Skip to main content
Download PDF

Comparative analysis of robotic gastrectomy and laparoscopic gastrectomy for gastric cancer in terms of their long-term oncological outcomes: a meta-analysis of 3410 gastric cancer patients

World Journal of Surgical Oncology volume 17, Article number: 86 (2019) Cite this article

Abstract

Background

Data regarding the long-term oncological outcomes of robotic gastrectomy (RG) are limited despite the increased commonality of this method as an alternative for gastric cancer treatment. Here, we conducted a meta-analysis to evaluate the long-term oncological outcomes of RG in comparison to that of laparoscopic gastrectomy (LG).

Methods

The PubMed, ISI Web of Science, EMBASE, and Cochrane Library databases were comprehensively searched for studies that compared RG and LG in terms of their long-term survival outcomes. The hazard ratios (HRs) of overall survival (OS), disease-free survival (DFS), and relapse-free survival (RFS) were obtained, while the odds ratio (OR) was recorded for the recurrence rate. A sensitivity analysis was performed. Egger’s test and Begg’s test were applied to evaluate publication bias.

Results

Eight studies were identified and involved 3410 gastric cancer patients (RG, 1009; LG, 2401). The two groups had no significant differences in OS (HR, 0.98; 95% CI, 0.80–1.20; P = 0.81), DFS (HR, 1.36; 95% CI, 0.33–5.59; P = 0.67), RFS (HR, 0.92; 95% CI, 0.72–1.19; P = 0.53), or recurrence rate (OR, 0.92; 95% CI, 0.71–1.19; P = 0.53). Moreover, the two techniques were comparable in length of hospital stay (LOS), postoperative complication rate, 30-day mortality rate, and rate of conversion to open surgery.

Conclusions

The long-term oncological outcomes, expressed as OS, DFS, RFS, and recurrence rate, were similar between RG and LG. However, more randomized controlled trials with rigorous study designs and patient cohorts are needed to evaluate the oncologic outcomes of RG in patients with gastric cancer.

Introduction

Gastric cancer (GC) is the third leading cause of cancer death, with 782,685 (8.2%) deaths (both sexes, all ages) and 1,033,701 (5.7%) new cases (both sexes, all ages) in 2018, making GC the fifth most common cancer worldwide [1]. Despite progress in multidisciplinary therapy, radical excision is regarded as the most effective curative treatment approach [2]. The safety and feasibility of laparoscopic gastrectomy (LG) are confirmed in the literature [3,4,5]. However, conventional laparoscopy has some limitations, including poor imaging, loss of faculties, and a long learning curve [6]. The application of robotic-assisted devices may surmount the technical drawbacks of laparoscopic surgery.

Many studies have demonstrated the safety and feasibility of treating gastric cancer with RG regarding the intraoperative outcomes and short-term outcomes. Some studies indicate that RG and LG are comparable [7,8,9]. However, the data are limited and mostly focus on the prognosis of RG; thus, we conducted an updated meta-analysis to provide a more comprehensive assessment of the two techniques.

Methods

Search strategies

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement was applied to perform the meta-analysis [10]. The search was independently performed by two authors (G.L. and Z.Z.) in October 3, 2018. The databases included PubMed (from 1980 to October 2018), ISI Web of Science (from 2000 to October 2018), Cochrane Library (from 1950 to October 2018), and EMBASE (from January 1990 to October 2018). The following search terms were employed: robotic, gastric cancer, gastrectomy, survival, and prognosis. The search strategy is shown in Additional file 1. The search had no language restrictions.

Inclusion and exclusion criteria

The search was independently conducted by two reviewers (G.L. and Z.Z.). The relevant data were recorded by the reviewers (G.L. and Z.Z.). If there was a disagreement, the reviewers discussed the issue and finally made a decision.

The inclusion criteria were as follows: (1) studies focused on resectable gastric cancer, (2) studies comparing RG and LG to evaluate the safety and feasibility of each technique, and (3) studies that effectively reported the prognosis after surgical intervention, and the prognosis was described in terms of overall survival (OS), disease-free survival (DFS), recurrence-free survival (RFS), or the recurrence rate. The time from surgery to all-cause death or the last follow-up in the study was defined as OS. The time to cancer recurrence, development of a second cancer, or disease development was defined as DFS. The time from surgery to cancer recurrence was defined as RFS.

Exclusion criteria

The exclusion criteria were as follows: (1) studies that were not focused on resectable gastric cancer; (2) studies that were non-comparative studies; (3) studies that were reviews or conference abstracts and were not human studies.

Outcomes of interest and data extraction

Two authors (G.L. and Z.Z.) carefully and independently reviewed the included studies and extracted the effective data in a standard form. The data included the basic characteristics of the study (author, publication year, country, cases in each group, age, body mass index, TNM stage, and the number of harvested lymph nodes). The primary outcomes were the survival outcomes, including OS, DFS, RFS and recurrence rate. The secondary outcomes included the length of hospital stay (LOS), postoperative complications, 30-day mortality, and the rate of conversion to open surgery. The follow-up time of each included study was recorded. If different opinions existed, the authors conducted a full discussion and a final decision was made.

Quality assessment

The quality of the included studies was evaluated with the Newcastle-Ottawa Scale. This quality assessment evaluated the cohort selection, comparability, and ascertainment of the outcomes [11]. The study quality was divided into three categories: poor, fair, and good.

Statistical analysis

Review Manager 5.3 software (Collaboration, Oxford, UK) was applied for pooling the meta-analysis. If the survival data were provided with HRs and 95% CIs, we extracted the data directly for meta-analysis. Otherwise, if the survival data were shown as Kaplan-Meier survival curves, we used the Engauge Digitizer (version 4.1) to estimate the HRs and 95% CIs and reconstruct the HR and standard error (SE), as described by Tierney et al. [12]. Dichotomous parameters were recorded as odds ratios (ORs) and 95% CIs. Risk difference (RD) was applied if both groups had no event occurrences. Continuous variables were assessed using the mean difference (MD). The I2 statistic was applied to test heterogeneity. If I2 < 50%, a fixed-effects model was adopted. Otherwise, the random-effects model was adopted. Sensitivity analysis was performed. Egger’s test and Begg’s test were applied to assess publication bias. The significance level was set at P < 0.05.

Results

Our comprehensive literature search identified 589 studies. There were 154 papers from PubMed, 182 papers from Web of Knowledge electronic database, 237 papers from EMBASE, and 46 papers from the Cochrane Library. We used Endnote software and removed 388 duplicated papers. The titles and abstracts of the remaining 231 papers were screened, and 10 papers potentially suitable for analysis were identified. After a thorough review of the full text of the 10 papers, one paper was excluded because it was a letter [13], and another study was excluded because the survival data were insufficient for analysis [14]. Finally, eight papers were included for our meta-analysis [15,16,17,18,19,20,21,22]. The study selection process is shown in Fig. 1. The basic characteristics are presented in Table 1. There were three papers from China, two papers from Japan, two papers from Korea, and one paper from Italy. Three studies were published in 2018 and included propensity score matching (PSM) analyses. In total, 1009 (29.60%) gastric cancer patients underwent RG, and 2401 (70.41%) gastric cancer patients underwent LG. All of the included studies were retrospective studies. The quality was fair for the study from Pugliese et al. [21] and was good in the rest of the studies.

Fig. 1
figure 1

The study selection process

Full size image
Table 1 The general characteristics of the extracted data and quality of the included studies
Full size table

The primary outcomes

All of the included studies reported OS outcomes [15,16,17,18,19,20,21,22]. The pooled data from the eight studies indicated no significant difference between the two groups (HR, 0.98; 95% CI, 0.80–1.20; P = 0.81), and a fixed-effects model was adopted due to the lack of significant heterogeneity (I2 = 0, P = 0.94, Fig. 2a). Only one study reported DFS results [16]; there was no significant difference between the two groups in DFS, the HR was 1.08 with a 95% CI from 0.26 to 4.44, and the P value was 0.67. Four studies described the RFS results [15,16,17, 20]. A meta-analysis of the four studies indicated that the two techniques had similar RFS outcomes (HR, 0.92; 95% CI, 0.72–1.19; P = 0.53). The analysis showed no significant heterogeneity (I2 = 0%, P = 0.97) using a fixed-effects model (Fig. 2b). Seven studies, with a total of 2780 gastric cancer patients, reported recurrence rates. In total, the recurrence rate was 12.63% (109/863) in the RG group and 13.30% (255/1917) in the LG group. The pooled data from the seven studies suggested that the recurrence rate was similar between the two techniques (OR, 0.92; 95% CI, 0.71–1.19; P = 0.53). The analysis had no obvious heterogeneity (I2 = 0, P = 0.71) (Fig. 2c).

Fig. 2
figure 2

Meta-analysis of survival outcomes between robotic gastrectomy (RG) and laparoscopic gastrectomy (LG): a overall survival, b relapse-free survival, and c recurrence rate

Full size image

The secondary outcomes

The two techniques had a comparable LOS (MD, − 0.24; 95% CI, − 0.60 to 0.11; P = 0.16) based on the pooled data from all the included studies [12, 15,16,17,18,19,20,21,22], and a fixed- effect model was adopted because there was no heterogeneity (Fig. 3a). Moreover, the two groups had similar rates in postoperative complications (OR, 0.90; 95% CI, 0.72–1.12; P = 0.34) (Fig. 3b), 30-day mortality (RD, 0.01; 95% CI, 0.00–0.01; P = 0.19) (Fig. 3c), and conversion to open surgery (RD, 0.00; 95% CI, − 0.01 to 0.01, P = 0.67) (Fig. 3d). These results were all measured using fixed- effects models due to the lack of significant heterogeneity.

Fig. 3
figure 3

Pooled data for the outcomes of interest between patients who underwent robotic gastrectomy (RG) and laparoscopic gastrectomy (LG): a length of hospital stay, b postoperative complication, c 30-day mortality, and d conversion to open surgery

Full size image

Sensitivity analysis

Three papers performed PSM analyses. We conducted a sensitivity analysis for papers that performed PSM analyses [15,16,17]. In terms of OS, the results showed that there was no significant difference between the two techniques (HR, 1.06; 95% CI, 0.81–1.38; P = 0.69) (Fig. 4a). In terms of RFS, the result was not influenced by the surgical technique (HR, 0.96; 95% CI, 0.76–1.23; P = 0.77), and there was no obvious heterogeneity (I2 = 12, P = 0.32) (Fig. 4b).

Fig. 4
figure 4

Sensitivity analysis of the studies that performed propensity score matching analyses for a overall survival and for b relapse-free survival

Full size image

Publication bias

A funnel plot for recurrence rate was adopted to assess publication bias. No evidence of publication bias was found, and all the results were within the 95% CI (Fig. 5). The statistical analysis revealed no significant publication bias (Begg’s test P = 0.764 and Egger’s test P = 0.571).

Fig. 5
figure 5

Funnel plot of the relapse rate between patients who underwent robotic gastrectomy (RG) and laparoscopic gastrectomy (LG). OR, odds ratio; SE, standard error

Full size image

Discussion

Currently, the benefits of treating gastric cancer with the laparoscopic technique have been well recognized. Many documents have indicated that compared to open surgery, laparoscopic surgery can improve the safety and efficacy of treating gastric cancer [23,24,25,26]. However, there are some limitations to laparoscopic gastric surgery. These drawbacks include poor imaging, inconvenient lymph node dissection in a narrow space, technical complexity, and a long and steep learning curve [27]. In an effort to address the drawbacks of the laparoscopic technique, robotic-assisted surgical systems were introduced. These surgical systems could offer some improvements in visibility and manipulation [28].

A body of literature has been published and indicates that RG is as safe and effective as LG [9, 29, 30]. Moreover, RG could reduce intraoperative blood loss and reduce the length of the hospital stay but requires a longer operative time [31].

In contrast, only a few studies focus on prognosis after RG as this technology has only existed for less than 20 years. However, as GC is a malignant tumor, the prognosis and long-term outcomes of GC patients are major concerns for surgeons [32]. Recently, some studies focusing on the prognosis after RG and LG have been published [15,16,17]. Hence, we performed this study to evaluate the long-term outcomes associated with the two techniques.

Our meta-analysis included eight studies involving 3410 patients. The results of our meta-analysis revealed no significant differences in OS, DFS, RFS, and recurrence rate between the RG and LG groups. These results indicate that the two approaches have similar long-term oncologic outcomes. Moreover, the two techniques were comparable in LOS, postoperative complication rate, 30-day mortality rate, and rate of conversion to open surgery. In the sensitivity analysis, the OS and RFS outcomes were not influenced after PSM between the two approaches. These results indicate that for the management of gastric cancer, RG is a safe technique in terms of oncologic outcomes.

The treatment of gastric cancer requires a multidisciplinary effort. It is recommended to include surgery, chemotherapy, and radiation therapy in treating gastric cancer [33]. For gastric cancer surgery, achieving R0 resection is a vital factor for prognosis, while R1 and R2 resection might predict worse survival outcomes [34, 35]. The benefits of RG in terms of visibility and manipulation might provide a good quality of surgery and thus might produce good oncologic outcomes. OS is a major oncologic outcome. In this study, the five-year OS was similar to that previously reported [36]. Furthermore, the results also indicate the oncological safety of RG as well as that of LG.

It is reported that the recurrence rate in gastric cancer patients is nearly 50% within 5 years after surgery [37], and 50–90% of patients die of tumour relapse [38]. To the best of our knowledge, no meta-analysis has previously reported RFS with RG and LG. Our meta-analysis indicates no significant difference in the two groups in terms of the RFS outcome. Moreover, in this meta-analysis, seven studies reported recurrence rates. The RFS and recurrence rate results further prove the comparability between RG and LG in terms of long-term oncological outcomes. It has been reported that after LG, lymph node metastasis can predict the recurrence of gastric cancer [39]. Nakauchi et al. demonstrated similar profiles for sites of recurrence between the two groups [20]. The recurrence rate was 12.63% in the RG group and 13.30% in the LG group. The recurrence rate in the RG group was similar to that in the LG group.

Moreover, no significant difference was found in the LOS between the two approaches. This was consistent with a previous meta-analysis [40]. Regarding the postoperative complication rate and 30-day mortality rate, the rates were equivalent between the two groups [6,7,8]. Furthermore, the comparable rate of conversion to open surgery also indicated that RG was as safe and effective as LG [6,7,8].

To minimize selection bias in these two approaches, we performed a sensitivity meta-analysis based on the studies that applied PSM. The results also indicate that the two groups had no significant differences.

Limitations in this meta-analysis should be taken into account. First, the studies included for analysis were retrospective studies, and none of the studies were randomized controlled trials. Pooling the retrospective studies may affect the effective power of an intervention [4], which could result in publication bias. However, there was no significant publication bias in this meta-analysis. Second, some studies did not provide HRs and SEs directly, and these data were extracted from the survival curves, which could introduce a potential source of bias. Third, adjuvant treatment might have been applied for the patients, and the differences in adjuvant treatment might also affect the individual survival time. Fourth, seven out of the eight included studies were located in East Asian countries, and the data regarding Western countries are limited. The applicability and generalizability of these results are limited. These results should be interpreted with caution. Fifth, most studies were from a single centre in Eastern countries. Multi-centre, prospective randomized controlled trials and high-quality studies are needed in the future. Fortunately, a randomized controlled trial study is ongoing [41].

Conclusion

RG is safe and effective and is comparable to LG. The two groups had similar OS, DFS, RFS, and recurrence rates after a long-term follow-up. Moreover, more randomized controlled trials with rigorous study designs and patient cohorts are needed to evaluate the long-term outcomes of RG in patients with gastric cancer.

Availability of data and materials

The data in this manuscript are all provided in the tables and texts.

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.

    Article  Google Scholar 

  2. Sano T, Sasako M, Yamamoto S, Nashimoto A, Kurita A, Hiratsuka M, Tsujinaka T, Kinoshita T, Arai K, Yamamura Y, Okajima K. 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. 2004;22:2767–73.

    Article  Google Scholar 

  3. Katai H, Mizusawa J, Katayama H, Takagi M, Yoshikawa T, Fukagawa T, Terashima M, Misawa K, Teshima S, Koeda K, et al. Short-term surgical outcomes from a phase III study of laparoscopy-assisted versus open distal gastrectomy with nodal dissection for clinical stage IA/IB gastric cancer: Japan Clinical Oncology Group Study JCOG0912. Gastric Cancer. 2017;20:699–708.

    Article  Google Scholar 

  4. Vinuela EF, Gonen M, Brennan MF, Coit DG, Strong VE. Laparoscopic versus open distal gastrectomy for gastric cancer: a meta-analysis of randomized controlled trials and high-quality nonrandomized studies. Ann Surg. 2012;255:446–56.

    Article  Google Scholar 

  5. Wei Y, Yu D, Li Y, Fan C, Li G. Laparoscopic versus open gastrectomy for advanced gastric cancer: A meta-analysis based on high-quality retrospective studies and clinical randomized trials. Clin Res Hepatol Gastroenterol. 2018;42:577-90.

    Article  Google Scholar 

  6. Liao G, Chen J, Ren C, Li R, Du S, Xie G, Deng H, Yang K, Yuan Y. Robotic versus open gastrectomy for gastric cancer: a meta-analysis. Plos One. 2013;8:e81946.

    Article  Google Scholar 

  7. Chen K, Pan Y, Zhang B, Maher H, Wang XF, Cai XJ. Robotic versus laparoscopic Gastrectomy for gastric cancer: a systematic review and updated meta-analysis. BMC Surg. 2017;17:93.

    Article  Google Scholar 

  8. Duan BS, Zhao J, Xie LF, Wang Y. Robotic verse laparoscopic gastrectomy for gastric cancer: a pooled analysis of 11 individual studies. Surg Laparosc Endosc Percutan Tech. 2017;27:147–53.

    Article  Google Scholar 

  9. Liao GX, Xie GZ, Li R, Zhao ZH, Sun QQ, Du SS, Ren C, Li GX, Deng HJ, Yuan YW. Meta-analysis of outcomes compared between robotic and laparoscopic gastrectomy for gastric cancer. Asian Pac J Cancer Prev. 2013;14:4871–5.

    Article  Google Scholar 

  10. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.

    Article  Google Scholar 

  11. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. NewCastle-Ottawa Quality Assessment Scale –cohort studies [EB/OL]. (2018). Available online at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (Accessed 06 Dec 2018)

  12. Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.

    Article  Google Scholar 

  13. Kim JW. After propensity score matching in long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer. 2018;21:1071.

    Article  Google Scholar 

  14. Leung K, Sun Z, Nussbaum DP, Adam MA, Worni M, Blazer DR. Minimally invasive gastrectomy for gastric cancer: a national perspective on oncologic outcomes and overall survival. Surg Oncol. 2017;26:324–30.

    Article  Google Scholar 

  15. Gao Y, Xi H, Qiao Z, Li J, Zhang K, Xie T, Shen W, Cui J, Wei B, Chen L. Comparison of robotic- and laparoscopic-assisted gastrectomy in advanced gastric cancer: updated short- and long-term results. Surg Endosc. 2019;33:528–34.

    Article  Google Scholar 

  16. Li Z, Li J, Li B, Bai B, Liu Y, Lian B, Zhao Q. Robotic versus laparoscopic gastrectomy with D2 lymph node dissection for advanced gastric cancer: a propensity score-matched analysis. Cancer Manag Res. 2018;10:705–14.

    Article  Google Scholar 

  17. Obama K, Kim YM, Kang DR, Son T, Kim HI, Noh SH, Hyung WJ. Long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer. 2018;21:285–95.

    Article  Google Scholar 

  18. Junfeng Z, Yan S, Bo T, Yingxue H, Dongzhu Z, Yongliang Z, Feng Q, Peiwu Y. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: comparison of surgical performance and short-term outcomes. Surg Endosc. 2014;28:1779–87.

    Article  Google Scholar 

  19. Lee J, Kim YM, Woo Y, Obama K, Noh SH, Hyung WJ. Robotic distal subtotal gastrectomy with D2 lymphadenectomy for gastric cancer patients with high body mass index: comparison with conventional laparoscopic distal subtotal gastrectomy with D2 lymphadenectomy. Surg Endosc. 2015;29:3251–60.

    Article  Google Scholar 

  20. Nakauchi M, Suda K, Susumu S, Kadoya S, Inaba K, Ishida Y, Uyama I. Comparison of the long-term outcomes of robotic radical gastrectomy for gastric cancer and conventional laparoscopic approach: a single institutional retrospective cohort study. Surg Endosc. 2016;30:5444–52.

    Article  Google Scholar 

  21. Pugliese R, Maggioni D, Sansonna F, Costanzi A, Ferrari GC, Di Lernia S, Magistro C, De Martini P, Pugliese F. Subtotal gastrectomy with D2 dissection by minimally invasive surgery for distal adenocarcinoma of the stomach: results and 5-year survival. Surg Endosc. 2010;24:2594–602.

    Article  Google Scholar 

  22. Son T, Lee JH, Kim YM, Kim HI, Noh SH, Hyung WJ. Robotic spleen-preserving total gastrectomy for gastric cancer: comparison with conventional laparoscopic procedure. Surg Endosc. 2014;28:2606–15.

    Article  Google Scholar 

  23. Kataoka K, Katai H, Mizusawa J, Katayama H, Nakamura K, Morita S, Yoshikawa T, Ito S, Kinoshita T, Fukagawa T, Sasako M. Non-randomized confirmatory trial of laparoscopy-assisted total gastrectomy and proximal gastrectomy with nodal dissection for clinical stage i gastric cancer: Japan Clinical Oncology Group Study JCOG1401. J Gastric Cancer. 2016;16:93–7.

    Article  Google Scholar 

  24. Kim YW, Yoon HM, Yun YH, Nam BH, Eom BW, Baik YH, Lee SE, Lee Y, Kim YA, Park JY, Ryu KW. Long-term outcomes of laparoscopy-assisted distal gastrectomy for early gastric cancer: result of a randomized controlled trial (COACT 0301). Surg Endosc. 2013;27:4267–76.

    Article  Google Scholar 

  25. Sakuramoto S, Yamashita K, Kikuchi S, Futawatari N, Katada N, Watanabe M, Okutomi T, Wang G, Bax L. 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. 2013;27:1695–705.

    Article  Google Scholar 

  26. Lu W, Gao J, Yang J, Zhang Y, Lv W, Mu J, Dong P, Liu Y. Long-term clinical outcomes of laparoscopy-assisted distal gastrectomy versus open distal gastrectomy for early gastric cancer: A comprehensive systematic review and meta-analysis of randomized control trials. Medicine (Baltimore). 2016;95:e3986.

    Article  Google Scholar 

  27. Jin SH, Kim DY, Kim H, Jeong IH, Kim MW, Cho YK, Han SU. Multidimensional learning curve in laparoscopy-assisted gastrectomy for early gastric cancer. Surg Endosc. 2007;21:28–33.

    Article  Google Scholar 

  28. Pigazzi A, Ellenhorn JD, Ballantyne GH, Paz IB. Robotic-assisted laparoscopic low anterior resection with total mesorectal excision for rectal cancer. Surg Endosc. 2006;20:1521–5.

    Article  CAS  Google Scholar 

  29. Yang SY, Roh KH, Kim YN, Cho M, Lim SH, Son T, Hyung WJ, Kim HI. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer. Ann Surg Oncol. 2017;24:1770–7.

    Article  Google Scholar 

  30. Eom BW, Yoon HM, Ryu KW, Lee JH, Cho SJ, Lee JY, Kim CG, Choi IJ, Lee JS, Kook MC, et al. Comparison of surgical performance and short-term clinical outcomes between laparoscopic and robotic surgery in distal gastric cancer. Eur J Surg Oncol. 2012;38:57–63.

    Article  CAS  Google Scholar 

  31. Wang Z, Wang Y, Liu Y. Comparison of short outcomes between laparoscopic and experienced robotic gastrectomy: A meta-analysis and systematic review. J Minim Access Surg. 2017;13:1–6.

    Article  Google Scholar 

  32. Tsai SH, Liu CA, Huang KH, Lan YT, Chen MH, Chao Y, Lo SS, Li AF, Wu CW, Chiou SH, et al. Advances in laparoscopic and robotic gastrectomy for gastric cancer. Pathol Oncol Res. 2017;23:13–7.

    Article  Google Scholar 

  33. Ajani JA, Bentrem DJ, Besh S, D’Amico TA, Das P, Denlinger C, Fakih MG, Fuchs CS, Gerdes H, Glasgow RE, et al. Gastric cancer, version 2.2013: featured updates to the NCCN Guidelines. J Natl Compr Canc Netw. 2013;11:531–46.

    Article  CAS  Google Scholar 

  34. Koumarianou A, Krivan S, Machairas N, Ntavatzikos A, Pantazis N, Schizas D, Martikos G, Kampoli K, Misiakos EP, Patapis P, Liakakos T. Ten-year survival outcomes of patients with potentially resectable gastric cancer: impact of clinicopathologic and treatment-related risk factors. Ann Gastroenterol. 2019;32:99–106.

    PubMed  Google Scholar 

  35. Ito H, Clancy TE, Osteen RT, Swanson RS, Bueno R, Sugarbaker DJ, Ashley SW, Zinner MJ, Whang EE. Adenocarcinoma of the gastric cardia: what is the optimal surgical approach? J Am Coll Surg. 2004;199:880–6.

    Article  Google Scholar 

  36. Harada K, Lopez A, Shanbhag N, Badgwell B, Baba H, Ajani J. Recent advances in the management of gastric adenocarcinoma patients. F1000Res. 2018;7. https://doi.org/10.12688/f1000research.15133.1

    Article  Google Scholar 

  37. Noh SH, Park SR, Yang HK, Chung HC, Chung IJ, Kim SW, Kim HH, Choi JH, Kim HK, Yu W, et al. 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. 2014;15:1389–96.

    Article  CAS  Google Scholar 

  38. Paoletti X, Oba K, Burzykowski T, Michiels S, Ohashi Y, Pignon JP, Rougier P, Sakamoto J, Sargent D, Sasako M, et al. Benefit of adjuvant chemotherapy for resectable gastric cancer: a meta-analysis. JAMA. 2010;303:1729–37.

    Article  CAS  Google Scholar 

  39. Kashihara H, Shimada M, Yoshikawa K, Higashijima J, Tokunaga T, Nishi M, Takasu C. Risk factors for recurrence of gastric cancer after curative laparoscopic gastrectomy. J Med Invest. 2017;64:79–84.

    Article  Google Scholar 

  40. Wang Y, Zhao X, Song Y, Cai A, Xi H, Chen L. A systematic review and meta-analysis of robot-assisted versus laparoscopically assisted gastrectomy for gastric cancer. Medicine (Baltimore). 2017;96:e8797.

    Article  Google Scholar 

  41. Ojima T, Nakamura M, Nakamori M, Hayata K, Katsuda M, Kitadani J, Maruoka S, Shimokawa T, Yamaue H. Robotic versus laparoscopic gastrectomy with lymph node dissection for gastric cancer: study protocol for a randomized controlled trial. Trials. 2018;19:409.

    Article  Google Scholar 

Download references

Acknowledgements

Thank you to the authors of the included studies and thank you to American Journal Experts for language editing. Guixiang Liao declares his thanks to his parents (Zehai Liao and Meiying Chen) for their support of his career.

Funding

The following funds were in support of this study: the Natural Science Foundation of Shenzhen (No. JCYJ20170307095828424), Shenzhen Health and Family Planning System Research Project (No. SZBC2017024), and the technical research and cultivation project for the youth of Shenzhen People’s Hospital (No. SYKYPY2019029).

Author information

Author notes

  1. Guixiang Liao, Zhihong Zhao, and Muhammad Khan contributed equally.

Authors and Affiliations

  1. Department of Radiation Oncology, Shenzhen People’s Hospital, Second Clinical Medicine Centre, Jinan University, Shenzhen, 518020, People’s Republic of China

    Guixiang Liao & Xianming Li

  2. Department of Nephrology, Shenzhen People’s Hospital, Second Clinical Medicine Centre, Jinan University, Shenzhen, People’s Republic of China

    Zhihong Zhao

  3. Department of Oncology, First Affiliated Hospital of Anhui Medical University, Hefei, People’s Republic of China

    Muhammad Khan

  4. Department of Radiation Oncology, Cancer Center of Guangzhou Medical University, Guangzhou, Guangdong, People’s Republic of China

    Yawei Yuan

Authors
  1. Guixiang Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhihong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yawei Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xianming Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GL and MK wrote the manuscript. ZZ performed the data search and data analysis. All authors corrected and proofed the final text. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Guixiang Liao, Yawei Yuan or Xianming Li.

Ethics declarations

Ethics approval and consent to participate

The study did not need ethics approval

Consent for publication

Not available.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Additional file

Additional file 1:

Search strategies. (DOCX 15 kb)

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liao, G., Zhao, Z., Khan, M. et al. Comparative analysis of robotic gastrectomy and laparoscopic gastrectomy for gastric cancer in terms of their long-term oncological outcomes: a meta-analysis of 3410 gastric cancer patients. World J Surg Onc 17, 86 (2019). https://doi.org/10.1186/s12957-019-1628-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12957-019-1628-2

Keywords

World Journal of Surgical Oncology

ISSN: 1477-7819

Contact us