The effects of traumatic brain injury on cerebral blood flow and brain tissue nitric oxide levels and cytokine expression

Journal of Neurotrauma

Volumn 21, Issue 10, 2004, Pages 1431-1442

  Ahn, Myung Ja ^a   Sherwood, Edward R ^a   Prough, Donald S ^a   Cheng, Yie Lin ^a   DeWitt, Douglas S ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Cerebral blood flow; Cytokine; Nitric oxide; Rats; Traumatic brain injury

Indexed keywords

CYTOKINE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOFLURANE; MESSENGER RNA; NITRIC OXIDE; OXYGEN; RNA; TUMOR NECROSIS FACTOR ALPHA;

AIR; ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; BRAIN BLOOD FLOW; BRAIN INJURY; BRAIN LEVEL; BRAIN TISSUE; CONTROLLED STUDY; DECAPITATION; DISEASE SEVERITY; ELECTRODE; INTUBATION; LASER DOPPLER FLOWMETRY; MALE; MEASUREMENT; NONHUMAN; PROTEIN EXPRESSION; RANDOMIZATION; RAT; RNA ISOLATION;

ANIMALS; BRAIN; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; CYTOKINES; LASER-DOPPLER FLOWMETRY; MALE; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 7244239069     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2004.21.1431     Document Type: Article

References (82)

1. AL-TURKI, A., and ARMSTEAD, W.M. (1998). Altered release of prostaglandins by opioids contributes to impaired cerebral hemodynamics following brain injury. Crit. Care Med. 26, 917-925.
2. ALAGARSAMY, S., DEWITT, D.S., and JOHNSON, K.M. (1998). Effects of moderate, central fluid percussion traumatic brain injury on nitric oxide synthase activity in rats. J. Neurotrauma 15, 627-633.
3. ARMSTEAD, W.M. (1996). Role of endothelin in pial artery vasoconstriction and altered responses to vasopressin after brain injury. J. Neurosurg. 85, 901-907.
4. ARMSTEAD, W.M. (1998). Brain injury impairs prostaglandin cerebrovasodilation. J. Neurotrauma 15, 721-729.
5. ARMSTEAD, W.M. (2000). NOC/oFQ contributes to age-dependent impairment of NMDA-induced cerebrovasodilation after brain injury. Am. J. Physiol. 279, H2188-H2195.
6. BEASLEY, D., SCHWARTZ, J.H., and BRENNER, B.M. (1991). Interleukin 1 induces prolonged L-arginine-dependent cyclic guanosine monophosphate and nitrite production in rat vascular smooth muscle cells. J. Clin. Invest. 87, 602-608.
7. BECKMAN, J.S., BECKMAN, T.W., CHEN, J., MARSHALL, P.A., and FREEMAN, B.A. (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87, 1620-1624.
8. BELL, M.J., KOCHANEK, P.M., DOUGHTY, L.A., et al. (1997). Interleukin-6 and interleukin-10 in cerebrospinal fluid after severe traumatic brain injury in children. J. Neurotrauma 14, 451-457.
9. BONVENTO, G., SEYLAZ, J., and LACOMBE, P. (1994). Widespread attenuation of the cerebrovascular reactivity to hypercapnia following inhibition of nitric oxide synthase in the conscious rat. J. Cereb. Blood Flow Metab. 14, 699-703.
10. BOUMA, G.J., MUIZELAAR, J.P., CHOI, S.C., NEWLON, P.G., and YOUNG, H.F. (1991). Cerebral circulation and metabolism after severe traumatic brain injury: the elusive role of ischemia. J. Neurosurg. 75, 685-693.
11. BRAMLETT, H.M., KRAYDIEH, S., GREEN, E.J., and DIETRICH, W.D. (1997). Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. J. Neuropathol. Exp. Neurol. 56, 1132-1141.
12. BRIAN, J.E., JR., FARACI, F.M., and HEISTAD, D.D. (1996). Recent insights into the regulation of cerebral circulation. Clin. Exp. Pharmacol. Physiol. 23, 449-457.
13. BRYAN, R.M., CHERIAN, L., and ROBERTSON, C. (1995). Regional cerebral blood flow after controlled cortical impact injury in rats. Anesth. Analg. 80, 687-695.
14. CARLOS, T.M., CLARK, R.S.B., FRANICOLA-HIGGINS, D., SCHIDING, J.K., and KOCHANEK, P.M. (1997). Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. J. Leukoc. Biol. 61, 279-285.
15. CHERIAN, L., CHACKO, G., GOODMAN, J.C., and ROBERTSON, C.S. (1999). Cerebral hemodynamic effects of phenylephrine and L-arginine after cortical impact injury. Crit. Care Med. 27, 2512-2517.
16. CHERIAN, L., GOODMAN, J.C., and ROBERTSON, C.S. (2000). Brain nitric oxide changes after controlled cortical impact injury in rats. J. Neurophysiol. 83, 2171-2178.
17. CHERIAN, L., ROBERTSON, C.S., CONTANT, C.F., and BRYAN, R.M. (1994). Lateral cortical impact injury in rats: cerebrovascular effects of varying depth of cortical deformation and impact velocity. J. Neurotrauma 11, 573-585.
18. CLARK, R.S.B., KOCHANEK, P.M., SCHWARZ, M.A., et al. (1996). Inducible nitric oxide synthase expression in cerebrovascular smooth muscle and neutrophils after traumatic brain injury in immature rats. Pediatr. Res. 39, 784-790.
19. DASH, P.K., MACH, S.A., and MOORE, A.N. (2000). Regional expression and role of cyclooxygenase-2 following experimental traumatic brain injury. J. Neurotrauma 17, 69-81.
20. DE VRIES, H.E., BLOM-ROOSEMALEN, M.C., VAN OOSTEN, M., et al. (1996). The influence of cytokines on the integrity of the blood-brain barrier in vitro. J Neuroimmunol. 64, 37-43.
21. 2 levels in rats. J. Neurotrauma 5, 303-313.
22. DEWITT, D.S., MATHEW, B., and PROUGH, D.S. (2000). Peroxynitrite and traumatic brain injury reduce vasodilatory response in isolated rodent middle cerebral arteries. J. Neurotrauma 17, 993.
23. DEWITT, D.S., SMITH, T.G., DEYO, D.J., MILLER, K.R., UCHIDA, T., and PROUGH, D.S. (1997). L-Arginine and superoxide dismutase prevent or reverse cerebral hypoperfusion after fluid-percussion traumatic brain injury. J. Neurotrauma 14, 223-233.
24. DHILLON, H.S., CARMAN, H.M., ZHANG, D., SCHEFF, S.W., and PRASAD, M.R. (1999). Severity of experimental brain injury on lactate and free fatty acid accumulation and Evans blue extravasation in the rat cortex and hippocampus. J. Neurotrauma 16, 455-469.
25. DIETRICH, W.D., ALONSO, O., BUSTO, R., et al. (1998). Posttraumatic cerebral ischemia after fluid percussion brain injury: an autoradiographic and histopathological study in rats. Neurosurgery 43, 585-594.
26. DING, A.H., NATHAN, C.F., and STUEHR, D.J. (1988). Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412.
27. FABIAN, R.H., DEWITT, D.S., and KENT, T.A. (1995). In vivo detection of superoxide anion production by the brain using a cytochrome c electrode. J. Cereb. Blood Flow Metab. 15, 242-247.
28. FAN, L., YOUNG, P.R., BARONE, F.C., FEUERSTEIN, G.Z., SMITH, D.H., and McINTOSH, T.K. (1996). Experimental brain injury induces differential expression of tumor necrosis factor-a mRNA in the CNS. Mol. Brain Res. 36, 287-291.
29. FARACI, F.M., and BRIAN, J.E., JR. (1994). Nitric oxide and the cerebral circulation. Stroke 25, 692-703.
30. FARACI, F.M., and SOBEY, C.G. (1998). Role of potassium channels in regulation of cerebral vascular tone. J. Cereb. Blood Flow Metab. 18, 1047-1063.
31. GAHM, C., HOLMIN, S., and MATHIESEN, T. (2002). Nitric oxide synthase expression after human brain contusion. Neurosurgery 50, 1319-1326.
32. GHIRNIKAR, R.S., LEE, Y.L., and ENG, L.F. (1998). Inflammation in traumatic brain injury: role of cytokines and chemokines. Neurochem. Res. 23, 329-340.
33. GOLDING, E.M., MARRELLI, S.P., YOU, J., and BRYAN, R.M., Jr. (2002). Endothelium-derived hyperpolarizing factor in the brain: a new regulator of cerebral blood flow? Stroke 33, 661-663.
34. GOLDING, E.M., ROBERTSON, C.S., and BRYAN, R.M. (1999). The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clin. Exp. Hypertens. 21, 299-332.
35. GOODMAN, J.C., ROBERTSON, C.S., GROSSMAN, R.G., and NARAYAN, R.K. (1990). Elevation of tumor necrosis factor in head injury. J Neuroimmunol. 30, 213-217.
36. GULBENKIAN, S., UDDMAN, R., and EDVINSSON, L. (2001). Neuronal messengers in the human cerebral circulation. Peptides 22, 995-1007.
37. HABERL, R.L., HEIZER, M.L., MARMAROU, A., and ELLIS, E.F. (1989). Laser-Doppler assessment of brain microcirculation: effect of systemic alterations. Am. J. Physiol. 256, H1247-H1254.
38. HLATKY, R., GOODMAN, J.C., VALADKA, A.B., and ROBERTSON, C.S. (2003). Role of nitric oxide in cerebral blood flow abnormalities after traumatic brain injury. J. Cereb. Blood Flow Metab. 23, 582-588.
39. HOLMIN, S., SCHALLING, M., HOJEBERG, B., NORDQVIST, A.C., SKEFTRUNA, A.K., and MATHIESEN, T. (1997). Delayed cytokine expression in rat brain following experimental contusion. J. Neurosurg. 86, 493-504.
40. KINOSHITA, K., CHATZIPANTELI, K., VITARBO, E., TRUETTNER, J.S., ALONSO, O.F., and DIETRICH, W.D. (2002). Interleukin-1b messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: importance of injury severity and brain temperature. Neurosurgery 51, 195-203.
41. KNOBLACH, S.M., and FADEN, A.I. (2000). Cortical interleukin-1 beta elevation after traumatic brain injury in the rat: no effect of two selective antagonists on motor recovery. Neurosci. Lett. 289, 5-8.
42. KOSSMANN, T., STAHEL, P.F., LENZLINGER, P.M., et al. (1997). Interleukin-8 released into the cerebrospinal fluid after brain injury is associated with blood-brain barrier dysfunction and nerve growth factor production. J. Cereb. Blood Flow Metab. 17, 280-289.
43. 1 ganglioside. Stroke 21, (Suppl III), III-95-III-97.
44. LEWELT, W., JENKINS, L.W., and MILLER, J.D. (1980). Autoregulation of cerebral blood flow after experimental fluid percussion injury of the brain. J. Neurosurg. 53, 500-511.
45. LEWELT, W., JENKINS, L.W., and MILLER, J.D. (1982). Effects of experimental fluid-percussion injury of the brain on cerebrovascular reactivity to hypoxia and to hypercapnia. J. Neurosurg. 56, 332-338.
46. MAIER, B., SCHWERDTFEGER, K., MAUTES, A., et al. (2001). Differential release of interleukines 6, 8, and 10 in cerebrospinal fluid and plasma after traumatic brain injury. Shock 15, 421-426.
47. McCLAIN, C.J., COHEN, D., OTT, L., DINARELLO, C.A., and YOUNG, B. (1987). Ventricular fluid interleukin-1 activity in patients with head injury. J. Lab. Clin. Med. 110, 48-54.
48. MONROY, M., KULUZ, J.W., HE, D., DIETRICH, W.D., and SCHLEIEN, C.L. (2001). Role of nitric oxide in the cerebrovascular and thermoregulatory response to interleukin-1 beta. Am. J. Physiol. 280, H1448-H1453.
49. MORGANTI-KOSSMANN, M.C., RANCAN, M., OTTO, V.I., STAHEL, P.F., and KOSSMANN, T. (2001). Role of cerebral inflammation after traumatic brain injury: a revisited concept. Shock 16, 165-177.
50. MORGANTI-KOSSMANN, M.C., RANCAN, M., STAHEL, P.F., and KOSSMANN, T. (2002). Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 8, 101-105.
51. MORIKAWA, E., GINSBERG, M.D., DIETRICH, W.D., et al. (1992a). The significance of brain temperature in focal cerebral ischemia: histopathological consequences of middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 12, 380-389.
52. MORIKAWA, E., ROSENBLATT, S., and MOSKOWITZ, M.A. (1992b). L-Arginine dilates rat pial arterioles by nitric oxide-dependent mechanisms and increases blood flow during focal cerebral ischaemia. Br. J. Pharmacol. 107, 905-907.
53. MUIR, J.K., BOERSCHEL, M., and ELLIS, E.F. (1992). Continuous monitoring of posttraumatic cerebral blood flow using laser-Doppler flowmetry. J. Neurotrauma 9, 355-362.
54. PELLIGRINO, D.A., KOENIG, H.M., and ALBRECHT, R.F. (1993). Nitric oxide synthesis and regional cerebral blood flow responses to hypercapnia and hypoxia in the rat. J. Cereb. Blood Flow Metab. 13, 80-87.
55. PRAT, R., MARKIV, V., DUJOVNY, M., and MISRA, M. (1997). Evaluation of cerebral autoregulation following diffuse brain injury in rats. Neurol. Res. 19, 393-402.
56. ROMAN, R.J. (2002). P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol. Rev. 82, 131-185.
57. ROSS, S.A., HALLIDAY, M.I., CAMPBELL, G.C., BYRNES, D.P., and ROWLANDS, B.J. (1994). The presence of tumour necrosis factor in CSF and plasma after severe head injury. Br. J. Neurosurg. 8, 419-425.
58. SHERWOOD, E.R., VARMA, T.K., FRAM, R.Y., LIN, C.Y., KOUTROUVELIS, A.P., and TOLIVER-KINSKY, T.E. (2001). Glucan phosphate potentiates endotoxin-induced interferon-γ expression in immunocompetent mice but attenuates induction of endotoxin tolerance. Clin. Sci. 101, 541-550.
59. SHOHAMI, E., BASS, R., WALLACH, D., YAMIN, A., and GALLILY, R. (1996). Inhibition of tumor necrosis factor alpha (TNFalpha) activity in rat brain is associated with cerebroprotection after closed head injury. J. Cereb. Blood Flow Metab. 16, 378-384.
60. SHOHAMI, E., GALLILY, R., MECHOULAM, R., BASS, R., and BEN HUR, T. (1997). Cytokine production in the brain following closed head injury: dexanabinol (HU-211) is a novel TNF-alpha inhibitor and an effective neuroprotectant. J. Neuroimmunol. 72, 169-177.
61. SHOHAMI, E., NOVIKOV, M., BASS, R., YAMIN, A., and GALLILY, R. (1994). Closed head injury triggers early production of TNFa and IL-6 by brain tissue. J. Cereb. Blood Flow Metab. 14, 615-619.
62. SHOHAMI, E., SHAPIRA, Y., SIDI, A., and COTEV, S. (1987). Head injury induces increased prostaglandin synthesis in rat brain. J. Cereb. Blood Flow Metab. 7, 58-63.
63. SOSIN, D.M., SNIEZEK, J.E., and WAXWEILER, R.J. (1995). Trends in death associated with traumatic brain injury, 1979 through 1992. JAMA 273, 1778-1780.
64. STERN, M.D., LAPPE, D.L., BOWEN, P.D., et al. (1977). Continuous measurement of tissue blood flow by laser Doppler spectroscopy. Am. J. Physiol. 232, H441-H448.
65. STOVER, J.F., SCHONING, B., BEYER, T.F., WOICIECHOWSKY, C., and UNTERBERG, A.W. (2000). Temporal profile of cerebrospinal fluid glutamate, interleukin-6, and tumor necrosis factor-alpha in relation to brain edema and contusion following controlled cortical impact injury in rats. Neurosci. Lett. 288, 25-28.
66. SULLIVAN, P.G., BRUCH-KELLER, A.J., RABCHEVSKY, A.G., et al. (1999). Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J. Neurosci. 19, 6248-6256.
67. TAUPIN, V., TOULMOND, S., SERRANO, A., BENAVIDES, J., and ZAVALA, F. (1993). Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre- and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neuroimmunol. 42, 177-186.
68. TOULMOND, S., and ROTHWELL, N.J. (1995). Interleukin-1 receptor antagonist inhibits neuronal damage caused by fluid percussion injury in the rat. Brain Res. 671, 261-266.
69. VARMA, T.K., LIN, C.Y., TOLIVER-KINSKY, T.E., and SHERWOOD, E.R. (2002). Endotoxin-induced gamma interferon production: contributing cell types and key regulatory factors. Clin. Diagn. Lab. Immunol. 9, 530-543.
70. VARMA, T.K., TOLIVER-KINSKY, T.E., LIN, C.Y., KOUTROUVELIS, A.P., NICHOLS, J.E., and SHERWOOD, E.R. (2001). Cellular mechanisms that cause suppressed gamma Interferon secretion in endotoxin-tolerant mice. Infect. Immun. 69, 5249-5263.
71. VITKOVIC, L., BOCKAERT, J., and JACQUE, C. (2000). " Inflammatory" cytokines: neuromodulators in normal brain? J. Neurochem. 74, 457-471.
72. WADA, K., CHATZIPANTELI, K., BUSTO, R., and DIETRICH, W.D. (1998a). Role of nitric oxide in traumatic brain injury in the rat. J. Neurosurg. 89, 807-818.
73. WADA, K., CHATZIPANTELI, K., KRAYDIEH, S., BUSTO, R., and DIETRICH, W.D. (1998b). Inducible nitric oxide synthase expression after traumatic brain injury and neuroprotection with aminoguanidine treatment in rats. Neurosurgery 43, 1427-1436.
74. G-nitro-L-arginine on cerebral blood flow response to changes in carbon dioxide tension. J. Cereb. Blood Flow Metab. 12, 947-953.
75. WEI, E.P., DIETRICH, W.D., POVLISHOCK, J.T., NAVARI, R.M., and KONTOS, H.A. (1980). Functional, morphological, and metabolic abnormalities of the cerebral microcirculation after concussive brain injury in cats. Circ. Res. 46, 37-47.
76. WEI, E.P., KONTOS, H.A., DIETRICH, W.D., POVLISHOCK, J.T., and ELLIS, E.F. (1981). Inhibition by free radical scavengers and by cyclooxygenase inhibitors of pial arteriolar abnormalities from concussive brain injury in cats. Circ. Res. 48, 95-103.
77. WHALEN, M.J., CARLOS, T.M., KOCHANEK, P.M., et al. (2000). Interleukin-8 is increased in cerebrospinal fluid of children with severe head injury. Crit. Care Med. 28, 929-934.
78. WHITE, P.F., JOHNSTON, R.R., and EGER II, E.I. (1974). Determination of anesthetic requirement in rats. Anesthesiology 40, 52-57.
79. WOODROOFE, M.N., SARNA, G.S., WADHWA, M., et al. (1991). Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production. J. Neuroimmunol. 33, 227-236.
80. YAMAKAMI, I., and McINTOSH, T.K. (1989). Effects of traumatic brain injury on regional cerebral blood flow in rats as measured with radiolabeled microspheres. J. Cereb. Blood Flow Metab. 9, 117-124.
81. YAMAKAMI, I., and McINTOSH, T.K. (1991). Alterations in regional cerebral blood flow following brain injury in the rat. J. Cereb. Blood Flow Metab. 11, 655-660.
82. YUAN, X.Q., PROUGH, D.S., SMITH, T.L., and DEWITT, D.S. (1988). The effects of traumatic brain injury on regional cerebral blood flow in rats. J. Neurotrauma 5, 298-301.