ORIGINAL ARTICLE: GASTROENTEROLOGY
Abdominal X-ray in Pediatric Acute Severe Colitis and
Radiographic Predictors of Response to
Intravenous Steroids
y
Alina Livshits, yzDrora Fisher, yIrith Hadas, yTali Bdolah-Abram, §jjDavid Mack,
ô
Jeffrey Hyams, #Wallace Crandall, Anne M. Griffiths, and yDan Turner
ABSTRACT
Background: Abdominal x-ray (AXR) can identify complications in acute
severe colitis (ASC) and may assist in selecting high-risk children for early
aggressive treatment. We aimed to describe AXR findings in pediatric ASC
and to explore radiological predictors of response to intravenous corticos-
teroid (IVCS) therapy.
Methods: A total of 56 children with ASC were included in a multicenter,
retrospective 1-year cohort study (41% boys, mean age 12.1  4.2).
Radiographs of responders to IVCS and those requiring second-line
salvage therapy by discharge were analyzed independently by 2 blinded
radiologists.
Results: A total of 33 responders to IVCS were compared with 23
nonresponders. The day-3 Pediatric Ulcerative Colitis Activity Index
(PUCAI) score was significantly higher in nonresponders (63  16 vs
46  21, P ¼ 0.001). The mean transverse colon luminal diameter was
30  16 mm in responders and 38  16 mm in nonresponders (P ¼ 0.94).
The upper range of transverse colonic diameter in children <12 years was
40 mm, whereas in older children it was 60 mm as accepted in adults.
Ulcerations and megacolon seen on AXR were associated with nonresponse
to IVCS (P ¼ 0.006 and 0.064, respectively).
Conclusions: The presence of mucosal ulcerations and megacolon on AXR
could be considered in the risk stratification of children with ASC for early
Received April 16, 2015; accepted July 7, 2015.
From the Juliet Keidan Institute of Pediatric Gastroenterology and
Nutrition, Shaare Zedek Medical Center, the yHebrew University of
Jerusalem, Jerusalem, Israel, the zAlder Hey Children’s NHS Foundation
Trust, Liverpool, UK, the §Children’s Hospital of Eastern Ontario IBD
Centre, the jjDepartment of Pediatrics, University of Ottawa, Ottawa,
Canada, the ôConnecticut Children’s Medical Center, Hartford, CT, the
#Nationwide Children’s Hospital, Ohio State University, Columbus, and
the SickKids Hospital, University of Toronto, Toronto, Canada.
Address correspondence and reprint requests to Dan Turner, MD, PhD,
Juliet Keidan Institute of Pediatric Gastroenterology and Nutrition,
Hebrew University of Jerusalem, Shaare Zedek Medical Center, PO
Box 3235, Jerusalem 91031, Israel (e-mail: turnerd@szmc.org.il).
J.H. has served on the advisory board and the speakers’ bureau of Janssen;
the advisory boards of AbbVie and UCB; has been a consultant to
Soligenix, TNI BioTech, Receptos, and Avaxia; and been a speaker for
Merck. D.F. received consultation fees, research grants, royalties, or
honoraria from MSD, Janssen, Pfizer, The Hospital for Sick Children,
Ferring, AbbVie, and Abbott. A.M.G. has received research grants from
Janssen and AbbVie, and is a consultant for AbbVie, Ferring, Janssen,
Nestlé, Nutricia, and Receptos. The participation of A.L. in this study
was performed in fulfillment of her research requirements toward the MD
degree at the Hebrew University Hadassah School of Medicine. The
other authors report no conflicts of interest.
Copyright # 2016 by European Society for Pediatric Gastroenterology,
Hepatology, and Nutrition and North American Society for Pediatric
Gastroenterology, Hepatology, and Nutrition
DOI: 10.1097/MPG.0000000000000910
JPGN  Volume 62, Number 2, February 2016
Copyright 2016 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.
aggressive treatment, together with the previously known day-3 and day-5
Pediatric Ulcerative Colitis Activity Index scores, albumin, and C-reactive
protein.
Key Words: abdominal x-ray, acute severe colitis, intravenous corticos-
teroid therapy, megacolon, ulcerative colitis
(JPGN 2016;62: 259–263)
What Is Known
 Acute severe ulcerative colitis carries a colectomy risk
of 30% and a mortality rate of 1%.
 If no response is documented to intravenous corti-
costeroids within 3 to 10 days, second-line treatment
should be introduced.
 There are almost no data on radiological findings in
children and their value in predicting treatmen fail-
ure.
What Is New

Our study characterized radiological finding in chil-
dren with acute severe colitis.
 Mucosal ulcerations and megacolon were different
between responders and nonresponders.
 We suggest that specific abdominal x-ray parameters
should be considered in predicting the need for
second-line medical therapy.
A
cute severe colitis (ASC) carries a colectomy risk of 30%
and a mortality rate of 1% (1,2). Prompt evaluation and
initiation of aggressive treatment is required while carefully
monitoring improvement on a day-to-day basis. According to the
European Crohn’s and Colitis Organisation–European Society for
Pediatric Gastroenterology, Hepatology, and Nutrition guidelines, a
low threshold should be practiced in ordering plain abdominal x-ray
(AXR) upon admission to identify complications such as mega-
colon and perforation (3). Certain radiographic characters in adults
predict the response to intravenous corticosteroid (IVCS) treatment
in ulcerative colitis (UC), such as transverse colon diameter and
small bowel luminal diameter (4), thereby facilitating early decision
making on commencing second-line medical therapy with calci-
neurin inhibitors or infliximab. Although children develop ASC
more often than adults (5), there is almost no similar data on the
259
 Turner et al
various radiological findings in children and their value in predict-
ing treatment failure. Extremely few small pediatric studies have
described selected AXR features in pediatric ASC including air-
fluid level and free gas, characteristics of mucosal lesions (ulcers
and tags), and transverse bowel width and small bowel involve-
ment, but none explored these features systematically as predictors
of treatment response (6–8).
We therefore aimed to describe the characteristics of AXR
performed during the first 3 hospital days of children with ASC. We
explored the following AXR features selected from the literature:
transverse colon luminal diameter, small bowel luminal diameter,
presence and number of discrete air fluid levels, presence of free
intraabdominal air or air in the portal vein, evidence of pneumatosis
intestinalis, mucosal tags, ulcers, bowel wall thickening, and pro-
nounced haustra. By that, we identified features predictive of
steroid failure, defined as the need for salvage medical therapy
or colectomy by hospital discharge. We hypothesized that the
transverse colon luminal diameter will be associated with treatment
outcome.
METHODS
This multicenter cohort study reports on children from the
prospective OSCI study who underwent AXR during the first
3 days of admission according to the physician’s discretion (9)
and, retrospectively, from searching the electronic database of
Shaare Zedek Medical Center, Jerusalem. The OSCI is a multi-
center study including 128 children who were admitted for IVCS
and reported the short and 1-year outcomes of ASC. It also high-
lighted predicting variables of the need for salvage therapy.
Children (2–18 years) with UC admitted for IVCS treatment for
acute severe flare (ie, Pediatric Ulcerative Colitis Activity Index
[PUCAI] >60 points) (10) were included. Children with Crohn
disease, IBD-unclassified (IBD-U), and infectious colitis (ident-
ified through stool culture and virology) were excluded. Patients
were treated according to the physicians’ discretion. Failure to
respond to IVCS was defined as the need for second-line medical
therapy (ie, calcineurin inhibitors or infliximab) or colectomy by
hospital discharge.
The following data were recorded on standardized case
report forms (prospectively in the OSCI study and retrospectively
in Jerusalem): basic characteristics, medical history, explicit
clinical and laboratory data during the admission including the
PUCAI and the Physician Global Assessment (scored on both 100-
mm visual analogue scale and a Likert scale of remission, mild,
moderate, severe, and fulminant disease), and 1-year outcome after
discharge.
The abdominal radiographs were read independently by 2
senior radiologists, each with >20 years of experience (D.F. and
I.H.), on a standardized data collection form. The radiologists were
blinded to each other’s assessments and to the patient’s clinical data.
The following radiographic variables were selected for scoring after
a systematic literature search: transverse colon luminal diameter
(mean of the 2 radiologists’ assessments), small bowel luminal
diameter, the presence and number of discrete air fluid levels, the
presence of free intraabdominal air or air in the portal vein, evidence
of pneumatosis intestinalis, mucosal tags (ie, pseudopolyps that are
remaining islands of healthy mucosa), ulcers (ie, atrophic mucosa,
appearing on x-ray as dentation of bowel wall), bowel wall thicken-
ing, and pronounced haustra. The diagnosis of ‘‘megacolon’’ was
made by the radiologists taking into consideration not only the
transverse colon luminal diameter but also the consistency of the
bowel mucosa, thickness of the intestinal wall, alterations in
haustral pattern, and the general appearance of the other parts of
the colon.
260
Copyright 2016 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.
JPGN  Volume 62, Number 2, February 2016
Statistical Analysis
Data are presented as means  standard deviation, medians
(interquartile range), and proportions (95% confidence interval
[CI]), as appropriate. Unpaired data were compared using x2, Fisher
exact, and Student t test or Wilcoxon rank sum test, as appropriate.
The Pearson correlation coefficient was calculated for assessing the
strength of the linear association between quantitative variables.
The agreement between the radiologists was assessed using the
intraclass correlation coefficient, using Shrout and Fleiss (11) 2,1
2-way random analysis of variance model  95% CI for continuous
variables and k statistics for discrete variables. Prediction utility of
the radiographic parameters is reflected by sensitivity, specificity,
positive and negative predictive values, and odds ratio. Compari-
sons were made using 2-sided significance levels of P < 0.05 but
given the small sample size, we also highlighted comparisons with
P < 0.075 as being marginal. Statistical analyses were performed
using SPSS version 22.0 (IBM SPSS Statistics, Armonk, NY). The
study was approved by the institutional research ethics board of
each participating center.
RESULTS
There were 56 children who met the eligibility criteria and
were included in this study, among whom 33 (59%) responded to
IVCS and 23 (41%) did not respond and went on to second-line
medical therapy (37 from the OSCI study of the original 128
children). Responders were younger and had a lower PUCAI score
at day 3 (Table 1). Of the 23 nonresponders, 19 (83%) received
infliximab of whom 5 proceeded to colectomy by discharge. Four
(17%) underwent colectomy without prior second-line medical
therapy. A further 3 (13%) children underwent colectomy within
the first year after discharge, bringing the 1-year colectomy rate in
the entire cohort to 21%.
There was good-to-excellent agreement between the 2 radi-
ologists. The intraclass correlation coefficient was 0.95 (95% CI
0.92–0.97) for transverse colon luminal diameter and 0.91 (95% CI
0.85–0.95) for small bowel luminal diameter. The k statistic was
0.70 (P < 0.001) for the presence of ulcers, 0.85 (P < 0.001) for
the presence of mucosal tags, 0.90 (P < 0.001) for the number of
air fluid levels counted, and 0.92 (P < 0.001) for bowel wall
thickening.
Mucosal ulcerations and megacolon were different or mar-
ginally different between responders and nonresponders (Table 2
and Fig. 1). Mucosal tags were also numerically different but did not
reach statistical significance. No abdominal radiograph in either
group displayed evidence of portal venous air or pneumatosis
intestinalis. Evidence of radiological megacolon was subjectively
defined by the radiologists’ general impression of the bowel
appearance and was only demonstrated in 3 (5%) patients. These
3 patients (all >11 years of age) had transverse colon diameter
measurement of 50 mm each, bowel wall thickening, and other
findings such as pronounced haustra, ulcers, and mucosal tags.
Clinical signs, mandatory for the diagnosis of toxic megacolon,
such as fever, tachycardia, and anemia (12) were not present in any
of the 3 patients. All of the 3 patients failed second-line therapy with
infliximab and eventually underwent colectomy, 1 during the
admission, and 2 in the subsequent 3 months.
A total of 6 patients had a transverse colon luminal diameter
that exceeded 50 mm, of whom 3 failed IVCS (Fig. 2A). The
presence of AXR ulcers was associated with the transverse colon
luminal diameter; those with ulcers had a width of 45  17 mm as
compared with 31  15 mm in those without (P ¼ 0.03). Seven of
the 10 (70%) children with mucosal tags and 7 of the 8 (88%)
children with the evidence of ulcerations on AXR failed IVCS and
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 JPGN  Volume 62, Number 2, February 2016 Abdominal X-Ray in Pediatric Acute Severe Colitis

TABLE 1. Patient characteristics stratified by response to IVCS; IQR or SD are presented as appropriate

Entire cohort (n ¼ 56) Responders (n ¼ 33) Nonresponders (n ¼ 23) P

Age at diagnosis, y 12.1  4.2 10.5  4.5 13.8  3.9 0.07

Sex (male, %) 23 (41) 14 (42) 9 (39) 0.805
Reason for admission
First attack (%) 19 (34) 9 (27) 10 (43) 0.208
Exacerbation (%) 37 (66) 24 (73) 13 (57)
Admission time, days 15 (2–27) 11 (3–22) 19 (1–33) <0.001
Disease duration, mo 28 (0–85) 29 (0–102) 28 (0–68) 0.795
Disease extent 0.172
Pancolitis (%) 46 (82) 25 (76) 21 (91)
Left-sided (%) 10 (18) 8 (24) 2 (8)
No. patients treated with opioids (%) 6 (11) 2 (6) 4 (17) 0.215
Daily IVCS dose, mg/kg 0.9 (0.8–1.1) 1 (0.8–1.4) 0.9 (0.7–1) 0.05
PGA at admission, 100-mm VAS 80  14 78  13 82  15 0.315
PUCAI at admission 73  11 70  12 75  10 0.104
PUCAI on hospital day 3 55  19 46  21 63  16 0.001
Remission, <10 (%) 2 (3) 2 (6) 0
Mild disease, 10–34 (%) 9 (16) 8 (24) 1 (4)
Moderate disease, 35–64 (%) 20 (36) 13 (40) 7 (30)
Severe disease, 65 (%) 25 (45) 10 (30) 15 (66)

IQR ¼ interquartile range; IVCS ¼ intravenous corticosteroids; PGA ¼ Physician Global Assessment; PUCAI ¼ Pediatric Ulcerative Colitis Activity Index;
VAS ¼ visual analogue score.

proceeded to second-line therapy, yielding sensitivity, specificity,
positive and negative predictive values of 70%, 65%, 30%, and
90%, respectively, and 88%, 67%, 30%, and 97%, respectively,
with odds ratio of 4.3 (95% CI 1.01–19.2) and 12.6 (95% CI
1.4–112) respectively, to predict steroid failure.
The upper range of transverse colon luminal diameter in
children >12 years was 60 to 70 mm, whereas children <12 years of
age seldom exceeded 35 to 40 mm (Fig. 2A). There was no clear
age-specific distribution of the small bowel luminal diameter
(Fig. 2B).
One dose of opioids (ie, morphine) was administered to
4 patients (2 responders of ages 13 and 14, and 2 nonresponders
of ages 13 and 16) with doses ranging 1 to 6 mg. Among the
nonresponders, the transverse colon and small bowel luminal
diameter of the 2 children treated with opioids were 34 and
20 mm, respectively, compared with 40  19 and 20  9 mm in
nonresponders, who did not receive opioids. Similarly, among the
responders, the corresponding figures in the 2 children treated with
opioids were 10 and 5 mm compared with 32  15 and 19  11 mm
in the nonopioid responders.
DISCUSSION
This study aimed to explore whether radiographic charac-
teristics at baseline could identify children likely to fail IVCS
therapy early in the admission and require second-line medical
therapy (ie, calcineurin inhibitors or infliximab) or colectomy by
hospital discharge, in addition to the known predictors in children
(primarily PUCAI score, albumin. and CRP) (5). This may mini-
mize futile steroid treatment and shorten time to other effective
treatment. We found that 70% of the patients with mucosal tags and
88% of the patients with ulcers detected on plain AXR failed to
respond to IVCS therapy. Although mucosal tags were numerically
but not statistically different between the groups, this is likely given
the small sample size (post hoc power calculation for this parameter
has been calculated as 71%). The presence of megacolon, judged by
the radiologist based on transverse colon luminal diameter with

TABLE 2. Abdominal radiographic findings in children admitted with ASC

Entire cohort (n ¼ 56) Responders (n ¼ 33) Nonresponders (n ¼ 23) P


Evidence of megacolon (%) 3 (5) 0 3 (13) 0.064
Mean transverse colon luminal diameter, cm 3.42  1.62 3.04  1.64 3.8  1.6 0.94
Mean small bowel luminal diameter, cm 1.91  1.1 1.8  1.28 2.03  0.92 0.455
Presence of air fluid levels (%) 38 (68) 25 (76) 13 (56) 0.129
Number of air fluid level 18  1.3 8  1.65 10  1.12 0.203
Presence of free air (%) 3 (5) 1 (3) 2 (8) 0.562
Presence of air in the portal vein 0 0 0 1.0
Presence of pneumatosis intestinalis 0 0 0 1.0
Presence of mucosal tags (%) 10 (18) 3 (9) 7 (30) 0.073
Presence of ulcerations (%) 8 (14) 1 (3) 7 (30) 0.006
Presence of bowel wall thickening (%) 23 (41) 12 (36) 11 (47) 0.391
Presence of pronounced haustra (%) 17 (30) 9 (27) 8 (34) 0.548

ASC ¼ acute severe colitis.


According to the radiologist’s impression (see text for description).

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 Turner et al JPGN  Volume 62, Number 2, February 2016

A B C

FIGURE 1. Plain AXR parameters. A, Mucosal tags (arrows) in a 13-year-old girl. B, Bowel wall thickening and ulcerations (dentation of the bowel
wall) (arrows) in a 14-year-old girl. C, Transverse bowel wall thickening and ulcerations (arrows) in a 10-year-old boy. AXR ¼ abdominal x-ray.

accompanied mucosal abnormalities, was rare and appeared only in
the nonresponders group. Unlike our a priori hypothesis and
previous adult studies, isolated transverse colon and small bowel
luminal width did not predict the outcome in this study. Other
radiological findings such as air fluids and bowel wall thickening
did not differ between responders and nonresponders, whereas
portal venous air and pneumatosis intestinalis were not documented
in our cohort.
The presence of ulcers and mucosal tags on AXR in adult
case reports is reported to be associated with poor outcome. Miller
(13) reported 2 patients with irregularities of the bowel wall on
AXR on day 4 of admission who underwent colectomy by dis-
charge. Werbeloff et al (14) reported the case of a patient with ASC
who had mucosal tags and megacolon on AXR, eventually requiring
colectomy and subsequently dying a month after discharge. Another
case series reported the utility of mucosal tags similar to our results;
8 of the 10 SC adult patients (80%) who had tags on AXR failed
IVCS treatment and required colectomy (15).
Studies in adults demonstrated that transverse colon luminal
diameter may predict the response to IVCS therapy (4,15,16). In
children, toxic megacolon (ie, megacolon with toxic clinical signs
and symptoms) has been previously associated with a 70% rate of
IVCS failure (3). Moreover, we did not observe an association
between bowel luminal diameter without the evidence of toxic
syndrome and response to corticosteroid therapy. It is possible that
the pediatric population is different from adults in that regard given
the age-dependent variations. Nonetheless, similar to our previous
published observation, where transverse colon luminal diameter in
children >11 years of age resembled the distribution found in
adults and that the diameter was not predictive of response to IVCS
(3,5), we found here that the upper range for colonic luminal
diameter in children <12 years is 40 mm, whereas older children
follow adult distribution with 60 mm still may be considered
normal (5,16–18).
The use of narcotic analgesia in patients with ASC is
considered controversial, given the theoretical risk for bowel
dilatation and perforations (19–23). In our study, 4 patients
received 1 dose of opioids before performing AXR, neither of
whom demonstrated radiographic or clinical features of megacolon.
This small sample of patients limits our ability to draw any
conclusion regarding the safety of these drugs in children with
ASC, but other manuscripts refer to this clinical dispute (3,12,24).
In conclusion, AXR features may have predictive merit in
pediatric ASC in addition to identifying complications. The knowl-
edge of the specific AXR criteria including mucosal tags, ulcers,
and megacolon at the different ages by radiologists and gastro-
enterologists providing care for children and youth with ASC may
aid in deciding when to initiate second-line medical therapy. The

A Transverse colon luminal diameter B Small bowel luminal diameter

20 20

18 18

16 16

14 14

12 12
Age, y
Age, y

10 10
Responders Responders
8 Nonresponders
8 Nonresponders

6 6

4 4

2 2
0 0
0 10 20 30 40 50 60 70 0 10 20 30 40 50 60
Transverse colon luminal diameter mm Small bowel luminal diameter mm

FIGURE 2. Radiographic appearance of pediatric ASC. A, Distribution of transverse colon luminal diameter according to age. Arrows pointing at 3
children diagnosed as having toxic megacolon; mean transverse colon luminal diameter 3.04  1.64 cm in responders versus 3.8  1.6 cm in
nonresponders (P ¼ 0.94). B, Distribution of small bowel luminal diameter according to age; mean small bowel luminal diameter 1.8  1.28 cm in
responders versus 2.03  0.92 in nonresponders (P ¼ 0.455). ASC ¼ acute severe colitis.

262 www.jpgn.org

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 JPGN  Volume 62, Number 2, February 2016
upper range of transverse colonic width in children <12 years is
40 mm, whereas older children follow the 60-mm range accepted
in adults. Precisely, how radiographic features should be incorp-
orated in the risk stratification of children with ASC, together with
day-3 and day-5 PUCAI scores, albumin, and C-reactive protein (5)
will need a further study.
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