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Canadian Association of Radiologists Journal xx (2017) 1e8

www.carjonline.org

Pediatric Radiology / Radiologie pediatrique

Lower Esophageal Disorders in Childhood Evaluated by Transabdominal


Ultrasound and Fluoroscopy: A Pictorial Essay
Chrysoula Koumanidou, MD, PhDa,*, Marina Vakaki, MD, PhDa, Argyro Mazioti, MD, PhDb,
Efthymia Alexopoulou, MD, PhDb
a
Radiology Department, P & A Kyriakou Children’s Hospital, Athens, Greece
b
2nd Radiology Department, National and Kapodistrian University of Athens, Attikon University Hospital, Athens, Greece

Key Words: Esophagus; Fluoroscopy; Pediatric; Ultrasound

Pediatric lower esophageal disorders and diseases are rare (Figures 1 and 2). Further imaging of the remainder of the
in the pediatric population. The most common include hiatus stomach and the duodenum is usually performed, which will
hernia, achalasia, duplication cyst, esophageal varices, and not be assessed in this essay. The ALARA (As Low As
esophagitis. In all these disorders transabdominal sonography Reasonably Achievable) principle should always be applied,
and fluoroscopy are able to provide substantial diagnostic data, to keep radiation dose low [1].
including both morphologic and functional information of the
lower esophagus. The educational objective of this pictorial
essay is to review the technique of esophageal ultrasound and Esophageal Sonography Technique
fluoroscopy, as well as the imaging findings of the commonest
pediatric lower esophageal disorders. The evaluation of the distal esophagus should be per-
formed in quiet and calm infants after giving a weight-related
food amount (milk or chamomile) for filling the stomach
Esophageal Fluoroscopy Technique sufficiently. Children should be examined in the supine and
anterior oblique positions, and in some cases in the erect
Esophageal fluoroscopy is performed after adequate position. The examination should be performed with a
fasting of the child, with the use of contrast material, most curvilinear transducer of 5-8 MHz or a linear high frequency
commonly barium sulfate. The contrast media is delivered by transducer, using the left hepatic lobe as acoustic window
a baby bottle in infants and small children, or taken from a [2,3]. In longitudinal section, the esophagus is revealed as a
cup in older children. The examination begins with the child tubular structure consisted of 2 hypoechoic peripheral bands,
in the lateral projection, obtaining images from the naso- which represent the muscular layers and a central hyper-
pharynx to the esophagogastric junction as well as the echoic line, which represents the mucosa and collapsed
stomach fundus. Subsequently the child lies supine, to lumen. In cross-sectional images esophagus appears as a
examine the esophagus in the anteroposterior projection. The target with a hypoechoic peripheral ring, which represents its
anatomic course, the calibre, the mucosal surface of the muscular layer and a hyperechoic centre, the mucosa and
esophagus, and the position of the gastroesophageal junction collapsed lumen. Some ultrasound measurements should be
should be evaluated. In addition, esophageal peristalsis made when necessary, for precise evaluation of esophageal
should be assessed and possible reflux should be documented disorders. Abdominal esophageal length should be measured
at the end of a normal exhalation, from the point at which the
* Address for correspondence: Chrysoula Koumanidou, MD, PhD, Fthio- esophagus penetrates the diaphragm, to the base of the
tidos 13, Marousi, Athens, 15122, Greece. triangular pad of gastric folds at the anterior surface of
E-mail address: argyromazioti@hotmail.com (C. Koumanidou). the fundus of the stomach. The mean length normally ranges

0846-5371/$ - see front matter Ó 2017 Canadian Association of Radiologists. All rights reserved.
https://doi.org/10.1016/j.carj.2017.10.001
2 C. Koumanidou et al. / Canadian Association of Radiologists Journal xx (2017) 1e8

Figure 2. Gastroesophageal reflux. Esophageal fluoroscopy in a 3-month-old


boy with recurrent vomiting demonstrates gross gastroesophageal reflux up
to the upper esophagus. The esophagus is dilated, with wide opening of its
intra-abdominal part and the gastroesophageal angle is obtuse (thin arrow).
Note the dysplastic ribs on the left hemithorax (thick arrow).

Figure 1. Gastroesophageal reflux. Esophageal fluoroscopy in a 2-month-old


boy with recurrent vomiting demonstrates gastroesophageal reflux up to the Fluoroscopy can easily demonstrate the sliding hernia,
intrathoracic esophagus. The gastroesophageal angle is normal (arrow). depicting the gastroesophageal junction located above the
diaphragmatic hiatus (Figure 6).
from 22.2 mm in newborns to 27.2 mm in 1-year-old infants Sonography, having the advantage of no radiation exposure,
and exceeds up to 34 mm in children older than 6 years of is also a reliable diagnostic tool. It can demonstrate: 1) the
age [2,3] (Figures 3A and 3B). In the same view the presence of severe GER, 2) a short abdominal esophagus, 3) an
gastroesophageal angle (angle of His) can be measured, be- increased gastroesophageal angle of more than 130 , and 4) an
tween the abdominal esophagus and the posterior gastric enlarged ‘‘beak’’ at the gastroesophageal junction with a wide
wall: an angle of 70 -100 is considered normal, whereas opening of gastroesophageal junction [4,5] (Figure 7). During
100-130 is obtuse and 130 -180 is completely obtuse real time examination sliding of the stomach fundus towards
(Figure 4). The total esophageal diameter should be 10 mm the diaphragm is observed [2].
normally, and the esophageal wall thickness (defined as the In paraesophageal hernia, part of the stomach herniates
total hypoechoic layer and measured on the anterior wall at through the esophageal hiatus, whereas the gastroesophageal
the midpoint of the abdominal esophagus) measures from junction remains in its normal location [4]. This type of hernia
2.1-5.7 mm, depending on the age of the child [3] (Figure 5). does not relate to gastroesophageal reflux disease (GERD), and
may present with respiratory tract symptoms and vomiting.
Fluoroscopy can reveal the normal position of gastroesopha-
Imaging Findings geal junction and the presence of stomach above the hiatus
(Figure 8). This may also be demonstrated by transabdominal
Hiatal Hernia sonography, after adequate filling of the stomach (Figure 9).
Further imaging is usually not required, although is some
Hiatal hernia is a herniation of the gastroesophageal cases esophageal endoscopy is also performed.
junction and part of the stomach through the esophageal
hiatus of the diaphragm into the mediastinum. There are
3 types of hiatal hernia: sliding hernia, paraesophageal Achalasia
hernia, and congenital short esophagus [4].
In sliding hernia, a widened hiatus permits upward The term achalasia is used to describe an abnormal
movement of the gastroesophageal junction and the cardia of lower esophageal sphincter relaxation in response to
stomach into the chest. It represents more than 95% of all deglutition [6,7]. Distal esophageal achalasia is a rare
hiatal hernias and is often associated with gross gastro- primary motility disorder in the pediatric population, with
esophageal reflux [2,4,5]. an annual incidence of 1 in 100,000 [6,7]. The most
Esophageal ultrasound and fluoroscopy / Canadian Association of Radiologists Journal xx (2017) 1e8 3

Figure 3. Normal abdominal esophagus. Sonographic longitudinal scan in a 3-month-old girl using the left hepatic lobe as acoustic window. (A) The panel is
not annotated. (B) The normal triangular pad of gastric folds at the anterior surface of the fundus of the stomach is shown (sketch triangle). The esophageal
length is measured from the point at which the esophagus penetrates the diaphragm, to the base of the triangular pad (double arrow).

common clinical symptoms include progressive dysphagia


for solid and liquid food, regurgitation, retrosternal pain,
and weight loss. Esophageal achalasia can be suspected
from a chest x-ray, when an air-filled distended esophagus
is demonstrated.
Imaging findings of achalasia in fluoroscopy include a
dilated proximal esophagus with a ‘‘bird’s beak’’elike
tapering of its lower part or a ‘‘champagne glass’’ appear-
ance, and dilatation of the esophagus above the gastro-
esophageal junction [6,7] (Figure 10). Delayed passage of
the barium and intermittent small spurts through the nar-
rowing lower esophageal sphincter are noted [6,7]. Lack of
esophageal peristalsis is also noted fluoroscopically. It should
be stressed that in the early phase of the disease none of these
signs may be present.
Transabdominal ultrasonography may also be used for the
evaluation of esophageal achalasia. It can reveal the ‘‘bird’s
beak’’ appearance of the lower esophagus, the dilatation of
the distal esophagus with a smooth and symmetric thickening
of the esophageal wall, and the absence of a mass located
near or at the gastric cardia [8,9] (Figure 11). Dilatation of
the distal part of esophagus is best revealed in the erect
position after deglutition of water.
Final diagnosis of achalasia is based on esophageal
manometry.

Duplication Cyst
Figure 4. Normal abdominal esophagus. Sonographic longitudinal scan in
Esophageal duplication cyst is a rare developmental the same 3-month-old girl. The gastroesophageal angle (angle of His) is
anomaly, with an estimated incidence of 1 in 8200 [10]. measured (curved line).
4 C. Koumanidou et al. / Canadian Association of Radiologists Journal xx (2017) 1e8

Figure 7. Hiatal sliding hernia. Sonographic longitudinal scan in a 20-month-


old girl with recurrent vomiting. The stomach is filled with milk and the
gastric fundus is located above the diaphragm.
Figure 5. Normal abdominal esophagus. Sonographic longitudinal scan in a
2-month-old girl. The stomach is filled with milk (asterisk). The abdominal
esophagus is a tubular structure that consists of 2 hypoechoic peripheral but also provide the final diagnosis by revealing the char-
bands that represent the muscular layers (double arrow) and a central acteristic ‘‘gut signature’’ of gastrointestinal duplication
hyperechoic line that represents the mucosa and collapsed lumen (arrow). cysts. The lesion appears as a cystic mass adjacent to the
abdominal part of esophagus, with an internal appearance
Although usually asymptomatic, they may present with that varies from anechoic to hyperechoic, depending on its
gastrointestinal symptoms due to compression of the
esophagus.
Fluoroscopy may reveal a mass lesion at the lower end of
esophagus. The study can also delineate possible communi-
cation of the cyst with the esophageal lumen (Figure 12).
Transabdominal ultrasound can be very helpful in the
evaluation of these cases, as it can not only depict the lesion,

Figure 8. Hiatal paraesophageal hernia. Esophageal fluoroscopy in a 2.5-


Figure 6. Hiatal sliding hernia. Esophageal fluoroscopy in an 8-month-old year-old boy with recurrent vomiting and weight loss. A portion of the
boy with vomiting. There is herniation of the gastric fundus above the stomach herniates, through the esophageal hiatus, inside the thoracic cavity,
diaphragm, into the thorax (arrow). The gastroesophageal junction is located anterior to the esophagus (short arrow). The gastroesophageal junction re-
above the diaphragm. mains in its normal location (long arrow).
Esophageal ultrasound and fluoroscopy / Canadian Association of Radiologists Journal xx (2017) 1e8 5

Figure 9. Hiatal paraesophageal hernia. Sonographic longitudinal scan. The


stomach is filled with milk and herniates into the thorax. The gastroesoph-
ageal junction remains in its normal location, but it cannot be demonstrated,
as the stomach (short arrow) is anterior to the esophagus (long arrow). Its Figure 11. Achalasia. Sonographic longitudinal scan in a 10-year-old girl
upper gastrointestinal contrast radiography corresponds to that shown in with dysphagia, vomiting, and abdominal pain. A dilated distal esophagus
Figure 8. with fluid retention is demonstrated (short arrow). There is narrowed ‘‘bird-
beak’’ appearance of esophageal end (long arrow) and thickened esophageal
wall (curved arrow).
content (infected or hemorrhagic). The characteristic
appearance of the cyst wall (‘‘gut signature’’) enables the Final diagnosis can be based on those examinations,
diagnosis by ultrasound: the inner part is hyperechoic (mu- although in many cases pediatric surgeons require further
cosa) and the outer part is hypoechoic (muscular layer) imaging with magnetic resonance imaging or computed to-
(Figure 13) [10]. mography to better appreciate the relevant anatomy.

Figure 10. Achalasia. Esophageal fluoroscopy in a 7-year-old boy with


regurgitation and dysphagia for liquid and solid demonstrates the typical Figure 12. Esophageal duplication cyst. Esophageal fluoroscopy in a 12-
narrowing of the abdominal esophagus with a ‘‘bird-beak’’ appearance year-old girl with dysphagia and intermittent abdominal pain. There is
(arrow). extrinsic smooth compression of the right esophageal wall (arrow).
6 C. Koumanidou et al. / Canadian Association of Radiologists Journal xx (2017) 1e8

Figure 13. Esophageal duplication cyst. Sonographic longitudinal scan. A


cystic mass is depicted in contact with the anterior wall of the abdominal
esophagus (arrow). The cyst demonstrates internal fluid-fluid level of
different echogenicity. This is the same child as in Figure 12.

Figure 15. Esophageal varices. Esophageal fluoroscopy in a 14-year-old girl


Esophageal Varices with cystic fibrosis demonstrates multiple serpentine filling defects of the
lower esophagus (arrows).
Esophageal varices represent a rare, life-threatening
In this scenario, abdominal ultrasound, together with
complication, mostly secondary to portal hypertension. The
other clinical parameters, may aid the diagnosis. First, vari-
presence of esophageal varices is related to an enlarged left
ces can be clearly depicted as tortuous veins in contact with
gastric vein. Whereas current guidelines for adults recom-
mend performing esophagogastroduodenoscopy in all pa-
tients with portal hypertension to identify patients with
varices who may benefit from prophylactic therapy, a similar
approach is not supported in children. This is due to the
invasiveness of the method and the need of sedation or
general anesthesia in children [11]. Therefore, a noninvasive
test is needed, able to triage children with higher risk of
esophageal varices.

Figure 14. Esophageal and gastric fundus varices. Sonographic longitudinal


scan in a 13-year-old girl with cirrhosis. There are several serpentine
hypoechoic tubular structures (arrow) in the area of the lesser omentum,
which correspond to the gastric varices. Fewer hypoechoic tubular structures Figure 16. Bacterial esophagitis. Barium meal in a 6-year-old boy demon-
that represent esophageal varices (small arrow) are also demonstrated in the strates thickened esophageal mucosal folds with stenosis of abdominal
anatomic position of the gastroesophageal junction. The latest area is not esophagus (arrow) and mucosal erosions at the upper part of esophagus
shown well in this image, as the cursor is slightly rotated. (thick arrow).
Esophageal ultrasound and fluoroscopy / Canadian Association of Radiologists Journal xx (2017) 1e8 7

Figure 19. Reflux esophagitis. Transabdominal ultrasound in a 7.5-month-


old boy with stagnation of weight, refusal to eat, and vomiting after
receiving food for the last trimester. The examination was performed to
exclude extraluminal causes of stenosis. An asymmetrically thickened wall
at the level of abdominal esophagus was revealed. Calibres demonstrate
measurement of wall thickness.

of LO thickness to aortic diameter at the same level is


increased in cases of esophageal varices. Considering 1.3 as
the lower limit, the predictive value of the method is 91%
[12]. However, it should be emphasized that not all children
with portal hypertension have a thick LO and that steroid
Figure 17. Eosinophilic esophagitis. Esophageal fluoroscopy in a 16-year-old
girl with dysphagia. The examination is normal.
therapy, obesity, and lymphadenopathy may also affect LO

the abdominal esophagus on longitudinal images (Figure 14).


Other ultrasound markers have also been reported. An
increased thickness of the lesser omentum (LO) has been
correlated with the presence of esophageal varices [12]. LO
thickness should be measured between the left hepatic lobe
and the aorta at the level of celiac axis. In this view, the ratio

Figure 18. Eosinophilic esophagitis. Transabdominal ultrasound in the same Figure 20. Reflux esophagitis. Barium meal in the same boy as in Figure 19.
girl as in Figure 17 demonstrates mild esophageal thickening. Wall thickness An eccentric stenosis at the level of abdominal esophagus is revealed (thick
(measured between calibres) is 0.41 cm. arrow). Further workup of the child revealed reflux esophagitis.
8 C. Koumanidou et al. / Canadian Association of Radiologists Journal xx (2017) 1e8

thickness. Another proposed reliable marker for the diag- upper gastrointestinal tract, esophageal fluoroscopy is one of
nosis of esophageal varices in children is the ratio of the the first imaging studies required. In addition, ultrasonogra-
portal vein to body surface [12]. It has been postulated that phy, having the advantages of being a low-cost and rapid im-
the correlation of a ratio of LO thickness to aortic diameter at aging method, with no patient discomfort, no radiation
the same level between 1.3-1.8 and a ratio of the portal vein exposure, and no need for patient hospitalization, is also able to
to body surface >12 mm or the presence of portal obstruc- contribute substantially to the diagnostic procedure, as it can
tion increases the diagnostic predictivity to 100% [12]. also provide both morphologic and functional information.
Esophageal fluoroscopy is able to detect varices as mul- This is why radiologists should be familiar with these imaging
tiple serpiginous filling defects, which interrupt the normal techniques as well as the imaging findings of these disorders, to
parallel course of the esophageal mucosal folds (Figure 15). guide the diagnostic process in a correct and quick manner. In
that way the need for performing more invasive studies (eg,
Esophagitis radionuclide scanning, endoscopy, esophageal manometry, pH
monitoring, endoscopic esophageal sonography) is carefully
Types of pediatric esophagitis include infectious, chemi- evaluated and is some cases may even be omitted or postponed.
cal (resulting from GERD or from the ingestion of corrosive
substances), radiation-induced, or eosinophilic esophagitis.
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