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Late-life cynical hostility is associated with white matter alterations and the risk of Alzheimer's disease

Published online by Cambridge University Press:  14 April 2021

Fabienne Cyprien ,
Claudine Berr ,
Jerome J. Maller ,
Chantal Meslin ,
Mélissa Gentreau ,
Thibault Mura ,
Audrey Gabelle ,
Philippe Courtet ,
Karen Ritchie  and
Marie-Laure Ancelin
...Show all authors
Fabienne Cyprien
Affiliation:
IGF, Univ Montpellier, CNRS, INSERM, Montpellier, France CHU Montpellier, Montpellier, France
Claudine Berr
Affiliation:
INM, Univ Montpellier, INSERM, Montpellier, France
Jerome J. Maller
Affiliation:
Monash Alfred Psychiatry Research Centre, The Alfred & Monash University School of Psychology and Psychiatry, Melbourne, Australia
Chantal Meslin
Affiliation:
Centre for Mental Health Research, Australian National University, Canberra, Australia
Mélissa Gentreau
Affiliation:
IGF, Univ Montpellier, CNRS, INSERM, Montpellier, France
Thibault Mura
Affiliation:
INM, Univ Montpellier, INSERM, Montpellier, France CHU Nîmes, Nîmes, France
Audrey Gabelle
Affiliation:
CHU Montpellier, Montpellier, France INM, Univ Montpellier, INSERM, Montpellier, France
Philippe Courtet
Affiliation:
IGF, Univ Montpellier, CNRS, INSERM, Montpellier, France CHU Montpellier, Montpellier, France
Karen Ritchie
Affiliation:
INM, Univ Montpellier, INSERM, Montpellier, France Centre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, UK
Marie-Laure Ancelin
Affiliation:
INM, Univ Montpellier, INSERM, Montpellier, France
Sylvaine Artero*
Affiliation:
IGF, Univ Montpellier, CNRS, INSERM, Montpellier, France
*
Author for correspondence: Sylvaine Artero, E-mail: [email protected]
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Abstract

Background

Cynical hostility (CH), a specific dimension of hostility that consists of a mistrust of others, has been suggested as a high-risk trait for dementia. However, the influence of CH on the incidence of Alzheimer's disease (AD) remains poorly understood. This study investigated whether late-life CH is associated with AD risk and structural neuroimaging markers of AD.

Methods

In community-dwelling older adults from the French ESPRIT cohort (n = 1388), incident dementia rate according to CH level was monitored during an 8-year follow-up and analyzed using Cox proportional hazards regression models. Brain magnetic resonance imaging volumes were measured at baseline (n = 508). Using automated segmentation procedures (Freesurfer 6.0), the authors assessed brain grey and white volumes on all magnetic resonance imaging scans. They also measured white matter hyperintensities volumes using semi-automated procedures. Mean volumes according to the level of CH were compared using ANOVA.

Results

Eighty-four participants developed dementia (32 with AD). After controlling for potential confounders, high CH was predictive of AD (HR 2.74; 95% CI 1.10–6.85; p = 0.030) and all dementia types are taken together (HR 2.30; 95% CI 1.10–4.80; p = 0.027). High CH was associated with white matter alterations, particularly smaller anterior corpus callosum volume (p < 0.01) after False Discovery Rate correction, but not with grey matter volumes.

Conclusions

High CH in late life is associated with cerebral white matter alterations, designated as early markers of dementia, and higher AD risk. Identifying lifestyle and biological determinants related to CH could provide clues on AD physiopathology and avenues for prevention strategies.

Keywords

PersonalityAlzheimer DiseaseCerebral white mattercorpus callosumcohortrisk factor
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 15 , November 2022 , pp. 3636 - 3645
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Amieva, H., Le Goff, M., Millet, X., Orgogozo, J. M., Pérès, K., Barberger-Gateau, P., … Dartigues, J. F. (2008). Prodromal Alzheimer's disease: Successive emergence of the clinical symptoms. Annals of Neurology, 64, 492–498.10.1002/ana.21509CrossRefGoogle ScholarPubMed
Amlien, I. K., & Fjell, A. M. (2014). Diffusion tensor imaging of white matter degeneration in Alzheimer's disease and mild cognitive impairment. Neuroscience, 276, 206–215.10.1016/j.neuroscience.2014.02.017CrossRefGoogle ScholarPubMed
Apostolova, L. G., Lu, P., Rogers, S., Dutton, R. A., Hayashi, K. M., Toga, A. W., … Thompson, P. M. (2008). 3D mapping of language networks in clinical and pre-clinical Alzheimer's disease. Brain and Language, 104, 33–41.CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289–300.CrossRefGoogle Scholar
Benton, A. (1965). Manuel pour l'Application du Test de Retention Visuelle: Applications Cliniques et Experimentales (2nd ed). Paris: Centre de psychologie appliquée.Google Scholar
Braak, H., & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82, 239–259.CrossRefGoogle ScholarPubMed
Braskie, M. N., & Thompson, P. M. (2014). A focus on structural brain imaging in the Alzheimer's disease neuroimaging initiative. Biological Psychiatry, 75, 527–533.CrossRefGoogle ScholarPubMed
Brickman, A. M., Sneed, J. R., Provenzano, F. A., Garcon, E., Johnert, L., Muraskin, J., … Roose, S. P. (2011). Quantitative approaches for assessment of white matter hyperintensities in elderly populations. Psychiatry Research, 193, 101–106.10.1016/j.pscychresns.2011.03.007CrossRefGoogle ScholarPubMed
Brydon, L., Lin, J., Butcher, L., Hamer, M., Erusalimsky, J. D., Blackburn, E. H., & Steptoe, A. (2012). Hostility and cellular aging in men from the Whitehall II cohort. Biological Psychiatry, 71, 767–773.10.1016/j.biopsych.2011.08.020CrossRefGoogle ScholarPubMed
Buss, A. H., & Durkee, A. (1957). An inventory for assessing different kinds of hostility. Journal of Consulting Psychology, 21, 343–349.CrossRefGoogle ScholarPubMed
Cipriani, G., Borin, G., Del Debbio, A., & Di Fiorino, M. (2015). Personality and dementia. The Journal of Nervous and Mental Disease, 203, 210–214.10.1097/NMD.0000000000000264CrossRefGoogle ScholarPubMed
Commenges, D., Letenneur, L., Joly, P., Alioum, A., & Dartigues, J. F. (1998). Modelling age-specific risk: Application to dementia. Statistics in Medicine, 17, 1973–1988.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Cook, W. W., & Medley, D. M. (1954). Proposed hostility and Pharisaic-virtue scales for the MMPI. Journal of Applied Psychology, 38, 414–418.10.1037/h0060667CrossRefGoogle Scholar
Cyprien, F., Courtet, P., Maller, J., Meslin, C., Ritchie, K., Ancelin, M.-L., & Artero, S. (2019). Increased serum C-reactive protein and corpus callosum alterations in older adults. Aging and Disease, 10, 463–469.10.14336/AD.2018.0329CrossRefGoogle ScholarPubMed
Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9, 179–194.CrossRefGoogle ScholarPubMed
Damian, R. I., Spengler, M., Sutu, A., & Roberts, B. W. (2019). Sixteen going on sixty-six: A longitudinal study of personality stability and change across 50 years. Journal of Personality and Social Psychology, 117, 674–695.10.1037/pspp0000210CrossRefGoogle ScholarPubMed
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31, 968–980.10.1016/j.neuroimage.2006.01.021CrossRefGoogle ScholarPubMed
Dufouil, C., Richard, F., Fiévet, N., Dartigues, J. F., Ritchie, K., Tzourio, C., … Alpérovitch, A. (2005). APOE genotype, cholesterol level, lipid-lowering treatment, and dementia: The three-city study. Neurology, 64, 1531–1538.10.1212/01.WNL.0000160114.42643.31CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M. I., & Dale, A. M. (1999a). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9, 195–207.10.1006/nimg.1998.0396CrossRefGoogle Scholar
Fischl, B., Sereno, M. I., Tootell, R. B., & Dale, A. M. (1999b). High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping, 8, 272–284.3.0.CO;2-4>CrossRefGoogle Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Ségonne, F., Salat, D. H., … Dale, A. M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex (New York, N.Y.: 1991), 14, 11–22.CrossRefGoogle ScholarPubMed
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle Scholar
GBD 2015 Neurological Disorders Collaborator Group (2017). Global, regional, and national burden of neurological disorders during 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. The Lancet. Neurology, 16, 877–897.10.1016/S1474-4422(17)30299-5CrossRefGoogle Scholar
Grober, E., Buschke, H., Crystal, H., Bang, S., & Dresner, R. (1988). Screening for dementia by memory testing. Neurology, 38, 900–903.CrossRefGoogle ScholarPubMed
Gu, J., Strauss, C., Bond, R., & Cavanagh, K. (2015). How do mindfulness-based cognitive therapy and mindfulness-based stress reduction improve mental health and wellbeing? A systematic review and meta-analysis of mediation studies. Clinical Psychology Review, 37, 1–12.CrossRefGoogle ScholarPubMed
Gurol, M. E., Irizarry, M. C., Smith, E. E., Raju, S., Diaz-Arrastia, R., Bottiglieri, T., … Greenberg, S. M. (2006). Plasma beta-amyloid and white matter lesions in AD, MCI, and cerebral amyloid angiopathy. Neurology, 66, 23–29.CrossRefGoogle ScholarPubMed
Hayes, A. F. (2017). Introduction to mediation, moderation, and conditional process analysis, second edition: A regression-based approach. New York, NY: Guilford Publications.Google Scholar
Hughes, J. W., Sherwood, A., Blumenthal, J. A., Suarez, E. C., & Hinderliter, A. L. (2003). Hostility, social support, and adrenergic receptor responsiveness among African-American and white men and women. Psychosomatic Medicine, 65, 582–587.10.1097/01.PSY.0000041546.04128.43CrossRefGoogle ScholarPubMed
Isaacs, B., & Kennie, A. T. (1973). The Set test as an aid to the detection of dementia in old people. The British Journal of Psychiatry: The Journal of Mental Science, 123, 467–470.CrossRefGoogle Scholar
Jack, C. R., Barkhof, F., Bernstein, M. A., Cantillon, M., Cole, P. E., Decarli, C., … Foster, N. L. (2011). Steps to standardization and validation of hippocampal volumetry as a biomarker in clinical trials and diagnostic criterion for Alzheimer's disease. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 7, 474–485.e4.CrossRefGoogle ScholarPubMed
Janicki-Deverts, D., Cohen, S., & Doyle, W. J. (2010). Cynical hostility and stimulated Th1 and Th2 cytokine production. Brain, Behavior, and Immunity, 24, 58–63.10.1016/j.bbi.2009.07.009CrossRefGoogle ScholarPubMed
Just, N., & Alloy, L. B. (1997). The response styles theory of depression: Tests and an extension of the theory. Journal of Abnormal Psychology, 106, 221–229.CrossRefGoogle Scholar
Lerch, J. P., Pruessner, J. C., Zijdenbos, A., Hampel, H., Teipel, S. J., & Evans, A. C. (2005). Focal decline of cortical thickness in Alzheimer's disease identified by computational neuroanatomy. Cerebral Cortex (New York, N.Y.: 1991), 15, 995–1001.CrossRefGoogle ScholarPubMed
Marchant, N. L., Lovland, L. R., Jones, R., Pichet Binette, A., Gonneaud, J., Arenaza-Urquijo, E. M., … PREVENT-AD Research Group (2020). Repetitive negative thinking is associated with amyloid, tau, and cognitive decline. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 16, 1054–1064.10.1002/alz.12116CrossRefGoogle ScholarPubMed
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology, 34, 939–944.CrossRefGoogle ScholarPubMed
Mortamais, M., Reynes, C., Brickman, A. M., Provenzano, F. A., Muraskin, J., Portet, F., … Artero, S. (2013). Spatial distribution of cerebral white matter lesions predicts progression to mild cognitive impairment and dementia. PLoS ONE, 8, e56972.CrossRefGoogle ScholarPubMed
Nakagawa, S., Takeuchi, H., Taki, Y., Nouchi, R., Sekiguchi, A., Kotozaki, Y., … Kawashima, R. (2017). The anterior midcingulate cortex as a neural node underlying hostility in young adults. Brain Structure & Function, 222, 61–70.CrossRefGoogle ScholarPubMed
Neuvonen, E., Rusanen, M., Solomon, A., Ngandu, T., Laatikainen, T., Soininen, H., … Tolppanen, A.-M. (2014). Late-life cynical distrust, risk of incident dementia, and mortality in a population-based cohort. Neurology, 82, 2205–2212.CrossRefGoogle Scholar
Plichart, M., Celermajer, D. S., Zureik, M., Helmer, C., Jouven, X., Ritchie, K., … Empana, J.-P. (2011). Carotid intima-media thickness in plaque-free site, carotid plaques and coronary heart disease risk prediction in older adults. The three-city study. Atherosclerosis, 219, 917–924.10.1016/j.atherosclerosis.2011.09.024CrossRefGoogle ScholarPubMed
Privado, J., Román, F. J., Saénz-Urturi, C., Burgaleta, M., & Colom, R. (2017). Gray and white matter correlates of the Big Five personality traits. Neuroscience, 349, 174–184.10.1016/j.neuroscience.2017.02.039CrossRefGoogle ScholarPubMed
Radanovic, M., Pereira, F. R. S., Stella, F., Aprahamian, I., Ferreira, L. K., Forlenza, O. V., & Busatto, G. F. (2013). White matter abnormalities associated with Alzheimer's disease and mild cognitive impairment: A critical review of MRI studies. Expert Review of Neurotherapeutics, 13, 483–493.10.1586/ern.13.45CrossRefGoogle ScholarPubMed
Radloff, L. S. (1977). The CES-D scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385–401.CrossRefGoogle Scholar
Reitan, R. (1958). Validity of TMT as an indication of organic brain damage. Perceptual and Motor Skills, 8, 271–276.CrossRefGoogle Scholar
Ritchie, K., Artero, S., Beluche, I., Ancelin, M.-L., Mann, A., Dupuy, A.-M., … Boulenger, J.-P. (2004). Prevalence of DSM-IV psychiatric disorder in the French elderly population. The British Journal of Psychiatry: The Journal of Mental Science, 184, 147–152.10.1192/bjp.184.2.147CrossRefGoogle ScholarPubMed
Roberts, B. W., Kuncel, N. R., Shiner, R., Caspi, A., & Goldberg, L. R. (2007). The power of personality: The comparative validity of personality traits, socioeconomic status, and cognitive ability for predicting important life outcomes. Perspectives on Psychological Science: A Journal of the Association for Psychological Science, 2, 313–345.10.1111/j.1745-6916.2007.00047.xCrossRefGoogle ScholarPubMed
Roberts, B. W., Wood, D., & Caspi, A. (2008). The development of personality traits in adulthood. In John, O. P., Robins, R. W. & Pervin, L. A. (eds), Handbook of personality: Theory and research (pp. 375–398). New York, NY: Guilford Press.Google Scholar
Román, G. C., Tatemichi, T. K., Erkinjuntti, T., Cummings, J. L., Masdeu, J. C., Garcia, J. H., … Hofman, A. (1993). Vascular dementia: Diagnostic criteria for research studies. Report of the NINDS-AIREN international workshop. Neurology, 43, 250–260.10.1212/WNL.43.2.250CrossRefGoogle ScholarPubMed
Rorden, C., & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12, 191–200.CrossRefGoogle ScholarPubMed
Sachdev, P. S., Zhuang, L., Braidy, N., & Wen, W. (2013). Is Alzheimer's a disease of the white matter? Current Opinion in Psychiatry, 26, 244–251.CrossRefGoogle ScholarPubMed
Scarmeas, N., & Stern, Y. (2003). Cognitive reserve and lifestyle. Journal of Clinical and Experimental Neuropsychology, 25, 625–633.CrossRefGoogle ScholarPubMed
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. The Journal of Clinical Psychiatry, 59(Suppl. 20), 22–33; quiz 34–57.Google ScholarPubMed
Stephan, Y., Boiché, J., Canada, B., & Terracciano, A. (2014). Association of personality with physical, social, and mental activities across the lifespan: Findings from US and French samples. British Journal of Psychology (London, England: 1953), 105, 564–580.CrossRefGoogle ScholarPubMed
Stern, Y. (2012). Cognitive reserve in ageing and Alzheimer's disease. The Lancet. Neurology, 11, 1006–1012.CrossRefGoogle ScholarPubMed
Sutin, A. R., Stephan, Y., & Terracciano, A. (2018). Psychological distress, self-beliefs, and risk of cognitive impairment and dementia. Journal of Alzheimer's Disease: JAD, 65, 1041–1050.CrossRefGoogle ScholarPubMed
Tautvydaitė, D., Kukreja, D., Antonietti, J.-P., Henry, H., von Gunten, A., & Popp, J. (2017). Interaction between personality traits and cerebrospinal fluid biomarkers of Alzheimer's disease pathology modulates cognitive performance. Alzheimer's Research & Therapy, 9, 6.CrossRefGoogle ScholarPubMed
Teipel, S. J., Meindl, T., Wagner, M., Stieltjes, B., Reuter, S., Hauenstein, K.-H., … Hampel, H. (2010). Longitudinal changes in fiber tract integrity in healthy aging and mild cognitive impairment: A DTI follow-up study. Journal of Alzheimer's Disease: JAD, 22, 507–522.CrossRefGoogle ScholarPubMed
Terracciano, A., Sutin, A. R., An, Y., O'Brien, R. J., Ferrucci, L., Zonderman, A. B., & Resnick, S. M. (2014). Personality and risk of Alzheimer's disease: New data and meta-analysis. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 10, 179–186.CrossRefGoogle ScholarPubMed
Tindle, H. A., Chang, Y.-F., Kuller, L. H., Manson, J. E., Robinson, J. G., Rosal, M. C., … Matthews, K. A. (2009). Optimism, cynical hostility, and incident coronary heart disease and mortality in the Women's Health Initiative. Circulation, 120, 656–662.10.1161/CIRCULATIONAHA.108.827642CrossRefGoogle ScholarPubMed
Vemuri, P., Whitwell, J. L., Kantarci, K., Josephs, K. A., Parisi, J. E., Shiung, M. S., … Jack, C. R. (2008). Antemortem MRI based STructural Abnormality iNDex (STAND)-scores correlate with postmortem Braak neurofibrillary tangle stage. NeuroImage, 42, 559–567.CrossRefGoogle ScholarPubMed
Vos, S. J. B., van Boxtel, M. P. J., Schiepers, O. J. G., Deckers, K., de Vugt, M., Carrière, I., … Köhler, S. (2017). Modifiable risk factors for prevention of dementia in midlife, late life and the oldest-old: Validation of the LIBRA index. Journal of Alzheimer's Disease: JAD, 58, 537–547.10.3233/JAD-161208CrossRefGoogle ScholarPubMed
Wang, X.-D., Ren, M., Zhu, M.-W., Gao, W.-P., Zhang, J., Shen, H., … Gao, K. (2015). Corpus callosum atrophy associated with the degree of cognitive decline in patients with Alzheimer's dementia or mild cognitive impairment: A meta-analysis of the region of interest structural imaging studies. Journal of Psychiatric Research, 63, 10–19.CrossRefGoogle ScholarPubMed
Watkins, E. R., Mullan, E., Wingrove, J., Rimes, K., Steiner, H., Bathurst, N., … Scott, J. (2011). Rumination-focused cognitive-behavioural therapy for residual depression: Phase II randomised controlled trial. The British Journal of Psychiatry: The Journal of Mental Science, 199, 317–322.10.1192/bjp.bp.110.090282CrossRefGoogle ScholarPubMed
Weston, S. J., Edmonds, G. W., & Hill, P. L. (2020). Personality traits predict dietary habits in middle-to-older adults. Psychology, Health & Medicine, 25, 379–387.CrossRefGoogle ScholarPubMed
Xu, J., & Potenza, M. N. (2012). White matter integrity and five-factor personality measures in healthy adults. NeuroImage, 59, 800–807.CrossRefGoogle ScholarPubMed
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