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Macari et al.

Gastrointestinal Imaging • Review


MDCT and CT
Enterography of the Small
Bowel

A Pattern Approach to the


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Abnormal Small Bowel:


Observations at MDCT and
CT Enterography
Michael Macari1 OBJECTIVE. Imaging of the vast array of pathologic processes occurring in the small
Alec J. Megibow bowel has been facilitated by recent advances, including the use of MDCT scanners that acquire
Emil J. Balthazar 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
Macari M, Megibow AJ, Balthazar EJ narrow the differential diagnosis when an abnormal small-bowel loop is detected on MDCT.

maging of pathologic processes identified in the small bowel at MDCT and

I occurring in the small bowel has


traditionally been performed with
barium small-bowel follow-through
CT enterography.

Technique
examinations, single- or double-contrast intu- Confident detection and optimal evaluation
bated enteroclysis, and CT [1]. Recent inno- of an abnormal segment or loop of small bowel
vations, including capsule endoscopy and is achieved when the small bowel is well dis-
MRI, have emerged as alternative small- tended, IV contrast has been administered, and
bowel imaging techniques that can be per- thin-section (≤ 1-mm) CT is used. Tradition-
formed without ionizing radiation [2, 3]. ally, positive contrast materials such as dilute
Technical advances have improved the imag- barium or water-soluble iodinated solutions
ing evaluation of the small bowel using CT [4, have been used to mark and sometimes distend
5]. These advances include the use of MDCT the small bowel at CT [1, 5]. These contrast
scanners that acquire isotropic data, oral con- agents work well in delineating the small
trast agents, and administration techniques that bowel, the degree of distention being propor-
improve small-bowel distention. These ad- tionate to the amount of contrast material con-
vances, coupled with imaging workstations that sumed, the rate at which it is consumed, and
allow multiplanar and 3D evaluation of these the time delay of the examination itself. When
isotropic data sets, have allowed improved de- the small bowel is distended with positive con-
piction and characterization of small-bowel pa- trast material, wall thickness ranges from im-
thology. The use of MDCT, neutral (attenuation perceptible to no greater than 2 mm [1]
Keywords: CT, CT technique, inflammatory bowel disease, values between 10–30 H) oral contrast agents to (Fig. 2). However, unless care is taken in ad-
small bowel distend the small bowel, and multiplanar thin- ministering these agents, any portion of the
section data evaluation has come to be known as bowel may be either underdistended or even
DOI:10.2214/AJR.06.0712 CT enterography (Fig. 1). unfilled with contrast material, leading to a
Received May 27, 2006; accepted after revision
Current indications for performing CT en- possible false-positive diagnosis. In general,
October 11, 2006. terography include the evaluation of obscure adequate luminal distention is present if the di-
gastrointestinal bleeding, the presence and ameter of the small bowel is ≥ 2 cm.
M. Macari and A. J. Megibow are consultants to E-Z-EM. activity of Crohn’s disease, and suspected When the small bowel is distended with
1All authors:
small-bowel neoplasia. Moreover, a vast ar- positive contrast material, the wall is thin and
Department of Radiology, Division of
Abdominal Imaging, NYU Medical Center, 560 First Ave.,
ray of pathologic processes occurring in the may be imperceptible but should not measure
Ste. HW 207, New York, NY 10016. Address small bowel will be detected incidentally at more that 1–2 mm [1]. Dilute barium and io-
correspondence to M. Macari MDCT in patients with abdominal pain. The dinated positive oral contrast agents are par-
(michael.macari@med.nyu.edu). differential diagnosis for these processes is ticularly well suited in evaluating thin pa-
AJR 2007; 188:1344–1355
broad and can be confusing. The purpose of tients without a lot of intraperitoneal adipose
this article is to show how a systematic pattern tissues and in oncology patients, in whom im-
0361–803X/07/1885–1344
approach can be used to narrow the differen- plants and lymph nodes will stand out from
© American Roentgen Ray Society tial diagnosis when an abnormal process is the small bowel. A potential limitation of pos-

1344 AJR:188, May 2007


MDCT and CT Enterography of the Small Bowel
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Fig. 1—30-year-old woman with normal CT findings at enterography. Coronal Fig. 2—60-year-old man with excellent small-bowel distention on CT using positive
reformatted image of small bowel using neutral oral and IV contrast agents shows oral contrast material. Coronal reformatted image of small bowel shows normal small
normal small bowel (arrows). Note wall of small bowel is thin, measuring 1–2 mm, and bowel. Note wall of small bowel (arrows) is barely perceptible.
shows uniform mural enhancement. Moreover, normal fold pattern of jejunum (many
folds) is distinguished from that of ileum (few folds).

itive oral contrast agents in the evaluation of they are superior to both water and methylcel- changing for the examination, the patient con-
the small bowel is that mucosal enhancement lulose in achieving small-bowel distention sumes 225 mL of water, and finally, on enter-
may be obscured by the luminal contrast ma- [5–7, 12]. The initial studies evaluating the ing the scanning room, the patient drinks a fi-
terial, and thus the pattern of enhancement, potential use of CT enterography were per- nal 225 mL of water. The total volume of fluid
which serves as a primary aid in the differen- formed with positive oral contrast agents [8]. is therefore 1,350 mL. Water is adequate for
tial diagnosis of an abnormal small-bowel However, since that time, CT enterography in the final contrast agent because it is designed
segment, may be impaired (Fig. 3). most reports has been performed with a neu- primarily to distend the stomach and duode-
Neutral oral contrast agents allow full visu- tral oral contrast agent [5–7, 9–12]. num. Other imaging centers deliver a similar
alization of the normal intestinal wall, thereby Peroral CT enterography differs from CT volume of contrast material over a 1-hour pe-
allowing analysis of the degree and pattern of enteroclysis in that the latter technique is per- riod (450 mL 60 minutes and 40 minutes be-
small-bowel enhancement [5–12]. “Neutral formed after placement of a nasojejunal tube fore scanning and 225 mL 20 and 10 minutes
contrast” refers to agents that have an attenua- in conjunction with active small-bowel dis- before scanning) [12].
tion value similar to that of water (10–30 H). tention. CT enterography performed with The optimal timing of the administration of
For neutral contrast agents to be effective, they VoLumen is inferior to CT enteroclysis in oral contrast material will continue to be in-
must be used with IV contrast material and the achieving small-bowel distention [9]. How- vestigated. It is likely easier for the patient to
small-bowel distention must be optimal. ever, the noninvasive nature and speed of CT ingest the oral volume over a longer period of
Several neutral contrast agents have been enterography make it well suited as a first-line time. However, if ingested over too long a pe-
evaluated for small-bowel distention, includ- technique for the evaluation of suspected riod, the contrast material may be in the co-
ing water, water in combination with a bulk- small-bowel disease [4, 5, 12]. lon. Whether the contrast material is adminis-
ing agent such as methylcellulose or locust Our specific protocol for performing CT tered over 30 or 60 minutes, if insufficient
bean gum, polyethylene glycol solutions, and enterography requires that the patient fast for volume is ingested, suboptimal small-bowel
a commercially available low-density barium at least 3 hours before the examination. This distention will limit the CT enterography ex-
solution (VoLumen [low-Hounsfield-value will decrease the possibility of misinterpret- amination. Therefore, the importance of the
barium sulfate], E-Z-EM) [5, 6]. A limitation ing a foreign body as a polyp or tumor. On ar- oral contrast agent must be explained to the
of using water is that it is rapidly absorbed rival at the imaging center, patients ingest two patient. This is facilitated by having the CT
across the small-intestinal mucosa, resulting 450-mL bottles of VoLumen over a 30-minute technologist or nurse instruct and monitor pa-
in suboptimal small-bowel distention. VoLu- period. The first bottle is ingested 30 minutes tients as they are ingesting the oral contrast
men and polyethylene glycol solutions are before the procedure, the second 20 minutes material. If patients are left on their own, sub-
less rapidly absorbed; studies have shown that before the procedure. Immediately before optimal distention may result.

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Macari et al.
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A B
Fig. 3—47-year-old man with ileal Crohn’s disease.
A, Axial CT image with positive intraluminal oral contrast material shows loop of thickened ileum (arrow). However, pattern of enhancement is obscured by contrast material.
B, 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.

IV contrast enhancement is essential when facts. At our institution, we use either a approach can be used to narrow the differen-
performing CT enterography. A 20-gauge 16 × 0.75 mm or 64 × 0.6 mm detector con- tial diagnosis [1]. Seven criteria can be used
catheter is inserted into an arm vein, and 1.5 figuration, depending on whether a 16- or 64- to aid in the evaluation of the abnormal small
mL/kg of iodinated contrast material (Ul- MDCT scanner is used, reconstructing either bowel on contrast-enhanced MDCT, includ-
travist, 300 mg I/mL, [iopromide], Berlex 1- or 0.8-mm slices. From this data set, the ing the pattern of enhancement, the length of
Laboratories) is injected at a rate of at least 4 technologist will generate a set of axial 4-mm involvement, the degree of thickening,
mL/s. Without IV contrast material, the bowel sections and a set of 3-mm-thick coronal mul- whether the thickening is symmetric or asym-
wall is not seen and intestinal marking is com- tiplanar reformatted images at 3-mm intervals metric, location of the lesion along the course
promised. If there is a possibility of compro- encompassing the entire bowel. These are of the small bowel (proximal or distal), loca-
mised venous access or the patient cannot re- sent to the PACS for review. tion of the lesion in the wall of the small
ceive IV contrast material, we perform the In addition, the thin slices are sent to a bowel (mucosal, submucosal, or serosal),
study with a positive contrast agent. workstation, where they are available for the and, finally, associated abnormalities in the
The optimal timing of data acquisition for radiologist to view the data in 3D volume- mesentery and vessels.
CT enterography is somewhat controversial. rendering or maximum-intensity-projection
We begin the acquisition 60 seconds after the displays [12, 13]. Images are acquired at 120 Mural Enhancement Pattern
initiation of the bolus. Others have suggested kVp, 0.4-second gantry rotation, and 180 ef- The first criterion that should be assessed
that an enterography phase (≈ 45 seconds af- fective mAs. A dose modulator, available on when evaluating an abnormal loop of small
ter the injection), or even a dual-phase acqui- all MDCT scanners, which automatically bowel is the mural enhancement pattern. Four
sition, may be helpful in patients with obscure decreases the radiation exposure to thinner patterns may be present during contrast-en-
gastrointestinal bleeding [10–12]. Glucagon areas of the patient, is used and can reduce hanced CT. These include a double-halo or
in a dose of 0.1 mg is administered IV and the dose up to 30%. target appearance, referred to as mural strati-
given a few minutes before data acquisition to fication; homogeneous or hyperenhance-
diminish peristalsis. A Pattern Approach to the ment; heterogeneous enhancement; and de-
MDCT enterography should be performed Abnormal Small Bowel at MDCT creased or absent enhancement.
on a 16-MDCT or higher scanner. These An abnormal small-bowel loop is present
scanners can acquire the submillimeter iso- when the wall thickness is ≥ 3 mm despite ad- Target Appearance
tropic data necessary for 3D displays in a equate luminal distention [1]. When an abnor- If the abnormal segment of small bowel
short enough time to minimize motion arti- mal small-bowel loop is recognized, a pattern displays a target appearance, a benign process

1346 AJR:188, May 2007


MDCT and CT Enterography of the Small Bowel

Fig. 4—35-year-old is present in the wall [14]. The target sign


woman with target results from mucosal and serosal enhance-
appearance in small
bowel due to lupus ment surrounding a prominent low-attenua-
vasculitis. Axial CT image tion submucosa (Fig. 4). Visualization of a
in this patient with target appearance is facilitated by having neu-
systemic lupus
erythematosus shows
tral contrast material in the small-bowel lu-
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marked mural thickening men (Fig. 3). The neutral contrast agent al-
(> 1 cm) (long arrow) and lows better depiction of the inner aspect of the
target appearance after wall of the small bowel. The target sign was
contrast administration.
Note edematous first described as a specific sign for Crohn’s
changes in right kidney disease [15], but it is now recognized that any
due to lupus nephritis nonneoplastic condition may lead to a target
(short arrow).
appearance in the small bowel. Common
causes include Crohn’s disease, infection, is-
chemia, radiation enteritis, angioedema, and
hemorrhage [1, 14, 16–20] (Figs. 4–6).
A relatively rare condition that generally
shows long segments or even diffuse small-
bowel involvement with a target appearance is
angioedema [16] (Fig. 7). Angioedema may
be congenital or acquired and is due to in-
creased capillary permeability in the mucosa
that results in submucosal edema. This condi-
tion may occur in the skin, airways, or intes-
tine 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 angio-
tensin-converting enzyme inhibitor, which ap-
pears to be an inciting event [16]. The major
differential diagnosis of angioedema is is-
chemia and vasculitis [16–20]. If the diagnosis
of angioedema is considered at imaging, labo-
Fig. 5—45-year-old ratory testing can be helpful because the C1
woman with target esterase inhibitor level is low in this condition.
appearance in small In patients with small-bowel thickening due to
bowel due to acute
radiation enteritis. A vasculitis, there is a combination of edema and
A, Axial CT image in hemorrhage in the wall secondary to the vas-
patient, who has cervical culitis-induced ischemia [19, 20].
cancer and just finished
4-week course of
Submucosal hemorrhage has been classi-
radiation therapy. Note cally thought to cause homogeneous en-
moderate mural hancement of the bowel wall after IV con-
thickening (5–10 mm) trast administration [17]. However, after
(arrow) and target
appearance after administration of a rapid bolus of IV con-
contrast administration. trast material, the small bowel usually
B, Coronal reformatted shows a target appearance in the setting of
image shows segmental
involvement of abnormal
submucosal hemorrhage [17] (Fig. 8). The
loop in pelvis (long major differential diagnosis of small-bowel
arrow) and normal- submucosal hemorrhage is intestinal is-
appearing loop in chemia. Both conditions tend to occur in
abdomen (short arrow).
Inflammatory process elderly patients. Most patients with submu-
was localized to loops of cosal hemorrhage will present with acute
small bowel in pelvis abdominal pain and will be found to be at in-
within radiation field;
findings were attributed creased risk of bleeding, usually from anti-
to acute radiation coagulation with warfarin. Laboratory tests
enteritis. will show an elevated international normal-
B ized ratio level, usually greater than 4 [17].

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Macari et al.

Fig. 6—80-year-old man shown that this may be a normal variant and
with target appearance may not necessarily be associated with
in small bowel due to
superior mesenteric chronic bowel inflammation [22]. In a study
artery (SMA) embolus. of 100 patients undergoing unenhanced CT to
A, Axial CT image in evaluate for kidney stones, 21 patients were
patient who has atrial
fibrillation and abdominal
shown to have submucosal adipose tissue in
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pain shows mild to the bowel, and in 4% it was in the terminal il-
moderate mural eum. These patients had no history of chronic
thickening (≈ 5 mm) (long bowel inflammation. Therefore, if this find-
arrows) and target
appearance diffusely ing is seen at CT, correlation with the clinical
throughout small bowel history is essential.
and ascending colon When a target sign is visualized on CT, the
(short arrow).
B, Axial CT image shows differential diagnosis can be narrowed by
filling defect (long arrow) observing the degree of thickening, the
in SMA and wedge- length of the abnormal segment, associated
shaped perfusion defect
imaging abnormalities, and the clinical his-
(short arrow) in left A
kidney. Findings are tory. Only a few conditions generally cause
consistent with intestinal marked thickening of the small bowel with a
ischemia due to embolus. target appearance. These include vasculitis,
C, Intraoperative image
shows diffuse infarction Crohn’s disease, venous thrombosis with as-
of small bowel and sociated bowel edema or ischemia, and in-
cecum (arrows). Patient tramural hemorrhage. Associated findings
subsequently died.
that suggest Crohn’s disease include fibro-
fatty proliferation, hyperemia of the vasa
recta (the comb sign), sinus and fistula for-
mation, and abscess. The small-bowel me-
senteric 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.
B 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 as-
sess 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 seg-
ment with other small-bowel loops is neces-
sary. In addition, the timing and adequacy of
the bolus of IV contrast material that was ad-
ministered need to be assessed.
C
If the enhancement is mild and the attenu-
ation is similar to muscle, one should con-
sider chronic inflammatory conditions, such
Occasionally, adipose tissue will be depos- low differentiation from edema. Submucosal as chronic Crohn’s disease, ischemia, or radi-
ited in the submucosa of the small intestine, fat deposition in the wall of the small bowel ation [1, 14]. The milder homogeneous en-
resulting in a target appearance. Recognition has been associated with chronic bowel in- hancement in these cases is likely related to
of the fat attenuation in the submucosa will al- flammation [1, 21]. However, one study has the development of fibrosis. Lymphoma and

1348 AJR:188, May 2007


MDCT and CT Enterography of the Small Bowel

Fig. 7—31-year-old man with segmental thickening of terminal ileum due to allergic
angioedema.
A, 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.
B, Coronal reformatted image better shows segmental area (30 cm) of thickening of
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terminal and distal ileum (arrows). Pattern of thickening suggests a submucosal


process. In light of submucosal appearance, differential diagnosis includes
vasculitis, angioedema, and infection.
C, 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.

B C

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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Macari et al.

Heterogeneous Enhancement
Heterogeneous enhancement is typical of
small-bowel neoplasms. Although any small-
bowel tumor may appear this way, heteroge-
neous enhancement is most frequent with ade-
nocarcinoma and malignant gastrointestinal
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stromal tumors (GISTs). The enhancement pat-


tern 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 en-
hance heterogeneously after contrast adminis-
tration [24, 25]. Metastasis and endometriotic
implants to the serosal surface of the bowel may
show heterogeneous or homogeneous enhance-
ment. Rarely, lymphoma will appear heteroge-
A
neous in its enhancement pattern.

Diminished Enhancement
The normal small bowel enhances after ad-
ministration 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 con-
trast agent and displayed in 3D, regional dif-
ferences in mural enhancement become ap-
parent. In the correct clinical situation,
decreased enhancement is pathognomonic for
intestinal ischemia [17, 18, 26]. When evalu-
ating 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. 10).
B The several causes of small-bowel ischemia
C
include strangulation due to a closed-loop ob-
Fig. 9—79-year-old man with segmental thickening of jejunum due to lymphoma. struction, low-flow states from cardiac arrhyth-
A, Axial CT image in patient with abdominal pain shows moderate thickening (9 mm) of loop of jejunum (arrow) and
adjacent abscess (arrowhead). mias, sepsis or shock, embolus or thrombosis of
B, Coronal reformatted CT image better shows segmental (15-cm) area of homogeneous thickening (long arrows). the superior mesenteric artery (SMA), and supe-
Note enlarged lymph node in adjacent mesentery (short arrow). Differential diagnosis includes Crohn’s disease rior mesenteric vein (SMV) thrombosis. In the
and lymphoma.
C, Surgical specimen reveals segmental primary small-bowel lymphoma (arrows). 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. 6). As the process
occasionally intramural hemorrhage can enhanced. If the small bowel is not well progresses to infarction, the bowel becomes thin
cause marked thickening and homogeneous distended, the wall may appear falsely and shows diminished enhancement; finally,
enhancement of the small bowel [17, 23] thick and show homogeneous enhance- when mucosal integrity is breached, pneumato-
(Fig. 9). Occasionally, Crohn’s disease will ment. This typically occurs in the jejunum. sis and perforation may occur [17, 18].
show homogeneous hyperenhancement of the In these cases, it is important to evaluate When small-bowel ischemia is suspected,
wall [4, 10]. Homogeneous hyperenhance- the perienteric mesentery for the presence the vessel caliber, presence of atheroscle-
ment in the setting of Crohn’s disease implies or absence of inflammatory changes and rotic plaque, thrombus, and embolus in the
active disease [4]. As depicted on MDCT en- vessels that should be normal as opposed to mesenteric vasculature should be carefully
terography, attenuation of the enhanced wall hyperemic. Visualization of small bubbles evaluated. At our institution, we perform a
exceeding 109 H in a loop of bowel affected of gas trapped between the valvulae con- dual-phase acquisition for patients sus-
by Crohn’s disease has a high degree of cor- niventes will help to confirm that the small- pected of having mesenteric ischemia: an
relation with disease activity [4]. bowel wall is not thickened. Finally, if arterial phase at about 30 seconds evaluat-
Again, visual assessment is usually suf- there is still concern, a small-bowel series ing the patency of the mesenteric arterial
ficient to determine if a segment is hyper- can be obtained. supply, followed by a mural phase at ap-

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MDCT and CT Enterography of the Small Bowel
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A B
Fig. 10—76-year-old man with diminished enhancement of multiple loops of small bowel. Fig. 11—49-year-old man with target appearance in
A, Coronal reformatted CT image in patient with closed-loop small-bowel obstruction due to transmesenteric segmental distribution due to acute Crohn’s disease.
hernia shows cluster of small-bowel loops with diminished enhancement (short arrows) when compared with Coronal reformatted CT image shows moderate mural
loops that are not in closed loop (long arrows). thickening (5–10 mm) with target appearance in
B, Surgical resection shows infarcted small bowel (arrow). ulcerated segment of terminal ileum (long arrows).
Additional findings supporting diagnosis of Crohn’s
disease include fibrofatty proliferation and prominent
vasa recta (short arrow).

Fig. 12—77-year-old man with focal thickening of


jejunum due to diverticulitis.
A, 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.
B, 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).
A B

proximately 60–65 seconds that captures Length of Involvement ages obtained with MDCT [13] (Figs. 5, 7, 9, and
the maximally enhanced intestinal wall. The second criterion used to evaluate an ab- 11). Pathologic conditions tend to cause focal in-
Neutral contrast-enhanced MDCT is ideal normal small-bowel loop is the length of involve- volvement (≤ 5 cm), segmental involvement
for these patients. If the patient is too ill to ment. Determination of the length of involvement (6–40 cm), or diffuse involvement (> 40 cm). Al-
drink, our ability to detect subtle changes of is particularly facilitated by using coronal multi- though these lengths are somewhat arbitrary, they
mural ischemia may be limited. planar reformatted and 3D volume-rendered im- aid in narrowing the differential diagnosis [1].

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Fig. 13—62-year-old woman with diffuse small-bowel thickening due to encasement Fig. 14—50-year-old man with abdominal pain. Axial CT image shows short segment
and obstruction of superior mesenteric vein (SMV) by neuroendocrine tumor. (15 cm) of marked (25 mm) mural thickening in distal ileum (arrows) with
Coronal reformatted CT image shows encasement of SMV by neoplasm homogeneous enhancement. Small-bowel lymphoma was confirmed at surgery.
(arrowheads) and mild diffuse edema throughout small bowel (arrows).

Focal Involvement distribution of abnormality [16, 19]. These fuse small-bowel thickening and marked hy-
Conditions that cause focal small-bowel ab- conditions classically show a target sign with perenhancement of the mucosa are seen [35].
normalities include neoplasms, endometriosis, small-bowel edema. When the segmental dis- The findings in these patients appear to be re-
small-bowel diverticulitis, foreign-body perfo- tribution is localized in a particular region of lated to reversible ischemia [35]. Other typi-
rations, small-bowel ulcers from the use of the peritoneal cavity in a patient with a prior cal CT findings in these patients include hy-
nonsteroidal antiinflammatory drugs, and, oc- malignancy, a history of radiation therapy perenhancing adrenal glands and a slitlike
casionally, granulomatous processes such as should be sought. The effects of radiation may inferior vena cava due to the hypovolemia.
tuberculosis and Crohn’s disease [24, 25, be acute or may manifest many years after
27–29] (Fig. 12). Focal tumors of the small therapy [32]. Although lymphoma may have Degree of Thickening
bowel are usually due to metastasis, adenocar- numerous morphologic manifestations, it The degree of thickening is the third major
cinoma, and GIST. GIST tumors tend to be tends to cause segmental involvement in the criterion used to evaluate an abnormal small
round and more eccentric or exophytic than small bowel. As opposed to the nonneoplastic bowel. When the normal small bowel is dis-
circumferential lesions such as adenocarci- conditions listed previously, lymphoma most tended, the wall measures no greater than 2
noma [24]. Foreign-body perforations are of- frequently results in homogeneous enhance- mm. If the small bowel is not distended, an ac-
ten due to fish bones that appear as thin, linear, ment in the affected segment [23]. curate assessment of the degree of wall thicken-
hyperdense structures in the small bowel. The ing is often impossible. Mural thickening can
affected segment will appear as a short length Diffuse Involvement be stratified into three categories: mild (3–4
of mural thickening, often with mural stratifi- Diffuse involvement of the small bowel is mm), moderate (5–9 mm), and marked (≥ 10
cation. Increased density in the perienteric fat seen in benign conditions. Conditions that mm). Although conditions that cause mild,
reflects the mesenteric reaction to the perfora- may cause diffuse thickening include hypo- moderate, and marked thickening overlap,
tion. Intraperitoneal gas may be present. albuminemia, low-flow intestinal ischemia these categories do help in narrowing the differ-
and proximal SMA embolus, vasculitis, an- ential diagnosis of the abnormal small bowel.
Segmental Involvement gioedema, graft-versus-host disease, and in-
Conditions that typically result in segmental fectious enteritis [17–19, 33, 34] (Figs. 6 and Mild Thickening
involvement of the affected small bowel in- 13). Patients with hypoalbuminemia will typ- Mild thickening of the small bowel is seen
clude intramural hemorrhage, Crohn’s disease, ically show edematous changes in the subcu- in hypoalbuminemia, infectious enteritis, and
lymphoma, infectious enteritis, and, occasion- taneous tissues, peritoneum, and retroperito- occasionally in patients with ischemia due to
ally, intestinal ischemia, particularly when the neum. When diffuse small-bowel thickening lack of arterial inflow or mild Crohn’s disease
cause is SMA embolus or SMV thrombosis is present, the SMA should be carefully in- [17, 18, 36–38] (Fig. 6). Patients with intesti-
[17, 18, 23, 30, 31]. Secondary signs will often spected for filling defects and caliber. In low- nal ischemia related to mesenteric venous
be present in patients with Crohn’s disease, in- flow states, the caliber of the SMA is usually thrombosis typically have moderate to
cluding skip areas, fibrofatty proliferation, fis- quite small. In patients with acute hypo- marked thickening of the small bowel [18,
tulas, prominent vasa recta, and, occasionally, volemia or shock, a typical appearance of the 30]. Most other common abnormalities af-
abscess formation [14]. Vasculitis and an- small bowel known as “shock bowel” may be fecting the small bowel cause moderate to
gioedema may result in a segmental or diffuse seen. In these patients, mild to moderate dif- marked thickening.

1352 AJR:188, May 2007


MDCT and CT Enterography of the Small Bowel

Fig. 15—Differentiating mucosal from submucosal


disease.
A, 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
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(arrowhead).
B, 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).

A B

Moderate Thickening small bowel is usually seen with neoplasms clude neoplasms and certain inflammatory pro-
Moderate thickening of the small bowel is [40]. Lymphoma in the small bowel may cesses such as Crohn’s disease and tuberculosis
seen in patients with Crohn’s disease, intestinal show symmetric thickening [23, 40]. (Fig. 11). Other infectious processes and intes-
ischemia, intramural hemorrhage, angio- tinal ischemia may affect the small-bowel mu-
edema, and vasculitis [14, 16–19] (Fig. 7). Location Along the Course of the cosa; however, these processes generally can-
Some neoplastic processes such as low-T-stage Small Bowel (Proximal or Distal) not be seen to disrupt the mucosa on CT.
adenocarcinoma and some lymphomas can In general, the location along the length of the
also show moderate thickening [23] (Fig. 9). small bowel cannot be used to reliably differen- Submucosal Disease
tiate abnormal conditions. Adenocarcinoma of Submucosal deposition of edema or blood
Marked Thickening the small bowel tends to occur proximally will cause a target sign that can be visualized
Conditions that cause marked thickening (duodenum and jejunum), whereas lymphoma on MDCT when a rapid bolus of IV contrast
(≥ 10 mm) of the small bowel include lym- and carcinoid tumors are more frequent in the il- agent is administered. Submucosal disease is
phoma and other neoplasms, vasculitis, eum [40]. Although Crohn’s disease has a pre- seen in intramural hemorrhage, vasculitis, is-
Crohn’s disease, and intramural hemorrhage dilection for the terminal ileum, it may affect chemia, angioedema, and hypoalbuminemia
(Fig. 14). Infectious bacterial and viral colitis any segment of the gastrointestinal tract [41]. (Figs. 4, 5, 7, and 8). The appearance of the
may result in marked thickening of the colon Celiac disease tends to affect the proximal small bowel wall on MDCT will show a smooth in-
[39]. However, it is unusual for infectious en- bowel, where a paucity of small-bowel folds ner surface or straightened thick parallel folds
teritis to show marked mural thickening. Is- may be detected at MDCT [41, 42]. that have been called a “stacked-coin” or
chemia of the small bowel causes mild to “picket fence” appearance on barium studies.
moderate thickening unless due to venous oc- Location in the Wall of the Small Bowel
clusion [17, 30]. Crohn’s disease may result (Mucosal, Submucosal, or Serosal) Serosal Disease
in mild, moderate, or marked thickening of The determination of whether a process af- On barium examinations, serosal disease is
the small bowel [14]. Finally, most cases of fects primarily the mucosa, the submucosa, or recognized as tethering or spiculation of the
small-bowel wall thickening measuring > 20 the serosal surface of the small bowel is an im- folds [43, 44]. This same pattern may be seen
mm are due to neoplasms and, occasionally, portant criterion in determining the cause of the on CT and, in addition, the cause of the sero-
to intramural hemorrhage. disorder. Although the fine mucosal detail of a sal disease can often be determined (Fig. 16).
small-bowel series or the actual visualization of Conditions that cause serosal disease include
Symmetric Versus the mucosal surface on endoscopy is superior to metastases, carcinoid tumors, endometriosis,
Asymmetric Thickening that on MDCT, the location can often be in- and other inflammatory conditions in the
Most conditions that cause symmetric ferred by typical MDCT signs (Fig. 15). peritoneal cavity.
thickening along the circumference of the
small bowel are benign. Crohn’s disease and Mucosal Disease Associated Abnormalities in the
other granulomatous conditions such as tu- The inner surface of the small bowel is the Mesentery and Vessels
berculosis may occasionally cause asymmet- mucosa, which should have a smooth appear- As has been discussed throughout this arti-
ric thickening [14, 29]. Asymmetric thicken- ance. Diseases that affect and disrupt the small- cle, the mesenteric vasculature; the size, loca-
ing along the circumference of the wall of the bowel mucosa and can be seen on MDCT in- tion, and attenuation of lymph nodes; and the

AJR:188, May 2007 1353


Macari et al.
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A B
Fig. 16—55-year-old woman with serosal disease due to carcinoid tumor.
A, Coronal reformatted CT image shows tethering of multiple loops of small bowel (arrows) toward partially calcified mass in mesentery (arrowhead).
B, 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.

status of the mesentery serve as important tikakis J, et al. Assessment of Crohn’s disease ac- terial: initial results of a noninvasive imaging ap-
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