Ultrasound Elastography for Characterization of Focal Liver Lesions

Yi Dong; Jonas Koch; Amjad Alhyari; Ehsan Safai Zadeh; Christian Görg; Wen-Ping Wang; Annalisa Berzigotti; Christoph F. Dietrich

doi:10.1055/a-1957-7370

Zeitschrift für Gastroenterologie, Table of Contents

Z Gastroenterol 2023; 61(04): 399-410
DOI: 10.1055/a-1957-7370

Übersicht

Ultrasound Elastography for Characterization of Focal Liver Lesions

Elastografie zur Charakterisierung von Lebertumoren

Authors

Yi Dong

¹Department of Ultrasound, Zhongshan Hospital Fudan University, Shanghai, China (Ringgold ID: RIN92323)

²Department of Ultrasound, Xinhua Hospital Affiliated to Shanghai Jiaotong University School of Medicine, Shanghai, China
Jonas Koch

³Department Allgemeine Innere Medizin, Kliniken (DAIM) Hirslanden Beau Site, Salem und Permanence, Bern, Switzerland
Amjad Alhyari

⁴Interdisciplinary Center of Ultrasound Diagnostics, University Hospital Giessen and Marburg, Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, Philipps University Marburg, Marburg, Germany (Ringgold ID: RIN61061)
Ehsan Safai Zadeh

⁴Interdisciplinary Center of Ultrasound Diagnostics, University Hospital Giessen and Marburg, Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, Philipps University Marburg, Marburg, Germany (Ringgold ID: RIN61061)
Christian Görg

⁴Interdisciplinary Center of Ultrasound Diagnostics, University Hospital Giessen and Marburg, Gastroenterology, Endocrinology, Metabolism and Clinical Infectiology, Philipps University Marburg, Marburg, Germany (Ringgold ID: RIN61061)
Wen-Ping Wang

¹Department of Ultrasound, Zhongshan Hospital Fudan University, Shanghai, China (Ringgold ID: RIN92323)
Annalisa Berzigotti

⁵Department of Visceral Surgery and Medicine, Bern University Hospital, University of Bern, Berne, Switzerland
Christoph F. Dietrich

³Department Allgemeine Innere Medizin, Kliniken (DAIM) Hirslanden Beau Site, Salem und Permanence, Bern, Switzerland

Abstract

Focal liver lesions (FLL) are typically detected by conventional ultrasound or other imaging modalities. After the detection of FLL, further characterization is essential, and this can be done by contrast-enhanced imaging techniques, e.g., contrast-enhanced ultrasound (CEUS) and magnetic resonance imaging (MRI) or by means of biopsy with histological evaluation. Elastographic techniques are nowadays integrated into high-end ultrasound systems and their value for the detection of severe liver fibrosis and cirrhosis has been shown in studies and meta-analyses. The use of an ultrasound elastographic technique for the differentiation of malignant and benign liver tumors is less well-established. This review summarizes the current data on utility and performance of ultrasound elastography for the characterization of FLL.

Zusammenfassung

Fokale Leberläsionen (FLL) werden typischerweise durch konventionellen Ultraschall oder andere bildgebende Verfahren detektiert. Eine weitere Charakterisierung erfolgt durch kontrastverstärkte bildgebende Verfahren, z. B. kontrastverstärkter Ultraschall (CEUS) und Magnetresonanztomografie (MRT), oder durch Biopsie mit histologischer Untersuchung. Elastografische Techniken werden heute routinemäßig in Ultraschallsysteme integriert und ihr Wert für die Erkennung der fortgeschrittenen Leberfibrose und -zirrhose wurde in Studien, Metaanalysen und Leitlinien belegt. Weniger etabliert ist der Einsatz elastografischer Techniken zur Differenzierung bösartiger und gutartiger Lebertumoren. Dieser Review fasst die aktuellen Daten zur Bedeutung der Ultraschall-Elastografie zur Charakterisierung von FLL zusammen.

Schlüsselwörter

Elastografie - fokale Leberläsionen - Lebertumoren - Steifheit - Ultraschall

Keywords

Elastography - focal liver lesions - liver tumors - stiffness - Ultrasound

Full Text

References

References
1 Chiorean L, Tana C, Braden B. et al. Advantages and Limitations of Focal Liver Lesion Assessment with Ultrasound Contrast Agents: Comments on the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) Guidelines. Med Princ Pract 2016; 25: 399-407
2 Chiorean L, Caraiani C, Radzina M. et al. Vascular phases in imaging and their role in focal liver lesions assessment. Clin Hemorheol Microcirc 2015; 62: 299-326
3 Dietrich CF, Bamber J, Berzigotti A. et al. EFSUMB Guidelines and Recommendations on the Clinical Use of Liver Ultrasound Elastography, Update 2017 (Long Version). Ultraschall in der Medizin 2017; 38: e16-e47
4 Dietrich CF, Bamber J, Berzigotti A. et al. EFSUMB Guidelines and Recommendations on the Clinical Use of Liver Ultrasound Elastography, Update 2017 (Short Version). Ultraschall in der Medizin 2017; 38: 377-394
5 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 der Medizin 2013; 34: 238-253
6 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 der Medizin 2013; 34: 169-184
7 Barr RG, Cosgrove D, Brock M. et al. WFUMB Guidelines and Recommendations on the Clinical Use of Ultrasound Elastography: Part 5. Prostate. Ultrasound Med Biol 2017; 43: 27-48
8 Cosgrove D, Barr R, Bojunga J. et al. WFUMB Guidelines and Recommendations on the Clinical Use of Ultrasound Elastography: Part 4. Thyroid. Ultrasound Med Biol 2017; 43: 4-26
9 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
10 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
11 Hu X, Liu Y, Qian L. Diagnostic potential of real-time elastography (RTE) and shear wave elastography (SWE) to differentiate benign and malignant thyroid nodules: A systematic review and meta-analysis. Medicine 2017; 96: e8282
12 Dong FJ, Li M, Jiao Y. et al. Acoustic Radiation Force Impulse imaging for detecting thyroid nodules: a systematic review and pooled meta-analysis. Medical Ultrasonography 2015; 17: 192-199
13 Kono Y, Lyshchik A, Cosgrove D. et al. Contrast Enhanced Ultrasound (CEUS) Liver Imaging Reporting and Data System (LI-RADS(R)): the official version by the American College of Radiology (ACR). Ultraschall in der Medizin 2017; 38: 85-86
14 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
15 Dighe M, Barr R, Bojunga J. et al. Thyroid Ultrasound: State of the Art: Part 1 – Thyroid Ultrasound reporting and Diffuse Thyroid Diseases. Medical Ultrasonography 2017; 19: 79-93
16 Kapoor A, Kapoor A, Mahajan G. et al. Real-time elastography in differentiating metastatic from nonmetastatic liver nodules. Ultrasound Med Biol 2011; 37: 207-213
17 Tian W, Hao S, Gao B. et al. Comparing the Diagnostic Accuracy of RTE and SWE in Differentiating Malignant Thyroid Nodules from Benign Ones: a Meta-Analysis. Cellular physiology and biochemistry. International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology 2016; 39: 2451-2463
18 Zhang B, Ma X, Zhan W. et al. Real-time elastography in the diagnosis of patients suspected of having prostate cancer: a meta-analysis. Ultrasound Med Biol 2014; 40: 1400-1407
19 Aboumarzouk OM, Ogston S, Huang Z. et al. Diagnostic accuracy of transrectal elastosonography (TRES) imaging for the diagnosis of prostate cancer: a systematic review and meta-analysis. BJU International 2012; 110: 1414-1423
20 Friedrich-Rust M, Vorlaender C, Dietrich CF. et al. Evaluation of Strain Elastography for Differentiation of Thyroid Nodules: Results of a Prospective DEGUM Multicenter Study. Ultraschall in der Medizin 2016; 37: 262-270
21 Onur MR, Poyraz AK, Ucak EE. et al. Semiquantitative strain elastography of liver masses. Journal of ultrasound in medicine. Official Journal of the American Institute of Ultrasound in Medicine 2012; 31: 1061-1067
22 Cesario V, Accogli E, Domanico A. et al. Percutaneous real-time sonoelastography as a non-invasive tool for the characterization of solid focal liver lesions: A prospective study. Digestive and liver disease. Official Journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver 2016; 48: 182-188
23 Dong Y, Sirli R, Ferraioli G. et al. Shear wave elastography of the liver – review on normal values. Z Gastroenterol 2017; 55: 153-166
24 Dietrich CF, Maurer M, Riemer-Hommel P. Challenges for the German Health Care System – Pharmaceuticals. Endheu 2014; 27: 45-53
25 Dietrich CF, Riemer-Hommel P. Challenges for the German Health Care System. ZGastroenterol 2012; 50: 557-572
26 Dietrich CF, Rosien U, Caspary WF. Diagnosis related groups (DRG)--current significance in gastroenterology. Z Gastroenterol 2001; 39: 357-363
27 Heide R, Strobel D, Bernatik T. et al. Characterization of focal liver lesions (FLL) with acoustic radiation force impulse (ARFI) elastometry. Ultraschall in der Medizin 2010; 31: 405-409
28 Frulio N, Laumonier H, Carteret T. et al. Evaluation of liver tumors using acoustic radiation force impulse elastography and correlation with histologic data. Journal of ultrasound in medicine. Official Journal of the American Institute of Ultrasound in Medicine 2013; 32: 121-130
29 Guo LH, Wang SJ, Xu HX. et al. Differentiation of benign and malignant focal liver lesions: value of virtual touch tissue quantification of acoustic radiation force impulse elastography. Medical Oncology 2015; 32: 68
30 Zhang P, Zhou P, Tian SM. et al. Diagnostic performance of contrast-enhanced sonography and acoustic radiation force impulse imaging in solid liver lesions. Journal of ultrasound in medicine. Official Journal of the American Institute of Ultrasound in Medicine 2014; 33: 205-214
31 Park H, Park JY, Kim DY. et al. Characterization of focal liver masses using acoustic radiation force impulse elastography. World Journal of Gastroenterology 2013; 19: 219-226
32 Cho SH, Lee JY, Han JK. et al. Acoustic radiation force impulse elastography for the evaluation of focal solid hepatic lesions: preliminary findings. Ultrasound Med Biol 2010; 36: 202-208
33 Davies G, Koenen M. Acoustic radiation force impulse elastography in distinguishing hepatic haemangiomata from metastases: preliminary observations. The British Journal of Radiology 2011; 84: 939-943
34 Gallotti A, D’Onofrio M, Romanini L. et al. Acoustic Radiation Force Impulse (ARFI) ultrasound imaging of solid focal liver lesions. European Journal of Radiology 2012; 81: 451-455
35 Goya C, Hamidi C, Yavuz A. et al. The Role of Acoustic Radiation Force Impulse Elastography in the Differentiation of Infectious and Neoplastic Liver Lesions. Ultrasonic Imaging 2015; 37: 312-322
36 Ying L, Lin X, Xie ZL. et al. Clinical utility of acoustic radiation force impulse imaging for identification of malignant liver lesions: a meta-analysis. European Radiology 2012; 22: 2798-2805
37 Dong Y, Wang WP, Xu Y. et al. Point shear wave speed measurement in differentiating benign and malignant focal liver lesions. Medical Ultrasonography 2017; 19: 259-264
38 Gerber L, Fitting D, Srikantharajah K. et al. Evaluation of 2D- Shear Wave Elastography for Characterisation of Focal Liver Lesions. Journal of Gastrointestinal and Liver Diseases : JGLD 2017; 26: 283-290
39 de Ledinghen V, Vergniol J, Capdepont M. et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. Journal of Hepatology 2014; 60: 1026-1031
40 Guibal A, Boularan C, Bruce M. et al. Evaluation of shearwave elastography for the characterisation of focal liver lesions on ultrasound. European Radiology 2013; 23: 1138-1149
41 Grgurevic I, Bokun T, Salkic NN. et al. Liver elastography malignancy prediction score for noninvasive characterization of focal liver lesions. Liver international. Official Journal of the International Association for the Study of the Liver 2017;
42 Jiao Y, Dong F, Wang H. et al. Shear wave elastography imaging for detecting malignant lesions of the liver: a systematic review and pooled meta-analysis. Medical Ultrasonography 2017; 19: 16-22
43 Dietrich CF, Mertens JC, Braden B. et al. Contrast-enhanced ultrasound of histologically proven liver hemangiomas. Hepatology 2007; 45: 1139-1145
44 Dong Y, Wang WP, Cantisani V. et al. Contrast-enhanced ultrasound of histologically proven hepatic epithelioid hemangioendothelioma. World Journal of Gastroenterology 2016; 22: 4741-4749
45 Trojan J, Hammerstingl R, Engels K. et al. Contrast-enhanced ultrasound in the diagnosis of malignant mesenchymal liver tumors. J Clin Ultrasound 2010; 38: 227-231
46 Claudon M, Dietrich CF, Choi BI. et al. Guidelines and good clinical practice recommendations for Contrast Enhanced Ultrasound (CEUS) in the liver – update 2012: A WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultrasound Med Biol 2013; 39: 187-210
47 Claudon M, Dietrich CF, Choi BI. et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver--update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultraschall in der Medizin 2013; 34: 11-29
48 Kim JE, Lee JY, Bae KS. et al. Acoustic radiation force impulse elastography for focal hepatic tumors: usefulness for differentiating hemangiomas from malignant tumors. Korean Journal of Radiology 2013; 14: 743-753
49 Dietrich CF, Schuessler G, Trojan J. et al. Differentiation of focal nodular hyperplasia and hepatocellular adenoma by contrast-enhanced ultrasound. The British Journal of Radiology 2005; 78: 704-707
50 Dietrich CF, Ignee A, Trojan J. et al. Improved characterisation of histologically proven liver tumours by contrast enhanced ultrasonography during the portal venous and specific late phase of SHU 508A. Gut 2004; 53: 401-405
51 Ronot M, Di Renzo S, Gregoli B. et al. Characterization of fortuitously discovered focal liver lesions: additional information provided by shearwave elastography. European Radiology 2015; 25: 346-358
52 Brunel T, Guibal A, Boularan C. et al. Focal nodular hyperplasia and hepatocellular adenoma: The value of shear wave elastography for differential diagnosis. European Journal of Radiology 2015; 84: 2059-2064
53 Lu Q, Ling W, Lu C. et al. Hepatocellular carcinoma: stiffness value and ratio to discriminate malignant from benign focal liver lesions. Radiology 2015; 275: 880-888
54 Ling W, Lu Q, Lu C. et al. Effects of vascularity and differentiation of hepatocellular carcinoma on tumor and liver stiffness: in vivo and in vitro studies. Ultrasound Med Biol 2014; 40: 739-746
55 Honjo M, Moriyasu F, Sugimoto K. et al. Relationship between the liver tissue shear modulus and histopathologic findings analyzed by intraoperative shear wave elastography and digital microscopically assisted morphometry in patients with hepatocellular carcinoma. Journal of ultrasound in medicine. Official Journal of the American Institute of Ultrasound in Medicine 2014; 33: 61-71
56 Kang J, Kwon H, Cho J. et al. Comparative study of shear wave velocities using acoustic radiation force impulse technology in hepatocellular carcinoma: the extent of radiofrequency ablation. Gut and Liver 2012; 6: 362-367
57 Park HS, Kim YJ, Yu MH. et al. Shear Wave Elastography of Focal Liver Lesion: Intraobserver Reproducibility and Elasticity Characterization. Ultrasound Quarterly 2015; 31: 262-271