Laparoscopic Versus Robotic Gastric Cancer Surgery: Short-Term Outcomes–Systematic Review and Meta-Analysis of 25,521 Patients

Abstract

Background:

Gastric cancer has the third highest cancer-related mortality worldwide. There is no consensus regarding the optimal surgical technique to perform curative resection surgery.

Objective:

Compare laparoscopic gastrectomy (LG) and robotic gastrectomy (RG) regarding short-term outcomes in patients with gastric cancer.

Materials and Methods:

This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. We searched the following topics: “Gastrectomy,” “Laparoscopic,” and “Robotic Surgical Procedures.” The included studies compared short-term outcomes between LG and RG. Individual risk of bias was assessed with the Methodological Index for Non-Randomized Studies (MINORS) scale.

Results:

There was no significant difference between RG and LG regarding conversion rate, reoperation rate, mortality, overall complications, anastomotic leakage, distal and proximal resection margin distances, and recurrence rate. However, mean blood loss (mean difference [MD] −19.43 mL, P < .00001), length of hospital stay (MD −0.50 days, P = .0007), time to first flatus (MD −0.52 days, P < .00001), time to oral intake (MD −0.17 days, P = .0001), surgical complications with a Clavien-Dindo grade ≥III (risk ratio [RR] 0.68, P < .0001), and pancreatic complications (RR 0.51, P = .007) were significantly lower in the RG group. Furthermore, the number of retrieved lymph nodes was significantly higher in the RG group. Nevertheless, the RG group showed a significantly higher operation time (MD 41.19 minutes, P < .00001) and cost (MD 3684.27 U.S. Dollars, P < .00001).

Conclusion:

This meta-analysis supports the choice of robotic surgery over laparoscopy concerning relevant surgical complications. However, longer operation time and higher cost remain crucial limitations. Randomized clinical trials are required to clarify the advantages and disadvantages of RG.

Introduction

Nowadays, gastric cancer is the fifth most common cancer worldwide, with its highest prevalence being in Mongolia, Japan, and South Korea. Moreover, WCRF International, in 2020, demonstrated that gastric cancer has the third highest cancer-related mortality rate (7.7/100,000) and it is the fifth most incident tumor in the entire world (11.1/100,000).^1,2

Despite the development of new surgical techniques and medical devices, prognosis remains poor.³ Therefore, it is necessary to improve screening methods to achieve earlier diagnosis and improve the odds of finding a resectable tumor, so as to reduce its burden.^4,5

There are two approaches to treat localized gastric cancer: endoscopic resection or radical gastrectomy. The first one is used for gastric cancer classified as stage IA (T1 N0 M0), according to the TNM classification. On the other hand, radical gastrectomy is used for stage IB-III gastric cancers (>T1 and/or ≥N0 M0), and is associated with a simultaneous D2 lymphadenectomy. To increase the probability of a curative resection, this treatment requires neoadjuvant and adjuvant chemotherapy, to reduce preoperative tumor size and probability of recurrence, respectively.⁶

Currently, the main surgical approaches are minimally invasive, including laparoscopic surgery and robotic surgery.⁵

The largely used conventional laparoscopic gastrectomy (LG) has shown several advantages, when compared with open gastrectomy, such as better surgical safety, less trauma, lower operative morbidity, and faster recovery, with similar overall survival, oncologic outcomes, and relapse-free survival.^6,7

On the other hand, robotic gastrectomy (RG) yields high-resolution three-dimensional (3D) images, wrist instruments that offer freedom, tremor filtering technology, and less fatigue. These features are expected to overcome some drawbacks of laparoscopic surgery.⁵

There are several studies that reported the advantages of RG, when compared with LG, on the following short-term outcomes in patients with gastric cancer: less blood loss, higher number of harvested lymph nodes, less time to first flatus, shorter length of hospital stay, and less postoperative complications.⁸ However, the cost and the operative time related to the expensive instruments and the low experience in performing robotic surgery are still relevant limitations to its current utilization.^5,9

Therefore, our systematic review includes the most recent observational studies and the current literature about the comparison of the short-term outcomes between LG and RG for gastric cancer patients to clarify the feasibility and efficiency of robotic surgery, as it is predicted to be more prevalent in the coming years.¹⁰

Materials and Methods

Search strategy/information sources

We conducted our meta-analysis according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. Literature search was performed independently by 2 reviewers, on the following databases: PubMed, Web of Science, and Cochrane Library. The query used in PubMed was as follows: “Search (((laparoscopic gastrectomy) OR ((“” Gastrectomy”” [Majr:NoExp]) AND “” Laparoscopy “”[Mesh]))) OR ((((“” Gastrectomy “” [Majr:NoExp]) AND “” Robotic Surgical Procedures “” [Mesh])) OR robotic gastrectomy).” In the Web of Science and Cochrane Library, we used the following query: “((“Gastrectomy” AND “Laparoscopy”) OR (“Laparoscopic Gastrectomy”)) AND (“Robotic Surgery” OR “Robotic Surgical Procedures” OR “Robotic Gastrectomy”).” Existing systematic reviews were also consulted for additional articles.

Study selection and eligibility criteria

The researchers screened the literature and selected articles based on their titles and abstracts. In accordance with previous reviews, we included observational clinical studies that compared short-term outcomes between the two surgical approaches (RG and LG), in patients with gastric cancer, who underwent curative-intent surgery.^8,11,12

Then, the authors reviewed the full texts and excluded articles that met the following exclusion criteria: (1) articles that also reported comparison of two robotic systems, (2) proximal gastrectomy comparison only, and (3) D1 lymphadenectomy only. One article was excluded due to the impossibility of obtaining an English version.

Data extraction

Two reviewers independently read and interpreted every original study. Data extraction comprised study information (author, region, published year, study period, study design, sample size, surgical extension, level of lymphadenectomy, and reconstruction options), patients' characteristics (age and gender), and short-term outcomes, which included 3 groups: surgical outcomes (operating time, blood loss, conversion rate, reoperation rate, and mortality rate), postoperative outcomes (length of hospital stay, time to first flatus, time to oral intake, overall complications, surgical complications according to Clavien-Dindo [CD] Grade, anastomotic leakage, pancreatic complication, and cost of operation), and oncological outcomes (distal resection margin distance, proximal resection margin distance, recurrence rate, and number of retrieved lymph nodes). These variables were chosen in accordance with previous systematic reviews^8,9,11,12 (Tables 1 and 2).

Table 1.

Summary of Studies Included in the Meta-Analysis

No.	Author (year)	Region	Year	Study period	Study design	Sample size		Surgical extension	Level of LND	Reconstruction	MINORS
No.	Author (year)	Region	Year	Study period	Study design	RG	LG	Surgical extension	Level of LND	Reconstruction	MINORS
(1)	Aktas et al. (2020)	Turkey	2020	2013–2018	OCS (P)	30	64	D, P, T, EGJ	D2	RY	21
(2)	Alhossaini et al. (2020)	Korea	2019	2005–2017	OCS (R)	25	30	T	NA	BI, BII	23
(3)	Cianchi et al. (2016)	Italy	2016	2008–2015	OCS (P)	30	41	D	D1+a/b, D2	BII, RY	21
(4)	Eom et al. (2012)	Korea	2011	2009–2010	OCS (P)	30	62	D	D1+b, D2	BII	22
(5)	Gao et al. (2022)	China	2022	2015–2021	OCS (R)	441	723	D	D2	BI, BII, RY	21
(6)	Gao et al. (2019)	China	2018	2011–2014	OCS (P)	163	339	D, P, T	D1+, D2	BI, BII, RY	21
(7)	Han et al. (2015)	Korea	2015	2008–2013	OCS (R)	68	68	PPG	D1+b	GG	23
(8)	Hikage et al. (2022)	Japan	2022	2013–2020	OCS (P)	36	58	T	D1+, D2	EJJ	21
(9)	Hong et al. (2016)	Korea	2016	2008–2015	OCS (P)	232	232	D	D1+a/b, D2	BI, BII, RY	22
(10)	Huang et al. (2014)	Taiwan	2014	2008–2014	OCS (P)	72	73	D, T	D1+a/b, D2	BI, RY	22
(11)	Hyun et al. (2013)	Korea	2013	2009–2010	OCS (P)	38	83	D, T	D1+a/b, D2	BI, BII, RY	22
(12)	Isobe et al. (2021)	Japan	2021	2018–2020	OCS (R)	69	88	D	D1, D1+, D2	BI, BII, RY	21
(13)	Junfeng et al. (2014)	China	2014	2010–2013	OCS (R)	120	394	D, P, T	D1, D2	BI, BII, RY	23
(14)	Kang et al. (2012)	Korea	2012	2008–2011	OCS (P)	100	282	D, T	D1+a/b, D2	BI, BII, RY	22
(15)	Kim et al. (2016a)	Korea	2013	2003–2009	OCS (P)	172	481	D, T	D1+a/b, D2	BI, BII	22
(16)	Kim et al. (2014)	Korea	2016	2011–2012	OCS (P)	185	185	D, T	D1+a/b, D2	BI, BII, RY	23
(17)	Kim et al. (2012)	Korea	2012	2005–2010	OCS (P)	436	861	D, T	D1+a/b, D2	BI, BII, RY	23
(18)	Kim et al. (2010)	Korea	2010	2007–2008	OCS (P)	16	11	D	D1+b, D2	BI, BII	22
(19)	Kim et al. (2016b)	Korea	2015	2009–2001	OCS (P)	87	288	D	D1, D2	NA	20
(20)	Kong et al. (2020)	China	2020	2014–2017	OCS (R)	294	750	D, P, T	D2, D2+	BI, BII, RY	21
(21)	Lee et al. (2015)	Korea	2015	2003–2010	OCS (P)	133	267	D	D2	BI, BII, RY	21
(22)	Liu et al. (2018)	China	2018	2017–201	OCS (R)	100	135	D, T	D1+a/b, D2	BII, RY	21
(23)	Li et al. (2018)	China	2018	2013–2017	OCS (P)	112	112	D, T	D2	BI, BII, RY	23
(24)	Lu et al. (2018)	China	2018	2016–2017	OCS (P)	101	303	D, T	D1+, D2	BI, BII, RY	20
(25)	Nakauchi et al. (2016)	Japan	2016	2009–2012	OCS (R)	84	437	D, T	D1+a/b, D2	BI, BII, RY	23
(26)	Nishi et al. (2022)	Japan	2022	2005–2020	OCS (R)	83	368	D, P, T, PPG	D1, D2	BI, RY	21
(27)	Noshiro et al. (2014)	Japan	2014	2010–2012	OCS (P)	21	160	D	D1+a/b, D2	BI, BII, RY	22
(28)	Obama et al. (2018)	Korea	2017	2005–2009	OCS (P)	315	525	D, T	D1+a/b, D2	BI, BII, RY	23
(29)	Okabe et al. (2021)	Japan	2021	2012–2020	OCS (P)	110	256	D, P, T	D1+, D2	BI, RY	22
(30)	Okumura et al. (2016)	Japan	2016	2003–2010	OCS (P)	370	132	D, T	D1+a/b, D2	BI, BII, RY	22
(31)	Omori et al. (2022)	Japan	2022	2014–2019	OCS (P)	210	979	D, P, T, EGJ	D1+, D2	BI	22
(32)	Parisi et al. (2017)	Italy	2017	2015–2016	OCS (P)	151	151	D, T	D2	BI, BII, RY	21
(33)	Park et al. (2015)	Korea	2015	2009–2011	OCS (P)	145	612	D, T	D1+a/b	BI, BII, RY	19
(34)	Pugliese et al. (2010)	Italy	2010	2000–200	OCS (R)	16	48	D	D2	RY	21
(35)	Roh et al. (2020)	Korea	2020	2015–2017	OCS (R)	56	152	D	D1+	BI, BII	21
(36)	Roh et al. (2021)	Korea	2021	2009–2018	OCS (P)	74	321	T	D1+, D2	RY	22
(37)	Ryan et al. (2020)	United States	2020	2010–2014	OCS (P)	631	1262	T, ST	NA	NA	22
(38)	Seo et al. (2015)	Korea	2014	2004–2009	OCS (P)	40	40	D	D1+b, D2	BI, BII, RY	20
(39)	Shen et al. (2016)	China	2016	2011–2014	OCS (R)	93	330	D, T	D1+a/b, D2	BI, BII, RY	21
(40)	Shibasaki et al. (2020)	Japan	2020	2009–2019	OCS (P)	359	1042	D, P, T	D1+, D2	BI, BII, RY	22
(41)	Song et al. (2009)	Korea	2008	2005–2006	OCS (P)	20	20	D	D1+a/b, D2	BI	21
(42)	Son et al. (2012)	Korea	2012	2007–2011	OCS (R)	21	42	D, P, T	D1+b, D2	BI, BII, RY	19
(43)	Son et al. (2014)	Korea	2014	2003–2010	OCS (P)	51	58	T	D2	RY	22
(44)	Suda et al. (2015)	Japan	2015	2009–2012	OCS (R)	88	438	D, T	D1+a/b, D2	BI, BII, RY	22
(45)	Tian et al. (2022)	China	2022	2014–2019	OCS (P)	463	877	T, ST	D1+, D2	BI, BII, RY	22
(46)	Uyama et al. (2012)	Japan	2012	2009–2010	OCS (P)	25	225	D	D2	BI	21
(47)	Wang et al. (2019)	China	2018	2016–2018	OCS (P)	223	223	D, T	D2	BII, RY	23
(48)	Woo et al. (2011)	Japan	2011	2005–2009	OCS (P)	236	591	D, T	D1+a/b, D2	BI, BII, RY	23
(49)	Yang et al. (2017)	Korea	2017	2009–2015	OCS (P)	173	511	D, T	D1+a/b, D2	BI, BII, RY	21
(50)	Yang et al. (2020)	China	2020	2010–2017	OCS (P)	126	257	T	D2	RY	22
(51)	Ye et al. (2020)	China	2020	2014–201	OCS (R)	325	358	D	D2	BI, BII, RY	21
(52)	Yoon et al. (2012)	Korea	2011	2009–2011	OCS (R)	36	65	T	D1+a/b, D2	BI, BII	23
(53)	Zheng-Yan et al. (2021)	China	2020	2010–2019	OCS (P)	519	957	D	D1, D2	BI, BII, RY	22

BI, Billroth I; BII, Billroth II; D, distal; EGJ, esophagogastric junction; EJJ, esophagojejunostomy; GG, gastro-gastro anastomosis; LG, laparoscopic gastrectomy; LND, lymphadenectomy; MINORS, Methodological Index for Non-Randomized Studies; NA, not available; OCS, observational clinical study; P, prospectively collected data; P, proximal; PCD, prospectively collected data; PPG, pylorus-preserving gastrectomy; R, retrospectively collected data; RG, robotic gastrectomy; RY, Roux-en-Y; ST, subtotal; T, total.

Table 2.

Patients' Characteristics

No.	Author (year)	Year	Age (RG)		Age (LG)		Sex (RG)			Sex (LG)
No.	Author (year)	Year	Mean	SD	Mean	SD	M	F	Pt	M	F	Pt
(1)	Aktas et al. (2020)	2020	55	8	59	10.5	18	12	30	41	23	64
(2)	Alhossaini et al. (2020)	2019	54	15	60	15	17	8	25	22	8	30
(3)	Cianchi et al. (2016)	2016	73	10.25	74	11.75	14	16	30	19	22	41
(4)	Eom et al. (2012)	2011	52	11.5	57	11	21	9	30	41	21	62
(5)	Gao et al. (2022)	2022	60	11	60	11	284	126	410	301	109	410
(6)	Gao et al. (2019)	2018	60	10	59	11	121	42	163	201	138	339
(7)	Han et al. (2015)	2015	50	8	49	11	31	37	68	32	36	68
(8)	Hikage et al. (2022)	2022	72	10.25	71	12.5	26	10	36	46	12	58
(9)	Hong et al. (2016)	2016	53	11	55	13	154	78	232	156	76	232
(10)	Huang et al. (2014)	2014	67	15	66	13	40	32	72	42	31	73
(11)	Hyun et al. (2013)	2013	54	12	60	12	25	13	38	55	28	83
(12)	Isobe et al. (2021)	2021	70	1	70	1	31	19	50	34	16	50
(13)	Junfeng et al. (2014)	2014	54	10	55	11	90	30	120	276	118	394
(14)	Kang et al. (2012)	2012	53	12	58	12	63	37	100	191	91	282
(15)	Kim et al. (2016a)	2013	55	13	61	11	103	69	172	294	187	481
(16)	Kim et al. (2014)	2016	53	11	56	11	113	72	185	113	72	185
(17)	Kim et al. (2012)	2012	54	12	58	12	265	171	436	550	311	861
(18)	Kim et al. (2010)	2010	53	15	57	13	10	6	16	10	1	11
(19)	Kim et al. (2016b)	2015	54	12	60	11	46	41	87	170	118	288
(20)	Kong et al. (2020)	2020	58	11	59	10	197	69	266	383	149	532
(21)	Lee et al. (2015)	2015	53	13	59	11	85	48	133	154	113	267
(22)	Liu et al. (2018)	2018	58	2.83	58	2.5	79	21	100	101	34	135
(23)	Li et al. (2018)	2018	55	11	56	11	78	34	112	79	33	112
(24)	Lu et al. (2018)	2018	NA	NA	NA	NA	73	28	101	212	91	303
(25)	Nakauchi et al. (2016)	2016	64	8.67	68	9	48	36	84	307	130	437
(26)	Nishi et al. (2022)	2022	67	12	67	11	62	21	83	243	125	368
(27)	Noshiro et al. (2014)	2014	66	10	69	12	14	7	21	102	58	160
(28)	Obama et al. (2018)	2017	54	12	59	11	189	126	315	327	198	525
(29)	Okabe et al. (2021)	2021	69	8	70	7.83	62	31	93	57	36	93
(30)	Okumura et al. (2016)	2016	NA	NA	NA	NA	227	143	370	83	49	132
(31)	Omori et al. (2022)	2022	66	1	66	1	152	58	210	153	57	210
(32)	Parisi et al. (2017)	2017	68	12	65	14	70	81	151	66	85	151
(33)	Park et al. (2015)	2015	54	11	58	11	75	70	145	369	243	612
(34)	Pugliese et al. (2010)	2010	NA	NA	NA	NA	NA	NA	16	NA	NA	48
(35)	Roh et al. (2020)	2020	58	11	58	11	27	24	51	27	24	51
(36)	Roh et al. (2021)	2021	54	12	55	13	42	32	74	42	32	74
(37)	Ryan et al. (2020)	2020	65	12	65	12	449	182	631	906	356	1262
(38)	Seo et al. (2015)	2014	51	4	55	5	19	21	40	20	20	40
(39)	Shen et al. (2016)	2016	56	10	57	11	75	18	93	249	81	330
(40)	Shibasaki et al. (2020)	2020	67	9.83	70	5	233	126	359	740	302	1042
(41)	Song et al. (2009)	2008	51	12	55	5	8	12	20	13	7	20
(42)	Son et al. (2012)	2012	52	13	52	13	14	7	21	26	16	42
(43)	Son et al. (2014)	2014	55	12	58	12	23	28	51	36	22	58
(44)	Suda et al. (2015)	2015	68	9	64	11.5	51	37	88	307	131	438
(45)	Tian et al. (2022)	2022	59	11	60	10	330	126	456	310	146	456
(46)	Uyama et al. (2012)	2012	61	11	62	9	14	11	25	156	69	225
(47)	Wang et al. (2019)	2018	57	10	57	11	183	40	223	180	43	223
(48)	Woo et al. (2011)	2011	54	12	58	11	136	100	236	364	227	591
(49)	Yang et al. (2017)	2017	NA	NA	NA	NA	98	75	173	335	176	511
(50)	Yang et al. (2020)	2020	60	9	61	9	105	21	126	100	26	126
(51)	Ye et al. (2020)	2020	57	8	57	9	189	96	285	186	99	285
(52)	Yoon et al. (2012)	2011	53	11	56	12	18	18	36	31	34	65
(53)	Zheng-Yan et al. (2021)	2020	55	10	55	12	354	162	516	333	184	516

F, female; LG, laparoscopic gastrectomy; M, male; NA, not available; Pt, patients; RG, robotic gastrectomy; SD, standard deviation.

Quality assessment

In our meta-analysis, we used the MINORS (Methodological Index for Non-Randomized Studies) scale to assess the quality and individual risk of bias of our nonrandomized studies. The final version of the MINORS scale comprises 12 items, which identify whether the included studies contained a clearly stated aim, included all potentially fit patients, involved prospective collection data, had appropriate endpoints according to the aim of the study, had blind evaluation of objectives and subjective endpoints, had an appropriate follow-up period, loss of follow-up under 5%, and prospective calculation of the study size. Furthermore, the MINORS scale also evaluates additional criteria for comparative studies such as the control group, the time period of both groups, their baseline equivalence, and an adequate statistical analysis. Each item is scored as 0 (not reported), 1 (reported, but inadequate), or 2 (report and adequate). The total score, in comparative studies, is 24 points.¹³

Statistical analysis

We performed our meta-analysis using Review Manager (Version 5.4.1).

For dichotomous outcomes, we presented the results as risk ratio (RR) with 95% confidence intervals (CIs), by using the Mantel-Haenszel method. For continuous outcomes, we presented the results as mean differences (MD) with 95% CI, by using the generic inverse variance method. Some studies presented their outcomes as median and range. Therefore, we applied a method described by Hozo et al.¹⁴ to estimate the mean and standard deviation. We used an alpha (α) level of 0.05 for statistical significance. The Chi-squared (χ²) test and the I-squared (I²) measure were used to assess heterogeneity. We applied a random effects model because of the clinical heterogeneity of included studies. We assessed the existence of publication bias among included studies using funnel plots, provided as Supplementary File S1.

Subgroup analysis

In our systematic review, 22 studies used propensity score matching (PSM) to minimize baseline differences that usually contribute to bias in the interpretation of results. The remaining 31 studies did not perform PSM. Hence, we conducted a subgroup analysis to understand whether PSM had any effect in the association between the surgical approach and the studied outcomes.

Results

Studies selected and characteristics

We selected 2848 articles from our research on PubMed, Web of Science and Cochrane Library. After reading their titles and abstracts, we selected 82 full-text articles to assess for eligibility. No additional study from other sources was deemed relevant. From these articles, we excluded 29 because they did not fulfill the inclusion criteria. Then, for our systematic review, we included 53 studies in the quality assessment and quantitative analysis (Fig. 1). These studies include a total of 25,521 participants, of which 8154 underwent RG and 17,367 underwent LG. All studies were retrospective observational studies.^15–67

FIG. 1.

Flow diagram according to the PRISMA guidelines. PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

Quality assessment

The median score in the MINORS scale was 22, with a range of 19–23. Therefore, all included studies were considered adequate to be included in the quantitative analysis.

Meta-analysis

A synthesis of every meta-analytical measure is presented in Table 3. We provide the results of each individual meta-analysis as forest plots in Supplementary File S2.

Table 3.

Results of the Meta-Analysis

Outcomes	No. of studies	No. of patients		Overall effect size (MD1/RR)	95% CI of overall effect	P	Heterogeneity (I², P)
Outcomes	No. of studies	RG	LG	Overall effect size (MD1/RR)	95% CI of overall effect	P	Heterogeneity (I², P)
Surgical outcomes
Operative time	50	6950	11,651	41.19	33.47 to 48.92	<.00001	I² = 98%, P < .00001
Blood loss	46	6734	11,856	19.43	−25.23 to −13.62	<.00001	I² = 92%, P < .00001
Conversion	33	4390	7730	0.68	0.43 to 1.07	.09	I² = 0%, P = .50
Reoperation	18	2677	4366	0.89	0.59 to 1.34	.57	I² = 0%, P = .72
Mortality	39	6708	10,776	1.20	0.81 to 1.77	.37	I² = 0%, P = .98
Perioperative outcomes
Length of hospital stay	52	7621	12,953	−0.50	−0.79 to −0.21	.0007	I² = 85%, P < .00001
Time to first flatus	25	4002	5623	−0.52	−0.55 to −0.50	<.00001	I² = 98%, P < .00001
Time to oral intake	27	4602	6296	−0.17	−0.25 to −0.08	.0001	I² = 53%, P = .0008
Overall complications	51	6732	11,469	0.93	0.85 to 1.03	.15	I² = 18%, P = .14
Surgical complications	31	5464	7303	0.68	0.57 to 0.82	<.0001	I² = 7%, P = .35
Anastomotic leakage	33	5289	8721	1.06	0.78 to 1.45	.71	I² = 16%, P = .21
Pancreatic complications	21	3445	5497	0.51	0.31 to 0.83	.007	I² = 0%, P = .60
Cost	8	1683	2184	3684.27	2986.11 to 4382.44	<.00001	I² = 90%, P < .00001
Oncological outcomes
Distal resection MD2	14	2184	3973	0.16	−0.19 to 0.51	.37	I² = 76% P < .00001
Proximal resection MD2	15	2235	4031	0.06	−0.05 to 0.18	.29	I² = 0%, P = .52
Recurrence	11	1358	2024	0.95	0.77 to 1.17	.61	I² = 0%, P = .91
No. of retrieved lymph nodes	49	7292	11,622	1.69	0.68 to 2.70	.001	I² = 93% P < .00001

CI, confidence interval; LG, laparoscopic gastrectomy; MD1, mean difference; MD2, margin distance; RG, robotic gastrectomy; RR, risk ratio.

Surgical outcomes

Operative time

Our meta-analysis included 50 studies, which reported the operation time. It was significantly shorter in the LG group, when compared with the robotic surgery group (MD 41.19, P < .00001 [95% CI: 33.47 to 48.92], I² = 98%, P < .00001). Mean operation time was 269.22 minutes in the robotic surgery group and 225.65 in the laparoscopic surgery group (Fig. 2).

FIG. 2.

Operative time.

Blood loss

Blood loss was reported in 46 studies. The mean blood loss was 90.72 mL in the RG group and 108.2 mL in the LG group. This difference was statistically significant (MD −19.43, P < .00001 [95% CI: −25.23 to −13.62], I² = 92% P < .00001).

Conversion

This outcome was included in 33 studies and demonstrated no statistically significant difference between the 2 groups (RR 0.68, P = .09 [95% CI: 0.43 to 1.07], I² = 0%, P = .50). Conversion rate to open surgery was 0.59% (26/4390) in the RG group and 0.89% (69/7730) in the LG group.

Reoperation

Eighteen studies reported reoperation rate. There was no statistically significant difference between both surgical approaches, regarding reoperation (RR 0.89, P = .57 [95% CI: 0.59 to 1.34], I² = 0%, P = .72). Reoperation rate was 1.38% (37/2677) in the RG group and 1.56% (68/4366) in the LG group.

Mortality

Thirty-nine studies were included, and mortality was comparable between both groups (RR 1.20, P = .37 [95% CI: 0.81 to 1.77], I² = 0%, P = .98). Mortality rate was 0.6% (40/6708) in the RG group and 0.59% (64/10,776) in the LG group (Fig. 3).

FIG. 3.

Mortality.

Postoperative outcomes

Length of hospital stay

This outcome was reported in 52 studies. The mean length of hospital stay was 8.74 days in the robotic surgery group and 9.38 days in the laparoscopic surgery group. The robotic surgery group displayed a significantly shorter hospital stay (MD −0.50, P = .0007 [95% CI −0.79 to −0.21], I² = 85% P < .00001).

Time to first flatus

There were 25 studies that reported time to first flatus. The robotic surgery group showed a significantly shorter time to first flatus (MD −0.52, P < .00001 [95% CI −0.55 to −0.50], I² = 98% P < .00001).

Time to oral intake

Twenty-seven studies included this outcome. Time to oral intake was significantly shorter in the robotic surgery group (MD −0.17, P = .0001 [95% CI −0.25 to −0.08], I² = 53% P = .0008).

Overall complications

The overall complication rate was 12.97% (873/6732) in the RG group and 13.11% (1504/11,469) in the LG group. There were 51 studies reporting this outcome, and the meta-analysis did not demonstrate a statistically significant difference (RR 0.93, P = .15 [95% CI 0.85 to 1.03], I² = 18%, P = .14).

Surgical complications (grade ≥III in the CD classification)

Thirty-one studies reported this outcome. Our study showed that the robotic surgery group had a significantly lower number of surgical complications (RR 0.68, P < .0001 [95% CI 0.57 to 0.82], I² = 7%, P = .35), with a rate of 3.88% (212/5464) in the RG group and 6.4% (467/7303) in the LG group (Fig. 4).

FIG. 4.

Surgical complications (Grade ≥III in the Clavien-Dindo classification).

Anastomotic leakage

Thirty-three studies included this outcome. The rate of anastomotic leakage was 1.72% (91/5289) in the RG group and 1.93% (168/8721) in the LG group. This difference was not significant (RR 1.06, P = .71 [95% CI 0.78 to 1.45], I² = 16%, P = .21).

Pancreatic complications

This outcome was included in 21 studies. The rate of pancreatic complications was 0.64% (22/3445) in the RG group and 1.42% (78/5497) in the LG group. This difference was statistically significant (RR 0.51, P = .007 [95% CI 0.31 to 0.83], I² = 0%, P = .60) (Fig. 5).

FIG. 5.

Pancreatic complications.

Cost

Cost was reported in eight studies. On average, the total cost of robotic surgery was 3684.27 U.S. dollars (3442.99 Euros), significantly higher compared with laparoscopic surgery (MD 3684.27, P < .00001 [95% CI 2986.11 to 4382.44], I² = 90% P < .00001) (Fig. 6).

FIG. 6.

Cost.

Oncological outcomes

Distal resection margin distance

Fourteen studies reported this outcome. The mean distal resection margin distance was 6.9 cm in the robotic surgery group and 6.82 cm in the laparoscopic surgery group. The difference was not statistically significant (MD 0.16, P = .37 [95% CI −0.19 to 0.51], I² = 76% P < .00001).

Proximal resection margin distance

Fifteen studies reported this outcome. The mean proximal resection margin distance was 4.35 cm in RG and 4.24 cm in LG. The difference was not statistically significant (MD 0.06, P = .29 [95% CI −0.05 to 0.18], I² = 0% P = .52).

Recurrence

Eleven studies reported this outcome. The recurrence rate was 9.9% (134/1358) in the RG group and 10.6% (215/2024) in the LG group. There was no statistically significant difference (RR 0.95, P = .61 [95% CI 0.77 to 1.17], I² = 0%, P = .91).

Number of retrieved lymph nodes

The number of retrieved lymph nodes was reported in 49 studies. The mean number of retrieved lymph nodes was 36.7 in the RG group and 35.61 in the LG group. The robotic surgery group had a significantly higher number of retrieved lymph nodes (MD 1.69, P = .001 [95% CI 0.68 to 2.70], I² = 93% P < .00001) (Fig. 7).

FIG. 7.

Number of retrieved lymph nodes.

Subgroup analysis

Surgical outcomes

Operative time

Both subgroups demonstrated a significantly longer operative time in the robotic surgery group. Heterogeneity was high and statistically significant. In addition, regarding subgroup differences, I² = 73.5% and P = .05 (Fig. 2).

Blood loss

There was significantly lower blood loss in the robotic surgery group in studies with and without PSM. This difference was more evident in the PSM subgroup. There was no significant difference between groups (I² = 0%, P = .76) and heterogeneity was similar.

Conversion

The PSM subgroup presented a stronger association between surgical approach and conversion rate, with the robotic surgery group being lower in both subgroups. However, neither subgroup had a statistically significant result (P = .06 for studies with PSM and P = .61 for studies without PSM). There was no significant difference between subgroups (I² = 0%, P = .63) and no significant heterogeneity in either.

Reoperation

The subgroups showed opposite results, both without statistical significance. Inside each subgroup, heterogeneity was not significant. There was no significant difference between subgroups either (I² = 68.4%, P = .08).

Mortality

There was no significant difference between subgroups (I² = 0%, P = .98) and neither displayed significant heterogeneity. Both favor the laparoscopic surgery group, although these results are not statistically significant (Fig. 3).

Postoperative complications

Length of hospital stay

The PSM subgroup displayed significantly lower length of hospital stay in the robotic surgery group, whereas there was no significant difference in studies without PSM, despite both favoring the robotic surgery group. Heterogeneity in both subgroups was significantly high. Between subgroups, there was no significant difference, with I² = 0%, P = .84.

Time to first flatus

Both subgroups showed a significantly shorter time to first flatus in the robotic surgery group, although there was significant heterogeneity. There was a significant difference between subgroups (I² = 99.8%, P < .00001). The PSM subgroup displayed lower heterogeneity.

Time to oral intake

The robotic surgery group had significantly lower time to oral intake in both subgroups. Heterogeneity was significant in the non-PSM subgroup (I² = 71%, P = .0008) There was no significant difference between subgroups (I² = 0%, P = .32).

Overall complications

There was no significant difference in either subgroup. The PSM subgroup favored the robotic surgery group, but P = .06. Differences between subgroups were not statistically significant (I² = 56%, P = .13).

Surgical complications (grade ≥III in the CD classification)

The PSM subgroup demonstrated a significantly lower rate of surgical complications in the robotic surgery group when compared to the laparoscopic surgery group (3.9% and 5.76%, respectively; RR = 0.66, P < .0001). In addition, both subgroups revealed low heterogeneity and there was no significant difference between them (I² = 0%, P = .97) (Fig. 4).

Anastomotic leakage

In the PSM subgroup, anastomotic leakage was lower in the robotic surgery group. However, the results were not statistically significant (RR = 0.73; P = .11). In both subgroups, heterogeneity was not significant. The differences between them were statistically significant (I² = 80.8%, P = .02), as they showed opposite results.

Pancreatic complications

Both subgroups favored the robotic surgery group, but the results were not statistically significant. There was no significant heterogeneity. Moreover, the 2 subgroups were similar (I² = 0%, P = .64) (Fig. 5).

Cost

Both subgroups significantly favored laparoscopic surgery. Heterogeneity was high and significant in both subgroups. There was no significant difference between subgroups (I² = 4.4%, P = .31) (Fig. 6).

Oncological outcomes

Distal and proximal resection margin distances

Regarding distal resection margin, both subgroups were similar (I² = 0%, P = .73). In studies without PSM, there was significant heterogeneity (I² = 85%, P < .00001). For the proximal resection margin, there was no significant difference between subgroups (I² = 23.6%, P = .25) and neither subgroup displayed significant heterogeneity.

Recurrence

None of the subgroups showed a significant difference in recurrence rate between the two approaches, and heterogeneity was not significant. There was no significant difference between subgroups (I² = 0%, P = .36).

Number of harvested lymph nodes

The 2 subgroups showed a significantly higher number of retrieved lymph nodes in the robotic surgery group. They appeared to be similar concerning subgroup differences (I² = 0%, P = 1.00), and they both showed high values of heterogeneity, individually (Fig. 7).

Discussion

This meta-analysis, which, as far as we know, is the largest one on the subject so far, provides insights into the comparison of short-term outcomes between robotic and laparoscopic gastrectomies in patients with gastric cancer. Marano et al.⁹ aggregated 14 meta-analyses published until December 2019 and showed better results in favor of robotic surgery, regarding blood loss, length of hospital stay, recovery of bowel function, distal resection margin distance, and number of retrieved lymph nodes. However, not all represented an acceptable level of evidence, concerning the high percentage of heterogeneity of some outcomes. Hence, it is still unclear if RG is more feasible and safer than LG.

Our results demonstrated that both surgical techniques are similarly effective in term of conversion rate, reoperation rate, mortality, overall complications, anastomotic leakage, distal and proximal resection margin distances, and recurrence rate.

Operative time and cost favor the laparoscopic approach, while blood loss, length of hospital stay, time to first flatus, time to oral intake, surgical complications (CD grade ≥III), pancreatic complications, and the number of retrieved lymph nodes favor the robotic approach.

Surgical outcomes

Operative time

This meta-analysis shows a similar result to previous studies, which demonstrated that operative time is significantly longer in RG when compared with LG.^9,11,12

Some studies have suggested that the learning curve associated with the use of robotic technology and the need for instrument exchange during the procedure may contribute to the longer operative time seen in the robotic surgery group.⁶⁸

As Gong et al.⁸ refer, the majority of studies did not discriminate the several steps of the surgery, regarding the operative time. Nishi et al.⁴⁰ and Ye et al.⁶⁵ divided the operative time into different steps of the surgery, which demonstrated that robotic surgery is not inferior regarding the effective operative time. However, the total operative time, which includes the effective time and “junk time” (setup, docking, and adjustment of surgical instruments), remains longer in robotic surgery due to the latter.^65,69

There were two studies demonstrating a shorter operative time in the robotic surgery group, one of them (Omori) with a statistically significant difference.^40,45 Omori et al.⁴⁵ applied relevant techniques to shorten the “junk” time, such as the standardization of the setup and the use of MBS and SPIDER techniques, which reduce pancreatic manipulation during lymphadenectomy.

So the early standardization of the setup as well as the surgical team's experience could contribute to similar results between both technical approaches.^26,40 On the other hand, there appear to be more possible factors that influence the operative time, rather than the docking time,⁴⁶ such as the more accurate and delicate lymphadenectomy provided by the robotic platform.^15,45

Blood loss

The mean blood loss was significantly lower in the robotic surgery group, compared to the laparoscopic surgery group. This result was also observed in previous systematic reviews.⁹ The majority of studies included in our meta-analysis demonstrates a tendency to lower blood loss in robotic surgery. However, there were some studies that showed the opposite and stated that robotic surgery still has some instrumental limitations.^22,55

The reasons for the significant difference in intraoperative blood loss could be due to reduction of the physiologic tremor, increased surgical field with 3D view, which provides greater instrument dexterity, and more precise and less damaging dissection. These allow for a more accurate lymphadenectomy, less blood loss, less pancreatic damage, and less muscle trauma.^65,70

Conversion/reoperation/mortality

Conversion, reoperation, and mortality were found to be comparable between the 2 groups. There was a tendency to favor the robotic surgery group, regarding conversion and reoperation, and previous studies also presented similar results with no statistically significant difference.^8,11,12 There were four studies that demonstrated more cases of conversion to open gastrectomy in the robotic surgery group, with the following causes: intra-abdominal bleeding, serosa involvement, massive abdominal adhesion, damage to adjacent organs with the insertion of trocars, inadequate surgical margins, and anatomical and dissection difficulties.^20,33,47,48 Some studies reported the causes of reoperation, such as anastomotic or intra-abdominal bleeding, pancreatic complications (postoperative pancreatic fistula), and intestinal obstruction.^34,65

The mortality rate was also found to be similar between the 2 groups. This holds true in this study, with the laparoscopic surgery group displaying a mortality of 0.59%, and the robotic surgery group displaying a value of 0.60%. These findings are consistent with previous studies.⁹

Perioperative outcomes

Length of hospital stay/time to first flatus/time to oral intake

The length of hospital stay, time to first flatus, and time to oral intake are outcomes associated with a faster recovery, as well as lower probability of intrahospital complications and better patient well-being.

This study showed significant results favoring robotic surgery, which appears to cause less damage to adjacent organs, less blood loss, and fewer postoperative complications. This finding supports the intrinsic advantages of the robotic platform, resulting in less trauma and, therefore, shorter time to recovery.

The mean of length of hospital stay was 8.74 days in the robotic surgery group and 9.38 days in the laparoscopic surgery group. Similar results can be seen in Hu et al., without significant heterogeneity.⁷¹

In fact, Liu et al. correlate the shorter hospital stay in the robotic surgery group with a better bowel function recovery and a faster shift from liquid to soft diet. In addition, the surgical operation area and the inflammatory response can influence gastrointestinal recovery, due to surgical manipulation of internal organs.^37,65 Moreover, Guerrini et al. referred the importance of early oral feeding in accelerating the recuperation process.¹²

Overall complications

Regarding overall complications, they did not differ considerably between both surgical approaches, despite a tendency for lower overall complications in the robotic surgery group. These results were also observed in other meta-analyses.^8,12 However, Jin et al. claimed to be the first meta-analysis to demonstrate fewer overall complications in the robotic surgery group with statistical significance.¹¹ Nevertheless, the possible cause of this observation remains unclear. They still add that this could be related with the statistically significant result in pancreatic complications.¹¹

Omori et al. demonstrated, by multivariate analysis, that laparoscopic surgery is an independent risk factor for postoperative complications.⁴⁵

Surgical complications (grade ≥III in the CD classification)

Several studies applied the CD classification to highlight the most severe complications, which have the most impact in postoperative morbidity and mortality. In fact, Guerrini et al. emphasized the importance of separate medical and surgical complications, because of a direct relation between surgical complications and postoperative recovery and prognosis.¹² Tian et al. showed that surgical complications, CD grade III–IV, are independent prognostic factors for both overall survival and relapse-free survival.⁵⁹

Furthermore, Hikage et al. established, according to their multivariate analysis, that laparoscopic surgery is an independent risk factor for postoperative complications with a CD grade of III or higher.²² In this article, these surgical complications were significantly lower in the robotic surgery group, with only 7% heterogeneity (P = .35). The rates of the surgical complications were 3.88% in the robotic surgery group and 6.39% in the laparoscopic surgery group. These observations are consistent with those of Guerrini's meta-analysis. However, our results presented slightly lower rates of surgical complications.¹² Hence, RG results in less relevant morbidity.

Anastomotic leakage

This study did not show a statistically significant difference in anastomotic leakage, which is congruent with previous studies.¹²

Pancreatic complications

Pancreatic morbidity is relatively rare. Nevertheless, it represents a real threat to the patient.⁷² One of the main concerns of gastrectomy is pancreatic manipulation during lymphadenectomy.⁵⁸

Jin et al. and Gong et al. showed that pancreatic complications were significantly lower in the robotic surgery group.^8,11 These results are consistent with our meta-analysis. In addition, Jin et al. discuss the influence of the extension of lymphadenectomy on pancreatic complications as an unexpected inverse relationship between the number of harvested lymph nodes and pancreatic morbidity.¹¹ In fact, these results support the efficacy and efficiency of the abovementioned characteristics of robotic surgery, which lead to minimization of pressure on the pancreas, as well as reduction on parenchymal injury.^16,58,72

Omori et al. used the SPIDER and MBS techniques to optimize the removal of suprapancreatic lymph nodes with an internal organ retractor, which held the pancreas, and a bipolar soft-coagulation forceps, which minimizes thermal damage.⁴⁵

Cost

The cost of robotic surgery remains an important drawback to this technique. On average, the total cost of robotic surgery was 3684.27 U.S. dollars (3442.99 Euros), significantly higher compared with laparoscopic surgery. Our meta-analysis includes 8 studies that reach the same conclusion: that the cost of the laparoscopic surgery is significantly lower, compared to that of robotic surgery.^9,12

Some studies suggest that the fewer postoperative complications and the faster recovery and hospital stay can compensate for the higher costs associated with robotic surgery.^9,59 Moreover, other studies predict a reduction in the cost of robotic surgery over time with an increase in competition and technological improvement.^12,19,34

Oncological outcomes

Distal and proximal resection margin distances

Our systematic review mainly includes studies on short-term outcomes. Therefore, it becomes difficult to analyze oncological variables, which demand a longer follow-up. To overcome this problem, we used distal and proximal resection margin distances as predictors for oncologic prognosis.¹²

This article did not show a significant difference in either resection margin distance, but there was a small tendency to favor the robotic approach. The mean distal resection margin distance was 6.9 cm in the robotic surgery group and 6.82 cm in the laparoscopic surgery group. Regarding the proximal resection margin distance, RG had a mean of 4.35 cm and LG had a mean of 4.24 cm.

Recurrence

Overall, the recurrence rate was comparable between the robotic and laparoscopic techniques (9.9% and 10.6%, respectively), although it appears to be lower in the robotic surgery group. Only one of the recent included studies analyses recurrence, particularly within 5 years after surgery, and it reported 7 cases of recurrence in 58 patients who underwent LG and 3 cases in 36 patients who underwent RG, with no locoregional recurrence in the robotic surgery group.²² Han et al.²¹ did not report any case of recurrence and the mean follow-up for both surgical groups was <2 years, when recurrence is more common.⁷³ In fact, recurrence rate can happen in more than half of gastric cancer patients after surgical treatment.^74,75 Furthermore, lymphovascular invasion, lymph node metastases, and tumor stage are independent risk factors of early recurrence (≤12 months) after curative resection.⁷⁶

Number of harvested lymph nodes

Lymphadenectomy is part of the standard treatment, and it is one of the main steps of the surgery, regarding the difficulty on managing and dissecting around critical organs, such as the pancreas, and an important predictor of the oncological prognosis, as they determine the extent of the tumor, according the TNM classification.

In our meta-analysis, the number of retrieved lymph nodes was significantly higher in the robotic surgery group, when compared with the laparoscopic surgery group, as demonstrated in previous meta-analysis.^8,11,12 All of these studies, including ours, showed a significant heterogeneity, which puts the external validity of their results into question.

In fact, some studies^40,59 revealed a significantly higher number of harvested lymph nodes in the robotic surgery group, particularly caused by the retrieval of the suprapancreatic lymph nodes.⁵⁹ They attribute these results to the better surgical field, with 3D vision and endowrist movements, and the reduction of the surgeon's physiologic tremor that the robotic platform provides.^40,59 Moreover, these differences were more evident in advanced gastric cancer⁵⁹ and Jin et al. demonstrated a preference for performing robotic surgery in patients whose body mass index was under 25 kg/m², whose age was under 65, and who had a tumor with a longest diameter above 5 cm.¹¹

Several studies defined that an adequate number of retrieved lymph nodes was more than 15.^34,49–51 Roh et al.⁴⁹ showed that there was an inadequate number of retrieved lymph nodes (<16) in the laparoscopic surgery group and the surgical success, which included this outcome, was significantly higher in the robotic surgery group. Nevertheless, it remained unclear what the real cause of these results was. This robotic surgery had a firefly system that was used for achieving a real-time fluorescence image, during lymphadenectomy, to detect lymphatic drainage and optimize the dissection and retrieval of lymph nodes with more accuracy.

On the other hand, despite the good results of the SPIDER and MBS techniques in reducing pancreatic damage, Omori et al.⁴⁵ found that laparoscopic and robotic surgeries are comparable, concerning the number of retrieved lymph nodes, as shown in a randomized control trial.⁷⁷ In opposition, another randomized clinical trial (RCT) described a significantly higher number of harvested lymph nodes.⁷⁸

Subgroup analysis

There were significant subgroup differences in the following outcomes: operative time, time to first flatus, and anastomotic leakage. Regarding operative time, while both subgroups favored robotic surgery, studies without PSM showed more pronounced differences.

The MD of time to first flatus was higher in the non-PSM subgroup, when compared to that of the PSM subgroup. However, the first subgroup showed higher heterogeneity. These findings demonstrated that PSM reduced both heterogeneity and difference between the robotic and laparoscopic surgery groups. The same happened in the following outcomes: conversion, time to oral intake, surgical complications (CD Grade ≥III), cost, and distal resection margin distance. Therefore, this method allows a better understanding of each comparison and a more accurate approximation of reality.

Concerning anastomotic leakage, the significant subgroup differences appear to be due to opposite results. The meta-analysis showed that, in the PSM subgroup, there is a tendency for lower anastomotic leakage when performing robotic surgery. There were other outcomes, which also showed results favoring robotic surgery in the PSM subgroup, in comparison with those in the non-PSM subgroup, such as blood loss, reoperation, overall complications, proximal resection margin distance, and recurrence. However, none of these outcomes demonstrated any significant difference between subgroups.

There were also outcomes where the PSM method did not reduce the heterogeneity of included studies. In fact, there were higher values of heterogeneity in the PSM subgroup regarding operative time, length of hospital stay, overall complications, pancreatic complications, and number of retrieved lymph nodes.

In addition, length of hospital stay and surgical complications with a CD Grade ≥III showed a significant difference only in the PSM subgroup.

On the one hand, PSM subgroups were more consistent and did not emphasize the differences between both surgical approaches. On the other hand, in certain outcomes, these subgroups demonstrated results that were more supportive of robotic surgery, highlighting its advantages when compared with laparoscopic surgery.

The demographic characteristics of people who underwent PSM were not equal in every study. Therefore, it is still possible that there are variables that did not undergo PSM and are affecting the validity of the results, in terms of heterogeneity.

This study also has some limitations: first, we included nonrandomized comparative studies; second, several outcomes demonstrated a high percentage of heterogeneity, which may put the validity of results into question. These differences between studies could be explained by discrepancies in the surgical team's experience in performing robotic surgery; third, about half of the studies included did not perform PSM, contributing to the influence of confounding factors on the results and conclusions about the outcomes in study; fourth, there was one article that we could not access, resulting in a slight reporting bias; fifth, the majority of the included studies is from Southeast Asia (Japan, China, and Korea), which may not be representative of the global reality; and sixth, postoperative inflammatory reaction and drain amylase levels, which could improve the assessment of pancreatic damage, were not included.

Conclusion

In conclusion, we believe that our results demonstrate RG is a safe and feasible procedure, when compared with LG.

Overall, robotic surgery presented better results regarding blood loss, length of hospital stay, time to first flatus, time to oral intake, relevant surgical complications, pancreatic complications, and the number of retrieved lymph nodes. However, operative time and financial cost remain the main drawbacks to its widespread use. Further studies are needed to understand mechanisms to minimize these downsides, aiming for a more efficient use of the robotic platform in gastric cancer curative-intent surgery.

Moreover, randomized clinical trials are also desired in contemplation of a better comprehension of advantages in performing RG.

Footnotes

Authors' Contributions

P.L.: conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); validation (equal); visualization (lead); writing—original draft (lead); and writing—review and editing (equal). J.P.B.: data curation (equal); formal analysis (equal); investigation (supporting); resources (lead); supervision (supporting); validation (equal); visualization (supporting); writing—original draft (supporting); and writing—review and editing (equal). J.F.V.: investigation (equal) and validation (equal). J.B.: conceptualization (equal); investigation (supporting); supervision (lead); visualization (supporting); and writing—review and editing (supporting).

Disclosure Statement

The authors have no conflicts of interest to disclose.

Funding Information

No funding was received for this project.

Supplementary Material

References

World Cancer Research Fund. Stomach Cancer Statistics. 2020. Available from: https://www.wcrf.org/cancer-trends/stomach-cancer-statistics [Last accessed: February 20, 2023].

Ferlay

, Ervik

, Lam

, et al. Global Cancer Observatory: Cancer Today. International Agency for Research on Cancer: Lyon, France; 2020. Available from: https://gco.iarc.fr/today [Last accessed: February 20, 2023].

Chandra

, Balachandar

, Wang

, et al. The changing face of gastric cancer: Epidemiologic trends and advances in novel therapies. Cancer Gene Ther, 2021; 28(5):390–399; doi: 10.1038/s41417-020-00234-z

Thrift

, Nguyen

. Gastric cancer epidemiology. Gastrointest Endosc Clin N Am, 2021; 31(3):425–439; doi: 10.1016/j.giec.2021.03.001

Wang

, Zhang

, Yang

, et al. Progress of gastric cancer surgery in the era of precision medicine. Int J Biol Sci, 2021; 17(4):1041–1049; doi: 10.7150/ijbs.56735

Lordick

, Carneiro

, Cascinu

, et al. Gastric cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up. Ann Oncol, 2022; 33(10):1005–1020; doi: 10.1016/j.annonc.2022.07.004

Zhang

, Yamashita

, Zhang

, et al. Reevaluation of laparoscopic versus open distal gastrectomy for early gastric cancer in Asia: A meta-analysis of randomized controlled trials. Int J Surg, 2018; 56:31–43; doi: 10.1016/j.ijsu.2018.05.733

Gong

, Li

, Tian

, et al. Clinical efficacy and safety of robotic distal gastrectomy for gastric cancer: A systematic review and meta-analysis. Surg Endosc, 2022; 36(5):2734–2748; doi: 10.1007/s00464-021-08994-x

Marano

, Fusario

, Savelli

, et al. Robotic versus laparoscopic gastrectomy for gastric cancer: An umbrella review of systematic reviews and meta-analyses. Updates Surg, 2021; 73(5):1673–1689; doi: 10.1007/s13304-021-01059-7

10.

Smyth

, Nilsson

, Grabsch

, et al. Gastric cancer. Lancet, 2020; 396(10251):635–648; doi: 10.1016/s0140-6736(20)31288-5

11.

Jin

, Liu

, Yang

, et al. Effectiveness and safety of robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: A meta-analysis of 12,401 gastric cancer patients. Updates Surg, 2022; 74(1):267–281; doi: 10.1007/s13304-021-01176-3

12.

Guerrini

, Esposito

, Magistri

, et al. Robotic versus laparoscopic gastrectomy for gastric cancer: The largest meta-analysis. Int J Surg, 2020; 82:210–228; doi: 10.1016/j.ijsu.2020.07.053

13.

Slim

, Nini

, Forestier

, et al. Methodological index for non-randomized studies (MINORS): Development and validation of a new instrument. ANZ J Surg, 2003; 73(9):712–716; doi: 10.1046/j.1445-2197.2003.02748.x

14.

Hozo

, Djulbegovic

, Hozo

. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol, 2005; 5:13; doi: 10.1186/1471-2288-5-13

15.

Aktas

, Aytac

, Bas

, et al. Totally minimally invasive radical gastrectomy with the da Vinci Xi((R)) robotic system versus straight laparoscopy for gastric adenocarcinoma. Int J Med Robot, 2020; 16(6):1–9; doi: 10.1002/rcs.2146

16.

Alhossaini

, Altamran

, Cho

, et al. Lower rate of conversion using robotic-assisted surgery compared to laparoscopy in completion total gastrectomy for remnant gastric cancer. Surg Endosc, 2020; 34(2):847–852; doi: 10.1007/s00464-019-06838-3

17.

Cianchi

, Indennitate

, Trallori

, et al. Robotic vs laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: A retrospective comparative mono-institutional study. BMC Surg, 2016; 16(1):65; doi: 10.1186/s12893-016-0180-z

18.

Eom

, Yoon

, Ryu

, 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(1):57–63; doi: 10.1016/j.ejso.2011.09.006

19.

Gao

, Liao

, Jiang

, et al. Surgical and oncological outcomes of robotic- versus laparoscopic-assisted distal gastrectomy with D2 lymphadenectomy for advanced gastric cancer: A propensity score-matched analysis of 1164 patients. World J Surg Oncol, 2022; 20(1):315; doi: 10.1186/s12957-022-02778-w

20.

Gao

, Xi

, Qiao

, et al. Comparison of robotic- and laparoscopic-assisted gastrectomy in advanced gastric cancer: Updated short- and long-term results. Surg Endosc, 2019; 33(2):528–534; doi: 10.1007/s00464-018-6327-5

21.

Han

, Suh

, Ahn

, 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(7):2323–2328; doi: 10.1245/s10434-014-4204-6

22.

Hikage

, Fujiya

, Kamiya

, et al. Comparisons of surgical outcomes between robotic and laparoscopic total gastrectomy in patients with clinical stage I/IIA gastric cancer. Surg Endosc, 2022; 36(7):5257–5266; doi: 10.1007/s00464-021-08903-2

23.

Hong

, Son

, Shin

, et al. Can robotic gastrectomy surpass laparoscopic gastrectomy by acquiring long-term experience? A propensity score analysis of a 7-year experience at a single institution. J Gastric Cancer, 2016; 16(4):240–246; doi: 10.5230/jgc.2016.16.4.240

24.

Huang

, Lan

, Fang

, et al. Comparison of the operative outcomes and learning curves between laparoscopic and robotic gastrectomy for gastric cancer. PLoS One, 2014; 9(10):e111499; doi: 10.1371/journal.pone.0111499

25.

Hyun

, Lee

, Kwon

, et al. Robot versus laparoscopic gastrectomy for cancer by an experienced surgeon: Comparisons of surgery, complications, and surgical stress. Ann Surg Oncol, 2013; 20(4):1258–1265; doi: 10.1245/s10434-012-2679-6

26.

Isobe

, Murakami

, Minami

, et al. Robotic versus laparoscopic distal gastrectomy in patients with gastric cancer: A propensity score-matched analysis. BMC Surg, 2021; 21(1):203; doi: 10.1186/s12893-021-01212-4

27.

Junfeng

, Yan

, Bo

, et al. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: Comparison of surgical performance and short-term outcomes. Surg Endosc, 2014; 28(6):1779–1787; doi: 10.1007/s00464-013-3385-6

28.

Kang

, Xuan

, Hur

, et al. Comparison of surgical outcomes between robotic and laparoscopic gastrectomy for gastric cancer: The learning curve of robotic surgery. J Gastric Cancer, 2012; 12(3):156–163; doi: 10.5230/jgc.2012.12.3.156

29.

Kim

, Han

, Yang

, et al. Multicenter prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg, 2016a;263(1):103–109; doi: 10.1097/sla.0000000000001249

30.

Kim

, Park

, Song

, et al. Rapid and safe learning of robotic gastrectomy for gastric cancer: Multidimensional analysis in a comparison with laparoscopic gastrectomy. Eur J Surg Oncol, 2014; 40(10):1346–1354; doi: 10.1016/j.ejso.2013.09.011

31.

Kim

, An

, Kim

, et al. Major early complications following open, laparoscopic and robotic gastrectomy. Br J Surg, 2012; 99(12):1681–1687; doi: 10.1002/bjs.8924

32.

Kim

, Heo

, Jung

. Robotic gastrectomy for gastric cancer: Surgical techniques and clinical merits. Surg Endosc, 2010; 24(3):610–615; doi: 10.1007/s00464-009-0618-9

33.

Kim

, Reim

, Park

, et al. Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer. Surg Endosc, 2016b;30(4):1547–1552; doi: 10.1007/s00464-015-4372-x

34.

Kong

, Cao

, Liu

, et al. Short-term clinical outcomes after laparoscopic and robotic gastrectomy for gastric cancer: A propensity score matching analysis. J Gastrointest Surg, 2020; 24(3):531–539; doi: 10.1007/s11605-019-04158-4

35.

Lee

, Kim

, Woo

, et al. 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(11):3251–3260; doi: 10.1007/s00464-015-4069-1

36.

, Li

, et al. Robotic versus laparoscopic gastrectomy with D2 lymph node dissection for advanced gastric cancer: A propensity score-matched analysis. Cancer Manag Res, 2018; 10:705–714; doi: 10.2147/cmar.S161007

37.

Liu

, Wang

, Li

, et al. Robotic versus conventional laparoscopic gastrectomy for gastric cancer: A retrospective cohort study. Int J Surg, 2018; 55:15–23; doi: 10.1016/j.ijsu.2018.05.015

38.

, Zheng

, Li

, 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(7):1152–1162; doi: 10.1007/s11605-018-3785-y

39.

Nakauchi

, Suda

, Susumu

, et al. Comparison of the long-term outcomes of robotic radical gastrectomy for gastric cancer and conventional laparoscopic approach: A single institutional retrospective cohort study. Surg Endosc, 2016; 30(12):5444–5452; doi: 10.1007/s00464-016-4904-z

40.

Nishi

, Shimada

, Yoshikawa

, et al. Propensity score-matched analysis of the short- and long-term outcomes of robotic versus laparoscopic gastrectomy for gastric cancer. Ann Surg Oncol, 2022; 29(6):3887–3895; doi: 10.1245/s10434-021-11203-7

41.

Noshiro

, Ikeda

, Urata

. Robotically-enhanced surgical anatomy enables surgeons to perform distal gastrectomy for gastric cancer using electric cautery devices alone. Surg Endosc, 2014; 28(4):1180–1187; doi: 10.1007/s00464-013-3304-x

42.

Obama

, Kim

, Kang

, et al. Long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer, 2018; 21(2):285–295; doi: 10.1007/s10120-017-0740-7

43.

Okabe

, Sunagawa

, Saji

, et al. Comparison of short-term outcomes between robotic and laparoscopic gastrectomy for gastric cancer: A propensity score-matching analysis. J Robot Surg, 2021; 15(5):803–811; doi: 10.1007/s11701-020-01182-4

44.

Okumura

, Son

, Kim

, 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(4):1125–1134; doi: 10.1007/s10120-015-0560-6

45.

Omori

, Yamamoto

, Hara

, et al. Comparison of robotic gastrectomy and laparoscopic gastrectomy for gastric cancer: A propensity score-matched analysis. Surg Endosc, 2022; 36(8):6223–6234; doi: 10.1007/s00464-022-09125-w

46.

Parisi

, Reim

, Borghi

, et al. Minimally invasive surgery for gastric cancer: A comparison between robotic, laparoscopic and open surgery. World J Gastroenterol, 2017; 23(13):2376–2384; doi: 10.3748/wjg.v23.i13.2376

47.

Park

, Ryu

, Reim

, 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(7):1789–1797; doi: 10.1007/s00268-015-2998-4

48.

Pugliese

, Maggioni

, Sansonna

, 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(10):2594–2602; doi: 10.1007/s00464-010-1014-1

49.

Roh

, Choi

, Seo

, et al. Comparison of surgical outcomes between integrated robotic and conventional laparoscopic surgery for distal gastrectomy: A propensity score matching analysis. Sci Rep, 2020; 10(1):485; doi: 10.1038/s41598-020-57413-z

50.

Roh

, Lee

, Son

, et al. Textbook outcome and survival of robotic versus laparoscopic total gastrectomy for gastric cancer: A propensity score matched cohort study. Sci Rep, 2021; 11(1):15394; doi: 10.1038/s41598-021-95017-3

51.

Ryan

, Tameron

, Murphy

, et al. Robotic versus laparoscopic gastrectomy for gastric adenocarcinoma: propensity-matched analysis. Surg Innov, 2020; 27(1):26–31; doi: 10.1177/1553350619868113

52.

Seo

, Shim

, Jeon

, et al. Postoperative pancreatic fistula after robot distal gastrectomy. J Surg Res, 2015; 194(2):361–366; doi: 10.1016/j.jss.2014.10.022

53.

Shen

, Xi

, Wei

, et al. Robotic versus laparoscopic gastrectomy for gastric cancer: Comparison of short-term surgical outcomes. Surg Endosc, 2016; 30(2):574–580; doi: 10.1007/s00464-015-4241-7

54.

Shibasaki

, Suda

, Nakauchi

, et al. Non-robotic minimally invasive gastrectomy as an independent risk factor for postoperative intra-abdominal infectious complications: A single-center, retrospective and propensity score-matched analysis. World J Gastroenterol, 2020; 26(11):1172–1184; doi: 10.3748/wjg.v26.i11.1172

55.

Son

S-Y

, Lee

C-M

, Ahn

S-H

, et al. Clinical outcome of robotic gastrectomy in gastric cancer in comparison with laparoscopic gastrectomy: A case-control study. J Minim Invasive Surg, 2012; 15,(2):27–31.

56.

Son

, Lee

, Kim

, et al. Robotic spleen-preserving total gastrectomy for gastric cancer: Comparison with conventional laparoscopic procedure. Surg Endosc, 2014; 28(9):2606–2615; doi: 10.1007/s00464-014-3511-0

57.

Song

, Kang

, Oh

, et al. Role of robotic gastrectomy using da Vinci system compared with laparoscopic gastrectomy: Initial experience of 20 consecutive cases. Surg Endosc, 2009; 23(6):1204–1211; doi: 10.1007/s00464-009-0351-4

58.

Suda

, Man

, Ishida

, et al. 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(3):673–685; doi: 10.1007/s00464-014-3718-0

59.

Tian

, Cao

, Kong

, et al. Short- and long-term comparison of robotic and laparoscopic gastrectomy for gastric cancer by the same surgical team: A propensity score matching analysis. Surg Endosc, 2022; 36(1):185–195; doi: 10.1007/s00464-020-08253-5

60.

Uyama

, Kanaya

, Ishida

, et al. Novel integrated robotic approach for suprapancreatic D2 nodal dissection for treating gastric cancer: Technique and initial experience. World J Surg, 2012; 36(2):331–337; doi: 10.1007/s00268-011-1352-8

61.

Wang

, Li

, Yu

, et al. Severity and incidence of complications assessed by the Clavien-Dindo classification following robotic and laparoscopic gastrectomy for advanced gastric cancer: A retrospective and propensity score-matched study. Surg Endosc, 2019; 33(10):3341–3354; doi: 10.1007/s00464-018-06624-7

62.

Woo

, Hyung

, Pak

, 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):1086–1092; doi: 10.1001/archsurg.2011.114

63.

Yang

, Shi

, Xie

, et al. Short-term outcomes of robotic- versus laparoscopic-assisted total gastrectomy for advanced gastric cancer: A propensity score matching study. BMC Cancer, 2020; 20(1):669; doi: 10.1186/s12885-020-07160-1

64.

Yang

, Roh

, Kim

, et al. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer. Ann Surg Oncol, 2017; 24(7):1770–1777; doi: 10.1245/s10434-017-5851-1

65.

, Shi

, Liu

, et al. Robotic- versus laparoscopic-assisted distal gastrectomy with D2 lymphadenectomy for advanced gastric cancer based on propensity score matching: Short-term outcomes at a high-capacity center. Sci Rep, 2020; 10(1):6502; doi: 10.1038/s41598-020-63616-1

66.

Yoon

, Kim

, Lee

, et al. Robot-assisted total gastrectomy is comparable with laparoscopically assisted total gastrectomy for early gastric cancer. Surg Endosc, 2012; 26(5):1377–1381; doi: 10.1007/s00464-011-2043-0

67.

Zheng-Yan

, Yong-Liang

, Feng

, et al. Morbidity and short-term surgical outcomes of robotic versus laparoscopic distal gastrectomy for gastric cancer: A large cohort study. Surg Endosc, 2021; 35(7):3572–3583; doi: 10.1007/s00464-020-07820-0

68.

Kim

, Kim

, Hyung

, et al. Comprehensive learning curve of robotic surgery: Discovery from a multicenter prospective trial of robotic gastrectomy. Ann Surg, 2021; 273(5):949–956; doi: 10.1097/sla.0000000000003583

69.

Liu

, Kinoshita

, Tonouchi

, et al. What are the reasons for a longer operative time in robotic gastrectomy than in laparoscopic gastrectomy for stomach cancer?. Surg Endosc, 2019; 33(1):192–198; doi: 10.1007/s00464-018-6294-x

70.

, Shi

, Liu

, et al. Robotic-assisted versus conventional laparoscopic-assisted total gastrectomy with D2 lymphadenectomy for advanced gastric cancer: Short-term outcomes at a mono-institution. BMC Surg, 2019; 19(1):86; doi: 10.1186/s12893-019-0549-x

71.

, Li

, Wang

, et al. Robotic versus laparoscopic gastrectomy for gastric carcinoma: A meta-analysis of efficacy and safety. Asian Pac J Cancer Prev, 2016; 17,(9):4327–4333.

72.

van Boxel

, Ruurda

, van Hillegersberg

. Robotic-assisted gastrectomy for gastric cancer: A European perspective. Gastric Cancer, 2019; 22(5):909–919; doi: 10.1007/s10120-019-00979-z

73.

Kang

, Meng

, Yu

, et al. Factors associated with early recurrence after curative surgery for gastric cancer. World J Gastroenterol, 2015; 21(19):5934–5940; doi: 10.3748/wjg.v21.i19.5934

74.

D'Angelica

, Gonen

, Brennan

, et al. Patterns of initial recurrence in completely resected gastric adenocarcinoma. Ann Surg, 2004; 240(5):808–816; doi: 10.1097/01.sla.0000143245.28656.15

75.

Spolverato

, Capelli

, Mari

, et al. Very early recurrence after curative-intent surgery for gastric adenocarcinoma. Ann Surg Oncol, 2022; 29(13):8653–8661; doi: 10.1245/s10434-022-12434-y

76.

, Shen

, Shui

, et al. Patterns of recurrence after curative D2 resection for gastric cancer: Implications for postoperative radiotherapy. Cancer Med, 2020; 9(13):4724–4735; doi: 10.1002/cam4.3085

77.

Ojima

, Nakamura

, Hayata

, et al. Short-term outcomes of robotic gastrectomy vs laparoscopic gastrectomy for patients with gastric cancer: A randomized clinical trial. JAMA Surg, 2021; 156(10):954–963; doi: 10.1001/jamasurg.2021.3182

78.

, Zheng

, Xu

, et al. Assessment of robotic versus laparoscopic distal gastrectomy for gastric cancer: A randomized controlled trial. Ann Surg, 2021; 273(5):858–867; doi: 10.1097/sla.0000000000004466

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