Physical activity and inflammation: effects on gray-matter volume and cognitive decline in aging

Human Brain Mapping

Volumn 37, Issue 10, 2016, Pages 3462-3473

  Papenberg, Goran ^a   Ferencz, Beata ^a   Mangialasche, Francesca ^a   Mecocci, Patrizia ^b   Cecchetti, Roberta ^b   Kalpouzos, Grégoria ^a   Fratiglioni, Laura ^a,c   Bäckman, Lars ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF PERUGIA   (Italy)

^c STOCKHOLM GERONTOLOGY RESEARCH CENTER   (Sweden)

Author keywords

aging; cognition; gray matter; inflammation; physical activity

Indexed keywords

C REACTIVE PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR;

ADULT; AGED; ARTICLE; BRAIN SIZE; COGNITION; DEMENTIA; DORSAL STRIATUM; FEMALE; FITNESS; GRAY MATTER; HIPPOCAMPUS; HUMAN; INFERIOR PARIETAL LOBULE; INFERIOR TEMPORAL CORTEX; INFLAMMATION; LATERAL PREFRONTAL CORTEX; MAJOR CLINICAL STUDY; MALE; MENTAL DETERIORATION; MINI MENTAL STATE EXAMINATION; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; ORBITAL CORTEX; PHYSICAL ACTIVITY; PHYSICAL INACTIVITY; PRIORITY JOURNAL; SELF REPORT; SENESCENCE; STRIATE CORTEX;

EID: 84985905737     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23252     Document Type: Article

References (66)

1. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.
2. Arbuckle, J. L. (2006). Amos (Version 7.0) [Computer Program]. Chicago: SPSS.
3. Ashburner J (2007): A fast diffeomorphic image registration algorithm. NeuroImage 38:95–113.
4. Ashburner J, Friston KJ (2005): Unified segmentation. NeuroImage 26:839–851.
5. Bendall LJ, Bradstock KF (2014): G-CSF: From granulopoietic stimulant to bone marrow stem cell mobilizing agent. Cytokine Growth Factor Rev 25:355–367.
6. Buckley DI, Fu R, Freeman M, Rogers K, Helfand M (2009): C-reactive protein as a risk factor for coronary heart disease: A systematic review and meta-analyses for the U.S. Preventive Services Task Force. Ann Intern Med 151:483–495.
7. Burzynska AZ, Wong CN, Voss MW, Cooke GE, Gothe NP, Fanning J, McAuley E, Kramer AF (2015): Physical activity is linked to greater moment-to-moment variability in spontanous brain activity in older adults. Plos One 10:e0134819.
8. Brown BM, Bourgeat P, Peiffer JJ, Burnham S, Laws SM, Rainey-Smith SR, Bartrés-Faz D, Villemagne VL, Taddei K, Rembach A, Bush A, Ellis KA, Macaulay SL, Rowe CC, Ames D, Masters CL, Maruff P, Martins RN (2014): Influence of BDNF Val66Met on the relationship between physical activity and brain volume. Neurology 83:1345–1352.
9. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF (2006): Aerobic exercise training increasesbrain volume in aging humans. J Gerontol a Biol Sci Med Sci 61:1166–1170.
10. Cotman CW, Berchtold NC, Christie LA (2007): Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends Neurosci 30:464–472.
11. Demirakca T, Brusniak W, Tunc-Skarka N, Wolf I, Meier S, Matthäus F, Ende G, Schulze TG, Diener C (2014): Does body shaping influence brain shape? Habitual physical activity is linked to brain morphology independent of age. World J Biol Psychiatry 15:387–396.
12. Elderkin-Thompson V, Irwin MR, Hellemann G, Kumar A (2012): Interleukin-6 and memory functions of encoding and recall in healthy and depressed elderly adults. Am J Geriatr Psychiatry 20:753–763.
13. Erickson KI, Leckie RL, Weinstein AM (2014): Physical activity, fitness, and gray matter volume. Neurobiol Aging 35:S20–S28.
14. Erickson KI, Prakash RS, Voss MW, Chaddock L, Hu L, Morris KS, White SM, Wojcicki TR, McAuley E, Kramer AF (2009): Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19:1030–1039.
15. Fandakova Y, Lindenberger U, Shing YL (2014): Maintenance of youth-like processing protects against false memory in later adulthood. Neurobiol Aging 36:933–941.
16. Folstein MF, Folstein SE, McHugh PR (1975): Mini-Mental State: A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198.
17. Floel A, Ruscheweyh R, Kruger K, Willemer C, Winter B, Volker K, Lohmann H, Zitzmann M, Mooren F, Breitenstein C, Knecht S (2010): Physical activity and memory functions: Are neurotrophins and cerebral gray matter volume the missing link? Neuroimage 49:2756–2763.
18. Gunning-Dixon FM, Head D, McQuain J, Acker JD, Raz N (1998): Differential aging of the human striatum: A prospective MR imaging study. AJNR Am J Neuroradiol 19:501–1507.
19. Hamer M, Sabia S, Batty GD, Shipley MJ, Tabak AG, Singh-Manoux A, Kivimaki M (2012): Physical activity and inflammatory markers over 10 years: Follow-up in men and women from the Whitehall II cohort study. Circulation 126:928–933.
20. Hartung T (1998): Anti-inflammatory effects of granulocyte colony-stimulating factor. Curr Opin Hematol 5:221–225.
21. Head D, Bugg JM, Goate AM, Fagan AM, Mintun MA, Benzinger T, Holzmann DM, Morris JC (2012): Exercise engagement as a moderator of APOE effects on amyloid deposition. Arch Neurol 69:636–643.
22. Johnson NF, Kim C, Clasey JL, Bailey A, Gold BT (2012): Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors. NeuroImage 59:1514–1523.
23. Kempermann G (2008): The neurogenic reserve hypothesis: What is adult hippocampal neurogenesis good for? Trends Neurosci 31:163–169.
24. Kline RB (2005): Principles and Practice of Structural Equation Modeling, 3rd ed. New York: Guilford Press.
25. Killgore WD, Olson EA, Weber M (2013): Physical exercise habits correlate with gray matter volume of the hippocampus in healthy adult humans. Sci Rep 3:3457.
26. Kitahara CM, Trabert B, Katki HA, Chaturvedi AK, Kemp TJ, Pinto LA, Moore SC, Purdue MP, Wentzensen N, Hildesheim A, Shiels MS (2014): Body mass index, physical activity, and serum markers of inflammation, immunity, and insulin resistance. Cancer Epidemiol Biomarkers Prev 23:2840–2849.
27. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, Cua DJ (2004): IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev 202:96–105.
28. Lim A, Krajina K, Marsland AL (2013): Peripheral inflammation and cognitive aging. Mod Trends Pharmacopsychiatry 28:175–187.
29. Lindenberger U, Burzynska AZ, Nagel IE (2013): Heterogeneity in frontal lobe aging. In Stuss DT, Knight RT, editors. Principles of Frontal Lobe Functions, 2nd ed. New York: Oxford University Press.
30. Lindwall M, Rennemark M, Halling A, Berglund J, Hassmen P (2007): Depression and exercise in elderly men and women: Findings from the Swedish national study on aging and care. J Aging Phys Act 15:41–55.
31. Lista I, Sorrentino G (2010): Biological mechanisms of physical activity in preventing cognitive decline. Cell Mol Neurobiol 30:493–503.
32. Maass A, Düzel S, Goerke M, Becke A, Sobieray U, Neumann K, Lövden M, Lindenberger U, Bäckman L, Braun-Dullaeus R, Ahrens D, Heinze HJ, Müller NG, Düzel E (2015): Vascular hippocampal plasticity after aerobic exercise in older adults. Mol Psychiatry 20:585–593.
33. Manos PJ, Wu R (1994): The ten point clock test: A quick screen and grading method for cognitive impairment in medical and surgical patients. Int J Psychiatry Med 24:229–244.
34. Marosi K, Bori Z, Hart N, Sárga L, Koltai E, Radák Z, Nyakas C (2012): Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats. Neuroscience 226:21–28.
35. Marsland AL, Petersen KL, Sathanoori R, Muldoon MF, Neumann SA, Ryan C, Flory JD, Manuck SB (2006): Interleukin-6 covaries inversely with cognitive performance among middle-aged community volunteers. Psychosom Med 68:895–903.
36. Marsland AL, Gianaros PJ, Kuan DC, Sheu LK, Krajina K, Manuck SB (2015): Brain morphology links systemic inflammation to cognitive function in midlife adults. Brain Behav Immun 48:195–204.
37. McAfoose J, Baune BT (2009): Evidence for a cytokine model of cognitive function. Neurosci Biobehav Rev 33:355–366.
38. McEwen SC, Hardy A, Ellingson BM, Jarrahi B, Sandhu N, Subotnik KL, Ventrura J, Nuechterlein KH (2015): Prefrontal and hippocampal brain volume deficits: Role of low physical activity on brain plasticity in first-episode schizophrenia patients. J Int Neuropsychol Soc 21:868–879.
39. Meredith W (1993): Measurement invariance, factor-analysis and factorial invariance. Psychometrika 58:525–543.
40. Nelson ME, Rejeski WJ, Blair SN, Duncan PW, Judge JO, King AC, Macera CA, Castaneda-Sceppa C (2007): Physical activity and public health in older adults: Recommendation from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 39:1435–1445.
41. Nyberg L, Lövdén M, Riklund K, Lindenberger U, Bäckman L (2012): Memory aging and brain maintenance. Trends Cogn Sci 16:292–305.
42. Raz N, Gunning-Dixon F, Head D, Rodrigue KM, Williamson A, Acker JD (2004): Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: Replicability of regional differences in volume. Neurobiol Aging 25:377–396.
43. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005): Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cereb Cortex 15:1676–1689.
44. Ray S, Britschgi M, Herbert C, Takeda-Uchimura Y, Boxer A, Blennow K, Friedman LF, Galasko DR, Jutel M, Karydas A, Kaye JA, Leszek J, Miller BL, Minthon L, Quinn JF, Rabinovici GD, Robinson WH, Sabbagh MN, So YT, Sparks DL, Tabaton M, Tinklenberg J, Yesavage JA, Tibshirani R, Wyss-Coray T (2007): Classification and prediction of clinical Alzheimer's diagnosis based on plasma signaling proteins. Nat Med 13:1359–1362.
45. Rizzuto D, Fratiglioni L (2014): Lifestyle factors related to mortality and survival: A mini-review. Gerontology 60:327–335.
46. Rennemark M, Lindwall M, Halling A, Berglund J (2009): Relationships between physical activity and perceived qualities of life in old age. Results of the SNAC study. Aging Ment Health 13:1–8.
47. Ruscheweyh R, Willemer C, Krüger K, Duning T, Warnecke T, Sommer J, Völker K, Ho HV, Mooren F, Knecht S, Flöel A (2011): Physical activity and memory functions: an interventional study. Neurobiol Aging 32:1304–1319.
48. Rönnlund M, Nyberg L, Bäckman L, Nilsson LG (2005): Stability, growth, and decline in adult life span development of declarative memory: Cross-sectional and longitudinal data from a population-based study. Psychol Aging 20:3–18.
49. Rovio S, Spulber G, Nieminen LJ, Niskanen E, Winblad B, Tuomilehto J, Nissinen A, Soininen H, Kivipelto M (2010): The effect of midlife physical activity on structural brain changes in the elderly. Neurobiol Aging 31:1927–1936.
50. Rydwik E, Welmer AK, Kareholt I, Angleman S, Fratiglioni L, Wang HX (2013): Adherence to physical exercise recommendations in people over 65–the SNAC-Kungsholmen study. Eur J Public Health 23:799–804.
51. Sanchez-Ramos J, Song S, Sava V, Catlow B, Lin X, Mori T, Cao C, Arendash GW (2009): Granulocyte colony stimulating factor decreases brain amyloid burden and reverses cognitive impairment in Alzheimer's mice. Neuroscience 163:55–72.
52. Satizabal CL, Zhu YC, Mazoyer B, Dufouil C, Tzourio C (2012): Circulating IL-6 and CRP are associated with MRI findings in the elderly: The 3C-Dijon Study. Neurology 78:720–727.
53. Schneider P, Hampel H, Buerger K (2009): Biological marker candidates of Alzheimer's disease in blood, plasma, and serum. CNS Neurosci Ther 15:358–374.
54. Shanely RA, Nieman DC, Henson DA, Jin F, Knab AM, Sha W (2013): Inflammation and oxidative stress are lower in physically fit and active adults. Scand J Med Sci Sports 23:215–223.
55. Shao W, Zhang SZ, Tang M, Zhang XH, Zhou Z, Yin YQ, Zhou QB, Huang YY, Liu YJ, Wawrousek E, Chen T, Li SB, Xu M, Zhou JN, Hu G, Zhou JW (2013): Suppression of neuroinflammation by astrocytic dopamine D2 receptors via alphaB-crystallin. Nature 494:90–94.
56. Shohamy D, Adcock RA (2010): Dopamine and adaptive memory. Trends Cogn Sci 14:464–472.
57. Sopova K, Gatsiou K, Stellos K, Laske C (2014): Dysregulation of neurotrophic and haematopoietic growth factors in alzheimer's disease: From pathophysiology to novel treatment strategies. Curr Alzheimer Res 11:27–39.
58. Sim YJ, Yu S, Yoon KJ, Loiacono CM, Kohut ML (2009): Chronic exercise reduces illness severity, decreases viral load, and results in greater anti-inflammatory effects than acute exercise during influenza infection. J Infect Dis 200:1434–1442.
59. Tan MS, Yu JT, Jiang T, Zhu XC, Guan HS, Tan L (2014): IL12/23 p40 inhibition ameliorates Alzheimer's disease-associated neuropathology and spatial memory in SAMP8 mice. J Alzheimers Dis 38:633–646.
60. Voelcker-Rehage C, Niemann C (2013): Structural and functional brain changes related to different types of physical activity across the life span. Neurosci Biobehav Rev 37:2268–2295.
61. Vom Berg J, Prokop S, Miller KR, Obst J, Kalin RE, Lopategui-Cabezas I, Wegner A, Mair F, Schipke CG, Peters O, Winter Y, Becher B, Heppner FL (2012): Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nat Med 18:1812–1819.
62. Voss MW, Heo S, Prakash RS, Erickson KI, Alves H, Chaddock L, Szabo AN, Mailey EL, Wojcicki TR, White SM, Gothe N, McAuley E, Sutton BP, Kramer AF (2012): The influence of aerobic fitness on cerebral white matterintegrity and cognitive function in older adults: Results of a one-year exerciseintervention. Hum Brain Mapp 34:2972–2985.
63. Walhovd KB, Storsve AB, Westlye LT, Drevon CA, Fjell AM (2014): Blood markers of fatty acids and vitamin D, cardiovascular measures, body mass index, and physical activity relate to longitudinal cortical thinning in normal aging. Neurobiol Aging 35:1055–1064.
64. Welmer AK, Angleman S, Rydwik E, Fratiglioni L, Qui C (2013): Association of cardiovascular burden with mobility limitation among elderly people: A population-based study. PLoS ONE 8:e65815.
65. World Health Organization (2010): Global recommendations on physical activity for health. Retrieved from http://whqlibdoc.who.int/publications/2010/9789241599979_eng.pdf
66. Zhang H, Sachdev PS, Wen W, Crawford JD, Brodaty H, Baune BT, Kochan NA, Slavin M, Reppermund S, Kang K, Troller JN (2015): The relationship between inflammatory markers and voxel-based gray matter volumes in nondemented older adults. Neurobiol Aging 37:138–146.