Introduction

Ulcerative colitis (UC) is a chronic inflammatory condition that greatly impacts patients’ quality of life (QOL) and daily functioning [1]. Despite significant advances in biologic treatments improving patient outcomes, approximately one-quarter to one-third of individuals with UC ultimately require colectomy due to complications like neoplasia or unmanageable disease [2]. The surgical procedure known as total proctocolectomy with ileal pouch-anal anastomosis (IPAA), introduced in 1978 [3], has become a standard intervention for UC and familial adenomatous polyposis. Research has consistently shown that IPAA can enhance QOL by preserving intestinal continuity and eliminating the need for permanent ostomies through J-pouch formation [4,5,6], whereas a comparable proportion of patients still undergo the early or late postoperative complications due to the technically demanding operation [7, 8]. Additionally, our previous study indicated that intraoperative intravenous fluid administration and surgical procedures were both associated with clinical outcomes [9, 10]. Thus, these developments emphasize the importance of delicate intraoperative implementation in the treatment of UC.

Currently, the proposed enhanced recovery program (ERP) addresses a perioperative multimodal approach beyond only the surgical management to reduce postoperative complications and improve rehabilitation [11]. The perioperative ERP includes aspects such as preoperative improved nutritional status, intraoperative standard anesthesia management, minimally invasive surgery, and postoperative early mobilization to improve clinical prognosis [12]. Initial studies have confirmed that the advancements in perioperative care through the use of ERP contributed to positive effects on patients’ clinical outcomes and recovery [13,14,15]. However, the current evidence of ERP is mainly based on oncology surgery, few studies focused on the feasibility and effectiveness of ERP in IBD patients [16]. A recent study reported that a specific perioperative ERP improved the clinical outcomes of patients with Crohn’s disease (CD) after surgery [17]. In contrast, a previous study with two heterogeneous cohorts (history group vs. modern group) indicated that ERP failed to reduce postoperative complications after IPAA [18]. Thus, the effect of perioperative ERP implementation on postoperative complications and long-term prognosis in a specific homogeneous cohort of UC patients after IPAA has yet to be evaluated and proven.

This research primarily sought to evaluate the potential impact of perioperative ERP implementation on UC patients undergoing IPAA within the China UC Pouch Center Union. Additionally, it aimed to investigate the association between perioperative ERP and clinical outcomes by examining postoperative complications and improvements in long-term QOL, offering practical guidance for clinicians regarding perioperative ERP adoption.

Methods

Patients

This research involved UC patients who underwent IPAA at our institute, a part of the China UC Pouch Center Union, from January 2008 to September 2023. Relevant clinical information was retrospectively obtained from electronic medical records and standard postoperative outpatient follow-up visits. Ethical approval for this study was granted by the Ethics Committee of Xinhua Hospital, under the Shanghai Jiaotong University School of Medicine (Approval No. XHEC-C-2024–186-1).

Inclusion and exclusion criteria

This study included patients diagnosed with UC who received IPAA and had comprehensive clinical and follow-up records at one of our four pouch surgery centers affiliated with the China UC Pouch Center Union. Exclusion criteria encompassed individuals with indeterminate colitis or Crohn’s disease, those who underwent permanent diverting ileostomy without pouch creation, and patients with incomplete data or poor compliance.

Recovery program

According to recent research, perioperative ERP was systematically categorized into three distinct phases: preoperative, intraoperative, and postoperative 17, following the well-recognized ERAS® Society guidelines [19, 20]. Preoperative ERP items included patients’ nutritional and general health status including normal albumin and hemoglobin Hb levels. The intraoperative phase mainly contained standard anesthesia management and minimally invasive surgery with less blood loss. Furthermore, postoperative ERP items were mainly characterized by early thromboprophylaxis, mobilization, removal of urinary catheter, and oral nutrition. In this study, UC patients who adhered to all perioperative ERP components were classified as the ERP group.

Clinical evaluation

The primary endpoints of this study included the incidence of post-IPAA complications and diminished long-term QOL. UC severity was classified into proctitis (E1), left-sided colitis (E2), and pancolitis (E3) following the Montreal classification criteria [21]. Postoperative complications were evaluated using the comprehensive complication index (CCI), derived from the Clavien-Dindo classification system [22], which categorizes complications into grades 1 through 4 based on the invasiveness required for management [23, 24]. Consistent with prior research [17, 22], complications with CCI > 26.2 were classified as severe complications in this study. Events occurring within 1 month post-IPAA were defined as early complications, while those beyond 1 month were classified as late complications. Long-term QOL was assessed using the Cleveland Global Quality of Life (CGQL) tool, which evaluates three domains: current QOL, current health status, and current energy levels (each scored from 0 to 10) [25]. The final CGQL score was calculated by averaging the total scores and dividing by 30. Preoperative CGQL was obtained through questionnaires administered during the initial hospital admission, whereas postoperative CGQL data were collected during the most recent follow-up. A postoperative CGQL improvement or decline exceeding 50% compared to baseline was defined as significantly improved or impaired long-term QOL, respectively, in alignment with our earlier findings [10, 26]. Preoperative laboratory results, medication, and intraoperative anesthesia data were also collected. This study adhered to the reporting recommendation (STROBE).

Statistical analysis

The statistical analyses in this study were conducted using SPSS version 22.0 (IBM, 2010, Chicago, IL, USA) and GraphPad Prism 8.0 (San Diego, CA, USA). Continuous and categorical data are presented as means with standard deviations or medians with interquartile ranges (IQR), respectively. For comparison of variables, two-sample Student’s t-test, Chi-squared test, Fisher’s exact test, and Wilcoxon’s rank-sum test were employed. Variables showing significant differences in univariate analysis were subjected to further evaluation through logistic regression analysis. All statistical tests were two-tailed, with a 95% confidence interval (CI), and p values below 0.05 were considered statistically significant.

Results

Baseline characteristics

A total of 230 UC patients who underwent IPAA at our institution were initially included in the study. After excluding 8 patients with incomplete follow-up data and 6 patients who did not undergo pouch construction, 216 UC patients with complete data remained eligible for analysis (Fig. 1). The median follow-up period and disease duration for the entire cohort were 8.0 years (IQR, 4.0–11.0) and 4.0 years (IQR, 2.0–7.0), respectively (Table 1). Among the participants, 62 patients (28.7%) followed a strict perioperative ERP protocol. The majority of patients (87.5%) underwent IPAA due to failure of medical management (Table 1).

Fig. 1
figure 1

The flow chart of this study

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Table 1 Main baseline characteristics of patients
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Postoperative complications

In this study, early postoperative complications occurred in 57 patients, accounting for 26.4% of the cohort. Of them, 30 (13.9%) developed early postoperative intestinal obstruction, 10 (4.6%) had a pouch and anastomotic bleeding, 7 (3.2%) experienced a pouch-anal anastomotic leak, 16 (7.4%) developed wound infection, and 3 (1.4%) had incision hernia. Furthermore, 75 patients (34.7%) experienced late postoperative complications, primarily including pouchitis, long-term postoperative intestinal obstruction, pouch-vagina fistula, and anastomotic stricture. Moreover, 44 patients (20.4%) had complications with Clavien-Dindo classification > 2, and 51 patients (23.6%) developed severe complications with CCI > 22.6 (Table 2).

Table 2 Main postoperative complications of IPAA
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Clinical outcomes in patients with or without perioperative ERP

To assess the impact of perioperative ERP on clinical outcomes, we compared postoperative complications and long-term QOL improvements between patients with and without perioperative ERP. As shown in Table 3, patients without perioperative ERP implementation had higher CCI (p = 0.036) and were more likely to develop complications with Clavien-Dindo classification > 2 (p = 0.036) and CCI > 26.2 (p = 0.019) as well as early postoperative complications (p = 0.004), mainly presented in early postoperative intestinal obstruction (p = 0.045) and wound infection (p = 0.044). Consistent with these results, the non-ERP group accounted for 74.5%, 85.2%, 82.4%, and 100% of complications with Clavien-Dindo classification II, IIIa, IIIb, and IVa, respectively (Fig. 2). Regarding long-term QOL, the ERP group demonstrated greater improvements in the postoperative current quality of life, health quality, energy level, and overall CGQL scores (Fig. 3). Additionally, patients who underwent perioperative ERP were more likely to show significant CGQL improvements (p < 0.001). Moreover, patients in the ERP group had a shorter hospital stay (LOS) compared to the non-ERP group (9 days vs. 16 days, p = 0.046, Table 3). Thus, our findings suggest that perioperative ERP may serve as a protective factor against postoperative complications and contribute to significant long-term QOL enhancement.

Table 3 Analysis of the clinical outcome and QOL in patients with or without perioperative ERP implementation
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Fig. 2
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The pERPentage of postoperative complications with different Clavien-Dindo classifications in the ERP and non-ERP groups

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Fig. 3
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Evaluation of the long-term QOL via the pre-IPAA and post-IPAA CGQL instrument in ERP and non-ERP group. Three items of the CGQL instrument—current quality of life (A), current quality of health (B), and current energy level (C)—and the overall CGQL scores (D) were compared in ERP and non-ERP group

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Perioperative ERP decreased the risk for severe post-IPAA complications with CCI > 26.2

Building on the above findings, we investigated whether the absence of perioperative ERP could contribute to severe post-IPAA complications. The univariate analysis revealed that perioperative ERP (p = 0.019), extraintestinal manifestations (p = 0.040), and intraoperative blood loss (p < 0.001) were significantly associated with severe post-IPAA complications (Table 4). Further analysis through multivariate logistic regression indicated that non-ERP implementation (odds ratio [OR], 3.195; 95% CI, 1.332 to 7.664; p = 0.009) and intraoperative blood loss exceeding 200 ml (OR, 4.090; 95% CI, 2.054 to 8.146; p < 0.001) were contributing factors for the occurrence of severe complications after IPAA, with a CCI > 26.2 (Table 5).

Table 4 Analysis of risk factors for severe postoperative complications in UC patients after IPAA
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Table 5 Logistic regression analysis of risk factors for severe postoperative complications in UC patients after IPAA
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Perioperative ERP improved the long-term QOL after IPAA

Additionally, we examined whether perioperative ERP influenced long-term QOL following IPAA. Initially, univariate analysis was conducted. As shown in Table 6, factors such as age at diagnosis (p = 0.023), perioperative ERP (p < 0.001), surgical approach (p = 0.009), and perioperative albumin (Alb) levels (p = 0.017) were significantly associated with improvements in postoperative long-term QOL. These variables were then selected for multivariate logistic regression, which revealed that being over 40 years old at diagnosis (OR, 1.805; 95% CI, 1.001 to 3.256; p = 0.049), non-ERP management (OR, 3.222; 95% CI, 1.462 to 7.101; p = 0.004), and undergoing open surgery (OR, 3.236; 95% CI, 1.462 to 7.101; p = 0.001) were independent factors contributing to impaired long-term QOL improvement after IPAA (Table 7).

Table 6 Analysis of influencing factors for long-term QOL improvement in UC patients after IPAA
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Table 7 Logistic regression analysis of risk factors for impaired long-term QOL in UC patients after IPAA
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Discussion

Current evidence of ERP mainly focused on oncological patients [16], and its effect on UC patients after IPAA remains unknown. This study, with the largest sample size and the longest follow-up period, is the first to report findings on the relationship between perioperative ERP and clinical outcomes in UC patients after IPAA from the China UC Pouch Center Union. Our results indicated that patients who received perioperative ERP experienced a lower incidence of severe complications, had a shorter LOS, and were more likely to achieve significant improvements in long-term QOL. We further demonstrated that non-ERP implementation and intraoperative blood loss exceeding 200 ml contributed to the development of severe complications with CCI > 22.6. Moreover, being over 40 years old at diagnosis, non-ERP implementation, and non-minimal invasive surgery contributed to the impairment of long-term QOL. Thus, perioperative ERP implementation is a necessary and considerable decision-making for UC patients.

Previous studies have demonstrated that CCI is a sensitive scale that reflects the number and severity of complications [22,23,24]. In this study, we reported intraoperative excessive blood loss and non-ERP implementation increased the risk of severe complications with CCI > 26.2. Previous research has shown that excessive blood loss is linked to higher mortality rates and longer LOS [27, 28]. Moreover, our earlier studies also revealed that intraoperative blood loss exceeding 200 ml was associated with an increased risk of early surgical complications [10, 26]. Thus, pouch surgery should pay more attention to minimize intraoperative blood loss due to excessive bleeding deteriorating the general physical conditions of the patients to affect prognosis [29]. Previous research indicated that IBD patients undergoing surgery were prone to develop postoperative complications compared with patients with neoplasm [30]. Currently, there is still controversy over whether ERP can reduce postoperative complications in IBD patients. Liska et al. [31] indicated that IBD patients benefited from the use of ERP, demonstrating decreased LOS and costs, whereas the incidence of postoperative complications has not decreased. Consistent with the result, the only small randomized study with 32 CD patients also reported the positive effect of perioperative ERP on LOS and costs, whereas ERP failed to decrease the incidence of postoperative complications [32]. In contrast, a previous study reported that perioperative ERP could reduce the incidence of postoperative complications in IBD patients after surgery [33]. Moreover, a recent prospective single-center study revealed that perioperative ERP implementation obviously improved the clinical outcomes of CD patients, mainly included decreased LOS and the rates of severe postoperative complications with CCI > 26.2 17. However, for UC patients, these studies failed to clarify the surgical procedures (colectomy with permanent ileostomy or total proctocolectomy with IPAA). Current evidence for the application of perioperative ERP in a specific homogeneous cohort of UC patients undergoing IPAA remains unclear. The latest study found that ERP reduced the LOS of UC patients after IPAA surgery, but it failed to reduce complications, which could be explained by a heterogeneous cohort of patients who had various different characteristics (history group vs. modern group) [18]. In the present study with a specific homogeneous cohort of UC patients from China UC Pouch Center Union, we first demonstrated that perioperative ERP effectively decreased the risk of severe postoperative complications with CCI > 26.2 for UC patients after IPAA, which provided more supporting evidence to promote perioperative ERP implementation to improve clinical outcomes for UC patients.

The effect of ERP on QOL in patients after colorectal surgery remains unclear. A recent systematic review indicated that ERP failed to affect the health-related QOL within 10 days after surgery, which could be explained that adjunctive chemotherapy was performed in some patients to influence the improvement of QOL [34]. Wang et al. [35] reported that ERP improved the short-term QOL in colonic cancer patients within 30 days after colonic resection. While these studies focused on oncological patients and evaluated their short-term QOL within 1 month after surgery, it was not demonstrated whether perioperative ERP implementation correlated with the long-term outcomes of UC patients after pouch surgery. This study with a long-term follow-up time first demonstrated that UC patients with perioperative ERP implementation achieved more obvious improvement of long-term QOL. Thus, strictly following perioperative ERP implementation could decrease the incidence of severe complications and further promote patients to achieve better long-term prognosis, which could be a considerable strategy for the perioperative management of UC patients.

Our study has certain limitations. The loss of follow-up and incomplete data are inevitable due to the characteristic of the retrospective study. Additionally, a multicenter prospective study should be conducted to further confirm our conclusions.

In conclusion, this study provides the first evidence that perioperative ERP notably enhances clinical outcomes, as reflected in a reduction of postoperative complications, a shorter length of hospital stay, and a marked improvement in long-term quality of life. Moreover, our findings underscore that the adoption of perioperative ERP serves as an independent protective factor, significantly reducing the incidence of severe postoperative complications and fostering substantial long-term improvements in quality of life. Thus, our study first provided supporting evidence for the application of perioperative ERP in a specific homogeneous cohort of UC patients after IPAA to make patients achieve better long-term prognosis.