Skip to main content


Log in

Technical aspects and short- and long-term outcomes of totally laparoscopic total gastrectomy for advanced gastric cancer: a single-institution retrospective study

  • Dynamic Manuscript
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript



D2 total gastrectomy combined with splenectomy or pancreaticosplenectomy reportedly increases morbidity and mortality. Totally laparoscopic total gastrectomy (TLTG) for advanced gastric cancer (AGC) remains controversial because of its technical difficulties and lack of long-term results. We determined the feasibility and safety of TLTG for AGC.


A single-institution retrospective study was conducted. Ninety-two consecutive AGC patients who underwent radical TLTG were enrolled. The primary end point was morbidity. The patients were observed for 3 years following TLTG. We assessed short-term surgical and long-term outcomes, including 3-year overall survival rates (3yOS) and 3-year recurrence-free survival rates (3yRFS).


Early and late morbidities (Clavien–Dindo grade ≥3) were 26.1 and 6.5 %, respectively. Operative time, estimated blood loss, number of dissected lymph nodes, and postoperative hospital stay were 444 (278–694) min, 100 (0–2267) g, 48 (16–89), and 23 (9–136) days, respectively, and 3yOS and 3yRFS rates were 70.7 and 60.9 %, respectively. Factors associated with postoperative complications and 3yOS were operative time [OR 1.011 (1.006–1.017), p < 0.01] and cancer recurrence within 3 years [HR 312.191 (1.126–86573.245], p = 0.045], respectively. 3yRFS was associated with tumor size (≥50 mm) [HR 10.325 (1.328–80.289), p = 0.026], pathological N factor ≥2 [HR 3.188 (1.196–8.495), p = 0.02], and postoperative pancreatic fistula combined with intra-abdominal abscesses Clavien–Dindo grade ≥2; [HR 3.670 (1.440–9.351), p = 0.006].


TLTG for AGC is sufficiently feasible and safe from both surgical and oncological point of view.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others



Totally laparoscopic total gastrectomy


Advanced gastric cancer


Early gastric cancer


Laparoscopic gastrectomy


Lymph node


Splenic hilar lymph node


Three-year overall survival rates


Three-year recurrence-free survival rates


D2 lymphadenectomy with preservation of station 10 lymph nodes and spleen


Spleen-preserving D2 lymphadenectomy

D2 + S:

D2 lymphadenectomy combined with splenectomy

D2 + PS:

D2 lymphadenectomy combined with distal pancreaticosplenectomy


Neoadjuvant chemotherapy


Body mass index


American Society of Anesthesiologists Physical Status


Japanese Classification of Gastric Carcinoma


Clavien–Dindo classification


Hazard ratio


  1. Crew KD, Neugut AI (2006) Epidemiology of gastric cancer. World J Gastroenterol 12:354–362

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sano T, Sasako M, Yamamoto S, Nishimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, Yamamura Y, Okajima K (2004) Gastric cancer surgery: morbidity and mortality results from a prospective randomized controlled trial comparing D2 and extended para-aortic lymphadenectomy-Japan clinical oncology group study 9501. J Clin Oncol 22:2767–2773

    Article  PubMed  Google Scholar 

  3. Japanese Gastric Cancer Association (2011) Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer 14:113–123

    Article  Google Scholar 

  4. Uyama I, Suda K, Satoh S (2013) Laparoscopic surgery for advanced gastric cancer: current status and future perspectives. J Gastric Cancer 13:19–25

    Article  PubMed  PubMed Central  Google Scholar 

  5. Persiani R, Antonacci V, Biondi A, Rausei S, La Greca A, Zoccali M, Ciccoritti L, D’Ugo D (2008) Determinants of surgical morbidity in gastric cancer treatment. J Am Coll Surg 207:13–19

    Article  PubMed  Google Scholar 

  6. Aoyagi K, Kouhuji K, Miyagi M, Imaizumi T, Kizaki J, Shirouzu K (2010) Prognosis of metastatic splenic hilum lymph node in patients with gastric cancer after total gastrectomy and splenectomy. World J Hepatol 2:81–86

    PubMed  PubMed Central  Google Scholar 

  7. Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P (1999) Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial, Surgical Co-operative Group. Br J Cancer 79:1522–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hartgrink HH, van de Velde CJ, Putter H, Bonenkamp JJ, Klein Kranenbang E, Songun I, Welvaart K, van Krieken JH, Meijer S, Plukker JT, van Lanschot JJ, Taat CW, de Graaf PW, von Meyenfeldt MF, Tilanus H, Sasako M (2004) Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J Clin Oncol 22:2069–2077

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Bamboat ZM, Strong VE (2013) Minimally invasive surgery for gastric cancer. J Surg Oncol 107:271–276

    Article  PubMed  Google Scholar 

  11. Wei HB, Wei B, Qi CL, Chen TF, Huang Y, Zheng ZH, Huang JL, Fang JF (2011) Laparoscopic versus open gastrectomy with D2 lymph node dissection for gastric cancer: a meta-analysis. Surg Laparosc Endosc Percutan Tech 21:383–390

    Article  PubMed  Google Scholar 

  12. Kawamura Y, Satoh S, Suda K, Ishida Y, Kanaya S, Uyama I (2014) Critical factors that influence the early outcome of laparoscopic total gastrectomy. Gastric Cancer. doi:10.1007/s10120-014-0392-9June7

    PubMed Central  Google Scholar 

  13. Shinohara T, Satoh S, Kanaya S, Ishida Y, Taniguchi K, Isogaki J, Inaba K, Yanaga K, Uyama I (2013) Laparoscopic versus open D2 gastrectomy for advanced gastric cancer: a retrospective cohort study. Surg Endosc 27:286–294

    Article  PubMed  Google Scholar 

  14. Kunisaki C, Makino H, Takagawa R, Kimura J, Ota M, Ichikawa Y, Kosaka T, Akiyama H, Endo I (2015) A systematic review of laparoscopic total gastrectomy for gastric cancer. Gastric Cancer 18:218–226

    Article  PubMed  Google Scholar 

  15. Uyama I, Sugioka A, Fujita J, Komori Y, Matsui H, Hasumi A (1999) Laparoscopic total gastrectomy with distal pancreatosplenectomy and D2 lymphadenectomy for advanced gastric cancer. Gastric Cancer 2:230–234

    Article  PubMed  Google Scholar 

  16. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Bassi C, Graf R, Vonlanthen R, Padburt R, Cameron JL, Makuuchi M (2009) The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg 250:187–196

    Article  PubMed  Google Scholar 

  17. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  18. Japan Clinical Oncology Group (2013) Postoperative complication criteria according to Clavien–Dindo Classification ver. 2.0. Available at:; Accessed 24 June 2015

  19. Suda K, Man-I M, Ishida Y, Kawamura Y, Satoh S, Uyama I (2015) Potential advantages of robotic radical gastrectomy for gastric adenocarcinoma in comparison with conventional laparoscopic approach: a single institutional retrospective comparative cohort study. Surg Endosc 29:673–685

    Article  PubMed  Google Scholar 

  20. Uyama I, Kanaya S, Ishida Y, Inaba K, Suda K, Satoh S (2012) Novel integrated robotic approach for suprapancreatic D2 nodal dissection for treating gastric cancer: technique and initial experience. World J Surg 36:331–337

    Article  PubMed  Google Scholar 

  21. Shinohara T, Kanaya S, Taniguchi K, Fujita T, Yanaga K, Uyama I (2009) Laparoscopic total gastrectomy with D2 lymph node dissection for gastric cancer. Arch Surg 144:1138–1142

    Article  PubMed  Google Scholar 

  22. Kanaya S, Haruta S, Kawamura Y, Yoshimura F, Inaba K, Hiramatsu Y, Ishida Y, Taniguchi K, Isogaki J, Uyama I (2011) Video: laparoscopy distinctive technique for suprapancreatic lymph node dissection: medial approach for laparoscopic gastric cancer surgery. Surg Endosc 25:3928–3929

    Article  PubMed  Google Scholar 

  23. Okabe H, Obama K, Tanaka E, Nomura A, Kawamura J, Nagayama S, Itami A, Watanabe G, Kanaya S, Sakai Y (2009) Intracorporeal esophagojejunal anastomosis after laparoscopic total gastrectomy for patients with gastric cancer. Surg Endosc 23:2167–2171

    Article  PubMed  Google Scholar 

  24. Inaba K, Satoh S, Ishida Y, Taniguchi Y, Isogaki J, Kanaya S, Uyama I (2010) Overlap method: novel intracorporeal esophagojejunostomy after laparoscopic total gastrectomy. J Am Coll Surg 211:e25–e29

    Article  PubMed  Google Scholar 

  25. Guan G, Jiang W, Chen Z, Liu X, Lu H, Zhang X (2013) Early results of a modified splenic hilar lymphadenectomy in laparoscopy-assisted total gastrectomy for gastric cancer with stage cT1-2: a case-control study. Surg Endosc 27:1923–1931

    Article  PubMed  Google Scholar 

  26. Ichikawa D, Komatsu S, Kubota T, Okamoto K, Konishi H, Shiozaki A, Fujiwara H, Otsuji E (2015) Evaluation of the safety and feasibility of laparoscopic total gastrectomy in clinical stage I gastric cancer patients. World J Surg 39:1782–1788

    Article  PubMed  Google Scholar 

  27. Nakata K, Nagai E, Ohuchida K, Shimizu S, Tanaka M (2015) Technical feasibility of laparoscopic total gastrectomy with splenectomy for gastric cancer: clinical short-term and long-term outcomes. Surg Endosc 29:1817–1822

    Article  PubMed  Google Scholar 

  28. Papenfuss WA, Kukar M, Oxenberg J, Attwood K, Nurkin S, Malhotra U, Wilkinson NW (2014) Morbidity and mortality associated with gastrectomy for gastric cancer. Ann Surg Oncol 21:3008–3014

    Article  PubMed  Google Scholar 

  29. da Costa WL Jr., Coimbra FJ, Ribeiro HS, Diniz AL, de Godoy AL, de Farias IC, Begnami MD, Soares FA (2015) Total gastrectomy for gastric cancer: an analysis of postoperative and long-term outcomes through time: results of 413 consecutive cases in a single cancer center. Ann Surg Oncol 22:750–757

  30. LaFemina J, Vinuela EF, Schattner MA, Gerdes H, Strong VE (2013) Esophagojejunal reconstruction after total gastrectomy for gastric cancer using a transorally inserted anvil delivery system. Ann Surg Oncol 20:2975–2983

    Article  CAS  PubMed  Google Scholar 

  31. Watanabe M, Miyata H, Gotoh M, Baba H, Kimura W, Tomita N, Nakagoe T, Shimada M, Kitagawa Y, Sugihara K, Mori M (2014) Total gastrectomy risk model: data from 20,011 Japanese patients in a nationwide internet-based database. Ann Surg 260:1034–1039

    Article  PubMed  Google Scholar 

  32. Filip JE, Mattar SG, Bowers SP, Smith CD (2002) Internal hernia formation after laparoscopic Roux-en-Y gastric bypass for morbid obesity. Am Surg 68:640–643

    PubMed  Google Scholar 

  33. Miyagaki H, Takiguchi S, Kurokawa Y, Hirao M, Tamura S, Nishida T, Kimura Y, Fujiwara Y, Mori M, Doki Y (2012) Recent trend of internal hernia occurrence after gastrectomy for gastric cancer. World J Surg 36:851–857

    Article  PubMed  Google Scholar 

  34. Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N, Japanese Laparoscopic Surgery Study Group (2007) A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 245:68–72

    Article  PubMed  PubMed Central  Google Scholar 

  35. Nagasako Y, Satoh S, Isogaki J, Inaba K, Taniguchi K, Uyama I (2012) Impact of anastomotic complications on outcome after laparoscopic gastrectomy for early gastric cancer. Br J Surg 99:849–854

    Article  CAS  PubMed  Google Scholar 

  36. Nashimoto A, Akazawa K, Isobe Y, Miyashiro I, Katai H, Kodera Y, Tsujitani S, Seto Y, Furukawa H, Oda I, Ono H, Tanabe S, Kaminishi M (2013) Gastric cancer treated in 2002 in Japan: 2009 annual report of the JGCA nationwide registry. Gastric Cancer 16:1–27

    Article  PubMed  Google Scholar 

  37. Sakuramoto S, Sasako M, Yamaguchi T, Kinoshita T, Fujii M, Nashimoto A, Furukawa H, Nakajima T, Ohashi Y, Imamura H, Higashino M, Yamamura Y, Kurita A, Arai K, Acts-Gc Group (2007) Adjuvant chemotherapy for gastric cancer with S-1, an oral fluoropyrimidine. N Engl J Med 357:1810–1820

    Article  CAS  PubMed  Google Scholar 

  38. Japanese Gastric Cancer Association (2014) Japanese gastric cancer treatment guidelines, 4th edn. Kanehara-Shuppan, Tokyo

    Google Scholar 

  39. Sano T, Sasako M, Mizusawa J, Katayama H, Katai H, Yoshikawa T, Yabusaki H, Ito S, Kaji M, Imamura H, Fukushima N, Fujitani K, Iwasaki Y, Kinoshita T (2015) Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma (JCOG0110): final survival analysis. J Clin Oncol 33:103

    Google Scholar 

Download references


The authors are indebted to Maruzen CO., LTD. (Tokyo, Japan) for their native English speaker’s review of this manuscript.

Funding information

This work was not supported by any grants or funding.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Koichi Suda.

Ethics declarations


Masaya Nakauchi, Koichi Suda, Shinichi Kadoya, Kazuki Inaba, Yoshinori Ishida, and Ichiro Uyama have no conflicts of interest or financial ties to disclose.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakauchi, M., Suda, K., Kadoya, S. et al. Technical aspects and short- and long-term outcomes of totally laparoscopic total gastrectomy for advanced gastric cancer: a single-institution retrospective study. Surg Endosc 30, 4632–4639 (2016).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: