Mechanical constraints on exercise hyperpnea in endurance athletes.

Mechanical constraints in endurance athletes

on exercise hyperpnea

BRUCE D. JOHNSON, KURT W. SAUPE, AND JEROME A. DEMPSEY John Rankin Laboratory of Pulmonary Medicine, Department of Preventive Medicine, Univckity of Wisconsin School of Medicine, Madison, Wisconsin 53705 JOHNSON, BRUCE D., KURT W. SAUPE, AND JEROME A. DEMPSEY. Mechanical constraints on exercise hyperpnea in endurance athletes. J. Appl. Physiol. 73(3): 874-886, 1992.-We determined how close highly trained athletes [n = 8; maximal oxygen consumption (vo2 ,,) = 73 k 1 ml kg-’ min-‘1 came to their mechanical limits for generating expiratory airflow and inspiratory pleural pressure during maximal short-term exercise. Mechanical limits to expiratory flow were assessed at rest by measuring, over a range of lung volumes, the pleural pressures beyond which no further increases in flow rate are observed (Pmax,). The capacity to generate inspiratory pressure (Pcapi) was also measured at rest over a range of lung volumes and flow rates. During progressive exercise, tidal pleural pressure-volume loops were measured and plotted relative to Pmax, and Pcapi at the measured end-expiratory lung volume. During maximal exercise, expiratory flow limitation was reached over 27-76% of tidal volume, peak tidal inspiratory pressure reached an average of 89% of Pcapi, and end-inspiratory lung volume averaged 86% of total lung capacity. Mechanical limits to ventilation ( VE) were generally reached coincident rewith the achievement of VO2 max;the greater the ventilatory sponse, the greater was the degree of mechanical limitation. Mean arterial blood gases measured during maximal exercise showed a moderate hyperventilation (arterial PCO, = 35.8 Torr, alveolar PO, = 110 Torr), a widened alveolar-to-arterial gas pressure difference (32 Torr), and variable degrees of hypoxemia (arterial PO, = 78 Torr, range 65-83 Torr). Increasing the stimulus to breathe during maximal exercise by inducing either hypercapnia (end-tidal Pco2 = 65 Torr) or hypoxemia (saturation = 75%) failed to increase VE, inspiratory pressure, or expiratory pressure. We conclude that during maximal exercise, highly trained individuals often reach the mechanical limits of the lung and respiratory muscle for producing alveolar ventilation. This level of ventilation is achieved at a considerable metabolic cost but with a mechanically optimal pattern of breathing and respiratory muscle recruitment and without sacrifice of a significant alveolar hyperventilation.

to accommodate further increases in VE, a small portion of the maximal exercise tidal FV and PV envelope on expiration does approach flow limitation near end-expiratory lung volume (EELV). This occurs as EELV is reduced below resting levels. Thus any further increase in iTE would necessitate an increase in flow rate at the initiation of expiration or an increase in EELV so that significant expiratory flow limitation would be avoided. The higher maximal oxygen uptake (vo2 max) and carbon dioxide production (VCO& of the endurance-trained athlete require a VE during maximal exercise that often approaches twice that of sedentary individuals. This increased demand on the pulmonary system exists even though the ventilatory capacity of the lungs and chest wall (i.e., for flow, volume, and pressure generation) are not different between trained and untrained subjects (28). Evidence suggests that some highly trained subjects lack an adequate hyperventilatory response to maximum exercise, contributing to an arterial hypoxemia already present because of a widened alveolar-to-arterial oxygen difference (8). The mechanical limitation to VE may be a primary reason for the constraint of this hyperventilatory response to maximal exercise. Our purpose was to determine the proximity with which tidal breaths during maximum exercise approach the mechanical limits for expiratory and inspiratory pressure and flow development in the highly trained athlete. In addition, we determined whether a relationship existed between the degree of mechanical limitation and the hyperventilatory response during maximal exercise. Finally, we attempted to stimulate VE and/or pressure developed by the inspiratory and expiratory muscles beyond that observed during maximal exercise by imposing hypercapnia and hypoxia during maximal exercise.

ventilatory pnea

METHODS

l

limits;

optimal

breathing

pattern;

l

control

of hyper-

Subjects

INHEALTHYUNTRAINED ADULTS, aconsiderablereserve for generating pulmonary ventilation (VE) has been shown to exist during maximal exercise (11, 13, 19, 26, 29).In these studies, flow-volume (FV) and pressure-volume (PV) responses during tidal breathing at maximal exercise are well below the mechanical constraints imposed by characteristics of the airways on expiration and the capacity for pressure generation by the inspiratory muscles. Despite the capacity of the lung and chest wall 874

0161-7567/92

$2.00

Copyright

Subjects (n = 8) were competitive male endurance runners with normal lung function (Tables 1 and 2). They performed moderate- to high-intensity training on a daily basis, running an average of 60-120 miles/wk. All subjects had been or were currently highly competitive in college or postcollege events ranging from 1,500 m to the marathon. All procedures were approved by the Institutional Review Board of the University of Wisconsin-Madison. Informed consent was obtained in writing from each subject.

0 1992 the American

Physiological

Society

Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (137.092.098.118) on August 4, 2018. Copyright © 1992 American Physiological Society. All rights reserved.

Subject

Age, yr

30 23 25 26 28 26 23 26 2521

& SE

VO

LIMITS

Ht, cm

Wt, kg

178 175 190 178 183 180 185 173 180&2

68.1 65 74 70.4 74.1 56.8 65 67.2 68t2

TO

2 -,

maximal

Pulmonary

O2 consumption;

Function

HR,,,

maximal

heart

875

VENTILATION

Tests

Pressure, Flow, Volume, and Gas Measurements

The breathing circuit for exercise testing and for preand postexercise resting measurements consisted of a Hans Rudolph automatic three-way directional valve (model 8600) that was connected to a low-resistance Hans Rudolph breathing valve. The three-way directional valve was connected to a pneumatic control box (model 8530), which was used for switching the valve for determination of EELV as described below. Inspired and expired flow rates were measured separately by pneumotachographs (model 3800, Hans Rudolph). Mouth pressure (Pm) was measured at the mouth and transferred by polyethylene tubing (PE-200) to a Validyne transducer (model MP45-871, t300 cmH,O). Esophageal pressure (Pes) was measured with a lo-cm latex balloon positioned in the lower one-third of the esophagus connected by polyethylene tubing (PE-200) to a Validyne transducer (model MP45-871, k200 cmH,O). Pm was subtracted from Pes for determination of transpulmonary pressure (Ptp). All flow and pressure signals were determined to be in phase up to 12 Hz. Inspired and expired 2. Preexercise lung volumes and flow rates Mean

TLC, liters VC, liters FRC, liters RV, liters FEVleO, liters MEF-50%, l/s

_+ SE

7.59t0.10 5.70&0.11 3.8OkO.09 1.90t0.11

4.98t0.13 5.94t0.43

%Predicted

ml

%nax, l

kg-’

76 74 73 80 74 70 66 75 73+1

l

min-’

HRMX9

beats/min

182 188 191

180 181 197 178 190 186t2

Best Event (Running), time

2 h 19 min 29:02 28:34 28:40 13:38 l3:53 3:45 3:34

(marathon) km) km) (10 km) (5 km) (5 km) (1.5 km) (1.5 km)

(10 (10

rate.

Vital capacity (VC) and inspiratory capacity (IC) were determined using a Collins 13.5-liter water-sealed spirometer. Thoracic gas volume and functional residual capacity (FRC) were determined in a Collins body plethysmograph as well as with a helium-nitrogen dilution rebreathe technique (16). Residual volume (RV) was measured using an inert-gas single-breath dilution method.

TABLE

EXERCISE

1. Subject characteristics

TABLE

PD PS KH SJ NH TS MD TH Mean

MECHANICAL

+ SE

lOOk2 lOlk3 92t3* 84t6” 106t3 102t7

Normal predicted values for vital capacity (VC), forced expired volume in 1 s (FE&,), and maximal expiratory flow rate at 50% of VC (MEF-50%) are based on age and height from Knudson et al. (18). Normal predicted values for total lung capacity (TLC), functional residual capacity (FRC), and residual volume (RV) are based on age and height from Needham et al. (25). * Measured value is less than predicted (P < 0.05).

gases were sampled at the mouth via a Perkin-Elmer mass spectrometer (model 1100). All signals were sent through an analog-to-digital board and sampled on a computer (Zenith model ZBF-2339-BK) at 75 Hz. Volumes were dete rmined by a computer in tegration of the flow signals. Tests of Ventilator-y Capacity Expiration. Two methods of quantifying expiratory flow limitation were used, one involving maximal FV loops (MFVL) and the other involving maximal effective pleural pressures (Pmax,). The first technique required that subjects perform three maximal volitional FV maneuvers before and immediately after exercise. Exercise tidal FV loops were then placed within the maximal loops based on a measured EELV. The amount of expiratory flow limitation was defined as the percentage of the tidal volume (VT) that met the boundary of the expiratory portion of the MFVL. The second technique involved measuring the maximal effective expiratory pressures over a range of lung volumes (at rest) via constructing isovolume pressure-flow diagrams according to the methods of Olafsson and Hyatt (26). Expiratory pressure, flow, and volume values were obtained from a series of 8-10 expirations from total lung capacity (TLC) to RV at different muscular efforts. In most cases flow did not completely level off at a discrete pressure but instead over a range of pressures. To describe this leveling off of flow over a range of pressures, Pmax, (when presented for an individual) is shown as an area with a finite width at any lung volume. Maneuvers were performed in a body plethysmograph where flow was measured by pneumotachograph at the mouth, and volume was determined by a wedge spirometer via volume displacement. To improve the frequency response of the spirometer, box pressure was added to the spirometer signal through a variable resistance mixing circuit as described elsewhere (23). Pm, Pes, and Ptp were measured as described previously. All signals were determined to be in phase up to 10 Hz. From the plots obtained by these maneuvers, the pressure at which flow becomes limited (Pmax,) for different lung volumes could be determined, and tidal breathing transpulmonary PV loops obtained during exercise were plotted relative to these flow-limiting pressures to further evaluate flow limitation and whether expiratory pressure development during exercise was ever excessive.


876

MECHANICAL

LIMITS

TO

Inspiration. The capacity of the inspiratory muscles to generate Pes at different flow rates and at various lung volumes was determined using techniques similar to those described by Agostoni and Fenn (2) and Leblanc et al. (19). Subjects seated in a body plethysmograph made maximal inspiratory efforts against variable resistances ranging from no added resistance to occlusion and at six different lung volumes ranging from RV to TLC. At least two reproducible efforts were performed at each resistance and lung volume. Using this technique we constructed a regression equation for each subject that described the effects of inspiratory muscle length (i.e., lung volume) and velocity of shortening (i.e., flow rate) on the ability to generate pressure. On the basis of the lung volume and the flow at which peak inspiratory Pes occurred during tidal breathing in exercise, we determined how close the inspiratory muscles were to their capacity for pressure generation (Pcapi).’ Pcapi therefore represents the pressure “available” to the fresh resting inspiratory muscles for a given flow rate and lung volume. The width of the Pcapi area represents the 95% confidence interval around the regression equation predicting maximal pleural pressure from lung volume and flow rate. Measurement of EELV. EELV was measured using a double-indicator inert-gas dilution technique (N2 and He) and an automated computer-controlled pneumatic valve-rebreathe system that switched the subject to the rebreathe mixture precisely at end expiration (16). EELV was also measured by having subjects perform inspiratory capacity maneuvers near the end of each work load. To ensure that TLC was reached during the IC maneuvers, subjects were required to reach a peak negative Ptp similar to that determined via multiple trials at rest. Protocol

Subjects completed four exercise tests on a motordriven treadmill; each test was conducted on a separate day. Preliminary maximal test. A preliminary progressive maximal exercise test was conducted to familiarize subjects with testing procedures. Mechanics test. Each test began with the subject running at either 6 or 8 mph with no grade. Speed was increased 2 mph every 3 min until it reached 10 mph. Subsequently, on a discontinuous basis, speed was increased to between 12 and 15 mph with the grade at 2-6% until a volitional maximum was achieved. Two to 5 min of recovery time were allowed between each of these 3-min work rates. EELV and IC measurements were performed during the final 20 s of each work rate. Ten to 20 breaths immediately preceding the IC maneuvers were averaged using a computer-averaging program. This provided representative FV and PV loops to be plotted for each subject for each work rate. Using the same breaths, ventilatory volume variables and ventilatory timing variables ’ Peak Pes normally occurred at a high lung volume and high flow rate, making it the closest point to reaching the Pcapi along the PV curve. However, in some subjects, peak inspiratory pressure occurred at very low lung volumes, especially during heavier exercise, and did not represent the point closest to this capacity. Therefore, a point other than the peak inspiratory pressure (usually only a slightly lower value), but at a higher lung volume much closer to the capacity, was chosen.

EXERCISE

VENTILATION

were measured, and pulmonary resistance (R&dynamic compliance (Cdyn), and ventilatory work (W,) were computed as described by Mead and Whittenberger (24) and Otis (27). Measurement of arterial blood gases. During an additional testing session, subjects had a 22-gauge 5-cm-long vinyl catheter placed in the radial artery under local anesthesia just before testing. Three to six 2-ml samples were taken with the subjects on and off the mouthpiece in the sitting position at rest, and single samples were drawn at 30-s intervals throughout each exercise load. Each sample was drawn over 20-30 s. Arterial blood was analyzed for arterial PO,, Pco,, and pH using electrodes (Radiometer) previously calibrated with tonometered blood. All blood gases were corrected for temperature changes during exercise as measured with an esophageal thermocouple placed intranasally (Mon-a-Therm 6500). Whole blood lactate concentration was determined using a lactate analyzer (Yellow Springs). Potassium concentrations in serum were analyzed using an ion-specific electrode (Kodak Ecktachem 700). Catecholamine concentration was measured by liquid chromatography with electrochemical detection. An identical exercise protocol was followed as described in the mechanics test. CO, and hypoxia stimulation. A final test was performed in all subjects to determine whether VE and respiratory muscle pressure development could be stimulated beyond that achieved during maximal air breathing exercise. During submaximal exercise (10 mph 0% grade) subjects were allowed to reach a steady-state VE while breathing air (2-3 min) before they were given 2-3 min of hypercapnic [inspired CO, fraction (FI,,,) = 0.04 and/or 0.061 or hypoxic [inspired 0, fraction (FI,,) = 0.161gas mixture. During maximal exercise 0.04 F1cozwas administered for the entire 3 min of exercise. After an appropriate recovery, 0.16 FI,, was breathed during a 3-min work rate that averaged 98% of the group’s vozmar. When TE between the various inspired gases was compared, care was taken to ensure that values were obtained at similar time points (2.5-3 min) from the start of a given work rate. Statistics. Paired t tests were used to determine whether significant differences existed between predicted values for lung function and mean values measured in our subjects. A one-way analysis of variance with Bonferroni post hoc test was used to compare mean values across work rates. Correlation coefficients are Pearson product moment coefficients. Significance for all tests was set at P < 0.05. RESULTS

Resting Measurements Expiration

(Pmax,):

of Mechanical isovolume

Constraints pressure-flow

curves.

Pleural pressure and flow rate increased together with increasing expiratory effort until a plateau in flow rate occurred with increasing pressure at iso-lung volumes between 50 and 75% of TLC. Beyond 80% of TLC no plateau in flow rate was generally obtained with increases in pleural pressure. The pleural pressure at the point where flow leveled off (Pmax,) averaged 13.2t 1.3 (SE) cmH,O at 50% of TLC (range 8-20 cmH,O) and


MECHANICAL

Vo2, llmin TE, l/min 7jA, l/min VT, liters Frequency, breaths/min EELV, liters RL*, cmH,O . 1-l . s Cdyn, llcmH,O w,, Jlmin

LIMITS

TO EXERCISE

877

VENTILATION

Rest

42%

61%

83%

95%

100%

0.31~0.01 9.6t0.5 7.1t0.4 0.79t0.05 12.5t0.8 3.8OkO.09 1.9OkO.12 0.30t0.03 2.1t0.4

2.09t0.05 50.4k1.4 44.OkO.9 1.66kO.09 30.921.6 3.38t0.08* 2.04kO.15 0.26kO.02 52.0t7.5

3.07t0.08 73.0k1.2 66.9k1.9 2.14kO.10 34.621.5 3.32t0.08* 2.11k0.15 0.23kO.02 110.2k9.4

4.18kO.19 117.3t6.7 103.4t6.2 2.67k0.18 44.5t2.1 3.39*0.08* 2.15t0.12' 0.20t0.02* 214.3k21.7

4.81kO.19 151.5t7.1 133.9k6.4 2.88~10.16 53.4t2.8 3.51t0.08" 2.30*0.19* 0.19_+0.02* 385.2k38.9

4.96t0.14 168.725.4 146.0t5.7 2.93t0.15 58.4k2.6 3.62t0.09* 2.06kO.16 0.17~0.01* 510.4+38.3

Values are means 2 SE for 8 subjects. voz, oxygen consumption; iTE, minute ventilation; \jA, alveolar ventilation; VT, tidal volume; EELV, end-expiratory lung volume; RL~, inspiratory resistance; Cdyn, dynamic compliance; WV, total ventilatory work. RL~ was measured at peak inspiratory flow rate (0.5 l/s at rest to 7.6 l/s during maximal exercise). * Significantly different from resting value (P < 0.05).

34.6 t 3.7 cmH,O at 75% of TLC (range 23-53 cmH,O). The relationship between lung volume (LV) expressed as a percentage of TLC (LV, %TLC) and maximal effective pressure development for the group is described in the following regression equation (r = 0.80) Pmax,(cmH,O)

= -34.4

+ 0.93 x (LV, %TLC)

Inspiration (PcapJ. At rest the capacity of the inspiratory muscles to develop pleural pressure against an occlusion was maximal between the lung volumes of 42 t 3 and 59 t 4% of TLC and averaged 108 t 5 cmH,O. Above 59% of TLC maximal volitional pleural pressure development declined as lung volume increased. This decline was 0.65 t 0.03% for every 1% increase in lung volume. Maximal pleural pressure development also declined at all lung volumes as flow rate increased. This decline was 5.21 t 0.3% for every l-l/s increase in flow rate between 0 (occlusion) and 7 l/s. The combined effect of lung volume and flow rate on pleural pressure development is described in the following regression equation for the eight subjects tested

PM& (% of maximal

occlusion

Pe)

= 112.8 - 0.65 x (LV, %TLC)

- 5.21

X (flow rate, l/s)

(r = 0.84)

Ventilatory and lung volume response to progressive exercise. The VE response to exercise for the group is shown in Table 3 for five work rates. All subjects showed a decline in slope or a plateau in VO, vs. work rate over the last two work rates of the discontinuous progressive exercise tests. Respiratory exchange ratio increased progressively from 0.9 at 61% of Vo, maxto 1.15 during maximal exercise. With light and moderate exercise VT showed a progressive increase, as did breathing frequency, until -83% of VO, m8X (75-90%), after which breathing frequency accounted for the majority of the increase in iTE (-50 l/min). Mean inspiratory flow rate increased progressively throughout exercise, and fractional inspiratory duration increased slightly from rest (0.44) to the second highest work rate (0.52) and then remained unchanged. Exercise effects on EELV are shown in Table 3. EELV was significantly below resting values during exercise at the lowest three work rates. With further increases in work rate and VE above 117 l/min, EELV progressively increased to 0.180 liter below

the resting EELV during maximal exercise (range 0.71 liter below to 0.11 liter above the resting values). Because of the rising EELV and a fairly constant VT over the highest three work .rates, end-inspiratory lung volume (EILV) reached 86 t 1% of TLC during maximal exercise. The increase in VT during moderate exercise was achieved by encroaching to a significant extent on both the inspiratory (56%) and expiratory (44%) reserve volumes, whereas during maximal exercise, 97% of the increased VT was derived from the inspiratory reserve volume. Pulmonary mechanics. Changes in the work of VE, RL, and Cdyn are also shown in Table 3. WV increased exponentially throughout exercise mainly as a result of the increase in the expiratory work of breathing. Expiratory resistance (measured at peak flow rate) increased 27% from rest to maximal exercise (2.4 vs. 3.0 cmH,O 1-l s) (P < 0.05). Inspiratory resistance remained near resting values, from rest to maximal exercise, showing a significant but small 23% increase during heavy work, despite a fourfold increase in peak inspiratory flow. Cdyn fell progressively from rest (0.30 t 0.03) to maximal exercise (0.17 t 0.01; P < 0.05). Flow and pressure demand vs. capacity during exercise. EXPIRATION. The group mean FV and PV response to progressive exercise is shown in Fig. 1 relative to Pmax, and Pcap;. Mean volitional MFVL are shown from preand immediately postexercise measurements. There was a slight but significant (P < 0.05) increase in maximal expiratory flow rate at 50% of VC (ME-F& from pre- to postexercise (0.3 l/s). Up to 61% of Vozmar, pressure, flow, and volume requirements during tidal breathing were well within the capacity of the pulmonary system. At 83% of Vozmax, VE increased to 117 t 7 l/min, and a small portion of the expiratory tidal flow rate (24 t 7% of the VT) and expiratory pressure (8 t 3% of the VT) reached flow limitation as lung volume approached end expiration. With further increases in VE, expiratory flow rate became more limited as 61 t 9% of the VT met the limit imposed by the postexercise MFVL and 46 t 7% of the tidal expiratory pressure met or exceeded the Pmax, during maximal exercise. The group mean expiratory pleural pressures partially exceeded the Pmax, (as shown in Fig. 1) because four of the eight subjects exceeded their maximal effective pressure by 5-20 cmH,O over l5-50% of their VT. This indicates some degree of l

l


878

MECHANICAL

120,*-\ \

a

an

LIMITS

TO

EXERCISE

VENTILATION

Young Athlete ‘*,

Max

Exuciso

1

PA02

- 110 78 36 .15 146 23

II ’ II ‘\, \ Pmaxe

mmHg mmHg mmHg

I

L/min L/mln

v

7

1 VOLUME (L)

-9oJ

3

2

1

r--I-,. =-\ ‘\pcapi iOLUME (L)

FIG. 1. Ventilatory response to progressive exercise. Group mean (n = 8) tidal flow-volume and pressure-volume loops plotted (from 10-20 breaths at each work load on each subject) using measured end-expiratory lung volumes for rest and exercise, which averaged 42, 61, 83, 95, and 100% of maximal O2 consumption. Tidal flow-volume loops are shown plotted within flow constraints set by pre- (solid line) and postexercise (dashed line) maximum volitional flow-volume loops. Tidal pressure-volume loops are shown within constraints for effective pressure generation (Pmax,) on expiration and within capacity for pressure generation on inspiration (Pcapi). Both panels are plotted relative to group mean total lung capacity and residual volume. Relevant gas exchange and ventilatory data obtained during maximal exercise are also shown. Widths of Pmax, and Pcapi at a given lung volume indicate 95% confidence Pco,; VDNT, dead space-to-tidal volume ratio; VA, intervals. PAo,, alveolar PO,; Pao,, arterial PO,; Pace,, arterial alveolar ventilation; VD, dead space ventilation.

ineffective generation of expiratory pressure, i.e., without increased flow rate. In the remaining subjects this effective limit to productive expiratory pressure generation was met but not exceeded, despite maximal exercise pleural pressures being equal to Pmax, along 26-76% of their VT. Figure 2 shows two examples of subjects who reached significant degrees of expiratory flow limitation during both very heavy and maximal exercise. INSPIRATION. Peak inspiratory pleural pressure during tidal breathing reached a progressively greater percentage of Pcapi as work rate increased (Fig. 3). During light to moderate exercise ~65% of Pcapi was achieved, increasing to 80% during heavy exercise and 89% during maximal exercise. In three subjects peak inspiratory pressure (or a pressure close to the peak) actually equaled the capacity of the respiratory muscles for pressure generation. The major reasons the capacity for inspiratory muscle pressure development was approached by the group and reached in some subjects were 1) increasing peak inspiratory pressures (37 cmH,O during maximal exercise) and 2) a decreasing Pcapi. The Pcapi fell because of increasing flow rates (7 l/s during maximal exercise) and because peak inspiratory pressures occurred at increasing lung volumes (80% of TLC). The latter occurred because EELV rose over the last three work rates and VT remained constant or increased. Figure 2 contrasts a subject who reached 100% of Pcapi at maximal exercise (subject SJ) to a subject (subject TH) who still had substantial reserve for inspiratory pressure development even during maximal exercise. Of the three subjects who had reached the Pcapi during maximal exercise, two of these subjects had >50% of their VT reach Pmax,. Ventilutory response to exerciseplus hypercapnia or hyp-

oxia. Figure 4 shows the mean FV and PV responses to increased FI,,, during submaximal and maximal exercise relative to air breathing responses obtained at the same exercise intensities. Table 4 shows the corresponding ventilatory responses. Hypercapnia. All eight subjects demonstrated a brisk ventilatory response to both 0.04 and 0.06 FI,,, during submaximal exercise at 61% of VO, max. At 0.06 FICHE, end-tidal PCO, increased from 42 to 58 Torr and the mean increase in Ti7E was 47 t 3 l/min, or 2.95 1. mine1 .mmHg-’ (range 1.45 to 5.41). This response was achieved primarily by a 34% increase in VT. During maximal exercise all subjects were able to complete the 3-min maximal work rate while breathing 0.04 FI,,,. No increase in group mean VE occurred (compared with air-breathing maximal exercise), although VT increased an average of 8% and breathing frequency fell by the same amount. While 4% CO, was breathed, EELV was similar to air, EILV remained at 86% of TLC, and peak inspiratory pressure remained unchanged (37 cmH,O). However, peak inspiratory pressure occurred at a slightly higher lung volume so that the available Pcapi was reduced, and 96% of this Pcapi was achieved compared with the 89% on room air. Pressures developed throughout expiration remained unchanged during CO, breathing, remaining equal to or slightly in excess of Pmax, over 46% of the VT. Figure 5 shows the same subjects previously shown in Fig. 2 but now demonstrates the effect of hypercapnia on the ventilatory response during maximal exercise. Subject SJ, who had reached both significant expiratory flow limitation and his capacity for inspiratory pressure generation while breathing air, did not further increase VE with added CO,. However, subject TH, who still had sig-


MECHANICAL

Max Exercise:

LIMITS

TO

EXERCISE

879

VENTILATION

\iE = 192 Lhnin

Pa02 = 80 mmHg

32

I 13 24 cu t = 161

PaC02 = 31.8 mmHg P(A-a)02 = 31.5

81

_-

YCXJME IL)

S.J. Age = 25 yrs

Max vO2 = 80 ml/kg/mn

-Qn VW

Max Exercise:

VOLUME

(L)

3E = 162 L/min

;

7.23

16 I

3’ Q)-24 z 12J

VOLUME (L) T.H. Age = 27 yrs Max \jO2 = 75 ml/kghnin

I

-32

t -401 ..

-lo&

FIG. 2. Tidal flow-volume and pressure-volume loops for 2 subjects during progressive exercise. Subjects were chosen because of differences in their hyperventilatory response during maximal exercise and differences in available inspiratory pressure during maximal exercise. Tidal loops are shown relative to each subject’s maximum flow-volume loops and individually determined maximal effective pressures and inspiratory pressure capacities. Width of Pmax, at a given lung volume represents range of pressures over which flow became limited for that individual. Width of Pcapi at any given lung volume represents the 95% confidence interval for the regression equation predicting maximal pleural pressure from volume and flow. PA,~ - Paoz) alveolar-to-arterial oxygen difference; irE, minute ventilation; max VO,, maximal 0, consumption.

nificant inspiratory pressure reserve, demonstrated a further increase in i7E. Hypoxia. Six subjects completed submaximal and near maximal (98% of VO, ,,,) exercise while breathing 0.16 ?I~,. As shown in Table 4, during submaximal exercise, VE increased 26 l/min while saturation dropped 10%. This 36% increase in TE was achieved by increases in both VT and breathing frequency. EELV was 240 ml greater during hypoxia than during air-breathing exercise. During near maximal exercise, 0.16 FI,~ caused arterial 0, saturation to drop to 75%; however, VE did not increase beyond that observed on room air. Neither the degree of expiratory flow limitation, nor inspiratory pressure development was different from values obtained on room air. Arterial blood gases and gas exchange. Mean results for blood gases during progressive exercise are shown in Fig. 6. The alveolar-to-arterial oxygen difference changed lit-

tle up to 50% of VQgrnax and then widened progressively up to a mean of 32 Torr (range 20-46 Torr) during maximal exercise. This was due to a gradual rise in alveolar PO, and a reduction in arterial PO,. Arterial PCO, remained constant during moderate exercise (near resting values). Above 60% of VO, maxhyperventilation occurred and arterial PCO, fell progressively coincident with a progressive metabolic acidosis as exercise intensity increased. During maximal exercise arterial PO, was 77.5 t 2 Torr and arterial PCO, was reduced to 35.8 t 0.6 Torr. Arterial lactate concentrations were 6.4 t- 0.6 mM during maximal exercise (10 t 1.3 mM after 2 min of recovery) and arterial pH was 7.28 t 0.14. Plasma norepinephrine concentrations rose progressively, reaching 13 times the resting value during maximal exercise (to 5.8 t 0.8 ngl ml), and plasma K+ also rose progressively from 3.8 t 0.4 mM at rest to 6.4 t 0.4 mM during maximal exercise. The dead space-to-VT ratio dropped from 0.27 at rest to 0.08


880

MECHANICAL

LIMITS

TO

EXERCISE

VENTILATION

during maximal exercise (arterial spite an arterial PO, of 69 Torr. f

“1

\

Capacity

DISCUSSION

Available

,-*A--

-

0 20 3 %i

e-

_#--

_#--

//e"--

Peak

hsp.

PCO, = 37.9 Torr), de-

Pressure

Q,

The focus of this study was to determine the degree to which available reserves for expiratory flow and inspiratory pressure development are utilized to meet the ventilatory requirements of the highly trained endurance athlete. In addition, we determined whether the degree of mechanical limitation to VE during exercise altered the magnitude of the hyperventilatory response to exercise.

-

Q

20 302

0

40

60

(Percent

80 of

100

Max)

FIG. 3. Peak inspiratory pleural pressure (means; dal breathing (dotted line) and capacity of inspiratory sure generation (solid line) with progressive exercise.

n = 8) during timuscles for pres-

with moderate exercise and then rose to 0.15 during maximal exercise. For the group, at maximal exercise arterial PO, was inversely related to alveolar-to-arterial oxygen difference (r = -0.96, P < 0.01; Fig. 7) but showed no relationship with arterial Pco,. The amount of the tidal breath that was flow limited during maximal exercise correlated with the degree of hyperventilation when expressed as either VEhO, (r = 0.57) or arterial PCO, (r = 0.54). Similarly, how close peak inspiratory pressure came to the Pcapi was positively correlated with ~Ei%O, (r = 0.65, P < 0.05). An example of these relationships is shown in Fig. 8, which presents the same subjects shown in Figs. 3 and 5. Subject SJ was extremely flow limited at maximal exercise and did not increase his VE above air-breathing levels during hypercapnic exercise; however, he had a substantial alveolar hyperventilation during maximal (air breathing) exercise (arterial PCO, = 31.5 Torr). On the other hand, subject TH, who did have the reserve to increase iTE during hypercapnia, showed very little relative hyperventilation

12-

VOLUME

Pulmonary

Function

in Athletes:

Capacity

There is some evidence to support the concept that highly trained endurance athletes might either gain through training or bring to their sport increased lung volumes, superior capacities for the generation of maximum airflow, and a greater capacity of the respiratory muscles for pressure development (7, 12, 20). The athletes we studied had mean values for lung volume subdivisions and forced expired volume in 1 s that were within 16% of the normal predicted values on the basis of height, weight, and age. We also obtained values for resting pulmonary function similar to those in larger samples of highly fit subjects (8,28) and for subjects of average fitness studied in our laboratory (9). During expiration, MEF,, averaged 102% of predicted in our subjects. In addition, our athletes showed Pmax, values, over a wide range of lung volumes, very similar to those described by Olaffson and Hyatt (26) in normal non-endurance-trained individuals and in other sedentary subjects we have studied in our own laboratory. Our athletic subjects also showed maximal inspiratory occlusion pressures that were very similar to those in nonathletic subjects (-90 to -120 cmH,O at FRC). We also found effects of flow rate (velocity of shortening) and lung volume (inspiratory muscle length) on reducing

(L)

FIG. 4. Ventilatory response (group mean; n = 8) to increased inspired CO, fraction during submaximal (smaller 2 loops) and maximal (larger 2 loops) exercise. COz, dotted lines; air, solid lines. During maximal exercise, end-tidal PCO~ was 38 Torr while air was breathed and 61 Torr while CO, was breathed. Increases in pressure, volume, and flow were noted with increased inspired CO, fraction during submaximal exercise, but no response was observed during maximal exercise (also see Table 4).


MECHANICAL

LIMITS

Submaximal

Air WC PI

02 02

42kl 58k2 38t2

96tl 96kl 86&l

73tl 120t5 99t4

38tl 61+2 34-tl

93&l 91t2 75t2

167k5 168t5 166k7

02 02

exercise

( Vo2 = 3.33

35k2 38t3 4023 Maximal

Air WC PI

TO EXERCISE

exercise

t 0.09 llmin)

2.09to. 10 3.16t0.16 2.55kO. 18 ( vo2

56k3 52k3 57t4

= 4.87

881

VENTILATION

3.3220.08 3.36t0.07 3.56-t0.21

43+2 6425 52+5

6_+3 2126 26+7

3.63kO.09 3.66kO.08 3.68kO.08

89+5 96k3 90+6

61+9 56+8 60+9

_t 0.17 l/min) 3.OOkO. 16 3.24t0.15 2.90&O. 18

Values are means * SE for 8 subjects during hypercapnia and 6 subjects during hypoxia. PETITE, end-tidal Pco~; Sao2, arterial 0, saturation. Peak PI, peak inspiratory pressure achieved during exercise expressed as percentage of available capacity for pressure generation (Pcapi). Inspired CO, fraction (FI,,~) = 0.06 during submaximal exercise and 0.04 during maximal exercise. Inspired 0, fraction (FI,J = 0.16 during submaximal and maximal exercise.

inspiratory pressure generation similar to those previously reported in less fit subjects (2,19). We caution that these data are limited in number and the normal variability of maximal inspiratory pressures and maximum effective pressures are large. Nevertheless, they do indicate that athletic and nonathletic subjects are very similar with regard to their capacity for pleural pressure generation. Expiratory Demand

and Inspiratory

Pressure Development:

Nonendurance athletes who achieve a VE of 115-120 l/min during maximal exercise (1,26) approach an expiratory flow limitation near EELV. At this level of VE, the degree of flow limitation is minimal, pleural pressures are only slightly positive, and EELV remains decreased below resting values, thereby preserving the length of the inspiratory muscles (13, 16). Considerable reserve remains for increasing VE during maximal exercise in these untrained subjects. On the inspiratory side, Leblanc et al. (19) showed that untrained subjects during maximal exercise (VE = 115 l/min) reached -40 to 60% of their available Pcapi. During submaximal exercise (83% of . VO 2 ,,) our athletes reached a VE (117 l/min) similar to that expected of untrained individuals during maximal exercise. At this exercise intensity, the trained subjects also reduced their EELV below resting values, generated pressures near end expiration that were only slightly positive, approached their flow-limiting pressures only at low lung volumes, and utilized -5O-60% of their Pcapi. Strategies available to increase expiratory flow rate with further increases in ventilatory requirement would involve increasing VTand either generating greater pressure early in expiration or increasing EELV to move the entire VT away from the flow-limiting pressures reached at the lower lung volumes. In most subjects (6 of 8) the dominant strategy was to increase EELV back toward or even slightly above resting levels. The two remaining subjects “chose” to simply increase VT, keeping EELV constant and below resting levels. They increased flow rates by generating high pressures very early during expiration, i.e., at higher lung volumes. The increasing degree of expiratory flow limitation with increasing exercise intensity has a significant effect

on pressure generation by inspiratory muscles. During maximal exercise, EILV averaged 86% of TLC because of the combination of a rise in EELV and a large VT.Inspiration occurring over such high lung volumes tends to increase the elastic load on the inspiratory muscles, as noted by the fall in Cdyn over the highest two work rates. These mechanical factors likely have a role in the adoption of a tachypneic pattern during very heavy exercise, as it would be extremely difficult to further increase VT because of the flow limitation on expiration and the increasing elastic load on inspiration. This increased elastic load occurs at a time when the capacity for pressure generation by the inspiratory muscles is already reduced because of the increased inspiratory flow rates (i.e., velocity of shortening) and decreased muscle length. The large inspiratory pleural pressure swings and increased EELV at high lung volumes caused subjects to come within 10% of (i.e., 5 cmH,O), or in some cases actually reach, their available capacity for pressure generation by the inspiratory muscles at or near peak inspiratory pressure. If EELV had not risen, peak inspiratory pressure would have reached only 75% of this capacity. In three of our subjects during maximal exercise the available capacity for pressure generation was actually reached and in one subject the Pcapi was reached during very heavy submaximal exercise. With further increases in exercise intensity, VE did not increase in this subject. Inspiratory and expiratory muscle regulation. The amount of ventilatory work observed in these subjects raises the possibility that respiratory muscle fatigue may have been occurring during maximum exercise. This has been previously suggested on the basis of changes in the frequency spectrum of the diaphragmatic electromyogram in untrained and moderately fit subjects during exercise (5) and by reduced maximum volitional inspiratory occlusion pressures after exercise in untrained but not trained subjects (7). Our data show no evidence that inspiratory muscle fatigue occurred during maximal short-term exercise. To the contrary, peak inspiratory esophageal pressure during the final 30 s at VO,max rose to reach peak inspiratory capacity (Pcapi) in three of our subjects. Furthermore, with CO, inhalation during maximal exercise, peak inspiratory pressure was either maintained precisely at its maximum level in those who had already achieved their Pcapi or was brought up to, or


882

MECHANICAL

LIMITS

TO

EXERCISE

VENTILATION

Max Exercise:

121

VOLUME (L) 1 S.J. Age = 25 yrs Max Exercise CO2 Response -9o[ -

Max Exercise: = 162 L/min -

I . ,,

w $0

Ir-!

a

7’

I\

: ‘,Rnaxe

II i II, ,I I I II

~,

1

401

i .=- .Fapl &.. -.. --: VOLUME (L)

I 6

5

4:3

I

‘2

1

I

12’

T.ii.

VOLUME (L)

Age = 27 yrs Max Exercise CO2 Responserlod

FIG. 5. Ventilatory response to increased inspired CO, fraction in individual subjects during maximal exercise. CO,, dashed lines; air, solid lines. Flow-volume and pressure-volume loops are shown plotted according to measured end-expiratory lung volumes and relative to each subject’s maximum flow-volume loop, Pmax,, and Pcapi. Subject SJ showed no ventilatory response to increased inspired CO, fraction, whereas subject TH showed a moderate response.

close to, Pcapi in those subjects whose air-breathing peak pleural pressure at maximal exercise was 10-E% short of the Pcapi. Because the Pcapi was determined in the resting “fresh” muscle under preexercise condition, the fact that it could be reached and sustained during maximum exercise speaks against inspiratory muscle fatigue having occurred. Our interpretation assumes that the “capacity” of inspiratory muscles for pressure development as determined via voluntary maneuvers at rest represents the capacity of the muscles actually used during tidal breathing during maximal exercise. Expiratory muscle force generation appears to have been precisely regulated during maximum exercise. All subjects showed substantial flow limitation during maximum exercise; in some cases up to 75% of the VT met the flow-limiting segment of the expiratory portion of the FV loop. Nevertheless, in four of eight subjects, pleural pressure throughout expiration did not exceed even the lower boundary of the maximum effective pressure. In the remaining four subjects, the upper boundary for maximal

effective pressure was exceeded but usually only by 5-10 cmH,O and only in one subject in excess of 20 cmH,O. These expiratory pressures are less than one-third of the maximum expiratory pressures generated during maximum voluntary ventilation maneuvers (17). Even when an increase of 15 Torr end-tidal PCO, (via increased FI,,,) was superimposed on maximum exercise, expiratory pressure generation still did not increase further beyond their effective limit. It is highly unlikely that sufficient neural drive to expiratory muscles was unavailable under these conditions, as both exercise and hypercapnia are known to be strong activators of expiratory muscle activity (3, 10, 13), nor would we suspect that expiratory muscles were actually fatigued under these conditions and “unable” to respond to an increased neural drive for expiration. A more reasonable explanation may be that expiratory muscle activity and tension development are precisely controlled via proprioceptive feedback in much the same way that others have suggested for the inspiratory muscles (15). Exactly how this


MECHANICAL

LIMITS

TO

PH 7.40 7.35 1.30 r.25 r.20

go

30 %

6, Arterial 0, difference

FIG.

rial

blood during

902

(MAX)

lvkf

gases, acid-base stat ‘us, and alveolarprogressive exercise (means; n = 8).

to-arte-

proposed feedback modulation of expiratory muscle activity might be sensed and mediated has not been tested directly. We do know that certain internal intercostal muscles contain abundant spindle afferents appropriate for proprioception, and in the awake exercising dog, vagal feedback was shown to be an important regulator of both abdominal and thoracic expiratory muscle recruitment (3). Demand

vs. Capacity in the Highly

Trained Human

Our data do permit us to address a number of fundamenta .l questions concern .ed with the determinants of the ventilatory response to maximal exercise and its consequences in the highly trained. Was a true mechanical limit to TjE reached during maximum exercise? Our data would support a positive response to this question in that during air breathing at vo2 maxy PCapi was nearly reached during at least a portion of inspiration .9 and the majority of expiration was flow limited. Furthermore, superimposing substantial levels of chemical stimuli on top of maximal exercise did not i .ncrease the mean ventilatory response. Thus these data support the idea that all of the available capacity for flow, volume, and inspiratory pressure development was used during maximum exercise. On the other hand, not all of the maximum volitional FV loop was used,. and Pcapi was not achieved during the early part of inspiration. Why didn’t subjects “choose” to achieve this higher VE available via maximal volitional efforts? One answer may be that the response obtained during exercise was mechanic lally more efficient bet ause, as di scusse d above, adopting for venti latory control a voluntary pattern markedly increases the amount of expiratory pressure and mechanical work performed (14, 17). It follows that the excessive carbon dioxide production required to produce this “extra” \jE may not actually provide additional “useful” alveolar hyperventil .ation (i.e., increased alveolar ventilation-to-VCO, ratio). Did mechanical factors limit the m agnitude of the comPlensatory alveola r hyper &ventilation during maximal ex-

EXERCISE

883

VENTILATION

ercise in the endurance-trained athlete? The evidence speaks against mechanical limitation as the only determinant of alveolar hyperventilation, because in all but one case, the maximal reserves for expiratory flow and inspiratory pressure generation were not achieved before, but rather coincident with the achievement of VO, max.Thus there was a positive correlation of the degree of hyperventilation with the magnitude of expiratory flow limitation, indicating that the increased ventilatory requirement was causing the athlete to reach his mechanical limitation rather than maximal exercise VE being determined by mechanical limitation. The fact that there was no absolute carbon dioxide retention above resting values at maximal exercise and that arterial PCO, did not rise with increasing work rate in any subject is further evidence that mechanical limitation did not severely limit the ventilatory response at any work rate. On the other hand, although mechanical limits to \jE were not reached until maximum exercise, it is still likely that reaching significant expiratory flow limitation even in moderately heavy exercise reduces the gain of the ventilatory response to available stimuli. This was shown by three of our athletes who, although mechanical limitation of VE was not reached during air breathing at . vo 2 maxy showed a marked blunting of the carbon dioxide and hypoxic response during maximal exercise relative to that obtained during submaximal exercise. These examples support the more extensive data of Clark et al. (6) obtained at substantially lower levels of VE in less fit subjects. They demonstrated significant reductions in the gain of the VT and ventilatory response to exogenous CO, as exercise intensity increased beyond 80% Vozmax and VE exceeded --120 Urnin. Thus a mechanical “constraint,” although not absolute limitation, to VE probably does exist during heavy submaximal exercise. Again this did not prevent some degree of hyperventilation throughout heavy to maximal exercise in the athlete; however, it may explain why the magnitude of hyperventilation in most of our presently studied athletes and in many of those we studied previously (8) was relatively modest (arterial PCO, 35-39 Torr, alveolar PO, 105-110 Torr) compared with the more substantial hyperventilation usually experienced in the less well trained at lower maximal work rates (9). Interindividual differences in control system responsiveness to the neurochemical stim-

20 """""" 60 65 70 75 80 Pa02 (mmHg) FIG. 7. P&, - PaoB vs. Pa,, [r = -0.96; Paoz = 105.55 - 0.853

85

during maximal (PAo, - Pao,)].

90 exercise

(n

= 8)


884

MECHANICAL uAge=25-

LIMITS

TO

EXERCISE

VENTILATION

T~Ags’nym.

liidio2=8o~m

lUkdO2=75~m

1

PA02

I

7.40

7.40

PH

1It 7.20

354 301

0 (Rwt)

90 (Max)

%i/O2 FIG.

17.20

0me80

30

Max 8. Arterial

60

%irO2 blood

gas respon

uli presented during maximal exercise probably also account for some of the individual variation in the degree of hyperventilation achieved. For example, as shown by contrasting the extreme responses in Fig. 8, some athletes simply failed to respond to their progressive arterial hypoxemia and metabolic acidosis, even when they were clearly not mechanically limited, whereas others did respond briskly despite their highly significant mechanical limitations. On the other hand, as a group, our athletes’ mean response to exogenous carbon dioxide, during submaximal exercise, was about the same (AVE/A end-tidal Pco, = 3.0 + - 0.5) as that observed by Clark et al. (6) in untrained subjects at the same level of irE during exercise and mean , VE increased 25% with a relati vel .y modest decrement in arterial oxygen saturatio n (96 to 86%; see Table 4). Perhaps these specific responses to CO, and hypoxia might not represent those to the combined effects of the m any pote ntial venti .latory sti .muli av vailable during heavy exercise including humoral agen .ts (metabolic [H+], K+, and norepinephrine) and locomotorlinked- (neural) influences. We propose that under the extrem e conditions of heavy to maximum exercise in the highly trained, the control system’s inherent sensitivity to available stimuli, the degree of mechanical constraint, and, most importantly , the interaction between these two sets of factors will determine the m agnitude of the ventilatory response. Finally, what are the consequences to the athlete (in terms of oxygen transport and . the metabolic cost of ‘\jE), when mechanical limits to VE are achieved during maximal exercise? First, the effects on arterial oxygenation are not substantial. It is clea r among our currently studied subj ects and those highly fit subjects previously studied (8) that the reduction in arterial PO, during maximal exe rcise wa .s rel ated most closely to the magnitude of the alveolar-to-arterial oxygen difference (Fig. 7). Thus re-

se in individual

7.30

subjects

(see Fig.

90 (Max)

Max 2).

ductions in arterial PO, to the range of 55-75 Torr were observed only in those subjects with alveolar-to-arterial oxygen differences in excess of 35 Torr (Fig. 7) (8). In these cases, the moderate hyperventilatory response may contribute to the arterial hypoxemia only indirectly in the sense that alveolar PO, was prevented from increasing to a very high value to compensate for the excessively widened alveolar-to-arterial oxygen difference and prevent arterial PO, from falling. In addition, expiratory flow limitation may contribute to maldistribution of ventilation-to-perfusion ratios during maximal exercise by causing nonuniformity in inspired VE distribution secondary to dynamic compression of airways on expiration. Our subjects with the greatest expiratory flow limitation also tended to be those who were the most hypoxemic at maximal work rates. We believe the major consequence to the athlete of . achieving mechanical limits to VE is to be found in the very high levels of W, and excessive metabolic cost of maximum VE. In addition to the very high levels of W, measured during maximal exercise using the conventional PV method (Table 3), there are also several additional sources of W, that are not accounted for, including 1) increased velocity of muscle shortening and work done by the diaphragm on the abdomen, which occur at all levels of exercise hyperpnea; and 2) the additional force expended by respiratory muscles devoted to distortion of chest wall shape (22) or to stabilization of the rib cage (2l), which might be invoked when high flow rates are being generated at the level of mechanical limits for expiratory flow and inspiratory muscle pressure generation. Recently, the oxygen cost of exercise hyperpnea and of WV was estimated by Aaron et al. (1) using a technique in which resting subjects mimicked their PV loop achieved during maximal exercise so that excessive pressure development would be avoided and the pattern of


MECHANICAL

LIMITS

TO

EXERCISE

885

VENTILATION

7p

m cn 800

% B -I

0

600

1D 4 s c cn 0

400

r m

0 N 0

0

200

W >

0

0 0

20

40

100

Gidh0~ FIG, 9. Individual responses of ventilatory work vs. exercise ventilation. muscle VO, based on a regression equation from Aaron et al. (1) where cise (ml/min) = 0.081 + 0.001 (exercise WV - rest WV).

respiratory muscle activity actually used for the hyperpnea would be approximated. In this study of moderately fit subjects the highest oxygen costs of VE were achieved in those with the greatest levels of WV and especially in those who experienced some degree of expiratory flow limitation. Using these conservative estimates of the oxygen cost per unit ventilatory demand, we estimated that minimal values for the oxygen cost of breathing during maximal exercise in our athletes would average 13% of . VO 2max (range 11-16%; Fig. 9). What might be the potential consequences to the athlete and his exercise performance of this excessive work and oxygen consumed by the respiratory muscles? First, given that inspiratory muscles were operating at or very close to their capacity for pressure generation, eventually muscle fatigue would be expected to occur. As discussed above, our evidence would not suggest that inspiratory muscle fatigue had actually occurred during the few minutes of exercise at %70Pmar. Perhaps fatigue of the diaphragm or other inspiratory muscles might eventually occur during longer endurance exercise, if a high enough level of exercise with sufficient ventilatory demand could be sustained for much longer periods of time (1,4). Thus, at least for short term, intense exercise at or near the level of VO 2 m8x,we would propose that the major consequence of the high level of W, to the athlete is in the high oxygen cost of VE, which represents a potentially significant “steal” of blood flow from locomotor muscles. We acknowledge the expert technical assistance of David Pegelow and thank Cheryl Crary and Dana Van Hoesen for typing the manuscript. This work was supported by the National Heart, Lung, and Blood Institute (NHLBI). the US Armv Research and Development Com-

120

140

shown

is an estimate muscles

160

en -I n 3E

r z zu

180

(L~IIN) Also

VO, of respiratory

of respiratory during exer-

mand, and the Wisconsin Heart Association. B. D. Johnson was a research fellow of the Wisconsin Heart Association and the NHLBI. Address for reprint requests: J. A. Dempsey, Preventive Medicine, 504 N. Walnut St., Madison, WI 53705. Received

23 January

1991;

accepted

in final

form

5 March

1992.

REFERENCES 1. AARON, E. A., B. D. JOHNSON, D. PEGELOW, AND J. A. DEMPSEY. The oxygen cost of exercise hyperpnea: implications for performance. J. Appl. Physiol. 72: 1818-1825, 1992. 2. AGOSTONI, E., AND W. 0. FENN. Velocity of muscle shortening as a limiting factor in respiratory air flow. J. Appl. Physiol. 15: 349-353, 1960. 3. AINSWORTH, D. M., C. A. SMITH, B. D. JOHNSON, S. W. EICHER, K. S. HENDERSON, AND J. A. DEMPSEY. Vagal modulation of respiratory muscle activity in awake dogs during exercise and hypercapnia. J. Appl. Physiol. 72: 1362-1367, 1992. 4. BAI, T. R., B. J. RABINOVITCH, AND R. L. PARDY. Near-maximal voluntary hyperpnea and ventilatory muscle function. J. Appl. Physiol. 57: 1742-1748, 1984. 5. BYE, P. T., S. A. ESAU, K. R. WALLEY, P. T. MACKLEM, AND R. L. PARDY. Ventilatory muscles during exercise in air and oxygen in normal men. J. Appl. Physiol. 56: 464-471, 1984. 6. CLARK, J. M., R. E. SINCLAIR, AND J. B. LENOX. Chemical and nonchemical components of ventilation during hypercapnic exercise in man. J. Appl. Physiol. 48: 1065-1076, 1980. 7. COAST, J. R., P. S. CLIFFORD, T. W. HENRICH, J. STRAY-GUNDERSON, AND R. L. JOHNSON, JR. Maximal inspiratory pressure following maximal exercise in trained and untrained subjects. 1Med. Sci. Sports Exercise 22: 811-815, 1990. 8. DEMPSEY, J. A., P. G. HANSON, AND K. S. HENDERSON. Exerciseinduced arterial hypoxemia in healthy human subjects at sea level. J. Physiol. Lond. 355: 161-175, 1984. 9. DEMPSEY, J. A., W. G. REDDAN, J. RANKIN, AND B. BALKE. Alveolar-arterial gas exchange during muscular work in obesity. J. Appl. Physiol. 21: 1807-1814, 1966. 10. GRIMBY, G., M. GOLDMAN, AND J. MEAD. Respiratory muscle action inferred from ribcage and abdominal V-P partitioning. J. Appl. Phvsiol. 41: 739-751. 1976.


886

MECHANICAL

LIMITS

TO EXERCISE

11. GRIMBY, G., G. SALTIN, AND L. WILHEMSEN. Pulmonary flow-volume and pressure-volume relationship during submaximal and maximal exercise in young well-trained men. Bull. Physio-Pathol. Respir. 7: 157-168, 12. HAGBERG, J. M.,

1971.

J. E. YERG II, AND D. R. SEALS. Pulmonary function in young and older athletes and untrained men. J. Appl. Phys-

iol. 65: 101-105, 13. HENKE, K. G.,

Regulation

1988.

M. SHARRATT, D. PEGELOW, AND J. A. DEMPSEY. of end-expiratory lung volume during exercise. J. Appl.

D. E., AND M. BRADLEY. Ventilatory muscle strength and endurance training. J. Appl. Physiol. 41: 508-516, 1976. 21. MACKLEM, P. T., D. GROSS, A. GRASSINO, AND C. Roussos. Partitioning of inspiratory pressure swings between diaphragm and intercostal/accessory muscles. J. Appl. Physiol. 44: 200-208, 1978. 22. MCCOOL, F. D., D. R. MCCANN, D. E. LEITH, AND F. G. HOPPIN, JR. Pressure-flow effects on endurance of inspiratory muscles. J.

20.

150-156,1989. 18. KNUDSON, BURROWS.

R. J., M. D. LEBOWITZ, C. J. HOLBERG, AND B. Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am. Rev. Respir. Dis. 127: 725-

734, 1983. 19. LEBLANC, CAMPBELL,

P., E. SUMMERS, M. D. INMAN, N. L. JONES, E. J. M. AND K. J. KILLIAN. Inspiratory muscles during exercise: a problem of supply and demand. J. Appl. Physiol. 65: 24822489,1988.

LEITH,

Appl. Physiol. 60: 299-303,1986 23. MEAD, J. Volume displacement

tory measurements

Physiol. 64: 13th146,1988. 14. HESSER, C. M., D. LINNARSSON,

AND L. FAGRAEUS. Pulmonary mechanics and work of breathing at maximal ventilation and raised air pressure. J. Appl. Physiol. 50: 747-753, 1981. 15. JAMMES, Y., B. BUCHLER, S. DELPIERRE, A. RASIDAKIS, C. GRIMAUD, AND C. ROUSSOS. Phrenic afferents and their role in inspiratory control. J. Appl. Physiol. 60: 854-860, 1986. 16. JOHNSON, B. D., K. C. SEOW, D. F. PEGELOW, AND J. A. DEMPSEY. Adaptation of the inert gas FRC technique for use in heavy exercise. J. Appl. Physiol. 68: 802-809, 1990. 17. KLAS, J. V., AND J. A. DEMPSEY. Voluntary versus reflex regulation of maximal exercise flow:volume loops. Am. Rev. Respir. Dis. 139:

VENTILATION

body plethysmograph for respirain human subjects. J. Appt. Physiol. 15: 736-

740,196O. 24.

MEAD, J., AND J. L. WHITTENBERGER. Physical properties of human lungs measured during spontaneous respiration. J. Appl. Phys-

iol. 12: 779-796, 1953. 25. NEEDHAM, C. D., M. C. ROGAN,

AND I. MCDONALD. Normal standards for lung volumes, intrapulmonary gas mixing, and maximal breathing capacity. Thorax 9: 313-325, 1954. 26. OLAFSSON, S., AND R. E. HYATT. Ventilatory mechanics and expiratory flow limitation during exercise in normal subjects. J. Clin. Invest.

48: 564-573,

1969.

OTIS, A. B. The work of breathing. In: Handbook of Physiology. Respiration. Washington, DC: Am. Physiol. Sot., 1964, sect. 3, vol. II, chapt. 17, p. 463-476. 28. REUSCHLEIN, P. L., W. G. REDDAN, J. F. BURPEE, J. B. L. GEE, AND J. RANKIN. The effect of physical training on the pulmonary diffusing capacity during submaximal work. J. Appl. Physiol. 24: 27.

152-158,1968. 29. YOUNES, M., AND

G. KIVINEN. Respiratory mechanics and breathing pattern during and following maximal exercise. J. Appl. Physiol. 57: 1773-1782,

1984.


Mechanical constraints on exercise hyperpnea in a fit aging population.

Validity of pulse oximetry during exercise in elite endurance athletes.

Left Ventricular Function After Prolonged Exercise in Equine Endurance Athletes.

Influence of polyphenol-rich diet on exercise-induced immunomodulation in male endurance athletes.

The effect of almond consumption on elements of endurance exercise performance in trained athletes.

Airway response to methacholine following eucapnic voluntary hyperpnea in athletes.

Mechanical load on the inspiratory muscles during exercise hyperpnea in patients with type 1 (insulin-dependent) diabetes mellitus.

Oxygen cost of exercise hyperpnea: measurement.

Blood gas disequilibria and exercise hyperpnea.

Differences in muscle mechanical properties between elite power and endurance athletes: a comparative study.

The effect of strength training on performance in endurance athletes.

Impact of reduced training on performance in endurance athletes.

Acute and Post-Exercise Physiological Responses to High-Intensity Interval Training in Endurance and Sprint Athletes.

Effects of submaximal and supramaximal interval training on determinants of endurance performance in endurance athletes.

Left ventricular response to submaximal exercise in endurance-trained athletes and sedentary adults.

Endurance running performance in athletes with asthma.

Reduced mortality in former elite endurance athletes.

Changes of magnesium concentrations in endurance athletes.

Echocardiographic assessment of the left ventricle of endurance athletes just before and after exercise.

Carbon dioxide flow and exercise hyperpnea. Cause and effect.

Oxygen cost of exercise hyperpnea: implications for performance.

Endurance exercise effects on cardiac hypertrophy in mice.

Role of Perceptual Factors on Endurance Profiles on Treadmill Exercise.

Effects of endurance exercise on mitochondrial function in mice.