Ultrasonography.  2014 Apr;33(2):75-82.

Ultrasound elastography for thyroid nodules: recent advances

• Kwak JY
• Kim EK

Abstract

Ultrasonography (US)-based elastography has been introduced as a noninvasive technique for evaluating thyroid nodules that encompasses a variety of approaches such as supersonic shear imaging and acoustic radiation force impulse imaging as well as real-time tissue elastography. However, the diagnostic performances for differentiating malignant thyroid nodules from benign ones with elastography as an adjunctive tool of gray-scale US is still under debate. In this review article, diagnostic performances of conventional US and a combination of conventional US and elastography are compared according to the type of elastography. Further, the interobserver variability of elastography is presented according to the type of elastography.

Keyword

Thyroid nodule; Ultrasonography; Elasticity imaging techniques

MeSH Terms

Elasticity Imaging Techniques*
Observer Variation
Thyroid Nodule*
Ultrasonography*

Figure

• 

  Fig. 1. Principle of ultrasound elastography. A. Strain elastography evaluates elasticity through tissue displacement caused by compression, with the degree of displacement being larger in soft tissue than in hard tissue. B. Shear wave elastography evaluates elasticity through the propagation speed of transverse-oriented shear waves, with the wave speed being faster in hard tissue than in soft tissue.

• 

  Fig. 2. Qualitative assessment of strain elastography.A. Strain elastographic scores by Rago et al. [6]. A score of 1 indicated even elasticity in the whole nodule. A score of 2 indicated elasticity in a large part of the nodule. A score of 3 indicated elasticity only at the peripheral part of the nodule. A score of 4 indicated no elasticity in the nodule. A score of 5 indicated no elasticity in the nodule or in the area showing posterior shadowing. B. Strain elastographic scores by Asteria et al. [7]. A score of 1 indicated elasticity in the entire examined area. A score of 2 indicated elasticity in a large part of the examined area. A score of 3 indicated stiffness in a large part of the examined area. A score of 4 indicated a nodule without elasticity.

• 

  Fig. 3. Quantitative assessment of shear wave elastography.Elasticity of the nodule is expressed in the unit of kilopascals (kPa) in the right Q-Box.

Reference

Reference

1. Kim EK, Park CS, Chung WY, Oh KK, Kim DI, Lee JT, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am J Roentgenol. 2002; 178:687–691.

2. Moon WJ, Baek JH, Jung SL, Kim DW, Kim EK, Kim JY, et al. Ultrasonography and the ultrasound-based management of thyroid nodules: consensus statement and recommendations. Korean J Radiol. 2011; 12:1–14.

3. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009; 19:1167–1214.

4. Gharib H, Papini E, Paschke R, Duick DS, Valcavi R, Hegedus 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.

5. Park SH, Kim SJ, Kim EK, Kim MJ, Son EJ, Kwak JY. Interobserver agreement in assessing the sonographic and elastographic features of malignant thyroid nodules. AJR Am J Roentgenol. 2009; 193:W416–W423.

6. Rago T, Santini F, Scutari M, Pinchera A, Vitti P. Elastography: new developments in ultrasound for predicting malignancy in thyroid nodules. J Clin Endocrinol Metab. 2007; 92:2917–2922.

7. Asteria C, Giovanardi A, Pizzocaro A, Cozzaglio L, Morabito A, Somalvico F, et al. US-elastography in the differential diagnosis of benign and malignant thyroid nodules. Thyroid. 2008; 18:523–531.

8. Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med. 2013; 34:238–253.

9. Cantisani V, Lodise P, Grazhdani H, Mancuso E, Maggini E, Di Rocco G, et al. Ultrasound elastography in the evaluation of thyroid pathology. Current status. Eur J Radiol. 2013. Jun 11 [Epub]. http://dx.doi.org/10.1016/j.ejrad.2013.05.008.

10. Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology. 2006; 239:341–350.

11. Cantisani V, Grazhdani H, Ricci P, Mortele K, Di Segni M, D'Andrea V, et al. Q-elastosonography of solid thyroid nodules: assessment of diagnostic efficacy and interobserver variability in a large patient cohort. Eur Radiol. 2014; 24:143–150.

12. Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall Med. 2013; 34:169–184.

13. Sebag F, Vaillant-Lombard J, Berbis J, Griset V, Henry JF, Petit P, et al. Shear wave elastography: a new ultrasound imaging mode for the differential diagnosis of benign and malignant thyroid nodules. J Clin Endocrinol Metab. 2010; 95:5281–5258.

14. Kim H, Kim JA, Son EJ, Youk JH. Quantitative assessment of shearwave ultrasound elastography in thyroid nodules: diagnostic performance for predicting malignancy. Eur Radiol. 2013; 23:2532–2537.

15. Zhang YF, Xu HX, He Y, Liu C, Guo LH, Liu LN, et al. Virtual touch tissue quantification of acoustic radiation force impulse: a new ultrasound elastic imaging in the diagnosis of thyroid nodules. PLoS One. 2012; 7:e49094.

16. Bhatia KS, Tong CS, Cho CC, Yuen EH, Lee YY, Ahuja AT. Shear wave elastography of thyroid nodules in routine clinical practice: preliminary observations and utility for detecting malignancy. Eur Radiol. 2012; 22:2397–2406.

17. Bojunga J, Dauth N, Berner C, Meyer G, Holzer K, Voelkl L, et al. Acoustic radiation force impulse imaging for differentiation of thyroid nodules. PLoS One. 2012; 7:e42735.

18. Ueno E, Itoh A. Diagnosis of breast cancer by elasticity imaging. Eizo Joho Med. 2004; 36(12):2–6.

19. 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; 262:1002–1013.

20. Bhatia K, Tong CS, Cho CC, Yuen EH, Lee J, Ahuja AT. Reliability of shear wave ultrasound elastography for neck lesions identified in routine clinical practice. Ultraschall Med. 2012; 33:463–468.

21. Veyrieres JB, Albarel F, Lombard JV, Berbis J, Sebag F, Oliver C, et al. A threshold value in Shear Wave elastography to rule out malignant thyroid nodules: a reality? Eur J Radiol. 2012; 81:3965–3972.

22. Szczepanek-Parulska E, Wolinski K, Stangierski A, Gurgul E, Biczysko M, Majewski P, et al. Comparison of diagnostic value of conventional ultrasonography and shear wave elastography in the prediction of thyroid lesions malignancy. PLoS One. 2013; 8:e81532.

23. Shweel M, Mansour E. Diagnostic performance of combined elastosonography scoring and high-resolution ultrasonography for the differentiation of benign and malignant thyroid nodules. Eur J Radiol. 2013; 82:995–1001.

24. Russ G, Royer B, Bigorgne C, Rouxel A, Bienvenu-Perrard M, Leenhardt L. Prospective evaluation of thyroid imaging reporting and data system on 4550 nodules with and without elastography. Eur J Endocrinol. 2013; 168:649–655.

25. Trimboli P, Guglielmi R, Monti S, Misischi I, Graziano F, Nasrollah N, et al. Ultrasound sensitivity for thyroid malignancy is increased by real-time elastography: a prospective multicenter study. J Clin Endocrinol Metab. 2012; 97:4524–4530.

26. Ragazzoni F, Deandrea M, Mormile A, Ramunni MJ, Garino F, Magliona G, et al. High diagnostic accuracy and interobserver reliability of real-time elastography in the evaluation of thyroid nodules. Ultrasound Med Biol. 2012; 38:1154–1162.

27. Cappelli C, Pirola I, Gandossi E, Agosti B, Cimino E, Casella C, et al. Real-time elastography: a useful tool for predicting malignancy in thyroid nodules with nondiagnostic cytologic findings. J Ultrasound Med. 2012; 31:1777–1782.

28. Unluturk U, Erdogan MF, Demir O, Gullu S, Baskal N. Ultrasound elastography is not superior to grayscale ultrasound in predicting malignancy in thyroid nodules. Thyroid. 2012; 22:1031–1038.

29. Razavi SA, Hadduck TA, Sadigh G, Dwamena BA. Comparative effectiveness of elastographic and B-mode ultrasound criteria for diagnostic discrimination of thyroid nodules: a meta-analysis. AJR Am J Roentgenol. 2013; 200:1317–1326.

30. Danese D, Sciacchitano S, Farsetti A, Andreoli M, Pontecorvi A. Diagnostic accuracy of conventional versus sonography-guided fineneedle aspiration biopsy of thyroid nodules. Thyroid. 1998; 8:15–21.

31. Kim SJ, Kim EK, Park CS, Chung WY, Oh KK, Yoo HS. Ultrasoundguided fine-needle aspiration biopsy in nonpalpable thyroid nodules: is it useful in infracentimetric nodules? Yonsei Med J. 2003; 44:635–640.

32. 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; 17:2147–2155.

33. Yoon JH, Moon HJ, Kim EK, Kwak JY. Inadequate cytology in thyroid nodules: should we repeat aspiration or follow-up? Ann Surg Oncol. 2011; 18:1282–1289.

34. Park SJ, Sun JY, Hong K, Kwak JY, Kim EK, Chung WY, et al. Application of BRAF, NRAS, KRAS mutations as markers for the detection of papillary thyroid cancer from FNAB specimens by pyrosequencing analysis. Clin Chem Lab Med. 2013; 51:1673–1680.

35. Kwak JY, Kim EK, Kim JK, Han JH, Hong SW, Park TS, et al. Dual priming oligonucleotide-based multiplex PCR analysis for detection of BRAFV600E mutation in FNAB samples of thyroid nodules in BRAFV600E mutation-prevalent area. Head Neck. 2010; 32:490–498.

36. Caraci P, Aversa S, Mussa A, Pancani G, Ondolo C, Conticello S. Role of fine-needle aspiration biopsy and frozen-section evaluation in the surgical management of thyroid nodules. Br J Surg. 2002; 89:797–801.

37. Cantisani V, Ulisse S, Guaitoli E, De Vito C, Caruso R, Mocini R, et al. Q-elastography in the presurgical diagnosis of thyroid nodules with indeterminate cytology. PLoS One. 2012; 7:e50725.

38. Rago T, Scutari M, Santini F, Loiacono V, Piaggi P, Di Coscio G, et al. Real-time elastosonography: useful tool for refining the presurgical diagnosis in thyroid nodules with indeterminate or nondiagnostic cytology. J Clin Endocrinol Metab. 2010; 95:5274–5280.

39. Lippolis PV, Tognini S, Materazzi G, Polini A, Mancini R, Ambrosini CE, et al. Is elastography actually useful in the presurgical selection of thyroid nodules with indeterminate cytology? J Clin Endocrinol Metab. 2011; 96:E1826–E1830.

40. Kim JK, Baek JH, Lee JH, Kim JL, Ha EJ, Kim TY, et al. Ultrasound elastography for thyroid nodules: a reliable study? Ultrasound Med Biol. 2012; 38:1508–1513.

41. Calvete AC, Rodriguez JM, Rios A, Abellan-Rivero D, Reus M. Interobserver agreement for thyroid elastography: value of the quality factor. J Ultrasound Med. 2013; 32:495–504.

42. Merino S, Arrazola J, Cardenas A, Mendoza M, De Miguel P, Fernandez C, et al. Utility and interobserver agreement of ultrasound elastography in the detection of malignant thyroid nodules in clinical care. AJNR Am J Neuroradiol. 2011; 32:2142–2148.

43. Lim DJ, Luo S, Kim MH, Ko SH, Kim Y. Interobserver agreement and intraobserver reproducibility in thyroid ultrasound elastography. AJR Am J Roentgenol. 2012; 198:896–901.

44. Bhatia KS, Rasalkar DP, Lee YP, Wong KT, King AD, Yuen HY, et al. Cystic change in thyroid nodules: a confounding factor for realtime qualitative thyroid ultrasound elastography. Clin Radiol. 2011; 66:799–807.

45. Lee SH, Chang JM, Cho N, Koo HR, Yi A, Kim SJ, et al. Practice guideline for the performance of breast ultrasound elastography. Ultrasonography. 2014; 33:3–10.

46. Youk JH, Son EJ, Park AY, Kim JA. Shear-wave elastography for breast masses: local shear wave speed (m/sec) versus Young modulus (kPa). Ultrasonography. 2014; 33:34–39.

47. Chang JM, Won JK, Lee KB, Park IA, Yi A, Moon WK. Comparison of shear-wave and strain ultrasound elastography in the differentiation of benign and malignant breast lesions. AJR Am J Roentgenol. 2013; 201:W347–W356.

48. Kim JE, Lee JY, Bae KS, Han JK, Choi BI. Acoustic radiation force impulse elastography for focal hepatic tumors: usefulness for differentiating hemangiomas from malignant tumors. Korean J Radiol. 2013; 14:743–753.

49. Kim JE, Lee JY, Kim YJ, Yoon JH, Kim SH, Lee JM, et al. Acoustic radiation force impulse elastography for chronic liver disease: comparison with ultrasound-based scores of experienced radiologists, Child-Pugh scores and liver function tests. Ultrasound Med Biol. 2010; 36:1637–1643.

50. Ko KH, Jung HK, Kim SJ, Kim H, Yoon JH. Potential role of shearwave ultrasound elastography for the differential diagnosis of breast non-mass lesions: preliminary report. Eur Radiol. 2014; 24:305–311.