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Radiología. 2012;54(2):137---148
www.elsevier.es/rx
UPDATE IN RADIOLOGY
a
Servicio de Radiodiagnóstico, Hospital Universitario Central de Asturias, Oviedo, Asturias, Spain
b
Servicio de Radiodiagnóstico, Hospital El Bierzo, Ponferrada, León, Spain
KEYWORDS Abstract Acute pain in the right iliac fossa (RIF) is common in children. It can arise from a wide
Abdominal variety of gastrointestinal and genitourinary processes that make up the differential diagnosis
ultrasonography; with acute appendicitis (AA). In this article, we describe the most representative findings of
Right iliac fossa; these processes on ultrasonography (US). We emphasize the characteristics that enable these
Pediatrics; processes to be differentiated from AA.
Acute abdomen; © 2011 SERAM. Published by Elsevier España, S.L. All rights reserved.
Appendicitis;
Crohn’s disease
PALABRAS CLAVE Utilidad de la ecografía en niños con dolor en la fosa ilíaca derecha
Ecografía abdominal;
Fosa ilíaca derecha; Resumen El dolor agudo en la fosa ilíaca derecha es un cuadro frecuente en la infancia. Su
Pediatría; origen puede ser secundario a un amplio abanico de procesos gastrointestinales y genitourinarios
Abdomen agudo; que constituyen el diagnóstico diferencial de la apendicitis aguda. En el presente artículo se
Apendicitis; describen los hallazgos ecográficos más representativos de tales procesos, insistiendo en las
Enfermedad de Crohn características que permiten diferenciarlos de la apendicitis aguda.
© 2011 SERAM. Publicado por Elsevier España, S.L. Todos los derechos reservados.
Introduction
2173-5107/$ – see front matter © 2011 SERAM. Published by Elsevier España, S.L. All rights reserved.
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appendectomy rate.1 Technological advances in US allow or three per cm) than in the ileum (two per cm). Given its
examination of the layers of the intestinal wall and intestinal origin, the appendix exhibits similar characteris-
surrounding mesentery with high spatial resolution. This tics to the digestive tract, therefore, its maximum diameter
provides new clinical applications such as the assessment should not exceed 6 mm in the transverse plane and its
of acute inflammatory activity, response to treatment and wall should not exceed 3 mm.3,4,6,9 Nonetheless, histologi-
complications of Crohn’s disease, US evaluation of acute cally normal appendixes > 6 mm can also be found in cases
recurrent appendicitis, follow-up of intestinal involvement of accumulation of secretions in the lumen, hyperplasia or
in Schönlein---Henoch purpura (SHP), preoperative assess- fecal impaction.10
ment of the viability in cases of ovarian torsion, or The normal appendix is oval-shaped in the transverse
support for the decision of performing a biopsy in celiac plane and easily compressible. Conversely, in appendicitis,
disease. the appendix walls are inflamed, rigid and noncompressible.
The objective of this study is to describe the US findings Its lumen may contain air or fluid, or be collapsed with adhe-
and the key diagnostic findings of those conditions that may sion of the mucosal layers, giving rise to a central echogenic
present with acute RIF pain in children, with an emphasis on line.
AA, since this is the most common disease in children requir- Lastly, the mesentery appears slightly echogenic.
ing surgery2,3 and the most common source of diagnostic
errors.
Acute appendicitis
Technique
AA is the most common condition requiring surgery in
children and the one leading to more diagnostic errors.
The graded compression technique described by Puylaert in
Traditionally, AA has been described to occur when fecal
1986 is based on the fact that gradual compression on the
matter or appendicoliths obstruct the appendiceal lumen,
anterior abdominal wall eliminates bowel gas and intralumi-
which is usually followed by infection. However, we know
nal fluid from the bowel loops, reduces the distance between
now that AA is not always secondary to obstruction and that
transducer and appendix, and displaces bowel loops out of
several causes may lead to AA: lymphoid follicular hyper-
the RIF.4 This compression allows visualization of iliac ves-
plasia obstructing the cecal---appendiceal junction, inflamed
sels and psoas muscle, since the appendix is anterior to these
follicles in infectious processes, foreign bodies, or trauma.
structures (Fig. 1A). In addition to be ineffective and painful,
These factors lead to inflammation and an increase in
fast compression may result in rupture of an appendix at risk
intraluminal pressure. As a result, the appendix enlarges
for perforation.2
and induces inflammatory changes in the surrounding tis-
The exam is performed in the longitudinal and transverse
sues, such as the pericecal fat and peritoneum.2 Ultimately,
planes. The ascending colon appears as a nonperistaltic
ischemia occurs and the inflamed appendix, eventually, per-
structure containing fluid and gas. Inferiorly, the terminal
forates.
ileum, compressible and peristaltic, can be identified. The
Sensitivity and specificity of sonography for the diagno-
cecal base, where the appendix arises, is 2---3 cm below the
sis of AA vary greatly between studies (up to 100 and 98%,
terminal ileum. While the base of the appendix is at a fairly
respectively).2---12 The appendiceal diameter is considered
constant location, its end may move freely, and its location
the most relevant morphologic criteria (sensitivity > 98%)
is therefore very variable; however, this does not trans-
and, traditionally, the threshold diameter > 6 mm has been
late into a statistically significant difference in the rate of
used for diagnosis of appendicitis. On transverse images,
appendicitis.5,6
the appendix appears fixed, round and noncompressible.
The topology of the superior mesenteric vessels and their
Hyperechogenicity of the pericecal fat is common. This
relationship with the aorta and inferior vena cava should be
fat may increase in volume and surround the appendix,
systematically identified.
which represents the inflamed omentum that migrates to the
appendiceal area in case perforation occurs (Fig. 2A). Free
Normal right iliac fossa fluid and mesenteric lymph nodes are frequent but unspe-
cific. In up to 30% of cases, appendicoliths are seen in the
The digestive tract comprises four concentric layers that appendiceal lumen.2
can be differentiated histologically. The layers from deep Doppler signal varies depending on the stage of the dis-
to superficial are the mucosa----consisting of an epithelium ease. Although it might increase in the acute phase (Fig. 2B),
with underlying lamina propria and the muscularis mucosa----, it may diminish in case of appendiceal perforation.2---4,9
the submucosa, the muscularis propria and the adventitia. Therefore, Doppler examination alone cannot reliably
US shows a penta-stratified pattern where the first (superfi- distinguish between normal and abnormal appendix. Per-
cial mucosa), third (submucosa) and fifth (adventitia) layers foration can be suspected in the presence of an irregular
are hyperechogenic, and the second (muscularis mucosa) contour of the appendix, fluid or collections, and dilated
and fourth (muscularis propria) layers are hypoechoic6---8 bowel loops with thickened walls2---4,7,10,13 (Fig. 1E). After
(Fig. 1B). perforation occurs, the appendix is usually decompressed
In adults, the thickness in any segment of the digestive and it is visible only in 30---60% of cases.4,9,13
tract is ≤3 mm. In children, it ranges between 1.5 and 3 mm Acute pain, gas and severe obesity may complicate visu-
in the terminal ileum and <2---3 mm in the colon, depending alization of the appendix. Therefore, the nonvisualization of
on the age.8 Valvulae conniventes are <2 mm in width and the appendix does not allow us to rule out AA despite the fact
2---5 mm in length, being more numerous in the jejunum (two that the first studies considered the nonvisualization on US
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Cecum
Terminal ileum
Appendix
Lumen m mm sb mc a
Iliac
vessels
Psoas
Figure 1 (A) US image of the normal right iliac fossa showing the psoas muscle and iliac vessels. (B) Axial US of the appendix
shows the correlation between the normal pentastratified pattern and the corresponding histological layers. Hyperechogenic layers
correspond to the superficial mucosa (m), submucosa (sb) and adventitia (a), while hypoechoic layers correspond to the mucosa
and (mm) and muscularis propria (mc).
an exclusion criterion.5 For an experienced ultrasonologist, resolving appendicitis’’, is thought to be due to the relief
nonvisualization has a negative predictive value of 90%.2,10 of obstruction. In these cases, US follow-up images show
Since some appendicitis are limited to the appendiceal a gradual decrease in the appendiceal diameter.10,14 US
tip, only the detection of a normal appendix throughout follow-up in patients with AA, performed 6---36 h after the
its entire length safely rules out AA.2,4,5 The detection initial examination, represents a useful diagnostic tool that
range of a normal appendix varies between 40 and 82% of complements clinical follow-up and helps reduce the num-
examinations, and this depends on the operator experience ber of CT studies done on children.
and the physical characteristics of the patient.5,6,10 Recurrence rate relates to the presence or absence of
enlarged mesenteric lymph nodes. A study carried out by
Cobben et al. on 60 patients showed that the subgroup of
Recurrent acute appendicitis male patients with no enlarged mesenteric lymph nodes had
a recurrence rate of 60%, which seems a clear indication
In 10% of patients with AA, the symptoms and signs sub- for surgery. Conversely, the presence of enlarged mesen-
side spontaneously 12---48 after the onset but they reappear teric lymph nodes was associated to a lower recurrence
later on.10,14 This phenomenon, known as ‘‘spontaneously rate.14
Figure 2 Appendicitis: (A) Transversal US image shows inflamed appendix with enlarged diameter and wall thickening, and
hyperechogenicity of periappendiceal fat. (B) Longitudinal color Doppler US image shows inflamed appendix with hyperemic wall.
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Cystic fibrosis
Appendiceal mucocele
Figure 3 Mucocele. Hypoechoic mass arising from the cecum,
Appendiceal mucocele is characterized by distension of the with ‘‘skin onion’’ structure (*), thin walls and no associated
appendix secondary to intraluminal accumulation of mucus. inflammatory changes.
To date, four pathological processes leading to appendiceal
mucocele have been described: obstruction at the cecal
appendiceal junction; mucosal hyperplasia; mucinous cys- refer to enlargement of some mesenteric lymph nodes, with
tadenoma and mucinous cystadenocarcinoma. US shows a or without ileitis.9,10 However, some papers describe the
distended appendix with no wall thickening and no regional presence of enlarged (>10 mm in the short axis) mesenteric
inflammatory signs, with abundant echogenic content in nodes in asymptomatic children.22 Increased color Doppler
the interior and the ‘‘onion skin’’ structure,18---20 a sign signal in the mesenteric vessels and minimal amount of free
considered to be characteristic of mucoid material that fluid may be seen (Fig. 3E). The nonvisualization of the
allows differential diagnosis with appendiceal abscesses21 inflamed appendix is more indicative of ML than AA.9
(Fig. 3).
Acute gastroenteritis
Lymphoid hyperplasia related to viral
infections Acute gastroenteritis (AGE) is the most common inflamma-
tory disease in children. It usually has a viral origin and the
Follicular lymphoid hyperplasia is a histopathologic finding iliocecal region is the most frequently affected. The classic
based on the enlargement of the lymphoid follicles in the presentation of AGE does not require imaging studies. US
lamina propria of the appendiceal mucosa, without infil- shows dilated, hyperperistaltic fluid-filled small bowel loops
tration of polymorphonuclear leukocytes. It is common in with thin walls, where it is not uncommon to see transient
childhood, and according to some authors, it may be the intussusception9 (Fig. 4E).
cause of acute RIF pain in children.7 It also relates to intesti-
nal intussusception. Infectious ileitis or iliocecitis
Only on rare occasions does US allow for the diagnosis
of this condition. In such cases, US findings include dilated
Some bacteria----such as Salmonella, Campylobacter
appendix and thickening of the appendiceal mucosa and
jejuni, Yersinia and, more rarely, Mycobacterium
ileocecal valve, secondary to the presence of hypoechogenic
tuberculosis----have a strong affinity for the lymphoid
nodules. Mesenteric lymph nodes are a constant. Cecum,
tissue of the terminal ileum and give rise to enteritis whose
mesenteric echogenicity and mobility of the distal ileum are
symptoms may simulate those of AA. US findings include
normal.7
intestinal wall thickening and hypogenicity----usually with
intact wall layers----, transmural or mucosal hypervascularity
Mesenteric lymphadenitis and enlargement of mesenteric lymph nodes.9,10 In contrast
to AA, the mesentery is normal and the thickened bowel
Mesenteric lymphadenitis (ML) is a controversial entity, and loops do not form a conglomerate around the appendix.
we frequently resort to this diagnosis in patients in whom Tuberculous ileitis is rare in developed countries. It
normal appendices have been removed. The term is used to appears as asymmetrical, non-stratified thickening of the
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Figure 4 (A and B) Patient with tuberculosis and pain in right iliac fossa. (A) Chest radiograph shows patchy lesions of alveolar
characteristics with bilateral distributions and diffuse secondary to tuberculous bronchopneumonia. (B) US images of the right flank
show diffuse hypoechoic thickening, with loss of normal stratification, secondary to tuberculous ileitis. Note the similarity to the
characteristic thickening of Crohn’s disease (see Fig. 5A and B).
ileocecal walls23---25 (Fig. 4A and B). Its clinical course is SHP, where vascular proliferation is less conspicuous. Ves-
similar to that of chronic diseases with US findings similar sel density, assessed by Doppler US in affected bowel loops,
to those of Crohn’s disease, but always with considerable correlates with disease activity and is used as a non-invasive
involvement of the cecum.9 The microorganism induces technique for monitoring the course of the disease and the
an inflammatory process that eventually leads to ulcer response to treatment.8,28,30 Vessel density is classified as
formation with subsequent healing, as well as extensive low, moderate and high if there are 0---2, 3---5, or more than
infiltration of peritoneum, omentum and mesentery associ- 5 Doppler signals per cm,2 respectively.30
ated with centrally hypodense lymph nodes.24---26 There are Appendiceal involvement appears in 23% of patients with
no pathognomonic findings. Biopsy during colonoscopy and CD, manifesting as appendiceal hyperemia similar to that of
culture of lesions is the diagnostic technique of choice, while AA. However, thickening > 5 mm and hyperemia of the termi-
negative histologic results do not preclude tuberculosis.26 nal ileum support the diagnosis of CD. US findings in cecum
and appendix are similar in both entities and therefore can-
not be used for differentiation.28
Crohn’s disease
Schönlein---Henoch purpura
In 25% of cases, Crohn’s disease (CD) begins in child-
hood, with involvement of the iliocecal region in 55% of
SHP is a small-vessel vasculitis that may affect the intestinal
patients.8 Acute abdominal symptoms simulating AA are not
tract. In some patients (10---30%), the intestinal involvement
unusual. CD causes transmural inflammation that extends
may precede skin lesions, simulating AA. The episodes of
to the surrounding mesentery. On US this translates into
paroxysmal pain are secondary to edema in the subserosa
circumferential wall thickening that may be segmental or
and submucosa and hemorrhagic infiltration.8,31
multifocal, and finally, loss of wall stratification.8---10,27,28
Characteristic US findings include diffuse, circumferen-
The wall appears hypoechoic with an echogenic cen-
tial thickening of the bowel wall, with focal intramural
tral line that represents the superficial mucosa (Fig. 5A
hematomas that appear as hyperechogenic areas, giving an
and B). The mesentery is hyperechogenic and there is
irregular appearance to the thickened wall.2,8,31 Associated
no motion of bowel loops with transducer pressure.10
mesenteric adenopathy and free fluid are common. The duo-
Enlarged lymph nodes are found in approximately 15% of CD
denum and jejunum are the initially involved sites but, with
patients.29
recurrent episodes, the disease extends to the ileum.
CD is associated with intestinal neovascularization. In
contrast with what happens in areas of fibrotic scarring,
in active disease there is mesenteric hypervascularity and Celiac disease
‘‘comb sign’’, indicative of increased blood flow in the vasa
recta (Fig. 5B). This finding may help differentiate CD from Up to 25% of children with celiac disease initially
infectious or eosinophilic ileitis or ileitis associated with present with acute abdomen. US may help make an
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Figure 5 Crohn’s disease. (A) Color Doppler US shows marked wall thickening of the terminal ileum mainly due to a hyperechogenic
submucosa, a finding characteristic of Crohn’s disease, and mural hypervascularity. (B) Presence of multiple enlarged lymph nodes
of inflammatory appearance (*) and mesenteric hyperechogenicity and hypervascularity.
initial diagnosis and institute an early treatment. Char- combined with the fact that pediatric patients are not good
acteristic findings include abnormally dilated fluid-filled candidates for surgery, makes the surgical management of
bowel loops and reversal of the jejuno-ileal fold pattern. these children, who present with appendiceal thickening
There is hyperperistalsis and minimal ascites in 82% of and RIF pain, controversial.39
cases.32,33
Intestinal intussusception is a common complication and
the presence of underlying celiac disease should be inves-
Intussusception
tigated in case of recurrent intussusception. Ulcerative
jejuno-ileitis should be suspected in adult patients with Intussusception involves invagination of a segment of
celiac disease and acute abdomen.34 intestine into the lumen of an immediately distal seg-
US findings may confirm the need for biopsy.35 ment. Intussusception is usually idiopathic, associated with
lymphoid hyperplasia, secondary to viral infections. Approx-
imately 90% of patients with intussusception are younger
than two years.3 Findings on abdominal radiograph may be
Typhlitis
Figure 9 (A---C) Ovarian torsion. (A) Axial US image of the RIF in a newborn shows a cystic structure with fluid---fluid level (arrows),
very suggestive of ovarian torsion secondary to the presence of a complicated cyst. Bladder (V). (B) T2 weighted images of MRI
study, with and without fat suppression, performed the following day cannot identify the right ovary but the cystic lesion is observed
in the left flank. The mobility of the lesion suggests ovarian origin, which was subsequently confirmed at surgery. (C) The left ovary
showed normal morphology and a normal location in the pelvis (arrow).
Figure 10 Persistent urachus. Child with abdominal pain, fever and mictional syndrome. Echogenic tubular structure connected
to the umbilicus (*) in contact with the bladder dome (v).
Hemorrhagic ovarian cyst helps differentiate it from an abscess. The presence of free
peritoneal fluid is common.
Ovarian cysts may cause pain due to hemorrhage or
rupture.9 Classically they appear as avascular complex cys- Ovarian tumors
tic lesions, with a thin reticular pattern, fluid-detritus levels
and/or hyperechogenic areas in relation to coagulated blood Most ovarian tumors in girls are benign and painless but,
(Fig. 8E).9 The absence of involvement of the adjacent fat on occasions, they may cause pain due to compression of
ILIOCECAL
LIOCECAL PATHOLOGY MESENTERIC/OMENTAL PATHOLOGY
Crohn's disease Mesenteric lymphadenitis
Infectious ileitis Lymphangioma
Typhlitis Omental infarction
Burkitt lymphoma Appendagitis
Intussusception
Duplication cyst
Meckel diverticulum
APPENDICEAL PATHOLOGY
Acute appendicitis
Mucocele GYNECOLOGIC PATHOLO
PATHOLOGY
Distension related to cystic fibrosis Ovarian torsion
Lymphoid hyperplasia Hemorrhagic cyst
Ovarian tumors
Figure 11 Diagram depicting the anatomy of RIF and the possible disorders arising from its structures.
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