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Endocrine

, Volume 53, Issue 2, pp 489–496 | Cite as

The 5-tiered categorization system for reporting cytology is sufficient for management of patients with thyroid nodules compared to the 6-tiered Bethesda system

  • Jieun Koh
  • Hee Jung MoonEmail author
  • Eun-Kyung Kim
  • Jin Young Kwak
  • Jung Hyun Yoon
Original Article

Abstract

To analyze whether the 5-tiered categorization system without the atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS) category is sufficient compared to the 6-tiered Bethesda system. This IRB-approved retrospective study was waived informed consent. The pre-Bethesda period was from March 2008 to December 2008 and the Bethesda period was from January 2012 to January 2013. Of 4677 nodules ≥10 mm with initial ultrasonography-guided fine-needle aspiration, 2553 nodules were from the pre-Bethesda period and 1754 nodules were from the Bethesda period. The utilization and malignancy rates of each category were compared between the two periods. The utilization rate of the benign category decreased from 67.7 % in the pre-Bethesda period to 60.0 % in the Bethesda period (p = 0.001). In the pre-Bethesda period, the malignancy rates of the non-diagnostic, benign, suspicious follicular neoplasm/Hürthle cell neoplasm, suspicious for malignancy, and malignancy categories were 3.8, 1.9, 25, 78.8, and 99.7 %, respectively. The malignancy rate of the benign category decreased from 1.9 to 0.3 % after the Bethesda system (p < 0.001). The utilization and malignancy rates of the AUS/FLUS category were 7 and 22.8 %. When the AUS/FLUS category was included in the benign category, the malignancy rate became 2.6 % which was not significantly different from 1.9 % in the pre-Bethesda period (p = 0.189). The malignancy rates of other categories were not significantly different. The 5-tiered categorization system without the AUS/FLUS category for reporting cytology was sufficient for management of patients with thyroid nodules compared to the 6-tiered categorization of the Bethesda system.

Keywords

Thyroid nodule Fine-needle aspiration Cytology Report 

Notes

Compliance with ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical approval

For this type of study formal consent is not required.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Informed consent

The Institutional Review Board approved this retrospective study and waived the requirement for informed consent.

References

  1. 1.
    R. Nayar, M. Ivanovic, The indeterminate thyroid fine-needle aspiration experience from an academic center using terminology similar to that proposed in the 2007 National Cancer Institute Thyroid Fine Needle Aspiration State of the Science Conference. Cancer Cytopathol. 117(3), 195–202 (2009)CrossRefGoogle Scholar
  2. 2.
    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 Cytopathol. 111(5), 306–315 (2007)CrossRefGoogle Scholar
  3. 3.
    A. Crowe, A. Linder, O. Hameed, C. Salih, J. Roberson, J. Gidley, I.A. Eltoum, The impact of implementation of the Bethesda system for reporting thyroid cytopathology on the quality of reporting, “risk” of malignancy, surgical rate, and rate of frozen sections requested for thyroid lesions. Cancer Cytopathol. 119(5), 315–321 (2011)CrossRefPubMedGoogle Scholar
  4. 4.
    K.J. Brister, R.S. Singh, H.H. Wang, Reporting thyroid FNA before and after implementation of the Bethesda system-one institution’s experience. Diagn. Cytopathol. 43(1), 28–31 (2015)CrossRefPubMedGoogle Scholar
  5. 5.
    A.M. Harvey, D.R. Mody, M. Amrikachi, Thyroid fine-needle aspiration reporting rates and outcomes before and after Bethesda implementation within a combined academic and community hospital system. Arch. Pathol. Lab. Med. 137(11), 1664–1668 (2013)CrossRefPubMedGoogle Scholar
  6. 6.
    C.M. Kiernan, J.T. Broome, C.C. Solorzano, The Bethesda system for reporting thyroid cytopathology: a single-center experience over 5 years. Ann. Surg. Oncol. 21(11), 3522–3527 (2014)CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    J.L. Rabaglia, W. Kabbani, L. Wallace, S. Holt, L. Watumull, J. Pruitt, W.H. Snyder, F.E. Nwariaku, Effect of the Bethesda system for reporting thyroid cytopathology on thyroidectomy rates and malignancy risk in cytologically indeterminate lesions. Surgery 148(6), 1267–1272 (2010)CrossRefPubMedGoogle Scholar
  8. 8.
    B.K. Richmond, B.A. O’Brien, W. Mangano, S. Thompson, S. Kemper, The impact of implementation of the Bethesda system for reporting thyroid cytopathology on the surgical treatment of thyroid nodules. Am. Surg. 78(6), 706–710 (2012)PubMedGoogle Scholar
  9. 9.
    J.Y. Song, Y.C. Chu, L. Kim, I.S. Park, J.Y. Han, J.M. Kim, Reclassifying formerly indeterminate thyroid FNAs using the Bethesda system reduces the number of inconclusive cases. Acta Cytol. 56(2), 122–129 (2012)CrossRefPubMedGoogle Scholar
  10. 10.
    C. Theoharis, A.J. Adeniran, S. Roman, J. Ann Sosa, D. Chhieng, The impact of implementing the Bethesda system for reporting of thyroid FNA at an academic center. Diagn. Cytopathol. 41(10), 858–863 (2013)PubMedGoogle Scholar
  11. 11.
    J.T. Broome, C.C. Solorzano, The impact of atypia/follicular lesion of undetermined significance on the rate of malignancy in thyroid fine-needle aspiration: evaluation of the Bethesda system for reporting thyroid cytopathology. Surgery 150(6), 1234–1239 (2011)CrossRefPubMedGoogle Scholar
  12. 12.
    E.S. Cibas, S.Z. Ali, The Bethesda system for reporting thyroid cytopathology. Thyroid 19(11), 1159–1165 (2009)CrossRefPubMedGoogle Scholar
  13. 13.
    A.A. Renshaw, J.F. Krane, Can changing the terminology for benign aspirates reduce the atypia of undetermined significance/follicular lesion of undetermined significance rate in thyroid fine-needle aspirates? Cancer Cytopathol. 121(4), 175–178 (2013)CrossRefPubMedGoogle Scholar
  14. 14.
    I. Kholova, M. Ludvikova, Thyroid atypia of undetermined significance or follicular lesion of undetermined significance: an indispensable bethesda 2010 diagnostic category or waste garbage? Acta Cytol. 58(4), 319–329 (2014)CrossRefPubMedGoogle Scholar
  15. 15.
    K.C. Suen, F.W. AbdulKarim, D.B. Kaminsky, L.J. Layfield, T.R. Miller, S.E. Spires, D.E. Stanley, C.W.M. Bedrossian, M.B. Cohen, W.J. Frable, T.S. Kline, V.A. LiVolsi, G.K. Nguyen, C.N. Powers, J.F. Silverman, M.W. Stanley, T.A. Thomson, Guidelines of the Papanicolaou Society of Cytopathology for fine-needle aspiration procedure and reporting. Diagn. Cytopathol. 17(4), 239–247 (1997)CrossRefGoogle Scholar
  16. 16.
    B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid. (2015). doi:  10.1089/thy.2015.0020 PubMedCentralGoogle Scholar
  17. 17.
    J.Y. Kwak, E.K. Kim, J.K. Kim, J.H. Han, S.W. Hong, T.S. Park, J.R. Choi, Dual priming oligonucleotide-based multiplex PCR analysis for detection of BRAFV600E mutation in FNAB samples of thyroid nodules in BRAFV600E mutation-prevalent area. Head Neck 32(4), 490–498 (2010)PubMedGoogle Scholar
  18. 18.
    J.Y. Kwak, K.H. Han, J.H. Yoon, H.J. Moon, E.J. Son, S.H. Park, H.K. Jung, J.S. Choi, B.M. Kim, E.K. Kim, Thyroid imaging reporting and data system for US features of nodules: a step in establishing better stratification of cancer risk. Radiology 260(3), 892–899 (2011)CrossRefPubMedGoogle Scholar
  19. 19.
    S.H. Choi, K.H. Han, J.H. Yoon, H.J. Moon, E.J. Son, J.H. Youk, E.K. Kim, J.Y. Kwak, Factors affecting inadequate sampling of ultrasound-guided fine-needle aspiration biopsy of thyroid nodules. Clin. Endocrinol. 74(6), 776–782 (2011)CrossRefGoogle Scholar
  20. 20.
    S.Y. Ko, H.S. Lee, E.K. Kim, J.Y. Kwak, Application of the thyroid imaging reporting and data system in thyroid ultrasonography interpretation by less experienced physicians. Ultrasonography 33(1), 49–57 (2014)CrossRefPubMedGoogle Scholar
  21. 21.
    H.J. Moon, J.Y. Kwak, E.K. Kim, J.R. Choi, S.W. Hong, M.J. Kim, E.J. Son, The role of BRAFV600E mutation and ultrasonography for the surgical management of a thyroid nodule suspicious for papillary thyroid carcinoma on cytology. Ann. Surg. Oncol. 16(11), 3125–3131 (2009)CrossRefPubMedGoogle Scholar
  22. 22.
    H.J. Moon, E.K. Kim, W.Y. Chung, J.R. Choi, J.H. Yoon, J.Y. Kwak, Diagnostic value of BRAF(V600E) mutation analysis of thyroid nodules according to ultrasonographic features and the time of aspiration. Ann. Surg. Oncol. 18(3), 792–799 (2011)CrossRefPubMedGoogle Scholar
  23. 23.
    H.J. Moon, J.Y. Kwak, E.K. Kim, M.J. Kim, A taller-than-wide shape in thyroid nodules in transverse and longitudinal ultrasonographic planes and the prediction of malignancy. Thyroid 21(11), 1249–1253 (2011)CrossRefPubMedGoogle Scholar
  24. 24.
    E.K. Kim, C.S. Park, W.Y. Chung, K.K. Oh, D.I. Kim, J.T. Lee, H.S. Yoo, New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am. J. Roentgenol. 178(3), 687–691 (2002)CrossRefPubMedGoogle Scholar
  25. 25.
    H.J. Moon, J.Y. Kwak, M.J. Kim, E.J. Son, E.K. Kim, Can vascularity at power Doppler US help predict thyroid malignancy? Radiology 255(1), 260–269 (2010)CrossRefPubMedGoogle Scholar
  26. 26.
    J.Y. Kwak, E.K. Kim, H.J. Kim, M.J. Kim, E.J. Son, H.J. Moon, How to combine ultrasound and cytological information in decision making about thyroid nodules. Eur. Radiol. 19(8), 1923–1931 (2009)CrossRefPubMedGoogle Scholar
  27. 27.
    A.A. Renshaw, E.W. Gould, Reducing indeterminate thyroid FNAs. Cancer Cytopathol. 123(4), 237–243 (2015)CrossRefPubMedGoogle Scholar
  28. 28.
    Y. Shi, X. Ding, M. Klein, C. Sugrue, S. Matano, M. Edelman, P. Wasserman, Thyroid fine-needle aspiration with atypia of undetermined significance: a necessary or optional category? Cancer 117(5), 298–304 (2009)PubMedGoogle Scholar
  29. 29.
    M. Bongiovanni, J.F. Krane, E.S. Cibas, W.C. Faquin, The atypical thyroid fine-needle aspiration: past, present, and future. Cancer Cytopathol. 120(2), 73–86 (2012)CrossRefPubMedGoogle Scholar
  30. 30.
    P.A. VanderLaan, A.A. Renshaw, J.F. Krane, Atypia of undetermined significance and nondiagnostic rates in the Bethesda System for reporting thyroid cytopathology are inversely related. Am. J. Clin. Pathol. 137(3), 462–465 (2012)CrossRefPubMedGoogle Scholar
  31. 31.
    J.H. Yoon, H.S. Lee, E.K. Kim, H.J. Moon, J.Y. Kwak, Thyroid nodules: nondiagnostic cytologic results according to thyroid imaging reporting and data system before and after application of the Bethesda System. Radiology 276(2), 579–587 (2015)CrossRefPubMedGoogle Scholar
  32. 32.
    A.A. Renshaw, E.W. Gould, Why there is the tendency to “overdiagnose” the follicular variant of papillary thyroid carcinoma. Am. J. Clin. Pathol. 117(1), 19–21 (2002)CrossRefPubMedGoogle Scholar
  33. 33.
    P. Straccia, E.D. Rossi, T. Bizzarro, C. Brunelli, F. Cianfrini, D. Damiani, G. Fadda, 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 (2015)CrossRefPubMedGoogle Scholar
  34. 34.
    A.S. Ho, E.E. Sarti, K.S. Jain, H. Wang, I.J. Nixon, A.R. Shaha, J.P. Shah, D.H. Kraus, R. Ghossein, S.A. Fish, R.J. Wong, O. Lin, L.G.T. Morris, Malignancy rate in thyroid nodules classified as Bethesda Category III (AUS/FLUS). Thyroid 24(5), 832–839 (2014)CrossRefPubMedGoogle Scholar
  35. 35.
    P.W. Rosario, Thyroid nodules with atypia or follicular lesions of undetermined significance (Bethesda Category III): importance of ultrasonography and cytological subcategory. Thyroid 24(7), 1115–1120 (2014)CrossRefPubMedGoogle Scholar
  36. 36.
    P.A. VanderLaan, E. Marqusee, J.F. Krane, Clinical outcome for atypia of undetermined significance in thyroid fine-needle aspirations should repeated FNA be the preferred initial approach? Am. J. Clin. Pathol. 135(5), 770–775 (2011)CrossRefPubMedGoogle Scholar
  37. 37.
    P.S. Sullivan, S.L. Hirschowitz, P.C. Fung, S.K. Apple, The impact of atypia/follicular lesion of undetermined significance and repeat fine-needle aspiration: 5 years before and after implementation of the Bethesda system. Cancer Cytopathol. 122(12), 866–872 (2014)CrossRefPubMedGoogle Scholar
  38. 38.
    V.Y. Park, E.K. Kim, J.Y. Kwak, J.H. Yoon, H.J. Moon, Malignancy risk and characteristics of thyroid nodules with two consecutive results of atypia of undetermined significance or follicular lesion of undetermined significance on cytology. Eur. Radiol. 25(9), 2601–2607 (2015)CrossRefPubMedGoogle Scholar
  39. 39.
    S. Bose, A.E. Walts, Thyroid fine needle aspirate: a post-Bethesda update. Adv. Anat. Pathol. 19(3), 160–169 (2012)CrossRefPubMedGoogle Scholar
  40. 40.
    A.M. Marchevsky, A.E. Walts, S. Bose, R. Gupta, X. Fan, D. Frishberg, K. Scharre, J. Zhai, Evidence-based evaluation of the risks of malignancy predicted by thyroid fine-needle aspiration biopsies. Diagn. Cytopathol. 38(4), 252–259 (2010)PubMedGoogle Scholar
  41. 41.
    R.S. Singh, H.H. Wang, Eliminating the “atypia of undetermined significance/follicular lesion of undetermined significance” category from the bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 136(6), 896–902 (2011)CrossRefPubMedGoogle Scholar
  42. 42.
    A.E. Walts, S. Bose, X. Fan, D. Frishberg, K. Scharre, M. de Peralta-Venturina, J. Zhai, A.M. Marchevsky, A simplified Bethesda system for reporting thyroid cytopathology using only four categories improves intra- and inter-observer diagnostic agreement and provides non-overlapping estimates of malignancy risks. Diagn. Cytopathol. 40, E62–E68 (2012)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Jieun Koh
    • 1
  • Hee Jung Moon
    • 1
    Email author
  • Eun-Kyung Kim
    • 1
  • Jin Young Kwak
    • 1
  • Jung Hyun Yoon
    • 1
  1. 1.Department of Radiology and Research Institute of Radiological Science, Severance HospitalYonsei University College of MedicineSeoulRepublic of Korea

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