ASGE guideline: endoscopy in the diagnosis and treatment GUIDELINE

GUIDELINE
ASGE guideline: endoscopy in the diagnosis and treatment
of inflammatory bowel disease
Copyright ª 2006 by the American Society for Gastrointestinal Endoscopy
0016-5107/$32.00
doi:10.1016/j.gie.2006.02.005
drugs (NSAIDs)3 can cause mucosal changes mimicking IBD, these agents should be avoided before initial
colonoscopy.
Patients with other colitides can have similar clinical presentations and similar endoscopic features to the patients
with IBD. These colitides include infectious colitis, druginduced colitis, ischemic colitis, and radiation colitis. The
value of endoscopy alone in distinguishing IBD from nonIBD colitides is limited.4 However, the acquisition of the detailed information from index colonoscopy is important for
the differential diagnosis of CD and UC because, once therapy is started, it may obscure discriminating features of CD
from UC such as segmental colitis (patchiness) and rectal
sparing.5,6 In a study of 39 patients with treated UC, 44%
of patients had endoscopic patchiness and 13% had endoscopic rectal sparing; 33% had histologic evidence of patchiness and 15% had histologic sparing.6 At the time of
colonoscopy, attention should be paid to the anal and
perianal area because abnormalities are commonly seen
in the setting of CD. The most useful endoscopic features
(particularly the initial or index endoscopy) used to differentiate CD from UC are segmental colitis (ie, patchiness),
rectal sparing, involvement of the terminal ileum, and
anal or perianal disease. Other endoscopic features suggestive of CD include aphthous ulcers, discrete ulcers, serpiginous ulcers, and cobblestoning of mucosa. However, none
of the endoscopic features is specific for CD or UC.
Ileoscopy is important to distinguish true CD ileitis
from backwash ileitis, which occurs in up to 10% of cases
of active pancolitis in UC.7 Features that favor CD ileitis include discrete ulcers or strictures of the terminal ileum or
ileocecal valve.7-9
UC may progress proximally over time.10 The finding of
inflammatory changes around the appendiceal orifice (cecal patch or periappendiceal patch) in the setting of UC
with an otherwise normal right colon should not be confused with CD.11,12 The clinical implication of cecal patch
is not clear, although a recent controlled study revealed
that patients with UC with cecal patch had a similar rate
of remission, relapse, and proximal extension compared
with those with no cecal patch.12
Endoscopy together with other diagnostic modalities
can differentiate CD from UC in R 85% of patients.13 In
a prospective study of more than 350 patients with IBD
followed up for more than 22 months, index colonoscopy
and biopsy were accurate in distinguishing CD from UC in
558 GASTROINTESTINAL ENDOSCOPY Volume 63, No. 4 : 2006
www.giejournal.org
This is one of a series of statements discussing the use
of gastrointestinal endoscopy in common clinical situations. The Standards of Practice Committee of the American Society for Gastrointestinal Endoscopy prepared this
text. In preparing this guideline, a MEDLINE literature
search was performed, and additional references were
obtained from the bibliographies of the identified articles
and from recommendations of expert consultants. When
little or no data exist from well-designed prospective
trials, emphasis is given to results from large series and
reports from recognized experts.
Guidelines for appropriate use of endoscopy are based
on a critical review of the available data and expert consensus. Further controlled clinical studies are needed
to clarify aspects of this statement, and revision may be
necessary as new data appear. Clinical consideration
may justify a course of action at variance to these
recommendations.
INTRODUCTION
Endoscopy is an important diagnostic and therapeutic
modality in inflammatory bowel disease (IBD), being useful for both Crohn’s disease (CD) and ulcerative colitis
(UC). Endoscopy is used to make an initial diagnosis of
IBD, distinguish CD from UC, assess the disease extent
and activity, monitor response to therapy, allow for surveillance of dysplasia or neoplasia, and provide endoscopic
treatment, such as stricture dilation.
COLONOSCOPY WITH ILEOSCOPY
Colonoscopy with ileoscopy allows direct visualization
and biopsy of the mucosa of rectum, colon, and terminal
ileum. Unless contraindicated because of severe colitis or
possible toxic megacolon, a full colonoscopy with intubation of the terminal ileum should be performed during the
initial evaluation of patients with a clinical presentation
suggestive of IBD. Because sodium phosphate–based
bowel preparations1,2 and nonsteroidal anti-inflammatory
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
89% of cases. IBD diagnosis was revised in 4% of cases,
and the diagnosis of indeterminate colitis remained in
7% of cases.14
Mucosal biopsy is a critical component of endoscopic
examination for patients with suspected IBD to differentiate IBD from other causes of colitis such as bacterial infection, ischemia, and NSAID use. Although there is no single
diagnostic pathologic criterion that can definitively establish an IBD diagnosis, biopsy specimens can help differentiate CD from UC and differentiate CD and UC from other
colitides. Specimens should be taken of both diseased and
adjacent normal-appearing mucosa. The biopsy specimens
from different locations should be separately labeled. Several features suggest chronicity (indicating IBD rather
than an acute self-limited or infectious colitis) such as architectural distortion, basal plasmacytosis, increased cellularity of lamina propria, pyloric gland metaplasia, and
Paneth cell metaplasia.15-17 Although the presence of granulomata suggests CD, the frequency of detection of granulomas varies from 15% to 36% of endoscopic biopsy
specimens.18 Higher detection rates of granulomas can
be achieved when biopsy specimens are taken from the
edge of ulcers and aphthous erosions.19 Granulomas are
not pathognomonic for CD and they can be found in
other disease conditions such as tuberculosis, fungal and
bacterial infections, diversion colitis, sarcoidosis,20 and foreign body reaction (particularly from the suture line in patients with prior bowel resection surgery).
Mucosal biopsy also helps to establish the extent of colon that is inflamed, which aids in determining prognosis,
directing appropriate medical and surgical therapy, and
stratifying risk for dysplasia. The extent inflammation
can be classified as proctitis, left-sided colitis (inflammation up to the splenic flexure), or extensive (inflammation
proximal to the splenic flexure) or pancolitis. Macroscopic
proximal extension of proctitis or left-side colitis occurs in
approximately one third to one half of patients.21,22 However, regression of disease to the extent of pancolitis was
also common after a long duration of disease (eg, 25
years).23 The extent of endoscopic inflammation does
not necessarily correlate with histologic inflammation. Colonoscopy underestimates the extent of disease compared
with histology.24 The extent of colitis (pancolitis, left-sided
colitis, or proctitis) should be based on histologic examination rather than on endoscopy.25
Endoscopy is an objective tool to assess the disease activity of CD and UC, whereas subjective symptoms are not
a reliable indicator of disease severity. Additionally, there is
a poor correlation between symptom scores and degree of
endoscopic inflammation and between clinical remission
and mucosal healing.27 Endoscopy may be helpful in predicting the need for intensified medical therapy or surgical
intervention.28,29 There are numerous disease activity
scores that are based on clinical symptoms or endoscopic
findings.24-26,30 With the use of immunomodulator and biologic therapy for IBD, objective endoscopic findings are
needed to assess response to the therapy.31-33 In more recent pharmaceutical trials, the documentation of endoscopic mucosal healing has become a critical component
of outcome measurement.29,34
www.giejournal.org
Volume 63, No. 4 : 2006 GASTROINTESTINAL ENDOSCOPY 559
FLEXIBLE SIGMOIDOSCOPY
Under certain circumstances, flexible sigmoidoscopy
may provide useful information in patients with IBD. An
adequate diagnosis may be obtained, and it should be performed preferentially when colonoscopy is considered
high risk (eg, fulminant colitis).33 In patients with established UC, flexible sigmoidoscopy may define disease activity and is useful in evaluating for superimposed
colitides including cytomegalovirus (CMV) and Clostridium difficile infections or ischemic colitis when disease
exacerbations occur.
ESOPHAGOGASTRODUODENOSCOPY
Esophagogastroduodenoscopy (EGD) can be a useful in
the evaluation of patients with IBD. Upper gastrointestinal
(GI) tract involvement (proximal to the ligament of Treitz)
occurs in up to 13% of patients with CD.35,36 CD can involve
the esophagus,37 stomach,38 and duodenum.39 It appears
that duodenal biopsy specimens more often display granulomas (40%-68%) than do colon biopsy specimens.39-41 In
patients with indeterminate colitis, upper GI tract involvement can help establish a diagnosis of CD.42 However,
when the upper GI tract is involved in CD, disease is usually
present elsewhere, such as the terminal ileum, colon, or
perianal area. Therefore, routine EGD is not recommended in all patients suspected of having CD. Additionally,
patients with UC may also have upper GI inflammation,
such as diffuse duodenitis.43 Endoscopic features in these
patients include edema, erythema, erosions, and thickened
mucosal folds.44 Histologic examination may show active
chronic inflammation with architectural mucosal distortion,44 villous atrophy, and intraepithelial lymphocytosis.45
Other applications of EGD with small bowel biopsy in patients with IBD include evaluation of concomitant celiac disease43,46 eosinophilic enteritis,45 common variable immune
deficiency,47 and small bowel neoplasia.44,48 In patients with
CD, symptomatic duodenal strictures may respond to endoscopic balloon dilation.49
ENTEROSCOPY
Push enteroscopy has a limited role in the management
of patients with IBD, especially in the era of capsule endoscopy (CE). In patients with abnormalities seen on
other imaging studies that are within reach, push enteroscopy allows endoscopic and histologic evaluation and
therapeutic intervention.50,51 Intraoperative endoscopy
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
has been used in selected patients with indeterminate colitis at the time of total colectomy and ileal pouch–anal
anastomosis.
radiographic evidence of small bowel narrowing in the setting of CD should not undergo CE. Capsule retention
above a CD stricture may be treated with anti-inflammatory medications, although there are no published
studies.76
CAPSULE ENDOSCOPY
CE allows for direct and minimally invasive visualization
of small bowel mucosa. It may help identify superficial lesions not detected by traditional endoscopy and radiography. It might be useful in the initial diagnosis of CD, for
detecting recurrences, for establishing extent of disease,
for assessing response to therapy, and for differentiating
CD from UC or indeterminate colitis. Data from retrospective studies, case series, and prospective studies have
shown that CE is useful for the diagnoses of CD when
small bowel follow through (SBFT) and ileoscopy are negative or unsuccessful.52-66 The diagnostic yield of CE
ranges from 10% to 71% depending on the clinical setting.
CE has been shown to be more sensitive in the detection
of small bowel CD than is computed tomographic (CT)
enterography,66 SBFT,66 and enteroclysis.67 In patients
with mild to moderate disease and a normal SBFT,68 CE
may allow for the detection of small bowel changes that
are not within reach of push enteroscopy (PE). A recent
prospective study of 42 patients compared SBFT, CT enterography, colonoscopy with ileoscopy, and CE in the assessment of small bowel CD. Of these 4 modalities, CE had the
highest sensitivity (83%) with the lowest specificity (53%)
and colonoscopy with ileoscopy had the highest specificity
(100%) with a sensitivity of 74%.69 A recent study in 39 patients, the majority with known CD, reported CE sensitivity
and specificity of 89.6% and 100%, respectively.70 Few studies have evaluated the benefit of CE in the evaluation of indeterminate colitis. One study found that 5 of 22 patients
with colitis were found to have mucosal breaks in the small
bowel on CE, thus changing their diagnosis to CD.62
The main limitations of CE in the assessment of small
bowel CD are the lack of uniform criteria for diagnosing
CD, inability to allow for tissue acquisition or therapeutic
intervention, and the risk for capsule retention. It is important to note that the finding of mucosal breaks the
small bowel is not necessarily indicative of CD. A variety
of disease entities can cause mucosal ulcerations such as
infection, ischemia, radiation injury, and drug-induced injury, particularly NSAIDs.71 In addition, it has been reported that up to 14% of healthy individuals had
mucosal breaks and other nonspecific lesions on CE.67
Capsule retention in CD patients resulting from underlying small bowel strictures is a major concern, occurring
in 1% to 13% of patients with known CD.72,73 Retained
capsules may require surgery74 in patients that may otherwise have not required surgery. A preingestion radiologic
study (CT or SBFT) is recommended73-75 because asymptomatic CD strictures occur in as many as 22%.73 Patients
with obstructive symptoms or with endoscopic and
560 GASTROINTESTINAL ENDOSCOPY Volume 63, No. 4 : 2006
ENDOSCOPIC ULTRASONOGRAPHY
Ultrasonography (US) including transperineal US and
endoscopic US (EUS) with a rigid scope or with flexible
endoscopes has been used to assess disease activity of colitis, transmural disease,77 fistulae,78-81 abscess,79-81 and regional lymphadenopathy.79 For patients with perianal
disease, EUS can accurately characterize perianal disease
to reduce the risk of incomplete healing, recurrent fistula,
or inadvertent sphincter injury if fistula anatomy is incorrectly delineated or an occult abscess missed at surgery.82
EUS has an excellent accuracy in the assessment of
Crohn’s perianal fistula and abscess.79,83 EUS may be
used to monitor medical and surgical therapy for CD
perianal fistulae.81,84-87 The EUS finding of transmural disease may allow for the differentiation of CD and UC.79-81
ENDOSCOPY IN PATIENTS WITH IBD-RELATED
SURGERY
Ileal pouch endoscopy
Ileal pouch anal anastomosis (IPAA) has become the
surgical treatment of choice for patients with UC who
required colectomy. IPAA significantly improves healthrelated quality of life, although complications can occur.
In addition to the immediate postoperative complications
such as pouch leak and abscess, long-term inflammatory
and noninflammatory complications commonly develop,
including pouchitis, ‘‘cuffitis,’’ irritable pouch syndrome,
and CD of the pouch. Pouchitis is the most common
long-term complication and symptom assessment alone
is not diagnostic.86,88 Endoscopic and histologic assessment allow the diagnosis of pouchitis and exclude other
causes of symptoms.88,89 Pouch endoscopy is also important for the evaluation and management of CD of the
pouch, cuffitis, pouch stricture, and irritable pouch syndrome.90-92 A gastroscope is easier to use than a flexible
sigmoidoscope for pouch evaluation because of its smaller
caliber and greater maneuverability. Endoscopic therapy
such as pouch stricture dilation can be performed.92,93 Endoscopic evaluation is also useful for evaluating symptomatic patients with ileal pouch–rectal anastomoses, Kock
pouches, and Brooke ileostomies.
Colonoscopy after partial colectomy or partial
ileocolectomy. Recurrence of CD after partial colectomy or partial ileocolectomy is common, typically occurring at the surgical anastomosis and neoterminal ileum.
Endoscopic recurrence rates range from 70% to 90%
within 1 year of surgery.30,94,95 Endoscopic recurrence
www.giejournal.org
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
typically precedes relapse of symptoms. Changes in the
neoterminal ileum after surgery are the most prognostic
factor for recurrence.96,97 Therefore, some investigators
recommend postoperative colonoscopy with inspection
of the neoterminal ileum 6 to 12 months after resection
to identify patients who are at risk for relapse and who
may benefit from appropriate medical therapy.
ENDOSCOPIC RETROGRADE
CHOLANGIOPANCREATOGRAPHY FOR
PRIMARY SCLEROSING CHOLANGITIS
The role of endoscopic retrograde cholangiopancreatography in patients with primary sclerosing cholangitis
has been addressed in a previous document.98
CANCER SURVEILLANCE
Individuals with long-standing UC and extensive CD colitis are at increased risk for development of dysplasia and
colorectal cancer (CRC) and should undergo colonoscopic
surveillance. The risk of CRC increases with longer duration and extensive severe colitis, family history of CRC,
young age at onset of disease, presence of backwash ileitis, and personal history of primary sclerosing cholangitis.96,97,99,100,101 The presence of proctitis alone does not
increase the risk for CRC. Patients with UC who have
left-sided colitis or more extensive disease are at increased
risk. In Crohn’s colitis, those patients with extensive disease involving more than a third of the colon also have
an increased risk of CRC, similar to patients with
UC.102,103 The extent of colonic involvement should be
based on both endoscopic and histologic criteria, whichever reveals more extensive disease.104 In a case-control
study of UC patients undergoing colonoscopic surveillance, there was a reduction in mortality resulting from
CRC in those patients in surveillance programs.105
Patients with UC or extensive Crohn’s colitis (greater
than one third colonic involvement) should undergo surveillance colonoscopy every 1 to 2 years beginning 8 to 10
years after disease onset.103 Biopsy specimens of the colon in patients with documented pancolitis should be obtained in all 4 quadrants every 10 cm from the cecum to
the rectum, to obtain a minimum of 32 biopsy samples.106,107 In patients with less extensive colitis, biopy
specimens can be limited to the microscopically involved
segments.106,107 Diagnosis of dysplasia should be confirmed by a second gastrointestinal pathologist.103 The
management of dysplastic polypoid lesions is currently
evolving. The presence of high-grade dysplasia or multifocal low-grade dysplasia in flat mucosa is an indication for
colectomy. The management of unifocal low grade dysplasia is controversial as to whether colectomy should be
performed. Biopsy specimens should be obtained of strictures, mass lesions, and macroscopic abnormalities other
www.giejournal.org
than pseudopolyps.108,109 Adenomatous-appearing polyps
encountered should be completely removed by polypectomy and biopsy samples should be obtained from the adjacent flat mucosa to determine the presence of dysplasia.
If a dysplastic polyp is identified outside an area of inflammation and there is no evidence of dysplasia in the adjacent mucosa, it can be managed as a sporadic polyp
similar to polyps in individuals without UC or Crohn’s colitis. If a dysplastic polyp is in an area of active inflammation (DALM [dysplasia associated lesion or mass]) and is
sessile, not amenable to endoscopic removal and there
is evidence of dysplasia in the adjacent mucosa, colectomy
is indicated.103,106,107,110-113 If a discrete polyp amenable
to polypectomy is found in an area of inflammation, it
should be completely removed and a biopsy specimen
of the mucosa adjacent to the polypectomy site should
be obtained and placed in separate jars.113 Tattooing of
the site should also be considered. If complete removal
was not possible or if there is evidence of flat dysplasia
in any other sites, then a total colectomy is recommended.
The finding of indefinite dysplasia requires repeat colonoscopy in 3 to 6 months and close follow-up.103
There is no clear evidence that surveillance colonoscopy
prolongs survival in patients with extensive colitis.114 However, patients in surveillance programs tend to have cancers
detected at an earlier stage and have a correspondingly
better prognosis, although these findings may be due to
lead-time bias.114 There is indirect evidence that surveillance is effective in reducing the risk of death from IBDassociated CRC and is acceptably cost-effective.114
Chromoendoscopy offers the potential for improved
sensitivity during colonoscopic surveillance by allowing
for targeted biopsies of enhanced mucosal abnormality.
Prospective trials of methylene blue and indigo carmine
staining reported improved detection of dysplasia in patients with UC.115,116 With chromoendoscopy using 0.1%
methylene blue staining, the detection of high- or lowgrade dysplasia in macroscopically normal mucosa was
increased 6-fold with the number of detected flat intraepithelial neoplasia of 24 in the chromoendoscopy group
versus 4 in the conventional colonoscopy group (P Z
.0007).115 In a separate study of back-to-back colonoscopy
and chromoendoscopy using 0.1% indigo carmine spray,
the overall detection rates of dysplasia (2% vs 7%) between the conventional colonoscopy and chromoendoscopy were not statistically different.116 While promising,
chromoendoscopy has not yet been adopted in routine
practice.
STRICTURE EVALUATION AND DILATION
Colonic strictures may complicate CD, and to a lesser
extent UC. In patients with CD, strictures may occur at
the ileocolonic valve, terminal ileum, and ileocolonic
surgical anastomosis and can be asymptomatic. In
Volume 63, No. 4 : 2006 GASTROINTESTINAL ENDOSCOPY 561
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
symptomatic patients, endoscopy is indicated for assessment and biopsy to exclude possible malignancy, especially in the setting of UC, where a stricture should be
considered malignant until proven otherwise. If it cannot
be thoroughly examined and biopsy performed117 surgical
resection should be considered. The finding of a colonic
stricture in the setting of CD is more likely to be benign,
although complete examination with biopsy is recommended. Balloon dilation may be required to completely evaluate the stricture. Endoscopic balloon dilation has been
investigated in patients with Crohn’s strictures of the small
bowel, colon, and anastomosis. The majority of these
studies are retrospective and the main outcome measurement is symptom relief and avoidance of surgery.
Endoscopic balloon dilation may relieve symptoms. Complications include perforation and bleeding.118–121 Corticosteroid injection into the stricture at the time of
balloon dilation may improve outcome.122,123
d
d
d
there is no dysplasia in flat mucosa surrounding the
polyp or elsewhere in the colon (B).
EUS is highly accurate for characterizing perianal
Crohn’s disease (C).
A colonic stricture in the setting of UC should be considered malignant until proven otherwise. If adequate evaluation cannot be performed, then colectomy is
indicated (C).
Chronic benign fibrotic strictures associated with obstructive symptoms may be managed with endoscopic
balloon dilation with or without steroid injections (B).
REFERENCES
Colonoscopy with ileoscopy should be performed in
the evaluation of IBD and for differentiating UC from
CD (B).
Mucosal biopsy specimens are important for the diagnosis of IBD and may help differentiate CD from UC (B).
When colonoscopy is contraindicated, or the extent of
disease is limited, flexible sigmoidoscopy may provide
an adequate diagnosis (C).
EGD or enteroscopy may be helpful for diagnosing IBD
when other studies have negative results and for differentiating CD from UC in indeterminate colitis (B).
CE is a less invasive technique for evaluating the small
intestine for Crohn’s involvement and has been shown
to be more sensitive than radiologic and endoscopic
procedures for detecting small bowel lesions (B).
In patients with CD and known or suspected high-grade
strictures, CE should not be performed (C). Small bowel
follow-through or CT enterography should be obtained
before CE in patients with CD to assess for high-grade
strictures (C).
CRC risk is increased in both UC and extensive Crohn’s
colitis and surveillance colonoscopy with multiple biopsies should be performed every 1 to 2 years beginning
after 8 to 10 years of disease (B).
The finding of dysplasia in flat mucosa, especially if multifocal, is an indication for total colectomy (B). Colectomy is indicated for colorectal cancer, high-grade
dysplasia or low-grade dysplasia (particularly multifocal)
in flat mucosa. A dysplastic mass lesion that cannot be
removed endoscopically, or is associated with dysplasia elsewhere in the colon, is an indication for total
colectomy (B).
Dysplastic polypoid lesions may be managed as sporadic
adenomas provided they are completely resected and
1. Zwas FR, Cirillo NW, El-Serag HB, et al. Colonic mucosal abnormalities
associated with oral sodium phosphate solution. Gastrointest Endosc
1996;43:463-6.
2. Rejchrt S, Bures J, Siroky M, et al. A prospective, observational study
of colonic mucosal abnormalities associated with orally administered
sodium phosphate for colon cleansing before colonoscopy. Gastroint
Endosc 2004;59:651-4.
3. Lengelling RW, Mitros FA, Brennan JA, et al. Ulcerative ileitis encountered at ileo-colonoscopy: likely role of nonsteroidal agents. Clin
Gastroenterol Hepatol 2003;1:160-9.
4. Tedesco FJ, Hardin RD, Harper RN, et al. Infectious colitis endoscopically simulating inflammatory bowel disease: a prospective evaluation. Gastrointest Endosc 1983;29:195-7.
5. Kim B, Barnett JL, Kleer CG, et al. Endoscopic and histological
patchiness in treated ulcerative colitis. Am J Gastroenterol 1999;94:
3258-62.
6. Bernstein CN, Shanahan F, Anton PA, et al. Patchiness of mucosal inflammation in treated ulcerative colitis: a prospective study. Gastrointest Endosc 1995;42:232-7.
7. Chutkan RK, Wayne JD. Endoscopy in inflammatory bowel disease.
In: Kirshner JB, editor. Inflammatory bowel disease. 5th ed. Baltimore: Williams & Wilkins; 2000. p. 453-77.
8. Moum B, Ekbom A, Vatn MH, et al. Change in the extent of colonoscopic and histological involvement in ulcerative colitis over time.
Am J Gastroenterol 1999;94:1564-9.
9. Rutgeerts P. Strategies in the prevention of post-operative recurrence in Crohn’s disease. Best Pract Res Clin Gastroenterol 2003;17:
63-73.
10. Geboes K, Ectors N, D’Haens G, et al. Is ileoscopy with biopsy worthwhile in patients presenting with symptoms of inflammatory bowel
disease? Am J Gastroenterol 1998;93:201-6.
11. Okawa K, Aoki T, Sano K, et al. Ulcerative colitis with skip lesions at
the mouth of the appendix: a clinical study. Am J Gastroenterol
1998;93:2405-10.
12. Byeon J-S, Yan S-K, Myung S-J, et al. Clinical course of distal ulcerative
colitis in relation to appendiceal orifice inflammation status. Inflamm
Bowel Dis 2005;11:366-71.
13. Chutkan RK, Scherl E, Waye JD. Colonoscopy in inflammatory bowel
disease. Gastrointest Endosc Clin North Am 2002;12:463-83.
14. Pera A, Bellando P, Caldera D, et al. Colonoscopy in inflammatory
bowel disease: diagnostic accuracy and proposal of an endoscopic
score. Gastroenterology 1987;92:181-5.
15. Surawicz CM, Bellic L. Rectal biotpsy helped to distinguish acute selflimited colitis from idiopathic inflammatory bowel disease. Gastroenterology 1984;86:104-13.
16. Dundas SA, Dutton J, Skipworth P. Reliability of rectal biopsy in distinguishing between chronic inflammatory bowel disease and acute
self-limited colitis. Histopathology 1997;31:60-6.
562 GASTROINTESTINAL ENDOSCOPY Volume 63, No. 4 : 2006
www.giejournal.org
SUMMARY
d
d
d
d
d
d
d
d
d
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
17. Tanaka M, Saito H, Kusumi T, et al. Spatial distribution and histogenesis of colorectal Paneth cell metaplasia in idiopathic inflammatory
bowel disease. J Gastroenterol Hepatol 2001;16:1353-9.
18. Ramzan NN, Leighton JA, Heigh RI, et al. Clinical significance of granuloma in Crohn’s disease. Inflamm Bowel Dis 2002;8:168-73.
19. Potzi R, Walgram M, Lochs H, et al. Diagnostic significance of endoscopic biopsy in Crohn’s disease. Endoscopy 1989;21:60-2.
20. Sands BE. From symptom to diagnosis: clinical distinctions among
various forms of intestinal inflammation. Gastroenterology 2004;
126:1518-32.
21. Meucci G, Vecchi M, Astegiano M, et al. The natural history of ulcerative proctitis: a multicenter, retrospective study, Gruppo di Studio
per le Malattie Infiammatorie Intestinali (GSMII). Am J Gastroenterol
2000;95:469-73.
22. Longholz E, Munkholm P, Davidsen M, et al. Changes in extent of ulcerative colitis: a study on the course and prognostic factors. Scand J
Gastroenterol 1996;31:260-6.
23. Mary JY, Modigliani R. Development and validation of an endoscopic
index of the severity for Crohn’s disease: a prospective multicentre
study. Groupe d’Etudes Therapeutiques dex Affections Inflammatoires du Tube Digestif (GETAID). Gut 1989;30:983-9.
24. Goboes K, Dalle I. Influence of treatment on morphological features
of mucosal inflammation. Gut 2002;50(3 Suppl):III37-42.
25. Floren CH, Benoni C, Willen R. Histologic and colonoscopic assessment of disease extension in ulcerative colitis. Scand J Gastroenterol
1987;22:459-62.
26. Reference removed.
27. Landi B, Anh TN, Cortot A, et al. Endoscopic monitoring of Crohn’s
disease treatment: a prospective, randomized clinical trial, the
Groupe d’Etudes Therapeutiques des Affections Inflammatoires Digestives. Gastroenterology 1992;102:1647-53.
28. Carbonnel F, Lavergne A, Lemann M, et al. Colonoscopy of acute colitis: a safe and reliable tool for assessment of severity. Dig Dis Sci
1994;39:1550-7.
29. Rugeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction
and maintenance therapy for ulcerative colitis. N Engl J Med 2005;
353:2462-76.
30. Olaison G, Smedh K Sjodahl R. Natural course of Crohn’s disease after
ileocolic resection: endoscopically visualized ieal ulcers preceding
symptoms. Gut 1992;33:331-5.
31. D’haens G, Van Deventer S, Van Hogezand R, et al. Endoscopic and
histological healing with infliximab anti-tumor necrosis factor antibodies in Crohn’s disease: a European multicenter trial. Gastroenterology 1999;116:1029-34.
32. D’Haens G, Geboes K, Rutgeerts P. Endoscopic and histologic healing
of Crohn’s (ileo-) colitis with azathioprine. Gastrointest Endosc 1999;
50:667-71.
33. American Society for Gastrointestinal Endoscopy. Appropriate use of
gastrointestinal endoscopy. Gastrointest Endosc 2000;52:831-7.
34. D’Haens G, Geboes K, Ponette E, et al. Healing of severe recurrent ileitis with azathioprine therapy in patients with Crohn’s disease. Gastroenterology 1997;112:1475-82.
35. Witte AM, Veenendaal RA, Van Hogezand RA, et al. Crohn’s disease of
the upper gastrointestinal tract: the value of endoscopic examination. Scand J Gastroenterol 1998;225(Suppl):100-5.
36. Wagtmans MJ, van Hogezand RA, Griffioen G, et al. Crohn’s disease of
the upper gastrointestinal tract. Neth J Med 1997;50:S2-7.
37. Decker GA, Loftus EV Jr, Pasha TM, et al. Crohn’s disease of the
esophagus: clinical features and outcomes. Inflamm Bowel Dis
2001;7:113-9.
38. Rutgeerts P, Onette E, Vantrappen G, et al. Crohn’s disease of the
stomach and duodenum: A clinical study with emphasis on the value
of endoscopy and endoscopic biopsies. Endoscopy 1980;12:288-94.
39. Curtis WD, Schuman BM, Griffin JW. Association of gluten-sensitive
enteropathy and Crohn’s colitis. Am J Gastroenterol 1992;87:1634-7.
40. Nugent FW, Roy MA. Duodenal Crohn’s disease: An analysis of 89
cases. Am J Gastroenterol 1989;84:249-54.
www.giejournal.org
41. Tobin JM, Sinha B, Ramani P, et al. Upper gastrointestinal mucosal
disease in pediatric Crohn disease and ulcerative colitis: a blinded,
controlled study. J Ped Gastroenterol Nutri 2001;32:443-8.
42. Kundhal PS, Stormon MO, Zachos M, et al. Gastral antral biopsy in
the differentiation of pediatric colitides. Am J Gastroenterol 2003;
98:557-61.
43. Valdez R, Appelman HD, Bronner MP, et al. Diffuse duodenitis associated with ulcerative colitis. Am J Surg Pathol 2000;24:1407-13.
44. Solem CA, Harmsen WS, Zinsmeister AR, et al. Small intestinal adenocarcinoma in Crohn’s disease: a case-control study. Inflamm Bowel
Dis 2004;10:32-5.
45. Talley NJ, Shorter RG, Phillips SF, et al. Eosinophilic gastroenteritis:
a clinicopathological study of patients with disease of the mucosa,
muscle layer, and subserosal tissues. Gut 1990;31:5-8.
46. Gillberg R, Dotevall G, Ahren C. Chronic inflammatory bowel disease in patients with coeliac disease. Scand J Gastroenterol 1982;
17:491-6.
47. Washington K, Stenzel T, Buckley RH, et al. Gastrointestinal pathology
in patients with common variable inmmunodeficiency and X-linked
agammaglobulinemia. Am J Surg Pathol 1996;20:1240-52.
48. Jess T, Winther KV, Munkholm P, et al. Intestinal and extra-intestinal
cancer in Crohn’s disease: follow-up of a population-based cohort in
Copenhagen County, Denmark. Aliment Pharmacol Ther 2004;19:
287-93.
49. Matsui T, Hatakeyama S, Ikeda K, et al. Long-term outcome of endoscopic balloon dilation in obstructive gastroduodenal Crohn’s disease. Endoscopy 1997;29:640-5.
50. Perez-Cuadrado E, Macenlle R, Iglesias J, et al. Usefulness of oral
video push enteroscopy in Crohn’s disease. Endoscopy 1997;29:
745-7.
51. Lescut D, Vanco D, Bonniere P, et al. Perioperative endoscopy of the
whole small bowel in Crohn’s disease. Gut 1993;34:647-9.
52. Scapa E, Jacob H, Lewkowicz S, et al. Initial experience of wirelesscapsule endoscopy for evaluating occult gastrointestinal bleeding
and suspected small bowel pathology. Am J Gastroenterol 2002;97:
2776-9.
53. Caunedo A, Rodrigues-Tellex M, Garcia-Montes J, et al. Usefulness of
capsule endoscopy in patients with suspected small bowel disease.
Rev Esp Enferm Dig 2004;96:10-21.
54. Dubcenco E, Jeejeebhoy KN, Tang SJ, et al. The value of capsule endoscopy in the diagnosis and management of Crohn’s disease: report
of two cases. Gastrointest Endosc 2004;59:314-6.
55. Hara AK, Leighton JA, Sharma VK, et al. Small bowel: preliminary
comparison of capsule endoscopy with barium study and CT. Radiology 2004;230:260-5.
56. Herrerias JM, Caunedo A, Rodriguez-Tellez M, et al. Capsule endoscopy in patients with suspected Crohn’s disease and negative endoscopy. Endoscopy 2003;35:564-8.
57. Mow WS, Lo SK, Targan SR, et al. Initial experience with wireless capsule enteroscopy in the diagnosis and management of inflammatory
bowel disease. Clin Gastroenterol Hepatol 2004;2:31-40.
58. Fireman Z, Mahajna E, Broide E, et al. Diagnosing small bowel Crohn’s
disease with wireless capsule endoscopy. Gut 2003;52:390-2.
59. Arguelles-Arias F, Caunedo A, Romero J, et al. The value of capsule
endoscopy in pediatric patients with a suspicion of Crohn’s disease.
Endoscopy 2004;36:869-73.
60. Costamagna G, Shah SK, Riccioni ME, et al. A prospective trial comparing small bowel radiographs and video capsule endoscopy for
suspected small bowel disease. Gastroenterology 2002;123:999-1005.
61. Eliakim R, Fischer D, Suissa A, et al. Wireless capsule video endoscopy
is a superior diagnostic tool in comparison to barium follow-through
and computerized tomography in patients with suspected Crohn’s
disease. Eur J Gastroenterol Hepatol 2003;15:363-7.
62. Eliakim R, Suissa A, Yassin K, et al. Wireless capsule video endoscopy
compared to barium follow-through and computerized tomography
in patients with suspected Crohn’s diseasedfinal report. Dig Liver
Dis 2004;36:519-22.
Volume 63, No. 4 : 2006 GASTROINTESTINAL ENDOSCOPY 563
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
63. Voderholzer WA, Ortner M, Rogalla P, et al. Diagnostic yield of wireless capsule enteroscopy in comparison with computed tomography
enteroclysis. Endoscopy 2003;35:1009-14.
64. Voderholzer WA, Beinhoelzl J, Rogalla P, et al. Small bowel involvement in Crohn’s disease: a prospective comparison of wireless capsule endoscopy and computed tomography enteroclysis. Gut 2005;
54:369-73.
65. Chong AKH, Taylor A, Miller A, et al. Capsule endoscopy vs. push enteroscopy and enteroclysis in suspected small-bowel Crohn’s disease.
Gastrointest Endosc 2005;61:255-61.
66. Reference removed.
67. Goldstein JL, Eisen GM, Lewis B, et al. Video capsule endoscopy to
prospectively assess small bowel injury with celecoxib, naproxen
plus omeprazole, and placebo. Clin Gastroenterol Hepatol 2005;3:
133-41.
68. Marmo R, Rotondano G, Piscopo R, et al. Capsule endoscopy versus enteroclysis in the detection of small-bowel involvement in
Crohn’s disease: a prospective trial. Clin Gastroenterol Hepatol
2005;3:772-6.
69. Solem CA, Loftus EV, Fletcher JG, et al. Small bowel (SB) imaging in
Crohn’s disease (CD): a prospective, blinded, 4-way comparison trial
[abstract]. Gastroenterology 2005;128(Suppl):A74.
70. Dubcenco E, Jeejeebhoy KN, Petroniene R, et al. Capsule endoscopy
findings in patients with established and suspected small-bowel
Crohn’s disease: correlation with radiologic, endoscopic, and histologic findings. Gastrointest Endosc 2005;62:538-44.
71. Yousfi MM, De Petris G, Leighton JA, et al. Diaphragm disease
after use of nonsteroidal anti-inflammatory agents: first report of
diagnosis with capsule endoscopy. J Clin Gastroenterol 2004;38:
686-91.
72. Faigel DO, Fennerty MB. ‘‘Cutting the cord’’ for capsule endoscopy.
Gastroenterology 2002;123:1385-8.
73. Cheifetz AS, Kornbluth AA, Legnani PE, et al. Incidence and outcome
of the retained video capsule endoscope (CE) in Crohn’s disease (CD)
is it a ‘‘therapeutic complication’’? [abstract]. Am J Gastroenterol
2004;99:S262.
74. Furukawa A, Yamasaki M, Furuichi K, et al. Helical CT in the diagnosis
of small bowel obstruction. Radiographics 2001;21:341-55.
75. Boudiaf M, Soyer P, Terem C, et al. CT evaluation of small bowel obstruction. Radiographics 2001;21:613-24.
76. Cave D, Lagnani P, de Franchis R, et al. ICCE consensus for capsule
retention. Endoscopy 2005;37:1065-7.
77. Dagli U, Over H, Tezel A, et al. Transrectal ultrasound in the diagnosis
and management of inflammatory bowel disease. Endoscopy 1999;
31:152-7.
78. Orsoni P, Barthet M, Portier F, et al. Prospective comparision of endosonography, magnetic resonance and surgical findings in anorectal
fistula and abscess complicating Crohn’s disease. Br J Surg 1999;86:
360-4.
79. Hildebrandt U, Kraus J, Ecker KW, et al. Endosonographic differentiation of mucosal and transmural nonspecific inflammatory bowel disease. Endoscopy 1992;24(1 Suppl):359-63.
80. Shimizu S, Tada M, Kawai K. Value of endoscopic ultrasonography
in the assessment of inflammatory bowel disease. Endoscopy 1992;
24(1 Suppl):354-8.
81. Shimizu S, Tada M, Kawai K. Endoscopic ultrasonography in the assessment of inflammatory bowel diseases. Gastrointest Endosc Clin
North Am 1995;5:851-9.
82. Schwartz DA, Harewood GC, Wiersema MJ. EUS in rectal disease. Gastrointest Endosc 2002;56:100-9.
83. Schwartz DA, Wiersema MJ, Dudiak KM, et al. A comparison of endoscopic ultrasound, magnetic resonance imaging, and exam under anesthesia for evaluation of Crohn’s perianal fistulas. Gastroenterology
2001;121:1064-72.
84. Schwartz DA, White CM, Wise PE, et al. Use of endoscopic ultrasound
to guide combination medical and surgical therapy for patients with
Crohn’s perianal fistulas. Inflamm Bowel Dis 2005;11:727-32.
85. Ardizzone S, Moconi G, Colombo E, et al. Perianal fistulae following
infliximab treatment: clinical and endosonographic outcome. Inflamm
Bowel Dis 2004;10:91-6.
86. Sandborn WJ, Tremaine WJ, Batts KP, et al. Pouchitis after ileal
pouch-anal anastomosis: a pouchitis disease activity index. Mayo
Clin Proc 1994;69:409-15.
87. Rasul I, Wilson SR, MacRae H, et al. Clinical and radiographical responses after infliximab treatment for perianal fistulizing Crohn’s disease. Am J Gastroenterol 2004;99:82-8.
88. Shen B, Achkar J-P, Lashner BA, et al. Endoscopic and histologic evaluations together with symptom assessment are required for the diagnosis of pouchitis. Gastroenterology 2001;121:261-7.
89. Shen B, Fazio VW, Remzi FH, et al. Comprehensive evaluation of inflammatory and non-inflammatory sequelae of ileal pouch-anal anastomosis. Am J Gastroenterol 2005;100:93-101.
90. Shen B, Achkar J-P, Lashner BA, et al. A randomized clinical trial of
ciprofloxacin and metronidazole to treat acute pouchitis. Inflamm
Bowel Dis 2001;7:301-5.
91. Shen B, Lashner BA, Bennett AE, et al. Treatment of rectal cuff inflammation (cuffitis) in patients with ulcerative colitis following restorative proctocolectomy and ileal pouch-anal anastomosis. Am J
Gastroenterol 2004;99:1527-31.
92. Shen B, Fazio VF, Remzi FH, et al. Endoscopic balloon dilation of ileal
pouch strictures. Am J Gastroenterol 2004;99:2340-7.
93. Reference removed.
94. Rutgeerts P, Geboes K, Vantrappen G, et al. Natural history of recurrent Crohn’s disease in the ileocolonic anastomosis after curative surgery. Gut 1984;25:665-72.
95. Rugeerts P, Geboes K, Vantrappen G, et al. Predicability of the postoperative course of Crohn’s disease. Gastroenterology 1990;99:95663.
96. Kornfeld D, Ekbom A, Ihre T. Is there an excess risk for colorectal
cancer in patients with ulcerative colitis and concomitant primary
sclerosing cholangitis? A population based study. Gut 1997;41:
522-5.
97. Lindberg BU, Broome U, Persson B. Proximal colorectal dysplasia or
cancer in ulcerative colitis: the impact of primary sclerosing cholangitis and sulfasalazine: results from a 20-year surveillance study. Dis
Colon Rectum 2001;444:77-85.
98. Adler DG, Baron TH, Davila RE, et al. Standards of Practice Committee
of American Society for Gastrointestinal Endoscopy, ASGE guideline:
the role of ERCP in diseases of the biliary tract and the pancreas. Gastrointest Endosc 2005;62:1-8.
99. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in
ulcerative colitis: a meta analysis. Gut 2001;48:526-35.
100. Prior P, Gyde SN, Macartney JC, et al. Cancer morbidity in ulcerative
colitis. Gut 1982;23:490-7.
101. Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients
with inflammatory bowel disease: a population-based study. Cancer
2001;91:854-62.
102. Friedman S, Rubin PH, Bodian C, et al. Screening and surveillance colonoscopy in chronic Crohn’s colitis. Gastroenterology 2001;120:820-6.
103. Itzkowitz SH, Present DH. Crohn’s and Colitis Foundation of America
Colon Cancer in IBD Study Group: consensus conference: colorectal
cancer screening and surveillance in inflammatory bowel disease. Inflamm Bowel Dis 2005;11:314-21.
104. Choi PM, Nugent FW, Schoetz DJJ, et al. Colonoscopic surveillance reduces mortality from colorectal cancer in ulcerative colitis. Gastroenterology 1993;105:418-24.
105. Eaden J, Abrams K, Ekbom A, et al. Colorectal cancer prevention in
ulcerative colitis: a case-control study. Aliment Pharmacol Ther
2000;14:145-53.
106. Reference removed.
107. Itzkowitz SH, Present DH. Crohn’s and Colitis Foundation of America
Colon Cancer in IBD Study Group. Consensus conference: colorectal
cancer screening and surveillance in inflammatory bowel disease. Inflamm Bowel Dis 2005;11:314-21.
564 GASTROINTESTINAL ENDOSCOPY Volume 63, No. 4 : 2006
www.giejournal.org
ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease
108. Eaden JA, Mayberry JF. British Society for Gastroenterology, Association of Coloproctology for Great Britan and Ireland. Guidelines for
screening and surveillance of asymptomatic colorectal cancer in
patients with inflammatory bowel disease. Gut 2002;51:v10-2.
109. Rutter MD, Saunders BP, Wilkinson KH, et al. Most dysplasia in ulcerative colitis is visible at colonoscopy. Gastrointest Endosc 2004;60:
334-9.
110. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is
a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004;126:451-9.
111. Heuschen UA, Hinz U, Allemeyer EH, et al. Backwash ileitis is strongly
associated with colorectal carcinoma in ulcerative colitis. Gastroenterology 2001;120:841-7.
112. Prior P, Gyde SN, Macartney JC, et al. Cancer morbidity in ulcerative
colitis. Gut 1982;23:490-7.
113. Odze RD, Farraye FA, Hecht JL, et al. Long-term follow-up after polypectomy treatment for adenoma-like dysplastic lesions in ulcerative
colitis. Clin Gastroeneterol Hepatol 2004;2:534-41.
114. Mpofu C, Watson AJ, Rhodes JM. Strategies for detecting colon cancer and/or dysplasia in patients with inflammatory bowel disease.
Cochrane Database Syst Rev 2004;2:CD000279.
115. Kiesslich R, Fritsch J, Holtmann M, et al. Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. Gastroenterology 2003;124:880-8.
116. Rutter MD, Saunders BP, Schofield G, et al. Pancolonic indigo carmine
dye spraying for the detection of dysplasia in ulcerative colitis. Gut
2004;53:256-60.
117. Gumaste V, Sachar DB, Greenstein AJ. Benign and malignant colorectal strictures in ulcerative colitis. Gut 1992;33:938-41.
118. Dear KL, Hunter JO. Colonoscopic hydrostatic balloon dilatation of
Crohn’s strictures. J Clin Gastroenterol 2001;33:315-8.
119. Blomberg B, Rolny P, Jarnerot G. Endoscopic treatment of anastomotic strictures in Crohn’s disease. Endoscopy 1991;23:195-8.
120. Couckuyt H, Gevers AM, Coremans G, et al. Efficacy and safety of hydrostatic balloon dilatation of ileocolonic Crohn’s strictures: a prospective longterm analysis. Gut 1995;36:577-80.
121. Thomas-Gibson S, Brooker JC, Hayward CM, et al. Colonoscopic balloon dilation of Crohn’s strictures: a review of long-term outcomes.
Eur J Gastroenterol Hepatol 2003;15:485-8.
122. Brooker JC, Beckett CG, Saunders BP, Benson MJ. Long-acting steroid
injection after endoscopic dilation of anastomotic Crohn’s strictures
may improve the outcome: a retrospective case series. Endoscopy
2003;35:333-7.
123. Ramboer C, Verhamme M, Dhondt E, et al. Endoscopic treatment of
stenosis in recurrent Crohn’s disease with balloon dilation combined
with local corticosteroid injection. Gastrointest Endosc 1995;42:252-5.
www.giejournal.org
Volume 63, No. 4 : 2006 GASTROINTESTINAL ENDOSCOPY 565
Prepared by:
STANDARDS OF PRACTICE COMMITTEE
Jonathan A. Leighton, MD
Bo Shen, MD
Todd H. Baron, MD, Vice Chair
Douglas G. Adler, MD
Raquel Davila, MD
James V. Egan, MD
Douglas O. Faigel, MD, Chair
Seng-Ian Gan, MD
William K. Hirota, MD
David Lichtenstein, MD
Waqar A. Qureshi, MD
Elizabeth Rajan, MD
Marc J. Zuckerman, MD
Trina VanGuilder, RN, SGNA Representative
Robert D. Fanelli, MD, SAGES Representative