The Ins and Outs of the BCCAo Model for Chronic Hypoperfusion: A Multimodal and Longitudinal MRI Approach

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Soria, Guadalupe ^a,b   Tudela, Raúl ^a,c   Márquez Martín, Ana ^d   Camón, Lluïsa ^b   Batalle, Dafnis ^a   Muñoz Moreno, Emma ^a   Eixarch, Elisenda ^a   Puig, Josep ^e   Pedraza, Salvador ^e   Vila, Elisabet ^d   Prats Galino, Alberto ^c   Planas, Anna M ^b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^e HOSPITAL JOSEP TRUETA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BASILAR ARTERY; BRAIN BLOOD FLOW; BRAIN DAMAGE; BRAIN INFARCTION; BRAIN NECROSIS; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; EXECUTIVE FUNCTION; GLIOSIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MYELINATED NERVE; NERVE DEGENERATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OPTIC TRACT; RAT; WHITE MATTER;

ANIMALS; ARTERIAL OCCLUSIVE DISEASES; BASILAR ARTERY; BEHAVIOR, ANIMAL; BRAIN; CAROTID ARTERY, COMMON; CHRONIC DISEASE; CONTRAST MEDIA; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; MULTIMODAL IMAGING; PERFUSION; RATS; RATS, WISTAR; TIME FACTORS; VISUAL PATHWAYS;

EID: 84884267135     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074631     Document Type: Article

References (60)

1. Kalaria RN, Akinyemi R, Ihara M, (2012) Does vascular pathology contribute to Alzheimer changes? J Neurol Sci 322: 141-147. doi:10.1016/j.jns.2012.07.032. PubMed: 22884479.
2. Moorhouse P, Rockwood K, (2008) Vascular cognitive impairment: current concepts and clinical developments. Lancet Neurol 7: 246-255. doi:10.1016/S1474-4422(08)70040-1. PubMed: 18275926.
3. Hainsworth AH, Brittain JF, Khatun H, (2012) Pre-clinical models of human cerebral small vessel disease: Utility for clinical application. J Neurol Sci 322: 237-240. doi:10.1016/j.jns.2012.05.046. PubMed: 22698483.
4. Okamoto Y, Yamamoto T, Kalaria RN, Senzaki H, Maki T, et al. (2012) Cerebral hypoperfusion accelerates cerebral amyloid angiopathy and promotes cortical microinfarcts. Acta Neuropathol 123: 381-394. doi:10.1007/s00401-011-0925-9. PubMed: 22170742.
5. Pimentel-Coelho PM, Michaud JP, Rivest S, (2013) Effects of mild chronic cerebral hypoperfusion and early amyloid pathology on spatial learning and the cellular innate immune response in mice. Neurobiol Aging 34: 679-693. doi:10.1016/j.neurobiolaging.2012.06.025. PubMed: 22819135.
6. Farkas E, Luiten PG, Bari F, (2007) Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain. Res Rev 54: 162-180. doi:10.1016/j.brainresrev.2007.01.003.
7. Kántor O, Schmitz C, Feiser J, Brasnjevic I, Korr H, et al. (2007) Moderate loss of cerebellar Purkinje cells after chronic bilateral common carotid artery occlusion in rats. Acta Neuropathol 113: 549-558. doi:10.1007/s00401-007-0204-y. PubMed: 17308915.
8. Hainsworth AH, Markus HS, (2008) Do in vivo experimental models reflect human cerebral small vessel disease? A systematic review. J Cereb Blood Flow Metab 28: 1877-1891. doi:10.1038/jcbfm.2008.91. PubMed: 18698331.
9. Jiwa NS, Garrard P, Hainsworth AH, (2010) Experimental models of vascular dementia and vascular cognitive impairment: a systematic review. J Neurochem 115: 814-828. doi:10.1111/j.1471-4159.2010.06958.x. PubMed: 20731763.
10. Schmidt-Kastner R, Aguirre-Chen C, Saul I, Yick L, Hamasaki D, et al. (2005) Astrocytes react to oligemia in the forebrain induced by chronic bilateral common carotid artery occlusion in rats. Brain Res 1052: 28-39. doi:10.1016/j.brainres.2005.06.018. PubMed: 16023090.
11. Busch HJ, Buschmann IR, Mies G, Bode C, Hossmann KA, (2003) Arteriogenesis in hypoperfused rat brain. J Cereb Blood Flow Metab 23: 621-628. PubMed: 12771578.
12. Choy M, Ganesan V, Thomas DL, Thornton JS, Proctor E, et al. (2006) The chronic vascular and haemodynamic response after permanent bilateral common carotid occlusion in newborn and adult rats. J Cereb Blood Flow Metab 26: 1066-1075. doi:10.1038/sj.jcbfm.9600259. PubMed: 16395291.
13. Yang YM, Feng X, Yao ZW, Tang WJ, Liu HQ, et al. (2008) Magnetic resonance angiography of carotid and cerebral arterial occlusion in rats using a clinical scanner. J Neurosci Methods 167: 176-183. doi:10.1016/j.jneumeth.2007.08.005. PubMed: 17889370.
14. Eixarch E, Batalle D, Illa M, Muñoz-Moreno E, Arbat-Plana A, et al. (2012) Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PLOS ONE 7: e31497. doi:10.1371/journal.pone.0031497. PubMed: 22347486.
15. Vercauteren T, Pennec X, Perchant A, Ayache N, (2009) Diffeomorphic demons: efficient non-parametric image registration. Neuroimage 45: S61-S72. doi:10.1016/j.neuroimage.2008.10.040. PubMed: 19041946.
16. Østergaard L, (2004) Cerebral perfusion imaging by bolus tracking. Top Magn Reson Imaging 15: 3-9. doi:10.1097/00002142-200402000-00002. PubMed: 15057169.
17. Castañé A, Theobald DE, Robbins TW, (2010) Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats. Behav Brain Res 210: 74-83. doi:10.1016/j.bbr.2010.02.017. PubMed: 20153781.
18. Boulougouris V, Castañé A, Robbins TW, (2009) Dopamine D2/D3 receptor agonist quinpirole impairs spatial reversal learning in rats: investigation of D3 receptor involvement in persistent behavior. Psychopharmacology (Berl) 202: 611-620. doi:10.1007/s00213-008-1341-2. PubMed: 18836703.
19. Floresco SB, Block AE, Tse MT, (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure Behav Brain Res 190: 85-96. doi:10.1016/j.bbr.2008.02.008. PubMed: 18359099.
20. Vivó M, Camón L, de Vera N, Martínez E, (2002) Lesion of substantia nigra pars compacta by the GluR5 agonist ATPA. Brain Res 955: 104-114. doi:10.1016/S0006-8993(02)03373-5. PubMed: 12419526.
21. Villalba N, Martínez P, Bríones AM, Sánchez A, Salaíces M, et al. (2009) Differential structural and functional changes in penile and coronary arteries from obese Zucker rats. Am J Physiol Heart Circ Physiol 297: 696-707. doi:10.1152/ajpheart.01308.2008. PubMed: 19542483.
22. Schambach SJ, Bag S, Steil V, Isaza C, Schilling L, et al. (2009). Ultrafast High-Resolution In Vivo Volume-CTA of Mice Cerebral Vessels. Stroke 40: 1444-1450. doi:10.1161/STROKEAHA.108.521740. PubMed: 19213951.
23. la Sala A, Pontecorvo L, Agresta A, Rosano G, Stabile E, (2012) Regulation of collateral blood vessel development by the innate and adaptive immune system. Trends Mol Med 18: 494-501. doi:10.1016/j.molmed.2012.06.007. PubMed: 22818027.
24. Mulvany MJ, (1999) Vascular remodelling of resistance vessels: can we define this? Cardiovasc Res 41: 9-13. doi:10.1016/S0008-6363(98)00289-2. PubMed: 10325946.
25. Lanari A, Silvestrelli G, (2012) Acute and chronic carotid occlusion syndromes. Front Neurol Neurosci 30: 185-190. doi:10.1159/000333639. PubMed: 22377892.
26. Pappas BA, de la Torre JC, Davidson CM, Keyes MT, Fortin T, (1996) Chronic reduction of cerebral blood flow in the adult rat: late-emerging CA1 cell loss and memory dysfunction. Brain Res 708: 50-58. doi:10.1016/0006-8993(95)01267-2. PubMed: 8720859.
27. Ohta H, Nishikawa H, Kimura H, Anayama H, Miyamoto M, (1997) Chronic cerebral hypoperfusion by permanent internal carotid ligation produces learning impairment without brain damage in rats. Neuroscience 79: 1039-1050. doi:10.1016/S0306-4522(97)00037-7. PubMed: 9219966.
28. Sarti C, Pantoni L, Bartolini L, Inzitari D, (2002) Persistent impairment of gait performances and working memory after bilateral common carotid artery occlusion in the adult Wistar rat. Behav Brain Res 136: 13-20. doi:10.1016/S0166-4328(02)00090-6. PubMed: 12385786.
29. Kitamura A, Fujita Y, Oishi N, Kalaria RN, Washida K, et al. (2012) Selective white matter abnormalities in a novel rat model of vascular dementia. Neurobiol Aging 331012:: 1012e-1012e.
30. Guarneri P, Guarneri R, La Bella V, Scondotto S, Scoppa F, et al. (1988) Lateral differences in GABA binding sites in rat brain. Neurochem Res 13: 209-211. doi:10.1007/BF00971534. PubMed: 2838763.
31. Schneider LH, Murphy RB, Coons EE, (1982) Lateralization of striatal dopamine (D2) receptors in normal rats. Neurosci Lett 33: 281-284. doi:10.1016/0304-3940(82)90385-8. PubMed: 7162690.
32. Gajendiran M, Ling GY, Pang Z, Xu ZC, (2001) Differential changes of synaptic transmission in spiny neurons of rat neostriatum following transient forebrain ischemia. Neuroscience 105: 139-152. doi:10.1016/S0306-4522(01)00163-4. PubMed: 11483308.
33. Wakita H, Tomimoto H, Akiguchi I, Kimura J, (1994) Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemical study. Acta Neuropathol 87: 484-492. doi:10.1007/BF00294175. PubMed: 8059601.
34. Kurumatani T, Kudo T, Ikura Y, Takeda M, (1998) White matter changes in the gerbil brain under chronic cerebral hypoperfusion. Stroke 29: 1058-1062. doi:10.1161/01.STR.29.5.1058. PubMed: 9596257.
35. Reimer MM, McQueen J, Searcy L, Scullion G, Zonta B, et al. (2011) Rapid disruption of axon-glial integrity in response to mild cerebral hypoperfusion. J Neurosci 31: 18185-18194. doi:10.1523/JNEUROSCI.4936-11.2011. PubMed: 22159130.
36. Ueno M, Tomimoto H, Akiguchi I, Wakita H, Sakamoto H, (2002) Blood-brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab 22: 97-104. PubMed: 11807399.
37. Farrall AJ, Wardlaw JM, (2009) Blood-brain barrier: Ageing and microvascular disease--systematic review and meta-analysis. Neurobiol Aging 30: 337-352. doi:10.1016/j.neurobiolaging.2007.07.015. PubMed: 17869382.
38. Wardlaw JM, Sandercock PA, Dennis MS, Starr J, (2003) Is breakdown of the blood-brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke 34: 806-812. doi:10.1161/01.STR.0000058480.77236.B3. PubMed: 12624314.
39. Pluta R, Januszewski S, Ułamek M, (2008) Ischemic blood-brain barrier and amyloid in white matter as etiological factors in leukoaraiosis. Acta Neurochir Suppl 102: 353-356. PubMed: 19388344.
40. Budde MD, Janes L, Gold E, Turtzo LC, Frank JA, (2011) The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 134: 2248-2260. doi:10.1093/brain/awr161. PubMed: 21764818.
41. Nitkunan A, Barrick TR, Charlton RA, Clark CA, Markus HS, (2008) Multimodal MRI in cerebral small vessel disease: its relationship with cognition and sensitivity to change over time. Stroke 39: 1999-2005. doi:10.1161/STROKEAHA.107.507475. PubMed: 18436880.
42. Shibata M, Yamasaki N, Miyakawa T, Kalaria RN, Fujita Y, et al. (2007) Selective impairment of working memory in a Mouse model of chronic cerebral hypoperfusion. Stroke 38: 2826-2832. doi:10.1161/STROKEAHA.107.490151. PubMed: 17761909.
43. Plaschke K, Grant M, Weigand MA, Züchner J, Martin E, et al. (2001) Neuromodulatory effect of propentofylline on rat brain under acute and long-term hypoperfusion. Br J Pharmacol 133: 107-116. doi:10.1038/sj.bjp.0704061. PubMed: 11325800.
44. Chidlow G, Wood JP, Sarvestani G, Manavis J, Casson RJ, (2009) Evaluation of Fluoro-Jade C as a marker of degenerating neurons in the rat retina and optic nerve. Exp Eye Res 88: 426-437. doi:10.1016/j.exer.2008.10.015. PubMed: 19010324.
45. Kalesnykas G, Tuulos T, Uusitalo H, Jolkkonen J, (2008) Neurodegeneration and cellular stress in the retina and optic nerve in rat cerebral ischemia and hypoperfusion models. Neuroscience 155: 937-947. doi:10.1016/j.neuroscience.2008.06.038. PubMed: 18640247.
46. Yamamoto H, Schmidt-Kastner R, Hamasaki DI, Yamamoto H, Parel JM, (2006) Complex neurodegeneration in retina following moderate ischemia induced by bilateral common carotid artery occlusion in Wistar rats. Exp Eye Res 82: 767-779. doi:10.1016/j.exer.2005.09.019. PubMed: 16359664.
47. Morrison JC, Johnson EC, Cepurna WO, Funk RH, (1999) Microvasculature of the rat optic nerve head. Invest Ophthalmol Vis Sci 40: 1702-1709. PubMed: 10393039.
48. Cox NH, Dorenbos J, (1974) The blood supply of the rat palate. J Anat 118: 507-510. PubMed: 4452650.
49. Lai SL, Chen YC, Weng HH, Chen ST, Hsu SP, et al. (2005) Bilateral common carotid artery occlusion--a case report and literature review. J Neurol Sci 238: 101-104. doi:10.1016/S0022-510X(05)80378-8. PubMed: 16111704.
50. Guo L, Duggan J, Cordeiro MF, (2010) Alzheimer's disease and retinal neurodegeneration. Curr Alzheimer Res 7: 3-14. doi:10.2174/156720510790274491. PubMed: 20205667.
51. Choi BR, Kwon KJ, Park SH, Jeon WK, Han SH, et al. (2011) Alternations of Septal-hippocampal System in the Adult Wistar Rat with Spatial Memory Impairments Induced by Chronic Cerebral Hypoperfusion. Exp Neurobiol: 20: 92-99.
52. Farkas E, Luiten PG, (2001) Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol 64: 575-611. doi:10.1016/S0301-0082(00)00068-X. PubMed: 11311463.
53. Liu HX, Zhang JJ, Zheng P, Zhang Y, (2005) Altered expression of MAP-2, GAP-43, and synaptophysin in the hippocampus of rats with chronic cerebral hypoperfusion correlates with cognitive impairment. Brain Res Mol Brain Res 139: 169-177. doi:10.1016/j.molbrainres.2005.05.014. PubMed: 15964096.
54. Otori T, Katsumata T, Muramatsu H, Kashiwagi F, Katayama Y, et al. (2003) Long-term measurement of cerebral blood flow and metabolism in a rat chronic hypoperfusion model. Clin Exp Pharmacol Physiol 30: 266-272. doi:10.1046/j.1440-1681.2003.03825.x. PubMed: 12680845.
55. Márquez-Martín A, Jiménez-Altayó F, Dantas AP, Caracuel L, Planas AM, et al. (2012) Middle cerebral artery alterations in a rat chronic hypoperfusion model. J Appl Physiol 112: 511-518. doi:10.1152/japplphysiol.00998.2011. PubMed: 22096118.
56. Hoefer IE, van Royen N, Rectenwald JE, Deindl E, Hua J, et al. (2004) Arteriogenesis proceeds via ICAM-1/Mac-1- mediated mechanisms. Circ Res 94: 1179-1185. doi:10.1161/01.RES.0000126922.18222.F0. PubMed: 15059933.
57. Demicheva E, Hecker M, Korff T, (2008) Stretch-induced activation of the transcription factor activator protein-1 controls monocyte chemoattractant protein-1 expression during arteriogenesis. Circ Res 103: 477-484. doi:10.1161/CIRCRESAHA.108.177782. PubMed: 18669921.
58. Duelsner A, Gatzke N, Glaser J, Hillmeister P, Li M, et al. (2012) Acetylsalicylic acid, but not clopidogrel, inhibits therapeutically induced cerebral arteriogenesis in the hypoperfused rat brain. J Cereb Blood Flow Metab 32: 105-114. doi:10.1038/jcbfm.2011.113. PubMed: 21829214.
59. Bergmann CE, Hoefer IE, Meder B, Roth H, van Royen N, et al. (2006) Arteriogenesis depends on circulating monocytes and macrophage accumulation and is severely depressed in op/op mice. J Leukoc Biol 80: 59-65. doi:10.1189/jlb.0206087. PubMed: 16684892.
60. Eitenmüller I, Volger O, Kluge A, Troidl K, Barancik M, et al. (2006) The range of adaptation by collateral vessels after femoral artery occlusion. Circ Res 99: 656-662. doi:10.1161/01.RES.0000242560.77512.dd. PubMed: 16931799.