Classification of small bowel Crohn’s subtypes based on

multimodality imaging

Dean D.T. Maglinte, MDa,*, Nicholas Gourtsoyiannis, MDb,Douglas Rex, MD, FACGc, Thomas J. Howard, MD, FACSd,

Frederick M. Kelvin, MDe

aDepartment of Radiology, Indiana University School of Medicine, University Hospital and Outpatient Center,

550 North University Boulevard, Room 0279, Indianapolis, IN 46202-5253, USAbDepartment of Radiology, University Hospital of Heraklion, Faculty of Medicine, University of Crete, Crete, Greece

cDivision of Gastroenterology and Hepatology, Indiana University School of Medicine,

University Hospital and Outpatient Center, 550 North University Boulevard, Room 0279, Indianapolis, IN 46202-5253, USAdDivision of Surgery, Indiana University School of Medicine, University Hospital and Outpatient Center,

550 North University Boulevard, Room 0279, Indianapolis, IN 46202-5253, USAeDepartment of Radiology, Methodist Hospital of Indiana, 1701 North Senate Boulevard, Indianapolis, IN 46202, USA

Crohn’s disease is a chronic, segmental, trans-

mural inflammatory disorder that frequently involves

the small bowel. The disease has a distinct tendency

to recur and result in complications such as

abscesses and fistulae. Its etiology is unknown,

although there is mounting evidence that the con-

dition represents an abnormal mucosal response to

unknown luminal antigens [1]. Crohn’s disease most

commonly affects the terminal ileum and proximal

colon, although it can occur anywhere in the gastro-

intestinal tract from the mouth to the anus. Radio-

logic evaluation remains of particular importance

when involvement is confined to or involves the

mesenteric small intestine between the ligament of

Trietz and the ileocecal valve, because this part of

the gastrointestinal tract is not generally evaluable

endoscopically [2,3]. Barium examinations, includ-

ing small bowel follow-through, enteroclysis, and

CT are the main radiologic techniques used to

show the various manifestations of Crohn’s disease

[3–20]. More recently, CT enteroclysis has been

developed and employed in patients with Crohn’s

disease [21,25]. MR imaging currently is being

studied in the small bowel and holds great promise

for the evaluation of this disease [26,30].

Crohn’s disease is unpredictable in both its clin-

ical presentation and evolution. Its variable behavior

has led investigators to classify the disease into

subtypes that include active inflammatory, fibroste-

nosing, and fistulizing/perforating categories. Clas-

sification of patients by subtype has clinical utility

because accurate classification can help to guide

decisions regarding medical and surgical therapy.

Classification of subtypes requires accurate informa-

tion concerning the presence of ulceration, edema,

spasm, stricture, fistula formation, and associated

inflammatory mass. For the small bowel, this

information is traditionally provided by barium

examination and CT. Newer techniques such as enter-

oclysis, multislice CT, MR imaging, CT enteroclysis,

and MR enteroclysis are now increasingly used in

clinical practice and provide additional detail that is

useful for the accurate classification of subtypes. This

article provides a pictorial atlas of the imaging find-

ings that distinguish the subtypes of Crohn’s disease

as they are seen in the small bowel utilizing conven-

tional and newer imaging technologies. The rel-

0033-8389/03/$ – see front matter D 2003, Elsevier Science (USA). All rights reserved.

doi:10.1016/S0033-8389(02)00117-3

* Corresponding author.

E-mail address: dmaglint@iupui.edu (D.D.T. Maglinte).

Radiol Clin N Am 41 (2003) 285–303

evance to clinical management of this morphologic

imaging-based classification scheme is discussed.

Imaging classification of small bowel

Crohn’s disease

The management of Crohn’s disease continues to

evolve both medically and surgically [1]. Classifica-

tion of disease activity in Crohn’s disease based

solely on clinical and laboratory parameters has not

been clinically reproducible [31,32]. The use of

imaging findings as part of the information that

supports the classification of a given disease sub-

type has the potential to make the classification

system more objective and reproducible. An

imaging-based classification system of Crohn’s dis-

ease subtypes can help clinicians to plan appropriate

therapy. For example, obstruction caused by active

inflammation may respond to intensive medical ther-

apy, whereas obstruction due to a fibrotic stricture is

generally unresponsive and frequently requires sur-

gical intervention (resection, stricturoplasty), pro-

vided there is no acute inflammation or phlegmon

at the strictured site.

The imaging classification presented in this

pictorial review (Table 1) represents a combination

of a clinical classification scheme based on disease

behavior [31,32] and a radiographic classification

scheme based on both degree of involvement and

anatomic extent of disease as seen on barium

examination supplemented by newer imaging tech-

nologies [33]. A characteristic feature of Crohn’s

disease of the small bowel is the wide variety of

radiologic features and multiplicity of abnormalities

that can be present in any individual patient. Fig. 1

is a diagram depicting the evolution and complex-

ity of the course of Crohn’s disease. Disease

progression is often influenced by disease severity

and by clinical intervention [31,32]. More than one

subtype of the disease process may be noted in a

segment or in multiple adjacent segments in the

same patient.

Active inflammatory disease subtype

The active inflammatory subtype of Crohn’s dis-

ease is characterized by focal inflammation, super-

ficial (aphthoid) and deep ulcers, an often transmural

inflammatory reaction with lymphoid aggregates and

granuloma formation. Minimal inflammatory activity

is characterized on barium examinations as blunting,

thickening, straightening, or distortion of the small

bowel folds secondary to edema [34,35]. Subtle

minimal bowel wall thickening may be seen. Small

ulcers can be shown by carefully performed radio-

logic examinations. Barium examination, particularly

air enteroclysis, is superior to other imaging studies

with regard to diagnosis in this subtype [9], although

early experience shows that MR enteroclysis may

also be more effective in the demonstration of

minimal disease [30]. The typical findings on barium

examination of minimal active inflammatory subtype

are shown in Fig. 2. The air double-contrast entero-

clysis method shows subtle surface changes—such as

mucosal granularity and aphthae—better than do

other radiologic methods, but consistently reliable

images may be more difficult to obtain [36] (Fig. 3;

see also Fig. 4D in the article by Maglinte et al

entitled ‘‘Technical Refinements in Enteroclysis,’’

this issue).

The subtle findings at CT in this subtype are

minimal and nonspecific (Fig. 4). Small ulcers or

aphthae are not shown by CT. Mucosal hyperemia

and mild submucosal edema are better evaluated by

multidetector intravenous (IV) contrast-enhanced CT

Table 1

Radiologic classification of small bowel Crohn’s disease

Active inflammatory subtype

Minimal changes

Superficial ulcerations (aphthae)

Minimal fold thickening or distortion (edema)

Severe changes

Deep ulcers, cobblestone mucosa (longitudinal and

transverse ulcers)

Marked wall thickening due to transmural

inflammation (mural stratification and target sign)

Obstruction secondary to spasm

‘‘Comb sign’’

Fibrostenotic subtype

Minimal stenosis

Minimal decrease in luminal diameter, mild

prestenotic dilatation

Minimal wall thickening, no bowel wall edema

Severe stenosis

Marked decrease in luminal diameter, with obvious

prestenotic dilatation

Marked wall thickening of soft tissue density, no

mural edema

Fistulizing/perforating subtype

Deep fissuring ulcers, sinus tracts

Fistulae to adjacent organs, bowel, skin

Associated inflammatory mass

Reparative or regenerative subtype

Mucosal atrophy

Regenerative polyps

Minimal decrease in luminal diameter—no mural edema

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303286

Fig. 1. Complexity of course of Crohn’s disease of the small bowel.

Fig. 2. Active inflammatory subtype, minimal changes. Findings on barium examination. (A) Enteroclysis of an 18-year-old

female with recurrent lower abdominal pain and diarrhea shows minimal diffuse fold abnormality (thickening and prominent

lymphoid follicles) in the terminal ileum with the scattered small ulcers (arrow in one). Colonoscopy to the terminal ileum

showed multiple aphthae. C, cecum. (B) Enteroclysis of a 28-year-old male with acute abdominal pain and diarrhea shows

thickened slightly irregular folds consistent with submucosal edema (arrow). No ulcers are demonstrated, but endoscopy

showed ulcerations. (From Maglinte DDT, Chernish SM, Kelvin FM, et al. Crohn disease of the small intestine: accuracy and

relevance of enteroclysis. Radiology 1992;184:541–5; with permission.)

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 287

anteroclysis with methylcellulose as intraluminal con-

trast agent [25]. Because conventional CTexamination

commonly is performed first in the evaluation of a

patient with known or suspected Crohn’s disease,

radiologists should recognize the mild subtle thick-

ening that should lead to a confirmatory examination.

Severe inflammatory activity is characterized

on barium examinations by deep ulcers seen as

contrast collections or marginal addition defects

(protrusion) in a thickened bowel wall or as a

‘‘cobblestone mucosa’’ (Fig. 5). The cobblestone

mucosa reflects severe edema between longitudinal

and transverse ulcerations that result in a cobblestone

street-like appearance of the mucosa. This cobble-

stone mucosa appears similar on both barium exam-

ination and CT enteroclysis with positive enteral

contrast (Fig. 6).

Unlike mild inflammatory disease activity, the

changes of severe inflammatory disease activity on

CT are easily appreciated. Contrast-enhanced CT

with positive intraluminal and IV contrast enhance-

ment will show moderate to marked bowel wall

thickening. The deep ulcers are manifested by

enteral contrast protrusions into the edematous wall

(Fig. 7). The demonstration on IV contrast-enhanced

CT of ‘‘mural stratification’’ indicates edema from

active inflammation [11]. This mural stratification is

composed of an inner ring of mucosal enhancement

surrounded by an outer ring of muscular and serosal

enhancement, with an intermediate low-density ring

due to submucosal edema [11,19,20]. The enhancing

layers reflect underlying active inflammatory dis-

ease. With effective treatment, the stratification

diminishes or resolves. When positive oral contrast

is used in CT with IV contrast, the inner ring of

mucosal enhancement is isoattenuated by the density

of the luminal contrast, but still can be faintly

discerned (Fig. 8). The ‘‘target’’ or ‘‘halo’’ sign

from active inflammatory disease subtype should

be differentiated from the ‘‘halo’’ produced by

submucosal fat deposition seen in chronic disease

(Fig. 9). Although mucosal hyperemia may not be

appreciated readily when positive intraluminal con-

trast is used, presence of the ‘‘comb sign’’ suggests

perienteric hyperemia and bowel wall inflammation

(Fig. 10) [37]. The comb sign should be differentiated

from mesenteric stranding that does not necessarily

indicate inflammation.

MR enteroclysis may disclose similar appearances

of the inflamed, thickened bowel wall after gadolin-

ium IVadministration (Fig. 11). A hyperemic mucosal

layer is identified by its high signal intensity due to

increased gadolinium uptake, whereas submucosal

edema has a low signal intensity, surrounded by a

seromuscular layer with moderate signal intensity that

results in a ‘‘target-type’’ configuration. The signal

intensity on postgadolinium T1-weighted images of

the thickened bowel wall is considered to be an

indicator of disease activity [38,39]. In addition, MR

enteroclysis demonstrates mesenteric inflammatory

changes in the form of vascular engorgement, the

comb sign, and lymphadenopathy in patients with

active Crohn’s disease (Fig. 12). The comb sign,

which corresponds to increased mesenteric vascular-

ity, can be seen ideally on true fast imaging with

steady-state free precession (FISP) images close to the

mesenteric border of a small bowel segment in the

form of short, parallel, low signal intensity, linear

structures perpendicular to the intestinal long axis of

the bowel [30]. Small mesenteric lymph nodes are

easily detected by their low signal intensity scattered

within the bright mesenteric fat on true FISP images.

The presence of lymph nodes is not as obvious with

the use of other MR enteroclysis sequences because of

short T2 filtering effects on half-Fourier acquisition

single-shot turbo spin echo (HASTE) images and to

saturation effects of mesenteric fat signal on three-

Fig. 3. Double-contrast enteroclysis with air showing subtle

mucosal granularity in a segment of small bowel (open arrow)

indicating mucosal atrophy. In addition, an ulcer (curved

arrow) is noted, andmultiple aphthae (small arrow in one) are

present, suggesting early recurrance. Chronic disease is seen

in a more distal segment. (Courtesy of M. Maruyama, MD,

Tokyo, Japan).

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303288

Fig. 4. Active inflammatory subtype, minimal changes. CT findings. (A) Conventional CT with positive oral contrast and IV

enhancement done 1 week before enteroclysis (see Fig. 2A) shows subtle mild but nonspecific fold thickening of the terminal

ileum (open arrow). C, cecum. (From Maglinte D, Hallett R, Rex D, et al. Imaging of small bowel Crohn’s disease: can

abdominal CT replace barium radiography? Emerg Rad 2001;8:129; with permission.) (B) Conventional CT of another patient

with positive oral and IV contrast enhancement shows mild diffuse mural thickening of distal small bowel (arrow). Contrast

attenuation of the thickened bowel wall is less than that of adjacent muscle, making these findings consistent with edema. CTwas

done 2 days prior to enteroclysis (see Fig. 2B). C, cecum. Axial (C) and coronal (D) images of CT enteroclysis using neutral

enteral with IV contrast enhancement in another patient show mucosal hyperemia at distal ileum (arrows) indicating mild active

inflammatory disease. Minimal bowel wall thickening is present. Dilatation of proximal small bowel segments with normally

enhancing mucosa (curved arrow in C) is a reflection of low-grade obstruction during enteral contrast infusion secondary to

spasm from active inflammatory disease in more distal segments. (Courtesy of G. A. Rollandi, MD, Genova, Italy.)

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 289

dimensional (3D) fast long angle shot (FLASH)

images [30].

Fistulizing/perforating disease subtype

This Crohn’s subtype is characterized by active

inflammation with a tendency toward or eventual

progression to transmural extension of the inflamma-

tory process with resultant fistula formation or

perforation. Deep ulcers precede sinus and fistulae

formation to adjacent organs. The features of this

subtype of Crohn’s disease include demonstration of

deep fissuring ulcers and sinus tracts, fistulae to

adjacent bowel loops or other organs, the demon-

stration of an associated abscess, and extraintesti-

nal involvement on barium examination and CT

(Fig. 13).

MR enteroclysis also may be used to depict and

define extraintestinal complications of Crohn’s dis-

ease; deep ulcers, sinus tracts, and fistulas can be

accurately disclosed on true FISP MR enteroclysis

images (Figs. 14, 15). The characteristic deep linear

ulcers typically seen in Crohn’s disease can be

identified on MR enteroclysis as transversely or

longitudinally oriented thin, high-intensity lines

within the bowel wall on true FISP images. True

FISP sequence is superior to HASTE in demonstrat-

ing discrete ulcers and intramural tracts, whereas 3D

FLASH sequence has lower performance in this

regard [30].

Fibrostenotic disease subtype

Small bowel obstruction is the predominant

clinical manifestation of this disease subtype. When

severe, this subtype can be seen on abdominal plain

radiographs. Barium examination shows fixed seg-

ments of stenosis without thickening of the folds.

There is marked prestenotic dilatation (Fig. 16). CT

imaging demonstrates a fixed narrowing of the

involved bowel with associated wall thickening.

This is seen during IV contrast-enhanced examina-

tions as a homogeneous soft tissue attenuation of

the thickened wall with no evidence of edema

(Fig. 17). The degree of stenosis is variable, ranging

from mild to severe. This subtype should be differ-

entiated from small bowel obstruction secondary to

spasm associated with active inflammatory disease

(see Fig. 8A).

Fig. 5. Active inflammatory subtype, severe changes. Findings on barium examination. (A) Enteroclysis of 30-year-old patient

with worsening diarrhea and abdominal pain shows deep marginal protrusions (arrows) along mesenteric margin of distal ileum

consistent with deep ulcers. A cobblestone mucosa also is seen. Separation between bowel loops suggests wall thickening

exaggerated by the compression paddle. C, cecum. (B) Cobblestone mucosa manifested by crisscrossing linear ulcers separated

by mounds of edema suggestive of severe inflammation of a long segment of distal ileum (arrow) in another patient.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303290

On MR enteroclysis, the rich tissue contrast

intrinsic to the nuclear MR phenomenon helps

to facilitate the differentiation between fibrotic

(Fig. 18) and edematous bowel wall thickening.

Collagen, the main component of the fibrotic wall

thickening, has long T1 and short T2 relaxation

times, thus exhibiting low signal intensity on both

T1 and T2 relaxation times while rendering high

signal intensity on T2-weighted images and low

signal intensity on T1-weighted images. Differenti-

ation between fibrotic and edematous stenosis

based on MR imaging properties is useful for

selecting patients for medical (edematous) versus

surgical (fibrotic) treatment.

Reparative or regenerative disease subtype

This subtype reflects inactive Crohn’s disease and

may be associated with other phases of Crohn’s

disease located in different locations in the same

small bowel. Mucosal atrophy and regenerative

polyps characterize this phase (Fig. 19). There may

be a decrease in lumen diameter, but there is no

evidence of active inflammation.

Selection of imaging modality and clinical

relevance of radiologic findings in small bowel

Crohn’s disease

Barium examination and CT are currently the

most commonly used radiologic methods of exam-

ination in the assessment of small bowel Crohn’s

disease. In many patients, both procedures are used

to determine the severity of disease activity and the

extent of the disease process [40]. The choice of

initial examination depends on the clinical issue in

question. The differences between conventional CT

and barium enteroclysis in demonstrating diagnostic

features and complications of small bowel Crohn’s

disease in 33 patients who had both procedures done

for the same indications recently were reported

(Table 2) [40]. Statistically significant differences

favoring enteroclysis were shown in the ability to

diagnose ulceration, obstruction, and strictures in the

small bowel. Unique and complementary diagnostic

information was provided by both methods of

examination. MR enteroclysis is an emerging tech-

nique for small bowel imaging that combines the

advantages of barium enteroclysis with those of

cross-sectional imaging [41,42]. MR imaging is

the emerging modality of choice for imaging of

small bowel Crohn’s disease, because of its superb

soft tissue contrast, the static and dynamic three-

dimensional imaging capabilities, and the absence

of ionizing radiation exposure. The availability of

ultrafast sequences is a new added advantage.

Realistically, however, cost and availability of this

technology may be significant limitations to its

widespread use.

Historically, barium studies have correlated

poorly with the clinical stage of the disease and

with the response of patients to treatment [43]. This

discrepancy is due, in part, to suboptimal barium

examination methods being employed. Significant

advances in the radiologic investigation of small

bowel Crohn’s disease have been made since these

original comparisons, primarily due to refinements

in enteroclysis, multidetector helical CT, and MR

imaging. In the National Cooperative Crohn’s Dis-

ease Study [43], the radiographic demonstration of a

stricture that caused obstruction or of a fistula was

associated with poor clinical response to medical

treatment. In a comparative study of small bowel

Fig. 6. CT enteroclysis with positive enteral contrast of a

17-year-old male with worsening diarrhea and weight loss

shows cobblestone mucosa of a long segment of distal small

bowel. Mounds of edema are manifest by ovoid or nodular

defects and ulcerations manifest as irregular marginal

protrusions (arrow in one) in the bowel wall. The involved

segment also shows a thickened wall.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 291

Fig. 7. Active inflammatory subtype, severe changes. CT manifestations. (A) Contrast-enhanced CT with IV contrast

enhancement. There is edema of the bowel wall with deep ulcers shown by linear contrast protrusion through the thickened wall

(arrow in one). Note prominent mesenteric blood vessels indicating hyperemia. Axial (B) and sagittal (C) images of lower

abdomen of another patient obtained using multidetector row CT with water as the enteral contrast with IV contrast shows

mucosal hyperemia (arrows) of a moderately long segment of ileum with moderate thickening of the bowel wall. Although ulcers

are not shown, they can be inferred by the irregular or disrupted segments of hyperemic mucosa with increased attenuation

relative to the edematous bowel wall (open arrows). (Courtesy of K. Horton, MD, Baltimore, MD.) (D) CT enteroclysis of

another patient using neutral enteral and IV contrast enhancement shows mucosal hyperemia of long segments (arrows) of small

bowel with irregular mucosa and thickening of bowel wall from edema. Mesenteric hyperemia is present. (Courtesy of G. A.

Rollandi, MD, Genova, Italy.)

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303292

Fig. 8. Active inflammatory disease subtype manifested by the ‘‘target sign’’ and ‘‘mural stratification’’ on IV contrast-enhanced

CT with water as the enteral contrast agent. (A) Seen on end, the target sign is indicated by the small inner ring of mucosal

enhancement surrounding the fluid in the lumen (small arrow), separated by an intermediate low-density ring from the outer ring

of muscular and serosal enhancement (curved arrow). Note distention of more proximal small bowel loops, which is a reflection

of spasm from active disease. (B) When seen tangentially, active inflammatory disease is manifested by mural stratification. The

inner line of mucosal enhancement (small arrow) is separated by the intermediate low-density (edema) thickening from the

enhancement (curved arrow), indicating muscular and serosal hyperemia. Note accompanying ascites. U, uterus. (From

Maglinte D, Hallett R, Rex D, et al. Imaging of small bowel Crohn’s disease: can abdominal CT replace barium radiography?

Emerg Rad 2001;8:129; with permission.) (C) Mucosal hyperemia (arrow) can be discerned from the positive intraluminal

contrast as a faint thin density and the outer layer of bowel wall edema of another patient. Note enlarged mesenteric nodes.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 293

follow-through versus enteroclysis [44], obstruction,

fistula, and other diagnostic aspects of Crohn’s

disease were better shown by enteroclysis. A more

detailed demonstration of the fold abnormalities seen

in inflammatory bowel disease is shown with the

infusion method [4,9,44,45]. Nevertheless, oral

methods of examination that visualize the entire

small bowel, when combined with intermittent fluo-

roscopy and adequate compression, may approach

the accuracy of enteroclysis [3,7]. The gas-enhanced

follow-through examination [46] and the peroral

pneumocolon method [47] have been recommended

for use with peroral methods to improve evaluation

of the distal small bowel in the region of the

ileocecal valve or ileocolic anastomosis.

Although CT is unable to identify early mucosal

changes of the disease, it is far superior for showing

mural abnormalities and extraintestinal manifesta-

tions including bowel wall thickening, and mes-

enteric inflammatory changes including adenopathy.

CT can determine whether a mesenteric mass repre-

sents phlegmon, abscess, or adenopathy [10,16,18],

which influences management decisions consid-

erably. Once identified, CT-guided catheter drainage

of an intra-abdominal abscess can be instituted. CT

also has been useful for the diagnosis of entero-

vesical fistula [48]. The widespread availability of

CT makes it an ideal initial method of examination.

The use of IV contrast-enhanced multidetector row

CT with water or methylcellulose as enteral contrast

agent, using reformatting in different planes or

volume rendering might be able to answer most

clinical queries relevant to patients management.

Barium enteroclysis, CT enteroclysis, or MR entero-

clysis could then be used if further assessment

is needed.

It remains to be seen whether CT enteroclysis, a

method that combines the advantages of the cross-

sectional display of CT and the volume challenge of

the small bowel induced by enteroclysis infusion, is

an ideal method of examination for showing the

complications of Crohn’s disease [21–25]. The

advantages of helical CT in demonstrating a greater

degree of mural enhancement following IV contrast

administration when compared with conventional CT

and the use of multiplanar reformatting may improve

its ability to delineate the extent of small bowel

disease [20]. The advantages of CT enteroclysis also

apply to MR enteroclysis; the latter technique has

the added advantages of increased soft tissue con-

trast and direct multiplanar capabilities [26–30,

Fig. 9. Submucosal fat deposition in chronic Crohn’s

disease. Arrow points to deposit of fat in submucosa

surrounding positive intraluminal contrast. Other manifes-

tations of Crohn’s disease are also present. Note mesenteric

stranding (open arrow).

Fig 10. ‘‘Comb sign’’ on IV contrast-enhanced CT. Prom-

inent vasa recta (arrow) are seen, indicating perienteric hy-

peremia. Edema of the bowel wall is also present. The ‘‘comb

sign’’ indicates severe active inflammatory disease subtype.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303294

Fig. 11. MR imaging of active inflammatory disease subtype. (A) 29-year-old male with abdominal pain and diarrhea. MR

enteroclysis postgadolinium 3D FLASH image (TR/TE/a = 4.8 ms/1.6 ms/45, 40 partitions, 2.5-mm thickness, 256 � 512 image

matrix, 22-second breath-hold duration). Stratified pattern of enhancement in active Crohn’s disease generates the target sign

(arrow) by the moderate signal intensity of the serosa, low signal intensity of the edematous submucosa, and high signal intensity

of the hyperemic mucosa. (B) True FISP (TR/TE/a = 6.5 ms/3 ms/70, 4-mm section thickness, 256 � 256 image matrix,

19-second breath-hold duration) coronal image demonstrates with high signal intensity (arrow) edematous wall thickening in

another patient with Crohn’s disease. (C) 3D FLASH with fat saturation (TR/TE/a= 4.8 ms/1.6 ms/45, 40 partitions, 2.5-mm

thickness, 256 � 512 image matrix, 22-second breath-hold duration) coronal image acquired after glucagon and IV gadolinium

administration of same patient (in B). Submucosal edema presents with low signal intensity against the high signal intensity

serosa and mucosal layers, generating an MR ‘‘mural stratification’’ (arrow).

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 295

38,39,41,42]. High contrast resolution ultrafast

sequences such as single-shot turbo spin echo, true

FISP, HASTE, and contrast-enhanced 3D FLASH

applied to a well-distended small bowel make MR

enteroclysis a powerful tool in demonstrating the

wide spectrum of disease abnormalities and compli-

cations of small bowel Crohn’s disease, while simul-

taneously providing information regarding disease

activity [30]. MR enteroclysis correlates with barium

enteroclysis in disclosing superficial and transmural

abnormalities of the disease, and musters all the

advantages of cross-sectional imaging in disclosing

extraintestinal manifestations and complications of

the disease. Changes in small bowel kinetics may

also be evaluated on MR fluoroscopy. In addition,

initial experience shows that MR imaging can pro-

vide an adequate pictorial assessment of local

inflammatory disease activity, thus directly influ-

encing patient management. It has been suggested

that MR imaging could be the evolving ‘‘all-in-one’’

examination technique that can answer all major

clinical questions that arise in the course of Crohn’s

disease [49]. The precise role of this technique

awaits further experience and research.

As noted above, imaging features, considered in

the context of clinical and endoscopic information,

helps to establish the subtype of Crohn’s affecting

individual patients. Patients with active inflamma-

tory disease respond best to medical therapy, and

may respond to a range of medical therapies.

Patients with fistulizing/perforating disease tend to

be most responsive to infliximab (Centocor, Inc.,

Malvern, PA) or azathioprine (Faro Pharmaceuticals,

Inc., Bedminster, NJ). Cyclosporine (Novartis

Pharm-Corp, East Hanover, NJ) may be effective

in fistulizing disease subtypes refractory to other

agents. Surgery is indicated in fistulizing disease

that is not responsive to medical treatment. Symp-

tomatic fibrostenosing disease may require manage-

ment by surgical resection, stricturoplasty, or

endoscopic balloon dilation in cases in which stric-

tures are short and endoscopically accessible.

Clearly there is overlap between different subtypes,

and individual patients may manifest features of

multiple subtypes at the same or different points

in time.

Summary

This article has reviewed the imaging features

that correspond to and support the classification of

patients into clinical subtypes of Crohn’s disease.

One study [50] showed that radiologic features on

barium studies closely correlated with the Crohn’s

Disease Activity Index, and another study [10]

indicated that CT findings changed patient manage-

ment in up to 29% of cases. Knowledge of the

location, severity, and presence of complications

assist in providing patients with appropriate treat-

ment options.

Reports of radiologic studies in Crohn’s disease

should include the presence or absence of imaging

features that support these different subtypes. An

additional advantage of the use of a reproducible

imaging classification that emphasizes morphologic

features would be improved comparison of the

results of different investigators and treatment pro-

tocols. Whatever method of radiologic investigation

is employed, it should be targeted to answer ques-

tions relevant to patient management. The imaging

modalities used should be able to classify the small

bowel Crohn’s subtypes and should be reflected in

the radiologists’ reports.

Fig 12. Increased mesenteric vascularity (comb sign) and

lymphadenopathy in a 26-year-old male patient with active

Crohn’s disease (Crohn’s disease activity index = 233).

Luminal narrowing and thickening of the bowel wall of

distal ileal loops. Dilated vasa recta at the mesenteric border

of the affected segment are clearly shown on true FISP

images (TR/TE/a = 6.5 ms/3 ms/70, 4-mm section thickness,

256 � 256 image matrix, 19-second breath-hold duration).

Multiple mesenteric lymph nodes measuring less than 1 cm

in diameter (arrows).

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303296

Fig. 13. Imaging findings of fistulizing/perforating subtype Crohn’s disease. (A) Barium enteroclysis of a 40-year-old patient

with known Crohn’s disease showing multiple ileoilial and ileosigmoid fistulae. The distal ileum forms the central pocket

(curved arrow) where the cecum and adjacent small bowel loops are ‘‘sucked’’ in and from which multiple fistulae originate.

R, rectum. (B) Enteroclysis examination of another patient shows multiple deep ulcers (small arrow in one) in long edematous

neodistal ileum with a long sinus tract communicating with a large cavity (arrow). (From Kelvin F, Herlinger H. Crohn’s

disease. In: Herlinger H, Maglinte D, Birnbaum B, editors. Clinical imaging of the small intestine. 2nd edition. New York:

Springer; 1999. p. 281; with permission.) (C) CT of same patient (in B) shows a large gas-containing abscess adjacent to the

diseased ileum. Deep ulcer (arrow) is seen in diseased neodistal ileum. (From Kelvin F, Herlinger H. Crohn’s disease. In:

Herlinger H, Maglinte D, Birnbaum B, editors. Clinical imaging of the small intestine. 2nd edition. New York: Springer; 1999.

p. 281; with permission.) (D) Anterior abdominal wall abscess (arrow) in another patient with adjacent anterior intraperitoneal

(curved arrow) abscess infiltrating the parietal peritoneum. Narrowed markedly edematous ileum (open arrow) is seen in right

lower abdomen.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 297

Fig. 14. 46-year-old male with Crohn’s disease diagnosed

10 years ago. Wall thickening associated with discrete

ulcers (arrows) is shown on a coronal spot view with a

true FISP sequence (TR/TE/a = 6.5 ms/3 ms/70, 4-mm

section thickness, 256 � 256 image matrix, 19-second

breath-hold duration). (From Gourtsoyiannis N, Papaniko-

laou N, Grammatikakis J, Maris T, Prassopoulos P. MR

enteroclysis protocol optimization: comparison between 3D

FLASH with fat saturation after intravenous gadolinium

injection and true FISP sequences. Eur Radiol 2001;11(6):

911; with permission.)

Fig 15. Fistulizing Crohn’s disease. Multiple enteroenteric

fistulas are seen on axial true FISP (TR/TE/a = 6.5 ms/3 ms/

70, 4-mm section thickness, 256 � 256 image matrix,

19-second breath-hold duration) image (arrows). (From

Gourtsoyiannis N, Papanikolaou N, Grammatikakis J, Maris

T, Prassopoulos P. MR enteroclysis protocol optimization:

comparison between 3D FLASH with fat saturation after

intravenous gadolinium injection and true FISP sequences.

Eur Radiol 2001;11(6):911; with permission.)

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303298

Fig. 16. Fibrostenosing Crohn’s disease subtype. (A) Enteroclysis of a patient with known Crohn’s disease who presented

with worsening abdominal pain. These are fixed segments of narrowing (curved arrows) with marked prestenotic dilatation.

The narrowed segments are not edematous. Filiform polyps are identified (small arrow in one). Note ileosigmoid fistula

(open arrow). (From Maglinte DDT, Chernish SM, Kelvin FM, et al. Crohn disease of the small intestine: accuracy and

relevance of enteroclysis. Radiology 1992;184:541–5; with permission.) (B) CT shows a segment of small bowel narrowing

with soft tissue attenuation (fibrosis) of thickened bowel wall (arrow). There is marked prestenotic dilatation.

Fig. 17. Multidetector row helical CT with water as enteral contrast with IV contrast enhancement in stenosing disease subtype.

(A) Axial image at level of midabdomen shows markedly dilated loops of small bowel with fluid and gas. Note normal mucosal

enhancement and thickness of uninvolved dilated loops (arrow). (B) Axial image at level of upper pelvis shows point of

obstruction (arrow). The attenuation of the stenosed segment is similar to that of soft tissue, consistent with fibrosis. There is no

evidence of mucosal hyperemia or mural stratification. (Courtesy of K. Horton, MD, Baltimore, MD.)

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 299

Fig. 18. 28-year-old female with longstanding Crohn’s disease presented with ileus. (A) True FISP (TR/TE/a = 6.5 ms/3 ms/70,

4-mm section thickness, 256 � 256 image matrix, 19-second breath-hold duration) coronal section. A short fibrostenotic ideal

segment with significant prestenotic dilation (B) 3D FLASH with fat saturation (TR/TE/a = 4.8 ms/1.6 ms/45, 40 partitions,

2.5-mm thickness, 256 � 512 image matrix, 22-second breath-hold duration). Coronal image shows homogeneous contrast

enhancement in the region of the fibrotic stricture (open arrow).

Fig. 19. CT enteroclysis showing filiform polyps (arrows) in a long segment of small bowel indicating reparative subtype of

Crohn’s disease. There is no evidence of fold thickening or ulcers (see also Fig. 16A).

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303300

Table 2

Diagnostic differences between CT and enteroclysis in demonstrating features of small bowel Crohn’s disease

CT Enteroclysis

No. patients % No. patients %

Ulcerations 7 19 29 78

Mural edema 15 41 17 46

Obstruction 6 16 17 46

Stricture 4 11 14 38

Sinus tract 2 5 10 27

Fistula 3 8 9 24

Abscess 10 27 7 19

Extraintestinal disease 3 0 0 0

Total sites 47 54

Data from Maglinte D, Hallett R, Rex D, et al. Imaging of small bowel Crohn’s disease: can abdominal CT replace

barium radiography? Emerg Rad 2001;8:127–33.

D.D.T. Maglinte et al / Radiol Clin N Am 41 (2003) 285–303 301

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