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Impact of Liver Fibrosis and Fatty Liver on T1rho Measurements: A Prospective Study

  • Xie, Shuangshuang (Department of Radiology, Tianjin First Center Hospital) ;
  • Li, Qing (Department of Radiology, Tianjin First Center Hospital) ;
  • Cheng, Yue (Department of Radiology, Tianjin First Center Hospital) ;
  • Zhang, Yu (Clinical Science, Philips Healthcare) ;
  • Zhuo, Zhizheng (Clinical Science, Philips Healthcare) ;
  • Zhao, Guiming (Department of Hepatology, Tianjin Second People's Hospital) ;
  • Shen, Wen (Department of Radiology, Tianjin First Center Hospital)
  • Received : 2016.12.04
  • Accepted : 2017.04.15
  • Published : 2017.12.01

Abstract

Objective: To investigate the liver T1rho values for detecting fibrosis, and the potential impact of fatty liver on T1rho measurements. Materials and Methods: This study included 18 healthy subjects, 18 patients with fatty liver, and 18 patients with liver fibrosis, who underwent T1rho MRI and mDIXON collections. Liver T1rho, proton density fat fraction (PDFF) and $T2^*$ values were measured and compared among the three groups. Receiver operating characteristic (ROC) curve analysis was performed to evaluate the T1rho values for detecting liver fibrosis. Liver T1rho values were correlated with PDFF, $T2^*$ values and clinical data. Results: Liver T1rho and PDFF values were significantly different (p < 0.001), whereas the $T2^*$ (p = 0.766) values were similar, among the three groups. Mean liver T1rho values in the fibrotic group ($52.6{\pm}6.8ms$) were significantly higher than those of healthy subjects ($44.9{\pm}2.8ms$, p < 0.001) and fatty liver group ($45.0{\pm}3.5ms$, p < 0.001). Mean liver T1rho values were similar between healthy subjects and fatty liver group (p = 0.999). PDFF values in the fatty liver group ($16.07{\pm}10.59%$) were significantly higher than those of healthy subjects ($1.43{\pm}1.36%$, p < 0.001) and fibrosis group ($1.07{\pm}1.06%$, p < 0.001). PDFF values were similar in healthy subjects and fibrosis group (p = 0.984). Mean T1rho values performed well to detect fibrosis at a threshold of 49.5 ms (area under the ROC curve, 0.855), had a moderate correlation with liver stiffness (r = 0.671, p = 0.012), and no correlation with PDFF, $T2^*$ values, subject age, or body mass index (p > 0.05). Conclusion: T1rho MRI is useful for noninvasive detection of liver fibrosis, and may not be affected with the presence of fatty liver.

Keywords

Acknowledgement

Supported by : National Natural Science Fund of China, Science and Technology Fund of Tianjin, Tianjin Clinical Research Center

References

  1. Su TH, Kao JH, Liu CJ. Molecular mechanism and treatment of viral hepatitis-related liver fibrosis. Int J Mol Sci 2014;15:10578-10604 https://doi.org/10.3390/ijms150610578
  2. Wallace K, Burt AD, Wright MC. Liver fibrosis. Biochem J 2008;411:1-18 https://doi.org/10.1042/BJ20071570
  3. Marcellin P, Gane E, Buti M, Afdhal N, Sievert W, Jacobson IM, et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year openlabel follow-up study. Lancet 2013;381:468-475 https://doi.org/10.1016/S0140-6736(12)61425-1
  4. Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HL, Chen CJ, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 2016;10:1-98
  5. Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 2003;38:1449-1457 https://doi.org/10.1053/jhep.2003.09022
  6. Standish RA, Cholongitas E, Dhillon A, Burroughs AK, Dhillon AP. An appraisal of the histopathological assessment of liver fibrosis. Gut 2006;55:569-578 https://doi.org/10.1136/gut.2005.084475
  7. Venkatesh SK, Wang G, Lim SG, Wee A. Magnetic resonance elastography for the detection and staging of liver fibrosis in chronic hepatitis B. Eur Radiol 2014;24:70-78 https://doi.org/10.1007/s00330-013-2978-8
  8. Sagir A, Erhardt A, Schmitt M, Haussinger D. Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology 2008;47:592-595
  9. Calvaruso V, Camma C, Di Marco V, Maimone S, Bronte F, Enea M, et al. Fibrosis staging in chronic hepatitis C: analysis of discordance between transient elastography and liver biopsy. J Viral Hepat 2010;17:469-474
  10. Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol 2011;54:650-659 https://doi.org/10.1016/j.jhep.2010.07.033
  11. Ronot M, Asselah T, Paradis V, Michoux N, Dorvillius M, Baron G, et al. Liver fibrosis in chronic hepatitis C virus infection: differentiating minimal from intermediate fibrosis with perfusion CT. Radiology 2010;256:135-142 https://doi.org/10.1148/radiol.10091295
  12. Wang L, Fan J, Ding X, Sun J, Zhang M. Assessment of liver fibrosis in the early stages with perfusion CT. Int J Clin Exp Med 2015;8:15276-15282
  13. Ogul H, Kantarci M, Genc B, Pirimoglu B, Cullu N, Kizrak Y, et al. Perfusion CT imaging of the liver: review of clinical applications. Diagn Interv Radiol 2014;20:379-389 https://doi.org/10.5152/dir.2014.13396
  14. Ding Y, Rao S, Yang L, Chen C, Zeng M. Comparison of the effect of region-of-interest methods using gadoxetic acidenhanced MR imaging with diffusion-weighted imaging on staging hepatic fibrosis. Radiol Med 2016;121:821-827 https://doi.org/10.1007/s11547-016-0669-7
  15. Watanabe H, Kanematsu M, Goshima S, Kondo H, Onozuka M, Moriyama N, et al. Staging hepatic fibrosis: comparison of gadoxetate disodium-enhanced and diffusion-weighted MR imaging--preliminary observations. Radiology 2011;259:142-150 https://doi.org/10.1148/radiol.10100621
  16. Kim H, Park SH, Kim EK, Kim MJ, Park YN, Park HJ, et al. Histogram analysis of gadoxetic acid-enhanced MRI for quantitative hepatic fibrosis measurement. PLoS One 2014;9:e114224 https://doi.org/10.1371/journal.pone.0114224
  17. Wang QB, Zhu H, Liu HL, Zhang B. Performance of magnetic resonance elastography and diffusion-weighted imaging for the staging of hepatic fibrosis: a meta-analysis. Hepatology 2012;56:239-247 https://doi.org/10.1002/hep.25610
  18. Yeom SK, Lee CH, Cha SH, Park CM. Prediction of liver cirrhosis, using diagnostic imaging tools. World J Hepatol 2015;7:2069-2079 https://doi.org/10.4254/wjh.v7.i17.2069
  19. Shi Y, Guo Q, Xia F, Dzyubak B, Glaser KJ, Li Q, et al. 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 2014;273:88-98 https://doi.org/10.1148/radiol.14132592
  20. Liu J, Ji Y, Ai H, Ning B, Zhao J, Zhang Y, et al. Liver shearwave velocity and serum fibrosis markers to diagnose hepatic fibrosis in patients with chronic viral hepatitis B. Korean J Radiol 2016;17:396-404 https://doi.org/10.3348/kjr.2016.17.3.396
  21. Yoo H, Lee JM, Yoon JH, Lee DH, Chang W, Han JK. Prospective comparison of liver stiffness measurements between two point shear wave elastography methods: virtual touch quantification and elastography point quantification. Korean J Radiol 2016;17:750-757 https://doi.org/10.3348/kjr.2016.17.5.750
  22. Markkola AT, Aronen HJ, Paavonen T, Hopsu E, Sipila LM, Tanttu JI, et al. Spin lock and magnetization transfer imaging of head and neck tumors. Radiology 1996;200:369-375 https://doi.org/10.1148/radiology.200.2.8685328
  23. Santyr GE, Henkelman RM, Bronskill MJ. Spin locking for magnetic resonance imaging with application to human breast. Magn Reson Med 1989;12:25-37 https://doi.org/10.1002/mrm.1910120104
  24. Sepponen RE, Pohjonen JA, Sipponen JT, Tanttu JI. A method for T1 rho imaging. J Comput Assist Tomogr 1985;9:1007-1011 https://doi.org/10.1097/00004728-198511000-00002
  25. Wang YX, Yuan J, Chu ES, Go MY, Huang H, Ahuja AT, et al. T1rho MR imaging is sensitive to evaluate liver fibrosis: an experimental study in a rat biliary duct ligation model. Radiology 2011;259:712-719 https://doi.org/10.1148/radiol.11101638
  26. Zhao F, Wang YX, Yuan J, Deng M, Wong HL, Chu ES, et al. MR $T1\rho$ as an imaging biomarker for monitoring liver injury progression and regression: an experimental study in rats with carbon tetrachloride intoxication. Eur Radiol 2012;22:1709-1716 https://doi.org/10.1007/s00330-012-2419-0
  27. Jiang J, Huang B, Bin G, Chen S, Feng F, Zou L. An experimental study on the assessment of rabbit hepatic fibrosis by using magnetic resonance $T1\rho$ imaging. Magn Reson Imaging 2016;34:308-311 https://doi.org/10.1016/j.mri.2015.10.017
  28. Rauscher I, Eiber M, Ganter C, Martirosian P, Safi W, Umgelter A, et al. Evaluation of $T1\rho$ as a potential MR biomarker for liver cirrhosis: comparison of healthy control subjects and patients with liver cirrhosis. Eur J Radiol 2014;83:900-904 https://doi.org/10.1016/j.ejrad.2014.02.017
  29. Allkemper T, Sagmeister F, Cicinnati V, Beckebaum S, Kooijman H, Kanthak C, et al. Evaluation of fibrotic liver disease with whole-liver $T1\rho$ MR imaging: a feasibility study at 1.5 T. Radiology 2014;271:408-415 https://doi.org/10.1148/radiol.13130342
  30. Singh A, Reddy D, Haris M, Cai K, Rajender Reddy K, Hariharan H, et al. $T1\rho$ MRI of healthy and fibrotic human livers at 1.5 T. J Transl Med 2015;13:292 https://doi.org/10.1186/s12967-015-0648-0
  31. Takayama Y, Nishie A, Asayama Y, Ushijima Y, Okamoto D, Fujita N, et al. $T1\rho$ relaxation of the liver: a potential biomarker of liver function. J Magn Reson Imaging 2015;42:188-195 https://doi.org/10.1002/jmri.24739
  32. Marino L, Jornayvaz FR. Endocrine causes of nonalcoholic fatty liver disease. World J Gastroenterol 2015;21:11053-11076 https://doi.org/10.3748/wjg.v21.i39.11053
  33. Kim SU, Park JY, Kim DY, Ahn SH, Choi EH, Seok JY, et al. Non-invasive assessment of changes in liver fibrosis via liver stiffness measurement in patients with chronic hepatitis B: impact of antiviral treatment on fibrosis regression. Hepatol Int 2010;4:673-680 https://doi.org/10.1007/s12072-010-9201-7
  34. Kukuk GM, Hittatiya K, Sprinkart AM, Eggers H, Gieseke J, Block W, et al. Comparison between modified Dixon MRI techniques, MR spectroscopic relaxometry, and different histologic quantification methods in the assessment of hepatic steatosis. Eur Radiol 2015;25:2869-2879 https://doi.org/10.1007/s00330-015-3703-6
  35. Fallatah HI, Akbar HO, Fallatah AM. Fibroscan compared to FIB-4, APRI, and AST/ALT ratio for assessment of liver fibrosis in Saudi patients with nonalcoholic fatty liver disease. Hepat Mon 2016;16:e38346
  36. La˘pa˘dat AM, Jianu IR, Ungureanu BS, Florescu LM, Gheonea DI, Sovaila S, et al. Non-invasive imaging techniques in assessing non-alcoholic fatty liver disease: a current status of available methods. J Med Life 2017;10:19-26
  37. Deng M, Zhao F, Yuan J, Ahuja AT, Wang YX. Liver $T1\rho$ MRI measurement in healthy human subjects at 3 T: a preliminary study with a two-dimensional fast-field echo sequence. Br J Radiol 2012;85:e590-e595 https://doi.org/10.1259/bjr/98745548
  38. Kim DY, Kim SU, Ahn SH, Park JY, Lee JM, Park YN, et al. Usefulness of FibroScan for detection of early compensated liver cirrhosis in chronic hepatitis B. Dig Dis Sci 2009;54:1758-1763 https://doi.org/10.1007/s10620-008-0541-2
  39. Kumar R, Rastogi A, Sharma MK, Bhatia V, Tyagi P, Sharma P, et al. Liver stiffness measurements in patients with different stages of nonalcoholic fatty liver disease: diagnostic performance and clinicopathological correlation. Dig Dis Sci 2013;58:265-274 https://doi.org/10.1007/s10620-012-2306-1
  40. Koon CM, Zhang X, Chen W, Chu ES, San Lau CB, Wang YX. Black blood T1rho MR imaging may diagnose early stage liver fibrosis: a proof-of-principle study with rat biliary duct ligation model. Quant Imaging Med Surg 2016;6:353-363 https://doi.org/10.21037/qims.2016.08.11
  41. Chen W, Chan Q, Wang YX. Breath-hold black blood quantitative T1rho imaging of liver using single shot fast spin echo acquisition. Quant Imaging Med Surg 2016;6:168-177 https://doi.org/10.21037/qims.2016.04.05
  42. Yuan J, Zhao F, Griffith JF, Chan Q, Wang YX. Optimized efficient liver T($1\rho$) mapping using limited spin lock times. Phys Med Biol 2012;57:1631-1640 https://doi.org/10.1088/0031-9155/57/6/1631
  43. Zhao F, Deng M, Yuan J, Teng GJ, Ahuja AT, Wang YX. Experimental evaluation of accelerated T1rho relaxation quantification in human liver using limited spin-lock times. Korean J Radiol 2012;13:736-742 https://doi.org/10.3348/kjr.2012.13.6.736
  44. Chandarana H, Lim RP, Jensen JH, Hajdu CH, Losada M, Babb JS, et al. Hepatic iron deposition in patients with liver disease: preliminary experience with breath-hold multiecho T2*-weighted sequence. AJR Am J Roentgenol 2009;193:1261-1267 https://doi.org/10.2214/AJR.08.1996

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