DOI:10.2214/AJR.04.1362
AJR 2006; 186:491-498
© American Roentgen Ray Society
Clinical Significance of Poor CT Enhancement of the Thickened Small-Bowel Wall in Patients with Acute Abdominal Pain
Chung Kuao Chou1,2,
Reng Hong Wu1,
Chee-Wai Mak1 and
Ming-Pin Lin1
1 All authors: Department of Radiology, Chi Mei Medical Center, 901 Chung Hwa
Rd., Tainan 71010, Taiwan, Republic of China.
2 Department of Radiological Technology, Central Taiwan University of Science of
Technology, Taiwan, Republic of China.
Received August 30, 2004;
accepted after revision January 24, 2005.
Address correspondence to C. K. Chou
(wushung{at}mail.chimei.org.tw).
Abstract
OBJECTIVE. Our purpose was to compare clinical outcomes in patients
with acute abdominal pain and inner-layer enhancement of a thickened
small-bowel wall, as shown on CT, with outcomes in similar patients without
such enhancement.
MATERIALS AND METHODS. We retrospectively studied outcomes in 126
patients with acute abdominal pain and small-bowel wall thickening on CT: 84
with inner-layer enhancement and 42 without this enhancement. We compared the
surgical, small-bowel resection, small-bowel necrosis, and mortality rates
between the two groups using the chi-square test.
RESULTS. Among the 42 patients without inner-layer enhancement, 32
(76%) underwent an operation, 27 (64%) received segmental small-bowel
resection, 26 (62%) had small-bowel necrosis, and seven (17%) died. All of
these proportions were significantly higher (p < 0.01) than the
corresponding rates—34 (40%), nine (11%), five (6%), and two (2%),
respectively—in the 84 patients with inner-layer enhancement. All 31
patients with necrotic small bowel had pathologic evidence of ischemic
necrosis involving the mucosa.
CONCLUSION. Among patients with acute abdominal pain, those whose CT
scans did not show inner-layer enhancement of a thickened small-bowel wall
were more prone to undergo surgery and small-bowel resection and were more
likely to have small-bowel necrosis than those with such enhancement. Poor
inner-layer enhancement on CT might be consistent with sloughed or necrotic
mucosa, as observed on pathology.
Keywords: abdomen • CT • ischemia • small bowel
Introduction
In patients with acute abdominal pain, uniform and circumferential
thickening of the small-bowel wall may result from a wide variety of diseases.
Examples include inflammatory bowel diseases, infectious diseases, vascular
disorders, radiation enteritis, shock, inflammation secondary to
intraabdominal infections, and other entities.
On contrast-enhanced CT images, this thickening can have different
appearances, including that of a homogeneous thickening with soft-tissue
attenuation and either avid (white attenuation pattern) or limited (gray
attenuation pattern) enhancement, the appearance of two concentric rings of
inner low-outer high attenuation (i.e., the double-halo sign), and that of
three concentric rings with high-low-high attenuation (i.e., the target sign)
[1-3].
In the case of the white attenuation pattern and the target sign, the
high-attenuating inner layer is often conveniently regarded as enhancing
mucosa, although this presumption might be doubted
[3]. In addition, whether
inner-layer enhancement is related to the severity of small-bowel damage is
unclear. Therefore, we conducted this retrospective study to compare the
clinical course, small-bowel viability, and outcomes in patients with acute
abdominal pain and inner-layer enhancement of thickened small-bowel wall on CT
and similar patients without such enhancement.
Materials and Methods
The patients were identified from the logbooks of our department in the
period between January 1997 and December 2003. The logbooks listed the
patient's name, sex, age, referring unit, and chief complaints. Those patients
referred from the emergency department or from the inpatient unit with a
specific mark for an emergent CT examination were recorded. We then checked
the CT reports, which included descriptions of the findings and diagnoses. If
the CT reports described thickening of the small-bowel wall, we collected the
CT scans and further reviewed the patients' medical records to determine the
nature of their abdominal pain, the causes of the small-bowel wall thickening,
and their clinical outcomes. The abdominal pain of patients referred from the
outpatient department or inpatient unit who received a routinely scheduled CT
examination was not always acute in nature.
In total, 135 CT examinations were collected. Nine patients died without
surgical intervention and were excluded because we were unable to determine
the condition of their small bowel. The remaining 126 patients included 70 men
and 56 women who ranged in age from 40 to 83 years, with a mean age of 65
years. The causes of small-bowel wall thickening are presented in
Table 1.
In all patients, the duration between the onset of abdominal pain and CT
examination was less than 72 hr; in most of them, the interval was less than
24 hr. For some patients, the duration was prolonged because they had sought
first aid in the outpatient clinic or at another hospital or because they
delayed seeking help until their pain became intolerable.
The CT examinations were performed using a single-detector helical CT
scanner (Sytec CT 4000, GE Healthcare). All patients underwent unenhanced and
enhanced CT of the whole abdomen. The section thickness was 7 mm with an
intersection gap of 3 mm. Scanning started about 30-40 sec after the beginning
of a bolus injection of 120 mL of ioxitalamate meglumine (Telebrix 30
Meglumine, Laboratorie Guerbet) at a rate of 1-2 mL sec. In order to avoid
obscuration of any enhancement of the small-bowel wall, oral contrast material
was given to these acutely ill patients.
Two experienced abdominal radiologists retrospectively reviewed the CT
scans that showed thickening of the small bowel. The normal small-bowel wall
thickness is dependent on the degree of luminal distention. On the basis of
descriptions provided in earlier articles
[1-7],
we defined small-bowel wall thickening as a thickness of greater than 3 mm if
the bowel was well distended or partially collapsed or as a thickness of
greater than 1 cm if it was collapsed or only slightly distended. The
radiologists were asked to determine whether the inner layer of the thickened
small-bowel wall was enhancing. Only two categories—without and with
enhancement—were applied. If their opinions differed, a third
radiologist was consulted to obtain a final decision. An enhanced inner layer
was defined as an inner layer with attenuation that was obviously higher on
contrast-enhanced images than on unenhanced images (Figs.
1A,
1B,
1C,
1D,
2A,
2B,
3A,
3B,
4A,
4B,
5A,
5B,
5C, and
5D). The radiologists compared
the attenuation of the thickened small-bowel wall with that of intraluminal
fluid, segments of normal small bowel, and abdominal wall or paraspinal
muscles (Table 2). If the CT
scan showed both areas with and without inner-layer enhancement in one
patient, we regarded that case as without inner-layer enhancement.
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Fig. 1A —62-year-old man with sepsis. Unenhanced (A) and enhanced
(B) CT scans. Longitudinal sections of thickened small bowel show inner
layer (arrow) before and after IV contrast administration. Intense
inner-layer enhancement is noted.
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Fig. 1B —62-year-old man with sepsis. Unenhanced (A) and enhanced
(B) CT scans. Longitudinal sections of thickened small bowel show inner
layer (arrow) before and after IV contrast administration. Intense
inner-layer enhancement is noted.
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Fig. 3A —76-year-old man with internal hernia. Unenhanced CT scan shows
circumferentially thickened wall (arrowhead) has density slightly
higher than body wall muscles. Adjacent thickened wall (arrow) is
darker than muscles.
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Fig. 3B —76-year-old man with internal hernia. Enhanced CT scan shows same
segment (arrowhead) as that seen in A has slightly lower
density than muscles. Adjacent segment (arrow) shows obviously
enhanced inner layer.
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Fig. 4A —42-year-old man with thrombosis of superior mesenteric vein.
Unenhanced (A) and enhanced (B) CT scans. Presence of
inner-layer enhancement (arrowheads) is in distinct contrast from
absence of inner-layer enhancement (arrows) in continuous small-bowel
segment.
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Fig. 4B —42-year-old man with thrombosis of superior mesenteric vein.
Unenhanced (A) and enhanced (B) CT scans. Presence of
inner-layer enhancement (arrowheads) is in distinct contrast from
absence of inner-layer enhancement (arrows) in continuous small-bowel
segment.
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Fig. 5A —53-year-old man with thrombosis of superior mesenteric vein.
Unenhanced (A) and enhanced (B) CT scans. Soft-tissue-density
hemorrhagic wall (arrowheads) does not show inner-layer enhancement.
Less damaged small bowel (arrows) shows faint whole-layer
enhancement.
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Fig. 5B —53-year-old man with thrombosis of superior mesenteric vein.
Unenhanced (A) and enhanced (B) CT scans. Soft-tissue-density
hemorrhagic wall (arrowheads) does not show inner-layer enhancement.
Less damaged small bowel (arrows) shows faint whole-layer
enhancement.
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Fig. 5C —53-year-old man with thrombosis of superior mesenteric vein.
Enhanced (C) and enhanced (D) CT scans. Cross-sectioned
(left arrow) and longitudinal-sectioned (right arrow) small
bowel shows absence of inner-layer enhancement. Hemorrhagic wall was nearly
isodense to abdominal wall muscles on unenhanced image and became hypodense on
enhanced image.
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Fig. 5D —53-year-old man with thrombosis of superior mesenteric vein.
Enhanced (C) and enhanced (D) CT scans. Cross-sectioned
(left arrow) and longitudinal-sectioned (right arrow) small
bowel shows absence of inner-layer enhancement. Hemorrhagic wall was nearly
isodense to abdominal wall muscles on unenhanced image and became hypodense on
enhanced image.
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For both groups, we calculated the rates of surgery, small-bowel resection,
small-bowel necrosis, and mortality and compared them using the chi-square
test. A p value of less than 0.05 was considered to be significant.
We also evaluated the interval between CT examination and surgery. For
patients who underwent small-bowel resection, we reviewed their records to
determine the cause and the pathologic findings.
Results
Inner-Layer Enhancement of the Small-Bowel Wall
The third radiologist was consulted in 17 cases (13%) to make a final
decision about the inner-layer enhancement pattern. Forty-two patients did not
have an obviously enhancing inner layer (group A), whereas 84 patients did
(group B). In 23 patients of group A, the CT scans showed both areas with and
areas without inner-layer enhancement in the same patient. In group B, CT
scans in 72 patients showed a targetlike appearance and images in 12 showed a
homogeneously enhancing layer.
Clinical Outcomes
The results are presented in Figures
6 and
7. Sixty patients recovered
with conservative treatment. We presumed that the small bowel was viable in
these cases. The other 66 patients underwent an operation. The interval
between CT and surgery was less than 6 hr in 30 patients (20 in group A and 10
in group B), 6-12 hr in 20 patients (seven in group A and 13 in group B), and
more than 12 hr in 16 patients (five in group A and 11 in group B).
In group A (n = 42), 32 patients (76%) underwent an operation, 27
(64%) received segmental small-bowel resection, 26 (62%) had small-bowel
necrosis, and seven (17%) died. All of these rates were significantly higher
(p < 0.01) than the respective rates in group B (n = 84):
34 (40%), nine (11%), five (6%), and two (2%). On further analysis, 27 (84%)
of the 32 surgical patients in group A received a segmental small-bowel
resection. This proportion was significantly higher (p < 0.01)
than that of group B (nine [26%] of 34).
Among the 36 patients who received small-bowel resections, 31 had
small-bowel necrosis (26 in group A and five in group B). Pathologic specimens
of these 31 cases of necrotic small bowel all revealed sloughing or
coagulative necrosis of the ghost villi, neutrophilic or erythrocytic
infiltrations in the ghost villi and submucosa, and various degrees of lysis
of the muscles. These appearances were typical of mucosal-to-transmural
necrosis due to ischemia. In our study, transmural necrosis occurred in 16
cases (14 in group A and two in group B) and mucosal necrosis in 15 cases (12
in group A and three in group B). The causes and types of small-bowel necrosis
are presented in Table 3. In
the patients with resected but nonnecrotic small bowel, small-bowel resection
was due to one case of intramural hemorrhage in group A and to two cases of
Crohn's disease, one case of volvulus, and one case of internal hernia in
group B. Two patients in group B died from peritonitis, which resulted from
bile leakage in one patient and a perforated marginal ulcer in the other.
On further analysis of the interval between CT and surgery, 20 (63%) of the
32 operations in group A were performed within 6 hr after CT examination,
whereas the operations were relatively equally distributed among the three
time intervals in group B. The difference in these trends in time interval was
significant (p < 0.05).
Discussion
Thickening of the small bowel wall may be a neoplastic or nonneoplastic
condition. Neoplasms are usually short (except lymphoma), irregular, and
asymmetric, and they tend to have a chronic onset. In contrast, nonneoplastic
small-bowel wall thickening is usually long, uniform, and circumferential,
with either an acute onset (e.g., ischemia, infection, inflammation,
intramural hemorrhage) or a chronic onset (e.g., Crohn's disease,
tuberculosis, liver cirrhosis, radiation enteritis, hypoalbuminemia,
lymphangiectasia, or other rare diseases). On contrast-enhanced CT scans, the
latter may have any of three appearances: homogeneous soft-tissue attenuation
and enhancing (white attenuation pattern) or poorly enhancing (gray
attenuation pattern); two concentric rings of inner low attenuation and outer
high attenuation (i.e., the double-halo sign); and three concentric rings of
high-low-high attenuation (i.e., the target or "water-halo" sign)
[1-3].
These different appearances may be related to the degrees of mucosal perfusion
or damage, the edematous or hemorrhagic changes of the submucosa, the amount
of fat deposition, and the quality of the CT examination.
Histologically and physiologically, the mucosa is the most vascularized
part of the intestines, followed by the submucosa and the muscularis propria.
A normally perfused mucosa should be the most intensely, or at least
isointensely, enhancing layer of a thickened small-bowel wall. The submucosa
is composed of connective tissue with nerves, vessels, and lymphatics
traversing it. However, its microvascular network is less abundant than that
of the mucosa. The normal submucosa is uncommonly seen as a separate structure
on CT scans unless it is edematous, hemorrhagic, or infiltrated by tumor, or
has fat deposits. Contrast enhancement of the thickened submucosa rarely if
ever approaches that of the normally perfused mucosa. Homogeneous enhancement
of a thickened wall might be attributed to a hyperemic mucosa.
Although poor inner-layer enhancement does not necessarily mean the absence
of perfusion, it may represent a severe compromise of the blood supply to the
mucosa or sloughing of the mucosa. In our study, the 31 cases of small-bowel
necrosis could be attributed to two main mechanisms of
ischemia—transient arterial insufficiency with reperfusion (three cases
of atrial fibrillation and two cases of thrombosis of the superior mesenteric
artery) or impaired venous drainage (four cases of intussusception and nine
cases of thrombosis of the superior mesenteric vein)—or their
combination (four cases of adhesion and five cases of closed-loop small-bowel
obstruction)
[8-11].
In the remaining four cases with intramural hemorrhage, massive blood
extravasation might have increased tissue tension in the extravascular
compartment, causing compression that limited microvascular blood flow and
that consequently led to ischemia. All these cases showed pathologic evidence
of mucosal necrosis and varying degrees of mural-to-transmural necrosis, 26 of
which did not have inner-layer enhancement on CT. This result might support
the presumption mentioned earlier that poor inner-layer enhancement may
represent a severe compromise of the blood supply to the mucosa or sloughing
or necrosis of the mucosa.
Because the mucosa is the most vascularized part of the intestines, an
ischemic insult first injures the mucosa, then the submucosa, and finally the
muscularis propria layer. Pathologically, small-bowel ischemia may be divided
into several types: first, mucosal necrosis in which the lesion is limited to
the mucosa; second, mural necrosis in which the lesion extends to the
submucosa or even into, but not through, the muscularis propria; and, third,
transmural necrosis in which the lesion extends through the muscularis propria
[12-14].
Mucosal or mural necrosis may heal without surgical intervention, although the
affected area may later become fibrotic and stenotic. Transmural necrosis
inevitably terminates with whole-layer necrosis and perforation. In group A,
the clinical course or pathologic evidence excluded transmural small-bowel
necrosis in 16 patients (10 did not undergo surgery, five underwent surgery
but not resection, and one underwent resection but did not have necrosis).
These results reflect the possibility that the damage was limited to the
mucosa and submucosa in these cases.
Compared with group B, group A had higher rates of surgery, small-bowel
resection, small-bowel necrosis, and mortality. Furthermore, the 32 surgical
patients in group A also had a small-bowel resection rate (n = 27,
84%) higher than that of the 34 surgical patients in group B (n = 9,
26%). This finding implied that the condition of the small bowel during
laparotomy was more likely to be judged as bad enough to need resection in
group A than in group B. From a clinical point of view, the final decision to
perform segmental small-bowel resection depends on several factors: the
surgeon's experience; the surgeon's judgment based on observation of the
external appearance, odor, and peristalsis of the thickened small bowel; and
the response of the small bowel to management such as embolectomy, detorsion,
enterolysis, or irrigation with warm saline. This assessment can be difficult,
and a second-look operation is sometimes necessary.
If the CT scan showed both areas with and areas without inner-layer
enhancement in a patient, we regarded it as without inner-layer enhancement
because we thought that the part without inner-layer enhancement had a worse
perfusion status and consequently would determine the fate of the thickened
small bowel.
The intervals between CT examinations and the operations were significantly
shorter in group A, as discussed in the Results section. The causes of this
difference are unclear; however, it may represent the need for an emergent
operation and thus may have indirectly reflected the more serious clinical
condition of the patients in group A.
The bowel wall enhancement patterns have been clearly described
[1-3],
and the terms are diverse. In our study, the appearance of the thickened wall
with poor inner-layer enhancement was similar to that described as the
double-halo sign [1],
homogeneous and poorly enhanced wall
[2], or a gray attenuation
pattern [3]. On the other hand,
the thickened wall with an inner-layer enhancement (group B) was similar
either to that described as a target sign
[1], stratified attenuation
[2], or
"water-halo" sign
[3]; or to that described as a
homogeneous and enhancing wall
[2] or white attenuation
pattern [3].
Our study had some limitations. First, visual comparison of the
intraluminal fluid, bowel wall, and muscles of the body wall may not be as
accurate as attenuation measurements in the evaluation of bowel wall
enhancement. Still, we believe that visual comparison is practical and
acceptable for daily routine work if an attenuation measurement is not
immediately available.
Second, we excluded nine patients who died without laparotomy or autopsy;
this exclusion might or might not have influenced our results. Two of these
patients (one with sepsis and one with congestive heart failure) were judged
to have no inner-layer enhancement and seven (three with sepsis and one each
with portal venous thrombosis, arrhythmia, aortic dissection, or undetermined
illness) to have inner-layer enhancement. When we included these patients with
the study groups, results for the rates of surgery, small-bowel resection, and
small-bowel necrosis remained the same. Only the mortality rates became
insignificantly different (group A vs B, 20% [9/44] vs 10% [9/91]; p
> 0.05). However, as stated earlier, we did not include these cases in the
study because data about their small-bowel conditions were not available.
Third, the CT manifestations might have been influenced by the duration
between the onset of abdominal pain and the CT examination, because
appearances on an early CT study might differ from those on a late study.
Finally, the clinical outcomes depended on the judgments of the physicians
in the emergency department, the surgeons, and the pathologists; the natures
of the diseases; and other factors. Solely attributing a high small-bowel
necrosis or mortality rate to a different bowel enhancement pattern may be an
oversimplification. Further large-scale studies may offer more definite
results to confirm the present findings.
In conclusion, our results suggest that patients with acute abdominal pain
without inner-layer enhancement of the thickened small-bowel wall on CT had a
prognosis worse than that of patients with this enhancement; their worse
outcomes included significantly higher probabilities of surgery, segmental
small-bowel resection, small-bowel necrosis, and mortality. Poor inner-layer
enhancement on CT scans might be consistent with a sloughed or necrotic
mucosa, as found on pathology.
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Abstract
Introduction
