Dr. Al-Hawary is a Clinical Assistant Professor, Dr. Kaza is a Clinical Assistant Professor, and Dr. Platt is
a Professor of Radiology, Director of Body CT, and Director of Abdomen
Division, Radiology Department, University of Michigan Health System,
Ann Arbor, MI.The utilization of cross-sectional imaging in
the evaluation of the small bowel has been growing in recent years, with
a significant shift away from fluoroscopic imaging modalities using
positive enteric contrast, and toward cross-sectional imaging, primarily
computed tomography (CT).
This change is attributed to several
technological advances in CT imaging, including the introduction of
multidetector technology that began with 4 slices and moved to, more
recently, clinically available scanners offering up to 320-detector
rows. Multidetector CT (MDCT) allows for the acquisition of multiple
image slices with every gantry rotation, improving temporal and spatial
resolution of the examination and increasing the area of coverage during
a short interval for homogeneous acquisition in a single-phase of
enhancement. The significantly shorter scanning time improves
visualization and assessment of the small bowel by decreasing motion
artifacts and allowing rapid scan acquisition at multiple phases of
enhancement. Decreasing slice thickness, on the other hand, improves
spatial resolution, leading to
acquisition of nearly isotropic voxels. This, in turn, improves
assessment of small structures, such as terminal mesenteric vessels, and
allows for optimal multiplanar and 3-dimensional-volumetric
reconstruction of the bowel and mesenteric vessels (Figure 1).
A
second, and probably equally, important advance that has improved
assessment of the small bowel is negative (neutral or low Hounsfield
units (HU)) enteric contrast. The low, near-water density of the new
oral contrast permits assessment of the mucosal density or enhancement
pattern, in the background of the low attenuation within the lumen,
which may be affected by multiple pathologies such as inflammation or
masses (Figure 2). Since the CT examination is optimized in technique
and use of oral contrast to evaluate the enteric system, it is usually
referred to as CT enterography (CTE).
This article reviews CTE
techniques for optimizing small bowel and mesentery evaluation,
including mesenteric vessels, and reviews the appearances of common
pathologies that can be evaluated more effectively with current MDCT
with an emphasis on the evaluation of patients with inflammatory bowel
disease.
MDCT scan parameters
Multidetector CT
scanners allow acquisition of several slices, depending on detector
configuration, during a single gantry rotation. These range from 4- to
320-multirow detectors, depending on scanner type and manufacturer.
Depending on the detector configuration, extremely thin, submillimeter
slices can be acquired. The imaging slices can then be reconstructed in
any thickness, commonly between 2 and 3 mm, preserving the quality of
the examination while decreasing the number of images for easier review.
The thinner slices are used for problem solving and for generating
3-dimensional and multiplanar images.1 The nearly isotropic
voxel acquisition offers an additional advantage in bowel imaging,
allowing for improved spatial resolution, better visualization of the
mucosa, and appreciation of the different bowel wall layers, especially
in disease states.
Timing of scan acquisition
After
intravenous (IV) contrast administration, the small bowel can be imaged
in 4 different phases of enhancement: arterial, enteric, venous, and
delayed. The selection of scan timing and number of acquisition phases
to optimize evaluation depends primarily on clinical presentation of the
suspected pathology. In evaluating patients with Crohn’s disease, a
single enteric or venous phase scan is considered adequate for
evaluation of bowel-wall abnormalities and enhancement patterns, and to
assess for extra-intestinal complications.2
For
imaging small bowel tumors and assessing vascular abnormalities a
biphasic evaluation in the arterial and
enteric or venous phases at minimum is essential to detect arterially
enhancing lesions, to assess the patency of vessels, and to evaluate the
solid organs for focal abnormalities, such as metastases. More delayed
phases may also be obtained in the investigation of occult
gastrointestinal (GI) bleeding for improved sensitivity and
characterization of small vascular malformations or minute amounts of
bleeding.3,4 Bolus-tracking or bolus-triggered methods for
the acquisition time can be optimized at the intended phase to get the
arterial phase, immediately followed by the enteric phase (20 to 25 sec)
or delayed phase (70 to 75 sec) after the beginning of the arterial
phase acquisition.5 Our CTE protocol is performed after
administration of 125 cc of Isovue-370 (Bracco Diagnostics Inc,
Princeton, NJ) at an injection rate of 4 cc/sec followed by a 50 cc
saline flush injected at a rate of 4 cc/sec. The scan is then acquired
65 sec from the start of the injection. For arterial phase imaging in
dual-phase scanning, the scan is triggered by a bolus-automated
technique starting 3 sec after a threshold density of 150 HU is reached
in the abdominal aorta.
Oral contrast
The routine
use of positive enteric contrast (barium- or iodine-based), with its
high attenuation, can mask visualization of the mucosal enhancement
pattern and also may limit scan sensitivity to hyper-attenuating
intraluminal or bowel wall lesions. It also may interfere with
volumetric reconstruction for assessing enhancing structures, especially
vessels. The introduction of negative (low HU or neutral) enteric
contrast accomplished 2 important tasks. The first was to optimize bowel
distention, which helps eliminate apparent bowel wall thickening, and
the second was to improve assessment of mucosal hyperattenuation. Both
of these can create false-positive results in interpretation (Figure
3).
Historically, water has been used to distend the bowel;
however, the use of water is limited in the distention of distal small
bowel, as most of it will be absorbed by the time it reaches the ileum.
Newer agents include an array of low-attenuation materials, such as
Mucofalk, mannitol, methylcellulose solution, polyethylene glycol
electrolyte solution, or low-concentration barium.6-8 We use
VoLumen (Bracco Diagnostics Inc, Princeton, NJ) in our department as a
neutral oral contrast agent that consists of barium sulphate suspension
(0.1% w/v, 0.1% w/w). The oral contrast is taken over the course of 1 hr
before the examination with a total approximate amount given of about
1800 ml split into 450 ml administered at 1 hr, 450 ml at 40 min, 225 ml
at
20 min and another 225 ml immediately
before the scan. Some patients, especially those with obstructive
symptoms, may not be able to consume the total dose of contrast; water
can be substituted for the last dose(s), since absorption is not an
issue in distending the stomach or duodenum.
Small bowel and mesentery evaluation
The
small bowel can be affected by a wide variety of disorders, including
inflammation, infection, ischemia, and malignancy. CTE is used most
commonly in the evaluation of patients with suspected inflammatory
diseases.9-12 Inflammatory bowel diseases (IBD) encompass
Crohn’s disease (CD), intermediate colitis, and ulcerative colitis (UC).
Crohn’s disease is a transmural inflammatory disease that involves the
small bowel, most commonly the terminal ileum, with or without upper
gastro-duodenal or colonic involvement. The terminal ileum can, however,
sometimes be involved with intermediate colitis and ulcerative colitis
in the form of back-wash ileitis, which is usually contiguous with large
bowel disease. Characteristically, Crohn’s disease demonstrates
multiple skip areas of involvement with intervening unaffected segments
in the more proximal small bowel, including the duodenum and stomach as
well as the colon. This is in contrast to the two other forms of IBD
that usually affect the colon in a contiguous fashion, starting distally
at the level of the colon.
The clinical workup of patients with
Crohn’s disease usually involves optical upper and lower endoscopy;
however, most of the small bowel between the duodenum and terminal ileum
is inaccessible with these techniques, limiting evaluation and missing
important areas of potential involvement. Another endoscopic “blind
spot” lies in evaluating extra-intestinal complications of IBD. A more
recently available clinical modality for evaluating the small bowel is
capsule endoscopy, which can image the entire small bowel mucosa.
However, this is also limited in visualizing extra-intestinal disease
and can potentially be complicated by retention of the capsule in a
localized high-grade stricture at sites of disease. This can lead to
obstruction that may require surgical intervention (Figure 4).
Historically,
patients with Crohn’s disease have had radiologic work-ups with small
bowel follow-up examinations (SBFT) that could provide details of
mucosal edema and assess the presence of strictures and fistulas/sinus
tract. However, these exams were limited in their ability to evaluate
the extra-enteric complications of IBD, especially abscess formation.
They
also typically require up to several hours to perform, especially in
patients with obstruction, in addition to the difficulty in separating
overlapping bowels that may limit evaluation. CTE evaluation, on the
other hand, provides several advantages over SBFT, including: more rapid
acquisition, requiring only a few seconds to obtain the diagnostic scan
(after the oral prep); assessment of the majority of the GI system in
the same setting (stomach, duodenum, small and large bowel); assessment
of the location, extent, and number of diseased segments; detecting the
presence or absence of bowel obstruction; more accurate assessment of
disease activity by assessing the presence or absence of intrinsic
mucosal and transmural inflammatory bowel changes; and detecting
extra-intestinal complications.
The common signs of active
Crohn’s disease include: increased mucosal enhancement, bowel wall
thickening, mural stratification, stranding of the surrounding fat and
engorgement of the mesenteric vessels supplying the diseased bowel
segment (Figures 5-7).6 However, CTE has poor sensitivity for
assessing fibrotic strictures due to the inability of CT to
characterize fibrosis or collagen deposition, and presence of fibrosis
is usually presumed if the typical inflammatory changes are absent. CTE
can assess for the presence of penetrating disease, detecting sinus or
fistula tracts extending from the diseased segment that are commonly
characterized by bowel tethering and visualization of linear tracts that
may communicate with adjacent structures, such as bowel or
extraperitoneal spaces (most commonly entero-enteric, entero-colic,
enterocutaneous) (Figures 8 and 9).
Another sign of penetrating
disease is abscess formation that is usually contiguous to the diseased
segment and can be seen in the peritoneal cavity or retroperitoneal
space (Figure 10). One important potential pitfall in the use of neutral
oral contrast is the detection of small mesenteric fluid collections
that appear similar in density to adjacent bowel loops (Figure 11). This
problem can be overcome by carefully following the bowel lumen and
separating the intraluminal fluid from the extraluminal fluid, as well
as by performing multiplanar projection for better display of the bowels
in the coronal or sagittal plane. When patients with Crohn’s disease
present with signs of acute flare or obstruction, the main advantage of
CTE is to assess the underlying cause, which would determine clinical
management.13
After detecting small bowel strictures
it becomes imperative to differentiate inflammatory strictures showing
signs of active inflammation that are managed mostly medically from
fibrostenosing strictures that are predominantly fibrotic and that may
require surgical intervention (Figure12). Frequently, CTE is also used
in the postoperative evaluation of Crohn’s disease patients with
symptoms suggesting recurrent disease; most frequently seen at or
immediately proximal to the anastomotic site (Figure13). Not uncommonly,
very low attenuation can be noted within the bowel wall in patients
with a history of longstanding IBD (both CD and UC) due to fat
deposition within the submucosal layer of the bowel (Figure 14).14
The presence of fat is not necessarily indicative of quiescent disease;
fat may be present with signs of active inflammation. An additional
potential CTE indication is its use as a baseline examination before
starting a new treatment—especially one with biologic agents, which
commonly cause immunosuppression—to exclude abscess formation, or as a
follow-up tool to assess treatment response.15 CTE can also
help to evaluate vascular patency in patients with IBD or other
suspected infectious or inflammatory bowel conditions
(Figure 15).
An additional potential clinical indication for CTE
is the assessment of small bowel tumors, mesenteric vessels or vascular
lesions. These examinations can be optimized by using biphasic arterial
and enteric or venous phase scans that improve both detection and
characterization of suspected abnormalities. Commonly encountered small
bowel malignancies include primary lesions, such as carcinoid tumors
(Figure16), primary adenocarcinoma, and GI tumors, as well as metastatic
lesions from a variety of primary tumors that include other GI
malignancies, melanoma, and breast and lung carcinomas. A variety of
incidental findings can be detected on CTE that may be related to the
bowels or within the abdomen and pelvis (Figures17-19). Multiphase CT
can also be used to evaluate for active GI bleeding, which is diagnosed
when high-attenuation, extravasated contrast material is seen
accumulating, and later diffusing, within the bowel lumen (Figure 20).
Common causes of upper GI bleeding include erosions or ulcers, variceal
bleeding, Mallory-Weiss tears, vascular lesions, and neoplasms.16
Conclusion
Recent
advances in CT, most importantly multidetector CT technology and
neutral oral contrast, are leading to a shift toward cross-sectional
imaging and away from fluoroscopic examination in evaluation of patients
with suspected small bowel or mesenteric disorders.
The most
common current indication for single-phase CTE is evaluation of patients
with inflammatory bowel disease, especially Crohn’s disease, in which
the modality has shown several advantages over other modalities, such as
endosocpy or SBFT. Careful consideration of patients for repeated
imaging or multiphase scanning is essential due to concern about
lifetime cumulative radiation dose.
References
- Huprich JE, Fletcher JG. CT enterography: Principles, technique and utility in Crohn’s disease. Eur J Radiol. 2009;69:393-397.
- Fletcher JG. CT enterography technique: Theme and variations. Abdom Imaging. 2009;34:283-288.
- Huprich JE, Fletcher JG, Alexander JA, et al. Obscure
gastrointestinal bleeding: Evaluation with 64-section multiphase CT
enterography—initial experience. Radiology. 2008;246:562-571.
- Scheffel H, Pfammatter T, Wildi S, et al. Acute gastrointestinal
bleeding: Detection of source and etiology with multidetector-row CT. Eur Radiol. 2007;17:1555-1565.
- Graça BM, Freire PA, Brito JB et al. Gastroenterologic and
radiologic approach to obscure gastrointestinal bleeding: How, why, and
when? Radiographics. 2010;30:235-252.
- Paulsen SR, Huprich JE, Fletcher JG, et al. CT enterography as a
diagnostic tool in evaluating small bowel disorders: Review of clinical
experience with over 700 cases. Radiographics. 2006;26:641-57.
- Reittner P, Goritschnig T, Petritsch W, et al. Multiplanar spiral CT
enterography in patients with Crohn’s disease using a negative oral
contrast material: Initial results of a noninvasive imaging approach. Eur Radiol. 2002;12:2253-2257.
- Zhang LH, Zhang SZ, Hu HJ, et al. Multi-detector CT enterography
with iso-osmotic mannitol as oral contrast for detecting small bowel
disease. World J Gastroenterol. 2005;11:
2324-2329.
- Solem CA, Loftus EV Jr., Fletcher JG, et.
al. Small-bowel imaging in Crohn’s disease: A prospective, blinded, 4-way comparison trial. Gastrointest Endosc. 2008;68:255-266.
- Vogel J, da Luz Moreira A, Baker M, et al. CT enterography for Crohn’s disease: Accurate preoperative diagnostic imaging. Dis Colon Rectum. 2007;50:1761-1769.
- Hara AK, Swartz PG. CT enterography of Crohn’s disease. Abdom Imaging. 2009;34:289-295.
- Lee SS, Kim AY, Yang SK, et al. Crohn disease of the small bowel:
Comparison of CT enterography, MR enterography, and small-bowel
follow-through as diagnostic techniques. Radiology. 2009;251:751-761.
- Higgins PD, Caoili E, Zimmermann M, et al. Computed tomographic
enterography adds information to clinical management in small bowel
Crohn’s disease. Inflamm Bowel Dis. 2007;13:262-268.
- Wittenberg J, Harisinghani MG, Jhaveri K, et al. Algorithmic approach to CT diagnosis of the abnormal bowel wall. Radiographics. 2002;22:1093-1107.
- Hara AK, Alam S, Heigh RI, et al. Using CT enterography to monitor Crohn’s disease activity: A preliminary study. Am J Roentgenol. 2008;190:1512-1516.
- Laing CJ, Tobias T, Rosenblum DI, et al. Acute gastrointestinal
bleeding: Emerging role of multidetector CT angiography and review of
current imaging techniques. Radiographics. 2007;27:1055-1070.