Digestive Endoscopy 2016; 28: 260–265 doi: 10.1111/den.

12505

Review

Surveillance colonoscopy for colitis-associated dysplasia and

cancer in ulcerative colitis patients
Keisuke Hata, Junko Kishikawa, Hiroyuki Anzai, Takahide Shinagawa, Shinsuke Kazama,
Hiroaki Ishii, Hiroaki Nozawa, Kazushige Kawai, Tomomichi Kiyomatsu, Junichiro Tanaka,
Toshiaki Tanaka, Takeshi Nishikawa, Kensuke Otani, Koji Yasuda, Hironori Yamaguchi,
Soichiro Ishihara, Eiji Sunami, Joji Kitayama and Toshiaki Watanabe
Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan

Long-standing ulcerative colitis patients are known to be at high risk
for the development of colorectal cancer. Therefore, surveillance
colonoscopy has been recommended for these patients. Because
colitis-associated colorectal cancer may be difficult to identify even
by colonoscopy, a random biopsy method has been recom-
mended. However, the procedure of carrying out a random biopsy
is tedious and its effectiveness has also not yet been demonstrated.
Instead, targeted biopsy with chromoendoscopy has gained popu-
larity in European and Asian countries. Chromoendoscopy is gener-
ally considered to be an effective tool for ulcerative colitis
surveillance and is recommended in the guidelines of the British So-
ciety of Gastroenterology and the European Crohn’s and Colitis
Organisation. Although image-enhanced endoscopy, such as
narrow-band imaging and autofluorescence imaging, has been in-
vestigated as a potential ulcerative colitis surveillance tool, it is not
routinely applied for ulcerative colitis surveillance in its present form.
The appropriate intervals of surveillance colonoscopy have yet to be
determined. Although the Japanese and American guidelines rec-
ommend annual or biannual colonoscopy, the British Society of Gas-
troenterology and the European Crohn’s and Colitis Organisation
stratified their guidelines according to the risks of colorectal cancer.
A randomized controlled trial comparing random and targeted bi-
opsy methods has been conducted in Japan and although the final
analysis is still ongoing, the results of this study should address this
issue. In the present review, we focus on the current detection
methods and characterization of dysplasia/cancer and discuss the
appropriate intervals of colonoscopy according to the stratified risks.
Key words: chromoendoscopy, colorectal cancer, image-
enhanced endoscopy, surveillance colonoscopy, ulcerative colitis

INTRODUCTION Colonoscopy was first introduced to St. Mark’s Hospital

from Japan in 1970, and St. Mark’s Hospital initiated a sur-
ROHN AND ROSENBERG reported the first case of
C colorectal cancer (CRC) in a patient with ulcerative colitis
(UC) in 1925.1 At that time, the only method to directly observe
veillance program for UC in 1973, which is the longest pro-
gram of its kind.3 Six years later, The University of Tokyo
started a similar program in Japan.4 Since then, endoscopic
the colorectum was rigid sigmoidoscopy. Since then, many
surveillance has long been considered to be the gold standard
cases with colitis-associated colorectal cancer (CAC) have been
for detecting CAC. CAC has distinct features compared to
reported. Until the 1960s, total proctocolectomy was carried out
sporadic CRC:5 (i) CAC is more common in the younger gen-
to prevent CAC for patients with pancolitis with disease
eration; (ii) CAC is difficult to detect using a barium enema or
durations of more than 10 years because there were no appro-
even by colonoscopy because of its widespread nature; (iii)
priate methods to survey the whole colorectum, such as colo-
histologically, mucinous adenocarcinoma and signet-ring cell
noscopy, at that time. In 1967, Dr Morson from St. Mark’s
carcinoma are frequent in CAC6 and dysplasia is often close
Hospital introduced the concept of surveillance by reporting
to or distant to CAC;2 and (iv) genetic alterations are different,
the importance of coexisting dysplasia anatomically near or
and the dysplasia-carcinoma sequence is postulated in CAC.7
distant to CAC.2 This report, together with the advent of endos-
Ekbom et al. reported that the relative risk of CRC for
copy, created the idea of surveillance colonoscopy for CAC.
pancolitis, left-sided colitis, and proctitis, compared with
healthy population, was 14.8, 2.8 and 1.7, respectively.8 An-
Corresponding: Toshiaki Watanabe, Department of Surgical
other well-known risk factor for CAC is disease duration.
Oncology, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo Most guidelines recommend surveillance colonoscopy for
113-8655, Japan. Email: toshwatanabe@yahoo.co.jp patients with pancolitis and left-sided colitis 6–10 years after
Received 2 May 2015; accepted 15 June 2015. onset.9–11 However, CAC may be difficult to identify even

260 © 2015 The Authors

Digestive Endoscopy © 2015 Japan Gastroenterological Endoscopy Society
bs_bs_banner

Digestive Endoscopy 2016; 28: 260–265
by colonoscopy because of the complex background muco-
sal changes of UC itself and the morphological diversity of
CAC. Therefore, four random biopsies from every 10 cm of
the whole colorectum have been recommended rather than
the targeted biopsy method used in Western countries un-
til recently. However, with the improvement of endoscopic
equipment, the concept of UC surveillance has been chang-
ing. Recent guidelines from the British Society of Gastroen-
terology (BSG) and the European Crohn’s and Colitis
Organisation (ECCO) recommend targeted biopsy with
panchromoendoscopy, especially when carried out by an ex-
perienced gastroenterologist.9 Otherwise, the random biopsy
method is still the preferred choice.9,11 However, the appropri-
ate intervals for UC surveillance have yet to be determined.
Recent guidelines have incorporated risk stratifications for
surveillance intervals in order to maximize the effectiveness
of the UC surveillance program.
In this review article, we focus on the detection (random vs
target biopsy) and characterization of dysplasia and cancer.
Additionally, we discuss the appropriate intervals of colonos-
copy according to the stratified risks using various modalities,
such as chromoendoscopy (CE) and magnification and image-
enhanced endoscopy (IEE), including narrow-band imaging
(NBI) and autofluorescence imaging (AFI).
Detection (random vs targeted biopsy) and
characterization of dysplasia and cancer
One of the major criticisms against UC surveillance has been
that CRC may be missed even by constant surveillance colo-
noscopy, and the results have not been satisfactory in terms
of saving the lives of long-standing UC patients.12 Watanabe
et al. reported that CAC patients showed a poorer prognosis
than sporadic CRC patients in stage III, although the prognosis
of CAC was comparable to that of sporadic CRC in stages I
and II.13 Rubin et al. reported surprising results from a mathe-
matical analysis of resected specimens of CAC patients to de-
termine how many ‘random’ biopsies are required to detect
one dysplastic lesion.14 According to this study, at least 34
and 64 biopsy specimens should be ‘blindly’ taken in order
to achieve 90% and 95% confidence, respectively, which com-
pelled most guidelines to recommend the acquisition of four
biopsies every 10 cm.9 However, this random biopsy method
is time-consuming and less cost-effective. Studies showed that
most dysplastic lesions are visible with newer high-definition
endoscopes;15,16 thus, the targeted biopsy method has been
adopted in many Japanese specialized institutions. The Japa-
nese Research Group for Intractable Inflammatory Bowel Dis-
ease of the Ministry of Health, Labour and Welfare of Japan
conducted a prospective study investigating the effectiveness
of the targeted biopsy method and demonstrated that the
Digestive Endoscopy © 2015 Japan Gastroenterological Endoscopy Society
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Surveillance colonoscopy for UC 261
detection rate of dysplastic lesions solely by the targeted bi-
opsy method was comparable to that of a random biopsy
method reported from the West.17 To maximize the effective-
ness of a targeted biopsy, endoscopists should know the typi-
cal shapes of CAC. For this purpose, an atlas of CAC was
published from the same group.17 Additionally, St. Mark’s
Hospital in the UK showed the effectiveness of the targeted
biopsy method combined with CE.18 Guidelines from
Europe, such as those from the ECCO and BSG, recom-
mend targeted biopsies with CE especially for endoscopists
who are specialized in UC surveillance, with the random
biopsy method as an alternative,9,11 whereas the American
College of Gastroenterology guidelines primarily recom-
mend the random biopsy method, but refer to the possibility
of using the targeted biopsy method.10 However, the evi-
dence level for the efficacy of the targeted biopsy method
is not so high, and few studies have directly compared the
effectiveness of targeted biopsy with that of the random
biopsy method. In order to answer this question, a Japanese
group has conducted a randomized controlled trial (RCT)
directly comparing the efficacy of the targeted versus the
step biopsy in surveillance colonoscopy for CAC.19 The
study, which includes 250 patients, has been completed
and is currently under submission. The results of this study
should have a major impact on the future clinical practice of
surveillance colonoscopy for UC.
Chromoendoscopy and magnifying endoscopy
In the 21st century, dramatic improvements in endoscopic
devices, such as magnifying endoscopy, NBI, and CE, have
been applied to surveillance colonoscopy for inflammatory
bowel disease (IBD) patients.20 There are two major types of
CE: contrast and staining. Contrast methods such as indigo
carmine dye spraying do not ‘stain’ the colonic mucosa,
rather the dye pools in the grooves such that contrast visual-
izes subtle mucosal irregularities. Conversely, staining
methods such as methylene blue and crystal violet stain the
convex area of the colonic mucosa but not the grooves. Thus,
the pit pattern images of the two methods are different, similar
to positive and negative films in a photograph.20,21 Kiesslich
et al. demonstrated the effectiveness of methylene blue-aided
CE by applying Kudo’s pit pattern diagnosis for UC surveil-
lance in 2003.22 They conducted a RCT with a total of 263
patients with UC and found more dysplastic lesions using
CE with the targeted method. They further investigated
the usefulness of chromoscopy-guided endomicroscopy
and showed a higher detection rate of neoplastic lesions
using chromoscopy-guided endomicroscopy compared with
conventional endoscopy in a RCT.23 However, this study
was controversial.24 Although this study reconfirmed the
© 2015 The Authors

262 K. Hata et al.
effectiveness of CE, it did not demonstrate any superiority of
endomicroscopy over CE.
In 2004, Rutter et al. also reported the effectiveness of
pancolonic indigo carmine dye spraying by back-to-back colo-
noscopies, first without CE followed by with CE.18 In 2011,
Subramanian et al. published a meta-analysis combining six
studies that investigated the usefulness of CE.25 They proved
that CE was superior to conventional white light endoscopy
(WLE) regarding the dysplasia detection rate in both flat and
raised lesions and the proportion of targeted biopsies, although
the examination time for CE was significantly longer than that
for WLE. Although a recent Dutch cohort did not show signif-
icant superiority of CE over WLE,26 the usefulness of CE has
been generally accepted.3
In light of these results, the BSG and ECCO guidelines rec-
ommend the pancolonic dye spraying method with targeted bi-
opsies as an option.9,11
Image-enhanced endoscopy
Newer endoscopic imaging modalities (also known as IEE),
including NBI, Fuji intelligent chromoendoscopy (FICE),
and iScan, have been under investigation for the application
of UC surveillance (Figure 1). Matsumoto et al. proposed
new NBI patterns categorized into three patterns (honey-
comb-like, villous, and tortuous) in their preliminary study
and reported that the tortuous pattern may be helpful for
detecting dysplastic lesions using the NBI system,27 which
sheds new light on the pit pattern diagnosis specific for UC
surveillance, as Kudo’s classification could not always be
applied to UC surveillance as a result of variable background
mucosal changes in long-standing UC patients.27,28 However,
Dekker et al. utilized a first-generation NBI system for UC
surveillance, which showed comparable sensitivity to conven-
tional colonoscopy,29,30 although the number of patients exam-
ined was small and the study was underpowered. Efthymiou
et al. compared NBI with CE and concluded that NBI was
not superior to CE in the ability to detect dysplasia.31 There-
fore, NBI is not yet recommended for routine UC surveillance
in its present form. However, it may be useful for characteriz-
ing dysplastic lesions. For instance, it may be worthwhile to
distinguish the tortuous pattern for any suspicious lesions
in order to maximize the sensitivity of targeted biopsies, as
NBI is an easily applied procedure which only requires the
pressing of a button to change the mode if equipped.27
Two original articles regarding AFI have been published so
far.32,33 van den Broek et al. conducted a cross-over study and
demonstrated better results with AFI. In the AFI-first group,
they found 10 neoplastic lesions in 25 patients by an initial
AFI inspection followed by WLE, which found no dysplastic
lesions. However, in the WLE-first group, they detected three
more neoplastic lesions by AFI following an initial WLE
© 2015 The Authors
Digestive Endoscopy © 2015 Japan Gastroenterological Endoscopy Society
14431661, 2016, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/den.12505 by Cochrane Colombia, Wiley Online Library on [08/05/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Digestive Endoscopy 2016; 28: 260–265
inspection that detected three neoplastic lesions. Furthermore,
the missing rates of detection of neoplasia using AFI were sig-
nificantly lower than those for WLE (0% vs 50%, respectively;
P = 0.036). Although AFI showed positive results, the studies
have not resulted in changes in the routine use of AFI. There
are several disadvantages to AFI in its current form. First,
the resolution of AFI remains poor. Second, AFI may also de-
tect inflammatory areas as magenta in color, which could lead
to false-positive results.
Few studies have so far investigated the efficacy of FICE
and iScan for UC surveillance. However, a RCT comparing
FICE and conventional colonoscopy is currently ongoing
(clinical trials.gov: NCT00816491).34
Risk stratification and interval for
colonoscopic surveillance
A population study from Sweden compared the risk of CRC in
UC patients matched with a non-IBD population. The relative
risk of CRC was 14.8, 2.8, and 1.7 in total colitis, left-sided
colitis, and proctitis, respectively.8 In 2001, Eaden et al. con-
ducted a meta-analysis and estimated the cumulative probabil-
ities of having cancer at 10, 20, and 30 years as 2%, 8% and
18%, respectively,35 which showed that the risk for the
development of CRC was increased exponentially rather
than proportionally by each decade. These figures may be
overestimated as a result of selection biases. Two surveillance
cohorts from St. Mark’s Hospital and The University of Tokyo
demonstrated that the cumulative neoplasia (dysplasia plus in-
vasive cancer) rates were comparable to the cumulative inva-
sive cancer rates from Eaden’s meta-analysis and showed
lower figures for CAC than Eaden’s meta-analysis.3,4,36 These
two factors, duration from onset and disease extent of UC, are
two consistent major risk factors for the development of CRC.
Colitis associated with primary sclerosing cholangitis
(PSC) has a different disease entity from typical UC, which
harbors a higher risk of developing CRC as well as
hepatobiliary malignancies. Therefore, the strategy for survey-
ing CRC in patients with PSC should be stricter. Some guide-
lines recommend annual colonoscopic surveillance soon after
the diagnosis of PSC.
Regarding the appropriate interval for surveillance colonos-
copy, most guidelines recommend 1–2 years with no obvious
reasons. Rutter et al. reported that not only the extent, but also
the severity, of UC was a risk factor for the development of
CRC.37 This is somewhat difficult to assess as surveillance co-
lonoscopy is preferably carried out during remission. They
assessed the presence of inflammatory polyposis, colonic stric-
tures, and histological inflammation as inflammation indica-
tors. A normal colonic appearance with the presence of
vascularity appears to be a low risk factor for the development

Digestive Endoscopy 2016; 28: 260–265
Figure 1 Neoplastic mass exhibiting a flat granular lesion with a
polypoid mass in the center. (A) High-definition white light (WL)
endoscopy. (B) Narrow-band imaging (NBI) of the same lesion. (C)
Indigo carmine dye spraying visualizes subtle bumps of the
lesion more vividly. (D) Autofluorescence imaging (AFI) of the
same lesion shows a purple-colored area.
of neoplasia. The BSG guidelines stratified the risk for the de-
velopment of CRC in UC patients by risk factors such as the
presence of a family history of CRC, inflammatory polyps, dis-
ease extent, histological inflammation, and a previous history
of dysplasia. Patients are then recommended to receive surveil-
lance colonoscopy every 1, 3, or 5 years according to the risk.11
Regarding the initiation of surveillance colonoscopy, many
guidelines set it at 8–10 years from UC onset. However,
Lutgens et al. reported that approximately 17–28% of the
cases developed CAC even earlier;38 thus, the ECCO guide-
lines revised the timing and recommended that colonoscopy
should be started at 6–8 years after onset.9
DISCUSSION
HE CONCEPT OF surveillance colonoscopy for detect-
T ing dysplasia by biopsy proposed by Morson has
succeeded until now;2 however, with the advent of high-
definition colonoscopy, the strategy of UC surveillance has
changed in this past decade.5 Typical morphology for UC-
associated dysplasia and cancer has been elucidated and
targeted biopsy methods are now acceptable and gaining
popularity in Japan.17 However, vigilant endoscopic obser-
vation is mandatory for UC surveillance. In 2015, The
Digestive Endoscopy © 2015 Japan Gastroenterological Endoscopy Society
14431661, 2016, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/den.12505 by Cochrane Colombia, Wiley Online Library on [08/05/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Surveillance colonoscopy for UC 263
American Gastroenterology Association and The American
Society for Gastrointestinal Endoscopy jointly declared In-
ternational Consensus Recommendations, referred to as the
Surveillance for Colorectal Endoscopic Neoplasia Detection
and Management in Inflammatory Bowel Disease Patients
(SCENIC) developed by worldwide specialists.39,40 In this
recommendation, several terminologies were suggested. For
instance, discontinued use of the terms ‘dysplasia-associated
lesion or mass (DALM)’, ‘adenoma-like’ and ‘non-ade-
noma-like’ was recommended, and the terms associated with
the Paris classification were adapted. In addition, specific
surveillance methods and management of dysplasia were
also recommended. Regarding surveillance, strong recom-
mendations include the use of high-definition endoscopy
and chromoendoscopy. SCENIC also strongly recommended
that polypoid dysplasia be managed by endoscopic resection
with follow-up surveillance colonoscopy rather than
colectomy. In our opinion, the recent advancement of
high-definition WLE and CE is outstanding and these two
modalities will likely remain the standard for the next 3–5
years. Target biopsies with these modalities may suffice
for experienced endoscopists, whereas step biopsies will be
an alternative for general endoscopists who are not very fa-
miliar with CAC. The results from an ongoing RCT with
head-to-head comparison between targeted and step biopsy
methods will determine whether the targeted biopsy method
is a feasible option.19 An improvement in IEE will also be
expected in the field of CAC surveillance. The major disad-
vantages of the current form of IEE are poor resolution and
weak light intensities, which are expected to improve in the
near future. For instance, the next-generation NBI system
has a brighter light intensity; thus, new RCT using next-
generation IEE are warranted. However, at this time, there
are few studies supporting the superiority of IEE use for
the detection of dysplasia compared to high-definition
WLE. The usefulness of endomicroscopy, which can visual-
ize the nuclei of cells in vivo, has also been investigated in
UC surveillance.23 However, even a pathological diagnosis
using hematoxylin and eosin staining may not easily dis-
tinguish real neoplasia from inflammatory changes, and
the inter- and intra-observer concordance rates are low
in the pathological diagnosis of UC dysplasia, even with
Riddell’s standardized criteria.41,42 Therefore, the current
usefulness of endomicroscopy is limited.
The management of dysplasia is another issue. Riddell’s
criteria have been widely used for the classification of dyspla-
sia in IBD, in which dysplasia was classified into high-grade
dysplasia (HGD), low-grade dysplasia (LGD), or indefinite
for dysplasia (IND).41 If HGD is detected, surgical resection
such as restorative total proctocolectomy and ileal-pouch anal
anastomosis (IPAA) is the treatment of choice.43 Recently,
© 2015 The Authors

264 K. Hata et al.
laparoscopic surgery was applied to IPAA for UC,44 and no-
scar operation except for trocar incisions can be carried out
for selected cases.45 The management of LGD is a bit contro-
versial. Some recommend immediate surgical resection as the
rate of concomitant invasive cancer is estimated to be very
high,12,46 whereas others offer careful extensive follow-up
surveillance.47 Such discrepancy may be because of low con-
cordance rates for the diagnosis of LGD.
The cost-effectiveness of UC surveillance is also a hot topic.
The ECCO and BSG guidelines adopted risk stratification for
the optimal surveillance interval.9,11 Risk factors include se-
verity of the disease, PSC, pancolitis, pseudopolyposis and
family history of CRC. In addition to these clinical parameters,
molecular mechanisms for CAC have been elucidated.
Watanabe et al. found a specific gene expression pattern from
rectal biopsy specimens to discriminate high risk for the devel-
opment of CAC using expression arrays validated by reverse
transcription–polymerase chain reaction (RT-PCR).48,49 Such
molecular methods will most likely be used for risk stratifica-
tion in the near future. Furthermore, the risk factors for CAC
may differ by ethnicity. For instance, the prevalence of PSC
is lower in Japan;50 therefore, risk stratification strategies spe-
cific to the Japanese population are needed.
In conclusion, surveillance colonoscopy for CAC has greatly
improved in this last decade. Biopsy methods recently tend to
be more targeted and the cost-effectiveness of a surveillance
program should be considered according to risk stratification.
ACKNOWLEDGMENTS
HIS WORK IS partly supported by the Research Group
T for Intractable Inflammatory Bowel Disease of the Min-
istry of Health, Labour and Welfare of Japan (RGIBD) and
Grant-in-Aid for Challenging Exploratory Research (MEXT
KAKENHI Grant Number 25670570 to H.N.), and the
Ministry of Education, Culture, Sports, Science and Tech-
nology, Japan.
CONFLICT OF INTERESTS
OSHIAKI WATANABE HAS a patent regarding the way
T of determining the risk of developing cancer in ulcerative
colitis patients, which was registered on the register of the
Japanese patent office.
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