Effect of different modes of therapy on vestibular and balance dysfunction in Parkinson’s disease

ORIGINAL ARTICLE

Effect of different modes of therapy on vestibular

and balance dysfunction in Parkinson’s disease

Wafaa Abdel-Hay El-Kholy a, Hesham Mohamed Taha a,*,

Soha Mohamed Hamada b, Mona Abdel-Fattah Sayed b

a Audiology Unit, Otorhinolaryngology Dept., Ain Shams University, Cairo, Egyptb Audiology Department, Hearing & Speech Institute, Giza, Egypt

Received 26 September 2014; accepted 15 February 2015

KEYWORDS

Parkinson’s disease;

Vestibular and balance

dysfunction;

Medical treatment;

Physiotherapy

Abstract Background: Patients with Parkinson’s disease (PD) have difficulties in performing vari-

ous motor tasks such as walking, writing and speaking, together with significant balance dysfunc-

tion. Despite gains made in the field of pharmacotherapy and deep brain stimulation, dopaminergic

medications may produce a limited improvement in postural stability. Sustained improvement in

motor skills can be achieved through physiotherapy.

Aim of the work: To measure the effect of different modes of therapy in controlling vestibular

and/or balance dysfunction in patients with PD.

Methodology: This study was conducted on 20 patients suffering from definite PD, subdivided

into two subgroups according to the mode of therapy they followed. Subgroup I received medical

treatment and physiotherapy, while subgroup II received medical treatment only. The control group

consisted of 10 age- and sex-matched normal subjects. All participants were evaluated using video-

nystagmography (VNG), Computerized Dynamic Posturography (CDP) including sensory impair-

ment, automatic motor and voluntary motor assessment. In addition, patients were evaluated using

functional limitation tests and were asked to fill the Freezing of Gait (FOG) questionnaire.

Results: This research documents vestibular as well as balance dysfunction in patients with PD.

Central vestibular disorders were more common than peripheral ones. The most prevalent balance

abnormality was encountered in the sensory organization subtest, though patients showed signifi-

cant affection in other domains; namely, autonomic motor, voluntary motor and functional

limitation. In general, patients receiving both medication and physiotherapy showed better vestibu-

lar and balance function than those receiving medication only, and approached the normal values in

many test parameters.

Conclusions: Since patients with PD receiving physiotherapy in conjunction with medical treat-

ment showed better control of their vestibular and balance functions, efforts should be directed to

* Corresponding author at: 12 Bagdad Street, Cairo, Egypt. Mobile:

+20 1227431717.

E-mail address: [email protected] (H.M. Taha).

Peer review under responsibility of Egyptian Society of Ear, Nose,

Throat and Allied Sciences.

Egyptian Journal of Ear, Nose, Throat and Allied Sciences (2015) xxx, xxx–xxx

HO ST E D BY

Egyptian Society of Ear, Nose, Throat and Allied Sciences

Egyptian Journal of Ear, Nose, Throat and Allied

Sciences

www.ejentas.com

http://dx.doi.org/10.1016/j.ejenta.2015.02.0052090-0740 ª 2015 Hosting by Elsevier B.V. on behalf of Egyptian Society of Ear, Nose, Throat and Allied Sciences.

Please cite this article in press as: El-Kholy WA-H et al. Effect of different modes of therapy on vestibular and balance dysfunction in Parkinson’s disease. Egypt J EarNose Throat Allied Sci (2015), http://dx.doi.org/10.1016/j.ejenta.2015.02.005

mailto:[email protected]

http://dx.doi.org/10.1016/j.ejenta.2015.02.005


http://www.sciencedirect.com/science/journal/20900740



start physiotherapy including vestibular rehabilitation as early as possible in order to improve bal-

ance, thus increasing independence in daily life activities.

ª 2015 Hosting by Elsevier B.V. on behalf of Egyptian Society of Ear, Nose, Throat and Allied Sciences.

1. Introduction and rationale

Parkinson’s disease (PD) is a neuro-degenerative disorder

characterized by cardinal features including resting tremors,

rigidity, bradykinesia, and postural difficulties which arise pri-

marily from the loss of dopamine producing neurons and sub-

sequent dysfunction of the basal ganglia–thalamo–cortical

pathway.24 Furthermore, PD leads to abnormalities in two

main components of postural control: orientation (maintain-

ing a normal postural arrangement and alignment) and

stabilization (maintaining equilibrium).44

The pathologic hallmark of PD is degeneration of dopami-

nergic neurons in the substantia nigra pars compacta (SNc),

resulting in the depletion of striatal dopamine.28 This

neurotransmitter regulates excitatory and inhibitory outflow

of the basal ganglia.38 Functional neuro-imaging modalities

such as fMRI, MRS, and DTI have been applied to document

functional deficits in PD. Neuro-imaging is undergoing a shift

from morphological to functional imaging as new technologies

are introduced and technical problems associated with the

local production of radio-isotopes are solved.47

Postural instability (PI) is a disabling disorder, which is

associated with sudden falls, progressive loss of independence

and immobility.16 It usually occurs at the later stages of the

disease and, unlike gait disorders, responds poorly to med-

ication. Marked alteration of gait is common in advanced

PD, although there is evidence suggesting that initial impair-

ment in gait can be detected even early in the course of the dis-

ease.1 Falls occur despite maximal treatment with levodopa,

confirming that axial disability in late stage PD is largely

dopa-resistant (likely due to extranigral and non-dopaminergic

brain lesions). Falls often have dramatic consequences, such as

traumas and fractures. The high risk of fractures was demon-

strated in a large case control study.45

To date, management concepts in PD are still diverse.

Despite gains made in the field of pharmacotherapy and deep

brain stimulation, dopaminergic medications may produce a

limited improvement in PI.4,46 Thus, physiotherapy is the most

commonly used procedure as an adjunct to drug therapy to

treat PD movement disorders.9 Accordingly this study was

designed to measure the effect of different modes of therapy

in controlling vestibular and/or balance dysfunction in patients

with PD.

2. Methodology

2.1. Subjects

The study group consisted of 20 patients with PD diagnosed

by an expert neurologist. Their age ranged from 40 to 60 years

with a mean age of 50.6 years (SD = 4.2 years). They were in

stages I, 2 and 3 according to Hoehm and Yarr staging scale.12

The study group was divided into 2 subgroups according to the

management they received. Patients who were receiving

medical treatment and physiotherapy were assigned to

Subgroup I (n= 8), while Subgroup II patients were receiving

medical treatment only (n = 12). Medical treatment was in the

form of Sinemet (levodopa) twice daily given orally as this is

the mostly utilized drug in this condition, physiotherapy was

twice daily which ranged from 2 to 9 years with a mean of

3.8 years (SD = 3.6 years).

Patients showing history, symptoms and/or signs of the

following were excluded: Otological disease, neurological

disease (other than PD), systemic disease such as long stand-

ing diabetes and hypertension (more than five years dura-

tion), head trauma and ototoxic drug intake. Patients who

were at stages IV and V of the disease were excluded

because of their severe disability which prevented them from

performing the tests. Also, patients complaining of visual

troubles like cataract or severe errors of refraction were

excluded.

The control group consisted of 10 normal age- and gender-

matched subjects with no symptoms and/or signs of otologic,

vestibular or neurologic disease or any disease affecting

vestibular and balance systems.

2.2. Method

All participants in this study were subjected to the following:

(1) Full history taking, otological and neuro-otological

examination.

(2) Freezing of gait (FOG) questionnaire (for PD patients

only). This detailed gait and falls questionnaire consists

of 6 items that assess gait in daily living, frequency and

severity of FOG, frequency of festinating gait and its

relation to falls, and finally frequency and severity of

falls. Responses to each item are on 5-point scales where

a score of 0 indicates absence of the symptom; while 4

indicates the most severe stage.14 All items were literally

translated to the Arabic language.

(3) Vestibular Assessment (VNG test) using I.C.S Computerized

infrared 4 Channel Video-nystagmography (version 5.1)

and the target being projected by an LCD projector on a

screen about 1.5 meters in front of the subject. VNG

included testing for spontaneous nystagmus, oculomo-

tor, Dix-Hallpike, positional and caloric tests.

(4) Balance Assessment (CDP test results) using Computerized

Dynamic Posturography long forceplate (Neurocom ver-

sion 4 Smart Balance Master). This included the following:

i. Sensory Impairment Assessment – Sensory Organization

Test (SOT): Patients were asked to maintain standing

balance during a combination of three visual and two

support surface conditions. Tasks were performed with

the eyes open and with the eyes closed.32 Participants

were asked to stand quietly and steadily for 3 trials in

each of the 6 conditions.

ii. Automatic Motor Assessment

2 W.A.-H. El-Kholy et al.



– Motor Control Test (MCT): Sequences of small,

medium and large platform translations in forward

and backward directions were used to elicit auto-

matic postural responses. The following parameters

were measured and compared to the default norms

of the equipment: latency, weight symmetry,

strength symmetry and amplitude scaling.36

– Adaptation Test (ADT): Adaptation was assessed

by determining the ability to suppress inappropri-

ate responses to the external disturbance.

Response time was measured to slow toes up

and toes down rotations at 8 degrees/s.21

iii. Voluntary Motor Assessment:

– Limit Of Stability (LOS): The subject was asked

to lean as quickly and accurately as possible

toward a target and to hold steady. The following

measures were recorded: Reaction time, mean

velocity level, directional control level and end-

point excursion percent.33

– Rhythmic Weight Shift (RWS): The subject is

asked to follow an on-screen cue as it moved

between the endpoints, from left to right (lateral)

and from forward to backward (anterior/pos-

terior) between 2 targets at three distinct speeds:

slow, medium, and fast.31

(5) Functional Limitation Tests

i. Tandem walk (TW): Subjects were required to walk

heel to toe along a 10-foot line. They were asked to

walk as quickly as they could without errors. The

performance time of three trials for performance of

each task was averaged for analyses.7

ii. Sit to stand (S-T-S): Subjects were asked to perform

this maneuver 3 times. The following parameters

were measured: weight transfer, rising index and

weight symmetry.26

2.3. Statistical analysis

Data were expressed as mean and standard deviation for

quantitative parametric measures and as median percentiles

for quantitative non-parametric data. Comparison between

two independent groups was done using Student ‘‘t’’ test and

Wilcoxon Rank Sum test for parametric and non-parametric

data respectively. For more than 2 groups, an ANOVA test

was followed by Post-hoc, LSD was used for parametric data

and Kruskall–Wallis test was used for non-parametric data.

Chi-square was used to compare categorical qualitative data.

The probability of error at 0.05 was considered significant.

3. Results

In the study group, the mean age of subjects was 49.1 years

(±4.1) in subgroup I and 51 years (±3.5) in subgroup 2, with

4:1 male-to-female ratio. The mean disease duration was

3.95 years (±2.14) and 4.15 years (±2.65) in subgroups I

and II respectively. Most patients were in stage II of PD dis-

ease (Fig. 1). There were no statistically significant differences

between the 2 study subgroups as regards age (p= 0.179),

gender (p = 0.914), duration of the disease (0.231) and disease

staging (p= 0.912). Moreover, FOG questionnaire scores did

not differ significantly (Table 1). In general, all vestibular and

balance function assessment tests showed better test scores in

subgroup I compared to subgroup II.

3.1. Vestibular assessment

The most affected group of tests in VNG was oculomotor sub-

tests reflecting central vestibular pattern of dysfunction (58.5%

in subgroup I and 50% in subgroup II – Table 2). Table 3

shows the number and percentage of VNG oculomotor test

abnormalities. As shown, the most affected oculomotor

subtests were OPK and smooth pursuit subtests. Subgroup II

consistently showed higher rates of abnormalities. Two

patients in Subgroup I (25%) and 4 patients in subgroup II

(33.3%) showed failure of fixation suppression which is con-

sidered a central vestibular finding. On the other hand, periph-

eral vestibular dysfunction was present in 41.7% in Subgroup

II and 12.5% in subgroup I. Abnormality was in the form of

posterior canal BPPV canalithiasis in 3 patients and unilateral

caloric weakness in another 3 patients. Neither spontaneous

nor positional nystagmus was recorded in any patient.

3.2. Balance assessment

Table 4 shows abnormalities encountered in balance assess-

ment. Similar to vestibular assessment, the percentage of

abnormalities was higher in Subgroup II. The most affected

test was CDP-SOT test (62.5% in Subgroup I and 100% in

Subgroup II), followed by CDP-LOS and TW tests.

0

1

2

3

4

5

6

Subgroup I Subgroup II

stage (1)

stage (2)

stage (3)

Figure 1 Number of patients belonging to the 3 disease stages in

subgroups I and II. Most patients were in stage (2).

Table 1 Comparison between PD subgroups in freezing of

gait (FOG) questionnaire using Kruskall–Wallis Test.

FOG score Subgroup I Subgroup II

Median 7.4 8.5

Percentile 2.00–14.6 2.75–16.00

F value 2.22

P value 0.612

Insignificant statistical difference between 2 subgroups.

Effects of therapy on vestibular and balance dysfunction 3



Subgroup I scores did not differ significantly from those of the

control group in the composite score as well as in conditions

C1 to C3 (Table 5). Subgroup II scores differed significantly

from those of the control group in all the SOT parameters.

Also, they differed significantly from those of subgroup I

except in C1 and C6 conditions.

As regards Autonomic Motor Assessment tests (MCT and

ADT), Subgroup I scores did not differ significantly from

those of the control group in all parameters (Tables 6 and

7). On the other hand, Subgroup II scores differed significantly

from those of the control group in all Balance Assessment tests

(p < 0.01 in most of the tests)(Tables 6–9). As regards com-

parison between the 2 subgroups, difference was significant

in all Autonomic Motor Assessment test parameters and only

some of the Voluntary Motor Assessment test parameters.

3.3. Functional limitation tests

Significant difference was recorded between the control group

and Subgroup II at high levels of significance (p < 0.01).

Subgroup I differed significantly from the control group and

Subgroup II in some of the parameters.

4. Discussion

The present study was conducted on 20 patients suffering from

Parkinson’s disease (PD). In order to measure the effect of

therapy in controlling vestibular and/or balance dysfunction,

the study group was subdivided into two subgroups.

Subgroup (I) received medical treatment and physiotherapy,

while subgroup (II) received medical treatment only. Table 1

shows the Freezing of gait questionnaire (FOG) scores in PD

patients and a comparison between the two subgroups. As

shown, subgroup II had higher median and percentile scores

when compared to subgroup I; however, this difference was

not statistically significant. This could be explained by the fact

that staging of the disease in both subgroups was not signifi-

cantly different from each other (Fig. 1) and agrees with

Giladi et al.15 who emphasized the relationship between stag-

ing of the disease and FOG scores.

4.1. Vestibular assessment

In the present study, 3 out of 8 patients belonging to subgroup

I, who received both medication and physiotherapy, had nor-

mal VNG test results (37.5% – Table 2). In affected patients,

those receiving medical treatment only (Subgroup II) showed

higher rates of affection. Also, central vestibular dysfunction

was more frequent than peripheral dysfunction in all patients.

This vestibular disturbance is assumed to be due to dysfunc-

tion of the nigro–striato–collicular tracts as reported by

Henzi et al.20 Conversely, Mota et al.29 denied the prevalence

of central vestibular syndromes in their population. This dif-

ference could be attributed to the different staging of the dis-

ease since we included disease stages I–III. They explained

the peripheral dysfunction on the basis of orthostatic hypoten-

sion either due to medication or 2 year to the disease itself. It is

assumed that central vestibular dysfunction is due to degenera-

tion in nigro–straito–cortical tracts.

A close observation of the VNG oculomotor test results

shows that about 55% of PD patients had reduced gain in

smooth pursuit test (average of all frequencies) and OPK

asymmetry (Table 3). These results were in agreement with

Gushikem17 It is worth noting that smooth pursuit gain deficits

Table 2 Number and percentage of affection based on VNG test results in the study subgroups.

Normal Central Peripheral Combined

No. % No. % No. % No. %

Subgroup I 3 37.5 4 50 1 12.5 – –

Subgroup II – – 7 58.3 5 41.7 – –

Central vestibular dysfunction was the most frequent disorder.

Table 3 Number and percentage of patients showing oculomotor subtests abnormalities.

Oculomotor subtest Subgroup I (n= 8) Subgroup II (n = 12)

No. % No. %

1-Gaze 1 12.5 3 25

Horizontal 1 12.5 2 16.7

Vertical – – 1 8.3

2-Smooth pursuit 4 50 7 58.3

Gain 0.1 Hz 1 12.5 3 25

Gain 0.2 Hz 3 37.5 4 33.3

Gain 0.4 Hz 4 50 6 50

Gain pattern (saccadic pursuit) – – 3 25

3-Saccade 3 37.5 6 50

Peak velocity 2 25 2 16.7

Latency 3 37.5 5 41.7

Accuracy 2 25 3 25

4-OPK symmetry 4 50 7 58.3




increased in more challenging tasks; appear to be more

affected in 0.4 Hz compared to 0.1 and 0.2 Hz frequencies in

the 2 study subgroups (Table 3). This is expected and agrees

with that of Hain et al.19 who stated that as the frequency or

acceleration of head movements increases (>1–2 Hz,

>2000 deg/s2), the efficacy of tracking of eye movement

decreases.

In both study subgroups, there is a general agreement in the

percentage of abnormalities in smooth pursuit and OPK tests

(Table 3), which agrees with that of Krauzlis.25 The pursuit

system is chiefly responsible for generating slow phases of

optokinetic nystagmus (OKN), which limit full-field motion

of the visual environment upon the retina during head move-

ment. In addition, much of the neural machinery of the pursuit

Table 5 Comparison between the control group and the study subgroups as regards SOT test scores.

Equilibrium-E (deg/s)

Strategy-S (deg)

Control group (n= 10) Subgroup I (n= 8) Subgroup II (n = 12) ANOVA test

F value P valueX (SD) X (SD) X (SD)

C 1 E 93.0 (2.3)a 90.9 (1.8)a 89.1 (3.9)a 2.4 0.118

S 99.0 (0.4)a 98.7 (1.7)a 94.0 (3.3)a 4.0 0.118

C 2 E 92.0 (1.4)a 90.1 (1.2)a 79.5 (6.0)b 5.4 0.023

S 97.0 (0.7)a 96.0 (0.9)a 83.5 (5.6)b 6.1 0.042

C 3 E 93.0 (2.3)a 87.3 (6.9)a 73.4 (10.2)b 6.3 0.025

S 98.0 (1.7)a 97.0 (1.3)a 85.0 (6.0)b 5.0 0.01

C 4 E 86.1 (5.5)a 80.4 (5.6)a 69.5 (14.3)b 7.2 0.003

S 83.2 (4.8)a 74.3 (3.6)b 66.8 (10.3)c 7.0 0.001

C 5 E 85.2 (9.7)a 75.3 (6.8)b 60.9 (16.1)c 16.3 0.002

S 77.6 (10.6)a 75.0 (4.7)a 57.5 (12.9)b 8.3 0.0

C 6 E 80.0 (10.2)a 70.4 (10.8)b 52.0 (18.5)b 22.4 0.0

S 76.5 (11.4)a 70.7 (11.7)b 56.0 (15.5)b 12.7 0.0

Significant difference between the control group and the study subgroups in condition (C2 and C3), highly significant difference in conditions

(C4–C6) and in the composite scores.

Table 6 Comparison between the control group and the study subgroups as regards MCT test parameters.

MCT Control group Subgroup I Subgroup II ANOVA test

X (SD) X (SD) X (SD) F value P value

Weight symmetry forward 98 (6.8)a 100 (8.8)a 125.7 (30.2)b 4.9 0.015

Weight symmetry backward 95.3 (7.6)a 98.5 (11.6)a 129 (24.7)b 11.04 0.00

Latency forward 140 (13)a 132.7 (22)a 162.5 (22.08)b 4.2 0.002

Latency backward 163 (10.6)a 147.4 (23.8)a 152.5 (17.7)a 2.3 0.117

Strength symmetry forward 115.3 (8.6)a 119 (22.06)a 122 (20.6)a 2.6 0.092

Kruskall–Wallis test

Median Median Median H value P value

Strength symmetry backward 96a 110a 124b 7.5 0.023

Amplitude forward 4.0a 3.7a 4.5a 0.2 0.89

Amplitude backward 4 3 5.15 0.28 0.23

Medians with different letters are significantly different from each other. Highly significant difference between the control group and the study

subgroups in weight symmetry backward and latency forward and significant statistical difference in Weight symmetry forward, and Strength

symmetry backward.

Table 4 Number and percentage of patients showing Computerized Dynamic Posturography and Functional Limitation tests

abnormalities in the study subgroups.

Test Subgroup I (n= 8) Subgroup II (n= 12)

No. % No. %

CDP (Sensory impairment assessment) SOT 5 62.5 12 100

CDP (Automatic motor assessment) MCT 2 25 6 50

ADT 2 25 5 33.3

CDP (Voluntary motor assessment) RWS 3 37.5 6 50

LOS 5 62.5 8 66.7

Functional limitation tests TW 2 25 9 75

S-T-S 2 25 6 50




system contributes to the suppression or enhancement of the

VOR by visual inputs. Thus, dysfunction of smooth pursuit,

OKN slow phases, and visual modulation of the VOR nearly

always parallel each other. In our study, six patients showed

failure of fixation suppression in caloric test (30%).

As regards the pattern of abnormality, 3 patients showed

cog-wheel appearance in smooth pursuit test (Table 3). A

similar pattern was reported by Campbell et al.6 They reported

that saccades are commonly used instead of smooth pur-

suits when following an object in PD being a basal ganglia

disease.

About 45% of PD patients showed saccade test abnormal-

ity; delayed latency being the most prevalent abnormality

(Table 3). These results agree with those of Jankovic23 who

reported prolonged saccade latency and hypometric saccades

in patients with PD. On the other hand, some authors reported

normal values.8,41 Others such as13 studied only mildly affected

patients. White et al.48 reported that L-DOPA had no effect on

the peak velocity performance index and suggested that

differences in anti-parkinsonian treatment do not account for

the discrepancies between reports. Differences in the severity

of the disease could provide an explanation.

When comparing the different oculomotor subtest results,

both smooth pursuit and OPK showed higher rates of affec-

tion compared to saccades. This agrees with that of Sparks39

and is based on the different pathways responsible for both

eye movements. The standard descending pathways for sac-

cades likewise contain cortico–ponto–cerebellar connections.

These include direct projections from cortical eye fields to

eye-movement-related structures in the brainstem such as the

superior colliculus (SC) and premotor including nuclei in the

reticular formation (PMN), and also pathways through the

basal ganglia, including the caudate nucleus (CN) and the sub-

stantia nigra pars reticulata (SNr). Thus, these pathways

include some degree of direct cortical control over the motor

output. On the other hand, the standard pathways for pursuit

simply link visual sensory areas to the cerebellum, consistent

with pursuit’s presumed role as a visuomotor reflex.

Table 7 Comparison between the control group and the study subgroups as regards ADT test parameters.

ADT Control group Subgroup I Subgroup II ANOVA test

X (SD) X (SD) X (SD) F value P value

Toes up 48.3 (6.9)a 53.9 (8.3)a 86.9 (21.4)b 7.5 0.000


Toes down Median Median Median H value P value

31.2a 32.7a 49.7b 16.4 0.000

Medians with different letters are significantly different from each other. Highly significant statistical differences between the study subgroups and

the control group in toes up and toes down tests.

Table 8 Comparison between the control group and the study subgroups as regards RWS test parameters.

RWS Control group Subgroup1 Subgroup2 ANOVA test


LT–RT velocity (deg/s) 4.9a 3.8ab 2.0b 11.7 0.003

Front–back velocity

(deg/s) 3.3a 2.4ab 1.1b 13.0 0.001

Front–back DCL (%) 81ab 68.5a 53b 16.3 0


LT–RT DCL (%) X (SD) X (SD) X (SD) F value P value

85.2 (1.9)a 83.2 (4.02)a 65.3 (9.6)b 30.0 0.00

Medians with different letters are significantly different from each other. Highly significant statistical differences between 2 groups in all RWS test

parameters.

Table 9 Comparison between the control group and the study subgroups as regards LOS test parameters.

LOS Control group Subgroup I Subgroup II Kruskall–Wallis test


Reaction time (sec) 0.66a 0.9b 1.55b 14.6 0.001

Mean velocity level (deg/s) 4.6a 3.0b 1.5b 15.3 0.00

Directional control level (%) 69.5a 72.0a 42.0b 17.65 0.00

(End point excursion – Maximum excursion end) (%) 71.0a 68.7b 48.5c 20.54 0.00

Medians with different letters are significantly different from each other. Highly significant statistical differences between the study subgroups and

the control group in all LOS parameters.




Six out of 20 patients had peripheral vestibular disorder in

the form of BPPV (3 patients–15%) and unilateral caloric

weakness (3 patients–15%). Bloem3 reported a lower percent-

age for BPPV in their PD group (8%). Caloric weakness was

also reported by Silveira et al.37 who stated that the reduction

in the response to the caloric tests was perceived as one of the

modifications of the vestibular system in relation to the PD

process. Several studies mention the loss of ciliated cells of

the ampullary crests and the maculae, decline in the number

of neurons of the vestibular ganglion, degeneration of the oto-

conia, decrease in the labyrinthine blood flow, progressive

depression of neural stability, reduction in the compensation

capacity of the vestibulo–ocular and vestibulospinal reflexes,

which contribute to a decrease in the speed of pursuit move-

ments and to rotational and caloric hypoactivity of the

vestibular system, at both the peripheral and central levels in

those patients37 However, no studies set explanation for the

unilateral affection encountered in our patients.

4.2. Balance assessment

Using the CDP equipment, PD patients were assessed in 4

main domains: Sensory impairment, automatic motor, volun-

tary motor and functional limitation. Though a considerable

number of patients from both subgroups showed abnormal

results in many of these tests, a consistently higher prevalence

of abnormalities was encountered in Subgroup II compared to

Subgroup I.

The highest percentage of affection was in the sensory

impairment SOT test (62.5% in subgroup I and 100% in sub-

group II – Table 4). As previously reported by many authors,

organization protocols are useful for the assessment of pos-

tural control under various sensory conditions and generally

accepted as a reliable paradigm of measuring the capacity of

the central nervous system to prioritize and reintegrate sensory

information.32,43 Tagliabue et al.40 reported that these patients

showed a breakdown in the temporal coordination between

postural adjustments and arm reaching during whole body

reaching to a target when closing their eyes. Abnormal pos-

tural coordination when vision was obscured is consistent with

impaired proprioceptive mapping compensated by the use of

vision. PD patients in our study showed a significant shift from

normative values in all conditions except C1 as well as the

composite score (Table 5). This is consistent with a combined

vestibular insult and propioceptive defect. It also points to the

fact that PD patients showed more difficulty in controlling

their balance in more complex sensory conflict situations com-

pared to the control group.

As regards automatic motor assessment MCT test, a signifi-

cant difference between the groups was recorded in forward

latency, weight strength and backward strength symmetry

(Table 6). Inkster and Eng22 reported that strength is a key

component to overall health and has been documented as defi-

cient in individuals with PD.30 This vital aspect of health is

important for integrity of both tendons and muscles, which

may be related to prolonged latency scores, falls and other

associated risk of injuries.31

Strength symmetry test showed significant difference

between the control group and subgroup II, but there was

no significant difference between the control group and sub-

group I (Table 6). In other words, patients who received

additional physiotherapy approximated performance of nor-

mal subjects in their age. Many studies reported that a

decrease in postural stability is commonly observed in levo-

dopa medicated PD patients in contrast to physiotherapy

due to decreased proprioceptive sensitivity.34,2 Thus, strategies

for enhancing balance among older adults with PD are needed,

because in the absence of regular physical activity, balance and

muscle strength deteriorate.

Similar to MCT, Adaptation (ADT) test scores, toes up and

toes down, differed significantly in subgroup II compared to

the control group (Table 7). Performance on the ADT requires

adequate ankle range of motion and muscle strength as well as

effective motor adaptation which is absent in PD. Results

agree with those of Fisher10 who reported that during the first

(unexpected) trials, the initial disruptive responses are cor-

rected by secondary responses in the opposing muscles. With

each subsequent trial, initial reactions are attenuated and sec-

ondary responses strengthened to reduce overall sway.

As regards voluntary motor assessment, both Rhythmic

Weight Shift (RWS) and Limits of Stability (LOS) were

affected, with variability among the parameters measured

(Tables 8 and 9). Rhythmic weight shift test is used to evaluate

the participants’ voluntary ability to move the COG in an

intended direction at different velocities. This agrees with that

of Mazzoni et al.27 who reported that PD patients had strik-

ingly worse directional control compared to the other healthy

elder and more so in the anterior-posterior than in the medio-

lateral direction.

As stated by Franchignomi et al.,11 the slower and smaller

LOS of patients with PD may be related to the perceived diffi-

culty of moving their COG toward the targets. In the present

study, patients belonging to subgroup I showed better LOS

test results than those in subgroup II. This result is in agree-

ment with that of Qutubuddin et al.35 who reported that

patients who had received physiotherapy showed significant

changes in reaction time, movement velocity and endpoint

excursion than other PD groups who received levodopa as a

life time therapy.

Finally, an analysis was done to evaluate the performance

of PD patients on functional limitation tests. Only one forth

of patients in subgroup I showed abnormal scores in this group

of tests, whereas three-quarters and one half of the patients in

subgroup II scored abnormally on Tandem Walk (TW) and

Sit-to-Stand (S-T-S) tests respectively (Tables 10 and 11).

Stated differently, three-quarters of patients who received

additional physiotherapy could successfully perform these

functional tests and, therefore, may be more immune to the

risk of falls. Patients with PD scores significantly lower when

compared to the control group in most of the functional lim-

itation assessment parameters (Tables 10 and 11). Our results

agree with those of Haas et al.18 who reported that tandem

walk is one of the greatest difficulties experienced in individu-

als with PD in overall mobility and gait. This is especially

apparent as the disease progresses increasing the risk of falling

and decreasing overall mobility.

Similarly, rising from a chair is a physically demanding

function that is a common problem in aging, particularly in

individual with PD. Brod et al.5 found that 81% of individuals

with PD self-reported having difficulty standing from a seated

position. Individuals must have adequate lower body strength

and exhibit the ability to control their center of gravity as it

shifts from an initial position over the seat to a location




centered over the base of support (feet). This explains the sig-

nificant difference between patients with PD and controls in

measures of weight symmetry and weight transfer (Table 11).

4.3. Effect of additional physiotherapy

In almost all tests of vestibular and balance assessment con-

ducted in this study, patients who received physiotherapy out-

stood their counterparts who did not receive such intervention.

It should be emphasized that, in some tests, their performance

approximated that of normal subjects in their age. They also

had much lower prevalence of functional limitations which

advantageously decrease the risk of falls and improve their

general ambulation and balance.

It can be argued that the difference in performance is

mainly due to the applied management protocols rather than

other factors such as age and gender distribution, duration

and staging of the disease since all were not significantly differ-

ent between the two study subgroups (Fig. 1). Many studies

found that balance impairment in older adults with longer

duration PD usually did not respond to levodopa alone;

38% of persons with PD experienced falls; and persons with

PD were 5 times more likely than healthy older adults to suffer

fall-related injuries, such as hip fractures.42

In conclusion, this research documents vestibular as well as

balance dysfunction in patients with PD. Central vestibular

disorders were more common than peripheral ones. The most

prevalent balance abnormality was encountered in the sensory

organization subtest, though patients showed significant affec-

tion in other domains; namely, autonomic motor, voluntary

motor and functional limitation. Physiotherapy, as an adjunct

to medical treatment, showed significant effect in improv-

ing both vestibular and balance dysfunction in patients

with PD; thus improving their functional ability and overall

ambulation in everyday challenging situations. It is, therefore,

recommended to incorporate vestibular rehabilitation in

physiotherapy programs specifically in those who suffer con-

siderable balance and gait disorders.

References

1. Baltadjieva R, Giladi N, Gruendlinger L, Peretz C, Hausdorff J.

Marked alterations in the gait timing and rhythmicity of patients

with de novo Parkinson’s disease. Eur J Neurosci..

2006;24(6):1815–1820.

2. Beuter A, Hernandez R, Rigal R, Modolo J, Blanchet P. Postural

sway and effect of levodopa in early Parkinson’s disease. Can J

Neurol Sci.. 2008;35:65–68.

3. Bloem B. Benign paroxysmal positional vertigo in Parkinson’s

disease: underestimated and undertreated. Mov Disord..

2012;27(Suppl 1):940 [abstract].

4. Bloem B, Beckley D, Van Dijk J, et al. Medium latency stretch

reflexes in young-onset Parkinson’s disease and MPTP-induced

Parkinsonism. J Neurol Sci.., 1878-5883 1994;123(1–2):52–58.

5. Brod M, Mendelsohn G, Roberts B. Patients’ experiences of

Parkinson’s disease. J Gerontol B Psychol Sci Soc Sci..

1998;53B(4):P213.

6. Campbell W, DeJong R, Haerer A. DeJong’s the Neurologic

Examination: Incorporating the Fundamentals of Neuroanatomy and

Neurophysiology. Philadelphia: Lippincott Williams & Wilkins;

2005.

7. Chong R. Factor analysis of the functional limitations test in

healthy individuals. Gait Posture. 2008;28(1):144–149.

8. De Jong J, Jones M, Akinesia G. Hypokinesia, and bradykinesia in

the oculomotor system of patients with Parkinson’s disease. Exp

Neurol.. 1971;32:58–68.

9. Deane K., Jones D., Playford E., Ben-Shlomo Y., Clarke C.

Physiotherapy versus placebo or no intervention in Parkinson’s

disease. In: The Cochrane Library; 2001: No. 4. Available from:

Update Software, Oxford, and ISSN 1469–493 X.

10. Fisher I. Reliability and validity of the modified functional reach

test at the sub-acute stage post-stroke. Disabil Rehabil..

2009;31(3):243–248.

11. Franchignomi F, Martignoni E, Ferriero G, Pasetti C. Balance

and fear of falling in Parkinson’s disease. Parkinsonism Relat

Disord.. 2005;11:427–433.

Table 11 Comparison between the control group and the study subgroups as regards S-T-S test parameters.

S-T-S Control group Subgroup1 Subgroup2 Kruskall–Wallis test


Weight transfer (sec) 0.41a 0.8b 2.5b 9.6 0.008

Rising index (%) 28.5a 9.75b 6.0b 13.26 0.001

Sway velocity (deg/s) 4.2a 3.05a 4.5a 4.9 0.083

Weight symmetry (%) 5.5a 5.5a 15.5b 10.8 0.004

Medians with different letters are significantly different from each other. Highly significant statistical difference between the control group and the

study subgroups in Sit to stand test Weight transfer test (WT), rising index test and Weight symmetry.

Table 10 Comparison between the control group and the study subgroups as regards TW test parameters.

TW Control group Subgroup I Subgroup II ANOVA test


Speed test(cm/s) 28.7a 14.2b 8.0c 19.3 0.000

Step width (cm) 6.0a 8.5a 10.0a 4.6 0.099

End sway (deg/s) 3.7a 3.6a 7.0b 9.6 0.006

Means with different letters are significantly different from each other. Highly significant statistical differences between the control group and the

2 study subgroups in tandem walk speed test& end sway test.



http://refhub.elsevier.com/S2090-0740(15)00010-9/h0005
































12. Geotz CG, Poewe W, Rasaco O, Sampio C, Stibbis GT,

Council C, Giladi N, Holloway RG, Moore GC, Wennig GK,

Yaar MD, Seidi L. Movement Society Task force on rating

scales for Parkinsos disease. Movement society task force on

Hoem and Yarr staging scale: status and recommendation.

Movement Disord. 2004;19(9):1020–1028.

13. Gibson J, Pimlott K, Kennard C. Ocular motor and manual

tracking in Parkinson’s disease and the effect of treatment. J

Neurol Neurosurg Psychiatry. 1987;50:853–860.

14. Giladi N, Shabtai H, et al. Construction of freezing of gait

questionnaire for patients with Parkinsonism. Parkinsonism Relat

Disord.. 2000;6(3):165–170.

15. Giladi N, Tal J, et al. Validation of the freezing of gait

questionnaire in patients with Parkinson’s disease. Mov Disord..

2009;24(5):655–661.

16. Grimbergen Y, Munneke M, Bloem B. Falls in Parkinson’s

disease. Curr Opin Neurol.. 2004;17(4):405–415.

17. Gushikem P. Otoneurologic assessment in elderly patients with

dizziness. 2001. 84f. Thesis. (MSc in Human Communication

Disorders) – Federal University of Sao Paulo-Paulista School of

Medicine, Sao Paulo. Acta A Who; 2001: 21:1–25.

18. Haas C, Turbanski S, Kessler K, Schmidtbleicher D. The effects of

random whole-body-vibration on motor symptoms in Parkinson’s

disease. NeuroRehabilitation., 1878-6448 2006;21(1).

19. Hain T., Ramaswamy T., Hillman M. Anatomy and physiology of

the normal vestibular system. In: HERDMAN, SJ Vestibular

Rehabil. 2nd ed., London: Manole; 1987: 3–24.

20. Henzi S, Stanga Z, Ludin H. Vestibular disorders in Parkinson

patients. Schweiz Med Wochenschr. 1990;120:1297–1303.

21. Horak F, Woollacott M. Parkinson’s disease impairs the ability to

change set quickly. J Neurol Sci.. 2000;175(1):57–70.

22. Inkster L, Eng J. Postural control during a sit-to-stand task in

individuals with mild Parkinson’s disease. Exp Brain Res..

2003;154(1):33–38.

23. Jankovic J. Parkinsonism: clinical features and differential

diagnosis. Program for a Comprehensive Review of Movement

Disorders for the Clinical Practitioner. Aspen, CO; 2003: 337–380.

24. Konczak J, Corcos D, Horak F, et al. Proprioception and motor

control in Parkinson’s disease. J Motor Behav..

2009;41(6):543–552.

25. Krauzlis R. Recasting the smooth pursuit eye movement system. J

Neurophysiol.. 2004;91:591–603.

26. Lord S, Murray S, Chapman K, et al. Sit-to-stand performance

depends on sensation, speed, balance, and psychological status in

addition to strength in older people. J Am Geriatr Soc..

2002;57:M539–M543.

27. Mazzoni P, Hristova A, Krakauer J. Why don’t we move faster?

Parkinson’s disease, movement vigor, and implicit motivation. J

Neurosci.. 2007;27(27):7105–7116.

28. McNaught K, Jenner P. Proteasoma impaired in substantia nigra

in Parkinson’s disease. Neurosci Lett.. 2001;297(3):191–194.

29. Mota P, Franco E, Pinto Monteiro A. Study of balance in the

elderly by electronystagmo-graphy. Acta A Who. 2005;21:1–12.

30. Nallegowda M, Singh U, Handa G, et al. Role of sensory input

and muscle strength in maintenance of balance, gait, and posture

in Parkinson’s disease: a pilot study. Am J Phys Med Rehabil..

2004;83:898–908.

31. Nallegowda M, Singh U, Bhan S, Wadwa S, Handa G, Dwivedi

SN. Balance and gait in total hip replacement: a pilot study. Am J

Sports Med Rehabil.. 2003;82:669–677.

32. Nashner LM. Computerized dynamic posturography. In:

Jacobson G, Newman C, Kartush J, editors. Handbook of balance

function and testing. Mosby Year Book; 1993:280–307.

33. Neurocom international Inc, 2012: Rhythmic weight shift test.

www.neurocom.com.

34. O’Suilleabhain P, Bullard J, Dewey R. Proprioception in

Parkinson’s disease is acutely depressed by dopaminergic med-

ications. J Neurol Neurosurg Psychiatry. 2001;71:607–610.

35. Qutubuddin A, Cifu D, Armistead-Jehle P, Carne W, Mcguirk T,

Baron M. A comparison of computerized dynamic posturography

therapy to standard balance physical therapy in individuals with

Parkinson’s disease: a pilot study. NeuroRehabilitation.

2007;22:261–265.

36. Shepard N.T. Clinical Utility of the Motor Control Test (MCT)

and Postural Evoked Responses (PER). NeuroCom Publication;

2000.

37. Silveira S., Taguchi C., Gananca F. Comparative analysis of two

lines of treatment for patients with peripheral vestibular syndrome

over the age of sixty. Acta A WHO. Sao Paulo; 2002: vol. 21, no.

1, p. 1–13, Jan seas.

38. Simuni T. Diagnosis and management of Parkinson’s disease.

Medscape Neurol.. 2007.

39. Sparks D. The brainstem control of saccadic eye movements. Nat

Rev Neurosci.. 2002;3:952–964.

40. Tagliabue M, Ferrigno G, Horak F. Effects of Parkinson’s disease

on proprioceptive control of posture and reaching while standing.

Neuroscience. 2009;158:1206–1214.

41. Teravainen H, Calne D. Studies of Parkinsonian movement: I.

Programming and execution of eye movements. Acta Neurol

Scand.. 1980;62:137–148.

42. Toole T, Hirsch M, Forkink A, Lehman D, Maitland C. The

effects of a balance and strength training program on

Parkinsonism: a preliminary study. J Neurol Rehabil..

2000;14:165–174.

43. Tsang W, Wong V, Fu S, Hui-Chan C. Tai chi improves standing

balance control under reduced or conflicting sensory conditions.

Arch Phys Med Rehabil.. 2004;85:129–137.

44. Vaugoyeau M, Azulay J. Role of sensory information in the

control of postural orientation in Parkinson’s disease. J Neurol

Sci.. 2010;289(1–2):66–68.

45. Vestergaard P, Rejnmark L, Mosekilde L. Fracture risk associated

with Parkinsonism and anti-Parkinson drugs. Calcified Tissue

Int.., 1432-0827 2007;81(3):153–161.

46. Visser J, Allum J, Carpenter M, et al. Effect of subthalamic

nucleus deep brain stimulation on axial motor control and

protective arm responses in Parkinson’s disease. Neuroscience.,

1873-7544 2008;157(4):798–812.

47. Walker R, Purnell G, Jones-Jackson L, Thomas K, Brito J, Ferris

E. Introduction to PET imaging with emphasis on biomedical

research. Neurotoxicology. 2004;25(4):533–542.

48. White O, Saint-Cyr J, Tomlinson R, Sharpe J. Ocular motor

deficits in Parkinson’s disease II. Control of the saccadic and

smooth pursuit systems. Brain. 1983;106:571–587.
























































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Effect of different modes of therapy on vestibular and balance dysfunction in Parkinson’s disease