Characterization of the Middle Hepatic Artery and Its Relevance to Living Donor Liver Transplantation

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1 LIVER TRANSPLANTATION 16: , 2010 ORIGINAL ARTICLE Characterization of the Middle Hepatic Artery and Its Relevance to Living Donor Liver Transplantation Shaofa Wang, 1,3 Xiaoshun He, 1 * Ziping Li, 2 * Zhenpeng Peng, 2 Nga Lei Tam, 1 Canhui Sun, 2 Anbin Hu, 1 and Jiefu Huang 1 1 Organ Transplantation Center and 2 Department of Radiology, First Affiliated Hospital, Sun Yat-Sen University, Guangzhou, China; and 3 Department of General Surgery, Shenzhen Hospital, Peking University, Shenzhen, China In comparison with the left and right hepatic arteries, there is a relative lack of information on the middle hepatic artery (MHA). In this study, data obtained by multidetector computed tomography from 145 patients were studied to evaluate anatomical variations of the MHA, a hilar artery that primarily supplies hepatic segment 4. An MHA was present in 103 (71%) of the subjects. In livers that had a replaced left hepatic artery, the MHA originated from the right hepatic artery; in livers that had a replaced right hepatic artery, it originated from the left hepatic artery. It always arose directly or indirectly from the common hepatic artery, from which the gastroduodenal artery also arose. We classified MHAs into 5 types according to the anatomical variations of the origin. This classification may have major relevance to modern surgical practice related to living donor liver transplantation (LDLT). The new classification of hepatic arterial anatomy may enhance the acquisition of further knowledge on arterial development, and its application may favorably influence the outcome of LDLT. Liver Transpl 16: , VC 2010 AASLD. Received November 11, 2009; accepted March 15, In living donor liver transplantation (LDLT), injuries to the middle hepatic artery (MHA), which supplies blood primarily to hepatic segment 4, may lead to a reduction in the functional volume of the left hepatic lobe and a decrease in the blood supply to bile ducts of this lobe. Complications of such arterial injuries, which may be severe, include insufficient hepatic volume, ischemic cholangiopathy, and hepatic artery thrombosis (HAT) in the right lobe donor or the left lobe recipient. 1,2 In 2 recent anatomic studies, the arterial supply to hepatic segment 4 was investigated. The origin of the MHA, always present, was classified into many subtypes that illustrated the anatomical diversity of this artery. 3,4 However, the proposed classifications appeared to be too complicated for application to surgical practice, and the concept of the MHA outlined in these studies was replaced by that of a constant artery to hepatic segment 4. In other studies, the MHA, without a clear definition, has been reported to be present in 15% to 47% of subjects. 5-7 In this study, we initially defined the MHA as a hilar artery, as it is in the embryo, 8 that supplies blood to hepatic segment 4. The hepatic hilum is a region of major interest in hepatic surgery. However, the artery to hepatic segment 4, like those to hepatic segments 2 and 3, primarily passes through hepatic parenchyma and, consequently, is an intrahepatic vessel that has no relevance to dissection of the hepatic hilum. Abbreviations: CHA, common hepatic artery; CT, computed tomography; GDA, gastroduodenal artery; HAT, hepatic artery thrombosis; LDLT, living donor liver transplantation; LGA, left gastric artery; LHA, left hepatic artery; MDCT, multidetector computed tomography; MHA, middle hepatic artery; PHA, proper hepatic artery; RAHA, right anterior hepatic artery; rcha, replaced common hepatic artery; RHA, right hepatic artery; rlha, replaced left hepatic artery; rrha, replaced right hepatic artery; SA, splenic artery; SMA, superior mesenteric artery. This work was supported by the China Medical Board of New York, Inc. (no ). *These authors contributed equally to this work. Address reprint requests to Xiaoshun He, M.D., Ph.D., Organ Transplantation Center, First Affiliated Hospital, Sun Yat-Sen University, 58 Zhongshan Er Lu, Guangzhou , China. Telephone: þ ; FAX: þ ; drsunyatsen@163.com or Ziping Li, M.D., Department of Radiology, First Affiliated Hospital, Sun Yat-Sen University, 58 Zhongshan Er Lu, Guangzhou , China. Telephone: þ ; FAX: þ ; drlizhiping@163.com DOI /lt Published online in Wiley InterScience ( VC 2010 American Association for the Study of Liver Diseases.

2 CHARACTERIZATION OF THE MIDDLE HEPATIC ARTERY 737 It is difficult to expose the course of the slender MHA and the segmental Glisson system during cadaveric dissection. Furthermore, it is also difficult to determine the margins of Couinaud s segments by conventional angiography. However, technologically advanced multidetector computed tomography (MDCT) permits rapid, high-resolution imaging of the liver and vasculature. Accordingly, this technique would appear to have appreciable potential for evaluating the relationship between the hepatic artery and individual hepatic segments. 9 The purpose of this study was to apply MDCT to characterize the MHA and hence to provide new information of potential relevance to surgical practice. PATIENTS AND METHODS Subjects The protocol of this study was approved by the medical review board of our institution. One hundred forty-five consecutive patients who underwent a standard triphasic scan of the liver between June 2008 and May 2009 were included in this retrospective study: 32 patients were candidates to be living liver donors, 77 were being followed up after treatment for a colorectal tumor, and 36 were being investigated for right-sided upper abdominal discomfort. The inclusion criterion was a computed tomography (CT) scan that showed appreciable vascular contrast in the second branch of the hepatic artery, especially in the artery to hepatic segment 4, which is used in reconstruction of the MHA. The study cohort consisted of 92 men and 53 women; their age range was 19 to 65 years (median ¼ 42 years). Protocol for CT and Processing of Images Images were generated with a 64-slice spiral CT scanner (Aquilion, Toshiba, Tokyo, Japan). A standard CT protocol with only minor modifications was adopted. 10 Postprocessing was undertaken retrospectively at a commercially available workstation (Vitrea 2, Vital Images, Minnetonka, MN). Details of the techniques applied have been described elsewhere. 10 Interpretation of Images The interpretation of all images was undertaken jointly by an attending radiologist and a transplant surgeon using a picture and archiving communication systems monitor. As the course of the umbilical part of the portal vein is within the umbilical fissure, the boundary between the horizontal part and umbilical part of the portal vein was designated as the border between the hilar plate and the umbilical fissure. 11 Discrepancies in the interpretation of images were reviewed by a third observer and were subsequently resolved by consensus. Sectional and reconstructed images were reviewed to characterize visceral arteries, including the celiac artery, hepatic artery, splenic artery (SA), gastroduodenal artery (GDA), left gastric artery (LGA), and superior mesenteric artery (SMA). Special attention was paid to the origin of a replaced or accessory left hepatic artery (LHA)/right hepatic artery (RHA) and the MHA. According to Michels, 12 a replaced hepatic artery acts as a substitute for an absent normal hepatic artery and supplies a hepatic lobe, whereas an accessory hepatic artery and an existing normal hepatic artery provide the blood supply to different parts of a hepatic lobe. In our experience, the meticulous evaluation of transverse slices in an interactive cine mode enables greater accuracy in assessing a liver segment, segmental artery, and MHA than 3-dimensional reconstructed images. The obtained results were regarded as original recordings after confirmation by a second reading of each image. RESULTS Anatomy of the MHA The MHA arose from its artery of origin at the hepatic hilum; it passed outside the liver to the right of the umbilical part of the left portal vein, and it then gave off branches, notably to hepatic segment 4. One hundred three of the patients (71%) had an MHA; at the umbilical fissure, it gave off a branch or branches to hepatic segment 4 in all 103 cases, to hepatic segment 3 in 7 cases, and to hepatic segment 2 in another 2 cases. In the remaining 42 patients (29%) who had no MHA, the artery to hepatic segment 4 originated from the LHA inside the umbilical fissure. The anatomical origins of the MHA in the group of 103 cases are shown in Fig. 1. There was no instance of an MHA originating from an accessory hepatic artery. There were only 5 cases in which the MHA arose from a replaced hepatic artery, and all the replaced hepatic arteries arose from the replaced common hepatic artery (rcha; Fig. 1C,E). Interestingly, in 13 cases in which the LHA was replaced by the LGA, each MHA originated from the RHA (Fig. 1D,E). In 11 cases in which the RHA was replaced by the SMA or celiac axis, each MHA originated from the LHA (Fig. 1F,G). In 3 extraordinary cases in which the LHA was replaced by the LGA and the RHA was replaced by the SMA, the MHA arose directly from the common hepatic artery (CHA; Fig. 1H). In this series, each MHA arose directly or indirectly from the CHA (normal or replaced; Fig. 1), from which the GDA also arose. Classification of the Anatomy of the MHA and Locations of Its Divisions For the sake of simplicity, the variant origin of the CHA (n ¼ 5; Fig. 1C,E) was regarded as normal because it did not influence the spatial relationship between the MHA and the LHA or RHA in LDLT. Variations in the origin of the MHA were classified into 5 types according to their anatomic features. Figure 2 shows the locations of divisions of arteries in procured left and right lobe allografts in patients with

3 738 WANG ET AL. Figure 1. Schematic representation of the anatomical origin of the MHA in 103 subjects. Figure 2. Scheme showing MHAs: (A) type I, (B) type II, (C) type III, and (D) type IV. The locations of the divisions of arteries in left and right lobe allograft procurements are indicated with small and large arrows, respectively. MHAs of types I to IV. Patients with a type V MHA should be assessed on a case-by-case basis. Type I MHAs accounted for 43.7% (n ¼ 45; Fig. 1A) of all cases with an MHA (n ¼ 103; Fig. 1) that originated from an RHA in patients with a normal hepatic arterial configuration (Fig. 2A). Type II MHAs accounted for 26.2% (n ¼ 27; Fig. 1B,C) of cases with an MHA that originated from an LHA in patients with a normal hepatic arterial configuration (Fig. 2B). Type III MHAs accounted for 12.6% (n ¼ 13; Fig. 1D,E) of cases with an MHA that originated from an RHA in the presence of a replaced left hepatic artery (rlha; Fig. 2C). Type IV MHAs accounted for 10.7% (n ¼ 11; Fig. 1F,G) of cases with an MHA that originated from an LHA in the presence of a replaced right hepatic artery (rrha; Fig. 2D). Type V MHAs accounted for 6.8% (n ¼ 7; Fig. 1H-J) of cases with an MHA that originated from a non-left and non-right hepatic injury along the axis of the CHA, which included the CHA, the proper hepatic artery (PHA), and the right anterior hepatic artery (RAHA).

4 CHARACTERIZATION OF THE MIDDLE HEPATIC ARTERY 739 Figure 3. Anatomical variations of arteries in which the GDA and CHA can be used to form a patch to facilitate arterial anastomosis. DISCUSSION The MHA is not mentioned in many textbooks of anatomy or surgery. Michels 12 characterized the MHA as an artery in the umbilical fossa that supplies hepatic segment 4; he believed that the MHA is always present. Since that publication, Michels and others have considered the MHA to be synonymous with the artery to hepatic segment 4. In this study, we first defined the MHA as a hilar artery; indeed, the embryonic MHA is a hilar vessel. 8 This artery is a significant vessel in dissections of the hepatic hilum. Arteries to hepatic segment 4 that arise from the LHA in the hepatic hilum or inside the umbilical fissure could be distinguished in the study of Yoshimura et al. 11 In several anatomic and clinical studies in which the MHA and the artery to hepatic segment 4 were considered to be the same, no typical pattern for the origin of the MHA was found; the classifications of the patterns were complex. 3,4,13,14 However, clarification of this issue was facilitated when the MHA was differentiated from the artery to hepatic segment 4. We found that the MHA always arose directly or indirectly from a normal CHA or rcha. Embryologically, the liver is supplied by 3 hepatic arteries: the embryonic LHA from the LGA, the embryonic MHA from the CHA, and the embryonic RHA from the SMA. 8 There has been a consensus that the rlha and rrha are derived from the embryonic LHA and RHA, respectively. We believe that the variations in the origin of the MHA imply that the MHA is derived from the embryonic MHA. Interestingly, we observed the typical embryonic hepatic arterial configuration in 3 adults. In those cases, the LHA arose from the LGA, the MHA arose from the CHA, and the RHA arose from the SMA. On the basis of the variations in the origin of the MHA found in this study, we classified the MHA into 5 types. Type I and II MHAs are the variations that are well known to surgeons. 1,13 Type III, IV, and V MHAs, which account for 30.1% of all cases in which an MHA is present, were summarized first; appropriate surgical strategies related to these variations have been proposed. Importantly, an rrha favors a left or right lobe allograft, regardless of whether an MHA is present, because the MHA, if present, originates from the LHA (type IV MHA); accordingly, no modification of the surgical procedure is required. This inference is consistent with the preference of surgeons to use a liver allograft that includes a replaced hepatic artery; this option is associated with some advantages in LDLT. 14,15 However, an rlha sometimes implies an unfavorable anatomic configuration in both left and right lobe LDLT because the MHA, when present, usually originates from the RHA (type III MHA); this anatomical variation necessitates a more complex surgical technique than that needed when the MHA is absent. In right lobe LDLT, preservation of the LHA and the MHA is a standard technique to ensure the blood supply to the remaining left lobe. 1,16 Likewise, an optimal procedure is reconstruction of the 2 arteries to ensure the blood supply to the left lobe allograft. Previously, reconstruction of the MHA has been associated with a high risk of fatal HAT, which may be related to the MHA usually being smaller than the LHA. Ikegami et al. 17 advocated ligation of the smaller of the LHA and MHA if pulsatile bleeding from the smaller artery is observed after anastomosis of the larger artery. This surgical strategy was associated with a reduction in the rate of HAT after liver transplantation. However, ligation of the MHA may lead to biliary complications in a left lobe allograft because the blood supply to the biliary system in the transplanted liver allograft is entirely dependent on the hepatic artery. 18 Suehiro et al. 2 reported that biliary strictures after liver transplantation occurred in 50% of recipients (5/10) who had undergone ligation of the MHA but in only 15% of recipients (4/27) who had not undergone ligation of the MHA. Furthermore, Egawa et al. 19 found that the incidence rates of biliary leaks were 7.9% and 16% in groups of patients that had undergone complete and partial arterial reconstruction, respectively. Although the liver receives a dual blood supply and has the potential to develop a rich collateral network of vessels, liver infarction after arterial complications has been found to involve hepatic segment 4 most frequently. 20 Occlusion of the MHA might be the direct cause of liver infarction. 21 Fortunately, current microsurgical techniques, which have been developed to facilitate anastomosing small arteries and reconstructing arteries with different calibers, enable the high risk of HAT to be minimized. 22,23 Accordingly, in an increasing number of transplant centers, including our center, both the LHA and the MHA are reconstructed when pulsatile backflow is observed after reconstruction of the LHA. 2,23 Even if reconstruction of the MHA is not undertaken in a left lobe allograft by some surgeons, preoperative identification and characterization of the MHA should be of considerable importance in enabling extensive dissection at the

5 740 WANG ET AL. hepatic hilum to be avoided; such dissection may predispose liver transplant patients to hepatic parenchymal ischemia and damage to bile ducts. 21,24 If we take into consideration the anatomic variations of the MHA, a surgical strategy that uses the CHA and GDA may be appropriate in some situations (Fig. 3). Because the MHA always arises directly or indirectly from the CHA, from which the GDA also arises, and a replaced hepatic artery does not arise from the CHA, the CHA and GDA can be procured with the hepatic arterial trunk of the graft and can be trimmed to form an arterial patch. In a liver with a type IV MHA, the LHA can be reshaped into a cuff with the GDA and CHA in a left lobe allograft (Fig. 3A); in a liver with a type III MHA, the RHA with the GDA and CHA can also be used in a right trisegmental split allograft (Fig. 3B). In the case of a type V MHA, in which the LHA, MHA, and RHA originate from the LGA, CHA, and SMA, respectively, the MHA together with the CHA and GDA can be procured for possible anastomosis in a left lobe allograft (Fig. 3C). Transplantation of a cadaveric liver allograft without a patch is associated with an increased incidence of HAT. 25 Full appreciation of the variations in the origin of the MHA and the surgical techniques that are currently available should facilitate the adoption of an appropriate surgical strategy and decrease the risk of HAT. Ligation of the MHA and extensive arterial dissection during LDLT predispose the transplant to ischemia of the hepatic parenchyma and the bile ducts. 1,2 The preoperative demonstration of variations in arterial anatomy and the availability of refined microvascular surgical techniques should enable the risk of these serious complications to be minimized. Although modern surgical techniques enable a surgical strategy to be selected that is appropriate for many anatomical variations of the liver, nevertheless, accurate characterization of hepatic arteries is of increasing importance, not only for liver surgeons but also for diagnostic and interventional radiologists. In summary, the MHA, a hilar vessel present in 71% of the subjects in this study, originates in the hepatic hilum and provides branches in the umbilical fissure that primarily supply hepatic segment 4. It originates from the RHA in the liver with an rlha and from the LHA in the liver with an rrha. It always arises directly or indirectly from the CHA, from which the GDA also arises. On the basis of the variability in the origin of the MHA, the anatomy of the MHA can be classified simply into 5 main types; this classification has major relevance to modern surgical practice in LDLT. Increasing characterization of hepatic arterial anatomy may promote the acquisition of further knowledge related to arterial development and should facilitate improvements for both donors and recipients in LDLT. ACKNOWLEDGMENT The authors thank Dr. Zhongwei Zhang and Dr. Xiaofeng Zhu for helpful discussions and Dr. Zhiyong Guo and Dr. Yi Ma for editing this article. REFERENCES 1. Fan ST, Lo CM, Liu CL, Wang WX, Wong J. Safety and necessity of including the middle hepatic vein in the right lobe graft in adult-to-adult live donor liver transplantation. Ann Surg 2003;238: Suehiro T, Ninomiya M, Shiotani S, Hiroshige S, Harada N, Ryosuke M, et al. Hepatic artery reconstruction and biliary stricture formation after living donor adult liver transplantation using the left lobe. Liver Transpl 2002;8: Jin GY, Yu HC, Lim HS, Moon JI, Lee JH, Chung JW, et al. Anatomical variations of the origin of the segment 4 hepatic artery and their clinical implications. 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