Influencing Factors of 2D Shear Wave Elastography of the Muscle – An Ex Vivo Animal Study

Abstract

Objective

To evaluate measurement confounders on 2D shear wave elastography (2D-SWE) elastography of muscle.

Materials and Methods

Ex vivo, porcine muscle was examined with a GE LOGIQ E9 ultrasound machine with a 9 L linear (9 MHz) and C1-6 convex probe (operating at 2.5 or 6 MHz). The influence of different confounders on mean shear wave velocity (SWVmean) was analyzed: probes, pressure applied by probe, muscle orientation, together with the impact of different machine settings such as frequency, placement depth and size of region of interest (ROI). The mean of twelve repeated SWVmean measurements (m/s) and coefficient of variation (CV; standard deviation/mean in %) were assessed for each test configuration.

Results

Reproducibility (CV) and maximum possible tissue depth of the linear probe were inferior to the convex probe. With the linear probe, there was a linear decrease of SWVmean with placement depth from 4.56 m/s to 1.81 m/s. A significant increase of SWVmean (p<0.001) was observed for larger ROI widths (range 3.96 m/s to 6.8 m/s). A change in the machine operation mode ('penetration' instead of 'general') led to a significant increase of SWVmean (p=0.04). SWVmean in the longitudinal direction of muscle was significantly higher than in cross section (p<0.001) (e. g. 4.56 m/s versus 3.42 m/s). An increase of linear probe pressure significantly increased muscle SWVmean from 5.29 m/s to 7.21 m/s (p<0.001).

Conclusions

2D-SWE of muscle is influenced by a wealth of parameters. Therefore, standardization of measurement is advisable before application in clinical research studies and routine patient assessment.

Key words

muscular - soft tissues - ultrasound - ultrasound 2D

• References

• 1 Ricci P, Marigliano C, Cantisani V. et al. Ultrasound evaluation of liver fibrosis: Preliminary experience with acoustic structure quantification (ASQ) software. La Radiologia medica 2013; 118: 995-1010
• 2 Correas JM, Drakonakis E, Isidori AM. et al. Update on ultrasound elastography: Miscellanea. Prostate, testicle, musculo-skeletal. Eur J Radiol 2013; 82: 1904-1912
• 3 Dietrich CF, Barr RG, Farrokh A. et al. Strain Elastography–How To Do It?. Ultrasound International Open 2017; 3: E137-e149
• 4 Brandenburg JE, Eby SF, Song P. et al. Ultrasound elastography: The new frontier in direct measurement of muscle stiffness. Arch Phys Med Rehabil 2014; 95: 2207-2219
• 5 Ewertsen C, Carlsen JF, Christiansen IR. et al. Evaluation of healthy muscle tissue by strain and shear wave elastography–Dependency on depth and ROI position in relation to underlying bone. Ultrasonics 2016; 71: 127-133
• 6 Sporea I, Gradinaru-Tascau O, Bota S. 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
• 7 Tang A, Cloutier G, Szeverenyi NM. et al. Ultrasound Elastography and MR Elastography for Assessing Liver Fibrosis: Part 2, Diagnostic Performance, Confounders, and Future Directions. AJR Am J Roentgenol 2015; 205: 33-40
• 8 Park MS, Kim SW, Yoon KT. et al. Factors Influencing the Diagnostic Accuracy of Acoustic Radiation Force Impulse Elastography in Patients with Chronic Hepatitis B. Gut Liver 2016; 10: 275-282
• 9 Pfeifer L, Goertz RS, Neurath MF. et al. Comparison of Acoustic Radiation Force Impulse (ARFI) Elastography Measurements with the 4C1 Transducer to the 6C1HD Transducer: A Phantom and Patient Study. Ultraschall Med 2016;
• 10 Chang S, Kim MJ, Kim J. et al. Variability of shear wave velocity using different frequencies in acoustic radiation force impulse (ARFI) elastography: A phantom and normal liver study. Ultraschall Med 2013; 34: 260-265
• 11 Yang L, Yuan J, Wang Q. et al. Reliability analysis of acoustic radiation force impulse ultrasound imaging with virtual touch tissue quantification: Ex vivo ox liver. Ultrasound Q 2015; 31: 59-62
• 12 Song P, Macdonald M, Behler R. et al. Two-dimensional shear-wave elastography on conventional ultrasound scanners with time-aligned sequential tracking (TAST) and comb-push ultrasound shear elastography (CUSE). IEEE Trans Ultrason Ferroelectr Freq Control 2015; 62: 290-302
• 13 Palmeri ML, McAleavey SA, Fong KL. et al. Dynamic mechanical response of elastic spherical inclusions to impulsive acoustic radiation force excitation. IEEE Trans Ultrason Ferroelectr Freq Control 2006; 53: 2065-2079
• 14 Varbobitis IC, Siakavellas SI, Koutsounas IS. et al. Reliability and applicability of two-dimensional shear-wave elastography for the evaluation of liver stiffness. Eur J Gastroenterol Hepatol 2016;
• 15 Boursier J, Zarski JP, de Ledinghen V. et al. Determination of reliability criteria for liver stiffness evaluation by transient elastography. Hepatology 2013; 57: 1182-1191
• 16 Procopet B, Berzigotti A, Abraldes JG. et al. Real-time shear-wave elastography: Applicability, reliability and accuracy for clinically significant portal hypertension. J Hepatol 2015; 62: 1068-1075
• 17 Thiele M, Madsen BS, Procopet B. et al. Reliability Criteria for Liver Stiffness Measurements with Real-Time 2D Shear Wave Elastography in Different Clinical Scenarios of Chronic Liver Disease. Ultraschall Med 2016;
• 18 Schellhaas B, Strobel D, Wildner D. et al. Two-dimensional shear-wave elastography: A new method comparable to acoustic radiation force impulse imaging?. Eur J Gastroenterol Hepatol 2017; 29: 723-729
• 19 Huang Z, Zheng J, Zeng J. et al. Normal liver stiffness in healthy adults assessed by real-time shear wave elastography and factors that influence this method. Ultrasound Med Biol 2014; 40: 2549-2555
• 20 Bortolotto C, Lungarotti L, Fiorina I. et al. Influence of subjects' characteristics and technical variables on muscle stiffness measured by shear wave elastosonography. J Ultrasound 2017; 20: 139-146
• 21 Blank MAB, Antaki JF. Breast lesion elastography region of interest selection and quantitative heterogeneity: A systematic review and meta-analysis. Ultrasound Med Biol 2017; 43: 387-397
• 22 Skerl K, Vinnicombe S, Giannotti E. et al. Influence of region of interest size and ultrasound lesion size on the performance of 2D shear wave elastography (SWE) in solid breast masses. Clin Radiol 2015; 70: 1421-1427
• 23 Drakonaki EE, Allen GM, Wilson DJ. Ultrasound elastography for musculoskeletal applications. Br J Radiol 2012; 85: 1435-1445
• 24 Gennisson JL, Catheline S, Chaffai S. et al. Transient elastography in anisotropic medium: Application to the measurement of slow and fast shear wave speeds in muscles. J Acoust Soc Am 2003; 114: 536-541
• 25 Gennisson JL, Deffieux T, Mace E. et al. Viscoelastic and anisotropic mechanical properties of in vivo muscle tissue assessed by supersonic shear imaging. Ultrasound Med Biol 2010; 36: 789-801
• 26 Eby SF, Song P, Chen S. et al. Validation of shear wave elastography in skeletal muscle. J Biomech 2013; 46: 2381-2387
• 27 Cortez CD, Hermitte L, Ramain A. et al. Ultrasound shear wave velocity in skeletal muscle: A reproducibility study. Diagn Interv Imaging 2016; 97: 71-79
• 28 Kot BC, Zhang ZJ, Lee AW. et al. Elastic modulus of muscle and tendon with shear wave ultrasound elastography: Variations with different technical settings. PloS one 2012; 7: e44348
• 29 Shiina T, Nightingale KR, Palmeri ML. et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: basic principles and terminology. Ultrasound Med Biol 2015; 41: 1126-1147
• 30 Jiang Y, Li GY, Qian LX. et al. Characterization of the nonlinear elastic properties of soft tissues using the supersonic shear imaging (SSI) technique: Inverse method, ex vivo and in vivo experiments. Med Image Anal 2015; 20: 97-111
• 31 Sanabria SJRM, Otesteanu CF, Mazza E, Goksel O. Non-linear characterization of the liver by combining shear and longitudinal wave speed with strain observations. In Int Tissue Elasticity Conf (ITEC). Vermont, NE, USA: 2016
• 32 Parker KJ, Partin A, Rubens DJ. What do we know about shear wave dispersion in normal and steatotic livers?. Ultrasound Med Biol 2015; 41: 1481-1487