Application of functional MRI in assessment of hepatic warm ischemia-reperfusion injury_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LU Tao ¹ ,  SONG Bin ² , PU Hong ¹ , YIN Longlin ¹

1. Department of Radiology, Sichuan Provincial People’s Hospital, Chengdu 610072, P. R. China;
2. Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

SONG Bin, Email: cjr.songbin@vip.163.com

Keywords：

liver; warm ischemia-reperfusion injury; functional magnetic resonance imaging

DOI：

10.7507/1007-9424.201812022

Video：

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Objective To explore performances of functional magnetic resonance imaging (MRI) in evaluation of hepatic warm ischemia-reperfusion injury.Method The relative references about the principle of functional MRI and its application in the assessment of hepatic warm ischemia-reperfusion injury were reviewed and summarized.Results The main functional MRI techniques for the assessment of hepatic warm ischemia-reperfusion injury included the diffusion weighted imaging (DWI), intravoxel incoherent motion (IVIM), diffusion tensor imaging (DTI), blood oxygen level dependent (BOLD), dynamic contrast enhancement MRI (DCE-MRI), and T2 mapping, etc.. These techniques mainly used in the animal model with hepatic warm ischemia-reperfusion injury currently.Conclusions From current results of researches of animal models, functional MRI is a non-invasive tool to accurately and quantitatively evaluate microscopic information changes of liver tissue in vivo. It can provide a useful information on further understanding of mechanism and prognosis of hepatic warm ischemia-reperfusion injury. With development of donation after cardiac death, functional MRI will play a more important role in evaluation of hepatic warm ischemia-reperfusion injury.

Citation： LU Tao, SONG Bin, PU Hong, YIN Longlin. Application of functional MRI in assessment of hepatic warm ischemia-reperfusion injury. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(3): 351-357. doi: 10.7507/1007-9424.201812022 Copy

1.	郑章强, 朱志军. 心脏死亡供体器官捐献在肝移植中的应用及研究进展. 实用器官移植电子杂志, 2014, 2(4): 212-216.
2.	Xia W, Ke Q, Wang Y, et al. Donation after cardiac death liver transplantation: Graft quality evaluation based on pretransplant liver biopsy. Liver Transpl, 2015, 21(6): 838-846.
3.	Jay CL, Lyuksemburg V, Ladner DP, et al. Ischemic cholangiopathy after controlled donation after cardiac death liver transplantation: a meta-analysis. Ann Surg, 2011, 253(2): 259-264.
4.	Broomhead R, Patel S, Fernando B, et al. Resource implications of expanding the use of DCD organs in liver transplantation. Liver Transpl, 2012, 18(7): 771-778.
5.	Liu Q, Monbaliu D, Vekemans K, et al. Can apparent diffusion coefficient discriminate ischemic from nonischemic livers? A pilot experimental study. Transplant Proc, 2007, 39(8): 2643-2646.
6.	Guo CW, Shen SD, Zhang Y, et al. Determination of apparent diffusion coefficient to quantitatively study partial hepatic ischemia reperfusion injury in a rabbit model. Transplant Proc, 2011, 43(5): 1474-1479.
7.	Zhu L, Cheng Q, Luo W, et al. A comparative study of apparent diffusion coefficient and intravoxel incoherent motion-derived parameters for the characterization of common solid hepatic tumors. Acta Radiol, 2015, 56(12): 1411-1418.
8.	Woo S, Lee JM, Yoon JH, et al. Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. Radiology, 2014, 270(3): 758-767.
9.	Lee Y, Lee SS, Kim N, et al. Intravoxel incoherent motion diffusion-weighted MR imaging of the liver: effect of triggering methods on regional variability and measurement repeatability of quantitative parameters. Radiology, 2015, 274(2): 405-415.
10.	Ye W, Li J, Guo C, et al. Can intravoxel incoherent motion diffusion-weighted imaging characterize the cellular injury and microcirculation alteration in hepatic ischemia-reperfusion injury? An animal study. J Magn Reson Imaging, 2016, 43(6): 1327-1336.
11.	Ji Q, Chu ZQ, Ren T, et al. Multiparametric functional magnetic resonance imaging for evaluation of hepatic warm ischemia-reperfusion injury in a rabbit model. BMC Gastroenterol, 2017, 17(1): 161.
12.	Cheung JS, Fan SJ, Chow AM, et al. In vivo DTI assessment of hepatic ischemia reperfusion injury in an experimental rat model. J Magn Reson Imaging, 2009, 30(4): 890-895.
13.	Tosun M, Inan N, Sarisoy HT, et al. Diagnostic performance of conventional diffusion weighted imaging and diffusion tensor imaging for the liver fibrosis and inflammation. Eur J Radiol, 2013, 82(2): 203-207.
14.	Chuck NC, Steidle G, Blume I, et al. Diffusion tensor imaging of the kidneys: influence of b-value and number of encoding directions on image quality and diffusion tensor parameters. J Clin Imaging Sci, 2013, 3: 53.
15.	Li X, Liang Q, Zhuang L, et al. Preliminary study of MR diffusion tensor imaging of the liver for the diagnosis of hepatocellular carcinoma. PLoS One, 2015, 10: e0135568.
16.	郭成伟, 梁长虹, 刘再毅, 等. 磁共振 DTI 诊断兔急性肝缺血再灌注损伤的价值. 影像诊断与介入放射学, 2016, 25(1): 9-12.
17.	Bane O, Besa C, Wagner M, et al. Feasibility and reproducibility of BOLD and TOLD measurements in the liver with oxygen and carbogen gaschallenge in healthy volunteers and patients with hepatocellular carcinoma. J Magn Reson Imaging, 2016, 43(4): 866-876.
18.	Park HJ, Kim YK, Min JH, et al. Feasibility of blood oxygenation level-dependent MRI at 3T in the characterization of hepatic tumors. Abdom Imaging, 2014, 39(1): 142-152.
19.	Kim JH, Joo I, Kim TY, et al. Diffusion-related MRI parameters for assessing early treatment response of liver metastases to cytotoxic therapy in colorectal cancer. AJR Am J Roentgenol, 2016, 207(3): W26-W32.
20.	Shimizu J, Dono K, Gotoh M, et al. Evaluation of regional liver function by gadolinium-EOB-DTPA-enhanced MR imaging. Dig Dis Sci, 1999, 44(7): 1330-1337.
21.	Zhang W, Kong X, Wang ZJ, et al. Dynamic contrast-enhanced magnetic resonance imaging with Gd-EOB-DTPA for the evaluation of liver fibrosis induced by carbon tetrachloride in rats. PLoS One, 2015, 10(6): e0129621.
22.	Boss MK, Muradyan N, Thrall DE. DCE-MRI: a review and applications in veterinary oncology. Vet Comp Oncol, 2013, 11(2): 87-100.
23.	Lu Y, Liu P, Fu P, et al. Comparison of the DWI and Gd-EOB-DTPA-enhanced MRI on assessing the hepatic ischemia and reperfusion injury after partial hepatectomy. Biomed Pharmacother, 2017, 86: 118-126.
24.	Getzin T, Gueler F, Hartleben B, et al. Gd-EOB-DTPA-enhanced MRI for quantitative assessment of liver organ damage after partial hepatic ischaemia reperfusion injury: correlation with histology and serum biomarkers of liver cell injury. Eur Radiol, 2018, 28(10): 4455-4464.
25.	Shah B, Anderson SW, Scalera J, et al. Quantitative MR imaging: physical principles and sequence design in abdominal imaging. Radiographics, 2011, 31(3): 867-880.
26.	Cheng HL, Stikov N, Ghugre NR, et al. Practical medical applications of quantitative MR relaxometry. J Magn Reson Imaging, 2012, 36(4): 805-824.
27.	Bönner F, Jacoby C, Temme S, et al. Multifunctional MR monitoring of the healing process after myocardial infarction. Basic Res Cardiol, 2014, 109(5): 430.
28.	Sprinkart AM, Luetkens JA, Träber F, et al. Gradient spin echo (GraSE) imaging for fast myocardial T2 mapping. J Cardiovasc Magn Reson, 2015, 17: 12.
29.	Verhaert D, Thavendiranathan P, Giri S, et al. Direct T2 quantification of myocardial edema in acute ischemic injury. JACC Cardiovasc Imaging, 2011, 4(3): 269-278.
30.	Wassmuth R, Prothmann M, Utz W, et al. Variability and homogeneity of cardiovascular magnetic resonance myocardial T2-mapping in volunteers compared to patients with edema. J Cardiovasc Magn Reson, 2013, 15: 27.
31.	Hueper K, Rong S, Gutberlet M, et al. T2 relaxation time and apparent diffusion coefficient for noninvasive assessment of renal pathology after acute kidney injury in mice: comparison with histopathology. Invest Radiol, 2013, 48(12): 834-842.
32.	Hueper K, Hensen B, Gutberlet M, et al. Kidney transplantation: multiparametric functional magnetic resonance imaging for assessment of renal allograft pathophysiology in mice. Invest Radiol, 2016, 51(1): 58-65.
33.	Hueper K, Lang H, Hartleben B, et al. Assessment of liver ischemia reperfusion injury in mice using hepatic T2 mapping: Comparison with histopathology. J Magn Reson Imaging, 2018, 48(6): 1586-1594.
34.	Olthof PB, van Golen RF, Meijer B, et al. Warm ischemia time-dependent variation in liver damage, inflammation, and function in hepatic ischemia/reperfusion injury. Biochim Biophys Acta Mol Basis Dis, 2017, 1863(2): 375-385.
35.	Brandlhuber M, Armbruster M, Zupanc B, et al. A novel and sensitive approach for the evaluation of liver ischemia-reperfusion injury after liver transplantation. Invest Radiol, 2016, 51(3): 170-176.

1. 郑章强, 朱志军. 心脏死亡供体器官捐献在肝移植中的应用及研究进展. 实用器官移植电子杂志, 2014, 2(4): 212-216.
2. Xia W, Ke Q, Wang Y, et al. Donation after cardiac death liver transplantation: Graft quality evaluation based on pretransplant liver biopsy. Liver Transpl, 2015, 21(6): 838-846.
3. Jay CL, Lyuksemburg V, Ladner DP, et al. Ischemic cholangiopathy after controlled donation after cardiac death liver transplantation: a meta-analysis. Ann Surg, 2011, 253(2): 259-264.
4. Broomhead R, Patel S, Fernando B, et al. Resource implications of expanding the use of DCD organs in liver transplantation. Liver Transpl, 2012, 18(7): 771-778.
5. Liu Q, Monbaliu D, Vekemans K, et al. Can apparent diffusion coefficient discriminate ischemic from nonischemic livers? A pilot experimental study. Transplant Proc, 2007, 39(8): 2643-2646.
6. Guo CW, Shen SD, Zhang Y, et al. Determination of apparent diffusion coefficient to quantitatively study partial hepatic ischemia reperfusion injury in a rabbit model. Transplant Proc, 2011, 43(5): 1474-1479.
7. Zhu L, Cheng Q, Luo W, et al. A comparative study of apparent diffusion coefficient and intravoxel incoherent motion-derived parameters for the characterization of common solid hepatic tumors. Acta Radiol, 2015, 56(12): 1411-1418.
8. Woo S, Lee JM, Yoon JH, et al. Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. Radiology, 2014, 270(3): 758-767.
9. Lee Y, Lee SS, Kim N, et al. Intravoxel incoherent motion diffusion-weighted MR imaging of the liver: effect of triggering methods on regional variability and measurement repeatability of quantitative parameters. Radiology, 2015, 274(2): 405-415.
10. Ye W, Li J, Guo C, et al. Can intravoxel incoherent motion diffusion-weighted imaging characterize the cellular injury and microcirculation alteration in hepatic ischemia-reperfusion injury? An animal study. J Magn Reson Imaging, 2016, 43(6): 1327-1336.
11. Ji Q, Chu ZQ, Ren T, et al. Multiparametric functional magnetic resonance imaging for evaluation of hepatic warm ischemia-reperfusion injury in a rabbit model. BMC Gastroenterol, 2017, 17(1): 161.
12. Cheung JS, Fan SJ, Chow AM, et al. In vivo DTI assessment of hepatic ischemia reperfusion injury in an experimental rat model. J Magn Reson Imaging, 2009, 30(4): 890-895.
13. Tosun M, Inan N, Sarisoy HT, et al. Diagnostic performance of conventional diffusion weighted imaging and diffusion tensor imaging for the liver fibrosis and inflammation. Eur J Radiol, 2013, 82(2): 203-207.
14. Chuck NC, Steidle G, Blume I, et al. Diffusion tensor imaging of the kidneys: influence of b-value and number of encoding directions on image quality and diffusion tensor parameters. J Clin Imaging Sci, 2013, 3: 53.
15. Li X, Liang Q, Zhuang L, et al. Preliminary study of MR diffusion tensor imaging of the liver for the diagnosis of hepatocellular carcinoma. PLoS One, 2015, 10: e0135568.
16. 郭成伟, 梁长虹, 刘再毅, 等. 磁共振 DTI 诊断兔急性肝缺血再灌注损伤的价值. 影像诊断与介入放射学, 2016, 25(1): 9-12.
17. Bane O, Besa C, Wagner M, et al. Feasibility and reproducibility of BOLD and TOLD measurements in the liver with oxygen and carbogen gaschallenge in healthy volunteers and patients with hepatocellular carcinoma. J Magn Reson Imaging, 2016, 43(4): 866-876.
18. Park HJ, Kim YK, Min JH, et al. Feasibility of blood oxygenation level-dependent MRI at 3T in the characterization of hepatic tumors. Abdom Imaging, 2014, 39(1): 142-152.
19. Kim JH, Joo I, Kim TY, et al. Diffusion-related MRI parameters for assessing early treatment response of liver metastases to cytotoxic therapy in colorectal cancer. AJR Am J Roentgenol, 2016, 207(3): W26-W32.
20. Shimizu J, Dono K, Gotoh M, et al. Evaluation of regional liver function by gadolinium-EOB-DTPA-enhanced MR imaging. Dig Dis Sci, 1999, 44(7): 1330-1337.
21. Zhang W, Kong X, Wang ZJ, et al. Dynamic contrast-enhanced magnetic resonance imaging with Gd-EOB-DTPA for the evaluation of liver fibrosis induced by carbon tetrachloride in rats. PLoS One, 2015, 10(6): e0129621.
22. Boss MK, Muradyan N, Thrall DE. DCE-MRI: a review and applications in veterinary oncology. Vet Comp Oncol, 2013, 11(2): 87-100.
23. Lu Y, Liu P, Fu P, et al. Comparison of the DWI and Gd-EOB-DTPA-enhanced MRI on assessing the hepatic ischemia and reperfusion injury after partial hepatectomy. Biomed Pharmacother, 2017, 86: 118-126.
24. Getzin T, Gueler F, Hartleben B, et al. Gd-EOB-DTPA-enhanced MRI for quantitative assessment of liver organ damage after partial hepatic ischaemia reperfusion injury: correlation with histology and serum biomarkers of liver cell injury. Eur Radiol, 2018, 28(10): 4455-4464.
25. Shah B, Anderson SW, Scalera J, et al. Quantitative MR imaging: physical principles and sequence design in abdominal imaging. Radiographics, 2011, 31(3): 867-880.
26. Cheng HL, Stikov N, Ghugre NR, et al. Practical medical applications of quantitative MR relaxometry. J Magn Reson Imaging, 2012, 36(4): 805-824.
27. Bönner F, Jacoby C, Temme S, et al. Multifunctional MR monitoring of the healing process after myocardial infarction. Basic Res Cardiol, 2014, 109(5): 430.
28. Sprinkart AM, Luetkens JA, Träber F, et al. Gradient spin echo (GraSE) imaging for fast myocardial T2 mapping. J Cardiovasc Magn Reson, 2015, 17: 12.
29. Verhaert D, Thavendiranathan P, Giri S, et al. Direct T2 quantification of myocardial edema in acute ischemic injury. JACC Cardiovasc Imaging, 2011, 4(3): 269-278.
30. Wassmuth R, Prothmann M, Utz W, et al. Variability and homogeneity of cardiovascular magnetic resonance myocardial T2-mapping in volunteers compared to patients with edema. J Cardiovasc Magn Reson, 2013, 15: 27.
31. Hueper K, Rong S, Gutberlet M, et al. T2 relaxation time and apparent diffusion coefficient for noninvasive assessment of renal pathology after acute kidney injury in mice: comparison with histopathology. Invest Radiol, 2013, 48(12): 834-842.
32. Hueper K, Hensen B, Gutberlet M, et al. Kidney transplantation: multiparametric functional magnetic resonance imaging for assessment of renal allograft pathophysiology in mice. Invest Radiol, 2016, 51(1): 58-65.
33. Hueper K, Lang H, Hartleben B, et al. Assessment of liver ischemia reperfusion injury in mice using hepatic T2 mapping: Comparison with histopathology. J Magn Reson Imaging, 2018, 48(6): 1586-1594.
34. Olthof PB, van Golen RF, Meijer B, et al. Warm ischemia time-dependent variation in liver damage, inflammation, and function in hepatic ischemia/reperfusion injury. Biochim Biophys Acta Mol Basis Dis, 2017, 1863(2): 375-385.
35. Brandlhuber M, Armbruster M, Zupanc B, et al. A novel and sensitive approach for the evaluation of liver ischemia-reperfusion injury after liver transplantation. Invest Radiol, 2016, 51(3): 170-176.

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CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Application of functional MRI in assessment of hepatic warm ischemia-reperfusion injury

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