Advertisement

Langenbeck's Archives of Surgery

, Volume 397, Issue 6, pp 951–957 | Cite as

Long-term outcomes after surgical resection for gastric cancer liver metastasis: an analysis of 64 macroscopically complete resections

  • Nobuyuki Takemura
  • Akio Saiura
  • Rintaro Koga
  • Junichi Arita
  • Ryuji Yoshioka
  • Yoshihiro Ono
  • Naoki Hiki
  • Takeshi Sano
  • Junji Yamamoto
  • Norihiro Kokudo
  • Toshiharu Yamaguchi
Original Article

Abstract

Purpose

The indication for hepatectomy in cases of gastric cancer liver metastases (GLM) remains unclear and it remains controversial whether surgical resection is beneficial for GLM. The objective of this retrospective study was to clarify the indications for and benefit of hepatectomy for GLM.

Methods

Seventy-three patients underwent hepatectomies for GLM from January 1993 to January 2011. Macroscopically complete (R0 or R1) resection was achieved in 64 patients. Among them, 32 patients underwent synchronous hepatectomy with gastrectomy and the remaining 32 patients underwent metachronous hepatectomy. Repeat hepatectomy was done in 14 patients for resectable intrahepatic recurrences. Clinicopathological factors were evaluated by univariate and multivariate analyses among patients who received macroscopically complete resection for those affecting survival.

Results

The overall 1-, 3-, and 5-year survival rates after macroscopically complete (R0 or R1) liver resection (n = 64) for GLM were 84, 50, and 37 %, respectively, with a median survival of 34 months. Univariate analysis identified serosal invasion of the primary gastric cancer and blood transfusions during surgery as poor prognosis indicators. By multivariate analysis, serosal invasion of the primary gastric cancer and larger hepatic tumor (>5 cm in diameter) were found to be independent indicators of poor prognosis.

Conclusions

GLM patients with the maximum diameter of hepatic tumors of <5 cm and without serosal invasion of the primary gastric cancer are the best candidate for hepatectomy.

Keywords

Gastric cancer liver metastasis (GLM) Prognosis Liver resection 

Notes

Acknowledgments

This work was supported in part by the National Cancer Center Research and Development Fund (23-A-14).

Conflicts of interest

None.

References

  1. 1.
    Imamura H, Seyama Y, Kokudo N, Aoki T, Sano K, Minagawa M, Sugawara Y, Makuuchi M (2004) Single and multiple resections of multiple hepatic metastases of colorectal origin. Surgery 135(5):508–517. doi: 10.1016/j.surg.2003.10.009 PubMedCrossRefGoogle Scholar
  2. 2.
    Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, Feuer EJ, Thun MJ (2005) Cancer statistics, 2005. CA Cancer J Clin 55(1):10–30PubMedCrossRefGoogle Scholar
  3. 3.
    Douglass HO Jr, Hundahl SA, Macdonald JS, Khatri VP (2007) Gastric cancer: D2 dissection or low Maruyama Index-based surgery—a debate. Surg Oncol Clin N Am 16(1):133–155. doi: 10.1016/j.soc.2006.10.005 PubMedCrossRefGoogle Scholar
  4. 4.
    Koga S, Kawaguchi H, Kishimoto H, Tanaka K, Miyano Y, Kimura O, Takeda R, Nishidoi H (1980) Therapeutic significance of noncurative gastrectomy for gastric cancer with liver metastasis. Am J Surg 140((3):356–359PubMedCrossRefGoogle Scholar
  5. 5.
    Okuyama K, Isono K, Juan IK, Onoda S, Ochiai T, Yamamoto Y, Koide Y, Satoh H (1985) Evaluation of treatment for gastric cancer with liver metastasis. Cancer 55(10):2498–2505PubMedCrossRefGoogle Scholar
  6. 6.
    Sakamoto Y, Ohyama S, Yamamoto J, Yamada K, Seki M, Ohta K, Kokudo N, Yamaguchi T, Muto T, Makuuchi M (2003) Surgical resection of liver metastases of gastric cancer: an analysis of a 17-year experience with 22 patients. Surgery 133(5):507–511. doi: 10.1067/msy.2003.147 PubMedCrossRefGoogle Scholar
  7. 7.
    Boku N, Yamamoto S, Fukuda H, Shirao K, Doi T, Sawaki A, Koizumi W, Saito H, Yamaguchi K, Takiuchi H, Nasu J, Ohtsu A (2009) Fluorouracil versus combination of irinotecan plus cisplatin versus S-1 in metastatic gastric cancer: a randomised phase 3 study. Lancet Oncol 10(11):1063–1069. doi: 10.1016/S1470-2045(09)70259-1 PubMedCrossRefGoogle Scholar
  8. 8.
    Sarela AI, Yelluri S (2007) Gastric adenocarcinoma with distant metastasis: is gastrectomy necessary? Arch Surg 142(2):143–149. doi: 10.1001/archsurg.142.2.143, discussion 149PubMedCrossRefGoogle Scholar
  9. 9.
    Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T, Aprile G, Kulikov E, Hill J, Lehle M, Ruschoff J, Kang YK (2010) 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 376(9742):687–697. doi: 10.1016/S0140-6736(10)61121-X PubMedCrossRefGoogle Scholar
  10. 10.
    Cunningham D, Okines AF, Ashley S (2010) Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med 362(9):858–859. doi: 10.1056/NEJMc0911925 PubMedCrossRefGoogle Scholar
  11. 11.
    Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, Toh Y, Nagaie T, Takagi S, Yamamura Y, Yanaoka K, Orita H, Takeuchi M (2008) S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol 9(3):215–221. doi: 10.1016/S1470-2045(08)70035-4 PubMedCrossRefGoogle Scholar
  12. 12.
    Folprecht G, Gruenberger T, Bechstein WO, Raab HR, Lordick F, Hartmann JT, Lang H, Frilling A, Stoehlmacher J, Weitz J, Konopke R, Stroszczynski C, Liersch T, Ockert D, Herrmann T, Goekkurt E, Parisi F, Kohne CH (2010) Tumour response and secondary resectability of colorectal liver metastases following neoadjuvant chemotherapy with cetuximab: the CELIM randomised phase 2 trial. Lancet Oncol 11(1):38–47. doi: 10.1016/S1470-2045(09)70330-4 PubMedCrossRefGoogle Scholar
  13. 13.
    Hecht JR, Mitchell E, Chidiac T, Scroggin C, Hagenstad C, Spigel D, Marshall J, Cohn A, McCollum D, Stella P, Deeter R, Shahin S, Amado RG (2009) A randomized phase IIIB trial of chemotherapy, bevacizumab, and panitumumab compared with chemotherapy and bevacizumab alone for metastatic colorectal cancer. J Clin Oncol 27(5):672–680. doi: 10.1200/JCO.2008.19.8135 PubMedCrossRefGoogle Scholar
  14. 14.
    Saltz LB, Clarke S, Diaz-Rubio E, Scheithauer W, Figer A, Wong R, Koski S, Lichinitser M, Yang TS, Rivera F, Couture F, Sirzen F, Cassidy J (2008) Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study. J Clin Oncol 26(12):2013–2019. doi: 10.1200/JCO.2007.14.9930 PubMedCrossRefGoogle Scholar
  15. 15.
    Kokudo N, Tada K, Seki M, Ohta H, Azekura K, Ueno M, Matsubara T, Takahashi T, Nakajima T, Muto T (2001) Anatomical major resection versus nonanatomical limited resection for liver metastases from colorectal carcinoma. Am J Surg 181(2):153–159PubMedCrossRefGoogle Scholar
  16. 16.
    Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL (2002) Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 235(6):759–766PubMedCrossRefGoogle Scholar
  17. 17.
    Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, Curley SA, Loyer EM, Muratore A, Mentha G, Capussotti L, Vauthey JN (2005) Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241(5):715–722, discussion 722-714PubMedCrossRefGoogle Scholar
  18. 18.
    Rees M, Tekkis PP, Welsh FK, O’Rourke T, John TG (2008) Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg 247(1):125–135. doi: 10.1097/SLA.0b013e31815aa2c2 PubMedCrossRefGoogle Scholar
  19. 19.
    de Jong MC, Pulitano C, Ribero D, Strub J, Mentha G, Schulick RD, Choti MA, Aldrighetti L, Capussotti L, Pawlik TM (2009) Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients. Ann Surg 250(3):440–448. doi: 10.1097/SLA.0b013e3181b4539b PubMedGoogle Scholar
  20. 20.
    Kanda T, Yajima K, Kosugi SI, Ishikawa T, Ajioka Y, Hatakeyama K (2011) Gastrectomy as a secondary surgery for stage IV gastric cancer patients who underwent S-1-based chemotherapy: a multi-institute retrospective study. Gastric Cancer. doi: 10.1007/s10120-011-0100-y
  21. 21.
    Lordick F (2012) To resect or not resect in metastatic gastric cancer: that is the question! Gastric Cancer. doi: 10.1007/s10120-011-0136-z
  22. 22.
    Ochiai T, Sasako M, Mizuno S, Kinoshita T, Takayama T, Kosuge T, Yamazaki S, Maruyama K (1994) Hepatic resection for metastatic tumours from gastric cancer: analysis of prognostic factors. Br J Surg 81(8):1175–1178PubMedCrossRefGoogle Scholar
  23. 23.
    Miyazaki M, Itoh H, Nakagawa K, Ambiru S, Shimizu H, Togawa A, Shiobara M, Ohtsuka M, Sasada K, Shimizu Y, Yoshioka S, Nakajima N, Suwa T, Kimura F (1997) Hepatic resection of liver metastases from gastric carcinoma. Am J Gastroenterol 92(3):490–493PubMedGoogle Scholar
  24. 24.
    Ambiru S, Miyazaki M, Ito H, Nakagawa K, Shimizu H, Yoshidome H, Shimizu Y, Nakajima N (2001) Benefits and limits of hepatic resection for gastric metastases. Am J Surg 181(3):279–283PubMedCrossRefGoogle Scholar
  25. 25.
    Okano K, Maeba T, Ishimura K, Karasawa Y, Goda F, Wakabayashi H, Usuki H, Maeta H (2002) Hepatic resection for metastatic tumors from gastric cancer. Ann Surg 235(1):86–91PubMedCrossRefGoogle Scholar
  26. 26.
    Saiura A, Umekita N, Inoue S, Maeshiro T, Miyamoto S, Matsui Y, Asakage M, Kitamura M (2002) Clinicopathological features and outcome of hepatic resection for liver metastasis from gastric cancer. Hepato-Gastroenterology 49(46):1062–1065PubMedGoogle Scholar
  27. 27.
    Shirabe K, Shimada M, Matsumata T, Higashi H, Yakeishi Y, Wakiyama S, Ikeda Y, Ezaki T, Fukuzawa S, Takenaka K, Kishikawa K, Ikeda T, Taguchi K, Maehara Y, Sugimachi K (2003) Analysis of the prognostic factors for liver metastasis of gastric cancer after hepatic resection: a multi-institutional study of the indications for resection. Hepato-Gastroenterology 50(53):1560–1563PubMedGoogle Scholar
  28. 28.
    Adam R, Chiche L, Aloia T, Elias D, Salmon R, Rivoire M, Jaeck D, Saric J, Le Treut YP, Belghiti J, Mantion G, Mentha G (2006) Hepatic resection for noncolorectal nonendocrine liver metastases: analysis of 1,452 patients and development of a prognostic model. Ann Surg 244(4):524–535. doi: 10.1097/01.sla.0000239036.46827.5f PubMedGoogle Scholar
  29. 29.
    Koga R, Yamamoto J, Ohyama S, Saiura A, Seki M, Seto Y, Yamaguchi T (2007) Liver resection for metastatic gastric cancer: experience with 42 patients including eight long-term survivors. Jpn J Clin Oncol 37(11):836–842. doi: 10.1093/jjco/hym113 PubMedCrossRefGoogle Scholar
  30. 30.
    Sakamoto Y, Sano T, Shimada K, Esaki M, Saka M, Fukagawa T, Katai H, Kosuge T, Sasako M (2007) Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol 95(7):534–539. doi: 10.1002/jso.20739 PubMedCrossRefGoogle Scholar
  31. 31.
    Cheon SH, Rha SY, Jeung HC, Im CK, Kim SH, Kim HR, Ahn JB, Roh JK, Noh SH, Chung HC (2008) Survival benefit of combined curative resection of the stomach (D2 resection) and liver in gastric cancer patients with liver metastases. Ann Oncol 19(6):1146–1153. doi: 10.1093/annonc/mdn026 PubMedCrossRefGoogle Scholar
  32. 32.
    Hirasawa T, Asahara S, Fujisaki S, Kuraoka K, Takano K, Kamei A, Ikari T (2008) Transcatheter arterial chemoembolization (TACE) using degradable starch microspheres (DSM) for metastatic liver tumors in patients with gastric cancer. Nihon Shokakibyo Gakkai Zasshi 105(3):367–372. doi: JST.JSTAGE/nisshoshi/105.367 PubMedGoogle Scholar
  33. 33.
    Kinoshita T, Nashimoto A, Yamamura Y, Okamura T, Sasako M, Sakamoto J, Kojima H, Hiratsuka M, Arai K, Sairenji M, Fukushima N, Kimura H, Nakajima T (2004) Feasibility study of adjuvant chemotherapy with S-1 (TS-1; tegafur, gimeracil, oteracil potassium) for gastric cancer. Gastric Cancer 7(2):104–109. doi: 10.1007/s10120-004-0278-3 PubMedCrossRefGoogle Scholar
  34. 34.
    Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, Furukawa H, Nakajima T, Ohashi Y, Imamura H, Higashino M, Yamamura Y, Kurita A, Arai K (2007) Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 357(18):1810–1820. doi: 10.1056/NEJMoa072252 PubMedCrossRefGoogle Scholar
  35. 35.
    Strasberg SM (2005) Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 12(5):351–355. doi: 10.1007/s00534-005-0999-7 PubMedCrossRefGoogle Scholar
  36. 36.
    Leporrier J, Maurel J, Chiche L, Bara S, Segol P, Launoy G (2006) A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br J Surg 93(4):465–474. doi: 10.1002/bjs.5278 PubMedCrossRefGoogle Scholar
  37. 37.
    Kobayashi H, Mochizuki H, Sugihara K, Morita T, Kotake K, Teramoto T, Kameoka S, Saito Y, Takahashi K, Hase K, Oya M, Maeda K, Hirai T, Kameyama M, Shirouzu K, Muto T (2007) Characteristics of recurrence and surveillance tools after curative resection for colorectal cancer: a multicenter study. Surgery 141(1):67–75. doi: 10.1016/j.surg.2006.07.020 PubMedCrossRefGoogle Scholar
  38. 38.
    Okuno K (2007) Surgical treatment for digestive cancer. Current issues—colon cancer. Dig Surg 24(2):108–114. doi: 10.1159/000101897 PubMedCrossRefGoogle Scholar
  39. 39.
    Makela JT, Laitinen SO, Kairaluoma MI (1995) Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg 130(10):1062–1067PubMedCrossRefGoogle Scholar
  40. 40.
    Schoemaker D, Black R, Giles L, Toouli J (1998) Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology 114(1):7–14PubMedCrossRefGoogle Scholar
  41. 41.
    Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D, Giacchetti S, Paule B, Kunstlinger F, Ghemard O, Levi F, Bismuth H (2004) Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg 240(4):644–657, discussion 657-648PubMedGoogle Scholar
  42. 42.
    Hwang SE, Yang DH, Kim CY (2009) Prognostic factors for survival in patients with hepatic recurrence after curative resection of gastric cancer. World J Surg 33(7):1468–1472. doi: 10.1007/s00268-009-0034-2 PubMedCrossRefGoogle Scholar
  43. 43.
    Tiberio GA, Coniglio A, Marchet A, Marrelli D, Giacopuzzi S, Baiocchi L, Roviello F, de Manzoni G, Nitti D, Giulini SM (2009) Metachronous hepatic metastases from gastric carcinoma: a multicentric survey. Eur J Surg Oncol 35(5):486–491. doi: 10.1016/j.ejso.2008.12.017 PubMedCrossRefGoogle Scholar
  44. 44.
    Tsujimoto H, Ichikura T, Ono S, Sugasawa H, Hiraki S, Sakamoto N, Yaguchi Y, Hatsuse K, Yamamoto J, Hase K (2010) Outcomes for patients following hepatic resection of metastatic tumors from gastric cancer. Hepatol Int 4(1):406–413. doi: 10.1007/s12072-009-9161-y PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Nobuyuki Takemura
    • 1
  • Akio Saiura
    • 1
  • Rintaro Koga
    • 1
  • Junichi Arita
    • 1
  • Ryuji Yoshioka
    • 1
  • Yoshihiro Ono
    • 1
  • Naoki Hiki
    • 1
  • Takeshi Sano
    • 1
  • Junji Yamamoto
    • 2
  • Norihiro Kokudo
    • 3
  • Toshiharu Yamaguchi
    • 1
  1. 1.Department of Gastroenterological Surgery, Cancer Institute Ariake HospitalJapanese Foundation for Cancer ResearchKoto-ku, TokyoJapan
  2. 2.Department of SurgeryNational Defense Medical CollegeTokorozawaJapan
  3. 3.Division of Hepato–Biliary–Pancreatic Surgery, Department of Surgery, Graduate School of MedicineUniversity of TokyoTokyoJapan

Personalised recommendations