Respiratory muscle weakness and respiratory muscle training in severely disabled multiple sclerosis

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Respiratory Muscle Weakness and Respiratory Muscle Trainingin Severely Disabled Multiple Sclerosis Patients

Rik Gosselink, PhD, Ludwig Kovacs, PT, Pierre Ketelaer, MD, Herwig Carton, PhD, Marc Decramer, PhD

ABSTRACT. Gosselink R, Kovacs L, Ketelaer P, Carton H,Decramer M. Respiratory muscle weakness and respiratorymuscle training in severely disabled multiple sclerosis patients.Arch Phys Med Rehabil 2000;81:747-51.

Objective: To evaluate the contribution of respiratory muscleweakness (part 1) and respiratory muscle training (part 2) topulmonary function, cough efficacy, and functional status inpatients with advanced multiple sclerosis (MS).

Design: Survey (part 1) and randomized controlled trial(part 2).

Setting: Rehabilitation center for MS.Patients: Twenty-eight bedridden or wheelchair-bound MS

patients (part 1); 18 patients were randomly assigned to atraining group (n 9) or a control group (n 9) (part 2).

Intervention: The training group (part 2) performed three

series of 15 contractions against an expiratory resistance (60%maximum expiratory pressure [PEmax]) two times a day,whereas the control group performed breathing exercises toenhance maximal inspirations.

Main Outcome Measures: Forced vital capacity (FVC),inspiratory and expiratory muscle strength (PImax and PEmax),neck flexion force (NFF), cough efficacy by means of thePulmonary Index (PI), and functional status by means of theExtended Disability Status Scale (EDSS).

Results: Part 1 revealed a significantly reduced FVC(43% 26% predicted), PEmax (18% 8% predicted), andPImax (27% 11% predicted), whereas NFF was only mildlyreduced (93% 26% predicted). The PI (median score, 10) andEDSS (median score, 8.5) were severely reduced. PEmax wassignificantly correlated to FVC, EDSS, and PI (r .77, .79,

and

.47, respectively). In stepwise multiple regression analy-sis, PEmax was the only factor contributing to the explainedvariance in FVC (R2 .60), whereas body weight (R2 .41)was the only factor for the PI. In part 2, changes in P Imax andPEmax tended to be higher in the training group ( p .06 andp .07, respectively). The PI was significantly improved after3 monthsof training compared with the control group ( p .05).After 6 months, the PI remained significantly better in thetraining group.

Conclusions: Expiratory muscle strength was significantlyreduced and related to FVC, cough efficacy, and functionalstatus. Expiratory muscle training tended to enhance inspiratoryand expiratory muscle strength. In addition, subjectively and

objectively rated cough efficacy improved significantly andlasted for 3 months after training cessation.Key Words: Multiple sclerosis; Respiratory function tests;

Rehabilitation; Respiratory muscles; Training.

2000 by the American Congress of Rehabilitation Medi-cine and the American Academy of Physical Medicine andRehabilitation

MULTIPLE SCLEROSIS (MS) is a primary disorder of thecentral nervous system that may affect motor pathwaysand cause muscle weakness. Recent reports address the impor-tance of respiratory muscle weakness in these patients.1-3

Respiratory complications are common in the terminal stages ofMS and contribute to mortality in these patients.4-6 Whenrespiratory motor pathways are involved, respiratory muscle

weakness frequently occurs in MS and may impair the perfor-mance of coughing. Aspiration, pneumonia, or even acuteventilatory failure may ensue.

Because pulmonary complications contribute importantly tomorbidity and mortality in MS,7 it appears worthwhile to studyrespiratory muscle function and its relationship with forcedvital capacity (FVC), cough efficacy, and functional status. Inaddition, strategies to improve respiratory muscle function arelikely to be important in reducing deterioration of pulmonaryfunction and perhaps in improving cough efficacy and survival.

The first part of the study was thus designed to examine thecontribution of respiratory muscle weakness to this impairedpulmonary function and health status. It was concluded thatexpiratory muscle strength was more affected than inspiratorymuscle strength. In addition, expiratory muscle weakness wassignificantly related to FVC, cough efficacy, and functionalstatus. Because of the observed expiratory muscle weaknessand its relationship to FVC and cough efficacy, the second partof the study was performed to investigate the effects ofexpiratory muscle training on respiratory muscle function,FVC, and cough efficacy.

MATERIALS AND METHODS

Part 1

Twenty-eight bedridden or wheelchair-bound MS patients(mean age, 58 14yrs; mean duration of the disease,27 13yrs) were studied to examine the contribution ofrespiratory muscle weakness to their impaired health status.FVC, inspiratory and expiratory muscle strength (PImax and

PE

max), Pulmonary Index (PI), and Extended Disability StatusScale (EDSS) were measured. All patients were in a clinicallystable condition for at least 4 weeks (no recent infection orexacerbation). All tests were performed in the early afternoon.Data are summarized in table 1.

Part 2

Twenty-one bedridden or wheelchair-bound MS patientswere included in the second part of the study to evaluate theeffects of expiratory muscle training on FVC, PImax andPEmax, and the PI (table 2). Power analysis based on the results

From the Respiratory Rehabilitation and Respiratory Division, University Hospi-

tals, Katholieke Universiteit Leuven, and Faculty of Physical Education and Physio-therapy, Katholieke Universiteit Leuven, Leuven (Gosselink, Decramer, Kovacs); andthe National Multiple Sclerosis Centre Melsbroek (Ketelaer, Carlton), Belgium.

Submitted July 6, 1999. Accepted November 18, 1999.Supported by the Fonds voor Wetenschappelijk OnderzoekVlaanderen, grant P.

0188.97.No commercial party having a direct financial interest in the results of the research

supporting this article has or will confer a benefit upon the authors or upon anyorganization with which the authors are associated.

Reprint requests to Rik Gosselink, PhD, Professor of Respiratory Rehabilitation,Division of Respiratory Rehabilitation, University Hospital Gasthuisberg, Herestraat49, 3000 Leuven Belgium.

0003-9993/00/8106-5720$3.00/0doi:10.1053/apmr.2000.5616

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of Smeltzer and coworkers8 showed that at least 5 patients wereneeded in each group. Because our patient group was moreseverely disabled, we included 21 patients. Three patientsdropped out from the study because of lack of cooperation.Patients were randomized by random numbers in sets of 10patients. The patients in the training group (n 9) performedthree series of 15 expiratory contractions (60% PEmax) with theThresholda adapted for expiratory loading two times a day. Thecontrol group (n 9) was instructed to perform breathingexercises to enhance maximal inspirations. These breathingexercises were routinely part of the physiotherapy treatment inthe MS center. No specific feedback was given to the controlgroup, and the breathing exercises were not supervised. Forthese reasons we considered this a control treatment. Themeasurements were repeated after 3 months of training and 3months after the training period.

The study was approved by the Medical Ethical Board of theNational Multiple Sclerosis Centre Melsbroek.

Pulmonary function test. All patients underwent spirom-etry in the sitting position with determination of the FVC

(Ohmeda 5420 Volume monitorb). Spirometry was repeateduntil no further improvement of recordings was obtained.Sufficient rest periods were left between tests until the patientsrespiratory rates were back to baseline and their subjectivefeeling was that they could continue. The highest value

obtained was related to the normal values of Quanjer andcolleagues.9

Anthropometric data. Body weight and height were takenfrom recent patient records. Body mass index was calculated asthe ratio of body weight and height squared (kg/m2).

Respiratory muscle strength. All patients underwent deter-mination of PImax and PEmax. These pressures were measuredwith a portable electronic manometer (Mouth pressure devi-cec).10 A mouthpiece or, in patients with more severe weakness,

a face mask was held firmly over the mouth and nose of thepatient by the investigator to prevent air leaking. PImax wasmeasured from residual volume (RV), whereas PEmax wasmeasured near total lung capacity (TLC). Tests were repeateduntil no further improvement was obtained and at least threeattempts differed less than 5%. Sufficient rest periods wereprovided between tests until patients respiratory rates wereback to baseline and their subjective feeling was that they couldcontinue. The highest values were taken for analysis.

Isometric hand-held dynamometer (MicroFETd) measure-ments of neck flexion force (NFF) were performed according tovan der Ploeg and associates.11 The measurements were relatedto their reference values.11

Cough efficacy and functional status. The PI12 was used toassess objectively and subjectively rated cough efficacy. Scores

range from 4 to 11; a score of 4 indicates normal cough efficacy,whereas a score of 11 is the most abnormal cough efficacy. Theimpact of the neurologic disorder on functional status wasassessed with the EDSS.13 Scores range from 0 to 10; a score of0 indicates no disability; 5, ambulatory without assistance; 8,wheelchair bound or bedridden; and 10, dead.

Statistics. Statistical analysis was performed on the dataobtained from the 28 patients who participated in part 1 of thestudy and from the 18 patients who participated in part 2.Pearsons correlation coefficients between variables were calcu-lated. For the variables significantly related to FVC, PI, andfunctional status, a stepwise multiple regression analysis wasperformed. Variables used in the model included age, gender,body weight, height, duration of illness, respiratory musclefunction, and pulmonary function. Only variables significantlycontributing in single correlation were retained.

Comparison between the control group and training groupwas done with unpaired t tests. Within-group comparison wasperformed with paired ttest analysis. All statistical analysis wasperformed using SAS statistical package.e Limits of signifi-cance were set as p .05.

RESULTS

Part 1

Pulmonary function, cough efficacy, and functional status.A significantly reduced FVC (1.4 0.9L, 43 26% predicted)was observed. The median PI score was 10 (ranging from 6 to11) indicating severely impaired cough efficacy. The highmedian score on the EDSS (8.5, ranging from 6.5 to 9.5) (table1) confirmed the markedly reduced mobility of the patients,

nearly all being wheelchair bound or bedridden.Respiratory muscle strength. The PEmax (29 15cmH2O,

18 8% predicted) was significantly more reduced than thePImax (25 14cmH2O, 27 11% predicted) ( p .01). Meanisometric neck flexion strength was only mildly reduced(93 36N, 93 26% predicted). Two patients failed to per-form a proper inspiratory and expiratory maneuver, whereas inseven patients one of the maneuvers was impossible to perform.Three patients failed inspiratory pressure measurement, andfour failed expiratory pressure measurement. The FVC in theseseven patients was significantly lower compared with those

Table 1: Patient Characteristics in Part 1

Male/Female 13/15

Bedridden/Wheelchair 11/17

Age (yrs) 58 14

Height (cm) 167 8

Weight (kg) 59 12

BMI (kg/m 2) 22 8

Illness duration (yrs) 27 13

EDSS (score)* 8.5 (6.5-9.5)

Pu lm on ar y Ind ex (scor e)* 10 (6-11)

FVC, L (%pred) 1.43 0.9 (43 26)

PImax, cmH2O (%pred) 25 14 (27 11)

PEmax, cmH2O (%pred) 29 15 (18 8)

Neck flexion, N (%pred) 93 36 (93 26)

Values are expressed as m ean SD or as * median (range).Abbreviations: BMI, body mass index; EDSS, Extended DisabilityStatus Scale; FVC, forced vital capacity; PImax, maximum inspiratorypressure; PEmax, maximum expiratory pressure.

Table 2: Patient Characteristics of the Control Group and theTraining Group in Part 2

Control (n 9) Training (n 9)

Male/Female 3/6 6/3

Age (yrs) 59 14 54 13

Height (cm) 165 5 170 10

Weight (kg) 58 10 62 15

BMI (kg/m2) 21 8 23 10

Il lness durat ion (yrs) 31

13 24

15EDSS (score)* 8.5 (8-9.5) 8 (7-9)

Pul monary In dex (score)* 10 ( 8-11) 10 ( 6-11)

FVC, L (%pred) 1.11 .52 (35 15) 1.88 1.13 (50 29)

PImax,cmH2O (%pred) 22 10 (26 6) 27 18 (26 16)

PEmax,cmH2O (%pred) 24 7 (17 3) 31 21 (17 10)

Values are expressed as mean SD or as * median (range). Nostatistically significant differences were observed between the con-trol group and the training group.Abbreviations: BMI, body mass index; EDSS, Extended DisabilityStatus Scale; FVC, forced vital capacity; PImax, maximum inspiratorypressure; PEmax, maximum expiratory pressure.

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who were able to perform the respiratory pressure maneuvers(19 8 vs 50 26% predicted, p .01).

Correlation analysis. The EDSS was significantly corre-lated to FVC (% predicted) (r.87, p .001), PEmax (%predicted) (r.79, p .001) (fig 1), and the PI (r .45,p .05). The PI was significantly correlated with body weight(r.64, p .001), PEmax(% predicted)(r.47, p .02),and FVC (% predicted) (r.36, p .05). The FVC (%predicted) was significantly correlated with PEmax (% pre-

dicted) (r .77, p .001) (fig 2), NFF (% predicted) (r .56,p .005), and PImax (% predicted) (r .48, p .01). Instepwise multiple regression analysis, PEmax was the onlyfactor contributing to explained variance in FVC (R2 .60),whereas body weight (R2 .41) was the only factor for the PI.

Part 2

Patient characteristics between training and control groupsdid not differ initially (table 2). The PImax was significantlyimproved after 3 months of training compared with baseline(9 9cmH2O, p .05), but not compared with the controlgroup ( p .06, table 3). Changes in PEmax were higher in thetraining group, but the improvement failed to reach statisticalsignificance compared with baseline (8 14cmH2O, p .08)as well as compared with the changes in the control group

( p .07). In addition, the PI improved significantly comparedwith baseline and with the control group ( p .05). Nosignificant changes were observed in pulmonary function(0.2 0.5L, p .41). Subgroup analysis showed that theimprovement in PImax in the training group was significantlyassociated with the initial EDSS (r.76, p .02; fig 3).

After 6 months, the PI remained significantly better in thetraining group ( p .05), whereas the improvements of PImaxtended to be higher, but failed to reach statistical significance( p .16).

DISCUSSION

It was concluded from the first part of the study that inwheelchair-bound and bedridden MS patients, expiratory muscle

strength was more affected than inspiratory muscle strength.Expiratory muscle strength was significantly related to FVC,cough efficacy, and functional status.

From the second part of the study, it was concluded thatexpiratory muscle training tended to enhance both inspiratoryand expiratory muscle strength and significantly improved theobjectively and subjectively rated cough efficacy, which lastedfor 3 months after training cessation.

Criticism of the Methods

The assessment of FVC and respiratory muscle strength iseffort and motivation dependent. Leakage during the maneuvers

was prevented by the use of a face mask, which was held firmlyby the investigator. Maneuvers were repeated until no furtherimprovement was observed. Although careful instruction wasgiven and patients were well motivated, full cooperation withtests was in some patients very difficult. In particular, timing ofthe onset of the maneuvers was sometimes difficult. Somepatients failed to follow specific instructions to perform maxi-mal inspiratory or expiratory mouth pressures at a specific lungvolume (RV or TLC). In seven patients, all with a FVC below600mL, data on PImax or PEmax were missing because of aninability of the patient to perform the test. Values below7cmH2O were not accepted by the mouth pressure measurement

Fig 1. Relation between expiratory m uscle strength (PEmax), mea-sured as percentage predicted (% pred) and Extended DisabilityStatus Score (EDSS).

Fig 2. Relation betw een expiratory muscle strength (PEmax), mea-

sured as percentage predicted (% pred), and forced vital capacity(FVC).

Table 3: Changesat 3 and 6 M onths After Training

Cont rol Gr oup Tr ai ning Grou p

3m o 6m o 3m o 6m o

VC (%init) 5 35 12 37 25 63 21 57

PIm ax (%i ni t) 11 36 12 21 39 41 31 35

PEmax (%init) 4 26 1 24 30 46 9 25

Pulmonary

Index* 0 1 0 1 2 1 1 1

Values are expressed as m ean SD.Abbreviations: VC, vital capacity; PImax, maximum inspiratory pres-sure; PEmax, maximum expiratory pressure.* Changes in absolute values; p .05; p .07 compared withcontrols; p .05; p .08 compared w ith b aseline.

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device. Therefore, the observed respiratory muscle weaknessmight have been underestimated.

The effects of inspiratory muscle training might have beenstudied in more detail when TLC and RV were measured.However, a body plethysmograph was not available in thecenter where the patients were hospitalized. Obviously, bedrid-den patients would be unable to perform these tests.

Respiratory Muscle Dysfunction, Impaired FVC,

and Cough Efficacy

Expiratory muscles were more affected than inspiratorymuscles, as observed previously.1,3,12,14,15 Obviously, the demy-elinating process affected abdominal muscles more than inspira-tory muscles. Neck flexors, acting as accessory inspiratorymuscles, had preserved strength but could not compensate forthe obvious weakness of primary inspiratory muscles. Thereduced inspiratory muscle strength is partly explained by theincreased RV. Consequently, the PImax maneuver was per-formed with the inspiratory muscles operating at a shorterlength, thereby reducing the force-generating capacity. Inaddition, deconditioning might also contribute to respiratorymuscle weakness.16-18 This studys findings were in agreementwith previous findings of the positive relationship betweenexpiratory muscle strength, and EDSS and pulmonary func-tion.12 Pulmonary function was also related to EDSS.1,3

Expiratory muscle weakness is associated with difficulty incoughing in neuromuscular disorders,12,19,20 shown by thesignificant correlation between PEmax and PI. The relationshipwas weaker than that observed by Smeltzer and associates,12

but their study also included patients with mild disease.Obviously, our patients had more severe disability as illustratedby the high EDSS (median 8.5 vs 7.0 in the study by Smeltzer).

The association between PI and body weight might be ex-plained by disease severity, which might be reflected in bodyweight due to loss of muscle mass, malnutrition, and cachexia.

Respiratory Muscle Training

The observed tendencies of enhanced respiratory musclefunction in the training group might be influenced by thesomewhat better baseline characteristics of the training group.Although no statistically significant differences were observedbetween both groups, the training group was somewhat youn-ger, had a better preserved FVC and respiratory muscle

function, and had 7 years less history of MS. These factorscould have contributed to somewhat more reserve to obtaintraining effects. We were, however, unable to identify cleardifferences in baseline patient characteristics between respond-ers (those with improved respiratory muscle function) andnonresponders. Only a reduced training response of PImax wasassociated with a higher EDSS (fig 2).

Our results differ in some respect with those of Smeltzer etal.8 The relative improvement in PEmax (35%) was similar, but

our results did not reach statistical significance ( p .08). Incontrast to the tendency of an improvement of PImax in thisstudy, Smeltzer observed only a marginal, nonsignificant in-crease of PImax (6%). These differences might be explained bydifferences in patient population, training protocol, or both. Thepatients in Smeltzers study had a shorter duration of disease(14 vs 27yrs), probably a lower EDSS score (range, 6.5 to 9.5;median score not reported), and substantially higher respiratorypressures (PImax 47% predicted, PEmax 37% predicted). Expi-ratory muscle loading protocol in our study was set at 60% ofPEmax and a low repetition number was chosen, as strengthrather than endurance capacity was aimed to improve. Effectivecoughing needs explosive expiratory muscle contraction. Smelt-zer8 aimed at a similar high-intensity protocol, but the obtainedintensity was not reported. It is not likely that the training

intensity in our study was too low, because subjectively ourpatients experienced a high training intensity. The lack ofsignificance might be caused by the very low expiratory musclestrength (18% predicted), probably indicating severe expiratorymuscle impairment and reduced trainability. We speculate thatthe poor training response of the expiratory muscles might berelated to the severity of the demyelination process. Demyelin-ation of the central nervous system might affect the innervationof expiratory muscles, thus reducing the force-generatingcapacity of the expiratory muscles.

An alternative explanation for the improved inspiratorymuscle strength is a reduction of RV. Expiratory muscle trainingmight have reduced expiratory lung volume, thus allowing theinspiratory muscles to operate at a more advantageous part ofthe length-tension relationship. Unfortunately data on RV were

not available, but the absence of a relationship between changesin FVC and changes in respiratory muscle function makes thisassumption unlikely.

The tendency of an improvement of PImax as a result ofexpiratory muscle training was surprising. We speculate thatduring expiratory loading, in the absence of sufficient expira-tory muscle strength, patients increased their inspiratory lungvolumeandhence, elastic recoilpressureto overcome theexpiratorypressure. This stimuluswas probably high enoughto cause a trainingresponse of the inspiratory muscles. Alternatively, a decrease of RVcaused by expiratory muscle training might put the inspiratorymuscles on a more advantageous part of their length-tensionrelationship. Because measurements of TLC and RV were notperformed, only speculations can be made.

Interestingly, in addition to improved respiratory muscle

function, FVC did not change significantly. This conclusionfollows the findings of the uncontrolled study by Olgiati andcoworkers.21 As expected in patients of Olgiatis study who hadonly moderate muscle weakness, vital capacity remains un-changed.22 However, our study included patients with severerespiratory muscle weakness, and accordingly a restrictivepulmonary dysfunction. Improvement of PImax and PEmax wasexpected to be associated with a proportional lung volumeincrease in patients with severe muscle weakness. The lack ofimprovement might perhaps also be explained by the absence ofspecificity of respiratory muscle training. We have no data on

Fig 3. Relation bet ween changes in maximal inspiratory pressure(PImax), measured as percentage predicted (% pred), after trainingand the initial Expanded Disability Status Score (EDSS) in thetraining group.

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the actual lung volumes during expiratory muscle training, butwe might speculate that these were not adequate to improvelung function. Inspiratory muscles need to be trained near TLCto improve inspiratory capacity, whereas expiratory musclesneed training near RV to enhance expiratory capacity. Inspira-tory muscles were probably loaded near TLC, but training wasnot targeted at these muscles. Expiratory muscles were notloaded near RV, but probably near TLC.

The PI decreased significantly indicating improved cough

efficiency. This was not studied in previous studies, but seemsimportant because it may contribute to a reduced incidence ofpulmonary complications. Importantly, this improvement wasmaintained during the follow-up period. Our follow-up was tooshort to obtain reliable results on the incidence of pulmonarycomplications. In addition, we were unable to reconstructreliable data from the period before the study period frompatient records. Future studies in patients with severe MSshould focus on inspiratory muscle training. Enhancing inspira-tory reserve volume increases elastic recoil pressure andalveolar pressure, which might contribute to improved coughefficacy and prevent pulmonary complications. Improvement ofinspiratory muscle function might be obtained through inspira-tory resistive training or through the use of incentive spirom-etry. Incentive spirometry may load the inspiratory muscles

near TLC, but has the disadvantage that the actual trainingintensity is not known. Inspiratory muscle training allowsaccurate control of the actual training intensity.

In conclusion, expiratory muscle strength was significantlyreduced and related to FVC, cough efficacy, and functionalstatus. Expiratory muscle training tended to enhance inspiratoryand expiratory muscle function. In addition, subjectively andobjectively rated cough efficacy improved significantly andlasted for 3 months after training cessation.

Acknowledgments: The authors gratefully thank Mrs.R. Schepersfor her expert help with statistical analysis, and Mrs. V. Debusschere,G. DeDekker, and N. Demolon for their assistance in data collectionand supervision of the training.

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Suppliersa. Healthscan Products Inc., 908 Prompton Ave, Cedar Grove, NJ

07009-1292.b. Ohmeda BOC Healthcare, Louisville, KY 80027.c. Precision Medical Ltd., Thornton Rd, North Yorks YO18 7JB, UK.d. Hoggan Health Industries, Biometrics Europe, Kabelstraat 11 1322

AD Almere, The Netherlands.

e. SAS Institute Inc., SAS Campus Dr, Cary, NC 27513.

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Respiratory muscle weakness and respiratory muscle training in severely disabled multiple sclerosis