Nomogram for Prediction of Prolonged Postoperative Ileus after Colorectal Resection

doi:10.21203/rs.3.rs-1740562/v1

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Nomogram for Prediction of Prolonged Postoperative Ileus after Colorectal Resection

https://doi.org/10.21203/rs.3.rs-1740562/v1

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Background: Prolonged postoperative ileus (PPOI) is a major complication in patients undergoing colorectal resection. The aim of this study was to analyze the risk factors contributing to PPOI, and to develop an effective nomogram to determine the risks of this population.

Methods: A total of 1,233 patients with colorectal cancer who underwent radical colorectal resection at Fujian Cancer Hospital from March 2016 to August 2021 were enrolled as a training cohort in this study. Univariate analysis and multivariate logistic regressions were performed to determine the correlation between PPOI and clinicopathological characteristics. A nomogram predicting the incidence of PPOI was constructed. The cohort of 151 patients from Fujian Provincial Hospital were enrolled as a validation cohort. Internal and external validations were used to evaluate the prediction ability by area under the receiver operating characteristic curve (AUC) and a calibration plot.

Results: In the training cohort, 125 patients (10.1%) had PPOI after colorectal resection. The independent predictive factors of PPOI were identified, and included gender, age, surgical approach, perioperative fluid overload and postoperative use of opioid analgesics. The AUC of nomogram were 0.788 (95% CI: 0.747-0.829) and 0.812(95% CI: 0.697-0.928) in the training and validation cohort, respectively. The two cohorts of calibration plots showed a good consistency between nomogram prediction and actual observation.

Conclusions: A highly accurate nomogram was developed and validated in this study, which can be used to provide individual prediction of PPOI in patients after colorectal resection, and this predictive power can potentially assist surgeons to make the optimal treatment decisions.

Colorectal resection

Prolonged postoperative ileus

Nomogram

Risk factor

Postoperative ileus (POI) refers to a temporary impairment of gastrointestinal transit due to nonmechanical causes following surgery. As POI occurs in almost all patients following intra-abdominal surgery, especially major abdominal surgery, it may be considered as a normal physiologic response [[i],[ii]]. Usually, it is resolved within 3 days, but may persist or reoccur, in which case it is termed prolonged postoperative ileus (PPOI)[[iii]]. The point at which POI becomes PPOI has not been clearly established. Manifestations of PPOI are characterized as a variable mixture of nausea and vomiting, intolerance of oral diet, abdominal distension and delayed passage of flatus and stool. PPOI is one of the most common complications after colorectal surgery, with an incidence of 3-32% [[iv],[v]]. The variability of reported incidences can be explained by absence of accurate classification criteria and heterogeneous definition of PPOI [[vi]]. PPOI could result in a range of significant consequences, including nutritional deficiencies and the need for parenteral nutrition, increased length of stay, a significant fiscal burden and a negative impact on quality of life which is higher than with other postoperative morbidities [[vii],[viii]].

The Enhanced Recovery after Surgery (ERAS) program is an effective and safe protocol, and has been widely implemented in colorectal cancer surgery [[ix]]. Early return of bowel function and prevention of PPOI are important items of clinical practice guidelines for ERAS in Elective Colorectal Surgery [[x]]. There is currently still a lack of effective treatment options for PPOI, and therefore, it is important to identify high-risk patients of PPOI, and allow early intervention with preventive strategies [[xi]].

Nomogram is a popular and simple tool used to predict the probability of an individual's particular outcome, and has been frequently implemented in clinical practice [[xii],[xiii]]. The aim of this study was to develop an effective nomogram for prediction of the occurrence of PPOI after colorectal resection.

Patients

A total of 1,233 patients hospitalized with colorectal cancer at Fujian Cancer Hospital from March 2016 to August 2021 were enrolled as a training cohort in this study. The inclusion criteria were as follows: (1) Pathologic diagnosis of adenocarcinoma of the colorectum; (2) Elective radical operation; (3) age ≥18 years. The exclusion criteria were as follows: (1) Preoperative intestinal obstruction; (2) Unassessable on account of dementia or postoperative delirium; (3) Some complications considered to be the cause of PPOI, including postoperative anastomotic leakage, intraabdominal abscess and peritonitis; (4) Conversion to an open approach.

151 patients hospitalized at Fujian Provincial Hospital from June 2018 to September 2020 were enrolled as a validation cohort. The inclusion and exclusion criteria were the same as those for training cohort. The entire flowchart of the selection of patients was depicted in Fig. 1.

Enhanced recovery program

The ERAS program has been applied in the department of Gastrointestinal Surgery Oncology since November 2014, and has achieved remarkable results. Briefly, our ERAS protocol contains the following: (1) Preoperative period: Preadmission patient education and instruction; Nutritional evaluation and optimization; No routine use of mechanical bowel preparation；carbohydrate loading beverage 12 h and 2 h prior to general anesthesia. (2) Intraoperation period: Minimally invasive surgery is preferred; Intraoperative fluid restriction and avoidance of hypothermia; Nasogastric tubes and drains should be avoided when possible. (3) Postoperative period: Multimodal analgesia; Antiemetic prophylaxis; Early feeding and mobilization.

Definition

PPOI was defined in accordance with the systematic review and global survey by Vather et al. [[i]]. Specifically, PPOI was diagnosed if patients met ≥2 of the following five criteria on POD 4 (postoperative day 4) or later: (1) Nausea or vomiting over the preceding 12 hours; (2) Inability to tolerate an oral diet over the prior 24 h; (3) Absence of flatus over the preceding 24 h; (4) Abdominal distention; (5) Radiologic confirmation.

Total intravenous (IV) volume administration on the day of surgery was used to calculate IV fluids at POD 0. Perioperative fluid overload was defined as POD 0 IV fluids of ＞3L and/or POD 2 weight gain of ＞2.5kg. These cutoffs were independent risk factors for postoperative ileus, and have been identified as critical thresholds for complications in colorectal surgery [[ii], [iii]].

Statistical analysis

Continuous variables with normal distributions are presented as the mean ± SD, and were compared using Student’s t test; Continuous variables with non-normally distributed variables were expressed as medians and interquartile ranges (IQR), and were assessed with Mann-Whitney U tests. Categorical variables were shown as numbers and percentages. Univariate analysis was performed with a Chi-square test to compare categorical variables. Parameters with significance (p<0.05 in univariate analysis) were selected into multiple logistic regression analysis. R software (version 4.1.1) was used to construct a nomogram based on multiple analysis. The nomogram was evaluated internally for the training cohort and externally for the validation cohort. Internal and external validations were adopted to assess regarding prediction ability by area under the receiver operating characteristic (ROC) curve (AUC) and calibration plot. The Hosmer-Lemeshow test was used to assess the goodness-of-fit of the model. Statistical analyses were performed through SPSS 26.0 software. A two-tailed P value <0.05 was considered statistically significant.

Patient characteristics and outcomes

125 patients (10.1%) and 14 patients (9.3%) in the training and validation cohort, respectively had PPOI after colorectal resection. No statistically significant differences in the baseline demographic and the clinicopathological characteristics of the patients were found between the two cohorts (P > 0.05), with the exception of hypertension (P = 0.027, Table 1).

Table 1. Characteristics of patients in the training and validation cohort

	Training cohort (n=1233)	validation cohort (n=151)	P value
Gender			0.344
Male	847	98
Female	386	53
Age (years)			0.362
≤65	613	81
＞65	620	70
BMI(kg/m²)			0.241
≤24	591	80
＞24	642	71
Smoking habit			0.340
Yes	307	43
No	926	108
Alcohol use			0.674
Yes	525	67
No	708	84
Diabetes Mellitus			0.712
Yes	286	33
No	947	118
Hypertension			0.027
Yes	350	56
No	883	95
Hyperlipidemia			0.511
Yes	400	53
No	833	98
Respiratory comorbidity			0.232
Yes	243	36
No	990	115
Cardiac comorbidity			0.486
Yes	240	33
No	993	118
Peripheral vascular disease			0.713
Yes	190	25
No	1043	126
Previous abdominal surgery			0.387
Yes	172	25
No	1061	126
Preoperative anemia			0.817
Yes	413	52
No	820	99
Preoperative hypoalbuminemia			0.286
Yes	195	29
No	1038	122
Preoperative WBC count, mean±SD, *10³/μL	6.8±1.7	6.9±1.6	0.332
Neoadjuvant treatment			0.456
Yes	238	33
No	995	118
ASA-classification			0.328
ASA I	763	84
ASA II	333	47
ASA III	137	20
Surgical approach			0.512
Minimally invasive surgery	1097	137
Open surgery	136	14
Surgical procedure			0.180
Right colectomy	323	33
Transverse colectomy	78	16
Left colectomy	325	37
Rectal resectiona	507	65
Diverting ileostomy			0.447
Yes	175	18
No	1058	133
Operation duration(min)			0.559
≤180	557	72
＞180	676	79
Intraoperative Blood loss (mL), median (IQR)	180(90-200)	160(80-200)	0.172
Bowel resection length (cm), median (IQR)	20(18-21)	20(17,22)	0.112
Anastomosis technique			0.797
Side-to-end	314	37
End-to-end	919	114
Perioperative fluid overload			0.352
Yes	694	91
No	539	60
Perioperative transfusion			0.502
Yes	110	11
No	1123	140
Postoperative opioid analgesic			0.670
Yes	322	37
No	911	114
Differentiation			0.350
Well	64	4
Moderate	1034	132
Poor	135	15
TNM stage			0.512
I	208	31
II	627	75
III	398	45

Univariate and multivariate analysis of PPOI in the training cohort

Clinical characteristics, including gender, age, surgical approach, operation duration, perioperative fluid overload, postoperative opioid analgesic were significantly associated with PPOI after univariate analysis (p<0.05, Table 2). Multivariate analysis showed that gender, age, surgical approach, perioperative fluid overload, postoperative opioid analgesic were independent predictive factors of PPOI (p<0.05, Table 2).

Table 2. Univariable analysis and multivariable logistic regression of clinicopathological variables associated with PPOI

	PPOI, No.		P value	Multivariate Analysis
	Absence (n =125)	Presence (n = 1108)	P value	OR(95% CI)	P value
Gender			0.004	1.826(1.150-2.899)	0.011
Male	100	747
Female	25	361
Age(years)			0.001	1.781(1.206-2.630)	0.004
≤65	45	568
＞65	80	540
BMI(kg/m²)			0.092
≤24	51	540
＞24	74	568
Smoking habit			0.200
Yes	37	270
No	88	838
Alcohol use			0.362
Yes	58	467
No	67	641
Diabetes Mellitus			0.117
Yes	36	250
No	89	858
Hypertension			0.344
Yes	40	310
No	85	798
Hyperlipidemia			0.487
Yes	44	356
No	81	752
Respiratory comorbidity			0.425
Yes	28	215
No	97	893
Cardiac comorbidity			0.266
Yes	29	211
No	96	897
Peripheral vascular disease			0.329
Yes	23	167
No	102	941
Previous abdominal surgery			0.130
Yes	23	149
No	102	959
Preoperative anemia			0.220
Yes	48	365
No	77	743
Preoperative hypoalbuminemia			0.274
Yes	24	171
No	101	937
Preoperative WBC count, mean±SD,*10³/μL	7.0±1.5	6.8±1.7	0.269
Neoadjuvant treatment			0.160
Yes	30	208
No	95	900
ASA-classification			0.261
ASA I	69	694
ASA II	39	294
ASA III	17	120
Surgical approach			0.000	2.575(1.600-4.143)	0.000
Minimally invasive surgery	97	1000
Open	28	108
Surgical procedure			0.129
Right colectomy	36	287
Transverse colectomy	8	70
Left colectomy	22	303
Rectal resectiona	59	448
Diverting ileostomy			0.378
Yes	21	154
No	104	954
Operation duration(min)			0.047	0.680(0.459-1.005)	0.053
≤180	46	511
＞180	79	597
Intraoperative Blood loss (mL), median (IQR)	200(100,250)	180(90,230)	0.063
Bowel resection length (cm), median (IQR)	20(18,22)	19(17,21)	0.366
Anastomosis technique			0.406
Side-to-end	28	286
End-to-end	97	822
Perioperative fluid overload			0.011	1.618(1.108-2.362)	0.013
Yes	57	637
No	68	471
Perioperative transfusion			0.346
Yes	14	96
No	111	1012
Postoperative opioid analgesic			0.008	1.636(1.098-2.436)	0.015
Yes	45	277
No	80	831
Differentiation			0.865
Well	7	57
Moderate	106	928
Poor	12	123
TNM stage			0.435
I	16	192
II	66	561
III	43	355

Construction of a nomogram for prediction of PPOI

The five variables that were finally determined to be significant in the multivariate logistic regression analysis were used to establish the intuitive nomogram model (Fig. 2). A total score is calculated by summing the scores for each variable, and the final predicted risk of PPOI is the corresponding probability of the total points of individual patients.

Validation of the nomogram

Internal validation was first performed in the training cohort. The AUC of the training cohort was 0.788 (95% CI: 0.747-0.829) (Fig. 3). A bootstrap resampling procedure was applied and a calibration curve was plotted (Fig. 4). There was good agreement between the predicted and observed probabilities. The Hosmer-Lemeshow test showed an excellent fit (χ²=7.314, p=0.503).

External validation was further performed in the validation cohort. The AUC was still as high as 0.812 (95%CI: 0.697-0.928) (Fig. 5). The nomogram calibration curve showed acceptable agreement between prediction and actual observation (Fig. 6).

In the present study, there was a 10.1% and 9.3% rate of PPOI in the training and validation cohort, respectively. This incidence was different from previous reports. Wolthuis et al. [3,4] found the rate of PPOI was 15.9% after colorectal resection [3] and Vather et al. [14] reported that PPOI occurred in 88 of 327 patients (26.9%) undergoing elective colorectal surgery [[i]]. Liang et al. demonstrated that the overall PPOI rate was 21.5% in 311 patients diagnosed with gastric or colorectal cancer [[ii]]. The difference of incidence was possibly due to ERAS programs have been widely implemented in our study.

Statistically significant differences were found in hypertension between the training and validation cohorts, but hypertension itself was not found to be associated with PPOI. In general, baseline data were essentially balanced in the two cohorts. The AUC of the nomogram was 0.788 in the training. The calibration plots showed a good agreement between nomogram prediction and actual observation, indicating that the model had a good diagnostic performance and an excellent calibration. In addition, the external validation of the nomogram showed a satisfactory outcome, which indicated that our nomogram could be used in various populations and clinical scenarios.

An age older than 65 years was identified as an independent risk factor for PPOI. This may be due to the fact that older individuals generally have more medical comorbidity and clinical frailty, and poorer nutritional and functional status compared with their younger counterparts [[iii]]. Our result emphasizes that postoperative surveillance should be especially carefully achieved in such patients who have an increased risk of morbidity and mortality after colorectal cancer surgery [[iv]].

The fact of male sex has also been shown to affect PPOI following colorectal resection. Consistent with the present study, some studies confirmed that the male sex was associated with increased risk of PPOI in elective colorectal surgery [[v]-[[vi]] [vii]]. This difference is explained by the narrower male pelvis which may make the surgery more difficult and challenging, and potentially secondary to the effects of estrogen and progesterone receptors throughout the gastrointestinal tract and differences in enteric nervous system signaling [17,[viii]].

Minimally invasive approaches include laparoscopic and robotic surgery. The advantages of robotic surgical systems such as superior instrumentatione and field of vision enable precise dissection in confined spaces such as the pelvis, allowing it to have rapidly gained acceptance in colorectal surgery [[ix]]. The robotic surgical systems for the treatment of colorectal cancer were introduced into this hospital in 2020, but only a minority of patients have been treated with robotic surgery because of its high cost. Previous studies have shown that there are no significant differences between laparoscopic and robotic approaches to PPOI and perioperative mortality [[x], [xi]]. Therefore, we combined laparoscopic and robotic surgery into one group in this study. The surgical approach was the strongest predictor of PPOI in our study. There is high-quality evidence supporting the routine use of a minimally invasive approach to patients with colorectal cancer. Compared with open surgery, minimally invasive surgery has shown better outcomes, including less postoperative pain, shorter time to flatus/bowel motion and oral nutrition, improved cosmesis, less intraoperative blood loss, reduced length of stay, improved cosmesis and similar long-term survival [[xii]-]-[[xiii]][xiv]].

Our finding describes an increased risk for PPOI in those who had opioid analgesic treatment. A multimodal, opioid-sparing, pain management plan should be employed throughout the ERAS [[xv]]. Patient controlled analgesia (PCA) of intravenous opioids was used when the pain control was poor. In addition to their intended central effect on pain receptors, opioids have an undesired influence peripherally in the GI tract, including decreased gastric motility and emptying and inhibiting bowel propulsion [[xvi]]. Opioid related dysmotility plays a central role in postoperative gut dysfunction [[xvii]]. More recently, peripheral μ-opioid receptor antagonists in patients have been developed for treatment or prevention of PPOI after surgery [[xviii]].

Previous studies believed that adherence to judicious intra-operative fluid management protocols was protective against development of PPOI [[xix],[xx]]. Similarly, this study showed that perioperative fluid overload was significantly associated with PPOI. This may be because hypervolemic management may result in electrolyte disturbances and splanchnic edema and increased abdominal pressure with decreased mesenteric blood flow, which in turn elicits disruptive tissue oxygenation and ultimately leads to prolongation of the recovery of bowel function [16].

PPOI is a common complication after colorectal surgery. Our results have shown that gender, age, surgical approach, perioperative fluid overload, postoperative opioid analgesic are significantly related to the risk of PPOI. The nomogram with these five factors can accurately predict the probability of PPOI and enable oncologists to guide clinical individualized activities.

PPOI: Prolonged postoperative ileus; POI: Postoperative ileus; ERAS: Enhanced recovery after surgery; AUC: Area under the receiver operating characteristic curve; IV: Total intravenous; POD: Postoperative day; IQR: Interquartile ranges; ROC: Receiver operating characteristic; PCA: Patient controlled analgesia

Acknowledgements

Not applicable.

Authors’ contributions

ZL and YL contributed to analysis data, secured funding and write the manuscript. Data collection was performed by JW. HZ review the manuscript. CY contributed to the conception, design. All authors read and proved the final manuscript.

Funding

This study was supported by the Startup Fund for scientific research, Fujian Medical University (Grant number: 2018QH1231, 2020QH1226), Fujian Provincial Health Technology Project (Grant number: 2021TG015) , Fujian Cancer Hospital Project (Grant number: 2021YN04, 2021YN16).

Availability of data and materials

The datasets generated and analyzed in this paper can be made available from the corresponding author on reasonable request.

Ethics approval and consent to participate

This study was performed in accordance with the principles of the Declaration of Helsinki. The study was reviewed and approved by the Institutional Ethics Committee of Fujian Cancer Hospital (NO. SQ2020-007-02) . As this study was strictly retrospective and collecting the existing data, the informed consent was waived by the Institutional Review Board of Fujian Cancer Hospital.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interest.

Author details

¹Department of Gastrointestinal Surgical Oncology, Fujian Medical University Cancer Hospital & Fujian Cancer Hospital, Fuzhou 350014, Fujian Province, China. ²Department of Gastrointestinal Surgical Oncology, Fujian Provincial Hospital, Fuzhou 350001, Fujian Province, China. ³Department of Anesthesiology Surgery, Fujian Medical University Cancer Hospital & Fujian Cancer Hospital, Fuzhou 350014, Fujian Province, China.

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No competing interests reported.

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Nomogram for Prediction of Prolonged Postoperative Ileus after Colorectal Resection

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