Risk factors for prolonged postoperative ileus after intracranial tumor surgery

doi:10.21203/rs.3.rs-1975250/v1

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Risk factors for prolonged postoperative ileus after intracranial tumor surgery

https://doi.org/10.21203/rs.3.rs-1975250/v1

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Background: Prolonged postoperative ileus (PPOI) is the most frequent postoperative complication and significantly increases postoperative morbidity and medical costs. The objective of this study was to identify the incidence and independent risk factors of PPOI after intracranial tumor surgery, so as to allow for advanced planning to reduce the incidence of PPOI.

Methods: After retrospective review of data from patients who underwent intracranial tumor surgery from January 2018 to March 2021, a total of 1135 patients (447 males and 688 females; median age 51 [41–61] years) were included in the study. Clinical parameters were compared between patients with PPOI and those without PPOI. Multivariate logistic regression analysis was performed to identify independent risk factors associated with PPOI.

Results: In total, 121 of 1135 (10.7%) patients experienced PPOI. Operation time ≥4 h (OR = 1.71, 95% CI 1.07–2.74, p = 0.03) and no flatus within postoperative 24 h (OR = 1.86, 95% CI 1.25–2.76, p = 0.002) were the independent risk factors of PPOI. In addition, in-hospital length of stay was longer and medical costs were higher in patients with PPOI than in those without PPOI (all p < 0.001).

Conclusions: Independent risk factors for PPOI are operation time ≥4 h and no flatus within postoperative 24 h. Patients with these risk factors should be carefully monitored, and steps such as attempting to shorten the duration of surgery and utilizing measures to facilitate flatus should be taken to minimize the development of PPOI and prevent the occurrence of secondary adverse events.

Trial registration: The study protocol was registered at Chinese Clinical Trial Registry (ChiCTR2200057468) on 13/03/2022.

intracranial tumor surgery

prolonged postoperative ileus

risk factors

Postoperative ileus (POI) is an iatrogenic, noninfectious inflammatory movement disorder. Definitions and incidence of POI varied among previous studies. Typically, the reported duration of POI ranges from 2 to 6 days [1], and that of prolonged POI (PPOI) ranges from 4 to 6 days [2, 3].

PPOI remains a serious public health problem. It is the most frequent postoperative complication [4], and affects 10% to 30% of patients after abdominal surgery [1]. Ineffective and weak peristalsis can result in the accumulation of gastrointestinal secretions, thereby causing nausea, vomiting, and abdominal distension, and PPOI may even require parenteral nutrition [5]. PPOI significantly increases postoperative morbidity, including dehydration, electrolyte imbalance, pneumonia, sepsis, deep vein thrombosis, and pulmonary embolism, which may lead to prolonged in-hospital length of stay (LOS) and increased costs of patient care [6-8]. Hence, it is important to identify the risk factors of PPOI to try to decrease these complications.

The already identified risk factors of POI or PPOI include age, sex, preexisting comorbidities, use of opioids, and type and duration of surgery [9-11]. Studies about the risk factors have been performed in gastrointestinal surgery and other types of surgery, including urological, gynecological, and orthopedic surgery [6-8, 12-16]. However, to the best of our knowledge, no study has focused on intracranial tumor surgery. Therefore, the objective of this study was to identify the incidence and independent risk factors of PPOI after intracranial tumor surgery.

Data source and study population

This was a single-center retrospective study. After ethics approval (LYS [2021] 232) from the Ethics Committee of the Xuanwu Hospital of Capital Medical University, the trial was registered with the Chinese Clinical Trial Registry (ChiCTR2200057468). This study was performed in accordance with the Declaration of Helsinki. All methods were performed in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [17].

Consecutive patients who underwent non-emergent intracranial tumor surgery from January 2018 to March 2021 in Xuanwu Hospital of Capital Medical University gave an informed consent for the use of their data, and the data were extracted from an electronic database and input into an excel sheet. Given that the use of opioid analgesics postoperatively has been reported as an independent risk factor of POI [9], patients who did not use patient-controlled intravenous analgesia (PCIA) postoperatively were excluded, so there was no variability in this regard. Patients with incomplete medical records, history of irritable bowel syndrome, <18 years of age, and those who returned to intensive care unit with tracheal tube and died within 72 h postoperatively were also excluded.

Measuring outcomes

The primary objective was to determine the incidence of PPOI after intracranial tumor surgery. PPOI was defined as interruption of gastrointestinal motility for more than 6 days postoperatively [3]. Namely, the definition of PPOI required two or more of the following criteria: abdominal distension and pain, nausea and vomiting, absence of flatus or stool, inability to tolerate oral diet, and ileus noted on computed tomography scans or plain abdominal films [18].

The secondary objective was to determine independent risk factors for PPOI. Demographic and perioperative characteristics were assessed between non-PPOI and PPOI groups. The recorded demographic characteristics included patients’ sex, age, body mass index (BMI), American Society of Anesthesiology (ASA) grade, and history of diabetes (based on clinical diagnosis). The recorded perioperative variables included duration of operation, the amount of sufentanil administered intraoperatively, intravenous fluid administration (defined as the volume of blood transfusion and fluid minus the volume of bleeding and urine), estimated blood loss, whether suspended red blood cells were transfused, and whether there was flatus within postoperative 24 h. The overall in-hospital LOS and medical costs were also compared between the non-PPOI and PPOI groups.

Intraoperative anesthesia management

All of the patients were induced with intravenous administration of etomidate (Nhwa Pharmaceutical Co., Ltd., Jiangsu, China) 0.1–0.2 mg/kg, sufentanil (Yichang Humanwell Pharmaceutical Co., Ltd., Hubei, China) 0.4–0.5 μg/kg, and rocuronium (Xianju Pharmaceutical Co., Ltd., Zhejiang, China) 0.6–0.9 mg/kg. To maintence the BIS value at 40–60, propofol (Fresenius Kabi AG, Bad Homburg, Germany) was administered at 3–5 mg/kg/h and dexmedetomidine (Hengrui Pharmaceutical Co., Ltd., Jiangsu, China) was administered at 0.2–0.3 μg/kg/h. And remifentanil (Yichang Humanwell Pharmaceutical Co., Ltd., Hubei, China) was administered at a rate of 0.3–0.4 μg/kg/min. Dexmedetomidine was discontinued infusion 1–2 h before the end of the operation. Low-dose norepinephrine infusion combined with goal-directed fluid therapy was used in fluid management [19].

Statistical analysis

Statistical analysis was performed using SPSS 26.0 software, and a level of 0.05 (two-sided) was used to indicate statistical significance. One-sample Kolmogorov–Smirnov Test was used to confirm normality for continuous variables. Univariate analyses were performed to assess the relationship between the potential predictive factors and the absence or presence of PPOI using Mann–Whitney U test for non-normally distributed continuous variables (data were expressed as median [interquartile range]), or chi-square test for categorical variables (data were expressed as the number [%] of patients). All variables with p < 0.10 in univariate analysis were then entered into a multivariate logistic regression model to assess independent risk factors.

A total of 2046 patients underwent non-emergent intracranial tumor surgery from January 2018 to March 2021 in our department. Among them, 911 patients were excluded for the following reasons: incomplete medical records (n = 286), history of irritable bowel syndrome (n = 11), age <18 years (n = 82), no use of PCIA (n = 230), return to intensive care unit with tracheal tube (n = 298), and death within 72 h postoperatively (n = 4). Ultimately, 1135 patients (447 males and 688 females) were included in the study. The median age was 51 (41–61) years, and median BMI was 24.4 (22.0–26.7) kg/m² (Fig. 1).

The overall rate of PPOI was 10.7% (121 of 1135 patients). Those who had developed PPOI had a significantly longer duration of in-hospital LOS than those who had not developed PPOI (19 [15-23] days vs.16 [14-21] days, p < 0.001) (Fig. 2A), and the medical costs were significantly higher in patients with PPOI than in those without PPOI (11.1 [9.5-13.6] thousand dollars vs. 9.8 [8.4-11.7] thousand dollars, p < 0.001) (Fig. 2B).

Sex distribution, age, BMI, and ASA grade were not significantly different between the non-PPOI and PPOI groups (all p > 0.05). The number of patients with history of diabetes was not significantly different between the non-PPOI and PPOI groups (p > 0.05) (Table 1).

Table 1 Comparison of patients’ demographic characteristics between the two groups

Factors	No PPOI (n = 1014)	PPOI (n = 121)	Z/χ²	p-value
Sex			1.24	0.27
Male	405 (39.9)	42 (34.7)
Female	609 (60.1)	79 (65.3)
Age (years)			0.43	0.51
<65	857 (84.5)	105 (86.8)
≥65	157 (15.5)	16 (13.2)
BMI (kg/m²)	24.4 (22.0-26.8)	24.1 (21.7-26.4)	-0.81	0.42
ASA grade			0.14	0.71
I–II	835 (82.3)	98 (81.0)
III–IV	179 (17.7)	23 (19.0)
Diabetes			0.22	0.64
No	942 (92.9)	111 (91.7)
Yes	72 (7.1)	10 (8.3)

PPOI prolonged postoperative ileus, BMI body mass index, ASA American Society of Anesthesiology

Data are expressed as number of patients (%) or median (interquartile range)

The perioperative characteristics were compared between the two groups. Compared with the patients without PPOI, those who had developed PPOI had a higher proportion of individuals with the operation time ≥4 h and a lower proportion of individuals with flatus occurrence within 24 h (all p < 0.05). The total estimated blood loss was significantly higher in the PPOI group than in the non-PPOI group (p < 0.05). Total intraoperative sufentanil use, intraoperative intravenous fluid administration, and whether suspended red blood cells were transfused were not significantly different between the non-PPOI and PPOI groups (all p > 0.05) (Table 2).

Table 2 Comparison of patients’ perioperative characteristics between the two groups

Factors	No PPOI (n = 1014)	PPOI (n = 121)	Z/χ²	p-value
Duration of operation (h)			7.47	0.006
<4	324 (32.0)	24 (19.8)
≥4	690 (68.0)	97 (80.2)
Intraoperative sufentanil (μg)	40 (30-45)	40 (30-45)	-0.88	0.376
Intravenous fluid administration (mL)	400 (0-900)	520 (100-900)	-1.14	0.255
Estimated blood loss (mL)	200 (100-400)	250 (200-500)	-2.38	0.017
Suspended red blood cells			0.02	0.902
No	979 (96.5)	116 (95.9)
Yes	35 (3.5)	5 (4.1)
Occurrence of flatus within 24 h			12.25	<0.001
Yes	531 (52.4)	43 (35.5)
No	483 (47.6)	78 (64.5)

PPOI prolonged postoperative ileus

Data are expressed as number of patients (%) or median (interquartile range)

Multivariate analysis

Multivariate logistic regression was performed to determine independent risk factors for PPOI. We showed that operation time ≥4 h and having no flatus within 24 h postoperatively were significantly associated with the development of PPOI. The odds of developing PPOI were nearly 1.71 times higher in those with operation time ≥4 h than in those with operation time <4 h (OR = 1.71, 95% CI 1.07–2.74, p = 0.03). The odds of developing PPOI were nearly 1.86 times higher in those without flatus within 24 h than in those with flatus within 24 h (OR = 1.86, 95% CI 1.25–2.76, p = 0.002) (Table 3).

Table 3 Multivariate logistic regression analyses of PPOI in patients undergoing intracranial tumor surgery

Risk factors	OR	95% CI	p-value
Duration of operation ³4 h	1.707	1.065-2.737	0.026
No flatus within postoperative 24 h	1.859	1.249-2.763	0.002

OR odds ratio, CI confidence interval

In this study, 10.7% of patients undergoing intracranial tumor surgery developed PPOI, indicating that the development of PPOI continues to be a common event. Operation time ≥4 h and no flatus within postoperative 24 h were the independent risk factors. As in previous reports [7, 20], patients who developed PPOI also had longer in-hospital LOS and higher medical costs. We did not identify some of the previously reported associations between perioperative variables and PPOI, including male sex, older age, and preexisting comorbidities [10, 11, 21], which may be attributed to different types of surgery and definitions of PPOI.

Temporary impairment of gastrointestinal motility is common but usually uncomplicated and associated with few consequences, while the onset of PPOI is usually accompanied by patient’s discomfort and decreased ambulation. As a result, patients with PPOI are at an increased risk of secondary adverse events, such as deep vein thrombosis, pulmonary embolism, and poor nutrition status, which may lead to wound infection and affect wound healing, thereby increasing medical costs and prolonging in-hospital LOS [6, 7]. There are two approaches to treat ileus: one is to prevent the onset of ileus, and the other one is to treat the subset of patients that have developed ileus; however, there is little to do to reverse an established ileus currently [16, 22]. Therefore, awareness of the risk factors for PPOI is important, which could allow clinicians to more closely to monitor high-risk patients. Such patients may benefit from certain interventions, such as attempting to shorten the duration of surgery, gum chewing, and multimodal pain regimens [23], to reduce the incidence of PPOI and prevent the occurrence of adverse events.

There is no single pathological mechanism of POI. The interplay between neurogenic, inflammatory, pharmacological components, fluid, and electrolytes is essential for the development of POI. The etiology of POI is thought to originate from neural reflexes activated during and immediately after surgery; namely, in response to surgery, sympathetic pathways are activated, leading to an inhibition of peristalsis. The second phase begins 3–4 h after surgery, where inflammatory cells are activated and sustained gut inflammation prolongs sympathetic overdrive to the gut and sensitizes extrinsic spinal sensory neurons, which prevents peristalsis. Agonists of gut opioid receptors exacerbate the process [24]. The final common pathway is impaired motility and contractility, as well as gut wall edema [18].

Surgical time may be used as a proxy measure of surgical invasiveness [16]. The longer the operation time is, the more severe the stress response and inflammatory response are, which may explain why the operation time ≥4 h was identified as a risk factor for PPOI. Results from previous studies are consistent with our findings. A study indicated that inflammation and strong surgical stress caused POI [24]. Another recent study with 531 patients reported that the duration of surgery was one of the five variables in the prediction model for POI after loop ileostomy closure [21]. In a retrospective study with 513 colon resections, duration of surgery >3 h was identified as an independent risk factor for POI [25].

Despite some controversies, there is evidence that opioid medication is involved in the pathogenesis of POI [3]. Previous studies have found that μ opioid receptors affect colonic motility through enteric nerve receptors [26]. A 17-year-long retrospective study indicated that a decreasing incidence of POI after total knee arthroplasty may be attributed to a reduction in opioid use postoperatively [27]. The present study excluded patients without analgesic pump and aimed to reduce the influence of postoperative opioid medication. Moreover, in this study, we did not find significant differences in the total intraoperative sufentanil amount between the non-PPOI and PPOI groups. Considering that surgical time may also be used as a proxy measure of intraoperative remifentanil consumption (a longer operation time is associated with a greater amount of intraoperative remifentanil consumption), we infer that intraoperative remifentanil consumption may be a risk factor. The relationship between intraoperative remifentanil consumption and development of POI has been previously described. Park et al. showed that the intraoperative dosage of remifentanil was an independent risk factor for POI in oblique lateral interbody fusion [28]. A study by Gifford et al. showed that intraoperative opioid dosage during spinal surgery, especially intraoperative remifentanil dosage, was an independent risk factor for POI, but preoperative opioid intake or postoperative dose of opioids (24 h or 72 h after surgery) were not able to predict POI [29].

In summary, the longer the operation is, the heavier the stress and inflammatory response are, and the greater intraoperative remifentanil consumption is, which may be the reason why the operation time ≥4 h was identified as an independent risk factor for PPOI.

In the present study, having no flatus within postoperative 24 h was an independent risk factor for PPOI. Although having no flatus is actually one of the symptoms of PPOI, we still include having no flatus within postoperative 24 h as a variable of PPOI, because it may help clinicians to identify patients at high risk of developing PPOI and take early interventions. To the best of our knowledge, no study has explored the relationship between no flatus within postoperative 24 h and PPOI.

A noteworthy finding in the present study is that intravenous fluid administration was not associated with PPOI. A previous retrospective trial found that stringent fluid management accelerated the recovery of bowel function after loop ileostomy closure [30]. Another study showed that increased intravenous fluid administration was associated with PPOI [31]. However, the median time to first flatus or first bowel motion did not differ between the restricted and standard groups following elective colorectal surgery [32]. Our study also did not find the association, which may be attributed to the fact that all patients in our study were managed with low-dose norepinephrine infusion combined with goal-directed fluid therapy. One recent review even found that goal-directed fluid therapy showed a beneficial effect in preventing POI [33].

There were some limitations in this study. First, given the nature of our retrospective study, there may be selection bias and confounding factors. Second, we did not identify some of the previously reported associations between perioperative variables and PPOI, which may be explained by the lack of a standardized definition of PPOI and the different types of surgery. Third, the data were from a single-center database and may not be generalized to other institutions. Forth, the data collected in the electronic database of this study were incomplete (such as preoperative bowel habits of patients, blood levels of potassium and calcium, the site and type of tumor); therefore, a prospective, multicenter study is needed.

Operation time ≥4 h and no flatus within postoperative 24 h are independent risk factors in the development of PPOI after intracranial tumor surgery. Identification of patients at a high risk of PPOI is useful to closely monitor them and take steps such as attempting to shorten the duration of surgery and utilizing measures to facilitate flatus to minimize the development of PPOI and prevent the occurrence of secondary adverse events.

PPOI: Prolonged postoperative ileus; POI: Postoperative ileus; LOS: length of stay; PCIA: patient-controlled intravenous analgesia; BMI: body mass index; ASA: American Society of Anesthesiology; OR: odds ratio; CI: confidence interval.

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of the Xuanwu Hospital of Capital Medical University (LYS [2021] 232). After obtaining informed consent from all the patients, the data were extracted from an electronic database.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This study was funded by the Beijing Municipal Health Commission (Jing2019-2).

Acknowledgments

We thank LetPub (www.letpub.com) for linguistic assistance and pre-submission expert review.

Authors’ contributions

F-FM designed and wrote the manuscript. LF designed and revised the manuscript. X-XF, K-PF and BJ to acquisition, analysis and interpretation of the data. T-LW designed and revised the manuscript. All authors read and approved the final version of the manuscript.

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No competing interests reported.

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Risk factors for prolonged postoperative ileus after intracranial tumor surgery

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