Impact of fatty acids on brain circulation, structure and function

https://doi.org/10.1016/j.plefa.2014.01.002Get rights and content

Abstract

The use of dietary intervention has evolved into a promising approach to prevent the onset and progression of brain diseases. The positive relationship between intake of omega-3 long chain polyunsaturated fatty acids (ω3-LCPUFAs) and decreased onset of disease- and aging-related deterioration of brain health is increasingly endorsed across epidemiological and diet-interventional studies. Promising results are found regarding to the protection of proper brain circulation, structure and functionality in healthy and diseased humans and animal models. These include enhanced cerebral blood flow (CBF), white and gray matter integrity, and improved cognitive functioning, and are possibly mediated through increased neurovascular coupling, neuroprotection and neuronal plasticity, respectively. Contrary, studies investigating diets high in saturated fats provide opposite results, which may eventually lead to irreversible damage. Studies like these are of great importance given the high incidence of obesity caused by the increased and decreased consumption of respectively saturated fats and ω3-LCPUFAs in the Western civilization. This paper will review in vivo research conducted on the effects of ω3-LCPUFAs and saturated fatty acids on integrity (circulation, structure and function) of the young, aging and diseased brain.

Introduction

Paleontological studies have shown that feeding habits played a crucial role in the development of the human brain [1]. Differences in diet among primates affected survival rate and the ability to reproduce, which are both related to brain size and cognitive functioning [2]. It is now known that brain size increased with the development of skills that required proper cognition, such as cooking and access to food and this led to the formation of the modern brain as we know now [3]. An evident example of diet effects on the brain was observed when comparing encephalisation (increasing brain/body-mass ratio) of hominids (early humans) living close to the shore with that of hominids living in-land [4]. A shore-based diet, which included high consumption of fish, led to extensive encephalisation in this population. This is probably related to the higher consumption of omega-3 fatty acids like docosahexaenoic acid (DHA; 22:6n−3) in this shore-based diet, as DHA is an important brain constituent present in cell membranes but cannot be synthesized efficiently by the human body itself.

When we analyze the situation now-a-days, a similar comparison can be made: with on one side a ‘Mediterranean-type diet’ and on the other side a ‘Western-type diet’. The conception of a Mediterranean-type diet (which is rich in long-chain polyunsaturated fatty acids) is derived from the combination of high intake of fruits, vegetables, nuts, cereals, olives and olive oil and more fish; less milk but more cheese; less meat; and moderate amounts of wine [5]. On the other hand, a Western-type diet is the result of increased saturated and trans fatty acids consumption due to introduction of food staples and food-processing procedures after the Industrial Revolution [6]. This difference in diet is reflected in an increased death rate caused by cancer and heart disease in the United States compared to Crete, which are characterized by consuming a Western-type diet and Mediterranean-type diet, respectively [7]. Outcome of cancer and heart disease is clearly affected by different diets and their effect on the cardiovascular system [8]. Cardiovascular risk factors are considered important risk factors for the onset of neurological diseases such as stroke and Alzheimer′s Disease (AD). The focus of this review will be on the effects of dietary components on the brain as there is abundant data available revealing the effects of specific diet components on brain health and mental functioning [9]. For example, high serum cholesterol levels, possibly via dietary intake of high saturated fat, in midlife increases the risk of AD in later life while a diet low in saturated fat like the Mediterranean diet is inversely related to this [10], [11]. Several groups tested the possibilities to slow down the progression of diseases like AD with nutrition-based intervention in animals and humans. Experimental data revealing the influence of diet components on three important indicators of brain health: (1) circulation, (2) structure and (3) function, will be highlighted in the present review. In this context, we will mainly emphasize the effects of omega-3 long-chain polyunsaturated fatty acids (ω3-LCPUFAs) on these aspects and compare this with the evidence found concerning the intake of saturated fatty acids. Obtaining more knowledge concerning the aftermaths of malnutrition on the brain is necessary since diseases like obesity, metabolic syndrome and diabetes gain prevalence in modern society.

Section snippets

Circulation

Due to high demands of energy by the brain and its low capacity to store this energy, the brain is the most highly perfused part of the human body [12]. Proper functioning, including adequate cerebral blood flow (CBF) and vessel reactivity, is necessary to ensure the microenvironment in which brain cells function efficiently. The importance of proper cerebral circulation is reflected in cerebrovascular and neurodegenerative diseases such as atherosclerosis, stroke and AD. Higher cerebral

Structure

The hypothesis that diet-induced changes on cerebral circulation may be linked to changes in brain structure is strengthened by a recent study of Chen et al. (2013). They showed a significant relationship between cortical CBF (using arterial spin labeling) and subcortical white-matter integrity (assessed by diffusion tensor imaging; DTI) in healthy human participants [51]. Since diet clearly affects cerebral blood flow based on the data reviewed earlier, potential diet effects are also expected

Function

Cognitive decline is a widely accepted phenomenon associated with normative aging and presumably caused by structural changes in the brain. Structural impairment of the brain, and especially white matter loss and dis-integrity, is significantly associated with poor brain functioning (i.e. cognitive performance). High FA values, and thus proper (white matter) connectivity between brain regions, are most often correlated with high levels of task performance [83], [84], [85], [86]. However, in

Conclusion

The awareness of food necessity has evolved from the simple means of providing energy and building material to the body into a potential therapeutic mediator to prevent and protect the body against the onset and progression of diseases. An increasing amount of studies demonstrated the beneficial and detrimental effects of distinct dietary components on the healthy and diseased brain. Within this framework, this review highlights important data regarding the effects of ω3-LCPUFAs and saturated

Acknowledgments

The research leading to these results has received funding from the European Community′s Seventh Framework Programme (FP7/2007-2013) under Grant agreement no. 211696.

References (147)

  • G.A. Bray et al.

    Dietary fat intake does affect obesity!

    Am. J. Clin. Nutr.

    (1998)
  • D. Parra et al.

    A diet rich in long chain omega-3 fatty acids modulates satiety in overweight and obese volunteers during weight loss

    Appetite

    (2008)
  • J.C. Umhau et al.

    Imaging incorporation of circulating docosahexaenoic acid into the human brain using positron emission tomography

    J. Lipid Res.

    (2009)
  • H. Tsukada et al.

    Regulation of cerebral blood flow response to somatosensory stimulation through the cholinergic system: a positron emission tomography study in unanesthetized monkeys

    Brain Res.

    (1997)
  • M. Minami et al.

    Dietary docosahexaenoic acid increases cerebral acetylcholine levels and improves passive avoidance performance in stroke-prone spontaneously hypertensive rats

    Pharmacol. Biochem. Behav.

    (1997)
  • S.E. Kanoski et al.

    Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity

    Physiol. Behav.

    (2011)
  • P. Li et al.

    Dietary supplementation with cholesterol and docosahexaenoic acid increases the activity of the arginine-nitric oxide pathway in tissues of young pigs

    Nitric Oxide: Biol. Chem./Off. J. Nitric Oxide Soc.

    (2008)
  • L.A. Horrocks et al.

    Docosahexaenoic acid in the diet: its importance in maintenance and restoration of neural membrane function

    Prostaglandins. Leukot. Essent. Fatty Acids

    (2004)
  • P.J. Basser et al.

    MR diffusion tensor spectroscopy and imaging

    Biophys. J.

    (1994)
  • A.L. Alexander et al.

    Diffusion tensor imaging of the brain

    Neurother.: J. Am. Soc. Exp. NeuroTher.

    (2007)
  • H. Hanyu et al.

    Diffusion-weighted MR imaging of the hippocampus and temporal white matter in Alzheimer′s disease

    J. Neurol. Sci.

    (1998)
  • V. Zerbi et al.

    Gray and white matter degeneration revealed by diffusion in an Alzheimer mouse model

    Neurobiol. Aging

    (2013)
  • S.K. Song et al.

    Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition

    Neurobiol. Dis.

    (2004)
  • D.H. Salat et al.

    Age-related alterations in white matter microstructure measured by diffusion tensor imaging

    Neurobiol. Aging

    (2005)
  • S.M. Conklin et al.

    Long-chain omega-3 fatty acid intake is associated positively with corticolimbic gray matter volume in healthy adults

    Neurosci. Lett.

    (2007)
  • F. Calon et al.

    Docosahexaenoic acid protects from dendritic pathology in an Alzheimer’s disease mouse model

    Neuron

    (2004)
  • C. Heurteaux et al.

    Alpha-linolenic acid and riluzole treatment confer cerebral protection and improve survival after focal brain ischemia

    Neuroscience

    (2006)
  • S.K. Orr et al.

    n-3 Polyunsaturated fatty acids in animal models with neuroinflammation

    Prostaglandins. Leukot. Essent. Fatty. Acids.

    (2013)
  • G.P. Eckert et al.

    Omega-3 fatty acids in neurodegenerative diseases: focus on mitochondria

    Prostaglandins. Leukot. Essent. Fatty. Acids.

    (2013)
  • D.J. Madden et al.

    Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time

    NeuroImage

    (2004)
  • T. Schmidt-Wilcke et al.

    Memory performance correlates with gray matter density in the ento-/perirhinal cortex and posterior hippocampus in patients with mild cognitive impairment and healthy controls--a voxel based morphometry study

    NeuroImage

    (2009)
  • J.C. McCann et al.

    Is docosahexaenoic acid, an n-3 long-chain polyunsaturated fatty acid, required for development of normal brain function? An overview of evidence from cognitive and behavioral tests in humans and animals

    Am. J. Clin. Nutr.

    (2005)
  • B.M. van Gelder et al.

    Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: the Zutphen Elderly Study

    Am. J. Clin. Nutr.

    (2007)
  • H. Francis et al.

    The longer-term impacts of Western diet on human cognition and the brain

    Appetite

    (2013)
  • R.K. McNamara et al.

    Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study

    Am. J. Clin. Nutr.

    (2010)
  • M.F. Muldoon et al.

    Serum phospholipid docosahexaenonic acid is associated with cognitive functioning during middle adulthood

    J. Nutr.

    (2010)
  • M.E. Thompson et al.

    Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda

    Am. J. Phys. Anthropol.

    (2008)
  • A. Gibbons

    Paleoanthropology. Food for thought

    Science

    (2007)
  • M.A. Crawford et al.

    Evidence for the unique function of docosahexaenoic acid during the evolution of the modern hominid brain

    Lipids

    (1999)
  • A.P. Simopoulos

    What is so special about the diet of Greece? The scientific evidence

    World Rev. Nutr. Diet.

    (2005)
  • G.H. Soule et al.

    Crete, a Case Study of an Underdeveloped Area, by Leland G. Allbaugh,... With the Editorial Assistance of George Soule. [Foreword by Chester I. Barnard.], N.J.

    (1953)
  • F. Gomez-Pinilla

    Brain foods: the effects of nutrients on brain function, Nature reviews

    Neuroscience

    (2008)
  • M. Kivipelto et al.

    Midlife vascular risk factors and Alzheimer′s disease in later life: longitudinal, population based study

    Br. Med. J.

    (2001)
  • M.H. Laitinen et al.

    Fat intake at midlife and risk of dementia and Alzheimer′s disease: a population-based study

    Dement. Geriatr. Cogn. Disord.

    (2006)
  • R.A. Haast et al.

    Sex differences in stroke

    J. Cereb. Blood Flow Metab.: Off. J. Int. Soc. Cereb. Blood Flow Metab.

    (2012)
  • J.C. de la Torre

    Alzheimer disease as a vascular disorder: nosological evidence

    Stroke

    (2002)
  • E. Vicenzini et al.

    Cerebrovascular reactivity in degenerative and vascular dementia: a transcranial Doppler study

    Eur. Neurol.

    (2007)
  • V. Zerbi et al.

    Microvascular cerebral blood volume changes in aging APPswe/PS1 dE9 AD mouse model: a voxel-wise approach

    Brain Struct. Funct.

    (2013)
  • V. Zerbi, D. Jansen, M. Wiesmann, X. Fang, L.M. Broersen, A. Veltien, A. Heerschap, A.J. Kiliaan, Multi-nutrient diets...
  • L.V. d’Uscio et al.

    Mechanism of endothelial dysfunction in apolipoprotein E-deficient mice

    Arterioscler. Thromb. Vasc. Biol.

    (2001)
  • Cited by (57)

    • Dietary patterns, cognitive function, and structural neuroimaging measures of brain aging

      2020, Experimental Gerontology
      Citation Excerpt :

      The Mediterranean diet pyramid (Willett et al., 1995) recommends infrequent consumption of red meat (<2 servings a week), considered a detrimental component in the calculation of a ‘Medi’ score. Red meat is high in saturated fats and trans fatty acids which are known to adversely impact the central nervous system pathways involved in neuroprotection and neuronal plasticity, which may eventually lead to irreversible damage (Haast and Kiliaan, 2015). Studies have found a direct association of saturated fat intake with incidence of cognitive decline (Okereke et al., 2012) and vascular changes leading to white matter damage (Wang et al., 2016).

    View all citing articles on Scopus
    View full text