Imaging of Liver Transplant Recipients

The radiologic evaluation of a potential candidate for orthotopic liver transplantation primarily focuses on an assessment of the degree of cirrhosis (liver size and morphology, presence of ascites) and patency and caliber of the portal vein and associated feeding veins (splenic vein and superior mesenteric vein) to determine whether a suitable site for venovenous anastomosis between the donor liver and recipient portal vein or feeding branches exists. Because of the greatly increased risk for development of hepatocellular carcinoma in cirrhotic livers, most centers perform routine sonographic surveillance for early detection of hepatocellular carcinoma. Whereas ultrasonography is sensitive in the evaluation of portal vein caliber, patency, and direction of flow, its operator-dependent nature limits its sensitivity for detection of hepatocellular carcinoma (20% to 40% for lesions smaller than 3 cm).³

Dynamic contrast-enhanced (multiphase) multidetector computed tomography (CT) and magnetic resonance imaging (MRI) enable rapid, whole-liver evaluation during arterial and portal venous phases of intravenous contrast enhancement, allowing a comprehensive assessment of the hepatic artery and the portal, splenic, and superior mesenteric veins as well as major collateral veins. In general, both contrast-enhanced CT and MRI are more sensitive than sonography for detection of hepatocellular carcinoma lesions larger than 2 cm (sensitivity, 74% to 96%). The 2-cm size is important because by the Model for End-Stage Liver Disease scoring system, cirrhotic patients with 2-cm or larger lesions are assigned priority for liver transplantation. Although both multiphase CT and MRI are less sensitive for detection of hepatocellular carcinoma lesions smaller than 2 cm, they are better than ultrasonography, which has sensitivities as low as 20% for these lesions.^4–9 MRI benefits from its ability to provide additional lesion characterization for further differentiation of the myriad types of liver nodules in cirrhotic livers based on signal intensity (e.g., T1 and T2) and contrast enhancement characteristics. Multiphase CT and MR examinations can determine vascular patency and are superior to ultrasound examination in the characterization of the recipient vascular anatomy.

Imaging of Potential Living Donors for Hepatic Transplantation

As an alternative to cadaveric liver transplantation, which is not an option in many European and Asian countries and usually entails a long wait time in many regions of the United States, living related and living donor hepatic transplantations have been advocated to expand the pool of available hepatic allografts. In adult-to-adult living donor transplantation, the right lobe (segments V, VI, VII, and VIII) is resected and transplanted. In adult-to-pediatric liver donation, the left lateral segment (segments II and III) is transplanted into the pediatric recipient. However, because of concerns of donor safety in the United States, fewer than 250 adult living donor hepatic transplantations were performed in 2007.¹⁰

At most centers performing this procedure, a thorough imaging evaluation of the donor liver is performed before surgery. This includes evaluation of the hepatic vasculature, bile ducts, hepatic lobar volume, and any possible diffuse (typically fat or iron deposition) or focal liver disease. A description of the size and branching pattern of these donor vessels is necessary in evaluation of the donor vasculature (hepatic arteries, hepatic veins, and portal veins) and bile ducts. Assessment of donor liver itself includes quantitative measurement of hepatic lobar volume and of some diffuse liver diseases, such as hepatic steatosis or siderosis. Detection and characterization of incidental liver lesions (typically cysts or hemangiomas) are necessary. Each component of this evaluation can be performed with either CT or MR by angiographic, parenchymal, and bile duct–specific imaging.

At a minimum, acceptable adult-to-adult donor liver volume criteria include a ratio between right lobe graft weight and recipient body weight of 0.8% or an estimated liver volume of 40% in an idealized whole liver. The healthy donor adult can function on a minimum of at least 30% residual liver volume without risking donor hepatic decompensation. These percentages are for a presumed normal liver free of diffuse liver disease. The most common unrecognized diffuse liver disease identifiable in the general population is macrovesicular hepatic steatosis, which may affect the liver diffusely or in a patchy, localized, and nodular fashion. Causes include obesity, steroid use, diabetes mellitus, and metabolic syndrome. With either CT or MR, steatosis may be detected and graded accurately in the absence of coexistent siderosis. In general, livers with less than 5% to 10% of macrovesicular steatosis are considered acceptable. Another form of common and unrecognized diffuse liver disease is diffuse siderosis. When both steatosis and siderosis are present, both CT and MR become unreliable for quantification, and a liver biopsy may be required.

In an adult-to-adult living donor transplantation, the entire donor right lobe is resected along a surgical plane surrounding the middle hepatic vein. In the United States, the middle hepatic vein is typically preserved in the donor, and the resection is usually 1 cm to the right of the middle hepatic vein from the dome of the liver to the portal bifurcation and gallbladder fossa. In the recipient, the right hepatic vein, right portal vein, and right hepatic artery will provide the vascular anastomoses in the graft. However, in some centers, especially outside the United States, the middle hepatic vein is resected along with the right lobe, and thus the resection plane is to the left of the middle hepatic vein.

Approximately 55% of patients have a conventional right and left hepatic artery arising from a common hepatic artery (Michel type I, Fig. 111-1).^11,12 However, in the remaining 45% of patients, there can be a wide range of hepatic artery variations (Fig. 111-2) that can be described by the Michel classification (Table 111-1). Proper identification of hepatic artery anatomy in the donor is critical for surgical planning and minimization of postoperative complications in both the donor and recipient. A donor may be rejected when aberrant arterial anatomy is also associated with other biliary and venous variants, which in combination result in an increased complexity of the operation.

FIGURE 111-1 Hepatic artery anatomy. Volume rendered three-dimensional image from CTA of typical normal hepatic anatomy in which the right hepatic artery (RHA) and left hepatic artery (LHA) arise from the hepatic artery (HA). CHA, common hepatic artery; GDA, gastroduodenal artery; Celiac, celiac artery; Spl A, splenic artery.

FIGURE 111-2 Replaced right hepatic artery. Volume rendered three-dimensional image from CTA in a patient with a replaced right hepatic artery (RHA) arising from the superior mesenteric artery (asterisk).

Table 111-1 Michel Classification of Arterial Variants

From Artioli D, Tagliabue M, Aseni P, et al: Detection of biliary and vascular anatomy in living liver doners: value of gadobenate dimeglumine enhanced MR and MDCT angiography. Eur J Radiol. In press.

Ideal portal venous anatomy has the right portal vein branching from the main portal vein (Fig. 111-3) and not from the left portal vein. Cases in which portal venous branches to segment IV arise from the right anterior portal vein may be a contraindication to transplantation.

FIGURE 111-3 Normal portal venous anatomy. Oblique maximum intensity projection image from portal CTA demonstrates normal portal vein (PV) bifurcation into left portal vein (LPV) and right portal vein (asterisk). RAPV, right anterior portal vein; RPPV, right posterior portal vein.

Ideal hepatic venous anatomy has the single dominant right hepatic vein available for anastomosis without significant (>5 mm diameter branch veins) hepatic venous branches draining into the now-missing middle hepatic vein. However, many variants in hepatic venous drainage exist. Hepatic venous branches larger than 5 mm that drain the right posterior lobe (VII and VI) and insert into the inferior vena cava (IVC) may require separate venous anastomoses in the recipient to prevent hepatic segmental congestion or bleeding and subsequent liver dysfunction. Hepatic venous branches larger than 5 mm that drain the right anterior lobe branches (VIII and V) into the middle hepatic vein will invariably transect the surgical resection plane and probably require separate venous anastomoses to also prevent complications such as hepatic venous congestion in the recipient.^13,14

Hepatic Artery

With an occurrence between 5% and 12% of adult patients and up to 42% of pediatric patients, presumably owing to small size of the transplant vessel, hepatic artery thrombosis is the most frequent and most serious vascular complication after liver transplantation.^21,27,30 Although the liver parenchyma has dual arterial and portal venous blood supply, the hepatic artery alone perfuses the biliary tree of the transplanted liver.

Hepatic artery thrombosis generally develops within the first 3 months after transplantation.³⁰ Risk factors for development of hepatic artery thrombosis include small native hepatic arteries, use of a Roux-en-Y biliary reconstruction, length of cold ischemia and operative times, volume of blood and plasma products used intraoperatively, and use of aortic conduits in arterial reconstruction.^15,31

Clinical presentation of hepatic artery thrombosis can be variable, depending on the time and severity of hepatic injury related to hepatic artery thrombosis. The most devastating is fulminant hepatic necrosis, which occurs in up to 33% of patients with hepatic artery thrombosis. Patients have rapid decompensation of liver synthetic function, fever, sepsis, hypotension, and coagulopathy, which can necessitate retransplantation. Somewhat more variable in nature are the biliary tract complications resulting from hepatic arterial ischemia or infarction. These include intrahepatic biliary strictures, intrahepatic bile leaks or bilomas, and biliary necrosis in up to 60% of cases of anastomotic hepatic artery stenosis and in up to 80% of cases of hepatic artery thrombosis.³² The clinical presentation of patients is variable. Some patients may present with intermittent episodes of sepsis without a clear source, presumably caused by focal abscesses in areas of infarcted liver or biliary necrosis. Others may remain asymptomatic or mildly symptomatic, with a diagnosis of hepatic artery thrombosis made incidentally.

For suspected postoperative hepatic artery thrombosis, ultrasonography is usually the first imaging modality performed because of its speed and portability. In addition to gray-scale two-dimensional imaging, color, power, and spectral Doppler ultrasound examinations may be performed to maximize chances of evaluating arterial flow. In experienced hands, ultrasonography has achieved up to 92% sensitivity for detection of hepatic artery thrombosis. Spectral Doppler findings include progressively decreased to absent diastolic flow, decreased slope and amplitude (tardus et parvus) of the peak systolic velocity, and finally absence of the hepatic waveform altogether. If this process is prolonged, the development of intrahepatic arterial collateral vessels can lead to a false-negative examination.³³ However, these collateral intrahepatic arterial vessels are often not completely normal, also often demonstrating a tardus-parvus waveform. CTA (Fig. 111-6) or MRA studies are usually relied on to confirm ultrasound findings and to determine the extent of the problems. False-positive diagnoses by Doppler study can be due to severe hepatic edema, hypotension, high-grade hepatic arterial stenosis, or technical limitations.

FIGURE 111-6 Hepatic artery thrombosis. A, Spectral Doppler ultrasound image demonstrates a tardus et parvus waveform in the left hepatic artery of a patient after an orthotopic liver transplantation. B, Axial CTA image demonstrates the development of a hepatic artery thrombosis (arrow). C, Coronal reformatted image from the same CTA confirming the hepatic artery thrombosis (arrow).

By CTA or MRA, arterial thrombosis of the hepatic artery (Fig. 111-7) or of other vessels (celiac artery, Fig. 111-8) is readily diagnosed. Hepatic arterial thrombosis can be diagnosed by the lack of contrast media opacification of the hepatic artery or graft. Hepatic artery thrombosis is often associated with hepatic and biliary complications (Figs. 111-9 to 111-12). Intrahepatic collateral vessels can be seen if progression toward hepatic artery thrombosis is advanced.

FIGURE 111-7 Hepatic artery thrombosis. A, Coronal reformatted image from CTA demonstrates hepatic artery thrombosis (arrow) in an orthotopic liver transplantation patient. B, Conventional x-ray hepatic angiography confirms the hepatic artery thrombosis (arrow).

FIGURE 111-8 Celiac artery thrombosis. Axial images from CTA demonstrate thrombosis in the celiac artery (arrow). The hepatic artery and splenic artery remain patent.

FIGURE 111-9 Hepatic artery thrombosis and biliary necrosis. A, Axial image from CTA of an orthotopic liver transplantation patient in hepatic arterial phase. The hepatic artery is not seen in its expected location because of thrombosis. B, Corresponding portal venous phase image demonstrating biliary necrosis.

FIGURE 111-10 Hepatic artery thrombosis associated with hepatic infarction and necrosis. Venous phase from CTA demonstrates hepatic infarcts (arrows) and necrosis in a patient with hepatic artery thrombosis after an orthotopic liver transplantation.

FIGURE 111-11 Hepatic artery thrombosis with associated hepatic and biliary findings. Hepatic artery thrombosis in an orthotopic liver transplantation patient is seen on MR to be associated with altered hepatic perfusion and biliary dilation. A, Postcontrast T1-weighted two-dimensional gradient-echo images with fat saturation in an early arterial phase reveal diminished perfusion (asterisk). B, Postcontrast T1-weighted two-dimensional gradient-echo images with fat saturation in a venous phase reveal dilated dark biliary ducts. C, Bright dilated biliary ducts are also noted on T2-weighted images.

FIGURE 111-12 Hepatic artery thrombosis associated with biliary necrosis. A, CTA demonstrates hepatic artery thrombosis (arrow) in an orthotopic liver transplantation patient. B, Subsequent endoscopic retrograde cholangiopancreatography image demonstrates development of biliary necrosis.

Because hepatic artery thrombosis may be clinically manifested with a spectrum of mild to severe clinical symptoms, its treatment varies correspondingly. In fulminant hepatic failure, the patient is resuscitated and listed for retransplantation. If thrombosis is acute and patients are symptomatic or minimally symptomatic, operative exploration with arterial reconstruction is performed. If the celiac artery inflow is adequate, thrombectomy with revision of the thrombosed segment may be performed without arterial reconstruction. If the inflow is inadequate, revascularization with an end-to-side anastomosis with the aorta or an interposition arterial graft is performed (Figs. 111-13 and 111-14). In some centers, percutaneous catheter–mediated thrombolysis, with or without angioplasty and stenting, is performed in those patients who are asymptomatic or minimally symptomatic. This technique works best in acute or subacute thromboses. Percutaneous management of biliary complications may be sufficient, but retransplantation may be required when diffuse biliary injury and breakdown are accompanied by infection. If the thrombosis is late and the patient is asymptomatic, the patient may be expectantly observed with no intervention performed because hepatic arterial collateral vessels may be sufficient.^34–36

FIGURE 111-13 Patent hepatic arterial conduit. Volume rendered image from CTA in a patient after an orthotopic liver transplantation reveals a patent hepatic arterial graft conduit (arrow).

FIGURE 111-14 Thrombosed hepatic artery conduit. A, Fluoroscopic abdominal aortogram demonstrates an abrupt cutoff of a hepatic artery conduit (arrow), indicating thrombosis, in a patient after an orthotopic liver transplantation. B, CTA in the same patient shows multiple hepatic infarcts (arrows). C, Follow-up CTA reveals the development of biliary dilation and bilomas (arrows). D, Corresponding spectral Doppler ultrasound image with tardus et parvus waveform in the right hepatic artery.

Hepatic artery stenosis is a common vascular complication of orthotopic liver transplantation, with a prevalence between 5% and 11%.^25,30,37 It can be difficult to diagnose because many cases progress to hepatic artery thrombosis by the time clinical symptoms develop. Hepatic artery stenosis most often occurs at the vascular anastomosis. Early clinical findings may be manifested by biliary dysfunction or graft failure progressing to cholangitis or areas of ischemic infarcts.

Doppler ultrasound study is frequently performed in the evaluation of hepatic artery stenosis. Elevation of blood flow velocities by twofold to threefold at the hepatic artery anastomosis, increased downstream diastolic flow, and downstream tardus-parvus arterial waveforms within intrahepatic arteries are diagnostic criteria. Mild degrees of stenosis, however, may have normal Doppler findings. CTA and MRA are more direct methods for anatomic assessment of the anastomosis and are sensitive in the evaluation for stenosis. Both CTA and MRA can overestimate the degree of narrowing.^22,25,26,38 Stenosis at the celiac axis should be assessed in all cases during evaluation of the hepatic arterial inflow (Figs. 111-15 to 111-17).

FIGURE 111-15 Volume rendered image from CTA demonstrates stenosis of the hepatic artery (arrow) in an orthotopic liver transplantation patient.

FIGURE 111-16 CTA demonstrates a high-grade hepatic artery stenosis (arrow) in a patient who had undergone an orthotopic liver transplantation.

FIGURE 111-17 Conventional x-ray hepatic arteriogram demonstrates hepatic artery stenosis in an orthotopic liver transplantation patient.

In patients who are symptomatic or who have a long-segment stenosis, operative revision may be performed. Otherwise, hepatic artery stenosis can be successfully treated with angioplasty, which can improve graft survival by preventing progression to arterial thrombosis.^39–41

Hepatic artery pseudoaneurysm (Fig. 111-18) is a rare complication of liver transplantation. Often at the vascular anastomosis, and frequently mycotic in nature, it is at increased risk for rupture. A pseudoaneurysm can be intrahepatic or peripheral after biopsy, instrumentation, or infection.^16,30 It can be treated surgically or by transarterial embolization.

FIGURE 111-18 Hepatic artery stenosis after an orthotopic liver transplantation. A, Spectral Doppler ultrasound interrogation of the left hepatic artery in an orthotopic liver transplantation patient demonstrates a tardus et parvus waveform. B, Volume rendered image from CTA demonstrates severe hepatic artery stenosis with small pseudoaneurysm (arrow). C, Conventional x-ray hepatic angiography confirms the hepatic artery stenosis and pseudoaneurysm seen on CTA.

Portal Vein

Portal vein thrombosis (Figs. 111-19 and 111-20) is an uncommon complication after orthotopic liver transplantation. Seen in 1% to 3% of cases, it can develop as late as 5 years after transplantation.^{18,21–23,25,30} Causes include surgical technique, misalignment or excessive vessel length, hypercoagulable states, previous portal vein surgery, and thrombus formation from portal venous bypass cannula used at transplantation. By ultrasound examination, echogenic thrombus within the portal vein is demonstrated. In some acute settings, the thrombus can be anechoic. In all instances, color Doppler and spectral analysis should be performed. On CT and MR, portal vein thrombosis is evident with lack of contrast media enhancement, either complete or partial, within the portal vein. MR has the added ability to detect thrombus without the need for contrast media by bright blood pulse sequences such as steady-state free precession. Postoperative venous aneurysms can also be seen (Fig. 111-21).

FIGURE 111-19 Portal vein thrombosis. A, Initial CTA examination after transplantation demonstrated a patent left portal vein. B, Follow-up CTA examination reveals new thrombus (arrow) in the left portal vein.

FIGURE 111-20 Coronal gadolinium-enhanced three-dimensional MRA with nonocclusive thrombus in the main portal vein (arrowhead) as well as right hepatic lobe abscess (arrow) in a patient after an orthotopic liver transplantation.

FIGURE 111-21 Coronal reformatted image from CTA reveals an extrahepatic portal vein and splenic vein aneurysm containing calcified thrombus (arrow) in an orthotopic liver transplantation patient.

Portal vein thrombus in the early post-transplantation setting can be manifested by graft failure, ascites, intestinal congestion, and gastrointestinal bleeding. Mortality is high in this setting; it can be treated by thrombectomy and in some instances may require retransplantation. Late portal vein thrombus can be treated with anticoagulation therapy if graft function is preserved. In some instances, a portacaval shunt may be required.

Portal vein stenosis (Fig. 111-22) can be an incidental finding or can be manifested by symptoms of portal hypertension.³⁰ In interpreting studies, however, it is important to note that size discrepancy between the donor and recipient portal vein can cause an apparent anastomotic stenosis. By Doppler ultrasound examination, an elevation in the velocity at the anastomosis by three or four times suggests a hemodynamically significant stenosis. Both CTA and MRA can demonstrate anastomotic narrowing. If it is not associated with other stigmata of portal hypertension, it is nonspecific in terms of hemodynamic significance. In evaluating the functional significance of an anastomotic narrowing, portal venography should be performed. A pressure gradient of 5 mm Hg or higher is compatible with a significant stenosis. Symptomatic stenosis can be treated by segmental portal vein resection or percutaneously by angioplasty with or without stent placement (Figs. 111-23 and 111-24).^39,42

FIGURE 111-22 Portal vein stenosis. A, Coronal image from gadolinium-enhanced three-dimensional MRA demonstrates an extrahepatic portal vein stenosis (arrow) in an orthotopic liver transplantation patient. Note collateral vessel (arrowhead). B, Conventional x-ray portal venogram confirms the findings on MRA. Note abundant collateral vessels. Venoplasty was performed.

FIGURE 111-23 Portal vein stenosis. A, Gadolinium-enhanced three-dimensional MRA demonstrating extrahepatic portal vein stenosis (arrow) in an orthotopic liver transplantation patient. B, On corresponding x-ray fluoroscopic image during venoplasty, a stenotic waist (arrow) in the portal vein is seen. The stenosis was associated with a portal venous pressure gradient from 12 mm Hg to 1 mm Hg. C, Follow-up three-dimensional gradient-echo MRA demonstrates reduction of the portal vein stenosis (arrow).

FIGURE 111-24 Portal vein stenosis. A, Coronal gadolinium-enhanced three-dimensional MRA demonstrates stenosis of the extrahepatic portal vein in a patient after an orthotopic liver transplantation. B, Conventional x-ray portal venogram confirmed the stenosis, and venoplasty was undertaken. C, Postvenoplasty x-ray portal venogram revealed reduction of the portal vein stenosis.

Hepatic Veins and Inferior Vena Cava

IVC stenosis is rare, occurring in less than 1% of transplants.^23,30 It is caused by technical problems related to surgery or compression by fluid collections.⁴² The clinical findings in significant IVC stenosis include hepatomegaly, pleural effusions, ascites, and extremity edema.¹⁶ A hemodynamically significant stenosis at the anastomosis may be manifested as a threefold to fourfold increase in velocity by spectral ultrasound examination. There may be dampened or reversed flow within the hepatic veins in a significant supracaval stenosis. With CTA or MRA, lack of or partial opacification of portions of the IVC due to thrombus or narrowing of the caval anastomosis can be seen (Figs. 111-25 to 111-28). As in portal vein stenosis, care must be taken not to mistake size discrepancy at the anastomosis between donor and recipient vessels for a hemodynamically significant stenosis (see Fig. 111-26). If a hemodynamically significant stenosis is suspected, venography should be performed to determine the presence of a significant pressure gradient. If one is found, angioplasty and stent placement can be successful.³⁹

FIGURE 111-25 IVC stenosis. A, Coronal reformatted image from CTA demonstrates a suprahepatic IVC anastomotic stenosis (arrow) in a patient after orthotopic liver transplantation. Note that a right pleural effusion is also present. B, The IVC anastomotic stenosis (arrow) is seen also on a corresponding gadolinium-enhanced three-dimensional MRA image.

FIGURE 111-26 IVC stenosis and thrombosis. Coronal reformatted images from CTA in a patient after an orthotopic liver transplantation reveal an infrahepatic IVC stenosis (A, arrow) and caval thrombosis (B, arrow). Note that ascites (A, asterisk) is also present.

FIGURE 111-27 Coronal gadolinium-enhanced T1-weighted two-dimensional gradient-echo image with fat saturation demonstrates extensive IVC thrombosis (arrow) as a result of a supracaval anastomotic stricture.

FIGURE 111-28 Coronal gadolinium-enhanced three-dimensional MRA reveals mild and clinically insignificant narrowings of the suprahepatic IVC anastomosis (A, arrow) and infrahepatic IVC anastomosis (B, arrow).

In cases of a piggyback caval anastomosis, there is an increased risk for venous outflow obstruction. Presumptive causes include direct compression of the vein by a graft that is too large, twisting of the venous anastomosis by a graft that is too small, surgical factors such as tight sutures, and, in late cases, intimal hyperplasia and fibrosis. Endovascular treatment with balloon-expandable stents can be an effective treatment in these cases.⁴³