Neuropsychiatric symptoms as early manifestation of Alzheimer’s disease

Česká verzia

Authors: V. Matušková; T. Nikolai; H. Marková; K. Čechová; J. Laczó; J. Hort; M. Vyhnálek
Authors place of work: Mezinárodní centrum klinického výzkumu, FN u sv. Anny v Brně ; Neurologická klinika 2. LF UK a FN Motol, Praha
Published in the journal: Cesk Slov Neurol N 2020; 83(1): 64-72
Category: Původní práce
doi: https://doi.org/10.14735/amcsnn202064

Neuropsychiatrické symptomy (NPS) jsou heterogenní skupina změn v osobnosti a chování, které lze pozorovat již v časných stadiích Alzheimerovy nemoci (AN). Mírná behaviorální porucha (mild behavioral impairment; MBI) je nová diagnostická kategorie popisující trvalé změny v osobnosti a chování s počátkem v pozdější fázi života. Na podkladě těchto kritérií byl vytvořen nový Dotazník mírné poruchy chování (Mild Behavioral Impairment Checklist; MBI-C) zaměřený na detekci NPS v časných stadiích AN. Cílem studie je představit námi adaptovanou českou verzi dotazníku MBI-C a studovat přítomnost a závažnost NPS na pilotním souboru pacientů.

Summary

Aim: Neuropsychiatric symptoms (NPS) are a heterogeneous group of changes in personality and behavior that can be observed already in early stages of Alzheimer’s disease (AD). Mild behavioral impairment (MBI) is a newly developed diagnostic category describing persistent changes in personality and behavior starting later in life. Based on these criteria, a new measure, the Mild Behavioral Impairment Checklist (MBI-C) has been developed, aimed at detecting NPS in early stages of AD. The aim of this study is to present the newly adapted Czech version of the MBI-C and to explore the presence of NPS in a pilot group of patients.

Patients and methods: The original MBI-C has been adapted to Czech and administered to close informants of 188 patients. The patients were divided according to the results of a complex neuropsychological, neurological examination and brain imaging into 3 groups: cognitively normal (N = 69), amnestic mild cognitive impairment (aMCI; N = 87) and dementia due to AD (N = 32).

Results: Patients with aMCI expressed in the MBI-C significantly more severe score compared to cognitively normal subjects and less severe compared to dementia patients. The differences were observed mainly in affective, motivation and impulse control domains.

Conclusion: The Czech version of the MBI-C detects the presence of NPS even before the onset of dementia syndrome and is useful in clinical practice.

Keywords:

mild cognitive impairment – neuropsychiatric symptoms – Alzheimer´s disease – mild behavioral impairment

Zdroje

1. Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med 2004; 256(3): 183– 194. doi: 10.1111/ j.1365-2796.2004.01388.x.

2. Albert MS, DeKosky ST, Dickson D et al. 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. Alzheimers Dement 2011; 7(3): 270– 279. doi: 10.1016/ j.jalz.2011.03.008.

3. Dubois B, Hampel H, Feldman HH et al. Preclinical Alzheimer’s disease: definition, natural history, and diagnostic criteria. Alzheimers Dement 2016; 12(3): 292– 323. doi: 10.1016/ j.jalz.2016.02.002.

4. Markova H, Andel R, Stepankova H et al. Subjective Cognitive complaints in cognitively healthy older adults and their relationship to cognitive performance and depressive symptoms. J Alzheimers Dis 2017; 59(3): 871– 881. doi: 10.3233/ JAD-160970.

5. Jessen F, Amariglio RE, van Boxtel M et al. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimers Dement 2014; 10(6): 844– 852. doi: 10.1016/ j.jalz.2014.01.001.

6. McKhann GM, Knopman DS, Chertkow H et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diag-nostic guidelines for Alzheimer’s disease. Alzheimers Dement J Alzheimers Assoc 2011; 7(3): 263– 269. doi: 10.1016/ j.jalz.2011.03.005.

7. Rascovsky K, Hodges JR, Knopman D et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain J Neurol 2011; 134(Pt 9): 2456– 2477. doi: 10.1093/ brain/ awr179.

8. McKeith IG, Boeve BF, Dickson DW et al. Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology 2017; 89(1): 88– 100. doi: 10.1212/ WNL.0000000000004058.

9. Ressner P, Hort J, Rektorová I et al. Doporučené postupy pro diagnostiku Alzheimerovy nemoci a dalších onemocnění spojených s demencí. Cesk Slov Neurol N 2008; 71/ 104(4): 494– 501.

10. Cerejeira J, Lagarto L, Mukaetova-Ladinska EB. Behavioral and psychological symptoms of dementia. Front Neurol 2012; 3: 73. doi: 10.3389/ fneur.2012.00073.

11. Apostolova LG, Cummings JL. Neuropsychiatric manifestations in mild cognitive impairment: a systematic review of the literature. Dement Geriatr Cogn Disord 2008; 25(2): 115– 126. doi: 10.1159/ 000112509.

12. Geda YE, Roberts RO, Knopman DS et al. Prevalence of neuropsychiatric symptoms in mild cognitive impairment and normal cognitive aging: population-based study. Arch Gen Psychiatry 2008; 65(10): 1193– 1198. doi: 10.1001/ archpsyc.65.10.1193.

13. Okura T, Plassman BL, Steffens DC et al. Prevalence of neuropsychiatric symptoms and their association with functional limitations in older adults in the United States: the aging, demographics, and memory study. J Am Geriatr Soc 2010; 58(2): 330– 337. doi: 10.1111/ j.1532-5415.2009.02680.x.

14. Gallagher D, Fischer CE, Iaboni A. Neuropsychiatric symptoms in mild cognitive impairment. Can J Psychiatry Rev Can Psychiatr 2017; 62(3): 161– 169. doi: 10.1177/ 0706743716648296.

15. Desmarais P, Lanctôt KL, Masellis M et al. Social inappropriateness in neurodegenerative disorders. Int Psychogeriatr 2018; 30(2): 197– 207. doi: 10.1017/ S10416102 17001260.

16. Fischer CE, Agüera-Ortiz L. Psychosis and dementia: risk factor, prodrome, or cause? Int Psychogeriatr 2018; 30(2): 209– 219. doi: 10.1017/ S1041610217000874.

17. Ismail Z, Gatchel J, Bateman DR et al. Affective and emotional dysregulation as pre-dementia risk markers: exploring the mild behavioral impairment symptoms of depression, anxiety, irritability, and euphoria. Int Psychogeriatr 2018; 30(2): 185– 196. doi: 10.1017/ S1041610217001880

18. Krell-Roesch J, Lowe VJ, Neureiter J et al. Depressive and anxiety symptoms and cortical amyloid deposition among cognitively normal elderly persons: the Mayo Clinic Study of Aging. Int Psychogeriatr 2018; 30(2): 245– 251. doi: 10.1017/ S1041610217002368.

19. Sherman C, Liu CS, Herrmann N et al. Prevalence, neurobiology, and treatments for apathy in prodromal dementia. Int Psychogeriatr 2018; 30(2): 177– 184. doi: 10.1017/ S1041610217000527.

20. Geda YE, Roberts RO, Mielke MM et al. Baseline neuropsychiatric symptoms and the risk of incident mild cognitive impairment: a population-based study. Am J Psychiatry 2014; 171(5): 572– 581. doi: 10.1176/ appi.ajp.2014.13060821.

21. Donovan NJ, Amariglio RE, Zoller AS et al. Subjective cognitive concerns and neuropsychiatric predictors of progression to the early clinical stages of Alzheimer disease. Am J Geriatr Psychiatry 2014; 22(12): 1642– 1651. doi: 10.1016/ j.jagp.2014.02.007.

22. Pink A, Stokin GB, Bartley MM et al. Neuropsychiatric symptoms, APOE ε4, and the risk of incident dementia: a population-based study. Neurology 2015; 84(9): 935– 943. doi: 10.1212/ WNL.0000000000001307.

23. Wise EA, Rosenberg PB, Lyketsos CG et al. Time course of neuropsychiatric symptoms and cognitive diag-nosis in National Alzheimer’s Coordinating Centers volunteers. Alzheimers Dement (Amst) 2019; 11: 333– 339. doi: 10.1016/ j.dadm.2019.02.006.

24. Rosenberg PB, Mielke MM, Appleby BS et al. The association of neuropsychiatric symptoms in MCI with incident dementia and Alzheimer disease. Am J Geriatr Psychiatry Off J Am Assoc Geriatr Psychiatry 2013; 21(7): 685– 695. doi: 10.1016/ j.jagp.2013.01.006.

25. Sugarman MA, Alosco ML, Tripodis Y et al. Neuropsychiatric symptoms and the diagnostic stability of mild cognitive impairment. J Alzheimers Dis 2018; 62(4): 1841– 1855. doi: 10.3233/ JAD-170527.

26. Singh-Manoux A, Dugravot A, Fournier A et al. Trajectories of depressive symptoms before diagnosis of dementia. JAMA Psychiatry 2017; 74(7): 712– 718. doi: 10.1001/ jamapsychiatry.2017.0660.

27. Steenland K, Karnes C, Seals R et al. Late-life depression as a risk factor for mild cognitive impairment or Alzheimer’s disease in 30 US Alzheimer’s disease centers. J Alzheimers Dis 2012; 31(2): 265– 275. doi: 10.3233/ JAD-2012-111922.

28. Tapiainen V, Hartikainen S, Taipale H et al. Hospital-treated mental and behavioral disorders and risk of Alzheimer’s disease: a nationwide nested case-control study. Eur Psychiatry 2017; 43: 92– 98. doi: 10.1016/ j.eurpsy.2017.02.486.

29. Andrews SJ, Ismail Z, Anstey KJ et al. Association of Alzheimer’s genetic loci with mild behavioral impairment. Am J Med Genet Part B Neuropsychiatr Genet 2018; 177(8): 727– 735. doi: 10.1002/ ajmg.b.32684.

30. Woolley JD, Khan BK, Murthy NK et al. The diagnostic challenge of psychiatric symptoms in neurodegenerative disease: rates of and risk factors for prior psychiatric diagnosis in patients with early neurodegenerative disease. J Clin Psychiatry 2011; 72(2): 126– 133. doi: 10.4088/ JCP.10m06382oli.

31. Ismail Z, Smith EE, Geda Y et al. Neuropsychiatric symptoms as early manifestations of emergent dementia: Provisional diagnostic criteria for mild behavioral impairment. Alzheimers Dement J Alzheimers Assoc 2016; 12(2): 195– 202. doi: 10.1016/ j.jalz.2015.05.017.

32. Taragano F, Allegri R, Krupitzki H et al. Mild behavioral impairment and risk of dementia. J Clin Psychiatry 2009; 70(4): 584– 592. doi: 10.4088/ jcp.08m04181.

33. Cummings JL. The Neuropsychiatric Inventory: assessing psychopathology in dementia patients. Neurology 1997; 48 (5 Suppl 6): S10– S16. doi: 10.1212/ wnl.48.5_suppl_6.10s.

34. Kaufer DI, Cummings JL, Ketchel P et al. Validation of the NPI-Q, a brief clinical form of the Neuropsychiatric Inventory. J Neuropsychiatry Clin Neurosci 2000; 12(2): 233– 239. doi: 10.1176/ jnp.12.2.233.

35. de Medeiros K, Robert P, Gauthier S et al. The Neuropsychiatric Inventory-Clinician rating scale (NPI-C): reliability and validity of a revised assessment of neuropsychiatric symptoms in dementia. Int Psychogeriatr 2010; 22(6): 984– 994. doi: 10.1017/ S1041610210000876.

36. Beck AT, Steer RA, Ball R et al. Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J Pers Assess 1996; 67(3): 588– 597. doi: 10.1207/ s15327752jpa6703_13.

37. Sheikh JI, Yesavage JA. Geriatric Depression Scale (GDS): recent evidence and development of a shorter version. Clin Gerontol J Aging Ment Health 1986; 5(1– 2): 165– 173. doi: 10.1300/ J018v05n01_09.

38. Beck AT, Epstein N, Brown G et al. An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 1988; 56(6): 893– 897. doi: 10.1037/ / 0022-006x.56.6.893.

39. The State-Trait Anxiety Inventory (STAI). [online]. Available from URL: https:/ / www.apa.org/ pi/ about/ publications/ caregivers/ practice-settings/ assessment/ tools/ trait-state.

40. Ismail Z, Agüera-Ortiz L, Brodaty H et al. The Mild Behavioral Impairment Checklist (MBI-C): a rating scale for neuropsychiatric symptoms in pre-dementia populations. J Alzheimers Dis 2017; 56(3): 929– 938. doi: 10.3233/ JAD-160979.

41. Mallo SC, Ismail Z, Pereiro AX et al. Assessing mild behavioral impairment with the mild behavioral impairment-checklist in people with mild cognitive impairment. J Alzheimers Dis 2018; 66(1): 83– 95. doi: 10.3233/ JAD-180131.

42. Mallo SC, Ismail Z, Pereiro AX et al. Assessing mild behavioral impairment with the mild behavioral impairment checklist in people with subjective cognitive decline. Int Psychogeriatr 2019; 31(2): 231– 239. doi: 10.1017/ S1041610218000698.

43. Štěpánková H, Nikolai T, Lukavský J et al. Mini‑Mental State Examination – česká normativní studie. Cesk Slov Neurol N 2015; 78/ 111(1): 57– 63.

44. Nikolai T, Stepankova H, Kopecek M et al. The uniform data set, Czech version: normative data in older adults from an international perspective. J Alzheimers Dis 2018; 61(3): 1233– 1240. doi: 10.3233/ JAD-170595.

45. Nikolai T, Štěpánková H, Michalec J et al. Testy verbální fluence, česká normativní studie pro osoby vyššího věku. Cesk Slov Neurol N 2015; 78/ 111(3): 292– 299. doi: 10.14735/ amcsnn2015292.

46. Bezdicek O, Stepankova H, Moták L et al. Czech version of Rey Auditory Verbal Learning test: normative data. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2014; 21(6): 693– 721. doi: 10.1080/ 13825585.2013.865699.

47. Drozdová K, Štěpánková H, Lukavský J et al. Normativní studie testu Reyovy-Osterriethovy komplexní figury v populaci českých seniorů. Cesk Slov Neurol N 2015; 78/ 111(5): 542– 549.

48. Sheikh F, Ismail Z, Mortby ME et al. Prevalence of mild behavioral impairment in mild cognitive impairment and subjective cognitive decline, and its association with caregiver burden. Int Psychogeriatr 2018; 30(2): 233– 244. doi: 10.1017/ S104161021700151X.

49. Mortby ME, Ismail Z, Anstey KJ. Prevalence estimates of mild behavioral impairment in a population-based sample of pre-dementia states and cognitively healthy older adults. Int Psychogeriatr 2018; 30(2): 221– 232. doi: 10.1017/ S1041610217001909.

50. Hill NL, Mogle J, Wion R et al. Subjective cognitive impairment and affective symptoms: a systematic review. Gerontologist 2016; 56(6): e109– e127. doi: 10.1093/ geront/ gnw091

51. MBItest. [online]. Available from URL: https:/ / mbitest.org/ .