Is there a viability-vulnerability tradeoff? Sex differences in fetal programming

Journal of Psychosomatic Research

Volumn 75, Issue 4, 2013, Pages 327-335

  Sandman, Curt A ^a   Glynn, Laura M ^a,b   Davis, Elysia Poggi ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHAPMAN UNIVERSITY   (United States)

^c UNIVERSITY OF DENVER   (United States)

Author keywords

Child development; Fetal behavior; Fetal programming; HPA axis; Prenatal stress; Sex differences

Indexed keywords

ANXIETY; ARTICLE; EXECUTIVE FUNCTION; FETAL WELL BEING; HUMAN; LONGITUDINAL STUDY; PRENATAL EXPOSURE; PROSPECTIVE STUDY; RISK ASSESSMENT; SEX DIFFERENCE; SEX RATIO;

CHILD DEVELOPMENT; FETAL BEHAVIOR; FETAL PROGRAMMING; HPA AXIS; PRENATAL STRESS; SEX DIFFERENCES;

ADAPTATION, PSYCHOLOGICAL; ANXIETY; BIOLOGICAL MARKERS; BRAIN; CHILD; CHILD DEVELOPMENT; CORTICOTROPIN-RELEASING HORMONE; EXECUTIVE FUNCTION; FEAR; FEMALE; FETAL DEVELOPMENT; FETAL VIABILITY; GESTATIONAL AGE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MILK, HUMAN; ORGAN SIZE; PITUITARY-ADRENAL SYSTEM; PLACENTA; PREDICTIVE VALUE OF TESTS; PREGNANCY; PREGNANT WOMEN; PRENATAL EXPOSURE DELAYED EFFECTS; PROSPECTIVE STUDIES; PSYCHOMOTOR PERFORMANCE; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84885382216     PISSN: 00223999     EISSN: 18791360     Source Type: Journal    
DOI: 10.1016/j.jpsychores.2013.07.009     Document Type: Article

References (56)

1. Smith JM Game theory and the evolution of fighting. On evolution 1972, Edinburgh University Press.
2. Graffelman J, Fugger EF, Keyvanfar K, Schulman JD Human live birth and sperm-sex ratios compared. Hum Reprod 1999, 14:2917-2920.
3. Cooperstock M, Campbell J Excess males in preterm birth: interactions with gestational age, race, and multiple birth. Obstet Gynecol 1996, 88:189-193.
4. Mathews TJ, Hamilton BE Trend analysis of the sex ratio at birth in the United States. Natl Vital Stat Rep 2005, 53:1-17.
5. Wells JC Natural selection and sex differences in morbidity and mortality in early life. J Theor Biol 2000, 202:65-76.
6. Argasinski K The dynamics of sex ratio evolution dynamics of global population parameters. J Theor Biol 2012, 309:134-146.
7. Kanazawa S Beautiful british parents have more daughters. Reprod Sci 2011, 18:353-358.
8. Hunt PA, Hassold TJ Sex matters in meiosis. Science 2002, 296:2181-2183.
9. James WH Hypotheses on the stability and variation of human sex ratios at birth. J Theor Biol 2012, 310:183-186.
10. Fisher RA The genetical theory of natural selection 1930, Clarendon Press, Oxford.
11. Peacock JL, Marston L, Marlow N, Calvert SA, Greenough A Neonatal and infant outcome in boys and girls born very prematurely. Pediatr Res 2012, 71:305-310.
12. Aiken CE, Ozanne SE Sex differences in developmental programming models. Reproduction 2013, 145:R1-R13.
13. Walker MG, Fitzgerald B, Keating S, Ray JG, Windrim R, Kingdom JC Sex-specific basis of severe placental dysfunction leading to extreme preterm delivery. Placenta 2012, 33:568-571.
14. Torday JS, Nielsen HC, Fencl Mde M, Avery ME Sex differences in fetal lung maturation. Am Rev Respir Dis 1981, 123:205-208.
15. Trivers RL, Willard DE Natural selection of parental ability to vary the sex ratio of offspring. Science 1973, 179:90-92.
16. Kanazawa S Violent men have more sons: further evidence for the generalized Trivers-Willard hypothesis (gTWH). J Theor Biol 2006, 239:450-459.
17. Song S Does famine influence sex ratio at birth? Evidence from the 1959-1961 great leap forward famine in China. Proc Biol Sci 2012, 279:2883-2890.
18. Clifton VL Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 2010, 31:S33-S39.
19. Glynn LM, Sandman CA Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Dev Sci 2012, 15:601-610.
20. Herman JP, Cullinan WE Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 1997, 20:78-84.
21. Joels M, Baram TZ The neuro-symphony of stress. Nat Rev Neurosci 2009, 10:459-466.
22. Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Physiol 2006, 572:31-44.
23. Mueller BR, Bale TL Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 2008, 28:9055-9065.
24. Rodrigues SM, LeDoux JE, Sapolsky RM The influence of stress hormones on fear circuitry. Annu Rev Neurosci 2009, 32:289-313.
25. Ellman LM, Dunkel-Schetter C, Hobel CJ, Chicz-DeMet A, Glynn LM, Sandman CA Timing of fetal exposure to stress hormones: effects on newborn physical and neuromuscular maturation. Dev Psychobiol 2008, 50:232-241.
26. Davis EP, Sandman CA The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev 2010, 81:131-148.
27. Bayley N Balyley scales of infant development 1993, The Psychological Corporation. 2nd ed.
28. Sandman CA, Davis EP, Glynn LM Prescient human fetuses thrive. Psychol Sci 2012, 23:93-100.
29. Davis EP, Glynn LM, Dunkel Schetter C, Hobel C, Chicz-Demet A, Sandman CA Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Dev Neurosci 2005, 27:299-305.
30. Davis EP, Sandman CA Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology 2012, 37:1224-1233.
31. Davis EP, Glynn LM, Schetter CD, Hobel C, Chicz-Demet A, Sandman CA Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry 2007, 46:737-746.
32. Gartstein MA, Rothbart MK Studying infant temperament via the revised infant behavior questionnaire. Infant Behav Dev 2003, 26:64-86.
33. Achenbach TM, Rescorla LA Manual for the ASEBA school-age forms and profiles: an integrated system of multi-informant assessment 2001, University of Vermont, Research Center for Children, Youth, & Families, Burlington, VT.
34. Grey KR, Davis EP, Sandman CA, Glynn LM Human milk cortisol is associated with infant temperament. Psychoneuroendocrinology 2012, 38:1178-1185.
35. Sandman CA, Davis EP Neurobehavioral risk is associated with gestational exposure to stress hormones. Expert Rev Endocrinol Metab 2012, 7:445-459.
36. Buss C, Davis EP, Muftuler LT, Head K, Sandman CA High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 2010, 35:141-153.
37. Buss C, Davis EP, Hobel CJ, Sandman CA Maternal pregnancy-specific anxiety is associated with child executive function at 6-9years age. Stress 2011, 14:665-676.
38. Sandman CA, Davis EP, Buss C, Glynn LM Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 2012, 95:8-21.
39. Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci U S A 2012, 109:E1312-E1319.
40. Davis EP, Buss C, Muftuler LT, Head K, Hasso A, Wing DA, et al. Children's brain development benefits from longer gestation. Front Psychol 2011, 2:1.
41. Bourgeois JP Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex. Acta Paediatr Suppl 1997, 422:27-33.
42. Volpe JJ Neurology of the newborn 2008, Elsevier, Philadelphia. 5th ed.
43. DiPietro JA, Costigan KA, Shupe AK, Pressman EK, Johnson TR Fetal neurobehavioral development: associations with socioeconomic class and fetal sex. Dev Psychobiol 1998, 33:79-91.
44. Buss C, Davis EP, Class QA, Gierczak M, Pattillo C, Glynn LM, et al. Maturation of the human fetal startle response: evidence for sex-specific maturation of the human fetus. Early Hum Dev 2009, 85:633-638.
45. Goel N, Bale TL Examining the intersection of sex and stress in modelling neuropsychiatric disorders. J Neuroendocrinol 2009, 21:415-420.
46. Gabory A, Attig L, Junien C Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 2009, 304:8-18.
47. Hintz SR, Kendrick DE, Vohr BR, Kenneth Poole W, Higgins RD For The NICHD Neonatal Research N. Gender differences in neurodevelopmental outcomes among extremely preterm, extremely-low-birth weight infants. Acta Paediatr 2006, 95:1239-1248.
48. Kesler SR, Reiss AL, Vohr B, Watson C, Schneider KC, Katz KH, et al. Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. J Pediatr 2008, 152:20. e1.
49. Buss C, Lord C, Wadiwalla M, Hellhammer DH, Lupien SJ, Meaney MJ, et al. Maternal care modulates the relationship between prenatal risk and hippocampal volume in women but not in men. J Neurosci 2007, 27:2592-2595.
50. Kagan J, Snidman N, Arcus D Childhood derivatives of high and low reactivity in infancy. Child Dev 1998, 69:1483-1493.
51. Pfeifer M, Goldsmith HH, Davidson RJ, Rickman M Continuity and change in inhibited and uninhibited children. Child Dev 2002, 73:1474-1485.
52. Schwartz CE, Snidman N, Kagan J Adolescent social anxiety as an outcome of inhibited temperament in childhood. J Am Acad Child Adolesc Psychiatry 1999, 38:1008-1015.
53. Schwartz CE, Wright CI, Shin LM, Kagan J, Rauch SL Inhibited and uninhibited infants "grown up": adult amygdalar response to novelty. Science 2003, 300:1952-1953.
54. Bruckner TA, Nobles J Intrauterine stress and male cohort quality: the case of September 11, 2001. Soc Sci Med 2013, 76:107-114.
55. Weinstock M Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 2001, 65:427-451.
56. Rice F, Harold GT, Boivin J, van den Bree M, Hay DF, Thapar A The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med 2010, 40:335-345.