Skip to main content

Advertisement

Log in

Peritumoral tissue on preoperative imaging reveals microvascular invasion in hepatocellular carcinoma: a systematic review and meta-analysis

  • Pictorial essay
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Background

Histologic microvascular invasion (MVI) substantially worsens the prognosis of patients with hepatocellular carcinoma, and can only be diagnosed postoperatively. Preoperative assessment of MVI by imaging has been focused on tumor-related features, while peritumoral imaging features have been indicated elsewhere to be more accurate. The aim of the present study is to evaluate the association between peritumoral imaging features and MVI.

Methods

Literature search was performed using the PubMed, Embase, and Cochrane Library databases. Summary results of the association between peritumoral imaging features and MVI were presented as the odds ratio (OR) and the 95% confidence interval. Meta-regression and subgroup analyses were performed when heterogeneity was detected. Diagnostic accuracy analysis was also conducted for identified features.

Results

Ten studies were included in the analysis. Moderate and low heterogeneities were found among the seven studies on peritumoral enhancement and four studies on peritumoral hypointensity on HBP, respectively. Summary results revealed a significant association between MVI and peritumoral enhancement (OR 4.04 [2.23, 7.32], p < 0.05), and peritumoral hypointensity on HBP (OR 10.62 [5.31, 21.26], p < 0.05). Diagnostic accuracy analysis revealed high specificity (0.90-0.94) but low sensitivity (0.29–0.40) for both features to assess MVI.

Conclusion

The two peritumoral imaging features are significantly associated with MVI. The two features highly suggest MVI only when present with a high false negative rate. Promotion of their diagnostic efficiency can be a worthwhile task for future research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Roayaie S, Blume IN, Thung SN, et al. (2009) A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology 137(3):850–855. https://doi.org/10.1053/j.gastro.2009.06.003

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fan ST, Poon RT, Yeung C, et al. (2011) Outcome after partial hepatectomy for hepatocellular cancer within the Milan criteria. Br J Surg 98(9):1292–1300. https://doi.org/10.1002/bjs.7583

    Article  CAS  PubMed  Google Scholar 

  3. Sumie S, Nakashima O, Okuda K, et al. (2014) The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol 21(3):1002–1009. https://doi.org/10.1245/s10434-013-3376-9

    Article  PubMed  Google Scholar 

  4. Du M, Chen L, Zhao J, et al. (2014) Microvascular invasion (MVI) is a poorer prognostic predictor for small hepatocellular carcinoma. BMC Cancer 14:38. https://doi.org/10.1186/1471-2407-14-38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yamashita Y, Tsuijita E, Takeishi K, et al. (2012) Predictors for microinvasion of small hepatocellular carcinoma <= 2 cm. Ann Surg Oncol 19(6):2027–2034. https://doi.org/10.1245/s10434-011-2195-0

    Article  PubMed  Google Scholar 

  6. Rodríguez-Perálvarez M, Luong TV, Andreana L, et al. (2013) A systematic review of microvascular invasion in hepatocellular carcinoma: diagnostic and prognostic variability. Ann Surg Oncol 20(1):325–339. https://doi.org/10.1245/s10434-012-2513-1

    Article  PubMed  Google Scholar 

  7. Llovet JM, Schwartz M, Mazzaferro V (2005) Resection and liver transplantation for hepatocellular carcinoma. Semin Liver Dis 25(2):181–200. https://doi.org/10.1055/s-2005-871198

    Article  PubMed  Google Scholar 

  8. Jun L, Zhenlin Y, Renyan G, et al. (2012) Independent factors and predictive score for extrahepatic metastasis of hepatocellular carcinoma following curative hepatectomy. Oncologist 17(7):963–969. https://doi.org/10.1634/theoncologist.2011-0447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kim H, Park MS, Choi JY, et al. (2009) Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol 19(7):1744–1751. https://doi.org/10.1007/s00330-009-1331-8

    Article  PubMed  Google Scholar 

  10. Kim KA, Kim MJ, Jeon HM, et al. (2012) Prediction of microvascular invasion of hepatocellular carcinoma: usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. JMRI. 35(3):629–634. https://doi.org/10.1002/jmri.22876

    Article  PubMed  Google Scholar 

  11. Chou CT, Chen RC, Lee CW, et al. (1014) Prediction of microvascular invasion of hepatocellular carcinoma by pre-operative CT imaging. Br J Radiol 2012(85):778–783. https://doi.org/10.1259/bjr/65897774

    Article  Google Scholar 

  12. Xu P, Zeng M, Liu K, et al. (2014) Microvascular invasion in small hepatocellular carcinoma: is it predictable with preoperative diffusion-weighted imaging? J Gastroenterol Hepatol (Australia) 29(2):330–336. https://doi.org/10.1111/jgh.12358

    Article  Google Scholar 

  13. Shin SK, Kim YS, Shim YS, et al. (2017) Peritumoral decreased uptake area of gadoxetic acid enhanced magnetic resonance imaging and tumor recurrence after surgical resection in hepatocellular carcinoma: a STROBE-compliant article. Medicine 96(33):e7761. https://doi.org/10.1097/md.0000000000007761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ahn SY, Lee JM, Joo I, et al. (2015) Prediction of microvascular invasion of hepatocellular carcinoma using gadoxetic acid-enhanced MR and (18)F-FDG PET/CT. Abdom Imaging 40(4):843–851. https://doi.org/10.1007/s00261-014-0256-0

    Article  PubMed  Google Scholar 

  15. Chou CT, Chen RC, Lin WC, et al. (2014) Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. Am J Roentgenol 203(3):W253–W259. https://doi.org/10.2214/ajr.13.10595

    Article  Google Scholar 

  16. 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. J Hepatol 67(3):526–534. https://doi.org/10.1016/j.jhep.2017.04.024

    Article  CAS  PubMed  Google Scholar 

  17. Yang C, Wang H, Sheng R, et al. (2016) Microvascular invasion in hepatocellular carcinoma: is it predictable with a new, preoperative application of diffusion-weighted imaging? Clin Imaging 41:101–105. https://doi.org/10.1016/j.clinimag.2016.10.004

    Article  PubMed  Google Scholar 

  18. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  PubMed  Google Scholar 

  19. Tsujita E, Yamashita Y, Takeishi K, et al. (2013) The clinicopathological impact of gross classification on solitary small hepatocellular carcinoma. Hepatogastroenterology 60(127):1726–1730

    PubMed  Google Scholar 

  20. Lee S, Kim SH, Lee JE (2017) Single hepatocellular carcinoma: preoperative imaging biomarker for predicting microvascular invasion on gadoxetic acid-enhanced MR imaging. Hepat Int 11(1):S370–S371. https://doi.org/10.1007/s12072-016-9783-9

    Article  Google Scholar 

  21. Renzulli M, Buonfiglioli F, Brocchi S, et al. (2016) Imaging features of microvascular invasion in hepatocellular carcinoma developed in HCV-related cirrhosis after direct-acting antiviral therapy. Hepatology 64(1):223A–224A

    Google Scholar 

  22. Shin SK, Kim YS, Shim YS, et al. (2017) Clinical significance of the peri-tumoral decreased uptake area on hepatobiliary phase of gadoxetic acid-enhanced MRI in hepatocellular carcinoma. Hepat Int 11(1):S375. https://doi.org/10.1007/s12072-016-9783-9

    Article  Google Scholar 

  23. Kobayashi T, Aikata H, Daijo K, et al. (2016) Comparison of 18F-FDG PET-CT and Gd-EOB-DTPA-enhanced MRI for prediction of microvascular invasion and outcome after curative resection for early-stage hepatocellular carcinoma. Hepatology 64(1):218A

    Google Scholar 

  24. Robinson E, Chandarana H, Droxhinin L, et al. (2009) MRI features of HCC do not predict microvascular invasion in liver transplant for hepatocellular carcinoma. Liver Transpl 15:S111

    Article  Google Scholar 

  25. Zhang W, Lai SL, Chen J, et al. (2017) Validated preoperative computed tomography risk estimation for postoperative hepatocellular carcinoma recurrence. World J Gastroenterol 23(35):6467–6473. https://doi.org/10.3748/wjg.v23.i35.6467

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nishie A, Yoshimitsu K, Irie H, et al. (2009) Radiological detectability of minute hepatic venous invasion in hepatocellular carcinoma. Eur J Radiol 70(3):517–524. https://doi.org/10.1016/j.ejrad.2008.02.021

    Article  PubMed  Google Scholar 

  27. Mendez-Sanchez N, Vasquez-Fernandez F, Zamora-Valdes D, Uribe M (2008) Sorafenib, a systemic therapy for hepatocellular carcinoma. Ann Hepatol 7(1):46–51

    CAS  PubMed  Google Scholar 

  28. Wang SN, Chuang SC, Lee KT (2014) Efficacy of sorafenib as adjuvant therapy to prevent early recurrence of hepatocellular carcinoma after curative surgery: a pilot study. Hepatol Res 44(5):523–531. https://doi.org/10.1111/hepr.12159

    Article  CAS  PubMed  Google Scholar 

  29. Sun JJ, Wang K, Zhang CZ, et al. (2016) Postoperative adjuvant transcatheter arterial chemoembolization after R0 hepatectomy improves outcomes of patients who have hepatocellular carcinoma with microvascular invasion. Ann Surg Oncol 23(4):1344–1351. https://doi.org/10.1245/s10434-015-5008-z

    Article  PubMed  Google Scholar 

  30. Banerjee S, Wang DS, Kim HJ, et al. (2015) A computed tomography radiogenomic biomarker predicts microvascular invasion and clinical outcomes in hepatocellular carcinoma. Hepatology 62(3):792–800. https://doi.org/10.1002/hep.27877

    Article  PubMed  PubMed Central  Google Scholar 

  31. Allen JC, Nault JC, Zhu G, et al. (2016) The transcriptomic G1-G6 signature of hepatocellular carcinoma in an Asian population Association of G3 with microvascular invasion. Medicine (United States). https://doi.org/10.1097/md.0000000000005263

    Article  PubMed  PubMed Central  Google Scholar 

  32. Pote N, Alexandrov T, Le Faouder J, et al. (2013) Imaging mass spectrometry reveals modified forms of histone H4 as new biomarkers of microvascular invasion in hepatocellular carcinomas. Hepatology 58(3):983–994. https://doi.org/10.1002/hep.26433

    Article  CAS  PubMed  Google Scholar 

  33. Minguez B, Hoshida Y, Villanueva A, et al. (2011) Gene-expression signature of vascular invasion in hepatocellular carcinoma. J Hepatol 55(6):1325–1331. https://doi.org/10.1016/j.jhep.2011.02.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kusano H, Han J, Bulthuis M, et al. (2013) Microvascular invasion in hepatocellular carcinoma is defined by tumor characteristics and aberrant angiogenesis in peritumoral tissue. Hepatology 58(4):1214A. https://doi.org/10.1002/hep.26883

    Article  Google Scholar 

  35. Semelka RC, Hussain SM, Marcos HB, Woosley JT (2000) Perilesional enhancement of hepatic metastases: correlation between MR imaging and histopathologic findings-initial observations. Radiology 215(1):89–94. https://doi.org/10.1148/radiology.215.1.r00mr2989

    Article  CAS  PubMed  Google Scholar 

  36. Matsui O, Kobayashi S, Sanada J, et al. (2011) Hepatocellular nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging 36(3):264–272. https://doi.org/10.1007/s00261-011-9685-1

    Article  PubMed  PubMed Central  Google Scholar 

  37. Nishie A, Asayama Y, Ishigami K, et al. (2014) Clinicopathological significance of the peritumoral decreased uptake area of gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid in hepatocellular carcinoma. J Gastroenterol Hepatol 29(3):561–567. https://doi.org/10.1111/jgh.12423

    Article  CAS  PubMed  Google Scholar 

  38. Yip SS, Aerts HJ (2016) Applications and limitations of radiomics. Phys Med Biol 61(13):R150–R166. https://doi.org/10.1088/0031-9155/61/13/r150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Braman NM, Etesami M, Prasanna P, et al. (2017) Intratumoral and peritumoral radiomics for the pretreatment prediction of pathological complete response to neoadjuvant chemotherapy based on breast DCE-MRI. Breast Cancer Res 19(1):57. https://doi.org/10.1186/s13058-017-0846-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Prasanna P, Patel J, Partovi S, Madabhushi A, Tiwari P (2016) Radiomic features from the peritumoral brain parenchyma on treatment-naive multi-parametric MR imaging predict long versus short-term survival in glioblastoma multiforme: preliminary findings. Eur Radiol. https://doi.org/10.1007/s00330-016-4637-3

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wei Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Disclosure

The authors declare that they have no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 105 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, HT., Shen, SL., Wang, Z. et al. Peritumoral tissue on preoperative imaging reveals microvascular invasion in hepatocellular carcinoma: a systematic review and meta-analysis. Abdom Radiol 43, 3324–3330 (2018). https://doi.org/10.1007/s00261-018-1646-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-018-1646-5

Keywords

Navigation