Exposure to severe urban air pollution influences cognitive outcomes, brain volume and systemic inflammation in clinically healthy children

Brain and Cognition

Volumn 77, Issue 3, 2011, Pages 345-355

  Calderón Garcidueñas, Lilian ^a,b   Engle, Randall ^c   Antonieta Mora Tiscareno A M ^a   Styner, Martin ^d   Gómez Garza, Gilberto ^a   Zhu, Hongtu ^e   Jewells, Valerie ^d   Torres Jardón, Ricardo ^f   Romero, Lina ^a   Monroy Acosta, Maria E ^a   Bryant, Christopher ^e   González González, Luis Oscar ^a   Medina Cortina, Humberto ^a   D'Angiulli, Amedeo ^g  

^a INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^b UNIVERSITY OF MONTANA   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e IL   (United States)

^f UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^g CARLETON UNIVERSITY   (Canada)

Author keywords

Air pollution; Brain MRI; Children; Cognition; Particulate matter; Systemic inflammation; White matter hyperintensities; White matter volume

Indexed keywords

C REACTIVE PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

AIR POLLUTION; ARTICLE; BRAIN GROWTH; BRAIN SIZE; CHILD; COGNITION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EOSINOPHIL COUNT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFLAMMATION; LYMPHOCYTE COUNT; MALE; NEUROIMAGING; NEUTROPHIL COUNT; NORMAL HUMAN; PARIETAL LOBE; PARTICULATE MATTER; PRESCHOOL CHILD; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; SCHOOL CHILD; TEMPORAL LOBE; WECHSLER INTELLIGENCE SCALE; WHITE MATTER; BRAIN; CHEMICALLY INDUCED DISORDER; COGNITIVE DEFECT; INTELLIGENCE TEST; MEXICO; MYELINATED NERVE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PATHOLOGY;

AIR POLLUTION; BRAIN; CHILD; COGNITION; COGNITION DISORDERS; FEMALE; HUMANS; INFLAMMATION; INTELLIGENCE TESTS; MAGNETIC RESONANCE IMAGING; MALE; MEXICO; NERVE FIBERS, MYELINATED; NEUROPSYCHOLOGICAL TESTS; ORGAN SIZE; PROSPECTIVE STUDIES;

EID: 84859258684     PISSN: 02782626     EISSN: 10902147     Source Type: Journal    
DOI: 10.1016/j.bandc.2011.09.006     Document Type: Article

References (66)

1. Block, M., & Calderón-Garcidueñas, L. (2009). Air pollution: Mechanisms of neuroinflammation & CNS disease. Trends in Neurosciences, 32, 506-516.
2. Bonner, J. C., Rice, A. B., Lindroos, P. M., et al. (1998). Induction of the lung myofibroblast PDGF receptor system by urban ambient particles from Mexico City. American Journal of Respiratory Cell and Molecular Biology, 19, 672-680.
3. Bravo-Alvarez, H. R., & Torres-Jardón, R. (2002). Air pollution levels and trends in the México City metropolitan area. In M. Fenn, L. de Bauer, & T. Hernández (Eds.). Urban air pollution and forest: Resources at risk in the Mexico City air basin. Ecological studies (Vol. 156, pp. 121-159). New York: Springer-Verlag.
4. Calderón-Garcidueñas, L., Azzarelli, B., Acuña, H., et al. (2002). Air pollution and brain damage. Toxicologic Pathology, 30, 373-389
5. Calderón-Garcidueñas, L., D'Angiulli, A., Kulesza, R. J., et al. (2011). Air pollution is associated with brainstem auditory nuclei pathology and delayed brainstem auditory evoked potentials. International Journal of Developmental Neuroscience, 29, 365-375.
6. Calderón-Garcidueñas, L., Kavanaugh, M., Block, M. L., et al. (2011). Neuroinflammation, hyperphosphorilated tau, diffuse amyloid plaques andand adults. Journal of Alzheimer Disease. [Epub ahead of print].
7. Calderón-Garcidueñas, L., Franco-Lira, M., Henriquez-Roldan, C., et al. (2009). Urban air pollution: Influences on olfactory function and pathology in exposed children and young adults. Experimental and Toxicologic Pathology, 37, 161-169.
8. Calderón-Garcidueñas, L., Franco-Lira, M., Torres-Jardón, R., et al. (2007). Pediatric respiratory and systemic effects of chronic air pollution exposure: Nose, lung, heart, and brain pathology. Toxicologic Pathology, 35, 154-162.
9. Calderón-Garcidueñas, L., Macias-Parra, M., Hoffman, H. J., et al. (2009). Immunotoxicity and environment: Immunodysregulation and systemic inflammation in children. Toxicologic Pathology, 37, 161-169.
10. Calderón-Garcidueñas, L., Mora-Tiscareño, A., Fordham, L. A., et al. (2003). Respiratory damage in children exposed to urban pollution. Pediatric Pulmonology, 36, 148-161.
11. Calderón-Garcidueñas, L., Mora-Tiscareño, A., Ontiveros, E., et al. (2008). Air pollution, cognitive deficits and brain abnormalities: A pilot study with children and dogs. Brain and Cognition, 68, 117-127.
12. Calderón-Garcidueñas, L., Reed, W., Maronpot, R. R., et al. (2004). Brain inflammation and Alzheimer's-like pathology in individuals exposed to severe air pollution. Toxicologic Pathology, 32, 650-658.
13. Calderón-Garcidueñas, L., Solt, A., Franco-Lira, M., et al. (2008). Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain-barrier, ultrafine particle deposition, and accumulation of amyloid beta 42 and alpha synuclein in children and young adults. Toxicologic Pathology, 36, 289-310.
14. Calderón-Garcidueñas, L., Valencia-Salazar, G., Rodríguez-Alcaraz, A., et al. (2001). Ultrastructural nasal pathology in children chronically and sequentially exposed to air pollutants. American Journal of Respiratory Cell and Molecular Biology, 24, 132-138.
15. Calderón-Garcidueñas, L., Villarreal-Calderon, R., Valencia-Salazar, G., et al. (2008). Systemic inflammation, endothelial dysfunction, and activation in clinically healthy children exposed to air pollutants. Inhalation Toxicology, 20, 499-506.
16. Calderón-Garcidueñas, L., Vincent, R., Mora-Tiscareño, A., et al. (2007). Elevated plasma endothelin-1 and pulmonary arterial pressure in children exposed to air pollution. Environmental Health Perspectives, 115, 1248-1253.
17. Calderón-Segura, M. E., Gómez-Arroyo, S., Villalobos-Pietrini, R., et al. (2004). The effects of seasonal weather on the genotoxicity, cytokinetic properties, cytotoxicity and organochemical content of extracts of airborne particulates in Mexico City. Mutation Research, 558, 7-17.
18. Chauhan, V., Breznan, D., Thomson, E., Karthikeyan, S., & Vincent, R. (2005). Effects of ambient air particles on the endothelin system in human pulmonary epithelial cells. Cell Biology and Toxicology, 21, 191-205.
19. Chertoff, M., Di Paolo, N., Schoeneberg, A., et al. (2011). Neuroprotective and neurodegenerative effects of the chronic expression of tumor necrosis factor a in the nigrostratial dopaminergic circuit of adult mice. Experimental Neurology, 227, 237-251.
20. Clark, I. A., Alleva, L. M., & Vissel, B. (2010). The role of TNF in brain dysfunction and disease. Pharmacology and Therapeutics, 128, 519-548.
21. Danzer, S. C. (2008). Postnatal and adult neurogenesis in the development of human disease. Neuroscientist, 14, 446-458.
22. Debette, S., & Markus, H. S. (2010). The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: Systematic review and meta-analysis. British Medical Journal, 26(341), c3666. doi:10.1136/bmj.c3666.
23. Dorado-Martinez, C., Paredes-Carbajal, C., Mascher, D., et al. (2001). Effects of different ozone doses on memory, motor activity and lipid peroxidation levels, in rats. International Journal of Neuroscience, 108, 149-161.
24. Dzepina, K., Arey, J., Marr, L., et al. (2007). Detection of particle-phase polycyclic aromatic hydrocarbons in Mexico City using an aerosol mass spectrometer. International Journal of Mass Spectrometry, 263, 152-170.
25. Estrada-Garcia, T., Cerna, J. F., Thompson, M. R., et al. (2002). Fecal contamination and enterotoxigenic Escherichia coli in street-vended chili sauces in Mexico and its public relevance. Epidemiology and Infection, 129, 223-226.
26. Farkas, E., Süle, Z., Tóth-Szuki, V., et al. (2006). Tumor necrosis factor-alpha increases cerebral blood flow and ultrastructural capillary damage through the release of nitric oxide in the rat brain. Microvascular Research, 72, 113-119.
27. Gerlofs-Nijland, M. E., van Berlo, D., Casee, F. R., et al. (2010). Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain. Particle and Fiber Toxicology, 17, 7-12.
28. Gläscher, J., Rudrauf, D., Colom, R., et al. (2010). Distributed neural system for general intelligence revealed by lesion mapping. Proceedings of the National Academy of Sciences of the United States of America, 107, 4705-4709.
29. Gläscher, J., Tranel, D., Paul, L. K., et al. (2009). Lesion mapping of cognitive abilities linked to intelligence. Neuron, 61, 681-691.
30. Gobierno del Estado de México. Plan Municipal de Desarrollo Urbano de Polotitlán, 2008. H. Ayuntamiento de Polotitlán. Secretaría de Desarrollo Urbano. Gobierno del Estado de México.
31. Gouttard, S., Styner, M. H., Prastawa, M., et al. (2008). Assessment of reliability of multi-site neuroimaging via traveling phantom study. Medical Image Computing and Computer Assisted Intervention, 11, 263-270.
32. Haier, R. J., Jung, R. E., Yeo, R. A., et al. (2004). Structural brain variation and general intelligence. Neuroimage, 23, 425-433.
33. Hong, Y. C., Lee, J. T., Kim, H., & Kwon, H. J. (2002). Air pollution: A new risk factor in ischemic stroke mortality. Stroke, 33, 2165-2169.
34. Huang, Y., Zhang, W., Lin, L., et al. (2010). Is endothelial dysfunction of cerebral small vessels responsible for white matter lesions after chronic cerebral hypoperfusion in rats? Journal of the Neurological Sciences.
35. Hwang, L. (2007). Environmental stressors and violence: Lead and polychlorinated biphenyls. Reviews on Environmental Health, 22, 313-328.
36. Jefferson, A. L., Massaro, J. M., Wolf, P. A., et al. (2007). Inflammatory markers are associated with total brain volume: The Framingham Heart Study. Neurology, 68, 1032-1038.
37. Joshi, S., Davis, B., Jomier, M., & Gerig, G. (2004). Unbiased diffeomorphic atlas construction for computational anatomy. Neuroimage, 23(SUPPL. 1), S151-S160.
38. Jung, R. E., & Haier, R. J. (2007). The parieto-frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence. Behavioral and Brain Sciences, 30, 135-154.
39. Kraut, M. A., Beason-Held, L. L., Elkins, W. D., & Resnick, S. M. (2008). The impact of magnetic resonance imaging-detected white matter hyperintensities on longitudinal changes in regional cerebral blood flow. Journal of Cerebral Blood Flow and Metabolism, 28, 190-197.
40. Levesque, S., Surace, M. J., McDonald, J., & Block, M. L. (2011). Air pollution and the brain: Subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease. Environmental Health Perspectives, 119, 1149-1155.
41. Maheswaran, R., Pearson, T., Campbell, M. J., et al. (2006). A protocol for investigation of the effects of outdoor air pollution on stroke incidence, phenotypes and survival using the South London Stroke Register. International Journal of Health Geographics, 5, 10-17.
42. Maillard, P., Fletcher, E., Harvey, D., et al. (2011). White matter hyperintensity penumbra. Stroke, 42, 1917-1922.
43. McCarron, R. M., Chen, Y., Tomori, T., et al. (2006). Endothelial-mediated regulation of cerebral microcirculation. Journal of Physiology and Pharmacology, 57(SUPPL. 11), 133-144.
44. Moldes, O., Sobrino, T., Millan, M., et al. (2008). High serum levels of endothelin-1 predict severe cerebral edema in patients with acute ischemic stroke treated with t-PA. Stroke, 39, 2006-2010.
45. Molina, L. T., Kolb, C. E., de Foy, B., Lamb, B. K., Brune, W. H., & Jimenez, J. L. (2007). Air quality in North America's most populous city-overview of the MCMA-2003 campaign. Atmospheric Chemistry and Physics, 7, 2447-2473.
46. Molina, L. T., Madronich, S., Gaffney, J. S., et al. (2010). An overview of the MILAGRO 2006 Campaign: Mexico City emissions and their transport and transformation. Atmospheric Chemistry and Physics, 10, 8697-8760.
47. Osornio-Vargas, A., Bonner, J. C., Alfaro-Moreno, E., et al. (2003). Proinflammatory and cytotoxic effects of Mexico City air pollution particulate matter in vitro are dependent on particle size and composition. Environmental Health Perspectives, 111, 1289-1293.
48. Peters, A., Veronesi, B., Calderón-Garcidueñas, L., et al. (2006). Translocation and potential neurological effects of fine and ultrafine particles a critical update. Particle and Fibre Toxicology, 8, 3-13.
49. Prastawa, M., Gilmore, J. H., Lin, W., & Gerig, G. (2005). Automatic segmentation of MR images of the developing newborn brain. Medical Image Analysis, 9, 457-466.
50. Querol, X., Pey, J., Minguillón, M. C., Pérez, N., et al. (2008). PM speciation and sources in Mexico during the MILAGRO-2006 Campaign. Atmospheric Chemistry and Physics, 8, 111-128.
51. Rosas-Pérez, I., Serrano, J., Alfaro-Moreno, E., et al. (2007). Relations between PM10 composition and cell toxicity: A multivariate and graphical Approach. Chemosphere, 67, 1218-1228.
52. Salonia, R., Empey, P. E., Poloyac, S. M., et al. (2010). Endothelin-1 is increased in cerebrospinal fluid and associated with unfavorable outcomes in children after severe traumatic brain injury. Journal of Neurotrauma, 27, 1819-1825.
53. Schmithorst, V. J., Wilke, M., Dardzinski, B. J., & Holland, S. K. (2005). Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study. Human Brain Mapping, 26, 139-147.
54. Simes, R. (1986). An improved Bonferroni procedure for multiple tests of significance. Biometrika, 73, 751-754.
55. SMA (2010). Secretaría del Medio Ambiente del Gobierno del Distrito Federal. Dirección General de Gestión de la Calidad del Aire. Sistema de monitoreo Atmosférico de la ciudad de México. Dirección de Monitoreo Atmosférico..
56. Stein, J., Schettler, T., Wallinga, D., & Valenti, M. (2002). In harm's way: Toxic threats to child development. Journal of Developmental and Behavioral Pediatrics, 23, S13-S22.
57. Styner, M. H., Charles, C., Park, J., Lieberman, J., & Gerig, G. (2002). Multi-site validation of image analysis methods-ssessing intra and inter-site variability. Proceedings of the SPIE Medical Imaging, 4684, 278-286.
58. Styner, M. H., Gerig, G., Brechbuhler, C., & Szekely, G. (2000). Parametric estimate of intensity inhomogeneities applied to MRI. IEEE Transactions on Medical Imaging, 19, 153-165.
59. Thomson, E. M., Kumarathasan, P., Calderón-Garcidueñas, L., & Vincent, R. (2007). Air pollution alters brain and pituitary endothelin-1 and inducible nitric oxide synthase gene expression. Environmental Research, 105, 224-233.
60. Villarreal-Calderon, A., Acuña, H., Villarreal-Calderón, J., et al. (2002). Archives of Environmental Health, 57, 450-460.
61. Villarreal-Calderon, R., Torres-Jardon, R., Osnaya, N., et al. (2010). Urban air pollution targets the dorsal vagal complex and dark chocolate offers neuroprotection. International Journal of Toxicology, 29, 604-615.
62. Wechsler, D. (1974). Wechsler intelligence scale for children-revised. The Psychological Corporation. New York, NY 10017, USA.
63. Wigle, D. T., Arbuckle, T. E., Walke, R. M., Liu, S., & Krewski, D. (2007). Environmental hazards: Evidence for effects on child health. Journal of Toxicology and Environmental Health, Part B: Critical Reviews, 10, 3-39
64. Woolgar, A., Parr, A., Cusack, R., et al. (2010). Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex. Proceedings of the National Academy of Sciences of the United States of America, 107, 14899-14902.
65. Yadav, A., Saini, V., & Arora, S. (2010). MCP-1: Chemoattractant with a role beyond immunity: A review. Clinica Chimica Acta, 411, 1570-1579.
66. Zlokovic, B. V. (2008). The blood-brain-barrier in health and chronic neurodegenerative diseases. Neuron, 57, 178-201.