Hala A Shaheen et al.

129

Parkinson's Disease and Pulmonary Dysfunction

Hala A Shaheen1, Mohammad A. Ali

2 , Mohy A. Abd Elzaher

3

Departments of Neurology1, Chest

2, Fayoum University; Chest

3, El-Mataria Teaching Hospital

ABSTRACT

Rationale and Background: Pulmonary functions impairment contributes significantly to morbidity and

mortality in Parkinson's disease (PD) patients. This study aimed to investigate the presence and type of pulmonary

dysfunction in (PD) patients, to relate it to clinical data and to study the effect of L -Dopa on it. Patients and

Methods: Thirty non smoker PD patients who had no history of respiratory disease were included according to

inclusion criteria of United Kingdom PD Society Brain Bank. Their mean age was (67.7±8.4) years. They were 28

males and 2 females. Fifteen healthy non smoker persons served as age and sex -matched control group. The clinical

disability of PD was indicated by Unified Parkinson Scale and Modified Hoehn-Yahr (MHY) scale. Pulmonary

functions were performed during a stable on state of disease and in an off state. Results: Forced Vital Capacity

(FVC) and Forced Expiratory Volume in 1 second (FEV1) in the PD patients were statistically significantly lower

than in the control group. Impairment of pulmonary function was detected in 24 patients (80%). Restrictive defect

was observed in19 patients (63.3%), while obstruction was present in 5 patients (16.7%). Correlations studies

between pulmonary functions parameters and clinical data showed no significant correlations. Pulmonary functions

improved after treatment but the difference did not reach statistical significance. Conclusion and

Recommendations: Pulmonary dysfunction mainly restrictive type is a frequent finding in PD. irrespective of

disease severity, partially responded to levodopa. Routine assessment of pulmonary functions is recommended in PD

even mild cases without respiratory complaint. (Egypt J. Neurol. Psychiat. Neurosurg., 2009, 46(1): 129-140)

INTRODUCTION

Parkinson's disease (PD) is a common

disabling progressive disorder1. Although dyspnea is

not a frequent complaint in patients with PD,

pulmonary dysfunctions is documented among

them2 contribute significantly to morbidity and

remains one of the most common causes of death in

these patients3. The spectrum of respiratory

dysfunction in Parkinson's disease (PD) has been

broadened to include not only the primary effects of

PD on the ventilation but also pulmonary

complications of antiparkinsonian therapy4. Primary

pulmonary abnormalities include a restrictive change

and airway obstruction5. A restrictive spirometric

defect was reported to be the main spirometric

finding in PD patients6. These restrictive changes

could be attributed to progressive impairment of

maneuvers that require rapid activation and

coordination of upper airway and chest wall

musculature as sequel of motor dysfunction

progression during the natural course of Parkinson

disease7,8

. These restrictive changes are responsive

to dopaminergic modulation9. Generalized airway

obstruction was reported to be present in patients

with Parkinson's disease10

. This probably reflects

involvement of the upper airway musculature.

Pulmonary obstruction reversibility after levodopa

therapy has been suggested11

. Levodopa may

produce its effects by improvement of respiratory

muscle weaknes12

.

Study Objectives:

This study was therefore carried out to

investigate the presence of pulmonary dysfunctions

in Parkinson's disease patients; in comparison to age

and sex-matched control subjects; in order to specify

the type of the impairment in breathing in PD and

relate these changes to clinical data of the disease

and to investigate the effects of oral intake of

levodopa on pulmonary functions in PD patients.

Correspondence to Hala A. Shaheen, e-mail: Shaheen_a_hala@yahoo.com. Contact number: 0107965888

Egypt J. Neurol. Psychiat. Neurosurg. Vol. 46 (1) - Jan

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PATIENTS AND METHODS

Patients:

This is a cross sectional case control study

conducted on 30 patients with idiopathic

Parkinson’s disease; who had no history of

respiratory disease and non smoker. Their age

ranged from to 47-84 years with a mean age of

67.7±8.4 years. The duration of illness ranged from

to one month to 10 years with a mean duration of

3±2.3 year. They were 28 males and 2 females.

Patients were included in the study according to

inclusion criteria of United Kingdom Parkinson’s

Disease Society Brain Bank by Gibb and Lees13

.

Patients with the exclusion criteria of United

Kingdom Parkinson’s Disease Society Brain Bank;

age below 40 years; presence of focal cerebral lesion

in the CT scan of the brain; Patients with a history of

smoking currently or in the past, lung disease, drugs

that might result in pulmonary dysfunction; and

those unable to perform pulmonary function test

(PFT) because of clinical sign of dementia (Mini

Mental state Examination less than 23)14

were

excluded from this study. According to clinical

presentation, the patients were classified into 2

groups; group (1) 23 patients (76.66%) presented

mainly with tremors and group (2) 7 patients

(23.33%) presented mainly with akinesia. Seventeen

patients (56.7%) was on L-dopa therapy and the

duration of therapy ranged from one month to 3years

with a mean duration (3±2.9) years.

Fifteen healthy non-smoker individuals with no

evidence of pulmonary disease age and sex matched

(14male and 1 female), their mean age was

(65.07±7.4) years were selected as “Control group”.

Methods:

All patients were subjected to the following battery

of assessment:

- Detailed history taking, general and

neurological examination,

- The clinical disability of PD was indicated by

Unified Parkinson Scale and Modified Hoehn-

Yahr (MHY) scale.

- Unified Parkinson’s Disease Rating Scale

(UPDRS)15

UPDRS is the most widely used scale for

measuring severity of parkinsonian symptoms,

as it has a nearly comprehensive coverage of

motor symptoms, and has a clinometric

properties, including reliability and validity16

. It

includes 36 items under 4 heading of

mentations, behavior and mood, activities of

daily living, motor examination and therapy

complications. Each item is graded from 0-4,

where 0 is normal and 4 can barely perform the

task.

- Modified Hoehn and Yahr staging (MHY)17

MHY is a simple and popular scale used to

establish the severity of PD consisting of 5

stages according to disease severity with stage 5

is the severest form. Whereby stage 1 is mild

unilateral Parkinsonism, stage 2 is mild bilateral

Parkinsonism, stage 3 includes postural

instability, stage 4 is marked incapitation with

the ability to walk still preserved and stage 5 is

confinement to bed or wheelchair.

- Mini-Mental State Examination (MMSE)14

MMSE is a brief clinical test designed to

grossly assess cognitive function. MMSE

assesses orientation, attention, calculation,

registration, immediate and short-term recall,

language and the ability to follow simple

verbal, written commands. A perfect score is

30 points. Patients had score > 23 were

excluded from the study for fear of they will

not cooperate during the (PFT).

- Neuroimaging: Computerized Tomography

(CT) of the Brain was performed for all

patients to exclude any focal cerebral lesions.

Assessment of pulmonary functions:

The pulmonary function tests (PFT) were

performed using 2200 pulmonary function

laboratory sensor medics to all patients and controls

participating in this study. After explaining the test

to the patient, entering age, height and sex, attach a

nasal clip to the patient. The maneuver was

performed by asking the patient to breathe through

mouth piece. First briefly in his normal tidal volume

range then to inhale to his maximum volume {forced

vital capacity (FVC)}. Then ask patient to exhale so

hard, fast and completely as possible {forced

expiratory volume in first second (FEV1)}. All

patients had to do each maneuver three times and the

Hala A Shaheen et al.

131

best of three technically accepted tests was

considered. The forced vital capacity (FVC) and

forced expiratory volume in first second (FEV1)

Ratio of Forced Vital Capacity (FVC) to Forced

Expiratory Volume in 1 second (FEV1/FVC) Ratio

were described as percentage of the predicted

values, based on each individual weight, height and

body surface area. To investigate how levodopa can

affect respiratory dysfunction in Parkinson's disease

(PD), we compared Spirometric values (FVC),

(FEV1), Ratio of (FEV1/FVC) after a 12-h

withdrawal of levodopa therapy (OFF) state, and 1 h

after oral intake of levodopa(ON) state in the

treated patients, Normal ranges is calculated

according to American Thoracic Society18

. FVC and

FEV1 > 80 % of predicted values were scored as

normal. Two basic types of lung dysfunction were

defined by spirometry: obstructive patterns and

restrictive patterns. A restrictive pattern means that

lung volumes are small. The primary criterion for

this diagnosis was FEV1/FVC ratio higher than 80%

provided that FEV1 and / or FVC less than 80% of

predicted value). The primary criterion for airflow

obstruction was a reduced FEV1/FVC ratio<70% of

normal value provided that FEV1 and/or FVC less

than 80% of predicted value18

.

Statistical analysis

All continuous (quantitative) variables were

expressed as mean±SD. Categorical (qualitative)

data were presented as frequency and percentages.

Comparisons of PFT parameters between patients

and control subjects were performed using Mann-

Whitney test. Chi square and student's independent

sample t test were used for comparison between

patients groups. ANOVA test was used to compare

means of clinical scales and pulmonary function

parameters among groups. P value of < 0.05 was

considered statistically significant. Correlations

between pulmonary functions and clinical data were

also performed using linear correlations.

RESULTS

This is study conducted on 30 patients with

idiopathic Parkinson’s disease who had no history of

respiratory disease and non smoker. Their age

ranged from to 47- 84 years with a mean age of

67.7±8.4 years. The duration of illness ranged from

to one month to 10 years with a mean of (3±2.3

years). They were 28 males and 2 females.

Seventeen patients (56.7%) was on L-dopa therapy

and the duration of therapy ranged from one month

to 3 years with a mean duration 3±2.9 years.

According to clinical presentation, the patients were

classified as 2 groups; group (1) 23 patients

(76.66%) presented mainly with tremors and group

(2) 7 patients (23.33%) presented mainly with

akinesia figure (1).

Unified Parkinson’s Disease Scale (UPDS)

score in our patients ranged from 13 to 61 with the

mean of 32±12.2. Motor activities in our patients

ranged from 10 to 32 with the mean of 21.3±6.27.

Daily living activities ranged from 2 to 21 with the

mean of 8.4±5.3. The number and percent of

patients in some UPDS sub-items are presented in

table (1).

Based on Hoehn and Yahr Severity Score, Six

patients (20%) were in H-Y grade 1.5, 7 cases

(23.3%) were in H-Y grade 2.5 and 15 patients

(50%) were in H-Y grade 3 and remaining 2

patients (6.7%) had severe PD (H-Y grade 4 (Fig. 2).

Fifteen non-smoker healthy individuals (14

male, 1female, mean age, 65.07±7.4 years) age

matched to our patients (P value was 0.298) with no

evidence of pulmonary disease were selected as

“Control group”.

Forced Vital Capacity (FVC) and Forced

Expiratory Volume in 1 second (FEV1) in the

patients groups were statistically significantly lower

than those in the control group (Table 2).

Of our thirty patients; 24 patients (80%) was

found to have abnormal respiratory functions. A

spirometric restrictive ventilatory defect was

observed in 19 patients (63.3%) and evidence of

upper airway obstruction was observed in 5 (16.7%).

Only 6 patients (20%) were found to have normal

respiratory functions (Fig. 3).

Comparing clinical data and pulmonary

functions in group (1) patients presented mainly

with tremors; and group (2) those presented mainly

with akinesia, the duration of illness was statistically

significantly longer in group (1) patients than group

(2). Other clinical data and pulmonary functions

parameters did not differ significantly between the 2

groups of patients (Table 3).

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Pattern of pulmonary functions whether normal,

restrictive or obstructive also did not differ

significantly between patients in group (1) and group

(2). Number of patients in each pattern of pulmonary

functions in the two patients groups is shown in figure

(4).

No significant difference was found among

patients had normal, those had restrictive and those

had obstructive pulmonary functions as regard

clinical data. Pulmonary functions parameters

indeed differed significantly (Table 4).

Correlations studies between pulmonary

functions parameters and clinical data showed no

significant correlations (Table 5).

Although pulmonary functions parameters in

the treated patients improved after treatment than

before treatment, the difference did not reach

statistical significance (Table 6).

Fig. (1): Clinical presentation of the patients.

Table 1. Sub items of Unified Parkinson’s Disease Scale in our patients.

UPDS Grade 0

Number (%)

Grade 1

Number (%)

Grade 2

Number (%)

Grade 3

Number (%)

Bradykinesia 0 (0%) 7 (23.3%) 21 (70%) 2 (6.7%)

Rigidity 0 (0%) 6 (20%) 21 (70%) 3 (10%)

Posture 0 (0%) 14 (46.7%) 16 (53.3%) 0 (0%)

Gait 0 (0%) 21 (70%) 8 (26.7%) 1 (3.3%)

Posture instability 0 (0%) 6 (20%) 24 (80%) 0 (0%)

Tremor 7 (23.3%) 5 (16.7%) 7 (23.3%) 11 (35.7%)

Action tremor 18 (60%) 3 (10%) 6 (20%) 3 (10%)

UPDS: Unified Parkinson’s Disease Scale

Table 2. Pulmonary functions test parameters in the patients and the control group.

Pulmonary functions Patients group Control group P Value

FVC 64.673±22.661 94.253±23.5500 0.000

FEV1 64.425±34.086 109.900±36.7031 0.000

FEV1/FVC 122.946±61.0044 113.860±19.8333 0.809

FVC: Forced Vital Capacity (FVC),

Hala A Shaheen et al.

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FEV1:Forced Expiratory Volume in 1 second

FEV1/FVC: Forced Vital Capacity to

Forced Expiratory Volume in 1 second Ratio

Fig. (2): Number of patients in each grade of Hoehn and Yahr Score.

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5

19

6

Normal

R estrictive

O bstructive

Fig. (3): Patterns of pulmonary functions in the patients group.

Table 3. Clinical data and pulmonary functions in the patients groups.

Parameter Group (1)

23 patients

Group (2)

7 patients P Value

Age 67.2±8.2 69.5±9.4 0.5

Duration of illness 36.2±28.8 11.5±11.6 0.009

On therapy 16 (59.6%) (85.7%) 6

0.01 Not on therapy 7 (30.4%) (14.3%)1

Duration of therapy, 32. 3±31.6 1 0.09

URPS (total) 33.6±10.1 26.8±17.1 0.09

Daily living activities 9.08±4.7 6.42±7.04 0.07

Motor 22.3±5.6 18±7.6 0.13

Bradykinesia

Grade (1)

Grade (2)

Grade (3)

5 (21.7%)

17 (73.9%)

1 (4.3%)

2 (28.6%)

4 (57.1%)

1 (14.3%)

0.57

Rigidity

Grade (1)

Grade (2)

Grade (3)

4 (17.4%)

17 (73.9%)

2 (8.7%)

4 (28.6%)

8 (57.1%)

2 (14.3%)

0.69

MHAY scale 2.5±0.7 2.9±0.5 0.17

FVC 66±23,8 60±19.2 0.82

FEV1 64.7±35.6 63.5±31 0.82

FEV1/FVC 131.2±64.4 95.7±40.1 0.39

Table 4. Clinical data and pulmonary functions in the patients.

Hala A Shaheen et al.

135

Clinical data

Patients with

normal

pulmonary

functions

Patients with

restrictive

pulmonary

functions

Patients with

obstructive

pulmonary

functions

P Value

Age 68.3±6.6 69.5±7.3 60.24±11.3 0.08

Duration of illness 24.3±14.5 35.4±32.6 18.8±13.5 0.9

On therapy 3 (50%) 14 (73.7%) 0 (0%) 0.012

Not on therapy 3 (50%) 5 (26.3%) 5 (100%)

Duration of therapy 32±13.8 30.1±34.5 0 0.49

URPS (total) 27.5±10.1 31.8±12.3 38±13.4 0.3

Daily living activities 7.3±3.8 8.2±5.6 10.8±6.01 0.64

Motor 18.3±5.7 21.6±6.6 23.6±4.9 0.369

Bradykinesia Grade (1) Grade (2) Grade(3)

0 (0%)

6 (100%) 0 (0%)

6 (31.9%)

12 (63.2%) 1 (5.3%)

1 (20%) 3 (60%) 1 (20%)

0.315

Rigidity Grade(1) Grade(2) Grade(3)

0 (0%)

5 (83.3%) 1 (16.7%)

5 (26.3%)

14 (73.7%) 0 (0%)

1 (20%) 2 (40%) 2 (40%)

0.059

MHAY scale 2.5±0.5 2.6±0.6 2.8±0.9 0.8

FVC 91.5±22.5 61.4±16.15 44.5±16.5 0.000

FEV1 108.8±35.5 60.5±20.9 25.9±2.7 0.000

FEV1/FVC 114.4±18.8 145±61.8 122.9±61 0.004

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43

16

22

3

0 2 4 6 8 10 12 14 16

G roup (1)

G roup (2)

R estrictive

O bstructive

Normal

Fig. (4): Number of patients in each pattern of pulmonary functions in the patients groups.

Table 5. Correlations studies between pulmonary functions parameters and clinical data.

Clinical data FVC FEV1 FEV1/FVC

R P R P R P

Age 0.310 0.095 0.240 0.201 0.350 0.058

Duration of illness 0.134 0.479 0.026 0.894 0.139 0.464

Duration of therapy 0.144 0.582 0.046 0.861 -0.019 0.942

URPS (total) -0.221 0.241 -0.231 0.219 0.011 0.954

Daily living activities

Motor -0.239 0.204 -0.260 0.166 0.028 0.881

Bradykinesia 0.213 0.259 0.021 0.911 -0.319 0.086

Rigidity -0.075 0.693 -0.015 0.939 -0.315 0.096

MHAY scale -0.056 0.768 -0.015 0.936 -0.292 0.117

Hala A Shaheen et al.

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Table 6. Pulmonary functions parameters in the treated patients before and after treatment.

Pulmonary functions

parameters Before treatment After treatment P-Value

FVC 66.7±12.8 60.7±11.7 0.108

FEV1 79.6±21.5 75.5±13.9 0.372

FEV1/FVC 117.1±17.5 121.6±8.7 0.276

DISCUSSION

Frequency of respiratory system involvement

in Parkinson's disease is more than what is usually

perceived19

. Respiratory dysfunction in Parkinson's

disease whether restrictive or obstructive remains

one of the most common causes of death in these

patients20

. Some authors found these pulmonary

dysfunctions correlating to disease severity and L-

dopa treatment21

, others reported pulmonary

dysfunctions even in mild cases unaffected by

medications22

.

In our study in agreement with De Bruin et

al.23

Forced Vital Capacity (FVC) and Forced

Expiratory Volume in 1 second (FEV1) in the PD

patients were statistically significantly lower than in

the control group. Of our thirty patients who had no

history of respiratory disease and non smoker; 24

patients (80%) was found to have abnormal

pulmonary functions. This goes with the results of

Pramod et al.24

, whose study showed that pulmonary

function abnormalities commonly exist in PD

patients in absence of respiratory symptoms. The

pulmonary status of PD patients probably remains

unnoticed because physical disability; in Parkinson's

disease patients; often limits their activities where

respiratory problems can manifest.

The restrictive pattern was the most common

pulmonary abnormality encountered in our study. A

restrictive ventilatory defect (FEV1/FVC ratio higher

than 80% provided that FEV1 and/or FVC less than

80% of predicted value) was observed in 19 patients

(63.3%) and evidence of upper airway obstruction

(reduced FEV1/FVC ratio < 70% of normal value

provided that FEV1 and/or FVC less than 80% of

predicted value) was observed in 5 patients (16.7%).

These findings are consistent with previous studies

which have indicated that restrictive pulmonary

dysfunction is the main abnormality noticed in

PD25,26

. This restriction is probably due to

incoordinated expiratory effort or abnormally low

chest wall compliance, secondary to chest wall

rigidity. In

Parkinson's disease

profound

degeneration of the nigrostriatal dopaminergic

system leads to dysfunction of basal ganglia and

consequently its output disrupting the pathways to

the thalamus that are mainly involved in the control

of voluntary movements.

By contrast, others had found obstructive

pattern of ventilatory abnormalities (FEV1/FVC<

80% of normal value) in most of their patients

attributing this to the increase in the parasympathic

activity.24,27

It is widely accepted that patients with

PD frequently have cardiac or bowel dysfunction

based on the visceral autonomic dysfunction,

pulmonary obstruction may also be caused by

possible autonomic dysfunction in patients with PD.

In this study comparing clinical data and

pulmonary functions in group (1) patients presented

mainly with tremors; and group (2) those presented

mainly with akinesia; the duration of illness was

statistically significantly longer in group (1). This

could be explained by the fact that tremors may be

less disabling to the patients and don’t enforce them to

seek medical advice rapidly. Other clinical data and

pulmonary functions parameters did not differ

significantly between the two groups of patients. Also

no significant difference was found between patients

had normal, those had restrictive and those had

obstructive pulmonary functions as regard clinical

data. Also correlations studies between pulmonary

functions parameters and clinical data showed no

significant correlations. Similarly Tzelepis

et al.28

reported that the clinical profile did not influence the

pattern of the pulmonary functions in their PD

patients. Conversely Bogaard et al.29

found a

significant correlations between PD scales and

spirographic parameters; patients with more severe PD

Hala A Shaheen et al.

137

had lower percentage forced vital capacity. Those with

fluctuations and/or dyskinesia had lower FVC% and

percentage forced expiratory flow volume in 1 sec

(FEV1%). Hovestadt et al.30

and Carasso et al.31

also

found more patients with severe disease had abnormal

PFT values than patients with mild Parkinsonism.

These discrepancies in the results could be explained

by several reasons: Most of our patients had mild to

moderate PD with no one had complications of

therapy. Some studies included all disease grades,

others included only severe cases. Moreover disease

duration differ between studies. Cut off point for

obstruction also differed among studies. Some authors

define obstructive pattern if (FEV1/FVC < 75% others

< 80% of normal value). We define obstructive

pattern according to American Thoracic Society18

if

(FEV1/FVC < 70% of normal value) and this

difference in patients selections and methodology

used could contribute to differences encountered

between the results of different studied and ours.

Reviewing the effects of antiparkinsonian

drugs on pulmonary functions in various studies

yielded conflicting results32

. Some authors reported

that the motor disability in PD patients can be partly

reversed with levodopa therapy through decreasing

muscle rigidity, improving coordination of muscles

and facilitation of movement. These effects should

improve respiratory functions33

. Indeed, in this study

although pulmonary functions parameters improved

after treatment, the difference did not reach

statistical significance. This may be explained by the

fact that we studied the effects of drugs on

pulmonary function tests one hour after oral intake

of drug, which is the usual levodopa plasma

concentration peak. However, the optimal

improvement in motor function hence pulmonary

functions improvement may be delayed34

. Similarly

Haas et al.35

reported that pulmonary dysfunction of

restrictive type partially responded to levodopa. But

Nakane et al.36

found significant improvement in

maximal voluntary ventilation, FEV1, FVC in

patients receiving levodopa. Also Herer et al.37

and

Weiner et al.2 reported significant improvement in

the restrictive ventilatory abnormalities of extra-

pulmonary origin (weakness of respiratory

musculature) in 'on' state compared to 'off' state.

Forced expiration volume (FEV1) improvement

suggests regained mobility during treatment. This

increase in (FVC) could be due to a raised

inspiratory capacity and thus an increase in the

active part of ventilation. A central effect or a

correction of uncoordinated respiratory movements

by L-dopa may contribute. Conversely Obenour et

al.38

, did not find any change in expiratory flow or

lung volumes after levodopa treatment and

Sathyaprabha et al.26

found both forced vital

capacity (FVC) and forced expiratory volume

(FEV1) remained almost identical after L-dopa

intake. These discrepancies in results could be

explained by several reasons: (1) difference in

patients selections and methodology used, (2) these

abnormalities may also depend on the motor status

of the patient, demonstrating partial or complete

benefit of levodopa. (3) Different dose of L-dopa

used; some studies use 100mg, others including us

use patient dose. Respiratory dyskinesia, a side

effect of levodopa therapy, may produce both

restrictive and dyskinetic ventilation39

. None of our

patients had dyskinesia

There is a raised issue of respiratory muscle

strength training has the potential to improve

expiratory muscle strength. This improvement in

respiratory muscle strength has positive impact on

reducing pulmonary complications and improving

quality of life in PD patients40,41

.

Conclusion and Recommendations

In Parkinson's disease patients who have no

respiratory symptoms, pulmonary dysfunction is a

frequent finding. A restrictive pattern is the most

common type encountered, which improves partially

with levodopa. Routine evaluation of pulmonary

function is suggested to be included in the

management of Parkinson’s disease irrespective of

disease severity as pulmonary function test are well

worth considering in anticipating and thus

preventing pulmonary complications in Parkinson's

disease patients. Future trials are therefore warranted

to investigate the clinical relevance of respiratory

muscle training and its potential to improve

expiratory muscle strength.

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الملخص العربى

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2009

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