Page 1 of 17 Progressive Resistance Exercise in Parkinson’s Disease Lamotte et al. http://dx.doi.org/10.1123/kr.2014-0074 Lamotte is with the Department of Neurology, University Hospital of Caen, Caen, France. Skender is with the Department of Kinesiology and Nutrition, University of Illinois at Chicago, IL. Rafferty is with the Graduate Program in Neuroscience, University of Illinois at Chicago, IL, and the Department of Physical Therapy & Human Movement Sciences, Northwestern University, Chicago, IL. David, Sadowsky, and Corcos are with the Department of Physical Therapy & Human Movement Sciences, Northwestern University, Chicago, IL. Corcos is also with the Department of Neurological Sciences, Rush University Medical Center, Chicago, IL. [AUQ1] Effects of Progressive Resistance Exercise Training on the Motor and Nonmotor Features of Parkinson’s Disease: A Review Guillaume Lamotte, Elizabeth Skender, Miriam R. Rafferty, Fabian David, Steve Sadowsky, and Daniel M. Corcos Objective: This paper reviews the therapeutically beneficial effects of progressive resistance exercise training (PRET) on motor and nonmotor symptoms in Parkinson’s disease (PD). Methods: First, we perform a systematic review of the literature on the effects of PRET on motor signs of PD, functional outcomes, quality of life, and patient perceived improvement, strength, and cognition in PD. Second, we perform a meta-analysis on the motor section of the UPDRS. Finally, we discuss the results of our review and we identify current knowledge gaps regarding PRET in PD. Conclusion: This systematic review synthesizes evidence that PRET can improve strength and motor signs of Parkinsonism in PD and may also be beneficial for physical function in individuals with PD. Further research is needed to explore the effects of PRET on nonmotor symptoms such as depression, cognitive impairment, autonomic nervous system dysfunction, and quality of life in individuals with PD. Keywords: Parkinson’s disease, progressive resistance exercise, exercise, resistance exercise, motor activity, gait, balance Parkinson’s disease (PD) is a neurodegenerative disorder characterized by motor symptoms such as bradykinesia, rigidity, tremor, gait dysfunction, and postural instability, as well as nonmotor symptoms such as cognitive impairment and mood disorders, among others. Symptoms of PD worsen with time, leading to a general decrease in activity and an altered quality of life with increased risk of falling, immobility, and cognitive impairment (Morris, Huxham, McGinley, Dodd, & Iansek, 2001; Olanow, Stern, & Sethi, 2009). To date, there is no neuroprotective strategy available for PD. Consequently, there is a need for new therapies that can slow disease progression and reduce the functional and cognitive declines seen with advancement of the disease. Epidemiological studies have supported a link between moderate to vigorous exercise habits in midlife and the reduced risk of later developing PD (Chen, Zhang, Schwarzschild, Hernán, & Ascherio, 2005; Xu et al., 2010). Recently, the American College of Sports Medicine issued new guidelines to promote exercise in older adults (Garber et al., 2011). According to these recommendations, older adults should exercise regularly and combine endurance exercise training and muscle strengthening activities (Garber et al., 2011). We recently reviewed the literature on the effect of endurance exercise training in PD (Lamotte et al., 2014). This review will synthesize the literature that has examined the effects of progressive resistance exercise training (PRET) on the motor and nonmotor signs of PD. PRET can be defined as a method of exercise that systematically and progressively increases the ability of muscle to generate force (Taylor, Dodd, & Damiano, 2005). PRET is based on three principles: (1) to perform a small number of repetitions until fatigue, (2) to allow sufficient rest between exercises for recovery, and (3) to increase the resistance as the ability to generate force increases (Taylor, Dodd, & Damiano, 2005). Several studies have shown that patients with PD have reduced muscle strength compared with controls (Allen, Canning, Sherrington, & Fung, 2009; Cano-de-la-Cuerda, Perez-de-Heredia, Miangolarra-Page, Munoz-Hellin, & Fernandez-de-Las-Penas, 2010). The fact that muscle weakness and bradykinesia may share common underlying mechanisms involving a dysfunction of the nigrostriatal pathway that alters corticospinal activation supports the use of PRET in this population (David et al., 2012). PRET has been established as a safe form of exercise, and a recent meta-analysis depicted PRET as having a moderate positive effect on strength and
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Page 1 of 17
Progressive Resistance Exercise in Parkinson’s Disease Lamotte et al.
http://dx.doi.org/10.1123/kr.2014-0074 Lamotte is with the Department of Neurology, University Hospital of Caen, Caen, France. Skender is with the Department of Kinesiology and
Nutrition, University of Illinois at Chicago, IL. Rafferty is with the Graduate Program in Neuroscience, University of Illinois at Chicago, IL, and the
Department of Physical Therapy & Human Movement Sciences, Northwestern University, Chicago, IL. David, Sadowsky, and Corcos are with the Department of Physical Therapy & Human Movement Sciences, Northwestern University, Chicago, IL. Corcos is also with the Department of
Neurological Sciences, Rush University Medical Center, Chicago, IL. [AUQ1]
Effects of Progressive Resistance Exercise Training on the Motor and Nonmotor Features of Parkinson’s Disease: A
Review
Guillaume Lamotte, Elizabeth Skender, Miriam R. Rafferty, Fabian David, Steve Sadowsky, and Daniel M. Corcos
Objective: This paper reviews the therapeutically beneficial effects of progressive resistance exercise training (PRET) on
motor and nonmotor symptoms in Parkinson’s disease (PD). Methods: First, we perform a systematic review of the
literature on the effects of PRET on motor signs of PD, functional outcomes, quality of life, and patient perceived
improvement, strength, and cognition in PD. Second, we perform a meta-analysis on the motor section of the UPDRS.
Finally, we discuss the results of our review and we identify current knowledge gaps regarding PRET in PD. Conclusion:
This systematic review synthesizes evidence that PRET can improve strength and motor signs of Parkinsonism in PD and
may also be beneficial for physical function in individuals with PD. Further research is needed to explore the effects of
PRET on nonmotor symptoms such as depression, cognitive impairment, autonomic nervous system dysfunction, and
Forbes, 2013), and we discussed the potential positive
effects of PRET on cognition in PD. Studies with longer
duration and an appropriate follow-up, including
evaluation of pharmacologic therapy, would be essential to
confirm the benefit of PRET and to explore if exercise-
induced changes in PD are maintained over time. Future
studies need to consider the stage of disease progression,
as the goal of the intervention may be different at different
stages of the disease.
Exercise and Nonmotor Symptoms in Parkinson’s Disease. In addition to the commonly recognized motor symptoms,
there has been a greater interest in nonmotor disturbances
in PD. These nonmotor symptoms include cognitive
impairment, depression, autonomic and sleep disturbances,
pain, and fatigue (Garcia-Ruiz, Chaudhuri, & Martinez-
Martin, 2014). These nondopaminergic symptoms are
important to consider as they occur in almost all patients
with PD, they affect almost all aspects of daily life, and
they have been shown to have a greater effect on health-
related quality of life than classic motor symptoms
(Maetzler, 2014). In this review, nonmotor symptoms have
been investigated as secondary outcomes and additional
clinical trials that include nonmotor symptoms as primary
outcome variables are needed to explore the potential
benefit of exercise in patients with PD.
Exercise Duration and Best Mode of Physical Activity for Patients With Parkinson’s Disease. Gerecke, Jiao, Pani, Pagala, and Smeyene (2010) have
suggested that duration of an intervention program is
crucial to protect dopaminergic neurons against death
caused by acute MPTP-intoxication in an animal model of
PD. In humans, the necessary duration of an exercise
program intervention to improve functional outcomes in
PD is unknown and most of the studies have investigated
exercise-induced changes with short-term duration and
follow-up (Table 1). The best mode of physical activity for
patients with PD is also a question that needs further
exploration. This current review provides evidence that
PRET improves motor signs of Parkinsonism in PD.
However, this review reveals that PRET may have a
limited effect on functional performance in PD. Other
types of exercise such as Tai Chi or endurance exercise
training may be more beneficial than PRET to improve
Page 9 of 17
functional performances in PD (Lamotte et al., 2014; Ni et
al., 2014). To date, the mechanisms underlying exercise-
induced changes for each program are not fully
understood. PD is a variable and progressive disease and it
is possible that only some patients can benefit from a
specific exercise regimen according to disease severity,
clinical presentation, or even lifestyle or genetics. There is
a real need for well-designed controlled clinical trials that
would compare or combine different modes of exercise.
Limitations
There were several limitations to this review. We limited
our search strategy and subsequent review to evidence
ranked as level I or II in articles that were published in
English-language, peer-reviewed publications. As noted
previously, participants included were moderately to
mildly affected by PD and, therefore, the results of the
study are not fully generalizable to the PD population at
large.
Conclusion and Implications and Directions for Future Research
This systematic review synthesizes evidence that PRET
can improve strength and motor signs of Parkinsonism in
PD. PRET may also be beneficial for functional outcomes
such as gait and balance but more research is needed to
explore the specific effect of PRET on physical function in
PD. Very few studies have investigated the effect of PRET
on cognition in PD. However, preliminary results suggest
a potential benefit on executive function in individuals
with PD. Further research is needed to explore the effects
of PRET on both motor symptoms and nonmotor
symptoms such as depression, cognition, sleep
disturbances, autonomic nervous system dysfunction, and
quality of life in individuals with PD. We conclude that a
highly supervised PRET program could be beneficial for
mild to moderate PD. There is a need for well-designed
large-scale randomized controlled trials to confirm
benefits and safety of PRET for this population and to
explore potential benefits on the motor and nonmotor signs
of PD. Further research on exercise in PD should address
specific questions about the optimal exercise mode,
intensity, and duration.
Author Contributions GL and ES contributed equally to the review of the literature, data
analysis, writing and preparation of the manuscript, and the
review and critique of the manuscript. MR, FD, SS and DC: data
analysis, writing contribution, review and critique of the
manuscript.
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Figure 1 — Meta-analyses on the effect of PRET on motor
signs of Parkinsonism in PD assessed by the UPDRS motor
subscale in PD. A: Meta-analysis comparing baseline and
postintervention UPRDS motor scores (within-group
difference). B: Meta-analysis comparing PRET with a control
group. The control group consisted of stretching exercise (Li
et al., 2012), stretching and balance training (Corcos et al.,
2013), and standard physiotherapy (Dibble et al., 2009). Note:
Corcos et al. (2013), off medication; Dibble et al. (2009),
Hass et al. (2007), and Li et al. (2012), on medication.
Squares indicate the individual mean difference in each study.
The size of each square is proportional to the percent weight
of that individual study in the meta-analysis, and the
horizontal line represents the 95% confidence interval (CI).
Pooled mean differences and 95% CIs are indicated by the