Colorectal cancer (CRC) is one of the most common malignancies (1). Among CRC, sigmoid colon cancer and rectosigmoid cancer are the most frequently operated diseases in Japan (2,3). Several studies have reported that laparoscopic surgery has benefits in short-term outcomes over open surgery with comparable long-term outcomes (2,4-7). Therefore, laparoscopic surgery is now more often performed. However, obesity is a major technical limiting factor for laparoscopic surgery because abundant visceral fat is known to extend the operation time (8,9). Furthermore, it is clear that extended operation time is correlated with higher complications (10,11).

The body mass index (BMI) is used as a simple measure tool to assess obesity. Several studies have shown that BMI is correlated with extended operation time and complications, while others did not (12-15). This is because no clear distinction was made between subcutaneous fat from visceral fat (16,17). Some studies showed that visceral fat area (VFA) is more strongly associated with postoperative morbidity than BMI (16-19). Recent studies have utilized quantitative computed tomography (CT) to determine visceral obesity by measuring VFA; however, special hardware is needed to assess it (16,17).

Preoperative contrast-enhanced CT (CECT) is performed generally to determine the stage of the tumor and to check the running pattern of the blood vessel. Goto et al. reported that the depth from the skin to the bifurcation of the celiac artery measured by CECT is more strongly associated with operation time during laparoscopic distal gastrectomy than BMI (20). Here, we hypothesized that the depth from the peritoneum to the bifurcation of the inferior mesenteric artery (IMA) defined as ‘peritoneum to IMA distance (PID)’ might better associate with extended operation time and surgical difficulty than BMI as in the previous study. Therefore, this study aimed to clarify the usefulness of measuring PID as a simple predictive factor for extended operation time during laparoscopic colectomy in patients with sigmoid or rectosigmoid colon cancer.

Patients. During December 2013 to December 2019, 134 patients diagnosed with sigmoid or rectosigmoid colon cancer underwent laparoscopic colectomy at the Kita-Harima Medical Center, Japan. Among the 134 patients, 10 patients were excluded: two patients were converted to laparotomy and eight patients had a resection of another major organ. A total of 124 patients who underwent laparoscopic colectomy were ultimately included (Figure 1). Of these patients, 56 patients were treated by surgeons who were board certified by the Japanese Society of Endoscopic Surgery (JSES). This system was established in 2004 to maintain quality and educate trainers by the JSES (21,22). To be a qualified surgeon of the JSES, an applicant is required to perform more than 20 laparoscopic major organ surgeries within 3 years. The applicant is also required to submit a non-edited video of these surgeries for review by at least two board-qualified referees.

In this retrospective study, the Union for International Cancer Control TNM staging system was used for staging (23). The lymph node stations and tumor locations were defined using the Japanese Society for Cancer of the Colon and Rectum (JSCCR) (24). The clinical, surgical, and pathological records of the patients were obtained from our database and individual electronic medical records. Postoperative complications were graded according to the Clavien–Dindo classification, and cases with a classification higher than grade II were defined as having a postoperative complication. The data collection and analysis were approved by the Institutional Review Board of the Kita-Harima Medical Center (03-22).

Surgical technique. Laparoscopic colectomy was performed using five trocars. The first 12-mm trocar was inserted transumbilically and the 12-mm port was placed in the lower right abdomen, and a 5 mm port was placed in upper side of both abdomen and lower left abdomen. The carbon dioxide pneumoperitoneum was maintained at 10 mmHg, and the patients were positioned on the operating table with the lithotomy position and head-right downed. Lymph node dissection was performed using an ultrasonically activated device through the trocars. The definition of D3 lymph node dissection was consistent with the JSCCR guidelines (24). Laparoscopic coagulation system was used in all cases. For the anastomosis technique, we selected Double Stapling Technique or functional end to end anastomosis according to the tumor location.

Definition of the depth of the inferior mesenteric artery from the peritoneum surface. We reviewed the preoperative CECT images of all patients and identified the peritoneum surface and the IMA bifurcation using the axial view. In all cases, we determined cancer stage using CECT in the supine position. The vertical distance from the peritoneum to the bifurcation from the aorta was defined as ‘peritoneum to IMA distance (PID)’ (Figure 2).

Statistical analysis. Statistical analysis was carried out using the EZR software. The relation between two variables was assessed using the Fisher exact test or chi-squared test and Student’s T-test or Mann–Whitney U-test. Variables with a p-value <0.05 in a univariate analysis were further evaluated in a multivariate analysis using the logistic regression model to assess the confounding variables. The optimal cut-off level of PID and thickness of subcutaneous fat (TSF) was determined by receiver operating characteristics (ROC) analysis. In all analyses, a p<0.05 was accepted as statistically significant.

The median (range) operation time was 213.5 (117-460) minutes. So, we classified patients into two groups according to the operation time: Early group (<210 min) and Late group (≥210 min). Patient characteristics are summarized in Table I. Higher rate of female sex and lower BMI were observed in the Early group than in the Late group (p=0.002 and p=0.021, respectively). Also, lower cT and cN stage were observed in the Early group than in the Late group (p=0.013 and p=0.022, respectively). PID was 46.9 mm in the Early group and 56.5 mm in the Late group (p=0.001).

Surgical outcomes are summarized in Table II. Significantly less blood loss was observed in the Early group than in the Late group (p=0.001). There was a trend of less left mobilization and more qualified surgeon operating in the Early group than in the Late group, although the difference was not significant. Postoperative complications were similar between the two groups.

We further examined factors that affected the operation time. The optimal cut-off levels and area under the curve (AUC) of PID and TSF were determined by ROC curve and were 54.5 mm (AUC 0.696) and 14.1 mm (AUC 0.549), respectively (Figure 3A and B). Univariate analyses showed that sex, cT, cN, and PID affected operation time. Multivariate analysis showed that PID was the only independent factor that affected operation time (p<0.001) (Table III). Several studies showed that technical proficiency level would affect the operation time (25,26). Therefore, we examined whether factors affecting the operation time differed between operator’s skill. Table IV and Table V show the results regarding the factors affecting the operation time for non-qualified surgeon and qualified surgeon, respectively. PID was the factor affecting the operation time in both non-qualified and qualified surgeon (p=0.032 and p=0.007, respectively).

We showed that PID was a favorable factor predicting operation time. Obesity is known to prolong the operation time, and BMI is often used to define obesity (27). However, abdominal shape is sexually dimorphic. Men accumulate more visceral fat whereas women accumulate more subcutaneous fat (28). Several studies showed that abundant subcutaneous fat is not associated with higher complications whereas abundant visceral fat is strongly associated with it (19,29,30). Also, Goto et al. showed that TSF did not reflect the operation time which was similar to our results. The results of these studies suggest that subcutaneous fat does not affect the difficulty of the operation. Therefore, BMI does not always reflect the difficulty and operation time.

There are several benefits of predicting the operation time using PID. First, it will help predict the difficulty of the operation (31). Surgical difficulty is known to relate with anastomotic leakage (32). Thus, it would be safer for difficult cases to be operated by skilled surgeons. Second, long operation times may cause surgeons to lose concentration, experience fatigue, and increase the number of intraoperative errors (33,34). Taking short breaks during surgery is known to preserve performance without prolonging the operation time (35,36). Therefore, surgeons can prevent excessive fatigue by taking breaks whenever the operation is thought to be long. Third, no special instruments are needed to measure the distance. Generally, CT is taken before the operation to determine the stage of the tumor, whether operation is appropriate, and to check the running pattern of the blood vessel. PID can be measured by using this CT, while special software is needed to assess VFA (16,17). Last, PID can be applied by all surgeons despite the skill. We showed that PID was a factor affecting the operation time in both non-qualified and qualified surgeons.

In this study, qualified surgeons had a trend of shorter operation time than non-qualified surgeons (205 min vs. 226 min, p=0.083) and there was no difference in patient characteristics between qualified and non-qualified surgeon (data not shown). However, operation by qualified surgeon was not a factor affecting the operation time among all cases. This might be because a qualified surgeon always attends laparoscopic colectomy at our hospital. Several studies showed that novice surgeons can maintain surgical quality under supervision by senior surgeons. Among these studies, Langhoff et al. reported that the operation time was similar when operated by either senior or novice surgeons (37). Also, Ichikawa et al. showed that non-qualified surgeon’s operation time reached plateau at the 18th case of laparoscopic colectomy (38). We therefore believe that quality of surgery was maintained by the attendance of a qualified surgeon and this was the reason qualified surgeon was not a factor affecting the operation time among all cases.

There are several limitations for this study. This is a retrospective study at a single institution, so the sample size is small. In addition, we could not measure VFA, since we did not have the hardware to assess it. Therefore, we still do not know whether PID correlates with VFA. Further studies are necessary to clarify this point.

In conclusion, PID is a simple factor that can predict the operation time despite the skills of the surgeon. PID longer than 54.5 mm is a risk of prolonged operation time over 210 min.

All Authors have no conflicts of interest to declare in relation to this study.

All Authors performed surgery and perioperative management on the patients. Takafumi Saeki, Yasunori Otowa and Keitaro Kakinoki conceived the study. Takafumi Saeki, Yuta Yamzaki and Takashi Shimizu collected data. Takafumi Saeki, Keisuke Arai and Yasuhiko Mii performed the data analysis. Takafumi Saeki and Yasunori Otowa wrote the manuscript. Shigeteru Oka, Tetsu Nakamura and Daisuke Kuroda revised the manuscript. All Authors approved the final version of the article.