J Pathol Transl Med.  2016 May;50(3):217-224. 10.4132/jptm.2016.02.15.

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

• Pyo JS
• Sohn JH
• Kang G

• KMID: 2164599
• DOI: http://doi.org/10.4132/jptm.2016.02.15

Abstract

BACKGROUND
This study investigated the appropriate management of thyroid nodules with prior non-diagnostic or atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS) through a systematic review and meta-analysis.
METHODS
This study included 4,235 thyroid nodules from 26 eligible studies. We investigated the conclusive rate of follow-up core needle biopsy (CNB) or repeat fine needle aspiration (rFNA) after initial fine needle aspiration (FNA) with non-diagnostic or AUS/FLUS results. A diagnostic test accuracy (DTA) review was performed to determine the diagnostic role of the follow-up CNB and to calculate the area under the curve (AUC) on the summary receiver operating characteristic (SROC) curve.
RESULTS
The conclusive rates of follow-up CNB and rFNA after initial FNA were 0.879 (95% confidence interval [CI], 0.801 to 0.929) and 0.684 (95% CI, 0.627 to 0.736), respectively. In comparison of the odds ratios of CNB and rFNA, CNB had more frequent conclusive results than rFNA (odds ratio, 5.707; 95% CI, 2.530 to 12.875). Upon subgroup analysis, follow-up CNB showed a higher conclusive rate than rFNA in both initial non-diagnostic and AUS/FLUS subgroups. In DTA review of followup CNB, the pooled sensitivity and specificity were 0.94 (95% CI, 0.88 to 0.97) and 0.88 (95% CI, 0.84 to 0.91), respectively. The AUC for the SROC curve was 0.981, nearing 1.
CONCLUSIONS
Our results show that CNB has a higher conclusive rate than rFNA when the initial FNA produced inconclusive results. Further prospective studies with more detailed criteria are necessary before follow-up CNB can be applied in daily practice.

Keyword

Thyroid nodule; Non-diagnostic or atypia of undetermined significance/follicular lesion of undetermined significance; Follow-up core needle biopsy; Repeat fine-needle aspiration; Meta-analysis

MeSH Terms

Area Under Curve
Biopsy, Fine-Needle*
Biopsy, Large-Core Needle*
Diagnostic Tests, Routine
Follow-Up Studies*
Methods*
Odds Ratio
Prospective Studies
ROC Curve
Sensitivity and Specificity
Thyroid Gland*
Thyroid Nodule*

Figure

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  Fig. 1. Flow chart of study search and selection methods.

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  Fig. 2. The sensitivity (A) and specificity (B) of follow-up core needle biopsy for prediction of papillary thyroid carcinoma after prior fine needle aspiration with non-diagnostic or atypia/follicular lesion of undetermined significance in thyroid nodules.

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  Fig. 3. The summary receiver operating characteristics (SROC) curve of follow-up core needle biopsy for prediction of papillary thyroid carcinoma after prior fine needle aspiration with non-diagnostic or atypia/follicular lesion of undetermined significance in thyroid nodules. AUC, area under the curve.

Reference

1. Sprague BL, Warren Andersen S, Trentham-Dietz A. Thyroid cancer incidence and socioeconomic indicators of health care access. Cancer Causes Control. 2008; 19:585–93.

2. Enewold L, Zhu K, Ron E, et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980-2005. Cancer Epidemiol Biomarkers Prev. 2009; 18:784–91.

3. Mercante G, Frasoldati A, Pedroni C, et al. Prognostic factors affecting neck lymph node recurrence and distant metastasis in papillary microcarcinoma of the thyroid: results of a study in 445 patients. Thyroid. 2009; 19:707–16.

4. Cibas ES, Ali SZ. The Bethesda System for Reporting Thyroid Cytopathology. Thyroid. 2009; 19:1159–65.

5. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009; 19:1167–214.

6. 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(5 suppl 1):51–6.

7. Yang J, Schnadig V, Logrono R, Wasserman PG. Fine-needle aspiration of thyroid nodules: a study of 4703 patients with histologic and clinical correlations. Cancer. 2007; 111:306–15.

8. 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.

9. 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.

10. 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.

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

12. Zamora J, Abraira V, Muriel A, Khan K, Coomarasamy A. Meta-DiSc: a software for meta-analysis of test accuracy data. BMC Med Res Methodol. 2006; 6:31.

13. Pyo JS, Sohn JH, Kang G. BRAF immunohistochemistry using clone VE1 is strongly soncordant with BRAF(V600E) mutation test in papillary thyroid carcinoma. Endocr Pathol. 2015; 26:211–7.

14. Anderson TJ, Atalay MK, Grand DJ, Baird GL, Cronan JJ, Beland MD. Management of nodules with initially nondiagnostic results of thyroid fine-needle aspiration: can we avoid repeat biopsy? Radiology. 2014; 272:777–84.

15. Baloch Z, LiVolsi VA, Jain P, et al. Role of repeat fine-needle aspiration biopsy (FNAB) in the management of thyroid nodules. Diagn Cytopathol. 2003; 29:203–6.

16. Chen JC, Pace SC, Chen BA, Khiyami A, McHenry CR. Yield of repeat fine-needle aspiration biopsy and rate of malignancy in patients with atypia or follicular lesion of undetermined significance: the impact of the Bethesda System for Reporting Thyroid Cytopathology. Surgery. 2012; 152:1037–44.

17. Choi YJ, Baek JH, Ha EJ, et al. Differences in risk of malignancy and management recommendations in subcategories of thyroid nodules with atypia of undetermined significance or follicular lesion of undetermined significance: the role of ultrasound-guided core-needle biopsy. Thyroid. 2014; 24:494–501.

18. Choi SH, Baek JH, Lee JH, et al. Thyroid nodules with initially nondiagnostic, fine-needle aspiration results: comparison of core-needle biopsy and repeated fine-needle aspiration. Eur Radiol. 2014; 24:2819–26.

19. Dincer N, Balci S, Yazgan A, et al. Follow-up of atypia and follicular lesions of undetermined significance in thyroid fine needle aspiration cytology. Cytopathology. 2013; 24:385–90.

20. Gocun PU, Karakus E, Bulutay P, Akturk M, Akin M, Poyraz A. What is the malignancy risk for atypia of undetermined significance? Three years’ experience at a university hospital in Turkey. Cancer Cytopathol. 2014; 122:604–10.

21. Gweon HM, Son EJ, Youk JH, Kim JA. Thyroid nodules with Bethesda system III cytology: can ultrasonography guide the next step? Ann Surg Oncol. 2013; 20:3083–8.

22. Ho AS, Sarti EE, Jain KS, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid. 2014; 24:832–9.

23. 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; 122:368–76.

24. 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.

25. Lee SH, Oh HW, Fang Y, et al. Identification of plant compounds that disrupt the insect juvenile hormone receptor complex. Proc Natl Acad Sci USA. 2015; 112:1733–8.

26. Lee SH, Kim MH, Bae JS, Lim DJ, Jung SL, Jung CK. Clinical outcomes in patients with non-diagnostic thyroid fine needle aspiration cytology: usefulness of the thyroid core needle biopsy. Ann Surg Oncol. 2014; 21:1870–7.

27. Moon HJ, Kim EK, Yoon JH, Kwak JY. Malignancy risk stratification in thyroid nodules with nondiagnostic results at cytologic examination: combination of thyroid imaging reporting and data system and the Bethesda System. Radiology. 2015; 274:287–95.

28. Moslavac S, Matesa-Anić D, Matesa N, Kusić Z. When to repeat thyroid fine needle aspiration cytology? Acta Clin Croat. 2012; 51:549–54.

29. 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; 4:189–96.

30. Na DG, Kim JH, Sung JY, 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.

31. Nagarkatti SS, Faquin WC, Lubitz CC, et al. Management of thyroid nodules with atypical cytology on fine-needle aspiration biopsy. Ann Surg Oncol. 2013; 20:60–5.

32. 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.

33. Park KT, Ahn SH, Mo JH, et al. Role of core needle biopsy and ultrasonographic finding in management of indeterminate thyroid nodules. Head Neck. 2011; 33:160–5.

34. Park VY, Kim EK, Kwak JY, Yoon JH, Moon HJ. 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. 2015; 25:2601–7.

35. 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.

36. 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; 122:866–72.

37. Trimboli P, Nasrollah N, Amendola S, et al. A cost analysis of thyroid core needle biopsy vs. diagnostic surgery. Gland Surg. 2015; 4:307–11.

38. 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.

39. 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.

40. 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.

41. 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.

42. Choi SH, Han KH, Yoon JH, et al. Factors affecting inadequate sampling of ultrasound-guided fine-needle aspiration biopsy of thyroid nodules. Clin Endocrinol (Oxf). 2011; 74:776–82.

43. Moon HJ, Kwak JY, Kim EK, Kim MJ. Ultrasonographic characteristics predictive of nondiagnostic results for fine-needle aspiration biopsies of thyroid nodules. Ultrasound Med Biol. 2011; 37:549–55.

44. Orija IB, Piñeyro M, Biscotti C, Reddy SS, Hamrahian AH. Value of repeating a nondiagnostic thyroid fine-needle aspiration biopsy. Endocr Pract. 2007; 13:735–42.

45. 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.

46. Lubitz CC, Nagarkatti SS, Faquin WC, et al. Diagnostic yield of nondiagnostic thyroid nodules is not altered by timing of repeat biopsy. Thyroid. 2012; 22:590–4.

47. Li L, Chen BD, Zhu HF, et al. Comparison of pre-operation diagnosis of thyroid cancer with fine needle aspiration and core-needle biopsy: a meta-analysis. Asian Pac J Cancer Prev. 2014; 15:7187–93.

48. Yoon JH, Kim EK, Kwak JY, Moon HJ. Effectiveness and limitations of core needle biopsy in the diagnosis of thyroid nodules: review of current literature. J Pathol Transl Med. 2015; 49:230–5.

49. Novoa E, Gürtler N, Arnoux A, Kraft M. Role of ultrasound-guided core-needle biopsy in the assessment of head and neck lesions: a meta-analysis and systematic review of the literature. Head Neck. 2012; 34:1497–503.