“Cardiac Hepatopathy”: A Review of Liver Dysfunction in Heart Failure
DOI:
https://doi.org/10.17140/lroj-1-101Keywords:
Congestive hepatopathy, Hypoxic hepatitis, Ischemic hepatitis, High-gradient ascites, Nutmeg liver, Heart failureAbstract
The unique dual circulation of the liver confers relative protection against ischemic injury; however, low oxygen tension in the microcirculation (sinusoidal blood of the hepatic acinus) may render hepatocytes in zone 3 relatively vulnerable to ischemic injury and necrosis. Severe congestive heart failure is associated with two distinct forms of liver dysfunction under the umbrella term “cardiac hepatopathy”. The two entities include: jaundice related to passive congestion (congestive hepatopathy from backward cardiac failure) and acute hepatocellular necrosis caused by impaired hepatic perfusion (hypoxic hepatitis from forward cardiac failure). This article provides a comprehensive, up-to-date review on the topic and focuses on the epidemiology, pathology, pathogenesis, clinical manifestations, diagnostic testing and treatment strategies pertaining to liver disease in circulatory failure.
References
Sherlock S. The liver in heart failure: relation of anatomical, functional, and circulatory changes. Br heart J. 1951; 13: 273- 293.
Myers R, Cerini R, Sayegh R, et al. Cardiac Hepatopathy: Clinical, hemodynamic, and histologic characteristics and cor-relations. Hepatology. 2003; 37(2): 393-400. doi: 10.1053/ jhep.2003.50062
Moller S, Dumcke C, Krag A. The heart and the liver. Ex-pert Rev Gastroenterol & hepatol. 2009; 3(1): 51-64. doi: 10.1586/17474124.3.1.51
Naschitz J, Slobodin G, Lewis R, Zuckerman E, Yeshurun D. Heart diseases affecting the liver and liver diseases affect-ing the heart. Am Heart J. 2000; 140(1): 111-120. doi: 10.1067/ mhj.2000.107177
Lautt WW, Greenway CV. Conceptual review of hepatic vascular bed. Hepatology. 1987; 7: 952-963. doi: 10.1002/ hep.1840070527
Giallourakis C, Rosenberg P, Friedman L. The liver in heart failure. Clin Liver Dis. 2002; 6(4): 947-967.
Wong F, Greenbloom S, Blendis L. The liver in heart failure. In: Friedman L, Keeffe E. Handbook of Liver Disease. 2nd Ed. Churchill Livingstone; 2004.
Rappaport AM. The microcirculatory hepatic unit. Microvasc Res. 1973; 6: 212-228. doi: 10.1016/0026-2862(73)90021-6
Rappaport AM. Hepatic blood flow: morphologic aspects and physiologic regulation. Int Rev Physiol. 1980; 21: 1-63.
Megalla S, Holtzman D, Aronow WS, et al. Prediction of cardiac hepatopathy in patients with right heart failure. Med Sci Monit. 2011; 17(10): 537-541.
Hoffman BT, Pate MB, Marsh WH, Lee WM. Cardiomyo-pathy unrecognized as a cause of hepatic failure. J Clin Gas-troenterology 1990; 12(3): 306-309. doi: 10.1097/00004836- 199006000-00015
Aboulhosn JA, Oudiz RJ, Dave AS, Ardehali A, Ross DJ. Suc-cessful tricuspid valve replacement in a patient with severe pul-monary arterial hypertension and preserved right ventricular sys-tolic function. Case Rep. Med. 2009. doi: 10.1155/2009/108295
Sheth AA, Lim JK. Liver disease from asymptomatic con-strictive pericaditis. J. Clin Gastroenterology 2008; 42(8): 956- 958. doi: 10.1097/MCG.0b013e318031915c
Harding MB, Harrison JK, Davidson CJ, Kisslo KB, Bashore TM. Critical mitral stenosis causing ischemic hepatic failure. Successful treatment by percutaneous balloon mitral valvotomy. Chest 1992; 101(3): 866-889. doi: 10.1378/chest.101.3.866
Dunn G, Hayes P, Breen K, Schenker S. The liver in conges-tive heart failure: a review. Am J Med Sci. 1973; 265(3): 174- 189.
Cohen J, Kaplan M. Left sided heart failure presenting as hepatitis. Gastroenterology. 1978; 74: 583-587.
White T, Wallace R, Gnassi A, Kemp N, Price H, Leevy C. Hepatic abnormalities in congestive heart failure. Needle biop-sy studies. Circulation. 1951; 3(4): 501-507. doi: 10.1161/01. CIR.3.4.501
Arcidi J, Moore G, Hutchins G. Hepatic morphology in car-diac dysfunction: A clinicopathologic study of 1000 subjects at autopsy. Am J Pathol. 1981; 104(2): 159-166.
Lefkowitch J, Mendez L. Morphologic features of hepatic in-jury in cardiac disease and shock. Journal of Hepatology. 1986; 2(3): 313-327. doi: 10.1016/S0168-8278(86)80043-5
Allen L, Felker G, Pocock S, et al. Liver function abnormali-ties and outcome in patients with chronic heart failure: data from the Candesartan in Heart Failure: Assessment of Reduction in Mortality and Morbidity(CHARM) program. Eur J Heart Fail-ure. 2009; 11(2):170-177. doi: 10.1093/eurjhf/hfn031
van Deursen V, Damman K, Hillege H, van Beek A, van Veldhuisen D, Voors A. Abnormal liver function in relation to hemodynamic profile in heart failure patients. J Card Fail. 2010; 16(1): 84-90. doi: 10.1016/j.cardfail.2009.08.002
Gelow J, Desai A, Hochberg C, Glickman J, Givertz M, Fang J. Clinical predictors of hepatic fibrosis in chronic advanced heart failure. Circ Heart Fail. 2010; 3(1): 59-65. doi: 10.1161/ CIRCHEARTFAILURE.109.872556
Calleja H, Rosenow O, Clark T. Pulsations of the liver in heart disease. Am J Med. 1961; 30(2): 202-210. doi: 10.1016/0002- 9343(61)90092-4
Jolliffe N. Liver function in congestive heart failure. J Clin Invest. 1930; 8(3): 419-434. doi: 10.1172/JCI100272
Richman S, Delman A, Grob D. Alterations in indices of liver function in congestive heart failure with particular ref-erence to serum enzymes. Am J Med. 1961; 30(2): 211-225. doi: 10.1016/0002-9343(61)90093-6
Akriviadis E, Kapnias D, Hadjigavriel M, Mitsiou A, Gou-lis J. Serum/ascites albumin gradient: its value as a rational ap-proach to the differential diagnosis of ascites. Scand J Gastroen-terol. 1996; 31(8): 814-817. doi: 10.3109/00365529609010358
Gore RM, Mathieu DG, White EM, et al. Passive hepatic congestion: cross sectional imaging features. Am J Roentgenol. 1994; 162: 71-75. doi: 10.2214/ajr.162.1.8273693
Bosch J, Mastai R, Kravetz D, Navasa M, Rodes J. Hemody-namic evaluation of the patient with portal hypertension. Semin Liver Dis. 1986; 6(4): 309-317. doi: 10.1055/s-2008-1040613
Reynolds T, Ito S, Iwatsuki S. Measurement of portal pres-sure and its clinical application. Am J Med. 1970; 49: 649-657. doi: 10.1016/S0002-9343(70)80131-0
Sherlock S. The liver in circulatory failure. In: Schiff L. Dis-eases of the Liver. 7th Ed. Philadelphia: Lippincott Williams & Wilkins; 1993: 1600.
Bayraktar U, Seren S, Bayraktar Y. Hepatic venous outflow obstruction: three similar syndromes. World J Gastroenterol. 2007; 13(13): 1912-1927. doi: 10.3748/wjg.v13.i13.1912
Marshall A, Ring N, Lewis T. Constrictive pericarditis: lessons from the past five years’ experience in the South West Cardiothoracic Centre. Clinical Medicine. 2006; 6(6): 592-597. doi: 10.7861/clinmedicine.6-6-592
Kubo S, Walter B, John D, Clark M, Cody R. Liver function abnormalities in chronic heart failure. Influence of systemic he-modynamics. Arch Internal Med. 1987; 147(7): 1227-1230. doi: 10.1001/archinte.1987.00370070041006
Johnson R, O’Connor M, Kerr R. Extreme serum elevations of aspartate aminotransferase. Am J Gastroenterol. 1995; 90(8): 1244-1245.
Bessman A, Evans J. The blood ammonia in congestive heart failure. Am Heart J. 1955; 50(5): 715-719. doi: 10.1016/0002- 8703(55)90178-2
Kisloff B, Schaffer G. Fulminant hepatic failure secondary to congestive heart failure. Am J Dig Dis. 1976; 21(10): 895-900. doi: 10.1007/BF01072084
Bansal S, Lindenfeld J, Schrier R. Sodium retention in heart failure and cirrhosis: potential role of natriuretic doses of min-eralocorticoid antagonist? Circ Heart Fail. 2009; 2(4): 370-376. doi: 10.1161/CIRCHEARTFAILURE.108.821199
Runyon B. Cardiac ascites: a characterization. J Clin Gastro-enterology. 1988; 10(4): 410-412.
Jafri S. Hypercoagulability in heart failure. Semin Thromb Hemost . 1997; 23(6): 543-545. doi: 10.1055/s-2007-996133
Frazier O, Rose E, Oz M, et al. Multicenter clinical evalu-ation of the HeartMate vented electric left ventricular assist system in patients awaiting heart transplantation. J Thorac Car-diovasc Surg. 2001; 122(6): 1186-1195. doi: 10.1016/S1053- 2498(00)00429-0
Russell S, Rogers J, Milano C, et al. Renal and hepatic func-tion improve in advanced heart failure patients during continu-ous flow support with HeartMate II left ventricular assist de-vice. Circulation. 2009; 120(23): 2352-2357. doi: 10.1161/ CIRCULATIONAHA.108.814863
Dichtl, W, Vogel W, Dunst K, et al. Cardiac hepatopathy before and after heart transplantation. Transpl Int. 2005; 18(6): 697-702. doi: 10.1111/j.1432-2277.2005.00122.x
Raichlin E, Daly R, Rosen C, et al. Combined heart and liver transplantation: a single-center experience. Transplantation. 2009; 88(2): 219-226. doi: 10.1097/TP.0b013e3181ac60db
Crespo-leiro M, Robels O, Paniagua M, et al. Reversal of cardiac cirrhosis following orthotopic heart transplantation. Am J Transplant. 2008; 8(6): 1336-1339. doi: 10.1111/j.1600-6143- .2008.02227.x
Nouel O, Henrion J, Bernauau J, Degott C, Rueff B, Ben-hamou J. Fulminant hepatic failure due to transient circulatory failure in patients with chronic heart disease. Digestive Diseases and Sciences. 1980; 25: 49-52. doi: 10.1007/BF01312732
Saner FH, Heuer M, Meyer M, et al. When the heart kills the liver: acute liver failure in congestive heart failure. Eur J Med Res. 2009; 14(12): 541-546. doi: 10.1186/2047-783X-14- 12-541
Pfeffer M, Swedberg K, Granger C, et al. Effects of can-desartan on mortality and morbidity in patients with chronic heart failure: the CHARM-Overall programme. Lancet. 2003; 362(9386): 759-766. doi: 10.1016/S0140-6736(03)14282-1
Batin P, Wickens M, McEntegart D, Fullwood L, Cowley A. The importance of abnormalities of liver function tests in predicting mortality in chronic heart failure. Eur Heart J. 1995; 16(11): 1613-1618.
Shinagawa H, Inomata T, Koitabashi T, et al. Prognos-tic significance of increased serum bilirubin levels coin-cident with cardiac decompensation in chronic heart fail-ure. Circ J. 2008; 72(3): 364-369. doi: 10.1253/circj.72.364
Fuhrmann V, Jager B, Zubkova A, Drolz A. Hypoxic hepa-titis - epidemiology, pathophysiology, and clinical management. Wien Klin Wochenschr. 2010; 122(5-6): 129-139. doi: 10.1007/ s00508-010-1357-6
Birgens H, Henriksen J, Matzen P, Poulsen H. The shock liver. Clinical and biochemical findings in patients with centri-lobular necrosis following cardiogenic shock. Acta Med Scand. 1978; 204(5): 417-421.
Bynum T, Boitnott J, Maddrey W. Ischemic hepatitis. Diges-tive Diseases and Sciences. 1979; 24(2): 129-135. doi: 10.1007/ BF01324740
Henrion J, Schapira M, Luwaert R, Colin L, Delannoy A, Heller F. Hypoxic hepatitis: Clinical and hemodynamic study in 142 consecutive cases. Medicine(Baltimore). 2003; 82(6): 392- 406. doi: 10.1097/01.md.0000101573.54295.bd
Birrer R, Takuda, Y, Takara T. Hypoxic hepatopathy: pathophysiology and prognosis. Intern Med. 2007; 46(14): 1063-1070. doi: 10.2169/internalmedicine.46.0059
Henrion J, Descamps O, Luwaert R, Schapira M, Parfonry A, Heller F. Hypoxic hepatitis in patients with cardiac failure: incidence in a coronary care unit and measurement of hepatic blood flow. J Hepatol. 1994; 21(5): 696-703. doi: 10.1016/ s0168-8278(94)80226-2
Fuchs S, Bogomolski-Yahalom V, Paltiel O, Ackerman Z. Ischemic hepatitis: clinical and laboratory observations of 34 pa-tients. J Clin Gastroenterology. 1998; 26(3): 183-186.
Seeto R, Fenn B, Rockey D. Ischemic hepatitis: clinical pre-sentation and pathogenesis. Am J Med. 2000; 109(2): 109-113. doi: 10.1016/s0002-9343(00)00461-7
Denis C, De Kerguennec C, Bernuau J, Beauvais F, Co-hen Solal A. Acute hypoxic hepatitis(‘liver shock’): still a fre-quently overlooked cardiological diagnosis. Eur J Heart Fail-ure. 2004; 6(5): 561-565. doi: 10.1016/j.ejheart.2003.12.008
Soultati A, Dourakis S. Liver dysfunction in the intensive care unit. Annals of Gastroenterology. 2005; 18(1): 35-45.
Ebert E. Hypoxic liver injury. Mayo Clinic Proceedings. 2006; 81(9): 1232-1236. doi: 10.4065/81.9.1232
Cassidy W, Reynolds T. Serum lactic dehydrogenase in the differential diagnosis of acute hepatocellular injury. J Clin Gastroenterol. 1994; 19(2): 118-121. doi: 10.1097/00004836- 199409000-00008
Stromeyer F, Ishak K. Nodular transformation(nodular ‘re-generative’ hyperplasia) of the liver. A clinicopathologic study of 30 cases. Hum Pathol. 1981; 12(1): 60-69. doi: 10.1016/ S0046-8177(81)80242-0
Stravitz R, Kramer A, Davert T, et al. Intensive care of pa-tients with acute liver failure: recommendations of the US Acute Liver Failure Study Group. Crit Care Med. 2007; 35(11): 2498- 2508.
Szabo G, Romics Jr L, Frendl G. Liver in sepsis and systemic inflammatory response syndrome. Clin Liver Dis. 2002; 6(4): 1045-1056. doi: 10.1016/s1089-3261(02)00058-2
Fuhrmann, V, Madl C, Mueller C, et al. Hepatopulmonary syndrome in patients wtih hypoxic hepatitis. Gastroenterology. 2006; 131(1): 69-76. doi: 10.1053/j.gastro.2006.04.014
Naschitz J, Yeshurun D. Compensated cardiogenic shock: a subset with damage limited to liver and kidneys. The possible salutary effect of low-dose dopamine. Cardiology. 1987; 74(3): 212-218. doi: 10.1159/000174199
Desai A, Kadleck D, Hufford L, Leikin J. N-Acetylcysteine use in ischemic hepatitis. Am J Ther. 2006; 13(1): 80-83. doi: 10.1097/01.mjt.0000158338.08483.59
Ming Z, Han C, Lautt W. Nitric oxide mediates hepatic arte-rial vascular escape from norepinephrine-induced constriction. Am J Physiol. 1999; 277: G1200-G1206.
Masuko H, Jin M, Horiuchi H, et al. Protective effect of an-giotensin II type I receptor antagonist, CV-11974, on ischemia and reperfusion injury of the liver. Transplantation. 2001; 71(8): 1034-1039. doi: 10.1097/00007890-200104270-00003 -
El Banayosy A, Kizner L, Schueler V, Bergmeier S, Cobaugh D, Koerfer R. First use of molecular adsorbent recirculating sys-tem technique on patients with hypoxic liver failure after cardio-genic shock. ASAIO J. 2004; 50(4): 332-337.
Laleman W, Wilmer A, Evenepoel P, et al. Effect of the mo-lecular adsorbent recirculating system and Prometheus devices in systemic haemodynamics and vasoactive agents in patients with acute-on-chronic liver failure. Crit Care. 2006; 10(4): R108. doi: 10.1186/cc4985
Stefoni S, Coli L, Bolondi L, et al. Molecular adsorbent re-circulating system(MARS) application in liver failure: clinical and hemodepurative results in 22 patients. Int J Artif Organs. 2006; 29(2): 207-218.
Downloads
Published
How to Cite
Issue
Section
License

This work is licensed under a Creative Commons Attribution 4.0 International License.
All content published in Liver Research (LROJ) is licensed under the Creative Commons Attribution 4.0 International License (CC BY 4.0). This license allows anyone to copy, distribute, transmit, and adapt the work — including for commercial purposes — provided appropriate credit is given to the original author(s) and source.