Decreases in Short Term Memory, IQ, and Altered Brain Metabolic Ratios in Urban Apolipoprotein ε4 Children Exposed to Air Pollution

Journal of Alzheimer's Disease

Volumn 45, Issue 3, 2015, Pages 757-770

  Calderón Garcidueñas, Lilian ^a,b   Mora Tiscareño, Antonieta ^c   Franco Lira, Maricela ^b   Zhu, Hongtu ^d   Lu, Zhaohua ^d   Solorio, Edelmira ^c   Torres Jardón, Ricardo ^e   D'Angiulli, Amedeo ^f  

^a UNIVERSITY OF MONTANA   (United States)

^b HOSPITAL CENTRAL MILITAR   (Mexico)

^c INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^d IL   (United States)

^e UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^f CARLETON UNIVERSITY   (Canada)

Author keywords

Air pollution; APOE; children; cognition; frontal white matter; hippocampus; magnetic resonance spectroscopy; megacities; neuroprotection; olfaction; particulate matter

Indexed keywords

APOLIPOPROTEIN E4; CHOLINE; CREATINE; INOSITOL; N ACETYLASPARTIC ACID; ASPARTIC ACID; N-ACETYLASPARTATE;

ADOLESCENT; AIR POLLUTION; ARTICLE; BRAIN METABOLISM; CHILD; COGNITION; ENVIRONMENTAL EXPOSURE; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HUMAN; INTELLIGENCE QUOTIENT; MALE; MEXICO; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PONS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SHORT TERM MEMORY; SMELLING; URBAN POPULATION; WECHSLER INTELLIGENCE SCALE; WHITE MATTER; AGE; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; BRAIN; GENETICS; INTELLIGENCE; MEMORY DISORDERS; METABOLISM; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ODOR; PATHOLOGY; PHYSIOLOGY;

ADOLESCENT; AGE FACTORS; AIR POLLUTION; ANALYSIS OF VARIANCE; APOLIPOPROTEIN E4; ASPARTIC ACID; BRAIN; CHILD; CHOLINE; CREATINE; FEMALE; HUMANS; INTELLIGENCE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MEXICO; NEUROPSYCHOLOGICAL TESTS; SMELL; WECHSLER SCALES;

EID: 84925814859     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-142685     Document Type: Article

References (109)

1. Calderón-Garcidueñas L, Kavanaugh M, Block ML, D'Angiulli A, Delgado-Chávez R, Torres-Jardón R, Gonz ález-Maciel A, Reynoso-Robles R, Villarreal- Calderón R, Guo R, Hua Z, Zhu H, Perry G, Diaz P (2012) Neuroinflammation, hyperphosphorylated tau, diffuse amyloid plaques and down-regulation of the cellular prion protein in air pollution exposed children and adults. J Alzheimers Dis 28, 93-107.
2. Michaelson DM (2014) ApoE4: The most prevalent yet understudied risk factor for Alzheimer's disease. Alzheimers Dement 10, 861-868.
3. Huang Y, Mahley RW (2014) Apolipoprotein E: Structure and function in lipid metabolism, neurobiology, and Alzheimer's disease. Neurobiol Dis 72PA, 3-12.
4. Kanekiyo T, Xu H, Bu G (2014) ApoE and Aβ in Alzheimer's disease: Accidental encounters or partners? Neuron 81, 740-754.
5. Calderón-Garcidueñas L, Azzarelli B, Acuña H, Garcia R, Gambling TM, Monroy S, Tizapantzi MR, Carson JL, Villarreal-Calderon A, Rewcastle B (2002) Air pollution and brain damage. Toxicol Pathol 30, 373-389.
6. Calderón-Garcidueñas L, Maronpot RR, Torres-Jardón R, Henríquez-Roldán C, Schoonhoven R, Acuña-Ayala H, Villarreal-Calderón A, Nakamura J, Fernando R, Reed W, Azzarelli B, Swenberg JA (2003) DNA damage in nasal and brain tissues of canines exposed to air pollutants is associated with evidence of chronic inflammation and neurodegeneration. Toxicol Pathol 31, 524-538.
7. Calderón-Garcidueñas L, Franco-Lira M, Henríquez-Roldán C, González-Maciel A, Reynoso-Robles R, Villarreal-Calderon R, Herritt L, Brooks D, Keefe S, Palacios-Moreno J, Villarreal-Calderon R, Torres-Jardón R, Medina-Cortina H, Delgado-Chávez R, Aiello-Mora M, Maronpot RR, Doty RL (2010) Urban air pollution: Influences on olfactory function and pathology in exposed children and young adults. Exp Toxicol Pathol 62, 91-102.
8. Calderón-Garcidueñas L, Valencia-Salazar G, Rodriguez-Alcaraz A, Gambling TM, Garcia R, Villarreal-Calderon A, Devlin RB, Carson JL (2001) Ultrastructural nasal pathology in children chronically and sequentially exposed to air pollutants. Am J Respir Cell Mol Biol 24, 132-138.
9. Calderón-Garcidueñas L, Mora-Tiscareño A, Styner M, Gómez-Garza G, Zhu H, Torres-Jardón R, Carlos E, Solorio-López E, Medina-Cortina H, Kavanaugh M, D'Angiulli A (2012) White matter hyperintensities, systemic inflammation, brain growth and cognitive functions in children exposed to air pollution. J Alzheimers Dis 31, 183-191.
10. Doty RL, Kamath V (2014) The influences of age on olfaction: A review. Front Psychol 5, 20.
11. Bravo-Alvarez HR, Torres-Jardón RJ (2002) Air pollution levels and trends in the Mexico City metropolitan area. In: Urban Air Pollution and Forests: Resources at Risk in the Mexico City Air Basin Ecological Studies, Fenn M, Bauer L, Hernández T, eds. Springer-Verlag, New York, pp. 121-159.
12. Molina LT, Kolb CE, de Foy B, Lamb BK, Brune WH, Jimenez JL, Ramos-Villegas R, Sarmiento J, Páramo-Figueroa VH, Cárdenas B, Gutierrez-Avedoy V, Molina MJ (2007) Air quality in North America's most populous city - overview of the MCMA-2003 campaign. Atmos Chem Phys 7, 2447-2473.
13. Molina LT, Madronich S, Gaffney JS, Apel E, de Foy B, Fast J, Ferrare R, Herndon S, Jimenez JL, Lamb B, Osornio- Vargas AR, Russell P, Schauer JJ, Stevens PS, Volkamer R, Zavala M (2010) An overview of the MILAGRO 2006 Campaign: Mexico City emissions and their transport and transformation. Atmos Chem Phys 10, 8697-8760.
14. SMA Secretaría del Medio Ambiente del Gobierno del Distrito Federal. Dirección General de Gestión de la Calidad del Aire. Sistema de monitoreo Atmosfárico de la Ciudad de Máxico. 2014. http://www.aire.df.gob.mx/default.php
15. Dzepina K, Arey J, Marr L, Worsnop DR, Salcedo D, Zhang Q, Onasch TB, Molina LT, Molina MJ, Jimenez JL (2007) Detection of particle-phase polycyclic aromatic hydrocarbons in Mexico City using an aerosol mass spectrometer. Int J Mass Spectrom 263, 152-170.
16. Estrada-Garcia T, Cerna JF, Thompson MR, López-Saucedo C (2002) Fecal contamination and enterotoxigenic Escherichia coli in street-vendor chili sauces in Mexico and its public relevance. Epidemiol Infect 129, 223-226.
17. Mugica-Álvarez V, Figueroa-Lara J, Romero-Romoa M, Sepúlveda-Sánchez J, López-Moreno T (2012) Concentrations and properties of airborne particles in the Mexico City subway system. Atmos Environ 49, 284-293.
18. Calderón-Segura ME, Gómez-Arroyo S, Villalobos-Pietrini R, Butterworth FM, Amador-Muñoz O (2004) The effects of seasonal weather on the genotoxicity, cytokinetic properties, cytotoxicity and organochemical content of extracts of airborne particulates in Mexico City. Mut Res 558, 7-17.
19. Rosas-Párez I, Serrano J, Alfaro-Moreno E, Baumgardner D, Garcia-Cuellar C, Martin del Campo JM, Raga GB, Castillejos M, Colin RD, Osornio-Vargas AR (2007) Relations between PM10 composition and cell toxicity: A multivariate and graphical approach. Chemosphere 67, 1218-1228.
20. Villarreal-Calderón A, Acuña H, Villarreal-Calderón J, Garduño M, Henriquez-Roldán CF, Calderón-Garcidueñas L, Valencia-Salazar G (2002) Assessment of physical education time and after-school outdoor time in elementary and middle school students in South Mexico City: The dilemma between physical fitness and adverse health effects of outdoor pollutant exposure. Arch Environ Health 57, 450-460.
21. Doty RL, Reyes PF, Gregor T (1987) Presence of both odor identification and detection deficits in Alzheimer's disease. Brain Res Bull 18, 597-600.
22. Doty RL, Bromley SM, Stern MB (1995) Olfactory testing as an aid in the diagnosis of Parkinson's disease: Development of optimal discrimination criteria. Neurodegeneration 4, 93-97.
23. Tabert MH, Liu X, Doty R, Serby M, Zamora D, Pelton GH, Marder K, Albers MW, Stern Y, Devanand DP (2005) A 10-item smell identification scale related to risk for Alzheimer's disease. Ann Neurol 58, 155-160.
24. Wechsler D (1974) Wechsler intelligence scale for childrenrevised, The Psychological Corporation, New York.
25. Gläscher J, Tranel D, Paul LK, Rudrauf D, Rorden C, Hornaday A, Grabowski T, Damasio H, Adolphs R (2009) Lesion mapping of cognitive abilities linked to intelligence. Neuron 61, 681-691.
26. Gläscher J, Rudrauf D, Colom R, Paul LK, Tranel D, Damasio H, Adolphs R (2010) Distributed neural system for general intelligence revealed by lesion mapping. Proc Natl Acad Sci U S A 107, 4705-4709.
27. Jung RE, Haier RJ (2007) The parieto-frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence. Behav Brain Sci 30, 135-154.
28. Haier RJ, Jung RE, Yeo RA, Head K, Alkire MT (2004) Structural brain variation and general intelligence. Neuroimage 23, 425-433.
29. Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK (2005) Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study. Hum Brain Mapp 26, 139-147.
30. Penke L, Maniega SM, Bastin ME, Valdés-Hernández MC, Murray C, Royle NA, Starr JM, Wardlaw JM, Deary IJ (2012) Brain white matter tract integrity as a neural foundation for general intelligence. Mol Psychiatry 17, 1026-1030.
31. Lyall DM, Harris SE, Bastin ME, Muñoz Maniega S, Murray C, Lutz MW, Saunders AM, Roses AD, Valdás-Hernandez MC, Royle NA, Starr JM, Porteous DJ, Wardlaw JM, Deary IJ (2014) Are APOE ε genotype and TOMM40 poly- T repeat length associations with cognitive ageing mediated by brain white matter tract integrity? Transl Psychiatry 4, e449.
32. Genin E, Hannequin D, Wallon D, Sleegers K, Hiltunen M, Combarros O, Bullido MJ, Engelborghs S, De Deyn P, Berr C, Pasquier F, Dubois B, Tognoni G, Fiévet N, Brouwers N, Bettens K, Arosio B, Coto E, Del Zompo M, Mateo I, Epelbaum J, Frank-Garcia A, Helisalmi S, Porcellini E, Pilotto A, Forti P, Ferri R, Scarpini E, Siciliano G, Solfrizzi V, Sorbi S, Spalletta G, Valdivieso F, Vepsäläinen S, Alvarez V, Bosco P, Mancuso M, Panza F, Nacmias B, Bossú P, Hanon O, Piccardi P, Annoni G, Seripa D, Galimberti D, Licastro F, Soininen H, Dartigues JF, Kamboh MI, Van Broeckhoven C, Lambert JC, Amouyel P, Campion D (2011) APOE and Alzheimer disease: A major gene with semi-dominant inheritance. Mol Psychiatry 16, 903-907.
33. Moffett JR, Arun P, Ariyannur PS, Namboodiri AM (2013) N-acetylaspartate reductions in brain injury: Impact on post-injury neuroenergetics, lipid synthesis, and protein acetylation. Front Neuroenergetics 5, 11.
34. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AM (2007) N-acetylaspartate in the CNS: From neurodiagnostics to neurobiology. Prog Neurobiol 81, 89-131.
35. Birken DL, Oldendorf WH (1989) N-acetyl-L-aspartic acid: A literature review of a compound prominent in 1H-NMR spectroscopic studies of the brain. Neurosci Biobehav Rev 13, 23-31.
36. Bjartmar C, Battistuta J, Terada N, Dupree E, Trapp BD (2002) N-acetylaspartate is an axon-specific marker of mature white matter in vivo: A biochemical and immunohistochemical study on the rat optic nerve. Ann Neurol 51, 51-58.
37. Zhu X, Schuff N, Kornak J, Soher B, Yaffe K, Kramer JH, Ezekiel F, Miller BL, Jagust WJ, Weiner MW (2006) Effects of Alzheimer disease on fronto parietal brain Nacetyl aspartate and myo-inositol using magnetic resonance spectroscopic imaging. Alzheimer Dis Assoc Disord 20, 77-85.
38. Lentz MR, Westmoreland SV, Lee V, Ratai EM, Halpern EF, Gonzalez RG (2008) Metabolic markers of neuronal injury correlate with SIV CNS disease severity and inoculum in the macaque model of neuro AIDS. Magn Reson Med 59, 475-484.
39. Mondino M, Brunelin J, Saoud M (2013) N-acetyl-aspartate level is decreased in the prefrontal cortex in subjects at risk for schizophrenia. Front Psychiatry 4, 99.
40. Harezlak J, Cohen R, Gongvatana A, Taylor M, Buchhal S, Schifitto G, Zhong J, Daar ES, Alger JR, Brown M, Singer EJ, Campbell TB, McMahon D, So YT, Yiannoutsos CT, Navia BA, the HIV, Neuroimaging, Consortium (2014) Predictors of CNS injury as measured by proton magnetic resonance spectroscopy in the setting of chronic HIV infection and CART. J Neurovirol 20, 294-303.
41. Lim TS, Hong YH, Lee HY, Choi JY, Kim HS, Moon SY (2012) Metabolite investigation in both anterior and posterior cingulate gyri in Alzheimer's disease spectrum using 3-tesla MR spectroscopy. Dement Geriatr Cogn Disord 33, 149-155.
42. Bittner DM, Heinze HJ, Kauffman J (2013) Association of1H-MR spectroscopy and cerebro-spinal fluid markers in Alzheimer's disease: Diverging behavior at three different brain regions. J Alzheimers Dis 36, 155-163.
43. Kantarci K (2007) 1H magnetic resonance spectroscopy in dementia. Br J Radiol 80, S146-S152.
44. Kantarci K (2013) Proton MRS in mild cognitive impairment. J Magn Reson Imaging 37, 770-777.
45. Kantarci K (2013) Magnetic resonance spectroscopy in common dementias. Neuroimaging Clin N Am 23, 393-406.
46. Kantarci K, Weigand SD, Przybelski SA, Preboske GM, Pankratz VS, Vemuri P, Senjem ML, Murphy MC, Gunter JL, Machulda MM, Ivnik RJ, Roberts RO, Boeve BF, Rocca WA, Knopman DS, Petersen RC, Jack CR Jr (2013) MRI and MRS predictors of mild cognitive impairment in a population-based sample. Neurology 81, 126-133.
47. Modrego PJ, Fayed N, Sarasa M (2011) Magnetic resonance spectroscopy in the prediction of early conversion from amnestic mild cognitive impairment to dementia: A prospective cohort study. BMJ Open 1, e000007.
48. Wang T, Xiao S, Li X, Ding B, Ling H, Chen K, Fang Y (2012) Using proton magnetic resonance spectroscopy to identify mild cognitive impairment. Int Psychogeriatr 24, 19-27.
49. Lipton ML, Kim N, Zimmerman ME, Kim M, Stewart WF, Branch CA, Lipton RB (2013) Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 268, 850-857.
50. Reijmer YD, Leemans A, Brundel M, Kappelle LJ, Biessels GJ, Utrecht Vascular Cognitive Impairment Study, Group (2013) Disruption of the cerebral white matter network is related to slowing of information processing speed in patients with type 2 diabetes. Diabetes 62, 2112-2115.
51. Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V, Patel MC, Counsell SJ, Sharp DJ (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134, 449-463.
52. Kosora E, Arciniegas DB, Duggan E, West S, Brown MS, Filley CM (2013) White matter abnormalities and working memory impairment in systemic lupus erythematosus. Cogn Behav Neurol 26, 63-72.
53. Sun X, Liang Y, Wang J, Chen K, Chen Y, Zhou X, Jia J, Zhang Z (2014) Early frontal structural and functional changes in mild white matter lesions relevant to cognitive decline. J Alzheimers Dis 40, 123-134.
54. Oertel-Knöchel V, Reinke B, Alves G, Jurcoane A, Wenzler S, Prvulovic D, Linden D, Knöchel C (2014) Frontal white matter alterations are associated with executive cognitive function in euthymic bipolar patients. J Affect Disord 155, 223-233.
55. Calderón-Garcidueñas L, Vincent R, Mora-Tiscareño A, Franco-Lira M, Henríquez-Roldán C, Barragán-Mejía G, Garrido-García L, Camacho-Reyes L, Valencia-Salazar G, Paredes R, Romero L, Osnaya H, Villarreal-Calderón R, Torres-Jardón R, Hazucha MJ, Reed W (2007) Elevated plasma endothelin-1 and pulmonary arterial pressure in children exposed to air pollution. Environ Health Perspect 115, 1248-1253.
56. Calderón-Garcidueñas L, Villarreal-Calderon R, Valencia-Salazar G, Henríquez-Roldán C, Gutiérrez-Castrellón P, Torres-Jardón R, Osnaya-Brizuela N, Romero L, Torres-Jardón R, Solt A, Reed W (2008) Systemic inflammation, endothelial dysfunction, and activation in clinically healthy children exposed to air pollutants. Inhal Toxicol 20, 499-506.
57. Maillard P, Fletcher E, Harvey D, Carmichael O, Reed B, Mungas D, DeCarli C (2011) White matter hyperintensity penumbra. Stroke 42, 1917-1922.
58. Barker R, Ashby EL, Wellington D, Barrow VM, Palmer JC, Kehoe PG, Esiri MM, Love S (2014) Pathophysiology of white matter perfusion in Alzheimer's disease and vascular dementia. Brain 137, 1524-1532.
59. Miyamoto N, Maki T, Pham LD, Hayakawa K, Seo JH, Mandeville JB, Kim KW, Lo EH, Arai K (2013) Oxidative stress interferes with white matter renewal after prolonged cerebral hypoperfusion in mice. Stroke 44, 3516-3521.
60. D'haeseleer M, Beelen R, Fierens Y, Cambron M, Vanbinst AM, Verborgh C, Derney J, DeKeyser J (2013) Cerebral hypoperfusion in multiple sclerosis is reversible and mediated by endothelin 1. Proc Natl Acad Sci U S A 110, 5654-5648.
61. Schreiber S, Bueche CZ, Garz C, Braun H (2013) Blood brain barrier breakdown as the standing point of cerebral small vessel disease? New insights from a rat model. Exp Transl Stroke Med 5, 4.
62. Calderón-Garcidueñas L, Solt AC, Henríquez-Roldán C, Torres-Jardón R, Nuse B, Herritt L, Villarreal-Calderón R, Stone I, García R, Brooks DM, González-Maciel A, Reynoso-Robles R, Delgado-Chávez R, Reed W (2008) 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 alphasynuclein in children and young adults. Toxicol Pathol 36, 289-310.
63. Chang Y, Lee JJ, Seo JH, Song HJ, Kim JH, Bae SJ, Ahn JH, Park SJ, Jeong KS, Kwon YJ, Kim SH, Kim Y (2010) Altered working memory process in the manganese-exposed brain. Neuroimage 53, 1279-1285.
64. Khan K, Wasserman GA, Liu X, Ahmed E, Parvez F, Slavkovich V, Levy D, Mey J, van Geen A, Graziano JH, Factor-Litvak P (2012) Manganese exposure from drinking water and children's academic achievement. Neurotoxicology 33, 91-97.
65. Xu H, Finkelstein DI, Adlard PA (2014) Interactions of metals and apolipoprotein E in Alzheimer's disease. Front Aging Neurosci 6, 121.
66. Guilarte TR (2013) Manganese neurotoxicity: New perspectives from behavioural, neuroimaging and neuropathological studies in human and non-human primates. Front Aging Neurosci 5, 23.
67. Guilarte TR, McGlothan JL, Degaonkar M, Chen MK, Barker PB, Syversen T, Schneider JS (2006) Evidence for cortical dysfunction and widespread manganese accumulation in the nonhuman primate brain following chronic manganese exposure: A1H-MRS and MRI study. Toxicol Sci 94, 351-358.
68. Calderón-Garcidueñas L, Serrano-Sierra A, Torres-Jardón R, Zhu H, Yuan Y, Smith D, Delgado-Chávez R, Cross JV, Medina-Cortina H, Kavanaugh M, Guilarte TR (2013) The impact of environmental metals in young urbanites' brains. Exp Toxicol Pathol 65, 503-511.
69. Calderón-Garcidueñas L, Vojdani A, Blaurock-Busch E, Busch Y, Friedle A, Franco-Lira M, Sarathi-Mukherjee P, Park S, Torres-Jardón R, D'Angiulli A (2015) 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, 1039-1058.
70. Kim J, Bhattachanee R, Kheirandish-Gozai L, Khalyfa A, Sans-Capdevila O, Tauman R, Gozai D (2010) Insulin sensitivity, serum lipids, and systemic inflammatory markers in school-aged obese and non-obese children. Int J Pediat 2010, 846098.
71. Dowd JB, Zaiacova A, Aiello E (2010) Predictors of inflammation in US children aged 3-16 years. Am J Prev Med 39, 314-320.
72. Tam CS, Cláment K, Baur LA, Tordjman J (2010) Obesity and low-grade inflammation:Apaediatric perspective. Obes Rev 11, 118-126.
73. Crespo AC, Silva B, Marques L, Marcelino E, Maruta C, Costa S, Timoteo A, Vilares A, Couto FS, Faustino P, Correia AP, Verdelho A, Porto G, Guerreiro M, Herrero A, Costa C, de Mendonc¸a A, Costa L, Martins M (2014) Genetic and biochemical markers in patients with Alzheimer's disease support a concerted systemic iron homeostasis dysregulation. Neurobiol Aging 35, 777-785.
74. Wong BX, Hung YH, Bush AI, Duce JA (2014) Metals and cholesterol: Two sides of the same coin in Alzheimer's disease pathology. Front Aging Neurosci 6, 91.
75. Gale SC, Gao L, Mikacenic C, Coyle SM, Rafaels N, Murray Dudenkov T, Madenspacher JH, Draper DW, Ge W, Aloor JJ, Azzam KM, Lai L, Blackshear PJ, Calvano SE, Barnes KC, Lowry SF, Corbett S, Wurfel MM, Fessler MB (2014) APOE4 is associated with enhanced in vivo innate immune responses in human subjects. J Allergy Immunol 134, 127-134.
76. Rohn TT (2014) Is apolipoprotein E4 an important risk factor for vascular dementia? Int J Clin Exp Pathol 7, 3504-3511.
77. Braak H, Del Tredeci K (2011) The pathological process underlying Alzheimer's disease in individuals under thirty. Acta Neuropathol 121, 171-181.
78. Braak H, Thal DR, Ghebremedhin E, Del Tredeci K (2011) Stages of the pathologic process in Alzheimer's disease: Age categories from 1-100 years. J Neuropathol Exp Neurol 70, 960-969.
79. Braak H, Del Tredeci K (2012) Where, when and in what form does sporadic Alzheimer's disease begin? Curr Opin Neurol 25, 708-714.
80. Braak H, Del Tredeci K (2013) Amyloid-β may be released from non-junctional varicosities of axons generated from abnormal tau-containing brainstem nuclei in sporadic Alzheimer's disease: A hypothesis. Acta Neuropathol 126, 303-306.
81. Braak H, Del Tredeci K (2013) Reply: The early pathological process in sporadic Alzheimer's disease. Acta Neuropathol 126, 615-618.
82. Del Tredeci K, Braak H (2013) Dysfunction of the locus-coeruleus- norepinephrine system and related circuitry in Parkinson's disease-related dementia. J Neurol Neurosurg Psychiatry 84, 774-783.
83. Calderón-Garcidueñas L, D'Angiulli A, Kulesza RJ, Torres-Jardón R, Romero L, Keefe S, Herritt L, Brooks DM, Avila-Ramirez J, Delgado-Chávez R, Medina-Cortina H, González-González LO (2011) Air pollution is associated with brainstem auditory nuclei pathology and delayed brainstem auditory evoked potentials. Int J Dev Neurosci 29, 365-375.
84. Rose SE, de Zubicaray GI, Greig I, Wang D, Galloway GJ, Chalk JB, Eagle SC, Semple J, Doddrell DM (1999) A 1H MRS study of probable Alzheimer's disease and normal aging: Implications for longitudinal monitoring of dementia progression. Magn Reson Imaging 17, 291-299.
85. Jessen F, Block W, Traber F, Keller E, Flacke S, Papassotiropoulos A (2000) Proton MR spectroscopy detects a relative increase of N-acetyl aspartate in the medial temporal lobe of patients with AD. Neurology 55, 684-688.
86. Chen SQ, Wang PJ, Ten GJ, Zhan W, Li MH, Zang FC (2009) Role of myo-inositol by magnetic resonance spectroscopy in early diagnosis of Alzheimer's disease in APP/PS1 transgenic mice. Dement Geriatr Cogn Disord 28, 558-566.
87. Westman E, Wahlund LO, Foy C, Poppe M, Cooper A, Murphy D, Spenger C, Lovestone S, Simmons A (2010) Combining MRI and MRS to distinguish between Alzheimer's disease and healthy controls. J Alzheimers Dis 22, 171-181.
88. Yang ZX, Huo SS, Cheng XF, Xu ZF, Cao Z, Zeng JX, Xiao YY, You KZ, Chen W, Liu YY, Wu RH (2012) Quantitative multivoxel proton MR spectroscopy study of the brain metabolites in patients with amnestic mild cognitive impairment: A pilot study. Neuroradiology 54, 451-458.
89. Schuff N, Zhu XP (2007) Imaging of mild cognitive impairment and early dementia. Br J Radiol 2, S109-S114.
90. Wolk DA, Dickerson BC, Alzheimer's Disease Neuroimaging, Initiative (2010) Apolipoprotein E (APOE) genotype has dissociable effects on memory and attentional-executive network function in Alzheimer's disease. Proc Natl Acad Sci U S A 107, 10256-10261.
91. Gao F, Parker PB (2014) Various MRS application tools for Alzheimer disease and mild cognitive impairment. AJNR Am J Neuroradiol 35, S4-S11.
92. Cross DJ, Anzai Y, Petrie EC, Martin N, Richards TL, Maravilla KR, Peskind ER, Minoshima S (2013) Loss of olfactory tract integrity affects cortical metabolism in the brain and olfactory regions in aging and mild cognitive impairment. J Nucl Med 54, 1278-1284.
93. Kjelvik G, Evensmoen HR, Brezova V, Håberg AK (2012) The human brain representation of odor identification. J Neurophysiol 108, 645-657.
94. Stäubli U, Ivy G, Lynch G (1984) Hippocampal denervation causes rapid forgetting of olfactory information in rats. Proc Natl Acad Sci U S A 81, 5885-5887.
95. Calderón-Garcidueñas L, Mora-Tiscareño A, Gómez-Garza G, Broadway J, Chapman S, Valencia-Salazar G, Jewells V, Maronpot RR, Henríquez-Roldán C, Pérez-Guillé B, Torres-Jardón R, Herrit L, Brooks D, Monroy ME, González-Maciel A, Reynoso-Robles R, Villarreal-Calderón R, Solt AC, Engle RW (2008) Air pollution, cognitive deficits and brain abnormalities:Apilot study with children and dogs. Brain Cogn 68, 117-127.
96. Calderón-Garcidueñas L, Engle R, Mora-Tiscareño A, Styner M, Gomez-Garza G, Zhu H, Jewells V, Torres-Jardón R, Romero L, Monroy-Acosta ME, Bryant C, González-González LO, Medina-Cortina H, D'Angiulli A (2011) Exposure to severe urban pollution influences cognitive outcomes, brain volume and systemic inflammation in clinically healthy children. Brain Cogn 77, 345-355.
97. Palouzier-Paulignan B, Lacroix MC, Aimé P, Baly C, Caillol M, Congar P, Julliard AK, Tucker K, Fadool DA (2012) Olfaction under metabolic influences. Chem Senses 37, 769-797.
98. Santos DV, Reiter ER, Dinardo LJ, Costanzo RM (2004) Hazardous events associated with impaired olfactory function. Arch Otolaryngol Head Neck Surg 130, 317-319.
99. Dean DC, 3rd, Jerskey BA, Chen K, Protas H, Thiyyagura P, Roontiva A, O'Muircheartaigh J, Dirks H, Waskiewicz N, Lehman K, Siniard AL, Turk MN, Hua X, Madsen SK, Thompson PM, Fleisher AS, Huentelman MJ, Deoni SC, Reiman EM (2014) Brain differences in infants at differential genetic risk for late-onset Alzheimer disease: A cross-sectional imaging study. JAMA Neurol 71, 11-22.
100. Dean DC 3rd, O'Muircheartaigh J, Dirks H, Waskiewicz N, Walker L, Doemberg E, Pirvatinsky I, Deoni SC (2014) Characterizing longitudinal white matter development during early childhood. Brain Struct Funct, doi: 10.1007/s00429-014-0763-3
101. Calderón-Garcidueñas L, Torres-Jardón R (2012) Air pollution, socioeconomic status and children's cognition in megacities: The Mexico City scenario. Front Psycho 3, 217.
102. Steinberg L (2013) The influence of neuroscience on US Supreme Court decisions about adolescents' criminal culpability. Nat Rev Neurosci 14, 513-518.
103. Emerson E, Halpin S (2013) Anti-social behaviour and police contact among 13 to 15 year old English adolescents with and without mild/moderate intellectual disability. J Appl Res Intellect Disabil 26, 362-369.
104. Newsome J, Sullivan CJ (2014) Resilience and vulnerability in adolescents: Genetic influences on differential response to risk for delinquency. J Youth Adolesc 43, 1080-1095.
105. Borghesani PR, Johnson LC, Shelton AL, Peskind ER, Aylward EH, Schellenberg GD, Cherrier MM (2008) Altered medial temporal lobe responses during visuospatial encoding in healthy APOE4 carriers. Neurobiol Aging 29, 981-991.
106. Filbey FM, Chen G, Sunderland T, Cohen RM (2010) Failing compensatory mechanisms duringworking memory in older apolipoprotein E-epsilon4 healthy adults. Brain Imag Behav 4, 177-188.
107. Han SD, Bondi MW (2008) Revision of the apolipoprotein E compensatory mechanism recruitment hypothesis. Alzheimers Dement 4, 251-254.
108. Castellani RJ, Perry G (2014) The complexities of the pathology-pathogenesis relationship in Alzheimer disease. Biochem Pharmacol 88, 671-676.
109. Calderón-Garcidueñas L, Mora-Tiscareño A, Franco-Lira M, Cross JV, Engle R, Aragón-Flores M, Gómez-Garza G, Jewells V, Medina-Cortina H, Solorio E, Chao CK, Zhu H, Mukherjee PS, Ferreira-Azevedo L, Torres-Jardón R, D'Angiulli A (2013) Flavonol-rich dark cocoa significantly decreases plasma endothelin-1 and improves cognition in urban children. Front Pharmacol 4, 104.