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Mild Cognitive Impairment in Parkinson’s Disease: Clustering and Switching Analyses in Verbal Fluency Test

Published online by Cambridge University Press:  12 May 2017

Iván Galtier*
Affiliation:
School of Psychology. University of La Laguna, Tenerife, Spain
Antonieta Nieto
Affiliation:
School of Psychology. University of La Laguna, Tenerife, Spain
Jesús N. Lorenzo
Affiliation:
Departament of Neurology, N.S. La Candelaria University Hospital, Ctra. Gral. del Rosario, S/C de Tenerife. Spain
José Barroso
Affiliation:
School of Psychology. University of La Laguna, Tenerife, Spain
*
Correspondence and reprint requests to: Ivan Galtier, School of Psychology, University of La Laguna, 38205, La Laguna, Tenerife, Spain. E-mail: [email protected].

Abstract

Objectives: Mild cognitive impairment is common in non-demented Parkinson disease patients (PD-MCI) and is considered as a risk factor for dementia. Executive dysfunction has been widely described in PD and the Verbal Fluency Tests (VFT) are often used for executive function assessment in this pathology. The Movement Disorder Society (MDS) published guidelines for PD-MCI diagnosis in 2012. However, no investigation has focused on the qualitative analysis of VFT in PD-MCI. The aim of this work was to study the clustering and switching strategies in VFT in PD-MCI patients. Moreover, these variables are considered as predictors for PD-MCI diagnosis. Methods: Forty-three PD patients and twenty normal controls were evaluated with a neuropsychological protocol and the MDS criteria for PD-MCI were applied. Clustering and switching analysis were conducted for VFT. Results: The percentage of patients diagnosed with PD-MCI was 37.2%. The Mann-Whitney U test analysis showed that PD-MCI performed poorly in different cognitive measures (digit span, Wisconsin Card Sorting Test, judgment of line orientation, and comprehension test), compared to PD patients without mild cognitive impairment (PD-nMCI). Phonemic fluency analyses showed that PD-MCI patients produced fewer words and switched significantly less, compared to controls and PD-nMCI. Concerning semantic fluency, the PD-MCI group differed significantly, compared to controls and PD-nMCI, in switches. Discriminant function analyses and logistic regression analyses revealed that switches predicted PD-MCI. Conclusions: PD-MCI patients showed poor performance in VFT related to the deficient use of production strategies. The number of switches is a useful predictor for incident PD-MCI. (JINS, 2017, 23, 511–520)

Type
Special Section: Mild Cognitive Impairment
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

Aarsland, D., Zaccai, J., & Brayne, C. (2005). A systematic review of prevalence studies of dementia in Parkinson’s disease. Movement Disorders, 20(10), 12551263. http://doi.org/10.1002/mds.20527 Google Scholar
Akamatsu, T., Fukuyama, H., & Kawamata, T. (2008). The effects of visual, auditory, and mixed cues on choice reaction in Parkinson’s disease. Journal of the Neurological Sciences, 269(1–2), 118125. http://doi.org/10.1016/j.jns.2008.01.002 CrossRefGoogle ScholarPubMed
Barone, P., Aarsland, D., Burn, D., Emre, M., Kulisevsky, J., & Weintraub, D. (2011). Cognitive impairment in nondemented Parkinson’s disease. Movement Disorders, 26(14), 24832495. http://doi.org/10.1002/mds.23919 CrossRefGoogle ScholarPubMed
Beck, A.T., Ward, C.H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561571.CrossRefGoogle ScholarPubMed
Benton, A., Hamsher, K., & Sivan, A. (1989). Multilingual aphasia examination (2nd ed.). Iowa City, IA: AJA Associates: University of Iowa.Google Scholar
Benton, A., Hamsher, S., Varney, O., & Spreen, N. (1983). Contributions to neuropsychological assessment: A clinical manual. New York: Oxford University Press.Google Scholar
Beyer, M.K., Bronnick, K.S., Hwang, K.S., Bergsland, N., Tysnes, O.B., Larsen, J.P., & Apostolova, L.G. (2013). Verbal memory is associated with structural hippocampal changes in newly diagnosed Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 84(1), 2328. http://doi.org/10.1136/jnnp-2012-303054 Google Scholar
Bouquet, C.A., Bonnaud, V., & Gil, R. (2003). Investigation of supervisory attentional system functions in patients with Parkinson’s disease using the Hayling task. Journal of Clinical and Experimental Neuropsychology, 25(6), 751760. http://doi.org/10.1076/jcen.25.6.751.16478 Google Scholar
Brand, M., Labudda, K., Kalbe, E., Hilker, R., Emmans, D., Fuchs, G.,& Markowitsch, H.J. (2004). Decision-making impairments in patients with Parkinson’s disease. Behavioural Neurology, 15(3–4), 7785.Google Scholar
Broeders, M., de Bie, R.M.A., Velseboer, D.C., Speelman, J.D., Muslimovic, D., & Schmand, B. (2013). Evolution of mild cognitive impairment in Parkinson disease. Neurology, 81(4), 346352. http://doi.org/10.1212/WNL.0b013e31829c5c86 Google Scholar
Camicioli, R.M., Wieler, M., de Frias, C.M., & Martin, W.R.W. (2008). Early, untreated Parkinson’s disease patients show reaction time variability. Neuroscience Letters, 441(1), 7780. http://doi.org/10.1016/j.neulet.2008.06.004 CrossRefGoogle ScholarPubMed
Delis, D., Kramer, J., Kaplan, E., & Ober, B. (1987). California Verbal Learning Test. Research Edition Manual. New York: Psychological Corporation.Google Scholar
Domellöf, M.E., Ekman, U., Forsgren, L., & Elgh, E. (2015). Cognitive function in the early phase of Parkinson’s disease, a five-year follow-up. Acta Neurologica Scandinavica, 132(2), 7988. http://doi.org/10.1111/ane.12375 CrossRefGoogle ScholarPubMed
Emre, M., Aarsland, D., Brown, R., Burn, D.J., Duyckaerts, C., Mizuno, Y.,& Dubois, B. (2007). Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Movement Disorders, 22(12), 16891707; quiz 1837. http://doi.org/10.1002/mds.21507 Google Scholar
Epker, M.O., Lacritz, L.H., & Munro Cullum, C. (1999). Comparative analysis of qualitative verbal fluency performance in normal elderly and demented populations. Journal of Clinical and Experimental Neuropsychology, 21(4), 425434. http://doi.org/10.1076/jcen.21.4.425.890 Google Scholar
Fahn, S., & Elton, R. (1987). Unified Parkinson’s Disease Rating Scale. In S. Fahn, C. Marsden, M. Goldstein & D. Calne (Eds.), Recent Developments in Parkinson’s disease (pp. 153163). New York: Raven Press.Google Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198.Google Scholar
Galtier, I., Nieto, A., Lorenzo, J.N., & Barroso, J. (2014). Cognitive impairment in Parkinson’s disease: More than a frontostriatal dysfunction. The Spanish Journal of Psychology, 17, 18. http://doi.org/10.1017/sjp.2014.69 Google Scholar
Galtier, I., Nieto, A., Lorenzo, J.N., & Barroso, J. (2016). Mild cognitive impairment in Parkinson’s disease: Diagnosis and progression to dementia. Journal of Clinical and Experimental Neuropsychology, 38(1), 4050. http://doi.org/10.1080/13803395.2015.1087465 CrossRefGoogle ScholarPubMed
Grossman, M., Carvell, S., Stern, M.B., Gollomp, S., & Hurtig, H.I. (1992). Sentence comprehension in Parkinson’s disease: The role of attention and memory. Brain and Language, 42(4), 347384.CrossRefGoogle ScholarPubMed
Heaton, R. (1981). Wisconsin Card Sorting Test manual. Odessa, FL: Psychological Assessment Resources.Google Scholar
Henry, J.D., & Crawford, J.R. (2004). A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology, 18(2), 284295. http://doi.org/10.1037/0894-4105.18.2.284 Google Scholar
Hobson, P., & Meara, J. (2015). Mild cognitive impairment in Parkinson’s disease and its progression onto dementia: A 16-year outcome evaluation of the Denbighshire cohort. International Journal of Geriatric Psychiatry, 30(10), 10481055. http://doi.org/10.1002/gps.4261 Google Scholar
Hoehn, M.M., & Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427442.CrossRefGoogle ScholarPubMed
Hsieh, Y.-H., Chen, K.-J., Wang, C.-C., & Lai, C.-L. (2008). Cognitive and motor components of response speed in the stroop test in Parkinson’s disease patients. The Kaohsiung Journal of Medical Sciences, 24(4), 197203. http://doi.org/10.1016/S1607-551X(08)70117-7 CrossRefGoogle ScholarPubMed
Hughes, A.J., Daniel, S.E., Kilford, L., & Lees, A.J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery, and Psychiatry, 55(3), 181184.Google Scholar
Janvin, C.C., Larsen, J.P., Aarsland, D., & Hugdahl, K. (2006). Subtypes of mild cognitive impairment in Parkinson’s disease: Progression to dementia. Movement Disorders, 21(9), 13431349. http://doi.org/10.1002/mds.20974 Google Scholar
Jokinen, P., Brück, A., Aalto, S., Forsback, S., Parkkola, R., & Rinne, J.O. (2009). Impaired cognitive performance in Parkinson’s disease is related to caudate dopaminergic hypofunction and hippocampal atrophy. Parkinsonism and Related Disorders, 15(2), 8893. http://doi.org/10.1016/j.parkreldis.2008.03.005 CrossRefGoogle ScholarPubMed
Koerts, J., Meijer, H.A., Colman, K.S.F., Tucha, L., Lange, K.W., & Tucha, O. (2013). What is measured with verbal fluency tests in Parkinson’s disease patients at different stages of the disease? Journal of Neural Transmission (Vienna, Austria: 1996), 120(3), 403411. http://doi.org/10.1007/s00702-012-0885-9 Google Scholar
Kosmidis, M.H., Vlahou, C.H., Panagiotaki, P., & Kiosseoglou, G. (2004). The verbal fluency task in the Greek population: Normative data, and clustering and switching strategies. Journal of the International Neuropsychological Society, 10(2), 164172. http://doi.org/10.1017/S1355617704102014 Google Scholar
Lee, J.E., Cho, K.H., Song, S.K., Kim, H.J., Lee, H.S., Sohn, Y.H., & Lee, P.H. (2014). Exploratory analysis of neuropsychological and neuroanatomical correlates of progressive mild cognitive impairment in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 85(1), 716. http://doi.org/10.1136/jnnp-2013-305062 Google Scholar
Liozidou, A., Potagas, C., Papageorgiou, S.G., & Zalonis, I. (2012). The role of working memory and information processing speed on wisconsin card sorting test performance in Parkinson disease without dementia. Journal of Geriatric Psychiatry and Neurology, 25(4), 215221. http://doi.org/10.1177/0891988712466456 CrossRefGoogle ScholarPubMed
Litvan, I., Goldman, J.G., Tröster, A.I., Schmand, B.A., Weintraub, D., Petersen, R.C., & Emre, M. (2012). Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Movement Disorders, 27(3), 349356. http://doi.org/10.1002/mds.24893 Google Scholar
Marek, K., Jennings, D., Lasch, S., Siderowf, A., Tanner, C., Simuni, T., & Taylor, P. (2011). The Parkinson Progression Marker Initiative (PPMI). Progress in Neurobiology, 95(4), 629635. http://doi.org/10.1016/j.pneurobio.2011.09.005 Google Scholar
Mimura, M., Oeda, R., & Kawamura, M. (2006). Impaired decision-making in Parkinson’s disease. Parkinsonism & Related Disorders, 12(3), 169175. http://doi.org/10.1016/j.parkreldis.2005.12.003 Google Scholar
Muslimovic, D., Post, B., Speelman, J.D., & Schmand, B. (2007). Motor procedural learning in Parkinson’s disease. Brain, 130(Pt 11), 28872897. http://doi.org/10.1093/brain/awm211 Google Scholar
Paolo, A.M., Axelrod, B.N., Tröster, A.I., Blackwell, K.T., & Koller, W.C. (1996). Utility of a Wisconsin Card Sorting Test short form in persons with Alzheimer’s and Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 18(6), 892897. http://doi.org/10.1080/01688639608408310 Google Scholar
Pedersen, K.F., Larsen, J.P., Tysnes, O.-B., & Alves, G. (2013). Prognosis of mild cognitive impairment in early Parkinson disease: The Norwegian ParkWest Study. JAMA Neurology, 70(5), 580586. http://doi.org/10.1001/jamaneurol.2013.2110 Google Scholar
Pereira, J.B., Junqué, C., Martí, M.J., Ramirez-Ruiz, B., Bartrés-Faz, D., & Tolosa, E. (2009). Structural brain correlates of verbal fluency in Parkinson’s disease. Neuroreport, 20(8), 741744. http://doi.org/10.1097/WNR.0b013e328329370b CrossRefGoogle ScholarPubMed
Rosenthal, L.S., Drake, D., Alcalay, R.N., Babcock, D., Bowman, F.D., Chen-Plotkin, A., & Gwinn, K. (2015). The NINDS Parkinson’s disease biomarkers program. Movement Disorders. http://doi.org/10.1002/mds.26438 CrossRefGoogle Scholar
Santangelo, G., Vitale, C., Picillo, M., Moccia, M., Cuoco, S., Longo, K., & Barone, P. (2015). Mild Cognitive Impairment in newly diagnosed Parkinson’s disease: A longitudinal prospective study. Parkinsonism & Related Disorders, 21(10), 12191226. http://doi.org/10.1016/j.parkreldis.2015.08.024 CrossRefGoogle ScholarPubMed
Schneider, J.S. (2007). Behavioral persistence deficit in Parkinson’s disease patients. European Journal of Neurology, 14(3), 300304. http://doi.org/10.1111/j.1468-1331.2006.01647.x Google Scholar
Skeel, R.L., Crosson, B., Nadeau, S.E., Algina, J., Bauer, R.M., & Fennell, E.B. (2001). Basal ganglia dysfunction, working memory, and sentence comprehension in patients with Parkinson’s disease. Neuropsychologia, 39(9), 962971. http://doi.org/10.1016/S0028-3932(01)00026-4 Google Scholar
Stefanova, E., Žiropadja, L., Stojković, T., Stanković, I., Tomić, A., Ječmenica-Lukić, M., & Kostić, V. (2015). Mild cognitive impairment in early Parkinson’s disease using the Movement Disorder Society Task Force Criteria: Cross-sectional study in Hoehn and Yahr Stage 1. Dementia and Geriatric Cognitive Disorders, 40(3–4), 199209. http://doi.org/10.1159/000433421 Google Scholar
Tröster, A.I., Fields, J.A., Testa, J.A., Paul, R.H., Blanco, C.R., Hames, K.A., & Beatty, W.W. (1998). Cortical and subcortical influences on clustering and switching in the performance of verbal fluency tasks. Neuropsychologia, 36(4), 295304.CrossRefGoogle ScholarPubMed
Troyer, A.K., Moscovitch, M., & Winocur, G. (1997). Clustering and switching as two components of verbal fluency: Evidence from younger and older healthy adults. Neuropsychology, 11(1), 138146.CrossRefGoogle ScholarPubMed
Troyer, A.K., Moscovitch, M., Winocur, G., Alexander, M.P., & Stuss, D. (1998). Clustering and switching on verbal fluency: The effects of focal frontal- and temporal-lobe lesions. Neuropsychologia, 36(6), 499504.Google Scholar
Troyer, A.K., Moscovitch, M., Winocur, G., Leach, L., & Freedman, M. (1998). Clustering and switching on verbal fluency tests in Alzheimer’s and Parkinson’s disease. Journal of the International Neuropsychological Society, 4(2), 137143.Google Scholar
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale - Administration and Scoring Manual (3rd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale - Third Edition. Technical Manual (3rd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Williams-Gray, C.H., Evans, J.R., Goris, A., Foltynie, T., Ban, M., Robbins, T.W., & Barker, R.A. (2009). The distinct cognitive syndromes of Parkinson’s disease: 5 year follow-up of the CamPaIGN cohort. Brain, 132(Pt 11), 29582969. http://doi.org/10.1093/brain/awp245 Google Scholar
Williams-Gray, C.H., Foltynie, T., Brayne, C.E.G., Robbins, T.W., & Barker, R.A. (2007). Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain, 130(Pt 7), 17871798. http://doi.org/10.1093/brain/awm111 CrossRefGoogle Scholar