Ulcerative colitis (UC) is a chronic intestinal inflammatory disease, which is characterized by recurrent relapse and remission (1). Total proctocolectomy with ileal pouch–anal anastomosis (IPAA), first proposed in 1978 (2), involved the construction of a “J” pouch to maintain the continuity of the intestine and prevent permanent ileostomy. IPAA was considered as a radical surgery for patients with UC (2).

Although IPAA can significantly improve the long-term quality of life (3–5), the postoperative complications are inevitable. Pouchitis is the most common late complication of IPAA (6, 7), which seriously compromises the prognosis of the patients. Moreover, the etiology of pouchitis remains unclear (8). The pouchitis disease activity index (PDAI), revised in 1994 (9), is widely used in clinical practice to assess the clinical manifestation, endoscopic examination, and histologic findings of the pouch (10). Exploring appropriate indicators to predict the occurrence of post-IPAA pouchitis has become increasingly important.

Preoperative colonoscopy is necessary for each patient to evaluate endoscopic activity. However, data on the predictive value of the two most commonly used indices, namely, ulcerative colitis endoscopic index of severity (UCEIS) and the Mayo endoscopic score (MES) are scarce (11–13). Thus, we aimed to clarify the predictive value of preoperative endoscopic activity on the occurrence of pouchitis after IPAA. We performed this study to discover the incidence of post-IPAA pouchitis in our institute. Then, we compared the predictive values of UCEIS and MES for pouchitis to establish the best cut-off indicators for early colonoscopic surveillance after IPAA to predict the occurrence of pouchitis.

The UCEIS and MES were widely used systems to assess the endoscopic severity of UC to allow for convenient and appropriate decision-making by clinicians. However, whether UCEIS and MES can predict the development of pouchitis after IPAA and the comparison between their predictive values are still unclear. First, our study indicated that pouchitis occurred in 21.6% of IPAA cases in our institute and then demonstrated the predictive value of preoperative endoscopic activity on the occurrence of pouchitis. Furthermore, we proved that pre-IPAA UCEIS ≥ 7 and MES = 3 were contributing factors to pouchitis and that UCEIS outperformed MES as a predictor of pouchitis. These findings indicated the need for earlier and more frequent colonoscopic surveillance of the pouch after IPAA when patients had preoperative UCEIS ≥ 7.

Many previous studies have reported the risk factors for pouchitis (16, 17). The most recent study reported that patients with longer disease duration were susceptible to development of pouchitis (18). Similarly, researchers found that the cumulative incidence rates of pouchitis at 1, 2, 3, 4, and 5 years after IPAA were 25, 32, 36, 40, and 45%, respectively (19). Moreover, researchers reported that patients with cholangitis are more likely to undergo pouchitis surgery, with an incidence rate of 79% in the 10th year after IPAA (20). In addition, pancolitis, EIM, use of non-steroidal anti-inflammatory drugs, and specific gut microbiota were contributing factors to pouchitis (21–23). However, whether UCEIS and MES were associated with pouchitis was not reported in the literature. To the best of our knowledge, this study is the first to demonstrate that patients with UCEIS ≥ 7 had a higher risk of developing pouchitis than those with MES = 3. Previous study reported that histological and asymptomatic pouchitis had higher preoperative white blood cell count (p < 0.001) (24). Kalkana et al. discovered the relationship between the preoperative severity and activity of the disease and subsequent pouchitis development. They found that a higher disease activity index (p = 0.02) was an independent risk factors for the development of pouchitis (25). Therefore, we first constructed the endoscopic prediction model of preoperative UCEIS ≥ 7, which could reflect degree of the preoperative inflammation to provide a more direct and convenient approach to predict post-IPAA pouchitis to some extent.

Exploring novel predictors for pouchitis to enable early intervention is important in enhancing the management of UC after IPAA. Several recent studies have focused on the predictive value of fecal calprotectin (FC) for pouchitis. Johnson et al. indicated that the concentration of FC in pouchitis was significantly higher than that in uninflamed pouches and was associated with PDAI. Moreover, an FC cut-off value of 92.5 μg/g demonstrated a satisfactory predictive value for pouchitis (26). In another prospective study in which the FC level had already been evaluated before the diagnosis of pouchitis, an FC cut-off value of 56 μg/g exhibited a sensitivity of 100% and a specificity of 84% in predicting pouchitis (27). Thus, FC appeared to be a non-invasive and effective predictor of post-IPAA (28). However, the optimal threshold value of FC in predicting pouchitis and the timing of retesting of FC after IPAA has not been unified. In addition, not all patients will be tested for FC after IPAA, but all patients who undergo IPAA surgery will be subjected to preoperative endoscopic assessment for UCEIS and MES. We herein first indicated that UCEIS ≥ 7 had a better predictive value than MES = 3. Taken together, UCEIS outperformed MES in predicting pouchitis. Preoperative evaluation of endoscopic severity to determine UCEIS score could help clinicians predict the occurrence of post-IPAA pouchitis and earlier and more frequent postoperative colonoscopic surveillance could be conducted to prevent the development of pouchitis.

Limitations of this study included the loss to follow-up, which is inevitable in a retrospective study. Our sample size was relatively small. Larger sample sizes are recommended for future research.

In this study, we discovered the incidence of post-IPAA pouchitis in our institute and demonstrated that the UCEIS performed better than MES in predicting post-IPAA pouchitis. We found that pre-IPAA UCEIS ≥ 7 had a significant association with PDAI and was an effective predictor of pouchitis. We further demonstrated that pre-IPAA UCEIS ≥ 7 was an independent risk factor for pouchitis with a higher risk than an MES = 3. Therefore, earlier and more frequent postoperative colonoscopic surveillance should be performed in patients with preoperative UCEIS ≥ 7 to prevent the occurrence of pouchitis and enhance its management.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by The Ethics Committee of Xinhua Hospital (Approval No. XHEC-D-2020-107). The patients/participants provided their written informed consent to participate in this study.

PD and ZD conceived the study. WX analyzed the data and wrote the manuscript. WT and WD assisted some analysis. HH, WC, QQ, and LC collaborated to collect the information of patients. All authors participated in revising the manuscript and approved the final version.

This work was supported by the National Natural Science Foundation of China (No. 82000481 and 81873547), the Shanghai Sailing Program (No. 20YF1429400), and the Supporting Project of the Medical Science and Technology Innovation Platform of Health Commission of Hubei Province (PTXM2020011).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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