Predictive model of the surgical difficulty of robot-assisted total mesorectal excision for rectal cancer: a multicenter, retrospective study
Of all malignant tumors, colorectal cancer (CRC) is the second most deadly kind, and it is the third most frequent in the globe . Within some countries, the frequency of rectal cancer in people under 50 years old has significantly increased . Although some advancements have been achieved in the comprehensive therapy for CRC, surgery remains the most effective treatment for most rectal cancers. Total mesorectal excision (TME) can significantly reduce the incidence of postoperative local recurrence in rectal cancer patients, increasing the postoperative survival rate . For CRC surgery, priority has been increasingly given to least intrusive procedures, encompassing robotic and laparoscopic surgery [ – ]. With the development of laparoscopic TME technology, several randomized controlled studies have confirmed that it has a variety of short-term benefits . However, performing laparoscopic TME in patients with a “difficult pelvis”, which is characterized by a narrow and deep pelvis, patients with large tumors, patients with tumors located on the anterior wall, patients who have received neoadjuvant chemoradiation, remains challenging [ – ]. Research has confirmed that the probability of transition from laparoscopic surgery to open surgery is significantly greater in individuals with rectal cancer as opposed to those with colon cancer . Many investigations have demonstrated that colorectal surgery performed with a robot is safer and more feasible than traditional surgery . Compared with laparoscopic TME, robot-assisted TME (R-TME) may overcome the problem of a “difficult pelvis” to a certain extent . However, there is still a lack of relevant research on estimating the R-TME surgical difficulties. This study’s objective was to assess the impact of clinical, anatomic, and tumor parameters on the difficulty of R-TME surgery and to develop a forecasting algorithm to assist medical professionals in selecting the best surgical strategy. This study may also help surgeons to select suitable patients for R-TME. 

Patient selection Within 10 cm of the anal border, patients with middle and low rectal cancer who underwent R-TME surgery at three high-volume colorectal surgery centers (Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University; Department of General Surgery, Beijing Friendship Hospital; Department of General Surgery, Affiliated Cancer Hospital of Zhengzhou University) between May 2021 and December 2022 were covered in this research. Each year, the quantity of patients with colorectal tumors who undergo surgery in each center exceeds 300. All the operations were performed by three surgeons, one at each center. The following were the inclusion criteria: (1) the anal verge was only 10 cm away from the tumour; (2) rectal adenocarcinoma was confirmed by preoperative pathologic examination; (3) complete magnetic resonance imaging (MRI) data were available before surgery; (4) the depth of tumor invasion was T 1−3 ; (5) the circumferential resection margin was assessed as negative via MRI; and (6) R0 resection could be achieved by MRI evaluation. Patients with a history of pelvic fractures; pelvic surgery; abdominoperineal resection; multivisceral resection; and Hartmann’s or Miles’ operation were excluded. All patients completed informed consent paperwork before having surgery. All the procedures were carried out by professionals with over 15 years of expertise in colorectal surgery and who had given more performances than 200 R-TME surgeries for rectal cancer patients. Data collection and analysis were authorized by the Ethics Committee of the First Affiliated Hospital of Zhengzhou University. Pelvic dimensions on MRI Anatomic characteristics were collected by a dedicated surgeon under the guidance of a radiologist. In line with previous research, we selected 13 pelvic measurements that are anticipated to have an impact on TME surgery’s difficulties (Table ; Figs , , ), such as the pelvic inlet diameter, pelvic outlet diameter, pubic tubercle height, sacral height, sacral depth, interspinous distance, intertuberosity distance, mesorectal thickness in the anterior region, posterior region in the posterior region, anterior–posterior mesorectal span, lateral mesorectal span, rectal area and mesorectal package area [ , , ]. Surgical procedure The detailed surgical steps can be found in our previously published study . In brief, a medial approach was utilized to establish the correct level of freeing, and submesenteric vessels were ligated with clips. To achieve tension-free intestinal anastomosis, the flexure of the spleen was selectively freed, and the left colonic artery was not preserved. The surgeon performed fine dissection of the presacral hiatus via monopolar electric scissors or ultrasonic knives while maintaining an appropriate zone of splits in between the intrinsic rectal fascia and the presacral fascia. Once the rectum was completely free, the bowel lumen distal to the tumor was clamped after ensuring adequate distal margins of dissection via rectal palpation or colonoscopy. An endoscopic linear-cutting anastomosis equipment was employed to transected the rectum. The surgical specimen was then removed through a 4–6-cm cut within the left side or right lower quadrant or periumbilical region, based on the preferences of every surgeon, and a wound-protection sleeve was placed. Intestinal anastomosis was performed via a double stapling technique. A protective ileal collateral stoma developed based on the surgeon’s judgment, and following the conclusion of surgical adjuvant treatment, bowel continuity was restored. Statistical analysis For comparisons between two groups with normally distributed variables, the independent Student’s t test was applied. The Mann–Whitney U test was used for analyzing categorical and non-normally distributed variables. Univariate and multivariate logistic regression analyses were performed to identify preoperative factors associated with surgical complexity. Variables with p value under 0.05 were entered into a multivariate logistic regression model using backward stepwise selection. A p value of less than 0.05 was considered statistically significant. The prediction model was then developed based on independent risk factors using the R software program. 

Within 10 cm of the anal border, patients with middle and low rectal cancer who underwent R-TME surgery at three high-volume colorectal surgery centers (Department of Colorectal Surgery, The First Affiliated Hospital of Zhengzhou University; Department of General Surgery, Beijing Friendship Hospital; Department of General Surgery, Affiliated Cancer Hospital of Zhengzhou University) between May 2021 and December 2022 were covered in this research. Each year, the quantity of patients with colorectal tumors who undergo surgery in each center exceeds 300. All the operations were performed by three surgeons, one at each center. The following were the inclusion criteria: (1) the anal verge was only 10 cm away from the tumour; (2) rectal adenocarcinoma was confirmed by preoperative pathologic examination; (3) complete magnetic resonance imaging (MRI) data were available before surgery; (4) the depth of tumor invasion was T 1−3 ; (5) the circumferential resection margin was assessed as negative via MRI; and (6) R0 resection could be achieved by MRI evaluation. Patients with a history of pelvic fractures; pelvic surgery; abdominoperineal resection; multivisceral resection; and Hartmann’s or Miles’ operation were excluded. All patients completed informed consent paperwork before having surgery. All the procedures were carried out by professionals with over 15 years of expertise in colorectal surgery and who had given more performances than 200 R-TME surgeries for rectal cancer patients. Data collection and analysis were authorized by the Ethics Committee of the First Affiliated Hospital of Zhengzhou University. 

Anatomic characteristics were collected by a dedicated surgeon under the guidance of a radiologist. In line with previous research, we selected 13 pelvic measurements that are anticipated to have an impact on TME surgery’s difficulties (Table ; Figs , , ), such as the pelvic inlet diameter, pelvic outlet diameter, pubic tubercle height, sacral height, sacral depth, interspinous distance, intertuberosity distance, mesorectal thickness in the anterior region, posterior region in the posterior region, anterior–posterior mesorectal span, lateral mesorectal span, rectal area and mesorectal package area [ , , ]. 

The detailed surgical steps can be found in our previously published study . In brief, a medial approach was utilized to establish the correct level of freeing, and submesenteric vessels were ligated with clips. To achieve tension-free intestinal anastomosis, the flexure of the spleen was selectively freed, and the left colonic artery was not preserved. The surgeon performed fine dissection of the presacral hiatus via monopolar electric scissors or ultrasonic knives while maintaining an appropriate zone of splits in between the intrinsic rectal fascia and the presacral fascia. Once the rectum was completely free, the bowel lumen distal to the tumor was clamped after ensuring adequate distal margins of dissection via rectal palpation or colonoscopy. An endoscopic linear-cutting anastomosis equipment was employed to transected the rectum. The surgical specimen was then removed through a 4–6-cm cut within the left side or right lower quadrant or periumbilical region, based on the preferences of every surgeon, and a wound-protection sleeve was placed. Intestinal anastomosis was performed via a double stapling technique. A protective ileal collateral stoma developed based on the surgeon’s judgment, and following the conclusion of surgical adjuvant treatment, bowel continuity was restored. 

For comparisons between two groups with normally distributed variables, the independent Student’s t test was applied. The Mann–Whitney U test was used for analyzing categorical and non-normally distributed variables. Univariate and multivariate logistic regression analyses were performed to identify preoperative factors associated with surgical complexity. Variables with p value under 0.05 were entered into a multivariate logistic regression model using backward stepwise selection. A p value of less than 0.05 was considered statistically significant. The prediction model was then developed based on independent risk factors using the R software program. 

Patient characteristics Based on the inclusion and exclusion criteria, a total of 166 patients—104 men (62.7%) and 62 women (37.3%)—were qualified for the analysis. 61.5 years was the median age, while 23.9 kg/m 2 was the median BMI; the median distance of the tumors from the anal verge was 6.3 cm; the median tumor length diameter was 4.5 cm; 19 patients received preoperative adjuvant radiotherapy; and 27 patients received preoperative adjuvant chemotherapy. Patients were split into two groups randomly: a test group (48 patients) and a training group (118 patients). There was no significant different between the training and validation group ( p > 0.05) (Table ). Pelvic dimensions We contrasted the male and female groups’ pelvic metrics (Table ), and the differences in the pelvic inlet diameter, pubic tubercle height, sacral height, interspinous distance, intertuberosity distance, posterior mesorectal thickness, anterior–posterior mesorectal span, lateral mesorectal span, and mesorectal package area among the groups were substantial ( p < 0.05). Other parameters, such as the pelvic outlet diameter, sacral depth, anterior mesorectal thickness, and rectal area, showed no discernible difference among both of the groups. Predictors of surgical difficulty Within this research, the median operation time was 207.5 min. The medical patients were split up into a difficult surgery group (operation time ≥ 207.5 min, 83 patients in total) and a nondifficult surgery group (operation time < 207.5 min, 83 patients in total) according to the median operation time, and the two groups were compared via binary logistic regression. The results revealed that several parameters, including age, BMI, preoperative radiotherapy status, preoperative chemotherapy status, the gap of the tumor from the anal edge, the interspinous distance, the anterior–posterior mesorectal span and the posterior mesorectal thickness, were significantly correlated with the difficulty of R-TME surgery according to univariate analysis ( p < 0.05). Binary logistic regression was utilized for the multivariate analysis process (backward: LR), and the results revealed that BMI, the gap of the tumor from the anal edge, and the posterior mesorectal thickness (all p < 0.05) were separate indicators of the duration of operation (Table ). Establishment of a predictive nomogram We developed a prediction model based on these independent risk indicators to evaluate the likelihood that patients with rectal cancer may experience challenging surgery (Fig. ). The overall performance of the nomogram was assessed, with a C-index of 0.795 (95% CI: 0.717–0.874) among the trainees and 0.833 (95% CI: 0.716–0.950) in the validation group, indicating the adequate discriminative ability of the predictive model (Fig. ). 

Based on the inclusion and exclusion criteria, a total of 166 patients—104 men (62.7%) and 62 women (37.3%)—were qualified for the analysis. 61.5 years was the median age, while 23.9 kg/m 2 was the median BMI; the median distance of the tumors from the anal verge was 6.3 cm; the median tumor length diameter was 4.5 cm; 19 patients received preoperative adjuvant radiotherapy; and 27 patients received preoperative adjuvant chemotherapy. Patients were split into two groups randomly: a test group (48 patients) and a training group (118 patients). There was no significant different between the training and validation group ( p > 0.05) (Table ). 

We contrasted the male and female groups’ pelvic metrics (Table ), and the differences in the pelvic inlet diameter, pubic tubercle height, sacral height, interspinous distance, intertuberosity distance, posterior mesorectal thickness, anterior–posterior mesorectal span, lateral mesorectal span, and mesorectal package area among the groups were substantial ( p < 0.05). Other parameters, such as the pelvic outlet diameter, sacral depth, anterior mesorectal thickness, and rectal area, showed no discernible difference among both of the groups. 

Within this research, the median operation time was 207.5 min. The medical patients were split up into a difficult surgery group (operation time ≥ 207.5 min, 83 patients in total) and a nondifficult surgery group (operation time < 207.5 min, 83 patients in total) according to the median operation time, and the two groups were compared via binary logistic regression. The results revealed that several parameters, including age, BMI, preoperative radiotherapy status, preoperative chemotherapy status, the gap of the tumor from the anal edge, the interspinous distance, the anterior–posterior mesorectal span and the posterior mesorectal thickness, were significantly correlated with the difficulty of R-TME surgery according to univariate analysis ( p < 0.05). Binary logistic regression was utilized for the multivariate analysis process (backward: LR), and the results revealed that BMI, the gap of the tumor from the anal edge, and the posterior mesorectal thickness (all p < 0.05) were separate indicators of the duration of operation (Table ). 

We developed a prediction model based on these independent risk indicators to evaluate the likelihood that patients with rectal cancer may experience challenging surgery (Fig. ). The overall performance of the nomogram was assessed, with a C-index of 0.795 (95% CI: 0.717–0.874) among the trainees and 0.833 (95% CI: 0.716–0.950) in the validation group, indicating the adequate discriminative ability of the predictive model (Fig. ). 

In recent years, TME has been widely applied as a common technique used to treat rectal cancer surgically. However, TME is still challenging to perform for individuals with middle and low rectal cancer who have a “difficult pelvis”. A difficult pelvis often leads to increased surgical difficulty, and its most direct manifestation is the prolongation of the operation time. Previous studies have shown that factors affecting surgical difficulty include BMI, sex, the gap between the anal verge and the tumour, and several MRI-based pelvimetry parameters [ , , – ]. Compared with traditional laparotomy and laparoscopic surgery, the surgical robot platform has a better ergonomic design, more stable 3D views, a more flexible “wrist” structure, and greater superiority in terms of visual field exposure and is especially suitable for surgical operations in narrow spaces . Therefore, robot-assisted surgery should have certain advantages in handling cases of middle and low rectal cancer under the condition of a “difficult pelvis” . The ROLARR and REAL trials confirmed that with the development of R-TME technology, this method has certain advantages over laparoscopic TME, and R-TME might be the development direction for the purpose of surgically treating rectal cancer . Nevertheless, there is still a lack of relevant research on what factors affect the difficulty of R-TME surgery and how to evaluate the risk of difficult R-TME surgery before the procedure is performed. In this study, we demonstrated that many pelvic parameters, such as the pelvic inlet diameter, pubic tubercle height, sacral height, interspinous distance, intertuberosity distance, front-to-back mesorectal span, posterior mesorectal thickness and mesorectal package area, differ between men and women with middle and low rectal cancer. This result is consistent with the anatomic differences between the male and female pelvises. According to the results of this study, however, sex is not a predictor of surgical difficulty, this may be due to several unique anatomical factors, such as the different volumes of uterus and prostate. This study confirmed that BMI is one of the factors affecting surgical difficulty. It has been established that obesity is linked to higher mesorectal fat area (MFA) and visceral fat volume . A larger margin of error (MOE) is linked to longer operating times and higher intraoperative blood loss in open, laparoscopic and robotic-assisted rectal cancer surgery . Previous studies have shown that a high BMI tends to increase the degree of surgical difficulty [ , , ]. We believe that patients with higher BMI tend to have thicker mesenteric and visceral fat, which have a certain impact on the exposure of the operative field and make it difficult to expose blood vessels and lymph nodes. In addition, this fat also restricts the pelvic operative space, which prolongs the operation time and ultimately leads to increased surgical difficulty. In addition, this study confirmed that the gap of the tumor from the anal verge is related to surgical difficulty, which is in line with the findings of earlier research . The lower the tumor is located; the distal rectum mesentery is thinner. When patients have “difficult pelvis”, excision of the distal rectal mesentery is more challenging for surgeons. The results also revealed that the posterior mesorectal thickness is one of the risk factors of surgical difficulties, which agrees with the results of earlier research . Retrorectal mesenteric thickness is defined as the maximum vertical distance between the muscularis propria behind the rectum and the very rear of the mesorectal fascia. McKechnie et al. reported that the operation time increased by 2 min and 6 s for every 1-mm increase in posterior rectal mesentery thickness while treating stage I–III rectal adenocarcinoma with low anterior rectal resection or transanal total mesorectal excision (TaTME) . On the basis of the operative experience of the surgeons, we believe that a large mesorectal thickness is not conducive to finding the best surgical plane during surgery and may lead to additional bleeding and nerve damage, ultimately prolonging the operation time. At present, the anorectal angle, interspinous distance, intertuberosity distance and mesorectal package area have been confirmed to be related addressing the challenges associated with R-TME surgery for rectal cancer . Furthermore, studies based on evaluations via a laparoscopic approach have revealed that the obstetric junction diameter, pelvic entrance diameter, pelvic outlet diameter, interstitial interspinous distance, interstitial intertubercular diameter, mesorectal area, sacral length, sacral angle, sacrococcygeal curvature and pelvic angle are elements influencing the level of surgical difficulty [ , , – ]. The variables influencing the complexity of robot-assisted surgery are less than those influencing laparoscopic surgery. This difference might be brought on by some of the robotic surgical system’s benefits for surgical operations in the narrow pelvic space, thus reducing the impact of the contracted pelvis on surgical difficulty. We developed a prediction model for the probability of challenging R-TME surgery in patients with middle and low rectal cancer based on the multivariate study results. The model’s strong predictive capacity was demonstrated by the validation findings. Before performing R-TME surgery, surgeons may use this model to objectively quantify preoperative risk in patients with middle and low rectal cancer. The following restrictions apply to this investigation. First, the research was done in the past, which inevitably suffers from selection bias. Second, although this was a multicenter study, the total sample size was limited. Thirdly, the judgment of the difficulty of R-TME surgery was mainly based on the personal experience of the surgeons, and there is a lack of recognized standards to define the difficulty of TME surgery. The standard to define the difficulty of R-TME surgery developed in this study needs to be refined in a more appropriate way. In theory, the time spent in the pelvis during surgery may reflect the difficulty more accurately than the overall operation time. In conclusion, the study’s findings should be regarded cautiously, and need to be confirmed by prospective multicenter studies with large sample sizes. Despite these limitations, our study demonstrated that BMI, the gap of the tumor from the anal edge, and the posterior mesorectal thickness were significant elements impacting the R-TME surgery’s difficulty. The assessment of preoperative MRI pelvimetric parameters and application of the predictive model may improve the accuracy in predicting the difficulty of R-TME surgery, thereby facilitating decision-making regarding surgical approach selection and preoperative planning by surgeons. 

This study revealed that BMI, the distance between the tumor and anal verge and the posterior mesorectal thickness are independent risk factors that affect the difficulty of R-TME surgery for the treatment of middle and low rectal cancer. The clinical predictive model established in this study has good predictive ability for the difficulty of R-TME surgery and could be helpful in making clinical decisions before surgery. 

