BACKGROUND: A low-risk thyroid tumour, non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) was introduced in 2016. NIFTP criteria require a thorough histological examination to rule out capsular and lymphovascular invasion, which denies the possibility of preoperative cytological diagnosis. Nevertheless, since the adoption of the new entity, the cytology of NIFTP has been a subject of interest. OBJECTIVES: The present systematic review and meta-analysis investigate the cytological diagnosis of NIFTP. METHOD: An online PubMed literature search was conducted between March 1, 2020, and June 30, 2020, for all original articles considering the cytology of histologically proven NIFTP. The studies including data on fine needle aspiration specimens classified by The Bethesda System for Reporting Thyroid Cytology (TBSRTC) categories, risk of malignancy (ROMs) in the TBSRTC categories, and cytomorphological features of NIFTP were included in the meta-analysis. Non-English studies and case reports were excluded. The data were tabulated and statistical analysis was performed with Open Meta-Analyst program. RESULTS: Fifty-eight studies with a total of 2,553 NIFTP cases were included in the study. The pooled prevalence of NIFTP cases was calculated among 25,892 surgically resected cases from 20 studies and the results show that NIFTP consisted 4.4% (95% confidence interval [CI]: 3.5-5.4%) of all cases. Most of the NIFTP cases (79.0%) belonged to the intermediate categories of TBSRTC. The pooled distribution of NIFTP cases in each TBSRTC category was 1.3% (95% CI: 0.8-1.7%) in non-diagnostic (ND), 8.9% (95% CI: 6.9-10.8%) in benign, 29.2% (95% CI: 25.0-33.4%) in atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS), 24.2% (95% CI: 19.6-28.9%) in follicular neoplasm (FN), 19.5% (95% CI: 16.1-22.9%) in suspicious for malignancy (SM), and 6.9% (95% CI: 5.2-8.7%) in malignant. Compared to pre-NIFTP era, the pooled risk differences of ROM were reduced by 2.4% in ND, 2.7% in benign, 8.2% in AUS/FLUS, 8.2% in FN, 7.3% in SM, and 1.1% in the malignant category. The cytomorphological features of NIFTP were similar to follicular variant of papillary thyroid carcinoma (FVPTC) but lesser to papillary thyroid carcinoma (PTC). CONCLUSIONS: Based on our results, NIFTP remains a histological diagnosis. Although cytomorphological features cannot be used in differentiating NIFTP from FVPTC, they may guide in separating NIFTP from PTC. Features such as papillae, microfollicles, giant cells, psammoma bodies, and the amount of papillary-like nuclear features should be taken into account when suspicious of NIFTP. NIFTP should not have papillae or psammoma bodies, and giant cells were rarely observed.

Department of Biology Faculty of Medicine in Pilsen Charles University Pilsen Czechia

Department of Otorhinolaryngology and Head and Neck Surgery 1st Faculty of Medicine Charles University University Hospital Motol Prague Czechia

Pathology Fimlab Laboratories Tampere Finland

Tampere University Faculty of Medicine and Health Technology Tampere Finland

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Lloyd R, Osamura R, Klöppel G, Rosai J. WHO classification of tumours of endocrine organs. 4th ed. 2017. pp. p. 1–355.

Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 2006;295((18)):2164–7. PubMed

Ahn HS, Kim HJ, Kim KH, Lee YS, Han SJ, Kim Y, et al. Thyroid cancer screening in South Korea increases detection of papillary cancers with no impact on other subtypes or thyroid cancer mortality. Thyroid. 2016;26((11)):1535–40. PubMed

Ahn HS, Kim HJ, Welch HG. Korea's thyroid-cancer “epidemic”: screening and overdiagnosis. N Engl J Med. 2014;371((19)):1765–7. PubMed

Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, 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. PubMed PMC

Hodak S, Tuttle RM, Maytal G, Nikiforov YE, Randolph G. Changing the cancer diagnosis: the case of follicular variant of papillary thyroid cancer − primum non nocere and NIFTP. Thyroid. 2016;26((7)):869–71. PubMed

Liu J, Singh B, Tallini G, Carlson DL, Katabi N, Shaha A, et al. Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer. 2006;107((6)):1255–64. PubMed

Rossi ED, Faquin WC. NIFTP revised: chronicle of a change foretold. Cancer Cytopathol. 2018;126((11)):897–901. PubMed

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. PubMed

Vivero M, Kraft S, Barletta JA. Risk stratification of follicular variant of papillary thyroid carcinoma. Thyroid. 2013;23((3)):273–9. PubMed

Nikiforov YE, Seethala RR, Tallini G, Baloch ZW, Basolo F, Thompson LD, 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. PubMed PMC

Haugen BR, Sawka AM, Alexander EK, Bible KC, Caturegli P, Doherty GM, 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. PubMed

Livolsi VA, Baloch Z. Noninvasive follicular tumor with papillary-like nuclear features: a practice changer in thyroid pathology. Arch Pathol Lab Med. 2020 Mar 30 PubMed

Ferris RL, Nikiforov Y, Terris D, Seethala RR, Ridge JA, Angelos P, et al. AHNS series: do you know your guidelines? AHNS endocrine section consensus statement: state-of-the-art thyroid surgical recommendations in the era of noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Head Neck. 2018;40((9)):1881–8. PubMed PMC

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. 2016;26((9)):1167–72. PubMed

Kakudo K. Asian and western practice in thyroid pathology: similarities and differences. Gland Surg. 2020;9((5)):1614–27. PubMed PMC

Nikiforov YE, Baloch ZW, Hodak SP, Giordano TJ, Lloyd RV, Seethala RR, et al. Change in diagnostic criteria for noninvasive follicular thyroid neoplasm with papillarylike nuclear features. JAMA Oncol. 2018;4((8)):1125–6. PubMed PMC

Alves VAF, Kakudo K, LiVolsi V, Lloyd RV, Nikiforov YE, Nosé V, et al. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): achieving better agreement by refining diagnostic criteria. Clinics. 2018;73:e576–4. PubMed PMC

Cibas ES, Ali SZ. The 2017 Bethesda system for reporting thyroid cytopathology. J Am Soc Cytopathol. 2017;6((6)):217–22. PubMed

Faquin WC, Wong LQ, Afrogheh AH, Ali SZ, Bishop JA, Bongiovanni M, 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)):181–7. PubMed

Kim M, Kim JE, Kim HJ, Chung YR, Kwak Y, Park SY. 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. 2018;52((3)):171–8. PubMed PMC

Mahajan S, Agarwal S, Kocheri N, Jain D, Mathur SR, Iyer VK. Cytopathology of non-invasive follicular thyroid neoplasm with papillary-like nuclear features: a comparative study with similar patterned papillary thyroid carcinoma variants. Cytopathology. 2018;29((3)):233–40. PubMed

Maletta F, Massa F, Torregrossa L, Duregon E, Casadei GP, Basolo F, et al. Cytological features of “noninvasive follicular thyroid neoplasm with papillary-like nuclear features” and their correlation with tumor histology. Hum Pathol. 2016;54:134–42. PubMed

Rosario PW, Mourão GF, Nunes MB, Nunes MS, Calsolari MR. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Endocr Relat Cancer. 2016;23((12)):893–7. PubMed

Shrestha RT, Ruanpeng D, Hennessey JV. Cytomorphology of noninvasive follicular thyroid neoplasm with papillary-like nuclear features and the impact of new nomenclature on molecular testing. Med Sci. 2019;7((2)):15. PubMed PMC

Strickland KC, Howitt BE, Barletta JA, Cibas ES, Krane JF. Suggesting the cytologic diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): a retrospective analysis of atypical and suspicious nodules. Cancer Cytopathol. 2018;126((2)):86–93. PubMed

Baloch ZW, Seethala RR, Faquin WC, Papotti MG, Basolo F, Fadda G, et al. 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)):616–20. PubMed

Lau RP, Paulsen JD, Brandler TC, Liu CZ, Simsir A, Zhou F. Impact of the reclassification of “noninvasive encapsulated follicular variant of papillary thyroid carcinoma” to “noninvasive follicular thyroid neoplasm with papillary-like nuclear features” on the Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol. 2018;149((1)):50–4. PubMed

Saglietti C, Bongiovanni M. The value of cytological examination in the diagnosis of noninvasive thyroid neoplasm with papillary-like nuclear features (NIFTP) J Basic Clin Med. 2017;6((1)):57–60.

Brandler TC, Zhou F, Liu CZ, Cho M, Lau RP, Simsir A, et al. 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. 2017;125((6)):378–88. PubMed

Brandler T, Cho M, Wei X-J, Simms A, Levine P, Hernandez O, et al. Noninvasive follicular thyroid neoplasm with papillary like nuclear features: an interobserver study of key cytomorphological features from a large academic medical centre. Cytopathology. 2019;30((1)):39–45. PubMed

Bychkov A, Keelawat S, Agarwal S, Jain D, Jung CK, Hong S, et al. 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. 2018;50((4)):411–7. PubMed

Celik M, Bulbul BY, Can N, Ayturk S, Tastekin E, Sezer A, et al. Comparison of clinicopathological features in patients with noninvasive follicular thyroid neoplasm with papillary-like nuclear features and follicular variant papillary thyroid cancer. Pol Arch Intern Med. 2020;130((2)):100–5. PubMed

Chandler JB, Colunga M, Prasad ML, Callender GG, Quinn C, Chhieng D, et al. Identification of distinct cytomorphologic features in the diagnosis of NIFTP at the time of preoperative FNA: implications for patient management. Cancer Cytopathol. 2017;125((11)):865–75. PubMed

Díaz Del Arco C, Fernández Aceñero MJ. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: can cytology face the challenge of diagnosis in the light of the new classification? Acta Cytol. 2018;62((4)):265–72. PubMed

Hahn SY, Shin JH, Lim HK, Jung SL, Oh YL, Choi IH, et al. Preoperative differentiation between noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) and non-NIFTP. Clin Endocrinol. 2017;86((3)):444–50. PubMed

Hirokawa M, Higuchi M, Suzuki A, Hayashi T, Kuma S, Miyauchi A. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a single-institutional experience in Japan. Endocr J. 2017;64((12)):1149–55. PubMed

Hirokawa M, Higuchi M, Suzuki A, Hayashi T, Kuma S, Miyauchi A. Prevalence and diagnostic significance of noninvasive follicular thyroid neoplasm with papillary-like nuclear features among tumors previously diagnosed as follicular adenoma: a single-institutional study in Japan. Endocr J. 2020;67((10)):1071–5. PubMed

Howitt BE, Chang S, Eszlinger M, Paschke R, Drage MG, Krane JF, et al. Fine-needle aspiration diagnoses of noninvasive follicular variant of papillary thyroid carcinoma. Am J Clin Pathol. 2015;144((6)):850–7. PubMed

Ibrahim AA, Wu HH. Fine-needle aspiration cytology of noninvasive follicular variant of papillary thyroid carcinoma is cytomorphologically distinct from the invasive counterpart. Am J Clin Pathol. 2016;146((3)):373–7. PubMed

Jaconi M, Manzoni M, Pincelli AI, Giardini V, Scardilli M, Smith A, et al. The impact of the non-invasive follicular thyroid neoplasm with papillary-like nuclear feature terminology in the routine diagnosis of thyroid tumours. Cytopathology. 2017;28((6)):495–502. PubMed

Katsakhyan L, Song S, Lepe M, Shojaei H, Montone KT, LiVolsi VA, et al. Practice paradigms before and after introduction of the diagnosis-noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): an institutional experience. Endocr Pathol. 2020;31((2)):174–81. PubMed

Ke J, Jianyong L, Ying L, Genpeng L, Linlin S, Zhihui L, et al. The use of the Bethesda system for reporting thyroid cytopathology in a Chinese population: an analysis of 13,351 specimens. Diagn Cytopathol. 2019;47((9)):876–80. PubMed

Kiernan CM, Weiss VL, Mehrad M, Ely K, Baregamian N, Solórzano CC. New terminology noninvasive follicular neoplasm with papillary-like nuclear features (NIFTP) and its effect on the rate of malignancy at a single institution. Surgery. 2018;163((1)):55–9. PubMed

Kopczyński J, Suligowska A, Niemyska K, Pałyga I, Walczyk A, Gąsior-Perczak D, 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. 2020;31((2)):143–9. PubMed

Koshikawa T, Fujita N, Ueda N, Ota Y, Sasaki E, Murakami Y, et al. Important cytological findings for distinction between follicular variant and conventional papillary thyroid carcinoma, including noninvasive follicular thyroid tumors with papillary-like nuclear features. Endocr J. 2019;66((5)):475–83. PubMed

Larouche V, Pusztaszeri MP, Filimon S, Payne R, Hier M, Tamilia M. Preoperative prediction of non-invasive follicular thyroid neoplasm with papillary-like nuclear features: a Canadian single-centre experience. J Otolaryngol Head Neck Surg. 2020;49((1)):1–8. PubMed PMC

Lastra RR, Birdsong G, Hwang DH, Jorda M, Kerr DA, McGrath C, et al. Preoperative cytologic interpretation of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a 1-year multi-institutional experience. J Am Soc Cytopathol. 2018;7((2)):79–85. PubMed

Layfield LJ, Baloch ZW, Esebua M, Kannuswamy R, Schmidt RL. Impact of the reclassification of the non-invasive follicular variant of papillary carcinoma as benign on the malignancy risk of the Bethesda system for reporting thyroid cytopathology: a meta-analysis study. Acta Cytol. 2017;61((3)):187–93. PubMed

Lee HS, Lee JW, Park JH, Kim WS, Han HS, Lee SE. Comprehensive analysis for diagnosis of preoperative non-invasive follicular thyroid neoplasm with papillary-like nuclear features. PLoS One. 2019;14((7)):e0218046–14. PubMed PMC

Legesse T, Parker L, Heath J, Staats PN. Distinguishing non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) from classic and invasive follicular-variant papillary thyroid carcinomas based on cytologic features. J Am Soc Cytopathol. 2019;8((1)):11–7. PubMed

Li W, Sciallis A, Lew M, Pang J, Jing X. Implementing noninvasive follicular thyroid neoplasm with papillary-like nuclear features may potentially impact the risk of malignancy for thyroid nodules categorized as AUS/FLUS and FN/SFN. Diagn Cytopathol. 2018;46((2)):148–53. PubMed

Lindeman BM, Nehs MA, Angell TE, Alexander EK, Gawande AA, Moore FD, et al. Effect of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) on malignancy rates in thyroid nodules: how to counsel patients on extent of surgery. Ann Surg Oncol. 2019;26((1)):93–7. PubMed

Linhares SM, Whitfield BW, Lee AF, Gordillo D, Picado O, Jeraq M, et al. Impact of noninvasive follicular thyroid neoplasm with papillary-like nuclear features on revised bethesda system malignancy rates at a single institution. J Surg Res. 2020;255:152–7. PubMed

Mainthia R, Wachtel H, Chen Y, Mort E, Parangi S, Sadow PM, et al. Evaluating the projected surgical impact of reclassifying noninvasive encapsulated follicular variant of papillary thyroid cancer as noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Surgery. 2018;163((1)):60–5. PubMed PMC

Maleki S, Zandvakili A, Gera S, Khutti SD, Gersten A, Khader SN. Differentiating noninvasive follicular thyroid neoplasm with papillary-like nuclear features from classic papillary thyroid carcinoma: analysis of cytomorphologic descriptions using a novel machine-learning approach sara. J Pathol Inform. 2019;10((29)) PubMed PMC

Mao ML, Joyal T, Picado O, Kerr D, Lew JI, Farrá JC. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features reclassification and its impact on thyroid malignancy rate and treatment. J Surg Res. 2018;230:47–52. PubMed

Mito JK, Alexander EK, Angell TE, Barletta JA, Nehs MA, Cibas ES, et al. A modified reporting approach for thyroid FNA in the NIFTP era: a 1-year institutional experience. Cancer Cytopathol. 2017;125((11)):854–64. PubMed

Ohori NP, Wolfe J, Carty SE, Yip L, LeBeau SO, Berg AN, et al. The influence of the noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) resection diagnosis on the false-positive thyroid cytology rate relates to quality assurance thresholds and the application of NIFTP criteria. Cancer Cytopathol. 2017;125((9)):692–700. PubMed

Paulson VA, Shivdasani P, Angell TE, Cibas ES, Krane JF, Lindeman NI, et al. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features accounts for more than half of “carcinomas” harboring RAS mutations. Thyroid. 2017;27((4)):506–11. PubMed

Rana C, Manjunath S, Ramakant P, Singh K, Babu S, Mishra A. Noninvasive follicular neoplasm with papillary like nuclear features: a comprehensive analysis with a diagnostic algorithm. Diagn Cytopathol. 2020;48((4)):330–41. PubMed

Range DE, Jiang X. Noninvasive follicular thyroid neoplasm with papillary like nuclear features and the risk of malignancy in the Bethesda system for the reporting of thyroid cytopathology. Diagn Cytopathol. 2020;48((6)):531–7. PubMed

Rosenblum RC, Shtabsky A, Marmor S, Trejo L, Yaish I, Barnes S, et al. Indeterminate nodules by the Bethesda system for reporting thyroid cytopathology in Israel: frequency, and risk of malignancy after reclassification of follicular thyroid neoplasm with papillary-like features. Eur J Surg Oncol. 2019;45((7)):1182–7. PubMed

Selvaggi SM. The presence of multinucleated giant cells: noninvasive follicular thyroid neoplasm with papillary-like nuclear features versus the follicular variant of papillary thyroid carcinoma. Diagn Cytopathol. 2019;47((10)):1007–10. PubMed

Singh R, Avila J, Jo K, Nguyen KTK, Carrillo NR, Huang EC, et al. Patients with non-invasive follicular thyroid neoplasm with papillary-like nuclear features are unlikely to have malignant preoperative cytology. Ann Surg Oncol. 2017;24((11)):3300–5. PubMed

Sohn SY, Lee JJ, Lee JH. Molecular profile and clinicopathologic features of follicular variant papillary thyroid carcinoma. Pathol Oncol Res. 2020;26((2)):927–36. PubMed

Song SJ, Livolsi VA, Montone K, Baloch Z. Preoperative features of noninvasive follicular thyroid neoplasms with papillary features: an analysis of their cytological, gene expression classifier and sonographic findings. Cytopathology. 2017;28((6)):488–94. PubMed

Strickland KC, Howitt BE, Marqusee E, Alexander EK, Cibas ES, Krane JF, et al. The impact of noninvasive follicular variant of papillary thyroid carcinoma on rates of malignancy for fine-needle aspiration diagnostic categories. Thyroid. 2015;25((9)):987–92. PubMed

Strickland KC, Vivero M, Jo VY, Lowe AC, Hollowell M, Qian X, et al. Preoperative cytologic diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a prospective analysis. Thyroid. 2016;26((10)):1466–71. PubMed

Sung S, Margolskee E, Chen D, Tiscornia-Wasserman P. Incidence of noninvasive follicular thyroid neoplasm with papillary-like nuclear features and change in risk of malignancy for “the Bethesda system for reporting thyroid cytology”. J Am Soc Cytopathol. 2019;8((3)):133–40. PubMed

Ventura M, Melo M, Fernandes G, Carrilho F. Risk of malignancy in thyroid cytology: the impact of the reclassification of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) Endocr Pract. 2019;25((7)):642–7. PubMed

Yan L, Sethi S, Park J-W. Cytologic and clinical features of NIFTP: can we diagnose based on preoperative fine needle aspiration. Diagn Cytopathol. 2019;47((12)):1259–66. PubMed

You S-H, Lee KE, Yoo R-E, Choi HJ, Jung KC, Won J-K, et al. Prevention of total thyroidectomy in noninvasive follicular thyroid neoplasm with papillary like nuclear features (NIFTP) based on combined interpretation of ultrasonographic and cytopathologic results. Clin Endocrinol. 2018;88((1)):114–22. PubMed

Zhang Z, Chhieng D, Harshan M, Zheng X, Zakowski M. Cytological features of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) J Am Soc Cytopathol. 2019;8((1)):5–10. PubMed

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 Cytopathol. 2017;125((5)):323–31. PubMed

Zhou H, Baloch ZW, Nayar R, Bizzarro T, Fadda G, Adhikari-Guragain D, et al. 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. 2018;126((1)):20–6. PubMed

Zhu Y, Song Y, Xu G, Fan Z, Ren W. The Bethesda system for reporting thyroid cytopathology (TBSRTC): a report of 2,781 cases in a Chinese population. Chin J Cancer Res. 2020;32((2)):140–8. PubMed PMC

Bizzarro T, Martini M, Capodimonti S, Straccia P, Lombardi CP, Pontecorvi A, et al. 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 Cytopathol. 2016;124((10)):699–710. PubMed

Boursier L, Clerc Urmes I, Garon J, Klein M, Demarquet L. Ultrasound and cytological characteristics of non-invasive follicular thyroid neoplasm with papillary-like nuclear features compared to papillary carcinomas. Ann Endocrinol. 2020;81((1)):28–33. PubMed

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;29((3)):276–88. PubMed PMC

Vuong HG, Ngo HTT, Bychkov A, Jung CK, Vu TH, Lu KB, et al. Differences in surgical resection rate and risk of malignancy in thyroid cytopathology practice between western and Asian countries: a systematic review and meta-analysis. Cancer Cytopathol. 2020;128((4)):238–49. PubMed

Kakudo K, Kameyama K, Miyauchi A, Nakamura H. Introducing the reporting system for thyroid fine-needle aspiration cytology according to the new guidelines of the Japan thyroid association. Endocr J. 2014;61((6)):539–52. PubMed

Kakudo K, Higuchi M, Hirokawa M, Satoh S, Jung CK, Bychkov A. Thyroid FNA cytology in Asian practice active surveillance for indeterminate thyroid nodules reduces overtreatment of thyroid carcinomas. Cytopathology. 2017;28((6)):455–66. PubMed

Rana C, Vuong HG, Nguyen TQ, Nguyen HC, Jung CK, Kakudo K, et al. The incidence of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a meta-analysis assessing worldwide impact of the reclassification. Thyroid. 2021 PubMed

Ruanpeng D, Cheungpasitporn W, Thongprayoon C, Hennessey JV, Shrestha RT. 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. Endocr Pathol. 2019;30((3)):189–200. PubMed

Nishino M. How is noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) shaping the way we interpret thyroid cytology? J Am Soc Cytopathol. 2019;8((1)):1–4. PubMed

Seethala RR, Baloch ZW, Barletta JA, Khanafshar E, Mete O, Sadow PM, et al. Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a review for pathologists. Mod Pathol. 2018;31((1)):39–55. PubMed

Johannessen JV, Sobrinho-Simões M. The origin and significance of thyroid psammoma bodies. Lab Invest. 1980;43((3)):287–96. PubMed

Haugen BR. 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: what is new and what has changed? Cancer. 2017;123((3)):372–81. PubMed

Noninvasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features (NIFTP): Tumour Entity with a Short History. A Review on Challenges in Our Microscopes, Molecular and Ultrasonographic Profile