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Parkinson Disease-Associated Cognitive Impairment

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Parkinson Disease-Associated Cognitive Impairment PRIMER Parkinson disease-associated cognitive impairment Dag Aarsland 1,2 ✉ , Lucia Batzu 3, Glenda M. Halliday 4, Gert J. Geurtsen 5, Clive Ballard 6, K. Ray Chaudhuri 3 and Daniel Weintraub7,8 Abstract | Parkinson disease (PD) is the second most common neurodegenerative disorder, affecting >1% of the population ≥65 years of age and with a prevalence set to double by 2030. In addition to the defining motor symptoms of PD, multiple non-motor symptoms occur; among them, cognitive impairment is common and can potentially occur at any disease stage. Cognitive decline is usually slow and insidious, but rapid in some cases. Recently, the focus has been on the early cognitive changes, where executive and visuospatial impairments are typical and can be accompanied by memory impairment, increasing the risk for early progression to dementia. Other risk factors for early progression to dementia include visual hallucinations, older age and biomarker changes such as cortical atrophy, as well as Alzheimer-type changes on functional imaging and in cerebrospinal fluid, and slowing and frequency variation on EEG. However, the mechanisms underlying cognitive decline in PD remain largely unclear. Cortical involvement of Lewy body and Alzheimer-type pathologies are key features, but multiple mechanisms are likely involved. Cholinesterase inhibition is the only high-level evidence-based treatment available, but other pharmacological and non-pharmacological strategies are being tested. Challenges include the identification of disease-modifying therapies as well as finding biomarkers to better predict cognitive decline and identify patients at high risk for early and rapid cognitive impairment. Parkinson disease (PD) is the most common movement The full spectrum of cognitive impairment occurs in disorder and the second most common neurodegenera­ individuals with PD, from subjective cognitive decline tive disorder after Alzheimer disease (AD). The neuro­ (SCD) and mild cognitive impairment (PD­MCI) pathological hallmarks of PD are neuronal loss in the to dementia (PDD). SCD is a self­perceived decline substantia nigra, which causes striatal dopaminergic in cognitive ability, unrelated to an acute event, deficiency, and α­synuclein accumulation in intra­ together with normal age­adjusted, sex­adjusted and neuronal inclusions. However, multiple mechanisms and education­adjusted performance on standardized cog­ pathway dysfunctions play a role in the pathogenesis of nitive tests6. By contrast, PD­MCI is a gradual decline PD, including oxidative stress, dysfunctional mitochon­ in cognitive ability reported by either a patient with PD dria, cellular calcium imbalance, neuroinflammation or an informant or observed by the clinician, associated and other neurotransmitter system deficits1. with cognitive deficits on either formal neuropsycho­ Apart from its cardinal motor features, such as brady­ logical testing or a scale of global cognitive abilities7. Subtle kinesia (slowness of movement), rigidity and resting difficulties on complex functional tasks may be present7 tremor, PD is associated with a heterogeneous spectrum and, based on the number of affected cognitive domains, of non­motor symptoms that contribute greatly to the PD­MCI can be classified as single or multiple domain7. overall disease burden. Cognitive impairment is up to PDD is defined as cognitive impairment in a patient with six times more common in individuals with PD than in PD with deficits in at least two of four cognitive domains the healthy population2 and is one of the most impor­ (executive abilities, attention, visuospatial abilities and tant non­motor manifestations of PD, integral to the memory) that are severe enough to significantly affect natural history of the disease. Cognitive impairment can normal functioning beyond impairment caused by severely affect quality of life (QOL) and function and has disease­related motor and autonomic symptoms8,9. PDD ✉e-mail: dag.aarsland@ been shown to have substantial economic consequences can be denoted as mild (mild effect on daily function­ kcl.ac.uk over and above the motor symptoms, even at the early ing), moderate and severe (inability for independent 3–5 https://doi.org/10.1038/ stages of PD , thereby representing a high priority for living) dementia. Multiple cognitive domains are affected s41572-021-00280-3 both patients and care partners. in those with cognitive impairment and PD, including NATURE REVIEWS | DISEASE PRIMERS | Article citation ID: (2021) 7:47 1 0123456789();: PRIMER Author addresses community­based cohorts, using consensus criteria for cognitive impairment classification, based on cognitive 1 Department of Old Age Psychiatry, Institute of Psychiatry, Psychology and testing and clinical interviews. Neuroscience, King’s College London, London, UK. 2 Centre for Age-Related Medicine, Stavanger University Hospital, Stavanger, Norway. Dementia 3Parkinson’s Foundation Centre of Excellence, King’s College Hospital and Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK. The cross­sectional proportion of patients with PD 18 4Brain and Mind Centre and Faculty of Medicine and Health School of Medical Sciences, who have dementia is 24–31% . Although findings University of Sydney, Sydney, New South Wales, Australia. vary among studies, the cumulative prevalence of 5Amsterdam UMC, University of Amsterdam, Department of Medical Psychology, PDD in patients with a mean age at diagnosis from Amsterdam Neuroscience, Amsterdam, The Netherlands. 54 to 70.2 years is 17% at 5 years after diagnosis19, 46% 6University of Exeter Medical School, Exeter, UK. at 10 years after diagnosis20 and 83% 20 at years after 7Departments of Psychiatry and Neurology, Perelman School of Medicine at the diagnosis21,22 (Table 1), compared with a global preva­ University of Pennsylvania, Philadelphia, PA, USA. lence of 5–7% of dementia in the general population 8 Parkinson’s Disease Research, Education and Clinical Center (PADRECC), Corporal >60 years of age23. Thus, despite variability, there is a high Michael J. Crescenz Veterans Affairs Medical Center, Philadelphia, PA, USA. risk of dementia in PD, with nearly half of patients hav­ ing dementia within 10 years after diagnosis and the vast memory, attention, visuospatial abilities and especially majority of patients having dementia within >20 years executive functions (mental flexibility, set­shifting, after diagnosis. Of note, there is a large variation in time switching, efficiently planning future actions and solv­ to dementia, as some patients develop dementia within ing problems)10. Of note, dementia with Lewy bodies the first few years after diagnosis whereas others remain (DLB) is a disorder characterized by limbic and cortical without dementia for decades. Although several risk Lewy body pathology and dementia occurring before or factors for cognitive impairment in individuals with PD within 1 year after the onset of motor parkinsonism11; have been identified (see ‘Risk Factors’, below), further a specific prodromal, pre­dementia stage has been understanding of the mechanisms driving this difference described12. DLB and PDD are thus very similar and and identifying those with a high risk of early dementia distinguished only by the relative timing of motor to allow for closer monitoring and management is cru­ and cognitive symptoms, although this is under debate13. cial. Importantly, the rate of cognitive decline in PDD is Despite increased research over the past two decades, similar to that in AD24 and many patients with PDD will the knowledge and treatment of cognitive difficulties become fully dependent on care and support from others in PD lag far behind our knowledge and treatment of and need nursing home placement25. its motor features. Continued efforts for a better com­ prehension of this complex feature of PD are required, Mild cognitive impairment particularly as there is no treatment to prevent or During the past decade, there has been increased delay cognitive decline in PD, no effective treatments focus on the pre­dementia stages of cognitive impair­ for PD­MCI, and only one treatment (cholinesterase ment in individuals with PD, in particular MCI, as has inhibitors) approved for PDD14,15. been the case in AD and, more recently, also in DLB12. This Primer describes the epidemiology of Cross­sectional studies suggest that 25.8% of patients PD­associated cognitive impairment and what is with PD without dementia have MCI26, whereas data known about its mechanisms and pathophysiological from the incidence cohort of the ParkWest Study (a pro­ changes. In addition, it reviews the diagnostic criteria, spective longitudinal multicentre study of patients with procedures and biomarkers to identify patients with PD incident PD in Norway) and other studies found that at increased risk for early and rapid cognitive decline. ~20.2% of patients have MCI at the time of diagnosis Finally, this Primer concludes with an overview of the (mean age 71.3 ± 7.5 SD), which increases to 40–50% after status of pharmacological and non­pharmacological 5 years of follow­up27–30 (Table 1). By contrast, the esti­ therapeutic strategies and an outline of the most promis­ mated prevalence of MCI in the general older population ing breakthroughs that are likely to drive future research (aged 60–90 years) ranges between 16% and 20%31. pathways. MCI is often described as a transitory stage between normal cognition (PD­NC) and dementia and it is Epidemiology important to understand
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