Introduction

Minimally invasive surgery (MIS) is becoming the gold standard in the treatment of colon cancer because of demonstrated benefits in postoperative recovery, pain and length of stay with comparable long-term oncological outcomes as for open surgery [1,2,3,4]. However, laparoscopic colon surgery requires a high degree of technical skills, especially in case of resection of locally advanced tumors, tumors at the hepatic flexure and proximal transverse colon or in the presence of extensive adhesions. These difficulties are associated with increased risk of conversion or not even considered for a laparoscopy at all.

The robotic platform is associated with a stable 3D view, an extra operative arm under the surgeon’s control and an increased dexterity thanks to articulating instruments. It therefore offers all advantages of MIS while decreasing the technical difficulties associated with laparoscopy, leading to significantly lower conversion rates [5]. It can also facilitate the use of an intracorporeal anastomosis which has a number of advantages over extracorporeal anastomosis including faster recovery of bowel function, decreased incidence of incisional hernias and reduction in surgical site infections [6].

These advantages of the robotic platform led us to initiate a robotic program for colon surgery at our institution. Since implementing this approach in our practice required a new set of skills, we used the standard right colectomy, a procedure considered representative of establishing a learning curve for robotic colorectal surgery [7], to evaluate its safety.

The current study determined a learning curve for the implementation of robotic right colectomy with ICA for right-sided colon tumors. We used conversion rate and postoperative morbidity to compare the safety of implementing robotic surgery in comparison with laparoscopic right colectomy with ECA, which was the standard in our practice.

Methods

Patient selection and data collection

Since the start of our robotic colorectal surgery program, data on patient demographics, clinical variables, procedure details and postoperative outcomes of all robotic colorectal resections have been prospectively collected for quality control and safety analysis in an anonymized database. Data on laparoscopic right colectomies were retrospectively collected from the electronic patient files of our hospital and added to our database.

From this data collection all consecutive laparoscopic and robotic standard right colectomies performed for (pre) malignant lesions between January 2014 and December 2020 by a single surgeon (EVE) were retrospectively analyzed. All laparoscopic procedures involved an extracorporeal anastomosis (ECA), while an intracorporeal anastomosis (ICA) was used in the robotic cases. Surgery for inflammatory bowel disease, redo-surgery, major concomitant surgery and emergency surgery were excluded from analysis, as were patients undergoing a robotic complete mesocolic resection with D3 resection that was stepwise implemented after establishing the learning curve.

Data analyzed included preoperative patient characteristics [age, gender, body mass index (BMI), American Society of Anesthesiology Score (ASA), Charlson comorbidity index, previous abdominal surgery], intraoperative details [total procedure time, conversion to laparotomy (and reason for conversion)] and postoperative outcome [length of stay, 30-day complication rate according to the Clavien–Dindo classification [8] and 90-day mortality]. Anastomotic leak was defined as a radiologically diagnosed intraperitoneal fluid collection or overt leak, requiring CT-guided drainage or reoperation and was reported separately. Peri-operative outcome variables were used for safety analysis of different study groups.

The study protocol was reviewed and approved by the ethics committee of our institution (B.U.N. 143201837797).

Surgical procedures for right colectomy

Laparoscopic right colectomy was performed using a medial to lateral approach with ligation of the ileocolic vessels followed by complete mobilization of the colon. The mesentery of the terminal ileum and colon (including the right colic vessels and the right branch of the middle colic vessels) was transected after externalization of the colon through an abdominal incision with wound protector, and an ECA was made.

Robotic standard right colectomy was performed using the da Vinci Xi Surgical System (Intuitive Surgical, Inc., Sunnyvale, CA, USA) after laparoscopic exploration, adhesiolysis, and positioning of the small bowel to the left side. A suprapubic bottom-up approach was implemented for bowel mobilization taking care to preserve the mesocolonic window. Mobilization was followed by ligation of the ileocolic vessels, ligation of the right branch of the middle colic artery and division of the remaining mesentery without bowel externalization. To determine the transection level of both bowel segments we evaluated vascularization by indocyanine green angiography (Firefly™ Fluorescent Imaging, Intuitive Surgical, Inc.). Bowel segments were transected using a robotic stapler and a mechanical isoperistaltic side-to-side anastomosis was created. The remaining enterotomy was closed with a running suture. After undocking the robot, the specimen was retrieved via a Pfannenstiel incision with wound protector.

Learning curve analysis

Cumulative sum (CUSUM) of total procedure time of all consecutive standard robotic right colectomies with ICA for (pre)malignant lesions since the start of our program until December 2020 was performed for learning curve analysis. Total procedure time is defined as the time between the first incision until skin closure and includes laparoscopic exploration, docking time as well as console time. When using chronologically arranged data, this method allows learning curve analysis thanks to its ability to reveal rapid trend changes in data sets [9].

Statistical analysis

Individual patient and operative characteristics were stored in our password protected Microsoft Excel database (Microsoft Corp., Redmond, WA, USA). Results are presented as median (range) or percentage if not otherwise specified. Statistical analysis was performed using SPSS (IBM, Armonk, NY, USA) and Prism 9 for macOS (GraphPad Software, San Diego, CA, USA). Non-parametric tests [two tailed Mann–Whitney U (MWU) test or Kruskall-Wallis test for continuous variables and Chi-squared test/Fisher’s exact test when appropriate for categorical variables] were used for analysis. Statistical significance was assumed at p < 0.05.

Results

Determination of a learning curve for robotic right colectomy

During the study period, 67 robotic standard right colectomies with intracorporeal anastomosis were performed at our center. We used total procedure time of these cases to create a CUSUM plot for learning curve analysis (Fig. 1). The initial learning phase of the plot (phase 1) consists of 11 cases, after which a first decrease in the slope is observed. After 35 cases, the second phase (consolidation phase) of the CUSUM plot turns into a negative slope, indicating the end of the learning phase and the start of the experienced phase (phase 3). A positive slope during phase 1, followed by a plateau for phase 2 and a negative slope during phase 3 was confirmed by linear regression testing (Fig. 1). When using console time as alternative variable for learning curve analysis, the learning phase ended after 29 cases (data not shown).

Fig. 1
figure 1

Total procedure time of robotic right colectomy represented as CUSUM plot and showing three phases—initial learning phase (phase 1), stabilization phase (phase 2) and experienced phase (phase 3)—of the learning curve separated by dotted lines (A), and lines of best fit for the initial learning phase 1 (B), the stabilization phase 2 (C) and the experienced phase 3 (D)

Safety of implementation of robotic standard right colectomy

Baseline patient and tumor characteristics of the 35 patients that underwent a robotic colectomy during initial learning phase 1 and consolidation phase 2 of the learning curve are summarized in Table 1 and compared to our last cohort of 38 patients that underwent a laparoscopic right colectomy. We could not identify any significant differences in patient body mass index (BMI) or comorbidities although patients treated by robotic surgery were older and tended to be more frequently classified as American Society of Anesthesiologists class III or IV. There were no differences in surgical indication or tumor stage.

Table 1 Patient characteristics and peri-operative outcome

Total procedure time was significantly longer in the robotic cases when compared to laparoscopy.

Peri- and postoperative outcome variables were used as safety measure for both procedures and are shown in Table 1. There was no difference in 30-day morbidity. There was no difference in anastomotic leakage rate between robotic and laparoscopic cases. The length of stay was statistically significantly shorter in the robotic group when compared to the laparoscopic group. Robotic right colectomy was associated with a reduction in conversion rate from 16 to 3 percent. There was one 90 day mortality in the robotic group (3%) while this was not the case in the laparoscopy-treated patients.

Outcome of robotic right colectomy beyond the learning phase

After initiating the experienced phase (from case 36), there was a significant reduction in total operative time for patients undergoing robotic right colectomy with intracorporeal anastomosis (Table 1). While console time also tended to be shorter, this difference was not significant. None of the procedures performed after completing the learning phase had to be converted to open surgery. We observed no mortality, but major postoperative morbidity was reduced from 11 to 6 percent. Median length of stay significantly decreased from 6 to 5 days.

Discussion and conclusions

Despite the fact that minimally invasive surgery for right-sided colon cancer has a variety of benefits for the patient with at least equivalent oncological outcomes [1, 3], open surgery is still widely performed [10]. A recent international survey demonstrated that laparoscopic right colectomy with ICA is performed in a minority of cases [11]. This is mainly attributed to technical challenges associated with laparoscopy. The robotic platform might help overcome these technical difficulties thanks to articulated instruments improving dexterity and a stable 3D view in combination with an additional arm that further aids exposure of the surgical field and allows precise dissection [12, 13].

This prompted us to initiate a robotic colorectal surgery program at our center. Since this technique requires a specific set of skills for the surgeon and operating team, patient morbidity and peri- and postoperative outcomes throughout its learning phase were studied and compared with preceding laparoscopic cases. To our knowledge, the present study is one of the first to perform such an assessment for robotic right colectomy with ICA using the da Vinci Xi system.

CUSUM analysis of total procedure time of all first consecutive robotic right colectomies was used to determine the length of the learning phase. It is considered a valuable tool for this purpose in different types of surgery, including colorectal robotic procedures [14,15,16] and compares sequential changes in total procedure time to their average. Data are represented in a CUSUM plot from which three different stages of surgical experience can be deduced. In our study, the total learning phase was completed after 35 patients. This is at variance with other authors that report a consolidation of the learning phase after 68 or 90 cases respectively [17, 18]. We were not able to identify patient or tumor characteristics attributing to these differences but patient characteristics, postoperative outcome and complication rate might be of added value to the learning curve analysis. However, this would make this analysis more complex [19] and given the low number of adverse events reported in our series also make such a risk-adjusted CUSUM analysis difficult to interpret.

We used peri-operative outcome and conversion rate of the 35 learning phase cases to evaluate the safety of implementing the robotic platform for right colectomy and compared it to the last cohort of 38 patients undergoing laparoscopy. While peri-operative morbidity was comparable in both groups, there was a significantly shorter length of stay for patients undergoing robotic surgery. This reflects a faster recovery from surgery and can at least partially be attributed to the ICA that was performed in patients undergoing robotic right colectomy while all laparoscopically treated patients had extracorporeal anastomosis [20]. A recent meta-analysis also favored ICA over ECA because of faster bowel function recovery, lower anastomotic leakage rate and less surgical site infections; however, most cited studies were retrospective [6]. We hope that the Mircast study, an ongoing prospective observational cohort study comparing intra- and extracorporeal anastomosis, will provide more evidence [21].

Even during the learning phase we observed a significant reduction in conversion rate (from 15.8 to 2.3%) in the robotic group compared to laparoscopy, to a level as low as previously reported for robotic right colectomy [22,23,24]. This reduction might be explained by the reasons for conversion, which were predominantly related to tumor characteristics (n = 3) and adhesions (n = 3) during laparoscopy, while bleeding was the cause in the robotic surgery group (n = 1). This observation is in line with reported differences in risk factors between laparoscopic and robotic colon procedures that can lead to unplanned conversion to open surgery [25].

Our reported initial experience with robotic surgery confirms that this technique can be safely implemented in a colorectal surgery practice without increasing risk for peri-operative complications, even during the learning phase.