization of staging of the neck with prophylactic central and lateral neck dissection for papillary thyroid carcinoma. Ann Surg 255(4):777–783.  https://doi.org/10.1097/SLA.0b013e31824b7b68 CrossRefPubMedGoogle Scholar
  19. 19.
    Chéreau N, Buffet C, Trésallet C, Tissier F, Leenhardt L, Menegaux F (2016) Recurrence of papillary thyroid carcinoma with lateral cervical node metastases: predictive factors and operative management. Surgery 159(3):755–762.  https://doi.org/10.1016/j.surg.2015.08.033 CrossRefPubMedGoogle Scholar
  20. 20.
    So YK, Seo MY, Son YI (2012) Prophylactic central lymph node dissection for clinically node-negative papillary thyroid microcarcinoma: influence on serum thyroglobulin level, recurrence rate, and postoperative complications. Surgery 151(2):192–198.  https://doi.org/10.1016/j.surg.2011.02.004 CrossRefPubMedGoogle Scholar
  21. 21.
    Roh JL, Park JY, Park CI (2007) Total thyroidectomy plus neck dissection in differentiated papillary thyroid carcinoma patients: pattern of nodal metastasis, morbidity, recurrence, and postoperative levels of serum parathyroid hormone. Ann Surg 245(4):604–610.  https://doi.org/10.1097/01.sla.0000250451.59685.67 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Lifante JC, Payet C, Ménégaux F, Sebag F, Kraimps JL, Peix JL et al (2017) Can we consider immediate complications after thyroidectomy as a quality metric of operation? Surgery 161(1):156–165.  https://doi.org/10.1016/j.surg.2016.04.049 CrossRefPubMedGoogle Scholar
  23. 23.
    Roh JL, Kim JM, Park CI (2011) Central compartment reoperation for recurrent/persistent differentiated thyroid cancer: patterns of recurrence, morbidity, and prediction of postoperative hypocalcemia. Ann Surg Oncol 18(5):1312–1318.  https://doi.org/10.1245/s10434-010-1470-9 CrossRefPubMedGoogle Scholar
  24. 24.
    Clain JB, Scherl S, Dos Reis L, Turk A, Wenig BM, Mehra S, Karle WE, Urken ML (2014) Extrathyroidal extension predicts extranodal extension in patients with positive lymph nodes: an important association that may affect clinical management. Thyroid 24(6):951–957.  https://doi.org/10.1089/thy.2013.0557 CrossRefPubMedGoogle Scholar
  25. 25.
    Suh S, Pak K, Seok JW, Kim IJ (2016) Prognostic value of extranodal extension in thyroid cancer: a meta-analysis. Yonsei Med J 57(6):1324–1328.  https://doi.org/10.3349/ymj.2016.57.6.1324 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ruel E, Thomas S, Dinan M, Perkins JM, Roman SA, Sosa JA (2015) Adjuvant radioactive iodine therapy is associated with improved survival for patients with intermediate-risk papillary thyroid cancer. J Clin Endocrinol Metab 100(4):1529–1536.  https://doi.org/10.1210/jc.2014-4332 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zerdoud S et al (2017) Radioactive iodine therapy, molecular imaging and serum biomarkers for differentiated thyroid cancer: 2017 guidelines of the French Societies of Nuclear Medicine, Endocrinology, Pathology, Biology, Endocrine Surgery and Head and Neck Surgery. Annales d’Endocrinologie. Elsevier MassonGoogle Scholar
  28. 28.
    Vaisman F, Shaha A, Fish S, Michael Tuttle R (2011) Initial therapy with either thyroid lobectomy or total thyroidectomy without radioactive iodine remnant ablation is associated with very low rates of structural disease recurrence in properly selected patients with differentiated thyroid cancer. Clin Endocrinol 75(1):112–119.  https://doi.org/10.1111/j.1365-2265.2011.04002.x CrossRefGoogle Scholar
  29. 29.
    Mallick U, Harmer C, Yap B, Wadsley J, Clarke S, Moss L, Nicol A, Clark PM, Farnell K, McCready R, Smellie J, Franklyn JA, John R, Nutting CM, Newbold K, Lemon C, Gerrard G, Abdel-Hamid A, Hardman J, Macias E, Roques T, Whitaker S, Vijayan R, Alvarez P, Beare S, Forsyth S, Kadalayil L, Hackshaw A (2012) Ablation with low-dose radioiodine and thyrotropin alfa in thyroid cancer. N Engl J Med 366(18):1674–1685.  https://doi.org/10.1056/NEJMoa1109589 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Nathalie Chereau
    • 1
  • Etienne Dauzier
    • 1
  • Gaëlle Godiris–Petit
    • 1
  • Séverine Noullet
    • 1
  • Isabelle Brocheriou
    • 2
  • Laurence Leenhardt
    • 3
  • Camille Buffet
    • 3
  • Fabrice Menegaux
    • 1
  1. 1.Department of General, Visceral, and Endocrine SurgeryPitié Salpêtrière Hospital, AP-HP, Sorbonne UniversitéParisFrance
  2. 2.Department of PathologyPitié Salpêtrière Hospital, AP-HP, Sorbonne UniversitéParisFrance
  3. 3.Department of Endocrinology, Thyroid and Endocrine Tumors UnitPitié Salpêtrière Hospital, AP-HP, Sorbonne UniversitéParisFrance

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