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

Scandinavian Journal of Trauma, Resuscitation and Emergency Medicine

Volumn 21, Issue 1, 2013, Pages

  Chen, Bo ^a   Mutschler, Manuel ^b   Yuan, Yongjun ^a   Neugebauer, Edmund ^b   Huang, Qiaobing ^a   Maegele, Marc ^b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF WITTEN HERDECKE   (Germany)

Author keywords

Brain injury; Hemorrhagic shock; Lateral fluid percussion; Microcirculation; Spinotrapezius muscle; Third order vessels; Trauma; Vasomotor response

Indexed keywords

SODIUM CHLORIDE;

ANIMAL; ARTERIOLE; ARTICLE; BLOOD FLOW; BRAIN INJURY; COMPARATIVE STUDY; DISEASE MODEL; FLUID THERAPY; HEMORRHAGIC SHOCK; MALE; METHODOLOGY; MICROCIRCULATION; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; RESUSCITATION; SPRAGUE DAWLEY RAT; VASODILATATION; VENULE;

ANIMALS; ARTERIOLES; BRAIN INJURIES; DISEASE MODELS, ANIMAL; FLUID THERAPY; MALE; MICROCIRCULATION; RATS; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; RESUSCITATION; SALINE SOLUTION, HYPERTONIC; SHOCK, HEMORRHAGIC; VASODILATION; VENULES;

EID: 84888264503     PISSN: None     EISSN: 17577241     Source Type: Journal    
DOI: 10.1186/1757-7241-21-77     Document Type: Article

References (63)

1. 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, 2545772, 3133060.
2. Bruns JJ, Hauser WA. The epidemiology of traumatic brain injury: a review. Epilepsia 2003, 44(Suppl 10):2-10.
3. 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, 19882185.
4. 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, 7869433.
5. 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, 2694227,2694227, 18781889.
6. 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, 3472682, 22738159.
7. 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, 12579057.
8. 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.
9. 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, 18090349.
10. 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, 20458265.
11. Yuan XQ, Wade CE. Influences of traumatic brain injury on the outcomes of delayed and repeated hemorrhages. Circ Shock 1991, 35:231-236.
12. 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, 1651379.
13. Law MM, Hovda DA, Cryer HG. Fluid-percussion brain injury adversely affects control of vascular tone during hemorrhagic shock. Shock 1996, 6:213-217.
14. 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, 18774014.
15. 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.
16. 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.
17. 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, 2931578.
18. 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, 1803030.
19. 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, 2258945.
20. 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, 15932599.
21. 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.
22. 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.
23. 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.
24. Cernak I. Animal models of head trauma. NeuroRx 2005, 2:410-422. 10.1602/neurorx.2.3.410, 1144485, 16389305.
25. 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, 3598659.
26. 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, 8834535.
27. Laurer HL, McIntosh TK. Experimental models of brain trauma. Curr Opin Neurol 1999, 12:715-721. 10.1097/00019052-199912000-00010, 10676754.
28. 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, 2761692.
29. Albert-Weissenberger C, Siren A. Experimental traumatic brain injury. Exp Transl Stroke Med 2010, 2:16. 10.1186/2040-7378-2-16, 2930598, 20707892.
30. 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, 11702936.
31. 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, 15834316.
32. McIntyre A, Lee T, Willems G, Teasell R. Evidence-based review of moderate to severe aquired brain injury. traumatic brain injury and animal research (modul 19) http://www.abiebr.com/sites/default/files/modules/Module%2019-Traumatic%20Brain%20Injury%20and%20Animal%20Research_V9_2013.pdf].
33. 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, 16242846.
34. 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, 15665602.
35. Wang H, Ma Y. Experimental models of traumatic axonal injury. J Clin Neurosci 2010, 17:157-162. 10.1016/j.jocn.2009.07.099, 20042337.
36. 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, 4709736.
37. 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.
38. 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.
39. 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.
40. 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, 419147.
41. 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, 19217831.
42. 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, 6726414.
43. Joyner MJ, Dietz NM. Sympathetic vasodilation in human muscle. Acta Physiol Scand 2003, 177:329-336. 10.1046/j.1365-201X.2003.01090.x, 12609003.
44. 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. 1159371, 9097945.
45. 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, 7310050.
46. 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. 1197393, 7153926.
47. 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, 207084.
48. 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, 17687516.
49. 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. 3316998, 22529516.
50. 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, 8965649.
51. 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, 9387012.
52. 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, 295234, 2022725.
53. 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, 11756837.
54. 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, 9525329.
55. 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.
56. 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, 11425059.
57. 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, 3293918, 22403729.
58. 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, 10397225.
59. 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, 15167688.
60. 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, 963835.
61. Vatner SF. Effects of anesthesia on cardiovascular control mechanisms. Environ Health Persp 1978, 26:193-206.
62. 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, 6471612.
63. Boerma EC. The microcirculation as a clinical concept: work in progress. Curr Opin Crit Care 2009, 15:261-265. 10.1097/MCC.0b013e32832b0ff4, 19346939.