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Olfaction deterioration in cognitive disorders in the elderly

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Abstract

Background

Parkinson’s and Alzheimer’s diseases are widespread neurodegenerative pathologies. Parkinson’s disease affects about 1 % of the population over the age of 65 years, while Alzheimer is considered the most common cause of dementia, with an annual incidence of 1 % in persons aged 65 years. It has been demonstrated that both these neurodegenerative diseases are associated with smell dysfunction.

Aim

The aim of the present review is to describe briefly modern olfactory evaluation tools as well as the importance of olfactory sensitivity screening in the elderly, especially where cognitive disorders, such as Alzheimer’s or Parkinson’s diseases, are suspected.

Methods

A brief literature review focusing on the basic principle of smell tests is illustrated together with their application in elderly patients affected by cognitive disorders, in particular Parkinson’s and Alzheimer’s diseases.

Results/Conclusions

Alzheimer’s and Parkinson’s diseases are both neurodegenerative disorders typically found in the elderly. As both diseases are characterized by the early presence of dysosmia, simple validated smell tests could very well help clinicians in the early diagnosis of these neuropathological conditions. Elderly patients complaining of smell loss and found to be dysosmic, by means of validated olfactory tests, should be neurologically evaluated as early as possible to detect slight motor abnormalities in an at-risk population.

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References

  1. Hummel T, Landis BN, Huttenbrink KB (2011) Smell and taste disorders. GMS Curr Top Otorhinolaryngol Head Neck Surg 10:Doc04. doi:10.3205/cto000077

    PubMed Central  PubMed  Google Scholar 

  2. Stevenson RJ (2010) An initial evaluation of the functions of human olfaction. Chem Senses 35:3–20

    Article  PubMed  Google Scholar 

  3. Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuro Endocrinol Lett 23:79–84

    PubMed  Google Scholar 

  4. Ottaviano G, Zuccarello D, Frasson G et al (2013) Olfactory sensitivity and sexual desire in young adult and elderly men: an introductory investigation. Am J Rhinol Allergy 27:157–161

    Article  PubMed  Google Scholar 

  5. Sorokowska A, Sorokowski P, Szmajke A (2012) Does personality smell? Accuracy of personality assessments based on body odour. Eu J Pers 26:496–503

    Article  Google Scholar 

  6. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  CAS  PubMed  Google Scholar 

  7. Sorokowska A, Schriever VA, Gudziol V et al (2014) Changes of olfactory abilities in relation to age: odor identification in more than 1400 people aged 4 to 80 years. Eur Arch Otorhinolaryngol. doi:10.1007/s00405-014-3263-4

    PubMed Central  PubMed  Google Scholar 

  8. Doty RL, Shaman P, Applebaum SL et al (1984) Smell identification ability: changes with age. Science 226:1441–1443

    Article  CAS  PubMed  Google Scholar 

  9. Nyenhuis SM, Mathur SK (2013) Rhinitis in older adults. Curr Allergy Asthma Rep 13:171–177

    Article  PubMed Central  PubMed  Google Scholar 

  10. Rahayel S, Frasnelli J, Joubert S (2012) The effect of Alzheimer’s disease and Parkinson’s disease on olfaction: a meta-analysis. Behav Brain Res 231:60–74

    Article  PubMed  Google Scholar 

  11. Wilson RS, Arnold SE, Schneider JA et al (2009) Olfactory impairment in pre-symptomatic Alzheimer’s disease. Ann NY Acad Sci 1170:730–735

    Article  PubMed Central  PubMed  Google Scholar 

  12. Doty RL (2012) Olfaction in Parkinson’s disease and related disorders. Neurobiol Dis 46:527–552

    Article  PubMed Central  PubMed  Google Scholar 

  13. Hummel T, Kobal G, Gudziol H 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 3000 subjects. Eur Arch Otorhinolaryngol 264:237–243

    Article  CAS  PubMed  Google Scholar 

  14. Sohrabi HR, Bates KA, Weinborn MG et al (2012) Olfactory discrimination predicts cognitive decline among community-dwelling older adults. Transl Psychiatry. doi:10.1038/tp.2012.43

    Google Scholar 

  15. Murphy C, Morgan CD, Geisler MW et al (2000) Olfactory event-related potentials and aging: normative data. Int J Psychophysiol 36:133–145

    Article  CAS  PubMed  Google Scholar 

  16. Rawson NE (2006) Olfactory loss in aging. Sci Aging Knowledge Environ 5:pe6

    Google Scholar 

  17. Mobley AS, Rodriguez-Gil DJ, Imamura F et al (2014) Aging in the olfactory system. Trends Neurosci 37:77–84

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Kern RC (2000) Chronic sinusitis and anosmia: pathologic changes in the olfactory mucosa. Laryngoscope 110:1071–1077

    Article  CAS  PubMed  Google Scholar 

  19. Dulay M, Gesteland R, Shear P et al (2008) Assessment of the influence of cognition and cognitive processing speed on three tests of olfaction. J Clin Exp Neuropsychol 30:327–337

    Article  PubMed  Google Scholar 

  20. Larsson M, Nilsson LG, Olofsson JK et al (2004) Demographic and cognitive predictors of cued odor identification: evidence from a population-based study. Chem Senses 29:547–554

    Article  PubMed  Google Scholar 

  21. Serby M, Larson P, Kalkstein D (1991) The nature and course of olfactory deficits in Alzheimer’s disease. Am J Psychiatry 148:357–360

    Article  CAS  PubMed  Google Scholar 

  22. Vyhnalek M, Magerova H, Andel R et al (2015) Olfactory identification in amnestic and non-amnestic mild cognitive impairment and its neuropsychological correlates. Neurol Sci 349:179–184

    Article  Google Scholar 

  23. Hedner M, Larsson M, Arnold N et al (2010) Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol 32:1062–1067

    Article  PubMed  Google Scholar 

  24. Koss E, Weiffenbach JM, Haxby JV et al (1988) Olfactory detection and identification performance are dissociated in early Alzheimer’s disease. Neurology 38:1228–1232

    Article  CAS  PubMed  Google Scholar 

  25. Potter H, Butters N (1980) An assessment of olfactory deficits in patients with damage to prefrontal cortex. Neuropsychologia 18:621–628

    Article  CAS  PubMed  Google Scholar 

  26. Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Hummel T, Kobal G (2002) Olfactory event-related potentials. In: Simon SA, Nicoleis MAL (eds) Methods in chemosensory research. CRC Press, London, pp 431–453

    Google Scholar 

  28. Welge-Lussen A (2009) Ageing, neurodegeneration, and olfactory and gustatory loss. B-ENT 5(Suppl 13):129–132

    PubMed  Google Scholar 

  29. Kovàcs T (2004) Mechanisms of olfactory dysfunction in aging and neurodegenerative disorders. Ageing Res Rev 2004(3):215–232

    Article  Google Scholar 

  30. Hawkes CH, Shephard BC, Daniel SE (1999) Is Parkinson’s disease a primary olfactory disorder? QJM 92:473–480

    Article  CAS  PubMed  Google Scholar 

  31. Sommer U, Hummel T, Cormann K et al (2004) Detection of presymptomatic Parkinson’s disease: combining smell tests, transcranial sonography, and SPECT. Mov Disord 19:1196–1202

    Article  PubMed  Google Scholar 

  32. Bostantjopoulou S, Katsarou Z, Karakasis C et al (2013) Evaluation of non-motor symptoms in Parkinson’s disease: an underestimated necessity. Hippokratia 17:214–219

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Spillantini MG, Schmidt ML, Lee VM et al (1997) Alpha-synuclein in Lewy bodies. Nature 388:839–840

    Article  CAS  PubMed  Google Scholar 

  34. Stroop WG (1995) Viruses and the olfactory system. In: Doty RL (ed) Handbook of olfaction and gustation. Marcel Dekker INC, New York, pp 367–393

    Google Scholar 

  35. Malec-Litwinowicz M, Rudzińska M, Szubiga M et al (2014) Cognitive impairment in carriers of glucocerebrosidase gene mutation in Parkinson disease patients. Neurol Neurochir Pol 48:258–261

    PubMed  Google Scholar 

  36. Haehner A, Hummel T, Hummel C et al (2007) Olfactory loss may be a first sign of idiopathic Parkinson’s disease. Mov Disord 22:839–842

    Article  PubMed  Google Scholar 

  37. Haehner A, Boesveldt S, Berendse HW et al (2009) Prevalence of smell loss in Parkinson’s disease-a multicenter study. Parkinsonism Relat Disord 15:490–494

    Article  CAS  PubMed  Google Scholar 

  38. Doty RL, Deems DA, Stellar S (1988) Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 38:1237–1244

    Article  CAS  PubMed  Google Scholar 

  39. Bohnen NI, Gedela S, Kuwabara H et al (2007) Selective hyposmia and nigrostriatal dopaminergic denervation in Parkinson’s disease. J Neurol 254:84–90

    Article  CAS  PubMed  Google Scholar 

  40. Rezaie P, Cairns NJ, Chadwick A et al (1996) Lewy bodies are located preferentially in limbic areas in diffuse Lewy body disease. Neurosci Lett 212:111–114

    Article  CAS  PubMed  Google Scholar 

  41. Braak H, Braak E, Yilmazer D et al (1994) Amygdala pathology in Parkinson’s disease. Acta Neuropathol 88:450–493

    Article  Google Scholar 

  42. Pearce RKB, Hawkes CH, Daniel SE (1995) The anterior olfactory nucleus in Parkinson’s disease. Mov Disord 10:283–287

    Article  CAS  PubMed  Google Scholar 

  43. Bohnen NI, Muller ML, Kotagal V et al (2010) Olfactory dysfunction, central cholinergic integrity and cognitive impairment in Parkinson’s disease. Brain 133:1747–1754

    Article  PubMed Central  PubMed  Google Scholar 

  44. Sun GH, Raji CA, Maceachern MP et al (2012) Olfactory identification testing as a predictor of the development of Alzheimer’s dementia: a systematic review. Laryngoscope 122:1455–1462

    Article  PubMed  Google Scholar 

  45. Merril CS (2013) Is sporadic Alzheimer’s disease associated with diphtheria toxin? J Alzheimers Dis 34:595–600

    CAS  PubMed  Google Scholar 

  46. Itzhaki RF, Wozniak MA, Appelt DM et al (2014) Infiltration of the brain by pathogens causes Alzheimer’s disease. Neurobiol Aging 25:619–627 Review

    Article  Google Scholar 

  47. Murphy C, Bacon AW, Bondi MW et al (1998) Apolipoprotein E status is associated with odor identification deficits in nondemented older persons. Ann N Y Acad Sci 855:744–750

    Article  CAS  PubMed  Google Scholar 

  48. Graves AB, Bowen JD, Rajaram L et al (1999) Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology 53:1480–1487

    Article  CAS  PubMed  Google Scholar 

  49. D’introno A, Solfrizzi V, Colacicco AM et al (2006) Current knowledge of chromosome 12 susceptibility genes for late-onset Alzheimer’s disease. Neurobiol Aging 27:1537–1553

    Article  PubMed  Google Scholar 

  50. Roberts E (1986) Alzheimer’s disease may begin in the nose and may be caused by aluminosilicates. Neurobiol Aging 7:561–567

    Article  CAS  PubMed  Google Scholar 

  51. Talamo BR, Rudel R, Kosik KS et al (1989) Pathological changes in olfactory neurons in patients with Alzheimer’s disease. Nature 337:736–739

    Article  CAS  PubMed  Google Scholar 

  52. Hock C, Golombowski S, Müller-Spahn F et al (1998) Histological markers in nasal mucosa of patients with Alzheimer’s disease. Eur Neurol 40:31–36

    Article  CAS  PubMed  Google Scholar 

  53. Kovács T, Cairn NJ, Lantos PL (1999) Amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer’s disease. Neuropathol Appl Neurobiol 25:481–491

    Article  PubMed  Google Scholar 

  54. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259

    Article  CAS  PubMed  Google Scholar 

  55. Kovács T, Cairns NJ, Lantos PL (2001) Olfactory centres in Alzheimer’s disease: olfactory bulb is involved in early Braak’s stages. NeuroReport 12:285–288

    Article  PubMed  Google Scholar 

  56. Kovacs I, Torok I, Zombori J et al (1998) Cholinergic structures and neuropathologic alterations in the olfactory bulb of Alzheimer’s disease brain samples. Brain Res 789:167–170

    Article  CAS  PubMed  Google Scholar 

  57. Doty RL, Shaman P, Dann M (1994) Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 32:489–502

    Article  Google Scholar 

  58. Hummel T, Sekinger B, Wolf SR et al (1997) Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22:39–52

    Article  CAS  PubMed  Google Scholar 

  59. Haehner A, Hummel T, Reichmann H (2011) Olfactory loss in Parkinson’s disease. Parkinsons Dis. doi:10.4061/2011/450939

    PubMed Central  PubMed  Google Scholar 

  60. Richardson JT, Zucco GM (1989) Cognition and olfaction: a review. Psychol Bull 105:352–360

    Article  CAS  PubMed  Google Scholar 

  61. Doty RL, Marcus A, Lee WW (1996) Development of the 12-Item Cross-Cultural Smell Identification Test. Laryngoscope 106:353–356

    Article  CAS  PubMed  Google Scholar 

  62. Jiang RS, Su MC, Liang KL et al (2010) A pilot study of a traditional Chinese version of the University of Pennsylvania Smell Identification Test for application in Taiwan. Am J Rhinol Allergy 24:45–50

    Article  CAS  PubMed  Google Scholar 

  63. Silveira-Moriyama L, Azevedo AM et al (2010) Applying a new version of the Brazilian-Portuguese UPSIT smell test in Brazil. Arq Neuropsiquiatr 68:700–705

    Article  PubMed  Google Scholar 

  64. Kobal G, Hummel T, Sekinger B et al (1996) “Sniffin’ Sticks”: screening of olfactory performace. Rhinology 34:222–226

    CAS  PubMed  Google Scholar 

  65. Hummel T, Konnerth CG, Rosenheim K et al (2001) Screening of olfactory function with a four-minute odor identification test: reliability, normative data, and investigations in patients with olfactory loss. Ann Otol Rhinol Laryngol 110:976–981

    Article  CAS  PubMed  Google Scholar 

  66. Haehner A, Mayer AM, Landis BN et al. (2009) High test-retest reliability of the extended version of the “Sniffin’ Sticks” test. Chem Senses 34:705–711

    Article  PubMed  Google Scholar 

  67. Sorokowska A, Albrecht E, Haehner A et al (2015) Extended version of the “Sniffin’ Sticks” identification test: test-retest reliability and validity. J Neurosci Methods 243:111–114

    Article  CAS  PubMed  Google Scholar 

  68. Kobal G (2003) Electrophysiological measurement of olfactory function. In: Doty RL (ed) Handbook of Olfaction and Gustation. Marcel Dekker INC, New York, pp 229–249

    Google Scholar 

  69. Rombaux P, Duprez T, Hummel T (2009) Olfactory bulb volume in the clinical assessment of olfactory dysfunction. Rhinology 47:3–9

    CAS  PubMed  Google Scholar 

  70. Wang J, You H, Liu JF et al (2011) Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol 32:677–681

    Article  CAS  PubMed  Google Scholar 

  71. Ottaviano G, Cantone E, D’Errico A et al. (2015) Sniffin’ Sticks and olfactory system imaging in patients with Kallmann syndrome. Int Forum Allergy Rhinol. doi:10.1002/alr.21550

    PubMed  Google Scholar 

  72. Baba T, Takeda A, Kikuchi A et al (2011) Association of olfactory dysfunction and brain. Metabolism in Parkinson’s disease. Mov Disord 26:621–628

    Article  PubMed  Google Scholar 

  73. Berendse HW, Ponsen MM (2009) Diagnosing premotor Parkinson’s disease using a two-step approach combining olfactory testing and DAT SPECT imaging. Parkinsonism Relat Disord 15(Suppl. 3):S26–S30

    Article  PubMed  Google Scholar 

  74. Deeb J, Shah M, Muhammed N et al (2010) A basic smell test is as sensitive as a dopamine transporter scan: comparison of olfaction, taste and DaTSCAN in the diagnosis of Parkinson’s disease. QJM 103:941–952

    Article  CAS  PubMed  Google Scholar 

  75. Mesholam RI, Moberg PJ, Mahr RN et al (1998) Olfaction in neurodegenerative disease. A meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch Neurol 55:84–90

    Article  CAS  PubMed  Google Scholar 

  76. Herting B, Schulze S, Reichmann H et al (2008) A longitudinal study of olfactory function in patients with idiopathic Parkinson’s disease. J Neurol 255:367–370

    Article  PubMed  Google Scholar 

  77. Wong KK, Muller ML, Kuwabara H et al (2010) Olfactory loss and nigrostriatal dopaminergic denervation in the elderly. Neurosci Lett 484:163–167

    Article  CAS  PubMed  Google Scholar 

  78. Wang J, Eslinger PJ, Doty RL et al (2010) Olfactory deficit detected by fMRI in early Alzheimer’s disease. Brain Res 1357:184–194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Babizhayev MA, DeyevAI Yegorov YE (2011) Olfactory dysfunction and cognitive impairment in age-related neurodegeneration: prevalence related to patient selection, diagnostic criteria and therapeutic treatment of aged clients receiving clinical neurology and community-based care. Curr Clin Pharmacol 6:236–259

    Article  CAS  PubMed  Google Scholar 

  80. Koivisto H, Grimm MO, Rothhaar TL et al (2014) Special lipid-based diets alleviate cognitive deficits in the APPswe/PS1dE9 transgenic mouse model of Alzheimer’s disease independent of brain amyloid deposition. J Nutr Biochem 25:157–169

    Article  CAS  PubMed  Google Scholar 

  81. Bernal-Mondragón C, Rivas-Arancibia S, Kendrick KM et al (2013) Estradiol prevents olfactory dysfunction induced by A-β 25-35 injection in hippocampus. BMC Neurosci 14:104

    Article  PubMed Central  PubMed  Google Scholar 

  82. Haehner A, Tosch C, Wolz M et al (2013) Olfactory training in patients with Parkinson’s disease. PLoS ONE 8:e61680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Knudsen K, Flensborg Damholdt M, Mouridsen K et al. (2015) Olfactory function in Parkinson’s disease—effects of training. Acta Neurol Scand (Epub)

  84. Cain WS, Gent JF, Goodspeed RB et al (1988) Evaluation of olfactory dysfunction in the Connecticut Chemosensory Clinical Research Center. Laryngoscope 98:83–88

    Article  CAS  PubMed  Google Scholar 

  85. Takagi SF (1989) Standardized olfactometries in Japan–a review over 10 years. Chem Senses 14:25–46

    Article  CAS  Google Scholar 

  86. Liu HC, Wang SJ, Lin KP et al (1995) Performance on a smell screening test (the MODSIT): a study of 510 predominantly illiterate Chinese subjects. Physiol Behav 58:1251–1255

    Article  CAS  PubMed  Google Scholar 

  87. Nordin S, Bramerson A, Liden E et al (1998) The Scandinavian odor-identification test: development, reliability, validity and normative data. Acta Otolaryngol 118:226–234

    Article  CAS  PubMed  Google Scholar 

  88. Simmen D, Briner HR, Hess K (1999) Screening test des Geruchssinnes mit Riechdiskette. Laryngorhinootologie 78:125–130

    Article  CAS  PubMed  Google Scholar 

  89. Kobal G, Palisch K, Wolf SR et al (2001) A threshold-like measure for the assessment of olfactory sensitivity: the “random” procedure. Eur Arch Otorhinolaryngol 258:168–172

    Article  CAS  PubMed  Google Scholar 

  90. Kurtz DB, White TL, Sheehe PR et al (2001) Odorant confusion matrix: the influence of patient history on patterns of odorant identification and misidentification in hyposmia. Physiol Behav 72:595–602

    Article  CAS  PubMed  Google Scholar 

  91. Kobayashi M, Saito S, Kobayakawa T et al (2006) Cross-cultural comparison of data using the odor stick identification test for Japanese (OSIT-J). Chem Senses 31:335–342

    Article  PubMed  Google Scholar 

  92. Cardesín A, Alobid I, Benítez P et al (2006) Barcelona Smell Test—24 (BAST-24): validation and smell characteristics in the healthy Spanish population. Rhinology 44:83–89

    PubMed  Google Scholar 

  93. Krantz EM, Schubert CR, Dalton DS et al (2009) Test-retest reliability of the San Diego odor identification test and comparison with the brief smell identification test. Chem Senses 34:435–440

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We are deeply indebted to the language editing by Professor Dennis Marino, Padova.

Conflict of interest

None of the authors have any conflicts of interest, financial or otherwise.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Authors and Affiliations

  1. Department of Neurosciences, Otolaryngology Section, University of Padova, Via Giustiniani 2, 35100, Padua, Italy

    Giancarlo Ottaviano, Giuliana Frasson, Ennio Nardello & Alessandro Martini

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  1. Giancarlo Ottaviano
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  2. Giuliana Frasson
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Correspondence to Giancarlo Ottaviano.

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Ottaviano, G., Frasson, G., Nardello, E. et al. Olfaction deterioration in cognitive disorders in the elderly. Aging Clin Exp Res 28, 37–45 (2016). https://doi.org/10.1007/s40520-015-0380-x

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