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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 volume 30, pages 189–200 (2019)Cite this article

Abstract

A re-named diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) likely impacts the prevalence of thyroid cancer and risk of malignancy in populations based on the established Bethesda System of Reporting Thyroid Cytopathology (TBSRTC). This study was done to investigate the prevalence and cytological distribution of NIFTP. PRISMA guided systematic review was done from a database search of Pubmed, EMBASE, and Medline using the search terms “non-invasive follicular thyroid neoplasm with papillary-like nuclear features”, “non-invasive follicular variant of papillary carcinoma”, “niftp”, and “Bethesda” until November 2018. Original articles with surgically proven diagnoses of NIFTP using strict NIFTP criteria were included. Twenty-nine studies with 1563 cases of NIFTP were included. The pooled prevalence of NIFTP in cases which would be classified previously as the follicular variant of papillary thyroid cancer (FVPTC) and papillary thyroid cancer (PTC) were 43.5% (95% CI 33.5–54.0%) and 4.4% (95% CI 2.0–9.0%) respectively. The pooled TBSRTC distribution of cases diagnosed as NIFTP was: from the non-diagnostic category 3.6% (95% CI 2.4–5.3%), benign 10.0% (95% CI 7.2–13.6%), AUS/FLUS 34.2% (95% CI 28.2–40.8%), FN/SFN 22.7% (95% CI 17.2–29.4%), suspicious for malignancy 22.4% (95% CI 17.7–27.9%), and malignant 7.5% (95% CI 4.2–12.9%). While a significant reduction in FVPTC prevalence is anticipated, a modest reduction of PTC prevalence is also expected with adoption of the NIFTP terminology that would be distributed mainly among lesions classified as indeterminate thyroid nodules. Further studies are needed to identify unique clinical characteristics of these lesions preoperatively.

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References

  1. Nikiforov, Y.E., Seethala, R.R., Tallini, G., Baloch, Z.W., Basolo, F., Thompson, L.D., Barletta, J.A., Wenig, B.M., Al Ghuzlan, A., Kakudo, K., Giordano, T.J., Alves, V.A., Khanafshar, E., Asa, S.L., El-Naggar, A.K., Gooding, W.E., Hodak, S.P., Lloyd, R.V., Maytal, G., Mete, O., Nikiforova, M.N., Nosé, V., Papotti, M., Poller, D.N., Sadow, P.M., Tischler, A.S., Tuttle, R.M., Wall, K.B., LiVolsi, V.A., Randolph, G.W., Ghossein, R.A.: 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 (2016). doi:https://doi.org/10.1001/jamaoncol.2016.0386

    Article  PubMed  PubMed Central  Google Scholar 

  2. Davies, L., Welch, H.G.: Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 295(18), 2164–2167 (2006). doi:https://doi.org/10.1001/jama.295.18.2164

    Article  CAS  PubMed  Google Scholar 

  3. Ahn, H.S., Kim, H.J., Welch, H.G.: Korea's thyroid-cancer "epidemic"--screening and overdiagnosis. N Engl J Med 371(19), 1765–1767 (2014). doi:https://doi.org/10.1056/NEJMp1409841

    Article  PubMed  Google Scholar 

  4. Hodak, S., Tuttle, R.M., Maytal, G., Nikiforov, Y.E., Randolph, G.: Changing the cancer diagnosis: the case of follicular variant of papillary thyroid cancer-primum non nocere and NIFTP. Thyroid 26(7), 869–871 (2016). doi:https://doi.org/10.1089/thy.2016.0205

    Article  PubMed  Google Scholar 

  5. Ramsey, S., Blough, D., Kirchhoff, A., Kreizenbeck, K., Fedorenko, C., Snell, K., Newcomb, P., Hollingworth, W., Overstreet, K.: Washington State cancer patients found to be at greater risk for bankruptcy than people without a cancer diagnosis. Health Aff (Millwood) 32(6), 1143–1152 (2013). doi:https://doi.org/10.1377/hlthaff.2012.1263

    Article  Google Scholar 

  6. Esserman, L.J., Thompson, I.M., Reid, B., Nelson, P., Ransohoff, D.F., Welch, H.G., Hwang, S., Berry, D.A., Kinzler, K.W., Black, W.C., Bissell, M., Parnes, H., Srivastava, S.: Addressing overdiagnosis and overtreatment in cancer: a prescription for change. Lancet Oncol 15(6), e234–e242 (2014). doi:https://doi.org/10.1016/S1470-2045(13)70598-9

    Article  PubMed  PubMed Central  Google Scholar 

  7. Faquin, W.C., Wong, L.Q., Afrogheh, A.H., Ali, S.Z., Bishop, J.A., Bongiovanni, M., Pusztaszeri, M.P., VandenBussche, C.J., Gourmaud, J., Vaickus, L.J., Baloch, Z.W.: 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 (2016). doi:https://doi.org/10.1002/cncy.21631

    Article  PubMed  Google Scholar 

  8. Canberk, S., Gunes, P., Onenerk, M., Erkan, M., Kilinc, E., Kocak Gursan, N., Kilicoglu, G.Z.: 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(3), 198–204 (2016). doi:https://doi.org/10.1159/000447990

    Article  PubMed  Google Scholar 

  9. Strickland, K.C., Vivero, M., Jo, V.Y., Lowe, A.C., Hollowell, M., Qian, X., Wieczorek, T.J., French, C.A., Teot, L.A., Sadow, P.M., Alexander, E.K., Cibas, E.S., Barletta, J.A., Krane, J.F.: Preoperative cytologic diagnosis of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a prospective analysis. Thyroid 26(10), 1466–1471 (2016). doi:https://doi.org/10.1089/thy.2016.0280

    Article  PubMed  Google Scholar 

  10. 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 64(12), 1149–1155 (2017). doi:https://doi.org/10.1507/endocrj.EJ17-0214

    Article  PubMed  Google Scholar 

  11. Wong, K.S., Strickland, K.C., Angell, T.E., Nehs, M.A., Alexander, E.K., Cibas, E.S., Krane, J.F., Howitt, B.E., Barletta, J.A.: The Flip side of NIFTP: an increase in rates of unfavorable histologic parameters in the remainder of papillary thyroid carcinomas. Endocr Pathol 28(2), 171–176 (2017). doi:https://doi.org/10.1007/s12022-017-9476-5

    Article  CAS  PubMed  Google Scholar 

  12. Bychkov, A., Keelawat, S., Agarwal, S., Jain, D., Jung, C.K., Hong, S., Lai, C.R., Satoh, S., Kakudo, K.: 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(4), 411–417 (2018). doi:https://doi.org/10.1016/j.pathol.2017.11.088

    Article  PubMed  Google Scholar 

  13. Lee, S.E., Hwang, T.S., Choi, Y.L., Kim, W.Y., Han, H.S., Lim, S.D., Kim, W.S., Yoo, Y.B., Kim, S.K.: Molecular profiling of papillary thyroid carcinoma in korea with a high prevalence of BRAF. Thyroid 27(6), 802–810 (2017). doi:https://doi.org/10.1089/thy.2016.0547

    Article  CAS  PubMed  Google Scholar 

  14. Lau, R.P., Paulsen, J.D., Brandler, T.C., Liu, C.Z., 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: a large academic institution’s experience. Am J Clin Pathol 149(1), 50–54 (2017). doi:https://doi.org/10.1093/ajcp/aqx136

    Article  PubMed  Google Scholar 

  15. Cibas, E.S., Ali, S.Z., Conference, N.T.F.S.o.t.S.: The Bethesda System For Reporting Thyroid Cytopathology. Am J Clin Pathol 132(5), 658–665 (2009). doi:https://doi.org/10.1309/AJCPPHLWMI3JV4LA

    Article  PubMed  Google Scholar 

  16. DerSimonian, R., Laird, N.: Meta-analysis in clinical trials revisited. Contemp Clin Trials 45(Pt A), 139–145 (2015). doi:https://doi.org/10.1016/j.cct.2015.09.002

    Article  PubMed  PubMed Central  Google Scholar 

  17. Higgins, J.P., Thompson, S.G., Deeks, J.J., Altman, D.G.: Measuring inconsistency in meta-analyses. BMJ 327(7414), 557–560 (2003). doi:https://doi.org/10.1136/bmj.327.7414.557

    Article  PubMed  PubMed Central  Google Scholar 

  18. Easterbrook, P.J., Berlin, J.A., Gopalan, R., Matthews, D.R.: Publication bias in clinical research. Lancet 337(8746), 867–872 (1991).

    Article  CAS  PubMed  Google Scholar 

  19. Jaconi, M., Manzoni, M., Pincelli, A.I., Giardini, V., Scardilli, M., Smith, A., Fellegara, G., Pagni, F.: The impact of the non-invasive follicular thyroid neoplasm with papillary-like nuclear feature terminology in the routine diagnosis of thyroid tumours. Cytopathology 28(6), 495–502 (2017). doi:https://doi.org/10.1111/cyt.12459

    Article  CAS  PubMed  Google Scholar 

  20. 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 46(2), 148–153 (2018). doi:https://doi.org/10.1002/dc.23866

    Article  PubMed  Google Scholar 

  21. Kim, M.J., Won, J.K., Jung, K.C., Kim, J.H., Cho, S.W., Park, D.J., Park, Y.J.: Clinical Characteristics of Subtypes of Follicular Variant Papillary Thyroid Carcinoma. Thyroid 28(3), 311–318 (2018). doi:https://doi.org/10.1089/thy.2016.0671

    Article  CAS  PubMed  Google Scholar 

  22. Bizzarro, T., Martini, M., Capodimonti, S., Straccia, P., Lombardi, C.P., Pontecorvi, A., Larocca, L.M., Rossi, E.D.: 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 124(10), 699–710 (2016). doi:https://doi.org/10.1002/cncy.21777

    Article  CAS  PubMed  Google Scholar 

  23. Mao, M.L., Joyal, T., Picado, O., Kerr, D., Lew, J.I., Farrá, J.C.: Noninvasive follicular thyroid neoplasm with papillary-like nuclear features reclassification and its impact on thyroid malignancy rate and treatment. J Surg Res 230, 47–52 (2018). doi:https://doi.org/10.1016/j.jss.2018.04.013

    Article  PubMed  Google Scholar 

  24. Kim, T.H., Lee, M., Kwon, A.Y., Choe, J.H., Kim, J.H., Kim, J.S., Hahn, S.Y., Shin, J.H., Chung, M.K., Son, Y.I., Ki, C.S., Yim, H.S., Kim, Y.L., Chung, J.H., Kim, S.W., Oh, Y.L.: Molecular genotyping of the non-invasive encapsulated follicular variant of papillary thyroid carcinoma. Histopathology 72(4), 648–661 (2018). doi:https://doi.org/10.1111/his.13401

    Article  PubMed  Google Scholar 

  25. Kiernan, C.M., Weiss, V.L., Mehrad, M., Ely, K., Baregamian, N., Solórzano, C.C.: 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(1), 55–59 (2018). doi:https://doi.org/10.1016/j.surg.2017.04.041

    Article  PubMed  Google Scholar 

  26. Mahajan, S., Agarwal, S., Kocheri, N., Jain, D., Mathur, S.R., Iyer, V.K.: Cytopathology of non-invasive follicular thyroid neoplasm with papillary-like nuclear features: A comparative study with similar patterned papillary thyroid carcinoma variants. Cytopathology 29(3), 233–240 (2018). doi:https://doi.org/10.1111/cyt.12537

    Article  CAS  PubMed  Google Scholar 

  27. Chandler, J.B., Colunga, M., Prasad, M.L., Callender, G.G., Quinn, C., Chhieng, D., Adeniran, A.J.: Identification of distinct cytomorphologic features in the diagnosis of NIFTP at the time of preoperative FNA: implications for patient management. Cancer Cytopathol 125(11), 865–875 (2017). doi:https://doi.org/10.1002/cncy.21910

    Article  PubMed  Google Scholar 

  28. Zhao, L., Dias-Santagata, D., Sadow, P.M., Faquin, W.C.: 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 125(5), 323–331 (2017). doi:https://doi.org/10.1002/cncy.21839

    Article  CAS  PubMed  Google Scholar 

  29. Yang, G.C.H., Fried, K.O., Scognamiglio, T.: Sonographic and cytologic differences of NIFTP from infiltrative or invasive encapsulated follicular variant of papillary thyroid carcinoma: a review of 179 cases. Diagn Cytopathol 45(6), 533–541 (2017). doi:https://doi.org/10.1002/dc.23709

    Article  PubMed  Google Scholar 

  30. Hahn, S.Y., Shin, J.H., Lim, H.K., Jung, S.L., Oh, Y.L., Choi, I.H., Jung, C.K.: Preoperative differentiation between noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) and non-NIFTP. Clin Endocrinol (Oxf) 86(3), 444–450 (2017). doi:https://doi.org/10.1111/cen.13263

    Article  CAS  Google Scholar 

  31. du Jour, K.P., Schmitt, A.C., Chen, A.Y., Griffith, C.C.: Application of strict criteria for noninvasive follicular thyroid neoplasm with papillary-like nuclear features and encapsulated follicular variant papillary thyroid carcinoma: a retrospective study of 50 tumors previously diagnosed as follicular variant PTC. Endocrine Pathology 29(1), 35–42 (2018). doi:https://doi.org/10.1007/s12022-017-9509-0

    Article  PubMed  Google Scholar 

  32. Strickland, K.C., Eszlinger, M., Paschke, R., Angell, T.E., Alexander, E.K., Marqusee, E., Nehs, M.A., Jo, V.Y., Lowe, A., Vivero, M., Hollowell, M., Qian, X.H., Wieczorek, T., French, C.A., Teot, L.A., Cibas, E.S., Lindeman, N.I., Krane, J.F., Barletta, J.A.: Molecular testing of nodules with a suspicious or malignant cytologic diagnosis in the setting of non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP). Endocrine Pathology 29(1), 68–74 (2018). doi:https://doi.org/10.1007/s12022-018-9515-x

    Article  PubMed  Google Scholar 

  33. Parente, D.N., Kluijfhout, W.P., Bongers, P.J., Verzijl, R., Devon, K.M., Rotstein, L.E., Goldstein, D.P., Asa, S.L., Mete, O., Pasternak, J.D.: Clinical safety of renaming encapsulated follicular variant of papillary thyroid carcinoma: is NIFTP truly benign? World J Surg 42(2), 321–326 (2018). doi:https://doi.org/10.1007/s00268-017-4182-5

    Article  PubMed  Google Scholar 

  34. Cho, U., Mete, O., Kim, M.H., Bae, J.S., Jung, C.K.: 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(6), 810–825 (2017). doi:https://doi.org/10.1038/modpathol.2017.9

    Article  CAS  PubMed  Google Scholar 

  35. Rosario, P.W., Mourão, G.F., Nunes, M.B., Nunes, M.S., Calsolari, M.R.: Noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Endocr Relat Cancer 23(12), 893–897 (2016). doi:https://doi.org/10.1530/ERC-16-0379

    Article  CAS  PubMed  Google Scholar 

  36. Maletta, F., Massa, F., Torregrossa, L., Duregon, E., Casadei, G.P., Basolo, F., Tallini, G., Volante, M., Nikiforov, Y.E., Papotti, M.: Cytological features of "noninvasive follicular thyroid neoplasm with papillary-like nuclear features" and their correlation with tumor histology. Hum Pathol 54, 134–142 (2016). doi:https://doi.org/10.1016/j.humpath.2016.03.014

    Article  CAS  PubMed  Google Scholar 

  37. Brandler, T.C., Zhou, F., Liu, C.Z., Cho, M., Lau, R.P., Simsir, A., Patel, K.N., Sun, W.: 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 (2017). doi:https://doi.org/10.1002/cncy.21848

    Article  CAS  PubMed  Google Scholar 

  38. Song, S.J., LiVolsi, V.A., Montone, K., Baloch, Z.: Pre-operative features of non-invasive follicular thyroid neoplasms with papillary-like nuclear features: an analysis of their cytological, Gene Expression Classifier and sonographic findings. Cytopathology 28(6), 488–494 (2017). doi:https://doi.org/10.1111/cyt.12501

    Article  CAS  PubMed  Google Scholar 

  39. Lastra, R.R., Birdsong, G., Hwang, D.H., Jorda, M., Kerr, D.A., McGrath, C., Odronic, S., Rao, R., VanderLaan, P.A., Walker, J.W., Antic, T.: Preoperative cytologic interpretation of noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a 1-year multi-institutional experience In, vol. 7. vol. 2, pp. 79–85. Elsevier Inc., Journal of the American Society of Cytopathology, (2018)

  40. Mito, J.K., Alexander, E.K., Angell, T.E., Barletta, J.A., Nehs, M.A., Cibas, E.S., Krane, J.F.: A modified reporting approach for thyroid FNA in the NIFTP era: a 1-year institutional experience. Cancer Cytopathol 125(11), 854–864 (2017). doi:https://doi.org/10.1002/cncy.21907

    Article  CAS  PubMed  Google Scholar 

  41. Lindeman, B.M., Nehs, M.A., Angell, T.E., Alexander, E.K., Gawande, A.A., Moore, F.D., Doherty, G.M., Cho, N.L.: 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 (2018). doi:https://doi.org/10.1245/s10434-018-6932-5, 26, 93, 97

    Article  PubMed  Google Scholar 

  42. Jiang, X.S., Harrison, G.P., Datto, M.B.: Young investigator challenge: molecular testing in noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Cancer Cytopathol 124(12), 893–900 (2016). doi:https://doi.org/10.1002/cncy.21802

    Article  CAS  PubMed  Google Scholar 

  43. Jung, C.K., Little, M.P., Lubin, J.H., Brenner, A.V., Wells, S.A., Sigurdson, A.J., Nikiforov, Y.E.: The increase in thyroid cancer incidence during the last four decades is accompanied by a high frequency of BRAF mutations and a sharp increase in RAS mutations. J Clin Endocrinol Metab 99(2), E276–E285 (2014). doi:https://doi.org/10.1210/jc.2013-2503

    Article  CAS  PubMed  Google Scholar 

  44. Hirokawa, M., Carney, J.A., Goellner, J.R., DeLellis, R.A., Heffess, C.S., Katoh, R., Tsujimoto, M., Kakudo, K.: Observer variation of encapsulated follicular lesions of the thyroid gland. Am J Surg Pathol 26(11), 1508–1514 (2002).

    Article  PubMed  Google Scholar 

  45. Paulson, V.A., Shivdasani, P., Angell, T.E., Cibas, E.S., Krane, J.F., Lindeman, N.I., Alexander, E.K., Barletta, J.A.: Noninvasive follicular thyroid neoplasm with papillary-like nuclear features accounts for more than half of "carcinomas" harboring RAS mutations. Thyroid 27(4), 506–511 (2017). doi:https://doi.org/10.1089/thy.2016.0583

    Article  CAS  PubMed  Google Scholar 

  46. Nikiforov, Y.E., Baloch, Z.W., Hodak, S.P., Giordano, T.J., Lloyd, R.V., Seethala, R.R., Wenig, B.M.: Change in diagnostic criteria for noninvasive follicular thyroid neoplasm with papillarylike nuclear features. JAMA Oncol 4(8), 1125–1126 (2018). doi:https://doi.org/10.1001/jamaoncol.2018.1446

    Article  PubMed  PubMed Central  Google Scholar 

  47. Yang, G.C.H., Fried, K.O.: Pathologic basis of the sonographic differences between thyroid cancer and noninvasive follicular thyroid neoplasm with papillary-like nuclear features. Ultrasonography 37(2), 157–163 (2018). doi:https://doi.org/10.14366/usg.17045

    Article  CAS  PubMed  Google Scholar 

  48. Díaz Del Arco, C., Fernández Aceñero, M.J.: 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 62(4), 265–272 (2018). doi:https://doi.org/10.1159/000488579

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine, University Minnesota, 516 Delaware St SE, Minneapolis, MN, 55455, USA

    Darin Ruanpeng & Rupendra T. Shrestha

  2. Department of Medicine, University of Mississippi Medical Center, Jackson, Mississippi, USA

    Wisit Cheungpasitporn

  3. Department of Medicine, Mayo Clinic, Rochester, MN, 55455, USA

    Charat Thongprayoon

  4. Department of Endocrinology, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, GZ-6, 02215, MA, USA

    James V. Hennessey

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Conceptualization and methodology, D.R. and R.T.S.; Software and formal analysis, W. C and C.T.; data curation, D.R., R.T.S, W.C., C.T.; writing—original draft preparation, D.R. and R.T.S; writing—review and editing R.T.S, J.V.H, W.C., C. T.; supervision: RTS.

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Correspondence to Rupendra T. Shrestha.

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Ruanpeng, D., Cheungpasitporn, W., Thongprayoon, C. et al. 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 30, 189–200 (2019). https://doi.org/10.1007/s12022-019-09583-4

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