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

doi:10.21203/rs.3.rs-2968794/v1

Since the da Vinci SP (dVSP) surgical system was introduced, single-incision robotic surgery (SIRS) for colorectal diseases has gained increasing acceptance. We compared the short-term outcomes of SIRS using dVSP with those of conventional multiport laparoscopic surgery (CMLS) 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.

colon cancer

laparoscopic surgery

robotic surgery

single incision

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 [1–11]. Although most studies included single cases or small-sized case series to investigate SIRS feasibility, they reported the feasibility of SIRS in colorectal diseases. 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]. However, to confirm its efficacy and safety, a comparative study with conventional laparoscopic surgery, which has traditionally been performed, is warranted.

There have been concerns regarding the surgical and oncological safety of minimally invasive single-incision surgery. According to recent studies, single-incision laparoscopic surgery (SILS) for colon cancer is a safe surgical modality, although technical difficulties, such as instrument crowding, inline positioning of the laparoscope, and insufficient triangulation, have been detected [12–15]. Therefore, concerns regarding surgical completeness are no longer controversial in minimally invasive, single-incision surgery performed by experienced surgeons. In addition, 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.

Since we reported the first study of SIRS with dVSP for colorectal disease, we have been continuously implementing SIRS with satisfactory outcomes for benign and malignant colorectal diseases [5]. 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. To the best of our knowledge, this is the first study to compare SIRS with CMLS.

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 single surgeon. 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. SIRS was performed through an approximately 3.5 cm trans-umbilical incision using the dVSP surgical system. Conventional laparoscopic surgery was performed using a multiport approach with four trocars.

All surgeries constituted complete mesocolic excision with central vascular ligation (CVL) [16, 17]. 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 gas-passing 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 enrollment

A total of 237 patients who underwent surgery for colon cancer between February 2019 and August 2022 were investigated. Patients who had open surgery (n=3), emergency surgery (n=13), combined surgery (n=30), surgery for double primary colorectal cancer (n=3), and distant metastasis (n=48) were excluded. Of the 140 patients, 43 (30.7%) underwent SIRS (RS group) and 97 (69.3%) underwent CMLS (LS group) (Fig. 1).

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±71.3ml, 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).

Postoperative short-term outcomes

The complication rate did not differ between the groups (16.3% vs. 20.6%, P=0.548), and major complications were only detected in the LS group (4.1%). The RS group showed faster first flatus passing (2.5±0.9 vs. 3.1±1.2 days, P=0.003) and a lower opioid analgesic requirement than the LS group (opioid analgesic withdrawal within 3 postoperative days: 37.2% vs. 18.6%, P=0.018) (Table 3).

Regarding basic inflammatory/immune markers, the RS group showed higher immediate postoperative albumin level (3.9±0.3 vs. 3.6±0.4 g/dL, P<0.001) and lower maximal CRP levels during the postoperative period (6.6±5.2 vs. 9.3±5.5 mg/dL, P=0.007) (Table 3).

Multivariate analysis for intra- and postoperative outcomes

Multivariate analysis was performed to adjust for the underlying characteristics of deviated patients. 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).

In the present study, SIRS for colon cancer showed short-term 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. In general, the operation time was longer in robotic surgery owing to the docking time and interchange of robotic instruments [18]. 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 our 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. The presence of less parietal trauma in SIRS may be related to these positive outcomes. In a previous meta-analysis comparing SILS and CMLS for colorectal cancer, the SILS group experienced less postoperative pain [19]. 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 [20]. Less wound pain may result in faster recovery, including bowel movement and better laboratory test results. 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 [21]. Until now, there have been several studies on the advantage of intracorporeal anastomosis using a robotic approach [22]. 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 [23]. 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 single-center study had a retrospective design with a relatively small number of patients, which 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.

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.

Author contributions Contributors to conception, design, acquisition of data, and interpretation of data: Noh GT, Kim HS. Manuscript writing and drafting: Kim HS. Revising it critically for important intellectual content: Noh GT. Final approval of the version to be published: Noh GT, Kim HS, Oh BY, Chung SS, Lee RA.

Funding The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Data availability The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing Interests The authors declare no conflict of interest for this article.

Ethics approval This is an observational study This study was reviewed and approved by the institutional review board of Ewha Womans University Seoul hospital [SEUMC 2023-01-019].

Informed consent Due to the retrospective nature of this study after the patient encounter and account were closed, the consent process for participation was waived by our Institutional Review Board.

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Table 1 Patient characteristics and pathologic data

	Robot (n=43)	Laparoscopy (n=97)	P
Age, years	58.8 ±7.7	70.6 ±7.7	<0.001
Gender, n (%) Male Female	12 (27.9) 31 (72.1)	63 (64.9) 34 (35.1)	<0.001
ASA classification, n (%) 1,2 3,4	41 (95.3) 2 (4.7)	61 (62.9) 36 (37.1)	<0.001
BMI, kg/m²	23.4 ±3.0	24.3 ±7.7	0.443
Preoperative CEA, ng/mL	4.9 ±8.8	6.0 ±7.9	0.467
Stage, n (%) 0 I II III	6 (14.0) 11 (25.6) 6 (14.0) 20 (46.5)	5 (5.2) 21 (21.6) 34 (35.1) 37 (38.1)	0.04
Histology, n (%) Well differentiated Moderately differentiated Poorly differentiated/mucinous/signet	12 (27.9) 30 (69.8) 1 (2.3)	12 (12.4) 76 (78.4) 9 (9.3)	0.039
Lympho-vascular invasion, n (%) Present Absent	13 (30.2) 30 (69.8)	34 (35.1) 63 (64.9)	0.578
Perineural invasion, n (%) Present Absent	8 (18.6) 35 (81.4)	26 (26.8) 71 (73.2)	0.297
Number of harvested lymph nodes	22.1 ± 10.5	23.4 ± 10.7	0.432
Number of positive lymph nodes	1.1 ± 1.8	1.6 ± 3.0	0.257
Resection margin involved, n (%)	0	0	NA
Distance to proximal margin, cm	10.8 ± 6.2	12.8 ± 6.7	0.09
Distance to distal margin, cm	9.2 ± 6.6	11.3 ± 7.3	0.102

Continuous variables are described as a mean and standard deviation.

SD standard deviation, ASA American society of anesthesiologists, BMI body mass index, CEA carcino-embryonic antigen, NA not applicable

Table 2 Intraoperative outcomes

	Robot (n=43)	Laparoscopy (n=97)	P
Procedures performed, n (%) Right hemicolectomy Transverse colectomy Left hemicolectomy Anterior resection Low anterior resection	12 (27.9) 0 6 (14.0) 22 (51.2) 3 (7.0)	42 (43.3) 1 (1.0) 8 (8.2) 33 (34.0) 13 (13.4)	0.162
Operation time, min	232.8 ± 46.0	204.1 ± 41.7	<0.001
Estimated blood loss, ml	60.0 ± 38.7	71.3 ± 71.3	0.305
Intraoperative transfusion, n (%)	0	3 (3.1)	0.553
Conversion to open surgery, n (%)	0	2 (2.1)	0.343

Continuous variables are described as a mean and standard deviation.

Table 3 Postoperative short-term outcomes

	Robot (n=43)	Laparoscopy (n=97)	P
Complication, n (%)	7 (16.3)	20 (20.6)	0.548
Major complication^a, n (%)	0 (0.0)	4 (4.1)	0.312
Days to first flatus	2.5 ± 0.9	3.1 ± 1.2	0.003
Days to resuming soft diet	3.4 ± 1.3	3.8 ± 1.9	0.210
Opioid withdrawal^b, n (%)	16 (37.2)	18 (18.6)	0.018
Postoperative hospital stay, days	7.7 ± 2.0	8.6 ± 3.5	0.060
Interval to start chemotherapy, days	24.1 ± 4.5	27.0 ± 7.5	0.118
Inflammatory/immune markers^c
WBC, 10³/μL	12399.1 ± 3019.1	11896.6 ± 3660.1	0.432
Neutrophil, %	84.6 ± 8.9	84.2 ± 6.6	0.745
Lymphocyte, %	9.9 ± 3.7	10.1 ± 4.8	0.804
Albumin, g/dL	3.9 ± 0.3	3.6 ± 0.4	<0.001
Maximal CRP after operation, mg/dL	6.6 ± 5.2	9.3 ± 5.5	0.007

Continuous variables are described as a mean and standard deviation.

WBC white blood cell, CRP c-reactive protein

^aMajor complication was defined as the Clavien-Dindo (CD) classification grade ≥ 3b.

^bOpioid withdrawal is conducted when opioid overdosing symptoms were complained of and pain could be manageable with non-opioid pain killer.

^cLaboratory test values are the results obtained immediately after surgery, except for the CRP level.

Table 4 Multivariate analysis for intra-, postoperative outcomes

	Robot (n=43)	Laparoscopy (n=97)	P
Intra-operative outcomes
Operation time, min	232.8 ± 46.0	204.1 ± 41.7	<0.001
Estimated blood loss, ml	60.0 ± 38.7	71.3 ± 71.3	0.492
Intraoperative transfusion, n (%)	0 (0.0%)	3 (3.1%)	0.998
Conversion to open surgery, n (%)	0 (0.0%)	2 (2.1%)	0.997
Post-operative outcomes
Complication, n (%)	7 (16.3%)	20 (20.6%)	0.814
Major complication^a, n (%)	0 (0.0%)	4 (4.1%)	0.998
Days to first flatus	2.5 ± 0.9	3.1 ± 1.2	0.501
Days to resuming soft diet	3.4 ± 1.3	3.8 ± 1.9	0.588
Opioid withdrawal^b, n (%)	16 (37.2%)	18 (18.6%)	0.852
Postoperative hospital stay, days	7.7 ± 2.0	8.6 ± 3.5	0.434
Interval to start chemotherapy, days	24.1 ± 4.5	27.0 ± 7.5	0.723
Inflammatory/immune markers^c
WBC, 10³/μL	12399.1 ± 3019.1	11896.6 ± 3660.1	0.537
Neutrophil, %	84.6 ± 8.9	84.2 ± 6.6	0.248
Lymphocyte, %	9.9 ± 3.7	10.1 ± 4.8	0.149
Albumin, g/dL	6.6 ± 5.2	9.3 ± 5.5	0.130
Maximal CRP after operation, mg/dL	3.9 ± 0.3	3.6 ± 0.4	0.187

Continuous variables are described as a mean and standard deviation.

WBC white blood cell, CRP c-reactive protein

^aMajor complication was defined as the Clavien-Dindo (CD) classification grade ≥ 3b.

^bOpioid withdrawal is conducted when opioid overdosing symptoms were complained of and pain could be manageable with non-opioid pain killer.

^cLaboratory test values are the results obtained immediately after surgery, except for the CRP level.

No competing interests reported.

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

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Patients

Surgical techniques and postoperative care

Statistical analysis

Results

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