Influence of Surgical Resection for Hepatic Metastases from Gastric Cancer: A Systematic Review_Chinese Journal of Evidence-Based Medicine

Authors：

 WUMing-song ^1,2 , LITian-wu ^1,2 , WEIWei ^1,2 , LITong-jie ^1,2 , LUOHai-quan ^1,2 ,  ZHONGJian-hong ³

1. Oncology Department, The Sixth Affiliated Hospital of Guangxi University of Traditional Chinese Medicine, Wuzhou 543002, China;
2. Oncology Department, Wuzhou Hospital of Traditional Chinese Medicine, Wuzhou 543002, China;
3. Hepatobiliary Surgery, Affiliated Tumor Hospital of Guangxi Medical University, Nanning 530021, China;

Corresponding author：

ZHONGJian-hong, Email: zhongjianhong66@163.com

Keywords：

Liver resection; Gastric cancer liver metastases; Systematic review; Meta-analysis

DOI：

10.7507/1672-2531.20160198

Video：

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Objective To examine long-term survival, morbidity, and mortality following hepatic resection for gastric cancer hepatic metastases and to identify prognostic factors that affect survival. Methods A systematic literature search of EMbase, PubMed, Web of Science, The Cochrane Library (Issue 2, 2015), CBM, WanFang Data, and CNKI was undertaken for studies that evaluated the role of hepatic resection for gastric cancer hepatic metastases. Two reviewers independently screened studies based on inclusion and exclusion criteria, extracted data, and evaluated risk of bias of included studies. RevMan 5.3 software was used for meta-analysis. Results Thirty-nine studies were included, of which, eight studies were included in meta-analysis. The median sample size was 21 (range 10 to 64). Procedures were associated with a median 30-day morbidity of 24% (0% to 47%) and mortality of 0% (0% to 30%). The median 1-year, 3-year, and 5-year survival rates were 68%, 31%, and 27%, respectively. Meta-analysis result of 8 cohort studies showed hepatic resection of hepatic metastases was associated with a significantly improved overall survival at 1-year and 2-year follow-up (RR=0.47, 95%CI 0.3 to 0.58, P < 0.000 01; RR=0.70, 95%CI 0.63 to 0.79, P < 0.000 01). Conclusions Patients with hepatic metastasis from gastric cancer may benefit from hepatic resection. More trials are needed to confirm this finding because of the limited included studies and their low quality.

Citation： WUMing-song, LITian-wu, WEIWei, LITong-jie, LUOHai-quan, ZHONGJian-hong. Influence of Surgical Resection for Hepatic Metastases from Gastric Cancer: A Systematic Review. Chinese Journal of Evidence-Based Medicine, 2016, 16(11): 1306-1312. doi: 10.7507/1672-2531.20160198 Copy

1.	Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, et al. Cancer incidence and mortality patterns in Europe:estimates for 40 countries in 2012. Eur J Cancer, 2013, 49(6):1374-1403.
2.	Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin, 2015, 65(1):5-29.
3.	Saiura A, Umekita N, Inoue S, et al. Clinicopathological features and outcome of hepatic resection for liver metastasis from gastric cancer. Hepatogastroenterology, 2002, 49(46):1062-1065.
4.	Zacherl J, Zacherl M, Scheuba C, et al. Analysis of hepatic resection of metastasis originating from gastric adenocarcinoma. J Gastrointest Surg, 2002, 6(5):682-689.
5.	D'Angelica M, Gonen M, Brennan MF, et al. Patterns of initial recurrence in completely resected gastric adenocarcinoma. Ann Surg, 2004, 240(5):808-816.
6.	Ajani JA, BD, Besh S, et al. Esophageal and Esophagogastric Junction Cancers (excluding the proximal 5cm of the stomach). NCCN Clinical Practice Guidelines in Oncology (version 2). 2012.
7.	Wagner AD, Unverzagt S, Grothe W, et al. Chemotherapy for advanced gastric cancer. Cochrane Database Syst Rev, 2010(3):Cd004064.
8.	Chen L, Song MQ, Lin HZ, et al. Chemotherapy and resection for gastric cancer with synchronous liver metastases. World J Gastroenterol, 2013, 19(13):2097-2103.
9.	Cheon SH, Rha SY, Jeung HC, et al. Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol, 2008, 19(6):1146-1153.
10.	DittmarY, Altendorf-Hofmann A, Rauchfuss F, et al. Resection of liver metastases is beneficial in patients with gastric cancer:report on 15 cases and review of literature. Gastric Cancer, 2012, 15(2):131-136.
11.	Makino H, Kunisaki C, Izumisawa Y, et al. Indication for hepatic resection in the treatment of liver metastasis from gastric cancer. Anticancer Res, 2010, 30(6):2367-2376.
12.	Miki Y, Fujitani K, Hirao M, et al. Significance of surgical treatment of liver metastases from gastric cancer. Anticancer Res, 2012, 32(2):665-670.
13.	Tiberio GA, Baiocchi GL, Morgagni P, et al. Gastric cancer and synchronous hepatic metastases:is it possible to recognize candidates to R0 resection? Ann Surg Oncol, 2015, 22(2):589-596.
14.	Tiberio GA, Coniglio A, Marchet A, et al. Metachronous hepatic metastases from gastric carcinoma:a multicentric survey. Eur J Surg Oncol, 2009, 35(5):486-491.
15.	Ueda K, Iwahashi M, Nakamori M, et al. Analysis of the prognostic factors and evaluation of surgical treatment for synchronous liver metastases from gastric cancer. Langenbecks Arch Surg, 2009, 394(4):647-653.
16.	Adam R, Chiche L, Aloia T, et al. Hepatic resection for noncolorectal nonendocrine liver metastases:analysis of 1, 452 patients and development of a prognostic model. Ann Surg, 2006, 244(4):524-535.
17.	Ambiru S, Miyazaki M, Ito H, et al. Benefits and limits of hepatic resection for gastric metastases. Am J Surg, 2001, 181(3):279-283.
18.	Aizawa M, Nashimoto A, Yabusaki H, et al. Clinical benefit of surgical management for gastric cancer with synchronous liver metastasis. Hepatogastroenterology, 2014, 61(133):1439-1445.
19.	Baek HU, Kim SB, Cho EH, et al. Hepatic resection for hepatic metastases from gastric adenocarcinoma. J Gastric Cancer, 2013, 13(2):86-92.
20.	Choi SB, Song J, Kang cm, et al. Surgical outcome of metachronous hepatic metastases secondary to gastric cancer. Hepatogastroenterology, 2010, 57(97):29-34.
21.	Fujii K, Fujioka S, Kato K, et al. Resection of liver metastasis from gastric adenocarcinoma. Hepatogastroenterology, 2001, 48(38):368-371.
22.	Garancini M, Uggeri F, Degrate L, et al. Surgical treatment of liver metastases of gastric cancer:is local treatment in a systemic disease worthwhile? HPB (Oxford), 2012, 14(3):209-215.
23.	Hirai I, Kimura W, Fuse A, et al. Surgical management for metastatic liver tumors. Hepatogastroenterology, 2006, 53(71):757-763.
24.	Imamura H, Matsuyama Y, Shimada R, et al. A study of factors influencing prognosis after resection of hepatic metastases from colorectal and gastric carcinoma. Am J Gastroenterol, 2001, 96(11):3178-3184.
25.	Koga R, Yamamoto J, Ohyama S, et al. Liver resection for metastatic gastric cancer:experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol, 2007, 37(11):836-842.
26.	Komeda K, Yamashi M, Kubo S, et al. High survival in patients operated for small isolated liver metastases from gastric cancer:a multi-institutional study. World J Surg, 2014, 38(10):2692-2697.
27.	Liu J, Li JH, Zhai RJ, et al. Predictive factors improving survival after gastric and hepatic surgical treatment in gastric cancer patients with synchronous liver metastases. Chin Med J (Engl), 2012, 125(2):165-171.
28.	Miyazaki M, Itoh H, Nakagawa K, et al. Hepatic resection of liver metastases from gastric carcinoma. Am J Gastroenterol, 1997, 92(3):490-493.
29.	Morise Z, Sugioka A, Hoshimoto S, et al. The role of hepatectomy for patients with liver metastases of gastric cancer. Hepatogastroenterology, 2008, 55(85):1238-1241.
30.	Nomura T, Kamio Y, Takasu N, et al. Intrahepatic micrometastases around liver metastases from gastric cancer. J Hepatobiliary Pancreat Surg, 2009, 16(4):493-501.
31.	Ochiai T, Sasako M, Mizuno S, et al. Hepatic resection for metastatic tumours from gastric cancer:analysis of prognostic factors. Br J Surg, 1994, 81(8):1175-1178.
32.	Okano K, Maeba T, Ishimura k, et al. Hepatic resection for metastatic tumors from gastric cancer. Ann Surg, 2002, 235(1):86-91.
33.	Qiu JL, Deng MG, Li W, et al. Hepatic resection for synchronous hepatic metastasis from gastric cancer. Eur J Surg Oncol, 2013, 39(7):694-700.
34.	Roh HR, Suh KS, Lee HJ, et al. Outcome of hepatic resection for metastatic gastric cancer. Am Surg, 2005, 71(2):95-99.
35.	Saito A, Korenaga D, Sakaguchi Y, et al. Surgical treatment for gastric carcinomas with concomitant hepatic metastasis. Hepatogastroenterology, 1996, 43(9):560-564.
36.	Sakamoto Y, Ohyama S, Yamamoto J, et al. Surgical resection of liver metastases of gastric cancer:an analysis of a 17-year experience with 22 patients. Surgery, 2003, 133(5):507-511.
37.	Sakamoto Y, Sano T, Shimada K, et al. Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol, 2007, 95(7):534-539.
38.	Schildberg CW, Croner R, Merkel S, et al. Outcome of operative therapy of hepatic metastatic stomach carcinoma:a retrospective analysis. World J Surg, 2012, 36(4):872-878.
39.	Shirabe K, Shimada M, Matsumata T, et al. Analysis of the prognostic factors for liver metastasis of gastric cancer after hepatic resection:a multi-institutional study of the indications for resection. Hepatogastroenterology, 2003, 50(53):1560-1563.
40.	Takemura N, Saiura A, Koga R, et al. Long-term outcomes after surgical resection for gastric cancer liver metastasis:an analysis of 64 macroscopically complete resections. Langenbecks Arch Surg, 2012, 397(6):951-957.
41.	Thelen A, Jonas S, BenckertC, et al. Liver resection for metastatic gastric cancer. Eur J Surg Oncol, 2008, 34(12):1328-1334.
42.	Tsujimoto H, Ichikura T, Ono S, et al. Outcomes for patients following hepatic resection of metastatic tumors from gastric cancer. Hepatol Int, 2010, 4(1):406-413.
43.	Vigano L, Vellone M, Ferrero A, et al. Liver resection for gastric cancer metastases. Hepatogastroenterology, 2013, 60(123):557-562.
44.	Wang W, Liang H, Zhang H, et al. Prognostic significance of radical surgical treatment for gastric cancer patients with synchronous liver metastases. Med Oncol, 2014, 31(11):258.
45.	Wang YN, Shen KT, Ling JQ, et al, Prognostic analysis of combined curative resection of the stomach and liver lesions in 30 gastric cancer patients with synchronous liver metastases. BMC Surg, 2012, 10(12):20.
46.	Waddell T, Chau I, Cunningham D, et al. 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 Oncol, 2013, 14(6):481-489.
47.	Bang YJ, 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, 2010, 376(9742):687-697.
48.	De Andrade JP, MezhirJJ. The critical role of peritoneal cytology in the staging of gastric cancer:an evidence-based review. J Surg Oncol, 2014, 110(3):291-297.
49.	Schmidt B, Look-Hong N, Maduekwe UN, et al. Noncurative gastrectomy for gastric adenocarcinoma should only be performed in highly selected patients. Ann Surg Oncol, 2013, 20(11):3512-3518.
50.	Markar SR, Wiggins T, Ni M, et al. Assessment of the quality of surgery within randomised controlled trials for the treatment of gastro-oesophageal cancer:a systematic review. Lancet Oncol, 2015, 16(1):23-31.
51.	Sasako M, Sano T, Yamamoto S, et al. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med, 2008, 359(5):453-462.
52.	Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med, 2006, 355(1):11-20.
53.	Kurokawa Y, Shibata T, Sasako M, et al. Validity of response assessment criteria in neoadjuvant chemotherapy for gastric cancer (JCOG0507-A). Gastric Cancer, 2014, 17(3):514-521.

1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, et al. Cancer incidence and mortality patterns in Europe:estimates for 40 countries in 2012. Eur J Cancer, 2013, 49(6):1374-1403.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin, 2015, 65(1):5-29.
3. Saiura A, Umekita N, Inoue S, et al. Clinicopathological features and outcome of hepatic resection for liver metastasis from gastric cancer. Hepatogastroenterology, 2002, 49(46):1062-1065.
4. Zacherl J, Zacherl M, Scheuba C, et al. Analysis of hepatic resection of metastasis originating from gastric adenocarcinoma. J Gastrointest Surg, 2002, 6(5):682-689.
5. D'Angelica M, Gonen M, Brennan MF, et al. Patterns of initial recurrence in completely resected gastric adenocarcinoma. Ann Surg, 2004, 240(5):808-816.
6. Ajani JA, BD, Besh S, et al. Esophageal and Esophagogastric Junction Cancers (excluding the proximal 5cm of the stomach). NCCN Clinical Practice Guidelines in Oncology (version 2). 2012.
7. Wagner AD, Unverzagt S, Grothe W, et al. Chemotherapy for advanced gastric cancer. Cochrane Database Syst Rev, 2010(3):Cd004064.
8. Chen L, Song MQ, Lin HZ, et al. Chemotherapy and resection for gastric cancer with synchronous liver metastases. World J Gastroenterol, 2013, 19(13):2097-2103.
9. Cheon SH, Rha SY, Jeung HC, et al. Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol, 2008, 19(6):1146-1153.
10. DittmarY, Altendorf-Hofmann A, Rauchfuss F, et al. Resection of liver metastases is beneficial in patients with gastric cancer:report on 15 cases and review of literature. Gastric Cancer, 2012, 15(2):131-136.
11. Makino H, Kunisaki C, Izumisawa Y, et al. Indication for hepatic resection in the treatment of liver metastasis from gastric cancer. Anticancer Res, 2010, 30(6):2367-2376.
12. Miki Y, Fujitani K, Hirao M, et al. Significance of surgical treatment of liver metastases from gastric cancer. Anticancer Res, 2012, 32(2):665-670.
13. Tiberio GA, Baiocchi GL, Morgagni P, et al. Gastric cancer and synchronous hepatic metastases:is it possible to recognize candidates to R0 resection? Ann Surg Oncol, 2015, 22(2):589-596.
14. Tiberio GA, Coniglio A, Marchet A, et al. Metachronous hepatic metastases from gastric carcinoma:a multicentric survey. Eur J Surg Oncol, 2009, 35(5):486-491.
15. Ueda K, Iwahashi M, Nakamori M, et al. Analysis of the prognostic factors and evaluation of surgical treatment for synchronous liver metastases from gastric cancer. Langenbecks Arch Surg, 2009, 394(4):647-653.
16. Adam R, Chiche L, Aloia T, et al. Hepatic resection for noncolorectal nonendocrine liver metastases:analysis of 1, 452 patients and development of a prognostic model. Ann Surg, 2006, 244(4):524-535.
17. Ambiru S, Miyazaki M, Ito H, et al. Benefits and limits of hepatic resection for gastric metastases. Am J Surg, 2001, 181(3):279-283.
18. Aizawa M, Nashimoto A, Yabusaki H, et al. Clinical benefit of surgical management for gastric cancer with synchronous liver metastasis. Hepatogastroenterology, 2014, 61(133):1439-1445.
19. Baek HU, Kim SB, Cho EH, et al. Hepatic resection for hepatic metastases from gastric adenocarcinoma. J Gastric Cancer, 2013, 13(2):86-92.
20. Choi SB, Song J, Kang cm, et al. Surgical outcome of metachronous hepatic metastases secondary to gastric cancer. Hepatogastroenterology, 2010, 57(97):29-34.
21. Fujii K, Fujioka S, Kato K, et al. Resection of liver metastasis from gastric adenocarcinoma. Hepatogastroenterology, 2001, 48(38):368-371.
22. Garancini M, Uggeri F, Degrate L, et al. Surgical treatment of liver metastases of gastric cancer:is local treatment in a systemic disease worthwhile? HPB (Oxford), 2012, 14(3):209-215.
23. Hirai I, Kimura W, Fuse A, et al. Surgical management for metastatic liver tumors. Hepatogastroenterology, 2006, 53(71):757-763.
24. Imamura H, Matsuyama Y, Shimada R, et al. A study of factors influencing prognosis after resection of hepatic metastases from colorectal and gastric carcinoma. Am J Gastroenterol, 2001, 96(11):3178-3184.
25. Koga R, Yamamoto J, Ohyama S, et al. Liver resection for metastatic gastric cancer:experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol, 2007, 37(11):836-842.
26. Komeda K, Yamashi M, Kubo S, et al. High survival in patients operated for small isolated liver metastases from gastric cancer:a multi-institutional study. World J Surg, 2014, 38(10):2692-2697.
27. Liu J, Li JH, Zhai RJ, et al. Predictive factors improving survival after gastric and hepatic surgical treatment in gastric cancer patients with synchronous liver metastases. Chin Med J (Engl), 2012, 125(2):165-171.
28. Miyazaki M, Itoh H, Nakagawa K, et al. Hepatic resection of liver metastases from gastric carcinoma. Am J Gastroenterol, 1997, 92(3):490-493.
29. Morise Z, Sugioka A, Hoshimoto S, et al. The role of hepatectomy for patients with liver metastases of gastric cancer. Hepatogastroenterology, 2008, 55(85):1238-1241.
30. Nomura T, Kamio Y, Takasu N, et al. Intrahepatic micrometastases around liver metastases from gastric cancer. J Hepatobiliary Pancreat Surg, 2009, 16(4):493-501.
31. Ochiai T, Sasako M, Mizuno S, et al. Hepatic resection for metastatic tumours from gastric cancer:analysis of prognostic factors. Br J Surg, 1994, 81(8):1175-1178.
32. Okano K, Maeba T, Ishimura k, et al. Hepatic resection for metastatic tumors from gastric cancer. Ann Surg, 2002, 235(1):86-91.
33. Qiu JL, Deng MG, Li W, et al. Hepatic resection for synchronous hepatic metastasis from gastric cancer. Eur J Surg Oncol, 2013, 39(7):694-700.
34. Roh HR, Suh KS, Lee HJ, et al. Outcome of hepatic resection for metastatic gastric cancer. Am Surg, 2005, 71(2):95-99.
35. Saito A, Korenaga D, Sakaguchi Y, et al. Surgical treatment for gastric carcinomas with concomitant hepatic metastasis. Hepatogastroenterology, 1996, 43(9):560-564.
36. Sakamoto Y, Ohyama S, Yamamoto J, et al. Surgical resection of liver metastases of gastric cancer:an analysis of a 17-year experience with 22 patients. Surgery, 2003, 133(5):507-511.
37. Sakamoto Y, Sano T, Shimada K, et al. Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol, 2007, 95(7):534-539.
38. Schildberg CW, Croner R, Merkel S, et al. Outcome of operative therapy of hepatic metastatic stomach carcinoma:a retrospective analysis. World J Surg, 2012, 36(4):872-878.
39. Shirabe K, Shimada M, Matsumata T, et al. Analysis of the prognostic factors for liver metastasis of gastric cancer after hepatic resection:a multi-institutional study of the indications for resection. Hepatogastroenterology, 2003, 50(53):1560-1563.
40. Takemura N, Saiura A, Koga R, et al. Long-term outcomes after surgical resection for gastric cancer liver metastasis:an analysis of 64 macroscopically complete resections. Langenbecks Arch Surg, 2012, 397(6):951-957.
41. Thelen A, Jonas S, BenckertC, et al. Liver resection for metastatic gastric cancer. Eur J Surg Oncol, 2008, 34(12):1328-1334.
42. Tsujimoto H, Ichikura T, Ono S, et al. Outcomes for patients following hepatic resection of metastatic tumors from gastric cancer. Hepatol Int, 2010, 4(1):406-413.
43. Vigano L, Vellone M, Ferrero A, et al. Liver resection for gastric cancer metastases. Hepatogastroenterology, 2013, 60(123):557-562.
44. Wang W, Liang H, Zhang H, et al. Prognostic significance of radical surgical treatment for gastric cancer patients with synchronous liver metastases. Med Oncol, 2014, 31(11):258.
45. Wang YN, Shen KT, Ling JQ, et al, Prognostic analysis of combined curative resection of the stomach and liver lesions in 30 gastric cancer patients with synchronous liver metastases. BMC Surg, 2012, 10(12):20.
46. Waddell T, Chau I, Cunningham D, et al. 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 Oncol, 2013, 14(6):481-489.
47. Bang YJ, 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, 2010, 376(9742):687-697.
48. De Andrade JP, MezhirJJ. The critical role of peritoneal cytology in the staging of gastric cancer:an evidence-based review. J Surg Oncol, 2014, 110(3):291-297.
49. Schmidt B, Look-Hong N, Maduekwe UN, et al. Noncurative gastrectomy for gastric adenocarcinoma should only be performed in highly selected patients. Ann Surg Oncol, 2013, 20(11):3512-3518.
50. Markar SR, Wiggins T, Ni M, et al. Assessment of the quality of surgery within randomised controlled trials for the treatment of gastro-oesophageal cancer:a systematic review. Lancet Oncol, 2015, 16(1):23-31.
51. Sasako M, Sano T, Yamamoto S, et al. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med, 2008, 359(5):453-462.
52. Cunningham D, Allum WH, Stenning SP, et al. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med, 2006, 355(1):11-20.
53. Kurokawa Y, Shibata T, Sasako M, et al. Validity of response assessment criteria in neoadjuvant chemotherapy for gastric cancer (JCOG0507-A). Gastric Cancer, 2014, 17(3):514-521.

Chinese Journal of Evidence-Based Medicine

Influence of Surgical Resection for Hepatic Metastases from Gastric Cancer: A Systematic Review

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