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

Journal of Developmental Origins of Health and Disease

Volumn 2, Issue 6, 2011, Pages 353-364

  Goldstein, J M ^a,b,c   Cherkerzian, S ^a,b   Buka, S L ^d   Fitzmaurice, G ^b   Hornig, M ^e   Gillman, M ^b   O'Toole, S ^a   Sloan, R P ^f  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BROWN UNIVERSITY   (United States)

^e Department of Medicine   (United States)

^f NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

autonomic nervous system; cardiovascular disease; depression; fetal programming; fetal risk; sex differences

Indexed keywords

EID: 84862800012     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174411000651     Document Type: Article

References (112)

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. (Pubitemid 38624764)
2. World Health Organization. The Global Burden of Disease: 2004 Update, 2008. World Health Organization: Geneva.
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. (Pubitemid 38668397)
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. (Pubitemid 32209674)
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. (Pubitemid 30252771)
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.
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. (Pubitemid 350087570)
8. Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol. 2001; 13, 113-128. (Pubitemid 32058738)
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.
10. MesulamMM. 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.
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. (Pubitemid 34101316)
12. DiGiulio D, Gervasi M, Romero R, et al. Microbial invasion of the amniotic cavity in pregnancies with small-forgestational-age fetuses. J Perinatal Med. 2010; 38, 495-502.
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.
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.
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.
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.
17. Quinkler M, Stewart PM. Hypertension and Cortisol-Cortisone Shuttle. J Clin Endocrinol Metab. 2003; 88, 2384-2392.
18. Barker DJ. The developmental origins of chronic adult disease. Acta Paediatr Suppl. 2004; 93, 26-33. (Pubitemid 39664526)
19. Barker DJ. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171-174.
20. Kessler RC. Epidemiology of women and depression. J Affect Disord. 2003; 74, 5-13. (Pubitemid 36329172)
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.
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. (Pubitemid 40721026)
23. Moller-Leimkuhler AM. Gender differences in cardiovascular disease and comorbid depression. Dialogues Clin Neurosci. 2007; 9, 71-83. (Pubitemid 46607132)
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.
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. (Pubitemid 47180373)
26. Gil K, Radziowicz 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.
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. (Pubitemid 39536186)
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.
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. (Pubitemid 29196806)
30. Ozanne S, Fernandez-Twinn D, Hales C. Fetal growth and adult diseases. Semin Perinatol. 2004; 28, 81-87. (Pubitemid 38298832)
31. Gale C, Martyn C. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 28-33. (Pubitemid 38085211)
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.
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. (Pubitemid 28551781)
34. Jacobsen B, Eklund G, Hamberger L, et al. Perinatal origin of adult self-destructive behavior. Acta Psychiatr Scand. 1987; 76, 364-371. (Pubitemid 18046344)
35. Sacker A, Done DJ, Crow TJ, Golding J. Antecedents of schizophrenia and affective illness obstetric complications. Br J Psychiatry. 1995; 166, 734-741.
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. (Pubitemid 351342445)
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. (Pubitemid 27306572)
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. (Pubitemid 27171917)
39. Watson JB, Mednick SA, Huttunen M, Wang X. Prenatal teratogens and the development of adult mental illness. Dev Psychopathol. 1999; 11, 457-466.
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.
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. (Pubitemid 30080897)
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. (Pubitemid 40070177)
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.
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.
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. (Pubitemid 32221350)
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. (Pubitemid 38241368)
47. Rajaleid K, Janszky I, Hallqvist J. Small birth size, adult overweight, and risk of acute myocardial infraction. Epidemiology. 2011; 22, 138-147.
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. (Pubitemid 350074717)
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. (Pubitemid 32619638)
50. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychiatry. 2007; 74, 224-242. (Pubitemid 46001789)
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.
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. (Pubitemid 28549160)
53. Tracey KJ. The inflammatory reflex. Nature. 2002; 420, 853-859. (Pubitemid 36019638)
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.
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.
56. Susser E, Buka S, Schaefer CA, et al. The EarlyDeterminants of Adult Health Study. J Dev Orig Health Dis. 2011; 2, 311-321.
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.
58. National High Blood Pressure Education 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.
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.
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. (Pubitemid 350218195)
61. Berntson GG, Quigley KS, Lang JF, Boysen ST. An approach to artifact identification: application to heart period data. Psychophysiology. 1990; 27, 586-598.
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.
63. Harris FJ. On the use of windows for harmonic analysis with the discrete Fourier transform. Proc IEEE. 1978; 66, 51-83. (Pubitemid 8338069)
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.
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. (Pubitemid 34537793)
66. Rose G, Marmot M. Social class and coronary heart disease. Br Heart J. 1981; 45, 13-19. (Pubitemid 11168836)
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. (Pubitemid 32591900)
68. Littell RC, Milliken GA, Stroup WW, Wolfinger RD. SAS System for Mixed Models, 1996. SAS Institute: Cary, NC.
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.
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.
71. Jones A, Beda A, Ward AM, et al. Size at birth and autonomic function during psychological stress. Hypertension. 2007; 49, 548-555.
72. Jones A, Beda A, Osmond C, et al. Sex-specific programming of cardiovascular physiology in children. Eur Heart J. 2008; 29, 2164-2170.
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. (Pubitemid 350085520)
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).
75. Vasiliadis HM, Gilman SE, Buka SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008; 117, 306-312. (Pubitemid 351347470)
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. (Pubitemid 38056379)
77. Seckl JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001; 185, 61-71. (Pubitemid 33103954)
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. (Pubitemid 36904437)
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. (Pubitemid 36398895)
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. (Pubitemid 36008665)
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.
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. (Pubitemid 37040573)
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. (Pubitemid 33641912)
84. Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001; 185, 73-79. (Pubitemid 33103955)
85. Ozanne SE, Hales CN. Lifespan: catch-up growth and obesity in male mice. Nature. 2004; 427, 411-412. (Pubitemid 38168484)
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.
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. (Pubitemid 37152485)
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.
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.
90. de Weerth C, Buitelaar J. Physiological stress reactivity in human pregnancy-a review. Neurosci Biobehav Rev. 2005; 29, 295-312. (Pubitemid 40461746)
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. (Pubitemid 24096599)
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. (Pubitemid 30033482)
93. Arduini D, Rizzo G, Rinaldo D, et al. Effects of Braxton-Hicks contractions on fetal heart rate variations in normal and growthretarded fetuses. Gynecol Obstet Invest. 1994; 38, 177-182. (Pubitemid 24297704)
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.
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.
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. (Pubitemid 19137109)
97. Meyer K, Zhang L. Fetal programming of cardiac function and disease. Reprod Sci. 2007; 14, 209-216. (Pubitemid 351168824)
98. Zhang L. Prenatal hypoxia and cardiac programming. J Soc Gynecol Investig. 2005; 12, 2-13. (Pubitemid 40039057)
99. Phillips KA, Vaillant GE, Schnurr P. Some physiologic antecedents of adult mental health. Am J Psychiatry. 1987; 144, 1009-1013. (Pubitemid 17143558)
100. Sherwood A, Girdler SS, Bragdon EE, et al. Ten-year stability of cardiovascular responses to laboratory stressors. Psychophysiology. 1997; 34, 185-191. (Pubitemid 27143352)
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.
102. Kagan J. Temperament and the reactions to unfamiliarity. Child Dev. 1997; 68, 139-143. (Pubitemid 127454373)
103. Calkins SD. Cardiac vagal tone indices of temperamental reactivity and behavioral regulation in young children. Dev Psychobiol. 1997; 31, 125-135. (Pubitemid 127465928)
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.
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. (Pubitemid 37059219)
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.
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. (Pubitemid 12186749)
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. (Pubitemid 29091640)
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. (Pubitemid 23334116)
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. (Pubitemid 34137386)
111. Goldstein JM. Sex, hormones and affective arousal circuitry dysfunction in schizophrenia. Horm Behav. 2006; 50, 612-622. (Pubitemid 44316825)
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.