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Identification of odors, faces, cities and naming of objects in patients with subjective cognitive decline, mild cognitive impairment and Alzheimer´s disease: a longitudinal study

Published online by Cambridge University Press:  21 September 2018

R. Tahmasebi ,
S. Zehetmayer ,
G. Pusswald ,
G. Kovacs ,
E. Stögmann  and
J. Lehrner Open the ORCID record for J. Lehrner [Opens in a new window]
R. Tahmasebi
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
S. Zehetmayer
Affiliation:
Center for Medical Statistics, Informatics, and Intelligent Systems, Medical University of Vienna, Vienna, Austria
G. Pusswald
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
G. Kovacs
Affiliation:
Institute of Neurology, Medical University of Vienna, Vienna, Austria
E. Stögmann
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
J. Lehrner*
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
*
Correspondence should be addressed to: Johann Lehrner, Department of Neurology, Medical University of Vienna, Währinger Gürtel 18-20, A-1097 Wien, Austria. Phone: 0043-1-40400-31090; Fax: 0043-1-40400-31410. Email: johann.lehrner@meduniwien.ac.at.
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Abstract

Objective:

Recent studies have tried to find a reliable way of predicting the development of Alzheimer´s Disease (AD) among patients with mild cognitive impairment (MCI), often focusing on olfactory dysfunction or semantic memory. Our study aimed to validate these findings while also comparing the predictive accuracy of olfactory and semantic assessments for this purpose.

Method:

Six hundred fifty patients (median age 68, 58% females) including controls, SCD (subjective cognitive decline), non-amnestic MCI (naMCI), amnestic MCI (aMCI), and AD patients were tested for olfactory dysfunction by means of odor identification testing and semantic memory. Of those 650 patients, 120 participants with SCD, naMCI, or aMCI at baseline underwent a follow-up examination after two years on average. Of these 120 patients, 12% had developed AD at follow-up (converters), while 88% did not develop AD at follow-up (non-converters).

Results:

Analysis showed a significant difference only for initial olfactory identification between converters and non-converters. Sensitivity of impairment of olfactory identification for AD prediction was low at 46.2%, although specificity was high at 81.9%. Semantic memory impairment at baseline was not significantly related to AD conversion, although, when naming objects, significant differences were found between AD patients and all other groups and between naMCI and aMCI patients compared to controls and SCD patients.

Conclusions:

Objective olfactory assessments are promising instruments for predicting the conversion to AD among MCI patients. However, due to their low sensitivity and high specificity, a combination with other neuropsychological tests might lead to an improved predictive accuracy. Further longitudinal studies with more participants are required to investigate the usefulness of semantic memory tests in this case.

Keywords

cognitive dysfunctionneuropsychologyolfactionsemantic memoryAlzheimer’s diseasemild cognitive impairmentsubjective cognitive decline
Type
Original Research Article
Information
International Psychogeriatrics , Volume 31 , Issue 4: Issue Theme: Aging and Well-Being , April 2019 , pp. 537 - 549
Copyright
© International Psychogeriatric Association 2018 

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References

Albert, M. S. et al. (2011). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7, 270–279. doi: 10.1016/j.jalz.2011.03.008.CrossRefGoogle Scholar
Backhaus, K. et al. (2016). Multivariate Analysemethoden – Eine anwendungsorientierte Einführung. Berlin/Heidelberg: Springer-Verlag.Google Scholar
Bondi, M. W. et al. (2008). Neuropsychological contributions to the early identification of Alzheimer’s disease. Neuropsychology Review, 18, 73–90. doi: 10.1007/s11065-008-9054-1.CrossRefGoogle ScholarPubMed
Calderón-Garcidueñas, L. et al. (2016). Cerebrospinal fluid biomarkers in highly exposed PM2.5 urbanites: the risk of Alzheimer’s and Parkinson’s diseases in young Mexico city residents. Journal of Alzheimer’s Disease, 54, 597–613. doi: 10.3233/JAD-160472.CrossRefGoogle ScholarPubMed
Chong, M. S. and Sahadevan, S. (2005). Preclinical Alzheimer’s disease: diagnosis and prediction of progression. The Lancet Neurology, 4, 576–579. doi: 10.1016/S1474-4422(05)70168-X.CrossRefGoogle ScholarPubMed
Clague, F. et al. (2011). Is knowledge of famous people compromised in mild cognitive impairment? Cognitive and Behavioral Neurology, 24(3), 134–144. doi: 10.1097/WNN.0b013e318234315a.CrossRefGoogle ScholarPubMed
Conti, M. Z. et al. (2013). Odor identification deficit predicts clinical conversion from mild cognitive impairment to dementia due to Alzheimer’s disease. Archives of Clinical Neuropsychology, 28, 391–399. doi: 10.1093/arclin/act032.CrossRefGoogle ScholarPubMed
Devanand, D. P. (2016). Olfactory identification deficits, cognitive decline, and dementia in older adults. American Journal of Geriatric Psychiatry, 24, 1151–1157. doi: 10.1016/j.jagp.2016.08.010.CrossRefGoogle ScholarPubMed
Devanand, D. P. et al. (2015). Olfactory deficits predict cognitive decline and Alzheimer dementia in an urban community. Neurology, 84, 182–189. doi: 10.1212/WNL.0000000000001132.CrossRefGoogle Scholar
Devanand, D. P. et al. (2008). Combining early markers strongly predicts conversion from mild cognitive impairment to Alzheimer’s disease. Biological Psychiatry, 64, 871–879. doi: 10.1016/j.biopsych.2008.06.020.CrossRefGoogle ScholarPubMed
Devanand, D. P. et al. (2010). Olfactory identification deficits and MCI in a multi-ethnic elderly community sample. Neurobiology of Aging, 31, 1593–1600. doi: 10.1016/j.neurobiolaging.2008.09.008.CrossRefGoogle Scholar
Dhilla Albers, A. et al. (2016). Episodic memory of odors stratifies Alzheimer biomarkers in normal elderly. Annals of Neurology, 80, 846–857. doi: 10.1002/ana.24792.CrossRefGoogle ScholarPubMed
Djordjevic, J. et al. (2008). Olfaction in patients with mild cognitive impairment and Alzheimer’s disease. Neurobiology of Aging, 29, 693–706. doi: 10.1016/j.neurobiolaging.2006.11.014.CrossRefGoogle ScholarPubMed
Doblinger, B. (2013). Das semantische Gedächtnis – Unterschiede bei gesunden, MCI, Parkinson, und Alzheimerpatienten. Wien, Austria: University of Vienna, Faculty of Psychology.Google Scholar
Doty, R. L. and Kamath, V. (2014). The influences of age on olfaction: a review. Frontiers in Psychology, 5, 20. doi: 10.3389/fpsyg.2014.00020.CrossRefGoogle ScholarPubMed
Folstein, M. F., Folstein, S. E. and McHugh, P. R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. doi: 10.1016/0022-3956(75)90026-6.CrossRefGoogle ScholarPubMed
Fusetti, M. et al. (2010). Smell and preclinical Alzheimer disease: study of 29 patients with amnesic mild cognitive impairment. Journal of Otolaryngology – Head & Neck Surgery = Le Journal d’oto-rhino-laryngologie et de chirurgie cervico-faciale, 39, 175–181.Google ScholarPubMed
Graves, A. B. et al. (1999). Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology, 53, 1480. doi: 10.1212/WNL.53.7.1480.CrossRefGoogle ScholarPubMed
Greene, J. D. W. and Hodges, J. R. (1996). Identification of famous faces and famous names in early Alzheimer’s disease Relationship to anterograde episodic and general semantic memory. Brain, 119, 111–128. doi: 10.1093/brain/119.1.111.CrossRefGoogle ScholarPubMed
Hagemeier, J. et al. (2016). Odor identification deficit in mild cognitive impairment and Alzheimer’s disease is associated with hippocampal and deep gray matter atrophy. Psychiatry Research – Neuroimaging, 255, 87–93. doi: 10.1016/j.pscychresns.2016.08.003.CrossRefGoogle ScholarPubMed
Hautzinger, M., Keller, F. and Kühner, C. (2006). Das Beck Depressionsinventar II. Deutsche Bearbeitung und Handbuch zum BDI-II. Frankfurt am Main: Harcourt Test Services.Google Scholar
Hummel, T. et al. (2007). Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. European Archives of Oto-Rhino-Laryngology, 264, 237–243. doi: 10.1007/s00405-006-0173-0.CrossRefGoogle ScholarPubMed
Hummel, T. et al. (1997). ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odour identification, odor discrimination and olfactory threshold. Chemical Senses, 22, 39–52. doi: 10.1093/chemse/22.1.39.CrossRefGoogle ScholarPubMed
Jack, C. R. et al. (2008). 11C PiB and structural MRI provide complementary information in imaging of Alzheimer’s disease and amnestic mild cognitive impairment. Brain, 131, 665–680.CrossRefGoogle ScholarPubMed
Jaeschke, R. et al. (1994). Users’ guides to the medical literature III. How to use an article about a diagnostic test B. What are the results and will they help me in caring for my patients? JAMA, 271, 703–707. doi: 10.1001/jama.1994.03510330081039.CrossRefGoogle ScholarPubMed
Jessen, F. et al. (2014). A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimer’s & Dementia, 10, 844–852. doi: 10.1016/j.jalz.2014.01.001.CrossRefGoogle ScholarPubMed
Joubert, S. et al. (2010). The cognitive and neural expression of semantic memory impairment in mild cognitive impairment and early Alzheimer’s disease. Neuropsychologia, 48, 978–988. doi: 10.1016/j.neuropsychologia.2009.11.019.CrossRefGoogle ScholarPubMed
Kaneda, H. et al. (2000). Decline in taste and odor discrimination abilities with age, and relationship between gustation and olfaction. Chemical Senses, 25, 331–337. doi: 10.1093/chemse/25.3.331.CrossRefGoogle ScholarPubMed
Lehrner, J. (2007). The Neuropsychological Test Battery Vienna (NTBV). Psychologie in Österreich, 4 & 5, 358–365.Google Scholar
Lehrner, J. P. et al. (1997). Olfactory functions in Parkinson’s disease and Alzheimer’s disease. Chemical Senses, 22, 105–110. doi: 10.1093/chemse/22.1.105.CrossRefGoogle ScholarPubMed
Lehrner, J. et al. (2016). Subjective memory complaints and conversion to dementia in patients with subjective cognitive decline and patients with mild cognitive impairment. Journal of Neuropsychology, 27, 85–93. doi: 10.1024/1016-264X/a000175.Google Scholar
Lehrner, J. et al. (2014). Awareness of memory deficits in subjective cognitive decline, mild cognitive impairment, Alzheimer’s disease and Parkinson’s disease. International Psychogeriatrics, 27, 357–366. doi: 10.1017/S1041610214002245.CrossRefGoogle ScholarPubMed
Lehrner, J. et al. (2009). Odor identification and self-reported olfactory functioning in patients with subtypes of mild cognitive impairment. The Clinical Neuropsychologist, 23, 818–830. doi: 10.1080/13854040802585030.CrossRefGoogle ScholarPubMed
Lojkowska, W. et al. (2011). Follow-up study of olfactory deficits, cognitive functions, and volume loss of medial temporal lobe structures in patients with mild cognitive impairment. Current Alzheimer Research, 8, 689–698. doi: 10.2174/156720511796717212.CrossRefGoogle ScholarPubMed
Masurkar, A. V and Devanand, D. P. (2014). Olfactory dysfunction in the elderly: basic circuitry and alterations with normal aging and Alzheimer’s disease. Current Geriatrics Reports, 3, 91–100. doi: 10.1007/s13670-014-0080-y.CrossRefGoogle ScholarPubMed
Mauri, M. et al. (2012). Progression to dementia in a population with amnestic mild cognitive impairment: clinical variables associated with conversion. Functional Neurology, 27, 49–54.Google Scholar
McKhann, G. et al. (1984). Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of department of health and human services task force on Alzheimer’s disease. Neurology, 34, 939. doi: 10.1212/WNL.34.7.939.CrossRefGoogle ScholarPubMed
Moon, J. et al. (2016). Early diagnosis of Alzheimer’s disease from elevated olfactory mucosal miR-206 level. Scientific Reports, 6, 20364. doi: 10.1038/srep20364.CrossRefGoogle ScholarPubMed
Morris, J. C. et al. (1989). The consortium to establish a registry for Alzheimer’s disease neuropathology. Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39, 1159. doi: 10.1212/WNL.39.9.1159.Google Scholar
Murphy, C. et al. (2002). Prevalence of olfactory impairment in older adults. JAMA, 288, 2307. doi: 10.1001/jama.288.18.2307.CrossRefGoogle ScholarPubMed
Nyberg, L. et al. (1996). Age differences in episodic memory, semantic memory, and priming: relationships to demographic, intellectual, and biological factors. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 51, P234–P240. doi: 10.1093/geronb/51B.4.P234.CrossRefGoogle ScholarPubMed
Patterson, K., Nestor, P. J. and Rogers, T. T. (2007). Where do you know what you know? The representation of semantic knowledge in the human brain. Nature Reviews Neuroscience, 8, 976–987. doi: 10.1038/nrn2277.CrossRefGoogle ScholarPubMed
Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194. doi: 10.1111/j.1365-2796.2004.01388.x.CrossRefGoogle ScholarPubMed
Petersen, R. C. et al. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56, 303–308. doi: 10.1001/archneur.56.3.303.CrossRefGoogle ScholarPubMed
Pusswald, G. et al. (2013). Prevalence of mild cognitive impairment subtypes in patients attending a memory outpatient clinic-comparison of two modes of mild cognitive impairment classification. Results of the Vienna conversion to dementia study. Alzheimer’s & Dementia, 9, 366–376. doi: 10.1016/j.jalz.2011.12.009.CrossRefGoogle ScholarPubMed
Rabin, L. A. et al. (2012). Predicting Alzheimer’s disease: neuropsychological tests, self-reports, and informant reports of cognitive difficulties. Journal of the American Geriatrics Society, 60, 1128–1134. doi: 10.1111/j.1532-5415.2012.03956.x.CrossRefGoogle ScholarPubMed
Roberts, R. O. et al. (2016). Association between olfactory dysfunction and amnestic mild cognitive impairment and Alzheimer disease dementia. JAMA Neurology, 73, 93–101. doi: 10.1001/jamaneurol.2015.2952.CrossRefGoogle ScholarPubMed
Saß, H., Wittchen, H.-U. and Zaudig, M. (1996). Diagnostisches und Statistisches Manual Psychischer Störungen DSM-IV: Übersetzt nach der vierten Auflage des [Diagnostic and Statistical Manual of Mental Disorders der American Psychiatric Association TT – Diagnostic and Statistical Manual of Mental Disor]. Available at: http://search.ebscohost.com/login.aspx?direct=true&db=pdx&AN=0103973&site=ehost-live.Google Scholar
Schmidt, K.-H. and Metzler, P. (1992). WST-Wortschatztest. Diagnostica, 40, 293–297.Google Scholar
Schubert, C. R. et al. (2008). Olfaction and the 5-year incidence of cognitive impairment in an epidemiological study of older adults. Journal of the American Geriatrics Society, 56, 1517–1521. doi: 10.1111/j.1532-5415.2008.01826.x.CrossRefGoogle Scholar
Sohrabi, H. R. et al. (2009). Olfactory dysfunction is associated with subjective memory complaints in community-dwelling elderly individuals. Journal of Alzheimer’s Disease, 17, 135–142. doi: 10.3233/JAD-2009-1020.CrossRefGoogle ScholarPubMed
Spaan, P. E. J. and Duregger, C. (2016). Episodic and semantic memory impairments in (very) early Alzheimer’s disease: the diagnostic accuracy of paired-associate learning formats. Cogent Psychology, 3, 1125076. doi: 10.1080/23311908.2015.1125076.CrossRefGoogle Scholar
Stanciu, I. et al. (2014). Olfactory impairment and subjective olfactory complaints independently predict conversion to dementia: a longitudinal, population-based study. Journal of the International Neuropsychological Society, 20, 209–217. doi: 10.1017/S1355617713001409.CrossRefGoogle ScholarPubMed
Sun, G. H. et al. (2012). Olfactory identification testing as a predictor of the development of Alzheimer’s dementia: a systematic review. The Laryngoscope, 122, 1455–1462. doi: 10.1002/lary.23365.CrossRefGoogle ScholarPubMed
Tabert, M. H. et al. (2005). A 10-item smell identification scale related to risk for Alzheimer’s disease. Annals of Neurology, 58, 155–160. doi: 10.1002/ana.20533.CrossRefGoogle ScholarPubMed
Tabert, M. H. et al. (2006). Neuropsychological prediction of conversion to Alzheimer disease in patients with mild cognitive impairment. Archives of General Psychiatry, 63, 916–924. doi: 10.1001/archpsyc.63.8.916.CrossRefGoogle ScholarPubMed
Tulving, E. (1972). Episodic and semantic memory. In Tulving, E. and Donaldson, W. (Eds.) Organization of Memory (pp. 381–403). New York: Academic Press.Google Scholar
Velayudhan, L. (2015). Smell identification function and Alzheimer’s disease: a selective review. Current Opinion in Psychiatry, 28, 173–179. doi: 10.1097/YCO.0000000000000146.Google ScholarPubMed
Werheid, K. and Clare, L. (2007). Are faces special in Alzheimer’s disease? Cognitive conceptualisation, neural correlates, and diagnostic relevance of impaired memory for faces and names. Cortex, 43, 898–906. doi: 10.1016/S0010-9452(08)70689-0.CrossRefGoogle ScholarPubMed
Whitwell, J. L. et al. (2008). MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology, 70, 512–520. doi: 10.1212/01.wnl.0000280575.77437.a2.CrossRefGoogle ScholarPubMed
Wolfensberger, M. (2000). Sniffin’ Sticks: a new olfactory test battery. Acta Oto-Laryngologica, 120, 303–306. doi: 10.1080/000164800750001134.CrossRefGoogle Scholar
Woodward, M. R. et al. (2017). Validation of olfactory deficit as a biomarker of Alzheimer disease. Neurology: Clinical Practice, 7, 5–14. doi: 10.1212/CPJ.0000000000000293.Google ScholarPubMed
Youden, W. J. (1950). Index for rating diagnostic tests. Cancer, 3, 32–35. doi: 10.1002/1097-0142(1950)3:1<32::AID-CNCR2820030106>3.0.CO;2-3.3.0.CO;2-3>CrossRefGoogle ScholarPubMed