Annals of Surgical Oncology

, Volume 20, Issue 1, pp 325–339 | Cite as

A Systematic Review of Microvascular Invasion in Hepatocellular Carcinoma: Diagnostic and Prognostic Variability

  • Manuel Rodríguez-Perálvarez
  • Tu Vinh Luong
  • Lorenzo Andreana
  • Tim Meyer
  • Amar Paul Dhillon
  • Andrew Kenneth Burroughs
Hepatobiliary Tumors

Abstract

Selected patients with hepatocellular carcinoma are candidates to receive potentially curative treatments, such as hepatic resection or liver transplantation, but nevertheless there is a high risk of tumor recurrence. Microvascular invasion is a histological feature of hepatocellular carcinoma related to aggressive biological behavior. We systematically reviewed 20 observational studies that addressed the prognostic impact of microvascular invasion, either after liver transplantation or resection. Outcomes were disease-free survival and overall survival. In liver transplantation, the presence of microvascular invasion shortened disease-free survival at 3 years (relative risk (RR) = 3.41 [2.05–5.7]; five studies, n = 651) and overall survival both at 3 years (RR = 2.41 [1.72–3.37]; five studies, n = 1,938) and 5 years (RR = 2.29 [1.85–2.83]; six studies, n = 2,003). After liver resection, microvascular invasion impacted disease-free survival at 3 and 5 years (RR = 1.82 [1.61–2.07] and RR = 1.51 [1.29–1.77]; four studies, n = 1,501 for both comparisons). However inter/intraobserver variability in reporting and the lack of definition and grading of microvascular invasion has led to great heterogeneity in evaluating this histological feature in hepatocellular carcinoma. Thus, there is an urgent need to clarify this issue, because determining prognosis and response to therapy have become important in the current management of hepatocellular carcinoma. In this systematic review, we summarize the diagnostic and prognostic data concerning microvascular invasion in hepatocellular carcinoma and present a basis for consensus on its definition.

Notes

Acknowledgment

M. Rodríguez-Perálvarez is a recipient of a grant from the Institute Maimónides for Biomedical research of Córdoba, Spain (IMIBIC).

Disclosure

The authors have no conflict of interest to disclose.

Supplementary material

10434_2012_2513_MOESM1_ESM.pdf (54 kb)
Supplementary material 1 (PDF 45 kb)

References

  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRefGoogle Scholar
  2. 2.
    Forner A, Reig ME, de Lope CR, Bruix J. Current strategy for staging and treatment: the BCLC update and future prospects. Semin Liver Dis 2010;30:61–74.PubMedCrossRefGoogle Scholar
  3. 3.
    Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005;42:1208–36.PubMedCrossRefGoogle Scholar
  4. 4.
    Onaca N, Davis GL, Jennings LW, Goldstein RM, Klintmalm GB. Improved results of transplantation for hepatocellular carcinoma: a report from the International Registry of Hepatic Tumors in Liver Transplantation. Liver Transpl. 2009;15:574–80.PubMedCrossRefGoogle Scholar
  5. 5.
    Bertuzzo VR, Cescon M, Ravaioli M, et al. Analysis of factors affecting recurrence of hepatocellular carcinoma after liver transplantation with a special focus on inflammation markers. Transplantation. 2011;91:1279–85.PubMedCrossRefGoogle Scholar
  6. 6.
    Bhangui P, Vibert E, Majno P, et al. Intention-to-treat analysis of liver transplantation for hepatocellular carcinoma: living versus deceased donor transplantation. Hepatology. 2011;53:1570–9.PubMedCrossRefGoogle Scholar
  7. 7.
    McHugh PP, Gilbert J, Vera S, Koch A, Ranjan D, Gedaly R. Alpha-fetoprotein and tumor size are associated with microvascular invasion in explanted livers of patients undergoing transplantation with hepatocellular carcinoma. HPB (Oxford). 2010;12:56–61.CrossRefGoogle Scholar
  8. 8.
    Kim H, Park MS, Park YN, et al. Preoperative radiologic and postoperative pathologic risk factors for early intra-hepatic recurrence in hepatocellular carcinoma patients who underwent curative resection. Yonsei Med J. 2009;50:789–95.PubMedCrossRefGoogle Scholar
  9. 9.
    Dudek K, Kornasiewicz O, Remiszewski P, et al. Impact of tumor characteristic on the outcome of liver transplantation in patients with hepatocellular carcinoma. Transplant Proc. 2009;41:3135–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Li J, Yan LN, Yang J, et al. Indicators of prognosis after liver transplantation in Chinese hepatocellular carcinoma patients. World J Gastroenterol. 2009;15:4170–6.PubMedCrossRefGoogle Scholar
  11. 11.
    Wang CC, Iyer SG, Low JK, et al. Perioperative factors affecting long-term outcomes of 473 consecutive patients undergoing hepatectomy for hepatocellular carcinoma. Ann Surg Oncol. 2009;16:1832–42.PubMedCrossRefGoogle Scholar
  12. 12.
    Mazzaferro V, Llovet JM, Miceli R, et al. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol. 2009;10:35–43.PubMedCrossRefGoogle Scholar
  13. 13.
    Gomez D, Farid S, Malik HZ, et al. Preoperative neutrophil-to-lymphocyte ratio as a prognostic predictor after curative resection for hepatocellular carcinoma. World J Surg. 2008;32:1757–62.PubMedCrossRefGoogle Scholar
  14. 14.
    Sumie S, Kuromatsu R, Okuda K, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol. 2008;15:1375–82.PubMedCrossRefGoogle Scholar
  15. 15.
    Parfitt JR, Marotta P, Alghamdi M, et al. Recurrent hepatocellular carcinoma after transplantation: use of a pathological score on explanted livers to predict recurrence. Liver Transpl. 2007;13:543–51.PubMedCrossRefGoogle Scholar
  16. 16.
    Bhattacharjya S, Bhattacharjya T, Quaglia A, et al. Liver transplantation in cirrhotic patients with small hepatocellular carcinoma: an analysis of pre-operative imaging, explant histology and prognostic histologic indicators. Dig Surg. 2004;21:152–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Lauwers GY, Terris B, Balis UJ, et al. Prognostic histologic indicators of curatively resected hepatocellular carcinomas: a multi-institutional analysis of 425 patients with definition of a histologic prognostic index. Am J Surg Pathol. 2002;26:25–34.PubMedCrossRefGoogle Scholar
  18. 18.
    Cucchetti A, Piscaglia F, Caturelli E, et al. Comparison of recurrence of hepatocellular carcinoma after resection in patients with cirrhosis to its occurrence in a surveilled cirrhotic population. Ann Surg Oncol. 2009;16:413–22.PubMedCrossRefGoogle Scholar
  19. 19.
    Fan L, Mac MT, Frishberg DP, et al. Interobserver and intraobserver variability in evaluating vascular invasion in hepatocellular carcinoma. J Gastroenterol Hepatol. 2010;25:1556–61.PubMedCrossRefGoogle Scholar
  20. 20.
    Clavien PA, Lesurtel M, Bossuyt PM, Gores GJ, Langer B, Perrier A. Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol. 2012;13:11–22.CrossRefGoogle Scholar
  21. 21.
    Huang ZY, Liang BY, Xiong M, et al. Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-center experience in China. Ann Surg Oncol. 2012;19:2515–25.PubMedCrossRefGoogle Scholar
  22. 22.
    Fan ST, Poon RT, Yeung C, et al. Outcome after partial hepatectomy for hepatocellular cancer within the Milan criteria. Br J Surg. 2011;98:1292–300.PubMedCrossRefGoogle Scholar
  23. 23.
    Altman DG. Systematic reviews of evaluations of prognostic variables. BMJ. 2001;323:224–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Whittaker S, Marais R, Zhu AX. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene. 2010; 29:4989–5005.PubMedCrossRefGoogle Scholar
  25. 25.
    Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.PubMedCrossRefGoogle Scholar
  26. 26.
    Wu SM, Huang YH, Yeh CT, et al. Cathepsin H regulated by the thyroid hormone receptors associate with tumor invasion in human hepatoma cells. Oncogene. 2011;30:2057–69.PubMedCrossRefGoogle Scholar
  27. 27.
    Fransvea E, Mazzocca A, Antonaci S, Giannelli G. Targeting transforming growth factor (TGF)-betaRI inhibits activation of beta1 integrin and blocks vascular invasion in hepatocellular carcinoma. Hepatology. 2009;49:839–50.PubMedCrossRefGoogle Scholar
  28. 28.
    Fransvea E, Angelotti U, Antonaci S, Giannelli G. Blocking transforming growth factor-beta up-regulates E-cadherin and reduces migration and invasion of hepatocellular carcinoma cells. Hepatology. 2008;47:1557–66.PubMedCrossRefGoogle Scholar
  29. 29.
    Matsumura T, Makino R, Mitamura K. Frequent down-regulation of E-cadherin by genetic and epigenetic changes in the malignant progression of hepatocellular carcinomas. Clin Cancer Res. 2001;7:594–9.PubMedGoogle Scholar
  30. 30.
    Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 2006;66:8319–26.PubMedCrossRefGoogle Scholar
  31. 31.
    Ding ZB, Shi YH, Zhou J, et al. Liver-intestine cadherin predicts microvascular invasion and poor prognosis of hepatitis B virus-positive hepatocellular carcinoma. Cancer. 2009;115:4753–65.PubMedCrossRefGoogle Scholar
  32. 32.
    Quaglia A, Etessami N, Sim R, Difford J, Dhillon AP. Vascular invasion and herniation by hepatocellular carcinoma in cirrhosis: a wolf in sheep’s clothing? Arch Pathol Lab Med. 2005;129:639–44.PubMedGoogle Scholar
  33. 33.
    Sugino T, Yamaguchi T, Hoshi N, et al. Sinusoidal tumor angiogenesis is a key component in hepatocellular carcinoma metastasis. Clin Exp Metastasis. 2008;25:835–41.PubMedCrossRefGoogle Scholar
  34. 34.
    Ding T, Xu J, Zhang Y, et al. Endothelium-coated tumor clusters are associated with poor prognosis and micrometastasis of hepatocellular carcinoma after resection. Cancer. 2011;117:4878–89.PubMedCrossRefGoogle Scholar
  35. 35.
    Mitsunobu M, Toyosaka A, Oriyama T, Okamoto E, Nakao N. Intrahepatic metastases in hepatocellular carcinoma: the role of the portal vein as an efferent vessel. Clin Exp Metastasis. 1996;14:520–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Shah SA, Tan JC, McGilvray ID, et al. Does microvascular invasion affect outcomes after liver transplantation for HCC? A histopathological analysis of 155 consecutive explants. J Gastrointest Surg. 2007;11:464–71.PubMedCrossRefGoogle Scholar
  37. 37.
    Lee CW, Chan KM, Lee CF, et al. Hepatic resection for hepatocellular carcinoma with lymph node metastasis: clinicopathological analysis and survival outcome. Asian J Surg. 2011;34:53–62.PubMedCrossRefGoogle Scholar
  38. 38.
    Unek T, Karademir S, Arslan NC, et al. Comparison of Milan and UCSF criteria for liver transplantation to treat hepatocellular carcinoma. World J Gastroenterol. 2011;17:4206–12.PubMedCrossRefGoogle Scholar
  39. 39.
    Lim KC, Chow PK, Allen JC, et al. Microvascular invasion is a better predictor of tumor recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the milan criteria. Ann Surg. 2011;254:108–13.PubMedCrossRefGoogle Scholar
  40. 40.
    Baek CK, Choi JY, Kim KA, et al. Hepatocellular carcinoma in patients with chronic liver disease: A comparison of gadoxetic acid-enhanced MRI and multiphasic MDCT. Clin Radiol. 2012;67:148–56.PubMedCrossRefGoogle Scholar
  41. 41.
    Chan SC, Fan ST, Chok KS, et al. Survival advantage of primary liver transplantation for hepatocellular carcinoma within the up-to-7 criteria with microvascular invasion. Hepatol Int. 2011;6:646–56.CrossRefGoogle Scholar
  42. 42.
    Sala M, Llovet JM, Vilana R, et al. Initial response to percutaneous ablation predicts survival in patients with hepatocellular carcinoma. Hepatology. 2004;40:1352–60.PubMedCrossRefGoogle Scholar
  43. 43.
    Fuks D, Dokmak S, Paradis V, Diouf M, Durand F, Belghiti J. Benefit of initial resection of HCC followed by transplantation in case of recurrence: an intention-to-treat analysis. Hepatology. 2012;55:132–40.PubMedCrossRefGoogle Scholar
  44. 44.
    Roayaie S, Blume IN, Thung SN, et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009; 137:850–5.PubMedCrossRefGoogle Scholar
  45. 45.
    Fujita N, Aishima S, Iguchi T, et al. Histologic classification of microscopic portal venous invasion to predict prognosis in hepatocellular carcinoma. Hum Pathol. 2011; 42:1531–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Stigliano R, Marelli L, Yu D, Davies N, Patch D, Burroughs AK. Seeding following percutaneous diagnostic and therapeutic approaches for hepatocellular carcinoma. What is the risk and the outcome? Seeding risk for percutaneous approach of HCC. Cancer Treat Rev. 2007;33:437–47.PubMedCrossRefGoogle Scholar
  47. 47.
    Silva MA, Hegab B, Hyde C, Guo B, Buckels JA, Mirza DF. Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut. 2008;57:1592–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Chandarana H, Robinson E, Hajdu CH, Drozhinin L, Babb JS, Taouli B. Microvascular invasion in hepatocellular carcinoma: is it predictable with pretransplant MRI? AJR Am J Roentgenol. 2011;196:1083–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Eguchi S, Takatsuki M, Hidaka M, et al. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J Surg. 2010; 34:1034–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Nagano Y, Shimada H, Takeda K, et al. Predictive factors of microvascular invasion in patients with hepatocellular carcinoma larger than 5 cm. World J Surg. 2008; 32:2218–22.PubMedCrossRefGoogle Scholar
  51. 51.
    Kim BK, Han KH, Park YN, et al. Prediction of microvascular invasion before curative resection of hepatocellular carcinoma. J Surg Oncol. 2008; 97:246–52.PubMedCrossRefGoogle Scholar
  52. 52.
    Pawlik TM, Delman KA, Vauthey JN, et al. Tumor size predicts vascular invasion and histologic grade: Implications for selection of surgical treatment for hepatocellular carcinoma. Liver Transpl. 2005; 11:1086–92.PubMedCrossRefGoogle Scholar
  53. 53.
    Esnaola NF, Lauwers GY, Mirza NQ, et al. Predictors of microvascular invasion in patients with hepatocellular carcinoma who are candidates for orthotopic liver transplantation. J Gastrointest Surg. 2002; 6:224–32.PubMedCrossRefGoogle Scholar
  54. 54.
    Kaibori M, Ishizaki M, Matsui K, Kwon AH. Predictors of microvascular invasion before hepatectomy for hepatocellular carcinoma. J Surg Oncol. 2010; 102:462–8.PubMedCrossRefGoogle Scholar
  55. 55.
    Shirabe K, Taketomi A, Morita K, et al. Comparative evaluation of expanded criteria for patients with hepatocellular carcinoma beyond the Milan criteria undergoing living-related donor liver transplantation. Clin Transplant. 2011; 25:491–498.CrossRefGoogle Scholar
  56. 56.
    Witjes CD, Willemssen FE, Verheij J, et al. Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging. 2012;36:641–47.PubMedCrossRefGoogle Scholar
  57. 57.
    Hatano E, Ikai I, Higashi T, et al. Preoperative positron emission tomography with fluorine-18-fluorodeoxyglucose is predictive of prognosis in patients with hepatocellular carcinoma after resection. World J Surg. 2006; 30:1736–41.PubMedCrossRefGoogle Scholar
  58. 58.
    Lee JW, Paeng JC, Kang KW, et al. Prediction of tumor recurrence by 18F-FDG PET in liver transplantation for hepatocellular carcinoma. J Nucl Med. 2009; 50:682–7.PubMedCrossRefGoogle Scholar
  59. 59.
    Decaens T IE, Laurent A, Luciani J, Tran Van Nhieu J, Auriault ML, Evangelista E, Meignan M, Azoulay D, Duvoux C. (2010) Role of FDG PET in patients waiting liver transplantation for hepatocellular carcinoma. J Hepatol. 54:S254.CrossRefGoogle Scholar
  60. 60.
    Kornberg A, Freesmeyer M, Barthel E, et al. 18F-FDG-uptake of hepatocellular carcinoma on PET predicts microvascular tumor invasion in liver transplant patients. Am J Transpl. 2009;9:592–600.PubMedCrossRefGoogle Scholar
  61. 61.
    Cheung TT, Chan SC, Ho CL, et al. Can positron emission tomography with the dual tracers [11 C]acetate and [18 F]fludeoxyglucose predict microvascular invasion in hepatocellular carcinoma? Liver Transpl. 2011; 17:1218–25.PubMedCrossRefGoogle Scholar
  62. 62.
    Kiriyama S, Uchiyama K, Ueno M, et al. Triple positive tumor markers for hepatocellular carcinoma are useful predictors of poor survival. Ann Surg. 2011; 254:984–91.PubMedCrossRefGoogle Scholar
  63. 63.
    Sterling R, Wright E, Morgan T, et al. Frequency of elevated hepatocellular carcinoma (HCC) biomarkers in patients with chronic hepatitis C and advanced fibrosis with and without HCC. Hepatology. 2010; 52 (Suppl1):328A [Abstract].Google Scholar
  64. 64.
    Cucchetti A, Piscaglia F, Grigioni AD, et al. Preoperative prediction of hepatocellular carcinoma tumor grade and micro-vascular invasion by means of artificial neural network: a pilot study. J Hepatol. 2010; 52:880–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Ren Y, Poon RT, Tsui HT, et al. Interleukin-8 serum levels in patients with hepatocellular carcinoma: correlations with clinicopathological features and prognosis. Clin Cancer Res. 2003;9:5996–6001.PubMedGoogle Scholar
  66. 66.
    Huang GW, Yang LY, Lu WQ. Expression of hypoxia-inducible factor 1alpha and vascular endothelial growth factor in hepatocellular carcinoma: Impact on neovascularization and survival. World J Gastroenterol. 2005;11:1705–8.PubMedGoogle Scholar
  67. 67.
    Lu XY, Xi T, Lau WY, et al. Hepatocellular carcinoma expressing cholangiocyte phenotype is a novel subtype with highly aggressive behavior. Ann Surg Oncol. 2011;18:2210–7.PubMedCrossRefGoogle Scholar
  68. 68.
    Thompson MD, Monga SP. WNT/beta-catenin signaling in liver health and disease. Hepatology. 2007; 45:1298–305.PubMedCrossRefGoogle Scholar
  69. 69.
    Cieply B, Zeng G, Proverbs-Singh T, Geller DA, Monga SP. Unique phenotype of hepatocellular cancers with exon-3 mutations in beta-catenin gene. Hepatology. 2009;49:821–31.PubMedCrossRefGoogle Scholar
  70. 70.
    Park NH, Chung YH, Youn KH, et al. Close correlation of p53 mutation to microvascular invasion in hepatocellular carcinoma. J Clin Gastroenterol. 2001;33:397–401.PubMedCrossRefGoogle Scholar
  71. 71.
    Iizuka N, Oka M, Yamada-Okabe H, et al. Oligonucleotide microarray for prediction of early intrahepatic recurrence of hepatocellular carcinoma after curative resection. Lancet. 2003;361:923–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Wang SM, Ooi LL, Hui KM. Identification and validation of a novel gene signature associated with the recurrence of human hepatocellular carcinoma. Clin Cancer Res. 2007;13:6275–83.PubMedCrossRefGoogle Scholar
  73. 73.
    Villanueva A, Minguez B, Forner A, Reig M, Llovet JM. Hepatocellular carcinoma: novel molecular approaches for diagnosis, prognosis, and therapy. Annu Rev Med. 2010; 61:317–28.PubMedCrossRefGoogle Scholar
  74. 74.
    Minguez B, Hoshida Y, Villanueva A, et al. Gene-expression signature of vascular invasion in hepatocellular carcinoma. J Hepatol. 2011;55:1325–31.PubMedCrossRefGoogle Scholar
  75. 75.
    Wei Y, Van Nhieu JT, Prigent S, Srivatanakul P, Tiollais P, Buendia MA. Altered expression of E-cadherin in hepatocellular carcinoma: correlations with genetic alterations, beta-catenin expression, and clinical features. Hepatology. 2002;36:692–701.PubMedCrossRefGoogle Scholar
  76. 76.
    Yan Q, Zhang ZF, Chen XP, et al. Reduced T-cadherin expression and promoter methylation are associated with the development and progression of hepatocellular carcinoma. Int J Oncol. 2008;32:1057–63.PubMedGoogle Scholar
  77. 77.
    Zhan DQ, Wei S, Liu C, et al. Reduced N-cadherin expression is associated with metastatic potential and poor surgical outcomes of hepatocellular carcinoma. J Gastroenterol Hepatol. 2012;27:173–80.PubMedCrossRefGoogle Scholar
  78. 78.
    Chen ZY, Wei W, Guo ZX, Lin JR, Shi M, Guo RP. Morphologic classification of microvessels in hepatocellular carcinoma is associated with the prognosis after resection. J Gastroenterol Hepatol. 2011; 26:866–74.PubMedCrossRefGoogle Scholar
  79. 79.
    Park YN, Yang CP, Fernandez GJ, Cubukcu O, Thung SN, Theise ND. Neoangiogenesis and sinusoidal “capillarization” in dysplastic nodules of the liver. Am J Surg Pathol. 1998; 22:656–62.PubMedCrossRefGoogle Scholar
  80. 80.
    Capurro M, Wanless IR, Sherman M, et al. Glypican-3: a novel serum and histochemical marker for hepatocellular carcinoma. Gastroenterology. 2003; 125:89–97.PubMedCrossRefGoogle Scholar
  81. 81.
    Coston WM, Loera S, Lau SK, et al. Distinction of hepatocellular carcinoma from benign hepatic mimickers using Glypican-3 and CD34 immunohistochemistry. Am J Surg Pathol. 2008;32:433–44.PubMedCrossRefGoogle Scholar
  82. 82.
    Tatrai P, Somoracz A, Batmunkh E, et al. Agrin and CD34 immunohistochemistry for the discrimination of benign versus malignant hepatocellular lesions. Am J Surg Pathol. 2009;33:874–85.PubMedCrossRefGoogle Scholar
  83. 83.
    Somoracz A, Tatrai P, Horvath G, et al. Agrin immunohistochemistry facilitates the determination of primary versus metastatic origin of liver carcinomas. Hum Pathol. 2010;41:1310–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Wang Q, Tian X, Zhang C. Upregulation of vasohibin-1 expression with angiogenesis and poor prognosis of hepatocellular carcinoma after curative surgery. Med Oncol. 2011;29:2727–36.PubMedCrossRefGoogle Scholar
  85. 85.
    Ryu SH, Chung YH, Lee H, et al. Metastatic tumor antigen 1 is closely associated with frequent postoperative recurrence and poor survival in patients with hepatocellular carcinoma. Hepatology. 2008;47:929–36.PubMedCrossRefGoogle Scholar
  86. 86.
    Baloch ZW, LiVolsi VA. Our approach to follicular-patterned lesions of the thyroid. J Clin Pathol. 2007;60:244–50.PubMedCrossRefGoogle Scholar
  87. 87.
    Chou CT, Chen RC, Lee CW, Ko CJ, Wu HK, Chen YL. Prediction of microvascular invasion of hepatocellular carcinoma by pre-operative CT imaging. Br J Radiol. 2012;85:778–83.PubMedCrossRefGoogle Scholar
  88. 88.
    Tanaka S, Mogushi K, Yasen M, et al. Gene-expression phenotypes for vascular invasiveness of hepatocellular carcinomas. Surgery. 2010;147:405–14.PubMedCrossRefGoogle Scholar
  89. 89.
    Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2012

Authors and Affiliations

  • Manuel Rodríguez-Perálvarez
    • 1
  • Tu Vinh Luong
    • 2
  • Lorenzo Andreana
    • 1
  • Tim Meyer
    • 3
  • Amar Paul Dhillon
    • 2
  • Andrew Kenneth Burroughs
    • 1
  1. 1.The Royal Free Sheila Sherlock Liver Centre and University Department of SurgeryRoyal Free HospitalLondonUK
  2. 2.Department of HistopathologyRoyal Free HospitalLondonUK
  3. 3.Department of OncologyRoyal Free HospitalLondonUK

Personalised recommendations