Differences in respiratory muscle activity during cycling and walking do not influence dyspnea perception in obese patients with COPD

Casey E. Ciavaglia, Jordan A. Guenette, Daniel Langer, Katherine A. Webb, J. Alberto Neder and Denis E. O'Donnell J Appl Physiol 117:1292-1301, 2014. First published 9 October 2014; doi:10.1152/japplphysiol.00502.2014 You might find this additional info useful... This article cites 44 articles, 20 of which can be accessed free at: /content/117/11/1292.full.html#ref-list-1 Updated information and services including high resolution figures, can be found at: /content/117/11/1292.full.html Additional material and information about Journal of Applied Physiology can be found at: http://www.the-aps.org/publications/jappl

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J Appl Physiol 117: 1292–1301, 2014. First published October 9, 2014; doi:10.1152/japplphysiol.00502.2014.

Differences in respiratory muscle activity during cycling and walking do not influence dyspnea perception in obese patients with COPD Casey E. Ciavaglia,1 Jordan A. Guenette,1,2 Daniel Langer,1,3 Katherine A. Webb,1 J. Alberto Neder,1 and Denis E. O’Donnell1 1

Respiratory Investigation Unit, Department of Medicine, Queen’s University & Kingston General Hospital, Kingston, Ontario, Canada; 2Department of Physical Therapy and UBC Centre for Heart Lung Innovation, University of British Columbia, Vancouver, British Columbia, Canada; and 3Rehabilitation Sciences, KU Leuven, Leuven, Belgium Submitted 10 June 2014; accepted in final form 3 October 2014

obesity; COPD; dyspnea; exercise modality; respiratory mechanics

dyspnea intensity in patients with chronic obstructive pulmonary disease (COPD) rises in association with increased central motor command output to the respiratory muscles (15, 19, 27, 41) and can be further modulated by altered afferent inputs from peripheral sensory receptors in the lungs, respiratory muscles, and chest wall (33, 35, 38). In patients with combined COPD and obesity, activityrelated dyspnea is a major symptom and likely contributes to poor health-related quality of life (46). The prevalence of both COPD and obesity is increasing at an alarming rate throughout the world, and improved symptom control in this subpopulation with combined disorders awaits a better understanding of how excessive weight interacts with the basic pathophysiology of COPD (14, 31). Studies have shown that dyspnea in obese

IT IS BELIEVED THAT EXERTIONAL

Address for reprint requests and other correspondence: D. E. O’Donnell, 102 Stuart St., Kingston, ON, Canada K7L 2V6 (e-mail: [email protected]). 1292

patients with moderate-to-severe COPD is multifactorial and we have argued that increased metabolic requirements (increased carbon dioxide output) related to excessive body ˙ E) during physical weight, which drive increased ventilation (V activity, are more important than respiratory mechanical factors, per se, in contributing to exertional dyspnea (31, 39). In a recent noninvasive study in obese COPD patients, we ˙ E slopes established that dyspnea/work rate and dyspnea/V were not affected by exercise test modality (cycling vs. walking when work rate was controlled), despite consistent intermodality differences in some metabolic factors, e.g., ˙ O2) and arterial oxygen saturation (8). In the oxygen uptake (V present study, we extend our previous work in obese COPD by examining, for the first time, the effect of potential differences in amplitude of central respiratory drive (measured indirectly by diaphragmatic electromyography) and respiratory muscle activity (measured by esophageal and gastric balloons) between exercise modalities on dyspnea across its intensity, quality, and affective dimensions. A number of studies in nonobese healthy individuals have documented compensatory adjustments in abdominal muscle activity to preserve diaphragmatic function when adopting a standing body position (10, 11, 23, 26, 48). Such studies have, to our knowledge, not been conducted during rest or exercise in obese individuals with COPD. It is reasonable to assume that these normal compensatory adjustments to standing upright may be undermined by exaggerated gravitational effects of abdominal obesity. Thus it is possible that diaphragmatic function may be more compromised during standing and walking (compared with weight-supported cycling) in obese patients, and this may have negative sensory consequences. The corollary is that relatively improved diaphragmatic function during cycling would be associated with favorable effects on dimensions of dyspnea, as has previously been shown in nonobese COPD patients after interventions that improve respiratory muscle function (e.g., leaning forward position, bronchodilators, noninvasive mechanical ventilation) (12, 34, 38). Accordingly, our objectives were to determine whether 1) diaphragmatic function, expiratory muscle activity, and respiratory muscle recruitment pattern were different during walking and cycling in obese COPD patients; and 2) whether such intermodality differences in respiratory muscle activity (and accompanying afferent inputs from muscle mechanoreceptors) had direct sensory consequences when external power output was standardized between tests. We, therefore, compared indirect indexes of central respiratory drive, esophageal (Pes) and transdiaphragmatic pressures (Pdi), diaphragmatic efficiency and intensity, quality, and affective components of

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Ciavaglia CE, Guenette JA, Langer D, Webb KA, Neder JA, O’Donnell DE. Differences in respiratory muscle activity during cycling and walking do not influence dyspnea perception in obese patients with copd. J Appl Physiol 117: 1292–1301, 2014. First published October 9, 2014; doi:10.1152/japplphysiol.00502.2014.—In patients with combined obesity and chronic obstructive pulmonary disease (COPD), dyspnea intensity at matched work rates during weight-supported cycling and weight-bearing walking is similar, despite consistent metabolic differences between test modalities. The present study examined the influence of differences in activity of the diaphragm and abdominal muscles during cycling and walking on intensity and quality of dyspnea at matched ventilation in obese patients with COPD. We compared respiratory muscle activity patterns and dyspnea ratings during incremental cycle and treadmill exercise tests, where work rate was matched, in 12 obese (body mass index 36.6 ⫾ 5.4 kg/m2; mean ⫾ SD) patients with moderate COPD. We used a multipair electrode-balloon catheter to compare electromyography of the diaphragm and esophageal, gastric, and transdiaphragmatic pressures during the two exercise tests. Ventilation, breathing pattern, operating lung volumes, global respiratory effort, and electrical activation of the diaphragm were similar across exercise modalities for a given work rate. The cycling position was associated with greater neuromuscular efficiency of the diaphragm (P ⬍ 0.01), greater diaphragm use (P ⬍ 0.01) measured by the ventilatory muscle recruitment index, and less expiratory muscle activity compared (P ⬍ 0.01) with treadmill walking. However, intensity and quality of dyspnea were similar between exercise modalities. In obese patients with COPD, altered respiratory muscle activity due to body position differences between cycling and walking did not modulate perceived dyspnea when indirect measures of respiratory neural drive were unchanged.

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dyspnea during incremental treadmill and cycle exercise when work rate was carefully matched.

ing” on a modified 10-point Borg scale at rest, every 2 min of exercise, and at peak exercise (4, 40). Immediately after exercise, subjects were asked why they stopped exercising.

METHODS

Diaphragm EMG and Respiratory Pressures

Subjects Twelve clinically stable obese (body mass index ⬎30 kg/m ) patients with COPD [forced expiratory volume in 1 s (FEV1)/forced vital capacity (FVC) ⬍70%] and a postbronchodilator FEV1 ⬍ 80% predicted were included. Exclusion criteria included the following: a significant disease (i.e., metabolic, cardiovascular, neuromuscular, and/or musculoskeletal) that could affect breathlessness or exercise capacity, daytime oxygen therapy, a respiratory disease other than COPD, too breathless to leave the house or not breathless (Medical Research Council dyspnea scale 5 or 1, respectively), and any contraindications to clinical exercise testing (3). 2

Study Design

Procedures Pulmonary function testing included routine spirometry, body plethysmography, single-breath diffusing capacity for carbon monoxide, maximum inspiratory and expiratory mouth pressures, static lung compliance, and static lung recoil pressure using automated testing equipment (Vs62j body plethysmograph with Vmax229d; SensorMedics, Yorba Linda, CA). Cardiopulmonary exercise tests were performed on an electronically braked cycle ergometer (Ergometrics 800S; SensorMedics) and on a treadmill (MedTrack ST55; Quinton Instrument, Bothell, WA) using a Vmax229d Cardiopulmonary Exercise Testing System (SensorMedics). Cycle and treadmill exercise tests were both performed with 10-W increments, which increased every 2 min to a symptom-limited peak. The treadmill work rate was adjusted as follows: speed began at 0.8 miles/h (21.46 m/min) and thereafter increased linearly by 0.2 miles/h (5.36 m/min) for every 10-W increment for all subjects; a curvilinear rise in percent grade was calculated for each subject based on the equation by Cooper and Storer [Watts ⫽ 0.1634 ⫻ speed (m/min) ⫻ %grade/100 ⫻ body mass (kg)] (9). Breath-by-breath data (cardiopulmonary, EMGdi, and respiratory-mechanical measurements) were analyzed using 30-s averages from each individual at steady-state rest, the first 30-s interval of the last minute from each exercise work rate, and the last 30-s of loaded pedaling (peak). Inspiratory capacity (IC) maneuvers were performed during the steady-state resting period, during the last 30-s of each exercise work rate, and at peak exercise. Operating lung volumes were derived from IC measurements (37): end-expiratory lung volume (EELV) ⫽ total lung capacity (TLC) ⫺ IC, endinspiratory lung volume (EILV) ⫽ EELV ⫹ tidal volume (VT), and inspiratory reserve volume (IRV) ⫽ IC ⫺ VT. Subjects rated “breathing discomfort,” “leg discomfort,” “work or effort of breathing,” “difficulty breathing in,” and “how unpleasant or bad is your breath-

Table 1. Subject characteristics Means ⫾ SD

Men/women, n Age, yr Height, cm Weight, kg BMI, kg/m2 Waist circumference, cm Men Women Waist-to-hip ratio Men Women Total body fat*, % Men (n ⫽ 4) Women (n ⫽ 5) Truncal fat mass*, %total trunk mass Men (n ⫽ 4) Women (n ⫽ 5) Smoking history, pack·yr Baseline dyspnea index (0–12) MRC dyspnea scale (1–5) Pulmonary function† FEV1, liters (%predicted) FEV1/FVC, % TLC, liters (%predicted) IC, liters (%predicted) FRC, liters (%predicted) RV, liters (%predicted) ERV, liters (%predicted) sRaw, cmH2O·s (%predicted) DLCO, ml·min⫺1·mmHg⫺1 (%predicted) MIP, cmH2O (%predicted) MEP, cmH2O (%predicted) CLst, l/cmH2O PLst, cmH2O

67 ⫾ 8 167 ⫾ 9 103 ⫾ 25 36.6 ⫾ 5.4

6: 6

134 ⫾ 9 113 ⫾ 7 1.05 ⫾ 0.07 0.92 ⫾ 0.07 41 ⫾ 2 40 ⫾ 2 42 ⫾ 3 43 ⫾ 5 45 ⫾ 5 42 ⫾ 5 49 ⫾ 35 6.5 ⫾ 2.0 2.5 ⫾ 0.8 1.43 ⫾ 0.44 (60 ⫾ 13) 50 ⫾ 11 5.67 ⫾ 1.24 (98 ⫾ 10) 2.37 ⫾ 0.85 (89 ⫾ 22) 3.30 ⫾ 0.83 (105 ⫾ 20) 2.77 ⫾ 0.73 (126 ⫾ 29) 0.54 ⫾ 0.28 (61 ⫾ 35) 16.7 ⫾ 7.9 (397 ⫾ 177) 11.4 ⫾ 4.6 (46 ⫾ 10) 68 ⫾ 27 (89 ⫾ 36) 138 ⫾ 56 (81 ⫾ 22) 0.27 ⫾ 19 20 ⫾ 6

Values are means ⫾ SD, unless otherwise noted; n, no. of subjects. BMI, body mass index; MRC, Medical Research Council; FEV1, forced expired volume in 1 s; FVC, forced vital capacity; TLC, total lung capacity; IC, inspiratory capacity; FRC, functional residual capacity; RV, residual volume; ERV, expiratory reserve volume; sRaw, specific airway resistance; DLCO, diffusing capacity of the lung for carbon monoxide; MIP, maximal inspiratory pressure measured at FRC; MEP, maximal expiratory pressure measured at TLC; CLst, static lung compliance; PLst, static lung recoil pressure. *Measurements obtained by dual-energy X-ray absorptiometry scan. †Pulmonary function test measurements are prebronchodilator, except for forced spirometry, which is postbronchodilator.

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This cross-sectional study received ethical approval from Queen’s University and Affiliated Hospitals Research Ethics Board (DMED1187-09). Patients provided written, informed consent before participation. Patients attended three visits separated by at least 48 h. Visit 1 included medical screening, detailed pulmonary function tests, and familiarization with all exercise testing procedures. At visits 2 and 3, patients were randomized to perform either a cycle or treadmill test with detailed diaphragmatic electromyogram (EMGdi) and pressurederived respiratory mechanical measurements. Before each visit, patients were instructed to withhold inhaler medication at least 4 h for short-acting ␤2-agonists, 6 h for anticholinergics, and 12 h for longacting bronchodilators. Patients were asked to refrain from the intake of caffeine, heavy meals, alcohol, and from major physical exertion before each visit. At a separate visit, patients underwent dual-energy X-ray absorptiometry scans to quantify body composition.

A combined EMGdi electrode catheter with esophageal and gastric balloons was inserted nasally and positioned according to the strength of inspiratory EMGdi recordings, i.e., position was optimal when the amplitude of the outer of the five electrode pairs was greatest and the middle electrode pair was lowest (22). The raw EMGdi signal was amplified and band-pass filtered between 20 and 1,000 Hz (Bioamplifier model RA-8; Guanzhou Yinghui Medical Equipment, Guangzhou, China) and then sampled at 2,000 Hz (PowerLab, model ML880; ADInstruments, CastleHill, NSW, Australia). This signal was converted to a root mean square and averaged during inspiration between cardiac QRS complexes using a 100-ms time constant and a moving window. The largest value from the five electrode pairs was representative of each inspiration. The highest EMGdi value from either resting/peak sniff maneuvers or resting and exercise IC measurements was used as the maximum EMGdi (EMGdimax).

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Statistical Analysis This study had a small sample size due to the complexity and invasiveness of the respiratory pressure/EMGdi measurements. However, in a previous study evaluating similar outcome measures, a sample size of 11 was sufficient to show significant within-subject

Ciavaglia CE et al.

differences in sensory and respiratory mechanical/EMGdi measurements at a standardized work rate across two conditions (22). Comparisons of exercise modalities were made at rest, at standardized work rates (i.e., 10, 20, 30 and 40 W), and at peak exercise using paired two-tailed t-tests. Linear interpolation was used to calculate Pdiinsp,rise for both tests at common levels of EMGdi/EMGdimax (i.e., 30, 40, and 50%). A two-way ANOVA for repeated measures was used to analyze measurements of respiratory muscle strength pre- and postexercise across test modalities. To evaluate the relationship between dyspnea intensity (dependent variable) and relevant independent variables during exercise, the following were included in a multivariable linear regression model: the independent variable of interest, exercise modality as a categorical effect, an interaction term to determine whether the relationship being tested was similar across test modality (independent variable ⫻ modality), and subjects were treated as random effects to account for serial measurements (subject nested within modality). Results are reported as means ⫾ SD, unless specified otherwise. A P ⬍ 0.05 was used for statistical significance. RESULTS

Subject characteristics and resting pulmonary function are presented in Table 1. Subjects fit either Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2 (n ⫽ 9) or GOLD 3 (n ⫽ 3) spirometric criteria for moderate or severe airflow obstruction, respectively (45). By GOLD recommendations, all subjects were symptomatic (category B or D) with either a modified Medical Research Council grade ⱖ2 or a COPD Assessment Test score ⱖ10 (45). The mean body mass index fell within the Class II obesity classification, which is associated with a “very high disease risk” when combined with a waist circumference ⬎88 cm in women and ⬎102 cm in men (47). Waist circumference was elevated by 22 cm in men and 25 cm in women relative to previously defined abdominal obesity criteria (16, 47). Dual-energy X-ray absorptiometry scans were available in nine subjects and revealed that men (n ⫽ 4) and women (n ⫽ 5) had a similar mean percentage of

Table 2. Cardiopulmonary measurements during rest and peak exercise Rest

Work rate, W Exercise time, mm:ss Dyspnea, Borg scale Leg discomfort, Borg scale ˙ O2, l/min V ˙ O2, %predicted V ˙ CO2, l/min V RER ˙ E, l/min V ˙ E/MVV, % V ˙ E/V ˙ CO2 V PETCO2, Torr VT, liters fb, breaths/min TI/TT IC, liters IRV, liters Heart rate, beats/min Heart rate, %predicted SpO2, %

Peak

Cycle

Treadmill

Cycle

Treadmill

0⫾0 0⫾0 0.1 ⫾ 0.2 0.2 ⫾ 0.3 0.44 ⫾ 0.14 23 ⫾ 6 0.37 ⫾ 0.12 0.83 ⫾ 0.05 15.6 ⫾ 3.7 35 ⫾ 13 43.9 ⫾ 6.0 33.6 ⫾ 2.6 0.81 ⫾ 0.24 21 ⫾ 5 38 ⫾ 5 2.38 ⫾ 0.80 1.57 ⫾ 0.69 80 ⫾ 8 48 ⫾ 4 95 ⫾ 2

0⫾0 0⫾0 0.2 ⫾ 0.2 0.2 ⫾ 0.4 0.43 ⫾ 0.17 21 ⫾ 10 0.34 ⫾ 0.13 0.81 ⫾ 0.11 14.9 ⫾ 4.5 34 ⫾ 13 44.9 ⫾ 8.1 33.1 ⫾ 3.2 0.81 ⫾ 0.10 20 ⫾ 6 37 ⫾ 4 2.37 ⫾ 0.79 1.56 ⫾ 0.55 80 ⫾ 7 48 ⫾ 4 95 ⫾ 3

73 ⫾ 17 14:09 ⫾ 3:30 7.7 ⫾ 2.5 7.6 ⫾ 2.4 1.55 ⫾ 0.45 84 ⫾ 22 1.53 ⫾ 0.40 0.99 ⫾ 0.08 49.0 ⫾ 9.7 107 ⫾ 20 32.9 ⫾ 5.4 36.2 ⫾ 5.9 1.34 ⫾ 0.36 37 ⫾ 7 40 ⫾ 4 1.73 ⫾ 0.34 0.38 ⫾ 0.15 120 ⫾ 16 72 ⫾ 9 91 ⫾ 3

78 ⫾ 22 15:13 ⫾ 4:41 7.1 ⫾ 2.1 5.8 ⫾ 3.1* 1.74 ⫾ 0.59* 93 ⫾ 25* 1.61 ⫾ 0.51 0.93 ⫾ 0.11 49.5 ⫾ 13.0 109 ⫾ 22 31.3 ⫾ 4.7* 37.5 ⫾ 5.6* 1.34 ⫾ 0.45 38 ⫾ 8 41 ⫾ 5 1.74 ⫾ 0.54 0.40 ⫾ 0.18 126 ⫾ 18 76 ⫾ 10 89 ⫾ 4*

˙ O2, oxygen uptake; V ˙ CO2, carbon dioxide production; RER, respiratory exchange ratio; V ˙ E, ventilation; MVV, maximal voluntary Values are means ⫾ SD. V ˙ E/V ˙ CO2, ventilatory equivalent for carbon dioxide production; PETCO , partial pressure of end-tidal carbon dioxide; VT, tidal volume; fb, breathing ventilation; V 2 frequency; TI/TT, inspiratory duty cycle; IRV, inspiratory reserve volume; SpO2, arterial oxygen saturation by pulse oximetry. *P ⬍ 0.05, treadmill vs. cycle test at peak exercise. J Appl Physiol • doi:10.1152/japplphysiol.00502.2014 • www.jappl.org

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The esophageal and gastric balloons were inflated with 1.0 and 1.2 ml of air, respectively, and connected to differential pressure transducers (model DP15-34; Validyne Engineering, Northridge, CA). Pes and gastric pressures (Pga) were continuously recorded at a rate of 200 Hz (PowerLab). Pdi was recorded as the difference between Pga and Pes signals. The PowerLab system received continuous flow signal input from the Vmax229d cardiopulmonary testing system for offline analysis. Pre- and postexercise inspiratory sniffs were performed to obtain maximum Pes and Pdi. IC maneuvers at rest and throughout exercise were used to obtain dynamic peak inspiratory Pes (PesIC) and Pdi (PdiIC). Pre- and postexercise FVC maneuvers were also performed to obtain dynamic peak expiratory Pes. Tidal Pes swings (Pestidal) were defined as the amplitude between the maximum expiratory value and minimum inspiratory value for each respiratory cycle and expressed relative to maximum Pes (Pesmax: difference between PesIC and FVC Pes). Similarly, tidal Pdi swings were defined as the excursion between maximum inspiratory (Pdiinsp) and minimum Pdi during expiration. The inspiratory rise in Pdi (Pdiinsp,rise) was defined as the increase in Pdi from the onset of inspiratory flow to peak Pdi during inspiration. The peak tidal expiratory Pga and expiratory rise in Pga (Pgaexp,rise), which is the increase in Pga from the lowest point after onset of expiratory flow to its peak value during expiration, were used to estimate expiratory muscle activation (41). End-inspiratory (EI) and end-expiratory (EE) data points of zero flow for Pes (PesEI and PesEE) and Pga (PgaEI and PgaEE) were collected. The ventilatory muscle recruitment (VMR) index was calculated as the difference between PgaEI and PgaEE divided by the difference between PesEI and PesEE (30): a negative value represents greater diaphragm contribution, and a positive value represents a greater rib cage muscle contribution to inspiration. Finally, neuromuscular efficiency of the diaphragm was defined as the relation between Pdiinsp,rise and EMGdi/EMGdimax.



Respiratory Muscle Activity during Exercise in Obese COPD

total body fat (40 and 42%, respectively) and truncal fat (45 and 42%, respectively) (Table 1). Exercise Responses Steady-state rest and peak exercise responses are reported in Table 2. Patients exercised to a peak work rate of 73 ⫾ 17 W on the cycle ergometer and 78 ⫾ 22 W on the treadmill (P ⫽ 0.27). Exercise duration was longer on the treadmill compared with the cycle ergometer by a mean difference of 67 s, but was ˙ O2 during treadnot significantly different (P ⫽ 0.17). Peak V mill exercise was significantly higher compared with cycle ˙ E (Fig. 1A) and carbon dioxide production (V ˙ CO2) exercise. V were similar at a given work rate and reached similar peak ˙ E/ values (Table 2) for both exercise modalities. Moreover, V ˙ CO2 relationships were superimposed across exercise modalV ˙ E during exercise, both exercise modalities. For any given V ities had similar EMGdi/EMGdimax, global respiratory muscle effort (Pestidal in absolute terms and relative to Pesmax), breathing pattern, and operating lung volumes (Fig. 1, B and C).



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icantly different across modalities for pre- and postexercise measurements when analyzed by two-way repeated-measures ANOVA; however, postexercise PdiIC and Pdi obtained by preand postexercise inspiratory sniffs decreased significantly from preexercise values with both modes of exercise (Table 3). Inspiratory Pes in absolute terms or relative to PesIC was similar during exercise under both conditions (Fig. 1C, Table 3). Pdiinsp was greater throughout cycle exercise compared with treadmill exercise (Fig. 3A); however, inspiratory diaphragmatic effort (Pdiinsp/PdiIC) was similar between both exercise conditions due to a concurrent increase in PdiIC during cycle exercise. Pdiinsp,rise was also significantly greater during cycling compared with treadmill exercise (Fig. 3B). Furthermore, the downward displacement of the VMR index during cycling indicates greater use of the diaphragm at rest and at any given work rate compared with treadmill exercise (Fig. 3C). Interpolated values of Pdiinsp,rise at standardized EMGdi/ EMGdimax of 30, 40, and 50% were greater during cycle compared with treadmill exercise, indicating increased diaphragm efficiency during cycling (Fig. 4).

Inspiratory Muscles

Cycle

B

Treadmill

EMGdi/EMGdi,max (%)

60

VE (L·min-1)

50



40 30 20 10 0 0

C 80

-40

70

-30

60 50 40 30 20

30 20

40

50

60

1.2 1.0 0.8



50

60

F

45 40 35 30 25 20

10

20

30

40

30

40

50

60



10

0.6

VE (L·min-1)

20

VE (L·min-1)

15 40

10

Operating lung volume (L)

ƒb (breaths·min-1)

VT (L)

30

Pes,exp



1.4

30

10

0 10

E

20

0

VE (L·min-1)

1.6

10

Pes,insp -10

20

10 20 30 40 50 60 70 80 90

Pes,IC

-20

10

Work rate (W)

D

There was greater abdominal expiratory muscle activity during treadmill compared with cycle exercise as shown by a greater Pgaexp,rise throughout exercise and by a greater proportion of

Pes (cmH2O)

A

Expiratory Muscles

50

60

6.0

TLC

5.5

EILV

IRV 5.0 4.5 4.0

EELV 3.5 3.0 2.5 10



VE (L·min-1)

20

30

40

50

60



VE (L·min-1)

˙ E) for a given work rate was similar between cycle and treadmill exercise. Electrical activation of the diaphragm as a percentage of Fig. 1. A: ventilation (V maximum (EMGdi/EMGdimax; B), esophageal pressure (Pes) swings (inspiration upward; C), tidal volume (VT; D), breathing frequency (fb; E), and operating ˙ E. C: maximum inspiratory Pes during an IC maneuver lung volumes (inspiration upward; F) were similar between exercise modalities and are shown relative to V (PesIC) was not significantly different across modalities for pre- and postexercise measurements when analyzed by two-way repeated-measures ANOVA. Values are means ⫾ SE. Pesinsp, inspiratory Pes; Pesexp, expiratory Pes; EELV, end-expiratory lung volume; EILV, end-inspiratory lung volume; IRV, inspiratory reserve volume; TLC, total lung capacity. J Appl Physiol • doi:10.1152/japplphysiol.00502.2014 • www.jappl.org

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Raw data tracings from a representative patient are shown in Fig. 2 to illustrate differences in Pga, Pdi, and the VMR at a ˙ E (cycle: 24 l/min; treadmill: 26 similar work rate (30 W) and V l/min). Indexes of inspiratory muscle strength were not signif-

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subjects exhibiting a Pgaexp,rise at rest and early in exercise (Fig. 3, E and F). PgaEE was similar during both modes of exercise, while PgaEI fell to a significantly greater extent during treadmill walking compared with cycling (Fig. 3D). Exertional Dyspnea Subjects reported similar intensity of “breathing discomfort” (Fig. 5A), “work/effort of breathing,” “difficulty breathing in,” and “unpleasantness of breathing” (Fig. 5B) during submaximal and symptom-limited peak exercise for both test modalities. There were no significant differences between modalities for reasons for stopping exercise. Breathing discomfort, alone

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Fig. 2. Raw data tracings for a representative female patient show mechanical measurements at the 30-W load of the cycle and treadmill ˙ E (cycle: 24 exercise tests. Despite a similar V l/min; treadmill: 26 l/min), tracings show different respiratory muscle recruitment patterns: inspiratory transdiaphragmatic pressures (Pdi) was greater during cycling, gastric pressure (Pga) was shifted downwards during walking, and the ventilatory muscle recruitment (VMR) index was more negative during cycling (cycle: ⫺0.67; treadmill: 0.45). Solid circles represent points of zero flow, and connecting bars represent Pga and Pes slopes for the VMR index calculation. Expir, expiration; Inspir, inspiration.

or in combination with leg discomfort, was reported as the main reason for stopping exercise in 58% of cycle tests and in 83% of treadmill tests. Conversely, leg discomfort, alone or in combination with breathing discomfort, was reported in 75% of cycle tests and in 58% of treadmill tests. Qualitative descriptors of breathlessness at end exercise were similar between modalities. Dyspnea increased similarly in both tests as ˙ E, EMGdi/EMGdimax, and Pestidal/ a function of increasing V Pesmax throughout exercise (Fig. 5). Dyspnea intensity during ˙ E/maximal voluntary ventiexercise correlated strongly with V lation, Pestidal/Pesmax, and EMGdi/EMGdimax (all P ⬍ 0.0005); these relationships were similar across testing modality.

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Table 3. Respiratory mechanical measurements during rest and peak exercise Rest

Pdisn, cmH2O PdiIC, cmH2O Pestidal, cmH2O Pestidal, %Pesmax VMR index EMGdi/EMGdimax, % Inspiratory muscle activity Pesinsp, cmH2O Pesinsp, %PesIC Pdiinsp, cmH2O Pdiinsp, %PdiIC Pdiinsp,rise, cmH2O Expiratory muscle activity Pesexp, cmH2O Pgaexp, cmH2O Pgaexp,rise, cmH2O PgaEI, cmH2O PgaEE, cmH2O

Peak

Cycle

Treadmill

88.4 ⫾ 19.6 68.3 ⫾ 23.6 9.8 ⫾ 3.6 9.8 ⫾ 3.3 ⫺0.6 ⫾ 0.8 18 ⫾ 10

89.5 ⫾ 24.5 62.0 ⫾ 18.8 10.4 ⫾ 4.7 10.0 ⫾ 4.4 ⫺0.1 ⫾ 0.8* 19 ⫾ 9

⫺7.5 ⫾ 2.2 28 ⫾ 10 26.7 ⫾ 5.6 42 ⫾ 15 10.0 ⫾ 3.9

⫺6.4 ⫾ 3.4 22 ⫾ 8 24.5 ⫾ 4.9 43 ⫾ 14 8.0 ⫾ 2.8*

2.3 ⫾ 2.8 20.2 ⫾ 4.9 2.3 ⫾ 1.6 19.5 ⫾ 5.0 16.6 ⫾ 3.3

4.0 ⫾ 2.3* 19.7 ⫾ 4.3 3.4 ⫾ 2.5 18.2 ⫾ 4.6 16.0 ⫾ 6.8

Cycle

74.7 ⫾ 22.6 49.7 ⫾ 15.4 38.3 ⫾ 17.8 37.9 ⫾ 17.2 0.5 ⫾ 0.6 64 ⫾ 14 ⫺16.1 ⫾ 2.2 60 ⫾ 16 34.1 ⫾ 7.1 71 ⫾ 13 11.5 ⫾ 6.1 22.2 ⫾ 15.2 37.0 ⫾ 17.8 22.3 ⫾ 17.8 17.7 ⫾ 6.2 26.8 ⫾ 8.5

Treadmill

65.0 ⫾ 24.8 38.8 ⫾ 10.2 37.9 ⫾ 16.3 36.1 ⫾ 15.8 1.2 ⫾ 0.4* 72 ⫾ 13* ⫺15.1 ⫾ 5.2 71 ⫾ 15 28.9 ⫾ 5.4* 74 ⫾ 10 8.3 ⫾ 3.9* 22.8 ⫾ 13.1 37.5 ⫾ 13.7 27.0 ⫾ 16.6* 10.1 ⫾ 4.2* 27.4 ⫾ 6.9

DISCUSSION

The novel findings of this study were as follows: 1) COPD patients with abdominal adiposity had greater diaphragmatic efficiency and less expiratory muscle activity when cycling compared with walking; and 2) differences in respiratory ˙ E during different muscle recruitment to achieve a given V exercise modalities did not impact intensity, affective, and qualitative domains of dyspnea. Our results do not support the hypothesis that differences in afferent inputs from the diaphragm and expiratory muscles during walking vs. cycling modulate dyspnea perception in obese patients with COPD, at ˙ E, indirect measures of respiraleast in circumstances where V tory neural drive, and dynamic respiratory mechanics are similar across exercise modalities. Patients in this study had moderate airway obstruction and were moderately obese with significant abdominal adiposity ˙ O2 rela(Table 1). Cardio-respiratory fitness expressed as peak V tive to ideal body weight was only modestly reduced. Mechan˙ E were similar at peak exercise, as was peak ical constraints on V dyspnea intensity, and breathing discomfort was a predominant reason for stopping exercise during both modalities. Respiratory Muscle Adjustments to Test Modality Maintaining effective diaphragmatic function in the upright posture in humans requires a number of compensatory actions that include the following: increased EMGdi activation, together with increased activation of abdominal and rib cage intercostal muscles (10, 11, 23, 26, 48). Gravitational displacement of the abdominal viscera (on standing) is believed to stretch the abdominal wall and to activate abdominal muscles to maintain intra-abdominal volume and pressure (compliance), thereby improving the geometric and length-tension relationships of the diaphragm (10). Increased tonic activation of the diaphragm and abdominal muscles has been described in healthy humans in the standing position during repetitive upper

limb movement (20, 21). The sensory consequences of this competition between the respiratory and trunk-stabilizing functions of the diaphragm and abdominal muscles during different lower limb exercises in patients with already compromised respiratory muscle function are unknown. In severely hyperinflated COPD, a reflexive increase in diaphragmatic and accessory muscle activity has been described in response to moving from the supine to the standing position (12). Whether such compensatory strategies exist in less hyperinflated patients such as ours with combined COPD and obesity (where IC is relatively preserved) has not been studied. To our knowledge, the present study is the first to determine whether the presence of abdominal obesity in COPD further undermines these posture-compensating strategies to maintain effective respiratory function of the diaphragm during exercise. Resting comparisons before onset of exercise (cycling vs. treadmill) showed small increases in Pdiinsp,rise, less accessory and expiratory muscle activity (more negative VMR), and modestly lower expiratory effort while sitting before cycling. At rest, there were no differences in tidal EMGdi or in diaphragmatic efficiency during sitting or standing. During cycling, obese COPD patients had greater Pdiinsp and greater peak force-generating capacity (PdiIC) compared with treadmill exercise, suggesting a distinct mechanical advantage (Fig. 3). Since efferent respiratory neural output (EMGdi/EMGdimax) to the crural diaphragm was similar during both modalities, the greater Pdiinsp,rise pressures during cycling suggest greater neuromuscular efficiency of this muscle (Fig. 4). Improved diaphragmatic efficiency (change in Pdi relative to change in EMGdi) during cycling may reflect relatively improved (reduced) abdominal compliance in this posture, allowing an enhanced fulcrum effect of increased abdominal impedance during diaphragmatic descent (11). A leaning forward position while seated with arms extended grasping the handlebars might improve length-tension relations of the diaphragm or permit

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Values are means ⫾ SD. Pdisn, transdiaphragmatic pressure (Pdi) obtained by pre- and postexercise inspiratory sniffs; PdiIC, Pdi obtained by IC maneuvers at rest and throughout exercise; Pestidal, tidal esophageal pressure (Pes) swings; Pesmax, maximum Pes; VMR, ventilatory muscle recruitment; EMGdi/EMGdimax, ratio of diaphragmatic electromyogram to maximum diaphragmatic electromyogram; Pesinsp, inspiratory Pes; PesIC, Pes obtained by IC maneuvers at rest and throughout exercise; Pdiinsp, inspiratory Pdi; Pdiinsp,rise, inspiratory rise in Pdi; Pesexp, expiratory Pes; Pgaexp, expiratory gastric pressure (Pga); Pgaexp,rise, expiratory rise in Pga; PgaEI, end-inspiratory Pga; PgaEE, end-expiratory Pga. *P ⬍ 0.05, treadmill vs. cycle exercise at that measurement point.

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Fig. 3. Pdi (A), Pdi inspiratory rise (Pdiinsp,rise; B), VMR index (C), Pga at zero flow (Pga, zero flow; D), expiratory gastric rise (Pgaexp,rise; E), and the frequency of expiratory muscle activity (F) are shown relative to work rate. Values are means ⫾ SE, unless specified otherwise. *P ⬍ 0.05, cycle vs. treadmill at a given work rate or at peak exercise. PdiIC, maximum inspiratory Pdi during an IC maneuver; PgaEE, end-expiratory Pga; PgaEI, end-inspiratory Pga.

inspiration (2, 42). Whether similar mechanisms are at play during walking in obese COPD patients could not be determined in the absence of concomitant measures of thoracoabdominal displacements. In contrast to the situation during treadmill exercise, PgaEE and PgaEI were similar in absolute terms throughout submaximal cycle exercise in our patients, 20

Pdi,insp.rise (cmH2O)

the pectoral and scalene muscles to act as accessory muscles of inspiration (18, 43), as has been previously proposed (11, 12). However, our ergometer and mouthpiece assembly ensured an almost vertical position of the thorax during cycling, suggesting that such factors are not instrumental in improving diaphragmatic efficiency in this circumstance. It is also possible that, with hip flexion during cycling, the proximal thighs supported the lower abdominal wall during the breathing cycle, thus helping to maintain positive intra-abdominal hydraulic pressure to assist the diaphragms inspiratory action (1). During walking, neuromuscular efficiency of the diaphragm was significantly reduced compared with cycling. Before exercise and consistent with previous studies in health (26), most patients had phasic expiratory muscle activity (Pgaexp,rise) while standing compared with sitting (91 vs. 50%, respectively). However, on average, the magnitude of expiratory muscle activity was similar in both cycle and treadmill positions at rest. During treadmill walking, there was a fall in PgaEI (Fig. 3) and a shift in the respiratory muscle recruitment pattern toward more activity of the inspiratory muscles of the rib cage and expiratory muscles, as indicated by analysis of the VMR plots of Macklem et al. (28). Greater expiratory muscle activity during walking may reflect increased abdominal muscle recruitment to stabilize the trunk. A reduction in PgaEI and increased abdominal volume have been reported during cycle and treadmill exercise in separate studies in healthy individuals and is thought to indicate abdominal wall relaxation during

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Fig. 5. Relationships between dyspnea intensity ˙ E (A), electrical activation of the diaand V phragm as a percentage of maximum (EMGdi/ EMGdimax; C), and tidal Pes swings as a percentage of maximum (Pestidal/Pesmax; D) were similar between cycle and treadmill exercise. B: intensity ratings for unpleasantness of breathing ˙ E were also similar. Values are relative to V means ⫾ SE.

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suggesting improved (decreased) abdominal compliance. In keeping with the results of a recent study (25), there was no difference in the behavior of EELV, despite the differences in expiratory muscle recruitment between modalities. Despite differences in respiratory muscle recruitment across tests, global measurements of respiratory muscle activity (tidal ˙ E. Individual respiswings of Pes) were similar for a given V ˙ E may vary such that reduced ratory muscle contributions to V diaphragmatic contributions during treadmill is likely counterbalanced by increased contribution of other respiratory muscles ˙ E dictated by the V ˙ CO2. Based on a previous to maintain the V study (25), we believe that the relatively increased expiratory muscle activity during treadmill testing in the present study is unlikely to translate into increased ventilatory output in the presence of expiratory flow limitation. A related question is why relatively increased diaphragmatic activity during cycling compared with walking did not translate ˙ E for a given work rate? In line with the into increased V argument above, one possibility is that increased diaphragmatic activity is linked to a corresponding reduction in activity of the other respiratory muscles (as suggested by our VMR ˙ CO2, ˙ E, as dictated by the prevailing V analysis) such that V remains constant. A second possibility is that, even in the face of increased inspiratory muscle activity during cycling, further ˙ E are not possible, particularly at higher exercise increases in V intensities where significant restrictive respiratory mechanical constraints are present (Fig. 1F). The similarity in ventilatory response during the two exercise modalities, despite differences in the contribution of var˙ E, is also explained by ious respiratory muscles to support V metabolic factors. Thus the ventilatory response to exercise, regardless of the test modality, was ultimately determined by

˙ CO2. As highlighted in our laboratory’s previous study (8), it is V ˙ CO2/work rate responses and V ˙ E/V ˙ CO2 (and conseclear that net V ˙ E/work rate) slopes were similar across tests, notwithquent V ˙ O2 and respiratory exchange ratio. standing differences in V Mechanisms of Exertional Dyspnea Increased central neural drive. Current concepts of the neurophysiology of exertional dyspnea in COPD emphasize the key role of increased respiratory neural drive from cortical and medullary centers in the brain and the attendant increased central corollary discharge to the somatosensory cortex (36, 40). We extended the results of our previous study by demonstrating that, not only ventilatory parameters, but also respiratory neural drive (EMGdi/EMGdimax) and global respiratory effort were similar during both exercise modalities and in˙ CO2. Thus we confirmed creased as a function of increasing V that the association between dyspnea intensity and measures of central respiratory drive was not influenced by differences in ˙ O2 requirements and arterial O2 saturation at a standardized V external power output during walking and cycling. The intermodality differences in arterial O2 saturation are expected and ˙ E, as previously are thought to reflect differences in alveolar V described (8, 29). The small decreases in arterial O2 saturation during walking are well below the threshold required to stimulate peripheral chemoreceptors or to directly influence respiratory sensation. The strong correlations (independent of exercise modality) between dyspnea intensity and the three indirect indexes of increasing respiratory neural drive (i.e., ˙ E/maximal voluntary ventilation, EMGdi/EMGdimax and V effort, and Pestidal/Pesmax) support the hypothesis that amplitude of central respiratory drive (and central corollary dis-

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Limitations The focus of the present study was to evaluate sensorymechanical relations in patients with combined COPD and

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obesity; therefore, the results may not be generalizable to nonobese patients who are more likely to have reduced resting IC. The lack of measurements of thoraco-abdominal excursions and tonic and phasic EMG recordings from respiratory muscles other than the diaphragm precludes definitive conclusions about variability in the complex respiratory muscle coordination strategies employed as a result of positional differences during exercise. Conclusions The present study shows, for the first time, that diaphragmatic and expiratory muscle activity is different during cycling and walking in obese individuals with COPD. However, despite the relatively reduced neuromuscular efficiency of the diaphragm during weight-bearing treadmill exercise compared with weight-supported cycling, perceived respiratory discomfort was not increased. Our results further indicate that exertional dyspnea intensity is ultimately dictated by the amplitude of respiratory neural drive and concomitant dynamic restrictive mechanical constraints (decreasing IRV). Moreover, under conditions where respiratory neural drive and the volume and timing components of breathing were constant, body positionrelated alterations in activity of major respiratory muscles to ˙ E during different exercise modalities had achieve a similar V no measurable effects on the intensity and quality of dyspnea. Implications Clinicians involved in laboratory cardiopulmonary exercise testing should be aware of the fundamental physiological differences between cycling and treadmill in obese COPD patients. Either test modality is suitable for evaluation of dyspnea, which, regardless of physical task, rises in association with increasing central neural drive. An important clinical implication is that interventions that reduce central respiratory ˙ CO2 by manipulation of energy drive (e.g., reduction of V substrate or exercise training) should successfully relieve exertional dyspnea in obese patients with COPD. GRANTS This study was supported by the Ontario Lung Association/Ontario Thoracic Society. D. Langer was supported by a postdoctoral fellowship from the Research Foundation Flanders. J. A. Guenette was supported by postdoctoral fellowships from the Natural Sciences and Engineering Research Council of Canada, the Canadian Thoracic Society, and the Canadian Lung Association, and a New Investigator Award from the Providence Health Care Research Institute and St. Paul’s Hospital Foundation. DISCLOSURES J. A. Neder has received research funding from Novartis and Nycomed and has served on speakers bureaus, consultation panels, and advisory boards for Boehringer Ingelheim, Novartis, and Chiesi Pharmaceutici. AUTHOR CONTRIBUTIONS Author contributions: C.E.C., J.A.G., and D.L. performed experiments; C.E.C. and K.A.W. analyzed data; C.E.C., J.A.G., D.L., K.A.W., J.A.N., and D.E.O. interpreted results of experiments; C.E.C. prepared figures; C.E.C., J.A.G., D.L., K.A.W., J.A.N., and D.E.O. drafted manuscript; C.E.C., J.A.G., D.L., K.A.W., J.A.N., and D.E.O. edited and revised manuscript; K.A.W. and D.E.O. conception and design of research; D.E.O. approved final version of manuscript.

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charge) is an important determinant of dyspnea, regardless of the nature of the physical task that provokes the symptom. Altered afferent sensory inputs. The previously established relationship between increase in dyspnea intensity and reduction of dynamic IRV toward its minimal value (34) has been shown to be independent of exercise modality (8). It is widely accepted that alteration of peripheral afferent inputs from the respiratory system (lung, chest wall, and respiratory muscles) can influence dimensions of dyspnea during exercise. For example, increased VT and IRV following pharmacological lung deflation, or changes in posture at rest, can affect (reduce) activity-related dyspnea intensity perception, presumably by altering peripheral afferent sensory inputs from the respiratory system and by partially reducing neuromechanical dissociation (33). It has long been postulated that afferent information from abundant sensory receptors in the respiratory muscles represents the proximate source of feedback regarding the status of the respiratory system and the appropriateness of its response to the prevailing central neural drive (7). In this context, it is reasonable to assume that, during exercise, alteration of afferent inputs from various active respiratory muscle groups (which sense tension and displacement) will modulate dyspnea perception. The present study design allowed us, for the first time, to evaluate the sensory consequences of body positionrelated changes in diaphragmatic efficiency and in expiratory muscle recruitment in relative isolation, in a setting where intensity of respiratory neural drive and global contractile respiratory muscle effort was constant. The finding that intensity, affective, and qualitative domains of dyspnea were unaffected by test-specific alterations in respiratory muscle activity ˙ E argues against a specific required to support a given V dyspneogenic role for mechanoreceptors in respiratory muscles of the chest wall and abdomen, at least under the experimental conditions of our study. The lack of a further increase in dyspnea as a result of greater diaphragmatic dysfunction during treadmill walking may reflect the relative paucity of spindles in this muscle, which provide sensory information about length and displacement (44). The lack of influence of increased expiratory muscle recruitment on dyspnea during treadmill walking is in keeping with the results of a recent study, which shows no association between increased expiratory effort and dyspnea during exercise in COPD (25). To the extent that between-test differences in the respiratory ˙ E had no measurable muscle activity required to generate a given V effect on dimensions of dyspnea, it would seem that there is substantial redundancy in the peripheral sensory systems. “Sense of effort,” as estimated by Pestidal/Pesmax, which was similar at a ˙ E during both test modalities, may be more closely linked given V to amplitude of central corollary discharge than to the pattern of afferent inputs from contracting respiratory muscles, per se (6, 13, 17, 24). Thus afferent inputs from other sources, such as pulmonary vagal receptors and chest wall mechanoreceptors, which are likely similar between tests (given the similarity of VT and operating lung volumes), may represent the primary source of peripheral afferent feedback to the somatosensory cortex, at least under the current experimental conditions.



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Differences in respiratory muscle activity during cycling and walking do not influence dyspnea perception in obese patients with COPD.

In patients with combined obesity and chronic obstructive pulmonary disease (COPD), dyspnea intensity at matched work rates during weight-supported cy...
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