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Published in: Surgical Endoscopy 3/2018

01-03-2018

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

Published in: Surgical Endoscopy | Issue 3/2018

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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.
Literature
1.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
2.
go back to reference 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):279–283CrossRefPubMed 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):279–283CrossRefPubMed
3.
go back to reference 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 CrossRef 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 CrossRef
4.
go back to reference 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):86–91CrossRefPubMedPubMedCentral 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):86–91CrossRefPubMedPubMedCentral
5.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
6.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
7.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
8.
go back to reference 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 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
9.
go back to reference 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 CrossRef 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 CrossRef
11.
go back to reference Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4(2):146–148PubMed Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4(2):146–148PubMed
12.
go back to reference 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 CrossRefPubMed 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​ CrossRefPubMed
14.
go back to reference 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 CrossRefPubMed 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​ CrossRefPubMed
15.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
16.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
17.
go back to reference 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):3768–3775CrossRefPubMed 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):3768–3775CrossRefPubMed
20.
go back to reference 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):3251–3260CrossRefPubMed 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):3251–3260CrossRefPubMed
22.
go back to reference 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 CrossRefPubMed 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​ CrossRefPubMed
24.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
25.
go back to reference 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 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
26.
27.
go back to reference 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):1779–1787CrossRefPubMed 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):1779–1787CrossRefPubMed
28.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
30.
31.
go back to reference 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 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​
32.
go back to reference 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):5–12CrossRefPubMed 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):5–12CrossRefPubMed
33.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
34.
go back to reference 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):678–685PubMed 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):678–685PubMed
35.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
36.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
38.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
40.
go back to reference 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 CrossRefPubMed 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​ CrossRefPubMed
Metadata
Title
Minimally invasive surgery as a treatment option for gastric cancer with liver metastasis: a comparison with open surgery
Publication date
01-03-2018
Published in
Surgical Endoscopy / Issue 3/2018
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-017-5826-0

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