Ann Surg Oncol (2010) 17:186–193 DOI 10.1245/s10434-009-0757-1
EDUCATIONAL REVIEW – PANCREATIC TUMORS
Vascular Anomalies Encountered During Pancreatoduodenectomy: Do They Influence Outcomes? Parul J. Shukla, MS, FRCS1, Savio G. Barreto, MS3, Aniruddha Kulkarni, MD2, Ganesh Nagarajan, MS1, and Abe Fingerhut, MD, FACS, FRCS4,5 Department of Gastrointestinal Surgical Oncology, Tata Memorial Hospital, Mumbai, India; 2Department of Radiodiagnosis, Tata Memorial Hospital, Mumbai, India; 3Department of General and Digestive Surgery, Flinders Medical Centre, Adelaide, Australia; 4Department of Gastrointestinal Surgery, Centre Hospitalier Intercommunal, Poissy, France; 5 Department of Surgery, University of Athens, Hippokration Hospital, Athens, Greece 1
ABSTRACT Background. Because of the potential risk of hemorrhage or ischemia, the presence of vascular anomalies adds to the surgical challenge in pancreatoduodenectomy (PD). Objective. To analyze the literature concerning the influence of aberrant peripancreatic arterial anatomy on outcomes of PD. Materials and Methods. A systematic search using Medline and Embase for the years 1950–2008. Results. The most common aberration in hepatic arterial anatomy is the replaced right hepatic artery. Other vascular abnormalities such as replaced common hepatic artery with a hepatomesenteric trunk and celiomesenteric trunk and arcuate ligament syndrome leading to celiac artery stenosis are also associated with post-PD complications. Damage to the biliary branches of the hepatic arteries increases the risk of postoperative biliary anastomotic leak. Conclusion. The most common abnormalities of the hepatic vasculature include a replaced RHA, replaced LHA, and accessory RHA or LHA. Celiac artery stenosis secondary to median arcuate ligament compression may also be encountered. Every attempt should be made to preserve the aberrant vessel unless their resection is oncologically indicated. Routine preoperative computerized tomography angiography helps to identify the hepatic vascular anatomy and thereby prepares the surgeon to better deal with the vascular anomalies intraoperatively. Increased awareness of the vascular anatomy would decrease the chances of
intraoperative vascular injury and consequent postoperative complications such as biliary anastomotic leaks as well as the chances of postoperative hemorrhage.
Intraoperative or postoperative hemorrhage remains a major determinant of morbidity and mortality in pancreatic resections.1–3 Vascular anomalies in the peripancreatic region including the hepatic artery and superior mesenteric artery as well as the celiac artery have been reported in literature, and add to the surgical challenge in pancreatoduodenectomy (PD) by not only altering the surgical approach and interfering with the resection but also the reconstruction of the pancreatic remnant.4–20 However, not all vascular anomalies of the hepatic artery affect the course of the operation. Anomalies such as an accessory hepatic artery or a replaced left hepatic artery are such examples. It thus appears pertinent that recognition of such aberrations in the vascular anatomy is essential to the surgeon when performing a PD. It would also be helpful if these aberrations could be delineated preoperatively as this would help to better prepare the surgeon to deal with the problem intraoperatively. This review aims at revisiting the types of vascular anomalies reported in the peripancreatic vascular tree, underlining the reported challenges encountered intraoperatively and how to manage these problems, and finally provides an update on preoperative radiological investigations available to detect such lesions.
Ó Society of Surgical Oncology 2009 First Received: 11 May 2009; Published Online: 17 October 2009 P. J. Shukla, MS, FRCS e-mail:
[email protected]
MATERIALS AND METHODS A systematic search of the scientific literature was carried out using Medline and Embase for the years
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1950–2008 to obtain access to all publications involving the various factors related to the aberrant vascular anatomy and outcomes of PD and also the detection of these anomalies. The search strategy was that described by Dickersin and colleagues21 with the appropriate specific search terms for ‘‘pancreatoduodenectomy,’’ ‘‘pancreaticoduodenectomy,’’ ‘‘hemorrhage,’’ ‘‘aberrant,’’ ‘‘vascular anatomy,’’ ‘‘hepatic artery,’’ ‘‘superior mesenteric artery,’’ ‘‘celiac artery,’’ ‘‘complications,’’ ‘‘angiography,’’ ‘‘computed tomography,’’ ‘‘pancreas’’, ‘‘hemorrhage,’’ ‘‘morbidity,’’ ‘‘mortality.’’
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that traverses the inferior border of the pancreas. The arteria pancreatica magna and the dorsal pancreatic artery are branches of the splenic artery lying dorsal to the pancreas. RESULTS Fifty-two articles were retrieved using the described search strategy and all 52 articles were analyzed in the review. Table 1 provides a summary of the literature search. Variations in Hepatic Arteries
Normal Peripancreatic Arterial Anatomy with the Reported Variations The classical hepatic arterial anatomy, as described by Covey et al., Hiatt et al., Koops et al., and Michels, entails the celiac artery originating from the abdominal aorta and then undergoing a trifurcation into the hepatic, splenic, and left gastric arteries.7,11,22–24 The common hepatic artery (CHA), traveling along the posterosuperior border of the pancreas, gives out the gastroduodenal artery (GDA), after which it is referred to as the proper hepatic artery. The proper hepatic artery then bifurcates into the right (RHA) and left hepatic (LHA) arteries. Thus we see (Fig. 1) that all the branches of the hepatic artery arise above the superior border of the pancreas. The superior pancreaticoduodenal artery derives from the GDA. The superior mesenteric artery (SMA) originates from the abdominal aorta and gives out the inferior pancreaticoduodenal artery
The hepatic arterial system has been found to display a variant anatomy in 55–79% of patients.7,11,23,24 Replaced RHA The most common variation in the hepatic arterial anatomy is the replaced (the artery does not arise from the celiac axis) RHA arising from the SMA. This has been reported to occur in 11–21% of patients.4,11,25 These vessels usually pass lateral and behind the portal vein and enter the hepatoduodenal ligament posterolateral to the bile duct and can be felt in this location when palpating the structures at the porta with the finger in the foramen of Winslow. However, there have been reports of such vessels traveling behind or through the head of the pancreas, in which case they are susceptible to damage.26 Kim et al., in their report demonstrating poor outcomes for patients with aberrant vascular anatomy and
TABLE 1 Summary of the literature search
Articles identified and screened for retrieval n=52
Articles retrieved for more detailed evaluation n=52
Articles included in the review n=52
FIG. 1 Three-dimensional reconstruction using CT angiography showing the normal peripancreatic arterial anatomy
Type of articles: Prospective cohort studies= 10 Retrospective cohort studies = 17 Case series and Case Reports = 19 Review articles = 4 Book chapter = 1 Educational article = 1
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intraoperative vascular complications, found 2 patients with replaced RHA out of 180 patients.27 In one of these patients the RHA was accidentally transected, while in the other patient there was an accidental portal vein injury. The danger in case of injury to a replaced RHA is its effect on the liver and more so the bile duct vascularity with the attendant risk of a leak in the bilioenteric anastomosis, as noted by Biehl et al.26 and Traverso et al.28 This is because the RHA is the chief source of blood supply to the bile duct. Replaced LHA This variation, also referred to as the type 2 variant in the Michels classification, is characterized by the LHA originating from the left gastric artery (LGA) and is seen in 3.8–10% of patients.7,11,22–24 A replaced LHA is easily identified intraoperatively as a prominent vessel running in the lesser omentum anterior to the caudate lobe and entering the liver at the base of the round ligament. It usually does not interfere with resection or reconstruction.20 Replaced RHA and LHA (Type 4 According to Michels)23,24 Exceedingly rare is the coexistence of a replaced RHA and LHA. There are no reports of such occurrences in literature by pancreatic surgeons. Intraoperatively this would be detected by the palpating replaced RHA passing lateral and behind the portal vein and entering the hepatoduodenal ligament posterolateral to the bile duct and coexistent with a prominent replaced LHA running in the lesser omentum anterior to the caudate lobe and entering the liver at the base of the round ligament.
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behind the head of pancreas and then lying medial to the common bile duct in the usual location of the GDA (already defined above).6,12,19 Volpe et al. as well as Woods et al. were able to preserve the replaced CHA lying in the location of the GDA owing to the preoperative angiogram suggesting the true nature of the vessel.6,19 Less common origins of a replaced CHA are from the LGA (Michels type 10) and the aorta.11 Owing to its origin to the left, such an anomaly would not commonly interfere with a pancreatic resection and reconstruction. Quadrifurcation of the Proper Hepatic Artery Such an aberrancy of the hepatic arterial anatomy in which the proper hepatic artery gives rise to four vessels, viz., the RHA, LHA, right accessory hepatic artery, and an intermediate branch, has been described by Adamathwaite et al.31 In this report, pylorus-preserving PD was completed after carefully identifying and dissecting the hepatic artery and its four branches. Variations of the Superior Mesenteric Artery and Celiac Trunk Hepatomesenteric Trunk (HMT) Furukawa et al. identified such an anomaly and preserved the vessels by dividing the pancreatic parenchyma.12 The authors have also encountered a HMT (Fig. 2). Although the vessel had been detected preoperatively on computed tomography (CT) and had even been preserved intraoperatively, the patient postoperatively developed delayed hemorrhage from a
Accessory RHA and/or LHA (Types 6, 5, and 7 According to Michels)23,24 As the name implies, these vessels arise from the SMA or LGA, respectively, and occur in addition to the RHA and LHA that are normal in origin and location. They are seen in 0.8–8% patients.4,25 They course along the paths of the replaced vessels and, on dissecting, the vessel is found to be accessory in the presence of the native RHA or LHA running along its normal course. Injury to these vessels is not associated with any major problems. Replaced CHA The replaced CHA arises from the SMA by a common trunk referred to as the hepatomesenteric trunk (HMT) and has been classified as type 9 by Michels.23,24 The incidence of such an anomaly has been reported in literature to range from 0.4% to 4.5%.4,9,12,14,29,30 Accidental ligation of this vessel can lead to ischemia of the bilioenteric anastomosis and a consequent leak as noted by Biehl et al.26 A similar incident has been reported by Traverso et al. where the patient developed a biliary anastomotic leak and sepsis and eventually died.28 The course of a replaced CHA arising from the SMA has been reported to be variable. The common courses include: running in or along the ventral surface of the pancreas, through the pancreatic parenchyma, or ascending
FIG. 2 Three-dimensional reconstruction using CT angiography showing the hepatomesenteric trunk (indicated by white arrow)
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pseudoaneurysm secondary to a postoperative pancreatic fistula. The aneurysm was successfully embolized and the patient improved with conservative management. Celiomesenteric Trunk (CMT) It is very rare for the celiac artery and superior mesenteric artery (SMA) to arise as a common trunk from the aorta.32 According to literature, this anomaly (referred to as a celiomesenteric trunk) is reported to occur in up to 2.7% of individuals based on cadaveric dissections.33 Anomalies at the Celiac Axis Origin (Including Celiac Artery Stenosis) Arcuate Ligament Syndrome (ALS) Celiac artery stenosis has been reported to be present in 2–7.6% of patients undergoing pancreatoduodenectomy.34–37 In this condition, the blood flow at the origin of the celiac axis is reduced due to external compression (median arcuate ligament, or enlarged lymph nodes) or internal occlusion (atherosclerotic plaque). This results in the development of major collateral pathways (pancreaticoduodenal arcades or the dorsal pancreatic artery) which arise from the SMA, resulting in the feeding of the branches of the CHA through retrograde flow via the GDA or the arc of Buhler.16,38,39 Thus, ligation of the GDA in such a patient can potentially lead to ischemia of the liver, stomach, and spleen besides predisposing to an increased risk of post-PD morbidity.16,17,36,40–45 The median arcuate ligament is a fibrous arch that unites the diaphragmatic crura on either side of the aortic hiatus and, while it normally passes cranial to the origin of the celiac axis, in 10–24% patients it may pass at the level of the origin of the celiac axis, leading to a compression of the celiac axis in what is referred to as ALS.46 Bron and Redman described two types of compression based on a lateral view aortogram, viz. eccentric and concentric. ALS is the result of ‘‘eccentric’’ compression of the celiac axis origin.47 Preoperative recognition of such a lesion is clinically difficult as most patients are asymptomatic. Some patients, though, do describe symptoms consistent with ‘‘abdominal angina.’’16 Preoperative CT angiography may provide a suspicion of the existence of such an anomaly, especially in the presence of prominent collateral vessels in the peripancreatic region including a large-calibre GDA including retrograde flow through these collaterals.16,36,48 DISCUSSION PD is a complex surgical procedure associated with high morbidity and even the risk of mortality.49–52 The technical challenges in the resection and reconstruction posed by
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presence of vascular anomalies to the already formidable surgery of PD are immense. Besides, aberrant arterial anatomy in patients undergoing pancreatic surgery increases the risk of injury to the hepatic arterial supply which may result in unexpected bleeding (intra- or postoperative) or ischemia.19 Also, any damage to the hepatic artery, especially the RHA or CHA, increases the risk of biliary anastomotic leak as well as liver dysfunction manifested in the form of elevations in hepatic enzymes, usually with no long-term consequences. In the 25–75% of patients in whom the dominant hepatic blood supply is from the hepatic arteries, it may lead to liver failure.53 Additionally, excessive handling of a vessel could potentially damage the vessel adventitia, increasing the chances of pseudoaneurysm formation in the event of a post-PD pancreatic anastomotic leak. The all-important factor in the management of vascular anomalies associated with pancreatic resections is recognition of the anomaly. The surgeon dealing with an anomalous vessel interfering with the pancreatic resection or reconstruction is faced with three options: ligation, dissection and traction away from the site of dissection, or division and anastomosis. Detection of such anomalies can be preoperative or intraoperative. Forewarning in the form of clues provided by preoperative imaging can help better preparation and planning for the surgical team. Intraoperatively, however, not all vascular aberrations are easily diagnosed. Traditionally, spiral CT scan was the preferred modality for preoperative imaging of pancreatic lesions. The advent of the multidetector row CT (MDCT) scan, with as well as without the capability for postprocessed volume-rendered images, has enhanced delineation of the pancreatic lesion and vascular structures.25,54,55 Covey et al., based on their prospective study of 600 patients and using an arterial anatomy database, were able to demonstrate comparable results of digital subtraction angiography to seminal angiographic techniques using the cut film technique when analyzing hepatic arterial anatomy.22 Winston et al. confirmed the benefit of CT angiography (CTA) in the preoperative delineation of the arterial anatomy.15 Recently, studies have focused on the different phases in imaging to determine the phase that would provide the best appreciation of the pancreatic lesion and the vasculature (Table 2).56–60 Brennan et al. have further described the technique of a virtual Whipple using CTA images that are postprocessed volume-rendered so as to aid preoperative identification of vascular anomalies.61 Routine preoperative CTA would therefore help in anticipating abnormalities in the pancreatic vasculature, thus enabling better preparation to manage the abnormal vasculature intraoperatively.
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TABLE 2 Studies comparing imaging modalities with respect to delineating pancreatic tumors and vascular anatomy Author
Modality
Comparison
Conclusion
Fletcher et al.56
MDCT
Hepatic, arterial, pancreatic phases
Pancreatic phase—best mean tumor to gland attenuation difference Hepatic phase—best for vascular delineation including vascular invasion
Graf et al.57
Dual-phase helical CT
Arterial and portal venous phase
Portal venous phase—better tumor conspicuity and venous involvment Arterial phase—better for arterial delineation
Lu et al.58
Dual-phase helical CT
Pancreatic and hepatic phase
Pancreatic phase—better pancreatic, arterial and portal venous enhancement
McNulty et al.59
MDCT
Pancreatic parenchymal, portal and arterial phase
Combination of pancreatic parenchymal and portal venous phases are better for pancreatic parenchymal and peripancreatic vascular enhancement Arterial phase—useful when CT angiography is required
Boland et al.60
Dual phase helical CT
Pancreatic and portal venous phase
Pancreatic phase—better for delineation of tumor and peripancreatic vascular structures
Whether the aberrant vascular anatomy is discovered pre- or intraoperatively, knowledge of the vascular anatomy helps in dealing with the aberrant vessel. An early step in every PD should be a conscious attempt to define the vascular anatomy. After complete kocherization of the duodenum and opening the pars flaccida, the surgeon should palpate the porta hepatis to determine the location of the arterial pulsation. Any variation from the normal location of the pulsation of the proper hepatic artery in the left lateral edge of the hepatoduodenal ligament should raise suspicion of aberrant anatomy. Presence of a prominent vessel in the pars flaccida is most likely a replaced/accessory LHA, which ideally should not interfere with the resection or reconstruction. Palpation of the arterial pulse/thrill behind the head of the pancreas or higher behind the portal vein and the common bile duct with a palpable pulse in the left lateral edge of the pancreas would indicate the presence of replaced RHA. The ‘‘proper hepatic artery’’ in these patients would appear smaller than normal. On the other hand, a similar finding with an absent pulse in the free lateral edge of the hepatoduodenal ligament would imply a replaced CHA. The replaced CHA may also course within the substance of the head of the pancreas or ventral to the head of the pancreas. Here it should be differentiated from a GDA by the fact that it fails to taper as it approaches the right gastroepiploic artery.6 A replaced RHA should generally be recognized and preserved. Should the vessel need to be divided at its origin for oncological reasons, the distal end should be anastomosed to the LHA or the aorta.20,62 In the case of a replaced CHA that courses ventral to the pancreas, the vessel should be carefully dissected and preserved. Should the vessel lie within the head of the pancreas, Furukawa et al. had suggested dividing the
pancreatic head to salvage the vessel.12 However, this is not recommended in a pancreatic head malignancy, in which case there are three options:(1) If the anomaly is detected preoperatively, an embolization of the vessel can be performed with microcoils, as shown by Miyamoto et al.10 (2) If detected intraoperatively, the artery may be divided and reconstructed. This, however, increases the risk of postoperative hemorrhage in the event of a pancreatic anastomotic leak. (3) Another option is to clamp the artery, check for pulsations, and visualize the hepatic blood flow using Doppler ultrasonography, as recommended by Yamamoto et al.63 A CMT usually presents as a large-caliber vessel coursing across the ventral surface of the neck of the pancreas. Applying a bulldog vascular clamp across the vessel would lead to marked reduction in the flow of blood to the hepatic arteries that are palpable in the free edge of the hepatoduodenal ligament. The vessel may then be dissected off and preserved, although it may need to be looped away during the resection and reconstruction. If celiac axis stenosis is suspected based on preoperative imaging or appreciated intraoperatively by the presence of dilated collateral vessels and a prominent GDA, the first step would be to dissect out the origin of the celiac artery and check for the presence of a compressing extrinsic structure. A compressing median arcuate ligament can be divided and is helpful in patients with ‘‘eccentric’’ compression of the vessel that was obviously due to the ligament. In patients with ‘‘concentric’’ compression, division of the median arcuate ligament may not be sufficient.64 Another important step after division of the median arcuate ligament, or in patients in whom an extrinsic cause may not be identified, is described by Bull et al. and involves clamping the GDA with a vascular clamp, checking the pulsations in the CHA, and noting the
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appearance of the liver.65 Nara et al. have described an additional step of using Doppler ultrasonography to study the hepatic vascular flow in these patients.66 In patients with a dampened flow following clamping of the GDA, an arterial reconstruction was advised by Nara et al. so as to reduce the chances of ischemic complications postoperatively.66 Opinion on the need for further vascular reconstruction in such patients is divided. Some surgeons feel that division of an arcuate ligament band or the sympathetic neural fibers (in patients in whom a hypertrophic celiac ganglion is compressing the celiac axis) is all that may be needed and the collateral blood supply is sufficient to maintain perfusion.34,35,40–42,67 However, other surgeons feel that some form of vascular reconstruction is needed to prevent any ischemic catastrophe postoperatively, especially in patients with decreased flow through the CHA following clamping of the GDA.43,68–70 The various procedures described as part of the vascular reconstruction for celiac axis stenosis include aortohepatic bypass, celiac artery reimplantation, use of autogenous vein graft from iliac artery to splenic artery, splenomesenteric anastomosis, venous grafts between the aorta and the celiac tributaries, and saphenous vein graft as a conduit between the common hepatic artery and the aorta.36,43,69–71 Takach et al. have described different procedures for this condition and believe that the choice of procedure should be tailored to the operative findings.68 They advise division of the median arcuate ligament or sympathetic neural fibers in all patients (depending on their presence) followed by aortoceliac bypass with a polytetrafluoroethylene or a vein graft, angioplasty using a knitted polyester fiber patch, or aortic reimplantation of the celiac artery. CONCLUSION The most common abnormalities of the hepatic vasculature include replaced RHA (11–21%), replaced LHA (3.8– 10%), accessory RHA or LHA (0.8–8%), and celiac artery stenosis (2–7.6%). CTA helps to clearly delineate the vascular anatomy preoperatively, which would help the surgeon by anticipation of a vascular anomaly. Every attempt should be made to carefully dissect and preserve anomalous vessels unless their division or resection is dictated by the need to obtain oncological clearance. In the case of celiac artery stenosis, management should be tailored according to operative findings. Routine division of the offending arcuate ligament or sympathetic nerve fibers form a hypertrophic celiac ganglion should be performed, followed by clamping of the GDA and Doppler ultrasonography of the CHA and left gastric vessels. Evidence of markedly decreased flow in these vessels or appearances of gross ischemia should prompt the need for vascular reconstruction. Increased
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