Anatomical variations of the origin of the segment 4 hepatic artery and their clinical implications
2008; Lippincott Williams & Wilkins; Volume: 14; Issue: 8 Linguagem: Inglês
10.1002/lt.21494
ISSN1527-6473
AutoresGuang Jin, Hee Chul Yu, Hyung-Sun Lim, Jang Moon, Jeong Hun Lee, Jin Wook Chung, Baik Hwan Cho,
Tópico(s)Congenital Anomalies and Fetal Surgery
ResumoLiver TransplantationVolume 14, Issue 8 p. 1180-1184 Original ArticlesFree Access Anatomical variations of the origin of the segment 4 hepatic artery and their clinical implications Guang Yu Jin, Guang Yu Jin Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of Korea Department of Radiology, Yanbian University Hospital, Medical College, Yanbian University, Yanji, ChinaSearch for more papers by this authorHee Chul Yu, Hee Chul Yu Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of KoreaSearch for more papers by this authorHyung-Sun Lim, Hyung-Sun Lim Department of Anesthesiology and Pain Medicine, Chonbuk National University Medical School, Jeonju, Republic of KoreaSearch for more papers by this authorJang Il Moon, Jang Il Moon Department of Surgery, Division of Transplantation, University of Miami School of Medicine, Miami, FLSearch for more papers by this authorJeong Hun Lee, Jeong Hun Lee Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of KoreaSearch for more papers by this authorJin Wook Chung, Jin Wook Chung Department of Radiology, Seoul National University College of Medicine, Seoul, Republic of Korea Institute of Radiation Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea Clinical Research Institute, Seoul National University Hospital, Seoul, Republic of KoreaSearch for more papers by this authorBaik Hwan Cho, Corresponding Author Baik Hwan Cho chobh@chonbuk.ac.kr Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of Korea Telephone: 82-63-250-1570; FAX: 82-63-271-6197Department of Surgery, Chonbuk National University Hospital, 634-18, Keumam-dong, Dukjin-gu, Jeonju, Jeonbuk, 561-712, Republic of KoreaSearch for more papers by this author Guang Yu Jin, Guang Yu Jin Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of Korea Department of Radiology, Yanbian University Hospital, Medical College, Yanbian University, Yanji, ChinaSearch for more papers by this authorHee Chul Yu, Hee Chul Yu Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of KoreaSearch for more papers by this authorHyung-Sun Lim, Hyung-Sun Lim Department of Anesthesiology and Pain Medicine, Chonbuk National University Medical School, Jeonju, Republic of KoreaSearch for more papers by this authorJang Il Moon, Jang Il Moon Department of Surgery, Division of Transplantation, University of Miami School of Medicine, Miami, FLSearch for more papers by this authorJeong Hun Lee, Jeong Hun Lee Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of KoreaSearch for more papers by this authorJin Wook Chung, Jin Wook Chung Department of Radiology, Seoul National University College of Medicine, Seoul, Republic of Korea Institute of Radiation Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea Clinical Research Institute, Seoul National University Hospital, Seoul, Republic of KoreaSearch for more papers by this authorBaik Hwan Cho, Corresponding Author Baik Hwan Cho chobh@chonbuk.ac.kr Department of Surgery and Research Institute of Clinical Medicine, Chonbuk National University Medical School, Jeonju, Republic of Korea Jeonbuk Cancer Center, Chonbuk National University Hospital, Jeonju, Republic of Korea Telephone: 82-63-250-1570; FAX: 82-63-271-6197Department of Surgery, Chonbuk National University Hospital, 634-18, Keumam-dong, Dukjin-gu, Jeonju, Jeonbuk, 561-712, Republic of KoreaSearch for more papers by this author First published: 30 July 2008 https://doi.org/10.1002/lt.21494Citations: 44 AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract The threat of ischemic complications following massive resection, especially in living donor hepatectomy or split liver transplantation, has been haunting surgeons for many years. Postmortem dissections of 62 livers were performed to investigate anatomical variations of the principal artery for segment 4 (A4). The origin of A4 was examined separately in the liver with (n = 46) or without (n = 16) an aberrant left hepatic artery (abLHA). A4s were found to be extrahepatic or intrahepatic branches of the right hepatic artery (RHA), left hepatic artery, or proper hepatic artery and were categorized into 4 different types according to their origins. The RHA type, originating from the RHA or right anterior hepatic artery (RAHA), was the most common pattern in our series. The A4 roots had a strong tendency of stemming from the RHA (n = 12) even in the livers with abLHA (n = 16). Among the RHA-type A4s, the A4 arising from RAHA (n = 2) is supposed to be the most dangerous variant because it can cause an ischemic change in the remaining part of the liver after right hepatectomy. In conclusion, in the era of living donor liver transplantation, paying particular attention to the point of origin of A4 is a prerequisite, especially when the lateral section is relatively small. Arterial injuries to A4 during split liver transplantation may also increase the risk of hepatic artery thrombosis and ischemic cholangiopathy. Liver Transpl 14:1180–1184, 2008. © 2008 AASLD. The artery to segment 4 has been an area of debate in segmental liver anatomy. Unlike the other segments, segment 4 has a peculiar pattern of arterial supply (earlier branching for segment 4) in comparison with the portal vein supply. Embryologically, there are 3 lobes in the early stage of hepatic formation, each supplied by an embryonic artery of its own: the lateral sector (segment 2) by the embryonic left hepatic artery, the medial and anterior sectors (segments 3, 4, 5, and 8) by the embryonic middle hepatic artery, and the posterior sector (segments 6 and 7) by the embryonic right hepatic artery1 (Fig. 1). In the adult liver, segment 4 is a part of the medial sector, and it has been called by various other names such as medial segment, left medial segment, and quadrate lobe. Likewise, the artery for segment 4 has many names, such as middle hepatic artery,2-5 medial segment artery,6 left medial artery,7 and segment 4 artery (A4).8 This inconsistency in nomenclature, stemming from various origins, leads only to more confusion. Michels2 defined this artery as a middle hepatic artery that courses in the umbilical fossa to supply the quadrate lobe and thought that the branches originate in equal proportions from the right hepatic artery (RHA) or left hepatic artery (LHA). Most of the anatomical studies have used the term middle hepatic artery synonymously for A4 and suggested that this artery frequently originates from the LHA (54%-61.5%).3-5, 7 However, a multidetector computed tomography study of candidates for living donor liver transplantation (LDLT) indicated that 62.5% of the arterial supply to segment 4 originated from the RHA.9 This inconsistent observation triggered this study designed to demonstrate the branching pattern of A4 and its anatomical relation to the left portal vein (LPV) in adult livers. Figure 1Open in figure viewerPowerPoint A schematic presentation of 3 embryonic hepatic arteries and their branches representing the number of supplying subsegments of Couinaud. Abbreviations: eRHA, embryonic right hepatic artery; eLHA, embryonic left hepatic artery; eMHA, embryonic middle hepatic artery; CA, celiac axis; CHA, common hepatic artery; SMA, superior mesenteric artery; LGA, left gastric artery; PV, portal vein. (Redrawn from Couinaud C. Surgical Anatomy of the Liver Revisited. Paris, Couinaud, 1989.) We believe that recognition of the origin of A4 is important for donor evaluation for LDLT and split liver transplantation. When the middle hepatic vein (MHV) trunk is included in the graft, as in an extended right lobe graft, the congestion of a part of segment 4 is inevitable if dominant venous drainage of segment 4 is through the MHV.10, 11 If the ischemic injury is added to an already congested part of the segment, it may threaten the donor's safety. Because the number of split liver transplantations and LDLTs using the left liver has recently been increasing, preoperative A4 evaluation is becoming more important for the safety of not only the donors but also the recipients. The aim of this study was to characterize A4 in detail and classify the variations through the anatomical study of cadaver livers. Abbreviations A2, segment 2 artery; A3, segment 3 artery; A4, segment 4 artery; A4*, dangerous type of segment 4 artery variation; abLHA, aberrant left hepatic artery; CA, celiac axis; CHA, common hepatic artery; eRHA, embryonic right hepatic artery; eLHA, embryonic left hepatic artery; eMHA, embryonic middle hepatic artery; LDLT, living donor liver transplantation; LGA, left gastric artery; LHA, left hepatic artery; LPV, left portal vein; MHV, middle hepatic vein; PHA, proper hepatic artery; RHA, right hepatic artery; RAHA, right anterior hepatic artery; PV, portal vein; SMA, superior mesenteric artery. MATERIALS AND METHODS The livers used in this study were recovered from bodies donated to the Chonbuk National University Medical School for education and research. Each donation was reviewed by a medical ethics committee, and the study was approved by an internal review board. A total of 62 adult livers without macroscopic abnormalities were examined. The livers were fixed in a 10% formalin solution. Anatomical variations of the hepatic artery, especially A4, were so numerous that it was not easy to categorize all the variants into a simple format. Therefore, in this study, we decided to divide the specimens on the basis of the presence of an aberrant left hepatic artery (abLHA) and examine them separately. We defined the RHA as a part or extension of the proper hepatic artery (PHA) located distal to the origin of the dominant or first LHA.2-5 Dissection of the hepatic artery was started from the lower part of the hepatic hilum. First, the origin of A4 was exposed; then, the branch of the artery was kept in position, and the point of its origin and its distribution were identified. We identified the origin of each A4 and its supplying territory schematically. In addition, we investigated spatial relationships between A4 and the LPV in the hilar plate. RESULTS On the basis of the dissection study, we depicted the variations of the hilar artery that were supplying the left liver with special reference to A4. Out of 62 specimens, there were 42 livers without abLHA and 16 livers with abLHA. Origin of A4 in the Liver With and Without abLHA A4 was characterized as extrahepatic or intrahepatic branches of the RHA, LHA, or PHA. There was no stereotypical pattern that we could apply in mapping the root of A4. Instead, it appeared to be wandering along the Y-shaped framework formed by the RHA, PHA, and LHA. On the basis of this wandering pattern, we categorized A4s into 4 different types according to their points of origin: RHA, LHA, PHA, and dual type. The RHA type originated from the RHA or right anterior hepatic artery (RAHA), which was distal to the origin of the dominant or first LHA. The RHA type accounted for 33 cases (53.2%) in our series. Most of the RHA-type A4s were extrahepatic branches of proximal RHA. Twenty-nine of 33 RHA types were the first branches of the RHA. However, there were 2 specimens that had an intrahepatic RHA type arising from the RAHA. The LHA type, which originated from the LHA, was identified in 20 cases (32.3%). The LHA type had a wider spectrum of origins than the RHA type. This type of A4 was either an extrahepatic or intrahepatic branch of the proximal or distal LHA. The PHA type originated directly from the PHA forming trifurcation; this type was found in 3 cases (4.8%). The dual type, which was defined as 2 principal arteries stemming from 2 different origins, was identified in 6 cases (9.7%; Table 1). The incidence of abLHA, a branch of the left gastric artery, was 25.8% (16/62) in our series. In the livers with abLHA, most A4s (12/16) also came from the RHA rather than from the abLHA. The total number of A4s that originated from the abLHA was 5. Table 1. Four Different Types of A4 in the Livers Abbreviations: A2, segment 2 artery; A3, segment 3 artery; A4, segment 4 artery; A4*, dangerous type of segment 4 artery variation; abLHA, aberrant left hepatic artery; LHA, left hepatic artery; PHA, proper hepatic artery; RHA, right hepatic artery. Spatial Relationship Between A4 and the LPV There were 68 branches of A4 in 62 livers. Fifty-seven branches traversed the ventral surface of the LPV (83.8%) within the hilar plate, and the rest (n = 11) ran the dorsal surface of the LPV (16.2%). All of the A4s that traversed the dorsal side of the LPV were branches of the distal part of the LHA, which was located near or within the umbilical plate, and not a single branch came from the proximal part of the LHA. Also, A4s as branches of the abLHA (n = 5) were all found within the umbilical plate system, and none were found within the hilar plate. All arterial branches that presented in front of the LPV had a supplying territory in segment 4. DISCUSSION It is essential for liver surgeons to have a comprehensive understanding of not only the standard hepatic anatomy but also variant hepatic anatomy. Recognition of the anatomical variations and an understanding of hepatic embryology would help surgeons to avoid serious surgical complications when they perform difficult types of hepatic resection. The diversities of the arteriobiliary system are far more complex than the portal system. According to Couinaud's description,1 the liver is supplied by 3 principal arteries during the developmental stage of life: the left gastric artery irrigates the left lateral segment, the common hepatic artery irrigates the paramedian sectors, and the superior mesenteric artery irrigates the right lateral segment. During the early period of human fetal life, the liver is bulky, the gut is very small, and the hepatic artery is predominant. Later, the size of the liver proportionally decreases while the gut reciprocally increases; 3 hepatic arteries are anastomosed in the hilum of the liver, and some of them regress while the enteric branches expand. If the right or left embryonic artery does not totally regress, it becomes the right or left aberrant hepatic artery. Miyaki12 reported that 1 or 2 aberrant hepatic arteries were found in 30% of human fetuses (over 5 months of pregnancy). The incidence of abLHA is about 24% according to Michels' classical data.2 The arterial supply to segment 4 presents a quite versatile pattern. The diversity of the origin of A4 remains to be elucidated. Michels2 and Healey and Schroy6 reported that the arteries originated from the RHA or LHA in about equal proportions. Several other studies have suggested that the artery for the most part originates from the LHA (54%-61.5%). Suzuki3 reported that the artery was a branch of the LHA in 54% of cases, the RHA in 34% of cases, and the bifurcation of the PHA in 8% of cases and was a direct branch from the common hepatic artery in 4% of cases. Onishi et al.4 reported that the artery branched from the LHA in 61.5%, from the RHA in 27.5%, from the bifurcation of the LHA and RHA in 5.5%, and from the branches of both the LHA and RHA in 5.5% of cases. In our study, however, most A4s were a branch of the RHA or PHA, regardless of the presence of abLHA. We believe that this is strong evidence that segment 4 is a descendant of the middle embryonic lobe (paramedian sector). The RHA type appears to be more frequent than what has been reported previously.2-6 The PHA is defined as the arterial segment from the origin of the gastroduodenal artery to the bifurcation of the hepatic artery. On the basis of the nomenclature of RHA and LHA, these arteries are supposed to irrigate the corresponding hemisphere of the liver. To accommodate that nomenclature, we may have to redefine the anatomy of the PHA. We could extend the length of the PHA from the gastroduodenal artery to the point of origin of A4 in the RHA type, rather than to the bifurcation of the hepatic artery. With this definition, the PHA may give off one or more right or left hepatic arteries. According to our data, all 57 principal A4s (83.8%) that traversed the ventral side of the LPV were extrahepatic in their origin (within the hilar plate). Therefore, if a surgeon could not find an A4 in front of LPV, the artery for segment 4 should be found to be intrahepatic, or it should be a branch of abLHA. The remaining liver volume after major liver resection is critical for preserving adequate liver function. Therefore, potential congestion and ischemia of the remaining liver should be prevented to preserve maximum liver function. Today, when there is an increasing demand for LDLT, a major concern of this procedure using the right lobe is the safety of the donor. The exclusion of the MHV trunk in the right lobe graft is carefully considered to avoid congestion of segment 4 for the donor's safety.11 Drainage of segment 4 is obviously more important than drainage of the anterior segment through the MHV trunk.13 Congestion may exacerbate the already existing detrimental effects of ischemia of the same segment and vice versa. When the MHV trunk is included in the graft, such as the extended right lobe graft, congestion of a part of segment 4 is a concern if there is no adequate drainage for segment 4 through LHV. In these cases, the congested part of the segment becomes more prone to ischemic injury, as shown in Fig. 2B. Progressive necrosis of segment 4 may not be well taken and may cause hepatic dysfunction if the liver volume is not enough. We believe that careful preservation of A4 will minimize this type of hepatic volume loss and possible dysfunction. In the case of split liver transplantation using both lobes, the division of the hepatic artery should be decided on the basis of the anatomy of A4 branching to avoid an ischemic change in segment 4. If there is no identifiable A4 branch in the extrahepatic portion or at the hilum, special attention is needed to find intrahepatic A4. Although it is rare, ischemia of A4 territory is inevitable if it takes off from the distal portion of the RAHA. Figure 2Open in figure viewerPowerPoint Portal phase of abdominal computed tomography of 2 different donors. (A) Case 1 had an irregular, rather concave resection margin after the donor's right hepatectomy in comparison with (C) case 2 at 1 week after surgery. Atrophy of S4 along with the resection margin was prominent in (B) case 1 at 2 weeks after surgery in comparison with (D) case 2. In conclusion, our study has shown that the incidence of A4 originating from the LHA is less common than what it has been reported in the past. Being well versed in anatomical variations of A4 is crucial in the hemiliver graft procedure. In the process of graft splitting, close attention needs to be paid to A4, especially when it arises from the RAHA. It may be necessary to divide the distal part of the origin of A4 to preserve inflow to segment 4. Such division may create 2 separate arterial anastomoses for the right liver graft. 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