Air pollution, a rising environmental risk factor for cognition, neuroinflammation and neurodegeneration: The clinical impact on children and beyond

Revue Neurologique

Volumn 172, Issue 1, 2016, Pages 69-80

  Calderon Garciduenas L ^a,b   Leray, E ^c   Heydarpour, P ^d   Torres Jardon R ^e   Reis, J ^f  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSIDAD DEL VALLE DE MÉXICO   (Mexico)

^c EHESP SCHOOL OF PUBLIC HEALTH   (France)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^f HÔPITAL DE HAUTEPIERRE   (France)

Author keywords

Air pollution; Alzheimer's disease; Children's brain development; Multiple sclerosis; Neurodegeneration; Nitrogen oxide gases; Ozone; Parkinson's disease; Particulate matter

Indexed keywords

APOLIPOPROTEIN E4; AUTOANTIBODY; NITROGEN OXIDE; OZONE; POLYCYCLIC AROMATIC HYDROCARBON; TIGHT JUNCTION PROTEIN;

AIR POLLUTION; ALZHEIMER DISEASE; ARTICLE; BRAIN STEM; CHILD HEALTH; COGNITIVE DEFECT; HIGH RISK POPULATION; HUMAN; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OCCUPATIONAL EXPOSURE; PARKINSON DISEASE; PARTICULATE MATTER; POLLUTANT; RISK FACTOR; ADVERSE EFFECTS; CHILD; COGNITION DISORDERS; NEURITIS; NEURODEGENERATIVE DISEASES;

AIR POLLUTION; ALZHEIMER DISEASE; CHILD; COGNITION DISORDERS; HUMANS; MULTIPLE SCLEROSIS; NEURITIS; NEURODEGENERATIVE DISEASES; PARKINSON DISEASE; RISK FACTORS;

EID: 84950300777     PISSN: 00353787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurol.2015.10.008     Document Type: Article

References (117)

1. J. Reis G.C. Roman Environmental neurology: A promising new field of practice and research J Neurol Sci 262 1-2 2007 3 6
2. J.J. Zhang J.M. Samet Chinese haze versus Western smog: Lessons learned J Thorac Dis 7 1 2015 3 13
3. A.D. Kyle C.C. Wright J.C. Caldwell P.A. Buffler T.J. Woodruff Evaluating the health significance of hazardous air pollutants using monitoring data Public Health Rep 116 1 2001 32 44
4. A.V. Bakian R.S. Huber H. Coon D. Gray P. Wilson W.M. McMahon, et al. Acute air pollution exposure and risk of suicide completion Am J Epidemiol 181 5 2015 295 303
5. M. Stafoggia G. Cesaroni A. Peters Z.J. Andersen C. Badaloni R. Beelen, et al. Long-term exposure to ambient air pollution and incidence of cerebrovascular events: Results from 11 European cohorts within the ESCAPE project Environ Health Perspect 122 9 2014 919 925
6. D. Fecht P. Fischer L. Fortunato G. Hoek K. de Hoogh M. Marra, et al. Associations between air pollution and socioeconomic characteristics, ethnicity and age profile of neighbourhoods in England and the Netherlands Environ Pollut 198 2015 201 210
7. S.M. Platt I.E. Haddad S.M. Pieber R.J. Huang A.A. Zardini M. Clairotte, et al. Two-stroke scooters are a dominant source of air pollution in many cities Nat Commun 5 2014 3749
8. L. Suissa M. Fortier S. Lachaud P. Staccini M.H. Mahagne Ozone air pollution and ischaemic stroke occurrence: A case-crossover study in Nice, France BMJ open 3 12 2013 e004060
9. L. Calderon-Garciduenas A. Mora-Tiscareno E. Ontiveros G. Gomez-Garza G. Barragan-Mejia J. Broadway, et al. Air pollution, cognitive deficits and brain abnormalities: A pilot study with children and dogs Brain Cogn 68 2 2008 117 127
10. L. Calderon-Garciduenas A. Mora-Tiscareno M. Styner G. Gomez-Garza H. Zhu R. Torres-Jardon, et al. White matter hyperintensities, systemic inflammation, brain growth, and cognitive functions in children exposed to air pollution J Alzheimers Dis 31 1 2012 183 191
11. L. Calderon-Garciduenas R. Engle A. Mora-Tiscareno M. Styner G. Gomez-Garza H. Zhu, et al. Exposure to severe urban air pollution influences cognitive outcomes, brain volume and systemic inflammation in clinically healthy children Brain Cogn 77 3 2011 345 355
12. K. Yolton K. Dietrich P. Auinger B.P. Lanphear R. Hornung Exposure to environmental tobacco smoke and cognitive abilities among U.S. children and adolescents Environ Health Perspect 113 1 2005 98 103
13. S.F. Suglia A. Gryparis R.O. Wright J. Schwartz R.J. Wright Association of black carbon with cognition among children in a prospective birth cohort study Am J Epidemiol 167 3 2008 280 286
14. E. van Kempen P. Fischer N. Janssen D. Houthuijs I. van Kamp S. Stansfeld, et al. Neurobehavioral effects of exposure to traffic-related air pollution and transportation noise in primary schoolchildren Environ Res 115 2012 18 25
15. L. Dix-Cooper B. Eskenazi C. Romero J. Balmes K.R. Smith Neurodevelopmental performance among school age children in rural Guatemala is associated with prenatal and postnatal exposure to carbon monoxide, a marker for exposure to woodsmoke Neurotoxicology 33 2 2012 246 254
16. E. Kim H. Park Y.C. Hong M. Ha Y. Kim B.N. Kim, et al. Prenatal exposure to PM(1)(0) and NO(2) and children's neurodevelopment from birth to 24 months of age: Mothers and Children's Environmental Health (MOCEH) study Science Total Environ 481 2014 439 445
17. M. Kicinski G. Vermeir N. Van Larebeke E. Den Hond G. Schoeters L. Bruckers, et al. Neurobehavioral performance in adolescents is inversely associated with traffic exposure Environ Int 75 2015 136 143
18. A.D. Murray C.J. McNeil S. Salarirad L.J. Whalley R.T. Staff Early life socioeconomic circumstance and late life brain hyperintensities-a population based cohort study PloS one 9 2 2014 e88969
19. L. Calderon-Garciduenas A. Mora-Tiscareno M. Franco-Lira H. Zhu Z. Lu E. Solorio, et al. Decreases in short term memory, IQ, and altered brain metabolic ratios in urban apolipoprotein epsilon4 children exposed to air pollution J Alzheimers Dis 45 3 2015 757 770
20. D.M. Michaelson APOE epsilon4: The most prevalent yet understudied risk factor for Alzheimer's disease Alzheimers Demen 10 6 2014 861 868
21. L. Calderon-Garciduenas A. Serrano-Sierra R. Torres-Jardon H. Zhu Y. Yuan D. Smith, et al. The impact of environmental metals in young urbanites' brains Exp Toxicol Pathol 65 5 2013 503 511
22. R.G. Lucchini S. Guazzetti S. Zoni F. Donna S. Peter A. Zacco, et al. Tremor, olfactory and motor changes in Italian adolescents exposed to historical ferro-manganese emission Neurotoxicology 33 4 2012 687 696
23. D.J. Curtis A. Sood T.J. Phillips V.H. Leinster A. Nishiguchi C. Coyle, et al. Secretions from placenta, after hypoxia/reoxygenation, can damage developing neurones of brain under experimental conditions Exp Neurol 261 2014 386 395
24. N.R. Saunders S.A. Liddelow K.M. Dziegielewska Barrier mechanisms in the developing brain Front Pharmacol 3 2012 46
25. B.S. Peterson V.A. Rauh R. Bansal X. Hao Z. Toth G. Nati, et al. Effects of prenatal exposure to air pollutants (polycyclic aromatic hydrocarbons) on the development of brain white matter, cognition, and behavior in later childhood JAMA psychiatry 2015
26. D. Yi Y. Yuan L. Jin G. Zhou H. Zhu R.H. Finnell, et al. Levels of PAH-DNA adducts in cord blood and cord tissue and the risk of fetal neural tube defects in a Chinese population Neurotoxicology 46 2015 73 78
27. P.H. Langlois A.T. Hoyt T.A. Desrosiers P.J. Lupo C.C. Lawson M.A. Waters, et al. Maternal occupational exposure to polycyclic aromatic hydrocarbons and small for gestational age offspring Occup Environ Med 71 8 2014 529 535
28. Z. Li C.D. Sandau L.C. Romanoff S.P. Caudill A. Sjodin L.L. Needham, et al. Concentration and profile of 22 urinary polycyclic aromatic hydrocarbon metabolites in the US population Environ Res 107 3 2008 320 331
29. K.H. Jung B. Liu S. Lovinsky-Desir B. Yan D. Camann A. Sjodin, et al. Time trends of polycyclic aromatic hydrocarbon exposure in New York City from 2001 to 2012: Assessed by repeat air and urine samples Environ Res 131 2014 95 103
30. F. Scinicariello M.C. Buser Urinary polycyclic aromatic hydrocarbons and childhood obesity: NHANES (2001-2006) Environ Health Perspect 122 3 2014 299 303
31. L. Calderon-Garciduenas A. Vojdani E. Blaurock-Busch Y. Busch A. Friedle M. Franco-Lira, et al. Air pollution and children: Neural and tight junction antibodies and combustion metals, the role of barrier breakdown and brain immunity in neurodegeneration J Alzheimers Dis 43 3 2015 1039 1058
32. L. Calderon-Garciduenas M. Franco-Lira A. Mora-Tiscareno H. Medina-Cortina R. Torres-Jardon M. Kavanaugh Early Alzheimer's and Parkinson's disease pathology in urban children: Friend versus Foe responses-it is time to face the evidence BioMed Res Int 2013 2013 161687
33. L. Calderon-Garciduenas M. Kavanaugh M. Block A. D'Angiulli R. Delgado-Chavez R. Torres-Jardon, et al. Neuroinflammation, hyperphosphorylated tau, diffuse amyloid plaques, and down-regulation of the cellular prion protein in air pollution exposed children and young adults J Alzheimers Dis 28 1 2012 93 107
34. L. Calderon-Garciduenas M. Franco-Lira C. Henriquez-Roldan N. Osnaya A. Gonzalez-Maciel R. Reynoso-Robles, et al. Urban air pollution: Influences on olfactory function and pathology in exposed children and young adults Exp Toxicol Pathol 62 1 2010 91 102
35. L. Calderon-Garciduenas A.C. Solt C. Henriquez-Roldan R. Torres-Jardon B. Nuse L. Herritt, 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 36 2 2008 289 310
36. G.-M.A. Calderón-Garcidueñas Lilian A. Vojdani M. Franco-Lira R. Reynoso-Robles H. Montesinos-Correa B. Pérez-Guillé, et al. The intestinal barrier in air pollution-associated neural invol vement in mexico city residents: Mind the gut, the evolution of a changing paradigm relevant to parkinson disease risk J Alzheimers Dis Parkinsonism 5 1 2015 1 12
37. A. Lampron A. Elali S. Rivest Innate immunity in the CNS: Redefining the relationship between the CNS and its environment Neuron 78 2 2013 214 232
38. E.S. Wohleb D.B. McKim J.F. Sheridan J.P. Godbout Monocyte trafficking to the brain with stress and inflammation: A novel axis of immune-to-brain communication that influences mood and behavior Front Neurosci 8 2014 447
39. H. Dong X. Zhang Y. Qian Mast cells and neuroinflammation Med Sci Monitor Basic Res 20 2014 200 206
40. W. Huang G. Wang S.E. Lu H. Kipen Y. Wang M. Hu, et al. Inflammatory and oxidative stress responses of healthy young adults to changes in air quality during the Beijing Olympics Am J Respir Crit Care Med 186 11 2012 1150 1159
41. B. Behbod B. Urch M. Speck J.A. Scott L. Liu R. Poon, et al. Endotoxin in concentrated coarse and fine ambient particles induces acute systemic inflammation in controlled human exposures Occup Environ Med 70 11 2013 761 767
42. T. Marchini N.D. Magnani M.L. Paz V. Vanasco D. Tasat D.H. Gonzalez Maglio, et al. Time course of systemic oxidative stress and inflammatory response induced by an acute exposure to residual oil fly ash Toxicol Appl Pharmacol 274 2 2014 274 282
43. S. Wittkopp N. Staimer T. Tjoa D. Gillen N. Daher M. Shafer, et al. Mitochondrial genetic background modifies the relationship between traffic-related air pollution exposure and systemic biomarkers of inflammation PloS one 8 5 2013 e64444
44. K. Huttunen T. Siponen I. Salonen T. Yli-Tuomi M. Aurela H. Dufva, et al. Low-level exposure to ambient particulate matter is associated with systemic inflammation in ischemic heart disease patients Environ Res 116 2012 44 51
45. M.L. Block L. Calderon-Garciduenas Air pollution: Mechanisms of neuroinflammation and CNS disease Trends Neurosci 32 9 2009 506 516
46. C. Terzano F. Di Stefano V. Conti E. Graziani A. Petroianni Air pollution ultrafine particles: Toxicity beyond the lung Eur Rev Med Pharmacol Sci 14 10 2010 809 821
47. J. Wu C. Wang J. Sun Y. Xue Neurotoxicity of silica nanoparticles: Brain localization and dopaminergic neurons damage pathways ACS nano 5 6 2011 4476 4489
48. T.T. Win-Shwe H. Fujimaki Nanoparticles and neurotoxicity Int J Mol Sci 12 9 2011 6267 6280
49. H.S. Sharma A. Sharma Neurotoxicity of engineered nanoparticles from metals CNS Neurol Disord Drug Targets 11 1 2012 65 80
50. A. Sharma D.F. Muresanu R. Patnaik H.S. Sharma Size- and age-dependent neurotoxicity of engineered metal nanoparticles in rats Mol Neurobiol 48 2 2013 386 396
51. K.H. Shim J. Hulme E.H. Maeng M.K. Kim S.S. An Analysis of SiO2 nanoparticles binding proteins in rat blood and brain homogenate Int J Nanomed 9 Suppl 2 2014 207 215
52. S. Levesque T. Taetzsch M.E. Lull U. Kodavanti K. Stadler A. Wagner, et al. Diesel exhaust activates and primes microglia: Air pollution, neuroinflammation, and regulation of dopaminergic neurotoxicity Environ Health Perspect 119 8 2011 1149 1155
53. S. Levesque T. Taetzsch M.E. Lull J.A. Johnson C. McGraw M.L. Block The role of MAC1 in diesel exhaust particle-induced microglial activation and loss of dopaminergic neuron function J Neurochem 125 5 2013 756 765
54. S. Levesque M.J. Surace J. McDonald M.L. Block Air pollution & the brain: Subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease J Neuroinflammation 8 2011 105
55. X. Wang W. Wang L. Li G. Perry H.G. Lee X. Zhu Oxidative stress and mitochondrial dysfunction in Alzheimer's disease Biochim Biophys Acta 1842 8 2014 1240 1247
56. R.J. Castellani G. Perry The complexities of the pathology-pathogenesis relationship in Alzheimer disease Biochem Pharmacol 88 4 2014 671 676
57. L. Calderon-Garciduenas M. Macias-Parra H.J. Hoffmann G. Valencia-Salazar C. Henriquez-Roldan N. Osnaya, et al. Immunotoxicity and environment: Immunodysregulation and systemic inflammation in children Toxicol Pathol 37 2 2009 161 169
58. R.L. Doty Olfaction in Parkinson's disease and related disorders Neurobiol Dis 46 3 2012 527 552
59. I.L. Bergin F.A. Witzmann Nanoparticle toxicity by the gastrointestinal route: Evidence and knowledge gaps Int J Biomed Nanosci Nanotechnol 3 1-2 2013
60. G.G. Kaplan M. Szyszkowicz J. Fichna B.H. Rowe E. Porada R. Vincent, et al. Non-specific abdominal pain and air pollution: A novel association PloS one 7 10 2012 e47669
61. G.G. Kaplan J. Hubbard J. Korzenik B.E. Sands R. Panaccione S. Ghosh, et al. The inflammatory bowel diseases and ambient air pollution: A novel association Am J Gastroenterol 105 11 2010 2412 2419
62. L. Kish N. Hotte G.G. Kaplan R. Vincent R. Tso M. Ganzle, et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome PloS one 8 4 2013 e62220
63. H. Braak U. Rub W.P. Gai K. Del Tredici Idiopathic Parkinson's disease: Possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen J Neural Transm 110 5 2003 517 536
64. E.C. Levin N.K. Acharya M. Han S.B. Zavareh J.C. Sedeyn V. Venkataraman, et al. Brain-reactive autoantibodies are nearly ubiquitous in human sera and may be linked to pathology in the context of blood-brain barrier breakdown Brain Res 1345 2010 221 232
65. B. Diamond G. Honig S. Mader L. Brimberg B.T. Volpe Brain-reactive antibodies and disease Ann Rev immunol 31 2013 345 385
66. L. Calderon-Garciduenas A. D'Angiulli R.J. Kulesza R. Torres-Jardon N. Osnaya L. Romero, et al. Air pollution is associated with brainstem auditory nuclei pathology and delayed brainstem auditory evoked potentials Int J Dev Neurosci 29 4 2011 365 375
67. H. Braak K. Del Tredici U. Rub R.A. de Vos E.N. Jansen Steur E. Braak Staging of brain pathology related to sporadic Parkinson's disease Neurobiol Aging 24 2 2003 197 211
68. K. Del Tredici H. Braak Dysfunction of the locus coeruleus-norepinephrine system and related circuitry in Parkinson's disease-related dementia J Neurol Neurosurg Psychiatry 84 7 2013 774 783
69. W.G. Meissner When does Parkinson's disease begin? From prodromal disease to motor signs Rev Neurol 168 11 2012 809 814
70. F. Tison W.G. Meissner Movement disorders in 2013: Diagnosing and treating PD-the earlier the better? Nat Rev Neurol 10 2 2014 65 66
71. R.D. Prediger A.S. Aguiar Jr. F.C. Matheus R. Walz L. Antoury R. Raisman-Vozari, et al. Intranasal administration of neurotoxicants in animals: Support for the olfactory vector hypothesis of Parkinson's disease Neurotox Res 21 1 2012 90 116
72. H. Braak K. Del Tredici Where, when, and in what form does sporadic Alzheimer's disease begin? Current Opin Neurol 25 6 2012 708 714
73. H. Braak D.R. Thal E. Ghebremedhin K. Del Tredici Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years J Neuropathol Exp Neurol 70 11 2011 960 969
74. L. Qin X. Wu M.L. Block Y. Liu G.R. Breese J.S. Hong, et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration Glia 55 5 2007 453 462
75. A.M. Hartz B. Bauer M.L. Block J.S. Hong D.S. Miller Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the blood-brain barrier FASEB J 22 8 2008 2723 2733
76. S.M. MohanKumar A. Campbell M. Block B. Veronesi Particulate matter, oxidative stress and neurotoxicity Neurotoxicology 29 3 2008 479 488
77. J.Z. Wang Y.Y. Xia I. Grundke-Iqbal K. Iqbal Abnormal hyperphosphorylation of tau: Sites, regulation, and molecular mechanism of neurofibrillary degeneration J Alzheimers Dis 33 Suppl 1 2013 S123 S139
78. J. Avila G. Leon-Espinosa E. Garcia V. Garcia-Escudero F. Hernandez J. Defelipe Tau phosphorylation by GSK3 in different conditions Int J Alzheimers Dis 2012 2012 578373
79. H.G. Lee G. Perry P.I. Moreira M.R. Garrett Q. Liu X. Zhu, et al. Tau phosphorylation in Alzheimer's disease: Pathogen or protector? Trends Mol Med 11 4 2005 164 169
80. L. Buee L. Troquier S. Burnouf K. Belarbi A. Van der Jeugd T. Ahmed, et al. From tau phosphorylation to tau aggregation: What about neuronal death? Biochem Soc Trans 38 4 2010 967 972
81. F. Hernandez J. Avila Intra- and extracellular protein interactions with tau Curr Alzheimer Res 7 8 2010 670 676
82. M.G. Spillantini M. Goedert Tau pathology and neurodegeneration Lancet Neurol 12 6 2013 609 622
83. F. Clavaguera J. Hench M. Goedert M. Tolnay Invited review: Prion-like transmission and spreading of tau pathology Neuropathol Applied Neurobiol 41 1 2015 47 58
84. M. Goedert B. Falcon F. Clavaguera M. Tolnay Prion-like mechanisms in the pathogenesis of tauopathies and synucleinopathies Curr Neurol Neurosci Reports 14 11 2014 495
85. C.R. Jung Y.T. Lin B.F. Hwang Ozone, particulate matter, and newly diagnosed Alzheimer's disease: A population-based cohort study in Taiwan J Alzheimers Dis 44 2 2015 573 584
86. D.J. Bonda X. Wang H.G. Lee M.A. Smith G. Perry X. Zhu Neuronal failure in Alzheimer's disease: A view through the oxidative stress looking-glass Neurosci Bull 30 2 2014 243 252
87. B.A. Silva L. Breydo A.L. Fink V.N. Uversky Agrochemicals, alpha-synuclein, and Parkinson's disease Mol Neurobiol 47 2 2013 598 612
88. M.T. Baltazar R.J. Dinis-Oliveira M. de Lourdes Bastos A.M. Tsatsakis J.A. Duarte F. Carvalho Pesticides exposure as etiological factors of Parkinson's disease and other neurodegenerative diseases-a mechanistic approach Toxicol Lett 230 2 2014 85 103
89. J.A. Palma H. Kaufmann Autonomic disorders predicting Parkinson's disease Parkinsonism Relat Disord 20 Suppl 1 2014 S94 S98
90. J.B. Anang J.F. Gagnon J.A. Bertrand S.R. Romenets V. Latreille M. Panisset, et al. Predictors of dementia in Parkinson disease: A prospective cohort study Neurology 83 14 2014 1253 1260
91. J. Xia D.M. Rocke G. Perry M. Ray Differential network analyses of Alzheimer's disease identify early events in Alzheimer's disease pathology Int J Alzheimers Dis 2014 2014 721453
92. R. Rodrigues R.B. Petersen G. Perry Parallels between major depressive disorder and Alzheimer's disease: Role of oxidative stress and genetic vulnerability Cell Mol Neurobiol 34 7 2014 925 949
93. A. Ascherio K.L. Munger Environmental risk factors for multiple sclerosis. Part II: Noninfectious factors Ann Neurol 61 6 2007 504 513
94. A. Ascherio K.L. Munger Environmental risk factors for multiple sclerosis. Part I: The role of infection Ann Neurol 61 4 2007 288 299
95. T. Riise M.W. Nortvedt A. Ascherio Smoking is a risk factor for multiple sclerosis Neurology 61 8 2003 1122 1124
96. Y. Mikaeloff G. Caridade M. Tardieu S. Suissa Parental smoking at home and the risk of childhood-onset multiple sclerosis in children Brain 130 10 2007 2589 2595
97. M.A. Hernán M.J. Oleky A. Ascherio Cigarette smoking and incidence of multiple sclerosis Am J Epidemiol 154 1 2001 69 74
98. S. Simpson L. Blizzard P. Otahal I. Van der Mei B. Taylor Latitude is significantly associated with the prevalence of multiple sclerosis: A meta-analysis J Neurol Neurosurg Psychiatry 2011 [jnnp. 2011.240432]
99. M. Soilu-Hanninen M. Laaksonen I. Laitinen J.P. Eralinna E.M. Lilius I. Mononen A longitudinal study of serum 25-hydroxyvitamin D and intact parathyroid hormone levels indicate the importance of vitamin D and calcium homeostasis regulation in multiple sclerosis J Neurol Neurosurg Psychiatry 79 2 2008 152 157
100. K.L. Munger S. Zhang E. O'reilly M. Hernan M. Olek W. Willett, et al. Vitamin D intake and incidence of multiple sclerosis Neurology 62 1 2004 60 65
101. K.L. Munger L.I. Levin B.W. Hollis N.S. Howard A. Ascherio Serum 25-hydroxyvitamin d levels and risk of multiple sclerosis JAMA 296 23 2006 2832 2838
102. F. Hosseinpanah H. Sima M. Heibatollahi N. Moghbel S. Asefzade F. Azizi The effects of air pollution on vitamin D status in healthy women: A cross sectional study BMC Public Health 10 1 2010 519
103. K.S. Agarwal M.Z. Mughal P. Upadhyay J.L. Berry E.B. Mawer J.M. Puliyel The impact of atmospheric pollution on vitamin D status of infants and toddlers in Delhi, India Arch Dis Child 87 2 2002 111 113
104. N. Baiz P. Dargent-Molina J.D. Wark J.C. Souberbielle R. Slama I. Annesi-Maesano, et al. Gestational exposure to urban air pollution related to a decrease in cord blood vitamin d levels J Clin Endocrinol Metab 97 11 2012 4087 4095
105. D.H. Manicourt J.P. Devogelaer Urban tropospheric ozone increases the prevalence of vitamin D deficiency among Belgian postmenopausal women with outdoor activities during summer J Clin Endocrinol Metab 93 10 2008 3893 3899
106. L. Calderon-Garciduenas B. Azzarelli H. Acuna R. Garcia T.M. Gambling N. Osnaya, et al. Air pollution and brain damage Toxicol Pathol 30 3 2002 373 389
107. M. Oikonen M. Laaksonen P. Laippala O. Oksaranta E.M. Lilius S. Lindgren, et al. Ambient air quality and occurrence of multiple sclerosis relapse Neuroepidemiology 22 1 2003 95 99
108. A.C. Gregory 2nd D.G. Shendell I.S. Okosun K.E. Gieseker Multiple Sclerosis disease distribution and potential impact of environmental air pollutants in Georgia Sci Total Environ 396 1 2008 42 51
109. P. Heydarpour H. Amini S. Khoshkish H. Seidkhani M.A. Sahraian M. Yunesian Potential impact of air pollution on multiple sclerosis in Tehran, Iran Neuroepidemiology 43 3-4 2014 233 238
110. M. Saei K. Holakouie-Naieni E. Mostafavi M.A. Sahraian M. Mahmoodi M.A. Mansournia, et al. Spatial analysis of multiple sclerosis disease in Tehran metro-politan zone, Iran, 2001-2012 Iran J Public Health 43 5 2014 621 629
111. M. Mehrpour N.S. Shams-hosseini S. Rezaali M.A. Sahraian S. Taki Effect of air pollutant markers on multiple sclerosis relapses Iran J Public Health 42 10 2013 1167 1173
112. S.D. Vojinoviü Slobodan S. Lukiü L. Saviü J. Vojinoviü Disease relapses in multiple sclerosis can be influenced by air pollution and climate seasonal conditions Vojnosanit Pregl 72 1 2015 44 49
113. M.K. Oikonen J.P. Eralinna Beta-interferon protects multiple sclerosis patients against enhanced susceptibility to infections caused by poor air quality Neuroepidemiology 30 1 2008 13 19
114. A. Campbell M. Oldham A. Becaria S.C. Bondy D. Meacher C. Sioutas, et al. Particulate matter in polluted air may increase biomarkers of inflammation in mouse brain Neurotoxicology 26 1 2005 133 140
115. M.T. Kleinman J.A. Araujo A. Nel C. Sioutas A. Campbell P.Q. Cong, et al. Inhaled ultrafine particulate matter affects CNS inflammatory processes and may act via MAP kinase signaling pathways Toxicol Lett 178 2 2008 127 130
116. M.E. Gerlofs-Nijland D. van Berlo F.R. Cassee R.P. Schins K. Wang A. Campbell Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain Particle Fibre toxicol 7 2010 12
117. E.E. Agency Safeguarding people from environmental risks to health; the European environment-state and outlook 2015: Synthesis report 2015 Copenhagen