Brain perfusion in sepsis

Current Vascular Pharmacology

Volumn 11, Issue 2, 2013, Pages 170-186

  Taccone, Fabio Silvio ^a   Scolletta, Sabino ^a   Franchi, Federico ^b   Donadello, Katia ^a   Oddo, Mauro ^c  

^a ERASME HOSPITAL   (Belgium)

^b UNIVERSITY OF SIENA   (Italy)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Autoregulation; Brain dysfunction; Carbon dioxide; Cerebral blood flow; Cerebral hemodynamics; Encephalopathy; Microcirculation; Sepsis

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ACTIVATED PROTEIN C; ADRENALIN; ANTIINFECTIVE AGENT; ANTIOXIDANT; AQUAPORIN 4; C REACTIVE PROTEIN; CARBON DIOXIDE; CD18 ANTIGEN; CURCUMIN; DEXAMETHASONE; DOPEXAMINE; ENDOTOXIN; GAMMA INTERFERON; HYPERTENSIVE FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MAGNESIUM; N (G) METHYLARGININE; NEURON SPECIFIC ENOLASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; NORADRENALIN; PADGEM PROTEIN; PROTEIN S100B; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOPRESSIN;

ARTERIAL CARBON DIOXIDE TENSION; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN DISEASE; BRAIN DYSFUNCTION; BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; BRAIN PERFUSION; CARDIOVASCULAR AUTOREGULATION; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAPHY; ENCEPHALITIS; ENDOTHELIAL DYSFUNCTION; GLASGOW COMA SCALE; HUMAN; HYPERCAPNIA; NONHUMAN; PATHOGENESIS; REVIEW; SEPSIS; SEPTIC SHOCK; VASOCONSTRICTION; ANIMAL; BRAIN CIRCULATION; BRAIN INJURIES; CLINICAL TRIAL (TOPIC); COMPLICATION; MICROCIRCULATION; NEUROFEEDBACK; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; CLINICAL TRIALS AS TOPIC; HUMANS; MICROCIRCULATION; NEUROFEEDBACK; SHOCK, SEPTIC;

EID: 84875295333     PISSN: 15701611     EISSN: 18756212     Source Type: Journal    
DOI: 10.2174/1570161111311020007     Document Type: Review

References (195)

1. Vincent JL, Taccone F, Schmit X. Classification, incidence and outcome of sepsis and multiple organ failure. Contrib Nephrol 2007; 156:64-74.
2. Gustot T. Multiple organ failure in sepsis: prognosis and role of systemic inflammatory response. Curr Opin Crit Care 2011; 17:153-159.
3. Eidelman LA, Putterman D, Putterman C, Sprung CL. The spectrum of septic encephalopathy. Definitions, etiologies and mortalities. JAMA 1996; 275:470-473.
4. Papadopoulos MC, Davies DC, Moss RF, Tighe D, Bennett ED. Pathophysiology of septic encephalopathy: a review. Crit Care Med 2000; 28:3019-3024.
5. Chadwick J, Mann WN. The Medical Works of Hippocrates. Oxford, Blackwell, 1950.
6. Osler W. The Principles and Practice of Medicine. New York, Appleton, 1892.
7. Iacobone E, Bailly-Salin J, Polito A, Friedman D, Stevens RD, Sharshar T. Sepsis-associated encephalopathy and its differential diagnosis. Crit Care Med 2009; 37(10 Suppl):S331-336.
8. Wilson JX, Young GB. Sepsis-associated encephalopathy: evolving concepts. Can J Neurol Sci 2003; 30:98-105.
9. Young GB, Bolton CF, Austin TW, Archibald YM, Gonder J, Wells GA. The encephalopathy associated with sepsis illness. Clin Invest Med 1990; 13:297-304.
10. Davies NWS, Sharief MK, Howard RS. Infection-associated encephalopathies-their investigation, diagnosis and treatment. J Neurol 2006; 253:833-845.
11. Ely EW, Shintani A, Truman B, et al. Delirium as a predictor of mortality in mechanically ventilated patients in the intensive care unit. JAMA 2004; 291:1753-1762.
12. Bleck TP, Smith MC, Pierre-Louis SJ, Jares JJ, Murray J, Hansen CA. Neurologic complications of critical medical illness. Crit Care Med 1993; 21:98-103.
13. Sprung CL, Peduzzi PN, Shatney CH, et al. Impact of encephalopathy on mortality in sepsis syndrome. Crit Care Med 1990; 18:474-479.
14. Suchyta MR, Jephson A, Hopkins RO. Neurologic changes during critical illness: brain imaging findings and neurobehavioral outcomes. Brain Imaging Behav 2010; 4:22-34.
15. Young GB, Bolton CF, Archibald YM, Austin TW, Wells GA. The electroencephalogram in sepsis-associated encephalopathy. J Clin Neurophysiol 1992; 9:145-152.
16. Wilson JX, Young GB. Progress in clinical neurosciences: sepsisassociated encephalopathy: evolving concepts. Can J Neurol Sci 2003; 30:98-105.
17. Ebersoldt M, Sharshar T, Annane D. Sepsis-associated delirium. Intensive Care Med 2007; 33:941-950.
18. Leon A, Lepousé C, Floch T, Graftieaux JP. Brain injury during severe sepsis. Ann Fr Anesth Rean 2006; 25:863-867.
19. Chawla J, Gruener G. Management of critical illness polyneuropathy and myopathy. Neurol Clin 2010; 28:961-977.
20. Sharshar T, Blanchard A, Paillard M, Raphael JC, Gajdos P, Annane D. Circulating vasopressin levels in septic shock. Crit Care Med 2003; 31:1752-1758.
21. De Jonghe B, Cook D, Griffith L, et al. Adaptation to the Intensive Care Environment (ATICE): development and validation of a new sedation assessment instrument. Crit Care Med 2003; 31:2344-2354.
22. Ely EW, Inouye SK, Bernard GR, et al. Delirium in mechanically ventilated patients: validity and reliability of the confusion assessment method for the intensive care unit (CAM-ICU). JAMA 2001; 286:2703-2710.
23. Towne AR, Waterhouse EJ, Boggs JG, et al. Prevalence of nonconvulsive status epilepticus in comatose patients. Neurology 2000; 54:340-345.
24. Oddo M, Carrera E, Claassen J, Mayer SA, Hirsch LJ. Continuous electroencephalography in the medical intensive care unit. Crit Care Med 2009; 37:2051-2056.
25. Zauner C, Gendo A, Kramer L, Funk GC, Bauer E, Schenk P. Impaired subcortical and cortical sensory evoked potentials pathways in septic patients. Crit Care Med 2002; 30:1136-1139.
26. Nguyen DN, Spapen H, Su F, et al. Elevated serum levels of S-100beta protein and neuron-specific enolase are associated with brain injury in patients with severe sepsis and septic shock. Crit Care Med 2006; 34:1967-1974.
27. Sharshar T, Carlier RY, Bernard F, et al. Brain lesions in septic shock-an MRI study. Intensive Care Med 2007; 33:798-806.
28. Russel JA, Singer J, Bernard GA, Wheeler A, Fulkerson W, Hudson L. Changing pattern of organ dysfunction in early human sepsis is related to mortality. Crit Care Med 2000; 28:2405-2411.
29. Iwashyna TJ, Ely EW, Smith DM, Langa KM. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA 2010; 304:1787-1794.
30. Spapen H, Nguyen DN, Troubleyn J, Huyghens L, Schiettecatte J. Drotrecogin alfa (activated) may attenuate severe sepsis-associated encephalopathy in clinical septic shock. Crit Care 2010; 14:R54.
31. Moss RF, Parmar NK, Tighe D, Davies DC. Adrenergic agents modify cerebral edema and microvessel ultrastructure in porcine sepsis. Crit Care Med 2004; 32:1916-1921.
32. Wang H, Wu YB, Du XH. Effect of dexamethasone on nitric oxide synthase and caspase-3 gene expressions in endotoxemia in neonate rat brain. Biomed Environ Sci 2005; 18:181-186.
33. Ruiz-Valdepeñas L, Martínez-Orgado JA, Benito C, Millán A, Tolón RM, Romero J. Cannabidiol reduces lipopolysaccharideinduced vascular changes and inflammation in the mouse brain: an intravital microscopy study. J Neuroinflamm 2011; 8:5.
34. Esen F, Erdem T, Aktan D, et al. Effect of magnesium sulfate administration on blood-brain barrier in a rat model of intraperitoneal sepsis: a randomized controlled experimental study. Crit Care 2005; 9:R18-23.
35. Siami S, Annane D, Sharshar T. The encephalopathy in sepsis. Crit Care Clin 2008; 24:67-82.
36. Bone RC. Sepsis, the sepsis syndrome multi-organ failure: a plea for comparable definitions. Ann Intern Med 1991; 114:332-333.
37. Pendlebury WW, Perl DP, Munoz DG. Multiple microabscesses in the central nervous system. J Neuropath Exp Neurol 1989; 48:290-300.
38. Sharshar T, Gray F, Lorin de la Grandmaison G, et al. Apoptosis of neurons in cardiovascular autonomic centres triggered by inducible nitric oxide synthase after death from septic shock. Lancet 2003; 362:1799-1805.
39. Weathers AL, Lewis SL. Rare and unusual or are they? Less commonly diagnosed encephalopathies associated with systemic disease. Semin Neurol 2009; 29:136-153.
40. Chong DL, Sriskandan S. Pro-inflammatory mechanisms in sepsis. Contrib Microbiol 2011; 17:86-107.
41. Anda T, Yamashita H, Tsutsumi K, Fujita H, Tokunaga Y, Shibata S. Effect of tumor necrosis factor-alpha on the permeability of bovine brain microvessel endothelial cells monolayers. Neurol Res 1997; 19:369-376
42. Huynh HK, Dorovini-Zis K. Effects of interferon-gamma on primary cultures of human brain microvessel endothelial cells. Am J Pathol 1993; 142: 1265-1278
43. Tureen J. Effect of recombinant human tumor necrosis factor-alpha on cerebral oxygen uptake, cerebrospinal fluid lactate and cerebral blood flow in the rabbit: role of nitric oxide. J Clin Invest 1995; 95:1086-1091
44. Alexander JJ, Jacob A, Cunningham P, Hensley L, Quigg RJ. TNF is a key mediator of septic encephalopathy acting through its receptor, TNF receptor-1. Neurochem Int 2008; 52:447-456.
45. Krueger J, Walter J, Dinarello CA, Wolff SM, Chedid L. Sleeppromoting effects of endogenous pyrogen (interleukin-1). Am J Physiol 1984; 246:R994-R999.
46. Dafny N, Prieto-Gomez B, Reyes-Vazquez C. Does the immune system communicate with the central nervous system? Interferon modifies central nervous activity. J Neuroimmunol 1985; 9:1-12.
47. Wuerfel E, Infante-Duarte C, Glumm R, Wuerfel JT. Gadofluorine M-enhanced MRI shows involvement of circumventricular organs in neuroinflammation. J Neuroinflamm 2010; 7:70.
48. Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405: 458-462.
49. Miyauchi T, Tsuruta R, Fujita M, Kaneko T, Kasaoka S, Maekawa T. Serum macrophage migration inhibitory factor reflects adrenal function in the hypothalamo-pituitary-adrenal axis of septic patients: an observational study. BMC Infect Dis 2009;9:209.
50. Soejima Y, Fujii Y, Ishikawa T, Takeshita H, Maekawa T. Local cerebral glucose utilization in septic rats. Crit Care Med 1990; 18: 423-427.
51. Semmler A, Frisch C, Debeir T, et al. Long-term cognitive impairment, neuronal loss and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model. Exp Neurol 2007; 204:733-740.
52. Kadoi Y, Saito S. An alteration in the gamma-aminobutyric acid receptor system in experimentally induced septic shock in rats. Crit Care Med 1996; 24:298-305.
53. Kadoi Y, Saito S, Kunimoto F, Imai T, Fujita T. Impairment of the brain beta-adrenergic system during experimental endotoxemia. J Surg Res 1996; 61:496-502.
54. Freund HR, Muggia-Sullam M, LaFrance R, Holroyde J, Fischer JE. Regional brain amino acid and neurotransmitter derangements during abdominal sepsis and septic encephalopathy in the rat. The effect of amino acid infusions. Arch Surg 1986; 121:209-216.
55. Ransohoff RM, Kivisakk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003; 3:569-581.
56. Dal-Pizzol F, Ritter C, Cassol-Jr OJ, et al. Oxidative mechanisms of brain dysfunction during sepsis. Neurochem Res 2010; 35:1-12.
57. Christians ES, Yan LJ, Benjamin IJ. Heat shock factor 1 and heat shock proteins: critical partners in protection against acute cell injury. Crit Care Med 2002; 30(1 Suppl):S43-50.
58. Polito A, Brouland JP, Porcher R, et al. Hyperglycaemia and apoptosis of microglial cells in human septic shock. Crit Care 2011; 15:R131.
59. Korcok J, Wu F, Tyml K, Hammond RR, Wilson JX. Sepsis inhibits reduction of dehydroascorbic acid and accumulation of ascorbate in astroglial cultures: intracellular ascorbate depletion increases nitric oxide synthase induction and glutamate uptake inhibition. J Neurochem 2002; 81:185-193.
60. Laflamme N, Rivest S. Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gramnegative bacterial cell wall components. FASEB J 2001; 15:155-163.
61. Fernandes A, Silva RF, Falcão AS, Brito MA, Brites D. Cytokine production, glutamate release and cell death in rat cultured astrocytes treated with unconjugated bilirubin and LPS. J Neuroimmunol 2004; 153:64-75.
62. Dugan LL, Bruno VMG, Amagasu SM, et al. Glia modulate the response of murine cortical neurons to excitotoxicity. Glia exacerbate AMPA neurotoxicity. J Neurosci 1995; 15: 4545-4555.
63. Wilson JX, Dragan M. Sepsis inhibits recycling and glutamatestimulated export of ascorbate by astrocytes. Free Radic Biol Med 2005; 39:990-998.
64. Jacob A, Hensley LK, Safratowich BD, Quigg RJ, Alexander JJ. The role of the complement cascade in endotoxin-induced septic encephalopathy. Lab Invest 2007; 87:1186-1194.
65. Ari I, Kafa IM, Kurt MA. Perimicrovascular edema in the frontal cortex in a rat model of intraperitoneal sepsis. Exp Neurol 2006; 198:242-249.
66. Zhan RZ, Fujiwara N, Shimoji K. Regionally different elevation of intracellular free calcium in hippocampus of septic rat brain. Shock 1996; 6:293-297.
67. Eckel B, Ohl F, Bogdanski R, Kochs EF, Blobner M. Cognitive deficits after systemic induction of inducible nitric oxide synthase: a randomised trial in rats. Eur J Anaesthesiol 2011; 28(9):655-63.
68. Minc-Golomb D, Tsarfaty I, Schwartz JP. Expression of inducible nitric oxide synthase by neurones following exposure to endotoxin and cytokine. Br J Pharmacol 1994; 112:720-722.
69. Aloisi F, Penna G, Cerase J, Menendez Iglesias B, Adorini L. IL-12 production by central nervous system microglia is inhibited by astrocytes. J Immunol 1997; 159:1604-1612.
70. Ledeboer A, Breve JJ, Wierinckx A, et al. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur J Neurosci 2002; 16:1175-1185.
71. Caggiano AO, Kraig RP. Prostaglandin E receptor subtypes in cultured rat microglia and their role in reducing lipopolysaccharideinduced interleukin-1beta production. J Neurochem 1999; 72:565-575.
72. Fontana A, Kristensen F, Dubs R, Gemsa D, Weber E. Production of prostaglandin E and an interleukin-1 like factor by cultured astrocytes and C6 glioma cells. J Immunol 1982; 129:2413-2419.
73. Akrout N, Sharshar T, Annane D. Mechanisms of brain signaling during sepsis. Curr Neuropharmacol 2009; 7:296-301.
74. Bowton DL, Bertels NH, Prough DS, et al. Cerebral blood flow is reduced in patients with sepsis syndrome. Crit Care Med 1989; 17:399-403.
75. Dagal A, Lam AM. Cerebral blood flow and the injured brain: how should we monitor and manipulate it? Curr Opin Anaesthesiol 2011; 24:131-137.
76. Peterson EC, Wang Z, Britz G. Regulation of cerebral blood flow. Int J Vasc Med 2011; 2011:823525.
77. Fieschi C, Mackenzie E, Lenzi GL, et al. Facts and trends in cerebral blood flow and metabolism: synopsis of brain '89. J Cereb Blood Flow Metab 1989; 9:573-578.
78. Tuor UI, Edvinsson L, McCulloch J. Catecholamines and the relationship between cerebral blood flow and glucose use. Am J Physiol 1986; 251:H824-H833.
79. Panerai RB, Dineen NE, Brodie FG, Robinson TG. Spontaneous fluctuations in cerebral blood flow regulation: contribution of PaCO2. J Appl Physiol 2010; 109:1860-1868.
80. Lagerkranser M, Stånge K, Sollevi A. Effects of propofol on cerebral blood flow, metabolism, and cerebral autoregulation in the anesthetized pig. J Neurosurg Anesthesiol 1997; 9:188-193.
81. Preckel MP, Leftheriotis G, Ferber C, Degoute CS, Banssillon V, Saumet JL. Effect of nitric oxide blockade on the lower limit of the cortical cerebral autoregulation in pentobarbital-anaesthetized rats. Int J Microcirc Clin Exp 1996; 16:277-283.
82. Roatta S, Micieli G, Bosone D, Losano G, Bini R, Cavallini A, Passatore M. Effect of generalised sympathetic activation by cold pressor test on cerebral haemodynamics in healthy humans. J Auton Nerv Syst 1998; 71:159-166.
83. Harper AM, Glass HI. Effect of alterations in the arterial carbon dioxide tension on the blood flow through the cerebral cortex at normal and low arterial blood pressures. J Neurol Neurosurg Psychiatry 1965; 28:449-452.
84. McDowall DG, Harper AM. Relationship between the blood flow and the extracellular pH of the cerebral cortex. Br J Anaesth 1967; 39:516.
85. Kuschinsky W, Wahl M. Local chemical and neurogenic regulation of cerebral vascular resistance. Physiol Rev 1978; 58:656-689.
86. Winn HR, Morii S, Berne RM. The role of adenosine in autoregulation of cerebral blood flow. Ann Biomed Eng 1985; 13:321-328.
87. Nguyen TS, Winn HR, Janigro D. ATP-sensitive potassium channels may participate in the coupling of neuronal activity and cerebrovascular tone. Am J Physiol Heart Circ Physiol 2000; 278:H878-H885.
88. Straub SV, Girouard H, Doetsch PE, Hannah RM, Wilkerson MK, Nelson MT. Regulation of intracerebral arteriolar tone by K(v) channels: effects of glucose and PKC. Am J Physiol Cell Physiol 2009; 297:C788-C796.
89. Pickard JD, MacDonell LA, Mackenzie ET, Harper AM. Prostaglandin-induced effects in the primate cerebral circulation. Eur J Pharmacol 1977; 43:343-351.
90. Erlichman JS, Leiter JC. Glia modulation of the extracellular milieu as a factor in central CO2 chemosensitivity and respiratory control. J Appl Physiol 2010; 108:1803-1811.
91. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke 1989; 20:45-52.
92. Bulte DP, Chiarelli PA, Wise RG, Jezzard P. Cerebral perfusion response to hyperoxia. J Cereb Blood Flow Met 2007, 27:69-75.
93. Rangel-Castilla L, Lara LR, Gopinath S, Swank PR, Valadka A, Robertson C. Cerebral hemodynamic effects of acute hyperoxia and hyperventilation after severe traumatic brain injury. J Neurotrauma 2010; 27:1853-1863.
94. Leybaert L. Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 2005; 25:2-16.
95. Kochanek PM, Hendrich KS, Jackson EK, et al. Characterization of the effects of adenosine receptor agonists on cerebral blood flow in uninjured and traumatically injured rat brain using continuous arterial spin-labeled magnetic resonance imaging. J Cereb Blood Flow Metab 2005; 25:1596-1612.
96. Paulson OB, Hasselbalch SG, Rostrup E, Knudsen GM, Pelligrino D. Cerebral blood flow response to functional activation. J Cereb Blood Flow Metab 2010; 30:2-14.
97. Straub SV, Bonev AD, Wilkerson MK, Nelson MT. Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J Gen Physiol 2006; 128:659-669.
98. Xu F, Uh J, Brier MR, et al. The influence of carbon dioxide on brain activity and metabolism in conscious humans. J Cereb Blood Flow Metab 2011; 31:58-67.
99. Franceschini MA, Radhakrishnan H, Thakur K, et al. The effect of different anesthetics on neurovascular coupling. Neuroimage 2010; 51:1367-1377.
100. Berkich DA, Ola MS, Cole J, Sweatt AJ, Hutson SM, LaNoue KF. Mitochondrial transport proteins of the brain. J Neurosci Res 2007; 85:3367-3377
101. Gordon GR, Howarth C, MacVicar BA. Bidirectional control of arteriole diameter by astrocytes. Exp Physiol 2011; 96:393-399.
102. Gordon GR, Choi HB, Rungta RL, Ellis-Davies GC, MacVicar BA. Brain metabolism dictates the polarity of astrocyte control over arterioles. Nature 2008; 456:745-749.
103. Hamel E. Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 2006; 100:1059-1064.
104. Kobayashi H, Hayashi M, Kawano H, Handa Y, Kabuto M, Ide H. Effect of chemical sympathectomy on cerebral blood flow in rats. J Neurosurg 1991; 75:906-910.
105. Cassaglia PA, Griffiths RI, Walker AM. Sympathetic withdrawal augments cerebral blood flow during acute hypercapnia in sleeping lambs. Sleep 2008; 31:1729-1734.
106. Krimer LS, Muly EC 3rd, Williams GV, Goldman-Rakic PS. Dopaminergic regulation of cerebral cortical microcirculation. Nat Neurosci 1998; 1:286-289.
107. Bayliss WM. On the local reactions of the arterial wall to changes of internal pressure. J Physiol 1902; 28:220-231
108. Halpern W, Osol G. Influence of transmural pressure of myogenic responses of isolated cerebral arteries of the rat. Ann Biomed Eng 1985; 13:287-293.
109. Mufti RE, Brett SE, Tran CH, et al. Intravascular pressure augments cerebral arterial constriction by inducing voltage-insensitive Ca2+ waves. J Physiol 2010; 588:3983-4005.
110. Ingyinn M, Rais-Bahrami K, Viswanathan M, Short BL. Altered cerebrovascular responses after exposure to venoarterial extracorporeal membrane oxygenation: role of the nitric oxide pathway. Pediatr Crit Care Med 2006; 7:368-73.
111. Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. SKCa and IKCa Channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke 2009; 40:1451-1457.
112. Paravicini TM, Miller AA, Drummond GR, Sobey CG. Flowinduced cerebral vasodilatation in vivo involves activation of phosphatidylinositol-3 kinase, NADPH-oxidase, and nitric oxide synthase. J Cereb Blood Flow Metab 2006; 26:836-845.
113. Hom GJ, Grant SK, Wolfe G, Bach TJ, MacIntyre DE, Hutchinson NI. Lipopolysaccharide-induced hypotension and vascular hyporeactivity in the rat: tissue analysis of nitric oxide synthase mRNA and protein expression in the presence and absence of dexamethasone, NG-monomethyl-L-arginine or indomethacin. J Pharmacol Exp Ther 1995; 272:452-459.
114. Johnson U, Nilsson P, Ronne-Engström E, Howells T, Enblad P. Favorable outcome in traumatic brain injury patients with impaired cerebral pressure autoregulation when treated at low cerebral perfusion pressure levels. Neurosurgery 2011; 68:714-721.
115. Bjerring PN, Eefsen M, Hansen BA, Larsen FS. The brain in acute liver failure. A tortuous path from hyperammonemia to cerebral edema. Metab Brain Dis 2009; 24:5-14.
116. Singh M, Mensah GA, Bakris G. Pathogenesis and clinical physiology of hypertension. Cardiol Clin 2010; 28:545-559.
117. Powers WJ, Videen TO, Diringer MN, Aiyagari V, Zazulia AR. Autoregulation after ischaemic stroke. J Hypertens 2009; 27: 2218-22.
118. Sharshar T, Hopkinson NS, Orlikowski D, Annane D. Science review: The brain in sepsis-culprit and victim. Crit Care 2005; 9:37-44.
119. Deng X, Wang X, Anderson R. Endothelial barrier resistance in multiple organs after septic and nonseptic challenges in the rat. J Appl Physiol 1995; 78: 2052-2061.
120. Jeppsson B, Freund HR, Gimmon Z, James JH, von Meyenfeldt MF, Fischer JE. Blood-brain barrier derangement in sepsis: Cause of septic encephalopathy? Am J Surg 1981; 141: 136-141.
121. Hofer S, Bopp C, Hoerner C, et al. Injury of the blood brain barrier and up-regulation of icam-1 in polymicrobial sepsis. J Surg Res 2008; 146:276-81.
122. Mayhan WG. Effect of lipopolysaccharide on the permeability and reactivity of the cerebral microcirculation: role of inducible nitric oxide synthase. Brain Res 1998; 792:353-357.
123. Hess DC, Bhutwala T, Sheppard JC, Zhao W, Smith J. ICAM-1 expression on human brain microvascular endothelial cells. Neurosci Lett 1994; 168:201-204.
124. Edvinsson L, Hardebo JE, MacKenzie ET, Owman C. Effect of exogenous noradrenaline on local cerebral blood flow after osmotic opening of the blood-brain barrier in the rat. J Physiol 1978; 274:149-156.
125. Wong CH, Crack PJ. Modulation of neuro-inflammation and vascular response by oxidative stress following cerebral ischemiareperfusion injury. Curr Med Chem 2008; 15:1-14.
126. Piagnerelli M, Boudjeltia KZ, Vanhaeverbeek M, Vincent JL. Red blood cell rheology in sepsis. Intensive Care Med 2003; 29:1052-1061.
127. Papadopoulos MC, Lamb FJ, Moss RF, Davies DC, Tighe D, Bennett ED. Faecal peritonitis causes oedema and neuronal injury in pig cerebral cortex. Clin Sci 1999; 96:461-466.
128. Bogdanski R, Blobner M, Becker I, Hanel F, Fink H, Kochs E. Cerebral histopathology following portal venous infusion of bacteria in a chronic porcine model. Anestesiology 2000; 93:793-804.
129. Feng SY, Samarasinghe T, Phillips DJ, et al. Acute and chronic effects of endotoxin on cerebral circulation in lambs. Am J Physiol Regul Integr Comp Physiol 2010; 298:R760-766.
130. Ekstrom-Jodal B, Elfverson J, Larsson LE. Early effects of E. coli endotoxin on superior sagittal sinus blood flow An experimental study in dogs. Acta Anaesthesiol Scand 1982; 26: 171-174.
131. Wang X, Rousset CI, Hagberg H, Mallard C. Lipopolysaccharideinduced inflammation and perinatal brain injury. Semin Fetal Neonatal Med 2006; 11: 343-353.
132. Maekawa T, Fujii Y, Sadamitsu D, Yokota K, Soejima Y, Ishikawa T, Miyauchi Y, Takeshita H. Cerebral circulation and metabolism in patients with septic encephalopathy. Am J Emerg Med 1991; 9: 139-143.
133. Jones MD Jr, Traystman RJ. Cerebral oxygenation of the fetus, newborn, and adult. Semin Perinatol 1984; 8: 205-216.
134. Sibson NR, Blamire AM, Perry VH, Gauldie J, Styles P, Anthony DC. TNF-alpha reduces cerebral blood volume and disrupts tissue homeostasis via an endothelin-and TNFR2-dependent pathway. Brain 2002; 125: 2446-2459.
135. Brian JE Jr, Faraci FM. Tumor necrosis factor-alpha-induced dilatation of cerebral arterioles. Stroke 1998; 29: 509-515.
136. Hernanz R, Alonso MJ, Briones AM, Vila E, Simonsen U, Salaices M. Mechanisms involved in the early increase of serotonin contraction evoked by endotoxin in rat middle cerebral arteries. Br J Pharmacol 2003; 140: 671-680.
137. Skopal J, Turbucz P, Vastag M, et al. Regulation of endothelin release from human brain microvessel endothelial cells. J Cardiovasc Pharmacol 1998; 31(Suppl 1):S370-S372.
138. Okamoto H, Ito O, Roman RJ, Hudetz AG. Role of inducible nitric oxide synthase and cyclooxygenase-2 in endotoxin-induced cerebral hyperemia. Stroke 1998; 29: 1209-1218.
139. Booke M, Westphal M, Hinder F, Traber LD, Traber DL. Cerebral blood flow is not altered in sheep with Pseudomonas aeruginosa sepsis treated with norepinephrine or nitric oxide synthase inhibition. Anesth Analg 2003; 96:1122-1128.
140. Meyer J, Hinder F, Stothert J, et al. Increased organ blood flow in chronic endotoxemia is reversed by nitric oxide synthase inhibition. J Appl Physiol 1994; 76: 2785-2793.
141. Lingnau W, McGuire R, Dehring DJ, et al. Changes in regional hemodynamics after nitric oxide inhibition during ovine bacteremia. Am J Physiol 1996; 270: R207-216.
142. Ince C. Microcirculation in distress: a new resuscitation end point? Crit Care Med 2004; 32:1963-1964.
143. Bateman RM, Walley KR. Microvascular resuscitation as a therapeutic goal in severe sepsis. Crit Care 2005; 9(Suppl 4):S27-S32.
144. Trzeciak S, McCoy JV, Phillip DR, et al. Early increases in microcirculatory perfusion during protocol-directed resuscitation are associated with reduced multi-organ failure at 24 h in patients with sepsis. Intens Care Med 2008; 34:2210-2217.
145. Zonta M, Angulo MC, Gobbo S, et al. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 2003; 6:43-50.
146. Panerai RB. Assessment of cerebral pressure autoregulation in humans--a review of measurement methods. Physiol Meas 1998; 19:305-338.
147. De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002; 166:98-104.
148. Lendemans S, Peszko A, Oberbeck R, et al. Microcirculatory alterations of hepatic and mesenteric microcirculation in endotoxin tolerance. Shock 2008; 29:223-231.
149. Piper RD, Pitt-Hyde M, Li F, Sibbald WJ, Potter RF. Microcirculatory changes in rat skeletal muscle in sepsis. Am J Respir Crit Care Med 1996; 154:931-937.
150. Verdant CL, De Backer D, Bruhn A, et al. Evaluation of sublingual and gut mucosal microcirculation in sepsis: a quantitative analysis. Crit Care Med 2009; 37:2875-2881.
151. Vachharajani V, Russell JM, Scott KL, et al. Obesity exacerbates sepsis-induced inflammation and microvascular dysfunction in mouse brain. Microcirculation 2005; 12:183-194.
152. Taccone FS, Su F, Pierrakos C, et al. Cerebral microcirculation is impaired during sepsis: an experimental study. Crit Care 2010, 14:R140.
153. Rosengarten B, Hecht M, Auch D, et al. Microcirculatory dysfunction in the brain precedes changes in evoked potentials in endotoxin-induced sepsis syndrome in rats. Cerebrovasc Dis 2007; 23:140-147.
154. Comim CM, Vilela MC, Constantino LS, et al. Traffic of leukocytes and cytokine up-regulation in the central nervous system in sepsis. Intens Care Med 2011; 37:711-718.
155. Vachharajani V, Wang SW, Mishra N, El Gazzar M, Yoza B, McCall C. Curcumin modulates leukocyte and platelet adhesion in murine sepsis. Microcirculation 2010; 17(6):407-16.
156. Vachharajani V, Vital S, Russell J, Granger DN. Hypertonic saline and the cerebral microcirculation in obese septic mice. Microcirculation 2007; 14:223-231.
157. Vachharajani V, Vital S, Russell J, Scott LK, Granger DN. Glucocorticoids inhibit the cerebral microvascular dysfunction associated with sepsis in obese mice. Microcirculation 2006; 13:477-487.
158. Rosengarten B, Wolff S, Klatt S, Schermuly RT. Effects of inducible nitric oxide synthase inhibition or norepinephrine on the neurovascular coupling in an endotoxic rat shock model. Crit Care 2009; 13:R139.
159. Parker JL, Emerson TE Jr. Cerebral hemodynamics, vascular reactivity, and metabolism during canine endotoxin shock. Circ Shock 1977; 4:41-53.
160. Martin CM, Sibbald WJ. Modulation of hemodynamics and organ blood flow by nitric oxide synthase inhibition is not altered in normotensive, septic rats. Am J Respir Crit Care Med 1994; 150:1539-44.
161. Raper RF, Sibbald WJ, Hobson J, Rutledge FS. Effect of PGE1 on altered distribution of regional blood flows in hyperdynamic sepsis. Chest 1991; 100(6):1703-11.
162. Rudinsky BF, Lozon M, Bell A, Hipps R, Meadow WL. Group B streptococcal sepsis impairs cerebral vascular reactivity to acute hypercarbia in piglets. Pediatr Res 1996; 39:55-63.
163. Tyml K, Yu J, McCormack DG. Capillary and arteriolar responses to local vasodilators are impaired in a rat model of sepsis. J Appl Physiol 1998; 84:837-844.
164. Hinkelbein J, Feldmann RE Jr, Peterka A, Schubert C, Schelshorn D, Maurer MH, Kalenka A. Alterations in cerebral metabolomics and proteomic expression during sepsis. Curr Neurovasc Res 2007; 4:280-288.
165. Pedersen M, Brandt CT, Knudsen GM, et al. The effect of S. pneumoniae bacteremia on cerebral blood flow autoregulation in rats. J Cereb Blood Flow Metab 2008; 28:126-134.
166. Rosengarten B, Hecht M, Wolff S, Kaps M. Autoregulative function in the brain in an endotoxic rat shock model. Inflamm Res 2008; 57:542-546.
167. Semmler A, Hermann S, Mormann F, et al. Sepsis causes neuroinflammation and concomitant decrease of cerebral metabolism. J Neuroinflamm 2008; 5:38.
168. Wijdicks EF, Stevens M. The role of hypotension in septic encephalopathy following surgical procedures. Arch Neurol 1992; 49:653-656.
169. Yonas H, Pindzola RP, Johnson DW. Xenon/computed tomography cerebral blood flow and its use in clinical management. Neurosurg Clin N Am 1996; 7:605-616.
170. Kety SS. The measurement of cerebral blood flow by means of inert diffusible tracers. Keio J Med 1994; 43:9-14.
171. Thees C, Kaiser M, Scholz M, et al. Cerebral haemodynamics and carbon dioxide reactivity during sepsis syndrome. Crit Care 2007; 11:R123.
172. Hamberg LM, Hunter GJ, Kierstead D, Lo EH, Gilberto González R, Wolf GL. Measurement of cerebral blood volume with subtraction three-dimensional functional CT. AJNR Am J Neuroradiol 1996; 17:1861-1869.
173. Kim HJ, Kim TW, Ryu SY, et al. Acetazolamide-challenged perfusion magnetic resonance imaging for assessment of cerebrovascular reserve capacity in patients with symptomatic middle cerebral artery stenosis: comparison with technetium-99m-hexamethylpropyleneamine oxime single-photon emission computed tomography. Clin Imaging 2011; 35:413-420.
174. Laureys S, Perrin F, Faymonville ME, et al. Cerebral processing in the minimally conscious state. Neurology 2004; 63:916-918.
175. Larsen FS, Olsen KS, Ejlersen E, Hansen BA, Paulson OB, Knudsen GM. Cerebral blood flow autoregulation and transcranial Doppler sonography in patients with cirrhosis. Hepatology 1995; 22:730-736.
176. Pfister D, Siegemund M, Dell-Kuster S, et al. Cerebral perfusion in sepsis-associated delirium. Crit Care 2008; 12:R63.
177. Steiner LA, Pfister D, Strebel SP, Radolovich D, Smielewski P, Czosnyka M. Near-infrared spectroscopy can monitor dynamic cerebral autoregulation in adults. Neurocrit Care 2009; 10:122-128.
178. Czosnyka M, Brady K, Reinhard M, Smielewski P, Steiner LA. Monitoring of cerebrovascular autoregulation: facts, myths, and missing links. Neurocrit Care 2009; 10:373-386.
179. Piechnik SK, Yang X, Czosnyka M, et al. The continuous assessment of cerebrovascular reactivity: a validation of the method in healthy volunteers. Anesth Analg 1999; 89:944-949.
180. Szatmári S, Végh T, Csomós A, et al. Impaired cerebrovascular reactivity in sepsis-associated encephalopathy studied by acetazolamide test. Crit Care 2010; 14:R50.
181. Møller K, Strauss GI, Qvist J, et al. Cerebral blood flow and oxidative metabolism during human endotoxemia. J Cereb Blood Flow Metab 2002; 22:1262-1270.
182. Pollard V, Prough DS, Deyo DJ, et al. Cerebral blood flow during experimental endotoxemia in volunteers. Crit Care Med 1997; 25:1700-1706.
183. Bowton DL, Bertels NH, Prough DS, Stump DA. Cerebral blood flow is reduced in patients with sepsis syndrome. Crit Care Med 1989; 17:399-403.
184. Straver JS, Keunen RW, Stam CJ, et al. Transcranial Doppler and systemic hemodynamic studies in septic shock. Neurol Res 1996; 18:313-318.
185. Matta BF, Stow PJ. Sepsis-induced vasoparalysis does not involve the cerebral vasculature: indirect evidence from autoregulation and carbon dioxide reactivity studies. Br J Anaesth 1996; 76:790-794.
186. Smith SM, Padayachee S, Modaresi KB, Smithies MN, Bihari DJ. Cerebral blood flow is proportional to cardiac index in patients with septic shock. J Crit Care 1998; 13:104-109.
187. Taccone FS, Castanares-Zapatero D, Peres-Bota D, Vincent JL, Berre' J, Melot C. Cerebral autoregulation is influenced by carbon dioxide levels in patients with septic shock. Neurocrit Care 2010; 12:35-42.
188. Terborg C, Schummer W, Albrecht M, Reinhart K, Weiller C, Röther J. Dysfunction of vasomotor reactivity in severe sepsis and septic shock. Intensive Care Med 2001; 27:1231-1234.
189. Bowie RA, O'Connor PJ, Mahajan RP. Cerebrovascular reactivity to carbon dioxide in sepsis syndrome. Anaesthesia 2003; 58:261-265.
190. Kadoi Y, Saito S, Kawauchi C, Hinohara H, Kunimoto F. Comparative effects of propofol vs dexmedetomidine on cerebrovascular carbon dioxide reactivity in patients with septic shock. Br J Anaesth 2008; 100:224-229.
191. Hamu Y, Kanmura Y, Tsuneyoshi I, Yoshimura N. The effects of vasopressin on endotoxin-induced attenuation of contractile responses in human gastroepiploic arteries in vitro. Anesth Analg 1999; 88:542-548.
192. Berré J, De Backer D, Moraine JJ, Mélot C, Kahn RJ, Vincent JL. Dobutamine increases cerebral blood flow velocity and jugular bulb hemoglobin saturation in septic patients. Crit Care Med 1997; 25:392-398.
193. Pfister D, Strebel SP, Steiner LA. Effects of catecholamines on cerebral blood vessels in patients with traumatic brain injury. Eur J Anaesthesiol Suppl 2008; 42:98-103.
194. Dotson B. Daily interruption of sedation in patients treated with mechanical ventilation. Am J Health Syst Pharm 2010; 67:1002-1006.
195. Pfister D, Schmidt B, Smielewski P, et al. Intracranial pressure in patients with sepsis. Acta Neurochir Suppl 2008; 102:71-75.