Skip to main content
Top
Published in: European Radiology 10/2019

01-10-2019 | Magnetic Resonance Imaging | Oncology

IVIM improves preoperative assessment of microvascular invasion in HCC

Authors: Yi Wei, Zixing Huang, Hehan Tang, Liping Deng, Yuan Yuan, Jiaxing Li, Dongbo Wu, Xiaocheng Wei, Bin Song

Published in: European Radiology | Issue 10/2019

Login to get access

Abstract

Purpose

To prospectively evaluate the potential role of intravoxel incoherent motion (IVIM) and conventional radiologic features for preoperative prediction of microvascular invasion (MVI) in patients with hepatocellular carcinoma (HCC).

Methods

Institutional review board approval and written informed consent were obtained for this study. A cohort comprising 115 patients with 135 newly diagnosed HCCs between January 2016 and April 2017 were evaluated. Two radiologists independently reviewed the radiologic features and the apparent diffusion coefficient (ADC), true diffusion coefficient (D), pseudodiffusion coefficient (D*), and pseudodiffusion component fraction (f) were also measured. Interobserver agreement was checked and univariate and multivariate logistic regressions were used for screening the risk factors. Receiver operating characteristics (ROC) curve analyses were performed to evaluate the diagnostic performance.

Results

Features significantly related to MVI of HCC at univariate analysis were reduced ADC (odds ratio, 0.341; 95% CI, 0.211–0.552; p < 0.001), D (odds ratio, 0.141; 95% CI, 0.067–0.299; p < 0.001), and irregular circumferential enhancement (odds ratio, 9.908; 95% CI, 3.776–25.996; p < 0.001). At multivariate analysis, only D value (odds ratio, 0.096; 95% CI, 0.025–0.364; p < 0.001) was the independent risk factor for MVI of HCC. The mean D value for MVI of HCC showed an area under ROC curves of 0.815 (95% CI, 0.740–0.877).

Conclusion

IVIM model–derived D value is superior to ADC measured with mono-exponential model for evaluating the MVI of HCC. Among MR imaging features, tumor margin, enhancement pattern, tumor capsule, and peritumoral enhancement were not predictive for MVI.

Key Points

• Diffusion MRI is useful for non-invasively evaluating the microvascular invasion of hepatocellular carcinoma.
• IVIM model is advantageous over mono-exponential model for assessing the microvascular invasion of hepatocellular carcinoma.
• Decreased D value was the independent risk factor for predicting MVI of HCC.
Literature
1.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108CrossRef Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin 65:87–108CrossRef
2.
4.
go back to reference Hirokawa F, Hayashi M, Asakuma M, Shimizu T, Inoue Y, Uchiyama K (2016) Risk factors and patterns of early recurrence after curative hepatectomy for hepatocellular carcinoma. Surg Oncol 25:24–29CrossRefPubMed Hirokawa F, Hayashi M, Asakuma M, Shimizu T, Inoue Y, Uchiyama K (2016) Risk factors and patterns of early recurrence after curative hepatectomy for hepatocellular carcinoma. Surg Oncol 25:24–29CrossRefPubMed
5.
go back to reference Rodriguez-Peralvarez M, Luong TV, Andreana L, Meyer T, Dhillon AP, Burroughs AK (2013) A systematic review of microvascular invasion in hepatocellular carcinoma: diagnostic and prognostic variability. Ann Surg Oncol 20:325–339CrossRef Rodriguez-Peralvarez M, Luong TV, Andreana L, Meyer T, Dhillon AP, Burroughs AK (2013) A systematic review of microvascular invasion in hepatocellular carcinoma: diagnostic and prognostic variability. Ann Surg Oncol 20:325–339CrossRef
6.
go back to reference Witjes CD, Willemssen FE, Verheij J et al (2012) Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging 36:641–647CrossRefPubMed Witjes CD, Willemssen FE, Verheij J et al (2012) Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging 36:641–647CrossRefPubMed
8.
go back to reference Pawlik TM, Gleisner AL, Anders RA, Assumpcao L, Maley W, Choti MA (2007) Preoperative assessment of hepatocellular carcinoma tumor grade using needle biopsy: implications for transplant eligibility. Ann Surg 245:435–442CrossRefPubMedPubMedCentral Pawlik TM, Gleisner AL, Anders RA, Assumpcao L, Maley W, Choti MA (2007) Preoperative assessment of hepatocellular carcinoma tumor grade using needle biopsy: implications for transplant eligibility. Ann Surg 245:435–442CrossRefPubMedPubMedCentral
9.
go back to reference Ramos Rubio E, Llado Garriga L (2010) [Usefulness of pre-surgical biopsy in selecting patients with hepatocellular carcinoma for liver transplant]. Cir Esp 87:133–138CrossRefPubMed Ramos Rubio E, Llado Garriga L (2010) [Usefulness of pre-surgical biopsy in selecting patients with hepatocellular carcinoma for liver transplant]. Cir Esp 87:133–138CrossRefPubMed
10.
11.
go back to reference Hirokawa F, Hayashi M, Miyamoto Y et al (2014) Outcomes and predictors of microvascular invasion of solitary hepatocellular carcinoma. Hepatol Res 44:846–853CrossRefPubMed Hirokawa F, Hayashi M, Miyamoto Y et al (2014) Outcomes and predictors of microvascular invasion of solitary hepatocellular carcinoma. Hepatol Res 44:846–853CrossRefPubMed
12.
go back to reference Renzulli M, Brocchi S, Cucchetti A et al (2016) Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology 279:432–442CrossRefPubMed Renzulli M, Brocchi S, Cucchetti A et al (2016) Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology 279:432–442CrossRefPubMed
13.
go back to reference Jiang HY, Chen J, Xia CC, Cao LK, Duan T, Song B (2018) Noninvasive imaging of hepatocellular carcinoma: from diagnosis to prognosis. World J Gastroenterol 24:2348–2362CrossRefPubMedPubMedCentral Jiang HY, Chen J, Xia CC, Cao LK, Duan T, Song B (2018) Noninvasive imaging of hepatocellular carcinoma: from diagnosis to prognosis. World J Gastroenterol 24:2348–2362CrossRefPubMedPubMedCentral
15.
go back to reference Yaprak O, Acar S, Ertugrul G, Dayangac M (2018) Role of pre-transplant 18F-FDG PET/CT in predicting hepatocellular carcinoma recurrence after liver transplantation. World J Gastrointest Oncol 10:336–343CrossRefPubMedPubMedCentral Yaprak O, Acar S, Ertugrul G, Dayangac M (2018) Role of pre-transplant 18F-FDG PET/CT in predicting hepatocellular carcinoma recurrence after liver transplantation. World J Gastrointest Oncol 10:336–343CrossRefPubMedPubMedCentral
17.
go back to reference Wei Y, Gao F, Wang M et al (2019) Intravoxel incoherent motion diffusion-weighted imaging for assessment of histologic grade of hepatocellular carcinoma: comparison of three methods for positioning region of interest. Eur Radiol 29:535–544CrossRefPubMed Wei Y, Gao F, Wang M et al (2019) Intravoxel incoherent motion diffusion-weighted imaging for assessment of histologic grade of hepatocellular carcinoma: comparison of three methods for positioning region of interest. Eur Radiol 29:535–544CrossRefPubMed
18.
go back to reference Xu P, Zeng M, Liu K, Shan Y, Xu C, Lin J (2014) Microvascular invasion in small hepatocellular carcinoma: is it predictable with preoperative diffusion-weighted imaging? J Gastroenterol Hepatol 29:330–336CrossRefPubMed Xu P, Zeng M, Liu K, Shan Y, Xu C, Lin J (2014) Microvascular invasion in small hepatocellular carcinoma: is it predictable with preoperative diffusion-weighted imaging? J Gastroenterol Hepatol 29:330–336CrossRefPubMed
19.
go back to reference Valerio M, Zini C, Fierro D et al (2016) 3T multiparametric MRI of the prostate: does intravoxel incoherent motion diffusion imaging have a role in the detection and stratification of prostate cancer in the peripheral zone? Eur J Radiol 85:790–794CrossRefPubMed Valerio M, Zini C, Fierro D et al (2016) 3T multiparametric MRI of the prostate: does intravoxel incoherent motion diffusion imaging have a role in the detection and stratification of prostate cancer in the peripheral zone? Eur J Radiol 85:790–794CrossRefPubMed
20.
go back to reference Marzi S, Piludu F, Sanguineti G et al (2017) The prediction of the treatment response of cervical nodes using intravoxel incoherent motion diffusion-weighted imaging. Eur J Radiol 92:93–102CrossRefPubMed Marzi S, Piludu F, Sanguineti G et al (2017) The prediction of the treatment response of cervical nodes using intravoxel incoherent motion diffusion-weighted imaging. Eur J Radiol 92:93–102CrossRefPubMed
21.
go back to reference Iima M, Le Bihan D (2016) Clinical intravoxel incoherent motion and diffusion MR imaging: past, present, and future. Radiology 278(1):13–32CrossRefPubMed Iima M, Le Bihan D (2016) Clinical intravoxel incoherent motion and diffusion MR imaging: past, present, and future. Radiology 278(1):13–32CrossRefPubMed
22.
go back to reference Meeus EM, Zarinabad N, Manias KA et al (2018) Diffusion-weighted MRI and intravoxel incoherent motion model for diagnosis of pediatric solid abdominal tumors. J Magn Reson Imaging 47:1475–1486CrossRefPubMed Meeus EM, Zarinabad N, Manias KA et al (2018) Diffusion-weighted MRI and intravoxel incoherent motion model for diagnosis of pediatric solid abdominal tumors. J Magn Reson Imaging 47:1475–1486CrossRefPubMed
23.
go back to reference Yuan SX, Yang F, Yang Y et al (2012) Long noncoding RNA associated with microvascular invasion in hepatocellular carcinoma promotes angiogenesis and serves as a predictor for hepatocellular carcinoma patients’ poor recurrence-free survival after hepatectomy. Hepatology 56(6):2231–2241CrossRefPubMed Yuan SX, Yang F, Yang Y et al (2012) Long noncoding RNA associated with microvascular invasion in hepatocellular carcinoma promotes angiogenesis and serves as a predictor for hepatocellular carcinoma patients’ poor recurrence-free survival after hepatectomy. Hepatology 56(6):2231–2241CrossRefPubMed
24.
go back to reference Nougaret S, Vargas HA, Lakhman Y et al (2016) Intravoxel incoherent motion-derived histogram metrics for assessment of response after combined chemotherapy and radiation therapy in rectal cancer: initial experience and comparison between single-section and volumetric analyses. Radiology 280:446–454CrossRefPubMedPubMedCentral Nougaret S, Vargas HA, Lakhman Y et al (2016) Intravoxel incoherent motion-derived histogram metrics for assessment of response after combined chemotherapy and radiation therapy in rectal cancer: initial experience and comparison between single-section and volumetric analyses. Radiology 280:446–454CrossRefPubMedPubMedCentral
25.
go back to reference Suo S, Lin N, Wang H et al (2015) Intravoxel incoherent motion diffusion-weighted MR imaging of breast cancer at 3.0 tesla: comparison of different curve-fitting methods. J Magn Reson Imaging 42:362–370CrossRefPubMed Suo S, Lin N, Wang H et al (2015) Intravoxel incoherent motion diffusion-weighted MR imaging of breast cancer at 3.0 tesla: comparison of different curve-fitting methods. J Magn Reson Imaging 42:362–370CrossRefPubMed
26.
go back to reference Shen N, Zhao L, Jiang J et al (2016) Intravoxel incoherent motion diffusion-weighted imaging analysis of diffusion and microperfusion in grading gliomas and comparison with arterial spin labeling for evaluation of tumor perfusion. J Magn Reson Imaging 44:620–632CrossRefPubMed Shen N, Zhao L, Jiang J et al (2016) Intravoxel incoherent motion diffusion-weighted imaging analysis of diffusion and microperfusion in grading gliomas and comparison with arterial spin labeling for evaluation of tumor perfusion. J Magn Reson Imaging 44:620–632CrossRefPubMed
27.
go back to reference Song XL, Kang HK, Jeong GW et al (2016) Intravoxel incoherent motion diffusion-weighted imaging for monitoring chemotherapeutic efficacy in gastric cancer. World J Gastroenterol 22:5520–5531CrossRefPubMedPubMedCentral Song XL, Kang HK, Jeong GW et al (2016) Intravoxel incoherent motion diffusion-weighted imaging for monitoring chemotherapeutic efficacy in gastric cancer. World J Gastroenterol 22:5520–5531CrossRefPubMedPubMedCentral
28.
go back to reference Woo S, Lee JM, Yoon JH, Joo I, Han JK, Choi BI (2014) Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. Radiology 270:758–767CrossRefPubMed Woo S, Lee JM, Yoon JH, Joo I, Han JK, Choi BI (2014) Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. Radiology 270:758–767CrossRefPubMed
29.
go back to reference Joo I, Lee JM, Han JK, Choi BI (2014) Intravoxel incoherent motion diffusion-weighted MR imaging for monitoring the therapeutic efficacy of the vascular disrupting agent CKD-516 in rabbit VX2 liver tumors. Radiology 272:417–426CrossRefPubMed Joo I, Lee JM, Han JK, Choi BI (2014) Intravoxel incoherent motion diffusion-weighted MR imaging for monitoring the therapeutic efficacy of the vascular disrupting agent CKD-516 in rabbit VX2 liver tumors. Radiology 272:417–426CrossRefPubMed
30.
go back to reference Lee Y, Lee SS, Kim N et al (2015) Intravoxel incoherent motion diffusion-weighted MR imaging of the liver: effect of triggering methods on regional variability and measurement repeatability of quantitative parameters. Radiology 274:405–415CrossRefPubMed Lee Y, Lee SS, Kim N et al (2015) Intravoxel incoherent motion diffusion-weighted MR imaging of the liver: effect of triggering methods on regional variability and measurement repeatability of quantitative parameters. Radiology 274:405–415CrossRefPubMed
31.
go back to reference Li H, Zhang J, Zheng Z et al (2018) Preoperative histogram analysis of intravoxel incoherent motion (IVIM) for predicting microvascular invasion in patients with single hepatocellular carcinoma. Eur J Radiol 105:65–71CrossRefPubMed Li H, Zhang J, Zheng Z et al (2018) Preoperative histogram analysis of intravoxel incoherent motion (IVIM) for predicting microvascular invasion in patients with single hepatocellular carcinoma. Eur J Radiol 105:65–71CrossRefPubMed
32.
go back to reference Amin MB, Edge SB, Greene FL et al (2017) AJCC cancer staging manual, 8th edn. Springer, New YorkCrossRef Amin MB, Edge SB, Greene FL et al (2017) AJCC cancer staging manual, 8th edn. Springer, New YorkCrossRef
33.
go back to reference Jerjir N, Bruyneel L, Haspeslagh M, Quenet S, Coenegrachts K (2017) Intravoxel incoherent motion and dynamic contrast-enhanced MRI for differentiation between hepatocellular adenoma and focal nodular hyperplasia. Br J Radiol 90:20170007CrossRefPubMedPubMedCentral Jerjir N, Bruyneel L, Haspeslagh M, Quenet S, Coenegrachts K (2017) Intravoxel incoherent motion and dynamic contrast-enhanced MRI for differentiation between hepatocellular adenoma and focal nodular hyperplasia. Br J Radiol 90:20170007CrossRefPubMedPubMedCentral
34.
go back to reference Choi IY, Lee SS, Sung YS et al (2017) Intravoxel incoherent motion diffusion-weighted imaging for characterizing focal hepatic lesions: correlation with lesion enhancement. J Magn Reson Imaging 45:1589–1598CrossRefPubMed Choi IY, Lee SS, Sung YS et al (2017) Intravoxel incoherent motion diffusion-weighted imaging for characterizing focal hepatic lesions: correlation with lesion enhancement. J Magn Reson Imaging 45:1589–1598CrossRefPubMed
35.
go back to reference Klauss M, Mayer P, Maier-Hein K et al (2016) IVIM-diffusion-MRI for the differentiation of solid benign and malign hypervascular liver lesions-evaluation with two different MR scanners. Eur J Radiol 85:1289–1294CrossRefPubMed Klauss M, Mayer P, Maier-Hein K et al (2016) IVIM-diffusion-MRI for the differentiation of solid benign and malign hypervascular liver lesions-evaluation with two different MR scanners. Eur J Radiol 85:1289–1294CrossRefPubMed
36.
go back to reference Shirota N, Saito K, Sugimoto K, Takara K, Moriyasu F, Tokuuye K (2016) Intravoxel incoherent motion MRI as a biomarker of sorafenib treatment for advanced hepatocellular carcinoma: a pilot study. Cancer Imaging 16(1) Shirota N, Saito K, Sugimoto K, Takara K, Moriyasu F, Tokuuye K (2016) Intravoxel incoherent motion MRI as a biomarker of sorafenib treatment for advanced hepatocellular carcinoma: a pilot study. Cancer Imaging 16(1)
37.
go back to reference Wang WT, Yang L, Yang ZX et al (2018) Assessment of microvascular invasion of hepatocellular carcinoma with diffusion kurtosis imaging. Radiology 286:571–580CrossRefPubMed Wang WT, Yang L, Yang ZX et al (2018) Assessment of microvascular invasion of hepatocellular carcinoma with diffusion kurtosis imaging. Radiology 286:571–580CrossRefPubMed
38.
go back to reference Matsui O, Kobayashi S, Sanada J et al (2011) Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging 36:264–272CrossRefPubMedPubMedCentral Matsui O, Kobayashi S, Sanada J et al (2011) Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging 36:264–272CrossRefPubMedPubMedCentral
39.
go back to reference Jerome NP, d’Arcy JA, Feiweier T et al (2016) Extended T2-IVIM model for correction of TE dependence of pseudo-diffusion volume fraction in clinical diffusion-weighted magnetic resonance imaging. Phys Med Biol 61:N667–n680CrossRefPubMedPubMedCentral Jerome NP, d’Arcy JA, Feiweier T et al (2016) Extended T2-IVIM model for correction of TE dependence of pseudo-diffusion volume fraction in clinical diffusion-weighted magnetic resonance imaging. Phys Med Biol 61:N667–n680CrossRefPubMedPubMedCentral
41.
go back to reference Chou CT, Chen RC, Lin WC, Ko CJ, Chen CB, Chen YL (2014) Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. AJR Am J Roentgenol 203:W253–W259CrossRefPubMed Chou CT, Chen RC, Lin WC, Ko CJ, Chen CB, Chen YL (2014) Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. AJR Am J Roentgenol 203:W253–W259CrossRefPubMed
42.
go back to reference Mürtz P, Sprinkart AM, Reick M et al (2018) Accurate IVIM model-based liver lesion characterisation can be achieved with only three b-value DWI. Eur Radiol 28:4418–4428CrossRefPubMed Mürtz P, Sprinkart AM, Reick M et al (2018) Accurate IVIM model-based liver lesion characterisation can be achieved with only three b-value DWI. Eur Radiol 28:4418–4428CrossRefPubMed
Metadata
Title
IVIM improves preoperative assessment of microvascular invasion in HCC
Authors
Yi Wei
Zixing Huang
Hehan Tang
Liping Deng
Yuan Yuan
Jiaxing Li
Dongbo Wu
Xiaocheng Wei
Bin Song
Publication date
01-10-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-019-06088-w

Other articles of this Issue 10/2019

European Radiology 10/2019 Go to the issue