Doppler Ultrasound Findings in the Hepatic Artery Shortly After Liver Transplantation

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1 Gastrointestinal Imaging Pictorial Essay García-riado et al. Hepatic rtery fter Liver Transplantation Gastrointestinal Imaging Pictorial Essay FOUS ON: Ángeles García-riado 1 Rosa Gilabert nnalisa erzigotti oncepción rú García-riado Á, Gilabert R, erzigotti, rú Keywords: Doppler sonography, hepatic artery, liver transplantation, sonography, ultrasound DOI: /JR Received February 27, 2008; accepted after revision December 13, ll authors: Department of Radiology, linic Hospital of arcelona, Villarroel 170, arcelona, Spain. ddress correspondence to Á. García-riado (magarcia@clinic.ub.es). JR 2009; 193: X/09/ merican Roentgen Ray Society Doppler Ultrasound Findings in the Hepatic rtery Shortly fter Liver Transplantation OJETIVE. 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. ONLUSION. 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. H epatic 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. surveillance program based on color Doppler ultrasound (DUS) 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 rterial Findings in the Immediate Posttransplantation Period The normal hepatic artery shows a lowresistance 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). 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]. ccording to the degree of resistance, the high RI has been classified by García-riado 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 DUS, suspecting a complication when the waveform does not become normal within 4 days. In these cases, T angiography (T), MR angiography (MR), or arteriography is indicated. In patients with a type 4 waveform indicating undetectable arterial DUS flow, DUS (if possible), T, or MR is indicated to exclude hepatic artery thrombosis. If a patent artery is seen, a daily DUS examination is mandatory until the flow becomes normal. Early and transient high RI, which has been shown to be related to an older donor and a prolonged period of ischemia, lacks clinical 128 JR:193, July 2009

2 Hepatic rtery fter Liver Transplantation repercussions and long-term prognostic implications [4]. Doppler Findings in Posttransplantation Hepatic rtery omplications Hepatic rtery 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. ecause 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 DUS 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 (Fig. 5). highresistance flow at the hilus (RI = 1) may be observed if the Doppler waveform is obtained in the main hepatic artery before the thrombus. Occasionally, low arterial flow may provoke a false-positive diagnosis of hepatic artery thrombosis. ontrast-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] (Fig. 5). When contrast-enhanced ultrasound cannot be used, other noninvasive imaging techniques such as MR or T 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 rtery 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. 6 and 6). 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. 6). 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]. Pseudoaneurysm of the Hepatic rtery 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 DUS and presents an arterial Doppler waveform (Fig. 7). rterial 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. ngiography 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]. 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 DUS; in such situations, contrast-enhanced ultrasound can be used to confirm arterial permeability (Fig. 8). 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. 9), but no precise data have been reported. References 1. Jain, osta G, Marsh W, et al. Thrombotic and nonthrombotic hepatic artery complications in adults and children following primary liver transplantation with long-term follow-up in 1000 consecutive patients. Transpl Int 2006; 19: García-riado, Gilabert R, Nicolau, et al. Early detection of hepatic artery thrombosis after liver transplantation by Doppler ultrasonography. J Ultrasound Med 2001; 20: Uzochukwu LN, luth EI, Smetherman DH, et al. Early postoperative hepatic sonography as a predictor of vascular and biliary complications in adult orthotopic liver transplant patients. JR 2005; 185: García-riado, Gilabert R, Salmerón JM, et al. Significance of and contributing factors for a high resistive index of Doppler sonography of the hepatic artery immediately after surgery: prognostic implications for liver transplant recipients. JR 2003; 181: Lafortune M, Patriquin H. The hepatic artery: studies using Doppler sonography. Ultrasound Q 1999; 15: Sheiner P, Varma, Guarrera JV, et al. Selective revascularization of hepatic artery thrombosis after liver transplantation improves patient and graft survival. Transplantation 1997; 64: Sidhu PS, Shaw S, Ellis SM, Karani J, Ryan SM. Microbubble ultrasound contrast in the assessment of hepatic artery patency following liver transplantation: role in reducing frequency of hepatic artery arteriography. Eur Radiol 2004; 14: Hom K, Shrestha R, Palmer SL, et al. Prospective evaluation of vascular complications after liver transplantation: comparison of conventional and microbubble contrast-enhanced US. Radiolo- JR:193, July

3 García-riado et al. gy 2006; 241: Dodd GD 3rd, Memel DS, Zajko, aron RL, Santaguida L. Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 1994; 192: bbasoglu O, Levy M, Vodapally M, et al. Hepatic artery stenosis after liver transplantation: incidence, presentation, treatment, and long-term outcome. Transplantation 1997; 63: Fig. 1 olor 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 Sidhu PS, Ellis SM, Karani J, Ryan SM. Hepatic artery stenosis following liver transplantation: significance of the tardus parvus waveform and the role of microbubble contrast media in the detection of a focal stenosis. lin Radiol 2002; 57: Nüssler N, Settmacher U, Haase R, Stange, Heise M, Neuhaus P. Diagnosis and treatment of arterial steal syndromes in liver transplant recipients. Liver Transpl 2003; 9: Uflacker R, Selby, havin K, Rogers J, aliga P. Transcatheter splenic artery occlusion for treatment of splenic artery steal syndrome after orthotopic liver transplantation. ardiovasc Intervent Radiol 2002; 25: Nishida S, Kadono J, De Faria W, Levi D, Moon J, Tzakis. Gastroduodenal artery steal syndrome during liver transplantation: intraoperative diagnosis with Doppler ultrasound and management. Transpl Int 2005; 18: 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-riado classification [4]. Fig. 3 bsence 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. 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. 130 JR:193, July 2009

4 Hepatic rtery fter Liver Transplantation E Fig. 5 Ultrasound of liver graft in 56-year-old man with hepatic artery thrombosis., olor Doppler ultrasound shows absence of flow in hepatic artery at hilus (arrow)., No arterial flow is detected on pulsed Doppler ultrasound., ontrast-enhanced ultrasound reveals no arterial perfusion in early phase at hilus level (arrow) nor at intrahepatic level. D, Later phase after contrast injection shows normal portal perfusion but no flow in hepatic artery. E, Thrombosis of hepatic artery is confirmed at angiography. D JR:193, July

5 García-riado et al. Fig. 6 Hepatic artery stenosis in 39-year-old man., Doppler ultrasound of hepatic artery at intrahepatic level shows prolonged acceleration time of second., Flow of intrahepatic artery shows diminished pulsatility and small difference between systolic and diastolic velocities that result in low resistive index of 0.40., Pulsed Doppler ultrasound shows elevation of blood flow velocity (2.99 m/s) at stenotic level. D, rteriography confirmed hepatic artery stenosis. D 132 JR:193, July 2009

6 Hepatic rtery fter Liver Transplantation Fig. 7 Pseudoaneurysm of hepatic artery in 60-year-old woman after liver transplantation., -mode ultrasound reveals small fluid liquid collection of cm (arrow) at hilus., olor 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., rteriography confirms diagnosis of pseudoaneurysm. Fig. 8 Splenic artery steal syndrome in 53-year-old man 4 days after liver transplantation., olor Doppler ultrasound does not detect hepatic artery., No arterial flow is identified on pulsed Doppler ultrasound in usual location of hepatic artery. (Fig. 8 continues on next page) JR:193, July

7 García-riado et al. Fig. 8 (continued) Splenic artery steal syndrome in 53-year-old man 4 days after liver transplantation., ontrast-enhanced ultrasound (SonoVue) shows patent hepatic artery (arrow). Note that filling of hepatic artery is delayed; also note simultaneous filling of portal vein. D, fter contrast administration, hepatic artery flow is detected on pulsed Doppler ultrasound. E, rteriography reveals sluggish flow at hepatic artery (arrow) associated with early and intense filling of splenic artery (arrowhead), which is enlarged. F, Selective angiography of hepatic artery shows normal vessel (arrow). G, fter surgical occlusion of splenic artery, hepatic arterial flow is normalized. E D F G 134 JR:193, July 2009

8 Hepatic rtery fter Liver Transplantation Fig. 9 Spleen ultrasound findings in 55-year-old woman with splenic arterial steal syndrome., -mode ultrasound shows splenomegaly., Enlarged splenic artery in its entire course is seen on -mode ultrasound (arrow). Figure shows splenic artery near its origin. Note location of aorta (arrowhead) and mesenteric artery (double arrowhead). and D, Pulsed Doppler ultrasound shows high blood flow velocity in splenic artery at its origin () and at splenic hilus (D), with maximum velocities of 2 m/s for entire course. D JR:193, July