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Sex-specific impact of maternal–fetal risk factors on depression and cardiovascular risk 40 years later

Published online by Cambridge University Press:  04 November 2011

J. M. Goldstein ,
S. Cherkerzian ,
S. L. Buka ,
G. Fitzmaurice ,
M. Hornig ,
M. Gillman ,
S. O'Toole  and
R. P. Sloan
J. M. Goldstein*
Affiliation:
Connors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, Boston, MA, USA Departments of Psychiatry and Medicine, Harvard Medical School, Boston, MA, USA Division of Psychiatric Neuroscience, Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA
S. Cherkerzian
Affiliation:
Connors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, Boston, MA, USA Departments of Psychiatry and Medicine, Harvard Medical School, Boston, MA, USA
S. L. Buka
Affiliation:
Department of Epidemiology, Brown University, Providence, RI, USA
G. Fitzmaurice
Affiliation:
Department of Psychiatry, Harvard Medical School at McLean Hospital, Belmont, MA, USA
M. Hornig
Affiliation:
Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, NY, USA
M. Gillman
Affiliation:
Department of Population Health, Harvard Medical School, Harvard Pilgrim Community Health
S. O'Toole
Affiliation:
Connors Center for Women's Health and Gender Biology, Brigham and Women's Hospital, Boston, MA, USA
R. P. Sloan
Affiliation:
Department of Psychiatry, Columbia University Medical Center, New York State Psychiatric Institute, New York, NY, USA
*
*Address for correspondence: Dr J. M. Goldstein, Division of Women's Health, Brigham and Women's Hospital, One Brigham Circle, 3rd Floor, 1620 Tremont St., Boston, MA 02120, USA. (Email [email protected])
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Abstract

Major depressive disorder (MDD) and cardiovascular disease (CVD) represent leading causes of morbidity and mortality worldwide. We tested the hypothesis that growth restriction and preeclampsia (referred to as fetal risk) are significant predictors of these conditions, with women at higher risk in adulthood. Adult offspring exposed to fetal risk factors and their discordant siblings were from two prenatal cohorts, whose mothers were followed through pregnancy and whom we recruited as adults 40 years later (n = 538; 250 males and 288 females). Subjects were psychiatrically diagnosed and underwent a stress challenge during which parasympathetic regulation was assessed by electrocardiogram, operationalized as high-frequency R-R interval variability (HF-RRV). Linear mixed models and generalized estimating equations were used to examine the relationship of fetal risk on HF-RRV, MDD and comorbidity of low HF-RRV (lowest 25th percentile) and MDD, including interactions with sex and socioeconomic status (SES). Fetal risk was significantly associated with low HF-RRV response (F = 3.64, P = 0.05), particularly among low SES (interaction: F = 4.31, P < 0.04). When stratified by MDD, the fetal risk impact was three times greater among MDD compared with non-MDD subjects (effect size: 0.21 v. 0.06). Females had a significantly higher risk for the comorbidity of MDD and low HF-RRV than males (relative risk (RR) = 1.36, 95% CI: 1.07–1.73), an association only seen among those exposed to fetal risk (RR = 1.38, 95% CI: 1.04–1.83). Findings suggest that these are shared fetal antecedents to the comorbidity of MDD and CVD risk 40 years later, an association stronger in females than in males.

Keywords

autonomic nervous systemcardiovascular diseasedepressionfetal programmingfetal risksex differences
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Special Issue 6: The Early Determinants of Adult Health Study , December 2011 , pp. 353 - 364
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

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References

1. Ustun, TB, Ayuso-Mateos, JL, Chatterji, S, Mathers, C, Murray, CJ. Global burden of depressive disorders in the year 2000. Br J Psychiatry. 2004; 184, 386–392.CrossRefGoogle ScholarPubMed
2. World Health Organization. The Global Burden of Disease: 2004 Update, 2008. World Health Organization: Geneva.Google Scholar
3. Lett, HS, Blumenthal, JA, Babyak, MA, et al. Depression as a risk factor for coronary artery disease: evidence, mechanisms, and treatment. Psychosom Med. 2004; 66, 305–315.Google ScholarPubMed
4. Penninx, BW, Beekman, AT, Honig, A, et al. Depression and cardiac mortality: results from a community-based longitudinal study. Arch Gen Psychiatry. 2001; 58, 221–227.CrossRefGoogle ScholarPubMed
5. Ferketich, A, Schwartzbaum, J, Frid, D, Moeschberger, M. Depression as an antecedent to heart disease among women and men in the NHANES I study. Arch Intern Med. 2000; 160, 1261–1268.CrossRefGoogle ScholarPubMed
6. Mallik, S, Spertus, JA, Reid, KJ, et al. Depressive symptoms after acute myocardial infarction: evidence for highest rates in younger women. Arch Intern Med. 2006; 166, 876–883.CrossRefGoogle ScholarPubMed
7. Vaccarino, V, Johnson, BD, Sheps, DS, et al. Depression, inflammation, and incident cardiovascular disease in women with suspected coronary ischemia: the National Heart, Lung, and Blood Institute-sponsored WISE study. J Am Coll Cardiol. 2007; 50, 2044–2050.CrossRefGoogle ScholarPubMed
8. Welberg, LA, Seckl, JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol. 2001; 13, 113–128.CrossRefGoogle ScholarPubMed
9. Phillips, DI, Jones, A. Fetal programming of autonomic and HPA function: do people who were small babies have enhanced stress responses? J Physiol. 2006; 572(Pt 1), 45–50.CrossRefGoogle ScholarPubMed
10. Mesulam, MM. Patterns in behavioral neuroanatomy: association areas, the limbic system, and hemispheric specialization. In Principles of Behavioral Neurology (ed. Mesulam MM), 1985; pp. 1–58. F.A. Davis Company: Philadelphia, PA.Google Scholar
11. Goncharuk, VD, Van Heerikhuize, J, Swaab, DF, Buijs, RM. Paraventricular nucleus of the human hypothalamus in primary hypertension: activation of corticotropin-releasing hormone neurons. J Comp Neurol. 2002; 443, 321–331.CrossRefGoogle ScholarPubMed
12. DiGiulio, D, Gervasi, M, Romero, R, et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinatal Med. 2010; 38, 495–502.CrossRefGoogle ScholarPubMed
13. Szarka, A, Rigo, J Jr, Lazar, L, Beko, G, Molvarec, A. Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol. 2010; 11, 59–67.CrossRefGoogle ScholarPubMed
14. Neta, GI, von Ehrenstein, OS, Goldman, LR, et al. Umbilical cord serum cytokine levels and risk of small-for-gestational-age and preterm birth. Am J Epidemiol. 2010; 171, 859–867.CrossRefGoogle ScholarPubMed
15. Tuovinen, S, Raikkonen, K, Kajantie, E, et al. Depressive symptoms in adulthood and intrauterine exposure to pre-eclampsia: the Helsinki Birth Cohort Study. BJOG. 2010; 117, 1236–1242.CrossRefGoogle ScholarPubMed
16. Van Lieshout, RJ, Boylan, K. Increased depressive symptoms in female but not male adolescents born at low birth weight in the offspring of a national cohort. Can J Psychiatry. 2010; 55, 422–430.CrossRefGoogle Scholar
17. Quinkler, M, Stewart, PM. Hypertension and Cortisol–Cortisone Shuttle. J Clin Endocrinol Metab. 2003; 88, 2384–2392.CrossRefGoogle ScholarPubMed
18. Barker, DJ. The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004; 93, 26–33.CrossRefGoogle ScholarPubMed
19. Barker, DJ. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171–174.CrossRefGoogle ScholarPubMed
20. Kessler, RC. Epidemiology of women and depression. J Affect Disord. 2003; 74, 5–13.CrossRefGoogle ScholarPubMed
21. Lloyd-Jones, D, Adams, RJ, Brown, TM, et al. Executive summary: heart disease and stroke statistics–2010 update: a report from the American Heart Association. Circulation. 2010; 121, 948–954.Google ScholarPubMed
22. Naqvi, TZ, Naqvi, SS, Merz, CN. Gender differences in the link between depression and cardiovascular disease. Psychosom Med. 2005; 67(Suppl 1), S15–S18.CrossRefGoogle ScholarPubMed
23. Moller-Leimkuhler, AM. Gender differences in cardiovascular disease and comorbid depression. Dialogues Clin Neurosci. 2007; 9, 71–83.CrossRefGoogle ScholarPubMed
24. Golston, K, Bailllie, AJ. Depression and coronary heart disease: a review of the epidemiological evidence, explanatory mechanisms and management approaches. Clin Psychol Rev. 2008; 28, 288–306.CrossRefGoogle Scholar
25. Van der Kooy, K, van Hout, H, Marwijk, H, et al. Depression and the risk for cardiovascular diseases: systematic review and meta analysis. Int J Geriatr Psychiatry. 2007; 22, 613–626.CrossRefGoogle ScholarPubMed
26. Gil, K, Radziłłowicz, P, Zdrojewski, T, et al. Relationship between the prevalence of depressive symptoms and metabolic syndrome. Results of the SOPKARD Project. Kardiol Pol. 2006; 64, 464–469.Google ScholarPubMed
27. Meyer, CM, Armenian, HK, Eaton, WW, Ford, DE. Incident hypertension associated with depression in the Baltimore Epidemiologic Catchment area follow-up study. J Affect Disord. 2004; 83, 127–133.CrossRefGoogle ScholarPubMed
28. Shin, JY, Suls, J, Martin, R. Are cholesterol and depression inversely related? A meta-analysis of the association between two cardiac risk factors. Ann Behav Med. 2008; 36, 33–43.CrossRefGoogle ScholarPubMed
29. Rozanski, A, Blumenthal, JA, Kaplan, J. Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation. 1999; 99, 2192–2217.CrossRefGoogle ScholarPubMed
30. Ozanne, S, Fernandez-Twinn, D, Hales, C. Fetal growth and adult diseases. Semin Perinatol. 2004; 28, 81–87.CrossRefGoogle ScholarPubMed
31. Gale, C, Martyn, C. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 28–33.CrossRefGoogle Scholar
32. Preti, A, Cardascia, L, Zen, T, et al. Obstetric complications in patients with depression – a population-based case–control study. J Affect Disord. 2000; 61, 101–106.CrossRefGoogle ScholarPubMed
33. Kinney, DK, Yurgelun-Todd, DA, Tohen, M, Tramer, S. Pre- and perinatal complications and risk for bipolar disorder: a retrospective study. J Affect Disord. 1998; 50, 117–124.CrossRefGoogle ScholarPubMed
34. Jacobsen, B, Eklund, G, Hamberger, L, et al. Perinatal origin of adult self-destructive behavior. Acta Psychiatr Scand. 1987; 76, 364–371.CrossRefGoogle Scholar
35. Sacker, A, Done, DJ, Crow, TJ, Golding, J. Antecedents of schizophrenia and affective illness obstetric complications. Br J Psychiatry. 1995; 166, 734–741.CrossRefGoogle ScholarPubMed
36. Räikkönen, K, Pesonen, AK, Heinonen, K, et al. Depression in young adults with very low birth weight: the Helsinki study of very low-birth-weight adults. Arch Gen Psychiatry. 2008; 65, 290–296.CrossRefGoogle ScholarPubMed
37. van Os, J, Jones, P, Lewis, G, Wadsworth, M, Murray, R. Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry. 1997; 54, 625–631.CrossRefGoogle Scholar
38. Machon, RA, Mednick, SA, Huttunen, MO. Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch Gen Psychiatry. 1997; 54, 322–328.CrossRefGoogle Scholar
39. Watson, JB, Mednick, SA, Huttunen, M, Wang, X. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol. 1999; 11, 457–466.CrossRefGoogle ScholarPubMed
40. Brown, AS, Susser, ES, Lin, SP, Neugebauer, R, Gorman, JM. Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch Hunger Winter of 1944–45. Br J Psychiatry. 1995; 166, 601–606.CrossRefGoogle Scholar
41. Brown, AS, van Os, J, Driessens, C, Hoek, HW, Susser, ES. Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry. 2000; 157, 190–195.CrossRefGoogle ScholarPubMed
42. Phillips, D. Fetal programming of the neuroendocrine response to stress: links between low birth weight and the metabolic syndrome. Endocr Res. 2004; 30, 819–826.CrossRefGoogle ScholarPubMed
43. Daly, B, Scragg, R, Schaaf, D, Metcalf, P. Low birth weight and cardiovascular risk factors in Auckland adolescents: a retrospective cohort study. NZ Med J. 2005; 118, 24–34.Google ScholarPubMed
44. Labayen, I, Ortega, F, Sjöström, M, Ruiz, J. Early life origins of low-grade inflammation and atherosclerosis risk in children and adolescents. J Pediatr. 2009; 155, 673–677.CrossRefGoogle ScholarPubMed
45. Leeson, C, Kattenhorn, M, Morley, R, Lucas, A, Deanfield, J. Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation. 2001; 103, 1264–1268.CrossRefGoogle ScholarPubMed
46. Eriksson, M, Wallander, M, Krakau, I, Wedel, H, Svärdsudd, K. Birth weight and cardiovascular risk factors in a cohort followed until 80 years of age: the study of men born in 1913. J Intern Med. 2004; 255, 236–246.CrossRefGoogle Scholar
47. Rajaleid, K, Janszky, I, Hallqvist, J. Small birth size, adult overweight, and risk of acute myocardial infraction. Epidemiology. 2011; 22, 138–147.CrossRefGoogle ScholarPubMed
48. Kajantie, E, Feldt, K, Räikkönen, K, et al. Body size at birth predicts hypothalamic–pituitary–adrenal axis response to psychosocial stress at age 60 to 70 years. J Clin Endocrinol Metab. 2007; 92, 4094–4100.CrossRefGoogle ScholarPubMed
49. Whitsel, EA, Raghunathan, T, Pearce, RM, et al. RR interval variation, the QT interval index and risk of primary cardiac arrest among patients without clinically recognized heart disease. Eur Heart J. 2001; 22, 165–173.CrossRefGoogle Scholar
50. Thayer, JF, Lane, RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychiatry. 2007; 74, 224–242.CrossRefGoogle ScholarPubMed
51. Dekker, JM, Crow, RS, Folsom, AR, et al. Low heart rate variability in a 2-minute rhythm strip predicts risk of coronary heart disease and mortality from several causes: the ARIC Study. Atherosclerosis Risk in Communities. Circulation. 2000; 102, 1239–1244.CrossRefGoogle Scholar
52. Liao, D, Sloan, RP, Cascio, WE, et al. Multiple metabolic syndrome is associated with lower heart rate variability. The Atherosclerosis Risk in Communities Study. Diabetes Care. 1998; 21, 2116–2122.CrossRefGoogle ScholarPubMed
53. Tracey, KJ. The inflammatory reflex. Nature. 2002; 420, 853–859.CrossRefGoogle ScholarPubMed
54. Mendonca, G, Heffernan, K, Rossow, L, et al. Sex differences in linear and nonlinear heart rate variability during early recovery from supramaximal exercise. Appl Physiol Nutr Metab. 2010; 35, 439–446.CrossRefGoogle ScholarPubMed
55. Chen, HC, Yang, CC, Kuo, TB, Su, TP, Chou, P. Gender differences in the relationship between depression and cardiac autonomic function among community elderly. Int J Geriatr Psychiatry. 2010; 25, 314–322.CrossRefGoogle ScholarPubMed
56. Susser, E, Buka, S, Schaefer, CA, et al. The Early Determinants of Adult Health Study. J Dev Orig Health Dis. 2011 (in press).CrossRefGoogle ScholarPubMed
57. Oken, E, Kleinman, KP, Rich-Edwards, J, Gillman, MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr. 2003; 3, 6.CrossRefGoogle ScholarPubMed
58. National High B lood Pressure Edu cation Program Working Group on High Blood Pressure in Pregnancy. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol. 2000; 183, S1–S22.CrossRefGoogle Scholar
59. First, MB, Spitzer, RL, Gibbon, M, Williams, JBW. Structured Clinical interview for DSM-IV Axis I Disorders – Patient Edition (SCID -I/P, vers. 2.0), 1996. American Psychiatric Press: Washington, DC.Google Scholar
60. Ruan, WJ, Goldstein, RB, Chou, SP, et al. The alcohol use disorder and associated disabilities interview schedule-IV (AUDADIS-IV): reliability of new psychiatric diagnostic modules and risk factors in a general population sample. Drug Alcohol Depend. 2008; 92, 27–36.CrossRefGoogle Scholar
61. Berntson, GG, Quigley, KS, Lang, JF, Boysen, ST. An approach to artifact identification: application to heart period data. Psychophysiology. 1990; 27, 586–598.CrossRefGoogle ScholarPubMed
62. deBoer, RW, Karemaker, JM, Strackee, J. Comparing spectra of a series of point events, particularly for heart rate variability spectra. IEEE Trans Biomed Eng. 1984; 4, 384–387.CrossRefGoogle Scholar
63. Harris, FJ. On the use of windows for harmonic analysis with the discrete Fourier transform. Proc IEEE. 1978; 66, 51–83.CrossRefGoogle Scholar
64. Myrianthopoulos, NC, French, KS. An application of the U. S. bureau of the census socioeconomic index to a large diversified patient population. Soc Sci Med. 1968; 2, 283–299.CrossRefGoogle Scholar
65. Gilman, SE, Kawachi, I, Fitzmaurice, GM, Buka, SL. Socioeconomic status in childhood and the lifetime risk of major depression. Int J Epidemiol. 2002; 31, 359–367.CrossRefGoogle ScholarPubMed
66. Rose, G, Marmot, M. Social class and coronary heart disease. Br Heart J. 1981; 45, 13–19.CrossRefGoogle ScholarPubMed
67. Salomaa, V, Miettinen, H, Niemelä, M, et al. Relation of socioeconomic position to the case fatality, prognosis and treatment of myocardial infarction events; the FINMONICA MI Register Study. J Epidemiol Community Health. 2001; 55, 475–482.CrossRefGoogle Scholar
68. Littell, RC, Milliken, GA, Stroup, WW, Wolfinger, RD. SAS System for Mixed Models, 1996. SAS Institute: Cary, NC.Google Scholar
69. Clark, AM, DesMeules, M, Luo, W, Duncan, AS, Wielgosz, A. Socioeconomic status and cardiovascular disease: risks and implications for care. Nat Rev Cardiol. 2009; 6, 712–722.CrossRefGoogle ScholarPubMed
70. Lloyd-Jones, D, Adams, R, Carnethon, M, et al. Heart disease and stroke statistics–2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2009; 119, e21–e181.Google ScholarPubMed
71. Jones, A, Beda, A, Ward, AM, et al. Size at birth and autonomic function during psychological stress. Hypertension. 2007; 49, 548–555.CrossRefGoogle ScholarPubMed
72. Jones, A, Beda, A, Osmond, C, et al. Sex-specific programming of cardiovascular physiology in children. Eur Heart J. 2008; 29, 2164–2170.CrossRefGoogle ScholarPubMed
73. Schlotz, W, Jones, A, Phillips, NM, Godfrey, KM, Phillips, DI. Size at birth and motor activity during stress in children aged 7 to 9 years. Pediatrics. 2007; 120, e1237–e1244.CrossRefGoogle ScholarPubMed
74. Lee, JH, Holsen, LM, Spaeth, SB, et al. Hypoactivation of the stress response circuitry in depression associated with loss of parasympathetic control of the heart: a combined analysis of fMRI and heart rate variability (manuscript resubmitted).Google Scholar
75. Vasiliadis, HM, Gilman, SE, Buka, SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008; 117, 306–312.CrossRefGoogle ScholarPubMed
76. Masuzaki, H, Yamamoto, H, Kenyon, CJ, et al. Transgenic amplification of glucocorticoid action in adipose tissue causes high blood pressure in mice. J Clin Invest. 2003; 112, 83–90.CrossRefGoogle ScholarPubMed
77. Seckl, JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001; 185, 61–71.CrossRefGoogle ScholarPubMed
78. Bispham, J, Gopalakrishnan, GS, Dandrea, J, et al. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology. 2003; 144, 3575–3585.CrossRefGoogle ScholarPubMed
79. Schwartz, J, Thornburg, KL. The influence of various physiological challenges on permanent changes to the cardiovascular system. Arch Physiol Biochem. 2003; 111, 3–7.CrossRefGoogle ScholarPubMed
80. Kind, KL, Clifton, PM, Grant, PA, et al. Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am J Physiol Regul Integr Comp Physiol. 2003; 284, R140–R152.CrossRefGoogle ScholarPubMed
81. Haussmann, MF, Carroll, JA, Weesner, GD, et al. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic–pituitary–adrenal (HPA) axis. J Anim Sci. 2000; 78, 2399–2411.CrossRefGoogle ScholarPubMed
82. Broberg, CS, Giraud, GD, Schultz, JM, et al. Fetal anemia leads to augmented contractile response to hypoxic stress in adulthood. Am J Physiol Regul Integr Comp Physiol. 2003; 285, R649–R655.CrossRefGoogle ScholarPubMed
83. Simmons, RA, Templeton, LJ, Gertz, SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes. 2001; 50, 2279–2286.CrossRefGoogle Scholar
84. Breier, BH, Vickers, MH, Ikenasio, BA, Chan, KY, Wong, WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001; 185, 73–79.CrossRefGoogle ScholarPubMed
85. Ozanne, SE, Hales, CN. Lifespan: catch-up growth and obesity in male mice. Nature. 2004; 427, 411–412.CrossRefGoogle ScholarPubMed
86. DiPietro, JA, Bornstein, M, Hahn, C, Costigan, K, Achy-Brou, A. Fetal heart rate and variability: stability and prediction to developmental outcomes in early childhood. Child Dev. 2007; 78, 1788–1798.CrossRefGoogle ScholarPubMed
87. Grimm, B, Kaehler, C, Schleussner, E, et al. Influence of intrauterine growth restriction on cardiac time intervals evaluated by fetal magnetocardiography. Early Hum Dev. 2003; 74, 1–11.CrossRefGoogle ScholarPubMed
88. Dipietro, JA, Irizarry, RA, Hawkins, M, Costigan, KA, Pressman, EK. Cross-correlation of fetal cardiac and somatic activity as an indicator of antenatal neural development. Am J Obstet Gynecol. 2001; 185, 1421–1426.CrossRefGoogle ScholarPubMed
89. Prechtl, HF. Continuity and change in early neural development. In Continuity of Neural Functions from Prenatal to Postnatal Life (ed. Prechtl HF), 1984; pp. 1–15. Lippincott: Philadelphia, PA.Google Scholar
90. de Weerth, C, Buitelaar, J. Physiological stress reactivity in human pregnancy–a review. Neurosci Biobehav Rev. 2005; 29, 295–312.CrossRefGoogle ScholarPubMed
91. Spassov, L, Curzi-Dascalova, L, Clairambault, J, et al. Heart rate and heart rate variability during sleep in small-for-gestational age newborns. Pediatr Res. 1994; 35, 500–505.CrossRefGoogle ScholarPubMed
92. Monk, C, Fifer, WP, Myers, MM, et al. Maternal stress responses and anxiety during pregnancy: effects on fetal heart rate. Dev Psychobiol. 2000; 36, 67–77.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
93. Arduini, D, Rizzo, G, Rinaldo, D, et al. Effects of Braxton-Hicks contractions on fetal heart rate variations in normal and growth-retarded fetuses. Gynecol Obstet Invest. 1994; 38, 177–182.CrossRefGoogle ScholarPubMed
94. Lee, JM, Park, KS, Hwang, JH, Park, MI, Yum, MK. Chaotic and periodic heart rate dynamics in uncomplicated intrauterine growth restricted fetuses. Early Hum Dev. 1998; 53, 121–128.CrossRefGoogle ScholarPubMed
95. Lewis, M, Wilson, CD, Ban, P, Baumel, MH. An exploratory study of resting cardiac rate and variability from the last trimester of prenatal life through the first year postpartum life. Child Dev. 1970; 41, 799–811.CrossRefGoogle Scholar
96. Thomas, PW, Haslum, MN, MacGillivray, I, Golding, MJ. Does fetal heart rate predict subsequent heart rate in childhood. Early Hum Dev. 1989; 19, 147–152.CrossRefGoogle ScholarPubMed
97. Meyer, K, Zhang, L. Fetal programming of cardiac function and disease. Reprod Sci. 2007; 14, 209–216.CrossRefGoogle Scholar
98. Zhang, L. Prenatal hypoxia and cardiac programming. J Soc Gynecol Investig. 2005; 12, 2–13.CrossRefGoogle ScholarPubMed
99. Phillips, KA, Vaillant, GE, Schnurr, P. Some physiologic antecedents of adult mental health. Am J Psychiatry. 1987; 144, 1009–1013.Google ScholarPubMed
100. Sherwood, A, Girdler, SS, Bragdon, EE, et al. Ten-year stability of cardiovascular responses to laboratory stressors. Psychophysiology. 1997; 34, 185–191.CrossRefGoogle ScholarPubMed
101. Dierckx, B, Tulen, J, Tharner, A, et al. Low autonomic arousal as vulnerability to externalising behaviour in infants with hostile mothers. Psychiatry Res. 2011; 185, 171–175.CrossRefGoogle ScholarPubMed
102. Kagan, J. Temperament and the reactions to unfamiliarity. Child Dev. 1997; 68, 139–143.CrossRefGoogle ScholarPubMed
103. Calkins, SD. Cardiac vagal tone indices of temperamental reactivity and behavioral regulation in young children. Dev Psychobiol. 1997; 31, 125–135.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
104. Bubier, J, Drabick, D, Breiner, T. Autonomic functioning moderates the relations between contextual factors and externalizing behaviors among inner-city children. J Fam Psychol. 2009; 23, 500–510.CrossRefGoogle ScholarPubMed
105. Burgess, K, Marshall, P, Rubin, K, Fox, N. Infant attachment and temperament as predictors of subsequent externalizing problems and cardiac physiology. J Child Psychol Psyc. 2003; 44, 819–831.CrossRefGoogle ScholarPubMed
106. Raine, A, Venables, PH, Williams, M. High autonomic arousal and electrodermal orienting at age 15 years as protective factors against criminal behavior at age 29 years. Am J Psychiatry. 1995; 152, 1595–1600.Google ScholarPubMed
107. Gillum, RF, Taylor, HL, Anderson, J, Blackburn, H. Longitudinal study (32 years) of exercise tolerance, breathing response, blood pressure, and blood lipids in young men. Arteriosclerosis. 1981; 1, 455–462.CrossRefGoogle ScholarPubMed
108. Kim, JR, Kiefe, CI, Liu, K, et al. Heart rate and subsequent blood pressure in young adults: the CARDIA study. Hypertension. 1999; 33, 640–646.CrossRefGoogle ScholarPubMed
109. Kessler, RC, McGonagle, KA, Swartz, M, Blazer, DG, Nelson, CB. Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence. J Affect Disord. 1993; 29, 85–96.CrossRefGoogle ScholarPubMed
110. Goldstein, JM, Seidman, LJ, O'Brien, LM, et al. Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. Arch Gen Psychiatry. 2002; 59, 154–164.CrossRefGoogle ScholarPubMed
111. Goldstein, JM. Sex, hormones and affective arousal circuitry dysfunction in schizophrenia. Horm Behav. 2006; 50, 612–622.CrossRefGoogle ScholarPubMed
112. Anastario, M, Salafia, CM, Fitzmaurice, G, Goldstein, JM. Impact of fetal versus perinatal hypoxia on sex differences in childhood outcomes: developmental timing matters. Soc Psychiatry Psychiatr Epidemiol. Epub 17 February 2011.Google ScholarPubMed