Annals of Surgical Oncology

, Volume 21, Issue 6, pp 1898–1903 | Cite as

Malignancy Risk Stratification in Thyroid Nodules with Benign Results on Cytology: Combination of Thyroid Imaging Reporting and Data System and Bethesda System

  • Hee Jung Moon
  • Eun-Kyung Kim
  • Jin Young KwakEmail author
Head and Neck Oncology



The indications of repeat fine-needle aspiration (FNA) for thyroid nodules with benign results of the Bethesda system were investigated.


A total of 1,398 nodules were classified according to the Thyroid Imaging Reporting and Data System (TIRADS). TIRADS category 3 included nodules without solidity, hypoechogenicity or marked hypoechogenicity, microlobulated or irregular margins, microcalcifications, and taller-than-wide shape on ultrasonography (US). Categories 4a, 4b, 4c, and 5 included nodules with one, two, three or four, or five suspicious US features, respectively. The malignancy risks, and odds ratio (OR) with 95 % confidence interval (CI) were calculated. Analyses were performed for all nodules, nodules >10 mm, and nodules ≤10 mm.


Of 1.398 nodules, 43 (3.1 %) were malignanct. The malignancy risks of benign nodules with categories 3, 4a, and 4b were 0.7, 1.2, and 0.7 %, respectively, whereas those for nodules with categories 4c and 5 were 9.8 and 22.2 %, respectively. The ORs of nodules with categories 4c and 5 were 19.4 (95 % CI 5.0–76.2) and 50.6 (95 % CI 10.4–245.0), respectively. In nodules >10 mm, the malignancy risks of categories 4c and 5 were 2.7 and 20 %, respectively, and the ORs were 10.7 (95 % CI 1.2–93.7) and 236.1 (95 % CI 12.6–4426.4), respectively. In nodules ≤ 10 mm, the malignancy risks of categories 4c and 5 were 12.6 and 22.6 %, respectively, and the ORs were 10.1 (95 % CI 1.3–78.0) and 18.9 (95 % CI 2.1–168.9), respectively.


Repeat US-guided FNA should be considered in benign thyroid nodules with three or more suspicious US features regardless of size.


Thyroid Nodule Nodule Size Benign Nodule Irregular Margin Malignancy Risk 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was supported by a faculty research grant of Yonsei University College of Medicine for 2013 (6-2013-0074).


  1. 1.
    Danese D, Sciacchitano S, Farsetti A, Andreoli M, Pontecorvi A. Diagnostic accuracy of conventional versus sonography-guided fine-needle aspiration biopsy of thyroid nodules. Thyroid. 1998;8:15–21.PubMedCrossRefGoogle Scholar
  2. 2.
    Gharib H. Fine-needle aspiration biopsy of thyroid nodules: advantages, limitations, and effect. Mayo Clin Proc. 1994;69:44–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Rosen IB, Azadian A, Walfish PG, Salem S, Lansdown E, Bedard YC. Ultrasound-guided fine-needle aspiration biopsy in the management of thyroid disease. Am J Surg. 1993;166:346–9.PubMedCrossRefGoogle Scholar
  4. 4.
    Yokozawa T, Miyauchi A, Kuma K, Sugawara M. Accurate and simple method of diagnosing thyroid nodules the modified technique of ultrasound-guided fine needle aspiration biopsy. Thyroid. 1995;5:141–5.PubMedCrossRefGoogle Scholar
  5. 5.
    Cibas ES, Ali SZ. The Bethesda System for reporting thyroid cytopathology. Am J Clin Pathol. 2009;132:658–65.PubMedCrossRefGoogle Scholar
  6. 6.
    Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167–214.PubMedCrossRefGoogle Scholar
  7. 7.
    Choi YJ, Jung I, Min SJ, Kim HJ, Kim JH, Kim S, et al. Thyroid nodule with benign cytology: is clinical follow-up enough? PLoS One. 2013;8:e63834.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Kwak JY, Kim EK, Kim HJ, Kim MJ, Son EJ, Moon HJ. How to combine ultrasound and cytological information in decision making about thyroid nodules. Eur Radiol. 2009;19:1923–31.PubMedCrossRefGoogle Scholar
  9. 9.
    Kwak JY, Koo H, Youk JH, Kim MJ, Moon HJ, Son EJ, et al. Value of US correlation of a thyroid nodule with initially benign cytologic results. Radiology. 2010;254:292–300.PubMedCrossRefGoogle Scholar
  10. 10.
    Yoon JH, Kwak JY, Kim EK, Moon HJ, Kim MJ, Kim JY, et al. How to approach thyroid nodules with indeterminate cytology. Ann Surg Oncol. 2010;17:2147–55.PubMedCrossRefGoogle Scholar
  11. 11.
    Yoon JH, Moon HJ, Kim EK, Kwak JY. Inadequate cytology in thyroid nodules: should we repeat aspiration or follow-up? Ann Surg Oncol. 2011;18:1282–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Lee SW, Lee HJ, Kim HJ, Lee J, Park JY, Kim SH, et al. Combined categorical reporting systems of US and cytology findings for thyroid nodules: guidance on repeat fine-needle aspiration cytology. Radiology. 2013;266:956–63.PubMedCrossRefGoogle Scholar
  13. 13.
    Blansfield JA, Sack MJ, Kukora JS. Recent experience with preoperative fine-needle aspiration biopsy of thyroid nodules in a community hospital. Arch Surg. 2002;137:818–21.PubMedCrossRefGoogle Scholar
  14. 14.
    Chernyavsky VS, Shanker BA, Davidov T, Crystal JS, Eng O, Ibrahim K, et al. Is one benign fine needle aspiration enough? Ann Surg Oncol. 2012;19:1472–6.PubMedCrossRefGoogle Scholar
  15. 15.
    Shin JH, Han BK, Ko K, Choe YH, Oh YL. Value of repeat ultrasound-guided fine-needle aspiration in nodules with benign cytological diagnosis. Acta Radiol. 2006;47:469–73.PubMedCrossRefGoogle Scholar
  16. 16.
    Horvath E, Majlis S, Rossi R, Franco C, Niedmann JP, Castro A, et al. An ultrasonogram reporting system for thyroid nodules stratifying cancer risk for clinical management. J Clin Endocrinol Metab. 2009;94:1748–51.PubMedCrossRefGoogle Scholar
  17. 17.
    Radiology ACo. Breast imaging reporting and data system, breast imaging atlas. 4th ed. Department of Quality and Safety, American College of Radiology: Reston, 2003.Google Scholar
  18. 18.
    Kwak JY, Han KH, Yoon JH, Moon HJ, Son EJ, Park SH, et al. Thyroid imaging reporting and data system for US features of nodules: a step in establishing better stratification of cancer risk. Radiology. 2011;260:892–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Park JY, Lee HJ, Jang HW, Kim HK, Yi JH, Lee W, et al. A proposal for a thyroid imaging reporting and data system for ultrasound features of thyroid carcinoma. Thyroid. 2009;19:1257–64.PubMedCrossRefGoogle Scholar
  20. 20.
    Moon HJ, Kwak JY, Kim MJ, Son EJ, Kim EK. Can vascularity at power Doppler US help predict thyroid malignancy? Radiology. 2010;255:260–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Moon HJ, Sung JM, Kim EK, Yoon JH, Youk JH, Kwak JY. Diagnostic performance of gray-scale US and elastography in solid thyroid nodules. Radiology. 2012;262:1002–13.PubMedCrossRefGoogle Scholar
  22. 22.
    Gharib H, Papini E, Paschke R, Duick DS, Valcavi R, Hegedüs L, et al. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and EuropeanThyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr Pract. 2010;16 Suppl 1:1–43.PubMedCrossRefGoogle Scholar
  23. 23.
    Kwak JY, Jung I, Baek JH, Baek SM, Choi N, Choi YJ,, et al. Image reporting and characterization system for ultrasound features of thyroid nodules: multicentric korean retrospective study. Korean J Radiol. 2013;14:110–7.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Wang CC, Friedman L, Kennedy GC, Wang H, Kebebew E, Steward DL, et al. A large multicenter correlation study of thyroid nodule cytopathology and histopathology. Thyroid. 2011;21:243–51.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Menendez Torre E, Pineda Arribas J, Martinez de Esteban JP, Lopez Carballo MT, de Miguel C, Salvador P. Value of repeated fine needle aspiration cytology in patients with nodular goiter. Acta Cytol. 2007;51:850–2.PubMedCrossRefGoogle Scholar
  26. 26.
    Orlandi A, Puscar A, Capriata E, Fideleff H. Repeated fine-needle aspiration of the thyroid in benign nodular thyroid disease: critical evaluation of long-term follow-up. Thyroid. 2005;15:274–8.PubMedCrossRefGoogle Scholar
  27. 27.
    Choi SH, Kim EK, Kwak JY, Kim MJ, Son EJ. Interobserver and intraobserver variations in ultrasound assessment of thyroid nodules. Thyroid. 2010;20:167–72.PubMedCrossRefGoogle Scholar
  28. 28.
    Hambly NM, Gonen M, Gerst SR, Li D, Jia X, Mironov S, et al. Implementation of evidence-based guidelines for thyroid nodule biopsy: a model for establishment of practice standards. AJR Am J Roentgenol. 2011;196:655–60.PubMedCrossRefGoogle Scholar
  29. 29.
    Kim GR, Kim MH, Moon HJ, Chung WY, Kwak JY, Kim EK. Sonographic characteristics suggesting papillary thyroid carcinoma according to nodule size. Ann Surg Oncol. 2013;20:906–13.PubMedCrossRefGoogle Scholar
  30. 30.
    Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M,, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353:1784–92.PubMedCrossRefGoogle Scholar
  31. 31.
    Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA. 2006;295:2164–7.PubMedCrossRefGoogle Scholar
  32. 32.
    Baloch Z, LiVolsi VA, Jain P, Jain R, Aljada I, Mandel S, et al. Role of repeat fine-needle aspiration biopsy (FNAB) in the management of thyroid nodules. Diagn Cytopathol. 2003;29:203–6.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2014

Authors and Affiliations

  • Hee Jung Moon
    • 1
  • Eun-Kyung Kim
    • 1
  • Jin Young Kwak
    • 1
    Email author
  1. 1.Department of Radiology, Research Institute of Radiological Science, Severance HospitalYonsei University College of MedicineSeoulKorea

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