Advertisement

Gastric Cancer

, Volume 22, Issue 5, pp 909–919 | Cite as

Robotic-assisted gastrectomy for gastric cancer: a European perspective

  • Gijsbert I. van Boxel
  • Jelle P. Ruurda
  • Richard van HillegersbergEmail author
Open Access
Review Article
  • 518 Downloads

Abstract

Gastrectomy is the mainstay treatment for gastric cancer. To reduce the associated patient burden, minimally invasive gastrectomy was introduced in almost 30 years ago. The increase in the availability of surgical robotic systems led to the first robotic-assisted gastrectomy to be performed in 2002 in Japan. Robotic gastrectomy however, particularly in Europe, has not yet gained significant traction. Most reports to date are from Asia, predominantly containing observational studies. These cohorts are commonly different in the tumour stage, location (particularly with regards to gastroesophageal junctional tumours) and patient BMI compared to those encountered in Europe. To date, no randomised clinical trials have been performed comparing robotic gastrectomy to either laparoscopic or open equivalent. Cohort studies show that robotic gastrectomy is equal oncological outcomes in terms of survival and lymph node yield. Operative times in the robotic group are consistently longer compared to laparoscopic or open gastrectomy, although evidence is emerging that resectional surgical time is equal. The only reproducibly significant difference in favour of robot-assisted gastrectomy is a reduction in intra-operative blood loss and some studies show a reduction in the risk of pancreatic fistula formation.

Keywords

Gastric cancer Robotic-assisted gastrectomy RAG Outcomes 

Introduction

Gastric cancer is the 5th most common cancer globally with a crude incidence of 13.5/100.000 in the population. Incidence varies widely between continents and the disease is far more prevalent in the Far East. To illustrate this, the crude incidence of gastric cancer is 10/100000 in The Netherlands compared to 90/100000 in Japan. Globally, gastric cancer is the third most deadly cancer annually [1]. The mainstay of curative treatment is surgical resection and lymphadenectomy with or without (neo)adjuvant therapy based on the stage of the disease and patient co-morbidity.

Minimally invasive surgery is associated across many surgical specialties with a reduction in post-operative pain, hospital length of stay and faster return to normal activities of daily living. Laparoscopic-assisted gastrectomy (LAG) has an established role in early, and increasingly locally advanced, gastric cancers since it was first described in 1994 [2]. The Japanese gastric cancer treatment guideline now recommends distal LAG for early gastric cancers in part based on the KLASS-01 study [3] and multiple meta-analyses [4, 5, 6, 7, 8]. The benefit for locally advanced cancers had until very recently not been proven by RCT, but Lee et al. have now published on the 3-year follow-up of the KLASS-02 trial [9]. This has shown that distal LAG with D2 lymphadenectomy for locally advanced gastric cancer has benefits in terms of lower complication rate, faster recovery, and less pain compared with open gastrectomy (OG). Cui et al. published an RCT comparing LAG and OG which included approximately one-third of total gastrectomies (42/128 LAG and 39/142 OG) amongst a majority of partial or distal resections. A subgroup analysis of this cohort focussing on OG total gastrectomy versus LAG total gastrectomy again showed similar benefits for LAG at no oncological expense [10]. A large multicentre Dutch randomised study, LOGICA, has just finished recruiting exclusively comparing total OG to total LAG [11]. Results are awaited in the second half of 2019.

Over the past 2 decades, robotic-assisted surgery has witnessed a meteorological rise in its uptake and applications [13]. The drivers for the ongoing and increasing innovation originate from the desire to offer greater operative precision that may translate into enhanced clinical outcomes. Robotic-assisted gastrectomy (RAG) for gastric cancer was first reported in 2002 [14]. A relatively recent publication from South Korea, one of the greatest developers and adopters of RAG, shows that the uptake is increasing exponential though only representing approximately 4% of the total robotic procedures performed annually [15], which represents about 2% of the gastrectomies performed in South Korea [16]. The premise is that RAG is expected to deliver at least the same benefits of laparoscopic surgery compared to open, but in addition, due to 3-dimensional vision, high magnification, increased degrees of freedom including endo-wristed instrumentation, stable optical platform and tremor reduction technology, potentially be superior to established minimally invasive methods. This could result in reducing a surgeon’s learning curve and creating improved training. To date, however, prospective multicentre randomised studies remain lacking, and evidence comprises several case-matched series [e.g. 17, 18, 19] and meta-analyses [12, 20, 21, 22, 23, 24]. However, the majority of the meta-analyses report on a small number of Asian cohort studies and often compare RAG to both LAG and OG. Furthermore, the difference in complexity and associated morbidity between distal gastrectomy and total gastrectomy is not always specified in comparative studies and this must be considered when interpreting the perceived lack of benefit for RAG.

This article reviews the current evidence base for robotic-assisted gastrectomy for gastric cancer. Oncological outcomes, potential benefits, complications, limitations and cost will all be discussed. The available evidence will be related to European cohorts, in whom there is relatively little known about the outcomes of RAG since only few comparative studies have been performed.

The operation

Minimally invasive gastrectomy follows the same oncological principles as those established for open surgery. Song et al. eloquently describe the procedure (both distal and total gastrectomy) using the da Vinci 4 arm system (Intuitive Surgical Inc, Sunnyvale, CA, USA) in great detail in a review of 100 sequential cases [25]. Patients are commonly placed supine in 15 degrees anti-Trendelenburg position. Four robot ports are placed and one assistant port across the above the midline of the abdomen in both quadrants.

The case series reported in the literature to date all utilise the Intuitive Surgery da Vinci system. Robotic surgery aims to address many of the ergonomically and optical disadvantages of laparoscopy. The operative field is magnified tenfold and allows the primary (console) surgeon better optical control through the high-definition 3-D views from a mounted, stabilized surgeon-controlled camera reducing reliance on an assistant surgeon. Furthermore, robotic surgical tools allow flexible, endo-wristed movement capabilities, self-assistance and retraction through a third operating robotic arm. The improved surgical dexterity and ergonomics provided by the robot result from the instruments’ 7 degrees of freedom, 90° articulation, and 540° rotation, permitting manipulation within small spaces. Although this is particularly relevant in a confined area such as the chest, hiatal dissection and lymphadenectomy on the superior border of the pancreas are certainly aided by this. Several studies have shown that the robot can enhance dexterity by up to 65%, reduce skill-based errors by 93%, and reduce the time needed to complete a given task by 40% [26, 27].

Earlier da Vinci system was more confined in terms of the operative field attainable without further port placement and/or re-docking. Gastrectomy requires abdominal surgical access from relatively deep into the diaphragmatic hiatus, the splenic hilum, the duodenum and the retro-colic space. Essentially this requires access to 3 quadrants of the abdomen, which until recently has proven challenging robotically. The new Xi system with its slim arms and rotating boom (and anticipated systems such as the Versius, [28], and Verb [29] with either independent arms or table mounted arms) are marketed to permit greater access range and multi-quadrant use.

Short-term surgical outcomes

Operative time and learning curve

The operative time for RAG is longer than LAG [24] (mean 58 min) which in turn is longer then open surgery (mean 64 min) [30], therefore, making RAG approximately 2 h longer than OG. The reasons for this are multiple, but the docking of the robot can be time consuming, particularly in theatres that use the robot intermittently. Most studies that make the distinction between docking time and console time report this to be in the order of 20 min. A recent study by Liu et al. [31] specifically investigated the time taken to perform distal gastrectomy by robotic and laparoscopic means. This retrospective study included 10 cases in the RAG and LAG groups and, once again, showed the total procedure time for RAG to be on average 57 min longer than LAG. It did, however, assess specific resectional components of the operation and showed that the actual surgical time was the same in the RAG and LAG groups. The conclusion was, therefore, that robotic-assisted surgery still incurs “junk” time, which may be addressed by simpler system setup, faster instrument changes and more sophisticated energy devices. In our own experience, we found that the average docking time/operative time reduced over 25 procedures and subsequently stabilised to 12–15 min [27]. The literature disproportionally reports on early experiences of RAG as take up is still relatively low. Nonetheless, these series are often compared to established open or laparoscopic methods where surgeons are many cases beyond there learning curve. Only a few studies formally assess their learning curve, which has been reported between 20 and 95 [25, 32, 33, 34] cases, depending on previous experience in gastrectomy. As such, it can be expected that many of the current operative times reported are not reflective of the optimal operative time a given surgeon can achieve.

Blood loss

A reduction in intra-operative blood loss has been the most consistent finding in the meta-analyses published on RAG to date. This is the case for those studies assessing RAG vs LAG and those that compare RAG with OG. The most recent study reports a mean reduction of blood loss of 23.7 ml for RAG compared to laparoscopic or open surgery [24]. Although this number is relatively low, differences in blood loss should not be disregarded as unimportant as there is certainly evidence of reduced peri-operative infection rates associated with reduced blood loss [35] and potentially even recurrence rates [36].

Pancreatic fistula

Pancreatic damage due to manipulation during dissection and D2 lymphadenectomy may result in pancreatic leaks and fistula formation. Although a relatively rare complication of gastrectomy, the morbidity associated with this can be significant. The introduction of LAG has led some groups to suggest that the incidence of pancreatic trauma is greater [37, 38, 39]. There have even been reports of specialised equipment being used to reduce the risk of pancreatic fistula [40], but some believe robotic dissection may reduce pancreatic damage by facilitating careful, yet radical, resection around the border of the pancreas based on their case series [41, 42, 43]. Guerra et al. [44] recently published a meta-analysis investigating the incidence of pancreatic complications between RAG and LAG, particularly looking at post-operative pancreatic fistula formation and acute pancreatitis. Although there was a trend towards fewer pancreatic complications with RAG, (with an OR of 0.8), this was not statistically significant. The review included 4 new case series not previously included in meta-analyses, one of which [42] showed a significant difference between pancreatic complications between RAG (10%) and LAG (22.5%). This study was specifically designed to formally assess pancreatic complications using drain and serum amylase and is worthy of separate mention beyond the aforementioned meta-analysis. The rationale for the difference, according to the authors, was the constant careful retraction achieved robotically, which is not replicated by a human first assistant. A recent study by Uyama et al. specifically assessed the morbidity of RAG with a historic control [45]. This multicentre, prospective, single arm study showed that pancreatic leaks occurred in 5.9% of patients, although the majority required no intervention. This reflects the findings of previous retrospective comparative studies.

Conversion to open and peri-operative mortality or anastomotic leak

There has been no significant difference in any of the studies published to date in terms of conversion to open or laparoscopy or re-operation following index surgery. Equally, peri-operative mortality (both 30 and 90 days) are not significantly different between RAG, LAG and OG (0.4–0.6% [24]). There was no difference observed in anastomotic leak rates between any of the groups.

Oncological outcomes

Cancer stage

The largest Far Eastern single-centre study of RAG reflects the fact that gastric cancer is detected earlier with consequently lower T stages and the majority being N0 [46]. This compares to a majority of Stage III disease (35%) in the largest available sole European cohort [47]. As such the available data, particularly in terms of resection margins, survival and conversions rates need to be carefully weight up when wanting to utilise evidence in a substantially different population.

Lymph node yield

Lymphatic drainage of the stomach has been extensively studied since the 1950s and the Japanese were the first to classify regional gastric lymph nodes into 16 stations which were widely adopted worldwide [48]. In 1997, the Japanese Gastric Cancer Association further defined and subdivided the nodal stations into 20 stations and a further 3 in the thorax (110, 111, 112) [49]. The nodes are further divided into tiers reflecting that certain stations lie outside the operative field (e.g. station 16b2; para-aortic) which would, therefore, represent distant metastases. Three types of lymphadenectomy are described in the context of oncological gastric resections; D1, D1 + and D2. For total gastrectomy, the lymph node stations to be dissected in D1 lymphadenectomy are stations from No. 1 to 7; D1 + includes D1 stations plus station 8a, 9, and 11p, and D2 includes D1 stations plus stations No. 8a, 9, 10 (although this remains under debate), 11p, 11d, and 12a. For tumours invading the oesophagus, D1 + includes Nos. 110 and D2 includes Nos. 19, 20, 110 and 111. A great deal of research has been performed to establish the oncological benefit of the various lymphadenectomy. The 15-year follow-up of the Dutch D1-D2 trial, randomising patients to a D1 or D2 lymphadenectomy, definitively showed a survival benefit for (spleen preserving) D2 lymphadenectomy, although associated with larger peri-operative morbidity and mortality [50]. With regard to RAG, the lymph node yield has not been significantly different in any of the meta-analyses published compared to LAG or OG. The only cohort studies that have shown a difference in favour of RAG were Cianchi et al. 2016 [51] and, in the context of spleen preserving D2 total gastrectomy, an increase in splenic artery nodes [52]. One study [53] has shown a benefit in “obese’ patients in terms of improved lymph node yield, but the mean BMI in this cohort was 27 (see Tables 1, 2). Conversely, Hyun showed the opposite with a decreased lymph node yield in “obese” patients for RAG [54]. Caruso et al. [55] showed a decreased lymph node yield for RAG when comparing it to OG.
Table 1

Eastern studies included in the meta-analyses on RAG performed to date

Study

Number of RAG (Total in study)

Type of RAG resection

% early tumours (< T2N1)

Country

BMI (mean kg/m2)

Outcome summary

Song et al. (2009) [25]

40

RAG 20

LAG 20

Subtotal

100

South Korea

23

Increased operative time RAG

Kim et al. (2010) [82]

39

RAG 12

LAG 11

OG 16

Subtotal

100

South Korea

21

Increased operative time RAG

Reduced blood loss and LOS RAG

Woo et al. (2011) [62]

827

RAG 236

LAG 591

Subtotal (73%)

Total (27%)

93

South Korea

23

Increased operative time RAG

Reduced blood loss RAG

Kim et al. (2012) [83]

5839

RAG 436

LAG 861

OG 4542

Subtotal (75%)

Total (25%)

86

South Korea

24

Increased operative time RAG

Makes comparisons between MIG and OG; increased anastomotic leak in MIG, reduced post op ileus and LOS in MIG

Park et al. (2012) [32]

150

RAG 30

LAG 120

Subtotal

100

South Korea

24

Increased operative time RAG

Reduced performance status and drain output in RAG

Eom et al. (2012) [84]

92

RAG 30

LAG 62

Subtotal

92

South Korea

24

Increased operative time RAG, smaller proximal margin RAG and increased cost

Huang et al. (2012) [85]

689

RAG 39

LAG 64

OG 586

Subtotal (96%)

Total (4%)

93

Taiwan

24

Reduced blood loss and LOS RAG Increased operative time RAG

Uyama et al. (2012) [86]

250

RAG 25

LAG 225

Subtotal

100

Japan

22

Decreased LOS RAG

Kang et al. (2012) [87]

382

RAG 100

LAG 282

Subtotal (84%)

Total (16%)

93

South Korea

24

Increased LOS for RAG

Reduced blood loss RAG

Yoon et al. (2012) [88]

101

RAG 36

LAG 65

Total

100

South Korea

23

Increased operative time RAG

Hyun et al. (2013) [54]

121

RAG 38

LAG 83

Subtotal (76%)

Total (24%)

87

South Korea

24

RAG group statistically younger

Subgroup analysis of “obese” pts (BMI > 25) showed reduced lymph node yield in RAG

Son et al.(2014) [52]

109

RAG 51

LAG 58

Total

74

South Korea

23

Increased operative time RAG

Increased lymph node yield along splenic artery RAG

Noshiro et al. (2014) [43]

181

RAG 21

LAG 160

Subtotal

85

Japan

23

Reduced LOS RAG

Huang et al. (2014) [85]

145

RAG 72

LAG 73

Subtotal (94%)

Total (6%)

90

China

24

Increased cost and operative time RAG

Decreased blood loss RAG

Junfeng et al. (2014) [89]

514

RAG 120

LAG 394

Subtotal (78%)

Total (22%)

45

China

22

Increased operative time, lymph node yield RAG

Reduced blood loss RAG

Park et al. (2015) [90]

770

RAG 148

LAG 622

Mixed

Subtotal (75%)

Total (25%)

97

South Korea

24

Increased operative time RAG

Lee et al. (2015) [53]

400

RAG 133

LAG 267

Subtotal

82

South Korea

23

Increased operative time, decreased blood loss RAG

Increased lymph node yield in “obese” (BMI 27) patients in RAG (RAG group was statistically younger)

Kim et al. (2016) [91]

370

RAG 185

LAG 185

Subtotal

94

South Korea (multicentre)

24

Increased operative time RAG

Okumura et al. (2016) [92]

502

RAG 370

LAG 132

Subtotal (77%)

Total (23%)

85

Japan

24

Increased operative time RAG

RAG is safe in the elderly (mean age 70)

Parisi et al. (2017) [18]

604

RAG 151

LAG 151

OG 302

Mixed

Subtotal (74%)

Total (26%)

75

Multicentre (IMIGASTRIC)

24

Increased operative time RAG

Reduced LOS RAG/LAG

Yang et al. (2017) [93]

915

RAG 173

LAG 511

OG 241

Mixed

Subtotal (86%)

Total (14%)

88

South Korea

24

Decreased LOS MIG

Li et al. (2018) [19]

224

RAG 112

LAG 112

Mixed

Subtotal (57%)

Total (43%)

35

China

24

Increased operative time RAG

Reduced blood loss RAG

Increased cost RAG

Liu et al. (2018) [94]

235

RAG 100

LAG 135

Mixed

Subtotal (58%)

Total (42%)

40

China

21

Reduced LOS RAG

Gao et al. (2019) [95]

326

RAG 163

LAG 163

Mixed

Subtotal (62%)

Total (38%)

35

China

24

Increased operative time and cost for RAG

RAG robot-assisted gastrectomy, LAG laparoscopic-assisted gastrectomy, OG open gastrectomy, LOS length of stay, MIG minimally invasive gastrectomy (RAG and LAG combined)

Table 2

Western studies included in the meta-analyses on RAG performed to date

Pugliese et al. (2009) [68]

64

RAG 16

LAG 48

Subtotal

55

Italy

29

No difference

Caruso et al. (2011) [55]

169

RAG 29

OG 120

Subtotal (59%)

Total (41%)

76

Italy

28

Increased operative time RAG

Reduced blood loss and LOS RAG

Reduced lymph node yield RAG

Cianchi et al. (2016) [51]

71

RAG 41

LAG 30

Distal

73

Italy

27

Increased operative time RAG

Increased number of lymph nodes retrieved in RAG

Procopiuc et al. (2016) [23]

47

RAG 18

OG 29

Mixed

Subtotal (44%)

Total (56%)

50

Romanian

26

Increased operative time RAG

Caruso et al. (2018) [47]

39

RAG 19

LAG 20

Total

Unknown

Spain

Unknown

Increased operative time RAG

Reduced blood loss and LOS RAG

RAG robot-assisted gastrectomy, LAG laparoscopic-assisted gastrectomy, OG open gastrectomy, LOS length of stay

Long-term outcomes

Survival

The evidence for oncological equivalence of minimally invasive gastrectomy has been published [5, 6, 7]. Because uptake of RAG is still relatively low, and the constraints imposed by the insurance systems in the Far East which mean the patient has to pay for the difference in cost compared to LAG, multicentre randomised controlled trials are not ongoing. The meta-analyses previously referenced to here, as well as the KLASS-01/02 Trials comparing LAG and OG, have not shown a significant difference in oncological outcomes between RAG, LAG or OG. The largest series on the oncological results, in terms of overall survival (OS), relapse-free survival (RFS) and recurrence patterns was published by Obama et al. [46]. This single-centre retrospective, prospectively collected, propensity-score matched study (the matching of which have been questioned some [56]) compared 313 RAG with 313 (out of 524) LAG. Total or subtotal gastrectomy was performed according to the Japanese gastric cancer treatment guidelines [57]. The median follow-up was 85 months and showed no significant difference in OS or RFS. It is important to realise, in the context of the disease stage experienced in Europe, that approximately 75% of these patients had T1N0 disease, and hence OS was > 90% for both groups.

Functional

There are very little data on the functional outcome of RAG compared to LAG or OG. The main reason for this is that the majority of functional problems are related to the reconstruction which, where available, in the studies published to date was all performed in an identical manner to LAG using laparoscopic staplers and or extracorporeal joins. Like in laparoscopy, there has been an increasing trend towards intracorporeal anastomoses. With the recent advances in laparoscopic and robotic tri-stapling devices, this trend is expected to continue.

Cost

The perceived additional cost associated with robotic surgery is a common argument against adopting the technology. Although the robot itself, the consumables and maintenance are a considerable financial investment, there are numerous examples, where robotic surgery has proven to be cost effective in high volume centres [58, 59] or even cost saving [60, 61], be it within certain, realistic, anticipated complication levels. Although the financial comparison between LAG and OG has not been formally assessed (although expected as part of the LOGICA trial), the cost of RAG was compared to LAG in a multicentre prospective match cohort study and found to be around $5000 higher ($13432 vs $8090) [17]. The cost assessment considered the entire expenditure of the admission; this included consumables as well as potential interventions required during the index hospital admission. Although the study was prospective, 8 out of 17 of the surgeons had relatively minimal robotic experience (fewer than 30 cases, including one surgeon who had only performed 4 RAG) and the learning curve effect can, therefore, not be excluded and should be considered whenever conclusions are drawn from, what is to date, the only multicentre prospective comparative study between RAG and LAG. In one of the largest single-centre case series to date (243 cases), Woo et al. [62] discuss the complexity surrounding the analysis of cost when comparing RAG and LAG. Because most the case series come from the Far East, the role of healthcare insurance plays an important part in the decision of a patient to have RAG or LAG; the patient are commonly expected to pay the difference between RAG and LAG as the insurance will not cover this. This, of course, means any cohort comparisons are non-randomised and potentially biased. For example, the matched cohorts are statistically different in age (RAG cohort is younger) and reconstruction [RAG majority Billroth II (51%) vs LAG Billroth I (54%)]. Beyond this, it has historically been challenging to truly calculate potential long-term cost savings for a given procedure. In colorectal surgery for example, the potential reduction in stoma rates for robotic low rectal resections could have a huge consequence for the health economics associated with the procedure, although this benefit is currently not proven [63]. Equally, reduced length of ICU admission or overall stay has cost effects [64]. Uyama et al. showed in their prospective study that complications are associated with increased cost [45]. The same study showed a significant reduction in complications (compared to a historic LAG group) and subsequently improved quality of life. These findings combined were sufficient to the Ministry of Health, Labour, and Welfare in Japan to recognise RAG as a valid minimally invasive technique from a health insurance perspective.

In the context of cancer surgery, especially gastric surgery where neoadjuvant therapy is the standard of care for most tumours, costs need to be contextualised; the cost of 4 courses of FLOT is in the order of $2000 [65]. However, drugs like Trastuzamab given in the context of Her2 + ve advanced gastric cancer attract far greater costs ($70000 annually) for a mean survival benefit of 2.7 months [66], vastly eclipsing the increased costs currently associated with robotic surgery. Nonetheless, in the absence of alternative high level evidence for the benefits of robotic surgery in certain procedures, the costs of robotic consumable and hardware are currently a major argument against mainstream implementation in many healthcare systems. The development of new robots has already seen a change in both design (open consoled, modular systems), but also the business models used to alter the associated costs with robotic surgery [67]. For example, Cambridge Medical Robotics from the UK have adopted alternative costing models which cover maintenance, instruments and even assistants as a comprehensive package, beyond solely charging for hardware.

RAG in Europe

To date only five European RAG cohort studies have been published [23, 47, 51, 55, 68]. The total number of RAG cases included in these is 123. Unit volume should, therefore, be considered carefully when interpreting the available data. The mean BMI of the combined European cohorts is 28 kg/m2, which according to WHO guidelines is overweight (the term obese is frequently incorrectly used in the RAG literature to include anyone with a BMI greater than 25). This compares to a mean BMI of 23 kg/m2 in the Asian cohorts. The stage of disease at the time of surgery is more advanced in the European cohort > T2N1 in 55–75%; only one Asian study reports a larger proportion of advanced tumours [19]. Gastroesophageal junctional adenocarcinomas are particularly relevant in this context; these tumours are more prevalent in Western countries [69] and typically present with more advanced disease and lymph node involvement [70]. Reports of increased prevalence in Far Eastern countries have become more commonplace [71], but the percentage of total gastrectomies in the Western studies is higher which, although not specifically commented on, would imply a greater proportion of proximal/junctional tumours. Interestingly, more recent reports from the Far East have started to include larger numbers of total gastrectomies—whether this reflects a shift in disease patterns or a greater willingness/aptitude at the procedure to therefore operate on more proximal tumours, again, is not specifically commented on. The 8th edition of the American Joint Commission on Cancer (AJCC) staging manual [72] redefined GEJ cancers. In this, more recent type III are now considered gastric tumours. Consequently, many centres now treat these tumours accordingly in a neo-adjuvant setting with FLOT [73]. Interestingly, the surgical management, however (total/extended gastrectomy versus esophagectomy), remains controversial and is the subject of a proposed prospective multicentre trial; the CARDIA trial [74].

The relatively limited European RAG comparative cohort studies that have been reported to date indeed show differences in the patient characteristics as illustrated above. Nonetheless, the outcomes in these studies in terms of overall outcomes, complications and technical aspects such as operative time and blood loss, despite being relatively small cohorts, do reflect those observed in the Far East.

The future

The available evidence to date shows RAG is a safe and oncologically sound alternative to LAG or OG. The benefits of RAG, thus far, have been relatively minor and appear to come with an increased cost and longer operation time based on available cohort studies. The majority of the studies include distal gastrectomies for early tumours performed by surgeons relatively early on in their learning curve. As such, some caution must be exercised when translating the current evidence to a European population. Ojima et al. have started a phase III single-centre randomised controlled trial comparing LAG vs RAG for stage I–III gastric cancer [75], which has been recruiting since April 2018.

Benefits of robotic systems not discussed here, or formally studied in the context of RAG, include the use of ICG to assess vascularity [76] and (sentinel) lymph nodes [77]. Inclusion of artificial intelligence and machine learning to aid the surgeon in these complex procedures are coming on the horizon [78]. A recent phase I/II trail [79] has shown reduced port robotic distal gastrectomy to be safe and feasible.

There has also been a global push to prospectively collect clinical information of patients undergoing RAG by means of the IMIGASTRIC project [80], which has been mirrored by other oesophagogastric operations such esophagectomy in the context of UGIRA [81]. These database initiatives are key to monitor and share experiences of a seismic change in surgical practice that is here to stay.

Notes

Funding

No funding was received for this paper.

Compliance with ethical standards

Conflict of interest

JR and RvH both proctor for Intuitive Surgery.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

References

  1. 1.
    IARC2018: https://www.iarc.fr/. Accessed 12 Mar 2019.
  2. 2.
    Kitano S, Iso Y, Moriyama M, Sugimachi K. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc. 1994;4:146–8.Google Scholar
  3. 3.
    Kim W, Kim HH, Han SU, et al. Decreased morbidity of laparoscopic distal gastrectomy compared with open distal gastrectomy for stage I gastric cancer: short-term outcomes from a multicenter randomized controlled trial (KLASS-01). Ann Surg. 2016;263:28–35.Google Scholar
  4. 4.
    Viñuela 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.Google Scholar
  5. 5.
    Qiu J, Pankaj P, Jiang H, Zeng Y, Wu H. Laparoscopy versus open distal gastrectomy for advanced gastric cancer: a systematic review and meta-analysis. Surg Laparosc Endosc Percutaneous Tech. 2013;23:1–7.Google Scholar
  6. 6.
    Zeng YK, Yang ZL, Peng JS, Lin HS, Cai L. Laparoscopy assisted versus open distal gastrectomy for early gastric cancer: evidence from randomized and nonrandomized clinical trials. Ann Surg. 2012;256:39–52.Google Scholar
  7. 7.
    Ding J, Liao GQ, Liu HL, Liu S, Tang J. Meta-analysis of laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for gastric cancer. J Surg Oncol. 2012;105:297–303.Google Scholar
  8. 8.
    Chen K, Pan Y, Zhang B, Maher H, Wang XF, Cai XJ. Robotic versus laparoscopic gastrectomy for gastric cancer: a systematic review and updated meta-analysis. BMC Surg. 2017;17:93.Google Scholar
  9. 9.
    Lee HJ, Hyung WJ, Yang HK, Han SU, et al. Korean Laparo-endoscopic Gastrointestinal Surgery Study (KLASS) Group. Short term outcomes a multicentre randomized controlled trial comparing laparoscopic distal gastrectomy with D2 lymphadenectomy to open distal gastrectomy for locally advanced gastric cancer (KLASS-02-RCT). Ann Surg. 2019;.  https://doi.org/10.1097/SLA.0000000000003217.Google Scholar
  10. 10.
    Cui M, Li Z, Xing J, Yao Z, Liu M, Chen L, et al. A prospective randomized clinical trial comparing D2 dissection in laparoscopic and open gastrectomy for gastric cancer. Med Oncol. 2015;32(10):241.Google Scholar
  11. 11.
    Haverkamp L, Brenkman HJ, Seesing MF, Gisbertz SS, van Berge Henegouwen MI, et al. Laparoscopic versus open gastrectomy for gastric cancer, a multicentre prospectively randomized controlled trial (LOGICA-trial). BMC Cancer. 2015;15:556.Google Scholar
  12. 12.
    Zong L, Seto Y, Aikou S, Takahashi T. Efficacy evaluation of subtotal and total gastrectomies in robotic surgery for gastric cancer compared with that in open and laparoscopic resections: a meta-analysis. PLoS One. 2014;9(7):e103312.Google Scholar
  13. 13.
    Tan A, Ashrafian H, Scott AJ, Mason SE, Harling L, et al. Robotic surgery: disruptive innovation or unfulfilled promise? A systematic review and meta-analysis of the first 30 years. Surg Endosc. 2016;10:4330–52.Google Scholar
  14. 14.
    Hashizume M, Shimada M, Tomikawa M, et al. Early experiences of endoscopic procedures in general surgery assisted by a computer enhanced surgical system. Surg Endosc. 2002;16:1187–91.Google Scholar
  15. 15.
    Lim SH, Lee HM, Son T, Hyung WJ, Kim HI. Robotic surgery for gastric tumor: current status and new approaches. Transl Gastroenterol Hepatol. 2016;7(1):28.Google Scholar
  16. 16.
    The Information Committee of Korean Gastric Cancer Association Corrigendum. Korean Gastric Cancer Association nationwide survey on gastric cancer in 2014. The Information Committee of Korean Gastric Cancer Association. J Gastric Cancer. 2014;16(4):277.Google Scholar
  17. 17.
    Kim HI, Han SU, Yang HK, et al. Multicentre prospective comparative study of robotic versus laparoscopic gastrectomy for gastric adenocarcinoma. Ann Surg. 2016;263:103–9.Google Scholar
  18. 18.
    Parisi A, Reim D, Borghi F, Nguyen NT, Qi F, Coratti A, et al. Minimally invasive surgery for gastric cancer: a comparison between robotic, laparoscopic and open surgery. World J Gastroenterol. 2017;23(13):2376–84.Google Scholar
  19. 19.
    Li Z, Li J, Li B, Bai B, Liu Y, et al. Robotic versus laparoscopic gastrectomy with D2 lymph node dissection for advanced gastric cancer: a propensity score-matched analysis. Cancer Manag Res. 2018;10:705–14.Google Scholar
  20. 20.
    Marano A, Choi YY, Hyung WJ, Kim YM, Kim J, Noh SH. Robotic versus laparoscopic versus open gastrectomy: a meta-analysis. J Gastric Cancer. 2013;13:136–48.Google Scholar
  21. 21.
    Shen WS, Xi HQ, Chen L, Wei B. A meta-analysis of robotic versus laparoscopic gastrectomy for gastric cancer. Surg Endosc. 2018;28(10):2795–802.Google Scholar
  22. 22.
    Liao G, Chen J, Ren C, Li R, Du S, Xie G, Deng H, Yang K, Yuan Y. Robotic versus open gastrectomy for gastric cancer: a meta-analysis. PLoS One. 2013;8(12):e81946.Google Scholar
  23. 23.
    Procopiuc L, Tudor S, Manuc M, Diculescu M, Vasilescu C. Open vs robotic radical gastrectomy for locally advanced gastric cancer. Int J Med Robot. 2016;12(3):502–8.Google Scholar
  24. 24.
    Bobo Z, Xin W, Jiang L, Quan W, Liang B, Xiangbing D, Ziqiang W. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: meta-analysis and trial sequential analysis of prospective observational studies. Surg Endosc. 2019;33(4):1033–48.Google Scholar
  25. 25.
    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.Google Scholar
  26. 26.
    Moorthy K, Munz Y, Dosis A, Hernandez J, Martin S, et al. Dexterity enhancement with robotic surgery. Surg Endosc. 2004;18(5):790–5.Google Scholar
  27. 27.
    Ruurda JP, Broeders IA, Simmermacher RP, Borel Rinkes IH, Van Vroonhoven TJ. Feasibility of robot-assisted laparoscopic surgery: an evaluation of 35 robot-assisted laparoscopic cholecystectomies. Surg Laparosc Endosc Percutaneous Tech. 2002;12(1):41–5.Google Scholar
  28. 28.
    https://cmrsurgical.com/versius/. Accessed 15 Mar 2019.
  29. 29.
    https://www.verbsurgical.com. Accessed 15 Mar 2019.
  30. 30.
    Wei Y, Yu D, Li Y, Fan C, Li G. Laparoscopic versus open gastrectomy for advanced gastric cancer: a meta-analysis based on high-quality retrospective studies and clinical randomized trials. Clin Res Hepatol Gastroenterol. 2018;42(6):577–90.Google Scholar
  31. 31.
    Liu H, Kinoshita T, Tonouchi A, Kaito A, Tokunaga M. What are the reasons for a longer operation time in robotic gastrectomy than in laparoscopic gastrectomy for stomach cancer? Surg Endosc. 2019;33(1):192–8.Google Scholar
  32. 32.
    Park SS, Kim MC, Park MS, Hyung WJ. Rapid adaptation of robotic gastrectomy for gastric cancer by experienced laparoscopic surgeons. Surg Endosc. 2012;26(1):60–7.Google Scholar
  33. 33.
    Huang KH, Lan YT, Fang WL, Chen JH, Lo SS, et al. Initial experience of robotic gastrectomy and comparison with open and laparoscopic gastrectomy for gastric cancer. J Gastrointest Surg. 2012;16:1303–10.Google Scholar
  34. 34.
    Kim HI, Park MS, Song KJ, 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;40:1346–54.Google Scholar
  35. 35.
    Xiao H, Quan H, Pan S, Yin B, Luo W, Huang G, Ouyang Y. Impact of peri-operative blood transfusion on post-operative infections after radical gastrectomy for gastric cancer: a propensity score matching analysis focusing on the timing, amount of transfusion and role of leukocyte depletion. J Cancer Res Clin Oncol. 2018;144(6):1143–54.Google Scholar
  36. 36.
    Jiang W, Fang YJ, Wu XJ, Wang FL, Lu ZH, et al. Intraoperative blood loss independently predicts survival and recurrence after resection of colorectal cancer liver metastasis. PLoS One. 2013;8(10):e76125.Google Scholar
  37. 37.
    Jiang X, Hiki N, Nunobe S, et al. Postoperative pancreatic fistula and the risk factors of laparoscopy-assisted distal gastrectomy for early gastric cancer. Ann Surg Oncol. 2012;19:115.Google Scholar
  38. 38.
    Komatsu S, Ichikawa D, Kashimoto K, Kubota T, Okamoto K, et al. Risk factors to predict severe postoperative pancreatic fistula following gastrectomy for gastric cancer. World J Gastroenterol. 2013;19:8696–702.Google Scholar
  39. 39.
    Fujita T, Ohta M, Ozaki Y, Takahashi Y, Miyazaki S, et al. Collateral thermal damage to the pancreas by ultrasonic instruments during lymph node dissection in laparoscopic gastrectomy. Asian J Endosc Surg. 2015;8:281–8.Google Scholar
  40. 40.
    Matsunaga T, Saito H, Murakami Y, Kuroda H, Fukumoto Y, Osaki T. Usefulness of T-shaped gauze for precise dissection of supra-pancreatic lymph nodes and for reduced postoperative pancreatic fistula in patients undergoing laparoscopic gastrectomy for gastric cancer. Yonago Acta Med. 2016;59:232–6.Google Scholar
  41. 41.
    Nakauchi M, Suda K, Susumu S, Kadoya S, Inaba K, 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;30:5444–52.Google Scholar
  42. 42.
    Seo HS, Shim JH, Jeon HM, Park CH, Song KY. Post-operative pancreatic fistula after robot distal gastrectomy. J Surg Res. 2015;194:361–6.Google Scholar
  43. 43.
    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.Google Scholar
  44. 44.
    Guerra F, Giuliani G, Formisano G, Bianchi PP, Patriti A, Coratti A. Pancreatic complications after conventional laparoscopic radical gastrectomy versus robotic radical gastrectomy: systematic review and meta-analysis. J Laparoendosc Adv Surg Tech A. 2018;28(10):1207–15.Google Scholar
  45. 45.
    Uyama I, Suda K, Nakauchi M, Kinoshita T, Noshiro H, Takiguchi S, Ehara K, Obama K, Kuwabara S, Okabe H, Terashima M. Clinical advantages of robotic gastrectomy for clinical stage I/II gastric cancer: a multi-institutional prospective single-arm study. Gastric Cancer. 2019;22(2):377–85.  https://doi.org/10.1007/s10120-010-0555-2 (Gastric Cancer. 2010 Jun;13(2):63–73) (Epub 2010 Jul 3).Google Scholar
  46. 46.
    Obama K, Kim YM, Kang DR, Son T, Kim HI, et al. Long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer. 2018;21(2):285–95.Google Scholar
  47. 47.
    Caruso R, Vicente E, Quijano Y, Ielpo B, Duran H, et al. Robotic assisted gastrectomy compared with open resection: a case-matched study. Updates Surg. 2018.  https://doi.org/10.1007/s13304-018-0533-5.Google Scholar
  48. 48.
    Kajitani T. The general rules for the gastric cancer study in surgery and pathology. Part I. Clinical classification. Jpn J Surg. 1981;11:127–39.Google Scholar
  49. 49.
    Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2010 (ver. 3). Gastric Cancer. 2011;14:113–23.Google Scholar
  50. 50.
    Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11(5):439–49.Google Scholar
  51. 51.
    Cianchi F, Indennitate G, Trallori G, Ortolani M, Paoli B, et al. Robotic vs laparoscopic distal gastrectomy with D2 lymphadenectomy for gastric cancer: a retrospective comparative mono-institutional study. BMC Surg. 2016;16:65.Google Scholar
  52. 52.
    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.Google Scholar
  53. 53.
    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.Google Scholar
  54. 54.
    Hyun MH, Lee CH, Kwon YJ, 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.Google Scholar
  55. 55.
    Caruso S, Patriti A, Marrelli D, Ceccarelli G, Ceribelli C, et al. Open vs robot-assisted laparoscopic gastric resection with D2 lymph node dissection for adenocarcinoma: a case-control study. Int J Med Robot. 2011;7(4):452–8.Google Scholar
  56. 56.
    Kim JW. After propensity score matching in long-term oncologic outcomes of robotic gastrectomy for gastric cancer compared with laparoscopic gastrectomy. Gastric Cancer. 2018;21(6):1071.Google Scholar
  57. 57.
    Nakajima T. Gastric cancer treatment guidelines in Japan. Gastric Cancer. 2002;5:1–5.Google Scholar
  58. 58.
    Liberman D, Trinh QD, Jeldres C, Zorn KC. Is robotic surgery cost-effective: yes. Curr Opin Urol. 2012;22(1):61–5.Google Scholar
  59. 59.
    Felder SI, Ramanathan R, Russo AE, Jimenez-Rodriguez RM, Hogg ME, Zureikat AH, Strong VE, Zeh HJ, Weiser MR. Robotic gastrointestinal surgery. Curr Probl Surg. 2018;55(6):198–246.Google Scholar
  60. 60.
    Martin AD, Nunez RN, Castle EP. Robot-assisted radical cystectomy versus open radical cystectomy: a complete cost analysis. Urology. 2011;77:621–5.Google Scholar
  61. 61.
    Bansal SS, Dogra T, Smith PW, et al. Cost analysis of open radical cystectomy versus robot-assisted radical cystectomy. BJU Int. 2018;121:437–44.Google Scholar
  62. 62.
    Woo Y, Hyung WJ, Pak KH, et al. Robotic gastrectomy as an oncologically sound alternative to laparoscopic resections for the treatment of early-stage gastric cancers. Arch Surg. 2011;146:1086–92.Google Scholar
  63. 63.
    Isik O, Gorgun E. How has the robot contributed to colon cancer surgery? Clin Colon Rectal Surg. 2015;28(4):220–7.Google Scholar
  64. 64.
    van der Sluis PC, van der Horst S, May AM, Schippers C, Brosens LAA, et al. Robot-assisted minimally invasive thoracolaparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer: a randomized controlled trial. Ann Surg. 2019;269(4):621–30.Google Scholar
  65. 65.
    Quintana M, Toriz J, Novick D, Jones K, Botello B, et al. Resources and costs associated with the treatment of advanced and metastatic gastric cancer in the Mexican Public Sector: a patient chart review. Pharmacoecon Open. 2018;2(2):191–201.Google Scholar
  66. 66.
    Bang Y, Van Cutsem E, Feyereislova A, Chung H, Shen L, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010;376:687–97.Google Scholar
  67. 67.
    Rassweiler JJ, Autorino R, Klein J, Mottrie A, Goezen AS, Stolzenburg JU, et al. Future of robotic surgery in urology. BJU Int. 2017;120:822–41.Google Scholar
  68. 68.
    Pugliese R, Maggioni D, Sansonna F, 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.Google Scholar
  69. 69.
    Hasegawa S, Yoshikawa T. Adenocarcinoma of the esophagogastric junction: incidence, characteristics, and treatment strategies. Gastric Cancer. 2010;13(2):63–73.Google Scholar
  70. 70.
    Liu K, Zang W, Chen X, et al. Comparison on clinicopathological features and prognosis between esophagogastric junctional adenocarcinoma (Siewert II/III types) and distal gastric adenocarcinoma: retrospective cohort study, a single institution, high volume experience in China. Medicine (Baltimore). 2015;94:e1386.Google Scholar
  71. 71.
    Liu K, Yang K, Zhang W, et al. Changes of esophagogastric junctional adenocarcinoma and gastroesophageal reflux disease among surgical patients during 1988–2012. A single-institution, high-volume experience in China. Ann Surg. 2016;263:88–95.Google Scholar
  72. 72.
    Rice TW, Kelsen DP, Blackstone EH, et al. Esophagus and esophagogastric junction. In: Amin MB, Edge SB, Greene FL, et al., editors. AJCC cancer staging manual. 8th ed. New York: Springer; 2017. p. 185–202.Google Scholar
  73. 73.
    Al-Batran SE, Homann N, Pauligk C, Goetze TO, Meiler J, et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versusfluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastricor gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet. 2019;393(10184):1948–57.Google Scholar
  74. 74.
  75. 75.
    Ojima T, Nakamura M, Nakamori M, Hayata K, Katsuda M, Kitadani J, Maruoka S, Shimokawa T, Yamaue H. Robotic versus laparoscopic gastrectomy with lymph node dissection for gastric cancer: study protocol for a randomized controlled trial. Trials. 2018;19(1):409.Google Scholar
  76. 76.
    Kim M, Son SY, Cui LH, Shin HJ, Hur H, Han SU. Real-time vessel navigation using indocyanine green fluorescence during robotic or laparoscopic gastrectomy for gastric cancer. J Gastric Cancer. 2017;17(2):145–53.Google Scholar
  77. 77.
    Park DJ, Kim HH, Park YS, Lee HS, Lee WW, et al. Simultaneous indocyanine green and (99 m)Tc-antimony sulfur colloid-guided laparoscopic sentinel basin dissection for gastric cancer. Ann Surg Oncol. 2011;18(1):160–5.Google Scholar
  78. 78.
    Aruni G, Amit G, Dasgupta P. New surgical robots on the horizon and the potential role of artificial intelligence. Investig Clin Urol. 2018;59(4):221–2.Google Scholar
  79. 79.
    Lee S, Kim JK, Kim YN, Jang DS, Kim YM, et al. Safety and feasibility of reduced-port robotic distal gastrectomy for gastric cancer: a phase I/IIclinical trial. Surg Endosc. 2017;31(10):4002–9.Google Scholar
  80. 80.
    http://www.imigastric.com. Accessed 12 Mar 2019.
  81. 81.
    UGIRA. https://ugira.org. Accessed 16 Mar 2019.
  82. 82.
    Kim MC, Heo GU, Jung GJ. Robotic gastrectomy for gastric cancer: surgical techniques and clinical merits. Surg Endosc. 2010;24(3):610–5.Google Scholar
  83. 83.
    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(12):1681–7.Google Scholar
  84. 84.
    Eom BW, Yoon HM, Ryu KW, 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.Google Scholar
  85. 85.
    Huang KH, Lan YT, Fang WL, et al. Comparison of the operative outcomes and learning curves between laparoscopic and robotic gastrectomy for gastric cancer. PLoS One. 2014;9:e111499.Google Scholar
  86. 86.
    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.Google Scholar
  87. 87.
    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.Google Scholar
  88. 88.
    Yoon HM, Kim YW, Lee JH, et al. Robot-assisted total gastrectomy is comparable with laparoscopically assisted total gastrectomy for early gastric cancer. Surg Endosc. 2012;26:1377–81.Google Scholar
  89. 89.
    Junfeng Z, Yan S, Bo T, et al. Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: comparison of surgical performance and short-term outcomes. Surg Endosc. 2014;28:1779–87.Google Scholar
  90. 90.
    Park JY, Ryu KW, Reim D, 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.Google Scholar
  91. 91.
    Kim YM, Son T, Kim HI, Noh SH, Hyung WJ. Robotic D2 lymph node dissection during distal subtotal gastrectomy for gastric cancer: toward procedural standardization. Ann Surg Oncol. 2016;23:2409–10.Google Scholar
  92. 92.
    Okumura N, Son T, Kim YM, Kim HI, An JY, Noh SH, Hyung WJ. 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.Google Scholar
  93. 93.
    Yang SY, Roh KH, Kim YN, Cho M, Lim SH, et al. Surgical outcomes after open, laparoscopic, and robotic gastrectomy for gastric cancer. Ann Surg Oncol. 2017;24(7):1770–7.Google Scholar
  94. 94.
    Liu HB, Wang WJ, Li HT, Han XP, Su L, et al. Robotic versus conventional laparoscopic gastrectomy for gastric cancer: a retrospective cohort study. Int J Surg. 2018;55:15–23.Google Scholar
  95. 95.
    Gao Y, Xi H, Qiao Z, Li J, Zhang K, et al. Comparison of robotic- and laparoscopic-assisted gastrectomy in advanced gastric cancer: updated short- and long-term results. Surg Endosc. 2019;33(2):528–34.Google Scholar

Copyright information

© The Author(s) 2019

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.

Authors and Affiliations

  • Gijsbert I. van Boxel
    • 1
  • Jelle P. Ruurda
    • 1
  • Richard van Hillegersberg
    • 1
    Email author
  1. 1.Department of Surgery, G04 228University Medical Centre UtrechtUtrechtThe Netherlands

Personalised recommendations