Journal of Surgical Oncology 2015;112:271–278
Robotic Gastrectomy for Gastric Cancer TAEIL SON, MD1
AND
WOO JIN HYUNG, MD, PhD2,3,4*
1
Department of Surgery, Eulji Medical Center, Eulji University School of Medicine, Seoul, South Korea 2 Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea 3 Gastric Cancer Center, Yonsei Cancer Hospital, Yonsei University Health System, Seoul, South Korea 4 Robot and MIS Center, Severance Hospital, Yonsei University Health System, Seoul, South Korea
Robotic surgery for gastric cancer overcomes technical difficulties with laparoscopic gastrectomy. Its benefits include reduced intraoperative bleeding and shorter hospital stays; it is also easier to learn. Because accuracy increases during lymphadenectomy, a larger number of lymph nodes is likely to be retrieved using robotic gastrectomy. Higher costs and longer operation times have hindered the widespread adaptation and use of robotic surgery. In this review, we summarize the current status and issues regarding robotic gastrectomy.
J. Surg. Oncol. 2015;112:271–278. © 2015 Wiley Periodicals, Inc.
KEY WORDS: stomach neoplasms; gastrectomy; robotics; minimally invasive surgery
INTRODUCTION Less invasive surgical techniques have been developed to facilitate patients’ recovery after gastrectomy. The use of laparoscopic surgery for gastric cancer was first reported in 1994 [1]. Much evidence has accumulated after the initiation of minimally invasive gastrectomy, which supports the short-term benefits of the use of this procedure for early gastric cancer patients. These benefits include reduced pain, early recovery of intestinal function, decreased inflammatory response, and a shorter hospital stay, while maintaining comparable oncologic safety [2–5]. In spite of these advantages, however, technical difficulties and critical issues (i.e., D2 lymph node dissection, anastomosis methods, total gastrectomy, and oncologic safety for advanced cancer) remain to be solved before the indications for minimally invasive gastrectomy for gastric cancer are expanded [6–8]. The new technology represented by the use of the surgical robot was expected to resolve the problems associated with laparoscopic surgery [9]. Experienced laparoscopic surgeons adopted robotic surgery procedures for gastric cancer treatment [10–12]. Within a decade after the initial reports describing its use for the treatment of gastric cancer [13,14], robotic gastrectomy has been found to be a safe and feasible alternative to conventional laparoscopic gastrectomy [10– 12,15]. Robotic surgery might also increase the accuracy and thoroughness of minimally invasive radical gastrectomy [16,17]. However, well-designed prospective randomized trials have not been published, and the practical cost-benefit trade-offs have not been determined. In this review, we discuss the current status of robotic gastrectomy, including indications, perioperative outcomes, benefits, critical limitations, and future perspectives, when it is used for the treatment of gastric cancer.
GENERAL OVERVIEW History and Development of Robotic Gastrectomy Since the initial reports of the use of robotic gastrectomy for the treatment of gastric cancer, the rate of adoption has been less rapid compared with the adoption of the use of robots for other complex urologic and thoracic procedures although these lags were dependent on surgeons or sub-specialties within general surgery [13,14,18]. Currently, laparoscopic gastrectomy for gastric cancer treatment
ß 2015 Wiley Periodicals, Inc.
remains widely accepted for treatment of relatively early gastric adenocarcinoma; however, the role of robotic surgery has not been adequately investigated, especially with regard to cost-effectiveness. When compared with laparoscopic gastrectomy, the use of robotic system rarely result in robot procedure-related complications, and acceptable short-term outcomes (including morbidity and mortality) are maintained although the reported series had small sample size, and the likelihood of robot-related complications exist regardless of robotic experiences of the surgeon [10,19]. Robotic surgery provides increased accuracy of surgical movements within the abdominal cavity, which maybe reduces blood loss and increases retrieved lymph node yield [16,19–22]. However, the better outcomes represented by these two benefits of reduced blood loss and larger number of retrieved lymph node are not consistent among reports, and some of the differences are clinically negligible even though they are statistically significant [7,23,24]. Unlike the evolution of the use of laparoscopic gastrectomy compared with open conventional surgery, the definite advantages and cost-effectiveness of robotic gastrectomy has not been proven using well-designed randomized trials [25]. Since a report of a large case series to examine robotic radical gastrectomy benefits was published [10], some experienced minimally invasive gastric surgeons have attempted to show that robotic application would provide better short-term outcomes and similar long-term outcomes, compared with conventional laparoscopic gastrectomy [16,17,20,21,26,27]. Overall it
Abbreviations: LGEA, left gastroepiploic artery; LGEV, left gastroepiploic vein; RGEV, right gastroepiploic vein; ASPDV, anterior superior pancreaticoduodenal vein; RGA, right gastric artery; CHA, common hepatic artery; GDA, gastroduodenal artery; PV, portal vein; LGV, left gastric vein; LGA, left gastric artery; SPA, splenic artery; SPV, splenic vein. Grant sponsor: Government of Korea; Grant number: 14ZC1400. * Correspondence to: Woo Jin Hyung, MD, PhD, Department of Surgery, Yonsei University College of Medicine, 50-1 Yonsei-ro Seodaemun-gu, Seoul 120-752, South Korea. Fax: þ82-2-313-8289. E-mail: [email protected] Received 11 january 2015; Accepted 8 April 2015 DOI 10.1002/jso.23926 Published online 29 May 2015 in Wiley Online Library (wileyonlinelibrary.com).
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appears that robotic gastrectomy is a feasible and safe method, but the cost-effectiveness has yet to be verified. Limited numbers of case series (Table I) and non-randomized comparative studies (Table II) were published by 2014. It is quite difficult to perform randomized controlled trials, mostly because of the considerably higher cost of robotic surgery. Consequently, all of the meta-analyses that have been published have been based on retrospective comparative study designs.
Indications and Preoperative Considerations The initial indications for the use of robotic gastric cancer surgery were similar to those of laparoscopic surgery, which are clinical diagnosis of early gastric cancers without evidence of lymph node metastasis (except for lesions for which endoscopic submucosal dissection is indicated) [28–30]. Indications for the use of robotic gastrectomy were expanded to clinical stage T1 cancer with perigastric lymph node involvement and serosa-negative gastric cancer without lymph node metastasis [31,32]. Because of the possibility of peritoneal seeding and port site metastasis, neither robotic nor laparoscopic gastrectomy are indicated for treatment of serosa-involved gastric cancer, especially in the East [33,34]. Although the published evidence is incomplete, it seems that serosa involvement would not be a clear contraindication for either of these approaches [35–37]. Nonetheless, there are specific limitations and contraindications for the minimally invasive approach, such as bulky tumors or tumors that require multivisceral resection [33]. For small or non-palpable tumors, preoperative endoscopic placement of radiopaque hemoclips or intraoperative endoscopic guidance for tumor localization is necessary to determine the proximal resection line [38– 40]. The extent of lymph node dissection is based on the Japanese Classification of Gastric Carcinoma guidelines [34].
Robotic Gastrectomy Procedure The robotic gastrectomy procedure has been described in previous articles [10,41]. In general, five trocars, including one assistant port, are used during subtotal and total robotic gastrectomy (Fig. 1A). Detailed procedures for radical subtotal and total gastrectomy have been described elsewhere [10,16,26,41–43]. The surgical cart or robotic system is usually positioned near the patient’s head, parallel to the operating table (Fig. 1B). Variation occurs in the location of the third robotic arm, which is arbitrarily placed at the either side of the patient, according to the surgeon’s preference. The side of patient most
appropriate for the placement of the third robotic arm to facilitate lymph node dissection is a point of controversy. It seems that it generally depends on the surgeon’s discretion, and no specific evidence supports one position as having an advantage over another position [17,22,43]. The location of the assistant port is determined according to the use of the third robotic arm. Since the first largest series that included 100 consecutive robotic gastrectomies by Song et al. [10], there have been concerns regarding the left hand (i.e., non-dominant) use of energy devices, such as ultrasonic shears. However, no reports of detrimental results when the left hand is used have been published. Therefore, the surgeon’s use of the non-dominant hand in the console for below-elbow and first three-finger movements might be quite accurate. In short, after camera and robotic arms are docked, the liver is first retracted with suture-gauze technique [44] to fully expose areas between the hepatoduodenal ligament and gastroesophageal junction. The greater omentum is partially divided from the midline to the left side of the patient up to the lower pole of the spleen (Fig. 2A) (Left side dissection). Then, the right side of the greater omentum is divided and detached from the mesocolon to expose infrapyloric area containing lymph node #6 (Fig. 2B; Right side dissection). After supraduodenal dissection, duodenum is transected 1–2 cm distal to the pylorus using an endoscopic linear stapler by the assistant. The right gastric artery then retracted to the patient’s left and ventral side isolated and ligated (Fig. 2C). Suprapancreatic lymph node dissection continues to retrieve soft tissue around the common hepatic artery, the celiac axis and left gastric artery for D1þ lymph node dissection. For D2 lymph node dissection, further dissection is needed around proper hepatic artery and the proximal part of the splenic artery (Fig. 2D–G). For D2 dissection in the case of spleen-preserving total gastrectomy, lymph node bearing soft tissues around the distal part of the splenic artery and splenic hilum should be dissected and the relevant vessels should be skeletonized cautiously (Fig. 2H). For reconstruction of gastrointestinal continuity after subtotal gastrectomy, gastroduodenostomy, gastrojejunostomy, or Roux-en-Y gastrojejunostomy can be performed by using endoscopic linear stapler intracorporeally. Recently, Roux-en-Y esophagojejunostomy after total gastrectomy by using endoscopic linear stapler can be performed safely during robotic gastrectomy. However, these current anastomoses techniques should be carried out by patient-side assistants.
Robotic Gastrectomy in Yonsei Robotic gastrectomy for gastric cancer in Severance Hospital, Yonsei University Health System started in 2005. The number of
TABLE I. Case Series Publications, Use of Robotic Gastrectomy for Gastric Cancer Treatment Type of surgery (TG/STG)
LN dissection (limited/D2)
Operation time (min)
Blood loss (ml)
Number of retrieved LN
Hospital stay (days)
Morbidity (%)
24 28.1 36.7 36 19–24(D1)/28–38 (D2) 43(TG)/42 (STG) 28 46 34.2
4 11.2 7.8 9 —
14.3 46.2 14 14 11
13.3
4
6 6.6 —
8 8 5
44.3 22.5 37.9 23.1
12.1 6.3 8.0 6.2
11.2 5 10 11.5
Author
Year
Number of patients
Anderson et al. [75] Patriti et al. [15] Song et al. [10] Hur et al. [76] Liu et al. [77]
2007 2008 2009 2010 2010
7 13 100 7 9
0/7 4/9 33/67 2/5 5/2(1W,1P)
— 0/13 58/42 7/0 —
420 286 231.3 205 150–440
300 103 128.2 — 10–100
Isogaki et al. [78]
2011
61
14/46(1P)
22/39
D’Annibale et al. [11] Lee et al. [79] Yu et al. [80]
2011 2011 2012
24 12 41
11/13 0/12 12/29
0/24 12/0 —
Uyama et al. [43] Jiang et al. [81] Park et al. [82] Liu et al. [83]
2012 2012 2013 2013
25 120 200 104
0/25 — 46/154 54/50(38D, 12P)
7/18 — — —
250(TG)/388 (STG) 267.5 253 285(TG)/225 (STG) 361 245 248.8 302.5(TG)/264.8 (STG)/233.2(P)
150(TG)/61.8 (STG) 30 135 180(TG)/150 (STG) 51.8 70 146.1 80.8
TG, total gastrectomy; STG, subtotal gastrectomy; W, wedge; P, proximal; D, distal.
Journal of Surgical Oncology
Robotic Gastrectomy
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TABLE II. Non-Randomized Clinical Trials, Robotic Versus Laparoscopic (vs. Open Gastrectomy) Techniques for Gastric Cancer Treatment Type of Number of Year approach patients
Author
Pernazza et al. [84] 2006 Pugliese et al. [85] 2009 Song et al. [86]
2009
Pugliese et al. [21] 2010 Kim et al. [42]
2010
Woo et al. [17]
2011
Caruso et al. [12]
2011
Yoon et al. [26]
2012
Eom et al. [27]
2012
Huang et al. [20]
2012
Kang et al. [51]
2012
Hyun et al. [87]
2013
Huang et al. [50]
2014
Junfeng et al. [49]
2014
Son et al. [16]
2014
Noshiro et al. [22]
2014
R O R L R, initial L, initial L, recent R L R L O R L R O R L R L R L O R L R L R L R L R L R L
45 45 9 46 20 20 20 16 48 16 11 12 236 591 29 120 36 65 30 62 39 64 586 100 282 38 83 72 73 120 394 51 58 21 160
Type of surgery (TG/STG) 24/21 — 0/9 0/46 0/20 0/20 0/20 0/16 0/48 0/16 0/11 0/12 62/172 108/481 12/17 37/83 36/0 65/0 0/30 0/62 7/32 7/57 179/407 16/84 37/245 9/29 18/65 8/64 10/63 26/94(92D, 2P) 118/276(261D, 15P) 51/0 58/0 0/21 0/160
LN dissection Operation Blood Number of Hospital Morbidity Mortality (limited/D2) time (min) loss (ml) retrieved LN stay (days) (%) (%) 0/45 — 0/9 0/46 16/4 10/10 12/8 0/18 0/52 2/14 3/8 0/12 131/105 312/279 0/29 0/120 — — 10/20 28/34 5/34 52/12 70/516 32/68 — 24/14 65/18 5/67 32/41 34.6 32.7 0/51 0/58 13/8 79/81
293.8 224.6 350 236 230 289 134 344 235 259.2 203.9 126.7 219.5 170.7 290 222 305.8 210.2 229.1 189.4 430 350 320 202 173 234.4 220.0 357.9 319.8 234.8 221.3 264.1 210.3 439 315
— — 92 156 94.8 — 39.5 90 148 30.3 44.7 78.8 91.6 147.9 197.6 386.1 — — 152.8 88.3 50 100 400 93.2 173.4 131.3 130.4 79.6 116.0 118.3 137.6 163.4 210.7 96 115
34.2 — 27.5 31.5 35.3 31.5 42.7 25 31 41.1 37.4 43.3 39.0 37.4 28.0 317 42.8 39.4 30.2 33.4 32.0 26.0 34.0 — — 32.8 32.6 30.6 28.1 34.6 32.7 47.2 42.8 44 40
— — 11 10 5.7 7.7 6.2 10 10 5.1 6.5 6.7 7.7 7.0 9.6 13.4 8.8 10.3 7.9 7.8 7 11 12 9.8 8.1 10.5 11.9 11.0 13.2 7.8 7.9 8.6 7.9 8 13
24.5 — — — 5 5 10 6 12.5 0 9 16 11 13.7 41.4 42.5 16.7 15.4 13 6 14.4 15.6 14.7 14 10.3 47.3 38.5 12.5 8.2 5.8 4.3 15.7 22.4 9.5 10.0
4.4 — — — 0 0 0 — — 0 0 — 0.4 0.3 0 3.3 0 0 0 0 2.6 2.6 1.4 0 0 0 0 1.4 1.4 — — 2.0 0 0 0
R, robotic; L, laparoscopic; O, open; TG, total gastrectomy; STG, subtotal gastrectomy; D, distal; P, proximal.
robotic gastrectomy cases has been gradually increased (Fig. 3). The indication of robotic gastrectomy was not different from that of laparoscopic surgery. The patients with clinical stage IA or IB disease (cT1 2N0M0 and cT1 2N1M0) were offered either robotic or laparoscopic surgery. Each patient was given comprehensive information regarding the possible approaches, instruments, cost of surgery, and the postoperative course including complications for both the robotic and laparoscopic surgery. The decision was made by the patient after having a meticulous discussion. After having comparable results with laparoscopic gastrectomy, the indication of robotic surgery was judiciously expanded to more advanced gastric cancer. Overall, intraoperative
Fig. 1.
A: Port placement. B: Docked robot arms.
Journal of Surgical Oncology
blood loss in our experience was shown to be decreased; however, clinical significance could not be found [17]. Recent analyses regarding robotic surgery in high BMI (25 kg/m2) showed that the robotic gastrectomy comparing laparoscopic counterpart have an advantages in reducing intraoperative blood loss during distal subtotal gastrectomy with D2 lymph node dissection [45]. Robotic gastrectomy also can retrieve a little bit more lymph nodes in extraperigastric area including splenic hilum during spleenpreserving total gastrectomy when compared to laparoscopic experience [16]. Largely, robotic gastrectomy may demonstrate the advantages when it is used for D2 lymph node dissection, obese patients and extended surgery.
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Fig. 2. Intraoperative view during robotic gastrectomy. A: Isolation of the LGEA and LGEV. B: Exposure of the RGEV and ASPDV. C: Isolation of the RGA. D: Dissection of the hepatoduodenal ligament and exposure of PV. E: Isolation of the LGV. F: Isolation and ligation of the LGA. G: Dissection along the SPA. H: View after spleen-preserving hilar lymph node dissection
PERIOPERATIVE OUTCOMES Operation Time In general, robotic gastrectomy requires a longer operation time compared with laparoscopic surgery (ranged 220–430 min vs. 171–350 min, respectively) and the difference varies from 40 to 110 min and depends on the extent of surgery [16,17,20,21,26,27,42]. The docking time was initially regarded as one of the key factors that increases operation time, but docking time does not seem to be a contributing factor [17,20]. Longer operation time and anesthesia time can affect patient recovery [46–48]. Although few publication describe the negative effects robotic gastrectomy’s longer operation time, longer operation times can have detrimental effects. Thus, safety should be investigated in patients who may be susceptible as a result of longer surgery and anesthesia times.
Blood Loss Although it is not an obvious difference, several investigators have reported that robotic gastrectomy results in reduced blood loss compared with laparoscopic gastrectomy (ranged 50–118 vs. 100–174 ml, respectively) [17,20,21,49–51]. Recent meta-analyses comparing robotic and laparoscopic gastrectomy revealed that there is significant reduction in blood loss when robotic gastrectomy is used [24,52,53]. It is quite noteworthy that this result was achieved even during early experiences with the technique. However, it is difficult to conclude that it was not the result of the robotic surgeries being performed by experienced laparoscopic gastric surgeons.
Moreover, a study showed increased blood loss, when surgery is performed using a robot in their early experience [27]. In general, the reduced blood loss may result from robotic system advantages such as 1 the three-dimensional view and EndoWrist function. However, this statistically significant difference is negligible unless the small amount of progress in blood loss reduction has a certain clinical or oncologic benefit [23]. Reduced blood loss during gastrectomy, especially for locally advanced cancer, is considered to have potential oncologic benefits because of reductions in free cancer cell dissemination and post-surgical maintenance of immune function [54–56]. These potential benefits may be non-negligible.
Length of Hospital Stay Compared with open surgery, minimally invasive gastrectomy is less stressful for the patient, thus the length of the post-surgical hospital stay is reduced. Almost all studies of laparoscopic gastrectomy have found that length of hospital stay is shorter [2,4,7]. However, robotic surgery requires a longer operation time and the same number of trocars as laparoscopic gastrectomy, so no further substantial reduction in length of hospital stay has been reported. Most investigators found no differences in length of hospital stay when they compared robotic with laparoscopic gastrectomy [57]. One study that compared robotic gastrectomy with laparoscopic surgery outcomes revealed that a significantly larger percentage of patients who underwent robotic gastrectomy was discharged by postoperative day 5, but the median hospital stay was not different between the two groups [17]. A smallsized comparative study showed earlier discharge in robotic gastrectomy group compared to open and laparoscopic gastrectomy group (5.1 vs. 6.7 vs. 6.5 days, respectively, P < 0.0001) [42]. The results of a recent study comparing robotic (n ¼ 21) with laparoscopic (n ¼ 160) distal subtotal gastrectomy in Japan indicated that the robotic group had a significantly shorter mean postoperative hospital stay (8 vs. 13 days, P ¼ 0.0295) [22].
Cost
Fig. 3. Annual number of robotic gastrectomy for gastric cancer. Journal of Surgical Oncology
The use of robotic systems remains controversial, mainly due to the substantial expense compared with other procedures. The higher cost has been noted as a main disadvantage in all reports. A retrospective analysis investigating the differences in the overall costs between robotic and laparoscopic distal subtotal gastrectomy revealed that the estimated difference was approximately 4,800,000 KRW (s3100) [25]. The principal reason for the higher robotic gastrectomy-associated cost
Robotic Gastrectomy is the cost of the robotic system itself, and the depreciation reserve. As other reports have indicated, this current higher cost is not acceptable. The difference in total cost between robot and laparoscopic gastrectomy has also been estimated to be approximately 2,800 USD [50]. Moreover, the difference in the costs could be increased if operation cost from extended length of robotic gastrectomy is thoroughly assessed.
Learning Curve Initially, robotic gastrectomy was criticized due to its longer operation time. However, the safety and efficacy of this new approach should be proven despite this extended operation time. The longer operation time is likely negligible because there has been rapid progress toward shortening operation times. This progress indicates that the robotic learning curve is shorter, compared with laparoscopic surgery. Forty to sixty cases of surgical experience are required to overcome the learning curves associated with laparoscopic gastrectomy [58–61], but 11–25 cases are required for robotic surgery [11,20,27,43,50,51]. To date, this procedure has been investigated using the initial experiences of very experienced laparoscopic gastric surgeons. A well-designed study of the role and efficacy of minimally invasive gastrectomy performed by novice surgeons is needed. Shorter learning curves would make it easier for inexperienced surgeons to adopt minimally invasive surgical techniques for gastric cancer treatment [62]. Shorter learning curves might also result in experienced surgeons more easily adopting advanced or complicated procedures for gastric cancer treatment.
ONCOLOGIC EFFICACY AND OUTCOMES Quality of Lymph Node Dissection Initially, the indications for robotic gastrectomy were the same as the indications for laparoscopic surgery. Both are performed relatively early gastric cancer. However, compared with laparoscopy, robotic gastrectomy can yield more lymph nodes in the same extent of lymph node dissection [16,49]. The differences in retrieved lymph nodes occur in the extraperigastric area (2nd tier). A comparative study of spleenpreserving total gastrectomy revealed that robotic gastrectomy consistently retrieved a larger number of lymph nodes at each station, regardless of statistical significance [16]. Robotic gastrectomy yielded significantly larger numbers of retrieved lymph nodes around the splenic artery and hilum. These areas contain the suprapancreatic or splenic hilar lymph nodes and are crucial for D2 lymph node dissection. The articulated function and stable image can enable surgeons to thoroughly retrieve lymph nodes around complicated vascular structures, such as the splenic vessels and hilum. Recently, a meta-analysis that compared laparoscopic gastrectomy to open gastrectomy revealed that laparoscopic gastrectomy retrieves a significantly lower number of lymph nodes compared with open gastrectomy, although the proportion of patients with
Robotic Gastrectomy for Gastric Cancer TAEIL SON, MD1
AND
WOO JIN HYUNG, MD, PhD2,3,4*
1
Department of Surgery, Eulji Medical Center, Eulji University School of Medicine, Seoul, South Korea 2 Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea 3 Gastric Cancer Center, Yonsei Cancer Hospital, Yonsei University Health System, Seoul, South Korea 4 Robot and MIS Center, Severance Hospital, Yonsei University Health System, Seoul, South Korea
Robotic surgery for gastric cancer overcomes technical difficulties with laparoscopic gastrectomy. Its benefits include reduced intraoperative bleeding and shorter hospital stays; it is also easier to learn. Because accuracy increases during lymphadenectomy, a larger number of lymph nodes is likely to be retrieved using robotic gastrectomy. Higher costs and longer operation times have hindered the widespread adaptation and use of robotic surgery. In this review, we summarize the current status and issues regarding robotic gastrectomy.
J. Surg. Oncol. 2015;112:271–278. © 2015 Wiley Periodicals, Inc.
KEY WORDS: stomach neoplasms; gastrectomy; robotics; minimally invasive surgery
INTRODUCTION Less invasive surgical techniques have been developed to facilitate patients’ recovery after gastrectomy. The use of laparoscopic surgery for gastric cancer was first reported in 1994 [1]. Much evidence has accumulated after the initiation of minimally invasive gastrectomy, which supports the short-term benefits of the use of this procedure for early gastric cancer patients. These benefits include reduced pain, early recovery of intestinal function, decreased inflammatory response, and a shorter hospital stay, while maintaining comparable oncologic safety [2–5]. In spite of these advantages, however, technical difficulties and critical issues (i.e., D2 lymph node dissection, anastomosis methods, total gastrectomy, and oncologic safety for advanced cancer) remain to be solved before the indications for minimally invasive gastrectomy for gastric cancer are expanded [6–8]. The new technology represented by the use of the surgical robot was expected to resolve the problems associated with laparoscopic surgery [9]. Experienced laparoscopic surgeons adopted robotic surgery procedures for gastric cancer treatment [10–12]. Within a decade after the initial reports describing its use for the treatment of gastric cancer [13,14], robotic gastrectomy has been found to be a safe and feasible alternative to conventional laparoscopic gastrectomy [10– 12,15]. Robotic surgery might also increase the accuracy and thoroughness of minimally invasive radical gastrectomy [16,17]. However, well-designed prospective randomized trials have not been published, and the practical cost-benefit trade-offs have not been determined. In this review, we discuss the current status of robotic gastrectomy, including indications, perioperative outcomes, benefits, critical limitations, and future perspectives, when it is used for the treatment of gastric cancer.
GENERAL OVERVIEW History and Development of Robotic Gastrectomy Since the initial reports of the use of robotic gastrectomy for the treatment of gastric cancer, the rate of adoption has been less rapid compared with the adoption of the use of robots for other complex urologic and thoracic procedures although these lags were dependent on surgeons or sub-specialties within general surgery [13,14,18]. Currently, laparoscopic gastrectomy for gastric cancer treatment
ß 2015 Wiley Periodicals, Inc.
remains widely accepted for treatment of relatively early gastric adenocarcinoma; however, the role of robotic surgery has not been adequately investigated, especially with regard to cost-effectiveness. When compared with laparoscopic gastrectomy, the use of robotic system rarely result in robot procedure-related complications, and acceptable short-term outcomes (including morbidity and mortality) are maintained although the reported series had small sample size, and the likelihood of robot-related complications exist regardless of robotic experiences of the surgeon [10,19]. Robotic surgery provides increased accuracy of surgical movements within the abdominal cavity, which maybe reduces blood loss and increases retrieved lymph node yield [16,19–22]. However, the better outcomes represented by these two benefits of reduced blood loss and larger number of retrieved lymph node are not consistent among reports, and some of the differences are clinically negligible even though they are statistically significant [7,23,24]. Unlike the evolution of the use of laparoscopic gastrectomy compared with open conventional surgery, the definite advantages and cost-effectiveness of robotic gastrectomy has not been proven using well-designed randomized trials [25]. Since a report of a large case series to examine robotic radical gastrectomy benefits was published [10], some experienced minimally invasive gastric surgeons have attempted to show that robotic application would provide better short-term outcomes and similar long-term outcomes, compared with conventional laparoscopic gastrectomy [16,17,20,21,26,27]. Overall it
Abbreviations: LGEA, left gastroepiploic artery; LGEV, left gastroepiploic vein; RGEV, right gastroepiploic vein; ASPDV, anterior superior pancreaticoduodenal vein; RGA, right gastric artery; CHA, common hepatic artery; GDA, gastroduodenal artery; PV, portal vein; LGV, left gastric vein; LGA, left gastric artery; SPA, splenic artery; SPV, splenic vein. Grant sponsor: Government of Korea; Grant number: 14ZC1400. * Correspondence to: Woo Jin Hyung, MD, PhD, Department of Surgery, Yonsei University College of Medicine, 50-1 Yonsei-ro Seodaemun-gu, Seoul 120-752, South Korea. Fax: þ82-2-313-8289. E-mail: [email protected] Received 11 january 2015; Accepted 8 April 2015 DOI 10.1002/jso.23926 Published online 29 May 2015 in Wiley Online Library (wileyonlinelibrary.com).
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appears that robotic gastrectomy is a feasible and safe method, but the cost-effectiveness has yet to be verified. Limited numbers of case series (Table I) and non-randomized comparative studies (Table II) were published by 2014. It is quite difficult to perform randomized controlled trials, mostly because of the considerably higher cost of robotic surgery. Consequently, all of the meta-analyses that have been published have been based on retrospective comparative study designs.
Indications and Preoperative Considerations The initial indications for the use of robotic gastric cancer surgery were similar to those of laparoscopic surgery, which are clinical diagnosis of early gastric cancers without evidence of lymph node metastasis (except for lesions for which endoscopic submucosal dissection is indicated) [28–30]. Indications for the use of robotic gastrectomy were expanded to clinical stage T1 cancer with perigastric lymph node involvement and serosa-negative gastric cancer without lymph node metastasis [31,32]. Because of the possibility of peritoneal seeding and port site metastasis, neither robotic nor laparoscopic gastrectomy are indicated for treatment of serosa-involved gastric cancer, especially in the East [33,34]. Although the published evidence is incomplete, it seems that serosa involvement would not be a clear contraindication for either of these approaches [35–37]. Nonetheless, there are specific limitations and contraindications for the minimally invasive approach, such as bulky tumors or tumors that require multivisceral resection [33]. For small or non-palpable tumors, preoperative endoscopic placement of radiopaque hemoclips or intraoperative endoscopic guidance for tumor localization is necessary to determine the proximal resection line [38– 40]. The extent of lymph node dissection is based on the Japanese Classification of Gastric Carcinoma guidelines [34].
Robotic Gastrectomy Procedure The robotic gastrectomy procedure has been described in previous articles [10,41]. In general, five trocars, including one assistant port, are used during subtotal and total robotic gastrectomy (Fig. 1A). Detailed procedures for radical subtotal and total gastrectomy have been described elsewhere [10,16,26,41–43]. The surgical cart or robotic system is usually positioned near the patient’s head, parallel to the operating table (Fig. 1B). Variation occurs in the location of the third robotic arm, which is arbitrarily placed at the either side of the patient, according to the surgeon’s preference. The side of patient most
appropriate for the placement of the third robotic arm to facilitate lymph node dissection is a point of controversy. It seems that it generally depends on the surgeon’s discretion, and no specific evidence supports one position as having an advantage over another position [17,22,43]. The location of the assistant port is determined according to the use of the third robotic arm. Since the first largest series that included 100 consecutive robotic gastrectomies by Song et al. [10], there have been concerns regarding the left hand (i.e., non-dominant) use of energy devices, such as ultrasonic shears. However, no reports of detrimental results when the left hand is used have been published. Therefore, the surgeon’s use of the non-dominant hand in the console for below-elbow and first three-finger movements might be quite accurate. In short, after camera and robotic arms are docked, the liver is first retracted with suture-gauze technique [44] to fully expose areas between the hepatoduodenal ligament and gastroesophageal junction. The greater omentum is partially divided from the midline to the left side of the patient up to the lower pole of the spleen (Fig. 2A) (Left side dissection). Then, the right side of the greater omentum is divided and detached from the mesocolon to expose infrapyloric area containing lymph node #6 (Fig. 2B; Right side dissection). After supraduodenal dissection, duodenum is transected 1–2 cm distal to the pylorus using an endoscopic linear stapler by the assistant. The right gastric artery then retracted to the patient’s left and ventral side isolated and ligated (Fig. 2C). Suprapancreatic lymph node dissection continues to retrieve soft tissue around the common hepatic artery, the celiac axis and left gastric artery for D1þ lymph node dissection. For D2 lymph node dissection, further dissection is needed around proper hepatic artery and the proximal part of the splenic artery (Fig. 2D–G). For D2 dissection in the case of spleen-preserving total gastrectomy, lymph node bearing soft tissues around the distal part of the splenic artery and splenic hilum should be dissected and the relevant vessels should be skeletonized cautiously (Fig. 2H). For reconstruction of gastrointestinal continuity after subtotal gastrectomy, gastroduodenostomy, gastrojejunostomy, or Roux-en-Y gastrojejunostomy can be performed by using endoscopic linear stapler intracorporeally. Recently, Roux-en-Y esophagojejunostomy after total gastrectomy by using endoscopic linear stapler can be performed safely during robotic gastrectomy. However, these current anastomoses techniques should be carried out by patient-side assistants.
Robotic Gastrectomy in Yonsei Robotic gastrectomy for gastric cancer in Severance Hospital, Yonsei University Health System started in 2005. The number of
TABLE I. Case Series Publications, Use of Robotic Gastrectomy for Gastric Cancer Treatment Type of surgery (TG/STG)
LN dissection (limited/D2)
Operation time (min)
Blood loss (ml)
Number of retrieved LN
Hospital stay (days)
Morbidity (%)
24 28.1 36.7 36 19–24(D1)/28–38 (D2) 43(TG)/42 (STG) 28 46 34.2
4 11.2 7.8 9 —
14.3 46.2 14 14 11
13.3
4
6 6.6 —
8 8 5
44.3 22.5 37.9 23.1
12.1 6.3 8.0 6.2
11.2 5 10 11.5
Author
Year
Number of patients
Anderson et al. [75] Patriti et al. [15] Song et al. [10] Hur et al. [76] Liu et al. [77]
2007 2008 2009 2010 2010
7 13 100 7 9
0/7 4/9 33/67 2/5 5/2(1W,1P)
— 0/13 58/42 7/0 —
420 286 231.3 205 150–440
300 103 128.2 — 10–100
Isogaki et al. [78]
2011
61
14/46(1P)
22/39
D’Annibale et al. [11] Lee et al. [79] Yu et al. [80]
2011 2011 2012
24 12 41
11/13 0/12 12/29
0/24 12/0 —
Uyama et al. [43] Jiang et al. [81] Park et al. [82] Liu et al. [83]
2012 2012 2013 2013
25 120 200 104
0/25 — 46/154 54/50(38D, 12P)
7/18 — — —
250(TG)/388 (STG) 267.5 253 285(TG)/225 (STG) 361 245 248.8 302.5(TG)/264.8 (STG)/233.2(P)
150(TG)/61.8 (STG) 30 135 180(TG)/150 (STG) 51.8 70 146.1 80.8
TG, total gastrectomy; STG, subtotal gastrectomy; W, wedge; P, proximal; D, distal.
Journal of Surgical Oncology
Robotic Gastrectomy
273
TABLE II. Non-Randomized Clinical Trials, Robotic Versus Laparoscopic (vs. Open Gastrectomy) Techniques for Gastric Cancer Treatment Type of Number of Year approach patients
Author
Pernazza et al. [84] 2006 Pugliese et al. [85] 2009 Song et al. [86]
2009
Pugliese et al. [21] 2010 Kim et al. [42]
2010
Woo et al. [17]
2011
Caruso et al. [12]
2011
Yoon et al. [26]
2012
Eom et al. [27]
2012
Huang et al. [20]
2012
Kang et al. [51]
2012
Hyun et al. [87]
2013
Huang et al. [50]
2014
Junfeng et al. [49]
2014
Son et al. [16]
2014
Noshiro et al. [22]
2014
R O R L R, initial L, initial L, recent R L R L O R L R O R L R L R L O R L R L R L R L R L R L
45 45 9 46 20 20 20 16 48 16 11 12 236 591 29 120 36 65 30 62 39 64 586 100 282 38 83 72 73 120 394 51 58 21 160
Type of surgery (TG/STG) 24/21 — 0/9 0/46 0/20 0/20 0/20 0/16 0/48 0/16 0/11 0/12 62/172 108/481 12/17 37/83 36/0 65/0 0/30 0/62 7/32 7/57 179/407 16/84 37/245 9/29 18/65 8/64 10/63 26/94(92D, 2P) 118/276(261D, 15P) 51/0 58/0 0/21 0/160
LN dissection Operation Blood Number of Hospital Morbidity Mortality (limited/D2) time (min) loss (ml) retrieved LN stay (days) (%) (%) 0/45 — 0/9 0/46 16/4 10/10 12/8 0/18 0/52 2/14 3/8 0/12 131/105 312/279 0/29 0/120 — — 10/20 28/34 5/34 52/12 70/516 32/68 — 24/14 65/18 5/67 32/41 34.6 32.7 0/51 0/58 13/8 79/81
293.8 224.6 350 236 230 289 134 344 235 259.2 203.9 126.7 219.5 170.7 290 222 305.8 210.2 229.1 189.4 430 350 320 202 173 234.4 220.0 357.9 319.8 234.8 221.3 264.1 210.3 439 315
— — 92 156 94.8 — 39.5 90 148 30.3 44.7 78.8 91.6 147.9 197.6 386.1 — — 152.8 88.3 50 100 400 93.2 173.4 131.3 130.4 79.6 116.0 118.3 137.6 163.4 210.7 96 115
34.2 — 27.5 31.5 35.3 31.5 42.7 25 31 41.1 37.4 43.3 39.0 37.4 28.0 317 42.8 39.4 30.2 33.4 32.0 26.0 34.0 — — 32.8 32.6 30.6 28.1 34.6 32.7 47.2 42.8 44 40
— — 11 10 5.7 7.7 6.2 10 10 5.1 6.5 6.7 7.7 7.0 9.6 13.4 8.8 10.3 7.9 7.8 7 11 12 9.8 8.1 10.5 11.9 11.0 13.2 7.8 7.9 8.6 7.9 8 13
24.5 — — — 5 5 10 6 12.5 0 9 16 11 13.7 41.4 42.5 16.7 15.4 13 6 14.4 15.6 14.7 14 10.3 47.3 38.5 12.5 8.2 5.8 4.3 15.7 22.4 9.5 10.0
4.4 — — — 0 0 0 — — 0 0 — 0.4 0.3 0 3.3 0 0 0 0 2.6 2.6 1.4 0 0 0 0 1.4 1.4 — — 2.0 0 0 0
R, robotic; L, laparoscopic; O, open; TG, total gastrectomy; STG, subtotal gastrectomy; D, distal; P, proximal.
robotic gastrectomy cases has been gradually increased (Fig. 3). The indication of robotic gastrectomy was not different from that of laparoscopic surgery. The patients with clinical stage IA or IB disease (cT1 2N0M0 and cT1 2N1M0) were offered either robotic or laparoscopic surgery. Each patient was given comprehensive information regarding the possible approaches, instruments, cost of surgery, and the postoperative course including complications for both the robotic and laparoscopic surgery. The decision was made by the patient after having a meticulous discussion. After having comparable results with laparoscopic gastrectomy, the indication of robotic surgery was judiciously expanded to more advanced gastric cancer. Overall, intraoperative
Fig. 1.
A: Port placement. B: Docked robot arms.
Journal of Surgical Oncology
blood loss in our experience was shown to be decreased; however, clinical significance could not be found [17]. Recent analyses regarding robotic surgery in high BMI (25 kg/m2) showed that the robotic gastrectomy comparing laparoscopic counterpart have an advantages in reducing intraoperative blood loss during distal subtotal gastrectomy with D2 lymph node dissection [45]. Robotic gastrectomy also can retrieve a little bit more lymph nodes in extraperigastric area including splenic hilum during spleenpreserving total gastrectomy when compared to laparoscopic experience [16]. Largely, robotic gastrectomy may demonstrate the advantages when it is used for D2 lymph node dissection, obese patients and extended surgery.
274
Son and Hyung
Fig. 2. Intraoperative view during robotic gastrectomy. A: Isolation of the LGEA and LGEV. B: Exposure of the RGEV and ASPDV. C: Isolation of the RGA. D: Dissection of the hepatoduodenal ligament and exposure of PV. E: Isolation of the LGV. F: Isolation and ligation of the LGA. G: Dissection along the SPA. H: View after spleen-preserving hilar lymph node dissection
PERIOPERATIVE OUTCOMES Operation Time In general, robotic gastrectomy requires a longer operation time compared with laparoscopic surgery (ranged 220–430 min vs. 171–350 min, respectively) and the difference varies from 40 to 110 min and depends on the extent of surgery [16,17,20,21,26,27,42]. The docking time was initially regarded as one of the key factors that increases operation time, but docking time does not seem to be a contributing factor [17,20]. Longer operation time and anesthesia time can affect patient recovery [46–48]. Although few publication describe the negative effects robotic gastrectomy’s longer operation time, longer operation times can have detrimental effects. Thus, safety should be investigated in patients who may be susceptible as a result of longer surgery and anesthesia times.
Blood Loss Although it is not an obvious difference, several investigators have reported that robotic gastrectomy results in reduced blood loss compared with laparoscopic gastrectomy (ranged 50–118 vs. 100–174 ml, respectively) [17,20,21,49–51]. Recent meta-analyses comparing robotic and laparoscopic gastrectomy revealed that there is significant reduction in blood loss when robotic gastrectomy is used [24,52,53]. It is quite noteworthy that this result was achieved even during early experiences with the technique. However, it is difficult to conclude that it was not the result of the robotic surgeries being performed by experienced laparoscopic gastric surgeons.
Moreover, a study showed increased blood loss, when surgery is performed using a robot in their early experience [27]. In general, the reduced blood loss may result from robotic system advantages such as 1 the three-dimensional view and EndoWrist function. However, this statistically significant difference is negligible unless the small amount of progress in blood loss reduction has a certain clinical or oncologic benefit [23]. Reduced blood loss during gastrectomy, especially for locally advanced cancer, is considered to have potential oncologic benefits because of reductions in free cancer cell dissemination and post-surgical maintenance of immune function [54–56]. These potential benefits may be non-negligible.
Length of Hospital Stay Compared with open surgery, minimally invasive gastrectomy is less stressful for the patient, thus the length of the post-surgical hospital stay is reduced. Almost all studies of laparoscopic gastrectomy have found that length of hospital stay is shorter [2,4,7]. However, robotic surgery requires a longer operation time and the same number of trocars as laparoscopic gastrectomy, so no further substantial reduction in length of hospital stay has been reported. Most investigators found no differences in length of hospital stay when they compared robotic with laparoscopic gastrectomy [57]. One study that compared robotic gastrectomy with laparoscopic surgery outcomes revealed that a significantly larger percentage of patients who underwent robotic gastrectomy was discharged by postoperative day 5, but the median hospital stay was not different between the two groups [17]. A smallsized comparative study showed earlier discharge in robotic gastrectomy group compared to open and laparoscopic gastrectomy group (5.1 vs. 6.7 vs. 6.5 days, respectively, P < 0.0001) [42]. The results of a recent study comparing robotic (n ¼ 21) with laparoscopic (n ¼ 160) distal subtotal gastrectomy in Japan indicated that the robotic group had a significantly shorter mean postoperative hospital stay (8 vs. 13 days, P ¼ 0.0295) [22].
Cost
Fig. 3. Annual number of robotic gastrectomy for gastric cancer. Journal of Surgical Oncology
The use of robotic systems remains controversial, mainly due to the substantial expense compared with other procedures. The higher cost has been noted as a main disadvantage in all reports. A retrospective analysis investigating the differences in the overall costs between robotic and laparoscopic distal subtotal gastrectomy revealed that the estimated difference was approximately 4,800,000 KRW (s3100) [25]. The principal reason for the higher robotic gastrectomy-associated cost
Robotic Gastrectomy is the cost of the robotic system itself, and the depreciation reserve. As other reports have indicated, this current higher cost is not acceptable. The difference in total cost between robot and laparoscopic gastrectomy has also been estimated to be approximately 2,800 USD [50]. Moreover, the difference in the costs could be increased if operation cost from extended length of robotic gastrectomy is thoroughly assessed.
Learning Curve Initially, robotic gastrectomy was criticized due to its longer operation time. However, the safety and efficacy of this new approach should be proven despite this extended operation time. The longer operation time is likely negligible because there has been rapid progress toward shortening operation times. This progress indicates that the robotic learning curve is shorter, compared with laparoscopic surgery. Forty to sixty cases of surgical experience are required to overcome the learning curves associated with laparoscopic gastrectomy [58–61], but 11–25 cases are required for robotic surgery [11,20,27,43,50,51]. To date, this procedure has been investigated using the initial experiences of very experienced laparoscopic gastric surgeons. A well-designed study of the role and efficacy of minimally invasive gastrectomy performed by novice surgeons is needed. Shorter learning curves would make it easier for inexperienced surgeons to adopt minimally invasive surgical techniques for gastric cancer treatment [62]. Shorter learning curves might also result in experienced surgeons more easily adopting advanced or complicated procedures for gastric cancer treatment.
ONCOLOGIC EFFICACY AND OUTCOMES Quality of Lymph Node Dissection Initially, the indications for robotic gastrectomy were the same as the indications for laparoscopic surgery. Both are performed relatively early gastric cancer. However, compared with laparoscopy, robotic gastrectomy can yield more lymph nodes in the same extent of lymph node dissection [16,49]. The differences in retrieved lymph nodes occur in the extraperigastric area (2nd tier). A comparative study of spleenpreserving total gastrectomy revealed that robotic gastrectomy consistently retrieved a larger number of lymph nodes at each station, regardless of statistical significance [16]. Robotic gastrectomy yielded significantly larger numbers of retrieved lymph nodes around the splenic artery and hilum. These areas contain the suprapancreatic or splenic hilar lymph nodes and are crucial for D2 lymph node dissection. The articulated function and stable image can enable surgeons to thoroughly retrieve lymph nodes around complicated vascular structures, such as the splenic vessels and hilum. Recently, a meta-analysis that compared laparoscopic gastrectomy to open gastrectomy revealed that laparoscopic gastrectomy retrieves a significantly lower number of lymph nodes compared with open gastrectomy, although the proportion of patients with
