DOI 10.1378/chest.113.4.900 1998;113;900-905Chest

 VarrayIsabelle Serres, Véronique Gautier, Christian Préfaut and Alain Lung Function in COPD Patients

AlteredRelated to Physical Inactivity and Impaired Skeletal Muscle Endurance

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Impaired Skeletal Muscle EnduranceRelated to Physical Inactivity andAltered Lung Function in COPDPatients*Isabelle Serres, PhD; Veronique Gautier, MD; Alain Varray, PhD; andChristian Prefaut, MD

Study objective: The aims of this work were to determine (1) whether patients with COPD haveimpaired skeletal muscle performance (ie, maximal strength and endurance) compared withhealthy subjects, and (2) whether the level of physical activity, body composition, and lungfunction are related to skeletal muscle performance in COPD patients.Methods: Seventeen COPD patients and eight healthy age-matched control subjects performedmaximum voluntary contraction (MVC) of the quadriceps and an endurance test consisting ofdynamic contractions of the quadriceps against 20% of MVC at an imposed regular pace untilexhaustion. The endurance test duration determined the muscle "limit time" (Tlim). A score ofphysical activity (PA score) was obtained using an adapted physical activity questionnaire for theelderly, and body composition was measured by the bioelectrical impedance method. Symptom-limited oxygen uptake (Vo2 si) was also assessed in COPD patients using a maximal incrementalexercise test.Results: The results showed that Tlim and PA score were significantly decreased in COPDpatients (p<0.05). Significant positive correlations were found in the COPD group between Tlimand the PA score (r=0.60; p<0.05), FEVX (r=0.52; p<0.05), and Pa02 (r=0.63; p<0.05). The same

results were found between the PA score and Vo2 si (r=0.57; p<0.05) and FEVX (r=0.63; p<0.05).Conclusion: These findings indicate impaired skeletal muscle endurance in COPD patientsrelated to altered lung function and associated physical inactivity.

(CHEST 1998; 113:900-05)

Key words: body composition; COPD; deconditioning; endurance; physical activity questionnaire; skeletal muscle;strengthAbbreviations: FFM=fat-free mass; MVC=maximum voluntary contraction; PA=physical activity; Tlim=limit time;Vo2=oxygen uptake; Vo2 sl=symptom-limited oxygen uptake

"D ecause exercise intolerance in patients with.** COPD appears to be due not only to pulmonaryobstruction but also to a combination of severalfactors,12 consideration has been given recently toskeletal muscle function. Indeed, the reduced activ¬

ity in the patient's daily life due to dyspnea may leadto deconditioning, ie, muscle function alteration.34Investigations of skeletal muscle with nuclear mag-

*From the Laboratoire de Physiologie des Interactions (Drs.Serres, Gautier, and Prefaut), Service EFR, Hopital Arnaud deVilleneuve, and the Laboratoire Sport Sante Developpement(Drs. Serres and Varray), UFRSTAPS, Montpellier, France.This work was supported by grant No. 93 1102 from InstitutNational de la Sante et de la Recherche Medicale (INSERM).Manuscript received March 11, 1997; revision accepted October8, 1997.Reprint requests: Isabelle Serres, PhD, Service EFR-Pr Prefaut,Hopital Arnaud de Villeneuve, 34295 Montpellier Cedex 5,France; email: physio.montp@hol.fr

netic resonance have shown abnormalities in musclemetabolism in these patients, indicating reducedoxidative capacity.56 Impaired muscle oxidative ca¬

pacity suggests that skeletal muscle endurance isdecreased,7 and such an alteration could explain thewell-known leg fatigue described in these patients.28A reduced maximal muscle strength was demon¬strated in COPD patients and was found to be a

significant contributor to work capacity limitation.89However, to our knowledge, no data are yet availableon skeletal muscle endurance and, for the assess¬

ment of peripheral muscle performance, isolatedmuscle strength alone is too limited. Moreover,although deconditioning has been suggested as an

explicative factor of impaired skeletal muscle func¬tion and exercise capacity in COPD patients, thelevel of daily physical activity in these patientssurprisingly has never been studied (to our knowl-

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edge),1011 nor has the possible relationships betweenthis level and peripheral muscle performance.The present study was thus undertaken to deter¬

mine (1) whether patients with COPD have im¬paired skeletal muscle performance not only in termsof maximal strength but also in terms of endurance,compared with healthy subjects; and (2) whether thelevel of physical activity (PA), body composition, andlung function are related to skeletal muscle perfor¬mance in COPD patients.

Materials and Methods

SubjectsSeventeen outpatient men with COPD (age, 62 years [SE, 2])

and eight healthy age-matched men (control group) were re¬

cruited to participate in this study. Each subject was informed ofthe purpose of the study and gave written consent. Patients wereex-smokers, had a clinical history consistent with COPD, and hadspirometric evidence of bronchial obstruction;12 respiratory im¬pairment ranged from moderate to severe according to theEuropean Respiratory Society classification.12 At the time ofthestudy, patients were in clinically stable condition with no recentinfective exacerbation and were not smokers. All received inhaledtreatment, including bronchodilators and corticoids. Subjectswith cardiovascular limitation, metabolic abnormalities, or artic¬ular dysfunction were excluded from the study.

Material and Measurements

Lung Function and Blood Gas Assessment: Lung functionstudies were done using a whole body plethysmograph (Trans¬mural Bodybox 2800; Sensormedics; Yorba Linda, Calif). Mea¬surements included FCV and FEVL. Tiffeneau's ratio (FEVX/FVC) was then calculated. The values obtained were comparedwith the normal values of Quanjer et al.13 Blood gas analyses werealso performed in the COPD patients. Arterialized blood samplesfor Pa02 and PaC02 were obtained at rest with the ear lobemicromethod (IL 1306; Milan, Italy).

Skeletal Muscle Performance Testing: We assessed maximumvoluntary contraction (MVC) and endurance of the quadricepsfor each leg using an exercise bench (Banc de Koch; GeninMedical; Les Angles, France). The apparatus for performing localmuscle exercise consists of an ankle harness attached to nonelas-tic cord connected to a minimal friction system of ball-bearingpulleys and a dynamometer or adjustable weights (Fig 1). MVCwas measured with a dynamometer. The exercise was performedwith the subject in a sitting position at 90° knee and hip flexion.With arms crossed in front of the chest and position maintained,subjects performed three brief (4 s) maximal contractions, eachseparated by 1 min of rest. If maximal values of strengthmaintained 3 s as read on the dynamometer were reproducible(<5% of variability between values), the highest value of thesethree contractions was defined as MVC. Endurance of thequadriceps was then tested on the same exercise bench accordingto the technique of Monod and Scherrer.14 The exercise protocolconsisted of extending one leg against weights corresponding to20% of MVC with a pace of 12 movements per minute imposedwith audio signal until exhaustion. The movement amplitudecorresponded to the maximal extension of the leg and was

identified before the start of the test. The duration of themovement was not imposed but it was required that subjects

Dynamometeror

Weights

&Figure 1. Diagram of the subject's position and the materialused to assess skeletal muscle performance.

release muscles just after maximal extension, without maintainingstatic contraction or resisting when weights were set back. Thus,the active part of the movement was considered to be the loadlift. The test was stopped when the subjects could no longerrespect the movement amplitude or frequency two consecutivetimes despite verbal encouragement; duration was then recorded.This duration was called "limit time" (Tlim). Subjects performedthese exercise tests for the two legs. The means of the two MVCand the two Tlim values (right and left muscle) were used foranalysis.

Level of PA: PA was assessed by using a PA questionnaireadapted for the elderly.15 The questionnaire consisted of scores

for household activities, sports activities, and other physicallyactive leisure-time activities, together resulting in an overall PAscore. Scores could not be obtained for three patients. Onepatient with depressive symptoms always responded that he hadno activity. The two other patients could not quantify theirphysically active leisure time activities according to the question¬naire.

Nutritional Assessment: Body composition was assessed by thesingle-frequency bioelectrical impedance method.16 The mea¬

surement required subjects to present with an empty stomach.After 15 min of rest in supine position, resistance (ARC 50;Eugedia; Chambly, France) was measured on the right body side.Fat-free mass (FFM) was then calculated from height2/resistanceand body weight using a patient-specific regression equationgenerated in 32 normal to underweight patients with COPD.17

Exercise Tolerance: Exercise capacity7 was assessed in COPDpatients by an incremental exercise test performed on a cycleergometer (ERG 602; DIMEQ; Berlin, Germany). Patientsbreathed through a mouthpiece with a noseclip in place. Oxygenuptake (Vo2) and carbon dioxide output were measured contin¬uously using a mass spectrometer system (Metabolic ExerciseTesting; Marquette Electronics; Milwaukee). A 12-lead ECG(Marquette Electronics) and pulse oximeter (Oxypal; NihonKohden Corporation; Tokyo, Japan) were monitored continu¬ously during exercise testing. The exercise test was performedaccording to the individualized exercise test protocol used in our

laboratory and defined as the following: first, the maximal

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predicted work rate was calculated according to the equation ofJones et al.18 This maximal value was then adapted to the patientby multiplying it by FEV1/FEV1 predicted. The 3-min warm upwas conducted at 20% of this adapted maximal work rate. Thework rate was then increased every minute. The increase rate wasdefined as 8% of the adapted maximal work rate in order toobtain the maximal work rate in about 10 min. This methodusually results in a test duration of 8 to 12 min, which meets theexercise testing recommendations.19 In our study, to ensure thatVo2 max was reached, three of the four following criteria had tobe met: (1) stability of Vo2 despite the increase in exercise

intensity; (2) attainment of age-predicted maximal heart rate

(210-0.65Xage±10%); (3) respiratory exchange ratio >1.1; and(4) inability to maintain the required pedaling frequency (50rpm) despite maximal effort and verbal encouragement. If one ofthe first three criteria was not observed, we considered that themaximal Vo2 was symptom limited (Vo2 si).

Protocol: All the experiments were performed in the morningon 2 days for the COPD group and on 1 day for the control group.Spirometric and blood gas variables, and Vo2 si were measured inCOPD patients on day L On day 2, spaced a week from day 1, theCOPD group performed the other experiments such as thecontrol group: subjects first underwent nutritional assessmentbetween 8 and 9 AM. After breakfast, spirometric variables were

measured for the control group. Subjects then were asked to

respond to the questionnaire of physical activity. At the end ofthemorning, skeletal muscle performance was assessed.

Statistical AnalysisStatistical analysis was performed using statistical software

(SigmaStat; Jandel Scientific; Erkrath, Germany). Statistical dif¬ferences between the COPD and control groups were tested byan unpaired t test. If the equal variance test failed, we used a

Mann-Whitney test. We analyzed relationships between skeletalmuscle performance (MVC and Tlim) and PA score, FFM,FEVX, and Pa02 for COPD data using the Pearson correlationanalysis, since the assumption of normal distribution was fulfilledfor all the analyzed variables. Correlation analysis was also madebetween PA score and both Vo2 si and FEV1. Statistical signifi¬cance was assumed for p<0.05. Values were expressed by theirmean and with SE.

Table 1.Characteristics of Study Population*COPD (n=17) Control (n=8)

Age, yrHeight, cmWeight, kgBMI, kg/m2FFM, kgFEV,, L

FEVl5 % predictedFEV/FVC, %Pa02, mm HgPaC02, mm HgPA score

62±2169±271±425±154±21.4±0.149±453±378+239±15±1

.t

60±4171±377±326±161±23.2±0.2103±378±3

10±2

*BMI=body mass index; values are expressed by their mean:!1 Significantly different from control value (p<0.001).Significantly different from control value (p<0.05).

SE.

(r=0.57, p<0.05), and between Vo2 si and MVC(r.0.59, p<0.05). No significant relationship was

observed between Vo2 si and Tlim (r=0.31).

Discussion

The major findings of this study are that (1)skeletal muscle endurance is impaired in COPDpatients compared with healthy subjects; and that (2)skeletal muscle endurance is associated with level ofdaily physical activity and severity of airways obstruc¬tion. To study muscle endurance, we used localmuscle exercise consisting of dynamic extension ofthe quadriceps at a regular pace. COPD patientsperformed a reduced number of contractions at a

power output adapted from their own maximal

Results

There were no significant differences between theCOPD and control groups for anthropometric data(Table 1). Differences between the two groups couldbe observed for spirometric function and level ofphysical activity (Table 1).

Analysis of peripheral muscle performanceshowed no significant difference in MVC betweenthe COPD group and the control group (22±1 kg vs

24±2 kg). In contrast, muscle endurance (Tlim) was

significantly decreased in COPD patients comparedwith healthy subjects (Fig 2).We found a significant relationship between MVC

and FFM (p<0.05), Tlim and PA score (p<0.05)(Fig 3), Tlim and FEVX (p<0.05) (Fig 4), and Tlimand Pa02 (p<0.05) (Table 2) in COPD patients.Significant correlations were also found between PAscore and FEVi (r=0.63, p<0.05), and Vo2 si

500

450

400

350

_300 H

E 250H

200

150 -\100

50

0

COPDcontrol

i

Figure 2. Peripheral muscle endurance in COPD patients andcontrol subjects. Values are expressed as mean (SE). Asterisk:significantly different from control value (p<0.05).

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500

450

400

350

_ 300

E 250p 200

150

100

50

0

Tlim =15.4 [PA score]+ 140.5r=0.60, p<0.05

I-1-1-1 I-1-1-1I-1-1-1 I-10 1 2 3 4 5 6 7 8 9 10 11 12 13 14

PA score

Figure 3. Relationship between peripheral muscle enduranceand level of PA in COPD patients.

strength. Since a subject's motivation may determineattainment of maximal effort, the same investigatorsupervised the endurance test and gave the same

encouragement to all subjects. Moreover, in a pre¬vious experiment consisting of repetitive tests withthe same technique, Tlim was found to be highlyreproducible since the correlation coefficients yield¬ing Tlim and limit work were always >0.9.20 Fur¬thermore, patients were not hypoxemic at rest and,during the incremental exercise test that involves a

large part of the muscles, they did not presentoxygen desaturation under 92%. It thus appears thatduring the endurance test involving one musclegroup, the limiting factor cannot be oxygen availabil¬ity, but rather the neuromuscular characteristics ofthe muscle.

Since deconditioning is a major problem oftensuggested as an explicative factor of exercise intoler¬ance in patients, we thought it interesting to inves¬tigate the level of physical activity in our patients.Since our COPD population did not work because ofage and/or pathology, we chose a questionnaireadapted for use in retired people with independentlifestyles.15 This questionnaire appears valid for

500

450

400

350

300

250

200

150

10050

0

Tlim = 2.28^^]+ 97.1r=0.52, p<0.05

20 30 40 50 60 70 80 90

FEV., (% pred)

Figure 4. Relationship between peripheral muscle enduranceand bronchial obstruction in COPD patients.

Table 2.Correlation Coefficients for Skeletal MusclePerformance With Level ofPA, Body Composition, and

Lung Function in COPD Patients

PA score FFM FEVi Pa09MVCTlim

0.040.60*

0.64f0.13

0.270.52*

-0.240.63*

*p<0.05.fp<0.01.

COPD patients since we found a significant positivecorrelation between PA score and Vo2 si. Patientshad lower scores than the healthy subjects, whothemselves had scores indicating sedentary lifestylesaccording to the questionnaire analysis.15 This resultindicates a reduced level of daily physical activity inthe patients and, to our knowledge, this is the firststudy of this variable in COPD patients.

Peripheral muscle weakness evidenced by reducedmaximal strength of the quadriceps has been ob¬served in COPD patients.8-9 However, skeletal mus¬

cle endurance assessment was not included in thesestudies. In the present work, we did not find maximalmuscle strength to be significantly lower in patientscompared with healthy subjects. This result, whichcontrasts with those of previous studies, could besurprising since the same muscular group, the quad¬riceps, was used for assessment of skeletal muscleperformance. However, in the previous works, max¬

imal quadriceps strength values in patients were

compared with predicted values and not with thoseof a control group.Our results showed that skeletal muscle endur¬

ance was decreased in COPD patients. A plausibleexplanation for this may be an abnormality of musclemetabolism. Indeed, the impaired muscle enduranceis consistent with the metabolic changes commonlyobserved in skeletal muscle in COPD patients. In¬vestigations of enzyme activities in the quadricepsfemoris of these patients compared with those ofcontrol subjects demonstrated lower activity of an

oxidative enzyme, the citrate synthase.2122 More¬over, several earlier reports showed that duringexercise, COPD subjects exhibited a higher inor¬ganic phosphate-to-phosphocreatine ratio, which isan index of muscle oxidative capacity, and a lowerintracellular pH than healthy control subjects.5-6These results indicate impaired skeletal muscle aer¬

obic capacity and suggest altered metabolic controlwith a metabolic shift toward dependence on lacticglycolysis. In a Tlim test, a rapid accumulation ofmetabolic byproducts in exercising muscle could beresponsible for the decline of force and, therefore,could be responsible for muscular fatigue. For ex¬

ample, muscular fatigue has been attributed to in-

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tracellular lactate accumulation, acidosis, or the in¬creased concentration of inorganic phosphate.2324We investigated relationships between skeletal mus¬

cle performance and several variables (PA score,FFM, FEV!, and Pa02) in COPD patients. Con¬cerning skeletal muscle strength, we found a positivecorrelation between MVC and FFM. Since FFM is

mainly composed of muscle cells, this result appearsin agreement with the literature concerning maximalstrength dependence on muscle cross-sectional area

and anthropometric parameters.25 In contrast, no

significant correlation was found between FFM andTlim. This result indicates that the decreased muscleendurance was independent of the patient's bodycomposition. In agreement with this observation, an

earlier study demonstrated that the altered oxidativemuscle metabolism in COPD patients is not affectedby their nutritional status.26An important mechanism of skeletal muscle alter¬

ations could be deconditioning. Indeed, the changesin skeletal muscle function described in COPDpatients are the opposite of training and the same as

the classic changes resulting from detraining.2728 In

agreement with a physical inactivity effect on skeletalmuscle endurance, we found a significant relation¬ship between Tlim and PA score. This result suggeststhat the level of PA is a determinant factor formuscle performance and, therefore, skeletal musclealterations in COPD patients can be the result ofdeconditioning. We found skeletal muscle endur¬ance also to be related to FEVX and resting Pa02.Skeletal muscle function in relation to hypoxemia hasbeen studied in COPD patients. Jakobsson et al29found significant correlations between muscle me¬

tabolite concentrations (glycogen, lactate, phospho¬creatine) and Pa02. Moreover, Mannix et al30 re¬

cently showed that the origin of adenosinetriphosphate flux (oxidative phosphorylation or an¬

aerobic glycolysis) in COPD patients is dependenton hypoxemia severity. The relations between Tlimand Pa02 and Tlim and FEVX thus appear consistentwith these findings, indicating the important role ofaltered lung function in limiting skeletal musclefunction. Since FEV] was also correlated with thepatients' scores, the reduced level of daily PA in thepatients seems to be dependent on the severity ofthedisease. The interrelationships among Tlim, FEV1?and PA score suggest that these variables are cofac-tors that progress together, and this is in agreementwith the secondary disease of deconditioning in

patients described by the model of the dyspneaspiral.34 However, it is impossible to determine therespective parts of bronchial obstruction and decon¬ditioning in altering skeletal muscle performance.Therefore, further studies matching healthy controlsubjects and COPD patients in terms of PA are

needed to investigate the role of bronchial obstruc¬tion in altering skeletal muscle function.

In conclusion, our data demonstrated impairedskeletal muscle endurance in COPD patients that isassociated with altered pulmonary function and re¬

duced daily PA.

ACKNOWLEDGMENTS: We thank Catherine Stott Carmenifor valuable technical assistance.

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DOI 10.1378/chest.113.4.900 1998;113; 900-905Chest

Isabelle Serres, Véronique Gautier, Christian Préfaut and Alain Varrayand Altered Lung Function in COPD Patients

Impaired Skeletal Muscle Endurance Related to Physical Inactivity

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