Updates on Management of Gastric Cancer

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LAURÉN P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Pathol Microbiol Scand. 1965;64(1):31–49. https://doi.org/10.1111/apm.1965.64.1.31 .

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Bass AJ, Thorsson V, Shmulevich I, et al. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513(7517):202–9. https://doi.org/10.1038/nature13480 .

Cristescu R, Lee J, Nebozhyn M, Kim KM, Ting JC, Wong SS, et al. Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med. 2015;21(5):449–56. https://doi.org/10.1038/nm.3850 .

Fonkoua LK, Yee NS. Biomedicines molecular characterization of gastric carcinoma: therapeutic implications for biomarkers and targets. doi: https://doi.org/10.3390/biomedicines6010032 , 2018.

Leake P-A, Cardoso R, Seevaratnam R, Lourenco L, Helyer L, Mahar A, et al. A systematic review of the accuracy and indications for diagnostic laparoscopy prior to curative-intent resection of gastric cancer. Gastric Cancer. 2012;15(S1):38–47. https://doi.org/10.1007/s10120-011-0047-z .

Amin MB, Edge SB, American Joint Committee on Cancer. AJCC Cancer Staging Manual. https://www.springer.com/us/book/9783319406176 . Accessed February 25, 2019. The 8 th edition AJCC Cancer Staging Manual for gastric cancer is integral for clinical practice. It has been updated with evidence-based clinical and post-neoadjuvant staging systems for facilitation of initial treatment plan recommendations.

Shu P, Qin J, Shen K, Chen W, Liu F, Fang Y, et al. The IGCA staging system is more accurate than AJCC7 system in stratifying survival of patients with gastric cancer in stage III. BMC Cancer. 2017;17(1):238. https://doi.org/10.1186/s12885-017-3235-3 .

Mocellin S, Pasquali S. Diagnostic accuracy of endoscopic ultrasonography (EUS) for the preoperative locoregional staging of primary gastric cancer. Cochrane Database Syst Rev. 2015;2:CD009944. https://doi.org/10.1002/14651858.CD009944.pub2 .

Puli S-R, Reddy J-B, Bechtold M-L, Antillon D, Ibdah J-A, Antillon M-R. Staging accuracy of esophageal cancer by endoscopic ultrasound: a meta-analysis and systematic review. World J Gastroenterol 2008;14(10):1479–1490. http://www.ncbi.nlm.nih.gov/pubmed/18330935 . Accessed March 6, 2019.

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Lisa Gurski N, McMillian N, Lenora Pluchino MA, et al. NCCN Guidelines Version 2.2018 Panel Members Gastric Cancer.; 2019. https://www.nccn.org/professionals/physician_gls/pdf/gastric.pdf . Accessed February 26, 2019. The NCCN Guidelines for gastric cancer are comprehensive, evidence-based, and frequently updated. They are compiled and published by a panel of experts in the field.

De Andrade JP, Mezhir JJ. The critical role of peritoneal cytology in the staging of gastric cancer: an evidence-based review. J Surg Oncol. 2014;110(3):291–7. https://doi.org/10.1002/jso.23632 .

The general rules for The gastric cancer study in surgery. Jpn J Surg. 1973;3(1):61–71. http://www.ncbi.nlm.nih.gov/pubmed/4803902 . Accessed February 26, 2019.

Songun I, Putter H, Kranenbarg EM-K, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11(5):439–49. https://doi.org/10.1016/S1470-2045(10)70070-X .

Mocellin S, McCulloch P, Kazi H, Gama-Rodrigues JJ, Yuan Y, Nitti D. Extent of lymph node dissection for adenocarcinoma of the stomach. Cochrane Database Syst Rev. 2015;8:CD001964. https://doi.org/10.1002/14651858.CD001964.pub4 .

Fujimura T, Nakamura K, Oyama K, et al. Selective lymphadenectomy of Para-aortic lymph nodes for advanced gastric cancer. Oncol Rep 2009;22(3):509–514. http://www.ncbi.nlm.nih.gov/pubmed/19639196 . Accessed February 26, 2019.

Schwarz RE, Smith DD. Clinical impact of lymphadenectomy extent in resectable gastric cancer of advanced stage. Ann Surg Oncol. 2007;14(2):317–28. https://doi.org/10.1245/s10434-006-9218-2 .

Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 1994;4(2):146–148. http://www.ncbi.nlm.nih.gov/pubmed/8180768 . Accessed February 26, 2019.

Hashizume M, Sugimachi K. Robot-assisted gastric surgery. Surg Clin North Am. 2003;83(6):1429–44. https://doi.org/10.1016/S0039-6109(03)00158-0 .

Huscher CGS, Mingoli A, Sgarzini G, Sansonetti A, di Paola M, Recher A, Ponzano C Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 2005;241(2):232–237. http://www.ncbi.nlm.nih.gov/pubmed/15650632 . Accessed February 28, 2019.

Soetikno R, Kaltenbach T, Yeh R, Gotoda T. Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol. 2005;23(20):4490–8. https://doi.org/10.1200/JCO.2005.19.935 .

Lian J, Chen S, Zhang Y, Qiu F. A meta-analysis of endoscopic submucosal dissection and EMR for early gastric cancer. Gastrointest Endosc. 2012;76(4):763–70. https://doi.org/10.1016/j.gie.2012.06.014 .

Facciorusso A, Antonino M, Di Maso M, Muscatiello N. Endoscopic submucosal dissection vs endoscopic mucosal resection for early gastric cancer: a meta-analysis. World J Gastrointest Endosc. 2014;6(11):555–63. https://doi.org/10.4253/wjge.v6.i11.555 .

Wagner AD, Syn NL, Moehler M, et al. Chemotherapy for advanced gastric cancer. Cochrane Database Syst Rev. 2017;8. https://doi.org/10.1002/14651858.CD004064.pub4 .

Hall J, Loggie BW, Shen P, et al. Cytoreductive surgery with intraperitoneal hyperthermic chemotherapy for advanced gastric cancer. J Gastrointest Surg. 2004;8(4):454–63. https://doi.org/10.1016/j.gassur.2003.12.014 .

Glehen O, Gilly FN, Arvieux C, et al. Peritoneal Carcinomatosis from gastric cancer: a multi-institutional study of 159 patients treated by cytoreductive surgery combined with perioperative intraperitoneal chemotherapy. Ann Surg Oncol. 2010;17(9):2370–7. https://doi.org/10.1245/s10434-010-1039-7 .

Gill RS, Al-Adra DP, Nagendran J, et al. Treatment of gastric cancer with peritoneal carcinomatosis by cytoreductive surgery and HIPEC: a systematic review of survival, mortality, and morbidity. J Surg Oncol. 2011;104(6):692–8. https://doi.org/10.1002/jso.22017 .

Bonnot PE, Piessen G, Pocard M, Meunier B, Bereder JM, Abboud K, et al. CYTO-CHIP: cytoreductive surgery versus cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for gastric cancer with peritoneal metastasis: a propensity-score analysis from BIG RENAPE and FREGAT working groups. J Clin Oncol. 2018;36(4_suppl):8–8. https://doi.org/10.1200/JCO.2018.36.4_suppl.8 . The CYTO-CHIP analysis data has only recently been reported, and provides evidence of survival benefit of cytoreductive surgery plus HIPEC in gastric cancer in patients with evidence of peritoneal disease.

Desiderio J, Chao J, Melstrom L, Warner S, Tozzi F, Fong Y, et al. The 30-year experience—a meta-analysis of randomised and high-quality non-randomised studies of hyperthermic intraperitoneal chemotherapy in the treatment of gastric cancer. Eur J Cancer. 2017;79:1–14. https://doi.org/10.1016/j.ejca.2017.03.030 .

Cunningham D, Allum WH, Stenning SP, Thompson JN, van de Velde C, Nicolson M, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20. https://doi.org/10.1056/NEJMoa055531 .

Al-Batran S-E, Homann N, Schmalenberg H, et al. Perioperative chemotherapy with docetaxel, oxaliplatin, and fluorouracil/leucovorin (FLOT) versus epirubicin, cisplatin, and fluorouracil or capecitabine (ECF/ECX) for resectable gastric or gastroesophageal junction (GEJ) adenocarcinoma (FLOT4-AIO): a multicenter, randomized phase 3 trial. J Clin Oncol. 2017;35(15_suppl):4004–4. https://doi.org/10.1200/JCO.2017.35.15_suppl.4004 The FLOT regimen recently showed improved survival over previous chemotherapy regimens in the perioperative setting. This has caused a dramatic change in the chemotherapeutic treatment of gastric cancer over a brief period of time.

Moertel C, Reitemeier R, Childs D, Colby M, Holbrook M. Combined 5-fluorouracil and SUPERVOLTAGE radiation therapy of locally UNRESECTABLE gastrointestinal cancer. Lancet. 1969;294(7626):865–7. https://doi.org/10.1016/S0140-6736(69)92326-5 .

Gastrointestinal Tumor Study Group. A comparison of combination chemotherapy and combined modality therapy for locally advanced gastric carcinoma. Cancer. 1982;49(9):1771–7 http://www.ncbi.nlm.nih.gov/pubmed/6176313 . Accessed February 28, 2019.

Smalley SR, Benedetti JK, Haller DG, Hundahl SA, Estes NC, Ajani JA, et al. Updated analysis of SWOG-directed intergroup study 0116: a phase III trial of adjuvant radiochemotherapy versus observation after curative gastric cancer resection. J Clin Oncol. 2012;30(19):2327–33. https://doi.org/10.1200/JCO.2011.36.7136 .

Cats A, Jansen EPM, van Grieken NCT, Sikorska K, Lind P, Nordsmark M, et al. Chemotherapy versus chemoradiotherapy after surgery and preoperative chemotherapy for resectable gastric cancer (CRITICS): an international, open-label, randomised phase 3 trial. Lancet Oncol. 2018;19(5):616–28. https://doi.org/10.1016/S1470-2045(18)30132-3 .

Leong T, Smithers BM, Haustermans K, Michael M, Gebski V, Miller D, 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):2252–8. https://doi.org/10.1245/s10434-017-5830-6 .

Lee J, Lim DH, Kim S, Park SH, Park JO, Park YS, et al. Phase III trial comparing capecitabine plus cisplatin versus capecitabine plus cisplatin with concurrent capecitabine radiotherapy in completely resected gastric cancer with D2 lymph node dissection: the ARTIST trial. J Clin Oncol. 2012;30(3):268–73. https://doi.org/10.1200/JCO.2011.39.1953 .

Park SH, Lee SJ, Kim ST, Lee J, Park JO, Park YS, et al. Multicenter phase III trial of adjuvant chemoradiotherapy in stomach tumors 2 (ARTIST 2). J Clin Oncol. 2015;33(3_suppl:TPS228–8. https://doi.org/10.1200/jco.2015.33.3_suppl.tps228 .

van Hagen P, Hulshof MCCM, van Lanschot JJB, Steyerberg EW, Henegouwen MIB, Wijnhoven BPL, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366(22):2074–84. https://doi.org/10.1056/NEJMoa1112088 .

Hoeppner J, Lordick F, Brunner T, Glatz T, Bronsert P, Röthling N, et al. ESOPEC: prospective randomized controlled multicenter phase III trial comparing perioperative chemotherapy (FLOT protocol) to neoadjuvant chemoradiation (CROSS protocol) in patients with adenocarcinoma of the esophagus (NCT02509286). BMC Cancer. 2016;16(1):503. https://doi.org/10.1186/s12885-016-2564-y .

Gravalos C, Jimeno A. HER2 in gastric cancer: a new prognostic factor and a novel therapeutic target. Ann Oncol. 2008;19(9):1523–9. https://doi.org/10.1093/annonc/mdn169 .

Bang Y-J, Van Cutsem E, Feyereislova A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet (London, England). 2010;376(9742):687–97. https://doi.org/10.1016/S0140-6736(10)61121-X .

Satoh T, Lee KH, Rha SY, Sasaki Y, Park SH, Komatsu Y, et al. Randomized phase II trial of nimotuzumab plus irinotecan versus irinotecan alone as second-line therapy for patients with advanced gastric cancer. Gastric Cancer. 2015;18(4):824–32. https://doi.org/10.1007/s10120-014-0420-9 .

Fuchs CS, Tomasek J, Yong CJ, Dumitru F, Passalacqua R, Goswami C, et al. Ramucirumab monotherapy for previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (REGARD): an international, randomised, multicentre, placebo-controlled, phase 3 trial. Lancet (London, England). 2014;383(9911):31–9. https://doi.org/10.1016/S0140-6736(13)61719-5 .

Wilke H, Muro K, Van Cutsem E, et al. Ramucirumab plus paclitaxel versus placebo plus paclitaxel in patients with previously treated advanced gastric or gastro-oesophageal junction adenocarcinoma (RAINBOW): a double-blind, randomised phase 3 trial. Lancet Oncol. 2014;15(11):1224–35. https://doi.org/10.1016/S1470-2045(14)70420-6 .

Kang Y-K, Boku N, Satoh T, Ryu MH, Chao Y, Kato K, et al. Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet (London, England). 2017;390(10111):2461–71. https://doi.org/10.1016/S0140-6736(17)31827-5 .

Muro K, Chung HC, Shankaran V, Geva R, Catenacci D, Gupta S, et al. Pembrolizumab for patients with PD-L1-positive advanced gastric cancer (KEYNOTE-012): a multicentre, open-label, phase 1b trial. Lancet Oncol. 2016;17(6):717–26. https://doi.org/10.1016/S1470-2045(16)00175-3 .

Bang Y-J, Cho JY, Kim YH, Kim JW, di Bartolomeo M, Ajani JA, et al. Efficacy of sequential ipilimumab monotherapy versus best supportive care for unresectable locally advanced/metastatic gastric or gastroesophageal junction cancer. Clin Cancer Res. 2017;23(19):5671–8. https://doi.org/10.1158/1078-0432.CCR-17-0025 .

Janjigian YY, Bendell J, Calvo E, Kim JW, Ascierto PA, Sharma P, et al. CheckMate-032 study: efficacy and safety of Nivolumab and Nivolumab plus Ipilimumab in patients with metastatic Esophagogastric Cancer. J Clin Oncol. 2018;36(28):2836–44. https://doi.org/10.1200/JCO.2017.76.6212 .

Moehler M, Ryu M-H, Dvorkin M, Lee KW, Coşkun HŞ, Wong R, et al. Maintenance avelumab versus continuation of first-line chemotherapy in gastric cancer: JAVELIN gastric 100 study design. Future Oncol. 2019;15(6):567–77. https://doi.org/10.2217/fon-2018-0668 .

Bang Y-J, Ruiz EY, Van Cutsem E, et al. Phase III, randomised trial of avelumab versus physician’s choice of chemotherapy as third-line treatment of patients with advanced gastric or gastro-oesophageal junction cancer: primary analysis of JAVELIN Gastric 300. Ann Oncol. 2018;29(10):2052–60. https://doi.org/10.1093/annonc/mdy264 .