Skip to main content
Top
Published in: World Journal of Surgery 4/2013

01-04-2013

Clinicopathological Features of Recurrence in Patients After 10-year Disease-free Survival Following Curative Hepatic Resection of Hepatocellular Carcinoma

Authors: Masaki Kaibori, Shoji Kubo, Hiroaki Nagano, Michihiro Hayashi, Seiji Haji, Takuya Nakai, Morihiko Ishizaki, Kosuke Matsui, Takahiro Uenishi, Shigekazu Takemura, Hiroshi Wada, Shigeru Marubashi, Koji Komeda, Fumitoshi Hirokawa, Yasuyuki Nakata, Kazuhisa Uchiyama, A-Hon Kwon

Published in: World Journal of Surgery | Issue 4/2013

Login to get access

Abstract

Background

The present study aimed to clarify the clinicopathologic features of long-term disease-fee survival after resection of hepatocellular carcinoma (HCC).

Methods

This retrospective study identified 940 patients who underwent curative resection of HCC between 1991 and 2000 at five university hospitals. Seventy-four patients with 10 years of recurrence-free survival were identified and followed up. They were divided into two groups, 60 recurrence-free and 14 with recurrence after a 10-year recurrence-free period.

Results

Overall survival rates of recurrence and non-recurrence groups were 68 and 91 % at 16 years, and 34 and 91 % at 20 years (p = 0.02), respectively. There were five (36 %), and two deaths (3 %), respectively, after 10 recurrence-free years. A second resection for recurrence was performed in four patients (29 %), and mean survival was 15.3 years after the first hepatectomy. Although three patients in the non-recurrence group (5 %) developed esophageal and/or gastric varices, seven patients in the recurrence group (50 %) developed varices during 10 years (p < 0.0001). In multivariate analysis, preoperative and 10-year platelet count was identified as a favorable independent factor for maintained recurrence-free survival after a 10-year recurrence-free period following curative hepatic resection of HCC.

Conclusions

Recurrence of HCC may occur even after a 10-year recurrence-free period. Long-term follow-up after resection of HCC is important, and should be life-long. Patients with higher preoperative and 10-year platelet counts are more likely to have long-term survival after resection. A low platelet count, related to the degree of liver fibrosis, is a risk factor for recurrence and survival of HCC after curative resection.
Literature
1.
go back to reference Bosch X, Ribes J, Borras J (1999) Epidemiology of primary liver cancer. Semin Liver Dis 19:271–285PubMedCrossRef Bosch X, Ribes J, Borras J (1999) Epidemiology of primary liver cancer. Semin Liver Dis 19:271–285PubMedCrossRef
2.
go back to reference Taylor-Robinson SD, Foster GR, Arora S et al (1997) Increase in primary liver cancer in the UK 1979–94. Lancet 350:1142–1143PubMedCrossRef Taylor-Robinson SD, Foster GR, Arora S et al (1997) Increase in primary liver cancer in the UK 1979–94. Lancet 350:1142–1143PubMedCrossRef
3.
go back to reference EI-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340:745–750CrossRef EI-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340:745–750CrossRef
4.
go back to reference Kotoh K, Sakai H, Sakamoto S et al (1994) The effect of percutaneous ethanol injection therapy on small solitary hepatocellular carcinoma is comparable to that of hepatectomy. Am J Gastroenterol 89:194–198PubMed Kotoh K, Sakai H, Sakamoto S et al (1994) The effect of percutaneous ethanol injection therapy on small solitary hepatocellular carcinoma is comparable to that of hepatectomy. Am J Gastroenterol 89:194–198PubMed
5.
go back to reference Seki T, Wakabayashi M, Nakagawa T et al (1994) Ultrasonically guided percutaneous microwave coagulation therapy for small hepatocellular carcinoma. Cancer 74:817–825PubMedCrossRef Seki T, Wakabayashi M, Nakagawa T et al (1994) Ultrasonically guided percutaneous microwave coagulation therapy for small hepatocellular carcinoma. Cancer 74:817–825PubMedCrossRef
6.
go back to reference Chen MS, Li JO, Zheng Y et al (2006) A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg 243:321–328PubMedCrossRef Chen MS, Li JO, Zheng Y et al (2006) A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg 243:321–328PubMedCrossRef
7.
go back to reference Tung-Ping Poon R, Fan ST, Wong J (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24PubMedCrossRef Tung-Ping Poon R, Fan ST, Wong J (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24PubMedCrossRef
8.
go back to reference Nagasue N, Uchida M, Makino Y et al (1993) Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma. Gastroenterology 105:488–494PubMedCrossRef Nagasue N, Uchida M, Makino Y et al (1993) Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma. Gastroenterology 105:488–494PubMedCrossRef
9.
go back to reference Shirabe K, Shimada M, Kajiyama K et al (1998) Clinicopathologic features of patients with hepatocellular carcinoma surviving >10 years after hepatic resection. Cancer 83:2312–2316PubMedCrossRef Shirabe K, Shimada M, Kajiyama K et al (1998) Clinicopathologic features of patients with hepatocellular carcinoma surviving >10 years after hepatic resection. Cancer 83:2312–2316PubMedCrossRef
10.
go back to reference Poon RT, Ng IO, Fan ST et al (2001) Clinicopathologic features of long-term survivors and disease-free survivors after resection of hepatotocellular carcinoma: a study of a prospective cohort. J Clin Oncol 19:3037–3044PubMed Poon RT, Ng IO, Fan ST et al (2001) Clinicopathologic features of long-term survivors and disease-free survivors after resection of hepatotocellular carcinoma: a study of a prospective cohort. J Clin Oncol 19:3037–3044PubMed
11.
go back to reference Shimada K, Sano T, Sakamoto Y et al (2005) A long-term follow-up and management study of hepatocellular carcinoma patients surviving for 10 years or longer after curative hepatectomy. Cancer 104:1939–1947PubMedCrossRef Shimada K, Sano T, Sakamoto Y et al (2005) A long-term follow-up and management study of hepatocellular carcinoma patients surviving for 10 years or longer after curative hepatectomy. Cancer 104:1939–1947PubMedCrossRef
12.
go back to reference Fukuda S, Itamoto T, Amano H et al (2007) Clinicopathologic features of hepatocellular carcinoma patients with compensated cirrhosis surviving more than 10 years after curative hepatectomy. World J Surg 31:345–352PubMedCrossRef Fukuda S, Itamoto T, Amano H et al (2007) Clinicopathologic features of hepatocellular carcinoma patients with compensated cirrhosis surviving more than 10 years after curative hepatectomy. World J Surg 31:345–352PubMedCrossRef
13.
go back to reference Strasberg SM, Belghiti J, Clavn P-A et al (2000) The Brisbane 2000 terminology of liver anatomy and resection. Terminology committee of the international hepato-pancreato-biliary association. HPB 2:333–339 Strasberg SM, Belghiti J, Clavn P-A et al (2000) The Brisbane 2000 terminology of liver anatomy and resection. Terminology committee of the international hepato-pancreato-biliary association. HPB 2:333–339
14.
go back to reference Couinaud C (ed) (1957) Le Foie: Etudes Anatomiques et Chirurgicale. Masson, Paris Couinaud C (ed) (1957) Le Foie: Etudes Anatomiques et Chirurgicale. Masson, Paris
15.
go back to reference Kaibori M, Matsui Y, Hijikawa T et al (2006) Comparison of limited and anatomic hepatic resection for hepatocellular carcinoma with hepatitis C. Surgery 139:385–394PubMedCrossRef Kaibori M, Matsui Y, Hijikawa T et al (2006) Comparison of limited and anatomic hepatic resection for hepatocellular carcinoma with hepatitis C. Surgery 139:385–394PubMedCrossRef
16.
go back to reference Sobin LH, Wittekind C (eds) (1997) TNM classification of malignant tumors, 5th edn. Wiley, New York Sobin LH, Wittekind C (eds) (1997) TNM classification of malignant tumors, 5th edn. Wiley, New York
17.
go back to reference Kubo S, Tsukamoto T, Hirohashi K et al (2003) Appropriate surgical management of small hepatocellular carcinomas in patients infected with hepatitis C virus. World J Surg 27:437–442PubMedCrossRef Kubo S, Tsukamoto T, Hirohashi K et al (2003) Appropriate surgical management of small hepatocellular carcinomas in patients infected with hepatitis C virus. World J Surg 27:437–442PubMedCrossRef
18.
go back to reference Yamamoto J, Kosuge T, Takayama T et al (1996) Recurrence of hepatocellular carcinoma after surgery. Br J Surg 83:1219–1222PubMedCrossRef Yamamoto J, Kosuge T, Takayama T et al (1996) Recurrence of hepatocellular carcinoma after surgery. Br J Surg 83:1219–1222PubMedCrossRef
19.
go back to reference Poon RT, Fan ST, Lo CM et al (2002) Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 235:373–382PubMedCrossRef Poon RT, Fan ST, Lo CM et al (2002) Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 235:373–382PubMedCrossRef
20.
go back to reference Poon RT, Fan ST, Wong J et al (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24CrossRef Poon RT, Fan ST, Wong J et al (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24CrossRef
21.
go back to reference Chen WT, Chau GY, Lui WY et al (2004) Recurrent hepatocellular carcinoma after hepatic resection: prognostic factors and long-term outcome. Eur J Surg Oncol 30:414–420PubMedCrossRef Chen WT, Chau GY, Lui WY et al (2004) Recurrent hepatocellular carcinoma after hepatic resection: prognostic factors and long-term outcome. Eur J Surg Oncol 30:414–420PubMedCrossRef
22.
go back to reference Poon RT, Fan ST, Lo CM et al (1999) Intrahepatic recurrence after curative resection of hepatocellular carcinoma: long term results of treatment and prognostic factors. Ann Surg 229:216–222PubMedCrossRef Poon RT, Fan ST, Lo CM et al (1999) Intrahepatic recurrence after curative resection of hepatocellular carcinoma: long term results of treatment and prognostic factors. Ann Surg 229:216–222PubMedCrossRef
23.
go back to reference Lee PH, Lin WJ, Tsang YM et al (1995) Clinical management of recurrent hepatocellular carcinoma. Ann Surg 222:670–676PubMedCrossRef Lee PH, Lin WJ, Tsang YM et al (1995) Clinical management of recurrent hepatocellular carcinoma. Ann Surg 222:670–676PubMedCrossRef
24.
go back to reference Shimada M, Takenaka K, Taguchi K et al (1998) Prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 227:80–85PubMedCrossRef Shimada M, Takenaka K, Taguchi K et al (1998) Prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 227:80–85PubMedCrossRef
25.
go back to reference Kosuge T, Makuuchi M, Takayama T et al (1993) Long-term results after resection of hepatocellular carcinoma: experience of 480 cases. Hepatogastroenterology 40:328–332PubMed Kosuge T, Makuuchi M, Takayama T et al (1993) Long-term results after resection of hepatocellular carcinoma: experience of 480 cases. Hepatogastroenterology 40:328–332PubMed
26.
go back to reference Okada S, Shimada K, Yamamoto J et al (1994) Predictive factors for postoperative recurrence of hepatocellular carcinoma. Gastroenterology 106:1618–1624PubMed Okada S, Shimada K, Yamamoto J et al (1994) Predictive factors for postoperative recurrence of hepatocellular carcinoma. Gastroenterology 106:1618–1624PubMed
27.
go back to reference Ryu M, Shimamura Y, Kinoshita T et al (1997) Therapeutic results of resection, transcatheter arterial embolization and percutaneous transhepatic ethanol injection in 3225 patients with hepatocellular carcinoma: a retrospective multicenter study. Jpn J Clin Oncol 27:252–257CrossRef Ryu M, Shimamura Y, Kinoshita T et al (1997) Therapeutic results of resection, transcatheter arterial embolization and percutaneous transhepatic ethanol injection in 3225 patients with hepatocellular carcinoma: a retrospective multicenter study. Jpn J Clin Oncol 27:252–257CrossRef
28.
go back to reference Zhou XD, Tang ZY, Yu YQ et al (1994) Recurrence after resection of alpha-fetoprotein-positive hepatocellular carcinoma. J Cancer Res Clin Oncol 120:369–373PubMedCrossRef Zhou XD, Tang ZY, Yu YQ et al (1994) Recurrence after resection of alpha-fetoprotein-positive hepatocellular carcinoma. J Cancer Res Clin Oncol 120:369–373PubMedCrossRef
29.
go back to reference Moriyama M, Matsumura H, Aoki H et al (2003) Long-term outcome, with monitoring of platelet counts, in patients with chronic hepatitis C and liver cirrhosis after interferon therapy. Intervirology 46:296–307PubMedCrossRef Moriyama M, Matsumura H, Aoki H et al (2003) Long-term outcome, with monitoring of platelet counts, in patients with chronic hepatitis C and liver cirrhosis after interferon therapy. Intervirology 46:296–307PubMedCrossRef
30.
go back to reference Imai Y, Kawata S, Tamura S et al (1998) Relation of interferon therapy and hepatocellular carcinonma in patients with chronic hepatitis C. Osaka hepatocellular carcinoma prevention study group. Ann Intern Med 129:94–99PubMed Imai Y, Kawata S, Tamura S et al (1998) Relation of interferon therapy and hepatocellular carcinonma in patients with chronic hepatitis C. Osaka hepatocellular carcinoma prevention study group. Ann Intern Med 129:94–99PubMed
31.
go back to reference Takano S, Yokosuka O, Imazeki F et al (1995) Incidence of hepatocellular carcinoma in chronic hepatitis B and C: a prospective study of 251 patients. Hepatology 21:650–655PubMedCrossRef Takano S, Yokosuka O, Imazeki F et al (1995) Incidence of hepatocellular carcinoma in chronic hepatitis B and C: a prospective study of 251 patients. Hepatology 21:650–655PubMedCrossRef
32.
go back to reference Yoshida H, Shiratori Y, Moriyama M et al (1999) Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan IHIT Study Group. Ann Intern Med 131:174–181PubMed Yoshida H, Shiratori Y, Moriyama M et al (1999) Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and noncirrhotic patients with chronic hepatitis C in Japan IHIT Study Group. Ann Intern Med 131:174–181PubMed
33.
go back to reference Poynard T, Bedossa P, Opolon P et al (1997) Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINVIR and DOSVIRC groups. Lancet 349:825–832PubMedCrossRef Poynard T, Bedossa P, Opolon P et al (1997) Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINVIR and DOSVIRC groups. Lancet 349:825–832PubMedCrossRef
34.
go back to reference Shibata M, Morizane T, Uchida T et al (1998) Irregular regeneration of hepatocytes and risk of hepatocellular carcinoma in chronic hepatitis and cirrhosis with hepatitis-C-virus infection. Lancet 351:1773–1777PubMedCrossRef Shibata M, Morizane T, Uchida T et al (1998) Irregular regeneration of hepatocytes and risk of hepatocellular carcinoma in chronic hepatitis and cirrhosis with hepatitis-C-virus infection. Lancet 351:1773–1777PubMedCrossRef
35.
go back to reference Tarao K, Ohkawa S, Shimizu A et al (1994) Significance of hepatocellular proliferation in the development of hepatocellular carcinoma from anti-hepatitis C virus-positive cirrhotic patients. Cancer 73:1149–1154PubMedCrossRef Tarao K, Ohkawa S, Shimizu A et al (1994) Significance of hepatocellular proliferation in the development of hepatocellular carcinoma from anti-hepatitis C virus-positive cirrhotic patients. Cancer 73:1149–1154PubMedCrossRef
36.
go back to reference Schmidt KG, Rasmussen JW, Bekker C et al (1985) Kinetics and in vivo distribution of 111-in labeled autologous platelets in chronic hepatic disease: mechanisms of thrombocytopenia. Scand J Haematol 34:39–46PubMedCrossRef Schmidt KG, Rasmussen JW, Bekker C et al (1985) Kinetics and in vivo distribution of 111-in labeled autologous platelets in chronic hepatic disease: mechanisms of thrombocytopenia. Scand J Haematol 34:39–46PubMedCrossRef
37.
go back to reference Peck-Radosavljevic M, Zacher J, Meng YG et al (1997) Is inadequate thrombopoietin production a major cause of thrombocytopenia in cirrhosis of the liver? J Hepatol 27:127–131PubMedCrossRef Peck-Radosavljevic M, Zacher J, Meng YG et al (1997) Is inadequate thrombopoietin production a major cause of thrombocytopenia in cirrhosis of the liver? J Hepatol 27:127–131PubMedCrossRef
38.
go back to reference Kawasaki T, Takeshita A, Souda K et al (1999) Serum thrombopoietin levels in patients with chronic hepatitis and liver cirrhosis. Am J Gastroenterol 94:1918–1922PubMedCrossRef Kawasaki T, Takeshita A, Souda K et al (1999) Serum thrombopoietin levels in patients with chronic hepatitis and liver cirrhosis. Am J Gastroenterol 94:1918–1922PubMedCrossRef
39.
go back to reference Grober D, Giuliani D, Leevy CM et al (1984) Platelet associated IgG in hepatitis and cirrhosis. J Clin Immunol 4:109–113 Grober D, Giuliani D, Leevy CM et al (1984) Platelet associated IgG in hepatitis and cirrhosis. J Clin Immunol 4:109–113
40.
go back to reference Nagamine T, Ohtuka T, Takehara K et al (1996) Thrombocytopenia associated with hepatitis C viral infection. J Hepatol 24:135–140PubMedCrossRef Nagamine T, Ohtuka T, Takehara K et al (1996) Thrombocytopenia associated with hepatitis C viral infection. J Hepatol 24:135–140PubMedCrossRef
41.
go back to reference Lu SN, Wang JH, Liu SL et al (2006) Thrombocytopenia as surrogate for cirrhosis and a marker for the identification of patients at high risk for hepatocellular carcinoma. Cancer 107:2212–2222PubMedCrossRef Lu SN, Wang JH, Liu SL et al (2006) Thrombocytopenia as surrogate for cirrhosis and a marker for the identification of patients at high risk for hepatocellular carcinoma. Cancer 107:2212–2222PubMedCrossRef
42.
go back to reference Kubo S, Tanaka H, Shuto T et al (2004) Correlation between low platelet count and multicentricity of hepatocellular carcinoma in patients with chronic hepatitis C. Hepatol Res 4:221–225CrossRef Kubo S, Tanaka H, Shuto T et al (2004) Correlation between low platelet count and multicentricity of hepatocellular carcinoma in patients with chronic hepatitis C. Hepatol Res 4:221–225CrossRef
43.
go back to reference Lok AS, Seeff LB, Morgan TR et al (2009) Incidence of hepatocellular carcinoma and associated risk factors in hepatitis-C-related advanced liver disease. Gastroenterology 136:138–148PubMedCrossRef Lok AS, Seeff LB, Morgan TR et al (2009) Incidence of hepatocellular carcinoma and associated risk factors in hepatitis-C-related advanced liver disease. Gastroenterology 136:138–148PubMedCrossRef
44.
go back to reference Kobayashi M, Ikeda K, Kawamura Y et al (2009) High serum des-gamma-carboxy prothrombin level predicts poor prognosis after radiofrequency ablation of hepatocellular carcinoma. Cancer 115:571–580PubMedCrossRef Kobayashi M, Ikeda K, Kawamura Y et al (2009) High serum des-gamma-carboxy prothrombin level predicts poor prognosis after radiofrequency ablation of hepatocellular carcinoma. Cancer 115:571–580PubMedCrossRef
45.
go back to reference Minagawa M, Makuuchi M, Takayama T et al (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238:703–710PubMedCrossRef Minagawa M, Makuuchi M, Takayama T et al (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238:703–710PubMedCrossRef
Metadata
Title
Clinicopathological Features of Recurrence in Patients After 10-year Disease-free Survival Following Curative Hepatic Resection of Hepatocellular Carcinoma
Authors
Masaki Kaibori
Shoji Kubo
Hiroaki Nagano
Michihiro Hayashi
Seiji Haji
Takuya Nakai
Morihiko Ishizaki
Kosuke Matsui
Takahiro Uenishi
Shigekazu Takemura
Hiroshi Wada
Shigeru Marubashi
Koji Komeda
Fumitoshi Hirokawa
Yasuyuki Nakata
Kazuhisa Uchiyama
A-Hon Kwon
Publication date
01-04-2013
Publisher
Springer-Verlag
Published in
World Journal of Surgery / Issue 4/2013
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-013-1902-3

Other articles of this Issue 4/2013

World Journal of Surgery 4/2013 Go to the issue