Cardiovascular risk factors affect hippocampal microvasculature in early AD

[1] Evans DA, Funkenstein HH, Albert MS, Scherr PA, Cook NR, et al. (1989) Prevalence of Alzheimer’s disease in a community population of older persons. Higher than previously reported. J Am Med Assoc 262: 2551–2556. http://dx.doi.org/10.1001/jama.262.18.255110.1001/jama.262.18.2551Search in Google Scholar

[2] Rapaport E (1993) Secondary prevention of cardiovascular disease. Am J Geriatr Cardiol 2: 42–47. Search in Google Scholar

[3] Fair JM (2003) Cardiovascular risk factor modification: is it effective in older adults? J Cardiovasc Nurs 18: 161–168. 10.1097/00005082-200307000-00002Search in Google Scholar PubMed

[4] Hardy J (2006) A hundred years of Alzheimer’s disease research. Neuron 52: 3–13. http://dx.doi.org/10.1016/j.neuron.2006.09.01610.1016/j.neuron.2006.09.016Search in Google Scholar PubMed

[5] Schonheit B, Zarski R, Ohm TG (2004) Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging 25: 697–711. http://dx.doi.org/10.1016/j.neurobiolaging.2003.09.00910.1016/j.neurobiolaging.2003.09.009Search in Google Scholar PubMed

[6] Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112: 389–404. http://dx.doi.org/10.1007/s00401-006-0127-z10.1007/s00401-006-0127-zSearch in Google Scholar PubMed PubMed Central

[7] Buée L, Hof PR, Delacourte A (1997) Brain microvascular changes in Alzheimer’s disease and other dementias. Ann N Y Acad Sci 826: 7–24. http://dx.doi.org/10.1111/j.1749-6632.1997.tb48457.x10.1111/j.1749-6632.1997.tb48457.xSearch in Google Scholar PubMed

[8] Giannakopoulos P, Gold G, Kovari E, von Gunten A, Imhof A, et al. (2007) Assessing the cognitive impact of Alzheimer disease pathology and vascular burden in the aging brain: the Geneva experience. Acta Neuropathol 113: 1–12. http://dx.doi.org/10.1007/s00401-006-0144-y10.1007/s00401-006-0144-ySearch in Google Scholar PubMed

[9] Dannenberg AL, Garrison RJ, Kannel WB (1988) Incidence of hypertension in the Framingham Study. Am J Public Health 78: 676–679. http://dx.doi.org/10.2105/AJPH.78.6.67610.2105/AJPH.78.6.676Search in Google Scholar PubMed PubMed Central

[10] Skoog I, Gustafson D (2006) Update on hypertension and Alzheimer’s disease. Neurol Res 28: 605–611. http://dx.doi.org/10.1179/016164106X13050610.1179/016164106X130506Search in Google Scholar PubMed

[11] Kaplan NM (2002) Clinical Hypertension. Philadelphia: Lippincott Williams & Wilkins. 560 p. Search in Google Scholar

[12] Skoog I, Gustafson D (2003) Hypertension, hypertension-clustering factors and Alzheimer’s disease. Neurol Res 25: 675–680. http://dx.doi.org/10.1179/01616410310120198610.1179/016164103101201986Search in Google Scholar PubMed

[13] Dickstein DL, Walsh J, Brautigam H, Stockton SD, Jr., Gandy S, et al. (2010) Role of vascular risk factors and vascular dysfunction in Alzheimer’s disease. Mt Sinai J Med 77: 82–102. http://dx.doi.org/10.1002/msj.2015510.1002/msj.20155Search in Google Scholar

[14] Duron E, Hanon O (2008) Vascular risk factors, cognitive decline, and dementia. Vasc Health Risk Manag 4: 363–381. 10.2147/VHRM.S1839Search in Google Scholar

[15] Lin Y, Sun Z (2010) Current views on type 2 diabetes. J Endocrinol 204: 1–11. http://dx.doi.org/10.1677/JOE-09-026010.1677/JOE-09-0260Search in Google Scholar

[16] Silvestre JS, Levy BI (2006) Molecular basis of angiopathy in diabetes mellitus. Circ Res 98: 4–6. http://dx.doi.org/10.1161/01.RES.0000200396.90220.4110.1161/01.RES.0000200396.90220.41Search in Google Scholar

[17] Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP (2005) The effects of type 1 diabetes on cognitive performance: a metaanalysis. Diabetes Care 28: 726–735. http://dx.doi.org/10.2337/diacare.28.3.72610.2337/diacare.28.3.726Search in Google Scholar

[18] Allen KV, Frier BM, Strachan MW (2004) The relationship between type 2 diabetes and cognitive dysfunction: longitudinal studies and their methodological limitations. Eur J Pharmacol 490: 169–175. http://dx.doi.org/10.1016/j.ejphar.2004.02.05410.1016/j.ejphar.2004.02.054Search in Google Scholar

[19] Pasquier F, Boulogne A, Leys D, Fontaine P (2006) Diabetes mellitus and dementia. Diabetes Metab 32: 403–414. http://dx.doi.org/10.1016/S1262-3636(07)70298-710.1016/S1262-3636(07)70298-7Search in Google Scholar

[20] Dooneief G, Marder K, Tang MX, Stern Y (1996) The Clinical Dementia Rating scale: community-based validation of “profound” and “terminal” stages. Neurology 46: 1746–1749. 10.1212/WNL.46.6.1746Search in Google Scholar PubMed

[21] Heyman A, Wilkinson WE, Hurwitz BJ, Helms MJ, Haynes CS, et al. (1987) Early-onset Alzheimer’s disease: clinical predictors of institutionalization and death. Neurology 37: 980–984. 10.1212/WNL.37.6.980Search in Google Scholar

[22] Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, et al. (1991) The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41: 479–486. 10.1212/WNL.41.4.479Search in Google Scholar PubMed

[23] Zaccai J, Ince P, Brayne C (2006) Population-based neuropathological studies of dementia: design, methods and areas of investigation—a systematic review. BMC Neurol 6: 2. http://dx.doi.org/10.1186/1471-2377-6-210.1186/1471-2377-6-2Search in Google Scholar

[24] Fillenbaum GG, van Belle G, Morris JC, Mohs RC, Mirra SS, et al. (2008) Consortium to Establish a Registry for Alzheimer’s Disease (CERAD): the first twenty years. Alzheimers Dement 4: 96–109. http://dx.doi.org/10.1016/j.jalz.2007.08.00510.1016/j.jalz.2007.08.005Search in Google Scholar

[25] Shu SY, Ju G, Fan LZ (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85: 169–171. http://dx.doi.org/10.1016/0304-3940(88)90346-110.1016/0304-3940(88)90346-1Search in Google Scholar

[26] Calhoun ME, Mouton PR (2001) Length measurement: new developments in neurostereology and 3D imagery. J Chem Neuroanat 21: 257–265. http://dx.doi.org/10.1016/S0891-0618(01)00093-X10.1016/S0891-0618(01)00093-XSearch in Google Scholar

[27] Kreczmanski P, Schmidt-Kastner R, Heinsen H, Steinbusch HW, Hof PR, et al. (2005) Stereological studies of capillary length density in the frontal cortex of schizophrenics. Acta Neuropathol 109: 510–518. http://dx.doi.org/10.1007/s00401-005-1003-y10.1007/s00401-005-1003-ySearch in Google Scholar PubMed

[28] Mouton PR, Gokhale AM, Ward NL, West MJ (2002) Stereological length estimation using spherical probes. J Microsc 206: 54–64. http://dx.doi.org/10.1046/j.1365-2818.2002.01006.x10.1046/j.1365-2818.2002.01006.xSearch in Google Scholar PubMed

[29] Schmitz C, Hof PR (2005) Design-based stereology in neuroscience. Neuroscience 130: 813–831. http://dx.doi.org/10.1016/j.neuroscience.2004.08.05010.1016/j.neuroscience.2004.08.050Search in Google Scholar PubMed

[30] Brown WR, Moody DM, Thore CR, Anstrom JA, Challa VR (2009) Microvascular changes in the white mater in dementia. J Neurol Sci 283: 28–31. http://dx.doi.org/10.1016/j.jns.2009.02.32810.1016/j.jns.2009.02.328Search in Google Scholar PubMed PubMed Central

[31] van Dijk EJ, Prins ND, Vrooman HA, Hofman A, Koudstaal PJ, et al. (2008) Progression of cerebral small vessel disease in relation to risk factors and cognitive consequences: Rotterdam Scan study. Stroke 39: 2712–2719. http://dx.doi.org/10.1161/STROKEAHA.107.51317610.1161/STROKEAHA.107.513176Search in Google Scholar PubMed

[32] Bell MA, Ball MJ (1981) Morphometric comparison of hippocampal microvasculature in ageing and demented people: diameters and densities. Acta Neuropathol 53: 299–318. http://dx.doi.org/10.1007/BF0069037210.1007/BF00690372Search in Google Scholar PubMed

[33] Hassler O (1965) Vascular changes in senile brains. A microangiographic study. Acta Neuropathol 5: 40–53. http://dx.doi.org/10.1007/BF0068916110.1007/BF00689161Search in Google Scholar

[34] Buée L, Hof PR, Bouras C, Delacourte A, Perl DP, et al. (1994) Pathological alterations of the cerebral microvasculature in Alzheimer’s disease and related dementing disorders. Acta Neuropathol 87: 469–480. http://dx.doi.org/10.1007/BF0029417310.1007/BF00294173Search in Google Scholar

[35] Bailey TL, Rivara CB, Rocher AB, Hof PR (2004) The nature and effects of cortical microvascular pathology in aging and Alzheimer’s disease. Neurol Res 26: 573–578. http://dx.doi.org/10.1179/01616410422501627210.1179/016164104225016272Search in Google Scholar

[36] Bouras C, Kovari E, Herrmann FR, Rivara CB, Bailey TL, et al. (2006) Stereologic analysis of microvascular morphology in the elderly: Alzheimer disease pathology and cognitive status. J Neuropathol Exp Neurol 65: 235–244. 10.1097/01.jnen.0000203077.53080.2cSearch in Google Scholar

[37] Richard E, van Gool WA, Hoozemans JJ, An Haastert ES, Eikelenboom P, et al. (2010) Morphometric changes in the cortical microvascular network in Alzheimer’s disease. J Alzheimers Dis 22: 811–818. 10.3233/JAD-2010-100849Search in Google Scholar

[38] Schmidt-Kastner R, Freund TF (1991) Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40: 599–636. http://dx.doi.org/10.1016/0306-4522(91)90001-510.1016/0306-4522(91)90001-5Search in Google Scholar

[39] Petito CK, Pulsinelli WA (1984) Delayed neuronal recovery and neuronal death in rat hippocampus following severe cerebral ischemia: possible relationship to abnormalities in neuronal processes. J Cereb Blood Flow Metab 4: 194–205. 10.1038/jcbfm.1984.28Search in Google Scholar

[40] Kirino T (2000) Delayed neuronal death. Neuropathology 20Suppl: S95–97. http://dx.doi.org/10.1046/j.1440-1789.2000.00306.x10.1046/j.1440-1789.2000.00306.xSearch in Google Scholar

[41] Calabresi P, Centonze D, Pisani A, Cupini L, Bernardi G (2003) Synaptic plasticity in the ischaemic brain. Lancet Neurol 2: 622–629. http://dx.doi.org/10.1016/S1474-4422(03)00532-510.1016/S1474-4422(03)00532-5Search in Google Scholar

[42] Quintana P, Alberi S, Hakkoum D, Muller D (2006) Glutamate receptor changes associated with transient anoxia/hypoglycaemia in hippocampal slice cultures. Eur J Neurosci 23: 975–983. http://dx.doi.org/10.1111/j.1460-9568.2006.04617.x10.1111/j.1460-9568.2006.04617.xSearch in Google Scholar PubMed

[43] Schuff N, Matsumoto S, Kmiecik J, Studholme C, Du A, et al. (2009) Cerebral blood flow in ischemic vascular dementia and Alzheimer’s disease, measured by arterial spin-labeling magnetic resonance imaging. Alzheimers Dement 5: 454–462. http://dx.doi.org/10.1016/j.jalz.2009.04.123310.1016/j.jalz.2009.04.1233Search in Google Scholar

[44] Hirao K, Ohnishi T, Hirata Y, Yamashita F, Mori T, et al. (2005) The prediction of rapid conversion to Alzheimer’s disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 28: 1014–1021. http://dx.doi.org/10.1016/j.neuroimage.2005.06.06610.1016/j.neuroimage.2005.06.066Search in Google Scholar

[45] Johnson NA, Jahng GH, Weiner MW, Miller BL, Chui HC, et al. (2005) Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. Radiology 234: 851–859. http://dx.doi.org/10.1148/radiol.234304019710.1148/radiol.2343040197Search in Google Scholar

[46] Mariani E, Polidori MC, Cherubini A, Mecocci P (2005) Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview. J Chromatogr B Analyt Technol Biomed Life Sci 827: 65–75. http://dx.doi.org/10.1016/j.jchromb.2005.04.02310.1016/j.jchromb.2005.04.023Search in Google Scholar

[47] Dyrks T, Dyrks E, Masters CL, Beyreuther K (1993) Amyloidogenicity of rodent and human beta A4 sequences. FEBS Lett 324: 231–236. http://dx.doi.org/10.1016/0014-5793(93)81399-K10.1016/0014-5793(93)81399-KSearch in Google Scholar

[48] Troncoso JC, Costello A, Watson AL, Jr., Johnson GV (1993) In vitro polymerization of oxidized tau into filaments. Brain Res 613: 313–316. http://dx.doi.org/10.1016/0006-8993(93)90918-D10.1016/0006-8993(93)90918-DSearch in Google Scholar

[49] Yang SP, Bae DG, Kang HJ, Gwag BJ, Gho YS, et al. (2004) Coaccumulation of vascular endothelial growth factor with betaamyloid in the brain of patients with Alzheimer’s disease. Neurobiol Aging 25: 283–290. http://dx.doi.org/10.1016/S0197-4580(03)00111-810.1016/S0197-4580(03)00111-8Search in Google Scholar

[50] Brickman AM, Reitz C, Luchsinger JA, Manly JJ, Schupf N, et al. (2010) Long-term blood pressure fluctuation and cerebrovascular disease in an elderly cohort. Arch Neurol 67: 564–569. http://dx.doi.org/10.1001/archneurol.2010.7010.1001/archneurol.2010.70Search in Google Scholar PubMed PubMed Central

[51] McCall AL (1992) The impact of diabetes on the CNS. Diabetes 41: 557–570. http://dx.doi.org/10.2337/diabetes.41.5.55710.2337/diabetes.41.5.557Search in Google Scholar

[52] Reitz C, Tang MX, Manly J, Mayeux R, Luchsinger JA (2007) Hypertension and the risk of mild cognitive impairment. Arch Neurol 64: 1734–1740. http://dx.doi.org/10.1001/archneur.64.12.173410.1001/archneur.64.12.1734Search in Google Scholar PubMed PubMed Central

[53] Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, et al. (1997) Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. J Am Med Assoc 277: 813–817. http://dx.doi.org/10.1001/jama.277.10.81310.1001/jama.277.10.813Search in Google Scholar

[54] Petrovitch H, White LR, Izmirilian G, Ross GW, Havlik RJ, et al. (2000) Midlife blood pressure and neuritic plaques, neurofibrillary tangles, and brain weight at death: the HAAS. Honolulu-Asia aging Study. Neurobiol Aging 21: 57–62. Search in Google Scholar

[55] Kuusisto J, Koivisto K, Mykkanen L, Helkala EL, Vanhanen M, et al. (1997) Association between features of the insulin resistance syndrome and Alzheimer’s disease independently of apolipoprotein E4 phenotype: cross sectional population based study. Br Med J 315: 1045–1049. 10.1136/bmj.315.7115.1045Search in Google Scholar

[56] Gispen WH, Biessels GJ (2000) Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23: 542–549. http://dx.doi.org/10.1016/S0166-2236(00)01656-810.1016/S0166-2236(00)01656-8Search in Google Scholar

[57] Kumari MV, Hiramatsu M, Ebadi M (2000) Free radical scavenging actions of hippocampal metallothionein isoforms and of antimetallothioneins: an electron spin resonance spectroscopic study. Cell Mol Biol 46: 627–636. Search in Google Scholar

[58] Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8: 1390–1397. http://dx.doi.org/10.1038/nm79310.1038/nm793Search in Google Scholar

[59] Schneider JA, Bennett DA (2010) Where vascular meets neurodegenerative disease. Stroke 41: S144–S146. http://dx.doi.org/10.1161/STROKEAHA.110.59832610.1161/STROKEAHA.110.598326Search in Google Scholar

[60] Mungas D, Reed BR, Ellis WG, Jagust WJ (2001) The effects of age on rate of progression of Alzheimer disease and dementia with associated cerebrovascular disease. Arch Neurol 58: 1243–1247. http://dx.doi.org/10.1001/archneur.58.8.124310.1001/archneur.58.8.1243Search in Google Scholar

[61] Esiri MM, Nagy Z, Smith MZ, Barnetson L, Smith AD (1999) Cerebrovascular disease and threshold for dementia in the early stages of Alzheimer’s disease. Lancet 354: 919–920. http://dx.doi.org/10.1016/S0140-6736(99)02355-710.1016/S0140-6736(99)02355-7Search in Google Scholar

[62] Jellinger KA (2002) Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 109: 813–836. http://dx.doi.org/10.1007/s00702020006810.1007/s007020200068Search in Google Scholar PubMed

[63] Zekry D, Duyckaerts C, Moulias R, Belmin J, Geoffre C, et al. (2002) Degenerative and vascular lesions of the brain have synergistic effects in dementia of the elderly. Acta Neuropathol 103: 481–487. http://dx.doi.org/10.1007/s00401-001-0493-510.1007/s00401-001-0493-5Search in Google Scholar PubMed

[64] Beeri MS, Silverman JM, Davis KL, Marin D, Grossman HZ, et al. (2005) Type 2 diabetes is negatively associated with Alzheimer’s disease neuropathology. J Gerontol A Biol Sci Med Sci 60: 471–475. 10.1093/gerona/60.4.471Search in Google Scholar PubMed PubMed Central

[65] Heitner J, Dickson D (1997) Diabetics do not have increased Alzheimer-type pathology compared with age-matched control subjects. A retrospective postmortem immunocytochemical and histofluorescent study. Neurology 49: 1306–1311. 10.1212/WNL.49.5.1306Search in Google Scholar PubMed

[66] Sonnen JA, Larson EB, Brickell K, Crane PK, Woltjer R, et al. (2009) Different patterns of cerebral injury in dementia with or without diabetes. Arch Neurol 66: 315–322. http://dx.doi.org/10.1001/archneurol.2008.57910.1001/archneurol.2008.579Search in Google Scholar PubMed PubMed Central

[67] Nelson PT, Smith CD, Abner EA, Schmitt FA, Scheff SW, et al. (2009) Human cerebral neuropathology of Type 2 diabetes mellitus. Biochim Biophys Acta 1792: 454–469. 10.1016/j.bbadis.2008.08.005Search in Google Scholar PubMed PubMed Central

[68] van den Berg E, Reijmer YD, de Bresser J, Kessels RP, Kappelle LJ, et al. (2010) A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia 53: 58–65. http://dx.doi.org/10.1007/s00125-009-1571-910.1007/s00125-009-1571-9Search in Google Scholar PubMed PubMed Central

[69] Kivipelto M, Helkala EL, Laakso MP, Hanninen T, Hallikainen M, et al. (2001) Midlife vascular risk factors and Alzheimer’s disease in later life: longitudinal, population based study. Br Med J 322: 1447–1451. http://dx.doi.org/10.1136/bmj.322.7300.144710.1136/bmj.322.7300.1447Search in Google Scholar PubMed PubMed Central

[70] Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, et al. (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15: 1676–1689. http://dx.doi.org/10.1093/cercor/bhi04410.1093/cercor/bhi044Search in Google Scholar PubMed

[71] Bouras C, Hof PR, Giannakopoulos P, Michel JP, Morrison JH (1994) Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population from a geriatric hospital. Cereb Cortex 4: 138–150. http://dx.doi.org/10.1093/cercor/4.2.13810.1093/cercor/4.2.138Search in Google Scholar PubMed

[72] Giannakopoulos P, Hof PR, Savioz A, Guimon J, Antonarakis SE, et al. (1996) Early-onset dementias: clinical, neuropathological and genetic characteristics. Acta Neuropathol 91: 451–465. http://dx.doi.org/10.1007/s00401005045210.1007/s004010050452Search in Google Scholar PubMed

[73] Vallet PG, Guntern R, Hof PR, Golaz J, Delacourte A, et al. (1992) A comparative study of histological and immunohistochemical methods for neurofibrillary tangles and senile plaques in Alzheimer’s disease. Acta Neuropathol 83: 170–178. http://dx.doi.org/10.1007/BF0030847610.1007/BF00308476Search in Google Scholar PubMed

[74] Brookmeyer R, Gray S, Kawas C (1998) Projections of Alzheimer’s disease in the United States and the public health impact of delaying disease onset. Am J Public Health 88: 1337–1342. http://dx.doi.org/10.2105/AJPH.88.9.133710.2105/AJPH.88.9.1337Search in Google Scholar