Skip to main content
Top
Published in: Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine 1/2013

Open Access 01-12-2013 | Original research

Superimposed traumatic brain injury modulates vasomotor responses in third-order vessels after hemorrhagic shock

Authors: Bo Chen, Manuel Mutschler, Yongjun Yuan, Edmund Neugebauer, Qiaobing Huang, Marc Maegele

Published in: Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine | Issue 1/2013

Login to get access

Abstract

Background

Traumatic brain injury (TBI) and hemorrhagic shock (HS) are the leading causes of death in trauma. Recent studies suggest that TBI may influence physiological responses to acute blood loss. This study was designed to assess to what extent superimposed TBI may modulate physiologic vasomotor responses in third-order blood vessels in the context of HS.

Methods

We have combined two established experimental models of pressure-controlled hemorrhagic shock (HS; MAP 50 mmHg/60 min) and TBI (lateral fluid percussion (LFP)) to assess vasomotor responses and microcirculatory changes in third-order vessels by intravital microscopy in a spinotrapezius muscle preparation. 23 male Sprague–Dawley rats (260–320 g) were randomly assigned to experimental groups: i) Sham, ii) HS, iii) TBI + HS, subjected to impact or sham operation, and assessed.

Results

HS led to a significant decrease in arteriolar diameters by 20% to baseline (p < 0.01). In TBI + HS this vasoconstriction was less pronounced (5%, non-significant). At completed and at 60 minutes of resuscitation arteriolar diameters had recovered to pre-injury baseline values. Assessment of venular diameters revealed similar results. Arteriolar and venular RBC velocity and blood flow decreased sharply to < 20% of baseline in HS and TBI + HS (p < 0.01). Immediately after and at 60 minutes of resuscitation, an overshoot in arterial RBC velocity (140% of baseline) and blood flow (134.2%) was observed in TBI + HS.

Conclusion

Superimposed TBI modulated arteriolar and venular responses to HS in third-order vessels in a spinotrapezius muscle preparation. Further research is necessary to precisely define the role of TBI on the microcirculation in tissues vulnerable to HS.
Appendix
Available only for authorised users
Literature
1.
go back to reference Anderson ID, Woodford M, de Dombal FT, Irving M: Retrospective study of 1000 deaths from injury in England and Wales. Br Med J (Clin Res Ed). 1988, 296: 1305-1308. 10.1136/bmj.296.6632.1305.CrossRef Anderson ID, Woodford M, de Dombal FT, Irving M: Retrospective study of 1000 deaths from injury in England and Wales. Br Med J (Clin Res Ed). 1988, 296: 1305-1308. 10.1136/bmj.296.6632.1305.CrossRef
2.
go back to reference Bruns JJ, Hauser WA: The epidemiology of traumatic brain injury: a review. Epilepsia. 2003, 44 (Suppl 10): 2-10.CrossRefPubMed Bruns JJ, Hauser WA: The epidemiology of traumatic brain injury: a review. Epilepsia. 2003, 44 (Suppl 10): 2-10.CrossRefPubMed
3.
go back to reference Evans JA, van Wessem KJP, McDougall D, Lee KA, Lyons T, Balogh ZJ: Epidemiology of traumatic deaths: comprehensive population-based assessment. World J Surg. 2010, 34: 158-163. 10.1007/s00268-009-0266-1.CrossRefPubMed Evans JA, van Wessem KJP, McDougall D, Lee KA, Lyons T, Balogh ZJ: Epidemiology of traumatic deaths: comprehensive population-based assessment. World J Surg. 2010, 34: 158-163. 10.1007/s00268-009-0266-1.CrossRefPubMed
4.
go back to reference Sauaia A, Moore FA, Moore EE, Moser KS, Brennan R, Read RA, Pons PT: Epidemiology of trauma deaths: a reassessment. J Trauma. 1995, 38: 185-193. 10.1097/00005373-199502000-00006.CrossRefPubMed Sauaia A, Moore FA, Moore EE, Moser KS, Brennan R, Read RA, Pons PT: Epidemiology of trauma deaths: a reassessment. J Trauma. 1995, 38: 185-193. 10.1097/00005373-199502000-00006.CrossRefPubMed
5.
go back to reference Dennis AM, Haselkorn ML, Vagni VA, Garman RH, Janesko-Feldman K, Bayir H, Clark RSB, Jenkins LW, Dixon CE, Kochanek PM: Hemorrhagic shock after experimental traumatic brain injury in mice: effect on neuronal death. J Neurotrauma. 2009, 26: 889-899. 10.1089/neu.2008.0512.PubMedCentralCrossRefPubMed Dennis AM, Haselkorn ML, Vagni VA, Garman RH, Janesko-Feldman K, Bayir H, Clark RSB, Jenkins LW, Dixon CE, Kochanek PM: Hemorrhagic shock after experimental traumatic brain injury in mice: effect on neuronal death. J Neurotrauma. 2009, 26: 889-899. 10.1089/neu.2008.0512.PubMedCentralCrossRefPubMed
6.
go back to reference Hemerka JN, Wu X, Dixon CE, Garman RH, Exo JL, Shellington DK, Blasiole B, Vagni VA, Janesko-Feldman K, Xu M, Wisniewski SR, Bayir H, Jenkins LW, Clark RSB, Tisherman SA, Kochanek PM: Severe brief pressure-controlled hemorrhagic shock after traumatic brain injury exacerbates functional deficits and long-term neuropathological damage in mice. J Neurotrauma. 2012, 29: 2192-2208. 10.1089/neu.2011.2303.PubMedCentralCrossRefPubMed Hemerka JN, Wu X, Dixon CE, Garman RH, Exo JL, Shellington DK, Blasiole B, Vagni VA, Janesko-Feldman K, Xu M, Wisniewski SR, Bayir H, Jenkins LW, Clark RSB, Tisherman SA, Kochanek PM: Severe brief pressure-controlled hemorrhagic shock after traumatic brain injury exacerbates functional deficits and long-term neuropathological damage in mice. J Neurotrauma. 2012, 29: 2192-2208. 10.1089/neu.2011.2303.PubMedCentralCrossRefPubMed
7.
go back to reference Jeremitsky E, Omert L, Dunham CM, Protetch J, Rodriguez A: Harbingers of poor outcome the day after severe brain injury: hypothermia, hypoxia, and hypoperfusion. J Trauma. 2003, 54: 312-319. 10.1097/01.TA.0000037876.37236.D6.CrossRefPubMed Jeremitsky E, Omert L, Dunham CM, Protetch J, Rodriguez A: Harbingers of poor outcome the day after severe brain injury: hypothermia, hypoxia, and hypoperfusion. J Trauma. 2003, 54: 312-319. 10.1097/01.TA.0000037876.37236.D6.CrossRefPubMed
8.
go back to reference Goldstein B, Toweill D, Lai S, Sonnenthal K, Kimberly B: Uncoupling of the autonomic and cardiovascular systems in acute brain injury. Am J Physiol. 1998, 275: R1287-R1292.PubMed Goldstein B, Toweill D, Lai S, Sonnenthal K, Kimberly B: Uncoupling of the autonomic and cardiovascular systems in acute brain injury. Am J Physiol. 1998, 275: R1287-R1292.PubMed
9.
go back to reference McMahon CG, Kenny R, Bennett K, Kirkman E: Modification of acute cardiovascular homeostatic responses to hemorrhage following mild to moderate traumatic brain injury. Crit Care Med. 2008, 36: 216-224. 10.1097/01.CCM.0000295425.41831.85.CrossRefPubMed McMahon CG, Kenny R, Bennett K, Kirkman E: Modification of acute cardiovascular homeostatic responses to hemorrhage following mild to moderate traumatic brain injury. Crit Care Med. 2008, 36: 216-224. 10.1097/01.CCM.0000295425.41831.85.CrossRefPubMed
10.
go back to reference McMahon CG, Kenny R, Bennett K, Little R, Kirkman E: Effect of acute traumatic brain injury on baroreflex function. Shock. 2011, 35: 53-58. 10.1097/SHK.0b013e3181e687c6.CrossRefPubMed McMahon CG, Kenny R, Bennett K, Little R, Kirkman E: Effect of acute traumatic brain injury on baroreflex function. Shock. 2011, 35: 53-58. 10.1097/SHK.0b013e3181e687c6.CrossRefPubMed
11.
go back to reference Yuan XQ, Wade CE: Influences of traumatic brain injury on the outcomes of delayed and repeated hemorrhages. Circ Shock. 1991, 35: 231-236.PubMed Yuan XQ, Wade CE: Influences of traumatic brain injury on the outcomes of delayed and repeated hemorrhages. Circ Shock. 1991, 35: 231-236.PubMed
12.
go back to reference Yuan XQ, Wade CE, Clifford CB: Suppression by traumatic brain injury of spontaneous hemodynamic recovery from hemorrhagic shock in rats. J Neurosurg. 1991, 75: 408-414. 10.3171/jns.1991.75.3.0408.CrossRefPubMed Yuan XQ, Wade CE, Clifford CB: Suppression by traumatic brain injury of spontaneous hemodynamic recovery from hemorrhagic shock in rats. J Neurosurg. 1991, 75: 408-414. 10.3171/jns.1991.75.3.0408.CrossRefPubMed
13.
go back to reference Law MM, Hovda DA, Cryer HG: Fluid-percussion brain injury adversely affects control of vascular tone during hemorrhagic shock. Shock. 1996, 6: 213-217.CrossRefPubMed Law MM, Hovda DA, Cryer HG: Fluid-percussion brain injury adversely affects control of vascular tone during hemorrhagic shock. Shock. 1996, 6: 213-217.CrossRefPubMed
14.
go back to reference den Uil CA, Klijn E, Lagrand WK, Brugts JJ, Ince C, Spronk PE, Simoons ML: The microcirculation in health and critical disease. Prog Cardiovasc Dis. 2008, 51: 161-170. 10.1016/j.pcad.2008.07.002.CrossRefPubMed den Uil CA, Klijn E, Lagrand WK, Brugts JJ, Ince C, Spronk PE, Simoons ML: The microcirculation in health and critical disease. Prog Cardiovasc Dis. 2008, 51: 161-170. 10.1016/j.pcad.2008.07.002.CrossRefPubMed
15.
go back to reference Kerger H, Waschke KF, Ackern KV, Tsai AG, Intaglietta M: Systemic and microcirculatory effects of autologous whole blood resuscitation in severe hemorrhagic shock. Am J Physiol. 1999, 276: H2035-H2043.PubMed Kerger H, Waschke KF, Ackern KV, Tsai AG, Intaglietta M: Systemic and microcirculatory effects of autologous whole blood resuscitation in severe hemorrhagic shock. Am J Physiol. 1999, 276: H2035-H2043.PubMed
16.
go back to reference Sakai H, Hara H, Tsai AG, Tsuchida E, Johnson PC, Intaglietta M: Changes in resistance vessels during hemorrhagic shock and resuscitation in conscious hamster model. Am J Physiol. 1999, 276: H563-H571.PubMed Sakai H, Hara H, Tsai AG, Tsuchida E, Johnson PC, Intaglietta M: Changes in resistance vessels during hemorrhagic shock and resuscitation in conscious hamster model. Am J Physiol. 1999, 276: H563-H571.PubMed
17.
go back to reference Zhao KS, Junker D, Delano FA, Zweifach BW: Microvascular adjustments during irreversible hemorrhagic shock in rat skeletal muscle. Microvasc Res. 1985, 30: 143-153. 10.1016/0026-2862(85)90046-9.CrossRefPubMed Zhao KS, Junker D, Delano FA, Zweifach BW: Microvascular adjustments during irreversible hemorrhagic shock in rat skeletal muscle. Microvasc Res. 1985, 30: 143-153. 10.1016/0026-2862(85)90046-9.CrossRefPubMed
18.
go back to reference Yuan XQ, Wade CE, Clifford CB: Immediate hypertensive response to fluid percussion brain injury may be related to intracerebral hemorrhage and hypothalamic damage. J Neurotrauma. 1991, 8 (3): 219-228. 10.1089/neu.1991.8.219.CrossRefPubMed Yuan XQ, Wade CE, Clifford CB: Immediate hypertensive response to fluid percussion brain injury may be related to intracerebral hemorrhage and hypothalamic damage. J Neurotrauma. 1991, 8 (3): 219-228. 10.1089/neu.1991.8.219.CrossRefPubMed
19.
go back to reference Yuan XQ, Wade CE, Prough DS, DeWitt DS: Traumatic brain injury creates biphasic systemic hemodynamic and organ blood flow responses in rats. J Neurotrauma. 1990, 7 (3): 141-153. 10.1089/neu.1990.7.141.CrossRefPubMed Yuan XQ, Wade CE, Prough DS, DeWitt DS: Traumatic brain injury creates biphasic systemic hemodynamic and organ blood flow responses in rats. J Neurotrauma. 1990, 7 (3): 141-153. 10.1089/neu.1990.7.141.CrossRefPubMed
20.
go back to reference Maegele M, Lippert-Gruener M, Ester-Bode T, Garbe J, Bouillon B, Neugebauer E, Klug N, Lefering R, Neiss W, Angelov D: Multimodal early onset stimulation combined with enriched environment is associated with reduced CNS lesion volume and enhanced reversal of neuromotor dysfunction after traumatic brain injury in rats. Eur J Neurosci. 2005, 21 (9): 2406-2418. 10.1111/j.1460-9568.2005.04070.x.CrossRefPubMed Maegele M, Lippert-Gruener M, Ester-Bode T, Garbe J, Bouillon B, Neugebauer E, Klug N, Lefering R, Neiss W, Angelov D: Multimodal early onset stimulation combined with enriched environment is associated with reduced CNS lesion volume and enhanced reversal of neuromotor dysfunction after traumatic brain injury in rats. Eur J Neurosci. 2005, 21 (9): 2406-2418. 10.1111/j.1460-9568.2005.04070.x.CrossRefPubMed
21.
go back to reference Lippert-Grüner M, Maegele M, Pokorny J, Angelov D, Svestkova O, Wittner M, Torjan S: Early rehabilitation model shows positive effects on neural degeneration and recovery from neuromotor deficits following traumatic brain injury. Physiol Res. 2007, 56 (3): 359-368.PubMed Lippert-Grüner M, Maegele M, Pokorny J, Angelov D, Svestkova O, Wittner M, Torjan S: Early rehabilitation model shows positive effects on neural degeneration and recovery from neuromotor deficits following traumatic brain injury. Physiol Res. 2007, 56 (3): 359-368.PubMed
22.
go back to reference Zhao KS, Liu J, Yang GY, Jin C, Huang Q, Huang X: Peroxynitrite leads to arteriolar smooth muscle cell membrane hyperpolarization and low vasoreactivity in severe shock. Clin Hemorheol Microcirc. 2000, 23: 259-267.PubMed Zhao KS, Liu J, Yang GY, Jin C, Huang Q, Huang X: Peroxynitrite leads to arteriolar smooth muscle cell membrane hyperpolarization and low vasoreactivity in severe shock. Clin Hemorheol Microcirc. 2000, 23: 259-267.PubMed
23.
go back to reference Zhao Q, Zhao K: Inhibition of l-type calcium channels in arteriolar smooth muscle cells is involved in the pathogenesis of vascular hyporeactivity in severe shock. Shock. 2007, 28: 717-721.PubMed Zhao Q, Zhao K: Inhibition of l-type calcium channels in arteriolar smooth muscle cells is involved in the pathogenesis of vascular hyporeactivity in severe shock. Shock. 2007, 28: 717-721.PubMed
25.
go back to reference Dixon CE, Lyeth BG, Povlishock JT, Findling RL, Hamm RJ, Marmarou A, Young HF, Hayes RL: A fluid percussion model of experimental brain injury in the rat. J Neurosurg. 1987, 67: 110-119. 10.3171/jns.1987.67.1.0110.CrossRefPubMed Dixon CE, Lyeth BG, Povlishock JT, Findling RL, Hamm RJ, Marmarou A, Young HF, Hayes RL: A fluid percussion model of experimental brain injury in the rat. J Neurosurg. 1987, 67: 110-119. 10.3171/jns.1987.67.1.0110.CrossRefPubMed
26.
go back to reference Hicks R, Soares H, Smith D, McIntosh T: Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol. 1996, 91: 236-246. 10.1007/s004010050421.CrossRefPubMed Hicks R, Soares H, Smith D, McIntosh T: Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol. 1996, 91: 236-246. 10.1007/s004010050421.CrossRefPubMed
27.
go back to reference Laurer HL, McIntosh TK: Experimental models of brain trauma. Curr Opin Neurol. 1999, 12: 715-721. 10.1097/00019052-199912000-00010.CrossRefPubMed Laurer HL, McIntosh TK: Experimental models of brain trauma. Curr Opin Neurol. 1999, 12: 715-721. 10.1097/00019052-199912000-00010.CrossRefPubMed
28.
go back to reference McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AL: Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience. 1989, 28: 233-244. 10.1016/0306-4522(89)90247-9.CrossRefPubMed McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AL: Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience. 1989, 28: 233-244. 10.1016/0306-4522(89)90247-9.CrossRefPubMed
30.
go back to reference Finnie J: Animal models of traumatic brain injury: a review. Aust Vet J. 2001, 79: 628-633. 10.1111/j.1751-0813.2001.tb10785.x.CrossRefPubMed Finnie J: Animal models of traumatic brain injury: a review. Aust Vet J. 2001, 79: 628-633. 10.1111/j.1751-0813.2001.tb10785.x.CrossRefPubMed
31.
go back to reference Maegele M, Riess P, Sauerland S, Bouillon B, Hess S, McIntosh TK, Mautes A, Brockmann M, Koebke J, Knifka J, Neugebauer EAM: Characterization of a new rat model of experimental combined neurotrauma. Shock. 2005, 23: 476-481. 10.1097/01.shk.0000159929.87737.5c.CrossRefPubMed Maegele M, Riess P, Sauerland S, Bouillon B, Hess S, McIntosh TK, Mautes A, Brockmann M, Koebke J, Knifka J, Neugebauer EAM: Characterization of a new rat model of experimental combined neurotrauma. Shock. 2005, 23: 476-481. 10.1097/01.shk.0000159929.87737.5c.CrossRefPubMed
33.
go back to reference Morales DM, Marklund N, Lebold D, Thompson HJ, Pitkanen A, Maxwell WL, Longhi L, Laurer H, Maegele M, Neugebauer E, Graham DI, Stocchetti N, McIntosh TK: Experimental models of traumatic brain injury: do we really need to build a better mousetrap?. Neuroscience. 2005, 136: 971-989. 10.1016/j.neuroscience.2005.08.030.CrossRefPubMed Morales DM, Marklund N, Lebold D, Thompson HJ, Pitkanen A, Maxwell WL, Longhi L, Laurer H, Maegele M, Neugebauer E, Graham DI, Stocchetti N, McIntosh TK: Experimental models of traumatic brain injury: do we really need to build a better mousetrap?. Neuroscience. 2005, 136: 971-989. 10.1016/j.neuroscience.2005.08.030.CrossRefPubMed
34.
go back to reference Thompson HJ, Lifshitz J, Marklund N, Grady MS, Graham DI, Hovda DA, McIntosh TK: Lateral fluid percussion brain injury: a 15-year review and evaluation. J Neurotrauma. 2005, 22: 42-75. 10.1089/neu.2005.22.42.CrossRefPubMed Thompson HJ, Lifshitz J, Marklund N, Grady MS, Graham DI, Hovda DA, McIntosh TK: Lateral fluid percussion brain injury: a 15-year review and evaluation. J Neurotrauma. 2005, 22: 42-75. 10.1089/neu.2005.22.42.CrossRefPubMed
35.
go back to reference Wang H, Ma Y: Experimental models of traumatic axonal injury. J Clin Neurosci. 2010, 17: 157-162. 10.1016/j.jocn.2009.07.099.CrossRefPubMed Wang H, Ma Y: Experimental models of traumatic axonal injury. J Clin Neurosci. 2010, 17: 157-162. 10.1016/j.jocn.2009.07.099.CrossRefPubMed
36.
go back to reference Gray SD: Rat spinotrapezius muscle preparation for microscopic observation of the terminal vascular bed. Microvasc Res. 1973, 5: 395-400. 10.1016/0026-2862(73)90055-1.CrossRefPubMed Gray SD: Rat spinotrapezius muscle preparation for microscopic observation of the terminal vascular bed. Microvasc Res. 1973, 5: 395-400. 10.1016/0026-2862(73)90055-1.CrossRefPubMed
37.
go back to reference Guo J, Sun K, Wang C, Fang S, Horie Y, Yang J, Liu Y, Wang F, Liu L, Fan J, Hibi T, Han J: Protective effects of dihydroxylphenyl lactic acid and salvianolic acid b on lps-induced mesenteric microcirculatory disturbance in rats. Shock. 2008, 29: 205-211.PubMed Guo J, Sun K, Wang C, Fang S, Horie Y, Yang J, Liu Y, Wang F, Liu L, Fan J, Hibi T, Han J: Protective effects of dihydroxylphenyl lactic acid and salvianolic acid b on lps-induced mesenteric microcirculatory disturbance in rats. Shock. 2008, 29: 205-211.PubMed
38.
go back to reference Han JY, Miura S, Akiba Y, Higuchi H, Kato S, Suzuki H, Yokoyama H, Ishii H: Chronic ethanol consumption exacerbates microcirculatory damage in rat mesentery after reperfusion. Am J Physiol Gastrointest Liver Physiol. 2001, 280: G939-G948.PubMed Han JY, Miura S, Akiba Y, Higuchi H, Kato S, Suzuki H, Yokoyama H, Ishii H: Chronic ethanol consumption exacerbates microcirculatory damage in rat mesentery after reperfusion. Am J Physiol Gastrointest Liver Physiol. 2001, 280: G939-G948.PubMed
39.
go back to reference Russell J, Cooper D, Tailor A, Stokes KY, Granger DN: Low venular shear rates promote leukocyte-dependent recruitment of adherent platelets. Am J Physiol Gastrointest Liver Physiol. 2003, 284: G123-G129.CrossRefPubMed Russell J, Cooper D, Tailor A, Stokes KY, Granger DN: Low venular shear rates promote leukocyte-dependent recruitment of adherent platelets. Am J Physiol Gastrointest Liver Physiol. 2003, 284: G123-G129.CrossRefPubMed
40.
go back to reference Beckman DL, Iams SG: Circulating catecholamines in cats before and after lethal head injury. Proc Soc Exp Biol Med. 1979, 160: 200-202. 10.3181/00379727-160-40419.CrossRefPubMed Beckman DL, Iams SG: Circulating catecholamines in cats before and after lethal head injury. Proc Soc Exp Biol Med. 1979, 160: 200-202. 10.3181/00379727-160-40419.CrossRefPubMed
41.
go back to reference Gao C, Liu X, Shi H, Xu S, Ji Z, Wang C, Wu P, Liu Z, Zhao S: Relationship between sympathetic nervous activity and inflammatory response after subarachnoid hemorrhage in a perforating canine model. Auton Neurosci. 2009, 147: 70-74. 10.1016/j.autneu.2009.01.010.CrossRefPubMed Gao C, Liu X, Shi H, Xu S, Ji Z, Wang C, Wu P, Liu Z, Zhao S: Relationship between sympathetic nervous activity and inflammatory response after subarachnoid hemorrhage in a perforating canine model. Auton Neurosci. 2009, 147: 70-74. 10.1016/j.autneu.2009.01.010.CrossRefPubMed
42.
go back to reference Rosner MJ, Newsome HH, Becker DP: Mechanical brain injury: the sympathoadrenal response. J Neurosurg. 1984, 61: 76-86. 10.3171/jns.1984.61.1.0076.CrossRefPubMed Rosner MJ, Newsome HH, Becker DP: Mechanical brain injury: the sympathoadrenal response. J Neurosurg. 1984, 61: 76-86. 10.3171/jns.1984.61.1.0076.CrossRefPubMed
43.
go back to reference Joyner MJ, Dietz NM: Sympathetic vasodilation in human muscle. Acta Physiol Scand. 2003, 177: 329-336. 10.1046/j.1365-201X.2003.01090.x.CrossRefPubMed Joyner MJ, Dietz NM: Sympathetic vasodilation in human muscle. Acta Physiol Scand. 2003, 177: 329-336. 10.1046/j.1365-201X.2003.01090.x.CrossRefPubMed
44.
go back to reference Matsukawa K, Shindo T, Shirai M, Ninomiya I: Direct observations of sympathetic cholinergic vasodilatation of skeletal muscle small arteries in the cat. J Physiol. 1997, 500: 213-225.PubMedCentralCrossRefPubMed Matsukawa K, Shindo T, Shirai M, Ninomiya I: Direct observations of sympathetic cholinergic vasodilatation of skeletal muscle small arteries in the cat. J Physiol. 1997, 500: 213-225.PubMedCentralCrossRefPubMed
45.
go back to reference Nagai M, Pleschka K: Brain stem sites mediating adrenergic and non-adrenergic vasodilatation in the dog’s nose and tongue. J Auton Nerv Syst. 1981, 4: 365-379. 10.1016/0165-1838(81)90039-4.CrossRefPubMed Nagai M, Pleschka K: Brain stem sites mediating adrenergic and non-adrenergic vasodilatation in the dog’s nose and tongue. J Auton Nerv Syst. 1981, 4: 365-379. 10.1016/0165-1838(81)90039-4.CrossRefPubMed
46.
go back to reference Marshall JM: The influence of the sympathetic nervous system on individual vessels of the microcirculation of skeletal muscle of the rat. J Physiol. 1982, 332: 169-186.PubMedCentralCrossRefPubMed Marshall JM: The influence of the sympathetic nervous system on individual vessels of the microcirculation of skeletal muscle of the rat. J Physiol. 1982, 332: 169-186.PubMedCentralCrossRefPubMed
47.
go back to reference Lundvall J, Hillman J: Fluid transfer from skeletal muscle to blood during hemorrhage. importance of beta adrenergic vascular mechanisms. Acta Physiol Scand. 1978, 102: 450-458. 10.1111/j.1748-1716.1978.tb06093.x.CrossRefPubMed Lundvall J, Hillman J: Fluid transfer from skeletal muscle to blood during hemorrhage. importance of beta adrenergic vascular mechanisms. Acta Physiol Scand. 1978, 102: 450-458. 10.1111/j.1748-1716.1978.tb06093.x.CrossRefPubMed
48.
go back to reference Maegele M, Sauerland S, Bouillon B, Schafer U, Trubel H, Riess P, Neugebauer EAM: Differential immunoresponses following experimental traumatic brain injury, bone fracture and “two-hit”-combined neurotrauma. Inflamm Res. 2007, 56: 318-323. 10.1007/s00011-007-6141-3.CrossRefPubMed Maegele M, Sauerland S, Bouillon B, Schafer U, Trubel H, Riess P, Neugebauer EAM: Differential immunoresponses following experimental traumatic brain injury, bone fracture and “two-hit”-combined neurotrauma. Inflamm Res. 2007, 56: 318-323. 10.1007/s00011-007-6141-3.CrossRefPubMed
49.
go back to reference Probst C, Mirzayan MJ, Mommsen P, Zeckey C, Tegeder T, Geerken L, Maegele M, Samii A, van Griensven M: Systemic inflammatory effects of traumatic brain injury, femur fracture, and shock: an experimental murine polytrauma model. Mediators Inflamm. 2012, 2012: 136020-PubMedCentralCrossRefPubMed Probst C, Mirzayan MJ, Mommsen P, Zeckey C, Tegeder T, Geerken L, Maegele M, Samii A, van Griensven M: Systemic inflammatory effects of traumatic brain injury, femur fracture, and shock: an experimental murine polytrauma model. Mediators Inflamm. 2012, 2012: 136020-PubMedCentralCrossRefPubMed
50.
go back to reference Fan L, Young PR, Barone FC, Feuerstein GZ, Smith DH, McIntosh TK: Experimental brain injury induces differential expression of tumor necrosis factor-alpha mrna in the cns. Brain Res Mol Brain Res. 1996, 36: 287-291. 10.1016/0169-328X(95)00274-V.CrossRefPubMed Fan L, Young PR, Barone FC, Feuerstein GZ, Smith DH, McIntosh TK: Experimental brain injury induces differential expression of tumor necrosis factor-alpha mrna in the cns. Brain Res Mol Brain Res. 1996, 36: 287-291. 10.1016/0169-328X(95)00274-V.CrossRefPubMed
51.
go back to reference Kita T, Liu L, Tanaka N, Kinoshita Y: The expression of tumor necrosis factor-alpha in the rat brain after fluid percussive injury. Int J Legal Med. 1997, 110: 305-311. 10.1007/s004140050093.CrossRefPubMed Kita T, Liu L, Tanaka N, Kinoshita Y: The expression of tumor necrosis factor-alpha in the rat brain after fluid percussive injury. Int J Legal Med. 1997, 110: 305-311. 10.1007/s004140050093.CrossRefPubMed
52.
go back to reference Vicaut E, Hou X, Payen D, Bousseau A, Tedgui A: Acute effects of tumor necrosis factor on the microcirculation in rat cremaster muscle. J Clin Invest. 1991, 87: 1537-1540. 10.1172/JCI115165.PubMedCentralCrossRefPubMed Vicaut E, Hou X, Payen D, Bousseau A, Tedgui A: Acute effects of tumor necrosis factor on the microcirculation in rat cremaster muscle. J Clin Invest. 1991, 87: 1537-1540. 10.1172/JCI115165.PubMedCentralCrossRefPubMed
53.
go back to reference Adanali G, Ozer K, Siemionow MM: Acute alterations in muscle flap microcirculation during tumor necrosis factor alpha-induced inflammation. Ann Plast Surg. 2001, 47: 652-659. 10.1097/00000637-200112000-00013.CrossRefPubMed Adanali G, Ozer K, Siemionow MM: Acute alterations in muscle flap microcirculation during tumor necrosis factor alpha-induced inflammation. Ann Plast Surg. 2001, 47: 652-659. 10.1097/00000637-200112000-00013.CrossRefPubMed
54.
go back to reference Minghini A, Britt LD, Hill MA: Interleukin-1 and interleukin-6 mediated skeletal muscle arteriolar vasodilation: in vitro versus in vivo studies. Shock. 1998, 9: 210-215. 10.1097/00024382-199803000-00009.CrossRefPubMed Minghini A, Britt LD, Hill MA: Interleukin-1 and interleukin-6 mediated skeletal muscle arteriolar vasodilation: in vitro versus in vivo studies. Shock. 1998, 9: 210-215. 10.1097/00024382-199803000-00009.CrossRefPubMed
55.
go back to reference Jaeschke H, Farhood A: Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol. 1991, 260: G355-G362.PubMed Jaeschke H, Farhood A: Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol. 1991, 260: G355-G362.PubMed
56.
go back to reference Serracino-Inglott F, Habib NA, Mathie RT: Hepatic ischemia-reperfusion injury. Am J Surg. 2001, 181: 160-166. 10.1016/S0002-9610(00)00573-0.CrossRefPubMed Serracino-Inglott F, Habib NA, Mathie RT: Hepatic ischemia-reperfusion injury. Am J Surg. 2001, 181: 160-166. 10.1016/S0002-9610(00)00573-0.CrossRefPubMed
57.
go back to reference Douzinas EE, Livaditi O, Tasoulis M, Prigouris P, Bakos D, Goutas N, Vlachodimitropoulos D, Andrianakis I, Betrosian A, Tsoukalas GD: Nitrosative and oxidative stresses contribute to post-ischemic liver injury following severe hemorrhagic shock: the role of hypoxemic resuscitation. PLoS ONE. 2012, 7: e32968-10.1371/journal.pone.0032968.PubMedCentralCrossRefPubMed Douzinas EE, Livaditi O, Tasoulis M, Prigouris P, Bakos D, Goutas N, Vlachodimitropoulos D, Andrianakis I, Betrosian A, Tsoukalas GD: Nitrosative and oxidative stresses contribute to post-ischemic liver injury following severe hemorrhagic shock: the role of hypoxemic resuscitation. PLoS ONE. 2012, 7: e32968-10.1371/journal.pone.0032968.PubMedCentralCrossRefPubMed
58.
go back to reference Venkatesh B, Townsend S, Boots RJ: Does splanchnic ischemia occur in isolated neurotrauma? a prospective observational study. Crit Care Med. 1999, 27: 1175-1180. 10.1097/00003246-199906000-00047.CrossRefPubMed Venkatesh B, Townsend S, Boots RJ: Does splanchnic ischemia occur in isolated neurotrauma? a prospective observational study. Crit Care Med. 1999, 27: 1175-1180. 10.1097/00003246-199906000-00047.CrossRefPubMed
59.
go back to reference Backstrom T, Liska J, Oldner A, Lockowandt U, Franco-Cereceda A: Splanchnic metabolism during gut ischemia and short-term endotoxin and hemorrhagic shock as evaluated by intravasal microdialysis. Shock. 2004, 21: 572-578. 10.1097/01.shk.0000127069.65490.65.CrossRefPubMed Backstrom T, Liska J, Oldner A, Lockowandt U, Franco-Cereceda A: Splanchnic metabolism during gut ischemia and short-term endotoxin and hemorrhagic shock as evaluated by intravasal microdialysis. Shock. 2004, 21: 572-578. 10.1097/01.shk.0000127069.65490.65.CrossRefPubMed
60.
go back to reference Manders WT, Vatner SF: Effects of sodium pentobarbital anesthesia on left ventricular function and distribution of cardiac output in dogs, with particular reference to the mechanism for tachycardia. Circ Res. 1976, 39: 512-10.1161/01.RES.39.4.512.CrossRefPubMed Manders WT, Vatner SF: Effects of sodium pentobarbital anesthesia on left ventricular function and distribution of cardiac output in dogs, with particular reference to the mechanism for tachycardia. Circ Res. 1976, 39: 512-10.1161/01.RES.39.4.512.CrossRefPubMed
61.
go back to reference Vatner SF: Effects of anesthesia on cardiovascular control mechanisms. Environ Health Persp. 1978, 26: 193-206.CrossRef Vatner SF: Effects of anesthesia on cardiovascular control mechanisms. Environ Health Persp. 1978, 26: 193-206.CrossRef
62.
go back to reference Kawaue Y, Iriuchijima J: Changes in cardiac output and peripheral flows on pentobarbital anesthesia in the rat. Jpn J Physiol. 1984, 34 (2): 283-294. 10.2170/jjphysiol.34.283.CrossRefPubMed Kawaue Y, Iriuchijima J: Changes in cardiac output and peripheral flows on pentobarbital anesthesia in the rat. Jpn J Physiol. 1984, 34 (2): 283-294. 10.2170/jjphysiol.34.283.CrossRefPubMed
63.
go back to reference Boerma EC: The microcirculation as a clinical concept: work in progress. Curr Opin Crit Care. 2009, 15: 261-265. 10.1097/MCC.0b013e32832b0ff4.CrossRefPubMed Boerma EC: The microcirculation as a clinical concept: work in progress. Curr Opin Crit Care. 2009, 15: 261-265. 10.1097/MCC.0b013e32832b0ff4.CrossRefPubMed
Metadata
Title
Superimposed traumatic brain injury modulates vasomotor responses in third-order vessels after hemorrhagic shock
Authors
Bo Chen
Manuel Mutschler
Yongjun Yuan
Edmund Neugebauer
Qiaobing Huang
Marc Maegele
Publication date
01-12-2013
Publisher
BioMed Central
DOI
https://doi.org/10.1186/1757-7241-21-77

Other articles of this Issue 1/2013

Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine 1/2013 Go to the issue