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Preoperative MRI features for characterization of vessels encapsulating tumor clusters and microvascular invasion in hepatocellular carcinoma

  • Hepatobiliary
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Abstract

Purpose

This study aimed to analyze imaging features based on preoperative dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) for the identification of vessels encapsulating tumor clusters (VETC)-microvascular invasion (MVI) in hepatocellular carcinoma (HCC), VM-HCC pattern.

Methods

Patients who underwent hepatectomy and preoperative DCE-MRI between January 2015 and March 2021 were retrospectively analyzed. Clinical and imaging features related to VM-HCC (VETC + /MVI-, VETC-/MVI +, VETC + /MVI +) and Non-VM-HCC (VETC-/MVI-) were determined by multivariable logistic regression analyses. Early and overall recurrence were determined using the Kaplan–Meier survival curve. Indicators of early and overall recurrence were identified using the Cox proportional hazard regression model.

Results

In total, 221 patients (177 men, 44 women; median age, 60 years; interquartile range, 52–66 years) were evaluated. The multivariable logistic regression analyses revealed fetoprotein > 400 ng/mL (odds ratio [OR] = 2.17, 95% confidence interval [CI] 1.07, 4.41, p = 0.033), intratumor vascularity (OR 2.15, 95% CI 1.07, 4.31, p = 0.031), and enhancement pattern (OR 2.71, 95% CI 1.17, 6.03, p = 0.019) as independent predictors of VM-HCC. In Kaplan–Meier survival analysis, intratumor vascularity was associated with early and overall recurrence (p < 0.05).

Conclusion

Based on DCE-MRI, intratumor vascularity can be used to characterize VM-HCC and is of prognostic significance for recurrence in patients with HCC.

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Abbreviations

HCC:

Hepatocellular carcinoma

MVI:

Microvascular invasion

VETC:

Vessels encapsulating tumor clusters

VM-HCC:

VETC-MVI-HCC

DCE-MRI:

Dynamic contrast-enhanced MRI

RFS:

Recurrence-free survival

HR:

Hazard ratio

OR:

Odds ratio

CI:

Confidence interval

ALT:

Alanine transaminase

AST:

Aspartate transaminase

GGT:

γ-Glutamyl transpeptidase

ALB:

Albumin

PT:

Plasma prothrombin time

AFP:

Serum α-fetoprotein

BCLC:

Barcelona Clinic Liver Cancer

HBV:

Hepatitis B virus

HCV:

Hepatitis C virus

APHE:

Arterial phase hyperenhancement

Rim APHE:

Rim arterial phase hyperenhancement

Non-rim dh-APHE:

Non-rim diffuse and heterogeneous arterial phase hyperenhancement

Non-rim sc-APHE:

Non-rim scattered arterial phase hyperenhancement

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Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Author notes

  1. Wenbin Ji

    Present address: Department of Radiology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, 150 Ximen St, Linhai, Taizhou, 317000, Zhejiang, China

  2. Jiawen Yang and Xue Dong have contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, 150 Ximen St, Linhai, Taizhou, 317000, Zhejiang, China

    Jiawen Yang, Guanliang Wang, Jinyao Chen, Binhao Zhang, Wenting Pan & Huangqi Zhang

  2. Department of Radiology, Taizhou Hospital, Zhejiang University, Taizhou, 318000, Zhejiang, China

    Xue Dong

  3. Department of Radiology, Taizhou Hospital of Zhejiang Province, Shaoxing University, Taizhou, 318000, Zhejiang, China

    Shengze Jin

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Appendices

Appendix E1 MRI protocol

MR images was performed with a 1.5-T scanner (Signa Twinspeed, GE Healthcare) and an 8-channel phased-array software coil. The MRI protocols were as follows: (1) for the breath-hold axial T1-weighted image, the protocol consisted of a 2D fast spoiled gradient-echo (FSPGR) sequence with a repetition time (TR) of 185 ms, an echo time (TE) of 4.7 ms (in phase) and 2.1 ms (out of phase), a flip angle of 80°, a matrix size of 288 × 150, a field of view (FOV) of 38 × 38 cm, a slice thickness of 8 mm, an space gap of 2 mm; (2) for the axial T2-weighted image, the protocol consisted of a respiratory-triggered fat-saturated fast recovery fast spin-echo(FRFSE) sequence with a TR of 6000 ms, a TE of 85 ms, a matrix size of 288 × 224, a FOV of 40 × 30 cm, a slice thickness of 8 mm, an space gap of 2 mm; (3) the axial diffusion-weighted image (DWI) was performed before contrast agent injection using the following protocol: a single shot spin-echo echo-planar imaging (SE-EPI) sequence with a fat-saturated technique respiratory-triggered (RTR), a b value of 0 s/mm2 and 500 s/mm2, a TR of 6667 ms, a TE of 67.5 ms, a matrix size of 128 × 128, a FOV of 38 × 38 cm, a slice thickness of 8 mm, an space gap of 2 mm (4) for the breath-hold axial dynamic contrast-enhanced fat-suppressed T1-weighted image, the protocol consisted of a 3D Liver Acquisition With Volume Acceleration (3D-LAVA) sequence, a TR of 3.2 ms, a TE of 1.5 ms, a flip angle of 12°, a matrix size of 288 × 170, a FOV of 315 × 350, a slice thickness of 5 mm; an space gap of 2.5 mm.

MR images were performed with a 3.0-T scanner (Discover MR750, GE Healthcare) and a 8-channel phased-array software coil. The MRI protocols were as follows: (1) for the breath-hold axial T1-weighted image, the protocol consisted of a 3D Liver Acquisition With Volume Acceleration (3D-LAVA) with a repetition time (TR) of 3.7 ms, an echo time (TE) of 2.2 ms (in phase) and1.1 ms (out of phase), a flip angle of 12°, a matrix size of 260 × 224, a field of view (FOV) of 40 × 36 cm, a slice thickness of 6 mm (2) for the axial T2-weighted image, the protocol consisted of a respiratory-triggered fat-saturated fast spin-echo(FSE) sequence with a TR of 14117 ms, a TE of 79 ms, a matrix size of 320 × 320, a FOV of 40 × 40 cm, a slice thickness of 6 mm, an space gap of 1 mm; (3) the axial diffusion-weighted image (DWI) was performed before contrast agent injection using the following protocol: a single shot spin-echo echo-planar imaging (SE-EPI) sequence with a fat-saturated technique respiratory-triggered (RTR), a b value of 0 s/mm2 and 800 s/mm2, a TR of 8571 ms, a TE of 47.5 ms, a matrix size of 128 × 96, a FOV of 40 × 32 cm, a slice thickness of 6 mm, an space gap of 1 mm; (4) for the breath-hold axial dynamic contrast-enhanced fat-suppressed T1-weighted image, the protocol consisted of a 3D Liver Acquisition With Volume Acceleration (3D-LAVA) sequence, a TR of 3.7 ms, a TE of 1.7 ms, a slice thickness of 6 mm, a flip angle of 12°, a matrix size of 260 × 224, a field of view (FOV) of 40 × 36(324 × 360)cm, a slice thickness of 6 mm; an space gap of 1 mm.

After a bolus injection of 0.2 mmol/kg body weight of Gadopentetate Dimeglumine (Gd-DTPA, Magnevist, Bayer Schering, Berlin, Germany) and images were obtained in the hepatic arterial phases (20 s), portal venous phases (60 s), and delayed phases (180 s).

No contrast-enhanced imaging examination was performed within 48 h before MRI examination, and fasting was performed within 4 h before the examination. Before the scan, the patient was trained to breathe, held his breath at the end of the breath, and was examined in the supine position.

Appendix E2 MRI features definition and evaluation

The MR imaging features included (1) Main tumor size: the largest outer-edge-to-outer-edge dimension of the main lesion; (2) Intratumor necrosis: a hypoattenuated central area on the non-enhanced images without enhancement during the postcontrast phases; (3) Substantial necrosis: spin-echo T2-weighted images without enhancement on postcontrast T1-weighted images and involving at least 20% of the tumor area at the level of the largest cross-sectional diameter; (4) Blood products in mass: a hyperintense area on T1-weighted images, with variable signal intensity on T2-weighted images; (5) Fat in mass: more than that in adjacent liver, defined as decreased out-of-phase T1-weighted signal intensity compared with in-phase T1-weighted signal intensity; (6) Rim arterial phase hyperenhancement (Rim APHE): Spatially defined subtype of APHE in which arterial phase enhancement is most pronounced in observation periphery. (7) Non-rim arterial phase hyperenhancement (Non-rim-APHE): Non-rim-like enhancement in arterial phase unequivocally greater in whole or in part than liver. Enhancing part must be higher in attenuation or intensity than liver in arterial phase. (8)/(9) Non-rim APHE can be diffuse and heterogeneous (non-uniform), scattered (patchy, spotty), which are called non-rim dh-APHE and non-rim sc-APHE; (10) Arterial peritumoral enhancement: detectable crescent- or polygonal-shaped enhancement surrounding the border on the arterial phase images, which becomes isointense during the delayed phase (11) intratumor vascularity which is the persistence of discrete arterial enhancement within the tumor in the arterial phase; (12) Non-peripheral washout: Non-peripheral visually assessed temporal reduction in enhancement in whole or in part relative to composite liver tissue from earlier to later phase resulting in hypoenhancement in the extracellular phase. (13) Enhancing capsule: Smooth, uniform, sharp border around most or all of an observation, unequivocally thicker or more conspicuous than fibrotic tissue around background nodules, and visible as enhancing rim in portal venous phase, delayed phase, or transitional phase. (14) Tumor in vein: defined as unequivocal enhancing soft tissue in the portal vein or its branches. (15) Tumor margin: classified as smooth and non-smooth. (16) Enhancement pattern: classified as typical dynamic enhancement, with arterial hypervascularity, and portal washout, as well as atypical dynamic enhancement.

All Multi-phasic contrast-enhanced MR images were retrospectively interpreted by 2 radiologists (C.J. and W.G. with 14 and 15 years of experience in abdominal imaging, respectively) who were blinded to the clinical and pathological data. When there was a discrepancy between the two radiologists, a third experienced radiologist (W.J. with 21 years of experience in abdominal imaging) was consulted. If a patient had multiple tumor lesions, the largest lesion (main tumor) was assessed.

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Yang, J., Dong, X., Wang, G. et al. Preoperative MRI features for characterization of vessels encapsulating tumor clusters and microvascular invasion in hepatocellular carcinoma. Abdom Radiol 48, 554–566 (2023). https://doi.org/10.1007/s00261-022-03740-w

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