A Dietary Treatment Improves Cerebral Blood Flow and Brain Connectivity in Aging apoE4 Mice
Open accessAbstract
APOE ε 4 (apoE4) polymorphism is the main genetic determinant of sporadic Alzheimer’s disease (AD). A dietary approach (Fortasyn) including docosahexaenoic acid, eicosapentaenoic acid, uridine, choline, phospholipids, folic acid, vitamins B12, B6, C, and E, and selenium has been proposed for dietary management of AD. We hypothesize that the diet could inhibit AD-like pathologies in apoE4 mice, specifically cerebrovascular and connectivity impairment. Moreover, we evaluated the diet effect on cerebral blood flow (CBF), functional connectivity (FC), gray/white matter integrity, and postsynaptic density in aging apoE4 mice. At 10–12 months, apoE4 mice did not display prominent pathological differences compared to wild-type (WT) mice. However, 16–18-month-old apoE4 mice revealed reduced CBF and accelerated synaptic loss. The diet increased cortical CBF and amount of synapses and improved white matter integrity and FC in both aging apoE4 and WT mice. We demonstrated that protective mechanisms on vascular and synapse health are enhanced by Fortasyn, independent of apoE genotype. We further showed the efficacy of a multimodal translational approach, including advanced MR neuroimaging, to study dietary intervention on brain structure and function in aging.
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APOE4 has a negative impact on cerebral blood flow and neurovascular coupling; APOE4 mice show reduced cerebral blood flow both at baseline and in stimulus-evoked paradigms, relative to APOE3 mice.
“APOE4 has a negative impact on cerebral blood flow and neurovascular coupling; APOE4 mice show reduced cerebral blood flow both at baseline and in stimulus-evoked paradigms, relative to APOE3 mice187–189.”
From Multifaceted roles of APOE in Alzheimer disease (2024) · cites this paper as [189]
The Results (§3.2.1) report lower resting cerebral blood flow in the cortex and thalamus of 18-month-old apoE4 mice. But the controls were wild-type mice, not apoE3 mice; the Methods (§2.3) describe resting-condition measurements, not stimulus-evoked blood flow or neurovascular coupling. The Discussion (§4.1) also says cerebral blood flow was unaffected at 10–12 months. (LLM, conf=0.90)
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Cerebral blood flow regulation and neurovascular dysfunction in Alzheimer disease
Kisler, K., Nelson, A. R., Montagne, A., & Zlokovic, B. V. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.48 · Cited by 1,243 · see citing works
Cai, W., Zhang, K., Li, P., Zhu, L., Xu, J., Yang, B., Hu, X., Lu, Z., & Chen, J. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.09.006 · Cited by 288 · see citing works
Nutrition for the ageing brain: Towards evidence for an optimal diet
Vauzour, D., Camprubi-Robles, M., Miquel-Kergoat, S., Andres-Lacueva, C., Bánáti, D., Barberger-Gateau, P., Bowman, G. L., Caberlotto, L., Clarke, R., Hogervorst, E., et al. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2016.09.010 · Cited by 241 · see citing works
Self-citationCommon functional networks in the mouse brain revealed by multi-centre resting-state fMRI analysis
Grandjean, J., Canella, C., Anckaerts, C., Ayrancı, G., Bougacha, S., Bienert, T., Buehlmann, D., Coletta, L., Gallino, D., Gass, N., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116278 · Cited by 221 · see citing works
Self-citationMultifaceted roles of APOE in Alzheimer disease
Jackson, R. J., Hyman, B. T., & Serrano-Pozo, A. (2024) · Nature Reviews Neurology · doi:10.1038/s41582-024-00988-2 · Cited by 193 · see citing works
Therapeutic approaches targeting Apolipoprotein E function in Alzheimer’s disease
Williams, T., Borchelt, D., & Chakrabarty, P. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-0358-9 · Cited by 166 · see citing works
Poor cognitive ageing: Vulnerabilities, mechanisms and the impact of nutritional interventions
Miquel, S., Champ, C., Day, J. E. L., Aarts, E., Bahr, B. A., Bakker, M. J., Bánáti, D., Calabrese, V., Cederholm, T., Cryan, J. F., et al. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.12.004 · Cited by 163 · see citing works
Gut-brain and brain-gut axis in Parkinson’s disease models: effects of a uridine and fish oil diet
Perez-Pardo, P., Dodiya, H. B., Broersen, L. M., Douna, H., van Wijk, N., Lopes da Silva, S., Garssen, J., Keshavarzian, A., & Kraneveld, A. D. (2018) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1294555 · Cited by 111 · see citing works
Self-citationGrimm, M. O. W., Michaelson, D. M., & Hartmann, T. (2017) · Journal of Lipid Research · doi:10.1194/jlr.r076331 · Cited by 110 · see citing works
Donofry, S. D., Stillman, C. M., & Erickson, K. I. (2019) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsz085 · Cited by 108 · see citing works
Köbe, T., Witte, A. V., Schnelle, A., Tesky, V. A., Pantel, J., Schuchardt, J. P., Hahn, A., Bohlken, J., Grittner, U., & Flöel, A. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00105 · Cited by 107 · see citing works
Sarne, Y., Toledano, R., Rachmany, L., Sasson, E., & Doron, R. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.09.025 · Cited by 81 · see citing works
Perez-Pardo, P., de Jong, E. M., Broersen, L. M., van Wijk, N., Attali, A., Garssen, J., & Kraneveld, A. D. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00057 · Cited by 74 · see citing works
Self-citationBetter diet quality relates to larger brain tissue volumes
Croll, P. H., Voortman, T., Ikram, M. A., Franco, O. H., Schoufour, J. D., Bos, D., & Vernooij, M. W. (2018) · Neurology · doi:10.1212/wnl.0000000000005691 · Cited by 78 · see citing works
APOE and Alzheimer’s Disease: Neuroimaging of Metabolic and Cerebrovascular Dysfunction
Brandon, J. A., Farmer, B. C., Williams, H. C., & Johnson, L. A. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00180 · Cited by 75 · see citing works
Gorges, M., Roselli, F., Müller, H.-P., Ludolph, A. C., Rasche, V., & Kassubek, J. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00200 · Cited by 76 · see citing works
[Metabolic difference between visceral fat and subcutaneous abdominal fat].
Björntorp, P. A. (2000) · PubMed · Cited by 60 · see citing works
A specific dietary intervention to restore brain structure and function after ischemic stroke
Wiesmann, M., Zinnhardt, B., Reinhardt, D., Eligehausen, S., Wachsmuth, L., Hermann, S., Dederen, P. J. W. C., Hellwich, M., Kuhlmann, M. T., Broersen, L. M., et al. (2017) · Theranostics · doi:10.7150/thno.17559 · Cited by 58 · see citing works
Self-citationJohnson, L. A., Torres, E. R., Weber Boutros, S., Patel, E., Akinyeke, T., Alkayed, N. J., & Raber, J. (2019) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17746186 · Cited by 56 · see citing works
Hypertension, cerebrovascular impairment, and cognitive decline in aged AβPP/PS1 mice
Wiesmann, M., Zerbi, V., Jansen, D., Lütjohann, D., Veltien, A. A., Heerschap, A., & Kiliaan, A. J. (2017) · Theranostics · doi:10.7150/thno.18509 · Cited by 52 · see citing works
Self-citationWeight Loss in Patients with Dementia: Considering the Potential Impact of Pharmacotherapy
Franx, B. A. A., Arnoldussen, I. A. C., Kiliaan, A. J., & Gustafson, D. (2017) · Drugs & Aging · doi:10.1007/s40266-017-0462-x · Cited by 53 · see citing works
Self-citationEffect of a multinutrient intervention after ischemic stroke in female C57Bl/6 mice
Wiesmann, M., Timmer, N., Zinnhardt, B., Reinhard, D., Eligehausen, S., Königs, A., Jeddi, H. B., Dederen, P. J. W. C., Jacobs, A. H., & Kiliaan, A. J. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14213 · Cited by 52 · see citing works
Self-citationThe application of lipidomics to biomarker research and pathomechanisms in Alzheimer's disease
Wong, M. W. K., Braidy, N., Poljak, A., & Sachdev, P. S. (2016) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000303 · Cited by 49 · see citing works
ApoE and cerebral insulin: Trafficking, receptors, and resistance
Rhea, E. M., Raber, J., & Banks, W. A. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104755 · Cited by 47 · see citing works
Wiesmann, M., Roelofs, M., Lugt, R. V. D., Heerschap, A., Kiliaan, A. J., & Claassen, J. A. H. R. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16667364 · Cited by 45 · see citing works
Self-citationCalahorra, J., Shenk, J. C., Wielenga, V. H., Verweij, V. G. M., Geenen, B., Dederen, P. J. W. C., Peinado, M. Á., Siles, E., Wiesmann, M., & Kiliaan, A. J. (2019) · Nutrients · doi:10.3390/nu11102430 · Cited by 45 · see citing works
Self-citationA multi‐hit hypothesis for an <i>APOE4</i> ‐dependent pathophysiological state
Steele, O. G., Stuart, A. C., Minkley, L., Shaw, K., Bonnar, O., Anderle, S., Penn, A. C., Rusted, J., Serpell, L., Hall, C., et al. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15685 · Cited by 44 · see citing works
Zinnhardt, B., Wiesmann, M., Honold, L., Barca, C., Schäfers, M. A., Kiliaan, A. J., & Jacobs, A. H. (2018) · Theranostics · doi:10.7150/thno.24128 · Cited by 44 · see citing works
Self-citationAdditive Effects of Levodopa and a Neurorestorative Diet in a Mouse Model of Parkinson’s Disease
Perez‐Pardo, P., Broersen, L. M., Kliest, T., van Wijk, N., Attali, A., Garssen, J., & Kraneveld, A. D. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00237 · Cited by 40 · see citing works
Self-citationNutritional status, brain network organization, and general intelligence
Zamroziewicz, M. K., Talukdar, M. T., Zwilling, C. E., & Barbey, A. K. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.08.043 · Cited by 39 · see citing works
Nock, T. G., Chouinard‐Watkins, R., & Plourde, M. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2017.07.004 · Cited by 37 · see citing works
Badea, A., Wu, W., Shuff, J., Wang, M. S., Anderson, R. J., Qi, Y. P., Johnson, G. A., Wilson, J. G., Koudoro, S., Garyfallidis, E., et al. (2019) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2019.00072 · Cited by 36 · see citing works
N-of-1 Clinical Trials in Nutritional Interventions Directed at Improving Cognitive Function
Soldevila‐Domenech, N., Boronat, A., Langohr, K., & de la Torre, R. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00110 · Cited by 27 · see citing works
A guide to using functional magnetic resonance imaging to study Alzheimer's disease in animal models
Asaad, M., & Lee, J. H. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.031724 · Cited by 26 · see citing works
Apolipoprotein E in Alzheimer’s Disease: Focus on Synaptic Function and Therapeutic Strategy
Qu, L., Xu, S., Lan, Z., Fang, S., Xu, Y., & Zhu, X. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04449-1 · Cited by 22 · see citing works
Kulkarni, P., Grant, S. E., Morrison, T. R., Cai, X., Iriah, S. C., Kristal, B. S., Honeycutt, J. A., Brenhouse, H. C., Hartner, J. C., Madularu, D., et al. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147030 · Cited by 19 · see citing works
Ordóñez‐Gutiérrez, L., Fabriàs, G., Casas, J., & Wandosell, F. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222010907 · Cited by 18 · see citing works
An appraisal of folates as key factors in cognition and ageing-related diseases
Craenen, K., Verslegers, M., Baatout, S., & Benotmane, M. A. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1549017 · Cited by 18 · see citing works
Wong, M. W. K., Braidy, N., Crawford, J., Pickford, R., Song, F., Mather, K. A., Attia, J., Brodaty, H., Sachdev, P. S., & Poljak, A. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190524 · Cited by 16 · see citing works
Neuroprotective effect of goat milk
Kaura, S., Parle, M., Insa, R., Yadav, B. S., & Sethi, N. (2022) · Small Ruminant Research · doi:10.1016/j.smallrumres.2022.106748 · Cited by 13 · see citing works
Otsuka, R., Nishita, Y., Nakamura, A., Kato, T., Ando, F., Shimokata, H., & Arai, H. (2022) · Preventive Medicine · doi:10.1016/j.ypmed.2022.107149 · Cited by 13 · see citing works
Vascular Function and Ion Channels in Alzheimer's Disease
Taylor, J. L., Baudel, M. A. S. M., Nieves‐Cintrón, M., & Navedo, M. F. (2024) · Microcirculation · doi:10.1111/micc.12881 · Cited by 13 · see citing works
Nieraad, H., de Bruin, N. M. W. J., Arne, O., Hofmann, M. C. J., Schmidt, M., Saito, T., Saido, T. C., Gurke, R., Schmidt, D., Till, U., et al. (2020) · Nutrients · doi:10.3390/nu12113248 · Cited by 13 · see citing works
Chen, H.-F., Lambers, H., Nagelmann, N., Sandbrink, M., Segelcke, D., Pogatzki-Zahn, E., Faber, C., & Pradier, B. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1187328 · Cited by 12 · see citing works
Secci, R., Hartmann, A., Walter, M., Grabe, H. J., der Auwera, S. V., Kowald, A., Palmer, D. H., Rimbach, G. H., Fuellen, G., & Barrantes, I. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1975638 · Cited by 11 · see citing works
Aging, Immunity, and Neuroinflammation: The Modulatory Potential of Nutrition
Benedetto, S. D., & Müller, L. (2019) · Springer eBooks · doi:10.1007/978-3-030-16073-9_14 · Cited by 11 · see citing works
van Straaten, E. C. W., de Waal, H., Lansbergen, M. M., Scheltens, P., Maestú, F., Nowak, R., Hillebrand, A., & Stam, C. J. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00161 · Cited by 10 · see citing works
Winter, S., Mahzarnia, A., Anderson, R. J., Han, Z. Y., Tremblay, J. T., Stout, J. A., Moon, H. S., Marcellino, D. J., Dunson, D. B., & Badea, A. (2024) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2024.110251 · Cited by 7 · see citing works
Role of Apolipoprotein E in the tangled mystery of pain
Dhillon, H., & Singh, S. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.02.033 · Cited by 7 · see citing works
de la Colina, A. N., Badji, A., Robitaille-Grou, M.-C., Gagnon, C., Boshkovski, T., Lamarre-Cliché, M., Joubert, S., Gauthier, C. J., Bherer, L., Cohen‐Adad, J., et al. (2021) · Hypertension · doi:10.1161/hypertensionaha.120.16124 · Cited by 6 · see citing works
Laing, K. K., Fialova, N., Wardlaw, J. M., & Montagne, A. (2026) · Alzheimer s Research & Therapy · doi:10.1186/s13195-026-02018-3 · Cited by 4 · see citing works
Aydin, B., & Cansev, M. (2025) · Pharmacological Reports · doi:10.1007/s43440-025-00788-5 · Cited by 3 · see citing works
Yu, J., Chen, T., Li, X., Chen, J., Wei, W., & Zhang, J. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1298385 · Cited by 4 · see citing works
APOE, Immune Factors, Sex, and Diet Interact to Shape Brain Networks in Mouse Models of AgingPreprint
Winter, S., Mahzarnia, A., Anderson, R. J., Han, Z. Y., Tremblay, J. T., Stout, J. A., Moon, H. S., Marcellino, D. J., Dunson, D. B., & Badea, A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.04.560954 · Cited by 3 · see citing works
Kurmi, S., Shirodkar, S., Parab, S. B., & Doshi, G. (2026) · Current Alzheimer Research · doi:10.2174/0115672050467997260323164241 · Cited by 1 · see citing works
Targeting the Gut-Brain axis in Parkinson's disease
Perez‐Pardo, P. (2017) · Utrecht University Repository (Utrecht University)
A role for nutrition in healthy brain aging
Zamroziewicz, M. K. (2017) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Alanko, V., Eroli, F., Végvári, Á., Solomon, A., Hartmann, T., Nilsson, P., Kivipelto, M., Maioli, S., & Matton, A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.23.614418
- Authors
- Wiesmann, M., Zerbi, V., Jansen, D., Haast, R., Lütjohann, D., Broersen, L. M., Heerschap, A., & Kiliaan, A. J.
- Affiliations
- Radboud University Medical Center (NL)
- University of Bonn (DE)
- Utrecht University (NL)
- Corresponding author
- Kiliaan, Amanda J.
- ORCID
- Venue
- Neural Plasticity
- Publisher
- Wiley
- Published
- 2016
- Volume
- 2016
- Pages
- 1-15
- ISSN
- 1687-5443 (ISSN-L)
- 2090-5904
- PMC
- PMC4806294
- OpenAlex
- W2301705290
- Cited by
- 60
- References
- 86
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 6 · 2023: 2 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 9 · 2018: 6 · 2017: 17 · 2016: 5
- FWCI
- 9.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Neural Plasticity (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Radboud Repository (Radboud University) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Funders
- European Community’s Seventh Framework Programme (211696, 91106021, 11528)
- NWO Investment (211696, 91106021, 11528)
- Internationale Stichting Alzheimer Onderzoek (211696, 91106021, 11528)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Keywords
- APOE ε4, Alzheimer's disease, dietary intervention, docosahexaenoic acid, eicosapentaenoic acid, cerebral blood flow, functional connectivity, white matter integrity, synaptic loss, postsynaptic density, aging, neurovascular unit
- MeSH terms
- Disks Large Homolog 4 Protein, Aging, Alzheimer Disease, Animals, Apolipoproteins E, Brain, Brain Mapping, Diet, Fatty Acids, Female, Magnetic Resonance Imaging, Male, Membrane Proteins, Mice, Inbred C57BL, Mice, Transgenic, Neural Pathways, Sterols, Mice, Guanylate Kinases, Apolipoprotein E4
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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