Skip to main content

Advertisement

SpringerLink
Log in

Three-year outcomes of robotic gastrectomy versus laparoscopic gastrectomy for the treatment of clinical stage I/II gastric cancer: a multi-institutional retrospective comparative study

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Oncological benefits of robotic gastrectomy (RG) remain unclear. We aimed to determine and compare the 3-year outcomes of RG and laparoscopic gastrectomy (LG) for the treatment of gastric cancer.

Methods

This was a multi-institutional retrospective study of patients who prospectively underwent RG in a previous study (UMIN000015388) and historical controls who underwent LG. Operable patients with cStage I/II primary gastric cancer were enrolled. The inverse probability of treatment weighting method based on propensity scores was used to balance patient demographic factors and surgeon volume between the RG and LG groups. The primary outcome measure was the 3-year overall survival rate (3yOS).

Results

Of the 1,127 patients in the previous study, 326 and 752 patients in the RG and LG groups, respectively, completed the study. The standardized difference of all confounding factors was reduced to 0.09 or less after weighting. In the weighted population, 3yOS was 96.3% and 89.6% in the RG and LG groups, respectively (hazard ratio [HR] 0.34 [0.15, 0.76]; p = 0.009), whereas there was no difference in 3-year recurrence-free survival rate (3yRFS) between the two groups (HR 0.58 [0.32, 1.05]; p = 0.073). Sub-analyses showed that RG improved 3yOS (HR 0.05 [0.01, 0.38]; p = 0.004) and 3yRFS (HR 0.05 [0.01, 0.34]; p = 0.003) in patients with pStage IA disease. Recurrence rates and patterns were similar between the RG and LG groups. RG did not improve the morbidity rate, however, it attenuated some of the adverse events, including anastomotic leakage and intra-abdominal abscess. RG improved estimated blood loss and duration of postoperative hospitalization.

Conclusion

This study showed surgical and oncological safety of RG for cStage I/II gastric cancer considering the 3-year outcomes, compared with those of LG.

Graphical abstract

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

RG:

Robotic gastrectomy

LG:

Laparoscopic gastrectomy

3yOS:

3-Year overall survival rate

3yRFS:

3-Year recurrence-free survival rate

HR:

Hazard ratio

ASA-PS:

American Society of Anesthesiologists physical status

OR:

Odds ratio

CI:

Confidence interval

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    Article  PubMed  Google Scholar 

  2. 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 

  3. Katai H, Mizusawa J, Katayama H, Morita S, Yamada T, Bando E, Ito S, Takagi M, Takagane A, Teshima S, Koeda K, Nunobe S, Yoshikawa T, Terashima M, Sasako M (2020) Survival outcomes after laparoscopy-assisted distal gastrectomy versus open distal gastrectomy with nodal dissection for clinical stage IA or IB gastric cancer (JCOG0912): a multicentre, non-inferiority, phase 3 randomised controlled trial. Lancet Gastroenterol Hepatol 5:142–151

    Article  PubMed  Google Scholar 

  4. Kim HH, Han SU, Kim MC, Kim W, Lee HJ, Ryu SW, Cho GS, Kim CY, Yang HK, Park DJ, Song KY, Lee SI, Ryu SY, Lee JH, Hyung WJ, Korean Laparoendoscopic Gastrointestinal Surgery Study (KLASS) Group (2019) Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with stage I gastric cancer: the KLASS-01 randomized clinical trial. JAMA Oncol 5:506–513

    Article  PubMed  PubMed Central  Google Scholar 

  5. Yu J, Huang C, Sun Y, Su X, Cao H, Hu J, Wang K, Suo J, Tao K, He X, Wei H, Ying M, Hu W, Du X, Hu Y, Liu H, Zheng C, Li P, Xie J, Liu F, Li Z, Zhao G, Yang K, Liu C, Li H, Chen P, Ji J, Li G, Chinese Laparoscopic Gastrointestinal Surgery Study (CLASS) Group (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

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hyung WJ, Yang HK, Park YK, Lee HJ, An JY, Kim W, Kim HI, Kim HH, Ryu SW, Hur H, Kim MC, Kong SH, Cho GS, Kim JJ, Park DJ, Ryu KW, Kim YW, Kim JW, Lee JH, Han SU, Korean Laparoendoscopic Gastrointestinal Surgery Study Group (2020) Long-term outcomes of laparoscopic distal gastrectomy for locally advanced gastric cancer: the KLASS-02-RCT randomized clinical trial. J Clin Oncol 38:3304–3313

    Article  PubMed  Google Scholar 

  7. Uyama I, Suda K, Nakauchi M, Kinoshita T, Noshiro H, Takiguchi S, Ehara K, Obama K, Kuwabara S, Okabe H, Terashima M (2019) Clinical advantages of robotic gastrectomy for clinical stage I/II gastric cancer: a multi-institutional prospective single-arm study. Gastric Cancer 22:377–385

    Article  PubMed  Google Scholar 

  8. Kim HI, Han SU, Yang HK, Kim YW, Lee HJ, Ryu KW, Park JM, An JY, Kim MC, Park S, Song KY, Oh SJ, Kong SH, Suh BJ, Yang DH, Ha TK, Kim YN, Hyung WJ (2016) Multicenter prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg 263:103–109

    Article  PubMed  Google Scholar 

  9. Ojima T, Nakamura M, Hayata K, Kitadani J, Katsuda M, Takeuchi A, Tominaga S, Nakai T, Nakamori M, Ohi M, Kusunoki M, Yamaue H (2021) Short-term outcomes of robotic gastrectomy vs laparoscopic gastrectomy for patients with gastric cancer: a randomized clinical trial. JAMA Surg 156:954–963

    Article  PubMed  Google Scholar 

  10. Lu J, Zheng CH, Xu BB, Xie JW, Wang JB, Lin JX, Chen QY, Cao LL, Lin M, Tu RH, Huang ZN, Lin JL, Zheng HL, Huang CM, Li P (2021) Assessment of robotic versus laparoscopic distal gastrectomy for gastric cancer: a. randomized controlled trial. Ann Surg 273:858–867

    Article  PubMed  Google Scholar 

  11. Hikage M, Fujiya K, Kamiya S, Tanizawa Y, Bando E, Notsu A, Mori K, Terashima M (2021) Robotic gastrectomy compared with laparoscopic gastrectomy for clinical stage I/II gastric cancer patients: a propensity score-matched analysis. World J Surg 45:1483–1494

    Article  PubMed  Google Scholar 

  12. Kikuchi K, Suda K, Shibasaki S, Tanaka T, Uyama I (2021) Challenges in improving the minimal invasiveness of the surgical treatment for gastric cancer using robotic technology. Ann Gastroenterol Surg 5:604–613

    Article  PubMed  PubMed Central  Google Scholar 

  13. Greenberg D, Hammerman A, Vinker S, Shani A, Yermiahu Y, Neumann PJ (2013) Which is more valuable, longer survival or better quality of life? Israeli oncologists’ and family physicians’ attitudes toward the relative value of new cancer and congestive heart failure interventions. Value Health 16:842–847

    Article  PubMed  Google Scholar 

  14. Suda K, Nakauchi M, Inaba K, Ishida Y, Uyama I (2016) Robotic surgery for upper gastrointestinal cancer: current status and future perspectives. Dig Endosc 28:701–713

    Article  PubMed  Google Scholar 

  15. Suda K, Nakauchi M, Inaba K, Ishida Y, Uyama I (2016) Minimally invasive surgery for upper gastrointestinal cancer: our experience and review of the literature. World J Gastroenterol 22:4626–4637

    Article  PubMed  PubMed Central  Google Scholar 

  16. Japanese Gastric Cancer Association (2017) Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 20:1–19

    Article  Google Scholar 

  17. Ali MS, Prieto-Alhambra D, Lopes LC, Ramos D, Bispo N, Ichihara MY, Pescarini JM, Williamson E, Fiaccone RL, Barreto ML, Smeeth L (2019) Propensity score methods in health technology assessment: principles, extended applications, and recent advances. Front Pharmacol 10:973

    Article  PubMed  PubMed Central  Google Scholar 

  18. Suda K, Yamamoto H, Nishigori T, Obama K, Yoda Y, Hikage M, Shibasaki S, Tanaka T, Kakeji Y, Inomata M, Kitagawa Y, Miyata H, Terashima M, Noshiro H, Uyama I (2022) Safe implementation of robotic gastrectomy for gastric cancer under the requirements for universal health insurance coverage: a retrospective cohort study using a nationwide registry database in Japan. Gastric Cancer 25:438–449

    Article  PubMed  Google Scholar 

  19. Mukai Y, Kurokawa Y, Takiguchi S, Mori M, Doki Y (2017) Are treatment outcomes in gastric cancer associated with either hospital volume or surgeon volume? Ann Gastroenterol Surg 1:186–192

    Article  PubMed  PubMed Central  Google Scholar 

  20. Feng Q, Ma H, Qiu J, Du Y, Zhang G, Li P, Wen K, Xie M (2021) Comparison of long-term and perioperative outcomes of robotic versus conventional laparoscopic gastrectomy for gastric cancer: a systematic review and meta-analysis of PSM and RCT studies. Front Oncol 11:759509

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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 

  22. Li Z, Bai B, Xie F, Zhao Q (2018) Distal versus total gastrectomy for middle and lower-third gastric cancer: a systematic review and meta-analysis. Int J Surg 53:163–170

    Article  PubMed  Google Scholar 

  23. Nakauchi M, Suda K, Shibasaki S, Nakamura K, Kadoya S, Kikuchi K, Inaba K, Uyama I (2021) Prognostic factors of minimally invasive surgery for gastric cancer: does robotic gastrectomy bring oncological benefit? World J Gastroenterol 27:6659–6672

    Article  PubMed  PubMed Central  Google Scholar 

  24. Shibasaki S, Suda K, Nakauchi M, Nakamura K, Tanaka T, Kikuchi K, Inaba K, Uyama I (2021) Impact of the endoscopic surgical skill qualification system on the safety of laparoscopic gastrectomy for gastric cancer. Surg Endosc 35:6089–6100

    Article  PubMed  Google Scholar 

  25. Shibasaki S, Suda K, Kadoya S, Ishida Y, Nakauchi M, Nakamura K, Akimoto S, Tanaka T, Kikuchi K, Inaba K, Uyama I (2022) The safe performance of robotic gastrectomy by second-generation surgeons meeting the operating surgeon’s criteria in the Japan Society for Endoscopic Surgery guidelines. Asian J Endosc Surg 15:70–81

    Article  PubMed  Google Scholar 

  26. Shibasaki S, Suda K, Obama K, Yoshida M, Uyama I (2020) Should robotic gastrectomy become a standard surgical treatment option for gastric cancer? Surg Today 50:955–965

    Article  PubMed  Google Scholar 

  27. Japanese Gastric Cancer Association (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112

    Article  Google Scholar 

  28. Katai H, Sasako M, Fukuda H, Nakamura K, Hiki N, Saka M, Yamaue H, Yoshikawa T, Kojima K, JCOG Gastric Cancer Surgical Study Group (2010) Safety and feasibility of laparoscopy-assisted distal gastrectomy with suprapancreatic nodal dissection for clinical stage I gastric cancer: a multicenter phase II trial (JCOG 0703). Gastric Cancer 13:238–244

    Article  PubMed  Google Scholar 

  29. 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 

  30. Coratti A, Fernandes E, Lombardi A, Di Marino M, Annecchiarico M, Felicioni L, Giulianotti PC (2015) Robot-assisted surgery for gastric carcinoma: five years follow-up and beyond: a single western center experience and long-term oncological outcomes. Eur J Surg Oncol 41:1106–1113

    Article  CAS  PubMed  Google Scholar 

  31. Obama K, Kim YM, Kang DR, Son T, Kim HI, Noh SH, Hyung WJ (2018) Long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer 21:285–295

    Article  PubMed  Google Scholar 

  32. Shimada H, Fukagawa T, Haga Y, Oba K (2017) Does postoperative morbidity worsen the oncological outcome after radical surgery for gastrointestinal cancers? A systematic review of the literature. Ann Gastroenterol Surg 1:11–23

    Article  PubMed  PubMed Central  Google Scholar 

  33. Gong S, Li X, Tian H, Song S, Lu T, Jing W, Huang X, Xu Y, Wang X, Zhao K, Yang K, Guo T (2022) Clinical efficacy and safety of robotic distal gastrectomy for gastric cancer: a systematic review and meta-analysis. Surg Endosc 36:2734–2748

    Article  PubMed  Google Scholar 

  34. Tang F, Tie Y, Tu C, Wei X (2020) Surgical trauma-induced immunosuppression in cancer: recent advances and the potential therapies. Clin Transl Med 10:199–223

    Article  PubMed  PubMed Central  Google Scholar 

  35. Yamada Y, Higuchi K, Nishikawa K, Gotoh M, Fuse N, Sugimoto N, Nishina T, Amagai K, Chin K, Niwa Y, Tsuji A, Imamura H, Tsuda M, Yasui H, Fujii H, Yamaguchi K, Yasui H, Hironaka S, Shimada K, Miwa H, Hamada C, Hyodo I (2015) Phase III study comparing oxaliplatin plus S-1 with cisplatin plus S-1 in chemotherapy-naïve patients with advanced gastric cancer. Ann Oncol 26:141–148

    Article  CAS  PubMed  Google Scholar 

  36. Lee SL, Hashimoto H, Kohro T, Horiguchi H, Koide D, Komuro I, Fushimi K, Yamazaki T, Yasunaga H (2014) Influence of municipality-level mean income on access to aortic valve surgery: a cross-sectional observational study under Japan’s universal health-care coverage. PLoS ONE 9:e111071

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the surgeons that participated in this study, especially Takahiro Kinoshita (National Cancer Center Hospital, East, Kashiwa, Japan), Shuji Takiguchi (Nagoya City University, Nagoya, Japan), Kazuhisa Ehara (Saitama Cancer Center, Saitama, Japan), Shiro Kuwabara (Niigata City General Hospital, Niigata, Japan), Hiroshi Okabe (New Tokyo Hospital, Matsudo, Chiba), Yoshihiro Hiramatsu (Hamamatsu University, Hamamatsu, Japan), Takeshi Omori (Osaka International Cancer Institute, Osaka, Japan), Yuji Watanabe (Ehime University, Toon, Japan), Hironori Odaira (International University of Health and Welfare, Narita, Japan), Tomohisa Egawa (Saiseikai Yokohamashi Tobu Hospital, Yokohama, Japan), and Yoshiharu Sakai (Kyoto University, Kyoto, Japan). We also thank Takaaki Kato, Takenao Koseki, and Hiroyuki Hiramatsu, who work in the data collection center (Center for Clinical Trial and Research Support, Fujita Health University). We thank Ms. Chie Yamamoto and Mr. Taiki Imaizumi of EP‐CRSU Co., Ltd. (Tokyo, Japan) for their dedicated administrative support. The authors are indebted to Editage (Tokyo, Japan, https://www.editage.jp/info/) for language review of this paper.

Funding

Administrative support for this study, provided by EP-CRSU Co., Ltd, was funded by Intuitive Surgical Sarl. The funder was not involved in the study design; the collection, analysis, and interpretation of data; the writing of this article; or the decision to submit the article for publication.

Author information

Authors and Affiliations

  1. Department of Surgery, Fujita Health University, 1-98 Dengakugakubo, Kutsukake, Toyoake, Aichi, 470-1192, Japan

    Koichi Suda, Susumu Shibasaki & Tsuyoshi Tanaka

  2. Collaborative Laboratory for Research and Development in Advanced Surgical Intelligence, Fujita Health University, Toyoake, Japan

    Koichi Suda

  3. EP‐CRSU Co., Ltd, Tokyo, Japan

    Miyoshi Sakai

  4. Department of Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan

    Kazutaka Obama, Shigeo Hisamori & Tatsuto Nishigori

  5. Department of Surgery, Faculty of Medicine, Saga University, Saga, Japan

    Yukie Yoda & Hirokazu Noshiro

  6. Department of Advanced Robotic and Endoscopic Surgery, Fujita Health University, Toyoake, Japan

    Masaya Nakauchi & Ichiro Uyama

  7. Unit of Public Health and Preventive Medicine, Yokohama City University School of Medicine, Yokohama, Japan

    Ataru Igarashi

  8. Department of Health Economics and Outcomes Research, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan

    Ataru Igarashi

  9. Division of Gastric Surgery, Shizuoka Cancer Center, Shizuoka, Japan

    Masanori Terashima

  10. Collaborative Laboratory for Research and Development in Advanced Surgical Technology, Fujita Health University, Toyoake, Japan

    Ichiro Uyama

Authors
  1. Koichi Suda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miyoshi Sakai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazutaka Obama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yukie Yoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Susumu Shibasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tsuyoshi Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masaya Nakauchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shigeo Hisamori
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tatsuto Nishigori
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ataru Igarashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hirokazu Noshiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Masanori Terashima
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ichiro Uyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors fully met the International Committee of Medical Journal Authors authorship criteria. All the authors read and approved the final manuscript. All authors are accountable for all aspects of this study and are responsible for ensuring that questions related to the accuracy or integrity of any part of the study are appropriately investigated and resolved.

Corresponding author

Correspondence to Koichi Suda.

Ethics declarations

Disclosures

Koichi Suda was funded by Sysmex, Co. in relation to the Collaborative Laboratory for Research and Development in Advanced Surgical Intelligence, Fujita Health University. Koichi Suda also received advisory fees from Medicaroid, Inc., outside of the present study. Tsuyoshi Tanaka and Ichiro Uyama were funded by Medicaroid, Inc. in relation to the Collaborative Laboratory for Research and Development in Advanced Surgical Technology, Fujita Health University. Ichiro Uyama received lecture fees from Intuitive Surgical, Inc., outside of the present study. Kazutaka Obama received lecture fees from Intuitive Surgical, Inc., Medtronic, Ethicon, Medicaroid, Inc., and Olympus, outside of the present study. Ataru Igarashi received research expenses from Intuitive Surgical, Inc., outside of the present study. Masanori Terashima received personal fees from Taiho Pharmaceutical, Chugai Pharmaceutical, Ono Pharmaceutical, BMS, Yakult Honsha, Takeda Pharmaceutical, Eli Lilly Japan, Pfizer Japan, Daiichi-Sankyo, Johnson and Johnson, Medtronic Japan, Intuitive Surgical Japan, and Olympus, outside the submitted work. Miyoshi Sakai, Yukie Yoda, Susumu Shibasaki, Masaya Nakauchi, Shigeo Hisamori, Tatsuto Nishigori, and Hirokazu Noshiro have no conflicts of interest or financial ties to disclose. Koichi Suda, Kazutaka Obama, Tsuyoshi Tanaka, Ataru Igarashi, Masanori Terashima, and Ichiro Uyama have no conflicts of interest or financial ties to disclose in relation to the present study.

Ethical approval

The protocol for this research project has been approved by a suitably constituted Ethics Committee (Institutional Review Board of Fujita Health University, Approval No. HM18-281), and it conforms to the provisions of the Declaration of Helsinki. The opt-out method was used to obtain informed consent from all participating patients. This study was registered in the University Hospital Medical Information Network (UMIN000034366) before the start of the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 168 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suda, K., Sakai, M., Obama, K. et al. Three-year outcomes of robotic gastrectomy versus laparoscopic gastrectomy for the treatment of clinical stage I/II gastric cancer: a multi-institutional retrospective comparative study. Surg Endosc 37, 2858–2872 (2023). https://doi.org/10.1007/s00464-022-09802-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-022-09802-w

Keywords

Search

Navigation