Ultrasonography.  2017 Oct;36(4):292-299. 10.14366/usg.17023.

Updated guidelines on the preoperative staging of thyroid cancer

• Kim HJ

• KMID: 2393095
• DOI: http://doi.org/10.14366/usg.17023

Abstract

Recent studies have provided prognostic information and recommendations for staging thyroid cancers that have changed the staging and management guidelines for the disease. Consequently, minimal extrathyroidal extension (ETE) was removed from the T3 stage classification in the eighth edition of the TNM staging system by the American Joint Committee on Cancer. New T categories have been subsequently added, including T3a, defined as a tumor >4 cm in its greatest dimension, limited to the thyroid gland, and T3b, defined as a tumor of any size with gross ETE invading only the strap muscles. In this article, the author reviews the changes in the TNM staging system for thyroid cancer, with an emphasis on ultrasonography in preoperative staging.

Keyword

Thyroid neoplasms; Neoplasm staging; Ultrasonography

MeSH Terms

Classification
Joints
Muscles
Neoplasm Staging
Thyroid Gland*
Thyroid Neoplasms*
Ultrasonography

Figure

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  Fig. 1. A 70-year-old woman with minimal extrathyroidal extension.Transverse (A) and longitudinal (B) ultrasonography reveals a 1.5-cm solid mass in the left lobe, abutting the thyroid capsule with an invisible thyroid capsule (arrows) overlying the mass. The pathologic T category is T1b.

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  Fig. 2. A 39-year-old woman with gross extrathyroidal extension.Transverse (A) and longitudinal (B) ultrasonography demonstrates a 1.0-cm solid mass in the right lobe, bulging from the normal thyroid contour with an invisible thyroid capsule (arrows) overlying the mass. The pathologic T category is T3b.

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  Fig. 3. A 55-year-old woman with gross invasion of the recurrent laryngeal nerve.Transverse (A) and longitudinal (B) ultrasonography shows a 1.0-cm solid mass in the left lobe, bulging from the normal thyroid contour with an invisible thyroid capsule (arrows) overlying the mass. Even though ultrasonography cannot directly assess recurrent laryngeal nerve invasion, this can be expected considering the tumor location. Recurrent laryngeal nerve invasion was confirmed pathologically. Therefore, the pathologic T category is T4a.

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  Fig. 4. A 32-year-old woman with metastatic lymph nodes on the left side of the neck.Transverse (A) and longitudinal (B) ultrasonography shows the loss of fatty hilum, microcalcifications, hyperechogenicity, and cystic changes (arrows) in the lymph node.

Reference

References

1. American Cancer Society. Cancer facts and figures 2016. Atlanta, GA: American Cancer Society;2016.

2. Hundahl SA, Fleming ID, Fremgen AM, Menck HR. A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995 [see commetns]. Cancer. 1998; 83:2638–2648.

3. Oh CM, Won YJ, Jung KW, Kong HJ, Cho H, Lee JK, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2013. Cancer Res Treat. 2016; 48:436–450.

4. Korean Central Cancer Registry; Ministry of Health and Welfare. Annual report of cancer statistics in Korea in 2014. Sejong: Ministry of Health and Welfare;2016.

5. Cho BY, Choi HS, Park YJ, Lim JA, Ahn HY, Lee EK, et al. Changes in the clinicopathological characteristics and outcomes of thyroid cancer in Korea over the past four decades. Thyroid. 2013; 23:797–804.

6. Ahn HS, Kim HJ, Welch HG. Korea's thyroid-cancer "epidemic": screening and overdiagnosis. N Engl J Med. 2014; 371:1765–1767.

7. Choi JS, Chung WY, Kwak JY, Moon HJ, Kim MJ, Kim EK. Staging of papillary thyroid carcinoma with ultrasonography: performance in a large series. Ann Surg Oncol. 2011; 18:3572–3578.

8. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 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. 2016; 26:1–133.

9. Amin MB, Edge S, Greene F, Byrd DR, Brookland RK, Washington MK, et al. AJCC cancer staging manual. 8th ed. New York: Springer;2017.

10. Kwak JY, Kim EK, Youk JH, Kim MJ, Son EJ, Choi SH, et al. Extrathyroid extension of well-differentiated papillary thyroid microcarcinoma on US. Thyroid. 2008; 18:609–614.

11. Park JS, Son KR, Na DG, Kim E, Kim S. Performance of preoperative sonographic staging of papillary thyroid carcinoma based on the sixth edition of the AJCC/UICC TNM classification system. AJR Am J Roentgenol. 2009; 192:66–72.

12. Choi JS, Kim J, Kwak JY, Kim MJ, Chang HS, Kim EK. Preoperative staging of papillary thyroid carcinoma: comparison of ultrasound imaging and CT. AJR Am J Roentgenol. 2009; 193:871–878.

13. Moon HJ, Kim EK, Yoon JH, Kwak JY. Clinical implication of elastography as a prognostic factor of papillary thyroid microcarcinoma. Ann Surg Oncol. 2012; 19:2279–2287.

14. Park YJ, Kim JA, Son EJ, Youk JH, Park CS. Quantitative shear wave elastography as a prognostic implication of papillary thyroid carcinoma (PTC): elasticity index can predict extrathyroidal extension (ETE). Ann Surg Oncol. 2013; 20:2765–2771.

15. Jin ZQ, Lin MY, Hu WH, Li WY, Bai SJ. Gray-scale ultrasonography combined with elastography imaging for the evaluation of papillary thyroid microcarcinoma: as a prognostic clinicopathology factor. Ultrasound Med Biol. 2014; 40:1769–1777.

16. Gweon HM, Son EJ, Youk JH, Kim JA, Park CS. Preoperative assessment of extrathyroidal extension of papillary thyroid carcinoma: comparison of 2- and 3-dimensional sonography. J Ultrasound Med. 2014; 33:819–825.

17. Mete O, Rotstein L, Asa SL. Controversies in thyroid pathology: thyroid capsule invasion and extrathyroidal extension. Ann Surg Oncol. 2010; 17:386–391.

18. Jukkola A, Bloigu R, Ebeling T, Salmela P, Blanco G. Prognostic factors in differentiated thyroid carcinomas and their implications for current staging classifications. Endocr Relat Cancer. 2004; 11:571–579.

19. Ito Y, Tomoda C, Uruno T, Takamura Y, Miya A, Kobayashi K, et al. Prognostic significance of extrathyroid extension of papillary thyroid carcinoma: massive but not minimal extension affects the relapse-free survival. World J Surg. 2006; 30:780–786.

20. Nixon IJ, Ganly I, Patel S, Palmer FL, Whitcher MM, Tuttle RM, et al. The impact of microscopic extrathyroid extension on outcome in patients with clinical T1 and T2 well-differentiated thyroid cancer. Surgery. 2011; 150:1242–1249.

21. Radowsky JS, Howard RS, Burch HB, Stojadinovic A. Impact of degree of extrathyroidal extension of disease on papillary thyroid cancer outcome. Thyroid. 2014; 24:241–244.

22. Andersen PE, Kinsella J, Loree TR, Shaha AR, Shah JP. Differentiated carcinoma of the thyroid with extrathyroidal extension. Am J Surg. 1995; 170:467–470.

23. Bellantone R, Lombardi CP, Boscherini M, Ferrante A, Raffaelli M, Rubino F, et al. Prognostic factors in differentiated thyroid carcinoma: a multivariate analysis of 234 consecutive patients. J Surg Oncol. 1998; 68:237–241.

24. Rim JH, Chong S, Ryu HS, Chung BM, Ahn HS. Feasibility study of ultrasonographic criteria for microscopic and macroscopic extra-thyroidal extension based on thyroid capsular continuity and tumor contour in patients with papillary thyroid carcinomas. Ultrasound Med Biol. 2016; 42:2391–2400.

25. Kebebew E, Greenspan FS, Clark OH, Woeber KA, McMillan A. Anaplastic thyroid carcinoma. Treatment outcome and prognostic factors. Cancer. 2005; 103:1330–1335.

26. Smallridge RC, Ain KB, Asa SL, Bible KC, Brierley JD, Burman KD, et al. American Thyroid Association guidelines for management of patients with anaplastic thyroid cancer. Thyroid. 2012; 22:1104–1139.

27. American Thyroid Association Surgery Working Group; American Association of Endocrine Surgeons; American Academy of Otolaryngology-Head and Neck Surgery; American Head and Neck Society, Carty SE, Cooper DS, et al. Consensus statement on the terminology and classification of central neck dissection for thyroid cancer. Thyroid. 2009; 19:1153–1158.

28. Sohn YM, Kwak JY, Kim EK, Moon HJ, Kim SJ, Kim MJ. Diagnostic approach for evaluation of lymph node metastasis from thyroid cancer using ultrasound and fine-needle aspiration biopsy. AJR Am J Roentgenol. 2010; 194:38–43.

29. Na DG, Lim HK, Byun HS, Kim HD, Ko YH, Baek JH. Differential diagnosis of cervical lymphadenopathy: usefulness of color Doppler sonography. AJR Am J Roentgenol. 1997; 168:1311–1316.

30. Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid. 2008; 18:411–418.

31. Shin JH, Baek JH, Chung J, Ha EJ, Kim JH, Lee YH, et al. Ultrasonography diagnosis and imaging-based management of thyroid nodules: revised Korean Society of Thyroid Radiology consensus statement and recommendations. Korean J Radiol. 2016; 17:370–395.

32. Cignarelli M, Ambrosi A, Marino A, Lamacchia O, Campo M, Picca G, et al. Diagnostic utility of thyroglobulin detection in fine-needle aspiration of cervical cystic metastatic lymph nodes from papillary thyroid cancer with negative cytology. Thyroid. 2003; 13:1163–1167.

33. Boi F, Baghino G, Atzeni F, Lai ML, Faa G, Mariotti S. The diagnostic value for differentiated thyroid carcinoma metastases of thyroglobulin (Tg) measurement in washout fluid from fine-needle aspiration biopsy of neck lymph nodes is maintained in the presence of circulating anti-Tg antibodies. J Clin Endocrinol Metab. 2006; 91:1364–1369.

34. Roh JL, Park JY, Kim JM, Song CJ. Use of preoperative ultrasonography as guidance for neck dissection in patients with papillary thyroid carcinoma. J Surg Oncol. 2009; 99:28–31.

35. Loevner LA, Kaplan SL, Cunnane ME, Moonis G. Cross-sectional imaging of the thyroid gland. Neuroimaging Clin N Am. 2008; 18:445–461.

36. Wang TS, Cheung K, Farrokhyar F, Roman SA, Sosa JA. A meta-analysis of the effect of prophylactic central compartment neck dissection on locoregional recurrence rates in patients with papillary thyroid cancer. Ann Surg Oncol. 2013; 20:3477–3483.

37. Gyorki DE, Untch B, Tuttle RM, Shaha AR. Prophylactic central neck dissection in differentiated thyroid cancer: an assessment of the evidence. Ann Surg Oncol. 2013; 20:2285–2289.

38. Randolph GW, Duh QY, Heller KS, LiVolsi VA, Mandel SJ, Steward DL, et al. The prognostic significance of nodal metastases from papillary thyroid carcinoma can be stratified based on the size and number of metastatic lymph nodes, as well as the presence of extranodal extension. Thyroid. 2012; 22:1144–1152.

39. Moreno MA, Edeiken-Monroe BS, Siegel ER, Sherman SI, Clayman GL. In papillary thyroid cancer, preoperative central neck ultrasound detects only macroscopic surgical disease, but negative findings predict excellent long-term regional control and survival. Thyroid. 2012; 22:347–355.

40. Choi YJ, Lee JH, Baek JH. Ultrasound elastography for evaluation of cervical lymph nodes. Ultrasonography. 2015; 34:157–164.

41. Lo WC, Cheng PW, Wang CT, Liao LJ. Real-time ultrasound elastography: an assessment of enlarged cervical lymph nodes. Eur Radiol. 2013; 23:2351–2357.

42. Jung WS, Kim JA, Son EJ, Youk JH, Park CS. Shear wave elastography in evaluation of cervical lymph node metastasis of papillary thyroid carcinoma: elasticity index as a prognostic implication. Ann Surg Oncol. 2015; 22:111–116.

43. Lee HY, Lee JH, Shin JH, Kim SY, Shin HJ, Park JS, et al. Shear wave elastography using ultrasound: effects of anisotropy and stretch stress on a tissue phantom and in vivo reactive lymph nodes in the neck. Ultrasonography. 2017; 36:25–32.

44. Pedersen OM, Aardal NP, Larssen TB, Varhaug JE, Myking O, Vik-Mo H. The value of ultrasonography in predicting autoimmune thyroid disease. Thyroid. 2000; 10:251–259.

45. Kim DW, Eun CK, In HS, Kim MH, Jung SJ, Bae SK. Sonographic differentiation of asymptomatic diffuse thyroid disease from normal thyroid: a prospective study. AJNR Am J Neuroradiol. 2010; 31:1956–1960.

46. Herh SJ, Kim EK, Sung JM, Yoon JH, Moon HJ, Kwak JY. Heterogeneous echogenicity of the thyroid parenchyma does not influence the detection of multi-focality in papillary thyroid carcinoma on preoperative ultrasound staging. Ultrasound Med Biol. 2014; 40:884–889.

47. Lee KJ, Cho YJ, Kim JG, Lee DH. How many contralateral papillary thyroid carcinomas can be missed? World J Surg. 2013; 37:780–785.

48. Moon HJ, Yoon JH, Kwak JY, Chung WY, Nam KH, Jeong JJ, et al. Positive predictive value and interobserver variability of preoperative staging sonography for thyroid carcinoma. AJR Am J Roentgenol. 2011; 197:W324–W330.

49. Paksoy N, Yazal K. Cervical lymphadenopathy associated with Hashimoto's thyroiditis: an analysis of 22 cases by fine needle aspiration cytology. Acta Cytol. 2009; 53:491–496.

50. Kim HJ, Kim NK, Choi JH, Sohn SY, Kim SW, Jin SM, et al. Associations between body mass index and clinico-pathological characteristics of papillary thyroid cancer. Clin Endocrinol (Oxf). 2013; 78:134–140.

51. Tresallet C, Seman M, Tissier F, Buffet C, Lupinacci RM, Vuarnesson H, et al. The incidence of papillary thyroid carcinoma and outcomes in operative patients according to their body mass indices. Surgery. 2014; 156:1145–1152.

52. Choi JS, Lee HS, Kim EK, Moon HJ, Kwak JY. The influence of body mass index on the diagnostic performance of pre-operative staging ultrasound in papillary thyroid carcinoma. Clin Endocrinol (Oxf). 2015; 83:550–555.

53. Ganly I, Nixon IJ, Wang LY, Palmer FL, Migliacci JC, Aniss A, et al. Survival from differentiated thyroid cancer: what has age got to do with it? Thyroid. 2015; 25:1106–1114.

54. Nixon IJ, Kuk D, Wreesmann V, Morris L, Palmer FL, Ganly I, et al. Defining a valid age cutoff in staging of well-differentiated thyroid cancer. Ann Surg Oncol. 2016; 23:410–415.