982 Physiology & Biochemistry
Prior Maximal Exercise Decreases Pulmonary Diffusing Capacity during Subsequent Exercise
Affiliations
Key words
▶ fatigue ● ▶ diffusing capacity ● ▶ pulmonary ● ▶ altitude ● ▶ exercise ● ▶ cardiac output ●
J. C. Baldi1, M. J. Dacey2, M. J. Lee2, J. R. Coast2 1 2
Medicine, University of Otago, Dunedin, New Zealand Biological Sciences, Northern Arizona University, Flagstaff, United States
Abstract
▼
Pulmonary diffusion (DLCO) increases during exercise due to greater pulmonary capillary volume (Vc) and membrane diffusing capacity (DM). However, after heavy exercise there is a reduction in resting DLCO. It is unclear whether this post-exercise effect will attenuate the normal increase in DLCO, Vc and DM during subsequent exercise and whether this affects SpO2 (pulse oximeter). DLCO, Vc, DM, cardiac output and SpO2 were measured at rest, moderate (~70 % VO2peak) and heavy (~90 VO2peak) exercise in 9 subjects during 2 sessions separated by ~90 min. DLCO, Vc and DM increased during exercise (P < 0.05).
Introduction
▼ accepted after revision February 24, 2014 Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1372635 Published online: May 16, 2014 Int J Sports Med 2014; 35: 982–986 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0172-4622 Correspondence Michelle Jane Lee Biological Sciences Northern Arizona University PO Box 5640 Flagstaff United States 86011 Tel.: + 1/928/523 8109 Fax: + 1/928/523 7500 [email protected]
Resting diffusing capacity of the lung for carbon monoxide (DLCO) decreases following intense exercise [14, 19, 20, 30]. The mechanistic cause(s) for reduced DLCO are equivocal. In the framework of the Roughton and Forster [27] equation (1/ DLCO = 1/DMCO + 1/ΘVC) 2 hypotheses have been proposed to explain post-exercise DLCO reduction: 1) pulmonary edema caused by increased pulmonary capillary hydrostatic pressure reduces alveolar membrane diffusing capacity (DM) by increasing diffusion distance [11], or 2) redistribution of blood volume to the periphery after exercise reduces central blood volume and pulmonary capillary volume (Vc) [19]. Manier and colleagues measured DLCO, DMCO and VC after a marathon [18] and an incremental maximal exercise test [17] and found that DMCO decreased by 11.1 % and 8.9 % respectively, but VC was unchanged within the first hour of recovery. In contrast, Johns et al. [14] found that DLCO was reduced by 3 % and VC fell by 4.1 % after a maximal exercise test in healthy females. Surprisingly, they found that DMCO increased by 3 %. Others
Baldi JC et al. Prior Maximal Exercise Decreases … Int J Sports Med 2014; 35: 982–986
DLCO (P < 0.05) and Vc (P < 0.10), but not DM or SpO2 were lower in session 2 compared to the first. Reductions in DLCO and Vc appeared to be smallest during rest (1–4 %) and greatest at highintensity exercise (8–20 %), but the interaction was not significant. SpO2 decreased by 4.9 % and 5.1 % from rest to high-intensity exercise during the first and second exercise bout, but these changes were not different. These data confirm that a bout of high-intensity exercise reduces DLCO and Vc, and may indicate that these changes are exacerbated during subsequent high-intensity exercise. Despite these changes, SpO2 was not affected by previous exercise.
[19, 30] have also shown a post-exercise reduction in VC, but not DMCO, leaving open the possibility that both components of the DL equation are affected by strenuous exercise. Diffusion limitations are exacerbated during highintensity exercise. During maximal exercise, 5 to 8-fold increments in cardiac output [29] increase pulmonary capillary volume through recruitment of additional pulmonary capillaries or distension of already perfused capillaries [16]. Despite increases in VC, red blood cell transit time through the alveolar capillaries is reduced by up to 40 % [4, 15]. The resultant pulmonary capillary transit times maintain normal arterial oxygen saturation in healthy subjects. However patients with a diffusion limitation [22, 23] or elite athletes [4] may experience hypoxemia when cardiac output is increased by exercise. This may result from diminished pulmonary capacity in the case of diffusion limitation or ‘relative hypoventilation’ in the case of elite athletes [9]. Surprisingly little is known about how post-exercise reductions in DL affect arterial saturation and performance during subsequent exercise. Small reductions in SaO2 (e. g. 94 %) can be associated
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Authors
with reduced endurance performance [1, 28]. Thus any exerciseinduced reduction in DL could impact subsequent aerobic performance, particularly in those susceptible to diffusion limitation. The purpose of this study was to determine whether exhaustive short-term exercise affected lung diffusing capacity, cardiac output and oxygen saturation during a subsequent bout of exercise. To achieve this, we used simultaneous measurements of DLCO, DLNO and cardiac output at rest and during moderate (70 % VO2peak) and high-intensity (~90 % VO2peak) exercise and then repeated these measurements between 1 and 2 h after the first exercise bout. The challenge of exercise was further increased because exercise was performed at an altitude of ~2 100 meters, where PAO2 is approximately 80 mm Hg, and the alveolar-pulmonary capillary PO2 gradient is reduced relative to sea level values. Because recent studies using similar methods have shown a post-exercise reduction in VC, we hypothesized that post-exercise DLCO would be reduced at rest and that this reduction would increase during high-intensity exercise when the demand for pulmonary capillary recruitment was greatest. We also hypothesized that post-exercise SpO2 would be unchanged during rest and moderate intensity exercise, but would decrease during high-intensity exercise.
Methods
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Subjects 9 healthy volunteers (6 males and 3 females) between the ages of 18 and 25 years signed an informed consent form to participate in the study. All subjects were nonsmokers, free from asthma and other respiratory impairments, and deemed healthy and fit for physical activity according to the Physical Activity Readiness Questionnaire (PAR-Q and You, Canadian Society for Exercise Physiology). The study was approved by the Institutional Review Board (IRB) at Northern Arizona University and meets the ethical standards of the International Journal of Sports Medicine [10].
Study design The study required 2 visits from each participant. During the first visit, height and weight were measured. Pulmonary function was measured, consisting of forced vital capacity (FVC), forced expiratory volume in one second (FEV1.0), slow vital capacity (SVC), and maximal inspiratory pressure (MIP). The MIP was performed in a standing position. The subjects were asked to exhale to residual volume (RV) and inhale maximally against an occluded airway with a 1.0 mm hole to prevent glottic closure (S&M Instrument Company INC., Doylestown, PA). All other pulmonary function tests were conducted in a seated position using a MedGraphics metabolic cart (St. Paul, MN) and pneumotach. All spirometry data is reported as a percent of predicted using NHANES III predictions [8]. A VO2peak test was then performed on an electronically-braked cycle ergometer (Corival Lode B.V., Goningen, Netherlands) as described previously [2]. After a 5–10 min warm-up at low resistance, pedaling workloads were set at 50 W (females) or 100 W (males) and increased incrementally by 25 W every 2 min. The test was terminated when the subject reached volitional exhaustion. A true maximum was accepted when the subject achieved either; 1) a plateau in oxygen consumption following
an increase in workload, or 2) both of the following criteria; a respiratory exchange ratio greater than 1.1, and reaching > 95 % age-predicted maximal heart rate. Oxygen uptake (VO2), carbon dioxide production (VCO2), respiratory rate (RR), respiratory exchange ratio (RER), tidal volume (TV), and minute ventilation (VE) were continuously monitored at rest, during the warm-up stage and throughout the test. These data were collected and analyzed by a ParvoMedics TrueOne 2 400 metabolic cart (Sandy, Utah), and averaged every 10 s. The VO2peak was determined as the average of the 3 highest consecutive values during the final minute of the test. Heart rate (HR) was obtained using a heart rate monitor (Polar F1, Electro Oy, Finland) that was interfaced with the metabolic cart. During the second visit subjects performed resting and exercise rebreathing maneuvers during 2 exercise sessions (EX1 and EX2). These sessions were separated by a rest interval of between 1 and 2 h (93 ± 20 min) during which time subjects sat quietly in a 20 °C room and were encouraged to drink water ad libitum. This interval was selected because Sheel et al. [30] showed that nearly 90 % of the post-exercise reduction in DLCO occurred in this time frame (peak at 6 h) in moderately trained subjects. Rebreathing maneuvers were performed 2 times at rest, 65–75 % and 85–95 % of subjects’ VO2peak as modified from Wheatley et al. [31]. During each rebreathing maneuver, DLCO, DLNO, and cardiac output were measured using a 5 L anesthesia bag containing 0.278 % C18O, 0.598 % C2H2, 9 % He, 36.1 % O2 and 40 ppm NO balanced with nitrogen. Subjects were instructed to breath with a metronome during each rebreathing maneuver. The metronome was set for 32 breaths per min during the moderate exercise (65–75 % of VO2peak) stage and 40 breaths per min during the near-maximal exercise (85–95 % of VO2peak) stage. A pneumatic switching valve was connected between the subject and the rebreathing gas mixture, which allowed for rapid switching from ambient air to the test gas mixture. Gases were continuously sampled and analyzed using a mass spectrometer (Perkin-Elmer 1100, Wesley, MA) and NO analyzer (Sievers Instruments, Boulder, CO). These data were integrated with custom analysis software (KCBeck, Liberty, UT) for the assessment of DLCO and DLNO using the end-tidal concentrations of C18O and NO, respectively. VC and DM were calculated from the DLCO and DLNO values using the formulae of Ceridon et al. [3]. Cardiac output and end expiratory lung volumes were calculated using the end-tidal concentrations of C2H2 and He, respectively. The volume of gas used to fill the rebreathing bag was determined by each subject’s tidal volume immediately before each maneuver such that the tidal volume + 300 mL = total bag volume. Subjects were switched into the rebreathing bag at the end of a normal expiration (end expiratory lung volume; EELV) and took 8 breaths at the abovementioned respiratory rates. Following each maneuver the bag was emptied using a vacuum pump.
Statistics A 2-way repeated measures ANOVA was used to test the main effects of exercise (EX1 vs. EX2) and condition (rest vs. moderate exercise vs. intense exercise) and the interaction of main effects. Our hypotheses were that DLCO and its components DM and VC would decrease, therefore a one-tailed application was used for analysis of these data. Data are expressed as mean ± standard error of the mean unless otherwise specified. Statistical significance was reported at p values of 0.05 unless otherwise stated.
Baldi JC et al. Prior Maximal Exercise Decreases … Int J Sports Med 2014; 35: 982–986
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Physiology & Biochemistry
Results
tive session. DM was not affected by previous exercise, suggesting that post-exercise reductions in pulmonary diffusing capacity were solely dependent upon reduced pulmonary capillary volume during a second exercise bout. Stroke volume and cardiac output were lower during exercise in the second exercise session (EX2), which may have affected VC during periods of high cardiac demand. Arterial oxygen saturation was reduced with increasing exercise intensity, but this reduction was not affected by previous exercise. Our data show that, as a ‘main effect’ statistic, previous exercise reduced DLCO to a degree consistent with previous studies [5, 18, 22, 30]. However, closer examination of our data complicates this interpretation. Our mean resting DLCO values (28.7 vs. 28.3 mL/min/mmHg) were virtually identical before and after previous exercise, while exercise values were 5–10 % lower during the second exercise session. Similarly, mean resting VC was only 4 % lower after previous exercise, but exercising mean values were 23 % and 17 % lower during the second exercise bout. This may indicate that the reductions in post-exercise pulmonary diffusion were associated with reduced pulmonary capillary volume that was most evident during subsequent intense exercise when cardiac demand was highest. This interpretation contradicts earlier studies that showed reduced DLCO at rest, but did not measure diffusion during exercise. It is possible that differences in protocol explain these discrepancies. We chose a 1- to 2-h period (average of 93 min) between 2 brief, but intense exercise bouts because a similar study showed that a peak reduction in resting DLCO of 8.9 % came during the first hour after a single maximal exercise test [14]. Another study showed that intense cycling induced the greatest reduction in DLCO (10–12 %) 6 h after a very short exercise bout, but approximately 90 % of this reduction had occurred after 2 h in moderately trained and untrained subjects [30]. In comparison, we found that post-exercise DLCO (main effect) was reduced by approximately 5 % and that resting values were only 1.4 % lower. This difference, though significant, is considerably less than the aforementioned studies, raising the possibility that our second session was not ideally timed for a reduction in resting DLCO. Nonetheless, the 8.3 % reduction in mean DLCO during subsequent high-intensity exercise indicates that our protocol reduced DLCO during periods of high cardiac output. Our subject selection may also have contributed to differences between our resting DLCO results and those of previous authors. Bronchoalveolar lavage [13] and pulmonary scintogram [6] studies suggest increased permeability of the pulmonary bloodgas barrier caused by mechanical stresses after high, but not moderate [12] intensity exercise in elite athletes. In addition, the
▼
▶ Table 1 summarizes the physical charSubject characteristics: ● acteristics, aerobic capacity and pulmonary function of the subjects. Our study population was typical of a young, moderately fit cohort with slightly above average aerobic capacity and pulmonary function. ▶ Table 2 summarizes participant responses during EX1 and ● EX2. The relative exercise intensities ( %VO2peak), pedaling workload and heart rate were not different during EX1 and EX2 (P > 0.05). While cardiac output and stroke volume increased during exercise in both conditions as expected (P < 0.05), the increases were only greater in EX1 than EX2 at a P < 0.10 level. Arterial oxygen saturation decreased linearly with exercise intensity in both conditions, but was not different between EX1 and EX2. ▶ Fig. 1a–c describe the pulmonary diffusion measurements of ● the 2 (EX1 and EX2) conditions. DLCO, VC, and DM increased from rest to moderate exercise (P < 0.05). DL and DM further increased from moderate to intense exercise (P < 0.05). DLCO (P < 0.05) and Vc (at P < 0.10) were decreased in EX2, but not DM. SpO2 was not different between EX1 and EX2 (P = 0.29). The mean differences in DLCO and Vc appeared to be greater during exercise than rest. However, there was not a significant condition by intensity interaction (pre- vs. post-exercise) interaction for DLCO and Vc (P = 0.24 and 0.20 respectively). Similarly, there was no interaction of previous exercise on DM and SpO2 (P = 0.32 and 0.27 respectively).
Discussion
▼
The primary findings of this study were that DLCO and Vc were reduced during exercise performed 1–2 h after a prior exhausTable 1 Subject characteristics.
age (years) height (cm) weight (kg) BMI VO2peak (L/min) FVC ( % predicted) FEV1 ( % predicted) SVC ( % predicted) MIP (cm H20)
Average ± SEM
Range
21 ± 1 177 ± 3 73 ± 4 23.1 ± 1.0 3.34 ± 0.23 106 ± 4 103 ± 4 108 ± 4 148 ± 12
18–25 170–188 53–88 18.2–27.3 2.20–4.51 91–125 80–115 94–125 95–200
Table 2 Physiological responses at rest, moderate and high intensities during the first and second bouts of exercise. Rest EX1 cardiac output (L/min) stroke volume (mL) SaO2 ( %) workload (W) VO2 (L/min) %VO2max heart rate (bpm)
7.5 ± 0.7 86.4 ± 9.1 96.5 ± 0.4 – 0.60 ± 0.10 – 88 ± 3.6
Moderate intensity EX2 7.0 ± 0.5 75.5 ± 6.1 95.5 ± 0.6 – 0.53 ± 0.07 – 94 ± 2.0
EX1 †*
20.0 ± 2.0 126 ± 12.6†* 93.7 ± 0.8 † 157 ± 12 2.38 ± 0.19† 71.4 ± 1.4 159 ± 2.4 †
*
Data are average ± SEM
† (P < 0.05) different from rest (combined EX 1 and EX 2 moderate) # (P < 0.05) different from moderate intensity (combined EX1 and EX2) *
(P < 0.10) EX1 vs. EX2 within condition
Baldi JC et al. Prior Maximal Exercise Decreases … Int J Sports Med 2014; 35: 982–986
High intensity
EX2
EX1 †
19.2 ± 2.0 121 ± 12.0† 93.6 ± 1.0 † 157 ± 13 2.33 ± 0.19† 69.5 ± 1.9 161 ± 9.0†
EX2 †#*
23.3 ± 2.2 130 ± 13.6†#* 91.6 ± 0.9 †# 205 ± 18 # 2.94 ± 0.26†# 89.2 ± 1.8 # 182 ± 3.6 †#
21.7 ± 1.7†# 118 ± 10.0†# 90.4 ± 1.4†# 206 ± 17 # 2.93 ± 0.25†# 89.0 ± 2.1 # 184 ± 3.6†#
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984 Physiology & Biochemistry
a
55
DLCO (mL/min/mmHg)
50 45
*
40 35 †
‡
Moderate
High
30 25 20 Rest
Workload DLCO EX1 b
DLCO EX2
220 200
VC (mL)
180 160
**
140 120 †
100 80 Rest
Moderate
High
Workload VC EX1 VC EX2
DM (mL/min/mmHg)
c
80 70 60 50
‡ †
40 30 Rest
Moderate
High
Workload DM EX1
DM EX2
Fig. 1 a–c Diffusing capacity for carbon monoxide (DLCO), pulmonary capillary volume (VC) and alveolar capillary membrane diffusing capacity (DM) during rest, moderate intensity and high-intensity exercise. Solid circles represent values obtained during the first exercise session and open circles are from a second session. * P < 0.05) first vs. second testing session. ** (P < 0.10) first vs. second testing session. † (P < 0.05) different from rest. ‡ (P < 0.05) different from moderate exercise.
majority of early studies reporting a post-exercise reduction in DLCO were conducted in trained athletes [6, 17, 18, 20, 25–27], which may be a poor comparison for the present study. Our subjects were typical of healthy active, but untrained young adults. Consequently, it is possible that the exercise intensities performed by our subjects failed to produce sufficient mechanical stress to alter the blood gas barrier. However, this cannot explain why Sheel et al. [30] found that there was no difference in postexercise reduction in DLCO in trained vs. untrained athletes. Our finding that cardiac output and pulmonary capillary volume were reduced during EX2 (p < 0.10), despite nearly identical workloads with EX1, is consistent with a reduction in central intravascular volume that affected pulmonary capillary volume [7, 19]. Nagashima et al. [21] showed that plasma volume is reduced by 2.1 % 2 h after a single bout of upright exercise. Moreover, Hanel and colleagues found that the distribution of 99 m Tc erythrocytes shifted away from the thoracic cavity and towards the periphery 2½ h after intense rowing exercise. They also reported that the blood volume shift corresponded to a reduction in DLCO and atrial natriuretic peptide, which responds in proportion to venous return [7]. If the subjects in this study had a similar reduction and redistribution of intravascular volume, it would explain the observed decrease in stroke volume. It might also explain how resting pulmonary capillary volume, which is affected by cardiac output, was maintained by increased heart rate (88 vs. 94 bpm in EX1 vs. EX2), while high-intensity exercise values, which are dependent on cardiac reserve, were reduced during EX2. Contrary to our second hypothesis, our data do not provide evidence that a previous bout of high-intensity exercise reduces subsequent aerobic performance due to decreased PaO2, which is consistent with the findings of McKenzie et al. [19]. Despite reduced DLCO, there were no differences in workload or heart rate during the 2 high-intensity exercise sessions. In our study, average SpO2 values during the first and second high-intensity exercise sessions (91.6 vs. 90.4 %) were typical of exercise performed at this altitude (2 100 meters) and were not different between exercise bouts. While acknowledging that pulse oximeter measurements have limitations, we interpret our data as suggesting that changes in DLCO caused by previous exercise are unable to significantly reduce SpO2 during subsequent highintensity whole body exercise, at least in non-endurance athletes. In summary, this study expanded upon previous studies by showing that resting and exercising DLCO and Vc were reduced, and cardiac output was lower following a previous bout of intense exercise in healthy untrained subjects. Previous exercise did not affect DM in this study, suggesting that lower post-exercise DLCO was caused by reduced pulmonary capillary volume. Our data also suggest that reductions in DLCO are more severe during subsequent exercise. The reductions in DLCO were not associated with reduced SpO2.
Acknowledgements
▼
This project was funded by NIH Grant R15 HL097335-01A1.
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Physiology & Biochemistry
Conflict of interest: There is no conflict of interest among authors. References 1 Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA. Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J Physiol 2006; 575: 937–952 2 Baldi JC, Cassuto NA, Foxx-Lupo WT, Wheatley CM, Snyder EM. Glycemic status affects cardiopulmonary exercise response in athletes with type 1 diabetes. Med Sci Sport Exerc 2010; 42: 1454–1459 3 Ceridon ML, Beck KC, Olson TP, Bilezikian JA, Johnson BD. Calculating alveolar capillary conductance and pulmonary capillary blood volume: comparing the multiple- and single-inspired oxygen tension methods. J Appl Physiol 2010; 109: 643–653 4 Dempsey JA, Hanson PG, Henderson KS. Exercise-induced arterial hypoxaemia in healthy human subjects at sea level. J Physiol 1984; 355: 161–175 5 Hanel B, Clifford PS, Secher NH. Restricted post-exercise pulmonary diffusion does not impair maximal transport for O2. J Appl Physiol 1994; 77: 2408–2412 6 Hanel B, Law I, Mortensen J. Maximal rowing has an acute effect on the blood-gas barrier in elite athletes. J Appl Physiol 2003; 95: 1076–1082 7 Hanel B, Teunissen I, Rabol A, Warberg J, Secher NH. Restricted postexercise pulmonary diffusion capacity and central blood volume depletion. J Appl Physiol 1997; 83: 11–17 8 Hankinson JL, Odendrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. Population. Am J Respir Crit Care Med 1999; 159: 179–187 9 Harms CA, Babcock MA, McClaran SR, Pegelow DF, Nickele GA, Nelson WB, Dempsey JA. Respiratory muscle work compromises leg blood flow during maximal exercise. J Appl Physiol 1997; 1573–1583 10 Harriss DL, Atkinson G. Update – ethical standards in sport and exercise science research: 2014 update. Int J Sports Med 2013; 34: 1025–1028 11 Hodges ANH, Mayo JR, McKenzie DC. Pulmonary oedema following exercise in humans. Sports Med 2006; 36: 501–512 12 Hopkins SR, Schoene RB, Henderson WR, Spragg RG, West JB. Sustained submaximal exercise does not alter the integrity of the lung blood-gas barrier in elite athletes. J Appl Physiol 1998; 84: 1185–1189 13 Hopkins SR, Schone RB, Henderson WR, Spragg RG, Martin TR, West JB. Intense exercise impairs the integrity of pulmonary blood-gas barrier in elite athletes. Am J Respir Crit Care Med 1997; 151: 1090–1094 14 Johns DP, Berry D, Maskrey M, Wood-Baker R, Reid DW, Walters EH, Walls J. Decreased lung capillary blood volume post-exercise is compensated by increased membrane diffusing capacity. Eur J Appl Physiol 2004; 93: 96–101 15 Johnson RL Jr. Pulmonary diffusion as a limiting factor in exercise stress. Circ Res 1967; 20: I-154–I-160
16 Johnson RL Jr, Spicer WS, Bishop JM, Forster RE. Pulmonary capillary blood volume, flow and diffusing capacity during exercise. J Appl Physiol 1960; 15: 893–902 17 Manier G, Moinard J, Stoicheff H. Pulmonary diffusing capacity after maximal exercise. J Appl Physiol 1993; 75: 2580–2585 18 Manier G, Moinard J, Techoueyres P, Varene N, Guenard H. Pulmonary diffusion limitation after prolonged strenuous exercise. Respir Physiol 1991; 83: 143–154 19 McKenzie DC, Lama IL, Potts JE, Sheel AW, Coutts KD. The effect of repeated exercise on pulmonary diffusing capacity and EIH in trained athletes. Med Sci Sports Exerc 1999; 31: 99–104 20 Miles DS, Doerr CE, Schoenfelf SA, Sinks DE, Gotshall RW. Changes in pulmonary diffusing capacity and closing volume after running a marathon. Respir Physiol 1983; 52: 349–359 21 Nagashima K, Mack GW, Haskell A, Nishiyasu T, Nadel ER. Mechanism for the posture-specific plasma volume increase after a single intense exercise protocol. J Appl Physiol 1999; 86: 867–873 22 Niranjan V, McBrayer DG, Ramirez LC, Raskin P, Hsia CC. Glycemic control and cardiopulmonary function in patients with insulin-dependent diabetes mellitus. Am J Med 1997; 103: 504–513 23 Olson LJ, Snyder EM, Beck KC, Johnson BD. Reduced rate of alveolarcapillary recruitment and fall of pulmonary diffusing capacity during exercise in patients with heart failure. J Cardiac Fail 2006; 12: 299–306 24 Rasmussen BD, Hanel B, Jenson K, Serup B, Secher NH. Decrease in pulmonary diffusion capacity after maximal exercises. J Sports Sci 1986; 4: 185–188 25 Rasmussen BD, Elkjaer P, Juhl B. Impaired pulmonary and cardiac function after maximal exercise. J Sports Sci 1988; 6: 219–228 26 Rasmussen BD, Hanel B, Saunamaki K, Secher NH. Recovery of pulmonary diffusing capacity after maximal exercise. J Sports Sci 1992; 10: 525–531 27 Roughton FJW, Forster RE. Relative importance of diffusion and chemical reaction rates in determining rate of exchange of gases in the human lung, with special reference to true diffusing capacity of pulmonary membrane and volume of blood in the lung capillaries. J Appl Physiol 1957; 11: 290–302 28 Romer LM, Haverkamp HC, Lovering AT, Pegelow DF, Dempsey JA. Effect of exercise-induced arterial hypoxemia on quadriceps muscle fatigue in healthy humans. Am J Physiol 2006; 2290: R365–R375 29 Rowell LB. Human Circulation Regulation During Physical Stress. NY: Oxford University Press, 1986 30 Sheel AW, Coutts KD, Potts JE, McKenzie DC. The time course of pulmonary diffusing capacity for carbon monoxide following short duration high intensity exercise. Respir Physiol 1998; 111: 271–281 31 Wheatley CM, Baldi JC, Cassuto NA, Foxx-Lupo WT, Snyder EM. Glycemic control influences lung membrane diffusion and oxygen saturation in exercise-trained subjects with type 1 diabetes. Eur J Appl Physiol 2011; 111: 567–578
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Prior Maximal Exercise Decreases Pulmonary Diffusing Capacity during Subsequent Exercise
Affiliations
Key words
▶ fatigue ● ▶ diffusing capacity ● ▶ pulmonary ● ▶ altitude ● ▶ exercise ● ▶ cardiac output ●
J. C. Baldi1, M. J. Dacey2, M. J. Lee2, J. R. Coast2 1 2
Medicine, University of Otago, Dunedin, New Zealand Biological Sciences, Northern Arizona University, Flagstaff, United States
Abstract
▼
Pulmonary diffusion (DLCO) increases during exercise due to greater pulmonary capillary volume (Vc) and membrane diffusing capacity (DM). However, after heavy exercise there is a reduction in resting DLCO. It is unclear whether this post-exercise effect will attenuate the normal increase in DLCO, Vc and DM during subsequent exercise and whether this affects SpO2 (pulse oximeter). DLCO, Vc, DM, cardiac output and SpO2 were measured at rest, moderate (~70 % VO2peak) and heavy (~90 VO2peak) exercise in 9 subjects during 2 sessions separated by ~90 min. DLCO, Vc and DM increased during exercise (P < 0.05).
Introduction
▼ accepted after revision February 24, 2014 Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1372635 Published online: May 16, 2014 Int J Sports Med 2014; 35: 982–986 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0172-4622 Correspondence Michelle Jane Lee Biological Sciences Northern Arizona University PO Box 5640 Flagstaff United States 86011 Tel.: + 1/928/523 8109 Fax: + 1/928/523 7500 [email protected]
Resting diffusing capacity of the lung for carbon monoxide (DLCO) decreases following intense exercise [14, 19, 20, 30]. The mechanistic cause(s) for reduced DLCO are equivocal. In the framework of the Roughton and Forster [27] equation (1/ DLCO = 1/DMCO + 1/ΘVC) 2 hypotheses have been proposed to explain post-exercise DLCO reduction: 1) pulmonary edema caused by increased pulmonary capillary hydrostatic pressure reduces alveolar membrane diffusing capacity (DM) by increasing diffusion distance [11], or 2) redistribution of blood volume to the periphery after exercise reduces central blood volume and pulmonary capillary volume (Vc) [19]. Manier and colleagues measured DLCO, DMCO and VC after a marathon [18] and an incremental maximal exercise test [17] and found that DMCO decreased by 11.1 % and 8.9 % respectively, but VC was unchanged within the first hour of recovery. In contrast, Johns et al. [14] found that DLCO was reduced by 3 % and VC fell by 4.1 % after a maximal exercise test in healthy females. Surprisingly, they found that DMCO increased by 3 %. Others
Baldi JC et al. Prior Maximal Exercise Decreases … Int J Sports Med 2014; 35: 982–986
DLCO (P < 0.05) and Vc (P < 0.10), but not DM or SpO2 were lower in session 2 compared to the first. Reductions in DLCO and Vc appeared to be smallest during rest (1–4 %) and greatest at highintensity exercise (8–20 %), but the interaction was not significant. SpO2 decreased by 4.9 % and 5.1 % from rest to high-intensity exercise during the first and second exercise bout, but these changes were not different. These data confirm that a bout of high-intensity exercise reduces DLCO and Vc, and may indicate that these changes are exacerbated during subsequent high-intensity exercise. Despite these changes, SpO2 was not affected by previous exercise.
[19, 30] have also shown a post-exercise reduction in VC, but not DMCO, leaving open the possibility that both components of the DL equation are affected by strenuous exercise. Diffusion limitations are exacerbated during highintensity exercise. During maximal exercise, 5 to 8-fold increments in cardiac output [29] increase pulmonary capillary volume through recruitment of additional pulmonary capillaries or distension of already perfused capillaries [16]. Despite increases in VC, red blood cell transit time through the alveolar capillaries is reduced by up to 40 % [4, 15]. The resultant pulmonary capillary transit times maintain normal arterial oxygen saturation in healthy subjects. However patients with a diffusion limitation [22, 23] or elite athletes [4] may experience hypoxemia when cardiac output is increased by exercise. This may result from diminished pulmonary capacity in the case of diffusion limitation or ‘relative hypoventilation’ in the case of elite athletes [9]. Surprisingly little is known about how post-exercise reductions in DL affect arterial saturation and performance during subsequent exercise. Small reductions in SaO2 (e. g. 94 %) can be associated
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Authors
with reduced endurance performance [1, 28]. Thus any exerciseinduced reduction in DL could impact subsequent aerobic performance, particularly in those susceptible to diffusion limitation. The purpose of this study was to determine whether exhaustive short-term exercise affected lung diffusing capacity, cardiac output and oxygen saturation during a subsequent bout of exercise. To achieve this, we used simultaneous measurements of DLCO, DLNO and cardiac output at rest and during moderate (70 % VO2peak) and high-intensity (~90 % VO2peak) exercise and then repeated these measurements between 1 and 2 h after the first exercise bout. The challenge of exercise was further increased because exercise was performed at an altitude of ~2 100 meters, where PAO2 is approximately 80 mm Hg, and the alveolar-pulmonary capillary PO2 gradient is reduced relative to sea level values. Because recent studies using similar methods have shown a post-exercise reduction in VC, we hypothesized that post-exercise DLCO would be reduced at rest and that this reduction would increase during high-intensity exercise when the demand for pulmonary capillary recruitment was greatest. We also hypothesized that post-exercise SpO2 would be unchanged during rest and moderate intensity exercise, but would decrease during high-intensity exercise.
Methods
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Subjects 9 healthy volunteers (6 males and 3 females) between the ages of 18 and 25 years signed an informed consent form to participate in the study. All subjects were nonsmokers, free from asthma and other respiratory impairments, and deemed healthy and fit for physical activity according to the Physical Activity Readiness Questionnaire (PAR-Q and You, Canadian Society for Exercise Physiology). The study was approved by the Institutional Review Board (IRB) at Northern Arizona University and meets the ethical standards of the International Journal of Sports Medicine [10].
Study design The study required 2 visits from each participant. During the first visit, height and weight were measured. Pulmonary function was measured, consisting of forced vital capacity (FVC), forced expiratory volume in one second (FEV1.0), slow vital capacity (SVC), and maximal inspiratory pressure (MIP). The MIP was performed in a standing position. The subjects were asked to exhale to residual volume (RV) and inhale maximally against an occluded airway with a 1.0 mm hole to prevent glottic closure (S&M Instrument Company INC., Doylestown, PA). All other pulmonary function tests were conducted in a seated position using a MedGraphics metabolic cart (St. Paul, MN) and pneumotach. All spirometry data is reported as a percent of predicted using NHANES III predictions [8]. A VO2peak test was then performed on an electronically-braked cycle ergometer (Corival Lode B.V., Goningen, Netherlands) as described previously [2]. After a 5–10 min warm-up at low resistance, pedaling workloads were set at 50 W (females) or 100 W (males) and increased incrementally by 25 W every 2 min. The test was terminated when the subject reached volitional exhaustion. A true maximum was accepted when the subject achieved either; 1) a plateau in oxygen consumption following
an increase in workload, or 2) both of the following criteria; a respiratory exchange ratio greater than 1.1, and reaching > 95 % age-predicted maximal heart rate. Oxygen uptake (VO2), carbon dioxide production (VCO2), respiratory rate (RR), respiratory exchange ratio (RER), tidal volume (TV), and minute ventilation (VE) were continuously monitored at rest, during the warm-up stage and throughout the test. These data were collected and analyzed by a ParvoMedics TrueOne 2 400 metabolic cart (Sandy, Utah), and averaged every 10 s. The VO2peak was determined as the average of the 3 highest consecutive values during the final minute of the test. Heart rate (HR) was obtained using a heart rate monitor (Polar F1, Electro Oy, Finland) that was interfaced with the metabolic cart. During the second visit subjects performed resting and exercise rebreathing maneuvers during 2 exercise sessions (EX1 and EX2). These sessions were separated by a rest interval of between 1 and 2 h (93 ± 20 min) during which time subjects sat quietly in a 20 °C room and were encouraged to drink water ad libitum. This interval was selected because Sheel et al. [30] showed that nearly 90 % of the post-exercise reduction in DLCO occurred in this time frame (peak at 6 h) in moderately trained subjects. Rebreathing maneuvers were performed 2 times at rest, 65–75 % and 85–95 % of subjects’ VO2peak as modified from Wheatley et al. [31]. During each rebreathing maneuver, DLCO, DLNO, and cardiac output were measured using a 5 L anesthesia bag containing 0.278 % C18O, 0.598 % C2H2, 9 % He, 36.1 % O2 and 40 ppm NO balanced with nitrogen. Subjects were instructed to breath with a metronome during each rebreathing maneuver. The metronome was set for 32 breaths per min during the moderate exercise (65–75 % of VO2peak) stage and 40 breaths per min during the near-maximal exercise (85–95 % of VO2peak) stage. A pneumatic switching valve was connected between the subject and the rebreathing gas mixture, which allowed for rapid switching from ambient air to the test gas mixture. Gases were continuously sampled and analyzed using a mass spectrometer (Perkin-Elmer 1100, Wesley, MA) and NO analyzer (Sievers Instruments, Boulder, CO). These data were integrated with custom analysis software (KCBeck, Liberty, UT) for the assessment of DLCO and DLNO using the end-tidal concentrations of C18O and NO, respectively. VC and DM were calculated from the DLCO and DLNO values using the formulae of Ceridon et al. [3]. Cardiac output and end expiratory lung volumes were calculated using the end-tidal concentrations of C2H2 and He, respectively. The volume of gas used to fill the rebreathing bag was determined by each subject’s tidal volume immediately before each maneuver such that the tidal volume + 300 mL = total bag volume. Subjects were switched into the rebreathing bag at the end of a normal expiration (end expiratory lung volume; EELV) and took 8 breaths at the abovementioned respiratory rates. Following each maneuver the bag was emptied using a vacuum pump.
Statistics A 2-way repeated measures ANOVA was used to test the main effects of exercise (EX1 vs. EX2) and condition (rest vs. moderate exercise vs. intense exercise) and the interaction of main effects. Our hypotheses were that DLCO and its components DM and VC would decrease, therefore a one-tailed application was used for analysis of these data. Data are expressed as mean ± standard error of the mean unless otherwise specified. Statistical significance was reported at p values of 0.05 unless otherwise stated.
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Results
tive session. DM was not affected by previous exercise, suggesting that post-exercise reductions in pulmonary diffusing capacity were solely dependent upon reduced pulmonary capillary volume during a second exercise bout. Stroke volume and cardiac output were lower during exercise in the second exercise session (EX2), which may have affected VC during periods of high cardiac demand. Arterial oxygen saturation was reduced with increasing exercise intensity, but this reduction was not affected by previous exercise. Our data show that, as a ‘main effect’ statistic, previous exercise reduced DLCO to a degree consistent with previous studies [5, 18, 22, 30]. However, closer examination of our data complicates this interpretation. Our mean resting DLCO values (28.7 vs. 28.3 mL/min/mmHg) were virtually identical before and after previous exercise, while exercise values were 5–10 % lower during the second exercise session. Similarly, mean resting VC was only 4 % lower after previous exercise, but exercising mean values were 23 % and 17 % lower during the second exercise bout. This may indicate that the reductions in post-exercise pulmonary diffusion were associated with reduced pulmonary capillary volume that was most evident during subsequent intense exercise when cardiac demand was highest. This interpretation contradicts earlier studies that showed reduced DLCO at rest, but did not measure diffusion during exercise. It is possible that differences in protocol explain these discrepancies. We chose a 1- to 2-h period (average of 93 min) between 2 brief, but intense exercise bouts because a similar study showed that a peak reduction in resting DLCO of 8.9 % came during the first hour after a single maximal exercise test [14]. Another study showed that intense cycling induced the greatest reduction in DLCO (10–12 %) 6 h after a very short exercise bout, but approximately 90 % of this reduction had occurred after 2 h in moderately trained and untrained subjects [30]. In comparison, we found that post-exercise DLCO (main effect) was reduced by approximately 5 % and that resting values were only 1.4 % lower. This difference, though significant, is considerably less than the aforementioned studies, raising the possibility that our second session was not ideally timed for a reduction in resting DLCO. Nonetheless, the 8.3 % reduction in mean DLCO during subsequent high-intensity exercise indicates that our protocol reduced DLCO during periods of high cardiac output. Our subject selection may also have contributed to differences between our resting DLCO results and those of previous authors. Bronchoalveolar lavage [13] and pulmonary scintogram [6] studies suggest increased permeability of the pulmonary bloodgas barrier caused by mechanical stresses after high, but not moderate [12] intensity exercise in elite athletes. In addition, the
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▶ Table 1 summarizes the physical charSubject characteristics: ● acteristics, aerobic capacity and pulmonary function of the subjects. Our study population was typical of a young, moderately fit cohort with slightly above average aerobic capacity and pulmonary function. ▶ Table 2 summarizes participant responses during EX1 and ● EX2. The relative exercise intensities ( %VO2peak), pedaling workload and heart rate were not different during EX1 and EX2 (P > 0.05). While cardiac output and stroke volume increased during exercise in both conditions as expected (P < 0.05), the increases were only greater in EX1 than EX2 at a P < 0.10 level. Arterial oxygen saturation decreased linearly with exercise intensity in both conditions, but was not different between EX1 and EX2. ▶ Fig. 1a–c describe the pulmonary diffusion measurements of ● the 2 (EX1 and EX2) conditions. DLCO, VC, and DM increased from rest to moderate exercise (P < 0.05). DL and DM further increased from moderate to intense exercise (P < 0.05). DLCO (P < 0.05) and Vc (at P < 0.10) were decreased in EX2, but not DM. SpO2 was not different between EX1 and EX2 (P = 0.29). The mean differences in DLCO and Vc appeared to be greater during exercise than rest. However, there was not a significant condition by intensity interaction (pre- vs. post-exercise) interaction for DLCO and Vc (P = 0.24 and 0.20 respectively). Similarly, there was no interaction of previous exercise on DM and SpO2 (P = 0.32 and 0.27 respectively).
Discussion
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The primary findings of this study were that DLCO and Vc were reduced during exercise performed 1–2 h after a prior exhausTable 1 Subject characteristics.
age (years) height (cm) weight (kg) BMI VO2peak (L/min) FVC ( % predicted) FEV1 ( % predicted) SVC ( % predicted) MIP (cm H20)
Average ± SEM
Range
21 ± 1 177 ± 3 73 ± 4 23.1 ± 1.0 3.34 ± 0.23 106 ± 4 103 ± 4 108 ± 4 148 ± 12
18–25 170–188 53–88 18.2–27.3 2.20–4.51 91–125 80–115 94–125 95–200
Table 2 Physiological responses at rest, moderate and high intensities during the first and second bouts of exercise. Rest EX1 cardiac output (L/min) stroke volume (mL) SaO2 ( %) workload (W) VO2 (L/min) %VO2max heart rate (bpm)
7.5 ± 0.7 86.4 ± 9.1 96.5 ± 0.4 – 0.60 ± 0.10 – 88 ± 3.6
Moderate intensity EX2 7.0 ± 0.5 75.5 ± 6.1 95.5 ± 0.6 – 0.53 ± 0.07 – 94 ± 2.0
EX1 †*
20.0 ± 2.0 126 ± 12.6†* 93.7 ± 0.8 † 157 ± 12 2.38 ± 0.19† 71.4 ± 1.4 159 ± 2.4 †
*
Data are average ± SEM
† (P < 0.05) different from rest (combined EX 1 and EX 2 moderate) # (P < 0.05) different from moderate intensity (combined EX1 and EX2) *
(P < 0.10) EX1 vs. EX2 within condition
Baldi JC et al. Prior Maximal Exercise Decreases … Int J Sports Med 2014; 35: 982–986
High intensity
EX2
EX1 †
19.2 ± 2.0 121 ± 12.0† 93.6 ± 1.0 † 157 ± 13 2.33 ± 0.19† 69.5 ± 1.9 161 ± 9.0†
EX2 †#*
23.3 ± 2.2 130 ± 13.6†#* 91.6 ± 0.9 †# 205 ± 18 # 2.94 ± 0.26†# 89.2 ± 1.8 # 182 ± 3.6 †#
21.7 ± 1.7†# 118 ± 10.0†# 90.4 ± 1.4†# 206 ± 17 # 2.93 ± 0.25†# 89.0 ± 2.1 # 184 ± 3.6†#
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984 Physiology & Biochemistry
a
55
DLCO (mL/min/mmHg)
50 45
*
40 35 †
‡
Moderate
High
30 25 20 Rest
Workload DLCO EX1 b
DLCO EX2
220 200
VC (mL)
180 160
**
140 120 †
100 80 Rest
Moderate
High
Workload VC EX1 VC EX2
DM (mL/min/mmHg)
c
80 70 60 50
‡ †
40 30 Rest
Moderate
High
Workload DM EX1
DM EX2
Fig. 1 a–c Diffusing capacity for carbon monoxide (DLCO), pulmonary capillary volume (VC) and alveolar capillary membrane diffusing capacity (DM) during rest, moderate intensity and high-intensity exercise. Solid circles represent values obtained during the first exercise session and open circles are from a second session. * P < 0.05) first vs. second testing session. ** (P < 0.10) first vs. second testing session. † (P < 0.05) different from rest. ‡ (P < 0.05) different from moderate exercise.
majority of early studies reporting a post-exercise reduction in DLCO were conducted in trained athletes [6, 17, 18, 20, 25–27], which may be a poor comparison for the present study. Our subjects were typical of healthy active, but untrained young adults. Consequently, it is possible that the exercise intensities performed by our subjects failed to produce sufficient mechanical stress to alter the blood gas barrier. However, this cannot explain why Sheel et al. [30] found that there was no difference in postexercise reduction in DLCO in trained vs. untrained athletes. Our finding that cardiac output and pulmonary capillary volume were reduced during EX2 (p < 0.10), despite nearly identical workloads with EX1, is consistent with a reduction in central intravascular volume that affected pulmonary capillary volume [7, 19]. Nagashima et al. [21] showed that plasma volume is reduced by 2.1 % 2 h after a single bout of upright exercise. Moreover, Hanel and colleagues found that the distribution of 99 m Tc erythrocytes shifted away from the thoracic cavity and towards the periphery 2½ h after intense rowing exercise. They also reported that the blood volume shift corresponded to a reduction in DLCO and atrial natriuretic peptide, which responds in proportion to venous return [7]. If the subjects in this study had a similar reduction and redistribution of intravascular volume, it would explain the observed decrease in stroke volume. It might also explain how resting pulmonary capillary volume, which is affected by cardiac output, was maintained by increased heart rate (88 vs. 94 bpm in EX1 vs. EX2), while high-intensity exercise values, which are dependent on cardiac reserve, were reduced during EX2. Contrary to our second hypothesis, our data do not provide evidence that a previous bout of high-intensity exercise reduces subsequent aerobic performance due to decreased PaO2, which is consistent with the findings of McKenzie et al. [19]. Despite reduced DLCO, there were no differences in workload or heart rate during the 2 high-intensity exercise sessions. In our study, average SpO2 values during the first and second high-intensity exercise sessions (91.6 vs. 90.4 %) were typical of exercise performed at this altitude (2 100 meters) and were not different between exercise bouts. While acknowledging that pulse oximeter measurements have limitations, we interpret our data as suggesting that changes in DLCO caused by previous exercise are unable to significantly reduce SpO2 during subsequent highintensity whole body exercise, at least in non-endurance athletes. In summary, this study expanded upon previous studies by showing that resting and exercising DLCO and Vc were reduced, and cardiac output was lower following a previous bout of intense exercise in healthy untrained subjects. Previous exercise did not affect DM in this study, suggesting that lower post-exercise DLCO was caused by reduced pulmonary capillary volume. Our data also suggest that reductions in DLCO are more severe during subsequent exercise. The reductions in DLCO were not associated with reduced SpO2.
Acknowledgements
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This project was funded by NIH Grant R15 HL097335-01A1.
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