Skip to main content
Top
Published in: European Radiology 4/2017

01-04-2017 | Hepatobiliary-Pancreas

Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma

Authors: Dong Ho Lee, Jeong Min Lee, Nam-Joon Yi, Kwang-Woong Lee, Kyung-Suk Suh, Jeong-Hoon Lee, Kyung Bun Lee, Joon Koo Han

Published in: European Radiology | Issue 4/2017

Login to get access

Abstract

Purpose

To evaluate prognostic value of hepatic stiffness (HS) measurement using MR elastography (MRE) in patients with hepatocellular carcinoma (HCC) treated by hepatic resection (HR).

Methods

We enrolled 144 patients with Barcelona Clinic Liver Cancer stage A HCCs initially treated by HR who underwent preoperative liver MRE between January 2010 and June 2013. HS values were measured using MRE. Receiver operating characteristics (ROC) and multivariate logistic regression analyses were used to determine significant predictive factors for posthepatecomy liver failure (PHLF). Overall survival (OS) was analyzed by evaluating prognostic factors using the Kaplan–Meier method and Cox proportional hazard regression model.

Results

After HR, 43 patients (29.9 %) experienced PHLF. HS values were significant predictive factors for PHLF. In ROC analysis, the area under the curve of HS was 0.740 (P = 0.001) for PHLF. Thirty-one patients had HS values ≥ 4.02 kPa; the estimated 1, 3, 5-year survival were 90.0 %, 74.7 % and 65.4 %, respectively, versus 98.1 %, 96.5 % and 96.5 % in 113 patients with HS values < 4.02 kPa (P = 0.015). An HS value ≥ 4.02 kPa was the only significant affecting factor for OS.

Conclusion

HS values measured by MRE could predict PHLF development post-HR. Furthermore, an HS value ≥4.02 kPa was a significant predicting factor for poor OS post-HR.

Key Points

Hepatic stiffness value was a predictive factor for developing posthepatectomy liver failure
Hepatic stiffness value was a significant affecting factor for OS
Hepatic stiffness value ≥ 4.02 kPa was a predictive factor for poor OS
Appendix
Available only for authorised users
Literature
1.
go back to reference Mazzaferro V (2007) Results of liver transplantation: with or without Milan criteria? Liver Transpl 13:S44–S47CrossRefPubMed Mazzaferro V (2007) Results of liver transplantation: with or without Milan criteria? Liver Transpl 13:S44–S47CrossRefPubMed
2.
go back to reference Imamura H, Seyama Y, Kokudo N et al (2003) One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 138:1198–1206, discussion 1206CrossRefPubMed Imamura H, Seyama Y, Kokudo N et al (2003) One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 138:1198–1206, discussion 1206CrossRefPubMed
3.
go back to reference Poon RT, Fan ST (2004) Hepatectomy for hepatocellular carcinoma: patient selection and postoperative outcome. Liver Transpl 10:S39–S45CrossRefPubMed Poon RT, Fan ST (2004) Hepatectomy for hepatocellular carcinoma: patient selection and postoperative outcome. Liver Transpl 10:S39–S45CrossRefPubMed
4.
go back to reference Cescon M, Colecchia A, Cucchetti A et al (2012) Value of transient elastography measured with FibroScan in predicting the outcome of hepatic resection for hepatocellular carcinoma. Ann Surg 256:706–712, discussion 712–703CrossRefPubMed Cescon M, Colecchia A, Cucchetti A et al (2012) Value of transient elastography measured with FibroScan in predicting the outcome of hepatic resection for hepatocellular carcinoma. Ann Surg 256:706–712, discussion 712–703CrossRefPubMed
5.
go back to reference Farges O, Malassagne B, Flejou JF, Balzan S, Sauvanet A, Belghiti J (1999) Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg 229:210–215CrossRefPubMedPubMedCentral Farges O, Malassagne B, Flejou JF, Balzan S, Sauvanet A, Belghiti J (1999) Risk of major liver resection in patients with underlying chronic liver disease: a reappraisal. Ann Surg 229:210–215CrossRefPubMedPubMedCentral
6.
go back to reference Ishikawa M, Yogita S, Miyake H et al (2002) Clarification of risk factors for hepatectomy in patients with hepatocellular carcinoma. Hepatogastroenterology 49:1625–1631PubMed Ishikawa M, Yogita S, Miyake H et al (2002) Clarification of risk factors for hepatectomy in patients with hepatocellular carcinoma. Hepatogastroenterology 49:1625–1631PubMed
7.
go back to reference Friedrich-Rust M, Ong MF, Martens S et al (2008) Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 134:960–974CrossRefPubMed Friedrich-Rust M, Ong MF, Martens S et al (2008) Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 134:960–974CrossRefPubMed
8.
go back to reference Roulot D, Czernichow S, Le Clesiau H, Costes JL, Vergnaud AC, Beaugrand M (2008) Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol 48:606–613CrossRefPubMed Roulot D, Czernichow S, Le Clesiau H, Costes JL, Vergnaud AC, Beaugrand M (2008) Liver stiffness values in apparently healthy subjects: influence of gender and metabolic syndrome. J Hepatol 48:606–613CrossRefPubMed
9.
go back to reference Wong JS, Wong GL, Chan AW et al (2013) Liver stiffness measurement by transient elastography as a predictor on posthepatectomy outcomes. Ann Surg 257:922–928CrossRefPubMed Wong JS, Wong GL, Chan AW et al (2013) Liver stiffness measurement by transient elastography as a predictor on posthepatectomy outcomes. Ann Surg 257:922–928CrossRefPubMed
10.
go back to reference Huwart L, Sempoux C, Salameh N et al (2007) Liver fibrosis: noninvasive assessment with MR elastography versus aspartate aminotransferase-to-platelet ratio index. Radiology 245:458–466CrossRefPubMed Huwart L, Sempoux C, Salameh N et al (2007) Liver fibrosis: noninvasive assessment with MR elastography versus aspartate aminotransferase-to-platelet ratio index. Radiology 245:458–466CrossRefPubMed
11.
12.
go back to reference 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 36:1490–1495CrossRefPubMed 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 36:1490–1495CrossRefPubMed
13.
go back to reference Godfrey EM, Mannelli L, Griffin N, Lomas DJ (2013) Magnetic resonance elastography in the diagnosis of hepatic fibrosis. Semin Ultrasound CT MR 34:81–88CrossRefPubMed Godfrey EM, Mannelli L, Griffin N, Lomas DJ (2013) Magnetic resonance elastography in the diagnosis of hepatic fibrosis. Semin Ultrasound CT MR 34:81–88CrossRefPubMed
14.
go back to reference Loomba R, Wolfson T, Ang B et al (2014) Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 60:1920–1928CrossRefPubMedPubMedCentral Loomba R, Wolfson T, Ang B et al (2014) Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 60:1920–1928CrossRefPubMedPubMedCentral
15.
go back to reference Monti S, Palma G, Ragucci M, Mannelli L, Mancini M, Prinster A (2014) Optimization of tagged MRI for quantification of liver stiffness using computer simulated data. PLoS ONE 9:e111852CrossRefPubMedPubMedCentral Monti S, Palma G, Ragucci M, Mannelli L, Mancini M, Prinster A (2014) Optimization of tagged MRI for quantification of liver stiffness using computer simulated data. PLoS ONE 9:e111852CrossRefPubMedPubMedCentral
16.
go back to reference Huwart L, Sempoux C, Vicaut E et al (2008) Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 135:32–40CrossRefPubMed Huwart L, Sempoux C, Vicaut E et al (2008) Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 135:32–40CrossRefPubMed
17.
go back to reference Van Beers BE, Daire JL, Garteiser P (2015) New imaging techniques for liver diseases. J Hepatol 62:690–700CrossRefPubMed Van Beers BE, Daire JL, Garteiser P (2015) New imaging techniques for liver diseases. J Hepatol 62:690–700CrossRefPubMed
18.
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 273:88–98CrossRefPubMedPubMedCentral 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 273:88–98CrossRefPubMedPubMedCentral
19.
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
20.
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
21.
go back to reference Ahn SS, Kim MJ, Lim JS, Hong HS, Chung YE, Choi JY (2010) Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 255:459–466CrossRefPubMed Ahn SS, Kim MJ, Lim JS, Hong HS, Chung YE, Choi JY (2010) Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 255:459–466CrossRefPubMed
22.
go back to reference Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology 273:30–50CrossRefPubMedPubMedCentral Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology 273:30–50CrossRefPubMedPubMedCentral
23.
go back to reference Lee DH, Lee JM, Baek JH, Shin CI, Han JK, Choi BI (2015) Diagnostic performance of gadoxetic acid-enhanced liver MR imaging in the detection of HCCs and allocation of transplant recipients on the basis of the Milan criteria and UNOS guidelines: correlation with histopathologic findings. Radiology 274:149–160CrossRefPubMed Lee DH, Lee JM, Baek JH, Shin CI, Han JK, Choi BI (2015) Diagnostic performance of gadoxetic acid-enhanced liver MR imaging in the detection of HCCs and allocation of transplant recipients on the basis of the Milan criteria and UNOS guidelines: correlation with histopathologic findings. Radiology 274:149–160CrossRefPubMed
24.
go back to reference Lee YJ, Lee JM, Lee JS et al (2015) Hepatocellular Carcinoma: Diagnostic Performance of Multidetector CT and MR Imaging-A Systematic Review and Meta-Analysis. Radiology 275:97–109CrossRefPubMed Lee YJ, Lee JM, Lee JS et al (2015) Hepatocellular Carcinoma: Diagnostic Performance of Multidetector CT and MR Imaging-A Systematic Review and Meta-Analysis. Radiology 275:97–109CrossRefPubMed
25.
go back to reference Fan ST, Lai EC, Lo CM, Ng IO, Wong J (1995) Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg 130:198–203CrossRefPubMed Fan ST, Lai EC, Lo CM, Ng IO, Wong J (1995) Hospital mortality of major hepatectomy for hepatocellular carcinoma associated with cirrhosis. Arch Surg 130:198–203CrossRefPubMed
26.
go back to reference Lee DH, Lee JM, Han JK, Choi BI (2013) MR elastography of healthy liver parenchyma: Normal value and reliability of the liver stiffness value measurement. J Magn Reson Imaging 38:1215–1223CrossRefPubMed Lee DH, Lee JM, Han JK, Choi BI (2013) MR elastography of healthy liver parenchyma: Normal value and reliability of the liver stiffness value measurement. J Magn Reson Imaging 38:1215–1223CrossRefPubMed
27.
go back to reference Wang Y, Ganger DR, Levitsky J et al (2011) Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol 196:553–561CrossRefPubMedPubMedCentral Wang Y, Ganger DR, Levitsky J et al (2011) Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol 196:553–561CrossRefPubMedPubMedCentral
28.
go back to reference Shin SU, Lee JM, Yu MH et al (2014) Prediction of esophageal varices in patients with cirrhosis: usefulness of three-dimensional MR elastography with echo-planar imaging technique. Radiology 272:143–153CrossRefPubMedPubMedCentral Shin SU, Lee JM, Yu MH et al (2014) Prediction of esophageal varices in patients with cirrhosis: usefulness of three-dimensional MR elastography with echo-planar imaging technique. Radiology 272:143–153CrossRefPubMedPubMedCentral
29.
go back to reference Rahbari NN, Garden OJ, Padbury R et al (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149:713–724CrossRefPubMed Rahbari NN, Garden OJ, Padbury R et al (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149:713–724CrossRefPubMed
30.
go back to reference Lee DH, Lee JM, Lee JY et al (2015) Non-hypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol 62:1122–1130CrossRefPubMed Lee DH, Lee JM, Lee JY et al (2015) Non-hypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol 62:1122–1130CrossRefPubMed
31.
go back to reference Contal C, O'Quigley J (1999) An application of changepoint methods in studying the effect of age on survival in breast cancer. Comput Stat Data Anal 30:253–270CrossRef Contal C, O'Quigley J (1999) An application of changepoint methods in studying the effect of age on survival in breast cancer. Comput Stat Data Anal 30:253–270CrossRef
32.
go back to reference Faraggi D, Simon R (1996) A simulation study of cross-validation for selecting an optimal cutpoint in univariate survival analysis. Stat Med 15:2203–2213CrossRefPubMed Faraggi D, Simon R (1996) A simulation study of cross-validation for selecting an optimal cutpoint in univariate survival analysis. Stat Med 15:2203–2213CrossRefPubMed
33.
go back to reference Grazi GL, Ercolani G, Pierangeli F et al (2001) Improved results of liver resection for hepatocellular carcinoma on cirrhosis give the procedure added value. Ann Surg 234:71–78CrossRefPubMedPubMedCentral Grazi GL, Ercolani G, Pierangeli F et al (2001) Improved results of liver resection for hepatocellular carcinoma on cirrhosis give the procedure added value. Ann Surg 234:71–78CrossRefPubMedPubMedCentral
34.
go back to reference Jarnagin WR, Gonen M, Fong Y et al (2002) Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg 236:397–406, discussion 406–397CrossRefPubMedPubMedCentral Jarnagin WR, Gonen M, Fong Y et al (2002) Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg 236:397–406, discussion 406–397CrossRefPubMedPubMedCentral
35.
go back to reference Bruix J, Castells A, Bosch J et al (1996) Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology 111:1018–1022CrossRefPubMed Bruix J, Castells A, Bosch J et al (1996) Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology 111:1018–1022CrossRefPubMed
36.
go back to reference Kim SU, Ahn SH, Park JY et al (2008) Prediction of postoperative hepatic insufficiency by liver stiffness measurement (FibroScan((R))) before curative resection of hepatocellular carcinoma: a pilot study. Hepatol Int 2:471–477CrossRefPubMedPubMedCentral Kim SU, Ahn SH, Park JY et al (2008) Prediction of postoperative hepatic insufficiency by liver stiffness measurement (FibroScan((R))) before curative resection of hepatocellular carcinoma: a pilot study. Hepatol Int 2:471–477CrossRefPubMedPubMedCentral
37.
go back to reference Poon RT, Fan ST, Lo CM et al (2002) Extended hepatic resection for hepatocellular carcinoma in patients with cirrhosis: is it justified? Ann Surg 236:602–611CrossRefPubMedPubMedCentral Poon RT, Fan ST, Lo CM et al (2002) Extended hepatic resection for hepatocellular carcinoma in patients with cirrhosis: is it justified? Ann Surg 236:602–611CrossRefPubMedPubMedCentral
38.
go back to reference Thabut D, Moreau R, Lebrec D (2011) Noninvasive assessment of portal hypertension in patients with cirrhosis. Hepatology 53:683–694CrossRefPubMed Thabut D, Moreau R, Lebrec D (2011) Noninvasive assessment of portal hypertension in patients with cirrhosis. Hepatology 53:683–694CrossRefPubMed
39.
go back to reference Venkatesh SK, Wang G, Lim SG, Wee A (2014) Magnetic resonance elastography for the detection and staging of liver fibrosis in chronic hepatitis B. Eur Radiol 24:70–78CrossRefPubMed Venkatesh SK, Wang G, Lim SG, Wee A (2014) Magnetic resonance elastography for the detection and staging of liver fibrosis in chronic hepatitis B. Eur Radiol 24:70–78CrossRefPubMed
40.
go back to reference Ichikawa S, Motosugi U, Morisaka H et al (2015) Validity and Reliability of Magnetic Resonance Elastography for Staging Hepatic Fibrosis in Patients with Chronic Hepatitis B. Magn Reson Med Sci 14:211–221CrossRefPubMed Ichikawa S, Motosugi U, Morisaka H et al (2015) Validity and Reliability of Magnetic Resonance Elastography for Staging Hepatic Fibrosis in Patients with Chronic Hepatitis B. Magn Reson Med Sci 14:211–221CrossRefPubMed
41.
go back to reference Castera L, Forns X, Alberti A (2008) Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol 48:835–847CrossRefPubMed Castera L, Forns X, Alberti A (2008) Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol 48:835–847CrossRefPubMed
42.
go back to reference Lee JE, Lee JM, Lee KB et al (2014) Noninvasive assessment of hepatic fibrosis in patients with chronic hepatitis B viral infection using magnetic resonance elastography. Korean J Radiol 15:210–217CrossRefPubMedPubMedCentral Lee JE, Lee JM, Lee KB et al (2014) Noninvasive assessment of hepatic fibrosis in patients with chronic hepatitis B viral infection using magnetic resonance elastography. Korean J Radiol 15:210–217CrossRefPubMedPubMedCentral
43.
go back to reference Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440CrossRefPubMed Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440CrossRefPubMed
44.
go back to reference Berzigotti A, Reig M, Abraldes JG, Bosch J, Bruix J (2015) Portal hypertension and the outcome of surgery for hepatocellular carcinoma in compensated cirrhosis: a systematic review and meta-analysis. Hepatology 61:526–536CrossRefPubMed Berzigotti A, Reig M, Abraldes JG, Bosch J, Bruix J (2015) Portal hypertension and the outcome of surgery for hepatocellular carcinoma in compensated cirrhosis: a systematic review and meta-analysis. Hepatology 61:526–536CrossRefPubMed
45.
go back to reference Llop E, Berzigotti A, Reig M et al (2012) Assessment of portal hypertension by transient elastography in patients with compensated cirrhosis and potentially resectable liver tumors. J Hepatol 56:103–108CrossRefPubMed Llop E, Berzigotti A, Reig M et al (2012) Assessment of portal hypertension by transient elastography in patients with compensated cirrhosis and potentially resectable liver tumors. J Hepatol 56:103–108CrossRefPubMed
46.
go back to reference Choi SY, Jeong WK, Kim Y, Kim J, Kim TY, Sohn JH (2014) Shear-wave elastography: a noninvasive tool for monitoring changing hepatic venous pressure gradients in patients with cirrhosis. Radiology 273:917–926CrossRefPubMed Choi SY, Jeong WK, Kim Y, Kim J, Kim TY, Sohn JH (2014) Shear-wave elastography: a noninvasive tool for monitoring changing hepatic venous pressure gradients in patients with cirrhosis. Radiology 273:917–926CrossRefPubMed
Metadata
Title
Hepatic stiffness measurement by using MR elastography: prognostic values after hepatic resection for hepatocellular carcinoma
Authors
Dong Ho Lee
Jeong Min Lee
Nam-Joon Yi
Kwang-Woong Lee
Kyung-Suk Suh
Jeong-Hoon Lee
Kyung Bun Lee
Joon Koo Han
Publication date
01-04-2017
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 4/2017
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-016-4499-8

Other articles of this Issue 4/2017

European Radiology 4/2017 Go to the issue