Ischemic Cholangiopathy

ABSTRACT

Bile ducts are supplied with blood exclusively via hepatic arteries. Obstruction of large arteries is rapidly compensated for by the opening of preexisting intrahepatic or transcapsular collateral arteries, which prevents ischemic damage. Ischemic bile duct injury may occur when small hepatic arteries or the peribiliary vascular plexus are injured, or when all possible arterial blood supplies are interrupted, as is the case in transplanted liver with hepatic artery thrombosis. Most causes of bile duct ischemia are iatrogenic. Systemic diseases involving small hepatic arteries may also be implicated. Depending on the extent and velocity of the arterial obstructive process, ischemic cholangiopathy may present as acute formation of biliary casts, bile duct necrosis, or chronic disease resembling primary sclerosing cholangitis. In many patients, correction of arterial obstruction is not possible. When biliary drainage or reconstruction is not possible or has failed, liver transplantation is the only means of providing potential cure.

KEYWORDS

Ischemic cholangitis - peribiliary plexus - hepatic artery thrombosis - liver transplantation - hereditary hemorrhagic telangiectasia

REFERENCES

• 1 Sherlock S. Overview of chronic cholestatic conditions in adults: terminology and definitions.  Clin Liver Dis. 1998;  2 217-233 vii
• 2 Deltenre P, Valla D C. Ischemic cholangiopathy.  J Hepatol. 2006;  44 806-817
• 3 Batts K P. Ischemic cholangitis.  Mayo Clin Proc. 1998;  73 380-385
• 4 Northover J M, Terblanche J. A new look at the arterial supply of the bile duct in man and its surgical implications.  Br J Surg. 1979;  66 379-384
• 5 Takasaki S, Hano H. Three-dimensional observations of the human hepatic artery (arterial system in the liver).  J Hepatol. 2001;  34 455-466
• 6 Ekataksin W, Zou Z Z, Wake K et al.. The hepatic microcirculatory subunits: an over-three-century-long search for the missing link between an exocrine unit and an endocrine unit in mammalian liver nodules. In: Motta PM Recent Advances in Microscopy of Cells, Tissues and Organs. Rome; University of Rome La Sapienza Press 1997: 375-380
• 7 Mays E T. Observations and management after hepatic artery ligation.  Surg Gynecol Obstet. 1967;  124 801-807
• 8 Kim D K, Kinne D W, Fortner J G. Occlusion of the hepatic artery in man.  Surg Gynecol Obstet. 1973;  136 966-968
• 9 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
• 10 Redman H C, Reuter S R. Arterial collaterals in the liver hilus.  Radiology. 1970;  94 575-579
• 11 Mays E T, Wheeler C S. Demonstration of collateral arterial flow after interruption of hepatic arteries in man.  N Engl J Med. 1974;  290 993-996
• 12 Koehler R E, Korobkin M, Lewis F. Arteriographic demonstration of collateral arterial supply to the liver after hepatic artery ligation.  Radiology. 1975;  117 49-54
• 13 Fisher A, Miller C H. Ischemic-type biliary strictures in liver allografts: the Achilles heel revisited?.  Hepatology. 1995;  21 589-591
• 14 Demachi H, Matsui O, Takashima T. Scanning electron microscopy of intrahepatic microvasculature casts following experimental hepatic artery embolization.  Cardiovasc Intervent Radiol. 1991;  14 158-162
• 15 Demachi H, Matsui O, Kawamori Y, Ueda K, Takashima T. The protective effect of portoarterial shunts after experimental hepatic artery embolization in rats with liver cirrhosis.  Cardiovasc Intervent Radiol. 1995;  18 97-101
• 16 Fouassier L, Beaussier M, Schiffer E et al.. Hypoxia-induced changes in the expression of rat hepatobiliary transporter genes.  Am J Physiol Gastrointest Liver Physiol. 2007;  293 G25-G35
• 17 Wagner M, Zollner G, Trauner M. Ischemia and cholestasis: more than (just) the bile ducts!.  Transplantation. 2008;  85 1083-1085
• 18 Hohn D, Melnick J, Stagg R et al.. Biliary sclerosis in patients receiving hepatic arterial infusions of floxuridine.  J Clin Oncol. 1985;  3 98-102
• 19 Shea Jr W J, Demas B E, Goldberg H I et al.. Sclerosing cholangitis associated with hepatic arterial FUDR chemotherapy: radiographic-histologic correlation.  AJR Am J Roentgenol. 1986;  146 717-721
• 20 Aldrighetti L, Arru M, Ronzoni M et al.. Extrahepatic biliary stenoses after hepatic arterial infusion (HAI) of floxuridine (FUdR) for liver metastases from colorectal cancer.  Hepatogastroenterology. 2001;  48 1302-1307
• 21 Terblanche J, Allison H F, Northover J M. An ischemic basis for biliary strictures.  Surgery. 1983;  94 52-57
• 22 Valente J F, Alonso M H, Weber F L, Hanto D W. Late hepatic artery thrombosis in liver allograft recipients is associated with intrahepatic biliary necrosis.  Transplantation. 1996;  61 61-65
• 23 Abbasoglu O, Levy M F, Vodapally M S et al.. Hepatic artery stenosis after liver transplantation–incidence, presentation, treatment, and long term outcome.  Transplantation. 1997;  63 250-255
• 24 Siegel J H, Ramsey W H. Endoscopic biliary stent placement for bile duct stricture after hepatic artery infusion of 5-FUDR.  J Clin Gastroenterol. 1986;  8 673-676
• 25 Gelbmann C M, Rummele P, Wimmer M et al.. Ischemic-like cholangiopathy with secondary sclerosing cholangitis in critically ill patients.  Am J Gastroenterol. 2007;  102 1221-1229
• 26 Ludwig J, Kim C H, Wiesner R H, Krom R A. Floxuridine-induced sclerosing cholangitis: an ischemic cholangiopathy?.  Hepatology. 1989;  9 215-218
• 27 Pettavel J, Gardiol D, Bergier N, Schnyder P. Fatal liver cirrhosis associated with long-term arterial infusion of floxuridine.  Lancet. 1986;  2 1162-1163
• 28 Dikengil A, Siskind B N, Morse S S et al.. Sclerosing cholangitis from intraarterial floxuridine.  J Clin Gastroenterol. 1986;  8 690-693
• 29 Pitre J, Houssin D, Louvel A et al.. Ectasing cholangitis and secondary biliary cirrhosis following intra-arterial hepatic chemotherapy. Treatment by liver transplantation.  Gastroenterol Clin Biol. 1991;  15 350-354
• 30 Makuuchi M, Sukigara M, Mori T et al.. Bile duct necrosis: complication of transcatheter hepatic arterial embolization.  Radiology. 1985;  156 331-334
• 31 Richardet J P, Lons T, Sibony M et al.. Secondary sclerosing cholangitis and chemo-embolization with lipiodol.  Gastroenterol Clin Biol. 1994;  18 168-171
• 32 Hasegawa K, Kubota K, Aoki T et al.. Ischemic cholangitis caused by transcatheter hepatic arterial chemoembolization 10 months after resection of the extrahepatic bile duct.  Cardiovasc Intervent Radiol. 2000;  23 304-306
• 33 Iwata M, Sasaki M, Harada K et al.. Intrahepatic cholangitis and arteritis after transcatheter arterial embolization in a patient with tumor-like lesion-associated autoimmune hepatitis.  Pathol Res Pract. 2001;  197 59-63
• 34 Herrmann G, Lorenz M, Kirkowa-Reimann M, Hottenrott C, Hubner K. Morphological changes after intra-arterial chemotherapy of the liver.  Hepatogastroenterology. 1987;  34 5-9
• 35 Pettavel J. Intra-arterial chemotherapy using a pump.  Antibiot Chemother. 1988;  40 36-40
• 36 Bognel C, Degott C, Rougier P et al.. Anatomo-pathologic study of hepatic toxicity in intra-arterial hepatic chemotherapy.  Gastroenterol Clin Biol. 1989;  13 125-131
• 37 Kobayashi S, Nakanuma Y, Matsui O. Histopathology of portal tracts in livers after transcatheter arterial chemo-embolization therapy for hepatocellular carcinoma.  J Gastroenterol Hepatol. 1994;  9 45-54
• 38 Llovet J M, Real M I, Montana X et al.. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial.  Lancet. 2002;  359 1734-1739
• 39 Kemeny N, Daly J, Reichman B et al.. Intrahepatic or systemic infusion of fluorodeoxyuridine in patients with liver metastases from colorectal carcinoma. A randomized trial.  Ann Intern Med. 1987;  107 459-465
• 40 Chang A E, Schneider P D, Sugarbaker P H et al.. A prospective randomized trial of regional versus systemic continuous 5-fluorodeoxyuridine chemotherapy in the treatment of colorectal liver metastases.  Ann Surg. 1987;  206 685-693
• 41 Kemeny N, Daly J, Oderman P et al.. Hepatic artery pump infusion: toxicity and results in patients with metastatic colorectal carcinoma.  J Clin Oncol. 1984;  2 595-600
• 42 Daly J M, Kemeny N, Oderman P, Botet J. Long-term hepatic arterial infusion chemotherapy. Anatomic considerations, operative technique, and treatment morbidity.  Arch Surg. 1984;  119 936-941
• 43 Johnson L P, Rivkin S E. The implanted pump in metastatic colorectal cancer of the liver. Risk versus benefit.  Am J Surg. 1985;  149 595-598
• 44 Kemeny N, Seiter K, Conti J A et al.. Hepatic arterial floxuridine and leucovorin for unresectable liver metastases from colorectal carcinoma. New dose schedules and survival update.  Cancer. 1994;  73 1134-1142
• 45 Tarazov P G, Polysalov V N, Prozorovskij K V, Grishchenkova I V, Rozengauz E V. Ischemic complications of transcatheter arterial chemoembolization in liver malignancies.  Acta Radiol. 2000;  41 156-160
• 46 Harada T, Matsuo K, Inoue T, Tamesue S, Nakamura H. Is preoperative hepatic arterial chemoembolization safe and effective for hepatocellular carcinoma?.  Ann Surg. 1996;  224 4-9
• 47 Benhamou Y, Caumes E, Gerosa Y et al.. AIDS-related cholangiopathy. Critical analysis of a prospective series of 26 patients.  Dig Dis Sci. 1993;  38 1113-1118
• 48 Eidelberg D, Sotrel A, Vogel H et al.. Progressive polyradiculopathy in acquired immune deficiency syndrome.  Neurology. 1986;  36 912-916
• 49 Foucar E, Mukai K, Foucar K, Sutherland D E, Van Buren C T. Colon ulceration in lethal cytomegalovirus infection.  Am J Clin Pathol. 1981;  76 788-801
• 50 Koeppen A H, Lansing L S, Peng S K, Smith R S. Central nervous system vasculitis in cytomegalovirus infection.  J Neurol Sci. 1981;  51 395-410
• 51 Morgello S, Cho E S, Nielsen S, Devinsky O, Petito C K. Cytomegalovirus encephalitis in patients with acquired immunodeficiency syndrome: an autopsy study of 30 cases and a review of the literature.  Hum Pathol. 1987;  18 289-297
• 52 Rene E, Marche C, Chevalier T et al.. Cytomegalovirus colitis in patients with acquired immunodeficiency syndrome.  Dig Dis Sci. 1988;  33 741-750
• 53 Shintaku M, Inoue N, Sasaki M et al.. Cytomegalovirus vasculitis accompanied by an exuberant fibroblastic reaction in the intestine of an AIDS patient.  Acta Pathol Jpn. 1991;  41 900-904
• 54 Cello J P. Acquired immunodeficiency syndrome cholangiopathy: spectrum of disease.  Am J Med. 1989;  86 539-546
• 55 Burt A D, Scott G, Shiach C R, Isles C G. Acquired immunodeficiency syndrome in a patient with no known risk factors: a pathological study.  J Clin Pathol. 1984;  37 471-474
• 56 Kavin H, Jonas R B, Chowdhury L, Kabins S. Acalculous cholecystitis and cytomegalovirus infection in the acquired immunodeficiency syndrome.  Ann Intern Med. 1986;  104 53-54
• 57 Blewitt R W, Brown C M, Wyatt J I. The pathology of acute hepatic disintegration in hereditary haemorrhagic telangiectasia.  Histopathology. 2003;  42 265-269
• 58 Garcia-Tsao G, Korzenik J R, Young L et al.. Liver disease in patients with hereditary hemorrhagic telangiectasia.  N Engl J Med. 2000;  343 931-936
• 59 DeCosse J J, Rhodes R S, Wentz W B et al.. The natural history and management of radiation induced injury of the gastrointestinal tract.  Ann Surg. 1969;  170 369-384
• 60 Chandrasekhara K L, Iyer S K. Obstructive jaundice due to radiation-induced hepatic duct stricture.  Am J Med. 1984;  77 723-724
• 61 Cherqui D, Palazzo L, Piedbois P et al.. Common bile duct stricture as a late complication of upper abdominal radiotherapy.  J Hepatol. 1994;  20 693-697
• 62 Nakakubo Y, Kondo S, Katoh H, Shimizu M. Biliary stricture as a possible late complication of radiation therapy.  Hepatogastroenterology. 2000;  47 1531-1532
• 63 Martenson Jr J A, Gunderson L L, Buskirk S J et al.. Hepatic duct stricture after radical radiation therapy for biliary cancer: recurrence or fibrosis?.  Mayo Clin Proc. 1986;  61 530-536
• 64 Doppman J L, Dunnick N R, Girton M, Fauci A S, Popovsky M A. Bile duct cysts secondary to liver infarcts: report of a case and experimental production by small vessel hepatic artery occlusion.  Radiology. 1979;  130 1-5
• 65 Goritsas C P, Repanti M, Papadaki E, Lazarou N, Andonopoulos A P. Intrahepatic bile duct injury and nodular regenerative hyperplasia of the liver in a patient with polyarteritis nodosa.  J Hepatol. 1997;  26 727-730
• 66 Griffith G C, Vural I L. A correlation of clinical and postmortem findings in seventeen cases.  Circulation. 1951;  3 481-491
• 67 Reidbord H E, McCormack L J, O'Duffy J D. Necrotizing angiitis. II. Findings at autopsy in twenty-seven cases.  Cleve Clin Q. 1965;  32 191-204
• 68 Barquist E S, Goldstein N, Zinner M J. Polyarteritis nodosa presenting as a biliary stricture.  Surgery. 1991;  109 16-19
• 69 Hashikura Y, Makuuchi M, Kawasaki S et al.. Benign stricture of the intrahepatic bile duct with arterial involvement.  Hepatogastroenterology. 1994;  41 79-81
• 70 Saiura A, Umekita N, Inoue S et al.. Benign biliary stricture associated with atherosclerosis.  Hepatogastroenterology. 2001;  48 81-82
• 71 Char D, Mohan E, George R, Gambarin S. Common bile duct necrosis after cardiac catheterization.  Am J Gastroenterol. 1998;  93 2597-2598
• 72 Chen W J, Ying D J, Liu Z J, He Z P. Analysis of the arterial supply of the extrahepatic bile ducts and its clinical significance.  Clin Anat. 1999;  12 245-249
• 73 Hillaire S, Gardin C, Attar A et al.. Cholangiopathy and intrahepatic stones in sickle cell disease: coincidence or ischemic cholangiopathy?.  Am J Gastroenterol. 2000;  95 300-301
• 74 Gear J H, Meyers K E, Steele M. Kawasaki disease manifesting with acute cholangitis. A case report.  S Afr Med J. 1992;  81 31-33
• 75 Viola S, Meyer M, Fabre M et al.. Ischemic necrosis of bile ducts complicating Schonlein-Henoch purpura.  Gastroenterology. 1999;  117 211-214
• 76 Alberti-Flor J J, Jeffers L, Schiff E R. Primary sclerosing cholangitis occurring in a patient with systemic lupus erythematosus and diabetes mellitus.  Am J Gastroenterol. 1984;  79 889-891
• 77 Lamy P, Valla D, Bourgeois P, Rueff B, Benhamou J P. Primary sclerosing cholangitis and systemic lupus erythematosus.  Gastroenterol Clin Biol. 1988;  12 962-964
• 78 Audan A, Bruley Des Varannes S, Georgelin T et al.. Primary sclerosing cholangitis and systemic lupus erythematosus.  Gastroenterol Clin Biol. 1995;  19 123-126
• 79 Heyman S N, Spectre G, Aamar S et al.. Autoimmune cholangiopathy associated with systemic lupus erythematosus.  Liver. 2002;  22 102-106
• 80 Kirby D F, Blei A T, Rosen S T, Vogelzang R L, Neiman H L. Primary sclerosing cholangitis in the presence of a lupus anticoagulant.  Am J Med. 1986;  81 1077-1080
• 81 Le Thi Huong D, Valla D, Franco D et al.. Cholangitis associated with paroxysmal nocturnal hemoglobinuria: another instance of ischemic cholangiopathy?.  Gastroenterology. 1995;  109 1338-1343
• 82 Scheurlen M, Mork H, Weber P. Hypereosinophilic syndrome resembling chronic inflammatory bowel disease with primary sclerosing cholangitis.  J Clin Gastroenterol. 1992;  14 59-63
• 83 Engler S, Elsing C, Flechtenmacher C et al.. Progressive sclerosing cholangitis after septic shock: a new variant of vanishing bile duct disorders.  Gut. 2003;  52 688-693
• 84 Putensen C, Wrigge H, Hering R. The effects of mechanical ventilation on the gut and abdomen.  Curr Opin Crit Care. 2006;  12 160-165
• 85 Trager K, Radermacher P, Georgieff M. PEEP and hepatic metabolic performance in septic shock.  Intensive Care Med. 1996;  22 1274-1275
• 86 Starzl T E, Demetris A J. Liver transplantation: a 31-year perspective. Part I.  Curr Probl Surg. 1990;  27 49-116
• 87 Demetris A J. Ischemic cholangitis.  Mayo Clin Proc. 1992;  67 601-602
• 88 Ludwig J, Batts K P, MacCarty R L. Ischemic cholangitis in hepatic allografts.  Mayo Clin Proc. 1992;  67 519-526
• 89 Sebagh M, Farges O, Kalil A et al.. Sclerosing cholangitis following human orthotopic liver transplantation.  Am J Surg Pathol. 1995;  19 81-90
• 90 Silva M A, Jambulingam P S, Gunson B K et al.. Hepatic artery thrombosis following orthotopic liver transplantation: a 10-year experience from a single centre in the United Kingdom.  Liver Transpl. 2006;  12 146-151
• 91 Drazan K, Shaked A, Olthoff K M et al.. Etiology and management of symptomatic adult hepatic artery thrombosis after orthotopic liver transplantation (OLT).  Am Surg. 1996;  62 237-240
• 92 Tzakis A G, Gordon R D, Shaw Jr B W, Iwatsuki S, Starzl T E. Clinical presentation of hepatic artery thrombosis after liver transplantation in the cyclosporine era.  Transplantation. 1985;  40 667-671
• 93 Gunsar F, Rolando N, Pastacaldi S et al.. Late hepatic artery thrombosis after orthotopic liver transplantation.  Liver Transpl. 2003;  9 605-611
• 94 Pinna A D, Smith C V, Furukawa H, Starzl T E, Fung J J. Urgent revascularization of liver allografts after early hepatic artery thrombosis.  Transplantation. 1996;  62 1584-1587
• 95 Nakamura N, Nishida S, Neff G R et al.. Intrahepatic biliary strictures without hepatic artery thrombosis after liver transplantation: an analysis of 1,113 liver transplantations at a single center.  Transplantation. 2005;  79 427-432
• 96 Ko W F, Cello J P, Rogers S J, Lecours A. Prognostic factors for the survival of patients with AIDS cholangiopathy.  Am J Gastroenterol. 2003;  98 2176-2181
• 97 Hohn D C, Stagg R J, Friedman M A et al.. A randomized trial of continuous intravenous versus hepatic intraarterial floxuridine in patients with colorectal cancer metastatic to the liver: the Northern California Oncology Group trial.  J Clin Oncol. 1989;  7 1646-1654
• 98 Gotoh M, Monden M, Sakon M et al.. Bile duct necrosis after partial hepatectomy and transcatheter hepatic arterial embolization.  AJR Am J Roentgenol. 1990;  154 1124
• 99 Kim B W, Won J H, Lee B M et al.. Intraarterial thrombolytic treatment for hepatic artery thrombosis immediately after living donor liver transplantation.  Transplant Proc. 2006;  38 3128-3131
• 100 Rogers J, Chavin K D, Kratz J M et al.. Use of autologous radial artery for revascularization of hepatic artery thrombosis after orthotopic liver transplantation: case report and review of indications and options for urgent hepatic artery reconstruction.  Liver Transpl. 2001;  7 913-917
• 101 Zhou J, Fan J, Wang J H et al.. Continuous transcatheter arterial thrombolysis for early hepatic artery thrombosis after liver transplantation.  Transplant Proc. 2005;  37 4426-4429
• 102 Hintze R E, Adler A, Veltzke W et al.. Endoscopic management of biliary complications after orthotopic liver transplantation.  Hepatogastroenterology. 1997;  44 258-262
• 103 Neuhaus P, Blumhardt G, Bechstein W O et al.. Technique and results of biliary reconstruction using side-to-side choledochocholedochostomy in 300 orthotopic liver transplants.  Ann Surg. 1994;  219 426-434
• 104 Theilmann L, Kuppers B, Kadmon M et al.. Biliary tract strictures after orthotopic liver transplantation: diagnosis and management.  Endoscopy. 1994;  26 517-522
• 105 Li S, Stratta R J, Langnas A N et al.. Diffuse biliary tract injury after orthotopic liver transplantation.  Am J Surg. 1992;  164 536-540
• 106 Schlitt H J, Meier P N, Nashan B et al.. Reconstructive surgery for ischemic-type lesions at the bile duct bifurcation after liver transplantation.  Ann Surg. 1999;  229 137-145
• 107 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
• 108 Bismuth H, Lazorthes F. 83rd Congress of the French Surgical Society (Paris, 21–24 September 1981). Second report. Operative injuries of the common biliary duct.  J Chir (Paris). 1981;  118 601-609
• 109 Northover J, Terblanche J. Bile duct blood supply. Its importance in human liver transplantation.  Transplantation. 1978;  26 67-69
• 110 Bauer T, Britton P, Lomas D et al.. Liver transplantation for hepatic arteriovenous malformation in hereditary haemorrhagic telangiectasia.  J Hepatol. 1995;  22 586-590