Home About us Editorial board Ahead of print Current issue Search Archives Submit article Instructions Subscribe Contacts Login 

 Table of Contents  
REVIEW ARTICLE
Year : 2019  |  Volume : 15  |  Issue : 7  |  Page : 1450-1463

Effectiveness and safety of robotic versus traditional laparoscopic gastrectomy for gastric cancer: An updated systematic review and meta-analysis


1 Department of General Surgery, The First Affiliated Hospital of Nanchang University; Jiangxi Medical College, Nanchang University, Nanchang, Jiangxi Province, China
2 Department of General Surgery, The First Affiliated Hospital of Nanchang University, Nanchang, Jiangxi Province, China
3 Department of Anesthesiology, Jiangxi Cancer Hospital, The Second People's Hospital of Jiangxi Province, Nanchang, Jiangxi Province, China

Date of Submission23-Nov-2018
Date of Decision12-Jun-2019
Date of Acceptance30-Oct-2019
Date of Web Publication13-Jan-2020

Correspondence Address:
Dr. Ren-Feng Shan
Department of General Surgery, The First Affiliated Hospital of Nanchang University, No. 17 Yongwai Zheng Street, Nanchang 330000, Jiangxi Province
China
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_798_18

Rights and Permissions
 > Abstract 


Gastrectomy is considered the gold standard treatment for gastric cancer patients. Currently, there are two minimally invasive surgical methods to choose from, robotic gastrectomy (RG) and laparoscopic gastrectomy (LG). Nevertheless, it is still unclear which is superior between the two. This meta-analysis aimed to investigate the effectiveness and safety of RG and LG for gastric cancer. A systematic literature search was performed using PubMed, Embase, and the Cochrane Library databases until September 2018 in studies that compared RG and LG in gastric cancer patients. Operative and postoperative outcomes analyzed were assessed. The quality of the evidence was rated using the Grading of Recommendations, Assessment, Development and Evaluations. Twenty-four English studies were analyzed. The meta-analysis revealed that the RG group had a significantly longer operation time, lower intraoperative blood loss, and higher perioperative costs compared to the LG group. However, there were no differences in complications, conversion rate, reoperation rate, mortality, number of lymph nodes harvested, days of first flatus, postoperative hospitalization time, and survival rate between the two groups. RG was shown to be associated with decreased intraoperative blood loss and increased perioperative cost and operation time compared to LG. Several higher-quality original studies and prospective clinical trials are required to confirm the advantages of RG.

Keywords: Gastric cancer, laparoscopic gastrectomy, meta-analysis, robot gastrectomy


How to cite this article:
Qiu H, Ai JH, Shi J, Shan RF, Yu DJ. Effectiveness and safety of robotic versus traditional laparoscopic gastrectomy for gastric cancer: An updated systematic review and meta-analysis. J Can Res Ther 2019;15:1450-63

How to cite this URL:
Qiu H, Ai JH, Shi J, Shan RF, Yu DJ. Effectiveness and safety of robotic versus traditional laparoscopic gastrectomy for gastric cancer: An updated systematic review and meta-analysis. J Can Res Ther [serial online] 2019 [cited 2020 Jul 13];15:1450-63. Available from: http://www.cancerjournal.net/text.asp?2019/15/7/1450/275568




 > Introduction Top


According to Bray et al.,[1] gastric cancer is the third most common cause of cancer-related death worldwide, and there were over 1,000,000 new cases and an estimated 783,000 deaths attributed to gastric cancer in 2018. Currently, gastrectomy with lymph node dissection is the gold standard treatment for gastric cancer.[2] Since minimally invasive gastrectomy was performed in the 1990s, laparoscopic gastrectomy (LG) has been widely accepted as a treatment for gastric cancer.[3] Compared to open surgical procedures, LG has been associated with better cosmetic results, less estimated blood loss, reduced pain, faster recovery, and favorable oncological outcomes.[4] However, LG still has several disadvantages, including its two-dimensional (2D) visualization, patient's restricted dexterity of movement, amplification of hand tremors, and inconvenient surgical field exposure, bringing challenges to lymph node dissection. Moreover, the technical complexities and substantial learning curves of LG restrict its wide adaptation in surgery in clinical practice.[5],[6]

Since the US Food and Drug Administration granted permission, robotic procedures have been performed in many fields of surgery, and robotic gastrectomy (RG) was first reported in 2003.[7] Being another minimally invasive surgery procedure, the robotic surgery system offers several advantages, such as its 3D high-definition visualization, seven degrees of wrist-like motion, high-definition view of the operative field, and less fatigue, thus assisting the surgeons in overcoming the technical difficulties and limitations encountered when performing traditional laparoscopic surgery.[8] Moreover, the learning curve, which is associated with surgeons gaining familiarity and proficiency, in RG is shorter than that in LG.[9]

Although several studies have revealed that RG was associated with less intraoperative blood loss and shorter postoperative length of stay than LG,[10],[11] the real superiority of RG versus LG in the treatment of gastric cancer remains controversial. Hence, we performed this review and meta-analysis to compare the feasibility and efficacy between RG and LG in treating gastric cancer. Moreover, the Grading of Recommendations Assessment, Development and Evaluation (GRADE) system was used to evaluate the outcomes of this meta-analysis.


 > Materials and Methods Top


Literature search

A systematic review was performed using PubMed, Embase, and the Cochrane Library databases until September 2018 in all studies that compared RG and LG in treating gastric cancer. The search terms included “gastric carcinoma,” “gastric cancer,” “gastrectomy,” “gastric resection,” “robotic,” and “minimally invasive.” The search was limited to studies published in English. References of the acquired articles were also carried out to identify additional studies.

Study selection

Two investigators (Hua Qiu and Dongjun Yu) reviewed all the records found and subsequently browsed the titles and abstracts independently. The studies that satisfied the following criteria were included in this meta-analysis: (1) comparative studies comparing the outcomes of RG and LG in the treatment of gastric cancer and (2) full-text articles containing at least one of the outcomes that we were interested in. The following studies were excluded: (1) noncomparative studies such as reviews, conference reports, letters, and case reports; (2) studies including nongastric cancer patients; (3) studies that lacked sufficient data for statistical analysis; and (4) duplicate studies.

Data extraction and quality assessment

Two reviewers (Hua Qiu and Dongjun Yu) independently extracted the following data: author, region, years of publication, study design, characteristics of the study population, operative time, intraoperative blood loss, conversion rate, the number of lymph nodes harvested, proximal and distal margin distances, the days of first flatus, postoperative length of hospital stay, postoperative complications, mortality, perioperative cost, and survival rates. Disagreements were resolved through discussion. The Newcastle–Ottawa scale [12] was used to assess the quality of nonrandomized studies. The evaluation system contains the following three factors: patient selection, comparability between the groups, and assessment of outcome. The score ranges from 0 to 9, and studies with a score equal to or higher than 6 were deemed qualified.

Subgroups analysis

The resection type, body mass index (BMI), age, and depth of invasion are factors considered to affect the surgical outcomes as reported in several studies.[13],[14],[15] To eliminate bias, we performed several subgroup analyses to analyze the impact of the resection type, BMI, age, and depth of invasion.

Statistical analysis

Review Manager version 5.3 (Cochrane Collaboration, Oxford, England) software was used to perform this meta-analysis. The differences between continuous variables and dichotomous variables were evaluated using the weighted mean difference (WMD) and odds ratios (ORs) with the 95% confidence interval (95% CI), respectively. Moreover, the standard mean difference (SMD) with the 95% CI was performed when the unit was different. When the studies only offered the medians, we calculated the means and standard deviations and range according to the method described by Hozo et al.[16] The heterogeneity was quantified using the I2 statistic.

Level of evidence

We rated the quality of the evidence using the GRADE, and the evidence profile was created using the GRADE profiler 3.6 software (The GRADE Working Group). There was quality degradation when the following considerations existed: the risks of biases, inconsistency, indirectness, imprecision, and publication biases. We evaluated the evidence qualities of the following outcomes: operative time, intraoperative blood loss, conversion rate, number of lymph nodes harvested, the days of first flatus, postoperative complications, postoperative length of hospital stay, and mortality.


 > Results Top


Search results and study characteristics

The process of reference selection is illustrated in [Figure 1]. A total of 516 potentially relevant studies were initially found in the literature review. Subsequently, 354 studies were eliminated as they were duplicates. After examining the titles and abstracts, we excluded 24 articles because of the following reasons: non-English, reviews, conference reports, letters, case reports, protocols, and studies including nongastric cancer patients. We excluded 14 studies that were based on overlapping patient cohorts after carefully browsing the full text. Finally, a total of 24 nonrandomized studies [17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40] were eligible for this meta-analysis, with 2741 patients undergoing RG and 5672 patients undergoing LG. The study characteristics and methodological quality assessment of the 24 studies are shown in [Table 1].
Figure 1: Flow diagram for identification of selected articles

Click here to view
Table 1: Characteristics and quality score of studies included in the meta-analysis

Click here to view


Operative time

The operative time was examined in all 24 studies. The pooled analysis including 8413 patients revealed that RG required a longer operative time compared to LG (WMD, 44.11; 95% CI, 24.20–64.01; P < 0.0001), with high heterogeneity among the studies (I2 = 99%) [Figure 2].
Figure 2: Forest plot and meta-analysis of the operation time

Click here to view


Intraoperative blood loss

The intraoperative blood loss was presented in 23 studies. The pooled analysis including 8225 patients revealed that the intraoperative blood loss was significantly lower for RG compared to LG (WMD, −17.78; 95% CI, −25.62–−9.94; P < 0.00001), with high heterogeneity among the studies (I2 = 89%) [Figure 3].
Figure 3: Forest plot and meta-analysis of the intraoperative blood loss

Click here to view


Days of first flatus

The days of first flatus was mentioned in 13 studies. The pooled analysis including 4127 patients revealed that there was no statistically significant difference between the two procedures (WMD, −0.20; 95% CI, −0.53–−0.14; P = 0.25), with high heterogeneity among the studies (I2 = 98%, P < 0.00001) [Figure 4].
Figure 4: Forest plot and meta-analysis of the days of first flatus

Click here to view


Conversion rate

The conversion rate was recorded in six studies. The pooled analysis including 2876 patients revealed that there was no statistically significant difference between the two procedures (OR, 1.34; 95% CI, 0.59–3.01; P = 0.49), with no observed heterogeneity among the studies (I2 = 0%, P = 0.92) [Figure 5].
Figure 5: Forest plot and meta-analysis of the conversion rate

Click here to view


Postoperative complication

The overall morbidity was mentioned in 23 studies. The pooled analysis including 8293 patients revealed that there was no statistically significant difference between the two procedures (OR, 0.88; 95% CI, 0.75–1.02; P = 0.09), with low heterogeneity among the studies (I2 = 13%) [Figure 6]. No significant differences in the rate of delayed gastric emptying (OR, 1.30; 95% CI, 0.61–2.80; P = 0.50; I2 = 0%), intestinal obstruction (OR, 1.26; 95% CI, 0.65–2.44; P = 0.49; I2 = 0%), intra-abdominal infection (OR, 0.95; 95% CI, 0.55–1.63; P = 0.85; I2 = 0%), wound infection (OR, 1.20; 95% CI, 0.76–1.87; P = 0.43; I2 = 0%), anastomotic leakage (OR, 0.88; 95% CI, 0.57–1.37; P = 0.58; I2 = 0%), and pancreas-related complications (OR, 0.52; 95% CI, 0.20–1.35; P = 0.18; I2 = 0%) were identified between the two procedures [Table 2].
Figure 6: Forest plot and meta-analysis of the overall morbidity

Click here to view
Table 2: Systematic review of postoperative complication

Click here to view


Mortality

The mortality was presented in four studies. The pooled analysis including 1345 patients revealed that there was no statistically significant difference between the two procedures (OR, 1.34; 95% CI, 0.36–4.96; P = 0.66), with no observed heterogeneity among the studies (I2 = 0%) [Figure 7].
Figure 7: Forest plot and meta-analysis of the mortality

Click here to view


Number of lymph nodes harvested

The number of lymph nodes harvested was presented in 21 studies. The pooled analysis including 7005 patients revealed that RG was associated with a significant increase in the number of lymph nodes harvested compared to LG (WMD, 1.92; 95% CI, 0.34–3.5; P = 0.02), with high heterogeneity among the studies (I2 = 86%) [Figure 8].
Figure 8: Forest plot and meta-analysis of the No. of lymph nodes harvested

Click here to view


Postoperative hospitalization time

The postoperative length of hospital stay was presented in 23 studies. The pooled analysis revealed that there was no statistically significant difference between the two procedures (WMD, −0.36, 95% CI, −0.88–−0.16; P = 0.18), with high heterogeneity among the studies (I2 = 87%, P < 0.00001) [Figure 9].
Figure 9: Forest plot and meta-analysis of the postoperative length of hospital stay

Click here to view


Perioperative costs

The perioperative costs were recorded in five studies. The pooled analysis revealed that the RG group was associated with higher perioperative costs compared to the LG group (SMD, 2.06; 95% CI, 1.05–3.06; P < 0.0001), with high heterogeneity among the studies (I2 = 98%) [Figure 10].
Figure 10: Forest plot and meta-analysis of the perioperative costs

Click here to view


Survival rate

The 3-year overall survival (OS) rate only presented in four studies. The pooled analysis revealed that the 3-year OS rate was comparable between the two procedures (OR, 1.12; 95% CI, 0.81–1.54; P = 0.50), with no observed heterogeneity among the studies (I2 = 0%) [Figure 11]. The 5-year OS rate was recorded in three studies. The pooled analysis indicated that the 5-year OS rate was comparable between the two procedures (OR, 0.54; 95% CI, 0.22–1.33; P = 0.18), with high heterogeneity among the studies (I2 = 79%, P = 0.008) [Figure 12]. The 5-year disease-free survival (DFS) rate was mentioned in two studies. The pooled analysis indicated that the 5-year DFS rate was comparable between the two procedures (OR, 0.79; 95% CI, 0.47–1.33; P = 0.38), with no observed heterogeneity among the studies (I2 = 0%) [Figure 13].
Figure 11: Forest plot and meta-analysis of the 3-year overall survival rate

Click here to view
Figure 12: Forest plot and meta-analysis of the 5-year overall survival rate

Click here to view
Figure 13: Forest plot and meta-analysis of the 5-year disease-free survival rate

Click here to view


Subgroup analysis of resection type

Considering distal gastrectomy, the meta-analysis revealed significantly lower operation time and low intraoperative blood loss in the RG group compared to the LG group, while the days of first flatus, overall complications, postoperative hospitalization time, and the number of lymph nodes harvested were comparable between the two procedures. As for total gastrectomy, the meta-analysis revealed that the operation time, intraoperative blood loss, days of first flatus, overall complications, postoperative hospitalization time, and number of lymph nodes harvested were comparable between the two procedures. The results of the subgroup analysis on resection type are shown in [Table 3].
Table 3: Results of the subgroup analysis of resection type

Click here to view


Subgroup analysis of body mass index

Considering BMI <25, the meta-analysis revealed significantly longer operation time and increased number of lymph nodes harvested in the RG group compared to the LG group, while intraoperative blood loss, overall complications, and postoperative hospitalization time were comparable between the two procedures. As for BMI ≥25, the meta-analysis revealed significantly longer operation time in the RG compared to the LG group, while intraoperative blood loss, overall complications, postoperative hospitalization time, and number of lymph nodes harvested were comparable between the two procedures. The results of the subgroup analysis on BMI are shown in [Table 4].
Table 4: Results of the subgroup analysis of body mass index

Click here to view


Subgroup analysis of age

Considering age <65, the meta-analysis revealed that the operation time, intraoperative blood loss, postoperative hospitalization time, and number of lymph nodes harvested were comparable between the two procedures. As for age ≥ 65, the meta-analysis revealed significantly longer operation time and low intraoperative blood loss in the RG group compared to the LG group, while postoperative hospitalization time and number of lymph nodes harvested were comparable between the two procedures. The results of the subgroup analysis on age are shown in [Table 5].
Table 5: Results of the subgroup analysis of age

Click here to view


Subgroup analysis of depth of invasion

Considering early gastric cancer, the meta-analysis revealed that the operation time was significantly longer in the RG group compared to the LG group, while intraoperative blood loss, overall complications, and postoperative hospitalization time were comparable between the two procedures. As for advanced gastric cancer, the meta-analysis revealed significantly longer operation time and low intraoperative blood loss in the RG group compared to the LG group, while the overall complications and postoperative hospitalization time were comparable between the two procedures. As for nonserosal invasion, the meta-analysis revealed significantly longer operation time and low intraoperative blood loss in the RG group compared to the LG group, while the overall complications, postoperative hospitalization time, and number of lymph nodes harvested were comparable between the two procedures. As for serosal invasion, the meta-analysis revealed significantly longer operation time, significantly increased number of lymph nodes harvested, and significantly low intraoperative blood loss in the RG group compared to the LG group, while the overall complications and postoperative hospitalization time were comparable between the two procedures. The results of the subgroup analysis on the depth invasion are shown in [Table 6].
Table 6: Results of the subgroup analysis of depth of invasion

Click here to view



 > Discussion Top


Gastrectomy with extensive lymphadenectomy is considered the gold standard in the treatment of gastric cancer. Nevertheless, different surgical strategies could influence the intraoperative and postoperative outcomes and directly affect the quality of life of the patients. With the rapid development of techniques and the increasing interest in minimally invasive surgery, LG has become increasingly used, which has been associated with a better short-term outcome and an equal long-term efficacy compared with conventional open gastrectomy.[41] With the development of robotic surgery, RG was gradually developed as an alternative minimally invasive surgery for the treatment of gastric cancer. However, the clinically significant benefits of robotic application on intraoperative effects, postoperative outcomes, and oncological outcomes of gastric cancer patients are yet to be sufficiently determined. The meta-analysis revealed that the complications, conversion rate, reoperation rate, morality, days of first flatus, postoperative hospitalization time, 3-year survival rate, and 5-year survival rate were comparable between the two procedures, which were similar to other recent studies.[42],[43] However, intraoperative blood loss decreased, and perioperative cost, operation time, and number of lymph nodes harvested were increased in the RG group.

Intraoperative blood loss is one of most important indices that surgeons are concerned about during surgery. Theoretically, robotic surgery is a more precise technique that could potentially reduce blood loss. With regard to intraoperative blood loss, this meta-analysis revealed significantly decreased intraoperative blood loss in the RG group compared to the LG group, which might be attributed to the robotic procedure being more stable on the surgeon's hands, hence drastically decreasing musculoskeletal fatigue and physiologic tremor over time in the surgeons. In addition, the robotic device provides augmented flexibility in a confined narrow operative space, and the 3D high-definition field of view allows surgeons to effectively minimize the risk of tissue and blood vessel injuries, which may be related to decreased intraoperative blood loss.

As for the operative time, RG takes longer than LG. The following are the reasons why longer operation time is associated with RG. First, the robotic procedure is an innovative technology, hence requiring an ample amount of time to adapt to it. This meta-analysis represents some studies on the surgeons' primary experiences with RG and some surgeons who were likely still in the learning phase. As reported, the operation time for RG stabilizes after at least finishing 15 cases and subsequently decreases gradually, and surgeons who have experience performing LG can perform RG successfully even in their first surgery and reach a plateau in operation time after 20 cases.[9],[19],[44],[45] Moreover, the learning curve for RG was a critical factor, which might exert an additional influence on this indicator. As surgeons become more skillful in performing robotic procedures, the operative time for RG might decrease. Second, in the RG group, the facility is more sophisticated and requires additional setup and docking time before the operations.[46] The setup procedure often takes half an hour to complete. Lu et al.[39] stated that the total operation time and purely operation time (subtracting time required for docking and undocking) are both longer than laparoscopic surgical system. Unfortunately, most of the included studies in this review and meta-analysis did not elaborate on whether the preparation times for devices included the operation times; thus, data that allowed us to perform a further analysis were insufficient. Third, because of the insufficient tactile feedback, the surgeons can only evaluate the applied force on the tissue, which depends on the analyzed visual information during the operation, which may lengthen the operation time. However, the prolonged operation time was not associated to any increase in open conversions, postoperative complications, or mortality.

The postoperative morbidity and mortality were important indicators in estimating the operational safety and feasibility. In this meta-analysis, the overall morbidity was comparable between the two procedures. The risk of complications is associated with conversion rate and intraoperative blood loss.[47],[48] In this meta-analysis, conversion rate and the intraoperative blood loss were comparable between the two groups. Thus, it is understandable that there was similar incidence of complications between the two groups. Anastomotic leakage is an important abdominal complication that leads to an increase in mortality after gastrectomy. In this meta-analysis, the anastomotic leakage rate in the RG group equally matched to those of the LG group. Hitherto, there is also no obvious evidence supporting the idea that the surgical procedures might affect the anastomotic leakage rate after gastrectomy. Moreover, obesity with heavy mesentery is associated with a higher incidence of intraoperative and postoperative surgical complications.[49],[50] The subgroup analysis of BMI mainly revealed similar result. In addition, the mortality in the RG group is equal to LG group. Thus, it is convictively accepted that both RG and LG are considered safe treatments in gastric cancer patients.

Adequate lymphadenectomy is important for long-term oncological outcomes. According to Son et al.,[25] the number of retrieved lymph nodes during extraperigastric lymphadenectomy, especially in the case of splenic pedicle and splenic hilum and in the suprapancreatic areas, was significantly higher for the robotic group compared to the laparoscopy group (15.9 vs. 12.2, P = 0.02). According to another included study, RG is accompanied by a significantly high number of lymph nodes harvested in total (37.1 ± 12.9 vs. 34.1 ± 12.1, P = 0.04) and particularly at the extraperigastric stations (16.3 ± 7.7 vs. 3.2 ± 5.3, P = 0.001).[51] The meta-analysis revealed that the number of lymph nodes harvested was statistically different between the RG group and the LG group. However, the subgroup analysis of resection type and depth of invasion revealed that the number of lymph nodes harvested was comparable between the two procedures. Therefore, case-matching studies on the type of gastrectomy and extent of lymphadenectomy that are closely associated between RG and LG should be analyzed in the future.

The main disadvantage of RG is that it is costly. The high price of robotic surgery could be attributed to initial purchasing costs, disposable consumables costs, and maintenance costs. A high therapy cost will affect the preferences of the majority of patients. In this meta-analysis, the hospitalization costs of RG were significantly higher compared to LG. However, when this disadvantage may be overcome, the robotic approach will be more widely used.

We estimated the quality of the evidence using the GRADE approach, and the results are shown in [Figure 14]. The quality of the evidence was considered only low (intraoperative blood loss, operation time, number of lymph nodes harvested, days of first flatus, morality, overall morbidity, and postoperative hospitalization time) and very low (reoperation and conversion rate) attribute to the limited evidence derived from nonrandomized controlled trials (RCTs), and another reason was the existence of publication bias. It is difficult for us to hypothesize that the association depends on the existing researches; hence, further RCTs are needed to measure the significant differences between intraoperative and postoperative outcomes.
Figure 14: Grading of Recommendations Assessment, Development and Evaluation profile evidence of the included studies

Click here to view


The following limitations of this meta-analysis should be considered: (1) most of the information were derived from retrospective nonrandomized comparisons, a key limitation that may have introduced a certain bias in the study; (2) it is difficult to eliminate the heterogeneity in patient characteristics and the skills and experience of the surgeons between the RG and LG groups; (3) the inclusion of different gastrectomy types and the extent of lymphadenectomy also have possibly introduced bias; and (4) a publication bias and lack of long-term follow-up data are some of the other notable limitations of our study. With all of these limitations, further multicenter, prospective RCTs should be performed to identify the potential advantages and disadvantages of RG.


 > Conclusions Top


This meta-analysis revealed that RG was associated with decreased intraoperative blood loss, increased perioperative cost and operation time, and number of lymph nodes harvested compared to LG. The effectiveness and safety of RG is similar to LG. Based on the GRADE system, the quality of the evidence of the investigation is low; hence, more high-quality studies, large samples, multiple centers, and long-term follow-up RCTs are needed to provide strong evidence to confirm the advantages of RG.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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.  Back to cited text no. 1
    
2.
Ju Y, Sun S, Jiao S. Prolonged overall survival in metastatic gastric cancer treated with ipilimumab and lapatinib. J Cancer Res Ther 2018;14:1589-93.  Back to cited text no. 2
    
3.
Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 1994;4:146-8.  Back to cited text no. 3
    
4.
Bamboat ZM, Strong VE. Minimally invasive surgery for gastric cancer. J Surg Oncol 2013;107:271-6.  Back to cited text no. 4
    
5.
Zhou D, Quan Z, Wang J, Zhao M, Yang Y. Laparoscopic-assisted versus open distal gastrectomy with D2 lymph node resection for advanced gastric cancer: Effect of learning curve on short-term outcomes. A meta-analysis. J Laparoendosc Adv Surg Tech A 2014;24:139-50.  Back to cited text no. 5
    
6.
Moon JS, Park MS, Kim JH, Jang YJ, Park SS, Mok YJ, et al. Lessons learned from a comparative analysis of surgical outcomes of and learning curves for laparoscopy-assisted distal gastrectomy. J Gastric Cancer 2015;15:29-38.  Back to cited text no. 6
    
7.
Hashizume M, Sugimachi K. Robot-assisted gastric surgery. Surg Clin North Am 2003;83:1429-44.  Back to cited text no. 7
    
8.
Gutt CN, Oniu T, Mehrabi A, Kashfi A, Schemmer P, Büchler MW. Robot-assisted abdominal surgery. Br J Surg 2004;91:1390-7.  Back to cited text no. 8
    
9.
Kim HI, Park MS, Song KJ, Woo Y, Hyung WJ. Rapid and safe learning of robotic gastrectomy for gastric cancer: Multidimensional analysis in a comparison with laparoscopic gastrectomy. Eur J Surg Oncol 2014;40:1346-54.  Back to cited text no. 9
    
10.
Marano A, Choi YY, Hyung WJ, Kim YM, Kim J, Noh SH. Robotic versus laparoscopic versus open gastrectomy: A meta-analysis. J Gastric Cancer 2013;13:136-48.  Back to cited text no. 10
    
11.
Zong L, Seto Y, Aikou S, Takahashi T. Efficacy evaluation of subtotal and total gastrectomies in robotic surgery for gastric cancer compared with that in open and laparoscopic resections: A meta-analysis. PLoS One 2014;9:e103312.  Back to cited text no. 11
    
12.
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010;25:603-5.  Back to cited text no. 12
    
13.
Lee JH, Park DJ, Kim HH, Lee HJ, Yang HK. Comparison of complications after laparoscopy-assisted distal gastrectomy and open distal gastrectomy for gastric cancer using the clavien-dindo classification. Surg Endosc 2012;26:1287-95.  Back to cited text no. 13
    
14.
Lee KG, Lee HJ, Yang JY, Oh SY, Bard S, Suh YS, et al. Risk factors associated with complication following gastrectomy for gastric cancer: Retrospective analysis of prospectively collected data based on the Clavien-Dindo system. J Gastrointest Surg 2014;18:1269-77.  Back to cited text no. 14
    
15.
Kim DJ, Lee JH, Kim W. Comparison of the major postoperative complications between laparoscopic distal and total gastrectomies for gastric cancer using clavien-dindo classification. Surg Endosc 2015;29:3196-204.  Back to cited text no. 15
    
16.
Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13.  Back to cited text no. 16
    
17.
Kim MC, Heo GU, Jung GJ. Robotic gastrectomy for gastric cancer: Surgical techniques and clinical merits. Surg Endosc 2010;24:610-5.  Back to cited text no. 17
    
18.
Pugliese R, Maggioni D, Sansonna F, Costanzi A, Ferrari GC, Di Lernia S, et al. 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.  Back to cited text no. 18
    
19.
Kang BH, Xuan Y, Hur H, Ahn CW, Cho YK, Han SU. Comparison of surgical outcomes between robotic and laparoscopic gastrectomy for gastric cancer: The learning curve of robotic surgery. J Gastric Cancer 2012;12:156-63.  Back to cited text no. 19
    
20.
Kim KM, An JY, Kim HI, Cheong JH, Hyung WJ, Noh SH. Major early complications following open, laparoscopic and robotic gastrectomy. Br J Surg 2012;99:1681-7.  Back to cited text no. 20
    
21.
Hyun MH, Lee CH, Kwon YJ, Cho SI, Jang YJ, Kim DH, et al. Robot versus laparoscopic gastrectomy for cancer by an experienced surgeon: Comparisons of surgery, complications, and surgical stress. Ann Surg Oncol 2013;20:1258-65.  Back to cited text no. 21
    
22.
Huang KH, Lan YT, Fang WL, Chen JH, Lo SS, Li AF, et al. Comparison of the operative outcomes and learning curves between laparoscopic and robotic gastrectomy for gastric cancer. PLoS One 2014;9:e111499.  Back to cited text no. 22
    
23.
Junfeng Z, Yan S, Bo T, Yingxue H, Dongzhu Z, Yongliang Z, et al. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: Comparison of surgical performance and short-term outcomes. Surg Endosc 2014;28:1779-87.  Back to cited text no. 23
    
24.
Noshiro H, Ikeda O, Urata M. Robotically-enhanced surgical anatomy enables surgeons to perform distal gastrectomy for gastric cancer using electric cautery devices alone. Surg Endosc 2014;28:1180-7.  Back to cited text no. 24
    
25.
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.  Back to cited text no. 25
    
26.
Han DS, Suh YS, Ahn HS, Kong SH, Lee HJ, Kim WH, et al. Comparison of surgical outcomes of robot-assisted and laparoscopy-assisted pylorus-preserving gastrectomy for gastric cancer: A propensity score matching analysis. Ann Surg Oncol 2015;22:2323-8.  Back to cited text no. 26
    
27.
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.  Back to cited text no. 27
    
28.
Park JY, Ryu KW, Reim D, Eom BW, Yoon HM, Rho JY, et al. Robot-assisted gastrectomy for early gastric cancer: Is it beneficial in viscerally obese patients compared to laparoscopic gastrectomy? World J Surg 2015;39:1789-97.  Back to cited text no. 28
    
29.
Suda K, Man-I M, Ishida Y, Kawamura Y, Satoh S, Uyama I. Potential advantages of robotic radical gastrectomy for gastric adenocarcinoma in comparison with conventional laparoscopic approach: A single institutional retrospective comparative cohort study. Surg Endosc 2015;29:673-85.  Back to cited text no. 29
    
30.
Cianchi F, Indennitate G, Trallori G, Ortolani M, Paoli B, Macrì G, et al. Robotic vs. laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: A retrospective comparative mono-institutional study. BMC Surg 2016;16:65.  Back to cited text no. 30
    
31.
Kim HI, Han SU, Yang HK, Kim YW, Lee HJ, Ryu KW, et al. Multicenter prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg 2016;263:103-9.  Back to cited text no. 31
    
32.
Shen W, Xi H, Wei B, Cui J, Bian S, Zhang K, et al. Robotic versus laparoscopic gastrectomy for gastric cancer: Comparison of short-term surgical outcomes. Surg Endosc 2016;30:574-80.  Back to cited text no. 32
    
33.
Pan HF, Wang G, Liu J, Liu XX, Zhao K, Tang XF, et al. Robotic versus laparoscopic gastrectomy for locally advanced gastric cancer. Surg Laparosc Endosc Percutan Tech 2017;27:428-33.  Back to cited text no. 33
    
34.
Yang SY, Roh KH, Kim YN, Cho M, Lim SH, Son T, et al. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer. Ann Surg Oncol 2017;24:1770-7.  Back to cited text no. 34
    
35.
Li Z, Li J, Li B, Bai B, Liu Y, Lian B, et al. 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.  Back to cited text no. 35
    
36.
Gao Y, Xi H, Qiao Z, Li J, Zhang K, Xie T, et al. Comparison of robotic – And laparoscopic-assisted gastrectomy in advanced gastric cancer: Updated short – And long-term results. Surg Endosc 2019;33:528-34.  Back to cited text no. 36
    
37.
Hikage M, Tokunaga M, Makuuchi R, Irino T, Tanizawa Y, Bando E, et al. Comparison of surgical outcomes between robotic and laparoscopic distal gastrectomy for cT1 gastric cancer. World J Surg 2018;42:1803-10.  Back to cited text no. 37
    
38.
Liu HB, Wang WJ, Li HT, Han XP, Su L, Wei DW, et al. Robotic versus conventional laparoscopic gastrectomy for gastric cancer: A retrospective cohort study. Int J Surg 2018;55:15-23.  Back to cited text no. 38
    
39.
Lu J, Zheng HL, Li P, Xie JW, Wang JB, Lin JX, et al. A propensity score-matched comparison of robotic versus laparoscopic gastrectomy for gastric cancer: Oncological, cost, and surgical stress analysis. J Gastrointest Surg 2018;22:1152-62.  Back to cited text no. 39
    
40.
Obama K, Kim YM, Kang DR, Son T, Kim HI, Noh SH, et al. Long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer 2018;21:285-95.  Back to cited text no. 40
    
41.
Best LM, Mughal M, Gurusamy KS. Laparoscopic versus open gastrectomy for gastric cancer. Cochrane Database Syst Rev 2016;3:CD011389.  Back to cited text no. 41
    
42.
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.  Back to cited text no. 42
    
43.
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.  Back to cited text no. 43
    
44.
Eom BW, Yoon HM, Ryu KW, Lee JH, Cho SJ, Lee JY, 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.  Back to cited text no. 44
    
45.
Park SS, Kim MC, Park MS, Hyung WJ. Rapid adaptation of robotic gastrectomy for gastric cancer by experienced laparoscopic surgeons. Surg Endosc 2012;26:60-7.  Back to cited text no. 45
    
46.
Rencuzogullari A, Gorgun E. Robotic rectal surgery. J Surg Oncol 2015;112:326-31.  Back to cited text no. 46
    
47.
Rottoli M, Bona S, Rosati R, Elmore U, Bianchi PP, Spinelli A, et al. Laparoscopic rectal resection for cancer: Effects of conversion on short-term outcome and survival. Ann Surg Oncol 2009;16:1279-86.  Back to cited text no. 47
    
48.
Ishino Y, Saigusa S, Ohi M, Yasuda H, Tanaka K, Toiyama Y, et al. Preoperative C-reactive protein and operative blood loss predict poor prognosis in patients with gastric cancer after laparoscopy-assisted gastrectomy. Asian J Endosc Surg 2014;7:287-94.  Back to cited text no. 48
    
49.
Tsujinaka T, Sasako M, Yamamoto S, Sano T, Kurokawa Y, Nashimoto A, et al. Influence of overweight on surgical complications for gastric cancer: Results from a randomized control trial comparing D2 and extended para-aortic D3 lymphadenectomy (JCOG9501). Ann Surg Oncol 2007;14:355-61.  Back to cited text no. 49
    
50.
Bickenbach KA, Denton B, Gonen M, Brennan MF, Coit DG, Strong VE. Impact of obesity on perioperative complications and long-term survival of patients with gastric cancer. Ann Surg Oncol 2013;20:780-7.  Back to cited text no. 50
    
51.
Kim YW, Reim D, Park JY, Eom BW, Kook MC, Ryu KW, et al. Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer. Surg Endosc 2016;30:1547-52.  Back to cited text no. 51
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

Top
 
 
  Search
 
Similar in PUBMED
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  >Abstract>Introduction>Materials and Me...>Results>Discussion>Conclusions>Article Figures>Article Tables
  In this article
>References

 Article Access Statistics
    Viewed1624    
    Printed136    
    Emailed0    
    PDF Downloaded94    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]