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Preoperative Diagnostic Categories of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features in Thyroid Core Needle Biopsy and Its Impact on Risk of Malignancy

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Abstract

This study was designed to evaluate the preoperative diagnostic categories of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) using thyroid core needle biopsy (CNB) and to analyze its impact on the risk of malignancy (ROM). A total of 2687 consecutive thyroid CNBs were reviewed retrospectively and classified into six diagnostic categories using a standardized reporting system similar to the Bethesda System for Reporting Thyroid Cytopathology. Diagnostic categories of CNBs were compared with the final surgical diagnoses, and the ROM in each category was calculated both before and after excluding NIFTP from malignancy. Of 946 surgically resected cases, 683 were diagnosed as papillary thyroid carcinoma (PTC), and 32 (4.7% of PTC) were reclassified as NIFTP. The CNB diagnostic categories of NIFTP were as follows: follicular neoplasm in 20 (62.5%; 14, with nuclear atypia), indeterminate lesion in 11 (34.4%), and suspicious for malignancy in one (3.1%). When combined, NIFTP and encapsulated follicular variant of PTC (EFVPTC) were more often categorized as follicular neoplasm compared with other PTC variants including infiltrative FVPTC. Exclusion of NIFTP from malignant diagnosis led to a significant decrease in the ROM in follicular neoplasm with nuclear atypia category. Thus, thyroid CNB enables to differentiate NIFTP/EFVPTC from other PTCs, providing a useful guide for optimal treatment in patients with these tumors.

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References

  1. Cibas ES, Ali SZ (2009) The Bethesda System for Reporting Thyroid Cytopathology. Thyroid 19 (11):1159–1165.

    Article  PubMed  Google Scholar 

  2. Cibas ES, Ali SZ (2017) The 2017 Bethesda System for Reporting Thyroid Cytopathology. Thyroid 27 (11):1341–1346.

    Article  PubMed  Google Scholar 

  3. Bongiovanni M, Spitale A, Faquin WC, Mazzucchelli L, Baloch ZW (2012) The Bethesda System for Reporting Thyroid Cytopathology: a meta-analysis. Acta Cytol 56 (4):333–339.

    Article  PubMed  Google Scholar 

  4. Kiernan CM, Broome JT, Solorzano CC (2014) The Bethesda system for reporting thyroid cytopathology: a single-center experience over 5 years. Ann Surg Oncol 21 (11):3522–3527.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Naim C, Karam R, Edde D (2013) Ultrasound-guided fine-needle aspiration biopsy of the thyroid: methods to decrease the rate of unsatisfactory biopsies in the absence of an on-site pathologist. Can Assoc Radiol J 64 (3):220–225.

    Article  PubMed  Google Scholar 

  6. Straccia P, Rossi ED, Bizzarro T, Brunelli C, Cianfrini F, Damiani D, Fadda G (2015) A meta-analytic review of the Bethesda System for Reporting Thyroid Cytopathology: has the rate of malignancy in indeterminate lesions been underestimated? Cancer Cytopathol 123 (12):713–722.

    Article  PubMed  Google Scholar 

  7. Anderson TJ, Atalay MK, Grand DJ, Baird GL, Cronan JJ, Beland MD (2014) Management of nodules with initially nondiagnostic results of thyroid fine-needle aspiration: can we avoid repeat biopsy? Radiology 272 (3):777–784.

    Article  PubMed  Google Scholar 

  8. Choi SH, Baek JH, Lee JH, Choi YJ, Hong MJ, Song DE, Kim JK, Yoon JH, Kim WB (2014) Thyroid nodules with initially non-diagnostic, fine-needle aspiration results: comparison of core-needle biopsy and repeated fine-needle aspiration. Eur Radiol 24 (11):2819–2826.

    Article  PubMed  Google Scholar 

  9. Hahn SY, Shin JH, Han BK, Ko EY, Ko ES (2013) Ultrasonography-guided core needle biopsy for the thyroid nodule: does the procedure hold any benefit for the diagnosis when fine-needle aspiration cytology analysis shows inconclusive results? Br J Radiol 86 (1025):20130007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Na DG, Kim JH, Sung JY, Baek JH, Jung KC, Lee H, Yoo H (2012) Core-needle biopsy is more useful than repeat fine-needle aspiration in thyroid nodules read as nondiagnostic or atypia of undetermined significance by the Bethesda system for reporting thyroid cytopathology. Thyroid 22 (5):468–475.

    Article  PubMed  Google Scholar 

  11. Baek JH (2017) Current status of core needle biopsy of the thyroid. Ultrasonography 36 (2):83–85.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yoon RG, Baek JH, Lee JH, Choi YJ, Hong MJ, Song DE, Kim JK, Yoon JH, Kim WB (2014) Diagnosis of thyroid follicular neoplasm: fine-needle aspiration versus core-needle biopsy. Thyroid 24 (11):1612–1617.

    Article  PubMed  Google Scholar 

  13. Nasrollah N, Trimboli P, Guidobaldi L, Cicciarella Modica DD, Ventura C, Ramacciato G, Taccogna S, Romanelli F, Valabrega S, Crescenzi A (2013) Thin core biopsy should help to discriminate thyroid nodules cytologically classified as indeterminate. A new sampling technique. Endocrine 43 (3):659–665.

    Article  CAS  PubMed  Google Scholar 

  14. Kim HC, Kim YJ, Han HY, Yi JM, Baek JH, Park SY, Seo JY, Kim KW (2017) First-line use of core needle biopsy for high-yield preliminary diagnosis of thyroid nodules. AJNR Am J Neuroradiol 38 (2):357–363.

    Article  CAS  PubMed  Google Scholar 

  15. Suh CH, Baek JH, Lee JH, Choi YJ, Kim JK, Sung TY, Yoon JH, Shong YK (2016) The role of core-needle biopsy as a first-line diagnostic tool for initially detected thyroid nodules. Thyroid 26 (3):395–403.

    Article  PubMed  Google Scholar 

  16. Trimboli P, Nasrollah N, Guidobaldi L, Taccogna S, Cicciarella Modica DD, Amendola S, Romanelli F, Lenzi A, Nigri G, Centanni M, Giovanella L, Valabrega S, Crescenzi A (2014) The use of core needle biopsy as first-line in diagnosis of thyroid nodules reduces false negative and inconclusive data reported by fine-needle aspiration. World J Surg Oncol 12:61.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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, Nose V, Papotti M, Poller DN, Sadow PM, Tischler AS, Tuttle RM, Wall KB, LiVolsi VA, 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 (8):1023–1029.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Rosario PW, Mourao GF, Nunes MB, Nunes MS, Calsolari MR (2016) Noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Endocr Relat Cancer 23 (12):893–897.

    Article  CAS  PubMed  Google Scholar 

  19. Xu B, Farhat N, Barletta JA, Hung YP, Biase D, Casadei GP, Onenerk AM, Tuttle RM, Roman BR, Katabi N, Nose V, Sadow P, Tallini G, Faquin WC, Ghossein R (2018) Should subcentimeter non-invasive encapsulated, follicular variant of papillary thyroid carcinoma be included in the noninvasive follicular thyroid neoplasm with papillary-like nuclear features category? Endocrine 59 (1):143–150.

    Article  CAS  PubMed  Google Scholar 

  20. 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 (4):512–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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 (8):1125–1126.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Faquin WC, Wong LQ, Afrogheh AH, Ali SZ, Bishop JA, Bongiovanni M, Pusztaszeri MP, VandenBussche CJ, 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 (3):181–187.

    Article  PubMed  Google Scholar 

  23. Strickland KC, Howitt BE, Marqusee E, Alexander EK, Cibas ES, Krane JF, Barletta JA (2015) The impact of noninvasive follicular variant of papillary thyroid carcinoma on rates of malignancy for fine-needle aspiration diagnostic categories. Thyroid 25 (9):987–992.

    Article  PubMed  Google Scholar 

  24. Zhou H, Baloch ZW, Nayar R, Bizzarro T, Fadda G, Adhikari-Guragain D, Hatem J, Larocca LM, Samolczyk J, Slade J, Rossi ED (2018) Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): implications for the risk of malignancy (ROM) in the Bethesda System for Reporting Thyroid Cytopathology (TBSRTC). Cancer Cytopathol 126 (1):20–26.

    Article  CAS  PubMed  Google Scholar 

  25. Chung SR, Baek JH, Lee JH, Lee YM, Sung TY, Chung KW, Hong SJ, Jeon MJ, Kim TY, Shong YK, Kim WB, Kim WG, Song DE (2019) Risk of malignancy according to the sub-classification of atypia of undetermined significance and suspicious follicular neoplasm categories in thyroid core needle biopsies. Endocr Pathol 30 (2):146–154.

    Article  CAS  PubMed  Google Scholar 

  26. Jeon MJ, Song DE, Jung CK, Kim WG, Kwon H, Lee YM, Sung TY, Yoon JH, Chung KW, Hong SJ, Baek JH, Lee JH, Kim TY, Shong YK, Kim WB (2016) Impact of reclassification on thyroid nodules with architectural atypia: from non-invasive encapsulated follicular variant papillary thyroid carcinomas to non-invasive follicular thyroid neoplasm with papillary-like nuclear features. PLoS One 11 (12):e0167756.

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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 (3):171–178.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Alexander EK, Heering JP, Benson CB, Frates MC, Doubilet PM, Cibas ES, Marqusee E (2002) Assessment of nondiagnostic ultrasound-guided fine needle aspirations of thyroid nodules. The Journal of clinical endocrinology and metabolism 87 (11):4924–4927.

    Article  CAS  PubMed  Google Scholar 

  29. Grani G, Calvanese A, Carbotta G, D’Alessandri M, Nesca A, Bianchini M, Del Sordo M, Fumarola A (2013) Intrinsic factors affecting adequacy of thyroid nodule fine-needle aspiration cytology. Clinical endocrinology 78 (1):141–144.

    Article  PubMed  Google Scholar 

  30. Choe JY, Kwak Y, Kim M, Chung YR, Kim HJ, Kim YK, Park SY (2018) Utility of a formatted pathologic reporting system in thyroid core needle biopsy: a validation study of 1998 consecutive cases. Clin Endocrinol (Oxf) 88 (1):96–104.

    Article  CAS  Google Scholar 

  31. Puxeddu E, Filetti S (2009) The 2009 American Thyroid Association Guidelines for management of thyroid nodules and differentiated thyroid cancer: progress on the road from consensus- to evidence-based practice. Thyroid 19 (11):1145–1147.

    Article  PubMed  Google Scholar 

  32. Moon WJ, Baek JH, Jung SL, Kim DW, Kim EK, Kim JY, Kwak JY, Lee JH, Lee JH, Lee YH, Na DG, Park JS, Park SW, Korean Society of Thyroid R, Korean Society of R (2011) Ultrasonography and the ultrasound-based management of thyroid nodules: consensus statement and recommendations. Korean J Radiol 12 (1):1–14, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Jung CK, Min HS, Park HJ, Song DE, Kim JH, Park SY, Yoo H, Shin MK, Korean Endocrine Pathology Thyroid Core Needle Biopsy Study G (2015) Pathology reporting of thyroid core needle biopsy: a proposal of the Korean Endocrine Pathology Thyroid Core Needle Biopsy Study Group. J Pathol Transl Med 49 (4):288–299, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Bychkov A, Hirokawa M, Jung CK, Liu Z, Zhu Y, Hong SW, Satoh S, Lai CR, Huynh L, Kakudo K (2017) Low rate of noninvasive follicular thyroid neoplasm with papillary-like nuclear features in Asian practice. Thyroid 27 (7):983–984.

    Article  PubMed  Google Scholar 

  35. 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 (12):1149–1155.

    Article  PubMed  Google Scholar 

  36. Singh R, Avila J, Jo K, Nguyen KTK, Carrillo NR, Huang EC, Campbell MJ (2017) Patients with non-invasive follicular thyroid neoplasm with papillary-like nuclear features are unlikely to have malignant preoperative cytology. Ann Surg Oncol 24 (11):3300–3305.

    Article  PubMed  Google Scholar 

  37. Hahn SY, Shin JH, Lim HK, Jung SL, Oh YL, Choi IH, Jung CK (2017) Preoperative differentiation between noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) and non-NIFTP. Clinical endocrinology 86 (3):444–450.

    Article  CAS  PubMed  Google Scholar 

  38. Brandler TC, Zhou F, Liu CZ, Cho M, Lau RP, Simsir A, Patel KN, Sun W (2017) Can noninvasive follicular thyroid neoplasm with papillary-like nuclear features be distinguished from classic papillary thyroid carcinoma and follicular adenomas by fine-needle aspiration? Cancer Cytopathol 125 (6):378–388.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82, Gumi-ro 173 Beon-gil, Bundang-gu, Seongnam, Gyeonggi, 13620, Republic of Korea

    Hee Young Na, Ji Won Woo & So Yeon Park

  2. Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea

    Jae Hoon Moon

  3. Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea

    June Young Choi

  4. Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea

    Woo-Jin Jeong

  5. Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea

    Yeo Koon Kim

  6. Department of Pathology, Hallym University Sacred Heart Hospital, Anyang, Gyeonggi, Republic of Korea

    Ji-Young Choe

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  1. Hee Young Na
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Correspondence to So Yeon Park.

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Ethical Approval

This study was approved by the Institutional Review Board (IRB) of the Seoul National University Bundang Hospital (IRB No. B-1812-510-108). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Na, H.Y., Woo, J.W., Moon, J.H. et al. Preoperative Diagnostic Categories of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features in Thyroid Core Needle Biopsy and Its Impact on Risk of Malignancy. Endocr Pathol 30, 329–339 (2019). https://doi.org/10.1007/s12022-019-09590-5

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