Daily electromyography in females with Parkinson's disease: A potential indicator of frailty
Introduction
Frailty is a complex geriatric syndrome that is often clinically characterized by five criteria: (1) Weight loss; (2) Reduced endurance; (3) Slowed gait speed; (4) Muscle weakness; and (5) Exhaustion, resulting in functional dependence (Fried et al., 2001). According to Fried et al. (2001), frailty can be assessed in terms of three phenotypes, or categories of frailty severity, which are defined by the sum of the five individual frailty criteria (i.e., 0: nonfrail, 1 or 2: prefrail, and 3–5: frail). Although frailty can exist independently, it may also co-exist in older adults with progressive neurological disorders, such as Parkinson's disease (PD) (Roland, Jakobi, Jones, & Powell, 2012). Co-morbidities and clinical symptoms interact between frailty and PD making identification of frailty in persons with PD challenging to diagnose (Powell, 2008). Few studies have examined how to identify frailty in the PD population (Ahmed et al., 2008, Lauretani et al., 2012).
Electromyography (EMG) recordings provide a measure of muscle activity that governs movement associated with sustaining physical function. EMG detects the bioelectrical activity associated with muscle contractions that produce movements and reveals important neural changes associated with aging and decline in physical function (Clark et al., 2010a, Clark et al., 2011). Previous work from our laboratory has determined portable EMG devices as a viable means to record muscle activity in older adults during daily life and offer a method to detect frailty-, disease- and age-related differences in muscle activity required to execute movement (Harwood et al., 2011, Howe and Rafferty, 2009, Jakobi et al., 2008, Kern et al., 2001, Roland et al., 2013, Theou et al., 2010, Theou et al., 2011).
Recent investigations (Theou et al., 2010) have used EMG to quantify periods of muscle quiescence (gaps) and muscle activity (bursts) in frail older females as they went about their routine daily activities. As the level of frailty advanced the number of gaps increased while the duration of gaps decreased, and the number of bursts decreased while the burst duration increased (Theou et al., 2010). This study indicated that EMG can be used to identify persons of different frailty phenotypes. Quantification of muscle quiescence during daily life has also provided insight into underlying asymmetric functional decline and differential change in performance in males and females with PD (Roland et al., 2013). EMG recordings of daily muscle activity that detect stages of frailty have not yet been quantified in females with PD. Females with PD are an under-represented group in research, yet they experience greater functional decline (Leveille et al., 2000, Paganelli et al., 2006, Smith and Baltes, 1998) and often become frail more so than age-matched males (Fried et al., 2001). This suggests there is a need to investigate the implications of frailty on muscle activity during daily function in females with PD. Evidence demonstrates factors that contribute to frailty in non-neurological populations, such as age and physical activity, are not associated with frailty in persons with PD (Roland, Cornett, Theou, Jakobi, & Jones, 2012). Therefore, additional factors should be considered, such as muscle activity to better understand frailty within PD.
This study aims to determine if daily muscle activity differs between frailty phenotype in females with PD to facilitate identification of frailty. It is hypothesized that greater periods of muscle quiescence and shorter periods of muscle activity will occur and this change will be exacerbated as females with PD progress across frailty phenotypes. These changes in muscle characteristics will be observed, despite the presence of PD. Understanding how muscle activity changes across frailty phenotypes may help to inform interventions aimed at delaying frailty progression in females with PD. Application of this new-knowledge may improve clinical practice by providing an indicator of change in muscle activity that precipitates increased disability in PD.
Section snippets
Study population and design
Females diagnosed with mild to moderate PD (stages I–III; Hoehn & Yahr, 1967) living in their own home were recruited through newsletter advertisement, public presentations and word-of-mouth. Interested females from the Greater Vancouver and Okanagan areas of British Columbia contacted a member of the research team to participate between March 2010 and January 2012. Subjects were right-hand dominant, able to ambulate independently (with or without gait-aid), and in a steady clinical state (i.e.
Subject characteristics
Thirteen community-dwelling females with PD (mean = 67 ± 8 years) participated and were classified as nonfrail (n = 4), prefrail (n = 6), and frail (n = 3) according to the CHSfi criteria. Power analysis for the EMG protocol determined a sample size of 13 subjects was sufficient (>0.8) to detect a moderate effect size (Cohen's d = 0.5–0.7). Berg Balance Scale score was less in frail females compared with nonfrail (p = 0.04), but all other physical attributes (age, BMI, daily physical activity) of the
Discussion
The current study measured daily muscle activity and quiescence in upper (BB, TB) and lower (VL, BF) limb muscles in nonfrail, prefrail and frail females with PD. The results of this investigation present differences in muscle activity characteristics (i.e., gaps, bursts) for frail compared with nonfrail females with PD. Frail females had decreased number of gaps and time occupied by gaps (gap percent) compared with nonfrail. Also, duration of bursts was greater in frail than nonfrail,
Conclusions
Operational definitions of frailty vary and PD is commonly listed as an exclusion criterion for the analysis of frailty (Wong et al., 2010). Understanding how frailty relates to PD progression is important since females with PD are at greater risk of becoming frail than males or persons without PD (Ahmed et al., 2008, Roland et al., 2012b). The results of this investigation suggest that EMG can be used to dissociate frail females with PD from nonfrail based on muscle activity characteristics,
Conflict of interest
The authors have no conflicts of interest that are directly relevant to the content of this manuscript.
Role of the funding source
Kaitlyn P. Roland's work on this manuscript was supported by a Doctoral Award from the Canadian Institutes of Health Research (CIHR; Neurosciences, Mental Health and Addiction)/Parkinson Society Canada (2010–2012). CIHR had no involvement in the study design, in the collection, analysis and interpretation of data; in the writing of the manuscript; and in the decision to submit the manuscript for publication. Kaitlyn P. Roland is currently funded by CIHR (Gender, Work, and Health) (2012–2014)
References (49)
- et al.
Frailty in Parkinson's disease and its clinical implications
Parkinsonism & Related Disorders
(2008) - et al.
Abnormal oxidative metabolism in exercise intolerance of undetermined origin
Neuromuscular Disorders: NMD
(1997) - et al.
Levodopa effect on electromyographic activation patterns of tibialis anterior muscle during walking in Parkinson's disease
Gait & Posture
(2011) - et al.
Leg muscle activation during gait in Parkinson's disease: Adaptation and interlimb coordination
Electroencephalography and Clinical Neurophysiology/Electromyography and Motor Control
(1995) Neural adaptations with chronic physical activity
Journal of Biomechanics
(1997)- et al.
A comparison of fatigue measures in Parkinson's disease
Parkinsonism & Related Disorders
(2007) - et al.
Age- and sex-related differences for electromyography gaps during daily activity and a discrete task
Gait & Posture
(2011) - et al.
Quadriceps activity and physical activity profiles over long durations in patients with osteoarthritis of the knee and controls
Journal of Electromyography and Kinesiology: Official Journal of the International Society of Electrophysiological Kinesiology
(2009) - et al.
Parkinson's disease (PD) in the elderly: An example of geriatric syndrome (GS)?
Archives of Gerontology and Geriatrics
(2012) - et al.
Pedunculopontine nucleus and basal ganglia: Distant relatives or part of the same family?
Trends in Neurosciences
(2004)
Frailty and Parkinson's disease: Theories and clinical implications
Parkinsonism & Related Disorders
Variability of EMG patterns: A potential neurophysiological marker of Parkinson's disease?
Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology
Parkinson's disease and sex-related differences in electromyography during daily life
Journal of Electromyography and Kinesiology
Daily muscle activity and quiescence in non-frail, pre-frail, and frail older women
Experimental Gerontology
Differences in the EMG pattern of leg muscle activation during locomotion in Parkinson's disease
Functional Neurology
Skeletal muscle fatigue: Cellular mechanisms
Physiological Reviews
Scaling of the size of the first agonist EMG burst during rapid wrist movements in patients with Parkinson's disease
Journal of Neurology, Neurosurgery & Psychiatry
Platelet mitochondrial respiratory chain function in Parkinson's disease
Movement Disorders: Official Journal of the Movement Disorder Society
Muscle activity during computer-based office work in relation to self-reported job demands and gender
European Journal of Applied Physiology
Differences in size, strength, and power of upper and lower body muscle groups in young and older men
Journals of Gerontology. Series A, Biological Sciences and Medical Sciences
Characteristics of the electromyographic patterns of lower limb muscle during gait in patients with Parkinson's disease when OFF and ON L-Dopa treatment
The Italian Journal of Neurological Sciences
Impaired voluntary neuromuscular activation limits muscle power in mobility-limited older adults
Journals of Gerontology. Series A, Biological Sciences and Medical Sciences
Muscle performance and physical function are associated with voluntary rate of neuromuscular activation in older adults
Journals of Gerontology. Series A, Biological Sciences and Medical Sciences
Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke
Journal of Neurophysiology
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Present address: Centre on Aging, University of Victoria, R Hut 103, PO Box 1700 STN CSC, Victoria, BC, Canada V8W 2Y2.