The hyperdynamic circulation of chronic liver diseases: From the patient to the molecule

The hyperdynamic circulatory syndrome observed in chronic liver diseases is a great example of research that originated from clinical observations and progressed in the last 50 years from the patient to the experimental laboratory. Our knowledge has evolved from the patient to the molecule, using experimental models that serve as a source for understanding the complex pathophysiological mechanisms that govern this complex syndrome. We now know that progressive vasodilatation is central to the detrimental effects observed in multiple organs. Although nitric oxide has been shown to be the primary vasodilator molecule in these effects, other molecules also participate in the complex mechanisms of vasodilatation. This review summarizes three major areas: first, clinical observation in patients; second, experimental models used to study the hyperdynamic circulatory syndrome; and third, the vasodilator molecules that play roles in vascular abnormalities observed in portal hypertension. (Hepatology 2006;43:S121–S131.)

[1]  R. Groszmann,et al.  Mild increases in portal pressure upregulate vascular endothelial growth factor and endothelial nitric oxide synthase in the intestinal microcirculatory bed, leading to a hyperdynamic state. , 2006, American journal of physiology. Gastrointestinal and liver physiology.

[2]  William M. Lee,et al.  Complications and use of intracranial pressure monitoring in patients with acute liver failure and severe encephalopathy , 2005, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[3]  A. Blei Monitoring cerebral blood flow: A useful clinical tool in acute liver failure? , 2005, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[4]  W. Jiménez,et al.  Circulatory function and hepatorenal syndrome in cirrhosis , 2005, Hepatology.

[5]  J. Schölmerich,et al.  Up-regulation of nNOS and associated increase in nitrergic vasodilation in superior mesenteric arteries in pre-hepatic portal hypertension. , 2005, Journal of hepatology.

[6]  R. Moreau,et al.  Norfloxacin reduces aortic NO synthases and proinflammatory cytokine up-regulation in cirrhotic rats: role of Akt signaling. , 2005, Gastroenterology.

[7]  A. Blei The pathophysiology of brain edema in acute liver failure , 2005, Neurochemistry International.

[8]  J. Rodés,et al.  Inhibition of VEGF receptor-2 decreases the development of hyperdynamic splanchnic circulation and portal-systemic collateral vessels in portal hypertensive rats. , 2005, Journal of hepatology.

[9]  M. Fallon Mechanisms of pulmonary vascular complications of liver disease: hepatopulmonary syndrome. , 2005, Journal of clinical gastroenterology.

[10]  W. Jiménez,et al.  Increased anandamide induced relaxation in mesenteric arteries of cirrhotic rats: role of cannabinoid and vanilloid receptors , 2005, Gut.

[11]  T. Macdonald,et al.  Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn's disease. , 2005, Gastroenterology.

[12]  A. Blei,et al.  Cerebral Blood Flow in Acute Liver Failure: A Finding in Search of a Mechanism , 2004, Metabolic Brain Disease.

[13]  K. Peters Exceptional matters: clinical research from bedside to bench. , 2004, Clinical medicine.

[14]  Rui Wang,et al.  Hydrogen sulfide-induced relaxation of resistance mesenteric artery beds of rats. , 2004, American journal of physiology. Heart and circulatory physiology.

[15]  W. Sessa eNOS at a glance , 2004, Journal of Cell Science.

[16]  M. Humbert,et al.  Prevention of hepatopulmonary syndrome and hyperdynamic state by pentoxifylline in cirrhotic rats , 2004, European Respiratory Journal.

[17]  R. Schrier,et al.  Increased vascular heme oxygenase‐1 expression contributes to arterial vasodilation in experimental cirrhosis in rats , 2004, Hepatology.

[18]  J. Mitchell,et al.  Submucosal "dissection" in collagenous colitis. , 2004, Gut.

[19]  M. Fallon,et al.  ET-1 and TNF-alpha in HPS: analysis in prehepatic portal hypertension and biliary and nonbiliary cirrhosis in rats. , 2004, American journal of physiology. Gastrointestinal and liver physiology.

[20]  N. Minamino,et al.  Adrenomedullin contributes to vascular hyporeactivity in cirrhotic rats with ascites via a release of nitric oxide , 2004, Scandinavian journal of gastroenterology.

[21]  Miguel Ángel Martínez,et al.  Adrenomedullin, a Vasodilator Peptide Implicated in Hemodynamic Alterations of Liver Cirrhosis Relationship to Nitric Oxide , 1999, Digestive Diseases and Sciences.

[22]  P. Ferenci Protease inhibitors for treatment of chronic hepatitis C--a new target for the magic bullet identified. , 2004, Journal of hepatology.

[23]  T. Takano,et al.  Pulmonary blood transit time and impaired arterial oxygenation in patients with chronic liver disease , 2004, Journal of Gastroenterology.

[24]  R. Groszmann,et al.  Bacterial translocation up‐regulates GTP‐cyclohydrolase I in mesenteric vasculature of cirrhotic rats , 2003, Hepatology.

[25]  S. Ryter,et al.  Analysis of pulmonary heme oxygenase-1 and nitric oxide synthase alterations in experimental hepatopulmonary syndrome. , 2003, Gastroenterology.

[26]  R. Groszmann,et al.  Mesenteric vasoconstriction triggers nitric oxide overproduction in the superior mesenteric artery of portal hypertensive rats. , 2003, Gastroenterology.

[27]  P. Angus,et al.  Evidence for altered vascular responses to exogenous endothelin-1 in patients with advanced cirrhosis with restoration of the normal vasoconstrictor response following successful liver transplantation , 2003, Gut.

[28]  J. Barberà,et al.  Increased carbon monoxide production in patients with cirrhosis with and without spontaneous bacterial peritonitis , 2003, Hepatology.

[29]  Hiroaki Shimokawa,et al.  Electron Spin Resonance Detection of Hydrogen Peroxide as an Endothelium-Derived Hyperpolarizing Factor in Porcine Coronary Microvessels , 2003, Arteriosclerosis, thrombosis, and vascular biology.

[30]  J. Henriksen,et al.  Central and noncentral blood volumes in cirrhosis: relationship to anthropometrics and gender. , 2003, American journal of physiology. Gastrointestinal and liver physiology.

[31]  Takashi Saito,et al.  Role for Hydrogen Peroxide in Flow-Induced Dilation of Human Coronary Arterioles , 2003, Circulation research.

[32]  M. Fallon,et al.  Prospective evaluation of outcomes and predictors of mortality in patients with hepatopulmonary syndrome undergoing liver transplantation , 2003, Hepatology.

[33]  L. Chauvelot‐Moachon,et al.  Terlipressin inhibits in vivo aortic iNOS expression induced by lipopolysaccharide in rats with biliary cirrhosis , 2002, Hepatology.

[34]  C. Leffler,et al.  Carbon Monoxide Dilates Cerebral Arterioles by Enhancing the Coupling of Ca2+ Sparks to Ca2+-Activated K+ Channels , 2002, Circulation research.

[35]  R. Bryan,et al.  Role of Cytoplasmic Phospholipase A2 in Endothelium-Derived Hyperpolarizing Factor Dilations of Rat Middle Cerebral Arteries , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[36]  Rui Wang,et al.  H2S-induced vasorelaxation and underlying cellular and molecular mechanisms , 2002 .

[37]  B. Kis,et al.  Hydrogen peroxide acts as an EDHF in the piglet pial vasculature in response to bradykinin. , 2002, American journal of physiology. Heart and circulatory physiology.

[38]  R. Groszmann,et al.  Phosphorylation of eNOS initiates excessive NO production in early phases of portal hypertension. , 2002, American journal of physiology. Heart and circulatory physiology.

[39]  Hiroaki Shimokawa,et al.  Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in human mesenteric arteries. , 2002, Biochemical and biophysical research communications.

[40]  T. Griffith,et al.  Relative contributions of NO and gap junctional communication to endothelium-dependent relaxations of rabbit resistance arteries vary with vessel size. , 2002, Microvascular research.

[41]  R. Martı́n-Ruiz,et al.  Endogenous cannabinoids: a new system involved in the homeostasis of arterial pressure in experimental cirrhosis in the rat. , 2002, Gastroenterology.

[42]  Rui Wang,et al.  H(2)S-induced vasorelaxation and underlying cellular and molecular mechanisms. , 2002, American journal of physiology. Heart and circulatory physiology.

[43]  Rui Wang,et al.  The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener , 2001 .

[44]  H. Nishimatsu,et al.  Adrenomedullin Induces Endothelium-Dependent Vasorelaxation via the Phosphatidylinositol 3-Kinase/Akt-Dependent Pathway in Rat Aorta , 2001, Circulation research.

[45]  C. Fernández-Rodríguez,et al.  The effect of liver transplantation on circulating levels of estradiol and progesterone in male patients: Parallelism with hepatopulmonary syndrome and systemic hyperdynamic circulation improvement , 2001, Journal of endocrinological investigation.

[46]  A. Sanyal,et al.  Endocannabinoids acting at vascular CB1 receptors mediate the vasodilated state in advanced liver cirrhosis , 2001, Nature Medicine.

[47]  D. Edwards,et al.  Gap junctional communication underpins EDHF-type relaxations evoked by ACh in the rat hepatic artery. , 2001, American journal of physiology. Heart and circulatory physiology.

[48]  A. Blei,et al.  Cerebral hyperemia and nitric oxide synthase in rats with ammonia-induced brain edema. , 2001, Journal of hepatology.

[49]  Jing Zhang,et al.  The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. , 2001, The EMBO journal.

[50]  G. G. Emerson,et al.  Electrical activation of endothelium evokes vasodilation and hyperpolarization along hamster feed arteries. , 2001, American journal of physiology. Heart and circulatory physiology.

[51]  H Shimokawa,et al.  Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. , 2000, The Journal of clinical investigation.

[52]  R. Schrier,et al.  Neuronal nitric oxide synthase and systemic vasodilation in rats with cirrhosis. , 2000, American journal of physiology. Renal physiology.

[53]  R. Moreau,et al.  Evidence for an endothelium‐derived hyperpolarizing factor in the superior mesenteric artery from rats with cirrhosis , 2000, Hepatology.

[54]  C. Hill,et al.  Incidence of myoendothelial gap junctions in the proximal and distal mesenteric arteries of the rat is suggestive of a role in endothelium-derived hyperpolarizing factor-mediated responses. , 2000, Circulation research.

[55]  W. Vogel,et al.  Hyperdynamic circulation in liver cirrhosis: no evidence for peripheral vasodilation detected by ultrasound of the brachial artery , 2000, American Journal of Gastroenterology.

[56]  富岡 拓志 Relaxation in different-sized rat blood vessels mediated by endothelium-derived hyperpolarizing factor : importance of processes mediating precontractions , 2000 .

[57]  R. Groszmann,et al.  Bacterial translocation in cirrhotic rats stimulates eNOS-derived NO production and impairs mesenteric vascular contractility. , 1999, The Journal of clinical investigation.

[58]  R. Aebersold,et al.  Identification of Flow-dependent Endothelial Nitric-oxide Synthase Phosphorylation Sites by Mass Spectrometry and Regulation of Phosphorylation and Nitric Oxide Production by the Phosphatidylinositol 3-Kinase Inhibitor LY294002* , 1999, The Journal of Biological Chemistry.

[59]  R. Bryan,et al.  Functional heterogeneity of endothelial P2 purinoceptors in the cerebrovascular tree of the rat. , 1999, American journal of physiology. Heart and circulatory physiology.

[60]  J. E. Griffiths,et al.  The Akt kinase signals directly to endothelial nitric oxide synthase , 1999, Current Biology.

[61]  R. Groszmann,et al.  Hsp90 regulation of endothelial nitric oxide synthase contributes to vascular control in portal hypertension. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[62]  A. Kitabatake,et al.  Relaxation in Different-Sized Rat BloodVessels Mediated by Endothelium-Derived Hyperpolarizing Factor: Importance of Processes Mediating Precontractions , 1999, Journal of Vascular Research.

[63]  R. Busse,et al.  Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation , 1999, Nature.

[64]  W. Sessa,et al.  Regulation of endothelium-derived nitric oxide production by the protein kinase Akt , 1999, Nature.

[65]  R. Groszmann,et al.  NO overproduction by eNOS precedes hyperdynamic splanchnic circulation in portal hypertensive rats. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[66]  M. Álvarez-Mon,et al.  Factors mediating the hemodynamic effects of tumor necrosis factor-alpha in portal hypertensive rats. , 1999, The American journal of physiology.

[67]  M. Álvarez-Mon,et al.  Factors mediating the hemodynamic effects of tumor necrosis factor-α in portal hypertensive rats. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[68]  T. Griffith,et al.  Nitric oxide-independent relaxations to acetylcholine and A23187 involve different routes of heterocellular communication. Role of Gap junctions and phospholipase A2. , 1999, Circulation research.

[69]  R. Groszmann,et al.  Enhanced release of nitric oxide in response to changes in flow and shear stress in the superior mesenteric arteries of portal hypertensive rats , 1998, Hepatology.

[70]  Z. Ba,et al.  The pivotal role of adrenomedullin in producing hyperdynamic circulation during the early stage of sepsis. , 1998, Archives of surgery.

[71]  C. Garland,et al.  K+ is an endothelium-derived hyperpolarizing factor in rat arteries , 1998, Nature.

[72]  Fabio Piscaglia,et al.  Superior mesenteric artery impedance in chronic liver diseases: relationship with disease severity and portal circulation , 1998, American Journal of Gastroenterology.

[73]  J. Prieto,et al.  Circulating adrenomedullin in cirrhosis: relationship to hyperdynamic circulation. , 1998, Journal of hepatology.

[74]  R. Bataller,et al.  Increased cerebrovascular resistance in cirrhotic patients with ascites , 1998, Hepatology.

[75]  D. Deutsch,et al.  Pharmacological evidence for anandamide amidase in human cardiac and vascular tissues. , 1998, International journal of cardiology.

[76]  A. Adeagbo,et al.  Calcium-Dependent Phospholipase A2 Mediates the Production of Endothelium-Derived Hyperpolarizing Factor in Perfused Rat Mesenteric Prearteriolar Bed , 1998, Journal of Vascular Research.

[77]  S. Milstien,et al.  Cytokines stimulate GTP cyclohydrolase I gene expression in cultured human umbilical vein endothelial cells. , 1998, Arteriosclerosis, thrombosis, and vascular biology.

[78]  D K Stevenson,et al.  Carbon monoxide and bilirubin production in neonates. , 2001, Seminars in perinatology.

[79]  E. Ellis,et al.  Activation of peripheral CB1 cannabinoid receptors in haemorrhagic shock , 1997, Nature.

[80]  A. Takeshita,et al.  Importance of endothelium-derived hyperpolarizing factor in human arteries. , 1997, The Journal of clinical investigation.

[81]  D. Deutsch,et al.  Production and physiological actions of anandamide in the vasculature of the rat kidney. , 1997, The Journal of clinical investigation.

[82]  N. Matsuki,et al.  The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. , 1997, Biochemical and biophysical research communications.

[83]  T. Rabelink,et al.  Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. , 1997, Biochemical and biophysical research communications.

[84]  M. Fallon,et al.  The role of endothelial nitric oxide synthase in the pathogenesis of a rat model of hepatopulmonary syndrome. , 1997, Gastroenterology.

[85]  Lingyun Wu,et al.  The direct effect of carbon monoxide on KCa channels in vascular smooth muscle cells , 1997, Pflügers Archiv.

[86]  S. D. Lee,et al.  Hyperdynamic circulation in prehepatic portal hypertension: role of tumor necrosis factor-alpha. , 1997, Zhonghua yi xue za zhi = Chinese medical journal; Free China ed.

[87]  C. Nathan,et al.  Nitric oxide and macrophage function. , 1997, Annual review of immunology.

[88]  R Busse,et al.  Nitric oxide attenuates the release of endothelium-derived hyperpolarizing factor. , 1996, Circulation.

[89]  W. Jiménez,et al.  Increased nitric oxide synthase expression in arterial vessels of cirrhotic rats with ascites. , 1996, Hepatology.

[90]  M. Fujishima,et al.  The importance of the hyperpolarizing mechanism increases as the vessel size decreases in endothelium-dependent relaxations in rat mesenteric circulation. , 1996, Journal of cardiovascular pharmacology.

[91]  K. Morris,et al.  Comparison of vascular nitric oxide production and systemic hemodynamics in cirrhosis versus prehepatic portal hypertension in rats , 1996, Hepatology.

[92]  P. Cahill,et al.  Increased endothelial nitric oxide synthase activity in the hyperemic vessels of portal hypertensive rats. , 1996, Journal of hepatology.

[93]  S. S. Lee,et al.  Cirrhotic cardiomyopathy: Getting to the heart of the matter , 1996, Hepatology.

[94]  D. Fulton,et al.  Role of phospholipase C and phospholipase A2 in the nitric oxide-independent vasodilator effect of bradykinin in the rat perfused heart. , 1996, The Journal of pharmacology and experimental therapeutics.

[95]  R. Groszmann,et al.  Thalidomide inhibits tumor necrosis factor α, decreases nitric oxide synthesis, and ameliorates the hyperdynamic circulatory syndrome in portal‐hypertensive rats , 1996, Hepatology.

[96]  R. Schrier,et al.  Upregulation of endothelial constitutive NOS: a major role in the increased NO production in cirrhotic rats. , 1996, The American journal of physiology.

[97]  R. Groszmann,et al.  The role of central blood volume in the development of sodium retention in portal hypertensive rats. , 1996, Gastroenterology.

[98]  S. Kourembanas,et al.  Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. , 1995, The Journal of clinical investigation.

[99]  P. Cahill,et al.  Enhanced nitric oxide synthase activity in portal hypertensive rabbits , 1995, Hepatology.

[100]  M. Hashizume,et al.  Increased prostacyclin content in gastric mucosa of cirrhotic patients with portal hypertensive gastropathy. , 1995, Prostaglandins, leukotrienes, and essential fatty acids.

[101]  D K Stevenson,et al.  Heme oxygenase activity in the adult rat aorta and liver as measured by carbon monoxide formation. , 1995, Canadian journal of physiology and pharmacology.

[102]  R. Groszmann,et al.  Tumor necrosis factor α: A major contributor to the hyperdynamic circulation in prehepatic portal-hypertensive rats , 1995 .

[103]  S. Kourembanas,et al.  Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[104]  R. Groszmann,et al.  Tumor necrosis factor alpha: a major contributor to the hyperdynamic circulation in prehepatic portal-hypertensive rats. , 1995, Gastroenterology.

[105]  R. Groszmann Hyperdynamic circulation of liver disease 40 years later: Pathophysiology and clinical consequences , 1994, Hepatology.

[106]  S. Milstien,et al.  Regulation of nitric oxide synthesis by proinflammatory cytokines in human umbilical vein endothelial cells. Elevations in tetrahydrobiopterin levels enhance endothelial nitric oxide synthase specific activity. , 1994, The Journal of clinical investigation.

[107]  K. Campbell,et al.  Prostacyclin production in acute, chronic, and long-term experimental portal hypertension. , 1994, Surgery.

[108]  R. Moreau,et al.  Effects of theophylline on hemodynamics and tissue oxygenation in patients with cirrhosis. , 1992, Journal of hepatology.

[109]  Terry D. Lee,et al.  Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. , 1992, Science.

[110]  R. Groszmann,et al.  Temporal relationship of peripheral vasodilatation, plasma volume expansion and the hyperdynamic circulatory state in portal‐hypertensive rats , 1992, Hepatology.

[111]  S. Moncada,et al.  Hyperdynamic circulation in cirrhosis: a role for nitric oxide? , 1991, The Lancet.

[112]  S. Snyder,et al.  Localization of nitric oxide synthase indicating a neural role for nitric oxide , 1990, Nature.

[113]  J. Polio,et al.  Na restriction blunts expansion of plasma volume and ameliorates hyperdynamic circulation in portal hypertension. , 1990, The American journal of physiology.

[114]  J. Roca,et al.  Effects of propranolol on arterial oxygenation and oxygen transport to tissues in patients with cirrhosis. , 1990, The American review of respiratory disease.

[115]  P. Belloni,et al.  Endothelial cell production of nitrogen oxides in response to interferon gamma in combination with tumor necrosis factor, interleukin-1, or endotoxin. , 1990, Journal of the National Cancer Institute.

[116]  R. Groszmann,et al.  Hemodynamic mechanisms of emerging portal hypertension caused by schistosomiasis in the hamster , 1990, Hepatology.

[117]  S. Snyder,et al.  Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[118]  K. Lenz,et al.  Beneficial effect of 8-ornithin vasopressin on renal dysfunction in decompensated cirrhosis. , 1989, Gut.

[119]  Vicente Arroyo,et al.  Peripheral arterial vasodilation hypothesis: A proposal for the initiation of renal sodium and water retention in cirrhosis , 1988, Hepatology.

[120]  L. Ignarro,et al.  Endothelium-dependent modulation of cGMP levels and intrinsic smooth muscle tone in isolated bovine intrapulmonary artery and vein. , 1987, Circulation research.

[121]  R. Groszmann,et al.  Interaction of flow and resistance in maintenance of portal hypertension in a rat model. , 1986, The American journal of physiology.

[122]  M. Maines,et al.  Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. , 1986, The Journal of biological chemistry.

[123]  B. Groves,et al.  Interrelationship between cardiac output and vascular resistance as determinants of effective arterial blood volume in cirrhotic patients. , 1985, Kidney international.

[124]  R. Groszmann,et al.  Increased blood flow through the portal system in cirrhotic rats. , 1984, Gastroenterology.

[125]  R. Groszmann,et al.  Hyperdynamic circulation in portal-hypertensive rat model: a primary factor for maintenance of chronic portal hypertension. , 1983, The American journal of physiology.

[126]  M. Stipanuk,et al.  Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. , 1982, The Biochemical journal.

[127]  R. Groszmann,et al.  Splanchnic hemodynamics in portal-hypertensive rats: measurement with gamma-labeled microspheres. , 1982, The American journal of physiology.

[128]  T. Brewer ARTERIAL PRESSURE AND HYPERTENSION , 1981 .

[129]  R. Furchgott,et al.  The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine , 1980, Nature.

[130]  Claesson Hans-Erik,et al.  Elevation of adenosine 3′,5′‐monophosphate levels in 3T3 fibroblasts by arachidonic acid: evidence for mediation by prostaglandin I2 , 1977 .

[131]  J. Lindgren,et al.  Elevation of adenosine 3',5'-monophosphate levels in 3T3 fibroblasts by arachidonic acid: evidence for mediation by prostaglandin I2. , 1977, FEBS letters.

[132]  J. Cohn Renal hemodynamic alterations in liver disease. , 1976, Perspectives in nephrology and hypertension.

[133]  R. Groszmann,et al.  Hepatic blood flow in alcoholic liver disease measured by an indicator dilution technic. , 1972, The American journal of medicine.

[134]  R. Groszmann,et al.  Circulation times in the splanchnic and hepatic beds in alcoholic liver disease. , 1972, Gastroenterology.

[135]  R. Groszmann,et al.  Different patterns of porta-systemic shunting in cirrhosis of the liver studied by an indicator dilution technique. , 1971, Acta gastroenterologica Latinoamericana.

[136]  F. Tristani,et al.  Systemic Vasoconstrictor and Renal Vasodilator Effects of PLV‐2 (Octapressin) in Man , 1968, Circulation.

[137]  J. H. Burke,et al.  Portal blood flow in cirrhosis of the liver. , 1967, The Journal of clinical investigation.

[138]  G R HERRMANN,et al.  Congestive heart failure. , 1962, Geriatrics.

[139]  S. Sherlock,et al.  Circulatory changes in chronic liver disease. , 1958, The American journal of medicine.

[140]  W. Abelmann,et al.  The cardiac output at rest in Laennec's cirrhosis. , 1953, The Journal of clinical investigation.