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Impact of laparoscopic gastrectomy on relapse-free survival for locally advanced gastric cancer patients with sarcopenia: a propensity score matching analysis

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Abstract

Background

Recent gastric cancer reports have shown that preoperative sarcopenia worsens long-term prognosis after gastrectomy. We investigated the impact of laparoscopic surgery on the long-term prognosis of locally advanced gastric cancer patients with sarcopenia.

Methods

This retrospective study included consecutive patients who underwent radical gastrectomy for primary c-stage II or III advanced gastric cancer, between April 2008 and April 2017, with computed tomography records of skeletal muscle mass. The skeletal muscle mass index was calculated, and sarcopenia was defined when values were below the cut-off. The patients were divided into a laparoscopy group and open group, in which the background was adjusted using propensity score matching; the relapse-free survival and overall survival were compared between them. The prognostic factors for relapse-free survival and overall survival were investigated by multivariate analyses.

Results

This study included 141 patients with sarcopenia (laparoscopy group, n = 69 [48.9%]; open group, n = 72 [51.1%]). After matching, there were 50 patients in both groups, with no significant differences in patient background. The median follow-up period was 38 months. Relapse-free survival was worse in the open group (hazard ratio: 1.662, 95% confidence interval: 0.910–3.034; P = 0.098), but there was no difference in the overall survival (P = 0.181). Multivariate analysis concluded that open surgery is an independent prognostic factor of relapse-free survival (hazard ratio: 3.219, 95% confidence interval: 1.381–7.502; P = 0.007) but not of OS.

Conclusion

Compared with the open surgery group, the laparoscopy group had a better RFS, although the difference was not statistically significant.

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References

  1. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39:412–23

    Article  Google Scholar 

  2. Kamarajah SK, Bundred J, Tan BHL (2019) Body composition assessment and sarcopenia in patients with gastric cancer: a systematic review and meta-analysis. Gastric Cancer 22:10–22

    Article  Google Scholar 

  3. Simonsen C, de Heer P, Bjerre ED, Suetta C, Hojman P, Pedersen BK, Svendsen LB, Christensen JF (2018) Sarcopenia and postoperative complication risk in gastrointestinal surgical oncology: a meta-analysis. Ann Surg 268:58–69

    Article  Google Scholar 

  4. Shen Y, Hao Q, Zhou J, Dong B (2017) The impact of frailty and sarcopenia on postoperative outcomes in older patients undergoing gastrectomy surgery: a systematic review and meta-analysis. BMC Geriatr 17:188

    Article  Google Scholar 

  5. Yang Z, Zhou X, Ma B, Xing Y, Jiang X, Wang Z (2018) Predictive Value of Preoperative sarcopenia in patients with gastric cancer: a meta-analysis and systematic review. J Gastrointest Surg 22:1890–1902

    Article  Google Scholar 

  6. Takiguchi S, Fujiwara Y, Yamasaki M, Miyata H, Nakajima K, Sekimoto M, Mori M, Doki Y (2013) Laparoscopy-assisted distal gastrectomy versus open distal gastrectomy. a prospective randomized single-blind study. World J Surg 37:2379–2386

    Article  Google Scholar 

  7. Sakuramoto S, Yamashita K, Kikuchi S, Futawatari N, Katada N, Watanabe M, Okutomi T, Wang G, Bax L (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 27:1695–1705

    Article  Google Scholar 

  8. Japanese Gastric Cancer Association (2017) Japanese Gastric Cancer Treatment Guidelines 2014 (Ver. 4). Gastric Cancer 20:1–19

    Article  Google Scholar 

  9. Zhang Y, Wang JP, Wang XL, Tian H, Gao TT, Tang LM, Tian F, Wang JW, Zheng HJ, Zhang L, Gao XJ, Li GL, Wang XY (2018) Computed tomography-quantified body composition predicts short-term outcomes after gastrectomy in gastric cancer. Curr Oncol 25:e411–e422

    Article  CAS  Google Scholar 

  10. Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transplant 48:452–458

    Article  CAS  Google Scholar 

  11. 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 357:1810–20

    Article  CAS  Google Scholar 

  12. Sasako M, Sakuramoto S, Katai H, Kinoshita T, Furukawa H, Yamaguchi T, Nashimoto A, Fujii M, Nakajima T, Ohashi Y (2011) Five-year outcomes of a randomized phase III trial comparing adjuvant chemotherapy with S-1 versus surgery alone in stage II or III gastric cancer. J Clin Oncol 29:4387–4393

    Article  CAS  Google Scholar 

  13. Noh SH, Park SR, Yang HK, Chung HC, Chung IJ, Kim SW, Kim HH, Choi JH, Kim HK, Yu W, Lee JI, Shin DB, Ji J, Chen JS, Lim Y, Ha S, Bang YJ, CLASSIC Trial Investigators (2014) Adjuvant capecitabine plus oxaliplatin for gastric cancer after D2 gastrectomy (CLASSIC): 5-year follow-up of an open-label, randomised phase 3 trial. Lancet Oncol 15:1389–1396

    Article  CAS  Google Scholar 

  14. Yoshida K, Kodera Y, Kochi M, Ichikawa W, Kakeji Y, Sano T, Nagao N, Takahashi M, Takagane A, Watanabe T, Kaji M, Okitsu H, Nomura T, Matsui T, Yoshikawa T, Matsuyama J, Yamada M, Ito S, Takeuchi M, Fujii M (2019) Addition of docetaxel to oral fluoropyrimidine improves efficacy in patients with stage III gastric cancer: interim analysis of JACCRO GC-07, a randomized controlled trial. J Clin Oncol 37:1296–1304

    Article  CAS  Google Scholar 

  15. Yoshikawa T, Terashima M, Mizusawa J, Nunobe S, Nishida Y, Yamada T, Kaji M, Fukushima N, Hato S, Choda Y, Yabusaki H, Yoshida K, Ito S, Takeno A, Yasuda T, Kawachi Y, Katayama H, Fukuda H, Boku N, Sano T, Sasako M (2019) Four courses versus eight courses of adjuvant S-1 for patients with stage II gastric cancer (JCOG1104 [OPAS-1]): an open-label, phase 3, non-inferiority, randomised trial. Lancet Gastroenterol Hepatol 4:208–216

    Article  Google Scholar 

  16. Cao J, Qi F, Liu T (2014) Adjuvant chemotherapy after curative resection for gastric cancer: a meta-analysis. Scand J Gastroenterol 49:690–704

    Article  CAS  Google Scholar 

  17. Aoyama T, Sato T, Hayashi T, Yamada T, Cho H, Ogata T, Oba K, Yoshikawa T (2018) Does a laparoscopic approach attenuate the body weight loss and lean body mass loss observed in open distal gastrectomy for gastric cancer? a single- institution exploratory analysis of the JCOG 0912 phase III trial. Gastric Cancer 21:345–352

    Article  CAS  Google Scholar 

  18. Aoyama T, Yoshikawa T, Maezawa Y, Kano K, Hara K, Sato T, Hayashi T, Yamada T, Cho H, Ogata T, Tamagawa H, Yukawa N, Rino Y, Masuda M, Oshima T (2018) A comparison of the body composition changes between laparoscopy-assisted and open total gastrectomy for gastric cancer. In Vivo 32:1513–1518

    Article  CAS  Google Scholar 

  19. Yamaoka Y, Fujitani K, Tsujinaka T, Yamamoto K, Hirao M, Sekimoto M (2015) Skeletal muscle loss after total gastrectomy, exacerbated by adjuvant chemotherapy. Gastric Cancer 18:382–389

    Article  CAS  Google Scholar 

  20. Aoyama T, Yoshikawa T, Shirai J, Hayashi T, Yamada T, Tsuchida K, Hasegawa S, Cho H, Yukawa N, Oshima T, Rino Y, Masuda M, Tsuburaya A (2013) Body weight loss after surgery is an independent risk factor for continuation of S-1 adjuvant chemotherapy for gastric cancer. Ann Surg Oncol 20:2000–2006

    Article  Google Scholar 

  21. Aoyama T, Kawabe T, Fujikawa H, Hayashi T, Yamada T, Tsuchida K, Yukawa N, Oshima T, Rino Y, Masuda M, Ogata T, Cho H, Yoshikawa T (2015) Loss of lean body mass as an independent risk factor for continuation of S-1 adjuvant chemotherapy for gastric cancer. Ann Surg Oncol 22:2560–2566

    Article  Google Scholar 

  22. Takayoshi K, Uchino K, Nakano M, Ikejiri K, Baba E (2017) Weight loss during initial chemotherapy predicts survival in patients with advanced gastric cancer. Nutr Cancer 69:408–415

    Article  CAS  Google Scholar 

  23. Aoyama T, Sato T, Maezawa Y, Kano K, Hayashi T, Yamada T, Yukawa N, Oshima T, Rino Y, Masuda M, Ogata T, Cho H, Yoshikawa T (2017) Postoperative weight loss leads to poor survival through poor S-1 efficacy in patients with stage II/III gastric cancer. Int J Clin Oncol 22(3):476–483

    Article  Google Scholar 

  24. Kudou K, Saeki H, Nakashima Y, Kimura K, Ando K, Oki E, Ikeda T, Maehara Y (2019) Postoperative skeletal muscle loss predicts poor prognosis of adenocarcinoma of upper stomach and esophagogastric junction. World J Surg 43:1068–1075

    Article  Google Scholar 

  25. Kugimiya N, Harada E, Oka K, Kawamura D, Suehiro Y, Takemoto Y, Hamano K (2018) Loss of skeletal muscle mass after curative gastrectomy is a poor prognostic factor. Oncol Lett 16:1341–1347

    PubMed  PubMed Central  Google Scholar 

  26. Daly LE, Ní Bhuachalla ÉB, Power DG, Cushen SJ, James K, Ryan AM (2018) Loss of skeletal muscle during systemic chemotherapy is prognostic of poor survival in patients with foregut cancer. J Cachexia Sarcopenia Muscle 9:315–325

    Article  Google Scholar 

  27. Aoyama T, Yoshikawa T, Maezawa Y, Kano K, Numata M, Hara K, Komori K, Yamada T, Hayashi T, Sato T, Tamagawa H, Yukawa N, Rino Y, Masuda M, Ogata T, Cho H, Oshima T (2019) The postoperative lean body mass loss at one month leads to a poor survival in patients with locally advanced gastric cancer. J Cancer 10:2450–2456

    Article  CAS  Google Scholar 

  28. Inaki N, Etoh T, Ohyama T, Uchiyama K, Katada N, Koeda K, Yoshida K, Takagane A, Kojima K, Sakuramoto S, Shiraishi N, Kitano S (2015) A multi-institutional, 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

    Article  Google Scholar 

  29. Lee HJ, Hyung WJ, Yang HK, Han SU, Park YK, An JY, Kim W, Kim HI, Kim HH, Ryu SW, Hur H, Kong SH, Cho GS, Kim JJ, Park DJ, Ryu KW, Kim YW, Kim JW, Lee JH, Kim MC, Korean Laparo-endoscopic Gastrointestinal Surgery Study (KLASS) Group (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 270:983–91

    Article  Google Scholar 

  30. Shi Y, Xu X, Zhao Y, Qian F, Tang B, Hao Y, Luo H, Chen J, Yu P (2018) Short-term surgical outcomes of a randomized controlled trial comparing laparoscopic versus open gastrectomy with D2 lymph node dissection for advanced gastric cancer. Surg Endosc 32:2427–2433

    Article  Google Scholar 

  31. Viñuela 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 255:446–456

    Article  Google Scholar 

  32. 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  Google Scholar 

  33. Zou ZH, Zhao LY, Mou TY, Hu YF, Yu J, Liu H, Chen H, Wu JM, An SL, Li GX (2014) Laparoscopic vs open D2 gastrectomy for locally advanced gastric cancer: a meta-analysis. World J Gastroenterol 20:16750–16764

    Article  Google Scholar 

  34. Huang YL, Lin HG, Yang JW, Jiang FQ, Zhang T, Yang HM, Li CL, Cui Y (2014) Laparoscopy-assisted versus open gastrectomy with D2 lymph node dissection for advanced gastric cancer: a meta-analysis. Int J Clin Exp Med 7:1490–1499

    PubMed  PubMed Central  Google Scholar 

  35. Cheng Q, Pang TC, Hollands MJ, Richardson AJ, Pleass H, Johnston ES, Lam VW (2014) Systematic review and meta-analysis of laparoscopic versus open distal gastrectomy. J Gastrointest Surg 18:1087–1099

    Article  Google Scholar 

  36. Wang S, Xu L, Wang Q, Li J, Bai B, Li Z, Wu X, Yu P, Li X, Yin J (2019) Postoperative complications and prognosis after radical gastrectomy for gastric cancer: a systematic review and meta-analysis of observational studies. World J Surg Oncol 17:52

    Article  Google Scholar 

  37. Jiang N, Deng JY, Ding XW, Zhang L, Liu HG, Liang YX, Liang H (2014) Effect of complication grade on survival following curative gastrectomy for carcinoma. World J Gastroenterol 20:8244–8252

    Article  Google Scholar 

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Acknowledgements

We would like to thank Dr. Shoryoku Hino for providing appropriate advice in the statistical analysis.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not for profit sectors.

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Authors and Affiliations

  1. Department of Gastroenterological Surgery, Ishikawa Prefectural Central Hospital, Kanazawa, Japan

    Ryota Matsui, Noriyuki Inaki & Toshikatsu Tsuji

  2. Department of Surgery, Juntendo University Urayasu Hospital, Urayasu, Japan

    Ryota Matsui

  3. Department of Gastrointestinal Surgery/Breast Surgery, Kanazawa University Graduate School of Medical Sciences, 13-1 Takara-machi, Kanazawa, Ishikawa, 920-8641, Japan

    Noriyuki Inaki

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  1. Ryota Matsui
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Contributions

Substantial contributions to the study conception and design, data acquisition or analysis, and data interpretation. Drafting the manuscript or reviewing it critically for important intellectual content. Approval of the final version of the manuscript. The main role of the authors was as follows: (1) Guarantor of the integrity of the entire study: NI. (2) Study conception and design: RM and NI. (3) Literature search: RM. (4) Clinical studies: All authors. (5) Data collection: RM and TT. (6) Statistical analysis: RM. (7) Manuscript preparation: RM and NI. (8) Manuscript review: all authors.

Corresponding author

Correspondence to Noriyuki Inaki.

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Disclosures

Drs. Ryota Matsui, Noriyuki Inaki, and Toshikatsu Tsuji have no conflicts of interest or financial ties to disclose.

Ethical approval

All experimental protocols described in this study were approved by the Institutional Ethical Review Committee of the Ishikawa Prefectural Central Hospital (authorization number: 1585). All procedures followed were in accordance with the ethical guidelines of Japan’s Ministry of Health, Labor, and Welfare for medical and health research involving human subjects and with the Helsinki Declaration of 1964 and later versions.

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The opt-out recruitment method was applied to provide all patients an opportunity to decline to participate.

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Matsui, R., Inaki, N. & Tsuji, T. Impact of laparoscopic gastrectomy on relapse-free survival for locally advanced gastric cancer patients with sarcopenia: a propensity score matching analysis. Surg Endosc 36, 4721–4731 (2022). https://doi.org/10.1007/s00464-021-08812-4

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  • DOI: https://doi.org/10.1007/s00464-021-08812-4

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