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      Motor complications in Parkinson's disease: 13‐year follow‐up of the CamPaIGN cohort

      brief-report

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          Abstract

          Background

          Long‐term population‐representative data on motor fluctuations and levodopa‐induced dyskinesias in Parkinson's disease is lacking.

          Methods

          The Cambridgeshire Parkinson's Incidence from GP to Neurologist (CamPaIGN) cohort comprises incident PD cases followed for up to 13 years (n = 141). Cumulative incidence of motor fluctuations and levodopa‐induced dyskinesias and risk factors were assessed using Kaplan‐Meyer and Cox regression analyses.

          Results

          Cumulative incidence of motor fluctuations and levodopa‐induced dyskinesias was 54.3% and 14.5%, respectively, at 5 years and 100% and 55.7%, respectively, at 10 years. Higher baseline UPDRS‐total and SNCA rs356219(A) predicted motor fluctuations, whereas higher baseline Mini‐mental State Examination and GBA mutations predicted levodopa‐induced dyskinesias. Early levodopa use did not predict motor complications. Both early motor fluctuations and levodopa‐induced dyskinesias predicted reduced mortality in older patients (age at diagnosis >70 years).

          Conclusions

          Our data support the hypothesis that motor complications are related to the severity of nigrostriatal pathology rather than early levodopa use and indicate that early motor complications do not necessarily confer a negative prognosis. © 2019 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.

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          The distinct cognitive syndromes of Parkinson's disease: 5 year follow-up of the CamPaIGN cohort.

          Caroline Williams-Gray, Jonathan Evans, An Goris … (2009)
          Cognitive abnormalities are common in Parkinson's disease, with important social and economic implications. Factors influencing their evolution remain unclear but are crucial to the development of targeted therapeutic strategies. We have investigated the development of cognitive impairment and dementia in Parkinson's disease using a longitudinal approach in a population-representative incident cohort (CamPaIGN study, n = 126) and here present the 5-year follow-up data from this study. Our previous work has implicated two genetic factors in the development of cognitive dysfunction in Parkinson's disease, namely the genes for catechol-O-methyltransferase (COMT Val(158)Met) and microtubule-associated protein tau (MAPT) H1/H2. Here, we have explored the influence of these genes in our incident cohort and an additional cross-sectional prevalent cohort (n = 386), and investigated the effect of MAPT H1/H2 haplotypes on tau transcription in post-mortem brain samples from patients with Lewy body disease and controls. Seventeen percent of incident patients developed dementia over 5 years [incidence 38.7 (23.9-59.3) per 1000 person-years]. We have demonstrated that three baseline measures, namely, age >or=72 years, semantic fluency less than 20 words in 90 s and inability to copy an intersecting pentagons figure, are significant predictors of dementia risk, thus validating our previous findings. In combination, these factors had an odds ratio of 88 for dementia within the first 5 years from diagnosis and may reflect the syndrome of mild cognitive impairment of Parkinson's disease. Phonemic fluency and other frontally based tasks were not associated with dementia risk. MAPT H1/H1 genotype was an independent predictor of dementia risk (odds ratio = 12.1) and the H1 versus H2 haplotype was associated with a 20% increase in transcription of 4-repeat tau in Lewy body disease brains. In contrast, COMT genotype had no effect on dementia, but a significant impact on Tower of London performance, a frontostriatally based executive task, which was dynamic, such that the ability to solve this task changed with disease progression. Hence, we have identified three highly informative predictors of dementia in Parkinson's disease, which can be easily translated into the clinic, and established that MAPT H1/H1 genotype is an important risk factor with functional effects on tau transcription. Our work suggests that the dementing process in Parkinson's disease is predictable and related to tau while frontal-executive dysfunction evolves independently with a more dopaminergic basis and better prognosis.
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            Evolution of cognitive dysfunction in an incident Parkinson's disease cohort.

            C. Williams-Gray, T. Foltynie, C. Brayne … (2007)
            We have previously performed detailed clinical and neuropsychological assessments in a community-based cohort of patients with newly diagnosed parkinsonism, and through analysis of a subcohort with idiopathic Parkinson's disease (PD), we have demonstrated that cognitive dysfunction occurs even at the time of PD diagnosis and is heterogeneous. Longitudinal follow-up of the cohort has now been performed to examine the evolution of cognitive dysfunction within the early years of the disease. One hundred and eighty (79%) eligible patients from the original cohort with parkinsonism were available for re-assessment at between 3 and 5 years from their initial baseline assessments. PD diagnoses were re-validated with repeated application of the UKPDS Brain Bank criteria in order to maximize sensitivity and specificity, following which a diagnosis of idiopathic PD was confirmed in 126 patients. Thirteen out of 126 (10%) had developed dementia at a mean (SD) of 3.5 (0.7) years from diagnosis, corresponding to an annual dementia incidence of 30.0 (16.4-52.9) per 1000 person-years. A further 57% of PD patients showed evidence of cognitive impairment, with frontostriatal deficits being most common amongst the non-demented group. However, the most important clinical predictors of global cognitive decline following correction for age were neuropsychological tasks with a more posterior cortical basis, including semantic fluency and ability to copy an intersecting pentagons figure, as well as a non-tremor dominant motor phenotype at the baseline assessment. This work clarifies the profile of cognitive dysfunction in early PD and demonstrates that the dementing process in this illness is heralded by both postural and gait dysfunction and cognitive deficits with a posterior cortical basis, reflecting probable non-dopaminergic cortical Lewy body pathology. Furthermore, given that these predictors of dementia are readily measurable within just a few minutes in a clinical setting, our work may ultimately have practical implications in terms of guiding prognosis in individual patients.
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              A five-year study of the incidence of dyskinesia in patients with early Parkinson's disease who were treated with ropinirole or levodopa.

              O Rascol, D. Brooks, A Korczyn … (2000)
              There is debate about whether the initial treatment for patients with Parkinson's disease should be levodopa or a dopamine agonist. In this prospective, randomized, double-blind study, we compared the safety and efficacy of the dopamine D2-receptor agonist ropinirole with that of levodopa over a period of five years in 268 patients with early Parkinson's disease. If symptoms were not adequately controlled by the assigned study medication, patients could receive supplementary levodopa, administered in an open-label fashion. The primary outcome measure was the occurrence of dyskinesia. Eighty-five of the 179 patients in the ropinirole group (47 percent) and 45 of the 89 patients in the levodopa group (51 percent) completed all five years of the study. In the ropinirole group 29 of the 85 patients (34 percent) received no levodopa supplementation. The analysis of the time to dyskinesia showed a significant difference in favor of ropinirole (hazard ratio for remaining free of dyskinesia, 2.82; 95 percent confidence interval, 1.78 to 4.44; P<0.001). At five years, the cumulative incidence of dyskinesia (excluding the three patients who had dyskinesia at base line), regardless of levodopa supplementation, was 20 percent (36 of 177 patients) in the ropinirole group and 45 percent (40 of 88 patients) in the levodopa group. There was no significant difference between the two groups in the mean change in scores for activities of daily living among those who completed the study. Adverse events led to the early withdrawal from the study of 48 of 179 patients in the ropinirole group (27 percent) and 29 of 89 patients in the levodopa group (33 percent). The mean (+/-SD) daily doses given by the end of the study were 16.5+/-6.6 mg of ropinirole (plus 427+/-221 mg of levodopa in patients who received supplementation) and 753+/-398 mg of levodopa (including supplements). Early Parkinson's disease can be managed successfully for up to five years with a reduced risk of dyskinesia by initiating treatment with ropinirole alone and supplementing it with levodopa if necessary.
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                Author and article information

                Contributors
                Han‐Joon Kim:
                ORCID: https://orcid.org/0000-0001-8219-9663
                movement@snu.ac.kr
                Caroline H. Williams‐Gray: chm27@cam.ac.uk
                Journal
                Journal ID (nlm-ta): Mov Disord
                Journal ID (iso-abbrev): Mov. Disord
                Journal ID (doi): 10.1002/(ISSN)1531-8257
                Journal ID (publisher-id): MDS
                Title: Movement Disorders
                Publisher: John Wiley & Sons, Inc. (Hoboken, USA )
                ISSN (Print): 0885-3185
                ISSN (Electronic): 1531-8257
                Publication date (Electronic): 11 November 2019
                Publication date (Print): January 2020
                Volume: 35
                Issue: 1 ( doiID: 10.1002/mds.v35.1 )
                Pages: 185-190
                Affiliations
                [ 1 ] Department of Neurology and Movement Disorder Center College of Medicine, Seoul National University Seoul Korea
                [ 2 ] John van Geest Centre for Brain Repair, Department of Clinical Neurosciences University of Cambridge Cambridge UK
                [ 3 ] Department of Clinical & Movement Neurosciences UCL Queen Square Institute of Neurology London UK
                Author notes
                [*] [* ] Correspondence to: Han‐Joon Kim, MD, PhD, Department of Neurology and Movement Disorder Center, College of Medicine, Seoul National University, 101 Daehakro, Jongno‐gu, Seoul, 03080, Korea; movement@ 123456snu.ac.kr . Caroline H. Williams‐Gray, PhD, MRCP, John Van Geest Centre for Brain Repair, Department of Clinical Neurosciences, University of Cambridge, Forvie Site, Robinson Way, Cambridge, CB2 0PY, UK; chm27@ 123456cam.ac.uk
                Author information
                https://orcid.org/0000-0001-8219-9663
                https://orcid.org/0000-0003-0752-1813
                Article
                Publisher ID: MDS27882
                DOI: 10.1002/mds.27882
                PMC ID: 7063985
                PubMed ID: 31965629
                SO-VID: 5dded66f-6173-4b26-80b6-5f3518da83b4
                Copyright © © 2019 The Authors. Movement Disorders published by Wiley Periodicals, Inc. on behalf of International Parkinson and Movement Disorder Society.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 14 March 2019
                Date revision received : 12 August 2019
                Date accepted : 09 September 2019
                Page count
                Figures: 1, Tables: 1, Pages: 6, Words: 4304
                Funding
                Funded by: Basic Science Research Program
                Funded by: National Research Foundation of Korea (NRF) , open-funder-registry 10.13039/501100003725;
                Funded by: Ministry of Education , open-funder-registry 10.13039/501100004565;
                Award ID: 2013‐R1A1A2010499
                Funded by: Wellcome Trust , open-funder-registry 10.13039/100004440;
                Funded by: Medical Research Council , open-funder-registry 10.13039/501100000265;
                Funded by: Patrick Berthoud Trust
                Funded by: Parkinson's UK , open-funder-registry 10.13039/501100000304;
                Funded by: National Institute for Health Research (NIHR) , open-funder-registry 10.13039/501100000272;
                Funded by: Cambridge Biomedical Research Centre Dementia and Neurodegeneration Theme
                Award ID: Grant Reference Number 146281
                Categories
                Subject: Brief Reports
                Subject: Brief Reports
                Custom metadata
                source-schema-version-number 2.0
                cover-date January 2020
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.7 mode:remove_FC converted:10.03.2020

                ScienceOpen disciplines: Medicine
                Keywords: levodopa‐induced dyskinesias,motor complications,motor fluctuations,parkinson's disease
                Data availability:
                ScienceOpen disciplines: Medicine
                Keywords: levodopa‐induced dyskinesias, motor complications, motor fluctuations, parkinson's disease

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