BJMB
Brazilian Journal of Motor Behavior
Special issue:
“Control of Gait and Posture: a tribute to Professor Lilian T. B.
Gobbi”
!
Beretta et al.
2023
VOL.17
N.4
103 of 108
Effect of long-term locomotion and balance exercise on functional mobility considering
the Parkinson’s disease subtypes: a pilot study
VICTOR S. BERETTA
1,2
| DIEGO ORCIOLI-SILVA
2
| DIEGO A. R. JAIMES
3
| BEATRIZ R. LEGUTKE
2
| THIAGO M.
SIRICO
2
| PEDRO L. GONÇALVES
2
| LILIAN T. B. GOBBI
2
(in memoriam)
1
São Paulo State University (Unesp), School of Technology and Sciences, Physical Education Department, Presidente Prudente, Brazil
2
São Paulo State University (Unesp), Institute of Biosciences, Posture and Gait Studies Laboratory (LEPLO), Rio Claro, Brazil
3
Faculty of Human Sciences and Education, Los Llanos University, Villavicencio, Colombia
Correspondence to:!Victor Spiandor Beretta Ph.D., São Paulo State University (Unesp), School of Technology and Sciences, Physical Education Department, Rua
Roberto Simonsen, 305 Zip code: 19060-900 - Presidente Prudente/SP, Brasil.
email: victor.beretta@unesp.br
https://doi.org/10.20338/bjmb.v17i4.360
HIGHLIGHTS
• Exercise improves functional mobility in dual-task
conditions in both PD subtypes.
• Both PD subtypes increase lower limb functional
strength after 16 weeks of exercise.
• The PIGD subtype improves functional mobility after 16
weeks of physical exercise.
• The severity of motor symptoms and cognitive condition
were not improved by exercise.
ABBREVIATIONS
DT Double-task
H&Y Hoehn & Yahr scale
MMSE Mini-Mental State Examination
PD Parkinson’s disease
PIGD Postural Instability and Gait Difficulty
post-test Post-intervention
pre-test Baseline
PwPD People with Parkinson’s disease
ST Single-task
TD Tremor Dominant
TUG Timed Up and Go test
UPDRS Unified Parkinson’s Disease Rating Scale
PUBLICATION DATA
Received 17 04 2023
Accepted 17 06 2023
Published 20 06 2023
BACKGROUND: Different clinical subtypes (i.e., Postural Instability and Gait Difficulty -PIGD
and Tremor Dominant -TD) have been highlighted in Parkinson's disease (PD). Although
physical exercise improves motor symptoms in PD, the knowledge about the effect of physical
exercise considering the PD subtype is limited.
AIM: To compare the effects of long-term locomotion and balance exercise on lower limb
functional strength and functional mobility in PD subtypes.
METHOD: Eight individuals PIGD and 10 TD participated in this study. All individuals
participated in the interventions with exercises focused on improving locomotion and balance.
48 sessions of exercise were performed three times per week for 60 minutes each session.
Functional Mobility was analyzed by the Timed Up and Go test (TUG) in a single (ST) and
double-task (DT – i.e., subtraction by three). Lower limb functional strength was analyzed by
the 30s sit-to-stand test. Both tests were performed at baseline (pre-test) and post-
intervention (post-test). Statistical analysis was performed by two-way ANOVA, with Group
(PIGD vs. TD) and Moment (pre vs. post-test) factors, with repeated measures for the second
factor.
RESULTS: PIGD decreased the time to perform TUG_ST in the post-test compared to the
pre-test (p=0.001). Both groups decreased the time in TUG_DT and increased the number of
repetitions in sit-to-stand test in the post-test in relation to the pre-test (p<0.05).
CONCLUSION: Long-term locomotion and balance exercise programs can improve functional
mobility mainly in PIGD. A possible explanation is due to the greater room for improvement of
PIGD subtypes and exercise specificity.
KEYWORDS: Physical activity | Rehabilitation | Exercise | Postural Instability and Gait Difficulty
| Tremor dominant
INTRODUCTION
The decrease of dopaminergic neurons in the basal ganglia, characteristic of Parkinson's disease (PD), promotes dysfunction
in several cortical and subcortical structures involved in the control and execution of voluntary movements and cognitive resources
1
. This
dysfunction causes motor deficits in people with PD (PwPD) such as bradykinesia, rigidity, resting tremor, gait impairments, and postural
instability
2
. In addition to motor symptoms, PwPD demonstrates non-motor symptoms such as cognitive impairments, anxiety, and
depression
2
. Although the PD symptoms are well-characterized, the prevalence of each one is variable.
PD is recognized as a heterogeneous neurodegenerative disease with different clinical features
3
. Due to the PD heterogeneity,
PwPD has been classified into two subtypes according to different clinical characteristics: postural instability and gait difficulty (PIGD) and
tremor dominant (TD)
4
. PIGD is characterized by the presence of severe gait impairments, postural instability, bradykinesia, and muscle
rigidity
3,4
. Also, PIGD subtype has faster disease progression, late-onset, and higher fall risk
5
. TD subtype has slower disease
progression and a predominance of tremor symptoms
2–4
.
Medication intake is the most common treatment for PD. Pharmacotherapy relieves the signs and symptoms of the disease, but
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
(
Beretta et al.
2023
VOL.17
N.4
104 of 108
Special issue:
“Control of Gait and Posture: a tribute to Professor Lilian T. B. Gobbi”
the impairments in some gait parameters and postural control are persistent
6
. Also, continuous use of the medication can bring several
side effects and diminish their effects over time. Thus, physical exercise has been increasingly explored in PD as a complementary
intervention to pharmacotherapy
7,8
. Physical exercise improves neurophysiological aspects (e.g., dopamine concentration and release)
9
,
improve motor symptoms in PwPD, and reduced the risk of falls
10
. The exercises focused on balance and locomotion in PwPD have
improved balance and gait function and reduced falls in PwPD
11,12
.
Studies investigating the characteristics and the effects of different interventions considering the PD subtypes are relevant to
advance the knowledge and propose optimized interventions for each condition in this population. A previous study highlighted the need
for personalized medicine in PD considering its subtypes (e.g., development of genotype-specific therapies) due to the development and
characteristics of each clinical subtype
13
. Although a short-term multidisciplinary exercise program (i.e., two weeks) improved motor
symptoms severity, balance, and functional mobility in both PD subtypes, the benefits in motor symptoms were superior in PIGD subtype
14
. However, to the best of our knowledge, there is a lack of information regarding the effects of a long-term exercise intervention in PIGD
and TD subtypes
15
.
Thus, this pilot study aimed to compare the effects of 48 sessions of locomotion and balance exercise on functional mobility in
PwPD considering the PIGD and TD subtypes. We expected that both PD subtypes would improve functional mobility after the exercise
program. We also expected that this improvement would be greater in the PIGD subtype due to the exercise specificity of the proposed
intervention considering the exacerbated deficits that could impact balance and gait performance in this subtype
14
.
METHODS
Participants
Eighteen PwPD participated in this pilot study and were distributed into two groups according to the PD subtype (eight PIGD
and ten TD). The participants were selected through a database from the Program of Physical Activity for People with Parkinson's
disease (PROPARKI). For inclusion criteria, PwPD should be diagnosed based on UK Brain Bank criteria, age > 50 years, took PD
medication, should present a score between one and three in the adapted Hoehn & Yahr scale (H&Y), and independent locomotion.
Exclusion criteria were: i) cognitive decline (score<24 in Mini-Mental State Examination – MMSE)
16
; ii) musculoskeletal, vestibular, or
visual impairments that made it impossible to participate in experimental procedures; and (iii) failing to attend at least 70% of the
sessions. Study approval was obtained from the research ethics committee at São Paulo State University (Unesp) (n. 1058). All
participants gave their signed informed consent before their participation.
Experimental procedures
The experimental protocol was conducted over four months. All experimental procedures (i.e., assessments of clinical
characteristics, cognition, lower limb functional strength, and functional mobility and the physical exercise sessions) were performed at
Unesp Rio Claro. Clinical and cognitive characteristics, lower limb functional strength, and functional mobility were collected before and
after 16 weeks of the physical exercise program.
Clinical, cognitive, and functional mobility assessment
For clinical, cognitive, and functional mobility characteristics, participants attended the Posture and Gait Studies Laboratory
(LEPLO) at the same University in two different times (before and after physical exercises). A specialist researcher applied the Unified
Parkinson’s Disease Rating Scale (UPDRS) and the H&Y scale adapted version to evaluate the severity of the symptoms and the stage
of PD, respectively. Also, the UPDRS was used to classify the individuals according to the PD subtype
4
. For that, we calculated the ratio
of the mean UPDRS tremor scores (i.e., eight items) to the mean UPDRS PIGD scores (i.e., five items). The PIGD group included
individuals with ratios ≤1, while the TD group included individuals with ratios ≥1.5
4
. individuals with ratios between 1 and 1.5 were
classified as indeterminate and were excluded from the study. MMSE was performed to assess global cognition.
Functional mobility was evaluated by the Timed Up and Go test (TUG). The TUG involves standing up from a chair, walking
three meters, turning around, walking back to the chair, and sitting down as quickly and safely as possible without running. Participants
performed three trials of the TUG under two conditions: single-task (ST) and dual-task (DT). In DT, participants completed the task
described above while counting backward by 3’s from the pre-selected number (i.e., 30, 42, and 51). The time to perform the test was
measured using a stopwatch and the average of the three trials was considered as the functional mobility performance for each condition.
Lower limb functional strength was assessed by the 30-second sit-to-stand test. Participants were instructed to stand up
(completely) and sit down from a chair as quickly as possible for 30 seconds. The number of repetitions was registered and considered
as the performance of lower limb functional strength.
BJMB! ! ! ! ! ! ! ! !
Brazilian(Journal(of(Motor(Behavior(
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Beretta et al.
2023
VOL.17
N.4
105 of 108
Special issue:
“Control of Gait and Posture: a tribute to Professor Lilian T. B. Gobbi”
Physical exercise intervention
The physical exercise program was performed for 16 weeks, three times a week, totalizing 48 sessions, and included exercises
focused to improve the locomotion, balance, and cognition of PwPD. All sessions lasted 60 min (10 min of warm-up, 40 min main part,
and 10 min cooldown)
7
. The main part was composed of locomotion and balance exercises that manipulated the step length, velocity,
and width, the sensorial conditions (i.e., visual, vestibular, and somatosensory systems), proprioception stimulus, and the task conditions
(i.e., different support bases and direction). The progression was performed every eight sessions by increasing the exercise complexity
(i.e., manipulating the surface, such as walking or standing on a firm or on a foam surface; manipulating the base of support, such as
walking on top of a rope, or on a low or high balance beam, standing in two or one legs; manipulating the vision, such as standing with
eyes open or closed) and intensity (i.e., increasing the velocity of movement execution or the number of exercises).
In addition, we included activities with DT to increase motor and cognitive function during the exercise, hence increasing the
exercise complexity. We added motor (e.g., throwing a ball/balloon in the air, touching a ball, or moving the arms and hands in different
ways) or cognitive secondary tasks (e.g., doing mathematical calculations or naming countries, animals, and objects) to the first task (i.e.,
walking or balance maintenance). The DT activities were performed in the last 40 sessions of the intervention. Sixteen sessions focused
mainly on cognitive DT and the other 24 on cognitive and motor DT activities. The individuals were encouraged to take their usual PD
medication during the intervention
7
.
Statistical analysis
Statistical analyses were performed by SPSS 22.0 software (SPSS, Inc.). The significance level was maintained as p<0.05.
Normality and homogeneity were verified by Shapiro-Wilk and Levene tests, respectively. Clinical and cognitive sample characteristics of
each subtype at pre-test were compared by Student t-test for independent samples or Mann-Whitney U test. Two-way ANOVA, with
Group (PIGD vs. TD) and Moment (pre vs. post-test) as factors, with repeated measures for the second factor was conducted to analyze
the effect of long-term exercise on lower limb functional strength, functional mobility, PD symptoms severity, and cognitive condition.
Bonferroni post hoc test with was applied when interaction between the factors and main effect of the moment were indicated in the
analysis.
RESULTS
Statistical analysis indicated that both groups were similar in the demographic characteristics, UPDRS motor section (p=0.722),
UPDRS total (p=0.098), and MMSE (p=0.298) at the pre-test (Table 1).
Table 1. Characteristics of PD subtypes at pre-test. Parametric variables are displayed as mean ± standard deviations and non-
parametric variables (scales and non-normally distributed data) as medians (quartiles).
PIGD (n=8)
TD (n=10)
p-value
Age (years)
69.88±11.28
71.00±6.46
0.793
Sex (M/F)
3/5
7/3
---
Body Mass (kg)
72.18±9.82
72.19±13.09
0.998
Height (cm)
160.88±7.45
163.75±10.02
0.510
H&Y stage (1.5/2/2.5/3)
0/4/3/1
1/7/2/0
---
ANOVA revealed Group*Moment interaction for the TUG in ST condition (F
1,16
= 5.647; p=0.030; ƞ
p
2
=0.261) (Figure 1). Post
hoc tests indicated that PIGD individuals decrease the time to complete the TUG at the post-test compared to the pre-test (p=0.001). In
addition, ANOVA revealed main effect of moment for TUG in DT condition (F
1,16
= 10.382; p=0.005; ƞ
p
2
=0.394) and lower limb functional
strength (F
1,16
= 5.120; p=0.038; ƞ
p
2
=0.242) (Figure 1). The ANOVA indicated that individuals, independent of PD subtype, decrease the
time to complete TUG in DT condition (delta = -1.65 seconds) and increase the number of repetitions in 30s sit-to-stand test (delta = 2.39
repetitions) at post-test in relation to pre-test.