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1 Allan McGavin Sports Medicine Centre and School of Human Kinetics, University of British Columbia, Vancouver, British Columbia V6T 1Z3; and 2 Division of Nuclear Medicine, Department of Radiology, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z1
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The effect of incremental exercise to exhaustion on
the change in pulmonary clearance rate (k) of aerosolized
99mTc-labeled diethylenetriaminepentaacetic acid
(99mTc-DTPA) and the relationship between k and
arterial PO2 (PaO2) during
heavy work were investigated. Ten male cyclists (age = 25 ± 2 yr, height = 180.9 ± 4.0 cm, mass = 80.1 ± 9.5 kg, maximal O2 uptake = 5.25 ± 0.35 l/min,
mean ± SD) completed a pulmonary clearance test shortly (39 ± 8 min) after a maximal O2 uptake test. Resting pulmonary
clearance was completed 
24 h before or after the exercise test.
Arterial blood was sampled at rest and at 1-min intervals during
exercise. Minimum PaO2 values and maximum alveolar-arterial PO2 difference ranged from 73 to 92 Torr and from 30 to 55 Torr, respectively. No significant
difference between resting k and postexercise k
for the total lung (0.55 ± 0.20 vs. 0.57 ± 0.17 %/min,
P > 0.05) was observed. Pearson product-moment correlation indicated no significant linear relationship between change
in k for the total lung and minimum PaO2
(r = 
0.26, P > 0.05). These results
indicate that, averaged over subjects, pulmonary clearance of
99mTc-DTPA after incremental maximal exercise to exhaustion
in highly trained male cyclists is unchanged, although the sampling
time may have eliminated a transient effect. Lack of a linear
relationship between k and minimum PaO2
during exercise suggests that exercise-induced hypoxemia occurs despite
maintenance of alveolar epithelial integrity.
pulmonary clearance of technetium-99m-diethylenetriaminepentaacetic acid; alveolar epithelium; gas exchange
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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EXERCISE-INDUCED
HYPOXEMIA (EIH), defined as the inability to maintain arterial
PO2 (PaO2) and arterial
oxyhemoglobin saturation (SaO2) during exercise,
occurs in some high-aerobic-power athletes and is associated with a
widened alveolar-arterial PO2 gradient (A-aPO2) (3, 4, 12, 29). The
precise etiology of EIH and the widened A-aPO2
remains unclear but is likely the result of, or an interaction among,
relative alveolar hypoventilation, ventilation-perfusion
(
A/
) inequality, and diffusion limitations (3, 25). Hopkins et al. (12), using the
multiple inert gas elimination technique, reported that 60% of the
widened A-aPO2 in highly trained athletes could
be explained by A/ inequality, whereas the
remainder was attributed to a diffusion limitation. This group has also
reported that athletes who develop EIH have high cardiac outputs, low
mixed venous PO2, and shortened pulmonary transit times (10).
Several authors have suggested that intense exercise might result in
injury to the alveolar-capillary membrane. West et al. (34) introduced the concept of "stress failure" after
they demonstrated disruptions to the capillary endothelium, alveolar
epithelium, and their respective basement membranes, in a rabbit lung
model when pulmonary arterial pressures were raised to 40 Torr.
Indirect evidence that may support the theory of stress failure in
humans includes several anecdotal reports of human athletes who have coughed up or tasted blood after strenuous exercise (32,
33). In addition, an increase in red blood cells (RBCs) and
protein has been reported in bronchoalveolar lavage fluid obtained
after 7 min of maximal exercise (13). This finding
supports the theory that structural failure of the blood-gas barrier
can result from heavy physical work. However, in these studies,
PaO2 or SaO2 was not measured, which
leaves the relationship between blood-gas barrier integrity and
gas exchange during intense exercise unresolved.
High pulmonary capillary perfusion pressure during heavy exercise may result in damage to the pulmonary capillaries and altered integrity of the blood-gas barrier. To permit efficient gas exchange by diffusion, the barrier between the alveoli and the capillaries must be extremely thin. In some sections it may measure only 0.3 µm (7). In contrast, the blood-gas barrier must also be strong enough to withstand elevated pulmonary vascular pressure associated with high cardiac output during intense exercise.
99mTc-labeled diethylenetriaminepentaacetic acid (99mTc-DTPA) has been used as a nonspecific, but extremely sensitive, method for detecting lung pathology (1, 22). 99mTc-DTPA is hydrophilic and normally limited to passive diffusion through the intercellular junctions of the alveolar epithelium and the capillary endothelium (5, 15). Alveolar epithelial junctions are 10 times less permeable than capillary endothelial junctions (8), and therefore diffusion of 99mTc-DTPA through the blood-gas barrier is primarily dependent on the permeability of the alveolar epithelial membrane. Damage to the blood-gas barrier during exercise, sufficient to alter permeability of the alveolar epithelium, would likely be detected by the change in the pulmonary clearance rate of 99mTc-DTPA. We hypothesized that alveolar epithelial permeability in highly trained cyclists after an incremental exercise test to exhaustion would be increased and related to the impairment in gas exchange.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects and preliminary tests.
Subjects reported to the laboratory 3 h postprandial and 24 h
after exhaustive exercise. Spirometry involved resting measurements of
forced vital capacity, forced expiratory volume in 1 s, and maximal forced expiratory flow (MedGraphics CPX-D Metabolic Cart, St.
Paul, MN). A maximal O2 uptake
(O2 max) test was performed on an
electronically braked cycle ergometer (Quinton Excalibur, Gronigen, The
Netherlands) starting at 0 W and increasing by 30 W/min until
volitional fatigue. A minimum O2 max of
65 ml · kg
1 · min1 or 5.0 l/min [determined as the average of the 2 highest consecutive 15-s
O2 consumption (O2) scores]
was required for further participation in the study. Ten competitive
male cyclists or triathletes who met this criterion were selected. All
subjects were nonsmokers and had no history of cardiorespiratory
disease. Participants signed an informed consent that described the
inherent risks associated with the study. All experimental procedures
were approved by the University Clinical Ethics Review Board.
Experimental protocol.
At least 48 h after preliminary tests, subjects returned to the
laboratory. On arrival, an arterial catheter was inserted into the
radial artery of the nondominant wrist before exercise, and blood was
sampled to measure PaO2, arterial
PCO2 (PaCO2), bicarbonate
(HCO3), and pH. After catheter insertion, subjects
completed a O2 max test (with use of
the same protocol described in the preliminary tests). Arterial blood
samples (3 ml) were collected immediately before the onset of exercise
and at 1-min intervals (starting at minute 4) for the
duration of the exercise test. Minute ventilation, O2, and heart rate (HR) were
continuously measured during exercise. Pulmonary clearance was
determined using 99mTc-DTPA aerosol in all subjects shortly
after the exercise test, with an average time interval between the
completion of the exercise test and after pulmonary clearance of
38 ± 8 (SD) min. Resting pulmonary clearance was completed 24 h
before or after the exercise test. HR was recorded during both lung
clearance tests.
Instrumentation. Ventilatory parameters were measured for the duration of the exercise tests with a low-resistance, two-way nonrebreathing valve (model 2700B, Hans Rudolph) and a 5-liter mixing chamber for collection of expired gases. From this chamber, continuous samples of air were analyzed for concentrations of O2 and CO2 at a rate of 300 ml/min (S-3A O2 analyzer and CD-3A CO2 analyzer, Applied Electrochemistry). Analyzers were calibrated with gases of known concentration before each test. Inspired ventilation was measured with a flowmeter (model 17150, Vacumetrics). This device was calibrated by pumping 100 liters of air through the system. Average ventilatory and gas exchange parameters were recorded every 15 s with use of a computerized system (Rayfield, Waitsfield, VT). HR was measured continuously and recorded every 15 s with a portable HR monitor (Polar Vantage XL, Kempele, Finland).
Following Allen's test for collateral circulation, a 20-gauge arterial catheter was inserted into the radial artery of the nondominant wrist by percutaneous cannulation with 1% lidocaine and sterile technique. Minimum-volume extension tubing, connected in series with two three-way stopcocks arranged at right angles, was flushed with saline-heparin solution (1 ml of 1:1,000 U in 500 ml of normal saline). A rapid-response (<0.01 s) thermistor (model 18T, Physitemp Instruments, Clifton, NJ) was inserted through a Touhy-Borsch heparin lock (Abbott Hospitals, North Chicago, IL) and used to measure peak arterial blood temperature during collection of the blood sample. Catheter patency was maintained with intermittent heparin infusion (<3 ml/h). Blood samples were placed on ice until analyzed for H+ concentration, PO2, PaCO2, and HCO3 (model 278 blood-gas
system, CIBA-Corning Diagnostics, Medfield, MA). Blood gases were
corrected for temperature. Arterial blood temperature increased
0.8 ± 0.2°C during the O2 max
test. SaO2 levels were calculated on the basis of
PaO2, changes in body temperature, and pH. The
alveolar gas equation was used to calculate the alveolar
PO2 and A-aPO2
(23).
The aerosol was created in a nebulizer by introducing 20-30 mCi
(740-1,110 MBq) of 99mTc-DTPA in 2 ml of saline and
driving it with compressed air at a flow rate of 10 l/min (Venti-Scan
III Disposable, Biodex Medical, New York, NY). Breathing procedures
were rehearsed before inhalation of the aerosol to ensure optimal
delivery. Each subject was fitted with a noseclip and a mouthpiece and
instructed to breathe through a two-way valve at normal tidal volumes
for 3 min in the seated position. The exhalate was trapped in a filter.
A dose of ~1-2 mCi (37-74 MBq) was administered to the
subject. The subject was seated with a large field-of-view gamma
scintillation camera (Siemens Orbiter, Iselin, NJ) positioned
posteriorly and set to image the entire lungs for 30 min. Subjects were
instructed to remain motionless during data acquisition.
Data analysis.
Output from the gamma camera was processed by computer. Decline in
radioactivity over time was recorded in 30-s image frames consisting of
a computer image of 128 × 128 pixels. Computer analysis of
regions of interest was carried out around each lung (left and
right); then each lung was further divided into regions
corresponding to apical and basal regions. The data obtained for the
total, left, right, apical, and basal regions were corrected for
physical decay and then plotted as a function of time. The data for all regions were fit by a monoexponential function: N = N0ekt, where
N0 is the y-intercept or count rate
at time 0, N is the count rate at any
time t (min), and k is the rate
constant for clearance. Total (kT), right
(kR), left (kL), apical
(kA), and basal (kB)
clearance rate constants were determined over the acquisition period
and expressed as a percentage of decreased radioactivity per minute
(%/min). No correction for recirculation was made.
Statistical analyses.
Differences in resting kT and postexercise
kT were analyzed by one-way ANOVA with repeated
measures. Two 2 (resting/postexercise) × 2 (region) ANOVAs with
repeated measures on both factors were used to assess differences for
kR and kL, as well as
differences for kB and
kA. Pearson product-moment correlation was used
to determine the strength of the linear relationship between
PaO2 and A-aPO2 and between
the change in kT
(
kT = postexercise
kT resting kT)
and the minimum PaO2 measured during exercise. A t-test for dependent means was used to determine differences
between HRs measured during the pulmonary clearance tests. A
t-test for dependent means was also used to determine
differences between PaO2 measured before exercise and
at maximum exercise. All significance was set at 
< 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Performance.
Anthropometric and lung parameters are shown in Table
1. Forced vital capacity, forced
expiratory volume in 1 s, and maximal forced expiratory flow were
within normal values predicted for men of similar age, height, and
weight. Performance variables obtained at maximal exercise are shown in
Table 2. Maximum respiratory exchange
ratio exceeded 1.15 and peak HR exceeded 90% of maximum predicted HR
(220 age) in all subjects.
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Gas exchange.
Figure 1 shows individual
PaO2,
A-aPO2, and
PaCO2, respectively, during the
progressive exercise test. Mean PaO2 at maximal exercise decreased significantly from resting levels (from
114.3 ± 4.4 to 87.1 ± 8.4 Torr, P < 0.05).
In three subjects the lowest PaO2 during exercise
remained between 90 and 100 Torr, in five subjects the lowest
PaO2 fell to 80-90 Torr, and in the three remaining subjects PaO2 during exercise fell to <80
Torr. The maximum A-aPO2 ranged from 30 to 55 Torr [42.5 ± 7.0 (SD) Torr]. There was a significant
negative correlation between PaO2 and A-aPO2 (r = 0.94,
P < 0.05). At maximal exercise, five subjects decreased PaCO2 levels below 36 Torr, whereas
in four subjects, PaCO2 values did not fall
below 38 Torr. Arterial pH and HCO3 levels remained
unchanged from light to moderate exercise intensity but progressively
declined during moderate to heavy exercise. Minimal values at maximal
exercise for pH and HCO3 reached 7.2 ± 0.1 and
14.1 ± 2.5 nmol/l, respectively.
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Pulmonary clearance.
The quality of the goodness of fit (R2) for the
total lung averaged 0.99. The resting and postexercise
kT for individual subjects is shown in Fig.
2. Pulmonary clearance rates averaged
over subjects for each region at rest and after exercise are shown in
Fig. 3.
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Pulmonary clearance and gas exchange.
There was no significant relationship (r = 0.26,
P > 0.05) between the minimum PaO2
obtained during the exercise test and kT
(Fig. 4). In addition, there was no
significant relationship (r = 0.07, P > 0.05) between the maximal A-aPO2 and
kT.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Pulmonary clearance and exercise.
The O2 max values and peak power
outputs indicated that these subjects were highly trained, whereas the
range of EIH and A-aPO2 during exercise were
consistent with other studies involving highly trained male athletes
(3, 12, 24).
A/ inequality observed during exercise and in the immediate recovery period. Human pulmonary arterial pressures at
maximal exercise can reach 40 mmHg (31), which is in the range shown to cause stress failure of the blood-gas barrier in a
rabbit lung model (34). At this magnitude, raised
transmural pulmonary vascular pressures in rabbits show disruption to
the capillary endothelium and the alveolar epithelium, and in some cases RBCs can be seen passing through the membranes (30,
34). RBCs and protein have been recovered from bronchoalveolar
lavage fluid from athletes after 7 min of heavy exercise compared with resting sedentary controls (13). These results suggested
loss of blood-gas barrier integrity. All six athletes recruited,
however, had a history of hemoptysis after intense exercise. None of
the athletes in the present study had such a history. Therefore, the conclusions from this study and the present one may not be comparable.
Hopkins et al. (14) performed broncholavage in athletes
after 1 h of submaximal exercise (77% of
O2 max) and found no evidence of RBC
and protein, indicating no or little damage to the membrane. There was
an unexpected finding of RBCs in the lavage fluid of resting control
subjects, questioning the sensitivity of this technique for
investigating blood-gas barrier integrity. Collectively, it appears
that prolonged submaximal exercise may alter Starling's forces and
result in a net fluid flux with or without alteration of the structural
integrity of the blood-gas barrier. Unfortunately, none of these
studies measured PaO2 or SaO2, and,
therefore, it is unknown whether extravascular lung water from
submaximal exercise is of sufficient magnitude to impair gas exchange.
The results from the present study do not exclude pulmonary
interstitial edema as a possible mechanism for the EIH and elevated A-aPO2 observed in our subjects, inasmuch as
this method is not a sensitive indicator of hemodynamically induced
pulmonary edema. Indeed, patients with cardiogenic edema can have a
normal DTPA clearance, despite significant clinical edema
(18).
Lorino et al. (16) assessed pulmonary clearance with
99mTc-DTPA in seven healthy volunteers before and after 75 min of exercise corresponding to 75% of the subject's
O2 max. After exercise, total, apical,
and basal clearance rates were significantly increased. They concluded
that the increased alveolar permeability was related to the mechanical
effects of prolonged, high ventilation rates. This is compatible with
data from the rabbit model where increasing lung volumes along with
constant pulmonary arterial pressure increased the incidence of stress
failure in rabbits (6). In a pilot study we investigated
whether ventilation rates alone would alter alveolar permeability in
five subjects. Isocapnic ventilation rates were assigned following data
previously obtained during a O2 max
test (~15 min duration). Mean minute ventilation reached a maximum
value of 145 ± 29 l/min during isocapnic ventilation. Total
pulmonary clearance rates remained unchanged before and after (30 ± 5 min) the O2 max test (0.54 ± 0.02 and 0.57 ± 0.03%/min, respectively, P > 0.05).
O2 max values in the study by Lorino et
al. (16) only reached 53 ± 3 ml · kg1 · min1, and the
O2 during the 75 min of exercise was
40 ± 2 ml · kg1 · min1. We believe
that stress failure would have been unlikely in these subjects,
inasmuch as pulmonary arterial pressures do not reach high values
during submaximal exercise, even if exercise is prolonged (11). Therefore, it seems unlikely that mechanical effects
of sustained ventilation and/or stress failure altered the alveolar epithelial permeability in the study by Lorino et al. Their exercise period was much longer than that in the present study (75 vs. 16 min),
and the DTPA measurement was made 25 min after exercise vs. 40 min
after exercise in this study. It is possible that the differences in
pulmonary clearance rate are a result of the longer exercise duration,
or possibly the longer recovery period in the present study missed a
transient change in pulmonary clearance immediately after exercise. For
many reasons, the study by Lorino et al. is not comparable to the
present investigation.
St. Croix et al. (27) have argued that EIH during heavy
exercise may reflect a functionally based mechanism, present only during exercise, rather than stress failure; a structural mechanism would be expected to have lasting effects. Their subjects performed a
progressive incremental exercise test to
O2 max followed by a constant load at
maximal workload 20 min later. A slight improvement in
PaO2 and A-aPO2 was found
during the second exercise bout. Therefore, a functional mechanism,
such as decreased mixed venous O2 saturation, combined with
high cardiac output to an already fully dilated and recruited pulmonary
vasculature, may decrease pulmonary capillary transit time and
result in decreased end-capillary O2, widened
A-aPO2, and EIH (10).
Methodological concerns. All subjects in the present study were nonsmokers. Pulmonary clearance rates in our subjects at rest were considered normal for healthy individuals (26). Faster apical than basal clearance rates reflect greater apical ventilation and greater surface area available for diffusion of 99mTc-DTPA (17, 18, 21).
It is possible that blood-gas barrier remodeling occurred in the time delay between the exercise test and the postexercise pulmonary clearance test. This time delay was designed to allow pulmonary blood flow and ventilation to return to near resting values. However, HRs recorded during the inhalation of the aerosol remained significantly elevated after exercise compared with resting, and it is uncertain whether pulmonary capillary blood volume and/or the area available for gas exchange was altered. Background correction for recirculation of radioactivity through the pulmonary capillaries is a contentious issue (2). Several studies (16, 20) have ignored recirculation and have argued that background radioactivity does not significantly affect the measured clearance rate. It is known that the rate at which the aerosol leaves the blood by normal kidney filtration is 10-fold faster than the rate the aerosol enters the blood through the blood-gas barrier (9). In contrast, using the liver for background correction, Mason et al. (19) recently demonstrated that when intravenous DTPA was administered before inhalation of the aerosol, pulmonary clearance curves were multiexponential. However, when the thigh was used for background correction, the pulmonary clearance curves were monoexponential. Apparently, the liver has a closer extravascular-to-intravascular compartment ratio to the lung, and therefore the authors concluded that liver background correction allows the true shape of the curve to be identified. Clearance curves in the present study were analyzed for 30 min and not corrected for recirculation. Staub et al. (28) reported that correction for recirculation was less of a concern if clearance curves were calculated within this time period. In conclusion, averaged over subjects, pulmonary clearance of 99mTc-DTPA after incremental maximal exercise to exhaustion in highly trained male cyclists was unchanged. Furthermore, there was no relationship between altered pulmonary clearance and the minimum PaO2 during heavy exercise, suggesting that exercise-induced hypoxemia occurs despite maintenance of alveolar epithelial integrity.| |
ACKNOWLEDGEMENTS |
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The authors thank Kirsten Struck, Diana Jespersen, and Dr. Jim Potts for technical assistance and Dr. Robert Schutz and Dr. Donald Lyster for helpful criticism.
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FOOTNOTES |
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M. R. Edwards was supported by the Natural Sciences and Engineering Research Council of Canada.
Address for reprint requests and other correspondence: D. C. McKenzie, Allan McGavin Sports Medicine Centre, 3055 Wesbrook Mall, Vancouver, BC, Canada V6T 1Z3 (E-mail: kari{at}interchange.ubc.ca).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 27 August 1999; accepted in final form 14 June 2000.
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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