Clin Endosc.  2023 Mar;56(2):229-238. 10.5946/ce.2022.135.

Defining the optimal technique for endoscopic ultrasound shear wave elastography: a combined benchtop and animal model study with comparison to transabdominal shear wave elastography

• Wang TJ
• Ryou M

• KMID: 2540741
• DOI: http://doi.org/10.5946/ce.2022.135

Abstract

Background/Aims
Shear wave elastography (SWE) is used for liver fibrosis staging based on stiffness measurements. It can be performed using endoscopic ultrasound (EUS) or a transabdominal approach. Transabdominal accuracy can be limited in patients with obesity because of the thick abdomen. Theoretically, EUS-SWE overcomes this limitation by internally assessing the liver. We aimed to define the optimal technique for EUS-SWE for future research and clinical use and compare its accuracy with that of transabdominal SWE.
Methods
Benchtop study: A standardized phantom model was used. The compared variables included the region of interest (ROI) size, depth, and orientation and transducer pressure. Porcine study: Phantom models with varying stiffness values were surgically implanted between the hepatic lobes.
Results
For EUS-SWE, a larger ROI size of 1.5 cm and a smaller ROI depth of 1 cm demonstrated a significantly higher accuracy. For transabdominal SWE, the ROI size was nonadjustable, and the optimal ROI depth ranged from 2 to 4 cm. The transducer pressure and ROI orientation did not significantly affect the accuracy. There were no significant differences in the accuracy between transabdominal SWE and EUS-SWE in the animal model. The variability among the operators was more pronounced for the higher stiffness values. Small lesion measurements were accurate only when the ROI was entirely situated within the lesion.
Conclusions
We defined the optimal viewing windows for EUS-SWE and transabdominal SWE. The accuracy was comparable in the non-obese porcine model. EUS-SWE may have a higher utility for evaluating small lesions than transabdominal SWE.

Keyword

Elastography in patients with obesity; Elastography of focal lesions; Liver fibrosis; Porcine model; Two-dimensional shear wave

Figure

• 

  Fig. 1. Visualization of the adjustable region of interest (ROI) parameters on transabdominal shear wave elastography (SWE) and endoscopic ultrasound SWE (EUS-SWE). E, stiffness value (kPa); Vs, velocity (used to calculate the stiffness value using the formula E=3Vs2ρ); ATT, attenuation coefficient (not analyzed in this study as it is only available for transabdominal SWE, not for EUS-SWE); VsN, reliability indicator.

• 

  Fig. 2. Comparison of the changes in the region of interest (ROI) size (A), ROI depth (B), ROI orientation (C), and pressure exerted by the transducer probe (D) relative to the accuracy of the measurements on endoscopic ultrasound shear wave elastography. All measurements are reported as averages±standard errors. Significant p-values (p<0.05) for pairwise comparisons are shown. Non-significant differences are not shown.

• 

  Fig. 3. Comparison of the changes in the region of interest (ROI) depth relative to the accuracy of the measurements on transabdominal shear wave elastography. All measurements are reported as averages±standard errors. Bars highlighted in dark orange indicate significantly higher percentage deviations than do bars highlighted in light orange (p<0.05), with p-values from pairwise comparisons shown. The same color bars demonstrate no significant difference in the pairwise comparison.

• 

  Fig. 4. Comparison of the accuracy of the varying stiffness measurements between transabdominal shear wave elastography (SWE) and endoscopic ultrasound SWE (EUS-SWE). All measurements are reported as averages±standard errors. There were no significant differences among the pairwise comparisons between transabdominal SWE and EUS-SWE for all reference stiffness values (p>0.05) (p-values not shown).

• 

  Fig. 5. Assessment of the variability in the accuracy among the operators for transabdominal shear wave elastography (SWE) and endoscopic ultrasound SWE. All measurements are reported as averages±standard errors. Significant p-values (p<0.05) in the pairwise comparisons are displayed, while non-significant values are not shown. No pairwise comparisons among the operators were significant at 7.3 kPa ([A, B] for EUS and transabdominal SWE, respectively), whereas for 19.2 kPa ([C, D] for EUS and transabdominal SWE, respectively) there were some pairwise differences in % deviation between operators.

• 

  Fig. 6. Accuracy of endoscopic ultrasound (EUS)-shear wave elastography in assessing smaller lesions of interest. t-test comparison between the region of interest (ROI) centered entirely within a lesion (bottom right ultrasound image) and ROI that included tissue outside the periphery of the lesion (top right ultrasound image). Significant differences (p<0.05) were observed.

Reference

1. Gennisson JL, Deffieux T, Fink M, et al. Ultrasound elastography: principles and techniques. Diagn Interv Imaging. 2013; 94:487–495.

2. Sandrin L, Fourquet B, Hasquenoph JM, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003; 29:1705–1713.

3. Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006; 55:403–408.

4. Gallotti A, D’Onofrio M, Romanini L, et al. Acoustic radiation force impulse (ARFI) ultrasound imaging of solid focal liver lesions. Eur J Radiol. 2012; 81:451–455.

5. Bota S, Herkner H, Sporea I, et al. Meta-analysis: ARFI elastography versus transient elastography for the evaluation of liver fibrosis. Liver Int. 2013; 33:1138–1147.

6. Friedrich-Rust M, Ong MF, Herrmann E, et al. Real-time elastography for noninvasive assessment of liver fibrosis in chronic viral hepatitis. AJR Am J Roentgenol. 2007; 188:758–764.

7. Ferraioli G, Parekh P, Levitov AB, et al. Shear wave elastography for evaluation of liver fibrosis. J Ultrasound Med. 2014; 33:197–203.

8. Guibal A, Boularan C, Bruce M, et al. Evaluation of shearwave elastography for the characterisation of focal liver lesions on ultrasound. Eur Radiol. 2013; 23:1138–1149.

9. Loomba R, Wolfson T, Ang B, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology. 2014; 60:1920–1928.

10. Kennedy P, Wagner M, Castéra L, et al. Quantitative elastography methods in liver disease: current evidence and future directions. Radiology. 2018; 286:738–763.

11. Friedrich-Rust M, Poynard T, Castera L. Critical comparison of elastography methods to assess chronic liver disease. Nat Rev Gastroenterol Hepatol. 2016; 13:402–411.

12. Kawada N, Tanaka S. Elastography for the pancreas: current status and future perspective. World J Gastroenterol. 2016; 22:3712–3724.

13. Sande JA, Verjee S, Vinayak S, et al. Ultrasound shear wave elastography and liver fibrosis: a prospective multicenter study. World J Hepatol. 2017; 9:38–47.

14. Sebag F, Vaillant-Lombard J, Berbis J, 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; 95:5281–5288.

15. Evans A, Whelehan P, Thomson K, et al. Quantitative shear wave ultrasound elastography: initial experience in solid breast masses. Breast Cancer Res. 2010; 12:R104.

16. Bruce M, Kolokythas O, Ferraioli G, et al. Limitations and artifacts in shear-wave elastography of the liver. Biomed Eng Lett. 2017; 7:81–89.

17. Staugaard B, Christensen PB, Mössner B, et al. Feasibility of transient elastography versus real-time two-dimensional shear wave elastography in difficult-to-scan patients. Scand J Gastroenterol. 2016; 51:1354–1359.

18. Cassinotto C, Boursier J, de Lédinghen V, 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.

19. Herrmann E, de Lédinghen V, Cassinotto C, 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.

20. Jamialahmadi T, Nematy M, Jangjoo A, et al. Measurement of liver stiffness with 2D-shear wave elastography (2D-SWE) in bariatric surgery candidates reveals acceptable diagnostic yield compared to liver biopsy. Obes Surg. 2019; 29:2585–2592.

21. Ohno E, Hirooka Y, Kawashima H, et al. Feasibility of EUS-guided shear-wave measurement: a preliminary clinical study. Endosc Ultrasound. 2019; 8:215–216.

22. Ohno E, Hirooka Y, Kawashima H, et al. Feasibility and usefulness of endoscopic ultrasonography-guided shear-wave measurement for assessment of autoimmune pancreatitis activity: a prospective exploratory study. J Med Ultrason (2001). 2019; 46:425–433.

23. Yamashita Y, Tanioka K, Kawaji Y, et al. Endoscopic ultrasonography shear wave as a predictive factor of endocrine/exocrine dysfunction in chronic pancreatitis. J Gastroenterol Hepatol. 2021; 36:391–396.

24. Ohno E, Kawashima H, Ishikawa T, et al. Diagnostic performance of endoscopic ultrasonography-guided elastography for solid pancreatic lesions: shear-wave measurements versus strain elastography with histogram analysis. Dig Endosc. 2021; 33:629–638.

25. Yada N, Sakurai T, Minami T, et al. A newly developed shear wave elastography modality: with a unique reliability index. Oncology. 2015; 89 Suppl 2:53–59.

26. Wong GL, Wong VW, Chim AM, et al. Factors associated with unreliable liver stiffness measurement and its failure with transient elastography in the Chinese population. J Gastroenterol Hepatol. 2011; 26:300–305.

27. Xia B, Wang F, Friedrich-Rust M, et al. Feasibility and efficacy of transient elastography using the XL probe to diagnose liver fibrosis and cirrhosis: a meta-analysis. Medicine (Baltimore). 2018; 97:e11816.

28. Dhyani M, Grajo JR, Bhan AK, et al. Validation of shear wave elastography cutoff values on the supersonic aixplorer for practical clinical use in liver fibrosis staging. Ultrasound Med Biol. 2017; 43:1125–1133.