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573
False-negative Duplex Doppler Studies in Children with Hepatic Artery Thrombosis After Liver Transplantation
Theodore Sue V. Mc Edward M. Ines Ronald W.
R. Hall1 Diarmid2
G. Grant1 Boechat1 Busuttil3
Recent
who have hepatic the role of duplex Doppler imaging in this population. Among i35 pediatric liver transplant patients, 20 had arteriography for suspected hepatic artery thrombosis. Duplex and/or color Doppler imaging was performed in 13 of these children. The Doppler examination failed to show hepatic artery signals in five patients. Arteriography showed hepatic artery thrombosis artery
reports
describe
thrombosis
in all five.
after
In three
liver
of these,
formation
of collateral
transplantation.
subsequent
This
Doppler
vessels
in children
led us to reevaluate
examinations
showed
reappearance
of
signals. Arteriography confirmed the interval development of collaterals. Hepatic artery signals were found on the Doppler examinations of the remaining eight patients. Four had normal arteriograms, but the remaining four had hepatic artery thrombosis with collateral formation. Patients with hepatic artery thrombosis and collateral circulation tended to have increased diastolic flow (decreased resistive index). In addition, early scans clearly identified patients with complete thrombosis before collateral formation. On the basis of our preliminary experience, a child with a liver transplant and a clinical history strongly suggestive of hepatic artery compromise should have arteriography despite an apparently normal Doppler examination. arterial
AJR
Aeceived
July 7, 1 989:
accepted
October 24, 1989. 1 Department of Aadiological
after
Sciences,
revision
Univer-
sity of California, Los Angeles, School of Medicine, 10833 LeConte Ave., Los Angeles, CA 900241006. Address reprint requests to I. A. Hall. 2 Department of Gastroenterology, University of California, Los Angeles, School of Medicine, Los Angeles. CA 90024-1 006. 3 Department of Surgery. University of California, Los Angeles, School of Medicine, Los Angeles, CA 90024-1 006. 0361 -803x/90/1 © American
543-0573
Roentgen
Ray Society
Doppler
154:573-575,
March
1990
Vascular compromise after liver transplantation may be related to thrombosis of the portal vein, hepatic veins, or hepatic artery [1 ]. Of the three, thrombosis of the hepatic artery is by far the most common. It typically results in sepsis, infarction, hepatic necrosis, bile duct strictures, and graft failure, requiring retransplantation [2-4]. In reports of large series, the prevalence of thrombosis of the hepatic artery ranged from 1 i .8% [5] to as high as 42% [6]. Both invasive and noninvasive techniques are available to establish patency of the hepatic artery. The accuracy of duplex sonography in this regard has been well documented [5, 6]. Recent reports [5, 6] have described formation of arterial collaterals in pediatric liver transplant patients who have thrombosis of the hepatic artery. Flint et al. [5] recently examined this problem and reported that Doppler signals were absent in all children who had thrombosis of the hepatic artery (with or without collaterals). Our study was undertaken after we saw arterial Doppler signals in the livers of two children with angiographically proved thrombosis of the hepatic artery and formation of collateral vessels. This prompted us to review the accuracy of duplex Doppler studies in pediatric liver transplant recipients who have thrombosis of the hepatic artery and collateral circulation.
Materials
and
Methods
Angiograms or autopsy results were reviewed in all pediatric patients with suspected thrombosis of the hepatic artery after liver transplantation. All studies were performed between December i , 1984, and November 30, 1988. Among the 135 transplant recipients younger
than i 7 years, 20 were examined with contrast angiography for suspected thrombosis of the hepatic artery. Seventeen duplex DoppIer studies were performed in i 3 of the 20 patients. The remaining seven patients were seen before the availability of Doppler sonography at our institution and were not included in this study. Duplex Doppler sonography and arteriography were performed within a 48hr period in all except two patients. In these cases angiography was
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delayed 4 and 5 days, respectively, until the patient was stable enough for a contrast-enhanced study. All angiograms were obtained via arterial
puncture
with selective
celiac axis and superior
mesenteric
artery catheterizations. Our protocol for duplex Doppler in the liver transplant patients includes a real-time survey of the liver and adjacent organs, followed by duplex Doppler sampling of the portal vein, hepatic artery, hepatic veins, and intrahepatic inferior vena cava. Hepatic artery thrombosis
was diagnosed signals
were
the region superior
on the basis of Doppler
absent
in the porta
of arterial
mesenteric
hepatis;
anastomosis
artery.
sonography both lobes
from the aorta,
In all patients
in whom
made on the basis of duplex Doppler sonography, obtained All mark eli,
when arterial of the liver; and
celiac axis, or
the diagnosis
was
an angiogram
was
for confirmation.
sonographic
with
four
Laboratories,
or
evaluations were performed Ultramark 9 (Advanced Technology
the ATL
was
every case. The resistive index in the hepatic artery was also calculated in 70 additional pediatric liver transplant recipients with no or radiologic
evidence
ischemia, of liver
graft
parenchyma
failure,
or bile
duct
stenoses
damage.
was confirmed these patients, on subsequent
criteria for diagnosis
by angiography in all five patients. In three of Doppler sonography identified arterial signals examinations.
This
was
thought
0.62). All patients
70 randomly
that
with were
patent
to be con-
confirmed
hepatic
arteries
selected
pediatric
by contrast
on Doppler
angiography
liver transplant
had
recipients
with
normal Doppler studies, the calculated resistive index ranged from 0.55 to 0.91 The mean resistive index in this population was 0.67 (SD = 0.1 ). Differences in the mean resistive index .
of the study population with patent hepatic arteries the control population (0.67) are due to the small patients (n = 4) in the study group.
The clinical courses
of the seven patients
(0.72) and number of
with thrombosis
of the hepatic artery and collateralization showed abnormalities that could be attributed directly to decreased or absent hepatic arterial flow: relapsing bacteremia and septicemia (7/
bile duct strictures
7),
and
initially
and segmental
technically
Among our patients
Results
Five of the 13 patients fulfilled our Doppler thrombosis of the hepatic artery. The sonographic
revealed
a resistive index greater than 0.64 with a calculated mean resistive index of 0.72. In the separate control population of
aging (Ultramark 9), phased-array technology was used. Spectral analysis was performed as part of both duplex and color Doppler examinations. The resistive index ([peak systolic end diastolic velocityj/peak systolic velocity) was calculated retrospectively in
of hepatic
who had angiography
a trend toward increased diastolic flow in the seven patients who had thrombosis of the hepatic artery and collateral circulation. The mean resistive index was 0.52 (range, 0.41-
Both-
the Doppler signal. Wall filters were set at 50 or iOO Hz. Anglecorrected velocity measurements were used whenever the course of the vessel under investigation was visible by using real-time or color Doppler imaging. Duplex Doppler evaluations (Ultramark four) were performed with mechanical sector scanners. For color Doppler im-
signs
hepatic arteries in our patients
sonography
sonographic systems. For real-time and Doppler examina3.0- or 5.0-MHz transducers were used. Frequency selection based on the size of the patient and the quality of the image and
clinical
,
Ultra-
WA)
tions,
sistent with the interval development of collateral circulation. The times between the initial Doppler examination and the appearance of an arterial Doppler signal were 21 48, and 62 days, respectively. Collateral circulation was confirmed by repeat angiography in two of these three patients (Fig. 1). Doppler signals from the hepatic artery were identified in the remaining eight patients. In four of these eight, normal, patent hepatic arteries were seen on angiography. In the other four, thrombosis of the hepatic artery was seen with collateralization. In two of these four patients, color Doppler imaging actually revealed an arterial vessel in the porta hepatis that proved to be a collateral but was indistinguishable from a normal hepatic artery (Figs. 2A and 2B). A retrospective evaluation of the Doppler spectra of the
difficult
biliary dilatation
arterial
with thrombosis
(4/7),
reconstruction
(3/7).
of the hepatic artery and
collateralization, one required retransplantation graft failure, four others are awaiting suitable and the remaining two are stable on antibiotic
because of donor organs, therapy.
Discussion
The liver transplantation fornia,
Los Angeles,
program
was started
Fig. 1.-Arterial collateral circulation. A, Duplex sonogram shows typical arterial tracing from right lobe of liver (see inset). B, Selective superior mesenteric arteriogram clearly shows collateral circulation from branch of superior mesenteric C, Selective celiac angiogram in same patient shows hepatic artery thrombosis with several small arterial collaterals
at the University
in 1 984. Overall
artery (arrows). (arrowheads).
of Cali-
survival
rate
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Fig. 2.-Arterial A, Color-flow
B,
collateral circulation in pediatric liver transplant recipient with thrombosis of hepatic artery. Doppler examination of ports hepatis clearly shows flow in transplanted liver. Analysis of spectral display confirms presence of arterial blood flow in ports (calculated resistive Index = 0.4).
C, Subsequent arterlogram shows thrombosis of hepatic artery and several tiny collateral vessels. Additional small collaterals were seen when injection of superior mesenteric artery was used (not shown).
in the first
40 pediatric
transplant
recipients
was
80%,
with
an actuarial survival rate of 78% [7]. Our current survival rate of 82% in pediatric transplant recipients most likely is related to increasing
experience
in managing
posttransplant
morbidity
and the use of OKT3 monoclonal antibody therapy for the management of rejection [8]. Thrombosis of the hepatic anteny, however, continues to be a major problem. Duplex sonography is the most practical and cost-effective screening
method
for the evaluation
of transplant
morphology
and vascular integrity. Its usefulness in the evaluation of the hepatic artery is based largely on the assumption that thrombosis
will eliminate
all arterial
flow
to the organ.
In three
of
Our findings
are contrary
to those recently
reported
by Flint
et al. [5]. In their series, 34 (92%) of 37 cases of thrombosis of the hepatic artery were diagnosed correctly by duplex Doppler imaging. A Doppler signal was not identified in any child in their study population who had arterial collaterals. Clearly,
however,
alization
arterial
has occurred.
studies is uncertain. tivity, wall-filter played a role.
flow
is present
The reason
Technical
settings,
in the liver
for the disparity
factors
if collater-
in the two
such as system
or transducer
frequency
sensi-
may
have
When our experience is analyzed, a number of ways of differentiating between patients with a patent hepatic artery
our 1 1 patients, collateralization was discovered when intrahepatic arterial Doppler signals reappeared after a documented thrombosis. In four others, thrombosis of the hepatic artery was not diagnosed prospectively because arterial DoppIer signals within the liver were taken to imply patency of the hepatic artery. In the native liver, occlusion of the main hepatic artery leads to rapid development of arterial collaterals. Formation of
and those with thrombosis and collateralization may exist. Thus far, the most promising possibility is the finding of
collateral
suggestive
vessels
and blood
flow
in the portal
the likelihood
of hepatic
ischemia
tients
With
transplantation,
[3, 9].
liver
vein decrease
and infarction potential
in most pa-
brings
the highly
vascular
jejunal
arterial
bed close
to the transplanted liver. With arterial occlusion, collateral vessels can be recruited from the jejunal vascular arcade. This hypothesis is supported by the fact that collaterals to the homograft originated from the superior mesentenic artery in all six patients by angiography.
whose collateral Adult transplant
circulation recipients
resistive index) in children vessels. Serial scanning
potentially can identify the first, possibly subclinical, episode of complete thrombosis before formation of collateral vessels occurs. Both hypotheses, however, require further investigation. On the basis of our experience, children with a strongly
clinical history of thrombosis
even if the duplex
Doppler
study
shows
require arteniography arterial
patency.
collateral
pathways are severed; the graft is far more vulnerable to disruption of the central arterial circulation. This pattern is seen in adult transplant recipients; however, collaterals do form in children who receive transplants. The potential to form collateral circulation may be related to the type of biliany reconstruction performed in pediatric liver transplant recipients. In our pediatric patients, particularly those with a pretransplant diagnoses of biliary atresia, a Rouxen-V choledochojejunostomy with a straight tube or internal stent is used for biliary anastomoses [7]. This type of reconstruction
increased diastolic flow (decreased who have formation of collateral
was documented undergo a differ-
ent type of biliary reconstruction (choledochocholedochostomy), which leads to more complete dearterialization and less opportunity for collateral formation.
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GM, et al. Liver transplantation
2. Shaw BW, Gordon AD, Iwatsuki 5, et al. Hepatic retransplantation.
today. Trans-
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3. Starzel TE, Groth CG, Brettschneider
L, et al. Orthotopic
homotransplan-
tation of the human liver. Ann Surg 1968:168:3:392-415 4. Tzakis AG, Gordon AD, Shaw Bw, et al. Clinical presentation artery thrombosis after liver transplantation in the cyclosporine plantation 1985:40: 667-671
of hepatic
era. Trans-
5. Flint EW, Sumkin JH, Zajko AB, et al. Duplex sonography of hepatic artery thrombosis after liver transplantation. AJR 1988:151 :481-483 6. Wozney P, zajko AB, Bron KM. et al. Vascular complications after liver transplantation:
a 5-year
experience.
AiR
1986:147
:657-663
7. Busuttil AW, Colonna JO, Hiah JR. et al. The first 100 liver transplants at UCLA. Ann Surg 1987:206:4:387-402 8. Goldstein G, Kremer AB, Bames L, Hirsch AL. OKT3 monoclonal antibody reversal of renal and hepatic rejection in pediatric patients. J Pediatr i987;1 1 1 :6(2):1046-1 050
9. Groth CG, Porter KA. Otte JB, et al. Studies of blood flow and ultrastructural changes in rejecting and non-rejecting canine orthotopic liver homografts. Surgery i968:63(4):658-668