Dr. Fletcher is a Professor of Radiology, Dr. Fidler is an Associate Professor of Radiology, Dr. Huprich is an Associate Professor of Radiology, Mr. Llano is a Research Fellow, Mr. Spencer is a Research Fellow, Department of Radiology, and Dr. Bruining is an Assistant Professor of Medicine, Division of Gastroenterology and Hepatology, at the Mayo Clinic, Rochester, MN.
advances in computed tomography (CT) and magnetic resonance (MR)
technology permit excellent visualization of the small-bowel wall and
lumen with enteric contrast when the organ is appropriately distended.1,2 These techniques can accurately detect small-bowel inflammation,3-6 tumors,7,8 and even vascular lesions.8,9
These imaging advances directly impact patient care and are changing
diagnostic approaches to patients with inflammatory bowel disease and
Overview of techniques: Acquisition and indication
variations exist for CT and MR imaging of the small bowel. Table 1
summarizes the clinical indications for different types of dedicated
small-bowel imaging exams with CT or MR. Table 2 summarizes the most
salient features of image acquisition for each of these imaging
is a global exam to assess for suspected small-bowel disease.
Predominant indications include Crohn’s disease (diagnosis and staging),
abdominal pain, diarrhea, diffuse small-bowel diseases, and low-grade
obstruction. It is performed with large volumes of neutral enteric
contrast, along with iodinated intravenous contrast, to maximize the
visualization of enhancing small-bowel wall and inflammation.
Multiplanar images are reconstructed with high spatial resolution (slice
thickness ≤3 mm) in multiple planes. While water can be used for
enteric contrast, agents that prohibit resorption of water along the
small-bowel lumen,such as polyethylene glycol and low-contrast barium
solution (Volumen), are preferred, as they improve small-bowel
distention and lengthen the period in which optimal imaging is possible.12 Our
institution typically gives patients 3 bottles (1350 cc) of
low-contrast barium solution (Volumen) over 30 to 60 min prior to a CT
or MR enterography examination, with an additional 500 cc of water 15 min
prior to imaging. Because of the large volume of ingested enteric
contrast, radiologists and clinicians should recognize that other
imaging alternatives should be contemplated for hospitalized patients.
Contrast-enhanced CT is typically performed 50 sec after the injection
of enteric contrast during the enteric phase, when peak small-bowel
enhancement is achieved.13 However, it should be recognized
that imaging in the portal phase of enhancement is also acceptable and
does not decrease the performance of the exam in identifying active
Crohn’s disease (Figure 1).14 Ideally, minimal detector
configurations of < 1 mm are selected to obtain crisp coronal images
that maximize z-axis spatial resolution. Radiologic technologists should
be taught that CT enterography exams must obtain images through the
entire perineum in order to detect perianal fistulizing disease, which
is the sole finding of active disease in some patients. CT enterography
exams should be performed with CTDIvol less than routine
abdominal CT, despite the decreased slice thickness, which is possible
because of the high contrast of the small-bowel wall and Crohn’s-related
enteric inflammation. Automatic exposure control should be utilized to
minimize and individualize radiation dose. Recent studies have shown
that automatic exposure control can be used to substantially decrease
radiation dose at CT enterography, while maintaining diagnostic
performance (Figure 1).15-17 Lower tube voltages can be used
to increase iodine signal to compensate for suboptimal intravenous
contrast or to reduce radiation dose (Figure 2).
Because segmental mural hyperenhancement is associated with histologic inflammation,4
CT enterography can be used to detect small-bowel, Crohn’s-related
inflammation. CT enterography has a sensitivity of approximately 80% to
90% for detecting active small-bowel inflammation from Crohn’s disease,
when CT enterography is performed as described above and using
ileocolonoscopy with biopsy as a reference standard.3-5, 18-22 However,
a recent comparison of CT and MR enterography demonstrated that active
small-bowel inflammation can be present when a normal-appearing ileal
mucosa is identified at ileocolonoscopy.6 The potential
systematic error in using ileocolonoscopy alone as a reference standard
for detecting small-bowel Crohn’s disease likely results in an 8% to 9%
underestimate of sensitivity in theafore mentioned studies.23 Radiologists should use a combination of mural thickness and hyperenhancement when identifying active small-bowel inflammation.3, 23 Similar findings can be used to identify colonic inflammation.24
enterography can be performed with standard 1.5 tesla (T) magnets
employing an 8-channel phased array coil to image the abdomen and
pelvis. The timing of enteric contrast ingestion is similar to CT
enterography. Precontrast images generally consist of axial and coronal
single-shot, fast-spin echo, and TrueFISP imaging. Single-shot,
fast-spin echo images permit clear depiction of the gut wall and have
few artifacts other than flow voids within the intestinal lumen from
peristalsis. TrueFISP imaging also clearly depicts the small-bowel wall
and is particularly useful for examining the small-bowel mesentery. We
employ a double-dose of gadolinium contrast for MR enterography, with
the 3D VIBE sequences being started at 45 sec after the beginning of
gadolinium injection. Dynamic coronal images are acquired in 3
sequential volumes,with 10 sec between scans to allow for breath
holding. Postcontrast VIBE and 2D SPGR images with saturation are also
obtained. 0.5 mg ofGlucagon is given subcutaneously at the beginning of
the MR examination and another 0.5 mg is given intravenously immediately
prior to gadolinium enhancement to alleviate motion artifact from bowel
For the detection of Crohn’s disease, several
prospective small studies and a large review have shown that the
sensitivity of MR enterography is similar to CT enterography.6, 25-27
Triple-phase CT enterography
CT enterography is performed similarly to single-phase CT enterography,
except that multiple acquisitions are obtained. Arterial-phase imaging
is performed to demonstrate angiodysplasias and arterial venous
shunting, with enteric-phase images acquired to display a majority of
small-bowel tumors and inflammation, with delayed-phase images
increasing diagnostic confidence and potentially demonstrating active
bleeding. Axial and coronal images are reconstructed at 2-mm slice width
and 1-mm reconstruction interval with coronal maximum intensity
projection (MIP) images often being used to highlight enhancing
pathology on coronal reconstruction.28 Radiation dose can be
minimized with automatic exposure control and kV selection, but most
importantly, with appropriate patient selection.11
CT enterography is reserved for patients with obscure GI bleeding and
in whom a suspected bleeding source is not found after initial primary
upper and lower endoscopy. It is a complementary test to capsule
endoscopy.8, 11 We recently performed a prospective study in
58 adult patients with obscure GI bleeding, with all patients undergoing
capsule endoscopy and multiphase CT enterography within one month. 29 Multiphase
CT enterography and capsule endoscopy exams were positive in 14 of 16
and 6 of 16 patients, respectively,yielding sensitivities of 88% vs 38%,
with multiphase CT enterography being significantly more sensitive.
This improved sensitivity was predominantly due to the improved
identification of small-bowel tumors with 6 of 9 being missed by capsule
endoscopy, but not multiphaseCT enterography (Figure 3).
enteroclysis provides superior bowel distention compared to
enterography at the expense of decreased patient acceptance. Therefore,
at our institution, enteroclysis is reserved for those cases with
negative conventional imaging or enterography and the need for excellent
small-bowel distention to detect subtle abnormalities. MR enteroclysis
is performed for suspected low-grade small-bowel obstruction when
routine imaging fails to demonstrate a partial small-bowel obstruction
(Figure 4). Following fluoroscopic placement of a nasojejunal tube,
precontrast monitoring scans are performed during the rapid infusion of
bi-phasic, enteric contrast agents (typically between 80 cc/min and 120
cc/min, depending upon patient symptoms). Precontrast radiologist
monitoring is required to assess for distention of the small bowel and
stomach. Once distention of the terminal ileum is achieved or when
patient symptoms develop or when a persistent transition zone is
identified, high-resolution axial and coronal images are acquired before
and after intravenous contrast administration.Multiphase imaging can be
helpful over suspected points of obstruction to demonstrate a typical
to-and-fro peristalsis seen at fluoroscopy proximal to points of
MR enteroclysis is predominantly used at our institution for the diagnosis of low-grade partial small-bowel obstruction.30 It is being increasingly employed to evaluate for suspected small-bowel tumors at other sites.31,32
Some have recently shown that MR enterography without placement of the
nasojejunal tube may also be useful in identifying small-bowel polyps.7
enteroclysis is performed similarly to MR enteroclysis. Positive
enteric contrast is generally utilized for suspected small-bowel
neoplasms or partial obstructions. Neutral enteric contrast is generally
employed when differential possibilities, such as radiation enteritis
or Crohn’s disease, are more likely. Low-dose monitoring scans are
performed after infusion of every 500-1000 cc of enteric contrast, with
rates of infusion being increased or decreased depending upon patient
symptomatology. During such monitoring scans, we increase the rate when
the bowel distention is < 2 cm and decrease the rate of infusion when
bowel diameter is > 3 cm. CT enteroclysis with neutral contrast is
performed at the same dose settings as routine CT enterography. With the
use of positive enteric contrast, high spatial resolution images can be
obtained at lower doses because of the large contrast differences
between the bright, contrast-filled enteric lumen and surrounding soft
tissue of the bowel wall. We typically perform low-dose CT enteroclysis
for patients with polyposis, employing dose settings one-half those of
routine CT enterography and obtaining excellent visualization of the
inflammation is best diagnosed using a combination of segmental mural
hyper-enhancement and small-bowel wall thickening.3,23 Segmental
hyperenhancement without wall thickening is a more sensitive marker of
small-bowel inflammation, but is less specific.Other findings, such as
the Comb sign (engorgement of the vasa recta), fibrofatty proliferation,
and stranding in the perienteric fat also indicate active inflammation.2,33 Asymmetric
and patchy hyperenhancement of the bowel wall is specific for Crohn’s
disease. Fistulas appear as extra-enteric enhancing tracts, which may or
may not contain fluid (Figure 5).34
Obscure GI bleeding (OGIB)
masses and vascular lesions account for the majority of abnormalities
causing OGIB. In most cases, their appearance on multiphase CTE is
characteristic and allows differentiation of masses from vascular
lesions. The appearance of small-bowel neoplasms is discussed below.
most common small-bowel vascular lesions causing OGIB are
angioectasias—endoscopically visible lesions up to several millimeters
in size consisting of dilated capillaries in the lamina propria.35 The
most common appearance on multiphase CTE is a round or plaque-like
focal area of enhancement, brightest on the enteric phase, which fades
slightly during the delayed phase. These lesions are frequently multiple
and commonly occur in patients without signs of OGIB. Therefore,
correlation with endoscopic findings is sometimes problematic (Figure
6).Enhancement characteristics are similar to carcinoid tumors; however,
lesion size and shape will usually allow differentiation. In some
cases, angioectasias may be visible during the arterial phase and can be
accompanied by an early draining vein.
The appearance of small-bowel neoplasms has been described, with each neoplasm having a spectrum of appearances.2 Carcinoid
tumors are typically hyperenhancing luminal polyps and masses, with
characteristic mesenteric metastases (when present). GIST tumors
frequently have an exoenteric component. Small-bowel lymphoma often is
polypoid and may be associated with lumen dilatation with nearby
lymphadenopathy, often affecting multiple points along the GI tract.
Small-bowel polyps can originate from a variety of histologies and
enhance variably, and can appear indistinguishable from other
small-bowel filling defects, such as ectopic pancreas.
CT vs. MRI vs. other small-bowel exams
CT and MR enterography perform similarly in identifying active Crohn’s
disease and its complications, a number of variables should beconsidered
when selecting the most appropriate test for any patient. Because of
the improved temporal and spatial resolution of CT, we generally select
CT enterography as a desired examination when there is a concern for
sepsis. CT enterography is generally the first examination performed for
suspected Crohn’s disease in adult patients, while MR enterography may
be the first exam performed in younger patients. We prefer MR
enterography when there is the question of low-grade obstruction or when
the clinician desires to assess response to immunomodulator therapy in
the absence of patient symptomatology.36 CT is, of course,
performed in patients with implantable devices or claustrophobia. MR is a
feasible alternative in patients with contraindications to CT, such as
renal impairment, contrast allergy, or pregnancy.
Much has been
made in the popular press regarding the radiation risks of CT; however,
it should be remembered that the risks of radiation forCT examination
are too low to be accurately estimated.37,38 CT enterography
can detect known causes of morbidity and mortality in Crohn’s disease
patients and change management decisions in approximately 50%, often
because protean symptoms are usually unrelated to biologic activity.
Furthermore, immunomodulator drugs are very expensive and have
significant risk,39 but the benefits of these drugs outweigh the risks.40 Finally,
CT enterography has been selected and judged by a panel of experts to
be the most appropriate imaging test in patients with suspected Crohn’s
disease.41 We generally perform MR enterography in younger patients and as a follow-up examination in asymptomatic adult patients.
urgency for enterography examination, as well as its costs and local
expertise, also affect these imaging decisions. CT is readily available
in most practices, but due to the growing use of MR in small-bowel
assessment, radiology practices should be encouraged to expand their MR
enterography access. At our institution CT enterography costs about
one-third that of MR enterography.
Small-bowel follow-through and
capsule endoscopy are also important small-bowel diagnostic tests that
may be more appropriate than cross-sectional enterography, depending on
the clinical situation. We often perform small-bowel follow through in
complex post-surgical cases, or suspected pseudo-obstruction,
scleroderma, or small-bowel diverticulosis. Capsule endoscopy is a
complementary test to multiphase CT enterography in patients with
obscure GI bleeding, owing to its exquisite mucosal assessment. It is
also useful in identifying erosions and other signs of mild Crohn’s
disease after a negative CT or MR enterography, when clinical symptoms
persist. Performing cross-sectional enterography prior to capsule
endoscopy decreases the risk of capsule retention.19,20
Impact on patient care
and MR enterography are dramatically altering Crohn’s disease
diagnostic and management algorithms. At our institution, 273 patients
with suspected or established Crohn’s disease recently underwent a
prospective study, in which referring gastroenterologists completed a
pre-CT enterography questionnaire regarding their postmanagement plans.42 After
reviewing imaging results, clinicians reported that CT enterography
altered their management plans in 51% (54% of these were those with
suspected Crohn’s disease and 48% with established Crohn’s disease).
Similar findings were noted by Higgins et al, where CTE data changed the
perception for the likelihood of steroid benefit in 41 of 67 Crohn’s
disease cases.43 These results likely reflect the uncertainty
that exists, as symptoms and clinical indices, such as the Crohn’s
Disease Activity Index (CDAI), have a poor correlation with endoscopic
disease activity.44, 45 Cross-sectional imaging can provide
objective measures of disease activity while also detecting occult
penetrating disease and extra-luminal disease manifestations.46 In addition, intestinal response to therapy (remodeling) can be followed on CTE or MRE,47
suggesting the possibility of using imaging indices or end-points to
tailor therapy. CT and MR enterography are becoming vital components of
global disease activity and intestinal damage assessments.
Obscure GI bleeding
endoscopy has been widely accepted as the diagnostic tool of choice for
the evaluation ofOGIB. However our experience, along with others,
suggests a significant false-negative rate for the diagnosis of
small-bowel tumors.48 Multiphase CTE has proven to be
sensitive in the detection of small-bowel masses. We believe the
addition of multiphase CTE to the routine diagnostic work-up of patients
with obscure GI bleeding is warranted, particularly in patients with a
prior negative capsule endoscopy.
patients with polyposis syndromes develop small-bowel polyps at an
early age, and patients are at risk for developing complications, such
as bleeding, intussusceptions, and gastrointestinal and extraluminal
malignancies. Therefore, routine surveillance of these patients is
usually performed. Endoscopy is performed to detect and treat gastric,
duodenal, proximal jejunal, and colonic polyps. Several techniques are
available to detect small-bowel polyps, including wireless capsule
endoscopy, cross-sectional enterography/enteroclysis, and
balloon-assisted endoscopy. Wireless capsule endoscopy and enterography
are well tolerated and can be used to detect larger polyps (1.0-1.5 cm)
that may be more clinically significant and require either
balloon-assisted endoscopic removal or surgery. Studies have shown that
while wireless capsule endoscopy may detect smaller polyps than MR
enterography, there is no significant difference in detection of larger,
more clinically significant polyps. MR enterography more accurately
localizes these polyps, is more reliable in size estimation, and can be
used as a guide for subsequent treatment approaches.7,49 An
additional advantage of cross-sectional imaging is the ability to screen
for extraluminal malignancies that can arise in Peutz-Jeghers syndrome.
Cross-sectional imaging is transforming
the radiologic and clinical assessment of the small bowel and care of
patients with small-bowel diseases. Techniques should be selected based
on clinical suspicion and adapted to individual patients.
- Fidler JL, Guimaraes L, Einstein DM. MR imaging of the small bowel. Radiographics. 2009;29: 1811-1825.
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;26:641-657; discussion 657-662.
ME, Walter J, Obuchowski NA, et al. Mural attenuation in normal small
bowel and active inflammatory Crohn’s disease on CT enterography:
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KD, Fletcher JG, Solem CA, et al. Crohn Disease: Mural attenuation and
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F, Fletcher JG, Huprich JE, et al. Active Crohn disease: CT findings
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