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Open Access 01-12-2017 | Research

Cognitive profile in prodromal dementia with Lewy bodies

Authors: Jennifer Kemp, Nathalie Philippi, Clélie Phillipps, Catherine Demuynck, Timothée Albasser, Catherine Martin-Hunyadi, Catherine Schmidt-Mutter, Benjamin Cretin, Frédéric Blanc

Published in: Alzheimer's Research & Therapy | Issue 1/2017

Abstract

Background

Cortical and subcortical cognitive impairments have been found in dementia with Lewy bodies (DLB). Roughly, they comprise visuoconstructive and executive dysfunction, whereas memory would remain relatively spared. However, the cognitive profile of patients with prodromal DLB remains poorly illustrated to date.

Methods

We included 37 patients with prodromal DLB (age 67.2 ± 8.6 years, 18 men, Mini Mental State Examination [MMSE] score 27.4 ± 2) and 29 healthy control subjects (HCs; age 68.8 ± 7.9 years, 15 men, MMSE score 29.0 ± 0.9). They were presented with an extensive neuropsychological test battery to assess memory; speed of processing; executive function; visuoperceptual, visuospatial and visuoconstructive abilities; language; and social cognition.

Results

Compared with HCs, patients had lower scores on a visual recognition memory test (Delayed Matching to Sample-48 items; p ≤ 0.021) and lower free recall (all p ≤ 0.035), but not total recall, performance on a verbal episodic memory test (Free and Cued Selective Reminding Test). Short-term memory (p = 0.042) and working memory (p = 0.002) scores were also lower in patients. Assessment of executive function showed no slowing but overall lower performance in patients than in HCs (all p ≤ 0.049), whereas assessment of instrumental function yielded mixed results. Indeed, patients had lower scores on language tests (p ≤ 0.022), apraxia for pantomime of tool use (p = 0.002) and imitation of meaningless gesture (p = 0.005), as well as weakened visuospatial abilities (p = 0.047). Visuoconstruction was also impaired in patients. However, visuoperceptual abilities did not differ between groups. Finally, theory of mind abilities were lower in patients than in HCs (p < 0.05), but their emotion recognition abilities were similar.

Conclusions

This study presents the cognitive profile in patients with prodromal DLB. In line with the literature on DLB with dementia, our results show lower performance on tests of executive function and visuoconstruction. However, we found, from a prodromal stage of DLB, memory (free recall and visual recognition) and social cognition deficits, as well as weakened visuospatial and praxic abilities.

McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology. 2005;65(12):1863–72.CrossRefPubMed

Zaccai J, McCracken C, Brayne C. A systematic review of prevalence and incidence studies of dementia with Lewy bodies. Age Ageing. 2005;34(6):561–6.CrossRefPubMed

Vann Jones SA, O’Brien JT. The prevalence and incidence of dementia with Lewy bodies: a systematic review of population and clinical studies. Psychol Med. 2014;44(4):673–83.CrossRefPubMed

Boeve BF. Mild cognitive impairment associated with underlying Alzheimer’s disease versus Lewy body disease. Parkinsonism Relat Disord. 2012;18 Suppl 1:S41–4.CrossRefPubMed

Donaghy PC, McKeith IG. The clinical characteristics of dementia with Lewy bodies and a consideration of prodromal diagnosis. Alzheimers Res Ther. 2014;6(4):46.CrossRefPubMedPubMedCentral

Auning E, Rongve A, Fladby T, Booij J, Hortobagyi T, Siepel FJ, et al. Early and presenting symptoms of dementia with Lewy bodies. Dement Geriatr Cogn Disord. 2011;32(3):202–8.CrossRefPubMed

Chiba Y, Fujishiro H, Iseki E, Ota K, Kasanuki K, Hirayasu Y, et al. Retrospective survey of prodromal symptoms in dementia with Lewy bodies: comparison with Alzheimer’s disease. Dement Geriatr Cogn Disord. 2012;33(4):273–81.CrossRefPubMed

Fujishiro H, Iseki E, Nakamura S, Kasanuki K, Chiba Y, Ota K, et al. Dementia with Lewy bodies: early diagnostic challenges. Psychogeriatrics. 2013;13(2):128–38.CrossRefPubMed

Beach TG, White CL, Hladik 3rd CL, Sabbagh MN, Connor DJ, Shill HA, et al. Olfactory bulb α-synucleinopathy has high specificity and sensitivity for Lewy body disorders. Acta Neuropathol. 2009;117(2):169–74.CrossRefPubMed

10.

Beach TG, Adler CH, Sue LI, Vedders L, Lue L, White CL, et al. Multi-organ distribution of phosphorylated α-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol. 2010;119(6):689–702.CrossRefPubMedPubMedCentral

11.

Blanc F, Colloby SJ, Philippi N, de Petigny X, Jung B, Demuynck C, et al. Cortical thickness in dementia with Lewy bodies and Alzheimer’s disease: a comparison of prodromal and dementia stages. PLoS One. 2015;10(6), e0127396.CrossRefPubMedPubMedCentral

12.

Blanc F, Colloby SJ, Cretin B, Loureiro de Sousa P, Demuynck C, O’Brien JT, et al. Grey matter atrophy in prodromal stage of dementia with Lewy bodies and Alzheimer’s disease. Alzheimers Res Ther. 2016;8(31):1.

13.

Fujishiro H, Iseki E, Murayama N, Yamamoto R, Higashi S, Kasanuki K, et al. Diffuse occipital hypometabolism on [¹⁸F]-FDG PET scans in patients with idiopathic REM sleep behavior disorder: prodromal dementia with Lewy bodies? Psychogeriatrics. 2010;10(3):144–52.CrossRefPubMed

14.

Noe E, Marder K, Bell KL, Jacobs DM, Manly JJ, Stern Y. Comparison of dementia with Lewy bodies to Alzheimer’s disease and Parkinson’s disease with dementia. Mov Disord. 2004;19(1):60–7.CrossRefPubMed

15.

Metzler-Baddeley C. A review of cognitive impairments in dementia with Lewy bodies relative to Alzheimer’s disease and Parkinson’s disease with dementia. Cortex. 2007;43(5):583–600.CrossRefPubMed

16.

Troster AI. Neuropsychological characteristics of dementia with Lewy bodies and Parkinson’s disease with dementia: differentiation, early detection, and implications for “mild cognitive impairment” and biomarkers. Neuropsychol Rev. 2008;18(1):103–19.CrossRefPubMed

17.

Simard M, van Reekum R, Cohen T. A review of the cognitive and behavioral symptoms in dementia with Lewy bodies. J Neuropsychiatry Clin Neurosci. 2000;12(4):425–50.CrossRefPubMed

18.

Calderon J, Perry RJ, Erzinclioglu SW, Berrios GE, Dening TR, Hodges JR. Perception, attention, and working memory are disproportionately impaired in dementia with Lewy bodies compared with Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 2001;70(2):157–64.CrossRefPubMedPubMedCentral

19.

Collerton D, Burn D, McKeith IG, O’Brien JT. Systematic review and meta-analysis show that dementia with Lewy bodies is a visual-perceptual and attentional-executive dementia. Dement Geriatr Cogn Disord. 2003;16(4):229–37.CrossRefPubMed

20.

Aarsland D, Litvan I, Salmon D, Galasko D, Wentzel-Larsen T, Larsen JP. Performance on the Dementia Rating Scale in Parkinson’s disease with dementia and dementia with Lewy bodies: comparison with progressive supranuclear palsy and Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 2003;74(9):1215–20.CrossRefPubMedPubMedCentral

21.

Mori E. Dementia with Lewy bodies [in Japanese]. Nihon Ronen Igakkai Zasshi. 2000;37(10):772–6.CrossRefPubMed

22.

Hansen L, Salmon D, Galasko D, Masliah E, Katzman R, DeTeresa R, et al. The Lewy body variant of Alzheimer’s disease: a clinical and pathologic entity. Neurology. 1990;40(1):1–8.CrossRefPubMed

23.

Ayre G, Ballard C, Pincock C, McKeith IG, Sahgal A, Wesnes K. Double dissociation between dementia with Lewy bodies and Alzheimer’s disease on tests of attentional and mnemonic function: the role of the basal forebrain. J Psychopharmacol. 1998;12(Suppl):A62–8.

24.

Oda H, Yamamoto Y, Maeda K. Neuropsychological profile of dementia with Lewy bodies. Psychogeriatrics. 2009;9(2):85–90.CrossRefPubMed

25.

Ferman TJ, Smith GE, Kantarci K, Boeve BF, Pankratz VS, Dickson DW, et al. Nonamnestic mild cognitive impairment progresses to dementia with Lewy bodies. Neurology. 2013;81(23):2032–8.CrossRefPubMedPubMedCentral

26.

Yoshizawa H, Vonsattel JP, Honig LS. Early neuropsychological discriminants for Lewy body disease: an autopsy series. J Neurol Neurosurg Psychiatry. 2013;84(12):1326–30.CrossRefPubMed

27.

Petrova M, Mehrabian-Spasova S, Aarsland D, Raycheva M, Traykov L. Clinical and neuropsychological differences between mild Parkinson’s disease dementia and dementia with Lewy bodies. Dement Geriatr Cogn Dis Extra. 2015;5(2):212–20.CrossRefPubMedPubMedCentral

28.

Petrova M, Pavlova R, Zhelev Y, Mehrabian S, Raycheva M, Traykov L. Investigation of neuropsychological characteristics of very mild and mild dementia with Lewy bodies. J Clin Exp Neuropsychol. 2016;38(3):354–60.CrossRefPubMed

29.

Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med. 2004;256(3):183–94.CrossRefPubMed

30.

American Psychiatric Association. Diagnostic and statistical manual of mental disorders: DSM-5. 5th ed. Arlington, VA: American Psychiatric Publishing; 2013.CrossRef

31.

Barberger-Gateau P, Commenges D, Gagnon M, Letenneur L, Sauvel C, Dartigues JF. Instrumental activities of daily living as a screening tool for cognitive impairment and dementia in elderly community dwellers. J Am Geriatr Soc. 1992;40(11):1129–34.CrossRefPubMed

32.

Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 1969;9(3):179–86.CrossRefPubMed

33.

Israel L, Waintraub L. Autonomie ou capacité fonctionnelle? Revue critique de quelques échelles actuellement utilisées en gériatrie pour l’évaluation des activités de la vie quotidienne. Psychol Med (Paris). 1986;18(14):2225–31.

34.

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

35.

Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P, et al. Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry. 1992;55(10):967–72.CrossRefPubMedPubMedCentral

36.

Dubois B, Feldman HH, Jacova C, DeKosky ST, Barberger-Gateau P, Cummings J, et al. Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol. 2007;6(8):734–46.CrossRefPubMed

37.

Lehmann S, Dumurgier J, Schraen S, Wallon D, Blanc F, Magnin E, et al. A diagnostic scale for Alzheimer’s disease based on cerebrospinal fluid biomarker profiles. Alzheimers Res Ther. 2014;6(3):38.CrossRefPubMedPubMedCentral

38.

Van der Linden M, Coyette F, Poitrenaud J, Kalafat M, Calicis F, Wyns C, et al. L’épreuve de rappel libre/rappel indicé à 16 items (RL/RI‐16). In: Van der Linden M, Adam S, Agniel A, Baisset‐Mouly C, editors. L’évaluation des troubles de la mémoire. Présentation de quatre tests de mémoire épisodique (avec leur étalonnage). Marseille, France: Solal; 2004. p. 25–47.

39.

Barbeau E, Tramoni E, Joubert S, Mancini J, Ceccaldi M, Poncet M, et al. Évaluation de la mémoire de reconnaissance visuelle: normalisation d’une nouvelle épreuve en choix forcé et utilité en neuropsychologie clinique. In: Van der Linden M, Adam S, Agniel A, Baisset‐Mouly C, editors. L’évaluation des troubles de la mémoire. Présentation de quatre tests de mémoire épisodique (avec leur étalonnage). Marseille, France: Solal; 2004. p. 85–101.

40.

Wechsler D. Wechsler Adult Intelligence Scale—3rd Edition (WAIS-3). San Antonio, TX: Pearson Clinical Assessment; 1997.

41.

Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a Frontal Assessment Battery at bedside. Neurology. 2000;55(11):1621–6.CrossRefPubMed

42.

Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19(2):203–14.CrossRefPubMed

43.

Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y. Formal and semantic lexical evocation in normal subjects: performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg. 1990;90(4):207–17.PubMed

44.

Deloche G, Hannequin D. Test de dénomination orale d’images – DO80. Paris: Editions du centre de psychologie appliquées; 1997.

45.

Rey A. Test de copie et de reproduction de mémoire de figures géométriques complexes. Paris: Editions du centre de psychologie appliquées; 1959.

46.

Warrington EK, James M. The Visual Object and Space Perception Battery. Bury St. Edmunds, UK: Thames Valley Test Company; 1991.

47.

Mahieux-Laurent F, Fabre C, Galbrun E, Dubrulle A, Moroni C, groupe de réflexion sur les praxies du CMRR Île-de-France Sud. Validation of a brief screening scale evaluating praxic abilities for use in memory clinics: evaluation in 419 controls, 127 mild cognitive impairment and 320 demented patients [in French]. Rev Neurol (Paris). 2009;165(6-7):560–7.CrossRef

48.

Bertoux M, Funkiewiez A, O’Callaghan C, Dubois B, Hornberger M. Sensitivity and specificity of ventromedial prefrontal cortex tests in behavioral variant frontotemporal dementia. Alzheimers Dement. 2013;9(5 Suppl):S84–94.CrossRefPubMed

49.

Stone VE, Baron-Cohen S, Knight RT. Frontal lobe contributions to theory of mind. J Cogn Neurosci. 1998;10(5):640–56.CrossRefPubMed

50.

Ekman P, Friesen W. Pictures of Facial Affect. Palo Alto, CA: Consulting Psychologists Press; 1976.

51.

Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry. 2001;42(2):241–51.CrossRefPubMed

52.

Metz-Lutz MN, Kremin H, Deloche G, Hannequin D, Ferrand I, Perrier D, et al. Standardisation d’un test de dénomination orale: contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. Rev Neuropsychol. 1991;1(1):73–95.

53.

Mitolo M, Salmon DP, Gardini S, Galasko D, Grossi E, Caffarra P. The new Qualitative Scoring MMSE Pentagon Test (QSPT) as a valid screening tool between autopsy-confirmed dementia with Lewy bodies and Alzheimer’s disease. J Alzheimers Dis. 2014;39(4):823–32.PubMedPubMedCentral

54.

Li X, Rastogi P, Gibbons JA, Chaudhury S. Visuo-cognitive skill deficits in Alzheimer’s disease and Lewy body disease: a comparative analysis. Ann Indian Acad Neurol. 2014;17(1):12–8.CrossRefPubMedPubMedCentral

55.

Nagahama Y, Okina T, Suzuki N. Impaired imitation of gestures in mild dementia: comparison of dementia with Lewy bodies, Alzheimer’s disease and vascular dementia. J Neurol Neurosurg Psychiatry. 2015;86(11):1248–52.CrossRefPubMed

56.

Cormack F, Aarsland D, Ballard C, Tovee MJ. Pentagon drawing and neuropsychological performance in dementia with Lewy bodies, Alzheimer’s disease, Parkinson’s disease and Parkinson’s disease with dementia. Int J Geriatr Psychiatry. 2014;19(4):371–7.CrossRef

57.

Cagnin A, Bussè C, Gardini S, Jelcic N, Guzzo C, Gnoato F, et al. Clinical and cognitive phenotype of mild cognitive impairment evolving to dementia with Lewy bodies. Dement Geriatr Cogn Dis Extra. 2015;5(3):442–9.CrossRefPubMedPubMedCentral

58.

Pal A, Biswas A, Pandit A, Roy A, Guin D, Gangopadhyay G, et al. Study of visuospatial skill in patients with dementia. Ann Indian Acad Neurol. 2016;19(1):83–8.CrossRefPubMedPubMedCentral

59.

Ota K, Murayama N, Kasanuki K, Kondo D, Fujishiro H, Arai H, et al. Visuoperceptual assessments for differentiating dementia with Lewy bodies and Alzheimer’s disease: illusory contours and other neuropsychological examinations. Arch Clin Neuropsychol. 2015;30(3):256–63.CrossRefPubMed

60.

Sahgal A, Galloway PH, McKeith IG, Lloyd S, Cook JH, Ferrier IN, et al. Matching-to-sample deficits in patients with senile dementias of the Alzheimer and Lewy body types. Arch Neurol. 1992;49(10):1043–6.CrossRefPubMed

61.

Mondon K, Gochard A, Marque A, Armand A, Beauchamp D, Prunier C, et al. Visual recognition memory differentiates dementia with Lewy bodies and Parkinson’s disease dementia. J Neurol Neurosurg Psychiatry. 2007;78(7):738–41.CrossRefPubMedPubMedCentral

62.

Philippi N, Noblet V, Duron E, Cretin B, Boully C, Wisniewski I, et al. Exploring anterograde memory: a volumetric MRI study in patients with mild cognitive impairment. Alzheimers Res Ther. 2016;8(1):26.CrossRefPubMedPubMedCentral

63.

Lambon-Ralph MA, Powell J, Howard D, Whitworth AB, Garrard P, Hodges JR. Semantic memory is impaired in both dementia with Lewy bodies and dementia of Alzheimer’s type: a comparative neuropsychological study and literature review. J Neurol Neurosurg Psychiatry. 2001;70(2):149–56.CrossRefPubMed

64.

Ferman TJ, Smith GE, Boeve BF, Graff-Radford NR, Lucas JA, Knopman DS, et al. Neuropsychological differentiation of dementia with Lewy bodies from normal aging and Alzheimer’s disease. Clin Neuropsychol. 2006;20(4):623–36.CrossRefPubMed

65.

Troster AI, Fields JA, Testa JA, Paul RH, Blanco CR, Hames KA, et al. Cortical and subcortical influences on clustering and switching in the performance of verbal fluency tasks. Neuropsychologia. 1998;36(4):295–304.CrossRefPubMed

66.

Troyer AK, Moscovitch M, Winocur G, Leach L, Freedman M. Clustering and switching on verbal fluency tests in Alzheimer’s and Parkinson’s disease. J Int Neuropsychol Soc. 1998;4(2):137–43.CrossRefPubMed

67.

Heitz C, Noblet V, Phillipps C, Cretin B, Vogt N, Philippi N, et al. Cognitive and affective theory of mind in dementia with Lewy bodies and Alzheimer’s disease. Alzheimers Res Ther. 2016;8(1):10.CrossRefPubMedPubMedCentral

68.

Aboulafia-Brakha T, Christe B, Martory MD, Annoni JM. Theory of mind tasks and executive functions: a systematic review of group studies in neurology. J Neuropsychol. 2011;5(Pt 1):39–55.CrossRefPubMed

69.

Ferman TJ, Smith GE, Boeve BF, Ivnik RJ, Petersen RC, Knopman D, et al. DLB fluctuations: specific features that reliably differentiate DLB from AD and normal aging. Neurology. 2004;62(2):181–7.CrossRefPubMed

Title: Cognitive profile in prodromal dementia with Lewy bodies
Authors: Jennifer Kemp
Nathalie Philippi
Clélie Phillipps
Catherine Demuynck
Timothée Albasser
Catherine Martin-Hunyadi
Catherine Schmidt-Mutter
Benjamin Cretin
Frédéric Blanc
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Alzheimer's Research & Therapy / Issue 1/2017
Electronic ISSN: 1758-9193
DOI: https://doi.org/10.1186/s13195-017-0242-1

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Springer Medicine

Cognitive profile in prodromal dementia with Lewy bodies

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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