Balance Versus Resistance Training On Postural Control in Patients With Parkinsons Disease

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COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
© 2016 EDIZIONI MINERVA MEDICA European Journal of Physical and Rehabilitation Medicine 2017 April;53(2):173-83
Online version at http://www.minervamedica.it DOI: 10.23736/S1973-9087.16.04313-6
ORIGINAL ARTICLE
Balance versus resistance training on

postural control in patients with Parkinson’s
disease: a randomized controlled trial
Suhaila M. SANTOS 1 *, Rubens A. da SILVA 2, Marcelle B. TERRA 1, 2,
Isabela A. ALMEIDA 1, 2, Lúcio B. de MELO 3, Henrique B. FERRAZ 4
1Department of Physiotherapy, Londrina State University, Londrina, Brazil; 2Norte do Paraná University, Londrina, Brazil; 3Department
of Neurology, Londrina State University, Londrina, Brazil; 4Department of Neurology and Neurosurgery, Federal University of São
Paulo, São Paulo, Brazil
*Corresponding author: Suhaila M. Santos, Department of Physiotherapy, Londrina State University, Av. Robert Koch 60, 86.038-350, Londrina, PR, Brazil.
E-mail: suhailaneuro@gmail.com
ABSTRACT
BACKGROUND: Evidences have shown that physiotherapy programs may improve the balance of individuals with Parkinson’s disease (PD),
although it is not clear which specific exercise program is better.
AIM: The aim of this study was to compare the effectiveness of balance versus resistance training on postural control measures in PD patients.
DESIGN: Randomized controlled trial.
SETTING: The study was conducted in a physiotherapy outpatient clinic of a university hospital.
POPULATION: A total of 40 PD participants were randomly divided into two groups: balance training (BT) and resistance training (RT).
METHODS: The BT group focused on balance training, functional independence and gait while the RT group performed resistance exercises
emphasizing the lower limbs and trunk, both supervised by trained physiotherapists. Therapy sessions were held twice a week (at 60 minutes),
totaling 24 sessions. The primary outcome was evaluated by force platform with center of pressure sway measures in different balance conditions
and the secondary outcome was evaluated by Balance Evaluation Systems Test (BESTest) scale to determine the effects of the intervention on
postural control.
RESULTS: Significant improvement of postural control (pre vs. post 15.1 vs. 9.6 cm2) was only reported in favor of BT group (d=1.17) for one-
legged stand condition on force platform. The standardized mean difference between groups was significantly (P<0.02), with 36% of improve-
ment for BT vs. 0.07% for RT on this condition. Significant improvement (P<0.05) was also observed in favor of BT (in mean 3.2%) for balance
gains in some BESTest scores, when compared to RT group (-0.98%).
CONCLUSIONS: Postural control in Parkinson’s disease is improved when training by a directional and specific balance program than a resist-
ance training program.
CLINICAL REHABILITATION IMPACT: Balance training is superior to resistance training in regard to improving postural control of individu-
als with PD. Gold standard instruments (high in cost and difficult to access) were used to assess balance, as well as scales with clinical appli-
cability (low cost, easily acceptable, applicable and valid), which can guide the management of physiotherapists both in their decision-making
and in clinical practice.
(Cite this article as: Santos SM, da Silva RA, Terra MB, Almeida IA, de Melo LB, Ferraz HB. Balance versus resistance training on postural control
in patients with Parkinson’s disease: a randomized controlled trial. Eur J Phys Rehabil Med 2017;53:173-83. DOI: 10.23736/S1973-9087.16.04313-6)
Key words: Parkinson disease - Postural balance - Neurological rehabilitation.
or other proprietary information of the Publisher.
P arkinson’s disease (PD) presents a combination of

symptoms, such as resting tremors, bradykinesia,
rigidity, postural instability, freezing of gait and cog-
nitive impairment.1 Muscle strength and power is also
reduced in this population when compared to healthy
elderly individuals and consequently, these factors can
Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 173

not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
©
SANTOS BALANCE VS. RESISTANCE TRAINING FOR PARKINSON’S DISEASE
reduce the functional capacity of individual with Par- comprising of 401 participants with early to advanced
kinson’s disease such as decreasing the walking speed PD, reported significant positive results in favor of re-
or mobility, balance capacity and in turn, increasing the sistance training compared to non-resistance training or
risk of falls.2 no intervention controls for muscle strength, balance
Some evidences have showed that postural instability and motor symptoms but not for gait, balance confi-
in PD is the most important factor for falls and increased dence and quality of life. When regarding specifically
morbidity.3 In fact, balance disorder represents nowa- balance results, only a study reported the use of COP
days a growing public health concern due to their as- sway measures for balance in their results, but during
sociation with falls, decline in independence and cause a walking task.2 At this moment, a limited number of
of injury-related hospitalization across older people.4 studies have made direct comparison between types
Adequate balance for PD is an skill to be working on of intervention for balance and functionality in PD. A
rehabilitation programs because life activities requires comparison based on postural control strategies by COP
complex integration of postural control system with re- sway, that is a reliable measure, during different balance
gard to promote appropriate motor responses to control conditions is also warranted.
body movement.5, 6 We hypothesized that the balance approach by motor
The complexity of controlling balance results in many control principles would relate better with balance re-
different types of balance problems that need systematic sults than resistance training. The main purpose of this
clinical assessment for effective treatment. Many clini- study was to assess the effect of two types of interven-
cal tests are designed to test a single “balance system”, tion on balance for PD patients: 1) balance training ap-
but balance control is complex and involves many dif- proach with directional exercises for postural control;
ferent underlying systems.7 and 2) resistance muscular training.
In the last decade, quantitative assessments of pos-
tural control during stance have been available as clini- Materials and methods
cal and research tool. Although different balance tools
are designated in the literature (Berg scale, Tinetti scale, This randomized clinical trial was conducted be-
Balance functional confidence, BESTest),7 few stud- tween February and August 2014 at Londrina State
ies have reported significant results on postural control University (Universidade Estadual de Londrina – UEL)
measures related to Centre of Pressure (COP) sway with in partnership with Norte do Paraná University at the
regard to balance directional rehabilitation program for Laboratory of Functional Assessment and Human Mo-
PD.8 COP parameters calculated from force platform tor Performance together with the Ágape Center of So-
data can provide finer information related to biome- cial Support (CASA) in Londrina, Brazil. The study
chanical and neuromuscular control strategies for main- was approved by the Institutional Review Board at the
taining balance among different populations.9‑12 State University of Londrina/University Hospital (Re-
Classical physiotherapy including some balance ex- port No. 028/2013), conducted according to standards
ercises may improve postural control in individuals with established by the Consort-Statement,19 and registered
PD.3 However, rehabilitation programs that require senso- and approved by REBEC (National Registry of Clini-
rimotor dexterity and functionality with an emphasis on cal Trials) under No. RBR-3p7zcf. All participants con-
exercises involving coordination, proprioception, chal- sented to participate in the study by signing free and
lenging balance tasks, gait training with speed variation, informed consent forms.
and cognitive tasks may also be most effective for increas-
ing the autonomy, independence and quality of life of these Randomization
individuals as reported previously 13‑15 and supported by a
systematic review with meta-analysis on this topic.16 The PD individuals were selected using a random
In addition, resistance training has been prescript for number table generator (www.random.org) and identi-
improving muscular endurance and strength, balance cal opaque sealed envelopes, identified with either “bal-
and functional capacity in healthy elderly individu- ance training” or “resistance training”. An independent
al.16-18 A recent systematic review with meta-analysis, researcher, working blind, performed the procedure and
174 European Journal of Physical and Rehabilitation Medicine April 2017

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BALANCE VS. RESISTANCE TRAINING FOR PARKINSON’S DISEASE SANTOS
the envelopes were opened in the presence of the par- Assessed for eligibility
ticipants initiating the formation of groups. The medica- (N.=62)
tion regimens of all the patients were maintained stable
throughout the entire experiment. Excluded (N.=22):
— Not meeting inclusion
criteria (N.=20)
Participants — Declined to participate
(N.=2)
The estimated sample size was 42 individuals with
PD, being 21 for the balance training group and 21 in
the resistance training group, considering an alpha of Randomized (N.=40)
5% and 90% power to detect a difference of 30% be-
tween groups.20 A total of 62 individuals diagnosed with
Parkinson’s disease attending the Medical Outpatient
Clinic of Neurology at the Hospital das Clínicas, State Allocated to Resistance Allocation Allocated to Balance
Training Group (RT) - Training Group (BT) -
University of Londrina were recruited, therefore, 40 (N.=19) (N.=21)
participants were randomized. The Figure 1 shows the
design and flow of the participants through the study:
21 were assigned to the balance training (BT) group, — Did not receive al- Post intervention — Did not receive al-
located intervention located intervention
while 19 were assigned to the resistance-training (RT) (N.=5): (N.=9):
group. We included individuals with idiopathic Parkin- - Withdrew (N.=4) - Withdrew (N.=6)
▪ More than 3 ▪ More than 3
son individuals according to criteria from the UK Brain falts in therapies falts in therapies
Bank,21 classified in stages from 1.5 to 3 according to (N.=4) (N.=4)
- Surgery: mastec- ▪ Change in dopami-
the Hoehn & Yahr Staging Scale,22 aged 50 years old or tomy (N.=1) nergic medication
older, able to walk independently, and not enrolled in (N.=2)
- Fall (N.=1)
any other therapeutic program besides medication. Indi- - Surgery: heart
viduals with neurological or musculoskeletal diseases, surgery (N.=1)/
cervical spine
associated or cognitive disorders that would potentially surgery (N.=1)
interfere in the assessment were excluded so that other
practices or preexisting diseases would not hinder data
collection or the therapeutic intervention. Completed (N.=14) Analysis Completed (N.=12)
Analyzed in ITT Analyzed in ITT
analysis (N.=19) analysis (N.=21)
Blinding
Figure 1.—CONSORT diagram of flow of participants in the study.
All physiotherapists engaged in the study (with the as-
sistance of students in Physiotherapy program) and re- 1) anthropometric data (weight, height and Body
sponsible for each intervention were not involved in bal- Mass Index);
ance assessment. Also, a blinded assessor (physiotherapist 2) the Modified Hoehn & Yahr Scale (HY) to assess the
and specialized in Parkinson disease) assessed the balance staging of the disease and impairment of individuals with
outcomes on the first day and the last day of intervention PD. Patients classified between stages 1.5 and 3 (mild to
(8 weeks after randomization) in a specific laboratory for moderate impairment) were selected for the study;22
postural control assessment. Due to the nature of the inter- 3) the Unified Parkinson´s Disease Rating Scale (UP-
ventions it was not possible to blind the individuals with
DRS), which assesses the progression of the disease
PD in regard to the two types of training in the study.
according to its clinical characteristics. Only domains
related to activities of daily living (part II) and the mo-
Procedures
tor exam (part III) were used;23

All procedures of study were performed with partici- 4) the Mini-Mental State Examination (MMSE),
pants in the “on” stage of medication. The first day of which is used to assess cognitive functions. The score
evaluation was for collecting: ranges from 0 to 30, and the cutoff point is 24.24

©
On day 2, the participants were with the experimen- tions. To avoid accumulate fatigue during the session
tal protocol of balance and with information related to in PD individuals; the exercises were performed with
training in each group (education about type of exercise, 2 sets of 10 repetitions for resistance gains. The load
practice, time, duration, pain or limitation, days to week intensity for start the training was placed between 1 to
and local). The training started in both groups after the 2 kg, depending on the single exercise (Appendix II).
balance assessment in the lab, respecting a maximum
time of one week. Balance outcomes
Interventions Primary outcome: force platform

Postural balance was assessed before and after in-
The intervention program consisted in two approach-
tervention by a trained physiotherapist. The postural
es: 1) balance approach with directed exercises for
balance assessment was performed on a force platform
postural control; and (2) resistance muscular training.
(BIOMEC 400, EMG system do Brasil, SP, Ltda). Sev-
Both approaches were performed by physiotherapists
en task conditions were performed and presented ran-
trained, in an adequate local (temperature, luminosity,
domly: 1) two-legged stand, representing bipedal, with
security) with equipment for exercises. The training in eyes open (EO); 2) Romberg, feet together, with EO;
each group lasted a 60-minute session, performed twice 3) Romberg with eyes closed (EC); 4) tandem, which
a week (2×), totaling 24 sessions (8 weeks). participant stands heel to toe, with EO; 5) tandem with
EC; 6) one-legged stand on the preferred leg indicated
BT group by the participant, with EO (Figure 2); and 7) tandem
double task with EO, which simple mathematical op-
The protocol of the BT group performed a program eration was performed by the participant concomitantly
based in postural control principles that integrated: bal- with balance performance. Bipedal condition was per-
ance per se, sensory integration, motor coordination, formed in 60 seconds, while for other tasks conditions
postural stability limits, mobility/agility, anticipatory a 30 second was executed. For each balance condition
and reactive postural adjustments, functional indepen- and to avoid residual fatigue from number of conditions,
dence, and gait. Therapy sessions were divided into only two trials were performed, with 30 seconds of rest
three stages: 1) therapy sessions 1 to 8; 2) therapy ses- between them, and the mean calculated for analysis.25, 26
sions 9 to 16; and 3) therapy sessions 17 to 24, which All participants were familiarized with the equip-
implied a progression of exercises in terms of complex- ment and protocol until they were comfortable with the
ity and challenging situations (unstable surface, use of testing. Balance assessment was performed with a stan-
balls, trampolines, most accelerations and fast neuromo- dardized protocol: barefoot with their arms at their sides
tor reaction responses, more complex coordination and or parallel to their trunk. During testing with eyes open
agility involving upper limbs, lower limbs and trunk in (EO), the participant would look at a target (a cross)
the same time, and gait circuits). This exercise training placed on a wall at eye level 2 m away. To prevent falls
program was registered in Appendix I. during testing, an investigator stood close to the volun-
teers during all tasks. For each balance condition, three
RT group (RT) trials of 30 s with 30-s rest intervals were performed and
the mean was retained for analysis.25, 26 A landmark on
The RT intervention program was based on muscu- the force platform was used to standardize the position
lar strengthening and stretching training including the of the feet during all balance conditions.
main muscle groups of the lower limbs and trunk. These The vertical ground reaction force data from the
muscle groups are always in action during balance and force platform were sampled at 100 Hz. All force sig-
gait activities. Again, therapy session was divided into nals were filtered with a 35-Hz low-pass second-order
three stages: 1) therapy sessions 1 to 8; 2) therapy ses- Butterworth filter. The signals from four sensors were
sions 9 to 16; and 3) therapy sessions 17 to 24, with a converted into COP data using computerized stabilog-
progressive increase in intensity and number of repeti- raphy, which was compiled with MATLAB routines

©
(MathWorks, Natick, MA). Stabilographic analysis of

COP data led to the computation of the main balance
parameter: the 95% confidence ellipse area of COP (A-
COP in cm2), amplitude of COP’s RMS (RMS in cm2),
and mean velocity (MV in cm/s) of COP oscillations
in both directions: Antero Posterior (AP) and Medial-
Lateral (ML).
Secondary outcome: Balance Evaluation Systems

Test
The Balance Evaluation Systems Test (BESTest) pro-
vides a clinical measurement of postural balance aiming
to assess the sub-systems involved in the control of bal-
ance and comprises 27 tasks. The test contains six sec-
tions corresponding to the balance sub-systems (sections):
1) biomechanical constraints;
2) stability limits;
3) transitions and anticipatory postural adjustments;
4) reactive postural responses;
5) sensory orientation;
6) stability in gait and total score.
It comprises a total of 36 items, each scoring from
zero (worst performance) to three (best performance),
totaling 108 points. The results are expressed in per-
centage.7
Figure 2.—Balance task condition: one-legged stand.
Statistical analysis
Descriptive data is expressed in mean and standard
deviation (SD) in according with the normal distri- Results
bution as verified by the Shapiro-Wilk test. The two
groups were compared using the Student-t test and pre- The characteristics of participants were presented
and post-interventions were compared using the paired- in the Table I, and both groups were homogeneous
samples t-test. The standardized mean differences (Δ) (P>0.05) with regard anthropometric and clinical vari-
from pre- and post-intervention values were also com- ables. The force platform balance results based in COP
puted for each dependent variable, and thus used as area sway are showed in the Table II. Significant im-
main variable on comparison between groups (BT vs. provement of postural control (pre vs. post 15.1 vs.
RT). 9.6 cm2) was only reported in favor of balance group
Finally, to determine the magnitude of changes post- (BT: large effect, d=1.17) for one-legged stand condi-
intervention, the effect size was calculated based on the tion (more challenging balance task). The standard-
values of Cohen’s d. The effect size is characterized ized mean differences (Δ) for this condition was sig-
as: small (d=0.0-0.20), medium (d=0.30-0.50), large nificantly (P<0.02) observed between the groups, being
(d=0.50-0.80).27 The statistical significance was set at BT=-5.5, representing 36% of improvement post-in-
P≤0.05 and all analyses were run in Statistical Package tervention (5.5/15.1=0.36), as compared to RT=-0.01,
for Social Sciences (SPSS) v.20. All statistics were per- with 0.07% only of improvement with mean difference
formed according to intention-to-treat analyses. 5.5 (95% CI: 1.1; 7.4). In addition, significant increase

©
of 48% in time-limit during one-legged stand condi- Table I.—Characteristics of participants.

tion was observed in favor of BT (pre 17.9±7.9 s, post Variables
RT group BT group
P values
26.5±6.4 s; P=0.007; Cohen’s d=1.08) compared to RT (N.=19) (N.=21)
(pre 15.7±9.5 s, post 13.1±7.9 s; P=0.06) that reduced Sex (M/F) 11/3 7/5 –
Age (years) 67.0±7.9 68.5±6.5 0.37
across intervention (16%). Weight (kg) 76.6±14.6 74.5±17.1 0.64
Again, significant improvement (P<0.05) was ob- Height (m) 1.68±0.07 1.64±0.07 0.76
served in favor of BT for balance gains in BESTest BMI (kg/m2) 26.9±5.2 27.4±5.8 0.42
scores (Table III). The positive results for this group H&Y 2.3±0.5 2.3±0.6 0.17
UPDRS ADL score 9.9±3.6 9.5±4.4 0.91
were found for the items of transitions/anticipatory UPDRS motor score 21.7±8.5 21.3±8.6 0.77
postural adjustment (Section III: pre vs. post 79.6 vs. UPDRS total score 31.7±11.3 30.9±12.4 0.95
84.9; medium effect, d=0.42), gait stability (Section VI: MMSE score 27.8±2.2 27.2±2.0 0.70
pre vs. post 75.9 vs. 82.5; medium effect, d=0.63) and Years diagnosed with PD 5.6±4.2 5.4±5.3 0.87
total score (pre vs. post 79.7 vs. 82.7; medium effect, Data presented as mean values±SD. No significant differences between groups
(P>0.05).
d=0.49). From standardized mean differences (Δ) be- RT: resistance training; BT: balance training; BMI: Body Mass Index; H&Y:
Modified Hoehn & Yahr Scale; UPDRS: Unified Parkinson’s Disease Rating
tween groups for these variables, significant (P<0.05) Scale; ADL: activities of daily living; MMSE: Mini-Mental State Examination.
superiority was showed for BT against RT in Section
III (3.9 vs. -1.1, mean difference -5.1 [95% CI: -10.7;
-0.45]), Section VI (5.6 vs. -3.9, mean difference -9.6
tance training for some balance variables investigated
[95% CI: -15.1; -3.9]), and total score (2.5 vs. -0.8,
in the study. In summary, 36% of improvement post-
mean difference -3.4 [95% CI: -6.3; -0.3]). In mean for
intervention was reported in favor of balance training
these items, 3.2% of improvement was reported for BT,
for COP sway during one-legged stand condition, while
while -0.98% across scores for RT.
only 0.07% for resistance training, supporting thus the
None the comparisons of the items concerning speed
specificity for a directional postural control interven-
(cm/s) and amplitude (cm2) of COP oscillations, mea-
tion than strength/endurance in PD individuals. These
sured before and after treatments presented significant
results were further supported by BESTest scores with
differences in the postures assessed for either group
regard to improvement of BT in transitions/anticipatory
(P>0.05 for all). postural adjustment, gait stability and total score of test.
No adverse events or side effects associated with the The results of present study are in agreement with
exercises programs were reported by BT and RT group. previous works.2, 16, 28 Furthermore, a recent review with
meta-analysis2 showed that moderate intensity progres-
Discussion
sive resistance training, 2-3/week over 8-10 weeks, can
The hypothesis of the present study was, at least, result in limited improvement of balance (0.36 only on
confirmed. Balance training was superior to resis- mean differences) in PD, which can be still task-depen-
Table II.—Force platform balance results based in COP area sway.

RT group BT group
A-COP (cm2) Mean diff. Mean diff.
Pre Post P value ES Pre Post P value ES
(95% CI) (95% CI)
Bipedal 3.2±3.0 3.2±3.5 0.99 -0.00 (-2.9; 2.8) 0.00 2.6±1.6 2.6±1.5 0.97 0.8 (-1.3; 3.0) 0.00
Romberg EO 5.8±3.5 5.7±4.5 0.77 -0.2 (-1.7; 1.2) -0.02 5.4±1.8 5.5±2.0 0.86 0.1 (-1.3; 1.5) 0.05
Romberg EC 8.9±4.9 9.2±6.5 0.74 0.1 (-2.3; 2.5) 0.06 6.0±2.3 5.7±1.8 0.58 0.3 (-0.7; 1.2) -0.13
Tandem EO 6.8±2.2 7.0±5.2 0.88 0.2 (-2.8; 3.2) 0.09 5.4±2.4 5.8±3.2 0.61 0.4 (-1.4; 2.2) 0.17
Tandem EC 12.2±5.5 14.6±10.6 0.26 2.3 (-2.0; 6.6) 0.43 9.6±5.5 7.3±2.6 0.22 -1.2 (-5.3; 2.9) -0.41
One-legged 14.1±4.5 14.0±5.5 0.98 -0.02 (-1.9; 1.9) -0.02 15.1±4.7 9.6±4.5 0.002* -5.5 (-6.9; -1.7) # -1.17
Double task 12.2±8.8 11.0±8.5 0.48 -1.0 (-4.1; 2.0) -0.13 8.7±4.4 7.6±4.6 0.12 -0.9 (-2.0; 0.3) -0.25
Data presented as mean±SD.
EO: eyes open; EC: eyes closed; Δ: standardized mean differences between pre- and post-intervention; ES: effect size computed only for significant difference between
pre- and post-intervention.
*Significant intragroup differences (P<0.05); # significant differences between groups (BT better than RT; P<0.02).

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Table III.—Functional balance results by BESTest assessment.

RT group BT group
Items Mean diff. Mean diff.
Pre Post P value ES Pre Post P value ES
(95% CI) (95% CI)
Section I (%) 69.9±22.6 70.7±22.5 0.82 0.7 (-6.2; 7.7) 0.03 71.8±20.0 71.9±20.7 0.99 0.1 (-4.2; 4.2) 0.00
Section II (%) 78.7±11.2 82.5±7.5 0.12 3.5 (-1.0; 8.2) 0.33 76.9±11.3 80.4±12.2 0.07 2.9 (-0.3; 6.2) 0.31
Section III (%) 79.9±13.2 78.7±11.5 0.57 -1.1 (-5.5; 3.1) -0.09 79.6±12.4 84.9±8.2 0.04* 3.9 (0.1; 7.8)# 0.42
Section IV (%) 85.8±17.9 84.5±18.7 0.55 -1.1 (-5.2; 2.8) -0.07 81.6±25.3 81.0±25.9 0.78 -0.5 (-4.5; 3.4) -0.02
Section V (%) 97.0±4.7 94.0±9.6 0.10 -2.8 (-6.2; 0.6) -0.63 98.1±3.1 97.7±3.2 0.57 -0.3 (-1.4; 0.8) -0.13
Section VI (%) 79.3±7.8 75.1±7.0 0.10 -3.9 (-8.8; 0.8) -0.53 75.9±10.4 82.5±6.1 0.002* 5.6 (2.4; 8.9) # 0.63
Total score (%) 81.6±7.8 80.7±7.0 0.48 -0.8 (-3.2; 1.5) -0.11 79.7±6.1 82.7±5.7 0.01* 2.5 (0.5; 4.5) # 0.49
Data presented as mean±SD.
Section I: Biomechanical constraints; Section II: Stability limits; Section III: Transitions and Anticipatory postural adjustments; Section IV: Reactive postural responses;
Section V: Sensory orientation; Section VI: Stability in gait; Δ: differences (post–pre); ES: effect size.
*Significant intragroup differences (P<0.05); # significant differences between groups (P<0.05) BT better than RT in Section III (3.9 vs. -1.1); Section VI (5.6 vs. -3.9),
total score (2.5 vs. -0.8).
dence because no effect was reported for some balance skills as balance. This can be explained by the ner-
variables such as balance confidence and others as gait vous system’s plastic capacity to respond in a more
and quality of life. dynamic and varied way to sensory and motor stimuli,
Wong-Yu et al.28 also reported in 68 individuals with varied experiences and learning from directional
with PD better results on BESTest scores for a specific exercises of postural control. Individuals with PD,
and more complete training related to postural re-edu- even with ideal medical treatment, still experience
cation, flexibility, balance training on the ground and progressive deterioration of their autonomy, which is
on uneven surfaces, in addition to gait training with largely related to non-dopaminergic symptoms such
double tasks, while the control group performed pos- as balance, posture, and gait. Thus, specific rehabili-
tural re-education, flexibility and strengthening exer- tation program as BT have been used to maximize
cises. These results are in agreement with our findings functional skills, improve quality of life and minimize
in favor of BT. secondary complications.36 Studies from animal mod-
Monticone et al. (2015),29 performing also balance els in PD, show evidences that exercises can stimulate
training based on activities with functional strategies events to the plasticity of the central nervous system
to balance and gait, reported better results on balance can include changes as neuronal growth, expression
and quality of life of PD patients in relation to group of neurotrophic factors, synaptogenesis and even neu-
that performed only general exercises of mobilization, rogenesis. Additionally, during the slow degeneration
stretching, and resistances. A similar study to present of nigrostriatal dopaminergic neurons, intense motor
work, reported positive improvement on balance con- sensory training seems to be associated with a modify-
fidence only for the directional postural control group ing action on the disease.37‑43
than for the resistance/strength training localized to As perspective, we assumed that rehabilitation pro-
lower limbs with use the machine.30 Apparently, re- grams for PD patients should not emphasize the im-
sistance training in PD is most efficient for muscular plementation of a series of isolated exercises (such as
strength and endurance gains of lower-limbs, hyper- the isolated training of muscle strength), but rather se-
trophy, and mobility than necessary with regard the quences of activities that involve various systems (cog-
balance problems associated to postural control sys- nitive, sensory, perceptual, motor, etc.) in increasing
tem of concern for the skills of PD individuals to per- skills levels to promote more lasting plastic phenom-
form daily activities.31‑35 ena with a beneficial functional impact so that patients
We believe thus that the balance training used in become able to transfer learning of these skills into
this study, that is, specific and task-driven protocol their daily routines. This contributes for functional in-
involving various sensory resources, is essential for dependence of individual with safety and to maintain
sensory-motor integration and is more easily managed or improve particular skills related to postural control
in the recovery of motor function and acquisition of into daily routines.

©
Limitations of ther study tems Test (BESTest) to Differentiate Balance Deficits. Phys Ther
2009;89:484-98.
8. Mancini, M, Horak FB. The relevance of clinical balance assess-
Some limitations of the study are related here. First, ment tools to differentiate balance deficits. Eur J Phys Rehabil Med
these results are generalized only for a specific group of 2010;46:239-48.
9. Visser JE, Carpenter MG, Kooij HVD, Bloem BR. The clinical utility of
PD with mild to moderate symptoms. We do not know posturography. Clin Neurophysiol 2008;119:2424-36.
whether the results apply to more advanced stages of 10. Snijders AH, Leunissen I, Bakker, M, Overeem S, Helmich RC, Bloem
BR, et al. Gait-related cerebral alterations in patients with Parkinson’s
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these individuals, considering the motor and cognitive 11. Zwergal A, la Fougère C, Lorenzl S, Rominger A, Xiong G, Deutschen-
symptoms of disease. Additionally, our losses, common baur L, et al. Postural imbalance and falls in PSP cor- relate with func-
tional pathology of the thalamus. Neurology 2011;77,101-9.
in studies involving human beings, could have led to a 12. Nardone A, Schieppati M. The role of instrumental assessment of bal-
type II error, although the present results indicate other- ance in clinical decision making. Eur J Phys Rehabil Med 2010;46:221-
37.
wise. Measures related to gait and quality of life should 13. Keus, SH, Bloem BR, Verbaan B, de Jonge PA, Hofman M, van Hilten
be included to verify whether these clinical improve- BJ, et al. Physiotherapy in Parkinson’s disease: utilisation and patient
satisfaction. J Neurol 2004;251:680-7.
ments of balance also are generalized for these other 14. Keus, SH, Bloem BR, Hendriks EJ, Bredero-Cohen AB, Munneke M.
variables. Finally, new randomized clinical trials that Evidence based analysis of physical therapy in Parkinson’s disease with
recommendations for practice and research. Mov Disord 2007;22:451-
assess the duration and frequency of therapy interven- 60.
tions necessary for beneficial effects and follow-up to 15. Yamashita FC, Saito TC, Almeida IA, Barboza NM, Santos SMS. Efe-
tividade da fisioterapia associada à musicoterapia na doença de Parkin-
verify how long the benefits arising from the interven- son. Revista ConScientiae Saúde 2012;11:677-84.
tion can last are needed to confirm the effects of physio- 16. Goodwin VA, Richards SH, Taylor RS, Taylor AH, Campbell JL. The
effectiveness of exercise interventions for people with Parkinson’s dis-
therapy on the balance of individuals with PD. ease: A systematic review and meta-analysis. Mov Dis 2008;23:631-40.
17. Howe TE, Rochester L, Jackson A, Banks PMH, Blair VA. Exercise for
improving balance in older people (Review). Cochrane Database Syst
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Conflicts of interest.—The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.
Article first published online: November 23, 2016. - Manuscript accepted: November 22, 2016. - Manuscript received: April 16, 2016.

©
Appendix I.—Intervention description balance training.

Therapy sessions 1 to 8 Therapy sessions 9 to 16 Therapy sessions 17 to 24
Objective: Balance training and sensory integration
Foam exercises Foam exercises Foam exercises
1. OE/CE Romberg wide/narrow base 1. Bilateral OE/CE tandem 1. Single-leg stance OE bilateral
2. Romberg associated with upper and lower 2. Tandem associated with upper and lower 2. Single-leg stance associated with upper and
limbs focusing on speed of movement, limbs exercises focusing on speed of lower limbs exercises focusing on the speed of
amplitude and postural transitions movement, amplitude, and postural movement, amplitude and postural transitions
3. Romberg with exercises varying weight shifts transitions 3. Single-leg stance associated with trunk
with step on lateral associating upper and 3. Tandem associated with trunk exercises exercises focusing on speed of movement,
lower limbs focusing on the speed of movement, amplitude and postural transitions
amplitude and postural transitions 4. Single-leg: slide a lower limb forward and
4. Tandem with exercises varying weight back and then make a circular movement
transference with step forward, side and rear bilaterally
associating upper and lower limbs movement
Objective: Balance training, agility and motor coordination
Exercises on a step bench Exercises on a step bench Exercises on a step bench
1. Step on the step bench changing the 1. Step on the step bench changing the 1. Step on the step bench changing the
movement sequences to stimulate movement sequences to stimulate motor movement sequences to stimulate motor
coordination, stability limits and postural coordination (more complex), stimulate coordination (even more complex),
adjustments stability and postural adjustments. Sequence stimulating stability limits and postural
of exercises using single-leg support and adjustments. Sequence of exercises using
sequence of exercises associated with upper single-leg support, maintenance of single-
limbs movement leg support in the sequences and sequence
of exercises associated with upper limbs
movement (more complex)
Objective: Balance training, stability limits, anticipatory and reactive adjustments
Trampoline Trampoline Trampoline
1. Exercise in Romberg position stimulating 1. Exercise in Tandem position stimulating 1. Exercise in single-leg stance changing the
side-to-side weight shifts anterior-posterior weight shifts position of the center of body gravity
2. Exercises in Romberg position stepping 2. Exercise in Romberg and Tandem positions 2. Exercises in the single-leg stance associating
forward, side and rear bilaterally associating trunk flexion, extension, upper limbs movement
3. Exercise in Romberg performing knew flexion and rotation and associated upper limbs 3. Introduction of short hops in Romberg
and extension to change the center of body movement
gravity 3. Introduction of short hops in Romberg
Objective: Balance training, stimulus to transitions of posture and functional independence
Ball Ball Ball
1. Facilitate transition of posture from sitting Same as before plus: Same as before plus:
on heels to kneeling and from knelling to 1. In semi-kneeling position, associating trunk 1. Exercise with patient sitting on a ball with
semi-kneeling, with and without trunk rotation rotation and upper limbs movement one-leg support elevating the other lower
holding a Bobath ball 2. In semi-kneeling position, facilitating limb, keeping the position for 10 seconds
2. In semi-kneeling position, facilitating trunk transition from semi-kneeling to standing
anterior displacement, pushing a Bobath ball
forward
Gait training with circuit 1 Gait training with com circuit 2 – increasing Gait training with com circuit 3 – increasing level
level of difficulty in comparison to 1 of difficulty in comparison to 1 and 2

©
Appendix II.—Intervention description of resistance training.

Therapy sessions 1 to 8 Therapy sessions 9 to 16 Therapy sessions 17 to 24
Objective: muscle strengthening and stretching
2 series of 10 repetitions of each exercise de- 2 series of 10 repetitions of each exercise de- 2 series of 10 repetitions of each exercise de-
scribed below with 1.0 kg dumbbell scribed with 1.5 kg dumbbell scribed with 2.0 kg dumbbell
Exercises performed in the supine position: Exercises performed in the supine position: Exercises performed in the supine position:
1. Lower limbs triple flexion on the trunk 1. Lower limbs triple flexion on the trunk 1. Lower limbs triple flexion on the trunk
2. Two-leg stance with lower limbs supported on 2. Two-leg stance with lower limbs supported 2. Two-leg stance with lower limbs supported
a ball on a ball on a ball
3. Two-leg stance with biceps strengthening 3. Two-leg stance with biceps strengthening 3. Two-leg stance with biceps strengthening
(elbow flexion) and pectoral strengthening (elbow flexion) and pectoral strengthening (elbow flexion) and pectoral strengthening
(shoulder abduction and adduction) with (shoulder abduction and adduction) with (shoulder abduction and adduction) with
lower limbs supported on a ball lower limbs supported on a ball lower limbs supported on a ball
4. Single-leg stance with lower limbs flexed on a 4. Single leg stance with lower limbs flexed on 4. Single leg stance with lower limbs flexed on
ball a ball a ball
5. Strengthening of upper limbs: triceps, biceps, 5. Strengthening of upper limbs: triceps, biceps, 5. Strengthening of upper limbs: triceps, biceps,
deltoid, and pectoral deltoid, and pectoral deltoid, and pectoral
6. Bilateral single-leg stance with lower limbs 6. Bilateral single leg stance with lower limbs 6. Bilateral single leg stance with lower limbs
supported on a ball supported on a ball supported on a ball
7. Strengthening of abdominal muscles (rectus 7. Strengthening of abdominal muscles (rectus 7. Strengthening of abdominal muscles (rectus
and oblique) and oblique) and oblique)
8. Strengthening of lower limbs: hip flexors, 8. Strengthening of lower limbs: hip flexors, 8. Strengthening of lower limbs: hip flexors,
knee extensors and dorsiflexors knee extensors and dorsiflexors knee extensors and dorsiflexors
Exercises performed in lateral decubitus position: Exercises performed in lateral decubitus posi- Exercises performed in lateral decubitus posi-
9. Strengthening of hip abductors and adductors tion: tion:
10. Triple flexion of lower limbs associated with 9. Strengthening of hip abductors and adductors 9. Strengthening of hip abductors and adductors
shoulder flexion and extension 10. Triple flexion of lower limbs associated with 10. Triple flexion of lower limbs associated with
11. Strengthening of shoulder muscles and girdle shoulder flexion and extension shoulder flexion and extension
Sitting on a chair: 11. Strengthening of shoulder muscles and girdle 11. Strengthening of shoulder muscles and girdle
12. Strengthening hip flexors and knee extensors Sitting on a chair: Sitting on a chair:
13. Anterior trunk flexion, back strengthening 12. Strengthening hip flexors and knee extensors 12. Strengthening hip flexors and knee extensors
14. Transition from sitting to standing associating 13. Anterior trunk flexion, back strengthening 13. Anterior trunk flexion, back strengthening
elbow and shoulder flexion 14. Transition from sitting to standing associating 14. Transition from sitting to standing associating
Standing: elbow and shoulder flexion elbow and shoulder flexion
15. Strengthening of knee flexors and upper limbs Standing: Standing:
supported on chair 15. Strengthening of knee flexors and upper 15. Strengthening of knee flexors and upper
16. Strengthening calf with plantar flexion and limbs supported on chair limbs supported on chair
upper limbs supported on chair 16. Strengthening calf with plantar flexion and 16. Strengthening calf with plantar flexion and
upper limbs supported on chair upper limbs supported on chair

Balance Versus Resistance Training On Postural Control in Patients With Parkinsons Disease

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Balance Versus Resistance Training On Postural Control in Patients With Parkinsons Disease

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Balance versus resistance training on

P arkinson’s disease (PD) presents a combination of

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 173

174 European Journal of Physical and Rehabilitation Medicine April 2017

tor exam (part III) were used;23

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 175

Interventions Primary outcome: force platform

176 European Journal of Physical and Rehabilitation Medicine April 2017

(MathWorks, Natick, MA). Stabilographic analysis of

Secondary outcome: Balance Evaluation Systems

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 177

of 48% in time-limit during one-legged stand condi- Table I.—Characteristics of participants.

Table II.—Force platform balance results based in COP area sway.

178 European Journal of Physical and Rehabilitation Medicine April 2017

Table III.—Functional balance results by BESTest assessment.

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 179

180 European Journal of Physical and Rehabilitation Medicine April 2017

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 181

Appendix I.—Intervention description balance training.

182 European Journal of Physical and Rehabilitation Medicine April 2017

Appendix II.—Intervention description of resistance training.

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 183

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