Advertisement

Abdominal Imaging

, Volume 40, Issue 4, pp 766–775 | Cite as

Non-invasive detection of liver fibrosis: MR imaging features vs. MR elastography

  • Sudhakar K. Venkatesh
  • Meng Yin
  • Naoki Takahashi
  • James F. Glockner
  • Talwalkar Jayant A. 
  • Richard L. Ehman
Article

Abstract

Purpose

To compare accuracy of morphological features of liver on MRI and liver stiffness with MR elastography (MRE) for detection of significant liver fibrosis and cirrhosis.

Materials and methods

In this retrospective study, we evaluated 62 patients who underwent liver MRI with MRE and histological confirmation of liver fibrosis within 6 months. Two radiologists, blinded to histology results, independently evaluated liver parenchyma texture, surface nodularity, signs of volumetric changes, and portal hypertension for presence of significant fibrosis and cirrhosis. Two more readers independently calculated mean liver stiffness values with MRE. Interobserver agreement was evaluated with kappa and intra-class correlation coefficient (ICC) analysis. Diagnostic accuracy was assessed with area under receiver operating characteristic (AUROC) analysis. Comparison of AUROCs of MRI and MRE was performed.

Results

Liver fibrosis was present in 37 patients. The interobserver agreement was poor to good (κ = 0.12–0.74) for MRI features and excellent for MRE (ICC 0.97, 95% CI 0.95–0.98). MRI features had 48.5%–87.9% sensitivity, 55.2%–100% specificity, and 71.5%–81.6% accuracy/for detection of significant fibrosis. MRE performed better with 100% sensitivity, 96.5% specificity, and 98.9% accuracy. For the detection of cirrhosis, MRE performed better than MRI features with 88.2% sensitivity (vs. 41.2%–82.3%), 91.1% specificity (vs. 64.4%–95.6%), and 93.5% accuracy (vs. 60.6%–80.5%). Among the MRI features, surface nodularity and overall impression had the best accuracies of 80.3% and 81.6% for detection of significant fibrosis, respectively. For cirrhosis, parenchyma texture and overall impression had the best accuracies of 80.5% and 79.7%, respectively. Overall, MRE had significantly greater AUROC than MRI features for detection of both significant fibrosis (0.98.9 vs 0.71–0.82, P < 0.001) and cirrhosis (0.93.5 vs. 0.61–0.80.5, P < 0.01).

Conclusion

MRE is superior to MRI for the non-invasive diagnosis of significant liver fibrosis and cirrhosis.

Keywords

Liver fibrosis Cirrhosis Magnetic resonance elastography Liver morphology Parenchyma texture Signs of cirrhosis 

References

  1. 1.
    Everhart JE, Ruhl CE (2009) Burden of digestive diseases in the United States Part III: liver, biliary tract, and pancreas. Gastroenterology 136(4):1134–1144CrossRefPubMedGoogle Scholar
  2. 2.
    Asrani SK, Larson JJ, Yawn B, Therneau TM, Kim WR (2013) Underestimation of liver-related mortality in the United States. Gastroenterology 145(2):375–82.e1–2CrossRefPubMedCentralPubMedGoogle Scholar
  3. 3.
    de Franchis R, Dell’Era A (2007) Non-invasive diagnosis of cirrhosis and the natural history of its complications. Best Pract Res 21(1):3–18CrossRefGoogle Scholar
  4. 4.
    Bataller R, Brenner DA (2005) Liver fibrosis. J Clin Investig 115(2):209–218CrossRefPubMedCentralPubMedGoogle Scholar
  5. 5.
    Friedman SL (2003) Liver fibrosis—from bench to bedside. J Hepatol 38(Suppl 1):S38–53CrossRefPubMedGoogle Scholar
  6. 6.
    Rockey DC (2005) Antifibrotic therapy in chronic liver disease. Clin Gastroenterol Hepatol 3(2):95–107CrossRefPubMedGoogle Scholar
  7. 7.
    Rockey DC, Bissell DM (2006) Noninvasive measures of liver fibrosis. Hepatology 43(2 Suppl 1):S113–S120CrossRefPubMedGoogle Scholar
  8. 8.
    Friedman SL, Bansal MB (2006) Reversal of hepatic fibrosis—fact or fantasy? Hepatology 43(2 Suppl 1):S82–S88CrossRefPubMedGoogle Scholar
  9. 9.
    Zhang Y, Zhang XM, Prowda JC, et al. (2009) Changes in hepatic venous morphology with cirrhosis on MRI. J Magn Reson Imaging 29(5):1085–1092CrossRefPubMedGoogle Scholar
  10. 10.
    Bravo AA, Sheth SG, Chopra S (2001) Liver biopsy. N Engl J Med 344(7):495–500CrossRefPubMedGoogle Scholar
  11. 11.
    Ratziu V, Charlotte F, Heurtier A, et al. (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128(7):1898–1906CrossRefPubMedGoogle Scholar
  12. 12.
    Standish RA, Cholongitas E, Dhillon A, Burroughs AK, Dhillon AP (2006) An appraisal of the histopathological assessment of liver fibrosis. Gut 55(4):569–578CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Bedossa P, Dargere D, Paradis V (2003) Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 38(6):1449–1457CrossRefPubMedGoogle Scholar
  14. 14.
    Piccinino F, Sagnelli E, Pasquale G, Giusti G (1986) Complications following percutaneous liver biopsy. A multicentre retrospective study on 68,276 biopsies. J Hepatol 2(2):165–173CrossRefPubMedGoogle Scholar
  15. 15.
    Parkes J, Guha IN, Roderick P, Rosenberg W (2006) Performance of serum marker panels for liver fibrosis in chronic hepatitis C. J Hepatol 44(3):462–474CrossRefPubMedGoogle Scholar
  16. 16.
    Castera L (2012) Noninvasive methods to assess liver disease in patients with hepatitis B or C. Gastroenterology 142(6):1293–302.e4CrossRefPubMedGoogle Scholar
  17. 17.
    Ito K, Mitchell DG (2000) Hepatic morphologic changes in cirrhosis: MR imaging findings. Abdom Imaging 25(5):456–461CrossRefPubMedGoogle Scholar
  18. 18.
    Harbin WP, Robert NJ, Ferrucci JT Jr (1980) Diagnosis of cirrhosis based on regional changes in hepatic morphology: a radiological and pathological analysis. Radiology 135(2):273–283CrossRefPubMedGoogle Scholar
  19. 19.
    Ito K, Mitchell DG, Gabata T, Hussain SM (1999) Expanded gallbladder fossa: simple MR imaging sign of cirrhosis. Radiology 211(3):723–726CrossRefPubMedGoogle Scholar
  20. 20.
    Ito K, Mitchell DG, Kim MJ, et al. (2003) Right posterior hepatic notch sign: a simple diagnostic MR finding of cirrhosis. J Magn Reson Imaging 18(5):561–566CrossRefPubMedGoogle Scholar
  21. 21.
    Gaiani S, Gramantieri L, Venturoli N, et al. (1997) What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. J Hepatol 27(6):979–985CrossRefPubMedGoogle Scholar
  22. 22.
    Aube C, Racineux PX, Lebigot J, et al. (2004) Diagnosis and quantification of hepatic fibrosis with diffusion weighted MR imaging: preliminary results. J Radiol 85(3):301–306CrossRefPubMedGoogle Scholar
  23. 23.
    Chen JH, Chai JW, Shen WC (1999) Magnetization transfer contrast imaging of liver cirrhosis. Hepatogastroenterology 46(29):2872–2877PubMedGoogle Scholar
  24. 24.
    Yeh WC, Li PC, Jeng YM, et al. (2002) Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med Biol 28(4):467–474CrossRefPubMedGoogle Scholar
  25. 25.
    Aguirre DA, Behling CA, Alpert E, Hassanein TI, Sirlin CB (2006) Liver fibrosis: noninvasive diagnosis with double contrast material-enhanced MR imaging. Radiology 239(2):425–437CrossRefPubMedGoogle Scholar
  26. 26.
    Cho SG, Kim MY, Kim HJ, et al. (2001) Chronic hepatitis: in vivo proton MR spectroscopic evaluation of the liver and correlation with histopathologic findings. Radiology 221(3):740–746CrossRefPubMedGoogle Scholar
  27. 27.
    Koinuma M, Ohashi I, Hanafusa K, Shibuya H (2005) Apparent diffusion coefficient measurements with diffusion-weighted magnetic resonance imaging for evaluation of hepatic fibrosis. J Magn Reson Imaging 22(1):80–85CrossRefPubMedGoogle Scholar
  28. 28.
    Taouli B, Losada M, Holland A, Krinsky G (2004) Magnetic resonance imaging of hepatocellular carcinoma. Gastroenterology 127(5 Suppl 1):S144–S152CrossRefPubMedGoogle Scholar
  29. 29.
    Pandharipande PV, Krinsky GA, Rusinek H, Lee VS (2005) Perfusion imaging of the liver: current challenges and future goals. Radiology 234(3):661–673CrossRefPubMedGoogle Scholar
  30. 30.
    Sandrin L, Fourquet B, Hasquenoph JM, et al. (2003) Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol 29(12):1705–1713CrossRefPubMedGoogle Scholar
  31. 31.
    Sarvazyan AP, Rudenko OV, Swanson SD, Fowlkes JB, Emelianov SY (1998) Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med Biol 24(9):1419–1435CrossRefPubMedGoogle Scholar
  32. 32.
    Nightingale K, Soo MS, Nightingale R, Trahey G (2002) Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 28(2):227–235CrossRefPubMedGoogle Scholar
  33. 33.
    Sarvazyan A, Hall TJ, Urban MW, et al. (2011) An overview of elastography—an emerging branch of medical imaging. Curr Med Imaging Rev 7(4):255–282CrossRefPubMedCentralPubMedGoogle Scholar
  34. 34.
    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(2):343–350CrossRefPubMedGoogle Scholar
  35. 35.
    Foucher J, Castera L, Bernard PH, et al. (2006) Prevalence and factors associated with failure of liver stiffness measurement using FibroScan in a prospective study of 2114 examinations. Eur J Gastroenterol Hepatol 18(4):411–412CrossRefPubMedGoogle Scholar
  36. 36.
    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(1):48–54CrossRefPubMedGoogle Scholar
  37. 37.
    Huwart L, Peeters F, Sinkus R, et al. (2006) Liver fibrosis: non-invasive assessment with MR elastography. NMR Biomed 19(2):173–179CrossRefPubMedGoogle Scholar
  38. 38.
    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(2):458–466CrossRefPubMedGoogle Scholar
  39. 39.
    Rouviere O, Yin M, Dresner MA, et al. (2006) MR elastography of the liver: preliminary results. Radiology 240(2):440–448CrossRefPubMedGoogle Scholar
  40. 40.
    Yin M, Talwalkar JA, Glaser KJ, et al. (2014) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5(10):1207–13.e2CrossRefGoogle Scholar
  41. 41.
    Venkatesh SK, Ehman RL (2014) Magnetic resonance elastography of liver. Magn Reson Imaging Clin N Am 22(3):433–446CrossRefPubMedGoogle Scholar
  42. 42.
    Ichikawa S, Motosugi U, Ichikawa T, et al. (2012) Magnetic resonance elastography for staging liver fibrosis in chronic hepatitis C. Magn Reson Med Sci. 11(4):291–297CrossRefPubMedGoogle Scholar
  43. 43.
    Chen J, Talwalkar JA, Yin M, et al. (2011) Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR Elastography. Radiology 259(3):749–756CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    Venkatesh SK, Yin M, Ehman RL (2013) Magnetic resonance elastography of liver: technique, analysis, and clinical applications. J Magn Reson Imaging 37(3):544–555CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Manduca A, Oliphant TE, Dresner MA, et al. (2001) Magnetic resonance elastography: non-invasive mapping of tissue elasticity. Med Image Anal 5(4):237–254CrossRefPubMedGoogle Scholar
  46. 46.
    Westin CF, Wigstrom L, Loock T, et al. (2001) Three-dimensional adaptive filtering in magnetic resonance angiography. J Magn Reson Imaging 14(1):63–71CrossRefPubMedGoogle Scholar
  47. 47.
    Ito K, Mitchell DG, Gabata T (2000) Enlargement of hilar periportal space: a sign of early cirrhosis at MR imaging. J Magn Reson Imaging 11(2):136–140CrossRefPubMedGoogle Scholar
  48. 48.
    Awaya H, Mitchell DG, Kamishima T, et al. (2002) Cirrhosis: modified caudate-right lobe ratio. Radiology 224(3):769–774CrossRefPubMedGoogle Scholar
  49. 49.
    Pozo AL, Godfrey EM, Bowles KM (2009) Splenomegaly: investigation, diagnosis and management. Blood Rev 23(3):105–111CrossRefPubMedGoogle Scholar
  50. 50.
    Kim H, Choi D, Gwak GY, et al. (2009) Evaluation of esophageal varices on liver computed tomography: receiver operating characteristic analyses of the performance of radiologists and endoscopists. J Gastroenterol Hepatol 24(9):1534–1540CrossRefPubMedGoogle Scholar
  51. 51.
    Lipp MJ, Broder A, Hudesman D, et al. (2011) Detection of esophageal varices using CT and MRI. Dig Dis Sci 56(9):2696–2700CrossRefPubMedGoogle Scholar
  52. 52.
    DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44(3):837–845CrossRefPubMedGoogle Scholar
  53. 53.
    Huwart L, Sempoux C, Vicaut E, et al. (2008) Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 135(1):32–40CrossRefPubMedGoogle Scholar
  54. 54.
    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(11):2535–2541CrossRefPubMedGoogle Scholar
  55. 55.
    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(1):70–78CrossRefPubMedGoogle Scholar
  56. 56.
    Venkatesh SK, Xu S, Tai D, Yu H, Wee A (2014) Correlation of MR elastography with morphometric quantification of liver fibrosis (fibro-C-index) in chronic hepatitis B. Magn Reson Med 72(4):1123–1129CrossRefPubMedGoogle Scholar
  57. 57.
    Rustogi R, Horowitz J, Harmath C, et al. (2012) Accuracy of MR elastography and anatomic MR imaging features in the diagnosis of severe hepatic fibrosis and cirrhosis. J Magn Reson Imaging 35(6):1356–1364CrossRefPubMedCentralPubMedGoogle Scholar
  58. 58.
    Giorgio A, Amoroso P, Lettieri G, et al. (1986) Cirrhosis: value of caudate to right lobe ratio in diagnosis with US. Radiology 161(2):443–445CrossRefPubMedGoogle Scholar
  59. 59.
    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(1):88–98CrossRefPubMedGoogle Scholar
  60. 60.
    Ichikawa S, Motosugi U, Nakazawa T, et al. (2014) Hepatitis activity should be considered a confounder of liver stiffness measured with MR elastography. J Magn Reson Imaging. doi: 10.1002/jmri.24666
  61. 61.
    Chung S, Breton E, Mannelli L, Axel L (2011) Liver stiffness assessment by tagged MRI of cardiac-induced liver motion. Magn Reson Med 65(4):949–955CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Sudhakar K. Venkatesh
    • 1
  • Meng Yin
    • 1
  • Naoki Takahashi
    • 1
  • James F. Glockner
    • 1
  • Talwalkar Jayant A. 
    • 2
  • Richard L. Ehman
    • 1
  1. 1.Department of RadiologyMayo ClinicRochesterUSA
  2. 2.Department of Gastroenterology and HepatologyMayo ClinicRochesterUSA

Personalised recommendations