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132
D. Franke and Z. Harkanyi
pulpa, and sinusoids. Approximately 50s postinjection, the UCA enhancement should be
homogeneous throughout the spleen. General
signs of benign lesions are persistent isoenhancement or absent enhancement with avascularity of the lesion (e.g., a cyst). Signs of
malignancy are a washout phenomenon or a
hypo-enhancement in the late parenchymal
phase.
13.3 Spenunculi or Accessory
Spleens, Splenosis,
andPolysplenia
Accessory spleens are very common and seen in
an overall prevalence of 15% in a meta-analysis
of 22,487 patients [2, 6]. Identication of splenunculi is particularly important in patients with
immune thrombocytopenia requiring splenectomy as unrecognized accessory spleens may
increase in size after splenectomy and responsible for refractory symptoms. The location of a
spenculus is most often at the hilum or lower pole
of the spleen, but may also be found within the
pancreas or elsewhere in the abdomen.
Splenunculi have the same B-mode ultrasonography (US) appearance and the same contrast
enhancement characteristics of the normal
spleen. This may be important in the diagnosis of
ectopic splenic tissue in the pancreatic tail or
elsewhere in the abdomen, particularly after traumatic splenic rupture, and in the differential diagnosis of lymph nodes at the splenic hilum. The
post-traumatic splenic auto-transplantation of
splenic tissue in the abdomen is called splenosis.
Contrast-enhanced ultrasound can identify the
characteristic persistent late-phase enhancement
of splenic tissue and may be useful in splenosis
[7]. Polyspenia is most commonly associated
with syndromes such as heterotaxy and is usually
diagnosed on the B-mode US.
13.4 Anomalies ofPosition:
Wandering Spleen
A “wandering spleen” is a hyper-mobile, abnormally positioned ectopic spleen and may be an
excellent indication for CEUS if painful torsion
is suspected, congestion or infarction occurs due
to the mobility [8, 9]. It is a rare and possibly
congenital condition due to abnormally lax ligaments failing to keep the spleen in the anatomical
position. The correct and early diagnosis is challenging, especially in children with symptoms
ranging from none, recurrent abdominal pain to
acute abdomen in case of torsion or infarction [9,
10]. The main CEUS nding is a non-
enhancement in the infarcted areas (Fig.13.1).
a
Fig. 13.1 Infarction of a wandering spleen. (a) The
spleen (arrow) is present in the left iliac fossa, above the
psoas muscle (arrowhead) in a 9-year old boy with 3days
of intractable abdominal pain, with identication of an
abnormal position of the spleen. (b) Following the admin-
b
istration of an UCA, there is only hilar vessel enhancement (arrow) consistent with infarction in a “wandering
spleen.” (Courtesy of Annamaria Deganello and Maria
Sellars)
ab
13 Pediatric Contrast-Enhanced Ultrasonography (CEUS) oftheSpleen
133
13.5 Splenic Infarction
Splenic infarction is seen in children with
sickle- cell disease, after septic embolism in
bacterial endocarditis or myeloproliferative
diseases. In the early phase, infarction of the
spleen is often iso-echogenic (later hypo-echogenic), may be ill delineated on the B-mode
US, and may, therefore, be overlooked. After
administration of the UCA, non-enhancement
is often triangular in the conguration in the
spleen (wedge-shaped). Complications after
splenic infarction are liquication of the
affected parenchyma, hemorrhage, post-infarction splenic rupture, or splenic pseudoaneurysm, all of which may be diagnosed using
CEUS [11, 12]. Splenic pseudoaneurysms are
particularly clinically relevant for the child
[13]. A study using CEUS in the assessment of
upper left quadrant pain and splenic inhomogeneity on the B-mode US in adults with focal
lesions found half of these lesions were splenic
infarction [11]. Recurrent splenic infarction
may lead to calcication, organ shrinkage, and
eventually functional asplenia/hyposplenia. In
functional asplenia, a reduced or even absent
CEUS enhancement in the parenchymal phase
can be suggestive [4].
13.6 Focal andDiuse Lesions
oftheSpleen
13.6.1 Benign Focal Lesions
oftheSpleen
13.6.1.1 Cystic Lesions
Simple cysts have a characteristic B-mode US
appearance; being round, anechoic with posterior
enhancement, with no vascularization on color
Doppler US and a thin smooth wall. Pseudo- or
secondary cysts are thought to be of traumatic or
inammatory origin, containing blood or debris
in the early stage and with a thickened or a calcied wall. In simple cysts, there is no indication
for a CEUS examination, only if the cyst is
thought complicated (Fig.13.2). Hydatid cysts of
the spleen are uncommon in comparison to the
liver and seen in only 5% of patients with
Echinicoccal disease. After administration of a
UCA, there may be a hyper enhanced rim and no
enhancement in the center of the cyst.
13.6.1.2 Hemangioma
Cavernous hemangiomas are the most common
solid focal splenic lesion. Usually, hemangiomas appear well delineated, round, hyperechoic with sometimes with echo-poor regions
Fig. 13.2 Simple splenic cysts. (a) Contrast-enhanced
ultrasound of a simple splenic cyst (arrow) sometimes following trauma to the left ank and an incidental nding
on ultrasound. (b) A simple cyst (arrow) with a hypoenhancing line (arrowheads) towards the capsule
134
D. Franke and Z. Harkanyi
and have no or few signals on color Doppler US
due to the slow blood ow. Calcication may
be present. On CEUS, a characteristic slow centripetal nodular rim enhancement can be
detected similar to that in hepatic hemangiomas. Hemangiomas may present solitary or
multiple (Fig.13.3).
13.6.1.4 Hamartoma
Splenic hamartomas are also termed “splenoma,”
“nodular splenic hyperplasia” or “focal nodular
hyperplasia of the spleen” are rare congenital
benign vascular tumors, which are usually
asymptomatic and diagnosed incidentally.
Complications may be an increase in size and
rupture. They are of variable B-mode US appear-
13.6.1.3 Lymphangioma
Lymphangiomas (lymphatic malformations) in
children are benign and can be found anywhere
in the body. Splenic manifestations are rare.
ance: hypo-echoic and lobulated. The CEUS criteria are a persistent hyper-enhancement of the
lesion and a spoke wheel pattern in the early
phase (Fig.13.5).
Lymphangiomas present on the B-Mode US as
an accumulation of well-delineated small or big
13.6.1.5 Malignant Solid Lesions
cysts with septae, containing a lymph-like uid
and possibly debris. The cysts show no contrast
enhancement, whereas the septae can enhance
due to the presence of vessels (Fig.13.4).
Metastasis
Primary malignancy of the spleen and splenic
metastasis is rare in adults and children.
ac
b
Fig. 13.3 Splenic hemangioma. (a) Hypoechoic solid
mass (arrow) in the spleen in a 16-year-old boy with no
prior clinical history. (b) On the CEUS image, the
hypoechoic lesion is seen to enhance (arrow, between cur-
sors) more than the surrounding spleen. (c) A microvascu-
lar CEUS mapping image of the mass
13 Pediatric Contrast-Enhanced Ultrasonography (CEUS) oftheSpleen
135
a
Fig. 13.4 Splenic lymphatic malformation. (a) Cystic
mass (arrow, between cursors) with multiple septa with no
vascularity on color Doppler US. (b) On the CEUS image
a
b
of the mass, there is no enhancement of the cystic component but enhancement of the septations is present (arrows),
typical of a rare isolated splenic lymphangioma
b
Fig. 13.5 Splenic hamartomas. (a) A 17-year-old patient
with multiple hypoechoic rounded lesions (arrows) present in the spleen, with a history of sickle cell disease. (b)
Following the CEUS examination, the lesions (arrows)
Angiosarcoma and primary lymphoma are
reported [14]. Lymphoma is the most common
secondary lesion of the spleen in children and is
described below. There is limited data for the role
of CEUS in the detection and characterization of
splenic metastasis in adults and none in children.
Contrast-enhanced ultrasound was found to
improve the imaging of metastasis with respect to
sensitivity and specicity compared to B-Mode
US by 40% [15]. Most of the metastasis was
are hyper-enhancing more than the adjacent spleen, and
remain hyper-enhancing throughout the examination.
(Courtesy of Maria Sellars)
hypoenhancing (66%) or complex (25%) in the
early arterial phase and 75% hypoenhancing in
the later parenchymal phase using CEUS.
Lymphoma
Involvement of the spleen is seen in approximately
10–30% of patients in Hodgkin’s lymphoma. The
spleen may be enlarged and the lymphoma lesion in
the spleen is usually hypo- echoic on B-Mode US,
with no alteration of the splenic vessels on colour-
136
D. Franke and Z. Harkanyi
Doppler imaging. Following administration of the
UCA, an often- progressive hypo-enhancement in
the splenic lymphoma nodule is seen in the parenchymal phase (Fig.13.6). However, splenic CEUS
cannot detect diffuse or small-nodular lymphoma
inltration. Therefore, it is not a standard procedure
in lymphoma staging and is reported to have no
clear advantage in the diagnosis of lymphoma
splenic involvement in adults [16]. However, it has
been shown that CEUS provides higher sensitivity
than computed tomography (CT) or positron emission tomography-CT (PET-CT) in the detection of
splenic involvement in Hodgkin’s lymphoma [17].
There are currently no studies in children.
a
b
13.6.1.6 Splenic Abscesses
Due to the immune competence of the spleen, the
incidence of splenic abscesses is lower than for
the liver. Hematological spread may occur in bacterial endocarditis or even be attributable to fungal infections in leukemia. The B-Mode US
appearance may be variable: well-or illdelineated, hypo-echoic or later hyper-echoic,
micro- or macro-abscesses containing air, debris
or liquid, with or without an abscess wall. A perilesional hyper-enhancement is highly suggestive
of a splenic abscess during CEUS, with the center of the mass usually showing no enhancement
(Fig.13.7).
Fig. 13.6 Splenic lymphoma. (a) Hodgkin’s lymphoma
of the spleen in a 14-year-old boy, on B-mode with several
hypoechoic focal lesions (arrows) in the spleen. (b) The
a
Fig. 13.7 Splenic abscess. (a) A 4-year-old child with
pain and fever. Longitudinal section through the spleen
with a hypoechoic round lesion and no vascularization on
b
CEUS examination depicts several lesions (arrows) with
persistent hypo-enhancement. The continuity of the
splenic vessels is respected
color Doppler study (arrow). (b) The CEUS shows nonenhancement within the lesion with a hyper-enhanced rim
around the abscess (arrows)
13 Pediatric Contrast-Enhanced Ultrasonography (CEUS) oftheSpleen
Fig. 13.8 Splenic trauma. Following a splenic biopsy, a splenic band-like hematoma (arrow) with clinical evidence of
bleeding. The CEUS examination shows no enhancement over all phases at the hematoma site (arrow)
137
13.6.1.7 Splenic Trauma
In blunt or penetrating abdominal trauma, injury
of the splenic is common, despite the intrathoracic position of the spleen. However, B-Mode
US imaging is not sensitive in the detection of
small lacerations, particularly in the rst 2 days
after the trauma. This is due to the initial isoechoic or hypo-echoic appearance of the laceration, and compression of the lesion a consequence
of surrounding parenchymal edema (Fig.13.8).
Using UCA, the sensitivity of detection of a
splenic laceration increases from 51% to 92%
[18] as CEUS improves the visualization of any
non-vascularized defect [19, 20]. For low-energy
abdominal trauma, CEUS has been suggested as
the rst-line imaging modality, especially in children to minimize the radiation burden [21], and
also for the detection and management of follow up complications. In the detection of the splenic
pseudoaneurysm, CEUS appears to be highly
sensitive and specic for diagnosis and follow-up
[13]. In a cohort of adult patients, Poletti etal.
described a 75% sensitivity and 100% specicity
of the CEUS examinations in abdominal trauma
[22], concluding that CEUS may be useful for the
screening of delayed traumatic splenic pseudoaneurysms. The incidence of post-traumatic splenic
pseudoaneurysms may be higher than previously
predicted with approximately 9% in a pediatric
cohort [13]. A splenic of hepatic pseudoaneurysm has potentially life-threatening rupture
often with a delayed presentation. The incidence
of pseudoaneurysms in the liver seems to be
higher than in the spleen. Monitoring after embolization or spontaneous thrombosis of the pseudoaneurysms can be performed using CEUS with
possible detection of pseudoaneurysms smaller
than 0.5cm, where the detection frequency with
CT would be lower. Using CEUS instead of
contrast- enhanced CT, radiation exposure can be
reduced, costs are lower, and bedside practice is
possible. No association was found between the
grade of trauma and the occurrence of pseudoaneurysms of the spleen or liver [13]. Follow-up
CEUS after a splenic injury can be performed
after major trauma, in suspected fractures or rupture of the spleen, delayed vascular injury, to rule
out pseudoaneurysms, in hemodynamic unstable
children, and in case of secondary active bleeding
[23, 24] (Fig.13.9).
138
Fig. 13.9 Splenic
contusion after blunt
trauma. In a 10-year-old
girl with blunt trauma to
the spleen, the CEUS
images demonstrate a
large contusion (arrow,
between cursors) of the
spleen in the
subdiaphragmatic
region. The patient was
treated conservatively
D. Franke and Z. Harkanyi
Table 13.1 Indications for pediatric CEUS of the spleen
Trauma
Unclear focal splenic lesions
Complicated cysts
Infarction
Functional asplenia/hyposplenia
Abscess
Table 13.2 Differential diagnosis of cystic and solid
focal splenic lesions
Cystic focal lesions
• Congenital cyst
• Post-traumatic cyst
• Splenic abscess (cystic or mixed)
• Infectious cyst
• Splenic lymphangioma
• Hydatid disease
Solid focal lesions
• Hemangioma
• Lymphoma
• Hamartoma
• Granulomatosus disease (sarcoidosis,
tuberculosis)
• Metastases
13.6.2 Diuse Lesions oftheSpleen
Diffuse splenic involvement may be caused by
diffuse lymphoma inltration, sarcoidosis with
diffuse manifestation or small nodules, tubercu-
losis, fungal microabscesses from Candida,
Aspergillus or Cryptococcous, and Niemann Pick
disease. CEUS investigations may reveal a
delayed global enhancement or a more prolonged
early phase inhomogenicity. However, these
changes are not constant or specic [25] (Tables
13.1 and 13.2).
13.7 Conclusion
Contrast-enhanced ultrasound has the potential to
become a landmark in the diagnostic improvement of imaging of splenic lesions in children
without the need for general anesthesia or radiation exposure.
References
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3. Sidhu PS, Cantisani V, Deganello A, Dietrich CF,
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6. Vikse J, Sanna B, Henry BM, Taterra D, Sanna S,
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7. Kruger R, Freeman S.An unusual pelvic mass: contrast enhanced sonographic diagnosis of pelvic splenosis. J Clin Ultrasound. 2019;47(3):172–4.
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Carmona MS, Minaya J.Wandering spleen torsionuse of contrast-enhanced ultrasound. BJR Case Rep.
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13. Durkin N, Deganello A, Sellars ME, Sidhu PS,
Davenport M, Makin E. Post-traumatic liver and
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De Laurentiis M, Grimaldi F, Rotoli B. Contrastenhanced harmonic compound US of the spleen
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Contrast-Enhanced Voiding
Urosonography (ceVUS): Current
Experience andAdvanced
Techniques
SusanJ.Back, KassaDarge, andAikateriniNtoulia
14
14.1 Background
14.1.1 Vesicoureteral Reux
Vesicoureteral reux (VUR) is the retrograde
ow of urine from the bladder to the ureter or
kidney. VUR occurs due to functional or structural insufciency of the one-way valve-like
mechanism around the ureteric orice at the vesicoureteral junction [1, 2]. The valve is formed by
the oblique insertion of the distal ureter through
the bladder wall. This tunnel is compressed as the
bladder lls preventing the backow of urine.
In primary VUR, a congenital defect shortens
the length of the ureteric tunnel relative to its
diameter, making the valve-like anti-reux mechanism incompetent [2]. Secondary VUR is an
acquired condition that occurs in association with
functional abnormalities of the lower urinary
S. J. Back (*) . K. Darge
Department of Radiology, Children’s Hospital of
Philadelphia, Perelman School of Medicine,
University of Pennsylvania, Philadelphia, PA, USA
e-mail: BackS@email.chop.edu
A. Ntoulia
Department of Radiology, Children’s Hospital of
Philadelphia, Philadelphia, PA, USA
e-mail: ntouliaa@email.chop.edu
tract (e.g., bladder bowel dysfunction or neurogenic bladder) or as a result of anatomic outlet
obstruction (e.g., posterior urethral valves).
The estimated prevalence of VUR in the general pediatric population is low ranging from
1% to 2% [3]. However, in children who present
with urinary tract infection (UTI), the frequency
of VUR can be as high as 25–40% in those
under 5years and up to 50% in those younger
than 1year [3, 4]. A familial prevalence of VUR
has been described with a rate of 24–51% in siblings and 66% in children whose parents had
VUR [5].
VUR nephropathy may occur due to recurrent
UTIs and pyelonephritis and can lead to substantial
morbidity including renal scarring, increased risk of
hypertension, and end-stage renal disease [6–8].
The management of children with UTI and
VUR remains controversial [9]. In most children,
even high grades of VUR will spontaneously
resolve over time and low grades may not require
treatment. Moderate to severe grades of VUR may
be treated with antibiotic prophylaxis to prevent
recurrent UTIs and correction of bladder and
bowel dysfunction if present [10]. Injection of a
bulking agent around the vesico-ureteric junction
is a minimally invasive approach to treating VUR
[11]. Surgical intervention may be needed in children who have recurrent infections along with
high-grade VUR [12]. Therefore, VUR imaging
© Springer Nature Switzerland AG 2021
P. S. Sidhu et al. (eds.), Contrast-Enhanced Ultrasound in Pediatric Imaging,
https://doi.org/10.1007/978-3-030-49691-3_14
141
142
S. J. Back et al.
in children is of great importance to determine
reux severity and plan for clinical management.
14.1.2 Imaging ofVesicoureteral
Reux
For many decades, uoroscopic voiding cystourethrography (VCUG) and radionuclide cystography
(RNC) have been the standard modalities for VUR
imaging. However, both of these methods expose
the ovaries and testes to ionizing radiation.
In the early 1980s, a radiation-free alternative
method was developed using ultrasonography
and ultrasound contrast agents (UCA), nowadays
termed contrast-enhanced voiding urosonography (ceVUS). Initially, rst-generation UCA,
comprised of air-lled microbubbles stabilized
with galactose and palmitic acid, was used for
ceVUS [13–15]. Levovist® (Schering AG, Berlin,
Germany) was the rst of these UCA to obtain
approval for intravesical pediatric use in some
European countries, but later the pharmaceutical
company voluntarily withdrew Levovist® from
the market as better UCA emerged.
In the early 2000s second-generation UCA,
composed of gas-lled microbubbles, became commercially available. SonoVue® (Bracco Imaging
S.p.A., Milan, Italy), or known as Lumason®
(Bracco Diagnostics Inc., Monroe Township, NJ,
USA) in the United States, is the most commonly
used second-generation UCA for ceVUS in children. It consists of sulfur hexauoride gas microbubbles stabilized within a phospholipid outer shell.
The improved physical and chemical characteristics
of SonoVue
echogenic effect of the microbubbles [16, 17]. This
combined with the continuous improvement of the
ultrasound imaging techniques and contrast-specic software further boosted the diagnostic performance of ceVUS, allowing the detection of
extremely small quantities of the UCA.
Since the past 20 years, ceVUS has been performed extensively in Europe and has been
shown to be a safe and highly sensitive imaging
method for the detection and grading of
VUR. More recently ceVUS has been used for
urethral pathology. Numerous studies detail the
comparative performance of ceVUS with VCUG
®
increased the stability and enhanced
and RNC with cumulative evidence of the high
diagnostic accuracy of ceVUS [18–38]. As a
result of this experience, ceVUS is performed as
the rst and only imaging examination in several
radiology departments, completely replacing the
two other reux imaging studies [22, 32, 39].
In 2012, the European Society of Pediatric
Radiology (ESPR) endorsed ceVUS examination
for the rst time in the imaging recommendations
and guidelines published in the eld of pediatric
uroradiology [40]. At the same time, the European
Federation of Societies for Ultrasound in
Medicine and Biology (EFSUMB) launched an
updated set of guidelines on the applications of
contrast-enhanced ultrasound including the use
of ceVUS in children with an emphasis on the
indications, technical performance, safety, and
diagnostic efcacy of the examination [41, 42].
®
In 2014 SonoVue
was introduced for the rst
time in the United States market under the trade
name Lumason®. In 2016 Lumason® received
approval by the United States Food and Drug
Administration (FDA) for intravesical applications of reux and urethral imaging studies in
children and in 2017 SonoVue® was also approved
by the European Medicines Agency (EMA) for
the same indication, opening new possibilities for
the wider acceptance of this technique. Optison™
(GE Healthcare Inc., Princeton, NJ) is another
second-generation UCA commercially available
in the United States that has been used off-label
for ceVUS in a prospective clinical trial and a
couple of case reports [20, 43, 44].
14.1.3 Indications forReux Imaging
The National Institute for Health and Clinical
Excellence (NICE) in 2007 and the American
Academy of Pediatrics (AAP) in 2011 revised
their UTI guidelines for febrile infants and young
children [45, 46]. The updated guidelines now
emphasize on identifying children who are most
at risk for UTI and long-term sequelae, tailoring
investigations and management to prevent future
renal damage.
Imaging investigation for VUR detection is now
recommended in children after the rst febrile UTI
if ultrasonography shows urinary tract dilation,