Annals of Surgical Oncology

, Volume 21, Issue 8, pp 2594–2600 | Cite as

Gastric Stump Cancer After Distal Gastrectomy for Benign Disease: Clinicopathological Features and Surgical Outcomes

  • Alberto Di LeoEmail author
  • Corrado Pedrazzani
  • Maria Bencivenga
  • Arianna Coniglio
  • Fausto Rosa
  • Paolo Morgani
  • Daniele Marrelli
  • Alberto Marchet
  • Luca Cozzaglio
  • Simone Giacopuzzi
  • Guido Alberto Massimo Tiberio
  • Giovanni Battista Doglietto
  • Giovanni Vittimberga
  • Franco Roviello
  • Francesco Ricci
Gastrointestinal Oncology



The purpose of the present study was to analyze clinicopathologic features and long-term prognosis of gastric stump cancer (GSC) arising in the remnant stomach 5 years or later after partial gastrectomy for benign disease.


We reviewed the results of 176 patients resected with curative intent for GSC at 8 Italian centers belonging to the Italian Research Group for Gastric Cancer (GIRCG). The median (range) follow-up time for surviving patients was 71.2 (6–207) months.


One hundred forty-six patients were men, the mean age at the time of diagnosis was 69.2 years, and the great majority (167 cases) underwent Billroth II reconstruction. R0 resection was achieved in 158 (90 %) patients, and in 94 (53 %) lymph node dissection was ≥D2. Postoperative mortality and complication rates were 6.2 and 43.2 %, respectively. T1 tumor was diagnosed in 45 (25 %) cases. Lymph node metastases were evident in 86 patients (49 %). Thirteen patients had involvement of the jejunal mesentery nodes (pJN+); five cases were T2–T3 and eight cases were T4. Overall 5-year survival rate was 53.1 %. Five-year survival rates were 68.1, 37.8, and 33.1 % for pT1, pT2-3, and pT4 tumors, respectively (P = 0.001). Five-year survival rate was 56.5 % for node-negative tumors (pN0), 32.3 % for tumors with nodal metastases without involvement of jejunal mesentery nodes (pN+), and 17.1 % for tumors with involvement of jejunal mesentery nodes (pJN+) (P = 0.002).


Our study suggests that an aggressive surgical approach can achieve a satisfactory outcome in GSC.


Gastric Cancer Endoscopic Submucosal Dissection Early Gastric Cancer Gastric Resection Remnant Stomach 
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.



All the authors declare that they have not potential commercial conflicts of interest relevant to this article.


  1. 1.
    Balfour DC. Factors influencing the life expectancy of patients operated on for gastric ulcer. Ann Surg. 1922;76:405–8.PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    Safatle-Ribeiro AV, Ribeiro U Jr, Reynolds JC. Gastric stump cancer: what is the risk? Dig Dis. 1998;16:159–68.PubMedCrossRefGoogle Scholar
  3. 3.
    Barillari P, Aurello P, Manetti G, Broglia S, Cioè I, Piovanello P, Naticchioni E. Carcinoma of the gastric stump. Our experience in 28 treated cases. Minerva Chir. 1997;52:713-6.PubMedGoogle Scholar
  4. 4.
    Thorban S, Böttcher K, Etter M, Roder JD, Bush R, Siewert JR. Prognostic factors in gastric stump cancer. Ann Surg. 2000;231:188–94.PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Schaefer N, Sinning C, Standop J, Overhaus M, Hirner A, Wolff M. Treatment and prognosis of gastric stump carcinoma in comparison with primary proximal gastric cancer. Am J Surg. 2007;194:63–7.PubMedCrossRefGoogle Scholar
  6. 6.
    Firat O, Guler A, Sozbilen M, Ersin S, Kaplan H. Gastric remnant cancer: an old problem with novel concerns. Langenbecks Arch Surg. 2009;394:93–7.PubMedCrossRefGoogle Scholar
  7. 7.
    Mezhir JJ, Gonen M, Ammori JB, Strong VE, Brennan MF, Coit DG. Treatment and outcome of patients with gastric remnant cancer after resection for peptic ulcer disease. Ann Surg Oncol. 2011;18:670–6.PubMedCrossRefGoogle Scholar
  8. 8.
    Gandolfi L, Vaira D, Bertoni F, Rossi A, Solmi L, Leo P, Muratori R. Cancer of gastric stump in Italy, 1979-1986. Gastrointest Endosc. 1988;34:242–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Sinning C, Schaefer N, Standop J, Hirner A, Wolff M. Gastric stump carcinoma—epidemiology and current concepts in pathogenesis and treatment. Eur J Surg Oncol. 2007;33:133–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Dindo D, Demartines N, Clavien PA. Classification of surgical complications. A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma, 2nd English edition. Gastric Cancer. 1998;1:10–24.PubMedCrossRefGoogle Scholar
  12. 12.
    Sobin LH, Wittekind C, Gospodarowicz M, eds. TNM classification of malignant tumors (UICC), 7th edn. New York: Wiley-Blackwell; 2009:73–7.Google Scholar
  13. 13.
    Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand. 1965;64:31–49.PubMedGoogle Scholar
  14. 14.
    Marrelli D, De Stefano A, de Manzoni G, Morgagni P, Di Leo A, Roviello F. Italian research group for gastric cancer. 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
  15. 15.
    Furukawa H, Iwanaga T, Hiratsuka M, et al. Gastric remnant cancer as a metachronous multiple lesion. Br J Surg. 1993;80:50–6.CrossRefGoogle Scholar
  16. 16.
    Tanigawa N, Nomura E, Lee SW, et al. Current state of gastric stump carcinoma in Japan: based on the results of a nationwide survey. World J Surg. 2010;34:1540–7.PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Sitarz R, Maciejewski R, Polkowski WP, Offerhaus GJA. Gastroenterostoma after Billroth antrectomy as a premalignant condition. World J Gastroenterol. 2012;18:3201–6.PubMedCentralPubMedGoogle Scholar
  18. 18.
    Kondo K. Duodenogastric reflux and gastric stump carcinoma. Gastric Cancer. 2002;5:16–22.PubMedCrossRefGoogle Scholar
  19. 19.
    Tanigawa N, Nomura E, Niki M, et al. Clinical study to identify specific characteristics of cancer newly developed in the remnant stomach. Gastric Cancer. 2002;5:23–8.PubMedCrossRefGoogle Scholar
  20. 20.
    Guzzo JL, Duncan M, Bass BL, Bass BL, Bochicchio GV, Napolitano LM. Severe and refractory peptic ulcer disease: the diagnostic dilemma: case report and comprehensive review. Dig Dis Sci. 2005;50:1999-2008.PubMedCrossRefGoogle Scholar
  21. 21.
    Kuwabara K, Matsuda S, Fushimi K, Ishikawa KB, Horiguchi H, Fujimori K. Reappraising the surgical approach on the perforated gastroduodenal ulcer: should gastric resection be abandoned? J Clin Med Res. 2011;213–22.Google Scholar
  22. 22.
    Czymec R, Großmann A, Roblick U, Fischer F, Bruch HP, Hildebrand P. Surgical management of acute upper gastrointestinal bleeding: still a major challenge. Hepatogastroenterology. 2012;59:768–73.Google Scholar
  23. 23.
    Pointner R, Shwab G, Königsrainer A, Bodner E, Shmid KW. Gastric stump cancer: etiopatological and clinical aspects. Endoscopy. 1989;21:115–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Chen CN, Lee WJ, Lee PH, Chang KJ, Chen KM. Clinicopathologic characteristics and prognosis of gastric stump cancer. J Clin Gastroenterol. 1996;23:251-5.PubMedCrossRefGoogle Scholar
  25. 25.
    La Vecchia C, Negri E, D’Avanzo B, Moller H, Franceschi S. Partial gastrectomy and subsequent gastric cancer risk. J Epidemiol Community Health. 1992;46:12–4.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Lundegårdh G, Adami HO, Helmick C, Zack M, Meirik O. Stomach cancer after partial gastrectomy for benign ulcer disease. N Engl J Med. 1988;319:195–200.PubMedCrossRefGoogle Scholar
  27. 27.
    Cunsolo A, Spangaro M, Principe A, et al. The Billroth II gastrectomy in surgical treatment of duodenal ulcer. Clinico-statistical studies of 784 operated cases. Minerva Dietol Gastroenterol. 1980;26:13–26.PubMedGoogle Scholar
  28. 28.
    Petrin C, Del Gaudio A. Billroth II gastric resection (100 homogeneous cases). Chir Ital. 1983;35:398–401.PubMedGoogle Scholar
  29. 29.
    Vigoni A, Marcato M, Mandelli L, Corradini C. Long-term evaluation of the treatment of peptic ulcer by the Billroth II method. Chir Ital. 1986;38:555–9.PubMedGoogle Scholar
  30. 30.
    Newman E, Brennan MF, Hochwald SN, Harrison L, Karpeh MS. Gastric remnant carcinoma: just another proximal gastric cancer or a unique entity? Am J Surg. 1997;173:292–7.PubMedCrossRefGoogle Scholar
  31. 31.
    Sasako M, Maruyama K, Kinoshita T, Okabayashi K. Surgical treatment of carcinoma of the gastric stump. Br J Surg. 1991;78:822–4.PubMedCrossRefGoogle Scholar
  32. 32.
    Verlato G, Roviello F, Marchet A, Giacopuzzi S, Marrelli D, Nitti D, de Manzoni G. Indexes of surgical quality in gastric cancer surgery: experience of an Italian network. Ann Surg Oncol. 2009;16:594–602.PubMedCrossRefGoogle Scholar
  33. 33.
    Han SL, Hua YW, Wang CH, JI SQ, Zhuang J. Metastatic pattern of lymph node and surgery for gastric stump cancer. J Surg Oncol. 2003;82:241–6.PubMedCrossRefGoogle Scholar
  34. 34.
    Pointer R, Schwab G, Königsrainer A, Bodner E. Early cancer of the gastric remnant. Gut. 1988;29:298–301.CrossRefGoogle Scholar
  35. 35.
    Sowa M, Onoda N, Nakanishi I, Maeda K, Yoshikawa K, Kato Y, Chung YS. Early stage carcinoma of the gastric remnant in Japan. Anticancer Res. 1993;13:1835–8.PubMedGoogle Scholar
  36. 36.
    Imada T, Rino Y, Hatori S, et al. Clinicopathologic differences between early gastric remnant cancer and early primary gastric cancer in the upper third of the stomach. Hepatogastroenterology. 2000;47:1186-8.PubMedGoogle Scholar
  37. 37.
    Nishide N, Ono H, Kakushima N, Takizawa K, Tanaka M, Matsubayashi H, Yamaguchi Y. Cinical outcomes of endoscopic submucosal dissection for early gastric cancer in remnant stomach or gastric tube. Endoscopy. 2012;44:577–83.PubMedCrossRefGoogle Scholar
  38. 38.
    Di Leo A, Marrelli D, Roviello F, et al. Lymph node involvement in gastric cancer for different tumor sites and T stage. Italian Research Group for Gastric Cancer (IRGGC) experience. J Gastrointest Surg. 2007;11:1146–53.PubMedCrossRefGoogle Scholar
  39. 39.
    Li F, Zhang R, Liang H, Liu H, Quan J, Zhao J. The pattern of lymph node metastasis and the suitability of 7th UICC N stage in predicting prognosis of remnant gastric cancer. J Cancer Res Clin Oncol. 2012;138:111–7.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2014

Authors and Affiliations

  • Alberto Di Leo
    • 1
    Email author
  • Corrado Pedrazzani
    • 1
  • Maria Bencivenga
    • 2
  • Arianna Coniglio
    • 3
  • Fausto Rosa
    • 4
  • Paolo Morgani
    • 5
  • Daniele Marrelli
    • 6
  • Alberto Marchet
    • 7
  • Luca Cozzaglio
    • 8
  • Simone Giacopuzzi
    • 2
  • Guido Alberto Massimo Tiberio
    • 3
  • Giovanni Battista Doglietto
    • 4
  • Giovanni Vittimberga
    • 5
  • Franco Roviello
    • 6
  • Francesco Ricci
    • 1
  1. 1.Unit of General Surgery, Rovereto HospitalAPSS of TrentoTrentoItaly
  2. 2.Unit of Upper G.I. SurgeryUniversity of VeronaVeronaItaly
  3. 3.Surgical ClinicUniversity of BresciaBresciaItaly
  4. 4.Department of Digestive SurgeryCatholic University of RomeRomeItaly
  5. 5.Department of General SurgeryMorgagni-Pierantoni HospitalForlìItaly
  6. 6.Division of Surgical OncologyUniversity of SienaSienaItaly
  7. 7.Department of Oncological and Surgical ScienceUniversity of PaduaPaduaItaly
  8. 8.Division of Surgical OncologyHumanitas HospitalMilanItaly

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