Skip to main content
SpringerLink
Log in

Recurrence Patterns After Anatomic or Parenchyma-Sparing Liver Resection for Hepatocarcinoma in a Western Population of Cirrhotic Patients

  • Hepatobiliary Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

The optimal surgical strategy to lessen the risk of hepatocarcinoma (HCC) recurrence is debated. This study aimed to investigate the role of anatomic resection (AR) and parenchyma-sparing resection (PSR) in HCC recurrence patterns.

Methods

The study analyzed 384 cirrhotic patients with a first diagnosis of HCC. Of these patients, 142 underwent AR, and 242 underwent PSR. The two groups were unbalanced at the univariate analysis. To minimize this bias, a 1:1 propensity score-matching analysis (PSA) was used. Disease-free survival (DFS) curves were analyzed by the Kaplan-Maier method.

Results

The PSA allowed pairing of 200 patients (100 for AR and 100 for PSR). In this study, 59 patients (62.8%) had recurrence after AR compared with 58 patients (63.7%) after PSR (p = 0.891). The rates of local recurrence were respectively 15.3% and 15.5% (p = 0.968). When microvascular invasion was considered, the median DFS was 10.7 months for AR and 9.4 months for PSR (p = 0.607). In comparisons of AR and PSR, DFS did not differ significantly between subgroups with high histologic grading (p = 0.520), multiple nodules (p = 0.307), and Child–Pugh B (p = 0.679).

Conclusion

Excision of the anatomic segment did not seem to reduce the rate of relapse or recurrence patterns significantly, even in high-risk subgroups.

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

Similar content being viewed by others

References

  1. Nagasue N, Uchida M, Makino Y, et al. Incidence and factors associated with intrahepatic recurrence following resection of hepatocellular carcinoma. Gastroenterology. 1993;105:488–94.

    Article  CAS  Google Scholar 

  2. Ercolani G, Grazi GL, Ravaioli M, et al. Liver resection for hepatocellular carcinoma on cirrhosis: univariate and multivariate analysis of risk factors for intrahepatic recurrence. Ann Surg. 2003;237:536–43.

    PubMed  PubMed Central  Google Scholar 

  3. Chen MF, Hwang TL, Jeng LB, Wang CS, Jan YY, Chen SC. Postoperative recurrence of hepatocellular carcinoma: two hundred five consecutive patients who underwent hepatic resection in 15 years. Arch Surg. 1994;129:738–42.

    Article  CAS  Google Scholar 

  4. Sakon M, Nagano H, Nakamori S, et al. Intrahepatic recurrences of hepatocellular carcinoma after hepatectomy: analysis based on tumor hemodynamics. Arch Surg. 2002;137:94–9.

    Article  Google Scholar 

  5. Yamamoto M, Takasaki K, Ohtsubo T, Katsuragawa H, Fukuda C, Katagiri S. Effectiveness of systematized hepatectomy with Glisson’s pedicle transection at the hepatic hilus for small nodular hepatocellular carcinoma: retrospective analysis. Surgery. 2001;130:443–8.

    Article  CAS  Google Scholar 

  6. Hasegawa K, Kokudo N, Imamura H, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg. 2005;242:252–9.

    Article  Google Scholar 

  7. Imamura H, Matsuyama Y, Miyagawa Y, et al. Prognostic significance of anatomical resection and des-gamma-carboxy prothrombin in patients with hepatocellular carcinoma. Br J Surg. 1999;86:1032–8.

    Article  CAS  Google Scholar 

  8. Eguchi S, Kanematsu T, Arii S, et al. Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery. 2008;143:469–75.

    Article  Google Scholar 

  9. Kim JM, Kwon CHD, Joh J-W, et al. Nonanatomical resection is comparable with anatomical resection in solitary hepatocellular carcinoma < 5 cm in the right posterior section. Medicine. 2016;95:e5382.

    Article  CAS  Google Scholar 

  10. Li S-Q, Huang T, Shen S-L, et al. Anatomical versus non-anatomical liver resection for hepatocellular carcinoma exceeding Milan criteria. Br J Surg. 2016;104:118–27.

    Article  CAS  Google Scholar 

  11. Kim S, Kim S, Song I, Chun K. Comparison of survival outcomes after anatomical resection and non-anatomical resection in patients with hepatocellular carcinoma. Korean J Hepatobil Pancreat Surg. 2015;19:161.

    Article  CAS  Google Scholar 

  12. Famularo S, Di Sandro S, Giani A, et al. Long-term oncologic results of anatomic vs parenchyma-sparing resection for hepatocellular carcinoma: a propensity score-matching analysis. Eur J Surg Oncol. 2018. https://doi.org/10.1016/j.ejso.2018.05.018.

    Article  PubMed  Google Scholar 

  13. Feo F, Pascale RM. Multifocal hepatocellular carcinoma: intrahepatic metastasis or multicentric carcinogenesis? Ann Transl Med. 2015;3:4.

    PubMed  PubMed Central  Google Scholar 

  14. von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007;4:e296.

    Article  Google Scholar 

  15. Dindo D, Demartines N, Clavien P-A. Classification of surgical complications. Ann Surg. 2004;240:205–13.

    Article  Google Scholar 

  16. Sakamoto M, Hirohashi S, Tsuda H, Shimosato Y, Makuuchi M, Hosoda Y. Multicentric independent development of hepatocellular carcinoma revealed by analysis of hepatitis B virus integration pattern. Am J Surg Pathol. 1989;13:1064–7.

    Article  CAS  Google Scholar 

  17. Morimoto O, Nagano H, Sakon M, et al. Diagnosis of intrahepatic metastasis and multicentric carcinogenesis by microsatellite loss of heterozygosity in patients with multiple and recurrent hepatocellular carcinomas. J Hepatol. 2003;39:215–21.

    Article  CAS  Google Scholar 

  18. Li Q, Wang J, Juzi JT, et al. Clonality analysis for multicentric origin and intrahepatic metastasis in recurrent and primary hepatocellular carcinoma. J Gastrointest Surg. 2008;12:1540–7.

    Article  Google Scholar 

  19. Yang S-L, Luo Y-Y, Chen M, et al. A systematic review and meta-analysis comparing the prognosis of multicentric occurrence and vs intrahepatic metastasis in patients with recurrent hepatocellular carcinoma after hepatectomy. HPB. 2017;19:835–42.

    Article  Google Scholar 

  20. Zhou L, Rui J-A, Wang S-B, Chen S-G, Qu Q. Early recurrence in large hepatocellular carcinoma after curative hepatic resection: prognostic significance and risk factors. Hepatogastroenterology. 2014;61:2035–41.

    PubMed  Google Scholar 

  21. Hung H-H, Lei H-J, Chau G-Y, et al. Milan criteria, multi-nodularity, and microvascular invasion predict the recurrence patterns of hepatocellular carcinoma after resection. J Gastrointest Surg. 2013;17:702–11.

    Article  Google Scholar 

  22. Hirokawa F, Hayashi M, Asakuma M, Shimizu T, Inoue Y, Uchiyama K. Risk factors and patterns of early recurrence after curative hepatectomy for hepatocellular carcinoma. Surg Oncol. 2016;25:24–9.

    Article  Google Scholar 

  23. Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet. 1985;161:346–50.

    CAS  PubMed  Google Scholar 

  24. Cucchetti A, Qiao G-L, Cescon M, et al. Anatomic versus nonanatomic resection in cirrhotic patients with early hepatocellular carcinoma. Surgery. 2014;155:512–21.

    Article  Google Scholar 

  25. Takano S, Oishi H, Kono S, et al. Retrospective analysis of type of hepatic resection for hepatocellular carcinoma. Br J Surg. 2000;87:65–70.

    Article  CAS  Google Scholar 

  26. Marubashi S, Gotoh K, Akita H, et al. Anatomical versus non-anatomical resection for hepatocellular carcinoma. Br J Surg. 2015;102:776–84.

    Article  CAS  Google Scholar 

  27. Marubashi S, Gotoh K, Akita H, et al. Analysis of recurrence patterns after anatomical or non-anatomical resection for hepatocellular carcinoma. Ann Surg Oncol. 2015;22:2243–52.

    Article  Google Scholar 

  28. Sakon M, Ogawa H, Fujita M, Nagano H. Hepatic resection for hepatocellular carcinoma based on tumor hemodynamics. Hepatol Res. 2013;43:155–64.

    Article  Google Scholar 

  29. Wang L, Li Y, Xu J, et al. Quantified postsurgical small cell size CTCs and EpCAM circulating tumor stem cells with cytogenetic abnormalities in hepatocellular carcinoma patients determine cancer relapse. Cancer Lett. 2018;412:99–107.

    Article  CAS  Google Scholar 

  30. Yamamoto T, Yagi S, Uryuhara K, Kaihara S, Hosotani R. Clinical factors that affect the outcomes after anatomical versus non-anatomical resection for hepatocellular carcinoma. Surg Today. 2017;47:193–201.

    Article  Google Scholar 

  31. Sasaki K, Shindoh J, Margonis GA, et al. Effect of background liver cirrhosis on outcomes of hepatectomy for hepatocellular carcinoma. JAMA Surg. 2017;152:e165059.

    Article  Google Scholar 

  32. Li S-L, Su M, Peng T, et al. Clinicopathologic characteristics and prognoses for multicentric occurrence and intrahepatic metastasis in synchronous multinodular hepatocellular carcinoma patients. Asian Pac J Cancer Prev. 2013;14:217–23.

    Article  Google Scholar 

  33. Zhang Y, Shi Z-L, Yang X, Yin Z-F. Targeting of circulating hepatocellular carcinoma cells to prevent postoperative recurrence and metastasis. World J Gastroenterol. 2014;20:142–7.

    Article  Google Scholar 

  34. Wang Z, Luo L, Cheng Y, et al. Correlation between postoperative early recurrence of hepatocellular carcinoma and mesenchymal circulating tumor cells in peripheral blood. J Gastrointest Surg. 2017;22:633–9.

    Article  Google Scholar 

  35. Fan ST, Yang ZF, Ho DWY, Ng MNP, Yu WC, Wong J. Prediction of posthepatectomy recurrence of hepatocellular carcinoma by circulating cancer stem cells: a prospective study. Ann Surg. 2011;254:569–76.

    Article  Google Scholar 

  36. Takenaka K, Adachi E, Nishizaki T, et al. Possible multicentric occurrence of hepatocellular carcinoma: a clinicopathological study. Hepatology. 1994;19:889–94.

    Article  CAS  Google Scholar 

  37. Austin PC. An Introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res. 2011;46: 399–424

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Medicine and Surgery, University of Milan-Bicocca, Monza, Italy

    Simone Famularo MD, Alessandro Giani MD, Marta Sandini MD, Fabio Uggeri MD, Fabrizio Romano MD, Luca Gianotti MD, ScD & Luciano De Carlis MD

  2. Department of General Surgery and Transplantation, Grande Ospedale Metropolitano Niguarda, Milan, Italy

    Simone Famularo MD, Stefano Di Sandro MD, Andrea Lauterio MD, Riccardo De Carlis MD, Vincenzo Buscemi MD & Luciano De Carlis MD

  3. Department of Surgery, San Gerardo Hospital, Monza, Italy

    Alessandro Giani MD, Marta Sandini MD, Fabio Uggeri MD, Fabrizio Romano MD & Luca Gianotti MD, ScD

Authors
  1. Simone Famularo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefano Di Sandro MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandro Giani MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea Lauterio MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marta Sandini MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Riccardo De Carlis MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vincenzo Buscemi MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fabio Uggeri MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fabrizio Romano MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Luca Gianotti MD, ScD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Luciano De Carlis MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luca Gianotti MD, ScD.

Ethics declarations

Disclosure

The authors disclose no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 199 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Famularo, S., Di Sandro, S., Giani, A. et al. Recurrence Patterns After Anatomic or Parenchyma-Sparing Liver Resection for Hepatocarcinoma in a Western Population of Cirrhotic Patients. Ann Surg Oncol 25, 3974–3981 (2018). https://doi.org/10.1245/s10434-018-6730-0

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-018-6730-0

Keywords

Search

Navigation