Abstract
Evidence of implementation of laparoscopic total gastrectomy (LTG) for surgical T4a stage (sT4a) gastric cancer (GC) remains inadequate. This study aimed to compare short- and long-term outcomes of LTG versus open total gastrectomy (OTG) for sT4a GC. This retrospective cohort study was conducted using data from patients with sT4a GC underwent total gastrectomy from 2014 to 2020. Short-term outcomes included operative characteristics and postoperative complications. Long-term oncological outcomes focused on 3-, and 5-year overall survival (OS) and disease-free survival (DFS). Propensity score matching (PSM) was applied to reduce potential biases in baseline characteristics between groups. There was a total of 161 patients, in which 96 underwent LTG and 65 underwent OTG. After PSM, both groups consisted of 51 patients each, with balanced baseline characteristics. There were no significant differences between the two groups regarding blood loss, length of proximal resected margin, postoperative hospital stays, and overall and major postoperative complications. Most of the complications were classified as minor according to the Clavien–Dindo classification. Operating time was significantly longer in the LTG group (mean: 257 min vs. 231 min, p = 0.006). LTG was superior to OTG groups in time to flatus (mean: 3.0 days vs 3.9 days, p < 0.001). Five-year OS and DFS rates were similar between the two groups (44% and 33% vs. 43% and 28% in the LTG and OTG groups, respectively). Our findings indicate that LTG is a feasible and safe technique, exhibiting comparable long-term oncological outcomes to OTG for sT4a GC. LTG may be an acceptable alternative to OTG for the treatment of sT4a GC.
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The data presented in this study are available on request from the corresponding author.
References
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492
Nussbaum DP, Pappas TN, Perez A (2015) Laparoscopic total gastrectomy in the western patient population: tips, techniques, and evidence-based practice. Surg Laparosc Endosc Percutan Tech 25(6):455–461. https://doi.org/10.1097/sle.0000000000000210
**ong JJ, Nunes QM, Huang W, Tan CL, Ke NW, **e SM, Ran X, Zhang H, Chen YH, Liu XB (2013) Laparoscopic vs open total gastrectomy for gastric cancer: a meta-analysis. World J Gastroenterol 19(44):8114–8132. https://doi.org/10.3748/wjg.v19.i44.8114
Etoh T, Honda M, Kumamaru H, Miyata H, Yoshida K, Kodera Y, Kakeji Y, Inomata M, Konno H, Seto Y, Kitano S, Hiki N (2018) Morbidity and mortality from a propensity score-matched, prospective cohort study of laparoscopic versus open total gastrectomy for gastric cancer: data from a nationwide web-based database. Surg Endosc 32(6):2766–2773. https://doi.org/10.1007/s00464-017-5976-0
Chen K, Pan Y, Cai JQ, Wu D, Yan JF, Chen DW, Yu HM, Wang XF (2016) Totally laparoscopic versus laparoscopic-assisted total gastrectomy for upper and middle gastric cancer: a single-unit experience of 253 cases with meta-analysis. World J Surg Oncol 14:96. https://doi.org/10.1186/s12957-016-0860-2
Huang C, Liu H, Hu Y, Sun Y, Su X, Cao H, Hu J, Wang K, Suo J, Tao K, He X, Wei H, Ying M, Hu W, Du X, Yu J, Zheng C, Liu F, Li Z, Zhao G, Zhang J, Chen P, Li G (2022) Laparoscopic vs open distal gastrectomy for locally advanced gastric cancer: five-year outcomes from the CLASS-01 randomized clinical trial. JAMA Surg 157(1):9–17. https://doi.org/10.1001/jamasurg.2021.5104
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(28):3304–3313. https://doi.org/10.1200/jco.20.01210
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 158(5):445–454. https://doi.org/10.1001/jamasurg.2023.0096
Hyung WJ, Yang HK, Han SU, Lee YJ, Park JM, Kim JJ, Kwon OK, Kong SH, Kim HI, Lee HJ, Kim W, Ryu SW, ** SH, Oh SJ, Ryu KW, Kim MC, Ahn HS, Park YK, Kim YH, Hwang SH, Kim JW, Cho GS (2019) A feasibility study of laparoscopic total gastrectomy for clinical stage I gastric cancer: a prospective multi-center phase II clinical trial, KLASS 03. Gastric Cancer 22(1):214–222. https://doi.org/10.1007/s10120-018-0864-4
Liu F, Huang C, Xu Z, Su X, Zhao G, Ye J, Du X, Huang H, Hu J, Li G, Yu P, Li Y, Suo J, Zhao N, Zhang W, Li H, He H, Sun Y (2020) Morbidity and mortality of laparoscopic vs open total gastrectomy for clinical stage I gastric cancer: the CLASS02 multicenter randomized clinical trial. JAMA Oncol 6(10):1590–1597. https://doi.org/10.1001/jamaoncol.2020.3152
Lee MS, Lee JH, Park DJ, Lee HJ, Kim HH, Yang HK (2013) Comparison of short- and long-term outcomes of laparoscopic-assisted total gastrectomy and open total gastrectomy in gastric cancer patients. Surg Endosc 27(7):2598–2605. https://doi.org/10.1007/s00464-013-2796-8
Jeong O, Jung MR, Kim GY, Kim HS, Ryu SY, Park YK (2013) Comparison of short-term surgical outcomes between laparoscopic and open total gastrectomy for gastric carcinoma: case-control study using propensity score matching method. J Am Coll Surg 216(2):184–191. https://doi.org/10.1016/j.jamcollsurg.2012.10.014
Kodera Y, Yoshida K, Kumamaru H, Kakeji Y, Hiki N, Etoh T, Honda M, Miyata H, Yamashita Y, Seto Y, Kitano S, Konno H (2019) Introducing laparoscopic total gastrectomy for gastric cancer in general practice: a retrospective cohort study based on a nationwide registry database in Japan. Gastric Cancer 22(1):202–213. https://doi.org/10.1007/s10120-018-0795-0
Son T, Hyung WJ, Lee JH, Kim YM, Noh SH (2014) Minimally invasive surgery for serosa-positive gastric cancer (pT4a) in patients with preoperative diagnosis of cancer without serosal invasion. Surg Endosc 28(3):866–874. https://doi.org/10.1007/s00464-013-3236-5
Li Z, Liu Y, Hao Y, Bai B, Yu D, Zhao Q (2019) Surgical and long-term oncologic outcomes of laparoscopic and open gastrectomy for serosa-positive (pT4a) gastric cancer: A propensity score-matched analysis. Surg Oncol 28:167–173. https://doi.org/10.1016/j.suronc.2019.01.003
Japanese gastric cancer treatment guidelines 2014 (ver. 4) (2017). Gastric Cancer 20 (1):1–19. https://doi.org/10.1007/s10120-016-0622-4
Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196. https://doi.org/10.1097/SLA.0b013e3181b13ca2
Wada N, Kurokawa Y, Takiguchi S, Takahashi T, Yamasaki M, Miyata H, Nakajima K, Mori M, Doki Y (2014) Feasibility of laparoscopy-assisted total gastrectomy in patients with clinical stage I gastric cancer. Gastric Cancer 17(1):137–140. https://doi.org/10.1007/s10120-013-0235-0
Liu D, Liang L, Liu L, Zhu Z, Liu S, Hu L, He Y, Fang Y, Wan X (2020) Short-term outcomes and prognosis of laparoscopy-assisted total gastrectomy in elderly patients with stomach cancer. Surg Endosc 34(12):5428–5438. https://doi.org/10.1007/s00464-019-07338-0
Katai H, Mizusawa J, Katayama H, Kunisaki C, Sakuramoto S, Inaki N, Kinoshita T, Iwasaki Y, Misawa K, Takiguchi N, Kaji M, Okitsu H, Yoshikawa T, Terashima M (2019) Single-arm confirmatory trial of laparoscopy-assisted total or proximal gastrectomy with nodal dissection for clinical stage I gastric cancer: Japan Clinical Oncology Group study JCOG1401. Gastric Cancer 22(5):999–1008. https://doi.org/10.1007/s10120-019-00929-9
Di Carlo S, Siragusa L, Fassari A, Fiori E, La Rovere F, Izzo P, Usai V, Cavallaro G, Franceschilli M, Dhimolea S, Sibio S (2022) Laparoscopic versus open total gastrectomy for locally advanced gastric cancer: short and long-term results. Curr Oncol 29(11):8442–8455. https://doi.org/10.3390/curroncol29110665
Eom SS, Park SH, Eom BW, Yoon HM, Kim Y-W, Ryu KW (2022) Short and long-term surgical outcomes of laparoscopic total gastrectomy compared with open total gastrectomy in gastric cancer patients. Cancers 15(1):76. https://doi.org/10.3390/cancers15010076
Fan Y, Liu M, Li S, Yu J, Qi X, Tan F, Xu K, Zhang N, Yao Z, Yang H, Zhang C, **ng J, Wang Z, Cui M, Su X (2021) Surgical and oncological efficacy of laparoscopic-assisted total gastrectomy versus open total gastrectomy for gastric cancer by propensity score matching: a retrospective comparative study. J Cancer Res Clin Oncol 147(7):2153–2165. https://doi.org/10.1007/s00432-020-03503-4
Lee SR, Kim HO, Son BH, Shin JH, Yoo CH (2014) Laparoscopic-assisted total gastrectomy versus open total gastrectomy for upper and middle gastric cancer in short-term and long-term outcomes. Surg Laparosc Endosc Percutan Tech 24(3):277–282. https://doi.org/10.1097/SLE.0b013e3182901290
Kim HS, Kim BS, Lee IS, Lee S, Yook JH, Kim BS (2013) Comparison of totally laparoscopic total gastrectomy and open total gastrectomy for gastric cancer. J Laparoendosc Adv Surg Tech A 23(4):323–331. https://doi.org/10.1089/lap.2012.0389
Feng X, Chen X, Ye Z, **ong W, Yao X, Wang W, Wang J, Chen L, Li Y (2021) Laparoscopic versus open total gastrectomy for advanced gastric cancer: a multicenter, propensity score-matched cohort study in China. Front Oncol 11:780398. https://doi.org/10.3389/fonc.2021.780398
Bo T, Peiwu Y, Feng Q, Yongliang Z, Yan S, Yingxue H, Huaxing L (2013) Laparoscopy-assisted vs. open total gastrectomy for advanced gastric cancer: long-term outcomes and technical aspects of a case–control study. J Gastro Surg 17(7):1202–1208. https://doi.org/10.1007/s11605-013-2218-1
Yang Y, Chen Y, Hu Y, Feng Y, Mao Q, Xue W (2022) Outcomes of laparoscopic versus open total gastrectomy with D2 lymphadenectomy for gastric cancer: a systematic review and meta-analysis. Eur J Med Res 27(1):124. https://doi.org/10.1186/s40001-022-00748-2
Lin JX, Lin JL, Zheng CH, Li P, **e JW, Wang JB, Lu J, Chen QY, Cao LL, Lin M, Tu RH, Huang ZN, Huang CM (2017) Short- and long-term outcomes of laparoscopy-assisted versus open total gastrectomy for gastric cancer: a propensity score-matched analysis. Oncotarget 8(45):80029–80038. https://doi.org/10.18632/oncotarget.16852
Liang Y, Ding X, Wang X, Wang B, Deng J, Zhang L, Liang H (2015) Prognostic value of surgical margin status in gastric cancer patients. ANZ J Surg 85(9):678–684. https://doi.org/10.1111/ans.12515
Cho BC, Jeung HC, Choi HJ, Rha SY, Hyung WJ, Cheong JH, Noh SH, Chung HC (2007) Prognostic impact of resection margin involvement after extended (D2/D3) gastrectomy for advanced gastric cancer: a 15-year experience at a single institute. J Surg Oncol 95(6):461–468. https://doi.org/10.1002/jso.20731
Juez LD, Barranquero AG, Priego P, Cuadrado M, Blázquez L, Sánchez-Picot S, Fernández-Cebrián JM, Galindo J (2021) Influence of positive margins on tumour recurrence and overall survival after gastrectomy for gastric cancer. ANZ J Surg 91(7–8):E465-e473. https://doi.org/10.1111/ans.16937
Shen JG, Cheong JH, Hyung WJ, Kim J, Choi SH, Noh SH (2006) Influence of a microscopic positive proximal margin in the treatment of gastric adenocarcinoma of the cardia. World J Gastroenterol 12(24):3883–3886. https://doi.org/10.3748/wjg.v12.i24.3883
Zhang X, Zhao L, Niu P, Wang T, Wang W, Sun C, Li Z, Chen Y, Zhao D (2022) Adjuvant Chemotherapy Might Be Recommended to Patients With Positive Margin After Gastrectomy: A 20-Year Retrospective Analysis in a Single Center. Frontiers in Oncology 11. https://doi.org/10.3389/fonc.2021.794032
Wang SY, Yeh CN, Lee HL, Liu YY, Chao TC, Hwang TL, Jan YY, Chen MF (2009) Clinical impact of positive surgical margin status on gastric cancer patients undergoing gastrectomy. Ann Surg Oncol 16(10):2738–2743. https://doi.org/10.1245/s10434-009-0616-0
Gaspar-Figueiredo S, Allemann P, Borgstein ABJ, Joliat GR, Luzuy-Guarnero V, Brunel C, Sempoux C, Gisbertz SS, Demartines N, van Berge Henegouwen MI, Schäfer M, Mantziari S (2023) Impact of positive microscopic resection margins (R1) after gastrectomy in diffuse-type gastric cancer. J Cancer Res Clin Oncol 149(13):11105–11115. https://doi.org/10.1007/s00432-023-04981-y
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Drs. Vo Duy Long, Doan Thuy Nguyen, Dang Quang Thong, Tran Quang Dat, Nguyen Viet Hai, Nguyen Lam Vuong, and Nguyen Hoang Bac disclose any potential or actual personal, political, or financial conflict of interest in the material, information or techniques described in the paper.
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The study was conducted according to the guidelines of the Declaration of Helsinki and approved by Institutional Review Board, University Medical Center at Ho Chi Minh city. Approval to perform research on human subjects in this study was provided by the Institutional Review Board, University Medical Center Ho Chi Minh city.
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Long, V.D., Nguyen, D.T., Thong, D.Q. et al. Laparoscopic versus open total gastrectomy for T4a gastric cancer: a propensity score-matched analysis of long-term outcomes. Updates Surg (2024). https://doi.org/10.1007/s13304-024-01910-7
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DOI: https://doi.org/10.1007/s13304-024-01910-7