Abdominal Radiology

, Volume 44, Issue 9, pp 3049–3057 | Cite as

Incomplete tumor capsule on preoperative imaging reveals microvascular invasion in hepatocellular carcinoma: a systematic review and meta-analysis

  • Fei Zhu
  • Fan Yang
  • Jing Li
  • Weixia ChenEmail author
  • Weilin Yang



Microvascular invasion (MVI), which is difficult to diagnose before surgery, is a major factor affecting postoperative recurrence in patients with hepatocellular carcinoma (HCC). The relationship between the radiological tumor capsule and MVI is controversial. This study aimed to evaluate the association between the tumor capsule and MVI.


We searched Medline (by PubMed) and Embase (by OvidSP). Two review authors independently screened titles and abstracts, selected studies about MVI prediction with radiologic tumor capsule and studies with enough data for extracted, assessed the methodological quality and collected data. Summary results were presented as the diagnostic odds ratio (DOR), sensitivity, specificity, and 95% confidence interval.


Fifteen studies with 2038 patients were included; fourteen studies, including 1331 patients, with no significant heterogeneity indicated no relationship between absent tumor capsule and MVI [DOR = 0.90 (0.64, 1.26)]. Six studies, including 541 patients, with no significant heterogeneity showed incomplete capsule could be used to predict MVI of HCC preoperatively [DOR = 1.85 (1.13, 3.04)]. The overall sensitivity and specificity estimate were 0.50 (0.37, 0.64) and 0.64 (0.53, 0.74), respectively. Eight studies, including 1349 patients, with highly significant heterogeneity revealed that complete capsule could be a protective factor for MVI [DOR = 1.97 (1.01, 3.86)].


For MVI of HCC, incomplete tumor capsule is a risk factor, while a complete tumor capsule might be a protective factor. However, absent capsule doesn’t show significant relationship with MVI. This might be due to combination of the risk and protective effects of present capsule in MVI.


Hepatocellular carcinoma Microvascular invasion Capsule Magnetic resonance imaging Computed tomography 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

Supplementary material

261_2019_2126_MOESM1_ESM.pdf (243 kb)
Supplementary material 1 (PDF 243 kb)


  1. 1.
    Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA: a cancer journal for clinicians 65 (2):87-108.
  2. 2.
    CCong WM, Bu H, Chen J, Dong H, Zhu YY, Feng LH, Chen J (2016) Practice guidelines for the pathological diagnosis of primary liver cancer: 2015 update. World J Gastroenterol 22 (42):9279-9287. CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Rodríguez-Perálvarez 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. Annals of Surgical Oncology 20 (1):325-339. CrossRefPubMedGoogle Scholar
  4. 4.
    Tsai TJ, Chau GY, Lui WY, Tsay SH, King KL, Loong CC, Hsia CY, Wu CW (2000) Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery 127 (6):603-608. CrossRefPubMedGoogle Scholar
  5. 5.
    Lim JH, Choi D, Park CK, Lee WJ, Lim HK (2006) Encapsulated hepatocellular carcinoma: CT-pathologic correlations. European Radiology 16 (10):2326-2333CrossRefPubMedGoogle Scholar
  6. 6.
    Adachi E, Maeda T, Kajiyama K, Kinukawa N, Matsumata T, Sugimachi K, Tsuneyoshi M (1996) Factors correlated with portal venous invasion by hepatocellular carcinoma: univariate and multivariate analyses of 232 resected cases without preoperative treatments. Cancer 77 (10):2022-2031.<2022::aid-cncr9>;2-s CrossRefPubMedGoogle Scholar
  7. 7.
    CChou CT, Chen RC, Lee CW, Ko CJ, Wu HK, Chen YL (2012) Prediction of microvascular invasion of hepatocellular carcinoma by pre-operative CT imaging. Br J Radiol 85 (1014):778-783. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Zhao H, Hua Y, Dai T, He J, Tang M, Fu X, Mao L, Jin H, Qiu Y (2017) Development and validation of a novel predictive scoring model for microvascular invasion in patients with hepatocellular carcinoma. European Journal of Radiology 88:32-40CrossRefPubMedGoogle Scholar
  9. 9.
    Zhang W, Wang P, Wang L, Liu L, Chen J, Su D (2018) Preoperative computed tomography and serum alpha-fetoprotein to predict microvascular invasion in hepatocellular carcinoma. Medicine (Baltimore) 97 (27):e11402. CrossRefGoogle Scholar
  10. 10.
    Ahn SJ, Kim JH, Park SJ, Kim ST, Han JK (2019) Hepatocellular carcinoma: preoperative gadoxetic acid-enhanced MR imaging can predict early recurrence after curative resection using image features and texture analysis. Abdominal radiology (New York) 44 (2):539-548. CrossRefGoogle Scholar
  11. 11.
    An C, Kim MJ (2018) Imaging features related with prognosis of hepatocellular carcinoma. Abdom Radiol 44:509–516. CrossRefGoogle Scholar
  12. 12.
    Witjes CD, Willemssen FE, Verheij J, van der Veer SJ, Hansen BE, Verhoef C, de Man RA, Ijzermans JN (2012) Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging 36 (3):641-647. CrossRefPubMedGoogle Scholar
  13. 13.
    Kim H, Park MS, Choi JY, Park YN, Kim MJ, Kim KS, Choi JS, Han KH, Kim E, Kim KW (2009) Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol 19 (7):1744-1751. CrossRefGoogle Scholar
  14. 14.
    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 American journal of roentgenology 203 (3):W253-259. CrossRefPubMedGoogle Scholar
  15. 15.
    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 (2):330-336. CrossRefGoogle Scholar
  16. 16.
    Ahn SY, Lee JM, Joo I, Lee ES, Lee SJ, Cheon GJ, Han JK, Choi BI (2015) Prediction of microvascular invasion of hepatocellular carcinoma using gadoxetic acid-enhanced MR and 18F-FDG PET/CT. Abdominal Imaging 40 (4):843-851. CrossRefPubMedGoogle Scholar
  17. 17.
    Lee S, Kim SH, Lee JE, Sinn DH, Park CK (2017) Preoperative gadoxetic acid–enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. Journal of Hepatology 67 (3):526-534. CrossRefPubMedGoogle Scholar
  18. 18.
    Reginelli A, Vanzulli A, Sgrazzutti C, Caschera L, Serra N, Raucci A, Urraro F, Cappabianca S (2017) Vascular microinvasion from hepatocellular carcinoma: CT findings and pathologic correlation for the best therapeutic strategies. Medical oncology (Northwood, London, England) 34 (5):93. CrossRefGoogle Scholar
  19. 19.
    Yang C, Wang H, Sheng R, Ji Y, Rao S, Zeng M (2017) Microvascular invasion in hepatocellular carcinoma: is it predictable with a new, preoperative application of diffusion-weighted imaging? Clinical Imaging 41:101-105. CrossRefPubMedGoogle Scholar
  20. 20.
    Zhou X, Wang G, Gao Y, Yu L, Li W, Jiao L, Li Z (2017) Predict microvascular invasion in hepatocellular carcinoma by dynamic contrast-enhanced magnetic resonance imaging in patients with hepatitis B virus. International Journal of Clinical and Experimental Medicine 10 (8):11728-11738Google Scholar
  21. 21.
    Huang M, Liao B, Xu P, Cai H, Huang K, Dong Z (2018) Prediction of Microvascular Invasion in Hepatocellular Carcinoma: Preoperative Gd-EOB-DTPA-Dynamic Enhanced MRI and Histopathological Correlation. Contrast Media & Molecular Imaging 2018:9674565. CrossRefGoogle Scholar
  22. 22.
    Ariizumi S-i, Kitagawa K, Kotera Y, Takahashi Y, Katagiri S, Kuwatsuru R, Yamamoto M (2011) A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. Journal of Hepato-Biliary-Pancreatic Sciences 18 (4):575-585. CrossRefPubMedGoogle Scholar
  23. 23.
    Wang WT, Yang L, Yang ZX, Hu XX, Ding Y, Yan X, Fu CX, Grimm R, Zeng MS, Rao SX (2018) Assessment of Microvascular Invasion of Hepatocellular Carcinoma with Diffusion Kurtosis Imaging. Radiology 286(2):571-580. CrossRefGoogle Scholar
  24. 24.
    Chandarana H, Robinson E, Hajdu CH, Drozhinin L, Babb JS, Taouli B (2011) Microvascular invasion in hepatocellular carcinoma: Is it predictable with pretransplant MRI? American Journal of Roentgenology 196 (5):1083-1089CrossRefPubMedGoogle Scholar
  25. 25.
    Zhao W, Liu W, Liu H, Yi X, Hou J, Pei Y, Liu H, Feng D, Liu L, Li W (2018) Preoperative prediction of microvascular invasion of hepatocellular carcinoma with IVIM diffusion-weighted MR imaging and Gd-EOB-DTPA-enhanced MR imaging. PloS one 13 (5):e0197488. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Lei Z, Li J, Wu D, Xia Y, Wang Q, Si A, Wang K, Wan X, Lau WY, Wu M, Shen F (2016) Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the milan criteriaCrossRefPubMedGoogle Scholar
  27. 27.
    Hu HT, Shen SL, Wang Z, Shan QY, Huang XW, Zheng Q, Xie XY, Lu MD, Wang W (2018) Peritumoral tissue on preoperative imaging reveals microvascular invasion in hepatocellular carcinoma: a systematic review and meta-analysis. Abdominal Radiology 43 (12):3324-3330. CrossRefPubMedGoogle Scholar
  28. 28.
    Hu H, Zheng Q, Huang Y, Huang XW, Lai ZC, Liu J, Xie X, Feng ST, Wang W (2017) A non-smooth tumor margin on preoperative imaging assesses microvascular invasion of hepatocellular carcinoma: A systematic review and meta-analysis. Scientific Reports 7 (1):15375. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Hu HT, Wang Z, Kuang M, Wang W (2018) Need for normalization: the non-standard reference standard for microvascular invasion diagnosis in hepatocellular carcinoma. World journal of surgical oncology 16 (1):50. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Kaibori M, Ishizaki M, Matsui K, Kwon AH (2010) Predictors of microvascular invasion before hepatectomy for hepatocellular carcinoma. J Surg Oncol 102 (5):462-468. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Fei Zhu
    • 1
  • Fan Yang
    • 2
  • Jing Li
    • 3
  • Weixia Chen
    • 1
    Email author
  • Weilin Yang
    • 1
  1. 1.Department of Radiology, West China HospitalSichuan UniversityChengduChina
  2. 2.Department of RadiologyChengdu First People’s HospitalChengduChina
  3. 3.Department of Evidence-Based Medicine and Clinical Epidemiology, West China HospitalSichuan UniversityChengduChina

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