Human serum albumin, systemic inflammation, and cirrhosis

Journal of Hepatology

Volumn 61, Issue 2, 2014, Pages 396-407

  Arroyo, Vicente ^a,b   García Martinez, Rita ^b   Salvatella, Xavier ^c  

^a Centre Esther Koplowitz   (Spain)

^b EASL Cronic Liver Failure Consortium Fundació Clinic   (Spain)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

Acute on chronic liver failure; Cirrhosis; Decompensated cirrhosis; Hepatorenal syndrome; Human serum albumin; Organ inflammation; Oxidative stress; Paracentesis induced circulatory dysfunction; Spontaneous bacterial peritonitis; Systemic inflammation

Indexed keywords

HUMAN SERUM ALBUMIN; VASOPRESSIN DERIVATIVE; SERUM ALBUMIN;

ASCITES; BACTERIAL PERITONITIS; CHEMICAL STRUCTURE; DECOMPENSATED LIVER CIRRHOSIS; DISEASE ASSOCIATION; HEPATORENAL SYNDROME; HUMAN; INFLAMMATION; LIVER METABOLISM; PARACENTESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; THERAPY EFFECT; TREATMENT DURATION; TREATMENT INDICATION; COMPLICATION; LIVER CIRRHOSIS; PERITONITIS;

HEPATORENAL SYNDROME; HUMANS; INFLAMMATION; LIVER CIRRHOSIS; PERITONITIS; SERUM ALBUMIN;

EID: 84904753993     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.04.012     Document Type: Review

References (154)

1. R. Moreau, R. Jalan, P. Ginès, M. Pavesi, P. Angeli, and J. Cordoba et al. Acute-on-chronic liver failure is a distinct syndrome that develops in patients with acute decompensation of cirrhosis Gastroenterology 144 2013 1426 1437
2. T. Peters Jr. All about albumin. Biochemistry and medical applications 1966 Academic Press Inc San Diego
3. G.W. Thorn, S.H. Armstrong Jr., and V.D. Davenport Chemical, clinical, and immunological studies on the products of human plasma fractionation. XXXI. The use of salt-poor concentrated human serum albumin solution in the treatment of hepatic cirrhosis J Clin Invest 25 1946 304 323
4. H.G. Kunkel, D.H. Labby, E.H. Ahrens, R.E. Shank, and C.L. Hoagland The use of concentrated human serum albumin in the treatment of cirrhosis of the liver J Clin Invest 27 1948 305 319
5. W.W. Faloon, R.D. Eckhardt, T. Lynch Murphy, A.M. Cooper, and C.S. Davidson An evaluation of human serum albumin in the treatment of cirrhosis of the liver J Clin Invest 28 1949 583 594
6. R. Hecker, and S. Sherlock Electrolyte and circulatory changes in terminal liver failure Lancet 271 1956 1121 1125
7. H. Traverso, P. Vesin, A. Combrisson, P. Besson, and R. Cattan Intravenous albumin loading in ascitic cirrhosis. Biological study Sem Hop 40 1964 17 20
8. S. Wapnick, S. Grosberg, M. Kinney, V. Azzara, and H.H. LeVeen Renal failure in ascites secondary to hepatic, renal, and pancreatic disease. Treatment with a LeVeen peritoneovenous shunt Arch Surg 113 1978 581 585
9. P. Ginès, V. Arroyo, E. Quintero, R. Planas, F. Bory, and J. Cabrera et al. Comparison of paracentesis and diuretics in the treatment of cirrhotics with tense ascites. Results of a randomized study Gastroenterology 93 1987 234 241
10. L. Titó, P. Ginès, V. Arroyo, R. Planas, J. Panés, and A. Rimola et al. Total paracentesis associated with intravenous albumin management of patients with cirrhosis and ascites Gastroenterology 98 1990 146 151
11. V. Arroyo, A. Ginès, and J. Saló A European survey on the treatment of ascites in cirrhosis J Hepatol 21 1994 667 672
12. P. Ginès, V. Arroyo, V. Vargas, R. Planas, F. Casafont, and J. Panés et al. Paracentesis with intravenous infusion of albumin as compared with peritoneovenous shunting in cirrhosis with refractory ascites N Engl J Med 325 1991 829 835
13. P. Ginès, L. Titó, V. Arroyo, R. Planas, J. Panés, and J. Viver et al. Randomized comparative study of therapeutic paracentesis with and without intravenous albumin in cirrhosis Gastroenterology 94 1988 1493 1502
14. R. Planas, P. Ginès, V. Arroyo, J. Llach, J. Panés, and V. Vargas et al. Dextran-70 vs. albumin as plasma expanders in cirrhotic patients with tense ascites treated with total paracentesis. Results of a randomized study Gastroenterology 99 1990 1736 1744
15. A. Ginès, G. Fernández-Esparrach, A. Monescillo, C. Vila, E. Domènech, and R. Abecasis et al. Randomized trial comparing albumin, dextran 70, and polygeline in cirrhotic patients with ascites treated by paracentesis Gastroenterology 111 1996 1002 1010
16. J. Saló, A. Ginès, P. Ginès, C. Piera, W. Jiménez, and M. Guevara et al. Effect of therapeutic paracentesis on plasma volume and transvascular escape rate of albumin in patients with cirrhosis J Hepatol 27 1997 645 653
17. L. Ruiz-del-Arbol, A. Monescillo, W. Jimenéz, A. Garcia-Plaza, V. Arroyo, and J. Rodés Paracentesis-induced circulatory dysfunction: mechanism and effect on hepatic hemodynamics in cirrhosis Gastroenterology 113 1997 579 586
18. M.C. Vila, R. Solà, L. Molina, M. Andreu, S. Coll, and J. Gana et al. Hemodynamic changes in patients developing effective hypovolemia after total paracentesis J Hepatol 28 1998 639 645
19. M. Bernardi, P. Caraceni, R.J. Navickis, and M.M. Wilkes Albumin infusion in patients undergoing large-volume paracentesis: a meta-analysis of randomized trials Hepatology 55 2012 1172 1181
20. A. Follo, J.M. Llovet, M. Navasa, R. Planas, X. Forns, and A. Francitorra et al. Renal impairment after spontaneous bacterial peritonitis in cirrhosis: incidence, clinical course, predictive factors and prognosis Hepatology 20 1994 1495 1501
21. L. Ruiz-del-Arbol, J. Urman, J. Fernández, M. González, M. Navasa, and A. Monescillo et al. Systemic, renal, and hepatic hemodynamic derangement in cirrhotic patients with spontaneous bacterial peritonitis Hepatology 38 2003 1210 1218
22. S. Fasolato, P. Angeli, L. Dallagnese, G. Maresio, E. Zola, and E. Mazza et al. Renal failure and bacterial infections in patients with cirrhosis: epidemiology and clinical features Hepatology 45 2007 223 229
23. M. Navasa, A. Follo, X. Filella, W. Jiménez, A. Francitorra, and R. Planas et al. Tumor necrosis factor and interleukin-6 in spontaneous bacterial peritonitis in cirrhosis: relationship with the development of renal impairment and mortality Hepatology 27 1998 1227 1232
24. C. Terra, M. Guevara, A. Torre, R. Gilabert, J. Fernández, and M. Martín-Llahí et al. Renal failure in patients with cirrhosis and sepsis unrelated to spontaneous bacterial peritonitis: value of MELD score Gastroenterology 129 2005 1944 1953
25. G. Pereira, M. Guevara, C. Fagundes, E. Solá, E. Rodríguez, and J. Fernández et al. Renal failure and hyponatremia in patients with cirrhosis and skin and soft tissue infection. A retrospective study J Hepatol 56 2012 1040 1046
26. B. Byl, I. Roucloux, A. Crusiaux, E. Dupont, and J. Devière Tumor necrosis factor alpha and interleukin 6 plasma levels in infected cirrhotic patients Gastroenterology 104 1993 1492 1497
27. M.J. Ramírez, A. Ibáñez, M. Navasa, E. Casals, M. Morales-Ruiz, and W. Jiménez et al. High-density lipoproteins reduce the effect of endotoxin on cytokine production and systemic hemodynamics in cirrhotic rats with ascites J Hepatol 40 2004 424 430
28. R.W. Schrier, V. Arroyo, M. Bernardi, M. Epstein, J.H. Henriksen, and J. Rodés Peripheral arterial vasodilation hypothesis: a proposal for the initiation of renal sodium and water retention in cirrhosis Hepatology 8 1988 1151 1157
29. A. Ginès, A. Escorsell, P. Ginès, J. Saló, W. Jiménez, and L. Inglada et al. Incidence, predictive factors, and prognosis of the hepatorenal syndrome in cirrhosis with ascites Gastroenterology 105 1993 229 236
30. J. Fernández, M. Navasa, R. Planas, S. Montoliu, D. Monfort, and G. Soriano et al. Primary prophylaxis of spontaneous bacterial peritonitis delays hepatorenal syndrome and improves survival in cirrhosis Gastroenterology 133 2007 818 824
31. P. Sort, M. Navasa, V. Arroyo, X. Aldeguer, R. Planas, and L. Ruiz-del-Arbol et al. Effect of intravenous albumin on renal impairment and mortality in patients with cirrhosis and spontaneous bacterial peritonitis N Engl J Med 341 1999 403 409
32. F. Salerno, R.J. Navickis, and M.M. Wilkes Albumin infusion improves outcomes of patients with spontaneous bacterial peritonitis: a meta-analysis of randomized trials Clin Gastroenterol Hepatol 11 2013 123 130
33. M.D. Shapiro, K.M. Nicholls, B.M. Groves, R. Kluge, H.M. Chung, and D.G. Bichet et al. Interrelationship between cardiac output and vascular resistance as determinants of effective arterial blood volume in cirrhotic patients Kidney Int 28 1985 206 211
34. M. Guevara, P. Ginès, G. Fernández-Esparrach, P. Sort, J.M. Salmerón, and W. Jiménez et al. Reversibility of hepatorenal syndrome by prolonged administration of ornipressin and plasma volume expansion Hepatology 27 1998 35 41
35. J. Uriz, P. Ginès, A. Cárdenas, P. Sort, W. Jiménez, and J.M. Salmerón et al. Terlipressin plus albumin infusion: an effective and safe therapy of hepatorenal syndrome J Hepatol 33 2000 43 48
36. P. Ginès, A. Cárdenas, V. Arroyo, and J. Rodés Management of cirrhosis and ascites N Engl J Med 350 2004 1646 1654
37. G. Garcia-Tsao, and J.K. Lim Members of Veterans Affairs Hepatitis C Resource Center Program. Management and treatment of patients with cirrhosis and portal hypertension: recommendations from the Department of Veterans Affairs Hepatitis C Resource Center Program and the National Hepatitis C Program Am J Gastroenterol 104 2009 1802 1829
38. P. Ginès, P. Angeli, K. Lenz, S. Møller, K. Moore, and R. Moreau et al. EASL clinical practice guidelines on the management of ascites, spontaneous bacterial peritonitis, and hepatorenal syndrome in cirrhosis J Hepatol 53 2010 397 417
39. P. Angeli, S. Fasolato, M. Cavallin, E. Trotta, G. Maresio, and A. Callegaro et al. Terlipressin given as continuous intravenous infusion vs. terlipressin given as intravenous boluses in the treatment of type 1 hepatorenal syndrome (HRS) in patients with cirrhosis J Hepatol 50 2009 S73
40. T.D. Boyer, A.J. Sanyal, G. Garcia-Tsao, A. Blei, D. Carl, and A.S. Bexon et al. Predictors of response to terlipressin plus albumin in hepatorenal syndrome (HRS) type 1: relationship of serum creatinine to hemodynamics J Hepatol 55 2011 315 321
41. J.C. Velez, and P.J. Nietert Therapeutic response to vasoconstrictors in hepatorenal syndrome parallels increase in mean arterial pressure: a pooled analysis of clinical trials Am J Kidney Dis 58 2011 928 938
42. A. Nazar, G.H. Pereira, M. Guevara, M. Martín-Llahi, M.N. Pepin, and M. Marinelli et al. Predictors of response to therapy with terlipressin and albumin in patients with cirrhosis and type 1 hepatorenal syndrome Hepatology 51 2010 219 226
43. R. Moreau, F. Durand, T. Poynard, C. Duhamel, J.P. Cervoni, and P. Ichaï et al. Terlipressin in patients with cirrhosis and type 1 hepatorenal syndrome: a retrospective multicenter study Gastroenterology 122 2002 923 930
44. V. Arroyo, and J. Fernández Management of hepatorenal syndrome in patients with cirrhosis Nat Rev Nephrol 7 2011 517 526
45. C. Alessandria, A. Ottobrelli, W. Debernardi-Venon, L. Todros, M.T. Cerenzia, and S. Martini et al. Noradrenalin vs. terlipressin in patients with hepatorenal syndrome: a prospective, randomized, unblinded, pilot study J Hepatol 47 2007 499 505
46. P. Sharma, A. Kumar, B.C. Shrama, and S.K. Sarin An open label, pilot, randomized controlled trial of noradrenaline vs. terlipressin in the treatment of type 1 hepatorenal syndrome and predictors of response Am J Gastroenterol 103 2008 1689 1697
47. V. Singh, S. Ghosh, B. Singh, P. Kumar, N. Sharma, and A. Bhalla et al. Noradrenaline vs. terlipressin in the treatment of hepatorenal syndrome: a randomized study J Hepatol 56 2012 1293 1298
48. R. Ortega, P. Ginès, J. Uriz, A. Cárdenas, B. Calahorra, and D. De Las Heras et al. Terlipressin therapy with and without albumin for patients with hepatorenal syndrome: results of a prospective, nonrandomized study Hepatology 36 2002 941 948
49. M. Martín-Llahí, M.N. Pépin, M. Guevara, F. Díaz, A. Torre, and A. Monescillo et al. Terlipressin and albumin vs. albumin in patients with cirrhosis and hepatorenal syndrome: a randomized study Gastroenterology 134 2008 1352 1359
50. A.J. Sanyal, T. Boyer, G. Garcia-Tsao, F. Regenstein, L. Rossaro, and B. Appenrodt et al. A randomized, prospective, double-blind, placebo-controlled trial of terlipressin for type 1 hepatorenal syndrome Gastroenterology 134 2008 1360 1368
51. J.M. Péron, C. Bureau, L. Gonzalez, F. Garcia-Ricard, O. de Soyres, and E. Dupuis et al. Treatment of hepatorenal syndrome as defined by the international ascites club by albumin and furosemide infusion according to the central venous pressure: a prospective pilot study Am J Gastroenterol 100 2005 2702 2707
52. E. Rodríguez, C. Elia, E. Solà, R. Barreto, I. Graupera, and A. Andrealli et al. Terlipressin and albumin for type-1 hepatorenal syndrome associated with sepsis J Hepatol 60 2014 955 961 [pii: S0168-8278[14]00055-5, Epub ahead of print]
53. C. Alessandria, W.D. Venon, A. Marzano, C. Barletti, M. Fadda, and M. Rizzetto Renal failure in cirrhotic patients: role of terlipressin in clinical approach to hepatorenal syndrome type 2 Eur J Gastroenterol Hepatol 14 2002 1363 1368
54. K. Tarao, and K. Iwamura Influence of long-term administration of serum albumin on the prognosis of liver cirrhosis in man Tokai J Exp Clin Med 8 1983 71 78
55. P. Gentilini, V. Casini-Raggi, G. Di Fiore, R.G. Romanelli, G. Buzzelli, and M. Pinzani et al. Albumin improves the response to diuretics in patients with cirrhosis and ascites: results of a randomized, controlled trial J Hepatol 30 1999 639 645
56. M. Guevara, C. Terra, A. Nazar, E. Solà, J. Fernández, and M. Pavesi et al. Albumin for bacterial infections other than spontaneous bacterial peritonitis in cirrhosis. A randomized, controlled study J Hepatol 57 2012 759 765
57. X.M. He, and D.C. Carter Atomic structure and chemistry of human serum albumin Nature 358 1992 209 215
58. K. Oettl, R. Birner-Gruenberger, W. Spindelboeck, H.P. Stueger, L. Dorn, and V. Stadlbauer Oxidative albumin damage in chronic liver failure: relation to albumin binding capacity, liver dysfunction and survival J Hepatol 59 2013 978 983
59. M. Anraku, V.T.G. Chuang, T. Maruyama, and M. Otagiri Redox properties of serum albumin Biochim Biophys Acta 1830 2013 5465 5472
60. D.C. Carter, X.M. He, S.H. Munson, P.D. Twigg, K.M. Gernert, and M.B. Broom et al. Three-dimensional structure of human serum albumin Science 244 1989 1195 1198
61. A.A. Bhattacharya, T. Grüne, and S. Curry Crystallographic analysis reveals common modes of binding of medium and long-chain fatty acids to HSA J Mol Biol 303 2000 721 732
62. H. Mao, A.H. Gunasekera, and S.W. Fesik Expression, refolding, and isotopic labeling of human serum albumin domains for NMR spectroscopy Protein Expr Purif 20 2000 492 499
63. J. Milojevic, and G. Melacini Stoichiometry and affinity of the human serum albumin-Alzheimer's Aβ peptide interactions Biophys J 100 2011 183 192
64. S.J. Burton, A.V. Quirk, and P.C. Wood Refolding human serum albumin at relatively high protein concentration Eur J Biochem 179 1989 379 387
65. Z. Chen, Y. He, B. Shi, and D. Yang Human serum albumin from recombinant DNA technology: challenges and strategies Biochim Biophys Acta 1830 2013 5515 5525
66. A. Hvidt, and K. Wallevik Conformational changes in human serum albumin as revealed by hydrogen-deuterium exchange studies J Biol Chem 247 1972 1530 1535
67. A.A. Bhattacharya, T. Grüne, and S. Curry Crystallographic analysis reveals common modes of binding of medium and long-chain fatty acids to human serum albumin J Mol Biol 303 2000 721 732
68. J. Ghuman, P.A. Zunszain, I. Petitpas, A.A. Bhattacharya, M. Otagiri, and S. Curry Structural basis of the drug-binding specificity of human serum albumin J Mol Biol 353 2005 38 52
69. K. Yamasaki, V.T.G. Chuang, T. Maruyama, and M. Otagiri Albumin-drug interaction and its clinical implication Biochim Biophys Acta 1830 2013 5435 5443
70. G. Fanali, G. Pariani, P. Ascenzi, and M. Fasano Allosteric and binding properties of Asp1-Glu382 truncated recombinant human serum albumin - an optical and NMR spectroscopic investigation FEBS J 276 2009 2241 2250
71. V.J. Hilser, and E.B. Thompson Structural dynamics, intrinsic disorder, and allostery in nuclear receptors as transcription factors J Biol Chem 286 2011 39675 39682
72. R. Jalan, K. Schnurr, R.P. Mookerjee, S. Sen, L. Cheshire, and S. Hodges et al. Alterations in the functional capacity of albumin in patients with decompensated cirrhosis is associated with increased mortality Hepatology 50 2009 555 564
73. N. Furusyo, and J. Hayashi Glycated albumin and diabetes mellitus Biochim Biophys Acta 1830 2013 5509 5514
74. A. Kawakami, K. Kubota, N. Yamada, U. Tagami, K. Takehana, and I. Sonaka et al. Identification and characterization of oxidized human serum albumin. A slight structural change impairs its ligand-binding and antioxidant functions FEBS J 273 2006 3346 3357
75. J.E. Schnitzer, and P. Oh Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins J Biol Chem 269 1994 6072 6082
76. R.D. Minshall, Ch. Tiruppathi, S.M. Vogel, and A.B. Malik Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function Histochem Cell Biol 117 2002 105 112
77. A.B. Malik Targeting endothelial cell surface receptors: novel mechanisms of microvascular endothelial barrier transport J Med Sci 2 2009 13 17
78. D. Sleep, J. Cameron, and L.R. Evans Albumin as a versatile platform for drug half-life extension Biochim Biophys Acta 1830 2013 5526 5534
79. N. Ghinea, A. Fixman, D. Alexandru, D. Popov, M. Hasu, and L. Ghitescu Identification of albumin-binding proteins in capillary endothelial cells J Cell Biol 107 1988 231 239
80. J.E. Schnitzer, A. Sung, R. Horvat, and J. Bravo Preferential interaction of albumin-binding proteins, gp30 and gp18, with conformationally modified albumins. Presence in many cells and tissues with a possible role in catabolism J Biol Chem 267 1992 24544 24553
81. J.E. Schnitzer, and J. Bravo High affinity binding, endocytosis, and degradation of conformationally modified albumins. Potential role of gp30 and gp18 as novel scavenger receptors J Biol Chem 268 1993 7562 7570
82. J.T. Andersen, M.B. Daba, G. Berntzen, T.E. Michaelsen, and I. Sandlie Cross-species binding analyses of mouse and human neonatal Fc receptor show dramatic differences in immunoglobulin G and albumin binding J Biol Chem 285 2010 4826 4836
83. J.T. Andersen, R. Pehrson, V. Tolmachev, M.B. Daba, L. Abrahmsén, and C. Ekblad Extending half-life by indirect targeting of the neonatal Fc receptor (FcRn) using a minimal albumin binding domain J Biol Chem 286 2011 5234 5241
84. B.J. Smith, A. Popplewell, D. Athwal, A.P. Chapman, S. Heywood, and M. Shauna et al. Prolonged in vivo residence times of antibody fragments associated with albumin Bioconjug Chem 12 2001 750 756
85. S. Fujiwara, and T. Amisaki Fatty acid binding to serum albumin: molecular simulation approaches Biochim Biophys Acta 1830 2013 5427 5434
86. G.J. Van der Vusse Albumin as fatty acid transporter Drug Metab Pharmacokinet 24 2009 300 307
87. C.E. Petersen, C.E. Ha, K. Harohalli, J.B. Feix, and N.V. Bhagavan A dynamic model for bilirubin binding to human serum albumin J Biol Chem 275 2000 20985 20995
88. C.E. Ha, and N.V. Bhagavan Novel insights into the pleiotropic effects of human serum albumin in health and disease Biochim Biophys Acta 1830 2013 5486 5493
89. Z.M. Wang, J.X. Ho, J.R. Ruble, J. Rose, F. Rüker, and M. Ellenburg et al. Structural studies of several clinically important oncology drugs in complex with human serum albumin Biochim Biophys Acta 1830 2013 5356 5374
90. S. Klammt, H.J. Wojak, A. Mitzner, S. Koball, J. Rychly, and E.C. Reisinger et al. Albumin-binding capacity (ABiC) is reduced in patients with chronic kidney disease along with an accumulation of protein-bound uraemic toxins Nephrol Dial Transplant 27 2012 2377 2383
91. S. Klammt, S. Mitzner, J. Stange, B. Brinkmann, B. Drewelow, and J. Emmrich et al. Albumin-binding function is reduced in patients with decompensated cirrhosis and correlates inversely with severity of liver disease assessed by model for end-stage liver disease Eur J Gastroenterol Hepatol 19 2007 257 263
92. G. Fanali, A. di Massi, V. Trezza, M. Marino, M. Fasano, and P. Ascenzi Human serum albumin: from bench to bedside Mol Aspects Med 33 2012 209 290
93. D.A. Smith, L. Di, and E.H. Kerns The effect of plasma protein binding on in vivo efficacy: misconceptions in drug discovery Nat Rev Drug Discov 9 2010 929 939
94. G. Jurgens, M. Muller, P. Garidel, M.H. Koch, H. Nakakubo, and A. Blume et al. Investigation into the interaction of recombinant human serum albumin with Re-lipopolysaccharide and lipid A J Endotoxin Res 8 2002 115 126
95. H. Fukui Relation of endotoxin, endotoxin binding proteins and macrophages to severe alcoholic liver injury and multiple organ failure Alcohol Clin Exp Res 29 2005 172S 179S
96. R. Dziarski Cell-bound albumin is the 70-kDa peptidoglycan-, lipopolysaccharide-, and lipoteichoic acid-binding protein on lymphocytes and macrophages J Biol Chem 269 1994 20431 20436
97. S.A. David, P. Balaram, and V.I. Mathan Characterization of the interaction of lipid A and lipopolysaccharide with human serum albumin: implications for an endotoxin carrier function for albumin J Endotoxin Res 2 1995 99 106
98. T.L. Gioannini, D. Zhang, A. Teghanemt, and J.P. Weiss An essential role for albumin in the interaction of endotoxin with lipopolysaccharide-binding protein and sCD14 and resultant cell activation J Biol Chem 277 2002 47818 47825
99. A.L. Blomkalns, L.L. Stoll, W. Shaheen, S.A. Romig-Martin, E.W. Dickson, and N.L. Weintraub et al. Low level bacterial endotoxin activates two distinct signaling pathways in human peripheral blood mononuclear cells J Inflamm (Lond) 8 2011 4
100. G.A. Esparza, A. Teghanemt, D. Zhang, T.L. Gioannini, and J.P. Weiss Endotoxin{middle dot}albumin complexes transfer endotoxin monomers to MD-2 resulting in activation of TLR4 Innate Immun 18 2012 478 491
101. O. Takeuchi, and S. Akira Pattern recognition receptors and inflammation Cell 140 2010 805 820
102. J.K. Chan, J. Roth, J.J. Oppenheim, K.J. Tracey, T. Vogl, and M. Feldmann et al. Alarmins: awaiting a clinical response J Clin Invest 122 2012 2711 2719
103. M. Singer The role of mitochondrial dysfunction in sepsis-induced multi-organ failure Virulence 5 2014 66 72
104. H.F. Galley Oxidative stress and mitochondrial dysfunction in sepsis Br J Anaesth 107 2011 57 64
105. H.F. Galley Bench-to-bedside review: targeting antioxidants to mitochondria in sepsis Crit Care 14 2010 230
106. M. Taverna, A.L. Marie, J.P. Mira, and B. Guidet Specific antioxidant properties of human serum albumin Anaesth Intensive Care 3 2013 4
107. M. Bruschi, G. Candiano, L. Santucci, and G.M. Ghiggeri Oxidized albumin. The long way of a protein of uncertain function Biochim Biophys Acta 1830 2013 5473 5479
108. A.M. Cantin, B. Paquette, M. Richter, and P. Larivée Albumin-mediated regulation of cellular glutathione and nuclear factor kappa B activation Am J Respir Crit Care Med 162 2000 1539 1546
109. W. Bal, M. Sokołowska, E. Kurowska, and P. Faller Binding of transition metal ions to albumin: sites, affinities and rates Biochim Biophys Acta 1830 2013 5444 5455
110. S.J. Stohs, and D. Bagchi Oxidative mechanisms in the toxicity of metal ions Free Radic Biol Med 18 1995 321 336
111. J. Neuzil, and R. Stocker Free and albumin-bound bilirubin are efficient co-antioxidants for alpha-tocopherol, inhibiting plasma and low density lipoprotein lipid peroxidation J Biol Chem 269 1994 16712 16719
112. E. Bourdon, N. Loreau, L. Lagrost, and D. Blache Differential effects of cysteine and methionine residues in the antioxidant activity of human serum albumin Free Radic Res 39 2005 15 20
113. B.S. Berlett, and E.R. Stadtman Protein oxidation in aging, disease, and oxidative stress J Biol Chem 272 1997 20313 20316
114. K. Oettl, and G. Marsche Redox state of human serum albumin in terms of cysteine-34 in health and disease Methods Enzymol 474 2010 181 195
115. O. Rafikova, R. Rafikov, and E. Nudler Catalysis of S-nitrosothiols formation by serum albumin: the mechanism and implication in vascular control Proc Natl Acad Sci U S A 99 2002 5913 5918
116. F.A. Fitzpatrick, W.F. Liggett, and M.A. Wynalda Albumin-eicosanoid interactions. A model system to determine their attributes and inhibition J Biol Chem 259 1984 2722 2777
117. U. Kragh-Hansen Molecular and practical aspects of the enzymatic properties of human serum albumin and of albumin-ligand complexes Biochim Biophys Acta 1830 2013 5535 5544
118. J. Yang, C.E. Petersen, C.E. Ha, and N.V. Bhagavan Structural insights into human serum albumin-mediated prostaglandin catalysis Protein Sci 11 2002 538 545
119. M.A. Wynalda, and F.A. Fitzpatrick Albumins stabilize prostaglandin I2 Prostaglandins 20 1980 853 861
120. G. Folco, E. Granström, and H. Kindahl Albumin stabilizes thromboxane A2 FEBS Lett 82 1977 321 324
121. O. Le Moine, T. Soupison, P. Sogni, A. Marchant, R. Moreau, and A. Hadengue et al. Plasma endotoxin and tumor necrosis factor-alpha in the hyperkinetic state of cirrhosis J Hepatol 23 1995 391 395
122. D.J. Bac, W.M. Pruimboom, P.G. Mulder, F.J. Zijlstra, and J.H. Wilson High interleukin-6 production within the peritoneal cavity in decompensated cirrhosis and malignancy-related ascites Liver 15 1995 265 270
123. M. Odeh, E. Sabo, I. Srugo, and A. Oliven Serum levels of tumor necrosis factor-alpha correlate with severity of hepatic encephalopathy due to chronic liver failure Liver Int 24 2004 110 116
124. F.Y. Lee, R.H. Lu, Y.T. Tsai, H.C. Lin, M.C. Hou, and C.P. Li et al. Plasma interleukin-6 levels in patients with cirrhosis. Relationship to endotoxemia, tumor necrosis factor-alpha, and hyperdynamic circulation Scand J Gastroenterol 31 1996 500 505
125. C.P. Li, F.Y. Lee, Y.T. Tsai, H.C. Lin, R.H. Lu, and M.C. Hou et al. Plasma interleukin-8 levels in patients with post-hepatitic cirrhosis: relationship to severity of liver disease, portal hypertension and hyperdynamic circulation J Gastroenterol Hepatol 11 1996 635 640
126. H. Tilg, A. Wilmer, W. Vogel, M. Herold, B. Nölchen, and G. Judmaier et al. Serum levels of cytokines in chronic liver diseases Gastroenterology 103 1992 264 274
127. J. Genesca, A. Gonzalez, R. Segura, R. Catalan, R. Marti, and E. Varela et al. Interleukin-6, nitric oxide, and the clinical and hemodynamic alterations of patients with liver cirrhosis Am J Gastroenterol 94 1999 169 177
128. L. Jain, B.C. Sharma, P. Sharma, S. Srivastava, A. Agrawal, and S.K. Sarin Serum endotoxin and inflammatory mediators in patients with cirrhosis and hepatic encephalopathy Dig Liver Dis 44 2012 1027 1031
129. C. Montoliu, B. Piedrafita, M.A. Serra, J.A. del Olmo, A. Urios, and J.M. Rodrigo et al. IL-6 and IL-18 in blood may discriminate cirrhotic patients with and without minimal hepatic encephalopathy J Clin Gastroenterol 43 2009 272 279
130. A. Albillos, A. de la Hera, M. González, J.L. Moya, J.L. Calleja, and J. Monserrat et al. Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement Hepatology 37 2003 208 217
131. R. Wiest, M. Lawson, and M. Geuking Pathological bacterial translocation in liver cirrhosis J Hepatol 60 2014 197 209
132. R. Wiest Role of sympathetic nervous activity for bacterial translocation in advanced experimental liver cirrhosis Gastroenterol Hepatol 34 2011 102 105
133. R. Wiest, S. Das, G. Cadelina, G. Garcia-Tsao, S. Milstien, and R.J. Groszmann Bacterial translocation in cirrhotic rats stimulates eNOS-derived NO production and impairs mesenteric vascular contractility J Clin Invest 104 1999 1223 1233
134. Y. Iwakiri, and R.J. Groszmann The hyperdynamic circulation of chronic liver diseases: from the patient to the molecule Hepatology 43 2006 S121 S131
135. L. Ruiz-del-Arbol, A. Monescillo, C. Arocena, P. Valer, P. Ginès, and V. Moreira et al. Circulatory function and hepatorenal syndrome in cirrhosis Hepatology 42 2005 439 447
136. A. Krag, F. Bendtsen, and J.H. Henriksen S Møller2. Low cardiac output predicts development of hepatorenal syndrome and survival in patients with cirrhosis and ascites Gut 59 2010 105 110
137. A. Bortoluzzi, G. Ceolotto, E. Gola, A. Sticca, S. Bova, and F. Morando et al. Positive cardiac inotropic effect of albumin infusion in rodents with cirrhosis and ascites: molecular mechanisms Hepatology 57 2013 266 276
138. H. Gomez, C. Ince, D. De Backer, P. Pickkers, D. Payen, and J. Hotchkiss et al. A unified theory of sepsis-induced acute kidney injury: inflammation, microcirculatory dysfunction, bioenergetics, and the tubular cell adaptation to injury Shock 41 2014 3 11
139. M.W. Merx, and C. Weber Sepsis and the heart Circulation 116 2007 793 802
140. I. Coltart, T.H. Tranah, and D.L. Shawcross Inflammation and hepatic encephalopathy Arch Biochem Biophys 536 2013 189 196
141. T.H. Tranah, G.K. Vijay, J.M. Ryan, and D.L. Shawcross Systemic inflammation and ammonia in hepatic encephalopathy Metab Brain Dis 28 2013 1 5
142. A.S. Seyan, R.D. Hughes, and D.L. Shawcross Changing face of hepatic encephalopathy: role of inflammation and oxidative stress World J Gastroenterol 16 2010 3347 3357
143. R.M. Berg, K. Møller, and D.M. Bailey Neuro-oxidative-nitrosative stress in sepsis J Cereb Blood Flow Metab 31 2011 1532 1544
144. R. Garcia-Martinez, and J. Cordoba Liver-induced inflammation hurts the brain J Hepatol 56 2012 515 517
145. M. Guevara, C. Bru, P. Ginès, G. Fernández-Esparrach, P. Sort, and R. Bataller et al. Increased cerebrovascular resistance in cirrhotic patients with ascites Hepatology 28 1998 39 44
146. G. Wright, N.A. Davies, D.L. Shawcross, S.J. Hodges, C. Zwingmann, and H.F. Brooks et al. Endotoxemia produces coma and brain swelling in bile duct ligated rats Hepatology 45 2007 1517 1526
147. D.L. Shawcross, N.A. Davies, R. Williams, and R. Jalan Systemic inflammatory response exacerbates the neuropsychological effects of induced hyperammonemia in cirrhosis J Hepatol 40 2004 247 254
148. D.L. Shawcross, Y. Sharifi, J.B. Canavan, A.D. Yeoman, R.D. Abeles, and N.J. Taylor et al. Infection and systemic inflammation, not ammonia, are associated with Grade 3/4 hepatic encephalopathy, but not mortality in cirrhosis J Hepatol 54 2011 640 649
149. J. Cordoba, M. Ventura-Cots, M. Simón-Talero, A. Amorós, M. Pavesi, and H. Vilstrup et al. Characteristics, risk factors, and mortality of cirrhotic patients hospitalized for hepatic encephalopathy with and without acute-on-chronic liver failure (ACLF) J Hepatol 60 2014 275 281
150. J. Fernández, M. Navasa, J.C. Garcia-Pagan, J. G-Abraldes, W. Jiménez, and J. Bosch et al. Effect of intravenous albumin on systemic and hepatic hemodynamics and vasoactive neurohormonal systems in patients with cirrhosis and spontaneous bacterial peritonitis J Hepatol 41 2004 384 390
151. J. Fernández, J. Monteagudo, X. Bargallo, W. Jiménez, J. Bosch, and V. Arroyo et al. A randomized unblinded pilot study comparing albúmina vs. hydroxyethyl starch in spontaneous bacterial peritonitis Hepatology 42 2005 627 634
152. M. Ferlitsch, T. Reiberger, M. Hoke, P. Salzl, B. Schwengerer, and G. Ulbrich et al. Von Willebrand factor as new noninvasive predictor of portal hypertension, decompensation and mortality in patients with liver cirrhosis Hepatology 56 2012 1439 1447
153. L. Albornoz, D. Alvarez, J.C. Otaso, A. Gadano, J. Salviú, and S. Gerona et al. Von Willebrand factor could be an index of endothelial dysfunction in patients with cirrhosis: relationship to degree of liver failure and nitric oxide levels J Hepatol 30 1999 451 455
154. D. Ferro, C. Quintarelli, A. Lattuada, R. Leo, M. Alessandroni, and P.M. Mannucci et al. High plasma levels of von Willebrand factor as a marker of endothelial perturbation in cirrhosis: relationship to endotoxemia Hepatology 23 1996 1377 1383