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14 Contrast-Enhanced Voiding Urosonography (ceVUS): Current Experience andAdvanced Techniques
143
scarring or other ndings that would suggest highgrade VUR or obstructive uropathy, as well as in
other atypical or complex clinical circumstances.
In view of these updated guidelines, the implementation of ceVUS provides a radiation-free imaging
alternative for VUR imaging that can be used for
the initial diagnosis, follow up, as well as for
screening siblings of children with known reux.
14.2 How toPerform ceVUS
The ceVUS examination is performed in a similar
manner to VCUG [47]. The urinary bladder is
catheterized and lled in a retrograde manner with
UCA and saline under continuous, real-time ultrasound (US) surveillance using contrast specic,
harmonic imaging software with low mechanical
index techniques. For newborns and infants, a 2–9
MHz linear or 5–8 MHZ convex transducers are
used, whereas for older children a convex multifrequency (1–5MHz) transducer is used [22, 47].
Initially, aseptic bladder catheterization is performed using a small catheter without a retention
balloon (feeding tube catheter). The size of the
catheter varies according to the child’s age and
usually ranges from 5 to 8 French. Then, the UCA
is reconstituted according to the manufacturer’s
package instructions and it is administered into the
bladder. Two techniques have been described in
the literature for intravesical UCA administration:
1. Injection technique: UCA is directly injected
into the partially lled bladder, which is then
lled with normal saline via gravity up to the
point of voiding or at least maximum expected
bladder capacity in milliliter as calculated by
the formula (age+2)×30 [48]. In this technique, a bolus dose of 0.5–1mL of SonoVue®
is reported to be sufcient for optimal ceVUS
performance [32, 36].
2. Infusion technique: UCA is initially diluted
in a normal saline bag and then the solution
is infused into the bladder by gravity.
Usually, 0.5 or 1mL of SonoVue® is diluted
into a 250 or 500mL of a normal saline bag,
to produce a solution of 0.2% of UCA/normal saline, although a dose up to 1% of the
bladder capacity is described [22, 23]. Using
Optison™, a 0.2% Optison™/normal saline
solution is sufcient [20]. Optimal bladder
lling results in a homogenous bladder distribution, which allows for better delineation
of the posterior bladder wall and better
imaging of a retro-vesical portion of the ureters (Fig. 14.1). The infusion technique is
Fig. 14.1 Optimal concentration of the UCA within the
urinary bladder. Grayscale (left) and contrast mode (right)
with contrast microbubbles homogenously distributed
within the bladder. The retro-vesical space is well seen
behind the posterior wall of the urinary bladder. A strong
acoustic shadow is related to the bladder catheter (arrow)
144
S. J. Back et al.
considered to be advantageous to have a
homogenous UCA concentration without
causing strong acoustic shadowing [22].
During the lling and voiding phases, realtime scanning of the bladder and right and left
kidney is performed alternatively in longitudinal
and transverse planes with the child lying in
supine, prone, or decubitus positions. A lateral
approach in the coronal plane through the ank
may enable simultaneous depiction of the entire
urinary tract including the bladder, ureters
throughout their course and the kidneys in a single image [22] (Fig.14.2).
When the child voids, the urethra is evaluated, with and without a catheter present, using
a suprapubic or trans-perineal/trans-scrotal
approach in boys and usually a suprapubic or
trans-perineal/trans-labial approach in girls
[22, 23, 29, 49] (Figs.14.3, 14.4, and 14.5). In
infants, more than one ceVUS lling/voiding
cycle is generally performed with the catheter
left in place during voiding [50]. In older children, the catheter can be removed once the
expected bladder capacity is reached, and the
child voids.
The reuxing UCA is depicted as echogenic
microbubbles owing retrograde within the urinary tract. Depending on the anatomic level of
urinary tract involvement and the volume of
reuxing UCA, VUR can be graded with ceVUS
into a ve-grade scale in a similar manner as in
VCUG [51].
During continuous US scanning, the region of
interest can be depicted in a single image in con-
Fig. 14.2 Coronal view from the ank. Contrast mode
image. The signal from the background soft tissues has
been suppressed and only the bright echoes from the
reuxing microbubbles can be identied within the pelvicalyceal system and ureter. The left kidney is scanned in
the coronal plane from the ank. From this view, the
entire urinary tract from the pelvicalyceal system (arrow)
to the bladder dome (dashed arrow) can be visualized in a
single image and thus the degree of ureteral tortuosity
(arrowhead) is better evaluated
Fig. 14.3 Normal male urethra. Suprapubic approach.
Grayscale (left) and contrast mode (right). In this technique, the ultrasound transducer is placed in the low
suprapubic region, just above the pubic bone. The structure closer to the ultrasound transducer is the bladder
neck. Echogenic microbubbles are seen owing from the
bladder through the urethra lumen (arrow) during micturition. The bladder catheter (arrow) remains in situ during
micturition
14 Contrast-Enhanced Voiding Urosonography (ceVUS): Current Experience andAdvanced Techniques
145
Fig. 14.4 Normal male urethra. Trans-perineal approach.
Contrast mode image. In this technique, the ultrasound
transducer is placed in the midline of the perineum. The
structure closer to the ultrasound transducer is the anterior
Fig. 14.5 Normal female urethra. Suprapubic approach.
Grayscale (left) and contrast mode (right) with echogenic
microbubbles are seen owing from the bladder (asterisk)
through the urethral lumen (arrow) during micturition,
urethra (arrowheads). The posterior urethra (arrow) is normal. Echogenic microbubbles are seen owing from the
bladder (asterisk) through the urethra lumen during
micturition
which appears with normal conical conguration. The
bladder catheter remained in situ during micturition
(arrowhead)
trast specic mode or as a dual display where the
US screen is split into two parts and the region of
interest is depicted simultaneously in grayscale
and contrast modes. The dual display is helpful
to serve as a reference image to maintain transducer positioning over the region of interest.
Contrast specic algorithms have been developed to increase the conspicuity of microbubbles. Contrast US technology combines low
mechanical index and intermittent pulse US
technology that decreases the breakage of the
microbubbles under the US acoustic pressure.
Subtraction techniques provide effective separation between the background tissues and the
contrast agent signals for improved diagnostic
information and shortened examination time.
Color overlay mode combines the contrast agent
and grayscale signal for real-time anatomic and
146
S. J. Back et al.
contrast information display simultaneously in a
single image.
14.3 Interpretation ofceVUS
Imaging Findings
14.3.1 Reux Grading
VUR grading for ceVUS was adopted from scoring systems established for other reux imaging
examinations [51]. The most commonly used
VUR scoring system was initially proposed for
the International Reux Study in Children (IRSC)
to describe ndings on VCUG [52]. It uses a 1
(lowest) to 5 (highest) scale based on whether
contrast material reuxes only into the ureter or
reaches the upper collecting system as well as the
degree of ureteral dilation and tortuosity, and
upper collecting system dilation. The ceVUS
VUR grading proposed by Darge and Troeger is
an extrapolated classication derived from the
IRSC uoroscopic scoring and built on earlier
authors’ experience with voiding sonographic
examinations using saline and rst-generation
UCA [51] (Figs. 14.6, 14.7, 14.8, 14.9, and
14.10). US has the added advantage over VCUG
and RNC in that it depicts pre-existing urinary
Fig. 14.6 Ureteral reux. Grayscale (left) and contrast
mode (right). Behind the bladder, the retro-vesical part of
the right ureter can be visualized moderately distended and
Fig. 14.7 Grade II reux. Grayscale (left) and contrast mode (right) of the right kidney. Reuxing microbubbles can
be identied within the pelvicalyceal system of the right kidney, which is not dilated (arrow)
lled with echogenic microbubbles (arrow). The dilated left
distal ureter is lled with clear anechoic uid content thus
demonstrating the absence of reux (arrowhead)
14 Contrast-Enhanced Voiding Urosonography (ceVUS): Current Experience andAdvanced Techniques
Fig. 14.8 Grade III VUR.Contrast mode images of the right kidney longitudinal (left) and axial (right) planes. There
is moderate dilation of the renal pelvis and calyces with minimal blunting of the fornices (arrow)
147
Fig. 14.9 Grade IV VUR. Contrast mode image of the
right kidney. Echogenic microbubbles are seen within the
dilated pelvis and calyces (arrow) with blunting of fornices. The papillary impressions are preserved
tract dilation prior to a VUR event. The initial
ceVUS scoring system proposed “a” and “b”
subcategories for each of the ve grades of reux
denoting if the system was primarily nondilated
or dilated, however, this notation has not been
widely used. The ve reux grades are:
• Grade I: reuxing UCA microbubbles reaches
the ureter.
• Grade II: reuxing UCA microbubbles reach
up to the pelvicalyceal system, without dila-
tion of the pelvicalyceal system.
Fig. 14.10 Grade V VUR. Contrast mode image of the
right kidney in the longitudinal plane. Echogenic microbubbles are seen within the severely dilated pelvis and
calyces (arrows), with loss of the papillary impressions
and tortuously dilated proximal ureter (arrowhead)
• Grade III: reuxing UCA microbubbles reach
up to the pelvicalyceal system, which is mildly
dilated, but with no signicant change of the
renal calyceal contour.
• Grade IV: reuxing UCA microbubbles
reach up to the pelvicalyceal system, which
is moderately dilated with blunting of the
renal fornices but papillary impressions still
visible.
• Grade V: reuxing UCA microbubbles reach
up to the pelvicalyceal system, which is
severely dilated with loss of papillary impressions and tortuous course of the ureter.
148
S. J. Back et al.
Less often a three-grade scoring system, such
as the one used to grade VUR by RNC, is used
for ceVUS [15, 38]. Of note, in an in-vitro experiment, it was shown that UCA microbubbles do
not passively ascend into the upper urinary tract,
and therefore the demonstration of microbubble
in the renal collecting system corresponds to
active VUR [53].
The less common phenomenon of intrarenal
reux is detectable by ceVUS and was comparable to detection by VCUG in a small series [43,
54]. With the more advanced contrast specic US
modalities, intrarenal reux appears to be
detected more frequently. While not a component
of the reux scoring system, identication of
intrarenal reux may aid in risk stratication for
renal scarring [54] (Fig.14.11). Intrarenal reux
Fig. 14.11 Intrarenal reux. Contrast mode image.
Echogenic microbubbles are extend from the calyces diffusely into the renal parenchyma (arrows)
is usually associated with compound papillae,
which are more frequently found in the upper
pole, and to a lesser extent in the lower pole of
the kidney [55].
ceVUS can also provide anatomic details
about the morphology of the pelvicalyceal system and detect reux in cases of complete or partial ureteral duplication (Figs.14.12 and 14.13).
14.3.2 Urethra
Assessment of the urethra for the presence of
posterior urethral valves (PUV) is an important
part of the evaluation of the urinary tract in male
infants and those with signs and symptoms suggesting lower urinary tract obstruction. Teele and
Share [56] and Cohen et al. [57] separately
described the utility of trans-perineal US to evaluate the bladder base and urethra in children and
showed this approach was complimentary and
favorable when compared with trans-pelvic
imaging in a non-voiding infant. Using VCUG as
a gold standard, Good etal. evaluated the diameter of the obstructed and non-obstructed posterior
male urethra at rest and with voiding [58]. They
showed signicant differences in the diameter of
the posterior urethra between non-voiding and
voiding in both the non-obstructed and obstructed
states. The non-obstructed posterior urethra had a
mean diameter of 1mm pre-void compared with
4mm while voiding; and obstructed urethras had
a mean diameter of 4.5 and 10mm pre-void and
Fig. 14.12 Vesicoureteral reux into a duplicated collecting system. Contrast mode of a duplex left kidney.
There is reux Grade III to the lower pole of the kidney
(arrow) and mild dilation of the proximal ureter (arrow-
head). There is no reux to the upper renal pole (dashed
arrow) in keeping with complete duplication of the collecting system
14 Contrast-Enhanced Voiding Urosonography (ceVUS): Current Experience andAdvanced Techniques
149
Fig. 14.13 Duplex kidney incomplete duplication. The
right kidney has a duplex conguration. Echogenic microbubbles are seen reuxing into the dilated upper (dashed
arrow) and lower (arrow) poles. At a lower level, the two
separate ureters (arrowheads) are moderately dilated and
Fig. 14.14 Normal male urethra. Trans-perineal
approach. Grayscale (left) and contrast mode (right). The
image is rotated 180° to resemble the classic voiding cystourethrography examination. The ultrasound transducer
is placed in the midline of the perineum. During micturition, the urethral lumen is lled with echogenic microbubbles which are seen owing from the bladder
both lled with echogenic microbubbles. These ndings
are suggestive of a partially duplicated collecting system
with two ureters joined together into one distal ureter
inserting into the bladder
(asterisk). The structure closer to the ultrasound transducer is the anterior urethra (arrowheads). The posterior
urethra (arrow) is normal in caliber and conguration. The
difference in the caliber between the posterior and anterior urethra should not exceed 2 mm. (Courtesy of Dr.
C. Duran. Parc Tauli University Hospital, Sabadell,
Barcelona, Spain)
voiding, respectively [58]. Applying a cut-off of
6 mm for the posterior urethra during voiding
yielded a sensitivity of 100% and specicity of
89% for obstruction [58] (Figs.14.14 and 14.15).
Using Good etal.’s threshold of 6mm, Mate
et al. identied abnormal urethras in 4 of 224
boys, assessing for PUV, examined with the rst
generation galactose based UCA during ceVUS
and conrmed the ndings with VCUG [59].
Bosio and Manzoni correctly identied 8 of 100
boys with PUVs using ceVUS by assessing for
dilation of the posterior urethra, delayed passage
150
S. J. Back et al.
Fig. 14.15 Normal male urethra. Trans-perineal
approach. Serial images. Contrast mode serial images. All
images are rotated 180° clockwise to resemble the classic
voiding cystourethrography examination. The ultrasound
transducer is placed in the midline of the perineum. The
catheter is withdrawn from the bladder (asterisk) during
of UCA through a narrowed segment, and less
distension of the anterior urethra [60]. Findings
were conrmed with VCUG.Following their initial publication, the group added an additional
110 boys in their study and recognized PUV in
one child using similar criteria to their initial
group. Recently, Duran etal. showed that newer,
more stable second-generation UCA could be
reliably used to image the urethra [29].
Independently, Berrocal etal. [61] and Duran
etal. [29, 49] derived similar normative measurements of the urethra obtained while voiding during
voiding. The urethra is lled with echogenic microbubbles. The posterior (arrow) and anterior (arrowhead) urethra are normal. The bladder empties completely.
(Courtesy of Dr. C.Duran. Parc Tauli University Hospital,
Sabadell, Barcelona, Spain)
ceVUS in boys and girls. They showed that urethral assessment is no longer a limitation to the use
of ceVUS as a primary evaluation of the urinary
tract in children and particularly in boys. The
authors respectively reported normal posterior
male urethral measurements during voiding of
6.3 ± 0.66 mm (range: 3.7–7.2 mm) and
6.4 ± 0.78 mm (range: 4–9.2 mm); and anterior
male urethral values of 6.1 ± 0.81 mm (range:
2.8–7.1 mm) and 5.8 ± 0.91 mm (range: 3.3–
8.9mm) [29, 61]. For girls, Berrocal etal. reported
a mean urethral diameter during voiding of 4.2
14 Contrast-Enhanced Voiding Urosonography (ceVUS): Current Experience andAdvanced Techniques
®
most commonly SonoVue
and to a lesser
extent Optison™. In these studies, more than
2600 children have been included and more
than 5200 pelvi-ureter-units (PUUs) have been
analyzed. In most studies, the diagnostic performance of ceVUS was reported to be at least
comparable to standard VCUG and RNC and in
many studies even higher [18–20, 22–29, 31–
34, 36, 39, 43, 44, 64–67]. Overall, it is consid-
ered that ceVUS detects approximately 10%
more reux cases compared to VCUG [50, 63].
Most important is to note that 70% of reux
cases detected only on ceVUS were of higher
grades (II–V) and thus of higher clinical signicance [68]. The high sensitivity of ceVUS
Fig. 14.16 Spinning top urethra and vaginal reux.
Suprapubic approach. Contrast mode image of the urethra
during micturition depicting the “spinning top” urethral
morphology (arrow) as well as intravaginal reux (arrowhead). “Spinning top” urethra refers to the non-obstructive
widening of the posterior urethra that occurs in girls with
a weak bladder neck mechanism and concomitant voluntary contraction of the distal sphincter. It is considered
suggestive of functional discoordinate voiding or bladder
instability. The bladder (asterisk) is lled with echogenic
microbubbles
might be explained by the fact that even a few
reuxing microbubbles can be easily depicted
with advanced contrast-specic software,
whereas in VCUG, a larger amount of reuxing
iodinated contrast is required to be visualized
especially in the presence of pre- existing urinary tract dilation. Moreover, the lack of ionizing radiation enables prolonged, real- time
examination of each kidney separately and thus
higher sensitivity in detecting intermittent or
intrarenal reux [50, 54, 68].
±1.01mm (range: 2.5–7.8mm) and Duran a mean
diameter of 5.9±1.1mm (range: 4–9mm) [61].
In addition to posterior urethral valves, ceVUS
has depicted urethrovaginal reux, spinning top
urethra, anterior urethral valves, urethral diverticula, prostatic utricles, and bulbar strictures [22, 23,
29, 49, 61] (Fig.14.16). Patel etal. reported a case
of duplicated urethra seen during ceVUS [62].
On the other hand, VCUG has a higher sensitivity to detect grade I reux, because the reuxing retro-vesical ureters may be difcult to
delineate from their echogenic surroundings, particularly if these are non-dilated [63]. However,
grade I reux is of uncertain clinical signicance
and in many cases does not even require
treatment.
In a recent meta-analysis including a total of
12 comparative ceVUS studies using VCUG as
14.3.3 Diagnostic Comparisons:
ceVUS vs VCUG andRNC
the reference standard and performed in 953 children, the pooled diagnostic accuracy parameters
for ceVUS in detecting VUR in children were as
Multiple studies have shown that ceVUS has
high diagnostic sensitivity and specicity compared to VCUG and RNC for detection and
grading or reux [63]. Up to 2019, 20 original
research studies have been published entailing
the comparative performance of VCUG and
ceVUS with the use of second-generation UCA,
follows: sensitivity 90.43% (95% CI 90.36–
90.50), specicity 92.82% (95% CI 92.76–
92.87), calculated positive likelihood-ratio 12.59
(95% CI 12.49–12.68), negative likelihood-ratio
0.103 (95% CI 0.102–0.104), and extrapolated
pooled diagnostic odds ratio was 122.12 (95% CI
120.75–123.49) [35, 37].
151
152
S. J. Back et al.
shown in adults with improved measurements
and detection of brosis [73].
The addition of UCA has improved visualization of adult urethras during sonourethrography
in the assessment of trauma [74], diverticula and
incontinence [75, 76], as well as long, narrow
strictures [72].
14.3.5 Complex Genitourinary
Anatomy
Fig. 14.17 Urogenital sinus. Suprapubic approach.
Contrast mode image depicts a long urethra (arrow) in this
infant with ambiguous genitalia. A communication
(arrowhead) between the posterior urethra and the vagina
(asterisk) was seen during the voiding phase of the examination. Contrast material lled the vagina
14.3.4 Retrograde Urethrography
Sonourethrography was rst described by
McAninch et al. in 1988 [69]. It is performed
after catheterization of the urethra and retrograde
lling with normal saline. In the literature, its use
is primarily described in adults where the detection of strictures is comparable to uoroscopic
retrograde urethrography (RUG) [70]. There is
reportedly improved sensitivity for measurement
of stricture length and diameter with sonourethrography versus uoroscopic retrograde urethrography (RUG) when compared with operative
ndings, especially shorter strictures, which is
attributed to differences in positioning and degree
of penile stretch during the examination [70, 71].
Some authors found the radiographic technique
underestimated stricture length despite concerns
about magnication, while others concluded
RUG has expected over-measurement of stricture
length due to magnication [72]. Because procedures to repair urethral strictures are predicated
on their length, accurate measurement is crucial
for surgical planning. Sonourethrography can
also detect spongiobrosis, not appreciated by
RUG, that can guide surgical management [70,
71]. In a retrospective analysis of 12 adolescent
patients, mean age 16.9 years (range 9.5–20.8
years), sonourethrography had similar benets as
In a similar manner to RUG and sonourethrography, a persistent genitourinary sinus can be
depicted with UCA administration [22]. The
UCA instilled in the urinary bladder may reux
into the vagina and show a common channel of
the urethra and lower [77, 78] (Fig. 14.17).
Rectourethral communication has also been
shown after the administration of UCA instilled
into the mucous stula of patients with imperforate anus [79].
14.4 Advanced Techniques
14.4.1 3D/4D ceVUS
Currently, ceVUS procedure is based on the standard two-dimensional (2D) US techniques that
provide still images and dynamic cinematic clips
of the urinary tract for anatomic imaging and
morphological evaluations. However, in recent
years, ongoing innovations in sonographic equipment have led to the development of three-dimensional (3D) and four- dimensional (4D) US
techniques that are gaining popularity in the eld
of pediatric uroradiology [33, 80]. 3D/4D US
enables static and real-time multiplanar sonographic imaging simultaneously in all orthogonal
planes and ofine volume rendering reconstructions for selective display of specic tissue
components.
These advanced US techniques coupled with
contrast imaging options can further expand the
diagnostic capability of ceVUS improving volumetric measurements and providing detailed
visualization of contrast within the pelvicalyceal