Skip to main content
SpringerLink
Log in

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

  • Endocrine Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  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.

    Article  PubMed  Google Scholar 

  2. Cibas ES, Ali SZ. The Bethesda System for reporting thyroid cytopathology. Am J Clin Pathol. 2009;132:658–65.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  6. Ali SZ. Thyroid cytopathology: Bethesda and beyond. Acta Cytol. 2011;55:4–12.

    Article  PubMed  Google Scholar 

  7. Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytopathology. Thyroid. 2009;19:1159–65.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Screaton NJ, Berman LH, Grant JW. US-guided core-needle biopsy of the thyroid gland. Radiology. 2003;226:827–32.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  15. Renshaw AA, Pinnar N. Comparison of thyroid fine-needle aspiration and core needle biopsy. Am J Clin Pathol. 2007;128:370–4.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  28. Renshaw AA. Sensitivity of fine-needle aspiration for papillary carcinoma of the thyroid correlates with tumor size. Diagn Cytopathol. 2011;39:471–4.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  31. Yoon JH, Kwak JY, Kim EK, et al. How to approach thyroid nodules with indeterminate cytology. Ann Surg Oncol. 2010;17:2147–55.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  33. Gharib H. Fine-needle aspiration biopsy of thyroid nodules: advantages, limitations, and effect. Mayo Clin Proc. 1994;69:44–9.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  35. Chow LS, Gharib H, Goellner JR, van Heerden JA. Nondiagnostic thyroid fine-needle aspiration cytology: management dilemmas. Thyroid. 2001;11:1147–51.

    Article  CAS  PubMed  Google Scholar 

  36. Cappelli C, Pirola I, Castellano M, et al. Fine needle cytology of complex thyroid nodules. Eur J Endocrinol. 2007;157:529–32.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  40. Polyzos SA, Anastasilakis AD. Clinical complications following thyroid fine-needle biopsy: a systematic review. Clin Endocrinol (Oxf). 2009;71:157–65.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  43. Renshaw AA. Should “atypical follicular cells” in thyroid fine-needle aspirates be subclassified? Cancer Cytopathol. 2010;118:186–9.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

The authors wish to acknowledge the financial support of the Catholic Medical Center Research Foundation made in the program year of 2013.

Disclosures

None.

Author information

Authors and Affiliations

  1. Department of Hospital Pathology, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    Sung Hak Lee MD, PhD & Chan Kwon Jung MD, PhD

  2. Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    Min Hee Kim MD & Dong Jun Lim MD, PhD

  3. Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    Ja Seong Bae MD, PhD

  4. Department of Radiology, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea

    So Lyung Jung MD, PhD

Authors
  1. Sung Hak Lee MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Min Hee Kim MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ja Seong Bae MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Jun Lim MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. So Lyung Jung MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chan Kwon Jung MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chan Kwon Jung MD, PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, S.H., Kim, M.H., Bae, J.S. et al. Clinical Outcomes in Patients with Non-Diagnostic Thyroid Fine Needle Aspiration Cytology: Usefulness of the Thyroid Core Needle Biopsy. Ann Surg Oncol 21, 1870–1877 (2014). https://doi.org/10.1245/s10434-013-3365-z

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-013-3365-z

Keywords

Search

Navigation