Abstract
Background
The feasibility and oncological safety of non-curative endoscopic submucosal dissection (ESD) prior to additional gastrectomy for early gastric cancer (EGC) are still unclear. The aim of this study was to evaluate the impact of non-curative ESD on short- and long-term outcomes of subsequent laparoscopic gastrectomy (LG) for pathological T1 (pT1) EGC.
Methods
We retrospectively investigated 422 patients who underwent LG for pT1 EGC between January 2007 and December 2017 at our center. Eighty-five of these patients underwent ESD with curative intent before surgery. Using propensity-score matching for sex, age, body mass index, American society of anesthesiologists score, history of previous abdominal surgery, tumor location, mucosal/submucosal infiltration, histology, lymph node metastasis, extent of lymph node dissection, operative method, lymphatic invasion, and venous invasion, the clinicopathologic and survival data of these patients were compared.
Results
The median follow-up period was 60 (range 2–168) months. Using propensity-score matching from a total of 422 patients, 75 patients were selected in the Non-ESD and the ESD cohorts each. There were no significant differences in terms of characteristics and clinicopathological findings between the two groups. Furthermore, there were no significant differences in postoperative morbidity (13.3% vs. 17.3%; P = 0.497) and mortality (1.3% vs. 0%; P = 0.316). Both the 5-year overall survival ratio (88.8% vs. 86.9%; P = 0.757) and 5-year disease-specific survival ratio (97.1% vs. 98.4%; P = 0.333) were similar in the two groups.
Conclusion
Short- and long-term outcomes of LG in patients with pT1 EGC are not related to preoperative ESD history. Even for non-curative resections, ESD prior to surgery is feasible in terms of oncological and surgical outcomes in pT1 EGC.
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References
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Donald MP, David F, Freddie B (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:359–386
Kato M, Kaise M, Yonezawa J, Toyoizumi H, Yoshimura N, Yoshida Y, Kawamura M, Tajiri H (2010) Magnifying endoscopy with narrow-band imaging achieves superior accuracy in the differential diagnosis of superficial gastric lesions identified with white-light endoscopy: a prospective study. Gastrointest Endosc 72:523–529
Noh GY, Ku HR, Kim YJ, Park SC, Kim J, Han CJ, Kim YC, Yang KY (2015) Clinical outcomes of early gastric cancer with lymphovascular invasion or positive vertical resection margin after endoscopic submucosal dissection. Surg Endosc 29:2583–2589
Yamada S, Doyama H, Yao K, Uedo N, Ezoe Y, Oda I, Kaneko K, Kawahara Y, Yokoi C, Sugiura Y, Ishikawa H, Takeuchi Y, Saito Y, Muto M (2014) An efficient diagnostic strategy for small, depressed early gastric cancer with magnifying narrow-band imaging: a post-hoc analysis of a prospective randomized controlled trial. Gastrointest Endosc 79:55–63
Ryu SJ, Kim BW, Kim BG, Kim JH, Kim JS, Kim JI, Park JM, Oh JH, Kim TH, Kim JJ, Park SM, Park CH, Song KY, Lee JH, Kim SG, Kim DJ, Kim W (2016) Endoscopic submucosal dissection versus surgical resection for early gastric cancer: a retrospective multicenter study on immediate and long-term outcome over 5years. Surg Endosc 30:5283–5289
Chiu PW, Teoh AY, To KF, Wong SK, Liu SY, Lam CC, Yung MY, Chan FK, Lau JY, Ng EK (2012) Endoscopic submucosal dissection (ESD) compared with gastrectomy for treatment of early gastric neoplasia: a retrospective cohort study. Surg Endosc 26:3584–3591
Gotoda T (2007) Endoscopic resection of early gastric cancer. Gastric Cancer 10:1–11
Choi KS, Jung HY, Choi KD, Lee GH, Song HJ, Kim DH, Lee JH, Kim MY, Kim BS, Oh ST, Yook JH, Jang SJ, Yun SC, Kim SO, Kim JH (2011) EMR versus gastrectomy for intramucosal gastric cancer: comparison of long-term outcomes. Gastrointest Endosc 73:942–948
Park CH, Shin S, Park JC, Shin SK, LeeSK LYC, Lee H (2013) Long-term outcome of early gastric cancer after endoscopic submucosal dissection: expanded indication is comparable to absolute indication. Dig Liver Dis 45:651–656
Nishizawa T, Yahagi N (2018) Long-term outcomes of using endoscopic submucosal dissection to treat early gastric cancer. Gut Liver 12:119–124
Sunagawa H, Kinoshita T, Kaito A, Shibasaki H, Kaneko K, Ochiai A, Ohtsu A, Nishida T (2017) Additional surgery for non-curative resection after endoscopic submucosal dissection for gastric cancer: a retrospective analysis of 200 cases. Surg Today 47:202–209
Tanabe S, Ishido K, Higuchi K, Sasaki T, Katada C, Azuma M, Naruke A, Kim M, Koizumi W (2014) Long-term outcomes of endoscopic submucosal dissection for early gastric cancer: a retrospective comparison with conventional endoscopic resection in a single center. Gastric Cancer 17:130–136
Suzuki S, Gotoda T, Hatta W, Oyama T, Takahashi A, Yoshifuku Y, Hoteya S, Nakagawa M, Hirano M, Esaki M, Matsuda M, Ohnita K, Yamanouchi K, Yoshida M, Dohi O, Takeda J, Tanaka K, Yamada S, Tsuji T, Ito H, Hayashi Y, Shimosegawa T (2017) Survival benefit of additional surgery after non-curative endoscopic submucosal dissection for early gastric cancer: a propensity scorematching analysis. Ann SurgOncol 24:3353–3360
Ishida R, Kanaji S, Maehara R, Hasegawa H, Yamamoto M, Matsuda Y, Yamashita K, Matsuda T, Oshikiri T, Sumi Y, Nakamura T, Suzuki S, Kakeji Y (2018) Significance of additional gastrectomy including endoscopic submucosal dissection scar for gastric cancer. Anticancer Res 38:5289–5294
Suzuki H, Oda I, Abe S, Sekiguchi M, Nonaka S, Yoshinaga S, Saito Y, Fukunaga T, Katai H (2017) Clinical outcomes of early gastric cancer patients after noncurative endoscopic submucosal dissection in a large consecutive patient series. Gastric Cancer 20:679–689
Akagi T, Shiraishi N, Hiroishi K, Etoh T, Yasuda K, Kitano S (2010) Case series of intra-abdominal adhesions induced by artificial ulceration after endoscopic submucosal dissection before additional laparoscopic gastrectomy. Gastrointest Endosc 72:438–443
Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y (1995) Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 38:1286–1295
Kawamura YJ, Sugamata Y, Yoshino K et al (1999) Endoscopic resection for submucosally invasive colorectal cancer: is it feasible? Surg Endosc 13:224–227
Matsuda K, Masaki T, Abo Y, Nara S, Sumita T, Setoyama R, Kiribuchi Y, Kawano N (1999) Rapid growth of residual colonic tumor after incomplete mucosal resection. J Gastroenterol 34:260–263
Koch M, Kienle P, Sauer P, Willeke F, Buhl K, Benner A, Lehnert T, Herfarth C, Doeberitz MV, Weitz J (2004) Hematogenous tumor cell dissemination during colonoscopy for colorectal cancer. Surg Endosc 18:587–591
Jörgren F, Johansson R, Damber L, Lindmark G (2010) Oncological outcome after incidental perforation in radical rectal cancer surgery. Int J Colorectal Dis 25:731–740
Japanese Gastric Cancer A (2017) Japanese gastric cancer treatmentguidelines, 2014 (ver. 4). Gastric Cancer 20:1–19
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(2):205–213
Ono H, Yao K, Fujishiro M, Oda I, Nimura S, Yahagi N, Iishi H, Oka M, Ajioka Y, Ichinose M, Matsui T (2016) Guidelines for endoscopic submucosal dissection and endoscopic mucosal resection for early gastric cancer. Dig Endosc 28:3–15
Ryu KW, Choi IJ, Doh YW, Kook MC, Kim CG, Park HJ, Lee JH, Lee JS, Lee JY, Kim YW, Bae JM (2007) Surgical indication for non-curative endoscopic resection in early gastric cancer. Ann Surg Oncol 14:3428–3434
Nagano H, Ohyama S, Fukunaga T, Seto Y, Fujisaki J, Yamaguchi T, Yamamoto N, Kato Y, Yamaguchi A (2005) Indications for gastrectomy after incomplete EMR forearly gastric cancer. Gastric Cancer 8:149–154
Jung H, Bae JM, Choi MG, Noh JH, Sohn TS, Kim S (2011) Surgical outcome after incomplete endoscopic submucosal dissection of gastric cancer. Br J Surg 98:73–78
Shindo K, Castillo J, Ohuchida K, Moriyama T, Nagai S, Moriyama T, Ohtsuka T, Nagai E, Shimizu S, Nakamura M (2020) Influence of endoscopic resection on additional laparoscopic distal gastrectomy: a propensity score-matching analysis. Surg Today 50:1290–1296
Kakushima N, Fujishiro M, Kodashima S, Kobayashi K, Tateishi A, Iguchi M, Imagawa A, Motoi T, Yahagi N, Omata M (2006) Histopathologic characteristics of gastric ulcers created by endoscopic submucosal dissection. Endoscopy 38:412–415
Kawata N, Kakushima N, Tokunaga M, Tanaka M, Sawai H, Takizawa K, Imai K, Hotta K, Yamaguchi Y, Matsubayashi H, Tanizawa Y, Bando E, Kawamura T, Terashima M, Ono H (2015) Influence of endoscopic submucosal dissection on additional gastric resections. Gastric Cancer 18:339–345
Jiang X, Hiki N, Yoshiba H, Nunobe S, Kumagai K, Sano T, Yamaguchi T (2011) Laparoscopy-assisted gastrectomy in patients with previous endoscopic resection for early gastric cancer. Br J Surg 98:385–390
Tsujimoto H, Yaguchi Y, Kumano I, Takahata R, Matsumoto Y, Yoshida K, Horiguchi H, Aosasa S, Ono S, Yamamoto J, Hase K (2012) Laparoscopic gastrectomy after incomplete endoscopic resection for early gastric cancer. Oncol Rep 28:2205–2210
Lee EG, Ryu KW, Eom BW, Yoon HM, Kim YI, Cho SJ, Lee JY, Kim CG, Choi IJ, Kim YW (2017) The effect of endoscopic resection on short-term surgical outcomes in patients with additional laparoscopic gastrectomy after non-curative resection for gastric cancer. J Gastric Canc 17:33–42
Choi J, Kim SG, Im JP, Kim JS, Jung HC (2013) Endoscopic estimation of tumor size in early gastric cancer. Dig Dis Sci 58:2329–2336
Shim CN, Song MK, Kang DR, Chung HS, Park JC, Lee H, Shin SK, lee SK, Lee YC, (2014) Size discrepancy between endoscopic size and pathologic size is not negligible in endoscopic resection for early gastric cancer. Surg Endosc 28:2199–2207
Kim JM, Sohn JH, Cho MY, Kim WH, Chang HK, Jung ES, Kook MC, Jin SY, Chae YS, Park YS, Kang MS, Kim H, Lee JH, Park DY, Kim KM, Kim H, Kim YW, Hwang SS, Seol SY, Jung HY, Lee NR, Park SH, You JH (2016) Pre- and post-ESD discrepancies in clinicopathologic criteria in early gastric cancer: the NECA-Korea ESD for early gastric cancer prospective study (N-Keep). Gastric Cancer 19:1104–1113
Sano T, Okuyama Y, Kobori O, Shimizu T, Morioka Y (1990) Early gastric cancer. Endoscopic diagnosis of depth of invasion. Dig Dis Sci 35:1340–1344
Takao M, Kakushima N, Takizawa K, Tanaka M, Yamaguchi Y, Matsubayashi H, Kusafuka K, Ono H (2012) Discrepancies in histologic diagnoses of early gastric cancer between biopsy and endoscopic mucosal resection specimens. Gastric Cancer 15:91–96
Min BH, Kang K, Lee J, Kim E, Min Y, Rhee PL, Kim JJ, Rhee JC, Kim KM (2014) Endoscopic resection for undifferentiated early gastric cancer: focusing on histologic discrepancies between forceps biopsybased and endoscopic resection specimen-based diagnosis. Dig Dis Sci 59:2536–2543
Martinez QA, Han WH, Eom BW, Yoon HM, Kim YI, Cho SJ, Lee JY, Kim CG, Conde SM, Ruiz JP, Kook MC, Choi IJ, Kim YW, Ryu KW (2018) The distribution pattern of metastatic lymph nodes after non-curative endoscopic resection in early gastric cancer. J Surg Oncol 118:1257–1263
Nohara K, Goto O, Takeuchi H, Sasaki M, Maehata T, Yahagi N, Kitagawa Y (2019) Gastric lymphatic flows may change before and after endoscopic submucosal dissection: in vivo porcine survival models. Gastric Cancer 22:723–730
Acknowledgements
I gratefully acknowledge the work of member of Digestive Disease Center, Showa University Northern Yokohama Hospital, Yokohama, Japan
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Drs. S. Shimada, N. Sawada, S. Oae, J. Seki, Y. Takano, K. Nakahara, Y. Takehara, S. Mukai, F. Ishida, and S. Kudo, have no conflicts of interest or financial ties to disclose.
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Shimada, S., Sawada, N., Oae, S. et al. Impact of non-curative endoscopic submucosal dissection on short- and long-term outcome of subsequent laparoscopic gastrectomy for pT1 gastric cancer. Surg Endosc 36, 3985–3993 (2022). https://doi.org/10.1007/s00464-021-08718-1
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DOI: https://doi.org/10.1007/s00464-021-08718-1