Multinutrient diets improve cerebral perfusion and neuroprotection in a murine model of Alzheimer's disease

Neurobiology of Aging

Volumn 35, Issue 3, 2014, Pages 600-613

  Zerbi, Valerio ^a,b   Jansen, Diane ^a   Wiesmann, Maximilian ^a,b   Fang, Xiaotian ^a   Broersen, Laus M ^c   Veltien, Andor ^b   Heerschap, Arend ^b   Kiliaan, Amanda J ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c DANONE RESEARCH   (Netherlands)

Author keywords

AD mouse model; Alzheimer's disease; APPswe Ps1de9; Cerebral blood flow; Diffusion tensor imaging; Mice; MRI; Nutrition; Omega 3 fatty acids

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CHOLINE; CYANOCOBALAMIN; DOCOSAHEXAENOIC ACID; FOLIC ACID; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; PHOSPHOLIPID; PYRIDOXINE; SELENIUM; URIDINE PHOSPHATE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN PERFUSION; BRAIN WATER; CONTROLLED STUDY; DENTATE GYRUS; DIET THERAPY; GRAY MATTER; HIPPOCAMPUS; MALE; MOUSE; NERVE DEGENERATION; NERVE FIBER; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SYNAPTIC MEMBRANE; THALAMUS; THERAPY EFFECT; WHITE MATTER;

AD MOUSE MODEL; ALZHEIMER'S DISEASE; APPSWE/PS1DE9; CEREBRAL BLOOD FLOW; DIFFUSION TENSOR IMAGING; MICE; MRI; NUTRITION; OMEGA-3 FATTY ACIDS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BODY WATER; BRAIN; CEREBROVASCULAR CIRCULATION; DIFFUSION TENSOR IMAGING; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FATTY ACIDS, OMEGA-3; MALE; MICE; MICE, TRANSGENIC; NEUROPROTECTIVE AGENTS; PRESENILIN-1; URIDINE MONOPHOSPHATE;

EID: 84889581933     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.09.038     Document Type: Article

References (103)

1. Akbar M., Calderon F., Wen Z., Kim H.Y. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc. Natl. Acad. Sci. U.S.A 2005, 102:10858-10863. 10.1073/pnas.0502903102.
2. Alsop D.C., Detre J.A., Grossman M. Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging. Ann. Neurol. 2000, 47:93-100.
3. Arendash G.W., Jensen M.T., Salem N., Hussein N., Cracchiolo J., Dickson A., Leighty R., Potter H. Adiet high in omega-3 fatty acids does not improve or protect cognitive performance in Alzheimer's transgenic mice. Neuroscience 2007, 149:286-302. 10.1016/j.neuroscience.2007.08.018.
4. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal 2008, 12:26-41. 10.1016/j.media.2007.06.004.
5. Barberger-Gateau P., Raffaitin C., Letenneur L., Berr C., Tzourio C., Dartigues J.F., Alperovitch A. Dietary patterns and risk of dementia: the Three-Citycohort study. Neurology 2007, 69:1921-1930. 10.1212/01.wnl.0000278116.37320.52.
6. Barberger-Gateau P., Samieri C., Feart C., Plourde M. Dietary omega 3 polyunsaturated fatty acids and Alzheimer's disease: interaction with apolipoprotein E genotype. Curr. Alzheimer Res. 2011, 8:479-491.
7. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994, 66:259-267. 10.1016/S0006-3495(94)80775-1.
8. Bazan N.G. Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol. 2005, 15:159-166.
9. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR. Biomed. 2002, 15:435-455. 10.1002/nbm.782.
10. Beydoun M.A., Kaufman J.S., Sloane P.D., Heiss G., Ibrahim J. n-3 Fatty acids, hypertension and risk of cognitive decline among older adults in the Atherosclerosis Risk in Communities (ARIC) study. Public Health Nutr. 2008, 11:17-29. 10.1017/S1368980007000080.
11. Binnewijzend M.A., Kuijer J.P., Benedictus M.R., van der Flier W.M., Wink A.M., Wattjes M.P., van Berckel B.N., Scheltens P., Barkhof F. Cerebral blood flow measured with 3D pseudocontinuous arterial spin-labeling MR imaging in Alzheimer disease and mild cognitive impairment: a marker for disease severity. Radiology 2013, 267:221-230. 10.1148/radiol.12120928.
12. Borchelt D.R., Ratovitski T., van Lare J., Lee M.K., Gonzales V., Jenkins N.A., Copeland N.G., Price D.L., Sisodia S.S. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997, 19:939-945.
13. Bourre J.M., Dumont O., Piciotti M., Clement M., Chaudiere J., Bonneil M., Nalbone G., Lafont H., Pascal G., Durand G. Essentiality of omega 3 fatty acids for brain structure and function. World Rev. Nutr. Diet. 1991, 66:103-117.
14. Bourre J.M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., Durand G. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J.Nutr. 1989, 119:1880-1892.
15. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 1995, 16:271-278. discussion 8-84.
16. Broersen L.M., Kuipers A.A., Balvers M., van Wijk N., Savelkoul P.J., de Wilde M.C., van der Beek E.M., Sijben J.W., Hageman R.J., Kamphuis P.J., Kiliaan A.J. Aspecific multi-nutrient diet reduces Alzheimer-like pathology in young adult AbetaPPswe/PS1dE9 mice. J.Alzheimers Dis. 2013, 33:177-190. 10.3233/JAD-2012-112039.
17. Calamante F., Thomas D.L., Pell G.S., Wiersma J., Turner R. Measuring cerebral blood flow using magnetic resonance imaging techniques. J. Cereb. Blood Flow Metab. 1999, 19:701-735. 10.1097/00004647-199907000-00001.
18. Canevari L., Clark J.B. Alzheimer's disease and cholesterol: the fat connection. Neurochem. Res. 2007, 32:739-750. 10.1007/s11064-006-9200-1.
19. Cansev M., Wurtman R.J. Chronic administration of docosahexaenoic acid or eicosapentaenoic acid, but not arachidonic acid, alone or in combination with uridine, increases brain phosphatide and synaptic protein levels in gerbils. Neuroscience 2007, 148:421-431. 10.1016/j.neuroscience.2007.06.016.
20. Cao D., Kevala K., Kim J., Moon H.-S., Jun S.B., Lovinger D., Kim H.-Y. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J. Neurochem. 2009, 111:510-521.
21. Casserly I., Topol E. Convergence of atherosclerosis and Alzheimer's disease: inflammation, cholesterol, and misfolded proteins. Lancet 2004, 363:1139-1146. 10.1016/S0140-6736(04)15900-X.
22. Chen H., Epelbaum S., Delatour B. Fiber tracts Anomalies in APPxPS1 transgenic mice modeling Alzheimer's disease. J.Aging Res. 2011, 2011:281274. 10.4061/2011/281274.
23. Cole G.M., Ma Q.L., Frautschy S.A. Omega-3 fatty acids and dementia. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81:213-221.
24. Cummings J.L. Food for thought: Souvenaid in mild Alzheimer's disease. J.Alzheimers Dis. 2012, 31:237-238. 10.3233/JAD-2012-120245.
25. Cunnane S.C., Plourde M., Pifferi F., Begin M., Feart C., Barberger-Gateau P. Fish, docosahexaenoic acid and Alzheimer's disease. Prog. Lipid Res. 2009, 48:239-256. 10.1016/j.plipres.2009.04.001.
26. de la Torre J.C. Alzheimer disease as a vascular disorder: nosological evidence. Stroke 2002, 33:1152-1162.
27. de la Torre J.C. Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol. 2004, 3:184-190.
28. de Toledo Ferraz Alves T.C., Ferreira L.K., Wajngarten M., Busatto G.F. Cardiac disorders as risk factors for Alzheimer's disease. J.Alzheimers Dis. 2010, 20:749-763. 10.3233/JAD-2010-091561.
29. de Wilde M.C., Farkas E., Gerrits M., Kiliaan A.J., Luiten P.G. The effect of n-3 polyunsaturated fatty acid-rich diets on cognitive and cerebrovascular parameters in chronic cerebral hypoperfusion. Brain Res. 2002, 947:166-173.
30. de Wilde M.C., Penke B., van der Beek E.M., Kuipers A.A, Kamphuis P.J., Broersen L.M. Neuroprotective effects of a specific multi-nutrient intervention against Abeta42-induced toxicity in rats. J. Alzheimers Dis 2011, 27:327-339. 10.3233/JAD-2011-110635.
31. Dubois A., Herard A.S., Flandin G., Duchesnay E., Besret L., Frouin V., Hantraye P., Bonvento G., Delzescaux T. Quantitative validation of voxel-wise statisticalanalyses of autoradiographic rat brain volumes: application to unilateral visual stimulation. NeuroImage 2008, 40:482-494. 10.1016/j.neuroimage.2007.11.054.
32. Dyall S.C., Michael G.J., Michael-Titus A.T. Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J.Neurosci. Res. 2010, 88:2091-2102.
33. Eskelinen M.H., Ngandu T., Helkala E.L., Tuomilehto J., Nissinen A., Soininen H., Kivipelto M. Fat intake at midlife and cognitive impairment later in life: a population-based CAIDE study. Int. J. Geriatr. Psychiatry 2008, 23:741-747. 10.1002/gps.1969.
34. Farkas E., de Wilde M.C., Kiliaan A.J., Meijer J., Keijser J.N., Luiten P.G. Dietary long chain PUFAs differentially affect hippocampal muscarinic 1 and serotonergic 1A receptors in experimental cerebral hypoperfusion. Brain Res. 2002, 954:32-41.
35. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 2001, 64:575-611.
36. Fellgiebel A., Wille P., Muller M.J., Winterer G., Scheurich A., Vucurevic G., Schmidt L.G., Stoeter P. Ultrastructural hippocampal and white matter alterations in mild cognitive impairment: a diffusion tensor imaging study. Dement. Geriatr. Cogn. Disord. 2004, 18:101-108.
37. Fontani G., Corradeschi F., Felici A., Alfatti F., Migliorini S., Lodi L. Cognitive and physiological effects of Omega-3 polyunsaturated fatty acid supplementation in healthy subjects. Eur. J. Clin. Invest. 2005, 35:691-699.
38. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego.
39. Frieden C., Garai K. Structural differences between apoE3 and apoE4 may be useful in developing therapeutic agents for Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A 2012, 109:8913-8918. 10.1073/pnas.1207022109.
40. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., Prada C., Greenberg S.M., Bacskai B.J., Frosch M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol. Dis. 2006, 24:516-524.
41. Green K.N., Martinez-Coria H., Khashwji H., Hall E.B., Yurko-Mauro K.A., Ellis L., LaFerla F.M. Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-beta and tau pathology via a mechanism involving presenilin 1 levels. J.Neurosci. 2007, 27:4385-4395. 10.1523/JNEUROSCI.0055-07.2007.
42. Hanyu H., Sakurai H., Iwamoto T., Takasaki M., Shindo H., Abe K. Diffusion-weighted MR imaging of the hippocampus and temporal white matter in Alzheimer's disease. J.Neurol. Sci. 1998, 156:195-200.
43. Harsan L.A., Paul D., Schnell S., Kreher B.W., Hennig J., Staiger J.F., von Elverfeldt D. Invivo diffusion tensor magnetic resonance imaging and fiber tracking of the mouse brain. NMR Biomed. 2010, 23:884-896. 10.1002/nbm.1496.
44. Iqbal K., Grundke-Iqbal I. Alzheimer's disease, a multifactorial disorder seeking multitherapies. Alzheimer's Demen. 2010, 6:420-424. 10.1016/j.jalz.2010.04.006.
45. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 2001, 17:157-165.
46. Jueptner M., Weiller C. Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. NeuroImage 1995, 2:148-156.
47. Kalmijn S., Launer L.J., Ott A., Witteman J.C., Hofman A., Breteler M.M. Dietary fat intake and the risk of incident dementia in the Rotterdam Study. Ann. Neurol. 1997, 42:776-782. 10.1002/ana.410420514.
48. Kamphuis P.J., Scheltens P. Can nutrients prevent or delay onset of Alzheimer's disease?. J.Alzheimers Dis. 2010, 20:765-775. 10.3233/JAD-2010-091558.
49. Kantarci K. Diffusion tensor imaging in Alzheimer's disease. Curr. Med. Imaging Rev. 2011, 7:6.
50. Kantarci K., Petersen R.C., Boeve B.F., Knopman D.S., Weigand S.D., O'Brien P.C., Shiung M.M., Smith G.E., Ivnik R.J., Tangalos E.G., Jack C.R. DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology 2005, 64:902-904. 10.1212/01.WNL.0000153076.46126.E9.
51. Kennedy E.P., Weiss S.B. The function of cytidine coenzymes in the biosynthesis of phospholipides. J.Biol. Chem. 1956, 222:193-214.
52. Kida I., Hyder F. Physiology of functional magnetic resonance imaging: energetics and function. Methods Mol. Med. 2006, 124:175-195.
53. Kim S.G. Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn. Reson. Med. 1995, 34:293-301.
54. Knott G.W., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex invivo. Nat. Neurosci. 2006, 9:1117-1124. 10.1038/nn1747.
55. Kozauer N., Katz R. Regulatory innovation and drug development for early-stage Alzheimer's disease. N.Engl. J. Med 2013, 368:1169-1171. 10.1056/NEJMp1302513.
56. Kwong K.K., McKinstry R.C., Chien D., Crawley A.P., Pearlman J.D., Rosen B.R. CSF-suppressed quantitative single-shot diffusion imaging. Magn. Reson. Med. official j. Soc. Magn. Reson. Med./Soc. Magn. Reson. Med. 1991, 21:157-163.
57. Lee J.H., O'Keefe J.H., Lavie C.J., Marchioli R., Harris W.S. Omega-3 fatty acids for cardioprotection. Mayo Clin. Proc. 2008, 83:324-332. 10.4065/83.3.324.
58. Leithner C., Gertz K., Schrock H., Priller J., Prass K., Steinbrink J., Villringer A., Endres M., Lindauer U., Dirnagl U., Royl G. Aflow sensitive alternating inversion recovery (FAIR)-MRI protocol to measure hemispheric cerebral blood flow in a mouse stroke model. Exp. Neurol. 2008, 210:118-127. 10.1016/j.expneurol.2007.10.003.
59. Lin A.L., Qin Q., Zhao X., Duong T.Q. Blood longitudinal (T1) and transverse (T2) relaxation time constants at 11.7 Tesla. MAGMA 2012, 25:245-249. 10.1007/s10334-011-0287-2.
60. Luchsinger J.A., Reitz C., Honig L.S., Tang M.X., Shea S., Mayeux R. Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 2005, 65:545-551. 10.1212/01.wnl.0000172914.08967.dc.
61. Meyer E.P., Ulmann-Schuler A., Staufenbiel M., Krucker T. Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A 2008, 105:3587-3592.
62. Mi W., van Wijk N., Cansev M., Sijben J.W., Kamphuis P.J. Nutritional approaches in the risk reduction and management of Alzheimer's disease. Nutrition 2013, 29:1080-1089. 10.1016/j.nut.2013.01.024.
63. Minihane A.M., Khan S., Leigh-Firbank E.C., Talmud P., Wright J.W., Murphy M.C., Griffin B.A., Williams C.M. ApoE polymorphism and fish oil supplementation in subjects with an atherogenic lipoprotein phenotype. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1990-1997.
64. Morgan D.R., Dixon L.J., Hanratty C.G., El-Sherbeeny N., Hamilton P.B., McGrath L.T., Leahey W.J., Johnston G.D., McVeigh G.E. Effects of dietary omega-3 fatty acid supplementation on endothelium-dependent vasodilation in patients with chronic heart failure. Am. J. Cardiol. 2006, 97:547-551. 10.1016/j.amjcard.2005.08.075.
65. Nakata Y., Sato N., Nemoto K., Abe O., Shikakura S., Arima K., Furuta N., Uno M., Hirai S., Masutani Y., Ohtomo K., Barkovich A.J., Aoki S. Diffusion abnormality in the posterior cingulum and hippocampal volume: correlation with disease progression in Alzheimer's disease. Magn. Reson. Imaging 2009, 27:347-354.
66. Niwa K., Carlson G.A., Iadecola C. Exogenous A beta1-40 reproduces cerebrovascular alterations resulting from amyloid precursor protein overexpression in mice. J.Cereb. Blood Flow Metab. 2000, 20:1659-1668. 10.1097/00004647-200012000-00005.
67. Oksman M., Iivonen H., Hogyes E., Amtul Z., Penke B., Leenders I., Broersen L., Lutjohann D., Hartmann T., Tanila H. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol. Dis. 2006, 23:563-572. 10.1016/j.nbd.2006.04.013.
68. Oosterlinck W.W., Dresselaers T., Geldhof V., Van Santvoort A., Robberecht W., Herijgers P., Himmelreich U. Response of mouse brain perfusion to hypo- and hyperventilation measured by arterial spin labeling. Magn. Reson. Med. 2011, 66:802-811. 10.1002/mrm.23060.
69. Perez S.E., Berg B.M., Moore K.A., He B., Counts S.E., Fritz J.J., Hu Y.S., Lazarov O., Lah J.J., Mufson E.J. DHA diet reduces AD pathology in young APPswe/PS1 Delta E9 transgenic mice: possible gender effects. J.Neurosci. Res. 2010, 88:1026-1040. 10.1002/jnr.22266.
70. Pooler A.M., Guez D.H., Benedictus R., Wurtman R.J. Uridine enhances neurite outgrowth in nerve growth factor-differentiated PC12 [corrected]. Neuroscience 2005, 134:207-214. 10.1016/j.neuroscience.2005.03.050.
71. Price J.M., Chi X., Hellermann G., Sutton E.T. Physiological levels of beta-amyloid induce cerebral vessel dysfunction and reduce endothelial nitric oxide production. Neurol. Res. 2001, 23:506-512.
72. Puglielli L., Tanzi R.E., Kovacs D.M. Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 2003, 6:345-351. 10.1038/nn0403-345.
73. Quinn J.F., Raman R., Thomas R.G., Yurko-Mauro K., Nelson E.B., Van Dyck C., Galvin J.E., Emond J., Jack C.R., Weiner M., Shinto L., Aisen P.S. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 2010, 304:1903-1911. 10.1001/jama.2010.1510.
74. Rao J.S., Ertley R.N., Lee H.J., DeMar J.C., Arnold J.T., Rapoport S.I., Bazinet R.P. n-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry 2007, 12:36-46. 10.1038/sj.mp.4001888.
75. Ruitenberg A., den Heijer T., Bakker S.L., van Swieten J.C., Koudstaal P.J., Hofman A., Breteler M.M. Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Ann. Neurol. 2005, 57:789-794.
76. Sakamoto T., Cansev M., Wurtman R.J. Oral supplementation with docosahexaenoic acid and uridine-5'-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res. 2007, 1182:50-59. 10.1016/j.brainres.2007.08.089.
77. Samieri C., Lorrain S., Buaud B., Vaysse C., Berr C., Peuchant E., Cunnane S.C., Barberger-Gateau P. Relationship between diet and plasma long-chain n-3 PUFAs in older people: impact of apolipoprotein E genotype. J.Lipid Res. 2013, 54:2559-2567. 10.1194/jlr.P036475.
78. Sawiak S.J., Wood N.I., Williams G.B., Morton A.J., Carpenter T.A. Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol. Dis. 2009, 33:20-27. 10.1016/j.nbd.2008.09.016.
79. Schaefer E.J., Bongard V., Beiser A.S., Lamon-Fava S., Robins S.J., Au R., Tucker K.L., Kyle D.J., Wilson P.W., Wolf P.A. Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch. Neurol. 2006, 63:1545-1550. 10.1001/archneur.63.11.1545.
80. Scheltens P., Kamphuis P.J., Verhey F.R., Olde Rikkert M.G., Wurtman R.J., Wilkinson D., Twisk J.W., Kurz A. Efficacy of a medical food in mild Alzheimer's disease: a randomized, controlled trial. Alzheimer's Demen. 2010, 6:1-10 e1. 10.1016/j.jalz.2009.10.003.
81. Scheltens P., Twisk J.W., Blesa R., Scarpini E., von Arnim C.A., Bongers A., Harrison J., Swinkels S.H., Stam C.J., de Waal H., Wurtman R.J., Wieggers R.L., Vellas B., Kamphuis P.J. Efficacy of Souvenaid in mild Alzheimer's disease: results from a randomized, controlled trial. J.Alzheimers Dis. 2012, 31:225-236. 10.3233/JAD-2012-121189.
82. Schreiber S.J., Doepp F., Spruth E., Kopp U.A., Valdueza J.M. Ultrasonographic measurement of cerebral blood flow, cerebral circulation time and cerebral blood volume in vascular and Alzheimer's dementia. J.Neurol. 2005, 252:1171-1177.
83. Sennvik K., Fastbom J., Blomberg M., Wahlund L.O., Winblad B., Benedikz E. Levels of alpha- and beta-secretase cleaved amyloid precursor protein in the cerebrospinal fluid of Alzheimer's disease patients. Neurosci. Lett. 2000, 278:169-172.
84. Shin H.K., Jones P.B., Garcia-Alloza M., Borrelli L., Greenberg S.M., Bacskai B.J., Frosch M.P., Hyman B.T., Moskowitz M.A., Ayata C. Age-dependent cerebrovascular dysfunction in a transgenic mouse model of cerebral amyloid angiopathy. Brain 2007, 130(Pt 9):2310-2319.
85. Song S.-K., Kimg J.H., Lin S.-J., Brendza R.P., Holtzman D.M. Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol. Dis. 2004, 15:640-647.
86. Song S.-K., Kimg J.H., Lin S.-J., Brendza R.P., Holtzman D.M. Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol. Dis. 2004, 15:7.
87. Song S.K., Kim J.H., Lin S.J., Brendza R.P., Holtzman D.M. Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol. Dis. 2004, 15:640-647. 10.1016/j.nbd.2003.12.003.
88. Song S.K., Yoshino J., Le T.Q., Lin S.J., Sun S.W., Cross A.H., Armstrong R.C. Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 2005, 26:132-140. 10.1016/j.neuroimage.2005.01.028.
89. Sun S.W., Liang H.F., Cross A.H., Song S.K. Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. NeuroImage 2008, 40:1-10. 10.1016/j.neuroimage.2007.11.049.
90. Sykova E., Vorisek I., Antonova T., Mazel T., Meyer-Luehmann M., Jucker M., Hajek M., Ort M., Bures J. Changes in extracellular space size and geometry in APP23 transgenic mice: a model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A 2005, 102:479-484. 10.1073/pnas.0408235102.
91. van de Rest O., Spiro A., Krall-Kaye E., Geleijnse J.M., de Groot L.C., Tucker K.L. Intakes of (n-3) fatty acids and fatty fish are not associated with cognitive performance and 6-year cognitive change in men participating in the Veterans Affairs Normative Aging Study. J.Nutr. 2009, 139:2329-2336. 10.3945/jn.109.113647.
92. van Wijk N., Watkins C.J., Bohlke M., Maher T.J., Hageman R.J., Kamphuis P.J., Broersen L.M., Wurtman R.J. Plasma choline concentration varies with different dietary levels of vitamins B6, B12 and folic acid in rats maintained on choline-adequate diets. Br. J. Nutr. 2012, 107:1408-1412. 10.1017/S0007114511004570.
93. van Wijk N., Watkins C.J., Hageman R.J., Sijben J.C., Kamphuis P.G., Wurtman R.J., Broersen L.M. Combined dietary folate, vitamin B-12, and vitamin B-6 intake influences plasma docosahexaenoic acid concentration in rats. Nutr. Metab. (Lond) 2012, 9:49. 10.1186/1743-7075-9-49.
94. Weidensteiner C., Metzger F., Bruns A., Bohrmann B., Kuennecke B., von Kienlin M. Cortical hypoperfusion in the B6.PS2APP mouse model for Alzheimer's disease: comprehensive phenotyping of vascular and tissular parameters by MRI. Magn. Reson. Med. 2009, 62:35-45. 10.1002/mrm.21985.
95. Wiesmann M., Jansen D., Zerbi V., Broersen L.M., Garthe A., Kiliaan A.J. Improved spatial learning strategy and memory in aged Alzheimer AbetaPPswe/PS1dE9 mice on a multi-nutrient diet. J.Alzheimers Dis. 2013, 37:233-245. 10.3233/JAD-130179.
96. Wolozin B., Manger J., Bryant R., Cordy J., Green R.C., McKee A. Re-assessing the relationship between cholesterol, statins and Alzheimer's disease. Acta Neurol. Scand. Suppl. 2006, 185:63-70. 10.1111/j.1600-0404.2006.00687.x.
97. Wurtman R.J., Cansev M., Sakamoto T., Ulus I.H. Use of phosphatide precursors to promote synaptogenesis. Annu. Rev. Nutr. 2009, 29:59-87. 10.1146/annurev-nutr-080508-141059.
98. Wurtman R.J., Ulus I.H., Cansev M., Watkins C.J., Wang L., Marzloff G. Synaptic proteins and phospholipids are increased in gerbil brain by administering uridine plus docosahexaenoic acid orally. Brain Res. 2006, 1088:83-92. 10.1016/j.brainres.2006.03.019.
99. Yurko-Mauro K., McCarthy D., Rom D., Nelson E.B., Ryan A.S., Blackwell A., Salem N., Stedman M. Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimer's Dement. 2010, 6:456-464. 10.1016/j.jalz.2010.01.013.
100. Zerbi V., Jansen D., Dederen P.J., Veltien A., Hamans B., Liu Y., Heerschap A., Kiliaan A.J. Microvascular cerebral blood volume changes in aging APP(swe)/PS1 (dE9) AD mouse model: a voxel-wise approach. Brain Struct. Funct. 2013, 10.1007/s00429-012-0448-8.
101. Zerbi V., Kleinnijenhuis M., Fang X., Jansen D., Veltien A., Van Asten J., Timmer N., Dederen P.J., Kiliaan A.J., Heerschap A. Gray and white matter degeneration revealed by diffusion in an Alzheimer mouse model. Neurobiol. Aging 2013, 34:1440-1450. 10.1016/j.neurobiolaging.2012.11.017.
102. Zheng B., Lee P.T., Golay X. High-sensitivity cerebral perfusion mapping in mice by kbGRASE-FAIR at 9.4 T. NMR Biomed. 2010, 23:1061-1070. 10.1002/nbm.1533.
103. Zwiers M.P. Patching cardiac and head motion artefacts in diffusion-weighted images. NeuroImage 2010, 53:565-575. 10.1016/j.neuroimage.2010.06.014.