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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.

REFERENCES 1 . Busuttil

RW, Goldstein LI, Danovitch Ann Intern Med i986;104:377-389

GM, et al. Liver transplantation

2. Shaw BW, Gordon AD, Iwatsuki 5, et al. Hepatic retransplantation.

today. Trans-

plant Proc 1985:17:264-271

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

False-negative duplex Doppler studies in children with hepatic artery thrombosis after liver transplantation.

Recent reports describe formation of collateral vessels in children who have hepatic artery thrombosis after liver transplantation. This led us to ree...
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