Abstract
Objective
Noninvasive follicular neoplasm with papillary-like nuclear features (NIFTP) is the term to describe what was previously known as encapsulated follicular variant of papillary thyroid carcinoma. This new paradigm shift was agreed upon by experts in the field. The objective of this study is to evaluate cases previously diagnosed as follicular adenomas, follicular variant of papillary thyroid carcinoma and hyperplastic nodules to be reclassified as NIFTP according to the new criteria. Furthermore, the clinical follow-up of these NIFTP cases is evaluated.
Methods
This retrospective study reviewed potential NIFTP cases over the last 13 years, at Jordan University Hospital.
Results
A total of 811 thyroid surgery reports were identified and revised to identify the potential NIFTP cases. The review yielded 173 cases identified as potential NIFTP cases. Further pathological slide review resulted in a revised diagnosis of 32 cases of NIFTP according to the new criteria. The NIFTP cases comprised 4% of the total number of thyroidectomy cases and 16.1% of the total pool of previously diagnosed papillary thyroid carcinoma cases at our institution. While 111 cases retained their original diagnosis. Follow-up showed that all patients are alive and well with no evidence of disease.
Conclusion
Patients with NIFTP are not uncommon and the diagnosis is made only after a thorough evaluation of excision. Therefore, initial conservative management of solitary thyroid nodules suspicious for NIFTP in the form of lobectomy is recommended to avoid unnecessary total thyroidectomies. Our follow-up of NIFTP cases is similar to all previous reports.
Similar content being viewed by others
References
V. Chaudhary, S. Bano, Thyroid ultrasound. Indian J. Endocrinol. Metab. 17, 219–227 (2013). https://doi.org/10.4103/2230-8210.109667
D.S. Dean, H. Gharib, Epidemiology of thyroid nodules. Best. Pract. Res Clin. Endocrinol. Metab. 22, 901–911 (2008)
D.J. Finley, B. Zhu, C.B. Barden, T.J. Fahey III, Discrimination of benign and malignant thyroid nodules by molecular profiling. Ann. Surg. 240, 425–436 (2004). discussion 436-7
J. Yang, V. Schnadig, R. Logrono, P.G. Wasserman, Fine-needle aspiration of thyroid nodules: a study of 4703 patients with histologic and clinical correlations. Cancer 111, 306–315 (2007). https://doi.org/10.1002/cncr.22955
H. Gharib, Fine-needle aspiration biopsy of thyroid nodules: advantages, limitations, and effect. Mayo Clin. Proc. 69, 44–49 (1994)
H. Gharib, J.R. Goellner, Fine-needle aspiration biopsy of the thyroid: an appraisal. Ann. Intern. Med. 118, 282–289 (1993)
S.I. Sherman, Thyroid carcinoma. Lancet 361, 501–511 (2003)
J.J. Wiltshire, T.M. Drake, L. Uttley, S.P. Balasubramanian, Systematic review of trends in the incidence rates of thyroid cancer. Thyroid (2016). https://doi.org/10.1089/thy.2016.0100
J.R. Burgess, P. Tucker, Incidence trends for papillary thyroid carcinoma and their correlation with thyroid surgery and thyroid fine-needle aspirate cytology. Thyroid 16, 47–53 (2006). https://doi.org/10.1089/thy.2006.16.47
M.H. Hajeer, H.A. Awad, N.I. Abdullah, G.H. Almuhaisen, L.E. Abudalu, The rising trend in papillary thyroid carcinoma: true increase or over diagnosis? Saudi Med. J. 39, 147–153 (2018). https://doi.org/10.15537/smj.2018.2.21211
A. Ogbera, S. Kuku, Epidemiology of thyroid diseases in Africa. Indian J. Endocrinol. Metab. (2011). https://doi.org/10.4103/2230-8210.83331
S.I. Sherman, P. Angelos, D.W. Ball, D. Byrd, O.H. Clark, G.H. Daniels, R.A. Dilawari, H. Ehya, W.B. Farrar, R.F. Gagel, F. Kandeel, R.T. Kloos, P. Kopp, D.M. Lamonica, T.R. Loree, W.M. Lydiatt, J. McCaffrey, J.A. Olson, J.A. Ridge, J.P. Shah, J.C. Sisson, R.M. Tuttle, M.M. Urist, Thyroid carcinoma. J. Natl Compr. Cancer Netw. (2007)
J. Drábek, J. Gatek, J. Lukas, J. Drabek, D. Lukas, L. Dusek, The epidemiology of thyroid cancer in the Czech Republic in comparison with other countries. Biomed. Pap. Med Fac. Univ. Palacky. Olomouc Czech Repub. 157, 266–275 (2012). https://doi.org/10.5507/bp.2012.086
M. Kim, M.J. Jeon, H.-S. Oh, S. Park, T.Y. Kim, Y.K. Shong, W.B. Kim, K. Kim, W.G. Kim, D.E. Song, BRAF and RAS mutational status in noninvasive follicular thyroid neoplasm with papillary-like nuclear features and invasive subtype of encapsulated follicular variant of papillary thyroid carcinoma in Korea. Thyroid 28, 504–510 (2018). https://doi.org/10.1089/thy.2017.0382
Z. Liu, A. Bychkov, C.K. Jung, M. Hirokawa, S. Sui, S.W. Hong, C.R. Lai, D. Jain, S. Canberk, K. Kakudo, Interobserver and intraobserver variation in the morphological evaluation of noninvasive follicular thyroid neoplasm with papillary-like nuclear features in Asian practice. Pathol. Int. 69, 202–210 (2019). https://doi.org/10.1111/pin.12779
Y. Ito, A. Miyauchi, M. Kihara, M. Fukushima, T. Higashiyama, A. Miya, Overall survival of papillary thyroid carcinoma patients: a single-institution long-term follow-up of 5897 patients. World J. Surg. (2018). https://doi.org/10.1007/s00268-018-4479-z
S.O. Sebastian, J.M.R. Gonzalez, P.P. Paricio, J.S. Perez, D.P. Flores, A.P. Madrona, P.R. Romero, F.J. Tebar, Papillary thyroid carcinoma. Arch. Surg. 135, 272 (2000). https://doi.org/10.1001/archsurg.135.3.272
E.L. Mazzaferri, R.L. Young, Papillary thyroid carcinoma: a 10 year foliow-up report of the impact of therapy in 576 patients. Am. J. Med. (1981). https://doi.org/10.1016/0002-9343(81)90573-8
S.A. Hundahl, I.D. Fleming, A.M. Fremgen, H.R. Menck, A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985–1995. Cancer 83, 2638–2648 (1998). https://doi.org/10.1002/(sici)1097-0142(19981215)83:123.0.co;2-1
R. Rahbari, L. Zhang, E. Kebebew, Thyroid cancer gender disparity. Future Oncol. 6, 1771–1779 (2010). https://doi.org/10.2217/fon.10.127
S. Lindsay, Carcinoma of the thyroid gland: a clinical and pathologic study of 293 patients at the University of California Hospital. Calif. Med. 93(4), 261 (1960)
A.K.Y. Lam, C.Y. Lo, K.S.L. Lam, Papillary carcinoma of thyroid: a 30-yr clinicopathological review of the histological variants. Endocr. Pathol. 16, 323–330 (2005)
M.J. Kim, J.-K. Won, K.C. Jung, J. Kim, S.W. Cho, D.J. Park, Y.J. Park, Clinical characteristics of subtypes of follicular variant papillary thyroid carcinoma. Thyroid. 28, 311–318 (2018). https://doi.org/10.1089/thy.2016.0671
S. Gupta, O. Ajise, L. Dultz, B. Wang, D. Nonaka, J. Ogilvie, K.S. Heller, K.N. Patel, Follicular variant of papillary thyroid cancer: encapsulated, nonencapsulated, and diffuse: distinct biologic and clinical entities. Arch. Otolaryngol. Neck Surg. 138, 227 (2012). https://doi.org/10.1001/archoto.2011.1466
J. Liu, B. Singh, G. Tallini, D.L. Carlson, N. Katabi, A. Shaha, R.M. Tuttle, R.A. Ghossein, Follicular variant of papillary thyroid carcinoma: a clinicopathologic study of a problematic entity. Cancer. (2006). https://doi.org/10.1002/cncr.22138
Y.E. Nikiforov, R.R. Seethala, G. Tallini, Z.W. Baloch, F. Basolo, L.D.R. Thompson, J.A. Barletta, B.M. Wenig, A. Al Ghuzlan, K. Kakudo, T.J. Giordano, V.A. Alves, E. Khanafshar, S.L. Asa, A.K. El-Naggar, W.E. Gooding, S.P. Hodak, R.V. Lloyd, G. Maytal, O. Mete, M.N. Nikiforova, V. Nosé, M. Papotti, D.N. Poller, P.M. Sadow, A.S. Tischler, T.R. Michael, K.B. Wall, V.A. LiVolsi, G.W. Randolph, R.A. Ghossein, Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol. (2016). https://doi.org/10.1001/jamaoncol.2016.0386
Y.E. Nikiforov, Z.W. Baloch, S.P. Hodak, T.J. Giordano, R.V. Lloyd, R.R. Seethala, B.M. Wenig, Change in diagnostic criteria for noninvasive follicular thyroid neoplasm with papillarylike nuclear features. JAMA Oncol. (2018)
D. Fonseca, S. Bhuyan, SS. Murthy, V. Rao, C. Rao, KVVN. Raju, C. Sundaram, Noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a distinct clinicopathologic entity. Indian J. Pathol. Microbiol. 61, 380–382 (2018)
L.D.R. Thompson, D.N. Poller, K. Kakudo, R. Burchette, Y.E. Nikiforov, R.R. Seethala, An international interobserver variability reporting of the nuclear scoring criteria to diagnose noninvasive follicular thyroid neoplasm with papillary-like nuclear features: a validation study. Endocr. Pathol. 29, 242–249 (2018). https://doi.org/10.1007/s12022-018-9520-0
A. Bychkov, S. Keelawat, S. Agarwal, D. Jain, C.K. Jung, S.W. Hong, C.R. Lai, S. Satoh, K. Kakudo, 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, 411–417 (2018). https://doi.org/10.1016/j.pathol.2017.11.088
W.C. Faquin, L.Q. Wong, A.H. Afrogheh, S.Z. Ali, J.A. Bishop, M. Bongiovanni, M.P. Pusztaszeri, C.J. VandenBussche, J. Gourmaud, L.J. Vaickus, Z.W. Baloch, 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 (2016). https://doi.org/10.1002/cncy.21631
F. Maletta, F. Massa, L. Torregrossa, E. Duregon, G.P. Casadei, F. Basolo, G. Tallini, M. Volante, Y.E. Nikiforov, M. Papotti, Cytological features of “noninvasive follicular thyroid neoplasm with papillary-like nuclear features” and their correlation with tumor histology. Hum. Pathol. 54, 134–142 (2016). https://doi.org/10.1016/J.HUMPATH.2016.03.014
Z.W. Baloch, R.R. Seethala, W.C. Faquin, M.G. Papotti, F. Basolo, G. Fadda, G.W. Randolph, S.P. Hodak, Y.E. Nikiforov, S.J. Mandel, Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): a changing paradigm in thyroid surgical pathology and implications for thyroid cytopathology. Cancer Cytopathol. 124, 616–620 (2016). https://doi.org/10.1002/cncy.21744
J.F. Krane, E.K. Alexander, E.S. Cibas, J.A. Barletta, Coming to terms with NIFTP: a provisional approach for cytologists. Cancer Cytopathol. 124, 767–772 (2016). https://doi.org/10.1002/cncy.21769
V.A.F. Alves, K. Kakudo, V. LiVolsi, R.V. Lloyd, Y.E. Nikiforov, V. Nosé, M. Papotti, L.D.R. Thompson, Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): achieving better agreement by refining diagnostic criteria. Clin. 73, e576 (2018). https://doi.org/10.6061/clinics/2018/e576
V.A. Paulson, P. Shivdasani, T.E. Angell, E.S. Cibas, J.F. Krane, N.I. Lindeman, E.K. Alexander, J.A. Barletta, Noninvasive follicular thyroid neoplasm with papillary-like nuclear features accounts for more than half of “carcinomas” harboring RAS mutations. Thyroid 27, 506–511 (2017). https://doi.org/10.1089/thy.2016.0583
L. Zhao, D. Dias-Santagata, P.M. Sadow, W.C. Faquin, 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, 323–331 (2017). https://doi.org/10.1002/cncy.21839
K.P. Du Jour, A.C. Schmitt, A.Y. Chen, C.C. Griffith, 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. Endocr. Pathol. 29, 35–42 (2018)
T.C. Brandler, F. Zhou, C.Z. Liu, M. Cho, R.P. Lau, A. Simsir, K.N. Patel, W. Sun, 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, 378–388 (2017). https://doi.org/10.1002/cncy.21848
J.B. Chandler, M. Colunga, M.L. Prasad, G.G. Callender, C. Quinn, D. Chhieng, A.J. Adeniran, Identification of distinct cytomorphologic features in the diagnosis of NIFTP at the time of preoperative FNA: implications for patient management. Cancer Cytopathol. 125, 865–875 (2017). https://doi.org/10.1002/cncy.21910
S.-H. You, K.E. Lee, R.-E. Yoo, H.J. Choi, K.C. Jung, J.-K. Won, K.M. Kang, T.J. Yoon, S.H. Choi, C.-H. Sohn, J. Kim, 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. 88, 114–122 (2018). https://doi.org/10.1111/cen.13473
P.W. Rosario, G.F. Mourão, Noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP): a review for clinicians. Endocr. Relat. Cancer 26, R259–R266 (2019). https://doi.org/10.1530/ERC-19-0048
R.T. Shrestha, D. Ruanpeng, J.V. Hennessey, Cytomorphology of noninvasive follicular thyroid neoplasm with papillary-like nuclear features and the impact of new nomenclature on molecular testing. Med. Sci. 7, 15 (2019). https://doi.org/10.3390/medsci7020015
H.G. Vuong, T.T.K. Tran, A. Bychkov, C.K. Jung, T. Nakazawa, K. Kakudo, R. Katoh, T. Kondo, 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 of 14,153 resected thyroid nodules. (2019)
Acknowledgements
This study was approved by the University and the Hospital institutional review board.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zurikat, R.O., Khader, M., Azzam, M.I. et al. Noninvasive follicular neoplasm with papillary-like nuclear features (NIFTP): a 13-year retrospective review at Jordan University Hospital. Endocrine 69, 339–346 (2020). https://doi.org/10.1007/s12020-020-02299-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12020-020-02299-0