Animal models of spontaneous intracerebral hemorrhage

Neurological Research

Volumn 38, Issue 5, 2016, Pages 448-455

  Alharbi, Bader Murshed ^a,b   Tso, Michael K ^a,b   Macdonald, R Loch ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Animal model; Cerebral amyloid angiopathy; Hypertension; Intracerebral hemorrhage; Spontaneous

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ANGIOTENSIN II; ANGIOTENSINOGEN; DIPYRIDAMOLE; HEMOSIDERIN; NITRIC OXIDE SYNTHASE; RENIN;

AGE; ALCOHOL CONSUMPTION; AMYLOID PLAQUE; ANIMAL MODEL; ANTICOAGULATION; ANXIETY; ASIAN; BRAIN BLOOD VESSEL; BRAIN HEMORRHAGE; CELL LOSS; CONGOPHILIC ANGIOPATHY; DEMENTIA; DIABETES MELLITUS; DISEASE MODEL; DISEASE SEVERITY; FAMILIAL DANISH DEMENTIA; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HYPERTENSION; IMAGING; MENOPAUSE; MORRIS WATER MAZE TEST; MOUSE MODEL; MUTATION; NERVOUS SYSTEM INFLAMMATION; NEUROFIBRILLARY TANGLE; NONHUMAN; OBESITY; OPEN FIELD TEST; REVIEW; RISK FACTOR; SMOKING; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CEREBRAL HEMORRHAGE; COMPLICATION; GENETICS; VASCULAR AMYLOIDOSIS;

ANIMALS; CEREBRAL AMYLOID ANGIOPATHY; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; HUMANS; HYPERTENSION; MICE, TRANSGENIC; RISK FACTORS;

EID: 84978380205     PISSN: 01616412     EISSN: 17431328     Source Type: Journal    
DOI: 10.1080/01616412.2016.1144671     Document Type: Review

References (61)

1. Heart and Stroke Foundation of Canada. The growing burden of heart disease and stroke in Canada 2003; 2003. Accessed 18 May 2015 http://www.cvdinfobase.ca/cvdbook/CVD_En03.pdf
2. D.Woo, J.P.Broderick. Spontaneous intracerebral hemorrhage: epidemiology and clinical presentation. Neurosurg Clin N Am. 2002;13(3):265–79.10.1016/S1042-3680(02)00011-6
3. C.J.van Asch, M.J.Luitse, G.J.Rinkel, I.van dT, A.Algra, C.J.Klijn. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9(2):167–76.
4. J.P.Broderick, T.Brott, T.Tomsick, R.Miller, G.Huster. Intracerebral hemorrhage more than twice as common as subarachnoid hemorrhage. J Neurosurg. 1993;78(2):188–91.10.3171/jns.1993.78.2.0188
5. J.Broderick, S.Connolly, E.Feldmann, D.Hanley, C.Kase, D.Krieger,. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Stroke. 2007;38(6):2001–23.10.1161/STROKEAHA.107.183689
6. R.N.Auer, G.R.Sutherland. Primary intracerebral hemorrhage: pathophysiology. Can J Neurol Sci. 2005;32(Suppl. 2):S3–12.
7. A.I.Qureshi, A.D.Mendelow, D.F.Hanley. Intracerebral haemorrhage. Lancet. 2009;373:1632–44.10.1016/S0140-6736(09)60371-8
8. M.I.Aguilar, W.D.Freeman. Spontaneous intracerebral hemorrhage. Semin Neurol. 2010;30(5):555–64.10.1055/s-0030-1268865
9. G.Xi, R.F.Keep, J.T.Hoff. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5(1):53–63.10.1016/S1474-4422(05)70283-0
10. Q.T.Wang, S.Tuhrim. Etiologies of intracerebral hematomas. Curr Atheroscler Rep. 2012;14(4):314–21.10.1007/s11883-012-0253-0
11. M.L.Flaherty. Anticoagulant-associated intracerebral hemorrhage. Semin Neurol. 2010;30(5):565–572.10.1055/s-0030-1268866
12. S.J.Connolly, M.D.Ezekowitz, S.Yusuf, J.Eikelboom, J.Oldgren, A.Parekh, Dabigatran versus warfarin in patients with atrial fibrillation. N Engl J Med. 2009;361(12):1139–51.
13. R.G.Hart, B.S.Boop, D.C.Anderson. Oral anticoagulants and intracranial hemorrhage. Facts and hypotheses. Stroke. 1995;26(8):1471–7.
14. R.G.Hart, S.B.Tonarelli, L.A.Pearce. Avoiding central nervous system bleeding during antithrombotic therapy: recent data and ideas. Stroke. 2005;36(7):1588–93.10.1161/01.STR.0000170642.39876.f2
15. F.Dentali, J.D.Douketis, W.Lim, M.Crowther. Combined aspirin-oral anticoagulant therapy compared with oral anticoagulant therapy alone among patients at risk for cardiovascular disease: a meta-analysis of randomized trials. Arch Intern Med. 2007;167(2):117–24.10.1001/archinte.167.2.117
16. G.C.Flaker, M.Gruber, S.J.Connolly, S.Goldman, S.Chaparro, A.Vahanian,. Risks and benefits of combining aspirin with anticoagulant therapy in patients with atrial fibrillation: an exploratory analysis of stroke prevention using an oral thrombin inhibitor in atrial fibrillation (SPORTIF) trials. Am Heart J. 2006;152(5):967–73.10.1016/j.ahj.2006.06.024
17. R.G.Hart, O.Benavente, L.A.Pearce. Increased risk of intracranial hemorrhage when aspirin is combined with warfarin: a meta-analysis and hypothesis. Cerebrovasc Dis. 1999;9(4):215–7.10.1159/000015958
18. A.Lauer, S.M.Greenberg, M.E.Gurol. Statins in intracerebral hemorrhage. Curr Atheroscler Rep. 2015;17(8):526.
19. S.Akoudad, N.Aarts, R.Noordam, M.A.Ikram, H.Tiemeier, A.Hofman,. Antidepressant use is associated with an increased risk of developing microbleeds. Stroke. 2016;47(1):251–4.10.1161/STROKEAHA.115.011574
20. M.J.Ariesen, S.P.Claus, G.J.Rinkel, A.Algra. Risk factors for intracerebral hemorrhage in the general population: a systematic review. Stroke. 2003;34(8):2060–5.10.1161/01.STR.0000080678.09344.8D
21. E.Feldmann, J.P.Broderick, W.N.Kernan, C.M.Viscoli, L.M.Brass, T.Brott,. Major risk factors for intracerebral hemorrhage in the young are modifiable. Stroke. 2005;36(9):1881–5.10.1161/01.STR.0000177480.62341.6b
22. E.Zia, B.Hedblad, H.Pessah-Rasmussen, G.Berglund, L.Janzon, G.Engstrom. Blood pressure in relation to the incidence of cerebral infarction and intracerebral hemorrhage: hypertensive hemorrhage: debated nomenclature is still relevant. Stroke. 2007;38(10):2681–5.10.1161/STROKEAHA.106.479725
23. N.Nago, S.Ishikawa, T.Goto, K.Kayaba. Low cholesterol is associated with mortality from stroke, heart disease, and cancer: the Jichi Medical School Cohort Study. J Epidemiol. 2011;21(1):67–74.10.2188/jea.JE20100065
24. D.L.Tirschwell, N.L.Smith, S.R.Heckbert, R.N.Lemaitre, W.T.LongstrethJr, B.M.Psaty. Association of cholesterol with stroke risk varies in stroke subtypes and patient subgroups. Neurology. 2004;63(10):1868–75.10.1212/01.WNL.0000144282.42222.DA
25. C.Garcia, T.Pinho e Melo, L.Rocha, M.C.Lechner. Cerebral hemorrhage and apoE. J Neurol. 1999;246(9):830–4.
26. D.F.Hanley. Intraventricular hemorrhage. Severity factor and treatment target in spontaneous intracerebral hemorrhage. Stroke. 2009;40:1533–1538.
27. A.D.Mendelow, B.A.Gregson, E.N.Rowan, G.D.Murray, A.Gholkar, P.M.Mitchell. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet. 2013;382(9890):397–408.
28. C.Cordonnier, S.R.Al-Shahi, J.Wardlaw. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain. 2007;130(8):1988–2003.10.1093/brain/awl387
29. C.Cordonnier, W.M.van der Flier. Brain microbleeds and Alzheimer’s disease: innocent observation or key player? Brain. 2011;134(2):335–44.10.1093/brain/awq321
30. D.J.Werring, S.M.Gregoire, L.Cipolotti. Cerebral microbleeds and vascular cognitive impairment. J Neurol Sci. 2010;299(1–2):131–5.10.1016/j.jns.2010.08.034
31. M.W.Vernooij, A.van der Lugt, M.A.Ikram, P.A.Wielopolski, W.J.Niessen, A.Hofman,. Prevalence and risk factors of cerebral microbleeds: the Rotterdam scan study. Neurology. 2008;70(14):1208–14.10.1212/01.wnl.0000307750.41970.d9
32. S.H.Lee, W.S.Ryu, J.K.Roh. Cerebral microbleeds are a risk factor for warfarin-related intracerebral hemorrhage. Neurology. 2009;72(2):171–6.10.1212/01.wnl.0000339060.11702.dd
33. C.L.MacLellan, G.Silasi, C.C.Poon, C.L.Edmundson, R.Buist, J.Peeling,. Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J Cereb Blood Flow Metab. 2008;28(3):516–25.10.1038/sj.jcbfm.9600548
34. S.Iida, G.L.Baumbach, J.L.Lavoie, F.M.Faraci, C.D.Sigmund, D.D.Heistad. Spontaneous stroke in a genetic model of hypertension in mice. Stroke. 2005;36(6):1253–8.10.1161/01.str.0000167694.58419.a2
35. Y.Wakisaka, Y.Chu, J.D.Miller, G.A.Rosenberg, D.D.Heistad. Spontaneous intracerebral hemorrhage during acute and chronic hypertension in mice. J Cereb Blood Flow Metab. 2010;30(1):56–69.10.1038/jcbfm.2009.183
36. D.C.Merrill, M.W.Thompson, C.L.Carney, B.P.Granwehr, G.Schlager, J.E.Robillard,. Chronic hypertension and altered baroreflex responses in transgenic mice containing the human renin and human angiotensinogen genes. J Clin Invest. 1996;97(4):1047–55.10.1172/JCI118497
37. J.S.Smeda. Hemorrhagic stroke development in spontaneously hypertensive rats fed a North American, Japanese-style diet. Stroke. 1989;20(9):1212–8.
38. S.Ahmad. Angiotensin receptor antagonists delay nitric oxide-deficient stroke in stroke- prone rats. Eur J Pharmacol. 1997;333(1):39–45.10.1016/S0014-2999(97)01089-3
39. Y.Wakisaka, J.D.Miller, Y.Chu, G.L.Baumbach, S.Wilson, F.M.Faraci,. Oxidative stress through activation of NAD(P)H oxidase in hypertensive mice with spontaneous intracranial hemorrhage. J Cereb Blood Flow Metab. 2008;28(6):1175–85.10.1038/jcbfm.2008.7
40. Y.Wakisaka, Y.Chu, J.D.Miller, G.A.Rosenberg, D.D.Heistad. Critical role for copper/zinc-superoxide dismutase in preventing spontaneous intracerebral hemorrhage during acute and chronic hypertension in mice. Stroke. 2010;41(4):790–7.10.1161/STROKEAHA.109.569616
41. C.Exley, M.M.Esiri. Severe cerebral congophilic angiopathy coincident with increased brain aluminium in a resident of Camelford, Cornwall, UK. J Neurol Neurosurg Psychiatry. 2006;77(7):877–9.10.1136/jnnp.2005.086553
42. T.Revesz, J.L.Holton, T.Lashley, G.Plant, A.Rostagno, J.Ghiso,. Sporadic and familial cerebral amyloid angiopathies. Brain Pathol. 2002;12(3):343–57.
43. K.A.Knudsen, J.Rosand, D.Karluk, S.M.Greenberg. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology. 2001;56(4):537–9.10.1212/WNL.56.4.537
44. K.A.Jellinger. Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm. 2002;109(5–6):813–36.10.1007/s007020200068
45. A.Biffi, S.M.Greenberg. Cerebral amyloid angiopathy: a systematic review. J Clin Neurol. 2011;7(1):1–9.10.3988/jcn.2011.7.1.1
46. J.Rosand, A.Muzikansky, A.Kumar, J.J.Wisco, E.E.Smith, R.A.Betensky,. Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy. Ann Neurol. 2005;58(3):459–62.10.1002/(ISSN)1531-8249
47. H.V.Vinters. Cerebral amyloid angiopathy. A critical review. Stroke. 1987;18(2):311–24.
48. H.A.Elfenbein, R.F.Rosen, S.L.Stephens, R.C.Switzer, Y.Smith, J.Pare,. Cerebral beta-amyloid angiopathy in aged squirrel monkeys. Histol Histopathol. 2007;22(2):155–67.
49. D.T.Winkler, L.Bondolfi, M.C.Herzig, L.Jann, M.E.Calhoun, K.H.Wiederhold,. Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci. 2001;21(5):1619–27.
50. J.Davis, F.Xu, R.Deane, G.Romanov, M.L.Previti, K.Zeigler,. Early-onset and robust cerebral microvascular accumulation of amyloid β-protein in transgenic mice expressing low levels of a vasculotropic dutch/iowa mutant form of amyloid β-protein precursor. J Biol Chem. 2004;279(19):20296–306.10.1074/jbc.M312946200
51. M.C.Herzig, D.T.Winkler, P.Burgermeister, M.Pfeifer, E.Kohler, S.D.Schmidt,. Aβ is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat Neurosci. 2004;7(9):954–60.10.1038/nn1302
52. J.Coomaraswamy, E.Kilger, H.Wolfing, C.Schafer, S.A.Kaeser, B.M.Wegenast-Braun,. Modeling familial Danish dementia in mice supports the concept of the amyloid hypothesis of Alzheimer’s disease. Proc Natl Acad Sci USA. 2010;107(17):7969–74.10.1073/pnas.1001056107
53. M.Fisher, V.Vasilevko, G.F.Passos, C.Ventura, D.Quiring, D.H.Cribbs. Therapeutic modulation of cerebral microhemorrhage in a mouse model of cerebral amyloid angiopathy. Stroke. 2011;42(11):3300–03.10.1161/STROKEAHA.111.626655
54. A.V.Braunmuhl. Senile vascular necrosis. Arch Psychiatr Nervenkr Z Gesamte Neurol Psychiatr. 1950;185(5):571–83.10.1007/BF00341626
55. L.C.Walker. Animal models of cerebral β-amyloid angiopathy. Brain Res Brain Res Rev. 1997;25(1):70–84.10.1016/S0165-0173(97)00017-9
56. A.Bilkei-Gorzo. Genetic mouse models of brain ageing and Alzheimer’s disease. Pharmacol Ther. 2014;142(2):244–57.10.1016/j.pharmthera.2013.12.009
57. C.Sturchler-Pierrat, D.Abramowski, M.Duke, K.H.Wiederhold, C.Mistl, S.Rothacher,. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA. 1997;94(24):13287–92.10.1073/pnas.94.24.13287
58. B.H.Han, M.L.Zhou, A.W.Johnson, I.Singh, F.Liao, A.K.Vellimana,. Contribution of reactive oxygen species to cerebral amyloid angiopathy, vasomotor dysfunction, and microhemorrhage in aged Tg2576 mice. Proc Natl Acad Sci USA. 2015;112(8):E881–90.10.1073/pnas.1414930112
59. P.Toth, S.Tarantini, Z.Springo, Z.Tucsek, T.Gautam, C.B.Giles,. Aging exacerbates hypertension-induced cerebral microhemorrhages in mice: role of resveratrol treatment in vasoprotection. Aging Cell. 2015;14(3):400–8.10.1111/acel.2015.14.issue-3
60. J.Yang, Y.Ji, P.Mehta, K.A.Bates, Y.Sun, T.Wisniewski. Blocking the apolipoprotein E/amyloid-beta interaction reduces fibrillar vascular amyloid deposition and cerebral microhemorrhages in TgSwDI mice. J Alzheimers Dis. 2011;24(2):269–85.
61. S.Rasool, R.AlbayIII, H.Martinez-Coria, L.Breydo, J.Wu, S.Milton,. Vaccination with a non-human random sequence amyloid oligomer mimic results in improved cognitive function and reduced plaque deposition and micro hemorrhage in Tg2576 mice. Mol Neurodegener. 2012;7:37.10.1186/1750-1326-7-37