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80
M. Piskunowicz et al.
c
Fig. 8.16 (continued)
metastasize to the liver include germ cell tumors,
osteosarcoma, and neuroendocrine tumors. Stage
4S NB can present with multiple ill-dened nodules or diffuse liver involvement, whereas stage 4
NB disease involving the liver usually presents
with multiple discrete lesions. The appearances of
hepatic metastasis are expected to mimic those in
adulthood. On grayscale US, they are found to be
predominantly hypoechoic (63.8%) and hyperechoic (28.3%); isoechoic (5.8%) and non-echoic
metastasis (0.4%) and mixed echogenicity (1.7%)
are rare [56]. On CEUS the majority of these
metastases show diffuse homogenous hyperenhancement (55.4%) or rim-like hyperenhancement
(33.3%) during the arterial phase. The vast majority, 99% of the lesions demonstrate washout occurring rapidly during the portal venous phase (97%)
rather than with a delayed washout (2%). Hypervascular metastasis shows a signicant longer
washout time compared to hypo-vascular metastases (Fig.8.17) [56].
A number of very rare malignant tumors are
also found in children and include, cholangiocarcinoma (Fig. 8.18), combined HCC-
a
Fig. 8.17 Neuroendocrine metastasis in a 10-year-old
male with an underlying pancreatic insulinoma. (a)
Grayscale ultrasound shows a hyperechoic nodule (arrow)
within a heterogeneous right liver lobe. (b) On the
contrast- enhanced ultrasound, the arterial phase at 15 s
demonstrates hyperenhancement (arrow). (c) On the
contrast- enhanced ultrasound, washout out of the lesion
(arrow) on the late portal venous phase at 120s
bc
ab
8 Contrast-Enhanced Ultrasound ofPediatric Focal Liver Lesions
Fig. 8.17 (continued)
81
Fig. 8.18 Liver cholangiocarcinoma in a 16-year-old
child. (a) Computed tomography in the venous phase
shows multiple hypoechoic lesions in the liver. (b)
Grayscale ultrasound demonstrates heterogeneous echogenicity within the liver. (c) The contrast-enhanced ultra-
sound examination demonstrates rapid peripheral and
heterogeneous central hypoenhancement of the lesion on
the arterial phase at 23s. (d) The contrast-enhanced ultrasound examination demonstrates washout of during the
late portal venous phase at 137s
82
cd
Fig. 8.18 (continued)
M. Piskunowicz et al.
cholangiocarcinoma, brolamellar hepatocellular
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8.6 Conclusion
The presence of an FLL found inadvertently in
the child on an US examination can often be an
anxious time for the parents, and presents a
diagnostic dilemma for the referring clinical
team. If there is underlying chronic liver disease, a known risk factor or an established primary tumor elsewhere, the clinical management
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nding of an FLL in an otherwise healthy child.
The ability to undergo a CEUS examination, to
safely and accurately characterize the FLL is
immense to alleviate the anxiety of the parents
and to allow subsequent appropriate clinical
management. The introduction of CEUS in the
assessment of an FLL in the child has implications for future imaging strategies and will be
benecial to the child reducing the need for MR
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Pediatric Contrast-Enhanced Ultrasonography (CEUS): Pediatric Transplantation
DorisFranke
9
Abbreviations
CEUS Contrast-enhanced ultrasonography
EBV Epstein–Barr virus
GvHD Graft versus host disease
PTLD Post-transplant lymphoproliferative
disease
RI Resistive indices
UCA Ultrasound contrast-agent
US Ultrasonography
9.1 Introduction
In the assessment before, during, and after solid
organ and stem cell transplantation in children,
ultrasonography (US) is the rst-line imaging
modality, especially in liver and kidney
transplantation.
Doppler Sonography is used for conrmation of vessel patency and diagnosis of vessel
pathologies like stenoses, arterio-venous-stulas, or aneurysms. In some cases, however, it
can be very troublesome even for an experi-
D. Franke (*)
Pediatric Ultrasonography, Department of Pediatric
Kidney, Liver and Metabolic Diseases, Children’s
Hospital, Hannover Medical School,
Hannover, Germany
e-mail: franke.doris@mh-hannover.de
enced investigator to nd the hepatic artery in
a complex liver transplantation or the artery
after renal transplantation. The inability to
identify the artery, a crucial nding, is one of
the indications for contrast-enhanced ultrasonography (CEUS); Table 9.1. CEUS has the
advantage of being available and applicable at
any location, including the operating theater or
the bedside in the bone marrow transplant
patient, and pertinently in the intensive care
unit with the very sick patient. CEUS is repeatable, cost-effective and, especially in children,
safe. Most importantly, CEUS has the potential
to reduce the overall radiation burden in children [1], which is of special impact in the eld
of pediatric transplantation as these children
will already have an overall increased malignancy risk due to immunosuppression and
underlying disease.
Furthermore, CEUS can be of help in pre-,
peri-, and post-transplant complications including perfusion abnormalities, systemic infections,
abscesses, or secondary malignancy, most commonly post-transplantation lymphoproliferative
disorder (PTLD).
No imaging modality has the ability to diagnose allograft rejection or calcineurin inhibitor
toxicity, but imaging can exclude or identify
other complications in the differential diagnosis
for rejection or transplant malfunction such as
biliary or urinary obstruction, bilioma or impaired
vessel patency. Ultrasound is routinely performed
© 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_9
85
86
D. Franke
Table 9.1 Indications for CEUS in pediatric
transplantation
Vascular
Patency of vessels
Arterio venous-stulas
Infarction
Pseudoaneurysm
Transplant renal artery stenosis
Non-vascular
Unclear masses
Unclear focal solid organ lesions
Complicated cysts
Abscess
Intra-cavitary CEUS (biliary system, vesicoureteral
reux, leakage, the position of drainage catheters)
as the initial screening imaging modality for the
detection and follow-up of both early and delayed
complications.
9.2 Liver Transplantation
Liver transplantation is performed for a variety of
benign and malignant conditions of the liver and
biliary system in children. The most common
cause in infants is biliary atresia, followed by
metabolic diseases and other conditions including hepatoblastoma. Depending on the donorrecipient graft size match, whole-organ grafts as
well as right or left split liver grafts are transplanted from deceased donors. Living donated
liver transplants in children are in the majority of
cases left lateral segments (segments II and III)
and only very exceptionally a right liver lobe.
The early detection and treatment of postoperative complications have contributed signicantly
to improved graft and patient survival with reliable imaging playing a critical role [2–5].
Complications after liver transplantation may
be distinguished in vascular and nonvascular.
Early and correct diagnosis is of critical importance [4, 6–9]. Vascular complications include
stenosis and thrombosis of the hepatic artery,
portal vein, inferior vena cava or hepatic veins,
hepatic artery pseudoaneurysm, and arteriovenous stulae [5, 10].
Hepatic artery thrombosis is the most signicant complication as it is usually associated
with graft failure due to biliary complications
and early development of secondary biliary cirrhosis as the bile ducts are solely supplied by
the hepatic artery. Mostly, hepatic artery thrombosis occurs in the early postoperative phase.
Due to the small vessel size in infants and possible anatomical variations, for example, in heterotaxy syndromes, the occurrence of hepatic
artery thrombosis is high with an estimated incidence of 2–12% [9].
Post-operative Doppler US has high sensitivity and specicity for the detection of hepatic
artery thrombosis, but the inability to depict very
low ow in a patent hepatic artery due to either a
post stenotic tardus parvus pattern, an overlaying
turbulent portal vein or reduced cardiocirculatory
perfusion remains a challenge [11–14]. CEUS
can ensure the diagnosis of patency in the hepatic
artery in questionable cases (Fig.9.1a, b).
CEUS is a safe, non-invasive and rapid tool to
detect potential complications and to enable early
intervention following liver transplantation.
When necessary CEUS has been used off-label
for identifying circulatory complications after
liver transplantation in children [2, 3].
Cho etal. investigated the inuence of ultrasound contrast agents (UCA) on spectral Doppler
analysis in liver transplantation recipients. The
measured velocities of graft hepatic vessels
tended to increase after administration of UCA,
but without statistical signicance. The comparison of serial Doppler parameters with or without
injection of UCA is valid during Doppler surveillance in liver transplantation recipients [15].
Portal vein thrombosis occurs in about 3% and
is characterizes by a lling defect on B-mode,
Doppler, or CEUS in the case of a partial thrombosis or a complete lack of enhancement in
occlusion of the portal vein stem or the intrahepatic branches.
Thrombosis of the inferior vena cava or the
hepatic veins is rarer than stenosis of the anastomotic sites, in our experience.
9 Pediatric Contrast-Enhanced Ultrasonography (CEUS): Pediatric Transplantation
a
b
87
Fig. 9.1 (a) CEUS in a liver transplant patient (left lateral
split liver) on the rst day after the operation with questionable patency of the hepatic artery. Depiction of the hepatic
9.2.1 Biliary and other nonvascular complications
The biliary anastomoses are performed between
the donor and recipient common bile duct in fullsize liver transplantations and right lobe liver
artery 10s post injection (arrows). The portal venous bed is
still not enhancing. (b) Enhancement of the portal vein
(arrows) and liver parenchyma 19s post-injection
transplantations. In a left lateral split liver lobe
transplantation, a Roux-Y hepatojejunostomy is
performed. The gallbladder is always removed
during transplantation. Biliary complications
occur in about 10% and are usually seen in the
early postoperative period (within in the rst 3
88
D. Franke
ab
c
Fig. 9.2 Chologenic liver abscesses following an episode
of severe cholangitis in a 14-year-old boy 7 years after left
lateral split liver transplantation with Roux-Yhepatojejunostomy. (a) B mode US imaging shows a
broadened and inhomogeneous periportal area and dilated
bile ducts (arrow). (b) Color Doppler US demonstrates
months), but may also present later due to recurrent cholangitis or inammatory stenosis of the
biliary system.
Biliary complications include obstruction due
to anastomotic and non-anastomotic strictures,
bile leak with biloma formation, recurrence of
the primary disease (e.g., primary sclerosing
cholangitis), infection, abscess formation, and
that the portal vein and the hepatic artery are patent, with
a focal area of altered reectivity adjacent to the portal
vein (arrows). (c) Contrast-enhanced ultrasonography
(CEUS) demonstrates the real extent of the hepatic
abscesses in association with the biliary tree, as intrahepatic areas of non-enhancement (arrows)
development of intraductal stones (Fig.9.2a–c).
Peri-hepatic leaks (biloma) are often located
along the resection site in split liver transplants.
These bilomas may require an US-guided drainage or may resolve spontaneously.
Other complications are post-operative perihepatic uid collections, which may be hematoma, seroma, or biloma.
9 Pediatric Contrast-Enhanced Ultrasonography (CEUS): Pediatric Transplantation
89
More rare complications are abscesses due to
cholangitis or systemic infections and posttransplant lymphoproliferative disease (PTLD).
Contrast-enhanced ultrasound may be useful
in delineating non-vascularized areas, such as
bile duct dilatation, biloma, or an abscess cavity
considered for potential aspiration or catheter
drainage.
9.3 Kidney transplanation
Similar to liver transplantation, early vascular
complications in infants and young pediatric
patients are more frequent than in adults
because of the small vessel diameters [16].
Therefore, in small children, anastomosis of
the donor renal artery and vein is usually performed with the recipient’s aorta and inferior
vena cava or common iliac vein. CEUS has a
promising role in early and late imaging of
vascular complications after renal transplantations such as thrombosis of renal vessels,
patency of polar arteries, arteriovenous stulas, pseudoaneurysm, renal artery stenosis, as
well as in the characterization of indeterminate
renal masses.
The lack of nephrotoxicity is a particular
advantage in CEUS, particularly relevant in renal
transplant patients.
After injection of UCA, three phases of
enhancement are distinguished:
1. The cortical phase starts 8–14 s after UCA
injection with initial intense enhancement in
the renal cortex.
2. The medullary phase follows the cortical
phase UCA enhancement, progressing from
the outer to the inner aspects of the renal
medullae.
3. In the late phase, UCA will disappear rst
from the medullae, later from the cortex. Due
to the high renal perfusion, the transit time
between renal artery enhancement and UCA
arrival in the renal vein is very short, often in
2–3s [17].
CEUS has been shown to be superior to
Doppler US in the detection of renal artery stenosis, which is not unusual following renal transplantation, with an incidence of 5–10% [18].
With Doppler US, a high resistive index (RI) is
associated with vascular complications. CEUS
however reveals information about kidney
allograft microvascular perfusion independent of
the recipient’s vascular compliance and may predict long-term allograft function [19, 20].
In children with delayed allograft function,
vascular causes can be ruled out by Doppler US
or if remaining uncertain, the addition of CEUS
may help.
A frequent nonvascular complication after
renal transplantation is pyelonephritis often associated with a clinical course of urosepsis, which
max results in renal abscess formation (Fig.9.3a–
c). Contrast-enhanced ultrasound may help to
delineate the abscess borders, and allow for percutaneous drainage.
9.4 Special indications and so on
9.4.1 Intra-Cavity CEUS
Intra-cavity CEUS can be performed in the same
way as cholangiography via T-tube or nasobiliary line following liver transplantation [21].
Other indications for intra-cavitary CEUS include
investigations for vesicoureteral reux or urinary
leakage after renal transplantation via a suprapubic or transurethral catheter. Furthermore, it is
easy to control the position of drainage catheters
using intra-cavitary CEUS.For all intra-cavitary
investigations, only a very tiny amount of UCA
diluted in sterile saline solution is necessary. It is
important to use sterile solutions contained in
plastic and not glass bottles, as glass can cause
deactivation of the microbubbles.