DOI:10.2214/AJR.07.3919
AJR 2009; 193:128-135
© American Roentgen Ray Society
Doppler Ultrasound Findings in the Hepatic Artery Shortly After Liver Transplantation
Ángeles García-Criado1,
Rosa Gilabert1,
Annalisa Berzigotti1 and
Concepción Brú1
1 Department of Radiology, Clinic Hospital of Barcelona, Villarroel 170, 08036
Barcelona, Spain.
Received February 27, 2008;
accepted after revision December 13, 2008.
Address correspondence to Á. García-Criado
(magarcia{at}clinic.ub.es).
Abstract
OBJECTIVE. The purpose of this article is to describe the Doppler
waveform findings in the hepatic artery in the early posttransplantation
period, both in the absence and presence of arterial complications.
CONCLUSION. The presence of transient high-resistance Doppler
waveforms in normal hepatic arteries is a common finding after grafting.
Hepatic artery thrombosis and stenosis, and arterial steal syndromes can be
diagnosed by Doppler in the early liver transplantation period.
Keywords: Doppler sonography • hepatic artery • liver transplantation • sonography • ultrasound
Introduction
Hepatic artery complications are one of the most frequent causes of
morbidity and graft loss in the immediate period after liver transplantation
because they can lead to liver graft ischemia
[1]. The early detection of
these complications is critical to treat them promptly and to reduce the liver
damage. A surveillance program based on color Doppler ultrasound (CDUS) in the
first days after liver transplantation has proven to be effective for the
early diagnosis of hepatic artery complications, and it is now considered a
standard of care [2,
3]. However, the interpretation
of Doppler findings in the immediate posttransplantation phase may be
difficult because the hepatic artery waveform also is commonly altered in the
absence of complications [4].
Moreover, the same Doppler findings can be observed in different
complications. The aim of this article is to describe the Doppler waveforms of
the hepatic artery in the immediate posttransplantation period, both in
patients with a normal artery and in those with arterial complications.
Doppler Arterial Findings in the Immediate Posttransplantation Period
The normal hepatic artery shows a low-resistance waveform with continuous
diastolic blood flow. The resistive index (RI) is the most commonly used
Doppler parameter in hepatic artery evaluation. It allows a semiquantitative
estimation of the resistance to arterial flow into the liver and its normal
value, both in healthy individuals and those with transplants, and it ranges
from 0.55 to 0.80 [5]
(Fig. 1).
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Fig. 1 —Color Doppler ultrasound study in 57-year-old woman 24 hours
after grafting shows patent hepatic artery. Pulsed Doppler ultrasound at
intrahepatic level (arrow) shows normal waveform with resistive index
of 0.76.
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In the first days after liver transplantation, almost half of patients have
a transient high RI at the hepatic artery that will return to normal in a few
days if there are no complications
[4]. According to the degree of
resistance, the high RI has been classified by García-Criado et al.
[4] into four types: type 1, RI
> 0.80 with continuous blood flow in the diastolic phase
(Fig. 2); type 2, RI = 1,
complete absence of the diastolic signal and preserved systolic velocity
(Fig. 3); type 3, absence of
diastolic signal and diminished systolic velocity
(Fig. 4); and, in severe cases,
type 4, undetectable Doppler flow. The last two types are a further
progression of the transient high-resistance flow, but these spectral
waveforms are indistinguishable from the arterial hypoperfusion secondary to
some arterial complications. Therefore, when a type 3 pattern appears in the
immediate postoperative period, it is mandatory to be alert and to perform
daily CDUS, suspecting a complication when the waveform does not become normal
within 4 days. In these cases, CT angiography (CTA), MR angiography (MRA), or
arteriography is indicated. In patients with a type 4 waveform indicating
undetectable arterial CDUS flow, CDUS (if possible), CTA, or MRA is indicated
to exclude hepatic artery thrombosis. If a patent artery is seen, a daily CDUS
examination is mandatory until the flow becomes normal.
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Fig. 2 —On second day after liver transplantation in 61-year-old
woman, Doppler waveform of hepatic artery at hilus (arrow) shows
high-resistance flow with presence of diastolic phase (resistive index of
0.88). This is waveform type 1 of García-Criado classification
[4].
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Fig. 3 —Absence of diastolic phase with normal systolic phase in
Doppler waveform of hepatic artery 24 hours after liver transplantation in
58-year-old man (resistive index = 1), waveform type 2.
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Fig. 4 —Doppler ultrasound of hepatic artery at hilus
(arrow) 24 hours after liver transplantation in asymptomatic
44-year-old man shows high-resistance flow in hepatic artery without diastolic
phase, as in Figure 3; but in
this patient diminished systolic velocity (type 3) is also present.
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Early and transient high RI, which has been shown to be related to an older
donor and a prolonged period of ischemia, lacks clinical repercussions and
long-term prognostic implications
[4].
Doppler Findings in Posttransplantation Hepatic Artery Complications
Hepatic Artery Thrombosis
Early hepatic artery thrombosis is the most serious arterial complication
after liver transplantation and has an incidence of 5-7% in adults and 11% in
children. Because the blood supply to the biliary tree is entirely arterial,
abnormal results on liver function tests are often its first manifestation.
However, hepatic artery thrombosis can be diagnosed at CDUS in the
presymptomatic phase, allowing early reperfusion that obviates
retransplantation [6]. Patients
with hepatic artery thrombosis who are treated by revascularization before the
development of clinical or laboratory alterations have a lower incidence of
late biliary complications [2],
which emphasizes the importance of performing close Doppler monitoring after
liver transplantation.
The ultrasound diagnosis of hepatic artery thrombosis is based on the
absence of Doppler arterial signal at the hilus as well as in the intrahepatic
arterial branches (Figs. 5A,
5B,
5C,
5D, and
5E). A high-resistance flow at
the hilus (RI = 1) may be observed if the Doppler waveform is obtained in the
main hepatic artery before the thrombus.
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Fig. 5C —Ultrasound of liver graft in 56-year-old man with hepatic
artery thrombosis. Contrast-enhanced ultrasound reveals no arterial perfusion
in early phase at hilus level (arrow) nor at intrahepatic level.
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Occasionally, low arterial flow may provoke a false-positive diagnosis of
hepatic artery thrombosis. Contrast-enhanced ultrasound can be useful in these
cases because it improves the sensitivity and accuracy of Doppler ultrasound
for hepatic artery flow detection. Moreover, contrast-enhanced ultrasound
helps to decrease the scanning time
[7,
8] (Figs.
5A,
5B,
5C,
5D, and
5E). When contrast-enhanced
ultrasound cannot be used, other noninvasive imaging techniques such as MRA or
CTA can be performed after Doppler ultrasound and before arteriography.
False-negative diagnoses of hepatic artery thrombosis have been described
in late phases after grafting when periportal collateral arteries develop at
the site of thrombosis. Unfortunately, the collateral flow is often inadequate
to allow satisfactory intrahepatic biliary perfusion. To correctly establish
the diagnosis, remember that the Doppler signal in the arterial collateral
vessels shows a pattern with prolonged systolic acceleration time and low RI
[9]. This pattern is
nonspecific of hepatic artery thrombosis and can also be found in hepatic
artery stenosis.
Hepatic Artery Stenosis
Hepatic artery stenosis is a frequent complication after liver
transplantation, with an incidence of 4-10%
[10]; in severe cases it may
cause liver ischemia and graft loss. However, this complication frequently
causes a subtle form of graft dysfunction, which delays the diagnosis.
Hepatic artery stenosis may be suspected when an intrahepatic Doppler
waveform shows a prolonged systolic acceleration time (
0.08 second) and a
low RI (< 0.5) [9] (Figs.
6A and
6B). In these cases, a
meticulous Doppler study along the course of the main hepatic artery is
mandatory because the detection of a focal peak velocity greater than 2 m/s is
diagnostic for hepatic artery stenosis
[9]
(Fig. 6C). When an increased
focal peak systolic velocity is not detected along the course of the hepatic
artery, the differential diagnosis must include hepatic artery thrombosis with
the development of collateral vessels. In these cases, contrast-enhanced
ultrasound examination has been advised, although it does not obviate an
angiographic study to establish the diagnosis
[11].
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Fig. 6B —Hepatic artery stenosis in 39-year-old man. Flow of
intrahepatic artery shows diminished pulsatility and small difference between
systolic and diastolic velocities that result in low resistive index of
0.40.
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Pseudoaneurysm of the Hepatic Artery
Even if pseudoaneurysm of the hepatic artery is an infrequent complication
after liver transplantation, its potential for rupture and subsequent fatal
hemorrhage makes early diagnosis important. The ultrasound diagnosis is based
on detection of a predominantly cystic lesion at the hepatic hilus, which
fills with color on CDUS and presents an arterial Doppler waveform (Figs.
7A,
7B, and
7C).
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Fig. 7B —Pseudoaneurysm of hepatic artery in 60-year-old woman after
liver transplantation. Color Doppler ultrasound shows complete filling of
collection with turbulent flow (arrow). Note situation of collection
above main portal vein (arrowhead), which is usual location of
hepatic artery.
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Arterial Steal Syndromes
The arterial steal syndromes have only recently been recognized as a cause
of hepatic hypoperfusion after liver transplantation. These syndromes are
characterized by low arterial flow toward the graft caused by a shift of flow
into the splenic artery, called splenic artery steal syndrome, the most
frequent; or into the gastroduodenal artery, called gastroduodenal artery
steal syndrome.
Angiography is mandatory for the diagnosis. The criteria are the presence
of an enlarged splenic artery ( 4 mm or 150% of the hepatic artery
diameter) and dynamic findings in relation to hypoperfusion of the liver
[12].
Data about the use of Doppler ultrasound in this syndrome are scarce and
include nonspecific findings such as loss of hepatic artery flow signal,
decrease of hepatic artery flow velocities, or high-resistance waveform with
an elevated RI in the main hepatic artery
[13]. A total absence of the
diastolic phase with low systolic peaks in the hepatic artery seems to be more
specific [14]; however, this
kind of waveform can also be found in the absence of arterial complications
during the first days after liver transplantation
[4]. In this latter case, no
clinical or laboratory data of hypoperfusion are observed, and, most
important, the waveform normalizes spontaneously some days later. In general,
an arterial steal syndrome must be suspected when a high arterial resistance
flow does not normalize within a few days after liver transplantation.
In some arterial steal syndromes, the flow in the intrahepatic artery is
scarce and slow and is not detectable on CDUS; in such situations,
contrast-enhanced ultrasound can be used to confirm arterial permeability
(Figs. 8A,
8B,
8C,
8D,
8E,
8F, and
8G).
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Fig. 8C —Splenic artery steal syndrome in 53-year-old man 4 days after
liver transplantation. Contrast-enhanced ultrasound (SonoVue) shows patent
hepatic artery (arrow). Note that filling of hepatic artery is
delayed; also note simultaneous filling of portal vein.
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Fig. 8E —Splenic artery steal syndrome in 53-year-old man 4 days after
liver transplantation. Arteriography reveals sluggish flow at hepatic artery
(arrow) associated with early and intense filling of splenic artery
(arrowhead), which is enlarged.
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Other ultrasound findings supporting the diagnosis are based on the
accepted angiographic criteria, such as the presence of splenomegaly and of a
large splenic artery with high blood flow velocity (Fig.
9A,
9B,
9C, and
9D), but no precise data have
been reported.
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Fig. 9B —Spleen ultrasound findings in 55-year-old woman with splenic
arterial steal syndrome. Enlarged splenic artery in its entire course is seen
on B-mode ultrasound (arrow). Figure shows splenic artery near its
origin. Note location of aorta (arrowhead) and mesenteric artery
(double arrowhead).
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Fig. 9C —Spleen ultrasound findings in 55-year-old woman with splenic
arterial steal syndrome. Pulsed Doppler ultrasound shows high blood flow
velocity in splenic artery at its origin (C) and at splenic hilus
(D), with maximum velocities of 2 m/s for entire course.
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Fig. 9D —Spleen ultrasound findings in 55-year-old woman with splenic
arterial steal syndrome. Pulsed Doppler ultrasound shows high blood flow
velocity in splenic artery at its origin (C) and at splenic hilus
(D), with maximum velocities of 2 m/s for entire course.
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Abstract
Introduction
