Western diet is associated with a smaller hippocampus: a longitudinal investigation

BMC Medicine

Peter Butterworth¹  Perminder Sachdev²  Kaarin J. Anstey¹  Nicolas Cherbuin¹  Felice N. Jacka³ 

[1] Centre for Research on Ageing, Health and Wellbeing, Research School of Population Health, The Australian National University, Canberra, Australia;Centre for Healthy Brain Ageing (CHeBA), School of Psychiatry, Faculty of Medicine, University of New South Wales, Sydney, Australia;Black Dog Institute, Sydney, Australia

关键词: Nutrition;    Neurogenesis;    Magnetic resonance imaging;    Diet;    Hippocampus;    Brain derived neurotrophic factor;   

Others  :  1224636
DOI  :  10.1186/s12916-015-0461-x

 received in 2015-05-13, accepted in 2015-08-25,  发布年份 2015

【 摘 要 】

Background

Recent meta-analyses confirm a relationship between diet quality and both depression and cognitive health in adults. While the biological pathways that underpin these relationships are likely multitudinous, extensive evidence from animal studies points to the involvement of the hippocampus. The aim of this study was to examine the association between dietary patterns and hippocampal volume in humans, and to assess whether diet was associated with differential rates of hippocampal atrophy over time.

Methods

Data were drawn from the Personality and Total Health Through Life Study and focused on a subsample of the cohort (n = 255) who were aged 60–64 years at baseline in 2001, completed a food frequency questionnaire, and underwent two magnetic resonance imaging scans approximately 4 years apart. Longitudinal generalized estimating equation linear regression models were used to assess the association between dietary factors and left and right hippocampal volumes over time.

Results

Every one standard deviation increase in healthy “prudent” dietary pattern was associated with a 45.7 mm ³(standard error 22.9 mm ³ ) larger left hippocampal volume, while higher consumption of an unhealthy “Western” dietary pattern was (independently) associated with a 52.6 mm ³(SE 26.6 mm ³ ) smaller left hippocampal volume. These relationships were independent of covariates including age, gender, education, labour-force status, depressive symptoms and medication, physical activity, smoking, hypertension and diabetes. While hippocampal volume declined over time, there was no evidence that dietary patterns influenced this decline. No relationships were observed between dietary patterns and right hippocampal volume.

Conclusions

Lower intakes of nutrient-dense foods and higher intakes of unhealthy foods are each independently associated with smaller left hippocampal volume. To our knowledge, this is the first human study to demonstrate associations between diet and hippocampal volume concordant with data previously observed in animal models.

【 授权许可】

   
2015 Jacka et al.

【 图 表 】

Fig. 1.

【 参考文献 】

• [1]Global status report on noncommunicable diseases 2010. WHO, Geneva; 2011.
• [2]Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML et al.. The global obesity pandemic: shaped by global drivers and local environments. Lancet. 2011; 378:804-14.
• [3]Adair LS, Popkin BM. Are child eating patterns being transformed globally? Obes Res. 2005; 13:1281-99.
• [4]Jacka FN, Sacks G, Berk M, Allender S. Food policies for mental and physical health. BMC Psychiatry. 2014; 14:132. BioMed Central Full Text
• [5]Sarris J, Logan AC, Akbaraly TS, Amminger GP, Balanzá-Martínez V, Freeman MP et al.. Nutritional medicine as mainstream in psychiatry. Lancet Psychiatry. 2015; 2:271-4.
• [6]Lai JS, Hiles S, Bisquera A, Hure AJ, McEvoy M, Attia J. A systematic review and meta-analysis of dietary patterns and depression in community-dwelling adults. Am J Clin Nutr. 2013; 99:181-97.
• [7]Psaltopoulou T, Sergentanis TN, Panagiotakos DB, Sergentanis IN, Kosti R, Scarmeas N. Mediterranean diet, stroke, cognitive impairment, and depression: a meta-analysis. Ann Neurol. 2013; 74:580-91.
• [8]Jacka F, Pasco J, Mykletun A, Williams L, Hodge A, O'Reilly S et al.. Association of Western and traditional diets with depression and anxiety in women. Am J Psychiatry. 2010; 167:305-11.
• [9]Jacka FN, Mykletun A, Berk M, Bjelland I, Tell GS. The association between habitual diet quality and the common mental disorders in community-dwelling adults: the Hordaland Health study. Psychosom Med. 2011; 73:483-90.
• [10]Jacka FN, Cherbuin N, Anstey KJ, Butterworth P. Dietary patterns and depressive symptoms over time: examining the relationships with socioeconomic position, health behaviours and cardiovascular risk. PLoS One. 2014; 9:e87657.
• [11]Berk M, Williams LJ, Jacka F, O'Neil A, Pasco JA, Moylan S et al.. So depression is an inflammatory disease, but where does the inflammation come from? BMC Med. 2013; 11:200.
• [12]Moylan S, Berk M, Dean OM, Samuni Y, Williams LJ, O'Neil A et al.. Oxidative & nitrosative stress in depression: Why so much stress? Neurosci Biobehav Rev. 2014; 45C:46-62.
• [13]Dash S, Clarke G, Berk M, Jacka FN. The gut microbiome and diet in psychiatry: focus on depression. Curr Opin Psychiatry. 2015; 28:1-6.
• [14]Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry. 2000; 57:925-35.
• [15]Das S, Basu A. Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res. 2008; 86:1199-208.
• [16]Dias GP, Cavegn N, Nix A, do Nascimento Bevilaqua MC, Stangl D, Zainuddin MS et al.. The role of dietary polyphenols on adult hippocampal neurogenesis: molecular mechanisms and behavioural effects on depression and anxiety. Oxid Med Cell Longev. 2012; 2012:541971.
• [17]Videbech P, Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry. 2004; 161:1957-66.
• [18]Malberg JE, Eisch AJ, Nestler EJ, Duman RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 2000; 20:9104-10.
• [19]Frodl T, Jager M, Smajstrlova I, Born C, Bottlender R, Palladino T et al.. Effect of hippocampal and amygdala volumes on clinical outcomes in major depression: a 3-year prospective magnetic resonance imaging study. J Psychiatry Neurosci. 2008; 33:423-30.
• [20]Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al.. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003; 301:805-9.
• [21]Sen S, Duman R, Sanacora G. Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol Psychiatry. 2008; 64:527-32.
• [22]Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience. 2002; 112:803-14.
• [23]Martire SI, Maniam J, South T, Holmes N, Westbrook RF, Morris MJ. Extended exposure to a palatable cafeteria diet alters gene expression in brain regions implicated in reward, and withdrawal from this diet alters gene expression in brain regions associated with stress. Behav Brain Res. 2014; 265:132-41.
• [24]Fotuhi M, Mohassel P, Yaffe K. Fish consumption, long-chain omega-3 fatty acids and risk of cognitive decline or Alzheimer disease: a complex association. Nat Clin Pract Neurol. 2009; 5:140-52.
• [25]Granzotto A, Zatta P. Resveratrol and Alzheimer’s disease: message in a bottle on red wine and cognition. Front Aging Neurosci. 2014; 6:95.
• [26]Zainuddin MS, Thuret S. Nutrition, adult hippocampal neurogenesis and mental health. Br Med Bull. 2012; 103:89-114.
• [27]Anstey KJ, Christensen H, Butterworth P, Easteal S, Mackinnon A, Jacomb T et al.. Cohort profile: the PATH through life project. Int J Epidemiol. 2012; 41:951-60.
• [28]Cherbuin N, Sachdev P, Anstey KJ. Higher normal fasting plasma glucose is associated with hippocampal atrophy: The PATH Study. Neurology. 2012; 79:1019-26.
• [29]Anstey KJ, Maller JJ, Meslin C, Christensen H, Jorm AF, Wen W et al.. Hippocampal and amygdalar volumes in relation to handedness in adults aged 60–64. Neuroreport. 2004; 15:2825-9.
• [30]Marmot MG, Smith GD, Stansfeld S, Patel C, North F, Head J et al.. Health inequalities among British civil servants: the Whitehall II study. Lancet. 1991; 337:1387-93.
• [31]Goldberg D, Bridges K, Duncan-Jones P, Grayson D. Detecting anxiety and depression in general medical settings. BMJ. 1988; 297:897-9.
• [32]Lassale C, Guilbert C, Keogh J, Syrette J, Lange K, Cox DN. Estimating food intakes in Australia: validation of the Commonwealth Scientific and Industrial Research Organisation (CSIRO) food frequency questionnaire against weighed dietary intakes. J Hum Nutr Diet. 2009; 22:559-66.
• [33]Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A et al.. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology. 1992; 42:1743-50.
• [34]Maller JJ, Anstey KJ, Reglade-Meslin C, Christensen H, Wen W, Sachdev P. Hippocampus and amygdala volumes in a random community-based sample of 60–64 year olds and their relationship to cognition. Psychiatry Res. 2007; 156:185-97.
• [35]Maller JJ, Reglade-Meslin C, Anstey KJ, Sachdev P. Sex and symmetry differences in hippocampal volumetrics: before and beyond the opening of the crus of the fornix. Hippocampus. 2006; 16:80-90.
• [36]Freesurfer 5.3 package. http://surfer. nmr.mgh.harvard.edu webcite
• [37]Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem. 2012; 98:25-32.
• [38]Wu A, Molteni R, Ying Z, Gomez-Pinilla F. A saturated-fat diet aggravates the outcome of traumatic brain injury on hippocampal plasticity and cognitive function by reducing brain-derived neurotrophic factor. Neuroscience. 2003; 119:365-75.
• [39]Beilharz JE, Maniam J, Morris MJ. Short exposure to a diet rich in both fat and sugar or sugar alone impairs place, but not object recognition memory in rats. Brain Behav Immun. 2014; 37:134-41.
• [40]Ross AP, Bartness TJ, Mielke JG, Parent MB. A high fructose diet impairs spatial memory in male rats. Neurobiol Learn Mem. 2009; 92:410-6.
• [41]Morrison CD, Pistell PJ, Ingram DK, Johnson WD, Liu Y, Fernandez-Kim SO et al.. High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J Neurochem. 2010; 114:1581-9.
• [42]Wu A, Ying Z, Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur J Neurosci. 2004; 19:1699-707.
• [43]Wu A, Ying Z, Gomez-Pinilla F. Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J Neurotrauma. 2004; 21:1457-67.
• [44]Lee S, Kim DH, Lee DH, Jeon SJ, Lee CH, Son KH et al.. Oroxylin A, a flavonoid, stimulates adult neurogenesis in the hippocampal dentate gyrus region of mice. Neurochem Res. 2010; 35:1725-32.
• [45]An L, Zhang YZ, Yu NJ, Liu XM, Zhao N, Yuan L et al.. The total flavonoids extracted from Xiaobuxin-Tang up-regulate the decreased hippocampal neurogenesis and neurotrophic molecules expression in chronically stressed rats. Prog Neuropsychopharmacol Biol Psychiatry. 2008; 32:1484-90.
• [46]Williams CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA et al.. Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med. 2008; 45:295-305.
• [47]Valente T, Hidalgo J, Bolea I, Ramirez B, Angles N, Reguant J et al.. A diet enriched in polyphenols and polyunsaturated fatty acids, LMN diet, induces neurogenesis in the subventricular zone and hippocampus of adult mouse brain. J Alzheimers Dis. 2009; 18:849-65.
• [48]Kawakita E, Hashimoto M, Shido O. Docosahexaenoic acid promotes neurogenesis in vitro and in vivo. Neuroscience. 2006; 139:991-7.
• [49]Albanes D, Heinonen OP, Huttunen JK, Taylor PR, Virtamo J, Edwards BK et al.. Effects of alpha-tocopherol and beta-carotene supplements on cancer incidence in the Alpha-Tocopherol Beta-Carotene Cancer Prevention Study. Am J Clin Nutr. 1995; 62:1427S-30S.
• [50]Guimaraes LR, Jacka FN, Gama CS, Berk M, Leitao-Azevedo CL, de Abreu MG B et al.. Serum levels of brain-derived neurotrophic factor in schizophrenia on a hypocaloric diet. Prog Neuropsychopharmacol Biol Psychiatry. 2008; 32:1595-8.
• [51]Edwards LM, Murray AJ, Holloway CJ, Carter EE, Kemp GJ, Codreanu I et al.. Short-term consumption of a high-fat diet impairs whole-body efficiency and cognitive function in sedentary men. FASEB J. 2011; 25:1088-96.
• [52]Cherbuin N, Anstey KJ. The Mediterranean diet is not related to cognitive change in a large prospective investigation: the PATH Through Life study. Am J Geriatr Psychiatry. 2012; 20:635-9.
• [53]Samieri C, Okereke OI, E Devore E, Grodstein F. Long-term adherence to the Mediterranean diet is associated with overall cognitive status, but not cognitive decline, in women. J Nutr. 2013; 143:493-9.
• [54]Scarmeas N, Stern Y, Tang MX, Mayeux R, Luchsinger JA. Mediterranean diet and risk for Alzheimer’s disease. Ann Neurol. 2006; 59:912-21.
• [55]Gardener S, Gu Y, Rainey-Smith SR, Keogh JB, Clifton PM, Mathieson SL et al.. Adherence to a Mediterranean diet and Alzheimer’s disease risk in an Australian population. Transl Psychiatry. 2012; 2:e164.
• [56]Thompson PM, Hayashi KM, Dutton RA, Chiang MC, Leow AD, Sowell ER et al.. Tracking Alzheimer’s disease. Ann N Y Acad Sci. 2007; 1097:183-214.
• [57]Shi F, Liu B, Zhou Y, Yu C, Jiang T. Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer’s disease: meta-analyses of MRI studies. Hippocampus. 2009; 19:1055-64.
• [58]Fraser MA, Shaw ME, Cherbuin N. A systematic review and meta-analysis of longitudinal hippocampal atrophy in healthy human ageing. Neuroimage. 2015; 112:364-74.
• [59]Giannakopoulos P, Kovari E, Herrmann FR, Hof PR, Bouras C. Interhemispheric distribution of Alzheimer disease and vascular pathology in brain aging. Stroke. 2009; 40:983-6.
• [60]O'Neil A, Quirk SE, Housden S, Brennan SL, Williams LJ, Pasco JA et al.. Relationship between diet and mental health in children and adolescents: a systematic review. Am J Public Health. 2014; 104:e31-42.