Resistive and elastic work of breathing in older and younger adults during exercise

Abstract

It is unknown whether the greater total work of breathing (WOB) with aging is due to greater elastic and/or resistive WOB. We hypothesized that older compared with younger adults would exhibit a greater total WOB at matched ventilations (V̇e) during graded exercise, secondary to greater inspiratory resistive and elastic as well as expiratory resistive WOB. Older (OA: 60 ± 8 yr; n = 9) and younger (YA: 38 ± 7 yr; n = 9) adults performed an incremental cycling test to volitional fatigue. Esophageal pressure, inspiratory (IRV) and expiratory reserve volumes (ERV), expiratory flow limitation (EFL), and ventilatory variables were measured at matched V̇e (i.e., 25, 50, and 75 l/min) during exercise. The inspiratory resistive and elastic as well as expiratory resistive WOB were quantified using the Otis method. At V̇e of 75 l/min, older adults had greater %EFL and larger tidal volumes to inspiratory capacity but smaller relative IRV (P ≤ 0.03) than younger adults. Older compared with younger adults had greater total WOB at V̇_E of 50 and 75 l/min (OA: 90 ± 43 vs. YA: 49 ± 21 J/min; P < 0.04 for both). At V̇e of 75 l/min, older adults had greater inspiratory elastic and resistive WOB (OA: 44 ± 27 vs. YA: 24 ± 22 and OA: 23 ± 15 vs. YA: 11 ± 3 J/min, respectively, P < 0.03 for both) and expiratory resistive WOB (OA: 23 ± 19 vs. YA: 14 ± 9 J/min, P = 0.02) than younger adults. These data demonstrate that aging-induced pulmonary alterations result in greater inspiratory elastic and resistive as well as expiratory resistive WOB, which may have implications for the integrated response during exercise.

NEW & NOTEWORTHY Aging-induced changes to the pulmonary system result in increased work of breathing (WOB) during exercise. However, it is not known whether this higher WOB with aging is due to differences in elastic and/or resistive WOB. Herein, we demonstrate that older adults exhibited greater inspiratory elastic and resistive as well as expiratory resistive WOB during exercise.

INTRODUCTION

Aging results in significant alterations in the structure and function of the pulmonary system. For example, aging is associated with the loss of lung elastic recoil and stiffening of the chest wall as well as decreased maximum respiratory pressure-generating capacity, airway caliber, and expiratory flow rates (18, 20, 24, 34). These structural and functional changes with aging have important implications during exercise. Specifically, older adults exhibit greater expiratory flow limitation (EFL) (7, 12, 27, 35, 45) and increased operating lung volumes than younger adults (7, 27, 35, 45) during exercise, and consequently the total work of breathing (WOB) has been shown to be greater (4, 20, 33). In fact, a recent study found that older adults have a greater total WOB compared with younger adults at ventilations (V̇e) >60 l/min (33). Because peak oxygen uptake (V̇o₂) and cardiac output reserve are diminished with aging, the elevated WOB has important implications as it will necessitate greater V̇o₂ and blood flow to the respiratory muscles at the expense of other organ systems (e.g., locomotor muscles) (19, 36, 44).

To better understand the mechanisms responsible for the elevated WOB with aging, the total WOB can be partitioned into the inspiratory and expiratory resistive as well as the inspiratory and expiratory elastic WOB. Specifically, the inspiratory and expiratory resistive WOB is the work required to overcome airway resistance during inspiration and expiration, respectively. The inspiratory elastic WOB is the work required to overcome the elasticity of the lung and chest wall (i.e., total respiratory system) during inspiration, whereas the expiratory elastic WOB is the work required to overcome the outward chest wall elasticity during expiration, when end-expiratory lung volume (EELV) is below functional residual capacity. Thus, the smaller airways and greater mechanical constraints during exercise likely result in increased resistive WOB in the older compared with the younger adults. Furthermore, the elevated operating lung volumes will likely lead to greater inspiratory elastic WOB during exercise in the older adults. Therefore, the purpose of this study was to comprehensively examine the WOB and its components at matched V̇e in younger and older adults. We hypothesized that older compared with younger adults will have greater total WOB for a matched V̇e arising from a greater resistive and elastic WOB.

METHODS

Eighteen older (n = 9; 9 men/0 women) and younger (n = 9; 6 men/3 women) adults matched for height and percent predicted pulmonary function were recruited to participate in this study. Exclusion criteria included the existence of acute or chronic pulmonary, cardiovascular, muscular, and/or metabolic disease. Furthermore, none of the participants were currently taking prescription medication for pulmonary, cardiovascular, muscular, and/or metabolic diseases. The younger women (n = 3) were tested randomly throughout their menstrual cycle, as female sex hormones do not influence exercising V̇e (or breathing strategy) (26, 41). Following written and verbal description of the study requirements, all participants provided written, informed consent. All aspects of this study were approved by the Mayo Clinic Institutional Review Board and conformed to the principles outlined in the Declaration of Helsinki.

Experimental design.

For this cross-sectional study, participants performed all measurements on one study visit. Participants were first familiarized with all experimental measures and protocols and then performed an incremental exercise test to exhaustion. During the incremental exercise test, participants performed inspiratory capacity (IC) maneuvers to determine inspiratory and expiratory reserve volumes (IRV and ERV) and EFL and esophageal pressure was measured for the determination of WOB. The older and younger groups were compared at rest and at matched V̇e of ∼25, 50, and 75 l/min as 75 l/min was the highest V̇e reached by all participants. Ventilatory variables and respiratory mechanics associated with each of these V̇e were compared.

Peak oxygen uptake test.

Participants performed the incremental test to determine V̇o_2peak on an electronically braked upright cycle ergometer (Lode Corival, Groningen, The Netherlands). The incremental cycling test consisted of increasing workloads in 25- to 40-W increments based on the participants’ perceived peak exercise workload. During the incremental cycling test, participants were instructed to stay seated and maintain 60–80 rpm. Ventilatory and gas exchange variables were collected during the incremental cycling test (MedGraphics CPX/D, St. Paul, MN) and averaged over 30 s. Heart rate was collected continuously and recorded at the end of each stage. Percent predicted V̇o_2peak was calculated from Hansen et al. (17).

Pulmonary function tests.

Participants performed pulmonary function tests according to ATS/ERS guidelines (31). Multiple maximum flow-volume loops (MFVL) were performed (from total lung capacity to residual volume) before and immediately following exercise, with the largest MFVL used for analysis (postexercise). Forced vital capacity (FVC), forced expiratory volume in 1 s (FEV₁), peak expiratory flow (PEF), FEV₁/FVC and percent predicted values are reported (25).

Respiratory pressure.

Esophageal pressure was measured using a latex balloon-tip catheter (CooperSurgical, Trumbull, CT) inserted via the nares ∼45 cm following local anesthetic. The balloon was inflated with 1 ml of air, and correct placement (i.e., lower one-third of the esophagus) was verified using the “occlusion” method (3). Mouth pressure was measured via a lateral port in the mouthpiece. The catheters were connected to a differential pressure transducer (MP45; Validyne Engineering Corporation, Northridge, CA) and calibrated using a water manometer before each test. Transpulmonary pressure (Ptp) was calculated by subtracting esophageal from mouth pressure.

Respiratory mechanics.

Prior to exercise, participants performed multiple IC maneuvers until the maneuvers were valid and consistent. At the end of each workload, participants performed an IC from end-expiratory lung volume (EELV) to determine placement of tidal volumes (V_T). A “typical” breath was determined if it had similar volume, pressure, and flow characteristics to the previous breaths before the IC maneuver. A computer program was used to correct for physiological drift during exercise (i.e., when there were unequal inspiratory and expiration volumes) using the IC ratio method described by Dolmage and Goldstein (9). Total lung capacity was assumed not to significantly change during exercise (21, 22). ERV was determined by subtracting IC from FVC, and IRV was determined by subtracting the sum of ERV and V_T from FVC. ERV and IRV were expressed as a percentage of FVC. EFL was quantified as the percentage of the V_T loop that met or exceeded the MFVL (5, 6, 23, 45, 46). EFL was determined to be present when the exercising V_T intersected with the MFVL by ≥10%. Pressure-volume loops from eight to 10 breaths (corresponding to the flow vs. volume loops discussed above) were selected for each participant at each matched V̇e and averaged. For each V_T loop, dynamic lung compliance (C_L,dyn) was determined by dividing V_T by the change in Ptp between points of zero-flow during inspiration (i.e., end-inspiratory lung volume and EELV). In the present study, the Otis method was used instead of other methodologies (e.g., integrating the area of the pressure-volume loop) because it allows for the components of WOB to be determined. Therefore, the Otis method was used to determine the inspiratory and expiratory resistive and inspiratory elastic work of the lung at matched V̇e for each subject (Fig. 1) (30, 37). However, as conventionally used, we will refer to the work of the lung as WOB (2, 8). For this method of calculating WOB, the Ptp-volume loop was plotted and C_L,dyn determined, allowing for calculation of the inspiratory resistive, expiratory resistive, and inspiratory elastic WOB. The inspiratory resistive WOB was calculated as the integrated area between the dynamic Ptp tracing and the line given by C_L,dyn during inspiration. The expiratory resistive WOB was calculated as the integrated area between the dynamic Ptp tracing and the ordinate axis when Ptp was <0 cmH₂O. The inspiratory elastic WOB was calculated as the integrated area between the ordinate axis (i.e., 0 cmH₂O) and the line given by C_L,dyn when Ptp was >0 cmH₂O during inspiration. For each breath, the WOB was calculated and then averaged. WOB was multiplied by breathing frequency (f_B) and reported as J/min.

Fig. 1.

Example of the quantification of work of breathing (WOB) using the Otis method. Diagonally hatched area represents the inspiratory resistive WOB. Stippled area represents the inspiratory elastic WOB. Horizontally hatched area represents the expiratory resistive WOB. ○, Zero-flow points during the tidal breath. Ptp, transpulmonary pressure.

Statistical analysis.

Values are reported as means ± SD. Statistical analyses were performed using SigmaStat 2.0 (Jandel Scientific, San Rafael, CA). Participant characteristics and peak exercise data were compared using unpaired t-tests. Ventilatory variables and WOB were compared within (V̇e at rest, 25, and 50, vs. 75 l/min) and between (older vs. younger adults) via two-way mixed-factorial analysis of variance, and Tukey’s post hoc analysis was performed to determine where significant differences existed. Relationships were determined via linear regression. Statistical significance was set at P < 0.05.

RESULTS

Participant characteristics.

Older adults were significantly older and heavier and had a higher BMI than the younger adults (Table 1). FVC and FEV₁ were lower in the older compared with younger adults, whereas FEV₁/FVC, PEF, and percent predicted values were not different between groups. Older adults had a lower peak V̇o₂ (relative), V̇co₂, heart rate (HR), and inspiratory time-to-total time ratio (Ti/Ttot) than younger adults (Table 2). Peak V̇e/V̇o₂ and V̇e/V̇co₂ were higher in the older than younger adults.

Table 1.

Participant characteristics

	Older Adults	Younger Adults	P Value
Men/Women	9/0	6/3
Age, yr	60 ± 8*	38 ± 7	<0.01
Height, cm	175 ± 6	179 ± 8	0.27
Weight (kg)	87 ± 9*	79 ± 8	0.05
BMI, kg/m2	29 ± 4*	25 ± 2	0.02
FVC, liters	4.3 ± 0.9*	5.5 ± 0.9	0.01
%Predicted	103 ± 14	108 ± 13	0.38
FEV1, liters	3.6 ± 0.6*	4.8 ± 0.8	<0.01
%Predicted	110 ± 10	118 ± 14	0.23
FEV1/FVC, %	86 ± 14	87 ± 5	0.74
PEF, l/s	9.6 ± 1.1	10.0 ± 1.8	0.52
%Predicted	115 ± 12	105 ± 15	0.17

Values are means ± SD. BMI, body mass index; FVC, forced vital capacity; FEV₁, forced expiratory volume in 1 s; PEF, peak expiratory flow.

^*Significantly different than younger adults.

Table 2.

Peak exercise data

	Older Adults	Younger Adults	P Value
V̇o2, ml·kg−1·min−1	30 ± 11*	42 ± 7	0.01
V̇o2 (% predicted)	103 ± 38	114 ± 22	0.46
V̇o2, l/min	2.6 ± 1.1	3.3 ± 0.9	0.13
V̇co2, l/min	2.8 ± 1.0*	3.7 ± 0.8	0.05
RER	1.11 ± 0.10	1.11 ± 0.09	0.98
HR, beats/min	146 ± 20*	172 ± 16	<0.01
HR (% predicted)	92 ± 13	94 ± 7	0.59
V̇e, l/min	116 ± 26	127 ± 52	0.57
VT, liters	2.9 ± 0.8	3.2 ± 0.7	0.48
fB, breaths/min	40 ± 8	40 ± 13	0.98
V̇e /V̇o2	51 ± 18*	38 ± 10	0.04
V̇e/V̇co2	46 ± 17*	34 ± 9	0.04
Ti, s	0.73 ± 0.12	0.83 ± 0.26	0.27
Te, s	0.82 ± 0.18	0.81 ± 0.28	0.88
Ti/Ttot	0.46 ± 0.05*	0.51 ± 0.03	0.04
Workload (W)	194 ± 85	258 ± 68	0.10

Values are means ± SD. f_B, breathing frequency; RER, respiratory exchange ratio; Te, expiratory time; Ti, inspiratory time; Ti/Ttot, Ti-to-total time ratio; V̇co₂, carbon dioxide production; V̇e, ventilation; V̇o₂, oxygen uptake; V_T, tidal volume; V̇e/V̇co₂, ventilatory equivalence for V̇co₂; V̇e/V̇o₂, ventilatory equivalence for V̇o₂;

^*Significantly different than younger adults.

Ventilatory response, EFL, and operating lung volumes.

V_T, f_B, Te, V_T/Ti, and V_T/Te were not significantly different among groups across V̇e (P > 0.06) (Table 3). At rest (i.e., V̇e of ∼13 l/min), older adults had lower Ti and Ti/Ttot compared with younger adults (both P < 0.02). At V̇_E of 75 l/min, C_L,dyn was lower in the older compared with younger adults (P < 0.04). Figure 2 shows the severity of EFL (Fig. 2A), V_T/IC (Fig. 2B), IRV (%FVC) (Fig. 2C), and ERV (%FVC) (Fig. 2D) at matched V̇e. At V̇e of 75 l/min, four of nine (44%) of the older adults exhibited EFL, whereas one of nine (11%) younger adults exhibited EFL. Older adults had a greater severity of EFL at V̇e of 75 (P = 0.03) but not 25 or 50 l/min (P > 0.14). Older adults had greater V_T/IC at V̇e of 50 and 75 l/min compared with the younger adults (P < 0.03). At rest, relative IRV was greater in older compared with younger adults (P < 0.01). Older adults had less relative IRV at V̇e of 75 l/min (P = 0.03), whereas no differences were present at V̇e of 25 or 50 l/min (P > 0.28). Older adults had a lower relative ERV than younger adults at rest and V̇e of 25 l/min (both P = 0.01), whereas no differences were present at V̇e of 50 or 75 l/min (P > 0.07). Compared with rest, relative ERV was lower in the younger adults at V̇e of 25, 50, and 75 l/min (P < 0.05), whereas these differences were not present in the older adults (P > 0.84).

Table 3.

Breathing strategy at matched V̇e

	Resting		25 l/min		50 l/min		75 l/min
	Older Adults	Younger Adults	Older Adults	Younger Adults	Older Adults	Younger Adults	Older Adults	Younger Adults
V̇e, l/min	13 ± 2	13 ± 3	25 ± 1	26 ± 3	50 ± 1	51 ± 3	74 ± 4	74 ± 7
VT, liters	0.9 ± 0.3	0.9 ± 0.2	1.2 ± 0.1	1.2 ± 0.3	2.0 ± 1.7	2.1 ± 0.3	2.4 ± 0.2	2.7 ± 0.9
fB, breaths/min	17 ± 5	16 ± 4	21 ± 2	22 ± 5	25 ± 2	25 ± 4	31 ± 3	28 ± 5
Ti, s	1.47 ± 0.61*	2.00 ± 0.98	1.31 ± 0.23	1.35 ± 0.33	1.12 ± 0.17	1.17 ± 0.18	0.89 ± 0.15	1.05 ± 0.19
Te, s	2.10 ± 0.53	2.07 ± 0.34	1.68 ± 0.16	1.54 ± 0.34	1.33 ± 0.11	1.31 ± 0.17	1.06 ± 0.09	1.12 ± 0.16
Ti/Ttot	0.40 ± 0.06*	0.46 ± 0.09	0.43 ± 0.03	0.46 ± 0.03	0.46 ± 0.03	0.47 ± 0.02	0.45 ± 0.04	0.48 ± 0.02
VT/Ti, l/s	0.63 ± 0.10	0.59 ± 0.36	0.95 ± 0.08	0.93 ± 0.10	1.81 ± 0.15	1.81 ± 0.12	2.73 ± 0.28	2.55 ± 0.26
VT/Te, l/s	0.42 ± 0.10	0.44 ± 0.10	0.73 ± 0.05	0.81 ± 0.10	1.52 ± 0.09	1.63 ± 0.13	2.26 ± 0.23	2.40 ± 0.23
CL,dyn, ml/cmH2O	291 ± 132	325 ± 84	278 ± 114	335 ± 97	283 ± 128	354 ± 130	257 ± 129*	368 ± 180

Values are means ± SD. C_L,dyn, dynamic lung compliance; ERV, expiratory reserve volume; f_B, breathing frequency; IRV, inspiratory reserve volume; Ti, inspiratory time; Te, expiratory time; Ti/Ttot, Ti-to-total time ratio; V̇e, ventilation; V_T, tidal volume; V_T/Te, mean expiratory flow;V_T/Ti, mean inspiratory flow;

^*Significantly different from younger adults.

Fig. 2.

Expiratory flow limitation (EFL), V_T/inspiratory capacity (IC), and operating lung volumes in older and younger adults Mean EFL severity (A), V_T/IC (B), inspiratory reserve volumes (IRV) [forced vital capacity (%FVC)] (C), and expiratory reserve volumes (ERV) (%FVC) (D) in older (○) and younger (●) adults. At ventilations (V̇e) of 75 l/min, older adults had greater EFL than younger adults (P = 0.03). At V̇e of 50 and 75 l/min, V_T/IC was greater in the older than younger adults (P < 0.03). IRV (%FVC) was less in the older compared with younger adults at V̇e of 75 l/min (P = 0.03). At rest and V̇e of 25 l/min, ERV (%FVC) was less in the older than younger adults (P = 0.01). *Significantly different from younger adults.

Work of breathing.

Total WOB at matched V̇e is shown in Fig. 3. Older adults had a greater total WOB at V̇e of 50 and 75 l/min (P < 0.04). Figure 4 shows the inspiratory elastic (Fig. 4A), inspiratory resistive (Fig. 4B), and expiratory resistive (Fig. 4C) WOB at matched V̇e. Inspiratory elastic WOB was greater in the older than younger adults at V̇e of 75 (P < 0.01), but not 25 or 50 l/min (P > 0.13). Older adults had a greater inspiratory resistive WOB than younger adults at V̇e of 50 and 75 l/min (both P < 0.03). Older adults had a greater expiratory resistive WOB at V̇e of 75 l/min (P = 0.02), with no other differences present (P > 0.49). Figure 5 shows relationships with total WOB and C_L,dyn with V_T/IC and IRV (%FVC), with all participants included at V̇e of 75 l/min. V_T/IC and IRV (%FVC) had positive and negative relationships with total WOB (r = 0.57 and r = −0.60, P ≤ 0.01). Furthermore, there were significant relationships between C_L,dyn with V_T/IC and IRV (%FVC) (r = −0.66 and r = 0.75, P < 0.01).

Fig. 3.

Total work of breathing (WOB) in older and younger adults during exercise mean total WOB for older (○) and younger (●) adults at rest and ventilations (V̇e) of 25, 50, and 75 l/min. Older adults had a greater total WOB at V̇e of 50 and 75 l/min (P < 0.04). *Significantly different from younger adults.

Fig. 4.

Elastic and resistive components of work of breathing (WOB) in older and younger adults Mean inspiratory elastic (A), inspiratory resistive (B), and expiratory resistive (C) WOB for older (○) and younger adults (●) at rest and ventilations (V̇e) of 25, 50, and 75 l/min. At V̇e of 50 l/min, inspiratory resistive WOB was greater in the older than younger adults (P = 0.03). At V̇e of 75 l/min, older adults had greater inspiratory elastic and resistive as well as expiratory resistive WOB compared with younger adults (P < 0.02). *Significantly different from younger adults.

Fig. 5.

Relationships between total WOB and dynamic lung compliance (C_L,dyn) with V_T/inspiratory capacity (IC) and IRV [forced vital capacity (%FVC)] There were significant relationships between total WOB and V_T/IC (r = 0.57, P = 0.01; A) and inspiratory reserve volumes (IRV) (%FVC) (r = −0.60, P < 0.01; B) in the older (○) and younger (●) individuals. Furthermore, C_L,dyn was significantly related to V_T/IC (r = −0.66, P < 0.01; C) and IRV (%FVC) (r = 0.75, P < 0.01; D). Total WOB, C_L,dyn, V_T/IC, and IRV (%FVC) values were obtained at ventilations (V̇e) of 75 l/min.

DISCUSSION

Major findings.

This study was designed to determine the total WOB and its components at matched V̇e between older and younger adults. The major findings were twofold. First, older adults exhibited a greater total WOB during exercise than younger adults at V̇e of 50 and 75 l/min. Second, older compared with younger adults exhibited greater inspiratory elastic as well as inspiratory and expiratory resistive WOB at V̇e of 75 l/min. These findings suggest that the aging-induced alterations to the pulmonary system result in an increased respiratory muscle oxygen cost and blood flow demand in older compared with younger adults at exercise intensities requiring moderate-to-high levels of V̇e.

EFL and operating lung volumes.

The influence of aging on EFL and operating lung volumes has been studied extensively (7, 12, 20–22, 27, 35, 45, 48). Consistent with the present data, previous studies have found that older adults exhibit greater EFL than younger adults (7, 12, 27, 35, 45). The EFL severity reported herein is in line with most studies that have reported EFL at a V̇e of ∼75 l/min (i.e., 10–25% V_T) (7, 21, 27). To date, the effect of aging on operating lung volumes during exercise has been inconclusive (7, 12, 27, 35, 45, 48). In the present study, we found that older adults had a lower relative ERV at V̇e at rest and at 25 l/min. Furthermore, relative ERV was reduced with exercise in the younger but not older adults. At V̇e of 75 l/min, relative IRV was reduced in the older compared with younger adults, which was associated with decreased C_L,dyn and augmented WOB. Although multiple factors influence operating lung volumes during exercise, two mediators are age and EFL. For example, progressive aging (i.e., ∼39 vs. 70 vs. 88 yr) results in corresponding increases in EELV during exercise (7). Furthermore, it has been suggested that impending EFL (i.e., when tidal expiratory flows encroach the expiratory portion of the MFVL) and/or distinct EFL may result in increases in ERV (1). In the present study, we found that relative ERV was not increased in the older adults at V̇e of 75 l/min when EFL was significantly greater compared with younger adults. This finding is likely attributed to the older adults nearing their limit in reducing IRV and increasing V_T relative to FVC. For example, previous studies have shown that older adults cease to further decrease IRV once they reach ∼15–20% of FVC during exercise. Furthermore, Johnson et al. (21) found that older endurance-trained men do not increase V_T once V_T comprises ∼60% of FVC. In the present study, the older adults had an IRV (%FVC) of 21% and V_T/FVC of 57% at V̇e of 75 l/min, suggesting that if the older adults increased ERV, then this would have compromised V_T.

Aging and WOB.

The aging-induced alterations in the structure and function of the pulmonary system have been shown to consequently increase total WOB during exercise (4, 20, 33). Consistent with these studies, we found the total WOB was elevated in the older compared with younger adults at a V̇e of 50 and 75 l/min. At V̇e of 75 l/min, the total WOB in the present study (i.e., 90 J/min) is in line with the total WOB previously reported in older men (i.e., ∼115–125 J/min) as well as endurance trained older men at a similar V̇e (i.e., ∼125 J/min) (6, 22, 33). The total WOB of the younger group at V̇_E of 75 l/min (i.e., 49 J/min) is consistent with some (∼65–75 J/min) (16, 33), but lower than others (113–160 J/min) (10, 11, 15, 30) reporting WOB at a similar V̇e in younger men. Possible explanations for the lower WOB reported in the present study are that chest wall compliance was not measured and that there are methodological differences in calculating WOB. It should be noted that the older adults were overweight (as indicated by their BMI), and obesity has been suggested to influence the pulmonary system (e.g., lung compliance, absolute lung volumes) (39). Importantly, however, mild to moderate obesity (BMI of 34–35 kg/m²) does not result in increased WOB during exercise (2, 8), indicating that overweight/obesity did not contribute to the increased WOB in the older adults.

To further determine the mechanistic underpinnings for the increased total WOB in the older adults, the WOB was partitioned into the inspiratory and expiratory resistive and inspiratory elastic WOB. We found that the inspiratory elastic as well as inspiratory and expiratory resistive WOB were increased in the older compared with younger adults. The component with the largest contribution to the total WOB was inspiratory elastic WOB in the older adults, likely resulting from their ventilatory strategy. Specifically, the older adults had a smaller inspiratory reserve and greater V_T/IC than younger adults and associated decreased C_L,dyn and increased WOB at V̇e of 75 l/min. In the present study, we did not observe differences in V_T or f_B at matched V̇e between groups, which was likely a result from the modest degree of EFL developed in the older adults, as EFL has been shown to limit V_T (and V̇e) during exercise (29). Although most of the older adults had lower IRV (%FVC) and C_L,dyn than their younger counterparts at V̇e of 75 l/min, the resulting increase in inspiratory elastic WOB was likely less than would have been accrued by adopting a higher f_B and thus inspiratory resistive WOB for a given V̇e.

In the present study, we found that older adults exhibited a greater inspiratory and expiratory resistive WOB compared with younger adults. It is likely that anatomic differences (i.e., smaller airway caliber) significantly contributed to the greater resistive WOB. Specifically, older adults exhibit a reduced mean bronchial diameter, thus increasing airway resistance (34). Although this does not replace direct measurement of airway size, we found that the older adults had more than two times greater inspiratory resistive WOB compared with younger adults, whereas the mean inspiratory flows (i.e., V_T/Ti) were not different between groups. Importantly, the greater inspiratory pressure generation by the older adults did not result in greater mean inspiratory flows at matched V̇e, which was likely due to the greater airway resistance. The smaller airways of the older adults likely also contributed to the expiratory resistive WOB, as smaller airways are associated with the development of EFL during exercise (16, 46), and this dynamic compression further increases airway resistance. In fact, the older adults who exhibited EFL at a V̇e of 75 l/min had a greater expiratory resistance WOB than those without EFL (35 ± 14 vs. 13 ± 17 J/min, P = 0.04). It would be pertinent to investigate interventions to alleviate the elevated elastic and resistive WOB in older adults.

The present findings have important implications regarding cardiac output distribution during exercise. Specifically, the greater WOB at a V̇e of 75 l/min in the older adults presented herein occurred at 85–100% of V̇o_2peak and, importantly, would necessitate a greater respiratory muscle blood flow response. During exercise, when cardiac output is limited, a metaboreflex arising from the respiratory muscles is activated [increasing muscle sympathetic nerve activity and limb vascular resistance (42, 43, 47)], consequently redistributing cardiac output from the locomotor to the respiratory muscles (19, 36, 44). The respiratory muscle metaboreflex activation is similar between older and younger men (40), which in combination with the present findings suggests that the respiratory muscle metaboreflex will be activated earlier during severe-intensity exercise in older compared with younger men, which may contribute to reduced exercise performance; however, future studies are necessary to confirm this hypothesis.

Methodological considerations.

In the present study, chest wall compliance was not measured, and the WOB reported herein is specific to the work of the lung. However, based on the characteristic increase in chest wall elastic recoil (and, therefore, decreased compliance) with aging (32), we would expect that WOB is even greater in the older compared with younger adults than reported in the present study. Furthermore, our estimates of the WOB performed by the respiratory muscles were likely underestimated, as they do not consider chest wall deformation, chest wall tissue hysteresivity, eccentric work performed by the respiratory muscles, abdominal work, or thoracic gas compression (13, 38). Recently, chest wall energy storage during the respiratory cycle has been shown to be modified with age, with less elastic energy used during inspiration but more used during expiration at a standardized V_T (4). Future studies are warranted to determine how aging influences chest wall mechanics across a range of V̇e in older and younger adults. Third, partial expiratory flow maneuvers were not performed to account for thoracic gas compression, which would underestimate the maximal flow-volume loop, resulting in the overestimation of EFL (14, 28). However, studies using an independent measurement of maximal Ptp during expiration have found close agreement in the degree of EFL between the tidal expiratory pressure versus maximal Ptp method and tidal volume versus maximal flow volume loop method (21, 22). Finally, measurements of total lung capacity and residual volume would have allowed us to confirm that the older adults in the present study had higher absolute operating lung volumes during exercise than the younger adults.

Conclusions.

During exercise, older adults have greater total WOB for a given V̇e, owing to greater inspiratory elastic as well as inspiratory and expiratory resistive WOB compared with younger adults. These findings suggest that respiratory muscle oxygen uptake is greater with aging during exercise. Future studies are warranted to determine the respiratory muscle blood flow response in older and younger adults during exercise.

GRANTS

This work was supported by the National Institutes of Health [HL126638 to TPO] and American Heart Association [18POST3990251 to JRS].

DISCLOSURES

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

AUTHOR CONTRIBUTIONS

J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. conceived and designed research; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. performed experiments; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. analyzed data; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. interpreted results of experiments; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. prepared figures; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. drafted manuscript; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. edited and revised manuscript; J.R.S., T.J.C., E.H.V.I., B.D.J., and T.P.O. approved final version of manuscript.