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Published in: Journal of Neurology 10/2017

01-10-2017 | Original Communication

Do cognition and other non-motor symptoms decline similarly among patients with Parkinson’s disease motor subtypes? Findings from a 5-year prospective study

Authors: L. Arie, Talia Herman, S. Shema-Shiratzky, N. Giladi, J. M. Hausdorff

Published in: Journal of Neurology | Issue 10/2017

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Abstract

Among patients with Parkinson’s disease (PD), a wide range of motor and non-motor symptoms (NMS) are evident. PD is often divided into tremor dominant (TD) and postural instability gait difficulty (PIGD) motor subtypes. We evaluated the effect of disease duration and aimed to characterize whether there are differences in the deterioration of cognitive function and other NMS between the PIGD and TD subtypes. Sixty-three subjects were re-evaluated at the follow-up visit about 5 years after baseline examination. Cognitive function and other NMS were assessed. At follow-up, the PIGD and TD groups were similar with respect to medications, comorbidities and disease-related symptoms. There was a significant time effect for all measures, indicating deterioration and worsening in both groups. However, cognitive scores, particularly those related to executive function, became significantly worse in the PIGD with a more moderate decrease in the TD group. For example, the computerized global cognitive score declined in the PIGD group from 94.21 ± 11.88 to 83.91 ± 13.76, p < 0.001. This decline was significantly larger (p = 0.03) than the decrease observed in the TD group (96.56 ± 10.29 to 92.21 ± 14.20, p = 0.047). A significant group × time interaction effect was found for the change in global cognitive score (p = 0.047), the executive function index (p = 0.002) and accuracy on a motor-cognitive catch game (p = 0.008). In contrast, several NMS including depression, health-related quality of life and fear of falling deteriorated in parallel in both subtypes, with no interaction effect. The present findings highlight the difference in the natural history of the disease between the two PD “motor” subtypes. While the PIGD group demonstrated a significant cognitive decline, especially in executive functions, a more favorable course was observed in the TD subtype. This behavior was not seen in regards to the other NMS.
Literature
1.
go back to reference Jankovic J (2008) Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79:368–376CrossRefPubMed Jankovic J (2008) Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 79:368–376CrossRefPubMed
2.
go back to reference Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P (2011) Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 17:717–723CrossRefPubMed Chaudhuri KR, Odin P, Antonini A, Martinez-Martin P (2011) Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 17:717–723CrossRefPubMed
3.
go back to reference Duncan GW, Khoo TK, Yarnall AJ, O’Brien JT, Coleman SY, Brooks DJ, Barker RA, Burn DJ (2014) Health-related quality of life in early Parkinson’s disease: the impact of nonmotor symptoms. Mov Disord 29:195–202CrossRefPubMed Duncan GW, Khoo TK, Yarnall AJ, O’Brien JT, Coleman SY, Brooks DJ, Barker RA, Burn DJ (2014) Health-related quality of life in early Parkinson’s disease: the impact of nonmotor symptoms. Mov Disord 29:195–202CrossRefPubMed
4.
go back to reference Martinez-Martin P, Rodriguez-Blazquez C, Kurtis MM, Chaudhuri KR (2011) The impact of non-motor symptoms on health-related quality of life of patients with Parkinson’s disease. Mov Disord 26:399–406CrossRefPubMed Martinez-Martin P, Rodriguez-Blazquez C, Kurtis MM, Chaudhuri KR (2011) The impact of non-motor symptoms on health-related quality of life of patients with Parkinson’s disease. Mov Disord 26:399–406CrossRefPubMed
5.
go back to reference Swick TJ, Friedman JH, Chaudhuri KR, Surmann E, Boroojerdi B, Moran K, Ghys L, Trenkwalder C (2014) Associations between severity of motor function and nonmotor symptoms in Parkinson’s disease: a post hoc analysis of the RECOVER Study. Eur Neurol 71:140–147CrossRefPubMed Swick TJ, Friedman JH, Chaudhuri KR, Surmann E, Boroojerdi B, Moran K, Ghys L, Trenkwalder C (2014) Associations between severity of motor function and nonmotor symptoms in Parkinson’s disease: a post hoc analysis of the RECOVER Study. Eur Neurol 71:140–147CrossRefPubMed
6.
go back to reference Ray CK, Rojo JM, Schapira AH, Brooks DJ, Stocchi F, Odin P, Antonini A, Brown RJ, Martinez-Martin P (2013) A proposal for a comprehensive grading of Parkinson’s disease severity combining motor and non-motor assessments: meeting an unmet need. PLoS One 8:e57221CrossRef Ray CK, Rojo JM, Schapira AH, Brooks DJ, Stocchi F, Odin P, Antonini A, Brown RJ, Martinez-Martin P (2013) A proposal for a comprehensive grading of Parkinson’s disease severity combining motor and non-motor assessments: meeting an unmet need. PLoS One 8:e57221CrossRef
7.
go back to reference Zis P, Martinez-Martin P, Sauerbier A, Rizos A, Sharma JC, Worth PF, Sophia R, Silverdale M, Chaudhuri KR (2015) Non-motor symptoms burden in treated and untreated early Parkinson’s disease patients: argument for non-motor subtypes. Eur J Neurol 22:1145–1150CrossRefPubMed Zis P, Martinez-Martin P, Sauerbier A, Rizos A, Sharma JC, Worth PF, Sophia R, Silverdale M, Chaudhuri KR (2015) Non-motor symptoms burden in treated and untreated early Parkinson’s disease patients: argument for non-motor subtypes. Eur J Neurol 22:1145–1150CrossRefPubMed
9.
go back to reference Herman T, Weiss A, Brozgol M, Wilf-Yarkoni A, Giladi N, Hausdorff JM (2015) Cognitive function and other non-motor features in non-demented Parkinson’s disease motor subtypes. J Neural Transm 122:1115–1124CrossRefPubMed Herman T, Weiss A, Brozgol M, Wilf-Yarkoni A, Giladi N, Hausdorff JM (2015) Cognitive function and other non-motor features in non-demented Parkinson’s disease motor subtypes. J Neural Transm 122:1115–1124CrossRefPubMed
10.
go back to reference Linder J, Birgander R, Olsson I, Riklund K, Larsson AK, Edstrom M, Stenlund H, Forsgren L (2009) Degenerative changes were common in brain magnetic resonance imaging in patients with newly diagnosed Parkinson’s disease in a population-based cohort. J Neurol 256:1671–1680CrossRefPubMed Linder J, Birgander R, Olsson I, Riklund K, Larsson AK, Edstrom M, Stenlund H, Forsgren L (2009) Degenerative changes were common in brain magnetic resonance imaging in patients with newly diagnosed Parkinson’s disease in a population-based cohort. J Neurol 256:1671–1680CrossRefPubMed
11.
go back to reference Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245CrossRefPubMed Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245CrossRefPubMed
12.
go back to reference Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, Middelkoop HA, van Hilten JJ (2007) Cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:1182–1187CrossRefPubMedPubMedCentral Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, Middelkoop HA, van Hilten JJ (2007) Cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:1182–1187CrossRefPubMedPubMedCentral
13.
go back to reference Dirnberger G, Jahanshahi M (2013) Executive dysfunction in Parkinson’s disease: a review. J Neuropsychol 7:193–224CrossRefPubMed Dirnberger G, Jahanshahi M (2013) Executive dysfunction in Parkinson’s disease: a review. J Neuropsychol 7:193–224CrossRefPubMed
14.
go back to reference Kudlicka A, Clare L, Hindle JV (2011) Executive functions in Parkinson’s disease: systematic review and meta-analysis. Mov Disord 26:2305–2315CrossRefPubMed Kudlicka A, Clare L, Hindle JV (2011) Executive functions in Parkinson’s disease: systematic review and meta-analysis. Mov Disord 26:2305–2315CrossRefPubMed
15.
go back to reference Taylor JP, Rowan EN, Lett D, O’Brien JT, McKeith IG, Burn DJ (2008) Poor attentional function predicts cognitive decline in patients with non-demented Parkinson’s disease independent of motor phenotype. J Neurol Neurosurg Psychiatry 79:1318–1323CrossRefPubMed Taylor JP, Rowan EN, Lett D, O’Brien JT, McKeith IG, Burn DJ (2008) Poor attentional function predicts cognitive decline in patients with non-demented Parkinson’s disease independent of motor phenotype. J Neurol Neurosurg Psychiatry 79:1318–1323CrossRefPubMed
16.
go back to reference Hoops S, Nazem S, Siderowf AD, Duda JE, Xie SX, Stern MB, Weintraub D (2009) Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 73:1738–1745CrossRefPubMedPubMedCentral Hoops S, Nazem S, Siderowf AD, Duda JE, Xie SX, Stern MB, Weintraub D (2009) Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 73:1738–1745CrossRefPubMedPubMedCentral
17.
go back to reference Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40:1529–1534CrossRefPubMed Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I (1990) Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40:1529–1534CrossRefPubMed
18.
go back to reference Fahn S, Elton R, Members of the UPDRS development committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, pp 153–163 Fahn S, Elton R, Members of the UPDRS development committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, pp 153–163
19.
go back to reference Selikhova M, Kempster PA, Revesz T, Holton JL, Lees AJ (2013) Neuropathological findings in benign tremulous parkinsonism. Mov Disord 28:145–152CrossRefPubMed Selikhova M, Kempster PA, Revesz T, Holton JL, Lees AJ (2013) Neuropathological findings in benign tremulous parkinsonism. Mov Disord 28:145–152CrossRefPubMed
20.
go back to reference Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 28:668–670CrossRefPubMed Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 28:668–670CrossRefPubMed
21.
go back to reference Allcock LM, Kenny RA, Burn DJ (2006) Clinical phenotype of subjects with Parkinson’s disease and orthostatic hypotension: autonomic symptom and demographic comparison. Mov Disord 21:1851–1855CrossRefPubMed Allcock LM, Kenny RA, Burn DJ (2006) Clinical phenotype of subjects with Parkinson’s disease and orthostatic hypotension: autonomic symptom and demographic comparison. Mov Disord 21:1851–1855CrossRefPubMed
22.
go back to reference Ba F, Obaid M, Wieler M, Camicioli R, Martin WR (2016) Parkinson disease: the relationship between non-motor symptoms and motor phenotype. Can J Neurol Sci 43:261–267CrossRefPubMed Ba F, Obaid M, Wieler M, Camicioli R, Martin WR (2016) Parkinson disease: the relationship between non-motor symptoms and motor phenotype. Can J Neurol Sci 43:261–267CrossRefPubMed
23.
go back to reference Burn DJ, Landau S, Hindle JV, Samuel M, Wilson KC, Hurt CS, Brown RG (2012) Parkinson’s disease motor subtypes and mood. Mov Disord 27:379–386CrossRefPubMed Burn DJ, Landau S, Hindle JV, Samuel M, Wilson KC, Hurt CS, Brown RG (2012) Parkinson’s disease motor subtypes and mood. Mov Disord 27:379–386CrossRefPubMed
24.
go back to reference Reijnders JS, Ehrt U, Lousberg R, Aarsland D, Leentjens AF (2009) The association between motor subtypes and psychopathology in Parkinson’s disease. Parkinsonism Relat Disord 15:379–382CrossRefPubMed Reijnders JS, Ehrt U, Lousberg R, Aarsland D, Leentjens AF (2009) The association between motor subtypes and psychopathology in Parkinson’s disease. Parkinsonism Relat Disord 15:379–382CrossRefPubMed
25.
go back to reference Tremblay C, Achim AM, Macoir J, Monetta L (2013) The heterogeneity of cognitive symptoms in Parkinson’s disease: a meta-analysis. J Neurol Neurosurg Psychiatry 84:1265–1272CrossRefPubMed Tremblay C, Achim AM, Macoir J, Monetta L (2013) The heterogeneity of cognitive symptoms in Parkinson’s disease: a meta-analysis. J Neurol Neurosurg Psychiatry 84:1265–1272CrossRefPubMed
26.
go back to reference van der Hoek TC, Bus BA, Matui P, van der Marck MA, Esselink RA, Tendolkar I (2011) Prevalence of depression in Parkinson’s disease: effects of disease stage, motor subtype and gender. J Neurol Sci 310:220–224CrossRefPubMed van der Hoek TC, Bus BA, Matui P, van der Marck MA, Esselink RA, Tendolkar I (2011) Prevalence of depression in Parkinson’s disease: effects of disease stage, motor subtype and gender. J Neurol Sci 310:220–224CrossRefPubMed
27.
go back to reference Khoo TK, Yarnall AJ, Duncan GW, Coleman S, O’Brien JT, Brooks DJ, Barker RA, Burn DJ (2013) The spectrum of nonmotor symptoms in early Parkinson disease. Neurology 80:276–281CrossRefPubMedPubMedCentral Khoo TK, Yarnall AJ, Duncan GW, Coleman S, O’Brien JT, Brooks DJ, Barker RA, Burn DJ (2013) The spectrum of nonmotor symptoms in early Parkinson disease. Neurology 80:276–281CrossRefPubMedPubMedCentral
28.
go back to reference Wu Y, Guo XY, Wei QQ, Ou RW, Song W, Cao B, Zhao B, Shang HF (2016) Non-motor symptoms and quality of life in tremor dominant vs postural instability gait disorder Parkinson’s disease patients. Acta Neurol Scand 133:330–337CrossRefPubMed Wu Y, Guo XY, Wei QQ, Ou RW, Song W, Cao B, Zhao B, Shang HF (2016) Non-motor symptoms and quality of life in tremor dominant vs postural instability gait disorder Parkinson’s disease patients. Acta Neurol Scand 133:330–337CrossRefPubMed
29.
go back to reference Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A (2009) Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology 73:206–212CrossRefPubMed Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A (2009) Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology 73:206–212CrossRefPubMed
30.
go back to reference Burn DJ, Rowan EN, Allan LM, Molloy S, O’Brien JT, McKeith IG (2006) Motor subtype and cognitive decline in Parkinson’s disease, Parkinson’s disease with dementia, and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 77:585–589CrossRefPubMedPubMedCentral Burn DJ, Rowan EN, Allan LM, Molloy S, O’Brien JT, McKeith IG (2006) Motor subtype and cognitive decline in Parkinson’s disease, Parkinson’s disease with dementia, and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 77:585–589CrossRefPubMedPubMedCentral
31.
go back to reference Domellof ME, Elgh E, Forsgren L (2011) The relation between cognition and motor dysfunction in drug-naive newly diagnosed patients with Parkinson’s disease. Mov Disord 26:2183–2189CrossRefPubMed Domellof ME, Elgh E, Forsgren L (2011) The relation between cognition and motor dysfunction in drug-naive newly diagnosed patients with Parkinson’s disease. Mov Disord 26:2183–2189CrossRefPubMed
32.
go back to reference Lyros E, Messinis L, Papathanasopoulos P (2008) Does motor subtype influence neurocognitive performance in Parkinson’s disease without dementia? Eur J Neurol 15:262–267CrossRefPubMed Lyros E, Messinis L, Papathanasopoulos P (2008) Does motor subtype influence neurocognitive performance in Parkinson’s disease without dementia? Eur J Neurol 15:262–267CrossRefPubMed
33.
go back to reference Herman T, Weiss A, Brozgol M, Giladi N, Hausdorff JM (2014) Gait and balance in Parkinson’s disease subtypes: objective measures and classification considerations. J Neurol 261:2401–2410CrossRefPubMed Herman T, Weiss A, Brozgol M, Giladi N, Hausdorff JM (2014) Gait and balance in Parkinson’s disease subtypes: objective measures and classification considerations. J Neurol 261:2401–2410CrossRefPubMed
34.
go back to reference Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80:1476–1484CrossRefPubMedPubMedCentral Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM (2013) Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80:1476–1484CrossRefPubMedPubMedCentral
35.
go back to reference Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, Stern MB, Tilley BC, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, Van Hilten JJ, LaPelle N (2007) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord 22:41–47CrossRefPubMed Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, Stern MB, Tilley BC, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, Van Hilten JJ, LaPelle N (2007) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): process, format, and clinimetric testing plan. Mov Disord 22:41–47CrossRefPubMed
36.
go back to reference Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRefPubMed
37.
go back to reference Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653CrossRefPubMed Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653CrossRefPubMed
38.
go back to reference 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 12:189–198CrossRefPubMed 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 12:189–198CrossRefPubMed
39.
go back to reference Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699CrossRefPubMed Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699CrossRefPubMed
40.
go back to reference Doniger GM, Simon ES, Schweiger A (2008) Adjustment of cognitive scores with a co-normed estimate of premorbid intelligence: implementation using mindstreams computerized testing. Appl Neuropsychol 15:250–263CrossRefPubMed Doniger GM, Simon ES, Schweiger A (2008) Adjustment of cognitive scores with a co-normed estimate of premorbid intelligence: implementation using mindstreams computerized testing. Appl Neuropsychol 15:250–263CrossRefPubMed
41.
go back to reference Hausdorff JM, Doniger GM, Springer S, Yogev G, Giladi N, Simon ES (2006) A common cognitive profile in elderly fallers and in patients with Parkinson’s disease: the prominence of impaired executive function and attention. Exp Aging Res 32:411–429CrossRefPubMedPubMedCentral Hausdorff JM, Doniger GM, Springer S, Yogev G, Giladi N, Simon ES (2006) A common cognitive profile in elderly fallers and in patients with Parkinson’s disease: the prominence of impaired executive function and attention. Exp Aging Res 32:411–429CrossRefPubMedPubMedCentral
42.
go back to reference Powell LE, Myers AM (1995) The Activities-specific Balance Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci 50A:M28–M34CrossRefPubMed Powell LE, Myers AM (1995) The Activities-specific Balance Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci 50A:M28–M34CrossRefPubMed
43.
go back to reference Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17:37–49CrossRefPubMed Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17:37–49CrossRefPubMed
44.
go back to reference Chaudhuri KR, Martinez-Martin P (2008) Quantitation of non-motor symptoms in Parkinson’s disease. Eur J Neurol 15(Suppl 2):2–7CrossRefPubMed Chaudhuri KR, Martinez-Martin P (2008) Quantitation of non-motor symptoms in Parkinson’s disease. Eur J Neurol 15(Suppl 2):2–7CrossRefPubMed
45.
go back to reference Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res 4:241–248CrossRefPubMed Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res 4:241–248CrossRefPubMed
46.
go back to reference Alves G, Larsen JP, Emre M, Wentzel-Larsen T, Aarsland D (2006) Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Mov Disord 21:1123–1130CrossRefPubMed Alves G, Larsen JP, Emre M, Wentzel-Larsen T, Aarsland D (2006) Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Mov Disord 21:1123–1130CrossRefPubMed
47.
go back to reference Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130:1787–1798CrossRefPubMed Williams-Gray CH, Foltynie T, Brayne CE, Robbins TW, Barker RA (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130:1787–1798CrossRefPubMed
48.
go back to reference Maidan I, Nieuwhof F, Bernad-Elazari H, Reelick MF, Bloem BR, Giladi N, Deutsch JE, Hausdorff JM, Claassen JA, Mirelman A (2016) The role of the frontal lobe in complex walking among patients with Parkinson’s disease and healthy older adults: an fNIRS study. Neurorehabil Neural Repair 30:963–971CrossRefPubMed Maidan I, Nieuwhof F, Bernad-Elazari H, Reelick MF, Bloem BR, Giladi N, Deutsch JE, Hausdorff JM, Claassen JA, Mirelman A (2016) The role of the frontal lobe in complex walking among patients with Parkinson’s disease and healthy older adults: an fNIRS study. Neurorehabil Neural Repair 30:963–971CrossRefPubMed
49.
go back to reference Stuss DT, Levine B (2002) Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol 53:401–433CrossRefPubMed Stuss DT, Levine B (2002) Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol 53:401–433CrossRefPubMed
50.
go back to reference Maidan I, Rosenberg-Katz K, Jacob Y, Giladi N, Deutsch JE, Hausdorff JM, Mirelman A (2016) Altered brain activation in complex walking conditions in patients with Parkinson’s disease. Parkinsonism Relat Disord 25:91–96CrossRefPubMed Maidan I, Rosenberg-Katz K, Jacob Y, Giladi N, Deutsch JE, Hausdorff JM, Mirelman A (2016) Altered brain activation in complex walking conditions in patients with Parkinson’s disease. Parkinsonism Relat Disord 25:91–96CrossRefPubMed
51.
go back to reference Factor SA, Steenland NK, Higgins DS, Molho ES, Kay DM, Montimurro J, Rosen AR, Zabetian CP, Payami H (2011) Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry 82:564–568CrossRefPubMed Factor SA, Steenland NK, Higgins DS, Molho ES, Kay DM, Montimurro J, Rosen AR, Zabetian CP, Payami H (2011) Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry 82:564–568CrossRefPubMed
52.
go back to reference Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132:2947–2957CrossRefPubMed Selikhova M, Williams DR, Kempster PA, Holton JL, Revesz T, Lees AJ (2009) A clinico-pathological study of subtypes in Parkinson’s disease. Brain 132:2947–2957CrossRefPubMed
53.
go back to reference Nutt JG (2016) Motor subtype in Parkinson’s disease: different disorders or different stages of disease? Mov Disord 31:957–961CrossRefPubMed Nutt JG (2016) Motor subtype in Parkinson’s disease: different disorders or different stages of disease? Mov Disord 31:957–961CrossRefPubMed
54.
go back to reference Antonini A, Barone P, Marconi R, Morgante L, Zappulla S, Pontieri FE, Ramat S, Ceravolo MG, Meco G, Cicarelli G, Pederzoli M, Manfredi M, Ceravolo R, Mucchiut M, Volpe G, Abbruzzese G, Bottacchi E, Bartolomei L, Ciacci G, Cannas A, Randisi MG, Petrone A, Baratti M, Toni V, Cossu G, Del DP, Bentivoglio AR, Abrignani M, Scala R, Pennisi F, Quatrale R, Gaglio RM, Nicoletti A, Perini M, Avarello T, Pisani A, Scaglioni A, Martinelli PE, Iemolo F, Ferigo L, Simone P, Soliveri P, Troianiello B, Consoli D, Mauro A, Lopiano L, Nastasi G, Colosimo C (2012) The progression of non-motor symptoms in Parkinson’s disease and their contribution to motor disability and quality of life. J Neurol 259:2621–2631CrossRefPubMed Antonini A, Barone P, Marconi R, Morgante L, Zappulla S, Pontieri FE, Ramat S, Ceravolo MG, Meco G, Cicarelli G, Pederzoli M, Manfredi M, Ceravolo R, Mucchiut M, Volpe G, Abbruzzese G, Bottacchi E, Bartolomei L, Ciacci G, Cannas A, Randisi MG, Petrone A, Baratti M, Toni V, Cossu G, Del DP, Bentivoglio AR, Abrignani M, Scala R, Pennisi F, Quatrale R, Gaglio RM, Nicoletti A, Perini M, Avarello T, Pisani A, Scaglioni A, Martinelli PE, Iemolo F, Ferigo L, Simone P, Soliveri P, Troianiello B, Consoli D, Mauro A, Lopiano L, Nastasi G, Colosimo C (2012) The progression of non-motor symptoms in Parkinson’s disease and their contribution to motor disability and quality of life. J Neurol 259:2621–2631CrossRefPubMed
55.
go back to reference Erro R, Picillo M, Vitale C, Amboni M, Moccia M, Santangelo G, Pellecchia MT, Barone P (2016) The non-motor side of the honeymoon period of Parkinson’s disease and its relationship with quality of life: a 4-year longitudinal study. Eur J Neurol 23:1673–1679CrossRefPubMed Erro R, Picillo M, Vitale C, Amboni M, Moccia M, Santangelo G, Pellecchia MT, Barone P (2016) The non-motor side of the honeymoon period of Parkinson’s disease and its relationship with quality of life: a 4-year longitudinal study. Eur J Neurol 23:1673–1679CrossRefPubMed
56.
go back to reference Muller B, Assmus J, Herlofson K, Larsen JP, Tysnes OB (2013) Importance of motor vs. non-motor symptoms for health-related quality of life in early Parkinson’s disease. Parkinsonism Relat Disord 19:1027–1032CrossRefPubMed Muller B, Assmus J, Herlofson K, Larsen JP, Tysnes OB (2013) Importance of motor vs. non-motor symptoms for health-related quality of life in early Parkinson’s disease. Parkinsonism Relat Disord 19:1027–1032CrossRefPubMed
57.
go back to reference Prakash KM, Nadkarni NV, Lye WK, Yong MH, Tan EK (2016) The impact of non-motor symptoms on the quality of life of Parkinson’s disease patients: a longitudinal study. Eur J Neurol 23:854–860CrossRefPubMed Prakash KM, Nadkarni NV, Lye WK, Yong MH, Tan EK (2016) The impact of non-motor symptoms on the quality of life of Parkinson’s disease patients: a longitudinal study. Eur J Neurol 23:854–860CrossRefPubMed
58.
go back to reference Zis P, Rizos A, Martinez-Martin P, Pal S, Silverdale M, Sharma JC, Sauerbier A, Chaudhuri KR (2014) Non-motor symptoms profile and burden in drug naive versus long-term Parkinson’s disease patients. J Parkinson’s Dis 4:541–547 Zis P, Rizos A, Martinez-Martin P, Pal S, Silverdale M, Sharma JC, Sauerbier A, Chaudhuri KR (2014) Non-motor symptoms profile and burden in drug naive versus long-term Parkinson’s disease patients. J Parkinson’s Dis 4:541–547
Metadata
Title
Do cognition and other non-motor symptoms decline similarly among patients with Parkinson’s disease motor subtypes? Findings from a 5-year prospective study
Authors
L. Arie
Talia Herman
S. Shema-Shiratzky
N. Giladi
J. M. Hausdorff
Publication date
01-10-2017
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 10/2017
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-017-8605-x

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