Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-20T17:40:32.388Z Has data issue: false hasContentIssue false

Associations between maternal prenatal cortisol and fetal growth are specific to infant sex: findings from the Wirral Child Health and Development Study

Published online by Cambridge University Press:  10 April 2018

E. C. Braithwaite*
Affiliation:
School of Life Sciences and Education, Staffordshire University, Stoke-on-Trent, UK
J. Hill
Affiliation:
School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK
A. Pickles
Affiliation:
Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK
V. Glover
Affiliation:
Institute of Reproductive and Developmental Biology, Imperial College London, London, UK
K. O’Donnell
Affiliation:
Douglas Hospital Research Centre, McGill University, Montreal, Canada Canadian Institute for Advanced Research, Child and Brain Development Program, Ontario, Canada
H. Sharp
Affiliation:
Department of Psychological Sciences, Institute of Psychology, Health and Society, Liverpool, UK
*
*Address for correspondence: E. C. Braithwaite, School of Life Sciences and Education, Staffordshire University, Stoke-on-Trent ST4 2DE, UK.E-mail: elizabeth.braithwaite@staffs.ac.uk

Abstract

Recent findings highlight that there are prenatal risks for affective disorders that are mediated by glucocorticoid mechanisms, and may be specific to females. There is also evidence of sex differences in prenatal programming mechanisms and developmental psychopathology, whereby effects are in opposite directions in males and females. As birth weight is a risk for affective disorders, we sought to investigate whether maternal prenatal cortisol may have sex-specific effects on fetal growth. Participants were 241 mothers selected from the Wirral Child Health and Development Study (WCHADS) cohort (n=1233) using a psychosocial risk stratifier, so that responses could be weighted back to the general population. Mothers provided saliva samples, which were assayed for cortisol, at home over 2 days at 32 weeks gestation (on waking, 30-min post-waking and during the evening). Measures of infant birth weight (corrected for gestational age) were taken from hospital records. General population estimates of associations between variables were obtained using inverse probability weights. Maternal log of the area under the curve cortisol predicted infant birth weight in a sex-dependent manner (interaction term P=0.029). There was a positive and statistically significant association between prenatal cortisol in males, and a negative association in females that was not statistically significant. A sex interaction in the same direction was evident when using the waking (P=0.015), and 30-min post-waking (P=0.013) cortisol, but not the evening measure. There was no interaction between prenatal cortisol and sex to predict gestational age. Our findings add to an emerging literature that suggests that there may be sex-specific mechanisms that underpin fetal programming.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Barker, DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998; 95, 115128.Google Scholar
2. Barker, DJ. Fetal origins of cardiovascular disease. Ann Med. 1999; 31(Suppl. 1), 36.Google Scholar
3. O’Donnell, KJ, Meaney, MJ. Fetal origins of mental health: the developmental origins of health and disease hypothesis. Am J Psychiatry. 2017; 174, 319328.Google Scholar
4. Breslau, N. Psychiatric sequelae of low birth weight. Epidemiol Rev. 1995; 17, 96106.Google Scholar
5. Sucksdorff, M, Lehtonen, L, Chudal, R, et al. Preterm birth and poor fetal growth as risk factors of attention-deficit/hyperactivity disorder. Pediatrics. 2015; 136, e599e608.Google Scholar
6. Thomas, K, Harrison, G, Zammit, S, et al. Association of measures of fetal and childhood growth with non-clinical psychotic symptoms in 12-year-olds: the ALSPAC cohort. Br J Psychiatry. 2009; 194, 521526.Google Scholar
7. Abel, KM, Wicks, S, Susser, ES, et al. Birth weight, schizophrenia, and adult mental disorder: is risk confined to the smallest babies? Arch Gen Psychiatry. 2010; 67, 923930.Google Scholar
8. Wiles, NJ, Peters, TJ, Leon, DA, Lewis, G. Birth weight and psychological distress at age 45-51 years: results from the Aberdeen Children of the 1950s cohort study. Br J Psychiatry. 2005; 187, 2128.Google Scholar
9. Mallen, C, Mottram, S, Thomas, E. Birth factors and common mental health problems in young adults: a population-based study in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol. 2008; 43, 325330.Google Scholar
10. Raikkonen, K, Pesonen, AK, Roseboom, TJ, Eriksson, JG. Early determinants of mental health. Best Pract Res Clin Endocrinol Metab. 2012; 26, 599611.Google Scholar
11. Berle, JO, Mykletun, A, Daltveit, AK, Rasmussen, S, Dahl, AA. Outcomes in adulthood for children with foetal growth retardation. A linkage study from the Nord-Trondelag Health Study (HUNT) and the Medical Birth Registry of Norway. Acta Psychiatr Scand. 2006; 113, 501509.Google Scholar
12. Herva, A, Pouta, A, Hakko, H, et al. Birth measures and depression at age 31 years: the Northern Finland 1966 Birth Cohort Study. Psychiatry Res. 2008; 160, 263270.Google Scholar
13. Vasiliadis, HM, Gilman, SE, Buka, SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008; 117, 306312.Google Scholar
14. Wojcik, W, Lee, W, Colman, I, Hardy, R, Hotopf, M. Foetal origins of depression? A systematic review and meta-analysis of low birth weight and later depression. Psychol Med. 2013; 43, 112.Google Scholar
15. Costello, EJ, Worthman, C, Erkanli, A, Angold, A. Prediction from low birth weight to female adolescent depression: a test of competing hypotheses. Arch Gen Psychiatry. 2007; 64, 338344.Google Scholar
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, 422430.Google Scholar
17. 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, 536545.Google Scholar
18. Quarini, C, Pearson, RM, Stein, A, et al. Are female children more vulnerable to the long-term effects of maternal depression during pregnancy? J Affect Disord. 2016; 189, 329335.Google Scholar
19. Sandman, CA, Glynn, LM, Davis, EP. Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res. 2013; 75, 327335.Google Scholar
20. Buss, C, Davis, EP, Shahbaba, B, et al. 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, E1312E1319.Google Scholar
21. Tibu, F, Hill, J, Sharp, H, et al. Evidence for sex differences in fetal programming of physiological stress reactivity in infancy. Dev Psychopathol. 2014; 26(Pt 1), 879888.Google Scholar
22. Vidal-Ribas, P, Pickles, A, Tibu, F, Sharp, H, Hill, J. Sex differences in the associations between vagal reactivity and oppositional defiant disorder symptoms. J Child Psychol Psychiatry 2017; 58, 988997.Google Scholar
23. Vidal-Ribas, P, Brotman, MA, Valdivieso, I, Leibenluft, E, Stringaris, A. The status of irritability in psychiatry: a conceptual and quantitative review. J Am Acad Child Adolesc Psychiatry. 2016; 55, 556570.Google Scholar
24. Rowe, R, Maughan, B, Pickles, A, Costello, EJ, Angold, A. The relationship between DSM-IV oppositional defiant disorder and conduct disorder: findings from the Great Smoky Mountains Study. J Child Psychol Psychiatry. 2002; 43, 365373.Google Scholar
25. Seckl, JR. Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res. 2008; 167, 1734.Google Scholar
26. Braithwaite, EC, Pickles, A, Sharp, H, et al. Maternal prenatal cortisol predicts infant negative emotionality in a sex-dependent manner. Physiol Behav. 2017; 175, 3136.Google Scholar
27. Braithwaite, EC, Murphy, SE, Ramchandani, PG, Hill, J. Associations between biological markers of prenatal stress and infant negative emotionality are specific to sex. Psychoneuroendocrinology. 2017; 86, 17.Google Scholar
28. Hinnant, JB, El-Sheikh, M. Codevelopment of externalizing and internalizing symptoms in middle to late childhood: sex, baseline respiratory sinus arrhythmia, and respiratory sinus arrhythmia reactivity as predictors. Dev Psychopathol. 2013; 25, 419436.Google Scholar
29. Morales, S, Beekman, C, Blandon, AY, Stifter, CA, Buss, KA. Longitudinal associations between temperament and socioemotional outcomes in young children: the moderating role of RSA and gender. Dev Psychobiol. 2015; 57, 105119.Google Scholar
30. Marsman, R, Swinkels, SH, Rosmalen, JG, et al. HPA-axis activity and externalizing behavior problems in early adolescents from the general population: the role of comorbidity and gender The TRAILS study. Psychoneuroendocrinology. 2008; 33, 789798.Google Scholar
31. Dietrich, A, Ormel, J, Buitelaar, JK, et al. Cortisol in the morning and dimensions of anxiety, depression, and aggression in children from a general population and clinic-referred cohort: an integrated analysis. The TRAILS study. Psychoneuroendocrinology. 2013; 38, 12811298.Google Scholar
32. Dorn, LD, Kolko, DJ, Susman, EJ, et al. Salivary gonadal and adrenal hormone differences in boys and girls with and without disruptive behavior disorders: contextual variants. Biol Psychol. 2009; 81, 3139.Google Scholar
33. Sharp, H, Pickles, A, Meaney, M, et al. Frequency of infant stroking reported by mothers moderates the effect of prenatal depression on infant behavioural and physiological outcomes. PLoS One. 2012; 7, e45446.Google Scholar
34. Noble, M, Wright, G, Dibben, C, et al. The English Indices of Deprivation 2004 (revised). Report to the Office of the Deputy Prime Minister. Neighbourhood Renewal Unit: London; 2004.Google Scholar
35. Wehby, GL, Gili, JA, Pawluk, M, Castilla, EE, Lopez-Camelo, JS. Disparities in birth weight and gestational age by ethnic ancestry in South American countries. Int J Public Health. 2015; 60, 343351.Google Scholar
36. Moffitt, TE, Caspi, A, Krueger, R, et al. Do partners agree about abuse in their relationship?: A psychometric evaluation of interpartner agreement. Psychological Assessment. 1997; 9, 4756.Google Scholar
37. Spielberger, CD, Gorsuch, RL, Lushene, R, Vagg, PR, Jacobs, GA. Manual for the State-Trait Anxiety Inventory. 1983. Consulting Psychologists Press, Inc: Palo Alto.Google Scholar
38. Hill, J, Breen, G, Quinn, J, et al. Evidence for interplay between genes and maternal stress in utero: monoamine oxidase A polymorphism moderates effects of life events during pregnancy on infant negative emotionality at 5 weeks. Genes Brain Behav. 2013; 12, 388396.Google Scholar
39. Binder, DA. On the variances of asymptotically normal estimators from complex surveys. Int Stat Rev. 1983; 51, 279292.Google Scholar
40. Newcombe, R, Milne, BJ, Caspi, A, Poulton, R, Moffitt, TE. Birthweight predicts IQ: fact or artefact? Twin Res Hum Genet. 2007; 10, 581586.Google Scholar
41. Hayes, B, Sharif, F. Behavioural and emotional outcome of very low birth weight infants – literature review. J Matern Fetal Neonatal Med. 2009; 22, 849856.Google Scholar
42. McCormick, MC, Gortmaker, SL, Sobol, AM. Very low birth weight children: behavior problems and school difficulty in a national sample. J Pediatr. 1990; 117, 687693.Google Scholar
43. Banerjee, TD, Middleton, F, Faraone, SV. Environmental risk factors for attention-deficit hyperactivity disorder. Acta Paediatr. 2007; 96, 12691274.Google Scholar
44. Sorensen, HT, Sabroe, S, Olsen, J, et al. Birth weight and cognitive function in young adult life: historical cohort study. BMJ. 1997; 315, 401403.Google Scholar
45. Leonard, H, Nassar, N, Bourke, J, et al. Relation between intrauterine growth and subsequent intellectual disability in a ten-year population cohort of children in Western Australia. Am J Epidemiol. 2008; 167, 103111.Google Scholar
46. van Mil, NH, Steegers-Theunissen, RP, Motazedi, E, et al. Low and high birth weight and the risk of child attention problems. J Pediatr. 2015; 166, 862869.e1-3.Google Scholar
47. Kim, DJ, Davis, EP, Sandman, CA, et al. Prenatal maternal cortisol has sex-specific associations with child brain network properties. Cereb Cortex. 2017; 27, 52305241.Google Scholar
48. Kivlighan, KT, DiPietro, JA, Costigan, KA, Laudenslager, ML. Diurnal rhythm of cortisol during late pregnancy: associations with maternal psychological well-being and fetal growth. Psychoneuroendocrinology. 2008; 33, 12251235.Google Scholar
49. Entringer, S, Buss, C, Andersen, J, Chicz-DeMet, A, Wadhwa, PD. Ecological momentary assessment of maternal cortisol profiles over a multiple-day period predicts the length of human gestation. Psychosomatic Med. 2011; 73, 469474.Google Scholar
50. Goedhart, G, Vrijkotte, TG, Roseboom, TJ, et al. Maternal cortisol and offspring birthweight: results from a large prospective cohort study. Psychoneuroendocrinology. 2010; 35, 644652.Google Scholar
51. Bale, TL. The placenta and neurodevelopment: sex differences in prenatal vulnerability. Dialogues Clin Neurosci. 2016; 18, 459464.Google Scholar
52. Bronson, SL, Bale, TL. The placenta as a mediator of stress effects on neurodevelopmental reprogramming. Neuropsychopharmacology. 2016; 41, 207218.Google Scholar
53. Elder, GJ, Wetherell, MA, Barclay, NL, Ellis, JG. The cortisol awakening response – applications and implications for sleep medicine. Sleep Med Rev. 2014; 18, 215224.Google Scholar
54. Clow, A, Thorn, L, Evans, P, Hucklebridge, F. The awakening cortisol response: methodological issues and significance. Stress. 2004; 7, 2937.Google Scholar