Skip to main content

Advertisement

SpringerLink
Log in

Treatment and outcomes of recurrent hepatocellular carcinomas

  • ORIGINAL ARTICLE
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

Surgery is one of the best options for curative treatment of hepatocellular carcinomas (HCC). Recurrences are nevertheless common (45–75%). This study aimed to compare overall survival (OS) of patients with recurrent HCC after primary resection to OS of patients without recurrence.

Methods

A retrospective review of all HCC patients operated between 1993 and 2015 was performed. Median and 5-year OS were calculated.

Results

This study included 147 HCC patients. Sixty-seven patients presented a recurrence (46%). Patients with recurrence had a worse prognosis than those without recurrence (median OS 63 vs. 82 months, 5-year OS 47 vs. 54%, p = 0.036). First-line performed treatments were radiofrequency ablation (18, RFA), chemo-embolization (16, TACE), repeat hepatectomy (10), systemic chemotherapy (4), radio-embolization (1), and alcoholization (1). Palliative care was performed in 17 patients. Median OS of patients treated by RFA, TACE, or repeat hepatectomy were similar (77, 71, and 84 months, p = 0.735). Patients treated with chemotherapy/palliative care had lower median OS compared to interventional treatments (20 vs. 77 months, p < 0.0001).

Conclusions

Recurrence after surgical HCC resection is frequent and negatively impacts OS. Interventional treatments of recurrences offered improved outcomes compared to medical care. In selected patients, RFA, TACE, and repeat hepatectomy allowed similar OS as non-recurrent cases.

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

Similar content being viewed by others

References

  1. El-Serag HB (2011) Hepatocellular carcinoma. N Engl J Med 365:1118–1127

    Article  CAS  PubMed  Google Scholar 

  2. Lafaro K, Grandhi MS, Herman JM, Pawlik TM (2016) The importance of surgical margins in primary malignancies of the liver. J Surg Oncol 113:296–303

    Article  PubMed  Google Scholar 

  3. Sangiovanni A, Colombo M (2016) Treatment of hepatocellular carcinoma: beyond international guidelines. Liver Int 36(Suppl 1):124–129

    Article  PubMed  Google Scholar 

  4. Liu H, Wang Z-G, Fu S-Y, Li A-J, Pan Z-Y, Zhou W-P et al (2016) Randomized clinical trial of chemoembolization plus radiofrequency ablation versus partial hepatectomy for hepatocellular carcinoma within the Milan criteria. Br J Surg 103:348–356

    Article  CAS  PubMed  Google Scholar 

  5. Meniconi RL, Komatsu S, Perdigao F, Boëlle P-Y, Soubrane O, Scatton O (2015) Recurrent hepatocellular carcinoma: a Western strategy that emphasizes the impact of pathologic profile of the first resection. Surgery 157:454–462

    Article  PubMed  Google Scholar 

  6. An HJ, Shin WY, Lee K-Y, Ahn S-I (2015) A comparison of the risk factors of intrahepatic recurrence, early recurrence, and multiple recurrences after resection for single nodular hepatocellular carcinoma. Korean J Hepato-Biliary-Pancreat Surg 19:89–97

    Article  Google Scholar 

  7. Hwang S, Lee Y-J, Kim K-H, Ahn C-S, Moon D-B, Ha T-Y et al (2015) The impact of tumor size on long-term survival outcomes after resection of solitary hepatocellular carcinoma: single-institution experience with 2558 patients. J Gastrointest Surg 19:1281–1290

    Article  PubMed  Google Scholar 

  8. Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S (2015) Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg 261:947–955

    Article  PubMed  Google Scholar 

  9. Wang D-Y, Liu L, Qi X-S, Su C-P, Chen X, Liu X et al (2015) Hepatic re-resection versus transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma after initial resection: a systematic review and meta-analysis. Asian Pac J Cancer Prev 16:5573–5578

    Article  PubMed  Google Scholar 

  10. Yamashita Y-I, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T et al (2015) Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: repeat hepatectomy versus salvage living donor liver transplantation. Liver Transplant 21:961–968

    Article  Google Scholar 

  11. Lacaze L, Scotté M (2015) Surgical treatment of intra hepatic recurrence of hepatocellular carcinoma. World J Hepatol 7:1755–1760

    Article  PubMed  PubMed Central  Google Scholar 

  12. Song KD, Lim HK, Rhim H, Lee MW, Kim Y-S, Lee WJ et al (2015) Repeated hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma after hepatic resection: a propensity score matching study. Radiology 275:599–608

    Article  PubMed  Google Scholar 

  13. Fukuhara T, Aikata H, Hyogo H, Honda Y, Morio K, Morio R et al (2015) Efficacy of radiofrequency ablation for initial recurrent hepatocellular carcinoma after curative treatment: comparison with primary cases. Eur J Radiol 84:1540–1545

    Article  PubMed  Google Scholar 

  14. Chen X, Chen Y, Li Q, Ma D, Shen B, Peng C (2015) Radiofrequency ablation versus surgical resection for intrahepatic hepatocellular carcinoma recurrence: a meta-analysis. J Surg Res 195:166–174

    Article  PubMed  Google Scholar 

  15. Mazzaferro V, Bhoori S, Sposito C, Bongini M, Langer M, Miceli R et al (2011) Milan criteria in liver transplantation for hepatocellular carcinoma: an evidence-based analysis of 15 years of experience. Liver Transplant 17(Suppl 2):S44–S57

    Article  Google Scholar 

  16. Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  17. Slankamenac K, Nederlof N, Pessaux P, de Jonge J, Wijnhoven BPL, Breitenstein S, et al (2014) The comprehensive complication index: a novel and more sensitive endpoint for assessing outcome and reducing sample size in randomized controlled trials. Ann Surg 260:757-762-763

  18. Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET et al (1982) Toxicity and response criteria of the eastern cooperative oncology group. Am J Clin Oncol 5:649–655

    Article  CAS  PubMed  Google Scholar 

  19. Zhang X, Li C, Wen T, Yan L, Li B, Yang J et al (2015) Appropriate treatment strategies for intrahepatic recurrence after curative resection of hepatocellular carcinoma initially within the Milan criteria: according to the recurrence pattern. Eur J Gastroenterol Hepatol 27:933–940

    Article  PubMed  Google Scholar 

  20. Shah SA, Cleary SP, Wei AC, Yang I, Taylor BR, Hemming AW et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339

    Article  PubMed  Google Scholar 

  21. Hou Y-F, Li B, Wei Y-G, Yang J-Y, Wen T-F, Xu M-Q et al (2015) Second hepatectomy improves survival in patients with microvascular invasive hepatocellular carcinoma meeting the Milan criteria. Medicine (Baltimore) 94:e2070

    Article  Google Scholar 

  22. Thomasset SC, Dennison AR, Garcea G (2015) Ablation for recurrent hepatocellular carcinoma: a systematic review of clinical efficacy and prognostic factors. World J Surg 39:1150–1160

    Article  CAS  PubMed  Google Scholar 

  23. Zhang C, Zhang J, Li X, Li L, Li X, Zhou X (2015) Is radiofrequency ablation equal to surgical re-resection for recurrent hepatocellular carcinoma meeting the Milan criteria? A meta-analysis. J BUON 20:223–230

    PubMed  Google Scholar 

  24. Jin Y-J, Lee J-W, Lee OH, Chung HJ, Kim YS, Lee JI et al (2014) Transarterial chemoembolization versus surgery/radiofrequency ablation for recurrent hepatocellular carcinoma with or without microvascular invasion. J Gastroenterol Hepatol 29:1056–1064

    Article  PubMed  Google Scholar 

  25. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S et al (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207

    Article  PubMed  Google Scholar 

  26. Shah SA, Greig PD, Gallinger S, Cattral MS, Dixon E, Kim RD et al (2006) Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg 202:275–283

    Article  PubMed  Google Scholar 

  27. Raza A, Sood GK (2014) Hepatocellular carcinoma review: current treatment, and evidence-based medicine. World J Gastroenterol 20:4115–4127

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ali MA, Li W-F, Wang J-H, Lin C-C, Chen Y-J, Lin T-L et al (2016) Impact of pathological features of primary hepatocellular carcinoma on the outcomes of intrahepatic recurrence management: single center experience from southern Taiwan. HPB 18:851–860

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wan X, Zhai X, Yan Z, Yang P, Li J, Wu D et al (2016) Retrospective analysis of transarterial chemoembolization and sorafenib in Chinese patients with unresectable and recurrent hepatocellular carcinoma. Oncotarget 7:83806–83816

    PubMed  PubMed Central  Google Scholar 

  30. Chen R, Gan Y, Ge N, Chen Y, Wang Y, Zhang B et al (2016) Transarterial chemoembolization versus radiofrequency ablation for recurrent hepatocellular carcinoma after resection within Barcelona clinic liver cancer stage 0/a: a retrospective comparative study. J Vasc Interv Radiol 27:1829–1836

    Article  PubMed  Google Scholar 

  31. Zhang J, Zhou Z-G, Huang Z-X, Yang K-L, Chen J-C, Chen J-B et al (2016) Prospective, single-center cohort study analyzing the efficacy of complete laparoscopic resection on recurrent hepatocellular carcinoma. Chin J Cancer 35:25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zou Q, Li J, Wu D, Yan Z, Wan X, Wang K et al (2016) Nomograms for pre-operative and post-operative prediction of long-term survival of patients who underwent repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg Oncol 23:2618–2626

    Article  PubMed  Google Scholar 

  33. Koh PS, Chan ACY, Cheung TT, Chok KSH, Dai WC, Poon RTP et al (2016) Efficacy of radiofrequency ablation compared with transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma: a comparative survival analysis. HPB 18:72–78

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yong C-C, Tsai M-C, Lin C-C, Wang C-C, Lu S-N, Hung C-H et al (2016) Comparison of salvage living donor liver transplantation and local regional therapy for recurrent hepatocellular carcinoma. World J Surg 40:2472–2480

    Article  PubMed  Google Scholar 

  35. Zu Q-Q, Liu S, Zhou C-G, Yang Z-Q, Xia J-G, Zhao L-B et al (2015) Chemoembolization of recurrent hepatoma after curative resection: prognostic factors. AJR Am J Roentgenol 204:1322–1328

    Article  PubMed  Google Scholar 

  36. Wang K, Liu G, Li J, Yan Z, Xia Y, Wan X et al (2015) Early intrahepatic recurrence of hepatocellular carcinoma after hepatectomy treated with re-hepatectomy, ablation or chemoembolization: a prospective cohort study. Eur J Surg Oncol 41:236–242

    Article  CAS  PubMed  Google Scholar 

  37. Mise Y, Hasegawa K, Shindoh J, Ishizawa T, Aoki T, Sakamoto Y et al (2015) The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 262:347–357

    Article  PubMed  Google Scholar 

  38. Yamashita Y-I, Imai D, Bekki Y, Takeishi K, Tsujita E, Ikegami T et al (2014) Surgical outcomes of anatomical resection for solitary recurrent hepatocellular carcinoma. Anticancer Res 34:4421–4426

    PubMed  Google Scholar 

  39. Cheng Y-C, Chen T-W, Fan H-L, Yu C-Y, Chang H-C, Hsieh C-B (2014) Transarterial chemoembolization for intrahepatic multiple recurrent HCC after liver resection or transplantation. Ann Transplant 19:309–301

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Visceral Surgery, University Hospital CHUV, Rue du Bugnon 46, 1011, Lausanne, Switzerland

    Gaëtan-Romain Joliat, Pierre Allemann, Ismail Labgaa, Nicolas Demartines & Nermin Halkic

Authors
  1. Gaëtan-Romain Joliat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierre Allemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ismail Labgaa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Demartines
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nermin Halkic
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GRJ: study conception and design, acquisition of data, analysis and interpretation of data, drafting of the manuscript, acceptance of the final version. PA: acquisition of data, analysis and interpretation of data, critical revision of the manuscript, acceptance of the final version. IL: analysis and interpretation of data, critical revision of the manuscript, acceptance of the final version. ND: analysis and interpretation of data, critical revision of the manuscript, acceptance of the final version. NH: study conception and design, analysis and interpretation of data, critical revision of the manuscript, acceptance of the final version.

Corresponding author

Correspondence to Nicolas Demartines.

Ethics declarations

This retrospective study based on chart review was in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study formal consent is not required.

Conflict of interest

The authors declare that they have no conflict of interest.

Source of funding

This study received no particular funding.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Joliat, GR., Allemann, P., Labgaa, I. et al. Treatment and outcomes of recurrent hepatocellular carcinomas. Langenbecks Arch Surg 402, 737–744 (2017). https://doi.org/10.1007/s00423-017-1582-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-017-1582-9

Keywords

Search

Navigation