AJR 2000; 174:107-115
© American Roentgen Ray Society
Bowel Wall Thickening on Transabdominal Sonography
Hans Peter Ledermann1,
Norbert Börner2,
Holger Strunk3,
Georg Bongartz1,
Christoph Zollikofer4 and
Gerd Stuckmann4
1
Department of Radiology, University Hospital of Basel, Petersgraben 4, CH-4031
Basel, Switzerland.
2
Gastroenterologische Gemeinschaftspraxis, Parcusstr. 8, 55116 Mainz,
Germany.
3
Department of Radiology,
Friedrich-Wilhelms-Universität Bonn,
Sigmund-Freud-str. 25, 53105 Bonn, Germany.
4
Department of Radiology, Kantonsspital Winterthur, Brauerstr. 15, 8400
Winterthur, Switzerland.
Received January 27, 1999;
accepted after revision June 7, 1999.
Address correspondence to H. P. Ledermann.
Introduction
The potential value of transabdominal sonography in the diagnosis of bowel
diseases is often not sufficiently appreciated and is even underestimated.
Bowel gas artifacts and the somewhat confusing sonographic appearance of the
gastrointestinal tract may render orientation and interpretation of
sonographic structures difficult. Bowel wall thickening, the main sonographic
correlate of bowel disorders, seems at first glance a very nonspecific sign,
which may explain why inexperienced investigators do not feel confident in the
sonographic evaluation of the gastrointestinal tract. However, it has been
shown that transabdominal sonography achieves good to excellent results as a
directed tool for evaluating potential bowel disorders: appendicitis can be
diagnosed with a sensitivity ranging from 80% to 93% and a specificity between
94% and 100% [1,
2]. Reported sensitivity rates
for evaluating inflammatory bowel disease range between 67% and 96%, with
specificities of 79-97% [3,
4]. Equal diagnostic accuracy
of 84% was found for CT and for sonography in the workup of diverticulitis,
with sensitivities of 91% and 85%, respectively, and specificities of 84% and
77%, respectively [5]. Although
the sonographic appearance of bowel wall thickening of different diseases
sometimes overlaps, careful examination of the thickened bowel segment in
context with the clinical information often leads to a limited differential
diagnosis or to the correct diagnosis.
The differential diagnoses of small-bowel wall thickening and of colonic
wall thickening are shown in Appendixes 1 and 2, respectively.
This article provides a systematic overview of diseases that may cause
bowel wall thickening. Typical sonographic features of these disorders are
discussed and compared. A review of the literature further summarizes the
reported diagnostic potential of sonography and its limitations.
Technique
Examination of the intestinal tract usually begins with a systematic
standardized survey using a curvilinear 3.5-5-MHz transducer. In patients with
localized abdominal pain, however, it may be helpful and timesaving to let
patients indicate the position of maximum pain with their fingers on the
abdominal wall and begin the examination there. In case of diffuse abdominal
pain, the frame of the colon is identified by its strong gas artifacts and is
screened from the cecum to the sigmoid colon. The rest of the abdomen is
examined in an individual standardized fashion to assure complete coverage of
the entire gastrointestinal tract. If intestinal wall thickening is found,
detailed evaluation of the diseased segment is performed with a linear or
curved high-frequency (7.5-13 MHz) transducer. When the affected bowel segment
is far from the abdominal surface and when the patient is obese, a fair amount
of pressure must be applied to the transducer to get acceptable images. For
optimal results, it may be necessary to change the patient's position several
times during the examination. Only careful methodic examination of the entire
abdomen leads to acceptable results; the accuracy of the examination depends
largely on the radiologist's experience and patience
[5]. Ideally, patients fast
overnight before the examination, but at least 4-5 hr of fasting are needed to
avoid excessive gas in the intestinal lumen.
Normal Sonographic Bowel Wall Anatomy
The typical sonographic appearance of the normal bowel wall consists of
five concentric, alternately echogenic and hypoechoic layers that we describe
from the lumen outward (Fig.
1). First, a small echogenic layer is seen that reflects the
superficial mucosal interface. The deep mucosa, including the muscularis
mucosa, is seen as a second hyperechoic layer. A third hyperechoic layer is
produced by the submucosa and the muscularis propria interface. The muscularis
propria is seen as a fourth hypoechoic layer. Finally, the marginal interface
to the serosa is seen as the fifth small hyperechoic layer. The average
thickness of the normal gut wall is 2-4 mm
[6].
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Fig. 1. —4-year-old girl with gastroenteritis. Sagittal sonogram shows normal
gut wall layering of rectum (RE) from lumen outward. Note small echogenic
layer in lumen that reflects superficial mucosal interface (short thin
arrow). Deep mucosa, including muscularis mucosa, is seen as second
hypoechoic layer (long thin arrow). Third broad hyperechoic layer is
produced by submucosa and muscularis propria interface (open arrow).
Muscularis propria is seen as fourth hypoechoic layer (short thick
arrow). Marginal interface to serosa is seen as small fifth hyperechoic
layer (curved arrow). ASC = ascites in retrovesical space, B =
bladder.
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Inflammatory Bowel Disease
The classic sonographic feature of Crohn's disease is the
"target" sign (Fig.
2A, Fig. 2B,
Fig. 2C) on transverse images,
which means a strong echogenic center surrounded by a relatively sonolucent
rim of more than 5 mm. This transmural inflammation or fibrosis can lead to
complete circumferential loss of the typical gut wall layers, which results in
a thick hypoechoic rim on axial images. Strictures are shown as marked
thickening of the gut wall with a fixed hyperechoic narrowed lumen
(Fig. 3A), dilatation, and
hyperperistalsis of the proximal gut. Peri-intestinal inflammation leads to
the "creeping fat" sign, which appears as a uniform hyperechoic
mass typically seen around the ileum and cecum. Mesenteric lymphadenopathy is
seen as multiple oval hypoechoic masses, usually in the right lower quadrant.
In contrast to other forms of colitis, Crohn's disease is suggested by skip
areas and involvement of the distal ileum
[7]. Possible complications of
Crohn's disease comprise fistulas, abscess formation, mechanical bowel
obstruction, and perforation
[8]. Abscesses are seen as
poorly defined, mostly hypoechoic focal masses that can contain hyperechoic
gas (Fig. 3B). Fistulas are a
hallmark of Crohn's disease and are seen in as many as one third of patients
with advanced disease as hypoechoic tracts with gas inclusions connecting
bowel loops or adjacent structures (bladder, abdominal wall, vagina, psoas
muscle) (Fig. 3C). Detection of
gas bubbles in abnormal locations raises the possibility of fistulous
communication.
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Fig. 2. —25-year-old woman with Crohn's disease who presented with new onset
of crampy abdominal pain.
A, Transverse sonogram shows concentric echolucent wall thickening
producing typical "target" sign.
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Fig. 2. —25-year-old woman with Crohn's disease who presented with new onset
of crampy abdominal pain.
B, Close-up longitudinal sonogram of same segment as A shows
circular hypoechoic wall thickening and loss of stratification that, together
with clinical information, led to diagnosis of Crohn's disease.
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Fig. 2. —25-year-old woman with Crohn's disease who presented with new onset
of crampy abdominal pain.
C, Small-bowel contrast-enhanced enema shows segmental bowel wall
edema (arrow) with "thumbprinting" and narrowing of
jejunal lumen in left lower abdomen. Diagnosis of Crohn's disease was later
clinically confirmed.
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Fig. 3. —Complications of Crohn's disease.
A, Stricture with obstruction in 52-year-old man. Transverse
sonogram of ileum (arrows) shows severe narrowing of small
hyperechoic central lumen caused by excessively echolucent wall thickening and
loss of stratification, indicating scarring of entire bowel wall.
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In expert hands, the distribution of frank lesions of inflammatory bowel
disease can be determined with a sensitivity of 73-87% on sonography
[3,
9,
10]. However, mild lesions
that produce less bowel wall thickening are frequently not diagnosed, and the
sensitivity for these lesions drops to 52%
[3]. These results indicate
that sonography cannot replace a contrast-enhanced examination or endoscopy
when highly accurate assessment of the extent of the inflammatory lesion is
requested [3].
Determination of disease activity by sonography is controversial. Whereas
some investigators showed correlation with disease activity
[4,
10,
11], others found only a loose
correlation between bowel wall thickening and disease activity
[9]. The ranges of reported
sensitivities and specificities in the diagnosis of Crohn's disease are 67-96%
and 79-97%, respectively [4,
12,
13,
14]. The relatively wide range
in the values of sensitivity and specificity may be explained by the use of
low-frequency transducers (3.5 MHz) in older studies and the use of
high-resolution equipment using 5-10-MHz broadband linear transducers. In
ulcerative colitis, sensitivity reaches 89% and specificity reaches 100%
[11]. Differentiation between
Crohn's disease and ulcerative colitis based on sonographic findings includes
the location of the disease, the presence of skip lesions, and the presence of
pericolic abscesses [14].
Bowel wall thickening is usually less marked in ulcerative colitis with
preserved stratification [15]
(Fig. 4A,
Fig. 4B). However, definite
differential diagnosis is difficult on transabdominal sonography
[4,
16].
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Fig. 4. —26-year-old man with ulcerative colitis and new onset of bloody
diarrhea.
A, Sagittal sonogram of descending colon reveals only subtle
thickening of bowel wall (4.2-mm-thick submucosa between crosses)
with preserved stratification and normal echo texture of adjacent mesenteric
fat.
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Fig. 4. —26-year-old man with ulcerative colitis and new onset of bloody
diarrhea.
B, Large-bowel enema with fine granularity of mucosa reflecting
hyperemia and edema confirms suspected sonographic diagnosis of early changes
in ulcerative colitis.
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Non-Hodgkin's Lymphoma of the Gastrointestinal Tract
The gut is the most commonly involved extranodal site of lymphoma
[17]. The most common sites,
in order of descending frequency, are stomach, small intestine, and colon,
especially cecum [17]. Eighty
percent of gastrointestinal lymphomas are of B-cell origin. In patients with
underlying celiac disease, however, T-lymphocyte origin predominates.
Sonography classically shows transmural circumferential, profoundly hypoechoic
wall thickening up to 4 cm in diameter
[18], with loss of normal
stratification (Fig. 5A). This
pattern, also known as the "pseudokidney" sign in longitudinal
views, is observed in 70% of patients
[19]
(Fig. 5B). The pseudokidney
sign is often seen in lymphoma because of extensive hypoechoic bowel wall
thickening, but it can be seen in any bowel disorder leading to marked bowel
wall thickening [20,
21]. Other findings include
nodular or bulky tumor spread caused by extraluminal involvement
[18]
(Fig. 5C). Mesenteric tumor
spread and bulky tumor growth need biopsy for definite diagnosis because they
cannot be reliably differentiated from other diseases such as primary bowel
tumors or metastases. Isolated mucosal involvement is rare and leads to
hyperechoic thickening of the mucosa (Fig.
5D). Sonographic patterns favoring the diagnosis of a
non-Hodgkin's lymphoma over adenocarcinoma are transmural circumferential,
profoundly hypoechoic wall thickening with preserved peristalsis; lack of
intestinal obstruction, because narrowing of the lumen is uncommon;
involvement of a long stretch of the gut; and the presence of multiple
prominent regional lymph nodes
[22]. Typical complications
are mucosal ulceration leading in 10-50% of patients to bleeding, perforation
of the small intestine, and intussusception of the bowel
[23]. The most commonly
involved nodal groups in non-Hodgkin's lymphoma of the gastrointestinal tract
are the celiac, retrocrural, perirenal, perisplenic, perihepatic, and
mesenteric nodes [22].
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Fig. 5. —Four typical sonographic variants of non-Hodgkin's lymphoma.
A, Most common circular involvement of entire wall with preserved
peristalsis in 45-year-old man with uncharacteristic abdominal pain.
Transverse sonogram reveals profound hypoechoic wall thickening.
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Fig. 5. —Four typical sonographic variants of non-Hodgkin's lymphoma.
B, "Pseudokidney" sign in ileocecal region: marked
hypoechoic thickening of bowel wall resembling form of kidney in longitudinal
sonogram of cecum. Patient is 57-year-old woman.
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Fig. 5. —Four typical sonographic variants of non-Hodgkin's lymphoma.
C, Bulky disease in cecum in 63-year-old woman. Axial sonogram
reveals large eccentric hypoechoic mass with compression of hyperechoic
lumen.
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Fig. 5. —Four typical sonographic variants of non-Hodgkin's lymphoma.
D, Isolated mucosal involvement in 43-year-old man. Transverse
sonogram of ileum with marked hyperechoic gyral thickening of mucosa and
preserved layering of bowel wall.
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Acute Terminal Ileitis
The clinical symptoms of acute ileitis are right-sided lower abdominal
pain, diarrhea, and nausea, with an accelerated erythrocyte sedimentation
rate, positive C-reactive protein, and leukocytosis. Only careful evaluation
in the preoperative workup for suspected appendicitis can prevent an
unnecessary operation [24].
Acute ileitis is caused by Yersinia species but
Campylobacter and Salmonella species may also be cultured.
Reported sonographic features include hypoechogenic mural thickening of the
terminal ileum and cecum between 6 and 10 mm with hypoechoic swollen ileal
folds in the edematous mucosa
[24,
25]. Hypoechoic enlarged
mesenteric lymph nodes ranging from 7 to 21 mm in diameter were found in most
patients. Color Doppler sonography in patients with infectious ileitis shows
increased flow centrally rather than peripherally (as in appendicitis)
[26].
Tuberculous enteritis and Behçet's syndrome
also predominantly affect the ileocecal region
[27]. In a series of 45
patients suffering from ileocecal tuberculosis, sonography showed segmental
predominantly concentric thickening of the terminal part of the ileum and
cecum in 43 patients [13],
with enlargement of the regional mesenteric lymph nodes in 50% of these
patients.
Appendicitis
The typical finding of acute appendicitis in transverse sonograms is the
target sign with a hypoechoic center, an inner hyperechoic ring, and an
external thicker hypoechoic ring (Fig.
6A). In sagittal images, the inflamed appendix is seen as a
blind-ending noncompressible tubular structure
(Fig. 6B). Focal or
circumferential loss of the inner layer of echoes usually indicates gangrenous
inflammation and ulceration of the submucosa. Several studies achieved
sensitivities of 80-93% and specificities of 94-100% in the sonographic workup
of acute appendicitis [1,
2]. On the other hand, CT has
shown sensitivities of 90-100% with specificities of 83-98%
28,
29,
30]. In one study with a low
(76%) sensitivity for sonography, CT was found to be more accurate than
sonography in the diagnosis of acute appendicitis
[28]. Graded compression
sonography gained widespread acceptance as a useful technique to examine
patients with atypical signs of appendicitis
[31]. In a prospective study,
the proposed treatment after clinical examination changed in 26% of all
patients after sonographic examination
[2]. The diagnosis can be
established with confidence if the appendix is noncompressible, shows no
peristalsis, and measures more than 6 mm in diameter
[32] on axial images, and if
compression leads to a localized pain response. The surrounding mesentery is
often inflamed, which can be seen as a hyperechoic diffuse halo sign around
the appendix (Fig. 6A). If an
appendicolith is identified in an appendix of any size, the findings of the
examination are always considered positive
[33]
(Fig. 6C). A simple additional
color Doppler examination may be helpful in the diagnosis of early acute
appendicitis [34]. The
presence of visible hyperemia or increased flow in the hypoechoic muscular
layer of the bowel wall may be a marker of appendicitis, whereas increased
flow in the mucosal layer most likely represents enteritis
[26]. Increased flow in the
fat surrounding the appendix is indicative of transmural extension of the
inflammation with mesenteric response. An inflamed appendix rarely measures
more than 15 mm in transverse diameter
[33], which usually allows
differentiation from ileitis. A markedly enlarged or perforating appendix or
dilated fallopian tubes may lead to interpretive pitfalls
[33].
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Fig. 6. —Sonographic findings in acute appendicitis.
A, "Target" sign (curved arrows) in acute
appendicitis in 12-year-old girl. On transverse image, inflamed appendix is
seen with hypoechoic center, inner hyperechoic ring, and outer hypoechoic
ring. Note hyperechoic circular area (straight arrows) of inflamed
mesentery ("halo" sign).
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Fig. 6. —Sonographic findings in acute appendicitis.
C, Multiple appendicoliths in 6-year-old girl. Longitudinal section
of inflamed appendix reveals five round hyperechoic appendicoliths with
acoustic shadows.
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Perforation occurs in 20-30% of young patients with appendicitis
(Fig. 6D). A statistically
significant association exists between perforation and two sonographic
findings: loculated pericecal fluid and loss of the echogenic submucosa
[35]. Abscess formation is the
major complication of perforating appendicitis. Abscesses may extend into the
pelvis or into the peritoneal spaces of the upper abdomen. They may be
sonolucent or appear as a complex mass. Advantages of sonography are wide
availability, lack of radiation, and lack of contrast administration.
Limitations of sonography occur in obese and extremely meteoristic patients
and in patients with severe pain due to peritonitis. Retrocecal appendicitis
may be difficult to diagnose on sonography. Because CT has been shown to be
more accurate in staging periappendiceal inflammation and abscesses
[5,
28,
36], CT may be preferred in
patients with suspected perforation or abscess; CT reliably differentiates
phlegmon from abscess and serves as an accurate "road map" for
potential abscess drainage.
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Fig. 6. —Sonographic findings in acute appendicitis.
D, Perforating appendicitis in 6-year-old girl. Longitudinal
sonogram of inflamed appendix shows typical blind-ending tubular structure and
hypoechoic collection around tip, indicative of perforation.
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Small-Bowel Diseases
Mesenteric infarction in its late stages leads to small-bowel wall
thickening [37,
38]. In the early stages,
however, no bowel wall thickening may be seen. Doppler sonography can aid in
differentiating ischemic and inflammatory bowel wall thickening. In
approximately 90% of cases, small-bowel infarctions are due to arterial
hypoperfusion; only 10% are caused by mesenteric vein occlusion. Acute
intramural intestinal hematoma leads typically to a homogeneous hypoechoic
symmetric thickening of a long stretch of the affected bowel segment, with
reduced or absent peristalsis and marked luminal narrowing
[39]
(Fig. 7). In the subacute
stage, strong internal echoes caused by thrombi may mimic an abscess
[40].
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Fig. 7. —72-year-old woman with intramural hematoma due to anticoagulant drug
therapy. Patient was sent for sonography to rule out atypical appendicitis.
Transverse sonogram of small-bowel segment discloses circumferential
hypoechoic thickening of bowel wall with loss of stratification and
compression of lumen.
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Amyloidosis is a rare condition; however, gastrointestinal involvement in
patients with amyloid is frequently seen
[41]. Marked hypoechoic
thickening of the affected bowel segments is found
[42,
43].
Eosinophilic enteritis is a rare disease characterized by infiltration of
the stomach or bowel wall with eosinophilic leukocytes. In three reported
cases, hypoechoic thickening of multiple ileal loops, narrowing of the lumen,
and loss of layer structure were described
[44,
45].
The sonographic features of primary lymphangiectasia have been described in
four patients [46,
47]. Diffuse hypoechoic
small-bowel wall thickening, ascites, mesenteric edema, and thickened walls of
the gallbladder and urinary bladder are found.
One case report describes the sonographic findings of nontropical sprue
(celiac disease) as diffuse hypoechoic thickening of the entire small-bowel
wall that disappears completely after 3 months of a gluten-free diet
[48].
Sonographic findings in a patient with Whipple's disease (intestinal
lipodystrophy) disclosed hyperechoic concentric thickening of the small bowel
with enlarged hyperechoic lymph nodes
[49]. The hyperechoic
structure of the intestinal wall and the enlarged lymph nodes are explained by
fat accumulation in these structures
[50]
(Fig. 8A,
Fig. 8B,
Fig. 8C).
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Fig. 8. —50-year-old man with Whipple's disease (intestinal lipodystrophy)
presenting with steatorrhea.
B, Transverse sonogram shows jejunal thickening and hyperechoic
lobulated lymph node (arrow).
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Fig. 8. —50-year-old man with Whipple's disease (intestinal lipodystrophy)
presenting with steatorrhea.
C, CT scan shows prominent jejunal folds and enlarged mesenteric
lymph nodes. (Courtesy of Disler M, Kantonsspital Liestal, Switzerland)
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Markedly thickened hypoechoic bowel loops, preferentially in the distal
ileum, were found in intestinal anisakiasis, a parasitic disease of the
gastrointestinal tract caused by ingestion of Anisakis larvae in raw
or undercooked fish [51].
Hypoechoic small-bowel wall thickening reaching 11 mm and revealing a
pseudokidney appearance was found in a patient suffering from intestinal
Behçet's disease
[21]. Cytomegalovirus
enteritis in AIDS patients leads to wall thickening of the small and large
bowels with preserved stratification.
Tumors of the Small Intestine Other Than Lymphomas
Peritoneal carcinomatosis is the most frequent malignant lesion of the
small bowel and may lead to irregular wall thickening with the typical
contraction of several bowel loops to a conglomerate. Most frequent primary
tumors originate from the ovary, stomach, colon, pancreas, gallbladder, lung,
and uterus. Primary small-bowel tumors constitute only 3-6% of
gastrointestinal neoplasms. Abdominal symptoms are usually vague and poorly
defined, and conventional radiography of the upper and lower intestinal tract
often has normal results. These factors may lead to a delayed diagnosis.
Carcinoid tumor is the most frequent small-bowel tumor
[52] and occurs in 80% of
cases in the distal ileum (Fig.
9A, Fig. 9B). All
small-bowel carcinoids are considered malignant because they eventually grow,
invade, and metastasize. Metastases will occur in 10% of lesions smaller than
1 cm and 95% of lesions larger than 2 cm
[53]. Only 4% of patients
present with the typical carcinoid syndrome
[54]. In a series of six
patients, small bowel carcinoids presented as hypoechoic, homogeneous
predominantly intraluminal masses with smooth intraluminal contour
[54]. The tumors were attached
to the wall by a broad base, with interruption of the submucosa and thickening
of the muscularis propria in all cases. Carcinoid tumors of the appendix were
described in two cases [55] as
hypoechoic, well-delineated elongated masses in the distal lumen and the tip
of the appendix.
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Fig. 9. —57-year-old man with ileal carcinoid tumor presenting with
mechanical small-bowel obstruction.
A, Transverse sonogram of terminal ileum reveals hypoechoic,
homogeneous intraluminal mass with smooth intraluminal contour and broad-based
hypoechoic infiltration of submucosa posteriorly. Note fluid-distended
small-bowel segments ventral to tumor, indicating mechanical obstruction.
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Fig. 9. —57-year-old man with ileal carcinoid tumor presenting with
mechanical small-bowel obstruction.
B, CT scan reveals strongly enhancing mass (arrow) in
terminal ileum, with infiltration of mesenteric fat dorsally and mechanical
obstruction of small bowel.
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Lipomas are the second most common tumors of the small intestine and occur
with greatest frequency in the distal ileum and at the ileocecal valve. The
location of these tumors is submucosal, or, less frequently, is subserosal. In
three fourths of cases, the tumors are clinically silent
[56]. If the lipoma becomes
larger than 4 cm, chronic hemorrhage caused by ulceration of the mucosa or
intestinal obstruction resulting from intussusception may cause symptoms
[57,
58]. Typical sonographic
features are a well-circumscribed hyperechoic round or oval mass with
deformation under compression. Leiomyomas and schwannomas are seen as
hypoechoic intramural round structures with smooth boundaries
[52,
58,
59]. Ulceration of the mucosa
may cause gastrointestinal hemorrhage of varying severity. Leiomyosarcomas
were described as large irregular masses with a heterogeneous echo pattern
[58]. Adenocarcinoma is the
second most common small intestine malignancy and the peak incidence is in the
seventh decade of life [52]. A
series of four cases with duodenal adenocarcinomas showed moderately large
intraluminal masses with medium echogenicity
[58]. The authors report
improved sonographic detection of small-bowel tumors by intermittent
observation of the small-bowel lesions during the first hour after water
ingestion. Transabdominal sonography reached excellent sensitivity in
detecting small-bowel tumors in unexplained gastrointestinal bleeding
[59] and in small-bowel
obstruction [60]. In most
cases, the tumors were seen as round and smoothly delineated hypoechoic
masses.
Colitis
The sonographic features of pseudomembranous colitis have been described in
a number of reports [61,
62]. Striking thickening of
the colonic wall with a wide inner circle of heterogeneous medium echogenicity
surrounded by a narrow hypoechoic muscularis propria is found in all patients,
reflecting the gross submucosal edema. The lumen of the colon is almost
completely effaced by the mural edema, and 64-77% of the patients have ascites
[61,
62]. The presence of these
sonographic features in a patient with watery diarrhea and a history of
antibiotic therapy strongly suggests the diagnosis of pseudomembranous
colitis. Pseudomembranous colitis shows typically a strong folding or gyral
pattern of the swollen submucosa.
Ischemic colitis cannot be differentiated solely by sonography from
inflammation or any other form of colonic wall thickening. However, duplex and
color Doppler sonography may be helpful in differentiating between ischemic
and inflammatory bowel wall thickening
[63]. Absence of or barely
visible color Doppler flow and absence of arterial signal suggest ischemia. On
the other hand, readily visible color Doppler flow and a stratified echo
texture suggest inflammation. Various case reports have described colonic wall
thickening in different forms of infectious and noninfectious colitis
[24,
64,
65,
66,
67].
Diverticulitis
Sonographic features of diverticulitis include visualization of diverticula
(Fig. 10A), thickening of the
bowel wall, inflammatory changes in the pericolic fat (typically on the
mesenteric side of the colonic wall) (Fig.
10B), intramural or periocolic abscess
(Fig. 10C), and (usually)
severe local tenderness induced by graded compression. Diverticula are round
or oval echogenic foci seen in or right next to the gut wall, mostly with
internal acoustic shadowing. Thickening of the bowel wall is usually
considered present when the distance from the echogenic lumen interface to the
hyperechogenic serosa and pericolic fat exceeds 4 mm
[5]. Inflammatory changes in
the pericolic fat are seen as ill-defined echogenic areas surrounding the
thickened colon segment. Pericolic abscesses typically present as hypoechoic
masses adjacent to the inflamed bowel. The major sonographic finding in
patients with uncomplicated acute diverticulitis of the right colon has been
found to be a hypoechoic round or oval focus protruding from the segmentally
thickened colonic wall and representing small abscesses in the pericolic fat
[68]. The sensitivity of
sonography in the diagnosis of acute colonic diverticulitis ranges in the
literature from 84% to 100% [5,
69,
70,
71]. In a recent study
comparing sonography and CT in the evaluation of acute colonic diverticulitis,
both techniques reached a similar sensitivity (85% and 91%, respectively) and
specificity (84% and 77%, respectively)
[5]. False-negative results may
occur if inflammatory bowel wall thickening is only mild
[3]. False-positive results are
reported in adenocarcinoma, lymphoma, Crohn's disease, ischemic colitis, and
extracolic inflammatory conditions adjacent to the colonic wall
[69,
71]. False-positive results
may be reduced with Doppler sonography
[63]. Potential pitfalls in
diagnosing pericolic abscesses are collections smaller than 2.5 cm in diameter
[5], interloop abscesses, and
abscesses with gas inclusions
[69]. CT is more accurate than
sonography in revealing abscesses
[5,
28,
36] and is helpful in planning
percutaneous drainage by exactly delineating the bowel loops
[5].
Colonic Carcinoma
Abdominal sonography may be the first imaging method that patients with
colonic cancer undergo when they present with nonspecific gastrointestinal
symptoms. Careful sonographic evaluation of the bowel may disclose a focal
mass or mural thickening. Sonographic diagnosis of colonic carcinoma has been
described by several authors
[72,
73,
74]. Colonic carcinomas have
two typical sonographic appearances
[75]. The first type is seen
as a localized hypoechoic mass up to 10 cm or more with an irregular shape and
a lobulated contour. The intraluminal gas, seen as a cluster of high
amplitude, is usually eccentrically located around the mass
(Fig. 11A). The second type
shows segmental eccentric or circumferential thickening of the colonic wall.
The mural thickening may be irregular but not as severe as in the first type
(Fig. 11B). The central echo
clusters are small because the diseased lumen is usually narrow. This type
leads frequently to colonic obstruction. Rectum carcinomas are seen only when
the bladder is well-filled (Figs.
11B and 11C).
Sonography enables localization of large-bowel obstruction in 85% of patients
and diagnosis of the cause of large-bowel obstruction in 81% of patients
[76]. Shirahama et al.
[77] described four
sonographic patterns that allowed correct diagnosis of colonic carcinoma in
90% of patients: localized irregular thickening of the colonic wall with
heterogeneous low echogenicity; irregular contour; lack of movement or change
in configuration on real-time scanning; and absence of a layered appearance of
the colonic wall. Other findings include lymphadenopathy in most patients and
abscess formation in 10% of patients. In a recent publication, malignant
conditions of the colon showed the following characteristics: loss of
stratification, absence of perigut findings, and involvement of a short bowel
segment with significantly greater wall thickness than is present in benign
processes [62]. However,
negative findings on sonographic examinations do not rule out the diagnosis of
colonic carcinoma because small masses and overlying bowel gas can lead to
false-negative results [72,
76]. Because of these
limitations, mainly in sensitivity, abdominal sonography is not an effective
screening technique in the diagnosis of colonic cancer.
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Fig. 11. —Sonographic features of colonic carcinoma.
A, Eccentric type in 52-year-old man. Transverse sonogram shows
typical irregular eccentric thickening of cecum wall and loss of
stratification. Note eccentrically located intraluminal air
(arrow).
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Fig. 11. —Sonographic features of colonic carcinoma.
B, Circumferential type in 66-year-old man. Longitudinal sonogram of
sigmoid colon with irregular circumferential thickening (arrows) of
short colonic wall segment.
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Fig. 11. —Sonographic features of colonic carcinoma.
C, Polypoid rectal carcinoma in 59-year-old man. Transvesical
transverse sonogram of rectum shows endoluminal round polypoid tumor measuring
3 cm in diameter (between crosses).
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Intussusception
Only 5-10% of all intussusceptions occur in adults
[78,
79]. The clinical symptoms may
suggest partial obstruction of the intestine, but diagnosis may be difficult
because symptoms are often nonspecific
[79]. The ileocecal region is
the most commonly affected area in children, whereas there is no clearly
preferred anatomic site in adults. Most intussusceptions in children are
idiopathic and are presumed to be the result of enlarged lymphoid follicles in
the terminal ileum. An organic cause can be shown in as many as 90% of cases
in adults [78,
79]. The leading mass is
nearly always a tumor of the intestinal wall, usually malignant in
intussusceptions of the colon
[80] and benign in
intussusceptions of the small intestine
[57,
78]. The sonographic hallmark
of intussusception has been described as the target
[81], "doughnut,"
or "bull's-eye" sign
[82]. Typically, one finds two
hypoechoic rings separated by a hyperechoic ring or crescent on axial images
(Fig. 12A,
Fig. 12B). On longitudinal
images, a pseudokidney structure or layering of hypoechoic lines with
hyperechoic areas is observed. The outer hypoechoic ring is formed by the
intussuscipiens and the everted returning limb of the intussusceptum, with
their mucosal surfaces face to face
[83]. The center of the
intussusception varies with the scan level. At the apex, the center is
hypoechoic because of the entering limb of the intussusceptum. At the base,
the entering bowel wall forms a hypoechoic center that is surrounded by the
hyperechoic mesentery [83]. In
a case of surgically proven triple jejunojejunocolonic intussusception
[84], three hypoechoic rings
separated by two hyperechoic rings were found on sonography.
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Fig. 12. —57-year-old man with intussusception of anastomosed jejunum into
remaining stomach after a Billroth II procedure (subtotal gastrectomy).
A, Transverse sonogram shows hypoechoic kidney-shaped mass
reflecting remnant of stomach with intussusception in its lumen. Small
hyperechoic ring formed by invaginated mesentery divides intussuscipiens
(gastrojejunal anastomosis) on outside from intussusceptum (jejunum) and leads
to a "ring-in-ring" structure.
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Conclusion
Sonography of the gastrointestinal tract should be included in abdominal
sonography of patients presenting with abdominal pain of unknown origin to
look for potential bowel disorders. Careful analysis of the sonographic
changes of a thickened bowel segment in context with the clinical information
often leads to a limited differential diagnosis or even to the correct
diagnosis. If a bowel disorder is detected, targeted use of barium enemas, CT,
endoscopy, or biopsy can be performed if additional workup is needed.
More large-scale studies are needed to compare the use of sonography with
other methods for imaging the various diseases of the gastrointestinal
tract.
APPENDIX 1: Differential Diagnosis of Small-Bowel Wall Thickening
Common:
- Inflammatory bowel disease (Crohn's disease and backwash ileitis)
- Acute ileitis (Yersinia, Campylobacter species)
- Postoperative edema
- Peritoneal carcinomatosis
- Mesenteric infarction (arterial, venous)
- Extraintestinal inflammatory conditions adjacent to bowel wall
Less common:
- Intestinal hematoma
- Cytomegalovirus enteritis in AIDS patients
- Intussusception
- Lymphoma
- Carcinoid and other malignant tumors
- Benign tumors (lipoma, adenoma, and schwannoma)
Rare:
- Tuberculosis
- Celiac disease
- Whipple's disease
- Eosinophilic enteritis
- Endometriosis
- Amyloidosis
- Anisakiasis
- Behçet's disease
- Sarcomas
APPENDIX 2: Differential Diagnosis of Colonic Wall Thickening
Common:
- Diverticulitis
- Carcinoma
- Inflammatory bowel disease (Crohn's disease and ulcerative colitis)
- Colitis
- Appendicitis
- Postoperative edema
- Peritoneal carcinomatosis
Less common:
- Extracolic inflammatory conditions adjacent to the colonic wall
- Intussusception
Rare:
- Lymphoma
- Amyloidosis
- Endometriosis
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