Full length articleImpaired set shifting is associated with previous falls in individuals with and without Parkinson’s disease
Introduction
Falls are a leading cause of accidental death [1], and fall risk is increased by about six times in individuals with Parkinson’s disease (PD) [2]. In addition to their direct physical sequelae, falls are associated with reduced confidence [3], activity level [4], and quality of life [5], and therefore may indicate the beginning of serious decline in many individuals with and without PD. Despite the significant morbidity and mortality resulting from falls – and the availability of successful fall risk reduction programs [[6], [7], [8]] – identifying candidates for intervention remains difficult, due to the multifactorial causes of falls [9].
Understanding motor and non-motor impairments associated with falls in people with and without PD is therefore critical to informing prevention strategies. In addition to many of the generic or conventional fall risk factors identified in the aging population, such as advanced age and female sex [9], prospective studies have identified multiple disease-specific risk factors for falls among individuals with PD – including the presence of freezing of gait (FOG), an episodic symptom in which patients feel as though their feet are glued to the floor [10]. Freezing episodes can directly cause falls; however, the presence of FOG is also associated with poorer static and dynamic balance at times other than during paroxysmal freezing episodes [11], suggesting that pathological changes leading to FOG may impair balance and cause falls at times other than during episodes. However, a comprehensive understanding of the pathologic precursors to falls remains lacking [12]. One of the strongest risk factors for falling among those with [13] and without PD [14] remains the presence of previous falls, which is of limited clinical utility for directing patients to interventions.
Many studies have demonstrated associations between impaired executive function and falls in PD and in neurotypical aging, which suggests that measures of subdomains of executive function could be useful in assessments of fall risk. For example, prospective studies have demonstrated elevated fall risk associated with impaired executive function assessed with the multiple-item initiation/perseveration subscale of the Mattis Dementia rating scale in PD [15] or assessed with a computerized testing battery in neurotypical individuals [16]. Multiple definitions of and assessment modalities for the construct of executive function have been proposed. However, one subdomain – set shifting – is central to many schemas and can be estimated quickly as the difference between parts B and A of the Trailmaking Test, which can be performed with pencil and paper [[17], [18]] (see Section 2.2). Set shifting (also referred to as “attention switching,” “task switching,” or “set switching”) is a component of executive function related to cognitive flexibility. Miyake and colleagues [19] define it as “shifting back and forth between multiple tasks, operations, or mental sets.”
Impaired set shifting, in particular, may be relevant to falls, although potential causal pathways between set shifting and falling remain unknown. Among neurotypical older adults, impairments in set shifting, but not in other components of executive function (i.e., inhibition or memory updating), are associated with increased gait variability during dual task conditions [20], which is an important marker of fall risk [21]. Among PD patients, in addition to falls being extremely commonplace, set shifting impairments are common during cognitive and motor tasks. For example, PD patients exhibit impaired ability to shift between sequential voluntary movements [22], to alter balance responses to match task requirements [23] and to (among those with FOG) shift step direction during cued stepping [24]. The extent to which dysfunctional basal ganglia or other disease processes in PD cause impairments in cognitive and/or motor set shifting is an area of substantial debate [[24], [25]]. However, it is reasonable that the inability to shift between ongoing motor programs could contribute to falls.
To the authors’ knowledge, no studies have attempted to relate impairments in the set shifting component of executive function to falling in individuals with or without PD. Here, we used baseline data of 138 adults with and without PD who had volunteered for exercise-based rehabilitation to test the hypotheses that: 1) impaired set shifting is associated with previous falls, and 2) this association is modified by the presence of PD or PD and FOG.
Section snippets
Participants
We assessed associations between impaired set shifting and previous falls using baseline measures of community-dwelling individuals with and without PD from balance and mobility rehabilitative interventions conducted by our group in 2011–2013 and 2014–2015.
Participants provided written informed consent according to protocols approved by the Institutional Review Boards of Emory University and the Georgia Institute of Technology. Participants met the following inclusion criteria: no diagnosed
Demographics
Demographic and clinical characteristics of the study population stratified on the presence of PD and/or FOG are presented in Table 1, Table 2. Overall prevalence of previous falls was 51/138 = 40%. Participants with PD exhibited significantly increased fall prevalence (34/65 = 52% vs. 17/73 = 23%, P < 0.01) despite being younger, higher functioning cognitively, and less likely to be female than the NON-PD group, all of which are known fall risk factors [9]. Among the PD group, individuals with
Discussion
To the authors’ knowledge, this is the first study to examine associations between impairments in the set shifting domain of cognitive function and previous falls in individuals with or without PD. Consistent with our hypothesis, we found that impaired set shifting was associated with previous falls in this cross-sectional study of 138 non-demented individuals after controlling for the large effects of PD and FOG, overall cognitive status, and other demographic and clinical variables. Because
Conclusion
In summary, impaired set shifting was associated with previous falls in non-demented individuals with and without PD. Set shifting may therefore be useful to include in fall risk assessments in older adults with and without PD, particularly when global cognitive measures are within reference limits.
Funding sources
This work was supported by the National Institutes of Health (NIH) UL1 TR000454, KL2 TR000455, TL1 TR000456, R21 HD075612, K25 HD086276 and the Department of Veterans Affairs R&D Service N0870W, the Dan and Merrie Boone Foundation, and the Emory Center for Injury Control. The study sponsors had no role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.
Conflicts of interest
None.
Author contributions
Research project: Conception, JLM, LHT, MEH; Organization, JLM, KCL, LHT, MEH; Execution, JLM, KCL, LHT, MEH. Statistical Analysis: Design and Execution: JLM; Review and Critique: LHT, MEH. Manuscript Preparation: Writing of the first draft: JLM; Review and Critique, KCL, LHT, MEH.
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