A mechanistic look at the effects of adversity early in life on cardiovascular disease risk during adulthood

Acta Physiologica

Volumn 210, Issue 2, 2014, Pages 277-287

  Loria, A S ^a   Ho, D H ^a   Pollock, J S ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Adverse childhood experience; Cardiovascular risk; Early life stress; Maternal separation

Indexed keywords

ADULTHOOD; BEHAVIORAL STRESS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CHILDHOOD; EARLY LIFE STRESS; HUMAN; LIFE EXPECTANCY; MATERNAL DEPRIVATION; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; VASCULAR DISEASE; ANIMAL; COMPLICATION; MENTAL STRESS; PSYCHOLOGY; RISK FACTOR;

ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; MATERNAL DEPRIVATION; RISK FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84892384496     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12189     Document Type: Review

References (118)

1. Alastalo, H., Raikkonen, K., Pesonen, A.K., Osmond, C., Barker, D.J., Kajantie, E., Heinonen, K., Forsen, T.J. & Eriksson, J.G. 2009. Cardiovascular health of Finnish war evacuees 60 years later. Ann Med 41, 66-72.
2. Alastalo, H., Raikkonen, K., Pesonen, A.K., Osmond, C., Barker, D.J., Heinonen, K., Kajantie, E. & Eriksson, J.G. 2012. Cardiovascular morbidity and mortality in Finnish men and women separated temporarily from their parents in childhood-a life course study. Psychosom Med 74, 583-587.
3. Alastalo, H., Raikkonen, K., Pesonen, A.K., Osmond, C., Barker, D.J., Heinonen, K., Kajantie, E. & Eriksson, J.G. 2013. Early life stress and blood pressure levels in late adulthood. J Hum Hypertens 27, 90-94.
4. Alciati, A., Gesuele, F., Casazza, G. & Foschi, D. 2011. The relationship between childhood parental loss and metabolic syndrome in obese subjects. Stress Health 29, 5-13.
5. Anda, R.F., Dong, M., Brown, D.W., Felitti, V.J., Giles, W.H., Perry, G.S., Valerie, E.J. & Dube, S.R. 2009. The relationship of adverse childhood experiences to a history of premature death of family members. BMC Public Health 9, 106.
6. Banerjee, S.B., Arterbery, A.S., Fergus, D.J. & Adkins-Regan, E. 2012. Deprivation of maternal care has long-lasting consequences for the hypothalamic-pituitary-adrenal axis of zebra finches. Proc Biol Sci 279, 759-766.
7. Barker, D.J., Eriksson, J.G., Forsen, T. & Osmond, C. 2002. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31, 1235-1239.
8. Bernardi, J.R., Ferreira, C.F., Senter, G., Krolow, R., de Aguiar, B.W., Portella, A.K., Kauer-Sant'anna, M., Kapczinski, F., Dalmaz, C., Goldani, M.Z. & Silveira, P.P. 2013. Early life stress interacts with the diet deficiency of omega-3 fatty acids during the life course increasing the metabolic vulnerability in adult rats. PLoS One 8, e62031.
9. Bernstein, I.S. & Dobrofsky, M. 1981. Compensatory social responses of older pigtailed monkeys to maternal separation. Dev Psychobiol 14, 163-168.
10. Beutel, M.E., Wiltink, J., Kirschner, Y., Sinning, C., Espinola-Klein, C., Wild, P.S., Munzel, T., Blettner, M., Zwiener, I., Lackner, K. & Michal, M. 2013. History of depression but not current depression is associated with signs of atherosclerosis: data from the Gutenberg Health Study. Psychol Med 1-7 [Epub ahead of print].
11. Bogdarina, I., Haase, A., Langley-Evans, S. & Clark, A.J. 2010. Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS One 5, e9237.
12. Caldji, C., Diorio, J. & Meaney, M.J. 2000. Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48, 1164-1174.
13. Cameron, N.M., Shahrokh, D., Del Corpo, A., Dhir, S.K., Szyf, M., Champagne, F.A. & Meaney, M.J. 2008. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 20, 795-801.
14. Cano, P., Jimenez, V., Alvarez, M.P., Alvarino, M., Cardinali, D.P. & Esquifino, A.I. 2005a. Effect of litter separation on 24-hour rhythmicity of plasma prolactin, follicle-stimulating hormone and luteinizing hormone levels in lactating rabbit does. J Circadian Rhythms 3, 9.
15. Cano, P., Jimenez-Ortega, V., Alvarez, M.P., Alvarino, M., Cardinali, D.P. & Esquifino, A.I. 2005b. Effect of rabbit doe-litter separation on 24-hour changes of luteinizing hormone, follicle stimulating hormone and prolactin release in female and male suckling pups. Reprod Biol Endocrinol 3, 50.
16. Carlyle, B.C., Duque, A., Kitchen, R.R., Bordner, K.A., Coman, D., Doolittle, E., Papademetris, X., Hyder, F., Taylor, J.R. & Simen, A.A. 2013. Maternal separation with early weaning: a rodent model providing novel insights into neglect associated developmental deficits. Dev Psychopathol 24, 1401-1416.
17. Champagne, F. & Meaney, M.J. 2001. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133, 287-302.
18. Champagne, F.A., Chretien, P., Stevenson, C.W., Zhang, T.Y., Gratton, A. & Meaney, M.J. 2004. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci 24, 4113-4123.
19. Chen, E., Miller, G.E., Kobor, M.S. & Cole, S.W. 2011. Maternal warmth buffers the effects of low early-life socioeconomic status on pro-inflammatory signaling in adulthood. Mol Psychiatry 16, 729-737.
20. Chida, Y. & Steptoe, A. 2009. The association of anger and hostility with future coronary heart disease: a meta-analytic review of prospective evidence. J Am Coll Cardiol 53, 936-946.
21. Danese, A., Pariante, C.M., Caspi, A., Taylor, A. & Poulton, R. 2007. Childhood maltreatment predicts adult inflammation in a life-course study. Proc Natl Acad Sci USA 104, 1319-1324.
22. Desbonnet, L., Garrett, L., Daly, E., McDermott, K.W. & Dinan, T.G. 2008. Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int J Dev Neurosci 26, 259-268.
23. Dong, M., Giles, W.H., Felitti, V.J., Dube, S.R., Williams, J.E., Chapman, D.P. & Anda, R.F. 2004. Insights into causal pathways for ischemic heart disease: adverse childhood experiences study. Circulation 110, 1761-1766.
24. van Eijsden, M., Vrijkotte, T.G., Gemke, R.J. & van der Wal, M.F. 2011. Cohort profile: the Amsterdam Born Children and their Development (ABCD) study. Int J Epidemiol 40, 1176-1186.
25. Enthoven, L., de Kloet, E.R. & Oitzl, M.S. 2008a. Differential development of stress system (re)activity at weaning dependent on time of disruption of maternal care. Brain Res 1217, 62-69.
26. Enthoven, L., Oitzl, M.S., Koning, N., van der Mark, M. & de Kloet, E.R. 2008b. Hypothalamic-pituitary-adrenal axis activity of newborn mice rapidly desensitizes to repeated maternal absence but becomes highly responsive to novelty. Endocrinology 149, 6366-6377.
27. Felitti, V.J. 1993. Childhood sexual abuse, depression, and family dysfunction in adult obese patients: a case control study. South Med J 86, 732-736.
28. Felitti, V.J., Anda, R.F., Nordenberg, D., Williamson, D.F., Spitz, A.M., Edwards, V., Koss, M.P. & Marks, J.S. 1998. Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am J Prev Med 14, 245-258.
29. Feng, X., Wang, L., Yang, S., Qin, D., Wang, J., Li, C., Lv, L., Ma, Y. & Hu, X. 2011. Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys. Proc Natl Acad Sci USA 108, 14312-14317.
30. Fish, E.W., Shahrokh, D., Bagot, R., Caldji, C., Bredy, T., Szyf, M. & Meaney, M.J. 2004. Epigenetic programming of stress responses through variations in maternal care. Ann N Y Acad Sci 1036, 167-180.
31. Forsdahl, A. 1978. Living conditions in childhood and subsequent development of risk factors for arteriosclerotic heart disease. J Epidemiol Community Health 32, 34-37.
32. Forsdahl, A. 1979. Are poor living conditions in childhood and adolescence and important risk factor for arteriosclerotic heart disease? Int J Rehabil Res 2, 238-239.
33. Forsdahl, S.H., Singh, K., Solberg, S. & Jacobsen, B.K. 2009. Risk factors for abdominal aortic aneurysms: a 7-year prospective study: the Tromso Study, 1994-2001. Circulation 119, 2202-2208.
34. Genest, S.E., Gulemetova, R., Laforest, S., Drolet, G. & Kinkead, R. 2004. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554, 543-557.
35. George, E.D., Bordner, K.A., Elwafi, H.M. & Simen, A.A. 2010. Maternal separation with early weaning: a novel mouse model of early life neglect. BMC Neurosci 11, 123.
36. Gluckman, P.D. & Hanson, M.A. 2004. Living with the past: evolution, development, and patterns of disease. Science 305, 1733-1736.
37. Hardy, R., Wadsworth, M.E., Langenberg, C. & Kuh, D. 2004. Birthweight, childhood growth, and blood pressure at 43 years in a British birth cohort. Int J Epidemiol 33, 121-129.
38. Heim, C. & Binder, E.B. 2012. Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol 233, 102-111.
39. Hennessy, M.B. 1988. Both prevention of physical contact and removal of distal cues mediate cortisol and vocalization responses of guinea pig pups to maternal separation in a novel environment. Physiol Behav 43, 729-733.
40. Hennessy, M.B. & Sharp, K. 1990. Voluntary and involuntary maternal separation in guinea pig pups with mothers required to forage. Dev Psychobiol 23, 783-796.
41. Hennessy, M.B., Deak, T., Schiml-Webb, P.A., Carlisle, C.W. & O'Brien, E. 2010. Maternal separation produces, and a second separation enhances, core temperature and passive behavioral responses in guinea pig pups. Physiol Behav 100, 305-310.
42. Hennessy, M.B., Tamborski, A., Schiml, P. & Lucot, J. 1989. The influence of maternal separation on plasma concentrations of ACTH, epinephrine, and norepinephrine in guinea pig pups. Physiol Behav 45, 1147-1152.
43. Hennessy, M.B., Schiml-Webb, P.A., Miller, E.E., Maken, D.S., Bullinger, K.L. & Deak, T. 2007. Anti-inflammatory agents attenuate the passive responses of guinea pig pups: evidence for stress-induced sickness behavior during maternal separation. Psychoneuroendocrinology 32, 508-515.
44. Herbert, C., Siegle, J.S., Shadie, A.M., Nikolaysen, S., Garthwaite, L., Hansbro, N.G., Foster, P.S. & Kumar, R.K. 2012. Development of asthmatic inflammation in mice following early-life exposure to ambient environmental particulates and chronic allergen challenge. Dis Model Mech 6, 479-488.
45. Holness, M.J., Langdown, M.L. & Sugden, M.C. 2000. Early-life programming of susceptibility to dysregulation of glucose metabolism and the development of Type 2 diabetes mellitus. Biochem J 349(Pt 3), 657-665.
46. Kanitz, E., Tuchscherer, M., Puppe, B., Tuchscherer, A. & Stabenow, B. 2004. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain Behav Immun 18, 35-45.
47. Kanitz, E., Puppe, B., Tuchscherer, M., Heberer, M., Viergutz, T. & Tuchscherer, A. 2009. A single exposure to social isolation in domestic piglets activates behavioural arousal, neuroendocrine stress hormones, and stress-related gene expression in the brain. Physiol Behav 98, 176-185.
48. Kaufman, D., Banerji, M.A., Shorman, I., Smith, E.L., Coplan, J.D., Rosenblum, L.A. & Kral, J.G. 2007. Early-life stress and the development of obesity and insulin resistance in juvenile bonnet macaques. Diabetes 56, 1382-1386.
49. Kelishadi, R., Mirghaffari, N., Poursafa, P. & Gidding, S.S. 2009. Lifestyle and environmental factors associated with inflammation, oxidative stress and insulin resistance in children. Atherosclerosis 203, 311-319.
50. Kermack, W.O., McKendrick, A.G. & McKinlay, P.L. 1934. Death rates in Great Britain and Sweden. Expression of specific mortality rates as products of two factors and some consequences thereof. J Hyg (Lond) 34, 433-457.
51. Klengel, T., Mehta, D., Anacker, C., Rex-Haffner, M., Pruessner, J.C., Pariante, C.M., Pace, T.W., Mercer, K.B., Mayberg, H.S., Bradley, B., et al. 2013. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 16, 33-41.
52. Kuh, D., Mishra, G.D., Black, S., Lawlor, D.A., Davey Smith, G., Okell, L., Wadsworth, M. & Hardy, R. 2008. Offspring birth weight, gestational age and maternal characteristics in relation to glucose status at age 53 years: evidence from a national birth cohort. Diabet Med 25, 530-535.
53. Labarba, R.C., Hibbs, S.E. & White, J.L. 1973. Maternal separation and emotional reactivity in BALB-c mice. Psychol Rep 32, 107-110.
54. Laudenslager, M.L., Reite, M. & Harbeck, R.J. 1982. Suppressed immune response in infant monkeys associated with maternal separation. Behav Neural Biol 36, 40-48.
55. Lehmann, J., Stohr, T. & Feldon, J. 2000. Long-term effects of prenatal stress experiences and postnatal maternal separation on emotionality and attentional processes. Behav Brain Res 107, 133-144.
56. Levine, S. 2005. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30, 939-946.
57. Lindgarde, F., Furu, M. & Ljung, B.O. 1987. A longitudinal study on the significance of environmental and individual factors associated with the development of essential hypertension. J Epidemiol Community Health 41, 220-226.
58. Lippmann, M., Bress, A., Nemeroff, C.B., Plotsky, P.M. & Monteggia, L.M. 2007. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci 25, 3091-3098.
59. Loria, A.S., D'Angelo, G., Pollock, D.M. & Pollock, J.S. 2010a. Early life stress downregulates endothelin receptor expression and enhances acute stress-mediated blood pressure responses in adult rats. Am J Physiol Regul Integr Comp Physiol 299, R185-R191.
60. Loria, A.S., Pollock, D.M. & Pollock, J.S. 2010b. Early life stress sensitizes rats to angiotensin II-induced hypertension and vascular inflammation in adult life. Hypertension 55, 494-499.
61. Loria, A.S., Kang, K.T., Pollock, D.M. & Pollock, J.S. 2011. Early life stress enhances angiotensin II-mediated vasoconstriction by reduced endothelial nitric oxide buffering capacity. Hypertension 58, 619-626.
62. Loria, A.S., Brands, M.W., Pollock, D.M. & Pollock, J.S. 2013. Early life stress sensitizes the renal and systemic sympathetic system in rats. Am J Physiol Renal Physiol 305, F390-F395.
63. Lyons, D.M., Yang, C., Sawyer-Glover, A.M., Moseley, M.E. & Schatzberg, A.F. 2001. Early life stress and inherited variation in monkey hippocampal volumes. Arch Gen Psychiatry 58, 1145-1151.
64. Lyons, D.M., Parker, K.J. & Schatzberg, A.F. 2010. Animal models of early life stress: implications for understanding resilience. Dev Psychobiol 52, 616-624.
65. Mascitelli, L., Pezzetta, F. & Sullivan, J.L. 2006. Why women live longer than men: sex differences in longevity. Gend Med 3, 341; author reply 342.
66. Mathieu, G., Oualian, C., Denis, I., Lavialle, M., Gisquet-Verrier, P. & Vancassel, S. 2011. Dietary n-3 polyunsaturated fatty acid deprivation together with early maternal separation increases anxiety and vulnerability to stress in adult rats. Prostaglandins Leukot Essent Fatty Acids 85, 129-136.
67. McGowan, P.O., Sasaki, A., D'Alessio, A.C., Dymov, S., Labonte, B., Szyf, M., Turecki, G. & Meaney, M.J. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12, 342-348.
68. McLamb, B.L., Gibson, A.J., Overman, E.L., Stahl, C. & Moeser, A.J. 2013. Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease. PLoS One 8, e59838.
69. McMillen, I.C. & Robinson, J.S. 2005. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571-633.
70. Meagher, M.W., Sieve, A.N., Johnson, R.R., Satterlee, D., Belyavskyi, M., Mi, W., Prentice, T.W., Welsh, T.H. Jr & Welsh, C.J. 2010. Neonatal maternal separation alters immune, endocrine, and behavioral responses to acute Theiler's virus infection in adult mice. Behav Genet 40, 233-249.
71. Meaney, M.J. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24, 1161-1192.
72. Meaney, M.J., Szyf, M. & Seckl, J.R. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 13, 269-277.
73. Mehta, M. & Schmauss, C. 2011. Strain-specific cognitive deficits in adult mice exposed to early life stress. Behav Neurosci 125, 29-36.
74. Miller, G.E., Chen, E., Fok, A.K., Walker, H., Lim, A., Nicholls, E.F., Cole, S. & Kobor, M.S. 2009. Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci USA 106, 14716-14721.
75. Millstein, R.A. & Holmes, A. 2007. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 31, 3-17.
76. Moeser, A.J., Klok, C.V., Ryan, K.A., Wooten, J.G., Little, D., Cook, V.L. & Blikslager, A.T. 2007. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am J Physiol Gastrointest Liver Physiol 292, G173-G181.
77. Murgatroyd, C., Patchev, A.V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., Holsboer, F., Wotjak, C.T., Almeida, O.F. & Spengler, D. 2009. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12, 1559-1566.
78. Navailles, S., Zimnisky, R. & Schmauss, C. 2010. Expression of glucocorticoid receptor and early growth response gene 1 during postnatal development of two inbred strains of mice exposed to early life stress. Dev Neurosci 32, 139-148.
79. Nugent, N.R., Tyrka, A.R., Carpenter, L.L. & Price, L.H. 2011. Gene-environment interactions: early life stress and risk for depressive and anxiety disorders. Psychopharmacology 214, 175-196.
80. Nuyt, A.M. 2008. Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci (Lond) 114, 1-17.
81. Nuyt, A.M. & Alexander, B.T. 2009. Developmental programming and hypertension. Curr Opin Nephrol Hypertens 18, 144-152.
82. O'Mahony, S., Chua, A.S., Quigley, E.M., Clarke, G., Shanahan, F., Keeling, P.W. & Dinan, T.G. 2008. Evidence of an enhanced central 5HT response in irritable bowel syndrome and in the rat maternal separation model. Neurogastroenterol Motil 20, 680-688.
83. O'Mahony, S.M., Marchesi, J.R., Scully, P., Codling, C., Ceolho, A.M., Quigley, E.M., Cryan, J.F. & Dinan, T.G. 2009. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65, 263-267.
84. Own, L.S. & Patel, P.D. 2012. Maternal behavior and offspring resiliency to maternal separation in c57bl/6 mice. Horm Behav 63, 411-417.
85. Pace, T.W., Mletzko, T.C., Alagbe, O., Musselman, D.L., Nemeroff, C.B., Miller, A.H. & Heim, C.M. 2006. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am J Psychiatry 163, 1630-1633.
86. Parker, K.J., Buckmaster, C.L., Justus, K.R., Schatzberg, A.F. & Lyons, D.M. 2005. Mild early life stress enhances prefrontal-dependent response inhibition in monkeys. Biol Psychiatry 57, 848-855.
87. Parker, K.J., Rainwater, K.L., Buckmaster, C.L., Schatzberg, A.F., Lindley, S.E. & Lyons, D.M. 2007. Early life stress and novelty seeking behavior in adolescent monkeys. Psychoneuroendocrinology 32, 785-792.
88. Paternain, L., Martisova, E., Milagro, F.I., Ramirez, M.J., Martinez, J.A. & Campion, J. 2012. Postnatal maternal separation modifies the response to an obesogenic diet in adulthood in rats. Dis Model Mech 5, 691-697.
89. Plotsky, P.M. & Meaney, M.J. 1993. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18, 195-200.
90. Power, C. & Elliott, J. 2006. Cohort profile: 1958 British birth cohort (National Child Development Study). Int J Epidemiol 35, 34-41.
91. Power, C., Barker, D.J. & Blacklock, N.J. 1987. Incidence of renal stones in 18 British towns. A collaborative study. Br J Urol 59, 105-110.
92. Power, C., Stansfeld, S.A., Matthews, S., Manor, O. & Hope, S. 2002. Childhood and adulthood risk factors for socio-economic differentials in psychological distress: evidence from the 1958 British birth cohort. Soc Sci Med 55, 1989-2004.
93. Rahman, I., Humphreys, K., Bennet, A.M., Ingelsson, E., Pedersen, N.L. & Magnusson, P.K. 2013. Clinical depression, antidepressant use and risk of future cardiovascular disease. Eur J Epidemiol 28, 589-595.
94. Rebollar, P.G., Milanes, A., Pereda, N., Millan, P., Cano, P., Esquifino, A.I., Villarroel, M., Silvan, G. & Lorenzo, P.L. 2006. Oestrus synchronisation of rabbit does at early post-partum by doe-litter separation or ECG injection: reproductive parameters and endocrine profiles. Anim Reprod Sci 93, 218-230.
95. Renard, G.M., Rivarola, M.A. & Suarez, M.M. 2007. Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int J Dev Neurosci 25, 373-379.
96. Rilling, J.K., Winslow, J.T., O'Brien, D., Gutman, D.A., Hoffman, J.M. & Kilts, C.D. 2001. Neural correlates of maternal separation in rhesus monkeys. Biol Psychiatry 49, 146-157.
97. Samuelsson, A.M., Matthews, P.A., Argenton, M., Christie, M.R., McConnell, J.M., Jansen, E.H., Piersma, A.H., Ozanne, S.E., Twinn, D.F., Remacle, C., Rowlerson, A., Poston, L. & Taylor, P.D. 2008. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51, 383-392.
98. Sanders, B.J. & Anticevic, A. 2007. Maternal separation enhances neuronal activation and cardiovascular responses to acute stress in borderline hypertensive rats. Behav Brain Res 183, 25-30.
99. Savignac, H.M., Dinan, T.G. & Cryan, J.F. 2011. Resistance to early-life stress in mice: effects of genetic background and stress duration. Front Behav Neurosci 5, 13.
100. Schmidt, M.V., Wang, X.D. & Meijer, O.C. 2011. Early life stress paradigms in rodents: potential animal models of depression? Psychopharmacology 214, 131-140.
101. Schooling, C.M., Jiang, C., Lam, T.H., Zhang, W., Cheng, K.K. & Leung, G.M. 2011. Parental death during childhood and adult cardiovascular risk in a developing country: the Guangzhou Biobank Cohort Study. PLoS One 6, e19675.
102. Shapero, B.G., Black, S.K., Liu, R.T., Klugman, J., Bender, R.E., Abramson, L.Y. & Alloy, L.B. 2013. Stressful life events and depression symptoms: the effect of childhood emotional abuse on stress reactivity. J Clin Psychol doi: 10.1002/jclp.22011.
103. Spencer, K.A., Evans, N.P. & Monaghan, P. 2009. Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 150, 1931-1934.
104. Spencer-Booth, Y. & Hinde, R.A. 1971. The effects of 13 days maternal separation on infant rhesus monkeys compared with those of shorter and repeated separations. Anim Behav 19, 595-605.
105. Spivey, J.M., Padilla, E., Shumake, J.D. & Gonzalez-Lima, F. 2011. Effects of maternal separation, early handling, and gonadal sex on regional metabolic capacity of the preweanling rat brain. Brain Res 1367, 198-206.
106. Suderman, M., McGowan, P.O., Sasaki, A., Huang, T.C., Hallett, M.T., Meaney, M.J., Turecki, G. & Szyf, M. 2012. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc Natl Acad Sci USA 109(Suppl 2), 17266-17272.
107. Szyf, M., Weaver, I.C., Champagne, F.A., Diorio, J. & Meaney, M.J. 2005. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 26, 139-162.
108. Tamborski, A., Lucot, J.B. & Hennessy, M.B. 1990. Central dopamine turnover in guinea pig pups during separation from their mothers in a novel environment. Behav Neurosci 104, 607-611.
109. Taylor, S.E. & Seeman, T.E. 1999. Psychosocial resources and the SES-health relationship. Ann N Y Acad Sci 896, 210-225.
110. Trombini, M., Hulshof, H.J., Graiani, G., Carnevali, L., Meerlo, P., Quaini, F. & Sgoifo, A. 2012. Early maternal separation has mild effects on cardiac autonomic balance and heart structure in adult male rats. Stress 15, 457-470.
111. Tuchscherer, M., Kanitz, E., Puppe, B., Tuchscherer, A. & Stabenow, B. 2004. Effects of postnatal social isolation on hormonal and immune responses of pigs to an acute endotoxin challenge. Physiol Behav 82, 503-511.
112. Tuchscherer, M., Kanitz, E., Puppe, B. & Tuchscherer, A. 2006. Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets. Horm Behav 50, 753-761.
113. Tucker, D.C. & Johnson, A.K. 1984. Influence of neonatal handling on blood pressure, locomotor activity, and preweanling heart rate in spontaneously hypertensive and Wistar Kyoto rats. Dev Psychobiol 17, 587-600.
114. Uchida, S., Hara, K., Kobayashi, A., Funato, H., Hobara, T., Otsuki, K., Yamagata, H., McEwen, B.S. & Watanabe, Y. 2010. Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci 30, 15007-15018.
115. Vig, R., Gordon, J.R., Thebaud, B., Befus, A.D. & Vliagoftis, H. 2010. The effect of early-life stress on airway inflammation in adult mice. NeuroImmunoModulation 17, 229-239.
116. Wadsworth, M.E., Cripps, H.A., Midwinter, R.E. & Colley, J.R. 1985. Blood pressure in a national birth cohort at the age of 36 related to social and familial factors, smoking, and body mass. Br Med J (Clin Res Ed) 291, 1534-1538.
117. Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M. & Meaney, M.J. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7, 847-854.
118. Yoo, S.B., Ryu, V., Park, E.Y., Kim, B.T., Kang, D.W., Lee, J.H. & Jahng, J.W. 2011. The arcuate NPY, POMC, and CART expressions responding to food deprivation are exaggerated in young female rats that experienced neonatal maternal separation. Neuropeptides 45, 343-349.