Parkinson’s disease and sex-related differences in electromyography during daily life

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Abstract

Scope: Daily bilateral electromyography (EMG) recordings reveal muscle activation patterns implicated in asymmetric Parkinson’s disease (PD)-related functional decline. Also, daily EMG recordings reveal sex-differences in muscle activity that give rise to unique PD presentation in males and females. Purpose: Quantify handgrip strength and daily muscle quiescence through analysis of gaps in the EMG signal in males and females with PD. Bilateral daily EMG was recorded and normalized to maximal voluntary exertions (MVE). EMG gap was defined as <1% amplitude of MVE for >0.1 s and characterized as number, duration and time occupied by gaps. A dynamometer evaluated maximal grip-strength. Three-way repeated measures ANOVA examined differences in gap characteristics and strength. Gap duration was shorter (p = 0.04) and occupied less time (p = 0.02) in PD than controls. Females had fewer gaps with shorter duration (p = 0.004), occupying less time (p = 0.004) compared with males. Gaps were fewer (p = 0.04) and occupied less time (p = 0.01) on more-affected than less-affected side. PD was weaker than controls (p = 0.04), females were weaker than males (p = 0.00), and the more-affected PD side was weaker than less-affected (p = 0.04). Conclusions: Quantification of muscle quiescence through gaps in the EMG signal recorded during daily life provides insight into mechanisms underlying differential change in functional performance in males and females with PD.

Introduction

Electromyography (EMG) reveals important information about changes in muscle activity that limits strength, power and functional performance (Clark et al., 2011). Parkinson’s disease (PD)-associated declines in physical function may be attributed to the disruption of dopamine-regulated neural transmission within the substantia nigra, and result in alterations in muscle activity patterns (DeLong and Wichmann, 2010, Galvan and Wichmann, 2008, Salenius et al., 2002). Alterations in muscle activity studied through EMG for controlled laboratory movements have been implicated in PD-related slow movement (Pfann et al., 2001) and muscle weakness (Brown et al., 1997). It is unknown how PD-mediated alterations in muscle activity impact daily life activities. Because physical performance varies between tasks and is influenced by one’s environment (Teasdale et al., 1990), it is imperative that muscle activity be measured in the context of daily life. Measuring EMG during typical daily activity ensures that stress and fatigue associated with everyday life is encompassed within the quantification of muscle activity that necessitates physical function (Christou et al., 2004, Kent-Braun, 2009).

EMG recorded during daily life has contributed valuable information to understanding the patterns of muscle activity that classify essential versus Parkinsonian tremor (Breit et al., 2008). EMG recordings also reveal the physical capacity required for functional tasks and daily life in young and old adults (Harwood et al., 2011, Kern et al., 2001), post-stroke (Jakobi et al., 2008), frailty (Theou et al., 2010), osteoarthritis (Howe and Rafferty, 2009), and within the framework of varied living environments (Theou et al., 2011). Neural alterations associated with aging, physical function and sex-differences can be quantified through periods of activity (bursts) and gaps (quiescence) in the EMG signal (Clark et al., 2010, Clark et al., 2011, Teasdale et al., 1990). During a typical day, sex- and age-differences in the EMG signal indicate that there are fewer gaps in the EMG signal from older adults compared with younger and females compared with males (Harwood et al., 2011). Less muscle quiescence is speculated to be associated with increased fatigue, reduced strength, and decreased functional ability (Clark et al., 2011, Blangsted et al., 2003, Laursen et al., 2001).

Differences in daily muscle activity between males and females may indicate sex-specific declines in physical function for independent living. Females with PD have more bursts, reach lower peak velocities, and lower magnitude agonist EMG than males for isolated elbow flexion tasks (Pfann et al., 2001). These changes combined with greater declines in muscle strength, power, and force likely impact physical function more in females with PD (Haaxma et al., 2007, Jankovic and Kapadia, 2001, Marusiak et al., 2009, Pfann et al., 2001). Reduced lower-extremity function is a predictor of physical function, mobility, and disability (Guralnik et al., 2000) where grip strength is regularly used as a measure of bilateral strength and overall lower-extremity function (Berkman et al., 1993, Fried et al., 1994). Assessment of bilateral muscle activity in persons with PD is essential since the progression of PD is often unequal across sides and asymmetrically influences strength, thus impacting functional decline in daily life (Hallett and Khoshbin, 1980, Kakinuma et al., 1998, Nogaki et al., 1995, Dijaldetti et al., 1996, Koller and Kase, 1986).

The purposes of this investigation were to: (1) Measure daily muscle activity through quantification of muscle quiescence through EMG gap analysis; (2) Examine handgrip strength in persons with PD and controls. It is hypothesized muscle quiescence will be less in persons with PD compared with controls and fewer gaps will be evident in the EMG signal of PD females compared with PD males. The more-affected PD side will demonstrate fewer EMG gaps and greater muscle weakness relative to less-affected side.

Section snippets

Research design

The Clinical Research Ethics Board (University of British Columbia) granted ethical approval and subjects provided written informed consent prior to participation. Males and females living independently at-home with mild to moderate PD severity (Hoehn & Yahr) were recruited. All subjects were right-hand dominant, independently mobile (with/without gait aids), and persons with PD were in a steady clinical state (i.e. controlled by medication). A disease history questionnaire gauged disease

Subject characteristics

Thirteen females and 10 males with PD (mean age = 67 ± 7.7 years) and eight females and six male controls (mean age = 66 ± 9.2 years) were investigated. PD duration ranged from 1 to 16 years (mean = 8 ± 5.8 years) and average PD severity was 2.1 ± 0.7 (Hoehn & Yahr score). Disease duration, severity and carbidopa–levodopa dose were similar between males and females with PD. Age, body mass index, and daily step count did not differ between groups (p > 0.2, Table 1).

Leg muscle quiescence in PD and controls

In all subjects, sex-disease-muscle interaction

Discussion

This is the first study to examine daily muscle activity through the quantification of muscle quiescence by evaluating gaps in the EMG signal from independent living males and females with PD. This study is vital as it indicates daily EMG can dissociate patterns of muscle activity between persons with PD from controls during daily living. In PD, gaps were shorter and occupied less time in the EMG signal than controls. Bilateral recordings indicated asymmetry in the gaps between sides; gaps were

Conclusion

In persons with PD, understanding and defining physiological change in daily muscle activity with EMG provides insight into asymmetry of disease progression between sides of the body and sex-specific changes in muscle activity. These measures of muscle activity suggest that differential rates of physiological change in muscle between body sides and sexes underlie the observed declines in daily functional performance in persons with PD. The present study provides insight into the foundation of

Conflict of interest

The authors declare no financial and personal relationships with other people or organisations that inappropriately influenced (bias) this work.

Acknowledgements

The authors would like to thank their participants for generously donating their time and to R. Brown, J. Carlyle, K.M.D. Cornett, N. Karn, O. Theou, & Dr. B O’Conner for their assistance with data collection and/or comments on the manuscript. KPR received a Doctoral Award from the Parkinson Society Canada and the Canadian Institutes of Health Research. The sponsor had no role in the study design, in the collection, analysis and interpretation of data; in the writing of the manuscript; and in

Kaitlyn P. Roland completed her PhD at University of British Columbia Okanagan (2012). Her research interests are in supporting independent daily function in persons living with Parkinson’s disease. Dr. Roland is currently a Canadian Institutes of Health Research-funded postdoctoral fellow at the Centre on Aging, University of Victoria, Victoria BC, Canada.

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