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Emergency Radiology

https://doi.org/10.1007/s10140-019-01670-7

REVIEW ARTICLE

Beyond appendicitis: ultrasound findings of acute bowel pathology


Jihee Choe 1 & Jeremy R. Wortman 2 & Aya Michaels 3 & Asha Sarma 4 & Urvi P. Fulwadhva 2 & Aaron D. Sodickson 1

Received: 16 December 2018 / Accepted: 3 January 2019


# American Society of Emergency Radiology 2019

Abstract
Bowel pathology is a common unexpected finding on routine abdominal and pelvic ultrasound. However, radiologists are often
unfamiliar with the ultrasound appearance of the gastrointestinal tract due to the underutilization of ultrasound for bowel
evaluation in the USA. The purpose of this article is to familiarize radiologists with the characteristic ultrasound features of a
variety of bowel pathologies. Basic ultrasound technique for bowel evaluation, ultrasound appearance of normal bowel, and key
ultrasound features of common acute bowel abnormalities will be reviewed.

Keywords Ultrasound . Emergency . Bowel . Abdominal pain

Introduction patient preparation, low cost, and capability of provid-


ing real-time information; however, drawbacks include
Acute abdominal pain is one of the most common clin- operator dependence and limited ability to evaluate
ical presentations in the Emergency Department (ED) as obese patients.
well as in the outpatient setting, accounting for 8% of Characteristic features of abnormal bowel, such as wall
all ED visits in the USA in 2014 and 1.5% of outpa- thickening, decreased motility, absence of luminal content,
tient visits in the USA in 2015, the most recent years and a fluid-filled distended lumen, can be readily detected
for which published data are available [1, 2]. Imaging by ultrasound; however, these findings may be unfamiliar to
evaluation of acute abdominal pain largely depends on radiologists who are more accustomed to using CT for assess-
the differential diagnosis generated after a thorough ment of the bowel. Bowel findings may be the only explana-
evaluation of the patient’s symptoms, physical examina- tion for abdominal pain on abdominal or pelvic ultrasound
tion, and laboratory testing are obtained. Ultrasound is exams. Therefore, familiarity with basic ultrasound scanning
frequently the first examination performed in the evalu- technique for bowel evaluation and characteristic ultrasound
ation of patients with nonspecific abdominal pain, par- features of normal bowel and bowel pathologies is essential.
ticularly in patients with right upper quadrant pain or in
female patients in whom a gynecologic etiology is
suspected. Ultrasound has the advantages of wide acces- Bowel ultrasound technique
sibility, lack of ionizing radiation, lack of need for
Ultrasound evaluation of bowel should be performed
with graded compression, which can significantly in-
* Jihee Choe crease sensitivity for bowel pathology [3]. Compression
jchoe@partners.org should be applied in a graded fashion to minimize pain,
similar to gentle palpation on physical examination [3].
1
Department of Radiology, Brigham and Women’s Hospital and Graded compression displaces bowel contents, fecal ma-
Harvard Medical School, Boston, MA, USA terial, and gas, which commonly obscure the area of
2
Department of Radiology, Lahey Hospital and Medical Center, interest. It also decreases distance between the area of
Burlington, MA, USA interest and the ultrasound probe, improving spatial res-
3
Department Radiology, Weill Cornell Medicine, New York, NY, olution [3]. In female patients, a transvaginal transducer
USA may be used to assess bowel pathologies in the deep
4
Department of Radiology and Radiological Sciences, Vanderbilt pelvis, such as distal sigmoid diverticulitis or appendici-
University School of Medicine, Nashville, TN, USA tis in an unusual deep location.
Emerg Radiol

General principles of bowel ultrasound decreased peristalsis can help to confirm true luminal
narrowing. In small bowel obstruction, small bowel
Ultrasound features that help distinguish normal from abnormal loops are dilated and typically measure greater than
bowel include wall layers, wall thickness, luminal diameter, 3 cm in diameter [7].
peristalsis, compressibility, vascularity, perienteric/pericolonic Real-time imaging by ultrasound can identify alter-
fat inflammatory changes, and associated enlarged lymph ations in peristalsis. Absent or diminished peristalsis is
nodes. seen in various disease states, including but not limited
Normal bowel on ultrasound is characterized by the to bowel ischemia, infection, inflammation, and malig-
wall stratification Bgut signature^ sign, in which five dis- nancy. Hyperperistalsis is frequently observed in small
tinct wall layers can be visualized (Fig. 1). Familiarity bowel obstruction and celiac disease [6, 8].
with the Bgut signature^ sign allows one to recognize Normal bowel should be easily compressible by transducer
bowel and distinguish it from other structures on ultra- pressure. Lack of compressibility may indicate diseased bow-
sound. Loss of the typical gut signature pattern is consid- el, as in appendicitis, intussusception, bowel malignancy, and
ered a sign of diseased bowel. luminal distention from obstruction.
The average bowel wall thickness on ultrasound is Color or power Doppler can provide additional infor-
2–4 mm for small bowel and up to 5 mm for large bowel. mation about increased vascularity in inflammatory dis-
The gastric wall is usually thicker and measures up to ease and solid masses. It is difficult to obtain Doppler
5–6 mm [4]. The wall thickness is measured from the signal in the normal bowel wall, as it is thin and compli-
central hyperechoic line of the lumen to the outer ant, with peristaltic activity [9, 10]. Decreased vascularity
hyperechoic margin of the wall [5]. Bowel wall thicken- in thickened bowel wall is highly suggestive of bowel
ing is the most common finding of bowel pathology, but wall ischemia in certain clinical settings, although it is
is nonspecific. Evaluation of the symmetry, degree, and not a sensitive finding [11, 12].
distribution of wall thickening can help in determining the Inflammatory changes increase the echogenicity of the
cause of bowel wall thickening. perienteric/pericolonic fat in various infectious and in-
Assessment of the caliber of the bowel lumen is im- flammatory bowel disease, whereas normal perienteric/
portant in the evaluation for bowel pathology. Luminal pericolonic fat is generally inconspicuous. Enlarged
narrowing can be seen in various conditions, such as lymph nodes are also a sign of bowel inflammation and
inflammatory bowel disease [6] and neoplasm, and at bowel malignancies and can commonly be visualized
transition points in cases of small bowel obstruction. It sonographically (Table 1).
may be difficult to distinguish luminal narrowing from
transiently contracted bowel segments; in this situation,
other associated findings such as wall thickening or Appendicitis

Ultrasound and CT are the most commonly used modali-


ties for diagnosing appendicitis. The decision to obtain
ultrasound or CT depends on operator experience, patient
age and body habitus, and institutional preference [13].
The major advantage of ultrasound over CT is lack of
radiation exposure, making ultrasound an ideal initial di-
agnostic imaging test for young patients with normal
BMI. Ultrasound has proven diagnostic value in acute
appendicitis, with reported sensitivity and specificity of
78–99 and 83–99%, respectively [14–17], and accuracy
of 70 to 99% [15–18].
Sonographic evaluation of appendicitis starts with
identifying the ascending colon and cecum, which is
achieved by scanning from the tip of the liver to the pel-
Fig. 1 The normal five distinct layers of bowel wall on ultrasound, also vic brim in the transverse plane, with several sweeps from
referred as the Bgut signature^ sign. The innermost hyperechoic layer the lateral to the medial aspect of the right lower quadrant
(pink) represents the interface between the mucosa and bowel contents. [13]. The ascending colon and cecum are nonperistaltic
The second, hypoechoic layer (peach) is the deep mucosa and third,
hyperechoic layer (green) is the submucosa. The fourth, hypoechoic
and can be distinguished from adjacent small bowel as a
layer (cyan) represents the muscularis propria and the outermost, gas-filled viscus with dirty shadowing and a Bbumpy^
hyperechoic layer (orange) represents the serosa and serosal fat outer contour. The terminal ileum is then identified as a
Emerg Radiol

Table 1 General principles of bowel ultrasound

Wall stratification/Bgut signature^ sign - Five distinct layers of the bowel wall can be visualized
- Loss of the typical gut signature pattern is a sign of diseased bowel
Wall thickness - The average thickness of small bowel wall on ultrasound is 2–4 mm and up to 5 mm for large bowel
- Wall thickening is the most common finding of bowel pathology
Luminal diameter - Luminal narrowing can be seen in various bowel abnormalities
- Dilated small bowel loops (>3 cm) can be found in small bowel obstruction
Peristalsis - Absent or diminished peristalsis is seen in various bowel diseases
- Hyperperistalsis is frequently observed in small bowel obstruction and celiac disease
Compressibility - Normal bowel should be easily compressible by transducer pressure
- Lack of compressibility may be evident in various causes of diseased bowel
Vascularity - Color or power Doppler can provide information about increased vascularity in inflammatory diseases
and suspicious solid masses
- Decreased vascularity in thickened bowel wall is highly suggestive of bowel wall ischemia in certain
clinical settings, although this is not a sensitive finding
Inflammation of adjacent fat - Inflammatory changes increase the echogenicity of the perienteric/pericolonic fat

compressible, peristalsing loop of bowel caudal to the identified in a patient with suspected appendicitis, ultrasound
ascending colon. The appendix typically arises from the is 65% sensitive and 86% specific for the diagnosis of appen-
posteromedial aspect of the cecum near the ileocecal dicitis [21]. Inflamed, hyperechoic periappendiceal fat is of-
valve in any direction, 1–2 cm below the terminal ileum. ten evident. Phlegmonous change appears as a hypoechoic
It is difficult to visualize a retrocecal appendix with a area with poor margination [22]. Periappendical abscess man-
standard anterior approach. The retrocecal appendix is ifests as an organized fluid collection with mass effect.
best identified via a lateral flank approach with the trans- Reactive enlarged mesenteric lymph nodes and reactive wall
ducer positioned adjacent to the cecum or ascending colon thickening and edema of the cecum near the base of the
[19]. An appendix in the deep pelvis may also be difficult appendix can be seen.
to identify with transabdominal scanning and is best seen Diagnostic pitfalls of appendicitis evaluation with ultra-
with transvaginal scanning in female patients. Another sound include perforated appendicitis and tip appendicitis.
approach to identifying the appendix in suspected appen- Compared to CT, an important limitation of ultrasound in
dicitis is to start by scanning in the area of the patient’s the evaluation of appendicitis is lower sensitivity and speci-
localized maximum tenderness, which can be helpful in ficity for perforated appendicitis. In a case of perforated ap-
identifying an aberrantly located appendix and reducing pendicitis, the appendix may appear normal in diameter be-
the duration of the examination in positive cases. When cause the appendix is often decompressed when perforated
the patient can decisively localize the site of maximal [13]. An inflamed appendix is identified by ultrasound in only
pain, there is a significant finding 95% of the time [20]. 38–55% of patients with perforated appendicitis [23, 24].
Eighty-five percent of patients with appendicitis are able Identification of secondary signs of a perforated appendix,
to self-localize the pain [20]. such as loculated fluid, phlegmon, or abscess, can be helpful
The normal appendix is seen as a tubular, blind-ending, clues for the diagnosis of perforated appendicitis and should
nonperistaltic structure that originates from the cecum. It increase suspicion (Fig. 2c) [25]. When inflammation is lim-
should be compressible and should measure less than 6 mm ited to the distal tip, the proximal appendix appears normal,
in diameter when compressed (Fig. 2a). The inflamed appen- which may lead to a false-negative exam. Therefore, it is im-
dix is noncompressible, immobile, and dilated to greater than portant to follow the appendix along its whole length and to
6 mm in diameter (Fig. 2b). The measurement of the appen- visualize the blind end as a part of every sonographic evalua-
dix should be taken in the anteroposterior dimension from tion of the appendix [26]. Rarely, the inflamed appendix can
outer wall to outer wall with full compression. Doppler ultra- get quite enlarged and be mistaken for small bowel due to its
sound may show hyperemia in the wall of the appendix as unusually large caliber [9].
supporting evidence of inflammation. An appendicolith may
be seen as a discrete echogenic focus with acoustic
shadowing in the lumen of appendix. While an appendicolith Infectious colitis
may occasionally be an incidental finding, the presence of an
appendicolith in a patient with acute abdominal pain and Infection is the most common cause of colitis. Infectious co-
suspected appendicitis is regarded as a highly specific finding litis can be bacterial, fungal, viral, or amebic in etiology. Most
for the diagnosis of appendicitis. When an appendicolith is of the causes of infectious colitis share similar ultrasound
Emerg Radiol

Fig. 2 a Normal appendix. Ultrasound image shows a normal appendix, (arrows). c Perforated appendicitis in a 10-year-old male with abdominal
which is seen as a tubular, blind-ending structure (arrow). The normal pain. Ultrasound image shows a blinding-ending tubular structure origi-
appendix should be compressible and should measure less than 6 mm in nating from the cecum measuring up to 1.1 cm in diameter (arrowheads),
diameter. b Appendicitis in a 15-year-old male with abdominal pain. A consistent with an inflamed appendix. There is discontinuity in the tip of
sonographic image of the right lower abdomen demonstrates a dilated the appendix (arrow) with surrounding extensive inflammatory changes
appendix that measures 1.0 cm in diameter (arrowheads) with at least (asterisk), concerning for perforated appendicitis, which was confirmed
two appendicoliths within the proximal and distal aspects of its lumen with subsequent CT

features of colonic wall thickening (> 5 mm) and pericolonic Pronounced wall thickening of the colon is present in most
fat inflammatory changes (Fig. 3). Ascites may or may not be cases of pseudomembranous colitis when compared with oth-
present. Because the normal colonic wall is not well visualized er types of colitis; however, definitive diagnosis is made with
sonographically, any visibly thickened wall should raise clin- stool assay for C. difficile toxin. Wall thickening represents
ical suspicion for colitis. In general, when wall thickening is severely edematous submucosa and mucosa, giving the
present, the affected segment of colon becomes much easier to Baccordion^ sign or Bgyral^ pattern (Fig. 4) [28, 29]. Wall
visualize. thickness ranges from 10 to 30 mm [28, 30]. Wall stratification
Since there is considerable overlap of appearance among is usually preserved despite increased wall thickness [30].
various causes of infectious colitis, specific diagnosis can only
be made with clinical history and laboratory testing. The dis-
tribution and site of a colonic abnormality may suggest a spe- Typhlitis
cific infectious agent. Cytomegalovirus and Escherichia coli
most commonly cause pancolitis, and Yersinia, Salmonella, Typhlitis is also known as neutropenic enterocolitis and occurs
and tuberculosis mainly affect the right colon. Colitis caused most commonly as a complication of neutropenia in a patient
by schistosomiasis, shigellosis, herpes, gonorrhea, syphilis, receiving chemotherapy. It was first described in children with
and lymphogranuloma venereum is usually left-sided [27]. acute leukemia treated with induction therapy [31]. It is a
necrotizing inflammatory disease mainly affecting the cecum
and often extending into the ascending colon and terminal
Pseudomembranous colitis ileum [32]. Predilection for the cecum may be related to its
specific anatomic characteristics, including vascular supply
Pseudomembranous colitis is a type of colitis caused by toxins from terminal branches of the superior mesenteric artery, high
produced by Clostridium difficile bacteria in the colon, usually concentration of lymphatic tissue, distensibility, and relatively
as a complication of antibiotic therapy and resultant bacterial static intraluminal contents [33, 34]. It may also occur in pa-
overgrowth [28]. It is also associated with abdominal surgery, tients with other immunosuppressive conditions who are not
prolonged hypotension, colonic obstruction, and uremia. on chemotherapy. Pathogenesis of typhlitis is not completely
Pseudomembranous colitis is most commonly a pancolitis. understood, but multiple factors severely damage the mucosa,

Fig. 3 Colitis in a 34-year-old


female with abdominal pain. a
Longitudinal and b transverse
sonographic images of the right
lower abdomen demonstrate wall
thickening of the cecum
(arrowheads) with adjacent
echogenic fat suggesting
inflammation (asterisk)
Emerg Radiol

Fig. 4 Pseudomembranous colitis


in a 2-year-old female.
Ultrasound images (a, b)
demonstrate diffuse marked wall
thickening of the large bowel
loops (arrowheads) with marked
submucosal edema (asterisk).
There is small ascites (arrows)

resulting in marked intramural edema and hemorrhage. The Diverticulitis develops due to microperforation of a diverticu-
severity of typhlitis ranges from mild gastrointestinal symp- lum when its neck is obstructed by a fecalith, stool, or inflam-
toms to sepsis with a potentially lethal outcome. The key matory edema [37].
ultrasound feature of bowel wall thickening is not specific Ultrasound has been demonstrated to have high sensi-
for typhlitis; however, the diagnosis should be suspected when tivity and specificity in diagnosing diverticulitis, with re-
wall thickening involves the cecum in a neutropenic patient ported sensitivity and specificity of 77–98 and 80–99%,
(Fig. 5) [35]. Other entities such as Crohn’s disease and infec- respectively [38–41]. Ultrasound features of diverticulitis
tious colitis caused by Yersinia, Salmonella, and tuberculosis include the presence of diverticula with associated colonic
commonly affect the right colon and should also be consid- wall thickening and inflammatory changes in the
ered in the differential diagnosis; however, clinical history and pericolonic fat (Fig. 6). A normal diverticulum presents
presentation usually allow distinction among these entities. as a thin-walled round or oval hyperechoic focus that
protrudes from the colonic wall, with focal disruption of
the normal layer continuity and posterior acoustic
Colonic diverticulosis/diverticulitis shadowing of variable intensity that is thought to arise
from air, feces, or enteroliths [37, 42]. An inflamed diver-
Colonic diverticulosis is characterized by herniation of the ticulum will be thick-walled [6], with inflamed surround-
mucosa and submucosa through an area of weakness in the ing pericolonic fat that is echogenic and thickened.
muscle layer of the bowel wall and mainly occurs in the distal Diverticulitis is considered complicated when it is associ-
colon, with only 15% involving the right colon [36]. ated with bowel obstruction, free air, abscess formation,

Fig. 5 Typhlitis in a 21-year-old


patient with acute lymphocytic
leukemia on chemotherapy (a–c).
The walls of the ascending colon
and cecum are markedly
thickened (arrowheads), with
power Doppler demonstrating
increased blood flow (curved
arrow). The lumen of the bowel is
narrowed (arrow)
Emerg Radiol

Fig. 6 Diverticulitis in a 44-year-


old female with abdominal pain.
Transverse (a) and longitudinal
(b) sonographic images in the
region of the patient’s maximal
tenderness (in the left lower
quadrant) demonstrate an
enlarged, inflamed diverticulum
(arrows) associated with colonic
wall thickening (letter C).
Associated hyperechoic
pericolonic fat is present
(asterisk), suggesting
inflammation

and fistula formation to adjacent structures such as blad- inflamed Meckel’s diverticulum may mimic appendicitis, as
der, vagina, skin, or other bowel loops. it may be noncompressible [48]. When it is compressible, it
may resemble a duplication cyst due to the presence of gut
signature sign in both entities; however, an inflamed Meckel’s
Meckel’s diverticulitis diverticulum will have an irregular internal wall, compared
with the smooth internal wall of a duplication cyst [49].
Meckel’s diverticulum is the most common congenital anom-
aly of the gastrointestinal tract, caused by failure of regression
of the omphalomesenteric duct. The omphalomesenteric duct Crohn’s disease
connects the yolk sac to the midgut through the umbilical cord
and typically is obliterated by the fifth to eighth week of ges- Crohn’s disease is an inflammatory bowel disease character-
tation [43]. Most Meckel’s diverticula are found within 40– ized by a chronic course with multiple episodes of remission
100 cm of the ileocecal valve and arise from the anti- and exacerbation. It can involve any portion of the gastroin-
mesenteric border of the distal small bowel [44]. They are testinal tract from the mouth to the anus, most often with ileal
present in approximately 2% of the population. On ultrasound, and/or colonic involvement. Granulomatous inflammation is
the Meckel’s diverticulum appears as a blind-ending, fluid-
filled tubular structure with typical gut signature that is con-
nected to a normal, peristaltic small bowel loop. Gut signature
sign helps to confirm origin from bowel. Enteroliths are pres-
ent in 10% of cases and are visualized as shadowing
echogenic foci [45].
Most affected patients remain asymptomatic during their
lifetime, but complications occur in 4–40% [43]. The most
common complications include bleeding, bowel obstruction,
diverticulitis, and intussusception. Hemorrhage is the most
frequent complication of Meckel’s diverticulum in the pediat-
ric population and is caused by peptic ulceration from hetero-
topic gastric and pancreatic mucosa [46]. Technetium-99m
pertechnetate scintigraphy is the imaging modality of choice
for evaluating pediatric patients presenting with gastrointesti-
nal hemorrhage from a suspected Meckel’s diverticulum [47].
Intestinal obstruction is the second most common complica-
tion of Meckel’s diverticulum, and the diagnosis of Meckel’s
diverticulum is most often made perioperatively. A Meckel’s Fig. 7 Meckel’s diverticulitis in a 6-year-old male with episodic, diffuse
diverticulum can become inflamed secondary to acid secretion abdominal pain for 3 days. A transverse sonographic image demonstrates
from ectopic gastric mucosa or due to obstruction by a blind-ending loop of bowel in the midline pelvis (arrow), with a mildly
thickened, slightly irregular wall (arrowheads). There is associated mild
enteroliths, foreign bodies, or neoplasms [43]. Ultrasound hyperemia within the wall with adjacent fat stranding (asterisk) and trace
signs of Meckel’s diverticulitis include thickened wall and free fluid (curved arrow). The finding of Meckel’s diverticulitis was
increased wall vascularity of the diverticulum (Fig. 7). An confirmed with CT and the patient was taken to surgery
Emerg Radiol

transmural and segmentally distributed, with skip areas and and resolves after inflammation subsides [56]. Reactive mes-
bowel wall thickening. Deep fissures, sinuses, and fistulas are enteric adenopathy is frequently seen in Crohn’s disease dur-
seen in advanced disease. Strictures occur in longstanding ing active as well as chronic intestinal inflammation.
disease and result from edema, inflammation, and ultimately
fibrosis and scarring [22].
Ultrasound has proven to be of value in detecting Crohn’s Intussusception
disease with reported sensitivity of 88% and specificity of
97% [50]. The most common sonographic finding of Intussusception is a condition in which a segment of the in-
Crohn’s disease is bowel wall thickening. A meta-analysis testine (intussusceptum) invaginates into an adjacent distal
evaluating different cutoff values for bowel wall thickness loop of intestine (intussuscipiens). It is much more common
showed that sensitivity and specificity of ultrasound in detect- in children than adults. In children, intussusception is most
ing Crohn’s disease were 88 and 93%, respectively, when the often caused by hypertrophied lymphoid follicles in the distal
bowel wall measured > 3 mm, and sensitivity and specificity ileum (considered a Bnonpathologic^ lead point); therefore,
were 75 and 97%, respectively, when a cutoff of 4 mm was ileocolic intussusception is the most common type.
used [51]. The echotexture of the thickened wall in Crohn’s Pathologic lead points are identified in 75 to 85% of cases of
disease is variable. Normal stratification can occasionally be adult intussusception [57]. In adults, 50% of colocolonic in-
maintained or may be lost partially or completely [6]. In cases tussusceptions are caused by malignant tumors, whereas the
with maintained stratification, variable enlargement of the mu- majority of small bowel intussusception lead points are benign
cosal, submucosal, or muscular layers is demonstrated [52]. lesions such as polyps [58, 59]. The classic presentation of
The typical gut layering can be lost secondary to transmural intussusception includes colicky abdominal pain, vomiting,
inflammation, edema, and fibrosis, resulting in a thick and the presence of Bcurrant jelly^ stool in a pediatric patient.
hypoechoic rim and the Btarget^ sign. The Btarget^ sign is This presentation is rare in adults, most of whom present with
the classic ultrasound feature of Crohn’s disease, seen as a vague abdominal pain [60].
hypoechoic rim of moderate to marked concentric wall thick- Reported sensitivity and specificity of ultrasound in diag-
ening with central echogenic bowel contents within the nosing intussusception are close to 100% in the pediatric pop-
narrowed lumen. The diseased bowel segment is relatively ulation [61]. Ultrasound has also been shown to be a useful
rigid and noncompressible, with reduced or absent peristalsis imaging technique for detecting intussusception in adults [62].
in the small bowel and loss of haustra in the colon [22]. A four-quadrant survey including Doppler imaging is per-
Luminal narrowing results from gross inflammatory thicken- formed. The characteristic appearance of intussusception
ing of the bowel wall or fibrotic strictures [6]. Although these when viewed transversely on ultrasound includes the presence
findings are characteristic of Crohn’s disease, a number of of the Btarget,^ Bdoughnut,^ or Bbull’s-eye^ sign, character-
other conditions, including infectious, ischemic, neoplastic, ized by concentric hyperechoic and hypoechoic rings (Fig. 8)
and radiation-induced bowel disease, can have a similar ap- [58, 63]. The hypoechoic ring represents the edematous walls
pearance. Diagnosis of Crohn’s disease can be suggested of the intussusceptum and intussuscipiens, while the
when there is segmental, circumferential bowel wall thicken- hyperechoic ring represents areas of decompressed mucosa
ing that affects the terminal ileum along with evidence of [61]. The terms Bhay fork,^ Btrident,^ and Bpseudokidney^
complications of Crohn’s disease (e.g., abscess or fistula).
In Crohn’s disease, mucosal ulcerations may penetrate into
the submucosa, muscularis, serosa, and outside of the bowel
and lead to formation of fissures, fistulae, and sometimes
intra-abdominal or retroperitoneal abscesses [6, 52].
Intramural ulcerations or abscesses may be identified.
Ultrasound is a useful imaging technique for assessing fistu-
lae, with reported sensitivity and specificity of 80–100 and
92–94% [53–55]. A fistulous tract appears as a hypoechoic
tract containing bubbles of gas that extends from the bowel to
the adjacent structures [22]. Transmural inflammation leads to
perienteric edema and fibrosis involving the adjacent mesen-
tery that creep over the anti-mesenteric serosal surface of the
bowel, giving a Bcreeping fat^ appearance of a uniform
Fig. 8 Intussusception in a 2-year-old male with nonbloody, nonbilious
hyperechoic thick layer of fatty tissue with a mass-like appear- vomiting, and a tender, distended abdomen. A sonographic image
ance [22]. Fibrofatty proliferation is an indication of active demonstrates a classic Btarget^ appearance of intussusception in the
inflammation. It occurs rapidly during an acute flare of disease right lower quadrant (arrows)
Emerg Radiol

Lymphoma

Most bowel lymphomas are extranodal marginal zone B cell


lymphomas or diffuse large B cell lymphomas [65].
Lymphoma affects the stomach, small bowel, and large bowel
in decreasing order of frequency and can involve multiple
sites [66].
The appearance of bowel lymphoma on ultrasound is var-
iable. The most common ultrasound imaging appearance of
lymphoma is circumferential wall thickening with loss of nor-
mal stratification. The thickened wall can measure up to 4 cm.
Other patterns, such as nodular and mass-like tumor or, rarely,
isolated mucosal involvement, may also be seen (Fig. 9) [67].
Features that suggest the diagnosis of lymphoma over adeno-
carcinoma include associated mesenteric lymphadenopathy,
Fig. 9 Bowel lymphoma in a 15-year-old male with right lower quadrant preserved peristalsis, and absence of intestinal obstruction de-
pain and a history of Crohn’s disease. An ultrasound image with color spite the marked degree of wall thickening [68].
Doppler demonstrates mass-like wall thickening of the cecum and
terminal ileum in right lower quadrant (arrows) Colon cancer

sign describe the appearance of the intussusceptum and Adenocarcinoma is the most common malignancy of the gas-
intussuscipiens on longitudinal images [62, 64]. trointestinal tract and colon. On ultrasound, colonic adenocar-
cinoma appears as a short segmental thickening or as a bulky
mass of the colonic wall with heterogeneous low echogenicity
Malignancy [69]. Wall thickening may be eccentric or circumferential.
Central linear echoes may represent air in the residual
Ultrasound can depict various bowel neoplasms, such as lym- narrowed lumen [70]. There is a lack of demonstrable move-
phoma, gastrointestinal stromal tumor, colonic carcinoma, and ment or change of configuration of the bowel on real-time
metastatic disease. Although there is overlap between the ap- ultrasound scanning [71].
pearances of benign and malignant conditions of the bowel,
some ultrasound features are helpful in differentiating benign
and malignant conditions. Malignant conditions are more Small bowel obstruction
commonly associated with greater wall thickening, asymmet-
ric wall thickening, involvement of a short segment, loss of Small bowel obstruction is a common condition caused by
stratification, and absence of pericolonic findings such as as- interruption of normal flow of intraluminal contents that can
cites, fistula, abscess, and abnormally echogenic pericolonic be due to mechanical or functional causes. The most common
fat [30]. causes of mechanical small bowel obstruction are hernias and

Fig. 10 Small bowel obstruction


in an 84-year-old female with
diffuse abdominal pain, nausea,
and vomiting. Sonographic
images of the abdomen (a, b)
demonstrate multiple dilated
loops of small bowel
(arrowheads)
Emerg Radiol

postoperative adhesions. Other causes include neoplasms, Publisher’s note Springer Nature remains neutral with regard to juris-
dictional claims in published maps and institutional affiliations.
strictures, volvulus, intussusception, gallstones, and foreign
bodies. In a case of mechanical small bowel obstruction, small
bowel loops proximal to the obstruction are dilated and fluid-
filled and bowel loops distal to the obstruction are References
decompressed.
Ultrasound is a useful imaging technique for assessing
small bowel obstruction. Reported sensitivity and accuracy 1. Centers for Disease Control and Prevention. National Hospital
Ambulatory Medical Care Survey: 2014 Emergency department
of ultrasound in diagnosing bowel obstruction are 95 and >
summary tables. https://www.cdc.gov/nchs/data/nhamcs/web_
80%, respectively [72, 73]. The ability to perform ultrasound tables/2014_ed_web_tables.pdf. Accessed 27 Jan 2018
at the bedside allows for a quicker diagnosis for patients who 2. Centers for Disease Control and Prevention. National Ambulatory
present with nonspecific symptoms of nausea, vomiting, and Medical Care Survey: 2015 State and national summary tables.
https://www.cdc.gov/nchs/data/ahcd/namcs_summary/2015_
abdominal pain and can expedite treatment. Small bowel ob-
namcs_web_tables.pdf. Accessed 27 Jan 2018
struction is easily detected with ultrasound because fluid with- 3. Puylaert JB (1986) Acute appendicitis: US evaluation using graded
in the bowel proximal to the point of obstruction serves as a compression. Radiology 158:355–360
contrast medium and distends the bowel loops. Diagnosis of 4. Rapaccini GL, Aliotta A, Pompili M, Grattagliano A, Anti M,
small bowel obstruction is considered if multiple dilated (> Merlino B, Gambassi G (1988) Gastric wall thickness in normal
and neoplastic subjects: a prospective study performed by abdom-
3 cm) fluid-filled loops of small bowel are seen (Fig. 10) along inal ultrasound. Gastrointest Radiol 13:197–199
with decompressed distal bowel loops. Peristalsis is increased 5. Maconi G, Rigazio C, Ercole E (2014) Bowel ultrasound: investi-
in dilated bowel loops as they attempt to pass the luminal gation technique and normal findings. In: Maconi G, Porro GB
contents beyond the obstruction site [8]. Associated ascites (eds) Ultrasound of the gastrointestinal tract. Springer-Verlag,
Berlin, pp 1–6
is frequently visualized. Occasionally, causes of bowel ob- 6. Muradali D, Goldberg DR (2015) US of gastrointestinal tract dis-
struction such as hernia, tumor, and intussusception can be ease. Radiographics 35:50–70
detected using fluid-filled bowel as a sonographic window. 7. Nicolaou S, Kai B, Ho S, Su J, Ahamed K (2005) Imaging of acute
When strangulation or excessive bowel dilatation occurs, per- small bowel obstruction. AJR Am J Roentgenol 185(4):1036–1044
8. Lim JH (2014) Intestinal obstruction. In: Maconi G, Porro GB (eds)
fusion of the bowel may be compromised, leading to infarc- Ultrasound of the gastrointestinal tract. Springer-Verlag, Berlin, pp
tion, necrosis, and perforation and increased morbidity and 45–51
mortality associated with small bowel obstruction. Ischemia 9. Lim HK, Lee WJ, Kim TH, Namgung S, Lee SJ, Lim JH (1996)
is suggested by bowel wall thickening and decreased or absent Appendicitis: usefulness of color Doppler US. Radiology 201:221–
225
peristalsis [73, 74]. The presence of free fluid between dilated
10. Quillin SP, Siegel MJ (1994) Appendicitis: efficacy of color
small bowel loops suggests worsening mechanical small bow- Doppler sonography. Radiology 191:557–560
el obstruction and the need for surgical management [75]. 11. Danse EM, Van Beers BE, Jamart J et al (2000) Prognosis of ische-
mic colitis: comparison of color Doppler sonography with early
clinical and laboratory findings. AJR Am J Roentgenol 175:1151–
1154
Conclusion 12. Ripolles T, Simo L, Martinez-Perez MJ, Pastor MR, Igual A, Lopez
A (2005) Sonographic findings in ischemic colitis in 58 patients.
AJR Am J Roentgenol 184:777–785
Given its lack of ionizing radiation, widespread availability, 13. Birnbaum BA, Wilson SR (2000) Appendicitis at the millennium.
low cost, and ability to provide real-time information, ultra- Radiology 215:337–348
sound continues to play an important role in the evaluation of 14. Doria AS, Moineddin R, Kellenberger CJ, Epelman M, Beyene J,
acute abdominal pain. Currently, many radiologists limit the Schuh S, Babyn PS, Dick PT (2006) US or CT for diagnosis of
appendicitis in children and adults? A meta-analysis. Radiology
use of abdominal and pelvic ultrasound to solid organs. 241(1):83–94
However, ultrasound can be a valuable tool for assessment 15. Chan I, Bicknell SG, Graham M (2005) Utility and diagnostic ac-
of bowel diseases such as appendicitis, diverticulitis, colitis, curacy of sonography in detecting appendicitis in a community
Meckel’s diverticulitis, small bowel obstruction, neoplasm, hospital. AJR Am J Roentgenol 184:1809–1812
16. Lee JH, Jeong YK, Park KB, Park JK, Jeong AK, Hwang JC (2005)
and intussusception. Familiarity with normal and pathologic Operator-dependent techniques for graded compression sonogra-
ultrasound features of the bowel along with a good under- phy to detect the appendix and diagnose acute appendicitis. AJR
standing of ultrasound technique can facilitate early detection Am J Roentgenol 184:91–97
of bowel disease. 17. Rettenbacher T, Hollerweger A, Gritzmann N, Gotwald T,
Schwamberger K, Ulmer H, Nedden D et al (2002) Appendicitis:
should diagnostic imaging be performed if the clinical presentation
Compliance with ethical standards is highly suggestive of the disease? Gastroenterology 123:992–998
18. Kessler N, Cyteval C, Gallix B (2004) Appendicitis: evaluation of
Conflict of interest The authors declare that they have no conflict of sensitivity, specificity, and predictive values of US, Doppler US,
interest. and laboratory findings. Radiology 230:472–478
Emerg Radiol

19. Jeffrey RB Jr, Jain KA, Nghiem HV (1994) Sonographic diagnosis computed tomography in acute colonic diverticulitis: meta-
of acute appendicitis: interpretive pitfalls. AJR Am J Roentgenol analysis of test accuracy. Eur Radiol 18:2498–2511
162:55–59 42. Pradel JA, Adell JF, Taourel P, Djafari M, Monnin-Delhom E, Bruel
20. Chesbrough RM, Burkhard TK, Balsara ZN, Goff WB II, Davis DJ JM (1997) Acute colonic diverticulitis: prospective comparative
(1993) Self-localization in US of appendicitis: an addition to graded evaluation with US and CT. Radiology 205:503–512
compression. Radiology 187:349–351 43. Elsayes KM, Menias CO, Harvin HJ, Francis IR (2007) Imaging
21. Lowe LH, Penney MW, Scheker LE, Perez R Jr, Stein SM, Heller manifestations of Meckel's diverticulum. AJR Am J Roentgenol
RM, Shyr Y, Hernanz-Schulman M (2000) Appendicolith revealed 189(1):81–88
on CT in children with suspected appendicitis: how specific is it in 44. Satya R, O’Malley JP (2005) Meckel diverticulum with massive
the diagnosis of appendicitis? AJR Am J Roentgenol 175:981–984 bleeding. Radiology 236:836–840
22. Sarrazin J, Wilson SR (1996) Manifestations of Crohn disease at 45. Pantongrag-Brown L, Levine MS, Buetow PC, Buck JL, Elsayed
US. RadioGraphics 16:499–520 AM (1996) Meckel’s enteroliths: clinical, radiologic, and patholog-
23. Ooms HWA, Koumans RKJ, Ho Kang You PJ, Puylaert JB (1991) ic findings. AJR Am J Roentgenol 167:1447–1450
Ultrasonography in the diagnosis of acute appendicitis. Br J Surg 46. Fink AM, Alexopoulou E, Carty H (1995) Bleeding Meckel’s di-
78:315–318 verticulum in infancy: unusual scintigraphic and ultrasound appear-
24. Quillin SP, Siegel MJ, Coffin CM (1992) Acute appendicitis in ances. Pediatr Radiol 25:155–156
children: value of sonography in detecting perforation. AJR Am J 47. Levy AD, Hobbs CM (2004) From the archives of the AFIP.
Roentgenol 159:1265–1268 Meckel diverticulum: radiologic features with pathologic correla-
25. Borushok KF, Jeffrey RB Jr, Laing FC, Townsend RR (1990) tion. RadioGraphics 24:565–587
Sonographic diagnosis of perforation in patients with acute appen- 48. Baldisserotto M, Maffazzoni DR, Dora MD (2003) Sonographic
dicitis. AJR Am J Roentgenol 154:275–278 findings of Meckel’s diverticulitis in children. AJR Am J
26. Lim HK, Lee WJ, Lee SJ, Namgung S, Lim JH (1996) Focal ap- Roentgenol 180:425–428
pendicitis confined to the tip: diagnosis at US. Radiology 200:799–
49. Daneman A, Lobo E, Alton DJ, Shuckett B (1998) The value of
801
sonography, CT and air enema for detection of complicated Meckel
27. Thoeni RF, Cello JP (2006) CT imaging of colitis. Radiology 240: diverticulum in children with nonspecific clinical presentation.
623–638 Pediatr Radiol 28:928–932
28. Downey DB, Wilson SR (1991) Pseudomembranous colitis: sono-
50. Dong J, Wang H, Zhao J, Zhu W, Zhang L, Gong J, Li Y, Gu L, Li J
graphic features. Radiology 180:61–64
(2014) Ultrasound as a diagnostic tool in detecting active Crohn's
29. Danse E, Geukens D (2014) Pseudomembranous colitis. In: Maconi disease: a meta-analysis of prospective studies. Eur Radiol 24:26–
G, Porro GB (eds) Ultrasound of the gastrointestinal tract. Springer- 33
Verlag, Berlin, German, pp 155–159
51. Fraquelli M, Colli A, Casazza G et al (2005) Role of US in detection
30. Truong M, Atri M, Bret PM, Reinhold C, Kintzen G, Thibodeau M,
of Crohn disease: meta-analysis. Radiology 236(1):95–101
Aldis AE, Chang Y (1998) Sonographic appearance of benign and
52. Maconi G (2014) Crohn’s disease. In: Maconi G, Porro GB (eds)
malignant conditions of the colon. AJR Am J Roentgenol 170:
Ultrasound of the gastrointestinal tract. Springer-Verlag, Berlin,
1451–1455
German, pp 95–108
31. Sloas MM, Flynn PM, Kaste SC, Patrick CC (1993) Typhlitis in
children with cancer: a 30-year experience. Clin Infect Dis 17:484– 53. Gasche C, Moser G, Turetschek K, Schober E, Moeschl P,
490 Oberhuber G (1999) Transabdominal bowel sonography for detec-
tion of intestinal complication in Crohn's disease. Gut 44:112–117
32. Katz JA, Wagner ML, Gresik MV, Mahoney DH Jr, Fernbach DJ
(1990) Typhlitis. An 18-year experience and post mortem review. 54. Kohn A, Cerro P, Milite G, De Angelis E, Prantera C (1999)
Cancer 65:1041–1047 Prospective evaluation of transabdominal bowel sonography in
33. Alt B, Glass NR, Sollinger H (1985) Neutropenic enterocolitis in the diagnosis of intestinal obstruction in Crohn’s disease: compar-
adults. Review of the literature and assessment of surgical interven- ison with plain abdominal film and small bowel enteroclysis.
tion. Am J Surg 149:405–408 Inflamm Bowel Dis 5:153–157
34. Ikard RW (1981) Neutropenic typhlitis in adults. Arch Surg 116: 55. Maconi G, Radice E, Greco S, Porro GB (2006) Bowel ultrasound
943–945 in Crohn’s disease. Best Pract Res Clin Gastroenterol 20:93–112
35. Teefey SA, Montana MA, Goldfogel GA, Shuman WP (1987) 56. Kucharzik T, Kannengiesser K, Petersen F (2017) The use of ultra-
Sonographic diagnosis of neutropenic typhlitis. Am J Roentgenol sound in inflammatory bowel disease. Ann Gastroenterol 30:135–
149:731–733 144
36. Roberts PL, Veidernheimer MC (1994) Current management of 57. Yeh H, Rabinowitz J (1982) Ultrasonography of gastrointestinal
diverticulitis. Adv Surg 27:189–208 tract. Semin Ultrasound CT MR 3:331–347
37. Valentino M, Serra C, Ansaloni L, Mantovani G, Pavlica P, Barozzi 58. Weissberg DL, Scheible W, Leopold GR (1977) Ultrasonographic
L (2009) Sonographic features of acute colonic diverticulitis. J Clin appearance of adult intussusception. Radiology 124(3):791–792
Ultrasound 37:457–463 59. Weilbaecher D, Bolin JA, Hearn D, Ogden W 2nd (1971)
38. Ripolles T, Agramunt M, Martinez MJ, Costa S, Gomez-Abril SA, Intussusception in adults. Review of 160 cases. Am J Surg 121:
Richart J (2003) The role of ultrasound in the diagnosis, manage- 531–535
ment and evolutive prognosis of acute left-sided colonic diverticu- 60. Bruce J, Huh YS, Cooney DR, Karp MP, Allen JE, Jewett TC
litis: a review of 208 patients. Eur Radiol 13:2587–2595 (1987) Intussusception: evolution of current management. J
39. Hollerweger A, Macheiner P, Hubner E et al (2002) Colonic diver- Pediatr Gastroenterol Nutr 6:663–674
ticulosis: a comparison between sonography and endoscopy. 61. Bhisitkul DM, Listernick R, Shkolnik A, Donaldson JS, Henricks
Ultraschall Med 23:41–46 BD, Feinstein KA, Fernbach SK (1992) Clinical application of
40. Schwerk WB, Schwarz S, Rothmund M (1992) Sonography in ultrasonography in the diagnosis of intussusception. J Pediatr 121:
acute colonic diverticulitis. Dis Colon Rectum 35:1077–1084 182–186
41. Laméris W, van Randen A, Bipat S, Bossuyt PMM, Boermeester 62. Cerro P, Magrini L, Porcari P, De Angelis O (2000) Sonographic
MA, Stoker J (2008) Graded compression ultrasonography and diagnosis of intussusceptions in adults. Abdom Imaging 25:45–47
Emerg Radiol

63. el-Pozo G, Albillos JC, Tejedor D (1996) Intussusception: US find- 70. O’Malley ME, Wilson SR (2003) US of gastrointestinal tract ab-
ings with pathologic correlation—the crescent-in-doughnut sign. normalities with CT correlation. Radiographics 23:59–72
Radiology 199:688–692 71. Shiramara M, Koga T, Ishibashi H, Uchida S, Ohta Y (1994)
64. Alessi V, Salerno G (1985) The hay fork sign in the ultrasonograph- Sonographic features of colon carcinoma seen with high-
ic diagnosis of intussusception. Gastrointest Radiol 10:177–179 frequency transabdominal ultrasound. J Clin Ultrasound 22:359–
65. Lewis RB, Mehrotra AK, Rodriguez P, Manning MA, Levine MS 365
(2014) From the radiologic pathology archives: gastrointestinal 72. Ko YT, Lim JH, Lee DH, Lee HW, Lim JW (1993) Small bowel
lymphoma: radiologic and pathologic findings. Radiographics obstruction: sonographic evaluation. Radiology 188:649–653
34(7):1934–1953 73. Schmutz GR, Benko A, Fournier L, Peron JM, Morel E, Chiche L
66. Levine MS, Rubesin SE, Pantongrag-Brown L, Buck JL, Herlinger (1997) Small bowel obstruction: role and contribution of sonogra-
H (1997) Non-Hodgkin’s lymphoma of the gastrointestinal tract: phy. Eur Radiol 7:1054–1058
radiographic findings. AJR Am J Roentgenol 168:165–172 74. Silva AC, Pimenta M, Guimarães LS (2009) Small bowel obstruc-
67. Goerg C, Schwerk WB, Goerg K (1990) Gastrointestinal lympho- tion: what to look for. Radiographics 29:423–443
ma: sonographic findings in 54 patients. AJR Am J Roentgenol
75. Grassi R, Romano S, D’Amario F, Giorgio Rossi A, Romano L,
155:795–798
Pinto F, Di Mizio R (2004) The relevance of free fluid between
68. Smith C, Kubicka RA, Thomas CR Jr (1992) Non Hodgkin lym-
intestinal loops detected by sonography in the clinical assessment
phoma of the gastrointestinal tract. RadioGraphics 12:887–899
of small bowel obstruction in adults. Eur J Radiol 50(1):5–14
69. Lim JH (1996) Colorectal cancer: sonographic findings. AJR Am J
Roentgenol 167:45–47

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