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Review
Bowel Wall Thickening on Transabdominal Sonography
Hans Peter Ledermann 1, Norbert Brner 2, Holger Strunk 3, Georg Bongartz 1, Christoph Zollikofer 4, Gerd Stuckmann 4
echoic layer. A third hyperechoic layer is Inflammatory Bowel Disease ers, which results in a thick hypoechoic rim on
produced by the submucosa and the muscu- The classic sonographic feature of Crohns axial images. Strictures are shown as marked
laris propria interface. The muscularis pro- disease is the target sign (Fig. 2) on trans- thickening of the gut wall with a fixed hyper-
pria is seen as a fourth hypoechoic layer. verse images, which means a strong echogenic echoic narrowed lumen (Fig. 3A), dilatation,
Finally, the marginal interface to the serosa is center surrounded by a relatively sonolucent and hyperperistalsis of the proximal gut. Peri-
seen as the fifth small hyperechoic layer. The rim of more than 5 mm. This transmural in- intestinal inflammation leads to the creeping
average thickness of the normal gut wall is flammation or fibrosis can lead to complete fat sign, which appears as a uniform hyper-
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24 mm [6]. circumferential loss of the typical gut wall lay- echoic mass typically seen around the ileum
and cecum. Mesenteric lymphadenopathy is
Fig. 1.4-year-old girl with gastroenteritis. Sagittal seen as multiple oval hypoechoic masses, usu-
sonogram shows normal gut wall layering of rectum ally in the right lower quadrant. In contrast to
(RE) from lumen outward. Note small echogenic layer
in lumen that reflects superficial mucosal interface
other forms of colitis, Crohns disease is sug-
(short thin arrow ). Deep mucosa, including muscu- gested by skip areas and involvement of the
laris mucosa, is seen as second hypoechoic layer distal ileum [7]. Possible complications of
(long thin arrow ). Third broad hyperechoic layer is Crohns disease comprise fistulas, abscess for-
produced by submucosa and muscularis propria inter-
face (open arrow ). Muscularis propria is seen as mation, mechanical bowel obstruction, and
fourth hypoechoic layer (short thick arrow ). Marginal perforation [8]. Abscesses are seen as poorly
interface to serosa is seen as small fifth hyperechoic defined, mostly hypoechoic focal masses that
layer (curved arrow ). ASC = ascites in retrovesical
space, B = bladder. can contain hyperechoic gas (Fig. 3B). Fistulas
are a hallmark of Crohns disease and are seen
in as many as one third of patients with ad-
vanced disease as hypoechoic tracts with gas
inclusions connecting bowel loops or adjacent
A B
Fig. 2.25-year-old woman with Crohns disease who presented with new onset of crampy abdominal pain.
A, Transverse sonogram shows concentric echolucent wall thickening producing typical target sign.
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 Crohns disease.
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 Crohns disease was later clinically confirmed.
C
A B C
Fig. 3.Complications of Crohns 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 exces-
sively echolucent wall thickening and loss of stratification, indicating scarring of entire bowel wall.
B, Hypoechoic ileal abscess (A) in highly hypertrophic and inflamed hyperechoic fat of mesentery of 25-year-old woman.
C, Sonogram obtained at time of suspected relapse of 31-year-old woman shows hypoechoic fistula with small hyperechoic gas inclusion (arrow ).
structures (bladder, abdominal wall, vagina, assessment of the extent of the inflammatory lution equipment using 510-MHz broadband
psoas muscle) (Fig. 3C). Detection of gas bub- lesion is requested [3]. linear transducers. In ulcerative colitis, sensitiv-
bles in abnormal locations raises the possibil- Determination of disease activity by sonog- ity reaches 89% and specificity reaches 100%
ity of fistulous communication. raphy is controversial. Whereas some investiga- [11]. Differentiation between Crohns disease
In expert hands, the distribution of frank tors showed correlation with disease activity [4, and ulcerative colitis based on sonographic find-
lesions of inflammatory bowel disease can 10, 11], others found only a loose correlation ings includes the location of the disease, the
be determined with a sensitivity of 7387% between bowel wall thickening and disease ac- presence of skip lesions, and the presence of
on sonography [3, 9, 10]. However, mild le- tivity [9]. The ranges of reported sensitivities pericolic abscesses [14]. Bowel wall thickening
sions that produce less bowel wall thicken- and specificities in the diagnosis of Crohns dis- is usually less marked in ulcerative colitis with
ing are frequently not diagnosed, and the ease are 6796% and 7997%, respectively [4, preserved stratification [15] (Fig. 4). However,
sensitivity for these lesions drops to 52% 1214]. The relatively wide range in the values definite differential diagnosis is difficult on
[3]. These results indicate that sonography of sensitivity and specificity may be explained transabdominal sonography [4, 16].
cannot replace a contrast-enhanced exami- by the use of low-frequency transducers (3.5
nation or endoscopy when highly accurate MHz) in older studies and the use of high-reso-
Non-Hodgkins Lymphoma of the
Gastrointestinal Tract
The gut is the most commonly involved ex-
tranodal site of lymphoma [17]. The most
common sites, in order of descending fre-
quency, are stomach, small intestine, and co-
lon, especially cecum [17]. Eighty percent of
gastrointestinal lymphomas are of B-cell ori-
gin. In patients with underlying celiac disease,
however, T-lymphocyte origin predominates.
Sonography classically shows transmural cir-
cumferential, 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
A B
sign is often seen in lymphoma because of ex-
Fig. 4.26-year-old man with ulcerative colitis and new onset of bloody diarrhea. tensive hypoechoic bowel wall thickening, but
A, Sagittal sonogram of descending colon reveals only subtle thickening of bowel wall (4.2-mm-thick submucosa it can be seen in any bowel disorder leading to
between crosses) with preserved stratification and normal echo texture of adjacent mesenteric fat.
B, Large-bowel enema with fine granularity of mucosa reflecting hyperemia and edema confirms suspected marked bowel wall thickening [20, 21]. Other
sonographic diagnosis of early changes in ulcerative colitis. findings include nodular or bulky tumor spread
appendicitis) [26].
Tuberculous enteritis and Behets syn-
drome also predominantly affect the ileoce-
cal region [27]. In a series of 45 patients
suffering from ileocecal tuberculosis, sonog-
raphy showed segmental predominantly con-
A B centric thickening of the terminal part of the
ileum and cecum in 43 patients [13], with en-
largement 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 tu-
bular structure (Fig. 6B). Focal or circumferen-
C D tial loss of the inner layer of echoes usually
indicates gangrenous inflammation and ulcer-
Fig. 5.Four typical sonographic variants of non-Hodgkins lymphoma. ation of the submucosa. Several studies
A, Most common circular involvement of entire wall with preserved peristalsis in 45-year-old man with unchar- achieved sensitivities of 8093% and specifici-
acteristic abdominal pain. Transverse sonogram reveals profound hypoechoic wall thickening.
B, Pseudokidney sign in ileocecal region: marked hypoechoic thickening of bowel wall resembling form of kid- ties of 94100% in the sonographic workup of
ney in longitudinal sonogram of cecum. Patient is 57-year-old woman. acute appendicitis [1, 2]. On the other hand, CT
C, Bulky disease in cecum in 63-year-old woman. Axial sonogram reveals large eccentric hypoechoic mass with has shown sensitivities of 90100% with speci-
compression of hyperechoic lumen.
D, Isolated mucosal involvement in 43-year-old man. Transverse sonogram of ileum with marked hyperechoic gy-
ficities of 8398% [2830]. In one study with a
ral thickening of mucosa and preserved layering of bowel wall. low (76%) sensitivity for sonography, CT was
found to be more accurate than sonography in
the diagnosis of acute appendicitis [28].
caused by extraluminal involvement [18] (Fig. bowel [23]. The most commonly involved Graded compression sonography gained wide-
5C). Mesenteric tumor spread and bulky tumor nodal groups in non-Hodgkins lymphoma of spread acceptance as a useful technique to
growth need biopsy for definite diagnosis be- the gastrointestinal tract are the celiac, retro- examine patients with atypical signs of appen-
cause they cannot be reliably differentiated crural, perirenal, perisplenic, perihepatic, and dicitis [31]. In a prospective study, the pro-
from other diseases such as primary bowel tu- mesenteric nodes [22]. posed treatment after clinical examination
mors or metastases. Isolated mucosal in- changed in 26% of all patients after sono-
volvement is rare and leads to hyperechoic graphic examination [2]. The diagnosis can be
thickening of the mucosa (Fig. 5D). Sono- Acute Terminal Ileitis established with confidence if the appendix is
graphic patterns favoring the diagnosis of a The clinical symptoms of acute ileitis are noncompressible, shows no peristalsis, and
non-Hodgkins lymphoma over adenocarci- right-sided lower abdominal pain, diarrhea, measures more than 6 mm in diameter [32] on
noma are transmural circumferential, pro- and nausea, with an accelerated erythrocyte axial images, and if compression leads to a lo-
foundly hypoechoic wall thickening with sedimentation rate, positive C-reactive protein, calized pain response. The surrounding mesen-
preserved peristalsis; lack of intestinal obstruc- and leukocytosis. Only careful evaluation in tery is often inflamed, which can be seen as a
tion, because narrowing of the lumen is un- the preoperative workup for suspected appen- hyperechoic diffuse halo sign around the ap-
common; involvement of a long stretch of the dicitis can prevent an unnecessary operation pendix (Fig. 6A). If an appendicolith is identi-
gut; and the presence of multiple prominent [24]. Acute ileitis is caused by Yersinia species fied in an appendix of any size, the findings of
regional lymph nodes [22]. Typical complica- but Campylobacter and Salmonella species the examination are always considered positive
tions are mucosal ulceration leading in 10 may also be cultured. Reported sonographic [33] (Fig. 6C). A simple additional color Dop-
50% of patients to bleeding, perforation of the features include hypoechogenic mural thicken- pler examination may be helpful in the diagno-
small intestine, and intussusception of the ing of the terminal ileum and cecum between 6 sis of early acute appendicitis [34]. The
C D
presence of visible hyperemia or increased ficult to diagnose on sonography. Because CT amyloid is frequently seen [41]. Marked hypo-
flow in the hypoechoic muscular layer of the has been shown to be more accurate in staging echoic thickening of the affected bowel seg-
bowel wall may be a marker of appendicitis, periappendiceal inflammation and abscesses ments is found [42, 43].
whereas increased flow in the mucosal layer [5, 28, 36], CT may be preferred in patients Eosinophilic enteritis is a rare disease charac-
most likely represents enteritis [26]. Increased with suspected perforation or abscess; CT reli- terized by infiltration of the stomach or bowel
flow in the fat surrounding the appendix is in- ably differentiates phlegmon from abscess and wall with eosinophilic leukocytes. In three re-
dicative of transmural extension of the inflam- serves as an accurate road map for potential ported cases, hypoechoic thickening of multiple
mation with mesenteric response. An inflamed abscess drainage. ileal loops, narrowing of the lumen, and loss of
appendix rarely measures more than 15 mm in layer structure were described [44, 45].
transverse diameter [33], which usually allows Small-Bowel Diseases
differentiation from ileitis. A markedly en- Mesenteric infarction in its late stages
larged or perforating appendix or dilated fallo- leads to small-bowel wall thickening [37, 38].
pian tubes may lead to interpretive pitfalls [33]. In the early stages, however, no bowel wall
Perforation occurs in 2030% of young pa- thickening may be seen. Doppler sonography
tients with appendicitis (Fig. 6D). A statisti- can aid in differentiating ischemic and in-
cally significant association exists between flammatory bowel wall thickening. In ap-
perforation and two sonographic findings: loc- proximately 90% of cases, small-bowel
ulated pericecal fluid and loss of the echogenic infarctions are due to arterial hypoperfusion;
submucosa [35]. Abscess formation is the ma- only 10% are caused by mesenteric vein oc-
jor complication of perforating appendicitis. clusion. Acute intramural intestinal he-
Abscesses may extend into the pelvis or into matoma leads typically to a homogeneous
the peritoneal spaces of the upper abdomen. hypoechoic symmetric thickening of a long
They may be sonolucent or appear as a com- stretch of the affected bowel segment, with
plex mass. Advantages of sonography are wide reduced or absent peristalsis and marked lu-
availability, lack of radiation, and lack of con- minal narrowing [39] (Fig. 7). In the subacute Fig. 7.72-year-old woman with intramural hematoma
trast administration. Limitations of sonogra- stage, strong internal echoes caused by due to anticoagulant drug therapy. Patient was sent for
phy occur in obese and extremely meteoristic sonography to rule out atypical appendicitis. Trans-
thrombi may mimic an abscess [40]. verse sonogram of small-bowel segment discloses cir-
patients and in patients with severe pain due to Amyloidosis is a rare condition; however, cumferential hypoechoic thickening of bowel wall with
peritonitis. Retrocecal appendicitis may be dif- gastrointestinal involvement in patients with loss of stratification and compression of lumen.
A B C
Fig. 8.50-year-old man with Whipples disease (intestinal lipodystrophy) presenting with steatorrhea.
A, Longitudinal sonogram depicts marked hyperechoic jejunal fold thickening.
B, Transverse sonogram shows jejunal thickening and hyperechoic lobulated lymph node (arrow ).
C, CT scan shows prominent jejunal folds and enlarged mesenteric lymph nodes. (Courtesy of Disler M, Kantonsspital Liestal, Switzerland)
The sonographic features of primary lym- may lead to irregular wall thickening with the the distal ileum (Fig. 9). All small-bowel carci-
phangiectasia have been described in four pa- typical contraction of several bowel loops to a noids are considered malignant because they
tients [46, 47]. Diffuse hypoechoic small-bowel conglomerate. Most frequent primary tumors eventually grow, invade, and metastasize. Me-
wall thickening, ascites, mesenteric edema, and originate from the ovary, stomach, colon, pan- tastases will occur in 10% of lesions smaller
thickened walls of the gallbladder and urinary creas, gallbladder, lung, and uterus. Primary than 1 cm and 95% of lesions larger than 2 cm
bladder are found. small-bowel tumors constitute only 36% of [53]. Only 4% of patients present with the typi-
One case report describes the sonographic gastrointestinal neoplasms. Abdominal symp- cal carcinoid syndrome [54]. In a series of six
findings of nontropical sprue (celiac disease) toms are usually vague and poorly defined, and patients, small bowel carcinoids presented as
as diffuse hypoechoic thickening of the entire conventional radiography of the upper and hypoechoic, homogeneous predominantly
small-bowel wall that disappears completely lower intestinal tract often has normal results. intraluminal masses with smooth intralumi-
after 3 months of a gluten-free diet [48]. These factors may lead to a delayed diagnosis. nal contour [54]. The tumors were attached to
Sonographic findings in a patient with Carcinoid tumor is the most frequent small- the wall by a broad base, with interruption of
Whipples disease (intestinal lipodystrophy) bowel tumor [52] and occurs in 80% of cases in the submucosa and thickening of the muscularis
disclosed hyperechoic concentric thickening
of the small bowel with enlarged hyper-
echoic lymph nodes [49]. The hyperechoic
structure of the intestinal wall and the en-
larged lymph nodes are explained by fat ac-
cumulation in these structures [50] (Fig. 8).
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 pseudokid-
ney appearance was found in a patient suffer-
ing from intestinal Behets disease [21].
Cytomegalovirus enteritis in AIDS patients
leads to wall thickening of the small and
large bowels with preserved stratification. A B
Fig. 9.57-year-old man with ileal carcinoid tumor presenting with mechanical small-bowel obstruction.
Tumors of the Small Intestine Other A, Transverse sonogram of terminal ileum reveals hypoechoic, homogeneous intraluminal mass with smooth in-
Than Lymphomas traluminal contour and broad-based hypoechoic infiltration of submucosa posteriorly. Note fluid-distended
small-bowel segments ventral to tumor, indicating mechanical obstruction.
Peritoneal carcinomatosis is the most fre- B, CT scan reveals strongly enhancing mass (arrow ) in terminal ileum, with infiltration of mesenteric fat dorsally
quent malignant lesion of the small bowel and and mechanical obstruction of small bowel.
propria in all cases. Carcinoid tumors of the ap- Colitis 10B), intramural or pericolic abscess (Fig.
pendix were described in two cases [55] as hy- The sonographic features of pseudomembra- 10C), and (usually) severe local tenderness in-
poechoic, well-delineated elongated masses in nous colitis have been described in a number of duced by graded compression. Diverticula are
the distal lumen and the tip of the appendix. reports [61, 62]. Striking thickening of the co- round or oval echogenic foci seen in or right
Lipomas are the second most common tumors lonic wall with a wide inner circle of heteroge- next to the gut wall, mostly with internal
of the small intestine and occur with greatest fre- neous medium echogenicity surrounded by a acoustic shadowing. Thickening of the bowel
quency in the distal ileum and at the ileocecal wall is usually considered present when the
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A B C
Fig. 10.Sonographic features of diverticulitis.
A, Diverticulum of sigmoid colon in 63-year-old man is seen as focal hyperechoic intramural structure with acoustic shadow.
B, Massive hyperechoic inflammatory infiltration in 76-year-old woman is seen on mesenteric side of sigmoid colon.
C, Echolucent fistula in 67-year-old woman is seen in mesentery with small, hyperechoic, gas-containing abscess (arrow ).
scesses with gas inclusions [69]. CT is more colonic obstruction. Rectum carcinomas are inal sonography is not an effective screening
accurate than sonography in revealing ab- seen only when the bladder is well-filled (Figs. technique in the diagnosis of colonic cancer.
scesses [5, 28, 36] and is helpful in planning 11B and 11C). Sonography enables localiza-
percutaneous drainage by exactly delineating tion of large-bowel obstruction in 85% of Intussusception
the bowel loops [5]. patients and diagnosis of the cause of large- Only 510% of all intussusceptions occur in
bowel obstruction in 81% of patients [76]. adults [78, 79]. The clinical symptoms may sug-
Colonic Carcinoma Shirahama et al. [77] described four sono- gest partial obstruction of the intestine, but diag-
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Abdominal sonography may be the first im- graphic patterns that allowed correct diagnosis nosis may be difficult because symptoms are
aging method that patients with colonic cancer of colonic carcinoma in 90% of patients: local- often nonspecific [79]. The ileocecal region is
undergo when they present with nonspecific ized irregular thickening of the colonic wall the most commonly affected area in children,
gastrointestinal symptoms. Careful sono- with heterogeneous low echogenicity; irregu- whereas there is no clearly preferred anatomic
graphic evaluation of the bowel may disclose a lar contour; lack of movement or change in site in adults. Most intussusceptions in children
focal mass or mural thickening. Sonographic configuration on real-time scanning; and ab- are idiopathic and are presumed to be the result
diagnosis of colonic carcinoma has been de- sence of a layered appearance of the colonic of enlarged lymphoid follicles in the terminal il-
scribed by several authors [7274]. Colonic wall. Other findings include lymphadenopathy eum. An organic cause can be shown in as many
carcinomas have two typical sonographic ap- in most patients and abscess formation in 10% as 90% of cases in adults [78, 79]. The leading
pearances [75]. The first type is seen as a local- of patients. In a recent publication, malignant mass is nearly always a tumor of the intestinal
ized hypoechoic mass up to 10 cm or more conditions of the colon showed the following wall, usually malignant in intussusceptions of
with an irregular shape and a lobulated con- characteristics: loss of stratification, absence of the colon [80] and benign in intussusceptions of
tour. The intraluminal gas, seen as a cluster of perigut findings, and involvement of a short the small intestine [57, 78]. The sonographic
high amplitude, is usually eccentrically located bowel segment with significantly greater wall hallmark of intussusception has been described
around the mass (Fig. 11A). The second type thickness than is present in benign processes as the target [81], doughnut, or bulls-eye
shows segmental eccentric or circumferential [62]. However, negative findings on sono- sign [82]. Typically, one finds two hypoechoic
thickening of the colonic wall. The mural graphic examinations do not rule out the diag- rings separated by a hyperechoic ring or crescent
thickening may be irregular but not as severe nosis of colonic carcinoma because small on axial images (Fig. 12). On longitudinal im-
as in the first type (Fig. 11B). The central echo masses and overlying bowel gas can lead to ages, a pseudokidney structure or layering of hy-
clusters are small because the diseased lumen false-negative results [72, 76]. Because of poechoic lines with hyperechoic areas is
is usually narrow. This type leads frequently to these limitations, mainly in sensitivity, abdom- observed. The outer hypoechoic ring is formed
A B C
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