Abstract
Objectives
To prospectively assess the stiffness of incidentally discovered focal liver lesions (FLL) with no history of chronic liver disease or extrahepatic cancer using shearwave elastography (SWE).
Methods
Between June 2011 and May 2012, all FLL fortuitously discovered on ultrasound examination were prospectively included. For each lesion, stiffness was measured (kPa). Characterization of the lesion relied on magnetic resonance imaging (MRI) and/or contrast-enhanced ultrasound, or biopsy. Tumour stiffness was analysed using ANOVA and non-parametric Mann-Whitney tests.
Results
105 lesions were successfully evaluated in 73 patients (61 women, 84 %) with a mean age of 44.8 (range: 20‒75). The mean stiffness was 33.3 ± 12.7 kPa for the 60 focal nodular hyperplasia (FNH), 19.7 ± 9.8 k Pa for the 17 hepatocellular adenomas (HCA), 17.1 ± 7 kPa for the 20 haemangiomas, 11.3 ± 4.3 kPa for the five focal fatty sparing, 34.1 ± 7.3 kPa for the two cholangiocarcinomas, and 19.6 kPa for one hepatocellular carcinoma (p < 0.0001). There was no difference between the benign and the malignant groups (p = 0.64). FNHs were significantly stiffer than HCAs (p < 0.0001). Telangiectatic/inflammatory HCAs were significantly stiffer than the steatotic HCAs (p = 0.014). The area under the ROC curve (AUROC) for differentiating FNH from other lesions was 0.86 ± 0.04.
Conclusion
SWE may provide additional information for the characterization of FFL, and may help in differentiating FNH from HCAs, and in subtyping HCAs.
Key Points
• SWE might be helpful for the characterization of solid focal liver lesions
• SWE cannot differentiate benign from malignant liver lesions
• FNHs are significantly stiffer than other benign lesions
• Telangiectatic/inflammatory HCA are significantly stiffer than steatotic ones
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Abbreviations
- ARFI:
-
acoustic radiation force impulse imaging
- CEUS:
-
contrast-enhanced ultrasound
- CT:
-
computed tomography
- FFS:
-
focal fatty sparing
- FLL:
-
focal liver lesion
- FNH:
-
focal nodular hyperplasia
- tHCA or sHCA:
-
telangiectatic/inflammatory or steatotic hepatocellular adenoma
- HCC:
-
hepatocellular carcinoma
- ICC:
-
intrahepatic cholangiocarcinoma
- MRI:
-
magnetic resonance imaging
- ROI:
-
region of interest
- SWE:
-
shearwave elastography
- US:
-
ultrasound
References
Reddy KR, Kligerman S, Levi J et al (2001) Benign and solid tumors of the liver: relationship to sex, age, size of tumors, and outcome. Am Surg 67:173–178
Vilgrain V (2006) Focal nodular hyperplasia. Eur J Radiol 58:236–245
Dokmak S, Paradis V, Vilgrain V et al (2009) A Single-Center Surgical Experience of 122 Patients With Single and Multiple Hepatocellular Adenomas. Gastroenterology 137:1698–1705
Harvey CJ, Albrecht T (2001) Ultrasound of focal liver lesions. Eur Radiol 11:1578–1593
Noone TC, Semelka RC, Chaney DM, Reinhold C (2004) Abdominal imaging studies: comparison of diagnostic accuracies resulting from ultrasound, computed tomography, and magnetic resonance imaging in the same individual. Magn Reson Imaging 22:19–24
Holzapfel K, Bruegel M, Eiber M et al (2010) Characterization of small (</=10 mm) focal liver lesions: value of respiratory-triggered echo-planar diffusion-weighted MR imaging. Eur J Radiol 76:89–95
Holzapfel K, Eiber MJ, Fingerle AA, Bruegel M, Rummeny EJ, Gaa J (2012) Detection, classification, and characterization of focal liver lesions: Value of diffusion-weighted MR imaging, gadoxetic acid-enhanced MR imaging and the combination of both methods. Abdom Imaging 37:74–82
Agnello F, Ronot M, Valla DC, Sinkus R, Van Beers BE, Vilgrain V (2012) High-b-value diffusion-weighted MR imaging of benign hepatocellular lesions: quantitative and qualitative analysis. Radiology 262:511–519
Tranquart F, Correas JM, Ladam Marcus V et al (2009) Real-time contrast-enhanced ultrasound in the evaluation of focal liver lesions: diagnostic efficacy and economical issues from a French multicentric study. J Radiol 90:109–122
Wang ZL, Tang J, Weskott HP et al (2008) Undetermined focal liver lesions on gray-scale ultrasound in patients with fatty liver: characterization with contrast-enhanced ultrasound. J Gastroenterol Hepatol 23:1511–1519
Quaia E, Calliada F, Bertolotto M et al (2004) Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: diagnostic performance and confidence. Radiology 232:420–430
Quaia E, Stacul F, Gaiani S et al (2004) Comparison of diagnostic performance of unenhanced vs SonoVue - enhanced ultrasonography in focal liver lesions characterization. The experience of three Italian centers. Radiol Med 108:71–81
Laumonier H, Bioulac-Sage P, Laurent C, Zucman-Rossi J, Balabaud C, Trillaud H (2008) Hepatocellular adenomas: magnetic resonance imaging features as a function of molecular pathological classification. Hepatology 48:808–818
Ronot M, Bahrami S, Calderaro J et al (2011) Hepatocellular adenomas: accuracy of magnetic resonance imaging and liver biopsy in subtype classification. Hepatology 53:1182–1191
Semelka RC, Sofka CM (1997) Hepatic hemangiomas. Magn Reson Imaging Clin N Am 5:241–253
Soussan M, Aubé C, Bahrami S, Boursier J, Valla DC, Vilgrain V (2010) Incidental focal solid liver lesions: diagnostic performance of contrast-enhanced ultrasound and MR imaging. Eur Radiol 20:1715–1725
Hussain SM, Semelka RC (2005) Hepatic imaging: comparison of modalities. Radiol Clin North Am 43:929–947, ix
Semelka RC, Worawattanakul S, Kelekis NL et al (1997) Liver lesion detection, characterization, and effect on patient management: comparison of single-phase spiral CT and current MR techniques. J Magn Reson Imaging 7:1040–1047
Holalkere NS, Sahani DV, Blake MA, Halpern EF, Hahn PF, Mueller PR (2006) Characterization of small liver lesions: Added role of MR after MDCT. J Comput Assist Tomogr 30:591–596
Ladam-Marcus V, Mac G, Job L, Piot-Veron S, Marcus C, Hoeffel C (2009) Contrast-enhanced ultrasound and liver imaging: review of the literature. J Radiol 90:93–106, quiz 107-108
Friedrich-Rust M, Klopffleisch T, Nierhoff J et al (2013) Contrast-Enhanced Ultrasound for the differentiation of benign and malignant focal liver lesions: a meta-analysis. Liver Int. doi:10.1111/liv.12115
Grazioli L, Bondioni M, Haradome H (2012) Hepatocellular Adenoma and Focal Nodular Hyperplasia: Value of Gadoxetic Acid–enhanced MR Imaging in Differential Diagnosis. Radiol
Ronot M, Paradis V, Duran R et al (2012) MR findings of steatotic focal nodular hyperplasia and comparison with other fatty tumours. Eur Radiol. doi:10.1007/s00330-012-2676-y
Yoneda N, Matsui O, Kitao A et al (2012) Beta-catenin-activated hepatocellular adenoma showing hyperintensity on hepatobiliary-phase gadoxetic-enhanced magnetic resonance imaging and overexpression of OATP8. Jpn J Radiol 30:777–782
Thomeer MG, Willemssen FE, Biermann KK et al (2013) MRI features of inflammatory hepatocellular adenomas on hepatocyte phase imaging with liver-specific contrast agents. J Magn Reson Imaging. doi:10.1002/jmri.24281
Purysko AS, Remer EM, Coppa CP, Obuchowski NA, Schneider E, Veniero JC (2012) Characteristics and distinguishing features of hepatocellular adenoma and focal nodular hyperplasia on gadoxetate disodium-enhanced MRI. Am J Roentgenol 198:115–123
Grieser C, Steffen IG, Kramme IB et al (2014) Gadoxetic acid enhanced MRI for differentiation of FNH and HCA: a single centre experience. Eur Radiol. doi:10.1007/s00330-014-3144-7
Garteiser P, Doblas S, Daire JL et al (2012) MR elastography of liver tumours: value of viscoelastic properties for tumour characterisation. Eur Radiol 22:2169–2177
Van Beers BE, Doblas S, Sinkus R (2012) New acquisition techniques: fields of application. Abdom Imaging 37:155–163
Sandrin L, Fourquet B, Hasquenoph JM et al (2003) Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol 29:1705–1713
Castera L, Vergniol J, Foucher J et al (2005) Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 128:343–350
Ziol M, Handra-Luca A, Kettaneh A et al (2005) Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology 41:48–54
Castera L (2012) Noninvasive methods to assess liver disease in patients with hepatitis B or C. Gastroenterology 142(1293–1302):e1294
Masuzaki R, Tateishi R, Yoshida H et al (2007) Assessing liver tumor stiffness by transient elastography. Hepatol Int 1:394–397
Fahey BJ, Nightingale KR, Nelson RC, Palmeri ML, Trahey GE (2005) Acoustic radiation force impulse imaging of the abdomen: demonstration of feasibility and utility. Ultrasound Med Biol 31:1185–1198
Bercoff J, Tanter M, Fink M (2004) Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 51:396–409
Cho SH, Lee JY, Han JK, Choi BI (2010) Acoustic radiation force impulse elastography for the evaluation of focal solid hepatic lesions: preliminary findings. Ultrasound Med Biol 36:202–208
Heide R, Strobel D, Bernatik T, Goertz RS (2010) Characterization of focal liver lesions (FLL) with acoustic radiation force impulse (ARFI) elastometry. Ultraschall Med 31:405–409
Gallotti A, D'Onofrio M, Romanini L, Cantisani V, Pozzi Mucelli R (2012) Acoustic Radiation Force Impulse (ARFI) ultrasound imaging of solid focal liver lesions. Eur J Radiol 81:451–455
Davies G, Koenen M (2011) Acoustic radiation force impulse elastography in distinguishing hepatic haemangiomata from metastases: preliminary observations. Br J Radiol 84:939–943
Zhang P, Zhou P, Tian SM, Qian Y, Deng J, Zhang L (2013) Application of acoustic radiation force impulse imaging for the evaluation of focal liver lesion elasticity. Hepatobiliary Pancreat Dis Int 12:165–170
Park H, Park JY, Do Kim Y et al (2013) Characterization of focal liver masses using acoustic radiation force impulse elastography. World J Gastroenterol 19:219–226
Frulio N, Laumonier H, Carteret T et al (2013) Evaluation of liver tumors using acoustic radiation force impulse elastography and correlation with histologic data. J Ultrasound Med 32:121–130
Yu H, Wilson SR (2011) Differentiation of benign from malignant liver masses with Acoustic Radiation Force Impulse technique. Ultrasound Q 27:217–223
Cosgrove D, Piscaglia F, Bamber J et al (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med 34:238–253
Ishak K, Baptista A, Bianchi L et al (1995) Histological grading and staging of chronic hepatitis. J Hepatol 22:696–699
Guibal A, Boularan C, Bruce M et al (2012) Evaluation of shearwave elastography for the characterisation of focal liver lesions on ultrasound. Eur Radiol. doi:10.1007/s00330-012-2692-y
Hata S, Imamura H, Aoki T et al (2011) Value of visual inspection, bimanual palpation, and intraoperative ultrasonography during hepatic resection for liver metastases of colorectal carcinoma. World J Surg 35:2779–2787
Ying L, Hou Y, Zheng HM, Lin X, Xie ZL, Hu YP (2012) Real-time elastography for the differentiation of benign and malignant superficial lymph nodes: a meta-analysis. Eur J Radiol 81:2576–2584
Bioulac-Sage P, Balabaud C, Bedossa P et al (2007) Pathological diagnosis of liver cell adenoma and focal nodular hyperplasia: Bordeaux update. J Hepatol 46:521–527
Bioulac-Sage P, Laumonier H, Couchy G, et al. (2009) Hepatocellular Adenoma Management and Phenotypic Classification: the Bordeaux Experience. Hepatol: 1-9
Mannelli L, Wilson GJ, Dubinsky TJ et al (2012) Assessment of the liver strain among cirrhotic and normal livers using tagged MRI. J Magn Reson Imaging 36:1490–1495
Venkatesh SK, Yin M, Ehman RL (2013) Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 37:544–555
Huwart L, Salameh N, ter Beek L et al (2008) MR elastography of liver fibrosis: preliminary results comparing spin-echo and echo-planar imaging. Eur Radiol 18:2535–2541
Acknowledgments
The scientific guarantor of this publication is Valérie Vilgrain. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: prospective, diagnostic, or prognostic study, performed at one institution.
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Ronot, M., Di Renzo, S., Gregoli, B. et al. Characterization of fortuitously discovered focal liver lesions: additional information provided by shearwave elastography. Eur Radiol 25, 346–358 (2015). https://doi.org/10.1007/s00330-014-3370-z
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DOI: https://doi.org/10.1007/s00330-014-3370-z