Dr. Huprich is an Associate Professor of Radiology, Dr. Fletcher is a Professor of Radiology, Dr. Fidler is an Associate Professor of Radiology, and Mr. Llano is a Research Fellow, Department of Radiology, Mayo Clinic, Rochester, MN.
Huprich and Dr. Fidler reported receiving research support from Bracco
Diagnostics and Dr. Fletcher reported receiving research support from
Obscure GI bleeding (OGIB), defined as
persistent or recurrent GI bleeding despite negative initial upper
endoscopy and colonoscopy, is one of the most challenging problems
facing the practicing clinician.1 In most cases the presumed
cause for the blood loss is a small bowel abnormality. Until recently,
results from conventional imaging techniques designed to detect small
bowel bleeding sources were disappointing. Introduced in 2000, wireless
capsule endoscopy (CE) has rapidly become the preferred technique for
the evaluation of OGIB. CE has a diagnostic yield of 32% to 76%, and a
negative predictive value of 83% to 100%.2 However, CE is not
a perfect test. In one report, complete examination of the small bowel
was achieved in only 74% of patients and trivial findings were seen in
23%.3 Capsule retention requiring endoscopic or surgical retrieval occurs in 1.9% .4
In addition, the procedure is contraindicated in patients with
pacemakers, dysphagia, and suspected small bowel strictures. Because of
the transit time through the GI tract and the huge number of images to
be reviewed, long turnaround times are common. This fact makes it
unsuitable for the evaluation of acute severe OGIB, in which early
diagnosis is important.
Multiple reports of the use of computed tomography (CT) in evaluating GI bleeding have been published.5
Most emphasize the detection of active bleeding. However, as we have
learned from angiographic and nuclear medicine studies, which are
designed to detect brisk active bleeding, bleeding tends to be
intermittent. Therefore, if multiphase CT enterography (MpCTE) is
performed between bleeding episodes, it will be falsely negative.
Furthermore, the majority of CT studies do not emphasize detection of
the etiology of the bleeding. Prompt determination of the bleeding
etiology may be important in directing treatment and predicting a
patient’s prognosis. Patients with small bowel angiodysplasias will
require different treatment and usually have a better prognosis than
those with potentially malignant small bowel neoplasms.
by the success of single-phase CT enterography in the evaluation of
inflammatory bowel disease and the exquisite images it produces,6
we modified the single-phase enterography technique to enhance our
ability to detect lesions responsible for small bowel bleeding and
introduced it in our practice in 2006. Our gastroenterology colleagues
have found this technique very useful and it has become the initial
diagnostic tool in the evaluation of obscure GI bleeding. The purposes
of this paper are to describe the technical aspects of MpCTE, to present
the imaging findings, and to discuss performance estimates in patients
with obscure GI bleeding.
MpCTE technique and interpretation methods
referred for MpCTE should have evidence of persistent or recurrent GI
blood loss (iron deficiency anemia and/or positive fecal occult blood
test with or without hematochezia or melena) and should have undergone
recent negative upper endoscopy and colonoscopy.
Because of the
high spatial and temporal resolution required, these exams should be
performed on a 64- or 128-slice CT system. After a 4-hour fast, patients
are given a total of 1350 cc of 0.1% w/v barium sulfate suspension
(VoLumen®, E-Z-EM, Lake Success, NY) orally, divided into
three 450-cc doses given every 15 minutes, beginning 60 minutes prior to
scanning. An additional 500 cc of water is given orally 15 minutes
before scanning. One hundred fifty cc of Omnipaque 300® (GE
Healthcare, Ltd, distributed by Amersham Health, Princeton, NJ) is power
injected intravenously through an antecubital catheter at a rate of 4
cc/second. Scanning is performed from the diaphragm to the symphysis
pubis during each of 3 phases: (1) a bolus-triggered “arterial phase;”
(2) an “enteric phase” beginning 50 sec after the beginning of
injection; and (3) a “delayed phase,” 90 sec after the beginning of
contrast injection, using a 64-slice or 128-slice CT system. Bolus
triggering is performed by the CT technologist by placing an ROI cursor
over the descending aorta 2 cm above the diaphragm. The ROI trigger
threshold is set at 150 HU at 120 kVp, with scanning initiated 6 seconds
after the threshold CT number is achieved. Patients are scanned at 120
kVp with quality reference effective mAs of 240 mAs. Detector
collimation is set to the minimum slice width. For each phase of
acquisition, axial images are reconstructed using a 2-mm slice width and
1-mm reconstruction interval. Coronal-multiplanar images are
reconstructed from the retroperitoneal border to the anterior abdominal
wall at 2-mm slice width and 1-mm reconstruction interval.
of these studies can be very challenging. Two-millimeter slices in the
axial and coronal planes covering the entire abdomen and pelvis,
repeated for 3 phases, can generate 1500-2500 images per case. Lesions
may consist of a tiny nidus of enhancement visible on only 1 of the 3
phases, which adds an additional challenge. Also, some masses may be
isodense with the bowel wall and completely undetectable if the bowel is
under-distended. To maximize the chances for successful interpretation,
it is necessary to have a strategy for viewing these studies. We read
all our studies on a dual-monitor workstation. Our method of review
consists of placing the enteric phase on the left monitor and the
arterial and delayed images on the right -- one above the other. All
images are synchronized so that identical anatomic locations are
displayed while we scroll through the images from each phase. Viewing
each phase simultaneously allows the appreciation of the evolving nature
of enhancing lesions. Once a suspicious area is found, the
corresponding co-registered coronal images are displayed to determine
the approximate location and lesion shape.
While this technique is
designed to detect small bowel abnormalities responsible for bleeding,
the entire GI tract should be examined. We know from previous reports
that endoscopy fails to detect endoscopically accessible lesions in the
upper GI tract in up to 26% of patients.7 It is therefore
important when interpreting MpCTE exams not only to evaluate the small
bowel, but also to carefully examine the upper GI tract and colon. A
poorly prepared colon may prevent detection of a lesion at colonoscopy
which may be visible on MpCTE. Furthermore, submucosal lesions may not
produce mucosal disruption and, therefore, they may go undetected by
MpCTE findings in OGIB
The list of
small-bowel abnormalities responsible for OGIB is long. The source of
small-bowel bleeding varies somewhat, depending upon the patient’s age.
In patients younger than 40 years, small-bowel tumors, Crohn’s disease,
Meckel’s diverticulum, and Dieulafoy lesions are more prevalent than in
older patients. In patients older than 50 years, vascular lesions make
up 40% of etiologies, followed by NSAID-induced small bowel disease, and
a variety of less common disorders.8
responsible for OGIB may be visible on MpCTE as focal areas of
enhancement that may vary in intensity on each phase, depending upon the
nature of the abnormality. Others may appear as mass lesions that may
or may not enhance. Isodense polypoid masses may be undetectable when
concealed by incompletely distended bowel. Isodense lesions, small
lesions, and lesions visible on only 1 phase or the 3 phases are the
most frequently overlooked.
The shape, enhancement
characteristics, and evolving appearance of the lesion during the 3
phases may allow a specific diagnosis, expediting treatment decisions.
For example, a tiny nidus of bright enhancement, evident only on the
arterial phase, with an associated early-draining mesenteric vein,
likely represents an arteriovenous malformation and may be treated with
embolization (Figure 1). On the other hand, a small-bowel carcinoid,
appearing as a plaque-like enhancing intramural mass, brightest on the
enteric phase and fading slightly on the delayed phase, should trigger a
surgical consult (Figure 2).
Small-bowel vascular lesions consist
of angioectasias, Dieulafoy lesions, arteriovenous malformations
(AVMs), venous angiomas and varices.9 The MpCTE enhancement
pattern of small-bowel vascular lesions is frequently characteristic
(Table 1). Angioectasias are the most common type; they may appear as
tiny nodular or plaque-like areas of enhancement brightest on the
enteric phase, fading slightly on the delayed phase (Figure 3), or as
segments of bulbous swelling within intramural vessels (Figure 4). This
latter appearance is often seen in the jejunum in older patients with no
history of OGIB. Boley described dilated intramural veins in
association with colonic angioectasia.10 Whether this finding
is associated with small-bowel angioectasias or it represents a normal
finding is uncertain. Due to the high flow, Dieulafoy lesions and AVMs
may be visible only on the arterial phase and disappear on subsequent
phases. Unlike Dieulafoy lesions, AVMs are sometimes accompanied by an
early draining vein.
Venous angiomas of the small bowel are rare.
Their MpCTE appearance resembles hepatic cavernous
hemangiomas—demonstrating progressive enhancement during subsequent
phases. Ectopic varices in the small intestine (Figure 5) represent
portal-systemic shunts; they usually occur in association with adhesions
between the small intestine and adjacent structures, such as the
abdominal wall, which develop as a result of prior operations or
In our experience, small-bowel carcinoids are
one of the most common neoplasms encountered in OGIB. When small, they
may appear as a nodule or plaque-like area of enhancement in the bowel
wall, brightest on the enteric phase and fading slightly on the delayed
images. The serosal surface may be slightly retracted because of
fibrotic reaction associated with these tumors (Figure 6). Associated
mesenteric adenopathy is common, even with small tumors, and should
trigger a closer look for an enhancing bowel wall mass.
of other small-bowel masses may be encountered. Often these lesions may
be small and isodense with bowel wall, making them very difficult to
detect. In addition, without adequate bowel distention, polypoid lesions
will be shrouded by the collapsed bowel wall and go undetected. Often,
the bowel loop will be distended enough during 1 or 2 of the phases to
permit detection of the mass (Figure 7). Sometimes an isodense lesion
may be more obvious on coronal or sagittal images.
is manifested on MpCTE as the progressive accumulation of intraluminal
contrast displayed over the 3 phases. The extravasated contrast may pool
on the dependent surface of the bowel or it may be dispersed by
peristalsis into a more irregular shape. Active bleeding should be
suspected whenever one sees a contrast collection that expands in size
over subsequent phases (Figure 8). Compared to prior reports on the use
of CT in GI bleeding, in our practice, which consists principally of
hemodynamically stable outpatients, active bleeding is relatively
uncommon. The ability of MpCTE to detect non-bleeding small bowel
lesions responsible for OGIB is a testimony to the robustness of this
Performance of MpCTE in obscure GI bleeding
introduced MpCTE into our practice in 2005. We reported our initial
experience in a retrospective study of 22 patients with OGIB who
underwent multiphase CT enterography using the technique described
above. CT findings were compared with capsule and traditional endoscopy,
surgery, and angiography. MpCTE was positive for a bleeding source in
10 of 22 patients (45%). Eight of 10 positive MpCTE exams agreed with
capsule endoscopy findings or subsequent final diagnosis. MpCTE
correctly identified 3 lesions undetected at capsule endoscopy. The
results of the study suggested an important role in evaluating obscure
GI bleeding.11 In a follow-up blinded, prospective study
conducted at our institution comparing MpCTE with capsule endoscopy in a
group of patients with obscure GI bleeding, MpCTE detected a
small-bowel bleeding source in 14 of 16 patients (88%) compared to 6 of
16 (38%) for CE. MpCTE detected all 9 small-bowel masses compared to 3
of 9 for CE.12 As a result of these studies, MpCTE has become
the initial preferred exam in our practice for the workup of patients
with OGIB. We currently perform 20 to 30 MpCTE exams each month.
Patients with negative MpCTE exams usually undergo capsule endoscopy.
major drawback of MpCTE is the significant patient radiation dose
(equivalent to 3 single-phase CT-enterography exams—approximately 35 to
40 mSv). Obviously, the dose can be reduced by eliminating 1 or 2 of the
phases, but based upon our previous study, doing so significantly
lowers sensitivity.13 The recent introduction of dose
reduction techniques promises to offer significantly reduced patient
dose without loss of diagnostic accuracy.14 Furthermore, we
should apply this technique judiciously by insisting that patients
undergo upper endoscopy and colonoscopy to exclude a bleeding source
prior to performing MpCTE. In younger patients whose cumulative lifetime
radiation risk is likely to be greater than older patients, one must be
even more cautious so as not to expose them to unnecessary risks
MpCTE is a robust technique
for the evaluation of OGIB. It can be performed easily in routine
clinical settings. Combined with capsule endoscopy, it offers the best
chance for detecting the cause of obscure GI bleeding.
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- Boley SJ, Sammartano R, Adams A, et al. On the nature and etiology
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- Huprich J, Fletcher J, Alexander JA, et al. Obscure gastrointestinal
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- Huprich JE, Fletcher JG, Fidler JL, et al. Prospective blinded
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- Thacker P, Huprich J, Barlow J, et al. The performance of
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