Evidence - Total gastrectomy, robotically assisted with D2 lymphadenectomy

  1. Surgical therapy of gastric carcinoma

    Gastric Carcinoma

    Gastric carcinoma is among the most common solid malignancies worldwide, with an incidence of over 1 million new cases [1]. In Germany, the incidence is approximately 15,000 new cases per year (about 9,000 men and 6,000 women), with the current 5-year survival rate being gender-dependent at 30% for men and 33% for women [2]. While in Asia, due to screening programs, 5-year survival rates of over 70% are achieved, gastric carcinoma in this country often presents at an advanced stage at initial diagnosis, which can no longer be removed locally by endoscopic resection.

    The only option for curative therapy in locally advanced gastric carcinomas and adenocarcinomas of the esophagogastric junction (AEG) currently is oncological-surgical resection with the goal of complete removal of the primary tumor (tumor-free resection margins, R0) and the regional lymphatic drainage pathways (systematic D2 lymphadenectomy) [3].

    Endoscopic Submucosal Dissection (ESD)

    An exception is early carcinomas (pT1a and N0), which can be resected en bloc endoscopically if they meet all of the following four criteria [3]:

    • < 2 cm in diameter
    • not ulcerated
    • mucosal carcinoma
    • intestinal type or histological differentiation grade good or moderate (G1/G2)

    Since some criteria (grading, submucosal invasion) are only available after precise histopathological diagnosis, endoscopic resection can initially be performed for diagnostic purposes. However, it should be ensured that this is done with the aim of an en-bloc R0 resection. Endoscopic submucosal dissection (ESD) is the method of choice, as it is the only one that allows a safe en-bloc R0 resection regardless of size.

    Early gastric carcinomas with at most one "expanded criterion" can also be resected curatively endoscopically [3]:

    • differentiated mucosal carcinoma (G1/G2) without ulceration and size > 2 cm
    • differentiated mucosal carcinoma with ulceration and size ≤ 3 cm
    • well-differentiated carcinomas with submucosal invasion < 500 µm and size < 3 cm
    • undifferentiated mucosal carcinoma < 2 cm in diameter (provided no biopsy evidence of tumor cells within ≤ 1 cm distance)

    If more than one expanded criterion is present, oncological-surgical resection should be performed [3].

    Oncological-Surgical Resection

    In addition to total and transhiatal extended gastrectomy, depending on the indication and tumor size, partial gastric resection in the form of proximal or distal gastric resection is possible.

    For early gastric carcinoma, the indication for surgery exists whenever the carcinoma confined to the mucosa (T1a) cannot be curatively resected endoscopically or when greater depth of invasion (T1b) increases the risk of lymph node metastases and adequate lymphadenectomy is essential for achieving a cure [3, 4].

    For early carcinomas, there is high evidence that laparoscopic procedures are technically safe and oncologically comparable to open surgery, regardless of tumor location and type of resection [5-18]. Compared to conventionally open-operated patients, patients recover faster after laparoscopic resection, show significantly earlier oral tolerance of food intake, shortened postoperative atony, faster mobilization, and a shorter hospital stay [5, 9-11, 16-18]. Overall morbidity after laparoscopic surgery is significantly lower in RCTs: laparoscopic vs. open 2.0–2.8% vs. 2.0–57.1% [13, 18]. The 30-day mortality of laparoscopic and open techniques is the same at 0.1–3.0% [4, 5, 19]. An LAD with more than 25 removed lymph nodes and a D2 LAD can be performed laparoscopically without increasing morbidity [17].

    Sufficient data are available to make reliable statements about the oncological outcome after laparoscopic resection of early gastric carcinomas. The Korean COACT0301 trial found a 5-year DFS (disease-free survival) of 98.8% in the laparoscopic group and 97.6% in the conventionally open group. The 5-year overall survival was almost identical at 97.6% in the laparoscopic group and 96.3% in the open group [20]. Other comparative studies came to similar results [11, 21].

    For locally advanced gastric carcinomas that are proximally located, gastrectomy is usually required. For adenocarcinomas of the esophagogastric junction (cardiac carcinoma, AEG type II and III), distal esophageal resection is additionally indicated. Depending on the luminal tumor spread, subtotal esophagectomy with proximal gastric resection or esophagogastrectomy may be necessary to achieve an R0 resection. For distal tumors, the proximal stomach can be preserved without worsening the prognosis. An adequate resection margin of 5 cm (intestinal type according to Lauren) or 8 cm (diffuse type according to Lauren) should be aimed for. If the safety margin is undershot orally, a rapid section examination should take place. Structures adherent to the tumor (e.g., diaphragm, spleen) should be removed en bloc with the tumor if possible. Routine splenectomy should be avoided [22–27].

    Numerous studies are now available for laparoscopic procedures for curative surgery of gastric carcinoma, which have a high level of evidence for distal, locally advanced carcinomas and distal or subtotal gastric resections, combining technical feasibility and oncological outcome with the advantages of better early postoperative recovery [19, 28–42]. For proximally located advanced carcinomas, the safety of laparoscopic techniques is proven, but evidence-grade 1 studies (RCT) for oncological equivalence are still pending.

    The current German S3 guideline (update 2019) does not generally recommend laparoscopic procedures for curative surgery of gastric carcinoma [3]. The goal of cure should be pursued in all functionally operable patients with T1 to T4 tumors [43]. Patients with T4b tumors involving unresectable structures and those with distant metastases should not undergo radical surgery.

    Role of Minimally Invasive Techniques

    Regarding the indication for minimally invasive procedures in advanced gastric carcinoma, the latest results of large prospective randomized studies indicate an equivalent oncological outcome of laparoscopic gastrectomy compared to open gastric resection. A corresponding Chinese study has already shown comparable disease-specific 3-year results [44]. The Korean KLASS-02 study (Korean Laparoendoscopic Gastrointestinal Study Group) showed lower postoperative morbidity after laparoscopic gastrectomy with D2 lymphadenectomy, while an equivalent Japanese study demonstrated equivalence [45, 46]. Western evidence on minimally invasive gastrectomies (MIG) is based on smaller studies that investigate the postoperative outcome as the primary endpoint. Notable are the LOGICA study (NCT02248519) and the STOMACH study (NCT02130726), which compare postoperative morbidity, length of stay, and surgical quality of laparoscopic gastrectomy to open gastrectomy.

    Robotics in Gastric Surgery

    With the same indication, a Korean prospective multicenter, non-randomized study showed equivalent postoperative outcomes in robotic gastrectomy compared to laparoscopic gastrectomy. A subgroup analysis showed less blood loss in the D2 lymphadenectomy in the robotic group [47, 48].

    A Japanese prospective multicenter single-arm study for gastric carcinomas in UICC stage I/II showed lower morbidity after robot-assisted gastrectomy compared to a historical laparoscopic cohort [49].

    The number of resected lymph nodes was not different in this and other studies, so equivalent long-term results are expected.

    In larger retrospective series, it has been shown that long-term results after robotic resection are not inferior to those after laparoscopic resection. Already published results on gastric resection could always show equivalent lymph node numbers even for selected, technically demanding lymph node stations [50, 51].

  2. Currently ongoing studies on this topic

  3. Literature on this topic


    1. Bray F et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer JClin. 2. Robert Koch-Institut GDEKID (2017) Krebs in Deutschland 2013–2014, 11. Aufl., S 32–35 (Kapitel3.4:Magen)

    3. Moehler M et al (2019) S3-Leitlinie Magenkarzinom–Diagnostik und Therapie der Adenokarzinome des Magens und des ösophagogastralen Übergangs –Langversion 2.0 –August 2019. AWMF-Registernummer: 032/009OL. Z Gastroenterol 57(12):1517–1632.

    4. Ludwig K et al (2018) Chirurgische Strategie bei Frühkarzinomen des Magens. Chirurg.89:347–357.

    5. Lee JH et al  (2005) A prospective randomized study comparing open vs laparoscopy-assisted distal gastrectomy in early gastric cancer: early results. Surg Endosc.19(2):168-73.

    6. Best LM et al (2016) Laparoscopic versus open gastrectomy for gastric cancer. Cochrane Database Syst Rev, 3: p. CD011389

    7. Kitano S et al (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): p. S306-11.

    8. Hayashi H et al (2005) Prospective randomized study of open versus laparoscopy-assisted distal gastrectomy with extraperigastric lymph node dissection for early gastric cancer. Surg Endosc. 19(9): p. 1172-6.

    9. Kim YW 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(5): p. 721-7.

    10. Sakuramoto S 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): p. 1695-705.

    11. Takiguchi S et al (2013) Laparoscopy-assisted distal gastrectomy versus open distal gastrectomy. A prospective randomized single-blind study. World J Surg. 37(10): p. 2379-86.

    12. Hosono S. et al (2006) Meta-analysis of short-term outcomes after laparoscopy-assisted distal gastrectomy. World J Gastroenterol. 12(47): p. 7676-83.

    13. Memon MA et al (2008) Meta-analysis of laparoscopic and open distal gastrectomy for gastric carcinoma. Surg Endosc. 22(8): p. 1781-9.

    14. Chen XZ et al (2009) Short-term evaluation of laparoscopy-assisted distal gastrectomy for predictive early gastric cancer: a meta-analysis of randomized controlled trials. Surg Laparosc Endosc Percutan Tech. 19(4): p. 277-84.

    15. Yakoub D et al (2009) Laparoscopic assisted distal gastrectomy for early gastric cancer: is it an alternative to the open approach? Surg Oncol. 18(4): p. 322-33.

    16. Vinuela EF et al (2012) Laparoscopic versus open distal gastrectomy for gastric cancer: a metaanalysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg. 255(3): p. 446-56

    17. Zeng YK et al (2012) Laparoscopy-assisted versus open distal gastrectomy for early gastric cancer: evidence from randomized and nonrandomized clinical trials. Ann Surg. 256(1): p. 39-52.

    18. Deng Y et al (2015) Laparoscopy-assisted versus open distal gastrectomy for early gastric cancer: A meta-analysis based on seven randomized controlled trials. Surg Oncol. 24(2): p. 71-7.

    19. Hu Y et al (2016) Morbidity and Mortality of Laparoscopic Versus Open D2 Distal Gastrectomy for Advanced Gastric Cancer: A Randomized Controlled Trial. J Clin Oncol. 34(12): p. 1350- 7

    20. Kim YW et al (2013) Long-term outcomes of laparoscopy-assisted distal gastrectomy for early gastric cancer: result of a randomized controlled trial (COACT 0301). Surg Endosc. 27(11): p. 4267-76.

    21. Lee JH et al (2009) Comparison of long-term outcomes of laparoscopy-assisted and open distal gastrectomy for early gastric cancer. Surg Endosc. 23(8): p. 1759-63.

    22. Squires MH et al (2015) Is it time to abandon the 5-cm margin rule during resection of distal gastric adenocarcinoma? A multi-institution study of the U.S. Gastric Cancer Collaborative. Ann Surg Oncol. 22(4): p. 1243-51.

    23. Squires MH et al (2014) Utility of the proximal margin frozen section for resection of gastric adenocarcinoma: a 7-Institution Study of the US Gastric Cancer Collaborative. Ann Surg Oncol. 21(13): p. 4202-10.

    24. Kim MG et al (2014) The distance of proximal resection margin dose not significantly influence on the prognosis of gastric cancer patients after curative resection. Ann Surg Treat Res. 87(5): p. 223-31.

    25. Bozzetti F et al (1997) Total versus subtotal gastrectomy: surgical morbidity and mortality rates in a multicenter Italian randomized trial. The Italian Gastrointestinal Tumor Study Group. Ann Surg. 226(5): p. 613-20.

    26. Mine S et al (2013) Proximal margin length with transhiatal gastrectomy for Siewert type II and III adenocarcinomas of the oesophagogastric junction. Br J Surg. 100(8): p. 1050-4.

    27. Ajani JA et al (2016) Gastric Cancer, Version 3.2016, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 14(10): p. 1286-1312.

    28. Hyung WJ et al (2020) Long-term outcomes of laparoscopic distal gastrectomy for locally advancedgastric cancer: the KLASS-02-RCT randomized clinical trial. J Clin Oncol.

    29. Park YK  et al (2018) Laparoscopy assisted versus open D2 distal gastrectomy for advanced gastric cancer: results from a randomized phase II multicenter clinical trial (COACT 1001). AnnSurg267:638–645.

    30. Hiki N et al (2018) Long-term outcomes of laparoscopy-assisted distal gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer: amulticenterphase II trial (JCOG0703).GastricCancer 21:155–161.

    31. Inaki N et al (2015) A multiinstitutional, prospective, phase II feasibility study of laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for locally advanced gastric cancer (JLSSG0901).World JSurg39:2734–2741.

    32. Huscher CGS et al (2005) Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. AnnSurg241:232–237.

    33. Wang Z  et al (2019) Short-term surgical outcomes of laparoscopy-assisted versus open D2 distal gastrectomy for locally advanced gastric cancer in North China: a multicenter randomized controlled trial. SurgEndosc33:33–45.

    34. Ziyu L et al (2019) Assessment of laparoscopic distal gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer. A randomized clinical trial. JAMA Surg 154:1093–1101.

    35. Ludwig K et al (2018) Laparoskopische vs. konventionell-offene D2-Gastrektomie bei Magenkarzinom: eine Matched-Pair-Analyse. Zentralbl Chir143(2):145–154.

    36. Ramagem CAG et al (2015) Comparison of laparoscopic total gastrectomy and laparotomic total gastrectomy for gastric cancer. ArqBrasCirDig28:65–69.

    37. Siani LM et al (2012) Completely laparoscopic versus open total gastrectomy in stage I–III/C gastric cancer: safety, efficacy and five-year oncologic outcome. Minerva Chir 67:319–326.

    38. Takiguchi S et al (2013) Laparoscopy-assisted distal gastrectomy versus open distal gastrectomy. A prospective randomized single-blind study. World J Surg37:2379–2386.

    39. Lu Y et al (2016) Laparoscopic versus open total gastrectomy for advanced proximal gastric carcinoma: a matchedpair analysis. JBUON21:903–908.

    40. Shu B et al (2016) Laparoscopic total gastrectomy compared with open resection for gastric carcinoma: a case-matched study with long-termfollow-up. JBUON21:101–107.

    41. Wu H et al (2016) Outcome of laparoscopic total gastrectomy for gastric carcinoma. JBUON21:603–608.

    42. Yu J et al (2019) Effect of laparoscopic vs open distal gastrectomy on 3-year disease-free survival in patients with locally advanced gastric cancer: the CLASS-01 randomized clinical trial. JAMA321:1983–1992.

    43. Edge SB et al (2010) The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 17(6): p. 1471-4.

    44. Li G, Yu J, Huang C, Sun Y et al (2018) Effect of Laparoscopic vs Open Distal Gastrectomy on 3-Year Disease-Free Survival in Patients With Locally Advanced

    Gastric Cancer: The CLASS-01 Randomized Clinical Trial. JAMA 321:1983–1992

    45. Lee H-J, Hyung WJ, Yang H-K et al (2019) Short-term outcomes of a multicenter randomized controlled trial comparing laparoscopic distal gastrectomy with D2 lymphadenectomy to open distal gastrectomy for locally advanced gastric cancer (KLASS-02-RCT).Ann Surg 270(6):983–991

    46. Lee S-W, Etoh T, Ohyama T et al (2018) Short-term outcomes from a multi-institutional, phase III study of laparoscopic versus open distal gastrectomy with D2 lymph node dissection for locally advanced gastric cancer (JLSSG0901). J Clin Oncol 39(11):2734-41

    47. Kim H-I, Han S-U, Yang H-K et al (2016) Multicenter prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg 263(1):103–109

    48. Park JM, Kim HI, Han SU et al (2016) Who may benefit from robotic gastrectomy?: a subgroup analysis of multicenter prospective comparative study data on robotic versus laparoscopic gastrectomy. Eur J Surg Oncol 42(12):1944–1949

    49. Uyama I, Suda K, Nakauchi M et al (2019) Clinical advantages of robotic gastrectomy for clinical stage I/II gastric cancer: a multi-institutional prospective single-arm study. Gastric Cancer 22(2):377–385

    50. Kim YW, Reim D, Park JY et al (2016) Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer. Surg Endosc 30(4): 1547–1552

    51. Han D-S, Suh Y-S, Ahn HS et al (2015) Comparison of surgical outcomes of robot-assisted and laparoscopy-assisted pylorus-preserving gastrectomy for gastric cancer: a propensity score matching analysis. Ann Surg Oncol 22(7):2323–2328

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Merga ZC, Lee JS, Gong CS. Outcomes of Gastrectomy for Gastric Cancer in Patients Aged &gt;80 Years

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