Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T05:05:05.389Z Has data issue: false hasContentIssue false
  • English
  • Français

Parental responsiveness moderates the association between early-life stress and reduced telomere length

Published online by Cambridge University Press:  26 March 2013

A. Asok ,
K. Bernard ,
T. L. Roth ,
J. B. Rosen  and
M. Dozier
A. Asok*
Affiliation:
University of Delaware
K. Bernard
Affiliation:
University of Delaware
T. L. Roth
Affiliation:
University of Delaware
J. B. Rosen
Affiliation:
University of Delaware
M. Dozier
Affiliation:
University of Delaware
*
Address correspondence and reprint requests to: Arun Asok, University of Delaware, 105 The Green Room 108, Newark, DE 19716; E-mail address: aasok@psych.udel.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

Early-life stress, such as maltreatment, institutionalization, and exposure to violence, is associated with accelerated telomere shortening. Telomere shortening may thus represent a biomarker of early adversity. Previous studies have suggested that responsive parenting may protect children from the negative biological and behavioral consequences of early adversity. This study examined the role of parental responsiveness in buffering children from telomere shortening following experiences of early-life stress. We found that high-risk children had significantly shorter telomeres than low-risk children, controlling for household income, birth weight, gender, and minority status. Further, parental responsiveness moderated the association between risk and telomere length, with more responsive parenting associated with longer telomeres only among high-risk children. These findings suggest that responsive parenting may have protective benefits on telomere shortening for young children exposed to early-life stress. Therefore, this study has important implications for early parenting interventions.

Type
Regular Articles
Information
Development and Psychopathology , Volume 25 , Issue 3 , August 2013 , pp. 577 - 585
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

Afifi, T. O., & Macmillan, H. L. (2011). Resilience following child maltreatment: A review of protective factors. Canadian Journal of Psychiatry, 56, 266–272.Google Scholar
Benetos, A., Okuda, K., Lajemi, M., Kimura, M., Thomas, F., Skurnick, J., et al. (2001). Telomere length as an indicator of biological aging: The gender effect and relation with pulse pressure and pulse wave velocity. Hypertension, 37, 381–385.CrossRefGoogle ScholarPubMed
Bernard, K., Butzin-Dozier, Z., Rittenhouse, J., & Dozier, M. (2010). Cortisol production patterns in young children living with birth parents vs children placed in foster care following involvement of Child Protective Services. Archives of Pediatrics and Adolescent Medicine, 164, 438–443.CrossRefGoogle ScholarPubMed
Bernard, K., & Dozier, M. (2010). Examining infants' cortisol responses to laboratory tasks among children varying in attachment disorganization: Stress reactivity or return to baseline? Developmental Psychology, 46, 1771–1778.CrossRefGoogle ScholarPubMed
Beyne-Rauzy, O., Prade-Houdellier, N., Demur, C., Recher, C., Ayel, J., Laurent, G., et al. (2005). Tumor necrosis factor-alpha inhibits hTERT gene expression in human myeloid normal and leukemic cells. Blood, 106, 3200–3205.CrossRefGoogle ScholarPubMed
Blackburn, E. H. (2001). Switching and signaling at the telomere. Cell, 106, 661–673.Google Scholar
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51, 14–23.Google Scholar
Bruce, J., Kroupina, M., Parker, S., & Gunnar, M. R. (2000). The relationships between cortisol patterns, growth retardation, and developmental delays in postinstitutionalized children. Paper presented at the International Conference on Infant Studies, Brighton, UK.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
Cawthon, R. M. (2002). Telomere measurement by quantitative PCR. Nucleic Acids Research, 30, e47.Google Scholar
Cicchetti, D. (2010). Resilience under conditions of extreme stress: A multilevel perspective. World Psychiatry, 9, 145–154.Google Scholar
Cicchetti, D., Rogosch, F., Toth, S. L., & Sturge-Apple, M. L. (2011). Normalizing the development of cortisol regulation in maltreated infants through preventive interventions. Development and Psychopathology, 23, 789–800.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Toth, S. L. (2005). Child maltreatment. Annual Review of Clinical Psychology, 1, 409–438.CrossRefGoogle ScholarPubMed
Danese, A., Pariante, C. M., Caspi, A., Taylor, A., & Poulton, R. (2007). Childhood maltreatment predicts adult inflammation in a life-course study. Proceedings of the National Academy of Sciences, 104, 1319–1324.Google Scholar
Dozier, M., Manni, M., Gordon, M. K., Peloso, E., Gunnar, M. R., Stovall-McClough, K. C., et al. (2006). Foster children's diurnal production of cortisol: An exploratory study. Child Maltreatment, 11, 189–197.Google Scholar
Drury, S. S., Theall, K., Gleason, M. M., Smyke, A. T., De Vivo, I., Wong, J. Y., et al. (2012). Telomere length and early severe social deprivation: Linking early adversity and cellular aging. Molecular Psychiatry, 17, 719–727.CrossRefGoogle ScholarPubMed
Edwards, V. J., Holden, G. W., Felitti, V. J., & Anda, R. F. (2003). Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: Results from the adverse childhood experiences study. American Journal of Psychiatry, 160, 1453–1460.Google Scholar
Evans, G. W., Kim, P., Ting, A. H., Tesher, H. B., & Shannis, D. (2007). Cumulative risk, maternal responsiveness, and allostatic load among young adolescents. Developmental Psychology, 43, 341–351.Google Scholar
Feldman, R. (2007). Parent–infant synchrony and the construction of shared timing: Physiological precursors, developmental outcomes, and risk conditions. Journal of Child Psychology and Psychiatry, 48, 329–354.CrossRefGoogle ScholarPubMed
Fisher, P. A., Gunnar, M. R., Dozier, M., Bruce, J., & Pears, K. C. (2006). Effects of therapeutic interventions for foster children on behavioral problems, caregiver attachment, and stress regulatory neural systems. Annals of New York Academy of Science, 1094, 215–225.Google Scholar
Fisher, P. A., Stoolmiller, M., Gunnar, M. R., & Burraston, B. O. (2007). Effects of a therapeutic intervention for foster preschoolers on diurnal cortisol activity. Psychoneuroendocrinolgy, 32, 892–905.Google Scholar
Floyd, R. A., Hensley, K., Jaffery, F., Maidt, L., Robinson, K., Pye, Q., et al. (1999). Increased oxidative stress brought on by pro-inflammatory cytokines in neurodegenerative processes and the protective role of nitrone-based free radical traps. Life Sciences, 65, 1893–1899.Google Scholar
Frenck, R. W. Jr., Blackburn, E. H., & Shannon, K. M. (1998). The rate of telomere sequence loss in human leukocytes varies with age. Proceedings of the National Academy of Sciences, 95, 5607–5610.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Cheatham, C. L. (2003). Brain and behavior interface: Stress and the developing brain. Infant Mental Health Journal, 24, 195–211.Google Scholar
Gunnar, M. R., & Donzella, B. (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology, 27, 199–220.Google Scholar
Gunnar, M. R., Fisher, P. A., & the Early Experience, Stress, and Prevention Network. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Developmental Psychopathology, 18, 651–677.CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Quevedo, K. (2007). The neurobiology of stress and development. Annual Review of Psychology, 58, 145–173.Google Scholar
Gunnar, M. R., Talge, N. M., & Herrera, A. (2009). Stressor paradigms in developmental studies: What does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology, 34, 953–967.CrossRefGoogle Scholar
Harley, C. B. (1990). Aging of cultured human skin fibroblasts. Methods for Molecular Biology, 5, 25–32.Google ScholarPubMed
Hayflick, L., & Moorhead, P. S. (1961). The serial cultivation of human diploid cell strains. Experimental Cell Research, 25, 585–621.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008). The link between childhood trauma and depression: Insights from HPA axis studies in humans. Psychoneuroendocrinology, 33, 693–710.Google Scholar
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010). Neurobiological and psychiatric consequences of child abuse and neglect. Developmental Psychobiology, 52, 671–690.Google Scholar
Hertsgaard, L., Gunnar, M., Erickson, M. F., & Nachmias, M. (1995). Adrenocortical responses to the strange situation in infants with disorganized/disoriented attachment relationships. Child Development, 66, 1100–1106.Google Scholar
Hewakapuge, S., van Oorschot, R. A., Lewandowski, P., & Baindur-Hudson, S. (2008). Investigation of telomere lengths measurement by quantitative real-time PCR to predict age. Legal Medicine (Tokyo), 10, 236–242.Google Scholar
Houben, J. M., Moonen, H. J., van Schooten, F. J., & Hageman, G. J. (2008). Telomere length assessment: Biomarker of chronic oxidative stress? Free Radical Biology and Medicine, 44, 235–246.Google Scholar
Juster, R. P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews, 35, 2–16.Google Scholar
Kananen, L., Surakka, I., Pirkola, S., Suvisaari, J., Lonnqvist, J., Peltonen, L., et al. (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.CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, J. K., Gouin, J. P., Weng, N. P., Malarkey, W. B., Beversdorf, D. Q., & Glaser, R. (2011). Childhood adversity heightens the impact of later-life caregiving stress on telomere length and inflammation. Psychosomatic Medicine, 73, 16–22.Google Scholar
Larson, M. C., White, B. P., Cochran, A., Donzella, B., & Gunnar, M. (1998). Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. Developmental Psychobiology, 33, 327–337.Google Scholar
Laucht, M., Esser, G., & Schmidt, M. H. (2001). Differential development of infants at risk for psychopathology: The moderating role of early maternal responsivity. Developmental Medicine and Child Neurology, 43, 292–300.Google Scholar
Masten, A., Best, K., & Garmezy, N. (1990). Resilience and development: Contributions from the study of children who overcome adversity. Development and Psychopathology, 2, 425–444.Google Scholar
McCrory, E., De Brito, S. A., & Viding, E. (2010). Research review: The neurobiology and genetics of maltreatment and adversity. Journal of Child Psychology and Psychiatry, 51, 1079–1095.Google Scholar
McEachern, M. J., Krauskopf, A., & Blackburn, E. H. (2000). Telomeres and their control. Annual Review of Genetics, 34, 331–358.Google Scholar
McEwen, B. S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179.Google Scholar
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108–124.CrossRefGoogle ScholarPubMed
McEwen, B. S. (2008). Understanding the potency of stressful early life experiences on brain and body function. Metabolism, 57(Suppl. 2), S11–S15.CrossRefGoogle ScholarPubMed
Melchior, M., Moffitt, T. E., Milne, B. J., Poulton, R., & Caspi, A. (2007). Why do children from socioeconomically disadvantaged families suffer from poor health when they reach adulthood? A life-course study. American Journal of Epidemiology, 166, 966–974.Google Scholar
Moriceau, S., Roth, T. L., & Sullivan, R. M. (2010). Rodent model of infant attachment learning and stress. Developmental Psychobiology, 52, 651–660.CrossRefGoogle ScholarPubMed
National Institute of Child Health and Human Development Early Child Care Research Network. (1999). Child care and mother–child interaction in the first 3 years of life. Developmental Psychology, 35, 1399–1413.CrossRefGoogle Scholar
National Institute of Child Health and Human Development Early Child Care Research Network. (2003). Early child care and mother–child interaction from 36 months through first grade. Infant Behavior and Development, 26, 345–370.Google Scholar
Neigh, G. N., Gillespie, C. F., & Nemeroff, C. B. (2009). The neurobiological toll of child abuse and neglect. Trauma, Violence, and Abuse, 10, 389–410.Google Scholar
O'Callaghan, N. J., & Fenech, M. (2011). A quantitative PCR method for measuring absolute telomere length. Biological Procedures Online, 13, 3.Google Scholar
O'Donovan, A., Tomiyama, A. J., Lin, J., Puterman, E., Adler, N. E., Kemeny, M., et al. (2012). Stress appraisals and cellular aging: A key role for anticipatory threat in the relationship between psychological stress and telomere length. Brain, Behavior, and Immunity, 26, 573–579.Google Scholar
Petersen, S., Saretzki, G., & von Zglinicki, T. (1998). Preferential accumulation of single-stranded regions in telomeres of human fibroblasts. Experimental Cell Research, 239, 152–160.Google Scholar
Price, L. H., Kao, H. T., Burgers, D. E., Carpenter, L. L., & Tyrka, A. R. (2013). Telomeres and early-life stress: An overview. Biological Psychiatry, 73, 15–23.Google Scholar
Raver, C. C. (1996). Relations between social contingency in mother–child interaction and 2-year-olds' social competence. Developmental Psychology, 32, 850–859.Google Scholar
Rocissano, L., Lynch, V., & Slade, A. (1987). Dyadic synchrony and toddler compliance. Developmental Psychology, 23, 698–704.Google Scholar
Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research, 396, 64–76.CrossRefGoogle ScholarPubMed
Shalev, I. (2012). Early life stress and telomere length: Investigating the connection and possible mechanisms: A critical survey of the evidence base, research methodology and basic biology. Bioessays, 34, 943–952.Google Scholar
Shalev, I., Moffitt, T. E., Sugden, K., Williams, B., Houts, R. M., Danese, A., et al. (2012). Exposure to violence during childhood is associated with telomere erosion from 5 to 10 years of age: A longitudinal study. Molecular Psychiatry. Advance online publication. doi:10.1038/mp.2012.32 mp201232Google ScholarPubMed
Shonkoff, J. P., & Bales, S. N. (2011). Science does not speak for itself: Translating child development research for the public and its policymakers. Child Development, 82, 17–32.Google Scholar
Spangler, G., & Grossmann, K. E. (1993). Biobehavioral organization in securely and insecurely attached infants. Child Development, 64, 1439–1450.Google Scholar
Surtees, P. G., Wainwright, N. W., Pooley, K. A., Luben, R. N., Khaw, K. T., Easton, D. F., et al. (2011). Life stress, emotional health, and mean telomere length in the European Prospective Investigation into Cancer (EPIC)–Norfolk population study. Journals of Gerontology, 66A, 1152–1162.Google Scholar
Tomiyama, A. J., O'Donovan, A., Lin, J., Puterman, E., Lazaro, A., Chan, J., et al. (2012). Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiology & Behavior, 106, 40–45.Google Scholar
Tyrka, A. R., Price, L. H., Kao, H. T., Porton, B., Marsella, S. A., & Carpenter, L. L. (2010). Childhood maltreatment and telomere shortening: Preliminary support for an effect of early stress on cellular aging. Biological Psychiatry, 67, 531–534.Google Scholar
von Zglinicki, T. (2002). Oxidative stress shortens telomeres. Trends in Biochemical Sciences, 27, 339–344.CrossRefGoogle ScholarPubMed
Winberg, J. (2005). Mother and newborn baby: Mutual regulation of physiology and behavior—A selective review. Developmental Psychobiology, 47, 217–229.Google Scholar
You, J. M., Yun, S. J., Nam, K. N., Kang, C., Won, R., & Lee, E. H. (2009). Mechanism of glucocorticoid-induced oxidative stress in rat hippocampal slice cultures. Canadian Journal of Physiology and Pharmacology, 87, 440–447.Google Scholar
Zeichner, S. L., Palumbo, P., Feng, Y., Xiao, X., Gee, D., Sleasman, J., et al. (1999). Rapid telomere shortening in children. Blood, 93, 2824–2830.Google Scholar