Ulcerative Colitis Endoscopic Index of Severity (UCEIS) versus Mayo Endoscopic Score (MES) in guiding the need for colectomy in patients with acute severe colitis

Gastroenterology Report, Feb 2018

The Ulcerative Colitis Endoscopic Index of Severity (UCEIS) and the Mayo Endoscopic Score (MES) were developed as an objective method of the endoscopic severity in ulcerative colitis (UC); however, it was still unclear whether UCEIS vs MES could guide the need for colectomy in acute severe colitis (ASC).

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Ulcerative Colitis Endoscopic Index of Severity (UCEIS) versus Mayo Endoscopic Score (MES) in guiding the need for colectomy in patients with acute severe colitis

Gastroenterology Report Ulcerative Colitis Endoscopic Index of Severity (UCEIS) versus Mayo Endoscopic Score (MES) in guiding the need for colectomy in patients with acute severe colitis Tingbin Xie 1 Tenghui Zhang 0 Chao Ding 0 Xujie Dai 0 Yi Li 0 Zhen Guo 0 Yao Wei 0 Jianfeng Gong 0 1 Weiming Zhu 0 Jieshou Li 0 0 Department of General Surgery, Jinling Hospital, Medical School of Nanjing University , Nanjing, Jiangshu , China 1 Department of General Surgery, Jinling Hospital Affiliated to Southern Medical University , Guangzhou, Guangdong , China Background: The Ulcerative Colitis Endoscopic Index of Severity (UCEIS) and the Mayo Endoscopic Score (MES) were developed as an objective method of the endoscopic severity in ulcerative colitis (UC); however, it was still unclear whether UCEIS vs MES could guide the need for colectomy in acute severe colitis (ASC). Methods: Consecutive ASC patients between January 2012 and May 2016 were retrospectively evaluated. Demographic data, previous therapy, clinical observations, laboratory parameters, medical therapy and endoscopic assessments were documented. The primary outcome was the need for colectomy during admission and follow-up. Results: Ninety-two patients were enrolled. 37 (40.2%) needed colectomy. UCEIS score is a predictor of requirement for colectomy in multivariate analysis (OR, 3.25; 95% CI, 1.77-5.97; P < 0.001). Receiver-operator characteristic (ROC) area of UCEIS is 0.85, with a sensitivity of 60.3% and specificity of 85.5% using cut-off value of 7, which outperforms MES with the ROC area of 0.65; When UCEIS score 7, 80% of patients eventually need colectomy. Conclusion: UCEIS outperformed MES as a predictor for need for colectomy in ASC patients. The high probability of medical treatment failure and benefits of early colectomy should be discussed in patients with baseline UCEIS 7. Acute severe colitis; colectomy; Ulcerative Colitis Endoscopic Index of Severity; Mayo Endoscopic Score Introduction Ulcerative colitis (UC) is a chronic inflammatory disorder involving exclusively the colonic mucosa. Overall, 24.8% had at least one admission for acute severe colitis (ASC) [ 1 ]. When ASC arises, the cornerstone of management remains intravenous (IV) corticosteroids, with a response rate between 57 and 70% [ 2,3 ]. The introduction of rescue therapy with cyclosporine A (CsA) and infliximab (IFX) has provided an effective alternative to early colectomy. However, the failure rate of rescue therapy is about 54–60% [ 1,4 ]. Therefore, a substantial number of patients will eventually need colectomy, and 19.9% of ASC patients required colectomy at first admission. As prolonged medical therapy is associated with increased health care expenditures and probably a delay to subsequent restorative procedures and post-colectomy complications, it is important to identify patients who will not respond to corticosteroid therapy and necessitate prompt rescue therapy or colectomy. Traditionally, outcomes following IV corticosteroid therapy in ASC were predicted by clinical or laboratory parameters, such as stool frequency, C-reactive protein (CRP) and serum albumin levels. Prognostic models such as Ho-index, Travis and Lindgren criteria have also been used [ 5,6 ], but these indices are somewhat subjective and inconsistently used in clinical practice. As mucosal healing is increasingly emerging as a specific treatment goal in UC, the importance of endoscopic evaluation in predicting outcomes is being increasingly recognized. Currently, there are mainly two endoscopic score systems of mucosal inflammation in clinical practice. The sigmoidoscopic component of the Mayo Endoscopic Score (MES) and the Ulcerative Colitis Endoscopic Index of Severity (UCEIS) show the most promise as reliable evaluative instruments of endoscopic disease activity. The MES has been widely used since 1987, and a score of 0 and 1 is used as a definition of mucosal healing in clinical studies and trials [ 7 ]. The UCEIS was developed by Travis et al. in 2012 as a tool to accurately predict the overall assessment of the endoscopic severity of UC [ 8 ]. It was found that UCEIS scoring is minimally affected by clinical information of disease activity and strongly correlated with patient-reported symptoms. Ikeya et al. suggest that the UCEIS is more responsive to change following tacrolimus remission induction therapy for active UC than the MES [ 9 ]. Also, Ikeya et al. found that endoscopic severity is associated with the outcome in ASC and when the UCEIS is 7, almost all patients need salvage therapy [ 10 ]. However, there is a lack of studies comparing the predictive value of the need for colectomy by the two scoring systems in ASC. The aim of the current study is to compare the predictive value of need for colectomy with two endoscopic score systems in our cohort of ASC patients. Patients and methods Patients The Ethics Committee of Jinling Hospital approved the study protocol. Consecutive patients diagnosed as ASC from the inflammatory bowel disease (IBD) centre of the hospital between January 2012 and May 2016 were retrospectively reviewed through the medical records. Inclusion criteria were as follows: (i) age 18 or over, (ii) a confirmed diagnosis of ASC, (iii) available data on the in-hospital clinical course, (iv) availability of a flexible sigmoidoscopy within 1 week before start of treatment. Patients with toxic megacolon, emergency situations needing urgent surgery (massive bleeding, perforation), Crohn’s colitis or indeterminate colitis were excluded. The diagnosis of UC was based on clinical, radiological and pathological criteria. The definition of ASC was made using Truelove & Witt’s criteria [ 11 ], defined as six or more bloody stools per day with one or more additional criteria (pulse > 90 bpm; temperature > 37.8 C; haemoglobin < 105 g/L; erythrocyte sedimentation rate (ESR) > 30 mm/h; or CRP > 30 mg/dL). The extent of colon involvement was determined by abdominal CT scan. Management Inpatient management followed the standard protocol. Clostridium difficile and cytomegalovirus infection were excluded. IV steroids were started with methylprednisolone 60 mg/d or hydrocortisone 400 mg/d. Malnourished patients received nutritional support, and enteral nutrition was preferred over parenteral nutrition. For patients with hypoalbuminemia (<25 g/L), IV albumin was given. Subcutaneous low-molecular heparin as thromboembolic prophylaxis was used. The response to IV steroid therapy was assessed at days 3 to 5. The decision and timing of colectomy were made by the joint discussion of the gastroenterologists and colorectal surgeons. Patients with deterioration in general condition or adverse prognostic characteristics underwent emergency colectomy in 24–48 hours. Those who were refractory or had incomplete response to steroid were colectomized, switched to rescue therapy with IV infliximab 5 mg/kg/d or cyclosporine 2 mg/kg/d, or maintained under IV corticosteroids for a few additional days (7–10 days maximum). Those who had complete response were switched to oral prednisolone. Data on duration of IV steroid therapy and response were recorded, as well as rescue therapy. All patients were followed up until May 2016. Data collection For each patient, clinical data recorded during hospital admission were retrieved, which included: (i) demographics, age, sex, duration of disease, previous maintenance therapy, maximum extent of macroscopic disease on CT scan, baseline sigmoidoscopy appearances; (ii) clinical observation—daily stool frequency, pulse rate and temperature; and (iii) laboratory parameters. Image analysis Sigmoidoscopy images within 1 week before initiation of treatment were obtained from the PACS system of the hospital and endoscopy was performed using an Olympus-CF-H260 endoscopy (9.8-mm diameter; Tokyo, Japan) without fluoroscopic guidance. Two gastrointestinal endoscopic physicians majored in IBD who were unaware of the outcome were involved in image analysis, with disagreement being resolved by a senior physician. All cases were evaluated using the UCEIS and the MES. The UCEIS consists of the following three descriptors and was calculated as a simple sum: vascular pattern (scored 0–2), bleeding (scored 0–3), and erosions and ulcers (scored 0–3). Since this was a pragmatic study, vascular pattern (scored 0–2), erosions and ulcers (scored 0–3) were analysed according to colonoscopic images, and bleeding (scored 0–3) was analysed according to colonoscopic reports that contained the colonoscopy performer’s description at the time of the bleeding situation. The range in the UCEIS scores is 0 to 8 (Table 1), which was stratified into four grades: remission (0–1); mild (2–4); moderate (5–6); and severe (7–8). The MES was classified into the following four categories: 0, normal or inactive disease; 1, mild disease with erythema, decreased vascular patterns and mild friability; 2, moderate disease with marked erythema, absence of vascular patterns, friability and erosions; 3, severe disease with spontaneous bleeding and ulceration. Outcome assessments The main objective was to compare the predictive value of two widely used scoring systems (the UCEIS and the MES) in ASC, and the primary outcome was the need for colectomy during admission or on follow-up. Corticosteroid non-responders during admission, including patients who needed rescue therapy, Statistical analysis was performed using SPSS 20.0 (SPSS, Inc., IBM Company, Chicago, IL). Categorical variables were compared using the v2 test or Fisher’s exact test. Correlations were tested using Spearman’s test. Parametric variables were analysed using t-tests and non-parametric variables were compared using the Mann–Whitney U test. Kaplan–Meier survival analysis was performed to examine the development of endpoints by UCEIS at admission over time, with significance determined using a log rank test. Univariate analysis was performed and factors with a significant univariate probability (p < 0.1) were included in the multivariate logistic regression analysis to examine the binary outcomes and hypothesized predictors. The receiver-operating characteristic (ROC) curve analysis was also performed. A twotailed p < 0.05 was considered statistically significant. Results Patients Of the 764 UC patients screened, 92 met the criteria of modified Truelove & Witts criteria for ASC. Among them, 50 (54.3%) were male. The mean age was 42.1614.8 years. The median disease duration was 23 (range 1–296) months. For previous medical history in the past 1 year of admission, 6 (6.5%) patients had no treatment, 31 (33.70%) had 5-ASA, 10 (10.9%) with sulfasalazine, 16 (17.4%) with azathioprine, 29 (31.5%) had steroid therapy for 3 months and 7 (7.6%) had previous rescue therapy with infliximab or cyclosporine. Other baseline characteristics (significant comorbid diseases, active smokers, location and extent of disease, nutritional support during admission) are included in Table 2. Clinical course Among the 92 patients, 41 succeeded with IV steroid therapy and switched to oral steroid and maintenance therapy. Of the remaining 51 patients, 23 had deterioration of the situation and need emergency colectomy and 28 patients had incomplete respond to IV steroid therapy by day 5. Among the 28 patients with incomplete response, 13 had prolonged IV steroid therapy and 15 (39.4%) received rescue therapy with IFX (n ¼ 14) and CsA (n ¼ 1), among whom 6 patients (5 with IFX and 1 with CsA rescue therapy) did not achieve clinical remission and underwent colectomy during the hospital stay. Of the 63 patients who were discharged after medical therapy, 50 were maintained at remission and 13 were re-admitted, among whom 8 patients underwent colectomy during a median follow-up of 73.7 (range 40.1–123.1) weeks. Thus, a total of 37 patients (40.2%) underwent colectomy during hospital admission and follow-up. Surgical procedures performed were subtotal colectomy (n ¼ 2), proctocolectomy with ileal pouch anal anastomosis (n ¼ 31) and proctocolectomy with permanent ileostomy (n ¼ 4). There was one death after colectomy due to multiple organ dysfunction syndrome (MODS). Univariate and multivariate analysis of factors related to need for colectomy The UCEIS and the MES score were significantly higher in colectomized patients compared to non-colectomized patients (UCEIS: 6.2461.21 vs 4.4961.15, p < 0.001; MES: 2.8960.32 vs 2.5660.50; p ¼ 0.010). Other factors found to be significantly associated with the need for colectomy in the univariate analysis included baseline CRP level (31.8623.6 vs 42.4626.0; p ¼ 0.042) and albumin level (35.367.3 vs 31.165.8; p ¼ 0.004). These factors were then analysed using a multivariate analysis model to determine the risk factors independently associated with the need for colectomy. Age, stool frequency and platelet were also included in the multivariate model (all p < 0.10). In the multivariate analysis, only the UCEIS was found to be an independent risk factor for colectomy (p < 0.001; odds ratio [OR]: 3.25, 95% confidence interval [CI]: 1.77–5.97). Details of colectomy and non-colectomy groups are listed in Table 3. The colectomy rate was 0% when the UCEIS ¼ 3, 17.4% when the UCEIS ¼ 4 and 80.0% when the UCEIS ¼ 7–8, with an OR of colectomy from 1 to 4.37 (95% CI: 1.17–9.05; p < 0.001) when the UCEIS increased from 3 to 8, as shown in Figure 1A. The colectomy rate was 13.8% when the MES ¼ 2 and 60.0% when the MES ¼ 3, with an OR of colectomy from 1 to 3.42 (95%CI: 1.35–8.74; p < 0.001) when the UCEIS increased from 2 to 3, as Figure 1B shows. Prognostic accuracy of the UCEIS vs the MES for the need for colectomy The ROC curve analysis was performed to evaluate the performance of the UCEIS vs the MES to predict the need for colectomy. be refractory to IV steroids than low-risk patients: 84.0% for UCEIS 7–8 vs 57.6% for UCEIS 5–6 vs 11.8% for UCEIS 2–4 (p < 0.001) and 62.1% for MES 3 vs 11.5% for MES 2 (p < 0.001). Patients classified as high-risk according to UCEIS criteria were also more likely to be refractory to salvage therapy: 87.5% for UCEIS 7–8 vs 14.3% for UCEIS 5–6 vs 0.0% for UCEIS 2–4 (p ¼ 0.003). The MES high-risk group did not demonstrate an increased failure rate of salvage therapy compared to the low-risk group (53.8% vs 50.0%, p ¼ 1.000). The UCEIS and MES classifications identified a population that was at higher risk of colectomy. Overall colectomy rates were 80.0% for UCEIS 7–8 vs 39.4% for UCEIS 5–6 vs 11.8% for UCEIS 2–4 (p < 0.001) and 51.5% for MES 3 vs 11.5% for MES 2 (p < 0.001). Details are explained in Table 4. A Kaplan–Meier survival analysis was performed in patients with UCEIS 7 vs UCEIS < 7, and in patients with MES ¼ 3 vs MES ¼ 2, as shown in Figure 3. The overall colectomy-free survival rate at week 100 in patients with UCEIS 7–8 was significantly lower compared to those with UCEIS <7 (p < 0.001). When MES ¼ 3, the overall colectomy-free survival rate at 100 was significantly lower compared to MES ¼ 2 (p < 0.001). Cost-effectiveness of early colectomy vs late or no colectomy in patients with UCEIS 7 Early colectomy was defined as colectomy without rescue therapy. Late colectomy was defined as colectomy after rescue therapy on admission or during follow-up. Among the 25 patents with UCEIS 7, 11 (44%) underwent early colectomy, 9 (36%) underwent late colectomy and 5 (20%) were maintained on medical therapy without surgery. Figure 4 depicts the mean hospitalization cost of different treatment strategies in ACS patients with UCEIS 7. The mean hospitalization costs of patients with non-colectomy, early colectomy and late colectomy were CNY 120 082.2611 029.2, 111525.5635 532.1 and 183 550.2633 054.5, respectively. Costs of late-colectomy patients were significantly higher compared with others (p < 0.001); costs between the early-colectomy group and the non-colectomy group were comparable (p ¼ 0.221) (Table 5). The UCEIS score has a good predictive value with an area under the ROC curve (AUC) of 0.85 (sensitivity 60.3%, specificity 85.5%, cut-off value 7 points). The predictive value of the MES was lower, with an AUC of 0.65 (sensitivity 89.2%, specificity 43.6%, cut-off value 3 points), as shown in Figure 2. A significant association between the UCEIS and the MES was noted (Spearman’s rho ¼ 0.704, p < 0.001). We also tested the correlation between the UCEIS score and Mayo Clinic score, and there was significant correlation (Spearman’s rho ¼ 0.762, p < 0.001). Patient outcomes according to the UCEIS or MES risk stratifications According to the day 3 risk criteria of IV steroid therapy, patients categorized as high-risk (UCEIS 7–8 and MES 3) were more likely to 0.076 0.704 0.751 0.428 0.267 0.267 0.422 0.601 0.062 <0.001 0.010 0.264 0.042 0.854 0.166 0.085 0.004 1.00 (0.85–1.19) 3.25 (1.77–5.97) 0.45 (0.08–2.59) 1.00 (0.98–1.03) 1.01 (0.99–1.01) 0.96 (0.88–1.05) 0.960 <0.001 0.372 Discussion Despite improvements in medical care and the introduction of biologics therapy, a substantial number of patients with ASC require subsequent colectomy. The present study was to examine the role of the UCEIS vs the MES as a predictive measure to translate endoscopic disease appearance into a prediction of the clinical course of ASC. In our study, the UCEIS had a better predictive value for colectomy than the MES in ASC patients; when the UCEIS is 7, 80% of the patients will require colectomy during admission and follow-up, whether or not the patients received rescue therapy, and the clear economic advantages of early colectomy in patients with UCEIS 7–8 are also worth mentioning. The right time for surgery is important for ASC. It is often considered that, in patients with poor prognostic features or fulminant disease, a prolonged preoperative hospitalization correlates with worse outcomes after colectomy [ 12–14 ], and the case for early surgery (rather than further medical intervention) may be more compelling in patients with high-risk scores, so an accurate scientific risk-assessing method is of great importance to the clinical pathways. For example, the Ho score and Travis criteria have been widely used to identify patients who are at high risk of failing therapy and needing second-line therapy or colectomy. The value of colonoscopy in predicting the response to medical therapy has been proven in previous studies. Carbonyl et al. found that severe endoscopic lesions with deep extensive ulcerations, well-like ulcerations, large mucosal abrasion or mucosal detachment were associated with an increased risk of failure of intensive intravenous treatment of steroids [ 15 ]. According to the study by Cacheux et al., in 118 patients, the presence of severe endoscopic lesions was an independent predictive factor of colectomy in patients undergoing CsA therapy [ 16 ]. However, due to the significant inter-observer variation, these evaluations were rather subjective in defining the severity of the endoscopic appearance. The advantage of the UCEIS score is that it is a rather objective method to evaluate the endoscopic severity of UC. According to its developers, Travis et al., the UCEIS and its components show satisfactory intra- and interinvestigator reliability [ 8 ]. Among investigators, the UCEIS accounted for a median of 86% of the variability in the evaluation of overall severity on the visual analogue scale (VAS) when assessing the endoscopic severity of UC and was unaffected by knowledge of clinical details [ 4 ]. According to the result of Ho et al., 87% of patients with calprotectin greater than 1922.5 mg/g had colectomy at 6 months of follow-up [ 17 ]. Theede et al. showed that almost all patients with UCEIS 7–8 had fecal calprotectin >1000 lg/g [ 18 ]. Therefore, correlation of the UCEIS with the need for colectomy seems to be proven indirectly by previous studies. In our study, the relation between the UCEIS and the MES was evaluated and the result indicated a good correlation. The UCEIS better predicted requirement for colectomy than the MES; this difference is possibly due to the narrow distribution and small range of MES criteria, and UCEIS ranges from 3 to 8 for those patients with MES ¼ 3. Prognostic variables were analysed by ROC curves and the result was consistent with our hypothesis. Despite the MES (cut-off value: 3) having a higher sensitivity (89.2% vs 60.3%) than the UCEIS (cut-off value: 7), the specificity of the MES for colectomy was only 43.6%. Because surgical extirpation was the last effective treatment, the UCEIS might guide a more rational selection. In the current study, the UCEIS score and the MES score were both based on the examination of sigmoidoscopy, which might underestimate the severity of the disease in some patients, especially for those with rectum-sparing disease. Menasci et al. have shown that the UCEIS calculated as a sum of the single colonic segments performed better than regular UCEIS in UC outpatients [ 19 ]. Also, Lobaton et al. suggested that the Modified MES, which evaluated all the colon segments, could serve as a new index for the assessment of the extension and severity of endoscopic activity in UC patients [ 20 ]. However, full colonoscopy in the presence of ASC is not advisable due to the possibility of toxic megacolon or colonic perforation. Also, according to a recent study by Colombel et al., there is a high degree of correlation in assessments of UC activity made by rectosigmoidoscopy vs colonoscopy in both the UCEIS and the MES scores [ 21 ]. In the current study, CT scan was used to evaluate the extent of the disease in ASC patients. There were three main limitations of our study. First, our study had a retrospective nature and was from a single centre. Thus, treatment was not controlled, which might affect the outcomes. However, a strategy of management was standardized in our centre, including routine use of corticosteroids after admission as well as optimization of patient status with nutritional support and careful timing of surgery. Second, bleeding of the UCEIS (scored 0–3) was analysed according to the report that contains the colonoscopy performer’s description at the time of the bleeding situation, and this might decrease the accuracy of estimates to some extent, which should be pointed out as a limitation. Third, some patients who met the conditions of the ASC did not have colonoscopy available for UCEIS analyses after admission and therefore were excluded from the study. Finally, a relatively small sample size, which was not adequate to demonstrate significant correlations between some comparators, makes a valid statistical interpretation of postoperative complications difficult. Further work with larger cohorts is needed to confirm these findings. Medication cost (¥) Rescue therapy-related cost Non-rescue therapy-related cost Diagnostics procedures (¥) Surgery-related cost (¥) Hospitalization (¥) Nursery care cost (¥) Overall cost (¥) *Three patients had rescue therapy included; †§Five patients had rescue therapy included In conclusion, the current study revealed that the UCEIS outperformed the MES as a predictor for colectomy in ASC patients. Eighty per cent of ASC patients with UCEIS 7 subsequently needed colectomy, irrespective of medical therapy; also, early colectomy seems to be more cost-effective than late colectomy or prolonged medical therapy. Therefore, for ASC patients with UCEIS 7, a high probability of medical treatment failure and the benefit of early colectomy should be discussed to avoid treatment delay. Funding This study was funded in part by the National Natural Science Foundation of China (81270006) and Jiangsu Provincial Special Program of Medical Sciences, China (BL2012006). Conflict of interest statement: none declared. 1. Laharie D , Bourreille A , Branche J et al. Ciclosporin versus infliximab in patients with severe ulcerative colitis refractory to intravenous steroids: a parallel, open-label randomised controlled trial . Lancet 2012 ; 380 : 1909 - 15 . 2. Bewtra M , Newcomb CW , Wu Q et al. Mortality associated with medical therapy versus elective colectomy in ulcerative colitis: a cohort study . 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Xie, Tingbin, Zhang, Tenghui, Ding, Chao, Dai, Xujie, Li, Yi, Guo, Zhen, Wei, Yao, Gong, Jianfeng, Zhu, Weiming, Li, Jieshou. Ulcerative Colitis Endoscopic Index of Severity (UCEIS) versus Mayo Endoscopic Score (MES) in guiding the need for colectomy in patients with acute severe colitis, Gastroenterology Report, 2018, 38-44, DOI: 10.1093/gastro/gox016