Predictive model of the surgical difficulty of robot-assisted total mesorectal excision for rectal cancer: A multicenter, retrospective study

doi:10.21203/rs.3.rs-5008951/v1

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Research Article

Predictive model of the surgical difficulty of robot-assisted total mesorectal excision for rectal cancer: A multicenter, retrospective study

https://doi.org/10.21203/rs.3.rs-5008951/v1

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Background

Rectal cancer robotic surgery is becoming more and more common, but evidence for predicting surgical difficulty is scarce. Our goal was to look at the elements that influence the complexity of robot-assisted total mesorectal excision (R-TME) in the medical care of middle and low rectal cancer as well as to establish and validate a predictive model on the basis of these factors.

Methods

Within this multicenter retrospective investigation, 166 consecutive patients receiving R-TME between January 2021 and December 2022 with middle and low rectal cancer were included and categorized according to the median operation time. A nomogram was created to forecast the procedure's complexity after variables that could affect its difficulty were found using logistic regression analysis.

Results

Using R software, a total of 166 patients were randomly split into two groups: a test group (48 patients) and a training group (118 patients) at a ratio of 7 to 3. The median operation time of all patients was 207.5 min; patients whose operation time was ≥ 207.5 min were allocated to the difficult surgery group (83 patients), and patients whose operation time was < 207.5 min were allocated to the nondifficult surgery group. Multivariate analysis revealed that body mass index (BMI), the gap between the tumour and the anal verge and the posterior rectal mesenteric thickness were independent predictors of surgical duration. A clinical predictive model was created and assessed employing the above independent predictors. The results of the receiver operating characteristic (ROC) analysis revealed the adequate discriminative ability of the predictive model.

Conclusion

Our study revealed that it is feasible to predict surgical difficulty by obtaining clinical and magnetic resonance parameters for imaging (the gap between the anal verge and the tumour, and posterior mesorectal thickness), and these predictions could be useful in making clinical decisions.

rectal cancer

robot-assisted total mesorectal excision

pelvimetric parameters

difficulty of surgery

Of all malignant tumours, colorectal cancer (CRC) is the second most deadly kind, and it is the third most frequent in the globe [1]. Within some countries, the frequency of rectal cancer in people under 50 years old has significantly increased [2]. Although some advancements have been achieved in the comprehensive therapy for colorectal cancer, 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 [3, 4]. For CRC surgery, priority has been increasingly given to least intrusive procedures, encompassing robotic and laparoscopic surgery [5–7]. With the development of laparoscopic TME technology, several randomized controlled studies have confirmed that it has a variety of short-term benefits [5]. 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 [9–11]. 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 [12]. Many investigations have demonstrated that colorectal surgery performed with a robot is safer and more feasible than traditional surgery [13, 14]. Compared with laparoscopic TME, robot-assisted TME (R-TME) may overcome the problem of a "difficult pelvis" to a certain extent [15]. 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, anatomical, 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.

2.1 Patient selection

Within 10 centimeters 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 pathological 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 authorised by the Ethics Committee of the First Affiliated Hospital of Zhengzhou University.

2.2 Pelvic dimensions on MRI

Anatomical 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 1; Fig. 1–3), 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 [11, 16, 17].

Table 1

Pelvimetric parameters and definitions.
Pelvimetric parameters	Definitions
Pelvic inlet diameter	The distance between the sacral promontory and the superior middle aspect of the pubic symphysis
Pelvic outlet diameter	The length measured from the apex of the coccyx to the inferior edge of the pubic symphysis
Pubic tubercle height	Distance from the superior to the inferior middle aspect of the pubic symphysis
Sacral height	Distance from the sacral promontory to the tip of the coccyx
Sacral depth	Distance from the sacral length to the deepest point of the sacral hollow
Interspinous distance	The narrowest distance between the ischial spines
Inter-tuberosity distance	The shortest distance between the two ischial nodes
Lateral mesorectal span	The linear distance between the mesorectal fascia's most left and most right lateral aspects
Anterior-posterior mesorectal span	The linear distance between the mesorectal fascia's most anterior and most posterior aspects
Anterior mesorectal thickness	Maximum linear distance between the anterior facing muscularis propria of the rectum and the most anterior portion of the mesorectal fascia
Posterior mesorectal thickness	Maximal lateral separation between the posterior portion of the mesorectal fascia and the posterior facing muscularis propria of the rectum
Rectal area	Area confined by the muscularis propria of the rectum
Mesorectal package area	Area confined by the mesorectal fascia

2.3 Surgical procedure

The detailed surgical steps can be found in our previously published study [18]. 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 judgement, and following the conclusion of surgical adjuvant treatment, bowel continuity was restored.

2.4 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-values 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.

3.1 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/m2 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 2).

Table 2

Patient characteristics between training group and validation group.
Characteristic	Total (n = 166)	Training group (n = 118)	Validation group (n = 48)	P
Sex				0.980
male	104	74	30
female	62	44	18
Age [years] (SD)	61.9(10.3)	61.9(10.8)	61.8(9.3)	0.960
BMI [kg/m²] (SD)	24.0(2.8)	23.9(2.9)	24.2(2.6)	0.462
Preoperative radiotherapy				0.418
Yes	19	12	7
No	147	106	41
Preoperative chemotherapy				0.309
Yes	27	17	10
No	139	101	38
Distance from tumor to anal verge [cm] (SD)	6.4(2.1)	6.4(2.1)	6.5(2.0)	0.740
Tumor size [cm] (SD)	4.7(1.8)	4.6(1.7)	4.8(2.1)	0.677
Operative time [min] (SD)	220.2(63.5)	220.1(66.4)	218.6(56.6)	0.835
Pelvic inlet diameter [cm] (SD)	11.6(1.0)	11.6(1.1)	11.6(0.9)	0.948
Pelvic outlet diameter [cm] (SD)	8.2(0.8)	8.1(0.8)	8.2(0.8)	0.488
Pubic tubercle height [cm] (SD)	4.6(0.4)	4.6(0.4)	4.6(0.5)	0.688
Sacral height [cm] (SD)	12.7(1.3)	12.8(1.3)	12.5(1.1)	0.180
Sacral depth [cm] (SD)	3.9(0.5)	3.9(0.5)	4.0(0.6)	0.467
Interspinous distance [cm] (SD)	9.7(1.0)	9.7(1.0)	9.7(1.1)	0.857
Inter-tuberosity distance [cm] (SD)	12.2(1.2)	12.2(1.2)	12.2(1.3)	0.864
Lateral mesorectal span [cm] (SD)	7.6(0.9)	7.6(0.9)	7.7(0.9)	0.849
Anterior-posterior mesorectal span [cm] (SD)	5.5(1.0)	5.5(1.1)	5.5(0.9)	0.968
Anterior mesorectal thickness [cm] (SD)	1.0(0.4)	1.0(0.4)	1.0(0.4)	0.561
Posterior mesorectal thickness [cm] (SD)	1.5(0.5)	1.5(0.5)	1.5(0.5)	0.865
Rectal area [cm²] (SD)	8.3(4.1)	8.3(4.5)	8.1(2.8)	0.769
Mesorectal package area [cm²] (SD)	32.6(7.1)	32.9(7.1)	31.9(7.0)	0.426

3.2 Pelvic dimensions

We contrasted the male and female groups' pelvic metrics (Table 3), 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.

Table 3

Anatomical parameters between men and women.
Anatomical parameters	Total (n = 166)	Men (n = 104)	Women (n = 62)	P
Pelvic inlet diameter	11.6(1.0)	11.3(0.9)	12.1(1.0)	< 0.001
Pelvic outlet diameter	8.2(0.8)	8.1(0.8)	8.3(0.8)	0.181
Pubic tubercle height	4.6(0.4)	4.7(0.4)	4.3(0.4)	< 0.001
Sacral height	12.7(1.3)	13.0(1.3)	12.2(1.1)	< 0.001
Sacral depth	3.9(0.5)	3.9(0.5)	3.9(0.5)	0.882
Interspinous distance	9.7(1.0)	9.2(0.7)	10.5(0.8)	< 0.001
Inter-tuberosity distance	12.2(1.2)	11.6(1.0	13.2(1.0)	< 0.001
Lateral mesorectal span	7.6(0.9)	7.5(0.9)	7.9(0.9)	0.005
Anterior-posterior mesorectal span	5.5(1.0)	5.8(1.0)	4.9(1.0)	< 0.001
Anterior mesorectal thickness	1.0(0.4)	1.0(0.3)	1.0(0.4)	0.747
Posterior mesorectal thickness	1.5(0.5)	1.6(0.5)	1.4(0.4)	< 0.001
Rectal area	8.3(4.1)	8.5(3.7)	7.8(4.7)	0.286
Mesorectal package area	32.6(7.1)	34.1(7.4)	30.2(5.8)	0.001

3.3 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 tumour 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 utilised for the multivariate analysis process (backward: LR), and the results revealed that BMI, the gap of the tumour from the anal edge, and the posterior mesorectal thickness (all P < 0.05) were separate indicators of the duration of operation (Table 4).

Table 4

Univariable and multivariable logistic regression analysis to identify the preoperative risk factors of surgical difficulty in 118 patients of the training group who underwent R-TME for rectal cancer.
	Univariable		Multivariable
	OR(95%)	P	OR(95%)	P
SEX (male vs. female)	1.337(0.633–2.827)	0.447
Age (years)	0.963(0.929–0.998)	0.037	0.974(0.932–1.017)	0.234
BMI (kg/m²)	1.231(1.062–1.426)	0.006	1.221(1.031–1.445)	0.020
Preoperative radiotherapy	0.075(0.009–0.604)	0.015	0.112(0.006–2.134)	0.145
Preoperative chemotherapy	0.172(0.047–0.636)	0.008	0.792(0.095–6.585)	0.829
Distance from tumor to anal verge(cm)	0.701(0.578–0.851)	< 0.001	0.777(0.620–0.966)	0.023
Tumor size(cm)	1.052(0.850–1.300)	0.643
Pelvic inlet diameter(cm)	1.219(0.867–1.716)	0.255
Pelvic outlet diameter(cm)	0.906(0.584–1.404)	0.657
Pubic tubercle height(cm)	0.611(0.245–1.525)	0.291
Sacral height(cm)	1.157(0.877–1.526)	0.304
Sacral depth(cm)	1.029(0.516–2.052)	0.935
Interspinous distance(cm)	0.665(0.452–0.978)	0.038	0.685(0.398–1.118)	0.173
Inter-tuberosity distance(cm)	1.188(0.876–1.613)	0.267
Lateral mesorectal span(cm)	0.937(0.637–1.378)	0.741
Anterior-posterior mesorectal span(cm)	1.146(0.817–1.607)	0.430	0.634(0.355–1.132)	0.123
Anterior mesorectal thickness(cm)	0.590(0.210–1.659)	0.317
Posterior mesorectal thickness(cm)	6.940(2.584–18.637)	< 0.001	6.164(1.840-20.658)	0.003
Rectal area(cm²)	1.068(0.970–1.177)	0.182
Mesorectal package area(cm²)	1.030(0.978–1.085)	0.259

3.4 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. 4). 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. 5).

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 [9, 16, 20–23]. 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 [19, 34]. Therefore, robot-assisted surgery should have certain advantages in handling cases of middle and low rectal cancer under the condition of a "difficult pelvis" [23]. 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 [18, 19]. 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 anatomical 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 [25, 26]. A larger margin of error (MFA) is linked to longer operating times and higher intraoperative blood loss in open, laparoscopic and robotic-assisted rectal cancer surgery [11, 27]. Previous studies have shown that a high BMI tends to increase the degree of surgical difficulty [21, 27, 28]. 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 tumour from the anal verge is related to surgical difficulty, which is in line with the findings of earlier research [9, 20]. The lower the tumour 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 [16]. 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 seconds for every one-millimeter increase in posterior rectal mesentery thickness while treating stage I–III rectal adenocarcinoma with low anterior rectal resection or transanal total mesorectal excision (TaTME) [16]. 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 [11, 23]. 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 [20, 27, 29–31]. 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. Firstly, the research was done in the past, which inevitably suffers from selection bias. Secondly, 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 tumour 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.

Disclosures

Mingyu Han, Shihao Guo, Shuai Ma, Quanbo Zhou, Weitao Zhang, Jinbang Wang, Jing Zhuang, Hongwei Yao, Weitang Yuan and Yugui Lian have no conflicts of interest or financial ties to disclose.

Funding

The authors undertake not to have received funds, grants or other support from any institution or individual during the conduct of this study.

Competing Interests

The author undertakes that no relevant interests need to be disclosed.

Ethics approval

The study was carried out in strict accordance with the principles of the Declaration of Helsinki and was approved by the Ethics Committee of Zhengzhou University before the study began.

Consent to participate

All the participants included in this study signed informed consent.

Consent to publish

The authors undertake that participants have signed informed consent for the publication of the images in Figs. 1, 2 and 3.

Author Contribution

Mingyu Han, Shihao Guo, Jing Zhuang, Hongwei Yao, Weitang Yuan and Yugui Lian wrote the main manuscript text. Shuai Ma and Quanbo Zhou prepared figures 1-3. Weitao Zhang and Jinbang Wang prepared figures 4-5. All authors reviewed the manuscript.

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No competing interests reported.

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Reviewers agreed at journal
19 Sep, 2024
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14 Sep, 2024
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Predictive model of the surgical difficulty of robot-assisted total mesorectal excision for rectal cancer: A multicenter, retrospective study

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Abstract

Background

Methods

Results

Conclusion

Figures

1. Introduction

2. Materials and methods

2.1 Patient selection

2.2 Pelvic dimensions on MRI

2.3 Surgical procedure

2.4 Statistical analysis

3. Results

3.1 Patient characteristics

3.2 Pelvic dimensions

3.3 Predictors of surgical difficulty

3.4 Establishment of a predictive nomogram

4. Discussion

5. Conclusions

Declarations

Disclosures

Funding

Author Contribution

References

Additional Declarations

Supplementary Files

Status:

Version 1