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Evidence - Gastrectomy, subtotal, robotically assisted

  1. Surgical Therapy of Gastric Carcinoma

    Gastric carcinoma, with a worldwide incidence of over 1 million new cases, is among the most common solid malignancies [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 depending on gender between 30% (men) and 33% (women) [2]. While in Asia, due to screening programs, 5-year survival rates of over 70% are achieved, gastric carcinoma in this region 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 made for 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. Here, 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.

    Gastric early carcinomas with a maximum of one "extended criterion" can also be resected endoscopically in a curative manner [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 extended criterion is present, an 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.

    In the case of gastric early carcinoma, the indication for surgery exists whenever the carcinoma confined to the mucosa (T1a) cannot be resected curatively endoscopically or when greater depth of invasion (T1b) increases the risk of lymph node metastases and adequate lymphadenectomy is indispensable for safely 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, reduced postoperative atony, faster mobilization, and a shorter hospital stay [5, 9-11, 16-18]. Overall morbidity after laparoscopic surgery is significantly lower in RTCs: laparoscopic vs. open 2.0-2.8% vs. 2.0-57.1% [13,18]. The 30-day mortality of the laparoscopic and open technique is equal 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].

    There is sufficient data available to make reliable statements about the oncological outcome after laparoscopic resection of gastric early carcinomas. In the Korean COACT0301 trial, a 5-year DFS (disease-free survival) of 98.8% was found in the laparoscopic group and 97.6% in the conventionally open group. The 5-year overall survival was nearly 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 (cardia 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 frozen section examination should be performed. 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 level-1 studies (RCT) for oncological equivalence are still pending.

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

    Significance 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 (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 MIG consists of smaller studies that examine the postoperative outcome as the primary endpoint. Notable here are the LOGICA study (NCT02248519) and the STOMACH study (NCT02130726), which compare postoperative morbidity, length of stay, and surgical quality of laparoscopic gastrectomy with 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. In a subgroup analysis, there was less blood loss with D2 lymphadenectomy in the robotics group [47, 48].

    A Japanese prospective multicenter single-arm study for gastric carcinomas in UICC stage I/II showed lower morbidity after robotically assisted gastrectomy compared to a historical laparoscopic group [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 consistently show equivalent lymph node numbers even for selected, technically challenging lymph node locations [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 J Clin. 2. Robert Koch Institute GDEKID (2017) Cancer in Germany 2013–2014, 11th ed., pp. 32–35 (Chapter 3.4: Stomach)

    2. Robert Koch Institute and Society of Epidemiological Cancer Registries in Germany e. V. (GEKID). (2023). Cancer in Germany for 2019/2020 – 13th Edition. Berlin: RKI. Chapter: Stomach (C16). Available at: https://www.krebsdaten.de/Krebs/DE/Content/Publikationen/Krebs_in_Deutschland/kid_2023/kid_2023_c16_magen.pdf

    3. Moehler M et al (2019) S3-Guideline Gastric Carcinoma–Diagnosis and Treatment of Adenocarcinomas of the Stomach and Esophagogastric Junction –Long Version 2.0 –August 2019. AWMF Registry Number: 032/009OL. Z Gastroenterol 57(12):1517–1632.

    4. Ludwig K et al (2018) Surgical Strategy for Early Gastric Carcinomas. 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 meta-analysis 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 does 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 advanced gastric 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). Ann Surg 267:638–645.

    30. Hiki N et al (2018) Long-term outcomes of laparoscopy-assisted distal gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer: a multicenter phase II trial (JCOG0703). Gastric Cancer 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 J Surg 39:2734–2741.

    32. Huscher CGS et al (2005) Laparoscopic versus open subtotal gastrectomy for distal gastric cancer: five-year results of a randomized prospective trial. Ann Surg 241:232–237.

    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. Surg Endosc 33:33–45.

    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) Laparoscopic vs. conventional open D2-gastrectomy in gastric cancer: a matched-pair analysis. Zentralbl Chir 143(2):145–154.

    36. Ramagem CAG et al (2015) Comparison of laparoscopic total gastrectomy and laparotomic total gastrectomy for gastric cancer. Arq Bras Cir Dig 28:65–69.

    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 Surg 37:2379–2386.

    39. Lu Y et al (2016) Laparoscopic versus open total gastrectomy for advanced proximal gastric carcinoma: a matched-pair analysis. JBUON 21:903–908.

    40. Shu B et al (2016) Laparoscopic total gastrectomy compared with open resection for gastric carcinoma: a case-matched study with long-term follow-up. JBUON 21:101–107.

    41. Wu H et al (2016) Outcome of laparoscopic total gastrectomy for gastric carcinoma. JBUON 21:603–608.

    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. JAMA 321:1983–1992.

    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

  4. Reviews

    Merga ZC, Lee JS, Gong CS. Outcomes of Gastrectomy for Gastric Cancer in Patients Aged >80 Years: A Systematic Literature Review and Meta-Analysis. J Gastric Cancer. 2023 Jul;23(3):428-450.

    Heng W, Lye JYT, Lee ZJ, Chan WH, Tan JTH. Laparoscopic completion gastrectomy: A single-institution case series and systematic review of the literature. Asian J Endosc Surg. 2023 Jul 31.

    Salavatizadeh M, Soltanieh S, Radkhah N, Ataei Kachouei AH, Bahrami A, Khalesi S, Hejazi E. The association between skeletal muscle mass index (SMI) and survival after gastrectomy: A systematic review and meta-analysis of cohort studies. Eur J Surg Oncol. 2023 Jul 6:106980.

    Aiolfi A, Sozzi A, Bonitta G, Lombardo F, Cavalli M, Campanelli G, Bonavina L, Bona D. Short-term outcomes of different esophagojejunal anastomotic techniques during laparoscopic total gastrectomy: a network meta-analysis. Surg Endosc. 2023 Aug;37(8):5777-5790.

    Fu YY, Yao Q, Shao WZ, Sun GW, Wang DR. Single-port versus conventional laparoscopic distal gastrectomy for gastric cancer: A systematic review and meta-analysis. Asian J Surg. 2022 Aug 30. pii: S1015-9584(22)01083-1

    Schröder W, Fuchs H, Straatman J, Babic B. Reconstruction and functional results after gastric resection. Chirurgie (Heidelb). 2022 Aug 29

    Ali M, Wang Y, Ding J, Wang D. Postoperative outcomes in robotic gastric resection compared with laparoscopic gastric resection in gastric cancer: A meta-analysis and systemic review. Health Sci Rep. 2022 Aug 16;5(5):e746.

    de Jong MHS, Gisbertz SS, van Berge Henegouwen MI, Draaisma WA. Prevalence of nodal metastases in the individual lymph node stations for different T-stages in gastric cancer: a systematic review. Updates Surg. 2022 Aug 13.

    Jiang Y, Yang F, Ma J, Zhang N, Zhang C, Li G, Li Z. Surgical and oncological outcomes of distal gastrectomy compared to total gastrectomy for middle-third gastric cancer: A systematic review and meta-analysis. Oncol Lett. 2022 Jul4;24(3):291.

    Bestetti AM, de Moura DTH, Proença IM, Junior ESDM, Ribeiro IB, Sasso JGRJ, Kum AST, Sánchez-Luna SA, Marques Bernardo W, de Moura EGH. Endoscopic Resection Versus Surgery in the Treatment of Early Gastric Cancer: A Systematic Review and Meta-Analysis. Front Oncol. 2022 Jul 12;12:939244.

    Yang Y, Chen Y, Hu Y, Feng Y, Mao Q, Xue W. Outcomes of laparoscopic versus open total gastrectomy with D2 lymphadenectomy for gastric cancer: a systematic review and meta-analysis. Eur J Med Res. 2022 Jul 18;27(1):124.

    Baral S, Arawker MH, Sun Q, Jiang M, Wang L, Wang Y, Ali M, Wang D. Robotic Versus Laparoscopic Gastrectomy for Gastric Cancer: A Mega Meta-Analysis. Front Surg. 2022 Jun 28;9:895976.

    Lee S, Kim HH. Minimally invasive surgery in advanced gastric cancer. Ann Gastroenterol Surg. 2022 Feb 25;6(3):336-343.

    Lou S, Yin X, Wang Y, Zhang Y, Xue Y. Laparoscopic versus open gastrectomy for gastric cancer: A systematic review and meta-analysis of randomized controlled trials. Int J Surg. 2022 Jun;102:106678.

  5. Guidelines

  6. literature search

    Literature search on the pages of pubmed.