Bloodbrain barrier permeability is positively correlated with cerebral microvascular perfusion in the early fluid percussion-injured brain of the rat

Laboratory Investigation

Volumn 92, Issue 11, 2012, Pages 1623-1634

  Lin, Yong ^a   Pan, Yaohua ^a   Wang, Mingliang ^b   Huang, Xianjian ^a   Yin, Yuhua ^a   Wang, Yu ^a   Jia, Feng ^a   Xiong, Wenhao ^a   Zhang, Nu ^c   Jiang, Ji Yao ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^c WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

blood brain barrier; MRI; rat; traumatic brain injury; vascular reactivity

Indexed keywords

GELATIN; GELATINASE B; DIAGNOSTIC AGENT; EVANS BLUE; MMP9 PROTEIN, RAT;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; BRAIN CAPILLARY; BRAIN CORTEX; BRAIN PERFUSION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; HEART PERFUSION; MALE; MEMBRANE PERMEABILITY; MICROVASCULATURE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY; ZYMOGRAPHY; ANIMAL; BRAIN CIRCULATION; BRAIN INJURY; CAPILLARY PERMEABILITY; ENZYMOLOGY; METABOLISM; MICROCIRCULATION; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CAPILLARY PERMEABILITY; CEREBROVASCULAR CIRCULATION; EVANS BLUE; MAGNETIC RESONANCE IMAGING; MALE; MATRIX METALLOPROTEINASE 9; MICROCIRCULATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84868595134     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2012.118     Document Type: Article

References (47)

1. Lindsay KW, McLatchie G, Jennett B. Serious head injury in sport. BMJ 1980;281:789-791. (Pubitemid 10048555)
2. Ghajar J. Traumatic brain injury. Lancet 2000;356:923-929.
3. Dewey CW. Emergency management of the head trauma patient. Vet Clin N Am Small Anim Pract 2000;30:207-225.
4. Shackford SR, Mackersie RC, Davis JW, et al. Epidemiology and pathology of traumatic deaths occurring at a Level I Trauma Center in a regionalized system: the importance of secondary brain injury J Trauma 1989;29:1392-1397. (Pubitemid 19283262)
5. Werner C, Engelhard K. Pathophysiology of traumatic brain injury. Br J Anaesth 2007;99:4-9. (Pubitemid 47072553)
6. Sande A, West C. Traumatic brain injury: a review of pathophysiology and management. J Vet Emerg Crit Care (San Antonio) 2010;20: 177-190.
7. Janzer RC, Raff M. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 1987;325:253-257. (Pubitemid 17049884)
8. Kniesel U, Wolburg H. Tight junctions of the blood-brain barrier. Cell Mol Neurobiol 2000;20:57-76. (Pubitemid 30090916)
9. Duvdevani R, Roof RL, Fulop Z, et al. Blood-brain barrier breakdown and edema formation following frontal cortical contusion: does hormonal status play a role?. J Neurotrauma 1995;12:65-75.
10. Shigemori Y, Katayama Y, Mori T, et al. Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir Suppl 2006;96:130-133.
11. Fukuda K, Tanno H, Okimura Y, et al. The blood-brain barrier disruption to circulating proteins in the early period after fluid percussion brain injury in rats. J Neurotrauma 1995;12:315-324.
12. Habgood MD, Bye N, Dziegielewska KM, et al. Changes in blood-brain barrier permeability to large and small molecules following traumatic brain injury in mice. Eur J Neurosci 2007;25:231-238. (Pubitemid 46096237)
13. Ford JC, Wood AK, Van Winkle TJ, et al. Magnetic resonance imaging observations of blood-brain-barrier permeability in an animal model of brain injury. Acad Radiol 1997;4:115-126. (Pubitemid 127469598)
14. Schneider G, Fries P, Wagner-Jochem D, et al. Pathophysiological changes after traumatic brain injury: comparison of two experimental animal models by means of MRI. MAGMA 2002;14:233-241. (Pubitemid 34786974)
15. Yamaguchi M, Jadhav V, Obenaus A, et al. Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery 2007;61:1067-1075, discussion 1075-1076. (Pubitemid 350306967)
16. Nilsson P, Gazelius B, Carlson H, et al. Continuous measurement of changes in regional cerebral blood flow following cortical compression contusion trauma in the rat. J Neurotrauma 1996;13: 201-207. (Pubitemid 26142612)
17. Hayward NM, Tuunanen PI, Immonen R, et al. Magnetic resonance imaging of regional hemodynamic and cerebrovascular recovery after lateral fluid-percussion brain injury in rats. J Cereb Blood Flow Metab 2011;31:166-177.
18. McGoron AJ, Capille M, Georgiou MF, et al. Post traumatic brain perfusion SPECT analysis using reconstructed ROI maps of radioactive microsphere derived cerebral blood flow and statistical parametric mapping. BMC Med Imag 2008;8:4.
19. Gö bel U, Theilen H, Kuschinsky W. Congruence of total and perfused capillary network in rat brains. Circ Res 1990;66:271-281. (Pubitemid 20041159)
20. Zoccoli G, Lucchi ML, Andreoli E, et al. Brain capillary perfusion during sleep. J Cereb Blood Flow Metab 1996;16:1312-1318. (Pubitemid 26365385)
21. Dawson DA, Ruetzler CA, Hallenbeck JM. Temporal impairment of microcirculatory perfusion following focal cerebral ischemia in the spontaneously hypertensive rat. Brain Res 1997;749:200-208. (Pubitemid 27104200)
22. Clifton GL, Choi SC, Miller ER, et al. Intercenter variance in clinical trials of head trauma-experience of the National Acute Brain Injury Study: Hypothermia. J Neurosurg 2001;95:751-755. (Pubitemid 33043346)
23. Grände PO. The 'Lund Concept' for the treatment of severe head trauma-physiological principles and clinical application. Intens Care Med 2006;32:1475-1484.
24. McIntosh TK, Vink R, Noble L, et al. Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 1989;28:233-244. (Pubitemid 19026758)
25. del Valle J, Camins A, Pallas M, et al. A new method for determining blood-brain barrier integrity based on intracardiac perfusion of an Evans Blue-Hoechst cocktail. J Neurosci Methods 2008;174:42-49.
26. Weiss HR. Measurement of cerebral capillary perfusion with a fluorescent label. Microvasc Res 1988;36:172-180.
27. Barth KN, Onesti ST, Krauss WE, et al. A simple and reliable technique to monitor intracranial pressure in the rat: technical note. Neurosurgery 1992;30:138-140.
28. Wang-Fischer Y, Koetzner L. Endpoints for stroke studies. In: Wang-Fischer Y (ed) Manual of Stroke Models in Rats, Boca Raton, FL, 2009; pp193-221.
29. Kroppenstedt SN, Kern M, Thomale UW, et al. Effect of cerebral perfusion pressure on contusion volume following impact injury. J Neurosurg 1999;90:520-526. (Pubitemid 29104601)
30. Hawkins BT, Egleton RD. Fluorescence imaging of blood-brain barrier disruption. J Neurosci Methods 2006;151:262-267. (Pubitemid 43294448)
31. Oertel M, Boscardin WJ, Obrist WD, et al. Posttraumatic vasospasm: the epidemiology, severity, and time course of an underestimated phenomenon: a prospective study performed in 299 patients J Neurosurg 2005;103:812-824. (Pubitemid 43194574)
32. Baethmann A, Eriskat J, Stoffel M, et al. Special aspects of severe head injury: recent developments. Curr Opin Anaesthesiol 1998; 11:193-200. (Pubitemid 28165573)
33. Smith MJ, Hartl R. Maintaining cerebral perfusion after polytrauma using arginine vasopressin: a classic drug revisited. Crit Care Med 2008;36:2703-2704.
34. Lundblad C, Grände PO, Bentzer P. A mouse model for evaluation of capillary perfusion, microvascular permeability, cortical blood flow, and cortical edema in the traumatized brain. J Neurotrauma 2004; 21:741-753. (Pubitemid 38880246)
35. Park E, Bell JD, Siddiq IP, et al. An analysis of regional microvascular loss and recovery following two grades of fluid percussion trauma: a role for hypoxia-inducible factors in traumatic brain injury. J Cereb Blood Flow Metab 2009;29:575-584.
36. Kita T, Liu L, Tanaka N, et al. The expression of tumor necrosis factoralpha in the rat brain after fluid percussive injury. Int J Legal Med 1997;110:305-311. (Pubitemid 27475675)
37. Maikos JT, Shreiber DI. Immediate damage to the blood-spinal cord barrier due to mechanical trauma. J Neurotrauma 2007;24:492-507. (Pubitemid 46598283)
38. Uyama O, Okamura N, Yanase M, et al. Quantitative evaluation of vascular permeability in the gerbil brain after transient ischemia using Evans Blue fluorescence. J Cereb Blood Flow Metab 1988;8: 282-284. (Pubitemid 18079698)
39. Rancan M, Morganti-Kossmann MC, Barnum SR, et al. Central nervous system-targeted complement inhibition mediates neuroprotection after closed head injury in transgenic mice. J Cereb Blood Flow Metab 2003;23:1070-1074. (Pubitemid 37082432)
40. Beaumont A, Marmarou A, Fatouros P, et al. Secondary insults worsen blood brain barrier dysfunction assessed by MRI in cerebral contusion. Acta Neurochir Suppl 2002;81:217-219.
41. Beaumont A, Marmarou A, Hayasaki K, et al. The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury. Acta Neurochir Suppl 2000;76:125-129.
42. Tanno H, Nockels RP, Pitts LH, et al. Breakdown of the blood-brain barrier after fluid percussive brain injury in the rat. Part 1: Distribution and time course of protein extravasation. J Neurotrauma 1992;9:21-32.
43. Lotocki G, Vaccari JP, Perez ER, et al. Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of post-traumatic hypothermia. J Neurotrauma 2009;26:1123-1134.
44. Mathew P, Bullock R, Teasdale G, et al. Changes in local microvascular permeability and in the effect of intervention with 21-aminosteroid (Tirilazad) in a new experimental model of focal cortical injury in the rat. J Neurotrauma 1996;13:465-472. (Pubitemid 26313525)
45. Marmarou A, Signoretti S, Aygok G, et al. Traumatic brain edema in diffuse and focal injury: cellular or vasogenic?. Acta Neurochir Suppl 2006;96:24-29.
46. Hayashi T, Kaneko Y, Yu S, et al. Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats. Brain Res 2009;1280:172-177.
47. Higashida T, Kreipke CW, Rafols JA, et al. The role of hypoxia-inducible factor-1a, aquaporin-4, and matrix metalloproteinase-9 in blood-brain barrier disruption and brain edema after traumatic brain injury. J Neurosurg 2011;114:92-101.