Annals of Surgical Oncology

, Volume 21, Issue 6, pp 1870–1877 | Cite as

Clinical Outcomes in Patients with Non-Diagnostic Thyroid Fine Needle Aspiration Cytology: Usefulness of the Thyroid Core Needle Biopsy

  • Sung Hak Lee
  • Min Hee Kim
  • Ja Seong Bae
  • Dong Jun Lim
  • So Lyung Jung
  • Chan Kwon Jung
Endocrine Tumors

Abstract

Background

Patients with non-diagnostic thyroid fine needle aspiration cytology (FNAC) results undergo repeat FNAC or core needle biopsy (CNB) for definite diagnosis or surgical resection, or are followed up by clinical and ultrasound surveillance. We aimed at evaluating the risk of malignancy in patients with non-diagnostic FNACs and their clinical outcomes according to the follow-up modality.

Methods

We retrospectively reviewed 1,496 (8.8 %) cases with a non-diagnostic result on a first aspiration among 17,045 thyroid FNACs performed between October 2008 and August 2012. Of the non-diagnostic FNACs, 389 patients underwent a second FNAC; 125, CNB; and 89, thyroidectomy by clinical indication. The remaining patients were clinically followed up.

Results

The rate of a second non-diagnostic result was significantly higher on repeat FNAC than on CNB (33.2 vs. 2.4 %; p < 0.001). There was no significant difference in the malignancy risk among patients initially non-diagnostic, twice non-diagnostic, and thrice or more non-diagnostic, nor did this differ from the rate following CNB. No further malignancy was found in cases with ≥2 non-diagnostic CNBs. The malignancy risk was 51 % in those who underwent thyroidectomy. The sensitivity for detecting malignancy was 65 and 70 % for repeat FNACs and first CNBs, respectively, with no false positives seen in either test.

Conclusions

Approximately one-third of repeat FNACs after an initial non-diagnostic aspirate are non-diagnostic on repeat examination, and the malignancy risk may not reduce following repetitively non-diagnostic FNACs. However, a single CNB may be enough to exclude malignancy risk for patients with a non-diagnostic aspirate.

References

  1. 1.
    Cooper DS, Doherty GM, Haugen BR, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167–214.PubMedCrossRefGoogle Scholar
  2. 2.
    Cibas ES, Ali SZ. The Bethesda System for reporting thyroid cytopathology. Am J Clin Pathol. 2009;132:658–65.PubMedCrossRefGoogle Scholar
  3. 3.
    Yassa L, Cibas ES, Benson CB, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer. 2007;111:508–16.PubMedCrossRefGoogle Scholar
  4. 4.
    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.PubMedGoogle Scholar
  5. 5.
    Bongiovanni M, Spitale A, Faquin WC, Mazzucchelli L, Baloch ZW. The Bethesda System for reporting thyroid cytopathology: a meta-analysis. Acta Cytol. 2012;56:333–9.PubMedCrossRefGoogle Scholar
  6. 6.
    Ali SZ. Thyroid cytopathology: Bethesda and beyond. Acta Cytol. 2011;55:4–12.PubMedCrossRefGoogle Scholar
  7. 7.
    Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytopathology. Thyroid. 2009;19:1159–65.PubMedCrossRefGoogle Scholar
  8. 8.
    Al Maqbali T, Tedla M, Weickert MO, Mehanna H. Malignancy risk analysis in patients with inadequate fine needle aspiration cytology (FNAC) of the thyroid. PLoS One. 2012;7:e49078.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Orija IB, Pineyro M, Biscotti C, Reddy SS, Hamrahian AH. Value of repeating a nondiagnostic thyroid fine-needle aspiration biopsy. Endocr Pract. 2007;13:735–42.PubMedCrossRefGoogle Scholar
  10. 10.
    Alexander EK, Heering JP, Benson CB, Frates MC, Doubilet PM, Cibas ES, et al. Assessment of nondiagnostic ultrasound-guided fine needle aspirations of thyroid nodules. J Clin Endocrinol Metab. 2002;87:4924–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Lo Gerfo P, Colacchio T, Caushaj F, Weber C, Feind C. Comparison of fine-needle and coarse-needle biopsies in evaluating thyroid nodules. Surgery. 1982;92:835–8.PubMedGoogle Scholar
  12. 12.
    Samir AE, Vij A, Seale MK, et al. Ultrasound-guided percutaneous thyroid nodule core biopsy: clinical utility in patients with prior nondiagnostic fine-needle aspirate. Thyroid. 2012;22:461–7.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Screaton NJ, Berman LH, Grant JW. US-guided core-needle biopsy of the thyroid gland. Radiology. 2003;226:827–32.PubMedCrossRefGoogle Scholar
  14. 14.
    Harvey JN, Parker D, De P, Shrimali RK, Otter M. Sonographically guided core biopsy in the assessment of thyroid nodules. J Clin Ultrasound. 2005;33:57–62.PubMedCrossRefGoogle Scholar
  15. 15.
    Renshaw AA, Pinnar N. Comparison of thyroid fine-needle aspiration and core needle biopsy. Am J Clin Pathol. 2007;128:370–4.PubMedCrossRefGoogle Scholar
  16. 16.
    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;22:468–75.PubMedCrossRefGoogle Scholar
  17. 17.
    Khoo TK, Baker CH, Hallanger-Johnson J, et al. Comparison of ultrasound-guided fine-needle aspiration biopsy with core-needle biopsy in the evaluation of thyroid nodules. Endocr Pract. 2008;14:426–31.PubMedCrossRefGoogle Scholar
  18. 18.
    Moon WJ, Baek JH, Jung SL, et al. Ultrasonography and the ultrasound-based management of thyroid nodules: consensus statement and recommendations. Korean J Radiol. 2011;12:1–14.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Lee J, Lee SY, Cha SH, Cho BS, Kang MH, Lee OJ. Fine-needle aspiration of thyroid nodules with macrocalcification. Thyroid. 2013;23(9):1106–12.PubMedCrossRefGoogle Scholar
  20. 20.
    Yeon JS, Baek JH, Lim HK, et al. Thyroid nodules with initially nondiagnostic cytologic results: the role of core-needle biopsy. Radiology. 2013;268:274–80.PubMedCrossRefGoogle Scholar
  21. 21.
    Lim DJ, Kim JY, Baek KH, et al. Natural course of cytologically benign thyroid nodules: observation of ultrasonographic changes. Endocrinol Metab. 2013;28:110–118.CrossRefGoogle Scholar
  22. 22.
    Choi YS, Hong SW, Kwak JY, Moon HJ, Kim EK. Clinical and ultrasonographic findings affecting nondiagnostic results upon the second fine needle aspiration for thyroid nodules. Ann Surg Oncol. 2012;19:2304–9.PubMedCrossRefGoogle Scholar
  23. 23.
    Deandrea M, Ragazzoni F, Motta M, et al. Diagnostic value of a cytomorphological subclassification of follicular patterned thyroid lesions: a study of 927 consecutive cases with histological correlation. Thyroid. 2010;20:1077–83.PubMedCrossRefGoogle Scholar
  24. 24.
    Hryhorczuk AL, Stephens T, Bude RO, et al. Prevalence of malignancy in thyroid nodules with an initial nondiagnostic result after ultrasound guided fine needle aspiration. Ultrasound Med Biol. 2012;38:561–7.PubMedCrossRefGoogle Scholar
  25. 25.
    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;134:450–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Jo VY, Vanderlaan PA, Marqusee E, Krane JF. Repeatedly nondiagnostic thyroid fine-needle aspirations do not modify malignancy risk. Acta Cytol. 2011;55:539–43.PubMedCrossRefGoogle Scholar
  27. 27.
    Kim SK, Hwang TS, Yoo YB, et al. Surgical results of thyroid nodules according to a management guideline based on the BRAF (V600E) mutation status. J Clin Endocrinol Metab. 2011;96:658–64.PubMedCrossRefGoogle Scholar
  28. 28.
    Renshaw AA. Sensitivity of fine-needle aspiration for papillary carcinoma of the thyroid correlates with tumor size. Diagn Cytopathol. 2011;39:471–4.PubMedCrossRefGoogle Scholar
  29. 29.
    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; 9:1215–23.CrossRefGoogle Scholar
  30. 30.
    Wu HH, Rose C, Elsheikh TM. The Bethesda system for reporting thyroid cytopathology: An experience of 1,382 cases in a community practice setting with the implication for risk of neoplasm and risk of malignancy. Diagn Cytopathol. 2012;40:399–403.PubMedCrossRefGoogle Scholar
  31. 31.
    Yoon JH, Kwak JY, Kim EK, et al. How to approach thyroid nodules with indeterminate cytology. Ann Surg Oncol. 2010;17:2147–55.PubMedCrossRefGoogle Scholar
  32. 32.
    Grani G, Calvanese A, Carbotta G, et al. Intrinsic factors affecting adequacy of thyroid nodule fine-needle aspiration cytology. Clin Endocrinol (Oxf). 2013;78:141–4.CrossRefGoogle Scholar
  33. 33.
    Gharib H. Fine-needle aspiration biopsy of thyroid nodules: advantages, limitations, and effect. Mayo Clin Proc. 1994;69:44–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Degirmenci B, Haktanir A, Albayrak R, et al. Sonographically guided fine-needle biopsy of thyroid nodules: the effects of nodule characteristics, sampling technique, and needle size on the adequacy of cytological material. Clin Radiol. 2007;62:798–803.PubMedCrossRefGoogle Scholar
  35. 35.
    Chow LS, Gharib H, Goellner JR, van Heerden JA. Nondiagnostic thyroid fine-needle aspiration cytology: management dilemmas. Thyroid. 2001;11:1147–51.PubMedCrossRefGoogle Scholar
  36. 36.
    Cappelli C, Pirola I, Castellano M, et al. Fine needle cytology of complex thyroid nodules. Eur J Endocrinol. 2007;157:529–32.PubMedCrossRefGoogle Scholar
  37. 37.
    Redman R, Zalaznick H, Mazzaferri EL, Massoll NA. The impact of assessing specimen adequacy and number of needle passes for fine-needle aspiration biopsy of thyroid nodules. Thyroid. 2006;16:55–60.PubMedCrossRefGoogle Scholar
  38. 38.
    Sung JY, Na DG, Kim KS, Yoo H, Lee H, Kim JH, et al. Diagnostic accuracy of fine-needle aspiration versus core-needle biopsy for the diagnosis of thyroid malignancy in a clinical cohort. Eur Radiol. 2012; 22:1564–72.PubMedCrossRefGoogle Scholar
  39. 39.
    Taki S, Kakuda K, Kakuma K, et al. Thyroid nodules: evaluation with US-guided core biopsy with an automated biopsy gun. Radiology. 1997;202:874–7.PubMedGoogle Scholar
  40. 40.
    Polyzos SA, Anastasilakis AD. Clinical complications following thyroid fine-needle biopsy: a systematic review. Clin Endocrinol (Oxf). 2009;71:157–65.CrossRefGoogle Scholar
  41. 41.
    Gharib H, Papini E, Paschke R, 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;33:51–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Oertel YC, Miyahara-Felipe L, Mendoza MG, Yu K. Value of repeated fine needle aspirations of the thyroid: an analysis of over ten thousand FNAs. Thyroid. 2007;17:1061–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Renshaw AA. Should “atypical follicular cells” in thyroid fine-needle aspirates be subclassified? Cancer Cytopathol. 2010;118:186–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Bongiovanni M, Crippa S, Baloch Z, et al. Comparison of 5-tiered and 6-tiered diagnostic systems for the reporting of thyroid cytopathology: a multi-institutional study. Cancer Cytopathol. 2012;120:117–25.PubMedCrossRefGoogle Scholar
  45. 45.
    Bohacek L, Milas M, Mitchell J, Siperstein A, Berber E. Diagnostic accuracy of surgeon-performed ultrasound-guided fine-needle aspiration of thyroid nodules. Ann Surg Oncol. 2012;19:45–51.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2014

Authors and Affiliations

  • Sung Hak Lee
    • 1
  • Min Hee Kim
    • 2
  • Ja Seong Bae
    • 3
  • Dong Jun Lim
    • 2
  • So Lyung Jung
    • 4
  • Chan Kwon Jung
    • 1
  1. 1.Department of Hospital Pathology, College of MedicineThe Catholic University of KoreaSeoulRepublic of Korea
  2. 2.Department of Internal Medicine, College of MedicineThe Catholic University of KoreaSeoulRepublic of Korea
  3. 3.Department of Surgery, College of MedicineThe Catholic University of KoreaSeoulRepublic of Korea
  4. 4.Department of Radiology, College of MedicineThe Catholic University of KoreaSeoulRepublic of Korea

Personalised recommendations