Conversion to Open Surgery During Minimally Invasive Right Colectomy for Cancer: Results from a Large Multinational European Study

Introduction

More than 1.9 million new colorectal cancer (CRC) cases and 935,000 deaths were estimated to occur worldwide in 2020 based on the GLOBOCAN estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer. CRC represents 10% of the overall cancer cases and 9.4% of cancer-related deaths, ranking third in terms of incidence, and second in terms of mortality. These data critically vary geographically, with the highest rates seen in the most developed countries. ¹ Right colon cancer (RCC) includes those tumors located in the cecum, the ascending colon, and the hepatic flexure. They constitute a unique entity within CRC presentations; they represent ∼28% of all CRC cases, and are associated with poorer prognosis compared with other CRC locations. ² Within RCC, hepatic flexure cancers have been associated with the worst disease-specific and overall survival rates. ³

Oncologic right colectomy is one of the commonest procedures performed in colorectal surgical units worldwide. Laparoscopy is nowadays considered as the gold standard approach for the resection of colon cancers. The use of laparoscopy has been associated with short-term benefits (i.e., shorter hospital stays, less postoperative pain, and faster return to normal activities) compared with open surgery while assuring equal oncologic adequateness and long-term prognosis.^4–9 The use of robotic platforms adds potential advantages to conventional laparoscopic colorectal resections. They include better ergonomics for the operating surgeon, and an increased precision and maneuverability provided by the tremor filtering, endo-wrist instruments, and three-dimensional view.^10,11

The possibility of conversion to open surgery is inevitably present during any minimally invasive (MIS) colorectal surgical procedure, including both laparoscopy and robotic surgery. The decision to convert may be taken when unfavorable anatomy or intra-abdominal conditions preclude an adequate progression of the procedure. Moreover, conversion may be required in cases of intraoperative surgical or medical complications. The occurrence of conversion during laparoscopic colorectal surgery is estimated at 17.9% ± 10.1% ¹² and in 6%–7.7% % for robotic procedures.^13–15

Conversions have been associated with worsened early postoperative outcomes (e.g., higher postoperative complications, delayed bowel recovery, and extended hospitalization) compared with cases completed by the initial approach.^{12,13,15–18} Moreover, the most recent literature showed that converted patients also present with impaired long-term oncologic outcomes when taking into account all colonic^16,19,20 or colorectal resections.^12,17 However, anterior rectal resection, left colectomy, or segmental colonic resection at the splenic flexure are completely different procedures than right colectomy and should not be evaluated as a whole. ²¹ Indeed, right colectomy is technically challenging owing to the particularities of the right and middle colic vascular anatomy, which may hamper the application of MIS. Of note, a recent international survey of 440 digestive and colorectal surgeons observed that half of the responders performed <25% of right hemicolectomies via a laparoscopic approach. ²²

To the best of our knowledge, no previous study has evaluated the causes and consequences of conversion to open surgery during minimally invasive right colectomy (MIS-RC). To fill this gap, this study (i) describes the different reasons leading to convert to open surgery a MIS right colon cancer resection, and (ii) analyses the impact of conversion on short- and the long-term surgical and oncological outcomes.

Materials and Methods

This study was designed as an ancillary analysis of the Minimally InvasivE surgery for oncologic Right ColectomY (MERCY) Study Group database. ²³ The MERCY collaborators developed a multicenter retrospective cohort study including patients undergoing MIS-RC in 21 referral centers from 6 European countries (i.e., France, Ireland, Italy, Spain, Switzerland, United Kingdom). The MERCY database included anonymous patient data selected from prospectively maintained local databases. As previously described, the surgical procedures were performed according to standardized surgical techniques, with at least standard D2-lymphadenectomy.^23,24 All the patients were treated and followed up after surgery according to standardized local protocols.

The inclusion criteria were as follows: (a) adult patients undergoing an oncologic MIS-RC for the treatment of nonmetastatic adenocarcinoma (AJCC 0–III) located in the right colon (i.e., cecum, ascending colon, or hepatic flexure); (b) elective curative-intent surgeries performed by laparoscopy or robotic surgery between January 2014 and December 2020; and (c) procedures performed by experienced colorectal surgeons. Extended right colectomy and hand-assisted procedures were not considered. The study was conducted in accordance with the ethical principles of the Declaration of Helsinki and used exclusively patients' medical records, which were anonymized and treated in conformity to the principles declared to the National Commission for Data Protection and Liberties. The study was reported following the STROBE checklist. ²⁵

The primary endpoint was conversion to open surgery, as defined by extending one of the incisions to perform any step of the procedure other than the anastomosis or specimen removal, or performing a formal laparotomy to complete the operation. ²⁶ Therefore, an additional port insertion or an extracorporeal anastomosis confection were not considered as a conversion. To explore the potential associations between conversion to open surgery and patients' and disease characteristics, baseline (preoperative) data, including age, sex, previous surgeries, American Society of Anesthesiologists (ASA) classification, body mass index (BMI), and comorbidities were collected and compared between the group of converted patients and the group of nonconverted patients.^27,28 Disease characteristics included tumor location and histopathological variables such as: location, pT stage, pN stage, R0 resection, and number of lymph nodes retrieved. Postoperative complications were graded according to the Clavien–Dindo classification system, with severe morbidity being defined as grade ≥3. ²⁹ Prolonged postoperative ileus was defined as the absence of bowel movements or flatus associated with intolerance of oral intake lasting more than 3 days postoperatively. ³⁰ Anastomotic leakage was defined as all conditions characterized by a clinical or radiologic anastomotic dehiscence, with or without the need of surgical revision. ³¹ Disease-free survival (DFS) was measured from the date of surgery to the date of confirmed tumor recurrence (local or distant), or to the latest follow-up.

Results

The original MERCY database included a total of 1870 consecutive patients undergoing MIS-RC for nonmetastatic RCC. Of these, 296 patients were excluded from the present analyses owing to missing data regarding one or more variables of interest. Therefore, 1574 patients were included in the final analytic sample.

The median age was 75 (13) years, and 50.4% of the patients were women. Patient demographics and preoperative clinical data are given in Table 1. Overall, 120 patients (7.6%) required conversion to open surgery. Male gender was more prevalent in the group of converted patients than in nonconverted ones (59.2% versus 48.8%; P = .028), and the rate of obesity (BMI >30 kg/m²) was also higher among converted patients (25.8% 18.6%; P = .052). There were no significant differences between the groups regarding previous abdominal surgery, comorbidities, type of surgical approach, and tumor location. The conversion rate was 7.8% and 6.5% in laparoscopic ad robotic RC (P = .549), respectively. The main reasons for conversion, representing together >65% of cases, included the following: technical difficulties related to adherences of previous surgeries (39.2%) or owing to tumor size or infiltration of adjacent structures (26.7%). Other important causes of conversion were intraoperative bleeding, bowel injuries, difficulties owing to patient's adiposity or excessive bowel distension, intraoperative medical complications, and inability to find the colonic neoplasm by laparoscopy (Table 2).

The surgical procedures in which conversion occurred were characterized by longer operative times (180 minutes versus 175 minutes; P = .03) and higher intraoperative blood loss (100 mL versus 70 mL; P = .001). Converted patients developed more postoperative complications, both overall (39.2% versus 27.5%; P = .006) and severe postoperative complications (13.3% versus 8.3%; P = .061). Similarly, the incidence of postoperative ileus (6.7% versus 2.5%; P = .009) and the need of blood transfusion (18.3% versus 8.3%; P = .001) were higher in the conversion group. The median hospital stay was 1 day longer in the conversion group (8 days versus 7 days; P = .01). There were no significant differences between the groups in terms of anastomotic leak rates, hospital readmissions, and 90-day postoperative mortality (Table 3). Focusing the histopathologic outcomes, no differences were found in the number of harvested lymph nodes (22 versus 21; P = .829), but the presence of lymph node involvement was slightly higher among the converted cases (35% versus 28.7%; P = .143). There were significant differences in the rates of pT4 cancers (22.5% versus 9.6%; P = .001) and the presence of lymphovascular invasion (37.5% versus 23.8%; P = .001) between the two groups.

For the multivariate analysis, significant variables at univariate level were included in the model together with those considered clinically relevant (Table 4). The variables independently associated with the need of conversion to open surgery were male gender, obesity, prior abdominal surgery, and pT4 cancers. There was no significant impact of the use of robotic surgery in reducing the odds for conversion (Table 4). Although conversion was significantly associated with tumor recurrence at the univariate analysis, this association was no longer significant when considering multiple covariates in the multivariate analysis (P = .320). Predictors of tumor recurrence were severe postoperative complications, pT4 cancer, lymph node involvement, and presence of lymphovascular invasion.

Discussion

This study, based on a large European multicentric database, showed that MIS-RC is a safe and feasible surgical treatment for RCC being associated with a low rate of conversion to open surgery (7.6%). The main causes of conversion were related to patient and tumor characteristics. Only 16.7% of the conversion was caused by intraoperative medical or surgical complications. As expected, converted RC procedures required longer operative times and these patients experienced significantly more postoperative complications and thus longer hospital stays than patients for whom the MIS-RC went uneventful.^16–18 Unplanned conversion to open surgery during laparoscopic and robotic colorectal procedures has been shown to be an independent predictor of morbidity and mortality.^13,15 In accordance with previous evidence, male gender, obesity, previous abdominal surgery, and pT4 cancers were associated with greater odds for conversion.^{12,14,16–18} Although robotic colectomy has been associated with lesser conversion in other studies,^11,18,33 this result was not observed in this study where the incidence of conversion to open surgery was similar between laparoscopic and robotic RC.

Regarding the long-term oncologic outcomes, the most recent meta-analysis aiming to determine the oncological impact of conversion in laparoscopic colorectal cancer surgery was published in 2015. It included 5293 patients from 15 studies and showed that converted patients presented with unfavorable outcomes in terms of 30-day mortality, long-term disease recurrence, and overall mortality. ¹² A more recent report on 1196 patients with stages I–III colonic adenocarcinoma operated on between 2000 and 2012 concluded that conversion was a marker of worse oncologic outcomes, as both overall and DFS were impaired in those patients experiencing conversion. ¹⁹ Another retrospective analysis on 4010 patients also concluded that conversion was an independent predictor of overall and DFS. ¹⁶ The present data contrast with them, as conversion per se appeared to have no significant impact on the oncologic prognosis. These results were obtained via multivariate analyses in which the potential effect of confounders (e.g., T4 cancers, lymph node involvement) were taken into account. This has not been explored previously, as in our knowledge this is the first study to evaluate the reasons and impact of conversion specifically during MIS-RC for RCC.

The analyses were conducted on a large and relatively homogenous sample of patients with nonmetastatic RCC undergoing surgery in highly experienced European surgical units. This may explain the low rate of conversion observed and may also limit the generalizability of the findings. Moreover, data were analyzed retrospectively, and thus the possibility of residual confounders and bias cannot be ruled out. The decision-making process for converting an MIS-RC into open surgery is complex and based on several factors. The main reason for conversion was evaluated, but the exact timing for conversion was not recorded. It has been postulated that early conversions owing to adhesions or obesity are associated with better outcomes than latter conversions because complications or lack of progress.^15,34

In conclusion, conversion to open surgery during MIS-RC for cancer was more frequently because of technical difficulties related to tumoral invasion, previous surgical interventions, or patient adiposity. Its occurrence was associated to a worsened postoperative course although it did not impact on the patient's DFS.