Mesorectal fat area-based nomogram for predicting the difficulty of minimal invasive surgery in mid to low rectal cancer

doi:10.21203/rs.3.rs-4939757/v1

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Research Article

Mesorectal fat area-based nomogram for predicting the difficulty of minimal invasive surgery in mid to low rectal cancer

https://doi.org/10.21203/rs.3.rs-4939757/v1

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Purpose: This study aims to develop a mesorectal fat area-based nomogram, covering preoperative baseline characteristics and other pelvic MRI data, to predict the difficulty of robotic or laparoscopic-assisted total mesorectal excision (TME)in patients with mid to low rectal cancer.

Method: 378 patients were retrieved in our hospital and divided into non-difficult and difficult groups based on five criteria. Factors independently associated with the difficulty were identified by univariate and multivariate logistic regression analysis and then were used to develop a nomogram model to visualize the risk of surgical difficulty.

Result: Tumor distance from anal verge, intertuberous distance, pelvic depth, anorectal angle and mesorectal fat area independently predicted difficulty level. A nomogram model which combines these predictors including mesorectal fat area was developed and constructed. An area under the ROC curve (AUC) of 0.8668 was obtained for the training data set and 0.9134 for the internal validation one. Discrepancy in surgical approach (laparoscopic or robotic) was not the independent predictive factor of the surgical difficulty (P＞0.05).

Conclusions: The mesorectal fat area-based nomogram model is feasible for predicting the difficulty level of rectal surgery, combined other MRI-based pelvimetry parameters and clinical factors in mid-low RC cases.

Rectal cancer

mesorectal fat area

Nomogram

Minimal invasive

Surgical difficulty

Colorectal cancer ranks third in morbidity and second in mortality among malignant tumors. Rectal cancer incidences in China are much higher than those in developed countries and show a trend toward younger populations.[23, 27]. An efficient TME is a standard procedure for radical RC surgery, ensuring a decrease in local recurrence rates, and resulting in more favorable prognosis[12]. Even the surgeons with extensive experience in rectal cancer resection, nevertheless, could slip up and render poor-quality TME occasionally. Unsatisfied quality of rectal mesenteric resection has been reported to be found in 15%-50% of cases, especially in low and intermediate rectal cancers[19, 21, 33].

Compared to open surgery, laparoscopic and robotic assisted surgery are superior in less directly contact with the abdominal cavity, which leads to more minor damage to the plasma membrane of the abdominal organs, slighter systemic reaction to the operation, smaller stimulation to the immune function, and faster recovery of gastrointestinal function. Numerous studies believed that minimally invasive rectal surgery, such as laparoscopy, enables better visualization of the surgical field compared to open surgery, thus lead to a preferable quality of TME[9]. However, achieving tumor outcomes comparable to those achieved with open surgery remains challenging, especially for mid-low rectal cancers. Generally speaking, deeper pelvis in lower rectal cancers increases the difficulty of dissection during surgery, which may jeopardize the quality[1, 15, 34]. In this context, the quality of minimally invasive surgery for rectal cancer is highly dependent on the skill of the surgeon as well as the patient's preoperative characteristics, such as challenging anatomical pelvic conditions, and other underlying clinical factors.

Currently, there are relatively few articles on developing mesorectal fat area-based predictive models in mid to low rectal cancer surgery. The existing predictive models incorporate limited number of variables and thus more clinical indicators need to be incorporated[3, 35]. In the 1990s, obstetricians were the first to propose the use of X-ray and CT images for pelvic radial measurements to predict the difficulty of the labor process in pregnant women. In recent years, pelvic measurements have also found wide application in the diagnosis and prediction of general surgical disorders. Preoperative rectal magnetic resonance imaging(MRI) is now accepted in the evaluation of patients with rectal cancer, for its advantages in determining tumor depth, vascular invasion, lymph node metastasis, and circumferential resection margin (CRM) involvement[24, 25]. In addition, it allows the assessment of pelvic shape and localization of anatomical landmarks, making MRI an essential tool for developing optimal treatment strategies. However, the ability of MRI-based pelvic parameters to predict surgical difficulty for TME is still no fixed conclusion yet[18, 29], with conflicting results between different studies. To compare these reported data is formidable because of the discrepancy in surgical technique and method of measurement. But it follows that utilizing pelvic parameter alone to predict surgical difficulty is an oversimplification.

Nomogram, a prediction model base on multivariate regression analysis, is superior in visualizing multiple predictors, compared with traditional logistic regression.The aim of this study was to evaluate the relationship between patient’s preoperative characteristics, including MRI pelvic measurements, and surgical difficulty.

Patients with mid to low rectal cancer who underwent laparoscopic or robotic assisted resection between a were selected from our database retrospectively.

Inclusion criteria:

1) radical laparoscopic or robotic assisted resection of mid to low RC, 2) distinguishable rectal MRI scan performed in our hospital within 14 days before surgery, 3)pathologically confirmed rectal adenocarcinoma, 4) single lesion within 10 cm from the anal margin revealed by postoperative pathology, 5) total mesorectal excision.

The exclusion criteria were:1) synchronous or double primary cancer, 2) distant metastasis, 3) low-quality MRI images, 4)Total pelvic exenteration (TPE) TPE or combined resection of adjacent organs.

378 patients were retrieved eventually (Fig. 1). The following patient characteristics were extracted from the database individually: age, gender, BMI, CEA, CA199, albumin, preoperative radio/chemotherapy, tumor size, pathological T/N stage, tumor distance from anal verge and postoperative long-term follow-up data .

The Radiological images were reviewed by a radiologist with no knowledge of the patient's clinical information. Six pelvic dimensions and mesorectal fat area were measured on the preoperative MRI (Fig. 2). The definitions of the surgical difficulty criteria were consistent with previous studies, with modifications (Table 1)[7]. Ultimately, 5 criteria were selected to assess the difficulty of the surgery, and weighted scores were assigned to each criterion. The overall score was 0–10, based on which the surgical difficulty levels were categorized into two classes.Below a score of 4 was classified as no surgical difficulty, whereas a score of at least 4 indicated surgical difficulty. Subsequently, long-term prognostic results of the two groups were used to validated the scoring criteria with the .

Table 1

Surgical difficulty grading
	Points
Duration of surgery > 300 min	3
Conversion to open procedure	3
Postoperative hospital stay > 15 days	2
Blood loss > 100 ml	1
Morbidity (grades II and III)	1
Total score ≥ 4 was Difficulty; <4 was Non-difficulty

Sharp dissection was performed in the presacral space under direct vision while the integrity of the dirty layer of the pelvic fascia was kept intact and unbroken, and the tumor was resected in the distal rectal mesentery not less than 5 cm. Whether or not diverting stoma creation and/or lateral lymph node dissection was required during the operation depended on the surgeon in charge. The procedure (laparoscopic or robotic) was determined by the surgeon prior to surgery. Conversion to open surgery was recommended when it is not possible to perform the entire procedure laparoscopically or robotically.

R software, IBM SPSS Statistics 25.0 and GraphPad Prism 9.0 were used for the statistical analysis and visualization. T-tests were used In the comparison of continuous variables, while classified variables were compared with χ2 tests. Propensity score matching(PSM) was applied to moderate the effects of bias and confounding variables (matching method was nearest neighbor matching). Variables potentially affecting surgical difficulty were analyzed with univariate and multivariate logistic regression analyses. Overall survival(OS) was evaluated with the Kaplan–Meier method and log rank test. Development and internal validation of a predictive nomogram was also conducted in this study. Then discriminatory power of this scoring system and the value of the model in terms of clinical decision making were assessed by receiver operating characteristic curves (ROC) and decision curve analysis (DCA) respectively.

265 were assigned to the training data set, while 113 patients were assigned to the internal validation data set. For training data set, 203 (76.6%) were categorized as non-difficult group and 62 (23.4%) as difficult group, compared to 86 (76.1%) in non-difficult group and 27 (23.9%) patients in difficult group among the internal validation data set. An overview of the patients' baseline data is shown in Table 2 and radiological results is shown in Table 3. Apart from the N-stage, there were no significant difference in baseline data between the training and internal validation data sets (all P > 0.05). To compare the differences in surgical difficulty between laparoscopic and robotic surgery, 378 patients were divided into laparoscopic group (control group N = 323) and robotic group (treatment group N = 52) respectively. Individuals from the control group with the same or similar propensity score values as those in the treatment group were matched, and total sample size after matching was 104 (control group N = 52, treatment group N = 52), and there was no considerable discrepancy between the baseline figures of two data set can be observed (all P > 0.05) (Table 7 and 8).

Table 2

Patient characteristics
		Training data set N = 265	Internal validation data set N = 113	P
Gender (%)	male	153 (57.7)	76 (67.3)	0.105
	female	112 (42.3)	37 (32.7)
Age(%)	≥ 55 years	182 (68.7)	79 (69.9)
	<55 years	83 (31.3)	34 (30.1)	0.908
BMI(%)	≥ 24 kg/m²	103 (38.9)	41 (36.3)
	<24 kg/m²	162 (61.1)	72 (63.7)	0.72
Preoperative chemotherapy(%)	yes	56 (21.1)	21 (18.6)
	no	209 (78.9)	92 (81.4)	0.672
Preoperative radiotherapy(%)	no	234 (88.3)	106 (93.8)
	yes	31 (11.7)	7 (6.2)	0.149
Preoperative albumin(%)	≥ 35 g/L	212 (80.0)	96 (85.0)
	<35 g/L	53 (20.0)	17 (15.0)	0.322
CEA(%)	≥ 5 ng/ml	63 (23.8)	28 (24.8)
	<5 ng/ml	202 (76.2)	85 (75.2)	0.938
CA199(%)	≥ 37 U/ml	17 (6.4)	10 (8.8)
	<37 U/ml	248 (93.6)	103 (91.2)	0.533
Tumor size(cm,mean ± SD)		3.25 (1.62)	3.28 (1.74)	0.877
T stage(%)	Tis	2 (0.8)	0	0.919
	T1	30 (11.3)	12 (10.6)
	T2	90 (34.0)	40 (35.4)
	T3	94 (35.5)	40 (35.4)
	T4	49 (18.5)	21 (18.6)
N stage(%)	N0	184 (69.4)	64 (56.6)	0.04
	N1	56 (21.1)	37 (32.7)
	N2	25 (9.4)	12 (10.6)
Tumor distance from anal verge(cm, mean ± SD)		3.60 (2.17)	3.62 (2.06)	0.926

Table 3

MRI parameters
	Training data set N = 265	Internal validation data set N = 113	P
Interspinous distance(cm, mean ± SD)	96.00 (11.25)	95.42 (10.71)	0.642
Intertuberous distance(cm, mean ± SD)	110.75 (12.43)	109.89 (13.19)	0.544
Pelvic inlet(cm, mean ± SD)	109.62 (11.24)	110.20 (11.89)	0.65
Pelvic outlet(cm, mean ± SD)	86.21 (14.90)	85.36 (12.91)	0.599
Pelvic depth(cm, mean ± SD)	115.75 (16.49)	117.63 (15.38)	0.301
Transverse diameter(cm, mean ± SD)	118.93 (8.55)	117.08 (8.91)	0.059
Anorectal angle(cm, mean ± SD)	121.16 (12.70)	123.61 (12.66)	0.086
Mesorectal fat area(cm², mean ± SD)	16.44 (5.49)	17.05 (5.98)	0.34

Table 4 demonstrates the significant increase in operative time, blood loss, postoperative hospitalization, and complication rates in the difficult group compared to the non-difficult group in the training group. And the 3-year postoperative overall survival rate of the latter group was significantly higher than that of the difficult group(Fig. 3).

Table 4

Intraoperative and postoperative outcome
		Training data set N = 265			Internal validation data set N = 113
		Surgical difficulty			Surgical difficulty
		Non-difficulty N = 203	Difficulty N = 62	P	Non-difficulty N = 86	Difficulty N = 27	P
Duration of surgery (min, mean ± SD)		256.76 (67.25)	390.06 (76.13)	< 0.001	265.15 (79.25)	399.70 (125.20)	< 0.001
Blood loss (mean (SD))		63.97 (82.43)	165.16 (199.86)	< 0.001	55.00 (49.32)	228.15 (191.47)	< 0.001
Postoperative hospitalization (days,mean ± SD)		8.60 (7.59)	13.03 (9.26)	< 0.001	8.72 (5.73)	9.48 (5.22)	0.54
Operation.way(%)	Laparo-scopic	175 (86.2)	51 (82.3)	0.573	76 (88.4)	24 (88.9)	1
	robotic	28 (13.8)	11 (17.7)		10 (11.6)	3 (11.1)
Conversion to open procedure(%)	yes	0 (0.0)	3 (4.8)	0.014	0 (0.0)	1 (3.7)	0.539
	no	203 (100.0)	59 (95.2)		86 (100.0)	26 (96.3)
Morbidity(%)	yes	17 (8.4)	18 (29.0)	< 0.001	12 (14.0)	5 (18.5)	0.787
	no	186 (91.6)	44 (71.0)		74 (86.0)	22 (81.5)

According to the result of univariate analysis(Table 5), preoperative radio/chemotherapy, tumor distance from anal verge, intertuberous distance, pelvic depth, anorectal angle, and mesorectal fat area were related to the difficulty of the procedure (P < 0.05). Finally, tumor distance from anal verge, intertuberous distance, pelvic depth, anorectal angle, and mesorectal fat area were indentified as independent factors in multivariate analysis, serving as valuable assets to predicting surgical difficulty level (all P < 0.05)(Table 5).

Table 5

Univariate and Multivariate logistic regression analyses of associations between factors and surgical difficulty
		Univariate analyses		Multivariate analyses
		OR (95% CI)	P	OR (95% CI)	P
Gender	male	Ref
	female	1.07 (0.60–1.90)	0.815
Age	no	Ref
	yes	0.71 (0.39–1.29)	0.264
BMI	<24 kg/m²	Ref
	≥ 24 kg/m²	0.91 (0.50–1.63)	0.744
ALB	<35 g/L	Ref
	≥ 35 g/L	0.82 (0.41–1.63)	0.562
CEA	<5 ng/ml	Ref
	≥ 5 ng/ml	0.54 (0.26–1.15)	0.11
CA199	<37 U/ml	Ref
	≥ 37 U/ml	0.69 (0.19–2.47)	0.565
Chemotherapy	no	Ref
	yes	3.04 (1.61–5.74)	< .001	0.98 (0.32–2.95)	0.967
Radiotherapy	no	Ref
	yes	4.36 (2.01–9.46)	< .001	2.21 (0.59–8.30)	0.24
Tumor size	cm, mean ± SD	0.85 (0.71–1.02)	0.086
T stage	T0	Ref
	T1	0.36 (0.02–6.53)	0.492
	T2	0.25 (0.01–4.19)	0.335
	T3	0.25 (0.02–4.24)	0.339
	T4	0.48 (0.03–8.26)	0.617
N stage	N0	Ref
	N1	1.06 (0.53–2.12)	0.868
	N2	0.61 (0.20–1.86)	0.382
Tumor distance from anal verge	cm, mean ± SD	0.82 (0.71–0.93)	0.003	0.75 (0.63–0.90)	0.002
Interspinous distance	cm, mean ± SD	0.98 (0.96–1.01)	0.159
Intertuberous distance	cm, mean ± SD	0.95 (0.93–0.98)	< .001	0.97 (0.94-1.00)	0.027
Pelvic inlet	cm, mean ± SD	0.98 (0.96–1.01)	0.217
Pelvic outlet	cm, mean ± SD	0.99 (0.97–1.01)	0.391
Pelvicdepth	cm, mean ± SD	1.03 (1.01–1.05)	0.002	1.03 (1.00-1.06)	0.026
Transverse diameter)	cm, mean ± SD	0.98 (0.95–1.02)	0.33
Anorectal angle	cm, mean ± SD	1.08 (1.05–1.11)	< .001	1.05 (1.02–1.08)	0.002
Mesorectal fat_area	cm², mean ± SD	1.21 (1.14–1.29)	< .001	1.20 (1.12–1.29)	< .001
Operation way	laporoscopic	Ref
	robot	1.35 (0.63–2.89)	0.444
OR, odds ratio, Ref, reference.

A visual nomogram was then created to predict the surgical difficulty of minimally invasive surgery of mid to low rectal cancer (Fig. 4). High agreement of the calibration curves with the fitted line reflected superior accuracy of the predictive model for both the training and validation datasets (Fig. 5). The c-index for prediction model was 0.8668 in training datasets and 0.9134 in internal validation datasets respectively, indicating a high level of credibility in the predictive ability of the models (Fig. 5).

The relationship between preoperative parameters and surgical difficulty in patients with mid-low RC who underwent minimally invasive surgery was demonstrated in current study. A significantly more optimistic prognosis occurred in the non-difficult group rather than in the difficult group (P = 0.006) (Fig. 3), indicating a strong correlation for the criteria selected in our study to assess surgical difficulty and long-term survival outcomes. Multivariate logistic regression analysis demonstrated that tumor distance from anal verge, intertuberous distance, pelvic depth, anorectal angle, and mesorectal fat area were significantly associated with surgical difficulty in RC patients, meeting partial agreement of previously published findings[3, 31, 32].

Consistent with the results of previous reports[3, 20], tumour distance from the anal verge was a key factor in determining the surgical approach in this study. When performing total mesorectal excision (TME), rectal transection and anastomosis, the closer the tumour is to the anal margin, the greater the likelihood of bleeding and the greater the extent of dissection and exposure required.[14, 18]. Besides, low rectal cancer has a higher risk of local recurrence than the middle one, consequently, surgical procedures for low rectal cancer vary between surgeons[6]. Surgery for very low rectal cancer frequently requires diverting stoma creation, and longer surgical time usually required for these procedures.

Results also indicated that shorter intertuberous distance and deeper pelvic depth had a profound correlation with high degree surgical difficulty, which is the same as some previous studies[30, 35]. Pelvic that is deeper vertically and narrower transversally has a higher probability of interfering with surgical visualization and manipulation than other pelvic types[16]. In our study, larger anorectal angle was also significantly associated with higher degree of surgical difficulty, though it is not clear why anorectal angle was greater in the high-grade group. Part of the reason for this association may be tonic activity of the puborectalis and/or external sphincter. It is potentially feasible to minimize the difficulty of surgery by reducing the anorectal angle.

Generally speaking, a high BMI represent overall obesity and confirmed a negative impact during the performance of TME procedure[3, 13], particularly in obese male subjects[28]. However, our study found a significant positive correlation between mesorectal fat area and surgical difficulty (P < 0.01), while BMI was not an influencing factor(P > 0.05). This phenomenon is explained by the fact that even individuals with the same BMI could have different amounts of visceral fat content in their abdominal cavity[13], in other words, fat around the rectum, has a major impact on the surgical procedure. Higher fat content of abdominal viscera will obscure anatomical planes or limit device access to the pelvis, leading to poor visual field exposure and increase likelihood of intraoperative bleeding[4]. Given the inconsistent relationship between BMI and abdominal visceral fat, mesenteric fat area may be a better predictor of surgical difficulty.

It is generally accepted that the pelvic bony anatomical trajectories of male patients are significantly shorter than those of females in terms of the interspinous and intertuberous distance, whereas measurements such as pelvic inlet and outlet distance and pelvic depth are still inconclusive. Due to the narrower and potentially shallower pelvis, pelvic operation may be easier to be performed in female patients compared to the male, and some researches had confirmed this point[1]. Controversially, our research did not find a significant effect of gender on the difficulty of surgery. It seems that the ease of surgery cannot be judged by gender alone. Because although the male pelvis is generally narrower and deeper than that of the female, the presence of the uterus and its appendages, which are unique to the latter, can also complicate the procedure, affecting the field of vision, increasing the risk of surgery and the duration time of the operation.

Although preoperative chemo/radiotherapy were associated with the difficulty of the surgery in univariate analysis(P < 0.01), they were no the significant predictors in multivariate analysis outcomes(P > 0.05). On the one hand, preoperative chemo/radiotherapy may provide numerous clinical and pathological benefits to rectal cancer patients, such as tumor regression, prevention of the spread of cancer cells during surgery, stage reduction, increased chances of anal preservation and decrease in mesorectal fat area, all of which are beneficial for non-difficulty surgery. On the other hand, it can lead to fibrosis of the surgical area[5], which increases the difficulty of separation during surgery, resulting in a longer operation time, increased risk of bleeding and damage of tissues, and may ultimately lead to incidence of difficult operations.

There is no significant association between tumor diameter and surgical difficulty in this research.The reason for this may be that tumor diameter is essentially not an independent variable in the comprehensive measurement, in other words, "large" tumors in "large" pelvises may not lead to an increase in the difficulty of mid-low RC resection, whereas relatively harder surgery may be reasonable in smaller tumors. Tumor staging was mainly closely related to the degree of differentiation, infiltration and metastasis, hence the relationship with the difficulty of RC resection still needs to be further demonstrated by the study of a larger sample. In addition, the results of this study showed that age, CEA level, T and N stage were not independent predictors of the difficulty of minimally invasive RC surgery.

Robotic surgery for rectal cancer was firstly reported in 2006. The technological advantages of robotic surgery render more precise dissection in confined spaces because of its better ergonomic[17, 22, 26]. According to the results of a randomized controlled trial, robotic surgery had significantly less blood loss, shorter postoperative hospitalization, and fewer postoperative complications compared with the laparoscopic one[8]. Similarly, a number of previous studies had also shown that there were significant outcomes between the two surgical procedures in terms of perioperative morbidity, recovery of bowel function, conversion rates to open and quality of tumor resection[2, 10, 11]. The results of univariate and multivariate regression analyses in our study demonstrated that the difference in surgical approach (laparoscopic or robotic) was not well significant in affecting the surgical difficulty. To further verify this finding ,we also applied propensity score matching (PSM) analysis, and chi-square test performed subsequently with surgical difficulty as the outcome variable while surgical approach as the independent variable. It showed that there was no significant difference in surgical difficulty between the laparoscopic and robotic groups (P > 0.05), which further validated our results. Although the randomized, controlled trial described earlier suggested that robotic assisted total mesorectal excision offers potential benefits over laparoscopic surgery, the cost of equipment and the longer learning curve required for surgeon training may result in increased expenses, and that may offset any possible earnings of faster postoperative recovery.

In addition, we constructed a nomogram for predicting the risk of surgical difficulty in mid-low rectal cancer patients based on the results of multivariate analysis. The c-index of the training dataset and the internal validation dataset were 0.8668 and 0.9114 respectively, indicating that the predictive ability of the model had a high degree of confidence. Objective preoperative risk assessment could be performed for patients undergoing minimally invasive surgery for rectal cancer with this model. Combined with the DCA curve (Fig. 6), we can make appropriate interventions, such as reduction of mesorectal fat area and minimization of anorectal angle.

However, there are still several limitations in our study. It is a retrospective single center study, the infuence of selection bias might be underestimated. Despite the fact that multivariate analysis and internal validation were applied, external validation study was still further needed o verify the feasibility of nomogram. In addition, this study included patients undergoing surgical procedures such as transabdominal perineal resection (APR), which may require longer surgical time, but whether these extra time should be associated with surgical difficulty remains to be debated.

In this study, we developed an nomogram using multidimensional parameters, specifically the mesorectal fat area, which proved to be effective in predicting the surgical difficulty of mid to low RC in both laparoscopic and robotic procedures.

Ethics approval

The study was approved by the Ethics Committee of FAH-SYSU in Guangzhou China and followed the Declaration of Helsinki. Data collection was authorized by the ethics board of the institution (Ethics Review [2022] No. 090).

Funding

This research was funded by the Guangdong Science and Technology Special Support Plan[No. KPT2020331]

Author Contribution

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by HF.Z and JB.T. The first draft of the manuscript was written mainly by HF.Z and JB.T prepared tables, authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgement

Thanks to Dr. Qian Fang for providing precious advice on the study design and data collection of this study.

Data Availability

The data used in this study are available from the corresponding author.

Competing Interests

All of the authors in this manuscript have read and approved the final version submitted, and there are no conflicts involved in this submission.

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Mesorectal fat area-based nomogram for predicting the difficulty of minimal invasive surgery in mid to low rectal cancer

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