Radiological Evaluation of the Small Bowel
Conventional Radiology
The conventional small bowel follow-through (SBFT) examination that was routinely
practiced has been shown to be inadequate in the evaluation of the small intestine.
A large multi-institutional prospective study showed that the SBFT had inadequate
definition of 35% of the proximal ileum, 32% of the distal ileum, and 24% of the jejunum.[1] It is quite clear that the traditional SBFT examination that involves a patient
drinking barium followed by serial radiographs at regular intervals should be abandoned
as more than a third of the small bowel is not adequately visualized. “The SBFT fails
to apply the same principles of diagnostic care that are the rule in virtually all
other areas of radiology”—for example, does a radiologist still perform a skull radiograph
for suspected stroke?
Nevertheless, barium studies still hold a limited place in the radiologist's arsenal.
If performed, they should be done together with fluoroscopic evaluation, where segments
of the bowel are observed during peristalsis and manual compression. Some added modifications
such as pneumocolon should be used to visualize the ileocaecal junction. Barium examinations
are useful in the evaluation of intestinal infections as they can show irregularities
of fold patterns and more importantly peristaltic abnormalities that are not readily
appreciated on other imaging modalities.
The most accurate conventional radiologic method in the diagnosis of small-bowel obstruction,
inflammatory bowel disease (IBD), gastrointestinal bleeding, and small intestinal
neoplasms is the double-contrast enteroclysis (DCE).[2] The advantages of DCE over SBFT are greater and more consistent distension of the
bowel may highlight strictures or small lesions. Subtle mucosal disease may also be
better appreciated on DCE examinations ([Fig. 1]). The major disadvantages of enteroclysis are patient discomfort and higher radiation
dosages. However, studies have shown that the technique of DCE especially with air-contrast
technique provides similar diagnostic accuracy to capsule endoscopy. The technique
of enteroclysis is also used in computed tomography (CT) and magnetic resonance imaging
(MRI) examinations of the small intestine.
Fig. 1 Double-contrast enteroclysis (DCE) in a 36-year-old male patient with chronic diarrhea
shows fine detail of the intestinal mucosa with aphthous ulcers, enlarged follicular
nodules, and small, shallow ulcers in early Crohn's disease. These early changes may
not be appreciated on routine computed tomography (CT) or magnetic resonance imaging
(MRI) examinations.
In recent times, newer modalities have emerged for investigation of intestinal disorders
and diseases. Innovations in intestinal imaging have been driven by the demand for
detailed clinical information, better diagnoses, and higher accuracy rates.
CT and MR Imaging of the Small Bowel
The small intestine can be imaged using the technique of enteroclysis combined with
CT or MRI (CT enteroclysis and MR enteroclysis, respectively). Another technique for
imaging the intestine is the enterography procedure (CT enterography [CTE] or MR enterography
[MRE]).
A major advantage of CT- or MR-based examinations over traditional barium examinations
are that they allow assessment of the bowel lumen, bowel wall, surrounding mesentery,
and other abdominal organs. The major advantages of MR imaging over CT are its inherent
tissue contrast resolution and absence of ionizing radiation. Real-time imaging for
peristaltic activity and dynamic contrast studies are therefore possible with MRE
without the risk of increased radiation burden. The major disadvantage of CT is its
exposure to ionizing radiation which makes it unsuitable for pediatric population.
(Please add here the advantages of CT over MRI). CT may be useful in the acute setting
or the unwell patient who may not tolerate the longer MR examination. Better anatomical
detail may also be achieved on CT due to its greater spatial resolution.
The fundamental principle behind obtaining diagnostic small intestinal images is good
distension of the bowel lumen. Collapsed segments can even hide larger lesions and
may appear falsely thickened or abnormally enhanced. Distension of the small intestine
can be achieved via the enteroclysis of enterographic techniques. Although the enteroclysis
technique can provide consistent and optimal distension, the procedure is technically
challenging and discomfiting for patients. Furthermore, radiation is still involved
during placement of the nasojejunal catheter. Small prospective studies have shown
no difference in the diagnostic capabilities of MR enteroclysis and MRE studies. The
enteroclysis technique is also more costly as it involves the use of the MR and fluoroscopy
suites, time, staff, and nursing support.
Therefore, for practical purposes, the authors’ choice for imaging the bowel is either
CTE or MRE. The use of CT or MR enteroclysis is reserved for patients in whom the
enterographic procedure has been suboptimal despite a high clinical index of suspicion.
Enteroclysis may also be used in patients suspected of having partial strictures that
may not be highlighted with enterography examinations. Invasive procedures like enteroclysis
should ideally be used in selected problem-solving cases rather than a first-line
test.
Patient Preparation for Enterography
Distention of the small intestine depends on patient compliance, volume of contrast
ingested, and the timing of imaging. The intake of sufficient volumes of contrast
medium combined with optimal timing of image acquisition is paramount for achieving
good quality diagnostic images on CTE or MRE.
Currently, no consensus exists for volume of contrast required. In a study by Kuehle
et al, it was observed that good distension of the bowel was achieved with 1,350 mL
of contrast and that no additional benefit was achieved by increasing the contrast
volume to 1,800 mL.[3] A study by Lohan et al reported that oral contrast reached the terminal ileum at
a mean time of 55 minutes.[4] The optimal time for imaging the entire small bowel has been reported to range between
50 and 60 minutes.[4]
[5]
[6] Although there is no consensus on amount of contrast, experts agree that water should
not be used as an enterographic agent. Several studies have reported water to be inadequate
for distending the distal small bowel after oral intake[5]
[7] Water may only be used during the enteroclysis procedure where the instillation
of contrast is under the operator's direct control through the nasojejunal tube. Oral
agents for CTE include methylcellulose, lactulose, mannitol, solutions containing
locust-bean gum, or polyethylene glycol.[7]
[8]
[9] Enteral agents work by retarding the resorption of water in the intestine and promoting
luminal distention. A neutral density contrast should be preferred as high-density
agents may mask mucosal abnormalities and mucosal enhancement ([Fig. 2]). Positive density contrast may be used in specific instances when filling defects
or bands are suspected (such as polyps or nonsteroidal anti-inflammatory drug-related
webs), as the dense contrast tends to highlight luminal abnormalities. However, for
most practical purposes, neutral-density contrast is ideal for CTE examinations.
Fig. 2 Computed tomography enterography (CTE) examinations in a 44-year-old female patient.
(A) Note positive enteral contrast obscures the mucosal enhancement (arrow). (B) CTE examination with neural-density contrast. The mucosal enhancement is clearly
visible (arrow). (C) CTE examination with positive contrast in a 39-year-old patient with Whipple's disease.
Note dense contrast highlights the thickened, nodular valvulae conniventes.
On MRE, contrast agents may be positive, that is, they produce increased signal intensity
within the bowel lumen (gadolinium chelates), whereas negative agents cause a signal
drop out (superparamagnetic particles).[10] Biphasic agents (e.g., polyethylene glycol, mannitol solution) behave as positive
or negative agents depending on the imaging sequence applied. At the authors’ institution,
a solution of 3% mannitol in 1,200 mL is used for CTE or MRE examinations.
It has been reported that a divided oral dose promotes a more uniform distension of
the intestine. At our institution, the oral contrast material is divided in two aliquots
of 600 mL each, and the patient drinks one aliquot every 25 to 30 minutes. An oral
suspension of 10 mg of metoclopramide is given with the first aliquot to promote gastric
emptying. Continuous, steady ingestion of the oral contrast material over the allocated
time promotes uniform and consistent filling of the proximal and distal small bowel[11] ([Fig. 3]). The most important factor for promoting intestinal transit is a full stomach.[12] Therefore, the addition of a second dose of oral contrast distends the stomach,
promoting peristalsis and filling of the intestine. Just prior to acquiring images,
patients are asked to drink another 200 mL of contrast material to outline the stomach
and duodenum.
Fig. 3 True-fast imaging with steady-state free precession (FISP) coronal image from magnetic
resonance enterography (MRE) examination in a 41-year-old male patient shows optimal
distension of the small intestine up to the ileocaecal junction.
CT and MR Imaging Sequences
CTE imaging is performed with injection of iodinated contrast (~1–1.5 mg/kg) at a
rate of 4 mL/s with a delay of 50 seconds. Images are acquired from the diaphragm
to the symphysis pubis ([Fig. 2]). An intravenous injection of 20 mg of hyoscine-N-butylbromide (Buscopan) or 1 mg
of glucagon is administered as an antiperistaltic agent.
MRE is performed using ultra-fast sequences based on steady-state precession such
as true-fast imaging with steady-state with free precession (true-FISP), balanced
fast field echo, steady-state free precession, or fast imaging employing steady-state
precession. These sequences need short, single breath-holds and are relatively insensitive
to movement artifacts. These sequences provide high contrast between the bowel wall,
lumen, and the mesentery. A disadvantage of these sequences is a black boundary artifact
along the bowel wall which is often seen and can be minimized with fat suppression
([Figs. 4]
[5]).
Fig. 4 Magnetic resonance enterography (MRE) examinations in a 36-year-old female patient.
(A) Coronal true-fast imaging with steady-state free precession (FISP) image shows black-boundary
artifact adjacent to the bowel wall (arrows). This artifact can obscure early mural
changes. (B) Coronal true-FISP image in a 46-year-old male patient with fat suppression removes
the artifact and early sinuses and fistulae from the inflamed transverse colon are
easily appreciated (arrow).
Fig. 5 True-fast imaging with steady-state free precession (FISP) axial image from magnetic
resonance enterography (MRE) examination in a 21-year-old male patient shows marked
mural thickening, ulcers, and inflammation of the bowel in Crohn's disease (arrow).
MR images are also acquired using T2-weighted fast sequences such as half-Fourier
acquisition single-shot turbo spin-echo (HASTE) or single shot fast spin echo. These
sequences produce high contrast between the lumen and the bowel wall and are relatively
insensitive to the black boundary artifact. Thin-section, high-resolution images using
a combination of true FISP and HASTE sequences with fat suppression and small field
of view may also be acquired parallel and perpendicular to the affected segments to
maximize visualization of mucosal and mural abnormalities ([Figs. 5]
[6]
[7]).
Fig. 6 High-resolution true-fast imaging with steady-state free precession (FISP) coronal
image from magnetic resonance enterography (MRE) examination in a 31-year-old female
patient shows marked nodular thickening of mucosal folds with target-type aphthous
ulcers in Crohn's disease (arrows).
Fig. 7 Color-coded enhancement signal on magnetic resonance enterography (MRE) in a 22-year-old
female patient shows hyperemia/perfusion in the descending colon with enlarged branches
of the inferior mesenteric arcade (arrow). The lumen is narrowed due to an inflammatory
stricture.
Postintravenous contrast images are acquired on T1-weighted sequences either in two
or three dimensions. These sequences are commonly known as two-dimensional and three-dimensional
(3D) fast low angle shot or volumetric sequences such as volumetric interpolated breath-hold
examination. Fat saturation should be used to increase contrast resolution and also
allows better assessment of bowel enhancement.[5] Changes in bowel peristalsis can be evaluated on MRI fluoroscopy to demonstrate
either an obstructive fibrotic or inflammatory stricture.[13]
Diffusion-Weighted MR Imaging
Diffusion-weighted (DW) MRI signal is derived from the motion of water molecules within
cells or extracellular spaces. The use of high b values (b = 1,000 second/mm2) is recommended in DW MRI of the intestines to negate the high signal intensity of
normal bowel mucosa and shine through effect from luminal contrast.[14] Intestinal tumors or inflammation have restricted water diffusion and show up as
areas retaining high signal intensity on high b values.
The advantages of DW MR imaging are its noninvasive nature and no need for intravenous
contrast injection. As DW MR imaging can be integrated with standard MRE imaging,
this does not require any additional equipment. DW MR imaging uses the diffusion of
water to produce images. It therefore provides functional, quantitative information
at the cellular level that provides accurate assessment of intestinal inflammation,
tumors, and also response to therapy ([Fig. 8]).
Fig. 8 Diffusion-weighted magnetic resonance imaging (MRI) in a 46-year-old male patient
with colitis shows marked inflammation of the descending colon as area of transmural
high signal (arrow).
Perfusion Imaging
Perfusion CT is a technique that combines anatomy with assessment of vascular physiology.
Analyses of tumor enhancement, tumor blood flow, blood volume, mean transit time,
and permeability surface area product are evaluated. Perfusion CT demonstrates angiogenesis
in tumors and is used in the assessment of colorectal tumors and their response to
treatment.[15]
Bowel Length Measurement
Recent reports have described using MR imaging to measure intestinal length.[16] Accurate measurements are important in surgical management for patients where repeated
resections are required, such as in patients with Crohn's disease. Short intestinal
length may lead to intestinal failure and extensive distal ileal resections lead to
vitamin B12 deficiency and bile salt loss. There have been reports describing the
use of software for small intestinal measurements. This is done using segmentation
of MRE images using 3D directional gradient vector flow snakes with centerline extraction
([Fig. 9]).[17]
Fig. 9 Snapshot of a bowel length measurement with a vector snake (arrow). The length of
bowel interrogated (arrowheads) is displayed prior to surgical planning.
In conclusion, currently MRE has become the preferred technique for imaging of the
small intestine. It is used in the diagnosis and follow-up of IBDs.[18]
[19] MRE may also be used in pediatric population to avoid exposure to radiation. CTE
may be used in patients who may not tolerate MRI examinations. Furthermore, CT imaging
combined with enteroclysis is the most accurate diagnostic modality in the detection
of partial strictures, adhesions, and tumors of the small bowel. New refinements such
as perfusion imaging, bowel length measurement, and motility studies will further
enhance the role of CR and MR imaging of the small intestine in the future.[20] In current practice, MR- or CT-based imaging should be the preferred choice for
intestinal imaging rather than barium examinations.
