The first successful solid organ transplant in humans was performed by Harrison and Murray in 1954, between two identical twins (1). Subsequent work on immunosuppression in the three decades after 1950 revolutionized the area of transplantation, facilitating the work of Starzl when he completed the first successful liver transplant (LT) in 1967 (2-5). In association with improvements in organ preservation and extended donor eligibility, organ transplantation has become an increasingly important and successful component of modern medicine with more than 34,000 transplants performed in the United States alone in 2017 (6). Imaging plays a critical role in organ transplantation as it allows assessment of donors and recipients both before and after transplantation. The growing use of living candidates to meet the demand for organ donors has resulted in frequent imaging of donors during pre-transplantation assessment. These requests are not restricted solely to tertiary transplant centers given the increasing development of regional and national transplant networks. Identification of donor anatomy, variants and any associated pathology is essential for the selection of appropriate surgical candidates and suitable surgical technique. This process has been facilitated by the improved multimodality protocols and techniques available to radiologists. Detailed knowledge and understanding of these options and protocols is critical to ensuring optimal patient outcomes, and ultimately survival. This article will focus on imaging evaluation of donor candidates for liver and pancreas transplantation.
First described in 1968, liver transplantation has since become the definitive treatment for end-stage liver disease in suitable recipient candidates (3). As a result, the number of LTs has increased substantially, with 8082 transplants performed in 2017 in the United States (US) compared to 1713 in 1988 according to the United Network for Organ Sharing (UNOS) (7). While living donor liver transplantation (LDLT) has become an increasingly accepted alternative to deceased donors over this period, it still only accounted for 11.5% of LTs in the US in 2014–2016, compared to 0% in 1988 (7-11). However, almost 14,000 candidates remain on the LT waiting list in the US as of May 2018 (12).
Types of liver transplantation
Depending on the nature of the organ used, liver transplantation broadly includes deceased donor transplantation and LDLT (13). Evaluation of the donor liver requires a knowledge of the segmental anatomy of the liver (Figure 1).
Deceased donor transplant
The most commonly performed LT surgical technique involves the replacement of the native liver with a donor liver from a deceased donor. LT can involve the transplant of the whole donor liver into one recipient, or a split liver transplant (SLT), whereby one donor liver is split into independent anatomical segments to allow for two recipients to be transplanted (11). SLT evolved from techniques developed to resize adult donor livers for pediatric recipients (14) and has been considered a means of expanding the donor pool in the context of a limited donor organ supply (15-17). SLT accounted for 1.2% of LT in adults in the US in 2016 (11).
The splitting of the donor liver into separate grafts can be performed in the donor prior to procurement or as a back-table procedure after retrieval, known as in situ and ex vivo techniques, respectively (18). The original technique allowed for the transplant of a child and adult, with the liver split along the falciform ligament into a left lateral segment incorporating segments II and III for the child and a larger tri-segment which includes segments I, IV, V, VI, VII and VIII for the adult (Figure 2A) (19). Subsequent advances have led to the development of a technique that allows for the creation of two comparably sized grafts, one including segments I–IV and the other segments V–VIII. The conventional dissection plane is made to the right of, or along, the middle hepatic vein (MHV) given the smaller volume of the left liver lobe, but alternative approaches and reconstructive techniques have been described in the literature (Figure 2B) (20-23).
Living donor liver transplant
LDLT involves removal of a portion of healthy liver from a matched donor and placement into a recipient. Current techniques and expertise result in an overall donor complication rate of 40%, a major donor complication rate of 1.3% and mortality rate of 0.2% (24-26). The critical factor to be considered when contemplating a LDLT is the health of the donor and that sufficient residual liver volume remains in the donor to avoid donor liver failure after hepatectomy. Sufficient residual liver volume should be at least 30–35% of the donor’s total liver volume depending on the quality of the underlying liver parenchyma (24,27,28). Ensuring that the graft weight/recipient body weight ratio (GWBWR) remains greater than 0.8% is also critical to minimize the risk of the recipient developing small for size syndrome (SFSS) (29). Both considerations influence the approach and technique to the donor hepatectomy.
If a graft is required for a pediatric recipient, a left lateral segmentectomy along the falciform ligament to include segments II and III can be performed as described for the deceased donor graft procurement. An alternate approach for an adult recipient includes a full left hepatectomy with the transection margin passing to the left of, or including, the MHV and sometimes segment I (Figure 3A). However, to avoid SFSS in the recipient, a full right hepatectomy is also a consideration, which involves segment V, VI, VII and VIII, and sometimes segment I (Figure 3B). This transection occurs along the MHV which is sometimes included in the donor graft depending on the risk to the donor (8,27,30).
Liver donor: imaging evaluation
Organ Procurement and Transplantation Network (OPTN) donor evaluation includes anatomical assessment of certain living liver donor parameters; projected graft volume, the donor’s remnant volume, vascular anatomy and determination of hepatic steatosis (31). This is predicated on the fact that up to 11% of potential LDLT donor candidates have been shown to be excluded from consideration for anatomic reasons (32), while another study found that 38% of donor candidates were excluded in total (33). Tailored multidetector computed tomography (MDCT) (Table 1) and magnetic resonance imaging (MRI) (Table 2) studies can be performed to achieve a comprehensive assessment of the donor anatomy (Table 3) (31).
Multiphasic contrast-enhanced CT provides improved spatial resolution relative to MRI, permitting evaluation of the liver parenchyma itself. A sample multiphasic protocol includes a limited non-contrast phase incorporating four 10 mm slices of the mid liver to allow for hepatic steatosis evaluation, an arterial phase of the whole liver with image acquisition triggered by bolus tracking from a region of interest over the aorta to evaluate the arterial anatomy and a portal venous phase of the whole liver acquired 60 seconds after contrast injection to assess the portal and hepatic venous anatomy (Table 1). Both post-contrast phases play a role in assessing for focal liver lesions. Isotropic MDCT data can be post-processed as necessary to allow for the creation of three-dimensional (3-D) image construction, maximum intensity projection and volume rendering. In addition, it allows for more accurate characterization of the hepatic vasculature [hepatic arteries (HAs), portal veins (PVs) and hepatic veins (HVs)] (37).
Dual energy CT (DECT) is now increasingly established in mainstream radiology practice since its commercial release in 2006 (38,39). It has been shown to improve the conspicuity of hypovascular liver metastases, as well as improved diagnostic accuracy and characterization of hypervascular liver lesions (39). In addition, the development of improved virtual enhanced images, as well as a reduced intravenous iodinated contrast requirement, may in future help to reduce donor radiation exposure (40,41).
Newer MRI techniques acquired over shorter periods allow for increasing spatial resolution in studies without any associated radiation exposure to the donor. The availability of hepatobiliary contrast agents also permits the delineation of biliary anatomy, which is particularly important given the discontinuation of the CT cholangiographic contrast agent, iodipamide meglumine (42). These agents, including gadoxetate disodium and gadobenate dimeglumine, allow for sensitivity and specificity of up to 88% and 93% respectively when combined with heavily T2 weighted 2D and reconstructed 3D maximum intensity projection magnetic resonance cholangiograms (43,44). Given the equivalent biliary image quality associated with both agents, gadoxetate disodium (Eovist; Bayer AG, Leverkusen, Germany) is increasingly favored due to its shorter hepatobiliary phase image acquisition timing of 10–20 minutes versus up to 60 minutes for gadobenate dimeglumine (34,45). The use of post-processing MRI techniques, such as multiplanar reconstruction (MPR), allows for the creation of clear images which can be of assistance in defining the anatomy and surgical planning (Figure 4).
In the context of MRI utilization, radiologists must remain cognizant of the consequences of gadolinium administration. While the incidence of adverse reactions is reported to be 0.01–2.4%, lower than that associated with iodinated CT contrast agents, and with an exceedingly low mortality rate of 0.00008% to 0.0019% (46), the use of gadolinium in those patients with renal impairment remains controversial. Nephrogenic system fibrosis (NSF) is a systemic fibrosing process with high morbidity and mortality first described in 1997 and subsequently linked to gadolinium-based contrast agents (GBCAs) in 2006 (47). It is most closely linked with the use of certain linear non-ionic GBCA in the setting of renal dysfunction, either chronic kidney disease (CKD) or acute kidney injury (AKI) (48). However since its identification and characterization, NSF has been almost eliminated after changes in the Food and Drug Administration (FDA) and European Medicines Agency (EMA) regulatory framework (49,50), and subsequently in the European Society of Urogenital Radiology (ESUR) and the American College of Radiology (ACR) guidelines (51,52), resulting in the withdrawal or restriction of the GBCAs of concern and more rigorous evaluation of contrast use in those patients with renal impairment. An ongoing discussion centers on the recently established entity of gadolinium deposition within bone and the central nervous system (CNS), even in the absence of renal impairment or increased blood-brain barrier permeability (53-58). Recent studies have also demonstrated a relationship between the degree of deposition and the numbers of doses and types of GBCAs, particularly linear agents, administered (59). Despite an updated FDA Drug Safety Communication being issued in May 2018 (60), no adverse consequences to tissue deposition of gadolinium have been identified but clinical discretion regarding the judicious use of GBCAs remains important (51).
Hepatic parenchymal evaluation
Imaging of the donor hepatic parenchyma should allow for evaluation for both focal and diffuse hepatic processes. The incidence of hepatic steatosis (HS) amongst donor candidates has been estimated at 25% (61). Moderate-severe HS (30–60% hepatic steatosis) in deceased donor livers is associated with decreased graft survival, while severe HS (>60% hepatic steatosis) is associated with an increased risk of poor graft function and primary graft non-function requiring re-transplantation (62,63). Recipient outcomes using grafts with varying fatty infiltration beneath 30% do not vary significantly and therefore, deceased donor grafts with greater than 30% fatty infiltration are not commonly considered (64-66), while this threshold falls to 10–15% for LDLT grafts at most centers (67). A further influencing factor limiting use of moderate-severe HS LDLT grafts is the increased perioperative mortality and morbidity associated with major hepatectomies (68), and the additional risk to the donor. While liver biopsy remains the gold standard for assessment of HS, it still carries complication and mortality rates of 0.6% and 0.03% respectively (69), and therefore non-invasive assessment is preferred in living donors. CT can be used to quantify moderate-severe HS by a number of means; an absolute liver parenchymal attenuation less than 40 Hounsfield Units (HU), a liver/spleen attenuation ratio of less than 0.8, both on a non-contrast CT, an attenuation of 10 HU or greater less the spleen (35,70,71). Overall, CT demonstrates high accuracy in detecting moderate-severe HS in liver donors (72) but is less effective in quantitative assessment of HS (73). MRI Dixon-based protocols which demonstrate 30% signal drop out on the out of phase sequences relative to in phase sequences normalized to spleen have been shown to effectively differentiate mild-moderate HS from moderate-severe HS (34,74,75). In addition to hepatic steatosis, it is important not to overlook any other parenchymal abnormality such as hemochromatosis, or a focal liver lesion (FLL), such as a cyst, hemangioma, hepatic adenoma or focal nodular hyperplasia. In a cohort of LDLT donors assessed with CT, 25% were shown to have a FLL (76), while a similar study with MR showed 29% with FLL (77), however all were benign. Depending on location and size, diffuse or focal processes can exclude a potential donor from consideration.
In LDLT scenarios, liver volumes are calculated to ensure that sufficient liver will be available to both the donor and graft to the recipient to prevent donor liver failure and SFSS in the recipient respectively. Both MRI and MDCT can both be used to calculate volumes as long as there is sufficient tissue contrast and minimal movement artifact (34), with both producing safe estimates (37,78,79). Precise delineation of the transection planes is particularly important in the setting of right liver lobe donation given the absence of clear anatomical landmarks (80).
Assessment of hepatic vascular anatomy in the donor is very important for optimal donor performance after hepatectomy and successful liver transplantation in the recipient. Only 35% of the population has been shown to possess conventional HA, HV and PV anatomy, with variant HA and HV each found in 40% of the population, and variant PV anatomy found in 20% (81). Therefore, knowledge and awareness of variant hepatic vasculature is critical in liver donor evaluation and surgical planning.
Hepatic arterial anatomy
Conventional hepatic arterial anatomy (HAA) is defined as a common hepatic artery arising from the celiac axis supplying the whole liver through right and left hepatic arteries, resulting from normal hepatic embryological development (Figure 4) (82). This normal anatomical configuration has been reported in as low as 55% of the population (83,84). The Michels Classification describes ten anatomic variant categories (Figure 5), but only a subset of these are surgically relevant for donor LT evaluation and are outlined in Table 4 (81,85,86). Accessory HAs are variant arteries present in addition to the conventional HAA while replaced HAs are present in place of the conventional HAA (Figures 6,7). An important variation not covered by the Michels Classification is the origin of the segment IV HA or middle hepatic artery (MHA), a relevant finding for both right and left donor hepatectomy donor candidates (87). These anatomical variants are most relevant in living donors where arterial supply to both the graft and the remnant liver has to be fully maintained. They also are important in deceased donors, to determine the possibility of splitting the liver into two grafts if that was intended, and, in the case of a full liver graft, to determine the arterial reconstruction required to maintain arterial supply. This reconstruction is often performed ex-vivo prior to implanting the graft.
Portal venous anatomy
Conventional PV anatomy (PVA) has been reported in 65–80% of the population, but up to a fifth of donor candidates have been excluded from consideration due to PVA variants (84,88,89) (Figure 8). Conventional PVA describes the main portal vein (MPV) formed by the confluence of the splenic vein (SV) and superior mesenteric vein (SMV) before it branches into the right portal vein (RPV) and left portal vein (LPV) at the hilum. The RPV then divides into anterior RPV (ARPV) which supplies segments V and VIII, and the posterior RPV (PRPV) which supplies segments VI and VII. The LPV supplies segments II, III and IV, and branches from both the RPV and LPV supply segment I (90). PV anatomical variants of surgical relevance are detailed in Table 5 (Figures 9,10) (85). Additional surgical considerations are the angle of the MPV bifurcation, with too small an angle allowing for possible compromised portal vein supply in the recipient of whole livers as the donor liver hypertrophies and encases both the RPV and LPV, as well as the length of the MPV and its diameter at the anticipated site of anastomosis, both of which also influence surgical technique (91).
Hepatic venous anatomy
Normal HV anatomy is seen in up to 70% of the population and describes three hepatic veins; the right hepatic vein (RHV) draining segments V, VI, VII and VIII, the MHV draining segments IV, V and VIII, and the left hepatic vein (LHV) draining segments II and III, with segment I draining directly into the inferior vena cava (IVC) (Figure 11) (84,93). Approximately 60% of patients demonstrate common drainage of the LHV and MHV into the IVC. Surgically relevant HV anatomical variants are detailed in Table 6 (92). Pre-operative identification of accessory HVs in the donor is important to minimize excessive bleeding during the transplant hepatectomy, while accurate estimation of their distance from the HV/IVC confluence permits accurate surgical planning as a distance greater than 4 cm often precludes a single anastomosis with the conventional donor HV to the recipient IVC (Figures 12,13) (94). Accessory HVs smaller than 0.3 cm in diameter can be ligated with minimal risk of graft congestion (85). The most common accessory HV, an accessory inferior RHV draining predominantly segments VI and VII directly into the IVC, can be present in up to 47% of donors, while variant segment VIII drainage via a separate accessory vein is seen in 9% (81,87).
Location and orientation of the HV anatomy is critically important, as the transection plane for a right hepatectomy in LDLT is usually positioned 1.0 cm to the right of the MHV. Pre-operative knowledge of accessory hepatic veins within the donor graft are essential as failure to identify and anastomose these vessels to the recipient structures can potentially lead to hepatic parenchymal congestion, graft failure and/or parenchymal atrophy (81,85).
Conventional biliary anatomy is seen in approximately 60–70% of the population (Figures 14,15) (95-99). This describes a right hepatic duct (RHD), comprised of an anterior right hepatic duct (ARHD) draining segments V and VIII and a posterior right hepatic duct (PRHD) draining segments VI and VII, joining with a left hepatic duct (LHD) which drains segments II, III and IV to form a common hepatic duct (CHD). Segment I drains into the more central segments of the LHD or RHD. The cystic duct then joins with the CHD to form the common bile duct (CBD). Biliary duct complications occur in 10–25% of recipients and up to 1.8% of donors (85,100). The risk of biliary complications is increased with the number of anastomoses, HA thrombosis and small hepatic duct caliber (101,102). Bile duct strictures are the most common recipient complication in LT, causing around 40% of all biliary complications, and are seen in up to 5% of deceased donor LT and between 7.4–60% of LDLT depending on the type of donor hepatectomy performed (103). Normal anatomy allows for an uncomplicated single duct-to-duct anastomosis but appropriate pre-operative donor evaluation and tailored surgical techniques allow for the risk of biliary complications to be minimized (104). The relevant biliary anatomy variants are described in Table 7.
Often overlooked in the overall liver donor evaluation process is the importance of effective, accurate, reproducible and succinct communication of the radiologist’s findings to the transplant surgeon and hepatologist. To facilitate this process, the use of structured reporting can be of benefit, providing for effective communication and referring physician satisfaction (105,106). This also helps to ensure that all relevant information is included in reports, reduces the risk for oversights or errors and ensures that critical findings are conveyed to the referrer (107-109).
Achieving normoglycemia in insulin-dependent diabetic patients is the primary indication for pancreas transplant (PT), first performed in 1966, with the secondary benefit of limiting the sequelae of uncontrolled diabetes, such as diabetic nephropathy and retinopathy (110-112). While not performed as frequently as LTs, PTs are increasingly performed with 213 performed in the United States in 2017 compared to 78 in 1988, all of which were from deceased donors (7). 75% of PTs are performed simultaneously with kidney transplants, known as simultaneous pancreas-kidney (SPK) transplants, with pancreas after kidney (PAK) transplants and pancreas transplants alone (PTA) making up the remainder with 18% and 7% respectively (113). Given the lack of living donors, imaging plays no formal role in pre-transplant donor evaluation, with intra-operative appraisal by the transplant surgeon the most important assessment (114). However in limited situations, prior imaging of a deceased donor may be available for review and knowledge of the surgical techniques used and salient vascular anatomy may be beneficial if the radiologist’s opinion is sought (Figure 16). The graft can also be assessed for fibrosis, fatty infiltration and calcification.
The donor pancreas is procured with the adjacent duodenal stump including the ampulla of Vater and local vasculature, as well as the donor common, internal and external iliac arteries in continuity, to allow the creation of an arterial Y graft (115). The Y graft is used to anastomose the donor superior mesenteric artery (SMA) to the donor external iliac artery to supply the pancreatic head, and the internal iliac artery to the splenic artery to supply the pancreatic body and tail. The donor common iliac artery is then anastomosed to a recipient common or external iliac artery to facilitate arterial blood supply to the graft. The donor portal vein is also resected intact to facilitate superior mesenteric and splenic vein drainage, and this is anastomosed to the recipient superior mesenteric vein (SMV) or an iliac vein in portal or systemic venous techniques respectively (116-118).
The two most prevalent surgical techniques in use currently include systemic venous-enteric exocrine drainage (Figure 17A), where the donor portal vein and recipient common or external iliac vein are anastomosed for systemic venous drainage while the donor duodenum is anastomosed to a recipient jejunal loop to allow for exocrine drainage and portal venous-enteric drainage (Figure 17B) where the donor portal vein is anastomosed to the recipient SMV. Rarely used is the bladder drainage of the donor duodenum (Figure 17C), given the complications associated with fluid and bicarbonate loss in the urine and cystitis secondary to the pancreatic enzymes effect in the bladder (116-119).
As a result, it may be of some benefit to the radiologist’s surgical colleagues if it is possible to establish the patency of the relevant arterial and venous structures on prior imaging, as well as the infrequent presence of relevant SMA variant anatomy, such as a common origin of the celiac trunk and SMA (120).
Imaging plays a critical role in the evaluation of liver donors prior to transplantation allowing for assessment of hepatic parenchymal, biliary and vascular anatomy. Adequate knowledge and understanding of these anatomic considerations is required for radiologists to provide precise information to the surgeons for preoperative planning to enable successful transplantation.
Conflicts of Interest: The authors have no conflicts of interest to declare.
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