CT Angiography for Delineation of Celiac and Superior Mesenteric Artery Variants in Patients Undergoing Hepatobiliary and Pancreatic Surgery

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1 CT of Celiac rtery and SM Variants Hepatobiliary Imaging Clinical Observations Corinne. Winston 1 Nancy. Lee 2 William R. Jarnagin 3 Jerrold Teitcher 1 Ronald P. DeMatteo 3 Yuman Fong 3 Leslie H. lumgart 3 Winston C, Lee N, Jarnagin WR, et al. Keywords: arteriography, CT angiography, hepatobiliary imaging, pancreas, superior mesenteric artery DOI: /JR Received ugust 31, 2004; accepted after revision September 13, Department of Radiology, Memorial Sloan-Kettering Cancer Center, 160 E 53rd St., 8th Fl., New York, NY ddress correspondence to C.. Winston. 2 Department of Radiology, Thomas Jefferson University Hospital, Philadelphia, P Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY WE This is a Web exclusive article. JR 2007; 188:W13 W X/07/1887 W13 merican Roentgen Ray Society CT ngiography for Delineation of Celiac and Superior Mesenteric rtery Variants in Patients Undergoing Hepatobiliary and Pancreatic Surgery OJECTIVE. The objective of our study was to determine the frequency of different arterial variants identified at abdominal CT angiography (CT) performed before pancreatic and hepatobiliary surgery. CONCLUSION. Variant hepatic and celiac arterial anatomy is common. CT can be used to identify common and uncommon variants that are important for the surgical management of patients with pancreatic and hepatobiliary neoplasms. DCT allows the rapid acquisition M of high-resolution images through the hepatic and mesenteric arteries during the phase of maximal contrast enhancement. The role of CT angiography (CT) in determining tumor resectability in patients with pancreatic and hepatobiliary malignancy has been described [1, 2]. n important additional role of CT for evaluating patients with pancreatic and hepatobiliary malignancy is the delineation of variant arterial anatomy. Variant arterial anatomy is common, occurring in more than half of the population [3]. Visualization of the surgical field can often be limited in patients with pancreatic and hepatobiliary malignancy, especially if there has been prior surgery, if there is local inflammation such as that accompanying a biliary stent, or if the patient is obese. Preoperative knowledge of variant anatomy can assist in selection of treatment options and in surgical planning, facilitate surgical dissection, and help avoid iatrogenic injury. The purpose of this study was to determine the frequency of different arterial variants identified at abdominal CT performed in a large series of patients before major pancreatic or hepatobiliary surgery. Materials and Methods Patient Population CT database from ugust 2001 to February 2003 included 394 consecutive CT angiograms in 371 patients, all of whom were under consideration for surgical resection for a suspected pancreatic or hepatobiliary neoplasm. Each patient was included only once in the study. CT was performed to determine tumor resectability and to aid surgical planning. Our institutional review board approved this retrospective report review, and patient informed consent was not required. CT ll CT examinations were performed on a 4- MDCT scanner (LightSpeed QX/i, GE Healthcare). Water was administered to all patients as a nonopaque oral contrast agent. CT was performed after the IV administration of 140 ml of nonionic contrast material (iohexol [Omnipaque, Nycomed]) with a power injector through an 18-gauge catheter at a rate of 4 ml/s when possible (n = 325 patients, 88%). If limited venous access precluded this injection rate, a slower injection rate was used. 10-mL timing bolus was used to determine peak enhancement of the upper abdominal aorta; 1.25-mm images were acquired with a 1-mm overlap (table speed, 7.5 mm per 0.8-second rotation; pitch, HS) at the point of maximal arterial enhancement. For patients with suspected hypervascular lesions, including hepatocellular carcinoma and neuroendocrine carcinoma, CT was performed as part of a triphasic examination with 2.5-mm slices acquired at a 1.25-mm interval in the early arterial phase and 5-mm slices obtained during the same breath-hold in the late arterial phase. For patients with suspected pancreatic lesions, 3.75-mm-slice images acquired with a 2-mm overlap were obtained in the late arterial phase (table speed, mm per 0.8-second rotation; pitch, HQ) in the same breath-hold as the angiographic images; 5-mmslice images acquired at a 2.5-mm interval through the abdomen were obtained at 70 seconds after the start of the injection (table speed, mm per 0.8-second rotation; pitch, HQ). W13

2 Data Collection During routine interpretation of the CT examinations, the attending radiologist prospectively assessed for the presence of variant celiac axis and hepatic arterial anatomy. ll radiologists interpreting these examinations were attending oncologic imagers experienced in using CT for preoperative planning. The official reports of the CT examinations were reviewed to identify whether variant hepatic arterial or variant celiac axis anatomy was present. The reports were also reviewed to determine if a study was considered of limited or if it was of diagnostic quality. For patients in whom a variant was identified, the specific type of variant was recorded according to Michels criteria [3]. For those patients in whom no mention of the arterial anatomy was reported (n = 24), one attending radiologist retrospectively reviewed the scans to assess the vascular anatomy. ll studies were evaluated in the cine mode on PCS. Threedimensional reconstructions were created by the attending radiologist at the time of interpretation Fig. 1 Classic hepatic arterial anatomy in 58-year-old man with metastatic colon cancer to liver. Volume-rendered 3D image created from axial contrast-enhanced CT data reveals classic branching arterial anatomy. Celiac axis (short solid arrow) trifurcates into splenic artery, common hepatic artery (long solid arrow), and left gastric artery. Common hepatic artery gives rise to gastroduodenal artery (open arrowhead) and proper hepatic artery (solid arrowhead). Right hepatic artery (long open arrow) and left hepatic artery (short open arrow) originate from proper hepatic artery. Fig. 2 Replaced right hepatic artery in 69-year-old woman., Volume-rendered 3D image created from axial contrast-enhanced CT data reveals right hepatic artery (small open arrow) originating from superior mesenteric artery (SM) (large solid arrow). Right hepatic artery courses posterior to stent (large open arrow) located within common bile duct. Note left hepatic artery (small solid arrow) originating from left gastric artery., Thin-slab maximum-intensity-projection axial image reveals right hepatic artery (small solid arrow) originating from SM (small open arrow). Right hepatic artery courses through portacaval space, between portal vein (large open arrow) and inferior vena cava (large solid arrow). of the CT scan based on the discretion of the radiologist interpreting that examination. Results ll studies were considered of diagnostic quality, although the examination was considered somewhat limited due to respiratory motion in one patient. One hundred eighty-eight (51%) of the 371 patients had classic arterial anatomy identified at CT (Fig. 1). One hundred sixty-two (44%) patients had a single ar- W14

3 CT of Celiac rtery and SM Variants terial variant identified, and 21 (6%) patients had more than one arterial variant seen. The most common variant identified was a replaced right hepatic artery originating from the superior mesenteric artery (SM), which was seen in 54 (15%) patients (Fig. 2). The second most common variant was a replaced left hepatic artery originating from the left gastric artery, seen in 30 (8%) patients (Fig. 3). Variations in the origin of the common hepatic artery were seen in 12 (3%) patients. In six (2%) patients, the common hepatic artery originated from the SM (Fig. 4), and in six (2%) patients, the common hepatic artery originated from the abdominal aorta (Fig. 4). double hepatic artery, as described by Fasel et al. [4] and Covey et al. [5], refers to one or both hepatic arteries originating from the celiac axis or the aorta. This was seen in 15 (4%) of the patients in our study population. The right hepatic artery originated from the celiac axis in 13 (4%) patients (Fig. 5 and 5) and from the aorta in one (< 1%) patient (Fig. 5C). The left hepatic artery originated from the celiac axis in one (< 1%) patient (Fig. 5D). ccessory hepatic arteries were identified in 16 (4%) patients. The frequencies of the different types of arterial variants identified are reported in Table 1. Fig. 3 Replaced left hepatic artery originating from left gastric artery in 73-year-old woman., Volume-rendered 3D image created from axial contrast-enhanced CT data reveals replaced left hepatic artery (small arrow) originating from left gastric artery (arrowhead). Common hepatic artery (large arrow) arises from celiac axis., Thin-slab axial maximum-intensity-projection image reveals replaced left hepatic artery (arrow) coursing through fissure for ligamentum venosum to perfuse left hepatic lobe. Discussion CT is often performed in patients with pancreatic and hepatobiliary neoplasms to determine tumor resectability. In addition to evaluating for vascular involvement by tumor, it is also important for the radiologist to assess for the presence of variant arterial anatomy. Variant hepatic and celiac arterial anatomy have been reported in 55% of patients on the basis of initial cadaveric dissections by Michels [3]. In 1969, Redman and Reuter [6] reported most of the variations seen in roughly 50% of the population have little surgical significance. Since that time, however, there are new surgical and interventional treatment options for patients with resectable and unresectable disease. The presence of different arterial variants may alter patient management. Therefore, having an awareness of the CT appearance of these variants and an appreciation of their clinical significance is of great importance. MDCT enables the rapid acquisition of thin-slice high-resolution images of the abdominal arteries during the phase of maximal contrast enhancement. The volumetric acquisition of data allows 3D reconstructions to be created, providing the surgeon with a 3D model of the patient s arterial anatomy [7]. major benefit of CT over conventional arteriography is that the relationship of arteries to the adjacent organs and the biliary tree is displayed so that the course of an aberrant vessel is clearly delineated. This can be of great value because direct visualization of the surgical field is often limited in patients with pancreatic and hepatobiliary malignancy, especially if there has been prior surgery, if there is local inflammation such as that accompanying a biliary stent, or if the patient is obese. Preoperative knowledge of variant arterial anatomy may obviate extensive dissection to identify the vessels and may avert vascular damage. The mortality rate associated with liver resection ranges from 3% to 5%, with hemorrhage a leading cause of perioperative mortality [8, 9]. MDCT angiography has a reported accuracy of 97 98% compared with conventional angiography for detecting arterial variants [2, 10]. The role of CT in the preoperative evaluation of patients with hepatic [2, 11] and pancreatic [1] neoplasms has been described. However, for those studies, the authors evaluated a relatively small number of patients. To the best of our knowledge, this report is the first describing the ability of CT to delineate the broad range of clinically significant different arterial variants encountered in a large surgical population. W15

4 We identified classical arterial anatomy in 51% of the patients who underwent CT (Fig. 1). In classic visceral anatomy, the celiac trunk originates from the abdominal aorta and gives origin to the left gastric artery, the splenic artery, and the common hepatic artery [12]. The common hepatic artery extends anteriorly and bifurcates into the gastroduodenal artery and the proper hepatic artery. The proper hepatic artery extends cephalad and runs to the left side of the common hepatic duct to bifurcate into the right and left hepatic arteries, usually just below the bifurcation of the common hepatic duct [13]. Variant arterial anatomy was seen in 49% of the patients who underwent CT. This frequency is similar to the results of the cadaveric study by Michels [3]. The most common variant seen at CT was a replaced right hepatic artery originating from the SM, identified in 15% of the patients. Identification of a replaced right hepatic artery is critical when performing pancreaticoduodenectomy and for porta hepatis dissection during hepatic resection. Whereas the right hepatic artery usually courses anterior to the right portal vein, the replaced right hepatic artery originates from the SM, courses posterior to the main Fig. 4 Variation in origin of common hepatic artery., Common hepatic artery originates from superior mesenteric artery (SM) in 62-year-old man. Volume-rendered 3D image created from axial contrast-enhanced CT data reveals common hepatic artery (small open arrow) originates from SM (large solid arrow). Gastroduodenal artery (large open arrow) originates from common hepatic artery. Note accessory left hepatic artery (small solid arrow) originating from left gastric artery., Common hepatic artery originates directly from aorta in 68-year-old woman who also has trifurcation of common hepatic artery. Volume-rendered 3D image created from axial contrast-enhanced CT data reveals common hepatic artery (small open arrow) originates directly from abdominal aorta. Common hepatic artery trifurcates into right hepatic artery (large solid arrow), left hepatic artery (small solid arrow), and gastroduodenal artery (large open arrow). portal vein in the portacaval space, and classically ascends posterolateral to the common bile duct [13] (Fig. 2). Palpation for the presence of the artery can be unreliable when there is portal inflammation, enlarged portal lymph nodes, or an existing biliary stent. In a patient with cancer in the pancreatic head or uncinate process, a replaced right hepatic artery may be involved by tumor, precluding the patient from surgical resection. If the right hepatic artery is not involved, particular care needs to be taken in this region so as not to inadvertently injure such an artery during dissection. This is especially important because patients with pancreatic head tumors are often jaundiced. Unlike the nonjaundiced patient, in whom the portal blood flow can sustain viability of the liver, the liver in the jaundiced patient is prone to hepatic necrosis if the arterial blood flow is compromised [14]. Therefore, the surgeon may choose biliary drainage for the jaundiced patient with a replaced right hepatic artery to relieve the jaundice before pancreaticoduodenectomy. The second most common arterial variant identified at CT was a replaced left hepatic artery originating from the left gastric artery, seen in 8% of the patients. This frequency is consistent with the findings reported by Michels [3]. The replaced left hepatic artery originates off the left gastric artery and courses to the right through the lesser sac, through the fissure for the ligamentum venosum, and into the umbilical fissure to perfuse the left hepatic lobe. efore left hepatectomy is performed, this vessel must be identified and ligated. Preoperative knowledge of this variant facilitates portal dissection because the major arterial branch to the left liver does not need to be found in the porta hepatis. The double hepatic artery as described by Fasel et al. [4] refers to a right or left hepatic artery that originates from the celiac axis or aorta. We identified a double hepatic artery in 4% of our patients, a result similar to that reported by Covey et al. [5] (3.7%) as seen at digital subtraction angiography. To the best of our knowledge, this latter type of arterial variant has not been described in the CT literature. n anomalous location of the right hepatic artery that originates from the celiac axis or aorta and extends posterior to the bile duct may result in iatrogenic injury to such a vessel if that vessel is not seen by the surgeon. ccessory left and right hepatic arteries were identified in 4% and 1%, respectively, of W16

5 CT of Celiac rtery and SM Variants C Fig. 5 Double hepatic artery., Double hepatic artery in 62-year-old woman. Right hepatic artery originates from celiac axis. Steep oblique volume-rendered 3D image created from axial contrastenhanced CT data image viewed from below reveals right hepatic artery (thick arrow) originates from celiac axis (arrowhead). Right hepatic artery extends posterior to stent (thin arrow) that is located within common bile duct., Double hepatic artery in 62-year-old woman. Right hepatic artery originates from celiac axis. Volume-rendered 3D image created from axial contrast-enhanced CT data reveals right hepatic artery (small arrow) originates from celiac axis (arrowhead) proximal to origin of common hepatic artery (large arrow). C, Double hepatic artery in 71-year-old woman. Right hepatic artery originates from aorta. Thick-slab maximum-intensity-projection image obtained from axial contrastenhanced CT data reveals right hepatic artery (long arrow) originates directly from abdominal aorta, parallel to origin of superior mesenteric artery (SM) (short arrow). rrowhead indicates celiac axis. D, Double hepatic artery in 77-year-old woman. Left hepatic artery originates from celiac axis. Volume-rendered 3D image created from axial contrast-enhanced CT data reveals origin (small open arrow) of left hepatic artery (large open arrow) directly from celiac axis. Common hepatic artery (large solid arrow) originates from celiac axis. Origin of SM (small solid arrow) is obscured by splenic artery. D W17

6 TLE 1: Frequency of Different rterial Variants Seen at CT ngiography in 371 Patients Type of Finding No. of Findings (n = 394) % of Patients (n = 371) Classic celiac arterial anatomy Replaced RH off SM Replaced LH off LG 30 8 rtery to segments 2 and 3 off LG 19 5 rtery to segments 4 and 4 off RH 17 5 Trifurcation of CH into GD, RH, and LH 15 4 RH off celiac axis 13 4 ccessory LH off LG 13 4 LG directly off abdominal aorta 11 3 CH off SM 6 2 CH directly off the aorta 6 2 RH off GD 5 1 ccessory RH 3 1 Common trunk of celiac axis and SM 2 < 1 Medial and lateral branches separate off CH 2 < 1 LH off CH 2 < 1 GD off RH 2 < 1 SM gives rise to GD 2 < 1 LH off celiac axis 1 < 1 RH off aorta 1 < 1 Segment 4 branch off GD 1 < 1 Extrahepatic branching of RH into anterior and posterior with artery to segment 4 off anterior division of RH 1 < 1 Note Twenty patients had two variants seen at CT and one patient had four variants. LH = left hepatic artery, RH = right hepatic artery, LG = left gastric artery, SM = superior mesenteric artery, CH = common hepatic artery, GD = gastroduodenal artery. Reprinted with permission from [5]. the patients in our study. n accessory left hepatic artery usually originates from the left gastric artery and follows the same course through the lesser sac as does the replaced left hepatic artery. This accessory artery provides an additional source of arterial blood to the left hepatic lobe (it is seen in addition to the classic left hepatic artery) and may be sacrificed without compromising the arterial supply to the left hepatic lobe. n accessory left hepatic artery needs to be occluded separately when controlling the inflow to the left hepatic lobe because this artery will not be occluded when the blood supply in the porta hepatis is occluded. The course of an accessory right hepatic artery is similar to that of a replaced right hepatic artery and is present in addition to the classic right hepatic artery. s with the accessory left hepatic artery, the accessory right hepatic artery provides additional blood supply to the respective hepatic lobe and may be sacrificed without compromising the arterial supply to the right lobe. Distinction between an accessory and a replaced artery is therefore important. n awareness of an accessory right hepatic artery is also important so that inadvertent injury to this artery does not result in hemorrhage. The common hepatic artery originated from the SM in 2% as seen at CT. When pancreaticoduodenectomy is performed, it is important that the common hepatic artery be preserved so the artery must be dissected to its origin from the SM. The anomalous course of the common hepatic artery is in proximity to the pancreatic head and may be involved by tumor, making resection impossible. Even if this variant vessel is not involved, if not recognized, if may be inadvertently injured during resection. This is particularly problematic in the jaundiced patient. In recent years, clinical data have shown hepatic artery infusional chemotherapy to have efficacy as adjuvant to resection in controlling hepatic disease [15]. The goal of intraarterial chemotherapy is to provide uni- form perfusion of the chemotherapeutic agent throughout the liver. The catheter is surgically placed via an arteriotomy in the gastroduodenal artery with the catheter tip inserted up to but not beyond the junction of the gastroduodenal artery and the common hepatic artery. Variant arterial anatomy does not necessarily preclude a patient from placement of a pump. Recognition of a replaced or an accessory artery is important so that the vessel can be ligated at the time of catheter placement to allow uniform perfusion of the hepatic parenchyma. In our institution, CT has replaced direct catheter angiography in the preoperative evaluation of patients before intraarterial pump chemotherapy. We assessed the main arteries surrounding the pancreatic head because these are the vessels that are clinically relevant for pancreatic surgery. Variations in the pancreaticoduodenal arcade, gastric arteries, and gastroepiploic arteries are not usually significant for pancreatic and hepatobiliary surgery. Variations of the portosplenic confluence are quite rare and, therefore, not discussed in this article. Variations in the branching of the intrahepatic portal venous system and the hepatic veins are encountered more frequently. We are presently performing a large-scale prospective study assessing the frequency of variant portal venous and hepatic venous anatomy as seen at CT with surgical correlation. limitation of this study is that we do not have surgical or conventional arteriographic confirmation of the accuracy of the CT findings. However, the overall prevalence of arterial variants in our study is concordant with that described in the anatomy and conventional angiography literature [3, 5]. direct comparison of CT findings with conventional angiography findings is not be possible at our institution because CT has replaced invasive catheter angiography for preoperative staging and for preoperative vascular mapping for placement of intraarterial pump chemotherapy. We did not intend to assess the sensitivity or specificity of CT in detecting arterial variants, which have already been reported, but rather to show that the broad range of common and uncommon clinically significant arterial variants are visible using CT. lthough there have been previous studies describing arterial variants, to the best of our knowledge, those studies did not have large patient populations. Some of the more uncommon variants that have surgical significance have not been described at CT. In addition, the importance of recognizing arterial W18

7 CT of Celiac rtery and SM Variants variants in preoperative planning for the resection of hepatic and pancreatic neoplasms has not been systematically addressed. Most articles that focus on arterial variants describe the clinical relevance of arterial variants in patients undergoing hepatic transplantation. ecause CT is becoming more widely used in the evaluation of patients with hepatic and pancreatic neoplasms, recognition of both the CT appearance and the clinical significance of these variants is essential for patient management. The surgical relevance and clinical utility reported in this article are based on a lifetime of experiences of the surgical coauthors of this study, all of whom are experienced hepatobiliary surgeons. Whereas, classically, interventional radiologists have been the radiologists who were familiar with the conventional angiographic appearances of the liver and pancreas, now CT radiologists must gain an awareness of the broad range of arterial variants visible at CT. The images in this study were all obtained on a 4-MDCT unit and depict the anatomy and variants of the major arteries. It is likely that use of 16- or 64-MDCT scanners would enable visualization of the smaller arteries. However, it is the major arteries that are clinically significant. Not all institutions (including academic institutions) have 16-MDCT scanners. Some arterial variants can even be identified on standard 5-mm slices, such as a replaced right hepatic artery coursing through the portacaval space. It is important to recognize that valuable information can be obtained from a 4-MDCT scanner. We did not describe the clinical significance of arterial variants in patients undergoing liver transplantation because that is a separate topic and has been discussed extensively by other authors. In conclusion, variant celiac and hepatic arterial anatomy as seen at CT is common, occurring in 49% of our patient population. CT can be used to identify both the common and rare arterial variants. The role of CT in patients with pancreatic and hepatobiliary malignancies has broadened from one of staging to include vascular mapping, which is essential for surgical planning. Preoperative knowledge of variant anatomy can assist in the selection of treatment options, facilitate surgical dissection, and help avoid iatrogenic injury. cknowledgment We would like to express our tremendous gratitude to Lachlan Smith for much valued computer expertise and assistance in database management. His efforts are greatly appreciated. References 1. Raptopoulos V, Steer ML, Sheiman RG, Vrachliotis TG, Gougoutas C, Movson JS. The use of helical CT and CT angiography to predict vascular involvement from pancreatic cancer: correlation with findings at surgery. JR 1997; 168: Sahani D, Saini S, Pena C, et al. Using multidetector CT for preoperative vascular evaluation of liver neoplasms: technique and results. JR 2002; 179: Michels N. lood supply and anatomy of the upper abdominal organs with a descriptive atlas. Philadelphia, P: Lippincott, Fasel JHD, Muster M, Gailloud P, Mentha G, Terrier F. Duplicated hepatic artery: radiologic and surgical implications. cta nat 1996; 157: Covey M, rody L, Maluccio M, Getrajdman GI, rown KT. Variant hepatic arterial anatomy revisited: digital subtraction angiography performed in 600 patients. Radiology 2002; 224: Redman HC, Reuter SR. ngiographic demonstration of surgically important vascular variations. Surg Gynecol Obstet 1969; 129: Winter TC, Nghiem HV, Freeny PC, Hommeyer SC, Mack L. Hepatic arterial anatomy: demonstration of normal supply and vascular variants with three-dimensional CT angiography. RadioGraphics 1995; 15: Jarnagin WR, Gonen M, Fong Y, et al. Improvement in perioperative outcome after hepatic resection. nn Surg 2002; 236: Fong Y. Surgical therapy of hepatic colorectal metastasis. C Cancer J Clin 1999; 49: Takahashi S, Murakami T, Takamura M, et al. Multi-detector row helical CT angiography of hepatic vessels: depiction with dual-arterial phase acquisition during single breath hold. Radiology 2002; 222: Kapoor V, rancatelli G, Federle MP, Katyal S, Marsh JW, Geller D. Multidetector CT arteriography with volumetric three-dimensional rendering to evaluate patients with metastatic colorectal disease for placement of a floxuridine infusion pump. JR 2003; 181: Vandamme JPJ, onte J, Van der Schueren G. revaluation of hepatic and cystic arteries: the importance of the aberrant hepatic branches. cta nat 1969; 73: lumgart L, Fong Y. Surgery of the liver and biliary tract. New York, NY: Saunders, 2000: Thomas PG, aer HU, Matthews J, Gertsch P, lumgart LH. Post-operative hepatic necrosis due to reduction in hepatic arterial blood flow during surgery for chronic biliary obstruction. Dig Surg 1990; 7: Kemeny N, Huang Y, Cohen M, et al. Hepatic arterial infusion of chemotherapy after resection of hepatic metastases from colorectal cancer. N Engl J Med 1999; 341: W19