Korean J Radiol.  2019 Jun;20(6):880-893. 10.3348/kjr.2018.0812.

Technical Performance of Two-Dimensional Shear Wave Elastography for Measuring Liver Stiffness: A Systematic Review and Meta-Analysis

Affiliations
  • 1Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea. medimash@gmail.com
  • 2WHO Collaborating Center for Pharmaceutical Policy and Regulation, Department of Pharmaceutical Science, Utrecht University, Utrecht, Netherlands.
  • 3Department of Radiology, Chonnam National University Hospital, Gwangju, Korea.

Abstract


OBJECTIVE
To assess the technical performance of two-dimensional shear wave elastography (2D-SWE) for measuring liver stiffness.
MATERIALS AND METHODS
The Ovid-MEDLINE and EMBASE databases were searched for studies reporting the technical performance of 2D-SWE, including concerns with technical failures, unreliable measurements, interobserver reliability, and/or intraobserver reliability, published until June 30, 2018. The pooled proportion of technical failure and unreliable measurements was calculated using meta-analytic pooling via the random-effects model and inverse variance method for calculating weights. Subgroup analyses were performed to explore potential causes of heterogeneity. The pooled intraclass correlation coefficients (ICCs) for interobserver and intraobserver reliability were calculated using the Hedges-Olkin method with Fisher's Z transformation of the correlation coefficient.
RESULTS
The search yielded 34 articles. From 20 2D-SWE studies including 6196 patients, the pooled proportion of technical failure was 2.3% (95% confidence interval [CI], 1.3-3.9%). The pooled proportion of unreliable measurements from 20 studies including 6961 patients was 7.5% (95% CI, 4.7-11.7%). In the subgroup analyses, studies conducting more than three measurements showed fewer unreliable measurements than did those with three measurements or less, but no intergroup difference was found in technical failure. The pooled ICCs for interobserver reliability (from 10 studies including 517 patients) and intraobserver reliability (from 7 studies including 679 patients) were 0.87 (95% CI, 0.82-0.90) and 0.93 (95% CI, 0.89-0.95), respectively, suggesting good to excellent reliability.
CONCLUSION
2D-SWE shows good technical performance for assessing liver stiffness, with high technical success and reliability. Future studies should establish the quality criteria and optimal number of measurements.

Keyword

Elasticity imaging techniques; Liver; Meta-analysis; Ultrasonography

MeSH Terms

Elasticity Imaging Techniques*
Humans
Liver*
Methods
Population Characteristics
Ultrasonography
Weights and Measures

Figure

  • Fig. 1 Flow diagram of study selection.

  • Fig. 2 Forest plots of proportions of technical failure.CI = confidence interval, F = fixed, R = random.

  • Fig. 3 Forest plots of proportions of unreliable measurements.

  • Fig. 4 Forest plot of interobserver reliability (A) and intraobserver reliability (B).ICC = intraclass correlation coefficient


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Korean J Radiol. 2019;20(11):1527-1535.    doi: 10.3348/kjr.2019.0109.

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Hee Jeong Park, Sun Mi Kim, Bo La Yun, Mijung Jang, Bohyoung Kim, Soo Hyun Lee, Hye Shin Ahn
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Reference

1. Kennedy P, Wagner M, Castéra L, Hong CW, Johnson CL, Sirlin CB, et al. Quantitative elastography methods in liver disease: current evidence and future directions. Radiology. 2018; 286:738–763. PMID: 29461949.
Article
2. Herrmann E, de Lédinghen V, Cassinotto C, Chu WC, Leung VY, Ferraioli G, et al. Assessment of biopsy-proven liver fibrosis by two-dimensional shear wave elastography: an individual patient data-based meta-analysis. Hepatology. 2018; 67:260–272. PMID: 28370257.
Article
3. Lupșor-Platon M, Badea R, Gersak M, Maniu A, Rusu I, Suciu A, et al. Noninvasive assessment of liver diseases using 2D shear wave elastography. J Gastrointestin Liver Dis. 2016; 25:525–532. PMID: 27981309.
Article
4. Amur S, LaVange L, Zineh I, Buckman-Garner S, Woodcock J. Biomarker qualification: toward a multiple stakeholder framework for biomarker development, regulatory acceptance, and utilization. Clin Pharmacol Ther. 2015; 98:34–46. PMID: 25868461.
Article
5. Li C, Zhang C, Li J, Huo H, Song D. Diagnostic accuracy of real-time shear wave elastography for staging of liver fibrosis: a meta-analysis. Med Sci Monit. 2016; 22:1349–1359. PMID: 27102449.
Article
6. Shan QY, Liu BX, Tian WS, Wang W, Zhou LY, Wang Y, et al. Elastography of shear wave speed imaging for the evaluation of liver fibrosis: a meta-analysis. Hepatol Res. 2016; 46:1203–1213. PMID: 26857658.
Article
7. Dietrich CF, Bamber J, Berzigotti A, Bota S, Cantisani V, Castera L, et al. EFSUMB guidelines and recommendations on the clinical use of liver ultrasound elastography, update 2017 (long version). Ultraschall Med. 2017; 38:e16–e47.
Article
8. Bende F, Sporea I, Sirli R, Popescu A, Mare R, Miutescu B, et al. Performance of 2D-SWE.GE for predicting different stages of liver fibrosis, using transient elastography as the reference method. Med Ultrason. 2017; 19:143–149. PMID: 28440347.
Article
9. Bota S, Paternostro R, Etschmaier A, Schwarzer R, Salzl P, Mandorfer M, et al. Performance of 2-D shear wave elastography in liver fibrosis assessment compared with serologic tests and transient elastography in clinical routine. Ultrasound Med Biol. 2015; 41:2340–2349. PMID: 26004669.
Article
10. Cassinotto C, Charrie A, Mouries A, Lapuyade B, Hiriart JB, Vergniol J, et al. Liver and spleen elastography using supersonic shear imaging for the non-invasive diagnosis of cirrhosis severity and oesophageal varices. Dig Liver Dis. 2015; 47:695–701. PMID: 25959234.
Article
11. Cassinotto C, Boursier J, de Lédinghen V, Lebigot J, Lapuyade B, Cales P, et al. Liver stiffness in nonalcoholic fatty liver disease: a comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy. Hepatology. 2016; 63:1817–1827. PMID: 26659452.
Article
12. Deffieux T, Gennisson JL, Bousquet L, Corouge M, Cosconea S, Amroun D, et al. Investigating liver stiffness and viscosity for fibrosis, steatosis and activity staging using shear wave elastography. J Hepatol. 2015; 62:317–324. PMID: 25251998.
Article
13. Elkrief L, Ronot M, Andrade F, Dioguardi Burgio M, Issoufaly T, Zappa M, et al. Non-invasive evaluation of portal hypertension using shear-wave elastography: analysis of two algorithms combining liver and spleen stiffness in 191 patients with cirrhosis. Aliment Pharmacol Ther. 2018; 47:621–630. PMID: 29322599.
Article
14. Fang C, Konstantatou E, Romanos O, Yusuf GT, Quinlan DJ, Sidhu PS. Reproducibility of 2-dimensional shear wave elastography assessment of the liver: a direct comparison with point shear wave elastography in healthy volunteers. J Ultrasound Med. 2017; 36:1563–1569. PMID: 28370146.
Article
15. Ferraioli G, Tinelli C, Zicchetti M, Above E, Poma G, Di Gregorio M, et al. Reproducibility of real-time shear wave elastography in the evaluation of liver elasticity. Eur J Radiol. 2012; 81:3102–3106. PMID: 22749107.
Article
16. Ferraioli G, Tinelli C, Dal Bello B, Zicchetti M, Filice G, Filice C. Accuracy of real-time shear wave elastography for assessing liver fibrosis in chronic hepatitis C: a pilot study. Hepatology. 2012; 56:2125–2133. PMID: 22767302.
Article
17. Gerber L, Kasper D, Fitting D, Knop V, Vermehren A, Sprinzl K, et al. Assessment of liver fibrosis with 2-D shear wave elastography in comparison to transient elastography and acoustic radiation force impulse imaging in patients with chronic liver disease. Ultrasound Med Biol. 2015; 41:2350–2359. PMID: 26116161.
Article
18. Guibal A, Renosi G, Rode A, Scoazec JY, Guillaud O, Chardon L, et al. Shear wave elastography: an accurate technique to stage liver fibrosis in chronic liver diseases. Diagn Interv Imaging. 2016; 97:91–99. PMID: 26655870.
Article
19. Hudson JM, Milot L, Parry C, Williams R, Burns PN. Inter- and intra-operator reliability and repeatability of shear wave elastography in the liver: a study in healthy volunteers. Ultrasound Med Biol. 2013; 39:950–955. PMID: 23453379.
Article
20. Kim TY, Kim JY, Sohn JH, Lee HS, Bang SY, Kim Y, et al. Assessment of substantial liver fibrosis by real-time shear wave elastography in methotrexate-treated patients with rheumatoid arthritis. J Ultrasound Med. 2015; 34:1621–1630. PMID: 26269292.
Article
21. Lee ES, Lee JB, Park HR, Yoo J, Choi JI, Lee HW, et al. Shear wave liver elastography with a propagation map: diagnostic performance and inter-observer correlation for hepatic fibrosis in chronic hepatitis. Ultrasound Med Biol. 2017; 43:1355–1363. PMID: 28431795.
Article
22. Lee SM, Lee JM, Kang HJ, Yang HK, Yoon JH, Chang W, et al. Liver fibrosis staging with a new 2D-shear wave elastography using comb-push technique: applicability, reproducibility, and diagnostic performance. PLoS ONE. 2017; 12:e0177264. PMID: 28510583.
Article
23. Leung VY, Shen J, Wong VW, Abrigo J, Wong GL, Chim AM, et al. Quantitative elastography of liver fibrosis and spleen stiffness in chronic hepatitis B carriers: comparison of shear-wave elastography and transient elastography with liver biopsy correlation. Radiology. 2013; 269:910–918. PMID: 23912619.
Article
24. Maruyama H, Kobayashi K, Kiyono S, Sekimoto T, Kanda T, Yokosuka O. Two-dimensional shear wave elastography with propagation-based reliability assessment for grading hepatic fibrosis and portal hypertension. J Hepatobiliary Pancreat Sci. 2016; 23:595–602. PMID: 27440720.
Article
25. Mulazzani L, Salvatore V, Ravaioli F, Allegretti G, Matassoni F, Granata R, et al. Point shear wave ultrasound elastography with Esaote compared to real-time 2D shear wave elastography with supersonic imagine for the quantification of liver stiffness. J Ultrasound. 2017; 20:213–225. PMID: 28900522.
Article
26. Pellot-Barakat C, Lefort M, Chami L, Labit M, Frouin F, Lucidarme O. Automatic assessment of shear wave elastography quality and measurement reliability in the liver. Ultrasound Med Biol. 2015; 41:936–943. PMID: 25701517.
Article
27. Poynard T, Munteanu M, Luckina E, Perazzo H, Ngo Y, Royer L, et al. Liver fibrosis evaluation using real-time shear wave elastography: applicability and diagnostic performance using methods without a gold standard. J Hepatol. 2013; 58:928–935. PMID: 23321316.
Article
28. Poynard T, Pham T, Perazzo H, Munteanu M, Luckina E, Elaribi D, et al. Real-time shear wave versus transient elastography for predicting fibrosis: applicability, and impact of inflammation and steatosis. A non-invasive comparison. PLoS ONE. 2016; 11:e0163276. PMID: 27706177.
Article
29. Procopet B, Berzigotti A, Abraldes JG, Turon F, Hernandez-Gea V, García-Pagán JC, et al. Real-time shear-wave elastography: applicability, reliability and accuracy for clinically significant portal hypertension. J Hepatol. 2015; 62:1068–1075. PMID: 25514554.
Article
30. Sigrist RMS, El Kaffas A, Jeffrey RB, Rosenberg J, Willmann JK. Intra-individual comparison between 2-D shear wave elastography (GE system) and virtual touch tissue quantification (Siemens system) in grading liver fibrosis. Ultrasound Med Biol. 2017; 43:2774–2782. PMID: 28967501.
Article
31. Sporea I, Bota S, Gradinaru-Taşcău O, Sirli R, Popescu A, Jurchiş A. Which are the cut-off values of 2D-shear wave elastography (2D-SWE) liver stiffness measurements predicting different stages of liver fibrosis, considering transient elastography (TE) as the reference method? Eur J Radiol. 2014; 83:e118–e122. PMID: 24380640.
Article
32. Suh CH, Kim SY, Kim KW, Lim YS, Lee SJ, Lee MG, et al. Determination of normal hepatic elasticity by using real-time shear-wave elastography. Radiology. 2014; 271:895–900. PMID: 24555633.
Article
33. Thiele M, Detlefsen S, Sevelsted Møller L, Madsen BS, Fuglsang Hansen J, Fialla AD, et al. Transient and 2-dimensional shear-wave elastography provide comparable assessment of alcoholic liver fibrosis and cirrhosis. Gastroenterology. 2016; 150:123–133. PMID: 26435270.
Article
34. Thiele M, Madsen BS, Hansen JF, Detlefsen S, Antonsen S, Krag A. Accuracy of the enhanced liver fibrosis test vs fibroTest, elastography, and indirect markers in detection of advanced fibrosis in patients with alcoholic liver disease. Gastroenterology. 2018; 154:1369–1379. PMID: 29317276.
Article
35. Varbobitis IC, Siakavellas SI, Koutsounas IS, Karagiannakis DS, Ioannidou P, Papageorgiou MV, et al. Reliability and applicability of two-dimensional shear-wave elastography for the evaluation of liver stiffness. Eur J Gastroenterol Hepatol. 2016; 28:1204–1209. PMID: 27340898.
Article
36. Woo H, Lee JY, Yoon JH, Kim W, Cho B, Choi BI. Comparison of the reliability of acoustic radiation force impulse imaging and supersonic shear imaging in measurement of liver stiffness. Radiology. 2015; 277:881–886. PMID: 26147680.
Article
37. Yoneda M, Thomas E, Sclair SN, Grant TT, Schiff ER. Supersonic shear imaging and transient elastography with the XL probe accurately detect fibrosis in overweight or obese patients with chronic liver disease. Clin Gastroenterol Hepatol. 2015; 13:1502–1509.e5. PMID: 25804329.
Article
38. Yoon JH, Lee JM, Han JK, Choi BI. Shear wave elastography for liver stiffness measurement in clinical sonographic examinations: evaluation of intraobserver reproducibility, technical failure, and unreliable stiffness measurements. J Ultrasound Med. 2014; 33:437–447. PMID: 24567455.
39. Yoon K, Jeong WK, Kim Y, Kim MY, Kim TY, Sohn JH. 2-dimensional shear wave elastography: interobserver agreement and factors related to interobserver discrepancy. PLoS ONE. 2017; 12:e0175747. PMID: 28414822.
Article
40. Zeng J, Liu GJ, Huang ZP, Zheng J, Wu T, Zheng RQ, et al. Diagnostic accuracy of two-dimensional shear wave elastography for the non-invasive staging of hepatic fibrosis in chronic hepatitis B: a cohort study with internal validation. Eur Radiol. 2014; 24:2572–2581. PMID: 25027837.
Article
41. Zeng J, Zheng J, Huang Z, Chen S, Liu J, Wu T, et al. Comparison of 2-D shear wave elastography and transient elastography for assessing liver fibrosis in chronic hepatitis B. Ultrasound Med Biol. 2017; 43:1563–1570. PMID: 28483579.
Article
42. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med. 2009; 151:W65–W94. PMID: 19622512.
Article
43. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011; 155:529–536. PMID: 22007046.
Article
44. Suh CH, Park SH. Successful publication of systematic review and meta-analysis of studies evaluating diagnostic test accuracy. Korean J Radiol. 2016; 17:5–6. PMID: 26798211.
Article
45. Kim KW, Lee J, Choi SH, Huh J, Park SH. Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part I. General guidance and tips. Korean J Radiol. 2015; 16:1175–1187. PMID: 26576106.
Article
46. Lee J, Kim KW, Choi SH, Huh J, Park SH. Systematic review and meta-analysis of studies evaluating diagnostic test accuracy: a practical review for clinical researchers-part II. Statistical methods of meta-analysis. Korean J Radiol. 2015; 16:1188–1196. PMID: 26576107.
Article
47. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Bmj. 2003; 327:557–560. PMID: 12958120.
Article
48. Higgins J, Green S. Cochrane handbook for systematic reviews of interventions. Version 5.1.0. The Cochrane Collaboration Web site. Updated March 2011. Accessed January 8, 2017. https://handbook-5-1.cochrane.org/.
49. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315:629–634. PMID: 9310563.
Article
50. Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000; 56:455–463. PMID: 10877304.
Article
51. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010; 36:1–48.
52. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016; 15:155–163. PMID: 27330520.
Article
53. Castéra L, Foucher J, Bernard PH, Carvalho F, Allaix D, Merrouche W, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology. 2010; 51:828–835. PMID: 20063276.
Article
54. Wang CZ, Zheng J, Huang ZP, Xiao Y, Song D, Zeng J, et al. Influence of measurement depth on the stiffness assessment of healthy liver with real-time shear wave elastography. Ultrasound Med Biol. 2014; 40:461–469. PMID: 24361224.
55. Barr RG, Ferraioli G, Palmeri ML, Goodman ZD, Garcia-Tsao G, Rubin J, et al. Elastography assessment of liver fibrosis: Society of Radiologists in Ultrasound consensus conference statement. Radiology. 2015; 276:845–861. PMID: 26079489.
Article
56. Buckler AJ, Bresolin L, Dunnick NR, Sullivan DC, Aerts HJ, Bendriem B, et al. Quantitative imaging test approval and biomarker qualification: interrelated but distinct activities. Radiology. 2011; 259:875–884. PMID: 21325035.
Article
57. Sporea I, Bota S, Jurchis A, Sirli R, Grădinaru-Tascău O, Popescu A, et al. Acoustic radiation force impulse and supersonic shear imaging versus transient elastography for liver fibrosis assessment. Ultrasound Med Biol. 2013; 39:1933–1941. PMID: 23932281.
Article
58. Sporea I, Grădinaru-Taşcău O, Bota S, Popescu A, Şirli R, Jurchiş A, et al. How many measurements are needed for liver stiffness assessment by 2D-shear wave elastography (2D-SWE) and which value should be used: the mean or median? Med Ultrason. 2013; 15:268–272. PMID: 24286089.
Article
59. Singh S, Loomba R. Role of two-dimensional shear wave elastography in the assessment of chronic liver diseases. Hepatology. 2018; 67:13–15. PMID: 28777887.
Article
60. Ferraioli G, Filice C, Castera L, Choi BI, Sporea I, Wilson SR, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 3: liver. Ultrasound Med Biol. 2015; 41:1161–1179. PMID: 25800942.
Article
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