Skip to main content

Advertisement

SpringerLink
Log in

Aggressive variants of follicular cell-derived thyroid carcinoma: an overview

  • Review
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

The incidence of thyroid carcinoma has increased globally in the past years. Papillary thyroid carcinoma (PTC) is the most frequent neoplasm of the thyroid gland comprehending the 90% of the thyroid carcinoma and has an indolent clinical behaviour. However, some variants of follicular cell-derived thyroid carcinoma, including variants of classic of PTC, have been identified that show a more aggressive biological behaviour. An accurate diagnosis of these entities is crucial for planning a more aggressive treatment and improving patients’ prognosis of patients. The aim of this review is to present the main clinical, histological, and molecular features of aggressive variants of follicular cell-derived thyroid carcinoma, and to provide useful histological parameters for determining the most suitable therapeutic strategy for patients affected by these forms.

Results

Variants of classic PTC such as the diffuse sclerosing variant (DSV), the tall cell variant (TCV), the columnar cell variant (CCV), the solid/trabecular variant (STV) and the hobnail variant (HV), and other variants of follicular cell-derived thyroid carcinoma, such as poorly differentiated thyroid carcinoma (PDTC), and anaplastic thyroid carcinoma (ATC), are associated with aggressive behaviour.

Conclusions

The correct identification and diagnosis of aggressive variants of follicular cell-derived thyroid carcinoma is important, as they allow the clinician to adopt the most refined therapeutic strategies in order to the survival of the patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. E.D. Rossi, L. Pantanowitz, J.L. Hornick, A worldwide journey of thyroid cancer incidence centred on tumour histology. Lancet Diabetes Endocrinol. 9, 193 (2021). https://doi.org/10.1016/S2213-8587(21)00049-8

    Article  PubMed  Google Scholar 

  2. J. Rosai, R.V. Lloyd, R.Y Osamura, G. Kloppel, WHO Classification of Tumours of Endocrine Organs (4th edition). International Agency for Research on Cancer (IARC), Lyon (2017)

  3. B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 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 (2016). https://doi.org/10.1089/thy.2015.0020

    Article  PubMed  PubMed Central  Google Scholar 

  4. I. Ganly, T. Ibrahimpasic, M. Rivera, I. Nixon, F. Palmer, S.G. Patel, R.M. Tuttle, J.P. Shah, R. Ghossein, Prognostic implications of papillary thyroid carcinoma with tall-cell features. Thyroid 24, 662 (2014). https://doi.org/10.1089/thy.2013.0503

    Article  CAS  PubMed  Google Scholar 

  5. F. Ambrosi, A. Righi, C. Ricci, L.A. Erickson, R.V. Lloyd, S. Asioli, Hobnail Variant of Papillary Thyroid Carcinoma: a Literature Review. Endocr. Pathol. 28, 293 (2017). https://doi.org/10.1007/s12022-017-9502-7

    Article  CAS  PubMed  Google Scholar 

  6. S. Asioli, L.A. Erickson, T.J. Sebo, J. Zhang, L. Jin, G.B. Thompson, R.V. Lloyd, Papillary thyroid carcinoma with prominent hobnail features: a new aggressive variant of moderately differentiated papillary carcinoma. A clinicopathologic, immunohistochemical, and molecular study of eight cases. Am. J. Surg. Pathol. 34, 44 (2010). https://doi.org/10.1097/PAS.0b013e3181c46677

    Article  PubMed  Google Scholar 

  7. A.L. Vickery Jr, M.L. Carcangiu, J.V. Johannessen, M. Sobrinho-Simoes, Papillary carcinoma. Semin Diagn. Pathol. 2(2), 90–100 (1985)

    PubMed  Google Scholar 

  8. L.A.K.S. Pillai, V. Gopalan, R.A. Smith, Diffuse sclerosing variant of papillary thyroid carcinoma–an update of its clinicopathological features and molecular biology. Crit. Rev. Oncol. Hematol. 94, 64 (2015). https://doi.org/10.1016/j.critrevonc.2014.12.001

    Article  PubMed  Google Scholar 

  9. M.V. Fridman, N.N. Savva, O.V. Krasko, A.A. Zborovskaya, S.V. Mankovskaya, K.W. Schmid, Y.E. Demidchik, Clinical and pathologic features of “sporadic” papillary thyroid carcinoma registered in the years 2005 to 2008 in children and adolescents of Belarus. Thyroid 22, 1016 (2012). https://doi.org/10.1089/thy.2011.0005

    Article  PubMed  Google Scholar 

  10. A. Coca-Pelaz, J.P. Shah, J.C. Hernandez-Prera, R.A. Ghossein, J.P. Rodrigo, D.M. Hartl, K.D. Olsen, A.R. Shaha, M. Zafereo, C. Suarez, I.J. Nixon, G.W. Randolph, A.A. Mäkitie, L.P. Kowalski, V. Vander Poorten, A. Sanabria, O. Guntinas-Lichius, R. Simo, P. Zbären, P. Angelos, A. Khafif, A. Rinaldo, A. Ferlito, Papillary thyroid cancer-aggressive variants and impact on management: a narrative review. Adv. Ther. 37, 3112 (2020). https://doi.org/10.1007/s12325-020-01391-1

    Article  PubMed  PubMed Central  Google Scholar 

  11. Y.K. Jin, E.K. Kim, W.H. Soon, J.M. Hee, J.K. Min, J.S. Eun, S.P. Cheong, Diffuse sclerosing variant of papillary carcinoma of the thyroid gland: specimen radiographic features with histopathological correlation. J. Clin. Endocrinol. Metab. 94, 1491 (2009). https://doi.org/10.1210/jc.2009-0072

    Article  CAS  Google Scholar 

  12. M.B. Yun, P.S. Sundar, P.Y. Lan, S.X. Ying, Z. Hua, Ultrasonographic Features of Diffuse Sclerosing Variant of Papillary Thyroid Carcinoma. J. Med. Ultrasound 19, 41 (2011). https://doi.org/10.1016/j.jmu.2011.05.006

    Article  Google Scholar 

  13. E.D. Rossi, W.C. Faquin, L. Pantanowitz, Cytologic features of aggressive variants of follicular-derived thyroid carcinoma. Cancer Cytopathol. 127, 432 (2019). https://doi.org/10.1002/cncy.22136

    Article  PubMed  PubMed Central  Google Scholar 

  14. N. Irrera, M. Vaccaro, A. Bitto, G. Pallio, G. Pizzino, M. Lentini, V. Arcoraci, L. Minutoli, M. Scuruchi, G. Cutroneo, G.P. Anastasi, R. Ettari, F. Squadrito, D. Altavilla, N. Irrera, M. Vaccaro, A. Bitto et al. BAY 11-7082 inhibits the NF-κB and NLRP3 inflammasome pathways and protects against IMQ-induced psoriasis. Clin. Sci. 131, 487 (2017). https://doi.org/10.1042/CS20160645

    Article  CAS  Google Scholar 

  15. J.Y. Joung, T.H. Kim, D.J. Jeong, S.M. Park, Y.Y. Cho, H.W. Jang, Y.Y. Jung, Y.L. Oh, H.S. Yim, Y.L. Kim, J.H. Chung, C.S. Ki, S.W. Kim, Diffuse sclerosing variant of papillary thyroid carcinoma: major genetic alterations and prognostic implications. Histopathology 69, 45 (2016). https://doi.org/10.1111/his.12902

    Article  PubMed  Google Scholar 

  16. T. Carling, I.T. Ocal, R. Udelsman, Special variants of differentiated thyroid cancer: does it alter the extent of surgery versus well-differentiated thyroid cancer? World J. Surg. 31, 916 (2007). https://doi.org/10.1007/s00268-006-0837-3

    Article  PubMed  Google Scholar 

  17. S.-M. Chow, J.K.C. Chan, S.C.K. Law, D.L.C. Tang, C.-M. Ho, W.-Y. Cheung, I.S.M. Wong, W.-H. Lau, Diffuse sclerosing variant of papillary thyroid carcinoma–clinical features and outcome. Eur. J. Surg. Oncol. 29, 446 (2003). https://doi.org/10.1016/s0748-7983(03)00005-2

    Article  PubMed  Google Scholar 

  18. A.K.Y. Lam, C.Y. Lo, Diffuse sclerosing variant of papillary carcinoma of the thyroid: a 35-year comparative study at a single institution. Ann. Surg. Oncol. 13, 176 (2006). https://doi.org/10.1245/ASO.2006.03.062

    Article  PubMed  Google Scholar 

  19. H.G. Vuong, T. Kondo, T.Q. Pham, N. Oishi, K. Mochizuki, T. Nakazawa, L. Hassell, R. Katoh, Prognostic significance of diffuse sclerosing variant papillary thyroid carcinoma: a systematic review and meta-analysis. Eur. J. Endocrinol. 176, 433 (2017). https://doi.org/10.1530/EJE-16-0863

    Article  CAS  PubMed  Google Scholar 

  20. L. Falvo, L. Giacomelli, V. D’Andrea, A. Marzullo, G. Guerriero, E. de Antoni, Prognostic importance of sclerosing variant in papillary thyroid carcinoma. Am. Surg. 72, 438 (2006)

    Article  Google Scholar 

  21. C. Regalbuto, P. Malandrino, A. Tumminia, R. Le Moli, R. Vigneri, V. Pezzino, A diffuse sclerosing variant of papillary thyroid carcinoma: clinical and pathologic features and outcomes of 34 consecutive cases. Thyroid 21, 383 (2011). https://doi.org/10.1089/thy.2010.0331

    Article  PubMed  Google Scholar 

  22. W.A. Hwak, J.B. Hazard, The many appearances of papillary carcinoma of the thyroid. Cleve Clin. Q 43, 207 (1976). https://doi.org/10.3949/ccjm.43.4.207

    Article  Google Scholar 

  23. X. Wang, W. Cheng, C. Liu, J. Li, Tall cell variant of papillary thyroid carcinoma: current evidence on clinicopathologic features and molecular biology. Oncotarget 7, 40792 (2016). https://doi.org/10.18632/oncotarget.8215

    Article  PubMed  PubMed Central  Google Scholar 

  24. R. Ghossein, V.A. Livolsi, Papillary thyroid carcinoma tall cell variant. Thyroid 18, 1179 (2008). https://doi.org/10.1089/thy.2008.0164

    Article  CAS  PubMed  Google Scholar 

  25. B. Gunalp, K. Okuyucu, S. Ince, A. Ayan, E. Alagoz, Impact of tall cell variant histology on predicting relapse and changing the management of papillary thyroid carcinoma patients. Hell. J. Nucl. Med. 20, 122 (2017). https://doi.org/10.1967/s002449910552

    Article  PubMed  Google Scholar 

  26. Y.J. Choi, J.H. Shin, J. Kim, S.L. Jung, E.J. Son, Y.L. Oh, Tall cell variant of papillary thyroid carcinoma: sonographic and clinical findings. J. Ultrasound Med 30, 853 (2011). https://doi.org/10.7863/jum.2011.30.6.853

    Article  PubMed  Google Scholar 

  27. A.M. Poma, D. Viola, E. Macerola, A. Proietti, E. Molinaro, D. de Vietro, R. Elisei, G. Materazzi, P. Miccoli, F. Basolo, C. Ugolini, Tall cell percentage alone in PTC without aggressive features should not guide patients’ clinical management. J. Clin. Endocrinol. Metab. 106, E4109 (2021). https://doi.org/10.1210/clinem/dgab388

    Article  PubMed  Google Scholar 

  28. N. Agrawal, R. Akbani, B.A. Aksoy, A. Ally, H. Arachchi, S.L. Asa, J.T. Auman, M. Balasundaram, S. Balu, S.B. Baylin, M. Behera, B. Bernard, R. Beroukhim, J.A. Bishop, A.D. Black, T. Bodenheimer, L. Boice, M.S. Bootwalla, J. Bowen, R. Bowlby, C.A. Bristow, R. Brookens, D. Brooks, R. Bryant, E. Buda, Y.S.N. Butterfield, T. Carling, R. Carlsen, S.L. Carter, S.E. Carty, T.A. Chan, A.Y. Chen, A.D. Cherniack, D. Cheung, L. Chin, J. Cho, A. Chu, E. Chuah, K. Cibulskis, G. Ciriello, A. Clarke, G.L. Clayman, L. Cope, J.A. Copland, K. Covington, L. Danilova, T. Davidsen, J.A. Demchok, D. DiCara, N. Dhalla, R. Dhir, S.S. Dookran, G. Dresdner, J. Eldridge, G. Eley, A.K. El-Naggar, S. Eng, J.A. Fagin, T. Fennell, R.L. Ferris, S. Fisher, S. Frazer, J. Frick, S.B. Gabriel, I. Ganly, J. Gao, L.A. Garraway, J.M. Gastier-Foster, G. Getz, N. Gehlenborg, R. Ghossein, R.A. Gibbs, T.J. Giordano, K. Gomez-Hernandez, J. Grimsby, B. Gross, R. Guin, A. Hadjipanayis, H.A. Harper, D.N. Hayes, D.I. Heiman, J.G. Herman, K.A. Hoadley, M. Hofree, R.A. Holt, A.P. Hoyle, F.W. Huang, M. Huang, C.M. Hutter, T. Ideker, L. Iype, A. Jacobsen, S.R. Jefferys, C.D. Jones, S.J.M. Jones, K. Kasaian, E. Kebebew, F.R. Khuri, J. Kim, R. Kramer, R. Kreisberg, R. Kucherlapati, D.J. Kwiatkowski, M. Ladanyi, P.H. Lai, P.W. Laird, E. Lander, M.S. Lawrence, D. Lee, E. Lee, S. Lee, W. Lee, K.M. Leraas, T.M. Lichtenberg, L. Lichtenstein, P. Lin, S. Ling, J. Liu, W. Liu, Y. Liu, V.A. LiVolsi, Y. Lu, Y. Ma, H.S. Mahadeshwar, M.A. Marra, M. Mayo, D.G. McFadden, S. Meng, M. Meyerson, P.A. Mieczkowski, M. Miller, G. Mills, R.A. Moore, L.E. Mose, A.J. Mungall, B.A. Murray, Y.E. Nikiforov, M.S. Noble, A.I. Ojesina, T.K. Owonikoko, B.A. Ozenberger, A. Pantazi, M. Parfenov, P.J. Park, J.S. Parker, E.O. Paull, C.S. Pedamallu, C.M. Perou, J.F. Prins, A. Protopopov, S.S. Ramalingam, N.C. Ramirez, R. Ramirez, B.J. Raphael, W.K. Rathmell, X. Ren, S.M. Reynolds, E. Rheinbay, M.D. Ringel, M. Rivera, J. Roach, A.G. Robertson, M.W. Rosenberg, M. Rosenthal, S. Sadeghi, G. Saksena, C. Sander, N. Santoso, J.E. Schein, N. Schultz, S.E. Schumacher, R.R. Seethala, J. Seidman, Y. Senbabaoglu, S. Seth, S. Sharpe, K.R.M. Shaw, J.P. Shen, R. Shen, S. Sherman, M. Sheth, Y. Shi, I. Shmulevich, G.L. Sica, J.V. Simons, R. Sinha, P. Sipahimalani, R.C. Smallridge, H.J. Sofia, M.G. Soloway, X. Song, C. Sougnez, C. Stewart, P. Stojanov, J.M. Stuart, S.O. Sumer, Y. Sun, B. Tabak, A. Tam, D. Tan, J. Tang, R. Tarnuzzer, B.S. Taylor, N. Thiessen, L. Thorne, V. Thorsson, R.M. Tuttle, C.B. Umbricht, D.J. Van Den Berg, F. Vandin, U. Veluvolu, R.G.W. Verhaak, M. Vinco, D. Voet, V. Walter, Z. Wang, S. Waring, P.M. Weinberger, N. Weinhold, J.N. Weinstein, D.J. Weisenberger, D. Wheeler, M.D. Wilkerson, J. Wilson, M. Williams, D.A. Winer, L. Wise, J. Wu, L. Xi, A.W. Xu, L. Yang, L. Yang, T.I. Zack, M.A. Zeiger, D. Zeng, J.C. Zenklusen, N. Zhao, H. Zhang, J. Zhang, J. Zhang, W. Zhang, E. Zmuda, L. Zou, Integrated genomic characterization of papillary thyroid carcinoma. Cell 159, 676 (2014). https://doi.org/10.1016/j.cell.2014.09.050

    Article  CAS  PubMed Central  Google Scholar 

  29. G. Grani, V. Ramundo, A. Verrienti, M. Sponziello, C. Durante, Thyroid hormone therapy in differentiated thyroid cancer. Endocrine 66, 43 (2019). https://doi.org/10.1007/s12020-019-02051-3

    Article  CAS  PubMed  Google Scholar 

  30. H.L. Evans, Columnar-cell carcinoma of the thyroid. A report of two cases of an aggressive variant of thyroid carcinoma. AM J. Clin. Pathol. 85, 77 (1986). https://doi.org/10.1093/ajcp/85.1.77

    Article  CAS  PubMed  Google Scholar 

  31. M. Sywak, J.L. Pasieka, T. Ogilvie, A review of thyroid cancer with intermediate differentiation. J. Surg. Oncol. 86, 44 (2004). https://doi.org/10.1002/jso.20044

    Article  PubMed  Google Scholar 

  32. V. Chen, J. Faquin, W.C. Lloyd, R.V. Nose, Clinicopathological and molecular characterization of nine cases of columnar cell variant of papillary thyroid carcinoma. Mod. Pathol. 24, 739 (2011). https://doi.org/10.1038/modpathol.2011.2

    Article  CAS  PubMed  Google Scholar 

  33. M. Bongiovanni, M. Mermod, S. Canberk, C. Saglietti, G.P. Sykiotis, M. Pusztaszeri, M. Ragazzi, L. Mazzucchelli, L. Giovanella, S. Piana, Columnar cell variant of papillary thyroid carcinoma: Cytomorphological characteristics of 11 cases with histological correlation and literature review. Cancer Cytopathol. 125, 389 (2017). https://doi.org/10.1002/cncy.21860

    Article  PubMed  Google Scholar 

  34. J. Cho, J.H. Shin, S.Y. Hahn, Y.L. Oh, Columnar cell variant of papillary thyroid carcinoma: ultrasonographic and clinical differentiation between the indolent and aggressive types. Korean J. Radiol. 19, 1000 (2018). https://doi.org/10.3348/kjr.2018.19.5.1000

    Article  PubMed  PubMed Central  Google Scholar 

  35. V.A. Enriquez, M.L. Baloch, Z.W. Montone, K.T. Zhang, P.J. LiVolsi, CDX2 expression in columnar cell variant of papillary thyroid carcinoma. AM J. Clin. Pathol. 137, 722 (2012). https://doi.org/10.1309/AJCPXE3PUBWVZCGZ

    Article  PubMed  Google Scholar 

  36. J.A. Janovitz, T. Williamson, D.F.K. Wong, K.S. Dong, F. Barletta, Genomic profile of columnar cell variant of papillary thyroid carcinoma. Histopathology 79, 491 (2021). https://doi.org/10.1111/his.14374

    Article  PubMed  Google Scholar 

  37. B.R. Haugen, A.M. Sawka, E.K. Alexander, K.C. Bible, P. Caturegli, G.M. Doherty, S.J. Mandel, J.C. Morris, A. Nassar, F. Pacini, M. Schlumberger, K. Schuff, S.I. Sherman, H. Somerset, J.A. Sosa, D.L. Steward, L. Wartofsky, M.D. Williams, 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 27, 481 (2017). https://doi.org/10.1089/thy.2016.0628

    Article  CAS  PubMed  Google Scholar 

  38. L.A. Nath, M.C. Erickson, Aggressive variants of papillary thyroid carcinoma: hobnail, tall cell, columnar, and solid. Adv. Anat. Pathol. 25, 172 (2018). https://doi.org/10.1097/PAP.0000000000000184

    Article  CAS  PubMed  Google Scholar 

  39. C. Jiang, T. Cheng, X. Zheng, S. Hong, S. Liu, J. Liu, J. Wang, S. Wang, Clinical behaviors of rare variants of papillary thyroid carcinoma are associated with survival: a population-level analysis. Cancer Manag. Res. 10, 465 (2018). https://doi.org/10.2147/CMAR.S157823

    Article  PubMed  PubMed Central  Google Scholar 

  40. S. Wang, Y. Xiong, Q. Zhao, H. Song, P. Yi, C. Liu, Columnar cell papillary thyroid carcinoma prognosis: findings from the SEER database using propensity score matching analysis. Am. J. Transl. Res. 11, 6262 (2019)

    PubMed  PubMed Central  Google Scholar 

  41. C.S. Wenig, B.M. Thompson, L.D. Adair, C.F. Shmookler, B. Heffess, Thyroid papillary carcinoma of columnar cell type: a clinicopathologic study of 16 cases. Cancer 82, 740 (1988)

    Article  Google Scholar 

  42. M.L. Carcangiu, G. Zampi, A. Pupi, A. Castagnoli, J. Rosai, apillary carcinoma of the thyroid. A clinicopathologic study of 241 cases treated at the University of Florence, Italy. Cancer 55, 805 (1985)

    Article  CAS  Google Scholar 

  43. R. Ohashi, Solid variant of papillary thyroid carcinoma: an under-recognized entity. Endocr. J. 67, 241 (2020). https://doi.org/10.1507/endocrj.EJ19-0414

    Article  CAS  PubMed  Google Scholar 

  44. Ç. Vural, U. Kiraz, G. Turan, S.K. Özkara, M. Sözen, B. Çetinarslan, Solid variant of papillary thyroid carcinoma: An analysis of 28 cases with current literature. Ann. Diagn. Pathol. 52, (2021). https://doi.org/10.1016/j.anndiagpath.2021.151737

  45. H. Chang, S.M. Kim, K.W. Chun, B.W. Kim, Y.S. Lee, H.S. Chang, S.W. Hong, C.S. Park, Clinicopathologic features of solid variant papillary thyroid cancer. ANZ J. Surg. 84, 380 (2014). https://doi.org/10.1111/ans.12307

    Article  PubMed  Google Scholar 

  46. R. Ohashi, K. Kawahara, S. Namimatsu, T. Igarashi, T. Sakatani, I. Sugitani, Z. Naito, Clinicopathological significance of a solid component in papillary thyroid carcinoma. Histopathology 70, 775 (2017). https://doi.org/10.1111/his.13132

    Article  PubMed  Google Scholar 

  47. J.H. Shin, Ultrasonographic imaging of papillary thyroid carcinoma variants. Ultrasonography 36, 103 (2017). https://doi.org/10.14366/usg.16048

    Article  PubMed  PubMed Central  Google Scholar 

  48. V. Trovisco, P. Soares, R. Soares, J. Magalhães, P. Sá-Couto, M. Sobrinho-Simões, A new BRAF gene mutation detected in a case of a solid variant of papillary thyroid carcinoma. Hum. Pathol. 36, 694 (2005). https://doi.org/10.1016/j.humpath.2005.04.011

    Article  CAS  PubMed  Google Scholar 

  49. M.L. Prasad, M. Vyas, M.J. Horne, R.K. Virk, R. Morotti, Z. Liu, G. Tallini, M.N. Nikiforova, E.R. Christison-Lagay, R. Udelsman, C.A. Dinauer, Y.E. Nikiforov, NTRK fusion oncogenes in pediatric papillary thyroid carcinoma in northeast United States. Cancer 122, 1097 (2016). https://doi.org/10.1002/cncr.29887

    Article  CAS  PubMed  Google Scholar 

  50. H.G. Vuong, T. Odate, U.N.P. Duong, K. Mochizuki, T. Nakazawa, R. Katoh, T. Kondo, Prognostic importance of solid variant papillary thyroid carcinoma: a systematic review and meta-analysis. Head. Neck 40, 1588 (2018). https://doi.org/10.1002/hed.25123

    Article  PubMed  Google Scholar 

  51. A. Ieni, V. Barresi, R. Cardia, L. Licata, F. Di Bari, S. Benvenga, G. Tuccari, The micropapillary/hobnail variant of papillary thyroid carcinoma: a review of series described in the literature compared to a series from one southern Italy pathology institution. Rev. Endocr. Metab. Disord. 17, 521 (2016). https://doi.org/10.1007/s11154-016-9398-4

    Article  CAS  PubMed  Google Scholar 

  52. L. Teng, W. Deng, J. Lu, J. Zhang, X. Ren, H. Duan, S. Chuai, F. Duan, W. Gao, T. Lu, H. Wu, Z. Liang, obnail variant of papillary thyroid carcinoma: molecular profiling and comparison to classical papillary thyroid carcinoma, poorly differentiated thyroid carcinoma and anaplastic thyroid carcinoma. Oncotarget 8, 22023 (2017). https://doi.org/10.18632/oncotarget.15786

    Article  PubMed  PubMed Central  Google Scholar 

  53. A.M. Amacher, B. Goyal, J.S. Lewis, S.K. El-Mofty, R.D. Chernock, Prevalence of a hobnail pattern in papillary, poorly differentiated, and anaplastic thyroid carcinoma: a possible manifestation of high-grade transformation. Am. J. Surg. Pathol. 39, 260 (2015). https://doi.org/10.1097/PAS.0000000000000329

    Article  PubMed  Google Scholar 

  54. A.M. Poma, E. Macerola, A. Proietti, P. Vignali, R. Sparavelli, L. Torregrossa, A. Matrone, A. Basolo, R. Elisei, F. Santini, C. Ugolini, Clinical-pathological features and treatment outcome of patients with hobnail variant papillary thyroid carcinoma. Front. Endocrinol. 13, 1 (2022). https://doi.org/10.3389/fendo.2022.842424

    Article  Google Scholar 

  55. D. Karunaratne, T.-T. Zhang, Z.A.S. Ali, A. Moore, P. Kirkland, D. Howlett, Sonographic appearances of hobnail papillary thyroid carcinoma: a case report of a rare tumour. Ultrasound 1742271X2110383 (2021). https://doi.org/10.1177/1742271X211038338

  56. L. Morandi, A. Righi, F. Maletta, P. Rucci, F. Pagni, M. Gallo, S. Rossi, L. Caporali, A. Sapino, R.V. Lloyd, S. Asioli, Somatic mutation profiling of hobnail variant of papillary thyroid carcinoma. Endocr. Relat. Cancer 24, 107 (2017). https://doi.org/10.1530/ERC-16-0546

    Article  CAS  PubMed  Google Scholar 

  57. S. Asioli, L.A. Erickson, A. Righi, R.V. Lloyd, Papillary thyroid carcinoma with hobnail features: histopathologic criteria to predict aggressive behavior. Hum. Pathol. 44, 320 (2013). https://doi.org/10.1016/j.humpath.2012.06.003

    Article  PubMed  Google Scholar 

  58. S.L. Cassol, C.A. Asa, Molecular pathology of thyroid cancer. Diagn. Histopathol. 17, 124 (2011)

    Article  Google Scholar 

  59. J.A. Granner, D.K., Buckwalter, Poorly differentiated carcinoma of the thyroid gland. Surg Gynecol Obs. 116, 650 (1963).

  60. M.L. Carcangiu, G. Zamp, J. Rosai, Poorly differentiated (“insular”) thyroid carcinoma. A reinterpretation of Langhans’ “wuchernde Struma”. Am. J. Surg. Pathol. 8, 655 (1984). https://doi.org/10.1097/00000478-198409000-00005

    Article  CAS  PubMed  Google Scholar 

  61. K. Kakudo, Y. Bai, S. Katayama, M. Hirokawa, Y. Ito, A. Miyauchi, K. Kuma, Classification of follicular cell tumors of the thyroid gland: analysis involving Japanese patients from one institute. Pathol. Int. 59, 359 (2009). https://doi.org/10.1111/j.1440-1827.2009.02378.x

    Article  PubMed  Google Scholar 

  62. S. Asioli, L.A. Erickson, A. Righi, L. Jin, M. Volante, S. Jenkins, M. Papotti, G. Bussolati, R.V. Lloyd, Poorly differentiated carcinoma of the thyroid: validation of the Turin proposal and analysis of IMP3 expression. Mod. Pathol. 23, 1269 (2010). https://doi.org/10.1038/modpathol.2010.117

    Article  PubMed  Google Scholar 

  63. M. I. Bellini, M. Biffoni, R. Patrone, M. C. Borcea, M. L. Costanzo, T. Garritano, R. Melcarne, R. Menditto, A. Metere, C. Scorziello, M. Summa, L. Ventrone, V. D’andrea, L. Giacomelli, Poorly differentiated thyroid carcinoma: single centre experience and review of the literature. J. Clin. Med. 10, (2021). https://doi.org/10.3390/jcm10225258

  64. D.Y. Lee, J.-K. Won, S.-H. Lee, D.J. Park, K.C. Jung, M.-W. Sung, H.-G. Wu, K.H. Kim, Y.J. Park, J.H. Hah, Changes of clinicopathologic characteristics and survival outcomes of anaplastic and poorly differentiated thyroid carcinoma. Thyroid 26, 404 (2016). https://doi.org/10.1089/thy.2015.0316

    Article  PubMed  Google Scholar 

  65. Z.W. Baloch, V.A. LiVolsi, Special types of thyroid carcinoma. Histopathology 72, 40 (2018). https://doi.org/10.1111/his.13348

    Article  PubMed  Google Scholar 

  66. S.Y. Hahn, J.H. Shin, Description and comparison of the sonographic characteristics of poorly differentiated thyroid carcinoma and anaplastic thyroid carcinoma. J. Ultrasound Med. 35, 1873 (2016). https://doi.org/10.7863/ultra.15.09058

    Article  PubMed  Google Scholar 

  67. A. Lacout, P.Y. Marcy, J. Thariat, RE: role of duplex doppler US for thyroid nodules: looking for the “sword” sign. Korean J. Radiol. 12, 400 (2011). https://doi.org/10.3348/kjr.2011.12.3.400

    Article  PubMed  PubMed Central  Google Scholar 

  68. M. Volante, P. Collini, Y.E. Nikiforov, A. Sakamoto, K. Kakudo, R. Katoh, R.V. Lloyd, V.A. LiVolsi, M. Papotti, M. Sobrinho-Simoes, G. Bussolati, J. Rosai, Poorly differentiated thyroid carcinoma: the Turin proposal for the use of uniform diagnostic criteria and an algorithmic diagnostic approach. Am. J. Surg. Pathol. 31, 1256 (2007). https://doi.org/10.1097/PAS.0b013e3180309e6a

    Article  PubMed  Google Scholar 

  69. D. Hiltzik, D.L. Carlson, R.M. Tuttle, S. Chuai, N. Ishill, A. Shaha, J.P. Shah, B. Singh, R.A. Ghossein, Poorly differentiated thyroid carcinomas defined on the basis of mitosis and necrosis: a clinicopathologic study of 58 patients. Cancer 106, 1286 (2006). https://doi.org/10.1002/cncr.21739

    Article  PubMed  Google Scholar 

  70. S. Bai, Z.W. Baloch, T.D. Samulski, K.T. Montone, V.A. LiVolsi, Poorly differentiated oncocytic (hürthle cell) follicular carcinoma: an institutional experience. Endocr. Pathol. 26, 164 (2015). https://doi.org/10.1007/s12022-015-9367-6

    Article  CAS  PubMed  Google Scholar 

  71. B. Xu, R. Ghossein, Genomic landscape of poorly differentiated and anaplastic thyroid carcinoma. Endocr. Pathol. 27, 205 (2016). https://doi.org/10.1007/s12022-016-9445-4

    Article  CAS  PubMed  Google Scholar 

  72. T. Ibrahimpasic, R. Ghossein, D.L. Carlson, N. Chernichenko, I. Nixon, F.L. Palmer, N.Y. Lee, A.R. Shaha, S.G. Patel, R.M. Tuttle, A.J.M. Balm, J.P. Shah, I. Ganly, Poorly differentiated thyroid carcinoma presenting with gross extrathyroidal extension: 1986-2009 Memorial Sloan-Kettering Cancer Center experience. Thyroid 23, 997 (2013). https://doi.org/10.1089/thy.2012.0403

    Article  CAS  PubMed  Google Scholar 

  73. M.S. Brose, C.M. Nutting, B. Jarzab, R. Elisei, S. Siena, L. Bastholt, C. de la Fouchardiere, F. Pacini, R. Paschke, Y.K. Shong, S.I. Sherman, J.W.A. Smit, J. Chung, C. Kappeler, C. Peña, I. Molnár, M.J. Schlumberger, Sorafenib in radioactive iodine-refractory, locally advanced or metastatic differentiated thyroid cancer: a randomised, double-blind, phase 3 trial. Lancet 384, 319 (2014). https://doi.org/10.1016/S0140-6736(14)60421-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. M. Schlumberger, M. Tahara, L.J. Wirth, B. Robinson, M.S. Brose, R. Elisei, M.A. Habra, K. Newbold, M.H. Shah, A.O. Hoff, A.G. Gianoukakis, N. Kiyota, M.H. Taylor, S.-B. Kim, M.K. Krzyzanowska, C.E. Dutcus, B. de las Heras, J. Zhu, S.I. Sherman, Lenvatinib versus placebo in radioiodine-refractory thyroid cancer. N. Engl. J. Med 372, 621 (2015). https://doi.org/10.1056/NEJMoa1406470

    Article  CAS  PubMed  Google Scholar 

  75. L.J. Wirth, C. Durante, D.J. Topliss, E. Winquist, E. Robenshtok, H. Iwasaki, M. Luster, R. Elisei, S. Leboulleux, M. Tahara, Lenvatinib for the treatment of radioiodine-refractory differentiated thyroid cancer: treatment optimization for maximum clinical benefit. Oncologist (2022). https://doi.org/10.1093/oncolo/oyac065

  76. M.S. Brose, B. Robinson, S.I. Sherman, J. Krajewska, C.-C. Lin, F. Vaisman, A.O. Hoff, E. Hitre, D.W. Bowles, J. Hernando, L. Faoro, K. Banerjee, J.W. Oliver, B. Keam, J. Capdevila, Cabozantinib for radioiodine-refractory differentiated thyroid cancer (COSMIC-311): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 22, 1126 (2021). https://doi.org/10.1016/S1470-2045(21)00332-6

    Article  CAS  PubMed  Google Scholar 

  77. B. Lin, H. Ma, M. Ma, Z. Zhang, Z. Sun, I.Y. Hsieh, O. Okenwa, H. Guan, J. Li, W. Lv, The incidence and survival analysis for anaplastic thyroid cancer: a SEER database analysis. Am. J. Transl. Res. 11, 5888 (2019)

    PubMed  PubMed Central  Google Scholar 

  78. E. Molinaro, C. Romei, A. Biagini, E. Sabini, L. Agate, S. Mazzeo, G. Materazzi, S. Sellari-Franceschini, A. Ribechini, L. Torregrossa, F. Basolo, P. Vitti, R. Elisei, Anaplastic thyroid carcinoma: from clinicopathology to genetics and advanced therapies. Nat. Rev. Endocrinol. 13, 644 (2017). https://doi.org/10.1038/nrendo.2017.76

    Article  CAS  PubMed  Google Scholar 

  79. K. Murshed, I. Al-Bozom, S. Vattoth, M. Akhtar, Mediastinal seminoma presenting as a neck mass falsely diagnosed as anaplastic thyroid carcinoma: a case report. Diagn. Cytopathol. 47, 334 (2019). https://doi.org/10.1002/dc.24090

    Article  PubMed  Google Scholar 

  80. E. Szczepanek‑Parulska, K. Piątek, P. Majewski, R. Czepczyński, J. Narożna, M. Ruchała, Unsuspected melanoma misdiagnosed as anaplastic thyroid carcinoma in fine‑needle aspiration biopsy. Pol. Arch. Intern. Med. 123, 558 (2013)

    Article  Google Scholar 

  81. H.J. Suh, H.J. Moon, J.Y. Kwak, J.S. Choi, E.K. Kim, Anaplastic thyroid cancer: ultrasonographic findings and the role of ultrasonography-guided fine needle aspiration biopsy. Yonsei Med. J. 54, 1400 (2013). https://doi.org/10.3349/ymj.2013.54.6.1400

    Article  PubMed  PubMed Central  Google Scholar 

  82. S. Ahmed, M.P. Ghazarian, M.E. Cabanillas, M.E. Zafereo, M.D. Williams, T. Vu, D.F. Schomer, J.M. Debnam, Imaging of anaplastic thyroid carcinoma. Am. J. Neuroradiol. 39, 547 (2018). https://doi.org/10.3174/ajnr.A5487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. A. Matrone, L. De Napoli, L. Torregrossa, A. Aghababyan, P. Papini, C.E. Ambrosini, R. Cervelli, C. Ugolini, F. Basolo, E. Molinaro, R. Elisei, G. Materazzi, Core needle biopsy can early and precisely identify large thyroid masses. Front. Oncol. 12, 1 (2022). https://doi.org/10.3389/fonc.2022.854755

    Article  Google Scholar 

  84. K.C. Bible, E. Kebebew, J. Brierley, J.P. Brito, M.E. Cabanillas, T.J. Clark, A. Di Cristofano, R. Foote, T. Giordano, J. Kasperbauer, K. Newbold, Y.E. Nikiforov, G. Randolph, M.S. Rosenthal, A.M. Sawka, M. Shah, A. Shaha, R. Smallridge, C.K. Wong-Clark, 2021 American Thyroid Association Guidelines for Management of Patients with Anaplastic Thyroid Cancer. Thyroid 31, 337 (2021). https://doi.org/10.1089/thy.2020.0944

    Article  PubMed  PubMed Central  Google Scholar 

  85. N. Pozdeyev, L.M. Gay, E.S. Sokol, R. Hartmaier, K.E. Deaver, S. Davis, J.D. French, P. Vanden Borre, D.V. LaBarbera, A.-C. Tan, R.E. Schweppe, L. Fishbein, J.S. Ross, B.R. Haugen, D.W. Bowles, Genetic analysis of 779 advanced differentiated and anaplastic thyroid cancers. Clin. Cancer Res. 24, 3059 (2018). https://doi.org/10.1158/1078-0432.CCR-18-0373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. C. Romei, A. Tacito, E. Molinaro, P. Piaggi, V. Cappagli, L. Pieruzzi, A. Matrone, D. Viola, L. Agate, L. Torregrossa, C. Ugolini, F. Basolo, L. De Napoli, M. Curcio, R. Ciampi, G. Materazzi, P. Vitti, R. Elisei, Clinical, pathological and genetic features of anaplastic and poorly differentiated thyroid cancer: a single institute experience. Oncol. Lett. (2018). https://doi.org/10.3892/ol.2018.8470

  87. S. De Leo, M. Trevisan, L. Fugazzola, Recent advances in the management of anaplastic thyroid cancer. Thyroid Res. 13, 17 (2020). https://doi.org/10.1186/s13044-020-00091-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. V. Subbiah, R.J. Kreitman, Z.A. Wainberg, J.Y. Cho, J.H.M. Schellens, J.C. Soria, P.Y. Wen, C.C. Zielinski, M.E. Cabanillas, A. Boran, P. Ilankumaran, P. Burgess, T. Romero Salas, B. Keam, Dabrafenib plus trametinib in patients with BRAF V600E-mutant anaplastic thyroid cancer: updated analysis from the phase II ROAR basket study. Ann. Oncol. 33, 406 (2022). https://doi.org/10.1016/j.annonc.2021.12.014

    Article  CAS  PubMed  Google Scholar 

  89. C. Dierks, J. Seufert, K. Aumann, J. Ruf, C. Klein, S. Kiefer, M. Rassner, M. Boerries, A. Zielke, P. La Rosee, P.T. Meyer, M. Kroiss, C. Weißenberger, T. Schumacher, P. Metzger, H. Weiss, C. Smaxwil, K. Laubner, J. Duyster, N. Von Bubnoff, C. Miething, O. Thomusch, Combination of lenvatinib and pembrolizumab is an effective treatment option for anaplastic and poorly differentiated thyroid carcinoma. Thyroid 31, 1076 (2021). https://doi.org/10.1089/thy.2020.0322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. L.J. Wirth, M.S. Brose, E.J. Sherman, L. Licitra, M. Schlumberger, S.I. Sherman, K.C. Bible, B. Robinson, P. Rodien, Y. Godbert, C. de la Fouchardiere, K. Newbold, C. Nutting, S. Misir, R. Xie, A. Almonte, W. Ye, M.E. Cabanillas, Open-label, single-arm, multicenter, phase ii trial of lenvatinib for the treatment of patients with anaplastic thyroid cancer. J. Clin. Oncol. 39, 2359 (2021). https://doi.org/10.1200/JCO.20.03093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. S. Filetti, C. Durante, D.M. Hartl, S. Leboulleux, L. D. Locati, K. Newbold, M.G. Papotti, A. Berruti, Clinical practice guideline update on the use of systemic therapy in advanced thyroid cancer. Ann. Oncol. (2022). https://doi.org/10.1016/j.annonc.2022.04.009

  92. G. Fadda, P. Straccia. The he Italian Reporting System for Thyroid Cytology. Thyroid FNA Cytol. (Springer Singapore, Singapore), 2019) 53–57

    Book  Google Scholar 

  93. P. Trimboli, M. Castellana, A. Piccardo, F. Romanelli, G. Grani, L. Giovanella, C. Durante, The ultrasound risk stratification systems for thyroid nodule have been evaluated against papillary carcinoma. A meta-analysis. Rev. Endocr. Metab. Disord. 22, 453 (2021). https://doi.org/10.1007/s11154-020-09592-3

    Article  PubMed  Google Scholar 

  94. D. Laha, N. Nilubol, M. Boufraqech, New therapies for advanced thyroid cancer. Front. Endocrinol. 11, 1 (2020). https://doi.org/10.3389/fendo.2020.00082

    Article  Google Scholar 

Download references

Author contributions

Conceptualisation: C.P., G.F.; Methodology: C.P., M.M., G.F.; Formal analysis and investigation: C.P., A.I.; Writing—original draft preparation: C.P., V.F.; Writing—review and editing: M.M., G.T., M.L.; Funding acquisition: G.F.; Resources: G.F., M.M.; Supervision: G.F. All authors read and approved the final paper.

Author information

Authors and Affiliations

  1. Department of Biomedical, Dental, Morphological and Functional Imaging Sciences, University of Messina, 98124, Messina, Italy

    Cristina Pizzimenti

  2. Department of Pathology, Foundation “Agostino Gemelli”, University Hospital IRCCS, 00168, Rome, Italy

    Vincenzo Fiorentino

  3. Department of Human Pathology of the Adulthood and Developing Age “Gaetano Barresi”, Section of Pathology, University of Messina, 98124, Messina, Italy

    Antonio Ieni, Maurizio Martini, Giovanni Tuccari, Maria Lentini & Guido Fadda

Authors
  1. Cristina Pizzimenti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vincenzo Fiorentino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonio Ieni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maurizio Martini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Giovanni Tuccari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Lentini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guido Fadda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristina Pizzimenti.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pizzimenti, C., Fiorentino, V., Ieni, A. et al. Aggressive variants of follicular cell-derived thyroid carcinoma: an overview. Endocrine 78, 1–12 (2022). https://doi.org/10.1007/s12020-022-03146-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-022-03146-0

Keywords

Search

Navigation