Partial liver transplantation

Abstract

Partial liver transplantation, including reduced-size liver transplantation, split liver transplantation, and living donor liver transplantation, has been developed with several innovative techniques because of donor shortage. Reduced-size liver transplantation is based on Couinaud’s anatomical classification, benefiting children and small adult recipients but failing to relieve the overall donor shortage. Split liver transplantation provides chances to two or even more recipients when only one liver graft is available. The splitting technique must follow stricter anatomical and physiological criteria either ex situ or in situ to ensure long-term quality. The first and most important issue involving living donor liver transplantation is donor safety. Before surgery, a series of donor evaluations—including anatomical, liver volume, and liver function evaluations—is indispensable, followed by ethnic agreement. At different recipient conditions, auxiliary liver transplantation and auxiliary partial orthotopic liver transplantation, which employ piggyback techniques, are good alternatives. Partial liver transplantation enriches the practice and knowledge of the transplant society.

Keywords

partial liver transplantation / reduced-size liver transplantation / split liver transplantation / living donor liver transplantation

Introduction

The number of people in the waiting list for liver transplantation is increasing worldwide because of donor shortage. Hence, innovative techniques must be developed to enlarge the organ pool. Partial liver transplantation, including reduced-size liver transplantation, split liver transplantation, and living donor liver transplantation, currently attracts more and more efforts in the liver transplant community.

Reduced-size liver transplantation

For children and small adult recipients, reduced-size liver transplantation has been developed to maximize the use of donor organs. To avoid withdrawing relatively large livers from the adult donor pool, the split liver technique has emerged [1].This technique was first described by Bismuth and Houssin in 1984 [2]. Couinaud’s anatomical classification permits the creation of partial liver allografts from either deceased or living donors. Fundamental to the application of this technique is an understanding of intrahepatic vascular and biliary anatomy. Couinaud’s classification divides the liver into eight independent segments, each of which has its own vascular inflow, outflow, and biliary drainage [3]. Theoretically, because of this division into self-contained units, each liver segment can be resected or transplanted without damaging the remaining segments. Generally, resection lines need to be parallel with hepatic veins while preserving portal veins, bile ducts, and hepatic arteries that provide vascular flow and biliary drainage through the center of the segment. Segments IV to VIII are used for adults, whereas left lateral lobes (Segments II and III) or left lobes (Segments II, III, and IV) are used for pediatric recipients.

The successful application of partial liver allografts demands detailed anatomical considerations because the procedure is predisposed to unique complications. Bleeding, bilomas, and portal vein thrombosis are complications related to the procedure itself, which are associated with an increased number of re-operation. The results of reduced-size liver transplantation are reported to be similar with those of full-size liver transplantation, and the waiting time and the mortality of child recipients in the waiting list are significantly reduced [4,5]. This is consistent with an experience in Spain where patient and graft survival rates are similar across kinds of partial liver grafts (reduced, split, and living), although there is a trend of lower graft survival rate in patients receiving whole livers [6].

Although reduced-size liver transplantation fails to relieve the overall donor shortage, it lays the groundwork for other innovative modalities, such as split liver transplantation and living donor liver transplantation.

Split liver transplantation

Split liver transplantation was first performed in 1988 by Pichlmayr et al. in Hannover and Bismuth et al. in Paris [7,8]. The technique of liver splitting allows the division of the adult donor liver, together with its vascular and biliary structures, into two or more functional grafts, which can be transplanted into two or more recipients. Usually, a graft is split into a left, or left lateral liver, and a right part. Donor livers eligible for splitting should meet certain selection criteria formulated by Ville de Goyet: donors must be less than 45 years old, hemodynamically stable, receiving low or mild inotropic support, have normal or slightly altered liver tests, with less than five days in the intensive care unit, and with normal macroscopic aspect at procurement [9].

Liver splitting is performed either ex situ or in situ. Splitting ex situ, first performed by Pichlmayr et al. in 1988 [7], means that the whole liver is procured and subsequently divided into two grafts on the back table. Splitting in situ, first proposed by Rogiers et al., means that the liver is split during organ procurement from a heart-beating donor [10]. The main advantages of the in situ technique include shorter warm ischemia time, better hemostasis, and lower rate of biliary complications [11,12]. However, this technique significantly prolongs the time of organ procurement, and it might cause hemodynamic instability during the donor procedure. So far, there is no consensus on which technique is superior because both techniques demonstrate similar patient and graft survival rates compared with whole liver grafting [13].

The outcomes of split liver transplantation differ greatly depending on several factors, such as donor liver quality, donor age, the medical urgency of the recipient, and the expertise of the surgical team. The rate of arterial complications is 0%-15%, compared with 0%-6% in whole-liver transplantation in adults and 3.2%-16.7% in whole-liver transplantation in children. The application of microsurgical techniques can optimize the results. Venous outflow obstruction is rare, especially when venoplasty technique is used. Biliary complications occur in 22% of recipients. There are two types of biliary complications: leaks from the raw surface, which are usually resolved with percutaneous drainage; and biliary anastomoses, such as stenisis, which are more troublesome. Several approaches, including percutaneous balloon dilatation, temporary stenting, and an improved anatomosis technique, can resolve these complications.

Living donor liver transplantation

Clinical attempts at living donor liver transplantation (LDLT) were initiated in 1988 and 1989 by Raia et al. [14]. In 1989, Strong et al. first transplanted successfully a left lateral segment from a mother to her 17-month-old son with biliary atresia [15]. Since then, many centers, especially in Asia, have been developing LDLT [16]. Asian centers have designed several graft types, such as left liver grafts with caudate lobe, and right liver, modified right liver, and right lateral grafts.

Donor screening

Compared with other techniques, the first issue in LDLT is ethnic in nature—the origin of the donor. Ethnic principles stem from the local culture, the local religion, and even the economy in different areas and countries. The critical issue is that all donations must be voluntary and altruistic. In China, the Regulations of Organ Transplantation has been established for years, and the relationship between donors and recipients must comply with the criteria. Living organ recipients are limited to people who are spouses, lineal blood relatives, or collateral blood relatives within three generations of the living organ donors, or those with substantive evidence of kinship between recipients and donors. Most transplant centers require that donors be between 18 and 60 years of age, and ask informed consent signed by the donors themselves and their close relatives. Considering the physiological and psychological sacrifice by the donor, a high expectation of 0% donor mortality should be achieved. Strict donor screening is helpful in reaching this goal.

The living donor is asked to complete an evaluation process, including an initial health screening survey, blood tests, viral serology, imaging studies, and medical and psychiatric assessments. In many centers, liver biopsy is a routine step. Absolute exclusion criteria consist of any underlying medical condition that can increase the risk of complications, ABO incompatibility, positive hepatitis serology, underlying liver diseases, inadequate graft size, body mass index greater than 35 kg/m², and steatosis greater than 10%. Triphasic computerized tomography (CT) is used to assess the arterial and venous anatomy of the donor, and clarify whether the middle hepatic vein should be reserved for the donor or grafted. Magnetic resonance cholangiography is used to assess biliary anatomy. The volume and the mass of the whole liver, the planned donated tissue, and the remaining liver must be measured by CT or magnetic resonance imaging. Ethical issues are first assessed by the Transplant Ethics Committee before surgery is scheduled.

The donor’s liver function is sometimes evaluated pre-operatively by indocyanine green (ICG) retention test. The retention of ICG within 15 min following an injection of 0.5 mg/kg is the most widely used clearance test. The retention depends on hepatic blood flow and functional hepatic capacity. An alternative is the monoethylglycinexylidide test. It is a quantitative liver function test depending on cytochrome p450 activity, which is related to the severity of liver diseases [17]. A value of<25 ng/ml predicts safe hepatic resection [18]. This test is useful but is less accurate than ICG.

Liver donor and recipient match

The minimum graft volume for successful LDLT is controversial. In living donors, the graft–recipient bodyweight ratio (GRWR) is desired to be at 1% or more [19,20]. However, successful results have been reported with grafts having a GRWR of less than 0.7% [21,22]. A liver remnant volume of approximately 30% of the total liver volume is sufficient for donor survival, provided that the liver parenchyma is normal without evidence of fatty infiltration or fibrosis [23]. For patients with advanced liver diseases, a graft volume greater than 40% of the recipient standard liver volume is necessary [24].

A small graft may result in malfunction or the small for size syndrome (SFS) in which the recipient fails to sustain adequate metabolic function. Insufficient hepatocyte volume is the major cause of SFS in adult-to-adult LDLT. To avoid SFS, potential donors must be denied if their estimated graft volume is less than 0.8%-1.0% of GRWR, or 30%-40% of the graft volume to the standard liver volume ratio (GV/SLV) [25-30]. No SFS syndrome has been found in several reports: 0.59% of GRWR by Kiuchi et al. [25], 25% of GV/SLV by Lo et al. [23], and 26% of GV/SLV by Nishizaki et al. [30]. Therefore, the minimum liver volume to be transplanted must be established in consideration of multiple factors. Although there is no consensus on the definition of SFS, an SFS diagnosis is generally based on persistent hyperbilirubinemia and massive ascites during the post-transplant subacute phase without evidence of any other cause [31]. On the other hand, a large graft is associated with risks of graft compression and poor perfusion (large for size syndrome), which do not happen often and can be avoided through the reduced-size technique. Therefore, the accuracy of total and segmental liver volumes is important to avoid donor–recipient volume mismatch [32].

Donation and transplantation

Usually, the left lateral segment represents 15%-20% of the total liver mass, the full left lobe 30%-35%, and the full right lobe>50%. After evaluating the quality and the volume of all lobes of the liver, surgery on the donor begins with hilar dissection. Left lobectomy is started by dissecting the left hepatic artery, followed by the left portal vein and the left hepatic vein. Afterward, the left lateral segment bile duct is transected, followed by parenchymal transection, which is generally performed using Cavitron Ultrasonic Surgical Aspirator (CUSA) and without clamping the portal vein and the hepatic artery. The left and middle hepatic veins are usually preserved with the graft, and the donor right lobe is drained through the right hepatic vein and the retrohepatic veins. Right lobectomy is performed by resection along the Cantlie line after cholecystectomy. After their removal, the grafts are immediately flushed with a cold preservation solution and prepared for implantation. In right lobe grafts, if the hepatic veins of Segments V and VIII are larger than 5 mm, venous reconstruction is required on the back table using interposition vein grafts.

The first step in transplantation is the removal of the native liver. In the left lateral segment grafts, the left hepatic vein can be attached to the common orifice of the recipient hepatic veins, or it can be anastomosed to the caval opening with triangulation of the recipient vena cava. Portal vein reconstruction is performed in an end-to-end fashion. After liver reperfusion, hepatic artery anastomosis is performed between the graft hepatic artery and the recipient right, left, or proper hepatic artery depending on the alignment and the size match. The arteries can also be reconstructed before liver reperfusion to avoid second warm ischemia; this can be beneficial to bile duct recovery. In most cases, bile duct anastomosis is performed by Roux-Y hepaticojejunostomy in children, but an end-to-end anastomosis of the bile ducts is preferred in adults. Duct-to-duct biliary reconstruction was first reported by Kiuchi et al. [33], and is now performed enthusiastically in a growing number of programs [34].

The grafts are generally implanted in a piggy-back fashion in which the native inferior vena cava (IVC) remains in situ during hepatectomy. Piggyback technique was used during the pioneering period in Colorado (US) and Cambridge (UK), and was popularized by Tzakis et al. in 1989 [35-37]. The classical piggyback technique, in which venous outflow reconstruction is performed between the suprahepatic end of the donor IVC and a common orifice created from two or three hepatic veins [37], has to be modified occasionally based on the different types of donor hepatic veins. The donor hepatic vein is anastmosed to the hepatic vein, or to a new V-shape incision on the anterior wall of the recipient IVC after closing all hepatic veins [38,39].

Auxiliary partial orthotopic liver transplantation

In auxiliary liver transplantation (ALT), the native liver remains and the graft is transplanted in a heterotopic position. However, the long-term results are disappointing and inferior to those of orthotopic liver transplantation [40,41]. In 1985, Chen et al. proposed a new ALT technique in a dog transplant model in which the left lobe is reserved, the right lobe is removed, and then the partial liver is grafted using a piggyback method [42]. In this technique, squeezing the graft is avoided due to the relatively small space for the transplanted liver in the abdomen, and thus the graft obtains both input and output physiologic flow (Fig. 1). In 1991, Gubernatis et al. introduced a similar technique for acute liver failure called auxiliary partial orthotopic liver transplantation (APOLT), in which part of the native liver is removed and a partial liver graft is implanted orthotopically [43]. In LDLT, APOLT is a good alternative in cases of metabolic liver disorders that cause life-threatening extrahepatic complications, such as Wilson’s disease, Crigler–Najjar syndrome Type 1, urea-cycle enzyme deficiencies, and Type 1 primary hyperoxaluria [44-46].

In our center, four APOLT with living donors were performed from 2008 to 2009. All the recipients suffered from Wilson’s disease. The grafts were obtained from the recipients’ parents, from whom the left or right liver lobes were harvested and then planted into the recipients orthotopically. Reserving the majority of the native liver to secure the safety of recipients, the APOLT method involves implanting a small but sufficient normal liver graft to correct the metabolic disorders of patients. After surgery, the donors exhibited no complications. One recipient lost the graft because of portal vein thrombosis within one month post-transplant, but she underwent a second liver transplant immediately and recovered fully.

Complications

The overall complication rate in donors is 37% [47]. The earliest most common serious complication is postoperative bleeding, which occurs on postoperative day one. The source of bleeding is sometimes a small artery in the hilar plate that requires operation. Other early complications are bile leak (3%), subphrenic or pleural collections requiring drainage (3%), and pulmonary embolus (1%). Bile leaks can be treated with endoscopic retrograde cholangiopancreatography, stent placement, papillotomy, or percutaneous drain. The temporary percutaneous drainage of subphrenic or pleural effusion is required. Late complications include incisional hernia, pneumonia, late pulmonary embolism, and partial bowel obstruction.

In recipients, biliary reconstruction remains a significant source of morbidity, with a complication rate of 6%-47%. Complications include anastomotic leakage and stenosis, problems related with T or stent tubes, and rarely, nonanastomotic strictures or intrahepatic bilomas. These complications may lead to cholangitis, sepsis, and eventual retransplantation or even death. However, most of these complications have been resolved with non-surgical management [48-50]. Duct-to-duct reconstruction allows easy endoscopic access to the biliary tree for diagnostic and therapeutic instrumentation and management. The endoscopic approach appears to be a therapeutic alternative to re-operation. Hepatic artery thrombosis is also more common with a rate of 1%-7% [51-53]. SFS is an important phenomenon with an unknown frequency and clinical course in LDLT; its mechanism needs further investigation.

Survival rate of donors and recipients

The risk of death for donors of left lateral segments or left lobes is estimated at ~0.1%, whereas the risk for donors of right lobes is estimated at ~0.4%-0.5% [54]. To justify the risk to donors, the outcome of LDLT should at least be equal to the outcome of deceased donor liver transplant. The most important advantage of a living donation is that it optimizes the timing of transplantation. Preservation time should be minimal to decrease liver damage significantly. However, there is no strong evidence of a significant advantage in post-transplant survival rate with living donations. LDLT graft survival rate is reported at 87% and 81% at 90 days and 1 year, respectively [48]. A number of LDLT disadvantages must be considered carefully; LDLT is technically more complex than whole-organ deceased transplantation. The incidence of biliary complications increases from 30%-40% with partial grafts. Furthermore, SFS is essentially seen only in patients with partial grafts when they do not receive enough functional liver mass. Center experience also influences the final effect; an experience of>20 cases increases the survival rate [48,55].

Regeneration of grafts and remnant donor livers

The hepatic regeneration of grafts in recipients and remnant donor livers is central to the success of LDLT. The graft and the remnant donor liver both need regeneration to adequate volumes. Blood dynamics and other factors influence this process. At the cellular level, regeneration begins immediately. In theory, the majority of the process is completed within the first or second week, and the process of remodeling likely continues up to one year [56-58]. In one of our APOLT cases, the graft volume increased gradually for three months post-transplant, and remained stable afterward. Meanwhile, the remnant native liver experienced atrophy. At 18 months post-transplant, the mass of the graft increased to 181% of the original volume. By the end of a two-year follow-up, the volume of the donor’s liver increased compared with the volume after donation, but was moderately smaller than the original. To date, the regeneration of the graft and the remnant donor liver remains an important area for further detailed investigation.

Conclusion

Partial liver transplantation, especially split liver transplantation and LDLT, is an increasingly common approach to liver transplantation, accounting for approximately 5% of all liver transplantations nowadays. Modern diagnostic tools, improved techniques, more efforts, and cumulative experience will hopefully lead to better outcomes for patients.

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