Skip to main content

Advertisement

SpringerLink
Log in

Nomogram predicting long-term survival after the diagnosis of intrahepatic recurrence of hepatocellular carcinoma following an initial liver resection

  • Original Article
  • Published:
International Journal of Clinical Oncology Aims and scope Submit manuscript

A Letter to the Editor to this article was published on 28 April 2017

Abstract

Background

The aim of this study was to construct and validate a nomogram for predicting survival after the intrahepatic recurrence of hepatocellular carcinoma (HCC) following an initial hepatectomy.

Methods

A primary cohort of 268 patients who underwent curative hepatectomy for HCC at Shinshu University Hospital between 1990 and 2010 was retrospectively studied. A nomogram was constructed based on independent prognostic factors for overall survival after recurrence. The predictive performance was evaluated using the concordance index (c-index) and a calibration curve. The nomogram was then externally validated in a cohort of patients from Tokyo University Hospital (n = 296).

Results

In multivariate analysis, the following 5 variables were identified as independent predictors of overall survival and incorporated into the nomogram—Japan Integrated Stage score at initial liver resection, platelet count at initial liver resection, time until intrahepatic recurrence, vascular invasion at recurrence, and type of treatment used for intrahepatic recurrence. The nomogram had a c-index of 0.75 (95% confidence interval 0.60–0.85) for the Shinshu cohort and 0.71 (0.57–0.81) for the Tokyo cohort. The predicted 3- and 5-year survival probabilities corresponded well with the actual outcomes.

Conclusions

The established nomogram might be useful for estimating survival after the intrahepatic recurrence of HCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–2576

    Article  CAS  PubMed  Google Scholar 

  2. Ferlay J, Soerjomataram I, Dikshit R et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–386

    Article  CAS  PubMed  Google Scholar 

  3. Forner A, Llovet JM, Bruix J (2012) Hepatocellular carcinoma. Lancet 379:1245–1255

    Article  PubMed  Google Scholar 

  4. Belghiti J, Panis Y, Farges O et al (1991) Intrahepatic recurrence after resection of hepatocellular carcinoma complicating cirrhosis. Ann Surg 214:114–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  6. Adachi E, Maeda T, Matsumata T et al (1995) Risk factors for intrahepatic recurrence in human small hepatocellular carcinoma. Gastroenterology 108:768–775

    Article  CAS  PubMed  Google Scholar 

  7. Llovet JM, Bru C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19:329–338

    Article  CAS  PubMed  Google Scholar 

  8. 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  CAS  PubMed  PubMed Central  Google Scholar 

  9. Majno PE, Sarasin FP, Mentha G et al (2000) Primary liver resection and salvage transplantation or primary liver transplantation in patients with single, small hepatocellular carcinoma and preserved liver function: an outcome-oriented decision analysis. Hepatology 31:899–906

    Article  CAS  PubMed  Google Scholar 

  10. 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  PubMed Central  Google Scholar 

  11. Kakazu T, Makuuchi M, Kawasaki S et al (1993) Repeat hepatic resection for recurrent hepatocellular carcinoma. Hepatogastroenterology 40:337–341

    CAS  PubMed  Google Scholar 

  12. Hu RH, Lee PH, Yu SC et al (1996) Surgical resection for recurrent hepatocellular carcinoma: prognosis and analysis of risk factors. Surgery 120:23–29

    Article  CAS  PubMed  Google Scholar 

  13. Nagasue N, Kohno H, Hayashi T et al (1996) Repeat hepatectomy for recurrent hepatocellular carcinoma. Br J Surg 83:127–131

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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  PubMed Central  Google Scholar 

  16. Itamoto T, Nakahara H, Amano H et al (2007) Repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 141:589–597

    Article  PubMed  Google Scholar 

  17. Kubo S, Takemura S, Uenishi T et al (2008) Second hepatic resection for recurrent hepatocellular carcinoma in patients with chronic hepatitis C. World J Surg 32:632–638

    Article  PubMed  Google Scholar 

  18. Wu CC, Cheng SB, Yeh DC et al (2009) Second and third hepatectomies for recurrent hepatocellular carcinoma are justified. Br J Surg 96:1049–1057

    Article  PubMed  Google Scholar 

  19. Roayaie S, Bassi D, Tarchi P et al (2011) Second hepatic resection for recurrent hepatocellular cancer: a Western experience. J Hepatol 55:346–350

    Article  PubMed  Google Scholar 

  20. Kobayashi A, Kawasaki S, Miyagawa S et al (2006) Results of 404 hepatic resections including 80 repeat hepatectomies for hepatocellular carcinoma. Hepatogastroenterology 53:736–741

    PubMed  Google Scholar 

  21. Choi D, Lim HK, Rhim H et al (2007) Percutaneous radiofrequency ablation for recurrent hepatocellular carcinoma after hepatectomy: long-term results and prognostic factors. Ann Surg Oncol 14:2319–2329

    Article  PubMed  Google Scholar 

  22. Okuwaki Y, Nakazawa T, Kokubu S et al (2009) Repeat radiofrequency ablation provides survival benefit in patients with intrahepatic distant recurrence of hepatocellular carcinoma. Am J Gastroenterol 104:2747–2753

    Article  PubMed  Google Scholar 

  23. Okazaki M, Yamasaki S, Ono H et al (1993) Chemoembolotherapy for recurrent hepatocellular carcinoma in the residual liver after hepatectomy. Hepatogastroenterology 40:320–323

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shim JH, Kim KM, Lee YJ et al (2010) Complete necrosis after transarterial chemoembolization could predict prolonged survival in patients with recurrent intrahepatic hepatocellular carcinoma after curative resection. Ann Surg Oncol 17:869–877

    Article  PubMed  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. 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 

  28. Taura K, Ikai I, Hatano E et al (2006) Implication of frequent local ablation therapy for intrahepatic recurrence in prolonged survival of patients with hepatocellular carcinoma undergoing hepatic resection: an analysis of 610 patients over 16 years old. Ann Surg 244:265–273

    Article  PubMed  PubMed Central  Google Scholar 

  29. Shah SA, Cleary SP, Wei AC et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339

    Article  PubMed  Google Scholar 

  30. Shimada K, Sakamoto Y, Esaki M et al (2007) Analysis of prognostic factors affecting survival after initial recurrence and treatment efficacy for recurrence in patients undergoing potentially curative hepatectomy for hepatocellular carcinoma. Ann Surg Oncol 14:2337–2347

    Article  PubMed  Google Scholar 

  31. Choi GH, Kim DH, Kang CM et al (2008) Prognostic factors and optimal treatment strategy for intrahepatic nodular recurrence after curative resection of hepatocellular carcinoma. Ann Surg Oncol 15:618–629

    Article  PubMed  Google Scholar 

  32. Kawano Y, Sasaki A, Kai S et al (2009) Prognosis of patients with intrahepatic recurrence after hepatic resection for hepatocellular carcinoma: a retrospective study. Eur J Surg Oncol 35:174–179

    Article  CAS  PubMed  Google Scholar 

  33. Kishi Y, Saiura A, Yamamoto J et al (2011) Repeat treatment for recurrent hepatocellular carcinoma: is it validated? Langenbecks Arch Surg 396:1093–1100

    Article  PubMed  Google Scholar 

  34. Kattan MW, Potters L, Blasko JC et al (2001) Pretreatment nomogram for predicting freedom from recurrence after permanent prostate brachytherapy in prostate cancer. Urology 58:393–399

    Article  CAS  PubMed  Google Scholar 

  35. Bochner BH, Kattan MW, Vora KC (2006) Postoperative nomogram predicting risk of recurrence after radical cystectomy for bladder cancer. J Clin Oncol 24:3967–3972

    Article  PubMed  Google Scholar 

  36. Ferrone CR, Kattan MW, Tomlinson JS et al (2005) Validation of a postresection pancreatic adenocarcinoma nomogram for disease-specific survival. J Clin Oncol 23:7529–7535

    Article  PubMed  PubMed Central  Google Scholar 

  37. Han DS, Suh YS, Kong SH et al (2012) Nomogram predicting long-term survival after d2 gastrectomy for gastric cancer. J Clin Oncol 30:3834–3840

    Article  PubMed  Google Scholar 

  38. Rudloff U, Jacks LM, Goldberg JI et al (2010) Nomogram for predicting the risk of local recurrence after breast-conserving surgery for ductal carcinoma in situ. J Clin Oncol 28:3762–3769

    Article  PubMed  Google Scholar 

  39. Kattan MW, Gonen M, Jarnagin WR et al (2008) A nomogram for predicting disease-specific survival after hepatic resection for metastatic colorectal cancer. Ann Surg 247:282–287

    Article  PubMed  Google Scholar 

  40. Cho CS, Gonen M, Shia J et al (2008) A novel prognostic nomogram is more accurate than conventional staging systems for predicting survival after resection of hepatocellular carcinoma. J Am Coll Surg 206:281–291

    Article  PubMed  Google Scholar 

  41. Shim JH, Jun MJ, Han S et al (2015) Prognostic nomograms for prediction of recurrence and survival after curative liver resection for hepatocellular carcinoma. Ann Surg 261:939–946

    Article  PubMed  Google Scholar 

  42. Makuuchi M, Kosuge T, Takayama T et al (1993) Surgery for small liver cancers. Semin Surg Oncol 9:298–304

    Article  CAS  PubMed  Google Scholar 

  43. Miyagawa S, Makuuchi M, Kawasaki S et al (1995) Criteria for safe hepatic resection. Am J Surg 169:589–594

    Article  CAS  PubMed  Google Scholar 

  44. Liebman HA, Furie BC, Tong MJ et al (1984) Des-gamma-carboxy (abnormal) prothrombin as a serum marker of primary hepatocellular carcinoma. N Engl J Med 310:1427–1431

    Article  CAS  PubMed  Google Scholar 

  45. Lok AS, Sterling RK, Everhart JE et al (2010) Des-gamma-carboxy prothrombin and alpha-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology 138:493–502

    Article  CAS  PubMed  Google Scholar 

  46. Pencina MJ, D’Agostino RB (2004) Overall C as a measure of discrimination in survival analysis: model specific population value and confidence interval estimation. Stat Med 23:2109–2123

    Article  PubMed  Google Scholar 

  47. Kudo M, Chung H, Haji S et al (2004) Validation of a new prognostic staging system for hepatocellular carcinoma: the JIS score compared with the CLIP score. Hepatology 40:1396–1405

    Article  PubMed  Google Scholar 

  48. Balachandran VP, Gonen M, Smith JJ et al (2015) Nomograms in oncology: more than meets the eye. Lancet Oncol 16:e173–180

    Article  PubMed  PubMed Central  Google Scholar 

  49. The Liver Cancer Study Group of Japan (2010) The general rules for clinical and pathological study of primary liver cancer, 3rd edn. Kanehara & Co., Ltd, Tokyo

    Google Scholar 

  50. Pugh RN, Murray-Lyon IM, Dawson JL et al (1973) Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 60:646–649

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Shinshu University School of Medicine, 3-1-1 Asahi, Matsumoto, 390-8621, Japan

    Tsuyoshi Notake, Akira Kobayashi, Akira Shimizu, Takahide Yokoyama & Shin-ichi Miyagawa

  2. Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery, Graduate School of Medicine, University of Tokyo, Tokyo, Japan

    Hiroji Shinkawa, Kiyoshi Hasegawa & Norihiro Kokudo

  3. Department of Biostatistics, School of Public Health, University of Tokyo, Tokyo, Japan

    Takuya Kawahara & Yutaka Matsuyama

  4. Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery, Japanese Red Cross Medical Center, Tokyo, Japan

    Masatoshi Makuuchi

Authors
  1. Tsuyoshi Notake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akira Kobayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroji Shinkawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takuya Kawahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Akira Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takahide Yokoyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kiyoshi Hasegawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Norihiro Kokudo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yutaka Matsuyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Masatoshi Makuuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Shin-ichi Miyagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Akira Kobayashi.

Ethics declarations

Conflicts of interest

The authors have declared that no conflicts of interest exist.

Financial support

none.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Notake, T., Kobayashi, A., Shinkawa, H. et al. Nomogram predicting long-term survival after the diagnosis of intrahepatic recurrence of hepatocellular carcinoma following an initial liver resection. Int J Clin Oncol 22, 715–725 (2017). https://doi.org/10.1007/s10147-017-1114-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10147-017-1114-1

Keywords

Search

Navigation