Arquivos de Neuro-Psiquiatria, Table of Contents

CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2017; 75(07): 470-476
DOI: 10.1590/0004-282X20170076

VIEWS AND REVIEWS

Cerebral hemodynamic and metabolic changes in fulminant hepatic failure

Modificações da hemodinâmica e metabolismo cerebral na insuficiência hepatica fulminante

Fernando Mendes Paschoal Junior

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

²Universidade Federal do Pará, Faculdade de Medicina, Universidade Federal do Pará, Belém PA, Brasil;

,

Ricardo de Carvalho Nogueira

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

,

Marcelo de Lima Oliveira

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

,

Eric Homero Albuquerque Paschoal

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

²Universidade Federal do Pará, Faculdade de Medicina, Universidade Federal do Pará, Belém PA, Brasil;

,

Manoel Jacobsen Teixeira

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

,

Luiz Augusto Carneiro D’Albuquerque

³Universidade de São Paulo, Faculdade de Medicina, Departamento de Gastroenterologia, São Paulo SP, Brasil.

,

Edson Bor-Seng-Shu

¹Universidade de São Paulo, Faculdade de Medicina, Hospital das Clínicas, Divisão de Cirurgia Neurológica, Laboratório de Neurosonologia e Hemodinâmica Cerebral, São Paulo SP, Brasil;

› Author Affiliations

ABSTRACT

Intracranial hypertension and brain swelling are a major cause of morbidity and mortality of patients suffering from fulminant hepatic failure (FHF). The pathogenesis of these complications has been investigated in man, in experimental models and in isolated cell systems. Currently, the mechanism underlying cerebral edema and intracranial hypertension in the presence of FHF is multi-factorial in etiology and only partially understood. The aim of this paper is to review the pathophysiology of cerebral hemodynamic and metabolism changes in FHF in order to improve understanding of intracranial dynamics complication in FHF.

RESUMO

O edema cerebral e a hipertensão intracraniana (HIC) são as principais causas de morbidade e mortalidade de pacientes com insuficiência hepática fulminante (IHF). A patogênese dessas complicações tem sido investigada no homem, em modelos experimentais e em sistemas celulares isolados. Atualmente, o mecanismo subjacente ao edema cerebral e HIC na presença de IHF é multifatorial em etiologia e pouco compreendido na literatura. O objetivo deste trabalho é revisar a fisiopatologia das alterações hemodinâmicas e metabólicas cerebrais na IHF, visando melhorar a compreensão da complicação da hemodinâmica encefálica na IHF.

hepatic insufficiency - intracranial hypertension - brain edema

insuficiência hepatica - hipertenção intracraniana - edema encefálico

References
1 Hoofnagle JH, Carithers RL Jr, Shapiro C, Ascher N. Fulminant hepatic failure: summary of a workshop. Hepatology. 1995;21(1):240-52. https://doi.org/10.1016/0270-9139(95)90434-4
2 Ostapowicz G, Fontana RJ, Schiødt FV, Larson A, Davern TJ, Han SH et al. Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med. 2002;137(12):947-54. https://doi.org/10.7326/0003-4819-137-12-200212170-00007
3 O’Grady JG. Paracetamol hepatotoxicity: how to prevent. J R Soc Med. 1997;90(7):368-70.
4 Perazzo JC, Tallis S, Delfante A, Souto PA, Lemberg A, Eizayaga FX et al. Hepatic encephalopathy: an approach to its multiple pathophysiological features. World J Hepatol. 2012;4(3):50-65. https://doi.org/10.4254/wjh.v4.i3.50
5 Lucké B. The pathology of fatal epidemic hepatitis. Am J Pathol. 1944;20(3):471-593.
6 Ede RJ, Gimson AE, Bihari D, Williams R. Controlled hyperventilation in the prevention of cerebral oedema in fulminant hepatic failure. J Hepatol. 1986;2(1):43-51. https://doi.org/10.1016/S0168-8278(86)80007-1
7 Canalese J, Gimson AE, Davis C, Mellon PJ, Davis M, Williams R. Controlled trial of dexamethasone and mannitol for the cerebral oedema of fulminant hepatic failure. Gut. 1982;23(7):625-9. https://doi.org/10.1136/gut.23.7.625
8 Donovan JP, Schafer DF, Shaw BW Jr, Sorrell MF. Cerebral oedema and increased intracranial pressure in chronic liver disease. Lancet .1998;351(9104):719-21. https://doi.org/10.1016/S0140-6736(97)07373-X
9 Crippin JS, Gross JB Jr, Lindor KD. Increased intracranial pressure and hepatic encephalopathy in chronic liver disease. Am J Gastroenterol. 1992;87(7):879-82.
10 Bingaman WE, Frank JI. Malignant cerebral edema and intracranial hypertension. Neurol Clin. 1995;13(3):479-509.
11 Czosnyka M, Pickard JD. Monitoring and interpretation of intracranial pressure. J Neurol Neurosurg Psychiatry. 2004;75(6):813-.21. https://doi.org/10.1136/jnnp.2003.033126
12 Muñoz SJ, Robinson M, Northrup B, Bell R, Moritz M, Jarrell B et al. Elevated intracranial pressure and computed tomography of the brain in fulminant hepatocellular failure. Hepatology. 1991;13(2):209-12. https://doi.org/10.1002/hep.1840130202
13 Ganz R, Swain M, Traber P, DalCanto M, Butterworth RF, Blei AT. Ammonia-induced swelling of rat cerebral cortical slices: implications for the pathogenesis of brain edema in acute hepatic failure. Metab Brain Dis. 1989;4(3):213-23. https://doi.org/10.1007/BF01000297
14 Detry O, De Roover A, Honoré P, Meurisse M. Brain edema and intracranial hypertension in fulminant hepatic failure: pathophysiology and management. World J Gastroenterol. 2006;12(46):7405-12. https://doi.org/10.3748/wjg.v12.i46.7405
15 Traber PG, Dal Canto M, Ganger DR, Blei AT. Electron microscopic evaluation of brain edema in rabbits with galactosamine-induced fulminant hepatic failure: ultrastructure and integrity of the blood-brain barrier. Hepatology. 1987;7(6):1272-7. https://doi.org/10.1002/hep.1840070616
16 Traber P, DalCanto M, Ganger D, Blei AT. Effect of body temperature on brain edema and encephalopathy in the rat after hepatic devascularization. Gastroenterology. 1989;96(3):885-91. https://doi.org/10.1016/0016-5085(89)90917-7
17 Matkowskyj KA, Marrero JA, Carroll RE, Danilkovich AV, Green RM, Benya RV. Azoxymethane-induced fulminant hepatic failure in C57BL/6J mice: characterization of a new animal model. Am J Physiol. 1999;277(2):G455-62.
18 Gove CD, Hughes RD, Ede RJ, Williams R. Regional cerebral edema and chloride space in galactosamine-induced liver failure in rats. Hepatology. 1997;25(2):295-301. https://doi.org/10.1002/hep.510250207
19 Kallaras C, Anogianakis G, Apostolakis M, Manthos A, Sioga A, Economou L et al. Ultrastructural alterations of the rabbit sciatic nerve, spinal cord and cerebellum, following methionine sulphoximine administration. Histol Histopathol. 1994;9(1):105-12.
20 Aitken PG, Borgdorff AJ, Juta AJ, Kiehart DP, Somjen GG, Wadman WJ. Volume changes induced by osmotic stress in freshly isolated rat hippocampal neurons. Pflugers Arch. 1998;436(6):991-8. https://doi.org/10.1007/s004240050734
21 Norenberg MD, Jayakumar AR, Rama Rao KV. Oxidative stress in the pathogenesis of hepatic encephalopathy. Metab Brain Dis. 2004;19(3-4):313-29. https://doi.org/10.1023/B:MEBR.0000043978.91675.79
22 Häussinger D, Schliess F. Astrocyte swelling and protein tyrosine nitration in hepatic encephalopathy. Neurochem Int. 2005;47(1-2):64-70. https://doi.org/10.1016/j.neuint.2005.04.008
23 Blei AT, Olafsson S, Therrien G, Butterworth RF. Ammonia-induced brain edema and intracranial hypertension in rats after portacaval anastomosis. Hepatology. 1994;19(6):1437-44. https://doi.org/10.1002/hep.1840190619
24 Swain M, Butterworth RF, Blei AT. Ammonia and related amino acids in the pathogenesis of brain edema in acute ischemic liver failure in rats. Hepatology. 1992;15(3):449-53. https://doi.org/10.1002/hep.1840150316
25 Cordoba J, Gottstein J, Blei AT. Glutamine, myo-inositol and organic brain osmolytes after portocaval anastomosis in the rat: implications for ammonia-induced brain edema. Hepatology. 1996;24(4):919-23. https://doi.org/10.1002/hep.510240427
26 Noble LJ, Hall JJ, Chen S, Chan PH. Morphologic changes in cultured astrocytes after exposure to glutamate. J Neurotrauma. 1992;9(3):255-67. https://doi.org/10.1089/neu.1992.9.255
27 Vaquero J, Chung C, Blei AT. Brain edema in acute liver failure. A window to the pathogenesis of hepatic encephalopathy. Ann Hepatol. 2003;2(1):12-22.
28 Bor-Seng-Shu E, Hirsch R, Teixeira MJ, Andrade AF, Marino Junior R. Cerebral hemodynamic changes gauged by transcranial Doppler ultrasonography in patients with posttraumatic brain swelling treated by surgical decompression. J Neurosurg. 2006;104(1):93-100. https://doi.org/10.3171/jns.2006.104.1.93
29 Wendon JA, Harrison PM, Keays R, Williams R. Cerebral blood flow and metabolism in fulminant liver failure. Hepatology. 1994;19(6):1407-13. https://doi.org/10.1002/hep.1840190614
30 Larsen FS. Pott F, Hansen BA, Ejlersen E, Knudsen GM, Clemmesen JD et al. Transcranial Doppler sonography may predict brain death in patients with fulminant hepatic failure. Transplant Proc. 1995;27(6):3510-31.
31 Aggarwal S, Kramer D, Yonas H, Obrist W, Kang Y, Martin M, Policare R. Cerebral hemodynamic and metabolic changes in fulminant hepatic failure: a retrospective study. Hepatology 1994;19(1):80-7. https://doi.org/10.1002/hep.1840190114
32 Larsen FS, Ejlersen E, Clemmesen JO, Kirkegaard P, Hansen BA. Preservation of cerebral oxidative metabolism in fulminant hepatic failure: an autoregulation study. Liver Transpl Surg. 1996;2(5):348-53. https://doi.org/10.1002/lt.500020504
33 Nilsson B, Siesjö BK. Evidence against H⁺ as a regulator of cerebral blood flow. In: Owman C, Edvinsson L, editors. Neurogenic control of the brain circulation. Oxford: Pergamon Press; 1977. p. 295-300.
34 Kontos HA, Raper AJ, Patterson JL Jr. Analysis of vasoactivity of local pH, PCO₂ and bicarbonate on pial vessels. Stroke. 1977;8(3):358-60. https://doi.org/10.1161/01.STR.8.3.358
35 Kuschinsky W, Wahl M. Interactions between perivascular norepinephrine and potassium or osmolarity on pial arteries of cats. Microvasc Res. 1977;14(2):173-80. https://doi.org/10.1016/0026-2862(77)90016-4
36 Wahl M, Kuschinsky W. The dilatatory action of adenosine on pial arteries of cats and its inhibition by theophylline. Pflugers Arch. 1976;362(1):55-9. https://doi.org/10.1007/BF00588681
37 Park TS, Van Wylen DG, Rubio R, Berne RM. Brain interstitial adenosine and sagittal sinus blood flow during systemic hypotension in piglets. J Cereb Blood Flow Metab. 1988;8(6):822-8. https://doi.org/10.1038/jcbfm.1988.138
38 Winn HR, Rubio R, Berne RM. Brain adenosine concentration during hypoxia in rats. Am J Physiol. 1981;241(2):H235-42.
39 Lassen NA. Cerebral blood flow and oxygen consumption in man. Physiol Rev. 1959;39(2):183-238.
40 MacKenzie ET, Strandgaard S, Graham DI, Jones JV, Harper AM, Farrar JK. Effects of acutely induced hypertension in cats on pial arteriolar caliber, local cerebral blood flow and the blood-brain barrier. Circ Res. 1976;39(1):33-41. https://doi.org/10.1161/01.RES.39.1.33
41 Kogure K, Scheinberg P, Reinmuth OM, Fujishima M, Busto R. Mechanisms of cerebral vasodilation in hypoxia. J Appl Physiol. 1970;29(2):223-9.
42 Kuschinsky W, Wahl M, Bosse O, Thurau K. Perivascular potassium and pH as determinants of local pial arterial diameter in cats: a microapplication study. Circ Res. 1972;31(2):240-7. https://doi.org/10.1161/01.RES.31.2.240
43 Winn HR, Rubio GR, Berne RM. The role of adenosine in the regulation of cerebral blood flow. J Cereb Blood Flow Metab. 1981;1(3):239-44. https://doi.org/10.1038/jcbfm.1981.29
44 Rangel-Castilla L, Gasco J, Nauta HJ, Okonkwo DO, Robertson CS. Cerebral pressure autoregulation in traumatic brain injury. Neurosurg Focus. 2008;25(4):E7. https://doi.org/10.3171/FOC.2008.25.10.E7
45 Panerai RB. Assessment of cerebral pressure autoregulation in humans: a review of measurement methods. Physiol Meas. 1998;19(3):305-38. https://doi.org/10.1088/0967-3334/19/3/001
46 Dirnagl U, Niwa K, Lindauer U, Villringer A. Coupling of cerebral blood flow to neuronal activation: role of adenosine and nitric oxide. Am J Physiol. 1994;267(1):H296-301.
47 Macrae IM, Dawson DA, Norrie JD, McCulloch J. Inhibition of nitric oxide synthesis: effects of cerebral blood flow and glucose utilization in the rat. J Cereb Blood Flow Metab. 1993;13(6):985-92. https://doi.org/10.1038/jcbfm.1993.123
48 Brusilow SW, Traystman R. Hepatic encephalopathy. N Engl J Med. 1986;314(12):786-7.
49 Jalan R, Olde Damink SW, Hayes PC, Deutz NE, Lee A. Pathogenesis of intracranial hypertension in acute liver failure: inflammation, ammonia and cerebral blood flow. J Hepatol. 2004;41(4):613-20. https://doi.org/10.1016/j.jhep.2004.06.011
50 Rolando N, Wade J, Davalos M, Wendon J, Philpott-Howard J, Williams R. The systemic inflammatory response syndrome in acute liver failure. Hepatology. 2000;32(4):734-9. https://doi.org/10.1053/jhep.2000.17687
51 Takahashi H, Koehler RC, Brusilow SW, Traystman RJ. Inhibition of brain glutamine accumulation prevents cerebral edema in hyperammonemic rats. Am J Physiol. 1991;261(3):H825-9.
52 Enevoldsen EM, Jensen FT. Autoregulation and CO2 responses of cerebral blood flow in patients with acute severe head injury. J Neurosurg. 1978;48(5):689-703. https://doi.org/10.3171/jns.1978.48.5.0689.
53 Tiecks FP, Lam AM, Aaslid R, Newell DW. Comparison of static and dynamic cerebral autoregulation measurements. Stroke. 1995;26(6):1014-9. https://doi.org/10.1161/01.STR.26.6.1014
54 Lewelt W, Jenkins LW, Miller JD. Autoregulation of cerebral blood flow after experimental fluid percussion injury of the brain. J Neurosurg. 1980;53(4):500-11. https://doi.org/10.3171/jns.1980.53.4.0500
55 Aaslid R. Cerebral autoregulation and vasomotor reactivity. Front Neurol Neurosci. 2006;21:216-28. https://doi.org/10.1159/000092434
56 Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke. 1989;20(1):45-52. https://doi.org/10.1161/01.STR.20.1.45
57 Larsen FS, Ejlersen E, Hansen BA, Knudsen GM, Tygstrup N, Secher NH. Functional loss of cerebral blood flow autoregulation in patients with fulminant hepatic failure. J Hepatol. 1995;23(2):212-7. https://doi.org/10.1016/0168-8278(95)80338-6
58 Strauss G, Hansen BA, Kirkegaard P, Rasmussen A, Hjortrup A, Larsen FS. Liver function, cerebral blood flow autoregulation, and hepatic encephalopathy in fulminant hepatic failure. Hepatology. 1997;25(4):837-9. https://doi.org/10.1002/hep.510250409