Skip to main content
Log in

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

  • Published:
World Journal of Surgery Aims and scope Submit manuscript

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.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bosch X, Ribes J, Borras J (1999) Epidemiology of primary liver cancer. Semin Liver Dis 19:271–285

    Article  PubMed  CAS  Google Scholar 

  2. Taylor-Robinson SD, Foster GR, Arora S et al (1997) Increase in primary liver cancer in the UK 1979–94. Lancet 350:1142–1143

    Article  PubMed  CAS  Google Scholar 

  3. EI-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340:745–750

    Article  Google Scholar 

  4. 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 89:194–198

    PubMed  CAS  Google Scholar 

  5. Seki T, Wakabayashi M, Nakagawa T et al (1994) Ultrasonically guided percutaneous microwave coagulation therapy for small hepatocellular carcinoma. Cancer 74:817–825

    Article  PubMed  CAS  Google Scholar 

  6. 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 243:321–328

    Article  PubMed  Google Scholar 

  7. Tung-Ping Poon R, Fan ST, Wong J (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24

    Article  PubMed  CAS  Google Scholar 

  8. Nagasue N, Uchida M, Makino Y et al (1993) Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma. Gastroenterology 105:488–494

    Article  PubMed  CAS  Google Scholar 

  9. Shirabe K, Shimada M, Kajiyama K et al (1998) Clinicopathologic features of patients with hepatocellular carcinoma surviving >10 years after hepatic resection. Cancer 83:2312–2316

    Article  PubMed  CAS  Google Scholar 

  10. 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 19:3037–3044

    PubMed  CAS  Google Scholar 

  11. 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 104:1939–1947

    Article  PubMed  Google Scholar 

  12. 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 31:345–352

    Article  PubMed  Google Scholar 

  13. 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

    Google Scholar 

  14. Couinaud C (ed) (1957) Le Foie: Etudes Anatomiques et Chirurgicale. Masson, Paris

    Google Scholar 

  15. Kaibori M, Matsui Y, Hijikawa T et al (2006) Comparison of limited and anatomic hepatic resection for hepatocellular carcinoma with hepatitis C. Surgery 139:385–394

    Article  PubMed  Google Scholar 

  16. Sobin LH, Wittekind C (eds) (1997) TNM classification of malignant tumors, 5th edn. Wiley, New York

    Google Scholar 

  17. 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 27:437–442

    Article  PubMed  Google Scholar 

  18. Yamamoto J, Kosuge T, Takayama T et al (1996) Recurrence of hepatocellular carcinoma after surgery. Br J Surg 83:1219–1222

    Article  PubMed  CAS  Google Scholar 

  19. 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 235:373–382

    Article  PubMed  Google Scholar 

  20. Poon RT, Fan ST, Wong J et al (2000) Risk factors, prevention, and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24

    Article  Google Scholar 

  21. 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 30:414–420

    Article  PubMed  Google Scholar 

  22. 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 229:216–222

    Article  PubMed  CAS  Google Scholar 

  23. Lee PH, Lin WJ, Tsang YM et al (1995) Clinical management of recurrent hepatocellular carcinoma. Ann Surg 222:670–676

    Article  PubMed  CAS  Google Scholar 

  24. Shimada M, Takenaka K, Taguchi K et al (1998) Prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 227:80–85

    Article  PubMed  CAS  Google Scholar 

  25. Kosuge T, Makuuchi M, Takayama T et al (1993) Long-term results after resection of hepatocellular carcinoma: experience of 480 cases. Hepatogastroenterology 40:328–332

    PubMed  CAS  Google Scholar 

  26. Okada S, Shimada K, Yamamoto J et al (1994) Predictive factors for postoperative recurrence of hepatocellular carcinoma. Gastroenterology 106:1618–1624

    PubMed  CAS  Google Scholar 

  27. 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 27:252–257

    Article  Google Scholar 

  28. Zhou XD, Tang ZY, Yu YQ et al (1994) Recurrence after resection of alpha-fetoprotein-positive hepatocellular carcinoma. J Cancer Res Clin Oncol 120:369–373

    Article  PubMed  CAS  Google Scholar 

  29. 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 46:296–307

    Article  PubMed  CAS  Google Scholar 

  30. 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 129:94–99

    PubMed  CAS  Google Scholar 

  31. 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 21:650–655

    Article  PubMed  CAS  Google Scholar 

  32. 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 131:174–181

    PubMed  CAS  Google Scholar 

  33. 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 349:825–832

    Article  PubMed  CAS  Google Scholar 

  34. 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 351:1773–1777

    Article  PubMed  CAS  Google Scholar 

  35. 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 73:1149–1154

    Article  PubMed  CAS  Google Scholar 

  36. 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 34:39–46

    Article  PubMed  CAS  Google Scholar 

  37. 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 27:127–131

    Article  PubMed  CAS  Google Scholar 

  38. Kawasaki T, Takeshita A, Souda K et al (1999) Serum thrombopoietin levels in patients with chronic hepatitis and liver cirrhosis. Am J Gastroenterol 94:1918–1922

    Article  PubMed  CAS  Google Scholar 

  39. Grober D, Giuliani D, Leevy CM et al (1984) Platelet associated IgG in hepatitis and cirrhosis. J Clin Immunol 4:109–113

    Google Scholar 

  40. Nagamine T, Ohtuka T, Takehara K et al (1996) Thrombocytopenia associated with hepatitis C viral infection. J Hepatol 24:135–140

    Article  PubMed  CAS  Google Scholar 

  41. 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 107:2212–2222

    Article  PubMed  Google Scholar 

  42. 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 4:221–225

    Article  Google Scholar 

  43. 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 136:138–148

    Article  PubMed  CAS  Google Scholar 

  44. 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 115:571–580

    Article  PubMed  CAS  Google Scholar 

  45. Minagawa M, Makuuchi M, Takayama T et al (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238:703–710

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masaki Kaibori.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaibori, M., Kubo, S., Nagano, H. et al. Clinicopathological Features of Recurrence in Patients After 10-year Disease-free Survival Following Curative Hepatic Resection of Hepatocellular Carcinoma. World J Surg 37, 820–828 (2013). https://doi.org/10.1007/s00268-013-1902-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-013-1902-3

Keywords

Navigation