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Endocrine Pathology

, Volume 28, Issue 2, pp 128–138 | Cite as

RETRACTED ARTICLE: Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features: Historical Context, Diagnosis, and Future Challenges

  • Bin Xu
  • Giovanni Tallini
  • Ronald A. Ghossein
Article

Abstract

The encapsulated/well-demarcated non-invasive form of follicular variant of papillary thyroid carcinoma (FVPTC) that occurs annually in 45,000 patients worldwide was thought for 30 years to be a carcinoma. Many studies have now shown almost no recurrence in these non-invasive tumors, even in patients treated by surgery without radioactive iodine therapy. The categorization of the tumor as cancer has led to aggressive forms of treatment, with their side effects, financial costs, and the psychological and social impact of a cancer diagnosis. Recently, the encapsulated/well-demarcated non-invasive, FVPTC was renamed as noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) by an international group of experts. The new terminology lacks the carcinoma label enabling clinicians to avoid aggressive therapy. By taking the reader through the history of FVPTC, this article explains how diagnostic criteria for thyroid carcinoma of follicular cells have evolved over the last 60 years. It discusses the steps that led to the labeling of FVPTC as cancer and highlights the various studies that helped reclassify and rename this tumor. It also sheds light on the impact of this reclassification on cytologic diagnosis and focuses on the studies needed to refine and expand the histologic criteria of NIFTP. By understanding the history of this change in nomenclature, future classification of tumors will be greatly improved.

Keywords

Papillary thyroid carcinoma Follicular variant Noninvasive follicular thyroid neoplasm with papillary-like nuclear features RAS BRAF 

Notes

Acknowledgment

This study was supported in part by an Italian Government-Ministero Della Salute Grant No. RF-2011-02350857 to G.T.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Tallini G, Tuttle RM, Ghossein RA: The History of the Follicular Variant of Papillary Thyroid Carcinoma. The Journal of clinical endocrinology and metabolism 2016:jc20162976.Google Scholar
  2. 2.
    Lindsay S: Carcinoma of the thyroid gland: a clinical and pathologic study of 293 patients at the university of California hospital. Springfield Ill: Charles C Thomas; 1960.Google Scholar
  3. 3.
    Chen KT, Rosai J: Follicular variant of thyroid papillary carcinoma: a clinicopathologic study of six cases. Am J Surg Pathol 1977, 1(2):123–130.CrossRefGoogle Scholar
  4. 4.
    Williams ED: Guest editorial: two proposals regarding the terminology of thyroid tumors. Int J Surg Pathol 2000, 8(3):181–183.CrossRefPubMedGoogle Scholar
  5. 5.
    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. American journal of clinical pathology 2003, 120(1):71–77.CrossRefPubMedGoogle Scholar
  6. 6.
    Wreesmann VB, Ghossein RA, Hezel M, Banerjee D, Shaha AR, Tuttle RM, Shah JP, Rao PH, Singh B: Follicular variant of papillary thyroid carcinoma: genome-wide appraisal of a controversial entity. Genes Chromosomes Cancer 2004, 40(4):355–364.CrossRefPubMedGoogle Scholar
  7. 7.
    Giordano TJ, Kuick R, Thomas DG, Misek DE, Vinco M, Sanders D, Zhu Z, Ciampi R, Roh M, Shedden K 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):6646–6656.CrossRefPubMedGoogle Scholar
  8. 8.
    Liu J, Singh B, Tallini G, Carlson DL, Katabi N, Shaha A, Tuttle RM, Ghossein RA: Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer 2006, 107(6):1255–1264.CrossRefPubMedGoogle Scholar
  9. 9.
    Cancer Genome Atlas Research N: Integrated genomic characterization of papillary thyroid carcinoma. Cell 2014, 159(3):676–690.CrossRefGoogle Scholar
  10. 10.
    Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LD, Barletta JA, Wenig BM, Al Ghuzlan A, Kakudo K et al: Nomenclature Revision for Encapsulated Follicular Variant of Papillary Thyroid Carcinoma: A Paradigm Shift to Reduce Overtreatment of Indolent Tumors. JAMA oncology 2016.Google Scholar
  11. 11.
    Warren S, Meissner W: Tumors of the thyroid gland, Fascicle 14. Washington DC, Armed Forces Institute of Pathology; 1953.Google Scholar
  12. 12.
    Woolner LB, Beahrs OH, Black BM, Mc CW, Keating FR, Jr.: Classification and prognosis of thyroid carcinoma. A study of 885 cases observed in a thirty year period. Am J Surg 1961, 102:354–387.CrossRefPubMedGoogle Scholar
  13. 13.
    Carcangiu ML, Zampi G, Pupi A, Castagnoli A, Rosai J: Papillary carcinoma of the thyroid. A clinicopathologic study of 241 cases treated at the University of Florence, Italy. Cancer 1985, 55(4):805–828.CrossRefPubMedGoogle Scholar
  14. 14.
    Vickery AL, Jr., Carcangiu ML, Johannessen JV, Sobrinho-Simoes M: Papillary carcinoma. Semin Diagn Pathol 1985, 2(2):90–100.PubMedGoogle Scholar
  15. 15.
    DeLellis RA: Orphan Annie eye nuclei: a historical note. Am J Surg Pathol 1993, 17(10):1067–1068.CrossRefPubMedGoogle Scholar
  16. 16.
    LiVolsi VA, Asa SL: The demise of follicular carcinoma of the thyroid gland. Thyroid 1994, 4(2):233–236.CrossRefPubMedGoogle Scholar
  17. 17.
    Baloch ZW, LiVolsi VA: Encapsulated follicular variant of papillary thyroid carcinoma with bone metastases. Mod Pathol 2000, 13(8):861–865.CrossRefPubMedGoogle Scholar
  18. 18.
    Chan J: Strict criteria should be applied in the diagnosis of encapsulated follicular variant of papillary thyroid carcinoma. American journal of clinical pathology 2002, 117(1):16–18.CrossRefPubMedGoogle Scholar
  19. 19.
    Renshaw AA, Gould EW: Why there is the tendency to "overdiagnose" the follicular variant of papillary thyroid carcinoma. American journal of clinical pathology 2002, 117(1):19–21.CrossRefPubMedGoogle Scholar
  20. 20.
    Hirokawa M, Carney JA, Goellner JR, DeLellis RA, Heffess CS, Katoh R, Tsujimoto M, Kakudo K: Observer variation of encapsulated follicular lesions of the thyroid gland. The American journal of surgical pathology 2002, 26(11):1508–1514.CrossRefPubMedGoogle Scholar
  21. 21.
    Lloyd RV, Erickson LA, Casey MB, Lam KY, Lohse CM, Asa SL, Chan JK, DeLellis RA, Harach HR, Kakudo K et al: Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. The American journal of surgical pathology 2004, 28(10):1336–1340.CrossRefPubMedGoogle Scholar
  22. 22.
    Elsheikh TM, Asa SL, Chan JK, DeLellis RA, Heffess CS, LiVolsi VA, Wenig BM: Interobserver and intraobserver variation among experts in the diagnosis of thyroid follicular lesions with borderline nuclear features of papillary carcinoma. American journal of clinical pathology 2008, 130(5):736–744.CrossRefPubMedGoogle Scholar
  23. 23.
    Rosai J: The encapsulated follicular variant of papillary thyroid carcinoma: back to the drawing board. Endocrine pathology 2010, 21(1):7–11.CrossRefPubMedGoogle Scholar
  24. 24.
    Thompson LD: Ninety-four cases of encapsulated follicular variant of papillary thyroid carcinoma: A name change to noninvasive follicular thyroid neoplasm with papillary-like nuclear features would help prevent overtreatment. Mod Pathol 2016, 29(7):698–707.CrossRefPubMedGoogle Scholar
  25. 25.
    Tielens ET, Sherman SI, Hruban RH, Ladenson PW: Follicular variant of papillary thyroid carcinoma. A clinicopathologic study. Cancer 1994, 73(2):424–431.CrossRefPubMedGoogle Scholar
  26. 26.
    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):1181–1185.CrossRefPubMedGoogle Scholar
  27. 27.
    Papotti M, Rodriguez J, De Pompa R, Bartolazzi A, Rosai J: Galectin-3 and HBME-1 expression in well-differentiated thyroid tumors with follicular architecture of uncertain malignant potential. Mod Pathol 2005, 18(4):541–546.CrossRefPubMedGoogle Scholar
  28. 28.
    Rivera M, Tuttle RM, Patel S, Shaha A, Shah JP, Ghossein RA: Encapsulated papillary thyroid carcinoma: a clinico-pathologic study of 106 cases with emphasis on its morphologic subtypes (histologic growth pattern). Thyroid: official journal of the American Thyroid Association 2009, 19(2):119–127.CrossRefGoogle Scholar
  29. 29.
    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. The American journal of surgical pathology 2010, 34(6):868–872.CrossRefPubMedGoogle Scholar
  30. 30.
    Vivero M, Kraft S, Barletta JA: Risk stratification of follicular variant of papillary thyroid carcinoma. Thyroid: official journal of the American Thyroid Association 2013, 23(3):273–279.CrossRefGoogle Scholar
  31. 31.
    Rosario PW, Penna GC, Calsolari MR: Noninvasive encapsulated follicular variant of papillary thyroid carcinoma: is lobectomy sufficient for tumours >/=1 cm? Clin Endocrinol (Oxf) 2014, 81(4):630–632.CrossRefGoogle Scholar
  32. 32.
    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):80–85.CrossRefPubMedGoogle Scholar
  33. 33.
    Ganly I, Wang L, Tuttle RM, Katabi N, Ceballos GA, Harach HR, Ghossein R: 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. Human pathology 2015, 46(5):657–664.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Jiang XS, Harrison GP, Datto MB: Young investigator challenge: molecular testing in noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Cancer 2016, 124(12):893–900.Google Scholar
  35. 35.
    Monchik JM, De Petris G, De Crea C: Occult papillary carcinoma of the thyroid presenting as a cervical cyst. Surgery 2001, 129(4):429–432.CrossRefPubMedGoogle Scholar
  36. 36.
    Rivera M, Ricarte-Filho J, Knauf J, Shaha A, Tuttle M, Fagin JA, Ghossein RA: Molecular genotyping of papillary thyroid carcinoma follicular variant according to its histological subtypes (encapsulated vs infiltrative) reveals distinct BRAF and RAS mutation patterns. Mod Pathol 2010, 23(9):1191–1200.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Howitt BE, Jia Y, Sholl LM, Barletta JA: Molecular alterations in partially-encapsulated or well-circumscribed follicular variant of papillary thyroid carcinoma. Thyroid: official journal of the American Thyroid Association 2013, 23(10):1256–1262.CrossRefGoogle Scholar
  38. 38.
    American Thyroid Association Guidelines Taskforce on Thyroid N, Differentiated Thyroid C, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B et al: Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid: official journal of the American Thyroid Association 2009, 19(11):1167–1214.CrossRefGoogle Scholar
  39. 39.
    Esserman LJ, Thompson IM, Reid B, Nelson P, Ransohoff DF, Welch HG, Hwang S, Berry DA, Kinzler KW, Black WC et al: Addressing overdiagnosis and overtreatment in cancer: a prescription for change. The Lancet Oncology 2014, 15(6):e234–e242.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Shi X, Liu R, Basolo F, Giannini R, Shen X, Teng D, Guan H, Shan Z, Teng W, Musholt TJ et al: Differential clinicopathological risk and prognosis of major papillary thyroid cancer variants. J Clin Endocrinol Metab 2016, 101(1):264–274.CrossRefPubMedGoogle Scholar
  41. 41.
    Farhat N, Xu B, Onermek AM, Tuttle RM, Roman BR, Katabi N, Nose V, Sadow PM, Tallini G, Faquin WC et al: Should subcentimeter non-invasive encapsulated, follicular variant of papillary thyroid carcinoma (NI-EFV PTC) be included as non-invasive follicular thyroid neoplasms with papillary-like nuclear features (NIFTP)? In: USCAP 2017. San Antonio, TX.Google Scholar
  42. 42.
    Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Torotti A: AJCC Cancer Staging Manual. 7th edition. New York: Springer-Verlag; 2010.Google Scholar
  43. 43.
    Haugen BRM, Alexander EK, Bible KC, Doherty G, Mandel SJ, Nikiforov YE, Pacini F, Randolph G, Sawka A, Schlumberger M et al: 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid: official journal of the American Thyroid Association 2016, 26:1–133.Google Scholar
  44. 44.
    Xu B, Tallini G, Scognamiglio T, Roman BR, Tuttle RMM, Ghossein RM: Outcome of large noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP). Thyroid: official journal of the American Thyroid Association 2017.Google Scholar
  45. 45.
    Baloch ZW, Seethala RR, Faquin WC, Papotti MG, Basolo F, Fadda G, Randolph GW, Hodak SP, Nikiforov YE, Mandel SJ: Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): A changing paradigm in thyroid surgical pathology and implications for thyroid cytopathology. Cancer Cytopathol 2016, 124(9):616–620.CrossRefPubMedGoogle Scholar
  46. 46.
    Bizzarro T, Martini M, Capodimonti S, Straccia P, Lombardi CP, Pontecorvi A, Larocca LM, Rossi ED: Young investigator challenge: The morphologic analysis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features on liquid-based cytology: Some insights into their identification. Cancer 2016, 124(10):699–710.Google Scholar
  47. 47.
    Faquin WC, Wong LQ, Afrogheh AH, Ali SZ, Bishop JA, Bongiovanni M, Pusztaszeri MP, Vanden Bussche CJ, Gourmaud J, Vaickus LJ et al: Impact of reclassifying noninvasive follicular variant of papillary thyroid carcinoma on the risk of malignancy in The Bethesda System for Reporting Thyroid Cytopathology. Cancer Cytopathol 2016, 124(3):181–187.CrossRefPubMedGoogle Scholar
  48. 48.
    Hahn SY, Shin JH, Lim HK, Jung SL, Oh YL, Choi IH, Jung CK: Preoperative differentiation between noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) and non-NIFTP. Clin Endocrinol (Oxf) 2016.Google Scholar
  49. 49.
    Ibrahim AA, Wu HH: Fine-needle aspiration cytology of noninvasive follicular variant of papillary thyroid carcinoma is cytomorphologically distinct from the invasive counterpart. American journal of clinical pathology 2016, 146(3):373–377.CrossRefPubMedGoogle Scholar
  50. 50.
    Krane JF, Alexander EK, Cibas ES, Barletta JA: Coming to terms with NIFTP: A provisional approach for cytologists. Cancer 2016, 124(11):767–772.Google Scholar
  51. 51.
    Strickland KC, Vivero M, Jo VY, Lowe AC, Hollowell M, Qian X, Wieczorek TJ, French CA, Teot LA, Sadow PM et al: Preoperative cytologic diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a prospective analysis. Thyroid: official journal of the American Thyroid Association 2016, 26(10):1466–1471.CrossRefGoogle Scholar
  52. 52.
    Zhao L, Dias-Santagata D, Sadow PM, Faquin WC: Cytological, molecular, and clinical features of noninvasive follicular thyroid neoplasm with papillary-like nuclear features versus invasive forms of follicular variant of papillary thyroid carcinoma. Cancer 2017.Google Scholar
  53. 53.
    Howitt BE, Chang S, Eszlinger M, Paschke R, Drage MG, Krane JF, Barletta JA: Fine-needle aspiration diagnoses of noninvasive follicular variant of papillary thyroid carcinoma. American journal of clinical pathology 2015, 144(6):850–857.CrossRefPubMedGoogle Scholar
  54. 54.
    Maletta F, Massa F, Torregrossa L, Duregon E, Casadei GP, Basolo F, Tallini G, Volante M, Nikiforov YE, Papotti M: Cytological features of "noninvasive follicular thyroid neoplasm with papillary-like nuclear features" and their correlation with tumor histology. Human pathology 2016, 54:134–142.CrossRefPubMedGoogle Scholar
  55. 55.
    Ali SZ, Cibas ES: The Bethesda System for Reporting Thyroid Cytopathology: Definitions, Criteria, and Explanatory Notes: Springer New York, Dordrecht Heidelberg London; 2010.CrossRefGoogle Scholar
  56. 56.
    Nikiforova MN, Wald AI, Roy S, Durso MB, Nikiforov YE: Targeted next-generation sequencing panel (Thyro Seq) for detection of mutations in thyroid cancer. The Journal of clinical endocrinology and metabolism 2013, 98(11):E1852–E1860.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Alexander EK, Kennedy GC, Baloch ZW, Cibas ES, Chudova D, Diggans J, Friedman L, Kloos RT, LiVolsi VA, Mandel SJ et al: Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. The New England journal of medicine 2012, 367(8):705–715.CrossRefPubMedGoogle Scholar
  58. 58.
    Valderrabano P, Khazai L, Leon ME, Thompson ZJ, Ma Z, Chung CH, Hallanger-Johnson JE, Otto KJ, Rogers KD, Centeno BA et al: Evaluation of Thyro Seq v2 performance in thyroid nodules with indeterminate cytology. Endocrine-related cancer 2017, 24(3):127–136.CrossRefPubMedGoogle Scholar
  59. 59.
    Wong KS, Angell TE, Strickland KC, Alexander EK, Cibas ES, Krane JF, Barletta JA: Noninvasive follicular variant of papillary thyroid carcinoma and the afirma gene-expression classifier. Thyroid: official journal of the American Thyroid Association 2016, 26(7):911–915.CrossRefGoogle Scholar
  60. 60.
    Likhterov I, Osorio M, Moubayed SP, Hernandez-Prera JC, Rhodes R, Urken ML: The Ethical Implications of the Reclassification of Noninvasive Follicular Variant Papillary Thyroid Carcinoma. Thyroid: official journal of the American Thyroid Association 2016, 26(9):1167–1172.CrossRefGoogle Scholar
  61. 61.
    Roerink SH, de Ridder M, Prins J, Huijbers A, de Wilt HJ, Marres H, Repping-Wuts H, Stikkelbroeck NM, Timmers HJ, Hermus AR et al: High level of distress in long-term survivors of thyroid carcinoma: results of rapid screening using the distress thermometer. Acta oncologica (Stockholm, Sweden) 2013, 52(1):128–137.CrossRefGoogle Scholar
  62. 62.
    Buchmann L, Ashby S, Cannon RB, Hunt JP: Psychosocial distress in patients with thyroid cancer. Otolaryngology--head and neck surgery: official journal of American Academy of. Otolaryngology-Head and Neck Surgery 2015, 152(4):644–649.CrossRefPubMedGoogle Scholar
  63. 63.
    Hauch A, Al-Qurayshi Z, Randolph G, Kandil E: Total thyroidectomy is associated with increased risk of complications for low- and high-volume surgeons. Annals of surgical oncology 2014, 21(12):3844–3852.CrossRefPubMedGoogle Scholar
  64. 64.
    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):4439–4446.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Lubitz CC, Kong CY, McMahon PM, Daniels GH, Chen Y, Economopoulos KP, Gazelle GS, Weinstein MC: Annual financial impact of well-differentiated thyroid cancer care in the United States. Cancer 2014, 120(9):1345–1352.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Sunnybrook Health Sciences CentreTorontoCanada
  2. 2.Department of Medicine (Dipartimento di Medicina Specialistica Diagnostica e Sperimentale)University of Bologna School of Medicine, Anatomic Pathology, Ospedale BellariaBolognaItaly
  3. 3.Department of PathologyMemorial Sloan-Kettering Cancer CenterNew YorkUSA

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