Parkinson disease (PD) is a common neurodegenerative disorder in which people experience deficits in motor function including impaired gait, balance, and mobility.1,2 Decrements in gait velocity occur during forward and backward walking and persist with optimal medication.3 Furthermore, impaired gait, balance, and mobility can be detected early in the disease course, and subsequent decline in gait may indicate the onset of disability.4 These factors highlight the need for complementary approaches, such as exercise, to address these debilitating impairments in PD.1
Group exercise classes using dance, treadmill, and stretching are safe and feasible for individuals with PD, and randomized controlled trials indicate these approaches provide motor benefits.5–9 However, many studies compare exercise programs to nonexercise controls and few studies directly compare the effects of different interventions on motor function in PD to determine whether certain types of exercise better address particular motor impairments. In addition, limited data examine persistence of benefits after completion of exercise interventions. Unfortunately, variability in outcome measures and exercise programs makes it difficult to compare findings across studies.
To address these issues, we aimed to directly compare how tango, treadmill walking, and stretching exercise classes with matching delivery variables affect gait, balance, and motor function in PD immediately following the intervention and after a period without continued intervention. We hypothesized that different types of exercise would preferentially improve certain deficits in PD through targeted training, and the effects would persist short term in the absence of continued training. Specifically, for our primary aim, we hypothesized that persons in the tango and treadmill groups would improve in forward walking, persons in tango would also improve in backward walking, and no changes in walking velocity in the stretching group would be observed. For our secondary aims, we hypothesized that both tango and treadmill would improve motor symptom severity, and dynamic balance and quality of life would improve more among those people in the tango group compared with treadmill and stretching. If different types of exercise best address specific impairments in PD, this could inform the development of personalized or combined programs that may be more beneficial than single-mode training.
MATERIALS AND METHODS
This was a prospective, controlled trial evaluating the effects of 3 exercise interventions (tango, treadmill, and stretching) on gait and mobility in people with PD. Data were collected between 2013 and 2016. Participants were recruited and serially assigned to the exercise intervention currently enrolling by a research assistant. Serial enrollment, rather than purely random assignment, was required to accommodate limited availability of exercise instructors and the need to complete the trial in a timely fashion. Class sizes ranged from 8 to 13 participants with 3 or 4 waves of classes per intervention. Participants provided written informed consent and the study was approved by the Washington University Human Research Protection Office. All aspects of the study occurred in research facilities on the School of Medicine campus at Washington University in St Louis.
Participants with idiopathic PD were recruited from the Washington University School of Medicine's Movement Disorders Center, the Greater St Louis Area Chapter of the American Parkinson Disease Association, and the surrounding St Louis community. Inclusion criteria were 30 years and older, clear benefit from levodopa, Hoehn & Yahr stages I to IV, ability to walk independently with or without an assistive device for at least 10 ft, no history of vestibular disease or dementia, and diagnosis of “clinically definite PD.”10 Briefly, a clinically definite PD diagnosis requires a participant to demonstrate either 3 of the following features, or 2 symptoms with 1 of the first 3 displaying asymmetry: rest tremor, rigidity, bradykinesia, or postural instability; as well as 3 or more of the following features: unilateral onset, persistent asymmetry, rest tremor, progression, excellent subjective response to levodopa, severe levodopa-induced chorea, levodopa response of at least 5 years or more, or clinical course of at least 10 years. Exclusion criteria included a medical condition for which exercise is contradicted, evidence of abnormality other than PD-related changes on brain imaging, history or evidence of neurological deficit other than PD such as stroke or muscle disease, or orthopedic or muscular problem. Participants were instructed to continue ongoing exercise but not begin new exercise activities until after the follow-up evaluation.
Participants completed community-based group exercise classes twice per week for 12 weeks. Class sessions lasted 1 hour and included a brief warm-up and cooldown at the beginning and end, respectively. Warm-up and cooldown activities were the same across all 3 classes, were minimal, and involved deep breathing exercise, trunk rotation, moving neck side-to-side, walking in a circle, side bending stretch, and bending over to touch knees. The same set of 3 music (tango) CDs was used during all interventions with a new CD introduced every 4 weeks. All interventions were overseen by a physical therapist knowledgeable of PD. Instructors for the stretching and treadmill groups were laboratory staff trained to work with people who have PD. The tango dance instructors also had training on how to work with people with PD but did not have formal training in tango adapted for people with PD. Two makeup classes were offered for all groups, and participants had to attend at least 19/26 classes for inclusion in analyses.
Participants practiced Argentine tango using an adapted curriculum for persons with PD. Initial classes focused on basic steps; more complex steps and sequences were added over 12 weeks (see Supplementary Digital Content 2, for review of tango syllabus, available at: http://links.lww.com/JNPT/A238). Participants were asked to change partners and to change roles from leader to follower several times during the course of each session. Dance partners were spouses, caregivers, volunteers, and laboratory staff. The syllabus was standardized and the same instructors taught all tango classes to maintain consistency.
To approximate the intensity of activity in the tango classes, treadmill participants walked at their preferred overground walking speed. Preferred speed was assessed weekly and treadmill settings were adjusted individually to match overground walking speeds. Treadmills were arranged in groups of 4 (2 pairs facing each other) to allow for social interactions.
This active control group focused on gentle stretching and whole-body flexibility exercises designed for people with PD.11,12 Exercises targeting strength were not included. All exercises were performed seated or standing with support to limit balance challenge (see Supplemental Digital Content 2, for review of stretching syllabus, available at: http://links.lww.com/JNPT/A238). Social interactions were encouraged through partnered stretching and while holding stretches.
Gender, age, height, weight, Mini-Mental State Examination (MMSE),13 years since PD diagnosis, levodopa-equivalent daily dose,14 Physical Activity Scale for the Elderly,15 and Activities-Specific Balance Confidence Scale16 were collected at baseline.
The Mini-Balance Evaluation Systems Test (Mini-BESTest) to measure dynamic balance,17 the Movement Disorders Society Unified Parkinson Disease Rating Scale motor subsection (MDS-UPDRS-III) scores with Hoehn & Yahr staging18 to measure motor symptom severity, and the Parkinson Disease Questionnaire-39 (PDQ-39)19 to measure quality of life were assessed at baseline, after the 12-week intervention (posttest), and follow-up (12 weeks after posttest). Spatiotemporal gait characteristics were also collected at all 3 time points using a 5-m GAITRite walkway (CIR Systems Inc, Franklin, New Jersey). Participants walked at their “normal, comfortable pace” forward (FWD) and backward (BKD). Three trials of each were averaged for analyses. Ground covered (meters) is also reported for the 6-minute walk test (SMWT). For the SMWT, participants were asked to “walk for 6 minutes, covering as much ground as possible” back and forth along a 30-m path.
Participants were assessed in the practically defined OFF-medication state (≥12-hour withdrawal from anti-Parkinson medications) and evaluations occurred at the same time of day for all time points for each participant. Participants were permitted to rest as often as needed during each evaluation session.
Blinded ratings were used in analyses for the MDS-UPDRS-III and the Mini-BESTest. Videos were assigned unpatterned 10-character alphanumeric codes to ensure the MDS-certified rater was blinded to group, medication status, and time point.
Baseline characteristics were compared between groups using χ2, analysis of variance, or Kruskal-Wallis, as appropriate. Generalized estimating equations (GEEs) with time (baseline, posttest, and follow-up), group (tango, treadmill, and stretching), and the interaction of time by group as categorical predictors were conducted for each of our outcomes: FWD gait velocity, BKD gait velocity, SMWT, Mini-BESTest, MDS-UPDRS-III, and PDQ-39. GEE models are able to account for within-subject correlations of repeated measures using an autoregressive correlation structure and include all available data points using the all-available-pairs method.20 Normal distributions using the identity link were specified. Residuals from each GEE model were checked for extreme outliers. One participant in the treadmill group had an extreme outlier at follow-up for the Mini-BESTest. As a conservative method, this value was changed to match baseline and posttest to indicate no change. Wald-test statistics for type 3 GEE analysis are reported along with the parameter estimates and robust empirical standard error estimates. Simple differences of the group by time interactions least square means were examined to determine the significant changes for each outcome. A significance level of P < 0.05 initially set for primary outcome; however, due to multiple comparisons for 6 outcomes, a probability level less than a corrected P < 0.008 was considered significant for the GEE estimates. SAS 9.4 was used for statistical analyses. A power analysis using the clinically meaningful difference of 0.1 m/s for forward velocity, 0.2 standard deviation,21 and 80% power indicated a total sample size of 42 was needed. To account for 30% attrition, a sample size of 55 was needed for this 3-group repeated measure analysis.
No adverse events were reported. Twenty-two participants who withdrew or had incomplete data were excluded from analyses (Figure 1). Baseline characteristics for the 22 individuals excluded from the analyses (Table 1) were not different from the included participants for gender, age, height, weight, MMSE, years since PD diagnosis, levodopa-equivalent daily dose, Physical Activity Scale for the Elderly, Activities-Specific Balance Confidence Scale, or baseline MDS-UPDRS-III scores (P > 0.05, Table 1). Spearman correlation between Hoehn & Yahr stage and group assignment was not significant among those who did not finish the study (r = −0.03, P = 0.90). Exercise groups did not differ in any of the aforementioned baseline characteristics (P > 0.05, Table 1) nor did they differ at baseline for any of the outcome measures.
Table 1. -
Participant Demographics at Baseline
||Alla (n = 96)
||Tango (n = 39)
||Treadmill (n = 31)
||Stretching (n = 26)
||Drop/Incomplete (n = 22)
|Disease duration, y
|Hoehn & Yahr
Abbreviations: ABC, Activities-Specific Balance Confidence Scale; LEDD, Levodopa Equivalent Daily Dose; MDS-UPDRS-III, Movement Disorders Society Unified Parkinson Disease Rating Scale-III; MMSE, Mini-Mental State Examination; PASE, Physical Activity Scale for the Elderly; SD, Standard deviation.
aDoes not include participants counted in the dropped out/incomplete column.
bDrop/Incomplete is n=21 due to missing data on one participant's measure.
Wald estimates for the overall models are presented in Table 2. Analyses of GEE parameter estimates with empirical standard errors and simple differences for the interaction terms with confidence intervals are included in Supplemental Digital Content 3 (available at: http://links.lww.com/JNPT/A239). Means and standard errors are illustrated in Figure 2 (also see Supplemental Digital Content 3).
Table 2. -
Wald Statistics for Generalized Estimating Equation Analysis
||Pr > χ2
||Time × group
||Time × group
||Time × group
||Time × group
||Time × group
||Time × Group
Abbreviations: MDS-UPDRS-III, Movement Disorders Society Unified Parkinson Disease Rating Scale-III; Mini-BESTest, Mini-Balance Evaluation Systems Test; PDQ-39, Parkinson Disease Questionnaire-39; SMWT, 6-minute walk test.
aP < 0.008.
For forward velocity, the Wald estimates for time and group were not significant, nor was the interaction. However, the GEE parameter estimates indicated a trend toward the treadmill group improving between baseline and posttest (Figure 2A) compared with the stretching group (b = 6.98, standard error = 3.3, P = 0.03) and this improvement was maintained through follow-up. For backward velocity, the Wald estimates and GEE parameter estimates indicated a significant time effect. Simple differences indicate the treadmill (P < 0.0001) and stretching (P = 0.005) groups significantly improved between baseline and posttest, and the increase in backward velocity was maintained at follow-up for the treadmill group (Figure 2B). The Wald estimate for time was also significant for the SMWT; the tango group showed the most improvement among the 3 groups between baseline and posttest (P = 0.026), but they also declined more than the other 2 groups between posttest and follow-up (Figure 2C). None of the effects were significant for the Mini-BESTest (Figure 2D). Both Wald and GEE estimates indicated significant effects of time for the MDS-UPDRS-III; the stretching group significantly improved between baseline and posttest (P = 0.0004); however, the improvement was not maintained from posttest to follow-up (Figure 2E). The PDQ-39 measure showed significant time and time by group effects; simple differences indicated no improvement between baseline and posttest for any group, but the stretching group improved between posttest and follow-up (Figure 2F).
This study is the first to directly compare tango, treadmill, and stretching interventions with similar delivery variables in people with PD. While our results indicate different exercises may differentially improve outcomes relating to gait, motor functioning, balance, and quality of life, few of our hypotheses were confirmed. It is worth noting that our results may have been different if we measured participants in the “ON” state that more closely corresponds to their everyday living. We conducted assessments in the “OFF” state to reduce variance associated with Parkinson-related medications.
For our outcomes relating to gait, we anticipated improvements for both the tango and treadmill groups for forward velocity, but this was only true for participants in the treadmill group. We also expected improvement among the tango group in backward velocity considering the dance includes backward stepping. However, while the tango group showed some improvement, the stretching and treadmill groups both significantly improved their backward walking velocity between baseline and posttest. Moreover, this improvement persisted for the treadmill group. With regard to walking endurance, all 3 groups improved on the SMWT with tango improving the most, although these changes were not significant.
We speculate that the lack of improvement on the gait assessments for the tango group may be related to more time spent observing and learning dance steps compared with the treadmill group engaging in continuous walking during the classes, or related to the training of the instructors for the tango classes. Previously, our tango instructors were physical therapists, certified personal trainers, or movement scientists with training in dance, whereas for this intervention the dance instructors were not trained in physical therapy or movement science.
Our results do suggest treadmill exercise may be beneficial for forward and backward walking. Our findings are similar to a systematic review that reported treadmill training in PD increased gait speed and stride length, but walking distance did not consistently improve,6 and an independent study showed increases on the SMWT for people with PD in a low-intensity treadmill intervention as well as in a stretching and resistance intervention.8 In regard to stretching, a previous intervention designed to increase spinal flexibility and improve mobility reported favorable outcomes in functional axial rotation.22 Similarly, it is possible that the stretching group may have improved in backward walking because of enhanced flexibility and freedom of movement.
Next, we predicted the tango and treadmill groups would experience improvements on the MDS-UPDRS-III, a measure of motor symptom severity. While all 3 groups improved, the improvement was only significant for the stretching group. This is in keeping with a previous study that found improvement on the MDS-UPDRS-III among people in a stretching group compared with treadmill training.8 In addition, Schenkman and colleagues23 found less change on this measure among people with PD in a high-intensity treadmill exercise group compared with a moderate-intensity exercise group or usual care.23
Lastly, we expected the tango group would also experience benefits in balance and quality of life. Changes in balance, as tested with the Mini-BESTest, were unremarkable. We may have seen changes in balance with a more sensitive posturographic assessment. Quality-of-life scores also did not change between baseline and posttest for any of our groups. This may be related to the length of our study, as a sensitivity to change analyses noted 4 months may be too brief of a period to observe noticeable changes on the PDQ-39.24 A 6-month study comparing a progressive resistance exercise intervention to a stretching, balance, and strengthening exercise program among people with PD found improvement in PDQ-39 scores among the former intervention only.25
We also considered whether our findings indicated any improvements that were clinically meaningful. The treadmill group changed the most in forward gait velocity (6.3 cm/s). The stretching group changed the most in backward velocity (10 cm/s) and motor symptom severity (4.65 points). The tango group changed the most in timed walking distance (4.4%). None of these differences are of a magnitude that would make them clinically meaningful.
Strengths of our exercise interventions include keeping the warm-ups and cooldowns, session length, sessions per week, intervention duration, class environment, and class location consistent across classes. However, further investigation of the components and variables necessary and sufficient for a successful exercise program may facilitate design of optimal combined or tailored programs for persons with PD. Components may relate to the physical activity performed (intensity, duration, and type), class environment (groups size, instructor interaction, and social/emotional support), participant characteristics (baseline activity levels and disease severity), and/or participant education/expectations (knowledge of exercise benefits, motivation, and belief in effectiveness). For example, participants in our treadmill training group walked at their preferred overground walking speed to approximate the intensity of the tango group, whereas other researchers have found beneficial effects of high-intensity treadmill training compared with moderate-intensity.23 Thus, future studies should consider maximizing an individual's response to exercise and tailoring the program to match each individual's baseline function and ability to progress.
Likewise, considering the impact of personalized medicine approaches for exercise compared with group programs is important for this population. King et al26 reported that individualized physical therapy focusing on function and balance combined with group therapy to improve gait may be more efficacious than unsupervised exercise among people with PD.26 Future work should also investigate the differential effects of interventions and retention of benefits for active versus sedentary individuals and investigate what other factors may be predictive of responsiveness to exercise. Additional studies are needed before definitive recommendations can be made.
To our surprise, the improvements noted in all 3 groups across 3 months of exercise were modest at best and not of sufficient magnitude to be clinically meaningful. Nonetheless, the improvements suggest group exercise, regardless of modality, may convey some benefit to individuals with PD. This is in keeping with prior studies and suggests that patients have a variety of potentially beneficial options to pursue when considering community-based group exercise approaches. Regardless of the form of exercise, the maintenance of participation over the course of the disease is likely a critical factor. As such, patient preference and motivation, in addition to feasibility and effectiveness of different exercise approaches, should be taken into account when determining which activities will be useful for a given person. Future research should examine what factors predict who will benefit the most and who will remain engaged over the long-term, in various exercise approaches. There is also a need for studies examining optimization of exercise dosing and whether multifaceted approaches (eg, employing stretching, treadmill, and tango in combination) are more effective than single-mode approaches.
1. Shen X, Wong-Yu IS, Mak MK. Effects of exercise
on falls, balance, and gait ability in Parkinson's disease: a meta-analysis. Neurorehabil Neural Repair. 2016;30(6):512–527. doi:10.1177/1545968315613447.
2. Fahn S. Description of Parkinson's disease as a clinical syndrome. Ann N Y Acad Sci. 2003;991(1):1–14. doi:10.1111/j.1749-6632.2003.tb07458.x.
3. McNeely ME, Duncan RP, Earhart GM. Medication improves balance and complex gait performance in Parkinson disease
. Gait Posture. 2012;36(1):144–148. doi:10.1016/j.gaitpost.2012.02.009.
4. Shulman LM, Gruber-Baldini AL, Anderson KE, et al. The evolution of disability in Parkinson disease
. Mov Disord. 2008;23(6):790–796. doi:10.1002/mds.21879.
5. Sharma NK, Robbins K, Wagner K, Colgrove YM. A randomized controlled pilot study of the therapeutic effects of yoga in people with Parkinson's disease. Int J Yoga. 2015;8(1):74–79. doi:10.4103/0973-6131.146070.
6. Mehrholz J, Kugler J, Storch A, Pohl M, Hirsch K, Elsner B. Treadmill
training for patients with Parkinson's disease. Cochrane Database Syst Rev. 2015;(9):CD007830. doi:10.1002/14651858.CD007830.pub4.
7. Lötzke D, Ostermann T, Büssing A. Argentine tango
in Parkinson disease
—a systematic review and meta-analysis. BMC Neurol. 2015;15:226. doi:10.1186/s12883-015-0484-0.
8. Shulman LM, Katzel LI, Ivey FM, et al. Randomized clinical trial of 3 types of physical exercise
for patients with Parkinson disease
. JAMA Neurol. 2013;70(2):183–190. doi:10.1001/jamaneurol.2013.646.
9. Duncan RP, Earhart GM. Randomized controlled trial of community-based dancing to modify disease progression in Parkinson disease
. Neurorehabil Neural Repair. 2012;26(2):132–143. doi:10.1177/1545968311421614.
10. Racette BA, Rundle M, Parsian A, Perlmutter JS. Evaluation of a screening questionnaire for genetic studies of Parkinson's disease. Am J Med Genet. 1999;88(5):539–543.
11. Ellis T, Rork T, Dalton D. Be Active! An Exercise
Program for People With Parkinson's Disease. Staten Island, NY: The American Parkinson Disease
Association; 2008. https://www.apdaparkinson.org/uploads/files/BeActive_Feb2008-enw.pdf
12. Cianci H. Parkinson's Disease: Fitness Counts. Miami, FL: National Parkinson Foundation; 2006. http://www.parkinson.org/sites/default/files/Fitness_Counts.pdf
13. Cockrell JR, Folstein MF. Mini-Mental State Examination (MMSE). Psychopharmacol Bull. 1988;24(4):689–692.
14. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE. Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Mov Disord. 2010;25(15):2649–2653. doi:10.1002/mds.23429.
15. Washburn RA, Ficker JL. Physical Activity Scale for the Elderly (PASE): the relationship with activity measured by a portable accelerometer. J Sports Med Phys Fit Turin. 1999;39(4):336–340.
16. Powell LE, Myers AM. The Activities-specific Balance Confidence (ABC) Scale. J Gerontol Ser A. 1995;50A(1):M28–M34. doi:10.1093/gerona/50A.1.M28.
17. Franchignoni F, Horak F, Godi M, Nardone A, Giordano A. Using psychometric techniques to improve the Balance Evaluation Systems Test: The mini-BESTest. J Rehabil Med. 2010;42(4):323–331. doi:10.2340/16501977-0537.
18. Goetz CG, Tilley BC, Shaftman SR, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008;23(15):2129–2170. doi:10.1002/mds.22340.
19. Jenkinson C, Fitzpatrick R, Peto V, Greenhall R, Hyman N. The Parkinson's Disease Questionnaire (PDQ-39): development and validation of a Parkinson's disease summary index score. Age Ageing. 1997;26(5):353–357. doi:10.1093/ageing/26.5.353.
20. Ballinger GA. Using generalized estimating equations for longitudinal data analysis. Organ Res Methods. 2004;7(2):127–150. doi:10.1177/1094428104263672.
21. Hackney ME, Earhart GM. Short duration, intensive tango
dancing for Parkinson disease
: an uncontrolled pilot study. Complement Ther Med. 2009;17(4):203–207. doi:10.1016/j.ctim.2008.10.005.
22. Schenkman M, Cutson TM, Kuchibhatla M, et al. Exercise
to improve spinal flexibility and function for people with Parkinson's disease: a randomized, controlled trial. J Am Geriatr Soc. 1998;46(10):1207–1216. doi:10.1111/j.1532-5415.1998.tb04535.x.
23. Schenkman M, Moore CG, Kohrt WM, et al. Effect of high-intensity treadmill exercise
on motor symptoms in patients with de novo Parkinson disease
: a phase 2 randomized clinical trial. JAMA Neurol. 2018;75(2):219–226. doi:10.1001/jamaneurol.2017.3517.
24. Jenkinson C, Fitzpatrick R, Peto V. Sensitivity to change of the PDQ-39. In: The Parkinson's Disease Questionnaire: User Manual for the PDQ-39, PDQ-8, and PDQ Summary Index. Oxford, England: University of Oxford; 1998:34–37.
25. Corcos DM, Robichaud JA, David FJ, et al. A two-year randomized controlled trial of progressive resistance exercise
for Parkinson's disease. Mov Disord. 2013;28(9):1230–1240. doi:10.1002/mds.25380.
26. King LA, Wilhelm J, Chen Y, et al. Effects of group, individual, and home exercise
in persons with Parkinson disease
: a randomized clinical trial. J Neurol Phys Ther. 2015;39(4):204–212. doi:10.1097/NPT.0000000000000101.