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Accessory extrahepatic arteries: Blood supply of a human liver by three arteries
ARTICLE IN PRESS Ann Anat 191 (2009) 477—484
www.elsevier.de/aanat
RESEARCH ARTICLE
Accessory extrahepatic arteries: Blood supply of a human liver by three arteries A case report with brief literature review Bao-Gui Wang, Rosemarie Fro ¨ber Department of Anatomy, Faculty of Medicine, Friedrich Schiller University of Jena, Germany Received 20 December 2008; received in revised form 26 June 2009; accepted 27 June 2009
KEYWORDS Accessory hepatic arteries; Anatomical variations; Liver surgery and transplantation
Summary The coexistence of three hepatic arteries – accessory left hepatic artery (aLHA), proper hepatic artery (pHA), and accessory right hepatic artery (aRHA) – was demonstrated during a routine dissection of an 85-year-old male cadaver. The aLHA arose from the left gastric artery and ran in the hepatogastric ligament, whereas the aRHA took its origin from the superior mesenteric artery and ran in the hepatoduodenal ligament. The anatomy of the origins and the course of the arteries in the liver are described. Knowledge of these variations is of importance for surgical and radiological procedures in the upper abdominal region, in order to avoid complications during invasive treatment. The embryological background of the variations is discussed. & 2009 Elsevier GmbH. All rights reserved.
Introduction The liver develops at an early embryonic stage and rapidly becomes one of the indispensable organs of the human foetus (Keibel and Mall, 1910; Waddington, 1940). Normally, it has a dual blood supply that stems from the proper hepatic artery (pHA) and the portal vein. It is well-known that the portal vein and the pHA deliver approximately 70% and 30%, respectively, of the blood Corresponding authors.
E-mail addresses: [email protected] (B.-G. Wang), [email protected] (R. Fro ¨ber).
supply volume flowing into the liver. The liver is the largest internal organ of the human body, accounting for approximately 2–3% of the total body weight of an adult. The most commonly described hepatic arterial supply consists of a single pHA arising from a common hepatic artery, which also gives rise to the gastroduodenal artery. The pHA runs to the left of the common bile duct within the hepatoduodenal ligament. The portal vein, lying behind the pHA and the common bile duct, forms the ventral border of the epiploic foramen (Winslow’s foramen). These three structures form the Glisson’s portal triad and continue to the porta hepatis, where the pHA divides into a right branch and a left
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branch that enter into the liver to supply its eight segments. Proximately, the common hepatic artery arises from the coeliac trunk, which is a ventral branch of the abdominal aorta and has two other branches, the left gastric artery and the splenic artery. Normally, the superior mesenteric artery has no branch to the liver (Quain, 1844; Adachi, 1928; Van Damme and Bonte, 1985; Kadir et al., 1991). However, the patterns of the hepatic arterial blood supply are highly variable (Table 1). Numerous variations of the hepatic artery have been described (do Rio-Branco, 1912; Flint, 1923; Adachi, 1928; Daly et al., 1984; Hiatt et al., 1994). The hepatic artery is aberrant in 20–50% of individuals and may receive blood supply from the superior mesenteric artery, the left gastric artery, or the aorta (Michels, 1966; Van Damme and Bonte, 1985; Nelson et al., 1988; Makisalo et al., 1993; Hiatt et al., 1994; Soin et al., 1996; De Santis et al., 2000; Koops et al., 2004). Since the earliest description of the hepatic artery variants (Haller, Table 1.
1756), statistical records of these aberrations have become available (Lipshutz, 1917; Browne, 1940; Healey and Schwartz, 1964; Rygaard et al., 1986; Kemeny et al., 1986; Rong and Sindelar, 1987; Bergman et al., 1988; Hiatt et al., 1994; Gruttadauria et al., 2001; Saeed et al., 2002; Koops et al., 2004; Abdullah et al., 2006; Pai et al., 2008). In 1917, Lipshutz reported a detailed study of dissections of 83 adult cadavers and found an accessory hepatic artery as a branch of the left gastric artery in 35% of his cases and as a branch of the superior mesenteric artery in 15%. The term ‘‘accessory’’ hepatic artery in his description is used only for an aberrant artery when it coexists with a normal hepatic branch from the coeliac artery. Michels (1966) described a classification scheme based on his results of dissections of 200 cadavers and defined the main patterns of the hepatic artery variations. Hiatt et al. (1994) reviewed records of 1000 patients who underwent liver harvesting for orthotopic transplantation and modified Michels’ basic classification scheme. In 2001, Gruttadauria
Hepatic arterial types (%).
Literature review
Variation
Replaced or Replaced or Replaced accessory LHA (%) accessory RHA (%) LHA+replaced RHA
Accessory LHA+accessory RHA
Michels, 1966, cadaver dissection Suzuki et al., 1971, arteriography Daly et al., 1984, arteriography Kemeny et al., 1986, arteriography Rygaard et al., 1986, arteriography Rong and Sindelar, 1987, arteriography Hiatt et al., 1994, liver graft Soin et al., 1996, liver graft Chen et al., 1998, arteriography De Santis et al., 2000, arteriography Gruttadauria et al., 2001, liver graft Saeed et al., 2002, cadaver dissection Koops 2004, arteriography Abdullah et al., 2006, liver graft
45% (n ¼ 200) 45% (n ¼ 200) 24% (n ¼ 200) 50% (n ¼ 100) 24.5% (n ¼ 216) 34% (n ¼ 120) 24.3% (n ¼ 1000) 30.6% (n ¼ 527) 19.7% (n ¼ 381) 48% (n ¼ 150) 42.23% (n ¼ 701) 25% (n ¼ 52) 21.9% (n ¼ 604) 31.9% (n ¼ 932)
18
18
1%
1%
18
18
0.9%
0.5%
7.5 17 4.6 11
10 20 13.4 16
9.7
10.6
14.2
8.7
9.1
6.7
0.7%
0.5%
10.6
17.5
0.6%
0.6%
11.55
14.98
0.56%
0.14%
7.6
3.8
1.9%
3.0
11.9
8.1
10.2
1.4%
‘‘Replaced’’ means that the proper hepatic artery is absent; ‘‘Accessory’’ means that the proper hepatic artery coexists.
ARTICLE IN PRESS Accessory extrahepatic arteries: Blood supply of a human liver by three arteries reported that the hepatic artery was anomalous in 296 out of 701 cases with an overall incidence of hepatic artery anomalies of 42.23%. Koops et al. (2004) carried out a retrospective study of a total of 604 coeliac and superior mesenteric angiographies. His results indicated that the prevalence of an aLHA arising from the left gastric artery was only 3.0%. Studies of 932 cases in liver transplantation including the harvested livers and operated patients showed that variations in the hepatic artery existed in 31.9% (Abdullah et al., 2006). Other studies (Daseler et al., 1947; Fontaine et al., 1970; Reuter and Redman, 1977; Chen et al., 1998; Troupis et al., 2008) reported a prevalence of approximately 10–20% for an aberrant right hepatic artery arising from the superior mesenteric artery and of 8–18% for an aberrant left hepatic artery arising from the left gastric artery. The variations in the extrahepatic arteries are of great clinical importance because the incidence of hepatic vascular injuries increases when an aberrant anatomy is present (Suzuki et al., 1971; Rela et al., 1998a; Jones and Hardy, 2001). Thus, knowledge of the anatomy and frequency of abnormalities in the extrahepatic arterial system is a prerequisite for successful liver transplantation, laparoscopic surgery, and radiological procedures in the upper abdomen, and for the treatment of penetrating injuries in the perihepatic area, both for surgeons and radiologists. Although a single anomaly in the coeliac-mesenteric arterial system is not rare, complex combinations, such as the ones observed in the present case, represent a significant deviation from the normal hepatic arterial pattern. More importantly, the origin and course of the accessory arteries can vary dramatically among individuals. Hence, knowledge of each of the variations can be of paramount importance in individual clinical cases. The present study addresses the occurrence of the accessory extrahepatic arteries with a special emphasis on the anatomical description of their origins, branching pattern, distribution, and topography.
Materials and methods An unusual case of an anomalous pattern of the hepatic artery was encountered during a routine dissection carried out at our institute. The cadaver was that of a Caucasian adult male who died of acute heart failure at the age of 85. No liver disease had been recorded in the donor who had voluntarily agreed that his body or parts of it could
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be used for education and research purposes at our institution. The pseudonymized body was embalmed in a fixative solution containing 60% ethanol and 2% formaldehyde. The donation procedure for anatomical bequests in Germany has been described in detail elsewhere (McHanwell et al., 2008; Korf et al., 2008).
Results In addition to the pHA, two other extrahepatic arteries – an accessory on the left and an accessory on the right – were observed in a human cadaver (Figures 1 and 2). On the left, a 4-cm-long aLHA arose from the left gastric artery and ran in the hepatogastric ligament, first traversing in the left direction, then immediately turning for about 3 cm upwards and finally turning slightly to the right until this artery entered into its accessory porta hepatis. The left gastric artery ran along the lesser curvature of the stomach. In the mid-epigastric region, a 6.4-cm-long pHA originated from the common hepatic artery. The common hepatic artery, stemming from the coeliac trunk, ran dorsalwards and toward the right until it reached the superior portion of the duodenum, where it divided into the pHA and the gastroduodenal artery. The pHA, continuing further along the common hepatic artery after the branching-off of the gastroduodenal artery, turned upwards to ascend in the right free margin of the lesser omentum. Along its further course, the pHA was enveloped by the hepatoduodenal ligament, in which it lay ventral to the portal vein and the aRHA and located on the left side of the other three components lying in this ligament. It finally bifurcated into two arteries, the left and right hepatic arteries, at or near the porta hepatis and supplied oxygenated blood to the left and right hepatic lobes. The pHA did not give off any branches to the gallbladder. On the right side, an 8-cm-long aRHA took origin from the superior mesenteric artery. In its further course, it runs obliquely cranialwards and to the right side, then reached the hepatoduodenal ligament, in which it was accompanied by the pHA, the bile duct, and the portal vein. The aRHA was the most hidden of the three arteries, since it was perfectly sequestered on the dorsal side of the pHA and the portal vein within the hepatoduodenal ligament. This accessory vessel arose from the right edge of the ventral surface of the superior mesenteric artery at an origin site that was located 1.8 cm distal to the origin of the superior
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Figure 2. Drawings show the three hepatic arteries and the coeliac trunk with its three branches (LGA, CHA, SA). The portal vein was omitted in Fig. A in order to provide a clear overview of the accessory hepatic arteries. The cystic artery supplying the gallbladder originated from the aRHA. Normal bile duct was located in the hepatoduodenal ligament. The portal vein, lying between the pHA and the aRHA, was pushed ventrally by the latter to take up an unusual ventral position in the gastroduodenal ligament. (1) aLHA arising from LGA; (2) pHA arising from CHA; (3) aRHA arising from SMA; (4) CBD; and (5) PV.
Figure 1. Photographs of the visceral surface of the porta hepatis showing the three hepatic arteries and their topography. (A) Overview in situ; (B) magnification of the region of interest marked in Fig. A. The portal vein was pulled aside to visualize the three branches of the coeliac trunk arising from aorta (left gastric artery [LGA], common hepatic artery [CHA], Splenic artery [SA]). The accessory left hepatic artery (aLHA), the proper hepatic artery (pHA), and the accessory right hepatic artery (aRHA) supply arterial blood for the liver. Amongst the arteries, the aRHA seemed to be the dominant one for the blood supply to the liver, as judged from the diameter of the blood vessels. (1) Accessory left hepatic artery arising from left gastric artery; (2) proper hepatic artery arising from common hepatic artery; (3) accessory right hepatic artery arising from the superior mesenteric artery (SMA); (4) portal vein (PV) comprising two drainage veins: superior mesenteric vein (SMV) and splenic vein (SV); (5) common bile duct (CBD); (6) superior mesenteric vein (SMV); (7) splenic vein (SV) after the merging of IMV; (8) inferior mesenteric vein (IMV); (9) splenic vein (SV) before the merging of IMV; (10) gastroduodenal artery (GDA); (11) splenic artery (SA); (12) superior mesenteric artery (SMA); (13) liver; (14) gallbladder; (15) cardia of stomach; (16) common hepatic artery; (17) left gastric artery; (18) coeliac trunk (CT); and (19) aorta. Scale bar for Fig. B: 2 cm.
mesenteric artery from the abdominal aorta. The aRHA supplied blood not only to the right lobe of the liver (segments IVa, V, VI, VII, VIII), but also to part of the caudatus lobe (segment I) and the quadratus lobe (segment IVb). Before entering the liver, the aRHA released the cystic artery. This artery, feeding the gallbladder, was found between the cystic duct and the common bile duct, where it is also called the hepatocystic triangle. Within the hepatoduodenal ligament, the common bile duct lay on its right edge and behind the portal vein. The portal vein, as the sole vein in the hepatoduodenal ligament, was formed in a regular manner behind the pancreas by the confluence of the superior mesenteric vein and the splenic vein. However, it was pushed ventrally by the aRHA within this ligament and therefore assumed a position in front of the aRHA and the common bile duct. As a result, the ventral border of Winslow’s foramen was formed by the aRHA instead of by the portal vein in this case. In contrast to the extrahepatic artery variations, the coeliac trunk, arising at the level of the first lumbar intervertebral disc, showed its characteristic tripod disposition: the common hepatic artery, the left gastric artery, and the splenic artery. The superior mesenteric artery was located 3.2 cm distal to the origin of the coeliac trunk from the aorta. Besides the irregular arterial branch to the liver, the superior mesenteric artery gave rise to its normal branches, including the inferior pancreaticoduodenal artery, the jejunal arteries, the ileal
ARTICLE IN PRESS Accessory extrahepatic arteries: Blood supply of a human liver by three arteries arteries, the iliocolic artery, the right colic artery, and the middle colic artery. These regular branches showed normal branching and distribution patterns. On general inspection, no pathology or malformation was evident within the upper abdomen.
Discussion In the present report, we describe an unusual case of three extrahepatic arteries in a human cadaver. This variation is the first observation among 100 human adult specimens from a 10-year retrospective screening of the dissection records at our institute. The present variation should be defined as an Adachi type of I 11 variation, which has a prevalence of 2%, or as a Michels type of VII variation (1% prevalence), or as a Hiatt type IV variation (2.3% prevalence, replaced or accessory RHA+replaced or accessory LHA) (Adachi, 1928; Michels, 1966; Hiatt et al., 1994). Recently, Koops et al. (2004) reported this combination in 1.4% based on their angiographic examinations. However, all of the previous reports were predominantly concentrated on their statistical records instead of on the anatomical details of the variations. Among the three hepatic arteries reported, the aRHA was the thickest one. Its diameter can even be compared to that of the common hepatic trunk. The aRHA was thereby believed to be the dominant blood supply to the liver in our case. In view of the arrangement of the three hepatic arteries, the porta hepatis could be considered as a portal quinta. During human embryonic development, the liver normally arises as a bud of the entoderm at the junction between the primitive fore- and midgut. In the angiogenesis of the coeliac-mesenteric arterial system, the ventral splanchnic arteries arising from the dorsal aorta are the stem vessels. Initially, the ventral splanchnic arteries generate four roots for supplying the fore- and the midgut. These four roots are connected to each other through longitudinal anastomoses at different levels. During further development, the second and third roots obliterate gradually. Only the first and the fourth root persist and are connected by a ventral longitudinal anastomosis. The common hepatic, the left gastric, and the splenic arteries usually originate from the first root, the so-called primitive coeliac axis, whereas the superior mesenteric artery normally arises from the fourth root. In contrast, data from animal embryology show that the persistence of a primitive trunk ‘‘Coeliaco-Mesen-
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terica’’, joining the first and the fourth roots, is an entirely normal condition in some lower animals such as the anura, the reptiles and also in some mammals. In other words, the coeliac trunk and the superior mesenteric artery originate from the primitive trunk in these species. Furthermore, Bremer suggested that an extrinsic factor, acting in the form of some developing sympathetic fibers, might entwine the coeliac root and the superior mesenteric groups to alter their growth and even the branches of the vessels in the chick (Bremer, 1924). In contrast, the ventral longitudinal anastomosis between these two existing roots is usually interrupted in human beings. If this separation occurs abnormally, any one of the arterial variations can emerge (Tandler, 1904; Broman, 1908; Keibel and Mall, 1910; Waddington, 1940; C-avdar et al., 1997; Zaret, 2001). A review of these previous embryological studies suggests that the partial persistence of this longitudinal anastomosis might explain the occurrence of the aRHA originating from the SMA in our study. The growing number of hepatic transplants and the use of new laparoscopic techniques are the main reason for the renewed interest in extrahepatic arterial variations (Abdullah et al., 2006; Streitparth et al., 2007). Not only for laparoscopic surgery and radiological procedures, but also for liver transplantation, an accurate diagnostic workup of the hepatic vascular anatomy is essential. Currently, the split liver transplantation, in which the donor liver is cut in half for two recipients, results in a high interest in the anatomical variations of the extrahepatic blood supply. During the transplant procedure, the extrahepatic arterial patterns of the donor liver and the recipient liver must be determined with precision. Division of or damage to a hepatic artery owing to the ignorance of the variations may induce subsequent liver ischemia (Brems et al., 1989; Soin et al., 1996; Pulakunta et al., 2008). More important, the pHA should be differentiated from an accessory hepatic artery during surgery. Any erroneous ligation could lead to necrosis of a liver segment or lobe (Grundmann et al., 1980; Todo et al., 1987; Merion et al., 1989; Brems et al., 1989; Settmacher et al., 2000; Abdullah et al., 2006; Pulakunta et al., 2008). As a result, all variations must be defined and appropriately managed to ensure a complete vascular and biliary supply of both grafts in a liver transplantation (Rela et al., 1998b; Chaib et al., 2005; Streitparth et al., 2007; Mu ¨ller et al., 2007). To make much safer surgery, Harms et al. (2005) recommends a 3D visualization system that improves anatomical assessment, allows for the determination of individual vascular territories,
ARTICLE IN PRESS 482 and acts as an intraoperative guide with enhanced precision for the assessment of the optimal surgical splitting line of the transplanted livers. In the present case, the cystic artery originated from the aRHA instead of from the pHA. Since the early 1990s, laparoscopic cholecystectomy has been accepted as the preferred method for the treatment of gallbladder stones (Hugh et al., 1992). Because only a limited surgical field is magnified on a video monitor during the minimally-invasive operation, the surgeon needs to have a thorough knowledge of variations in the cystic arterial supply. Thus, the awareness of anomalous extrahepatic arteries is also important for a successful hepatobiliary surgery. Arterial variations consisting of an accessory right hepatic artery must also be considered when a pancreatic or duodenal surgery is contemplated. Variations of the mesenteric arterial branches are also important in other surgical procedures, such as right hemi-colectomy and resection of the transverse colon. Furthermore, when a porto-caval shunt is performed, preoperative knowledge of an interposition of an aberrant right hepatic artery between the portal vein and the abdominal vena cava can be of vital importance (Woods and Traverso, 1993; Abdullah et al., 2006; Streitparth et al., 2007; Lo ´pez-Andu ´jar et al., 2007).
Acknowledgements The authors are grateful for the body donation and wish to acknowledge the contributions of the medical students and tutors (matriculation year of 2007) who participated in the cadaver dissection during their medical training at our institution. They also thank Prof. Christoph Redies for his excellent editing of this manuscript and Jens Geiling, Michael Szabo ´, and Simone Freund for their expert help with photography, drawing, and technical assistances.
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ARTICLE IN PRESS 484 Suzuki, T., Nakayasu, A., Kawabe, K., Takeda, H., Honjo, I., 1971. Surgical significance of anatomic variations of the hepatic artery. Am. J. Surg. 122, 505–512. Tandler, J., 1904. Ueber die varietaten der Arteria coeliaca und deren Entwicklung. Anat. Hefte 25, 473–500. Todo, S., Makowka, L., Tzakis, A.G., Marsh Jr., J.W., Karrer, F.M., Armany, M., Miller, C., Tallent, M.B., Esquivel, C.O., Gordon, R.D., Iwatsuki, S., Starzl, T.E., 1987. Hepatic artery in liver transplantation. Transplant. Proc. 19, 2406–2411. Troupis, T., Chatzikokolis, S., Zachariadis, M., Troupis, G., Anagnostopoulou, S., Skandalakis, P., 2008. Rare anatomic variation of left gastric artery and right
B.-G. Wang, R. Fro ¨ber hepatic artery in a female cadaver. Am. Surg. 74 (5), 430–432. Van Damme, J.P.J., Bonte, J., 1985. The branches of the celiac trunk. Acta Anat. 122, 110–114. Waddington, C.H., 1940. A manual of embryology. Nature 146 (3710), 728–729. Woods, M.S., Traverso, L.W., 1993. Sparing a replaced common hepatic artery during pancreaticoduodenectomy. Am. Surg. 59, 719–721. Zaret, K.S., 2001. Embryonic development of the liver. In: Arias, I.M. (Ed.), The Liver – Biology and Pathobiology, 4th edition. Lippincott Williams & Wilkins, Philadelphia.
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RESEARCH ARTICLE
Accessory extrahepatic arteries: Blood supply of a human liver by three arteries A case report with brief literature review Bao-Gui Wang, Rosemarie Fro ¨ber Department of Anatomy, Faculty of Medicine, Friedrich Schiller University of Jena, Germany Received 20 December 2008; received in revised form 26 June 2009; accepted 27 June 2009
KEYWORDS Accessory hepatic arteries; Anatomical variations; Liver surgery and transplantation
Summary The coexistence of three hepatic arteries – accessory left hepatic artery (aLHA), proper hepatic artery (pHA), and accessory right hepatic artery (aRHA) – was demonstrated during a routine dissection of an 85-year-old male cadaver. The aLHA arose from the left gastric artery and ran in the hepatogastric ligament, whereas the aRHA took its origin from the superior mesenteric artery and ran in the hepatoduodenal ligament. The anatomy of the origins and the course of the arteries in the liver are described. Knowledge of these variations is of importance for surgical and radiological procedures in the upper abdominal region, in order to avoid complications during invasive treatment. The embryological background of the variations is discussed. & 2009 Elsevier GmbH. All rights reserved.
Introduction The liver develops at an early embryonic stage and rapidly becomes one of the indispensable organs of the human foetus (Keibel and Mall, 1910; Waddington, 1940). Normally, it has a dual blood supply that stems from the proper hepatic artery (pHA) and the portal vein. It is well-known that the portal vein and the pHA deliver approximately 70% and 30%, respectively, of the blood Corresponding authors.
E-mail addresses: [email protected] (B.-G. Wang), [email protected] (R. Fro ¨ber).
supply volume flowing into the liver. The liver is the largest internal organ of the human body, accounting for approximately 2–3% of the total body weight of an adult. The most commonly described hepatic arterial supply consists of a single pHA arising from a common hepatic artery, which also gives rise to the gastroduodenal artery. The pHA runs to the left of the common bile duct within the hepatoduodenal ligament. The portal vein, lying behind the pHA and the common bile duct, forms the ventral border of the epiploic foramen (Winslow’s foramen). These three structures form the Glisson’s portal triad and continue to the porta hepatis, where the pHA divides into a right branch and a left
0940-9602/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2009.06.006
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branch that enter into the liver to supply its eight segments. Proximately, the common hepatic artery arises from the coeliac trunk, which is a ventral branch of the abdominal aorta and has two other branches, the left gastric artery and the splenic artery. Normally, the superior mesenteric artery has no branch to the liver (Quain, 1844; Adachi, 1928; Van Damme and Bonte, 1985; Kadir et al., 1991). However, the patterns of the hepatic arterial blood supply are highly variable (Table 1). Numerous variations of the hepatic artery have been described (do Rio-Branco, 1912; Flint, 1923; Adachi, 1928; Daly et al., 1984; Hiatt et al., 1994). The hepatic artery is aberrant in 20–50% of individuals and may receive blood supply from the superior mesenteric artery, the left gastric artery, or the aorta (Michels, 1966; Van Damme and Bonte, 1985; Nelson et al., 1988; Makisalo et al., 1993; Hiatt et al., 1994; Soin et al., 1996; De Santis et al., 2000; Koops et al., 2004). Since the earliest description of the hepatic artery variants (Haller, Table 1.
1756), statistical records of these aberrations have become available (Lipshutz, 1917; Browne, 1940; Healey and Schwartz, 1964; Rygaard et al., 1986; Kemeny et al., 1986; Rong and Sindelar, 1987; Bergman et al., 1988; Hiatt et al., 1994; Gruttadauria et al., 2001; Saeed et al., 2002; Koops et al., 2004; Abdullah et al., 2006; Pai et al., 2008). In 1917, Lipshutz reported a detailed study of dissections of 83 adult cadavers and found an accessory hepatic artery as a branch of the left gastric artery in 35% of his cases and as a branch of the superior mesenteric artery in 15%. The term ‘‘accessory’’ hepatic artery in his description is used only for an aberrant artery when it coexists with a normal hepatic branch from the coeliac artery. Michels (1966) described a classification scheme based on his results of dissections of 200 cadavers and defined the main patterns of the hepatic artery variations. Hiatt et al. (1994) reviewed records of 1000 patients who underwent liver harvesting for orthotopic transplantation and modified Michels’ basic classification scheme. In 2001, Gruttadauria
Hepatic arterial types (%).
Literature review
Variation
Replaced or Replaced or Replaced accessory LHA (%) accessory RHA (%) LHA+replaced RHA
Accessory LHA+accessory RHA
Michels, 1966, cadaver dissection Suzuki et al., 1971, arteriography Daly et al., 1984, arteriography Kemeny et al., 1986, arteriography Rygaard et al., 1986, arteriography Rong and Sindelar, 1987, arteriography Hiatt et al., 1994, liver graft Soin et al., 1996, liver graft Chen et al., 1998, arteriography De Santis et al., 2000, arteriography Gruttadauria et al., 2001, liver graft Saeed et al., 2002, cadaver dissection Koops 2004, arteriography Abdullah et al., 2006, liver graft
45% (n ¼ 200) 45% (n ¼ 200) 24% (n ¼ 200) 50% (n ¼ 100) 24.5% (n ¼ 216) 34% (n ¼ 120) 24.3% (n ¼ 1000) 30.6% (n ¼ 527) 19.7% (n ¼ 381) 48% (n ¼ 150) 42.23% (n ¼ 701) 25% (n ¼ 52) 21.9% (n ¼ 604) 31.9% (n ¼ 932)
18
18
1%
1%
18
18
0.9%
0.5%
7.5 17 4.6 11
10 20 13.4 16
9.7
10.6
14.2
8.7
9.1
6.7
0.7%
0.5%
10.6
17.5
0.6%
0.6%
11.55
14.98
0.56%
0.14%
7.6
3.8
1.9%
3.0
11.9
8.1
10.2
1.4%
‘‘Replaced’’ means that the proper hepatic artery is absent; ‘‘Accessory’’ means that the proper hepatic artery coexists.
ARTICLE IN PRESS Accessory extrahepatic arteries: Blood supply of a human liver by three arteries reported that the hepatic artery was anomalous in 296 out of 701 cases with an overall incidence of hepatic artery anomalies of 42.23%. Koops et al. (2004) carried out a retrospective study of a total of 604 coeliac and superior mesenteric angiographies. His results indicated that the prevalence of an aLHA arising from the left gastric artery was only 3.0%. Studies of 932 cases in liver transplantation including the harvested livers and operated patients showed that variations in the hepatic artery existed in 31.9% (Abdullah et al., 2006). Other studies (Daseler et al., 1947; Fontaine et al., 1970; Reuter and Redman, 1977; Chen et al., 1998; Troupis et al., 2008) reported a prevalence of approximately 10–20% for an aberrant right hepatic artery arising from the superior mesenteric artery and of 8–18% for an aberrant left hepatic artery arising from the left gastric artery. The variations in the extrahepatic arteries are of great clinical importance because the incidence of hepatic vascular injuries increases when an aberrant anatomy is present (Suzuki et al., 1971; Rela et al., 1998a; Jones and Hardy, 2001). Thus, knowledge of the anatomy and frequency of abnormalities in the extrahepatic arterial system is a prerequisite for successful liver transplantation, laparoscopic surgery, and radiological procedures in the upper abdomen, and for the treatment of penetrating injuries in the perihepatic area, both for surgeons and radiologists. Although a single anomaly in the coeliac-mesenteric arterial system is not rare, complex combinations, such as the ones observed in the present case, represent a significant deviation from the normal hepatic arterial pattern. More importantly, the origin and course of the accessory arteries can vary dramatically among individuals. Hence, knowledge of each of the variations can be of paramount importance in individual clinical cases. The present study addresses the occurrence of the accessory extrahepatic arteries with a special emphasis on the anatomical description of their origins, branching pattern, distribution, and topography.
Materials and methods An unusual case of an anomalous pattern of the hepatic artery was encountered during a routine dissection carried out at our institute. The cadaver was that of a Caucasian adult male who died of acute heart failure at the age of 85. No liver disease had been recorded in the donor who had voluntarily agreed that his body or parts of it could
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be used for education and research purposes at our institution. The pseudonymized body was embalmed in a fixative solution containing 60% ethanol and 2% formaldehyde. The donation procedure for anatomical bequests in Germany has been described in detail elsewhere (McHanwell et al., 2008; Korf et al., 2008).
Results In addition to the pHA, two other extrahepatic arteries – an accessory on the left and an accessory on the right – were observed in a human cadaver (Figures 1 and 2). On the left, a 4-cm-long aLHA arose from the left gastric artery and ran in the hepatogastric ligament, first traversing in the left direction, then immediately turning for about 3 cm upwards and finally turning slightly to the right until this artery entered into its accessory porta hepatis. The left gastric artery ran along the lesser curvature of the stomach. In the mid-epigastric region, a 6.4-cm-long pHA originated from the common hepatic artery. The common hepatic artery, stemming from the coeliac trunk, ran dorsalwards and toward the right until it reached the superior portion of the duodenum, where it divided into the pHA and the gastroduodenal artery. The pHA, continuing further along the common hepatic artery after the branching-off of the gastroduodenal artery, turned upwards to ascend in the right free margin of the lesser omentum. Along its further course, the pHA was enveloped by the hepatoduodenal ligament, in which it lay ventral to the portal vein and the aRHA and located on the left side of the other three components lying in this ligament. It finally bifurcated into two arteries, the left and right hepatic arteries, at or near the porta hepatis and supplied oxygenated blood to the left and right hepatic lobes. The pHA did not give off any branches to the gallbladder. On the right side, an 8-cm-long aRHA took origin from the superior mesenteric artery. In its further course, it runs obliquely cranialwards and to the right side, then reached the hepatoduodenal ligament, in which it was accompanied by the pHA, the bile duct, and the portal vein. The aRHA was the most hidden of the three arteries, since it was perfectly sequestered on the dorsal side of the pHA and the portal vein within the hepatoduodenal ligament. This accessory vessel arose from the right edge of the ventral surface of the superior mesenteric artery at an origin site that was located 1.8 cm distal to the origin of the superior
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Figure 2. Drawings show the three hepatic arteries and the coeliac trunk with its three branches (LGA, CHA, SA). The portal vein was omitted in Fig. A in order to provide a clear overview of the accessory hepatic arteries. The cystic artery supplying the gallbladder originated from the aRHA. Normal bile duct was located in the hepatoduodenal ligament. The portal vein, lying between the pHA and the aRHA, was pushed ventrally by the latter to take up an unusual ventral position in the gastroduodenal ligament. (1) aLHA arising from LGA; (2) pHA arising from CHA; (3) aRHA arising from SMA; (4) CBD; and (5) PV.
Figure 1. Photographs of the visceral surface of the porta hepatis showing the three hepatic arteries and their topography. (A) Overview in situ; (B) magnification of the region of interest marked in Fig. A. The portal vein was pulled aside to visualize the three branches of the coeliac trunk arising from aorta (left gastric artery [LGA], common hepatic artery [CHA], Splenic artery [SA]). The accessory left hepatic artery (aLHA), the proper hepatic artery (pHA), and the accessory right hepatic artery (aRHA) supply arterial blood for the liver. Amongst the arteries, the aRHA seemed to be the dominant one for the blood supply to the liver, as judged from the diameter of the blood vessels. (1) Accessory left hepatic artery arising from left gastric artery; (2) proper hepatic artery arising from common hepatic artery; (3) accessory right hepatic artery arising from the superior mesenteric artery (SMA); (4) portal vein (PV) comprising two drainage veins: superior mesenteric vein (SMV) and splenic vein (SV); (5) common bile duct (CBD); (6) superior mesenteric vein (SMV); (7) splenic vein (SV) after the merging of IMV; (8) inferior mesenteric vein (IMV); (9) splenic vein (SV) before the merging of IMV; (10) gastroduodenal artery (GDA); (11) splenic artery (SA); (12) superior mesenteric artery (SMA); (13) liver; (14) gallbladder; (15) cardia of stomach; (16) common hepatic artery; (17) left gastric artery; (18) coeliac trunk (CT); and (19) aorta. Scale bar for Fig. B: 2 cm.
mesenteric artery from the abdominal aorta. The aRHA supplied blood not only to the right lobe of the liver (segments IVa, V, VI, VII, VIII), but also to part of the caudatus lobe (segment I) and the quadratus lobe (segment IVb). Before entering the liver, the aRHA released the cystic artery. This artery, feeding the gallbladder, was found between the cystic duct and the common bile duct, where it is also called the hepatocystic triangle. Within the hepatoduodenal ligament, the common bile duct lay on its right edge and behind the portal vein. The portal vein, as the sole vein in the hepatoduodenal ligament, was formed in a regular manner behind the pancreas by the confluence of the superior mesenteric vein and the splenic vein. However, it was pushed ventrally by the aRHA within this ligament and therefore assumed a position in front of the aRHA and the common bile duct. As a result, the ventral border of Winslow’s foramen was formed by the aRHA instead of by the portal vein in this case. In contrast to the extrahepatic artery variations, the coeliac trunk, arising at the level of the first lumbar intervertebral disc, showed its characteristic tripod disposition: the common hepatic artery, the left gastric artery, and the splenic artery. The superior mesenteric artery was located 3.2 cm distal to the origin of the coeliac trunk from the aorta. Besides the irregular arterial branch to the liver, the superior mesenteric artery gave rise to its normal branches, including the inferior pancreaticoduodenal artery, the jejunal arteries, the ileal
ARTICLE IN PRESS Accessory extrahepatic arteries: Blood supply of a human liver by three arteries arteries, the iliocolic artery, the right colic artery, and the middle colic artery. These regular branches showed normal branching and distribution patterns. On general inspection, no pathology or malformation was evident within the upper abdomen.
Discussion In the present report, we describe an unusual case of three extrahepatic arteries in a human cadaver. This variation is the first observation among 100 human adult specimens from a 10-year retrospective screening of the dissection records at our institute. The present variation should be defined as an Adachi type of I 11 variation, which has a prevalence of 2%, or as a Michels type of VII variation (1% prevalence), or as a Hiatt type IV variation (2.3% prevalence, replaced or accessory RHA+replaced or accessory LHA) (Adachi, 1928; Michels, 1966; Hiatt et al., 1994). Recently, Koops et al. (2004) reported this combination in 1.4% based on their angiographic examinations. However, all of the previous reports were predominantly concentrated on their statistical records instead of on the anatomical details of the variations. Among the three hepatic arteries reported, the aRHA was the thickest one. Its diameter can even be compared to that of the common hepatic trunk. The aRHA was thereby believed to be the dominant blood supply to the liver in our case. In view of the arrangement of the three hepatic arteries, the porta hepatis could be considered as a portal quinta. During human embryonic development, the liver normally arises as a bud of the entoderm at the junction between the primitive fore- and midgut. In the angiogenesis of the coeliac-mesenteric arterial system, the ventral splanchnic arteries arising from the dorsal aorta are the stem vessels. Initially, the ventral splanchnic arteries generate four roots for supplying the fore- and the midgut. These four roots are connected to each other through longitudinal anastomoses at different levels. During further development, the second and third roots obliterate gradually. Only the first and the fourth root persist and are connected by a ventral longitudinal anastomosis. The common hepatic, the left gastric, and the splenic arteries usually originate from the first root, the so-called primitive coeliac axis, whereas the superior mesenteric artery normally arises from the fourth root. In contrast, data from animal embryology show that the persistence of a primitive trunk ‘‘Coeliaco-Mesen-
481
terica’’, joining the first and the fourth roots, is an entirely normal condition in some lower animals such as the anura, the reptiles and also in some mammals. In other words, the coeliac trunk and the superior mesenteric artery originate from the primitive trunk in these species. Furthermore, Bremer suggested that an extrinsic factor, acting in the form of some developing sympathetic fibers, might entwine the coeliac root and the superior mesenteric groups to alter their growth and even the branches of the vessels in the chick (Bremer, 1924). In contrast, the ventral longitudinal anastomosis between these two existing roots is usually interrupted in human beings. If this separation occurs abnormally, any one of the arterial variations can emerge (Tandler, 1904; Broman, 1908; Keibel and Mall, 1910; Waddington, 1940; C-avdar et al., 1997; Zaret, 2001). A review of these previous embryological studies suggests that the partial persistence of this longitudinal anastomosis might explain the occurrence of the aRHA originating from the SMA in our study. The growing number of hepatic transplants and the use of new laparoscopic techniques are the main reason for the renewed interest in extrahepatic arterial variations (Abdullah et al., 2006; Streitparth et al., 2007). Not only for laparoscopic surgery and radiological procedures, but also for liver transplantation, an accurate diagnostic workup of the hepatic vascular anatomy is essential. Currently, the split liver transplantation, in which the donor liver is cut in half for two recipients, results in a high interest in the anatomical variations of the extrahepatic blood supply. During the transplant procedure, the extrahepatic arterial patterns of the donor liver and the recipient liver must be determined with precision. Division of or damage to a hepatic artery owing to the ignorance of the variations may induce subsequent liver ischemia (Brems et al., 1989; Soin et al., 1996; Pulakunta et al., 2008). More important, the pHA should be differentiated from an accessory hepatic artery during surgery. Any erroneous ligation could lead to necrosis of a liver segment or lobe (Grundmann et al., 1980; Todo et al., 1987; Merion et al., 1989; Brems et al., 1989; Settmacher et al., 2000; Abdullah et al., 2006; Pulakunta et al., 2008). As a result, all variations must be defined and appropriately managed to ensure a complete vascular and biliary supply of both grafts in a liver transplantation (Rela et al., 1998b; Chaib et al., 2005; Streitparth et al., 2007; Mu ¨ller et al., 2007). To make much safer surgery, Harms et al. (2005) recommends a 3D visualization system that improves anatomical assessment, allows for the determination of individual vascular territories,
ARTICLE IN PRESS 482 and acts as an intraoperative guide with enhanced precision for the assessment of the optimal surgical splitting line of the transplanted livers. In the present case, the cystic artery originated from the aRHA instead of from the pHA. Since the early 1990s, laparoscopic cholecystectomy has been accepted as the preferred method for the treatment of gallbladder stones (Hugh et al., 1992). Because only a limited surgical field is magnified on a video monitor during the minimally-invasive operation, the surgeon needs to have a thorough knowledge of variations in the cystic arterial supply. Thus, the awareness of anomalous extrahepatic arteries is also important for a successful hepatobiliary surgery. Arterial variations consisting of an accessory right hepatic artery must also be considered when a pancreatic or duodenal surgery is contemplated. Variations of the mesenteric arterial branches are also important in other surgical procedures, such as right hemi-colectomy and resection of the transverse colon. Furthermore, when a porto-caval shunt is performed, preoperative knowledge of an interposition of an aberrant right hepatic artery between the portal vein and the abdominal vena cava can be of vital importance (Woods and Traverso, 1993; Abdullah et al., 2006; Streitparth et al., 2007; Lo ´pez-Andu ´jar et al., 2007).
Acknowledgements The authors are grateful for the body donation and wish to acknowledge the contributions of the medical students and tutors (matriculation year of 2007) who participated in the cadaver dissection during their medical training at our institution. They also thank Prof. Christoph Redies for his excellent editing of this manuscript and Jens Geiling, Michael Szabo ´, and Simone Freund for their expert help with photography, drawing, and technical assistances.
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