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The Interplay Between Nutrition and Stress in Pregnancy: Implications for Fetal Programming of Brain Development

  • Karen L. Lindsay
    Affiliations
    Department of Pediatrics, University of California, Irvine, Irvine, California

    UC Irvine Development, Health and Disease Research Program, University of California, Irvine, Irvine, California
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  • Claudia Buss
    Affiliations
    Department of Pediatrics, University of California, Irvine, Irvine, California

    UC Irvine Development, Health and Disease Research Program, University of California, Irvine, Irvine, California

    Institute of Medical Psychology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
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  • Pathik D. Wadhwa
    Affiliations
    Department of Pediatrics, University of California, Irvine, Irvine, California

    Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, California

    Department of Obstetrics and Gynecology, University of California, Irvine, Irvine, California

    UC Irvine Development, Health and Disease Research Program, University of California, Irvine, Irvine, California
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  • Sonja Entringer
    Correspondence
    Address correspondence to Sonja Entringer, Ph.D., Department of Medical Psychology, Charité – Universitätsmedizin Berlin, Luisenstrasse 57, Berlin 10117, Germany.
    Affiliations
    Department of Pediatrics, University of California, Irvine, Irvine, California

    UC Irvine Development, Health and Disease Research Program, University of California, Irvine, Irvine, California

    Institute of Medical Psychology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
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      Abstract

      Growing evidence supports an important role for the intrauterine environment in shaping fetal development and subsequent child health and disease risk. The fetal brain is particularly plastic, whereby even subtle changes in structure and function produced by in utero conditions can have long-term implications. Based on the consideration that conditions related to energy substrate and likelihood of survival to reproductive age are particularly salient drivers of fetal programming, maternal nutrition and stress represent the most commonly, but independently, studied factors in this context. However, the effects of maternal nutrition and stress are context dependent and may be moderated by one another. Studies examining the effects of the bidirectional nutrition-stress interplay in pregnancy on fetal programming of brain development are beginning to emerge in the literature. This review incorporates all currently available animal and human studies of this interplay and provides a synthesis and critical discussion of findings. Nine of the 10 studies included here assessed nutrition–stress interactions and offspring neurodevelopmental or brain development outcomes. Despite significant heterogeneity in study design and methodology, two broad patterns of results emerge to suggest that the effects of prenatal stress on various aspects of brain development may be mitigated by 1) higher fat diets or increased intake and/or status of specific dietary fats and 2) higher dietary intake or supplementation of targeted nutrients. The limitations of these studies are discussed, and recommendations are provided for future research to expand on this important area of fetal programming of brain development.

      Keywords

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      References

        • Entringer S.
        • Buss C.
        • Swanson J.M.
        • Cooper D.M.
        • Wing D.A.
        • Waffarn F.
        • et al.
        Fetal programming of body composition, obesity, and metabolic function: The role of intrauterine stress and stress biology.
        J Nutr Metab. 2012; 2012: 632548
        • Wadhwa P.D.
        • Buss C.
        • Entringer S.
        • Swanson J.M.
        Developmental origins of health and disease: Brief history of the approach and current focus on epigenetic mechanisms.
        Semin Reprod Med. 2009; 27: 358-368
        • Gluckman P.D.
        • Hanson M.A.
        Living with the past: Evolution, development, and patterns of disease.
        Science. 2004; 305: 1733-1736
        • Gluckman P.D.
        • Low F.M.
        • Buklijas T.
        • Hanson M.A.
        • Beedle A.S.
        How evolutionary principles improve the understanding of human health and disease.
        Evol Appl. 2011; 4: 249-263
        • Hanson M.
        • Godfrey K.M.
        • Lillycrop K.A.
        • Burdge G.C.
        • Gluckman P.D.
        Developmental plasticity and developmental origins of non-communicable disease: Theoretical considerations and epigenetic mechanisms.
        Prog Biophys Mol Biol. 2011; 106: 272-280
        • Tau G.Z.
        • Peterson B.S.
        Normal development of brain circuits.
        Neuropsychopharmacology. 2010; 35: 147-168
        • Buss C.
        • Entringer S.
        • Moog N.K.
        • Toepfer P.
        • Fair D.A.
        • Simhan H.N.
        • et al.
        Intergenerational transmission of maternal childhood maltreatment exposure: Implications for fetal brain development.
        J Am Acad Child Adolesc Psychiatry. 2017; 56: 373-382
        • Buss C.
        • Entringer S.
        • Wadhwa P.D.
        Fetal programming of brain development: Intrauterine stress and susceptibility to psychopathology.
        Sci Signal. 2012; 5: pt7
        • Bale T.L.
        • Baram T.Z.
        • Brown A.S.
        • Goldstein J.M.
        • Insel T.R.
        • McCarthy M.M.
        • et al.
        Early life programming and neurodevelopmental disorders.
        Biol Psychiatry. 2010; 68: 314-319
        • Buss C.
        • Lord C.
        • Wadiwalla M.
        • Hellhammer D.H.
        • Lupien S.J.
        • Meaney M.J.
        • 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
        • Tully L.A.
        • Arseneault L.
        • Caspi A.
        • Moffitt T.E.
        • Morgan J.
        Does maternal warmth moderate the effects of birth weight on twins’ attention-deficit/hyperactivity disorder (ADHD) symptoms and low IQ?.
        J Consult Clin Psychol. 2004; 72: 218-226
        • Kim D.J.
        • Davis E.P.
        • Sandman C.A.
        • Sporns O.
        • O’Donnell B.F.
        • Buss C.
        • et al.
        Prenatal maternal cortisol has sex-specific associations with child brain network properties.
        Cerebral Cortex. 2017; 27: 5230-5241
        • Mueller B.R.
        • Bale T.L.
        Sex-specific programming of offspring emotionality after stress early in pregnancy.
        J Neurosci. 2008; 28: 9055
        • Lindsay K.L.
        • Buss C.
        • Wadhwa P.D.
        • Entringer S.
        The interplay between maternal nutrition and stress during pregnancy: Issues and considerations.
        Ann Nutr Metab. 2017; 70: 191-200
        • Georgieff M.K.
        Nutrition and the developing brain: Nutrient priorities and measurement.
        Am J Clin Nutr. 2007; 85: 614S-620S
        • Crawford M.A.
        The role of essential fatty acids in neural development: Implications for perinatal nutrition.
        Am J Clin Nutr. 1993; 57: 703S-710S
        • Breton C.
        The hypothalamus-adipose axis is a key target of developmental programming by maternal nutritional manipulation.
        J Endocrinol. 2013; 216: R19-R31
        • Szutorisz H.
        • Hurd Y.L.
        Feeding the developing brain: The persistent epigenetic effects of early life malnutrition.
        Biol Psychiatry. 2016; 80: 730-732
        • de Rooij S.R.
        • Wouters H.
        • Yonker J.E.
        • Painter R.C.
        • Roseboom T.J.
        Prenatal undernutrition and cognitive function in late adulthood.
        Proc Natl Acad Sci U S A. 2010; 107: 16881
        • Rong H.
        • Xi Y.
        • An Y.
        • Tao L.
        • Zhang X.
        • Yu H.
        • et al.
        The correlation between early stages of life exposed to Chinese famine and cognitive decline in adulthood: Nutrition of adulthood plays an important role in the link?.
        Front Aging Neurosci. 2017; 9: 444
        • Czeizel E.A.
        • Dudás I.
        • Vereczkey A.
        • Bánhidy F.
        Folate deficiency and folic acid supplementation: The prevention of neural-tube defects and congenital heart defects.
        Nutrients. 2013; 5: 4760-4775
        • Roth C.
        • Magnus P.
        • Schjølberg S.
        • Stoltenberg C.
        • Surén P.
        • McKeague I.W.
        • et al.
        Folic acid supplements in pregnancy and severe language delay in children.
        JAMA. 2011; 306: 1566-1573
        • Whitehouse A.J.
        • Holt B.J.
        • Serralha M.
        • Holt P.G.
        • Kusel M.M.
        • Hart P.H.
        Maternal serum vitamin D levels during pregnancy and offspring neurocognitive development.
        Pediatrics. 2012; 129: 485-493
        • Ars C.L.
        • Nijs I.M.
        • Marroun H.E.
        • Muetzel R.
        • Schmidt M.
        • Steenweg-de Graaff J.
        • et al.
        Prenatal folate, homocysteine and vitamin B12 levels and child brain volumes, cognitive development and psychological functioning: The Generation R Study.
        Br J Nutr. 2016; ([published online ahead of print Jan 22])
        • Eyles D.W.
        • Burne T.H.J.
        • McGrath J.J.
        Vitamin D, effects on brain development, adult brain function and the links between low levels of vitamin D and neuropsychiatric disease.
        Front Neuroendocrinol. 2013; 34: 47-64
        • Surén P.
        • Roth C.
        • Bresnahan M.
        • Haugen M.
        • Hornig M.
        • Hirtz D.
        • et al.
        Association between maternal use of folic acid supplements and risk of autism spectrum disorders in children.
        JAMA. 2013; 309: 570-577
        • Talge N.M.
        • Neal C.
        • Glover V.
        • Early Stress, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health
        Antenatal maternal stress and long-term effects on child neurodevelopment: How and why?.
        J Child Psychol Psychiatry. 2007; 48: 245-261
        • Kinsella M.T.
        • Monk C.
        Impact of maternal stress, depression and anxiety on fetal neurobehavioral development.
        Clin Obstet Gynecol. 2009; 52: 425-440
        • King S.
        • Dancause K.
        • Turcotte-Tremblay A.-M.
        • Veru F.
        • Laplante D.P.
        Using natural disasters to study the effects of prenatal maternal stress on child health and development.
        Birth Defects Res C Embryo Today. 2012; 96: 273-288
        • Sandman C.A.
        • Buss C.
        • Head K.
        • Davis E.P.
        Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood.
        Biol Psychiatry. 2015; 77: 324-334
        • Buss C.
        • Davis E.P.
        • Muftuler L.T.
        • Head K.
        • Sandman C.A.
        High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9 year-old children.
        Psychoneuroendocrinology. 2010; 35: 141-153
        • Buss C.
        • Davis E.P.
        • Hobel C.J.
        • Sandman C.A.
        Maternal pregnancy-specific anxiety is associated with child executive function at 6–9 years age.
        Stress. 2011; 14: 665-676
        • Sandman C.A.
        • Davis E.P.
        • Buss C.
        • Glynn L.M.
        Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus.
        Neuroendocrinology. 2012; 95: 7-21
        • Van den Bergh B.R.
        • Mulder E.J.
        • Mennes M.
        • Glover V.
        Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: Links and possible mechanisms. A review.
        Neurosci Biobehav Rev. 2005; 29: 237-258
        • O’Donnell K.J.
        • Meaney M.J.
        Fetal origins of mental health: The developmental origins of health and disease hypothesis.
        Am J Psychiatry. 2017; 174: 319-328
        • Buss C.
        • Davis E.P.
        • Shahbaba B.
        • Pruessner J.C.
        • Head K.
        • Sandman C.A.
        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
        • Graham A.M.
        • Rasmussen J.M.
        • Rudolph M.D.
        • Heim C.M.
        • Gilmore J.H.
        • Styner M.
        • et al.
        Maternal systemic interleukin-6 during pregnancy is associated with newborn amygdala phenotypes and subsequent behavior at 2 years of age.
        Biol Psychiatry. 2018; 83: 109-119
        • Adam T.C.
        • Epel E.S.
        Stress, eating and the reward system.
        Physiol Behav. 2007; 91: 449-458
        • Torres S.J.
        • Nowson C.A.
        Relationship between stress, eating behavior, and obesity.
        Nutrition. 2007; 23: 887-894
        • Kiecolt-Glaser J.K.
        Stress, food, and inflammation: Psychoneuroimmunology and nutrition at the cutting edge.
        Psychosom Med. 2010; 72: 365-369
        • Groesz L.M.
        • McCoy S.
        • Carl J.
        • Saslow L.
        • Stewart J.
        • Adler N.
        • et al.
        What is eating you? Stress and the drive to eat.
        Appetite. 2012; 58: 717-721
        • Yin J.
        • Levanon D.
        • Chen J.D.
        Inhibitory effects of stress on postprandial gastric myoelectrical activity and vagal tone in healthy subjects.
        Neurogastroenterol Motil. 2004; 16: 737-744
        • Stoney C.M.
        • West S.G.
        • Hughes J.W.
        • Lentino L.M.
        • Finney M.L.
        • Falko J.
        • et al.
        Acute psychological stress reduces plasma triglyceride clearance.
        Psychophysiology. 2002; 39: 80-85
        • Le Fur C.
        • Romon M.
        • Lebel P.
        • Devos P.
        • Lancry A.
        • Guedon-Moreau L.
        • et al.
        Influence of mental stress and circadian cycle on postprandial lipemia.
        Am J Clin Nutr. 1999; 70: 213-220
        • Teff K.L.
        Visceral nerves: Vagal and sympathetic innervation.
        JPEN J Parenter Enteral Nutr. 2008; 32: 569-571
        • Mikolajczyk R.T.
        • El Ansari W.
        • Maxwell A.E.
        Food consumption frequency and perceived stress and depressive symptoms among students in three European countries.
        Nutr J. 2009; 8: 31
        • Dallman M.F.
        Stress-induced obesity and the emotional nervous system.
        Trends Endocrinol Metab. 2010; 21: 159-165
        • Kiecolt-Glaser J.K.
        • Fagundes C.P.
        • Andridge R.
        • Peng J.
        • Malarkey W.B.
        • Habash D.
        • et al.
        Depression, daily stressors and inflammatory responses to high-fat meals: When stress overrides healthier food choices.
        Mol Psychiatry. 2017; 22: 476-482
        • Entringer S.
        • Buss C.
        • Wadhwa P.D.
        Prenatal stress, development, health and disease risk: A psychobiological perspective—2015 Curt Richter Award Winner.
        Psychoneuroendocrinology. 2015; 62: 366-375
        • Yehuda S.
        Omega-6/omega-3 ratio and brain-related functions.
        World Rev Nutr Diet. 2003; 92: 37-56
        • Alessandri J.M.
        • Guesnet P.
        • Vancassel S.
        • Astorg P.
        • Denis I.
        • Langelier B.
        • et al.
        Polyunsaturated fatty acids in the central nervous system: Evolution of concepts and nutritional implications throughout life.
        Reprod Nutr Dev. 2004; 44: 509-538
        • Cunnane S.C.
        • Francescutti V.
        • Brenna J.T.
        • Crawford M.A.
        Breast-fed infants achieve a higher rate of brain and whole body docosahexaenoate accumulation than formula-fed infants not consuming dietary docosahexaenoate.
        Lipids. 2000; 35: 105-111
        • Spencer S.J.
        • Korosi A.
        • Layé S.
        • Shukitt-Hale B.
        • Barrientos R.M.
        Food for thought: How nutrition impacts cognition and emotion.
        npj Science of Food. 2017; 1: 7
        • Joffre C.
        • Nadjar A.
        • Lebbadi M.
        • Calon F.
        • Laye S.
        n-3 LCPUFA improves cognition: The young, the old and the sick.
        Prostaglandins Leukot Essent Fatty Acids. 2014; 91: 1-20
        • Rao T.S.
        • Asha M.R.
        • Ramesh B.N.
        • Rao K.S.
        Understanding nutrition, depression and mental illnesses.
        Indian J Psychiatry. 2008; 50: 77-82
        • Coe C.L.
        • Lubach G.R.
        • Shirtcliff E.A.
        Maternal stress during pregnancy predisposes for iron deficiency in infant monkeys impacting innate immunity.
        Pediatr Res. 2007; 61: 520
        • Ganz T.
        • Nemeth E.
        Hepcidin and iron homeostasis.
        Biochim Biophys Acta. 2012; 1823: 1434-1443
        • Marques A.H.
        • O’Connor T.G.
        • Roth C.
        • Susser E.
        • Bjørke-Monsen A.-L.
        The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders.
        Front Neurosci. 2013; 7: 120
        • Monk C.
        • Georgieff M.K.
        • Osterholm E.A.
        Research review: Maternal prenatal distress and poor nutrition—mutually influencing risk factors affecting infant neurocognitive development.
        J Child Psychol Psychiatry. 2013; 54: 115-130
        • Hoeijmakers L.
        • Lucassen P.J.
        • Korosi A.
        The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function.
        Front Mol Neurosci. 2014; 7: 103
        • Lucassen P.J.
        • Naninck E.F.
        • van Goudoever J.B.
        • Fitzsimons C.
        • Joels M.
        • Korosi A.
        Perinatal programming of adult hippocampal structure and function: Emerging roles of stress, nutrition and epigenetics.
        Trends Neurosci. 2013; 36: 621-631
        • Baskin R.
        • Hill B.
        • Jacka F.N.
        • O’Neil A.
        • Skouteris H.
        The association between diet quality and mental health during the perinatal period. A systematic review.
        Appetite. 2015; 91: 41-47
        • Yam K.Y.
        • Naninck E.F.
        • Schmidt M.V.
        • Lucassen P.J.
        • Korosi A.
        Early-life adversity programs emotional functions and the neuroendocrine stress system: The contribution of nutrition, metabolic hormones and epigenetic mechanisms.
        Stress. 2015; 18: 328-342
        • Milaneschi Y.
        • Simmons W.K.
        • van Rossum E.F.C.
        • Penninx B.W.
        Depression and obesity: Evidence of shared biological mechanisms.
        Mol Psychiatry. 2018; ([published online ahead of print Feb 16])
        • Borsonelo E.C.
        • Suchecki D.
        • Calil H.M.
        • Galduroz J.C.
        Supplementation with fish oil and coconut fat prevents prenatal stress-induced changes in early postnatal development.
        Int J Dev Neurosci. 2011; 29: 521-527
        • Huang C.F.
        • Du J.X.
        • Deng W.
        • Cheng X.C.
        • Zhang S.Y.
        • Zhao S.J.
        • et al.
        Effect of prenatal exposure to LPS combined with pre- and post-natal high-fat diet on hippocampus in rat offspring.
        Neuroscience. 2015; 286: 364-370
        • Yajima M.
        • Matsumoto M.
        • Harada M.
        • Hara H.
        • Yajima T.
        Effects of constant light during perinatal periods on the behavioral and neuronal development of mice with or without dietary lutein.
        Biomed Res. 2013; 34: 197-204
        • Schulz K.M.
        • Pearson J.N.
        • Gasparrini M.E.
        • Brooks K.F.
        • Drake-Frazier C.
        • Zajkowski M.E.
        • et al.
        Dietary choline supplementation to dams during pregnancy and lactation mitigates the effects of in utero stress exposure on adult anxiety-related behaviors.
        Behav Brain Res. 2014; 268: 104-110
        • Rincel M.
        • Lepinay A.L.
        • Delage P.
        • Fioramonti J.
        • Theodorou V.S.
        • Laye S.
        • et al.
        Maternal high-fat diet prevents developmental programming by early-life stress.
        Transl Psychiatry. 2016; 6: e966
        • Paternain L.
        • de la Garza A.L.
        • Batlle M.A.
        • Milagro F.I.
        • Martinez J.A.
        • Campion J.
        Prenatal stress increases the obesogenic effects of a high-fat-sucrose diet in adult rats in a sex-specific manner.
        Stress. 2013; 16: 220-232
        • Naninck E.F.
        • Oosterink J.E.
        • Yam K.Y.
        • de Vries L.P.
        • Schierbeek H.
        • van Goudoever J.B.
        • et al.
        Early micronutrient supplementation protects against early stress-induced cognitive impairments.
        FASEB J. 2017; 31: 505-518
        • Lipton L.R.
        • Brunst K.J.
        • Kannan S.
        • Ni Y.M.
        • Ganguri H.B.
        • Wright R.J.
        • et al.
        Associations among prenatal stress, maternal antioxidant intakes in pregnancy, and child temperament at age 30 months.
        J Dev Orig Health Dis. 2017; 8: 638-648
        • Brunst K.J.
        • Enlow M.B.
        • Kannan S.
        • Carroll K.N.
        • Coull B.A.
        • Wright R.J.
        Effects of prenatal social stress and maternal dietary fatty acid ratio on infant temperament: Does race matter?.
        Epidemiology (Sunnyvale). 2014; 4
        • Barker E.D.
        • Kirkham N.
        • Ng J.
        • Jensen S.K.
        Prenatal maternal depression symptoms and nutrition, and child cognitive function.
        Br J Psychiatry. 2013; 203: 417-421
        • Clancy B.
        • Finlay B.L.
        • Darlington R.B.
        • Anand K.J.S.
        Extrapolating brain development from experimental species to humans.
        Neurotoxicology. 2007; 28: 931-937
        • Johnson A.R.
        • Zeisel S.H.
        Dietary choline for brain development.
        in: Preedy V.R. Watson R.R. Martin C.R. Handbook of Behavior, Food and Nutrition. Springer New York, New York2011: 2089-2104
        • Zeisel S.H.
        Choline: Critical role during fetal development and dietary requirements in adults.
        Annu Rev Nutr. 2006; 26: 229-250
        • Vishwanathan R.
        • Kuchan M.J.
        • Sen S.
        • Johnson E.J.
        Lutein and preterm infants with decreased concentrations of brain carotenoids.
        J Pediatr Gastroenterol Nutr. 2014; 59: 659-665
        • Johnson E.J.
        Role of lutein and zeaxanthin in visual and cognitive function throughout the lifespan.
        Nutr Rev. 2014; 72: 605-612
        • Sánchez-Hernández D.
        • Anderson G.H.
        • Poon A.N.
        • Pannia E.
        • Cho C.E.
        • Huot P.S.P.
        • et al.
        Maternal fat-soluble vitamins, brain development, and regulation of feeding behavior: An overview of research.
        Nutr Res. 2016; 36: 1045-1054
        • Innis S.M.
        Dietary omega 3 fatty acids and the developing brain.
        Brain Res. 2008; 1237: 35-43
        • Innis S.M.
        Dietary (n-3) fatty acids and brain development.
        J Nutr. 2007; 137: 855-859
        • Lai M.
        • Chandrasekera P.C.
        • Barnard N.D.
        You are what you eat, or are you? The challenges of translating high-fat-fed rodents to human obesity and diabetes.
        Nutr Diabetes. 2014; 4: e135
        • Sullivan E.L.
        • Riper K.M.
        • Lockard R.
        • Valleau J.C.
        Maternal high-fat diet programming of the neuroendocrine system and behavior.
        Horm Behav. 2015; 76: 153-161
        • Sullivan E.L.
        • Nousen L.
        • Chamlou K.
        Maternal high fat diet consumption during the perinatal period programs offspring behavior.
        Physiol Behav. 2014; 123: 236-242
        • Edlow A.G.
        Maternal obesity and neurodevelopmental and psychiatric disorders in offspring.
        Prenat Diagn. 2017; 37: 95-110
        • Sullivan E.L.
        • Grayson B.
        • Takahashi D.
        • Robertson N.
        • Maier A.
        • Bethea C.L.
        • et al.
        Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring.
        J Neurosci. 2010; 30: 3826
        • Watters J.L.
        • Satia J.A.
        • Kupper L.L.
        Correlates of antioxidant nutrients and oxidative DNA damage differ by race in a cross-sectional study of healthy African American and white adults.
        Nutr Res. 2008; 28: 565-576
        • Salihu H.M.
        • Ghaji N.
        • Mbah A.K.
        • Alio A.P.
        • August E.M.
        • Boubakari I.
        Particulate pollutants and racial/ethnic disparity in feto-infant morbidity outcomes.
        Matern Child Health J. 2012; 16: 1679-1687
        • Krolow R.
        • Noschang C.G.
        • Arcego D.
        • Andreazza A.C.
        • Peres W.
        • Gonçalves C.A.
        • et al.
        Consumption of a palatable diet by chronically stressed rats prevents effects on anxiety-like behavior but increases oxidative stress in a sex-specific manner.
        Appetite. 2010; 55: 108-116
        • Nyirenda M.J.
        • Lindsay R.S.
        • Kenyon C.J.
        • Burchell A.
        • Seckl J.R.
        Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring.
        J Clin Invest. 1998; 101: 2174-2181
        • Ozanne S.E.
        • Hales C.N.
        Early programming of glucose-insulin metabolism.
        Trends Endocrinol Metab. 2002; 13: 368-373
        • Glenn M.J.
        • Gibson E.M.
        • Kirby E.D.
        • Mellott T.J.
        • Blusztajn J.K.
        • Williams C.L.
        Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats.
        Eur J Neurosci. 2007; 25: 2473-2482
        • Glenn M.J.
        • Kirby E.D.
        • Gibson E.M.
        • Wong-Goodrich S.J.
        • Mellott T.J.
        • Blusztajn J.K.
        • et al.
        Age-related declines in exploratory behavior and markers of hippocampal plasticity are attenuated by prenatal choline supplementation in rats.
        Brain Res. 2008; 1237: 110-123
        • Rajarethnem H.J.
        • Bhat K.M.R.
        • Jc M.
        • Gopalkrishnan S.K.
        • Gopalram R.B.M.
        • Rai K.S.
        Combined supplementation of choline and docosahexaenoic acid during pregnancy enhances neurodevelopment of fetal hippocampus.
        Neurol Res Int. 2017; 2017: 8748706
        • Napoli I.
        • Blusztajn J.K.
        • Mellott T.J.
        Prenatal choline supplementation in rats increases the expression of IGF2 and its receptor IGF2R and enhances IGF2-induced acetylcholine release in hippocampus and frontal cortex.
        Brain Res. 2008; 1237: 124-135
        • Sandstrom N.J.
        • Loy R.
        • Williams C.L.
        Prenatal choline supplementation increases NGF levels in the hippocampus and frontal cortex of young and adult rats.
        Brain Res. 2002; 947: 9-16
        • Santocono M.
        • Zurria M.
        • Berrettini M.
        • Fedeli D.
        • Falcioni G.
        Lutein, zeaxanthin and astaxanthin protect against DNA damage in SK-N-SH human neuroblastoma cells induced by reactive nitrogen species.
        J Photochem Photobiol B. 2007; 88: 1-10
        • Ohta H.
        • Mitchell A.C.
        • McMahon D.G.
        Constant light disrupts the developing mouse biological clock.
        Pediatr Res. 2006; 60: 304
        • Sandu C.
        • Hicks D.
        • Felder-Schmittbuhl M.-P.
        Rat photoreceptor circadian oscillator strongly relies on lighting conditions.
        Eur J Neurosci. 2011; 34: 507-516
        • Pardini L.
        • Kaeffer B.
        Feeding and circadian clocks.
        Reprod Nutr Dev. 2006; 46: 463-480
        • Kelvin E.A.
        • Edwards S.
        • Jedrychowski W.
        • Schleicher R.L.
        • Camann D.
        • Tang D.
        • 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: 2262-2268
        • Gallo C.
        • Renzi P.
        • Loizzo S.
        • Loizzo A.
        • Piacente S.
        • Festa M.
        • et al.
        Potential therapeutic effects of vitamin E and C on placental oxidative stress induced by nicotine: An in vitro evidence.
        Open Biochem J. 2010; 4: 77-82
        • Ledig M.
        • Holownia A.
        • Copin J.C.
        • Tholey G.
        • Anokhina I.
        Development of glial cells cultured from prenatally alcohol treated rat brain: Effect of supplementation of the maternal alcohol diet with a grape extract.
        Neurochem Res. 1996; 21: 313-317
        • Martin C.K.
        • Nicklas T.
        • Gunturk B.
        • Correa J.B.
        • Allen H.R.
        • Champagne C.
        Measuring food intake with digital photography.
        J Hum Nutr Diet. 2014; 27: 72-81
        • Kirkpatrick S.I.
        • Subar A.F.
        • Douglass D.
        • Zimmerman T.P.
        • Thompson F.E.
        • Kahle L.L.
        • et al.
        Performance of the automated self-administered 24-hour recall relative to a measure of true intakes and to an interviewer-administered 24-h recall.
        Am J Clin Nutr. 2014; 100: 233-240