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Hepatocellular Carcinoma

  • Irene Bargellini
  • Laura Coletti
  • Giulia Lorenzoni
Chapter
Part of the Cancer Dissemination Pathways book series (CDP)

Abstract

HCC is the third leading cause of cancer-related death worldwide. It is more frequently associated with liver cirrhosis, developing through a long-lasting process of carcinogenesis involving several steps, from regenerative nodules to overt HCC. In cirrhotic patients, HCC can be reliably diagnosed by non-invasive dynamic imaging, when the typical wash-in/wash-out pattern is identified. Besides these radiological hallmarks, several imaging features can be detected indicating different biological aggressiveness and risk of metastasis. The main dissemination pathway for HCC is through the venous circulation causing microvascular and macrovascular invasion, as well as extrahepatic tumour spread. Staging and treatment options are based not only on tumour extension but also on liver function and general clinical conditions. Patients’ prognosis is mainly related to the intrahepatic tumour burden, since mortality is predominantly determined by liver failure secondary to tumour progression. Metastases are relatively infrequent and are indicators of tumour aggressiveness, reducing the chances for cure. The chapter will review main imaging features associated with HCC prognosis and routes of tumour dissemination and discuss treatment options in relation to HCC staging and sites of metastasis.

References

  1. 1.
    Ferlay J, Soerjomataram II, Dikshit R et al (2014) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386PubMedCrossRefGoogle Scholar
  2. 2.
    Njei B, Rotman Y, Ditah I, Lim JK (2015) Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology 61:191–199PubMedCrossRefGoogle Scholar
  3. 3.
    European Association for the Study of the Liver; European Organisation for Research and Treatment of Cancer (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56(4):908–943CrossRefGoogle Scholar
  4. 4.
    Bucci L, Garuti F, Lenzi B, et al.; Italian Liver Cancer (ITA.LI.CA) Group (2016) The evolutionary scenario of hepatocellular carcinoma in Italy: an update. Liver Int.  https://doi.org/10.1111/liv.13204. [Epub ahead of print]
  5. 5.
    Younossi ZM, Otgonsuren M, Henry L et al (2015) Association of nonalcoholic fatty liver disease (NAFLD) with hepatocellular carcinoma (HCC) in the United States from 2004 to 2009. Hepatology 62(6):1723–1730PubMedCrossRefGoogle Scholar
  6. 6.
    Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    International Consensus Group for Hepatocellular Neoplasia (2009) Pathologic diagnosis of early hepatocellular carcinoma: a report of the International Consensus Group for Hepatocellular Neoplasia. Hepatology 49:658–664CrossRefGoogle Scholar
  8. 8.
    Roncalli M, Terracciano L, Di Tommaso L, David E, Colombo M, Gruppo Italiano Patologi Apparato Digerente (GIPAD); Società Italiana di Anatomia Patologica e Citopatologia Diagnostica/International Academy of Pathology, Italian division (SIAPEC/IAP) (2011) Liver precancerous lesions and hepatocellular carcinoma: the histology report. Dig Liver Dis 43(suppl 4):S361–S372PubMedCrossRefGoogle Scholar
  9. 9.
    Yamamoto T, Hirohashi K, Kaneda K et al (2001) Relationship of the microvascular type to the tumor size, arterialization and dedifferentiation of human hepatocellular carcinoma. Jpn J Cancer Res 92:1207–1213PubMedCrossRefGoogle Scholar
  10. 10.
    Park YN, Yang CP, Fernandez GJ, Cubukcu O, Thung SN, Theise ND (1998) Neoangiogenesis and sinusoidal “capillarization” in dysplastic nodules of the liver. Am J Surg Pathol 22:656–662PubMedCrossRefGoogle Scholar
  11. 11.
    Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology 272(3):635–654PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Kudo M (2009) Multistep human hepatocarcinogenesis: correlation of imaging with pathology. J Gastroenterol 44(suppl 19):112–118PubMedCrossRefGoogle Scholar
  13. 13.
    Roskams T, Kojiro M (2010) Pathology of early hepatocellular carcinoma: conventional and molecular diagnosis. Semin Liver Dis 30:17–25PubMedCrossRefGoogle Scholar
  14. 14.
    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 36:264–272PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Park HS, Lee JM, Kim SH et al (2009) Differentiation of well-differentiated hepatocellular carcinomas from other hepatocellular nodules in cirrhotic liver: value of SPIO-enhanced MR imaging at 3.0 tesla. J Magn Reson Imaging 29:328–335PubMedCrossRefGoogle Scholar
  16. 16.
    Bartolozzi C, Crocetti L, Lencioni R, Cioni D, Della Pina C, Campani D (2007) Biliary and reticuloendothelial impairment in hepatocarcinogenesis: the diagnostic role of tissue-specific MR contrast media. Eur Radiol 17:2519–2530PubMedCrossRefGoogle Scholar
  17. 17.
    Paradis V (2013) Histopathology of hepatocellular carcinoma. Recent Results Cancer Res 190:21–32PubMedCrossRefGoogle Scholar
  18. 18.
    Adhoute X, Penaranda G, Raoul JL, Bourlière M (2016) Hepatocellular carcinoma scoring and staging systems. Do we need new tools? J Hepatol 64(6):1449–1450PubMedCrossRefGoogle Scholar
  19. 19.
    Llovet JM, Brú C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19(3):329–338PubMedCrossRefGoogle Scholar
  20. 20.
    Bruix J, Reig M, Sherman M (2016) Evidence-based diagnosis, staging, and treatment of patients with hepatocellular carcinoma. Gastroenterology 150(4):835–853PubMedCrossRefGoogle Scholar
  21. 21.
    Oken M, Creech R, Tormey D et al (1982) Toxicity and response criteria of the eastern cooperative oncology group. Am J Clin Oncol 5:649–655PubMedCrossRefGoogle Scholar
  22. 22.
    Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60:646–649PubMedCrossRefGoogle Scholar
  23. 23.
    Livraghi T, Meloni F, Di Stasi M et al (2008) Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: is resection still the treatment of choice? Hepatology 47:82–89PubMedCrossRefGoogle Scholar
  24. 24.
    Cucchetti A, Piscaglia F, Cescon M et al (2013) Cost-effectiveness of hepatic resection versus percutaneous radiofrequency ablation for early hepatocellular carcinoma. J Hepatol 59:300–307PubMedCrossRefGoogle Scholar
  25. 25.
    Roberts JP, Venook A, Kerlan R et al (2010) Hepatocellular carcinoma: ablate and wait versus rapid transplantation. Liver Transpl 16:925–929PubMedCrossRefGoogle Scholar
  26. 26.
    Ferrer-Fàbrega J, Forner A, Liccioni A et al (2016) Prospective validation of “ab initio” liver transplantation in hepatocellular carcinoma upon detection of risk factors for recurrence after resection. Hepatology 63:839–849PubMedCrossRefGoogle Scholar
  27. 27.
    Mazzaferro V, Regalia E, Doci R et al (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334(11):693–699PubMedCrossRefGoogle Scholar
  28. 28.
    Yao FY, Ferrell L, Bass NM et al (2001) Liver transplantation for hepatocellular carcinoma: expansion of the tumor size limits does not adversely impact survival. Hepatology 33(6):1394–1403PubMedCrossRefGoogle Scholar
  29. 29.
    Mazzaferro V, Llovet JM, Miceli R, et al.; Metroticket Investigator Study Group (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10(1):35–43Google Scholar
  30. 30.
    Clavien PA, Lesurtel M, Bossuyt PM, Gores GJ, Langer B, Perrier A, OLT for HCC Consensus Group (2012) Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol 13(1):e11–e22PubMedCrossRefGoogle Scholar
  31. 31.
    Majno P, Lencioni R, Mornex F, Girard N, Poon RT, Cherqui D (2011) Is the treatment of hepatocellular carcinoma on the waiting list necessary? Liver Transpl 17(Suppl 2):S98–108PubMedCrossRefGoogle Scholar
  32. 32.
    Lu DS, Yu NC, Raman SS et al (2005) Radiofrequency ablation of hepatocellular carcinoma: treatment success as defined by histologic examination of the explanted liver. Radiology 234(3):954–960PubMedCrossRefGoogle Scholar
  33. 33.
    Peng ZW, Zhang YJ, Chen MS et al (2013) Radiofrequency ablation with or without transcatheter arterial chemoembolization in the treatment of hepatocellular carcinoma: a prospective randomized trial. J Clin Oncol 31(4):426–432PubMedCrossRefGoogle Scholar
  34. 34.
    Cha C, Fong Y, Jarnagin WR, Blumgart LH, DeMatteo RP (2003) Predictors and patterns of recurrence after resection of hepatocellular carcinoma. J Am Coll Surg 197:753–758PubMedCrossRefGoogle Scholar
  35. 35.
    Lencioni R, Cioni D, Crocetti L et al (2005) Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous image-guided radiofrequency ablation. Radiology 234(3):961–967PubMedCrossRefGoogle Scholar
  36. 36.
    Yang B, Zou J, Xia J et al (2011) Risk factors for recurrence of small hepatocellular carcinoma after long-term follow-up of percutaneous radiofrequency ablation. Eur J Radiol 79(2):196–200PubMedCrossRefGoogle Scholar
  37. 37.
    Bruix J, Takayama T, Mazzaferro V et al.; STORM investigators (2015) Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol 16(13):1344–1354Google Scholar
  38. 38.
    Llovet JM, Real MI, Montana X et al (2002) Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet 359:1734–1739PubMedCrossRefGoogle Scholar
  39. 39.
    Llovet JM, Bruix J (2003) Systematic review of randomized trials for unresectable hepatocellular carcinoma: chemoembolization improves survival. Hepatology 37:429–442PubMedCrossRefGoogle Scholar
  40. 40.
    Lencioni R, de Baere T, Soulen MC, Rilling WS, Geschwind JF (2016) Lipiodol transarterial chemoembolization for hepatocellular carcinoma: a systematic review of efficacy and safety data. Hepatology 64(1):106–116PubMedCrossRefGoogle Scholar
  41. 41.
    Burrel M, Reig M, Forner A et al (2012) Survival of patients with hepatocellular carcinoma treated by transarterial chemoembolisation (TACE) using drug eluting beads. Implications for clinical practice and trial design. J Hepatol 56:1330–1335PubMedCrossRefGoogle Scholar
  42. 42.
    Malagari K, Pomoni M, Moschouris H et al (2012) Chemoembolization with doxorubicin-eluting beads for unresectable hepatocellular carcinoma: five-year survival analysis. Cardiovasc Intervent Radiol 35:1119–1128PubMedCrossRefGoogle Scholar
  43. 43.
    Takayasu K, Arii S, Kudo M et al (2012) Superselective transarterial chemoembolization for hepatocellular carcinoma. Validation of treatment algorithm proposed by Japanese guidelines. J Hepatol 56:886–892PubMedCrossRefGoogle Scholar
  44. 44.
    Lencioni R, Llovet JM, Han G et al (2016) Sorafenib or placebo plus TACE with doxorubicin-eluting beads for intermediate stage HCC: the SPACE trial. J Hepatol 64(5):1090–1098PubMedCrossRefGoogle Scholar
  45. 45.
    Kudo M, Han G, Finn RS et al (2014) Brivanib as adjuvant therapy to transarterial chemoembolization in patients with hepatocellular carcinoma: a randomized phase III trial. Hepatology 60:1697–1707PubMedCrossRefGoogle Scholar
  46. 46.
    Salem R, Lewandowski RJ, Kulik L et al (2011) Radioembolization results in longer time-to-progression and reduced toxicity compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology 140(2):497–507PubMedCrossRefGoogle Scholar
  47. 47.
    Moreno-Luna LE, Yang JD, Sanchez W et al (2013) Efficacy and safety of transarterial radioembolization versus chemoembolization in patients with hepatocellular carcinoma. Cardiovasc Intervent Radiol 36(3):714–723PubMedCrossRefGoogle Scholar
  48. 48.
    Cucchetti A, Djulbegovic B, Tsalatsanis A et al (2015) When to perform hepatic resection for intermediate-stage hepatocellular carcinoma. Hepatology 61(3):905–914PubMedCrossRefGoogle Scholar
  49. 49.
    Yao FY, Mehta N, Flemming J et al (2015) Downstaging of hepatocellular cancer before liver transplant: long-term outcome compared to tumors within Milan criteria. Hepatology 61(6):1968–1977PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Bolondi L, Burroughs A, Dufour JF et al (2012) Heterogeneity of patients with intermediate (BCLC B) hepatocellular carcinoma: proposal for a subclassification to facilitate treatment decisions. Semin Liver Dis 32(4):348–359PubMedGoogle Scholar
  51. 51.
    Cheng AL, Kang YK, Chen Z et al (2009) Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10(1):25–34PubMedCrossRefGoogle Scholar
  52. 52.
    Llovet JM, Ricci S, Mazzaferro V et al.; SHARP Investigators Study Group (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359(4):378–390Google Scholar
  53. 53.
    Bruix J, Qin S, Merle P et al.; RESORCE Investigators (2017) Regorafenib for patients with hepatocellular carcinoma who progressed on sorafenib treatment (RESORCE): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 389(10064):56–66Google Scholar
  54. 54.
    Mazzaferro V, Sposito C, Bhoori S et al (2013) Yttrium-90 radioembolization for intermediate-advanced hepatocellular carcinoma: a phase 2 study. Hepatology 57(5):1826–1837PubMedCrossRefGoogle Scholar
  55. 55.
    Sangro B, Carpanese L, Cianni R et al.; European Network on Radioembolization with Yttrium-90 Resin Microspheres (ENRY) (2011) Survival after yttrium-90 resin microsphere radioembolization of hepatocellular carcinoma across Barcelona clinic liver cancer stages: a European evaluation. Hepatology 54(3):868–878Google Scholar
  56. 56.
    Gramenzi A, Golfieri R, Mosconi C et al.; BLOG (Bologna Liver Oncology Group) (2015) Yttrium-90 radioembolization vs sorafenib for intermediate-locally advanced hepatocellular carcinoma: a cohort study with propensity score analysis. Liver Int 35(3):1036–1047Google Scholar
  57. 57.
    Kokudo T, Hasegawa K, Matsuyama Y et al.; Liver Cancer Study Group of Japan (2016) Survival benefit of liver resection for hepatocellular carcinoma associated with portal vein invasion. J Hepatol 65(5):938–943Google Scholar
  58. 58.
    Yau T, Tang VY, Yao TJ, Fan ST, Lo CM, Poon RT (2014) Development of Hong Kong liver cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology 146(7):1691–1700.e3PubMedCrossRefGoogle Scholar
  59. 59.
    Kutami R, Nakashima Y, Nakashima O, Shiota K, Kojiro M (2000) Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J Hepatol 33(2):282–289PubMedCrossRefGoogle Scholar
  60. 60.
    ACR American College of Radiology. http://www.acr.org/Quality-Safety/Resources/LIRADS. Accessed 27 Oct 2016
  61. 61.
    Mitchell DG, Bruix J, Sherman M, Sirlin CB (2015) LI-RADS (Liver Imaging Reporting and Data System): summary, discussion, and consensus of the LI-RADS Management Working Group and future directions. Hepatology 61(3):1056–1065PubMedCrossRefGoogle Scholar
  62. 62.
    Li M, Xin Y, Fu S et al (2016) Corona enhancement and mosaic architecture for prognosis and selection between of liver resection versus transcatheter arterial chemoembolization in single hepatocellular carcinomas >5  cm without extrahepatic metastases: an imaging-based retrospective study. Medicine (Baltimore) 95(2):e2458CrossRefGoogle Scholar
  63. 63.
    Ishigami K, Yoshimitsu K, Nishihara Y et al (2009) Hepatocellular carcinoma with a pseudocapsule on gadolinium-enhanced MR images: correlation with histopathologic findings. Radiology 250(2):435–443PubMedCrossRefGoogle Scholar
  64. 64.
    Iguchi T, Aishima S, Sanefuji K et al (2009) Both fibrous capsule formation and extracapsular penetration are powerful predictors of poor survival in human hepatocellular carcinoma: a histological assessment of 365 patients in Japan. Ann Surg Oncol 16(9):2539–2546PubMedCrossRefGoogle Scholar
  65. 65.
    Nishie A, Yoshimitsu K, Asayama Y et al (2008) Radiologic detectability of minute portal venous invasion in hepatocellular carcinoma. AJR Am J Roentgenol 190(1):81–87PubMedCrossRefGoogle Scholar
  66. 66.
    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):1744–1751PubMedCrossRefGoogle Scholar
  67. 67.
    Sakon M, Nagano H, Nakamori S et al (2002) Intrahepatic recurrences of hepatocellular carcinoma after hepatectomy: analysis based on tumor hemodynamics. Arch Surg 137(1):94–99PubMedCrossRefGoogle Scholar
  68. 68.
    Trevisani F, Cantarini MC, Wands JR, Bernardi M (2008) Recent advances in the natural history of hepatocellular carcinoma. Carcinogenesis 29(7):1299–1305PubMedCrossRefGoogle Scholar
  69. 69.
    Wang J, Li Q, Sun Y et al (2009) Clinicopathologic features between multicentric occurrence and intrahepatic metastasis of multiple hepatocellular carcinomas related to HBV. Surg Oncol 18(1):25–30PubMedCrossRefGoogle Scholar
  70. 70.
    Gouw AS, Balabaud C, Kusano H, Todo S, Ichida T, Kojiro M (2011) Markers for microvascular invasion in hepatocellular carcinoma: where do we stand? Liver Transpl 17(Suppl 2):S72–S80PubMedCrossRefGoogle Scholar
  71. 71.
    Okamura S, Sumie S, Tonan T et al (2016) Diffusion-weighted magnetic resonance imaging predicts malignant potential in small hepatocellular carcinoma. Dig Liver Dis 48(8):945–952PubMedCrossRefGoogle Scholar
  72. 72.
    Asman Y, Evenson AR, Even-Sapir E, Shibolet O (2015) [18F]fludeoxyglucose positron emission tomography and computed tomography as a prognostic tool before liver transplantation, resection, and loco-ablative therapies for hepatocellular carcinoma. Liver Transpl 21(5):572–580PubMedCrossRefGoogle Scholar
  73. 73.
    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):792–800PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Segal E, Sirlin CB, Ooi C et al (2007) Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol 25(6):675–680PubMedCrossRefGoogle Scholar
  75. 75.
    Nakashima Y, Nakashima O, Tanaka M, Okuda K, Nakashima M, Kojiro M (2003) Portal vein invasion and intrahepatic micrometastasis in small hepatocellular carcinoma by gross type. Hepatol Res 26(2):142–147PubMedCrossRefGoogle Scholar
  76. 76.
    Reynolds AR, Furlan A, Fetzer DT et al (2015) Infiltrative hepatocellular carcinoma: what radiologists need to know. Radiographics 35(2):371–386PubMedCrossRefGoogle Scholar
  77. 77.
    Engelbrecht M, Akin O, Dixit D, Schwartz L (2011) Bland and tumor thrombi in abdominal malignancies: magnetic resonance imaging assessment in a large oncologic patient population. Abdom Imaging 36(1):62–68PubMedCrossRefGoogle Scholar
  78. 78.
    Ascenti G, Sofia C, Mazziotti S et al (2016) Dual-energy CT with iodine quantification in distinguishing between bland and neoplastic portal vein thrombosis in patients with hepatocellular carcinoma. Clin Radiol 71(9):938.e1-9PubMedCrossRefGoogle Scholar
  79. 79.
    Catalano OA, Choy G, Zhu A, Hahn PF, Sahani DV (2010) Differentiation of malignant thrombus from bland thrombus of the portal vein in patients with hepatocellular carcinoma: application of diffusion-weighted MR imaging. Radiology 254(1):154–162PubMedCrossRefGoogle Scholar
  80. 80.
    Sinn DH, Cho JY, Gwak GY et al (2015) Different survival of Barcelona clinic liver cancer stage C hepatocellular carcinoma patients by the extent of portal vein invasion and the type of extrahepatic spread. PLoS One 10(4):e0124434PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Shi J, Lai EC, Li N et al (2011) A new classification for hepatocellular carcinoma with portal vein tumor thrombus. J Hepatobiliary Pancreat Sci 18(1):74–80PubMedCrossRefGoogle Scholar
  82. 82.
    Yang T, Lin C, Zhai J et al (2012) Surgical resection for advanced hepatocellular carcinoma according to Barcelona Clinic Liver Cancer (BCLC) staging. J Cancer Res Clin Oncol 138(7):1121–1129PubMedCrossRefGoogle Scholar
  83. 83.
    Prajapati HJ, Dhanasekaran R, El-Rayes BF et al (2013) Safety and efficacy of doxorubicin drug-eluting bead transarterial chemoembolization in patients with advanced hepatocellular carcinoma. J Vasc Interv Radiol 24(3):307–315PubMedCrossRefGoogle Scholar
  84. 84.
    Kokudo T, Hasegawa K, Yamamoto S et al (2014) Surgical treatment of hepatocellular carcinoma associated with hepatic vein tumor thrombosis. J Hepatol 61(3):583–588PubMedCrossRefGoogle Scholar
  85. 85.
    Zhang YF, Wei W, Guo ZX, Wang JH, Shi M, Guo RP (2015) Hepatic resection versus transcatheter arterial chemoembolization for the treatment of hepatocellular carcinoma with hepatic vein tumor thrombus. Jpn J Clin Oncol 45(9):837–843PubMedCrossRefGoogle Scholar
  86. 86.
    Qiao W, Yu F, Wu L et al (2016) Surgical outcomes of hepatocellular carcinoma with biliary tumour thrombus: a systematic review. BMC Gastroenterol 16:11PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Rammohan A, Sathyanesan J, Rajendran K et al (2015) Bile duct thrombi in hepatocellular carcinoma: is aggressive surgery worthwhile? HPB 17:508–513PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Ueda M, Takeuchi T, Takayasu T et al (1994) Classification and surgical treatment of hepatocellular carcinoma (HCC) with bile duct thrombi. Hepato-Gastroenterology 41:349–354PubMedGoogle Scholar
  89. 89.
    Yoo JJ, Lee JH, Lee SH et al (2014) Comparison of the effects of transarterial chemoembolization for advanced hepatocellular carcinoma between patients with and without extrahepatic metastases. PLoS One 9(11):e113926PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Natsuizaka M, Omura T, Akaike T et al (2005) Clinical features of hepatocellular carcinoma with extrahepatic metastases. J Gastroenterol Hepatol 20(11):1781–1787PubMedCrossRefGoogle Scholar
  91. 91.
    Katyal S, Oliver JH 3rd, Peterson MS, Ferris JV, Carr BS, Baron RL (2000) Extrahepatic metastases of hepatocellular carcinoma. Radiology 216(3):698–703PubMedCrossRefGoogle Scholar
  92. 92.
    Sneag DB, Krajewski K, Giardino A et al (2011) Extrahepatic spread of hepatocellular carcinoma: spectrum of imaging findings. AJR Am J Roentgenol 197(4):W658–W664PubMedCrossRefGoogle Scholar
  93. 93.
    Uchino K, Tateishi R, Shiina S et al (2011) Hepatocellular carcinoma with extrahepatic metastasis: clinical features and prognostic factors. Cancer 117(19):4475–4483PubMedCrossRefGoogle Scholar
  94. 94.
    Jung SM, Jang JW, You CR et al (2012) Role of intrahepatic tumor control in the prognosis of patients with hepatocellular carcinoma and extrahepatic metastases. J Gastroenterol Hepatol 27(4):684–689PubMedCrossRefGoogle Scholar
  95. 95.
    Lee HS (2011) Management of patients with hepatocellular carcinoma and extrahepatic metastasis. Dig Dis 29(3):333–338PubMedCrossRefGoogle Scholar
  96. 96.
    Kwon JB, Park K, Kim YD et al (2008) Clinical outcome after pulmonary metastasectomy from primary hepatocellular carcinoma: analysis of prognostic factors. World J Gastroenterol 14(37):5717–5722PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Kitano K, Murayama T, Sakamoto M et al (2012) Outcome and survival analysis of pulmonary metastasectomy for hepatocellular carcinoma. Eur J Cardiothorac Surg 41(2):376–382PubMedCrossRefGoogle Scholar
  98. 98.
    Hiraki T, Yamakado K, Ikeda O et al (2011) Percutaneous radiofrequency ablation for pulmonary metastases from hepatocellular carcinoma: results of a multicenter study in Japan. J Vasc Interv Radiol 22(6):741–748PubMedCrossRefGoogle Scholar
  99. 99.
    Kaczynski J, Hansson G, Wallerstedt S (1995) Metastases in cases with hepatocellular carcinoma in relation to clinicopathologic features of the tumor. An autopsy study from a low endemic area. Acta Oncol 34(1):43–48PubMedCrossRefGoogle Scholar
  100. 100.
    Dodd GD 3rd, Baron RL, Oliver JH III, Federle MP, Baumgartel PB (1997) Enlarged abdominal lymph nodes in end-stage cirrhosis: CT-histopathologic correlation in 507 patients. Radiology 203(1):127–130PubMedCrossRefGoogle Scholar
  101. 101.
    Kobayashi S, Takahashi S, Kato Y et al (2011) Surgical treatment of lymph node metastases from hepatocellular carcinoma. J Hepatobiliary Pancreat Sci 18(4):559–566PubMedCrossRefGoogle Scholar
  102. 102.
    Mou Y, Zhao Q, Zhong L, Chen F, Jiang T (2016) Preliminary results of ultrasound-guided laser ablation for unresectable metastases to retroperitoneal and hepatic portal lymph nodes. World J Surg Oncol 14(1):165PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Fukutomi M, Yokota M, Chuman H et al (2001) Increased incidence of bone metastases in hepatocellular carcinoma. Eur J Gastroenterol Hepatol 13(9):1083–1088PubMedCrossRefGoogle Scholar
  104. 104.
    Seong J, Koom WS, Park HC (2005) Radiotherapy for painful bone metastases from hepatocellular carcinoma. Liver Int 25(2):261–265PubMedCrossRefGoogle Scholar
  105. 105.
    Kashima M, Yamakado K, Takaki H et al (2010) Radiofrequency ablation for the treatment of bone metastases from hepatocellular carcinoma. AJR Am J Roentgenol 194(2):536–541PubMedCrossRefGoogle Scholar
  106. 106.
    Ogura K, Miyake R, Shiina S et al (2012) Bone radiofrequency ablation combined with prophylactic internal fixation for metastatic bone tumor of the femur from hepatocellular carcinoma. Int J Clin Oncol 17(4):417–421PubMedCrossRefGoogle Scholar
  107. 107.
    Hasegawa T, Yamakado K, Nakatsuka A et al (2015) Unresectable adrenal metastases: clinical outcomes of radiofrequency ablation. Radiology 277(2):584–593PubMedCrossRefGoogle Scholar
  108. 108.
    Jung J, Yoon SM, Park HC et al (2016) Radiotherapy for adrenal metastasis from hepatocellular carcinoma: a multi-institutional retrospective study (KROG 13-05). PLoS One 11(3):e0152642PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Park JS, Yoon DS, Kim KS et al (2007) What is the best treatment modality for adrenal metastasis from hepatocellular carcinoma? J Surg Oncol 96(1):32–36PubMedCrossRefGoogle Scholar
  110. 110.
    Yamakado K, Anai H, Takaki H et al (2009) Adrenal metastasis from hepatocellular carcinoma: radiofrequency ablation combined with adrenal arterial chemoembolization in six patients. AJR Am J Roentgenol 192(6):W300–W305PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Irene Bargellini
    • 1
  • Laura Coletti
    • 2
  • Giulia Lorenzoni
    • 1
  1. 1.Department of Interventional RadiologyPisa University HospitalPisaItaly
  2. 2.Department of Liver Surgery and TransplantationPisa University HospitalPisaItaly

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