Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 874201, 7 pages
http://dx.doi.org/10.1155/2015/874201
Review Article

Diffusion-Weighted MRI for the Assessment of Liver Fibrosis: Principles and Applications

Radiodiagnostic and Radiotherapy Unit, University Hospital “Policlinico-Vittorio Emanuele”, 95123 Catania, Italy

Received 11 July 2014; Revised 14 December 2014; Accepted 1 January 2015

Academic Editor: Edward Lee

Copyright © 2015 Stefano Palmucci et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Wang, D. R. Ganger, J. Levitsky et al., “Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging,” American Journal of Roentgenology, vol. 196, no. 3, pp. 553–561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. S. L. Friedman, “Mechanisms of hepatic fibrogenesis,” Gastroenterology, vol. 134, no. 6, pp. 1655–1669, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. B. K. Kim, J. Fung, M.-F. Yuen, and S. U. Kim, “Clinical application of liver stiffness measurement using transient elastography in chronic liver disease from longitudinal perspectives,” World Journal of Gastroenterology, vol. 19, no. 12, pp. 1890–1900, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. S. L. Friedman, D. C. Rockey, and D. M. Bissell, “Hepatic fibrosis 2006: report of the third AASLD single topic conference,” Hepatology, vol. 45, no. 1, pp. 242–249, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. J. Hadziyannis, N. C. Tassopoulos, E. J. Heathcote et al., “long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B for up to 5 years,” Gastroenterology, vol. 131, no. 6, pp. 1743–1751, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Bruno, T. Stroffolini, M. Colombo et al., “Sustained virological response to interferon-α is with improved outcome in HCV-related cirrhosis: a retrospective study,” Hepatology, vol. 45, no. 3, pp. 579–587, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Taouli, A. J. Tolia, M. Losada et al., “Diffusion-weighted MRI for quantification of liver fibrosis: preliminary experience,” American Journal of Roentgenology, vol. 189, no. 4, pp. 799–806, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. D. B. McGill, J. Rakela, A. R. Zinsmeister, and B. J. Ott, “A 21-year experience with major hemorrhage after percutaneous liver biopsy,” Gastroenterology, vol. 99, no. 5, pp. 1396–1400, 1990. View at Google Scholar · View at Scopus
  9. F. Froehlich, O. Lamy, M. Fried, and J. J. Gonvers, “Practice and complications of liver biopsy: results of a nationwide survey in Switzerland,” Digestive Diseases and Sciences, vol. 38, no. 8, pp. 1480–1484, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Y. Jin, “Role of liver biopsy in the assessment of hepatic fibrosis: its utility and limitations,” The Korean Journal of Hepatology, vol. 13, no. 2, pp. 138–145, 2007. View at Google Scholar · View at Scopus
  11. C.-T. Wai, J. K. Greenson, R. J. Fontana et al., “A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C,” Hepatology, vol. 38, no. 2, pp. 518–526, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Imbert-Bismut, V. Ratziu, L. Pieroni, F. Charlotte, Y. Benhamou, and T. Poynard, “Biochemical markers of liver fibrosis in patients with hepatitis C virus infection: a prospective study,” The Lancet, vol. 357, no. 9262, pp. 1069–1075, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. N. N. Salkic, P. Jovanovic, G. Hauser, and M. Brcic, “Fibrotest/fibrosure for significant liver fibrosis and cirrhosis in chronic hepatitis B: a meta-analysis,” The American Journal of Gastroenterology, vol. 109, pp. 796–809, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Papastergiou, E. Tsochatzis, and A. K. Burroughs, “Non-invasive assessment of liver fibrosis,” Annals of Gastroenterology, vol. 25, no. 3, pp. 218–231, 2012. View at Google Scholar · View at Scopus
  15. A. Bonder and N. Afdhal, “Utilization of FibroScan in clinical practice,” Current Gastroenterology Reports, vol. 16, no. 2, article 372, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Tatsumi, M. Kudo, K. Ueshima et al., “Noninvasive evaluation of hepatic fibrosis using serum fibrotic markers, transient elastography (FibroScan) and real-time tissue elastography,” Intervirology, vol. 51, supplement 1, pp. 27–33, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Poynard, J. Vergniol, Y. Ngo et al., “Staging chronic hepatitis C in seven categories using fibrosis biomarker (FibroTest) and transient elastography (FibroScan),” Journal of Hepatology, vol. 60, no. 4, pp. 706–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Lee and D. Y. Kim, “Non-invasive diagnosis of hepatitis B virus-related cirrhosis,” World Journal of Gastroenterology, vol. 20, no. 2, pp. 445–459, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. W. C. Yeh, P. C. Li, Y. M. Jeng et al., “Elastic modulus measurements of human liver and correlation with pathology,” Ultrasound in Medicine and Biology, vol. 28, no. 4, pp. 467–474, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Palmucci, L. A. Mauro, M. Messina et al., “Diffusion-weighted MRI in a liver protocol: its role in focal lesion detection,” World Journal of Radiology, vol. 4, no. 7, pp. 302–310, 2012. View at Google Scholar
  21. S. Colagrande, S. F. Carbone, L. M. Carusi, M. Cova, and N. Villari, “Magnetic resonance diffusion-weighted imaging: extraneurological applications,” Radiologia Medica, vol. 111, no. 3, pp. 392–419, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Taouli, M. Chouli, A. J. Martin, A. Qayyum, F. V. Coakley, and V. Vilgrain, “Chronic hepatitis: role of diffusion-weighted imaging and diffusion tensor imaging for the diagnosis of liver fibrosis and inflammation,” Journal of Magnetic Resonance Imaging, vol. 28, no. 1, pp. 89–95, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Pasquinelli, G. Belli, L. N. Mazzoni et al., “MR-diffusion imaging in assessing chronic liver diseases: does a clinical role exist?” Radiologia Medica, vol. 117, no. 2, pp. 242–253, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Bruegel, K. Holzapfel, J. Gaa et al., “Characterization of focal liver lesions by ADC measurements using a respiratory triggered diffusion-weighted single-shot echo-planar MR imaging technique,” European Radiology, vol. 18, no. 3, pp. 477–485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Holzapfel, M. Bruegel, M. Eiber et al., “Characterization of small (10 mm) focal liver lesions: value of respiratory-triggered echo-planar diffusion-weighted MR imaging,” European Journal of Radiology, vol. 76, no. 1, pp. 89–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Coenegrachts, J. Delanote, L. ter Beek et al., “Improved focal liver lesion detection: comparison of single-shot diffusion-weighted echoplanar and single-shot T2 weighted turbo spin echo techniques,” The British Journal of Radiology, vol. 80, no. 955, pp. 524–531, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Mungai, F. Pasquinelli, L. N. Mazzoni et al., “Diffusion-weighted magnetic resonance imaging in the prediction and assessment of chemotherapy outcome in liver metastases,” Radiologia Medica, vol. 119, no. 8, pp. 625–633, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Kokabi, J. C. Camacho, M. Xing et al., “Apparent diffusion coefficient quantification as an early imaging biomarker of response and predictor of survival following yttrium-90 radioembolization for unresectable infiltrative hepatocellular carcinoma with portal vein thrombosis,” Abdominal Imaging, vol. 39, no. 5, pp. 969–978, 2014. View at Publisher · View at Google Scholar
  29. D. Le Bihan, R. Turner, P. Douek, and N. Patronas, “Diffusion MR imaging: clinical applications,” The American Journal of Roentgenology, vol. 159, no. 3, pp. 591–599, 1992. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Y. Carr and E. M. Purcell, “Effects of diffusion on free precession in nuclear magnetic resonance experiments,” Physical Review, vol. 94, no. 3, pp. 630–638, 1954. View at Publisher · View at Google Scholar · View at Scopus
  31. D. le Bihan, R. Turner, J. Pekar, and C. T. W. Moonen, “Diffusion and perfusion imaging by gradient sensitization: design, strategy and significance,” Journal of Magnetic Resonance Imaging, vol. 1, pp. 7–28, 1991. View at Google Scholar
  32. D. Le Bihan, “Molecular diffusion nuclear magnetic resonance imaging,” Magnetic Rresonance Quarterly, vol. 7, no. 1, pp. 1–30, 1991. View at Google Scholar · View at Scopus
  33. R. Turner, D. Le Bihan, and A. S. Chesnick, “Echo-planar imaging of diffusion and perfusion,” Magnetic Resonance in Medicine, vol. 19, no. 2, pp. 247–253, 1991. View at Publisher · View at Google Scholar · View at Scopus
  34. M. F. Reiser, W. Semmler, and H. Hricak, Magnetic Resonance Tomography, Springer, Berlin, Germany, 2008. View at Publisher · View at Google Scholar
  35. J. H. Burdette, A. D. Elster, and P. E. Ricci, “Acute cerebral infarction: quantification of spin-density and T2 shine-through phenomena on diffusion-weighted MR images,” Radiology, vol. 212, no. 2, pp. 333–339, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Liney, MRI in Clinical Practice, Springer, Berlin, Germany, 2007.
  37. I. Yamada, W. Aung, Y. Himeno, T. Nakagawa, and H. Shibuya, “Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging,” Radiology, vol. 210, no. 3, pp. 617–623, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. A. D. Culverwell, M. B. Sheridan, J. A. Guthrie, and A. F. Scarsbrook, “Diffusion-weighted MRI of the liver—interpretative pearls and pitfalls,” Clinical Radiology, vol. 68, no. 4, pp. 406–414, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Kanematsu, S. Goshima, H. Watanabe et al., “Diffusion/perfusion MR imaging of the liver: practice, challenges, and future,” Magnetic Resonance in Medical Sciences, vol. 11, no. 3, pp. 151–161, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Minematsu, L. Li, C. H. Sotak, M. A. Davis, and M. Fisher, “Reversible focal ischemic injury demonstrated by diffusion-weighted magnetic resonance imaging in rats,” Stroke, vol. 23, no. 9, pp. 1304–1311, 1992. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Hayashida, T. Hirai, S. Morishita et al., “Diffusion-weighted imaging of metastatic brain tumors: comparison with histologic type and tumor cellularity,” American Journal of Neuroradiology, vol. 27, no. 7, pp. 1419–1425, 2006. View at Google Scholar · View at Scopus
  42. H. Ozkurt, F. Keskiner, O. Karatag, C. Alkim, S. M. Erturk, and M. Basak, “Diffusion weighted MRI for hepatic fibrosis: impact of b-value,” Iranian Journal of Radiology, vol. 11, no. 1, Article ID e3555, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Hong, Y. Shi, W. Liao et al., “Relative ADC measurement for liver fibrosis diagnosis in chronic hepatitis B using spleen/renal cortex as the reference organs at 3 T,” Clinical Radiology, vol. 69, no. 6, pp. 581–588, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Fujimoto, T. Tonan, S. Azuma et al., “Evaluation of the mean and entropy of apparent diffusion coefficient values in chronic hepatitis C: correlation with pathologic fibrosis stage and inflammatory activity grade,” Radiology, vol. 258, no. 3, pp. 739–748, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. A. A. Bakan, E. Inci, S. Bakan, S. Gokturk, and T. Cimilli, “Utility of diffusion-weighted imaging in the evaluation of liver fibrosis,” European Radiology, vol. 22, no. 3, pp. 682–687, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Mürtz, S. Flacke, F. Träber, J. S. van den Brink, J. Gieseke, and H. H. Schild, “Abdomen: diffusion-weighted MR imaging with pulse-triggered single-shot sequences,” Radiology, vol. 224, no. 1, pp. 258–264, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Taouli and D.-M. Koh, “Diffusion-weighted MR imaging of the liver,” Radiology, vol. 254, no. 1, pp. 47–66, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Palmucci, L. A. Mauro, M. Coppolino et al., “Evaluation of the biliary and pancreatic system with 2D SSFSE, breathhold 3D FRFSE and respiratory-triggered 3D FRFSE sequences,” Radiologia Medica, vol. 115, no. 3, pp. 467–482, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. L. S. Yoon, O. A. Catalano, S. Fritz, C. R. Ferrone, P. F. Hahn, and D. V. Sahani, “Another dimension in magnetic resonance cholangiopancreatography: comparison of 2- and 3-dimensional magnetic resonance cholangiopancreatography for the evaluation of intraductal papillary mucinous neoplasm of the pancreas,” Journal of Computer Assisted Tomography, vol. 33, no. 3, pp. 363–368, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. J. D. Barnwell, J. K. Smith, and M. Castillo, “Utility of navigator-prospective acquisition correction technique (PACE) for reducing motion in brain MR imaging studies,” American Journal of Neuroradiology, vol. 28, no. 4, pp. 790–791, 2007. View at Google Scholar · View at Scopus
  51. B. Taouli, A. Sandberg, A. Stemmer et al., “Diffusion-weighted imaging of the liver: comparison of navigator triggered and breathhold acquisitions,” Journal of Magnetic Resonance Imaging, vol. 30, no. 3, pp. 561–568, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. T. C. Kwee, T. Takahara, R. Ochiai, R. A. J. Nievelstein, and P. R. Luijten, “Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potential applications in oncology,” European Radiology, vol. 18, no. 9, pp. 1937–1952, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Naganawa, H. Kawai, H. Fukatsu et al., “Diffusion-weighted imaging of the liver: technical challenges and prospects for the future,” Magnetic Resonance in Medical Sciences, vol. 4, no. 4, pp. 175–186, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Nasu, Y. Kuroki, H. Fujii, and M. Minami, “Hepatic pseudo-anisotropy: a specific artifact in hepatic diffusion-weighted images obtained with respiratory triggering,” Magnetic Resonance Materials in Physics, Biology and Medicine, vol. 20, no. 4, pp. 205–211, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Sandberg, T. Parikh, G. Johnson, A. Stemmer, and B. Taouli, “Feasibility of a respiratory-triggered SSEPI diffusion-weighted sequence for liver imaging using navigator echo technique: comparison with breath-hold diffusion-weighted sequence,” Proceedings of the International Society for Magnetic Resonance in Medicine, vol. 14, 2006, abstract number 400. View at Google Scholar
  56. K. Nasu, Y. Kuroki, R. Sekiguchi, and S. Nawano, “The effect of simultaneous use of respiratory triggering in diffusion-weighted imaging of the liver,” Magnetic Resonance in Medical Sciences, vol. 5, no. 3, pp. 129–136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. T. C. Kwee, T. Takahara, D. M. Koh, R. A. Nievelstein, and P. R. Luijten, “Comparison and reproducibility of ADC measurements in breathhold, respiratory triggered, and free-breathing diffusion-weighted MR imaging of the liver,” Journal of Magnetic Resonance Imaging, vol. 28, no. 5, pp. 1141–1148, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Sasaki, K. Yamada, Y. Watanabe et al., “Variability in absolute apparent diffusion coefficient values across different platforms may be substantial: a multivendor, multi-institutional comparison study,” Radiology, vol. 249, no. 2, pp. 624–630, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Bonekamp, M. S. Torbenson, and I. R. Kamel, “Diffusion-weighted magnetic resonance imaging for the staging of liver fibrosis,” Journal of Clinical Gastroenterology, vol. 45, no. 10, pp. 885–892, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. K. Sandrasegaran, F. M. Akisik, C. Lin et al., “Value of diffusion-weighted MRI for assessing liver fibrosis and cirrhosis,” American Journal of Roentgenology, vol. 193, no. 6, pp. 1556–1560, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. D. le Bihan, E. Breton, D. Lallemand, M.-L. Aubin, J. Vignaud, and M. Laval-Jeantet, “Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging,” Radiology, vol. 168, no. 2, pp. 497–505, 1988. View at Publisher · View at Google Scholar · View at Scopus
  62. J. H. Yoon, J. M. Lee, M. H. Yu, B. Kiefer, J. K. Han, and B. I. Choi, “Evaluation of hepatic focal lesions using diffusion-weighted MR imaging: comparison of apparent diffusion coefficient and intravoxel incoherent motion-derived parameters,” Journal of Magnetic Resonance Imaging, vol. 39, no. 2, pp. 276–285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Colagrande, F. Pasquinelli, L. N. Mazzoni, G. Belli, and G. Virgili, “MR-diffusion weighted imaging of healthy liver parenchyma: repeatability and reproducibility of apparent diffusion coefficient measurement,” Journal of Magnetic Resonance Imaging, vol. 31, no. 4, pp. 912–920, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Hong, Y. Shi, W. Liao et al., “Relative ADC measurement for liver fibrosis diagnosis in chronic hepatitis B using spleen/renal cortex as the reference organs at 3 T,” Clinical Radiology, vol. 69, no. 6, pp. 581–588, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. R. K. Do, H. Chandanara, E. Felker et al., “Diagnosis of liver fibrosis and cirrhosis with diffusion-weighted imaging: value of normalized apparent diffusion coefficient using the spleen as reference organ,” The American Journal of Roentgenology, vol. 195, no. 3, pp. 671–676, 2010. View at Publisher · View at Google Scholar · View at Scopus