Skip to main content
Top
Published in: European Radiology 2/2019

01-02-2019 | Gastrointestinal

Magnetic resonance elastography can predict development of hepatocellular carcinoma with longitudinally acquired two-point data

Authors: Shintaro Ichikawa, Utaroh Motosugi, Nobuyuki Enomoto, Hiroshi Onishi

Published in: European Radiology | Issue 2/2019

Login to get access

Abstract

Objective

To evaluate the usefulness of longitudinal observation of liver stiffness measured using magnetic resonance elastography (MRE) to stratify the risk of hepatocellular carcinoma (HCC) in patients with chronic liver disease.

Materials and methods

We retrospectively reviewed data for 161 patients with chronic liver disease using the following inclusion criteria: two MRE examinations separated by at least a 12-month interval, no history of HCC, no development of HCC between the two examinations and availability of laboratory results. Liver stiffness was classified as low (< 3 kPa), moderate (3–4.7 kPa) or high (> 4.7 kPa). The patients were divided into three groups according to sequential changes in liver stiffness as follows: high on the first MRE (group A, n = 60), low on both MRE examinations (group C, n = 36) and other combinations (group B, n = 65). Cox analyses and Kaplan-Meier methods were used to determine the risk of developing HCC.

Results

Forty-seven patients (29.2%) developed HCC during follow-up (46.7% [28/60] in group A, 26.2% [17/65] in group B, and 5.6% [2/36] in group C). There was a significant difference in the rate of development of HCC between groups A (45.1%), B (26.1%) and C (12.4%) at 3 years (p = 0.0002). The independent risk factors for development of HCC were group A classification, age and a high alanine aminotransferase level (risk ratio 1.018–6.030; p = 0.0028–0.0268).

Conclusion

Longitudinal observation of liver stiffness using MRE can stratify the risk of HCC during follow-up of chronic liver disease.

Key Points

• The results of MRE can stratify the risk for development of HCC during follow-up in patients with chronic liver disease.
• Patients with chronic liver disease and high liver stiffness (> 4.7 kPa) on a previous MRE examination are at high risk for developing HCC, regardless of current liver stiffness.
• Management of patients with chronic liver disease becomes more appropriate using longitudinally acquired two-point MRE data.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wong VW, Janssen HL (2015) Can we use HCC risk scores to individualize surveillance in chronic hepatitis B infection? J Hepatol 63:722–732CrossRefPubMed Wong VW, Janssen HL (2015) Can we use HCC risk scores to individualize surveillance in chronic hepatitis B infection? J Hepatol 63:722–732CrossRefPubMed
2.
go back to reference Sugino Y, Yamakado K, Yamanaka T et al (2017) Role of curative treatment in patients with intermediate-stage hepatocellular carcinoma. Jpn J Radiol 35:254–261CrossRefPubMed Sugino Y, Yamakado K, Yamanaka T et al (2017) Role of curative treatment in patients with intermediate-stage hepatocellular carcinoma. Jpn J Radiol 35:254–261CrossRefPubMed
3.
go back to reference Takyar V, Etzion O, Heller T et al (2017) Complications of percutaneous liver biopsy with Klatskin needles: a 36-year single-centre experience. Aliment Pharmacol Ther 45:744–753CrossRefPubMedPubMedCentral Takyar V, Etzion O, Heller T et al (2017) Complications of percutaneous liver biopsy with Klatskin needles: a 36-year single-centre experience. Aliment Pharmacol Ther 45:744–753CrossRefPubMedPubMedCentral
4.
go back to reference Chindamo MC, Nunes-Pannain VL, Araújo-Neto JM et al (2015) Intermediate fibrosis staging in hepatitis C: a problem not overcome by optimal samples or pathologists' expertise. Ann Hepatol 14:652–657PubMed Chindamo MC, Nunes-Pannain VL, Araújo-Neto JM et al (2015) Intermediate fibrosis staging in hepatitis C: a problem not overcome by optimal samples or pathologists' expertise. Ann Hepatol 14:652–657PubMed
5.
go back to reference Huang Z, Zheng W, Zhang YJ et al (2017) Assessing hepatic fibrosis using 2-D shear wave elastography in patients with liver tumors: a prospective single-center study. Ultrasound Med Biol 43:2522–2529CrossRefPubMed Huang Z, Zheng W, Zhang YJ et al (2017) Assessing hepatic fibrosis using 2-D shear wave elastography in patients with liver tumors: a prospective single-center study. Ultrasound Med Biol 43:2522–2529CrossRefPubMed
6.
go back to reference Wang T, Shao C, Zhang G, Xu Y (2017) Real-time elastography (RTE): a valuable sonography-based non-invasive method for the assessment of liver fibrosis in chronic hepatitis B. Abdom Radiol (NY) 42:2632–2638CrossRef Wang T, Shao C, Zhang G, Xu Y (2017) Real-time elastography (RTE): a valuable sonography-based non-invasive method for the assessment of liver fibrosis in chronic hepatitis B. Abdom Radiol (NY) 42:2632–2638CrossRef
7.
go back to reference Masuzaki R, Tateishi R, Yoshida H et al (2008) Risk assessment of hepatocellular carcinoma in chronic hepatitis C patients by transient elastography. J Clin Gastroenterol 42:839–843CrossRefPubMed Masuzaki R, Tateishi R, Yoshida H et al (2008) Risk assessment of hepatocellular carcinoma in chronic hepatitis C patients by transient elastography. J Clin Gastroenterol 42:839–843CrossRefPubMed
8.
go back to reference Park MS, Han KH, Kim SU (2014) Non-invasive prediction of development of hepatocellular carcinoma using transient elastography in patients with chronic liver disease. Expert Rev Gastroenterol Hepatol 8:501–511CrossRefPubMed Park MS, Han KH, Kim SU (2014) Non-invasive prediction of development of hepatocellular carcinoma using transient elastography in patients with chronic liver disease. Expert Rev Gastroenterol Hepatol 8:501–511CrossRefPubMed
9.
go back to reference Ichikawa S, Motosugi U, Enomoto N, Matsuda M, Onishi H (2017) Noninvasive hepatic fibrosis staging using MR elastography: the usefulness of the bayesian prediction method. J Magn Reson Imaging 46:375–382CrossRefPubMed Ichikawa S, Motosugi U, Enomoto N, Matsuda M, Onishi H (2017) Noninvasive hepatic fibrosis staging using MR elastography: the usefulness of the bayesian prediction method. J Magn Reson Imaging 46:375–382CrossRefPubMed
10.
go back to reference Yin M, Glaser KJ, Talwalkar JA, Chen J, Manduca A, Ehman RL (2016) Hepatic MR elastography: clinical performance in a series of 1377 consecutive examinations. Radiology 278:114–124CrossRefPubMed Yin M, Glaser KJ, Talwalkar JA, Chen J, Manduca A, Ehman RL (2016) Hepatic MR elastography: clinical performance in a series of 1377 consecutive examinations. Radiology 278:114–124CrossRefPubMed
11.
go back to reference Kim SU, Kim BK, Park JY et al (2016) Transient elastography is superior to FIB-4 in assessing the risk of hepatocellular carcinoma in patients with chronic hepatitis B. Medicine (Baltimore) 95:e3434CrossRef Kim SU, Kim BK, Park JY et al (2016) Transient elastography is superior to FIB-4 in assessing the risk of hepatocellular carcinoma in patients with chronic hepatitis B. Medicine (Baltimore) 95:e3434CrossRef
12.
go back to reference Motosugi U, Ichikawa T, Koshiishi T et al (2013) Liver stiffness measured by magnetic resonance elastography as a risk factor for hepatocellular carcinoma: a preliminary case-control study. Eur Radiol 23:156–162CrossRefPubMed Motosugi U, Ichikawa T, Koshiishi T et al (2013) Liver stiffness measured by magnetic resonance elastography as a risk factor for hepatocellular carcinoma: a preliminary case-control study. Eur Radiol 23:156–162CrossRefPubMed
13.
go back to reference Heimbach JK, Kulik LM, Finn RS et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380CrossRefPubMed Heimbach JK, Kulik LM, Finn RS et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380CrossRefPubMed
15.
go back to reference Rouviere O, Yin M, Dresner MA et al (2006) MR elastography of the liver: preliminary results. Radiology 240:440–448CrossRefPubMed Rouviere O, Yin M, Dresner MA et al (2006) MR elastography of the liver: preliminary results. Radiology 240:440–448CrossRefPubMed
16.
go back to reference Yin M, Talwalkar JA, Glaser KJ et al (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5:1207–1213.e2CrossRefPubMedPubMedCentral Yin M, Talwalkar JA, Glaser KJ et al (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5:1207–1213.e2CrossRefPubMedPubMedCentral
17.
go back to reference Manduca A, Oliphant TE, Dresner MA et al (2001) Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal 5:237–254CrossRefPubMed Manduca A, Oliphant TE, Dresner MA et al (2001) Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal 5:237–254CrossRefPubMed
18.
go back to reference Talwalkar JA, Yin M, Venkatesh S et al (2009) Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension. AJR Am J Roentgenol 193:122–127CrossRefPubMedPubMedCentral Talwalkar JA, Yin M, Venkatesh S et al (2009) Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension. AJR Am J Roentgenol 193:122–127CrossRefPubMedPubMedCentral
19.
go back to reference Wang JH, Chuah SK, Lu SN et al (2014) Baseline and serial liver stiffness measurement in prediction of portal hypertension progression for patients with compensated cirrhosis. Liver Int 34:1340–1348CrossRefPubMed Wang JH, Chuah SK, Lu SN et al (2014) Baseline and serial liver stiffness measurement in prediction of portal hypertension progression for patients with compensated cirrhosis. Liver Int 34:1340–1348CrossRefPubMed
20.
go back to reference Coulon S, Heindryckx F, Geerts A, Van Steenkiste C, Colle I, Van Vlierberghe H (2011) Angiogenesis in chronic liver disease and its complications. Liver Int 31:146–162CrossRefPubMed Coulon S, Heindryckx F, Geerts A, Van Steenkiste C, Colle I, Van Vlierberghe H (2011) Angiogenesis in chronic liver disease and its complications. Liver Int 31:146–162CrossRefPubMed
21.
go back to reference Machado MV, Cortez-Pinto H (2015) Proangiogenic factors in the development of HCC in alcoholic cirrhosis. Clin Res Gastroenterol Hepatol 39(Suppl 1):S104–S108CrossRef Machado MV, Cortez-Pinto H (2015) Proangiogenic factors in the development of HCC in alcoholic cirrhosis. Clin Res Gastroenterol Hepatol 39(Suppl 1):S104–S108CrossRef
22.
23.
go back to reference Guo J, Büning C, Schott E et al (2015) In vivo abdominal magnetic resonance elastography for the assessment of portal hypertension before and after transjugular intrahepatic portosystemic shunt implantation. Invest Radiol 50:347–351CrossRefPubMed Guo J, Büning C, Schott E et al (2015) In vivo abdominal magnetic resonance elastography for the assessment of portal hypertension before and after transjugular intrahepatic portosystemic shunt implantation. Invest Radiol 50:347–351CrossRefPubMed
24.
go back to reference Morisaka H, Motosugi U, Ichikawa S et al (2015) Association of splenic MR elastographic findings with gastroesophageal varices in patients with chronic liver disease. J Magn Reson Imaging 41:117–124CrossRefPubMed Morisaka H, Motosugi U, Ichikawa S et al (2015) Association of splenic MR elastographic findings with gastroesophageal varices in patients with chronic liver disease. J Magn Reson Imaging 41:117–124CrossRefPubMed
25.
go back to reference Asrani SK, Talwalkar JA, Kamath PS et al (2014) Role of magnetic resonance elastography in compensated and decompensated liver disease. J Hepatol 60:934–939CrossRefPubMed Asrani SK, Talwalkar JA, Kamath PS et al (2014) Role of magnetic resonance elastography in compensated and decompensated liver disease. J Hepatol 60:934–939CrossRefPubMed
26.
go back to reference Takamura T, Motosugi U, Ichikawa S et al (2016) Usefulness of MR elastography for detecting clinical progression of cirrhosis from child-pugh class A to B in patients with type C viral hepatitis. J Magn Reson Imaging 44:715–722CrossRefPubMed Takamura T, Motosugi U, Ichikawa S et al (2016) Usefulness of MR elastography for detecting clinical progression of cirrhosis from child-pugh class A to B in patients with type C viral hepatitis. J Magn Reson Imaging 44:715–722CrossRefPubMed
27.
go back to reference Thompson SM, Wang J, Chandan VS et al (2017) MR elastography of hepatocellular carcinoma: correlation of tumor stiffness with histopathology features—preliminary findings. Magn Reson Imaging 37:41–45CrossRefPubMed Thompson SM, Wang J, Chandan VS et al (2017) MR elastography of hepatocellular carcinoma: correlation of tumor stiffness with histopathology features—preliminary findings. Magn Reson Imaging 37:41–45CrossRefPubMed
28.
go back to reference Hennedige TP, Hallinan JT, Leung FP et al (2016) Comparison of magnetic resonance elastography and diffusion-weighted imaging for differentiating benign and malignant liver lesions. Eur Radiol 26:398–406CrossRefPubMed Hennedige TP, Hallinan JT, Leung FP et al (2016) Comparison of magnetic resonance elastography and diffusion-weighted imaging for differentiating benign and malignant liver lesions. Eur Radiol 26:398–406CrossRefPubMed
29.
go back to reference Gordic S, Ayache JB, Kennedy P et al (2017) Value of tumor stiffness measured with MR elastography for assessment of response of hepatocellular carcinoma to locoregional therapy. Abdom Radiol (NY) 42:1685–1694CrossRef Gordic S, Ayache JB, Kennedy P et al (2017) Value of tumor stiffness measured with MR elastography for assessment of response of hepatocellular carcinoma to locoregional therapy. Abdom Radiol (NY) 42:1685–1694CrossRef
30.
go back to reference Lee DH, Lee JM, Yi NJ et al (2017) Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma. Eur Radiol 27:1713–1721CrossRefPubMed Lee DH, Lee JM, Yi NJ et al (2017) Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma. Eur Radiol 27:1713–1721CrossRefPubMed
31.
go back to reference Crespo G, Castro-Narro G, García-Juárez I et al (2016) Usefulness of liver stiffness measurement during acute cellular rejection in liver transplantation. Liver Transpl 22:298–304CrossRefPubMed Crespo G, Castro-Narro G, García-Juárez I et al (2016) Usefulness of liver stiffness measurement during acute cellular rejection in liver transplantation. Liver Transpl 22:298–304CrossRefPubMed
32.
go back to reference Anthony PP, Ishak KG, Nayak NC et al (1978) The morphology of cirrhosis. Recommendations on definition, nomenclature, and classification by a working group sponsored by the World Health Organization. J Clin Pathol 31:395–414CrossRefPubMedPubMedCentral Anthony PP, Ishak KG, Nayak NC et al (1978) The morphology of cirrhosis. Recommendations on definition, nomenclature, and classification by a working group sponsored by the World Health Organization. J Clin Pathol 31:395–414CrossRefPubMedPubMedCentral
33.
go back to reference D'Amico G, Garcia-Tsao G, Pagliaro L (2006) Natural history and prognostic indicators of survival in cirrhosis: a systematic review of 118 studies. J Hepatol 44:217–231CrossRefPubMed D'Amico G, Garcia-Tsao G, Pagliaro L (2006) Natural history and prognostic indicators of survival in cirrhosis: a systematic review of 118 studies. J Hepatol 44:217–231CrossRefPubMed
34.
go back to reference Shiratori Y, Imazeki F, Moriyama M et al (2000) Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy. Ann Intern Med 132:517–524CrossRefPubMed Shiratori Y, Imazeki F, Moriyama M et al (2000) Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy. Ann Intern Med 132:517–524CrossRefPubMed
35.
go back to reference Kim SU, Oh HJ, Wanless IR et al (2012) The Laennec staging system for histological sub-classification of cirrhosis is useful for stratification of prognosis in patients with liver cirrhosis. J Hepatol 57:556–563CrossRefPubMed Kim SU, Oh HJ, Wanless IR et al (2012) The Laennec staging system for histological sub-classification of cirrhosis is useful for stratification of prognosis in patients with liver cirrhosis. J Hepatol 57:556–563CrossRefPubMed
36.
go back to reference Wang W, Li J, Pan R et al (2015) Association of the Laennec staging system with degree of cirrhosis, clinical stage and liver function. Hepatol Int 9:621–626CrossRefPubMed Wang W, Li J, Pan R et al (2015) Association of the Laennec staging system with degree of cirrhosis, clinical stage and liver function. Hepatol Int 9:621–626CrossRefPubMed
37.
go back to reference Kim SU, Kim JK, Park YN et al (2012) Discordance between liver biopsy and Fibroscan® in assessing liver fibrosis in chronic hepatitis b: risk factors and influence of necroinflammation. PLoS One 7:e32233CrossRefPubMedPubMedCentral Kim SU, Kim JK, Park YN et al (2012) Discordance between liver biopsy and Fibroscan® in assessing liver fibrosis in chronic hepatitis b: risk factors and influence of necroinflammation. PLoS One 7:e32233CrossRefPubMedPubMedCentral
38.
go back to reference Krawczyk M, Ligocka J, Ligocki M et al (2017) Does transient elastography correlate with liver fibrosis in patients with PSC? Laennec score-based analysis of explanted livers. Scand J Gastroenterol 52:1407–1412CrossRefPubMed Krawczyk M, Ligocka J, Ligocki M et al (2017) Does transient elastography correlate with liver fibrosis in patients with PSC? Laennec score-based analysis of explanted livers. Scand J Gastroenterol 52:1407–1412CrossRefPubMed
39.
go back to reference Yoshida H, Shiratori Y, Moriyama M et al (1999) Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan. IHIT Study Group. Inhibition of Hepatocarcinogenesis by Interferon Therapy. Ann Intern Med 131:174–181CrossRefPubMed Yoshida H, Shiratori Y, Moriyama M et al (1999) Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan. IHIT Study Group. Inhibition of Hepatocarcinogenesis by Interferon Therapy. Ann Intern Med 131:174–181CrossRefPubMed
40.
go back to reference Tran SA, Le A, Zhao C et al (2008) Rate of hepatocellular carcinoma surveillance remains low for a large, real-life cohort of patients with hepatitis C cirrhosis. BMJ Open Gastroenterol 5:e000192CrossRef Tran SA, Le A, Zhao C et al (2008) Rate of hepatocellular carcinoma surveillance remains low for a large, real-life cohort of patients with hepatitis C cirrhosis. BMJ Open Gastroenterol 5:e000192CrossRef
41.
go back to reference Ichikawa S, Motosugi U, Nakazawa T et al (2015) Hepatitis activity should be considered a confounder of liver stiffness measured with MR elastography. J Magn Reson Imaging 41:1203–1208CrossRefPubMed Ichikawa S, Motosugi U, Nakazawa T et al (2015) Hepatitis activity should be considered a confounder of liver stiffness measured with MR elastography. J Magn Reson Imaging 41:1203–1208CrossRefPubMed
42.
go back to reference Yoshimitsu K, Mitsufuji T, Shinagawa Y et al (2016) MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades; preliminary clinical experience. Eur Radiol 26:656–663CrossRefPubMed Yoshimitsu K, Mitsufuji T, Shinagawa Y et al (2016) MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades; preliminary clinical experience. Eur Radiol 26:656–663CrossRefPubMed
43.
go back to reference Shi Y, Guo Q, Xia F et al (2014) MR elastography for the assessment of hepatic fibrosis in patients with chronic hepatitis B infection: does histologic necroinflammation influence the measurement of hepatic stiffness? Radiology 273:88–98CrossRefPubMed Shi Y, Guo Q, Xia F et al (2014) MR elastography for the assessment of hepatic fibrosis in patients with chronic hepatitis B infection: does histologic necroinflammation influence the measurement of hepatic stiffness? Radiology 273:88–98CrossRefPubMed
44.
go back to reference Chhatwal J, Wang X, Ayer T et al (2016) Hepatitis C disease burden in the United States in the era of oral direct-acting antivirals. Hepatology 64:1442–1450CrossRefPubMed Chhatwal J, Wang X, Ayer T et al (2016) Hepatitis C disease burden in the United States in the era of oral direct-acting antivirals. Hepatology 64:1442–1450CrossRefPubMed
45.
go back to reference Alexopoulou A, Karayiannis P (2015) Interferon-based combination treatment for chronic hepatitis C in the era of direct acting antivirals. Ann Gastroenterol 28:55–65PubMedPubMedCentral Alexopoulou A, Karayiannis P (2015) Interferon-based combination treatment for chronic hepatitis C in the era of direct acting antivirals. Ann Gastroenterol 28:55–65PubMedPubMedCentral
46.
go back to reference Kanwal F, Kramer J, Asch SM, Chayanupatkul M, Cao Y, El-Serag HB (2017) Risk of hepatocellular cancer in HCV patients treated with direct acting antiviral agents. Gastroenterology 153:996–1005.e1CrossRefPubMed Kanwal F, Kramer J, Asch SM, Chayanupatkul M, Cao Y, El-Serag HB (2017) Risk of hepatocellular cancer in HCV patients treated with direct acting antiviral agents. Gastroenterology 153:996–1005.e1CrossRefPubMed
47.
go back to reference Ogata F, Kobayashi M, Akuta N et al (2017) Outcome of all-oral direct-acting antiviral regimens on the rate of development of hepatocellular carcinoma in patients with hepatitis C virus genotype 1-related chronic liver disease. Oncology 93:92–98CrossRefPubMed Ogata F, Kobayashi M, Akuta N et al (2017) Outcome of all-oral direct-acting antiviral regimens on the rate of development of hepatocellular carcinoma in patients with hepatitis C virus genotype 1-related chronic liver disease. Oncology 93:92–98CrossRefPubMed
Metadata
Title
Magnetic resonance elastography can predict development of hepatocellular carcinoma with longitudinally acquired two-point data
Authors
Shintaro Ichikawa
Utaroh Motosugi
Nobuyuki Enomoto
Hiroshi Onishi
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 2/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5640-7

Other articles of this Issue 2/2019

European Radiology 2/2019 Go to the issue