Skip to main content

Advertisement

Log in

Impact of intermittent portal clamping on the early recurrence of hepatocellular carcinoma after surgery

  • Original Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the impact of intermittent portal clamping (IPC) during surgery on the early recurrence of hepatocellular carcinoma (HCC).

Methods

The subjects of this retrospective study were 266 patients who underwent curative liver resection for HCC. The patients were grouped as follows: an intermittent portal clamping (IPC) group, n = 78; a continuous portal clamping (CPC) group, n = 128; and a non-portal clamping (NPC) group, n = 60.

Results

The median recurrence-free interval within 2 years of follow-up was significantly shorter in the IPC group (14.2 ± 4.6 months) than in the CPC group (18.0 ± 4.8 months, P = 0.008) or the NPC group (19.04 ± 4.1 months, P = 0.023). Moreover, 2-year recurrence-free survival was much lower in the IPC group than in the CPC group (63.6 vs. 75.8 %, P = 0.025) or the NPC group (63.6 vs. 78.0 %, P = 0.030). However, the 2-year OS rate among the three groups was comparable (72.7 vs. 79.9 %; P = 0.101) and 83.1 %, (P = 0.125). According to univariable analysis, tumor size (>5 cm), tumor number (≥2), tumor grade (low/undifferentiated), TNM stage (III), vascular infiltration, blood transfusion, and IPC were significantly associated with the early postoperative recurrence of HCC. After multivariate analysis, significance of tumor grade (low/undifferentiated) and TNM stage (III) disappeared, whereas tumor size (>5 cm), tumor number (≥2), vascular infiltration, blood transfusion, and IPC remained significant.

Conclusions

IPC is an independent risk factor for the early recurrence of HCC after surgery.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

HCC:

Hepatocellular carcinoma

IPC:

Intermittent portal clamping

CPC:

Continuous portal clamping

NPC:

Non-portal clamping

RFS:

Recurrence-free survival

OS:

Overall survival

CI:

Confidence interval

RR:

Risk ratio

References

  1. Shah SA, Clearly SP, Wei AC, Yang I, Taylor BR, Hemming AW, et al. Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery. 2007;141(3):330–9.

    Article  PubMed  Google Scholar 

  2. Shah SA, Greig PD, Gallinger S, Cattral MS, Dixon E, Kim RD, et al. Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg. 2006;202:275–83.

    Article  PubMed  Google Scholar 

  3. Cha C, Fong Y, Jarnagin WR, Blumgart LH, DeMatteo RP. Predictors and patterns of recurrence after resection of hepatocellular carcinoma. J Am Coll Surg. 2003;197(5):753–8.

    Article  PubMed  Google Scholar 

  4. Belghiti J, Noun R, Malafosse R, Mlofosse R, Jaqot P, Sauvanet A, et al. Continuous versus intermittent portal triad clamping for liver resection. Ann Surg. 1999;229:369–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Nuzzo G, Giuliante F, Giovannini I, Tebala GD, Cosmo G. Hepatic resections in normothermic ischemia. Surgery. 1996;120:852–8.

    Article  CAS  PubMed  Google Scholar 

  6. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, et al. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003;38:200–7.

    Article  PubMed  Google Scholar 

  7. Katz SC, Shia J, Liau KH, Gonen M, Ruo L, Jarnagin WR, et al. Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg. 2009;249:617–23.

    Article  PubMed  Google Scholar 

  8. Mizuquchi T, Kawamoto M, Mequro M, Okita K, Ota S, Ishii M, Nishidate T, Furuhata T, Hirata K. Impact of aging on morbidity and mortality after liver resection: a systematic review and meta-analysis. Surg Today. 2015;45:259–70.

    Article  Google Scholar 

  9. Poon RT, Fan ST, Wong J. Risk factors, prevention, management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg. 2000;232(1):10–24.

    Article  Google Scholar 

  10. Regimbeau JM, Abdalla EK, Vauthey JN, Lauwers GY, Durand F, Nagorney DM, et al. Risk factors for early death due to recurrence after liver resection for hepatocellular carcinoma: results of a multicenter study. J Surg Oncol. 2004;85:36–41.

    Article  PubMed  Google Scholar 

  11. Tandon P, Garcia-Tsao G. Prognostic indicators in hepatocellular carcinoma: a systemic review of 72 studies. Liver Int. 2009;29:502–10.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Nanashima A, Naqayasu T. Development and clinical usefulness of the liver hanging maneuver in various anatomical hepatectomy procedures. Surg Today. 2015;. doi:10.1007/s00595-015-1166-7.

    PubMed  Google Scholar 

  13. Kusano T, Sasaki A, Kai S, Endo Y, Iwaki K, Shibata K, et al. Predictors and prognostic significance of operative complications in patients with hepatocellular carcinoma who underwent hepatic resection. Eur J Surg Oncol. 2009;35:1179–85.

    Article  CAS  PubMed  Google Scholar 

  14. Hanazaki K, Kajikawa S, Shimozawa N, Mihara M, Shimada K, Hiraquri M, et al. Survival and recurrence after hepatic resection of 386 consecutive patients with hepatocellular carcinoma. J Am Coll Surg. 2000;191:381–8.

    Article  CAS  PubMed  Google Scholar 

  15. Bruns H, Kratschmer K, Hins U, Brechtel A, Keller M, Buchler MW, et al. Quality of life after curative liver resection: a single center analysis. World J Gastroenterol. 2010;16:2388–95.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lei Z, Chang L, Fan-di M, Qi-Fei W, Ming-Hui T, Ji-Chao W. Exploration on surgical-related factors influencing HCC patients prognosis. Hepatogastroenterology. 2012;59:1541–3.

    PubMed  Google Scholar 

  17. de Boer MT, Molenaar IQ, Porte RJ. Impact of blood loss on outcome after liver resection. Dig Surg. 2007;24:259–64.

    Article  PubMed  Google Scholar 

  18. Buell JF, Koffron A, Yoshida A, Hanaway M, Lo A, Layman R, et al. Is any method of vascular control superior in hepatic resection of metastatic cancers? Longmire clamping, pringle maveuver, and total vascular isolation. Arch Surg. 2001;136(5):569–75.

    Article  CAS  PubMed  Google Scholar 

  19. Doi K, Horiuchi T, Uchinami M, Tabo T, Kimura N, Yokomachi J. Hepatic ischemia–reperfusion promotes liver metastasis of colon cancer. J Surg Res. 2002;105(2):243–7.

    Article  CAS  PubMed  Google Scholar 

  20. Nicoud IB, Jones CM, Pierce JM, Earl TM, Matrisian LM, Chari RS, et al. Warm hepatic ischemia–reperfusion promotes growth of colorectal carcinoma micrometastases in mouse liver via matrix metalloproteinase-9 induction. Cancer Res. 2007;67(6):2720–8.

    Article  CAS  PubMed  Google Scholar 

  21. Man K, Ng KT, Lo CM, Ho JW, Sun BS, Sun CK, et al. Ischemia–reperfusion of small liver remnant promotes liver tumor growth and metastasis—activation of cell invasion and migration pathways. Liver Transpl. 2007;13(12):1669–77.

    Article  PubMed  Google Scholar 

  22. Nijkamp MW, van der Bilt JD, Snoeren N, Hoogwater FJ, van Houdt WJ, Molenaar IQ, et al. Prolonged portal triad clamping during liver surgery for colorectal liver metastases is associated with decreased time to hepatic tumor recurrence. Eur J Surg Oncol. 2010;36(2):182–8.

    Article  CAS  PubMed  Google Scholar 

  23. Wang J, Liu Y, Zhang A, Li C, Dong J. Inhibitory CpG sequences reduced ischemis–reperfusion-induced hepatic metastases of liver tumor in a murine model. J Surg Res. 2012;178(1):248–54.

    Article  CAS  PubMed  Google Scholar 

  24. Yang Y, Fu SY, Lau WY, Lai ECh, Li AJ, Zhou WP, et al. Selective main portal vein clamping to minimize the risk of recurrence after curative liver resection for hepatocellular carcinoma. Hepatogastroenterology. 2012;59(117):1560–5.

    PubMed  Google Scholar 

  25. Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Duration of hepatic vascular inflow clamping and survival after liver resection for hepatocellular carcinoma. Br J Surg. 2011;98(9):1284–90.

    Article  CAS  PubMed  Google Scholar 

  26. Yamanaka N, Okamoto E, Fujihara S, Kato T, Fujimoto J, Oriyama T, et al. Do the tumor cells of hepatocellular carcinoma dislodge into the portal venous stream during hepatic resection? Cancer. 1992;70(9):2263–7.

    Article  CAS  PubMed  Google Scholar 

  27. Matsumata T, Kanemetsu T, Takenaka K, Sugimachi K. Lack of intrahepatic recurrence of hepatocellular carcinoma by temporary portal venous embolization with starch microspheres. Surgery. 1989;105(2):188–91.

    CAS  PubMed  Google Scholar 

  28. Tanaka T, Yamanaka N, Oriyama T, Furakawa K, Okamoto, E. Factors regulating tumor pressure in hepatocellular carcinoma and implication for tumor spread. Hepatology. 1997;26(2):283–7.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shenghua Hao.

Ethics declarations

Conflict of interest

Dr. Shenghua Hao and other co-authors have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hao, S., Chen, S., Yang, X. et al. Impact of intermittent portal clamping on the early recurrence of hepatocellular carcinoma after surgery. Surg Today 46, 1290–1295 (2016). https://doi.org/10.1007/s00595-016-1316-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-016-1316-6

Keywords

Navigation