Brain derived neurotrophic factor, cardiopulmonary fitness and cognition in patients with coronary artery disease

Brain, Behavior, and Immunity

Volumn 25, Issue 6, 2011, Pages 1264-1271

  Swardfager, W ^a,b   Herrmann, N ^a,b   Marzolini, S ^c   Saleem, M ^a,b   Shammi, P ^a   Oh, P I ^a,c   Albert, P R ^d   Daigle, M ^d   Kiss, A ^a   Lanctot K L ^a,b,c  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c TORONTO REHABILITATION INSTITUTE   (Canada)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

BDNF; Brain derived neurotrophic factor; Cardiopulmonary fitness; Cognition; Coronary artery disease; Executive function; Memory; Psychomotor processing speed

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ARTICLE; CARDIOPULMONARY FITNESS; CARDIOPULMONARY FUNCTION; COGNITION; CONFOUNDING VARIABLE; CORONARY ARTERY DISEASE; DIGIT SYMBOL CODING TASK; ENZYME LINKED IMMUNOSORBENT ASSAY; EXERCISE TEST; FEMALE; GENOTYPE; HUMAN; LEARNING; MAJOR CLINICAL STUDY; MALE; MINI MENTAL STATE EXAMINATION; PERFORMANCE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PSYCHOLOGIC TEST; STANDARD; STROOP TEST;

AGED; BRAIN-DERIVED NEUROTROPHIC FACTOR; C-REACTIVE PROTEIN; COGNITION; CONFOUNDING FACTORS (EPIDEMIOLOGY); CORONARY DISEASE; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXERCISE TEST; FEMALE; GENOTYPE; HUMANS; INTERLEUKIN-6; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PHYSICAL FITNESS; POLYMORPHISM, SINGLE NUCLEOTIDE; PSYCHOMOTOR PERFORMANCE; RISK FACTORS;

EID: 79960222163     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.04.017     Document Type: Article

References (68)

1. Angevaren, M., Aufdemkampe, G., Verhaar, H.J., Aleman, A., Vanhees, L., 2008. Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev (3), CD005381.
2. Baker L.D., Frank L.L., Foster-Schubert K., Green P.S., Wilkinson C.W., McTiernan A., Plymate S.R., Fishel M.A., Watson G.S., Cholerton B.A., Duncan G.E., Mehta P.D., Craft S. Effects of aerobic exercise on mild cognitive impairment: a controlled trial. Arch. Neurol. 2010, 67(1):71-99.
3. Barnes D.E., Yaffe K., Satariano W.A., Tager I.B. A longitudinal study of cardiorespiratory fitness and cognitive function in healthy older adults. J. Am. Geriatr. Soc. 2003, 51(4):459-465.
4. Bayas A., Hummel V., Kallmann B.A., Karch C., Toyka K.V., Rieckmann P. Human cerebral endothelial cells are a potential source for bioactive BDNF. Cytokine 2002, 19(2):55-58.
5. Berchtold N.C., Castello N., Cotman C.W. Exercise and time-dependent benefits to learning and memory. Neuroscience 2010, 167(3):588-597.
6. Blumenthal J.A., Lett H.A., Babyak M.A., White W., Smith P.K., Mark D.B., Jones R., Mathew J.P., Newman M.F. Depression as a risk factor for mortality after coronary artery bypass surgery. Lancet 2003, 362(9384):604-609. NORG Investigators.
7. Chopp M., Zhang Z.G., Jiang Q. Neurogenesis, angiogenesis, and MRI indices of functional recovery from stroke. Stroke 2007, 38(2 Suppl.):827-831.
8. Colcombe S.J., Erickson K.I., Scalf P.E., Kim J.S., Prakash R., McAuley E., Elavsky S., Marquez D.X., Hu L., Kramer A.F. Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A: Biol. Sci. Med. Sci. 2006, 61(11):1166-1170.
9. Elkins J.S., Knopman D.S., Yaffe K., Johnston S.C. Cognitive function predicts first-time stroke and heart disease. Neurology 2005, 64(10):1750-1755.
10. Ferris L.T., Williams J.S., Shen C.L. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med. Sci. Sports Exerc. 2007, 39(4):728-734.
11. First, M.B., Spitzer, R.L., Gibbon, M. et al., 1996. Structured Clinical Interview For DSM-IV Diagnoses (SCID): Clinician and Research Versions. Biometrics Research Department, Columbia University, New York, NY.
12. Fried L.P., Kronmal R.A., Newman A.B., Bild D.E., Mittelmark M.B., Polak J.F., Robbins J.A., Gardin J.M. Risk factors for 5-year mortality in older adults: the Cardiovascular Health Study. JAMA 1998, 279(8):585-592.
13. Fujimura H., Altar C.A., Chen R., Nakamura T., Nakahashi T., Kambayashi J., Sun B., Tandon N.N. Brain-derived neurotrophic factor is stored in human platelets and released by agonist stimulation. Thromb. Haemost. 2002, 87(4):728-734.
14. Fujino H., Kitaoka Y., Hayashi Y., Munemasa Y., Takeda H., Kumai T., Kobayashi S., Ueno S. Axonal protection by brain-derived neurotrophic factor associated with CREB phosphorylation in tumor necrosis factor-alpha-induced optic nerve degeneration. Acta Neuropathol. 2009, 117(1):75-84.
15. Goekint M., Roelands B., De Pauw K., Knaepen K., Bos I., Meeusen R. Does a period of detraining cause a decrease in serum brain-derived neurotrophic factor?. Neurosci. Lett. 2010, 486(3):146-149.
16. Golden E., Emiliano A., Maudsley S., Windham B.G., Carlson O.D., Egan J.M., Driscoll I., Ferrucci L., Martin B., Mattson M.P. Circulating brain-derived neurotrophic factor and indices of metabolic and cardiovascular health: data from the Baltimore Longitudinal Study of Aging. PLoS One 2010, 5(4):e10099.
17. Goldhammer E., Tanchilevitch A., Maor I., Beniamini Y., Rosenschein U., Sagiv M. Exercise training modulates cytokines activity in coronary heart disease patients. Int. J. Cardiol. 2005, 100(1):93-99.
18. Gunstad J., Benitez A., Smith J., Glickman E., Spitznagel M.B., Alexander T., Juvancic-Heltzel J., Murray L. Serum brain-derived neurotrophic factor is associated with cognitive function in healthy older adults. J. Geriatr. Psychiatry Neurol. 2008, 21(3):166-170.
19. Guo S., Kim W.J., Lok J., Lee S.R., Besancon E., Luo B.H., Stins M.F., Wang X., Dedhar S., Lo E.H. Neuroprotection via matrix-trophic coupling between cerebral endothelial cells and neurons. Proc. Natl. Acad. Sci. USA 2008, 105(21):7582-7587.
20. Hachinski V., Iadecola C., Petersen R.C., Breteler M.M., Nyenhuis D.L., Black S.E., Powers W.J., DeCarli C., Merino J.G., Kalaria R.N., Vinters H.V., Holtzman D.M., Rosenberg G.A., Dichgans M., Marler J.R., Leblanc G.G. National Institute of Neurological Disorders and Stroke-Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke 2006, 37(9):2220-2241.
21. Hajjar I., Quach L., Yang F., Chaves P.H., Newman A.B., Mukamal K., Longstreth W., Inzitari M., Lipsitz L.A. Hypertension, white matter hyperintensities, and concurrent impairments in mobility, cognition, and mood: the cardiovascular health study. Circulation 2011, 123(8):858-865.
22. Hamm L.F., Kavanagh T. The Toronto Cardiac Rehabilitation and Secondary Prevention Program: 1968 into the new millennium. J. Cardiopulm. Rehabil. 2000, 20(1):16-22.
23. Jimenez I., Sobrino T., Rodriguez-Yanez M., Pouso M., Cristobo I., Sabucedo M., Blanco M., Castellanos M., Leira R., Castillo J. High serum levels of leptin are associated with post-stroke depression. Psychol. Med. 2009, 39(7):1201-1209.
24. Jones N.L., Campbell E.J.M. Clinical Exercise Testing 1982, W.B. Saunders, Philadelphia. second ed.
25. Jovinge S., Hamsten A., Tornvall P., Proudler A., Bavenholm P., Ericsson C.G., Godsland I., de Faire U., Nilsson J. Evidence for a role of tumor necrosis factor alpha in disturbances of triglyceride and glucose metabolism predisposing to coronary heart disease. Metabolism 1998, 47(1):113-118.
26. Katsuki H., Kurimoto E., Takemori S., Kurauchi Y., Hisatsune A., Isohama Y., Izumi Y., Kume T., Shudo K., Akaike A. Retinoic acid receptor stimulation protects midbrain dopaminergic neurons from inflammatory degeneration via BDNF-mediated signaling. J. Neurochem. 2009, 110(2):707-718.
27. Kerschensteiner M., Stadelmann C., Dechant G., Wekerle H., Hohlfeld R. Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann. Neurol. 2003, 53(3):292-304.
28. Kim H., Li Q., Hempstead B.L., Madri J.A. Paracrine and autocrine functions of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) in brain-derived endothelial cells. J. Biol. Chem. 2004, 279(32):33538-33546.
29. Kim Y.J., Shin Y.O., Bae J.S., Lee J.B., Ham J.H., Son Y.J., Kim J.K., Kim C., Lee B.K., Oh J.K., Othman T., Min Y.K., Yang H.M. Beneficial effects of cardiac rehabilitation and exercise after percutaneous coronary intervention on hsCRP and inflammatory cytokines in CAD patients. Pflugers Arch. 2008, 455(6):1081-1088.
30. Knopman D., Boland L.L., Mosley T., Howard G., Liao D., Szklo M., McGovern P., Folsom A.R. Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology 2001, 56(1):42-48.
31. Komulainen P., Pedersen M., Hanninen T., Bruunsgaard H., Lakka T.A., Kivipelto M., Hassinen M., Rauramaa T.H., Pedersen B.K., Rauramaa R. BDNF is a novel marker of cognitive function in ageing women: the DR's EXTRA study. Neurobiol. Learn. Mem. 2008, 90(4):596-603.
32. Lang U.E., Hellweg R., Sander T., Gallinat J. The Met allele of the BDNF Val66Met polymorphism is associated with increased BDNF serum concentrations. Mol. Psychiatry 2009, 14(2):120-122.
33. Li G., Peskind E.R., Millard S.P., Chi P., Sokal I., Yu C.E., Bekris L.M., Raskind M.A., Galasko D.R., Montine T.J. Cerebrospinal fluid concentration of brain-derived neurotrophic factor and cognitive function in non-demented subjects. PLoS One 2009, 4(5):e5424.
34. Li Q., Ford M.C., Lavik E.B., Madri J.A. Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between neural stem cells and endothelial cells: an in vitro study. J. Neurosci. Res. 2006, 84(8):1656-1668.
35. Linker R.A., Lee D.H., Demir S., Wiese S., Kruse N., Siglienti I., Gerhardt E., Neumann H., Sendtner M., Luhder F., Gold R. Functional role of brain-derived neurotrophic factor in neuroprotective autoimmunity: therapeutic implications in a model of multiple sclerosis. Brain 2010, 133(Pt 8):2248-2263.
36. Lommatzsch M., Zingler D., Schuhbaeck K., Schloetcke K., Zingler C., Schuff-Werner P., Virchow J.C. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol. Aging 2005, 26(1):115-123.
37. Lorgis L., Amoureux S., de Maistre E., Sicard P., Bejot Y., Zeller M., Vergely C., Sequeira-Le Grand A., Lagrost A.C., Berchoud J., Cottin Y., Rochette L. Serum brain-derived neurotrophic factor and platelet activation evaluated by soluble P-selectin and soluble CD-40-ligand in patients with acute myocardial infarction. Fundam. Clin. Pharmacol. 2010, 24(4):525-530.
38. Louissaint A., Rao S., Leventhal C., Goldman S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002, 34(6):945-960.
39. Luc G., Bard J.M., Juhan-Vague I., Ferrieres J., Evans A., Amouyel P., Arveiler D., Fruchart J.C., Ducimetiere P. C-reactive protein, interleukin-6, and fibrinogen as predictors of coronary heart disease: the PRIME Study. Arterioscler. Thromb. Vasc. Biol. 2003, 23(7):1255-1261.
40. Marzolini S., Candelaria H., Oh P. Prevalence and impact of musculoskeletal comorbidities in cardiac rehabilitation. J. Cardiopulm. Rehabil. Prev. 2010, 30(6):391-400.
41. Milani R.V., Lavie C.J., Mehra M.R., Ventura H.O. Understanding the basics of cardiopulmonary exercise testing. Mayo Clin. Proc. 2006, 81(12):1603-1611.
42. Miyajima F., Ollier W., Mayes A., Jackson A., Thacker N., Rabbitt P., Pendleton N., Horan M., Payton A. Brain-derived neurotrophic factor polymorphism Val66Met influences cognitive abilities in the elderly. Genes Brain Behav. 2008, 7(4):411-417.
43. Naimark A., Wasserman K., McIlroy M.B. Continuous measurement of ventilatory exchange ratio during exercise. J. Appl. Physiol. 1964, 19:644-652.
44. Nakagawa T., Tsuchida A., Itakura Y., Nonomura T., Ono M., Hirota F., Inoue T., Nakayama C., Taiji M., Noguchi H. Brain-derived neurotrophic factor regulates glucose metabolism by modulating energy balance in diabetic mice. Diabetes 2000, 49(3):436-444.
45. Nakahashi T., Fujimura H., Altar C.A., Li J., Kambayashi J., Tandon N.N., Sun B. Vascular endothelial cells synthesize and secrete brain-derived neurotrophic factor. FEBS Lett. 2000, 470(2):113-117.
46. Ohab J.J., Fleming S., Blesch A., Carmichael S.T. A neurovascular niche for neurogenesis after stroke. J. Neurosci. 2006, 26(50):13007-13016.
47. Pietranera L., Lima A., Roig P., De Nicola A.F. Involvement of brain-derived neurotrophic factor and neurogenesis in oestradiol neuroprotection of the hippocampus of hypertensive rats. J. Neuroendocrinol. 2010, 22(10):1082-1092.
48. Puddu P., Puddu G.M., Zaca F., Muscari A. Endothelial dysfunction in hypertension. Acta Cardiol. 2000, 55(4):221-232.
49. Qin L., Kim E., Ratan R., Lee F.S., Cho S. Genetic variant of BDNF (Val66Met) polymorphism attenuates stroke-induced angiogenic responses by enhancing anti-angiogenic mediator CD36 expression. J. Neurosci. 2011, 31(2):775-783.
50. Radloff L.S. The CES-D scale: a self-report depression scale for research in the general population. Appl. Psychol. Measure. 1977, 1:385-401.
51. Rosano C., Newman A.B., Katz R., Hirsch C.H., Kuller L.H. Association between lower digit symbol substitution test score and slower gait and greater risk of mortality and of developing incident disability in well-functioning older adults. J. Am. Geriatr. Soc. 2008, 56(9):1618-1625.
52. Schulte-Herbruggen O., Nassenstein C., Lommatzsch M., Quarcoo D., Renz H., Braun A. Tumor necrosis factor-alpha and interleukin-6 regulate secretion of brain-derived neurotrophic factor in human monocytes. J. Neuroimmunol. 2005, 160(1-2):204-209.
53. Seifert T., Brassard P., Wissenberg M., Rasmussen P., Nordby P., Stallknecht B., Adser H., Jakobsen A.H., Pilegaard H., Nielsen H.B., Secher N.H. Endurance training enhances BDNF release from the human brain. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298(2):R372-R377.
54. Sen S., Duman R., Sanacora G. Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol. Psychiatry 2008, 64(6):527-532.
55. Smith P.J., Blumenthal J.A., Hoffman B.M., Cooper H., Strauman T.A., Welsh-Bohmer K., Browndyke J.N., Sherwood A. Aerobic exercise and neurocognitive performance. a meta-analytic review of randomized controlled trials. Psychosom. Med. 2010, 72(3):239-252.
56. Swardfager W., Herrmann N., Marzolini S., Saleem M., Kiss A., Shammi P., Oh P.I., Lanctot K.L. Cardiopulmonary fitness is associated with cognitive performance in patients with coronary artery disease. J. Am. Geriatr. Soc. 2010, 58(8):1519-1525.
57. Tang S.W., Chu E., Hui T., Helmeste D., Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci. Lett. 2008, 431(1):62-65.
58. Taylor W.D., Zuchner S., McQuoid D.R., Payne M.E., MacFall J.R., Steffens D.C., Speer M.C., Krishnan K.R. The brain-derived neurotrophic factor VAL66MET polymorphism and cerebral white matter hyperintensities in late-life depression. Am. J. Geriatr. Psychiatry 2008, 16(4):263-271.
59. van Exel E., de Craen A.J., Remarque E.J., Gussekloo J., Houx P., Bootsma-van der Wiel A., Frolich M., Macfarlane P.W., Blauw G.J., Westendorp R.G. Interaction of atherosclerosis and inflammation in elderly subjects with poor cognitive function. Neurology 2003, 61(12):1695-1701.
60. Walsh J.H., Bilsborough W., Maiorana A., Best M., O'Driscoll G.J., Taylor R.R., Green D.J. Exercise training improves conduit vessel function in patients with coronary artery disease. J. Appl. Physiol. 2003, 95(1):20-25.
61. Woo N.H., Teng H.K., Siao C.J., Chiaruttini C., Pang P.T., Milner T.A., Hempstead B.L., Lu B. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci. 2005, 8(8):1069-1077.
62. Wu S.Y., Wang T.F., Yu L., Jen C.J., Chuang J.I., Wu F.S., Wu C.W., Kuo Y.M. Running exercise protects the substantia nigra dopaminergic neurons against inflammation-induced degeneration via the activation of BDNF signaling pathway. Brain Behav. Immun. 2011, 25(1):135-146.
63. Yaffe K., Lindquist K., Penninx B.W., Simonsick E.M., Pahor M., Kritchevsky S., Launer L., Kuller L., Rubin S., Harris T. Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology 2003, 61(1):76-80.
64. Yang L., Zhang Z., Sun D., Xu Z., Yuan Y., Zhang X., Li L. Low serum BDNF may indicate the development of PSD in patients with acute ischemic stroke. Int. J. Geriatr. Psychiatry 2011, 26(5):495-502.
65. Yasutake C., Kuroda K., Yanagawa T., Okamura T., Yoneda H. Serum BDNF, TNF-alpha and IL-1beta levels in dementia patients: comparison between Alzheimer's disease and vascular dementia. Eur. Arch. Psychiatry Clin. Neurosci. 2006, 256(7):402-406.
66. Zhang F., Wu Y., Jia J. Exercise preconditioning and brain ischemic tolerance. Neuroscience 2011, 177:170-176.
67. Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., Bruggen N., Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 2000, 106(7):829-838.
68. Ziegenhorn A.A., Schulte-Herbruggen O., Danker-Hopfe H., Malbranc M., Hartung H.D., Anders D., Lang U.E., Steinhagen-Thiessen E., Schaub R.T., Hellweg R. Serum neurotrophins - a study on the time course and influencing factors in a large old age sample. Neurobiol. Aging 2007, 28(9):1436-1445.