Respiratory muscle strength and training in stroke and neurology: a systematic review

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Respiratory muscle strength and training in stroke andneurology: a systematic review

Ross D Pollock1*, Ged F Rafferty2, John Moxham2, and Lalit Kalra1

We undertook two systematic reviews to determine the

levels of respiratory muscle weakness and effects of respira-

tory muscle training in stroke patients. Two systematic

reviews were conducted in June 2011 using a number

of electronic databases. Review 1 compared respiratory

muscle strength in stroke and healthy controls. Review 2 was

expanded to include randomized controlled trials assessingthe effects of respiratory muscle training on stroke and other

neurological conditions. The primary outcomes of interest

were maximum inspiratory and expiratory mouth pressure

(maximum inspiratory pressure and maximum expira-

tory pressure, respectively). Meta-analysis of four studies

revealed that the maximum inspiratory pressure and

maximum expiratory pressure were significantly lower

(P< 000001) in stroke patients compared with healthy

individuals (weighted mean difference -4139 and

-5462 cmH2O, respectively). Nine randomized controlled

trials indicate a significantly (P =00009) greater effect of

respiratory muscle training on maximum inspiratory pres-

sure in neurological patients compared with control subjects

(weighted mean difference 694 cmH2O) while no effect on

maximum expiratory pressure. Respiratory muscle strength

appears to be impaired after stroke, possibly contributing to

increased incidence of chest infection. Respiratory muscle

training can improve inspiratory but not expiratory muscle

strength in neurological conditions, although the paucity of

studies in the area and considerable variability between

them is a limiting factor. Respiratory muscle training may

improve respiratory muscle function in neurological con-

ditions, but its clinical benefit remains unknown.

Key words: neurology, rehabilitation, respiratory, stroke,

weakness

Introduction

Stroke is one of the leading causes of morbidity and mortalityin the Western world (1) with up to 78 % of stroke patients

presenting with dysphagia (2,3). Dysphagia is associated with

a threefold increase in the risk of developing a chest infection,

which increases to 11-fold in those with definite aspiration

(2,4). Cough is an important mechanism to guard against

aspiration, which is often impaired in stroke patients (5) and

results in greater incidences of aspiration and chest infection

(6,7).

A strong cough is dependent on the ability to draw air into

the lungs, generate high pressures and air flow velocities, while

maintaining the patency of the airways (8), each of which are

influenced by respiratory muscle function. In stroke patients,respiratory muscle weakness and altered chest wall kinematics

(9,10) may be responsible for impaired cough. Although

muscle weakness is often present in the acute stages of stroke,

this is likely due to impaired central drive to the muscles (11)

rather than reductions in the intrinsic strength of the muscle

(12). Whatever the mechanism, a means of improving respi-

ratory muscle strength and/or central drive to the muscle may

be beneficial for stroke patients.

Inspiratory muscle training (IMT) or expiratory muscle

training (EMT) have been found to improve respiratory

muscle strength and function in multiple sclerosis (MS)

(13,14) and Parkinsons disease (PD) (15). These results

suggest that respiratory muscle training (RMT) can have a

beneficial effect on respiratory muscle function in neurologi-

cal conditions. If similar results were to occur in stroke

patients, this could provide a potential treatment to improve

muscle function and cough and reduce the incidence of chest

infections.

Relatively little is known about the effects of stroke on res-

piratory muscle function or effective rehabilitation strategies

to improve muscle function. The aim of this review is twofold:

To perform a systematic review of studies in which respira-tory muscle strength has been assessed in stroke patients

Correspondence: Ross D. Pollock*, Kings College London, Denmark

Hill Campus, Academic Neuroscience Centre, PO41 Institute of

Psychiatry, London SE5 8AF, UK.

E-mail: [email protected] of Clinical Neurosciences, Kings College London,

London, UK2Division of Asthma, Allergy and Lung Biology, Kings College London,

London, UK

Conflict of interest: None declared.

DOI: 10.1111/j.1747-4949.2012.00811.x

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To conduct a meta-analysis of studies investigating theeffects of RMT on individuals who have had a stroke.

Methods

Two literature reviews without any time restrictions were

performed in June 2011 using a number of electronic data-bases (PubMed, EMBASE, ISI Web of Science; review 1 also

included Scopus, while review 2 included the Cochrane

Central Register for Controlled Trials). The key words in

review 1 were stroke or cerebrovascular accident in combina-

tion with inspiratory, expiratory, or respiratory and strength

or weakness. Review 2 included randomized controlled

trials (RCTs) investigating the effect RMT on stroke patients;

however, initial searches revealed only two articles of this

nature. In light of this, review 2 was expanded to include other

neurological conditions. The key words used in review 2 were

stroke, cerebrovascular accident, multiple sclerosis, Parkinsons

disease,motor neurone disease, andneurologyin combination

with inspiratory, expiratory, respiratory, or ventilatory andtraining,loading, andmuscle. The reference list of each article

identified from these searches were checked for any further

publications, while a forward search using the Science Citation

Index was also conducted.

Study selection criteria

Review 1

Only articles that assessed respiratory muscle strength in

stroke patients compared with healthy controls were included

in the review. No age limit for stroke patients was defined.

Review 2

This review was restricted to RCTs conducted in subjects 18

years or older. Only studies investigating RMT (IMT or EMT)

were included. Articles in which subjects were not randomly

assigned to an intervention or control group were excluded.

Abstracts, letters to the editor, and commentaries were also

excluded due to insufficient reported details.

For both reviews, only original articles written in English

and published in peer-reviewed journals were included. After

the initial search, duplicates were removed with titles and

abstracts of the remaining articles assessed for eligibility. Any

uncertainty was discussed between authors until a consensus

was reached. The risk of bias of each study included in review

2 was determined using the Cochrane Collaborations tool

for assessing risk of bias (16). The quality of randomization,

blinding, and description of dropouts was assessed using the

scale reported by Jadadet al. (17). One point each is awarded

for randomization, double-blinding, and adequate des-

cription of withdrawals; one further point can be added for

randomization and blinding if the method used to do this is

described, while points are deducted if it is done inappro-

priately. A maximum score of 5 can be obtained.

The primary outcome of interest in both reviews was

maximal inspiratory and expiratory mouth pressure (PImax

and PEmax, respectively). For each outcome in review 2, data

were extracted from before the intervention and immediately

after the intervention for treatment and control groups.When

required, authors were contacted and original data were

sought. When these were not available, values were inputtedfrom the results in these papers using previously described

methods (18,19).

Results

Review 1

Four articles were included in the review (Fig. S1) (5,9,12,20).

PImax and PEmax were recorded in 57 stroke patients and

64 control subjects. Study characteristics and outcomes are

reported in Table 1. PImax was significantly lower in the

stroke patients than in the control subjects [weighted mean

difference (WMD) -4139 cmH2O, 95% confidence interval(CI) -5374 to -2903, P< 000001] as was PEmax (WMD

-5462 cmH2O, 95% CI-6124 to -4781, P< 000001; Fig. 1).

The one study conducted in patients greater than three-

months after stroke onset (20) reported higher values of

PImax and PEmax suggesting improvement with time.

Review 2

Nine articles were included in the review (Fig. S2 to be found

online); two assessed stroke patients (21,22), four MS

(13,14,23,24), one PD (15), one amyotrophic lateral sclerosis

(ALS) (25), and one myasthenia gravis (MG) (26).

Characteristics of studies

All of the studies were RCTs, which investigated RMT in neu-

rological subjects. The duration of the interventions varied

between studies and ranged from six-weeks to 12 weeks

(Table 2). Six studies performed IMT, two EMT, and one

studied combined IMT with diaphragmatic breathing and

pursed lip breathing; the intensity and duration of training

sessions is listed in Table 2.

The median methodological score of all studies was 3

(range 1 to 5). Three trials (13,14,23) scored less than 3, indi-

cating low methodological quality with the remainder being

good methodological quality. All trials were described as ran-domized; however, only two were classified as low risk of bias

(22,25) with the rest being unclear, except Fry et al. (13),

which was classified as high risk as randomization was based

on the date of recruitment. Three studies were double-blinded

(15,21,25). Where dropouts occurred, explanation was given

in all studies with outcome data always being reported.

Effect of intervention

All nine studies reported PImax in a total of 103 neurological

subjects and 100 healthy controls. Overall postintervention,

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PImax was significantly greater in the neurological patients

than in the control subjects (WMD 694 cmH2O, 95 % CI 284

to 1104, P= 00009; Fig. 2). The stroke subjects showed a

significant improvement compared with controls with RMT

(WMD 693 cmH20, 95% CI 176 to 1209, P=0009), whereas

no difference was found between MS and the control subjects.

As only one study investigated PD, ALS, and MG patients each,they could not be assessed individually. Two studies per-

formed EMT (14,24), which showed no difference in PImax

between groups (P=093), while the remaining studies, all

using IMT, showed a significantly greater increase in neuro-

logical subjects (WMD 839 cmH2O, 95% CI 390 to 1287,

P =00002).

In total, seven trials reported PEmax in 84 neurological

and 81 control subjects. Overall, there was no difference in

PEmax values recorded in neurological and control subjects

(P=045). In the MS patients, there was no effect of RMT on

PEmax (P=091), while lack of studies did not allow this to be

tested in other neurological conditions (Fig. 3). Analysis of the

two studies where EMT was performed showed no differencebetween groups in PEmax (P= 040). The same results for

studies performing IMT (P =022) were recorded.

Adverse events

In one study, it was reported that one subject suffered

from light headedness at the start of the intervention (13).

Two further studies explicitly stated that no adverse events

occurred (23,25). It is unknown if this repeated in the remain-

ing studies.

Discussion

Pooled data from existing studies suggest that respiratory

muscle strength is decreased after stroke by 4139 and

5462 cmH2O for PImax and PEmax, respectively. There is

some evidence that RMT may improve inspiratory but not

expiratory muscle strength in stroke survivors, with PImax, on

average, increasing by 693 cmH2O. Limitations of current

studies include the paucity of studies in the area,small samples

sizes and heterogeneity in patient selection, study design,

interventions, and outcome measurement. Although evidence

suggests that respiratory muscle weakness may contribute to

increased chest infections (4,7), no studies have assessed

whether RMT is clinically meaningful or makes a difference to

clinical outcomes.

Inspiratory and expiratory muscle weakness has a serious

impact on cough function. Inspiratory muscle weakness leads

to a reduced lung volume at the beginning of a cough and

expiratory muscle weakness leads to reduced intrathoracic

pressure needed to produce adequate airflow (27). Inspiratory

and expiratory muscle strength after acute stroke is approxi-

mately half of that recorded in healthy age-matched controls,

and studies show PImax values of considerably less than

80 cmH2O, the threshold for clinically meaningful weaknessTable

1

Characteristicsandoutcomes

ofstudiesassessingrespiratorymusclestrengt

h

Study

Group

n

Age(years)

Gender

(m:f)

Stroke

side(R:L)

D

aysafter

onset

PImax

(cmH2O)

PEmax

(cmH2O)

Other

Harrafetal.(2008)(12)

stroke

15

689(98)

7:8

8(5)

367(282)

626(28)

PgasrecordedafterTMSofinjuredsidewassignificantlylower

thantheuninjuredside.

Nodifferencebe

tweenstrokeand

controlinTwT10Pgas

control16

758(7)

8:8

758(195)*

1027(30)*

Laninietal.(2003)(9)

stroke

8

519(102)

8:0

4:4

30(12)

5343(214)

616(16)

Noasymmetryinchestwallkinematicsofcontrols.

Duringquiet

breathing,nodifferencebetweenparetic

andhealthysidein

strokepatients,althoughpareticsidemovementdecreased

duringvoluntaryhyperventilation

control

9

467(121)

9:0

994(84)*

1218(181)*

Teixeira-Salmelaetal.

(2005)(20)

stroke

16

5837(1547)

8:8

10:6

>

273

7362(206)

8944(4127)

Tidalvolume,minuteventilation,andrespiratoryratearesimilar

betweenthegroups.Greaterinvolvementinribcagebutlower

abdomenmovementinthestrokepatientsduringbreathing

control19

6021(447)

9:10

9921(2905)*

13416(5676)*

Wardetal.(2010)(5)

stroke

18

62(15)

11:7

9:9

6(3)

389(251)

525(874)

TwT10Pgassimilarbetweenthegroups.Vo

luntaryandreflex

coughpeakflowratesimpairedinstroke.

Pgaswasdecreased

duringvoluntarybutnotreflexcoughinstrokesubjects

control20

56(16)

15:5

951(33)*

1087(1659)*

*Significantlygreaterthanstrokegrou

p(P 80 cmH2O is still not achieved at nine-months

poststroke (20).

The findings of this review need to be interpreted in the

context of the limitations of studies included. A major limi-

tation, common to all studies, is the method used to assess

respiratory muscle strength. PImax and PEmax are volitional

tasks, which require maximum effort from the subject. Hence,

it is likely to be influenced by subjects motivation and alert-

ness as well as their ability to make an airtight seal around the

Fig. 1 Comparison of PImax and PEmax in stroke patients and control subjects.

Fig. 2 Comparison or PImax values for neurological and control subjects after RMT.

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mouthpiece of the measuring device. Many studies did not

control for practice effects in using measurement devices or

difference in contact time between intervention and control

groups.RMT improves respiratory muscle strength, but training

appears to be task-specific and improvements in PImax

(13,15,2123,25,26) or PEmax (14,24) were seen depending

whether training was aimed toward inspiratory or expiratory

muscle function, respectively. The duration of training ranged

from six-weeks to 12 weeks, the number of sessions from three

daily to one session performed three-days per week, and the

duration of training sessions from five-minutes to 30 mins

(Table 2). Only four studies monitored compliance with train-

ing schedules (13,21,23,25). Training tended to be performed

between 30% and 60% of maximum inspiratory and expira-

tory pressure; however, how this was altered or progressed in

each study varied markedly (Table 2). A number of studies

increased training loads based on the baseline measurements

of PImax/PEmax, and two studies altered training intensity

based on the rate of perceived exertion during training

(13,23). Only four studies had control groups that followed

the same training protocol but at lower pressure thresholds

(14,15,21,25). In the remaining studies, the control group was

sedentary (13,22,23) or instructed to perform nonspecific

breathing exercises (24,26).

Although various measures of functional status, fatigue

severity, and quality of life were used, measurement of these

was variable and did not allow meta-analysis to be performed.

Aspiration risk or cough function was not assessed in any

intervention study. None of the studies reported adverse

events associated with RMT despite the theoretical risks ofelevated thoracic pressures or repeated Valsalvas maneuvers

in patients with stroke and cardiovascular comorbidities.

Conclusion

Good evidence exists that respiratory muscle strength is

significantly impaired after stroke because of decreased

corticorespiratory outflow from the damaged cortex. This has

also been shown to result in a weak cough, with decreased

ability to clear airways and increased risk of chest infections.

Extrapolation of findings from studies in other neurological

diseases suggests that RMT may improve respiratory function

in stroke patients, but this remains to be proven and its clinical

benefits remain unknown. The review identified several meth-

odological challenges, which need to be met when designing

intervention studies to assess the effectiveness of RMT in

stroke patients.

Acknowledgements

This paper presents independent research funded by the

National Institute for Health Research (NIHR) under its

Research for Patient Benefit (RfPB) Programme (Grant

Fig. 3 Comparison of PEmax values for neurological and control subjects after RMT.

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Reference Number PB-PG-0408-16096). The views expressed

are those of the author(s) and not necessarily those of the

NHS, the NIHR or the Department of Health.

References

1 WolfeCD, Rudd T.The Burdenof Stroke White Paper. London, StrokeAlliance for Europe (SAFE), 2007.

2 Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R.

Dysphagia after stroke: incidence, diagnosis, and pulmonary com-

plications.Stroke2005;36:275663.

3 Mann G, Hankey GJ, Cameron D. Swallowing disorders following

acute stroke: prevalence and diagnostic accuracy. Cerebrovasc Dis

2000;10:3806.

4 Smith Hammond CA, Goldstein LB, Horner RDet al. Predicting

aspiration in patients with ischemic stroke: comparison of clinical

signs and aerodynamic measures of voluntary cough. Chest 2009;

135:76977.

5 Ward K, Seymour J, Steier Jet al. Acute ischaemic hemispheric stroke

is associated withimpairment of reflex in addition to voluntary cough.

Eur Respir J2010;36:138390.

6 Smith Hammond CA, Goldstein LB, Zajac DJ, Gray L, DavenportPW, Bolser DC. Assessment of aspiration risk in stroke patients with

quantification of voluntary cough.Neurology2001;56:5026.

7 Addington WR, Stephens RE, Gilliland KA. Assessing the laryngeal

cough reflex and the risk of developing pneumonia after stroke: an

interhospital comparison.Stroke1999;30:12037.

8 Lasserson D, Mills K, Arunachalam R, Polkey M, Moxham J, Kalra L.

Differences in motor activation of voluntary and reflex cough in

humans.Thorax2006;61:699705.

9 Lanini B, Bianchi R, Romagnoli I et al. Chest wall kinematics

in patients with hemiplegia. Am J Respir Crit Care Med2003; 168:

10913.

10 Cohen E, Mier A, Heywood P, Murphy K, Boultbee J, Guz A.

Diaphragmatic movement in hemiplegic patients measured by

ultrasonography.Thorax1994;49:8905.

11 Newham DJ, Hsiao S-F. Knee muscle isometric strength, voluntary

activation and antagonist co-contraction in the first six months after

stroke.Disabil Rehabil2001;23:37986.

12 Harraf F, Ward K, Man W et al. Transcranial magnetic stimulation

study of expiratory muscle weakness in acute ischemic stroke.Neuro-

logy2008;71:20007.

13 Fry DK, Pfalzer LA, Chokshi AR, Wagner MT, Jackson ES. Rand-

omized control trial of effects of a 10-week inspiratory muscle training

program on measures of pulmonary function in persons withmultiple

sclerosis.J Neurol Phys Ther2007;31:16272.

14 Smeltzer SC, Levietes MH, Cook SD. Expiratory training in multiple

sclerosis.Arch Phys Med Rehabil1996;77:90912.

15 Inzelberg R, Peleg N, Nisipeanu P, Magadle R, Carasso RL, Weiner P.

Inspiratory muscle training and the perception of dyspnea in Parkin-

sons disease.Can J Neurol Sci2005;32:2137.

16 Higgins J, Altman D, Sterne J. Chapter 8: assessing risk of bias in

included studies; in Higgins J, Green S (eds): Cochrane Handbook for

Systematic Reviews of Interventions Version 510 (Updated March

2011). The Cochrane Collaboration, 2011. Available at http://www.

cochrane-handbook.org

17 Jadad AR, Moore RA, Carroll Det al. Assessing the quality of reports

of randomized clinical trials: is blinding necessary?Control Clin Trials

1996;17:112.

18 Hozo S, Djulbegovic B, Hozo I. Estimating the mean and variance

from the median, range, and the size of a sample. BMC Med Res

Methodol2005;5:13.

19 Higgins J, Deeks J, Altman D. Chapter 16: special topics in statistics;

in Higgins J, Green S (eds): Cochrane Handbook for Systematic

Reviews of Interventions Version 510 (updated March 2011). The

Cochrane Collaboration, 2011. Available at http://www.cochrane-

handbook.org

20 Teixeira-Salmela LF, Parreira VF, Britto RRet al. Respiratory pressures

and thoracoabdominal motion in community-dwelling chronic stroke

survivors.Arch Phys Med Rehabil2005;86:19748.

21 Britto RR, Rezende NR, Marinho KC, Torres JL, Parreira VF, Teixeira-

Salmela LF. Inspiratory muscular training in chronic stroke survivors:

a randomized controlled trial.Arch Phys Med Rehabil2011; 92:18490.

22 Sutbeyaz ST,Koseoglu F, Inan L, Coskun O. Respiratory muscle train-

ing improves cardiopulmonary function and exercisetolerancein sub-

jects with subacute stroke: a randomized controlled trial.Clin Rehabil

2010;24:24050.

23 Klefbeck B, Hamrah Nedjad J. Effect of inspiratory muscle training

in patients with multiple sclerosis. Arch Phys Med Rehabil 2003;

84:9949.

24 Gosselink R, Kovacs L,Ketelaer P, Carton H, Decramer M. Respiratory

muscle weakness and respiratory muscle training in severely disabled

multiple sclerosis patients.Arch Phys Med Rehabil2000;81:74751.

25 Cheah BC, Boland RA, Brodaty NEet al. Inspirational inspiratory

muscle training in amyotrophic lateral sclerosis. Amyotroph Lateral

Scler2009;10:38492.

26 De Freitas Fregonezi GA, Resqueti VR, Guell R, Pradas J, Casan P.

Effects of 8-week, interval-based inspiratory muscle training and

breathing retraining in patients with generalized myasthenia gravis.

Chest2005;128:152430.

27 McCool FD. Global physiology and pathophysiology of cough.Chest

2006;129(1 Suppl.):48S53S.

28 American Thoracic Society/European Respiratory Society. ATS/ERS

statement on respiratory muscle testing.Am J Respir Crit Care Med

2002;166:518624.

Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Fig. S1 Flow diagram of the review process with reasons for

article exclusion for review 1.

Fig. S2 Flow diagram of the selection process for articles in

review 2.

Please note: Wiley-Blackwell are not responsible for the

content or functionality of any supporting materials supplied

by the authors. Any queries (other than missing material)

should be directed to the corresponding author for the article.

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Respiratory muscle strength and training in stroke and neurology: a systematic review

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