Ulcerative Colitis Endoscopic Index of Severity (UCEIS) versus Mayo Endoscopic Score (MES) in guiding the need for colectomy in patients with acute severe colitis
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
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) [
]. When ASC
arises, the cornerstone of management remains intravenous
(IV) corticosteroids, with a response rate between 57 and 70%
]. 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% [
]. 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 [
], 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 [
]. 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 [
]. 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 [
]. 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
]. 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
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 [
], 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.
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.
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
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.
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.
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.
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)
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
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 [
], 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 [
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
]. 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 [
]. 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 [
]. 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 [
]. Theede et al.
showed that almost all patients with UCEIS 7–8 had fecal
calprotectin >1000 lg/g [
]. Therefore, correlation of the UCEIS with
the need for colectomy seems to be proven indirectly by
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
]. 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 [
]. 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 [
]. 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 (¥)
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.
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.
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