Abstract
Objectives
To explore whether intravoxel incoherent motion (IVIM) parameters could evaluate liver regeneration preoperatively.
Methods
A total of 175 HCC patients were initially recruited. The apparent diffusion coefficient, true diffusion coefficient (D), pseudodiffusion coefficient (D*), pseudodiffusion fraction (f), diffusion distribution coefficient, and diffusion heterogeneity index (Alpha) were measured by two independent radiologists. Spearman’s correlation test was used to assess correlations between IVIM parameters and the regeneration index (RI), calculated as 100% × (the volume of the postoperative remnant liver − the volume of the preoperative remnant liver) / the volume of the preoperative remnant liver. Multivariate linear regression analyses were used to identify the factors for RI.
Results
Finally, 54 HCC patients (45 men and 9 women, mean age 51.26 ± 10.41 years) were retrospectively analyzed. The intraclass correlation coefficient ranged from 0.842 to 0.918. In all patients, fibrosis stage was reclassified as F0–1 (n = 10), F2–3 (n = 26), and F4 (n = 18) using the METAVIR system. Spearman correlation test showed D* (r = 0.303, p = 0.026) was associated with RI; however, multivariate analysis showed that only D value was a significant predictor (p < 0.05) of RI. D and D*showed moderate correlations with fibrosis stage (r = −0.361, p = 0.007; r = −0.457, p = 0.001). Fibrosis stage showed a negative correlation with RI (r = −0.263, p = 0.015). In the 29 patients who underwent minor hepatectomy, only the D value showed a positive association (p < 0.05) with RI, and a negative correlation with fibrosis stage (r = −0.360, p = 0.018). However, in the 25 patients who underwent major hepatectomy, no IVIM parameters were associated with RI (p > 0.05).
Conclusions
The D and D* values, especially the D value, may be reliable preoperative predictors of liver regeneration.
Key Points
• The D and D* values, especially the D value, derived from IVIM diffusion-weighted imaging may be useful markers for the preoperative prediction of liver regeneration in patients with HCC.
• The D and D* values derived from IVIM diffusion-weighted imaging show significant negative correlations with fibrosis, an important predictor of liver regeneration.
• No IVIM parameters were associated with liver regeneration in patients who underwent major hepatectomy, but the D value was a significant predictor of liver regeneration in patients who underwent minor hepatectomy.
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Abbreviations
- ADC:
-
Apparent diffusion coefficient
- ALB:
-
Albumin
- Alpha:
-
Diffusion heterogeneity index
- CT:
-
Computed tomography
- D* :
-
Pseudodiffusion coefficient
- D:
-
True diffusion coefficient
- DDC:
-
Diffusion distribution coefficient
- f :
-
Pseudodiffusion fraction
- HCC:
-
Hepatocellular carcinoma
- ICC:
-
Intraclass correlation coefficient
- IVIM:
-
Intravoxel incoherent motion
- LAVA:
-
Liver acceleration volume acquisition
- LR:
-
Liver regeneration
- LVpost:
-
The volume of the postoperative remnant liver
- LVpre:
-
The volume of the preoperative remnant liver
- MRE:
-
Magnetic resonance elastography
- NEX:
-
Number of excitations
- PHRR:
-
The parenchymal hepatic resection rate
- RI:
-
Regeneration index
- SWE:
-
Shear wave elastography
References
Sung H, Ferlay J, Siegel RL et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249
Park JW, Chen M, Colombo M et al (2015) Global patterns of hepatocellular carcinoma management from diagnosis to death: the BRIDGE Study. Liver Int 35(9):2155–66
Inoue Y, Fujii K, Ishii M et al (2019) Volumetric and functional regeneration of remnant liver after hepatectomy. J Gastrointest Surg 23(5):914–921
Cieslak KP, Runge JH, Heger M, Stoker J, Bennink RJ, van Gulik TM (2014) New perspectives in the assessment of future remnant liver. Dig Surg 31(4–5):255–68
Fukushima K, Fukumoto T, Kuramitsu K et al (2014) Assessment of ISGLS definition of posthepatectomy liver failure and its effect on outcome in patients with hepatocellular carcinoma. J Gastrointest Surg 18(4):729–36
Marrone G, Shah VH, Gracia-Sancho J (2016) Sinusoidal communication in liver fibrosis and regeneration. J Hepatol 65(3):608–17
Hori T, Uemoto S, Chen F et al (2014) Oxidative stress and extracellular matrices after hepatectomy and liver transplantation in rats. World J Hepatol 6(2):72–84
Ramos Rubio E, LladoGarriga L (2010) Usefulness of pre-surgical biopsy in selecting patients with hepatocellular carcinoma for liver transplant. Cir Esp 87:133–138
Jang S, Lee JM, Lee DH et al (2017) Value of MR elastography for the preoperative estimation of liver regeneration capacity in patients with hepatocellular carcinoma. J Magn Reson Imaging 45:1627–1636
Gao Y, Zheng J, Liang P et al (2018) Liver fibrosis with two-dimensional US shear-wave elastography in participants with chronic hepatitis B: a prospective multicenter study. Radiology 289:407–415
Li YT, Cercueil JP, Yuan J, Chen W, Loffroy R, Wáng YX (2017) Liver intravoxel incoherent motion (IVIM) magnetic resonance imaging: a comprehensive review of published data on normal values and applications for fibrosis and tumor evaluation. Quant Imaging Med Surg 7:59–78
Luciani A, Vignaud A, Cavet M et al (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging–pilot study. Radiology 249:891–899
Zhang Y, Jin N, Deng J et al (2013) Intra-voxel incoherent motion MRI in rodent model of diethylnitrosamine-induced liver fibrosis. Magn Reson Imaging 31:1017–1021
Zhang T, Wei Y, He X et al (2021) Prediction of remnant liver regeneration after right hepatectomy in patients with hepatocellular carcinoma using preoperative CT texture analysis and clinical features. Contrast Media Mol Imaging 2021:5572470
Fruscione M, Pickens R, Baker EH et al (2019) Robotic-assisted versus laparoscopic major liver resection: analysis of outcomes from a single center. HPB (Oxford) 21:906–911
Kele PG, de Boer M, van der Jagt EJ et al (2012) Early hepatic regeneration index and completeness of regeneration at 6 months after partial hepatectomy. Br J Surg 99:1113–1119
Pulitano C, Crawford M, Joseph D et al (2014) Preoperative assessment of postoperative liver function: the importance of residual liver volume. J Surg Oncol 110:445–450
Haimerl M, Schlabeck M, Verloh N et al (2016) Volume-assisted estimation of liver function based on Gd- EOB-DTPA-enhanced MR relaxometry. Eur Radiol 26:1125–1133
Park J, Kim JH, Kim JE et al (2020) Prediction of liver regeneration in recipients after living-donor liver transplantation in using preoperative CT texture analysis and clinical features. Abdom Radiol (NY) 45:3763–3774
Park YS, Park SH, Lee SS et al (2011) Biopsy-proven nonsteatotic liver in adults: estimation of reference range for difference in attenuation between the liver and the spleen at nonenhanced CT. Radiology 258:760–766
Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C The METAVIR cooperative study group. Hepatology 24:289–293
Scheuer PJ (1991) Classification of chronic viral hepatitis: a need for reassessment. J Hepatol 13:372–374
Zhang Y, Kuang S, Shan Q et al (2019) Can IVIM help predict HCC recurrence after hepatectomy. Eur Radiol 29:5791–5803
Shao S, Shan Q, Zheng N, Wang B, Wang J (2019) Role of intravoxel incoherent motion in discriminating hepatitis B virus-related intrahepatic mass-forming cholangiocarcinoma from hepatocellular carcinoma based on liver imaging reporting and data system v2018. Cancer Biother Radiopharm 34:511–518
Le Bihan D, Ichikawa S, Motosugi U (2017) Diffusion and intravoxel incoherent motion MR imaging-based virtual elastography: a hypothesis-generating study in the liver. Radiology 285:609–619
Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505
Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS (2003) Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med 50:727–734
Lai V, Lee VH, Lam KO, Sze HC, Chan Q, Khong PL (2015) Intravoxel water diffusion heterogeneity MR imaging of nasopharyngeal carcinoma using stretched exponential diffusion model. Eur Radiol 25:1708–1713
Seo N, Chung YE, Park YN, Kim E, Hwang J, Kim MJ (2018) Liver fibrosis: stretched exponential model outperforms mono-exponential and bi-exponential models of diffusion-weighted MRI. Eur Radiol 28:2812–2822
Slinker BK, Glantz SA (1985) Multiple regression for physiological data analysis: the problem of multicollinearity. Am J Physiol 249:R1-12
Huebert RC, Shah VH (2014) Sinusoidal endothelial cells direct traffic at the intersection of regeneration and fibrosis. Hepatology 60:754–756
Wiemann SU, Satyanarayana A, Tsahuridu M et al (2002) Hepatocyte telomere shortening and senescence are general markers of human liver cirrhosis. FASEB J 16:935–942
Ding BS, Cao Z, Lis R et al (2014) Divergent angiocrine signals from vascular niche balance liver regeneration and fibrosis. Nature 505:97–102
Tosun M, Onal T, Uslu H, Alparslan B, ÇetinAkhan S (2020) Intravoxel incoherent motion imaging for diagnosing and staging the liver fibrosis and inflammation. Abdom Radiol (NY) 45:15–23
Chow AM, Gao DS, Fan SJ et al (2012) Liver fibrosis: an intravoxel incoherent motion (IVIM) study. J Magn Reson Imaging 36:159–167
Moreno AH, Burchell AR, Rousselot LM, Panke WF, Slafsky F, Burke JH (1967) Portal blood flow in cirrhosis of the liver. J Clin Invest 46:436–445
Ren H, Liu Y, Lu J et al (2021) Evaluating the clinical value of MRI multi-model diffusion-weighted imaging on liver fibrosis in chronic hepatitis B patients. Abdom Radiol (NY) 46:1552–1561
Hu G, Chan Q, Quan X et al (2015) Intravoxel incoherent motion MRI evaluation for the staging of liver fibrosis in a rat model. J Magn Reson Imaging 42:331–339
Zipprich A, Steudel N, Behrmann C et al (2003) Functional significance of hepatic arterial flow reserve in patients with cirrhosis. Hepatology 37:385–392
Bai Y, Lin Y, Tian J et al (2016) Grading of gliomas by using monoexponential, biexponential, and stretched exponential diffusion-weighted MR imaging and diffusion kurtosis MR imaging. Radiology 278:496–504
Park JH, Seo N, Chung YE et al (2021) Noninvasive evaluation of liver fibrosis: comparison of the stretched exponential diffusion-weighted model to other diffusion-weighted MRI models and transient elastography. Eur Radiol 31:4813–4823
Anderson SW, Barry B, Soto J et al (2014) Characterizing non-Gaussian, high b-value diffusion in liver fibrosis: Stretched exponential and diffusional kurtosis modeling. J Magn Reson Imaging 39:827–834
Standish RA, Cholongitas E, Dhillon A, Burroughs AK, Dhillon AP (2006) An appraisal of the histopathological assessment of liver fibrosis. Gut 55:569–578
Biagini G, Ballardini G (1989) Liver fibrosis and extracellular matrix. J Hepatol 8:115–124
Sandrasegaran K, Territo P, Elkady RM et al (2018) Does intravoxel incoherent motion reliably stage hepatic fibrosis, steatosis, and inflammation? Abdom Radiol (NY) 43:600–606
Manning P, Murphy P, Wang K et al (2017) Liver histology and diffusion-weighted MRI in children with nonalcoholic fatty liver disease: a MAGNET study. J Magn Reson Imaging 46:1149–1158
Lefebvre T, Hébert M, Bilodeau L et al (2021) Intravoxel incoherent motion diffusion-weighted MRI for the characterization of inflammation in chronic liver disease. Eur Radiol 31:1347–1358
Abdalla EK, Denys A, Chevalier P, Nemr RA, Vauthey JN (2004) Total and segmental liver volume variations: implications for liver surgery. Surgery 135:404–410
Kim JE, Kim JH, Park SJ, Choi SY, Yi NJ, Han JK (2019) Prediction of liver remnant regeneration after living donor liver transplantation using preoperative CT texture analysis. Abdom Radiol (NY) 44:1785–1794
Meier M, Andersen KJ, Knudsen AR, Nyengaard JR, Hamilton-Dutoit S, Mortensen FV (2016) Liver regeneration is dependent on the extent of hepatectomy. J Surg Res 205:76–84
Gruttadauria S, Parikh V, Pagano D et al (2012) Early regeneration of the remnant liver volume after right hepatectomy for living donation: a multiple regression analysis. Liver Transpl 18:907–913
Ma HY, Dong L, Quan SZ, Li RY, Wang XR (2021) Comparison of four markers of hepatic fibrosis and hepatic function indices in patients with liver cirrhosis and hepatoma. Ann Palliat Med 10:4108–4121
Cheemerla S, Balakrishnan M (2021) Global epidemiology of chronic liver disease. Clin Liver Dis (Hoboken) 17:365–370
Nadalin S, Testa G, Malagó M et al (2004) Volumetric and functional recovery of the liver after right hepatectomy for living donation. Liver Transpl 10:1024–1029
Yokoi H, Isaji S, Yamagiwa K et al (2005) Donor outcome and liver regeneration after right-lobe graft donation. Transpl Int 18:915–922
Gong WF, Zhong JH, Lu Z et al (2019) Evaluation of liver regeneration and post-hepatectomy liver failure after hemihepatectomy in patients with hepatocellular carcinoma. Biosci Rep 39. https://doi.org/10.1042/BSR20190088
Haga J, Shimazu M, Wakabayashi G et al (2008) Liver regeneration in donors and adult recipients after living donor liver transplantation. Liver Transpl 14:1718–1724
Funding
This study has received funding by China Postdoctoral Science Foundation (2021M692289), Science and Technology Support Program of Sichuan Province (Grant number 2021YFS0144, Grant number 2021YFS0021), and Post-Doctor Research Project, West China Hospital, Sichuan University (Grant number 2020HXBH130).
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The scientific guarantor of this publication is Dr. Bin Song.
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One of the authors (Lisha Nie) is an employee of GE Healthcare. The remaining authors declare no relationships with any companies whose products or services may be related to the subject matter of the article.
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Li, Q., Zhang, T., Che, F. et al. Intravoxel incoherent motion diffusion weighted imaging for preoperative evaluation of liver regeneration after hepatectomy in hepatocellular carcinoma. Eur Radiol 33, 5222–5235 (2023). https://doi.org/10.1007/s00330-023-09496-1
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DOI: https://doi.org/10.1007/s00330-023-09496-1