M Guindi, R H Riddell
J Clin Pathol 2004;57:1233–1244. doi: 10.1136/jcp.2003.015214
Indeterminate colitis (IC) originally referred to those 10–
15% of cases of inflammatory bowel disease (IBD) in which
there was difficulty distinguishing between ulcerative colitis
(UC) and Crohn’s disease (CD) in the colectomy specimen.
However, IC is increasingly used when a definitive
diagnosis of UC or CD cannot be made at colonoscopy, in
colonic biopsies or at colectomy. The diagnostic difficulties
may explain the variably reported prevalence of IC.
Clinically, most patients with IC evolve to a definite
diagnosis of UC or CD on follow up. The role of ancillary
tests in the distinction of UC from CD is reviewed. The low
sensitivity of serological markers limits their usefulness.
Other tests include upper endoscopy and magnetic
resonance imaging. The definition of IC may not be a
purely histological one derived from resected specimens,
but rather a clinicopathological one. This review offers
some personal observations and viewpoints, and proposes
an approach to some of the relatively more esoteric
combinations of findings.
See end of article for
Dr M Guindi, Department
of Pathology, Toronto
General Hospital, 200
Elizabeth Street, 4th floor,
Room EC4-305, Toronto,
Ontario, Canada, M5G
Accepted for publication
1 June 2004
treatment, timing of surgery, prognosis, and
disease course. In addition, there is a need for
surveillance in UC, and possibly also in Crohn’s
colitis, because it may have a similar risk to UC.
The distinction between UC and CD usually
determines whether an ileal pouch anal anasto-
mosis (IPAA) is offered to the patient, and
correlates with the occurrence of morbidity and
complications from pouch and pouch failure.
Because there can be overlapping features of UC
and CD in the colons of some patients, the term
indeterminate colitis (IC) was coined in an
attempt to classify these entities more effectively.
Patients with indeterminate colitis appear to
have a higher rate of pouch failure and longterm
complications than those with UC.
he distinction between ulcerative colitis
(UC) and Crohn’s disease (CD) has major
implications, including the choice of medical
‘‘The distinction between ulcerative colitis and
Crohn’s disease has major implications,
including the choice of medical treatment,
timing of surgery, prognosis, and disease
This review of IC will deal with its original
definition and features, how it evolved over time,
and the controversies associated with this evolu-
tion. The incidence, prevalence, and clinical
evolution of IC will be followed by a detailed
discussion of the settings that give rise to the
diagnosis of IC, and the problems and pitfalls
associated with them, including variations of
inflammatory bowel disease (IBD), both UC and
colitis of CD, which can be mistaken for IC. These
include the more common features such as IBD
in the fulminant or refractory phase, but also IBD
in the chronic phase, and the effects of treatment
on the histology of IBD, especially UC, which can
result in pronounced focality, relative rectal
sparing, and focal healing. The issues of inter-
observer variability in the diagnosis and classi-
fication of IBD and colitis as a result of causes
other than UC or CD are discussed. Recent
developments, and the usefulness of ancillary
tests that are potentially helpful, in the further
classification of IC are summarised, with special
reference to serological markers and the role of
upper endoscopy. The outcome of ileoanal pouch
construction in IC is also discussed.
DEFINITIONS AND FEATURES
UC characteristically affects the rectum, involves
the colon contiguously and symmetrically, and
the disease is more severe distally. Crohn’s colitis
is not continuous or symmetrical, and need not
involve the rectum.1–5In 1978, Price introduced
the term IC to refer to a subgroup of approxi-
mately 10–15% of IBD cases in which there
was difficulty in distinguishing between UC
and CD in the excised colectomy specimen
because the features of typical severe UC were
replaced by deep ulcers—often with knife-like
fissures—relative rectal sparing, and transmural
Table 1 summarises the histological features
and incidence of discriminating attributes in
Price’s UC, CD, and IC groups.
Idiopathic granulomas were only present in
CD. Typical CD fissuring-type ulcerations (mostly
single and narrow) were present in 13% of cases
of IC, but the other histological features of these
IC cases were reportedly so atypical that a
diagnosis of CD could not be justified. A second
form of fissuring ulceration, V shaped clefts,
usually multiple, was present in 60% of cases of
IC, and appeared to be a feature of any form of
fulminant colitis. Transmural lymphoid aggre-
gates, a feature accepted as very important in the
diagnosis of CD, was present in 6% of cases of IC,
Abbreviations: ASCA, anti-Saccharomyces cervisiae
antibodies; ASLC, acute self limited colitis; CD, Crohn’s
disease; DDAC, diverticular disease associated colitis;
IBD, inflammatory bowel disease; IC, indeterminate
colitis; IPAA, ileal pouch anal anastomosis; NSAID, non-
steroidal anti-inflammatory drug; P-ANCA, perinuclear
antineutrophil cytoplasmic antibodies; UC, ulcerative
but were poorly developed. Transmural inflammation was
present in most cases of IC, but was only related to areas of
severe ulceration. The mucosal glandular pattern/architecture
and goblet cell population were obscured or modified by
extensive ulceration in the IC cases. The islands of surviving
mucosa were only mildly inflamed, with a regular glandular
pattern and preserved goblet cells—features that favoured
CD, or disease in mucosa that was previously unaffected by
the disease process, conceivably including fulminant infec-
tions by organisms that were not identified on routine stool
culture. However, these features were present in cases where
the cumulative evidence was unclear, and two thirds of these
proved to be UC on subsequent follow up in Price’s series.7
‘‘The presence of scattered mononuclear inflammatory
cells in the muscularis propria adjacent to ulceration was
regarded as a non-specific response, and not a discrimi-
nating feature between ulcerative colitis and Crohn’s
Approximately a half of the cases of IC described by Price6
had uneven disease that fell into two patterns, both of which
would normally bias towards CD (table 2).
In the subgroup with relative rectal sparing, the description
of the rectal mucosa was not very detailed. The rectal mucosa
was described as being ‘‘mildly abnormal’’ on histological
examination in all seven cases. In the three judged to be
probably UC, glandular irregularity was noted. In the
remainder of the IC cases with relative rectal sparing, the
inflammation was described as mild, without specific
reference to the presence or absence of basal plasmacytosis
or architectural distortion. The second pattern was of
intermittent ulceration and superficially resembled the skip
lesions of CD.
Lee et al found IC in 16% of colectomy specimens.8Some of
the features of IC they described are similar to those of Price
et al, such as normal or minimally altered colonic mucosa
adjacent to or between ulcers and the absence of granulomas.
They described deep slit-like fissures in the IC cases, but did
not specifically describe the V shaped cleft-like fissures seen
in IC by Price, although these may just be synonyms. They
also emphasised that the term ‘‘transmural inflammation’’, a
feature of CD, is loosely used and that accurate definition of
this criterion removes much of the difficulty from the
differential diagnosis of IBD. They defined transmural
inflammation as lymphocytes in an aggregated pattern in
all layers of the colon, including the serosa. The presence of
scattered mononuclear inflammatory cells in the muscularis
propria adjacent to ulceration was regarded as a non-specific
response, and not a discriminating feature between UC and
CD. Their IC cases contained scattered non-aggregated
inflammatory cells involving the full thickness of the bowel
wall, but only in those areas deep to ulceration. Unlike Price’s
series, all their patients had an acute onset and required
urgent colectomy after a short period of unsuccessful medical
THE EVOLUTION OF IC
The term IC is increasingly being used clinically and
histologically in patients with some form of IBD in whom a
definitive diagnosis of either UC or CD has not been made,
either on colonoscopy or colonic biopsy before colectomy. IC
may not be a purely histological entity, but rather a
Incidence of discriminating histological features in UC, CD, and IC*
Urgent surgery Elective surgeryUrgent surgery Elective surgery
V shaped clefts
Normal goblet cells, regular gland pattern, and focal mucosal
Goblet cell depletion, glandular irregularity, ¡ diffuse mucosal
Feature suggestive of acute disease ¡ dilatation
Myocytolysis and capillary congestion
V shaped clefts
*Modified from Price.
CD, Crohn’s disease; ID, indeterminate colitis; UC, ulcerative colitis.
indeterminate colitis from Price6
Findings in uneven disease pattern in
Uneven pattern (n=14)
Relative rectal sparing
Number of cases
UC more likely
CD more likely
Not specifically mentioned
Mild inflammation in all
CD, Crohn’s disease; UC, ulcerative colitis.
congested and less diseased appearing mucosa at the distal end of the
colon, compared with the erythematous ulcerated colonic mucosa seen
more proximally. In the right colon, the transition from normal to
diseased mucosa is irregular and patchy.
Relative distal sparing. Colectomy specimen showing less
IBD in biopsy specimens is uncertain, it is better to call it
‘‘IBD of uncertain subtype’’ or ‘‘IBD not yet classified’’, and if
uncertain of IBD, a descriptive diagnosis may be appropriate.
M Guindi, Department of Laboratory Medicine and Pathobiology,
University of Toronto, and Department of Pathology, University Health
Network, Toronto, Ontario, Canada, M5G 2C4
R H Riddell, Department of Pathology, Mount Sinai Hospital, Toronto,
1 Lewin KJ, Riddell RH, Weinstein WM. Gastrointestinal pathology and its
clinical implications. New York: Igaku-Shoin, 1992.
2 Tanaka M, Riddell RH, Saito H, et al. Morphologic criteria applicable to
biopsy specimens for effective distinction of inflammatory bowel disease from
other forms of colitis and of Crohn’s disease from ulcerative colitis.
Scand J Gastroenterol 1999;34:55–67.
3 Riddell RH. Histopathology of ulcerative colitis. In: Allan RN, Rhodes JM,
Hanauer SB, et al, eds. Inflammatory bowel disease, 3rd ed. New York:
4 Goldblum JK, Petras RE. Histopathology of Crohn’s disease. In: Allan RN,
Rhodes JM, Hanauer SB, et al, eds. Histopathology of Crohn’s disease, 3rd
ed. New York: Churchill-Livingstone, 1997:311–15.
5 Schachter H, Kirsner JB. Definitions of inflammatory bowel disease of
unknown etiology. Gastroenterology 1975;68:591–600.
6 Price AB. Overlap in the spectrum of non-specific inflammatory bowel
disease: colitis indeterminate. J Clin Pathol 1978;31:567–77.
7 Wells AD, McMillan I, Price AB, et al. Natural history of indeterminate colitis.
Br J Surg 1991;78:179–81.
8 Lee KS, Medline A, Shockey S. Indeterminate colitis in the spectrum of
inflammatory bowel disease. Arch Pathol Lab Med 1979;103:173–6.
9 Nicholls RJ, Wells AD. Indeterminate colitis. Baillieres Clin Gastroenterol
10 Rudolph WG, Uthoff SM, McAuliffe TL, et al. Indeterminate colitis: the real
story. Dis Colon Rectum 2002;45:1528–34.
11 Swan NC, Geoghegan JG, O’Donoghue DP, et al. Fulminant colitis in
inflammatory bowel disease: detailed pathologic and clinical analysis. Dis
Colon Rectum 1998;41:1511–15.
12 Mahadeva U, Martin JP, Patel NK, et al. Granulomatous ulcerative colitis: a
re-appraisal of the mucosal granuloma in the distinction of Crohn’s disease
from ulcerative colitis. Histopathology 2002;41:50–5.
13 Lee FD, Maguire C, Obeidat W, et al. Importance of cryptolytic lesions and
pericryptal granulomas in inflammatory bowel disease. J Clin Pathol
14 Bernstein CN, Shanahan F, Anton PA, et al. Patchiness of mucosal
inflammation in treated ulcerative colitis: a prospective study. Gastrointest
15 Bernstein CN, Shanahan F, Weinstein WM. Histological patchiness and
sparing of the rectum in ulcerative colitis: refuting the dogma. J Clin Pathol
16 Kleer CG, Appelman HD. Ulcerative colitis: patterns of involvement with
colorectal biopsies and changes with time. Am J Surg Pathol
17 Levine TS, Tzardi M, Mitchell S, et al. Diagnostic difficulty arising from rectal
recovery in ulcerative colitis. J Clin Pathol 1996;49:319–23.
18 Spiliadis CA, Lennard-Jones JE. Ulcerative colitis with relative sparing of the
rectum. Clinical features, histology, and prognosis. Dis Colon Rectum
19 Hamilton SR. Diagnosis comparison of ulcerative colitis and Crohn’s disease
involving the colon. In: Norris HT, ed. Pathology of the colon, small intestine
and anus. New York: Churchill Livingstone, 1983:1–19.
20 Hamilton SR. The differential diagnosis of idiopathic inflammatory disease
by colorectal biopsy. Int J Colorectal Dis 1987;2:113–17.
21 Greenson J, Odze R. Inflammatory bowel disease of the large intestine. In:
Odze RD, Goldblum JR, Crawford JM, eds. Surgical pathology of the GI
tract, liver, biliary tract, and pancreas. Philadelphia, Pennsylvania:
22 D’Haens G, Geboes K, Peeters M, et al. Patchy cecal inflammation
associated with distal ulcerative colitis: a prospective endoscopic study.
Am J Gastroenterol 1997;92:1275–9.
23 Okawa K, Aoki T, Sano K, et al. Ulcerative colitis with skip lesions at the
mouth of the appendix. Am J Gastroenterol 1998;93:2405–10.
24 Yang SK, Jung HY, Kang GH, et al. Appendiceal orifice inflammation as a
skip lesion in ulcerative colitis: an analysis in relation to medical therapy and
disease extent. Gastrointest Endosc 1999;49:743–77.
25 Mutinga M, Farraye F, Wang H, et al. Clinical significance of right colonic
inflammation in patients with left sided chronic ulcerative colitis [abstract].
26 Davison AM, Dixon MF. The appendix as a ‘‘skip lesion’’ in ulcerative colitis.
27 Groisman GM, George J, Harpaz N. Ulcerative appendicitis in universal and
nonuniversal ulcerative colitis. Mod Pathol 1994;7:322–35.
28 Saltzstein SL, Rosenberg BF. Ulcerative colitis of the ileum, and regional
enteritis of the colon; a comparative histological study. Am J Clin Pathol
29 Gustavsson S, Weiland LH, Kelly KA. Relationship of backwash ileitis to ileal
pouchitis after ileal pouch–anal anastomosis. Dis Colon Rectum
30 Schmidt CM, Lazenby AJ, Hendrickson RJ, et al. Preoperative terminal ileal
and colonic resection histopathology predicts risk of pouchitis in patients after
ileoanal pull-through procedure. Ann Surg 1998;227:654–62.
31 Kim B, Barnett JL, Kleer CG, et al. Endoscopic and histological patchiness in
treated ulcerative colitis. Am J Gastroenterol 1999;94:3258–62.
32 Odze R, Antonioli D, Peppercorn M, et al. Effects of topical 5-aminosalicylic
acid (5-ASA) therapy on rectal mucosal biopsy morphology in chronic
ulcerative colitis. Am J Surg Pathol 1993;17:869–75.
33 Geboes K, Dalle I. Influence of treatment on morphological features of
mucosal inflammation. Gut 2002;50(suppl 3):II37–42.
34 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.
35 Driman DK, Preiksaitis HG. Colorectal inflammation and increased cell
proliferation associated with oral sodium phosphate bowel preparation
solution. Hum Pathol 1998;29:972–8.
36 Schumacher G, Kollberg B, Sandstedt B. A prospective study of first attacks of
inflammatory bowel disease and infectious colitis. Histologic course during
the 1st year after presentation. Scand J Gastroenterol 1994;29:318–32.
37 Washington K, Greenson JK, Montgomery E, et al. Histopathology of
ulcerative colitis in initial rectal biopsy in children. Am J Surg Pathol
38 Tang LH, Reyes-Mugica M, Hao L, et al. Histologic differences between
children and adults presenting with ulcerative colitis [abstract]. Mod Pathol
Take home messages
N The settings that give rise to the diagnosis of
indeterminate colitis (IC) include confounding histolo-
gical features of inflammatory bowel disease (IBD) in
the fulminant or refractory phase, IBD in the chronic
phase, the effects of treatment on the histology of IBD,
unusual patterns of ulcerative colitis (UC), observer
bias, colitis not caused by UC or Crohn’s disease (CD),
and non-specific fulminant colitis
N The distinction between CD and UC rests with the
weight of evidence derived from a pattern of inflam-
mation and a constellation of findings in a given case
N It is preferable to reserve the term IC for colectomy
N When faced with difficulties in classifying IBD into CD
or UC in biopsies, the term IC should not be used. We
prefer to use the term ‘‘IBD, not yet classified’’ or
‘‘colitis of uncertain aetiology’’. This designation leaves
the door open for biopsy classification of IBD in repeat
or future biopsies or resections, or from other clinical
N The diagnosis of IC in a colectomy specimen in a given
patient may stand as the clinical diagnosis indefinitely,
or may change to UC or CD if and when additional
evidence for one or the other becomes available with
N Serological markers, anti-Saccharomyces cervisiae
and perinuclear antineutrophil cytoplasmic antibodies,
have been suggested as a method for differentiating
UC from CD, but their sensitivity is only 40–60%,
limiting their clinical usefulness. They tend to be non-
contributory when most needed
N IC should not be regarded as a contraindication for
ileal pouch anal anastomosis (IPAA). The overall
higher rate of severe pouch complications in patients
with IC compared with those with UC and IPAA may
result from the heterogeneity of patients designated as
having IC in different series, such that they frequently
represent an admixture of patients with UC and CD
39 Markowitz J, Kahn E, Grancher K, et al. Atypical rectosigmoid histology in
children with newly diagnosed ulcerative colitis. Am J Gastroenterol
40 Glickman J, Bousvaros A, Farraye F. Relative rectal sparing and skip lesions
are not uncommon at initial presentation in pediatric patients with chronic
ulcerative colitis [abstract]. Mod Pathol 2002;15:127A.
41 Glickman J, Bousvaros A, Farraye F. Relative rectal sparing and skip lesions
are not uncommon at initial presentation in pediatric patients with chronic
ulcerative colitis [abstract]. Mod Pathol 2002;15:127A.
42 Moum B, Ekbom A, Vatn MH, et al. Inflammatory bowel disease: re-
evaluation of the diagnosis in a prospective population based study in south
eastern Norway. Gut 1997;40:328–32.
43 Evans JM, McMahon AD, Murray FE, et al. Non-steroidal anti-inflammatory
drugs are associated with emergency admission to hospital for colitis due to
inflammatory bowel disease. Gut 1997;40:619–22.
44 Faucheron JL, Parc R. Non-steroidal anti-inflammatory drug-induced colitis.
Int J Colorectal Dis 1996;11:99–101.
45 Tanaka M, Riddell RH. The pathological diagnosis and differential diagnosis
of Crohn’s disease. Hepatogastroenterology 1990;37:18–31.
46 Kumar NB, Nostrant TT, Appelman HD. The histopathologic spectrum of
acute self-limited colitis (acute infectious-type colitis). Am J Surg Pathol
47 Surawicz CM, Belic L. Rectal biopsy helps to distinguish acute self-limited
colitis from idiopathic inflammatory bowel disease. Gastroenterology
48 Le Berre N, Heresbach D, Kerbaol M, et al. Histological discrimination of
idiopathic inflammatory bowel disease from other types of colitis. J Clin
49 Makapugay LM, Dean PJ. Diverticular disease-associated chronic colitis.
Am J Surg Pathol 1996;20:94–102.
50 Shepherd NA. Diverticular disease and chronic idiopathic inflammatory
bowel disease: associations and masquerades. Gut 1996;38:801–2.
51 Goldstein NS, Leon-Armin C, Mani A. Crohn’s colitis-like changes in sigmoid
diverticulitis specimens is usually an idiosyncratic inflammatory response to
the diverticulosis rather than Crohn’s colitis. Am J Surg Pathol
52 Gledhill A, Dixon MF. Crohn’s-like reaction in diverticular disease. Gut
53 Burroughs SH, Bowrey DJ, Morris-Stiff GJ, et al. Granulomatous
inflammation in sigmoid diverticulitis: two diseases or one? Histopathology
54 Gupta J, Shepherd NA. Colorectal mass lesions masquerading as chronic
inflammatory bowel disease on mucosal biopsy. Histopathology
55 Tendler DA, Aboudola S, Zacks JF, et al. Prolapsing mucosal polyps: an
underrecognized form of colonic polyp—a clinicopathological study of 15
cases. Am J Gastroenterol 2002;97:370–6.
56 Gurudu S, Fiocchi C, Katz JA. Inflammatory bowel disease. Best Pract Res
Clin Gastroenterol 2002;16:77–90.
57 Brandt L, Boley S, Goldberg L, et al. Colitis in the elderly. A reappraisal.
Am J Gastroenterol 1981;76:239–45.
58 Bharucha AE, Tremaine WJ, Johnson CD, et al. Ischemic proctosigmoiditis.
Am J Gastroenterol 1996;91:2305–9.
59 Tsang P, Rotterdam H. Biopsy diagnosis of colitis: possibilities and pitfalls.
Am J Surg Pathol 1999;23:423–30.
60 Theodossi A, Spiegelhalter DJ, Jass J, et al. Observer variation and
discriminatory value of biopsy features in inflammatory bowel disease. Gut
61 Farmer M, Petras RE, Hunt LE, et al. The importance of diagnostic accuracy in
colonic inflammatory bowel disease. Am J Gastroenterol 2000;95:3184–8.
62 Bentley E, Jenkins D, Campbell F, et al. How could pathologists improve the
initial diagnosis of colitis? Evidence from an international workshop. J Clin
63 Kangas E, Matikainen M, Mattila J. Is ‘‘indeterminate colitis’’ Crohn’s
disease in the long-term follow-up? Int Surg 1994;79:120–3.
64 Shivananda S, Lennard-Jones J, Logan R, et al. Incidence of inflammatory
bowel disease across Europe: is there a difference between north and south?
Results of the European collaborative study on inflammatory bowel disease
(EC-IBD). Gut 1996;39:690–7.
65 Moum B, Vatn MH, Ekbom A, et al. Incidence of ulcerative colitis and
indeterminate colitis in four counties of southeastern Norway, 1990–93—a
prospective population-based study. Scand J Gastroenterol 1996;31:362–6.
66 Martinez-Salmeron JF, Rodrigo M, de Teresa J, et al. Epidemiology of
inflammatory bowel disease in the province of Granada, Spain: a
retrospective study from 1979 to 1988. Gut 1993;34:1207–9.
67 Russel MGVM, Dorant E, Volovics A, et al. High incidence of inflammatory
bowel disease in the Netherlands—results of a prospective study. Dis Colon
68 Meucci G, Bortoli A, Riccioli FA, et al. Frequency and clinical evolution of
indeterminate colitis: a retrospective multi-centre study in northern Italy.
GSMII (Gruppo di Studio per le Malattie Infiammatorie Intestinali).
Eur J Gastroenterol Hepatol 1999;11:909–13.
69 Hildebrand H, Fredrikzon B, Holmquist L, et al. Chronic inflammatory bowel
disease in children and adolescents in Sweden. J Pediatr Gastroenterol Nutr
70 Quinton JF, Sendid B, Reumaux D, et al. Anti-Saccharomyces cerevisiae
mannan antibodies combined with antineutrophil cytoplasmic autoantibodies
in inflammatory bowel disease: prevalence and diagnostic role. Gut
71 Zachos M, Reumaux D, Critch J, et al. Clinical utility of ASCA and ANCA in
pediatric colitis. J Pediatr Gastroenterol Nutr 2001;33:378–81.
72 Legnani PE, Kornbluth A. Difficult differential diagnoses in IBD: ileitis and
indeterminate colitis. Semin Gastrointest Dis 2001;12:211–22.
73 Targan SR. The utility of ANCA and ASCA in inflammatory bowel disease.
Inflamm Bowel Dis 1999;5:61–3.
74 MacDermott RP. Lack of current clinical value of serological testing in the
evaluation of patients with IBD. Inflamm Bowel Dis 1999;5:64–5.
75 Present DH, Banks PA. The role of pANCA and ASCA in differentiating
ulcerative colitis, Crohn’s disease, and indeterminate colitis. Inflamm Bowel
76 Joossens S, Reinisch W, Vermeire S, et al. The value of serologic markers in
indeterminate colitis: a prospective follow-up study. Gastroenterology
77 Tobin JM, Sinha B, Ramani P, et al. Upper gastrointestinal mucosal disease in
pediatric Crohn’s disease and ulcerative colitis: a blinded, controlled study.
J Pediatr Gastroenterol Nutr 2001;32:443–8.
78 Kaufman SS, Vanderhoof JA, Young R, et al. Gastroenteric inflammation in
children with ulcerative colitis. Am J Gastroenterol 1997;92:1209–12.
79 Sasaki M, Okada K, Koyama S, et al. Ulcerative colitis complicated by
gastroduodenal lesions. J Gastroenterol 1996;31:585–9.
80 Honma J, Mitomi H, Murakami K, et al. Nodular duodenitis involving CD8+
cell infiltration in patients with ulcerative colitis. Hepatogastroenterology
81 Kundhal PS, Stormon MO, Zachos M, et al. Gastral antral biopsy in the
differentiation of pediatric colitides. Am J Gastroenterol 2003;98:557–61.
82 Valdez R, Appelman HD, Bronner MP, et al. Diffuse duodenitis associated
with ulcerative colitis. Am J Surg Pathol 2000;24:1407–13.
83 Schmitz-Moormann P, Malchow H, Pittner PM. Endoscopic and bioptic study
of the upper gastrointestinal tract in Crohn’s disease patients. Pathol Res
84 Parente F, Cucino C, Bollani S, et al. Focal gastric inflammatory infiltrates in
inflammatory bowel diseases: prevalence, immunohistochemical
characteristics, and diagnostic role. Am J Gastroenterol 2000;95:705–11.
85 Wright CL, Riddell RH. Histology of the stomach and duodenum in Crohn’s
disease. Am J Surg Pathol 1998;22:383–90.
86 Meining A, Bayerdo ¨rffer E, Ba ¨stlein E, et al. Focal inflammatory infiltrations
in gastric biopsy specimens are suggestive of Crohn’s disease.
Scand J Gastroenterol 1997;32:813–18.
87 Oberhuber G, Puspok A, Oesterreicher C, et al. Focally enhanced gastritis: a
frequent type of gastritis in patients with Crohn’s disease. Gastroenterology
88 Sharif F, McDermott M, Dillon M, et al. Focally enhanced gastritis in children
with Crohn’s disease and ulcerative colitis. Am J Gastroenterol
89 Oberhuber G, Hirsch M, Stolte M. High incidence of upper gastrointestinal
tract involvement in Crohn’s disease. Virchows Arch 1998;432:49–52.
90 Durno CA, Sherman P, Williams T, et al. Magnetic resonance imaging to
distinguish the type and severity of pediatric inflammatory bowel diseases.
J Pediatr Gastroenterol Nutr 2000;30:170–14.
91 Bezabeh T, Somorjai RL, Smith IC, et al. The use of 1H magnetic resonance
spectroscopy in inflammatory bowel diseases: distinguishing ulcerative colitis
from Crohn’s disease. Am J Gastroenterol 2001;96:442–8.
92 Wolff BG. Is ileoanal the proper operation for indeterminate colitis: the case
for. Inflamm Bowel Dis 2002;8:362–5.
93 Schoetz DJJ. Is ileoanal the proper operation for indeterminate colitis: the
case against. Inflamm Bowel Dis 2002;8:366–7.
94 Pezim ME, Pemberton JH, Beart RW, et al. Outcome of ‘‘indeterminant’’
colitis following ileal pouch–anal anastomosis. Dis Colon Rectum
95 McIntyre PB, Pemberton JH, Wolff BG, et al. Indeterminate colitis. Long-term
outcome in patients after ileal pouch–anal anastomosis. Dis Colon Rectum
96 Yu CS, Pemberton JH, Larson D. Ileal pouch–anal anastomosis in patients
with indeterminate colitis: long-term results. Dis Colon Rectum
97 Delaney CP, Remzi FH, Gramlich T, et al. Equivalent function, quality of life
and pouch survival rates after ileal pouch–anal anastomosis for
indeterminate and ulcerative colitis. Ann Surg 2002;236:43–8.
98 Koltun WA, Schoetz DJJ, Roberts PL, et al. Indeterminate colitis predisposes
to perineal complications after ileal pouch–anal anastomosis. Dis Colon
99 Marcello PW, Schoetz DJ Jr, Roberts PL, et al. Evolutionary changes in the
pathologic diagnosis after the ileoanal pouch procedure. Dis Colon Rectum
100 Rauh SM, Schoetz DJJ, Roberts PL, et al. Pouchitis—is it a wastebasket
diagnosis? Dis Colon Rectum 1991;34:685–9.
101 Gramlich T, Delaney CP, Lynch AC, et al. Pathological subgroups may
predict complications but not late failure after ileal pouch–anal anastomosis
for indeterminate colitis. Colorectal Dis 2003;5:315–19.
102 Hanby AM, Wright NA. The ulcer-associated cell lineage: the
gastrointestinal repair kit? J Pathol 1993;171:3–4.
103 Price AB. Indeterminate colitis—broadening the perspective. Curr Diagn