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Original Research |
1 Department of Radiology, Albert Einstein Medical Center, 5501 Old York Rd.,
Philadelphia, PA 19141-3098.
2 Present address: Department of Radiology, Hospital of the University of
Pennsylvania, Philadelphia, PA 19104.
3 Department of Surgery, Division of Transplant Surgery, Albert Einstein Medical
Center, Philadelphia, PA.
Received November 28, 2006;
accepted after revision March 28, 2007.
Address correspondence to M. M. Horrow
(horrowm{at}einstein.edu).
Abstract
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MATERIALS AND METHODS. The subjects included all adult recipients with orthotopic liver transplants during a 10.5-year period. A retrospective review of all cases of hepatic artery thrombosis detected on angiography or at surgery was correlated with sonography findings at diagnosis. Clinical and sonography outcomes were recorded. Patients were divided into early (< 1 week) and late hepatic artery thrombosis groups. Hepatic artery thrombosis was considered primary or secondary due to treatment of other hepatic artery complications.
RESULTS. Of 522 transplants, 25 (4.8%) developed hepatic artery thrombosis that was primary in 18 (3.5%), with five early (1.0%) and 13 late (2.5%), and secondary in seven (1.3%). Sensitivities of sonography compared with angiography were 100% for detection of early hepatic artery thrombosis and 72.7% for late hepatic artery thrombosis. Seventeen patients (68%) with an episode of hepatic artery thrombosis are currently alive, 11 of whom have irreversible hepatic artery thrombosis; in 10 of the 11 cases, sonography showed that collateral arterial flow had developed. The mean survival was 51.4 months in the patients with irreversible hepatic artery thrombosis, eight of whom had documented biliary or septic complications (or both).
CONCLUSION. Hepatic artery thrombosis is uncommon after liver transplantation in adults. Sonography is extremely sensitive for the detection of hepatic artery thrombosis in symptomatic patients during the immediate postoperative period. Sonography becomes less sensitive as the interval between transplantation and diagnosis of hepatic artery thrombosis increases due to collateral arterial flow. Patients with irreversible hepatic artery thrombosis typically develop interval arterial collaterals that can be seen on sonography. Biliary and septic complications are common but usually are self-limited.
Keywords: hemodynamics • hepatic artery thrombosis • liver transplantation • sonography • surgical complications • thrombosis • transplantation
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Doppler sonography is the established technique for the initial surveillance of vascular integrity after liver transplantation, and angiography—CT angiography (CTA), MR angiography (MRA), or catheter angiography—is used for confirmation. The reported sensitivity and specificity of Doppler sonography for hepatic artery thrombosis range from 54% to 92% and from 64% to 88%, respectively [10-12]. False-negative reports (presence of hepatic arterial flow with angiographically proven hepatic artery thrombosis) are well known in children [13, 14] with only some false-negative reports documented in adults [7, 15, 16].
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In this study, we review our experience with hepatic artery thrombosis after liver transplantation in adults over a 10.5-year period to determine, first, the frequency and timing of hepatic artery thrombosis in an adult liver transplant population; second, the ability to make this diagnosis in symptomatic patients using sonography; and, third, the clinical and sonographic outcomes of these patients with particular attention to the Doppler sonography findings in the subgroup of long-term survivors with hepatic artery thrombosis.
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A search of the liver transplant database found all recipients with documented hepatic artery thrombosis. For purposes of evaluating outcomes, we included not only patients with primary hepatic artery thrombosis, but also those with secondary hepatic artery thrombosis due to treatment of other hepatic artery complications.
Recorded data included the time between transplantation and the development
of hepatic artery thrombosis, method of diagnosis (imaging or surgical), any
treatment undertaken (thrombectomy or retransplantation), and any
complications after hepatic artery thrombosis and follow-up sonography. All
hepatic artery thrombosis cases were characterized as either early (< 1
week of transplantation) or late (
1 week after transplantation). This
designation was based on our surgeons preferred method of treatment: Surgical
revascularization, as opposed to percutaneous interventional techniques, was
performed for cases occurring within 1 week of the original surgery. The
sonography equipment used to examine most patients was an ATL 5000 scanner
(Philips Medical Systems). Some earlier cases were studied using ATL 3000
equipment (Philips) and a few later cases with IU22 equipment (Philips).
Routine gray-scale imaging was followed by color and pulsed Doppler imaging using moderate settings, but these settings were adjusted to greater sensitivity if the hepatic artery was difficult to locate. The hepatic artery was imaged at the porta hepatis, just anterior to the portal vein, and then within the liver if possible. Measurements included the angle-corrected peak systolic and end-diastolic velocities and the resistive index (RI). A qualitative assessment of the hepatic arterial upstroke was made. Parvus-tardus flow consisted of a low RI (< 0.55) and a delay in systolic upstroke [17]. Our routine required a sonography examination with color and pulsed Doppler imaging of the liver within 24 hours after transplantation. Whether any further imaging examinations were performed depended on the initial imaging findings or clinical signs and symptoms. All studies were performed initially by certified technologists, and any patient with abnormal or absent arterial flow was rescanned by the radiologist. Sensitivities for hepatic artery thrombosis were calculated. Because this study was based on a retrospective review of a clinical database, specificities could not be calculated.
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Early Hepatic Artery Thrombosis
All five patients in this group were initially diagnosed by a lack of
hepatic arterial flow on sonography. The sonography findings were confirmed
with angiography, yielding a sensitivity of 100% (Figs.
1 and
2A,
2B,
2C,
2D).
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Figure 5 describes the outcomes of the 18 patients with irreversible hepatic artery thrombosis. One of the patients who died after a second transplantation had proven collateral flow on sonography and angiography and developed an infected biloma before undergoing the second transplantation 27 months after diagnosis of hepatic artery thrombosis. Of the 11 patients currently alive with hepatic artery thrombosis, 10 had documented collateral arterial flow on sonography, three at the time of the hepatic artery thrombosis diagnosis and seven with interval development (Fig. 6A, 6B, 6C, 6D). One patient did not undergo imaging follow-up at our institution. Five of these patients had a confirmatory study for the presence of arterial collaterals, two by angiography only, two by angiography and CTA, and one by MRA only.
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Of the 25 patients who developed hepatic artery thrombosis, 17 (68%) are currently alive, 11 with hepatic artery thrombosis. Of the 11 patients with irreversible hepatic artery thrombosis, 10 had collateral flow detected on sonography and confirmed on angiography in four patients and on MRA in one patient. The mean survival of patients with irreversible hepatic artery thrombosis was 51.4 months (range, 9-98 months). One patient had hepatic artery thrombosis documented on sonography and angiography before undergoing a second transplantation.
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Regarding outcomes, 68% of the hepatic artery thrombosis population is currently alive, and most did not require a second liver transplant. For the treatment of early postoperative hepatic artery thrombosis, urgent surgical revascularization was the procedure of choice. Nonetheless, these patients still had a high mortality. During the late period, nonurgent retransplantation was an option in a minority of patients. From our review, we found a substantial cohort of patients with long-term survival after the diagnosis of irreversible hepatic artery thrombosis. Although this group was at great risk for sepsis and biliary complications, these complications usually were self-limiting. Most of these patients developed collateral arterial flow based on sonographic detection of arterial flow at the porta hepatis and within the liver.
Our finding that Doppler sonography had a sensitivity of 72.7% for the diagnosis of hepatic artery thrombosis based on a lack of arterial flow is consistent with the literature. Dodd et al. [12] reported a sensitivity of 50%, and Nolten and Sproat [11] reported 82%. Our finding of a population of adult patients living with hepatic artery thrombosis, with a mean survival of more than 4 years, is unusual. There are only a few reports of adult transplant recipients with long-term survival after hepatic artery thrombosis. Leonardi et al. [7] reported nine cases of late hepatic artery thrombosis in patients with a mean survival of 40 months, six of whom did not undergo a revascularization procedure. Gunsar et al. [8] reported one long-term survivor with hepatic artery thrombosis at 53 months, and De Gaetano et al. [9] found long-term survival in two of 12 patients with delayed hepatic artery thrombosis. In contrast, long-term survival after hepatic artery thrombosis is well established in children. Stringer et al. [13] reported a series of 31 pediatric patients with hepatic artery thrombosis. Using a combined approach of retransplantation, revascularization, and conservative management, they achieved 83% survival. In our study, 13 of the patients with irreversible hepatic artery thrombosis survived with a mean follow-up of 4.1 years.
We can only speculate about the reasons for long-term survival of adult liver recipients with hepatic artery thrombosis. Improved treatment of biliary and septic complications may be a factor. The interval development of collateral arterial flow may be beneficial. The phenomenon of collateral flow resulting in false-negative sonography findings has been well established in the pediatric population [10-13, 18, 19] but has been reported less frequently in adults [7, 15, 16]. Stringer et al. [13] reported that eight of 13 pediatric patients with long-term survival after irreversible hepatic artery thrombosis showed hepatic arterial collateral flow on angiography [13]. Collaterals were first detected 3 weeks after transplantation and were well developed by 3 months after transplantation. In their study of adults, Leonardi et al. [7] found that five of nine long-term hepatic artery thrombosis survivors showed collateral flow at angiography. McDiarmid et al. [14] advised caution when interpreting a sonogram obtained 2 weeks or more after transplantation in a pediatric population. If patients had arterial flow on sonography but developed infarcts, bacteremia, or sepsis, angiography was recommended.
Our findings have several important clinical implications. During the early postoperative period, liver transplant recipients should receive priority sonography because surgical revascularization can be effective at that time. As the interval between transplantation and sonography increases, sonograms must be interpreted with caution because collateral flow has had time to develop. Comparison with prior studies for subtle changes in the RI and in the shape of the waveform is crucial. As has been suggested in the pediatric population, biliary complications or unexplained sepsis in adult transplant patients should prompt a further evaluation for hepatic artery thrombosis despite hepatic arterial flow on sonography. CTA and MRA now provide noninvasive imaging alternatives to catheter angiography.
Several criticisms can be made of our study. Because this study is retrospective, patients did not undergo screening or follow-up sonography at specific intervals. As a result, we do not know exactly when acute thrombosis occurred, particularly in the delayed cases. We know only when the patients became symptomatic and underwent imaging. We suspect that the cases of hepatic artery thrombosis without flow on sonography occurred close to the time of diagnosis. The cases discovered at 10, 44, and 48 months after transplantation all had collateral flow, so the interval between thrombosis and imaging diagnosis was likely longer. Thus, many of these patients may have been living with hepatic artery thrombosis for longer than we can document.
In addition, there may have been more patients with hepatic artery thrombosis than we have documented. Some patients may have died with undiagnosed hepatic artery thrombosis, whereas others may be alive with undiagnosed hepatic artery thrombosis because they have no clinical complications. Furthermore, we cannot determine how long it takes for collateral flow to develop after hepatic artery thrombosis occurs. The shortest interval we know of is 2 months in a patient who developed hepatic artery thrombosis 2 weeks after transplantation.
A major assumption in our study is that the interval development of hepatic arterial flow on sonography after an established angiographic diagnosis of hepatic artery thrombosis is a reflection of collaterals. We only have angiographic (catheter angiography, CTA, or MRA) confirmation of collateral flow in six patients. Nonetheless, we believe this assumption is reasonable. Arterial flow did not reappear immediately; instead, it was noted only on follow-up studies months or even years after the original thrombosis. Collateral flow also accounted for all three of the false-negative cases of hepatic artery thrombosis.
In summary, our study results show that hepatic artery thrombosis is an uncommon complication of adult liver transplantation that occurs rarely in the early postoperative period and occasionally thereafter, with most cases occurring during the first postoperative year. In symptomatic patients, based on a lack of hepatic arterial flow, Doppler sonography is 100% sensitive for hepatic artery thrombosis during the early postoperative period. The sensitivity remains high several months after transplantation, but subsequently decreases due to the development of collateral flow. Furthermore, patients with irreversible hepatic artery thrombosis will frequently develop sonographically detectable collateral arterial flow to the liver.
Outcomes and treatment vary depending on when the hepatic artery thrombosis occurred. During the immediate postoperative period, surgical revascularization is the treatment of choice. During the late period, a minority of patients will require a second liver transplant. Most patients can live with hepatic artery thrombosis, but they often develop sepsis and biliary complications. Thus, these complications should prompt further evaluation for hepatic artery thrombosis despite arterial flow at sonography.
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  P. B. Dydynski, E. I. Bluth, W. Altmeyer, D. A. Devun, and J. M. Milburn Collateral Transformation of the Hepatic Artery After Liver Transplantation Am. J. Roentgenol., August 1, 2008; 191(2): 546 - 549. [Abstract] [Full Text] [PDF]
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