Associations between prenatal exposure to black carbon and memory domains in urban children: Modification by sex and prenatal stress

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Cowell, Whitney J ^a   Bellinger, David C ^b,c   Coull, Brent A ^c   Gennings, Chris ^d   Wright, Robert O ^d   Wright, Rosalind J ^d  

^a Department of Medicine   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLACK CARBON; SOOT;

ADULT; AFRICAN AMERICAN; ARTICLE; ATTENTION CONCENTRATION INDEX; CHILD; COGNITION ASSESSMENT; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; CRISIS IN FAMILY SYSTEMS REVISED; EDUCATIONAL STATUS; FEMALE; GENERAL MEMORY INDEX; HISPANIC; HUMAN; LEARNING; MALE; MEMORY; MINORITY GROUP; PREGNANT WOMAN; PRENATAL EXPOSURE; PRENATAL STRESS; PROSPECTIVE STUDY; SCHOOL CHILD; SEX; STRESS ASSESSMENT; UNITED STATES; URBAN AREA; WIDE RANGE ASSESSMENT OF MEMORY AND LEARNING SECOND EDITION; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; LEARNING DISORDERS; MASSACHUSETTS; MEMORY DISORDERS; MENTAL STRESS; PHYSIOLOGICAL STRESS; PREGNANCY; PSYCHOLOGY; SEX DIFFERENCE; SOOT; URBAN POPULATION; YOUNG ADULT;

ADULT; BOSTON; CHILD; COHORT STUDIES; FEMALE; HUMANS; LEARNING; LEARNING DISORDERS; MALE; MEMORY; MEMORY DISORDERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSPECTIVE STUDIES; SEX FACTORS; SOOT; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; URBAN POPULATION; YOUNG ADULT;

EID: 84952649139     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142492     Document Type: Article

References (75)

1. Grahame TJ, Klemm R, Schlesinger RB. Public health and components of particulate matter: the changing assessment of black carbon. Journal of the Air & Waste Management Association. 2014; 64 (6):620-60.
2. Block ML, Elder A, Auten RL, Bilbo SD, Chen H, Chen JC, et al. The outdoor air pollution and brain health workshop. Neurotoxicology. 2012; 33(5):972-84. doi: 10.1016/j.neuro.2012.08.014 PMID: 22981845
3. Chiu YH, Bellinger DC, Coull BA, Anderson S, Barber R, Wright RO, et al. Associations between trafficrelated black carbon exposure and attention in a prospective birth cohort of urban children. Environmental health perspectives. 2013; 121(7):859-64. doi: 10.1289/ehp.1205940 PMID: 23665743
4. Newman NC, Ryan P, Lemasters G, Levin L, Bernstein D, Hershey GK, et al. Traffic-related air pollution exposure in the first year of life and behavioral scores at 7 years of age. Environmental health perspectives. 2013; 121(6):731-6. doi: 10.1289/ehp.1205555 PMID: 23694812
5. Perera F, Li Z, Whyatt R, Hoepner L, Wang S, Camann D, et al. Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics. 2009; 124(2):e195-202. doi: 10.1542/ peds.2008-3506 PMID: 19620194
6. Perera F, Tang D, Wang S, Vishnevetsky J, Zhang B, Diaz D, et al. Prenatal polycyclic aromatic hydrocarbon (PAH) exposure and child behavior at age 6-7 years. Environmental health perspectives. 2012; 120(6):921-6. doi: 10.1289/ehp.1104315 PMID: 22440811
7. Suglia SF, Gryparis A, Wright RO, Schwartz J, Wright RJ. Association of black carbon with cognition among children in a prospective birth cohort study. American journal of epidemiology. 2008; 167 (3):280-6. PMID: 18006900
8. Wang S, Zhang J, Zeng X, Zeng Y, Wang S, Chen S. Association of traffic-related air pollution with children's neurobehavioral functions in Quanzhou, China. Environmental health perspectives. 2009; 117 (10):1612-8. doi: 10.1289/ehp.0800023 PMID: 20019914
9. Hougaard KS, Hansen AM. Enhancement of developmental toxicity effects of chemicals by gestational stress. A review. Neurotoxicology and teratology. 2007; 29(4):425-45. PMID: 17433620
10. Wright RJ. Moving towards making social toxins mainstream in children's environmental health. Current opinion in pediatrics. 2009; 21(2):222-9. doi: 10.1097/MOP.0b013e3283292629 PMID: 19300262
11. Erickson AC, Arbour L. The shared pathoetiological effects of particulate air pollution and the social environment on fetal-placental development. Journal of environmental and public health. 2014; 2014:20.
12. Allen JL, Liu X, Pelkowski S, Palmer B, Conrad K, Oberdorster G, et al. Early postnatal exposure to ultrafine particulate matter air pollution: persistent ventriculomegaly, neurochemical disruption, and glial activation preferentially in male mice. Environmental health perspectives. 2014; 122(9):939-45. doi: 10.1289/ehp.1307984 PMID: 24901756
13. Llop S, Lopez-Espinosa MJ, Rebagliato M, Ballester F. Gender differences in the neurotoxicity of metals in children. Toxicology. 2013; 311(1-2):3-12. doi: 10.1016/j.tox.2013.04.015 PMID: 23632092
14. Luine V. Sex differences in chronic stress effects on memory in rats. Stress. 2002; 5(3):205-16. PMID: 12186683
15. Mueller BR, Bale TL. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiology & behavior. 2007; 91(1):55-65.
16. Sagiv SK, Thurston SW, Bellinger DC, Amarasiriwardena C, Korrick SA. Prenatal exposure to mercury and fish consumption during pregnancy and attention-deficit/hyperactivity disorder-related behavior in children. Archives of pediatrics & adolescent medicine. 2012; 166(12):1123-31.
17. Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature. 2014; 509 (7500):282-3. PMID: 24834516
18. Cory-Slechta DA, Virgolini MB, Rossi-George A, Thiruchelvam M, Lisek R, Weston D. Lifetime consequences of combined maternal lead and stress. Basic Clin Pharmacol Toxicol. 2008; 102(2):218-27. doi: 10.1111/j.1742-7843.2007.00189.x PMID: 18226077
19. Weston HI, Weston DD, Allen JL, Cory-Slechta DA. Sex-dependent impacts of low-level lead exposure and prenatal stress on impulsive choice behavior and associated biochemical and neurochemical manifestations. Neurotoxicology. 2014; 44:169-83. doi: 10.1016/j.neuro.2014.06.013 PMID: 25010656
20. Bolton JL, Huff NC, Smith SH, Mason SN, Foster WM, Auten RL, et al. Maternal stress and effects of prenatal air pollution on offspring mental health outcomes in mice. Environmental health perspectives. 2013; 121(9):1075-82. doi: 10.1289/ehp.1306560 PMID: 23823752
21. Ema M, Naya M, Horimoto M, Kato H. Developmental toxicity of diesel exhaust: a review of studies in experimental animals. Reproductive toxicology. 2013; 42:1-17. doi: 10.1016/j.reprotox.2013.06.074 PMID: 23831197
22. Wright RJ, Suglia SF, Levy J, Fortun K, Shields A, Subramanian S, et al. Transdisciplinary research strategies for understanding socially patterned disease: the Asthma Coalition on Community, Environment, and Social Stress (ACCESS) project as a case study. Ciencia & saude coletiva. 2008; 13 (6):1729-42.
23. Chiu Y-HM, Coull BA, Cohen S, Wooley A, Wright RJ. Prenatal and postnatal maternal stress and wheeze in urban children: effect of maternal sensitization. American journal of respiratory and critical care medicine. 2012; 186(2):147-54. doi: 10.1164/rccm.201201-0162OC PMID: 22582161
24. Gryparis A, Coull BA, Schwartz J. Semiparametric latent variable regression models for spatiotemporal modeling of mobile source particles in the greater Boston area. Journal of the Royal Statistical Society: Series C (Applied Statistics). 2007; 56:183-209.
25. Sheslow DV, Adams WV. Wide Range Assessment of Memory and Learning ( 2nd ed.). Wilmington, DE: Wide Range, Inc.; 2003.
26. Berry CA, Quinn KA, Portillo N, Shalowitz MU. Reliability and validity of the Spanish version of the Crisis in Family Systems-Revised. Psychological reports. 2006; 98(1):123-32. PMID: 16673963
27. Shalowitz MU, Berry CA, Rasinski KA, Dannhausen-Brun CA. A new measure of contemporary life stress: development, validation, and reliability of the CRISYS. Health services research. 1998; 33(5 Pt 1):1381-402. PMID: 9865225
28. Myers HF. Ethnicity-and socio-economic status-related stresses in context: an integrative review and conceptual model. Journal of behavioral medicine. 2009; 32(1):9-19. doi: 10.1007/s10865-008-9181-4 PMID: 18989769
29. Oken E, Kleinman KP, Rich-Edwards J, Gillman MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC pediatrics. 2003; 3:6. PMID: 12848901
30. Arcangeli T, Thilaganathan B, Hooper R, Khan KS, Bhide A. Neurodevelopmental delay in small babies at term: a systematic review. Ultrasound in obstetrics & gynecology: the official journal of the International Society of Ultrasound in Obstetrics and Gynecology. 2012; 40(3):267-75.
31. Lakshmanan A, Chiu YH, Coull BA, Just AC, Maxwell SL, Schwartz J, et al. Associations between prenatal traffic-related air pollution exposure and birth weight: Modification by sex and maternal pre-pregnancy body mass index. Environmental research. 2015; 137C:268-77.
32. Pedersen M, Giorgis-Allemand L, Bernard C, Aguilera I, Andersen AM, Ballester F, et al. Ambient air pollution and low birthweight: a European cohort study (ESCAPE). The Lancet Respiratory medicine. 2013; 1(9):695-704. doi: 10.1016/S2213-2600(13)70192-9 PMID: 24429273
33. Genc S, Zadeoglulari Z, Fuss SH, Genc K. The adverse effects of air pollution on the nervous system. Journal of Toxicology. 2012; 2012:782462. doi: 10.1155/2012/782462 PMID: 22523490
34. Zanchi AC, Fagundes LS, Barbosa F Jr, Bernardi R, Rhoden CR, Saldiva PH, et al. Pre and post-natal exposure to ambient level of air pollution impairs memory of rats: the role of oxidative stress. Inhalation toxicology. 2010; 22(11):910-8. doi: 10.3109/08958378.2010.494313 PMID: 20569119
35. Edwards SC, Jedrychowski W, Butscher M, Camann D, Kieltyka A, Mroz E, et al. Prenatal exposure to airborne polycyclic aromatic hydrocarbons and children's intelligence at 5 years of age in a prospective cohort study in Poland. Environmental health perspectives. 2010; 118(9):1326-31. doi: 10.1289/ehp. 0901070 PMID: 20406721
36. Guxens M, Aguilera I, Ballester F, Estarlich M, Fernandez-Somoano A, Lertxundi A, et al. Prenatal exposure to residential air pollution and infant mental development: modulation by antioxidants and detoxification factors. Environmental health perspectives. 2012; 120(1):144-9. doi: 10.1289/ehp. 1103469 PMID: 21868304
37. Guxens M, Garcia-Esteban R, Giorgis-Allemand L, Forns J, Badaloni C, Ballester F, et al. Air pollution during pregnancy and childhood cognitive and psychomotor development: six European birth cohorts. Epidemiology. 2014; 25(5):636-47. doi: 10.1097/EDE.0000000000000133 PMID: 25036432
38. Kim E, Park H, Hong YC, Ha M, Kim Y, Kim BN, et al. Prenatal exposure to PM10 and NO2 and children's neurodevelopment from birth to 24 months of age: mothers and children's environmental health (MOCEH) study. The science of the total environment. 2014; 481:439-45. doi: 10.1016/j.scitotenv. 2014.01.107 PMID: 24631606
39. Perera FP, Tang D, Wang S, Vishnevetsky J, Zhang B, Diaz D, et al. Prenatal polycyclic aromatic hydrocarbon (PAH) exposure and child behavior at age 6-7 years. Environmental health perspectives. 2012; 120(6):921-6. doi: 10.1289/ehp.1104315 PMID: 22440811
40. Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R. Residential proximity to freeways and autism in the CHARGE study. Environmental health perspectives. 2011; 119(6):873-7. doi: 10.1289/ ehp.1002835 PMID: 21156395
41. Schneider ML, Moore CF, Kraemer GW, Roberts AD, DeJesus OT. The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology. 2002; 27(1-2):285-98. PMID: 11750784
42. Gutteling BM, de Weerth C, Zandbelt N, Mulder EJ, Visser GH, Buitelaar JK. Does maternal prenatal stress adversely affect the child's learning and memory at age six? Journal of abnormal child psychology. 2006; 34(6):789-98. PMID: 17063407
43. 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:S10-5. PMID: 17651905
44. Weinstock M. Changes induced by prenatal stress in behavior and brain morphology: can they be prevented or reversed?. In: Antonelli MC, editor. Perinatal Programming of Neurodevelopment, Advances of Neurobiology 10. New York: Springer Science+Business; 2015.
45. Bolton JL, Auten RL, Bilbo SD. Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflammatory outcomes in adult offspring. Brain, behavior, and immunity. 2014; 37:30-44. doi: 10.1016/j.bbi.2013.10.029 PMID: 24184474
46. Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, Auten RL, et al. Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2012; 26(11):4743-54.
47. Levesque S, Surace MJ, McDonald J, Block ML. Air pollution & the brain: Subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease. Journal of neuroinflammation. 2011; 8:105. doi: 10.1186/1742-2094-8-105 PMID: 21864400
48. Tau GZ, Peterson BS. Normal development of brain circuits. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2010; 35(1):147-68.
49. Semmler A, Okulla T, Sastre M, Dumitrescu-Ozimek L, Heneka MT. Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. Journal of chemical neuroanatomy. 2005; 30(2-3):144-57. PMID: 16122904
50. Hauser TU, Iannaccone R, Ball J, Mathys C, Brandeis D, Walitza S, et al. Role of the medial prefrontal cortex in impaired decision making in juvenile attention-deficit/hyperactivity disorder. JAMA psychiatry. 2014; 71(10):1165-73. doi: 10.1001/jamapsychiatry.2014.1093 PMID: 25142296
51. Ramirez-Amaya V, Balderas I, Sandoval J, Escobar ML, Bermudez-Rattoni F. Spatial long-term memory is related to mossy fiber synaptogenesis. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2001; 21(18):7340-8.
52. Shors TJ. Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends in neurosciences. 2004; 27(5):250-6. PMID: 15111006
53. Green HF, Nolan YM. Inflammation and the developing brain: consequences for hippocampal neurogenesis and behavior. Neuroscience and biobehavioral reviews. 2014; 40:20-34. doi: 10.1016/j. neubiorev.2014.01.004 PMID: 24462889
54. Leal G, Afonso PM, Salazar IL, Duarte CB. Regulation of hippocampal synaptic plasticity by BDNF. Brain research. 2014.
55. Khandaker GM, Zimbron J, Lewis G, Jones PB. Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies. Psychological medicine. 2013; 43(2):239-57. doi: 10.1017/S0033291712000736 PMID: 22717193
56. Knuesel I, Chicha L, Britschgi M, Schobel SA, Bodmer M, Hellings JA, et al. Maternal immune activation and abnormal brain development across CNS disorders. Nature reviews Neurology. 2014; 10(11):643-60. doi: 10.1038/nrneurol.2014.187 PMID: 25311587
57. Davis EP, Pfaff D. Sexually dimorphic responses to early adversity: implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology. 2014; 49:11-25. doi: 10.1016/j.psyneuen. 2014.06.014 PMID: 25038479
58. Cordier S, Garel M, Mandereau L, Morcel H, Doineau P, Gosme-Seguret S, et al. Neurodevelopmental investigations among methylmercury-exposed children in French Guiana. Environmental research. 2002; 89(1):1-11. PMID: 12051779
59. Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, et al. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicology and teratology. 1997; 19(6):417-28. PMID: 9392777
60. Engel SM, Miodovnik A, Canfield RL, Zhu C, Silva MJ, Calafat AM, et al. Prenatal phthalate exposure is associated with childhood behavior and executive functioning. Environmental health perspectives. 2010; 118(4):565-71. doi: 10.1289/ehp.0901470 PMID: 20106747
61. Sagiv SK, Thurston SW, Bellinger DC, Altshul LM, Korrick SA. Neuropsychological measures of attention and impulse control among 8-year-old children exposed prenatally to organochlorines. Environmental health perspectives. 2012; 120(6):904-9. doi: 10.1289/ehp.1104372 PMID: 22357172
62. Perera F, Vishnevetsky J, Herbstman JB, Calafat AM, Xiong W, Rauh V, et al. Prenatal bisphenol A exposure and child behavior in an inner-city cohort. Environmental health perspectives. 2012; 120 (8):1190-4. doi: 10.1289/ehp.1104492 PMID: 22543054
63. Horton MK, Kahn LG, Perera F, Barr DB, Rauh V. Does the home environment and the sex of the child modify the adverse effects of prenatal exposure to chlorpyrifos on child working memory? Neurotoxicology and teratology. 2012; 34(5):534-41. doi: 10.1016/j.ntt.2012.07.004 PMID: 22824009
64. Bronson SL, Bale TL. Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment. Endocrinology. 2014; 155(7):2635-46. doi: 10.1210/en.2014-1040 PMID: 24797632
65. Bowman RE. Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. Journal of neuroendocrinology. 2005; 17(8):526-35. PMID: 16011489
66. Bowman RE, Micik R, Gautreaux C, Fernandez L, Luine VN. Sex-dependent changes in anxiety, memory, and monoamines following one week of stress. Physiology & behavior. 2009; 97(1):21-9.
67. Cory-Slechta DA, Virgolini MB, Thiruchelvam M, Weston DD, Bauter MR. Maternal stress modulates the effects of developmental lead exposure. Environmental health perspectives. 2004; 112(6):717-30. PMID: 15121516
68. Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL. Sexual dimorphism of the developing human brain. Progress in neuro-psychopharmacology & biological psychiatry. 1997; 21(8):1185-201.
69. Vahter M, Gochfeld M, Casati B, Thiruchelvam M, Falk-Filippson A, Kavlock R, et al. Implications of gender differences for human health risk assessment and toxicology. Environmental research. 2007; 104(1):70-84. PMID: 17098226
70. Schwarz JM, McCarthy MM. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. Journal of neurochemistry. 2008; 105(5):1561-72. doi: 10.1111/j.1471-4159. 2008.05384.x PMID: 18384643
71. Andreano JM, Cahill L. Sex influences on the neurobiology of learning and memory. Learning & memory. 2009; 16(4):248-66.
72. Sacher J, Neumann J, Okon-Singer H, Gotowiec S, Villringer A. Sexual dimorphism in the human brain: evidence from neuroimaging. Magnetic resonance imaging. 2013; 31(3):366-75. doi: 10.1016/j.mri. 2012.06.007 PMID: 22921939
73. Fougnie D. The relationship between attention and working memory. In: Johansen NB, editor. New Research on Short-Term Memory: Nova Science Publishers, Inc; 2008.
74. Adams W, Reynolds CR. Essentials of WRAML2 and TOMAL-2 Assessment. Kaufman AS, Kaufman NL, editors: John Wiley & Sons, Inc; 2008.
75. Aguiar A, Eubig PA, Schantz SL. Attention deficit/hyperactivity disorder: a focused overview for children's environmental health researchers. Environmental health perspectives. 2010; 118(12):1646-53. doi: 10.1289/ehp.1002326 PMID: 20829148