Ann Surg Oncol (2013) 20:2625–2632 DOI 10.1245/s10434-013-2895-8
ORIGINAL ARTICLE – COLORECTAL CANCER
Oncologic Outcomes and Perioperative Clinicopathologic Results after Robot-assisted Tumor-specific Mesorectal Excision for Rectal Cancer Seung Hyuk Baik, MD, PhD, Nam Kyu Kim, MD, PhD, Dae Ro Lim, MD, Hyuk Hur, MD, Byung So Min, MD, and Kang Young Lee, MD, PhD Section of Colon Rectal Surgery, Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea
ABSTRACT Background. Robot-assisted surgery is a new and emerging surgical procedure for rectal cancer patients. However, there is a lack of information regarding oncologic outcomes for this procedure. We aimed to evaluate oncologic and perioperative clinicopathologic outcomes of surgical resection using robotic instruments for rectal cancer. Methods. Data from rectal cancer patients (n = 370) diagnosed with stage I–IV disease sited below 15 cm from the anal verge who underwent robot-assisted tumor-specific mesorectal excision consecutively from June 2006 to December 2010 were evaluated. Clinicopathologic and follow-up data were recorded prospectively and analyzed retrospectively. Perioperative clinicopathologic outcomes, postoperative complications, 3-year overall survival rate, and 3-year disease-free survival rate were analyzed. Results. All patients underwent robot-assisted tumor-specific mesorectal excision. Of all postoperative pathologic stages, 15 (4.1 %) were stage 0 (pathologic complete remission), 126 (34.1 %) stage I, 95 (25.7 %) stage II, 118 (31.9 %) stage III, and 16 (4.3 %) stage IV. The 3-year overall survival rate was 93.1 % (pathologic complete remission = 100 %, stage I = 99.2 %, stage II = 97.1 %, stage III = 90.1 %, and stage IV = 48.4 %). The 3-year disease-free survival rate was 79.2 % (pathologic complete remission = 100 %, stage I = 93.7 %, stage II = 79.8 %, stage III = 69.6 %, and stage IV = 0.0 %). The 3-year cumulative local recurrence rate was 3.6 % (n = 10). The
Ó Society of Surgical Oncology 2013 First Received: 29 April 2012; Published Online: 16 February 2013 N. K. Kim, MD, PhD e-mail:
[email protected]
circumferential resection margin positive rate was 5.7 % (n = 21). Local recurrence developed in one patient and systemic recurrence developed in five patients. The total number of patients with postoperative complications was 86 (23.2 %). Conclusions. These data show the feasibility and safety of robot-assisted tumor-specific mesorectal excision for rectal cancer in terms of oncologic outcomes.
The basic surgical procedure of robot-assisted rectal cancer surgery is similar to conventional laparoscopic surgery because both procedures use the pneumoperitoneum and long surgical instruments through trocars. Conventional laparoscopic surgery for rectal cancer is not inferior to open surgery. This has been proven by largescale randomized trials and single center experiences.1–6 Robotic surgery for rectal cancer is based on these experiences and has been performed around the world since 2001.7 Robot-assisted rectal cancer surgery was adopted at several major hospitals because robotic systems have several advanced core technologies compared to conventional laparoscopic instruments. These technologies include three-dimensional images, motion scaling, tremor elimination and instrument tips with seven degrees of freedom.8 All these advanced technologies are why the robotic system is essentially helpful for achieving better surgical outcomes compared to conventional laparoscopic surgery for rectal cancer. However, studies documenting oncologic outcomes of robotic surgery for rectal cancer are lacking. Therefore, this study aims to present the oncologic outcomes of rectal cancer patients who underwent robotassisted surgery with perioperative clinicopathologic outcomes in a single institution.
2626
PATIENTS AND METHODS Patients A total of 370 patients at Severance Hospital, Yonsei University, Seoul, South Korea, were prospectively enrolled. These patients underwent curative robot-assisted tumor-specific mesorectal excision for the treatment of rectal cancer between June 2006 and December 2010.9 The enrollment criteria included location of the tumor less than 15 cm from the anal verge and, a pathologic diagnosis of primary adenocarcinoma of the rectum. Stage IV disease was defined as metastasis confined to one organ or site. Laparoscopic radiofrequency ablation for liver metastatic lesion (n = 10) and video-assisted thoracoscopic surgery for lung metastatic lesion (n = 6) were performed simultaneously with robotic surgery for rectal cancer. All enrolled patients were consecutive patients who underwent robot-assisted, tumor-specific mesorectal excision. Robotic and laparoscopic surgeries were not performed on patients with direct tumor invasion or a tumor adherent to other organs or structures, as detected by a preoperative imaging study. The surgery method (open, laparoscopic, or robotic) used was based on the decision of the patient and performed with informed consent. During the same study period, open curative rectal cancer and laparoscopic rectal cancer surgeries were performed in 569 and 398 cases, respectively. Preoperative chemoradiotherapy was performed on patients who had clinical T3-4N0 or N?M0 stage cancer among mid and low rectal cancer patients. The preoperative clinical stage was obtained by a rectal magnetic resonance imaging, transrectal ultrasonography, abdominopelvic computed tomography scan, and chest computed tomography scan. Postoperative chemoradiotherapy was provided to patients whose postoperative pathologic stage was above T3-4N0 or N?M0 among patients who did not receive preoperative chemoradiotherapy. The clinicopathologic data for these patients were collected prospectively from the Yonsei Colorectal Cancer Database. These clinicopathologic data were used in the study, and missing data were evaluated retrospectively by reviewing electronic medical charts and conducting telephone interviews. Postoperative complications were categorized using the Accordion Severity Grading System.10 Conversion was defined as a length of incision more than the routine length for specimen extraction (4 cm) necessary to complete the procedure. Conversion refers to open conversion and not conversion to the laparoscopic procedure. After discharge, patients were examined in the outpatient setting after 1 and 3 months, then every 3 months for 3 years. After 3 years, patients were examined every
S. H. Baik et al.
6 months for 2 years. Surgeons and medical oncologists evaluated each patient twice during every visit. Local recurrence was defined by radiologically or histologically confirmed tumor recurrence in the pelvic cavity or anastomosis site. The Yonsei University College of Medicine institutional review board approved the study protocol, and informed consent was obtained from all patients. Surgical Techniques The da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA) was used as the robotic instrument. Four surgeons (NKK, KYL, SHB, and BSM) performed the robotic procedures, and two robotic techniques were used: hybrid robotic surgery and totally robotic surgery.11,12 The main difference between these two techniques is the difference in left colon and splenic flexure mobilization. Left colon and splenic flexure mobilization is performed by a conventional laparoscopic instrument in the hybrid robotic procedure (five ports; specimen is extracted from the left lower abdomen) and by the robotic system in the totally robotic procedure (six ports; specimen is extracted from the mid lower abdomen). However, rectal dissection is performed by the robotic system in both procedures. The surgeon’s preference determined which technique was used. Both the hybrid and the totally robotic techniques fulfill standard oncologic surgery concepts and follow total mesorectal excision principles.13 Detailed surgical procedures are described in previous studies.11,12 Diverting ileostomies were performed generally upon a surgeon’s decision during the operation when the following criteria were met: the rectal muscle wall was injured during rectal dissection, the air inflation test was positive, coloanal anastomosis was performed, severe combined medical disease was present, poor nutritional status was determined, and preoperative chemoradiation was performed.
Statistical Analysis Data were analyzed by SPSS software, version 18 (SPSS, Chicago, IL). Demographic data were expressed as the mean, with standard deviation and range. The Fisher’s exact test for categorical variables and the Student’s t test for continuous variables were used. Overall survival and disease-free survival were analyzed using the Kaplan– Meier method. Converted cases were considered on an intention-to-treat basis. Local recurrence and local recurrence with simultaneous systemic recurrence were calculated as a local recurrence case. P values of less than 0.05 were considered statistically significant.
Robot-assisted Surgery for Rectal Cancer
2627
TABLE 1 Patient characteristics and operation details (n = 370) Characteristic
Total (n = 370)
Hybrid (n = 131)
Totally robotic (n = 239)
Age (years)
58.0 ± 11.9 (26–86)
59.1 ± 11.8
57.4 ± 11.9
Male
232 (62.7)
82 (62.6)
150 (62.8)
Female
138 (37.3)
49 (37.4)
89 (37.2)
23.3 ± 2.9 (13.8–32.7)
22.9 ± 3.0
23.5 ± 2.9
1
248 (67.0)
90 (68.7)
158 (66.1)
2
120 (32.4)
41 (31.3)
79 (33.1)
3
2 (0.5)
0 (0.0)
2 (0.8)
Low (0–5 cm) Mid (5.1–10 cm)
99 (26.8) 190 (51.4)
33 (25.2) 64 (48.9)
66 (27.6) 126 (52.7)
Upper (10.1–15 cm)
81 (21.9)
34 (26.0)
47 (19.7)
20 (5.4)
7 (5.3)
13 (5.4)
Yes
78 (21.1)
12 (9.2)
66 (27.6)
No
292 (78.9)
119 (90.8)
173 (72.4)
Sex
BMI (kg/m2)
0.069 0.532
Tumor location from anal verge
0.375
0.969 \0.001
Preoperative CRT, n (%)
Operation methods
0.204 0.975
ASA score
History of abdominal surgery
P
Operation time (min) 215.0 ± 69.7 (92.0–477.0) 363.3 ± 94.8 (138.0–702.0) \0.001
Total LAR (319[86.2])
300.6 ± 105.5 (92.0–663.0)
uLAR with CAA (46[12.4])
362.6 ± 123.3 (93.0–687.0)
APR 3 (0.8)
518.6 ± 158.8 (423.0–702.0)
Hartmann operation (2[0.5])
431.5 ± 194.5 (294.0–569.0)
Diverting ileostomy
132 (35.7)
24 (18.3)
108 (45.2)
Conversion
3 (0.8)
0 (0.0)
3 (1.3)
\0.001 0.198
Intraoperative bleeding, ml
245.7 ± 222.1 (10.0–1300.0) 204.4 ± 163.9
258.2 ± 235.9
0.071
IOC or event Bladder injury
9 (2.4) 1 (0.3)
2 (1.5) 1 (0.8)
7 (2.9)
0.402
1 (0.8)
4 (1.7)
Perforation of the rectum
1 (0.3)
Disruption of colorectal anastomosis
5 (1.4)
1 (0.4)
Marginal artery injury of descending colon 1 (0.3)
1 (0.4)
Bleeding from right pelvic wall
1 (0.4)
1 (0.3)
Data are presented as mean ± SD (range) or as n (%) SD standard deviation, BMI body mass index, ASA American Society of Anesthesiologists, CRT chemoradiotherapy, LAR low anterior resection, SD standard deviation, uLAR with CAA ultra low anterior resection with coloanal anastomosis, APR abdominoperineal resection, IOC intraoperative complication
RESULTS
procedure in 239 cases. Other detailed patient characteristics are displayed in Table 1.
Patient Characteristics Clinical Outcomes During the Operation The mean patient age was 58 ± 11.9 years. The mean body mass index was 23.3 ± 2.9 kg/m2. There were 99 (26.8 %) cases of low rectal cancer, 190 (51.4 %) cases of mid rectal cancer, and 81 (21.9 %) cases of upper rectal cancer. A history of abdominal surgery was associated with 20 (5.4 %) cases. Preoperative chemoradiotherapy was performed in 78 (21.1 %) cases. The hybrid robotic procedure was performed in 131 cases, and the totally robotic
Rectal dissection was performed in all patients using the robotic system. Conversion occurred in three cases as a result of difficulty of pelvic dissection. All three conversions were open conversions. There were no cases in which a robotic procedure was changed to laparoscopy or a totally robotic procedure was changed to the hybrid method.
2628
S. H. Baik et al.
TABLE 2 Postoperative pathologic outcomes Characteristic
CRT (n = 78)
Non-CRT (n = 292)
Total (n = 370)
\0.001
TNM stage CR
P
15 (19.2)
15 (4.1)
I
21 (26.9)
105 (36.0)
126 (34.1)
II
20 (25.6)
75 (25.7)
95 (25.7)
III
19 (24.4)
99 (33.9)
118 (31.9)
IV
3 (3.8)
13. (4.5)
16 (4.3)
Well
8 (10.3)
56 (19.2)
64 (17.3)
Moderate Poor
66 (84.6) 3 (3.8)
227 (77.7) 7 (2.4)
293 (79.2) 10 (2.7)
Mucinous
3 (0.8)
Grade of differentiation
0.267
1 (1.3)
2 (0.7)
Collected no. of lymph nodes
12.1 ± 7.6 (1–38)
16.6 ± 9.2 (2–49)
15.6 ± 9.0 (1–49)
\0.001
PRM (cm)
13.5 ± 4.6 (6–27)
11.3 ± 4.5 (4–50)
11.7 ± 4.6 (4–50)
\0.001
DRM (cm)
1.9 ± 1.2 (1–6)
2.6 ± 1.4 (1–8)
2.5 ± 1.4 (1–8)
\0.001
CRM Noninvolved ([1 mm)
75 (96.2)
274 (93.8)
349 (94.3)
Involved (B1 mm)
3 (3.8)
18 (6.2)
21 (5.7)
Hybrid (n = 131)
Totally robotic (n = 239)
Total (n = 370)
TNM stage CR
0.586
0.006 0 (0.0)
15 (6.3)
I
45 (34.4)
81 (33.9)
15 (4.1) 126 (34.1)
II
30 (22.9)
65 (27.2)
95 (25.7)
III
46 (35.1)
72 (30.1)
118 (31.9)
IV
10 (7.6)
6 (2.5)
16 (4.3)
Collected no. of lymph nodes
17.1 ± 9.6
14.8 ± 8.7
15.6 ± 9.0 (1–49)
0.022
PRM (cm)
11.5 ± 4.3
11.8 ± 4.8
11.7 ± 4.6 (4–50)
0.404
DRM (cm)
2.6 ± 1.4
2.4 ± 1.4
2.5 ± 1.4 (1–8)
0.382
Noninvolved ([1 mm)
122 (93.1)
227 (95.0)
349 (94.3)
Involved (B1 mm)
9 (6.9)
12 (5.0)
21 (5.7)
CRM
0.462
Data are presented as mean ± SD (range) or as n (%) CRT chemoradiotherapy, CR complete remission, PRM proximal resection margin, DRM distal resection margin, SD standard deviation, CRM circumferential resection margin
Intraoperative events occurred in nine cases. There was one case each of rectum perforation, bladder injury, iatrogenic marginal artery injury and right pelvic wall bleeding. There were five case of colorectal anastomosis disruption. Hartmann’s operation was performed in two cases in which there was iatrogenic marginal artery injury of the descending colon (Table 1). Postoperative Clinical Outcomes and Postoperative Pathologic Results Days to first passed gas and first bowel movement were 2.8 ± 2.2 and 4.1 ± 2.7 days, respectively. Days to first soft diet was 5.3 ± 3.6 days and length of stay was
10.0 ± 6.5 days. The length of stay of the hybrid robotic procedure was 8.4 ± 4.3 days, and the length of stay of the totally robotic procedure was 10.8 ± 7.3 days (P \ 0.001). The mean number of collected lymph nodes was 15.6 ± 9.0 across all cases. Circumferential resection margin (CRM) was involved in 21 cases (5.7 %). CRM was involved in 18 cases (6.2 %, 18 of 274) where preoperative chemoradiotherapy was not given, and in 3 cases (3.8 %) where preoperative chemoradiotherapy (P = 0.586) was given (Table 2). Preoperative chemoradiotherapy was given in 78 cases, and the preoperative clinical stage was cT3N0 in 2 cases, cT3N1 in 21 cases, cT3N2 in 28 cases, cT4N0 in 8 cases, cT4N1 in 11 cases and cT4N2 in 8 cases. Pathologic T4
Robot-assisted Surgery for Rectal Cancer
2629
TABLE 3 Postoperative complications Characteristic
Hybrid (n = 131)
Totally robotic (n = 239)
Total (n = 370)
14 (10.7)
33 (13.8)
47 (12.7)
2
2
P
Postoperative complications Mild complications, n (%) Ascites
4 (1.1)
Chyloperitoneum
2
4
6 (1.6)
Voiding difficulty
5
6
11 (2.9)
Fever
0
3
3 (0.8)
Ileus
3
12
15 (4.1)
Wound infection
2
3
5 (1.4)
Wound infection with UTI
0
1
1 (0.3)
Wound infection with voiding difficulty Back pain Moderate complications, n (%)
0
1
1 (0.3)
0 0 (0.0)
1 8 (3.4)
1 (0.3) 8 (2.2)
Pneumonia
0
1
1 (0.3)
Bleeding from anastomosis site
0
1
1 (0.3)
Pelvic abscess
0
6
5 (3.8)
26 (10.9)
Ischemic colitis
1
0
Rectovaginal fistula
0
1
1 (0.3)
Intra-abdominal abscess
0
1
1 (0.3)
Anastomotic leakage (total)
4 (4.5) (4/131a)
24 (10.3) (24/234a)
28 (7.7) (28/365a)
Anastomotic leakage only
4
22
26 (7.1) (26/365a)
Anastomotic leakage with pleural effusion
0
1
1 (0.3) (1/365a)
Anastomotic leakage with wound infection, UTI
0
1
1 (0.3) (1/365a)
Deaths (30-day mortality), n (%)
0 (0.0)
0 (0.0)
Severe complications
Total number of complications, n (%)
6 (1.6) 31 (8.4) 1 (0.3)
0 (0.0) 91 (24.6)
Total number of patients with complications, n (%)
21 (16.0)
65 (27.2)
86 (23.2)
0.015
Readmission due to complications
2 (1.5)
11 (4.6)
13 (3.5)
0.124
SD standard deviation, UTI urinary tract infection a
Number of patients who underwent sphincter saving surgery
stage was associated with 16 cases. These cases, except 1 case, had tumor penetration to the visceral peritoneum surface and did not have direct adjacent organ invasion. One case, which showed cT3 on a rectal magnetic resonance imaging after concurrent chemoradiotherapy, had direct tumor invasion into the seminal vesicle. There were no cases with a positive distal resection margin. The total number of patients with complications was 86 (23.2 %). Among the severe complications, the anastomotic leakage rate was 7.7 % (28 of 365). A pelvic abscess, which was categorized as a moderate complication (n = 6), can be considered a complication related to anastomotic leakage with rectovesical and rectovaginal fistulas (n = 3). Thus, the total anastomotic complication rate was 10.1 % (37 of 356). The total number of patients with complications was relatively lower (P = 0.015) in the hybrid procedure (16.0 %), than the totally robotic procedure (27.2 %). There were no 30-day postoperative mortalities (Table 3).
Oncologic Results The mean follow-up period was 26.5 ± 13.5 (interquartile range 15–38) months and the median follow-up period was 24 (range 4–61) months. The 3-year overall survival rate was 93.1 % (95 % confidence interval [CI] 91.3–94.9 %) for all stages (Fig. 1a), 100 % in pathologic complete remission (n = 15), 99.2 % (95 % CI 100–98.4 %) in stage I (n = 126), 97.1 % (95 % CI 95.0–99.2 %) in stage II (n = 95), 90.0 % (95 % CI 86.2–93.8 %) in stage III (n = 118) and 48.4 % (95 % CI 33.3–63.5 %) in stage IV (n = 16; Fig. 1c). During the follow-up period, 16 patients died. Of these patients, 10 patients died from rectal cancer and 6 from pulmonary tuberculosis (n = 1), acute cholecystitis (n = 1), pneumonia (n = 1), massive gastrointestinal bleeding (n = 1), and sepsis (n = 2). The rate of cancer related death per total deaths was 62.5 % (10 of 16).
2630 FIG. 1 Survival curves. a The 3-year overall survival rate. b The 3-year disease-free survival rate. c The 3-year overall survival rate according to stages. d The 3-year diseasefree survival rate according to stages. pCR pathologic complete remission
S. H. Baik et al.
a
b
c
d
The 3-year disease-free survival rate was 79.2 % (95 % CI 76.4–82.0 %) for all stages (Fig. 1b), 100 % in pathologic complete remission, 93.7 % (95 % CI 91.4–96.0 %) in stage I, 79.8 % (95 % CI 73.7–85.9 %) in stage II, 69.6 % (95 % CI 64.1–75.1 %) in stage III, and 0 % in stage IV (Fig. 1d). The 3-year cumulative incidence of local recurrence was 3.6 % (95 % CI 2.4–4.8 %) for all stages, 0 % in pathologic complete remission, 4.8 % (95 % CI 2.7–6.9 %) in stage I, 5.7 % (95 % CI 2.1–9.3 %) in stage II, 1 % (95 % CI 0.1–1.9 %) in stage III, and 10 % (95 % CI 0.5–19.5 %) in stage IV. There was one patient who had local and
systemic recurrence simultaneously. This patient was counted as a patient with local recurrence. The 3-year cumulative incidence of the systemic recurrence rate was 17.6 % (95 % CI 14.6–20.3 %) for all stages, 0 % in pathologic complete remission, 1.6 % (95 % CI 0.5–2.7 %) in stage I, 15.3 % (95 % CI 9.7–20.9 %) in stage II, 29.7 % (95 % CI 24.2–35.2 %) in stage III and 100 % in stage IV. Local recurrence occurred in 10 patients between 4 and 30 months after surgery. Positive CRM was noted in 1 patient among the 10 patients with local recurrences. Wound or portsite recurrences did not occur in any patients.
Robot-assisted Surgery for Rectal Cancer
2631
TABLE 4 Oncologic outcomes and postoperative complications of recent laparoscopic or robot-assisted surgery for rectal cancer Study Baik et al.4 Pigazzi et al.
14
Year
Type of procedure (no. of cases)
Postoperative complication rate (%)
Follow-up (mo)
Oncologic outcomes and CRM, overall survival/ disease-free survival/CRM-positive rate
2011
Laparoscopy (n = 54)
22.2
60.0
5-year (90.8 %)/5-year (88.5 %)/1.9 %
2010
Robot (n = 143)
41.3
17.4
3-year (97 %)/3-year (77.6 %)/0.7 %
Baek et al.15
2010
Robot (n = 72)
37.6
20.2
3-year (96.2 %)/3-year (73.7 %)/NA
Laurent et al.5
2009
Laparoscopy (n = 238)
22.7
52
5-year (83.0 %)/5-year (82.0 %)/7.0 %
Jayne et al.2
2007
Laparoscopy (n = 167)a
40.0
36.8
3-year (74.6 %)/3-year (70.9 %)/7.0 %a
Tasang et al.16
2006
Laparoscopy (n = 51)
26.7
26.9
5-year (76.9 %)/5-year (64.4 %)/1.0 %
Robot (n = 370)
23.2
26.5
3-year (93.1 %)/3-year (79.2 %)/5.7 %
Present study
CRM circumferential resection margin, NA not available a
Patients who underwent anterior resection as a result of rectal cancer (n = 167)
DISCUSSION The results of this study showed acceptable long-term oncologic outcomes of robotic surgery for rectal cancer with feasible and acceptable perioperative clinical outcomes. The overall survival rate of this study is acceptable compared to the CLASICC trial and the disease-free survival rate showed a similar pattern.2 In 2010, two studies reported the oncologic outcomes of patients who underwent robot-assisted surgery for rectal cancer.14,15 In these studies, the 3-year overall survival and 3-year disease-free survival rates were 96.2–97 and 73.7–77.6 %, respectively. These oncologic and the results from this study are similar to the results previously reported for laparoscopic and robotic surgery for rectal cancer (Table 4).1–6,16,17 Macroscopic evaluation of the resected rectal specimen has been recognized as an important prognostic factor.18 Robot-assisted rectal dissection may be helpful in achieving a complete mesorectal grade because of the advanced technology inherent to the robotic surgical system. Mesorectal grade can be related to CRM involvement, and CRM involvement is related to oncologic outcomes.19,20 In this study, the CRM was 5.7 %. In the CLASICC trial, the CRM involvement rate for rectal cancer was 16 % for laparoscopic surgery and 14 % for open surgery.1–3 Other studies have reported CRM involvement rates of 0.0 to 16 % for laparoscopic surgery.1–6,16,17 Robotic surgery may be better than conventional laparoscopic dissection in terms of the local recurrence rate because of the technological advantages of the robotic surgical system. In this study the circumferential resection margin involvement rate was acceptable compared to previous studies (robot 0–7 %, laparoscopy 0–16 %).1–6,16,17,21–23 Both local recurrence and CRM involvement rate are acceptable compared to previous studies, which evaluated the oncologic outcomes of conventional laparoscopic surgery for rectal cancer, but were not better than previous studies.1–6,16,17 Thus, our results do
not prove the postulation favoring robotic surgery based on the CRM involvement rates and local recurrence rates. Besides the oncologic outcomes, the postoperative clinical outcomes of robot-assisted surgery are another important issue because the robotic system has advanced technology compared to that of laparoscopic surgery. Postoperative complications and intraoperative complications are major concerns in robotic surgery because surgeons and patients have high expectations that the robotic system will have low intraoperative complication rates as a result of its advanced technologies compared to those of conventional laparoscopic surgery. In this study, nine adverse events (2.4 %) were noted, and four events (1.1 %) occurred during the robotic procedure. However, these results cannot be compared with other studies because there are no data related to intraoperative events in previous publications. The mean hospital stay was approximately 5 days longer than the mean first day of soft diet. The main reason for this longer hospital stay compared to previous studies is the Korean medical insurance system.11,12,15 Korean patients prolong their stays because hospital stays are inexpensive.11 In this study, short-term perioperative outcomes seemed to be better in the hybrid procedure than in the totally robotic procedure. The anastomotic leakage rate seemed to be lower in hybrid cases than in totally robotic cases. The preoperative chemoradiotherapy rate (hybrid: 9.2 %; totally robotic: 27.6 %) may be the cause of the lower anastomotic leakage rate of the hybrid procedure. There was a statistically significant lower number of lymph nodes collected in the totally robotic cases compared to the hybrid cases. Similarly, the difference in the preoperative chemoradiotherapy rate could be a main cause of a statistically significant lower lymph node collection in the totally robotic cases compared to the hybrid cases. However, these results cannot be considered conclusive because the study was a single-center and nonrandomized with a
2632
relatively small number of cases. Moreover, this study may have a potential selection bias. Future studies will evaluate the differences of intraoperative complications or events between robotic and conventional laparoscopic surgery and between the hybrid and the totally robotic procedures. In conclusion, the present data show the feasibility and safety of robot-assisted surgery for rectal cancer as well as oncologic outcomes. However, this study does not show that the advanced technologies of the robotic system positively influenced the effects on oncologic and perioperative clinical outcomes when compared to conventional laparoscopic surgery for rectal cancer. Although 370 cases were evaluated, we believe this single-center study is not insufficient for drawing conclusions. Thus, future large-scale comparative studies comparing robotic and laparoscopic surgeries for rectal cancer are necessary to justify the general adoption of robotic surgical instruments. ACKNOWLEDGMENT This study was supported by a faculty research Grant from the Yonsei University College of Medicine (6-2011-0114).
REFERENCES 1. Guillou PJ, Quirke P, Thorpe H, et al. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718–26. 2. Jayne DG, Guillou PJ, Thorpe H, et al. Randomized trial of laparoscopic-assisted resection of colorectal carcinoma: 3-year results of the UK MRC CLASICC trial group. J Clin Oncol. 2007;25:3061–8. 3. Jayne DG, Thorpe H, Copeland J, et al. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg. 2010;97:1638–45. 4. Baik SH, Gincherman M, Mutch MG, et al. Laparoscopic vs open resection for patients with rectal cancer: comparison of perioperative outcomes and long-term survival. Dis Colon Rectum. 2011;54:6–14. 5. Laurent C, Leblanc F, Wu¨trich P, et al. Laparoscopic versus open surgery for rectal cancer: long-term oncologic results. Ann Surg. 2009;250:54–61. 6. Morino M, Parini U, Giraudo G, et al. Laparoscopic total mesorectal excision: a consecutive series of 100 patients. Ann Surg. 2003;237:335–42. 7. Ballantyne GH, Merola P, Weber A, et al. Robotic solutions to the pitfalls of laparoscopic colectomy. Osp Ital Chir. 2001;7:405–12.
S. H. Baik et al. 8. Baik SH, Kwon HY, Kim JS, et al. Robotic versus laparoscopic low anterior resection of rectal cancer: short-term outcome of a prospective comparative study. Ann Surg Oncol. 2009;16:1480–7. 9. Kim NK, Baik SH, et al. Oncologic outcomes after neoadjuvant chemoradiation followed by curative resection with tumor-specific mesorectal excision for fixed locally advanced rectal cancer. Ann Surg. 2006;244:1024–30. 10. Strasberg SM, Linehan DC, Hawkins WG. The accordion severity grading system of surgical complications. Ann Surg. 2009;250:177–86. 11. Baik SH, Lee WJ, Rha KH, et al. Robotic total mesorectal excision for rectal cancer using four robotic arms. Surg Endosc. 2008;22:792–7. 12. Park YA, Kim JM, Kim SA, et al. Totally robotic surgery for rectal cancer: from splenic flexure to pelvic floor in one set up. Surg Endosc. 2010;24:715–20. 13. Heald RJ, Moran BJ, Brown G, et al. Optimal total mesorectal excision for rectal cancer is by dissection in front of Denonvillier’s fascia. Br J Surg. 2004;91:121–3. 14. Pigazzi A, Luca F, Patriti A, et al. Multicentric study on robotic tumor-specific mesorectal excision of the treatment of rectal cancer. Ann Surg Oncol. 2010;17:1614–20. 15. Baek JH, Mckenzie S, Garcia-Aguilar J, et al. Oncologic outcomes of robotic assisted total mesorectal excision for the treatment of rectal cancer. Ann Surg. 2010;251:882–6. 16. Tasang WW, Chung CC, Kwok SY, et al. Laparoscopic sphincter-preserving total mesorectal excision with colonic J-pouch reconstruction: five-year result. Ann Surg. 2006;243:353–8. 17. Ng SS, Leung KL, Lee JF, et al. Laparoscopic-assisted versus open abdominoperineal resection for low rectal cancer: a prospective randomized trial. Ann Surg Oncol. 2008;15:2418–25. 18. Nagtegaal ID, van de Velde CJ, et al.; Cooperative Clinical Investigators of the Dutch Colorectal Cancer Group. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol. 2002;20: 1729–34. 19. Kelly SB, Mills SJ, Bradburn DM, et al. Effect of the circumferential resection margin on survival following rectal cancer surgery. Br J Surg. 2011;98:573–81. 20. Tilney SH, Rasheed S, Northover JM, et al. The influence of circumferential resection margins on long-term outcomes following rectal cancer surgery. Dis Colon Rectum. 2009;52:1723–9. 21. Leong QM, Son DN, Cho JS, et al. Robotic-assisted intersphincteric resection for low rectal cancer: technique and short-term outcome for 29 consecutive patients. Surg Endosc. 2011;25:2987–92. 22. Bianchi PP, Ceriani C, Locatelli A, et al. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a comparative analysis of oncologic safety and short-term outcomes. Surg Endosc. 2010;24:2888–94. 23. Park JS, Choi GS, Lim KH, et al. Robotic-assisted versus laparoscopic surgery for low rectal cancer; case-matched analysis of short-term outcomes. Ann Surg Oncol. 2010;17:3195–202.
