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Collateral Transformation of the Hepatic Artery After Liver Transplantation

¹ All authors: Department of Radiology, Ochsner Medical Center, 1514 Jefferson Hwy., New Orleans, LA 70121.

Received January 5, 2008; accepted after revision February 23, 2008.

 
Address correspondence to P. B. Dydynski (pdydynski{at}ochsner.org).

Abstract

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OBJECTIVE. A high rate of false-negative sonographic examinations for evaluation for hepatic artery thrombosis in the setting of collateral artery vessel formation has been documented. Subacute hepatic artery compromise with collateral vessel formation can be subclinical, and we believe that this phenomenon may occur more commonly than currently appreciated.

CONCLUSION. We discuss two cases of subacute hepatic artery compromise with collateral artery vessel formation that were prospectively diagnosed in July 2007 by sonography and confirmed by angiography. We refer to this phenomenon as "collateral transformation of the hepatic artery."

Keywords: collateral transformation of hepatic artery • hepatic artery stenosis • hepatic artery thrombosis • liver transplantation

Introduction

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Hepatic artery thrombosis in patients after liver transplantation is a significant cause of morbidity and mortality. Sonography is very sensitive for the diagnosis of hepatic artery thrombosis in the acute setting [1]. Detection of compromise to the vascular supply of the allograft in the subacute setting (> 10 days) represents a challenge to radiologists and the transplant surgeon. Clinical symptoms (if any) are often nonspecific and vary from elevated liver enzymes to eventual hepatic necrosis and sepsis. In the past, suboptimal sensitivity with sonography and CT frequently required angiography for a definitive diagnosis.

A high rate of false-negative sonographic examinations for evaluation for hepatic artery thrombosis in the setting of collateral artery vessel formation (especially in the pediatric population) has been well documented [2]. Horrow et al. [1] recently reported that sonography becomes less sensitive as the interval between transplantation and diagnosis of hepatic artery thrombosis increases because of collateral arterial flow. Because subacute hepatic artery compromise with subsequent collateral vessel formation can be subclinical, we believe that this phenomenon may occur more commonly than currently appreciated in the adult liver transplantation population. Increased awareness of this entity, as well as improved understanding of some of the secondary signs that can be seen on sonographic examination, can result in improved sensitivity in prospectively making this diagnosis and thereby improve patient management.

We discuss two cases of subacute hepatic artery compromise with collateral arterial vessel formation that were prospectively diagnosed in July 2007 by sonography and subsequently confirmed by angiography. We describe this phenomenon as "collateral transformation of the hepatic artery." Collateral transformation of the hepatic artery conceptually parallels the cavernous transformation of the portal vein secondary to portal vein thrombosis. Both processes involve occlusion of a main vascular channel in the porta hepatis with subsequent collateral formation. This similarity is purely anatomic, with the two processes possessing separate underlying causes.

Materials and Methods

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Patient 1
The first patient was a 44-year-old woman who underwent liver transplantation in March 2007 for a history of liver cirrhosis secondary to primary sclerosing cholangitis. An orthotopic liver transplantation was performed as well as a Roux-en-Y hepaticojejunostomy. Postoperative sonography showed normal resistive indices in the main, right, and left hepatic arteries. A tardus parvus waveform in the right hepatic artery was noted on sonography on the first postoperative day, and this persisted on the repeat sonographic study on the second postoperative day. The postoperative sonographic examinations were otherwise within nor mal limits. The patient did well clinically and was discharged on the seventh postoperative day on standard immunosuppressive therapy.

View larger version (72K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —44-year-old woman who underwent orthotopic liver transplantation as well as Roux-en-Y hepaticojejunostomy. Sonogram acquired at 1-month follow-up shows hepatofugal flow in posterior branch of right hepatic artery (RHA). RPV = right portal vein, REV = reverse, POS = posterior.

View larger version (70K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —44-year-old woman who underwent orthotopic liver transplantation as well as Roux-en-Y hepaticojejunostomy. Sonogram acquired at 3-month follow-up shows collateral arteries (arrows) in porta hepatis region.

View larger version (146K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —44-year-old woman who underwent orthotopic liver transplantation as well as Roux-en-Y hepaticojejunostomy. Angiogram acquired 1 day after sonogram in B shows collateral transformation of hepatic artery, confirming occlusion of main hepatic artery.

Results

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Patient 1
One-month follow-up sonographic examination showed decreased resistive indices of 0.4, 0.44, and 0.38 in the main, left, and right hepatic arteries, respectively. The main hepatic artery velocity was elevated, measuring 375 cm/s. Although suggestive for significant stenosis of the main hepatic artery, angiography was not performed because the patient was asymptomatic. Reversal of flow in the posterior branch of the right hepatic artery was also identified, which was a new finding of undetermined clinical significance (Fig. 1A).

Three-month postoperative sonography again showed decreased resistive indices not significantly changed from the prior examination. Reversal of flow (hepatofugal) in the right hepatic artery was still present and was again of undetermined significance at the time. Numerous small, tortuous arterial vessels in the region of the main hepatic artery were newly identified and suggestive for collateral vessel formation (Fig. 1B). No flow was identified in the main hepatic artery, suggestive of complete occlusion or severe stenosis. Angiography was performed the next day, confirming occlusion of the main hepatic artery.

Numerous collateral arterial vessels reconstituted arterial flow to the left and right hepatic arteries (Fig. 1C). We refer to this phenomenon as "collateral transformation of the hepatic artery," an entity that conceptually parallels the cavernous transformation of the portal vein. The patient was subsequently started on low-dose aspirin to prevent thrombosis of the small collateral arterial vessels. The patient has been doing well clinically for 9 months since transplantation, with liver function tests slightly above normal limits.

Patient 2
Three-week postoperative sonography showed a detrimental change in the resistive indices measuring 0.4 in the main hepatic artery, 0.45 in the left hepatic artery, and 0.24 in the right hepatic artery. This patient had also been doing well clinically, with liver function tests within normal limits. For this reason, the patient did not undergo angiography. Two-month postoperative sonography again showed decreased resistive indices measuring 0.36, 0.34, and 0.32 in the main, right, and left hepatic arteries, respectively. Significantly elevated velocity in the main hepatic artery was identified, suggestive for significant stenosis or thrombosis. Small, tortuous arterial vessels were now visualized in the porta hepatis region, consistent with collateral vessel formation (Fig. 2A).

View larger version (85K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —55-year-old man who underwent orthotopic liver transplantation for cirrhosis secondary to chronic hepatitis C. Sonogram acquired 2 months after transplantation shows small collateral vessels in porta hepatis region. No Doppler flow of extrahepatic main hepatic artery was identified, suggestive for hepatic artery thrombosis.

View larger version (171K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —55-year-old man who underwent orthotopic liver transplantation for cirrhosis secondary to chronic hepatitis C. Angiogram acquired after sonogram in A shows multiple collateral vessels reconstituting right hepatic artery branches.

View larger version (75K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C —55-year-old man who underwent orthotopic liver transplantation for cirrhosis secondary to chronic hepatitis C. Sonogram acquired 1 month after angiogram in B shows similar findings. Reversal of flow (hepatofugal) in right hepatic artery (RHA) was identified (arrow) and showed triphasic arterial waveform thought to be secondary to retrograde flow from supplying collateral arteries—similar to patient 1. RPV = right portal vein, REV = reverse, POS = posterior.

The patient was started on low-dose aspirin and, aside from a transient elevation in his liver function tests, has been doing well clinically. One month after angiography, sonography showed similar findings. Reversal of flow (hepatofugal) in the right hepatic artery was identified and showed a triphasic arterial waveform. We believe that this was secondary to retrograde flow from supplying collateral arteries (Fig. 2C)—a similar finding to that in patient 1.

Discussion

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A diagnosis of hepatic artery thrombosis with collateral vessel formation has important implications. These patients are at high risk for developing biliary strictures and other complications secondary to chronic ischemia of the biliary epithelium. Leonardi et al. [3] have shown a high mortality rate in these patients in the chronic setting, with a mean survival of 40 months. For these reasons, such patients merit close clinical follow-up and routine sonographic examination.

In the setting of chronic hepatic artery thrombosis, the survival of the allograft depends on the patency of the collateral arteries. These likely represent tiny vessels transplanted with the donor hepatic artery that have hypertrophied. The small lumen of these arteries makes them prone to occlusion. The use of antiplatelet therapy (such as low-dose aspirin) is therefore considered in these patients to help prevent thrombosis. Both of the patients discussed were started on low-dose aspirin and have since been doing well clinically.

Collateral transformation of the hepatic artery has been a source of false-negative examinations in the past [4–6]. Poor resolution with older generation ultrasound machines could make it difficult to distinguish the normal hepatic artery from a collateral vessel in the porta hepatis region. Detection of a normal intrahepatic Doppler arterial waveform (secondary to collateral vessels reconstituting flow to the intrahepatic arteries) can still be a cause for false-negative sonographic examinations. It is therefore important to look for secondary signs of collateral vessel formation on sonography. Careful interrogation of the porta hepatis region for the presence of small tortuous arteries should be routinely performed in the subacute and chronic setting. Their presence is strongly suggestive for hepatic artery compromise. Horrow et al. [1] reported that sonography was able to show collateral vessel formation in 10 of 11 patients who had irreversible hepatic artery thrombosis in the chronic setting.

Both of our patients also showed an interesting finding that was suggestive of collateral vessel formation: hepatofugal flow in the right hepatic artery. In this setting, it is believed that the right hepatic artery is being supplied distally from collateral vessels with resultant hepatofugal flow. We believe that this finding represents an additional secondary sign of hepatic artery thrombosis with collateral vessel formation and should be evaluated for on follow-up sonography. To our knowledge, this is a finding that has not been reported previously.

Retrospective review of these cases raises an important question: What is the appropriate time for angiographic intervention? When findings suggestive for complete hepatic artery thrombosis are discovered by sonography, it is often too late for intervention. The patient then most likely requires surgical revascularization—which carries a high morbidity—or a second transplant. Significant changes in laboratory values may also occur only after complete occlusion—in which case it is again too late for angiographic intervention. Both of our patients showed a drop in resistive indices approximately 3–4 weeks after transplantation. Angiography was not performed because there was still flow in the extra- and intrahepatic arteries, and both patients were doing well clinically, with no significant abnormalities in laboratory values. Angiography was only performed when follow-up sonography suggested complete hepatic artery thrombosis (with collateral vessel formation).

A significant drop in the resistive index of an intrahepatic artery suggests vascular compromise to the allograft [7, 8]. Formation of collateral vessels in the chronic setting is likely secondary to progressing stenosis from intimal hyperplasia. These cases may be amenable to angioplasty if diagnosed early. A significant drop in the resistive index of the hepatic artery or its main branches should therefore be considered a valid indication for angiography. Continued monitoring of the patient clinically or continued sonographic follow-up may only serve to delay possible therapeutic angioplasty—or surgical revascularization if the hepatic artery is already completely occluded.

In conclusion, sonography is still the safest and most cost-effective screening examination to monitor the patient after liver transplantation. Improved resolution and contrast with today's ultrasound machines enables radiologists to diagnose hepatic artery thrombosis with improved sensitivity even in the setting of collateral vessel formation. Increased awareness of this entity and understanding of the secondary signs of collateral vessel formation can be helpful in making this diagnosis. A significant drop in the resistive indices in the chronic setting should be a consideration for angiography irrespective of laboratory values or patient symptomatology. Collateral transformation of the hepatic artery carries important patient management implications and therefore should be evaluated for on all follow-up sonographic examinations.

References

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1. Horrow MM, Blumenthal BM, Reich DJ, Manzarbeitia C. Sonographic diagnosis and outcome of hepatic artery thrombosis after orthotopic liver transplantation in adults. AJR 2007;189 : 346-351[Abstract/Free Full Text]
2. McDiarmid SV, Hall TR, Grant EG, et al. Failure of duplex sonography to diagnose hepatic artery thrombosis in a high-risk group of pediatric liver transplant recipients. J Pediatr Surg1991; 26:710 -713[CrossRef][Medline]
3. Leonardi MI, Boin I, Leonardi LS. Late hepatic artery thrombosis after liver transplantation: clinical setting and risk factors. Transplant Proc 2004;36 : 967-969[CrossRef][Medline]
4. Hall TR, McDiarmid SV, Grant EG, Boechat MI, Busuttil RW. False-negative duplex Doppler studies in children with hepatic artery thrombosis after liver transplantation. AJR1990; 154:573 -575[Abstract/Free Full Text]
5. Flint EW, Sumkin JH, Zajko AB, Bowen A. Duplex sonography of hepatic artery thrombosis after liver transplantation. AJR 1988; 151:481 -483[Abstract/Free Full Text]
6. Crossin JD, Muradali D, Wilson SR. US of liver transplants: normal and abnormal. RadioGraphics 2003;23 : 1093-1114[Abstract/Free Full Text]
7. Dodd GD 3rd, Memel DS, Zajko AB, Baron RL, Santaguida LA. Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 1994;192 : 657-661[Abstract/Free Full Text]
8. Nghiem HV, Tran K, Winter TC 3rd, et al. Imaging of complications in liver transplantation. RadioGraphics1996; 16:825 -840[Abstract]

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				P. S. Sidhu, S. M. Ryan, and J. B. Karani Collateral Transformation of the Hepatic Artery After Liver Transplantation: Significance of the Tardus-Parvus Waveform Am. J. Roentgenol., May 1, 2009; 192(5): W264 - W264. [Full Text] [PDF]

				P. B. Dydynski, E. I. Bluth, and J. M. Milburn Reply Am. J. Roentgenol., May 1, 2009; 192(5): W265 - W265. [Full Text] [PDF]

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