Abstract
Background
Gastric cancer is the fifth most prevalent malignancy globally and the fourth major contributor to cancer-related mortality. The comparative effectiveness of robotic gastrectomy (RG) versus laparoscopic gastrectomy (LG) at different stages of gastric cancer is unclear regarding surgical and survival outcomes. We compared surgical and survival outcomes between RG and LG in early-stage (cStage I) and advanced (cStage II/III) gastric cancers to elucidate the difference in the efficacy of RG across various stages of gastric cancer.
Methods
We identified 299 patients (LG, 170; RG, 129) with cStage II/III disease and 569 (LG, 455; RG, 114) with cStage I disease who underwent either LG or RG. Following propensity score matching for RG and LG, 118 pairs were selected for cStage II/II and 113 pairs for cStage I. Surgical and survival outcomes of LG and RG were separately compared for cStage II/III and cStage I.
Results
In cStage II/III, RG showed significantly fewer intra-abdominal complications of Clavien–Dindo (C.D.) Grade ≥ III in the RG group than in the LG group (LG = 8.5 vs. RG = 1.7%, P = 0.033). Multivariate analysis identified LG as an independent risk factor for intra-abdominal complications of C.D. Grade ≥ III (OR 5.69, 95% CI 1.17–27.70, P = 0.031). However, in cStage I, no difference in surgical outcomes between LG and RG was observed. No differences were observed in survival outcomes between LG and RG in both cStage I or cStage II/III.
Conclusions
The real benefit of RG was demonstrated in surgical outcomes, especially for advanced-stage gastric cancer.
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References
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
Sasako M (2020) Progress in the treatment of gastric cancer in Japan over the last 50 years. Ann Gastroenterol Surg 4:21–29
Japanese Gastric Cancer Association (2023) Japanese gastric cancer treatment guidelines 2021 (6th edition). Gastric Cancer 26:1–25
Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4:146–148
Terashima M (2021) The 140 years’ journey of gastric cancer surgery: from the two hands of Billroth to the multiple hands of the robot. Ann Gastroenterol Surg 5:270–277
Kinoshita T, Uyama I, Terashima M, Noshiro H, Nagai E, Obama K, Tamamori Y, Nabae T, Honda M, Abe T (2019) Long-term outcomes of laparoscopic versus open surgery for clinical stage II/III gastric cancer: a multicenter cohort study in Japan (LOC-A study). Ann Surg 269:887–894
Katai H, Mizusawa J, Katayama H, Morita S, Yamada T, Bando E, Ito S, Takagi M, Takagane A, Teshima S, Koeda K, Nunobe S, Yoshikawa T, Terashima M, Sasako M (2020) Survival outcomes after laparoscopy-assisted distal gastrectomy versus open distal gastrectomy with nodal dissection for clinical stage IA or IB gastric cancer (JCOG0912): a multicentre, non-inferiority, phase 3 randomised controlled trial. Lancet Gastroenterol Hepatol 5:142–151
Yu J, Huang C, Sun Y, Su X, Cao H, Hu J, Wang K, Suo J, Tao K, He X, Wei H, Ying M, Hu W, Du X, Hu Y, Liu H, Zheng C, Li P, **e J, Liu F, Li Z, Zhao G, Yang K, Liu LH, Chen P, Ji J, Li G (2019) Effect of laparoscopic vs open distal gastrectomy on 3-year disease-free survival in patients with locally advanced gastric cancer. The CLASS-01 randomized clinical trial. JAMA 321:1983–1992
Hyung WJ, Yang HK, Park YK, Lee HJ, An JY, Kim W, Kim HI, Kim HH, Ryu SW, Hur H, Kim MC, Kong SH, Cho GS, Kim JJ, Park DJ, Ryu KW, Kim YW, Kim JW, Lee JH, Han SU (2020) Long-term outcomes of laparoscopic distal gastrectomy for locally advanced gastric cancer: the KLASS-02-RCT randomized clinical trial. J Clin Oncol 38:3304–3313
Etoh T, Ohyama T, Sakuramoto S, Tsuji T, Lee SW, Yoshida K, Koeda K, Hiki N, Kunisaki C, Tokunaga M, Otsubo D, Takagane A, Misawa K, Kinoshita T, Cho H, Doki Y, Nunobe S, Shiraishi N, Kitano S (2023) Five-year survival outcomes of laparoscopy-assisted vs open distal gastrectomy for advanced gastric cancer: the JLSSG0901 randomized clinical trial. JAMA Surg 1585:445–454
van der Veen A, Brenkman HJF, Seesing MFJ, Haverkamp L, Luyer MDP, Nieuwenhuijzen GAP, Stoot JHMB, Tegels JJW, Wijnhoven BPL, Lagarde SM, de Steur WO, Hartgrink HH, Kouwenhoven EA, Wassenaar EB, Draaisma WA, Gisbertz SS, van der Peet DL, May AM, Ruurda JP, van Hillegersberg R (2021) Laparoscopic versus open gastrectomy for gastric cancer (LOGICA): a multicenter randomized clinical trial. J Clin Oncol 39:978–989
Hashizume M, Sugimachi K (2003) Robot-assisted gastric surgery. Surg Clin North Am 83:1429–1444
Ryan S, Tameron A, Murphy A, Hussain L, Dunki-Jacobs E, Lee DY (2020) Robotic versus laparoscopic gastrectomy for gastric adenocarcinoma: propensity-matched analysis. Surg Innov 27:26–31
Zheng-Yan L, Yong-Liang Z, Feng Q, Yan S, Pei-Wu Y (2021) Morbidity and short-term surgical outcomes of robotic versus laparoscopic distal gastrectomy for gastric cancer: a large cohort study. Surg Endosc 35:3572–3583
Omori T, Yamamoto K, Hara H, Shinno N, Yamamoto M, Fujita K, Kanemura T, Takeoka T, Akita H, Wada H, Yasui M, Matsuda C, Nishimura J, Fujiwara Y, Miyata H, Ohue M, Sakon M (2022) Comparison of robotic gastrectomy and laparoscopic gastrectomy for gastric cancer: a propensity score-matched analysis. Surg Endosc 36:6223–6234
Nishi M, Shimada M, Yoshikawa K, Takasu C, Wada Y, Tokunaga T, Nakao T, Kashihara H, Yoshimoto T, Yamashita S (2022) Propensity score-matched analysis of the short- and long-term outcomes of robotic versus laparoscopic gastrectomy for gastric cancer. Ann Surg Oncol 29:3887–3895
Brierley JD, Gospodarowicz MK, Wittekind C (2017) TNM classification of malignant tumours. Wiley-Blackwell, United Kingdom.
Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma, 3rd English edn. Gastric Cancer 14:101–112
Dindo D, Demartines N, Clavien PA (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
Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, Furukawa H, Nakajima T, Ohashi Y, Imamura H, Higashino M, Yamamura Y, Kurita A, Arai K (2007) Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 357:1810–1820
Yoshida K, Kodera Y, Kochi M, Ichikawa W, Kakeji Y, Sano T, Nagao N, Takahashi M, Takagane A, Watanabe T, Kaji M, Okitsu H, Nomura T, Matsui T, Yoshikawa T, Matsuyama J, Yamada M, Ito S, Takeuchi M, Fujii M (2019) Addition of docetaxel to oral fluoropyrimidine improves efficacy in patients with stage III gastric cancer: interim analysis of JACCRO GC-07, a randomized controlled trial. J Clin Oncol 37:1296–1304
Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649–655
Hiki N, Honda M, Etoh T, Yoshida K, Kodera Y, Kakeji Y, Kumamaru H, Miyata H, Yamashita Y, Inomata M, Konno H, Seto Y, Kitano S (2018) Higher incidence of pancreatic fistula in laparoscopic gastrectomy. Real-world evidence from a nationwide prospective cohort study. Gastric Cancer 21:162–170
Shigeno T, Kizuki M, Tokunaga M, Fushimi K, Kinugasa Y, Fujiwara T (2023) A comparison of the short-term outcomes between laparoscopic and robotic distal gastrectomy: a retrospective study using a nationwide inpatient database. Surgery 173:1169–1175
Lu J, Wu D, Huang JB, Lin J, Xu BB, Xue Z, Zheng HL, Lin GS, Shen LL, Li P, Wang JB, Lin JX, Chen QY, Cao LL, **e JW, Zheng CH, Huang CM (2023) Comparison of robotic versus laparoscopic versus open distal gastrectomy for locally advanced gastric cancer: a prospective trial-based economic evaluation. Surg Endosc 37:7472–7485
Ojima T, Nakamura M, Hayata K, Kitadani J, Katsuda M, Takeuchi A, Tominaga S, Nakai T, Nakamori M, Ohi M, Kusunoki M, Yamaue H (2021) Short-term outcomes of robotic gastrectomy vs laparoscopic gastrectomy for patients with gastric cancer: a randomized clinical trial. JAMA Surg 156:954–963
Lu J, Zheng CH, Xu BB, **e JW, Wang JB, Lin JX, Chen QY, Cao LL, Lin M, Tu RH, Huang ZN, Lin JL, Zheng HL, Huang CM, Li P (2021) Assessment of robotic versus laparoscopic distal gastrectomy for gastric cancer: a randomized controlled trial. Ann Surg 273:858–867
Shibasaki S, Suda K, Nakauchi M, Nakamura K, Kikuchi K, Inaba K, Uyama I (2020) Non-robotic minimally invasive gastrectomy as an independent risk factor for postoperative intra-abdominal infectious complications: a single-center, retrospective and propensity score-matched analysis. World J Gastroenterol 26:1172–1184
Tian Y, Cao S, Kong Y, Shen S, Niu Z, Zhang J, Chen D, Jiang H, Lv L, Liu X, Li Z, Zhong H, Zhou Y (2022) Short- and long-term comparison of robotic and laparoscopic gastrectomy for gastric cancer by the same surgical team: a propensity score matching analysis. Surg Endosc 36:185–195
Tokunaga M, Tanizawa Y, Bando E, Kawamura T, Terashima M (2013) Poor survival rate in patients with postoperative intra-abdominal infectious complications following curative gastrectomy for gastric cancer. Ann Surg Oncol 20:1575–1583
Fujiya K, Tokunaga M, Mori K, Makuuchi R, Tanizawa Y, Bando E, Kawamura T, Terashima M (2016) Long-term survival in patients with postoperative intra-abdominal infectious complications after curative gastrectomy for gastric cancer: a propensity score matching analysis. Ann Surg Oncol 23:809–816
Han WH, Oh YJ, Eom BW, Yoon HM, Kim YW, Ryu KW (2020) Prognostic impact of infectious complications after curative gastric cancer surgery. Eur J Surg Oncol 46:1233–1238
Gao G, Liao H, Jiang Q, Liu D, Li T (2022) Surgical and oncological outcomes of robotic- versus laparoscopic-assisted distal gastrectomy with D2 lymphadenectomy for advanced gastric cancer: a propensity score-matched analysis of 1164 patients. World J Surg Oncol 20:315. https://doi.org/10.7150/jca.58154
Suda K, Sakai M, Obama K, Yoda Y, Shibasaki S, Tanaka T, Nakauchi M, Hisamori S, Nishigori T, Igarashi A, Noshiro H, Terashima M, Uyama I (2023) Three-year outcomes of robotic gastrectomy versus laparoscopic gastrectomy for the treatment of clinical stage I/II gastric cancer: a multi-institutional retrospective comparative study. Surg Endosc 37:2858–2872
Nakauchi M, Suda K, Shibasaki S, Nakamura K, Kadoya S, Kikuchi K, Inaba K, Uyama I (2021) Prognostic factors of minimally invasive surgery for gastric cancer: does robotic gastrectomy bring oncological benefit? World J Gastroenterol 27:6659–6672
Acknowledgements
We would like to thank Editage (www.editage.jp) for English language editing.
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Study conception and design: Shirou Kuwabara. Acquisition of data: Shirou Kuwabara, Kazuaki Kobayashi, and Natsuru Sudo. Data analysis and interpretation: Shirou Kuwabara, Kazuaki Kobayashi, and Natsuru Sudo. Manuscript drafting: Shirou Kuwabara. Critical revision of the manuscript: Kazuaki Kobayashi and Natsuru Sudo.
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Shirou Kuwabara, Kazuaki Kobayashi, and Natsuru Sudo have no conflicts of interest or financial ties to disclose..
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All procedures involving human participants performed in this study were in accordance with the ethical standards of the institutional and/or national research committee and the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This study was approved by the Institutional Review Board of Niigata City General Hospital (#23-032).
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Kuwabara, S., Kobayashi, K. & Sudo, N. Robotic gastrectomy is more beneficial for advanced than early-stage gastric cancer: a comparison with laparoscopic gastrectomy using propensity score matching. Surg Endosc 38, 3799–3809 (2024). https://doi.org/10.1007/s00464-024-10905-9
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DOI: https://doi.org/10.1007/s00464-024-10905-9