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Extremely low birth weight influences the relationship between stress and telomere length in adulthood

Published online by Cambridge University Press:  29 May 2020

Calan D. Savoy*
Affiliation:
Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ONL8S 4L8, Canada
Louis A. Schmidt
Affiliation:
Department of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, ONL8S 4L8, Canada
Patrick O. McGowan
Affiliation:
Department of Biological Sciences, University of Toronto Scarborough, Toronto, ONM1C 1A4, Canada
Saroj Saigal
Affiliation:
Department of Pediatrics, McMaster University, Hamilton, ONL8S 4L8, Canada
Ryan J. Van Lieshout
Affiliation:
Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, ONL8S 4L8, Canada
*
Address for correspondence: Calan D. Savoy, Department of Psychiatry and Behavioural Neurosciences, McMaster University, St. Joseph’s Healthcare Hamilton, West 5th Campus, 100 West 5th Street, Hamilton, ONL8N 3K7, Canada. Email: savoycd@mcmaster.ca

Abstract

This study examined the link between two biological markers of stress vulnerability at 22–26 years of age and telomere length at 30–35 among extremely low birth weight (ELBW; <1000 g) survivors and normal birth weight (NBW; >2500 g) control participants. Sixteen ELBW and 22 NBW participants provided baseline afternoon salivary cortisol samples and resting frontal electroencephalogram (EEG) alpha asymmetry data at 22–26 years. Buccal cells were assayed for telomere length at 30–35 years. Analyses controlled for sex, postnatal steroid exposure, childhood socioeconomic status, time of cortisol sample collection, and body mass index at 22–26 years. Salivary cortisol and frontal asymmetry at age 22–26 independently predicted telomere length at age 30–35, such that relatively higher cortisol and greater relative right frontal asymmetry at rest predicted telomere shortening among NBW controls, but not among ELBW survivors. However, similar associations were not noted in ELBW survivors, suggesting that ELBW survivors may have different mechanisms of stress coping as a result of their early-life exposures. These findings offer preliminary evidence in support of the role of stress in the genesis of cellular senescence at least among those born at NBW, but that these links may differ in those born preterm.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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References

Factor-Litvak, P, Susser, E. The importance of early life studies of telomere attrition. Paediatr Perinat Epidemiol. 2015; 29, 144145.CrossRefGoogle ScholarPubMed
Samani, NJ, Boultby, R, Butler, R, et al. Telomere shortening in atherosclerosis. Lancet. 2001; 358, 472473.CrossRefGoogle ScholarPubMed
Martínez, P, Blasco, MA. Telomere-driven diseases and telomere-targeting therapies. J Cell Biol. 2017; 216, 875887. doi: 10.1083/jcb.201610111.CrossRefGoogle ScholarPubMed
Epel, ES, Blackburn, EH, Lin, J, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci U S A. 2004; 101, 1731217315.CrossRefGoogle ScholarPubMed
Woody, A, Hamilton, K, Livitz, IE, et al. Buccal telomere length and its associations with cortisol, heart rate variability, and blood pressure responses to an acute social evaluative stressor. Stress. 2017; 20, 249257.CrossRefGoogle Scholar
Ockenfels, MC, Porter, L, Smyth, J, et al. Effect of chronic stress associated with unemployment on salivary cortisol: overall cortisol levels, diurnal rhythm, and acute stress reactivity. Psychosom Med. 1995; 57, 460467.CrossRefGoogle ScholarPubMed
Gunnar, MR, Talge, NM, Herrera, A. Stressor paradigms in developmental studies: what does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology. 2009; 34, 953967.CrossRefGoogle Scholar
Khoury, JE, Gonzalez, A, Levitan, RD, et al. Summary cortisol reactivity indicators: Interrelations and meaning. Neurobiol Stress. 2015; 2, 3443.CrossRefGoogle ScholarPubMed
Burke, HM, Davis, MC, Otte, C, et al. Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology. 2005; 30, 846856.CrossRefGoogle ScholarPubMed
Coan, JA, Allen, JJ. Frontal EEG asymmetry as a moderator and mediator of emotion. Biol Psychol. 2004; 67, 750.CrossRefGoogle ScholarPubMed
Reznik, SJ, Allen, JJB. Frontal asymmetry as a mediator and moderator of emotion: an updated review. Psychophysiology. 2018; 55, e12965.CrossRefGoogle Scholar
Jesulola, E, Sharpley, CF, Bitsika, V, et al. Frontal alpha asymmetry as a pathway to behavioural withdrawal in depression: research findings and issues. Behav Brain Res. 2015; 292, 5667.CrossRefGoogle ScholarPubMed
Price, LH, Kao, HT, Burgers, DE, et al. Telomeres and early-life stress: an overview. Biological Psychiatry. 2013; 73, 1523.CrossRefGoogle ScholarPubMed
Drury, SS, Theall, K, Gleason, MM, et al. Telomere length and early severe social deprivation: linking early adversity and cellular aging. Mol Psychiatry. 2012; 17, 719727.CrossRefGoogle ScholarPubMed
Entringer, S, Epel, ES, Kumsta, R, et al. Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc Natl Acad Sci U S A. 2011; 108, E513E518.CrossRefGoogle ScholarPubMed
Vasu, V, Turner, KJ, George, S, et al. Preterm infants have significantly longer telomeres than their term born counterparts. PLoS One. 2017; 12, e0180082.CrossRefGoogle ScholarPubMed
Provenzi, L, Giorda, R, Fumagalli, M, et al. Pain exposure associates with telomere length erosion in very preterm infants. Psychoneuroendocrinology. 2018; 89, 113119.CrossRefGoogle ScholarPubMed
Provenzi, L, Scotto di Minico, G, Giorda, R, et al. Telomere length in preterm infants: a promising biomarker of early adversity and care in the Neonatal Intensive Care Unit? Front Endocrinol; 8. Epub ahead of print 31 October 2017. doi: 10.3389/fendo.2017.00295.Google Scholar
Mathewson, KJ, Pyhälä, R, Hovi, P, et al. Cardiovascular responses to psychosocial stress reflect motivation state in adults born at extremely low birth weight. Glob Pediatr Heal. 2015; 2, 19.Google Scholar
Waxman, J, Van Lieshout, RJ, Schmidt, LA. Early adversity and mental health: linking extremely low birth weight, emotion regulation, and internalizing disorders. Curr Pediatr Rev. 2014; 10, 208215.Google ScholarPubMed
Kajantie, E, Phillips, DIW, Andersson, S, et al. Size at birth, gestational age and cortisol secretion in adult life: foetal programming of both hyper- and hypocortisolism? Clin Endocrinol. 2002; 57, 635641.CrossRefGoogle ScholarPubMed
Irving, RJ, Belton, NR, Elton, RA, et al. Adult cardiovascular risk factors in premature babies. Lancet. 2000; 355, 21352136.CrossRefGoogle ScholarPubMed
Van Lieshout, RJ, Boyle, MH, Saigal, S, et al. Mental health of extremely low birth weight survivors in their 30s. Pediatrics; 135. Epub ahead of print 2015. doi: 10.1542/peds.2014-3143.Google Scholar
Goffinet, F. Primary predictors of preterm labour. BJOG. 2005; 112, 3847.CrossRefGoogle ScholarPubMed
Mooney-Leber, SM, Brummelte, S. Neonatal pain and reduced maternal care: early-life stressors interacting to impact brain and behavioral development. Neuroscience. 2017; 342, 2136.CrossRefGoogle ScholarPubMed
Harris, A, Seckl, J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011; 59, 279289.CrossRefGoogle ScholarPubMed
Murgatroyd, C, Spengler, D. Epigenetic programming of the HPA axis: early life decides. Stress. 2011; 14, 581589.CrossRefGoogle ScholarPubMed
Entringer, S, Kumsta, R, Hellhammer, DH, et al. Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm Behav. 2009; 55, 292298.CrossRefGoogle ScholarPubMed
Van Lieshout, RJ, Boyle, MH, Favotto, L, et al. Impact of extremely low-birth-weight status on risk and resilience for depression and anxiety in adulthood. J Child Psychol Psychiatry Allied Discip. 2018; 59, 596603.CrossRefGoogle ScholarPubMed
Mathewson, KJ, Van Lieshout, RJ, Saigal, S, et al. Reduced respiratory sinus arrhythmia in adults born at extremely low birth weight: evidence of premature parasympathetic decline? Int J Psychophysiol. 2014; 93, 198203.CrossRefGoogle ScholarPubMed
Schmidt, LA, Miskovic, V, Boyle, M, et al. Frontal electroencephalogram asymmetry, salivary cortisol, and internalizing behavior problems in young adults who were born at extremely low birth weight. Child Dev. 2010; 81, 183199.CrossRefGoogle ScholarPubMed
Schmidt, LA, Miskovic, V, Boyle, MH, et al. Shyness and timidity in young adults who were born at extremely low birth weight. Pediatrics. 2008; 122, 181187.CrossRefGoogle ScholarPubMed
Somsen, RJM, Van’t Klooster, BJ, Van Der Molen, MW, et al. Growth spurts in brain maturation during middle childhood as indexed by EEG power spectra. Biol Psychol. 1997; 44, 187209.CrossRefGoogle ScholarPubMed
Jasper, H. Report of the committee on methods of clinical examination in electroencephalography. Electroencephalogr Clin Neurophysiol. 1958; 10, 370375.Google Scholar
Davidson, RJ. Affective style, psychopathology, and resilience: brain mechanisms and plasticity. Am Psychol. 2000; 55, 11961214.CrossRefGoogle ScholarPubMed
Tomarken, AJ, Davidson, RJ, Wheeler, RE, et al. Psychometric properties of resting anterior EEG asymmetry: temporal stability and internal consistency. Psychophysiology. 1992; 29, 576592.CrossRefGoogle ScholarPubMed
Kroenke, CH, Epel, E, Adler, N, et al. Autonomic and adrenocortical reactivity and buccal cell telomere length in kindergarten children. Psychosom Med. 2011; 73, 533540.CrossRefGoogle ScholarPubMed
Thomas, P, O’ Callaghan, NJ, Fenech, M. Telomere length in white blood cells, buccal cells and brain tissue and its variation with ageing and Alzheimer’s disease. Mech Ageing Dev. 2008; 129, 183190.CrossRefGoogle ScholarPubMed
Gadalla, SM, Cawthon, R, Giri, N, et al. Correlation of telomere length in blood, buccal cells, and fibroblasts from patients with inherited bone marrow failure syndromes. Blood. 2009; 114, 1083. doi: 10.1182/blood.V114.22.1083.1083.CrossRefGoogle Scholar
Gramatges, MM, Bertuch, AA. Measuring relative telomere length: is tissue an issue? Aging. 2010; 2, 756757.CrossRefGoogle ScholarPubMed
O’Callaghan, NJ, Fenech, M. A quantitative PCR method for measuring absolute telomere length. Biol Proced Online. 2011; 13, 3.CrossRefGoogle ScholarPubMed
Daly, JR, Evans, JI. Daily rhythms of steroid and associated pituitary hormones in man and their relationship to sleep. Adv Steroid Biochem Pharmacol. 1974; 4, 61110.CrossRefGoogle ScholarPubMed
Benetos, A, Okuda, K, Lajemi, M, et al. Telomere length as an indicator of biological aging: the gender effect and relation with pulse pressure and pulse wave velocity. Hypertension. 2001; 37, 381385.CrossRefGoogle ScholarPubMed
Incollingo Rodriguez, AC, Epel, ES, White, ML, et al. Hypothalamic-pituitary-adrenal axis dysregulation and cortisol activity in obesity: a systematic review. Psychoneuroendocrinology. 2015; 62, 301318.CrossRefGoogle ScholarPubMed
Crane, JD, Yellin, SA, Ong, FJ, et al. ELBW survivors in early adulthood have higher hepatic, pancreatic and subcutaneous fat. Sci Rep. 2016; 6, 17.CrossRefGoogle ScholarPubMed
Winchester, SB, Sullivan, MC, Roberts, MB, et al. Prematurity, birth weight, and socioeconomic status are linked to atypical diurnal hypothalamic-pituitary-adrenal axis activity in young adults. Res Nurs Health. 2016; 39, 1529.CrossRefGoogle ScholarPubMed
Hollingshead, AB. Two factor index of social position. Unpublished manuscript, Yale Univ.Google Scholar
Zalli, A, Carvalho, LA, Lin, J, et al. Shorter telomeres with high telomerase activity are associated with raised allostatic load and impoverished psychosocial resources. Proc Natl Acad Sci U S A. 2014; 111, 45194524.CrossRefGoogle ScholarPubMed
Nederhof, E, Schmidt, M V. Mismatch or cumulative stress: toward an integrated hypothesis of programming effects. Physiol Behav. 2012; 106, 701706.CrossRefGoogle ScholarPubMed
Santarelli, S, Lesuis, SL, Wang, XD, et al. Evidence supporting the match/mismatch hypothesis of psychiatric disorders. Eur Neuropsychopharmacol. 2014; 24, 907918.CrossRefGoogle ScholarPubMed
Choi, J, Fauce, SR, Effros, RB. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain Behav Immun. 2008; 22, 600605.CrossRefGoogle Scholar
Daskalakis, NP, Kloet, ER De, Yehuda, R, et al. Early life stress effects on glucocorticoid—BDNF interplay in the hippocampus. Front Mol Neurosci. 2015; 8, 113.CrossRefGoogle ScholarPubMed
Finnicum, CT, Dolan, CV, Willemsen, G, et al. Relative telomere repeat mass in buccal and leukocyte-derived DNA. PLoS One. 2017; 12, e0170765.CrossRefGoogle ScholarPubMed