Dementia, diabetes, Alzheimer's disease, and insulin resistance in the brain: Progress, dilemmas, new opportunities, and a hypothesis to tackle intersecting epidemics

Journal of Alzheimer's Disease

Volumn 25, Issue 1, 2011, Pages 29-41

  Kuljiš, Rodrigo O ^a,b,c   Šalković Petrišić, Melita ^d  

^a University of Texas Medical Branch School of Medicine   (United States)

^b Encephalogistics Inc   (United States)

^c Brain Mind Project Inc   (United States)

^d UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Alzheimer's disease; dementia; diabetes; insulin resistance; streptozotocin

Indexed keywords

AMYLOID BETA PROTEIN; INSULIN; INSULIN RECEPTOR; STREPTOZOCIN;

ALZHEIMER DISEASE; CEREBROVASCULAR DISEASE; COGNITION; DEMENTIA; EPIDEMIC; HUMAN; HYPERGLYCEMIA; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; MAZE TEST; NEUROPATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; RISK FACTOR;

EID: 79959639874     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-101392     Document Type: Review

References (107)

1. Kuljiš RO (2010) Grand challenges in dementia 2010. Front Neur 1, 4. doi: 10.3389/fneur.2010.00004.
2. Wild S, Roglic G, Green A, Sicree R, King H (May 2004) Global prevalence of diabetes: Estimates for 2000 and projections for 2030. Diabetes Care 27, 1047-1053. (Pubitemid 38579764)
3. Stolk RP, Breteler MM, Ott A, Pols HA, Lamberts SW, Grobbee DE, Hofman A (1997) Insulin and cognitive function in an elderly population. The Rotterdam Study. Diabetes Care 20, 792-795. (Pubitemid 27202530)
4. Leibson CL, Rocca WA, Hanson VA, Cha R, Kokmen E, O'Brien PC, Palumbo PJ (1997) Risk of dementia among persons with diabetes mellitus: A population-based cohort study. Am J Epidemiol 145, 301-308. (Pubitemid 27082028)
5. Hoyer S (1998) Risk factors for Alzheimer's disease during aging. Impacts of glucose/energy metabolism. J Neural Transm Suppl 54, 187-194. (Pubitemid 28539355)
6. GeertsH(2009) Of mice and men. Bridging the translational disconnect in CNS drug discovery. CNS Drugs 23, 915-926.
7. Kuljiš RO (2009) Toward a multi-dimensional formulation of the pathogenesis and pathophysiology of the Alzheimer dementia-like syndrome applicable to a variety of degenerative disorders and normal cognition. Med Hypotheses 73, 315-318.
8. Kuljiš RO (2010) Integrative understanding of emergent brain properties, Quantum Brain hypotheses and Connectome Alterations in dementia are key challenges to conquer Alzheimer's disease. Front Neur 1, 15. doi: 10.3389/ fneur.2010.00015.
9. Takeda S, Sato N, Uchio-Yamada K, Sawada K, Kunieda T, Takeuchi D, Kurinami H, Shinohara M, Rakugi H, Morishita R (2010) Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc Natl Acad Sci U S A 107, 7036-7041.
10. Mussico M, Palmer K, Salamone G, Lupo F, Perri R, Mosti S, Spalletta G, di Lulio F, Pettenati C, Cravello L, Caltagirone C (2009) Predictors of progression of cognitive decline in Alzheimer's disease: The role of vascular and sociodemographic factors. J Neurol 256, 1288-1295.
11. Kodl CT, Seaquist ER (2008) Cognitive dysfunction and diabetes mellitus. Endocr Rev 29, 494-511. (Pubitemid 351831510)
12. Beeri MS, Silverman JM, Davis KL, Marin D, Grossman HZ, Schmeidler J, Purohit DP, Perl DP, Davidson M, Mohs RC, Haroutunian V (2005) Type 2 diabetes is negatively associated with Alzheimer's disease neuropathology. J Gerontol A Biol Sci Med Sci 60, 471-475. (Pubitemid 40712864)
13. Sanz C, Andrieu S, Sinclair A, Hanaire H, Vellas B; REAL FR Study Group (2009) Diabetes is associated with a slower rate of cognitive decline in Alzheimer disease. Neurology 73, 1359-1366.
14. Benedict C, Hallschmid M, Hatke A, Schultes B, Fehm HL, Born J, KernW(2004) Intranasal insulin improves memory in humans. Psychoneuroendocrinol 29, 1326-1334. (Pubitemid 39024358)
15. Benedict C, Hallschmid M, Schultes B, Born J, Kern W (2007) Intranasal insulin to improve memory function in humans. Neuroendocrinol 86, 136-142. (Pubitemid 47494214)
16. Benedict C, Hallschmid M, Schmidtz K, Schultes B, Ratter F, Fehm HL, Born J, Kern W (2007) Intranasal insulin improves memory in humans: Superiority of insulin aspart. Neuropsychopharmacol 32, 239-243. (Pubitemid 44967803)
17. Reger MA, Watson GS, Frey II WH, Baker LD, Cholerton B, Keeling ML, Belongia DA, Fishel MA, Plymate SR, Schellenberg GD, Cherrier MM, Craft S (2006) Effects of intranasal insulin on cognition in memory-impaired older adults: Modulation by APOE genotype. Neurobiol Aging 27, 451-458. (Pubitemid 43185331)
18. Reger MA, Watson GS, Green PS, Wilkinson CW, Baker LD, Cholerton B, Fishel MA, Plymate SR, Breitner JCS, DeGroodt W, Mehta P, Craft S (2008) Intranasal insulin improves cognition and modulates β-amyloid in early AD. Neurology 70, 440-448.
19. Reger MA, Watson GS, Green PS, Baker LD, Cholerton B, Fishel MA, Plymate SR, Cherrier M, Schellenberg GD, Frey IIWH,Craft S (2008) Intranasal insulin administration dosedependently modulates verbal memory and plasma amyloid- β in memory-impaired older adults. J Alzheimers Dis 13, 323-331. (Pubitemid 352039034)
20. Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol 118, 103-113.
21. Neumann KF, Rojo L, Navarrete LP, Farías G, Reyes P, Maccioni RB (2008) Insulin resistance and Alzheimer's disease: Molecular links & clinical implications. Curr Alzheimer Res 5, 438-447.
22. Williams JW, Plassman BL, Burke J, Holsinger T, Benjamin S (2010) Preventing Alzheimer's disease and cognitive decline. Agency for Healthcare Research and Quality Publication No. 10-E005. Evidence Report/Technology Assessment number it193, United States Department of Health and Human Services.
23. Flood JF, Mooradian AD, Morley JE (1990) Characteristics of learning and memory in streptozocin-induced diabetic mice. Diabetes 39, 1391-1398. (Pubitemid 20372228)
24. Farr SA, Yamada KA, Butterfield AD, Abdul HM, Xu L, Miller NE, BanksWA, Morley JE (2008) Obesity and hypertriglyceridemia produce cognitive impairment. Endocrinol 149, 2628-2636. (Pubitemid 351574482)
25. Morley JE, Banks WA (2010) Lipids and cognition. J Alzheimers Dis 20, 737-747.
26. Farr SA, Banks WA, Morley JE (2006) Effects of leptin on memory processing. Peptides 27, 1420-1425. (Pubitemid 43767004)
27. Lieb W, Beiser AS, Vasan RS, Tan ZS, Au R, Harris TB, Roubenoff R, Auerbach S, DeCarli C, Wolf PA, Seshadri S (2009) Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging. JAMA 302, 2565-2572.
28. Greco SJ, Bryan KJ, Sarkar S, Zhu X, Smith MA, Ashford JW, Johnston JM, Tezapsidis N, Casadesus G (2010) Leptin reduces pathology and improves memory in a transgenic mouse model of Alzheimer's disease. J Alzheimers Dis 19, 1155-1167.
29. Hogervorst E, Bandelow S, Combrinck M, Smith AD (2004) Low free testosterone is an independent risk factor for Alzheimer's disease. Exp Gerontol 39, 1633-1639. (Pubitemid 39576135)
30. Moffat SD, Zonderman AB, Metter EJ, Kawas C, Blackman MR, Harman SM, Resnick SM (2004) Free testosterone and risk for Alzheimer disease in older men. Neurology 62, 188-193. (Pubitemid 38167123)
31. Rosario ER, Chang L, Stanczyk FZ, Pike CJ (2004) Age-related testosterone depletion and the development of Alzheimer disease. JAMA 292, 1431-1432. (Pubitemid 39258334)
32. Chu L-W, Tam S, Wong RLC, Yik P-Y, Song Y, Cheung BMY, Morley JE, Lam KSL (2010) Bioavailable testosterone predicts a lower risk of Alzheimer's disease in older men. J Alzheimers Dis 21, 1335-1345.
33. Prasad AS, Mantzoros CS, Beck FW, Hess JW, Brewer GJ (1996) Zinc status and serum testosterone levels of healthy adults. Nutrition 12, 344-348. (Pubitemid 26294996)
34. Marín DP, Figueira AJ Jr, Pinto LG (2006) One session of resistance training may increase serum testosterone and triiodetironine in young men. Med Sci Sports Exercise 38, S285.
35. Jellinger KA (2009) Alzheimer's disease: A challenge for modern neuropathobiology. Acta Neuropathol 118, 1-3.
36. Kuljiš RO (2009) Selective cerebrocortical regional, laminar, modular and cellular vulnerability and sparing in Alzheimer's disease: Unexploited clues to pathogenesis, pathophysiology, molecular- and systems-level hypothesis generation and testing. In: Current Hypotheses and Research Milestones in Alzheimer's Disease, Maccioni RB, Perry G, eds., Springer Science & Business Media, New York- Heidelberg, pp. 191-204.
37. Lannfelt L, Folkesson R, Mohammed AH, Winblad B, Hellgren D, Duff K, Hardy J (1993) Alzheimer's disease: Molecular genetics and transgenic animal models. Behav Brain Res 57, 207-213. (Pubitemid 24027151)
38. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102. (Pubitemid 26332733)
39. Price DL, Sisodia SS (1994) Cellular and molecular biology of Alzheimer's disease and animal models. Annu Rev Med 45, 435-446. (Pubitemid 24158173)
40. Price DL, Sisodia SS (1998) Mutant genes in familial Alzheimer's disease and transgenic models. Annu Rev Neurosci 21, 479-505. (Pubitemid 28150671)
41. Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT (1997) APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 56, 965-973. (Pubitemid 27386126)
42. Ashe KH (2001) Learning and memory in transgenic mice modeling Alzheimer's disease. Learn Mem 8, 301-308. (Pubitemid 34037573)
43. Gómez-Isla T, Irizarry MC (2001) Alzheimer's disease and transgenic mouse models. In: Handbook of Neuropsychology, Boller F, Kappa S, eds, Elsevier, Amsterdam, pp. 23-37.
44. Dodart JC, Mathis C, Bales KR, Paul SM (2002) Does my mouse have Alzheimer's disease? Genes Brain Behav 1, 142-155. (Pubitemid 36717672)
45. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younking L, Hyman BT, Younkin S, Ashe KH (2002) Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 22, 6331-6335. (Pubitemid 35386387)
46. Mudher A, Lovestone S (2002) Alzheimer's disease-do tauists and baptists finally shake hands? Trends Neurosci 25, 22-26. (Pubitemid 34093781)
47. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, Younkin LH, Carlson GA, Younkin SG, Ashe KH (2002) The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22, 1858-1867. (Pubitemid 35386304)
48. Higgins GA, Jacobsen H (2003) Transgenic mouse models of Alzheimer's disease: Phenotype and application. Behav Pharmacol 14, 419-438. (Pubitemid 37176800)
49. van Dooren T, Dewachter I, Borghgraef P, van Leuven F (2005) Transgenic mouse models for APP processing and Alzheimer's disease: Early and late defects. Subcell Biochem 38, 45-63.
50. Bayer TA, Wirths O (2008) Review on the APP/PS1KI mouse model: Intraneuronal Abeta accumulation triggers axonopathy, neuron loss and working memory impairment. Genes Brain Behav 7(Suppl. 1), 6-11.
51. Kuljiš RO (2010) The Fourth Element targeting hypothesis of Alzheimer's pathogenesis and pathophysiology. Front Neur 1, 144. doi: 10.3389/fneur.2010.00144.
52. Knight WD, Ahsan RL, Jackson J, Cipolotti L, Warrington EK, Fox NC, Rossor MN (2009) Pure progressive amnesia and the APPV717G mutation. Alzheimer Dis Assoc Disord 23, 410-414.
53. Shepherd C, McCann H, Halliday GM (2009) Variations in the neuropathology of familial Alzheimer's disease. Acta Neuropathol 118, 37-52.
54. Roses AD (1996) The Alzheimer diseases. Curr Opin Neurobiol 6, 644-650. (Pubitemid 26387720)
55. Ito M, Echizenya N, Nemoto D, Kase M (2009) A case series of epilepsy-derived memory impairment resembling Alzheimer disease. Alzheimer Dis Assoc Disord 23, 406-409.
56. Sarasa Pesini P (2009) Natural non-transgenic animal models for research in Alzheimer's disease. Curr Alzheimer Res 6, 171-178.
57. Lacković Z, Šalković M (1990) Streptozotocin and alloxan produce alterations in rat brain monoamines independently of pancreatic beta cells destruction. Life Sci 46, 49-54. (Pubitemid 20019513)
58. Blondel O, Portha B (1989) Early appearance of in vivo insulin resistance in adult streptozotocin-injected rats. Diabetes Metab 15, 382-387. (Pubitemid 20076229)
59. Kadowaki T, Kasuga M, Akanuma Y, Ezaki O, Takaku F (1984) Decreased autophosphorylation of the insulin receptor-kinase in streptozotocin-diabetic rats. J Biol Chem 259, 14208-14216. (Pubitemid 15223998)
60. Szkudelski T (2001) The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50, 537-546. (Pubitemid 34087272)
61. Brant AM, Jess TJ, Milligan G, Brown CM, Gould GW (1993) Immunological analysis of glucose transporters expressed in different regions of the rat brain and central nervous system. Biochem Biophys Res Commun 192, 1297-1302. (Pubitemid 23218553)
62. Arluison M, Quignon M, Nguyen P, Thorens B, Leloup C, Penicaud L (2004) Distribution and anatomical localization of the glucose transporter 2 (GLUT2) in the adult rat brain-an immunohistochemical study. J Chem Neuroanat 28, 117-136. (Pubitemid 39336524)
63. Hoyer S, LannertH(2007) Long-term abnormalities in brain glucose/energy metabolism after inhibition of the neuronal insulin receptor: Implication of tau-protein. J Neural Transm Suppl 72, 195-202.
64. Plaschke K, Hoyer S (1993) Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int JDev Neurosci 11, 477-483.
65. Šalković-Petrišić M, Riederer P (2010) Brain glucose transporter protein 2 and sporadic Alzheimer's disease. Translat Neurosci 1, 202-206.
66. Unger J, McNeill TH, Moxley RT 3rd, White M, Moss A, Livingston JN (1989) Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience 31, 143-157. (Pubitemid 19209704)
67. Šalković-PetrišićM, Tribl F, Schmidt M, Hoyer S, Riederer P (2006) Alzheimer-like changes in protein kinase B and glycogen synthase kinase-3 in rat frontal cortex and hippocampus after damage to the insulin signalling pathway. J Neurochem 96, 1005-1015.
68. Grünblatt E, Šalković-Petrišić M, Osmanovic J, Riederer P, Hoyer S (2007) Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem 101, 757-770. (Pubitemid 46633313)
69. Plaschke K, Kopitz J, Siegelin M, Schliebs R, Šalković- Petrišić M, Riederer P, Hoyer S (2010) Insulin-resistant brain state after intracerebroventricular streptozotocin injection exacerbates Alzheimer-like changes in Tg2576 AbetaPP-overexpressing mice. J Alzheimers Dis 19, 691-704.
70. Mayer G, Nitsch R, Hoyer S (1990) Effects of changes in peripheral and cerebral glucose metabolism on locomotor activity, learning and memory in adult male rats. Brain Res 532, 95-100. (Pubitemid 20384645)
71. Hoyer S, Lannert H, Noldner M, Chatterjee SS (1999) Damaged neuronal 127 energy metabolism and behavior are improved by Ginkgo biloba 128 extract (EGb 761). J Neural Transm 106, 1171-1188. (Pubitemid 30009214)
72. Nitsch R, Hoyer S (1991) Local action of the diabetogenic drug, streptozotocin, on glucose and energy metabolism in rat brain cortex. Neurosci Lett 128, 199-202.
73. Šalković-Petrišić M, Hoyer S (2007) Central insulin resistance as a trigger for sporadic Alzheimer-like pathology: An experimental approach. J Neural Transm Suppl 72, 217-233.
74. Weinstock M, Shoham S (2004) Rat models of dementia based on reductions in regional glucose metabolism, cerebral blood flow and cytochrome oxidase activity. J Neural Transm 111, 347-366. (Pubitemid 38316610)
75. Hellweg R, Nitsch R, Hock C, Jaksch M, Hoyer S (1992) Nerve growth factor and choline acetyltransferase activity levels in the rat brain following experimental impairment of cerebral glucose and energy metabolism. J Neurosci Res 31, 479-486.
76. Hoyer S, Lannert H (2008) Long-term effects of corticosterone on behavior, oxidative and energy metabolism of parietotemporal cerebral cortex and hippocampus of rats: Comparison to intracerebroventricular streptozotocin. J Neural Transm 115, 1241-1249.
77. Labak M, Foniok T, Kirk D, Rushforth D, Tomanek B, Jasinski A, Grieb P (2010) Metabolic changes in rat brain following intracerebroventricular injections of streptozotocin: A model of sporadic Alzheimer's disease. Acta Neurochir Suppl 106, 177-181.
78. Shoham S, Bejar C, Kovalev E, Weinstock M (2003) Intracerebroventricular injection of streptozotocin causes neurotoxicity to myelin that contributes to spatial memory deficits in rats. Exp Neurol 184, 1043-1052. (Pubitemid 38182835)
79. Nikkel A, Lee Y, Kohlhaas K, Rustay N, Day M, Bitner R (2010) Central injection of streptozotocin induces and Alzheimer's disease-like phenotype in mice. Program No. 247.25. 2010 Neuroscience Meeting Planner. Society for Neuroscience, San Diego, CA, Online.
80. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH (2003) Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40, 471-483. (Pubitemid 37494698)
81. Hoyer S (1998) Is sporadic Alzheimer disease the brain type of non-insulin dependent diabetes mellitus? A challenging hypothesis. J Neural Transm 105, 415-422. (Pubitemid 28365026)
82. Lannert H, Hoyer S (1998) Intracerebroventricular administration of streptozotocin causes long-term diminutions in learning and memory abilities and in cerebral energy metabolism in adult rats. Behav Neurosci 112, 1199-1208. (Pubitemid 28519002)
83. Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K,Wands JR, de la Monte SM (2006) Intracerebral streptozotocin model of type 3 diabetes: Relevance to sporadic Alzheimer's disease. J Alzheimers Dis 9, 13-33.
84. de la Monte SM, Tong M, Lawton M, Longato L (2009) Nitrosamine exposure exacerbates high fat diet-mediated type 2 diabetes mellitus, non-alcoholic steatohepatitis, and neurodegeneration with cognitive impairment. Mol Neurodegen 4, 54-74.
85. Šalković-Petrišić M, Osmanovic J, Grünblat E, Hoyer S, Riederer P (2008) Brain insulin dysfunction triggers plaques formation in rat model of sporadic Alzheimer's disease. Alzheimer Dement 4(Suppl. 2), T-206.
86. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
87. Šalković-Petrišić M, Osmanovic J, Grünblatt E, Riederer P, Hoyer S (2009) Modeling sporadic Alzheimer disease: The insulin resistant brain state generates multiple long-term morphobiological abnormalities including hyperphosphorylated tau protein and amyloid-beta. A synthesis. J Alzheimers Dis 18, 729-750.
88. Hoyer S (2004) Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur J Pharmacol 490, 115-125. (Pubitemid 38482165)
89. Deng Y, Li B, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX (2009) Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain: Implication for Alzheimer's disease. Am J Pathol 175, 2089-2098.
90. Agrawal R, Mishra B, Tyagi E, Nath C, Sukla R (2010) Effect of curcumin on brain insulin receptors and memory function in STZ (ICV) induced dementia model of rat. Phramacol Res 61, 247-252.
91. Morel F (1943) Angiopathie topistique atteignant électivement la IVéme couche de l'aire striée. Monatschrift zum Psiquiatrie und Neurologie 108, 248-254.
92. Pantelakis S (1954) Un type particulier d'angiopathie senile du systéme nerveux central: L'angiopathie congophile, Topographie et frequence. Monatsschrifi für Psychiatrie und Neurologie 128, 219-256.
93. Neumann MA (1960) Combined amyloid vascular changes and argyrophilic plaques in the central nervous system. J Neuropathol Exp Neurol 19, 370-382.
94. Buée L, Hof PR, Bouras C, Delacourte A, Perl DP, Morrison JH, Fillit HM (1994) Pathological alterations of the cerebral microvasculature in Alzheimer's disease and related dementing disorders. Acta Neuropathol 87, 469-480. (Pubitemid 24128974)
95. Thal DR, Griffin WS, de Vos RA, Ghebremedhin E (2008) Cerebral amyloid angiopathy and its relationship to Alzheimer's disease. Acta Neuropathol 115, 599-609.
96. Kuljiš RO, Tikoo RK (1997) Discontinuous distribution of senile plaques within striate cortex hypercolumns in Alzheimer's disease. Vision Res 37, 3573-3591. (Pubitemid 27491636)
97. Kuljiš RO (1994) The human primary visual cortex. In: Cerebral Cortex, Vol. 10, Chapter 12. Peters AA, Rockland KS eds., New York, Plenum, pp. 469-503.
98. Bell MA, Ball MJ (1985) Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 335, 139-143. (Pubitemid 15035367)
99. Yamada M, Itoh Y, Shintaku M, Kawamura J, Jensson O, Thorsteinsson L, Suematsu N, Matsushita M, Otomo E (1996) Immune reactions associated with cerebral amyloid angiopathy. Stroke 27, 1155-1162. (Pubitemid 26226947)
100. Jellinger KA, Attems J (2010) Prevalence of dementia disorders in the oldest-old: An autopsy study. Acta Neuropathol 119, 421-433.
101. Fernández J, Rojo L, Kuljiš RO, Maccioni RB (2008) The damage signals hypothesis of Alzheimer's disease. J Alzheimers Dis 14, 329-333. (Pubitemid 352040051)
102. Sharma M, Gupta YK (2001) Intracerebroventricular injection of streptozotocin in rats produces both oxidative stress in the brain and cognitive impairment. Life Sci 68, 1021-1029. (Pubitemid 32168054)
103. Sapcanin A, Sofić E, Tahirovic I, Šalković- PetrišićM,Hoyer S, Riederer P (2008) Antioxidant capacity in rat brain after intracerebroventricular treatment with streptozotocin and alloxan - a preliminary study. Neurotox Res 13, 97-104.
104. Fraenkel L, Fried TR (2010) Individualized medical decision making: Necessary, achievable, but not yet attainable. Arch Intern Med 170, 566-569.
105. Niederhuber JE (2010) Translating discovery to patient care. JAMA 303, 1088-1089.
106. Haacke EM, DelProposto ZS, Chaturvedi S, Sehgal V, Tenzer M, Neelavalli J, Kido D (2007) Imaging cerebral amyloid angiopathy with susceptibility- weighted imaging. Am J Neuroradiol 28, 316-317. (Pubitemid 46281054)
107. Bonda DJ, Wang X, Perry G, Nunomura A, Tabaton M, Zhu X, SmithMA(2010) Oxidative stress in Alzheimer disease: A possibility for prevention. Neuropharmacol 59, 290-294.