Abstract
Background
Few details of the clinical features of hepatocellular carcinoma (HCC) developing extrahepatic recurrence after a curative resection have been published. The purpose of this study was to clarify the clinicopathologic findings of patients with HCC who experienced extrahepatic metastases.
Methods
Clinicopathologic data were available for 119 patients who underwent an R0 resection for HCC. Twenty-three patients who developed extrahepatic metastases during the follow-up period were compared with the patients who remained free from recurrence for at least 5 years after resection (n = 21) or with only intrahepatic recurrences (n = 75).
Results
Patients with extrahepatic recurrences were more likely to have their tumor macro- or microscopically invading the tumor capsule (P < 0.001) and hepatic vein (P = 0.003), a high AFP concentration (P = 0.014), and advanced TNM stage (P = 0.006) than the other patients. As for treatment-related variables, inflow vessel occlusion during hepatectomy was less frequently associated with extrahepatic recurrences than if it were not performed (P < 0.001). By multivariate analysis, absence of tumor invasion to the capsule (relative risk [RR] = 0.080; P = 0.023) or to the hepatic vein (RR = 0.108; P = 0.014) and a hepatectomy in which inflow vessel occlusions were performed (RR = 0.161; P = 0.004) were selected as independent factors for reducing extrahepatic recurrences after a hepatectomy.
Conclusion
In HCC patients, the control of intrahepatic recurrences and extrahepatic recurrences after a hepatectomy is important to improve the prognosis. Inflow occlusion during the hepatectomy may reduce HCC metastases to extrahepatic sites.
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Abbreviations
- AFP:
-
α-fetoprotein
- CH:
-
Chronic hepatitis
- CT:
-
Computed tomography
- HbsAg:
-
anti-HB surface antigen
- HbcAb:
-
anti-HB core antibody
- HCVAb:
-
Hepatitis C virus antibody
- HCC:
-
Hepatocellular carcinoma
- Hx:
-
Hepatectomy
- ICGR15:
-
Indocyanine green retention rate at 15 min
- LC:
-
Liver cirrhosis
- Moderate:
-
Moderately differentiated hepatocellular carcinoma
- NBNC:
-
Non-B viral non-C viral
- NL:
-
Normal liver
- Poor:
-
Poorly differentiated hepatocellular carcinoma
- PS:
-
Prediction score
- PT-INR:
-
Prothrombin time as the International Normalized Ratio
- Well:
-
Welldifferentiated hepatocellular carcinoma
References
Uka K, Aikata H, Takaki S et al (2007) Clinical features and prognosis of patients with extrahepatic metastases from hepatocellular carcinoma. World J Gastroenterol 13:414–420
Lo CM, Lai EC, Fan ST et al (1994) Resection for extrahepatic recurrence of hepatocellular carcinoma. Br J Surg 81:1019–1021
Poon RT, Fan ST, O’Suilleabhain CB et al (2002) Aggressive management of patients with extrahepatic and intrahepatic recurrences of hepatocellular carcinoma by combined resection and locoregional therapy. J Am Coll Surg 195:311–318
Yang Y, Nagano H, Ota H et al (2007) Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery 141:196–202
Shimada M, Takenaka K, Gion T et al (1996) Prognosis of recurrent hepatocellular carcinoma: a 10-year surgical experience in Japan. Gastroenterology 111:720–726
Ishii H, Furuse J, Kinoshita T et al (2004) Extrahepatic spread from hepatocellular carcinoma: who are candidates for aggressive anti-cancer treatment? Jpn J Clin Oncol 34:733–739
Yamanaka N, Okamoto E, Oriyama T et al (1994) A prediction scoring system to select the surgical treatment of liver cancer. Further refinement based on 10 years of use. Ann Surg 219:342–346
The Brisbane 2000 Terminology of Liver Anatomy and Resection (2000) Terminology Committee of the International Hepato-Pancreato-Biliary Association. HPB 2:333–239
Makuuchi M, Mori T, Gunvén P et al (1987) Safety of hemihepatic vascular occlusion during resection of the liver. Surg Gynecol Obstet 164:155–158
Takasaki K, Kobayashi S, Tanaka S et al (1986) Highly selected hepatic resection by Glissonean sheath-binding method. Dig Surg 3:121
Tanaka K, Shimada H, Togo S et al (1999) Use of transcatheter arterial infusion of anti-cancer agents with lipiodol to prevent recurrence of hepatocellular carcinoma after hepatic resection. Hepatogastroenterology 46:1083–1089
Greene FL, Page DL, Fleming ID et al (2002) AJCC cancer staging manual, 6th edn. Springer, Chicago, pp 131–144
Ichida F, Tsuji T, Omata M et al (1996) New Inuyama classification for histological assessment of chronic hepatitis. Int Hepatol Commun 6:112–119
Katyal S, Oliver JH 3rd, Peterson MS et al (2000) Extrahepatic metastases of hepatocellular carcinoma. Radiology 216:698–703
Natsuizaka M, Omura T, Akaike T et al (2005) Clinical features of hepatocellular carcinoma with extrahepatic metastases. J Gastroenterol Hepatol 20:1781–1787
Nakashima T, Okuda K, Kojiro M et al (1983) Pathology of hepatocellular carcinoma in Japan: 232 consecutive cases autopsied in ten years. Cancer 51:863–877
Yuki K, Hirohashi S, Sakamoto M et al (1990) Growth and spread of hepatocellular carcinoma. A review of 240 consecutive autopsy cases. Cancer 66:2174–2179
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 34:43–48
The Liver Cancer Study Group of Japan (1990) Primary liver cancer in Japan. Ann Surg 211:277–287
Kim PN, Kim IY, Lee KS (1994) Intraperitoneal seeding from hepatoma. Abdom Imaging 19:309–312
Schwartz JD, Schwartz M, Mandeli J et al (2002) Neoadjuvant and adjuvant therapy for resectable hepatocellular carcinoma: review of the randomised clinical trials. Lancet Oncol 3:593–603
Ono T, Yamanoi A, Nazmy El et al (2001) Adjuvant chemotherapy after resection of hepatocellular carcinoma causes deterioration of long-term prognosis in cirrhotic patients: metaanalysis of three randomized controlled trials. Cancer 91:2378–2385
Nowak AK, Chow PK, Findlay M (2004) Systemic therapy for advanced hepatocellular carcinoma: a review. Eur J Cancer 40:1474–1484
Lam CM, Lo CM, Yuen WK et al (1998) Prolonged survival in selected patients following surgical resection for pulmonary metastasis from hepatocellular carcinoma. Br J Surg 85:1198–1200
Belghiti J, Panis Y, Farges O et al (1991) Intrahepatic recurrence after resection of hepatocellular carcinoma complicating cirrhosis. Ann Surg 214:114–117
Pompili M, Rapaccini GL, de Luca F et al (1997) Risk factors for intrahepatic recurrence of hepatocellular carcinoma in cirrhotic patients treated by percutaneous ethanol injection. Cancer 79:1501–1508
Takata M, Yamanaka N, Tanaka T et al (2000) What patients can survive disease free after complete resection for hepatocellular carcinoma? A multivariate analysis. Jpn J Clin Oncol 30:75–81
Yeh CN, Chen MF (2004) Resection of peritoneal implantation of hepatocellular carcinoma after hepatic resection: risk factors and prognostic analysis. World J Surg 28:382–386
Wu CC, Ho YZ, Ho WL et al (1995) Preoperative transcatheter arterial chemoembolization for resectable large hepatocellular carcinoma: a reappraisal. Br J Surg 82:122–126
Yamanaka N, Okamoto E, Fujihara S et al (1992) Do the tumor cells of hepatocellular carcinomas dislodge into the portal venous stream during hepatic resection? Cancer 70:2263–2267
Yamanaka N, Okamoto E, Toyosaka A et al (1990) Prognostic factors after hepatectomy for hepatocellular carcinomas. A univariate and multivariate analysis. Cancer 65:1104–1110
Vauthey JN, Klimstra D, Franceschi D et al (1995) Factors affecting long-term outcome after hepatic resection for hepatocellular carcinoma. Am J Surg 169:28–34
Sakon M, Nagano H, Nakamori S et al (2002) Intrahepatic recurrences of hepatocellular carcinoma after hepatectomy: analysis based on tumor hemodynamics. Arch Surg 137:94–99
Matsumata T, Kanematsu T, Takenaka K et al (1989) Patterns of intrahepatic recurrence after curative resection of hepatocellular carcinoma. Hepatology 9:457–460
Makino I, Chijiiwa K, Kondo K et al (2005) Prognostic benefit of selective portal vein occlusion during hepatic resection for hepatocellular carcinoma. Surgery 137:626–631
Kim YI, Ishii T, Aramaki M et al (1995) The Pringle maneuver induces only partial ischemia of the liver. Hepatogastroenterology 42:169–171
Tatsuma T, Kim YI, Kai T et al (1995) Importance of hepatovenous back-perfusion for maintenance of liver viability during the Pringle maneuver. Br J Surg 82:1071–1075
van der Bilt JD, Kranenburg O, Verheem A et al (2006) Selective portal clamping to minimize hepatic ischaemia-reperfusion damage and avoid accelerated outgrowth of experimental colorectal liver metastases. Br J Surg 93:1015–1022
Gozzetti G, Mazziotti A, Grazi GL et al (1995) Liver resection without blood transfusion. Br J Surg 82:1105–1110
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Tanaka, K., Shimada, H., Matsuo, K. et al. Clinical Features of Hepatocellular Carcinoma Developing Extrahepatic Recurrences After Curative Resection. World J Surg 32, 1738–1747 (2008). https://doi.org/10.1007/s00268-008-9613-x
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DOI: https://doi.org/10.1007/s00268-008-9613-x