Skip to main content Accessibility help
Hostname: page-component-cf9d5c678-9z9qw Total loading time: 0.288 Render date: 2021-07-31T08:01:28.677Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

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

Published online by Cambridge University Press:  27 June 2017

L. R. Lipton
Department of Pediatrics, Kravis Children’s Hospital, Icahn School of Medicine at Mount Sinai, New York City, NY, USA
K. J. Brunst
Department of Pediatrics, Kravis Children’s Hospital, Icahn School of Medicine at Mount Sinai, New York City, NY, USA
S. Kannan
Department of Human Nutrition and Dietetics, College of Agricultural Sciences, Southern Illinois University, Carbondale, IL, USA Department of Nutrition, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, USA
Y.-M. Ni
Department of Medicine, Cedars-Sinai Medical Center, Los Angeles, CA, USA
H. B. Ganguri
Department of Computer Science, Southern Illinois University, Carbondale, IL, USA
R. J. Wright
Department of Pediatrics, Kravis Children’s Hospital, Icahn School of Medicine at Mount Sinai, New York City, NY, USA Department of Environmental Medicine & Public Health, Icahn School of Medicine at Mount Sinai, New York City, NY, USA
M. Bosquet Enlow
Department of Psychiatry, Boston Children’s Hospital, Boston, MA, USA Department of Psychiatry, Harvard Medical School, Boston, MA, USA


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.

Original Article
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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.)



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


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


1. Gartstein, MA, Rothbart, MK. Studying infant temperament via a revision of the Infant Behavior Questionnaire. Infant Behav Dev. 2003; 7, 517522.Google Scholar
2. Bale, TL, Baram, TZ, Brown, AS, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010; 68, 314319.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
4. Shonkoff, JP, Garner, AS. The lifelong effects of early childhood adversity and toxic stress. Pediatrics. 2012; 129, e232e246.CrossRefGoogle ScholarPubMed
5. Charil, A, Laplante, DP, Vaillancourt, C, et al. Prenatal stress and brain development. Brain Res Rev. 2010; 65, 5679.CrossRefGoogle ScholarPubMed
6. Weiss, B, Bellinger, DC. Social ecology of children’s vulnerability to environmental pollutants. Environ Health Perspect. 2006; 114, 14791485.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
21. Sivonova, M, Zitnanova, I, Hlincikova, L, et al. Oxidative stress in university students during examinations. Stress. 2004; 7, 183188.CrossRefGoogle ScholarPubMed
22. Davis, JM, Auten, RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med. 2010; 15, 191195.CrossRefGoogle ScholarPubMed
23. Myllynen, P, Pasanen, M, Vahakangas, K. The fate and effects of xenobiotics in human placenta. Expert Opin Drug Metab Toxicol. 2007; 3, 331346.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
25. McKinney, BC, Oh, H, Sibille, E. Age-by-disease biological interactions: implications for late-life depression. Front Genet. 2012; 3, 237.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
32. Stringhini, S, Sabia, S, Shipley, M, et al. Association of socioeconomic position with health behaviors and mortality. JAMA. 2010; 303, 11591166.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
34. Hurley, KM, Caulfield, LE, Sacco, LM, et al. Psychosocial influences in dietary patterns during pregnancy. J Am Diet Assoc. 2005; 105, 963966.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
39. Georgieff, MK. Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr. 2007; 85, 614S620S.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
45. Bosquet Enlow, M, Devick, KL, Brunst, KJ, et al. Maternal lifetime trauma exposure, prenatal cortisol, and infant negative affectivity. Infancy. (In press).Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
49. Myers, HF. Ethnicity- and socio-economic status-related stresses in context: an integrative review and conceptual model. J Behav Med. 2009; 32, 919.CrossRefGoogle ScholarPubMed
50. DiPietro, JA. Maternal stress in pregnancy: considerations for fetal development. J Adolesc Health. 2012; 51, S3S8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
55. Block, G. Invited commentary: another perspective on food frequency questionnaires. Am J Epidemiol. 2001; 154, 11031104, discussion 1105–1106.CrossRefGoogle ScholarPubMed
56. Department of Agriculture. USDA National Nutrient Database for Standard Reference. 1998. Nutrient Data Laboratory: Beltsville, MD.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
61. Putnam, SP, Rothbart, MK. Development of short and very short forms of the children’s behavior questionnaire. J Pers Assess. 2006; 87, 103113.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
67. Parisi, F, Laoreti, A, Cetin, I. Multiple micronutrient needs in pregnancy in industrialized countries. Ann Nutr Metab. 2014; 65, 1321.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
70. Blair, MM, Glynn, LM, Sandman, CA, et al. Prenatal maternal anxiety and early childhood temperament. Stress. 2011; 14, 644651.CrossRefGoogle ScholarPubMed
71. Davis, EP. Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy. 2004; 6, 319331.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
73. Belsky, J, Pluess, M. Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull. 2009; 135, 885908.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
76. Kochanska, G. Toward a synthesis of parental socialization and child temperament in early development of conscience. Child Dev. 1993; 64, 325347.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
78. Pluess, M, Belsky, J. Differential susceptibility to rearing experience: the case of childcare. J Child Psychol Psychiatry. 2009; 50, 396404.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *