Background: Simultaneous injury to the common bile duct and hepatic artery is an increasingly recognized complication of laparoscopic cholecystectomy (LC). The impact of an associated arterial injury in patients with an iatrogenic bile duct injury (BDI) remains debatable, although it is claimed to increase the risk of septic complications, increase the difficulty of biliary repair and increase the risk of recurrent stricture.
Data Sources : A literature search on the clinical significance and management of a concomitant hepatic artery injury (HAI) to the outcome of biliary-enteric reconstruction following BDI was reviewed. Relevant articles were extracted through Medline, with secondary references obtained from key articles.
Conclusions: The early reported association between failure of biliary repair and arterial injuries is not confirmed by the largest studies which showed no difference in anastomotic stricture rate between patients who had an isolated BDI and those who had a combined HAI and BDI. However right arterial injury associated with liver necrosis or damage to the right hepatic duct may require right hepatectomy.
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The impact of an associated arterial injury in patients with an iatrogenic bile duct injury (BDI) remains debatable. The aim of this review is to address the issue of concomitant vascular injuries with emphasis to its clinical relevance.
With the widespread use of laparoscopic cholecystectomy (LC), the incidence of iatrogenic bile duct injury (BDI) has increased over the past decade. Despite the expertise gained worldwide in performing this procedure, the overall incidence of injury to the bile duct is approximately twice as high as that following open cholecystectomy [1-3]. Because BDI sustained during LC is known to occur more proximally compared with open cholecystectomy and misidentification of the anatomy is not exclusively restricted to the biliary tree, a higher incidence of concomitant hepatic artery injury (HAI) can be anticipated [4-6].
HAI injury may accompany BDI, the commonest involving the right hepatic artery in association with an excisional injury of the common hepatic duct, due to the proximity of the artery and the duct. This association was noted by Meyers and colleagues in the early 1990s , and recent articles have expanded our knowledge of this complication [8-19]. Although simultaneous injury to the common bile duct and hepatic artery is an increasingly recognized complication of LC, the clinical significance of the associated vascular injury remains controversial. Disruption of the hepatic arterial flow is usually tolerated in an otherwise healthy patient. However, the sensitivity of the biliary tree to the deprivation of arterial blood supply is well known and might explain the pathogenesis of biliary leaks and stenosis after reconstruction of a transected common bile duct .
The aim of this review is to address the issue of concomitant vascular injuries with emphasis to its clinical relevance.
An online search of the Medline database was undertaken using the keywords 'bile duct injury', 'vascular injury', 'laparoscopic cholecystectomy', and 'outcome' in various combinations. Boolean operators AND, OR and NOT were used. No date or language restriction was used. Manual cross-referencing was performed.
The incidence of HAI in association with BDI is difficult to ascertain, as few reports on BDI mention the subject, and most series include highly selected patient populations in the context of BDI [8-19]. In addition, it is often difficult to determine the status of the right hepatic artery (RHA) during operations to repair a BDI, because the artery is often encased in inflammation resulting from tissue damage, bile collections, or infection . Furthermore, routine arterial imaging is not common place in the assessment of such injuries. As a consequence, the real incidence of concomitant vascular injury is probably underestimated.
In a multi-institutional collection of 77,604 laparoscopic cholecystectomies, Deziel et al. reported 44 cases (12%) of hepatic arterial injury in 365 patients with major bile duct injuries . In selected series the presence of concomitant injury of the hepatic artery has been reported in 12 - 47 per cent of patients with LC-related iatrogenic BDI [7,16,19,21-22]. This considerable variability in the rate of HAI seems in part related to the type of preoperative investigation used, with the diagnosis of HAI being higher in series where mesenteric angiography has been routinely performed . The most common vascular structure injured during dissection of Calot's triangle is the RHA (90%). Damage to the main hepatic artery is the second highest ranking injury (8%), while the portal vein (usually in combination with hepatic artery injury) is the third highest ranking injury, although it is considerably less common (4%) [16-17].
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HAI must be suspected in any patient with BDI referred for primary repair or refashioning of an unsuccessful primary repair. Modern magnetic resonance or computed tomography angiography are usually adequate to exclude injury to either the arterial or portal venous systems, or to identify the presence of a pseudoaneurysm that may follow sepsis or traumatic injury . Non-enhancement of the right hepatic lobe during the arterial phase of a contrast CT scan is usually the most common radiological feature suggesting an HAI  (Figure 1). Duplex ultrasonography is often unreliable, but is useful in the intraoperative assessment of the hepatic vasculature .
Although some authors support the routine use of preoperative mesenteric angiography in patients with BDI , most centres now limit the use of this invasive investigation to patients with arterial occlusion suspected by non-invasive diagnostic procedures [13-16,19] (Figure 2). Vascular assessment is particularly important if there has been a previous attempt at repair and in the management of more proximal injuries, which may be associated with damage to the RHA .
Initial symptoms may be nonspecific; typically related to the effects of biliary leak or biliary obstruction rather than due to vascular-related complications . The clinical presentation of patients with and without arterial injuries is comparable [17,19]. Alves et al. reported that approximately one third of patients had their HAI identified at the time of cholecystectomy (usually after conversion) , with the remaining patients having the injury identified in the early postoperative period if there was a bile leak, or later if they presented with jaundice. Presenting symptoms, timing of diagnosis and number of previous attempts at treatment were comparable in patients with and without an arterial injury.
Specific early symptoms related to arterial injury have been reported sporadically and may include bleeding, haemobilia, acute hepatic insufficiency, and sepsis related to right lobe atrophy, necrosis and abscess formation [11-14]. Macroscopic ischemic changes of the liver can be noticed as early as the fourth day after the arterial injury . Development of hepatic ischaemia was reported in 11-67 per cent of patients with concurrent RHA and BDI in recent studies [11-18].
Hepatic artery pseudoaneurysm is a rare complication of LC, variably occurring in the early or late postoperative period and may cause gastrointestinal or intraperitoneal bleeding . Pseudoaneurysm complicating LC frequently affects the RHA, but may be confined to the cystic artery remnant. However, these lesions are usually amenable to angiographic management, with low related morbidity and favourable long-term results .
Several classifications of bile duct injury have been proposed, but there is no universally accepted standard. However, the only classification of laparoscopic bile duct injuries which incorporates concomitant vascular injury according to the mechanism of injury is the Stewart-Way classification .
Mechanisms of injury and prevention
A high risk of concurrent vascular injury in patients with proximal bile duct injury has been confirmed in recent analyses of LC-related complications [12-18]. The RHA is at risk during LC, as it is present in Calot's triangle in 82% of occasions, and may therefore be mistaken for the cystic artery and thus ligated .
Stewart et al. described how the right hepatic duct could be mistaken for the cystic duct, and the RHA for the cystic artery, which accounts for the most common pattern of injury . During operations that result in injury of the common hepatic duct or right hepatic duct, the RHA is in a position to be injured or, if the artery is seen, it may be misidentified as the cystic artery. The common bile duct (mistaken for the cystic duct) can be clipped and mobilized, exposing the RHA, which lies behind the common hepatic duct . The surgeon is led to believe that the RHA is actually a posterior cystic artery, and it is often clipped based on that erroneous assumption. Factors that influence the occurrence of HAI include the level of the common hepatic duct injury and the point where the RHA crosses the common hepatic duct. Similar mechanisms could result in RHA with right hepatic duct injuries because of either deliberate ligation or injury during a dissection that is too close to the right hepatic duct. These factors emphasize the importance of identifying the cystic artery, following its course to the gallbladder wall, and clipping it close to the gallbladder, even if this entails clipping anterior and posterior branches of the cystic artery separately.
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Three patterns of arterial injury are noted: transection, occlusion by clips and thrombosis of the vessel . The most common type of arterial injury is transection of the RHA, usually being mistaken as the cystic artery. The hepatic artery may be injured inadvertently while attempting to control haemorrhage during the course of dissection. Bleeding encountered during LC should be addressed by tamponade rather than blindly trying to apply clips, then the bleeding vessel should be isolated and a secure clip placed precisely. If these manoeuvres are unsuccessful, conversion is indicated. Another possible cause of vessel occlusion is thrombosis of the hepatic artery, often secondary to biliary peritonitis.
Surgeons who are referred patients for biliary reconstruction with stricture, hepatic necrosis, or abscess should review prior operative notes and query the primary surgeon specifically with regard to intraoperative bleeding and how this was managed intra-operatively.
Consequences of Vascular Injury
Two arterial plexuses play an important role in maintaining adequate vascularization of the extrahepatic biliary system [27-28]. One is the arterial plexus on the surface of the common bile duct and the common hepatic duct, connecting the posterosuperior pancreaticoduodenal artery and the RHA. The other is at the hilar plate on the inferior surface of the hilum of the liver. It is formed by the collateral vessels coming from the RHA and the left hepatic artery. In patients with a major BDI and simultaneous HAI, the arterial plexus on the bile duct is totally transected, but in addition the arterial blood supply to the right liver lobe may be impaired and the hilar plate plexus might be jeopardized.
Experimental studies provide relevant information. Even though the hepatic parenchymal blood supply comes predominantly from the portal circulation, and hepatic artery ligation is usually tolerated without clinical sequelae [29-32], biliary obstruction in addition to RHA injury may predispose to the development of hepatic necrosis. Doppman et al.  demonstrated hepatic necrosis and infarction in liver segments with biliary obstruction following hepatic artery embolization. Similarly, Yoshidome et al.  noted increased susceptibility to hepatic ischemia with obstructive jaundice. Okada  and Soares and colleagues  noted that hepatic artery occlusion in the setting of obstructive jaundice caused hepatic necrosis. These data may explain the development of hepatic ischemia, necrosis, and abscess formation in patients with persistent biliary obstruction.
Early reports suggest that BDI associated with HAI typically produces severe consequences [11,14-15,18]. Buell et al. in a series of 49 bile duct injuries, reported a mortality rate of 38% in patients with HAI compared to 3% in patients with isolated bile duct injuries . Similarly, Gupta et al.  and Bachellier et al.  demonstrated that concomitant arterial injury is a crucial risk factor for postoperative liver necrosis, liver abscess formation, stenosis of the hepaticojejunostomy and late stricture within the intrahepatic biliary tract.
Schmidt et al reported that six of 11 patients (54.5%) with combined BDI and RHA injuries had biliary complications . Aside from these small series, there are anecdotal reports of patients with combined bile duct and RHA injuries during LC resulting in high mortality and severe biliary complications.
However, two significant studies do not support these findings [16, 17]. Stewart et al., in a series of 84 patients with combined BDI and HAI out of a total of 345 patients with BDI, reported that complications such as bleeding, haemobilia, hepatic abscess formation, hepatic ischemia, and need for hepatectomy were more common in patients with HAI compared with those without HAI. Nevertheless, the overall incidence of morbidity was lower (54%) than what might have been expected from the earlier studies cited above. For example, only 11% of the patients with HAI developed hepatic ischemia, and only 5% required right hepatic resections. Furthermore, the mortality rate and incidence of secondary biliary cirrhosis were unaffected by HAI. Postoperative complications were significantly more common (41%) if the biliary repair was undertaken by the primary surgeon rather than a hepatobiliary specialist (3%), supporting the view that specific surgical experience is the main determinant of surgical outcome.
Similary, Alves and colleagues evaluated prospectively a series of 55 patients, by coeliac and superior mesenteric angiography, but failed to demonstrate a negative influence of concomitant arterial injuries in the short or long term outcome after biliary injury . Neither of these studies showed any difference in anastomotic stricture rate between patients who had an isolated BDI and those who had a combined vascular and biliary injury although the numbers of patients studied was not large. Biliary complications in earlier series occurred in up to 60 per cent of patients with combined biliary and arterial injuries undergoing biliary-enteric anastomosis without arterial reconstruction [8,11-13]. In more recent series, where the repair was fashioned by employing the left hepatic duct approach, an overall success rate of 93 per cent has been achieved [16-17].
Overall there is evidence that HAI associated with BDI may increase morbidity, but in terms of long-term anastomotic stricture formation, there is no strong evidence to support a negative impact of a concomitant vascular injury; this is especially true when the repair is performed in a specialist hepatobiliary unit. In patients who are unable to undergo early repair, proximal extension of an ischaemic stricture may make repair technically more difficult.
Coexisting portal vein injuries have been sporadically reported and are associated with particularly devastating injuries as a normal portal circulation is prerequisite for recuperation of the dearterialized liver parenchyma . Portal vein thrombosis may lead to cavernous transformation of the portal vein. This increases the difficulty of later repair and may itself lead to bile duct compression.
Management depends on the timing of recognition of the arterial injury and whether there is evidence of liver injury. There is debate in the literature about whether repair of the right hepatic artery should be done. However, the limited number of patients who have had RHA reconstruction (only 7 patients in the series analyzed), does not allow definitive conclusions to be drawn. With intraoperative or early recognition (within 4 days) of RHA injury, some authors suggest arterial reconstruction to avoid hepatic necrosis, biliary-enteric anastomotic leakage and late biliary stricture [11-12, 19]. Reanastomosis using an end-to-end technique is usually possible only if the injury is related to a partial or complete transectional injury of the vessel, and is undertaken following immediate conversion to laparotomy. Vascular reconstruction using autologous venous graft or allograft has also been described [12,19]. If revascularization is not technically feasible but where the confluence of the right and left ducts is intact, a Hepp-Couinaud reconstruction using the extrahepatic portion of the left hepatic duct to ensure adequate blood supply to the hepatico-jejunostomy represents the most effective technique to avoid development of anastomotic stricture [16-17].
Other authors have suggested not attempting reconstruction of the injured artery, as RHA ligation in a non-cholestatic liver is usually tolerated without clinical sequelae owing to the portal flow and the supply of arterial blood from collateral vessels [16-17, 38]. Similarly, the excisional injury to the artery may render revascularisations impossible.
When a hepatic artery injury is identified late, HAI may influence the decision to perform liver resection at the time of biliary repair or revisional surgery if liver atrophy is present. Alves et al. reported that right hepatectomy was inevitable in 12 of 26 patients with vascular injury, 20 of whom had disruption of the RHA . The precise mechanism of atrophy is not known but may be related to the combination of arterial injury with systemic or portal hypotension seen in some patients with bile duct injury in the early post-cholecystectomy period, when sepsis or haemorrhage is poorly controlled. However, unrecognized injury to the right ductal system or poor initial repair may lead to chronic biliary obstruction, which may in turn lead to atrophy of the affected liver, particularly if it is associated with arterial injury. The absence of right lobe atrophy may signify the presence of a significant cross-circulation between the left and right hepatic artery
Portal vein injuries are usually managed by suture repair or occasional reconstruction of the occluded portal vein at the time of biliary reconstruction . These types of injuries are exceptionally rare but can be associated with fatal complications and as most references refer only to scarce case reports rather than series of patients, it is difficult to draw firm conclusions regarding their management.
In severe vascular injures, the vascular component may become the predominant feature of the injury with necrosis of the intrahepatic biliary system, similar to that seen when the hepatic artery thromboses after liver transplantation, or even hepatic infarction. Infarction of the intrahepatic biliary tree requires liver transplantation, while hepatic infarction may lead to the need for hepatic resection or transplantation [39-40]. Difficult right hepatic duct repair when biliary injury is associated with RHA damage may account for the much higher rate of complications involving the right liver and may therefore be best treated by right hepatectomy . Based on the available data, a general treatment algorithm is proposed in Figure 3.
In the laparoscopic era, BDI tend to be located more proximally compared to those observed in open surgical era and vascular injuries occur more often than believed in the past. The early reported association between failure of biliary repair and arterial injuries may simply reflect that HAI is more common among high biliary injuries, and high biliary injuries are also more difficult to repair. However, as patients with an arterial injury are more likely to have ischemic biliary mucosa, there is a higher risk of stricture formation if the anastomosis is performed below the biliary confluence. Long term outcome of patients with and without hepatic artery injury is comparable as long as the Hepp-Couinaud technique is used to perform the biliary repair at the hilar level and onto the left hepatic duct. The discovery of a simple disruption of the right branch of the hepatic artery should not affect management if a Hepp-Couinaud biliary repair is performed. Evidence of atrophy of the right liver lobe or severe stricturing of the right hepatic duct precluding repair, may indicate the need for right hepatic resection. When the HAI is identified early, there may be an option for repair, although this is controversial; in delayed cases it seems reasonable to ignore the vascular injury. Early referral to a specialist hepatobiliary centre, without attempting repair, is recommended.
- Roslyn JJ, Binns GS, Hughes EF, et al. Open cholecystectomy: a contemporary analysis of 42 474 patients. Ann Surg 1993; 218: 129-137.
- Fletcher DR, Hobbs MST, Tan P, Valinsky LJ, et al. Complications of cholecystectomy: risks of the laparoscopic approach and protective effects of operative cholangiography: a population-based study. Ann Surg 1999; 229: 449-457.
- Adamsen S, Hansen OH, Funch-Jensen P, et al.. Bile duct injury during laparoscopic cholecystectomy: a prospective nationwide series. J AmColl Surg 1997; 184: 571-578.
- Strasberg SM, Hertl M, Soper NJ. An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg 1995;189:101- 25.
- Chaudhary A, Manisegran M, Chandra A, et al.. How do bile duct injuries sustained during laparoscopic cholecystectomy differ from those during open cholecystectomy? J Laparoendosc Adv Surg Tech 2001;4:187-91.
- Bergman JJ, van den Brink GR, Rauws EAJ, , et al. Treatment of bile duct lesions after laparoscopic cholecystectomy. Gut 1996;38: 141-7.
- Davidoff AM, Pappas TN, Murray EA, et al. Mechanisms of major biliary injury during laparoscopic cholecystectomy Ann Surg 1992; 215: 196-202.
- Madariaga JR, Dodson SF, Selby R, et al. Corrective treatment and anatomic considerations for laparoscopic cholecystectomy injuries. J Am Coll Surg 1994; 179: 321-325.
- Holbert BL, Baron RL, Dodd GD. Hepatic infarction caused by arterial insufficiency: spectrum and evolution of CT findings. Am J Gastroenterol 1996; 166: 815.
- Smith GS, Birnbaum BA, Jacobs JE. Hepatic infarction secondary to arterial insufficiency in native livers: CT findings in 10 patients. Radiology 1998; 208: 223-229.
- Gupta N, Solomon H, Fairchild R, Kaminski D: Management and outcome of patients with combined bile duct and hepatic artery injuries. Arch Surg 1998; 133: 176-181.
- Bachellier P, Nakano H, Weber JC, et al.. Surgical repair after bile duct and vascular injuries during laparoscopic cholecystectomy: when and how? World J Surg 2001;25: 1335-1345.
- Koffron A, Ferrario M, Parsons W, et al. Failed primary management of iatrogenic biliary injury: incidence and significance of concomitant hepatic arterial disruption. Surgery 2001; 130: 722-731.
- Buell JF, Cronin DC, Funaki B, , et al: Devastating and fatal complications associated with combined vascular and bile duct injuries. Arch Surg 2002; 137: 703-710.
- Bilge O, Bozkiran S, Ozden I, et al. The effect of concomitant vascular disruption in patients with iatrogenic biliary injuries. Langenbecks Arch Surg 2003; 388: 265-269.
- Stewart L, Robinson TN, Lee CM, et al. Right hepatic injury associated with laparoscopic bile duct injury: Incidence, mechanism and consequences. J Gastrointest Surg 2004;8: 523-531.
- Alves A, Farges O, Nicolet J, et al. Incidence and consequence of an hepatic artery injury in patients with postcholecystectomy bile duct strictures. Ann Surg 2003; 238: 93-96.
- Schmidt SC, Settmacher U, Langrehr JM, Neuhaus P. Management and outcome of patients with combined bile duct and hepatic arterial injuries after laparoscopic cholecystectomy. Surgery 2004; 135: 613-618.
- Li J, Frilling A, Nadalin S, et al. Management of concomitant hepatic artery injury in patients with iatrogenic major bile duct injury after laparoscopic cholecystectomy. Br J Surg. 2008 ;95(4):460-5
- Terblanche J, Allison HF, Northover JMA. An ischemic basis for biliary strictures. Surgery 1993;94:52-7.
- Deziel DJ, Millikan KW, Economou SG, et al. Complications of laparoscopic cholecystectomy: A national survey of 4,292 hospitals and an analysis of 77,704 cases. Am J Surg 1993;165:9-14.
- Chapman WC, Halevy A, Blumgart LH, Benjamin IS. Postcholecystectomy bile duct strictures. Management and outcome in 130 patients. Arch Surg 1995; 130: 597-602.
- Connor S, Garden OJ. Bile duct injury in the era of laparoscopic cholecystectomy. Br J Surg 2006; 93: 158-168.
- Nicholson T, Travis S, Ettles D, et al. Hepatic artery angiography and embolization for hemobilia following laparoscopic cholecystectomy. Cardiovasc Intervent Radiol 1999; 22: 20.
- Tessier DJ, Fowl RJ, Stone WM, et al. Iatrogenic hepatic artery pseudoaneurysms: an uncommon complication after hepatic, biliary, and pancreatic procedures. Ann Vasc Surg. 2003 Nov;17(6):663-9.
- Gray S, Skandalakis J. Atlas of Surgical Anatomy for General Surgeons. Baltimore:Williams & Wilkins, 1985.
- Stapleton GN, Hickman R, Terblanche J. Blood supply of the right and left hepatic ducts. Br J Surg 1998; 85: 202-207.
- Vellar ID. The blood supply of the biliary ductal system and its relevance to vasculobiliary injuries following cholecystectomy. Aust N Z J Surg 1999; 69: 816-820.
- Allison DJ, Jordan H, Hennessy O. Therapeutic embolisation of the hepatic artery: A review of 75 procedures. Lancet 1985; 1:595-599.
- Sheldon GF, Rutledge R. Hepatic trauma. Adv Surg 1989;22: 179-193.
- Mays ET, Wheeler CS. Demonstration of collateral arterial flow after interruption of hepatic arteries in man. N Engl J Med 1974;290:993-996.
- Bengmark S, Rosengren K. Angiographic study of the collateral circulation to the liver after ligation of the hepatic artery in man. Am J Surg 1970;119:620-624.
- Doppman JL, Girton M, Vermess M. The risk of hepatic artery embolization in the presence of obstructive jaundice. Radiology 1982;143:37-43.
- Yoshidome H, Miyazaki M, Shimizu H, et al. Obstructive jaundice impairs hepatic sinusoidal endothelial cell function and renders liver susceptible to hepatic ischemia/reperfusion. J Hepatol 2000;33:59-67.
- Okada Y. Experimental study on the interruption of hepatic blood flow in obstructive jaundice, with special reference to the causes of death and prolonged jaundice after biliary decompression. Nippon Geka Hokan 1989;58:275-288.
- Soares AF, Castro e Silva Junior O, Ceneviva R, et al. Biochemical and morphological changes in the liver after hepatic artery ligation in the presence or absence of extrahepatic cholestasis. Int J Exp Pathol 1993;74:367-370.
- Frilling A, Li J, Weber F, et al. Major bile duct injuries after laparoscopic cholecystectomy: a tertiary center experience. J Gastrointest Surg 2004; 8: 679-685.
- Halasz NA: Cholecystectomy and hepatic artery injury. Arch Surg 1991; 126: 137-138.
- Thomson BN, Parks RW, Madhavan KK, Garden OJ. Liver resection and transplantation in the management of iatrogenic biliary injury. World J Surg. 2007 Dec;31(12):2363-9.
- Laurent A, Sauvanet A, Farges O, et al. Major hepatectomy for the treatment of complex bile duct injury. Ann Surg. 2008 ;248(1):77-83.