Surg Endosc DOI 10.1007/s00464-015-4372-x
and Other Interventional Techniques
Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer Young-Woo Kim1 • Daniel Reim1 • Ji Yeon Park1 • Bang Wool Eom1 Myeong-Cherl Kook1 • Keun Won Ryu1 • Hong Man Yoon1
•
Received: 16 February 2015 / Accepted: 23 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Purpose Despite theoretical advantages, no clear benefit was proven for initial application of robotic surgery for gastric cancer so far. The aim of this analysis was to examine the role of robotic surgery regarding nodal dissection technically demanding areas compared to conventional laparoscopic surgery. Methods This analysis included 87 patients who underwent robot-assisted distal gastrectomy (RADG) and 288 patients who underwent laparoscopy-assisted distal gastrectomy (LADG) at the National Cancer Center, Korea, between February 2009 and September 2011. Clinicopathologic data, surgery-related data, postoperative morbidity, and pathologic data for each nodal station were analyzed. Results Time to flatulence was 3.5 ± 0.8 days for RADG and 3.8 ± 0.8 days for LADG (P = 0.01). Postoperative hospital stay was 6.7 ± 1.0 days in RADG and 7.4 ± 2.4 days in LADG (P \ 0.001).The number of dissected lymph nodes was 37.1 ± 12.9 in the RADG group and 34.1 ± 12.1 in the LADG group (P = 0.044). In patients undergoing D2 gastrectomy, the number of dissected lymph nodes in the N2 area was 16.3 ± 7.7 for RADG and 13.2 ± 5.3 for LADG (P = 0.001). The number of dissected lymph nodes around the splenic artery area was 2.9 ± 2.9 in RADG and 2.2 ± 2.0 in LADG (P = 0.04). Regarding postoperative complications, there was no statistically significant difference [five patients
& Hong Man Yoon [email protected] 1
Gastric Cancer Branch, Research Institute and Hospital, National Cancer Center, 323 Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do 410-769, Korea
(5.7 %) in RADG and 26 patients (9 %) in LADG) (P = 0.330)]. Conclusion RADG could provide an advantage over LADG in the dissection of the N2 area lymph nodes, especially around the splenic artery area. Keywords Gastric cancer Robotic surgery D2 gastrectomy Lymph node dissection Case–control study
Since the introduction of robotic surgery, its role is controversly debated especially in relation to the cost of the procedure [1, 2]. The general idea of evidence-based medicine, which is strongly backed up by health economics, is considered to evoke innovative and improved treatment [3]. Therefore, evaluation of robotic surgery is supposed to provide improvements for diverse outcome measures, such as quality of life and survival outcomes in oncologic surgery. Robotic surgery is now vigorously implemented in clinical practice without proof of concept from randomized controlled trial. In contrast, laparoscopic surgery for gastric cancer has been quite accepted for early cancer proven by various published clinical trials and numerous articles demonstrating many advantages over open surgery [4–10]. In contrast, application of robotic surgery for early gastric cancer has failed to show any clear benefit. However, initial data mainly from Korea at least demonstrated feasibility, safety, and comparable outcomes. [1, 2, 11–14]. Apparently, next step for robotic gastrectomy for gastric cancer should focus on the identification of some specific benefit. Clinical studies on laparoscopic gastrectomy for advanced gastric cancer unveiled technical difficulties in the dissection of the suprapancreatic area. The COACT 1001 trial data showed that the noncompliance rate of
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Surg Endosc
lymph node dissection was significantly higher in stage III disease. In Western countries and the countries without a national screening program, gastric cancer is mainly detected in advanced stages [15]. Therefore, the major area of research in minimally invasive surgery should focus on advanced gastric cancer. The major barrier of minimally invasive surgery for this disease considered to be the technically demanding suprapancreatic nodal dissection. Considering the theoretical advantages of robotic surgery, the suprapancreatic area could be more easily and effectively cleared. The main purpose of this analysis was to define mainly the oncologic advantages of robotic surgery for gastric cancer over laparoscopic surgery.
Methods
Results Demographics Between February 2009 and September 2011, 87 patients underwent RADG and 288 patients underwent LADG by a single surgeon (YWK). The patient characteristics are shown in Table 1. Patients in the RADG group were younger than those receiving LADG. (P \ 0.001) No significant differences existed with respect to gender and body mass index (BMI) between the two groups. Regarding the history of abdominal surgeries and comorbidities, there was no significant difference between the two groups. Intra-operatively, 3.4 and 5.9 % of patients in the RADG and LADG groups underwent combined resections, mainly cholecystectomy not influencing surgical outcome considerably (P = 0.586), and therefore were included in the final analysis.
Study approval Surgical outcomes This study followed the Declaration of Helsinki as a statement of ethical principles for medical research involving human subjects, including research on identifiable human material and data, and was approved by the institutional review board of NCCK. (IRB No. NCC20140177). Patients From February 2009, when the da Vinci surgical system (Intuitive Surgical Inc., Sunnyvale, CA, USA) was introduced at our hospital, to September 2011, a total of 2039 patients underwent curative resection for gastric cancer at National Cancer Center, Korea (NCCK). To see whether the surgical method influences the outcome, most experienced and having higher caseloads surgeon’s cases were selected. Other inclusion criteria were clinical stages T1N0, T1N1, or T2N0 diagnosed by esophagogastrodudenoscopy, endoscopic ultrasound and abdominopelvic computed tomography, and gastric cancer locations that guaranteed the application of subtotal gastrectomy. Data for clinicopathologic, surgical, and oncologic outcomes were extracted from the prospectively documented database at the Center for Gastric Cancer, NCCK. Statistical analysis Statistical analysis was performed using the Student’s t test for continuous variables and the Chi-square test for categorical variables. Two-sided P values were calculated for all tests and are reported here. P values \0.05 were considered to indicate statistical significance. The SAS (SAS Institute Inc., Cary, NC, USA) program was used for analyses.
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The short-term data of surgical outcomes in the two groups are shown in Table 2. The postoperative hospital stay was significantly shorter in the RADG group than in the LADG group. (6.7 ± 1.0 vs. 7.4 ± 2.4 days, P \ 0.001). The period which elapsed before passage of flatulence was shorter in RADG than in LADG. (3.5 ± 0.8 vs. 3.8 ± 0.8 days, P = 0.01). The difference between the preoperative and dayof-surgery hemoglobin levels was not significantly different between the two groups. The mean operative time for the RADG group was significantly longer than for the LADG group (248.4 ± 40.1 vs. 230.0 ± 55.8 min; P \ 0.001). Five patients (5.7 %) in the RADG group developed complications: four patients (4.6 %) had minor complications, and one patient (1.1 %) had a major complication. Twenty-six patients (9.0 %) in the LADG group demonstrated complications: 16 patients (4.5 %) developed minor and 10 patients (3.5 %) revealed major complications. There were no significant differences in overall complication rate, and major and minor complications between the two groups. (P = 0.330, 0.469, and [0.999, respectively). Regarding mortality, there was one case in each group during the postoperative period within 1 month without statistical significance (P = 0.411). In the RADG group, the patient died of acute myocardial infarction on postoperative day 1 without any surgical problem, negligible bleeding of \20 ml and short operating time. In the LADG group, one old aged patient died of acute mesenteric infarction of unknown cause, most probably thromboembolism. There were two patients who underwent conversion to open surgery during RADG due to massive adhesion in the abdominal cavity because of previous surgery. The other patient had a small bowel injury by the trocar during insertion.
Surg Endosc Table 1 Demographic data
RADG (n = 87)
LADG (n = 288)
P
Age (years)
54.1 ± 12.0
60.5 ± 11.0
\0.001*
Gender (male/female)
46: 41
170: 118
0.309
24.1 ± 3.4
24.0 ± 4.3
0.859*
None
80 (92 %)
241 (83.7 %)
0.054
Appendectomy
5 (5.7 %)
27 (9.4 %)
Gynecologic procedure
1 (1.1 %)
12 (4.2 %)
Laparoscopic cholecystectomy
0 (0 %)
1 (0.3 %)
Others
1 (1.1 %)
7 (2.4 %)
None
54 (62.1 %)
144 (50 %)
DM
8 (9.2 %)
40 (13.9 %)
Hypertension
27 (31 %)
104 (36.1 %)
Heart disease
3 (3.4 %)
8 (3.1 %)
Pulmonary disease Liver cirrhosis
4 (4.5 %) 0 (0 %)
12 (4.2 %) 2 (0.7 %)
2
BMI (kg/m ) Previous abdominal surgery
Comorbidity
Cerbrovascular disease
0 (0 %)
2 (0.7 %)
Others
2 (2.3 %)
10 (3.3 %)
None
84 (96.6 %)
271 (94.1 %)
Gallbladder
3 (3.4 %)
9 (3.1 %)
0.048
Combined resection
Salphinx, ovary, uterus
0 (0 %)
4 (1.4 %)
Others
0 (0 %)
4 (1.4 %)
Less than D2
8 (9.2 %)
95 (33.0 %)
D2
79 (90.8 %)
193 (67.0 %)
0.586à
\0.001
Lymph node dissection
RADG Robot-assisted distal gastrectomy, LADG laparoscopy-assisted distal gastrectomy * Student’s t test
Pearson’s Chi-square test
à
Fisher’s exact test
Oncologic outcomes The number of dissected lymph nodes in the RADG group for all areas and N2 areas was significantly higher than that in the LADG group. (37.1 ± 12.9 vs. 34.1 ± 12.1 and 16.3 ± 7.7 vs. 13.2 ± 5.3, P = 0.044 and 0.001, respectively). The pathological outcomes are shown in Table 3. There were no significant differences in the depth of invasion, lymph node metastasis, and pathologic stage between the two groups. (P = 0.655, 0.175, and 0.227, respectively) The proximal and distal margins were not significantly different between the two groups.
Discussion This analysis demonstrated the advantages of RADG over LADG regarding the number of dissected lymph nodes, especially in the technically demanding N2 area and, more
specifically, in the suprapancreatic area around the splenic vessels. Recent retrospective studies investigating the role of robotic surgery for gastric cancer did not show meaningful clinical benefits compared to laparoscopic surgery [2, 11, 16, 17]. Despite the fact that a higher number of dissected lymph nodes does not necessarily improve overall survival for early gastric cancer patients, an increased number of harvested lymph nodes may at least influence accurate staging. Moreover, an increased number of harvested nodes in the suprapancreatic area may have implications on improving the quality of nodal dissection for advanced gastric cancer. This may be related to the articulating function of the robotic system which enables the surgeon to dissect the lymph node along the splenic artery easily and efficiently. The importance of suprapancreatic lymph node dissection in advanced gastric cancer surgery has been advocated before in order to improve long-term survival (Reference: Dutch trial 15-year results). This fact may justify the application of a robotic system. In contrast, a
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Surg Endosc Table 2 Short-term surgical outcomes
RADG (n = 87)
LADG (n = 288)
P
Operative time (min)
248.4 ± 40.1
230.0 ± 55.8
Hospital days (days)
6.7 ± 1.0
7.4 ± 2.4
\0.001
Flatulence (pod#)
3.5 ± 0.8
3.8 ± 0.8
0.01
Transfusion rate
0
0
None
82 (94.3 %)
262 (91 %)
Yes
5 (5.7 %)
26 (9.0 %)
4 (4.6 %)
16 (5.6 %)
Wound
3 (3.4 %)
8 (2.8 %)
Fluid collection
1 (1.1 %)
3 (1.0 %)
Ileus
0 (0 %)
1 (0.3 %)
Others
0 (0 %)
4 (1.3 %)
1 (1.1 %)
10 (3.5 %)
Bleeding
0 (0 %)
2 (0.7 %)
Anastomotic leakage Intra-abdominal abscess
0 (0 %) 0 (0 %)
3 (1.0 %) 2 (0.7 %)
Stricture
0 (0 %)
1 (0.3 %)
Myocardial infarction
1 (1.1 %)
1 (0.3 %)
Acute mesenteric infarction
0 (0 %)
1 (0.3 %)
0.001
Complications
Minor complications
Major complications
0.330à [0.999à
0.469à
0.411à
Mortality None
86 (98.9 %)
287 (99.7 %)
Yes
1 (1.1 %)
1 (0.3 %)
RADG Robot-assisted distal gastrectomy, LADG laparoscopy-assisted distal gastrectomy * Difference in hemoglobin levels between the preoperative and immediate postoperative periods
Table 3 Pathological and short-term oncological outcomes
Student’s t test
à
Fisher’s exact test
RADG (n = 87)
LADG (n = 288)
T1 (mucosa and submucosa)
25 (69.4 %)
50 (76.9 %)
T2 (propria muscle)
6 (16.7 %)
7 (10.8 %)
T3 (subserosa)
5 (13.9 %)
8 (12.3 %)
N0
31 (86.1 %)
58 (89.2 %)
N1 (1–2)
4 (11.1 %)
2 (3.1 %)
1 (2.8 %)
5 (7.7 %)
I
29 (80.6 %)
55 (84.5 %)
II
7 (19.4 %)
7 (10.8 %)
III
0 (0 %)
3 (4.6 %)
Proximal resection margin (cm)
3.4 ± 2.1
3.3 ± 2.2
0.820
Distal resection margin (cm)
6.6 ± 3.1
6.4 ± 2.8
0.506
Number of harvested lymph nodes
37.1 ± 12.9
34.1 ± 12.1
0.044
Depth of invasion
0.655*
Lymph node metastasis
N2 (3–6) Stage
0.175*
0.227*
RATG Robot-assisted total gastrectomy, LATG laparoscopy-assisted total gastrectomy * Pearson’s Chi-square test
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Student’s t test
P
Surg Endosc Table 4 Number of harvested lymph nodes in patients underwent D2 lymph node dissection
RADG (n = 79)
LADG (n = 193)
P
Number of harvested lymph nodes at N2 area
16.3 ± 7.7
3.2 ± 5.3
0.001*
Number of harvested lymph nodes at No. 8a station
3.2 ± 2.4
2.9 ± 2.2
0.270*
Number of harvested lymph nodes at No. 9 station
3.1 ± 2.4
2.7 ± 2.0
0.141*
Number of harvested lymph nodes at No. 11p station
2.9 ± 2.9
2.2 ± 2.0
0.04*
Number of harvested lymph nodes at 12a station
2.5 ± 2.0
2.2 ± 2.0
0.151*
Total number of harvested lymph nodes
RATG Robot-assisted total gastrectomy, LATG laparoscopy-assisted total gastrectomy *
Student’s t test
conventional straight laparoscopic instrument does not provide the surgeon with enough degrees of freedom and cannot reach deep to the posterior side of the suprapancreatic node-bearing area effectively, even with excessive downward compression of the pancreas. Further, this may cause pancreatic injuries and pancreatitis (Table 4). Because the most important reason to use expensive robot for gastric cancer and justifying cost is intuitively articulating function of the instrument, maximizing benefit of robot using monopolar spatula-type dissecting instrument does make sense. An ultrasonic shears in born cannot be flexed with articulation. Many laparoscopic surgeons used to operate with an ultrasonic shears still stick to use it. There are no data to show any improved oncological outcome. As we have shown that surgical stress is not improved with robotic surgery compared to laparoscopic surgery, this functional benefit for surgical technique to improve nodal dissection without hampering normal anatomic structure is important. So, not only robot but more specifically adequate instrumentation could be a crucial point. Only utilizing three-dimensional views and stable working platform lowering of tremor and increasing accuracy of instrumentation in robotic operation are not enough to justify using robot if there is no clear physiological and oncological benefits. And, there are a lot of 3D laparoscopy products already in market and practice. There is another supporting report by Noshiro et al. [18] who performed successfully RADG using electrocautery devices alone without using ultrasonic shears like us and achieved same or more number of retrieved nodes compared with LADG. Longer operating time for RADG was usually reported previously and matches this report. This is considered to be related to docking, additional time for instrument changes and somewhat slow movement of the robotic arms for safety control. On the other hand, relatively accurate movement and less frequency of errors may make robotic surgery faster. According to previous reports after a short learning curve and consecutively performed 100 cases, a reduction in operating time may still be detected. [19, 20].
In the near future, we could expect a reduction in operating time for robotic surgery because of technological advancement and increased experience. Hospital stay is a redundant outcome measure often influenced by nonmedical reasons. Nonetheless, there was a reduction in the robotic group. Reasons may be statistically significant younger age and less comorbidity in the RADG group. Younger people recover well and faster in general, which is mostly related to less postoperative complications [21–25]. That could be a more tentative factor than surgical method when we think our previous report that surgical stress-wise robot does not have any benefit [1]. Previous reports with similar age showed similar or even lower complications rates of RADG and reduced amount of bleeding compared to laparoscopic surgery, which might be related to less surgical trauma and faster recovery. However, it is still controversial to state that robotic gastrectomy is beneficial with regard to postoperative recovery [1, 2, 11–13, 16, 26–30]. However, with increasing experience, robotic surgery may prevail in terms of recovery and hospital stay. Aside from the controversial and vague issue of clinical benefit related to recovery and quality of life in robotic surgery, RADG could have strong potential advantages over LADG in terms of oncological benefit related to the dissection of lymph nodes at the N2 area, especially around the splenic vessels area. A well-designed prospective controlled study is proposed to elucidate this field. Disclosures Young-Woo Kim, Hong Man Yoon, Ji Yeon Park, Daniel Reim, Bang-Ul Eom, Myeong-Cherl Kook, and Keun Won Ryu have no conflicts of interest or financial ties to disclose.
References 1. Park JY, Jo MJ, Nam BH, Kim Y, Eom BW, Yoon HM, Ryu KW, Kim YW, Lee JH (2012) Surgical stress after robot-assisted distal gastrectomy and its economic implications. Br J Surg 99:1554–1561 2. Hyun MH, Lee CH, Kim HJ, Tong Y, Park SS (2013) Systematic review and meta-analysis of robotic surgery compared with
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conventional laparoscopic and open resections for gastric carcinoma. Br J Surg 100:1566–1578 Meakins JL (2002) Innovation in surgery: the rules of evidence. Am J Surg 183:399–405 Kim YW, Baik YH, Yun YH, Nam BH, Kim DH, Choi IJ, Bae JM (2008) Improved quality of life outcomes after laparoscopyassisted distal gastrectomy for early gastric cancer: results of a prospective randomized clinical trial. Ann Surg 248:721–727 Kim YW, Yoon HM, Yun YH, Nam BH, Eom BW, Baik YH, Lee SE, Lee Y, Kim YA, Park JY, Ryu KW (2013) Long-term outcomes of laparoscopy-assisted distal gastrectomy for early gastric cancer: result of a randomized controlled trial (COACT 0301). Surg Endosc 27:4267–4276 Kim HH, Han SU, Kim MC, Hyung WJ, Kim W, Lee HJ, Ryu SW, Cho GS, Song KY, Ryu SY (2014) Long-term results of laparoscopic gastrectomy for gastric cancer: a large-scale case–control and casematched Korean multicenter study. J Clin Oncol 32(7):627–633 Yasunaga H, Horiguchi H, Kuwabara K, Matsuda S, Fushimi K, Hashimoto H, Ayanian J (2013) Outcomes after laparoscopic or open distal gastrectomy for early-stage gastric cancer: a propensity-matched analysis. Ann Surg 257:640–646 Zeng YK, Yang ZL, Peng JS, Lin HS, Cai L (2012) Laparoscopyassisted versus open distal gastrectomy for early gastric cancer: evidence from randomized and nonrandomized clinical trials. Ann Surg 256:39–52. Kitano S, Shiraishi N, Uyama I, Sugihara K, Tanigawa N (2007) A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg 245:68–72 Strong V, Devaud N, Allen P, Gonen M, Brennan M, Coit D (2009) Laparoscopic versus open subtotal gastrectomy for adenocarcinoma: a case–control study. Ann Surg Oncol 16:1507–1513 Kim MC, Heo GU, Jung GJ (2010) Robotic gastrectomy for gastric cancer: surgical techniques and clinical merits. Surg Endosc 24:610–615 Woo Y, Hyung WJ, Pak KH, Inaba K, Obama K, Choi SH, Noh SH (2011) Robotic gastrectomy as an oncologically sound alternative to laparoscopic resections for the treatment of earlystage gastric cancers. Arch Surg 146(9):1086–1092 Eom BW, Yoon HM, Ryu KW, Lee JH, Cho SJ, Lee JY, Kim CG, Choi IJ, Lee JS, Kook MC, Rhee JY, Park SR, Kim YW (2012) Comparison of surgical performance and short-term clinical outcomes between laparoscopic and robotic surgery in distal gastric cancer. Eur J Surg Oncol (EJSO) 38:57–63 Yoon H, Kim Y-W, Lee J, Ryu K, Eom B, Park J, Choi I, Kim C, Lee J, Cho S, Rho J (2011) Robot-assisted total gastrectomy is comparable with laparoscopically assisted total gastrectomy for early gastric cancer. Surg Endosc 26(5):1377–1381 Bickenbach K, Strong VE (2012) Comparisons of gastric cancer treatments: east versus West. J Gastric Cancer 12:55–62 Coratti A, Annecchiarico M, Di Marino M, Gentile E, Coratti F, Giulianotti P (2013) Robot-assisted gastrectomy for gastric cancer: current status and technical considerations. World J Surg 37:2771–2781
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17. Song J, Kang WH, Oh SJ, Hyung WJ, Choi SH, Noh SH (2009) Role of robotic gastrectomy using da Vinci system compared with laparoscopic gastrectomy: initial experience of 20 consecutive cases. Surg Endosc 23:1204–1211 18. Noshiro H, Ikeda O, Urata M (2013) Robotically-enhanced surgical anatomy enables surgeons to perform distal gastrectomy for gastric cancer using electric cautery devices alone. Surg Endosc 28(4): 1180–1187 19. Park SS, Kim MC, Park MS, Hyung WJ (2012) Rapid adaptation of robotic gastrectomy for gastric cancer by experienced laparoscopic surgeons. Surg Endosc 26:60–67 20. Park JY, Kim YW, Ryu KW, Eom BW, Yoon HM, Reim D (2013) Emerging role of robot-assisted gastrectomy: analysis of consecutive 200 cases. J Gastric Cancer 13:255–262 21. Jeong O, Ryu SY, Zhao XF, Jung MR, Kim KY, Park YK (2012) Short-term surgical outcomes and operative risks of laparoscopic total gastrectomy (LTG) for gastric carcinoma: experience at a large-volume center. Surg Endosc 26:3418–3425 22. Kim MG, Kim HS, Kim BS, Kwon SJ (2013) The impact of old age on surgical outcomes of totally laparoscopic gastrectomy for gastric cancer. Surg Endosc 27:3990–3997 23. Komatsu S, Ichikawa D, Kashimoto K, Kubota T, Okamoto K, Konishi H, Shiozaki A, Fujiwara H, Otsuji E (2013) Risk factors to predict severe postoperative pancreatic fistula following gastrectomy for gastric cancer. World J Gastroenterol 19:8696–8702 24. Otsuji E, Fujiyama J, Takagi T, Ito T, Kuriu Y, Toma A, Okamoto K, Hagiwara A, Yamagishi H (2005) Results of total gastrectomy with extended lymphadenectomy for gastric cancer in elderly patients. J Surg Oncol 91:232–236 25. Seo SH, Hur H, An CW, Yi X, Kim JY, Han SU, Cho YK (2011) Operative risk factors in gastric cancer surgery for elderly patients. J Gastric Cancer 11:116–121 26. Pugliese R, Maggioni D, Sansonna F, Costanzi A, Ferrari G, Di Lernia S, Magistro C, Martini P, Pugliese F (2010) Subtotal gastrectomy with D2 dissection by minimally invasive surgery for distal adenocarcinoma of the stomach: results and 5-year survival. Surg Endosc 24:2594–2602 27. D’Annibale A, Pende V, Pernazza G, Monsellato I, Mazzocchi P, Lucandri G, Morpurgo E, Contardo T, Sovernigo G (2011) Full robotic gastrectomy with extended (D2) lymphadenectomy for gastric cancer: surgical technique and preliminary results. J Surg Res 166:e113–e120 28. Marano A, Choi YY, Hyung WJ, Kim YM, Kim J, Noh SH (2013) Robotic versus laparoscopic versus open gastrectomy: a meta-analysis. J Gastric Cancer 13:136–148 29. Yu H, Friedlander DF, Patel S, Hu JC (2013) The current status of robotic oncologic surgery. CA Cancer J Clin 63:45–56 30. Junfeng Z, Yan S, Bo T, Yingxue H, Dongzhu Z, Yongliang Z, Feng Q, Peiwu Y (2014) Robotic gastrectomy versus laparoscopic gastrectomy for gastric cancer: comparison of surgical performance and short-term outcomes. Surg Endosc 28(6):1779–1787
and Other Interventional Techniques
Role of robot-assisted distal gastrectomy compared to laparoscopy-assisted distal gastrectomy in suprapancreatic nodal dissection for gastric cancer Young-Woo Kim1 • Daniel Reim1 • Ji Yeon Park1 • Bang Wool Eom1 Myeong-Cherl Kook1 • Keun Won Ryu1 • Hong Man Yoon1
•
Received: 16 February 2015 / Accepted: 23 June 2015 Ó Springer Science+Business Media New York 2015
Abstract Purpose Despite theoretical advantages, no clear benefit was proven for initial application of robotic surgery for gastric cancer so far. The aim of this analysis was to examine the role of robotic surgery regarding nodal dissection technically demanding areas compared to conventional laparoscopic surgery. Methods This analysis included 87 patients who underwent robot-assisted distal gastrectomy (RADG) and 288 patients who underwent laparoscopy-assisted distal gastrectomy (LADG) at the National Cancer Center, Korea, between February 2009 and September 2011. Clinicopathologic data, surgery-related data, postoperative morbidity, and pathologic data for each nodal station were analyzed. Results Time to flatulence was 3.5 ± 0.8 days for RADG and 3.8 ± 0.8 days for LADG (P = 0.01). Postoperative hospital stay was 6.7 ± 1.0 days in RADG and 7.4 ± 2.4 days in LADG (P \ 0.001).The number of dissected lymph nodes was 37.1 ± 12.9 in the RADG group and 34.1 ± 12.1 in the LADG group (P = 0.044). In patients undergoing D2 gastrectomy, the number of dissected lymph nodes in the N2 area was 16.3 ± 7.7 for RADG and 13.2 ± 5.3 for LADG (P = 0.001). The number of dissected lymph nodes around the splenic artery area was 2.9 ± 2.9 in RADG and 2.2 ± 2.0 in LADG (P = 0.04). Regarding postoperative complications, there was no statistically significant difference [five patients
& Hong Man Yoon [email protected] 1
Gastric Cancer Branch, Research Institute and Hospital, National Cancer Center, 323 Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do 410-769, Korea
(5.7 %) in RADG and 26 patients (9 %) in LADG) (P = 0.330)]. Conclusion RADG could provide an advantage over LADG in the dissection of the N2 area lymph nodes, especially around the splenic artery area. Keywords Gastric cancer Robotic surgery D2 gastrectomy Lymph node dissection Case–control study
Since the introduction of robotic surgery, its role is controversly debated especially in relation to the cost of the procedure [1, 2]. The general idea of evidence-based medicine, which is strongly backed up by health economics, is considered to evoke innovative and improved treatment [3]. Therefore, evaluation of robotic surgery is supposed to provide improvements for diverse outcome measures, such as quality of life and survival outcomes in oncologic surgery. Robotic surgery is now vigorously implemented in clinical practice without proof of concept from randomized controlled trial. In contrast, laparoscopic surgery for gastric cancer has been quite accepted for early cancer proven by various published clinical trials and numerous articles demonstrating many advantages over open surgery [4–10]. In contrast, application of robotic surgery for early gastric cancer has failed to show any clear benefit. However, initial data mainly from Korea at least demonstrated feasibility, safety, and comparable outcomes. [1, 2, 11–14]. Apparently, next step for robotic gastrectomy for gastric cancer should focus on the identification of some specific benefit. Clinical studies on laparoscopic gastrectomy for advanced gastric cancer unveiled technical difficulties in the dissection of the suprapancreatic area. The COACT 1001 trial data showed that the noncompliance rate of
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Surg Endosc
lymph node dissection was significantly higher in stage III disease. In Western countries and the countries without a national screening program, gastric cancer is mainly detected in advanced stages [15]. Therefore, the major area of research in minimally invasive surgery should focus on advanced gastric cancer. The major barrier of minimally invasive surgery for this disease considered to be the technically demanding suprapancreatic nodal dissection. Considering the theoretical advantages of robotic surgery, the suprapancreatic area could be more easily and effectively cleared. The main purpose of this analysis was to define mainly the oncologic advantages of robotic surgery for gastric cancer over laparoscopic surgery.
Methods
Results Demographics Between February 2009 and September 2011, 87 patients underwent RADG and 288 patients underwent LADG by a single surgeon (YWK). The patient characteristics are shown in Table 1. Patients in the RADG group were younger than those receiving LADG. (P \ 0.001) No significant differences existed with respect to gender and body mass index (BMI) between the two groups. Regarding the history of abdominal surgeries and comorbidities, there was no significant difference between the two groups. Intra-operatively, 3.4 and 5.9 % of patients in the RADG and LADG groups underwent combined resections, mainly cholecystectomy not influencing surgical outcome considerably (P = 0.586), and therefore were included in the final analysis.
Study approval Surgical outcomes This study followed the Declaration of Helsinki as a statement of ethical principles for medical research involving human subjects, including research on identifiable human material and data, and was approved by the institutional review board of NCCK. (IRB No. NCC20140177). Patients From February 2009, when the da Vinci surgical system (Intuitive Surgical Inc., Sunnyvale, CA, USA) was introduced at our hospital, to September 2011, a total of 2039 patients underwent curative resection for gastric cancer at National Cancer Center, Korea (NCCK). To see whether the surgical method influences the outcome, most experienced and having higher caseloads surgeon’s cases were selected. Other inclusion criteria were clinical stages T1N0, T1N1, or T2N0 diagnosed by esophagogastrodudenoscopy, endoscopic ultrasound and abdominopelvic computed tomography, and gastric cancer locations that guaranteed the application of subtotal gastrectomy. Data for clinicopathologic, surgical, and oncologic outcomes were extracted from the prospectively documented database at the Center for Gastric Cancer, NCCK. Statistical analysis Statistical analysis was performed using the Student’s t test for continuous variables and the Chi-square test for categorical variables. Two-sided P values were calculated for all tests and are reported here. P values \0.05 were considered to indicate statistical significance. The SAS (SAS Institute Inc., Cary, NC, USA) program was used for analyses.
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The short-term data of surgical outcomes in the two groups are shown in Table 2. The postoperative hospital stay was significantly shorter in the RADG group than in the LADG group. (6.7 ± 1.0 vs. 7.4 ± 2.4 days, P \ 0.001). The period which elapsed before passage of flatulence was shorter in RADG than in LADG. (3.5 ± 0.8 vs. 3.8 ± 0.8 days, P = 0.01). The difference between the preoperative and dayof-surgery hemoglobin levels was not significantly different between the two groups. The mean operative time for the RADG group was significantly longer than for the LADG group (248.4 ± 40.1 vs. 230.0 ± 55.8 min; P \ 0.001). Five patients (5.7 %) in the RADG group developed complications: four patients (4.6 %) had minor complications, and one patient (1.1 %) had a major complication. Twenty-six patients (9.0 %) in the LADG group demonstrated complications: 16 patients (4.5 %) developed minor and 10 patients (3.5 %) revealed major complications. There were no significant differences in overall complication rate, and major and minor complications between the two groups. (P = 0.330, 0.469, and [0.999, respectively). Regarding mortality, there was one case in each group during the postoperative period within 1 month without statistical significance (P = 0.411). In the RADG group, the patient died of acute myocardial infarction on postoperative day 1 without any surgical problem, negligible bleeding of \20 ml and short operating time. In the LADG group, one old aged patient died of acute mesenteric infarction of unknown cause, most probably thromboembolism. There were two patients who underwent conversion to open surgery during RADG due to massive adhesion in the abdominal cavity because of previous surgery. The other patient had a small bowel injury by the trocar during insertion.
Surg Endosc Table 1 Demographic data
RADG (n = 87)
LADG (n = 288)
P
Age (years)
54.1 ± 12.0
60.5 ± 11.0
\0.001*
Gender (male/female)
46: 41
170: 118
0.309
24.1 ± 3.4
24.0 ± 4.3
0.859*
None
80 (92 %)
241 (83.7 %)
0.054
Appendectomy
5 (5.7 %)
27 (9.4 %)
Gynecologic procedure
1 (1.1 %)
12 (4.2 %)
Laparoscopic cholecystectomy
0 (0 %)
1 (0.3 %)
Others
1 (1.1 %)
7 (2.4 %)
None
54 (62.1 %)
144 (50 %)
DM
8 (9.2 %)
40 (13.9 %)
Hypertension
27 (31 %)
104 (36.1 %)
Heart disease
3 (3.4 %)
8 (3.1 %)
Pulmonary disease Liver cirrhosis
4 (4.5 %) 0 (0 %)
12 (4.2 %) 2 (0.7 %)
2
BMI (kg/m ) Previous abdominal surgery
Comorbidity
Cerbrovascular disease
0 (0 %)
2 (0.7 %)
Others
2 (2.3 %)
10 (3.3 %)
None
84 (96.6 %)
271 (94.1 %)
Gallbladder
3 (3.4 %)
9 (3.1 %)
0.048
Combined resection
Salphinx, ovary, uterus
0 (0 %)
4 (1.4 %)
Others
0 (0 %)
4 (1.4 %)
Less than D2
8 (9.2 %)
95 (33.0 %)
D2
79 (90.8 %)
193 (67.0 %)
0.586à
\0.001
Lymph node dissection
RADG Robot-assisted distal gastrectomy, LADG laparoscopy-assisted distal gastrectomy * Student’s t test
Pearson’s Chi-square test
à
Fisher’s exact test
Oncologic outcomes The number of dissected lymph nodes in the RADG group for all areas and N2 areas was significantly higher than that in the LADG group. (37.1 ± 12.9 vs. 34.1 ± 12.1 and 16.3 ± 7.7 vs. 13.2 ± 5.3, P = 0.044 and 0.001, respectively). The pathological outcomes are shown in Table 3. There were no significant differences in the depth of invasion, lymph node metastasis, and pathologic stage between the two groups. (P = 0.655, 0.175, and 0.227, respectively) The proximal and distal margins were not significantly different between the two groups.
Discussion This analysis demonstrated the advantages of RADG over LADG regarding the number of dissected lymph nodes, especially in the technically demanding N2 area and, more
specifically, in the suprapancreatic area around the splenic vessels. Recent retrospective studies investigating the role of robotic surgery for gastric cancer did not show meaningful clinical benefits compared to laparoscopic surgery [2, 11, 16, 17]. Despite the fact that a higher number of dissected lymph nodes does not necessarily improve overall survival for early gastric cancer patients, an increased number of harvested lymph nodes may at least influence accurate staging. Moreover, an increased number of harvested nodes in the suprapancreatic area may have implications on improving the quality of nodal dissection for advanced gastric cancer. This may be related to the articulating function of the robotic system which enables the surgeon to dissect the lymph node along the splenic artery easily and efficiently. The importance of suprapancreatic lymph node dissection in advanced gastric cancer surgery has been advocated before in order to improve long-term survival (Reference: Dutch trial 15-year results). This fact may justify the application of a robotic system. In contrast, a
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Surg Endosc Table 2 Short-term surgical outcomes
RADG (n = 87)
LADG (n = 288)
P
Operative time (min)
248.4 ± 40.1
230.0 ± 55.8
Hospital days (days)
6.7 ± 1.0
7.4 ± 2.4
\0.001
Flatulence (pod#)
3.5 ± 0.8
3.8 ± 0.8
0.01
Transfusion rate
0
0
None
82 (94.3 %)
262 (91 %)
Yes
5 (5.7 %)
26 (9.0 %)
4 (4.6 %)
16 (5.6 %)
Wound
3 (3.4 %)
8 (2.8 %)
Fluid collection
1 (1.1 %)
3 (1.0 %)
Ileus
0 (0 %)
1 (0.3 %)
Others
0 (0 %)
4 (1.3 %)
1 (1.1 %)
10 (3.5 %)
Bleeding
0 (0 %)
2 (0.7 %)
Anastomotic leakage Intra-abdominal abscess
0 (0 %) 0 (0 %)
3 (1.0 %) 2 (0.7 %)
Stricture
0 (0 %)
1 (0.3 %)
Myocardial infarction
1 (1.1 %)
1 (0.3 %)
Acute mesenteric infarction
0 (0 %)
1 (0.3 %)
0.001
Complications
Minor complications
Major complications
0.330à [0.999à
0.469à
0.411à
Mortality None
86 (98.9 %)
287 (99.7 %)
Yes
1 (1.1 %)
1 (0.3 %)
RADG Robot-assisted distal gastrectomy, LADG laparoscopy-assisted distal gastrectomy * Difference in hemoglobin levels between the preoperative and immediate postoperative periods
Table 3 Pathological and short-term oncological outcomes
Student’s t test
à
Fisher’s exact test
RADG (n = 87)
LADG (n = 288)
T1 (mucosa and submucosa)
25 (69.4 %)
50 (76.9 %)
T2 (propria muscle)
6 (16.7 %)
7 (10.8 %)
T3 (subserosa)
5 (13.9 %)
8 (12.3 %)
N0
31 (86.1 %)
58 (89.2 %)
N1 (1–2)
4 (11.1 %)
2 (3.1 %)
1 (2.8 %)
5 (7.7 %)
I
29 (80.6 %)
55 (84.5 %)
II
7 (19.4 %)
7 (10.8 %)
III
0 (0 %)
3 (4.6 %)
Proximal resection margin (cm)
3.4 ± 2.1
3.3 ± 2.2
0.820
Distal resection margin (cm)
6.6 ± 3.1
6.4 ± 2.8
0.506
Number of harvested lymph nodes
37.1 ± 12.9
34.1 ± 12.1
0.044
Depth of invasion
0.655*
Lymph node metastasis
N2 (3–6) Stage
0.175*
0.227*
RATG Robot-assisted total gastrectomy, LATG laparoscopy-assisted total gastrectomy * Pearson’s Chi-square test
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Student’s t test
P
Surg Endosc Table 4 Number of harvested lymph nodes in patients underwent D2 lymph node dissection
RADG (n = 79)
LADG (n = 193)
P
Number of harvested lymph nodes at N2 area
16.3 ± 7.7
3.2 ± 5.3
0.001*
Number of harvested lymph nodes at No. 8a station
3.2 ± 2.4
2.9 ± 2.2
0.270*
Number of harvested lymph nodes at No. 9 station
3.1 ± 2.4
2.7 ± 2.0
0.141*
Number of harvested lymph nodes at No. 11p station
2.9 ± 2.9
2.2 ± 2.0
0.04*
Number of harvested lymph nodes at 12a station
2.5 ± 2.0
2.2 ± 2.0
0.151*
Total number of harvested lymph nodes
RATG Robot-assisted total gastrectomy, LATG laparoscopy-assisted total gastrectomy *
Student’s t test
conventional straight laparoscopic instrument does not provide the surgeon with enough degrees of freedom and cannot reach deep to the posterior side of the suprapancreatic node-bearing area effectively, even with excessive downward compression of the pancreas. Further, this may cause pancreatic injuries and pancreatitis (Table 4). Because the most important reason to use expensive robot for gastric cancer and justifying cost is intuitively articulating function of the instrument, maximizing benefit of robot using monopolar spatula-type dissecting instrument does make sense. An ultrasonic shears in born cannot be flexed with articulation. Many laparoscopic surgeons used to operate with an ultrasonic shears still stick to use it. There are no data to show any improved oncological outcome. As we have shown that surgical stress is not improved with robotic surgery compared to laparoscopic surgery, this functional benefit for surgical technique to improve nodal dissection without hampering normal anatomic structure is important. So, not only robot but more specifically adequate instrumentation could be a crucial point. Only utilizing three-dimensional views and stable working platform lowering of tremor and increasing accuracy of instrumentation in robotic operation are not enough to justify using robot if there is no clear physiological and oncological benefits. And, there are a lot of 3D laparoscopy products already in market and practice. There is another supporting report by Noshiro et al. [18] who performed successfully RADG using electrocautery devices alone without using ultrasonic shears like us and achieved same or more number of retrieved nodes compared with LADG. Longer operating time for RADG was usually reported previously and matches this report. This is considered to be related to docking, additional time for instrument changes and somewhat slow movement of the robotic arms for safety control. On the other hand, relatively accurate movement and less frequency of errors may make robotic surgery faster. According to previous reports after a short learning curve and consecutively performed 100 cases, a reduction in operating time may still be detected. [19, 20].
In the near future, we could expect a reduction in operating time for robotic surgery because of technological advancement and increased experience. Hospital stay is a redundant outcome measure often influenced by nonmedical reasons. Nonetheless, there was a reduction in the robotic group. Reasons may be statistically significant younger age and less comorbidity in the RADG group. Younger people recover well and faster in general, which is mostly related to less postoperative complications [21–25]. That could be a more tentative factor than surgical method when we think our previous report that surgical stress-wise robot does not have any benefit [1]. Previous reports with similar age showed similar or even lower complications rates of RADG and reduced amount of bleeding compared to laparoscopic surgery, which might be related to less surgical trauma and faster recovery. However, it is still controversial to state that robotic gastrectomy is beneficial with regard to postoperative recovery [1, 2, 11–13, 16, 26–30]. However, with increasing experience, robotic surgery may prevail in terms of recovery and hospital stay. Aside from the controversial and vague issue of clinical benefit related to recovery and quality of life in robotic surgery, RADG could have strong potential advantages over LADG in terms of oncological benefit related to the dissection of lymph nodes at the N2 area, especially around the splenic vessels area. A well-designed prospective controlled study is proposed to elucidate this field. Disclosures Young-Woo Kim, Hong Man Yoon, Ji Yeon Park, Daniel Reim, Bang-Ul Eom, Myeong-Cherl Kook, and Keun Won Ryu have no conflicts of interest or financial ties to disclose.
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