Short-term outcomes of single-incision robotic colectomy versus conventional multiport laparoscopic colectomy for colon cancer

Since the da Vinci SP (dVSP) surgical system was introduced, single-incision robotic surgery (SIRS) for colorectal diseases has gained increasing acceptance. Comparison of the short-term outcomes between SIRS using dVSP and those of conventional multiport laparoscopic surgery (CMLS) was performed to verify its efficacy and safety in colon cancer. The medical records of 237 patients who underwent curative resection for colon cancer by a single surgeon were retrospectively reviewed. Patients were divided into two groups according to surgical modality: SIRS (RS group) and CMLS (LS group). Intra- and postoperative outcomes were analyzed. Of the 237 patients, 140 were included in the analysis. Patients in the RS group (n = 43) were predominantly female, younger, and had better general performance than those in the LS group (n = 97). The total operation time was longer in the RS group than in the LS group (232.8 ± 46.0 vs. 204.1 ± 41.7 min, P < 0.001). The RS group showed faster first flatus passing (2.5 ± 0.9 vs. 3.1 ± 1.2 days, P = 0.003) and less opioid analgesic requirement (analgesic withdrawal within 3 postoperative days: 37.2% vs. 18.6%, P = 0.018) than the LS group. The RS group showed a higher immediate postoperative albumin level (3.9 ± 0.3 vs. 3.6 ± 0.4 g/dL, P < 0.001) and lower C-reactive protein level (6.6 ± 5.2 vs. 9.3 ± 5.5 mg/dL, P = 0.007) than the LS group during the postoperative period. On multivariate analysis after adjusting for deviated patient characteristics, no significant difference was observed in short-term outcomes, except for operation time. SIRS with dVSP showed short-term outcomes comparable with those of CMLS for colon cancer.


Introduction
Since the recent introduction of the da Vinci SP (dVSP) surgical system (Intuitive Surgical System, Sunnyvale, CA, USA), single-incision robotic surgery (SIRS) has been adopted in various surgical fields. Several reports are available on the application of SIRS in colorectal diseases [1][2][3][4][5][6][7][8][9][10][11]. Although most studies included single cases or small-sized case series to investigate SIRS feasibility, they reported the feasibility of SIRS in colorectal diseases with favorable perioperative outcomes including intraoperative complications, estimated blood loss, operation time, and postoperative recovery. In addition, its oncological safety, estimated by the extent of lymph node dissection and resection margin, has been validated in patients with malignancies [1,2,5,6,8,9,11].
A recent randomized controlled trial has indicated that single-incision laparoscopic surgery (SILS) can be considered as a viable surgical option for selected patients, particularly when executed by a proficient and skilled surgeon [12]. Despite numerous previous studies confirming the surgical completeness achieved through SILS, it remains a formidable procedure for inexperienced surgeons, necessitating a substantial level of expertise for successful adaptation [13,14]. According to previous studies, SILS for colon cancer may involve technical difficulties such as instrument crowding, inline positioning of the laparoscope, and insufficient triangulation due to the use of straight instruments through a single port [15][16][17][18]. SIRS can overcome the problems observed in SILS due to technical innovations, which include two joints called wrist and elbow joints, an articulating endoscope, and a 360° rotatable boom.

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To confirm the efficacy and safety of SIRS, a comparative study with conventional laparoscopic surgery, which has traditionally been performed, is warranted. This study aimed to compare the short-term outcomes of single-incision robotic colectomy with those of conventional multiport laparoscopic surgeries (CMLSs) to verify their efficacy and safety in the treatment of colon cancer.

Patients
The medical records of 237 patients who underwent curative resection for colon cancer between February 2019 and August 2022 were retrospectively reviewed. All surgeries were performed by a same surgeon. The selection of surgical modalities was determined by patient preference subsequent to a comprehensive explanation of each procedure. We included patients diagnosed with pathologically proven adenocarcinoma from the cecum to the rectosigmoid junction and excluded those who underwent open and emergency colectomy for colon cancer. Patients with metastatic disease or synchronous malignancies and who underwent combined surgery for other diseases were excluded. Patients were divided into two groups according to surgical modality: SIRS (RS group) and CMLS (LS group). Patient characteristics, pathological data, and intra-and postoperative outcomes were compared between the groups.

Surgical techniques and postoperative care
Overall surgical techniques were similar between the two approaches, except for the surgical modality. The operation theater setup for SIRS is illustrated in Fig. 1a. In the context of left-sided colon surgery, the patient cart was positioned on the left side of the patient. Conversely, for right-sided colon surgery, the positioning of the patient cart was reversed. Following the creation of a mini-laparotomy through a vertical trans-umbilical incision, a single-port entry system was implemented for SIRS. Throughout the procedure, the surgical assistant carried out tasks such as endoscopic suction, placement of suture materials within the pelvic cavity, and specimen removal via the remaining trocar of the single-port entry system (Fig. 1b). Conventional laparoscopic surgery was performed using a multiport approach with four ports. A trocar with a diameter of 10 mm was inserted through the umbilicus for endoscopic camera application, while three additional trocars were positioned corresponding to the tumor location. In the context of leftsided colon surgery, a 12-mm trocar was placed in the right lower quadrant, while two 5-mm trocars were positioned in the right upper and left lower quadrants, respectively. Similarly, for right-sided colon surgery, a 12-mm trocar was inserted into the left lower quadrant, and two 5-mm trocars were placed in the left upper and right lower quadrants, respectively. The umbilical port was extended to serve as the site for specimen extraction following the completion of the intracorporeal procedure.  [19,20]. After complete mobilization of the colon along the embryologic plane, lymph node dissection and CVL were performed according to the tumor location. In the case of right hemicolectomy, the ileocolic artery was ligated at the origin from the superior mesenteric artery. The root of mid-colic artery was invariably dissected, and the level of ligation varied depending on the tumor location. In the case of transverse colectomy, the root of mid-colic artery was ligated. For left colon cancer, lymph node dissection around the root of the inferior mesenteric artery (IMA) was performed, and the ligation level of IMA depended on the tumor location. In the case of left hemicolectomy, the left colic artery was ligated. Low ligation of IMA was usually performed in anterior resection (AR) and low anterior resection (LAR). High ligation of IMA was performed when lymph node metastasis around IMA was suspected. During right, transverse, and left colectomy, bowel resection and anastomosis were performed extracorporeally, except during the most recent four cases. After the recent adoption of intracorporeal anastomosis for right and left colectomy, two cases of right colectomy in CMLS and two cases of left colectomy in SIRS followed this procedure. An umbilical incision for docking was used for SIRS, and mini-laparotomy through the umbilicus was used in CMLS. In AR and LAR, the abovementioned incision was used for extracorporeal procedures. The technique for abdominal wall closure was the same in both groups.
We applied the same postoperative protocol to patients who underwent minimally invasive surgery. Regarding diet building, sips of water were started on postoperative day 1, and a liquid diet was started on postoperative day 2. A soft diet was initiated when the patient showed gaspassing and tolerable bowel gas patterns on radiography. The Foley catheter was removed on postoperative day 1. Primarily, fentanyl-based patient-controlled analgesics were administered to all patients. Additionally, we administered a low dose (25 mg) of pethidine three times per day for 3 days postoperatively. Opioid withdrawal was conducted when opioid overdose symptoms, such as dizziness and nausea, were reported by the patient and pain could be managed with non-opioid analgesics, such as acetaminophen or NSAIDs. Routine laboratory tests including complete blood counts, liver function tests, and C-reactive protein (CRP) levels were performed daily immediately after surgery until postoperative day 5. Major complication was defined as Clavien-Dindo (CD) classification grade ≥ 3b, which required intervention under general anesthesia.

Statistical analysis
Continuous variables were compared using Student's t-test and are presented as means and standard deviations. Categorical variables were analyzed using the chi-square test or Fisher's exact test and presented as frequencies. Logistic or multiple regression analysis was used for multivariate analysis to adjust for differences in baseline characteristics between the two groups. P < 0.05 was considered statistically significant. All data were analyzed using IBM SPSS Statistics for Windows version 23 (IBM Corp., Armonk, NY, USA).

Patient characteristics and pathological data
Baseline patient characteristics differed between the two groups, except for body mass index (BMI) and preoperative carcinoembryonic antigen levels. Patients in the RS group showed lower ages (58.8 ± 7.7 vs. 70.6 ± 7.7 years, P < 0.001) and higher female predominance (72.1% vs. 35.1%, P < 0.001) than the LS group. The patients with American Society of Anesthesiologists classification 1 and 2 were found more often in the RS group than in the LS group (95.3% vs. 62.9%, P < 0.001) ( Table 1).
The RS group showed a lower pathological stage (P = 0.04) and histological grade (P = 0.039) than the LS group. No significant difference in rates of lymphovascular (P = 0.578) or perineural invasion (P = 0.297) was observed. The number of harvested lymph nodes was sufficient in both groups, and no difference was observed between the groups (22.1 ± 10.5 vs. 23.4 ± 10.7, P = 0.432). No cases of tumor involvement at the resection margins and no significant difference in the distance from the tumor to the proximal and distal margins were observed between the two groups ( Table 1).

Intraoperative outcomes
The procedures performed were right/left hemicolectomy, transverse colectomy, and anterior/low anterior resection; their distributions were not significantly different (P = 0.162). Operation time was longer in the RS group than in the LS group (232.8 ± 46.0 vs. 204.1 ± 41.7 min, P < 0.001). Estimated blood loss was not different between the groups (60.0 ± 38.7 vs. 71.3 ± 71.3 ml, P = 0.305). Intraoperative transfusion (3.1%) and conversion to open surgery (2.1%) were observed only in the LS group, although the difference was not statistically significant (Table 2).

Multivariate analysis for intra-and postoperative outcomes
Multivariate analysis was performed to adjust for the baseline characteristics of patients, including age, gender, American Society of Anesthesiologists (ASA) classification, body mass index (BMI), and tumor stage. In the intraoperative outcomes, only the operation time was longer in the RS group than in the LS group (P < 0.001). The days to first flatus and rate of opioid withdrawal, which showed significant results in univariate analysis, were not different between the two groups in multivariate analysis. Moreover, postoperative inflammatory/immune marker levels did not differ between the two groups (Table 4).

Discussion
In the present study, SIRS for colon cancer showed shortterm outcomes comparable to those of CMLS. Although the operation time was longer in SIRS than in CMLS, all robotic surgeries were performed safely, with proper lymph node harvesting and adequate resection margins. In the univariate analysis, several outcomes, such as bowel movement recovery, postoperative pain, and laboratory results, were better in SIRS than in CMLS. After adjusting for baseline   characteristics, there was no significant difference between the two groups in terms of short-term outcomes. Among the intra-and postoperative outcomes, the operation time was longer in the RS group than in the LS group after adjusting for baseline characteristics. According to previous studies, robotic surgery generally entails a longer operating time than that of laparoscopic surgery, which is primarily attributed to the time-consuming processes involved such as docking and interchanging robotic instruments [21]. Although only a few minutes were necessary for a docking for all procedures in SIRS using dVSP, the time required to interchange robotic instruments during the procedure extended the operation time. Considering the characteristics of SIRS using dVSP, frequent boom movement also consumes operation time due to the inherent limitation of the working range of robotic arms. In addition, similar to other new techniques, such as laparoscopic and robotic surgery, a learning curve for SIRS is unavoidable. We enrolled patients who underwent SIRS from the beginning of our use of robotic surgery in this facility-and slower surgeries at the beginning of the learning curve could be a factor in the longer operation times. The lack of advanced energy devices in dVSP for fast architectural dissection and safe excision of the bowel mesentery and omentum can be another reason for the longer operation time in SIRS.
There are concerns regarding the oncological safety of SIRS. Although previous studies on SIRS were conducted with small sample sizes to investigate the feasibility of the procedures, they reported sufficient number of lymph node harvest for staging and proper resection margin [1,2,5,6,8,9,11]. Our results are consistent with those of previous studies. In the present study, the number of harvested lymph nodes and resection margins did not differ from those of CMLS. Although tumor stage and histology were advanced in the LS group, oncological safety may not differ in the same tumor staging between the two groups. Long-term oncological outcomes must be investigated after proper follow-up.
Univariate analysis revealed faster bowel movement, less pain, and favorable laboratory test results in the RS group. Less wound pain may result in faster recovery, including bowel movement and better laboratory test results. In a previous meta-analysis comparing SILS and CMLS for colorectal cancer, the SILS group experienced less postoperative pain [22]. In a randomized controlled study assessing only postoperative pain in patients who underwent colectomy, Poon et al. also reported less postoperative pain in the SILS group than in the CMLS group [13]. Recently, we adopted intracorporeal anastomosis for right and left colectomies in both CMLS and SIRS. Recently enrolled patients in the present study followed this procedure (two cases of right colectomy in CMLS and two cases of left colectomy in SIRS). Although faster bowel recovery has been reported in patients who underwent intracorporeal anastomosis, judging by the limited number of cases and balanced distribution in both groups, the effect of this procedure on the overall results of present study might be minimal [23]. Further study on the advantage of intracorporeal anastomosis in SIRS will be performed after the accumulation of enough cases to be statistically significant.
In the present study, baseline characteristics differed between the two groups. This can be explained by patients' selection of the surgical modality. In our experience, younger, female patients, and patients with better general health are more health conscious and preferred robotic procedures. Furthermore, these patients were more likely to have private insurance, which could cover the high cost of robotic surgery; this may be another reason for selecting robotic surgery. Qiu et al. commented that differences in patient characteristics, such as age and general health status, between robotic and laparoscopic approaches might have affected the results of their meta-analysis of long-term oncological outcomes [24]. In the multivariate analysis to adjust for the difference between the two groups, no difference was observed in the short-term outcomes, except for operation time, which might be interpreted to imply that SIRS can be performed as safely as CMLS.
This study has several limitations. First, this singlecenter study had a retrospective design with a relatively small number of patients, which might have led to the heterogeneity of comparator groups and limits the generalization of the results. Second, a single surgeon performed all procedures, and the experience gap existed between conventional laparoscopic surgery and the recently adopted SIRS. Initial SIRS cases were enrolled during the surgeon's learning period, which might have negatively related to the outcomes in patients who underwent SIRS. Nevertheless, this study might be the first to compare SIRS with CMLS for colon cancer. Furthermore, although no significant results were observed in the multivariate analysis, better outcomes of SIRS in the univariate analysis, especially in terms of patient recovery and pain, may provide a clue for further studies.

Conclusions
SIRS showed short-term outcomes comparable to those of CMLS for colon cancer. Further analyses with a larger and more balanced cohort are required to confirm the efficacy and safety of single-incision robotic colectomy.