Longitudinal assessment of blood-brain barrier leakage during epileptogenesis in rats. A quantitative MRI study

Neurobiology of Disease

Volumn 63, Issue , 2014, Pages 74-84

  van Vliet, E A ^a,b   Otte, W M ^c,d   Gorter, J A ^a,b   Dijkhuizen, R M ^c   Wadman, W J ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Blood brain barrier; Fluorescein; Gadolinium; Magnetic resonance imaging; Status epilepticus; Temporal lobe epilepsy

Indexed keywords

GADOBUTROL;

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER LEAKAGE; BRAIN DISEASE; BRAIN MAPPING; BRAIN RADIOGRAPHY; BRAIN REGION; CONTROLLED STUDY; ENTORHINAL CORTEX; EPILEPTIC STATE; EPILEPTOGENESIS; HIPPOCAMPUS; LONGITUDINAL STUDY; MALE; MICROSCOPY; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PYRIFORM CORTEX; QUANTITATIVE ANALYSIS; RAT; SENSITIVITY AND SPECIFICITY; STEADY STATE;

BBB; BLOOD-BRAIN BARRIER; FLUORESCEIN; FSC; GADOLINIUM; KA; KAINIC ACID; MAGNETIC RESONANCE IMAGING; SE; STATUS EPILEPTICUS; TEMPORAL LOBE EPILEPSY;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CAPILLARY PERMEABILITY; CONTRAST MEDIA; DISEASE MODELS, ANIMAL; IMAGE PROCESSING, COMPUTER-ASSISTED; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; ORGANOMETALLIC COMPOUNDS; RATS; RATS, SPRAGUE-DAWLEY; STATISTICS, NONPARAMETRIC; STATUS EPILEPTICUS; TIME FACTORS;

EID: 84890834335     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.11.019     Document Type: Article

References (42)

1. Abbott N.J., et al. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37:13-25.
2. Bouilleret V., et al. Mapping of the progressive metabolic changes occurring during the development of hippocampal sclerosis in a model of mesial temporal lobe epilepsy. Brain Res. 2000, 852:255-262.
3. Carlin B.P., et al. Hierarchical Bayesian analysis of changepoint problems. Appl. Stat. 1992, 41:389-405.
4. Chassidim Y., et al. Quantitative imaging assessment of blood-brain barrier permeability in humans. Fluids Barriers CNS 2013, 10:9.
5. Dijkhuizen R.M. Advances in MRI-based detection of cerebrovascular changes after experimental traumatic brain injury. Transl. Stroke Res. 2011, 2:524-532.
6. Friedman A. Blood-brain barrier dysfunction, status epilepticus, seizures, and epilepsy: a puzzle of a chicken and egg?. Epilepsia 2011, 52(Suppl. 8):19-20.
7. Kassner A., Thornhill R. Measuring the integrity of the human blood-brain barrier using magnetic resonance imaging. Methods Mol. Biol. 2011, 686:229-245.
8. Knight R.A., et al. Estimating blood and brain concentrations and blood-to-brain influx by magnetic resonance imaging with step-down infusion of Gd-DTPA in focal transient cerebral ischemia and confirmation by quantitative autoradiography with Gd-[(14)C]DTPA. J. Cereb. Blood Flow Metab. 2009, 29:1048-1058.
9. Korn A., et al. Focal cortical dysfunction and blood-brain barrier disruption in patients with postconcussion syndrome. J. Clin. Neurophysiol. 2005, 22:1-9.
10. Leroy C., et al. In the lithium-pilocarpine model of epilepsy, brain lesions are not linked to changes in blood-brain barrier permeability: an autoradiographic study in adult and developing rats. Exp. Neurol. 2003, 182:361-372.
11. Liu J.Y., et al. Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy. Brain 2012, 135:3115-3133.
12. Marchi N., et al. The etiological role of blood-brain barrier dysfunction in seizure disorders. Cardiovasc. Psychiatry Neurol. 2011, 2011:482415.
13. Marchi N., et al. Blood-brain barrier dysfunction and epilepsy: pathophysiologic role and therapeutic approaches. Epilepsia 2012, 53:1877-1886.
14. Mihaly A., Bozoky B. Immunohistochemical localization of extravasated serum albumin in the hippocampus of human subjects with partial and generalized epilepsies and epileptiform convulsions. Acta Neuropathol. (Berl.) 1984, 65:25-34.
15. Nagaraja T.N., et al. Step-down infusions of Gd-DTPA yield greater contrast-enhanced magnetic resonance images of BBB damage in acute stroke than bolus injections. Magn. Reson. Imaging 2007, 25:311-318.
16. Nagaraja T.N., et al. Multiparametric magnetic resonance imaging and repeated measurements of blood-brain barrier permeability to contrast agents. Methods Mol. Biol. 2011, 686:193-212.
17. Nitsch C., Klatzo I. Regional patterns of blood-brain barrier breakdown during epileptiform seizures induced by various convulsive agents. J. Neurol. Sci. 1983, 59:305-322.
18. Oby E., Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006, 47:1761-1774.
19. Otte W.M., et al. Focal neocortical epilepsy affects hippocampal volume, shape, and structural integrity: a longitudinal MRI and immunohistochemistry study in a rat model. Epilepsia 2012, 53:1264-1273.
20. Pavlovsky L., et al. Persistent BBB disruption may underlie alpha interferon-induced seizures. J. Neurol. 2005, 252:42-46.
21. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego 1998.
22. Pont F., et al. Early and transient increase of rat hippocampal blood-brain barrier permeability to amino acids during kainic acid-induced seizures. Neurosci. Lett. 1995, 184:52-54.
23. Raabe A., et al. Cliniconeuropathologic correlations show astroglial albumin storage as a common factor in epileptogenic vascular lesions. Epilepsia 2012, 53:539-548.
24. Ravizza T., et al. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol. Dis. 2008, 29:142-160.
25. Rigau V., et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007, 130:1942-1956.
26. Roch C., et al. Magnetic resonance imaging in the study of the lithium-pilocarpine model of temporal lobe epilepsy in adult rats. Epilepsia 2002, 43:325-335.
27. Ruth R.E. Increased cerebrovascular permeability to protein during systemic kainic acid seizures. Epilepsia 1984, 25:259-268.
28. Saija A., et al. Blood-brain barrier dysfunctions following systemic injection of kainic acid in the rat. Life Sci. 1992, 51:467-477.
29. Schmitz A.K., et al. Albumin storage in neoplastic astroglial elements of gangliogliomas. Seizure 2013, 22:144-150.
30. Seiffert E., et al. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J. Neurosci. 2004, 24:7829-7836.
31. Stanimirovic D.B., Friedman A. Pathophysiology of the neurovascular unit: disease cause or consequence?. J. Cereb. Blood Flow Metab. 2012, 32:1207-1221.
32. Tomkins O., et al. Frequent blood-brain barrier disruption in the human cerebral cortex. Cell. Mol. Neurobiol. 2001, 21:675-691.
33. Tomkins O., et al. Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiol. Dis. 2007, 25:367-377.
34. van Meer M.P., et al. Extent of bilateral neuronal network reorganization and functional recovery in relation to stroke severity. J. Neurosci. 2012, 32:4495-4507.
35. Van Vliet E.A., et al. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007, 130:521-534.
36. van Vliet E.A., et al. Region specific overexpression of P-glycoprotein at the blood-brain barrier affects brain uptake of phenytoin in epileptic rats. J. Pharmacol. Exp. Ther. 2007, 322:141-147.
37. van Vliet E.A., et al. COX-2 inhibition controls P-glycoprotein expression and promotes brain delivery of phenytoin in chronic epileptic rats. Neuropharmacology 2010, 58:404-412.
38. van Vliet E.A., et al. Atorvastatin treatment during epileptogenesis in a rat model for temporal lobe epilepsy. Epilepsia 2011, 52:1319-1330.
39. van Vliet E.A., et al. Inhibition of mammalian target of rapamycin reduces epileptogenesis and blood-brain barrier leakage but not microglia activation. Epilepsia 2012, 53:1254-1263.
40. Vezzani A., Friedman A. Brain inflammation as a biomarker in epilepsy. Biomark. Med 2011, 5:607-614.
41. Vezzani A., et al. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7:31-40.
42. Zucker D.K., et al. Blood-brain barrier changes with kainic acid-induced limbic seizures. Exp. Neurol. 1983, 79:422-433.