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Published in: Gastric Cancer 1/2012

01-09-2012 | Review Article

Systematic review of the predictors of positive margins in gastric cancer surgery and the effect on survival

Authors: Hamid Reza Raziee, Roberta Cardoso, Rajini Seevaratnam, Alyson Mahar, Lucy Helyer, Calvin Law, Natalie Coburn

Published in: Gastric Cancer | Special Issue 1/2012

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Abstract

Background

Complete resection is the only definitive treatment available for gastric cancer. Factors associated with positive margins and their survival effects have been the subject of many studies, but the appropriate management for these patients is still debated. The objective of this review is to examine positive margins after gastric cancer resections by exploring predictive factors, impact on survival, and optimal strategies for re-resection.

Methods

A systematic electronic literature search was conducted using Medline and EMBASE from January 1, 1998, to December 31, 2009. Studies on gastric or gastroesophageal junction adenocarcinoma that either investigated the predictors for positive margin or employed multivariate methods to analyze the survival effects of positive margins were selected.

Results

Twenty-two studies incorporating 19355 patients were included in this review. Positive margins were associated with larger tumor size, deeper wall penetration, more extensive gastric involvement, greater nodal involvement, higher stage, diffuse histology, higher Borrmann type, lymphatic vessel involvement, and total gastrectomy. Patient survival was independently associated with margin status, and this survival effect was more prominent in early cancers in most studies that performed subgroup analyses.

Conclusions

The probability of acquiring positive margins is highly dependent on the biology and the extent of the tumor. There is a significant negative effect on survival, which is more prominent in cancers at early stages, making re-resection or a second operation important. Patients with more advanced disease can be offered more extensive surgery to remove disease, but this should be balanced against the risks of more extensive resections.
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Literature
1.
go back to reference Fleming ID, Cooper JS, Henson DE, Hutter RVP, Kennedy BJ. AJCC cancer staging manual. 5th ed. Philadelphia: Lippincott-Raven Publishers; 1997. Fleming ID, Cooper JS, Henson DE, Hutter RVP, Kennedy BJ. AJCC cancer staging manual. 5th ed. Philadelphia: Lippincott-Raven Publishers; 1997.
2.
go back to reference Kim SH, Karpeh MS, Klimstra DS, Leung D, Brennan MF. Effect of microscopic resection line disease on gastric cancer survival. J Gastrointest Surg. 1999;3(1):24–33.PubMedCrossRef Kim SH, Karpeh MS, Klimstra DS, Leung D, Brennan MF. Effect of microscopic resection line disease on gastric cancer survival. J Gastrointest Surg. 1999;3(1):24–33.PubMedCrossRef
3.
go back to reference Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg. 1998;228(4):449–61.PubMedCrossRef Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg. 1998;228(4):449–61.PubMedCrossRef
4.
go back to reference Bozzetti F, Bonfanti G, Bufalino R, Menotti V, Persano S, Andreola S. Adequacy of margins of resection in gastrectomy for cancer. Ann Surg. 1982;196(6):685–90.PubMedCrossRef Bozzetti F, Bonfanti G, Bufalino R, Menotti V, Persano S, Andreola S. Adequacy of margins of resection in gastrectomy for cancer. Ann Surg. 1982;196(6):685–90.PubMedCrossRef
5.
go back to reference Sun Z, Li DM, Wang ZN, Huang BJ, Xu Y, Li K. Prognostic significance of microscopic positive margins for gastric cancer patients with potentially curative resection. Ann Surg Oncol. 2009;16(11):3028–37.PubMedCrossRef Sun Z, Li DM, Wang ZN, Huang BJ, Xu Y, Li K. Prognostic significance of microscopic positive margins for gastric cancer patients with potentially curative resection. Ann Surg Oncol. 2009;16(11):3028–37.PubMedCrossRef
6.
go back to reference An JY, Kang TH, Choi MG, Noh JH, Sohn TS, Kim S. Borrmann type IV: an independent prognostic factor for survival in gastric cancer. J Gastrointest Surg. 2008;12(8):1364–9.PubMedCrossRef An JY, Kang TH, Choi MG, Noh JH, Sohn TS, Kim S. Borrmann type IV: an independent prognostic factor for survival in gastric cancer. J Gastrointest Surg. 2008;12(8):1364–9.PubMedCrossRef
7.
go back to reference Chan WH, Wong WK, Khin LW, Chan HS, Soo KC. Significance of a positive oesophageal margin in stomach cancer. Aust N Z J Surg. 2000;70(10):700–3.PubMedCrossRef Chan WH, Wong WK, Khin LW, Chan HS, Soo KC. Significance of a positive oesophageal margin in stomach cancer. Aust N Z J Surg. 2000;70(10):700–3.PubMedCrossRef
8.
go back to reference Dicken BJ, Saunders LD, Jhangri GS, de Gara C, Cass C, Andrews S. Gastric cancer: establishing predictors of biologic behavior with use of population-based data. Ann Surg Oncol. 2004;11(6):629–35.PubMedCrossRef Dicken BJ, Saunders LD, Jhangri GS, de Gara C, Cass C, Andrews S. Gastric cancer: establishing predictors of biologic behavior with use of population-based data. Ann Surg Oncol. 2004;11(6):629–35.PubMedCrossRef
9.
go back to reference Johansson J, Djerf P, Oberg S, Zilling T, von Holstein CS, Johnsson F. Two different surgical approaches in the treatment of adenocarcinoma at the gastroesophageal junction. World J Surg. 2008;32(6):1013–20.PubMedCrossRef Johansson J, Djerf P, Oberg S, Zilling T, von Holstein CS, Johnsson F. Two different surgical approaches in the treatment of adenocarcinoma at the gastroesophageal junction. World J Surg. 2008;32(6):1013–20.PubMedCrossRef
10.
go back to reference Kim JH, Jang YJ, Park SS, Park SH, Kim SJ, Mok YJ. Surgical outcomes and prognostic factors for T4 gastric cancers. Asian J Surg. 2009;32(4):198–204.PubMedCrossRef Kim JH, Jang YJ, Park SS, Park SH, Kim SJ, Mok YJ. Surgical outcomes and prognostic factors for T4 gastric cancers. Asian J Surg. 2009;32(4):198–204.PubMedCrossRef
11.
go back to reference Kycler W, Teresiak M, Łoziński C. Prognostic factors for patients with gastric cancer after surgical resection. Rep Pract Oncol Radiother. 2006;11(5):235–46.CrossRef Kycler W, Teresiak M, Łoziński C. Prognostic factors for patients with gastric cancer after surgical resection. Rep Pract Oncol Radiother. 2006;11(5):235–46.CrossRef
12.
go back to reference Lello E, Furnes B, Edna TH. Short and long-term survival from gastric cancer. A population-based study from a county hospital during 25 years. Acta Oncol. 2007;46(3):308–15.PubMedCrossRef Lello E, Furnes B, Edna TH. Short and long-term survival from gastric cancer. A population-based study from a county hospital during 25 years. Acta Oncol. 2007;46(3):308–15.PubMedCrossRef
13.
go back to reference Mariette C, Castel B, Balon JM, Van Seuningen I, Triboulet JP. Extent of oesophageal resection for adenocarcinoma of the oesophagogastric junction. Eur J Surg Oncol. 2003;29(7):588–93.PubMedCrossRef Mariette C, Castel B, Balon JM, Van Seuningen I, Triboulet JP. Extent of oesophageal resection for adenocarcinoma of the oesophagogastric junction. Eur J Surg Oncol. 2003;29(7):588–93.PubMedCrossRef
14.
go back to reference Morgagni P, Garcea D, Marrelli D, De Manzoni G, Natalini G, Kurihara H. Resection line involvement after gastric cancer surgery: clinical outcome in nonsurgically retreated patients. World J Surg. 2008;32(12):2661–7.PubMedCrossRef Morgagni P, Garcea D, Marrelli D, De Manzoni G, Natalini G, Kurihara H. Resection line involvement after gastric cancer surgery: clinical outcome in nonsurgically retreated patients. World J Surg. 2008;32(12):2661–7.PubMedCrossRef
15.
go back to reference Nazli O, Derici H, Tansug T, Yaman I, Bozdag AD, Isguder AS. Survival analysis after surgical treatment of gastric cancer: review of 121 cases. Hepatogastroenterology. 2007;54(74):625–9.PubMed Nazli O, Derici H, Tansug T, Yaman I, Bozdag AD, Isguder AS. Survival analysis after surgical treatment of gastric cancer: review of 121 cases. Hepatogastroenterology. 2007;54(74):625–9.PubMed
16.
go back to reference Samson PS, Escovidal LA, Yrastorza SG, Veneracion RG, Nerves MY. Re-study of gastric cancer: analysis of outcome. World J Surg. 2002;26(4):428–33.PubMedCrossRef Samson PS, Escovidal LA, Yrastorza SG, Veneracion RG, Nerves MY. Re-study of gastric cancer: analysis of outcome. World J Surg. 2002;26(4):428–33.PubMedCrossRef
17.
go back to reference Takahashi I, Matsusaka T, Onohara T, Nishizaki T, Ishikawa T, Tashiro H. Clinicopathological features of long-term survivors of scirrhous gastric cancer. Hepatogastroenterology. 2000;47(35):1485–8.PubMed Takahashi I, Matsusaka T, Onohara T, Nishizaki T, Ishikawa T, Tashiro H. Clinicopathological features of long-term survivors of scirrhous gastric cancer. Hepatogastroenterology. 2000;47(35):1485–8.PubMed
18.
go back to reference Cascinu S, Giordani P, Catalano V, Agostinelli R, Catalano G. Resection-line involvement in gastric cancer patients undergoing curative resections: implications for clinical management. Jpn J Clin Oncol. 1999;29(6):291–3.PubMedCrossRef Cascinu S, Giordani P, Catalano V, Agostinelli R, Catalano G. Resection-line involvement in gastric cancer patients undergoing curative resections: implications for clinical management. Jpn J Clin Oncol. 1999;29(6):291–3.PubMedCrossRef
19.
go back to reference Cho BC, Jeung HC, Choi HJ, Rha SY, Hyung WJ, Cheong JH. Prognostic impact of resection margin involvement after extended (D2/D3) gastrectomy for advanced gastric cancer: a 15-year experience at a single institute. J Surg Oncol. 2007;95(6):461–8.PubMedCrossRef Cho BC, Jeung HC, Choi HJ, Rha SY, Hyung WJ, Cheong JH. Prognostic impact of resection margin involvement after extended (D2/D3) gastrectomy for advanced gastric cancer: a 15-year experience at a single institute. J Surg Oncol. 2007;95(6):461–8.PubMedCrossRef
20.
go back to reference Wang SY, Yeh CN, Lee HL, Liu YY, Chao TC, Hwang TL. Clinical impact of positive surgical margin status on gastric cancer patients undergoing gastrectomy. Ann Surg Oncol. 2009;16(10):2738–43.PubMedCrossRef Wang SY, Yeh CN, Lee HL, Liu YY, Chao TC, Hwang TL. Clinical impact of positive surgical margin status on gastric cancer patients undergoing gastrectomy. Ann Surg Oncol. 2009;16(10):2738–43.PubMedCrossRef
21.
go back to reference Casson AG, Darnton SJ, Subramanian S, Hiller L. What is the optimal distal resection margin for esophageal carcinoma? Ann Thorac Surg. 2000;69(1):205–9.PubMedCrossRef Casson AG, Darnton SJ, Subramanian S, Hiller L. What is the optimal distal resection margin for esophageal carcinoma? Ann Thorac Surg. 2000;69(1):205–9.PubMedCrossRef
22.
go back to reference Kodera Y, Yamamura Y, Ito S, Kanemitsu Y, Shimizu Y, Hirai T. Is Borrmann type IV gastric carcinoma a surgical disease? An old problem revisited with reference to the result of peritoneal washing cytology. J Surg Oncol. 2001;78(3):175–81 (discussion 81–2). Kodera Y, Yamamura Y, Ito S, Kanemitsu Y, Shimizu Y, Hirai T. Is Borrmann type IV gastric carcinoma a surgical disease? An old problem revisited with reference to the result of peritoneal washing cytology. J Surg Oncol. 2001;78(3):175–81 (discussion 81–2).
23.
go back to reference Piessen G, Messager M, Leteurtre E, Jean-Pierre T, Mariette C. Signet ring cell histology is an independent predictor of poor prognosis in gastric adenocarcinoma regardless of tumoral clinical presentation. Ann Surg. 2009;250(6):878–87.PubMedCrossRef Piessen G, Messager M, Leteurtre E, Jean-Pierre T, Mariette C. Signet ring cell histology is an independent predictor of poor prognosis in gastric adenocarcinoma regardless of tumoral clinical presentation. Ann Surg. 2009;250(6):878–87.PubMedCrossRef
24.
go back to reference Shiraishi N, Adachi Y, Kitano S, Bandoh T, Inomata M, Yasuda K. Gastric cancer with extragastric lymph node metastasis: multivariate prognostic study. Gastric Cancer. 2000;3(4):211–8.PubMedCrossRef Shiraishi N, Adachi Y, Kitano S, Bandoh T, Inomata M, Yasuda K. Gastric cancer with extragastric lymph node metastasis: multivariate prognostic study. Gastric Cancer. 2000;3(4):211–8.PubMedCrossRef
25.
go back to reference Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ. AJCC cancer staging manual. 4th ed. Philadelphia: Lippincott-Raven Publishers; 1992. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ. AJCC cancer staging manual. 4th ed. Philadelphia: Lippincott-Raven Publishers; 1992.
26.
go back to reference Greene FL, Page DL, Fleming ID, Fritz AG, Balch CM, Haller DG. AJCC cancer staging manual. 6th ed. New York: Springer; 2002. Greene FL, Page DL, Fleming ID, Fritz AG, Balch CM, Haller DG. AJCC cancer staging manual. 6th ed. New York: Springer; 2002.
27.
go back to reference Papachristou DN, Agnanti N, D’Agostino H, Fortner JG. Histologically positive esophageal margin in the surgical treatment of gastric cancer. Am J Surg. 1980;139(5):711–3.PubMedCrossRef Papachristou DN, Agnanti N, D’Agostino H, Fortner JG. Histologically positive esophageal margin in the surgical treatment of gastric cancer. Am J Surg. 1980;139(5):711–3.PubMedCrossRef
28.
go back to reference Hockey MS, Fielding JWL, Kelly KA. Resection line disease in stomach cancer. Br Med J. 1984;289(6445):601–3.CrossRef Hockey MS, Fielding JWL, Kelly KA. Resection line disease in stomach cancer. Br Med J. 1984;289(6445):601–3.CrossRef
29.
go back to reference Shiu MH, Moore E, Sanders M, Huvos A, Freedman B, Goodbold J. Influence of the extent of resection on survival after curative treatment of gastric carcinoma. A retrospective multivariate analysis. Arch Surg. 1987;122(11):1347–51.PubMedCrossRef Shiu MH, Moore E, Sanders M, Huvos A, Freedman B, Goodbold J. Influence of the extent of resection on survival after curative treatment of gastric carcinoma. A retrospective multivariate analysis. Arch Surg. 1987;122(11):1347–51.PubMedCrossRef
30.
go back to reference Gall CA, Rieger NA, Wattchow DA. Positive proximal resection margins after resection for carcinoma of the oesophagus and stomach: effect on survival and symptom recurrence. Aust N Z J Surg. 1996;66(11):734–7.PubMedCrossRef Gall CA, Rieger NA, Wattchow DA. Positive proximal resection margins after resection for carcinoma of the oesophagus and stomach: effect on survival and symptom recurrence. Aust N Z J Surg. 1996;66(11):734–7.PubMedCrossRef
31.
go back to reference Songun I, Bonenkamp JJ, Hermans J, van Krieken JH, van de Velde CJ. Prognostic value of resection-line involvement in patients undergoing curative resections for gastric cancer. Eur J Cancer. 1996;32A(3):433–7.PubMedCrossRef Songun I, Bonenkamp JJ, Hermans J, van Krieken JH, van de Velde CJ. Prognostic value of resection-line involvement in patients undergoing curative resections for gastric cancer. Eur J Cancer. 1996;32A(3):433–7.PubMedCrossRef
32.
go back to reference Jeong O, Choi WY, Park YK. Appropriate selection of patients for combined organ resection in cases of gastric carcinoma invading adjacent organs. J Surg Oncol. 2009;100(2):115–20.PubMedCrossRef Jeong O, Choi WY, Park YK. Appropriate selection of patients for combined organ resection in cases of gastric carcinoma invading adjacent organs. J Surg Oncol. 2009;100(2):115–20.PubMedCrossRef
33.
go back to reference Zhang M, Zhang H, Ma Y, Zhu G, Xue Y. Prognosis and surgical treatment of gastric cancer invading adjacent organs. ANZ J Surg. 2010;80(7–8):510–4.PubMedCrossRef Zhang M, Zhang H, Ma Y, Zhu G, Xue Y. Prognosis and surgical treatment of gastric cancer invading adjacent organs. ANZ J Surg. 2010;80(7–8):510–4.PubMedCrossRef
34.
go back to reference Kitamura K, Tani N, Koike H, Nishida S, Ichikawa D, Taniguchi H, et al. Combined resection of the involved organs in T4 gastric cancer. Hepatogastroenterology. 2000;47(36):1769–72.PubMed Kitamura K, Tani N, Koike H, Nishida S, Ichikawa D, Taniguchi H, et al. Combined resection of the involved organs in T4 gastric cancer. Hepatogastroenterology. 2000;47(36):1769–72.PubMed
35.
go back to reference Ozer I, Bostanci E, Orug T, Ozogul Y, Ulas M, Ercan M, et al. Surgical outcomes and survival after multiorgan resection for locally advanced gastric cancer. Am J Surg. 2009;198(1):25–30.PubMedCrossRef Ozer I, Bostanci E, Orug T, Ozogul Y, Ulas M, Ercan M, et al. Surgical outcomes and survival after multiorgan resection for locally advanced gastric cancer. Am J Surg. 2009;198(1):25–30.PubMedCrossRef
36.
go back to reference Saito H, Tsujitani S, Maeda Y, Fukuda K, Yamaguchi K, Ikeguchi M, et al. Combined resection of invaded organs in patients with T4 gastric carcinoma. Gastric Cancer. 2001;4(4):206–11.PubMedCrossRef Saito H, Tsujitani S, Maeda Y, Fukuda K, Yamaguchi K, Ikeguchi M, et al. Combined resection of invaded organs in patients with T4 gastric carcinoma. Gastric Cancer. 2001;4(4):206–11.PubMedCrossRef
37.
go back to reference Sano T, Mudan SS. No advantage of reoperation for positive resection margins in node positive gastric cancer patients? Jpn J Clin Oncol. 1999;29(6):283–4.PubMedCrossRef Sano T, Mudan SS. No advantage of reoperation for positive resection margins in node positive gastric cancer patients? Jpn J Clin Oncol. 1999;29(6):283–4.PubMedCrossRef
38.
go back to reference Ferriero JA, Myers JL, Bostwick DG. Accuracy of frozen-section diagnosis in surgical pathology—review of a 1-year experience with 24,880 cases at Mayo-Clinic Rochester. Mayo Clin Proc. 1995;70(12):1137–41.CrossRef Ferriero JA, Myers JL, Bostwick DG. Accuracy of frozen-section diagnosis in surgical pathology—review of a 1-year experience with 24,880 cases at Mayo-Clinic Rochester. Mayo Clin Proc. 1995;70(12):1137–41.CrossRef
39.
go back to reference Mcdonald JS. Gastric cancer—new therapeutic options. N Engl J Med. 2006;355(1):76–7.CrossRef Mcdonald JS. Gastric cancer—new therapeutic options. N Engl J Med. 2006;355(1):76–7.CrossRef
Metadata
Title
Systematic review of the predictors of positive margins in gastric cancer surgery and the effect on survival
Authors
Hamid Reza Raziee
Roberta Cardoso
Rajini Seevaratnam
Alyson Mahar
Lucy Helyer
Calvin Law
Natalie Coburn
Publication date
01-09-2012
Publisher
Springer Japan
Published in
Gastric Cancer / Issue Special Issue 1/2012
Print ISSN: 1436-3291
Electronic ISSN: 1436-3305
DOI
https://doi.org/10.1007/s10120-011-0112-7

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