Preoperative liver donor evaluation: Imaging and pitfalls

Preoperative Liver Donor Evaluation: Imaging and Pitfalls Koenraad J. Mortele´,* Vito Cantisani,* Roberto Troisi,† Bernard de Hemptinne,† and Stuart G. Silverman* This article discusses the rationale behind living (related) donor liver transplantation, the role of imaging in the preoperative evaluation of the potential donor, and the currently available imaging modalities for fulfilling this task. Furthermore, the normal hepatic vascular and biliary anatomy, as seen on imaging, is reviewed and the most common anomalies are highlighted. Finally, critical concepts in the diagnostic evaluation of a donor are discussed with special emphasis on how to accurately measure liver volumes. (Liver Transpl 2003;9:S6-S14.)

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here is an increasing demand for liver transplants in the United States, that is attributable, in part, to an increasing incidence of cirrhosis caused by hepatitis C and the detection of small hepatocellular carcinomas that are curable with transplantation.1,2 To cope with the shortage of donor organs for transplantation, cadaveric split liver transplantation and living (related) donor transplantation were introduced. Since the 1980s, adults have successfully donated portions of their left lobes to pediatric patients, with a transplantation survival rate of 80%.3-5 This success has sparked an international interest in applying the same procedure in adults.6 Recent improvements in surgical technique have permitted the safe performance of right hepatectomy for transplantation, thereby allowing adults awaiting transplants to benefit from living-related donors.7 However, given the far greater complexity of right hepatectomy, safe harvesting and successful transplantation requires careful selection of donors. The role of imaging in the preoperative evaluation of a potential donor is important. Preoperative imaging of the donor is essential in excluding focal or diffuse liver disease (e.g., steatosis); in detecting vascular abnormal-

ities (e.g., portal vein thrombosis), vascular anomalies, and biliary anatomic variants; and in assessing liver volumes. Identifying vascular and biliary anatomic variants is crucial, and requires sufficient knowledge of normal anatomy. Anatomic variants are common. For example, the usual arterial anatomy, as described by Michels,8 is only seen in 55% of the general population, whereas the common biliary tract anatomy is visualized only 65% of the time. Because many of these anatomic variants preclude living donor liver transplantation, preoperative recognition is mandatory to avoid unnecessary laparotomies in healthy subjects. Currently, there is no clear consensus regarding which imaging modality is the best method for the evaluation of a potential donor. Both multiphasic multidetector computed tomographic (CT) and magnetic resonance imaging (MRI) are accurate in the detection and characterization of focal liver disease. CT and MRI angiography both allow sufficient evaluation of the hepatic vasculature, including visualization of thirdorder branches of the arterial system. Both techniques provide accurate assessments of liver volumes. CT has disadvantages compared with MRI because of exposure to ionizing radiation, the use of a potential nephrotoxic and allergenic contrast material, and the absence of information about the biliary tract unless performed with orally administered biliary contrast agents.9 Another advantage of MRI compared with CT is its higher sensitivity in the detection of diffuse liver diseases.

Preoperative Donor Evaluation Focal and Diffuse Liver Disease

From the *Department of Radiology, Division of Abdominal Imaging and Intervention, Brigham & Women’s Hospital, Harvard Medical School, Boston, MA, and †Department of Surgery, Liver Transplant Unit, University Hospital Ghent, Ghent University, Belgium. Address reprint requests to Koenraad J. Mortele´, Department of Radiology, Abdominal Imaging and Intervention, Brigham & Women’s Hospital, Harvard Medical School, 75 Francis St, Boston, MA 02115. Telephone: 617-732-7624; FAX: 617-732-6317; E-mail: kmortele@ partners.org Copyright © 2003 by the American Association for the Study of Liver Diseases 1527-6465/03/0909-0024$30.00/0 doi:10.1053/jlts.2003.50199

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The first step in the comprehensive preoperative evaluation of a potential donor is a screening test for the presence of focal liver disease. In a study reported by Fulcher et al,9 focal liver lesions were detected in 18% of living liver donors. Although almost all such lesions are benign cysts or hemangiomas, the presence of any lesion, especially when large, can preclude a right lobe transplant. Donors should be evaluated also for the presence and extent of hepatic steatosis. Marsman et al10 noted that the acceptable upper limit of steatosis in a donor liver is 30% because liver grafts with more than

Liver Transplantation, Vol 9, No 9, Suppl 1 (September), 2003: pp S6-S14

Preoperative Liver Donor Evaluation: Imaging and Pitfalls

30% fatty change carry an unacceptable high risk of postoperative liver dysfunction in the donors and graft nonfunction in the recipients. Fatty infiltration is recognized on CT as regions of low attenuation of liver parenchyma, often with geographic borders. The entire liver may be involved. Focal fatty change typically occurs anterior to the porta hepatis and straddling the falciform ligament. The native attenuation value of normal liver on unenhanced CT typically measures between 45 and 65 HU, and is generally at least 8 HU

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higher than the spleen.11 In patients with fatty change, however, liver parenchymal attenuation is reduced, typically 10 HU less than the spleen on unenhanced CT (Fig. 1A) and 25 HU less than the spleen on enhanced CT.12 Because the relative densities of liver and spleen are variable on enhanced CT scans, the diagnosis of hepatic steatosis is more reliably made on nonenhanced images. The most sensitive technique for detecting fatty change of the liver is, however, the use of gradient echo MR pulse sequences because of the lack of a 180° refo-

Figure 1. Liver steatosis. (A) Unenhanced axial computed tomography scan shows markedly decreased density of the liver (compared with the spleen) because of fatty change of the liver. (B) In-phase breath-hold gradient-echo T1-weighted magnetic resonance image shows the liver to be brighter in signal intensity than the spleen. (C) Out-of-phase magnetic resonance image shows a significant decrease in signal intensity of the liver characteristic of diffuse fatty change.

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cusing pulse.13 By varying the echo time (TE) to image water and fat in and out of phase, the chemical shift between water and lipid protons can be shown.14 With in-phase imaging, typically performed with a TE of 4.2 ms at 1.5 Tesla, water and lipid protons are in phase and their intravoxel signal intensities are additive. During out-of-phase imaging, obtained with a TE of 2.1 ms, the intravoxel signal intensities of water and fat are directly opposed and cancel each other out.14 Thus, on out-of-phase images, tissues with intracellular lipid will show lower signal intensity than on the corresponding in-phase images. This loss of signal intensity between the two types of images allows physicians to establish the diagnosis of fatty change13,15 (Fig. 1B to 1C). The detection of fatty change is so important that many surgeons routinely biopsy the donor’s liver before surgery to exclude it, despite the fact that parenchymal liver biopsy carries an estimated complication rate of 1%.16,17 In the future, MR spectroscopy (MRS) may be sensitive enough to exclude fatty infiltration.9 MRS, in fact, allows the examination of resonance frequencies of all proton species within a region of interest. Although the absolute differences in resonance frequencies in MRS are relatively small, they can be separated out into a spectrum based on individual frequencies. MR spectra are traditionally plotted on an axis of chemical shift expressed as parts per million (ppm). This facilitates comparison between spectra obtained at different field strengths because chemical shift does not depend on the strength of the magnetic fields. In MRS, the concentration of any given molecule in a sample is represented by the height of the specific resonance peak within the spectrum, or more precisely the area under the peak.18 Spectroscopic evaluation of hepatic steatosis requires evaluation of the two dominant peaks within the unsuppressed MR spectrum, water at 4.7 ppm and lipid at 1.0 to 1.5 ppm. Livers with fatty change show an increase in the intensity of the lipid resonance peak. Because MRS allows direct measurement of the area under the lipid resonance, it can thus be used both to detect fatty change and to quantify it. To date, only isolated reports have described the use MRS to assess fatty change in vivo.19,20 Thomsen et al19 have observed a correlation between the amount of liver lipid assayed by proton spectroscopy and chemical methods in liver bioptates from patients with postalcoholic liver steatosis at various stages. However, they have not observed any essential relationships between the histologic degree of steatosis and the lipid contents determined chemically. On the other hand, Longo et al20 have shown a relationship between histologic degree of liver steatosis and lipid contents evaluated on

the basis of 1H MR examinations. Further studies are needed to evaluate the clinical effectiveness of this new technique before it is used clinically. Volume Assessment of total and segmental liver volumes of both the recipient and donor are needed to gauge the appropriateness of the donor liver size because the graft and the remainder of the liver must be adequate to provide function in the recipient and donor, respectively. Liver remnant volume of 30% to 40% of the total liver volume is sufficient for a donor to survive, provided that the parenchyma is normal without evidence of fatty change.21 The minimum graft volume required to provide sufficient hepatocellular function in the recipient is approximately 40% of the standard liver mass21 as calculated using the body surface area.22 The larger the graft, the more challenging the surgery, especially when performing the vascular anastomosis and when controlling bleeding. Small-for-size grafts are prone to dysfunction, not only because of insufficient functional hepatic mass but also because the graft and sinusoidal cells may be injured by excessive portal perfusion.23 A small-for-size graft is also prone to torsion. In such cases, the falciform ligament can be surgically fixed to the anterior aspect of the peritoneal cavity to reduce the risk of this rare complication. Determining the liver volume in the recipient is also helpful in assigning priority to transplant candidates. Small livers in cirrhotic patients have the poorest function, making transplantation more urgent.24 Volume calculations are achieved by hand-tracing of the assigned liver segments, with exclusion of large vessels and major fissures, which allows automated surface calculation on all currently commercially available CT and MRI scanners. Liver volumes, expressed in cm3, are then obtained by multiplication of the surface areas with the used slice thickness. A three-dimensional model of the liver can then be generated using the “paintbrush” method, with commercially available software. A virtual right hepatectomy, using the liver and hepatic vein models as guidance, in a curved plane, can be performed (Fig. 2A). The plane should avoid major vessels, traversing between the right and left lobes, immediately to the right of the middle hepatic vein (Fig. 2B). This relatively avascular plane lies along the main portal scissura, which corresponds to the anatomic Cantlies line.25 Finally, because the relative attenuation of liver and water approximate 1 g/mL, liver weight in grams can be calculated. The reported correlation between liver volume estimations, both by CT and MRI, and the actual weight is sufficiently high.9,25

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sures perfused liver while postoperative weight measurements are performed on exsanguinated liver. Biliary Tract Anatomy

Figure 2. Virtual hepatectomy. (A) Three-dimensional image of the liver reconstructed from an axial computed tomography data set shows volume-rendered hepatic veins and virtual hepatectomy plane adjacent to the middle hepatic vein. (B) Axial contrast-enhanced computed tomography image shows the presumed location of the right hepatectomy plane in a living related donor.

Usually, the calculated liver volume typically overestimates the actual weight of the graft because of several reasons25: (1) imaging sometimes does not depict the peripheral course of the middle hepatic vein (MHV); (2) during surgery, a thicker plane of dissection next to the MHV is used compared with the trace immediately left to the MHV; and finally, (3) the radiologist mea-

In the assessment of a living related donor, a thorough knowledge of normal biliary anatomy is crucial. MR cholangiography (MRCP) is now the modality of choice for noninvasive evaluation of the biliary tract anatomy.26 In fact, intraoperative cholangiography, considered the gold standard, is invasive and uses ionizing radiation. Endoscopic retrograde cholangiopancreatography is invasive also and has multiple inherent complications. New techniques, including CT cholangiography and MRCP after administration of a hepatobiliary contrast agent, have not been fully established yet. Normally, the right posterior duct courses to the right and fuses with the right anterior duct from a left (medial) approach to form the right hepatic duct. The left hepatic duct is formed by segmental tributaries draining segments II to IV. The common hepatic duct is formed by fusion of the right and left hepatic ducts. The bile duct draining the caudate lobe usually joins the origin of the left or right hepatic duct.27 The cystic duct typically joins the common hepatic duct below the confluence of the right and left hepatic ducts. This normal biliary anatomy is thought to be present in 58% of the population.26,27 The most common anatomic variants in the branching of the biliary tree involve the right posterior duct and its fusion with the left hepatic duct, which can occur in 13% to 19% of the population,27,28 or with the right aspect of the right anterior duct27,28 (Fig. 3). Another common variant of the main hepatic biliary branching is the so-called triple confluence, which is an anomaly characterized by simultaneous emptying of the right posterior duct, right anterior duct, and left hepatic duct into the common hepatic duct and occurr in 11% of the patients.26 Several less common and more complicated anatomic variations of the bile ducts have been described and consist of both aberrant and accessory bile ducts. Familiarity with these two different entities is important clinically because an aberrant bile duct is the only bile duct draining a particular hepatic segment, whereas an accessory one is an additional bile duct draining the same area of the liver.29 Therefore, inadvertent ligation of aberrant branches draining the remnant liver would lead to atrophy of the involved portions. The direct drainage of the right posterior duct into the common hepatic duct, right-or left-sided, is a variant also known as the aberrant hepatic duct and is present in approximately 5% and less than 1% of the population, respectively.26

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Figure 3. Intrahepatic biliary anatomic variation. Coronal oblique thick-slab projective magnetic resonance cholangiography image of the biliary tree shows drainage of the right posterior biliary duct into the left hepatic duct.

Accessory hepatic ducts are observed in approximately 2% of patients and may originate either the left or right ductal system.27 Although biliary duct variants do not usually preclude right lobe resection in many institutions, their identification usually indicates that multiple anastomoses will be required. Evaluation of Arterial Hepatic Vasculature Preoperative knowledge of vascular anatomy is important in the comprehensive workout of a liver donor

because transplant survival mandates patency of all supplying and draining vessels. Knowledge of the Michels classification of arterial variations is, therefore, essential (Table 1).8 In fact, the risk of arterial thrombosis is one of the most common severe complications of right donor liver transplantation, and can be dramatically reduced if grafts with unfavorable arterial anatomy are excluded.30 Digital substraction arteriography of the hepatic vasculature used to be done routinely. Now multidetector CT and gadolinium-enhanced magnetic resonance angiography can be used to assess hepatic vasculature.31-35 When compared with single-detector helical CT, multidetector CT provides better multiplanar and three-dimensional images, and allows more accurate delineation of the intrahepatic tertiary branches as small as 1 mm in size.34 There are two common techniques for three-dimensional reconstructions: surface rendering, also called shaded surface display, and volume rendering. The latter incorporates all of the image data and allows more flexibility in manipulating the display but at the same time requires more computing power. CT arterial and MR angiography data sets using several three-dimensional techniques permit a comprehensive assessment of all supplying and draining vessels of the liver. The complex vascular anatomy, often difficult to delineate with conventional angiography, can be “dissected” and interactively scrolled in any desired plane, thus allowing the identification of all anatomic variants with high confidence. Arterial anatomy influences donor selection because liver grafts with multiple arteries are usually avoided and significant anomalies (e.g., replaced left hepatic artery), in many centers, exclude right hepatectomy (Fig. 4). When the main hepatic artery originates from the superior mesenteric artery instead of the celiac axis,

Table 1. Hepatic Arterial Variants According to Michels8 Variant Type I II III IV V VI VII VIII IX X

Description Conventional anatomy: proper HA arising from common HA and giving rise to right and left HAs as the sole supply of arterial blood to liver Replaced left HA arising from left gastric artery Replaced right HA arising from SMA Both replaced left and right HAs described for types II and III Accessory left HA arising from left gastric artery Accessory right HA arising from SMA Accessory right HA arising from SMA and accessory left HA arising from left gastric artery Replaced right HA and accessory left HA or replaced left HA and accessory right HA Entire hepatic trunk arising from SMA Entire hepatic trunk arising from left gastric artery

Abbreviations: HA, hepatic artery; SMA, superior mesenteric artery.

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Evaluation of Venous Hepatic Vasculature When evaluating venous anatomy, both portal and hepatic, here the major task of the radiologist is to determine the size and length of the veins to plan the site of anastomosis; to detect aberrant vessels or side branching that might interfere with the avascular nature of the surgical plane, venous supply, and drainage of the graft; and the number of anastomoses needed. Variations in the portal venous anatomy are seen in approximately 20% of cases and have been described

Figure 4. Arterial anatomic variant. Three-dimensional volume-rendered image of the hepatic vasculature reconstructed from a contrast-enhanced computed tomography data set shows a replaced left hepatic artery originating from the left gastric artery.

it takes an aberrant course deep to the portal vein. This course may necessitate alteration of the routine sequence of vascular anastomoses during transplantation such that the arterial anastomosis is performed before the portal venous anastomosis.36 Depiction of the arterial supply to segment IV, which arises from the right hepatic artery in approximately 11% of patients, is very important because preservation of the vascular supply to segment IV is mandatory to ensure function of this segment in the donor7,37 (Fig. 5). In fact, its origin may not be appreciated intraoperatively without significant dissection at the porta hepatis. When performing a right lobectomy, the surgeon divides the right hepatic artery distal to the branches to segment IV to ensure adequate blood supply during regeneration of the remaining left lobe. If the artery to IV segment arises from the right hepatic artery, the distance between its origin and the origin of the right hepatic artery is important because it provides reference to the surgeon during graft harvesting.34 The size of the recipient hepatic artery determines the arterial blood flow to the liver. A small-caliber recipient hepatic artery (3 mm or less) or multiple small hepatic arteries supplying the liver from different sources may result in inadequate arterial inflow to the graft after transplantation and may require an alternative inflow source, such as an aortohepatic interposition graft.36

Figure 5. Normal arterial anatomy. Contrast-enhanced thin-section computed tomography images show the arterial branch supplying segment 4 originating from the left hepatic artery.

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using ultrasound and CT arterial portography.33,38 Important portal venous variants to recognize include: (1) absence of the right portal vein (PV). This occurs in 16.5% of patients and is associated with trifurcation of the main PV to right anterior, posterior segmental veins and left PV (Fig. 6A); direct origin of right posterior

Figure 6. Portal-venous anatomic variants. (A) Maximum-intensity projection image of the portal-venous vasculature reconstructed from a contrast-enhanced magnetic resonance imaging data set shows trifurcation of the portal vein. (B) Three-dimensional volume-rendered image of the portal vein reconstructed from a contrastenhanced computed tomography data set shows origin of the left portal vein from the anterior branch of the right portal vein.

segmental branch from main PV; or origin of right anterior segmental branch from left33; and (2) absence of left PV. This occurs in 1% of patients. Portal vein trifurcation is a relative contraindication to liver transplantation using living related donors because multiple anastomoses will be needed for right lobe graft transplantation. A left portal vein arising from the anterior branch of the right PV is another relative contraindication for right lobe living transplant because of the short length of the grafted portal vein, the need for multiple anastomoses, and an increased risk for PV thrombosis (Fig. 6B). Variations of hepatic venous anatomy are common and have been visualized by ultrasound in approximately 30% of cases.39 These also have been depicted on CT arterial portography33 and by MR angiography with high diagnostic accuracy.9 The radiologic requirements for hepatic vein delineation depend largely on the experience and preference of local surgeons. The axial images acquired using multidetector CT during the portal venous phase show best early branching and early bifurcation of the middle hepatic vein that may alter the right hepatectomy plane.34 To facilitate surgery, the site of the confluence of the middle hepatic vein is identified, allowing the surgeon to anticipate where larger venous structures will need to be transected. In addition, it is very important to clearly depict: (1) the presence of a vein in segment 4 that drains into the left hepatic vein; (2) the branching and size of side branches of the middle hepatic vein. For instance, if there is an early branching of the left branch of the middle hepatic vein into two major veins (Fig. 7A) detected in the preoperative evaluation of the right hepatectomy, the branch for segments 8 and 5 should be included in the graft and reimplanted for survival of segment 5/8; and (3) the presence of accessory hepatic veins measuring more than 5 mm in diameter. The latter is important because they are anastomosed to the inferior vena cava to prevent venous congestion of the corresponding liver part9 (Fig. 7B). Furthermore, acknowledgement of accessory veins may limit blood loss by careful dissection. Special attention should be paid to the presence of an accessory inferior right hepatic vein, which is reported in 68% of cases.25 This important vein should be preserved during surgery to reduce the risk of graft malfunction. If an accessory inferior right vein is identified, its distance from the right hepatic vein should be measured in the coronal plane. If the distance between the right hepatic vein and accessory inferior right hepatic vein is more than 4 cm, it may be difficult to surgically implant both

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tive evaluation of the liver in potential living donors. Both techniques allow accurate delineation of hepatic vascular anatomy and important anomalies in a noninvasive and reliable manner. MRI also delineates the biliary tract and is, therefore, probably the better technique. When using CT, the use of thin collimation provides accurate liver volume measurements and illustrative three-dimensional reconstructions that are helpful in virtual hepatic resection. Thorough knowledge of normal hepatic anatomy and its variants by the radiologist is important in the prevention of complications and tranplantation failures. Therefore, a close working relationship between radiologist and surgeon also helps assure that the knowledge guided by preoperative imaging of these patients is transmitted to the operating room.

Acknowledgement The authors thank Rolnick Joshua and Allen Jean for their help with creating the postprocessed three-dimensional images.

References

Figure 7. Hepatic venous anatomic variants. (A) Threedimensional volume-rendered image of the hepatic veins reconstructed from a contrast-enhanced computed tomography data set shows early trifurcation of the middle hepatic vein. (B) Contrast-enhanced computed tomography study shows a accessory hepatic vein with a diameter >5 mm draining directly into the inferior vena cava.

veins using a single partially occluding clamp on the recipient’s IVC.

Conclusions In conclusion, both multidetector CT and MRI are excellent modalities for “one-stop shopping” preopera-

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