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Daily Physical Activity Is Associated with Subcortical Brain Volume and Cognition in Heart Failure

Published online by Cambridge University Press:  19 November 2015

Michael L. Alosco ,
Adam M. Brickman ,
Mary Beth Spitznagel ,
Lawrence H. Sweet ,
Richard Josephson ,
Erica Y. Griffith ,
Atul Narkhede ,
Joel Hughes  and
John Gunstad
Michael L. Alosco
Affiliation:
Department of Psychological Sciences, Kent State University, Kent, Ohio
Adam M. Brickman
Affiliation:
Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Department of Neurology, College of Physicians and Surgeons, Columbia University, New York, New York
Mary Beth Spitznagel
Affiliation:
Department of Psychological Sciences, Kent State University, Kent, Ohio
Lawrence H. Sweet
Affiliation:
Department of Psychology, University of Georgia, Athens, Georgia
Richard Josephson
Affiliation:
University Hospitals Case Medical Center and Department of Medicine, Cleveland, Ohio Harrington Heart & Vascular Institute, Cleveland, Ohio Case Western Reserve University School of Medicine, Cleveland, Ohio
Erica Y. Griffith
Affiliation:
Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Department of Neurology, College of Physicians and Surgeons, Columbia University, New York, New York
Atul Narkhede
Affiliation:
Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Department of Neurology, College of Physicians and Surgeons, Columbia University, New York, New York
Joel Hughes
Affiliation:
Department of Psychological Sciences, Kent State University, Kent, Ohio
John Gunstad*
Affiliation:
Department of Psychological Sciences, Kent State University, Kent, Ohio
*
Correspondence and reprint requests to: John Gunstad, Department of Psychological Sciences, Kent State University, Kent, OH 44242. E-mail: [email protected]
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Abstract

Cognitive impairment in heart failure (HF) is believed to in part stem from structural brain alterations, including shrinkage of subcortical regions. Fortunately, neurocognitive dysfunction in HF can be mitigated by physical activity (PA), though mechanisms for this phenomenon are unclear. PA is protective against age-related cognitive decline that may involve improved structural integrity to brain regions sensitive to aging (e.g., subcortical structures). Yet, no study has examined the benefits of PA on the brain in HF and we sought to do so and clarify related cognitive implications. Fifty older adults with HF completed a neuropsychological battery and wore an accelerometer for 7 days. All participants underwent brain MRI. This study targeted subcortical brain volume given subcortical alterations are often observed in HF and the sensitivity of PA to subcortical structures in other patient populations. Participants averaged 4348.49 (SD=2092.08) steps per day and greater daily steps predicted better attention/executive function, episodic memory, and language abilities, p’s<.05. Medical and demographically adjusted regression analyses revealed higher daily steps per day predicted greater subcortical volume, with specific effects for the thalamus and ventral diencephalon, p’s<.05. Greater subcortical volume was associated with better attention/executive function, p<.05. Higher daily PA was associated with increased subcortical brain volume and better cognition in older adults with HF. Longitudinal work is needed to clarify whether daily PA can attenuate brain atrophy in HF to reduce accelerated cognitive decline in this population. (JINS, 2015, 21, 851–860)

Keywords

Physical activityHeart failureMRIBrain volumeCognitive functionAccelerometry
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 21 , Special Issue 10: Physical Activity and Brain Plasticity , November 2015 , pp. 851 - 860
Copyright
Copyright © The International Neuropsychological Society 2015 

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References

Acosta-Cabronero, J., & Nestor, P.J. (2014). Diffusion tensor imaging in Alzheimer’s disease: Insights into the limbic-diencephalic network and methodological considerations. Frontiers in Aging Neuroscience, 6, 266.CrossRefGoogle ScholarPubMed
Almeida, O.P., Beer, C., Lautenschlager, N.T., Arnolda, L., Alfonso, H., & Flicker, L. (2012). Two-year course of cognitive function and mood in adults with congestive heart failure and coronary artery disease: The Heart-Mind Study. International Psychogeriatrics, 24, 38–47.CrossRefGoogle ScholarPubMed
Alosco, M.L., Spitznagel, M.B., Miller, L., Raz, N., Cohen, R., Sweet, L.H., Colbert, L.H., Gunstad, J. (2012). Depression is associated with reduced physical activity in persons with heart failure. Health Psychology, 31, 754–762.CrossRefGoogle ScholarPubMed
Alosco, M.L., Spitznagel, M.B., Cohen, R., Sweet, L.H., Hayes, S.M., Josephson, R., Hughes, J., Gunstad, J. (2015). Decreases in daily physical activity predict acute decline in attention and executive function in heart failure. Journal of Cardiac Failure, 21, 339–346.CrossRefGoogle ScholarPubMed
Alosco, M.L., Spitznagel, M.B., Cohen, R., Sweet, L.H., Josephson, R., Hughes, J., Rosneck, J., … Gunstad, J. (2014). Cardiac rehabilitation is associated with lasting improvements in cognitive function in older adults with heart failure. Acta Cardiologica, 69, 407–414.CrossRefGoogle ScholarPubMed
Alosco, M.L., Brickman, A.M., Spitznagel, M.B., Griffith, E.Y., Narkhede, A., Raz, N., & Gunstad, J. (2013a). Poorer physical fitness is associated with reduced structural brain integrity in heart failure. Journal of the Neurological Sciences, 328, 51–57.CrossRefGoogle ScholarPubMed
Alosco, M.L., Brickman, A.M., Spitznagel, M.B., Griffith, E.Y., Narkhede, A., Raz, N., Cohen, R., … Gunstad, J. (2013b). The adverse impact of type 2 diabetes on brain volume in heart failure. Journal of Clinical and Experimental Neuropsychology, 35, 309–318.CrossRefGoogle ScholarPubMed
Alosco, M.L., Spitznagel, M.B., van Dulmen, M., Raz, N., Cohen, R., Sweet, L.H., & Gunstad, J. (2012). Cognitive function and treatment adherence in older adults with heart failure. Psychosomatic Medicine, 74, 965–973.CrossRefGoogle ScholarPubMed
Anazodo, U.C., Shoemaker, J.K., Suskin, N. St, & Lawrence, K.S. (2013). An investigation of changes in regional gray matter volume in cardiovascular disease patients, pre and post cardiovascular rehabilitation. Neuroimage: Clinical, 3, 388–395.CrossRefGoogle ScholarPubMed
Alwerdt, J., Edwards, J.D., Athilingam, P., O’Connor, M.L., & Valdes, E.G. (2013). Longitudinal differences in cognitive functioning among older adults with and without heart failure. Journal of Aging and Health, 25, 1358–1377.CrossRefGoogle ScholarPubMed
Athilingam, P., Moynihan, J., Chen, L., D’Aoust, R., Groer, K., & Kip, K. (2013). Elevated levels of interleukin 6 and C-reactive protein associated with cognitive impairment in heart failure. Congestive Heart Failure, 19, 92–98.CrossRefGoogle ScholarPubMed
Barnes, D.E., Blackwell, T., Stone, K.L., Goldman, S.E., Hillier, T., & Yaffe, K. (2008). Cognition in older women: The importance of daytime movement. Journal of the American Geriatrics Society, 56, 1658–1664.CrossRefGoogle ScholarPubMed
Brown, B.M., Peiffer, J.J., Sohrabi, H.R., Mondal, A., Gupta, V.B., & Rainey-Smith, S.R. (2012). Intense physical activity is associated with cognitive performance in the elderly. Translational Psychiatry, 2, e191.CrossRefGoogle ScholarPubMed
Buchman, A.S., Boyle, P.A., Yu, L., Shah, R.C., Wilson, R.S., & Bennett, D.A. (2012). Total daily physical activity and the risk of AD and cognitive decline in older adults. Neurology, 78, 1323–1329.CrossRefGoogle ScholarPubMed
Buchman, A.S., Wilson, R.S., & Bennett, D.A. (2008). Total daily activity is associated with cognition in older persons. American Journal of Geriatric Psychiatry, 16, 697–701.CrossRefGoogle ScholarPubMed
Delis, D., Kramer, J., Kaplan, E., & Ober, B. (2000). California Verbal Learning Test-second Edition: Adult version. Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Doi, T., Makizako, H., Shimada, H., Tsutsumimoto, K., Hotta, R., Nakaubo, S., & Suzuki, T. (2015). Objectively measured physical activity, brain atrophy, and white matter lesions in older adults with mild cognitive impairment. Experimental Gerontology, 62, 1–6.CrossRefGoogle ScholarPubMed
Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2000). The FAB: A frontal assessment battery at bedside. Neurology, 55, 1621–1626.CrossRefGoogle ScholarPubMed
Enzinger, C., Dawes, H., Johansen-Berg, H., Wade, D., Bogdanovic, M., Collett, J., & Matthews, P.M. (2009). Brain activity changes associated with treadmill training after stroke. Stroke, 40, 2460–2467.CrossRefGoogle ScholarPubMed
Erickson, K.I., Weinstein, A.M., & Lopez, O.L. (2012). Physical activity, brain plasticity, and Alzheimer’s disease. Archives of Medical Research, 43, 615–621.CrossRefGoogle ScholarPubMed
Erickson, K.I., Raji, C.A., Lopez, O.L., Becker, J.T., Rosano, C., Newman, A.B., & Kuller, L.H. (2010). Physical activity predicts gray matter volume in late adulthood: The Cardiovascular Health Study. Neurology, 75, 1415–1422.CrossRefGoogle ScholarPubMed
Farina, N., Tabet, N., & Rusted, J. (2014). Habitual physical activity (HPA) as a factor in sustained executive function in Alzheimer-type dementia: A cohort study. Archives of Gerontology and Geriatrics, 59, 91–97.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., & Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355.CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9, 195–207.CrossRefGoogle Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., & Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.CrossRefGoogle ScholarPubMed
Fulcher, K.K., Alosco, M.L., Miller, L., Spitznagel, M.B., Cohen, R., Raz, N., & Gunstad, J. (2014). Greater physical activity is associated with better cognitive function in heart failure. Health Psychology, 33, 1337–1343.CrossRefGoogle ScholarPubMed
Garcia, S., Spitznagel, M.B., Cohen, R., Raz, N., Sweet, L., Colbert, L., & Gunstad, J. (2011). Depression is associated with cognitive dysfunction in older adults with heart failure. Cardiovascular Psychiatry and Neurology, 2011, 368324.CrossRefGoogle ScholarPubMed
Gons, R.A., Tuladhar, A.M., de Laat, K.F., van Norden, A.G., van Dijk, E.J., Norris, D.G., & de Leeuw, F.E. (2013). Physical activity is related to the structural integrity of cerebral white matter. Neurology, 81, 971–976.CrossRefGoogle Scholar
Hayes, S.M., Hayes, J.P., Cadden, M., & Verfaellie, M. (2013). A review of cardiorespiratory fitness-related neuroplasticity in the aging brain. Frontiers in Aging Neuroscience, 5, 31.CrossRefGoogle ScholarPubMed
Hjelm, C., Dahl, A., Brostrom, A., Martensson, J., Johansson, B., & Stromberg, A. (2012). The influence of heart failure on longitudinal changes in cognition among individuals 80 years of age and older. Journal of Clinical Nursing, 7–8, 994–1003.CrossRefGoogle Scholar
Hunkin, N.M., Awad, M., & Mayes, A.R. (2015). Memory for between-list and within-list information in amnesic patients with temporal lobe and diencephalic lesions. Journal of Neuropsychology, 9, 137–156.CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). Boston Naming Test. Philadelphia: Lea & Febiger.Google Scholar
Kimura, K., Yasunage, A., & Wang, L.Q. (2013). Correlation between moderate daily physical activity and neurocognitive variability in healthy elderly people. Archives of Gerontology and Geriatrics, 56, 109–117.CrossRefGoogle ScholarPubMed
Klenk, J., Denkinger, M., Nikolaus, T., Peter, R., Rothenbacher, D., Koenig, W., & ActiFE Study Group (2013). Association of objectively measured physical activity with establish and novel cardiovascular biomarkers in elderly subjects: Every step counts. Journal of Epidemiology and Community Health, 67, 194–197.CrossRefGoogle ScholarPubMed
Kooistra, M., Boss, H.M., van der Graaf, Y., Kappelle, L.J., Biessels, G.J., Geerlings, M.I., & SMART-MR Study Group (2014). Physical activity, structural brain changes and cognitive decline. The SMART-MR study. Atherosclerosis, 234, 47–53.CrossRefGoogle ScholarPubMed
Lee, T.M., Wong, M.L., Lau, B.W., Lee, J.C., Yau, S.Y., & So, K.F. (2014). Aerobic exercise interacts with neurotrophic factors to predict cognitive functioning in adolescents. Psychoneuroendocrinology, 39, 214–224.CrossRefGoogle ScholarPubMed
Lezak, M.D. (2004). Neuropsychological assessment (4th ed.) New York: Oxford University Press.Google Scholar
Makizako, H., Liu-Ambrose, T., Shimada, H., Doi, T., Park, H., Tsutsumimoto, K., & Suzuki, T. (2015). Moderate-Intensity physical activity, hippcampal volume, and memory in older adults with mild cognitive impairment. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 70, 480–486.CrossRefGoogle Scholar
Miralbell, J., Soriano, J.J., Spulber, G., Lopez-Cancio, E., Arenillas, J.F., Bargallo, N., & Mataro, M. (2012). Structural brain changes and cognition in relation to markers of vascular dysfunction. Neurobiology of Aging, 33, e9–e17.CrossRefGoogle ScholarPubMed
Morris, J., Heyman, A., Mohs, R., Hughes, J.P., van Belle, G., Fillenbaum, G., & Clark, C. (1989). The consortium to establish a registry for Alzheimer’s disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39, 1159–1165.Google Scholar
O’Brien, L.M., Ziegler, D.A., Deutsch, C.K., Frazier, J.A., Herbert, M.R., & Locascio, J.J. (2011). Statistical adjustments for brain size in volumetric neuroimaging studies: Some practical implications in methods. Psychiatry Research, 193, 113–122.CrossRefGoogle ScholarPubMed
Okonkwo, O.C., Schultz, S.A., Oh, J.M., Larson, J., Edwards, D., Cook, D., & Sager, M.A. (2014). Physical activity attenuates age-related biomarker alterations in preclinical AD. Neurology, 83, 1753–1760.CrossRefGoogle ScholarPubMed
Pan, A., Kumar, R., Macey, P.M., Fonarow, G.C., Harper, R.M., & Woo, M.A. (2013). Visual assessment of brain magnetic resonance imaging detects injury to cognitive regulatory sites in patients with heart failure. Journal of Cardiac Failure, 19, 94–100.CrossRefGoogle ScholarPubMed
Pressler, S.J., Subramanian, U., Kareken, D., Perkins, S.M., Gradus-Pizlo, I., Sauve, M.J., & Shaw, R.M. (2010). Cognitive deficits in chronic heart failure. Nursing Research, 59, 127–139.CrossRefGoogle ScholarPubMed
Qiu, C., Winblad, B., Marengoni, A., Klarin, I., Fastbom, J., & Fratiglioni, L. (2006). Heart failure and risk of dementia and Alzheimer disease: A population-based cohort study. Archives of Internal Medicine, 166, 1003–1008.CrossRefGoogle ScholarPubMed
Reitan, R. (1958). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual & Motor Skills, 8, 271–276.CrossRefGoogle Scholar
Sachdev, P.S., Brodaty, H., Valenzuela, M.J., Lorentz, L., Looi, J.C., Wen, W., & Zagami, A.S. (2004). The neuropsychological profile of vascular cognitive impairment in stroke and TIA paitents. Neurology, 62, 912–919.CrossRefGoogle Scholar
Smith, J.C., Nielson, K.A., Woodard, J.L., Seidenberg, M., Durgerian, S., Hazlett, K.E., & Rao, S.M. (2014). Physical activity reduces hippocampal atrophy in elders at genetic risk for Alzheimer’s disease. Frontiers in Aging Neuroscience, 6, 61.CrossRefGoogle ScholarPubMed
Tanigawa, T., Takechi, H., Arai, H., Yamada, M., Nishiguchi, S., & Aoyama, T. (2014). Effect of physical activity on memory function in older adults with mild Alzheimer’s disease and mild cognitive impairment. Geriatrics & Gerontology International, 14, 758–762.CrossRefGoogle ScholarPubMed
Tian, Q., Glynn, N.W., Erickson, K.I., Aizenstein, H.J., Simonsick, E.M., Yaffe, K., … Health ABC study (2015). Objective measures of physical activity, white matter integrity and cognitive status in adults over age 80. Behavioural Brain Research, 284, 51–57.CrossRefGoogle ScholarPubMed
Tian, Q., Erickson, K.I., Simonsick, E.M., Aizenstein, H.J., Glynn, N.W., Boudreau, R.M., & Rosano, C. (2014). Physical activity predicts microstructural integrity in memory-related network in very old adults. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 69, 1284–1290.CrossRefGoogle ScholarPubMed
Tsao, C.W., Seshadri, S., Beiser, A.S., Westwood, A.J., Decarli, C., Au, R., & Mitchell, G.F. (2013). Relations of arterial stiffness and endothelial function to brain aging in the community. Neurology, 81, 984–991.CrossRefGoogle ScholarPubMed
Tudor-Locke, C., Washington, T.L., & Hart, T.L. (2009). Expected values for steps/day in special populations. Preventative Medicine, 49, 3–11.CrossRefGoogle ScholarPubMed
Van den Hurk, K., Reijmer, Y.D., van den Berg, E., Alssema, M., Mijpels, G., Kostense, P.J., & Biessels, G.J. (2011). Heart failure and cognitive function in the general population: The Hoorn Study. European Journal of Heart Failure, 13, 1362–1369.CrossRefGoogle ScholarPubMed
Varma, V.R., Chuang, Y., Harris, G.C., Tan, E.J., & Carlson, M.C. (2015). Low-intensity daily walking activity is associated with hippocampal volume in older adults. Hippocampus, 25, 605–615.CrossRefGoogle ScholarPubMed
Vogels, R.L.C., van der Flier, W.M., van Harten, B., Gouw, A.A., Scheltens, P., Schroeder-Tanka, J.M., Weinstein, H.C. (2007). Brain magnetic resonance imaging abnormalities in patients with heart failure. European Journal of Heart Failure, 9, 1003–1009.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale—Third edition (WAIS-III). San Antonio, TX: Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale—Third edition (WMS-III). San Antonio, TX: Psychological Corporation.Google Scholar
Wilbur, J., Marquez, D.X., Fogg, L., Wilson, R.S., Staffileon, B.A., & Hoyem, R.L. (2012). The relationship between physical activity and cognition in older Latinos. The Journals of Gerontology Series B, Psychological Sciences and Social Sciences, 67, 525–534.CrossRefGoogle ScholarPubMed
Woo, M.A., Kumar, R., Macey, P.M., Fonarow, G.C., & Harper, R.M. (2009). Brain injury in autonomic, emotional, and cognitive regulatory areas in patients with heart failure. Journal of Cardiac Failure, 15, 214–223.CrossRefGoogle ScholarPubMed
Zhang, L.J., Wen, J., Ni, L., Zhong, J., Liang, X., Zheng, G., Lu, G.M. (2013). Predominant gray matter volume loss in patients with end-stage renal disease: A voxel-based morphometry study. Metabolic Brain Disease, 28, 647–654.CrossRefGoogle ScholarPubMed
Zuccala, G., Pedone, C., Cesari, M., Onder, G., Pahor, M., Marzetti, E., & Bernaei, R. (2003). The effects of cognitive impairment on mortality among hospitalized patients with heart failure. American Journal of Medicine, 115, 97–103.CrossRefGoogle ScholarPubMed