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Associations among prenatal stress, maternal antioxidant intakes in pregnancy, and child temperament at age 30 months

  • L. R. Lipton (a1), K. J. Brunst (a1), S. Kannan (a2) (a3), Y.-M. Ni (a4), H. B. Ganguri (a5), R. J. Wright (a1) (a6) and M. Bosquet Enlow (a7) (a8)...


Prenatal stress and prenatal nutrition each have demonstrable impact on fetal development, with implications for child neurodevelopment and behavior. However, few studies have examined their joint influences despite evidence of potential interactive effects. We examined associations among prenatal stress, prenatal antioxidant intakes, and child temperament in a sociodemographically diverse pregnancy cohort (N=137 mother–child dyads). In mid-pregnancy, mothers completed an assessment of recent negative life events as a measure of prenatal stress and an assessment of prenatal diet. When the children were 30 months of age, mothers completed the Early Childhood Behavior Questionnaire-Very Short form, which provides scores on child Negative Affectivity, Effortful Control, and Surgency/Extraversion. Linear regressions tested associations between maternal prenatal negative life events and child temperament, and effect modification by maternal prenatal antioxidant intakes (vitamins A, C, and E, magnesium, zinc, selenium, β-carotene). Analyses revealed that increased maternal prenatal negative life events were associated with higher child Negative Affectivity (β=0.08, P=0.009) but not with child Effortful Control (β=−0.03, P=0.39) or Surgency/Extraversion (β=0.04, P=0.14). Prenatal intakes of zinc and selenium modified this effect: Maternal exposure to prenatal negative life events was associated with higher child Negative Affectivity in the presence of lower intakes of zinc and selenium. Modification effects approached significance for vitamins A and C. The results suggest that the combination of elevated stress exposures and lower antioxidant intakes in pregnancy increases the likelihood of heightened child temperamental negative affectivity. Increased antioxidant intakes during pregnancy may protect against influences of prenatal stress on child temperament.


Corresponding author

*Address for correspondence: M. Bosquet Enlow, Department of Psychiatry, Boston Children’s Hospital, 300 Longwood Avenue, AT-120.3, Mailstop BCH 3199, Boston, MA 02115, USA. (Email


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Present address: Department of Environmental Health, University of Cincinnati College of Medicine, Cincinnati, OH, USA.


Present address: Kronsys, Inc., Raleigh, NC, USA.



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1. Gartstein, MA, Rothbart, MK. Studying infant temperament via a revision of the Infant Behavior Questionnaire. Infant Behav Dev. 2003; 7, 517522.
2. Bale, TL, Baram, TZ, Brown, AS, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010; 68, 314319.
3. Knudsen, EI, Heckman, JJ, Cameron, JL, et al. Economic, neurobiological, and behavioral perspectives on building America’s future workforce. Proc Natl Acad Sci U S A. 2006; 103, 1015510162.
4. Shonkoff, JP, Garner, AS. The lifelong effects of early childhood adversity and toxic stress. Pediatrics. 2012; 129, e232e246.
5. Charil, A, Laplante, DP, Vaillancourt, C, et al. Prenatal stress and brain development. Brain Res Rev. 2010; 65, 5679.
6. Weiss, B, Bellinger, DC. Social ecology of children’s vulnerability to environmental pollutants. Environ Health Perspect. 2006; 114, 14791485.
7. Brunst, K, Enlow, M, Kannan, S, et al. Effects of prenatal social stress and maternal dietary fatty acid ratio on infant temperament: Does race matter? Epidemiology. 2014; 4, 1000167.
8. Huizink, AC, de Medina, PG, Mulder, EJ, et al. Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry. 2002; 41, 10781085.
9. Brand, SR, Engel, SM, Canfield, RL, et al. The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Ann N Y Acad Sci. 2006; 1071, 454458.
10. Davis, EP, Glynn, LM, Schetter, CD, et al. Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry. 2007; 46, 737746.
11. Lin, B, Crnic, KA, Luecken, LJ, et al. Maternal prenatal stress and infant regulatory capacity in Mexican Americans. Infant Behav Dev. 2014; 37, 571582.
12. Buitelaar, JK, Huizink, AC, Mulder, EJ, et al. Prenatal stress and cognitive development and temperament in infants. Neurobiol Aging. 2003; 24(Suppl. 1), S53S60, discussion S67–S58.
13. Gutteling, BM, de Weerth, C, Willemsen-Swinkels, SH, et al. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry. 2005; 14, 4151.
14. Zhu, P, Sun, MS, Hao, JH, et al. Does prenatal maternal stress impair cognitive development and alter temperament characteristics in toddlers with healthy birth outcomes? Dev Med Child Neurol. 2014; 56, 283289.
15. Monk, C, Georgieff, MK, Osterholm, EA. Research review: maternal prenatal distress and poor nutrition – mutually influencing risk factors affecting infant neurocognitive development. J Child Psychol Psychiatry. 2013; 54, 115130.
16. Van den Bergh, BR, Marcoen, A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev. 2004; 75, 10851097.
17. Michel, TM, Frangou, S, Thiemeyer, D, et al. Evidence for oxidative stress in the frontal cortex in patients with recurrent depressive disorder—a postmortem study. Psychiatry Res. 2007; 151, 145150.
18. Moylan, S, Jacka, FN, Pasco, JA, et al. How cigarette smoking may increase the risk of anxiety symptoms and anxiety disorders: a critical review of biological pathways. Brain Behav. 2013; 3, 302326.
19. Arcego, DM, Krolow, R, Lampert, C, et al. Stress during the pre-pubertal period leads to long-term diet-dependent changes in anxiety-like behavior and in oxidative stress parameters in male adult rats. Neurochem Res. 2013; 38, 17911800.
20. Feng, Z, Zou, X, Jia, H, et al. Maternal docosahexaenoic acid feeding protects against impairment of learning and memory and oxidative stress in prenatally stressed rats: possible role of neuronal mitochondria metabolism. Antioxid Redox Signal. 2012; 16, 275289.
21. Sivonova, M, Zitnanova, I, Hlincikova, L, et al. Oxidative stress in university students during examinations. Stress. 2004; 7, 183188.
22. Davis, JM, Auten, RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med. 2010; 15, 191195.
23. Myllynen, P, Pasanen, M, Vahakangas, K. The fate and effects of xenobiotics in human placenta. Expert Opin Drug Metab Toxicol. 2007; 3, 331346.
24. Wolkowitz, OM, Epel, ES, Reus, VI, et al. Depression gets old fast: do stress and depression accelerate cell aging? Depress Anxiety. 2010; 27, 327338.
25. McKinney, BC, Oh, H, Sibille, E. Age-by-disease biological interactions: implications for late-life depression. Front Genet. 2012; 3, 237.
26. Kananen, L, Surakka, I, Pirkola, S, et al. Childhood adversities are associated with shorter telomere length at adult age both in individuals with an anxiety disorder and controls. PLoS One. 2010; 5, e10826.
27. Johnson, AW, Jaaro-Peled, H, Shahani, N, et al. Cognitive and motivational deficits together with prefrontal oxidative stress in a mouse model for neuropsychiatric illness. Proc Natl Acad Sci U S A. 2013; 110, 1246212467.
28. Teyssier, JR, Ragot, S, Chauvet-Gelinier, JC, et al. Expression of oxidative stress-response genes is not activated in the prefrontal cortex of patients with depressive disorder. Psychiatry Res. 2011; 186, 244247.
29. Gallo, C, Renzi, P, Loizzo, S, et al. Potential therapeutic effects of vtiamin E and C on placental oxidative stress induced by nicotine: an in vitro evidence. Open Biochem J. 2010; 4, 7782.
30. Kelvin, EA, Edwards, S, Jedrychowski, W, et al. Modulation of the effect of prenatal PAH exposure on PAH-DNA adducts in cord blood by plasma antioxidants. Cancer Epidemiol Biomarkers Prev. 2009; 18, 22622268.
31. Hossain, M, Mazzone, P, Tierney, W, et al. In vitro assessment of tobacco smoke toxicity at the BBB: do antioxidant supplements have a protective role? BMC Neurosci. 2011; 12, 92.
32. Stringhini, S, Sabia, S, Shipley, M, et al. Association of socioeconomic position with health behaviors and mortality. JAMA. 2010; 303, 11591166.
33. Mouchacca, J, Abbott, GR, Ball, K. Associations between psychological stress, eating, physical activity, sedentary behaviours and body weight among women: a longitudinal study. BMC Public Health. 2013; 13, 828.
34. Hurley, KM, Caulfield, LE, Sacco, LM, et al. Psychosocial influences in dietary patterns during pregnancy. J Am Diet Assoc. 2005; 105, 963966.
35. Braveman, P, Marchi, K, Egerter, S, et al. Poverty, near-poverty, and hardship around the time of pregnancy. Matern Child Health J. 2010; 14, 2035.
36. Brunst, KJ, Wright, RO, DiGioia, K, et al. Racial/ethnic and sociodemographic factors associated with micronutrient intakes and inadequacies among pregnant women in an urban US population. Public Health Nutr. 2014; 17, 19601970.
37. Mukherjee, S, Coxe, S, Fennie, K, et al. Stressful life event experiences of pregnant women in the United States: a latent class analysis. Womens Health Issues. 2017; 27, 8392.
38. Burns, ER, Farr, SL, Howards, PP. Stressful life events experienced by women in the year before their infants’ births – United States, 2000–2010. MMWR Morb Mortal Wkly Rep. 2015; 64, 247251.
39. Georgieff, MK. Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr. 2007; 85, 614S620S.
40. Patra, J, Bakker, R, Irving, H, et al. Dose-response relationship between alcohol consumption before and during pregnancy and the risks of low birthweight, preterm birth and small for gestational age (SGA)-a systematic review and meta-analyses. BJOG. 2011; 118, 14111421.
41. Testa, M, Quigley, BM, Eiden, RD. The effects of prenatal alcohol exposure on infant mental development: a meta-analytical review. Alcohol Alcohol. 2003; 38, 295304.
42. Berry, C, Shalowitz, M, Quinn, K, et al. Validation of the crisis in family systems-revised, a contemporary measure of life stressors. Psychol Rep. 2001; 88, 713724.
43. Shalowitz, MU, Berry, CA, Rasinski, KA, et al. A new measure of contemporary life stress: development, validation, and reliability of the CRISYS. Health Serv Res. 1998; 33, 13811402.
44. Berry, CA, Quinn, KA, Portillo, N, et al. Reliability and validity of the Spanish version of the crisis in family systems-revised. Psychol Rep. 2006; 98, 123132.
45. Bosquet Enlow, M, Devick, KL, Brunst, KJ, et al. Maternal lifetime trauma exposure, prenatal cortisol, and infant negative affectivity. Infancy. (In press).
46. Cowell, WJ, Bellinger, DC, Coull, BA, et al. Associations between prenatal exposure to black carbon and memory domains in urban children: modification by sex and prenatal stress. PLoS One. 2015; 10, e0142492.
47. Suglia, SF, Staudenmayer, J, Cohen, S, et al. Cumulative stress and cortisol disruption among Black and Hispanic pregnant women in an urban cohort. Psychol Trauma. 2010; 2, 326334.
48. Tse, AC, Rich-Edwards, JW, Koenen, K, et al. Cumulative stress and maternal prenatal corticotropin-releasing hormone in an urban U.S. cohort. Psychoneuroendocrinology. 2012; 37, 970979.
49. Myers, HF. Ethnicity- and socio-economic status-related stresses in context: an integrative review and conceptual model. J Behav Med. 2009; 32, 919.
50. DiPietro, JA. Maternal stress in pregnancy: considerations for fetal development. J Adolesc Health. 2012; 51, S3S8.
51. Block, G, Hartman, AM, Dresser, CM, et al. A data-based approach to diet questionnaire design and testing. Am J Epidemiol. 1986; 124, 453469.
52. Snook Parrott, M, Bodnar, LM, Simhan, HN, et al. Maternal cereal consumption and adequacy of micronutrient intake in the periconceptional period. Public Health Nutr. 2009; 12, 12761283.
53. Siega-Riz, AM, Bodnar, LM, Savitz, DA. What are pregnant women eating? Nutrient and food group differences by race. Am J Obstet Gynecol. 2002; 186, 480486.
54. Palmer, FB, Anand, KJ, Graff, JC, et al. Early adversity, socioemotional development, and stress in urban 1-year-old children. J Pediatr. 2013; 163, 17331739.e1731.
55. Block, G. Invited commentary: another perspective on food frequency questionnaires. Am J Epidemiol. 2001; 154, 11031104, discussion 1105–1106.
56. Department of Agriculture. USDA National Nutrient Database for Standard Reference. 1998. Nutrient Data Laboratory: Beltsville, MD.
57. Brunst, KJ, Kannan, S, Ni, YM, et al. Validation of a food frequency questionnaire for estimating micronutrient intakes in an urban US sample of multi-ethnic pregnant women. Matern Child Health J. 2016; 20, 250260.
58. Dwyer, J, Picciano, MF, Raiten, DJ. Future directions for the integrated CSFII-NHANES: what we eat in America-NHANES. J Nutr. 2003; 133, 576S581S.
59. Moshfegh, AJ, Rhodes, DG, Baer, DJ, et al. The US Department of Agriculture Automated Multiple-Pass Method reduces bias in the collection of energy intakes. Am J Clin Nutr. 2008; 88, 324332.
60. Willett, WC, Howe, GR, Kushi, LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997; 65, 1220S1228S, discussion 1229S–1231S.
61. Putnam, SP, Rothbart, MK. Development of short and very short forms of the children’s behavior questionnaire. J Pers Assess. 2006; 87, 103113.
62. Putnam, SP, Jacobs, J, Gartstein, MA, et al. Development and assessment of short and very short forms of the Early Childhood Behavior Questionnaire. Paper presented at the International Conference on Infant Studies, 2010; Baltimore, MD.
63. Putnam, S, Ellis, LK, Rothbart, MK. The structure of temperament from infancy through adolescence. In Advances/Proceedings in Research on Temperament (eds. Eliasz A, Angleitner A), 2001; pp. 165–182. Pabst Scientist: Lengerich, Germany.
64. Putnam, SP, Gartstein, MA, Rothbart, MK. Measurement of fine-grained aspects of toddler temperament: the Early Childhood Behavior Questionnaire. Infant Behav Dev. 2006; 29, 386401.
65. Nomaguchi, K, House, AN. Racial-ethnic disparities in maternal parenting stress: the role of structural disadvantages and parenting values. J Health Soc Behav. 2013; 54, 386404.
66. Hovens, JG, Giltay, EJ, van Hemert, AM, et al. Childhood maltreatment and the course of depressive and anxiety disorders: the contribution of personality characteristics. Depress Anxiety. 2016; 33, 2734.
67. Parisi, F, Laoreti, A, Cetin, I. Multiple micronutrient needs in pregnancy in industrialized countries. Ann Nutr Metab. 2014; 65, 1321.
68. Perez-Edgar, K, Schmidt, LA, Henderson, HA, et al. Salivary cortisol levels and infant temperament shape developmental trajectories in boys at risk for behavioral maladjustment. Psychoneuroendocrinology. 2008; 33, 916925.
69. Blumfield, ML, Hure, AJ, Macdonald-Wicks, L, et al. A systematic review and meta-analysis of micronutrient intakes during pregnancy in developed countries. Nutr Rev. 2013; 71, 118132.
70. Blair, MM, Glynn, LM, Sandman, CA, et al. Prenatal maternal anxiety and early childhood temperament. Stress. 2011; 14, 644651.
71. Davis, EP. Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy. 2004; 6, 319331.
72. Davis, EP, Glynn, LM, Dunkel Schetter, C, et al. Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Dev Neurosci. 2005; 27, 299305.
73. Belsky, J, Pluess, M. Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull. 2009; 135, 885908.
74. Belsky, J, Hsieh, KH, Crnic, K. Mothering, fathering, and infant negativity as antecedents of boys’ externalizing problems and inhibition at age 3 years: differential susceptibility to rearing experience? Dev Psychopathol. 1998; 10, 301319.
75. Feldman, R, Greenbaum, CW, Yirmiya, N. Mother-infant affect synchrony as an antecedent of the emergence of self-control. Dev Psychol. 1999; 35, 223231.
76. Kochanska, G. Toward a synthesis of parental socialization and child temperament in early development of conscience. Child Dev. 1993; 64, 325347.
77. Kochanska, G, Aksan, N, Joy, ME. Children’s fearfulness as a moderator of parenting in early socialization: two longitudinal studies. Dev Psychol. 2007; 43, 222237.
78. Pluess, M, Belsky, J. Differential susceptibility to rearing experience: the case of childcare. J Child Psychol Psychiatry. 2009; 50, 396404.
79. van Aken, C, Junger, M, Verhoeven, M, et al. The interactive effects of temperament and maternal parenting on toddlers’ externalizing behaviours. Infant Child Dev. 2007; 16, 553572.


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Associations among prenatal stress, maternal antioxidant intakes in pregnancy, and child temperament at age 30 months

  • L. R. Lipton (a1), K. J. Brunst (a1), S. Kannan (a2) (a3), Y.-M. Ni (a4), H. B. Ganguri (a5), R. J. Wright (a1) (a6) and M. Bosquet Enlow (a7) (a8)...


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