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Physiology of Walking in Patients with Moderate to Severe Chronic Obstructive Pulmonary Disease

MARQUIS, NICOLE1; DEBIGARÉ, RICHARD1; BOUYER, LAURENT2; SAEY, DIDIER3; LAVIOLETTE, LOUIS1; BROUILLARD, CYNTHIA1; MALTAIS, FRANÇOIS1

Medicine & Science in Sports & Exercise: August 2009 - Volume 41 - Issue 8 - p 1540-1548
doi: 10.1249/MSS.0b013e31819c717f
CLINICAL SCIENCES
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Purpose: Little is known about the physiology of walking in chronic obstructive pulmonary disease (COPD). Our objective was to evaluate the cardiac and respiratory responses as well as the electrical activity of lower limb muscles during walking in patients with COPD compared with healthy controls.

Methods: Cardiorespiratory parameters were monitored during a 6-min walking test (6MWT) in 10 patients with COPD and 11 healthy controls. Surface EMG (sEMG) data were recorded in five muscle groups (soleus, medial gastrocnemius, tibialis anterior, vastus lateralis, and rectus femoris) of the right leg during walking. The integrated signal (iEMG) and the median frequency were obtained from the sEMG signal of each muscle group.

Results: Although the walking distance and speed were significantly reduced in patients with COPD compared with those in controls, patients walked at a higher percentage of peak V˙O2. The overall sEMG patterns were similar between patients with COPD and controls. A fall in the sEMG median frequency during the 6 MWT was observed for the vastus lateralis and the rectus femoris in patients with COPD and in controls suggesting a muscle fatiguing contracting profile.

Conclusion: The 6 MWT was performed at a relatively higher intensity in patients with COPD compared with healthy controls. The progressive fall in the sEMG median frequency of the vastus lateralis and rectus femoris in both groups suggested the occurrence of a muscle fatiguing profile during walking. The performance of a daily activity such as walking imposes a high physiological demand in patients with COPD.

1Centre de Recherche, Institut Universitaire de Cardiologie et de Pneumologìe, Université Laval, Québec, CANADA; 2Centre Interdisciplinaire de Recherche en Réadaptation et Intégration Sociale (CIRRIS) de l'Institut de Réadaptation en Déficience Physique de Québec, Québec, CANADA; and 3Leuven Catholic University, Leuven, BELGIUM

Address for correspondence: François Maltais, M.D., Centre de pneumologie, Hôpital Laval, 2725 Chemin Ste-Foy, Québec, Québec, Canada G1V 4G5; E-mail: francois.maltais@med.ulaval.ca.

Submitted for publication August 2008.

Accepted for publication January 2009.

The exercise response is distinctly abnormal during cycling in patients with chronic obstructive pulmonary disease (COPD) compared with healthy subjects of similar age. Increased ventilatory requirements for a given exercise task, the occurrence of dynamic hyperinflation, and premature muscle fatigue leading to early perception of dyspnea and leg fatigue are characteristic features of the responses to cycling exercise in patients with COPD (25).

Much less is known about the physiological response during the 6-min walking test (6 MWT) in patients with COPD. Although the 6-min walking test was initially developed to evaluate the tolerance to daily functional activity, this testing modality was subsequently shown to represent a submaximal but intense cardiac and ventilatory stimuli (24,36) and to be associated with O2 desaturation (27) and dynamic hyperinflation (21) in patients with COPD. Whether the 6 MWT elicits a similarly intense response in healthy subjects is questionable in the absence of a direct comparison with patients affected by COPD. Because of a ceiling effect in the maximum speed that can be achieved during walking, without having to run, healthy fit subjects may walk at a lower relative intensity in comparison to patients with COPD. It is therefore possible that the significance of the 6 MWT in its intensity may differ according to the population under study. If true, this would be an important distinction between the 6 MWT versus the incremental cycling exercise test during which healthy and disabled subjects are allowed to reach their maximum, irrespective of their fitness level.

The role of quadriceps muscle dysfunction in impaired exercise tolerance has been well documented during cycling exercise in patients with COPD (14,31). The relevance of this observation for activities of daily living such as walking is unclear. To date, the exploration of muscle fatigue during walking in COPD has been limited to one muscle group, the quadriceps. Investigators reported that the occurrence of quadriceps contractile fatigue is much less common during walking compared with cycling (20,26). The possibility exists that fatigue may occur in other muscle groups that are activated during walking.

Surface EMG (sEMG) can provide useful indices reflecting motor unit recruitment and may represent an attractive means to assess muscle activity in situ. This method has been used in COPD to detect early abnormalities in muscle electrical activity during cycling exercise (1,11) while allowing to explore several muscle groups simultaneously. We recently used this technique to show that a fall in sEMG median frequency (MF) of greater than 4% was a good surrogate of contractile fatigue of the quadriceps in patients with COPD (30).

The present study was therefore undertaken to compare cardiac, respiratory, and lower limb sEMG responses during a 6 MWT in patients with COPD in comparison to healthy controls of similar age. To this extent, subjects performed a 6 MWT while being equipped with a portable oxygen consumption (V˙O2) system and a telemetric sEMG system evaluating the electrical activation of five different muscle groups of the right lower limb: the soleus (SOL), tibialis anterior (TA), medial gastrocnemius (MG), vastus lateralis (VL), and rectus femoris (RF). We hypothesized that the 6 MWT would be performed at a higher relative intensity in patients with COPD in comparison to healthy subjects. We also speculated that changes in sEMG of the working muscles, reflecting the occurrence of a muscle contractile fatiguing pattern during walking, would be found in patients with COPD as well as in healthy controls.

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METHODS

Subjects

Ten patients with COPD (9 men) and 11 sedentary healthy subjects (10 men) were recruited to participate in the study. The diagnosis of COPD was based on spirometry showing moderate to severe irreversible airflow obstruction (forced expiratory volume at 1 s [FEV1] < 60% predicted value and FEV1/forced vital capacity < 70%) and current or past smoking history (≥10 packs per year). All patients with COPD were stable at the time of experimentation and had a resting PaO2 > 60 mm Hg. Study subjects underwent medical screening that included a review of their medical history, medication, pulmonary function testing, and resting ECG. None had evidence of cardiovascular, neurological, musculoskeletal disorders, or any other conditions that could have altered their capacity to perform the walking test. The research protocol was approved by the institutional ethics committee, and a signed informed consent was obtained from each subject.

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Study Protocol

Three visits to the laboratory were necessary to complete the study. The first visit included height and weight measurements, resting ECG, pulmonary function assessment, familiarization with the 6 MWT, and the administration of a physical activity questionnaire (37). Muscle cross-sectional areas of the thigh and calf were measured by computed tomodensitometry. During the second visit, subjects performed a 6 MWT during which cardiopulmonary parameters were monitored and sEMG signals from five muscle groups of the right lower limb, namely, SOL, TA, MG, VL, and RF, were recorded throughout the walking test. These muscles were selected for their relevance during the different phases of walking (12,13). Finally, the perception of dyspnea and leg fatigue was evaluated at the end of the test. During the third visit, peak V˙O2 was assessed during an incremental shuttle walking test (ISWT) (34). Patients were asked to continue their usual medication throughout the study.

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Evaluation

Pulmonary function testing.

Subjects underwent resting spirometry (Jeager Masterscreen, Wüerzburg, Germany) according to the ATS recommendations (3) while being on their usual bronchodilator regimen. Results were compared with predicted normal values from the European Community for Coal and Steel/European Respiratory Society (28). Maximum voluntary ventilation (MVV) was calculated by multiplying FEV1 by 35.

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Physical activity level.

The level of physical activity in daily living was assessed using the activity questionnaire described by Baecke et al. (6), adapted for elderly individuals (37), and used in patients with COPD (32). A score between 9 and 16 indicates a moderate level of daily physical activity, whereas a score <9 is seen in sedentary subjects.

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Computed tomography.

Computed tomography (Highspeed CTi; General Electric, Chalfort St. Giles, United Kingdom) of the thigh and calf from each leg was performed to quantify muscle mass. Thigh measurements were taken halfway between the pubic symphysis and the inferior condyle of the femur (7). Calf measurements were performed in the proximal third of the distance between the lateral condyle of the tibia and the external malleolus of the ankle, in the zone of the calf belly (29). Five-millimeter-thick images were obtained with a scanning time of 0.8 s at 120 kV and 240 mA, with subjects in a supine position. The muscle cross-sectional area of the thigh (thigh CSA) and of the calf (calf CSA) was obtained by measuring the surface area of the tissue with a density of 40-100 Hounsfield units (HU).

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6-min walking test

The 6 MWT was completed in an enclosed corridor on a flat 30-m-long course according to the procedures recommended by the American Thoracic Society (4). Test time was recorded for every 30 m completed to estimate walking speed. Dyspnea and muscle fatigue perception were evaluated at the beginning and at the end of the 6 MWT using the modified 10-point Borg scale (8). Before each test, patients were instructed to cover as much ground as possible in the allotted period. Patients were also notified that no encouragement would be provided to them during the test, but that they would be kept aware of time, as per the American Thoracic Society guidelines.

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Surface EMG.

sEMG signals from the SOL, TA, MG, VL, and RF muscles of the right lower limb were measured during the 6 MWT using a wireless amplifier system (TeleMyo2400T; Noraxon, Inc., Scottsdale, AZ). The electrical activity of each muscle group was recorded by bipolar Ag-AgCl surface electrodes (Meditrace 200; Kendall, Miami, FL) with an interelectrode distance of 2 cm. The electrodes were placed over the approximate center of the muscle bellies on both sides of the motor point. Soleus electrodes were placed over the distal one third of the muscle, medial to the Achilles tendon. The EMG signal was high-pass-filtered (10 Hz) and preamplified near the recording electrodes. A second level of filtering (band-pass 10-500 Hz) and amplification was performed by the receiver box before data were collected by a portable computer. The MF of the signal was derived from a fast Fourier transform analysis. The MF was defined as the frequency that divided the power density spectrum into two regions of equal power (16). The level of muscle utilization was quantified using integrated EMG (iEMG). EMG data were first separated on a stride-by-stride basis, and the area under the rectified EMG signal (iEMG) was then calculated for each stride in each muscle. Average iEMG values were then obtained for each muscle over each minute of the 6 MWT. Only strides obtained during straight line walking at constant speed were considered for averaging. Periods of slowing down, negotiating turns, and reacceleration were discarded using an interactive program.

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Incremental shuttle walk.

The incremental shuttle walk was performed in an enclosed corridor on a flat 10-m-long course as previously described by Singh et al. (34). Briefly, patients walked around two cones, each positioned 0.5 m from either end, following the rhythm dictated by the audio signal. Walking speed was initially set at 0.50 m·s−1 and subsequently increased by 0.17 m·s−1 every minute until the patient reached a symptom-limited maximum.

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Cardiorespiratory parameters.

HR, O2 pulse saturation (SpO2), and breath-by-breath gas exchange parameters (V˙O2, E) were monitored during the 6 MWT and the incremental shuttle walk with a portable telemetric system (Oxycon Mobile; Jaeger, Viasys Healthcare GmbH, Germany). We used the equation of Jones et al. (2) to predict peak V˙O2 and the following equation to predict peak HR: 202 − 0.72 × age.

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Statistical Analysis

Results are expressed as mean ± SD unless specified otherwise. Within-group comparisons were made using paired Student's t-tests, whereas between-group comparisons were done using unpaired Student's t-tests. A custom program, written in Matlab (The Mathworks, Natick, MA), was used to analyze the EMG signals. EMG parameters (iEMG and MF) and their changes from minute 1 to 6 during the 6 MWT in control subjects and in patients with COPD were compared using a mixed ANOVA procedure that allowed us to evaluate and compare the time course of different EMG variables between the groups. The data were analyzed using the statistical package Sigmastat 1.0 (Jandel Scientific, San Rafael, CA) and SAS program (SAS Institute, Cary, NC) version 9.1 service pack 4. The level of statistical significance was set at P < 0.05.

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RESULTS

Characteristics of subjects.

Anthropometric characteristics and pulmonary function data are provided in Table 1. Both groups were well matched for age, body mass index, and activity level. On average, patients with COPD had severe airflow obstruction with a mean FEV1 of 37 ± 13% of the predicted value (range, 15%-56% of the predicted value). Lower limb muscle atrophy was present in patients with COPD as indicated by the significant reduction in thigh CSA compared with healthy subjects, P < 0.05. Calf CSA also tended to be smaller in patients compared with that in controls. Peak oxygen consumption averaged 20 ± 5 mL·kg−1·min−1 in patients with COPD compared with 27 ± 17 mL·kg−1·min−1 in healthy subjects, P < 0.05.

TABLE 1

TABLE 1

Group mean results for the physiological variables obtained during the 6 MWT are provided in Table 2 and Figures 1 and 2. Walking speed was constant throughout the 6-min period in both groups, and it was reduced in patients with COPD compared with that in healthy controls (P < 0.01, Table 2). Patients with COPD also covered a significantly shorter distance during the walking test (494 ± 116 vs 625 ± 50 m in healthy controls, P < 0.01). Figure 1 shows that patients with COPD work at lower absolute V˙O2, E, and HR during the 6 MWT compared with the healthy controls. However, when expressed in percentage of their respective peak values achieved during the ISWT, V˙O2, E, and HR were proportionally higher in COPD compared with those in healthy controls (Fig. 2 and Table 2). Breathing pattern was characterized by a faster breathing frequency and a smaller tidal volume in patients compared with that in healthy controls. The perception of dyspnea was significantly higher at the end of the 6 MWT in patients with COPD than in controls (P < 0.05). About 30% of patients with COPD and 40% of healthy controls reported a higher Borg score for leg fatigue than for dyspnea at the end of the 6 MWT (Fig. 3). SpO2 remained stable in controls, whereas it fell progressively to 87 ± 5% in patients with COPD.

FIGURE 1

FIGURE 1

FIGURE 2

FIGURE 2

FIGURE 3

FIGURE 3

TABLE 2

TABLE 2

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sEMG during walking.

Figures 4 and 5 demonstrate the changes in iEMG and in sEMG MF, respectively, from minute 1 to 6, expressed in absolute and relative units for the five studied muscle groups of the right lower limb. The iEMG of each of the five muscles were smaller in patients compared with controls; this was true throughout the exercise period. However, the kinetics of changes in iEMG was similar between patients with COPD and controls. In both groups, there was a fall in iEMG during the 6 MWT for the SOL, MG, and VL. Conversely, the electrical activities of the TA (ankle flexor) and RF (hipflexor/knee extensor), two muscles involved in bringing the leg forward during swing, increased in the control group and did not change in COPD, although this difference did not reach statistical significance. Overall, the pattern of changes in MF did not differ between COPD and controls subjects. The fall in sEMG MF was statistically significant and greater than 4% for the two thigh muscles (VL and RF). Conversely, the changes in MF of the shank muscles (SOL, TA, and MG) for the two groups during the 6 MWT were small and not statistically significant.

FIGURE 4-C

FIGURE 4-C

FIGURE 5-C

FIGURE 5-C

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DISCUSSION

The present study provides a comprehensive physiological evaluation during walking in patients with moderate to severe COPD in comparison to healthy controls. It extends previous work on the 6 MWT by providing a direct comparison between patients with COPD and healthy controls and by reporting about the sEMG patterns of five lower limb muscles during walking. Despite walking at lower speed and covering less distance, patients with COPD performed the 6 MWT at a higher proportion of their peak capacity compared with healthy controls. Overall, the electrical activity of five different lower limb muscle groups behaved in a similar fashion in patients with COPD and in healthy controls. A fall in sEMG MF during walking was observed in the VL and RF in healthy subjects and patients with COPD, suggesting that a fatiguing contracting pattern was occurring during the 6 MWT in both groups (30). These results support the idea that the performance of a daily activity such as walking imposes a high physiological demand in patients with COPD.

Before discussing our results, some methodological comments are warranted. The ISWT is not the standard exercise for determining peak V˙O2 in older active healthy subjects. This test was selected because we wanted to relate the exercise data obtained during the 6-min walking test to peak values obtained during the same exercise modality (walking). Previous studies have validated the ISWT as a measure of peak exercise capacity in patients with COPD (5,23,33). In line with this, peak physiological responses during incremental cycling exercise are very similar to those obtained during ISWT in patients with COPD (26). Thus, we believe that, although less extensively studied than incremental cycling exercise, the ISWT is adequate in assessing peak exercise capacity in patients with COPD. The situation in healthy subjects might be different in that it would be possible for fit individuals to complete all stages of the ISWT without reaching true peak capacity. No such individuals were included in the present study because only sedentary individuals were recruited. Also, Table 1 clearly shows that peak exercise data obtained in healthy controls and in patients with COPD were consistent with the performance of a maximal effort during the ISWT.

We mostly restricted the inclusion to men with COPD to minimize the variability of the results. COPD may have a different impact in women compared with that in men. For example, pulmonary function (19) and exercise tolerance (9) show significant gender differences in COPD. Also, muscle activation during walking in the healthy population shows a distinctive pattern between genders (15). Our results apply to a population of patients with moderate to severe COPD and may not be generalizable to patients with mild disease.

The present results are consistent with a previous report (36) indicating that the 6 MWT elicits a near-maximum physiological response in patients with COPD, as evidenced by peak V˙O2 and HR values at the end of the 6-min walking protocol that were more than 90% of the maximal values achieved during an ISWT. This is in striking contrast with healthy controls in whom the 6 MWT was less demanding, a finding in agreement with past investigations (17,18). This observation highlights the plateauing effect of the 6 MWT during which subjects are not allowed to run, indicating that the 6 MWT may not be a good tool in assessing maximal capacity in less disabled subjects.

We report a detailed description of the electrical activities of lower limb muscles during the 6 MWT. The iEMG provides information about the state of activation of a given muscle. The iEMG of the lower limb muscles was decreased throughout the walking period in patient with COPD compared with that in controls, likely reflecting the lower walking speed in the former group. This is supported by the close relationship between the magnitude of lower muscles activation and walking speed (22). The progressive fall in iEMG of the SOL, MG, and VL that was observed in the two groups is difficult to interpret when considering that walking speed remained stable during the walking test. One possible explanation is that the mechanical efficiency of these muscles improved during the walking test so that the required level of electrical activation to produce a given external work would be decreased. Another possibility is that the external work performed during walking was shared with other muscle groups that were not evaluated herein. Lastly, subjects may have adopted a more efficient walking pattern by modifying their cadence and step length. Although exploring this issue was beyond the scope of the present investigation, it is nevertheless interesting to observe that patients with COPD and control subjects intuitively selected the same pattern of antigravitational muscle activation for the SOL, MG, and VL. The progressive increase in iEMG of the TA and RF, two muscles involved in the flexion of the lower limbs during the swing phase of the walking cycle, in normal subjects during the 6 MWT could be interpreted as an attempt to increase motor unit recruitment by the central nervous system to maintain power output. No such central adaptation was seen in patients with COPD, perhaps indicating the occurrence of central fatigue in these individuals. Alternatively, an increased activation of these lower limb flexors was perhaps unnecessary in COPD because of their slower walking velocity.

This study was designed to investigate whether lower limb muscles in patients with COPD could be susceptible to fatigue during walking. A recent investigation reported that patients with COPD intuitively adopt the maximum walking speed that can be tolerated for the duration of the 6 MWT (10). When compared with cycling, walking places a higher demand on the ventilatory system (24) and may exert a greater physiological stress on the respiratory system than on lower limb muscles. This statement is supported by the observation that ventilatory demand and dyspnea levels were higher, whereas oxygen desaturation was more profound, during walking exercises compared with cycle ergometry (24). Work partitioning among several muscle groups during walking (as opposed to cycling) would also reduce the likelihood of developing overt muscle fatigue during walking. In line with this reasoning, investigators reported that walking did not elicit contractile fatigue of the quadriceps in patients with COPD (20,26). It is thus possible that the walking speed, being naturally adjusted to the capacity of the respiratory system to accommodate the ventilatory requirements of exercise, would not be sufficient to induce overt leg fatigue during walking in this population.

To further explore this issue, we took advantage of a telemetric EMG system to investigate the sEMG pattern of five different muscle groups during walking. The sEMG frequency shift found in the fatiguing muscle has been attributed to the decrease in muscle fibers' conduction velocity (35), as well as to the lowering in muscle pH and to the progressive recruitment of Type I fibers that have a lower frequency than Type II fibers. Although a progressive decrease in sEMG MF cannot be viewed as indicating the presence of overt muscle fatigue, Saey et al. (30) determined that a 4% or greater fall in sEMG MF of the quadriceps during cycling exercise was a good clinical predictor of contractile fatigue. Whether this 4% criterion also applies to other muscles during other forms of exercise was not evaluated in this study. Nevertheless, the pattern of sEMG MF found in the RF and VL, in patients with COPD and healthy controls, is consistent with the occurrence of a fatiguing contracting pattern with a progressive recruitment of Type I fibers during walking. The pattern of changes in sEMG MF was similar between the two groups, despite slower walking pace in patients with COPD, and it is conceivable that the observed sEMG changes would have been more profound in patients with COPD had they walked at the same speed as healthy controls. Whether the electrical changes observed in the RF and VL would be sufficient to be associated with a fall in muscle force and contractile fatigue after walking was not investigated. It is nevertheless interesting to observe that 30% of our patients reported a higher Borg score for leg fatigue than for dyspnea at the end of the walking test.

In summary, the present study indicates that the 6 MWT is performed at a higher relative intensity in patients with moderate to severe COPD when compared with healthy controls of similar age. Our detailed physiological analysis of this exercise modality also indicates that the overall activation profile of the lower limb muscles was strikingly similar in patients with COPD and controls, despite a much lower walking speed in the former group. We interpret these observations as indicative that patients with COPD may be more vulnerable to muscle fatigue during a common activity of daily living such as walking.

Financial support: N. Marquis was a recipient of a salary support award from the Centre de Recherche de l'Hôpital Laval. R. Degibaré, L. Bouyer and F. Maltais are research scholars of the fonds de la recherché en santé du Québec. This work was supported by CIHR grant MOP-84091.

The authors acknowledge the contribution of Marthe Bélanger, Marie-Josée Breton, Brigitte Jean, and Josée Picard and Éric Nadreau for their help in accomplishing this study and of Marquis Dubois for his assistance in data analysis.

Conflict of interest: They authors declare that they have no relationship to disclose in regards to the current study. The results of the present study do not constitute endorsement by ACSM.

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Keywords:

COPD; EXERCISE; MUSCLE; FATIGUE; ELECTROMYOGRAPHY

© 2009 American College of Sports Medicine