Neck muscle cross-sectional area, brain volume and cognition in healthy older men; a cohort study

BMC Geriatrics

John M Starr²  Alasdair MJ MacLullich²  Joanna M Wardlaw¹  Ian J Deary³  Calum D Gray¹  Karen J Ferguson²  Alixe HM Kilgour² 

[1] Scottish Imaging Network, A Platform for Scientific Excellence (SINAPSE), Edinburgh, UK;Geriatric Medicine Unit, University of Edinburgh, Edinburgh, UK;Department of Psychology, University of Edinburgh, Edinburgh, UK

关键词: Brain volume;    Muscle cross-sectional area;    Aging;    Cognition;    Sarcopenia;   

Others  :  857855
DOI  :  10.1186/1471-2318-13-20

 received in 2012-10-30, accepted in 2013-02-22,  发布年份 2013

【 摘 要 】

Background

Two important consequences of the normal ageing process are sarcopenia (the age-related loss of muscle mass and function) and age-related cognitive decline. Existing data support positive relationships between muscle function, cognition and brain structure. However, studies investigating these relationships at older ages are lacking and rarely include a measure of muscle size. Here we test whether neck muscle size is positively associated with cognition and brain structure in older men.

Methods

We studied 51 healthy older men with mean age 73.8 (sd 1.5) years. Neck muscle cross-sectional area (CSA) was measured from T1-weighted MR-brain scans using a validated technique. We measured multiple cognitive domains including verbal and visuospatial memory, executive functioning and estimated prior cognitive ability. Whole brain, ventricular, hippocampal and cerebellar volumes were measured with MRI. General linear models (ANCOVA) were performed.

Results

Larger neck muscle CSA was associated with less whole brain atrophy (t = 2.86, p = 0.01, partial eta squared 17%). Neck muscle CSA was not associated with other neuroimaging variables or current cognitive ability. Smaller neck muscle CSA was unexpectedly associated with higher prior cognition (t = −2.12, p < 0.05, partial eta squared 10%).

Conclusions

In healthy older men, preservation of whole brain volume (i.e. less atrophy) is associated with larger muscle size. Longitudinal ageing studies are now required to investigate these relationships further.

【 授权许可】

   
2013 Kilgour et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M: Sarcopenia: European consensus on definition and diagnosis. Age Ageing 2010, 39:412-423.
• [2]Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J, Breuille D, Cederholm T, Chandler J, De Meynard C, Donini L, Harris T, Kannt A, Keime Guibert F, Onder G, Papanicolaou D, Rolland Y, Rooks D, Sieber C, Souhami E, Verlaan S, Zamboni M: Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 2011, 12:249-256.
• [3]Muscaritoli M, Anker SD, Argiles J, Aversa Z, Bauer JM, Biolo G, Boirie Y, Bosaeus I, Cederholm T, Costelli P, Fearon KC, Laviano A, Maggio M, Fanelli FR, Schneider SM, Schols A, Sieber CC: Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by special interest groups (sig) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr 2010, 29:154-159.
• [4]Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L: Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol 2003, 95:1851-1860.
• [5]Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD: Epidemiology of sarcopenia among the elderly in new mexico. Am J Epidemiol 1998, 147:755-763.
• [6]Rantanen T: Muscle strength, disability and mortality. Scand J Med Sci Sports 2003, 13:3-8.
• [7]Janssen I, Heymsfield SB, Wang ZM, Ross R: Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 2000, 89:81-88.
• [8]Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB, Hlth ABCS: The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 2006, 61:1059-1064.
• [9]Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R: Aging of skeletal muscle: A 12-yr longitudinal study. J Appl Physiol 2000, 88:1321-1326.
• [10]Skelton DA, Greig CA, Davies JM, Young A: Strength, power and related functional ability of healthy people aged 65–89 years. Age Ageing 1994, 23:371-377.
• [11]Deary IJ, Corley J, Gow AJ, Harris SE, Houlihan LM, Marioni RE, Penke L, Rafnsson SB, Starr JM: Age-associated cognitive decline. Br Med Bull 2009, 92:135-152.
• [12]Hedden T, Gabrieli JD: Insights into the ageing mind: a view from cognitive neuroscience; Nat rev neurosci. England 2004, 5:87-96.
• [13]Park DC, Reuter-Lorenz P: The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol 2009, 60:173-196.
• [14]Salthouse TA: When does age-related cognitive decline begin? Neurobiol aging United States 2009, 30:507-514.
• [15]Angevaren M, Aufdemkampe G, Verhaar HJ, Aleman A, Vanhees L: Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008, CD005381.
• [16]Coley N, Andrieu S, Gardette V, Gillette-Guyonnet S, Sanz C, Vellas B, Grand A: Dementia prevention: methodological explanations for inconsistent results. Epidemiol Rev 2008, 30:35.
• [17]Weuve J, Kang JH, Manson JE, Breteler MM, Ware JH, Grodstein F: Physical activity, including walking, and cognitive function in older women. JAMA 2004, 292:1454-1461.
• [18]Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF: Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006, 61:1166-1170.
• [19]Kramer AF, Erickson KI, Colcombe SJ: Exercise, cognition, and the aging brain. J Appl Physiol 2006, 101:1237-1242.
• [20]Rosano C, Simonsick EM, Harris TB, Kritchevsky SB, Brach J, Visser M, Yaffe K, Newman AB: Association between physical and cognitive function in healthy elderly: the health, aging and body composition study. Neuroepidemiology 2005, 24:8-14.
• [21]Fitzpatrick AL, Buchanan CK, Nahin RL, Dekosky ST, Atkinson HH, Carlson MC, Williamson JD: Ginkgo evaluation of memory study I: associations of gait speed and other measures of physical function with cognition in a healthy cohort of elderly persons. J Gerontol A Biol Sci Med Sci 2007, 62:1244-1251.
• [22]Raji MA, Kuo YF, Snih SA, Markides KS, Peek MK, Ottenbacher KJ: Cognitive status, muscle strength, and subsequent disability in older mexican americans. J Am Geriatr Soc 2005, 53:1462-1468.
• [23]Deary IJ, Johnson W, Gow AJ, Pattie A, Brett CE, Bates TC, Starr JM: Losing one’s grip: a bivariate growth curve model of grip strength and nonverbal reasoning from age 79 to 87 years in the lothian birth cohort 1921. J Gerontol B Psychol Sci Soc Sci 2011, 66:609-707.
• [24]Meaney MJ, Odonnell D, Rowe W, Tannenbaum B, Steverman A, Walker M, Nair NPV, Lupien S: Individual-differences in hypothalamic-pituitary-adrenal activity in later life and hippocampal aging. Exp Gerontol 1995, 30:229-251.
• [25]Ma K, Mallidis C, Bhasin S, Mahabadi V, Artaza J, Gonzalez-Cadavid N, Arias J, Salehian B: Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am J Physiol Endocrinol Metab 2003, 285:E363-E371.
• [26]Weaver JD, Huang MH, Albert M, Harris T, Rowe JW, Seeman TE: Interleukin-6 and risk of cognitive decline - macarthur studies of successful aging. Neurology 2002, 59:371-378.
• [27]Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB, Nevitt M, Harris TB: Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the health abc study. J Gerontol A Biol Sci Med Sci 2002, 57:M326-M332.
• [28]Kachiwala SJ, Harris SE, Wright AF, Hayward C, Starr JM, Whalley LJ, Deary IJ: Genetic influences on oxidative stress and their association with normal cognitive ageing. Neurosci Lett 2005, 386:116-120.
• [29]Trounce I, Byrne E, Marzuki S: Decline in skeletal-muscle mitochondrial respiratory-chain function - possible factor in aging. Lancet 1989, 1:637-639.
• [30]Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, Gage FH: Neurogenesis in the adult human hippocampus. Nat Med 1998, 4:1313-1317.
• [31]Welle S: Cellular and molecular basis of age-related sarcopenia. Can J Appl Physiol 2002, 27:19-41.
• [32]Castillo EM, Goodman-Gruen D, Kritz-Silverstein D, Morton DJ, Wingard DL, Barrett-Connor E: Sarcopenia in elderly men and women: the rancho bernardo study. Am J Prev Med 2003, 25:226-231.
• [33]Anstey KJ, von Sanden C, Salim A, O’Kearney R: Smoking as a risk factor for dementia and cognitive decline: a meta-analysis of prospective studies. Am J Epidemiol 2007, 166:367-378.
• [34]Baltes PB, Lindenberger U: Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? Psychol Aging 1997, 12:12-21.
• [35]Lindenberger U, Baltes PB: Sensory functioning and intelligence in old-age - a strong connection. Psychol Aging 1994, 9:339-355.
• [36]Anstey KJ, Smith GA: Interrelationships among biological markers of aging, health, activity, acculturation, and cognitive performance in late adulthood. Psychol Aging 1999, 14:605-618.
• [37]Christensen H, Mackinnon AJ, Korten A, Jorm AF: The “common cause hypothesis” of cognitive aging: evidence for not only a common factor but also specific associations of with vision and grip strength in a cross-sectional analysis. Psychol Aging 2001, 16:588-599.
• [38]Young A, Stokes M, Crowe M: The size and strength of the quadriceps muscles of old and young men. Clin Physiol 1985, 5:145-154.
• [39]Burns JM, Johnson DK, Watts A, Swerdlow RH, Brooks WM: Reduced lean mass in early alzheimer disease and its association with brain atrophy. Arch Neurol 2010, 67:428-433.
• [40]Auyeung T, Lee J, Kwok T, Woo J: Physical frailty predicts future cognitive decline - a four-year prospective study in 2737 cognitively normal older adults. J Nutr Health Aging 2011, 15:690-694.
• [41]Nourhashemi F, Andrieu S, Gillette-Guyonnet S, Reynish E, Albarede J-L, Grandjean H, Vellas B: Is there a relationship between fat-free soft tissue mass and low cognitive function? Results from a study of 7,105 women. J Am Geriatr Soc 2002, 50:1796-1801.
• [42]Wirth R, Smoliner C, Sieber C, Volkert D: Cognitive function is associated with body composition and nutritional risk cognitive function is associated with body composition and nutritional risk of geriatric patients. J Nutr Health Aging 2011, 15:706-710.
• [43]MacLullich AM, Ferguson KJ, Reid LM, Deary IJ, Starr JM, Wardlaw JM, Walker BR, Andrew R, Seckl JR: 11beta-hydroxysteroid dehydrogenase type 1, brain atrophy and cognitive decline. Neurobiol Aging 2012, 33:207. e201-208
• [44]MacLullich AM, Deary IJ, Starr JM, Ferguson KJ, Wardlaw JM, Seckl JR: Plasma cortisol levels, brain volumes and cognition in healthy elderly men. Psychoneuroendocrinology 2005, 30:505-515.
• [45]Ferguson KJ, Wardlaw JM, Deary IJ, MacLullich AMJ: Intracranial area: a validated method for estimating intracranial volume. J Neuroimaging 2005, 15:76-78.
• [46]Kilgour A, Subedi D, Gray C, Deary I, Lawrie S, Wardlaw J, Starr J: Design and validation of a novel method to measure cross-sectional area of neck muscles included during routine MR brain volume imaging. PLoS One 2012. 7.
• [47]Deary I, Strand S, Smith P, Fernandes C: Intelligence and educational achievement. Intelligence 2007, 35:13-21.
• [48]Mori E, Hirono N, Yamashita H, Imamura T, Ikejiri Y, Ikeda M, Kitagaki H, Shimomura T, Yoneda Y: Premorbid brain size as a determinant of reserve capacity against intellectual decline in alzheimer’s disease. Am J Psychiatry 1997, 154:18-24.
• [49]Neisser U, Boodoo G, Bouchard TJ, Boykin AW, Brody N, Ceci SJ, Halpern DF, Loehlin JC, Perloff R, Sternberg RJ, Urbina S: Intelligence: knowns and unknowns. Am Psychol 1996, 51:77-101.
• [50]Mackintosh NJ: IQ and human intelligence. New York, NY, US: Oxford University Press; 1998.