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A prospective study of diurnal cortisol and cognitive function in community-dwelling elderly people

Published online by Cambridge University Press:  09 October 2009

I. Beluche ,
I. Carrière ,
K. Ritchie  and
M. L. Ancelin
I. Beluche
Affiliation:
Inserm, U888, University of Montpellier 1, Montpellier, France
I. Carrière
Affiliation:
Inserm, U888, University of Montpellier 1, Montpellier, France
K. Ritchie
Affiliation:
Inserm, U888, University of Montpellier 1, Montpellier, France
M. L. Ancelin*
Affiliation:
Inserm, U888, University of Montpellier 1, Montpellier, France
*
*Address for correspondence: M. L. Ancelin, Ph.D., Inserm U888, La Colombiere Hospital, pav 42, 39 avenue Flahault, BP 34493, 34093 Montpellier Cedex 5, France. (Email: marie-laure.ancelin@inserm.fr)
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Abstract

Background

Elevated cortisol levels due to hypothalamic–pituitary–adrenal (HPA) axis stress response have been associated with cognitive impairment. However, the causal relationship between stress and subsequent cognitive impairment remains unclear, notably because of the small number of gender-stratified prospective studies.

Method

Salivary cortisol secretion was evaluated in 197 non-depressed community-dwelling elderly people at three time points on the day of hospital attendance for a clinical examination and again on the following day at home, in a distinct environmental context. Cognitive performance was evaluated at baseline and at 2- and 4-year follow-up.

Results

Cross-sectional logistic analyses adjusted for age and education indicated that men with high morning cortisol at the hospital had higher risk of low cognitive performance in verbal fluency [odds ratio (OR) 3.0, p=0.05] and visuospatial performance (OR 5.1, p=0.03). Impairment in verbal fluency was observed in women with moderate high morning cortisol (OR 3.6, p=0.05) or moderate slow diurnal rhythm (OR 3.7, p=0.04). In longitudinal analyses, slow diurnal rhythm (flatter slope) was associated with decline over 4 years in visuospatial performance (OR 7.7, p=0.03) and visual memory (OR 4.1, p=0.03) in men, and in verbal fluency (OR 6.0, p=0.01) in women. High morning cortisol was associated with decline in visual memory in women (OR 5.1, p=0.06).

Conclusions

HPA axis dysregulation seems to be associated with low cognitive performance in the elderly. Slower cortisol elimination rates could predict cognitive decline affecting principally non-verbal functioning in men and verbal functioning in women. The effects are independent of environmental context, apolipoprotein E (ApoE) genotype or psychopathology. Interventions blocking this pathway may provide new therapeutic options to prevent cognitive decline.

Keywords

CognitioncortisolelderlyHPA axisstress
Type
Original Articles
Information
Psychological Medicine , Volume 40 , Issue 6 , June 2010 , pp. 1039 - 1049
Copyright
Copyright © Cambridge University Press 2009

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References

APA (1994). Diagnostic and Statistical Manual of Mental Disorders (DSM-IV). American Psychiatric Association: Washington, DC.Google Scholar
Benton, A (1965). Manual for the application of the visual retention test. Clinical and experimental applications [in French]. Centre de Psychologie Appliquée: Paris.Google Scholar
Blair, JR, Spreen, O (1989). Predicting premorbid IQ: a revision of the National Adult Reading Test. Clinical Neuropsychology 3, 129–136.Google Scholar
Carlson, LE, Sherwin, BB (1999). Relationships among cortisol (CRT), dehydroepiandrosterone-sulfate (DHEAS), and memory in a longitudinal study of healthy elderly men and women. Neurobiology of Aging 20, 315–324.Google Scholar
Chaudieu, I, Beluche, I, Norton, J, Boulenger, JP, Ritchie, K, Ancelin, ML (2008). Abnormal reactions to environmental stress in elderly persons with anxiety disorders: evidence from a population study of diurnal cortisol changes. Journal of Affective Disorders 106, 307–313.Google Scholar
De Kloet, ER, Vreugdenhil, E, Oitzl, MS, Joels, M (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews 19, 269–301.Google Scholar
Dufouil, C, Richard, F, Fievet, N, Dartigues, JF, Ritchie, K, Tzourio, C, Amouyel, P, Alperovitch, A (2005). APOE genotype, cholesterol level, lipid-lowering treatment, and dementia: the Three-City Study. Neurology 64, 1531–1538.Google Scholar
Folstein, MF, Folstein, SE, McHugh, PR (1975). ‘Mini-mental state’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research 12, 189–198.Google Scholar
Gomez, RG, Fleming, SH, Keller, J, Flores, B, Kenna, H, DeBattista, C, Solvason, B, Schatzberg, AF (2006). The neuropsychological profile of psychotic major depression and its relation to cortisol. Biological Psychiatry 60, 472–478.Google Scholar
Greendale, GA, Kritz-Silverstein, D, Seeman, T, Barrett-Connor, E (2000). Higher basal cortisol predicts verbal memory loss in postmenopausal women: Rancho Bernardo Study. Journal of the American Geriatrics Society 48, 1655–1658.CrossRefGoogle ScholarPubMed
Hellhammer, DH, Kirschbaum, C, Belkien, L (1987). Measurement of salivary cortisol under psychological stimulation. In Advanced Methods in Psychobiology (ed. Hingtgen, J. N., Hellhammer, D. H. and Huppman, G.), pp. 281–289. Hogrefe: Toronto.Google Scholar
Isaacs, B, Kennie, AT (1973). The Set Test as an aid to the detection of dementia in old people. British Journal of Psychiatry 123, 467–470.CrossRefGoogle Scholar
Kalmijn, S, Launer, LJ, Stolk, RP, de Jong, FH, Pols, HA, Hofman, A, Breteler, MM, Lamberts, SW (1998). A prospective study on cortisol, dehydroepiandrosterone sulfate, and cognitive function in the elderly. Journal of Clinical Endocrinology and Metabolism 83, 3487–3492.CrossRefGoogle ScholarPubMed
Karlamangla, AS, Singer, BH, Chodosh, J, McEwen, BS, Seeman, TE (2005). Urinary cortisol excretion as a predictor of incident cognitive impairment. Neurobiology of Aging 26, 80–84.Google Scholar
Kirschbaum, C, Hellhammer, DH (1989). Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 22, 150–169.CrossRefGoogle ScholarPubMed
Kirschbaum, C, Hellhammer, DH (1994). Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19, 313–333.Google Scholar
Kumsta, R, Entringer, S, Koper, JW, van Rossum, EF, Hellhammer, DH, Wust, S (2007). Sex specific associations between common glucocorticoid receptor gene variants and hypothalamus-pituitary-adrenal axis responses to psychosocial stress. Biological Psychiatry 62, 863–869.CrossRefGoogle ScholarPubMed
Lecrubier, Y, Sheehan, D, Weiller, E, Amorim, P, Bonara, I, Sheehan, K, Janavs, J, Dunbar, G (1997). The Mini International Neuropsychiatric Interview (MINI), a short diagnostic interview: reliability and validity according to the CIDI. European Psychiatry 12, 232–241.CrossRefGoogle Scholar
Lee, BK, Glass, TA, McAtee, MJ, Wand, GS, Bandeen-Roche, K, Bolla, KI, Schwartz, BS (2007). Associations of salivary cortisol with cognitive function in the Baltimore memory study. Archives of General Psychiatry 64, 810–818.Google Scholar
Lee, BK, Glass, TA, Wand, GS, McAtee, MJ, Bandeen-Roche, K, Bolla, KI, Schwartz, BS (2008). Apolipoprotein E genotype, cortisol, and cognitive function in community-dwelling older adults. American Journal of Psychiatry 165, 1456–1464.CrossRefGoogle ScholarPubMed
Li, G, Cherrier, MM, Tsuang, DW, Petrie, EC, Colasurdo, EA, Craft, S, Schellenberg, GD, Peskind, ER, Raskind, MA, Wilkinson, CW (2006). Salivary cortisol and memory function in human aging. Neurobiology of Aging 27, 1705–1714.Google Scholar
Lupien, SJ, de Leon, M, de Santi, S, Convit, A, Tarshish, C, Nair, NP, Thakur, M, McEwen, BS, Hauger, RL, Meaney, MJ (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience 1, 69–73.CrossRefGoogle ScholarPubMed
Lupien, SJ, Fiocco, A, Wan, N, Maheu, F, Lord, C, Schramek, T, Tu, MT (2005). Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30, 225–242.Google Scholar
Lupien, SJ, Gaudreau, S, Tchiteya, BM, Maheu, F, Sharma, S, Nair, NP, Hauger, RL, McEwen, BS, Meaney, MJ (1997). Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. Journal of Clinical Endocrinology and Metabolism 82, 2070–2075.Google Scholar
Lupien, S, Lecours, AR, Lussier, I, Schwartz, G, Nair, NP, Meaney, MJ (1994). Basal cortisol levels and cognitive deficits in human aging. Journal of Neuroscience 14, 2893–2903.Google Scholar
Lupien, SJ, Maheu, F, Tu, M, Fiocco, A, Schramek, TE (2007). The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain and Cognition 65, 209–237.Google Scholar
MacLullich, AM, Deary, IJ, Starr, JM, Ferguson, KJ, Wardlaw, JM, Seckl, JR (2005). Plasma cortisol levels, brain volumes and cognition in healthy elderly men. Psychoneuroendocrinology 30, 505–515.Google Scholar
Meaney, MJ, Szyf, M, Seckl, JR (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends in Molecular Medicine 13, 269–277.Google Scholar
O'Hara, R, Schroder, CM, Mahadevan, R, Schatzberg, AF, Lindley, S, Fox, S, Weiner, M, Kraemer, HC, Noda, A, Lin, X, Gray, HL, Hallmayer, JF (2007). Serotonin transporter polymorphism, memory and hippocampal volume in the elderly: association and interaction with cortisol. Molecular Psychiatry 12, 544–555.CrossRefGoogle ScholarPubMed
Otte, C, Hart, S, Neylan, TC, Marmar, CR, Yaffe, K, Mohr, DC (2005). A meta-analysis of cortisol response to challenge in human aging: importance of gender. Psychoneuroendocrinology 30, 80–91.Google Scholar
Radloff, L (1977). The CES-D scale: a self-report depression scale for research in the general population. Applied Psychological Measurement 1, 385–401.Google Scholar
Reitan, R (1965). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills 8, 271–276.CrossRefGoogle Scholar
Ritchie, K, Artero, S, Beluche, I, Ancelin, ML, Mann, A, Dupuy, AM, Malafosse, A, Boulenger, JP (2004). Prevalence of DSM-IV psychiatric disorder in the French elderly population. British Journal of Psychiatry 184, 147–152.CrossRefGoogle ScholarPubMed
Sandeep, TC, Yau, JL, MacLullich, AM, Noble, J, Deary, IJ, Walker, BR, Seckl, JR (2004). 11Beta-hydroxysteroid dehydrogenase inhibition improves cognitive function in healthy elderly men and type 2 diabetics. Proceedings of the National Academy of Sciences USA 101, 6734–6739.CrossRefGoogle ScholarPubMed
Sauro, MD, Jorgensen, RS, Pedlow, CT (2003). Stress, glucocorticoids, and memory: a meta-analytic review. Stress 6, 235–245.Google Scholar
Seeman, TE, McEwen, BS, Singer, BH, Albert, MS, Rowe, JW (1997). Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. Journal of Clinical Endocrinology and Metabolism 82, 2458–2465.Google Scholar
Sephton, SE, Sapolsky, RM, Kraemer, HC, Spiegel, D (2000). Diurnal cortisol rhythm as a predictor of breast cancer survival. Journal of the National Cancer Institute 92, 994–1000.Google Scholar
Van Cauter, E, Leproult, R, Kupfer, DJ (1996). Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol. Journal of Clinical Endocrinology and Metabolism 81, 2468–2473.Google Scholar
Wang, J, Korczykowski, M, Rao, H, Fan, Y, Pluta, J, Gur, RC, McEwen, BS, Detre, JA (2007). Gender difference in neural response to psychological stress. Social Cognitive and Affective Neuroscience 2, 227–239.Google Scholar
WHO (1992). The ICD-10 Classification of Mental and Behavioral Disorders: Clinical Descriptions and Diagnostic Guidelines. World Health Organization: Geneva.Google Scholar
Wolf, OT (2003). HPA axis and memory. Best Practice and Research. Clinical Endocrinology and Metabolism 17, 287–299.Google Scholar
Wright, CE, Kunz-Ebrecht, SR, Iliffe, S, Foese, O, Steptoe, A (2005). Physiological correlates of cognitive functioning in an elderly population. Psychoneuroendocrinology 30, 826–838.Google Scholar