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Published in: World Journal of Surgical Oncology 1/2018

Open Access 01-12-2018 | Research

A comparison of the operative outcomes of D1 and D2 gastrectomy performed at a single Western center with multiple surgeons: a retrospective analysis with propensity score matching

Authors: Susanna Lam, Elinor Tan, Audrey Menezes, David Martin, James Gallagher, David Storey, Charbel Sandroussi

Published in: World Journal of Surgical Oncology | Issue 1/2018

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Abstract

Background

There has been worldwide debate on lymphadenectomy for gastric cancer, with increasing consensus on performing an extended (D2) resection. There is a paucity of data in Australia. Our aim is to compare overall outcomes between a D1 and D2 lymphadenectomy for gastric cancer in a single specialist unit.

Methods

We performed a retrospective analysis on patients who underwent a curative primary gastric resection for gastric adenocarcinoma between January 1996 and April 2016, primary outcomes included overall survival (OS) and disease-free survival (DFS). Propensity score matching (PSM) analysis was used to balance covariates between D1/D1+ and D2 groups. Kaplan-Meier survival curves of D1/D1+ versus D2 were constructed and evaluated using the log-rank test with subgroup analyses for pathological node (pN) status. Multiple Cox proportional hazards model was used to determine predictors of overall survival.

Results

Two hundred four patients underwent a gastrectomy, 54 had D1/D1+, and 150 had a D2 lymphadenectomy. After PSM, there were 39 patients in each group, the 10-year OS for D1/D1+ was 52.1 and 76.2% for D2 (p = 0.008), and 10-year DFS was 35% for D1 and 58.1% for D2 (p = 0.058). Subgroup analysis showed that node-negative (N0) patients had improved 5-year OS for D2 (90.9%), compared to D1/D1+ (76.4%) (p = 0.028). There was no difference in operative mortality between the groups (D1 vs D2: 2 vs 0%, p = 0.314), nor in post-operative complications (p = 0.227). Multiple Cox analysis showed advanced tumor stage (stages III and IV), and lymphadenectomy type (D1) and the presence of postoperative complications were independent predictors of poor overall survival.

Conclusions

D2 lymphadenectomy with spleen and pancreas preservation can be performed safely on patients with gastric adenocarcinoma. Significant improvement in overall survival is observed in patients with N0 disease who underwent D2 lymphadenectomy without increasing operative morbidity or mortality. This paper supports the notion of a global consensus for a D2 lymphadenectomy, particularly in the Western context.
Literature
1.
go back to reference Ferlay JSI, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2014;136(5):E359–86.CrossRefPubMed Ferlay JSI, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2014;136(5):E359–86.CrossRefPubMed
2.
go back to reference AIHW. Cancer in Australia: an overview 2014. Canberra: Australian Institute of Health and Welfare; 2014. AIHW. Cancer in Australia: an overview 2014. Canberra: Australian Institute of Health and Welfare; 2014.
3.
go back to reference Maehara YOH, Okuyama T, Moriguchi S, Tsujitani S, Korenaga D, Sugimachi K. Predictors of lymph node metastasis in early gastric cancer. Br J Cancer. 1992;79(3):245–7. Maehara YOH, Okuyama T, Moriguchi S, Tsujitani S, Korenaga D, Sugimachi K. Predictors of lymph node metastasis in early gastric cancer. Br J Cancer. 1992;79(3):245–7.
5.
go back to reference Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20(1):1–19.CrossRef Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20(1):1–19.CrossRef
6.
go back to reference Cuschieri AWS, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P. Patient survival after D 1 and D 2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Br J Cancer. 1999;79(9–10):1522–30.CrossRefPubMedPubMedCentral Cuschieri AWS, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P. Patient survival after D 1 and D 2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Br J Cancer. 1999;79(9–10):1522–30.CrossRefPubMedPubMedCentral
7.
go back to reference Hartgrink HH vVC, Putter H, Bonenkamp JJ, Klein Kranenbarg E, Songun I, Welvaart K, van Krieken JH, Meijer S, Plukker JT, van Elk PJ, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Sasako M. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol. 2004;22(11):2069–77.CrossRefPubMed Hartgrink HH vVC, Putter H, Bonenkamp JJ, Klein Kranenbarg E, Songun I, Welvaart K, van Krieken JH, Meijer S, Plukker JT, van Elk PJ, Obertop H, Gouma DJ, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Sasako M. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol. 2004;22(11):2069–77.CrossRefPubMed
8.
go back to reference Songun I, Putter H, Kranenbarg EM-K, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. The lancet oncology. 2010;11(5):439–49.CrossRefPubMed Songun I, Putter H, Kranenbarg EM-K, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. The lancet oncology. 2010;11(5):439–49.CrossRefPubMed
9.
go back to reference Degiuli M, Sasako M, Ponti A, Vendrame A, Tomatis M, Mazza C, Borasi A, Capussotti L, Fronda G, Morino M, et al. Randomized clinical trial comparing survival after D1 or D2 gastrectomy for gastric cancer. Br J Surg. 2014;101(2):23–31.CrossRefPubMed Degiuli M, Sasako M, Ponti A, Vendrame A, Tomatis M, Mazza C, Borasi A, Capussotti L, Fronda G, Morino M, et al. Randomized clinical trial comparing survival after D1 or D2 gastrectomy for gastric cancer. Br J Surg. 2014;101(2):23–31.CrossRefPubMed
10.
go back to reference Thomson I, Gotley D, Barbour A, Martin I, Jayasuria N, Thomas J, Smithers B. Treatment results of curative gastric resection from a specialist Australian unit: low volume with satisfactory outcomes. Gastric Cancer. 2014;17(1):152–60.CrossRefPubMed Thomson I, Gotley D, Barbour A, Martin I, Jayasuria N, Thomas J, Smithers B. Treatment results of curative gastric resection from a specialist Australian unit: low volume with satisfactory outcomes. Gastric Cancer. 2014;17(1):152–60.CrossRefPubMed
11.
go back to reference Sano T, Sasako M, Mizusawa J, Yamamoto S, Katai H, Yoshikawa T, Nashimoto A, Ito S, Kaji M, Imamura H, et al. Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma. Ann Surg. 2017;265(2):277–83.CrossRefPubMed Sano T, Sasako M, Mizusawa J, Yamamoto S, Katai H, Yoshikawa T, Nashimoto A, Ito S, Kaji M, Imamura H, et al. Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma. Ann Surg. 2017;265(2):277–83.CrossRefPubMed
12.
go back to reference Washington K. 7th edition of the AJCC Cancer staging manual: stomach. Ann Surg Oncol. 2010;17(12):3077–9.CrossRefPubMed Washington K. 7th edition of the AJCC Cancer staging manual: stomach. Ann Surg Oncol. 2010;17(12):3077–9.CrossRefPubMed
13.
go back to reference Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRef Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer. 2011;14:101–12.CrossRef
14.
go back to reference Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96.CrossRefPubMed Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96.CrossRefPubMed
15.
go back to reference D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med. 1998;17(19):2265–81.CrossRefPubMed D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med. 1998;17(19):2265–81.CrossRefPubMed
16.
go back to reference Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Mulitvariate Behavior Research. 2011;46(3):399–424.CrossRef Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Mulitvariate Behavior Research. 2011;46(3):399–424.CrossRef
17.
go back to reference Austin PC. Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat. 2010;10:150–61.CrossRefPubMedCentral Austin PC. Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat. 2010;10:150–61.CrossRefPubMedCentral
18.
go back to reference McMurry TL, Hu Y, Blackstone EH, Kozower BD. Propensity scores: methods, considerations, and applications in the journal of thoracic and cardiovascular surgery. J Thorac Cardiovasc Surg. 2015;150(1):14–9.CrossRefPubMed McMurry TL, Hu Y, Blackstone EH, Kozower BD. Propensity scores: methods, considerations, and applications in the journal of thoracic and cardiovascular surgery. J Thorac Cardiovasc Surg. 2015;150(1):14–9.CrossRefPubMed
19.
go back to reference Elze MC, Gregson J, Baber U, Williamson E, Sartori S, Mehran R, Nichols M, Stone GW, Pocock SJ. Comparison of propensity score methods and covariate adjustment: evaluation in 4 cardiovascular studies. J Am Coll Cardiol. 2017;69(3):345–57.CrossRefPubMed Elze MC, Gregson J, Baber U, Williamson E, Sartori S, Mehran R, Nichols M, Stone GW, Pocock SJ. Comparison of propensity score methods and covariate adjustment: evaluation in 4 cardiovascular studies. J Am Coll Cardiol. 2017;69(3):345–57.CrossRefPubMed
20.
go back to reference Brookhart MA, Schneeweiss S, Rothman KJ, Glynn RJ, Avorn J, Stürmer T. Variable selection for propensity score models. Am J Epidemiol. 2006;163(12):1149–56.CrossRefPubMedPubMedCentral Brookhart MA, Schneeweiss S, Rothman KJ, Glynn RJ, Avorn J, Stürmer T. Variable selection for propensity score models. Am J Epidemiol. 2006;163(12):1149–56.CrossRefPubMedPubMedCentral
21.
go back to reference Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of US adults. N Engl J Med. 2003;348(17):1625–38.CrossRefPubMed Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of US adults. N Engl J Med. 2003;348(17):1625–38.CrossRefPubMed
22.
go back to reference Noguchi Y, Yoshikawa T, Tsuburaya A, Motohashi H, Karpeh MS, Brennan MF. Is gastric carcinoma different between Japan and the United States? Cancer. 2000;89(11):2237–46.CrossRefPubMed Noguchi Y, Yoshikawa T, Tsuburaya A, Motohashi H, Karpeh MS, Brennan MF. Is gastric carcinoma different between Japan and the United States? Cancer. 2000;89(11):2237–46.CrossRefPubMed
23.
go back to reference Maruyama K. The most important prognostic factors for gastric cancer patients: a study using univariate and multivariate analyses. Scand J Gastroenterol. 1987;22(sup133):63–8.CrossRef Maruyama K. The most important prognostic factors for gastric cancer patients: a study using univariate and multivariate analyses. Scand J Gastroenterol. 1987;22(sup133):63–8.CrossRef
24.
go back to reference Siewert JR, Böttcher 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.CrossRefPubMedPubMedCentral Siewert JR, Böttcher 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.CrossRefPubMedPubMedCentral
25.
go back to reference Röcken C, Behrens HM. Validating the prognostic and discriminating value of the TNM-classification for gastric cancer—a critical appraisal. Eur J Cancer. 2015;51(5):577–86.CrossRefPubMed Röcken C, Behrens HM. Validating the prognostic and discriminating value of the TNM-classification for gastric cancer—a critical appraisal. Eur J Cancer. 2015;51(5):577–86.CrossRefPubMed
26.
go back to reference Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.CrossRefPubMed Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M, Scarffe JH, Lofts FJ, Falk SJ, Iveson TJ. Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med. 2006;355(1):11–20.CrossRefPubMed
27.
go back to reference DW a H, Lemeshow S. Applied Survival Analysis. In: Regression modeling of time to event data. United States of America: John Wiley & Sons, INC; 1999. DW a H, Lemeshow S. Applied Survival Analysis. In: Regression modeling of time to event data. United States of America: John Wiley & Sons, INC; 1999.
28.
go back to reference Bauer KSM, Porzsolt F, Henne-Bruns D. Comparison of international guidelines on the accompanying therapy for advanced gastric cancer: reasons for the differences. Journal of Gastric Cancer. 2015;15(1):10–8.CrossRefPubMedPubMedCentral Bauer KSM, Porzsolt F, Henne-Bruns D. Comparison of international guidelines on the accompanying therapy for advanced gastric cancer: reasons for the differences. Journal of Gastric Cancer. 2015;15(1):10–8.CrossRefPubMedPubMedCentral
29.
go back to reference Degiuli MMG, Leo AD, D’Ugo D, Galasso E, Marrelli D, Petrioli R, Polom K, Roviello F, Santullo F, Morino M. Gastric cancer: current status of lymph node dissection. World J Gastroenterol. 2016;22(10):2875–93.CrossRefPubMedPubMedCentral Degiuli MMG, Leo AD, D’Ugo D, Galasso E, Marrelli D, Petrioli R, Polom K, Roviello F, Santullo F, Morino M. Gastric cancer: current status of lymph node dissection. World J Gastroenterol. 2016;22(10):2875–93.CrossRefPubMedPubMedCentral
30.
go back to reference Smith DLEL, Learn PA, Raut CP, Mansfield PF. Factors influencing the volume-outcome relationship in gastrectomies: a population-based study. Ann Oncol. 2007;14(6):1846–52.CrossRef Smith DLEL, Learn PA, Raut CP, Mansfield PF. Factors influencing the volume-outcome relationship in gastrectomies: a population-based study. Ann Oncol. 2007;14(6):1846–52.CrossRef
31.
go back to reference El-Sedfy A, Dixon M, Seevaratnam R, Bocicariu A, Cardoso R, Mahar A, Kiss A, Helyer L, Law C, Coburn NG. Personalized surgery for gastric adenocarcinoma: a meta-analysis of D1 versus D2 lymphadenectomy. Ann Surg Oncol. 2015;22(6):1820–7.CrossRefPubMed El-Sedfy A, Dixon M, Seevaratnam R, Bocicariu A, Cardoso R, Mahar A, Kiss A, Helyer L, Law C, Coburn NG. Personalized surgery for gastric adenocarcinoma: a meta-analysis of D1 versus D2 lymphadenectomy. Ann Surg Oncol. 2015;22(6):1820–7.CrossRefPubMed
32.
go back to reference Sasako MST, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, YamamuraY, Okajima K. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med. 2008;359(5):453–62.CrossRefPubMed Sasako MST, Yamamoto S, Kurokawa Y, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, YamamuraY, Okajima K. D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med. 2008;359(5):453–62.CrossRefPubMed
33.
go back to reference Saito HKH, Matsunaga T, Fukuda K, Tatebe S, Tsujitani S, Ikeguchi M. Prognostic indicators in node-negative advanced gastric cancer patients. J Surg Oncol. 2010;101(7):622–5.CrossRefPubMed Saito HKH, Matsunaga T, Fukuda K, Tatebe S, Tsujitani S, Ikeguchi M. Prognostic indicators in node-negative advanced gastric cancer patients. J Surg Oncol. 2010;101(7):622–5.CrossRefPubMed
34.
go back to reference J-y H, Y-y X, Li M, Sun Z, Zhu Z, Y-x S, Z-f M, Wu J-h, H-m X. The prognostic impact of occult lymph node metastasis in node-negative gastric cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2013;20(12):3927–34.CrossRef J-y H, Y-y X, Li M, Sun Z, Zhu Z, Y-x S, Z-f M, Wu J-h, H-m X. The prognostic impact of occult lymph node metastasis in node-negative gastric cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2013;20(12):3927–34.CrossRef
35.
go back to reference Chadwich GVM, Brand C, Cromwell D, Riley S, Crosby T, Michalowski J. National oesiphago-gastric cancer audit. London: Healthcare Quality Improvement Partnership Ltd (HQIP); 2016. Chadwich GVM, Brand C, Cromwell D, Riley S, Crosby T, Michalowski J. National oesiphago-gastric cancer audit. London: Healthcare Quality Improvement Partnership Ltd (HQIP); 2016.
36.
go back to reference Park CHSK, Kim SN. Treatment results for gastric cancer surgery: 12 years’ experience at a single institute in Korea. Eur J Surg Oncol. 2008;34(1):36–41.CrossRefPubMed Park CHSK, Kim SN. Treatment results for gastric cancer surgery: 12 years’ experience at a single institute in Korea. Eur J Surg Oncol. 2008;34(1):36–41.CrossRefPubMed
37.
go back to reference Bozzetti F, Marubini E, Bonfanti G, Miceli R, Piano C, Crose N, Gennari L. Total versus subtotal gastrectomy: surgical morbidity and mortality rates in a multicenter Italian randomized trial. The Italian gastrointestinal tumor study group. Ann Surg. 1997;226(5):613–20.CrossRefPubMedPubMedCentral Bozzetti F, Marubini E, Bonfanti G, Miceli R, Piano C, Crose N, Gennari L. Total versus subtotal gastrectomy: surgical morbidity and mortality rates in a multicenter Italian randomized trial. The Italian gastrointestinal tumor study group. Ann Surg. 1997;226(5):613–20.CrossRefPubMedPubMedCentral
38.
go back to reference Sanchez LJ, Sylvester MJ, Zhang S, Mariotti V, Duma N, Wang Y, Parrondo R, Eloy JA, Gutierrez M. Post-gastrectomy complications and mortality in elderly patients with gastric cancer: a population-based study. J Clin Oncol. 2016;34(15_suppl):e21533.CrossRef Sanchez LJ, Sylvester MJ, Zhang S, Mariotti V, Duma N, Wang Y, Parrondo R, Eloy JA, Gutierrez M. Post-gastrectomy complications and mortality in elderly patients with gastric cancer: a population-based study. J Clin Oncol. 2016;34(15_suppl):e21533.CrossRef
39.
go back to reference Edwards P, Blackshaw P, Barry J, Jones R, Lewis W. Randomised comparison of D1versusmodified D2 gastrectomy for gastric cancer. Br J Surg-Supplement. 2003;90:30.CrossRef Edwards P, Blackshaw P, Barry J, Jones R, Lewis W. Randomised comparison of D1versusmodified D2 gastrectomy for gastric cancer. Br J Surg-Supplement. 2003;90:30.CrossRef
40.
go back to reference Bartlett EKRR, Kelz RR, Drebin JA, Fraker DL, Karakousis GC. Morbidity and mortality after total gastrectomy for gastric malignancy using the American College of Surgeons National Surgical Quality Improvement Program database. Surgery. 2014;157(2):406–507. Bartlett EKRR, Kelz RR, Drebin JA, Fraker DL, Karakousis GC. Morbidity and mortality after total gastrectomy for gastric malignancy using the American College of Surgeons National Surgical Quality Improvement Program database. Surgery. 2014;157(2):406–507.
41.
go back to reference Jiang LYK, Guan QL, Zhao P, Chen Y, Tian JH. Survival and recurrence free benefits with different lymphadenectomy for resectable gastric cancer: a meta-analysis. J Surg Oncol. 2013;107(8):807–14.CrossRefPubMed Jiang LYK, Guan QL, Zhao P, Chen Y, Tian JH. Survival and recurrence free benefits with different lymphadenectomy for resectable gastric cancer: a meta-analysis. J Surg Oncol. 2013;107(8):807–14.CrossRefPubMed
42.
go back to reference Wu CWHC, Lo SS, Hsieh MC, Shia LT, Whang-Peng J. Randomized clinical trial of morbidity after D1 and D3 surgery for gastric cancer. Br J Surg. 2004;91:283–7.CrossRefPubMed Wu CWHC, Lo SS, Hsieh MC, Shia LT, Whang-Peng J. Randomized clinical trial of morbidity after D1 and D3 surgery for gastric cancer. Br J Surg. 2004;91:283–7.CrossRefPubMed
Metadata
Title
A comparison of the operative outcomes of D1 and D2 gastrectomy performed at a single Western center with multiple surgeons: a retrospective analysis with propensity score matching
Authors
Susanna Lam
Elinor Tan
Audrey Menezes
David Martin
James Gallagher
David Storey
Charbel Sandroussi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2018
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-018-1422-6

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