A Review of the Association Between Dietary Intake and Brain Iron Levels in Older Adults: Preliminary Findings and Future Directions
Abstract
:1. Introduction
2. Scope of Review
3. Nutrition and Brain Iron: Insights from Neuroimaging Research
4. Conclusions from the Neuroimaging Findings
5. Proposed Future Directions
Author Contributions
Funding
Conflicts of Interest
References
- Raz, N.; Daugherty, A.M. Pathways to Brain Aging and Their Modifiers: Free-Radical-Induced Energetic and Neural Decline in Senescence (FRIENDS) Model—A Mini-Review. Gerontology 2018, 64, 49–57. [Google Scholar] [CrossRef] [PubMed]
- Todorich, B.; Pasquini, J.M.; Garcia, C.I.; Paez, P.M.; Connor, J.R. Oligodendrocytes and myelination: The role of iron. Glia 2009, 57, 467–478. [Google Scholar] [CrossRef] [PubMed]
- Mills, E.; Dong, X.-P.; Wang, F.; Xu, H. Mechanisms of brain iron transport: Insight into neurodegeneration and CNS disorders. Futur. Med. Chem. 2010, 2, 51–64. [Google Scholar] [CrossRef] [PubMed]
- Muñoz, P.; Humeres, A. Iron deficiency on neuronal function. BioMetals 2012, 25, 825–835. [Google Scholar] [CrossRef] [PubMed]
- Chakravarti, B.; Chakravarti, D.N. Oxidative Modification of Proteins: Age-Related Changes. Gerontology 2007, 53, 128–139. [Google Scholar] [CrossRef]
- Ward, R.J.; Zucca, F.A.; Duyn, J.H.; Crichton, R.R.; Zecca, L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014, 13, 1045–1060. [Google Scholar] [CrossRef]
- Martin, W.R.W.; Ye, F.Q.; Allen, P.S. Increasing striatal iron content associated with normal aging. Mov. Disord. 1998, 13, 281–286. [Google Scholar] [CrossRef]
- Zecca, L.; Youdim, M.B.H.; Riederer, P.; Connor, J.R.; Crichton, R.R. Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 2004, 5, 863–873. [Google Scholar] [CrossRef]
- Ke, Y.; Qian, Z.M. Brain iron metabolism: Neurobiology and neurochemistry. Prog. Neurobiol. 2007, 83, 149–173. [Google Scholar] [CrossRef]
- Daugherty, A.M.; Haacke, E.M.; Raz, N. Striatal iron content predicts its shrinkage and changes in verbal working memory after two years in healthy adults. J. Neurosci. 2015, 35, 6731–6743. [Google Scholar] [CrossRef]
- Daugherty, A.M.; Raz, N. Accumulation of iron in the putamen predicts its shrinkage in healthy older adults: A multi-occasion longitudinal study. NeuroImage 2016, 128, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Butterfield, D.A.; Halliwell, B. Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nat. Rev. Neurosci. 2019, 20, 148–160. [Google Scholar] [CrossRef]
- Hentze, M.W.; Muckenthaler, M.U.; Andrews, N.C. Balancing Acts: Molecular Control of Mammalian Iron Metabolism. Cell 2004, 117, 285–297. [Google Scholar] [CrossRef]
- Moos, T.; Nielsen, T.R.; Skjørringe, T.; Morgan, E.H. Iron trafficking inside the brain. J. Neurochem. 2007, 103, 1730–1740. [Google Scholar] [CrossRef] [PubMed]
- Hallgren, B.; Sourander, P. The effect of age on the non-haemin iron in the human brain. J. Neurochem. 1958, 3, 41–51. [Google Scholar] [CrossRef] [PubMed]
- Hayflick, S.J.; Kurian, M.A.; Hogarth, P. Neurodegeneration with brain iron accumulation. Handb. Clin. Neurol. 2018, 147, 293. [Google Scholar] [CrossRef]
- Spence, H.; McNeil, C.J.; Waiter, G.D. The impact of brain iron accumulation on cognition: A systematic review. PLoS ONE 2020, 15, e0240697. [Google Scholar] [CrossRef]
- Penke, L.; Hernandéz, M.C.V.; Maniega, S.M.; Gow, A.J.; Murray, C.; Starr, J.M.; Bastin, M.E.; Deary, I.J.; Wardlaw, J.M. Brain iron deposits are associated with general cognitive ability and cognitive aging. Neurobiol. Aging 2012, 33, 510–517.e2. [Google Scholar] [CrossRef]
- Gustavsson, J.; Papenberg, G.; Falahati, F.; Laukka, E.J.; Kalpouzos, G. Contributions of the Catechol-O-Methyltransferase Val158Met Polymorphism to Changes in Brain Iron Across Adulthood and Their Relationships to Working Memory. Front. Hum. Neurosci. 2022, 16, 838228. [Google Scholar] [CrossRef]
- Li, J.; Zhang, Q.; Che, Y.; Zhang, N.; Guo, L. Iron Deposition Characteristics of Deep Gray Matter in Elderly Individuals in the Community Revealed by Quantitative Susceptibility Mapping and Multiple Factor Analysis. Front. Aging Neurosci. 2021, 13, 611891. [Google Scholar] [CrossRef]
- Zachariou, V.; Bauer, C.E.; Seago, E.R.; Raslau, F.D.; Powell, D.K.; Gold, B.T. Cortical iron disrupts functional connectivity networks supporting working memory performance in older adults. NeuroImage 2020, 223, 117309. [Google Scholar] [CrossRef] [PubMed]
- Zachariou, V.; Bauer, C.E.; Pappas, C.; Gold, B.T. High cortical iron is associated with the disruption of white matter tracts supporting cognitive function in healthy older adults. Cereb. Cortex 2022, 33, 4815–4828. [Google Scholar] [CrossRef] [PubMed]
- Zachariou, V.; Bauer, C.E.; Seago, E.R.; Panayiotou, G.; Hall, E.D.; Butterfield, D.A.; Gold, B.T. Healthy dietary intake moderates the effects of age on brain iron concentration and working memory performance. Neurobiol. Aging 2021, 106, 183–196. [Google Scholar] [CrossRef] [PubMed]
- Gustavsson, J.; Ištvánfyová, Z.; Papenberg, G.; Falahati, F.; Laukka, E.J.; Lehtisalo, J.; Mangialasche, F.; Kalpouzos, G. Lifestyle, biological, and genetic factors related to brain iron accumulation across adulthood. Neurobiol. Aging 2024, 144, 56–67. [Google Scholar] [CrossRef]
- Hagemeier, J.; Tong, O.; Dwyer, M.G.; Schweser, F.; Ramanathan, M.; Zivadinov, R. Effects of diet on brain iron levels among healthy individuals: An MRI pilot study. Neurobiol. Aging 2015, 36, 1678–1685. [Google Scholar] [CrossRef]
- Zachariou, V.; Pappas, C.; Bauer, C.E.; Seago, E.R.; Gold, B.T. Exploring the links among brain iron accumulation, cognitive performance, and dietary intake in older adults: A longitudinal MRI study. Neurobiol. Aging 2024, 145, 1–12. [Google Scholar] [CrossRef]
- Dolic, K.; Weinstock-Guttman, B.; Marr, K.; Valnarov, V.; Carl, E.; Hagemeier, J.; Brooks, C.; Kilanowski, C.; Hojnacki, D.; Ramanathan, M.; et al. Risk Factors for Chronic Cerebrospinal Venous Insufficiency (CCSVI) in a Large Cohort of Volunteers. PLoS ONE 2011, 6, e28062. [Google Scholar] [CrossRef]
- Langkammer, C.; Schweser, F.; Krebs, N.; Deistung, A.; Goessler, W.; Scheurer, E.; Sommer, K.; Reishofer, G.; Yen, K.; Fazekas, F.; et al. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. NeuroImage 2012, 62, 1593–1599. [Google Scholar] [CrossRef]
- Haacke, E.M.; Makki, M.; Ge, Y.; Maheshwari, M.; Sehgal, V.; Hu, J.; Selvan, M.; Wu, Z.; Latif, Z.; Xuan, Y.; et al. Characterizing iron deposition in multiple sclerosis lesions using susceptibility weighted imaging. J. Magn. Reson. Imaging 2009, 29, 537–544. [Google Scholar] [CrossRef]
- Schweser, F.; Deistung, A.; Lehr, B.W.; Reichenbach, J.R. Quantitative imaging of intrinsic magnetic tissue properties using MRI signal phase: An approach to in vivo brain iron metabolism? NeuroImage 2011, 54, 2789–2807. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, T. Quantitative susceptibility mapping (QSM): Decoding MRI data for a tissue magnetic biomarker. Magn. Reson. Med. 2015, 73, 82–101. [Google Scholar] [CrossRef] [PubMed]
- Haacke, E.M.; Liu, S.; Buch, S.; Zheng, W.; Wu, D.; Ye, Y. Quantitative susceptibility mapping: Current status and future directions. Magn. Reson. Imaging 2015, 33, 1–25. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Chang, S.; Liu, T.; Wang, Q.; Cui, D.; Chen, X.; Jin, M.; Wang, B.; Pei, M.; Wisnieff, C.; et al. Reducing the object orientation dependence of susceptibility effects in gradient echo MRI through quantitative susceptibility mapping. Magn. Reson. Med. 2012, 68, 1563–1569. [Google Scholar] [CrossRef] [PubMed]
- Larsen, B.; Bourque, J.; Moore, T.M.; Adebimpe, A.; Calkins, M.E.; Elliott, M.A.; Gur, R.C.; Gur, R.E.; Moberg, P.J.; Roalf, D.R.; et al. Longitudinal Development of Brain Iron Is Linked to Cognition in Youth. J. Neurosci. 2020, 40, 1810–1818. [Google Scholar] [CrossRef] [PubMed]
- House, M.J.; Pierre, T.G.S.; Milward, E.A.; Bruce, D.G.; Olynyk, J.K. Relationship between brain R2 and liver and serum Iron concentrations in elderly men. Magn. Reson. Med. 2010, 63, 275–281. [Google Scholar] [CrossRef]
- Satia, J.A.; Watters, J.L.; Galanko, J.A. Validation of an antioxidant nutrient questionnaire in whites and African Americans. J. Am. Diet. Assoc. 2009, 109, 502–508.e6. [Google Scholar] [CrossRef]
- Ogłuszka, M.; Lipiński, P.; Starzyński, R.R. Interaction between iron and omega-3 fatty acids metabolisms: Where is the cross-link? Crit. Rev. Food Sci. Nutr. 2020, 62, 3002–3022. [Google Scholar] [CrossRef]
- Dixon, S.J.; Lemberg, K.M.; Lamprecht, M.R.; Skouta, R.; Zaitsev, E.M.; Gleason, C.E.; Patel, D.N.; Bauer, A.J.; Cantley, A.M.; Yang, W.S.; et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012, 149, 1060–1072. [Google Scholar] [CrossRef]
- Liu, T.; Liu, J.; de Rochefort, L.; Spincemaille, P.; Khalidov, I.; Ledoux, J.R.; Wang, Y. Morphology enabled dipole inversion (MEDI) from a single-angle acquisition: Comparison with COSMOS in human brain imaging. Magn. Reson. Med. 2011, 66, 777–783. [Google Scholar] [CrossRef]
- Liu, C.; Li, W.; Tong, K.A.; Yeom, K.W.; Kuzminski, S. Susceptibility-weighted imaging and quantitative susceptibility mapping in the brain. J. Magn. Reson. Imaging 2015, 42, 23–41. [Google Scholar] [CrossRef]
- Wang, Y.; Spincemaille, P.; Liu, Z.; Dimov, A.; Deh, K.; Li, J.; Zhang, Y.; Yao, Y.; Gillen, K.M.; Wilman, A.H.; et al. Clinical quantitative susceptibility mapping (QSM): Biometal imaging and its emerging roles in patient care. J. Magn. Reson. Imaging 2017, 46, 951–971. [Google Scholar] [CrossRef] [PubMed]
- Morris, M.C.; Tangney, C.C.; Wang, Y.; Sacks, F.M.; Barnes, L.L.; Bennett, D.A.; Aggarwal, N.T. MIND diet slows cognitive decline with aging. Alzheimer’s Dement. 2015, 11, 1015–1022. [Google Scholar] [CrossRef] [PubMed]
- Rodrigue, K.M.; Daugherty, A.M.; Foster, C.M.; Kennedy, K.M. Striatal iron content is linked to reduced fronto-striatal brain function under working memory load. Neuroimage 2020, 210, 116544. [Google Scholar] [CrossRef] [PubMed]
- Madden, D.J.; Merenstein, J.L. Quantitative susceptibility mapping of brain iron in healthy aging and cognition. NeuroImage 2023, 282, 120401. [Google Scholar] [CrossRef]
- Suh, J.H.; Moreau, R.; Heath, S.-H.D.; Hagen, T.M. Dietary supplementation with (R)-α-lipoic acid reverses the age-related accumulation of iron and depletion of antioxidants in the rat cerebral cortex. Redox Rep. 2005, 10, 52–60. [Google Scholar] [CrossRef]
- Ahmed, H.H. Modulatory effects of vitamin E, acetyl-l-carnitine and α-lipoic acid on new potential biomarkers for Alzheimer’s disease in rat model. Exp. Toxicol. Pathol. 2012, 64, 549–556. [Google Scholar] [CrossRef]
- Vela, D. Hepcidin, an emerging and important player in brain iron homeostasis. J. Transl. Med. 2018, 16, 25. [Google Scholar] [CrossRef]
- Hare, D.J.; Cardoso, B.R.; Raven, E.P.; Double, K.L.; Finkelstein, D.I.; Szymlek-Gay, E.A.; Biggs, B.-A. Excessive early-life dietary exposure: A potential source of elevated brain iron and a risk factor for Parkinson’s disease. NPJ Park. Dis. 2017, 3, 1. [Google Scholar] [CrossRef]
- Andersen, H.H.; Johnsen, K.B.; Moos, T. Iron deposits in the chronically inflamed central nervous system and contributes to neurodegeneration. Cell. Mol. Life Sci. 2014, 71, 1607–1622. [Google Scholar] [CrossRef]
- Kurowska, A.; Ziemichód, W.; Herbet, M.; Piątkowska-Chmiel, I. The Role of Diet as a Modulator of the Inflammatory Process in the Neurological Diseases. Nutrients 2023, 15, 1436. [Google Scholar] [CrossRef]
- Loughnan, R.; Ahern, J.; Tompkins, C.; Palmer, C.E.; Iversen, J.; Thompson, W.K.; Andreassen, O.; Jernigan, T.; Sugrue, L.; Dale, A.; et al. Association of Genetic Variant Linked to Hemochromatosis With Brain Magnetic Resonance Imaging Measures of Iron and Movement Disorders. JAMA Neurol. 2022, 79, 919–928. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zachariou, V.; Bauer, C.E.; Pappas, C.; Gold, B.T. A Review of the Association Between Dietary Intake and Brain Iron Levels in Older Adults: Preliminary Findings and Future Directions. Nutrients 2024, 16, 4193. https://doi.org/10.3390/nu16234193
Zachariou V, Bauer CE, Pappas C, Gold BT. A Review of the Association Between Dietary Intake and Brain Iron Levels in Older Adults: Preliminary Findings and Future Directions. Nutrients. 2024; 16(23):4193. https://doi.org/10.3390/nu16234193
Chicago/Turabian StyleZachariou, Valentinos, Christopher E. Bauer, Colleen Pappas, and Brian T. Gold. 2024. "A Review of the Association Between Dietary Intake and Brain Iron Levels in Older Adults: Preliminary Findings and Future Directions" Nutrients 16, no. 23: 4193. https://doi.org/10.3390/nu16234193
APA StyleZachariou, V., Bauer, C. E., Pappas, C., & Gold, B. T. (2024). A Review of the Association Between Dietary Intake and Brain Iron Levels in Older Adults: Preliminary Findings and Future Directions. Nutrients, 16(23), 4193. https://doi.org/10.3390/nu16234193