Skip to main content
Erschienen in: Metabolic Brain Disease 6/2016

08.10.2015 | Original Article

Clinical science workshop: targeting the gut-liver-brain axis

verfasst von: Vishal C. Patel, Helen White, Sidsel Støy, Jasmohan S. Bajaj, Debbie L. Shawcross

Erschienen in: Metabolic Brain Disease | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

A clinical science workshop was held at the ISHEN meeting in London on Friday 11th September 2014 with the aim of thrashing out how we might translate what we know about the central role of the gut-liver-brain axis into targets which we can use in the treatment of hepatic encephalopathy (HE). This review summarises the integral role that inter-organ ammonia metabolism plays in the pathogenesis of HE with specific discussion of the roles that the small and large intestine, liver, brain, kidney and muscle assume in ammonia and glutamine metabolism. Most recently, the salivary and gut microbiome have been shown to underpin the pathophysiological changes which culminate in HE and patients with advanced cirrhosis present with enteric dysbiosis with small bowel bacterial overgrowth and translocation of bacteria and their products across a leaky gut epithelial barrier. Resident macrophages within the liver are able to sense bacterial degradation products initiating a pro-inflammatory response within the hepatic parenchyma and release of cytokines such as tumour necrosis factor alpha (TNF-α) and interleukin-8 into the systemic circulation. The endotoxemia and systemic inflammatory response that are generated predispose both to the development of infection as well as the manifestation of covert and overt HE. Co-morbidities such as diabetes and insulin resistance, which commonly accompany cirrhosis, may promote slow gut transit, promote bacterial overgrowth and increase glutaminase activity and may need to be acknowledged in HE risk stratification assessments and therapeutic regimens. Therapies are discussed which target ammonia production, utilisation or excretion at an individual organ level, or which reduce systemic inflammation and endotoxemia which are known to exacerbate the cerebral effects of ammonia in HE. The ideal therapeutic strategy would be to use an agent that can reduce hyperammonemia and reduce systemic inflammation or perhaps to adopt a combination of therapies that can address both.
Literatur
Zurück zum Zitat Agrawal A, Sharma BC, Sharma P, Sarin SK (2012) Secondary prophylaxis of hepatic encephalopathy in cirrhosis: an open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am J Gastroenterol 107:1043–1050. doi:10.1038/ajg.2012.113 PubMedCrossRef Agrawal A, Sharma BC, Sharma P, Sarin SK (2012) Secondary prophylaxis of hepatic encephalopathy in cirrhosis: an open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am J Gastroenterol 107:1043–1050. doi:10.​1038/​ajg.​2012.​113 PubMedCrossRef
Zurück zum Zitat Ahboucha S, Pomier-Layrargues G, Mamer O, Butterworth RF (2006) Increased levels of pregnenolone and its neuroactive metabolite allopregnanolone in autopsied brain tissue from cirrhotic patients who died in hepatic coma. Neurochem Int 49:372–378. doi:10.1016/j.neuint.2006.02.002 PubMedCrossRef Ahboucha S, Pomier-Layrargues G, Mamer O, Butterworth RF (2006) Increased levels of pregnenolone and its neuroactive metabolite allopregnanolone in autopsied brain tissue from cirrhotic patients who died in hepatic coma. Neurochem Int 49:372–378. doi:10.​1016/​j.​neuint.​2006.​02.​002 PubMedCrossRef
Zurück zum Zitat Bai G, Rama Rao KV, Murthy CR, Panickar KS, Jayakumar AR, Norenberg MD (2001) Ammonia induces the mitochondrial permeability transition in primary cultures of rat astrocytes. J Neurosci Res 66:981–991PubMedCrossRef Bai G, Rama Rao KV, Murthy CR, Panickar KS, Jayakumar AR, Norenberg MD (2001) Ammonia induces the mitochondrial permeability transition in primary cultures of rat astrocytes. J Neurosci Res 66:981–991PubMedCrossRef
Zurück zum Zitat Banares R et al (2013) Extracorporeal albumin dialysis with the molecular adsorbent recirculating system in acute-on-chronic liver failure: the RELIEF trial. Hepatology 57:1153–1162. doi:10.1002/hep.26185 PubMedCrossRef Banares R et al (2013) Extracorporeal albumin dialysis with the molecular adsorbent recirculating system in acute-on-chronic liver failure: the RELIEF trial. Hepatology 57:1153–1162. doi:10.​1002/​hep.​26185 PubMedCrossRef
Zurück zum Zitat Banks WA, Ortiz L, Plotkin SR, Kastin AJ (1991) Human interleukin (IL) 1 alpha, murine IL-1 alpha and murine IL-1 beta are transported from blood to brain in the mouse by a shared saturable mechanism. J Pharmacol Exp Ther 259:988–996PubMed Banks WA, Ortiz L, Plotkin SR, Kastin AJ (1991) Human interleukin (IL) 1 alpha, murine IL-1 alpha and murine IL-1 beta are transported from blood to brain in the mouse by a shared saturable mechanism. J Pharmacol Exp Ther 259:988–996PubMed
Zurück zum Zitat Banks WA, Kastin AJ, Gutierrez EG (1994) Penetration of interleukin-6 across the murine blood–brain barrier. Neurosci Lett 179:53–56PubMedCrossRef Banks WA, Kastin AJ, Gutierrez EG (1994) Penetration of interleukin-6 across the murine blood–brain barrier. Neurosci Lett 179:53–56PubMedCrossRef
Zurück zum Zitat Bass NM et al (2010) Rifaximin treatment in hepatic encephalopathy. New Engl J Med 362:1071–1081PubMedCrossRef Bass NM et al (2010) Rifaximin treatment in hepatic encephalopathy. New Engl J Med 362:1071–1081PubMedCrossRef
Zurück zum Zitat Basu S, Zethelius B, Helmersson J, Berne C, Larsson A, Arnlov J (2011) Cytokine-mediated inflammation is independently associated with insulin sensitivity measured by the euglycemic insulin clamp in a community-based cohort of elderly men. Int J Clin Exp Med 4:164–168PubMedPubMedCentral Basu S, Zethelius B, Helmersson J, Berne C, Larsson A, Arnlov J (2011) Cytokine-mediated inflammation is independently associated with insulin sensitivity measured by the euglycemic insulin clamp in a community-based cohort of elderly men. Int J Clin Exp Med 4:164–168PubMedPubMedCentral
Zurück zum Zitat Bernal W, Hall C, Karvellas CJ, Auzinger G, Sizer E, Wendon J (2007) Arterial ammonia and clinical risk factors for encephalopathy and intracranial hypertension in acute liver failure. Hepatology 46:1844–1852. doi:10.1002/hep.21838 PubMedCrossRef Bernal W, Hall C, Karvellas CJ, Auzinger G, Sizer E, Wendon J (2007) Arterial ammonia and clinical risk factors for encephalopathy and intracranial hypertension in acute liver failure. Hepatology 46:1844–1852. doi:10.​1002/​hep.​21838 PubMedCrossRef
Zurück zum Zitat Blei AT, Olafsson S, Therrien G, Butterworth RF (1994) Ammonia-induced brain edema and intracranial hypertension in rats after portacaval anastomosis. Hepatology 19:1437–1444PubMedCrossRef Blei AT, Olafsson S, Therrien G, Butterworth RF (1994) Ammonia-induced brain edema and intracranial hypertension in rats after portacaval anastomosis. Hepatology 19:1437–1444PubMedCrossRef
Zurück zum Zitat Caly WR, Strauss E (1993) A prospective study of bacterial infections in patients with cirrhosis. J Hepatol 18:353–358PubMedCrossRef Caly WR, Strauss E (1993) A prospective study of bacterial infections in patients with cirrhosis. J Hepatol 18:353–358PubMedCrossRef
Zurück zum Zitat Cauli O, Rodrigo R, Piedrafita B, Boix J, Felipo V (2007) Inflammation and hepatic encephalopathy: ibuprofen restores learning ability in rats with portacaval shunts. Hepatology 46:514–519. doi:10.1002/hep.21734 PubMedCrossRef Cauli O, Rodrigo R, Piedrafita B, Boix J, Felipo V (2007) Inflammation and hepatic encephalopathy: ibuprofen restores learning ability in rats with portacaval shunts. Hepatology 46:514–519. doi:10.​1002/​hep.​21734 PubMedCrossRef
Zurück zum Zitat Cauli O, Mansouri MT, Agusti A, Felipo V (2009) Hyperammonemia increases GABAergic tone in the cerebellum but decreases it in the rat cortex. Gastroenterology 136(1359–1367):e1351–e1352. doi:10.1053/j.gastro.2008.12.057 Cauli O, Mansouri MT, Agusti A, Felipo V (2009) Hyperammonemia increases GABAergic tone in the cerebellum but decreases it in the rat cortex. Gastroenterology 136(1359–1367):e1351–e1352. doi:10.​1053/​j.​gastro.​2008.​12.​057
Zurück zum Zitat Chastre A, Jiang W, Desjardins P, Butterworth RF (2010) Ammonia and proinflammatory cytokines modify expression of genes coding for astrocytic proteins implicated in brain edema in acute liver failure. Metab Brain Dis 25:17–21. doi:10.1007/s11011-010-9185-y PubMedCrossRef Chastre A, Jiang W, Desjardins P, Butterworth RF (2010) Ammonia and proinflammatory cytokines modify expression of genes coding for astrocytic proteins implicated in brain edema in acute liver failure. Metab Brain Dis 25:17–21. doi:10.​1007/​s11011-010-9185-y PubMedCrossRef
Zurück zum Zitat Chen MF, Mo LR, Lin RC, Kuo JY, Chang KK, Liao C, Lu FJ (1997) Increase of resting levels of superoxide anion in the whole blood of patients with decompensated liver cirrhosis. Free Radic Biol Med 23:672–679PubMedCrossRef Chen MF, Mo LR, Lin RC, Kuo JY, Chang KK, Liao C, Lu FJ (1997) Increase of resting levels of superoxide anion in the whole blood of patients with decompensated liver cirrhosis. Free Radic Biol Med 23:672–679PubMedCrossRef
Zurück zum Zitat Cirera I et al (2001) Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol 34:32–37PubMedCrossRef Cirera I et al (2001) Bacterial translocation of enteric organisms in patients with cirrhosis. J Hepatol 34:32–37PubMedCrossRef
Zurück zum Zitat Clemmesen JO, Larsen FS, Kondrup J, Hansen BA, Ott P (1999) Cerebral herniation in patients with acute liver failure is correlated with arterial ammonia concentration. Hepatology 29:648–653. doi:10.1002/hep.510290309 PubMedCrossRef Clemmesen JO, Larsen FS, Kondrup J, Hansen BA, Ott P (1999) Cerebral herniation in patients with acute liver failure is correlated with arterial ammonia concentration. Hepatology 29:648–653. doi:10.​1002/​hep.​510290309 PubMedCrossRef
Zurück zum Zitat Cordoba J et al (2001) The development of low-grade cerebral edema in cirrhosis is supported by the evolution of (1)H-magnetic resonance abnormalities after liver transplantation. J Hepatol 35:598–604PubMedCrossRef Cordoba J et al (2001) The development of low-grade cerebral edema in cirrhosis is supported by the evolution of (1)H-magnetic resonance abnormalities after liver transplantation. J Hepatol 35:598–604PubMedCrossRef
Zurück zum Zitat Courson A, Jones GM, Twilla JD (2015) Treatment of acute hepatic encephalopathy: comparing the effects of adding rifaximin to lactulose on patient outcomes. J Pharm Pract. doi:10.1177/0897190014566312 PubMed Courson A, Jones GM, Twilla JD (2015) Treatment of acute hepatic encephalopathy: comparing the effects of adding rifaximin to lactulose on patient outcomes. J Pharm Pract. doi:10.​1177/​0897190014566312​ PubMed
Zurück zum Zitat Erceg S, Monfort P, Cauli O, Montoliu C, Llansola M, Piedrafita B, Felipo V (2006) Role of extracellular cGMP and of hyperammonemia in the impairment of learning in rats with chronic hepatic failure. Therapeutic implications. Neurochem Int 48:441–446. doi:10.1016/j.neuint.2005.10.016 PubMedCrossRef Erceg S, Monfort P, Cauli O, Montoliu C, Llansola M, Piedrafita B, Felipo V (2006) Role of extracellular cGMP and of hyperammonemia in the impairment of learning in rats with chronic hepatic failure. Therapeutic implications. Neurochem Int 48:441–446. doi:10.​1016/​j.​neuint.​2005.​10.​016 PubMedCrossRef
Zurück zum Zitat Gluud LL et al (2013) Oral branched-chain amino acids have a beneficial effect on manifestations of hepatic encephalopathy in a systematic review with meta-analyses of randomized controlled trials. J Nutr 143:1263–1268. doi:10.3945/jn.113.174375 PubMedCrossRef Gluud LL et al (2013) Oral branched-chain amino acids have a beneficial effect on manifestations of hepatic encephalopathy in a systematic review with meta-analyses of randomized controlled trials. J Nutr 143:1263–1268. doi:10.​3945/​jn.​113.​174375 PubMedCrossRef
Zurück zum Zitat Haussinger D, Lamers WH, Moorman AF (1992) Hepatocyte heterogeneity in the metabolism of amino acids and ammonia. Enzyme 46:72–93PubMed Haussinger D, Lamers WH, Moorman AF (1992) Hepatocyte heterogeneity in the metabolism of amino acids and ammonia. Enzyme 46:72–93PubMed
Zurück zum Zitat Haussinger D, Kircheis G, Fischer R, Schliess F, vom Dahl S (2000) Hepatic encephalopathy in chronic liver disease: a clinical manifestation of astrocyte swelling and low-grade cerebral edema? J Hepatol 32:1035–1038PubMedCrossRef Haussinger D, Kircheis G, Fischer R, Schliess F, vom Dahl S (2000) Hepatic encephalopathy in chronic liver disease: a clinical manifestation of astrocyte swelling and low-grade cerebral edema? J Hepatol 32:1035–1038PubMedCrossRef
Zurück zum Zitat Hermenegildo C, Montoliu C, Llansola M, Munoz MD, Gaztelu JM, Minana MD, Felipo V (1998) Chronic hyperammonemia impairs the glutamate-nitric oxide-cyclic GMP pathway in cerebellar neurons in culture and in the rat in vivo. Eur J Neurosci 10:3201–3209PubMedCrossRef Hermenegildo C, Montoliu C, Llansola M, Munoz MD, Gaztelu JM, Minana MD, Felipo V (1998) Chronic hyperammonemia impairs the glutamate-nitric oxide-cyclic GMP pathway in cerebellar neurons in culture and in the rat in vivo. Eur J Neurosci 10:3201–3209PubMedCrossRef
Zurück zum Zitat Hermenegildo C, Monfort P, Felipo V (2000) Activation of N-methyl-D-aspartate receptors in rat brain in vivo following acute ammonia intoxication: characterization by in vivo brain microdialysis. Hepatology 31:709–715. doi:10.1002/hep.510310322 PubMedCrossRef Hermenegildo C, Monfort P, Felipo V (2000) Activation of N-methyl-D-aspartate receptors in rat brain in vivo following acute ammonia intoxication: characterization by in vivo brain microdialysis. Hepatology 31:709–715. doi:10.​1002/​hep.​510310322 PubMedCrossRef
Zurück zum Zitat Jalan R, Kapoor D (2003) Enhanced renal ammonia excretion following volume expansion in patients with well compensated cirrhosis of the liver. Gut 52:1041–1045PubMedPubMedCentralCrossRef Jalan R, Kapoor D (2003) Enhanced renal ammonia excretion following volume expansion in patients with well compensated cirrhosis of the liver. Gut 52:1041–1045PubMedPubMedCentralCrossRef
Zurück zum Zitat Jones EA (2003) Potential mechanisms of enhanced GABA-mediated inhibitory neurotransmission in liver failure. Neurochem Int 43:509–516PubMedCrossRef Jones EA (2003) Potential mechanisms of enhanced GABA-mediated inhibitory neurotransmission in liver failure. Neurochem Int 43:509–516PubMedCrossRef
Zurück zum Zitat Kircheis G, Wettstein M, Dahl S, Haussinger D (2002) Clinical efficacy of L-ornithine-L-aspartate in the management of hepatic encephalopathy. Metab Brain Dis 17:453–462PubMedCrossRef Kircheis G, Wettstein M, Dahl S, Haussinger D (2002) Clinical efficacy of L-ornithine-L-aspartate in the management of hepatic encephalopathy. Metab Brain Dis 17:453–462PubMedCrossRef
Zurück zum Zitat Maffeo E, Montuschi A, Stura G, Giordana MT (2014) Chronic acquired hepatocerebral degeneration, pallidal T1 MRI hyperintensity and manganese in a series of cirrhotic patients. Neurol Sci 35:523–530. doi:10.1007/s10072-013-1458-x PubMedCrossRef Maffeo E, Montuschi A, Stura G, Giordana MT (2014) Chronic acquired hepatocerebral degeneration, pallidal T1 MRI hyperintensity and manganese in a series of cirrhotic patients. Neurol Sci 35:523–530. doi:10.​1007/​s10072-013-1458-x PubMedCrossRef
Zurück zum Zitat Marchesini G et al (2003) Nutritional supplementation with branched-chain amino acids in advanced cirrhosis: a double-blind, randomized trial. Gastroenterology 124:1792–1801PubMedCrossRef Marchesini G et al (2003) Nutritional supplementation with branched-chain amino acids in advanced cirrhosis: a double-blind, randomized trial. Gastroenterology 124:1792–1801PubMedCrossRef
Zurück zum Zitat Martinez-Hernandez A, Bell KP, Norenberg MD (1977) Glutamine synthetase: glial localization in brain. Science 195:1356–1358PubMedCrossRef Martinez-Hernandez A, Bell KP, Norenberg MD (1977) Glutamine synthetase: glial localization in brain. Science 195:1356–1358PubMedCrossRef
Zurück zum Zitat Muto Y et al (2005) Effects of oral branched-chain amino acid granules on event-free survival in patients with liver cirrhosis. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc 3:705–713 Muto Y et al (2005) Effects of oral branched-chain amino acid granules on event-free survival in patients with liver cirrhosis. Clin Gastroenterol Hepatol Off Clin Pract J Am Gastroenterol Assoc 3:705–713
Zurück zum Zitat Nagaraja TN, Brookes N (1998) Intracellular acidification induced by passive and active transport of ammonium ions in astrocytes. Am J Physiol 274:C883–C891PubMed Nagaraja TN, Brookes N (1998) Intracellular acidification induced by passive and active transport of ammonium ions in astrocytes. Am J Physiol 274:C883–C891PubMed
Zurück zum Zitat Olde Damink SW, Deutz NE, Dejong CH, Soeters PB, Jalan R (2002) Interorgan ammonia metabolism in liver failure. Neurochem Int 41:177–188PubMedCrossRef Olde Damink SW, Deutz NE, Dejong CH, Soeters PB, Jalan R (2002) Interorgan ammonia metabolism in liver failure. Neurochem Int 41:177–188PubMedCrossRef
Zurück zum Zitat Ong JP et al (2003) Correlation between ammonia levels and the severity of hepatic encephalopathy. Am J Med 114:188–193PubMedCrossRef Ong JP et al (2003) Correlation between ammonia levels and the severity of hepatic encephalopathy. Am J Med 114:188–193PubMedCrossRef
Zurück zum Zitat Patel V et al (2014) Rifaximin is efficacious in the treatment of chronic overt hepatic encephalopathy: a UK liver multi-centre experience. Gut 63(Suppl 1):A14–A15. doi:10.1136/gutjnl-2014-307263.29 Patel V et al (2014) Rifaximin is efficacious in the treatment of chronic overt hepatic encephalopathy: a UK liver multi-centre experience. Gut 63(Suppl 1):A14–A15. doi:10.​1136/​gutjnl-2014-307263.​29
Zurück zum Zitat Plauth M et al (1993) Long-term treatment of latent portosystemic encephalopathy with branched-chain amino acids. A double-blind placebo-controlled crossover study. J Hepatol 17:308–314PubMedCrossRef Plauth M et al (1993) Long-term treatment of latent portosystemic encephalopathy with branched-chain amino acids. A double-blind placebo-controlled crossover study. J Hepatol 17:308–314PubMedCrossRef
Zurück zum Zitat Pomier-Layrargues G, Spahr L, Butterworth RF (1995) Increased manganese concentrations in pallidum of cirrhotic patients. Lancet 345:735PubMedCrossRef Pomier-Layrargues G, Spahr L, Butterworth RF (1995) Increased manganese concentrations in pallidum of cirrhotic patients. Lancet 345:735PubMedCrossRef
Zurück zum Zitat Poo JL et al (2006) Efficacy of oral L-ornithine-L-aspartate in cirrhotic patients with hyperammonemic hepatic encephalopathy. Results of a randomized, lactulose-controlled study. Ann Hepatol 5:281–288PubMed Poo JL et al (2006) Efficacy of oral L-ornithine-L-aspartate in cirrhotic patients with hyperammonemic hepatic encephalopathy. Results of a randomized, lactulose-controlled study. Ann Hepatol 5:281–288PubMed
Zurück zum Zitat Prasad S, Dhiman RK, Duseja A, Chawla YK, Sharma A, Agarwal R (2007) Lactulose improves cognitive functions and health-related quality of life in patients with cirrhosis who have minimal hepatic encephalopathy. Hepatology 45:549–559. doi:10.1002/hep.21533 PubMedCrossRef Prasad S, Dhiman RK, Duseja A, Chawla YK, Sharma A, Agarwal R (2007) Lactulose improves cognitive functions and health-related quality of life in patients with cirrhosis who have minimal hepatic encephalopathy. Hepatology 45:549–559. doi:10.​1002/​hep.​21533 PubMedCrossRef
Zurück zum Zitat Romero LI, Tatro JB, Field JA, Reichlin S (1996) Roles of IL-1 and TNF-alpha in endotoxin-induced activation of nitric oxide synthase in cultured rat brain cells. Am J Physiol 270:R326–R332PubMed Romero LI, Tatro JB, Field JA, Reichlin S (1996) Roles of IL-1 and TNF-alpha in endotoxin-induced activation of nitric oxide synthase in cultured rat brain cells. Am J Physiol 270:R326–R332PubMed
Zurück zum Zitat Romero-Gomez M, Ramos-Guerrero R, Grande L, de Teran LC, Corpas R, Camacho I, Bautista JD (2004) Intestinal glutaminase activity is increased in liver cirrhosis and correlates with minimal hepatic encephalopathy. J Hepatol 41:49–54. doi:10.1016/j.jhep.2004.03.021 PubMedCrossRef Romero-Gomez M, Ramos-Guerrero R, Grande L, de Teran LC, Corpas R, Camacho I, Bautista JD (2004) Intestinal glutaminase activity is increased in liver cirrhosis and correlates with minimal hepatic encephalopathy. J Hepatol 41:49–54. doi:10.​1016/​j.​jhep.​2004.​03.​021 PubMedCrossRef
Zurück zum Zitat Rose C, Michalak A, Pannunzio P, Therrien G, Quack G, Kircheis G, Butterworth RF (1998) L-ornithine-L-aspartate in experimental portal-systemic encephalopathy: therapeutic efficacy and mechanism of action. Metab Brain Dis 13:147–157PubMedCrossRef Rose C, Michalak A, Pannunzio P, Therrien G, Quack G, Kircheis G, Butterworth RF (1998) L-ornithine-L-aspartate in experimental portal-systemic encephalopathy: therapeutic efficacy and mechanism of action. Metab Brain Dis 13:147–157PubMedCrossRef
Zurück zum Zitat Shawcross DL, Davies NA, Williams R, Jalan R (2004) Systemic inflammatory response exacerbates the neuropsychological effects of induced hyperammonemia in cirrhosis. J Hepatol 40:247–254PubMedCrossRef Shawcross DL, Davies NA, Williams R, Jalan R (2004) Systemic inflammatory response exacerbates the neuropsychological effects of induced hyperammonemia in cirrhosis. J Hepatol 40:247–254PubMedCrossRef
Zurück zum Zitat Sidhu SS, Goyal O, Mishra BP, Sood A, Chhina RS, Soni RK (2011) Rifaximin improves psychometric performance and health-related quality of life in patients with minimal hepatic encephalopathy (the RIME Trial). Am J Gastroenterol 106:307–316. doi:10.1038/ajg.2010.455 PubMedCrossRef Sidhu SS, Goyal O, Mishra BP, Sood A, Chhina RS, Soni RK (2011) Rifaximin improves psychometric performance and health-related quality of life in patients with minimal hepatic encephalopathy (the RIME Trial). Am J Gastroenterol 106:307–316. doi:10.​1038/​ajg.​2010.​455 PubMedCrossRef
Zurück zum Zitat Streetz K et al (2000) Tumor necrosis factor alpha in the pathogenesis of human and murine fulminant hepatic failure. Gastroenterology 119:446–460PubMedCrossRef Streetz K et al (2000) Tumor necrosis factor alpha in the pathogenesis of human and murine fulminant hepatic failure. Gastroenterology 119:446–460PubMedCrossRef
Zurück zum Zitat Takada Y et al (2001) Increased intracranial pressure in a porcine model of fulminant hepatic failure using amatoxin and endotoxin. J Hepatol 34:825–831PubMedCrossRef Takada Y et al (2001) Increased intracranial pressure in a porcine model of fulminant hepatic failure using amatoxin and endotoxin. J Hepatol 34:825–831PubMedCrossRef
Zurück zum Zitat Taylor NJ et al (2014) The severity of circulating neutrophil dysfunction in patients with cirrhosis is associated with 90-day and 1-year mortality. Aliment Pharmacol Ther 40:705–715. doi:10.1111/apt.12886 PubMedCrossRef Taylor NJ et al (2014) The severity of circulating neutrophil dysfunction in patients with cirrhosis is associated with 90-day and 1-year mortality. Aliment Pharmacol Ther 40:705–715. doi:10.​1111/​apt.​12886 PubMedCrossRef
Zurück zum Zitat Vilstrup H et al (2014) Hepatic encephalopathy in chronic liver disease: 2014 practice guideline by the American association for the study of liver diseases and the european association for the study of the liver. Hepatology 60:715–735. doi:10.1002/hep.27210 PubMedCrossRef Vilstrup H et al (2014) Hepatic encephalopathy in chronic liver disease: 2014 practice guideline by the American association for the study of liver diseases and the european association for the study of the liver. Hepatology 60:715–735. doi:10.​1002/​hep.​27210 PubMedCrossRef
Zurück zum Zitat Xu J, Ma R, Chen LF, Zhao LJ, Chen K, Zhang RB (2014) Effects of probiotic therapy on hepatic encephalopathy in patients with liver cirrhosis: an updated meta-analysis of six randomized controlled trials. Hepatobiliary Pancreat Dis Int: HBPD INT 13:354–360PubMedCrossRef Xu J, Ma R, Chen LF, Zhao LJ, Chen K, Zhang RB (2014) Effects of probiotic therapy on hepatic encephalopathy in patients with liver cirrhosis: an updated meta-analysis of six randomized controlled trials. Hepatobiliary Pancreat Dis Int: HBPD INT 13:354–360PubMedCrossRef
Zurück zum Zitat Yoshida Y, Higashi T, Nouso K, Nakatsukasa H, Nakamura SI, Watanabe A, Tsuji T (2001) Effects of zinc deficiency/zinc supplementation on ammonia metabolism in patients with decompensated liver cirrhosis. Acta Med Okayama 55:349–355PubMed Yoshida Y, Higashi T, Nouso K, Nakatsukasa H, Nakamura SI, Watanabe A, Tsuji T (2001) Effects of zinc deficiency/zinc supplementation on ammonia metabolism in patients with decompensated liver cirrhosis. Acta Med Okayama 55:349–355PubMed
Zurück zum Zitat Ytrebo LM et al (2009) L-ornithine phenylacetate attenuates increased arterial and extracellular brain ammonia and prevents intracranial hypertension in pigs with acute liver failure. Hepatology 50:165–174. doi:10.1002/hep.22917 PubMedCrossRef Ytrebo LM et al (2009) L-ornithine phenylacetate attenuates increased arterial and extracellular brain ammonia and prevents intracranial hypertension in pigs with acute liver failure. Hepatology 50:165–174. doi:10.​1002/​hep.​22917 PubMedCrossRef
Metadaten
Titel
Clinical science workshop: targeting the gut-liver-brain axis
verfasst von
Vishal C. Patel
Helen White
Sidsel Støy
Jasmohan S. Bajaj
Debbie L. Shawcross
Publikationsdatum
08.10.2015
Verlag
Springer US
Erschienen in
Metabolic Brain Disease / Ausgabe 6/2016
Print ISSN: 0885-7490
Elektronische ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-015-9743-4

Weitere Artikel der Ausgabe 6/2016

Metabolic Brain Disease 6/2016 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.