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Laparoscopic versus open subtotal gastrectomy for adenocarcinoma of the stomach in a Western population: peri-operative and 5-year oncological outcomes

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Abstract

Background

This study compares the peri-operative and long-term oncological outcomes for laparoscopic subtotal gastrectomy (LSG) versus open subtotal gastrectomy (OSG) for adenocarcinoma of the stomach in a Western population.

Methods

A retrospective, intention-to-treat analysis study was conducted for consecutive patients undergoing gastrectomy with curative intent for adenocarcinoma of the stomach between November 2006 and October 2016. Univariate analysis was used to compare peri-operative outcomes between LSG and OSG. Logistic regression with bootstrapping validation was used to identify independent risk factors for predicting 2-year overall survival.

Results

The final analysis included 79 patients. When comparing LSG (n = 30) to OSG (n = 49), there was no difference in the number of resected lymph nodes (36 (IQR 24.3–44) vs. 42 (IQR 28–59), p = 0.165), a reduction in intra-operative blood loss (150 ml (IQR 100–250) vs. 553 ml (IQR 338–1075), p < 0.001) and an increase incidence of post-operative bleeding (3 patients vs. 0, p = 0.024), respectively. Five-year overall survival for LSG (n = 22) versus OSG (n = 20) was 63.6% and 50% (p = 0.372), respectively. The number of positive lymph nodes [OR 0.64 (CI 0.47–0.88), p = 0.006] was the only significant independent risk factor for 2-year overall survival. Pre-operative ASA grading and operative approach did not influence survival outcomes at 2 years.

Conclusion

This study suggests that LSG is comparable to OSG in Western patients with respect to oncological quality and peri-operative morbidity. Two-year overall survival is predicted by the number of positive lymph nodes and not the operative access employed for resection.

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References

  1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al (2012) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN. Int J Cancer 136(5):E359–E386

    Article  CAS  Google Scholar 

  2. Washington K (2010) 7th edition of the AJCC cancer staging manual: stomach. Ann Surg Oncol 17(12):3077–3079

    Article  PubMed  Google Scholar 

  3. Tada M, Murakami A, Karita M, Yanai H, Okita K (1993) Endoscopic resection of early gastric cancer. Endoscopy 25(7):445–450

    Article  CAS  PubMed  Google Scholar 

  4. Balmadrid B, Hwang JH (2015) Endoscopic resection of gastric and esophageal cancer. Gastroenterol Rep (Oxf) 3(4):330–338

    Google Scholar 

  5. Japanese Gastric Cancer Association (2011) Japanese gastric cancer treatment guidelines: 3rd English Edition. Gastric Cancer 14(2):113–123

    Article  Google Scholar 

  6. Waddell T, Verheij M, AllumW Cunningham D, Cervantes A, Arnold D (2013) Gastric cancer: ESMO-ESSO-ESTRO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi57–vi63

    Article  PubMed  Google Scholar 

  7. Cunningham D, Allum WH, Stenning SP, Thompson JN, Van de Velde CJ, Nicolson M et al (2006) Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med 355(1):11–20

    Article  CAS  PubMed  Google Scholar 

  8. Ronellenfitsch U, Schwarzbach M, Hofheinz R, Kienle P, Kieser M, Slanger TE et al (2013) Perioperative chemo(radio)therapy versus primary surgery for resectable adenocarcinoma of the stomach, gastroesophageal junction, and lower esophagus. Cochrane Database Syst Rev 5:CD008107

    Google Scholar 

  9. Association of Upper Gastrointestinal Surgeons of Great Britain and Ireland. National Oesophago-gastric Cancer Audit Annual Report. https://www.nogca.org.uk/content/uploads/2017/12/NOGCA-Annual-Report-2017.pdf. Accessed 3 Nov 2018

  10. McCulloch P, Nita ME, Kazi H, Gama-Rodrigues J (2004) Extended versus limited lymph nodes dissection technique for adenocarcinoma of the stomach. Cochrane Database Syst Rev 4:CD001964

    Google Scholar 

  11. Cuschieri A (1986) Gastrectomy for gastric cancer: definitions and objectives. Br J Surg 73:513–514

    CAS  PubMed  Google Scholar 

  12. Siewert JR, Sendler A (1999) The current management of gastric cancer. Adv Surg 33:69–93

    CAS  PubMed  Google Scholar 

  13. Hioki K, Nakane Y, Yamamoto M (1990) Surgical strategy for early gastric cancer. Br J Surg 77:1330–1334

    Article  CAS  PubMed  Google Scholar 

  14. Cuschieri SA, Hanna GB (2014) Meta-analysis of D1 versus D2 gastrectomy for gastric adenocarcinoma: let us move on to another era. Ann Surg 259(6):e90

    Article  PubMed  Google Scholar 

  15. Degiuli M, Sasako M, Ponti A, Vendrame A, Tomatis M, Mazza C, Borasi A et al (2014) Randomized clinical trial comparing survival after D1 or D2 gastrectomy for gastric cancer. Br J Surg 101(2):23–31

    CAS  PubMed  Google Scholar 

  16. Memon MA, Subramanya MS, Khan S, Hossain MB, Osland E, Memon B (2011) Meta-analysis of D1 versus D2 gastrectomy for gastric adenocarcinoma. Ann Surg 253(5):900–911

    Article  PubMed  Google Scholar 

  17. Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ (2010) Surgical treatment of gasric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 11(5):439–449

    Article  PubMed  Google Scholar 

  18. Kitano S, Iso Y, Moriyama M, Sugimachi K (1994) Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 4(2):146–148

    CAS  PubMed  Google Scholar 

  19. Hayashi H, Ochiai T, Shimada H, Gunji Y (2005) Prospective randomized study of open versus laparoscopy-assisted distal gastrectomy with extraperigastric lymph node dissection for early gastric cancer. Surg Endosc 19(9):1172–1176

    Article  CAS  PubMed  Google Scholar 

  20. Kim HH, Hyung WJ, Cho GS, KimMC Han SU, Kim W et al (2010) Morbidity and mortality of laparoscopic gastrectomy versus open gastrectomy for gastric cancer: an interim report—a phase III multicentre, prospective, randomized trial (KLASS trial). Ann Surg 251(3):417–420

    Article  PubMed  Google Scholar 

  21. Kitano S, Shiraishi N, Fujii K, Yasuda K, Inomata M, Adachi Y (2002) A randomized controlled trial comparing open vs laparoscopy-assisted distal gastrectomy for the treatment of early gastric cancer: an interim report. Surgery 131(1 Suppl):S306–S311

    Article  PubMed  Google Scholar 

  22. Lee JH, Nam BH, Ryu KW, Ryu SY, Park YK, Kim S, Kim YW (2015) Comparison of outcomes after laparoscopy-assisted and open total gastrectomy for early gastric cancer. Br J Surg 102(12):1500–1505

    Article  CAS  PubMed  Google Scholar 

  23. Sakuramoto S, Yamashita K, Kikuchi S, Futawatari N, Katada N, Watanabe M et al (2013) Laparoscopy versus open distal gastrectomy by expert surgeons for early gastric cancer in Japanese patients: short-term clinical outcomes of a randomized clinical trial. Surg Endosc 27(5):1695–1705

    Article  PubMed  Google Scholar 

  24. Hayashi H, Ochiai T, Shimada H, Gunji Y (2005) Prospective randomized study of open versus laparoscopy-assisted distal gastrectomy with extraperigastric lymph node dissection for early gastric cancer. Surg Endosc 19:1172–1176

    Article  CAS  PubMed  Google Scholar 

  25. Kim YW, Baik YH, Yun YH, Nam BH, Kim DH, Choi IJ et al (2008) Improved quality of life outcomes after laparoscopy-assisted distal gastrectomy for early gastric cancer: results of a prospective randomized clinical trial. Ann Surg 248:721–727

    Article  PubMed  Google Scholar 

  26. Kostakis ID, Alexandrou A, Armeni E, Damaskos C, Kouraklis G, Diamantis T et al (2017) Comparison between minimally invasive and open gastrectomy for gastric cancer in Europe: a systematic review and meta-analysis. Scand J Surg 106(1):3–20

    Article  CAS  PubMed  Google Scholar 

  27. Deng Y, Zhang Y, Guo TK (2015) Laparoscopy-assisted versus open distal gastrectomy for early gastric cancer: a meta-analysis based on seven randomized controlled trials. Surg Oncol 24:71–77

    Article  CAS  PubMed  Google Scholar 

  28. Vinuela EF, Gonen M, Brennan MF, Coit DG, Strong VE (2012) Laparoscopic versus open distal gastrectomy for gastric cancer: a meta-analysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg 255(3):446–456

    Article  PubMed  Google Scholar 

  29. Jiang L, Yang KH, Guan QL, Cao N, Chen Y, Zhao P et al (2013) Laparoscopy-assisted gastrectomy versus open gastrectomy for resectable gastric cancer: an update meta-analysis based on randomized controlled trials. Surg Endosc 27(7):2466–2480

    Article  PubMed  Google Scholar 

  30. Zeng YK, Yang ZL, Peng JS, Lin HS, Cai L (2012) Laparoscopy-assisted versus open distal gastrectomy for early gastric cancer: evidence from randomized and nonrandomized clinical trials. Ann Surg 256(1):39–52

    Article  PubMed  Google Scholar 

  31. Huscher CG, Mingoli A, Sgarzini G, Sansonetti A, Massimiliano DP, Recher A et al (2005) Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 241:232–237

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hu YF, Huang CM, Sun YH, Su XQ, Li ZY, Xue YW et al (2015) Laparoscopic d2 distal gastrectomy versus conventional open surgery for advanced gastric cancer: the safety analysis from a multicentre prospective randomized controlled trial in china (CLASS-01 trial). J Clin Oncol 33(15 Suppl):1

    CAS  Google Scholar 

  33. Nam BH, Kim YW, Reim D, Eom BW, Yu WS, Park YK et al (2013) Laparoscopy assisted versus open distal gastrectomy with D2 lymph node dissection for advanced gastric cancer: design and rationale of a phase II randomized controlled multicentre trial (COACT 1001). J Gastric Cancer 13(3):164–171

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kinoshita T, Uyama I, Terashima M, Noshiro H, Nagai E, Obama K et al (2019) Long-term outcomes of laparoscopic versus open surgery for clinical stage II/III gastric cancer: a Multicenter Cohort Study in Japan (LOC-A Study). Ann Surg 269(5):887–894

    Article  PubMed  Google Scholar 

  35. Griffin SM (2005) Gastric cancer in the East: same disease, different patient. Br J Surg 92(9):1055–1056

    Article  CAS  PubMed  Google Scholar 

  36. Brenkman HJF, Gisbertz SS, Slaman AE, Goense L, Ruurda JP, van Berge Henegouwen MI et al (2017) Postoperative outcomes of minimally invasive gastrectomy versus open gastrectomy during the early introduction of minimally invasive gastrectomy in the Netherlands: a population-based cohort study. Ann Surg 266(5):831–838

    Article  PubMed  Google Scholar 

  37. Haverkamp L, Brenkman HJ, Seesing MF, Gisbertz SS, van Berge Henegouwen MI, Luyer MD et al (2015) Laparoscopic versus open gastrectomy for gastric cancer, a multicentre prospectively randomized controlled trial (LOGICA-trial). BMC Cancer 15:556

    Article  PubMed  PubMed Central  Google Scholar 

  38. Straatman J, van der Wielen N, Cuesta MA, Gisbertz SS, Hartemink KJ, Alonso Poza A et al (2015) Surgical techniques, open versus minimally invasive gastrectomy after chemotherapy (STOMACH trial): study protocol for a randomized controlled trial. Trials 16:123

    Article  PubMed  PubMed Central  Google Scholar 

  39. Pugliese R, Maggioni D, Sansonna F, Ferrari GC, Lernia SD, Forgione A et al (2010) Subtotal gastrectomy with D2 dissection by minimally invasive surgery for distal ad-enocarcinoma of the stomach: results and 5-year survival. Surg Endosc 24:2594–2602

    Article  PubMed  Google Scholar 

  40. Ludwig K, Schneider-Koriath S, Scharlau U, Steffen H, Möller D, Bernhardt J (2018) Totally laparoscopic versus open gastrectomy for gastric cancer: a matched pair analysis. Zentralbl Chir 143(2):145–154

    Article  PubMed  Google Scholar 

  41. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, Initiative STROBE (2007) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370(9596):1453–1457

    Article  Google Scholar 

  42. Griffin SM, Raimes SA, Shenfine J (2011) Oesophagogastric surgery: a companion to specialist surgical practice, 5th edn. Elsevier Publishing, London

    Google Scholar 

  43. Association JGC (2010) Japanese gastric cancer treatment guidelines (ver. 3). Gastric Cancer 14(2):113–123

    Article  Google Scholar 

  44. Bruce J, Krukowski ZH, Al-Khairy G, Russell EM, Park KG (2001) Systematic review of the definition and measurement of anastomotic leak after gastrointestinal surgery. Br J Surg 88(9):1157–1168

    Article  CAS  PubMed  Google Scholar 

  45. American Thoracic Society, Infectious Diseases Society of America (2005) Guidelines for the management of adults with hospital-acquired, ventilator associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med 171:388–416

    Article  Google Scholar 

  46. Markar SR, Wiggins T, Ni M, Steyerberg EW, Van Lanschot JJ, Sasako M et al (2015) Assessment of the quality of surgery within randomised controlled trials for the treatment of gastro-oesophageal cancer: a systematic review. Lancet Oncol 16(1):e23–e31

    Article  PubMed  Google Scholar 

  47. Abbassi-Ghadi N, Boshier PR, Goldin R, Hanna GB (2012) Techniques to increase lymph node harvest from gastrointestinal cancer specimens: a systematic review and meta-analysis. Histopathology 61(4):531–542

    Article  PubMed  Google Scholar 

  48. Achen MG, McColl BK, Stacker SA (2005) Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7:121–127

    Article  CAS  PubMed  Google Scholar 

  49. Siewert JR, Bottcher K, Stein HJ, Roder JD (1998) Relevant prognostic factors in gastric cancer: ten year results of the German Gastric Cancer Study. Ann Surg 228(4):449–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sava J, Velmahos GC, Karaiskakis M, Kirkman P, Toutouzas K, Sarkisyan G et al (2003) Abdominal insufflation for prevention of exsanguination. J Trauma Inj Infect Crit Care 54(3):590–594

    Article  Google Scholar 

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Acknowledgements

The authors received no financial support for this work. The authors would like to show their gratitude to Sukhpal Singh, Krishna K Singh and Yuen Soon who perfomed surgeries in this cohort of patients. We would also like to thank Izhar Bagwan and Poonam Pingle for the histopathological assessment of the cancer resection specimens.

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Correspondence to Shaun R. Preston.

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Drs. N Abbassi-Ghadi, S Durakovic, G Piessen, P Gatenby, J Sultan, SR Preston have no conflicts of interest or financial ties to disclose.

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Abbassi-Ghadi, N., Durakovic, S., Piessen, G. et al. Laparoscopic versus open subtotal gastrectomy for adenocarcinoma of the stomach in a Western population: peri-operative and 5-year oncological outcomes. Surg Endosc 34, 3818–3826 (2020). https://doi.org/10.1007/s00464-019-07146-6

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