The Effects of Stress on Cognitive Aging, Physiology and Emotion (ESCAPE) Project

BMC Psychiatry

Martin J. Sliwinski⁷  Nilam Ram⁵  Elizabeth Munoz⁹  Jacqueline A. Mogle⁷  Richard B. Lipton²  Mindy J. Katz³  David M. Almeida⁹  Joshua M. Smyth⁶  Christopher G. Engeland⁴  Jennifer E. Graham-Engeland¹  Stacey B. Scott⁸ 

[1] Department of Biobehavioral Health, Pennsylvania State University, Pennsylvania, USA;Department of Neurology, Department of Psychiatry and Behavioral Sciences, Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, USA;Department of Neurology, Albert Einstein College of Medicine, Bronx, USA;Department of Biobehavioral Health and College of Nursing, Pennsylvania State University, Pennsylvania, USA;Department of Human Development and Family Studies, Pennsylvania State University, Pennsylvania, USA;Departments of Biobehavioral Health and Medicine, Pennsylvania State University and Hershey Medical Center, Pennsylvania, USA;Center for Healthy Aging and College of Nursing, Pennsylvania State University, University Park, Pennsylvania 16802, PA, USA;School of Aging Studies, University of South Florida, Tampa, USA;Department of Human Development and Family Studies and Center for Healthy Aging, Pennsylvania State University, Pennsylvania, USA

关键词: Burst measurement design;    Cortisol;    Cytokines;    Unconstructive repetitive thought;    Ecological momentary assessment;    Inflammation;    Aging;    Cognition;    Stress;   

Others  :  1217898
DOI  :  10.1186/s12888-015-0497-7

 received in 2014-12-05, accepted in 2015-05-15,  发布年份 2015

【 摘 要 】

Background

Despite evidence that psychological stress is an important risk factor for age-related cognitive loss, little research has directly evaluated psychological and physiological mediators of the relationship between stressful experiences and cognitive function. A key objective of the ESCAPE (Effects of Stress on Cognitive Aging, Physiology, and Emotion) project is to evaluate whether engaging in stress-related unconstructive repetitive thought (URT) is a pathway through which stressful experiences negatively affect cognitive health over the short- and long-term. Over the short-term, we hypothesize that engaging in URT will deplete attentional resources and result in worse cognitive performance in daily life. Over the long-term, we expect that the effects of chronic stress, from repeated exposure to stressors and regular engagement in URT, will be apparent in dysregulated hypothalamic-pituitary-adrenal (HPA) axis function and inflammation. Over time, stress-related physiological dysregulation will result in accelerated cognitive decline.

Methods/Design

This study utilizes a prospective longitudinal measurement-burst design. A systematic probability sample of participants aged 25 to 65 is recruited from residents of the Bronx, NY. Consenting participants complete a baseline assessment and follow-up waves at 9, 18, and 27 months post-baseline. At each wave, participants complete a 14 day measurement burst of brief surveys and cognitive assessments delivered via study smartphones during daily life. Participants provide saliva samples four times each day for five days during the measurement burst and fasting blood samples at the end of each burst from which cortisol and dehydroepiandrosterone sulfate (DHEAS), circulating inflammatory markers, and stimulated inflammatory responses to lipopolysaccharide in whole blood are determined.

Discussion

This study takes a multi-pronged approach to assessing stress (i.e., early adversity, chronic strains, major events, daily hassles), psychological mediators (e.g., URT), biological mechanisms (i.e., HPA function, inflammation) and outcomes across different time-scales (i.e., momentary cognitive performance, cognitive decline across years). The systematic probability sample is locally representative and can be compared with national norms on key markers of health and well-being. The findings will improve our understanding of how environmental, psychological, and physiological stress-related influences accumulate to affect cognitive health and identify potential targets (e.g., URT, inflammation) for prevention and intervention promoting cognitive health.

【 授权许可】

   
2015 Scott et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

【 参考文献 】

• [1]Plassman BL, Langa KM, McCammon RJ, Fisher GG, Potter GG, Burke JR, Steffens DC, Foster NL, Giordani B, Unverzagt FW, Welsh-Bohmer KA, Heeringa SG, Weir DR, Wallace RB: Incidence of dementia and cognitive impairment, not dementia in the united states. Ann Neurol 2011, 70:418-426.
• [2]Hebert LE, Weuve J, Scherr PA, Evans DA: Alzheimer disease in the United States (2010-2050) estimated using the 2010 census. Neurology 2013, 80:1778-1783.
• [3]Alzheimer’s Association. 2011 Alzheimer’s Disease Facts and Figures. 2011, 7:1–68
• [4]Charles ST, Piazza JR, Mogle J, Sliwinski MJ, Almeida DM: The wear and tear of daily stressors on mental health. Psychological Science 2013, 24:733-741.
• [5]Wilson RS, Bennett DA, de Leon CF M, Bienias JL, Morris MC, Evans DA: Distress proneness and cognitive decline in a population of older persons. Psychoneuroendocrinology 2005, 30:11-17.
• [6]Epel ES, Blackburn EH, Lin J, Dhabhar FS, Adler NE, Morrow JD, Cawthon RM: Accelerated telomere shortening in response to life stress. PNAS 2004, 101:17312-17315.
• [7]Piazza JR, Charles ST, Sliwinski MJ, Mogle J, Almeida DM: Affective reactivity to daily stressors and long-term risk of reporting a chronic physical health condition. Annals of Behavioral Medicine 2012, 45:110-120.
• [8]Andel R, Crowe M, Kareholt I, Wastesson J, Parker MG: Indicators of job strain at midlife and cognitive functioning in advanced old age. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences 2011, 66B:287-291.
• [9]Sliwinski MJ, Smyth JM, Hofer SM, Stawski RS: Intraindividual coupling of daily stress and cognition. Psychology and Aging 2006, 21:545-557.
• [10]Stawski RS, Sliwinski MJ, Smyth JM: Stress-related cognitive interference predicts cognitive function in old age. Psychology and Aging 2006, 21:535-544.
• [11]Kahneman D: Attention & Effort. Prentice-Hall, Englewood Cliffs; 1973.
• [12]Lazarus RS: Stress and Emotion: A New Synthesis. Springer, New York; 1999.
• [13]Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW: From inflammation to sickness and depression: when the immune system subjugates the brain. Nature Reviews Neuroscience 2008, 9:46-56.
• [14]Korten NCM, Sliwinski MJ, Comijs HC, Smyth JM: Mediators of the relationship between life events and memory functioning in a community sample of adults: life events, memory functioning, and possible mediators. Applied Cognitive Psychology 2014, 28:626-633.
• [15]Aggarwal NT, Wilson RS, Beck TL, Rajan KB, de Leon CF M, Evans DA, Everson-Rose SA: Perceived stress and change in cognitive function among adults 65 years and older. Psychosomatic Medicine 2014, 76:80-85.
• [16]Wilson RS, Arnold SE, Schneider JA, Li Y, Bennett DA: Chronic distress, age-related neuropathology, and late-life dementia. Psychosomatic Medicine 2007, 69:47-53.
• [17]McEwen BS: Stress, adaptation, and disease. Allostasis and allostatic load. Ann N Y Acad Sci 1998, 840:33-44.
• [18]Chen E, Miller GE, Lachman ME, Gruenewald TL, Seeman TE: Protective factors for adults from low-childhood socioeconomic circumstances: The benefits of shift-and-persist for allostatic load. Psychosomatic Medicine 2012, 74:178-186.
• [19]Black PH: Stress and the inflammatory response: A review of neurogenic inflammation. Brain, Behavior, and Immunity 2002, 16:622-653.
• [20]Miller GE, Chen E, Parker KJ: Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychological Bulletin 2011, 137:959-997.
• [21]Sapolsky RM, Krey LC, McEwen BS: The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocrine Reviews 1986, 7:284-301.
• [22]Kiecolt-Glaser JK, Preacher KJ, MacCallum RC, Atkinson C, Malarkey WB, Glaser R: Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proceedings of the National Academy of Sciences 2003, 100:9090-9095.
• [23]Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NPV, Thakur M, McEwen BS, Hauger RL, Meaney MJ: Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience 1998, 1:69-73.
• [24]Seeman TE, McEwen BS, Rowe JW, Singer BH: Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. PNAS 2001, 98:4770-4775.
• [25]Yaffe K, Lindquist K, Penninx BW, Simonsick EM, 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, 61:76-80.
• [26]Brosschot JF, Pieper S, Thayer JF: Expanding stress theory: Prolonged activation and perseverative cognition. Psychoneuroendocrinology 2005, 30:1043-1049.
• [27]Smyth J, Zawadzki M, Gerin W: Stress and disease: a structural and functional analysis: Chronic stress and health. Social and Personality Psychology Compass 2013, 7:217-227.
• [28]Segerstrom SC, Stanton AL, Alden LE, Shortridge BE: A multidimensional structure for repetitive thought: what’s on your mind, and how, and how much? J Pers Soc Psychol 2003, 85:909-921.
• [29]Watkins ER: Constructive and unconstructive repetitive thought. Psychological Bulletin 2008, 134:163-206.
• [30]Moberly NJ, Watkins ER: Ruminative self-focus and negative affect: An experience sampling study. Journal of Abnormal Psychology 2008, 117:314-323.
• [31]Nesselroade JR: The warp and the woof of the developmental fabric. In Visions of aesthetics, the environment & development: The legacy of Joachim F. Wohlwill. Edited by Downs RM, Liben LS, Palermo DS. Lawrence Erlbaum Associates Inc, Hillsdale; 1991:213-240.
• [32]Sliwinski MJ: Measurement-burst designs for social health research. Social and Personality Psychology Compass 2008, 2:245-261.
• [33]Sliwinski MJ: Approaches to modeling intraindividual and interindividual facets of change for developmental research. In Handbook of life-span development. Edited by Fingerman KL, Berg CA, Smith J, Antonucci TC. Springer Publishing Co, New York; 2011:1-25.
• [34]Ram N, Gerstorf D: Time-structured and net intraindividual variability: Tools for examining the development of dynamic characteristics and processes. Psychology and Aging 2009, 24:778-791.
• [35]Vitaliano PP, Echeverria D, Yi J, Phillips PEM, Young H, Siegler IC: Psychophysiological mediators of caregiver stress and differential cognitive decline. Psychology and Aging 2005, 20:402-411.
• [36]Baum A, Garofalo JP, Yali AM: Socioeconomic status and chronic stress: Does stress account for SES effects on health? Annals of the New York Academy of Sciences 1999, 896:131-144.
• [37]Wegner DM, Zanakos S: Chronic thought suppression. Journal of Personality 1994, 62:615-640.
• [38]Trapnell PD, Campbell JD: Private self-consciousness and the five-factor model of personality: Distinguishing rumination from reflection. Journal of Personality and Social Psychology 1999, 76:284-304.
• [39]Beck MD: Aaron: The evolution of the cognitive model of depression and its neurobiological correlates. Am J Psychiatry 2008, 165:969-977.
• [40]Raven J: The Raven’s Progressive Matrices: Change and Stability over Culture and Time. Cognitive Psychology 2000, 41:1-48.
• [41]Shipley WC: A self-administering scale for measuring intellectual impairment and deterioration. The Journal of Psychology: Interdisciplinary and Applied 1940, 9:371-377.
• [42]Conway ARA, Cowan N, Bunting MF, Therriault DJ, Minkoff SRB: A latent variable analysis of working memory capacity, short-term memory capacity, processing speed, and general fluid intelligence. Intelligence 2002, 30:163-183.
• [43]Daneman M, Carpenter PA: Individual differences in working memory and reading. Journal of Verbal Learning and Verbal Behavior 1980, 19:450-466.
• [44]Waters GS, Caplan D: The reliability and stability of verbal working memory measures. Behavior Research Methods, Instruments, & Computers 2003, 35:550-564.
• [45]Schmidt M: Rey Auditory Verbal Learning Test. Western Psychological Services, Los Angeles; 1996.
• [46]Schmiedek F, Lovden M, Lindenberger U: Hundred days of cognitive training enhance broad cognitive abilities in adulthood: Findings from the COGITO study. Front Aging Neurosci 2010, 2:1-10.
• [47]Verhaeghen P, Basak C: Ageing and switching of the focus of attention in working memory: results from a modified N -Back task. Quarterly Journal of Experimental Psychology: Section A 2005, 58:134-154.
• [48]Miller GE, Chen E, Zhou ES: If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin 2007, 133:25-45.
• [49]Boudarene M, Legros JJ, Timsit-Berthier M: Study of the stress response: role of anxiety, cortisol and DHEAs. Encephale 2002, 28:139-146.
• [50]Heffner KL: Neuroendocrine Effects of Stress on Immunity in the Elderly: Implications for Inflammatory Disease. Immunology and Allergy Clinics of North America 2011, 31:95-108.
• [51]Magri F, Cravello L, Barili L, Sarra S, Cinchetti W, Salmoiraghi F, Micale G, Ferrari E: Stress and dementia: The role of the hypothalamicpituitary-adrenal axis. Aging Clinical and Experimental Research 2006, 18:167-170.
• [52]Bauer ME, Jeckel CMM, Luz C: The role of stress factors during aging of the immune system. Annals of the New York Academy of Sciences 2009, 1153:139-152.
• [53]Thomas N, Morris HA, Scopacasa F, Wishart JM, Need AG: Relationships between age, dehydro-epiandrosterone sulphate and plasma glucose in healthy men. Age and Ageing 1999, 28:217-220.
• [54]Morrison MF, Redei E, TenHave T, Parmelee P, Boyce AA, Sinha PS, Katz IR: Dehydroepiandrosterone sulfate and psychiatric measures in a frail, elderly residential care population. Biological Psychiatry 2000, 47:144-150.
• [55]De Bruin VMS, Vieira MCM, Rocha MNM, Viana GSB: Cortisol and dehydroepiandosterone sulfate plasma levels and their relationship to aging, cognitive function, and dementia. Brain and Cognition 2002, 50:316-323.
• [56]Ravaglia G, Forti P, Maioli F, Sacchetti L, Nativio V, Scali CR, Mariani E, Zanardi V, Stefanini A, Macini PL: Dehydroepiandrosterone-sulfate serum levels and common age-related diseases: Results from a cross-sectional Italian study of a general elderly population. Experimental Gerontology 2002, 37:701-712.
• [57]Rhodes B, Fürnrohr BG, Vyse TJ: C-reactive protein in rheumatology: Biology and genetics. Nature Reviews Rheumatology 2011, 7:282-289.
• [58]Snijders T, Bosker R: Multilevel Modeling: An Introduction to Basic and Advanced Multilevel Modeling. Sage, London; 1999.
• [59]Bauer DJ, Preacher KJ, Gil KM: Conceptualizing and testing random indirect effects and moderated mediation in multilevel models: New procedures and recommendations. Psychological Methods 2006, 11:142-163.
• [60]Mehta PD, Neale MC: People are variables too: Multilevel structural equations modeling. Psychol Methods 2005, 10:259-284.
• [61]Bollen KA. Structural Equation Models. In Encyclopedia of Biostatistics. John Wiley & Sons, Ltd; 2005
• [62]Sliwinski MJ, Almeida DM, Smyth J, Stawski RS: Intraindividual change and variability in daily stress processes: Findings from two measurement-burst diary studies. Psychology and Aging 2009, 24:828-840.
• [63]Hedeker D, Gibbons RD: Application of random-effects pattern-mixture models for missing data in longitudinal studies. Psychological Methods 1997, 2:64-78.
• [64]Cella D, Yount S, Rothrock N, Gershon R, Cook K, Reeve B, Ader D, Fries JF, Bruce B, Rose M: The Patient-Reported Outcomes Measurement Information System (PROMIS). Med Care 2007, 45(5 Suppl 1):S3-S11.
• [65]Graham JE, Christian LM, Kiecolt-Glaser JK: Stress, age, and immune function: Toward a lifespan approach. J Behav Med 2006, 29:389-400.
• [66]Pulopulos MM, Hidalgo V, Almela M, Puig-Perez S, Villada C, Salvador A: Hair cortisol and cognitive performance in healthy older people. Psychoneuroendocrinology 2014, 44:100-111.
• [67]Lee BK, Glass TA, McAtee MJ, Wand GS, Bandeen-Roche K, Bolla KI, Schwartz BS: Associations of salivary cortisol with cognitive function in the Baltimore memory study. Arch Gen Psychiatry 2007, 64:810-818.
• [68]Koyama A, O’Brien J, Weuve J, Blacker D, Metti AL, Yaffe K: The role of peripheral inflammatory markers in dementia and alzheimer’s disease: a meta-analysis. J Gerontol A Biol Sci Med Sci 2013, 68:433-440.
• [69]Wichmann MA, Cruickshanks KJ, Carlsson CM, Chappell R, Fischer ME, Klein BEK, Klein R, Tsai MY, Schubert CR: Long-term systemic inflammation and cognitive impairment in a population-based cohort. Journal of the American Geriatrics Society 2014, 62:1683-1691.
• [70]Turner RJ, Wheaton B, Lloyd DA: The Epidemiology of Social Stress. American Sociological Review 1995, 60:104.
• [71]Williams DR, Yu Y, Jackson JS, Anderson NB: Racial differences in physical and mental health socio-economic status, stress and discrimination. J Health Psychol 1997, 2:335-351.
• [72]Mujahid MS, Roux AVD, Morenoff JD, Raghunathan T: Assessing the measurement properties of neighborhood scales: From psychometrics to ecometrics. Am J Epidemiol 2007, 165:858-867.
• [73]Cohen S, Kamarck T, Mermelstein R: A Global Measure of Perceived Stress. Journal of Health and Social Behavior 1983, 24:385-396.
• [74]Almeida DM, Wethington E, Kessler RC: The daily inventory of stressful events an interview-based approach for measuring daily stressors. Assessment 2002, 9:41-55.
• [75]Weiss DS, Marmar CR: The impact of event scale-Revised. In Assessing psychological trauma and PTSD. Edited by Wilson J, Keane M. Guilford Press, New York; 1996:399-411.
• [76]Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: The PANASscales. Journal of Personality and Social Psychology. 1988;54.
• [77]Diener E, Emmons RA, Larsen RJ, Griffin S: The satisfaction with life scale. Journal of Personality Assessment 1985, 49:71.
• [78]Goldberg LR, Johnson JA, Eber HW, Hogan R, Ashton MC, Cloninger CR, Gough HG: The international personality item pool and the future of public-domain personality measures. Journal of Research in Personality 2006, 40:84-96.
• [79]Spielberger CD, Sydeman SJ, Owen AE, Marsh BJ: Measuring anxiety and anger with the state-trait anxiety inventory (STAI) and the state-trait anger expression inventory. In The use of psychological testing for treatment planning and outcomes assessment. 2nd edition. Lawrence Erlbaum Associates Publishers, Mahwah; 1999:993-1021.
• [80]MacPhillamy DJ, Lewinsohn PM: The pleasant events schedule: Studies on reliability, validity, and scale intercorrelation. Journal of Consulting and Clinical Psychology 1982, 50:363-380.
• [81]Bohlmeijer E, ten Klooster PM, Fledderus M, Veehof M, Baer R: Psychometric Properties of the Five Facet Mindfulness Questionnaire in Depressed Adults and Development of a Short Form. Assessment 2011, 18:308-320.
• [82]Evans DE, Rothbart MK: Developing a model for adult temperament. Journal of Research in Personality 2007, 41:868-888.
• [83]Scheier MF, Carver CS: Optimism, coping, and health: Assessment and implications of generalized outcome expectancies. Health Psychology 1985, 4:219-247.