Skip to content

Advertisement

  • Research article
  • Open Access
  • Open Peer Review

Robotic versus laparoscopic Gastrectomy for gastric cancer: a systematic review and updated meta-analysis

  • 1,
  • 1,
  • 1,
  • 2,
  • 1 and
  • 1Email author
BMC SurgeryBMC series – open, inclusive and trusted201717:93

https://doi.org/10.1186/s12893-017-0290-2

  • Received: 11 June 2017
  • Accepted: 17 August 2017
  • Published:
Open Peer Review reports

Abstract

Background

Advanced minimally invasive techniques including robotic surgery are being employed with increasing frequency around the world, primarily in order to improve the surgical outcomes of laparoscopic gastrectomy (LG). We conducted a systematic review and meta-analysis to evaluate the feasibility, safety and efficacy of robotic gastrectomy (RG).

Methods

Studies, which compared surgical outcomes between LG and RG, were retrieved from medical databases before May 2017. Outcomes of interest were estimated as weighted mean difference (WMD) or risk ratio (RR) using the random-effects model. The software Review Manage version 5.1 was used for all calculations.

Results

Nineteen comparative studies with 5953 patients were included in this analysis. Compared with LG, RG was associated with longer operation time (WMD = −49.05 min; 95% CI: -58.18 ~ −39.91, P < 0.01), less intraoperative blood loss (WMD = 24.38 ml; 95% CI: 12.32 ~ 36.43, P < 0.01), earlier time to oral intake (WMD = 0.23 days; 95% CI: 0.13 ~ 0.34, P < 0.01), and a higher expense (WMD = −3944.8 USD; 95% CI: -4943.5 ~ −2946.2, P < 0.01). There was no significant difference between RG and LG regarding time to flatus, hospitalization, morbidity, mortality, harvested lymph nodes, and cancer recurrence.

Conclusions

RG can be performed as safely as LG. However, it will take more effort to decrease operation time and expense.

Keywords

  • Laparoscopy
  • Robot
  • Gastrectomy
  • Stomach neoplasms
  • Morbidity
  • Meta-analysis

Background

Laparoscopic gastrectomy (LG) has been widely used for the treatment of gastric cancer and a number of other different minimally invasive procedures have been developed to date [1, 2]. There are several benefits for patients; including better cosmesis, reduced pain, early recovery of intestinal function, and shorter hospital stay, while maintaining comparable oncologic safety [14].

Robotic surgery was first put into practice in 2000, after being approved by the US Food and Drug Administration (FDA). It plays an essential role in ergonomics and offers advantages such as motion scaling, less fatigue, tremor filtering, seven degrees of wrist-like motion, and three-dimensional vision [5, 6]. Surgeons hoped that such innovative technology could overcome some limitations innate to traditional laparoscopic surgery. Thus, experienced laparoscopic surgeons are increasingly trying to develop new procedures that best exploit the capabilities of robotic surgery in the treatment of gastric cancer [7].

Nonetheless, the present status of robotic gastrectomy (RG) is, as of the writing of this paper, still restricted and this is in part to due to the lack of randomized controlled trials (RCTs). Several previous studies including meta-analyses have argued that RG can be a more effective and safer operation in comparison with conventional LG. In spite of these studies, many questions still need to be answered, most notably, RG’s efficacy with regard to oncologic, long-term survival outcomes and its cost-effectiveness. Moreover, a series of studies on RG for the treatments of gastric cancer have been recently published. These studies are meaningful in highlighting the status of RG in the treatment of gastric cancer. Therefore, this paper’s current research is intended to conduct a comprehensive systematic review of all the currently available literature and a meta-analysis of RG in comparison to LG in order to assess the feasibility, security and efficacy of RG.

Methods

Search strategy

A systematic search of Web of Science, Cochrane Library, Embase, and PubMed was conducted to find studies comparing RG and LG for gastric cancer treatment published up until May 2017. Search terms included “gastric carcinoma”, “gastric cancer”, “laparoscopic”, “robotic”, and “gastrectomy”. The links in search results and references were also reviewed to find the additional literature. Based on the language competencies of the reviewers, English and Chinese were the only languages of searched papers.

Eligibility criteria

The standards for research were comparative, using peer-reviewed studies of RG versus LG in gastric cancer for which the full texts were available. The most recent study or the study with the most subjects was chosen if overlapping research studies were found. Articles including any of the following were excluded: (1) Non-comparative studies such as letters, reviews, comments, posters, protocols, et al. (2) Studies including non-gastric carcinoma cases such as gastrointestinal stromal tumors, or benign gastric diseases; (3) Studies in which less than 2 of the interesting indices were reported.

Data extraction and quality assessment

Two reviewers (Chen K and Pan Y) reviewed the publications thoroughly and independently. Data extracted included the following items: author, region, operation time, intraoperative estimated blood loss (EBL), time to flatus, time to oral intake, length of hospital stay (LOS), morbidity, mortality, costs, retrieved lymph nodes (RLN), proximal and distal margin distance, and long-term oncologic outcomes. In accordance with the morbidity reporting system of Memorial Sloan-Kettering Cancer Center [8], postoperative complications were categorized into medical complications (respiratory, cardiovascular, metabolic events, deep venous thrombosis, phlebitis, et al.) or surgical complications (bleeding, any complication required reoperation, anastomotic leakage or stricture, delayed gastric emptying, et al.). The means and standard deviations (SDs) were estimated as described by Hozo et al. [9] if the research offered medians and ranges. The choice of the articles included in this review adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement (PRISMA). The Newcastle-Ottawa Quality Assessment Scale (NOS) was utilized to evaluate the research quality (http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp). The scale ranges from 0 to 9 stars: research with a score higher than or equal to 6 could be deemed as methodologically sound.

Subgroup analysis

The uneven distribution of the surgical extension between the groups could affect the outcomes. Therefore, to eliminate the bias, a subgroup analysis of total or distal gastrectomy was conducted. It has been reported that robotic surgery may benefit obese patients, because of improved visualization, instrumentation, and ergonomics [10]. Therefore, we conducted a subgroup analysis to analyze the impact of operation-related factors on body mass index (BMI).

Statistical analysis

The risk ratio (RR) was utilized to analyze the dichotomous variables and the weighted mean difference (WMD) was utilized to assess the continuous variables. Based on DerSimonian and Laird’s approach, the random-effects model was utilized to account for clinical heterogeneity, which refers to diversity in a sense that is relevant for clinical situations. According to the overall complication, the potential publication bias was determined by carrying out an informal visual inspection of funnel plots. The software of Review Manager version 5.1 (RevMan 5.1) was used to conduct data analysis. P < 0.05 was considered statistically significant.

Results

Studies selected

A total of 378 potential articles, which were published from 1996 to 2017, were found. 37 articles were chosen based on the titles and abstracts, and then a thorough check of each text was conducted. Seven of them failed to meet our standards and were excluded. A further eleven papers were excluded due to overlapping patient cohorts (one from Hospital Niguarda Ca Granda, Italy [11]; one from Fujita Health University, Japan [12]; one from Taipei Veterans General Hospital, Taiwan [13]; four from Yonsei University, Korea [1417]; four from National Cancer Center, Korea [1821]). Finally, a total of nineteen studies were included for final meta-analysis [2240]. A flow chart of the search strategies, which contains reasons for the exclusion of studies, is elucidated in Fig. 1.
Fig. 1
Fig. 1

Flow chart of literature search strategies

Study characteristics and quality

A total of 5953 patients were included in the analysis with 4123 undergoing LG (69.3%) and 1830 undergoing RG (30.7%). Most of the studies came from East Asia (10 Korea, 2 Japan, 4 China, 1 Taiwan) and 2 research studies came from Italy. The baseline features of the included studies are shown in Table 1; the evaluation of quality according to the NOS is shown in Table 2. NOS shows that four out of the 19 studies observed had 9 stars, one had 8 stars, seven had 7 stars and the remaining seven had 6 stars.
Table 1

Summary of studies included in the meta-analysis

Author

Region

Study design

Year

Study

period

Sample size

Level of lymphadenectomy

Surgical extension

Reconstruction

Conversion (%)

LG

RG

LG

RG

Pugliese

Italy

OCS (R)

2010

2000–2009

48

16

D2

D

R-Y

3(6)

2(12)

Kim MC

Korea

OCS (P)

2010

2007–2008

11

16

D1 + β, D2

D

B-I, B-II

0

0

Kim KM

Korea

OCS (P)

2012

2005–2010

861

436

D1 + α/β, D2

D, T

B-I, B-II, R-Y

NR

NR

Son SY

Korea

OCS (R)

2012

2007–2011

42

21

D1 + β, D2

D, P, T

B-I, B-II, R-Y

NR

NR

Kang

Korea

OCS (P)

2012

2008–2011

282

100

D1 + α/β, D2

D, T

B-I, B-II, R-Y

E

0

Zhang

China

OCS (R)

2012

2009–2011

70

97

D2

D, P, T

B-I, B-II, R-Y

0

0

Hyun

Korea

OCS (P)

2013

2009–2010

83

38

D1 + α/β, D2

D, T

B-I, B-II, R-Y

0

0

Son T

Korea

OCS (R)

2014

2003–2010

58

51

D2

T

R-Y

0

0

Noshiro

Japan

OCS (P)

2014

2010–2012

160

21

D1 + α/β, D2

D

B-I, B-II, R-Y

0

0

Huang

Taiwan

OCS (P)

2014

2008–2014

73

72

D1 + α/β, D2

D, T

B-I, R-Y

NR

NR

Zhou

China

OCS (R)

2014

2010–2013

394

120

D1 + α/β, D2

D, P, T

B-I, B-II, R-Y

E

E

Liu

China

OCS (R)

2014

2012–2013

100

100

D2

D, P, T

B-I, B-II, R-Y

1(1)

0

Lee

Korea

OCS (P)

2015

2003–2010

267

133

D2

D

B-I, B-II, R-Y

NR

NR

Han

Korea

OCS (R)

2015

2008–2013

68

68

D1 + β

PPG

GG

0

0

Park

Korea

OCS (P)

2015

2009–2011

612

145

D1 + α/β

D, T

B-I, B-II, R-Y

10(1.6)

3(2.0)

Suda

Japan

OCS (R)

2015

2009–2012

438

88

D1 + α/β, D2

D, T

B-I, B-II, R-Y

0

0

Kim HI

Korea

OCS (P)

2016

2011–2012

185

185

D1 + α/β, D2

D, T

B-I, B-II, R-Y

2(1.1)

1(0.5)

Shen

China

OCS (R)

2016

2011–2014

330

93

D1 + α/β, D2

D, T

B-I, B-II, R-Y

0

0

Cianchi

Italy

OCS (R)

2016

2008–2015

41

30

D1 + α/β, D2

D

B-II, R-Y

0

0

OCS observational clinical study, P prospectively collected data, R retrospectively collected data, D distal gastrectomy, P proximal gastrectomy, T total gastrectomy, PPG pylorus-preserving gastrectomy, B-I Billroth-I, B-II Billroth-II, R-Y Roux-en-Y, GG gastro-gastro anastomosis, E exclude, NR not reported

Table 2

Quality assessment based on the NOS for observational studies

Author

Selection (Out of 4)

Comparability (Out of 2)

Outcomes (Out of 3)

Total (Out of 9)

Pugliese

*

*

*

*

**

*

*

*

9

Kim MC

*

*

*

*

*

*

  

6

Kim KM

*

*

*

*

*

*

  

6

Son SY

*

*

*

*

**

*

  

7

Kang

*

*

*

*

*

*

  

6

Zhang

*

*

*

*

**

*

  

7

Hyun

*

*

*

*

*

*

  

6

Son T

*

*

*

*

**

*

*

*

9

Noshiro

*

*

*

*

**

*

  

7

Huang

*

*

*

*

**

*

  

7

Zhou

*

*

*

*

**

*

*

*

9

Liu

*

*

*

*

**

*

  

7

Lee

*

*

*

*

*

*

*

*

8

Han

*

*

*

*

**

*

*

*

9

Park

*

*

*

*

*

*

  

6

Suda

*

*

*

*

*

*

 

*

7

Kim HI

*

*

*

*

*

*

  

6

Shen

*

*

*

*

**

*

  

7

Cianchi

*

*

*

*

*

*

  

6

representativeness of exposed cohort

selection of nonexposed cohort

ascertainment of exposure

outcome not present at the start of the study

assessment of outcomes

length of follow-up

adequacy of follow-up

Intraoperative effects and postoperative recovery

As shown in Table 1, three studies did not report the information of conversion; two studies excluded the conversion cases, whereas another nine research studies had no conversion. The pooled data based on four studies, which reported conversion cases, showed similar conversion rates between groups (RR = 0.88, 95% CI: 0.36 ~ 2.17, P = 0.78). A longer operation time for RG than for LG was reported in the majority of research and meta-analysis revealed that the average operation time of LG was 49.05 min shorter than RG (WMD = −49.05 min; 95% CI: -58.18 ~ −39.91, P < 0.01) (Fig. 2a). Intraoperative EBL was reported in eighteen of the research studies, which was lower in RG than LG (WMD = 24.38 ml; 95% CI: 12.32 ~ 36.43, P < 0.01) (Fig. 2b).
Fig. 2
Fig. 2

Forest plot of the meta-analysis for intraoperative effects and postoperative recovery. a Operation time. b Estimated blood loss. c Time to first flatus. d Time to restart oral intake. e Length of postoperative hospital stay

The pooled mean time to first flatus indicated no significant difference between the two groups (WMD = 0.09 days; 95% CI: -0.10 ~ 0.27, P = 0.36) (Fig. 2c). Nonetheless, according to the meta-analysis, the mean time to restart oral intake was longer in LG than in RG (WMD = 0.23 days; 95% CI: 0.13 ~ 0.34, P < 0.01) (Fig. 2d). All studies reported the LOS. According to the pooled data, a significant difference did not exist between the two groups with regard to LOS (WMD = 0.35 days; 95% CI: -0.25 ~ 0.95, P = 0.25) (Fig. 2e). All intraoperative effects and postoperative recovery outcomes are summarized in Table 3.
Table 3

Results of the meta-analysis

Outcomes

No. of studies

Sample size

Heterogeneity (P, I 2 )

Overall effect size

95% CI of overall effect

P

LG

RG

Conversion

4

16

6

0.68, 0%

RR =0.88

0.36 ~ 2.17

0.78

Operation time (min)

19

4123

1830

<0.001, 88%

WMD = −49.05

-58.18 ~ −39.91

<0.01

Blood loss (mL)

18

4055

1762

<0.001, 93%

WMD =24.38

12.32 ~ 36.43

<0.01

Time to first flatus (days)

9

1231

713

<0.001, 74%

WMD =0.09

-0.10 ~ 0.27

0.36

Time to oral intake (days)

9

2055

1096

0.67, 0%

WMD =0.23

0.13 ~ 0.34

<0.01

Hospital stay (days)

19

4123

1830

<0.001, 82%

WMD =0.35

-0.25 ~ 0.95

0.25

Overall complications

19

4123

1830

0.82, 0%

RR =0.96

0.82 ~ 1.13

0.65

Surgical complications

17

3234

1552

0.52, 0%

RR =0.87

0.72 ~ 1.05

0.15

Medical complications

12

2137

907

0.82, 0%

RR =1.34

0.75 ~ 2.40

0.32

Reoperation

7

1796

789

0.35, 11%

RR =0.69

0.29 ~ 1.62

0.39

Mortality

7

2131

838

0.91, 0%

RR =0.67

0.26 ~ 1.74

0.41

Retrieved lymph nodes

17

3229

1585

<0.001, 86%

WMD = −1.44

-3.26 ~ 0.37

0.12

Proximal margin (cm)

9

2006

1024

0.21, 26%

WMD = −0.14

-0.36 ~ 0.07

0.18

Distal margin (cm)

8

1948

973

<0.001, 81%

WMD =0.09

-0.46 ~ 0.65

0.74

Recurrence

3

500

187

0.39, 0%

RR =1.09

0.57 ~ 2.05

0.80

Cost (USD)

4

390

384

<0.001, 93%

WMD = −3944.8

-4943.5 ~ −2946.2

<0.01

Morbidity and mortality

All studies reported adverse incidents ranging from 0% to 47.4% in RG and from 4.3% to 38.6% in LG. No significant difference in the rate of overall postoperative complications was identified between the groups of RG and LG (RR = 0.96, 95% CI: 0.82 ~ 1.13, P = 0.65) (Fig. 3a). Symmetry was shown in the visual inspection of the funnel plot, showing no severe publication bias (Fig. 4). After further analysis, surgical complications were similar between groups (RR = 0.87, 95% CI: 0.72 ~ 1.05, P = 0.15) (Fig. 3b), as were the medical complications (RR = 1.34, 95% CI: 0.75 ~ 2.40, P = 0.32) (Fig. 3c). Reoperation cases were reported in seven studies, and there was no significant difference in the reoperation rates (RR = 0.69, 95% CI: 0.29 ~ 1.62, P = 0.39) (Fig. 3d). Also, seven studies reported mortality and no significant difference could be found in postoperative mortality (RR = 0.67, 95% CI: 0.26 ~ 1.74, P = 0.41) (Fig. 3e). The specific reoperation and causes of mortality reported in the studies are summarized in Table 4. The meta-analysis results on morbidity and mortality are outlined in Table 3.
Fig. 3
Fig. 3

Forest plot of the meta-analysis for morbidity and mortality. a Overall postoperative complications. b Surgical complications. c Medical complications. d Reoperation. e Mortality

Fig. 4
Fig. 4

Funnel plot of the overall postoperative complications

Table 4

Systematic review of the specific reoperation and death reasons

Author

Group

Reoperation

Death

Pugliese

LG

Enterocutaneous leak (n = 1)

Severe bleeding due to hepatic failure (n = 1)

RG

NC

Hemorrhagic stroke (n = 1)

Kim KM

LG

Leak-related (n = 4)a

Leak-related (n = 2)a

RG

Leak-related (n = 6)a

NC

RG

Leakage and obstruction (n = 5)

NC

Lee

LG

Anastomotic leakage (n = 1)

NC

RG

Anastomotic leakage (n = 1), anastomotic bleeding (n = 1)

Anastomotic bleeding (n = 1)

Huang

LG

NC

Duodenal stump leakage (n = 1)

RG

NC

Gastrojejunostomy leakage (n = 1)

Han

LG

Intra-abdominal bleeding due to liver capsular injury (n = 1)

NC

Park

LG

NC

Immediate postoperative bleeding (n = 1), mesenteric infarction (n = 1), septic shock caused by afferent loop syndrome (n = 1)

Cianchi

LG

NC

Duodenal stump leakage with peritonitis and sepsis (n = 1), acute myocardial infarction (n = 1)

RG

Intestinal occlusion (n = 1)

Cerebral vascular accident (n = 1)

NC no case

a: included anastomotic leakage and duodenal stump leakage

Oncologic outcomes and long-term survival

The differences in the average number of RLNs were not considerable in the pooled statistics with a tendency towards a reduction in the LG group when compared to the RG group (WMD = −1.44; 95% CI: -3.26 ~ 0.37, P = 0.12) (Fig. 5a). The distal or proximal margin distances were described in nine studies. Meta-analysis of the proximal margin distances showed no significant difference between the two groups (WMD = −0.14 cm; 95% CI: -0.36 ~ 0.07, P = 0.18) (Fig. 5b), the same applies to the distal margin distance (WMD = 0.09 cm; 95% CI: -0.46 ~ 0.65, P = 0.74) (Fig. 5c). Cancer recurrence was reported in three research studies and the pooled data indicated that the difference between RG and LG was not significant (RR = 1.09, 95% CI: 0.57 ~ 2.05, P = 0.80). Long-term survival rates were reported in three research studies, and no considerable difference in the survival rates between the LG group and RG group could be found. In addition, during the follow-up time, no significant difference in the survival rates between both of the groups could be found in the studies of Lee et al. [34] and Han et al. [35] though they failed to report the particular survival rates. The meta-analysis of survival rates cannot be done due to the limited data. The systematic review outcomes of follow-up time, recurrence patterns and sites, and long-term survival rates are summarized in Table 5.
Fig. 5
Fig. 5

Forest plot of the meta-analysis for oncologic outcomes. a Number of retrieved lymph nodes. b Proximal margin distances. c Distal margin distance. d Cancer recurrence

Table 5

Systematic Review of Recurrence and Long-term Survivals

Author

Group

Stage

Chemotherapy

Follow-up (mo)

Recurrence

Survival (%)

Pugliese

LG

Any TNM0

T3 or any TN+

53 (3–112)

8a

3y–OS: 85; 5y–OS: 83&

RG

28 (2–44)

4a

3y–OS: 78&

Son T

LG

Any TNM0

NR

70

3b

5y–DFS: 91.2; 5y–OS: 91.1

RG

3b

5y–DFS: 90.2; 5y–OS: 89.5

Zhou

LG

Any TNM0

Routinely#

17(3–41)

28

1, 2, 3-OS: 87.3, 77.1, 69.9

3y–OS N:82.6, 3y–OS N+:60.3

RG

5

1, 2, 3-OS: 90.2, 78.1, 67.8

3y–OS N: 84.4, 3y–OS N+: 57.5

Lee

LG

Any TNM0

NR

75

NR

NSD

RG

Han

LG

cT1-2N0M0

3 cases (4.4%)$

19.3

0

NSD

RG

3 cases (4.4%)$

22.7

0

Follow-up time were shown as median (range) or median only

DFS disease-free survival, OS overall survival, y year, N negative nodal metastasis, N + positive nodal metastasis, NR not report, NSD only reported no significant difference between two groups without specific survival rate

asome patients had mixed tumor recurrence, identified recurrence in LG: local (n = 2), peritoneum (n = 2), liver (n = 1), lung (n = 2), bone (n = 1); identified recurrence in RG: peritoneum (n = 1), liver (n = 1), bone (n = 1). &: for overall patients, 5y–OS N: 97%, 5y–OS N+: 52%

bLG, peritoneum (n = 2), lung (n = 1); RG, breast (n = 1), splenic hilum (n = 1), ovary (n = 1). #: 5-fluorouracil + oxaliplatin intravenous chemotherapy. $: because of advanced disease status after surgery

Total cost

Only four studies recorded their total cost and they all reported a higher cost for RG than LG. The meta-analysis demonstrated that the total cost of RG groups was significantly higher than LG groups (WMD = −3944.8 USD; 95% CI: -4943.5 ~ −2946.2, P < 0.01) (Fig. 6).
Fig. 6
Fig. 6

Forest plot of the meta-analysis for total cost

Subgroup analysis of distal or total gastrectomy

For the subgroup analysis of distal gastrectomy (DG), the RG group still holds the longer operation time (P < 0.01), lower EBL (P < 0.05) and with similar LOS, overall complications, mortality as well as RLN (P > 0.05). However, there was a reduced time to oral intake for RG, but with only a marginal difference compared to the LG group (P = 0.05). As for total gastrectomy (TG), there is no large difference between the outcomes of operation time, EBL, time to oral intake, LOS, overall complications and mortality against DG subgroup analysis, the number of RLNs of RG was more than that of LG with a significant difference (P = 0.03). The subgroup analysis results of surgical extension are summarized in Table 6. Generally speaking, the difference in surgical extension had little effect on the overall meta-analysis results.
Table 6

Results of the subgroup analysis of distal or total gastrectomy

Outcomes

No. of studies

Sample size

Heterogeneity (P, I 2 )

Overall effect size

95% CI of overall effect

P

LG

RG

Operation time (min)

 DG

8

1635

453

<0.001, 78%

WMD = −57.08

−68.62 ~ −45.54

<0.01

 TG

5

448

166

0.004, 74%

WMD = −42.62

−66.72 ~ −18.52

<0.01

Blood loss (mL)

 DG

8

1635

453

<0.001, 77%

WMD =19.27

3.86 ~ 34.68

0.01

 TG

5

448

166

0.54, 0%

WMD =23.77

1.97 ~ 45.56

0.03

Time to oral intake (days)

 DG

3

344

116

0.49, 0%

WMD =0.18

0.00 ~ 0.36

0.05

 TG

3

251

100

0.71, 0%

WMD = −0.18

−0.55 ~ 0.20

0.36

Hospital stay (days)

 DG

8

1635

453

<0.001, 92%

WMD =0.52

−0.69 ~ 1.74

0.40

 TG

5

448

166

0.75, 0%

WMD =0.28

−0.80 ~ 1.36

0.61

Overall complications

 DG

8

1635

453

0.86, 0%

RR =1.19

0.83 ~ 1.71

0.34

 TG

4

330

140

0.49, 0%

RR =1.32

0.80 ~ 2.18

0.27

Mortality

 DG

4

942

213

0.84, 0%

RR =0.84

0.21 ~ 3.30

0.80

 TG

2

194

81

0.55, 0%

RR =0.15

0.02 ~ 1.41

0.10

Retrieved lymph nodes

 DG

8

1635

453

<0.001, 92%

WMD = −2.10

−5.90 ~ 1.70

0.28

 TG

5

448

166

0.63, 0%

WMD = −2.51

−4.83 ~ −0.19

0.03

DG distal gastrectomy, TG total gastrectomy

Subgroup analysis of weight influence

Only two studies had data for subgroup analysis based on weight [28, 34]. The patients were divided based on preoperative BMI into non-overweight (BMI < 25 kg/m2) and overweight (BMI >25 kg/m2) groups. In the non-overweight subgroup, the RG group still had a longer operation time (P < 0.01), while in the overweight subgroup; the operation time was similar between groups (P = 0.27). In addition, there was no significant difference between LG and RG for the outcomes of EBL and RLNs regardless of overweight or non-overweight subgroup. Other perioperative outcomes cannot be analyzed due to the limited data. The subgroup analysis results based on weight are summarized in Table 7.
Table 7

Results of the subgroup analysis of weight

Outcomes

No. of studies

Sample size

Heterogeneity (P, I 2 )

Overall effect size

95% CI of overall effect

P

LG

RG

Operation time (min)

 non-overweight

2

232

127

0.06, 72%

WMD = −37.63

−62.82 ~ −12.43

<0.01

 overweight

2

118

44

0.008, 86%

WMD = −28.58

−79.11 ~ 21.94

0.27

Blood loss (mL)

 non-overweight

2

232

127

0.11, 60%

WMD =0.90

−13.44 ~ 15.25

0.90

 overweight

2

118

44

0.03, 80%

WMD =39.84

−41.71 ~ 121.39

0.34

Retrieved lymph nodes

 non-overweight

2

232

127

0.34, 0%

WMD = −1.88

−4.78 ~ 1.01

0.20

 overweight

2

118

44

0.03, 79%

WMD =4.32

−4.10 ~ 12.74

0.31

Discussion

The cost-effectiveness and definite advantages of RG have not been well documented, which is different when compared to the evolution of LG versus conventional open surgery [20]. However, the number of publications on RG has gradually increased in recent years. The oncologic outcomes, postoperative outcome, intraoperative effects and costs of a total of 1830 patients who underwent RG for gastric cancer treatment in 19 studies were reviewed as we believe such research would contribute to a more objective and comprehensive assessment of the current RG surgical status.

In spite of the considerable heterogeneity, the prolonged operating time in RG was shown in almost all the included research studies. The prolonged exposure time to pneumoperitoneum and the associated increased time of anesthesia is a major concern. Few publications describe the effect of longer operation times during RG. However, previous research of LG in senior patients has shown that longer operation time did not result in detrimental effects with regard to surgical results [41]. Therefore, a prolonged operating time should not affect surgeons directly on conducting research on RG’s new utility. Inevitably, the docking time was considered as an essential factor, which enhanced the operating time. The docking time was between 20 min to 60 min as reported in our study [7, 13, 15, 31], We found RG had longer operation times than LG by 49 min, which suggested the ‘true’ time spent on operations was similar or even shorter than LG. Furthermore, with the increased utilization of the new robotic surgical system, operation times are expected to shorten. Several studies have reported that the da Vinci Xi robotic platform is more user-friendly and is easier to install in rectal and nephritic surgery [42, 43]. As a result, we believed that RG is technically feasible with regard to operation time.

Surgeons have to go through a learning curve to master a technique. The surgical results, such as operation time, oncological outcomes and postoperative complications can be affected by surgeon’s familiarity with the instrument, experience and assistant compliance. In general, before stabilization, LG should be conducted on around 40 to 60 cases [44]. The learning curve for RG was shorter for experienced surgeon who had performed LG, which is forecasted to be only 10 to 20 cases [12, 13, 18, 26]. A surgeon experienced in laparoscopic surgery can conduct robotic surgery securely even in their first case [16]. Several studies investigated in this meta-analysis compared the initial and later experiences of robotic surgery [12, 13, 18, 26]. The later cases performed by the same surgical team could progress toward shortening operation times.

Postoperative morbidity is the main indicator for assessing the safety and feasibility of one procedure. It is widely accepted that laparoscopic surgery for gastric cancer is safer and could have fewer complications than open surgery [45]. Our meta-analysis demonstrated a comparable complication rate in RG versus LG group, and the low heterogeneity regardless of overall, surgical or medical complications encourages us to believe that RG indeed is as safe as LG. Improvements such as three-dimension images and tremor filtering could theoretically contribute to safer implementations of the robotic system for gastrectomy and lymphadenectomy. According to the multivariate analyses in the Suda study, the application of RG was an important independent protective factor in regards to the postoperative complication [37]. Tokunaga et al. [46, 47] reported the incidences of overall adverse events after RG which were 14.2% and 22.2% based on their two-phase II studies, which are comparable to the rates of 19–27% in previous studies of LG [48, 49].

Obesity is one of the most significant health problems today and rates are still increasing around the world. Some studies claim obesity causes increased blood loss, operation time, and wound infection rate et al. [50, 51], whereas others did not observe any negative effect on surgical outcomes [52]. Recently, Harr et al. [10] showed that the benefits of robotic methods were more evident in high versus normal BMI patients when performing a colostomy. The authors concluded that robotic surgery might overcome the difficulties associated with thick abdominal walls and excessive intra-abdominal fat, thanks to improved visualization, instrumentation, and ergonomics [10]. However, compared to other operations such as the colorectal or prostatic surgeries, which are in relatively narrow regions, the superiority of da Vinci over the laparoscopy may not be obvious, in that gastric surgery is conducted in the upper abdomen of a relatively spacious location. In our study, the overall mean operation time of RG and LG were similar in the overweight subgroups, contrasting with those in the non-overweight subgroups, which implied RG to be superior to LG when used on overweight patients. However, the sample size of the overweight subgroups was not large enough to be conclusive.

The traditional straight forceps in LG fail to enable surgeons to reach deep-seated vessels and other areas, like the supra pancreatic one, in which the dissection of lymph nodes around the splenic hilum, splenic artery, and hepatic artery areas is deemed extremely hard. The tremor filtering, wristed instruments, as well as stable exposure and high-solution image can help surgeons thoroughly retrieve the lymph nodes around the delicate areas [21]. According to one included study, the amount of RLNs was considerably higher with robotic surgery in the splenic hilum and splenic artery areas [29]. Our meta-analysis shows adequate RLNs with means of 35.4 and 36.1 in the LG and RG groups, respectively. The mean number of RLNs of RG was more than that of LG with a marginal difference observed in the pooled data, even though most studies had been done during initial implementation of the robotic technique. Therefore, we believe that robotic technique could be superior to the conventional laparoscopic technique for lymphadenectomy. Since the history of the clinical application of RG is a short one, few reports have compared long-term survival outcomes with other methods. Coratti et al. [53] demonstrated that the 5-year survival rate after RG stratified with Stage IA, IB, II, and III was 100%, 84.6%, 76.9%, and 21.5%, respectively. Pugliese et al. [11] reported a cumulative overall 5-year survival rate of 78% with a mean follow up of 30 months (range 2–86) after RG for gastric cancer.

The application of robotic surgery remains controversial, mainly due to the considerable expense. The total difference in cost between the LG and RG groups has been predicted to be around 3900 USD [18, 31, 38], which is mainly derived from the robotic system itself. According to the opinions of some investigators, the higher cost of robotic surgery is not enough to justify the theoretical advantages of this technology [54]. If RG can reduce complications and shorten hospital stay, the higher costs of the robotic system would be partially offset. Based on this, it is essential for robotic operators to inspect whether the potential advantages of the robotic approach justifies its high cost in the treatment of gastric cancer.

Our research has the following limitations: (1) Selection bias: As no RCT was available to be included in the meta-analysis due to the higher cost of robotic surgery, selection biases are inevitable in surgical abstention which should be carefully interpreted. (2) Clinical heterogeneity: The homogeneity test for the continuous variables exhibited substantial heterogeneity due to the inherent flaws of a retrospective study, the uneven surgical skills of the different surgeons, as well as regional differences, etc. More importantly, for surgeons in the East, radical distal gastrectomy for middle and distal gastric cancer is popular [55], while the distal subtotal is preferred in the West [56]. Thus we cataloged distal gastrectomy and subtotal gastrectomy as a subgroup. Though it brings some interesting results due to the expansion of sample size, such a combination would result in clinical heterogeneity. (3) Regional difference: The majority of the included studies came from East Asia, because East Asia has the highest prevalence of gastric cancer, while gastric cancer is relatively uncommon in Western countries. Besides, in East Asia, particularly Korea, Japan and some areas of China, the proportion of early gastric cancer has increased as a result of the improved surveillance of gastric cancer in these regions [57, 58]. On the other hand, although increasing evidence continues to show no difference between patients undergoing open or laparoscopic surgery for oncologic outcomes, the Japanese Gastric Cancer Association still classifies minimal invasive surgery as investigational treatment and only recommends minimal invasive surgery for early stage gastric cancer patients [55]. Therefore, the cases in our studies, especially those from East Asia, were mainly early stage cases. All of the above limitations must be kept in mind when interpreting the results of our study.

Conclusions

Except for the longer operation time and higher costs, RG for the patients with gastric cancer was not inferior to LG. Besides; RG holds the potential benefits for larger numbers of lymph node dissection and reduced intraoperative blood loss. Further prospective studies are needed in order to confirm these advantages. In addition, long-term results are needed, particularly for the oncological adequacy of robotic gastric cancer resections.

Abbreviations

BMI: 

body mass index

EBL: 

estimated blood loss

LG: 

laparocopic gastrectomy

LOS: 

length of hospital stay

NOS: 

Newcastle-Ottawa Quality Assessment Scale

RCT: 

randomized controlled trial

RG: 

robotic gastrectomy

RLN: 

retrieved lymph nodes

RR: 

risk ratio

SD: 

standard deviation

WMD: 

weighted mean difference

Declarations

Acknowledgments

Not applicable.

Funding

Not applicable.

Availability of data and materials

The datasets analyzed during the current study available from the corresponding author on reasonable request.

Authors’ contributions

KC and YP designed the study; BZ and XFW collected literatures and conducted the analysis of pooled data; HM helped to draft the manuscript; KC and YP wrote the manuscript; XJC proofread and revised the manuscript. All authors have approved the version to be published.

Competing interest

The authors declare that they have no competing interests.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Publisher’s Note

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

Open AccessThis 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.

Authors’ Affiliations

(1)
Department of General Surgery, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, 3 East Qingchun Road, Hangzhou, Zhejiang Province, 310016, China
(2)
School of Medicine, Zhejiang University, 866 Yuhangtang Road, Hangzhou, Zhejiang Province, 310058, China

References

  1. Chen K, Mou YP, Xu XW, Pan Y, Zhou YC, Cai JQ, et al. Comparison of short-term surgical outcomes between totally laparoscopic and laparoscopic-assisted distal gastrectomy for gastric cancer: a 10-y single-center experience with meta-analysis. J Surg Res. 2015;194:367–74.View ArticlePubMedGoogle Scholar
  2. Chen K, Wu D, Pan Y, Cai JQ, Yan JF, Chen DW, et al. Totally laparoscopic gastrectomy using intracorporeally stapler or hand-sewn anastomosis for gastric cancer: a single-center experience of 478 consecutive cases and outcomes. World J Surg Oncol. 2016;14:115.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Chen K, He Y, Cai JQ, Pan Y, Wu D, Chen DW, et al. Comparing the short-term outcomes of intracorporeal esophagojejunostomy with extracorporeal esophagojejunostomy after laparoscopic total gastrectomy for gastric cancer. BMC Surg. 2016;16:13.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Chen K, Xu XW, Zhang RC, Pan Y, Wu D, Mou YP. Systematic review and meta-analysis of laparoscopy-assisted and open total gastrectomy for gastric cancer. World J Gastroenterol. 2013;19:5365–76.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Rockall TA, Darzi A. Robot-assisted laparoscopic colorectal surgery. Surg Clin North Am. 2003;83:1463–8. xiView ArticlePubMedGoogle Scholar
  6. Gutt CN, Oniu T, Mehrabi A, Kashfi A, Schemmer P, Buchler MW. Robot-assisted abdominal surgery. Br J Surg. 2004;91:1390–7.View ArticlePubMedGoogle Scholar
  7. Song J, Oh SJ, Kang WH, Hyung WJ, Choi SH, Noh SH. Robot-assisted gastrectomy with lymph node dissection for gastric cancer: lessons learned from an initial 100 consecutive procedures. Ann Surg. 2009;249:927–32.View ArticlePubMedGoogle Scholar
  8. Grobmyer SR, Pieracci FM, Allen PJ, Brennan MF, Jaques DP. Defining morbidity after pancreaticoduodenectomy: use of a prospective complication grading system. J Am Coll Surg. 2007;204:356–64.View ArticlePubMedGoogle Scholar
  9. 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.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Harr JN, Luka S, Kankaria A, Juo YY, Agarwal S, Obias V. Robotic-assisted colorectal surgery in obese patients: a case-matched series. Surg Endosc. 2017;31:2813–9.View ArticlePubMedGoogle Scholar
  11. Pugliese R, Maggioni D, Sansonna F, Ferrari GC, Forgione A, Costanzi A, et al. Outcomes and survival after laparoscopic gastrectomy for adenocarcinoma. Analysis on 65 patients operated on by conventional or robot-assisted minimal access procedures. Eur J Surg Oncol. 2009;35:281–8.View ArticlePubMedGoogle Scholar
  12. Uyama I, Kanaya S, Ishida Y, Inaba K, Suda K, Satoh S. Novel integrated robotic approach for suprapancreatic D2 nodal dissection for treating gastric cancer: technique and initial experience. World J Surg. 2012;36:331–7.View ArticlePubMedGoogle Scholar
  13. Huang KH, Lan YT, Fang WL, Chen JH, Lo SS, Hsieh MC, et al. Initial experience of robotic gastrectomy and comparison with open and laparoscopic gastrectomy for gastric cancer. J Gastrointest Surg. 2012;16:1303–10.View ArticlePubMedGoogle Scholar
  14. Song J, Kang WH, Oh SJ, Hyung WJ, Choi SH, Noh SH. Role of robotic gastrectomy using da Vinci system compared with laparoscopic gastrectomy: initial experience of 20 consecutive cases. Surg Endosc. 2009;23:1204–11.View ArticlePubMedGoogle Scholar
  15. Woo Y, Hyung WJ, Pak KH, Inaba K, Obama K, Choi SH, et al. Robotic gastrectomy as an oncologically sound alternative to laparoscopic resections for the treatment of early-stage gastric cancers. Arch Surg. 2011;146(9):1086–92.View ArticlePubMedGoogle Scholar
  16. 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.View ArticlePubMedGoogle Scholar
  17. Okumura N, Son T, Kim YM, Kim HI, An JY, Noh SH, et al. Robotic gastrectomy for elderly gastric cancer patients: comparisons with robotic gastrectomy in younger patients and laparoscopic gastrectomy in the elderly. Gastric Cancer. 2016;19:1125–34.View ArticlePubMedGoogle Scholar
  18. 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.View ArticlePubMedGoogle Scholar
  19. Yoon HM, Kim YW, Lee JH, Ryu KW, Eom BW, Park JY, et al. Robot-assisted total gastrectomy is comparable with laparoscopically assisted total gastrectomy for early gastric cancer. Surg Endosc. 2012;26:1377–81.View ArticlePubMedGoogle Scholar
  20. Park JY, Jo MJ, Nam BH, Kim Y, Eom BW, Yoon HM, et al. Surgical stress after robot-assisted distal gastrectomy and its economic implications. Br J Surg. 2012;99:1554–61.View ArticlePubMedGoogle Scholar
  21. 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.View ArticlePubMedGoogle Scholar
  22. 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.View ArticlePubMedGoogle Scholar
  23. Kim MC, Heo GU, Jung GJ. Robotic gastrectomy for gastric cancer: surgical techniques and clinical merits. Surg Endosc. 2010;24:610–5.View ArticlePubMedGoogle Scholar
  24. 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.View ArticlePubMedGoogle Scholar
  25. Son SY, Lee CM, Ahn SH, Lee JH, Park DJ, Kim HH. Clinical outcome of robotic Gastrectomy in gastric cancer in comparison with laparoscopic Gastrectomy: a case-control study. Journal of Minimally Invasive Surgery. 2012;15:27–31.View ArticleGoogle Scholar
  26. 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.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Zhang XL, Jiang ZW, Zhao K. Comparative study on clinical efficacy of robot-assisted and laparoscopic gastrectomy for gastric cancer. Zhonghua Wei Chang Wai Ke Za Zhi. 2012;15:804–6.PubMedGoogle Scholar
  28. 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.View ArticlePubMedGoogle Scholar
  29. 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.View ArticlePubMedGoogle Scholar
  30. 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.View ArticlePubMedGoogle Scholar
  31. 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.View ArticlePubMedPubMed CentralGoogle Scholar
  32. 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.View ArticlePubMedGoogle Scholar
  33. Liu J, Ruan H, Zhao K, Wang G, Li M, Jiang Z. Comparative study on da Vince robotic and laparoscopic radical gastrectomy for gastric cancer. Zhonghua Wei Chang Wai Ke Za Zhi. 2014;17:461–4.PubMedGoogle Scholar
  34. 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.View ArticlePubMedGoogle Scholar
  35. 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.View ArticlePubMedGoogle Scholar
  36. 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.View ArticlePubMedGoogle Scholar
  37. Suda K, Man IM, 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.View ArticlePubMedGoogle Scholar
  38. 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.View ArticlePubMedGoogle Scholar
  39. 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.View ArticlePubMedGoogle Scholar
  40. Cianchi F, Indennitate G, Trallori G, Ortolani M, Paoli B, Macri 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.View ArticlePubMedPubMed CentralGoogle Scholar
  41. Hwang SH, Park DJ, Jee YS, Kim HH, Lee HJ, Yang HK, et al. Risk factors for operative complications in elderly patients during laparoscopy-assisted gastrectomy. J Am Coll Surg. 2009;208:186–92.View ArticlePubMedGoogle Scholar
  42. Patel MN, Aboumohamed A, Hemal A. Does transition from the da Vinci Si to xi robotic platform impact single-docking technique for robot-assisted laparoscopic nephroureterectomy? BJU Int. 2015;116:990–4.View ArticlePubMedGoogle Scholar
  43. Morelli L, Guadagni S, Di Franco G, Palmeri M, Caprili G, D'Isidoro C, et al. Use of the new da Vinci xi during robotic rectal resection for cancer: a pilot matched-case comparison with the da Vinci Si. Int J Med Robot. 2017;13:e1728.Google Scholar
  44. Jin SH, Kim DY, Kim H, Jeong IH, Kim MW, Cho YK, et al. Multidimensional learning curve in laparoscopy-assisted gastrectomy for early gastric cancer. Surg Endosc. 2007;21:28–33.View ArticlePubMedGoogle Scholar
  45. 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.View ArticlePubMedGoogle Scholar
  46. Tokunaga M, Sugisawa N, Kondo J, Tanizawa Y, Bando E, Kawamura T, et al. Early phase II study of robot-assisted distal gastrectomy with nodal dissection for clinical stage IA gastric cancer. Gastric Cancer. 2014;17:542–7.View ArticlePubMedGoogle Scholar
  47. Tokunaga M, Makuuchi R, Miki Y, Tanizawa Y, Bando E, Kawamura T, et al. Late phase II study of robot-assisted gastrectomy with nodal dissection for clinical stage I gastric cancer. Surg Endosc. 2016;30:3362–7.View ArticlePubMedGoogle Scholar
  48. Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, et al. Long-term results of laparoscopic gastrectomy for gastric cancer: a large-scale case-control and case-matched Korean multicenter study. J Clin Oncol. 2014;32:627–33.View ArticlePubMedGoogle Scholar
  49. Chen K, Xu X, Mou Y, Pan Y, Zhang R, Zhou Y, et al. Totally laparoscopic distal gastrectomy with D2 lymphadenectomy and Billroth II gastrojejunostomy for gastric cancer: short- and medium-term results of 139 consecutive cases from a single institution. Int J Med Sci. 2013;10:1462–70.View ArticlePubMedPubMed CentralGoogle Scholar
  50. Sugimoto M, Kinoshita T, Shibasaki H, Kato Y, Gotohda N, Takahashi S, et al. Short-term outcome of total laparoscopic distal gastrectomy for overweight and obese patients with gastric cancer. Surg Endosc. 2013;27:4291–6.View ArticlePubMedGoogle Scholar
  51. Chen K, Pan Y, Zhai ST, Cai JQ, Chen QL, Chen DW, et al. Laparoscopic gastrectomy in obese gastric cancer patients: a comparative study with non-obese patients and evaluation of difference in laparoscopic methods. BMC Gastroenterol. 2017;17:78.View ArticlePubMedPubMed CentralGoogle Scholar
  52. Wang Z, Zhang X, Liang J, Hu J, Zeng W, Zhou Z. Short-term outcomes for laparoscopy-assisted distal gastrectomy for body mass index >/=30 patients with gastric cancer. J Surg Res. 2015;195:83–8.View ArticlePubMedGoogle Scholar
  53. Coratti A, Fernandes E, Lombardi A, Di Marino M, Annecchiarico M, Felicioni L, et al. 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. 2015;41:1106–13.View ArticlePubMedGoogle Scholar
  54. Park JS, Choi GS, Park SY, Kim HJ, Ryuk JP. Randomized clinical trial of robot-assisted versus standard laparoscopic right colectomy. Br J Surg. 2012;99:1219–26.View ArticlePubMedGoogle Scholar
  55. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer. 2017;20:1–19.View ArticleGoogle Scholar
  56. De Manzoni G, Marrelli D, Baiocchi GL, Morgagni P, Saragoni L, Degiuli M, et al. The Italian research Group for Gastric Cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer. 2017;20:20–30.View ArticlePubMedGoogle Scholar
  57. Inoue M, Tsugane S. Epidemiology of gastric cancer in Japan. Postgrad Med J. 2005;81:419–24.View ArticlePubMedPubMed CentralGoogle Scholar
  58. Jeong O, Park YK. Clinicopathological features and surgical treatment of gastric cancer in South Korea: the results of 2009 nationwide survey on surgically treated gastric cancer patients. J Gastric Cancer. 2011;11:69–77.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s). 2017

Advertisement