Spatiotemporal correlations between blood-brain barrier permeability and apparent diffusion coefficient in a rat model of ischemic stroke

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Taheri, Saeid ^a   Candelario Jalil, Eduardo ^a   Estrada, Eduardo Y ^a   Rosenberg, Gary A ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL FUNCTION; BRAIN CORTEX; BRAIN DAMAGE; BRAIN EDEMA; BRAIN REGION; CEREBROVASCULAR ACCIDENT; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CONVALESCENCE; CORRELATIONAL STUDY; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; DISEASE MODEL; IMAGE ANALYSIS; IMAGE QUALITY; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RAT; REPERFUSION; ANIMAL; BRAIN ISCHEMIA; PATHOPHYSIOLOGY; PERMEABILITY; STROKE;

RATTUS;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; PERMEABILITY; RATS; STROKE;

EID: 68749108299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006597     Document Type: Article

References (38)

1. Jiang Q, Zhang RL, Zhang ZG, Ewing JR, Divine GW, et al. (1998) Diffusion-, T2-, and perfusion-weighted nuclear magnetic resonance imaging of middle cerebral artery embolic stroke and recombinant tissue plasminogen activator intervention in the rat. J Cereb Blood Flow Metab 18: 758-767.
2. Engelhorn T, Doerfler A, Kastrup A, Beaulieu C, de Crespigny A, et al. (1999) Decompressive craniectomy, reperfusion, or a combination for early treatment of acute "malignant" cerebral hemispheric stroke in rats? Potential mechanisms studied by MRI. Stroke 30: 1456-1463.
3. Dijkhuizen RM, Asahi M, Wu O, Rosen BR, Lo EH (2002) Rapid breakdown of microvascular barriers and subsequent hemorrhagic transformation after delayed recombinant tissue plasminogen activator treatment in a rat embolic stroke model. Stroke 33: 2100-2104.
4. Sood RR, Taheri S, Candelario-Jalil E, Estrada EY, Rosenberg GA (2008) Early beneficial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J Cereb Blood Flow Metab 28: 431-438.
5. Marks MP, Tong DC, Beaulieu C, Albers GW, de Crespigny A, et al. (1999) Evaluation of early reperfusion and i.v. tPA therapy using diffusion- and perfusion-weighted MRI. Neurology 52: 1792-1798.
6. Mitsias PD, Jacobs MA, Hammoud R, Pasnoor M, Santhakumar S, et al. (2002) Multiparametric MRI ISODATA ischemic lesion analysis: correlation with the clinical neurological deficit and single-parameter MRI techniques. Stroke 33: 2839-2844.
7. Lansberg MG, Thijs VN, Bammer R, Olivot JM, Marks MP, et al. (2008) The MRA-DWI mismatch identifies patients with stroke who are likely to benefit from reperfusion. Stroke 39: 2491-2496.
8. Warach S, Latour LL (2004) Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 35: 2659-2661.
9. Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S (2004) Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 56: 468-477.
10. Yang Q, Tress BM, Barber PA, Desmond PM, Darby DG, et al. (1999) Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 30: 2382-2390.
11. Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Leon OS, Fiebich BL (2007) Post-ischaemic treatment with the cyclooxygenase-2 inhibitor nimesulide reduces blood-brain barrier disruption and leukocyte infiltration following transient focal cerebral ischaemia in rats. J Neurochem 100: 1108-1120.
12. Rosenberg GA, Estrada EY, Dencoff JE (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 29: 2189-2195.
13. Belayev L, Busto R, Zhao W, Ginsberg MD (1996) Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res 739: 88-96.
14. Neumann-Haefelin T, Kastrup A, de Crespigny A, Yenari MA, Ringer T, et al. (2000) Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 31: 1965-1973.
15. Plaschke K, Bardenheuer HJ, Martin E, Sartor K, Heiland S (2006) Evolution of apparent diffusion coefficient and transverse relaxation time (T2) in the subchronic stage of global cerebral oligemia in different rat models. Exp Brain Res 169: 361-368.
16. Ringer TM, Neumann-Haefelin T, Sobel RA, Moseley ME, Yenari MA (2001) Reversal of early diffusion-weighted magnetic resonance imaging abnormalities does not necessarily reflect tissue salvage in experimental cerebral ischemia. Stroke 32: 2362-2369.
17. Nagaraja TN, Karki K, Ewing JR, Croxen RL, Knight RA (2008) Identification of variations in blood-brain barrier opening after cerebral ischemia by dual contrast-enhanced magnetic resonance imaging and T1sat measurements. Stroke 39: 427-432.
18. Liu KF, Li F, Tatlisumak T, Garcia JH, Sotak CH, et al. (2001) Regional variations in the apparent diffusion coefficient and the intracellular distribution of water in rat brain during acute focal ischemia. Stroke 32: 1897-1905.
19. Nicoli F, Lefur Y, Denis B, Ranjeva JP, Confort-Gouny S, et al. (2003) Metabolic counterpart of decreased apparent diffusion coefficient during hyperacute ischemic stroke: a brain proton magnetic resonance spectroscopic imaging study. Stroke 34: e82-e88.
20. Knight RA, Nagaraja TN, Ewing JR, Nagesh V, Whitton PA, et al. (2005) Quantitation and localization of blood-to-brain influx by magnetic resonance imaging and quantitative autoradiography in a model of transient focal ischemia. Magn Reson Med 54: 813-821.
21. Ewing JR, Knight RA, Nagaraja TN, Yee JS, Nagesh V, et al. (2003) Patlak plots of Gd-DTPA MRI data yield blood-brain transfer constants concordant with those of 14C-sucrose in areas of blood-brain opening. Magn Reson Med 50: 283-292.
22. Larsson HB, Stubgaard M, Frederiksen JL, Jensen M, Henriksen O, et al. (1990) Quantitation of blood-brain barrier defect by magnetic resonance imaging and gadolinium-DTPA in patients with multiple sclerosis and brain tumors. Magn Reson Med 16: 117-131.
23. Tofts PS (1996) Optimal detection of blood-brain barrier defects with Gd-DTPA MRI-the influences of delayed imaging and optimised repetition time. Magn Reson Imaging 14: 373-380.
24. Tofts PS, Kermode AG (1991) Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magn Reson Med 17: 357-367.
25. Patlak CS, Blasberg RG (1985) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab 5: 584-590.
26. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA (2007) Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 27: 697-709.
27. Jiang Q, Ewing JR, Ding GL, Zhang L, Zhang ZG, et al. (2005) Quantitative evaluation of BBB permeability after embolic stroke in rat using MRI. J Cereb Blood Flow Metab 25: 583-592.
28. Carano RA, Li F, Irie K, Helmer KG, Silva MD, et al. (2000) Multispectral analysis of the temporal evolution of cerebral ischemia in the rat brain. J Magn Reson Imaging 12: 842-858.
29. Li F, Silva MD, Sotak CH, Fisher M (2000) Temporal evolution of ischemic injury evaluated with diffusion-, perfusion-, and T2-weighted MRI. Neurology 54: 689-696.
30. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397.
31. Abo-Ramadan U, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, et al. (2009) Post-ischemic leakiness of the blood-brain barrier: A quantitative and systematic assessment by Patlak plots. Exp Neurol: ( in press).
32. Olah L, Wecker S, Hoehn M (2000) Secondary deterioration of apparent diffusion coefficient after 1-hour transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 20: 1474-1482.
33. Wu O, Koroshetz WJ, Ostergaard L, Buonanno FS, Copen WA, et al. (2001) Predicting tissue outcome in acute human cerebral ischemia using combined diffusion- and perfusion-weighted MR imaging. Stroke 32: 933-942.
34. Hoehn-Berlage M, Norris DG, Kohno K, Mies G, Leibfritz D, et al. (1995) Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: the relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances. J Cereb Blood Flow Metab 15: 1002-1011.
35. Candelario-Jalil E, Taheri S, Yang Y, Sood R, Grossetete M, et al. (2007) Cyclooxygenase inhibition limits blood-brain barrier disruption following intracerebral injection of tumor necrosis factor-alpha in the rat. J Pharmacol Exp Ther 323: 488-498.
36. Patlak CS, Blasberg RG, Fenstermacher JD (1983) Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cereb Blood Flow Metab 3: 1-7.
37. R-Project (2007) The R Project for Statistical Computing. http://www.r-project.org.
38. McCullagh P, Nelder JA (1989) Generalized Linear Models: CRC Press.