Surgical treatment of stage IV gastric cancer: is it worthwhile?

Abstract

Aim: To analyze clinical features and survival outcomes of patients with surgically-treated stage IV gastric cancer, in order to evaluate the suitability of surgery in these patients.

Methods: We performed a systematic literature search using PubMed, MEDLINE, and Embase on October 9th, 2017. Survival outcomes data were collected.

Results: The original search returned 2434 papers. Thirty-nine studies were included in the final review, of which 26 evaluated liver metastasis resection, four pulmonary metastasis resections and nine palliative gastrectomies. In total 933 patients underwent hepatectomy for liver metastasis from gastric cancer and median survival rates were 73%, 37% and 27% at 1-, 3- and 5-year respectively, with a median overall survival of 22 months (9-52 months). Data regarding resection of lung metastases were scarce and extremely heterogeneous. In total 1115 patients underwent palliative gastrectomy and median overall survival of patients was 12 months (8-53 months). In the only randomized controlled trial, no survival benefit of additional gastrectomy over chemotherapy alone was found, in contrast with the retrospective studies.

Conclusion: Survival benefit of surgery in advanced gastric cancer is still unclear. Surgery may play an important role in highly selected patients. However, further randomized controlled trials are necessary to clarify the actual impact of surgery in these patients.

Keywords

Gastric cancer / metastasis / surgical treatment

References

[1] Blot WJ,Kneller RW FJJ.Rising incidence of adenocarcinoma of the esophagus and gastric cardia.JAMA1991;265:1287-9

[2] Siegel R,Jemal A.Cancer statistics, 2017.CA Cancer J Clin2017;67:7-30

[3] National Cancer Institute - Surveillance, Epidemiology, and End Results Program. SEER*Stat Databases: November 2015 Submission. Available from: https://seer.cancer.gov/data/seerstat/nov2015/. [Last accessed on 27 Feb 2018].

[4] Shin A,Park S.Gastric cancer epidemiology in Korea.J Gastric Cancer2011;11:135-40 PMCID:PMC3204471

[5] Kemp CD,Kerkar S,Marquardt JU,Avital I.Pulmonary resection for metastatic gastric cancer.J Thorac Oncol2010;5:1796-805

[6] Spolverato G,Kim Y,Poultsides GA,Schmidt C,Votanopoulos K,Pawlik TM.Rates and patterns of recurrence after curative intent resection for gastric cancer: a United States multi-institutional analysis.J Am Coll Surg2014;219:664-75

[7] Deng J,Wang D,Pan Y.Investigation of the recurrence patterns of gastric cancer following a curative resection.Surg Today2011;41:210-5

[8] Nio Y,Omori H,Itakura M,Higami T.A randomized consent design trial of neoadjuvant chemotherapy with tegafur plus uracil (UFT) for gastric cancer - a single institute study.Anticancer Res2004;24:1879-87

[9] Kodera Y.Japanese gastric cancer treatment guidelines 2014 (ver.4). Gastric Cancer2017;20:1-19 PMCID:PMC5215069

[10] Ajani JA,Almhanna K,Chao J,Denlinger CS,Farjah F,Gerdes H,Glasgow RE,Hochwald S,Ilson DH,Johung KL,Kleinberg LR,Leong S,Lockhart AC,Mulcahy MF,Perry KA,Scott WJ,Washington MK,Willett CG,Zelman D,Sundar H.Gastric Cancer, Version 3.2016, NCCN Clinical Practice Guidelines in Oncology.J Natl Compr Canc Netw2016;14:1286-312

[11] Kodera Y,Fukushima N,Muro K,Yoshikawa T,Tanaka C.Surgical resection of hepatic metastasis from gastric cancer: a review and new recommendation in the Japanese gastric cancer treatment guidelines.Gastric Cancer2014;17:206-12

[12] AJCC..Cancer Staging Manual, 7th edition.New York: Springer-Verlag;2010;

[13] AJCC..Cancer Staging Manual, 8th edition.New York: Springer-Verlag;2016;

[14] AJCC..Cancer Staging Manual, 6th edition.New York: Springer-Verlag;2003;

[15] Sano T.Japanese classification of gastric carcinoma: 3rd English edition.Gastric Cancer2011;14:101-12

[16] Bosman FT,Hruban RH.WHO classification of tumours of the digestive system.Lyon: IARC Press;2010;

[17] Hu B,Sittler S,Barnes R.Gastric cancer: classification, histology and application of molecular pathology.J Gastrointest Oncol2012;3:251-61 PMCID:PMC3418539

[18] Baek HU,Cho EH,Yu HJ,Bang HY.Hepatic resection for hepatic metastases from gastric adenocarcinoma.J Gastric Cancer2013;13:86-92 PMCID:PMC3705137

[19] Chen L,Lin HZ,Jiang XJ,Chen YX.Chemotherapy and resection for gastric cancer with synchronous liver metastases.World J Gastroenterol2013;19:2097-103 PMCID:PMC3623989

[20] Cheon SH,Jeung HC,Kim SH,Ahn JB,Noh SH.Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases.Ann Oncol2008;19:1146-53

[21] Dittmar Y,Rauchfuss F,Scheuerlein H,Settmacher U.Resection of liver metastases is beneficial in patients with gastric cancer: report on 15 cases and review of literature.Gastric Cancer2012;15:131-6

[22] Garancini M,Degrate L,Gianotti L,Uggeri F.Surgical treatment of liver metastases of gastric cancer: is local treatment in a systemic disease worthwhile?.HPB2012;14:209-15 PMCID:PMC3371204

[23] Kinoshita T,Saiura A,Sakamoto H.Multicentre analysis of long-term outcome after surgical resection for gastric cancer liver metastases.Br J Surg2015;102:102-7

[24] Koga R,Ohyama S,Seki M,Yamaguchi T.Liver resection for metastatic gastric cancer: Experience with 42 patients including eight long-term survivors.Jpn J Clin Oncol2007;37:836-42

[25] Komeda K,Kubo S,Nakai T,Wada H,Kinoshita M,Matsumoto M,Inoue Y,Kwon AH.High survival in patients operated for small isolated liver metastases from gastric cancer: a multi-institutional study.World J Surg2014;38:2692-7

[26] Li S,Hung C,Chen J.Surgical resection of metachronous hepatic metastases from gastric cancer improves long-term survival: a population-based study.PLoS One2017;12:1-10

[27] Liu J,Zhai RJ,Shao MZ.Predictive factors improving survival after gastric and hepatic surgical treatment in gastric cancer patients with synchronous liver metastases.Chin Med J2012;125:165-71

[28] Makino H,Izumisawa Y,Oshima T,Fujii S,Takagawa R,Ono HA,Tanaka K.Indication for hepatic resection in the treatment of liver metastasis from gastric cancer.Anticancer Res2010;30:2367-76

[29] Miki Y,Hirao M,Mano M,Miyamoto A,Tsujinaka T.Significance of surgical treatment of liver metastases from gastric cancer.Anticancer Res2012;32:665-70

[30] Morise Z,Hoshimoto S,Ikeda M,Horiguchi A.The role of hepatectomy for patients with liver metastases of gastric cancer.Hepatogastroenterology2008;55:1238-4

[31] Nomura T,Takasu N,Takeshita A,Hachiya O,Kimura W.Intrahepatic micrometastases around liver metastases from gastric cancer.J Hepatobiliary Pancreat Surg2009;16:493-501

[32] Qiu JL,Li W,Li BK,Lao XM,Yuan YF.Hepatic resection for synchronous hepatic metastasis from gastric cancer.Eur J Surg Oncol2013;39:694-700

[33] Roh H,Lee H,Choe K.Outcome of hepatic resection for metastatic gastric cancer.Am Surg2005;71:95-9

[34] Sakamoto Y,Yamamoto J,Seki M,Kokudo N,Muto T.Surgical resection of liver metastases of gastric cancer: an analysis of a 17-year experience with 22 patients.Surgery2003;133:507-11

[35] Sakamoto Y,Shimada K,Saka M,Katai H,Sasako M.Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer.J Surg Oncol2007;95:534-9

[36] Takemura N,Koga R,Yoshioka R,Hiki N,Yamamoto J,Yamaguchi T.Long-term outcomes after surgical resection for gastric cancer liver metastasis: an analysis of 64 macroscopically complete resections.Langenbecks Arch Surg2012;397:951-7

[37] Thelen A,Benckert C,Neumann U,Schumacher G.Liver resection for metastatic gastric cancer.Eur J Surg Oncol2008;34:1328-34

[38] Tiberio GAM,Morgagni P,Marchet A,Graziosi L,Vittimberga G,Nitti D,Coniglio A.Gastric cancer and synchronous hepatic metastases: is it possible to recognize candidates to R0 resection?.Ann Surg Oncol2015;22:589-96

[39] Tsujimoto H,Ono S,Hiraki S,Yaguchi Y,Yamamoto J.Outcomes for patients following hepatic resection of metastatic tumors from gastric cancer.Hepatol Int2010;4:406-13 PMCID:PMC2836442

[40] Viganò L,Ferrero A,Nuzzo G.Liver resection for gastric cancer metastases.Hepatogastroenterology2013;60:557-62

[41] Wang YN,Ling JQ,Hou YY,Qin J,Qin XY.Prognostic analysis of combined curative resection of the stomach and liver lesions in 30 gastric cancer patients with synchronous liver metastases.BMC Surg2012;12:20 PMCID:PMC3607939

[42] Wang W,Zhang H,Xue Q.Prognostic significance of radical surgical treatment for gastric cancer patients with synchronous liver metastases.Med Oncol2014;31:1-8

[43] Zacherl J,Scheuba C,Wenzl E,Jakesz R.Analysis of hepatic resection of metastasis originating from gastric adenocarcinoma.J Gastrointest Surg2002;6:682-9

[44] Shiono S,Horio H,Matsuguma H,Nakajima J.Outcomes and prognostic factors of survival after pulmonary resection for metastatic gastric cancer.Eur J Cardiothorac Surg2013;43:e13-6

[45] Yoshida Y,Yoneda S,Inada K.Ten cases of resected solitary pulmonary metastases arising from gastric cancer.Asian Cardiovasc Thorac Ann2013;22:578-82

[46] Iijima Y,Atari M,Nakajima Y,Uramoto H.Pulmonary resection for metastatic gastric cancer.Ann Thorac Cardiovasc Surg2016;22:230-6 PMCID:PMC5045850

[47] Kobayashi Y,Ito S,Ito S,Mitsudomi T.Pulmonary metastasectomy for gastric cancer: a 13-year single-institution experience.Surg Today2013;43:1382-9

[48] Li C,Chen J,Zhu ZG,Lin YZ.Survival benefit of non-curative gastrectomy for gastric cancer patients with synchronous distant metastasis.J Gastrointest Surg2010;14:282-8

[49] Ko KJ,Yoo HM,Jeon HM,Jeon DJ.The clinical value of non-curative resection followed by chemotherapy for incurable gastric cancer.World J Surg2012;36:1800-5

[50] Hartgrink HH,Klein Kranenbarg E,van de Velde CJH.Value of palliative resection in gastric cancer.Br J Surg2002;89:1438-43

[51] Saidi RF,Dudrick PS.Is there a role for palliative gastrectomy in patients with stage IV gastric cancer?.World J Surg2006;30:21-7

[52] Kokkola A,Puolakkainen P.Does non-curative gastrectomy improve survival in patients with metastatic gastric cancer?.J Surg Oncol2012;106:193-6

[53] Samarasam I,Sitaram V,Nair A.Palliative gastrectomy in advanced gastric cancer: is it worthwhile?.ANZ J Surg2006;76:60-3

[54] Lin SZ,You T,Wu WJ,Zhang W,Li CM,Xu JR.Palliative gastrectomy and chemotherapy for stage IV gastric cancer.J Cancer Res Clin Oncol2008;134:187-92

[55] Sougioultzis S,Xynos ID,Kosmas C,Dokou A,Zografos G,Papalambros E.Palliative gastrectomy and other factors affecting overall survival in stage IV gastric adenocarcinoma patients receiving chemotherapy: a retrospective analysis.Eur J Surg Oncol2011;37:312-8

[56] Funakoshi T,Boku N,Yamazaki K,Todaka A,Yokota T,Kenmotsu H.Clinicopathological features and outcomes of gastric cancer patients with pulmonary lymphangitis carcinomatosa.Jpn J Clin Oncol2014;44:792-8

[57] Thomford NR,Clagett OT.The surgical treatment of metastatic tumors in the lungs.J Thorac Cardiovasc Surg1965;49:357-63

[58] Fujitani K,Mizusawa J,Terashima M,Iwasaki Y,Takagane A,Yoshikawa T,Nakamura K,Kurokawa Y,Park BJ,Tsujinaka T16.Gastrectomy plus chemotherapy versus chemotherapy alone for advanced gastric cancer with a single non-curable factor (REGATTA): a phase 3, randomised controlled trial.Lancet Oncol2016;17:309-18

[59] Waddell T,Cunningham D,Frances A,Wotherspoon A,Middleton G,Ferry D,Crosby T,Smith D,Iveson T,Slater S,Barbachano Y.Epirubicin, oxaliplatin, and capecitabine with or without panitumumab for patients with previously untreated advanced oesophagogastric cancer (REAL3): a randomised, open-label phase 3 trial.Lancet Oncol2013;14:481-9

[60] Bang YJ,Feyereislova A,Shen L,Lordick F,Omuro Y,Aprile G,Hill J,Rüschoff J.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.Lancet2010;376:687-97

[61] Liao YY,Long D,Zhang S,Li LQ.Hepatectomy for liver metastases from gastric cancer: a systematic review.BMC Surg2017;17:14 PMCID:PMC5307809

[62] Sun J,Wang Z,Gao P,Zhou B.Clinical significance of palliative gastrectomy on the survival of patients with incurable advanced gastric cancer: a systematic review and meta-analysis.BMC Cancer2013;13:577 PMCID:PMC4235220

[63] Krasniqi E,Formica V.Emerging role of S-1 in gastric cancer.Indian J Med Paediatr Oncol2015;36:219-28 PMCID:PMC4711220