Annals of Surgical Oncology

, Volume 22, Issue 2, pp 589–596 | Cite as

Gastric Cancer and Synchronous Hepatic Metastases: Is It Possible to Recognize Candidates to R0 Resection?

  • Guido Alberto Massimo Tiberio
  • Gian Luca Baiocchi
  • Paolo Morgagni
  • Daniele Marrelli
  • Alberto Marchet
  • Chiara Cipollari
  • Luigina Graziosi
  • Silvia Ministrini
  • Giovanni Vittimberga
  • Annibale Donini
  • Donato Nitti
  • Franco Roviello
  • Arianna Coniglio
  • Giovanni de Manzoni
Gastrointestinal Oncology



Management of patients with synchronous hepatic metastases as the sole metastatic site at diagnosis of gastric cancer is debated. We studied a cohort of patients admitted to surgical units, investigating prognostic factors of clinical relevance and the results of various therapeutic strategies.


Retrospective multicentre chart review. We evaluated how survival from surgery was influenced by patient-related, gastric cancer-related, metastasis-related and treatment-related candidate prognostic factors.


Forty-four patients received palliative surgery without resection, 98 palliative gastrectomy (in 16 cases associated with R+ hepatectomy), whereas 53 patients received both curative gastrectomy and hepatic resection(s) (R0). Adjuvant chemotherapy was administered to 44 patients. Therapeutic approach was selected on the basis of extension of disease, patient’s general conditions and surgeon’s attitude. Surgical mortality was 4.6 % and morbidity was 17.4 %. Survival was independently influenced by the factor T of the gastric primary (p = 0.036) and by the degree of hepatic involvement (p = 0.010). T > 2 and H3 liver involvement were associated with worse prognosis with cumulative effect (p = 0.002). Therapeutic approach to the metastases (p = 0.009) and adjuvant chemotherapy (p < 0.001) displayed independent impact upon survival, with benefit for those receiving aggressive multimodal treatment. The 1-, 3-, and 5-year survival rates were 50.4, 14.0, and 9.3 %, respectively, for patients submitted to curative surgery, 16, 8.5, and 4.3 % after palliative gastrectomy, and 6.8, 2.3, and 0 % after palliative surgery without resection.


Our data suggest some clinical criteria that may facilitate selection of candidates to curative surgery, which offers the best survival chances, especially when associated with adjuvant chemotherapy.


Gastric Cancer Adjuvant Chemotherapy Hepatic Metastasis Peritoneal Metastasis Hepatic Involvement 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are grateful to Mr. Richard Humphies (BA Hons English Literature) for his precious help in revising the English language of the manuscript.



Supplementary material

10434_2014_4018_MOESM1_ESM.doc (84 kb)
Supplementary material 1 (DOC 84 kb)
10434_2014_4018_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 18 kb)
10434_2014_4018_MOESM3_ESM.tif (60 kb)
Supplementary Fig. 1 Effect of chemotherapy. A Survival according to chemotherapy. B Cumulative survival according to the number of negative prognostic factors related to gastric primary (T > 2) and hepatic involvement (H3). Supplementary material 3 (TIFF 60 kb)


  1. 1.
    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;244:524–35.PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Lehner F, Ramackers W, Bektas H, et al. Liver resection for non-colorectal, non-neuroendocrine liver metastases—is hepatic resection justified as part of the oncosurgical treatment? Zentralbl Chir. 2009;134:430–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Ochiai T, Sasako M, Mizuno S, et al. Hepatic resection for metastatic tumours from gastric cancer: analysis of prognostic factors. Br J Surg. 1994;81:1175–8.PubMedCrossRefGoogle Scholar
  4. 4.
    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;394:647–53.PubMedCrossRefGoogle Scholar
  5. 5.
    Okano K, Maeba T, Ishimura K, et al. Hepatic resection for metastatic tumors from gastric cancer. Ann Surg. 2002;235:86–91.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Hwang S-E, Yang D-H, Kim C-Y. Prognostic factors for survival in patients with hepatic recurrence after curative resection of gastric cancer. World J Surg. 2009;33:1468–72.PubMedCrossRefGoogle Scholar
  7. 7.
    Tiberio GAM, Coniglio A, Marchet A, et al. Metachronous hepatic metastases from gastric carcinoma: a multicentric survey. Eur J Surg Oncol. 2009;35:486–91.PubMedCrossRefGoogle Scholar
  8. 8.
    Makino H, Kunisaki C, Izumisawa Y, et al. Indication for hepatic resection in the treatment of liver metastasis from gastric cancer. Anticanc Res. 2010;30:2367–76.Google Scholar
  9. 9.
    Ambiru S, Miyazaki M, Ito H, et al. Benefits and limits of hepatic resection for gastric metastases. Am J Surg. 2001;181:279–83.PubMedCrossRefGoogle Scholar
  10. 10.
    Miyazaki M, Itoh H, Nakagawa K, et al. Hepatic resection of liver metastases from gastric carcinoma. Am J Gastroenterol. 1997;92:490–93.PubMedGoogle Scholar
  11. 11.
    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;50:1560–3.PubMedGoogle Scholar
  12. 12.
    Sakamoto Y, Sano T, Shimada K, et al. Favorable indications for hepatectomy in patients with liver metastasis from gastric cancer. J Surg Oncol. 2007;95:534–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Thelen A, Jonas S, Benckert C, et al. Liver resection for metastatic gastric cancer. Eur J Surg Oncol. 2008;34:1328–34.PubMedCrossRefGoogle Scholar
  14. 14.
    Tsujimoto H, Ichikura T, Ono S, et al. Outcomes for patients following hepatic resection of metastatic tumors from gastric cancer. Hepatol Int. 2010;4:406–13.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    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. 2012;14:209–15.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Schildberg CW, Croner R, Merkel S, et al. Outcome of operative therapy of hepatic metastatic stomach carcinoma: a retrospective analysis. World J Surg. 2012;36:872–8.PubMedCrossRefGoogle Scholar
  17. 17.
    Miki Y, Fujitani K, Hirao M, et al. Significance of surgical treatment of liver metastases from gastric cancer. Anticancer Res. 2012;32:665–70.PubMedGoogle Scholar
  18. 18.
    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;397:951–7.PubMedCrossRefGoogle Scholar
  19. 19.
    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;125:165–71.PubMedGoogle Scholar
  20. 20.
    Dicken BJ, Bigam DL, Cass C, et al. Gastric adenocarcinoma. Review and considerations for future directions. Ann Surg. 2005;241:27–39.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Liu J, Chen L. Current status and progress in gastric cancer with liver metastasis. Chin Med J (Engl). 2011;124:445–56.PubMedGoogle Scholar
  22. 22.
    Tiberio GAM, Portolani N, Giulini SM. Hepatic metastases from gastric cancer. In: Mahmoud L, editor. Gastric carcinoma—molecular aspects and current advances. InTech. 2011. doi: 10.5772/16638.
  23. 23.
    Kerkar SP, Kemp CD, Avital I. Liver resections in metastatic gastric cancer. HPB. 2010;12:589–96.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Chiche L, Ducreux M, Lebreton G, et al. Métastases hépatiques des cancers de l’estomac. In: Adam R, Chiche L, editors. Chirurgie des métastases hépatiques de cancers non colorectaux non endocrine. Monographies de l’association Française de Chirurgie. Paris: Arnette; 2005. p. 45–9.Google Scholar
  25. 25.
    Edge SB, Byrd DR, Compton CC, eds. AJCC cancer staging manual. 7th ed. New York, NY: Springer; 2010.Google Scholar
  26. 26.
    Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English ed. Gastric Cancer. 2011;14:101–12.CrossRefGoogle Scholar
  27. 27.
    Marrelli D, De Stefano A, de Manzoni G, et al. Prediction of recurrence after radical surgery for gastric cancer: a scoring system obtained from a prospective multicenter study. Ann Surg. 2005;241:247–55.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    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;96:3178–84.PubMedCrossRefGoogle Scholar
  29. 29.
    Roh HR, Suh KS, Lee HJ, et al. Outcome of hepatic resection for metastatic gastric cancer. Am Surg. 2005;71:95–9.PubMedGoogle Scholar
  30. 30.
    Yang XW, Li Z, Liu K, et al. Correlation between the survival rate of the patients with synchronous hepatic metastases from gastric carcinoma after surgical resection and patient’s index. Chin Med J. 2012;125:747–51.PubMedGoogle Scholar
  31. 31.
    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;12:20.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Shirabe K, Wakiyama S, Gion T, et al. Hepatic resection for the treatment of liver metastases in gastric carcinoma: review of the literature. HPB. 2006;8:89–92.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Cheon SH, Rha SY, Jeung H-C, 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;19:1146–153.PubMedCrossRefGoogle Scholar
  34. 34.
    Kim HR, Cheon SH, Lee KH, et al. Efficacy and feasibility of radiofrequency ablation for liver metastases from gastric adenocarcinoma. Int J Hyperthermia. 2010;26:305–15.PubMedCrossRefGoogle Scholar
  35. 35.
    Misleh JG, Santoro P, Strasser JF, et al. Multidisciplinary management of gastric cancer. Surg Oncol Clin N Am. 2013;22:247–64.PubMedCrossRefGoogle Scholar
  36. 36.
    Hartgrink HH, Putter H, Klein Kranenbarg E, et al. Value of palliative resection in gastric cancer. Br J Surg. 2002;89:1438–43.PubMedCrossRefGoogle Scholar
  37. 37.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14:113–23.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2014

Authors and Affiliations

  • Guido Alberto Massimo Tiberio
    • 1
  • Gian Luca Baiocchi
    • 1
  • Paolo Morgagni
    • 2
  • Daniele Marrelli
    • 3
  • Alberto Marchet
    • 4
  • Chiara Cipollari
    • 5
  • Luigina Graziosi
    • 6
  • Silvia Ministrini
    • 1
  • Giovanni Vittimberga
    • 2
  • Annibale Donini
    • 6
  • Donato Nitti
    • 4
  • Franco Roviello
    • 3
  • Arianna Coniglio
    • 1
  • Giovanni de Manzoni
    • 5
  1. 1.Surgical Clinic, Department of Clinical and Experimental SciencesUniversity of BresciaBresciaItaly
  2. 2.Department of General SurgeryMorgagni HospitalForlìItaly
  3. 3.Surgical Oncology, Department of Human Pathology and OncologyUniversity of SienaSienaItaly
  4. 4.Department of Oncological and Surgical SciencesUniversity of PadovaPadovaItaly
  5. 5.Division of General SurgeryUniversity of VeronaVeronaItaly
  6. 6.General Surgery, Department of Surgical Sciences, Radiology and DentistryUniversity of PerugiaPerugiaItaly

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