Impact of aging on the work of breathing during exercise in healthy men

Abstract

This study examined the impact of aging on the elastic and resistive components of the work of breathing (W_b) during locomotor exercise at a given 1) ventilatory rate, 2) metabolic rate, and 3) operating lung volume. Eight healthy younger (25 ± 4 yr) and 8 older (72 ± 6 yr) participants performed incremental bicycle exercise, from which retrospective analyses identified similar ventilatory rates (approximately 40, 70, and 100 L·min⁻¹), similar metabolic rates (V̇o₂: approximately 1.2, 1.6, and 1.9 L·min⁻¹), and similar lung volumes [inspiratory and expiratory reserve volumes (IRV/ERV: approximately 25/34%, 16/33%, and 13-34% of vital capacity]. W_b at each level was quantified by integrating the averaged esophageal pressure-volume loop, which was then partitioned into elastic and resistive components of inspiratory and expiratory work using the modified Campbell diagram. IRV was smaller in the older participants during exercise at ventilations of 70 and 100 L·min⁻¹ and during exercise at the three metabolic rates (P < 0.05). Mainly because of a greater inspiratory elastic and resistive W_b in the older group (P < 0.05), total W_b was augmented by 40%–50% during exercise at matched ventilatory and matched metabolic rates. When examined during exercise evoking similar lung volumes, total W_b was not different between the groups (P = 0.86). Taken together, although aging exaggerates total W_b during locomotor exercise at a given ventilatory or a given metabolic rate, this difference is abolished during exercise at a given operating lung volume. These findings highlight the significance of operating lung volume in determining the age-related difference in W_b during locomotor exercise.

NEW & NOTEWORTHY This study evaluated the impact of aging on the work of breathing (W_b) during locomotor exercise evoking similar ventilatory rates, metabolic rates, and operating lung volumes in young and older individuals. Mainly because of a greater inspiratory elastic and resistive W_b in older participants, total W_b was higher during exercise at any given ventilatory and metabolic rate with aging. However, this age-related difference was abolished during exercise evoking similar operating lung volumes in both age groups. These findings highlight the significance of lung volumes in determining the age-related difference in total W_b.

INTRODUCTION

Healthy aging significantly impacts the pulmonary system by increasing chest wall stiffness and blunting, for example, gas exchange efficiency, lung elasticity, maximal expiratory flow rate, and respiratory muscle strength (1–6). These age-related changes lead to an increase in minute ventilation (V̇e) at a given workload (7, 8), and a greater power required by the respiratory muscles (i.e., power of breathing, P_b, J·min⁻¹) to achieve a given $\dot{\text{V}}\text{E}$ (8, 9). However, the latter observation might be misleading since aging also decreases maximal (V̇E_max) during exercise (10), resulting in older operating closer to their maximal ventilatory capacity at any given $\dot{\text{V}}\text{E}$. This may influence the evaluation of the impact of aging on P_b as increases in V̇E/V̇E_max are associated with increases in operating lung volumes (8) which are known to exponentially raise the P_b, regardless of age or sex (8, 11, 12).

Attempts to address this issue have been made by comparing the P_b between young and old individuals during exercise resulting in similar operating lung volumes in both age groups (i.e., exercise at a similar relative intensity) (8). However, as $\dot{\text{V}}\text{E}$ was significantly greater in the young, this difference skewed the comparison such that the young had a greater P_b than the old (8), which is, in part, due to the fact that the P_b (i.e., J·min⁻¹) is calculated as the product of respiratory work and breathing frequency (f_b). Therefore, to elucidate the role of aging on the energetic cost of breathing, a comparison is needed which directly examines the work required to move a given volume of air, i.e., the work of breathing (W_b, i.e., respiratory work per tidal volume, J·L⁻¹). However, a comprehensive examination of the influence of aging on W_b during exercise evoking similar operational lung volumes has yet to be conducted.

This study therefore investigated the influence of aging on the constituents of W_b during exercise at a range of similar 1) $\dot{\text{V}}\text{E}$, 2) ${\dot{\text{V}}\text{O}}_{\text{2}}$, and 3) operating lung volumes. Since operational lung volumes are higher during locomotor exercise at a given ventilatory or metabolic rate in the old (10), it was hypothesized that the greater W_b at similar $\dot{\text{V}}\text{E}$ and ${\dot{\text{V}}\text{O}}_{\text{2}}$ in the elderly is mainly attributed to increased inspiratory (resistive and elastic) and expiratory resistive work, and that the difference in W_b is diminished during exercise eliciting similar operating lung volumes.

METHODS

Participants

Eight healthy younger (25 ± 4 yr) and eight healthy, activity-, height-, and BMI-matched older (72 ± 6 yr) males participated in this study (Table 1). All participants were nonsmokers, free from any cardiovascular or pulmonary disease, and were not taking any medications that would alter pulmonary function. Written informed consent was obtained from all participants before their inclusion in this investigation. The Institutional Review Boards of the University of Utah and the Salt Lake City Veterans Affairs Medical Center approved all protocols.

Table 1.

Participant characteristics

	Young	Old
Anthropometrics and Physical Activity
Age (yr)	25 ± 4*	72 ± 6
Height (cm)	179 ± 8	176 ± 5
Weight (kg)	81 ± 11	82 ± 15
BMI (kg·m−2)	25 ± 2	27 ± 4
Steps per day	8,162 ± 2,552	8,609 ± 2,465
Pulmonary Function
FVC (L)	5.86 ± 0.61*	4.46 ± 0.67
% Predicted	101 ± 6	109 ± 15
FEV1 (L)	5.09 ± 0.80*	3.29 ± 0.40
% Predicted	105 ± 6	107 ± 11
FEV1/FVC (%)	86 ± 7*	75 ± 8
% Predicted	103 ± 9	98 ± 10
PEF (L/s)	11.5 ± 1.9*	9.7 ± 1.1
% Predicted	108 ± 11	119 ± 14
FEF25–75 (L/s)	5.29 ± 1.28*	2.87 ± 0.69
% Predicted	105 ± 20	112 ± 21
FEF25–75/FVC (%)	0.89 ± 0.20*	0.65 ± 0.16

Data are mean ± SD. BMI, body mass index; FEF_25–75, forced expiratory flow between 25 and 75% FVC; FEV₁, forced expired volume in 1 s; FVC, forced vital capacity; PEF, peak expiratory flow rate.

*Significant difference between groups, P < 0.05.

Experimental Protocol

Participants completed two study visits separated by at least 24 h. All participants reported to the laboratory 2 h postprandial and abstained from caffeine for 6 h, and from exercise for 24 h, before each session. Preceding the exercise portion of each visit, participants performed a 5-min warm-up on a cycle ergometer (Velotron, Elite model, Racer Mate, Seattle, WA) at 30 W. Participants were asked to remain seated and maintain a consistent cadence of 80 rpm during cycling exercise throughout all testing procedures.

The first session was a familiarization trial in which participants were thoroughly accustomed to pulmonary function testing and inspiratory capacity (IC) maneuvers at rest and during an incremental cycling test (30 W + 30 W·2 min⁻¹) performed to task failure (>10% drop in rpm for 5 s despite verbal encouragement). In the second session, participants repeated the same incremental cycling exercise for the determination of peak power output (W_peak, power of last completed stage), maximal oxygen consumption (i.e., V̇o_2max), operating lung volumes, V̇E_max, and the W_b. Intrapleural pressure excursions were quantified via an esophageal balloon. Retrospective analyses were performed to identify $\dot{\text{V}}\text{E}$ and ${\dot{\text{V}}\text{O}}_{\text{2}}$ values that were similar in young and old. Prior conducted pilot work, and previous findings (8, 13, 14), suggested that exercise at a given relative intensity evokes similar lung volumes in younger and older participants. Therefore, the impact of aging on the W_b at similar lung volumes was based on the comparisons of data obtained during exercise performed at various relative exercise intensities, i.e., 50, 80, and 100% of W_peak.

Measurements

Physical activity level.

Once instructed on proper operating procedures, participants wore an accelerometer (GTIM, Actigraph, Pensacola, FL) for a minimum of 7 consecutive days and daily physical activity was assessed as steps per day as previously done (15).

Pulmonary function.

Baseline pulmonary function were quantified before exercise while participants were seated on a cycle ergometer. This test included four forced vital capacity (FVC) maneuvers from which the largest vital capacity, forced expiratory volume in one second (FEV₁), Tiffeneau-Pinelli Index (FEV₁/FVC), peak expiratory flow rate, and midexpiratory flow between 25% and 75% of expiration (FEF-_25–75) were obtained according to American Thoracic Society guidelines (16). The single maneuver with the largest FVC and FEV₁ was chosen (17) and values are reported as absolute and percent predicted (18).

Heart rate and metabolic measurements.

Heart rate was obtained via the R-R interval derived from a 12-lead electrocardiogram. Metabolic data were collected continuously during exercise using a gas-calibrated indirect calorimetry system (Parvomedics Inc., Sandy, UT). Maximal metabolic and ventilatory responses are reported for the last minute of each stage of the incremental cycling test (2nd session) and the percent predicted ${\dot{\text{V}}\text{O}}_{\text{2}}{}_{\text{max}}$ was calculated as previously reported (19).

Flow, volume, and pressure measurements.

During all exercise sessions, participants breathed through a low-resistance circuit (∼0.6 cmH₂O·L⁻¹·s⁻¹) consisting of two-way nonrebreathing valves (series 2700, Hans Rudolph, Shawnee, KS) with heated and calibrated pneumotachographs on the inspiratory and expiratory side (series 3813, Hans Rudolph, Shawnee, KS). Inspired and expired volume was calculated from the integration of the flow signal and corrected for body temperature, pressure, and saturated conditions. As described previously (20), a latex balloon-tipped catheter (CooperSurgical, Trumbull, CT) was placed ∼40–50 cm from the nares for the measurement of esophageal pressure. After the balloon was inflated with 1 mL of air, correct placement within the lower one-third of the esophagus was verified using an occlusion test (21). Mouth pressure was sampled through a port in the mouthpiece. Esophageal and mouth pressures were quantified via individual differential pressure transducers (DP45-30, Validyne Engineering, Northridge, CA) which were calibrated before each visit.

Flow-volume and lung volume measurements.

Four postexercise FVCs were, in addition to the four pre-exercise FVCs, collected within 3 min after exercise and used for the construction of maximal flow-volume loops. Although postexercise FVCs account for exercise-induced bronchodilation (22), expiratory flow limitation (EFL) may still be slightly overestimated due to thoracic gas compression (22). At rest and during exercise, two IC maneuvers, verified against esophageal pressures obtained during the FVC, were performed (∼30 s apart) to correct for electronic and physiologic drift in the volume signal. Gated by the IC maneuvers, ∼8–10 representative tidal breaths were averaged for each stage. Tidal flow-volume loops were considered “representative” if they had similar volume and flow characteristics as the breaths before the first IC maneuver. EFL was identified as the percentage of the tidal flow-volume loop that met or exceeded the maximal flow-volume loop (23). Expiratory reserve volume (ERV) was determined by subtracting the IC from FVC and inspiratory reserve volume (IRV) was determined by subtracting the sum of ERV and tidal volume (V_T) from FVC. When expressed as percent vital capacity, IRV and ERV serve as an index of operating lung volumes in relation to a participants available functional capacity (e.g., a lower IRV equates to a higher relative end-inspiratory lung volume) (24–27).

Work of breathing.

An average esophageal pressure-volume loop (PVL) was created from the same 8–10 breaths identified in Flow-volume and lung volume measurements. Total system compliance (C_dyn), i.e., lungs, chest wall, and resistance of the breathing apparatus, was calculated as the quotient of the V_T and change in esophageal pressure between end-inspiratory and end-expiratory lung volume for each averaged loop. To examine potential age-related differences in W_b, PVLs were analyzed using the modified Campbell diagram analysis which accounts for group differences in chest wall stiffness and operating lung volumes (12, 28, 29) (Fig. 1). To partition the components into resistive (work performed to overcome airflow resistance) and elastic (work performed to overcome tissue deformation) work for inspiration and expiration, two lines were created through the PVL. The first line connects the points of zero flow on the PVL (i.e., end-inspiratory and end-expiratory lung volume) and represents dynamic lung compliance. The second line passes through FRC connecting end-inspiratory and end-expiratory lung volume using the slope of age-specific chest wall compliance which was estimated based on age and sex (1). Inspiratory resistive work (light gray, vertical hatching, Fig. 1) was then determined as the area to the left of the lung compliance line bound by the PVL, whereas expiratory resistive work (light gray, horizontal hatching) was determined as the area to the right of the chest wall compliance line bound by the PVL. Inspiratory elastic work (dark gray, square hatching, Fig. 1) was determined as the area of the triangle created between the lung and chest wall compliance lines above FRC; expiratory elastic work (dark gray, stippling) was determined the area of the triangle created between the lung and chest wall compliance lines below FRC. Each respective component was then normalized to V_T to obtain the W_b (J·L⁻¹). This represents the energetic cost to move a volume of air in contrast to the P_b traditionally utilized which incorporates f_b and may, therefore, be influenced by breathing strategy and represents a total amount of respiratory work performed over a given time.

Figure 1.

Example of a modified Campbell diagram pressure-volume loop analysis (J) for a younger (left: 26 yr, 185 cm, 78 kg) and older (right: 74 yr, 172 cm, 75 kg) participant at a similar level of ventilation. Zero point on Y-axis represents residual volume. Vertical hatching represents inspiratory resistive W_b (I_r), square hatching represents and inspiratory elastic W_b (I_e), horizontal hatching represents expiratory resistive W_b (E_r), and stippling represents expiratory elastic W_b (E_e). Arrows on the pressure-volume loop indicate direction of inspiration and expiration. C_cw, chest wall compliance; C_L, dynamic lung compliance; EELV, end expiratory lung volume as percentage of VC; EILV, end inspiratory lung volume as percentage of VC; F_b, breathing frequency; FRC, function residual capacity; J, Joules; VC, vital capacity; V_E, minute ventilation; V_T, tidal volume; W_b, work of breathing.

Data and statistical analysis.

Based on the data from the incremental cycling test, three ventilations ($\dot{\text{V}}\text{E}$, L·min⁻¹), three metabolic rates (${\dot{\text{V}}\text{O}}_{\text{2}}$, L·min⁻¹), and three lung volumes (determined by comparing IRV and ERV evoked during similar relative intensity exercise) present during exercise in both the younger and the older participants were identified. To evaluate the influence of aging, a priori planned comparisons for the W_b, ventilatory, and metabolic variables between younger and older participants were made at: 1) similar ventilations, 2) similar metabolic rates, and 3) relative exercise intensities eliciting similar operating lung volumes. A two-way mixed model analysis of variance (ANOVA) was performed for each comparison. If an ANOVA indicated a main effect, a Holm–Sidak post hoc test was performed to identify any differences. Additional Student’s t tests were employed to compare baseline characteristics and pulmonary function. Data are reported as mean ± standard deviation (SD). Statistical significance was set at P < 0.05.

RESULTS

Subject characteristics are reported in Table 1. Resting lung volumes (IRV, young: 37 ± 6% VC, older: 30 ± 10% VC, P = 0.15; ERV, young: 44 ± 6% VC, older: 40 ± 8% VC, P = 0.39) and respiratory compliance (young: 0.32 ± 0.06 L·cmH₂O⁻¹, older: 0.28 ± 0.09 L·cmH₂O⁻¹, P = 0.29) were unchanged with aging. Peak ventilatory and metabolic responses to the incremental test are reported in Table 4 under the 100% W_peak condition. W_peak was ∼55% greater in the younger group (P < 0.05). The total P_b (J·min⁻¹) plotted against $\dot{\text{V}}\text{E}$ for each individual during incremental exercise is presented in Fig. 2. Based on retrospective analysis of the incremental cycling test, similar ventilatory rates (∼40, 70, 100 L·min⁻¹), metabolic rates (∼1.2, 1.6, 1.9 L·min⁻¹), and lung volumes (∼IRV/ERV: 50% W_peak, 25/34% VC; 80% W_peak, 16/33% VC; 100% W_peak, 13%–34% VC) between young and older participants were identified.

Table 4.

Respiratory and metabolic responses during exercise eliciting similar lung volumes between young and older participants

	50% Wpeak		80% Wpeak		100% Wpeak		P Value
	Younger	Older	Younger	Older	Younger	Older	Main Effect of Age	Main Effect of Stage	Interaction Effect
Respiratory Variables
V̇e (L/min)	59 ± 14	50 ± 8	121 ± 30*	84 ± 11	152 ± 27*	113 ± 24	<0.01	<0.01	0.01
V̇e·V̇Emax-1 (%)	39 ± 4	44 ± 9	65 ± 9	68 ± 11	100	100	0.17	<0.01	0.46
Fb (breaths/min)	25 ± 5	29 ± 7	36 ± 9	40 ± 11	48 ± 8	45 ± 12	0.82	<0.01	0.72
VT (L)	2.4 ± 0.6*	1.8 ± 0.3	3.3 ± 1*	2.2 ± 0.4	3.3 ± 0.7*	2.3 ± 0.5	<0.01	0.01	0.68
Ttot (s)	2.5 ± 0.5	2.2 ± 0.5	1.7 ± 0.3	1.6 ± 0.4	1.2 ± 0.2	1.3 ± 0.3	0.66	<0.01	0.36
Ti (s)	1.1 ± 0.2	1.1 ± 0.2	0.8 ± 0.1	0.7 ± 0.2	0.6 ± 0.1	0.6 ± 0.1	0.57	<0.01	0.63
Te (s)	1.4 ± 0.3	1.2 ± 0.3	0.9 ± 0.2	0.9 ± 0.2	0.6 ± 0.1	0.7 ± 0.2	0.72	<0.01	0.28
Ti·Ttot-1 (%)	44 ± 4	45 ± 2	47 ± 3	46 ± 3	49 ± 3	47 ± 3	0.42	0.02	0.31
VT·Ti-1 (L/s)	2.3 ± 0.6	1.8 ± 0.3	4.3 ± 1.1*	3.1 ± 0.4	5.8 ± 1.5*	3.9 ± 0.5	<0.01	<0.01	0.06
VT·Te-1 (L/s)	1.8 ± 0.4	1.5 ± 0.3	3.8 ± 1.0*	2.6 ± 0.4	5.4 ± 1.1*	3.4 ± 0.8	<0.01	<0.01	<0.01
IRV (%VC)	26 ± 8	25 ± 10	17 ± 8	15 ± 9	14 ± 6	13 ± 9	0.79	<0.01	0.99
ERV (%VC)	33 ± 7	35 ± 7	30 ± 7	36 ± 10	33 ± 6	37 ± 10	0.30	0.64	0.46
EFL (%)	0 ± 0	2 ± 3	5 ± 14	7 ± 13	7 ± 14	22 ± 20	0.17	0.00	0.15
Cdyn (L/cmH2O)	0.27 ± 0.03	0.24 ± 0.10	0.21 ± 0.04	0.19 ± 0.08	0.17 ± 0.02	0.15 ± 0.03	0.45	<0.01	0.99
Metabolic Variables
Workload (W)	146 ± 37*	86 ± 19	249 ± 48*	146 ± 30	289 ± 55*	180 ± 36	<0.01	<0.01	<0.01
HR (beats/min)	132 ± 2*	117 ± 17	159 ± 13*	138 ± 14	177 ± 9*	151 ± 13	<0.01	<0.01	0.18
V̇o2 (L/min)	2.2 ± 0.6*	1.5 ± 0.3	3.1 ± 0.7*	2.0 ± 0.4	3.5 ± 0.7*	2.3 ± 0.4	0.01	<0.01	<0.01
V̇co2 (L/min)	2.1 ± 0.5*	1.4 ± 0.3	3.3 ± 0.7*	2.2 ± 0.4	4.2 ± 0.8*	2.9 ± 0.5	0.00	<0.01	<0.01
RER	0.96 ± 0.07	0.91 ± 0.09	1.10 ± 0.07	1.08 ± 0.07	1.20 ± 0.09	1.26 ± 0.13	0.96	<0.01	0.02
V̇e/V̇o2	27 ± 3	31 ± 4	32 ± 4	36 ± 6	40 ± 7	47 ± 10	0.10	<0.01	0.68
V̇e/V̇co2	28 ± 3	34 ± 4	29 ± 4	33 ± 4	34 ± 6	37 ± 6	0.07	<0.01	0.23
Wb Components
Ir (J/L)	0.23 ± 0.04	0.19 ± 0.07	0.43 ± 0.11	0.39 ± 0.16	0.73 ± 0.12*	0.55 ± 0.18	0.12	<0.01	0.04
Ie (J/L)	0.58 ± 0.09	0.74 ± 0.35	0.78 ± 0.20	1.05 ± 0.38	1.02 ± 0.27	1.18 ± 0.23	0.10	<0.01	0.62
Er (J/L)	0.09 ± 0.06	0.05 ± 0.06	0.22 ± 0.12	0.11 ± 0.09	0.41 ± 0.23	0.26 ± 0.22	0.07	<0.01	0.48
Ee (J/L)	0.08 ± 0.09	0.04 ± 0.07	0.12 ± 0.11	0.03 ± 0.05	0.09 ± 0.08	0.03 ± 0.05	0.10	0.62	0.34
Total (J/L)	0.97 ± 0.12	1.03 ± 0.27	1.53 ± 0.30	1.58 ± 0.37	2.20 ± 0.26	2.02 ± 0.39	0.86	<0.01	0.11

Data are mean ± SD. C_dyn, respiratory dynamic compliance; EFL, expiratory flow limitation; ERV, expiratory reserve volume as a percent of vital capacity; F_b, breathing frequency; HR, heart rate; IRV, inspiratory reserve volume as a percent of vital capacity; RER, respiratory exchange ratio; T_e, expiratory time; T_i, inspiratory time; T_tot, total time for one respiratory cycle; V̇co₂, carbon dioxide production; V̇e, minute ventilation; V̇E_Max, maximal V̇E; V̇e/V̇co₂, ventilatory equivalent for CO₂; V̇e/V̇o₂, ventilatory equivalent for O₂; V̇o₂, oxygen consumption; V_T, tidal volume; W_b, work of breathing. Data analyzed via 2-way analysis of variance for age and stage (n = 8).

*Significant difference between groups, P < 0.05.

Figure 2.

Illustration of the relationship between power of breathing and minute ventilation (V_E) during cycling exercise in each of the younger (black, n = 8) and older (gray, n = 8) participants.

Matched Ventilatory Rate

Stages eliciting similar $\dot{\text{V}}\text{E}$ values in both groups (Table 2) were identified for 40 (range 38–45 L·min⁻¹ in younger and 31–45 L·min⁻¹ in older), 70 (range 59–79 L·min⁻¹ in younger and 58–75 L·min⁻¹ in older), and 100 L·min⁻¹ (range 93–115 L·min⁻¹ in younger and 95–119 L·min⁻¹ in older). Heart rate and metabolic responses to exercise at these ventilatory rates are presented in Table 2. Although there was no significant effect of age on HR, ${\dot{\text{V}}\text{O}}_{\text{2}}$ and V̇co₂ were significantly lower and RER, $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{O}}_{\text{2}}$ and V̇E/V̇co₂ significantly greater in the older, compared to the younger, group. Ventilatory parameters are presented in Table 2. At similar levels of $\dot{\text{V}}\text{E}$, workload was ∼25% lower in the older group (P < 0.05, Table 2). V̇E/V̇E_max was higher, while C_dyn was lower in the older (P < 0.05, Table 2). Breathing at 70 and 100 L·min⁻¹ was attained by a greater f_b and smaller V_T in the older group, and this resulted in a shorter total time for any given respiratory cycle (P < 0.05). Furthermore, IRV was significantly smaller in the older group at 70 and 100 L·min⁻¹ whereas ERV was greater in the older group at 100 L·min⁻¹. Three of the eight older participants demonstrated EFL (range of EFL: 13%–27%) at a $\dot{\text{V}}\text{E}$ of 70 L·min⁻¹, and five of the eight older participants had EFL (range of EFL: 26%–62%) at 100 L·min⁻¹. Only one of the younger participants was flow limited at 100 L·min⁻¹ (EFL of 17%). Overall, the older participants presented with significantly greater EFL than the younger at a $\dot{\text{V}}\text{E}$ of 70 L·min⁻¹ (9 ± 11% versus 0%) and 100 L·min⁻¹ (22 ± 21% versus 5 ± 7%).

Table 2.

Respiratory and metabolic responses during exercise eliciting similar ventilatory rates between young and older participants

	∼40 L·min-1		∼70 L·min-1		∼100 L·min-1		P Value
	Younger	Older	Younger	Older	Younger	Older	Main Effect of Age	Main Effect of Stage	Interaction Effect
Respiratory Variables
V̇e (L/min)	42 ± 2	40 ± 5	70 ± 6	71 ± 5	101 ± 6	101 ± 9	0.87	<0.01	0.75
V̇e·V̇eMax-1 (%)	27 ± 4*	35 ± 7	45 ± 8*	62 ± 11	65 ± 9*	88 ± 11	<0.01	<0.01	<0.01
Fb (breaths/min)	22 ± 5	24 ± 5	27 ± 5*	32 ± 5	34 ± 4*	47 ± 12	0.03	<0.01	0.01
VT (L)	2.0 ± 0.6	1.7 ± 0.3	2.6 ± 0.5*	2.2 ± 0.4	3.1 ± 0.5*	2.2 ± 0.5	0.02	<0.01	0.14
Ttot (s)	2.9 ± 0.7	2.6 ± 0.4	2.3 ± 0.5*	1.8 ± 0.4	1.8 ± 0.2*	1.4 ± 0.3	0.04	<0.01	0.80
Ti (s)	1.3 ± 0.4	1.1 ± 0.2	1.0 ± 0.2	0.8 ± 0.2	0.8 ± 0.1*	0.6 ± 0.1	0.04	<0.01	0.71
Te (s)	1.6 ± 0.4	1.4 ± 0.2	1.3 ± 0.2*	1.0 ± 0.2	1.0 ± 0.2*	0.7 ± 0.2	0.04	<0.01	0.75
Ti·Ttot-1 (%)	43 ± 3	44 ± 2	44 ± 5	45 ± 4	47 ± 4	46 ± 3	0.86	<0.01	0.46
VT·Ti-1 (L/s)	1.6 ± 0.2	1.5 ± 0.2	2.7 ± 0.5	2.7 ± 0.4	3.7 ± 0.6	3.7 ± 0.4	0.85	<0.01	0.73
VT·Te-1 (L/s)	1.2 ± 0.1	1.2 ± 0.2	2.1 ± 0.1	2.2 ± 0.2	3.2 ± 0.3	3.2 ± 0.5	0.90	<0.01	0.61
IRV (%VC)	30 ± 9	24 ± 8	23 ± 10*	15 ± 7	20 ± 8*	9 ± 7	0.04	<0.01	0.24
ERV (%VC)	35 ± 9	36 ± 4	33 ± 6	39 ± 8	28 ± 7*	40 ± 6	0.08	0.38	<0.01
EFL (%)	0 ± 0	2 ± 4	0 ± 0*	9 ± 11	5 ± 7*	22 ± 21	0.02	<0.01	0.04
Cdyn (L/cmH2O)	0.30 ± 0.07*	0.22 ± 0.06	0.24 ± 0.03*	0.18 ± 0.05	0.23 ± 0.05*	0.17 ± 0.05	0.02	<0.01	0.80
Metabolic Variables
Workload (W)	94 ± 19	68 ± 21	173 ± 21*	128 ± 27	225 ± 28*	173 ± 31	<0.01	<0.01	0.07
HR (beats/min)	102 ± 17	106 ± 11	143 ± 16	135 ± 17	153 ± 17	145 ± 13	0.54	<0.01	0.37
V̇o2 (L/min)	1.4 ± 0.2	1.2 ± 0.3	2.4 ± 0.2*	2.1 ± 0.3	3.0 ± 0.3*	2.2 ± 0.4	0.01	<0.01	<0.01
V̇co2 (L/min)	1.3 ± 0.1	1.1 ± 0.2	2.4 ± 0.4	2.1 ± 0.3	3.3 ± 0.4*	2.7 ± 0.5	0.03	<0.01	0.10
RER	0.88 ± 0.08	0.88 ± 0.10	1.02 ± 0.10	1.07 ± 0.08	1.10 ± 0.09*	1.21 ± 0.10	0.26	<0.01	0.02
V̇e/V̇o2	25 ± 2*	31 ± 5	28 ± 2*	35 ± 5	32 ± 3*	42 ± 6	<0.01	<0.01	0.03
V̇e/V̇co2	29 ± 3*	35 ± 3	28 ± 3*	33 ± 4	29 ± 4*	35 ± 4	0.01	<0.01	0.60
Wb Components
Ir (J/L)	0.17 ± 0.03	0.16 ± 0.07	0.27 ± 0.05	0.30 ± 0.11	0.35 ± 0.05*	0.51 ± 0.19	0.15	<0.01	<0.01
Ie (J/L)	0.51 ± 0.17	0.68 ± 0.30	0.63 ± 0.18*	0.96 ± 0.35	0.71 ± 0.18*	1.23 ± 0.22	0.01	<0.01	<0.01
Er (J/L)	0.06 ± 0.04	0.05 ± 0.06	0.11 ± 0.07	0.08 ± 0.07	0.20 ± 0.10	0.17 ± 0.11	0.42	<0.01	0.91
Ee (J/L)	0.06 ± 0.09	0.05 ± 0.06	0.08 ± 0.06	0.03 ± 0.05	0.14 ± 0.10*	0.01 ± 0.01	0.06	0.16	<0.01
Total (J/L)	0.80 ± 0.09	0.94 ± 0.24	1.08 ± 0.17*	1.38 ± 0.34	1.41 ± 0.17*	1.92 ± 0.39	0.02	<0.01	<0.01

Data are mean ± SD. C_dyn, respiratory dynamic compliance; EFL, expiratory flow limitation; ERV, expiratory reserve volume as a percent of vital capacity; F_b, breathing frequency; HR, heart rate; IRV, inspiratory reserve volume as a percent of vital capacity; RER, respiratory exchange ratio; T_e, expiratory time; T_i, inspiratory time; T_tot, total time for one respiratory cycle; V̇co₂, carbon dioxide production; V̇e, minute ventilation; V̇e_Max, maximal V̇e; V̇e/V̇co₂, ventilatory equivalent for CO₂; V̇e/V̇o₂, ventilatory equivalent for O₂; V̇o₂, oxygen consumption; V_T, tidal volume; W_b, work of breathing. Data analyzed via 2-way analysis of variance for age and stage (n = 8).

*Significant difference between groups, P < 0.05.

The W_b is presented in Fig. 3, A–C. The total W_b was not different between younger and older participants at a $\dot{\text{V}}\text{E}$ of 40 L·min⁻¹ (P = 0.81), but was ∼40% greater in the older at 70 L·min⁻¹ and 100 L·min⁻¹ (P < 0.05, Fig. 3). Further analysis revealed a greater inspiratory elastic and resistive W_b (P < 0.05, Table 2), and lower expiratory elastic W_b, in the older group (P < 0.05, Table 2, Fig. 3).

Figure 3.

Data are mean ± SD. The work of breathing (W_b) per tidal volume (J·L⁻¹) between younger (black bars, n = 8) and older (gray bars, n = 8) participants during cycling exercise at matched ventilatory rates (A–C), matched metabolic rates (D–F), and matched operating lung volumes (G–I). Modified Campbell diagram analyses partitioned respiratory work into inspiratory [resistive (I_r), elastic (I_e)] and expiratory [resistive (E_r) and elastic (E_e)] work. A two-way mixed model ANOVA was performed for each variable within each condition and a Holm–Sidak post hoc was employed if a main effect was found. *Significant group difference, P < 0.05. ERV, expiratory reserve volume as percentage of VC; IRV, inspiratory reserve volume as percentage of VC; VC, vital capacity.

Matched Metabolic Rate

Stages eliciting a similar metabolic rate (${\dot{\text{V}}\text{O}}_{\text{2}}$) between groups (Table 3) were identified at 60 W (${\dot{\text{V}}\text{O}}_{\text{2}}$ range 1.13–1.73 L·min⁻¹ in younger and 1.02–1.86 L·min⁻¹ in older), 90 W (${\dot{\text{V}}\text{O}}_{\text{2}}$ range 1.45–1.98 L·min⁻¹ in younger and 1.22–2.13 L·min⁻¹ in older), and 120 W (${\dot{\text{V}}\text{O}}_{\text{2}}$ range 1.71–2.20 L·min⁻¹ in younger and 1.44–2.42 L·min⁻¹ in older). Heart rate and metabolic responses to exercise performed at matched ${\dot{\text{V}}\text{O}}_{\text{2}}$ values of 1.2, 1.6, and 1.9 L·min⁻¹ are presented in Table 3. Although there was no significant effect of age on HR, ${\dot{\text{V}}\text{O}}_{\text{2}}$, ${\dot{\text{V}}\text{CO}}_{\text{2}}$, or RER, $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{O}}_{\text{2}}$ and $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{CO}}_{\text{2}}$ were significantly greater in the older group (Table 3). Ventilatory parameters are presented in Table 2. Exercise at any given metabolic rate resulted in an increased f_b, ∼30% greater $\dot{\text{V}}\text{E}$ response, and lower IRV in the older group. Furthermore, C_dyn was reduced aging. There were no statistical differences in ERV or EFL between the two groups (P > 0.17). The W_b is presented in Fig. 3, D–F. Total W_b was ∼50% higher with aging (P < 0.05). Further analyses revealed that the increased W_b in the older group was due to a greater inspiratory elastic and resistive work; expiratory work was not different between the two age groups (P > 0.10).

Table 3.

Respiratory and metabolic responses during exercise eliciting similar metabolic rates between young and older participants

	60 W		90 W		120 W		P Value
	Younger	Older	Younger	Older	Younger	Older	Main Effect of Age	Main Effect of Stage	Interaction Effect
Respiratory Variables
V̇e (L/min)	31 ± 5	39 ± 10	41 ± 5*	51 ± 10	49 ± 5*	67 ± 16	<0.01	<0.01	0.32
V̇e·V̇EMax-1 (%)	26 ± 4*	39 ± 7	29 ± 4*	46 ± 10	35 ± 6*	57 ± 11	<0.01	<0.01	0.34
Fb (breaths/min)	19 ± 2	24 ± 7	20 ± 5*	28 ± 7	21 ± 4*	34 ± 13	0.00	0.05	0.37
VT (L)	1.7 ± 0.2	1.5 ± 0.3	2.1 ± 0.5	1.9 ± 0.3	2.4 ± 0.5	2.1 ± 0.3	0.25	<0.01	0.58
Ttot (s)	3.2 ± 0.3	2.6 ± 0.6	3.2 ± 1.2*	2.3 ± 0.5	3.0 ± 0.7*	2.0 ± 0.6	<0.01	0.18	0.75
Ti (s)	1.4 ± 0.2	1.1 ± 0.3	1.4 ± 0.7	1.0 ± 0.2	1.3 ± 0.3*	0.9 ± 0.2	0.01	0.46	0.67
Te (s)	1.9 ± 0.1	1.5 ± 0.3	1.8 ± 0.6*	1.3 ± 0.3	1.7 ± 0.4*	1.1 ± 0.3	<0.01	0.06	0.82
Ti·Ttot-1 (%)	42 ± 3	44 ± 2	44 ± 4	45 ± 2	44 ± 3	46 ± 3	0.10	0.08	0.86
VT·Ti-1 (L/s)	1.3 ± 0.2	1.5 ± 0.4	1.5 ± 0.3	1.9 ± 0.4	1.8 ± 0.3*	2.5 ± 0.6	<0.01	<0.01	0.45
VT·Te-1 (L/s)	0.9 ± 0.1	1.1 ± 0.3	1.2 ± 0.1*	1.6 ± 0.3	1.5 ± 0.1*	2.1 ± 0.5	<0.01	<0.01	0.28
IRV (%VC)	35 ± 6*	25 ± 9	30 ± 10*	19 ± 6	27 ± 9*	16 ± 6	0.01	<0.01	0.92
ERV (%VC)	36 ± 8	37 ± 3	36 ± 8	38 ± 5	34 ± 9	38 ± 5	0.52	0.33	0.08
EFL (%)	0 ± 0	1 ± 3	0 ± 0	5 ± 10	0 ± 0	6 ± 11	0.17	0.09	0.09
Cdyn (L/cmH2O)	0.35 ± 0.06*	0.26 ± 0.11	0.29 ± 0.05*	0.21 ± 0.06	0.28 ± 0.06*	0.21 ± 0.07	0.02	<0.01	0.79
Metabolic Variables
Workload (W)	60	60	90	90	120	120
HR (beats/min)	105 ± 16	104 ± 7	111 ± 14	114 ± 8	124 ± 10	130 ± 14	0.43	<0.01	0.40
V̇o2 (L/min)	1.2 ± 0.3	1.1 ± 0.3	1.7 ± 0.2	1.5 ± 0.3	1.9 ± 0.2	1.8 ± 0.3	0.37	<0.01	0.43
V̇co2 (L/min)	1.1 ± 0.3	0.9 ± 0.2	1.5 ± 0.2	1.4 ± 0.3	1.8 ± 0.2	1.8 ± 0.3	0.71	<0.01	0.09
RER	0.90 ± 0.11	0.87 ± 0.09	0.90 ± 0.07	0.93 ± 0.09	0.94 ± 0.07	1.00 ± 0.09	0.34	<0.01	0.22
V̇e/V̇o2	29 ± 5*	33 ± 6	24 ± 2*	32 ± 4	25 ± 2*	33 ± 6	0.01	0.23	0.73
V̇e/V̇co2	33 ± 6*	37 ± 5	27 ± 1*	34 ± 3	27 ± 1*	33 ± 4	<0.01	0.00	0.65
Wb Components
Ir (J/L)	0.12 ± 0.04	0.16 ± 0.06	0.17 ± 0.04	0.22 ± 0.08	0.18 ± 0.04*	0.30 ± 0.14	0.06	<0.01	0.04
Ie (J/L)	0.37 ± 0.19*	0.63 ± 0.26	0.52 ± 0.14*	0.82 ± 0.25	0.54 ± 0.16*	0.92 ± 0.28	0.01	<0.01	0.30
Er (J/L)	0.05 ± 0.04	0.04 ± 0.06	0.05 ± 0.03	0.04 ± 0.04	0.07 ± 0.03	0.09 ± 0.08	0.99	<0.01	0.30
Ee (J/L)	0.07 ± 0.10	0.05 ± 0.07	0.05 ± 0.08	0.02 ± 0.03	0.07 ± 0.08	0.02 ± 0.03	0.33	0.05	0.40
Total (J/L)	0.62 ± 0.15*	0.88 ± 0.19	0.79 ± 0.09*	1.11 ± 0.20	0.86 ± 0.10*	1.33 ± 0.31	<0.01	<0.01	0.08

Data are mean ± SD. C_dyn, respiratory dynamic compliance; EFL, expiratory flow limitation; ERV, expiratory reserve volume as a percent of vital capacity; F_b, breathing frequency; HR, heart rate; IRV, inspiratory reserve volume as a percent of vital capacity; RER, respiratory exchange ratio; T_e, expiratory time; T_i, inspiratory time; T_tot, total time for one respiratory cycle; V̇co₂, carbon dioxide production; V̇e, minute ventilation; V̇e_Max maximal V̇e; V̇e/V̇co₂, ventilatory equivalent for CO₂; V̇e/V̇o₂, ventilatory equivalent for O₂; V̇o₂, oxygen consumption; V_T, tidal volume; W_b, work of breathing. Data analyzed via 2-way analysis of variance for age and stage (n = 8).

*Significant difference between groups, P < 0.05.

Matched Operating Lung Volume

Stages eliciting similar lung volumes (IRV and ERV) between groups (Table 4) were identified using relative exercise intensities of 50% (IRV range 15%–34% in younger and 17%–41% in older; ERV range 23%–40% in younger and 22%–47% in older), 80% (IRV range 6%–32% in younger and 4%–29% in older; ERV range 19%–38% in younger and 25%–46% in older), and 100% W_peak (IRV range 7%–23% in younger and 2%–26% in older; ERV range 23%–42% in younger and 20%–46% in older). Heart rate and metabolic responses to exercise performed when operating lung volumes were similar are presented in Table 4. There was no effect of age on RER, $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{O}}_{\text{2}}$, or $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{CO}}_{\text{2}}$. However, HR, ${\dot{\text{V}}\text{O}}_{\text{2}}$, and ${\dot{\text{V}}\text{CO}}_{\text{2}}$ were significantly lower in the older group. Ventilatory parameters are presented in Table 4. Despite similar f_b in both age groups, the older group demonstrated a lower V_T resulting in a ∼25% lower $\dot{\text{V}}\text{E}$. EFL and C_dyn were not different between groups (P > 0.17). The W_b is presented in Fig. 3, G–I. Total W_b (P = 0.86) was not different between groups (Fig. 3).

DISCUSSION

It was the goal of this investigation to examine the impact of aging on the W_b during exercise evoking similar ventilatory rates, similar metabolic rates, or similar operating lung volumes in younger and older individuals. By focusing on W_b, instead of, as previously done, the P_b, this study demonstrates that healthy aging exaggerates the energetic cost to move a given volume of air at a given ventilatory rate (at which metabolic rate and IRV are lower in the elderly). This age-related difference in the W_b was, based on the modified Campbell diagram analysis, mainly due to the augmented elastic and resistive inspiratory work which likely resulted from the compromised respiratory compliance and the higher operating lung volume in the elderly. A greater W_b (increased inspiratory elastic and resistive work) with aging was also observed during exercise at a given metabolic rate, at which ventilatory rates were higher, and IRV lower, in the elderly. However, during exercise characterized by similar lung volumes in younger and older participants (at which metabolic rate and ventilatory rate were lower in the elderly), total W_b was found to be similar between groups. This novel finding suggests that the age-related difference observed at matched metabolic and at matched ventilatory rates is, at least in part, attributable to differences in lung volumes, i.e., a lower IRV, in the elderly. Taken together, the current findings highlight the significance of operating lung volumes in influencing the difference in W_b between healthy younger and older individuals.

Ventilatory, Metabolic, and Operating Lung Volume Response to Cycling Exercise

Compared to their younger counterparts, W_peak, ${\dot{\text{V}}\text{O}}_{\text{2}}{}_{\text{max}}$, and peak ventilatory rate were ∼30% lower in the older participants (Table 4, 100% W_peak column), a difference which is in line with earlier findings (8, 24, 30). Although age-related reductions in lung elastic recoil impair expiratory flow generation (e.g., FEF_25-75, Table 1) and limit V̇E_Max during exercise (10), the ventilatory demand declines at a similar, or even greater, rate with aging such that the maximal metabolic demand does not typically exceed maximal exercising ventilatory capacity (31). Therefore, the age-related decline in ventilatory capacity is presumed to play a minor role in the decrease in exercise capacity associated with healthy aging. Indeed, despite the decline in maximal ventilatory capacity, the older adults were characterized by an augmented ventilatory response to any given metabolic rate (i.e., increased $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{CO}}_{\text{2}}$ and $\dot{\text{V}}\text{E}$/${\dot{\text{V}}\text{O}}_{\text{2}}$, Table 3). This augmented ventilation is considered a necessary adjustment compensating for the inefficiency in gas exchange typical for older individuals (7, 32, 33).

To compare W_b between the younger and the older group at a given ventilatory rate, participants performed incremental cycling exercise which was used to identify three different levels of $\dot{\text{V}}\text{E}$ achieved by all participants (40, 70, and 100 L·min⁻¹). The older individuals exercising at these ventilatory rates had a ∼27% lower power output and metabolic rate, and an increased operating lung volume. Compared with the young, the older participants achieved these ventilatory rates with a significantly greater f_b combined with a lower V_T. This ventilatory strategy resulted in a lower IRV (i.e., higher relative lung volume) and increased V̇e/V̇E_Max and ERV in the older group (Table 2). Importantly, at these levels of V_E, ERV was not different from rest in the older participants (P > 0.25), although a significant reduction was observed in the young. One reason for the lack of change in the older group may be due to the relatively high relative $\dot{\text{V}}\text{E}$ values examined in the current study, which was not lower than ∼40 L·min⁻¹, or ∼40% maximal $\dot{\text{V}}\text{E}$ in the old group. Indeed, ERV has been shown to be similar to resting values in older individuals at $\dot{\text{V}}\text{E}$ values of ≥50 L·min⁻¹ (24). Although EFLs were not present at 40 and 70 L·min⁻¹ in the younger, and only minimal at 100 L·min⁻¹, older participants experienced considerably greater EFL at all ventilatory rates (Table 2), a finding consistent with previous literature (8, 9, 24, 32). Importantly, although controversial (8, 9, 32), EFL, or impending EFL, has been suggested to influence operating lung volumes during exercise (34, 35). Thus, older participants in the current study may have increased lung volume to avoid a greater magnitude of EFL.

To compare the impact of aging on the W_b during exercise at a given metabolic rate, the younger participants cycled at the same workload as the older participants (i.e., 60, 90, and 120 W; corresponding to a ${\dot{\text{V}}\text{O}}_{\text{2}}$ of ∼1.2, 1.6, and 1.9 L·min⁻¹). At any given ${\dot{\text{V}}\text{O}}_{\text{2}}$ (Table 3), the elderly were, primarily due to a greater f_b, characterized by a ∼30% higher ventilatory rate, a lower IRV, and considerable EFL. Finally, cycling workloads corresponding to similar percentages of W_peak in younger and older participants were chosen to compare the impact of aging on W_b during exercise at given operating lung volumes. When IRV and ERV were similar between groups, both the metabolic requirement and the ventilatory response were lower in the older group (Table 4).

Impact of Aging on W_b

The total W_b at a given ventilatory and metabolic rate was augmented in older participants. This somewhat confirms previous work suggesting greater P_b at matched ventilatory rates in older individuals (8, 9, 36). However, it is important to recognize that the P_b can be influenced by a tachynpeic breathing pattern, which is characteristic of the elderly (7), making it unclear as to whether the age-related difference in P_b was due to ventilatory strategy (i.e., f_b), or a difference in the energetic cost to move a given volume of air during exercise. By examining the W_b, the current study addresses this point and demonstrates that aging is associated with a greater energetic cost to move a given volume of air during exercise eliciting a given V_E or metabolic rate. Furthermore, this study shows, for the first time, that the age-related difference in total W_b is abolished when lung volumes are similar during exercise in younger and older individuals (Fig. 3). Overall, these findings suggest that the greater total P_b in previous studies, and greater W_b in the current study, observed at a given ventilatory or metabolic rate with aging is, at least in part, related to an earlier shift toward a higher operating lung volume with aging.

Elastic Work

The elastic work of breathing represents the work needed to overcome chest wall stiffness and inward lung recoil during inspiration and outward chest wall recoil during expiration. The older participants displayed a greater inspiratory elastic work during exercise at any given ventilatory rate, confirming previous findings (8, 9), and at any given metabolic rate (Fig. 3). This difference likely resulted from the age-related decrease in respiratory compliance (Table 2,3), which occurs due to increases in chest wall stiffness (37) and the loss in lung elastic recoil (38). Furthermore, based on the sigmoidal relationship between respiratory compliance and lung volume (as a percentage of vital capacity, Ref. 39), and the age-related increase in lung volume at any given ventilatory and metabolic rate (Tables 2 and 3), the older presumably operated on a stiffer portion of the respiratory compliance curve, which likely also contributed to the higher inspiratory elastic work compared to the younger participants. This, however, remains speculative as static respiratory compliance was not quantified in the current study. Regardless, when C_dyn was similar between groups, as during the similar lung volume comparisons (Table 4), the difference in inspiratory elastic work was no longer observed.

Expiratory elastic work during exercise at a given ventilatory rate was lower with aging (Fig. 3). Specifically, the expiratory elastic component accounted for ∼8% of the total W_b in the younger group, while only contributing ∼2% in the older group. One potential explanation is that an increase in end-expiratory lung volume relative to FRC with aging would, based on the modified Campbell analysis, reduce the work performed against chest wall recoil and decrease the contribution of expiratory elastic work. Indeed, when examined at a similar V_E, older adults did not decrease ERV (i.e., end-expiratory lung volume relative to VC) from rest as observed in the younger group. Furthermore, three of those older adults demonstrated hyperinflation during exercise (an increase in ERV ≥ 0.15 L from rest, Ref. 8). Another potential contribution to the age-related difference in expiratory elastic work is that, due to parallel displacement of the static pressure-volume curve of the chest wall (36), end-inspiratory lung volume may lie above the intrinsic relaxation volume of the chest wall in the older adults. This would result in greater stored potential energy of the chest wall, which is then utilized to drive expiration, and thereby reduce expiratory elastic work (36).

Resistive Work

Aging amplified inspiratory resistive work during exercise at any given metabolic and ventilatory rate (Fig. 3). The observed difference at a given metabolic rate can partly be explained by the higher ventilatory and mean inspiratory flow rates (i.e., V_T/T_i) in the older participants. However, interestingly, even when ventilatory and mean inspiratory flow rates were the same in both groups (i.e., at 70 and 100 L·min⁻¹), the difference persisted, suggesting that the higher inspiratory resistive work with aging likely also results from the age-related reduction in airway size and the associated increase in airway resistance (40, 41). Finally, although inspiratory resistive work was similar in both groups during exercise performed at the same lung volumes, mean inspiratory flow rates (i.e., V_T/T_i) were ∼25% lower in the older group (Table 4), a difference which further suggests that aging increases the inspiratory resistive work required for a given inspiratory flow.

Expiratory resistive work was not different between groups at any comparison (Fig. 3). Interestingly, this lack of a difference occurred despite more EFL in the older group at any given ventilatory rate (Table 2), a factor which has been suggested to increase the expiratory resistive work by augmenting airway resistance secondary to the dynamic compression of small airways (9). However, since EFL does not necessarily affect transpulmonary pressures (i.e., pressure generated without a subsequent change in flow rate) in younger (35) or older (42) adults, the actual impact of EFL on expiratory resistive work is rather unclear. It is, in this context, also important to mention that EFL may have been slightly overestimated in both groups as postexercise MFVLs do not inherently account for thoracic gas compression (22). Regardless, the similar expiratory resistive work at a given ventilation is in contrast to an earlier study reporting age-related increases in the P_b at matched ventilations (9). Although the exact reasons remain unknown, the discrepancy might be, at least in part, explained by the fact that the current study utilized the modified Campbell diagram. Specifically, decreases in chest wall compliance, as associated with aging, reduce the relative contribution of expiratory resistive work (43) when using the modified Campbell diagram, an effect which is not appreciated when utilizing other methods (44).

Finally, this investigation has certain limitations that need to be considered. First, healthy aging might affect the W_b during exercise differently in men compared to women (12, 45). Since the data presented here are based on adult males, inferences for the female population might be limited. Second, similar to previous investigations (12, 46), chest wall compliance for all participants was estimated based on earlier findings (1). Although this introduces a potential source of error, the actual consequence for the quantification of the W_b is likely negligible, as a 12% difference between estimated and measured chest wall compliance has been shown to influence inspiratory elastic and expiratory resistive work by only ±5% when using the modified Campbell diagram analysis in young participants (43). Whether this holds true in older populations is not known. Third, residual volume was not measured in the current study, limiting the presentation of lung volume, similar to previous studies, to a percentage of vital capacity (24–27). However, as residual volume generally increases with aging (18), this could mean that, despite operating at a similar percentage of FVC, the absolute lung volume may have been higher in the older group. Finally, despite the absence of a statistically significant group difference in operating lung volumes, subtle differences could have considerably influenced this comparison.

Summary and Conclusions

This study compared the impact of aging on the resistive and elastic components of respiratory work during exercise performed at given ventilatory and metabolic rates, and at given operating lung volumes. Aging augmented total W_b primarily through inspiratory elastic and resistive sources during exercise at matched ventilatory and metabolic rates. As the age-related differences in total W_b were abolished when operating lung volumes were similar between groups, the current findings suggest that the greater total W_b observed in older individuals at a given ventilatory or metabolic rate is, at least in part, related to the elderly’s earlier shift toward a higher inspiratory lung volume.

GRANTS

This study was supported by the National Heart, Lung, and Blood Institute (HL-116579 and HL-139451) and the Veterans Affairs Rehabilitation Research and Development (E3343-R).

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the authors.

AUTHOR CONTRIBUTIONS

J.C.W. and M.A. conceived and designed research; J.C.W., T.J.H., J.R.G., S.A., H-Y.W., and R.H.J. performed experiments; J.C.W. and S.A. analyzed data; J.C.W. and M.A. interpreted results of experiments; J.C.W. prepared figures; J.C.W. drafted manuscript; J.C.W., T.S.T., T.J.H., J.R.G., S.A., H-Y.W., R.H.J., and M.A. edited and revised manuscript; J.C.W., T.S.T., T.J.H., J.R.G., S.A., H-Y.W., R.H.J., and M.A. approved final version of manuscript.