Accepted for Publication: December 19, 2021.
Published Online: March 23, 2022. doi:10.1001/jamasurg.2022.0182
Corresponding Author: Jiping Wang, MD, PhD, Department of Surgery, Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115 (jwang39@bwh.harvard.edu).
Author Contributions: Dr Wang had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Concept and design: All authors.
Acquisition, analysis, or interpretation of data: Wang.
Drafting of the manuscript: Li, Wang.
Critical revision of the manuscript for important intellectual content: All authors.
Administrative, technical, or material support: Doherty, Wang.
Supervision: Doherty, Wang.
Conflict of Interest Disclosures: None reported.
2.Parsonnet
J , Vandersteen
D , Goates
J , Sibley
RK , Pritikin
J , Chang
Y .
Helicobacter pylori infection in intestinal- and diffuse-type gastric adenocarcinomas.
J Natl Cancer Inst. 1991;83(9):640-643. doi:
10.1093/jnci/83.9.640PubMedGoogle ScholarCrossref 4.Bray
F , Ferlay
J , Soerjomataram
I , Siegel
RL , Torre
LA , Jemal
A . Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
CA Cancer J Clin. 2018;68(6):394-424. doi:
10.3322/caac.21492PubMedGoogle ScholarCrossref 7.Abdelfatah
MM , Barakat
M , Lee
H ,
et al. The incidence of lymph node metastasis in early gastric cancer according to the expanded criteria in comparison with the absolute criteria of the Japanese Gastric Cancer Association: a systematic review of the literature and meta-analysis.
Gastrointest Endosc. 2018;87(2):338-347. doi:
10.1016/j.gie.2017.09.025PubMedGoogle ScholarCrossref 8.Kamarajah
SK , Markar
SR , Phillips
AW , Salti
GI , Dahdaleh
FS . Local endoscopic resection is inferior to gastrectomy for early clinical stage T1a and T1b gastric adenocarcinoma: a propensity-matched study.
Ann Surg Oncol. 2021;28(6):2992-2998. doi:
10.1245/s10434-020-09485-4PubMedGoogle ScholarCrossref 9.Manner
H , Rabenstein
T , May
A ,
et al. Long-term results of endoscopic resection in early gastric cancer: the Western experience.
Am J Gastroenterol. 2009;104(3):566-573.
PubMedGoogle Scholar 12.Smyth
EC , Verheij
M , Allum
W , Cunningham
D , Cervantes
A , Arnold
D ; ESMO Guidelines Committee. Gastric cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment, and follow-up.
Ann Oncol. 2016;27(suppl 5):v38-v49. doi:
10.1093/annonc/mdw350PubMedGoogle ScholarCrossref 14.Fukase
K , Kato
M , Kikuchi
S ,
et al; Japan Gast Study Group. Effect of eradication of
Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial.
Lancet. 2008;372(9636):392-397. doi:
10.1016/S0140-6736(08)61159-9PubMedGoogle ScholarCrossref 18.Miyashiro
I , Hiratsuka
M , Sasako
M ,
et al; Gastric Cancer Surgical Study Group (GCSSG) in the Japan Clinical Oncology Group (JCOG). High false-negative proportion of intraoperative histological examination as a serious problem for clinical application of sentinel node biopsy for early gastric cancer: final results of the Japan Clinical Oncology Group multicenter trial JCOG0302.
Gastric Cancer. 2014;17(2):316-323. doi:
10.1007/s10120-013-0285-3PubMedGoogle ScholarCrossref 20.Ryu
KW , Eom
BW , Nam
B-H ,
et al. Is the sentinel node biopsy clinically applicable for limited lymphadenectomy and modified gastric resection in gastric cancer? a meta-analysis of feasibility studies.
J Surg Oncol. 2011;104(6):578-584. doi:
10.1002/jso.21995PubMedGoogle ScholarCrossref 21.Park
JY , Kim
Y-W , Ryu
KW ,
et al. Assessment of laparoscopic stomach preserving surgery with sentinel basin dissection versus standard gastrectomy with lymphadenectomy in early gastric cancer—a multicenter randomized phase III clinical trial (SENORITA trial) protocol.
BMC Cancer. 2016;16:340. doi:
10.1186/s12885-016-2336-8PubMedGoogle ScholarCrossref 22.Slagter
AE , Jansen
EPM , van Laarhoven
HWM ,
et al. CRITICS-II: a multicentre randomised phase II trial of neo-adjuvant chemotherapy followed by surgery versus neo-adjuvant chemotherapy and subsequent chemoradiotherapy followed by surgery vs neoadjuvant chemoradiotherapy followed by surgery in resectable gastric cancer.
BMC Cancer. 2018;18(1):877. doi:
10.1186/s12885-018-4770-2PubMedGoogle ScholarCrossref 23.Leong
T , Smithers
BM , Haustermans
K ,
et al. TOPGEAR: a randomized, phase III trial of perioperative ECF chemotherapy with or without preoperative chemoradiation for resectable gastric cancer: interim results from an international, intergroup trial of the AGITG, TROG, EORTC, and CCTG.
Ann Surg Oncol. 2017;24(8):2252-2258. doi:
10.1245/s10434-017-5830-6PubMedGoogle ScholarCrossref 24.Cui
S-Z , Liang
H , Li
Y ,
et al; Chinese Peritoneal Oncology Study Group. PILGRIM: Phase III Clinical Trial in Evaluating the Role of Hyperthermic Intraperitoneal Chemotherapy for Locally Advanced Gastric Cancer Patients After Radical Gastrectomy With D2 Lymphadenectomy (HIPEC-01).
J Clin Oncol. 2020;38(15):4538. doi:
10.1200/JCO.2020.38.15_suppl.4538Google ScholarCrossref 25.Al-Batran
SE , Goetze
TO , Mueller
DW ,
et al. The RENAISSANCE (AIO-FLOT5) trial: effect of chemotherapy alone vs. chemotherapy followed by surgical resection on survival and quality of life in patients with limited-metastatic adenocarcinoma of the stomach or esophagogastric junction—a phase III trial of the German AIO/CAO-V/CAOGI.
BMC Cancer. 2017;17(1):893. doi:
10.1186/s12885-017-3918-9PubMedGoogle ScholarCrossref 27.Isozaki
H , Matsumoto
S , Murakami
S ,
et al. Diminished gastric resection preserves better quality of life in patients with early gastric cancer.
Acta Med Okayama. 2016;70(2):119-130.
PubMedGoogle Scholar 28.Abe
N , Takeuchi
H , Ohki
A ,
et al. Long-term outcomes of combination of endoscopic submucosal dissection and laparoscopic lymph node dissection without gastrectomy for early gastric cancer patients who have a potential risk of lymph node metastasis.
Gastrointest Endosc. 2011;74(4):792-797. doi:
10.1016/j.gie.2011.06.006PubMedGoogle ScholarCrossref 29.Zhao
L , Ling
R , Chen
J ,
et al. Clinical outcomes of proximal gastrectomy versus total gastrectomy for proximal gastric cancer: a systematic review and meta-analysis.
Dig Surg. 2021;38(1):1-13. doi:
10.1159/000506104PubMedGoogle ScholarCrossref 31.Cuschieri
A , Fayers
P , Fielding
J ,
et al. Postoperative morbidity and mortality after D1 and D2 resections for gastric cancer: preliminary results of the MRC randomised controlled surgical trial. the Surgical Cooperative Group.
Lancet. 1996;347(9007):995-999. doi:
10.1016/S0140-6736(96)90144-0PubMedGoogle ScholarCrossref 32.Cuschieri
A , Weeden
S , Fielding
J ,
et al; Surgical Co-operative Group. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial.
Br J Cancer. 1999;79(9-10):1522-1530. doi:
10.1038/sj.bjc.6690243PubMedGoogle ScholarCrossref 38.Sano
T , Sasako
M , Yamamoto
S ,
et al. Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy—Japan Clinical Oncology Group study 9501.
J Clin Oncol. 2004;22(14):2767-2773. doi:
10.1200/JCO.2004.10.184PubMedGoogle ScholarCrossref 39.Hyung
WJ , Yang
H-K , Park
Y-K ,
et al; Korean Laparoendoscopic Gastrointestinal Surgery Study Group. Long-term outcomes of laparoscopic distal gastrectomy for locally advanced gastric cancer: the KLASS-02-RCT randomized clinical trial.
J Clin Oncol. 2020;38(28):3304-3313. doi:
10.1200/JCO.20.01210PubMedGoogle ScholarCrossref 40.Kim
W , Kim
H-H , Han
S-U ,
et al; Korean Laparo-endoscopic Gastrointestinal Surgery Study (KLASS) Group. Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric cancer: short-term outcomes from a multicenter randomized controlled trial (KLASS-01).
Ann Surg. 2016;263(1):28-35. doi:
10.1097/SLA.0000000000001346PubMedGoogle ScholarCrossref 41.Yu
J , Huang
C , Sun
Y ,
et al; Chinese Laparoscopic Gastrointestinal Surgery Study (CLASS) Group. 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. 2019;321(20):1983-1992. doi:
10.1001/jama.2019.5359PubMedGoogle ScholarCrossref 43.van der Veen
A , Brenkman
HJF , Seesing
MFJ ,
et al; LOGICA Study Group. Laparoscopic Versus Open Gastrectomy for Gastric Cancer (LOGICA): a multicenter randomized clinical trial.
J Clin Oncol. 2021;39(9):978-989. doi:
10.1200/JCO.20.01540PubMedGoogle ScholarCrossref 47.Li
Z-Y , Zhou
Y-B , Li
T-Y ,
et al; Robotic, Laparoscopic Surgery Committee of Chinese Research Hospital Association. Robotic gastrectomy vs laparoscopic gastrectomy for gastric cancer: a multicenter cohort study of 5402 patients in China.
Ann Surg. 2021. doi:
10.1097/SLA.0000000000005046PubMedGoogle ScholarCrossref 51.Al-Batran
SE , Homann
N , Pauligk
C ,
et al; FLOT4-AIO Investigators. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial.
Lancet. 2019;393(10184):1948-1957. doi:
10.1016/S0140-6736(18)32557-1PubMedGoogle ScholarCrossref 52.Cats
A , Jansen
EPM , van Grieken
NCT ,
et al; CRITICS investigators. Chemotherapy vs chemoradiotherapy after surgery and preoperative chemotherapy for resectable gastric cancer (CRITICS): an international, open-label, randomised phase 3 trial.
Lancet Oncol. 2018;19(5):616-628. doi:
10.1016/S1470-2045(18)30132-3PubMedGoogle ScholarCrossref 53.Rivera
F , Izquierdo-Manuel
M , García-Alfonso
P ,
et al. Perioperative trastuzumab, capecitabine and oxaliplatin in patients with
HER2-positive resectable gastric or gastro-oesophageal junction adenocarcinoma: NEOHX phase II trial.
Eur J Cancer. 2021;145:158-167. doi:
10.1016/j.ejca.2020.12.005PubMedGoogle ScholarCrossref 54.Shitara
K , Van Cutsem
E , Bang
YJ ,
et al. Efficacy and safety of pembrolizumab or pembrolizumab plus chemotherapy vs chemotherapy alone for patients with first-line, advanced gastric cancer: the KEYNOTE-062 phase 3 randomized clinical trial.
JAMA Oncol. 2020;6(10):1571-1580. doi:
10.1001/jamaoncol.2020.3370PubMedGoogle ScholarCrossref 55.Ajani
JA , Winter
K , Okawara
GS ,
et al. Phase II trial of preoperative chemoradiation in patients with localized gastric adenocarcinoma (RTOG 9904): quality of combined modality therapy and pathologic response.
J Clin Oncol. 2006;24(24):3953-3958. doi:
10.1200/JCO.2006.06.4840PubMedGoogle ScholarCrossref 56.Bang
Y-J , Kim
Y-W , Yang
H-K ,
et al; CLASSIC trial investigators. Adjuvant capecitabine and oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): a phase 3 open-label, randomised controlled trial.
Lancet. 2012;379(9813):315-321. doi:
10.1016/S0140-6736(11)61873-4PubMedGoogle ScholarCrossref 57.Noh
SH , Park
SR , Yang
H-K ,
et al; CLASSIC trial investigators. Adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): 5-year follow-up of an open-label, randomised phase 3 trial.
Lancet Oncol. 2014;15(12):1389-1396. doi:
10.1016/S1470-2045(14)70473-5PubMedGoogle ScholarCrossref 58.Sasako
M , Sakuramoto
S , Katai
H ,
et al. Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 vs surgery alone in stage II or III gastric cancer.
J Clin Oncol. 2011;29(33):4387-4393. doi:
10.1200/JCO.2011.36.5908PubMedGoogle ScholarCrossref 59.Macdonald
JS , Smalley
SR , Benedetti
J ,
et al. Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction.
N Engl J Med. 2001;345(10):725-730. doi:
10.1056/NEJMoa010187PubMedGoogle ScholarCrossref 60.Park
SH , Sohn
TS , Lee
J ,
et al. Phase III trial to compare adjuvant chemotherapy with capecitabine and cisplatin vs concurrent chemoradiotherapy in gastric cancer: final report of the adjuvant chemoradiotherapy in stomach tumors trial, including survival and subset analyses.
J Clin Oncol. 2015;33(28):3130-3136. doi:
10.1200/JCO.2014.58.3930PubMedGoogle ScholarCrossref 61.Park
SH , Lim
DH , Sohn
TS ,
et al; ARTIST 2 investigators. A randomized phase III trial comparing adjuvant single-agent S1, S-1 with oxaliplatin, and postoperative chemoradiation with S-1 and oxaliplatin in patients with node-positive gastric cancer after D2 resection: the ARTIST 2 trial.
Ann Oncol. 2021;32(3):368-374. doi:
10.1016/j.annonc.2020.11.017PubMedGoogle ScholarCrossref 62.Yang
TS , Wang
XF , Fairweather
M , Sun
YH , Mamon
HJ , Wang
JP . The survival benefit from the addition of radiation to chemotherapy in gastric cancer patients following surgical resection.
Clin Oncol (R Coll Radiol). 2020;32(2):110-120. doi:
10.1016/j.clon.2019.09.047PubMedGoogle ScholarCrossref 64.Al-Batran
SE , Homann
N , Pauligk
C ,
et al. Effect of neoadjuvant chemotherapy followed by surgical resection on survival in patients with limited metastatic gastric or gastroesophageal junction cancer: the AIO-FLOT3 trial.
JAMA Oncol. 2017;3(9):1237-1244. doi:
10.1001/jamaoncol.2017.0515PubMedGoogle ScholarCrossref 65.Terashima
M , Yoshida
K , Rha
SY ,
et al. International retrospective cohort study of conversion therapy for stage IV gastric cancer 1 (CONVO-GC-1).
Ann Gastroenterol Surg. Published online October 20, 2021. doi:
10.1002/ags3.12515Google ScholarCrossref 67.Bonnot
PE , Piessen
G , Kepenekian
V ,
et al; FREGAT and BIG-RENAPE Networks. Cytoreductive Surgery With or Without Hyperthermic Intraperitoneal Chemotherapy for Gastric Cancer With Peritoneal Metastases (CYTO-CHIP study): a propensity score analysis.
J Clin Oncol. 2019;37(23):2028-2040. doi:
10.1200/JCO.18.01688PubMedGoogle ScholarCrossref 68.Yang
X-J , Huang
C-Q , Suo
T ,
et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy improves survival of patients with peritoneal carcinomatosis from gastric cancer: final results of a phase III randomized clinical trial.
Ann Surg Oncol. 2011;18(6):1575-1581. doi:
10.1245/s10434-011-1631-5PubMedGoogle ScholarCrossref 69.Mezhir
JJ , Shah
MA , Jacks
LM , Brennan
MF , Coit
DG , Strong
VE . Positive peritoneal cytology in patients with gastric cancer: natural history and outcome of 291 patients.
Ann Surg Oncol. 2010;17(12):3173-3180. doi:
10.1245/s10434-010-1183-0PubMedGoogle ScholarCrossref 70.Badgwell
B , Cormier
JN , Krishnan
S ,
et al. Does neoadjuvant treatment for gastric cancer patients with positive peritoneal cytology at staging laparoscopy improve survival?
Ann Surg Oncol. 2008;15(10):2684-2691. doi:
10.1245/s10434-008-0055-3PubMedGoogle ScholarCrossref 71.Okabe
H , Ueda
S , Obama
K , Hosogi
H , Sakai
Y . Induction chemotherapy with S-1 plus cisplatin followed by surgery for treatment of gastric cancer with peritoneal dissemination.
Ann Surg Oncol. 2009;16(12):3227-3236. doi:
10.1245/s10434-009-0706-zPubMedGoogle ScholarCrossref 72.Badgwell
B , Blum
M , Das
P ,
et al. Phase II trial of laparoscopic hyperthermic intraperitoneal chemoperfusion for peritoneal carcinomatosis or positive peritoneal cytology in patients with gastric adenocarcinoma.
Ann Surg Oncol. 2017;24(11):3338-3344. doi:
10.1245/s10434-017-6047-4PubMedGoogle ScholarCrossref 73.Marutsuka
T , Shimada
S , Shiomori
K ,
et al. 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. 2003;9(2):678-685.
PubMedGoogle Scholar 75.Fujitani
K , Yang
H-K , Mizusawa
J ,
et al; REGATTA study investigators. Gastrectomy plus chemotherapy versus chemotherapy alone for advanced gastric cancer with a single non-curable factor (REGATTA): a phase 3, randomised controlled trial.
Lancet Oncol. 2016;17(3):309-318. doi:
10.1016/S1470-2045(15)00553-7PubMedGoogle ScholarCrossref 78.Jeurnink
SM , van Eijck
CH , Steyerberg
EW , Kuipers
EJ , Siersema
PD . Stent versus gastrojejunostomy for the palliation of gastric outlet obstruction: a systematic review.
BMC Gastroenterol. 2007;7:18. doi:
10.1186/1471-230X-7-18PubMedGoogle ScholarCrossref