Odor identification impairment in carriers of ApoE-e{open}4 is independent of clinical dementia

Neurobiology of Aging

Volumn 31, Issue 4, 2010, Pages 567-577

  Olofsson, Jonas K ^a,b,c   Nordin, Steven ^a,d   Wiens, Stefan ^b,c   Hedner, Margareta ^b,c   Nilsson, Lars Göran ^b,c   Larsson, Maria ^b,c  

^a UMEÅ UNIVERSITY   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c Stockholm Brain Institute   (Sweden)

^d SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Aging; Alzheimer's disease; ApoE; Odor identification; Olfaction

Indexed keywords

APOLIPOPROTEIN E2; APOLIPOPROTEIN E4;

ADULT; AGED; AGING; ALLERGY; ALZHEIMER DISEASE; ARTICLE; ASTHMA; CARDIOVASCULAR DISEASE; COGNITION; COLD; DEMENTIA; DIABETES MELLITUS; EDUCATION; EYE DISEASE; FEMALE; HEAD INJURY; HEALTH STATUS; HUMAN; INFLUENZA; LINGUISTICS; MAJOR CLINICAL STUDY; MALE; MENTAL DISEASE; MINI MENTAL STATE EXAMINATION; NEUROLOGIC DISEASE; NOSE CONGESTION; NOSE DISEASE; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SMELLING; SMELLING DISORDER; SMOKING; THROAT DISEASE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; APOLIPOPROTEIN E4; COHORT STUDIES; DISABILITY EVALUATION; DISEASE PROGRESSION; DNA MUTATIONAL ANALYSIS; FEMALE; GENETIC MARKERS; HETEROZYGOTE; HUMANS; MALE; MASS SCREENING; MIDDLE AGED; OLFACTION DISORDERS; SMELL; TIME FACTORS;

EID: 77049098110     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2008.05.019     Document Type: Article

References (76)

1. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. 4. Cell proliferation and migration in anterior forebrain, with special reference to persisting neurogenesis in olfactory bulb. Journal of Comparative Neurology 1969, 137(4):433-457.
2. Bäckman L., Jones S., Berger A.K., Laukka E.J., Small B.J. Cognitive impairment in preclinical Alzheimer's disease: a meta-analysis. Neuropsychology 2005, 19(4):520-531.
3. Bacon A.W., Bondi M.W., Salmon D.P., Murphy C. Very early changes in olfactory functioning due to Alzheimer's disease and the role of apolipoprotein E in olfaction. Annals of the New York Academy of Science 1998, 855:723-731.
4. Bende M., Nordin S. Perceptual learning in olfaction: professional wine tasters versus controls. Physiology & Behavior 1997, 62(5):1065-1070.
5. Calhoun-Haney R., Murphy C. Apolipoprotein epsilon 4 is associated with more rapid decline in odor identification than in odor threshold or Dementia Rating Scale scores. Brain and Cognition 2005, 58(2):178-182.
6. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261(5123):921-923.
7. Corwin J., Loury M., Gilbert A.N. Workplace, age, and sex as mediators of olfactory function-data from the National Geographic Smell Survey. Journals of Gerontology Series B-Psychological Sciences and Social Sciences 1995, 50(4):179-186.
8. Deary I.J., Whiteman M.C., Pattie A., Starr J.M., Hayward C., Wright A.F., Carothers A., Whalley L.J. Cognitive change and the APOE epsilon 4 allele. Nature 2002, 418(6901):932.
9. Doty R.L., Shaman P., Applebaum S.L., Giberson R., Siksorski L., Rosenberg L. Smell identification ability-changes with age. Science 1984, 226(4681):1441-1443.
10. Doty R.L., Reyes P., Gregor T. Olfactory dysfunction in Alzheimers-disease. Chemical Senses 1986, 11(4):595.
11. Doty R.L., Reyes P.F., Gregor T. Presence of both odor identification and detection deficits in Alzheimers-disease. Brain Research Bulletin 1987, 18(5):597-600.
12. Diagnostic and Statistical Manual of Mental Disorders 1994, American Psychiatric Association, Washington, DC. 4th ed.
13. Dureman I., Sälde H. Psykometriska och experimental-psykologiska metoder för klinisk tillämpning 1959, Almqvist och Wiksell, Uppsala, Sweden.
14. Eggertsen G., Tegelman R., Ericsson S., Angelin B., Berglund L. Apolipoprotein-E polymorphism in a healthy Swedish population-variation of allele frequency with age and relation to serum-lipid concentrations. Clinical Chemistry 1993, 39(10):2125-2129.
15. Enwere E., Shingo T., Gregg C., Fujikawa H., Ohta S., Weiss S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. Journal of Neuroscience 2004, 24(38):8354-8365.
16. Esiri M.M., Wilcock G.K. The olfactory bulbs in Alzheimers-disease. Journal of Neurology Neurosurgery and Psychiatry 1984, 47(1):56-60.
17. Folstein M.F., Folstein S.E., Mchugh P.R. Mini-mental state-practical method for grading cognitive state of patients for clinician. Journal of Psychiatric Research 1975, 12(3):189-198.
18. Gilbert P.E., Murphy C. Differences between recognition memory and remote memory for olfactory and visual stimuli in nondemented elderly individuals genetically at risk for Alzheimer's disease. Experimental Gerontology 2004, 39(3):433-441.
19. Gilbert P.E., Murphy C. The effect of the ApoE epsilon 4 allele on recognition memory for olfactory and visual stimuli in patients with pathologically confirmed Alzheimer's disease, probable Alzheimer's disease, and healthy elderly controls. Journal of Clinical and Experimental Neuropsychology 2004, 26(6):779-794.
20. Gilbert P.E., Pirogovsky E., Ferdon S., Murphy C. The effects of normal aging on source memory for odors. The Journals of Gerontology 2006, 61(1):58-60.
21. Graves A.B., Bowen J.D., Rajaram L., McCormick W.C., McCurry S.M., Schellenberg G.D., Larson E.B. Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology 1999, 53(7):1480-1487.
22. Handley O.J., Morrison C.M., Miles C., Bayer A.J. ApoE gene and familial risk of Alzheimer's disease as predictors of odour identification in older adults. Neurobiology of Aging 2006, 27(10):1425-1430.
23. Kaplan M.S., Hinds J.W. Neurogenesis in adult rat-electron-microscopic analysis of light autoradiographs. Science 1977, 197(4308):1092-1094.
24. Kovacs T., Cairns N.J., Lantos P.L. Beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer's disease. Neuropathology and Applied Neurobiology 1999, 25(6):481-491.
25. Kovacs T., Cairns N.J., Lantos P.L. Olfactory centres in Alzheimer's disease: olfactory bulb is involved in early Braak's stages. Neuroreport 2001, 12(2):285-288.
26. Kuhn H.G., DickinsonAnson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. Journal of Neuroscience 1996, 16(6):2027-2033.
27. Larsson M., Bäckman L. Modality memory across the adult life span: evidence for selective age-related olfactory deficits. Experimental Aging Research 1998, 24(1):63-82.
28. Larsson M., Bäckman L. Age-related differences in episodic odour recognition: the role of access to specific odour names. Memory 1997, 5(3):361-378.
29. Larsson M., Bäckman L. Semantic mediation of age-related deficits in episodic recognition of common odors. Olfaction and Taste Xii 1998, 855:675-680.
30. Larsson M., Semb H., Winblad B., Amberla K., Wahlund L.O., Bäckman L. Odor identification in normal aging and early Alzheimer's disease: effects of retrieval support. Neuropsychology 1999, 13(1):47-53.
31. Larsson M., Finkel D., Pedersen N.L. Odor identification: influences of age, gender, cognition, and personality. Journals of Gerontology Series B-Psychological Sciences and Social Sciences 2000, 55(5):304-310.
32. Larsson M., Nilsson L.G., Olofsson J.K., Nordin S. Demographic and cognitive predictors of cued odor identification: evidence from a population-based study. Chemical Senses 2004, 29(6):547-554.
33. Larsson M., Öberg C., Bäckman L. Odor identification in old age: demographic, sensory and cognitive correlates. Aging Neuropsychology and Cognition 2005, 12(3):231-244.
34. Larsson M., Öberg C., Bäckman L. Recollective experience in odor recognition: influences of adult age and familiarity. Psychological Research-Psychologische Forschung 2006, 70(1):68-75.
35. Mahley R.W. Apolipoprotein-E-cholesterol transport protein with expanding role in cell biology. Science 1988, 240(4852):622-630.
36. Masliah E., Mallory M., Veinbergs I., Miller A., Samuel W. Alterations in apolipoprotein E expression during aging and neurodegeneration. Progress in Neurobiology 1996, 50(5-6):493-503.
37. Morgan C.D., Murphy C. Olfactory event-related potentials in Alzheimer's disease. Journal of the International Neuropsychological Society 2002, 8(6):753-763.
38. Murman D.L., Foster N.L., Kilgore S.P., McDonagh C.A., Fink J.K. Apolipoprotein E and Alzheimer's disease: strength of association is related to age at onset. Dementia (Basel, Switzerland) 1996, 7(5):251-255.
39. Murphy C., Bacon A.W., Bondi M.W., Salmon D.P. Apolipoprotein E status is associated with odor identification deficits in nondemented older persons. Annals of the New York Academy of Sciences 1998, 855:744-750.
40. Murphy C., Nordin S., Jinich S. Very early decline in recognition memory for odors in Alzheimer's disease. Aging Neuropsychology and Cognition 1999, 6(3):229-240.
41. Nathan B.P., Jiang Y., Wong G.K., Shen F., Brewer G.J., Struble R.G. Apolipoprotein E4 inhibits, and apolipoprotein E3 promotes neurite outgrowth in cultured adult mouse cortical neurons through the low-density lipoprotein receptor-related protein. Brain Research 2002, 928(1-2):96-105.
42. Nathan B.P., Yost J., Litherland M.T., Struble R.G., Switzer P.V. Olfactory function in apoE knockout mice. Behavioural Brain Research 2004, 150(1-2):1-7.
43. Nathan B.P., Nisar R., Short J., Randall S., Grissom E., Griffin G., Switzer P.V., Struble R.G. Delayed olfactory nerve regeneration in ApoE-deficient mice. Brain Research 2005, 1041(1):87-94.
44. Nathan B.P., Nannapaneni S., Gairhe S., Nwosu I., Struble R.G. The distribution of apolipoprotein E in mouse olfactory epithelium. Brain Research 2007, 1137(1):78-83.
45. Nilsson L.G., Bäckman L., Erngrund K., Nyberg L., Adolfsson R., Bucht G., Karlsson S., Widing M., Winblad B. The Betula prospective cohort study: memory, health and aging. Aging Neuropsychology and Cognition 1997, 4(1):1-32.
46. Nilsson E., Fastbom J., Wahlin A. Cognitive functioning in a population-based sample of very old non-demented and non-depressed persons: the impact of diabetes. Archives of Gerontology and Geriatrics 2002, 35(2):95-105.
47. Nilsson L.G., Adolfsson R., Bäckman L., de Frias C.M., Molander B., Nyberg L. Betula: a prospective cohort study on memory, health and aging. Aging Neuropsychology and Cognition 2004, 11(2-3):134-148.
48. Nilsson L.G., Adolfsson R., Bäckman L., Cruts M., Nyberg L., Small B.J., Van Broeckoven C. The influence of APOE status on episodic and semantic memory: data from a population-based study. Neuropsychology 2006, 20(6):645-657.
49. Nordin S., Murphy C. Odor memory in normal aging and Alzheimer's disease. Olfaction and Taste Xii 1998, 855:686-693.
50. Nordin S., Almkvist O., Berglund B., Wahlund L.O. Olfactory dysfunction for pyridine and dementia progression in Alzheimer disease. Archives of Neurology 1997, 54(8):993-998.
51. Nordin S., Brämerson A., Liden E., Bende M. The Scandinavian Odor-Identification Test: development, reliability, validity and normative data. Acta Oto-Laryngologica 1998, 118(2):226-234.
52. Nyberg L., Maitland S.B., Rönnlund M., Bäckman L., Dixon R.A., Wahlin A., Nilsson L.G. Selective adult age differences in an age-invariant multifactor model of declarative memory. Psychology and Aging 2003, 18(1):149-160.
53. Öberg C., Larsson M., Bäckman L. Differential sex effects in olfactory functioning: the role of verbal processing. Journal of the International Neuropsychological Society 2002, 8(5):691-698.
54. Poirier J., Davignon J., Bouthillier D., Kogan S., Bertrand P., Gauthier S. Apolipoprotein E polymorphism and Alzheimer's disease. Lancet 1993, 342(8873):697-699.
55. Riley K.P., Snowdon D.A., Saunders A.M., Roses A.D., Mortimer J.A., Nanayakkara N. Cognitive function and apolipoprotein E in very old adults: findings from the Nun Study. The Journals of Gerontology 2000, 55(2):69-75.
56. Rönnlund M., Nyberg L., Bäckman L., Nilsson L.G. Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychology and Aging 2005, 20(1):3-18.
57. Schiffman S.S. Taste and smell in disease (first of two parts). The New England Journal of Medicine 1983, 308(21):1275-1279.
58. Schiffman S.S. Taste and smell in disease (second of two parts). The New England Journal of Medicine 1983, 308(22):1337-1343.
59. Schiffman S., Pasternak M. Decreased discrimination of food odors in the elderly. Journal of Gerontology 1979, 34:73-79.
60. Schiffman S.S., Moss J., Erickson R.P. Thresholds of food odors in the elderly. Experimental Aging Research 1976, 2:389-398.
61. Serby M. Olfaction and Alzheimers-Disease. Progress in Neuro-psychopharmacology & Biological Psychiatry 1986, 10(3-5):579-586.
62. Ship J.A., Weiffenbach J.M. Age, gender, medical-treatment, and medication effects on smell identification. Journals of Gerontology 1993, 48(1):26-32.
63. Ship J.A., Pearson J.D., Cruise L.J., Brant L.J., Metter E.J. Longitudinal changes in smell identification. Journals of Gerontology Series A-Biological Sciences and Medical Sciences 1996, 51(2):86-91.
64. Smith J.D. Apolipoproteins and aging: emerging mechanisms. Ageing Research Reviews 2002, 1(3):345-365.
65. Stevens J.C., Cain W.S. Old-age deficits in the sense of smell as gauged by thresholds, magnitude matching, and odor identification. Psychology and Aging 1987, 2(1):36-42.
66. Struble R.G., Short J., Ghobrial M., Nathan B.P. Apolipoprotein E immunoreactivity in human and mouse olfactory bulb. Neuroscience Letters 1999, 267(2):137-140.
67. Tabert M.H., Liu X.H., Doty R.L., Serby M., Zamora D., Pelton G.H., Marder K., Albers M.W., Stern Y., Devanand D.P. A 10-item smell identification scale related to risk for Alzheimer's disease. Annals of Neurology 2005, 58(1):155-160.
68. Tulving E. Episodic and semantic memory. Organization of Memory 1972, 382-403. Academic Press, New York. E. Tulving, W. Donaldson (Eds.).
69. Tulving E. Elements of Episodic Memory 1983, Clarendon Press, Oxford.
70. Uren R.C., Riddle M.C., Lezak M.D., Benningtondavis M. The mental efficiency of the elderly person with type-II diabetes-mellitus. Journal of the American Geriatrics Society 1990, 38(5):505-510.
71. Weinstock R.S., Wright H.N., Smith D.U. Olfactory dysfunction in diabetes-mellitus. Physiology & Behavior 1993, 53(1):17-21.
72. Wenham P.R., Price W.H., Blundell G. Apolipoprotein-E genotyping by one-stage PCR. Lancet 1991, 337(8750):1158-1159.
73. Westervelt H.J., Ruffolo J.S., Tremont G. Assessing olfaction in the neuropsychological exam: the relationship between odor identification and cognition in older adults. Archives of Clinical Neuropsychology 2005, 20(6):761-769.
74. Wilson R.S., Arnold S.E., Schneider J.A., Tang Y., Bennett D.A. The relationship between cerebral Alzheimer's disease pathology and odour identification in old age. Journal of Neurology Neurosurgery and Psychiatry 2007, 78(1):30-35.
75. Wysocki C.J., Gilbert A.N. National geographic smell survey-effects of age are heterogenous. Annals of the New York Academy of Sciences 1989, 561:12-28.
76. Yamagishi M., Getchell M.L., Takami S., Getchell T.V. Increased density of olfactory receptor neurons immunoreactive for apolipoprotein E in patients with Alzheimer's disease. The Annals of Otology, Rhinology, and Laryngology 1998, 107(5 Pt 1):421-426.