Z Gastroenterol 2017; 55(02): 153-166
DOI: 10.1055/s-0042-117226
Übersicht
© Georg Thieme Verlag KG Stuttgart · New York

Shear wave elastography of the liver – review on normal values

Scherwellenelastografie der Leber, eine Normwertanalyse
Yi Dong
1   Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
,
Roxana Sirli
2   Department of Gastroenterology and Hepatology, University of Medicine and Pharmacy Victor Babes, Timisoara, Romania
,
Giovanna Ferraioli
3   Ultrasound Unit, Department of Infectious Diseases, Fondazione IRCCS Policlinico San Matteo, University of Pavia, Pavia, Italy
,
Ioan Sporea
2   Department of Gastroenterology and Hepatology, University of Medicine and Pharmacy Victor Babes, Timisoara, Romania
,
Liliana Chiorean
4   Department of Medical Imaging, des Cévennes Clinic, Annonay, France and Caritas Krankenhaus Bad Mergentheim, Bad Mergentheim, Germany
,
Xinwu Cui
5   Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
,
Mei Fan
6   Sino-German Research Center of Ultrasound in Medicine, The First Affiliated Hospital of Zhengzou University, Zhengzfou, China
,
Wen-Ping Wang
1   Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China
,
Odd Helge Gilja
7   National Centre for Ultrasound in Gastroenterology, Haukeland University Hospital, Bergen and Department of Clinical Medicine, University of Bergen, Norway
,
Paul S. Sidhu
8   Department of Radiology, King's College London, King's College Hospital, Denmark Hill, London
,
Christoph F. Dietrich
9   Medizinische Klinik 2, Caritas-Krankenhaus Bad Mergentheim, Germany. Sino-German Research Center of Ultrasound in Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
› Author Affiliations
Further Information

Publication History

13 July 2016

08 September 2016

Publication Date:
13 February 2017 (online)

Abstract

Shear wave elastography (SWE) has been developed to non-invasively estimate liver stiffness. Different techniques are available and they are described in detail in the EFSUMB guidelines on elastography. However, there are only a few published studies investigating normal ranges in healthy subjects by comparing different equipment and analysing influencing factors. In the present review, we summarize the impact factors on liver stiffness measurement (LSM) using SWE, report its reproducibility, and define normal range tables of LSM in healthy subjects for clinical practice according to the published literature.

Zusammenfassung

Die Scherwellenelastografie hat sich als nicht invasive Methode zur Leberfibrosediagnostik etabliert. Verschiedene Methoden wurden beschrieben und sind in den EFSUMB-Leitlinien zusammengefasst. Allerdings gibt es nur wenige Informationen zu der Vergleichbarkeit von Normwerten verschiedener Ultraschallgeräte. In der hier vorgestellten Übersichtsarbeit werden Normwerte, Reproduzierbar- sowie Vergleichbarkeit anhand der publizierten Literatur analysiert, zusammengefasst und diskutiert.

 
  • References

  • 1 Bamber J. Cosgrove D. Dietrich CF. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in Med 2013; 34: 169-184
  • 2 Cosgrove D. Piscaglia F. Bamber J. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall in Med 2013; 34: 238-253
  • 3 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
  • 4 Ferraioli G. Filice C. Castera L. et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 3: liver. Ultrasound Med Biol 2015; 41: 1161-1179
  • 5 Ling W. Lu Q. Quan J. et al. Assessment of impact factors on shear wave based liver stiffness measurement. Eur J Radiol 2013; 82: 335-341
  • 6 Lu Q. Lu C. Li J. et al. Stiffness values and serum biomarkers in liver fibrosis staging: study in large surgical specimens in patients with chronic Hepatitis B. Radiology 2016; DOI: ???. [Epub ahead of print]
  • 7 Chen S. Sanchez W. Callstrom M. et al. Assessment of liver viscoelasticity by Using shear waves induced by ultrasound radiation force. Radiology 2013; 266: 964­-970
  • 8 Franchi-Abella S. Corno L. Gonzales E. et al. Feasibility and diagnostic accuracy of supersonic shear-wave elastography for the assessment of liver stiffness and liver fibrosis in children: a pilot study of 96 patients. Radiology 2016; 278: 554-562
  • 9 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
  • 10 Leung VY. Shen J. Wong VW. 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 2015; 269: 910-918
  • 11 Barr RG. Ferraioli G. Palmeri ML. et al. Elastography assessment of liver fibrosis: Society of Radiologists in Ultrasound consensus conference statement. Radiology 2015; 276: 845-861
  • 12 Cui XW. Friedrich-Rust M. De Molo C. et al. Liver elastography, comments on EFSUMB elastography guidelines 2013. World J Gastroenterol 2013; 19: 6329-6347
  • 13 Dietrich CF. Saftoiu A. Jenssen C. Real time elastography endoscopic ultrasound (RTE-EUS), a comprehensive review. Eur J Radiol 2014; 83: 405-414
  • 14 Dietrich CF. Jenssen C. Arcidiacono PG. et al. Endoscopic ultrasound: Elastographic lymph node evaluation. Endosc Ultrasound 2015; 4: 176-190
  • 15 Cui XW. Chang JM. Kan QC. et al. Endoscopic ultrasound elastography: Current status and future perspectives. World J Gastroenterol 2015; 21: 13212-13224
  • 16 Saftoiu A. Vilmann P. Gorunescu F. et al. Efficacy of an artificial neural network-based approach to endoscopic ultrasound elastography in diagnosis of focal pancreatic masses. Clin Gastroenterol Hepatol 2012; 10: 84-90
  • 17 Saftoiu A. Vilmann P. Gorunescu F. et al. Accuracy of endoscopic ultrasound elastography used for differential diagnosis of focal pancreatic masses: a multicenter study. Endoscopy 2011; 43: 596-603
  • 18 Saftoiu A. Iordache SA. Gheonea DI. et al. Combined contrast-enhanced power Doppler and real-time sonoelastography performed during EUS, used in the differential diagnosis of focal pancreatic masses (with videos). Gastrointest Endosc 2010; 72: 739-747
  • 19 Carlsen JF. Pedersen MR. Ewertsen C. et al. A comparative study of strain and shear-wave elastography in an elasticity phantom. Am J Roentgenol 2015; 204: W236-W242
  • 20 Dillman JR. Chen S. Davenport MS. et al. Superficial ultrasound shear wave speed measurements in soft and hard elasticity phantoms: repeatability and reproducibility using two ultrasound systems. Pediatr Radiol 2015; 45: 376-385
  • 21 Shin HJ. Kim HY. Roh YH. et al. Comparison of shear wave velocities on ultrasound elastography between differentmachines, transducers, and acquisition depths: a phantom study. Eur Radiol 2016; DOI: ???. [Epub ahead of print]
  • 22 Hall TJ. Milkowski A. Garra B. et al. RSNA/QIBA: shear wave speed as a biomarker for liver fibrosis staging. Ultrasonics Symposium (IUS). Prague : IEEE International; 2013
  • 23 Goldschmidt I. Streckenbach C. Dingemann C. et al. Application and limitations of transient liver elastography in children. J Pediatr Gastroenterol Nutr 2013; 57: 109-113
  • 24 Ferraioli G. Lissandrin R. Zicchetti M. et al. Assessment of liver stiffness with transient elastography by using S and M probes in healthy children. Eur J Pediatr 2012; 171: 1415
  • 25 Myers RP. Pomier-Layrargues G. Kirsch R. et al. Feasibility and diagnostic performance of the FibroScan XL probe for liver stiffness measurement in overweight and obese patients. Hepatology 2012; 55: 199-208
  • 26 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 in Med 2013; 34: 260-265
  • 27 Fontanilla T. Canas T. Macia A. et al. Normal values of liver shear wave velocity in healthy children assessed by acoustic radiation force impulse imaging using a convex probe and a linear probe. Ultrasound Med Biol 2014; 40: 470-477
  • 28 Galgenmueller S. Jaeger H. Kratzer W. et al. Parameters affecting different acoustic radiation force impulse applications in the diagnosis of fibrotic liver changes. World J Gastroenterol 2015; 21: 8425-8432
  • 29 Yamanaka N. Kaminuma C. Taketomi-Takahashi A. et al. Reliable measurement by virtual touch tissue quantification with acoustic radiation force impulse imaging: phantom study. J Ultrasound Med 2012; 31: 1239-1244
  • 30 Hanquinet S. Courvoisier D. Kanavaki A. et al. Acoustic radiation force impulse imaging-normal values of liver stiffness in healthy children. Pediatr Radiol 2013; 43: 539-544
  • 31 Muller M. Gennisson JL. Deffieux T. et al. Quantitative viscoelasticity mapping of human liver using supersonic shear imaging: preliminary in vivo feasability study. Ultrasound Med Biol 2009; 35: 219-229
  • 32 Ferraioli G. Tinelli C. Lissandrin R. et al. Ultrasound point shear wave elastography assessment of liver and spleen stiffness: effect of training on repeatability of measurements. Eur Radiol 2014; 24: 1283-1289
  • 33 D’Onofrio M. Gallotti A. Mucelli RP. Tissue quantification with acoustic radiation force impulse imaging: Measurement repeatability and normal values in the healthy liver. Am J Roentgenol 2010; 195: 132-136
  • 34 Yoon J. Lee JM. Han JK. et al. 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
  • 35 Wang CZ. Zheng J. Huang ZP. 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
  • 36 Karlas T. Pfrepper C. Wiegand J. et al. Acoustic radiation force impulse imaging (ARFI) for non-invasive detection of liver fibrosis: examination standards and evaluation of interlobe differences in healthy subjects and chronic liver disease. Scand J Gastroenterol 2011; 46: 1458-1467
  • 37 Ferraioli G. Tinelli C. Zicchetti M. et al. Reproducibility of real-time shear wave elastography in the evaluation of liver elasticity. Eur J Radiol 2012; 81: 3102-3106
  • 38 Karlas T. Dietrich A. Peter V. et al. Evaluation of transient elastography, acoustic radiation force impulse imaging (ARFI), and enhanced liver function (ELF) score for detection of fibrosis in morbidly obese patients. PLoS One 2015; 10: e0141649
  • 39 Hudson JM. Milot L. Parry C. et al. 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
  • 40 Suh CH. Kim SY. Kim KW. et al. Determination of normal hepatic elasticity by using real-time shear-wave elastography. Radiology 2014; 271: 895-900
  • 41 Sirli R. Sporea I. Tudora A. et al. Transient elastographic evaluation of subjects without known hepatic pathology: does age change the liver stiffness?. J Gastrointestin Liver Dis 2009; 18: 57-60
  • 42 Roulot D. Czernichow S. Le Clésiau H. et al. Liver stiffness values in apparently healthy subjects: influence of gender and meolic syndrome. J Hepatol 2008; 48: 606-613
  • 43 Kumar M. Sharma P. Garg H. et al. Transient elastographic evaluation in adult subjects without overt liver disease: influence of alanine aminotransferase levels. J Gastroenterol Hepatol 2011; 26: 1318-1325
  • 44 Engelmann G. Gebhardt C. Wenning D. et al. Feasibility study and control values of transient elastography in healthy children. Eur J Pediatr 2012; 171: 353-360
  • 45 Colombo S. Belloli L. Zaccanelli M. et al. Normal liver stiffness and its determinants in healthy blood donors. Dig Liver Dis 2011; 43: 231-236
  • 46 Corpechot C. El Naggar A. Poupon R. Gender and liver: is the liver stiffness weaker in weaker sex?. Hepatology 2006; 44: 513-514
  • 47 Șirli R. Bota S. Sporea I. et al. Liver stiffness measurements by means of supersonic shear imaging in patients without known liver pathology. Ultrasound Med Biol 2013; 39: 1362-1367
  • 48 Arda K. Ciledag N. Arıbas BK. et al. Quantitative assessment of the elasticity values of liver with shear wave ultrasonographic elastography. Indian J Med Res 2013; 137: 911-915
  • 49 Alsebaey A. Allam N. Alswat K. et al. Normal liver stiffness: A study in living donors with normal liver histology. World J Hepatol 2015; 7: 1149-1153
  • 50 Popescu A. Sporea I. Sirli R. et al. The mean values of liver stiffness assessed by Acoustic Radiation Force Impulse elastography in normal subjects. Med Ultrason 2011; 13: 33-37
  • 51 Madhok R. Tapasvi C. Prasad U. et al. Acoustic radiation force impulse imaging of the liver: measurement of the normal mean values of the shearing wave velocity in a healthy liver. J Clin Diagn Res 2013; 7: 39-42
  • 52 Yun MH. Seo YS. Kang HS. et al. The effect of the respiratory cycle on liver stiffness values as measured by transient elastography. J Viral Hepat 2011; 18: 631-636
  • 53 Horster S. Mandel P. Zachoval R. et al. Comparing acoustic radiation force impulse imaging to transient elastography to assess liver stiffness in healthy volunteers with and without valsalva manoeuvre. Clin Hemorheol Microcirc 2010; 46: 159-168
  • 54 Grădinaru-Taşcău O. Sporea I. Bota S. et al. Does experience play a role in the ability to perform liver stiffness measurements by means of supersonic shear imaging (SSI)?. Med Ultrason 2013; 15: 180-183
  • 55 Sporea I. Bota S. Săftoiu A. et al. Romanian national guidelines and practical recommendations on liver elastography. Med Ultrason 2014; 16: 123-138
  • 56 Pellot-Barakat C. Lefort M. Chami L. et al. Automatic assessment of shear wave elastography quality and measurement reliability in the liver. Ultrasound Med Biol 2015; 41: 936-943
  • 57 Guzmán-Aroca F. Reus M. Berná-Serna JD. et al. Reproducibility of shear wave velocity measurements by acoustic radiation force impulse imaging of the liver: a study in healthy volunteers. J Ultrasound Med 2011; 30: 975-979
  • 58 Ferraioli G. Tinelli C. Lissandrin R. et al. Point shear wave elastography method for assessing liver stiffness. World J Gastroenterol 2014; 20: 4787-4796
  • 59 Ma JJ. Ding H. Mao F. et al. Assessment of liver fibrosis with elastography point quantification technique in chronic hepatitis B virus patients: a comparison with liver pathological results. J Gastroenterol Hepatol 2014; 29: 814-819
  • 60 Fraquelli M. Rigamonti C. Casazza G. et al. Reproducibility of transient elastography in the evaluation of liver fibrosis in patients with chronic liver disease. Gut 2007; 56: 968-973
  • 61 Boursier J. Konaté A. Gorea G. et al. Reproducibility of liver stiffness measurement by ultrasonographic elastometry. Clin Gastroenterol Hepatol 2008; 6: 1263-1269
  • 62 Cui XW. Pirri C. Ignee A. et al. Measurement of shear wave velocity using acoustic radiation force impulse imaging is not hampered by previous use of ultrasound contrast agents. Z Gastroenterol 2014; 52: 649-653
  • 63 Roulot D. Czernichow S. Le Clésiau H. et al. Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol 2008; 48 (04) 606-613
  • 64 Bende F. Sporea I. Sirli R. et al. Liver stiffness assessment in healthy subjects using 2D-Shear Wave Elastography implemented on GE LOGIQ E9. Athens: EUROSON 2015; 2015
  • 65 Son CY. Kim SU. Han WK. et al. Normal liver elasticity values using acoustic radiation force impulse imaging: a prospective study in healthy living liver and kidney donors. J Gastroenterol Hepatol 2012; 27: 130-136
  • 66 Raghuwanshi B. Jain N. Jain M. Normal values in healthy liver in central India by acoustic radiation force impulse imaging. J Clin Diagn Res 2013; 7: 2498-2501
  • 67 Lee MJ. Kim MJ. Han KH. et al. Age-related changes in liver, kidney, and spleen stiffness in healthy children measured with acoustic radiation force impulse imaging. Eur J Radiol 2013; 82: e290-e294
  • 68 Kim KM. Choi WB. Park SH. et al. Diagnosis of hepatic steatosis and fibrosis by transient elastography in asymptomatic healthy individuals: a prospective study of living related potential liver donors. J Gastroenterol 2007; 42: 382-388
  • 69 Fung J. Lee CK. Chan M. et al. Defining normal liver stiffness range in a normal healthy Chinese population without liver disease. PLoS One 2013; 8: e85067
  • 70 Fung J. Lai CL. Chan SC. et al. Correlation of liver stiffness and histological features in healthy persons and in patients with occult hepatitis B, chronic active hepatitis B, or hepatitis B cirrhosis. Am J Gastroenterol 2010; 105: 1116-1122
  • 71 Cournane S. Cannon L. Browne J. et al. Assessment of the accuracy of an ultrasound elastography liver scanning system using a pva-cryogel phantom with optimal acoustic and mechanical properties. Phys Med Biol 2010; 55: 5965-5983
  • 72 Melodelima D. Bamber JC. Duck FA. et al. Transient elastography using impulsive ultrasound radiation force: a preliminary comparison with surface palpation elastography. Ultrasound Med Biol 2007; 33: 959-969
  • 73 Oudry J. Chen J. Glaser KJ. et al. Cross-validation of magnetic resonance elastography and ultrasound-based transient elastography: a preliminary phantom study. J Magn Reson Imaging 2009; 30: 1145-1150
  • 74 Kishimoto R. Koyama A. Obata T. et al. Diagnostic reliability and validity of ultrasonographic tissue quantification using acoustic radiation force impulse (ARFI) elastography – phantom study. Chicago: Radiological Society of North America. Scientific Assembly and Annual Meeting; 2012
  • 75 Xie H. Shamdasani V. Zhao H. et al. A phantom study to cross-validate multimodality shear wave elastography techniques. Ultrasonics Symposium (IUS). Dresden: IEEE International; 2012: 1858-1861
  • 76 Sporea I. Sirli R. Deleanu A. et al. Liver stiffness measurement by transient elastography in clinical practice. J Gastrointestin Liver Dis 2008; 17: 395-399
  • 77 Pichon N. Loustaud-Ratti V. Clavel M. et al. Value of liver stiffness measured by transient elastography in the liver transplant pre-operative evaluation of the potential deceased liver donors: preliminary study. Clin Transplant 2011; 25: E205-E210
  • 78 Das K. Sarkar R. Ahmed SM. et al. "Normal" liver stiffness measure (LSM) values are higher in both lean and obese individuals: a population-based study from a developing country. Hepatology 2012; 55: 584-593
  • 79 Cho Y. Tokuhara D. Morikawa H. et al. Transient elastography-based liver profiles in a hospital-based pediatric population in Japan. PLoS One 2015; 10 (09) e0137239
  • 80 Wong GL. Chan HL. Choi PC. et al. Association between anthropometric parameters and measurements of liver stiffness by transient elastography. Clin Gastroenterol Hepatol 2013; 11: 295-302
  • 81 Gallotti A. D'Onofrio M. Pozzi Mucelli R. Acoustic Radiation Force Impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen. Radiol Med 2010; 115: 889-897
  • 82 Goertz RS. Amann K. Heide R. et al. An abdominal and thyroid status with Acoustic Radiation Force Impulse Elastometry-a feasibility study: Acoustic Radiation Force Impulse Elastometry of human organs. Eur J Radiol 2011; 80: e226-e230
  • 83 Kim JE. Lee JY. Kim YJ. 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
  • 84 Guzmán-Aroca F. Reus M. Berná-Serna JD. et al. Reproducibility of shear wave velocity measurements by acoustic radiation force impulse imaging of the liver: a study in healthy volunteers. J Ultrasound Med 2011; 30: 975-979
  • 85 Toshima T. Shirabe K. Takeishi K. et al. New method for assessing liver fibrosis based on acoustic radiation force impulse: a special reference to the difference between right and left liver. J Gastroenterol Hepatol 2011; 46: 705-711
  • 86 Rifai K. Cornberg J. Mederacke I. et al. Clinical feasibility of liver elastography by acoustic radiation force impulse imaging (ARFI). Dig Liver Dis 2011; 43: 491-497
  • 87 Motosugi U. Ichikawa T. Niitsuma Y. et al. Acoustic radiation force impulse elastography of the liver: can fat deposition in the liver affect the measurement of liver stiffness?. Jpn J Radiol 2011; 29: 639-643
  • 88 Jaffer OS. Lung PF. Bosanac D. et al. Acoustic radiation force impulse quantification: repeatability of measurements in selected liver segments and influence of age, body mass index and liver capsule-to-box distance. Br J Radiol 2012; 85: e858-e863
  • 89 Sporea I. Bota S. Grădinaru-Taşcău O. et al. Comparative study between two point Shear Wave Elastographic techniques: Acoustic Radiation Force Impulse (ARFI) elastography and ElastPQ. Med Ultrason 2014; 16: 309-314