Skip to main content
Erschienen in: Abdominal Radiology 5/2019

22.02.2019 | Hepatobiliary

MR elastography of liver at 3 Tesla: comparison of gradient-recalled echo (GRE) and spin-echo (SE) echo-planar imaging (EPI) sequences and agreement across stiffness measurements

verfasst von: Chenyang Zhan, Stephan Kannengiesser, Hersh Chandarana, Matthias Fenchel, Justin Ream, Krishna Prasad Shanbhogue

Erschienen in: Abdominal Radiology | Ausgabe 5/2019

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To compare 2D gradient-recalled echo (GRE) and 2D spin-echo (SE) echo-planar imaging (EPI) MR elastography (MRE) for measurement of hepatic stiffness in adult patients with known or suspected liver disease at 3 Tesla.

Materials and methods

Three hundred and eighty-seven consecutive patients underwent MRE of the liver at 3 Tesla with 2D-GRE and 2D-SE-EPI sequences. ‘Mean liver stiffness (LS)’ calculated by averaging 3 ROIs in the right lobe, ‘Maximum LS’ calculated by an ROI in the right lobe; and ‘Freehand LS’ calculated by an ROI in the entire liver were measured by two independent readers. Inter-observer and inter-class variability in stiffness measurements were assessed. Stiffness values were correlated with degree of liver fibrosis (METAVIR scores) in 97 patients who underwent biopsy. The diagnostic performance was compared by a receiver-operating characteristic analysis.

Results

The technical failure rate was 2.8% for 2D-SE-EPI (11/387) and 4.1% for 2D-GRE (16/387, 9 had R2* > 80 s−1 indicating iron overload). There is high reproducibility for both GRE and SE-EPI variants (ICC = 0.84–0.94 for both GRE and SE-EPI MRE). The highest sensitivity, specificity, and accuracy of differentiating mild fibrosis (F0–F2) from advanced fibrosis (F3–F4) are 0.84 (GRE Freehand measurement), 0.92 (GRE Maximum stiffness measurement), and 0.88 (GRE Freehand measurement), respectively.

Conclusions

High intra-class correlation and intra-reader correlation are seen on measured hepatic stiffness for both 2D-GRE and 2D-SE-EPI MRE. 2D-SE-EPI has lower failure rate. Diagnostic performance of both sequences is equivalent, with highest sensitivity for 2D-GRE Freehand stiffness measurement, and highest specificity 2D-GRE Maximum stiffness measurement.
Literatur
1.
Zurück zum Zitat Browning, J.D., L.S. Szczepaniak, R. Dobbins, P. Nuremberg, J.D. Horton, et al. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology, 40(6): p. 1387-95.CrossRefPubMed Browning, J.D., L.S. Szczepaniak, R. Dobbins, P. Nuremberg, J.D. Horton, et al. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology, 40(6): p. 1387-95.CrossRefPubMed
2.
Zurück zum Zitat Younossi, Z.M., M. Stepanova, M. Afendy, Y. Fang, Y. Younossi, et al. (2011) Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008. Clin Gastroenterol Hepatol, 9(6): p. 524-530 e1; quiz e60. Younossi, Z.M., M. Stepanova, M. Afendy, Y. Fang, Y. Younossi, et al. (2011) Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008. Clin Gastroenterol Hepatol, 9(6): p. 524-530 e1; quiz e60.
3.
Zurück zum Zitat Everhart, J.E., E.C. Wright, Z.D. Goodman, J.L. Dienstag, J.C. Hoefs, et al. (2010) Prognostic value of Ishak fibrosis stage: findings from the hepatitis C antiviral long-term treatment against cirrhosis trial. Hepatology, 51(2): p. 585-94.CrossRefPubMed Everhart, J.E., E.C. Wright, Z.D. Goodman, J.L. Dienstag, J.C. Hoefs, et al. (2010) Prognostic value of Ishak fibrosis stage: findings from the hepatitis C antiviral long-term treatment against cirrhosis trial. Hepatology, 51(2): p. 585-94.CrossRefPubMed
4.
Zurück zum Zitat Garcia-Tsao, G., A.J. Sanyal, N.D. Grace, W. Carey, D. Practice Guidelines Committee of the American Association for the Study of Liver, et al. (2007) Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis. Hepatology, 46(3): p. 922-38. Garcia-Tsao, G., A.J. Sanyal, N.D. Grace, W. Carey, D. Practice Guidelines Committee of the American Association for the Study of Liver, et al. (2007) Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis. Hepatology, 46(3): p. 922-38.
5.
Zurück zum Zitat Bruix, J., M. Sherman, and D. American Association for the Study of Liver (2011) Management of hepatocellular carcinoma: an update. Hepatology, 53(3): p. 1020-2.CrossRef Bruix, J., M. Sherman, and D. American Association for the Study of Liver (2011) Management of hepatocellular carcinoma: an update. Hepatology, 53(3): p. 1020-2.CrossRef
6.
Zurück zum Zitat Ratziu, V., F. Charlotte, A. Heurtier, S. Gombert, P. Giral, et al. (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology, 128(7): p. 1898-906.CrossRefPubMed Ratziu, V., F. Charlotte, A. Heurtier, S. Gombert, P. Giral, et al. (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology, 128(7): p. 1898-906.CrossRefPubMed
7.
Zurück zum Zitat Mannelli, L., E. Godfrey, M.J. Graves, A.J. Patterson, P. Beddy, et al. (2012) Magnetic resonance elastography: feasibility of liver stiffness measurements in healthy volunteers at 3T. Clin Radiol, 67(3): p. 258-62.CrossRefPubMed Mannelli, L., E. Godfrey, M.J. Graves, A.J. Patterson, P. Beddy, et al. (2012) Magnetic resonance elastography: feasibility of liver stiffness measurements in healthy volunteers at 3T. Clin Radiol, 67(3): p. 258-62.CrossRefPubMed
8.
Zurück zum Zitat Muthupillai, R., D.J. Lomas, P.J. Rossman, J.F. Greenleaf, A. Manduca, et al. (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science, 269(5232): p. 1854-7.CrossRefPubMed Muthupillai, R., D.J. Lomas, P.J. Rossman, J.F. Greenleaf, A. Manduca, et al. (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science, 269(5232): p. 1854-7.CrossRefPubMed
9.
Zurück zum Zitat Yin, M., J.A. Talwalkar, K.J. Glaser, A. Manduca, R.C. Grimm, et al. (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol, 5(10): p. 1207-1213 e2. Yin, M., J.A. Talwalkar, K.J. Glaser, A. Manduca, R.C. Grimm, et al. (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol, 5(10): p. 1207-1213 e2.
10.
Zurück zum Zitat Dulai, P.S., C.B. Sirlin, and R. Loomba (2016) MRI and MRE for non-invasive quantitative assessment of hepatic steatosis and fibrosis in NAFLD and NASH: Clinical trials to clinical practice. J Hepatol, 65(5): p. 1006-1016.CrossRefPubMedPubMedCentral Dulai, P.S., C.B. Sirlin, and R. Loomba (2016) MRI and MRE for non-invasive quantitative assessment of hepatic steatosis and fibrosis in NAFLD and NASH: Clinical trials to clinical practice. J Hepatol, 65(5): p. 1006-1016.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Loomba, R., C.B. Sirlin, B. Ang, R. Bettencourt, R. Jain, et al. (2015) Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel magnetic resonance imaging and magnetic resonance elastography in a randomized trial (MOZART trial). Hepatology, 61(4): p. 1239-50.CrossRefPubMedPubMedCentral Loomba, R., C.B. Sirlin, B. Ang, R. Bettencourt, R. Jain, et al. (2015) Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel magnetic resonance imaging and magnetic resonance elastography in a randomized trial (MOZART trial). Hepatology, 61(4): p. 1239-50.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Chen, J., J.A. Talwalkar, M. Yin, K.J. Glaser, S.O. Sanderson, et al. (2011) Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology, 259(3): p. 749-56.CrossRefPubMedPubMedCentral Chen, J., J.A. Talwalkar, M. Yin, K.J. Glaser, S.O. Sanderson, et al. (2011) Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology, 259(3): p. 749-56.CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Trout, A.T., R.M. Sheridan, S.D. Serai, S.A. Xanthakos, W. Su, et al. (2018) Diagnostic Performance of MR Elastography for Liver Fibrosis in Children and Young Adults with a Spectrum of Liver Diseases. Radiology, 287(3): p. 824-832.CrossRefPubMed Trout, A.T., R.M. Sheridan, S.D. Serai, S.A. Xanthakos, W. Su, et al. (2018) Diagnostic Performance of MR Elastography for Liver Fibrosis in Children and Young Adults with a Spectrum of Liver Diseases. Radiology, 287(3): p. 824-832.CrossRefPubMed
14.
Zurück zum Zitat Yin, M., K.J. Glaser, J.A. Talwalkar, J. Chen, A. Manduca, et al. (2016) Hepatic MR Elastography: Clinical Performance in a Series of 1377 Consecutive Examinations. Radiology, 278(1): p. 114-24.CrossRefPubMed Yin, M., K.J. Glaser, J.A. Talwalkar, J. Chen, A. Manduca, et al. (2016) Hepatic MR Elastography: Clinical Performance in a Series of 1377 Consecutive Examinations. Radiology, 278(1): p. 114-24.CrossRefPubMed
15.
Zurück zum Zitat Serai, S.D., J.R. Dillman, and A.T. Trout (2017) Spin-echo Echo-planar Imaging MR Elastography versus Gradient-echo MR Elastography for Assessment of Liver Stiffness in Children and Young Adults Suspected of Having Liver Disease. Radiology, 282(3): p. 761-770.CrossRefPubMed Serai, S.D., J.R. Dillman, and A.T. Trout (2017) Spin-echo Echo-planar Imaging MR Elastography versus Gradient-echo MR Elastography for Assessment of Liver Stiffness in Children and Young Adults Suspected of Having Liver Disease. Radiology, 282(3): p. 761-770.CrossRefPubMed
16.
Zurück zum Zitat Felker, E.R., K.S. Choi, K. Sung, H.H. Wu, S.S. Raman, et al. (2018) Liver MR Elastography at 3 T: Agreement Across Pulse Sequences and Effect of Liver R2* on Image Quality. AJR Am J Roentgenol: p. 1-7. Felker, E.R., K.S. Choi, K. Sung, H.H. Wu, S.S. Raman, et al. (2018) Liver MR Elastography at 3 T: Agreement Across Pulse Sequences and Effect of Liver R2* on Image Quality. AJR Am J Roentgenol: p. 1-7.
17.
Zurück zum Zitat Mariappan, Y.K., B. Dzyubak, K.J. Glaser, S.K. Venkatesh, C.B. Sirlin, et al. (2017) Application of Modified Spin-Echo-based Sequences for Hepatic MR Elastography: Evaluation, Comparison with the Conventional Gradient-Echo Sequence, and Preliminary Clinical Experience. Radiology, 282(2): p. 390-398.CrossRefPubMed Mariappan, Y.K., B. Dzyubak, K.J. Glaser, S.K. Venkatesh, C.B. Sirlin, et al. (2017) Application of Modified Spin-Echo-based Sequences for Hepatic MR Elastography: Evaluation, Comparison with the Conventional Gradient-Echo Sequence, and Preliminary Clinical Experience. Radiology, 282(2): p. 390-398.CrossRefPubMed
18.
Zurück zum Zitat Kim, Y.S., J.S. Song, S. Kannengiesser, and S.Y. Seo (2017) Comparison of spin-echo echoplanar imaging and gradient recalled echo-based MR elastography at 3 Tesla with and without gadoxetic acid administration. Eur Radiol, 27(10): p. 4120-4128.CrossRefPubMed Kim, Y.S., J.S. Song, S. Kannengiesser, and S.Y. Seo (2017) Comparison of spin-echo echoplanar imaging and gradient recalled echo-based MR elastography at 3 Tesla with and without gadoxetic acid administration. Eur Radiol, 27(10): p. 4120-4128.CrossRefPubMed
19.
Zurück zum Zitat Lee, Y., J.M. Lee, J.E. Lee, K.B. Lee, E.S. Lee, et al. (2014) MR elastography for noninvasive assessment of hepatic fibrosis: reproducibility of the examination and reproducibility and repeatability of the liver stiffness value measurement. J Magn Reson Imaging, 39(2): p. 326-31.CrossRefPubMed Lee, Y., J.M. Lee, J.E. Lee, K.B. Lee, E.S. Lee, et al. (2014) MR elastography for noninvasive assessment of hepatic fibrosis: reproducibility of the examination and reproducibility and repeatability of the liver stiffness value measurement. J Magn Reson Imaging, 39(2): p. 326-31.CrossRefPubMed
20.
Zurück zum Zitat Toguchi, M., M. Tsurusaki, N. Yada, K. Sofue, T. Hyodo, et al. (2017) Magnetic resonance elastography in the assessment of hepatic fibrosis: a study comparing transient elastography and histological data in the same patients. Abdom Radiol (NY), 42(6): p. 1659-1666.CrossRef Toguchi, M., M. Tsurusaki, N. Yada, K. Sofue, T. Hyodo, et al. (2017) Magnetic resonance elastography in the assessment of hepatic fibrosis: a study comparing transient elastography and histological data in the same patients. Abdom Radiol (NY), 42(6): p. 1659-1666.CrossRef
21.
Zurück zum Zitat Banerjee, R., M. Pavlides, E.M. Tunnicliffe, S.K. Piechnik, N. Sarania, et al. (2014) Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. J Hepatol, 60(1): p. 69-77.CrossRefPubMedPubMedCentral Banerjee, R., M. Pavlides, E.M. Tunnicliffe, S.K. Piechnik, N. Sarania, et al. (2014) Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. J Hepatol, 60(1): p. 69-77.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Wagner, M., I. Corcuera-Solano, G. Lo, S. Esses, J. Liao, et al. (2017) Technical Failure of MR Elastography Examinations of the Liver: Experience from a Large Single-Center Study. Radiology, 284(2): p. 401-412.CrossRefPubMedPubMedCentral Wagner, M., I. Corcuera-Solano, G. Lo, S. Esses, J. Liao, et al. (2017) Technical Failure of MR Elastography Examinations of the Liver: Experience from a Large Single-Center Study. Radiology, 284(2): p. 401-412.CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Garteiser, P., R.S. Sahebjavaher, L.C. Ter Beek, S. Salcudean, V. Vilgrain, et al. (2013) Rapid acquisition of multifrequency, multislice and multidirectional MR elastography data with a fractionally encoded gradient echo sequence. NMR Biomed, 26(10): p. 1326-35.CrossRefPubMed Garteiser, P., R.S. Sahebjavaher, L.C. Ter Beek, S. Salcudean, V. Vilgrain, et al. (2013) Rapid acquisition of multifrequency, multislice and multidirectional MR elastography data with a fractionally encoded gradient echo sequence. NMR Biomed, 26(10): p. 1326-35.CrossRefPubMed
24.
Zurück zum Zitat Guenthner, C. and S. Kozerke (2018) Encoding and readout strategies in magnetic resonance elastography. NMR Biomed, 31(10): p. e3919.CrossRefPubMed Guenthner, C. and S. Kozerke (2018) Encoding and readout strategies in magnetic resonance elastography. NMR Biomed, 31(10): p. e3919.CrossRefPubMed
25.
Zurück zum Zitat Dhyani, M., A. Anvari, and A.E. Samir (2015) Ultrasound elastography: liver. Abdom Imaging, 40(4): p. 698-708.CrossRefPubMed Dhyani, M., A. Anvari, and A.E. Samir (2015) Ultrasound elastography: liver. Abdom Imaging, 40(4): p. 698-708.CrossRefPubMed
26.
Zurück zum Zitat Chung, S., E. Breton, L. Mannelli, and L. Axel (2011) Liver stiffness assessment by tagged MRI of cardiac-induced liver motion. Magn Reson Med, 65(4): p. 949-55.CrossRefPubMedPubMedCentral Chung, S., E. Breton, L. Mannelli, and L. Axel (2011) Liver stiffness assessment by tagged MRI of cardiac-induced liver motion. Magn Reson Med, 65(4): p. 949-55.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Mannelli, L., G.J. Wilson, T.J. Dubinsky, C.A. Potter, P. Bhargava, et al. (2012) Assessment of the liver strain among cirrhotic and normal livers using tagged MRI. J Magn Reson Imaging, 36(6): p. 1490-5.CrossRefPubMed Mannelli, L., G.J. Wilson, T.J. Dubinsky, C.A. Potter, P. Bhargava, et al. (2012) Assessment of the liver strain among cirrhotic and normal livers using tagged MRI. J Magn Reson Imaging, 36(6): p. 1490-5.CrossRefPubMed
28.
Zurück zum Zitat Ichikawa, S., U. Motosugi, T. Ichikawa, K. Sano, H. Morisaka, et al. (2012) Magnetic resonance elastography for staging liver fibrosis in chronic hepatitis C. Magn Reson Med Sci, 11(4): p. 291-7.CrossRefPubMed Ichikawa, S., U. Motosugi, T. Ichikawa, K. Sano, H. Morisaka, et al. (2012) Magnetic resonance elastography for staging liver fibrosis in chronic hepatitis C. Magn Reson Med Sci, 11(4): p. 291-7.CrossRefPubMed
29.
30.
Zurück zum Zitat Regev, A., M. Berho, L.J. Jeffers, C. Milikowski, E.G. Molina, et al. (2002) Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol, 97(10): p. 2614-8.CrossRefPubMed Regev, A., M. Berho, L.J. Jeffers, C. Milikowski, E.G. Molina, et al. (2002) Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol, 97(10): p. 2614-8.CrossRefPubMed
31.
Zurück zum Zitat Runge, J.H., A.E. Bohte, J. Verheij, V. Terpstra, A.J. Nederveen, et al. (2014) Comparison of interobserver agreement of magnetic resonance elastography with histopathological staging of liver fibrosis. Abdom Imaging, 39(2): p. 283-90.CrossRefPubMed Runge, J.H., A.E. Bohte, J. Verheij, V. Terpstra, A.J. Nederveen, et al. (2014) Comparison of interobserver agreement of magnetic resonance elastography with histopathological staging of liver fibrosis. Abdom Imaging, 39(2): p. 283-90.CrossRefPubMed
Metadaten
Titel
MR elastography of liver at 3 Tesla: comparison of gradient-recalled echo (GRE) and spin-echo (SE) echo-planar imaging (EPI) sequences and agreement across stiffness measurements
verfasst von
Chenyang Zhan
Stephan Kannengiesser
Hersh Chandarana
Matthias Fenchel
Justin Ream
Krishna Prasad Shanbhogue
Publikationsdatum
22.02.2019
Verlag
Springer US
Erschienen in
Abdominal Radiology / Ausgabe 5/2019
Print ISSN: 2366-004X
Elektronische ISSN: 2366-0058
DOI
https://doi.org/10.1007/s00261-019-01932-5

Weitere Artikel der Ausgabe 5/2019

Abdominal Radiology 5/2019 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.