Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-03T01:18:26.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal separation in childhood and diurnal cortisol patterns in mid-life: findings from the Whitehall II study

Published online by Cambridge University Press:  11 July 2012

M. Kumari ,
J. Head ,
M. Bartley ,
S. Stansfeld  and
M. Kivimaki
M. Kumari*
Affiliation:
Department of Epidemiology and Public Health, University College London, UK
J. Head
Affiliation:
Department of Epidemiology and Public Health, University College London, UK
M. Bartley
Affiliation:
Department of Epidemiology and Public Health, University College London, UK
S. Stansfeld
Affiliation:
Centre for Psychiatry, Barts and the London School of Medicine and Dentistry, London, UK
M. Kivimaki
Affiliation:
Department of Epidemiology and Public Health, University College London, UK
*
*Address for correspondence: Dr M. Kumari, Department of Epidemiology and Public Health, University College London, 1–19 Torrington Place, London WC1E 6BT, UK. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Animal studies suggest that maternal separation is associated with alterations in the hypothalamic–pituitary–adrenal (HPA) axis through effects that occur in a critical period following birth. Evidence for an association of the diurnal cortisol rhythm with maternal separation in humans is equivocal.

Method

We examined whether maternal separation in childhood is associated with diurnal cortisol pattern in 3712 middle-aged men and women. Two aspects of cortisol release were examined: the cortisol awakening response (CAR) and the diurnal slope in cortisol throughout the day.

Results

Maternal separation in childhood was reported by 12% of participants. Those participants who reported maternal separation had a larger CAR and flatter slopes in cortisol levels compared to those who did not report maternal separation [adjusted mean CAR in those reporting no separation versus separation: 7.1, 95% confidence interval (CI) 6.7–7.5 v. 8.4, 95% CI 7.3–9.5, p = 0.02, corresponding to adjusted mean diurnal slope: −0.129 (95% CI −0.130 to −0.128) v. −0.126 (95% CI −0.128 to −0.124), p = 0.01]. In participants who reported maternal separation, the age of separation was not associated with either cortisol measure (p = 0.11). The association between maternal separation and slope in cortisol secretion was largely explained by smoking behaviour and marital status at the time of sample collection whereas that of the CAR was explained by childhood psychosocial, material factors and adult health behaviours.

Conclusions

Our findings suggest that maternal separation in childhood is associated with alterations in the diurnal cortisol pattern in middle age. These associations are predominantly accounted for by adult circumstances and behaviours.

Keywords

Cortisol awakening responsediurnal slope in cortisollifecourse epidemiologymaternal separationsalivary cortisolstress
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 3 , March 2013 , pp. 633 - 643
Copyright
Copyright © Cambridge University Press 2012

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

Adam, EK, Kumari, M (2009). Assessing salivary cortisol in large-scale, epidemiological research. Psychoneuroendocrinology 34, 1423–1436.CrossRefGoogle ScholarPubMed
Agid, O, Shapira, B, Zislin, J, Ritsner, M, Hanin, B, Murad, H, Troudart, T, Bloch, M, Heresco-Levy, U, Lerer, B (1999). Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Molecular Psychiatry 4, 163–172.CrossRefGoogle ScholarPubMed
Badrick, E, Kirschbaum, C, Kumari, M (2007). Smoking status and salivary cortisol secretion. Journal of Clinical Endocrinology and Metabolism 92, 819–824.CrossRefGoogle Scholar
Bifulco, A, Brown, GW, Harris, TO (1994). Childhood Experience of Care and Abuse (CECA): a retrospective interview measure. Journal of Child Psychology and Psychiatry 35, 1419–1435.CrossRefGoogle ScholarPubMed
Bloch, M, Peleg, I, Koren, D, Aner, H, Klein, E (2007). Long-term effects of early parental loss due to divorce on the HPA axis. Hormones and Behavior 51, 516–523.CrossRefGoogle ScholarPubMed
Breier, A, Kelsoe, Jr. JR, Kirwin, PD, Beller, SA, Wolkowitz, OM, Pickar, D (1988). Early parental loss and development of adult psychopathology. Archives of General Psychiatry 45, 987–993.CrossRefGoogle ScholarPubMed
Brim, OG, Baltes, PB, Bumpass, LL, Clearly, PD, Featherman, DL, Hazzard, WR, et al. (1996). National Survey of Midlife Development in the United States (MIDUS), 1995–1996. Boston: Harvard Medical School, Department of Health Care Policy.Google Scholar
Carlson, M, Earls, F (1997). Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Annals of the New York Academy of Sciences 807, 419–428.CrossRefGoogle ScholarPubMed
Chida, Y, Steptoe, A (2009). Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biological Psychology 80, 265–278.CrossRefGoogle ScholarPubMed
Clow, A, Thorn, L, Evans, P, Hucklebridge, F (2004). The awakening cortisol response: methodological issues and significance. Stress 7, 29–37.CrossRefGoogle ScholarPubMed
Dockray, S, Bhattacharyya, MR, Molloy, GJ, Steptoe, A (2008). The cortisol awakening response in relation to objective and subjective measures of waking in the morning. Psychoneuroendocrinology 33, 77–82.CrossRefGoogle ScholarPubMed
Ferrie, JE, Kivimäki, M, Singh-Manoux, A, Shortt, A, Martikainen, P, Head, J, Marmot, M, Gimeno, D, De Vogli, R, Elovainio, M, Shipley, M (2009). Non-response to baseline, non-response to follow-up and mortality in the Whitehall II cohort. International Journal of Epidemiology 38, 831–837.CrossRefGoogle ScholarPubMed
Fisher, PA, Gunnar, MR, Dozier, M, Bruce, J, Pears, KC (2006). Effects of therapeutic interventions for foster children on behavioral problems, caregiver attachment, and stress regulatory neural systems. Annals of the New York Academy of Sciences 1094, 215–225.CrossRefGoogle ScholarPubMed
Flinn, MV, Quinlan, RJ, Decker, SA, Turner, MT, England, BG (1996). Male-female differences in effects of parental absence on glucocorticoid stress response. Human Nature 7, 125–162.CrossRefGoogle ScholarPubMed
Fries, E, Hesse, J, Hellhammer, J, Hellhammer, DH (2005). A new view on hypocortisolism. Psychoneuroendocrinology 30, 1010–1016.CrossRefGoogle ScholarPubMed
Gerritsen, L, Geerlings, MI, Beekman, ATF, Deeg, DJH, Penninx, BW, Comijs, HC (2010). Early and late life events and salivary cortisol in older persons. Psychological Medicine 40, 1569–1578.CrossRefGoogle ScholarPubMed
Gunnar, MR, Morison, SJ, Chisholm, K, Schuder, M (2001). Salivary cortisol levels in children adopted from Romanian orphanages. Developmental Psychopathology 13, 611–628.CrossRefGoogle ScholarPubMed
Hellhammer, J, Fries, E, Schweisthal, OW, Schlotz, W, Stone, AA, Hagemann, D (2007). Several daily measurements are necessary to reliably assess the cortisol rise after awakening: state and trait components. Psychoneuroendocrinology 32, 80–86.CrossRefGoogle ScholarPubMed
Kendler, KS, Neale, MC, Kessler, RC, Heath, AC, Eaves, LJ (1992). Childhood parental loss and adult psychopathology in women. A twin study perspective. Archives of General Psychiatry 49, 109–116.CrossRefGoogle ScholarPubMed
Kessler, RC, McGonagle, KA, Zhao, SY, Nelson, CB, Hughes, M, Eshleman, S, Wittchen, HU, Kendler, KS (1994). Lifetime and 12-month prevalence of DSM-III psychiatric disorders in the United States. Results from the National Co-morbidity Study. Archives of General Psychiatry 51, 8–19.CrossRefGoogle Scholar
Kraft, AJ, Luecken, LJ (2009). Childhood parental divorce and cortisol in young adulthood: evidence for mediation by family income. Psychoneuroendocrinology 34, 1363–1369.CrossRefGoogle ScholarPubMed
Kudielka, BM, Broderick, JE, Kirschbaum, C (2003). Compliance with saliva sampling protocols: electronic monitoring reveals invalid cortisol daytime profiles in noncompliant subjects. Psychosomatic Medicine 65, 313–319.CrossRefGoogle ScholarPubMed
Kumari, M, Badrick, E, Chandola, T, Adam, EK, Stafford, M, Marmot, MG, Kirschbaum, C, Kivimaki, M (2009). Cortisol secretion and fatigue: associations in a community based cohort. Psychoneuroendocrinology 34, 1476–1485.CrossRefGoogle Scholar
Kumari, M, Badrick, E, Chandola, T, Adler, NE, Epel, E, Seeman, T, Kirschbaum, C, Marmot, MG (2010 a). Measures of social position and cortisol secretion in an aging population: findings from the Whitehall II study. Psychosomatic Medicine 72, 27–34.CrossRefGoogle Scholar
Kumari, M, Chandola, T, Brunner, E, Kivimaki, M (2010 b). A nonlinear relationship of generalized and central obesity with diurnal cortisol secretion in the Whitehall II study. Journal of Clinical Endocrinology and Metabolism 95, 4415–4423.CrossRefGoogle ScholarPubMed
Kumari, M, Shipley, M, Stafford, M, Kivimaki, M (2011). Association of diurnal patterns in salivary cortisol with all-cause and cardiovascular mortality: findings from the Whitehall II study. Journal of Clinical Endocrinology and Metabolism 96, 1478–1485.CrossRefGoogle ScholarPubMed
Luecken, L (2000). Parental caring and loss during childhood and adult cortisol responses to stress. Psychology and Health 15, 841–851.CrossRefGoogle Scholar
Luecken, LJ, Appelhans, BM (2006). Early parental loss and salivary cortisol in young adulthood: the moderating role of family environment. Developmental Psychopathology 18, 295–308.CrossRefGoogle ScholarPubMed
Marmot, M, Brunner, E (2005). Cohort profile: the Whitehall II study. International Journal of Epidemiology 34, 251–256.CrossRefGoogle ScholarPubMed
Mathew, SJ, Coplan, JD, Smith, EL, Scharf, BA, Owens, MJ, Nemeroff, CB, Mann, JJ, Gorman, JM, Rosenblum, LA (2002). Cerebrospinal fluid concentrations of biogenic amines and corticotropin-releasing factor in adolescent non-human primates as a function of the timing of adverse early rearing. Stress 5, 185–193.CrossRefGoogle ScholarPubMed
Meinlschmidt, G, Heim, C (2005). Decreased cortisol awakening response after early loss experience. Psychoneuroendocrinology 30, 568–576.CrossRefGoogle ScholarPubMed
Nicolson, NA (2004). Childhood parental loss and cortisol levels in adult men. Psychoneuroendocrinology 29, 1012–1018.CrossRefGoogle ScholarPubMed
Pesonen, AK, Räikkönen, K, Feldt, K, Heinonen, K, Osmond, C, Phillips, DI, Barker, DJ, Eriksson, JG, Kajantie, E (2010). Childhood separation experience predicts HPA axis hormonal responses in late adulthood: a natural experiment of World War II. Psychoneuroendocrinology 35, 758–767.CrossRefGoogle ScholarPubMed
Pfeffer, CR, Altemus, M, Heo, M, Jiang, H (2007). Salivary cortisol and psychopathology in children bereaved by the September 11, 2001 terror attacks. Biological Psychiatry 61, 957–965.CrossRefGoogle ScholarPubMed
Plotsky, PM, Meaney, MJ (1993). Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) messenger RNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research 18, 195–200.CrossRefGoogle ScholarPubMed
Pryce, CR, Ruedi-Bettschen, D, Dettling, AC, Weston, A, Russig, H, Ferger, B, Feldon, J (2005). Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neuroscience Biobehavioral Review 29, 649–674.CrossRefGoogle ScholarPubMed
Radloff, LS (1977). The CES-D scale: a self report depression scale for research in the general population. Applied Psychological Measurement 1, 385–401.CrossRefGoogle Scholar
Rossi, AS, Rossi, PH (1990). Of Human Bonding: Parent–Child Relations across the Life Course. Aldine de Gruyter: New York.Google Scholar
Sanchez, MM, Ladd, CO, Plotsky, PM (2001). Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Developmental Psychopathology 13, 419–449.CrossRefGoogle ScholarPubMed
Sephton, SE, Sapolsky, RM, Kraemer, HC, Speigel, D (2000). Diurnal cortisol rhythm as a predictor of breast cancer survival. Journal of the National Cancer Institute 92, 944–1000.CrossRefGoogle ScholarPubMed
Shaw, BA, Krause, N, Chatters, LM, Connell, CM, Ingersoll-Dayton, B (2004). Emotional support from parents early in life, aging, and health. Psychology and Aging 19, 4–12.CrossRefGoogle ScholarPubMed
Stansfeld, S, Head, J, Bartley, M, Fonagy, P (2008). Social position, early deprivation and the development of attachment. Social Psychiatry and Psychiatric Epidemiology 43, 516–526.CrossRefGoogle ScholarPubMed
Tyrka, AR, Wier, L, Price, LH, Ross, N, Anderson, GM, Wilkinson, CW, Carpenter, LL (2008). Childhood parental loss and adult hypothalamic-pituitary-adrenal function. Biological Psychiatry 63, 1147–1154.CrossRefGoogle ScholarPubMed
van der Hal-Van Raalte, EA, Bakermans-Kranenburg, MJ, van Ijzendoorn, MH (2008). Diurnal cortisol patterns and stress reactivity in child Holocaust survivors reaching old age. Aging and Mental Health 12, 630–638.CrossRefGoogle ScholarPubMed
Wainwright, NWJ, Surtees, P (2002). Childhood adversity, gender and depression over the life-course. Journal of Affective Disorders 72, 33–44.CrossRefGoogle ScholarPubMed
Weller, EB, Weller, RA, Fristad, MA, Bowes, JM (1990). Dexamethasone suppression test and depressive symptoms in bereaved children: a preliminary report. Journal of Neuropsychiatry and Clinical Neuroscience 2, 418–421.Google ScholarPubMed