Skip to main content

Advertisement

SpringerLink
Log in

Comparison of olfactory and gustatory disorders in Alzheimer’s disease

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Patients with Alzheimer’s disease (AD) develop olfactory and gustatory disorders. However, the order of failure and relevance of the pathophysiology are unclear. We compared olfactory identification and whole mouth gustation in patients with AD to those with mild cognitive impairment (MCI) and to healthy controls (HC) and assessed correlations with pathophysiology. Patients with AD (n = 40), MCI (n = 34), and HC (n = 40) were recruited. We performed the Odor Stick Identification Test for Japanese (OSIT-J), gustatory test by the intraoral dropping method using taste solutions, Mini-Mental State Examination (MMSE), Alzheimer’s Disease Assessment Scale-cognitive subscale Japanese version (ADAS-J cog), Touch Panel-type Dementia Assessment Scale (TDAS), and measurement of amyloid β (Aβ) 42 and phosphorylated tau (p-tau) 181 levels in cerebrospinal fluid (CSF). Patients with AD and MCI had lower OSIT-J scores than did the HC. The OSIT-J score was correlated with the MMSE, ADAS-J cog, TDAS, and Aβ42 results. There were no significant differences in the gustatory test scores among the three groups. The gustatory test score was only correlated with the MMSE, ADAS-J cog, and TDAS results. Olfactory function decreased in AD and MCI patients and was associated with CSF biomarker levels and cognitive disorders. The results suggest that olfactory function is impaired in early stage of AD. Gustatory function was not correlated with CSF biomarkers, which suggests that it may not be impaired in early stage of AD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Kang JH, Korecka M, Toledo JB, Trojanowski JQ, Shaw LM (2013) Clinical utility and analytical challenges in measurement of cerebrospinal fluid amyloid-β(1-42) and τ proteins as Alzheimer disease biomarkers. Clin Chem 59:903–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Thal DR, Rüb U, Orantes M, Braak H (2002) Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791–1800

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404

    Article  PubMed  PubMed Central  Google Scholar 

  5. Jimbo D, Inoue M, Taniguchi M, Urakami K (2011) Specific feature of olfactory dysfunction with Alzheimer’s disease inspected by the Odor Stick Identification Test. Psychogeriatrics 11:196–204

    Article  PubMed  Google Scholar 

  6. Peters JM, Hummel T, Kratzsch T, Lötsch J, Skarke C, Frölich L (2003) Olfactory function in mild cognitive impairment and Alzheimer’s disease: an investigation using psychophysical and electrophysiological techniques. Am J Psychiatry 160:1995–2002

    Article  PubMed  Google Scholar 

  7. Eibenstein A, Fioretti AB, Simaskou MN, Sucapane P, Mearelli S, Mina C et al (2005) Olfactory screening test in mild cognitive impairment. Neurol Sci 26:156–160

    Article  CAS  PubMed  Google Scholar 

  8. Roberts RO, Christianson TJ, Kremers WK, Mielke MM, Machulda MM, Vassilaki M et al (2016) Association between olfactory dysfunction and amnestic mild cognitive impairment and Alzheimer disease dementia. JAMA Neurol 73:93–101

    Article  PubMed  PubMed Central  Google Scholar 

  9. Steinbach S, Hundt W, Vaitl A, Heinrich P, Förster S, Bürger K et al (2010) Taste in mild cognitive impairment and Alzheimer’s disease. J Neurol 257:238–246

    Article  PubMed  Google Scholar 

  10. Ogawa T, Irikawa N, Yanagisawa D, Shiino A, Tooyama I, Shimizu T (2017) Taste detection and recognition thresholds in Japanese patients with Alzheimer-type dementia. Auris Nasus Larynx 44:168–173

    Article  PubMed  Google Scholar 

  11. Sewards TV (2004) Dual separate pathways for sensory and hedonic aspects of taste. Brain Res Bull 62:271–283

    Article  PubMed  Google Scholar 

  12. Kim S, Youn YC, Hsiung GY, Ha SY, Park KY, Shin HW et al (2011) Voxel-based morphometric study of brain volume changes in patients with Alzheimer’s disease assessed according to the Clinical Dementia Rating score. J Clin Neurosci 18:916–921

    Article  PubMed  Google Scholar 

  13. Lang CJ, Leuschner T, Ulrich K, Stössel C, Heckmann JG, Hummel T (2006) Taste in dementing diseases and parkinsonism. J Neurol Sci 248:177–184

    Article  CAS  PubMed  Google Scholar 

  14. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington, D.C.

    Google Scholar 

  15. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (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 34:939–944

    Article  CAS  PubMed  Google Scholar 

  16. Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194

    Article  CAS  PubMed  Google Scholar 

  17. Petersen RC (2011) Clinical practice. Mild cognitive impairment. N Engl J Med 364:2227–2234

    Article  CAS  PubMed  Google Scholar 

  18. Saito S, Ayabe-Kanamura S, Takashima Y, Gotow N, Naito N, Nozawa T et al (2006) Development of a smell identification test using a novel stick-type odor presentation kit. Chem Senses 31:379–391

    Article  PubMed  Google Scholar 

  19. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  20. Homma A, Fukuzawa K, Tsukada Y, Ishii T, Hasegawa K (1992) Development of a Japanese version of Alzheimer’s disease assessment scale (ADAS). Jpn J Geriatr Psychiatry 3:647–655 (in Japanese)

    Google Scholar 

  21. Inoue M, Jimbo D, Taniguchi M, Urakami K (2011) Touch Panel-type Dementia Assessment Scale: a new computer-based rating scale for Alzheimer’s disease. Psychogeriatrics 11:28–33

    Article  PubMed  Google Scholar 

  22. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM et al (2011) Toward defining the preclinical stages of Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:280–292

    Article  PubMed  PubMed Central  Google Scholar 

  23. Berti V, Polito C, Lombardi G, Ferrari C, Sorbi S, Pupi A (2016) Rethinking on the concept of biomarkers in preclinical Alzheimer’s disease. Neurol Sci 37:663–672

    Article  PubMed  Google Scholar 

  24. Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC et al (2012) Clinical and biomarker changes in dominantly inherited Alzheimer’s disease. N Engl J Med 367:795–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lafaille-Magnan ME, Poirier J, Etienne P, Tremblay-Mercier J, Frenette J, Rosa-Neto P et al (2017) Odor identification as a biomarker of preclinical AD in older adults at risk. Neurology 89:327–335

    Article  PubMed  PubMed Central  Google Scholar 

  26. Doty RL, Brugger WE, Jurs PC, Orndorff MA, Snyder PJ, Lowry LD (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol Behav 20:175–185

    Article  CAS  PubMed  Google Scholar 

  27. Williams SS, Williams J, Combrinck M, Christie S, Smith AD, McShane R (2009) Olfactory impairment is more marked in patients with mild dementia with Lewy bodies than those with mild Alzheimer disease. J Neurol Neurosurg Psychiatry 80:667–670

    Article  CAS  PubMed  Google Scholar 

  28. Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (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 

  29. Yoshinaka M, Ikebe K, Uota M, Ogawa T, Okada T, Inomata C et al (2016) Age and sex differences in the taste sensitivity of young adult, young-old and old-old Japanese. Geriatr Gerontol Int 16:1281–1288

    Article  PubMed  Google Scholar 

  30. Frank ME, Hettinger TP, Mott AE (1992) The sense of taste: neurobiology, aging, and medication effects. Crit Rev Oral Biol Med 3:371–393

    Article  CAS  PubMed  Google Scholar 

  31. Kai K, Hashimoto M, Amano K et al (2015) Relationship between eating disturbance and dementia severity in patients with Alzheimer’s disease. PLoS One 10:e0133666. https://doi.org/10.1371/journal.pone.0133666

    Article  PubMed  PubMed Central  Google Scholar 

  32. Crum RM, Anthony JC, Bassett SS, Folstein MF (1993) Population-based norms for the mini-mental state examination by age and educational level. JAMA 269:2386–2391

    Article  CAS  PubMed  Google Scholar 

  33. Yamaguchi M, Mori K (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci U S A 102:9697–9702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Jimbo D, Kimura Y, Taniguchi M, Inoue M, Urakami K (2009) Effect of aromatherapy on patients with Alzheimer’s disease. Psychogeriatrics 9:173–179

    Article  PubMed  Google Scholar 

  35. Tsurugizawa T, Kondoh T, Torii K (2008) Forebrain activation induced by postoral nutritive substances in rats. Neuroreport 19:1111–1115

    Article  CAS  PubMed  Google Scholar 

  36. Tomoe M, Inoue Y, Sanbe A, Toyama K, Yamamoto S, Komatsu T (2009) Clinical trial of glutamate for the improvement of nutrition and health in the elderly. Ann N Y Acad Sci 1170:82–86

    Article  CAS  PubMed  Google Scholar 

  37. Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L (1984) Smell identification ability: changes with age. Science 226:1441–1443

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the patients who participated in our study and their families. We also thank the staff at Shinsei Hospital (Kurayoshi, Japan) who cooperated in this study.

Author information

Authors and Affiliations

  1. Department of Biological Regulation, School of Health Science, Faculty of Medicine, Tottori University, 86 Nishicho, Yonago, 683-8503, Japan

    Minoru Kouzuki, Tetsuya Suzuki, Masaya Nagano, Syouta Nakamura, Yuto Katsumata, Ayumi Takamura & Katsuya Urakami

Authors
  1. Minoru Kouzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tetsuya Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masaya Nagano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Syouta Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuto Katsumata
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ayumi Takamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Katsuya Urakami
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Minoru Kouzuki.

Ethics declarations

The study design was approved by the ethics committee of Tottori University. The research protocol was explained to the patients and/or relatives, and informed consent for their participation was obtained.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kouzuki, M., Suzuki, T., Nagano, M. et al. Comparison of olfactory and gustatory disorders in Alzheimer’s disease. Neurol Sci 39, 321–328 (2018). https://doi.org/10.1007/s10072-017-3187-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-017-3187-z

Keywords

Search

Navigation