DOI:10.2214/AJR.06.0712
AJR 2007; 188:1344-1355
© American Roentgen Ray Society
A Pattern Approach to the Abnormal Small Bowel: Observations at MDCT and CT Enterography
Michael Macari1,
Alec J. Megibow and
Emil J. Balthazar
1 All authors: Department of Radiology, Division of Abdominal Imaging, NYU
Medical Center, 560 First Ave., Ste. HW 207, New York, NY 10016.
Received May 27, 2006;
accepted after revision October 11, 2006.
Address correspondence to M. Macari
(michael.macari{at}med.nyu.edu).
M. Macari and A. J. Megibow are consultants to E-Z-EM.
Abstract
OBJECTIVE. Imaging of the vast array of pathologic processes
occurring in the small bowel has been facilitated by recent advances,
including the use of MDCT scanners that acquire isotropic data and neutral
oral contrast agents that improve small-bowel distention.
CONCLUSION. This review shows how a systematic pattern approach can
be used to narrow the differential diagnosis when an abnormal small-bowel loop
is detected on MDCT.
Keywords: CT • CT technique • inflammatory bowel disease • small bowel
Introduction
Imaging of pathologic processes occurring in the small bowel has
traditionally been performed with barium small-bowel follow-through
examinations, single- or double-contrast intubated enteroclysis, and CT
[1]. Recent innovations,
including capsule endoscopy and MRI, have emerged as alternative small-bowel
imaging techniques that can be performed without ionizing radiation
[2,
3].
Technical advances have improved the imaging evaluation of the small bowel
using CT [4,
5]. These advances include the
use of MDCT scanners that acquire isotropic data, oral contrast agents, and
administration techniques that improve small-bowel distention. These advances,
coupled with imaging workstations that allow multiplanar and 3D evaluation of
these isotropic data sets, have allowed improved depiction and
characterization of small-bowel pathology. The use of MDCT, neutral
(attenuation values between 10-30 H) oral contrast agents to distend the small
bowel, and multiplanar thin-section data evaluation has come to be known as CT
enterography (Fig. 1).
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Fig. 1 —30-year-old woman with normal CT findings at enterography. Coronal
reformatted image of small bowel using neutral oral and IV contrast agents
shows normal small bowel (arrows). Note wall of small bowel is thin,
measuring 1-2 mm, and shows uniform mural enhancement. Moreover, normal fold
pattern of jejunum (many folds) is distinguished from that of ileum (few
folds).
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Current indications for performing CT enterography include the evaluation
of obscure gastrointestinal bleeding, the presence and activity of Crohn's
disease, and suspected small-bowel neoplasia. Moreover, a vast array of
pathologic processes occurring in the small bowel will be detected
incidentally at MDCT in patients with abdominal pain. The differential
diagnosis for these processes is broad and can be confusing. The purpose of
this article is to show how a systematic pattern approach can be used to
narrow the differential diagnosis when an abnormal process is identified in
the small bowel at MDCT and CT enterography.
Technique
Confident detection and optimal evaluation of an abnormal segment or loop
of small bowel is achieved when the small bowel is well distended, IV contrast
has been administered, and thin-section (
1-mm) CT is used. Traditionally,
positive contrast materials such as dilute barium or water-soluble iodinated
solutions have been used to mark and sometimes distend the small bowel at CT
[1,
5]. These contrast agents work
well in delineating the small bowel, the degree of distention being
proportionate to the amount of contrast material consumed, the rate at which
it is consumed, and the time delay of the examination itself. When the small
bowel is distended with positive contrast material, wall thickness ranges from
imperceptible to no greater than 2 mm
[1]
(Fig. 2). However, unless care
is taken in administering these agents, any portion of the bowel may be either
underdistended or even unfilled with contrast material, leading to a possible
false-positive diagnosis. In general, adequate luminal distention is present
if the diameter of the small bowel is 
2 cm.
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Fig. 2 —60-year-old man with excellent small-bowel distention on CT using
positive oral contrast material. Coronal reformatted image of small bowel
shows normal small bowel. Note wall of small bowel (arrows) is barely
perceptible.
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When the small bowel is distended with positive contrast material, the wall
is thin and may be imperceptible but should not measure more that 1-2 mm
[1]. Dilute barium and
iodinated positive oral contrast agents are particularly well suited in
evaluating thin patients without a lot of intraperitoneal adipose tissues and
in oncology patients, in whom implants and lymph nodes will stand out from the
small bowel. A potential limitation of positive oral contrast agents in the
evaluation of the small bowel is that mucosal enhancement may be obscured by
the luminal contrast material, and thus the pattern of enhancement, which
serves as a primary aid in the differential diagnosis of an abnormal
small-bowel segment, may be impaired (Fig.
3A,
3B).
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Fig. 3A —47-year-old man with ileal Crohn's disease. Axial CT image with
positive intraluminal oral contrast material shows loop of thickened ileum
(arrow). However, pattern of enhancement is obscured by contrast
material.
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Fig. 3B —47-year-old man with ileal Crohn's disease. Axial CT image with
neutral intraluminal oral contrast material shows same loop of ileum is
thickened (arrow), but now pattern of enhancement is readily seen
with mucosal hyperenhancement indicative of active Crohn's disease.
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Neutral oral contrast agents allow full visualization of the normal
intestinal wall, thereby allowing analysis of the degree and pattern of
small-bowel enhancement
[5-12].
"Neutral contrast" refers to agents that have an attenuation value
similar to that of water (10-30 H). For neutral contrast agents to be
effective, they must be used with IV contrast material and the small-bowel
distention must be optimal.
Several neutral contrast agents have been evaluated for small-bowel
distention, including water, water in combination with a bulking agent such as
methylcellulose or locust bean gum, polyethylene glycol solutions, and a
commercially available low-density barium solution (VoLumen
[low-Hounsfield-value barium sulfate], E-Z-EM)
[5,
6]. A limitation of using water
is that it is rapidly absorbed across the small-intestinal mucosa, resulting
in suboptimal small-bowel distention. VoLumen and polyethylene glycol
solutions are less rapidly absorbed; studies have shown that they are superior
to both water and methylcellulose in achieving small-bowel distention
[5-7,
12]. The initial studies
evaluating the potential use of CT enterography were performed with positive
oral contrast agents [8].
However, since that time, CT enterography in most reports has been performed
with a neutral oral contrast agent
[5-7,
9-12].
Peroral CT enterography differs from CT enteroclysis in that the latter
technique is performed after placement of a nasojejunal tube in conjunction
with active small-bowel distention. CT enterography performed with VoLumen is
inferior to CT enteroclysis in achieving small-bowel distention
[9]. However, the noninvasive
nature and speed of CT enterography make it well suited as a first-line
technique for the evaluation of suspected small-bowel disease
[4,
5,
12].
Our specific protocol for performing CT enterography requires that the
patient fast for at least 3 hours before the examination. This will decrease
the possibility of misinterpreting a foreign body as a polyp or tumor. On
arrival at the imaging center, patients ingest two 450-mL bottles of VoLumen
over a 30-minute period. The first bottle is ingested 30 minutes before the
procedure, the second 20 minutes before the procedure. Immediately before
changing for the examination, the patient consumes 225 mL of water, and
finally, on entering the scanning room, the patient drinks a final 225 mL of
water. The total volume of fluid is therefore 1,350 mL. Water is adequate for
the final contrast agent because it is designed primarily to distend the
stomach and duodenum. Other imaging centers deliver a similar volume of
contrast material over a 1-hour period (450 mL 60 minutes and 40 minutes
before scanning and 225 mL 20 and 10 minutes before scanning)
[12].
The optimal timing of the administration of oral contrast material will
continue to be investigated. It is likely easier for the patient to ingest the
oral volume over a longer period of time. However, if ingested over too long a
period, the contrast material may be in the colon. Whether the contrast
material is administered over 30 or 60 minutes, if insufficient volume is
ingested, suboptimal small-bowel distention will limit the CT enterography
examination. Therefore, the importance of the oral contrast agent must be
explained to the patient. This is facilitated by having the CT technologist or
nurse instruct and monitor patients as they are ingesting the oral contrast
material. If patients are left on their own, suboptimal distention may
result.
IV contrast enhancement is essential when performing CT enterography. A
20-gauge catheter is inserted into an arm vein, and 1.5 mL/kg of iodinated
contrast material (Ultravist, 300 mg I/mL, [iopromide], Berlex Laboratories)
is injected at a rate of at least 4 mL/s. Without IV contrast material, the
bowel wall is not seen and intestinal marking is compromised. If there is a
possibility of compromised venous access or the patient cannot receive IV
contrast material, we perform the study with a positive contrast agent.
The optimal timing of data acquisition for CT enterography is somewhat
controversial. We begin the acquisition 60 seconds after the initiation of the
bolus. Others have suggested that an enterography phase (
45 seconds after
the injection), or even a dual-phase acquisition, may be helpful in patients
with obscure gastrointestinal bleeding
[10-12].
Glucagon in a dose of 0.1 mg is administered IV and given a few minutes before
data acquisition to diminish peristalsis.
MDCT enterography should be performed on a 16-MDCT or higher scanner. These
scanners can acquire the submillimeter isotropic data necessary for 3D
displays in a short enough time to minimize motion arti-facts. At our
institution, we use either a 16 x 0.75 mm or 64 x 0.6 mm detector
configuration, depending on whether a 16- or 64-MDCT scanner is used,
reconstructing either 1- or 0.8-mm slices. From this data set, the
technologist will generate a set of axial 4-mm sections and a set of
3-mm-thick coronal multiplanar reformatted images at 3-mm intervals
encompassing the entire bowel. These are sent to the PACS for review.
In addition, the thin slices are sent to a workstation, where they are
available for the radiologist to view the data in 3D volume-rendering or
maximum-intensity-projection displays
[12,
13]. Images are acquired at
120 kVp, 0.4-second gantry rotation, and 180 effective mAs. A dose modulator,
available on all MDCT scanners, which automatically decreases the radiation
exposure to thinner areas of the patient, is used and can reduce the dose up
to 30%.
A Pattern Approach to the Abnormal Small Bowel at MDCT
An abnormal small-bowel loop is present when the wall thickness is 3
mm despite adequate luminal distention
[1]. When an abnormal
small-bowel loop is recognized, a pattern approach can be used to narrow the
differential diagnosis [1].
Seven criteria can be used to aid in the evaluation of the abnormal small
bowel on contrast-enhanced MDCT, including the pattern of enhancement, the
length of involvement, the degree of thickening, whether the thickening is
symmetric or asymmetric, location of the lesion along the course of the small
bowel (proximal or distal), location of the lesion in the wall of the small
bowel (mucosal, submucosal, or serosal), and, finally, associated
abnormalities in the mesentery and vessels.
Mural Enhancement Pattern
The first criterion that should be assessed when evaluating an abnormal
loop of small bowel is the mural enhancement pattern. Four patterns may be
present during contrast-enhanced CT. These include a double-halo or target
appearance, referred to as mural stratification; homogeneous or
hyperenhancement; heterogeneous enhancement; and decreased or absent
enhancement.
Target Appearance
If the abnormal segment of small bowel displays a target appearance, a
benign process is present in the wall
[14]. The target sign results
from mucosal and serosal enhancement surrounding a prominent low-attenuation
submucosa (Fig. 4).
Visualization of a target appearance is facilitated by having neutral contrast
material in the small-bowel lumen (Fig.
3A,
3B). The neutral contrast agent
allows better depiction of the inner aspect of the wall of the small bowel.
The target sign was first described as a specific sign for Crohn's disease
[15], but it is now recognized
that any nonneoplastic condition may lead to a target appearance in the small
bowel. Common causes include Crohn's disease, infection, ischemia, radiation
enteritis, angioedema, and hemorrhage
[1,
14,
16-20]
(Figs. 4,
5A,
5B and
6A,
6B,
6C).
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Fig. 4 —35-year-old woman with target appearance in small bowel due to lupus
vasculitis. Axial CT image in this patient with systemic lupus erythematosus
shows marked mural thickening (> 1 cm) (long arrow) and target
appearance after contrast administration. Note edematous changes in right
kidney due to lupus nephritis (short arrow).
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Fig. 5A —45-year-old woman with target appearance in small bowel due to acute
radiation enteritis. Axial CT image in patient, who has cervical cancer and
just finished 4-week course of radiation therapy. Note moderate mural
thickening (5-10 mm) (arrow) and target appearance after contrast
administration.
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Fig. 5B —45-year-old woman with target appearance in small bowel due to acute
radiation enteritis. Coronal reformatted image shows segmental involvement of
abnormal loop in pelvis (long arrow) and normal-appearing loop in
abdomen (short arrow). Inflammatory process was localized to loops of
small bowel in pelvis within radiation field; findings were attributed to
acute radiation enteritis.
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Fig. 6A —80-year-old man with target appearance in small bowel due to
superior mesenteric artery (SMA) embolus. Axial CT image in patient who has
atrial fibrillation and abdominal pain shows mild to moderate mural thickening
( 5 mm) (long arrows) and target appearance diffusely throughout
small bowel and ascending colon (short arrow).
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Fig. 6B —80-year-old man with target appearance in small bowel due to
superior mesenteric artery (SMA) embolus. Axial CT image shows filling defect
(long arrow) in SMA and wedge-shaped perfusion defect (short
arrow) in left kidney. Findings are consistent with intestinal ischemia
due to embolus.
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Fig. 6C —80-year-old man with target appearance in small bowel due to
superior mesenteric artery (SMA) embolus. Intraoperative image shows diffuse
infarction of small bowel and cecum (arrows). Patient subsequently
died.
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A relatively rare condition that generally shows long segments or even
diffuse small-bowel involvement with a target appearance is angioedema
[16] (Fig.
7A,
7B,
7C). Angioedema may be
congenital or acquired and is due to increased capillary permeability in the
mucosa that results in submucosal edema. This condition may occur in the skin,
airways, or intestine and is usually self-limited and treated conservatively.
When it occurs in the small bowel, the condition causes acute abdominal pain.
When angioedema is acquired, there is often a recent history of the use of an
angiotensin-converting enzyme inhibitor, which appears to be an inciting event
[16]. The major differential
diagnosis of angioedema is ischemia and vasculitis
[16-20].
If the diagnosis of angioedema is considered at imaging, laboratory testing
can be helpful because the C1 esterase inhibitor level is low in this
condition. In patients with small-bowel thickening due to vasculitis, there is
a combination of edema and hemorrhage in the wall secondary to the
vasculitis-induced ischemia
[19,
20].
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Fig. 7A —31-year-old man with segmental thickening of terminal ileum due to
allergic angioedema. Axial CT image in patient with acute abdominal pain shows
multiple loops of moderately thickened (6 mm) small bowel (arrows).
Determining whether enhancement pattern shows target appearance is difficult
due to positive intraluminal contrast material. However, subtle increase is
seen in attenuation of serosal layer of small bowel.
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Fig. 7B —31-year-old man with segmental thickening of terminal ileum due to
allergic angioedema. Coronal reformatted image better shows segmental area (30
cm) of thickening of terminal and distal ileum (arrows). Pattern of
thickening suggests a submucosal process. In light of submucosal appearance,
differential diagnosis includes vasculitis, angioedema, and infection.
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Fig. 7C —31-year-old man with segmental thickening of terminal ileum due to
allergic angioedema. Small-bowel series in same patient performed 24 hours
later confirms submucosal disease with preservation of mucosa
(arrow). Stool cultures were negative for pathogens, as were
laboratory tests for vasculitis. Fecal material did show many Charcot-Leyden
crystals, suggesting allergic edema. Patient improved over several days.
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Submucosal hemorrhage has been classically thought to cause homogeneous
enhancement of the bowel wall after IV contrast administration
[17]. However, after
administration of a rapid bolus of IV contrast material, the small bowel
usually shows a target appearance in the setting of submucosal hemorrhage
[17]
(Fig. 8). The major
differential diagnosis of small-bowel submucosal hemorrhage is intestinal
ischemia. Both conditions tend to occur in elderly patients. Most patients
with submucosal hemorrhage will present with acute abdominal pain and will be
found to be at increased risk of bleeding, usually from anti-coagulation with
warfarin. Laboratory tests will show an elevated international normalized
ratio level, usually greater than 4
[17].
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Fig. 8 —76-year-old man with acute abdominal pain. Axial CT image shows
marked thickening (11 mm) of short segment (15 cm) of ileum (arrows)
and target appearance of wall. Patient was receiving warfarin with an
international normalized ratio of 7. Findings are consistent with acute
submucosal hemorrhage.
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Occasionally, adipose tissue will be deposited in the submucosa of the
small intestine, resulting in a target appearance. Recognition of the fat
attenuation in the submucosa will allow differentiation from edema. Submucosal
fat deposition in the wall of the small bowel has been associated with chronic
bowel inflammation [1,
21]. However, one study has
shown that this may be a normal variant and may not necessarily be associated
with chronic bowel inflammation
[22]. In a study of 100
patients undergoing unenhanced CT to evaluate for kidney stones, 21 patients
were shown to have submucosal adipose tissue in the bowel, and in 4% it was in
the terminal ileum. These patients had no history of chronic bowel
inflammation. Therefore, if this finding is seen at CT, correlation with the
clinical history is essential.
When a target sign is visualized on CT, the differential diagnosis can be
narrowed by observing the degree of thickening, the length of the abnormal
segment, associated imaging abnormalities, and the clinical history. Only a
few conditions generally cause marked thickening of the small bowel with a
target appearance. These include vasculitis, Crohn's disease, venous
thrombosis with associated bowel edema or ischemia, and intramural hemorrhage.
Associated findings that suggest Crohn's disease include fibrofatty
proliferation, hyperemia of the vasa recta (the comb sign), sinus and fistula
formation, and abscess. The small-bowel mesenteric arteries and veins should
always be evaluated when an abnormal small bowel is seen. The vasculature
should be assessed for both caliber (hypovolemia) and occlusion (embolus or
thrombus). Finally, the location of the abnormality should be determined.
Clustered loops in the pelvis or elsewhere suggest the possibility of
radiation enteritis.
Homogeneous Enhancement
When an abnormally thickened loop of small bowel enhances homogeneously
after contrast administration, it is important to assess whether the
enhancement is moderate or marked. Although quantitative measures of
determining the degree of enhancement have been developed, qualitative
assessment has been shown to be as good a predictor, or even a better
predictor, of hyperenhancement
[4]. When assessing the degree
of enhancement of a thickened segment, comparison of the segment with other
small-bowel loops is necessary. In addition, the timing and adequacy of the
bolus of IV contrast material that was administered need to be assessed.
If the enhancement is mild and the attenuation is similar to muscle, one
should consider chronic inflammatory conditions, such as chronic Crohn's
disease, ischemia, or radiation
[1,
14]. The milder homogeneous
enhancement in these cases is likely related to the development of fibrosis.
Lymphoma and occasionally intramural hemorrhage can cause marked thickening
and homogeneous enhancement of the small bowel
[17,
23] (Fig.
9A,
9B,
9C). Occasionally, Crohn's
disease will show homogeneous hyperenhancement of the wall
[4,
10]. Homogeneous
hyperenhancement in the setting of Crohn's disease implies active disease
[4]. As depicted on MDCT
enterography, attenuation of the enhanced wall exceeding 109 H in a loop of
bowel affected by Crohn's disease has a high degree of correlation with
disease activity [4].
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Fig. 9A —79-year-old man with segmental thickening of jejunum due to
lymphoma. Axial CT image in patient with abdominal pain shows moderate
thickening (9 mm) of loop of jejunum (arrow) and adjacent abscess
(arrowhead).
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Fig. 9B —79-year-old man with segmental thickening of jejunum due to
lymphoma. Coronal reformatted CT image better shows segmental (15-cm) area of
homogeneous thickening (long arrows). Note enlarged lymph node in
adjacent mesentery (short arrow). Differential diagnosis includes
Crohn's disease and lymphoma.
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Again, visual assessment is usually sufficient to determine if a segment is
hyperenhanced. If the small bowel is not well distended, the wall may appear
falsely thick and show homogeneous enhancement. This typically occurs in the
jejunum. In these cases, it is important to evaluate the perienteric mesentery
for the presence or absence of inflammatory changes and vessels that should be
normal as opposed to hyperemic. Visualization of small bubbles of gas trapped
between the valvulae conniventes will help to confirm that the small-bowel
wall is not thickened. Finally, if there is still concern, a small-bowel
series can be obtained.
Heterogeneous Enhancement
Heterogeneous enhancement is typical of small-bowel neoplasms. Although any
small-bowel tumor may appear this way, heterogeneous enhancement is most
frequent with adenocarcinoma and malignant gastrointestinal stromal tumors
(GISTs). The enhancement pattern of a GIST is related to its size; small
tumors tend to be well circumscribed and to enhance homogeneously, and large
tumors tend to have more irregular morphology, ulcerate, and enhance
heterogeneously after contrast administration
[24,
25]. Metastasis and
endometriotic implants to the serosal surface of the bowel may show
heterogeneous or homogeneous enhancement. Rarely, lymphoma will appear
heterogeneous in its enhancement pattern.
Diminished Enhancement
The normal small bowel enhances after administration of IV contrast
material (Fig. 1). Decreased or
diminished enhancement may be difficult to appreciate when the bowel is filled
with a positive contrast agent; however, when the bowel is filled with a
neutral contrast agent and displayed in 3D, regional differences in mural
enhancement become apparent. In the correct clinical situation, decreased
enhancement is pathognomonic for intestinal ischemia
[17,
18,
26]. When evaluating the small
bowel for intestinal ischemia, it is important to compare the loops that show
apparent decreased enhancement with the more normally enhancing loops (Fig.
10A,
10B).
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Fig. 10A —76-year-old man with diminished enhancement of multiple loops of
small bowel. Coronal reformatted CT image in patient with closed-loop
small-bowel obstruction due to transmesenteric hernia shows cluster of
small-bowel loops with diminished enhancement (short arrows) when
compared with loops that are not in closed loop (long arrows).
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The several causes of small-bowel ischemia include strangulation due to a
closed-loop obstruction, low-flow states from cardiac arrhythmias, sepsis or
shock, embolus or thrombosis of the superior mesenteric artery (SMA), and
superior mesenteric vein (SMV) thrombosis. In the setting of intestinal
ischemia, the small bowel will initially show mild thickening and often a
target appearance due to edema and intramural bleeding
[1,
17] (Fig.
6A,
6B,
6C). As the process progresses
to infarction, the bowel becomes thin and shows diminished enhancement;
finally, when mucosal integrity is breached, pneumatosis and perforation may
occur [17,
18].
When small-bowel ischemia is suspected, the vessel caliber, presence of
atherosclerotic plaque, thrombus, and embolus in the mesenteric vasculature
should be carefully evaluated. At our institution, we perform a dual-phase
acquisition for patients suspected of having mesenteric ischemia: an arterial
phase at about 30 seconds evaluating the patency of the mesenteric arterial
supply, followed by a mural phase at approximately 60-65 seconds that captures
the maximally enhanced intestinal wall. Neutral contrast-enhanced MDCT is
ideal for these patients. If the patient is too ill to drink, our ability to
detect subtle changes of mural ischemia may be limited.
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Fig. 11 —49-year-old man with target appearance in segmental distribution due
to acute Crohn's disease. Coronal reformatted CT image shows moderate mural
thickening (5-10 mm) with target appearance in ulcerated segment of terminal
ileum (long arrows). Additional findings supporting diagnosis of
Crohn's disease include fibrofatty proliferation and prominent vasa recta
(short arrow).
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Fig. 12A —77-year-old man with focal thickening of jejunum due to
diverticulitis. Coronal CT enterography image in patient with abdominal pain
shows focal (2 cm) area of jejunal thickening centered on small out-pouching
(arrow) with adjacent perienteric fat stranding. Note adjacent
mesenteric abscess (arrowheads). Differential diagnosis includes
foreign body perforation, perforated neoplasm, and diverticulitis.
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Fig. 12B —77-year-old man with focal thickening of jejunum due to
diverticulitis. Coronal CT enterography image in same patient several
centimeters caudal to A clearly shows a proximal jejunal diverticulum
(arrow). Note normal small bowel (arrowheads). Surgery
confirmed perforated diverticulitis (arrow).
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Length of Involvement
The second criterion used to evaluate an abnormal small-bowel loop is the
length of involvement. Determination of the length of involvement is
particularly facilitated by using coronal multiplanar reformatted and 3D
volume-rendered images obtained with MDCT
[13] (Figs.
5A,
5B,
7A,
7B,
7C,
9A,
9B,
9C, and
11). Pathologic conditions
tend to cause focal involvement ( 5 cm), segmental involvement (6-40 cm),
or diffuse involvement (> 40 cm). Although these lengths are somewhat
arbitrary, they aid in narrowing the differential diagnosis
[1].
Focal Involvement
Conditions that cause focal small-bowel abnormalities include neoplasms,
endometriosis, small-bowel diverticulitis, foreign-body perforations,
small-bowel ulcers from the use of nonsteroidal antiinflammatory drugs, and,
occasionally, granulomatous processes such as tuberculosis and Crohn's disease
[24,
25,
27-29]
(Fig. 12A,
12B). Focal tumors of the
small bowel are usually due to metastasis, adenocarcinoma, and GIST. GIST
tumors tend to be round and more eccentric or exophytic than circumferential
lesions such as adenocarcinoma
[24]. Foreign-body
perforations are often due to fish bones that appear as thin, linear,
hyperdense structures in the small bowel. The affected segment will appear as
a short length of mural thickening, often with mural stratification. Increased
density in the perienteric fat reflects the mesenteric reaction to the
perforation. Intraperitoneal gas may be present.
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Fig. 13 —62-year-old woman with diffuse small-bowel thickening due to
encasement and obstruction of superior mesenteric vein (SMV) by neuroendocrine
tumor. Coronal reformatted CT image shows encasement of SMV by neoplasm
(arrowheads) and mild diffuse edema throughout small bowel
(arrows).
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Fig. 14 —50-year-old man with abdominal pain. Axial CT image shows short
segment (15 cm) of marked (25 mm) mural thickening in distal ileum
(arrows) with homogeneous enhancement. Small-bowel lymphoma was
confirmed at surgery.
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Segmental Involvement
Conditions that typically result in segmental involvement of the affected
small bowel include intramural hemorrhage, Crohn's disease, lymphoma,
infectious enteritis, and, occasionally, intestinal ischemia, particularly
when the cause is SMA embolus or SMV thrombosis
[17,
18,
23,
30,
31]. Secondary signs will
often be present in patients with Crohn's disease, including skip areas,
fibrofatty proliferation, fistulas, prominent vasa recta, and, occasionally,
abscess formation [14].
Vasculitis and angioedema may result in a segmental or diffuse distribution of
abnormality [16,
19]. These conditions
classically show a target sign with small-bowel edema. When the segmental
distribution is localized in a particular region of the peritoneal cavity in a
patient with a prior malignancy, a history of radiation therapy should be
sought. The effects of radiation may be acute or may manifest many years after
therapy [32]. Although
lymphoma may have numerous morphologic manifestations, it tends to cause
segmental involvement in the small bowel. As opposed to the nonneoplastic
conditions listed previously, lymphoma most frequently results in homogeneous
enhancement in the affected segment
[23].
Diffuse Involvement
Diffuse involvement of the small bowel is seen in benign conditions.
Conditions that may cause diffuse thickening include hypoalbuminemia, low-flow
intestinal ischemia and proximal SMA embolus, vasculitis, angioedema,
graft-versus-host disease, and infectious enteritis
[17-19,
33,
34] (Figs.
6A,
6B,
6C and
13). Patients with
hypoalbuminemia will typically show edematous changes in the subcutaneous
tissues, peritoneum, and retroperitoneum. When diffuse small-bowel thickening
is present, the SMA should be carefully inspected for filling defects and
caliber. In low-flow states, the caliber of the SMA is usually quite small. In
patients with acute hypovolemia or shock, a typical appearance of the small
bowel known as "shock bowel" may be seen. In these patients, mild
to moderate diffuse small-bowel thickening and marked hyperenhancement of the
mucosa are seen [35]. The
findings in these patients appear to be related to reversible ischemia
[35]. Other typical CT
findings in these patients include hyperenhancing adrenal glands and a
slitlike inferior vena cava due to the hypovolemia.
Degree of Thickening
The degree of thickening is the third major criterion used to evaluate an
abnormal small bowel. When the normal small bowel is distended, the wall
measures no greater than 2 mm. If the small bowel is not distended, an
accurate assessment of the degree of wall thickening is often impossible.
Mural thickening can be stratified into three categories: mild (3-4 mm),
moderate (5-9 mm), and marked ( 10 mm). Although conditions that cause
mild, moderate, and marked thickening overlap, these categories do help in
narrowing the differential diagnosis of the abnormal small bowel.
Mild Thickening
Mild thickening of the small bowel is seen in hypoalbuminemia, infectious
enteritis, and occasionally in patients with ischemia due to lack of arterial
inflow or mild Crohn's disease
[17,
18,
36-38]
(Fig. 6A,
6B,
6C). Patients with intestinal
ischemia related to mesenteric venous thrombosis typically have moderate to
marked thickening of the small bowel
[18,
30]. Most other common
abnormalities affecting the small bowel cause moderate to marked
thickening.
Moderate Thickening
Moderate thickening of the small bowel is seen in patients with Crohn's
disease, intestinal ischemia, intramural hemorrhage, angioedema, and
vasculitis [14,
16-19]
(Fig. 7A,
7B,
7C). Some neoplastic processes
such as low-T-stage adenocarcinoma and some lymphomas can also show moderate
thickening [23] (Fig.
9A,
9B,
9C).
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Fig. 15A —Differentiating mucosal from submucosal disease. Coronal reformatted
image of terminal ileum in 27-year-old man with surgically proven perforated
appendicitis shows moderate to marked thickening of terminal ileum
(arrow). Mucosa is smooth, and at surgery secondary edema of terminal
ileum was present due to perforated appendix and abscess
(arrowhead).
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Fig. 15B —Differentiating mucosal from submucosal disease. Coronal reformatted
image of terminal ileum in 34-year-old man with endoscopically proven Crohn's
disease shows moderated to marked thickening and irregularity of terminal
ileum mucosa (arrow) consistent with multiple ulcerations. Note
adjacent abscess (arrowhead).
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Marked Thickening
Conditions that cause marked thickening ( 10 mm) of the small bowel
include lymphoma and other neoplasms, vasculitis, Crohn's disease, and
intramural hemorrhage (Fig.
14). Infectious bacterial and viral colitis may result in marked
thickening of the colon [39].
However, it is unusual for infectious enteritis to show marked mural
thickening. Ischemia of the small bowel causes mild to moderate thickening
unless due to venous occlusion
[17,
30]. Crohn's disease may
result in mild, moderate, or marked thickening of the small bowel
[14]. Finally, most cases of
small-bowel wall thickening measuring > 20 mm are due to neoplasms and,
occasionally, to intramural hemorrhage.
Symmetric Versus Asymmetric Thickening
Most conditions that cause symmetric thickening along the circumference of
the small bowel are benign. Crohn's disease and other granulomatous conditions
such as tuberculosis may occasionally cause asymmetric thickening
[14,
29]. Asymmetric thickening
along the circumference of the wall of the small bowel is usually seen with
neoplasms [40]. Lymphoma in
the small bowel may show symmetric thickening
[23,
40].
Location Along the Course of the Small Bowel (Proximal or Distal)
In general, the location along the length of the small bowel cannot be used
to reliably differentiate abnormal conditions. Adenocarcinoma of the small
bowel tends to occur proximally (duodenum and jejunum), whereas lymphoma and
carcinoid tumors are more frequent in the ileum
[40]. Although Crohn's disease
has a predilection for the terminal ileum, it may affect any segment of the
gastrointestinal tract [41].
Celiac disease tends to affect the proximal small bowel, where a paucity of
small-bowel folds may be detected at MDCT
[41,
42].
Location in the Wall of the Small Bowel (Mucosal, Submucosal, or Serosal)
The determination of whether a process affects primarily the mucosa, the
submucosa, or the serosal surface of the small bowel is an important criterion
in determining the cause of the disorder. Although the fine mucosal detail of
a small-bowel series or the actual visualization of the mucosal surface on
endoscopy is superior to that on MDCT, the location can often be inferred by
typical MDCT signs (Fig. 15A,
15B).
Mucosal Disease
The inner surface of the small bowel is the mucosa, which should have a
smooth appearance. Diseases that affect and disrupt the small-bowel mucosa and
can be seen on MDCT include neoplasms and certain inflammatory processes such
as Crohn's disease and tuberculosis (Fig.
11). Other infectious processes and intestinal ischemia may affect
the small-bowel mucosa; however, these processes generally cannot be seen to
disrupt the mucosa on CT.
Submucosal Disease
Submucosal deposition of edema or blood will cause a target sign that can
be visualized on MDCT when a rapid bolus of IV contrast agent is administered.
Submucosal disease is seen in intramural hemorrhage, vasculitis, ischemia,
angioedema, and hypoalbuminemia (Figs.
4,
5A,
5B,
7A,
7B,
7C, and
8). The appearance of the
bowel wall on MDCT will show a smooth inner surface or straightened thick
parallel folds that have been called a "stacked-coin" or
"picket fence" appearance on barium studies.
Serosal Disease
On barium examinations, serosal disease is recognized as tethering or
spiculation of the folds [43,
44]. This same pattern may be
seen on CT and, in addition, the cause of the serosal disease can often be
determined (Fig. 16A,
16B). Conditions that cause
serosal disease include metastases, carcinoid tumors, endometriosis, and other
inflammatory conditions in the peritoneal cavity.
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Fig. 16A —55-year-old woman with serosal disease due to carcinoid tumor.
Coronal reformatted CT image shows tethering of multiple loops of small bowel
(arrows) toward partially calcified mass in mesentery
(arrowhead).
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Fig. 16B —55-year-old woman with serosal disease due to carcinoid tumor. Spot
compression view from small-bowel series shows tethering and spiculation of
folds (arrows) along mesenteric surface of bowel. Carcinoid tumor was
removed at surgery. Tumor incites desmoplastic reaction, resulting in
appearance of small-bowel serosa.
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Associated Abnormalities in the Mesentery and Vessels
As has been discussed throughout this article, the mesenteric vasculature;
the size, location, and attenuation of lymph nodes; and the status of the
mesentery serve as important clues in the differential diagnosis of an
abnormal bowel. Low-attenuation lymph nodes suggest tuberculosis;
soft-tissue-attenuation lymph nodes suggest lymphoma, Crohn's disease, or
mesenteric adenitis. The SMA and SMV must always be assessed when an abnormal
small-bowel loop is present.
Conclusion
The differential diagnosis of the abnormal small bowel is extensive,
including variants and pitfalls, inflammatory conditions, and neoplasms.
Optimal evaluation of an abnormal small-bowel loop is facilitated when the
small bowel is well distended, IV contrast material has been administered, and
thin-section CT is used. CT enterography should be used when a clinical
concern exists for small-bowel disease. When an abnormal small-bowel loop is
recognized, a pattern approach as discussed herein can be used to narrow the
differential diagnosis.
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Abstract
Introduction
