Surgical anatomy of the right hepatic artery in Rouviere’s sulcus evaluated by preoperative multidetector-row CT images

Left-sided hepatectomy with caudate lobectomy is ordinarily applied for patients with Bismuth type IIIb hilar cholangiocarcinoma. In recent years, even if a Bismuth type IIIb tumor extends to the right-side hilum involving the right hepatic artery (RHA), long-term survival after left hepatectomy or trisectionectomy with concomitant arterial resection and reconstruction has been reported [1‐3]. However, this surgical technique is still extremely difficult and has a high risk for postoperative complications. To understand thoroughly the surgical anatomy around Rouviere’s sulcus (RS) is pivotal for lymph node dissection and arterial reconstruction in left-sided hepatectomy for hilar cholangiocarcinoma.

In RS, located at the boundary between the caudate lobe and the right hepatic lobe, the branches from the right hepatic artery, right portal vein and right hepatic bile duct run into the liver parenchyma. In general, RHA is bifurcated from the proper hepatic artery (primary bifurcation) and, thereafter, bifurcates into the anterior (Aant) and posterior (Apost) hepatic artery immediately before entering into the liver parenchyma (secondary bifurcation). Then, segmental (SA) or subsegmental arteries (SSA) from Aant or Apost are bifurcated within the liver parenchyma (tertiary bifurcation). However, SA or SSA is often atypically branched off from the RHA. In addition, the posterior SA or SSA occasionally run cranially to the right portal vein (RPV) (supraportal course), although Apost typically runs caudally to RPV (infraportal course) [4]. Thus, the branching form of the arteries around RS is complicated. The preoperative understanding of anatomical variation of the SA/SSA branches and course variations of the arterial posterior branches around RS, especially the supraportal/infraportal posterior SA/SSA, is crucial in left-sided hepatectomy for hilar cholangiocarcinoma in order to avoid critical surgical complications, such as intraoperative arterial injury, hepatic infarction and hepatic failure. However, there have been few reports that provide a detailed discussion about the anatomical variation of SA/SSA in RS from the standpoint of surgical resection.

The objective of this study is to elucidate the bifurcation patterns of the SA/SSA using multidetector-row computed tomography (MDCT). We clarified the incidence of early-bifurcated SA/SSA around RS, the variations in the courses they followed. The findings of this study should be helpful for left-sided hepatectomy for hilar cholangiocarcinoma.

Lymph node dissection in RS is essential in left-sided hepatectomy for hilar cholangiocarcinoma. In recent years, left-sided hepatectomy with concomitant resection and reconstruction of RHA may offer a better chance of long-term survival in patients with the Bismuth type IIIb cholangiocarcinoma involving RHA [1‐3]. However, small SA/SSA, which early bifurcate from the RHA and separately enter the hepatic parenchyma, are often found in RS during lymph node dissection. Therefore, a detail preoperative examination of these vascular bifurcation patterns around RS is more crucial in en block arterial resection with left-sided hepatectomy for hilar cholangiocarcinoma to avoid postoperative complications, such as hepatic infarction and subsequent hepatic failure. The present study clarified the various anatomical patterns of SA/SSA around the RS from three viewpoints, bifurcation patterns of the SA/SSA (typical or atypical form), course of the posterior SA/SSA for the RPV (supraportal or infraportal course) and bifurcation site of the SA/SSA (extrahepatic or intrahepatic bifurcations).

The ramification variant of RHA, bifurcated from the superior mesenteric artery or the celiac trunk, has already been reported [5]. On the other hand, there have been few detailed reports on anatomical variants of the SA or SSA around the RS. In this study, atypical SA or SSA (A6 or A6a and so on), which bifurcated independently prior to the main bifurcation of Aant and Apost, were observed in 34.7 % of the hilar cholangiocarcnioma patients. Furthermore, in cases with the atypical form, the early-bifurcated posterior SA/SSA following supraportal course, which is called as “partially supraportal type”, was seen in more than 30 %. In total cohort of our study, the frequency of supraportal posterior branches was 19.5 %, similar to that in a previous report [4]. In Bismuth type IIIb patients with supraportal posterior branches, the risk of intraoperative arterial injury during left-sided hepatectomy is increased. Particularly, during left trisectionectomy for patients with partially supraportal branches, meticulous attention is needed to avoid mistaking partially suprapotal branches (A7 and so on) for the anterior ones. Misidentification of the supraportal posterior branches can result in severe postoperative complications, such as hepatic infarction and hepatic failure [4]. Additionaly, in en bloc resection and reconstruction of RHA with cancer invasion, the uninvolved distal arterial branch should be identified around RS before hepatic transection. However, in cases of supraportal Apost, it is difficult to find uninvolved distal Apost. Since supraportal Apost runs behind portal pedicles, distal Apost is usually exposed on the cutting surface during or after hepatic transection, increasing the risk of arterial injury. Therefore, preoperative examination of the bifurcation pattern of SA/SSA and the course of the posterior SA/SSA (supraportal or partially supraportal) using MDCT is mandatory for left-sided hepatectomy, especially left trisectionectomy.

Anatomical variations of an artery, portal vein or bile duct commonly arise around the hepatic hilum before forming Glisson’s triad. Since Glisson’s triad is formed with an intimate fixation in the liver parenchyma, abnormal ramification of these vessels is rare in the liver parenchyma [6]. In this study, the SA/SSA were bifurcated extrahepatically (extrahepatic type) in 82 (66.1 %) of total cohort, all 43 atypical forms and in 39 of 75 typical forms. Even in typical forms, the extrahepatic bifurcation of SA/SSA was observed in 52 %. There is a limitation in our classification of the two types, the extrahepatic or intrahepatic types, due to the difficulty in identifying the starting point of Glisson’s sheath using MDCT. In other words, these types do not necessarily correspond to an anatomical boundary between the outside and inside of the liver. However, based on the CT criteria of the present study, a bifurcation of the SA/SSA determined to be the extrahepatic type is usually exposed during lymph node dissection for RS. Furthermore, even in some patients classified as the intrahepatic type, the bifurcation of the SA/SSA might be exposed at the extrahepatic area in cases of left trisectionectomy or soft hepatic parenchyma, enabling the RS to be opened easily. Our results showed that the extrahepatic type occurred with a high incidence (66.1 %).

In this study, arterial variation around the RS evaluated with preoperative MDCT was not confirmed intraoperatively in all cases because we included cases of right-sided hepatectomy. However, imagining of the vascular 3D structure has been dramatically improved due to advances in the spatial resolution of volume-rendered multidetector CT angiography. Consequently, homology between the preoperative anatomical imaging and intraoperative findings has been reported [4]. Meanwhile, in recent years, the advent of imaging analysis software such as SYNAPSE Vincent® (Fuji Film) has enabled 3D visualization of the vascular structure and liver volumetry of perfused regions, and is expected to be applied for intraoperative navigation [7, 8]. Nevertheless, there are limitations in the automated vascular analysis of these kinds of software. A thin and complex vessel configuration is not necessarily delineated by the software, such as branches of the SA/SSA in RS. Surgical procedures in which injury to the SA/SSA has a critical impact on the residual hepatic function still need a conventional detailed investigation using MDCT to obtain 3D imaging of the anatomical structure.

Extrahepatic bifurcation of the SA/SSA from RHA is relatively common (66.1 %). In particular, more than 30 % of the early-branched posterior SA/SSA from RHA (atypical form) often follow a supraportal course. Although the anatomical variation of arterial branches around the RS is complex, detailed preoperative knowledge of the anatomy, including SA/SSA, is crucial for left-sided hepatectomy for hilar cholangiocarcinoma.

3D images, three-dimensional images; Aant, anterior hepatic artery; Apost, posterior hepatic artery; MDCT, multidetector-row computed tomography; MPR, multi planar reformation; RHA, right hepatic artery; RPV, right portal vein; RS, Rouviere’s sulcus; SA, segmental artery; SSA, subsegmental arteries