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Review article: Biomedical intelligence

Vol. 142 No. 0102 (2012)

A review of epidemiological studies on neuropsychological effects of air pollution

  • M Guxens
  • J Sunyer
DOI
https://doi.org/10.57187/smw.2012.13322
Cite this as:
Swiss Med Wkly. 2012;142:w13322
Published
01.01.2012

Abstract

The aim of the present review is to provide an update of the epidemiological evidence of the effects of air pollution on neuropsychological development and impairment, as well as of the evidence on individual susceptibility to these effects. Animal studies have shown deposition of ultrafine particles containing metals in olfactory bulb and frontal cortical and subcortical areas, and overexpression of inflammatory responses, white matter lesions and vascular pathology in these areas that could be the basis for functional and structural brain effects. Several observational studies in the general population have observed cognitive deficits and behavioural impairment in children and the elderly. These effects, however, are not conclusive given the limited number of studies, their small size and their methodological constraints.

References

  1. Beddington J, Cooper CL, Field J, Goswami U, Huppert FA, Jenkins R, et al. The mental wealth of nations. Nature. 2008;455(7216):1057–60. DOI: https://doi.org/10.1038/4551057a
  2. Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108:Suppl3:511–33. DOI: https://doi.org/10.1289/ehp.00108s3511
  3. Landrigan PJ, Sonawane B, Butler RN, Trasande L, Callan R, Droller D. Early environmental origins of neurodegenerative disease in later life. Environ Health Perspect. 2005;113(9):1230–3. DOI: https://doi.org/10.1289/ehp.7571
  4. Brook RD, Rajagopalan S, Pope CA, III, Brook JR, Bhatnagar A, Diez-Roux AV, et al. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation. 2010;121(21):2331–78. DOI: https://doi.org/10.1161/CIR.0b013e3181dbece1
  5. Götschi T, Heinrich J, Sunyer J, Kunzli N. Long-term effects of ambient air pollution on lung function: a review. Epidemiology. 2008;19(5):690–701. DOI: https://doi.org/10.1097/EDE.0b013e318181650f
  6. Perez L, Rapp R, Künzli N. The Year of the Lung: outdoor air pollution and lung health. Swiss Med Wkly. 2010;140:w13129 DOI: https://doi.org/10.4414/smw.2010.13129
  7. Künzli N, Perez L. Evidence based public health – the example of air pollution. Swiss Med Wkly. 2009;139(17-18):242–50.
  8. Block ML, Calderón-Garcidueñas L. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci. 2009;32(9):506–16. DOI: https://doi.org/10.1016/j.tins.2009.05.009
  9. Araujo JA, Nel AE. Particulate matter and atherosclerosis: role of particle size, composition and oxidative stress. Part Fibre Toxicol. 2009;6:24. DOI: https://doi.org/10.1186/1743-8977-6-24
  10. Morawska L, Ristovski Z, Jayaratne ER, Keogh DU, Ling X. Ambient nano and ultrafine particles from motor vehicle emissions: characteristics, ambient processing and implications on human exposure. Atmos Environ. 2008;42(35):8113–38. DOI: https://doi.org/10.1016/j.atmosenv.2008.07.050
  11. Wichmann HE, Spix C, Tuch T, Wölke G, Peters A, Heinrich J, et al. Daily mortality and fine and ultrafine particles in Erfurt, Germany. Part I: Role of particle number and particle mass. Health Effects Institute – Research report. 2000;98.
  12. Mejìa JF, Wraith D, Mengersen K, Morawska L. Trends in size classified particle number concentration in subtropical Brisbane, Australia, based on a 5 year study. Atmos Environ. 2007;41:1064–79. DOI: https://doi.org/10.1016/j.atmosenv.2006.09.020
  13. Pey J, Querol X, Alastuey A, Rodríguez S, Putaud JP, Van Dingenen R. Source apportionment of urban fine and ultra-fine particle number concentration in a Western Mediterranean city. Atmos Environ. 2009;43(29):4407–15. DOI: https://doi.org/10.1016/j.atmosenv.2009.05.024
  14. Nemmar A, Vanbilloen H, Hoylaerts MF, Hoet PH, Verbruggen A, Nemery B. Passage of intratracheally instilled ultrafine particles from the lung into the systemic circulation in hamster. Am J Respir Crit Care Med. 2001;164(9):1665–8. DOI: https://doi.org/10.1164/ajrccm.164.9.2101036
  15. Donaldson K, Tran L, Jimenez LA, Duffin R, Newby DE, Mills N, et al. Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol. 2005;2:10. DOI: https://doi.org/10.1186/1743-8977-2-10
  16. Elder A, Gelein R, Silva V, Feikert T, Opanashuk L, Carter J, et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect. 2006;114(8):1172–8. DOI: https://doi.org/10.1289/ehp.9030
  17. Peters A, Veronesi B, Calderón-Garcidueñas L, Gehr P, Chen LC, Geiser M, et al. Translocation and potential neurological effects of fine and ultrafine particles a critical update. Part Fibre Toxicol. 2006;3:13. DOI: https://doi.org/10.1186/1743-8977-3-13
  18. Tin-Tin-Win-Shwe, Yamamoto S, Ahmed S, Kakeyama M, Kobayashi T, Fujimaki H. Brain cytokine and chemokine mRNA expression in mice induced by intranasal instillation with ultrafine carbon black. Toxicol Lett. 2006;163(2):153–60. DOI: https://doi.org/10.1016/j.toxlet.2005.10.006
  19. Calderón-Garcidueñas L, Mora-Tiscareno A, Gomez-Garza G, Carrasco-Portugal MC, Perez-Guille B, Flores-Murrieta FJ, et al. Effects of a cyclooxygenase-2 preferential inhibitor in young healthy dogs exposed to air pollution: a pilot study. Toxicol Pathol. 2009;37(5):644–60. DOI: https://doi.org/10.1177/0192623309340277
  20. Campbell A, Araujo JA, Li H, Sioutas C, Kleinman M. Particulate matter induced enhancement of inflammatory markers in the brains of apolipoprotein E knockout mice. J Nanosci Nanotechnol. 2009;9(8):5099–104. DOI: https://doi.org/10.1166/jnn.2009.GR07
  21. Gerlofs-Nijland ME, van Berlo D, Cassee FR, Schins RP, Wang K, Campbell A. Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain. Part Fibre Toxicol. 2010;7:12. DOI: https://doi.org/10.1186/1743-8977-7-12
  22. Levesque S, Taetzsch T, Lull ME, Kodavanti U, Stadler K, Wagner A, et al. Diesel Exhaust Activates & Primes Microglia: Air Pollution, Neuroinflammation, & Regulation of Dopaminergic Neurotoxicity. 2011;119(8):1149–55. DOI: https://doi.org/10.1289/ehp.1002986
  23. van Berlo D, Albrecht C, Knaapen AM, Cassee FR, Gerlofs-Nijland ME, Kooter IM, et al. Comparative evaluation of the effects of short-term inhalation exposure to diesel engine exhaust on rat lung and brain. Arch Toxicol. 2010;84(7):553–62. DOI: https://doi.org/10.1007/s00204-010-0551-7
  24. Calderón-Garcidueñas L, Azzarelli B, Acuna H, Garcia R, Gambling TM, Osnaya N, et al. Air pollution and brain damage. Toxicol Pathol. 2002;30(3):373–89. DOI: https://doi.org/10.1080/01926230252929954
  25. Calderón-Garcidueñas L, Reed W, Maronpot RR, Henriquez-Roldan C, Delgado-Chavez R, Calderón-Garcidueñas A, et al. Brain inflammation and Alzheimer’s-like pathology in individuals exposed to severe air pollution. Toxicol Pathol. 2004;32(6):650–8. DOI: https://doi.org/10.1080/01926230490520232
  26. Calderón-Garcidueñas L, Solt AC, Henriquez-Roldan C, Torres-Jardon R, Nuse B, Herritt L, et al. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid beta-42 and alpha-synuclein in children and young adults. Toxicol Pathol. 2008;36(2):289–310. DOI: https://doi.org/10.1177/0192623307313011
  27. Calderón-Garcidueñas L, Franco-Lira M, Henriquez-Roldan C, Osnaya N, Gonzalez-Maciel A, Reynoso-Robles R, et al. Urban air pollution: influences on olfactory function and pathology in exposed children and young adults. Exp Toxicol Pathol. 2010;62(1):91–102. DOI: https://doi.org/10.1016/j.etp.2009.02.117
  28. 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. Environ Health Perspect. 2010;118(9):1326–31. DOI: https://doi.org/10.1289/ehp.0901070
  29. Freire C, Ramos R, Puertas R, Lopez-Espinosa MJ, Julvez J, Aguilera I et al. Association of traffic-related air pollution with cognitive development in children. J Epidemiol Community Health. 2010;64(3):223–8. DOI: https://doi.org/10.1136/jech.2008.084574
  30. Perera F, Li TY, Zhou ZJ, Yuan T, Chen YH, Qu L, et al. Benefits of reducing prenatal exposure to coal-burning pollutants to children’s neurodevelopment in China. Environ Health Perspect. 2008;116(10):1396–400. DOI: https://doi.org/10.1289/ehp.11480
  31. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, Diaz D, et al. Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect. 2006;114(8):1287–92. DOI: https://doi.org/10.1289/ehp.9084
  32. Perera FP, 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–e202. DOI: https://doi.org/10.1542/peds.2008-3506
  33. Siddique S, Banerjee M, Ray MR, Lahiri T. Attention-deficit hyperactivity disorder in children chronically exposed to high level of vehicular pollution. Eur J Pediatr. 2011;170(7):923–9. DOI: https://doi.org/10.1007/s00431-010-1379-0
  34. Suglia SF, Gryparis A, Wright RO, Schwartz J, Wright RJ. Association of black carbon with cognition among children in a prospective birth cohort study. Am J Epidemiol. 2007;167(3):280–6. DOI: https://doi.org/10.1093/aje/kwm308
  35. Tang D, Li TY, Liu JJ, Zhou ZJ, Yuan T, Chen YH, et al. Effects of prenatal exposure to coal-burning pollutants on children’s development in China. Environ Health Perspect. 2008;116(5):674–9. DOI: https://doi.org/10.1289/ehp.10471
  36. 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. Environ Health Perspect. 2009;117(10):1612–8. DOI: https://doi.org/10.1289/ehp.0800023
  37. Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R. Residential Proximity to Freeways and Autism in the CHARGE Study. Environ Health Perspect. 2010;119(6):873–7. DOI: https://doi.org/10.1289/ehp.1002835
  38. Guxens M, Aguilera I, Ballester F, Estarlich M, Fernández-Somoano A, Lertxundi A, et al. Prenatal exposure to residential air pollution and infant mental development: modulation by antioxidants and detoxification factors. Environ Health Prespect. 2012;120(1):1–7. DOI: https://doi.org/10.1289/ehp.1103469
  39. Pastor M Jr, Morello-Frosch R, Sadd JL. Breathless: schools, air toxics, and environmental justice in California. Policy Studies Journal. 2006;34(3):337–62. DOI: https://doi.org/10.1111/j.1541-0072.2006.00176.x
  40. Mohai P, Kweon BS, Lee S, Ard K. Air pollution around schools is linked to poorer student health and academic performance. Health Aff (Millwood). 2011;30(5):852–62. DOI: https://doi.org/10.1377/hlthaff.2011.0077
  41. Kalkbrenner AE, Daniels JL, Chen JC, Poole C, Emch M, Morrissey J. Perinatal exposure to hazardous air pollutants and autism spectrum disorders at age 8. Epidemiology. 2010;21(5):631–41. DOI: https://doi.org/10.1097/EDE.0b013e3181e65d76
  42. Windham GC, Zhang L, Gunier R, Croen LA, Grether JK. Autism spectrum disorders in relation to distribution of hazardous air pollutants in the san francisco bay area. Environ Health Perspect. 2006;114(9):1438–44. DOI: https://doi.org/10.1289/ehp.9120
  43. Morales E, Julvez J, Torrent M, de Cid R, Guxens M, Bustamante M, et al. Association of early-life exposure to household gas appliances and indoor nitrogen dioxide with cognition and attention behavior in preschoolers. Am J Epidemiol. 2009;169(11):1327–36. DOI: https://doi.org/10.1093/aje/kwp067
  44. Vrijheid M, Martinez D, Aguilera I, Bustamante M, Ballester F, Estarlich M et al. Indoor air pollution from gas cooking and neurodevelopment in Infants. Epidemiology. 2012;23(1):23–32. DOI: https://doi.org/10.1097/EDE.0b013e31823a4023
  45. Yolton K, Dietrich K, Auinger P, Lanphear BP, Hornung R. Exposure to environmental tobacco smoke and cognitive abilities among U.S. children and adolescents. Environ Health Perspect. 2004;113(1):98–103. DOI: https://doi.org/10.1289/ehp.7210
  46. Bandiera FC, Richardson AK, Lee DJ, He JP, Merikangas KR. Secondhand smoke exposure and mental health among children and adolescents. Arch Pediatr Adolesc Med. 2011;165(4):332–8. DOI: https://doi.org/10.1001/archpediatrics.2011.30
  47. Llewellyn DJ, Lang IA, Langa KM, Naughton F, Matthews FE. Exposure to secondhand smoke and cognitive impairment in non-smokers: national cross sectional study with cotinine measurement. BMJ. 2009;338:b462. DOI: https://doi.org/10.1136/bmj.b462
  48. Ranft U, Schikowski T, Sugiri D, Krutmann J, Kramer U. Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environ Res. 2009;109(8):1004–11. DOI: https://doi.org/10.1016/j.envres.2009.08.003
  49. Power MC, Weisskopf MG, Alexeeff SE, Coull BA, Spiro A, III, Schwartz J. Traffic-related air pollution and cognitive function in a cohort of older men. Environ Health Perspect. 2010;119(5):682–7. DOI: https://doi.org/10.1289/ehp.1002767
  50. Crüts B, van Etten L, Tornqvist H, Blomberg A, Sandstrom T, Mills NL et al. Exposure to diesel exhaust induces changes in EEG in human volunteers. Part Fibre Toxicol. 2008;5:4. DOI: https://doi.org/10.1186/1743-8977-5-4
  51. Chen JC, Schwartz J. Neurobehavioral effects of ambient air pollution on cognitive performance in US adults. Neurotoxicology. 2009;30(2):231–9. DOI: https://doi.org/10.1016/j.neuro.2008.12.011
  52. Neale BM, Lasky-Su J, Anney R, Franke B, Zhou K, Maller JB, et al. Genome-wide association scan of attention deficit hyperactivity disorder. Am J Med Genet B Neuropsychiatr Genet. 2008;147B(8):1337–44. DOI: https://doi.org/10.1002/ajmg.b.30866
  53. Need AC, Attix DK, McEvoy JM, Cirulli ET, Linney KL, Hunt P, et al. A genome-wide study of common SNPs and CNVs in cognitive performance in the CANTAB. Hum Mol Genet. 2009;18(23):4650–61. DOI: https://doi.org/10.1093/hmg/ddp413
  54. Raijmakers MT, Steegers EA, Peters WH. Glutathione S-transferases and thiol concentrations in embryonic and early fetal tissues. Hum Reprod. 2001;16(11):2445–50. DOI: https://doi.org/10.1093/humrep/16.11.2445
  55. Wang S, Chanock S, Tang D, Li Z, Edwards S, Jedrychowski W, et al. Effect of gene-environment Interactions on mental development in African American, Dominican, and Caucasian mothers and newborns. Ann Hum Genet. 2010;74(1):46–56. DOI: https://doi.org/10.1111/j.1469-1809.2009.00550.x
  56. Abnet CC, Fagundes RB, Strickland PT, Kamangar F, Roth MJ, Taylor PR, et al. The influence of genetic polymorphisms in Ahr, CYP1A1, CYP1A2, CYP1B1, GST M1, GST T1 and UGT1A1 on urine 1-hydroxypyrene glucuronide concentrations in healthy subjects from Rio Grande do Sul, Brazil. Carcinogenesis. 2007;28(1):112–7. DOI: https://doi.org/10.1093/carcin/bgl131
  57. Gilliland FD, Li YF, Saxon A, Diaz-Sanchez D. Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: randomised, placebo-controlled crossover study. Lancet. 2004;363(9403):119–25. DOI: https://doi.org/10.1016/S0140-6736(03)15262-2
  58. Romieu I, Castro-Giner F, Kunzli N, Sunyer J. Air pollution, oxidative stress and dietary supplementation: a review. Eur Respir J. 2008;31(1):179–97. DOI: https://doi.org/10.1183/09031936.00128106
  59. Villarreal-Calderon R, Torres-Jardon R, Palacios-Moreno J, Osnaya N, Perez-Guille B, Maronpot RR, et al. Urban air pollution targets the dorsal vagal complex and dark chocolate offers neuroprotection. Int J Toxicol. 2010;29(6):604–15. DOI: https://doi.org/10.1177/1091581810383587
  60. Jedrychowski W, Perera F, Mrozek-Budzyn D, Flak E, Mroz E, Sochacka-Tatara E et al. Higher fish consumption in pregnancy may confer protection against the harmful effect of prenatal exposure to fine particulate matter. Ann Nutr Metab. 2010;56(2):119–26. DOI: https://doi.org/10.1159/000275918
  61. Jedrychowski W, Flak E, Mroz E, Pac A, Jacek R, Sochacka-Tatara E, et al. Modulating effects of maternal fish consumption on the occurrence of respiratory symptoms in early infancy attributed to prenatal exposure to fine particles. Ann Nutr Metab. 2008;52(1):8–16. DOI: https://doi.org/10.1159/000114289
  62. Kelvin EA, Edwards S, Jedrychowski W, Schleicher RL, 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(8):2262–8. DOI: https://doi.org/10.1158/1055-9965.EPI-09-0316
  63. Fujii T, Hayashi S, Hogg JC, Vincent R, Van Eeden SF. Particulate matter induces cytokine expression in human bronchial epithelial cells. Am J Respir Cell Mol Biol. 2001;25(3):265–71. DOI: https://doi.org/10.1165/ajrcmb.25.3.4445
  64. Jiménez LA, Drost EM, Gilmour PS, Rahman I, Antonicelli F, Ritchie H, et al. PM(10)-exposed macrophages stimulate a proinflammatory response in lung epithelial cells via TNF-alpha. Am J Physiol Lung Cell Mol Physiol. 2002;282(2):L237–L248. DOI: https://doi.org/10.1152/ajplung.00024.2001
  65. van Eeden SF, Tan WC, Suwa T, Mukae H, Terashima T, Fujii T, et al. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). Am J Respir Crit Care Med. 2001;164(5):826–30. DOI: https://doi.org/10.1164/ajrccm.164.5.2010160
  66. Hirano S, Furuyama A, Koike E, Kobayashi T. Oxidative-stress potency of organic extracts of diesel exhaust and urban fine particles in rat heart microvessel endothelial cells. Toxicology. 2003;187(2-3):161–70. DOI: https://doi.org/10.1016/S0300-483X(03)00053-2
  67. Rückerl R, Greven S, Ljungman P, Aalto P, Antoniades C, Bellander T, et al. Air pollution and inflammation (interleukin-6, C-reactive protein, fibrinogen) in myocardial infarction survivors. Environ Health Perspect. 2007;115(7):1072–80. DOI: https://doi.org/10.1289/ehp.10021
  68. Ljungman P, Bellander T, Schneider A, Breitner S, Forastiere F, Hampel R, et al. Modification of the interleukin-6 response to air pollution by interleukin-6 and fibrinogen polymorphisms. Environ Health Perspect. 2009;117(9):1373–9. DOI: https://doi.org/10.1289/ehp.0800370
  69. Peters A, Greven S, Heid IM, Baldari F, Breitner S, Bellander T, et al. Fibrinogen genes modify the fibrinogen response to ambient particulate matter. Am J Respir Crit Care Med. 2009;179(6):484–91. DOI: https://doi.org/10.1164/rccm.200805-751OC
  70. Steiner M, Boller M, Schulz T, Pronk W. Modelling heavy metal fluxes from traffic into the environment. J Environ Monit. 2007t;9(8):847–54. DOI: https://doi.org/10.1039/b703509h
  71. Lanphear BP, Hornung R, Khoury J, Yolton K, Baghurst P, Bellinger DC, et al. Low-level environmental lead exposure and children’s intellectual function: an international pooled analysis. Environ Health Perspect. 2005;113(7):894–9. DOI: https://doi.org/10.1289/ehp.7688
  72. Grandjean P, Landrigan PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167–78. DOI: https://doi.org/10.1016/S0140-6736(06)69665-7
  73. Froehlich TE, Lanphear BP, Auinger P, Hornung R, Epstein JN, Braun J, et al. Association of tobacco and lead exposures with attention-deficit/hyperactivity disorder. Pediatrics. 2009;124(6):e1054–e1063. DOI: https://doi.org/10.1542/peds.2009-0738