Advertisement

What’s New in Thyroid Tumor Classification, the 2017 World Health Organization Classification of Tumours of Endocrine Organs

  • Giovanni TalliniEmail author
  • Dario de Biase
  • Andrea Repaci
  • Michela Visani
Chapter
First Online:

Abstract

This chapter presents a brief summary and an overview of the main changes in the classification of thyroid tumors in the fourth edition of the World Health Organization (WHO) Classification of Tumours of Endocrine Organs published in 2017. The important topic of the diagnostic categories of follicular-patterned nodules with borderline histopathological features for a diagnosis of carcinoma covered in the fourth edition of the WHO represents the main focus of this chapter in order to provide the context for other chapters of this volume that also cover the topic.

Keywords

Thyroid gland Thyroid nodule Thyroid carcinoma Papillary thyroid carcinoma Follicular variant papillary carcinoma Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) Well-differentiated tumor of uncertain malignant potential (WDT-UMP) Follicular tumor of uncertain malignant potential (FT-UMP) 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    Lloyd RV, Osamura RY, Klöppel G, et al. Other encapsulated follicular-patterned thyroid tumours. In: IARC, editor. Classification of tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 75–80.Google Scholar
  2. 2.
    Lloyd RV, Osamura RY, Klöppel G, et al. Follicular thyroid carcinoma. In: IARC, editor. Classification of Tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 92–5.Google Scholar
  3. 3.
    Lloyd RV, Osamura RY, Klöppel G, et al. Hürthle (Oncocytic) cell tumours. In: IARC, editor. Classification of tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 96–9.Google Scholar
  4. 4.
    Lloyd RV, Osamura RY, Klöppel G, et al. Poorly differentiated thyroid carcinoma. In: IARC, editor. Classification of tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 100–3.Google Scholar
  5. 5.
    Lloyd RV, Osamura RY, Klöppel G, et al. Papillary thyroid carcinoma. In: IARC, editor. Classification of Tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 81–91.Google Scholar
  6. 6.
    Lloyd RV, Osamura RY, Klöppel G, et al. Anaplastic thyroid carcinoma. In: IARC, editor. Classification of tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 104–6.Google Scholar
  7. 7.
    Lloyd RV, Osamura RY, Klöppel G, et al. Multiple endocrine neoplasia type 2. In: IARC, editor. Classification of tumours of endocrine organs. 4th ed. Lyon, France: World Health Organization; 2017. p. 248–52.Google Scholar
  8. 8.
    Rosai J. The encapsulated follicular variant of papillary thyroid carcinoma: back to the drawing board. Endocr Pathol. 2010;21(1):7–11.PubMedGoogle Scholar
  9. 9.
    Baloch ZW, LiVolsi VA. Follicular-patterned afflictions of the thyroid gland: reappraisal of the most discussed entity in endocrine pathology. Endocr Pathol. 2014;25(1):12–20.PubMedGoogle Scholar
  10. 10.
    Kakudo K, Bai Y, Liu Z, Ozaki T. Encapsulated papillary thyroid carcinoma, follicular variant: a misnomer. Pathol Int. 2012;62(3):155–60.PubMedGoogle Scholar
  11. 11.
    Tallini G, Tuttle RM, Ghossein RA. The history of the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab. 2017;102(1):15–22.PubMedGoogle Scholar
  12. 12.
    Enewold L, Zhu K, Ron E, et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980–2005. Cancer Epidemiol Biomark Prev. 2009;18(3):784–91.Google Scholar
  13. 13.
    Chen AY, Jemal A, Ward EM. Increasing incidence of differentiated thyroid cancer in the United States, 1988-2005. Cancer. 2009;115(16):3801–7.PubMedGoogle Scholar
  14. 14.
    Davies L, Welch HG. Current thyroid cancer trends in the United States. JAMA Otolaryngol Head Neck Surg. 2014;140(4):317–22.PubMedGoogle Scholar
  15. 15.
    Esserman LJ, Thompson IM, Reid B, et al. Addressing overdiagnosis and overtreatment in cancer: a prescription for change. Lancet Oncol. 2014;15(6):e234–42.PubMedPubMedCentralGoogle Scholar
  16. 16.
    La Vecchia C, Malvezzi M, Bosetti C, et al. Thyroid cancer mortality and incidence: a global overview. Int J Cancer. 2015;136(9):2187–95.PubMedGoogle Scholar
  17. 17.
    Vaccarella S, Franceschi S, Bray F, Wild CP, Plummer M, Dal ML. Worldwide thyroid-cancer epidemic? the increasing impact of overdiagnosis. N Engl J Med. 2016;375(7):614–7.PubMedGoogle Scholar
  18. 18.
    Welch HG, Black WC. Overdiagnosis in cancer. J Natl Cancer Inst. 2010;102(9):605–13.PubMedGoogle Scholar
  19. 19.
    Rego-Iraeta A, Perez-Mendez LF, Mantinan B, Garcia-Mayor RV. Time trends for thyroid cancer in northwestern Spain: true rise in the incidence of micro and larger forms of papillary thyroid carcinoma. Thyroid. 2009;19(4):333–40.PubMedGoogle Scholar
  20. 20.
    Kilfoy BA, Zheng T, Holford TR, et al. International patterns and trends in thyroid cancer incidence, 1973–2002. Cancer Causes Control. 2009;20(5):525–31.PubMedGoogle Scholar
  21. 21.
    Hauch A, Al-Qurayshi Z, Randolph G, Kandil E. Total thyroidectomy is associated with increased risk of complications for low- and high-volume surgeons. Ann Surg Oncol. 2014;21(12):3844–52.PubMedGoogle Scholar
  22. 22.
    Iyer NG, Morris LG, 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(19):4439–46.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Lubitz CC, Kong CY, McMahon PM, et al. Annual financial impact of well-differentiated thyroid cancer care in the United States. Cancer. 2014;120(9):1345–52.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Ramsey S, Blough D, Kirchhoff A, et al. Washington State cancer patients found to be at greater risk for bankruptcy than people without a cancer diagnosis. Health Aff (Millwood). 2013;32(6):1143–52.Google Scholar
  25. 25.
    Ramsey SD, Bansal A, Fedorenko CR, et al. Financial Insolvency as a risk factor for early mortality among patients with cancer. J Clin Oncol. 2016;34(9):980–6.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Chen KT, Rosai J. Follicular variant of thyroid papillary carcinoma: a clinicopathologic study of six cases. Am J Surg Pathol. 1977;1(2):123–30.Google Scholar
  27. 27.
    Tielens ET, Sherman SI, Hruban RH, Ladenson PW. Follicular variant of papillary thyroid carcinoma. A clinicopathologic study. Cancer. 1994;73(2):424–31.PubMedGoogle Scholar
  28. 28.
    Zidan J, Karen D, Stein M, Rosenblatt E, Basher W, Kuten A. Pure versus follicular variant of papillary thyroid carcinoma: clinical features, prognostic factors, treatment, and survival. Cancer. 2003;97(5):1181–5.PubMedGoogle Scholar
  29. 29.
    Widder S, Guggisberg K, Khalil M, Pasieka JL. A pathologic re-review of follicular thyroid neoplasms: the impact of changing the threshold for the diagnosis of the follicular variant of papillary thyroid carcinoma. Surgery. 2008;144(1):80–5.PubMedGoogle Scholar
  30. 30.
    Bychkov A, Jung CK, Liu Z, Kakudo K. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features in Asian practice: perspectives for surgical pathology and cytopathology. Endocr Pathol. 2018;Google Scholar
  31. 31.
    Hirokawa M, Carney JA, Goellner JR, et al. Observer variation of encapsulated follicular lesions of the thyroid gland. Am J Surg Pathol. 2002;26(11):1508–14.PubMedGoogle Scholar
  32. 32.
    Chan J. Strict criteria should be applied in the diagnosis of encapsulated follicular variant of papillary thyroid carcinoma. Am J Clin Pathol. 2002;117(1):16–8.PubMedGoogle Scholar
  33. 33.
    Renshaw AA, Gould EW. Why there is the tendency to “overdiagnose” the follicular variant of papillary thyroid carcinoma. Am J Clin Pathol. 2002;117(1):19–21.PubMedGoogle Scholar
  34. 34.
    Lloyd RV, Erickson LA, Casey MB, et al. Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Pathol. 2004;28(10):1336–40.PubMedGoogle Scholar
  35. 35.
    Elsheikh TM, Asa SL, Chan JK, et al. Interobserver and intraobserver variation among experts in the diagnosis of thyroid follicular lesions with borderline nuclear features of papillary carcinoma. Am J Clin Pathol. 2008;130(5):736–44.PubMedGoogle Scholar
  36. 36.
    Williams ED. Guest editorial: two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol. 2000;8(3):181–3.PubMedGoogle Scholar
  37. 37.
    Zhu Z, Gandhi M, Nikiforova MN, Fischer AH, Nikiforov YE. Molecular profile and clinical-pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations. Am J Clin Pathol. 2003;120(1):71–7.PubMedGoogle Scholar
  38. 38.
    Wreesmann VB, Ghossein RA, Hezel M, et al. Follicular variant of papillary thyroid carcinoma: genome-wide appraisal of a controversial entity. Genes Chromosom Cancer. 2004;40(4):355–64.PubMedGoogle Scholar
  39. 39.
    Giordano TJ, Kuick R, Thomas DG, et al. Molecular classification of papillary thyroid carcinoma: distinct BRAF, RAS, and RET/PTC mutation-specific gene expression profiles discovered by DNA microarray analysis. Oncogene. 2005;24(44):6646–56.PubMedGoogle Scholar
  40. 40.
    Liu J, Singh B, Tallini G, et al. Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer. 2006;107(6):1255–64.PubMedGoogle Scholar
  41. 41.
    Piana S, Frasoldati A, Di Felice E, Gardini G, Tallini G, Rosai J. Encapsulated well-differentiated follicular-patterned thyroid carcinomas do not play a significant role in the fatality rates from thyroid carcinoma. Am J Surg Pathol. 2010;34(6):868–72.PubMedGoogle Scholar
  42. 42.
    Vivero M, Kraft S, Barletta JA. Risk stratification of follicular variant of papillary thyroid carcinoma. Thyroid. 2013;23(3):273–9.PubMedGoogle Scholar
  43. 43.
    Ganly I, Wang L, Tuttle RM, et al. Invasion rather than nuclear features correlates with outcome in encapsulated follicular tumors: further evidence for the reclassification of the encapsulated papillary thyroid carcinoma follicular variant. Hum Pathol. 2015;46(5):657–64.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Agrawal N, Akbani R, Arman Aksoy B, et al. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159(3):676–90.PubMedCentralGoogle Scholar
  45. 45.
    Nikiforov YE, Seethala RR, Tallini G, et al. Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol. 2016;2(8):1023–9.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Haugen BR, Alexander EK, Bible KC, 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):1–133.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Haugen BR, Sawka AM, Alexander EK, et al. American thyroid association guidelines on the management of thyroid nodules and differentiated thyroid cancer task force review and recommendation on the proposed renaming of encapsulated follicular variant papillary thyroid carcinoma without invasion to noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Thyroid. 2017;27(4):481–3.PubMedGoogle Scholar
  48. 48.
    Seethala RR, Baloch ZW, Barletta JA, et al. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a review for pathologists. Mod Pathol. 2018;31(1):39–55.PubMedGoogle Scholar
  49. 49.
    Hofman V, Lassalle S, Bonnetaud C, et al. Thyroid tumours of uncertain malignant potential: frequency and diagnostic reproducibility. Virchows Arch. 2009;455(1):21–33.PubMedGoogle Scholar
  50. 50.
    Liu Z, Zhou G, Nakamura M, et al. Encapsulated follicular thyroid tumor with equivocal nuclear changes, so-called well-differentiated tumor of uncertain malignant potential: a morphological, immunohistochemical, and molecular appraisal. Cancer Sci. 2011;102(1):288–94.PubMedGoogle Scholar
  51. 51.
    Arora N, Scognamiglio T, Lubitz CC, et al. Identification of borderline thyroid tumors by gene expression array analysis. Cancer. 2009;115(23):5421–31.PubMedGoogle Scholar
  52. 52.
    Fontaine JF, Mirebeau-Prunier D, Franc B, et al. Microarray analysis refines classification of non-medullary thyroid tumours of uncertain malignancy. Oncogene. 2008;27(15):2228–36.PubMedGoogle Scholar
  53. 53.
    Schmidt RJ, Wang CA. Encapsulated follicular carcinoma of the thyroid: diagnosis, treatment, and results. Surgery. 1986;100(6):1068–77.PubMedGoogle Scholar
  54. 54.
    van Heerden JA, Hay ID, Goellner JR, et al. Follicular thyroid carcinoma with capsular invasion alone: a nonthreatening malignancy. Surgery. 1992;112(6):1130–6; discussion 1136–1138.PubMedGoogle Scholar
  55. 55.
    Jorda M, Gonzalez-Campora R, Mora J, Herrero-Zapatero A, Otal C, Galera H. Prognostic factors in follicular carcinoma of the thyroid. Arch Pathol Lab Med. 1993;117(6):631–5.PubMedGoogle Scholar
  56. 56.
    Simpson H, Orr DJ, John PJ, Wilson K, Braidwood AS. Follicular carcinoma of thyroid presenting as back pain leading to a delay in diagnosis. Br J Clin Pract. 1994;48(6):334–6.PubMedGoogle Scholar
  57. 57.
    D’Avanzo A, Treseler P, Ituarte PH, et al. Follicular thyroid carcinoma: histology and prognosis. Cancer. 2004;100(6):1123–9.PubMedGoogle Scholar
  58. 58.
    Xu B, Wang L, Tuttle RM, Ganly I, Ghossein R. Prognostic impact of extent of vascular invasion in low-grade encapsulated follicular cell-derived thyroid carcinomas: a clinicopathologic study of 276 cases. Hum Pathol. 2015;46(12):1789–98.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Vuong HG, Kondo T, Duong UNP, et al. Prognostic impact of vascular invasion in differentiated thyroid carcinoma: a systematic review and meta-analysis. Eur J Endocrinol. 2017;177(2):207–16.PubMedGoogle Scholar
  60. 60.
    Tickoo SK, Pittas AG, Adler M, et al. Bone metastases from thyroid carcinoma: a histopathologic study with clinical correlates. Arch Pathol Lab Med. 2000;124(10):1440–7.PubMedGoogle Scholar
  61. 61.
    Haq M, Harmer C. Differentiated thyroid carcinoma with distant metastases at presentation: prognostic factors and outcome. Clin Endocrinol. 2005;63(1):87–93.Google Scholar
  62. 62.
    Rivera M, Ghossein RA, Schoder H, Gomez D, Larson SM, Tuttle RM. Histopathologic characterization of radioactive iodine-refractory fluorodeoxyglucose-positron emission tomography-positive thyroid carcinoma. Cancer. 2008;113(1):48–56.PubMedGoogle Scholar
  63. 63.
    Gasparre G, Porcelli AM, Bonora E, et al. Disruptive mitochondrial DNA mutations in complex I subunits are markers of oncocytic phenotype in thyroid tumors. Proc Natl Acad Sci U S A. 2007;104(21):9001–6.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Bishop JA, Wu G, Tufano RP, Westra WH. Histological patterns of locoregional recurrence in Hurthle cell carcinoma of the thyroid gland. Thyroid. 2012;22(7):690–4.PubMedGoogle Scholar
  65. 65.
    Gasparre G, Bonora E, Tallini G, Romeo G. Molecular features of thyroid oncocytic tumors. Mol Cell Endocrinol. 2010;321(1):67–76.PubMedGoogle Scholar
  66. 66.
    Maximo V, Lima J, Prazeres H, Soares P, Sobrinho-Simoes M. The biology and the genetics of Hurthle cell tumors of the thyroid. Endocr Relat Cancer. 2012;19(4):R131–47.PubMedGoogle Scholar
  67. 67.
    Bonora E, Porcelli AM, Gasparre G, et al. Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. Cancer Res. 2006;66(12):6087–96.PubMedGoogle Scholar
  68. 68.
    Mayr JA, Meierhofer D, Zimmermann F, et al. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res. 2008;14(8):2270–5.PubMedGoogle Scholar
  69. 69.
    Maximo V, Botelho T, Capela J, et al. Somatic and germline mutation in GRIM-19, a dual function gene involved in mitochondrial metabolism and cell death, is linked to mitochondrion-rich (Hurthle cell) tumours of the thyroid. Br J Cancer. 2005;92(10):1892–8.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Nikiforova MN, Lynch RA, Biddinger PW, et al. RAS point mutations and PAX8-PPAR gamma rearrangement in thyroid tumors: evidence for distinct molecular pathways in thyroid follicular carcinoma. J Clin Endocrinol Metab. 2003;88(5):2318–26.PubMedGoogle Scholar
  71. 71.
    Ganly I, Ricarte Filho J, Eng S, et al. Genomic dissection of Hurthle cell carcinoma reveals a unique class of thyroid malignancy. J Clin Endocrinol Metab. 2013;98(5):E962–72.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Evangelisti C, de Biase D, Kurelac I, et al. A mutation screening of oncogenes, tumor suppressor gene TP53 and nuclear encoded mitochondrial complex I genes in oncocytic thyroid tumors. BMC Cancer. 2015;15:157.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Wei S, LiVolsi VA, Montone KT, Morrissette JJ, Baloch ZW. PTEN and TP53 Mutations in Oncocytic Follicular Carcinoma. Endocr Pathol. 2015;26(4):365–9.PubMedGoogle Scholar
  74. 74.
    Tallini G, Hsueh A, Liu S, Garcia-Rostan G, Speicher MR, Ward DC. Frequent chromosomal DNA unbalance in thyroid oncocytic (Hurthle cell) neoplasms detected by comparative genomic hybridization. Lab Investig. 1999;79(5):547–55.PubMedGoogle Scholar
  75. 75.
    Erickson LA, Jalal SM, Goellner JR, et al. Analysis of Hurthle cell neoplasms of the thyroid by interphase fluorescence in situ hybridization. Am J Surg Pathol. 2001;25(7):911–7.PubMedGoogle Scholar
  76. 76.
    Volante M, Collini P, Nikiforov YE, et al. Poorly differentiated thyroid carcinoma: the Turin proposal for the use of uniform diagnostic criteria and an algorithmic diagnostic approach. Am J Surg Pathol. 2007;31(8):1256–64.Google Scholar
  77. 77.
    McDermott MB, Swanson PE, Wick MR. Immunostains for collagen type IV discriminate between C-cell hyperplasia and microscopic medullary carcinoma in multiple endocrine neoplasia, type 2a. Hum Pathol. 1995;26(12):1308–12.PubMedGoogle Scholar
  78. 78.
    Koperek O, Scheuba C, Cherenko M, et al. Desmoplasia in medullary thyroid carcinoma: a reliable indicator of metastatic potential. Histopathology. 2008;52(5):623–30.PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Giovanni Tallini
    • 1
    Email author
  • Dario de Biase
    • 2
  • Andrea Repaci
    • 3
  • Michela Visani
    • 1
  1. 1.Anatomic Pathology-Molecular Diagnostic UnitUniversity of Bologna School of MedicineBolognaItaly
  2. 2.Anatomic Pathology-Molecular Diagnostic Unit, Department of Pharmacy and BiotechnologyUniversity of BolognaBolognaItaly
  3. 3.Endocrinology UnitUniversity of Bologna School of MedicineBolognaItaly

Personalised recommendations

Cite chapter

Buy options