Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Comparison of Core Needle Biopsy and Repeat Fine-Needle Aspiration in Avoiding Diagnostic Surgery for Thyroid Nodules Initially Diagnosed as Atypia/Follicular Lesion of Undetermined Significance

  • Leehi Joo (Department of Radiology, Korea University Guro Hospital) ;
  • Dong Gyu Na (Department of Radiology, GangNeung Asan Hospital, University of Ulsan College of Medicine) ;
  • Ji-hoon Kim (Department of Radiology, Seoul National University College of Medicine) ;
  • Hyobin Seo (Department of Radiology, Human Medical Imaging and Intervention Center)
  • Received : 2021.08.04
  • Accepted : 2021.10.14
  • Published : 2022.02.01
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Abstract

Objective: To compare core needle biopsy (CNB) and repeat fine-needle aspiration (rFNA) to reduce the rate of diagnostic surgery and prevent unnecessary surgery in nodules initially diagnosed as atypia/follicular lesions of undetermined significance (AUS/FLUS). Materials and Methods: This study included 231 consecutive patients (150 female and 81 male; mean age ± standard deviation, 51.9 ± 11.7 years) with 235 thyroid nodules (≥ 1 cm) initially diagnosed as AUS/FLUS, who later underwent both rFNA and CNB. The nodules that required diagnostic surgery after the biopsy were defined using three different scenarios according to the rFNA and CNB results: criterion 1, surgery for low-risk indeterminate (categories I and III); criterion 2, surgery for high-risk indeterminate (categories IV and V); and criterion 3, surgery for all indeterminate nodules (categories I, III, IV, and V). We compared the expected rates of diagnostic surgery between CNB and rFNA in all 235 nodules using the three surgical criteria. In addition, the expected rates of unnecessary surgery (i.e., surgery for benign pathology) were compared in a subgroup of 182 nodules with available final diagnoses. Results: CNB showed significantly lower rates of nondiagnostic, AUS/FLUS, and suspicious for malignancy diagnoses (p ≤ 0.016) and higher rates of follicular neoplasm or suspicious for a follicular neoplasm (p < 0.001) and malignant diagnoses (p = 0.031). CNB showed a significantly lower expected rate of diagnostic surgery than rFNA for criterion 1 (29.8% vs. 48.1%, p < 0.001) and criterion 3 (46.4% vs. 55.3%, p = 0.029), and a significantly higher rate for criterion 2 (16.6% vs. 7.2%, p = 0.001). CNB showed a significantly lower expected rate of unnecessary surgery than rFNA for criterion 1 (18.7% vs. 29.7%, p = 0.024). Conclusion: CNB was superior to rFNA in reducing the rates of potential diagnostic surgery and unnecessary surgery for nodules initially diagnosed as AUS/FLUS in a scenario where nodules with low-risk indeterminate results (categories I and III) would undergo surgery.

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References

  1. Ha EJ, Lim HK, Yoon JH, Baek JH, Do KH, Choi M, et al. Primary imaging test and appropriate biopsy methods for thyroid nodules: guidelines by Korean Society of Radiology and National Evidence-Based Healthcare Collaborating Agency. Korean J Radiol 2018;19:623-631
  2. Bongiovanni M, Spitale A, Faquin WC, Mazzucchelli L, Baloch ZW. The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol 2012;56:333-339
  3. Nayar R, Ivanovic M. 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 2009;117:195-202
  4. Theoharis CG, Schofield KM, Hammers L, Udelsman R, Chhieng DC. The Bethesda thyroid fine-needle aspiration classification system: year 1 at an academic institution. Thyroid 2009;19:1215-1223
  5. Ohori NP, Nikiforova MN, Schoedel KE, LeBeau SO, Hodak SP, Seethala RR, et al. Contribution of molecular testing to thyroid fine-needle aspiration cytology of "follicular lesion of undetermined significance/atypia of undetermined significance". Cancer Cytopathol 2010;118:17-23
  6. Renshaw AA. Should "atypical follicular cells" in thyroid fine-needle aspirates be subclassified? Cancer Cytopathol 2010;118:186-189
  7. Jo VY, Stelow EB, Dustin SM, Hanley KZ. Malignancy risk for fine-needle aspiration of thyroid lesions according to the Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 2010;134:450-456
  8. Rabaglia JL, Kabbani W, Wallace L, Holt S, Watumull L, Pruitt J, et al. Effect of the Bethesda system for reporting thyroid cytopathology on thyroidectomy rates and malignancy risk in cytologically indeterminate lesions. Surgery 2010;148:1267-1272; discussion 1272-1273
  9. VanderLaan PA, Marqusee E, Krane JF. Clinical outcome for atypia of undetermined significance in thyroid fine-needle aspirations: should repeated fna be the preferred initial approach? Am J Clin Pathol 2011;135:770-775
  10. Vanderlaan PA, Krane JF, Cibas ES. The frequency of 'atypia of undetermined significance' interpretations for thyroid fine-needle aspirations is negatively correlated with histologically proven malignant outcomes. Acta Cytol 2011;55:512-517
  11. Padmanabhan V, Marshall CB, Akdas Barkan G, Ghofrani M, Laser A, Tolgay Ocal I, et al. Reproducibility of atypia of undetermined significance/follicular lesion of undetermined significance category using the bethesda system for reporting thyroid cytology when reviewing slides from different institutions: a study of interobserver variability among cytopathologists. Diagn Cytopathol 2017;45:399-405
  12. Cibas ES, Ali SZ. The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid 2017;27:1341-1346
  13. Gharib H, Papini E, Paschke R, Duick DS, Valcavi R, Hegedus L, et al. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules: executive summary of recommendations. J Endocrinol Invest 2010;33:51-56
  14. Perros P, Boelaert K, Colley S, Evans C, Evans RM, Gerrard Ba G, et al. Guidelines for the management of thyroid cancer. Clin Endocrinol (Oxf) 2014;81 Suppl 1:1-122
  15. 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 2015;26:1-133
  16. Shin JH, Baek JH, Chung J, Ha EJ, Kim JH, Lee YH, et al. Ultrasonography diagnosis and imaging-based management of thyroid nodules: revised Korean Society of Thyroid Radiology consensus statement and recommendations. Korean J Radiol 2016;17:370-395
  17. Faquin WC, Baloch ZW. Fine-needle aspiration of follicular patterned lesions of the thyroid: diagnosis, management, and follow-up according to National Cancer Institute (NCI) recommendations. Diagn Cytopathol 2010;38:731-739
  18. Na DG, Kim JH, Sung JY, Baek JH, Jung KC, Lee H, et al. 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 2012;22:468-475
  19. Ho AS, Sarti EE, Jain KS, Wang H, Nixon IJ, Shaha AR, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid 2014;24:832-839
  20. Hyeon J, Ahn S, Shin JH, Oh YL. The prediction of malignant risk in the category "atypia of undetermined significance/ follicular lesion of undetermined significance" of the Bethesda system for reporting thyroid cytopathology using subcategorization and BRAF mutation results. Cancer Cytopathol 2014;122:368-376
  21. Sullivan PS, Hirschowitz SL, Fung PC, Apple SK. 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 2014;122:866-872
  22. Choi YJ, Baek JH, Suh CH, Shim WH, Jeong B, Kim JK, et al. Core-needle biopsy versus repeat fine-needle aspiration for thyroid nodules initially read as atypia/follicular lesion of undetermined significance. Head Neck 2017;39:361-369
  23. Hong SH, Lee H, Cho MS, Lee JE, Sung YA, Hong YS. Malignancy risk and related factors of atypia of undetermined significance/follicular lesion of undetermined significance in thyroid fine needle aspiration. Int J Endocrinol 2018;2018:4521984
  24. Evranos Ogmen B, Aydin C, Kilinc I, Aksoy Altinboga A, Ersoy R, Cakir B. Can repeat biopsies change the prognoses of AUS/ FLUS nodule? Eur Thyroid J 2020;9:92-98
  25. Na DG, Min HS, Lee H, Won JK, Seo HB, Kim JH. Role of core needle biopsy in the management of atypia/follicular lesion of undetermined significance thyroid nodules: comparison with repeat fine-needle aspiration in subcategory nodules. Eur Thyroid J 2015;4:189-196
  26. Lee KH, Shin JH, Oh YL, Hahn SY. Atypia of undetermined significance in thyroid fine-needle aspiration cytology: prediction of malignancy by US and comparison of methods for further management. Ann Surg Oncol 2014;21:2326-2331
  27. Pyo JS, Sohn JH, Kang G. Core needle biopsy is a more conclusive follow-up method than repeat fine needle aspiration for thyroid nodules with initially inconclusive results: a systematic review and meta-analysis. J Pathol Transl Med 2016;50:217-224
  28. Jung SM, Koo HR, Jang KS, Chung MS, Song CM, Ji YB, et al. Comparison of core-needle biopsy and repeat fine-needle aspiration for thyroid nodules with inconclusive initial cytology. Eur Arch Otorhinolaryngol 2021;278:3019-3025
  29. Yoon JH, Kwak JY, Moon HJ, Kim EK. Ultrasonography-guided core needle biopsy did not reduce diagnostic lobectomy for thyroid nodules diagnosed as atypia of undetermined significance/follicular lesion of undetermined significance. Ultrasound Q 2019;35:253-258
  30. Na DG, Baek JH, Jung SL, Kim JH, Sung JY, Kim KS, et al. Core needle biopsy of the thyroid: 2016 consensus statement and recommendations from Korean Society of Thyroid Radiology. Korean J Radiol 2017;18:217-237
  31. Jung CK, Baek JH, Na DG, Oh YL, Yi KH, Kang HC. 2019 Practice guidelines for thyroid core needle biopsy: a report of the Clinical Practice Guidelines Development Committee of the Korean Thyroid Association. J Pathol Transl Med 2020;54:64-86
  32. Ha EJ, Suh CH, Baek JH. Complications following ultrasound-guided core needle biopsy of thyroid nodules: a systematic review and meta-analysis. Eur Radiol 2018;28:3848-3860
  33. Hong MJ, Na DG, Lee H. Diagnostic efficacy and safety of core needle biopsy as a first-line diagnostic method for thyroid nodules: a prospective cohort study. Thyroid 2020;30:1141-1149
  34. Polyzos SA, Anastasilakis AD. Clinical complications following thyroid fine-needle biopsy: a systematic review. Clin Endocrinol (Oxf) 2009;71:157-165
  35. Nikiforova MN, Mercurio S, Wald AI, Barbi de Moura M, Callenberg K, Santana-Santos L, et al. Analytical performance of the ThyroSeq v3 genomic classifier for cancer diagnosis in thyroid nodules. Cancer 2018;124:1682-1690
  36. Patel KN, Angell TE, Babiarz J, Barth NM, Blevins T, Duh QY, et al. Performance of a genomic sequencing classifier for the preoperative diagnosis of cytologically indeterminate thyroid nodules. JAMA Surg 2018;153:817-824
  37. Kim GR, Yoon JH, Kim EK, Moon HJ, Kwak JY. Benign aspirates on follow-up FNA may be enough in patients with initial atypia of undetermined significance/follicular lesion of undetermined significance. Int J Endocrinol 2014;2014:354612