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Did Introducing a New Category of Thyroid Tumors (Non-invasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features) Decrease the Risk of Malignancy for the Diagnostic Categories in the Bethesda System for Reporting Thyroid Cytopathology?

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Abstract

In 2016, Nikiforov et al. (JAMA Oncol 2:1023–1029, 2016) proposed replacing the term “non-invasive encapsulated follicular variant of papillary thyroid carcinoma” (FVPTC) with the term “non-invasive follicular thyroid neoplasm with papillary-like nuclear features” (NIFTP). In 2018, to avoid the misdiagnosis of papillary thyroid cancer as NIFTP, the authors proposed changes to the criteria for NIFTP classification. Some previous studies evaluated the impact of NIFTP on the risk of malignancy (ROM) in the fine-needle aspiration cytology (FNAC) diagnostic categories according to the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC). However, little is known about the influence of an NIFTP diagnosis on ROM on the basis of the revised criteria. The aim of this study was to assess the influence of NIFTP on ROM using the revised diagnostic criteria. The present study included 998 thyroid nodules that were diagnosed and resected at the same medical center. All specimens with a diagnosis of cancer were reviewed to identify NIFTP according to the revised 2018 criteria. Additionally, molecular diagnostics were performed to detect the BRAF p.V600E mutation and TERT promoter mutations in all the NIFTP cases. The number of cases that met the revised criteria was determined, and the ROM was calculated in each of the FNAC diagnostic categories. Only five cases (2.3% of all papillary thyroid carcinoma diagnoses) were considered NIFTP, according to the 2018 criteria. With respect to the FNAC category, one case was a follicular neoplasm or suspicious for a follicular neoplasm (FN/SFN), three cases were suspicious for malignancy (SM), and one case was malignant (M). The ROM decreased in each of the Bethesda categories (0.7% in FN/SFN, 4.3% in SM, and 0.5% in M) when a diagnosis of NIFTP was taken into account. These reductions were not statistically significant. These data indicate that the NIFTP entity has very little impact on ROM for the diagnostic categories of the Bethesda system.

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References

  1. Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LD, Barletta JA, Wenig BM, al Ghuzlan A, Kakudo K, Giordano TJ, Alves VA, Khanafshar E, Asa SL, el-Naggar AK, Gooding WE, Hodak SP, Lloyd RV, Maytal G, Mete O, Nikiforova MN, Nosé V, Papotti M, Poller DN, Sadow PM, Tischler AS, Tuttle RM, Wall KB, LiVolsi V, Randolph GW, Ghossein RA (2016) Nomenclature Revision for Encapsulated Follicular Variant of Papillary Thyroid Carcinoma: A Paradigm Shift to Reduce Overtreatment of Indolent Tumors. JAMA Oncol 2: 1023–1029. https://doi.org/10.1001/jamaoncol.2016.0386.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Haugen BR, Sawka AM, Alexander EK, Bible KC, Caturegli P, Doherty GM, Mandel SJ, Morris JC, Nassar A, Pacini F, Schlumberger M, Schuff K, Sherman SI, Somerset H, Sosa JA, Steward DL, Wartofsky L, Williams MD (2017) 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: 481–483. https://doi.org/10.1089/thy.2016.0628.

    Article  CAS  PubMed  Google Scholar 

  3. WHO classification of tumours of endocrine organs; Weltgesundheitsorganisation, Lloyd RV, Osamura RY, Klöppel G, Rosai J (2017) International Agency for Research on Cancer, Eds.; World Health Organization classification of tumours; 4th edition. International Agency for Research on Cancer: Lyon. ISBN 978–92–832-4493-6.

  4. Xu B, Tallini G, Scognamiglio T, Roman BR, Tuttle RM, Ghossein RA (2017) Outcome of Large Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features. Thyroid 27: 512–517. https://doi.org/10.1089/thy.2016.0649.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kim MJ, Won JK, Jung KC, Kim JH, Cho SW, Park DJ & Park YJ (2018) Clinical characteristics of subtypes of follicular variant papillary thyroid carcinoma. Thyroid 28: 311–318. https://doi.org/10.1089/thy.2016.0671.

    Article  CAS  PubMed  Google Scholar 

  6. Cho U, Mete O, Kim MH, Bae JS, Jung CK (2017) Molecular correlates and rate of lymph node metastasis of non-invasive follicular thyroid neoplasm with papillary-like nuclear features and invasive follicular variant papillary thyroid carcinoma: the impact of rigid criteria to distinguish non-invasive follicular thyroid neoplasm with papillary-like nuclear features. Mod. Pathol 30: 810–825. https://doi.org/10.1038/modpathol.2017.9.

    Article  CAS  PubMed  Google Scholar 

  7. Nikiforov YE, Baloch ZW, Hodak SP, Giordano TJ, Lloyd RV, Seethala RR, Wenig BM (2018) Change in Diagnostic Criteria for Noninvasive Follicular Thyroid Neoplasm With Papillary like Nuclear Features. JAMA Oncol 4:1125–1126. https://doi.org/10.1001/jamaoncol.2018.1446.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Parente DN, Kluijfhout WP, Bongers PJ, Verzijl R, Devon KM, Rotstein LE, Goldstein DP, Asa SL, Mete O, Pasternak JD (2018) Clinical Safety of Renaming Encapsulated Follicular Variant of Papillary Thyroid Carcinoma: Is NIFTP Truly Benign? World J Surg 42: 321–326. https://doi.org/10.1007/s00268-017-4182-5.

    Article  PubMed  Google Scholar 

  9. Bin Xu, Rene Serrette, R. Michael Tuttle, Bayan Alzumaili, Ian Ganly, Nora Katabi, Giovanni Tallini, and Ronald Ghossein (2019)How Many Papillae in Conventional Papillary Carcinoma? A Clinical Evidence-Based Pathology Study of 235 Unifocal Encapsulated Papillary Thyroid Carcinomas, with Emphasis on the Diagnosis of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features. Thyroid 29:1792–1803. https://doi.org/10.1089/thy.2019.0328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Bongiovanni M, Giovanella L, Romanelli F, Trimboli P (2019) Cytological Diagnoses Associated with Noninvasive Follicular Thyroid Neoplasms with Papillary-Like Nuclear Features According to the Bethesda System for Reporting Thyroid Cytopathology: A Systematic Review and Meta-Analysis. Thyroid 29: 222–228. https://doi.org/10.1089/thy.2018.0394.

    Article  PubMed  Google Scholar 

  11. Bychkov A, Keelawat S, Agarwal S, Jain D, Jung CK, Hong S, Lai CR, Satoh S, Kakudo K (2018) Impact of non-invasive follicular thyroid neoplasm with papillary-like nuclear features on the Bethesda system for reporting thyroid cytopathology: a multi-institutional study in five Asian countries. Pathology 50: 11–417. https://doi.org/10.1016/j.pathol.2017.11.088.

    Article  Google Scholar 

  12. Canberk S, Gunes P, Onenerk M, Erkan M, Kilinc E, Kocak Gursan N, Kilicoglu GZ (2016) New Concept of the Encapsulated Follicular Variant of Papillary Thyroid Carcinoma and Its Impact on the Bethesda System for Reporting Thyroid Cytopathology: A Single-Institute Experience. Acta Cytol.60:198–204. https://doi.org/10.1159/000447990.

    Article  PubMed  Google Scholar 

  13. Faquin WC, Wong LQ, Afrogheh AH, Ali SZ, Bishop JA, Bongiovanni M, Pusztaszeri MP, VandenBussche C, Gourmaud J, Vaickus LJ, Baloch ZW (2016) 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 124: 181–187. https://doi.org/10.1002/cncy.21631.

    Article  PubMed  Google Scholar 

  14. Kiernan CM, Weiss VL, Mehrad M, Ely K, Baregamian N, Solórzano CC (2018) New terminology-noninvasive follicular neoplasm with papillary-like nuclear features (NIFTP) and its effect on the rate of malignancy at a single institution. Surgery 163: 55–59. https://doi.org/10.1016/j.surg.2017.04.041.

    Article  PubMed  Google Scholar 

  15. Kim M, Kim JE, Kim HJ, Chung YR, Kwak Y, Park SY (2018) Cytologic Diagnosis of Noninvasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features and Its Impact on the Risk of Malignancy in the Bethesda System for Reporting Thyroid Cytopathology: An Institutional Experience. J Pathol Transl Med 52: 171–178. https://doi.org/10.4132/jptm.2018.04.03.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kopczyński J, Suligowska A, Niemyska K et al (2019) The influence of the reclassification of NIFTP as an uncertain tumour on risk of malignancy for the diagnostic categories according to the Bethesda system for reporting thyroid cytopathology. Endokrynol Pol 70: 232–236. https://doi.org/10.5603/EP.a2019.0008.

    Article  PubMed  Google Scholar 

  17. Bychkov A, Jung CK, Liu Z, Kakudo K (2018) Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features in Asian Practice: Perspectives for Surgical Pathology and Cytopathology. Endocr. Pathol. 29: 276–288. https://doi.org/10.1007/s12022-018-9519-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ruanpeng D, Cheungpasitporn W, Thongprayoon C, Hennessey JV & Shrestha RT (2019) Systematic review and meta-analysis of the impact of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) on cytological diagnosis and thyroid cancer prevalence. Endocrine Pathology 30: 189–200. https://doi.org/10.1007/s12022-019-09583-4.

    Article  CAS  PubMed  Google Scholar 

  19. Hirokawa M, Higuchi M, Suzuki A, Hayashi T, Kuma S, Miyauchi A (2017) Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a single-institutional experience in Japan. Endocr J 64: 1149–1155. https://doi.org/10.1507/endocrj.EJ17-0214.

    Article  PubMed  Google Scholar 

  20. Song YS, Lim JA, Park YJ (2015) Mutation Profile of Well-Differentiated Thyroid Cancer in Asians. Endocrinol Metab (Seoul) 30: 252–262. https://doi.org/10.3803/EnM.2015.30.3.252.

    Article  CAS  Google Scholar 

  21. Hirokawa M, Carney JA, Goellner JR, DeLellis RA, Heffess CS, Katoh R, Tsujimoto M, Kakudo K (2002) Observer variation of encapsulated follicular lesions of the thyroid gland. Am. J. Surg. Pathol. 26: 1508–1514.

    Article  PubMed  Google Scholar 

  22. Kakudo K, Higuchi M, Hirokawa M, Satoh S, Jung CK & Bychkov A. (2017) Thyroid FNA cytology in Asian practice-active surveillance for indeterminate thyroid nodules reduces overtreatment of thyroid carcinomas. Cytopathology 28: 455–466. https://doi.org/10.1111/cyt.12491

    Article  CAS  PubMed  Google Scholar 

  23. Lee SE, Hwang TS, Choi YL, Kim WY, Han HS, Lim SD, Kim WS, Yoo YB, Kim SK (2017) Molecular Profiling of Papillary Thyroid Carcinoma in Korea with a High Prevalence of BRAFV600E Mutation. Thyroid 27: 802–810. doi: https://doi.org/10.1089/thy.2016.0547.

    Article  CAS  PubMed  Google Scholar 

  24. Vuong HG, Tran TT, Bychkov A, Jung CK, Nakazawa T, Kakudo K, Katoh R, Kondo T (2019) Clinical impact of non- invasive follicular thyroid neoplasm with papillary like nuclear features on the risk of malignancy in the Bethesda System for reporting thyroid cytopathology: A meta-analysis od 14,153 resected thyroid nodules. Endocr Pract 25: 491–502. https://doi.org/10.4158/EP-2018-0506.

    Article  PubMed  Google Scholar 

  25. Ventura M, Melo M, Fernandes G, Carrilho F (2019) Risk of malignancy in thyroid cytology: The impact of the reclassification of noninvasive follicular thyroid neoplasm with papillary-like nuclear features. (NIFTP). Endocr Pract. 25:642–647. https://doi.org/10.4158/EP-2018-0423.

    Article  PubMed  Google Scholar 

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Funding

This project was granted under the program of the Minister of Science and Higher Education entitled as Regional Initiative of Excellence in the years, project no 024/RID/2018/19,

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Authors and Affiliations

  1. Department of Surgical Pathology, Holycross Cancer Center, Kielce, Poland

    Janusz Kopczyński & Kornelia Niemyska

  2. Endocrinology Clinic, Holycross Cancer Center, Artwińskiego 3 Street, 25-734, Kielce, Poland

    Agnieszka Suligowska, Iwona Pałyga, Agnieszka Walczyk, Danuta Gąsior-Perczak, Ryszard Mężyk & Aldona Kowalska

  3. Department of Molecular Diagnostics, Holycross Center, Kielce, Poland

    Artur Kowalik & Kinga Hińcza

  4. Oncology Clinic, Holycross Cancer Center, Kielce, Poland

    Stanisław Góźdź

  5. Collegium Medicum, Jan Kochanowski University, Kielce, Poland

    Stanisław Góźdź & Aldona Kowalska

Authors
  1. Janusz Kopczyński
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  2. Agnieszka Suligowska
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  3. Kornelia Niemyska
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Contributions

Conceptualization: Janusz Kopczyński, Agnieszka Suligowska. Methodology: Kornelia Niemyska, Ryszard Mężyk. Formal analysis and investigation: Iwona Pałyga, Agnieszka Walczyk. Writing—original draft preparation: Janusz Kopczyński, Aldona Kowalska. Writing—review and editing: Agnieszka Suligowska, Kinga Hińcza. Funding acquisition: Artur Kowalik. Resources: Danuta Gąsior-Perczak, Artur Kowalik. Supervision: Aldona Kowalska, Stanisław Góźdź.

Corresponding author

Correspondence to Agnieszka Suligowska.

Ethics declarations

The study plan was approved by the Bioethics Committee of the Regional Chamber of Physicians of Kielce. Patients’ written informed consent was obtained when molecular studies were performed. All patients with NIFTP tumors provided written consent for molecular testing for the BRAF p.V600E and hTERT promoter mutations.

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The authors declare that they have no conflict of interest.

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Kopczyński, J., Suligowska, A., Niemyska, K. et al. Did Introducing a New Category of Thyroid Tumors (Non-invasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features) Decrease the Risk of Malignancy for the Diagnostic Categories in the Bethesda System for Reporting Thyroid Cytopathology?. Endocr Pathol 31, 143–149 (2020). https://doi.org/10.1007/s12022-020-09619-0

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