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Open Access 01-12-2020 | Smelling Disorder | Research article

Correlations of apathy with clinical symptoms of Alzheimer’s disease and olfactory dysfunctions: a cross-sectional study

Authors: Shu-yang Yu, Teng-hong Lian, Peng Guo, Li-xia Li, Du-yu Ding, Dan-ning Li, Li Liu, Hui Zhao, Yang Hu, Li-jun Zuo, Jun-hua Gao, Qiu-jin Yu, Zhao Jin, Rui-dan Wang, Rong-yan Zhu, Xiao-min Wang, Wei Zhang

Published in: BMC Neurology | Issue 1/2020

Abstract

Background

Apathy is one of the most common symptoms of Alzheimer’s disease (AD), however, correlations of apathy with demographic variables, cognitive functions, neuropsychiatric symptoms, activity of daily living and olfactory functions in AD patients are still lacking comprehensive investigations.

Methods

This is a cross-sectional study. Total 124 typical AD patients were consecutively recruited from April 2014 to April 2017. In 124 AD patients, 47 cases (37.9%) were male and 77 cases were female; patients’ age were 43–93 years with an average of 68 years. Patients were divided into AD with apathy (AD-A) and AD with no apathy (AD-NA) groups according to the score of Modified Apathy Evaluation Scale, then were evaluated cognitive functions, neuropsychiatric symptoms and activity of daily living, and tested olfactory functions. Above variables were compared between AD-A and AD-NA groups. Further correlation analyses and linear regression analysis were performed between apathy and above variables.

Results

Compared with AD-NA group, global cognitive level, verbal memory, verbal fluency and activity of daily living were significantly compromised in AD-A group (P < 0.002); depression and agitation were severely displayed in AD-A group (P < 0.002). Apathy was negatively correlated with global cognitive function, verbal memory, verbal fluency and activity of daily living (P < 0.05). There was no significant difference of olfactory functions between the two groups (P > 0.002), and correlations between apathy and olfactory threshold, olfactory identification and global olfactory function were significant (P < 0.05) but quite weak (|r| < 0.3). Further linear regression analysis showed that only verbal fluency and instrumental activities of daily living were independently associated with apathy.

Conclusions

Independent correlations among apathy, verbal fluency and instrumental activities of daily living in AD patients might be related to the common brain area involved in their pathogeneses.

Onyike CU, Sheppard JM, Tschanz JT, Norton MC, Green RC, Steinberg M, et al. Epidemiology of apathy in older adults: the Cache County study. Am J Geriatr Psychiatry. 2007;15(5):365–75. https://doi.org/10.1097/01.JGP.0000235689.42910.0d.CrossRefPubMed

Mega MS, Cummings JL, Fiorello T, Gornbein J. The spectrum of behavioral changes in Alzheimer's disease. Neurology. 1996;46(1):130–5.CrossRef

Wesson DW, Wilson DA, Nixon RA. Should olfactory dysfunction be used as a biomarker of Alzheimer's disease? Expert Rev Neurother. 2010;10(5):633–5. https://doi.org/10.1586/ern.10.33.CrossRefPubMedPubMedCentral

Wilson RS, Arnold SE, Schneider JA, Boyle PA, Buchman AS, Bennett DA. Olfactory impairment in presymptomatic Alzheimer’s disease. Ann N Y Acad Sci. 2009;1170:730–5. https://doi.org/10.1111/j.1749-6632.2009.04013.x.CrossRefPubMedPubMedCentral

Dubois B, Feldman HH, Jacova C, Hampel H, Molinuevo JL, Blennow K, et al. Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria. Lancet Neurol. 2014;13(6):614–29. https://doi.org/10.1016/S1474-4422(14)70090-0.CrossRefPubMed

Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG. Reliability, validity, and clinical correlates of apathy in Parkinson's disease. J Neuropsychiatr Clin Neurosci. 1992;4(2):134–9. https://doi.org/10.1176/jnp.4.2.134.CrossRef

Marin RS. Differential diagnosis and classification of apathy. Am J Psychiatry. 1990;147(1):22–30. https://doi.org/10.1176/ajp.147.1.22.CrossRefPubMed

Cockrell JR, Folstein MF. Mini-mental state examination (MMSE). Psychopharmacol Bull. 1988;24(4):689–92.PubMed

Guo Q, Zhao Q, Chen M, Ding D, Hong Z. A comparison study of mild cognitive impairment with 3 memory tests among Chinese individuals. Alzheimer Dis Assoc Disord. 2009;23(3):253–9. https://doi.org/10.1097/WAD.0b013e3181999e92.CrossRefPubMed

10.

A S. Symbol digits modalities test: manual. Los Angeles: Western Psychological Services; 1982.

11.

Guo QHSY, Yuan J, Hong Z, Lu CZ. Application of eight executive tests in participants at Shanghai communities. Chin J Behavioral Med Sci. 2007;16:4.

12.

Sebaldt R, Dalziel W, Massoud F, Tanguay A, Ward R, Thabane L, et al. Detection of cognitive impairment and dementia using the animal fluency test: the DECIDE study. Can J Neurol Sci. 2009;36(5):599–604. https://doi.org/10.1017/s0317167100008106.CrossRefPubMed

13.

Guo QLC, Hong Z. Application of Rey-Osterrieth complex figure test in Chinese normal old people. Chin J Clin Psychol. 2000;8:3.

14.

Whisman MA, Strosahl K, Fruzzetti AE, Schmaling KB, Jacobson NS, Miller DM. A structured interview version of the Hamilton rating scale for depression: reliability and validity. Psychol Assess. 1989;1(3):238–41.CrossRef

15.

Guy W. HAMA Hamilton anxiety scale. ECDEU Assessment Manual. 1976;5.

16.

Lin LC, Kao CC, Tzeng YL, Lin YJ. Equivalence of Chinese version of the Cohen-Mansfield agitation inventory. J Adv Nurs. 2007;59(2):178–85. https://doi.org/10.1111/j.1365-2648.2007.04303.x.CrossRefPubMed

17.

Katz S, Ford AB, Moskowitz RW, Jackson BA, Jaffe MW. Studies of illness in the aged. The index of Adl: a standardized measure of biological and psychosocial function. JAMA. 1963;185:914–9. https://doi.org/10.1001/jama.1963.03060120024016.CrossRefPubMed

18.

Hummel T, Kobal G, Gudziol H, Mackay-Sim A. 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. Eur Arch Otorhinolaryngol. 2007;264(3):237–43. https://doi.org/10.1007/s00405-006-0173-0.CrossRefPubMed

19.

Boyle PA, Malloy PF. Treating apathy in Alzheime’s disease. Dement Geriatr Cogn Disord. 2004;17(1–2):91–9. https://doi.org/10.1159/000074280.CrossRefPubMed

20.

Rea R, Carotenuto A, Traini E, Fasanaro AM, Manzo V, Amenta F. Apathy treatment in Alzheimer's disease: interim results of the ASCOMALVA trial. J Alzheimers Dis. 2015;48(2):377–83. https://doi.org/10.3233/JAD-141983.CrossRefPubMed

21.

Cohen-Mansfield J, Golander H, Cohen R. Rethinking psychosis in dementia: an analysis of antecedents and explanations. Am J Alzheimers Dis Other Dement. 2017;32(5):265–71. https://doi.org/10.1177/1533317517703478.CrossRef

22.

Porsteinsson AP, Drye LT, Pollock BG, Devanand DP, Frangakis C, Ismail Z, et al. Effect of citalopram on agitation in Alzheimer disease: the CitAD randomized clinical trial. JAMA. 2014;311(7):682–91. https://doi.org/10.1001/jama.2014.93.CrossRefPubMedPubMedCentral

23.

Li XL, Hu N, Tan MS, Yu JT, Tan L. Behavioral and psychological symptoms in Alzheimer's disease. Biomed Res Int. 2014;2014:927804. https://doi.org/10.1155/2014/927804.CrossRefPubMedPubMedCentral

24.

Holthoff VA, Beuthien-Baumann B, Kalbe E, Ludecke S, Lenz O, Zundorf G, et al. Regional cerebral metabolism in early Alzheimer’s disease with clinically significant apathy or depression. Biol Psychiatry. 2005;57(4):412–21. https://doi.org/10.1016/j.biopsych.2004.11.035.CrossRefPubMed

25.

Husebo BS, Ballard C, Sandvik R, Nilsen OB, Aarsland D. Efficacy of treating pain to reduce behavioural disturbances in residents of nursing homes with dementia: cluster randomised clinical trial. BMJ. 2011;343:d4065. https://doi.org/10.1136/bmj.d4065.CrossRefPubMedPubMedCentral

26.

Guercio BJ, Donovan NJ, Munro CE, Aghjayan SL, Wigman SE, Locascio JJ, et al. The apathy evaluation scale: a comparison of subject, informant, and clinician report in cognitively Normal elderly and mild cognitive impairment. J Alzheimers Dis. 2015;47(2):421–32. https://doi.org/10.3233/JAD-150146.CrossRefPubMedPubMedCentral

27.

Kurz A, Thone-Otto A, Cramer B, Egert S, Frolich L, Gertz HJ, et al. CORDIAL: cognitive rehabilitation and cognitive-behavioral treatment for early dementia in Alzheimer disease: a multicenter, randomized, controlled trial. Alzheimer Dis Assoc Disord. 2012;26(3):246–53. https://doi.org/10.1097/WAD.0b013e318231e46e.CrossRefPubMed

28.

Nowrangi MA. Neuropsychiatric aspects of Alzheimer dementia: from mechanism to treatment. Psychiatr Clin North Am. 2020;43(2):383–97. https://doi.org/10.1016/j.psc.2020.02.012.CrossRefPubMed

29.

Lanctot KL, Herrmann N, Rothenburg L, Eryavec G. Behavioral correlates of GABAergic disruption in Alzheimer's disease. Int Psychogeriatr. 2007;19(1):151–8. https://doi.org/10.1017/S1041610206003899.CrossRefPubMed

30.

Matthews KL, Chen CP, Esiri MM, Keene J, Minger SL, Francis PT. Noradrenergic changes, aggressive behavior, and cognition in patients with dementia. Biol Psychiatry. 2002;51(5):407–16. https://doi.org/10.1016/s0006-3223(01)01235-5.CrossRefPubMed

31.

Nagata T, Kobayashi N, Shinagawa S, Yamada H, Kondo K, Nakayama K. Plasma BDNF levels are correlated with aggressiveness in patients with amnestic mild cognitive impairment or Alzheimer disease. J Neural Transm (Vienna). 2014;121(4):433–41. https://doi.org/10.1007/s00702-013-1121-y.CrossRef

32.

Seligman SC, Kamath V, Giovannetti T, Arnold SE, Moberg PJ. Olfaction and apathy in Alzheimer’s disease, mild cognitive impairment, and healthy older adults. Aging Ment Health. 2013;17(5):564–70. https://doi.org/10.1080/13607863.2013.768208.CrossRefPubMedPubMedCentral

Title: Correlations of apathy with clinical symptoms of Alzheimer’s disease and olfactory dysfunctions: a cross-sectional study
Authors: Shu-yang Yu
Teng-hong Lian
Peng Guo
Li-xia Li
Du-yu Ding
Dan-ning Li
Li Liu
Hui Zhao
Yang Hu
Li-jun Zuo
Jun-hua Gao
Qiu-jin Yu
Zhao Jin
Rui-dan Wang
Rong-yan Zhu
Xiao-min Wang
Wei Zhang
Publication date: 01-12-2020
Publisher: BioMed Central
Keywords: Smelling Disorder
Mood Disorders
Alzheimer's Disease
Affective Disorder
Smelling Disorder
Alzheimer's Disease
Agitation
Published in: BMC Neurology / Issue 1/2020
Electronic ISSN: 1471-2377
DOI: https://doi.org/10.1186/s12883-020-01978-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Correlations of apathy with clinical symptoms of Alzheimer’s disease and olfactory dysfunctions: a cross-sectional study

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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