Stress and androgen activity during fetal development

Endocrinology (United States)

Volumn 156, Issue 10, 2015, Pages 3435-3441

  Barrett, Emily S ^a   Swan, Shanna H ^b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; BIOLOGICAL MARKER; TESTOSTERONE;

FETUS DEVELOPMENT; HORMONE ACTION; HUMAN; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; ENVIRONMENTAL EXPOSURE; FEMALE; FEMALE GENITAL SYSTEM; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MALE; MALE GENITAL SYSTEM; MENTAL STRESS; METABOLISM; MOTHER; PHYSIOLOGY; PLACENTA;

ANDROGENS; ANIMALS; BIOMARKERS; FEMALE; FETAL DEVELOPMENT; GENITALIA, FEMALE; GENITALIA, MALE; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MATERNAL EXPOSURE; MOTHERS; PITUITARY-ADRENAL SYSTEM; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX FACTORS; STRESS, PSYCHOLOGICAL; TESTOSTERONE;

EID: 84943623556     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1335     Document Type: Review

References (99)

1. Veru F, Laplante DP, Luheshi G, King S. Prenatal maternal stress exposure and immune function in the offspring. Stress. 2014;17: 133-148.
2. Bellinger DL, Lubahn C, Lorton D. Maternal and early life stress effects on immune function: relevance to immunotoxicology. J Immunotoxicol. 2008;5:419-444.
3. Hohwu L, Zhu JL, Graversen L, Li J, Sorensen TI, Obel C. Prenatal parental separation and body weight, including development of overweight and obesity later in childhood. PloS One. 2015;10: e0119138.
4. Stout SA, Espel EV, Sandman CA, Glynn LM, Davis EP. Fetal programming of children's obesity risk. Psychoneuroendocrinology. 2015;53:29-39.
5. DiPietro JA, CostiganKA,Gurewitsch ED. Fetal response to induced maternal stress. Early Hum Dev. 2003;74:125-138.
6. Monk C, Fifer WP, Myers MM, Sloan RP, Trien L, Hurtado A. Maternal stress responses and anxiety during pregnancy: effects on fetal heart rate. Dev Psychobiol. 2000;36:67-77.
7. Betts KS, Williams GM, Najman JM, Alati R. The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems. Depress Anxiety. 2015;32:82-90.
8. Palagini L, Drake CL, Gehrman P, Meerlo P, Riemann D. Early-life origin of adult insomnia: does prenatal-early-life stress play a role? Sleep Med. 2015;16:446-456.
9. Henry C, KabbajM,Simon H, LeMoalM,Maccari S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol. 1994;6:341-345.
10. Maccari S, Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology. 2007; 32(suppl 1):S10 -S15.
11. Bergman K, Sarkar P, Glover V, O'Connor TG. Maternal prenatal cortisol and infant cognitive development: moderation by infantmother attachment. Biol Psychiatry. 2010;67:1026-1032.
12. 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.
13. Sarkar P, Bergman K, Fisk NM, Glover V. Maternal anxiety at amniocentesis and plasma cortisol. Prenat Diagn. 2006;26:505-509.
14. Sarkar P, Bergman K, Fisk NM, O'Connor TG, Glover V. Amniotic fluid testosterone: relationship with cortisol and gestational age. Clin Endocrinol (Oxf). 2007;67:743-747.
15. Mueller BR, Bale TL. Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity. Physiol Behav. 2006;88:605-614.
16. Bronson SL, Bale TL. Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal anti-inflammatory treatment. Endocrinology. 2014;155:2635-2646.
17. Markham JA, Mullins SE, Koenig JI. Periadolescent maturation of the prefrontal cortex is sex-specific and is disrupted by prenatal stress. J Comp Neurol. 2013;521:1828-1843.
18. Khashan AS, Abel KM, McNamee R, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008;65:146-152.
19. Kinney DK, MunirKM,Crowley DJ, MillerAM.Prenatal stress and risk for autism. Neurosci Biobehav Rev. 2008; 32:1519-1532.
20. Rodriguez A, Bohlin G. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry. 2005;46:246-254.
21. Turcotte-Tremblay AM, Lim R, Laplante DP, Kobzik L, Brunet A, King S. Prenatal maternal stress predicts childhood asthma in girls: project ice storm. BioMed Res Int. 2014;2014:201717.
22. Postma DS. Gender differences in asthma development and progression. Gend Med. 2007;4(suppl B):S133-S146.
23. Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology. 2008;33:536-545.
24. PiccinelliM,Wilkinson G. Gender differences in depression. Critical review. Br J Psychiatry. 2000;177:486-492.
25. Welsh M, Saunders PT, Fisken M, et al. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest. 2008;118:1479-1490.
26. Macleod DJ, Sharpe RM, Welsh M, et al. Androgen action in the masculinization programming window and development of male reproductive organs. Int J Androl. 2010;33:279-287.
27. van den Driesche S, Scott HM, MacLeod DJ, Fisken M, Walker M, Sharpe RM. Relative importance of prenatal and postnatal androgen action in determining growth of the penis and anogenital distance in the rat before, during and after puberty. Int J Androl. 2011; 34:e578-e586.
28. Hines M. Brain Gender. New York, NY: Oxford University Press; 2005.
29. Arnold AP, Gorski RA. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci. 1984; 7:413-442.
30. Dahlöf LG, Hard E, Larsson K. Influence of maternal stress on the development of the fetal genital system. Physiol Behav. 1978;20: 193-195.
31. Crump CJ, Chevins PF. Prenatal stress reduces fertility of male offspring in mice, without affecting their adult testosterone levels. Horm Behav. 1989;23:333-343.
32. Ward IL. Prenatal stress feminizes and demasculinizes the behavior of males. Science. 1972;175:82-84.
33. Pallarés ME, Adrover E, Baier CJ, et al. Prenatal maternal restraint stress exposure alters the reproductive hormone profile and testis development of the rat male offspring. Stress. 2013;16:429-440.
34. Kapoor A, Matthews SG. Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring. J Physiol. 2011;589:755-766.
35. Dean A, Sharpe RM. Clinical review: Anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders. J Clin Endocrinol Metab. 2013;98:2230-2238.
36. WolfCJr, Lambright C,MannP, PriceM,Cooper RL, Ostby J, Gray LE Jr. Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,pβ-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicol Ind Health. 1999;15:94-118.
37. Ward IL, Weisz J. Maternal stress alters plasma testosterone in fetal males. Science. 1980;207:328-329.
38. Ward IL, Weisz J. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers. Endocrinology. 1984; 114:1635-1644.
39. Bánszegi O, Altbäcker V, Bilkó A. Intrauterine position influences anatomy and behavior in domestic rabbits. Physiol Behav. 2009; 98:258-262.
40. Barrett ES, Parlett LE, Redmon JB, Swan SH. Evidence for sexually dimorphic associations between maternal characteristics and anogenital distance, a marker of reproductive development. Am J Epidemiol. 2014;179:57-66.
41. Foecking EM, McDevitt MA, Acosta-Martnez M, Horton TH, Levine JE. Neuroendocrine consequences of androgen excess in female rodents. Horm Behav. 2008;53:673-692.
42. Orgeur P. Sexual play behavior in lambs androgenized in utero. Physiol Behav. 1995;57:185-187.
43. Dean A, Smith LB, Macpherson S, Sharpe RM. The effect of dihydrotestosterone exposure during or prior to the masculinization programming window on reproductive development in male and female rats. Int J Androl. 2012;35:330-339.
44. Bánszegi O, Altbäcker V, Dcs A, Bilkó A. Testosterone treatment of pregnant rabbits affects sexual development of their daughters. Physiol Behav. 2010;101:422-427.
45. Herrenkohl LR. Prenatal stress reduces fertility and fecundity in female offspring. Science. 1979;206:1097-1099.
46. Vom Saal FS, Even MD, Quadagno DM. Effects of maternal stress on puberty, fertility and aggressive behavior of female mice from different intrauterine positions. Physiol Behav. 1991;49:1073-1078.
47. Schöpper H, Klaus T, Palme R, Ruf T, Huber S. Sex-specific impact of prenatal stress on growth and reproductive parameters of guinea pigs. J Comp Physiol B. 2012;182:1117-1127.
48. Herrenkohl LR, Politch JA. Effects of prenatal stress on the estrous cycle of female offspring as adults. Experientia. 1978;34:1240-1241.
49. Politch JA, Herrenkohl LR. Effects of prenatal stress on reproduction in male and female mice. Physiol Behav. 1984;32:95-99.
50. Kinsley C, Svare B. Genotype modulates prenatal stress effects on aggression in male and female mice. Behav Neural Biol. 1987;47: 138-150.
51. Kinsley C, Svare B. Prenatal stress alters maternal aggression in mice. Physiol Behav. 1988;42:7-13.
52. Hotchkiss AK, Lambright CS, Ostby JS, Parks-Saldutti L, Vandenbergh JG, Gray LE Jr. Prenatal testosterone exposure permanently masculinizes anogenital distance, nipple development, and reproductive tract morphology in female Sprague-Dawley rats. Toxicol Sci. 2007;96:335-345.
53. Trivers RL, Willard DE. Natural selection of parental ability to vary the sex ratio of offspring. Science. 1973;179:90-92.
54. Wells JC. Natural selection and sex differences in morbidity and mortality in early life. J Theor Biol. 2000;202:65-76.
55. Cooperstock M, Campbell J. Excess males in preterm birth: interactions with gestational age, race, and multiple birth. Obstet Gynecol. 1996;88:189-193.
56. 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.
57. Zetterstrom K, Lindeberg SN, Haglund B, Hanson U. The association of maternal chronic hypertension with perinatal death in male and female offspring: a record linkage study of 866,188 women. BJOG. 2008;115:1436-1442.
58. Bruckner TA, Catalano R, Ahern J. Male fetal loss in the U.S. following the terrorist attacks of September 11, 2001. BMC Public Health. 2010;10:273.
59. Fukuda M, Fukuda K, Shimizu T, Mller H. Decline in sex ratio at birth after Kobe earthquake. Hum Reprod. 1998;13:2321-2322.
60. Peterka M, Peterková R, Likovsk Z. Chernobyl: relationship between the number of missing newborn boys and the level of radiation in the Czech regions. Environ Health Perspect. 2007;115:1801-1806.
61. Bruckner T, Catalano R. The sex ratio and age-specific male mortality: evidence for culling in utero. Am J Hum Biol. 2007;19:763-773.
62. Desgent S, Duss S, SanonNT,et al. Early-life stress is associated with gender-based vulnerability to epileptogenesis in rat pups. PloS One. 2012;7:e42622.
63. Seale JV, Wood SA, Atkinson HC, Harbuz MS, Lightman SL. Postnatal masculinization alters the HPA axis phenotype in the adult female rat. J Physiol. 2005;563:265-274.
64. Steckler T, Wang J, Bartol FF, Roy SK, Padmanabhan V. Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology. 2005;146:3185-3193.
65. Carlsen SM, Jacobsen G, Romundstad P. Maternal testosterone levels during pregnancy are associated with offspring size at birth. Eur J Endocrinol. 2006;155:365-370.
66. Cocksedge KA, Saravelos SH, Wang Q, Tuckerman E, Laird SM, Li TC. Does free androgen index predict subsequent pregnancy outcome in women with recurrent miscarriage? Hum Reprod. 2008; 23:797-802.
67. James WH. Hypothesis: high levels of maternal adrenal androgens are a major cause of miscarriage and other forms of reproductive suboptimality. J Theor Biol. 2015;364:316-320.
68. Boomsma CM, Fauser BC, Macklon NS. Pregnancy complications in women with polycystic ovary syndrome. Semin Reprod Med. 2008;26:72-84.
69. Palomba S, Marotta R, Di Cello A, et al. Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: a longitudinal case-control study. Clin Endocrinol (Oxf). 2012;77:898-904.
70. Wainstock T, Shoham-Vardi I, Glasser S, Anteby E, Lerner-Geva L. Fetal sex modifies effects of prenatal stress exposure and adverse birth outcomes. Stress. 2015;18:49-56.
71. Torche F, Kleinhaus K. Prenatal stress, gestational age and secondary sex ratio: the sex-specific effects of exposure to a natural disaster in early pregnancy. Hum Reprod. 2012;27:558-567.
72. Sandman CA, Glynn LM, Davis EP. Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res. 2013;75:327-335.
73. Cao X, Laplante DP, Brunet A, Ciampi A, King S. Prenatal maternal stress affects motor function in 51/2-year-old children: project ice storm. Dev Psychobiol. 2014;56:117-125.
74. Huizink AC, Bartels M, Rose RJ, Pulkkinen L, Eriksson CJ, Kaprio J. Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring. J Epidemiol Community Health. 2008;62:e5.
75. Lumey LH. Reproductive outcomes inwomenprenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort. Proc Nutr Soc. 1998;57:129-135.
76. Mendiola J, Roca M, Minguez-Alarcon L, et al. Anogenital distance is related to ovarian follicular number in young Spanish women: a cross-sectional study. Environ Health. 2012;11:90.
77. Mendiola J, Stahlhut RW, Jrgensen N, Liu F, Swan SH. Shorter anogenital distance predicts poorer semen quality in young men in Rochester, New York. Environ Health Perspect. 2011;119:958-963.
78. Eisenberg ML, Shy M, Walters RC, Lipshultz LI. The relationship between anogenital distance and azoospermia in adult men. Int J Androl. 2012;35:726-730.
79. Dohrenwend BS, Dohrenwend BP. Some issues in research on stressful life events. J Nerv Ment Dis. 1978;166:7-15.
80. Dohrenwend BS, Krasnoff L, Askenasy AR, Dohrenwend BP. Exemplification of a method for scaling life events: the Peri Life Events Scale. J Health Soc Behav. 1978;19:205-229.
81. Holmes TH, Rahe RH. The Social Readjustment Rating Scale. J Psychosom Res. 1967;11:213-218.
82. Sathyanarayana S, Beard L, Zhou C, Grady R. Measurement and correlates of ano-genital distance in healthy, newborn infants. Int J Androl. 2010;33:317-323.
83. Barrett ES, Parlett LE, Sathyanarayana S, et al. Prenatal exposure to stressful life events is associated with masculinized anogenital distance (AGD) in female infants. Physiol Behav. 2013;114-115:14-20.
84. Barrett ES, Redmon JB, Wang C, Sparks A, Swan SH. Exposure to prenatal life events stress is associated with masculinized play behavior in girls. Neurotoxicology. 2014;41C:20-C27.
85. Swan SH. Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res. 2008;108:177-184.
86. Swan SH, Sathyanarayana S, Barrett ES, Janssen SJ, Liu F, Nguyen RHN, Redmon JB. First-trimester phthalate exposure is linked to shorter anogenital distance in newborn boys. Hum. Reprod. 2015; 30:963-972.
87. Suzuki Y, Yoshinaga J, Mizumoto Y, Serizawa S, Shiraishi H. Foetal exposure to phthalate esters and anogenital distance in male newborns. Int J Androl. 2012;35:236-244.
88. Bustamante-Montes LP, Hernandez-Valero MA, Flores-Pimentel D, et al. Prenatal exposure to phthalates is associated with decreased anogenital distance and penile size in male newborns. J Dev Orig Health Dis. 2013;4:300-306.
89. Callegari C, Everett S, Ross M, Brasel JA. Anogenital ratio: measure of fetal virilization in premature and full-term newborn infants. J Pediatr. 1987;111:240-243.
90. Pasterski V, Hindmarsh P, Geffner M, Brook C, Brain C, Hines M. Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH).HormBehav. 2007;52:368-374.
91. Pasterski V, Geffner ME, Brain C, Hindmarsh P, Brook C, Hines M. Prenatal hormones and childhood sex segregation: playmate and play style preferences in girls with congenital adrenal hyperplasia. Horm Behav. 2011;59:549-555.
92. Pasterski VL, Geffner ME, Brain C, Hindmarsh P, Brook C, Hines M. Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev. 2005;76:264-278.
93. Pasterski V, Zucker KJ, Hindmarsh PC, et al. Increased cross-gender identification independent of gender role behavior in girls with congenital adrenal hyperplasia: results from a standardized assessment of 4- to 11-year-old children. Arch Sex Behav. 2014;44:1363-1375.
94. Smith R, Smith JI, Shen X, et al. Patterns of plasma corticotropinreleasing hormone, progesterone, estradiol, and estriol change and the onset of human labor. J Clin Endocrinol Metab. 2009;94:2066-2074.
95. Hill M, Paková A, Kanßeva R, et al. Steroid profiling in pregnancy: a focus on the human fetus. J Steroid Biochem Mol Biol. 2014;139: 201-222.
96. Rehman KS, Carr BR. Sex differences in adrenal androgens. Semin Reprod Med. 2004;22:349-360.
97. Kaiser S, Kruijver FP, Swaab DF, Sachser N. Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav Brain Res. 2003;144:199-210.
98. Kaiser S, Sachser N. The social environment during pregnancy and lactation affects the female offsprings' endocrine status and behaviour in guinea pigs. Physiol Behav. 1998;63:361-366.
99. Bousfield GR, Butnev VY, Gotschall RR, Baker VL, Moore WT. Structural features of mammalian gonadotropins. Mol Cell Endocrinol. 1996;125:3-19.