Cumulative lead exposure is associated with reduced olfactory recognition performance in elderly men: The Normative Aging Study

NeuroToxicology

Volumn 49, Issue , 2015, Pages 158-164

  Grashow, Rachel ^a,b   Sparrow, David ^c,d   Hu, Howard ^e   Weisskopf, Marc G ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b Northeastern University   (United States)

^c BOSTON UNIVERSITY   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Aging; ApoE; Bone lead; GSTP1; HFE; Olfaction

Indexed keywords

APOLIPOPROTEIN E; GLUTATHIONE TRANSFERASE P1; HFE PROTEIN; LEAD; TRANSFERRIN; GSTP1 PROTEIN, HUMAN;

AGE; AGED; ARTICLE; ASSESSMENT OF HUMANS; BONE LEVEL; COGNITION; COHORT ANALYSIS; COMMUNITY LIVING; CONTROLLED STUDY; CORRELATION ANALYSIS; EDUCATIONAL STATUS; ENVIRONMENTAL EXPOSURE; GENOTYPE; HEMOCHROMATOSIS; HUMAN; IRON METABOLISM; LINEAR REGRESSION ANALYSIS; MALE; MINI MENTAL STATE EXAMINATION; PATELLA; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SMELLING; SMOKING; TIBIA; UNIVERSITY OF PENNSYLVANIA SMELL IDENTIFICATION TEST; X RAY FLUORESCENCE; AGING; BONE; CHEMICALLY INDUCED; CHEMISTRY; COGNITION DISORDERS; DRUG EFFECTS; GENETICS; MENTAL HEALTH; METABOLISM; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; OLFACTION DISORDERS; RECOGNITION; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; APOLIPOPROTEINS E; BONE AND BONES; COGNITION DISORDERS; COHORT STUDIES; ENVIRONMENTAL EXPOSURE; GENOTYPE; GLUTATHIONE S-TRANSFERASE PI; HUMANS; LEAD; MALE; MENTAL STATUS SCHEDULE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; OLFACTION DISORDERS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOGNITION (PSYCHOLOGY); RISK FACTORS;

EID: 84934766696     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2015.06.006     Document Type: Article

References (79)

1. Antunes M.B., Bowler R., Doty R.L. San Francisco/Oakland Bay Bridge Welder Study: olfactory function. Neurology 2007, 69:1278-1284.
2. Aro A.C., Todd A.C., Amarasiriwardena C., Hu H. Improvements in the calibration of 109Cd K X-ray fluorescence systems for measuring bone lead in vivo. Phys. Med. Biol. 1994, 39:2263-2271.
3. Bandeen-Roche K., Glass T.A., Bolla K.I., Todd A.C., Schwartz B.S. Cumulative lead dose and cognitive function in older adults. Epidemiology 2009, 20:831-839.
4. Bell B., Rose C.L., Damon A. The Veterans Administration longitudinal study of healthy aging. Gerontologist 1966, 6:179-184.
5. Bolla K.I., Schwartz B.S., Stewart W., Rignani J., Agnew J., Ford D.P. Comparison of neurobehavioral function in workers exposed to a mixture of organic and inorganic lead and in workers exposed to solvents. Am. J. Ind. Med. 1995, 27:231-246.
6. Calderon-Garciduenas 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, 62:91-102.
7. Caruso A., Lucchini R., Toffoletto F., Porro S., Moroni P., Mascagni P. Study of the olfactory function of a group of workers with significant lead exposure. Giornale italiano di medicina del lavoro ed ergonomia 2007, 29:460-463.
8. Chettle D., Arnold M., Aro A., Fleming D., Kondrashov V., McNeill F., et al. An agreed statement on calculating lead concentration and uncertainty in XRF in vivo bone lead analysis. Appl. Radiat. Isot. 2003, 58:603-605.
9. Claus Henn B., Kim J., Wessling-Resnick M., Tellez-Rojo M.M., Jayawardene I., Ettinger A.S., et al. Associations of iron metabolism genes with blood manganese levels: a population-based study with validation data from animal models. Environ. Health. 2011, 10:97.
10. Coon S., Stark A., Peterson E., Gloi A., Kortsha G., Pounds J., et al. Whole-body lifetime occupational lead exposure and risk of Parkinson's disease. Environ. Health Perspect. 2006, 114:1872-1876.
11. Dick R.B., Steenland K., Krieg E.F., Hines C.J. Evaluation of acute sensory-motor effects and test sensitivity using termiticide workers exposed to chlorpyrifos. Neurotoxicol. Teratol. 2001, 23:381-393.
12. Doty R.L. Influence of age and age-related diseases on olfactory function. Ann. N. Y. Acad. Sci. 1989, 561:76-86.
13. Doty R.L., Frye R.E., Agrawal U. Internal consistency reliability of the fractionated and whole University of Pennsylvania smell identification test. Percept. Psychophys. 1989, 45:381-384.
14. Doty R.L., Shaman P., Dann M. Development of the University of Pennsylvania smell identification test: a standardized microencapsulated test of olfactory function. Physiol. Behav. 1984, 32:489-502.
15. Eaton J.W., Qian M. Molecular bases of cellular iron toxicity. Free Radic. Biol. Med. 2002, 32:833-840.
16. Eum K.D., Seals R.M., Taylor K.M., Grespin M., Umbach D.M., Hu H., et al. Modification of the association between lead exposure and amyotrophic lateral sclerosis by iron and oxidative stress related gene polymorphisms. Amyotroph. Later. Scler. Frontotemporal Degener. 2014, 1-8.
17. Eum K.D., Wang F.T., Schwartz J., Hersh C.P., Kelsey K., Wright R.O., et al. Modifying roles of glutathione S-transferase polymorphisms on the association between cumulative lead exposure and cognitive function. Neurotoxicology 2013, 39:65-71.
18. Finkel D., Reynolds C.A., Larsson M., Gatz M., Pedersen N.L. Both odor identification and ApoE-epsilon4 contribute to normative cognitive aging. Psychol. Aging 2011, 26:872-883.
19. Gietzen D.W., Woolley D.E. Acetylcholinesterase activity in the brain of rat pups and dams after exposure to lead via the maternal water supply. Neurotoxicology 1984, 5:235-246.
20. Gorell J.M., Johnson C.C., Rybicki B.A., Peterson E.L., Kortsha G.X., Brown G.G., et al. Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease. Neurotoxicology 1999, 20:239-247.
21. Grashow R., Miller M.W., McKinney A., Nie L.H., Sparrow D., Hu H., et al. Lead exposure and fear-potentiated startle in the VA Normative Aging Study: a pilot study of a novel physiological approach to investigating neurotoxicant effects. Neurotoxicol. Teratol. 2013, 38:21-28.
22. Grashow R., Spiro A., Taylor K.M., Newton K., Shrairman R., Landau A., et al. Cumulative lead exposure in community-dwelling adults and fine motor function: comparing standard and novel tasks in the VA normative aging study. Neurotoxicology 2013, 35:154-161.
23. Green A.J., Cervantez M., Graves L.V., Morgan C.D., Murphy C. Age apolipoprotein E epsilon4 effects on neural correlates of odor memory. Behav. Neurosci. 2013, 127:339-349.
24. Hawkes C. Olfaction in neurodegenerative disorder. Adv. Otorhinolaryngol. 2006, 63:133-151.
25. Hayes J.D., Strange R.C. Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 2000, 61:154-166.
26. Hu H., Aro A., Payton M., Korrick S., Sparrow D., Weiss S.T., et al. The relationship of bone and blood lead to hypertension. The Normative Aging Study. JAMA 1996, 275:1171-1176.
27. Hu H., Rabinowitz M., Smith D. Bone lead as a biological marker in epidemiologic studies of chronic toxicity: conceptual paradigms. Environ. Health Perspect. 1998, 106:1-8.
28. Huang X., Moir R.D., Tanzi R.E., Bush A.I., Rogers J.T. Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann. N. Y. Acad. Sci. 2004, 1012:153-163.
29. Katzenschlager R., Zijlmans J., Evans A., Watt H., Lees A.J. Olfactory function distinguishes vascular parkinsonism from Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 2004, 75:1749-1752.
30. Kim J., Buckett P.D., Wessling-Resnick M. Absorption of manganese and iron in a mouse model of hemochromatosis. PLOS ONE 2013, 8:6494-6504.
31. Kim S., Hyun J., Kim H., Kim Y., Kim E., Jang J., et al. Effects of lead exposure on nitric oxide-associated gene expression in the olfactory bulb of mice. Biol. Trace Elem. Res. 2011, 142:683-692.
32. Kranick S.M., Duda J.E. Olfactory dysfunction in Parkinson's disease. Neurosignals 2008, 16:35-40.
33. Lim S.Y., Doherty J.D., McBride K., Miller-Ihli N.J., Carmona G.N., Stark K.D., et al. Lead exposure and (n-3) fatty acid deficiency during rat neonatal development affect subsequent spatial task performance and olfactory discrimination. J. Nutr. 2005, 135:1019-1026.
34. Louis E.D., Marder K., Tabert M.H., Devanand D.P. Mild Parkinsonian signs are associated with lower olfactory test scores in the community-dwelling elderly. Mov. Disord. 2008, 23:524-530.
35. Lucchini R.G., Guazzetti S., Zoni S., Donna F., Peter S., Zacco A., et al. Tremor, olfactory and motor changes in Italian adolescents exposed to historical ferro-manganese emission. Neurotoxicology 2012, 33:687-696.
36. Mariani S., Ventriglia M., Simonelli I., Spalletta G., Bucossi S., Siotto M., et al. Effects of hemochromatosis and transferrin gene mutations on peripheral iron dyshomeostasis in mild cognitive impairment and Alzheimer's and Parkinson's diseases. Front. Aging Neurosci. 2013, 5:37.
37. Mollenhauer B., Trautmann E., Sixel-Doring F., Wicke T., Ebentheuer J., Schaumburg M., et al. Nonmotor and diagnostic findings in subjects with de novo Parkinson disease of the DeNoPa cohort. Neurology 2013, 81:1226-1234.
38. Murphy C., Gilmore M.M., Seery C.S., Salmon D.P., Lasker B.R. Olfactory thresholds are associated with degree of dementia in Alzheimer's disease. Neurobiol. Aging 1990, 11:465-469.
39. Namekata K., Oyama F., Imagawa M., Ihara Y. Human transferrin (Tf): a single mutation at codon 570 determines Tf C1 or Tf C2 variant. Hum. Genet. 1997, 100:457-458.
40. Nandar W., Connor J.R. HFE gene variants affect iron in the brain. J. Nutr. 2011, 141:729S-739S.
41. Olofsson J.K., Nordin S., Wiens S., Hedner M., Nilsson L.G., Larsson M. Odor identification impairment in carriers of ApoE-varepsilon4 is independent of clinical dementia. Neurobiol. Aging 2010, 31:567-577.
42. Park S.K., O'Neill M.S., Wright R.O., Hu H., Vokonas P.S., Sparrow D., et al. HFE genotype, particulate air pollution, and heart rate variability: a gene-environment interaction. Circulation 2006, 114:2798-2805.
43. Payton M., Riggs K.M., Spiro A., Weiss S.T. Hu H. Relations of bone and blood lead to cognitive function: the VA Normative Aging Study. Neurotoxicol. Teratol. 1998, 20:19-27.
44. Poirier J., Miron J., Picard C., Gormley P., Theroux L., Breitner J., et al. Apolipoprotein E and lipid homeostasis in the etiology and treatment of sporadic Alzheimer's disease. Neurobiol. Aging 2014, 35(Suppl. 2):S3-S10.
45. Richardson J.R., Roy A., Shalat S.L., von Stein R.T., Hossain M.M., Buckley B., et al. Elevated serum pesticide levels and risk for Alzheimer disease. JAMA Neurol. 2014.
46. Richardson J.R., Shalat S.L., Buckley B., Winnik B., O'Suilleabhain P., Diaz-Arrastia R., et al. Elevated serum pesticide levels and risk of Parkinson disease. Arch. Neurol. 2009, 66:870-875.
47. Rose C.S., Heywood P.G., Costanzo R.M. Olfactory impairment after chronic occupational cadmium exposure. J. Occup. Med. 1992, 34:600-605.
48. Ross G.W., Abbott R.D., Petrovitch H., Tanner C.M., White L.R. Pre-motor features of Parkinson's disease: the Honolulu-Asia Aging Study experience. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S199-S202.
49. Royall D.R., Chiodo L.K., Polk M.S., Jaramillo C.J. Severe dysosmia is specifically associated with Alzheimer-like memory deficits in nondemented elderly retirees. Neuroepidemiology 2002, 21:68-73.
50. Samson F.E., Nelson S.R. The aging brain, metals and oxygen free radicals. Cell. Mol. Biol. (Noisy-le-grand) 2000, 46:699-707.
51. Sanders T., Liu Y., Buchner V., Tchounwou P.B. Neurotoxic effects and biomarkers of lead exposure: a review. Rev. Environ. Health. 2009, 24:15-45.
52. Scheuhammer A.M., Cherian M.G. The regional distribution of lead in normal rat brain. Neurotoxicology 1982, 3:85-92.
53. Schwartz B.S., Bolla K.I., Stewart W., Ford D.P., Agnew J., Frumkin H. Decrements in neurobehavioral performance associated with mixed exposure to organic and inorganic lead. Am. J. Epidemiol. 1993, 137:1006-1021.
54. Schwartz B.S., Doty R.L., Monroe C., Frye R., Barker S. Olfactory function in chemical workers exposed to acrylate and methacrylate vapors. Am. J. Public Health 1989, 79:613-618.
55. Schwartz B.S., Ford D.P., Bolla K.I., Agnew J., Rothman N., Bleecker M.L. Solvent-associated decrements in olfactory function in paint manufacturing workers. Am. J. Ind. Med. 1990, 18:697-706.
56. Seo H.S., Jeon K.J., Hummel T., Min B.C. Influences of olfactory impairment on depression, cognitive performance, and quality of life in Korean elderly. Eur. Arch. Otorhinolaryngol. 2009, 266:1739-1745.
57. Shih R.A., Glass T.A., Bandeen-Roche K., Carlson M.C., Bolla K.I., Todd A.C., et al. Environmental lead exposure and cognitive function in community-dwelling older adults. Neurology 2006, 67:1556-1562.
58. Sirivarasai J., Wananukul W., Kaojarern S., Chanprasertyothin S., Thongmung N., Ratanachaiwong W., et al. Association between inflammatory marker, environmental lead exposure, and glutathione S-transferase gene. Biomed. Res. Int. 2013, 2013:474963.
59. Sohrabi H.R., Bates K.A., Weinborn M.G., Johnston A.N., Bahramian A., Taddei K., et al. Olfactory discrimination predicts cognitive decline among community-dwelling older adults. Transl. Psychiatry 2012, 2:e118.
60. Sulkowski W.J., Rydzewski B., Miarzynska M. Smell impairment in workers occupationally exposed to cadmium. Acta Otolaryngol. 2000, 120:316-318.
61. Sunderman F.W. Nasal toxicity, carcinogenicity, and olfactory uptake of metals. Ann. Clin. Lab. Sci. 2001, 31:3-24.
62. Swan G.E., Carmelli D. Impaired olfaction predicts cognitive decline in nondemented older adults. Neuroepidemiology 2002, 21:58-67.
63. Takeda A., Baba T., Kikuchi A., Hasegawa T., Sugeno N., Konno M., et al. Olfactory dysfunction and dementia in Parkinson's disease. J. Parkinson's Dis. 2014, 4:181-187.
64. Teter B., Raber J., Nathan B., Crutcher K.A. The presence of apoE4, not the absence of apoE3, contributes to AD pathology. J. Alzheimer's Dis. 2002, 4:155-163.
65. Thompson M.D., Knee K., Golden C.J. Olfaction in persons with Alzheimer's disease. Neuropsychol. Rev. 1998, 8:11-23.
66. Todorich B.M., Connor J.R. Redox metals in Alzheimer's disease. Ann. N. Y. Acad. Sci. 2004, 1012:171-178.
67. van Wijngaarden E., Campbell J.R., Cory-Slechta D.A. Bone lead levels are associated with measures of memory impairment in older adults. Neurotoxicology 2009, 30:572-580.
68. Wang F.T., Hu H., Schwartz J., Weuve J., Spiro A.S., Sparrow D., et al. Modifying effects of the HFE polymorphisms on the association between lead burden and cognitive decline. Environ. Health Perspect. 2007, 115:1210-1215.
69. Wang J., Eslinger P.J., Doty R.L., Zimmerman E.K., Grunfeld R., Sun X., et al. Olfactory deficit detected by fMRI in early Alzheimer's disease. Brain Res. 2010, 1357:184-194.
70. Weisskopf M.G., Proctor S.P., Wright R.O., Schwartz J., Spiro A., Sparrow D., et al. Cumulative lead exposure and cognitive performance among elderly men. Epidemiology 2007, 18:59-66.
71. Weisskopf M.G., Weuve J., Nie H., Saint-Hilaire M.H., Sudarsky L., Simon D.K., et al. Association of cumulative lead exposure with Parkinson's disease. Environ. Health Perspect. 2010, 118:1609-1613.
72. Weisskopf M.G., Wright R.O., Schwartz J., Spiro A., Sparrow D., Aro A., et al. Cumulative lead exposure and prospective change in cognition among elderly men: the VA Normative Aging Study. Am. J. Epidemiol. 2004, 160:1184-1193.
73. Weuve J., Korrick S.A., Weisskopf M.G., Ryan L.M., Schwartz J., Nie H., et al. Cumulative exposure to lead in relation to cognitive function in older women. Environ. Health Perspect. 2009, 117:574-580.
74. White L.D., Cory-Slechta D.A., Gilbert M.E., Tiffany-Castiglioni E., Zawia N.H., Virgolini M., et al. New and evolving concepts in the neurotoxicology of lead. Toxicol. Appl. Pharmacol. 2007, 225:1-27.
75. Widmer H.R., Vedder H., Schlumpf M., Lichtensteiger W. Concurrent changes in regional cholinergic parameters and nest odor preference in the early postnatal rat after lead exposure. Neurotoxicology 1992, 13:615-624.
76. Wilker E., Korrick S., Nie L.H., Sparrow D., Vokonas P., Coull B., et al. Longitudinal changes in bone lead levels: the VA Normative Aging Study. J. Occup. Environ. Med. 2011, 53:850-855.
77. Wright R.O., Silverman E.K., Schwartz J., Tsaih S.W., Senter J., Sparrow D., et al. Association between hemochromatosis genotype and lead exposure among elderly men: the normative aging study. Environ. Health Perspect. 2004, 112:746-750.
78. Wright R.O., Tsaih S.W., Schwartz J., Spiro A., McDonald K., Weiss S.T., et al. Lead exposure biomarkers and mini-mental status exam scores in older men. Epidemiology 2003, 14:713-718.
79. Xu H., Finkelstein D.I., Adlard P.A. Interactions of metals and apolipoprotein E in Alzheimer's disease. Front. Aging Neurosci. 2014, 6:121.