Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-17T12:45:31.571Z Has data issue: false hasContentIssue false
  • English
  • Français

Olfactory Impairment and Subjective Olfactory Complaints Independently Predict Conversion to Dementia: A Longitudinal, Population-Based Study

Published online by Cambridge University Press:  22 January 2014

Ingrid Stanciu ,
Maria Larsson ,
Steven Nordin ,
Rolf Adolfsson ,
Lars-Göran Nilsson  and
Jonas K. Olofsson
Ingrid Stanciu
Affiliation:
Gösta Ekman Laboratory, Stockholm University, Stockholm, Sweden Psychology Department, Stockholm University, Stockholm, Sweden
Maria Larsson
Affiliation:
Gösta Ekman Laboratory, Stockholm University, Stockholm, Sweden Psychology Department, Stockholm University, Stockholm, Sweden
Steven Nordin
Affiliation:
Department of Psychology, Umeå University, Umeå, Sweden
Rolf Adolfsson
Affiliation:
Department of Clinical Sciences, Psychiatry, Umeå University, Umeå, Sweden
Lars-Göran Nilsson
Affiliation:
Psychology Department, Stockholm University, Stockholm, Sweden
Jonas K. Olofsson*
Affiliation:
Gösta Ekman Laboratory, Stockholm University, Stockholm, Sweden Psychology Department, Stockholm University, Stockholm, Sweden Swedish Collegium for Advanced Study, Uppsala, Sweden
*
Correspondence and reprint requests to: Jonas Olofsson, Psychology Department, Stockholm University, SE-10691 Stockholm, Sweden. E-mail: jonas.olofsson@psychology.su.se
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined whether conversion to dementia can be predicted by self-reported olfactory impairment and/or by an inability to identify odors. Common forms of dementia involve an impaired sense of smell, and poor olfactory performance predicts cognitive decline among the elderly. We followed a sample of 1529 participants, who were within a normal range of overall cognitive function at baseline, over a 10-year period during which 159 were classified as having a dementia disorder. Dementia conversion was predicted from demographic variables, Mini-Mental State Examination score, and olfactory assessments. Self-reported olfactory impairment emerged as an independent predictor of dementia. After adjusting for effects of other predictors, individuals who rated their olfactory sensitivity as “worse than normal” were more likely to convert to dementia than those who reported normal olfactory sensitivity (odds ratio [OR] = 2.17; 95% confidence interval [CI] [1.40, 3.37]). Additionally, low scores on an odor identification test also predicted conversion to dementia (OR per 1 point increase = 0.89; 95% CI [0.81, 0.98]), but these two effects were additive. We suggest that assessing subjective olfactory complaints might supplement other assessments when evaluating the risk of conversion to dementia. Future studies should investigate which combination of olfactory assessments is most useful in predicting dementia conversion. (JINS, 2014, 20, 1–9)

Keywords

OlfactionVascular dementiaAlzheimer type dementiaMemorySmell disorderAwareness
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 2 , February 2014 , pp. 209 - 217
Copyright
Copyright © The International Neuropsychological Society 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albers, M.W., Tabert, M.H., Devanand, D.P. (2006). Olfactory dysfunction as a predictor of neurodegenerative disease. Current Neurology and Neuroscience Reports, 6(5), 379–386. doi:10.1007/s11910-996-0018-7 Google Scholar
American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders (4th ed.). Washington, DC: American Psychiatric Association Press.Google Scholar
Bacon, A.W., Bondi, M.W., Salmon, D.P., Murphy, C.M. (1998). Very early changes in olfactory functioning due to Alzheimer's disease and the role of apolipoprotein E in olfaction. Annuals of the New York Acadamey of Sciences, 855, 723–731. doi:10.1111/j.1749-6632.1998.tb10651.x Google Scholar
Bahar-Fuchs, A., Moss, S., Rowe, C., Savage, G. (2011). Awareness of olfactory deficits in healthy aging, amnestic mild cognitive impairment and Alzheimer's disease. International Psychogeriatrics, 23(7), 1097–1106. doi:10.1017/S1041610210002371 Google Scholar
Bende, M., Nordin, S. (1997). Perceptual learning in olfaction: Professional wine tasters versus controls. Physiology & Behavior, 62(5), 1065–1070. doi:10.1016/S0031-9384(97)00251-5 CrossRefGoogle ScholarPubMed
Cooney, T.M., Schaie, W., Willis, S.L. (1988). The relationship between prior functioning on cognitive and personality dimensions and subject attrition in longitudinal research. Journal of Geronology, 43, 1217.Google Scholar
Da Silva, J., Gonçalves-Pereira, M., Xavier, M., Mukaetova-Ladinska, E.B. (2013). Affective disorders and risk of developing dementia: Systematic review. The British Journal ofPpsychiatry: The journal of Mental Science, 202, 177–186. doi:10.1192/bjp.bp.111.101931 CrossRefGoogle ScholarPubMed
Davies, D.C., Brooks, J.W., Lewis, D.A. (1993). Axonal loss from the olfactory tracts in Alzheimer's disease. Neurobiology of Aging, 14, 353–357. doi:10.1016/0197-4580(93)90121-Q Google Scholar
Devanand, D., Michaels-Marston, K.S., Xinhua, L., Pelton, G.H., Padilla, M., Marder, K., Mayeux, R. (2000). Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. American Journal of Psychiatry, 157, 1399–1405. doi:10.1176/appi.ajp.157.9.1399 Google Scholar
Djordjevic, J., Jones-Gotman, M., De Sousa, K., Chertkow, H. (2008). Olfaction in patients with mild cognitive impairment and Alzheimer's disease. Neurobiology of Aging, 29(5), 693–706. doi:10.1016/j.neurobiolaging.2006.11.014 CrossRefGoogle ScholarPubMed
Dureman, I., Kebbon, L., Österberg, E. (1971). A manual to the DS-battery. Psykologiförbundet AB, Stockholm.Google Scholar
Erk, S., Spottke, A., Meisen, A., Wagner, M., Walter, H., Jessen, F. (2011). Evidence of neuronal compensation during episodic memory in subjective memory impairment. Archives of General Psychiatry, 68(8), 845–852. doi:10.1001/archgenpsychiatry.2011.80 Google Scholar
Folstein, M.F., Folstein, S.E., 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.CrossRefGoogle Scholar
Geerlings, M.I., Jonker, C., Bouter, L.M., Adèr, H.J., Schmand, B. (1999). Association between memory complaints and incident Alzheimer's disease in elderly people with normal baseline cognition. The American Journal of Psychiatry, 156(4), 531–537.Google Scholar
Gorelick, P.B., Scuteri, A., Black, S.E., DeCarli, C., Greenberg, S.M., Iadecola, C., Seshadri, S. (2011). Vascular contributions to cognitive impairment and dementia: A statement for healthcare professionals from the American heart association/American stroke association. Stroke, 42(9), 2672–2713. doi:10.1161/STR.0b013e3182299496 Google Scholar
Graves, A.B., Bowen, J.D., Rajaram, L., McCormick, W.C., McCurry, S.M., Schellenberg, G.D., Larson, E.B. (1999). Impaired olfaction as a marker for cognitive decline: Interaction with apolipoprotein E ε4 status. Neurology, 53(7), 1480–1487. doi:10.1212/WNL.53.7.1480 CrossRefGoogle ScholarPubMed
Gray, A.J., Staples, V., Murren, K., Dhariwal, A., Bentham, P. (2001). Olfactory identification is impaired in clinic-based patients with vascular dementia and senile dementia of Alzheimer type. International Journal of Geriatric Psychiatry, 16(5), 513–517. doi:10.1002/gps.383 CrossRefGoogle ScholarPubMed
Hedner, M., Larsson, M., Arnold, N., Zucco, G.M., Hummel, T. (2010). Cognitive factors in odor detection, odor discrimination, and odor identification tasks. Journal of Clinical and Experimental Neuropsychology, 32(10), 1062–1067. doi:10.1080/13803391003683070 CrossRefGoogle ScholarPubMed
Hummel, T., Sekinger, B., Wolf, S.R., Pauli, E., Kobal, G. (1997). ‘Sniffin’ sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22, 39–52. doi:10.1586/ern.09.115 Google Scholar
Jorm, A.F., Christensen, H., Henderson, A.S., Korten, A.E., Mackinnon, A.J., Scott, R. (1994). Complaints of cognitive decline in the elderly: A comparison of reports by subjects and informants in a community survey. Psychological Medicine, 24, 365–374. doi:10.1017/S0033291700027343 CrossRefGoogle Scholar
Jorm, A.F., Christensen, H., Korten, A.E., Jacomb, P.A., Henderson, A.S. (2001). Memory complaints as a precursor of memory impairment in older people: A longitudinal analysis over 7-8 years. Psychological Medicine, 31, 441–449.Google Scholar
Larsson, M., Nilsson, L.G., Olofsson, J.K., Nordin, S. (2004). Demographic and cognitive predictors of cued odor identification: Evidence from a population-based study. Chemical Senses, 29(6), 547–554. doi:10.1093/chemse/bjh059 Google Scholar
Larsson, M., Semb, H., Winblad, B., Amberla, K., Wahlund, L.-O., Bäckman, L. (1999). Odor identification in normal aging and early Alzheimer's disease: Effects of retrieval support. Neuropsychology, 13, 1–7. doi:10.1037/0894-4105.13.1.47 CrossRefGoogle ScholarPubMed
McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R., Kawas, C.H., Phelps, C.H. (2011). The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers and Dementia, 7(3), 263–269. doi:10.1016/j.jalz.2011.03.005 CrossRefGoogle ScholarPubMed
Mesholam, R.I., Moberg, P.J., Mahr, R.N., Doty, R.L. (1998). Olfaction in neurodegenerative disease: A meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Archives of Neurology, 55(1), 84–90. doi:10.1001/archneur.55.1.84 CrossRefGoogle ScholarPubMed
Morgan, C.D., Nordin, S., Murphy, C. (1995). Odor identification as an early marker for Alzheimer's disease: Impact of lexical functioning and detection sensitivity. Journal of Clinical and Experimental Neuropsychology, 17(5), 793–803. doi:10.1080/01688639508405168 CrossRefGoogle ScholarPubMed
Murphy, C., Schubert, C.R., Cruickshanks, K.J., Klein, B.E., Klein, R., Nondahl, D.M. (2002). Prevalence of olfactory impairment in older adults. The Journal of the American Medical Association, 288(18), 2307–2312. doi:10.1001/jama.288.18.2307 CrossRefGoogle ScholarPubMed
Nilsson, L.G., Adolfsson, R., Backman, L., de Frias, C.M., Molander, B., Nyberg, L. (2004). Betula: A prospective cohort study on memory, health and aging. Aging Neuropsychology and Cognition, 11, 134–148. doi:10.1080/13825580490511026 Google Scholar
Nilsson, L.G., Backman, L., Erngrud, K., Nyberg, L., Adolfsson, R., Bucht, G., Winblad, B. (1997). The Betula prospective cohort study: Memory, health and aging. Aging Neuropsychology and Cognition, 4, 1–32. doi:10.1080/13825589708256633 Google Scholar
Nordin, S., Brämerson, A. (2008). Complaints of olfactory disorders: Epidemiology, assessment and clinical implications. Current Opinion in Allergy and Clinical Immunology, 8, 10–15. doi:10.1097/ACI.0b013e3282f3f473 Google Scholar
Nordin, S., Brämerson, A., Lidén, E., Bende, M. (1998). The Scandinavian odor-identification test: Development, reliability, validity and normative data. Acta Oto-Laryngologica, 118, 226–234. doi:10.1080/00016489850154946 Google Scholar
Nordin, S., Monsch, A., Murphy, C. (1995). Unawareness of smell loss in normal aging and Alzheimer's disease: Discrepancy between self-reported and diagnosed smell sensitivity. Journal of Gerontology, 50(B), 187–192. doi:10.1093/geronb/50B.4.P187 Google Scholar
O'Connor, D.W., Pollitt, P.A., Roth, M., Brook, P.B., Reiss, B.B. (1990). Memory complaints and impairment in normal, depressed, and demented elderly persons identified in a community survey. Archives of General Psychiatry, 47, 224–227. doi:10.1001/archpsyc.1990.01810150024005 CrossRefGoogle Scholar
O'Hara, M.W., Hinrichs, J.V., Kohout, F.J., Wallace, R.B., Lemke, J.H. (1986). Memory complaint and memory performance in the depressed elderly. Psychology and Aging, 1, 208–214. doi:10.1037/0882-7974.1.3.208 CrossRefGoogle ScholarPubMed
Ohm, T.G., Braak, H. (1987). Olfactory bulb changes in Alzheimer's disease. Acta Neuropathologica (Berlin), 73, 365–369. doi:10.1007%2FBF00688261 Google Scholar
Olofsson, J.K., Nordin, S., Wiens, S., Hedner, M., Nilsson, L.-G., Larsson, M. (2010). Odor identification impairment in elderly ApoE-e4 carriers is independent of dementia. Neurobiology of Aging, 31, 567–577. doi:10.1016/j.neurobiolaging.2008.05.019 Google Scholar
Olofsson, J.K., Rogalski, E., Harrison, T., Mesulam, M.-M., Gottfried, J. (2013). A cortical pathway to odor naming: Evidence from primary progressive aphasia. Brain, 136, 1245–1259. doi:10.1093/brain/awt019 CrossRefGoogle ScholarPubMed
Olofsson, J.K., Rönnlund, M., Nordin, S., Nyberg, L., Nilsson, L.-G., Larsson, M. (2009). Odor identification deficit as a predictor of five-year global cognitive change: Interactive effects with age and ApoE-epsilon4. Behavior Genetics, 39, 496–503. doi:10.1007/s10519-009-9289-5 Google Scholar
Pause, B.M., Miranda, A., Göder, R., Aldenhoff, J.B., Ferstl, R. (2001). Reduced olfactory performance in patients with major depression. Journal of Psychiatric Research, 35, 271–277. doi:10.1016/S0022-3956(01)00029-2 Google Scholar
Ponsen, M.M., Stoffers, D., Booij, J., van Eck-Smit, B.L.F., Wolters, E.Ch., Berendse, H.W. (2004). Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Annuals of Neurology, 56, 173–181. doi:10.1002/ana.20160 CrossRefGoogle ScholarPubMed
Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale of research in the general population. Applied Psychological Measurement, 1, 385–401. doi:10.1177/014662167700100306 Google Scholar
Schab, F.R. (1991). Odor memory: Taking stock. Psychological Bulletin, 2, 242–251. doi:10.1037%2F%2F0033-2909.109.2.242 Google Scholar
Schmand, B., Jonker, C., Geerlings, M.I., Lindeboom, J. (1997). Subjective memory complaints in the elderly: Depressive symptoms and future dementia. British Journal of Psychiatry, 171, 373–376. doi:10.1212/WNL.46.1.121 CrossRefGoogle ScholarPubMed
Schmand, B., Jonker, C., Hooijer, C., Lindeboom, J. (1996). Subjective memory complaints may announce dementia. Neurology, 46, 121–125. doi:10.1212/WNL.46.1.121 CrossRefGoogle ScholarPubMed
Schubert, C.R., Carmichael, L.L., Murphy, C., Klein, B.E.K., Klein, R., Cruickshanks, K.J. (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 Google Scholar
Sevush, S., Leve, N. (1993). Denial of memory deficit in Alzheimer's disease. American Journal of Psychiatry, 150, 748–751.Google ScholarPubMed
Shu, C.-H., Hummel, T., Lee, P.-L., Chiu, C.-H., Lin, S.-H., Yuan, B.-C. (2009). The proportion of self-rated olfactory dysfunction does not change across the life span. American Journal of Rhinology & Allergy, 23(4), 413–416. doi:10.2500/ajra.2009.23.3343 Google Scholar
Stevens, J., Cain, W., Burke, R. (1988). Variability of olfactory thresholds. Chemical Senses, 13(4), 643–653. doi:10.1093/chemse/13.4.643 CrossRefGoogle Scholar
Sunderland, A., Watts, K., Baddeley, A.D., Harris, J.E. (1986). Subjective memory assessment and test performance in elderly adults. Journal of Gerontology, 41, 376–384. doi:10.1093%2Fgeronj%2F41.3.376 CrossRefGoogle ScholarPubMed
Swan, G.E., Carmelli, D. (2002). Impaired olfaction predicts cognitive decline in nondemented older adults. Neuroepidemiology, 21, 58–67. doi:10.1159/000048618 Google Scholar
Tobiansky, R., Blizard, R., Livingston, G., Mann, A. (1995). The Gospel Oak Study stage IV: The clinical relevance of subjective memory impairment in older people. Psychological Medicine, 25, 779–786. doi:10.1017%2FS0033291700035029 Google Scholar
Vogel, A., Stokholm, J., Gade, A., Andersen, B.B., Hejl, A.-M., Waldemar, G. (2004). Awareness of deficits in mild cognitive impairment and Alzheimer's disease: Do MCI patients have impaired insight? Dementia and Geriatric Cognitive Disorders, 17(3), 181–187. doi :10.1159%2F000076354 CrossRefGoogle ScholarPubMed
Waldorff, F.B., Siersma, V., Vogel, A., Waldemar, G. (2012). Subjective memory complaints in general practice predicts future dementia: A 4-year follow-up study. International Journal of Geriatric Psychiatry, 27(11), 1180–1188. doi:10.1002%2Fgps.3765 CrossRefGoogle ScholarPubMed
Wang, L., Van Belle, G., Crane, P.K., Kukull, W.A., Bowen, J.D., McCormick, W.C., Larson, E.B. (2004). Subjective memory deterioration and future dementia in people aged 65 and older. Journal of the American Geriatrics Society, 52(12), 2045–2051. doi:10.1111/j.1532-5415.2004.52568.x Google Scholar
Wehling, E., Nordin, S., Espeseth, T., Reinvang, I., Lundervold, A. (2011). Unawareness of olfactory dysfunction and its association with cognitive functioning in middle aged and old adults. Archives of Clinical Neuropsychology, 26, 260–269. doi:10.1093%2Farclin%2Facr019 Google Scholar
Wilson, R.S., Arnold, S.E., Tang, X., Bennett, D.A. (2006). Odor identification and decline in different cognitive domains in old age. Neuroepidemiology, 26, 61–67. doi:10.1159%2F000090250 Google Scholar