Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-16T15:19:42.825Z Has data issue: false hasContentIssue false
  • English
  • Français

Does neuroticism make you old? Prospective associations between neuroticism and leukocyte telomere length

Published online by Cambridge University Press:  09 July 2013

S. L. van Ockenburg ,
P. de Jonge ,
P. van der Harst ,
J. Ormel  and
J. G. M. Rosmalen
S. L. van Ockenburg*
Affiliation:
Interdisciplinary Center for Psychopathology and Emotion Regulation, University of Groningen, University Medical Center Groningen, The Netherlands
P. de Jonge
Affiliation:
Interdisciplinary Center for Psychopathology and Emotion Regulation, University of Groningen, University Medical Center Groningen, The Netherlands
P. van der Harst
Affiliation:
Department of Cardiology, University of Groningen, University Medical Center Groningen, The Netherlands
J. Ormel
Affiliation:
Interdisciplinary Center for Psychopathology and Emotion Regulation, University of Groningen, University Medical Center Groningen, The Netherlands
J. G. M. Rosmalen
Affiliation:
Interdisciplinary Center for Psychopathology and Emotion Regulation, University of Groningen, University Medical Center Groningen, The Netherlands
*
*Address for correspondence: S. L. van Ockenburg, M.D., Interdisciplinary Center for Psychopathology and Emotion Regulation, University of Groningen, University Medical Center Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands. (Email: s.l.van.ockenburg@umcg.nl)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Telomere attrition, causing accelerated aging, might be one of the mechanisms through which neuroticism leads to somatic disease and increased all-cause mortality. In the current study we investigated whether neuroticism is prospectively associated with shorter telomere length (TL), a biological marker of aging.

Method

Participants were 3432 adults (mean age 52.9 years, range 32–79). Data were collected at baseline (T1) and at two follow-up visits after 4 years (T2) and 6 years (T3). Neuroticism was assessed using the 12-item neuroticism scale of the Revised Eysenck Personality Questionnaire (EPQ-R) at T2 and T3. TL was measured by a monochrome multiplex quantitative polymerase chain reaction (PCR) assay at T1, T2 and T3. A linear mixed model was used to assess whether neuroticism could predict TL prospectively after adjusting for age, sex, body mass index (BMI), frequency of sports, smoking status, presence of chronic diseases and level of education.

Results

Neuroticism was a significant negative predictor of TL at follow-up (B = −0.004, p = 0.044) after adjusting for sex, age, baseline TL and various biological and lifestyle factors.

Conclusions

High neuroticism is significantly and prospectively associated with telomere attrition independent of lifestyle and other risk factors.

Keywords

Cellular agingnegative affectivityneuroticismpersonalitystresstelomere length
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 4 , March 2014 , pp. 723 - 729
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aviv, A, Chen, W, Gardner, JP, Kimura, M, Brimacombe, M, Cao, X, Srinivasan, SR, Berenson, GS (2009). Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa Heart Study. American Journal of Epidemiology 169, 323–329.Google Scholar
Blasco, MA (2007). Telomere length, stem cells and aging. Nature Chemical Biology 3, 640–649.Google Scholar
Brydon, L, Lin, J, Butcher, L, Hamer, M, Erusalimsky, JD, Blackburn, EH, Steptoe, A (2011). Hostility and cellular aging in men from the Whitehall II cohort. Biological Psychiatry 71, 767–773.CrossRefGoogle ScholarPubMed
Cawthon, RM (2009). Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Research 37, e21.CrossRefGoogle ScholarPubMed
Cawthon, RM, Smith, KR, O'Brien, E, Sivatchenko, A, Kerber, RA (2003). Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 361, 393–395.CrossRefGoogle ScholarPubMed
Chan, SW, Blackburn, EH (2002). New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21, 553–563.Google Scholar
Chen, W, Kimura, M, Kim, S, Cao, X, Srinivasan, SR, Berenson, GS, Kark, JD, Aviv, A (2011). Longitudinal versus cross-sectional evaluations of leukocyte telomere length dynamics: age-dependent telomere shortening is the rule. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 66, 312–319.Google Scholar
Collado, M, Blasco, MA, Serrano, M (2007). Cellular senescence in cancer and aging. Cell 130, 223–233.Google Scholar
Costa, PT Jr., McCrae, RR (1992 a). Four ways five factors are basic. Personality and Individual Differences 13, 653–665.Google Scholar
Costa, PT, McCrae, RR (1992 b). Revised NEO Personality Inventory (NEO-PI-R) and the Five Factor Inventory (NEO-FFI): Professional Manual. Psychological Assessment Resources, Inc.: Odessa, FL.Google Scholar
Damjanovic, AK, Yang, Y, Glaser, R, Kiecolt-Glaser, JK, Nguyen, H, Laskowski, B, Zou, Y, Beversdorf, DQ, Weng, NP (2007). Accelerated telomere erosion is associated with a declining immune function of caregivers of Alzheimer's disease patients. Journal of Immunology 179, 4249–4254.Google Scholar
Dickerson, SS, Kemeny, ME (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin 130, 355–391.Google Scholar
Drury, SS, Theall, K, Gleason, MM, Smyke, AT, De Vivo, I, Wong, JY, Fox, NA, Zeanah, CH, Nelson, CA (2012). Telomere length and early severe social deprivation: linking early adversity and cellular aging. Molecular Psychiatry 17, 719–727.CrossRefGoogle ScholarPubMed
Du, M, Prescott, J, Kraft, P, Han, J, Giovannucci, E, Hankinson, SE, De Vivo, I (2012). Physical activity, sedentary behavior, and leukocyte telomere length in women. American Journal of Epidemiology 175, 414–422.Google Scholar
Epel, ES, Blackburn, EH, Lin, J, Dhabhar, FS, Adler, NE, Morrow, JD, Cawthon, RM (2004). Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences USA 101, 1173–1182.CrossRefGoogle ScholarPubMed
Flores, I, Cayuela, ML, Blasco, MA (2005). Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309, 1253–1256.CrossRefGoogle ScholarPubMed
Fries, E, Hesse, J, Hellhammer, J, Hellhammer, DH (2005). A new view on hypocortisolism. Psychoneuroendocrinology 30, 1010–1016.Google Scholar
Graham, JW (2009). Missing data analysis: making it work in the real world. Annual Review of Psychology 60, 549–576.Google Scholar
Harley, CB, Futcher, AB, Greider, CW (1990). Telomeres shorten during ageing of human fibroblasts. Nature 345, 458–460.Google Scholar
Honig, LS, Schupf, N, Lee, JH, Tang, MX, Mayeux, R (2006). Shorter telomeres are associated with mortality in those with APOE epsilon4 and dementia. Annals of Neurology 60, 181–187.Google Scholar
Huisman, M (2000). Imputation of missing item responses: some simple techniques. Quality and Quantity 34, 331–351.Google Scholar
Kananen, L, Surakka, I, Pirkola, S, Suvisaari, J, Lonnqvist, J, Peltonen, L, Ripatti, S, Hovatta, I (2010). Childhood adversities are associated with shorter telomere length at adult age both in individuals with an anxiety disorder and controls. PloS One 5, e10826.Google Scholar
Kenward, MG, Molenberghs, G (1998). Likelihood based frequentist inference when data are missing at random. Statistical Science 13, 236–247.Google Scholar
Kline, P (2000). A Psychometrics Primer. Free Association Books: London.Google Scholar
Lahey, BB (2009). Public health significance of neuroticism. American Psychologist 64, 241–256.CrossRefGoogle ScholarPubMed
Madsen, KS, Jernigan, TL, Iversen, P, Frokjaer, VG, Mortensen, EL, Knudsen, GM, Baare, WF (2012). Cortisol awakening response and negative emotionality linked to asymmetry in major limbic fibre bundle architecture. Psychiatry Research 201, 63–72.Google Scholar
Mangold, D, Mintz, J, Javors, M, Marino, E (2012). Neuroticism, acculturation and the cortisol awakening response in Mexican American adults. Hormones and Behavior 61, 23–30.CrossRefGoogle ScholarPubMed
McIntosh, LJ, Hong, KE, Sapolsky, RM (1998). Glucocorticoids may alter antioxidant enzyme capacity in the brain: baseline studies. Brain Research 791, 209–214.Google Scholar
McIntosh, LJ, Sapolsky, RM (1996). Glucocorticoids may enhance oxygen radical-mediated neurotoxicity. Neurotoxicology 17, 873–882.Google Scholar
Mroczek, DK, Spiro, A, Turiano, N (2009). Do health behaviors explain the effect of neuroticism on mortality? Longitudinal findings from the VA Normative Aging Study. Journal of Research in Personality 43, 653–659.Google Scholar
Nater, UM, Hoppmann, C, Klumb, PL (2010). Neuroticism and conscientiousness are associated with cortisol diurnal profiles in adults – role of positive and negative affect. Psychoneuroendocrinology 35, 1573–1577.CrossRefGoogle ScholarPubMed
Nordfjall, K, Svenson, U, Norrback, KF, Adolfsson, R, Lenner, P, Roos, G (2009). The individual blood cell telomere attrition rate is telomere length dependent. PLoS Genetics 5, e1000375.CrossRefGoogle ScholarPubMed
O'Donovan, A, Lin, J, Dhabhar, FS, Wolkowitz, O, Tillie, JM, Blackburn, E, Epel, E (2009). Pessimism correlates with leukocyte telomere shortness and elevated interleukin-6 in post-menopausal women. Brain, Behavior, and Immunity 23, 446–449.Google Scholar
Ormel, J, Rosmalen, J, Farmer, A (2004). Neuroticism: a non-informative marker of vulnerability to psychopathology. Social Psychiatry and Psychiatric Epidemiology 39, 906–912.Google Scholar
Pineles, SL, Rasmusson, AM, Yehuda, R, Lasko, NB, Macklin, ML, Pitman, RK, Orr, SP (2012). Predicting emotional responses to potentially traumatic events from pre-exposure waking cortisol levels: a longitudinal study of police and firefighters. Anxiety, Stress, and Coping 26, 241–253.CrossRefGoogle Scholar
Pinheiro, J, Bates, D, DebRoy, S, Sarkar, D, and the R Development Core Team (2012). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–105.Google Scholar
Pinto-Sietsma, SJ, Janssen, WM, Hillege, HL, Navis, G, de Zeeuw, D, de Jong, PE (2000). Urinary albumin excretion is associated with renal functional abnormalities in a nondiabetic population. Journal of the American Society of Nephrology 11, 1882–1888.CrossRefGoogle Scholar
Poulton, RG, Andrews, G (1992). Personality as a cause of adverse life events. Acta Psychiatrica Scandinavica 85, 35–38.Google Scholar
R Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (http://www.R-project.org/).Google Scholar
Riese, H, Rijsdijk, FV, Rosmalen, JG, Snieder, H, Ormel, J (2009). Neuroticism and morning cortisol secretion: both heritable, but no shared genetic influences. Journal of Personality 77, 1561–1575.Google Scholar
Rudolph, KL, Millard, M, Bosenberg, MW, Depinho, RA (2001). Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nature Genetics 28, 155–159.CrossRefGoogle ScholarPubMed
Sanderman, R, Eysenck, SBG, Arrindell, WA (1991). Cross-cultural comparisons of personality – the Netherlands and England. Psychological Reports 69, 1091–1096.Google Scholar
Shalev, I, Moffitt, TE, Sugden, K, Williams, B, Houts, RM, Danese, A, Mill, J, Arseneault, L, Caspi, A (2012). Exposure to violence during childhood is associated with telomere erosion from 5 to 10 years of age: a longitudinal study. Molecular Psychiatry 18, 576–581.Google Scholar
Shipley, BA, Weiss, A, Der, G, Taylor, MD, Deary, IJ (2007). Neuroticism, extraversion, and mortality in the UK Health and Lifestyle Survey: a 21-year prospective cohort study. Psychosomatic Medicine 69, 923–931.Google Scholar
Steptoe, A, Hamer, M, Butcher, L, Lin, J, Brydon, L, Kivimaki, M, Marmot, M, Blackburn, E, Erusalimsky, JD (2011). Educational attainment but not measures of current socioeconomic circumstances are associated with leukocyte telomere length in healthy older men and women. Brain, Behavior, and Immunity 25, 1292–1298.CrossRefGoogle Scholar
Svenson, U, Nordfjall, K, Baird, D, Roger, L, Osterman, P, Hellenius, ML, Roos, G (2011). Blood cell telomere length is a dynamic feature. PloS One 6, e21485.Google Scholar
Tabak, BA, McCullough, ME (2011). Perceived transgressor agreeableness decreases cortisol response and increases forgiveness following recent interpersonal transgressions. Biological Psychology 87, 386–392.Google Scholar
Tyrka, AR, Price, LH, Kao, HT, Porton, B, Marsella, SA, Carpenter, LL (2010). Childhood maltreatment and telomere shortening: preliminary support for an effect of early stress on cellular aging. Biological Psychiatry 67, 531–534.CrossRefGoogle ScholarPubMed
Valdes, AM, Andrew, T, Gardner, JP, Kimura, M, Oelsner, E, Cherkas, LF, Aviv, A, Spector, TD (2005). Obesity, cigarette smoking, and telomere length in women. Lancet 366, 662–664.Google Scholar
van Santen, A, Vreeburg, SA, Van der Does, AJ, Spinhoven, P, Zitman, FG, Penninx, BW (2011). Psychological traits and the cortisol awakening response: results from the Netherlands Study of Depression and Anxiety. Psychoneuroendocrinology 36, 240–248.Google Scholar
Wikgren, M, Maripuu, M, Karlsson, T, Nordfjall, K, Bergdahl, J, Hultdin, J, Del-Favero, J, Roos, G, Nilsson, LG, Adolfsson, R, Norrback, KF (2012). Short telomeres in depression and the general population are associated with a hypocortisolemic state. Biological Psychiatry 71, 294–300.Google Scholar
Willeit, P, Willeit, J, Mayr, A, Weger, S, Oberhollenzer, F, Brandstatter, A, Kronenberg, F, Kiechl, S (2010). Telomere length and risk of incident cancer and cancer mortality. Journal of the American Medical Association 304, 69–75.Google Scholar