Skip to main content

Minimally invasive surgery as a treatment option for gastric cancer with liver metastasis: a comparison with open surgery

Surgical Endoscopy volume 32, pages 1422–1433 (2018)Cite this article

Abstract

Background

As minimally invasive techniques advances, minimally invasive surgery (MIS) has emerged as an alternative modality for advanced gastric cancer. In this study, we compared the short- and long-term surgical outcomes of MIS and conventional open surgery for gastric cancer liver metastasis (GCLM) in terms of safety, feasibility, and efficacy.

Methods

This retrospective study used data from a prospective database at the Chinese People’s Liberation Army General Hospital. From January 2006 to June 2016, 53 gastric cancer patients with synchronous liver metastasis accepted radical gastrectomy combined with either or both hepatectomy and radiofrequency ablation for liver metastases. The 53 patients enrolled in the study were divided into two groups: a conventional open surgery group (n = 42) and an MIS group (n = 11). Propensity score matching (PSM) analysis was performed to overcome possible bias.

Results

With PSM performed at a 1:3 ratio, 11 patients who received MIS were compared with 33 open surgery cases. Mean operation time was significantly longer for the MIS group compared with the open surgery group (301 vs. 236 min, P = 0.032), while the open surgery group had a larger estimated blood loss than the MIS group (421 vs. 196 ml, P = 0.019). Time to first flatus and postoperative complications, including Clavien–Dindo classification, were similar in the two groups. However, patients undergoing MIS had a significantly shorter time to first sips of water (P = 0.020) and soft diet (P = 0.020) compared with open surgery counterparts. Long-term outcomes were comparable between groups (P = 0.090) after adjustment by PSM analysis.

Conclusions

MIS achieved superior short-term outcomes and comparable long-term outcomes compared with open surgery in GCLM patients. For experienced surgeons, both laparoscopic and robotic methods of MIS are reasonable approaches for the management of highly selected GCLM patients.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. Marrelli D, Roviello F, De Stefano A, Fotia G, Giliberto C, Garosi L, Pinto E (2004) Risk factors for liver metastases after curative surgical procedures for gastric cancer: a prospective study of 208 patients treated with surgical resection. J Am Coll Surg 198(1):51–58. doi:10.1016/j.jamcollsurg.2003.08.013

    Article  PubMed  Google Scholar 

  2. Ambiru S, Miyazaki M, Ito H, Nakagawa K, Shimizu H, Yoshidome H, Shimizu Y, Nakajima N (2001) Benefits and limits of hepatic resection for gastric metastases. Am J Surg 181(3):279–283

    CAS  Article  PubMed  Google Scholar 

  3. Garancini M, Uggeri F, Degrate L, Nespoli L, Gianotti L, Nespoli A, Uggeri F, Romano F (2012) Surgical treatment of liver metastases of gastric cancer: is local treatment in a systemic disease worthwhile? HPB (Oxford) 14(3):209–215. doi:10.1111/j.1477-2574.2011.00428.x

    Article  Google Scholar 

  4. Okano K, Maeba T, Ishimura K, Karasawa Y, Goda F, Wakabayashi H, Usuki H, Maeta H (2002) Hepatic resection for metastatic tumors from gastric cancer. Ann Surg 235(1):86–91

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sakamoto Y, Sano T, Shimada K, Esaki M, Saka M, Fukagawa T, Katai H, Kosuge T, Sasako M (2007) Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol 95(7):534–539. doi:10.1002/jso.20739

    Article  PubMed  Google Scholar 

  6. Takemura N, Saiura A, Koga R, Arita J, Yoshioka R, Ono Y, Hiki N, Sano T, Yamamoto J, Kokudo N, Yamaguchi T (2012) Long-term outcomes after surgical resection for gastric cancer liver metastasis: an analysis of 64 macroscopically complete resections. Langenbecks Arch Surg 397(6):951–957. doi:10.1007/s00423-012-0959-z

    Article  PubMed  Google Scholar 

  7. Cheon SH, Rha SY, Jeung HC, Im CK, Kim SH, Kim HR, Ahn JB, Roh JK, Noh SH, Chung HC (2008) Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol 19(6):1146–1153. doi:10.1093/annonc/mdn026

    CAS  Article  PubMed  Google Scholar 

  8. Liu J, Li JH, Zhai RJ, Wei B, Shao MZ, Chen L (2012) Predictive factors improving survival after gastric and hepatic surgical treatment in gastric cancer patients with synchronous liver metastases. Chin Med J (Engl) 125(2):165–171

    Google Scholar 

  9. Liu SF, Lu CR, Cheng HD, Xi HQ, Cui JX, Li JY, Shen WS, Chen L (2015) Comparison of therapeutic efficacy between gastrectomy with transarterial chemoembolization plus systemic chemotherapy and systemic chemotherapy alone in gastric cancer with synchronous liver metastasis. Chin Med J (Engl) 128(16):2194–2201. doi:10.4103/0366-6999.162497

    Article  Google Scholar 

  10. Japanese Gastric Cancer Association (2017) Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 20(1):1–19. doi:10.1007/s10120-016-0622-4

    Article  Google Scholar 

  11. Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4(2):146–148

    CAS  PubMed  Google Scholar 

  12. Kim HH, Hyung WJ, Cho GS, Kim MC, Han SU, Kim W, Ryu SW, Lee HJ, Song KY (2010) Morbidity and mortality of laparoscopic gastrectomy versus open gastrectomy for gastric cancer: an interim report–a phase III multicenter, prospective, randomized Trial (KLASS Trial). Ann Surg 251(3):417–420. doi:10.1097/SLA.0b013e3181cc8f6b

    Article  PubMed  Google Scholar 

  13. Lanfranco AR, Castellanos AE, Desai JP, Meyers WC (2004) Robotic surgery: a current perspective. Ann Surg 239(1):14–21. doi:10.1097/01.sla.0000103020.19595.7d

    Article  PubMed  PubMed Central  Google Scholar 

  14. Maeso S, Reza M, Mayol JA, Blasco JA, Guerra M, Andradas E, Plana MN (2010) Efficacy of the Da Vinci surgical system in abdominal surgery compared with that of laparoscopy: a systematic review and meta-analysis. Ann Surg 252(2):254–262. doi:10.1097/SLA.0b013e3181e6239e

    Article  PubMed  Google Scholar 

  15. Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, Ryu SW, Cho GS, Song KY, Ryu SY (2014) Long-term results of laparoscopic gastrectomy for gastric cancer: a large-scale case-control and case-matched Korean multicenter study. J Clin Oncol 32(7):627–633. doi:10.1200/JCO.2013.48.8551

    Article  PubMed  Google Scholar 

  16. Hayashi H, Ochiai T, Shimada H, Gunji Y (2005) Prospective randomized study of open versus laparoscopy-assisted distal gastrectomy with extraperigastric lymph node dissection for early gastric cancer. Surg Endosc 19(9):1172–1176. doi:10.1007/s00464-004-8207-4

    CAS  Article  PubMed  Google Scholar 

  17. Glenn JA, Turaga KK, Gamblin TC, Hohmann SF, Johnston FM (2015) Minimally invasive gastrectomy for cancer: current utilization in US academic medical centers. Surg Endosc 29(12):3768–3775

    Article  PubMed  Google Scholar 

  18. Hyung WJ, Song C, Cheong JH, Choi SH, Noh SH (2007) Factors influencing operation time of laparoscopy-assisted distal subtotal gastrectomy: analysis of consecutive 100 initial cases. Eur J Surg Oncol 33(3):314–319. doi:10.1016/j.ejso.2006.11.010

    CAS  Article  PubMed  Google Scholar 

  19. Ji WB, Wang HG, Zhao ZM, Duan WD, Lu F, Dong JH (2011) Robotic-assisted laparoscopic anatomic hepatectomy in China: initial experience. Ann Surg 253(2):342–348. doi:10.1097/SLA.0b013e3181ff4601

    Article  PubMed  Google Scholar 

  20. Lee J, Kim YM, Woo Y, Obama K, Noh SH, Hyung WJ (2015) Robotic distal subtotal gastrectomy with D2 lymphadenectomy for gastric cancer patients with high body mass index: comparison with conventional laparoscopic distal subtotal gastrectomy with D2 lymphadenectomy. Surg Endosc 29(11):3251–3260

    Article  PubMed  Google Scholar 

  21. Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection-2,804 patients. Ann Surg 250(5):831–841. doi:10.1097/SLA.0b013e3181b0c4df

    Article  PubMed  Google Scholar 

  22. Dagher I, O’Rourke N, Geller DA, Cherqui D, Belli G, Gamblin TC, Lainas P, Laurent A, Nguyen KT, Marvin MR, Thomas M, Ravindra K, Fielding G, Franco D, Buell JF (2009) Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg 250(5):856–860. doi:10.1097/SLA.0b013e3181bcaf46

    Article  PubMed  Google Scholar 

  23. Song J, Oh SJ, Kang WH, Hyung WJ, Choi SH, Noh SH (2009) Robot-assisted gastrectomy with lymph node dissection for gastric cancer: lessons learned from an initial 100 consecutive procedures. Ann Surg 249(6):927–932. doi:10.1097/01.sla.0000351688.64999.73

    Article  PubMed  Google Scholar 

  24. Austin PC (2011) Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat 10(2):150–161. doi:10.1002/pst.433

    Article  PubMed  Google Scholar 

  25. Chen PD, Wu CY, Hu RH, Chou WH, Lai HS, Liang JT, Lee PH, Wu YM (2016) Robotic versus open hepatectomy for hepatocellular carcinoma: a matched comparison. Ann Surg Oncol. doi:10.1245/s10434-016-5638-9

    Google Scholar 

  26. Son T, Lee JH, Kim YM, Kim HI, Noh SH, Hyung WJ (2014) Robotic spleen-preserving total gastrectomy for gastric cancer: comparison with conventional laparoscopic procedure. Surg Endosc 28(9):2606–2615. doi:10.1007/s00464-014-3511-0

    Article  PubMed  Google Scholar 

  27. Junfeng Z, Yan S, Bo T, Yingxue H, Dongzhu Z, Yongliang Z, Feng Q, Peiwu Y (2014) Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: comparison of surgical performance and short-term outcomes. Surg Endosc 28(6):1779–1787

    Article  PubMed  Google Scholar 

  28. Montalti R, Scuderi V, Patriti A, Vivarelli M, Troisi RI (2016) Robotic versus laparoscopic resections of posterosuperior segments of the liver: a propensity score-matched comparison. Surg Endosc 30(3):1004–1013. doi:10.1007/s00464-015-4284-9

    Article  PubMed  Google Scholar 

  29. Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G (2016) Comparative short-term benefits of laparoscopic Liver resection: 9000 cases and climbing. Ann Surg 263(4):761–777. doi:10.1097/SLA.0000000000001413

    Article  PubMed  Google Scholar 

  30. Komatsu S, Brustia R, Goumard C, Perdigao F, Soubrane O, Scatton O (2016) Laparoscopic versus open major hepatectomy for hepatocellular carcinoma: a matched pair analysis. Surg Endosc 30(5):1965–1974. doi:10.1007/s00464-015-4422-4

    Article  PubMed  Google Scholar 

  31. Yoon YI, Kim KH, Kang SH, Kim WJ, Shin MH, Lee SK, Jung DH, Park GC, Ahn CS, Moon DB, Ha TY, Song GW, Hwang S, Lee SG (2016) Pure laparoscopic versus open right hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a propensity score matched analysis. Ann Surg. doi:10.1097/SLA.0000000000002072

    Google Scholar 

  32. Hyung WJ, Noh SH, Shin DW, Huh J, Huh BJ, Choi SH, Min JS (2002) Adverse effects of perioperative transfusion on patients with stage III and IV gastric cancer. Ann Surg Oncol 9(1):5–12

    Article  PubMed  Google Scholar 

  33. Han TS, Kong SH, Lee HJ, Ahn HS, Hur K, Yu J, Kim WH, Yang HK (2011) Dissemination of free cancer cells from the gastric lumen and from perigastric lymphovascular pedicles during radical gastric cancer surgery. Ann Surg Oncol 18(10):2818–2825. doi:10.1245/s10434-011-1620-8

    Article  PubMed  Google Scholar 

  34. Marutsuka T, Shimada S, Shiomori K, Hayashi N, Yagi Y, Yamane T, Ogawa M (2003) Mechanisms of peritoneal metastasis after operation for non-serosa-invasive gastric carcinoma: an ultrarapid detection system for intraperitoneal free cancer cells and a prophylactic strategy for peritoneal metastasis. Clin Cancer Res 9(2):678–685

    PubMed  Google Scholar 

  35. Kwon IG, Cho I, Guner A, Choi YY, Shin HB, Kim HI, An JY, Cheong JH, Noh SH, Hyung WJ (2014) Minimally invasive surgery for remnant gastric cancer: a comparison with open surgery. Surg Endosc 28(8):2452–2458. doi:10.1007/s00464-014-3496-8

    Article  PubMed  Google Scholar 

  36. Laurent A, Tayar C, Andreoletti M, Lauzet JY, Merle JC, Cherqui D (2009) Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 16(3):310–314. doi:10.1007/s00534-009-0063-0

    Article  PubMed  Google Scholar 

  37. Tsung A, Geller DA, Sukato DC, Sabbaghian S, Tohme S, Steel J, Marsh W, Reddy SK, Bartlett DL (2014) Robotic versus laparoscopic hepatectomy: a matched comparison. Ann Surg 259(3):549–555. doi:10.1097/SLA.0000000000000250

    Article  PubMed  Google Scholar 

  38. Hu Y, Huang C, Sun Y, Su X, Cao H, Hu J, Xue Y, Suo J, Tao K, He X, Wei H, Ying M, Hu W, Du X, Chen P, Liu H, Zheng C, Liu F, Yu J, Li Z, Zhao G, Chen X, Wang K, Li P, Xing J, Li G (2016) Morbidity and mortality of laparoscopic versus open D2 distal gastrectomy for advanced gastric cancer: a randomized controlled trial. J Clin Oncol 34(12):1350–1357. doi:10.1200/JCO.2015.63.7215

    Article  PubMed  Google Scholar 

  39. Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res 46(3):399–424. doi:10.1080/00273171.2011.568786

    Article  Google Scholar 

  40. Cheung TT, Dai WC, Tsang SH, Chan AC, Chok KS, Chan SC, Lo CM (2016) Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg 264(4):612–620. doi:10.1097/SLA.0000000000001848

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all the patients who contributed data to this study.

Author information

Author notes

  1. Jiyang Li, Hongqing Xi, Jianxin Cui have contributed equally to this work.

Affiliations

  1. Department of General Surgery, Chinese People’s Liberation Army General Hospital, 28 Fuxing Road, Haidian District, Beijing, 100853, China

    Jiyang Li, Hongqing Xi, Jianxin Cui, Kecheng Zhang, Yunhe Gao, Wenquan Liang, Aizhen Cai, Bo Wei & Lin Chen

Authors
  1. Jiyang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongqing Xi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianxin Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kecheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yunhe Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenquan Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aizhen Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bo Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Bo Wei or Lin Chen.

Ethics declarations

Disclosures

Jiyang Li, Hongqing Xi, Jianxin Cui, Kecheng Zhang, Yunhe Gao, Wenquan Liang, Aizhen Cai, Bo Wei, and Lin Chen have no conflicts of interest or financial ties to disclose.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, J., Xi, H., Cui, J. et al. Minimally invasive surgery as a treatment option for gastric cancer with liver metastasis: a comparison with open surgery. Surg Endosc 32, 1422–1433 (2018). https://doi.org/10.1007/s00464-017-5826-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-017-5826-0

Keywords

  • Minimally invasive surgery
  • Robotics
  • Gastric cancer
  • Liver metastasis