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Physical Activity and Amyloid-&Beta Molecular Psychiatry (2013) 18, 875 -- 881 & 2013 Macmillan Publishers Limited All rights reserved 1359-4184/13 www.nature.com/mp ORIGINAL ARTICLE Physical activity and amyloid-b plasma and brain levels: results from the Australian Imaging, Biomarkers and Lifestyle Study of Ageing BM Brown1,2,3, JJ Peiffer1,4, K Taddei1,3, JK Lui1,3, SM Laws1,3, VB Gupta1,3, T Taddei1,3, VK Ward1,2,3, MA Rodrigues1,3, S Burnham5, SR Rainey-Smith1,3, VL Villemagne6,7, A Bush6,8, KA Ellis6,9,10, CL Masters6,8, D Ames9,10, SL Macaulay11, C Szoeke11, CC Rowe7 and RN Martins,1,2,3, for the AIBL Research Group12 Previous studies suggest physical activity improves cognition and lowers Alzheimer’s disease (AD) risk. However, key AD pathogenic factors that are thought to be influenced by physical activity, particularly plasma amyloid-b (Ab) and Ab brain load, have yet to be thoroughly investigated. The objective of this study was to determine if plasma Ab and amyloid brain deposition are associated with physical activity levels, and whether these associations differed between carriers and non-carriers of the apolipoprotein E (APOE) e4 allele. Five-hundred and forty six cognitively intact participants (aged 60--95 years) from the Australian Imaging, Biomarkers and Lifestyle Study of Ageing (AIBL) were included in these analyses. Habitual physical activity levels were measured using the International Physical Activity Questionnaire (IPAQ). Serum insulin, glucose, cholesterol and plasma Ab levels were measured in fasting blood samples. A subgroup (n ¼ 116) underwent 11C-Pittsburgh compound B (PiB) positron emission tomography (PET) scanning to quantify brain amyloid load. Higher levels of physical activity were associated with higher high density lipoprotein (HDL) (P ¼ 0.037), and lower insulin (Po0.001), triglycerides (P ¼ 0.019) and Ab1À42/1À40 ratio (P ¼ 0.001). After stratification of the cohort based on APOE e4 allele carriage, it was evident that only non-carriers received the benefit of reduced plasma Ab from physical activity. Conversely, lower levels of PiB SUVR (standardised uptake value ratio) were observed in higher exercising APOE e4 carriers. Lower plasma Ab1À42/1À40 and brain amyloid was observed in those reporting higher levels of physical activity, consistent with the hypothesis that physical activity may be involved in the modulation of pathogenic changes associated with AD. Molecular Psychiatry (2013) 18, 875--881; doi:10.1038/mp.2012.107; published online 14 August 2012 Keywords: Alzheimer’s disease; amyloid-b; APOE allele; blood biomarkers; dementia; physical activity INTRODUCTION (Ab) levels in response to physical activity. In AD transgenic mice, Dementia currently affects 35 million people worldwide, with the physical activity has been shown to decrease brain amyloid load, majority of those individuals having Alzheimer’s disease (AD).1 as well as increasing levels of endopeptidase and neprilysin; 11,12 Currently, no cure is available; therefore, preventive strategies are enzymes that degrade Ab peptides. Moreover, a physical essential to reduce disease incidence. Delaying AD onset and activity intervention study in humans showed a trend towards progression by 1 year has the potential to reduce worldwide lower Ab1À42 levels in individuals who undertook aerobic exercise, incidence by 9 million cases.2 when compared with those carrying out a stretching regime.13 It is In animal models and human cohorts,3--7 the use of physical likely that factors associated with cardiovascular disease (CVD) activity has been shown to enhance cognitive functioning and may have a role in the mechanism that links physical activity to protect against dementia. Furthermore, positive associations have Ab. Risk of CVD is lowered by physical activity through the been observed between physical activity and an induction of modulation of selective biochemical changes, including alterations brain-derived neurotrophic factor, cerebral blood flow, neurogen- in high density lipoprotein (HDL), triglyceride and insulin esis and synaptic plasticity; thus, indicating a possible protective levels.14--16 It is believed that these biomarkers may have a role role for physical activity against age-related cognitive decline and in the over production and/or decreased clearance of Ab, and thus dementias, such as AD.8--10 provides insight into a potential mechanism for the association Another factor that may mediate the relationship between between physical activity and Ab.17,18 Furthermore carriers of the physical activity and brain health is the reduction of amyloid-b apolipoprotein E (APOE) e4 allele (a widely accepted genetic risk 1Centre of Excellence for Alzheimer’s Disease Research and Care, School of Medical Sciences, Edith Cowan University, Joondalup, WA, Australia; 2School of Psychiatry and Clinical Neurosciences, University of Western Australia, Perth, WA, Australia; 3Sir James McCusker Alzheimer’s Disease Research Unit (Hollywood Private Hospital), Perth, WA, Australia; 4School of Chiropractic and Sport Science, Murdoch University, Perth, WA, Australia; 5CSIRO, Mathematics, Informatics and Statistics, Floreat, WA, Australia; 6Mental Health Research Institute, The University of Melbourne, Parkville, VIC, Australia; 7Department of Nuclear Medicine, Centre for PET, Austin Health, Heidelberg, VIC, Australia; 8Centre for Neuroscience, The University of Melbourne, Parkville, VIC, Australia; 9National Ageing Research Institute, Parkville, VIC, Australia; 10Academic Unit for Psychiatry of Old Age, Department of Psychiatry, The University of Melbourne, St Vincent’s Aged Psychiatry Service, St George’s Hospital, Melbourne, VIC, Australia and 11CSIRO, Preventative Health Flagship, CMSE, Parkville, VIC, Australia. Correspondence: Professor RN Martins, School of Medical Sciences, Edith Cowan University, 270 Joondalup Dr, Joondalup, WA 6027, Australia. E-mail: [email protected] 12http://www.aibl.csiro.au Received 27 September 2011; revised 15 June 2012; accepted 26 June 2012; published online 14 August 2012 Physical activity and Ab plasma and brain levels BM Brown et al 876 19 factor for sporadic AD) have been shown to have both increased o5.5 mmol LÀ1), HDL cholesterol (normal range 41.0 mmol LÀ1), low density levels of CVD blood biomarkers and Ab, when compared with lipoprotein cholesterol (normal range o3.0 mmol LÀ1) and triglyceride 20--22 non-carriers of the e4 allele. (normal range o2.0 mmol LÀ1) levels were quantified using standard analysis Through the use of brain imaging techniques such as magnetic techniques at PathWest Laboratory Medicine WA, Western Australia and resonance imaging and positron emission tomography (PET), Melbourne Health, Victoria. emerging evidence suggests that physical activity is associated with brain structure.23,24 The radiotracer 11C-Pittsburgh compound B (PiB) in PET scanning is now the gold standard in amyloid Brain imaging load quantification.25 However, since PET scanning is not suitable Data from PET imaging using PiB were collected from 116 cognitively 22 for widespread screening of the population, other more accessible healthy participants, as described previously. Individuals were randomly methods are needed. One approach has been to measure selected from a pool of willing participants to undergo brain imaging. Briefly, PET images were acquired 40--70 min post PiB injection, from which levels of blood-based biomarkers, including plasma Ab1À42. This is an attractive option, as it has the potential to be used as a a PET standardised uptake value is calculated. From this, a standardised screening tool in the wider community, but requires validation uptake value ratio (SUVR) was calculated, using the cerebellar cortex as the 22 against PiB PET. reference region. The current study was designed to examine the effect of physical activity on biomarkers associated with the development Genotyping of AD in a large cohort of aged healthy men and women. More Frozen whole blood samples containing EDTA/Prostaglandin E1 were specifically, we aimed to investigate: (1) whether physical activity thawed then centrifuged to separate leucocytes. DNA was isolated from is associated with lower plasma Ab levels and brain amyloid load the leucocytes, and PCR amplification and restrictions enzyme digestions and (2) whether the presence of an apoE e4 allele results in a took place to determine APOE genotype.31 weaker association between physical activity and plasma Ab and brain amyloid. Measurement of physical activity Habitual physical activity levels were measured using the International MATERIALS AND METHODS Physical Activity Questionnaire (IPAQ).32 The IPAQ is a subjective measure The study cohort consisted of 546 cognitively healthy males and females that asks participants to recall their physical activity from the previous 7 from an initial cohort of 1112 individuals participating in the Australian days. The questionnaire is separated into four sections; and consists Imaging, Biomarkers and Lifestyle Study of Ageing (AIBL) Study.26 For of work activity, transportation activity, housework and leisure-time inclusion, participants were required to demonstrate normal cognitive activity. Each question was allocated a metabolic equivalent score function (as determined by a panel of expert clinicians after 2 h of (MET), based on the intensity of the activity being undertaken.32 The neuropsychological testing) and complete a physical activity questionnaire. MET scores were then multiplied by the number of minutes per Of the original 1112 individuals, 344 were not
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