Narrow Band Imaging for Detection of Dysplasia

in Colitis: A Randomized Controlled Trial

Ana Ignjatovic, MD1,2, James E. East, MD1,2, Venkat Subramanian, PhD3, Noriko Suzuki, MD1, Thomas Guenther, PhD4, Nicky Palmer1,
Paul Bassett, BSc5, Krish Ragunath, MD3 and Brian P. Saunders, MD1
OBJECTIVES:

In ulcerative colitis surveillance, chromoendoscopy improves dysplasia detection 35-fold compared

with white light endoscopy (WLE). The aim of this study was to investigate whether narrow band
imaging (NBI) can improve dysplasia detection compared with WLE.

METHODS:

This was a randomized, parallel-group trial. A total of 220 patients were needed to be recruited
to detect a threefold increase in dysplasia detection. In all, 112 patients with long-standing
ulcerative colitis were randomized to colonoscopic extubation with NBI (56) or WLE (56) (1:1 ratio)
at two tertiary endoscopy units in the United Kingdom. Targeted biopsies of suspicious areas and
quadrantic random biopsies every 10 cm were taken in both groups. The primary outcome measure
was the proportion of patients with at least one area of dysplasia detected. In a prespecified
mid-point analysis, the criteria for trial discontinuation were met and the trial was stopped and
analyzed at this point.

RESULTS:

There was no difference in the primary outcome between the two groups, with 5 patients having at
least one dysplastic lesion in each group (odds ratio (OR) 1.00, 95% confidence interval (95% CI)
0.273.67, P = 1.00). This remained unchanged when adjusted for other variables (OR 0.69, 95%
CI 0.162.96, P = 0.62). Overall, dysplasia detection was 9% in each arm. Yield of dysplasia from
random nontargeted biopsies was 1/2,707 (0.04%).

CONCLUSIONS: Overall, in this multicenter parallel-group trial, there was no difference in dysplasia detection when

using NBI compared with high-definition WLE colonoscopy. Random background biopsies were
ineffective in detecting dysplasia.
Am J Gastroenterol 2012; 107:885890; doi:10.1038/ajg.2012.67; published online 22 May 2012

INTRODUCTION
Patients with long-standing ulcerative colitis (UC) have an
increased risk of dysplasia and colorectal cancer (CRC), with
cumulative incidence reported to be 7.7% at 20 years and 15.8% at
30 years after the onset of colitis (1,2). Colonoscopic surveillance
of these patients has been shown to improve survival from CRC
by detecting it at an earlier stage (3), and hence guidelines recommend for it to start 10 years after the onset of symptoms (4,5).
Dysplastic lesions in UC are often flat and subtle and easy to miss
with conventional colonoscopy, as demonstrated by a recent study
where 16 out of 30 cancers detected during the surveillance program were interval cancers (1). Therefore, most guidelines suggest
that, in addition to targeted biopsies, random quadrantic biopsies
should be taken every 10 cm at surveillance colonoscopy. The use

of random biopsies originates from a time when endoscopic resolution was much poorer than with modern instruments, and it has
been proposed that untargeted biopsies should be abandoned as
each individual biopsy only samples 0.03% of the colonic mucosal
surface, and that time should be spent on closer inspection and
dye-spraying, with a targeted biopsy approach (6).
Chromoendoscopy has been shown to improve dysplasia detection in colitis (Rutter et al. (7) no. 198; and Kiesslich et al. (8)
no. 362; (9)); however, it is time consuming, increasing the procedure time, and even when performed with specially designed dye
spray catheters, complete and even mucosal dye coverage is not
guaranteed (10,11).
Narrow band imaging (NBI), on the other hand, is easily activated
at a push of a button and provides complete mucosal enhancement.

1
Wolfson Unit for Endoscopy, St Marks Hospital, Harrow, UK; 2Translational Gastroenterology Unit, John Radcliffe Hospital, Oxford, UK; 3Wolfson Digestive Diseases
Centre, Nottingham University Hospitals NHS Trust, Nottingham, UK; 4Department of Academic Pathology, St Marks Hospital, Harrow, UK; 5Statsconsultancy,
Amersham, UK. Correspondence: Ana Ignjatovic, MD, Translational Gastroenterology Unit, Experimental Medicine Division, Nuffield Department
of Clinical Medicine, University of Oxford, John Radcliffe Hospital, Headley Way, Headington, Oxford OX3 9DU, UK. E-mail: anaignjatovic@me.com
Received 3 November 2011; accepted 3 February 2012

2012 by the American College of Gastroenterology

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ORIGINAL CONTRIBUTIONS

nature publishing group

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Ignjatovic et al.

As the relative contribution of red light is decreased, NBI highlights in particular the mucosal vascular pattern and could lead to
a more accurate diagnosis of dysplasia in colitis (12,13). To date,
three randomized, crossover studies, but no parallel-group trials,
have assessed the effectiveness of NBI for dysplasia detection in
UC (1416). In the study by Dekker et al. (14), a prototype NBI
system did not improve dysplasia detection when compared with
standard white light endoscopy (WLE). The same group then went
on to compare high-definition NBI with high-definition WLE and
again could not demonstrate improved dysplasia detection with
NBI (15). Pellise et al. (16) compared high-definition NBI with
high-definition chromoendoscopy and found similar rates of dysplasia detection between the two techniques. However, NBI had a
higher, although not statistically significant, neoplasia miss rates
(i.e., high specificity but low sensitivity), leading the authors to
recommend chromoendoscopy as the technique of choice for
detecting dysplasia in colitis.
The aim of this prospective, multicenter, randomized, parallel-group trial was to compare NBI with WLE for dysplasia
detection in patients undergoing surveillance colonoscopies for
long-standing UC.

METHODS
Participants

Consecutive patients with long-standing colitis scheduled for

a surveillance colonoscopy with one of four colonoscopists at
St Marks hospital (J.E.E., B.P.S., N.S., and A.I.) and two at Queens
Medical Centre (K.R. and V.S.) between May 2006 and May
2010 were invited to participate. The inclusion criteria were an
objective diagnosis of left-sided or pancolitis (endoscopic and
histological), disease duration of >8 years for pancolitis and >10
years for left-sided colitis, with evidence of histological inflammation at the previous colonoscopy. Because of slow recruitment,
the last inclusion criterion was abolished after 40 patients had
been recruited. Exclusion criteria were age 18 years, inability
or unwillingness to consent to the procedure, and severe active
colitis (endoscopist assessment). All patients gave informed consent and the study was approved by the Brent Research Ethics
Committee (06/Q0408/10).
Study design and randomization

This was a randomized parallel trial in which patients were randomized in a 1:1 ratio to a withdrawal with WLE or NBI. Randomization results obtained using a computer-generated sequence
were kept in sealed opaque envelopes that were opened by the
research nurse once the cecum had been reached.

the procedure or on reaching the cecum, with additional antispasmodic given at the discretion of the endoscopist. WLE was used
for intubation in all colonoscopies and no biopsies were taken
during insertion, although care was taken to wash and suction any
residual stool. Cecal intubation was confirmed by identification of
all three anatomical landmarks: the triradiate fold, the ileocecal
valve, and the appendiceal orifice. Assessment of bowel preparation was made once the cecum was reached as follows: good (only
liquid stool present removable with suction), adequate (some
semi-formed stool obscuring < 10% of the mucosa after suction),
and poor (>10% of the mucosa obscured by solid stool after suction). Patients with poor bowel preparation were excluded from
the study.
The Olympus Lucera Spectrum video endoscopy system
with high-definition colonoscopes was used for all cases (XCFH240FZL/I and CF-H260AZL video colonoscopes, XCLV-260HP
xenon light source and XCV-260HP video system center; Olympus,
Tokyo, Japan; NBI filters: blue, centered on 415 nm; green, centered on 540 nm). Output was to a high-definition 1080i (i.e. 1,080
lines of vertical resolution), 14-inch monitor (OEV181H, Olympus). The colon was examined segmentally, with targeted biopsies
or definite resection (snare polypectomy or endoscopic mucosal
resection) of any suspected dysplastic lesions. Areas suspicious
for dysplasia were defined as any mucosal irregularity, stricturing, or ulceration not consistent with active or chronic UC as seen
with WLE. In addition to these, suspicious lesions on NBI were
defined as those with increased vascular intensity and Kudo pit
pattern IIIV. The size (measured against open biopsy forceps),
position (colonic segment), shape (Paris classification), and endoscopic diagnosis were recorded for each lesion. Once a lesion was
resected, quadrantic biopsies from the surrounding mucosa were
taken. Targeted biopsies were sent to histopathology in a separate
pot. In both arms of the study, random, nontargeted quadrantic
biopsies were taken every 10 cm on withdrawal and the number of
suspicious lesions; the number of targeted biopsies and withdrawal
times were recorded.
Histopathological evaluation

Three pathologists, at least one of whom is considered an expert

in the field, assessed all the samples and classified them according to the Vienna classification, ranging from no intraepithelial
neoplasia to invasive neoplasia (17). The expert pathologist provided a second review of all dysplastic lesions. Neoplastic lesions
were classified as low-grade, high-grade, and invasive neoplasia;
those classified as indefinite for neoplasia were not considered
neoplastic.
Primary and secondary outcomes

Colonoscopic protocol

Patients were prepared with Senna and two sachets of magnesium

citrate (Citramag, Sanochemia, Vienna, Austria) or 4 liters of
PEG solution (Klean-Prep, Norgine, Harefield, Middlesex, UK).
Colonoscopies were performed with patients unsedated or under
conscious sedation using midazolam and pethidine. Patients were
given 20 mg of intravenous hyoscine butylbromide at the start of
The American Journal of GASTROENTEROLOGY

The primary end point of this study was the number of patients
with at least one dysplastic lesion detected (defined as at least
low-grade dysplasia). The secondary end points were the total
numbers and the number of patients with dysplastic, suspicious,
and false-positive lesions.
For conventional white light colonoscopy, based on previous
studies (8), we assumed the dysplasia detection rate of 7%. With a
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Statistical methods

Data were represented by their means (s.d.) or medians

( + interquartile range) as appropriate. Categorical variables were
compared using Fishers exact test. Continuous variables were
compared using unpaired t-test or MannWhitney test as appropriate. Binary outcomes were compared using logistic regression.
Count variables were compared using Poisson regression, as they
could not be transferred to a more normal distribution. Outcomes
were subsequently adjusted for withdrawal time, family history of
CRC, and previous history of a dysplastic lesion.
Interim analysis was planned at the halfway point (i.e., 55 in
each arm), and if the assumptions of the original power calculation were not met, the trial would be stopped. As the proportion
of patients with dysplasia in each arm was identical at the halfway point, with the trial size originally powered to detect at least a
threefold change, following statistical advice the trial was stopped.
Significant extension of recruitment to detect a smaller change was
not feasible.
A two-sided P value of < 0.05 was considered significant. Analyses were done using Stata statistical package, version 9.2 (StataCorp. 2005. Stata Statistical Software: Release 9. College Station,
TX: StataCorp LP). This study was reported according to the
CONSORT guidelines (18) and is registered with ClinicalTrials.
gov identifier NCT00292175.

RESULTS
Participants

Between May 2006 and May 2010, 119 patients were identified
and fulfilled the inclusion criteria, of whom 112 were randomized in a 1:1 ratio to undergo extubation with either WLE or
NBI. All 112 patients (56 in each arm) completed the study protocol. None of the participants experienced complications. Six
experienced colonoscopists performed all the procedures, with
two performing the majority of colonoscopies (n = 88). There
was no significant difference between the number of white light
and NBI examinations performed by each of the six colonoscopists (P = 0.54).
Baseline characteristics for patients who completed the trial are
demonstrated in Table 1; Figure 1).
Detection of dysplasia in targeted biopsies

The median extubation time for NBI was 11.5 min compared with
10 min for WLE (P = 0.01). A total of 32 targeted biopsies were
taken during extubation with NBI and 16 during withdrawal with
WLE. In the NBI arm, there were 17 suspicious lesions detected in
13 patients (Tables 2 and 3).
2012 by the American College of Gastroenterology

Table 1. Baseline characteristics of patients who completed

the trial
WLE, n=56

NBI, n=56

P value

52 (11)

53 (14)

0.70

31 (55%)

34 (61%)

0.70

UC duration, years,
median (IQR)

21 (1530)

21 (1528)

0.86

Withdrawal time,
min, median (IQR)

10.0 (8.6 12.4)

11.5 (9.5 14.2)

0.01

Pancolitis (E3)

51

45

0.18

Left sided (E2)

11

History of dysplasia,
n (%)

3 (5%)

6 (11%)

Mean age, years (s.d.)

Male, n (%)

Extent of colitis

History of PSC, n (%)

0.49

2 (4%)

2 (4%)

1.00

Maintenance 5ASA,
n (%)

29 (52%)

27 (48%)

0.85

Maintenance
sulphasalazine, n (%)

13 (23%)

12 (21%)

1.00

Maintenance
azathioprine, n (%)

13 (23%)

13 (23%)

1.00

Family history of CRC

7 (13%)

7 (13%)

1.00

Good

12 (21%)

17 (30%)

Adequate

44 (79%)

39 (70%)

Bowel preparation

0.38

CRC, colorectal cancer; IQR, interquartile range; NBI, narrow band imaging;
PSC, primary sclerosing cholangitis; 5ASA, 5-aminosalicylic acid; UC, ulcerative
colitis; WLE, white light endoscopy.

Histopathology confirmed 5 dysplastic lesions in 5 patients (all

5 low-grade dysplasia). Remaining lesions were inflammatory
(n = 7), normal mucosa (n = 4), or a hyperplastic polyp (n = 1). In
the WLE arm, 11 suspicious lesions were detected in 8 patients
and 7 lesions (in 5 patients) were neoplastic (low-grade dysplasia,
n = 5 and high-grade dysplasia, n = 2). The false-positive lesions
were inflammatory (n = 1), indefinite for dysplasia (n = 1), reactive
(n = 1), and inflammatory (n = 1). The phenotype of the true- and
false-positive lesions is shown in Table 4.
In addition, there was no difference between the two arms when
the outcomes were adjusted for withdrawal time, family history of
CRC, or previous history of a dysplastic lesion.
Detection of dysplasia in nontargeted random biopsies

In the NBI arm, 1,348 random biopsies were taken (mean per
patient, n = 25, s.d. 6.3), and histopathology revealed low-grade
dysplasia in 1 biopsy (from 1 patient). This patient had a dysplastic lesion already detected by targeted biopsies in ascending
colon (random biopsies detected dysplasia in sigmoid colon).
However, no further dysplastic lesions were detected in this
patient during 4 years of colonoscopic surveillance. During
withdrawal with WLE, 1,359 random biopsies were taken (mean
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power (1-) of 80% and a significance level of 5%, n = 220 patients

(110 in each arm) were required to detect a threefold difference in
the primary end point, from 7 to 21% (based on chromoendoscopy
studies) (7). Interim analysis was preplanned at the halfway point
(i.e., 55 in each arm). The trial was powered for primary outcome
measure and all others should be considered as exploratory or
hypothesis generating.

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Ignjatovic et al.

per patient, n = 24, s.d. 5.7) and none were found to harbor dysplasia. Yield of dysplasia from random nontargeted biopsies was
1/2,707 (0.04%).

leading to a darker image, insufficient to obtain a good overview

of mucosal surface. The second study by the same group (15)
compared new-generation NBI with high-definition white light
colonoscopy and again could not demonstrate improved dysplasia detection with NBI. However, both of these studies found
a much higher rate of dysplasia when using white light alone
(1719%) compared with dysplasia detection rates found in the
older chromoendoscopy studies (7.5%) (8). The factors likely to
have contributed to this higher dysplasia detection rates include
a high proportion of patients with primary sclerosing cholangitis included in the studies as well as the improved resolution
obtained with modern conventional white light colonoscopy.
The prevalence of dysplasia in our study of 9% in both arms is
more comparable to the historical data. Our original inclusion
criteria, necessitating the presence of histological inflammation
at the prior colonoscopy, aimed to identify high-risk patients
more likely to have dysplasia; however, because of slow recruitment this inclusion criterion was abolished after 40 patients
were recruited. Therefore, patients finally included in the study
fulfilled the same criteria as those in previously published studies (14,15).
Factors such as duration of the disease, previous history of
dysplasia, and family history of CRC and primary sclerosing
cholangitis have been associated with increased risk of dysplasia
in patients with UC, whereas the use of maintenance mesalazine
has been found to reduce the risk of dysplasia (19,20). In this study
there was no significant difference between the two arms with
regard to increased risk factors for dysplasia, and consequently
no significant difference in the primary outcome when data were
adjusted for withdrawal time, family history of CRC, or a previous history of dysplasia, although the number of dysplastic lesions
detected in total was small.
Most national guidelines on surveillance colonoscopy for
patients with long-standing UC recommend that quadrantic random biopsies should be taken every 10 cm to improve detection of
dysplasia. The most recent guideline from British Society of Gastroenterology (4) advises the use of chromoendoscopy with targeted biopsies as the preferred method of surveillance, although,
if not available, the usual random biopsies should be taken. The
yield of dysplasia from random nontargeted biopsies in this study
was 0.04%, and the only random biopsy that showed low-grade
dysplasia was detected in the patient who already had a dysplastic
lesion detected with a targeted biopsy. In addition, the long-term
outcome of low-grade dysplasia on a single biopsy in UC is not

DISCUSSION
This is the third randomized, but the first parallel-group, multicenter study comparing WLE and NBI for detection of dysplasia
in patients with long-standing UC. The results of this study show
that using NBI does not appear to lead to higher detection rates
of patients with dysplasia compared with WLE (five patients with
dysplasia detected in both arms). Using NBI appeared to lead to
detection of more suspicious lesions (17 for NBI vs. 11 for WLE),
and although there was a trend for more false-positive lesions
detected in NBI arm (12 vs. 4 for WLE) this was not statistically
significant.
This is in agreement with two other studies published on the
use of NBI in dysplasia detection in UC. Although the other
two studies used a different methodology of delayed crossover
design, they both showed no increase in detection of dysplasia when using NBI. The first study (14) attributed the lack of
improved detection with NBI to the fact that a first-generation
prototype NBI was used that provided reduced light intensity

119 Offered
participation
Excluded (n = 7)
2 Failed colonoscopy
2 Declined to
participate
3 Other reasons

112 Randomised

56 NBI

56 WLE

Figure 1. Participant flow through the trial. NBI, narrow band imaging;
WLE, white light endoscopy.

Table 2. Per-patient comparisons of the primary and secondary outcomes

NBI (n =56)

WLE (n =56)

Adjusted OR (95% CI)a

P value

True-positive lesions

0.69 (0.16 2.96)

0.62

Suspicious lesions

13

1.48 (0.51 4.25)

0.47

False-positive lesions

2.01 (0.53 7.68)

0.31

Number of patients with

CI, confidence interval; NBI, narrow band imaging; OR, odds ratio; WLE, white light endoscopy.
a

Adjusted for withdrawal time, family history of colorectal cancer (CRC), and past history of dysplasia.

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Number of lesions

NBI

WLE

Adjusted OR (95% CI)

P value

True-positive lesions

0.71 (0.23 2.25)

0.57

Suspicious lesions

17

11

1.55 (0.72 3.30)

0.26

False-positive lesions

12

3.00 (0.97 9.30)

0.06

CI, confidence interval; NBI, narrow band imaging; OR, odds ratio; WLE, white light endoscopy.

Table 4. Shape (Paris classification) of true- and false-positive

lesions
NBI

WLE

P value

0.57

0-IIa

1.00

0-Is

1.00

DALM

0.24

12

0-IIa

0.57

0-IIb

1.00

0-Is

0.11

0-Ip

1.00

True-positive
lesions

False-positive
lesions

DALM, dysplasia-associated lesion or mass; NBI, narrow band imaging; WLE,

white light endoscopy.

clear, and indeed this patient had no further dysplasia detected

during 4 years of colonoscopic surveillance. This level of dysplasia detection is low enough that serious consideration should be
given to abandoning nontargeted random biopsies in patients
with UC.
This study has a number of limitations. NBI was compared
with WLE and not chromoendoscopy, which many national guidelines now recommend as the gold standard surveillance strategy.
However, the dysplasia detection achieved with white light in
this study is comparable to that historically achieved when using
chromoendoscopy, suggesting an effect of improved resolution of
standard white light colonoscopy. In this study, the withdrawal was
done by using either WLE or NBIit is possible that using WLE
and NBI would result in higher rate of dysplasia detection than
using either technique on its own.
Power calculation for a parallel, randomized, controlled trial
necessitated inclusion of a large number of subjects, but a priori
decision was made to stop the trial early if assumptions of power
calculation were not met. At half-way point, there was no difference in dysplasia detection between WLE and NBI, with odds
ratio (OR) 0.69 (95% confidence interval (95% CI) 0.162.96)
suggesting that NBI was less likely to detect dysplasia than WLE
with CIs that were < 3, which was the basis of original power
2012 by the American College of Gastroenterology

calculation. The recruitment into the study was slow and any
further recruitment would have been protracted and unlikely to
detect the differences as specified in the original power calculation.
Although this study that included 112 patients represents the largest study to date on the use of NBI for dysplasia detection in UC, it
is possible that a smaller, real, and clinically important difference
between NBI and WLE does in fact exist, but the study was not
powered to detect it.
It appears that NBI is unlikely to have a role in dysplasia detection. Other narrow-spectrum technologies such as FICE and
iSCAN have not been formally studied in this setting, but like
NBI they are unlikely to lead to improved detection of dysplasia.
High-definition white light may in fact be as good as chromoendoscopy and warrants a formal comparative study in a multicenter setting.
NBI may aid lesion characterization, although as in the previous
studies, our study demonstrated a trend for more false-positive
lesions detected with NBI increasing the number of biopsies taken
at colonoscopy. There was no difference in the phenotype of the
false-positive lesions detected with WLE and NBI. However, the
number of false-positive findings may be reduced combining NBI
with other imaging tools (e.g., autofluorescene) (21). In a study
of endoscopic trimodal imaging (21), sensitivity, specificity, and
overall accuracy of NBI for characterization of neoplasia were 0.75
(95% CI 0.510.90), 0.81 (0.710.88), and 0.80 (0.710.86), with
relatively poor positive predictive value of 0.43, but the combined
use of NBI and automated function imaging could have prevented
taking targeted biopsies of 60% of lesions.
In conclusion, this study, although underpowered, could not
demonstrate improved dysplasia detection as specified in the
power calculation by using NBI when compared with conventional
white light colonoscopy. Further work should compare NBI with
chromoendoscopy for detection of dysplasia using randomized,
crossover, back-to-back study design.
CONFLICT OF INTEREST

Guarantor of the article: Ana Ignjatovic, MD.

Specific author contributions: J.E.E., B.P.S., and A.I. designed and
planned the study; J.E.E., B.P.S., N.S., V.S., K.R., N.P., and A.I. collected the data; A.I., J.E.E., T.G., and P.B. interpreted the data. All
authors contributed to and approved the final manuscript.
Financial support: A.I. was funded by the Leigh family Trust who
had no role in the design or conduct of the study.
Potential competing interests: None.
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INFLAMMATORY BOWEL DISEASE

Table 3. Per-lesion comparison between NBI and WLE arms

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Ignjatovic et al.

INFLAMMATORY BOWEL DISEASE

Study Highlights
WHAT IS CURRENT KNOWLEDGE

3In ulcerative colitis surveillance, by enhancing mucosal

contrast, chromoendoscopy improves dysplasia detection
35-fold when compared with white light colonoscopy.

3Narrow band imaging (NBI) improves contrast for superficial

microcapillaries and hence might also improve dysplasia
detection compared with white light colonoscopy.

3NBI has not been shown to improve dysplasia detection in

back-to-back studies, but no randomized, parallel-group
trials have been performed.

WHAT IS NEW HERE

3There was no difference in dysplasia detection between NBI

and white light in this study.
3The yield of dysplasia from nontargeted random biopsies
was negligible.

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