J Appl Physiol Articles in PresS. Published on August 16, 2002 as DOI 10.1152/japplphysiol.01108.2001
JAP 1108-2001.R2
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Ventilation-perfusion inequality during normoxic and hypoxic exercise in the emu
P.M. Schmittb,+, F.L. Powella,b, and S.R. Hopkinsa*
a
Department of Medicine, University of California San Diego, 9500 Gilman Drive, 0623A, La Jolla, CA 92093-0623
b
White Mountain Research Station, University of California San Diego, 9500 Gilman Dr. 0689, La Jolla, CA 92093-0689
Susan R. Hopkins, M.D., Ph.D.
Department of Medicine
University of California, San Diego
9500 Gilman Drive, 0623A
La Jolla, CA 92093-0623
Tel: (858) 534-2680
Fax: (858) 534-4812
Email: [email protected]
+
Current Address:
Department of Internal Medicine
University of California, Davis
One Shields Avenue
Davis, CA 95616-8636
Copyright 2002 by the American Physiological Society.
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*Corresponding Author:
JAP 1108-2001.R2
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Abstract: Many avian species exhibit an extraordinary ability to exercise under hypoxic
condition compared to mammals and more efficient pulmonary oxygen transport has been hypothesized to
contribute to this avian advantage. We studied 6 Emus (Dromaius novaehollandaie, 4-6 months old, 2540 kg) at rest and during treadmill exercise in normoxia (N) and hypoxia (H; FIO2≈0.13). The multiple
. .
inert gas elimination technique (MIGET) was used to measure V/Q distribution of the lung and calculate
.
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cardiac output ( Q T ) and parabronchial ventilation ( VP ). In both N and H, exercise increased PaO2 and
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decreased PaCO2, reflecting hyperventilation, while pH remained unchanged. The V/Q distribution was
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unimodal with a log standard deviation of Q distribution = 0.60±0.06 at rest, this did not change
conditions. CO2 elimination was enhanced by hypoxia and exercise but O2 exchange was not affected by
exercise in normoxia or hypoxia. The stability of ventilation-perfusion matching under conditions of
hypoxia and exercise may be advantageous for birds flying at altitude.
Keywords: Inert gases, comparative gas exchange, altitude, birds.
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significantly with either exercise or hypoxia. Intrapulmonary shunt was <1% of the cardiac output in all
JAP 1108-2001.R2
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Introduction
Birds are known for their extreme tolerance to hypoxia, and the ability to cope with high oxygen
demands in hypoxia. For example, Barheaded geese use energetically expensive flapping flight to
migrate at altitudes that would render an unacclimatized human unconscious (26). In hummingbirds,
hovering flight results in the highest mass specific oxygen uptake in an exercising vertebrate, and this can
be maintained up to simulated altitudes of 6 km (1). One of the most obvious differences in oxygen
transport between birds and mammal is the unique structure of their respiratory systems (17). The
confer an advantage for birds over mammals during exercise at altitude (16, 25). For instance, the crosscurrent model of gas exchange for avian lungs predicts a negative expired-arterial PO2 difference, while
the best that can be achieved in mammals is zero.
The quantitative role of cross-current gas exchange in explaining the abilities of birds at altitude is
not clear, however. For example, in extreme hypoxia, the advantage of cross-current gas exchange,
compared to alveolar gas exchange, is predicted to decrease (25). However, at an altitude equivalent to
the summit of Mount Everest, cross-current exchange is still predicted to provide an advantage over
alveolar exchange equivalent to descending 700m (25). Experiments on birds exercising in normoxia
show that gas exchange is similar to mammals (reviewed by ref. 17). The only studies on birds exercising
in hypoxia that have measured all of the necessary data to calculate O2 exchange efficiency, were done on
Barheaded geese and Pekin ducks running on a treadmill (6,14). However, maximal O2 consumption was
.
not reached by these flying birds during running exercise, and the measured VO2 increased 1.5 to 3 fold,
i.e. much less than the levels expected during flapping flight to reach high altitudes.
Another limitation of previous studies is the inability to distinguish between the different
physiological factors that prevent gas exchange from operating at ideal levels. The main factors are
. .
ventilation-perfusion (V/Q) heterogeneity and diffusion limitation. Distinguishing between these factors
is complicated because ventilation-perfusion heterogeneity can affect gas exchange "as if" there were a
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structure-function relationship of the avian respiratory system has been modeled and is hypothesized to
JAP 1108-2001.R2
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. .
diffusion limitation. However, the consequences of V/Q heterogeneity and diffusion limitation are not
necessarily the same under different conditions, (e.g. hypoxia and normoxia), so one cannot extrapolate
from experimental measurements to other interesting situations in nature.
Therefore, this study was designed to quantify O2 exchange and ventilation-perfusion
heterogeneity in birds exercising in normoxia and hypoxia. We chose emus because running is their
normal mode of locomotion. Running emus are capable of obtaining O2 consumption rates (corrected for
body mass) that are equivalent to flying birds and are significantly greater than rates measured during
We hypothesized that the avian lung would show improved efficiency of gas exchange during hypoxia
exercise compared to mammals.
Methods
This study was approved by the Animal Subjects committee of the University of California, San
Diego. Starting at 2 weeks of age, eleven Emus, were trained to run on a treadmill (Jager,
Model#8203410H3N, Jaeger Hoechberg, Germany) wearing a light weight plastic mask constructed in
our laboratory. Six of the emus of either gender, aged 4-6 months, who were the best runners were
selected for further study (weights = 32 ± 5kg, range 25-40 kg).
Surgical preparation. Surgical anesthesia was induced with Diazepam (0.1 mg • kg-1 i.m.)
followed by Isoflurane 4-5% in 100% oxygen. The birds were intubated and their necks were wrapped
lightly with an elastic (Ace) bandage to prevent inflation of the tracheal air sac. This air sac is used for
vocalization and acts as increased anatomical deadspace if allowed to inflate. Anesthesia was maintained
with 2-3% isoflurane. Under sterile conditions, catheters were placed in the carotid artery (PE 90), the left
jugular vein at the upper third of the neck (7Fr, 24 cm) and a wing vein (PE90). The catheter sites were
cleaned and catheters were flushed with heparin (1,000 IU/ml) and filled with a PVP-Heparin-Saline
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running in birds that normally fly, e.g. water fowl (2). Furthermore, their large body size permits multiple
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blood samples required for the multiple inert gas elimination technique for measuring V/Q heterogeneity.
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solution (0.5 ml 5000 IU Heparin, 9.5 ml Saline, 0.3g PVP) to maintain patency. Animals were allowed
to recover at least 24 hours before study.
Protocol. On the day of the experiment, a triple lumen Swan Ganz catheter with thermistor (size
#7 F) was inserted into the lumen of the jugular cannula, advanced via the external jugular vein and into
the right ventricle, and when possible into the pulmonary artery, using direct pressure monitoring. This
catheter was used for sampling of pulmonary mixed venous blood and measurement of blood temperature.
The experiments took place in a temperature-controlled ventilated room (21-23˚C). Data were collected
after at least 20 minutes of rest and after 5 minutes of exercise in normoxia and normobaric hypoxia (FIO2
(determined during previous training sessions). Each set of measurements included sampling of
pulmonary mixed venous blood, arterial blood and mixed expired gases for the multiple inert gas
analyses, blood gases, cardiac output calculations and metabolic rate measurements.
After normoxic measurements, hypoxic measurements at rest and during exercise were made at a
simulated altitude of 3,300-4,000m by adding nitrogen to a tent surrounding the treadmill to lower the
FIO2 to 0.13-0.14. FIO2 and FICO2 were monitored continuously using a mass Spectrometer (Perkin-Elmer,
MGA1100, Pomona CA). Small amounts of nitrogen were added during the hypoxic study to maintain a
constant FIO2. Because of logistical constraints, it was necessary to study hypoxia last, so the order of
FIO2 was not randomized.
Ventilation, and metabolic measurements. A custom-made facemask (without valves) was
strapped to the animals head and room air was drawn through the mask at a rate of 80 L/min at rest and
~160 L/min during exercise using a vacuum. This bias flow rate was determined to be sufficient to
collect all expired gas by testing for CO2 leak using the mass spectrometer probe placed at the back of the
animal’s mask. Room air was drawn around the animal’s face and mixed with the expired gas in a small
light weight, heated respiratory tubing (Hans Rudolph 10.5mm OD, Kansas, City, MO) leading into a
heated mixing chamber. Total flow (i.e. bias and expired gas) was measured using a pneumotachometer
(Fleisch #3) and integrated to obtain volume. Gas temperature and relative humidity were measured in
the gas stream adjacent to the pneumotach. The expired concentrations of O2 and CO2 were measured
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= 0.13-0.14) at sea level. Running speed was increased to the maximum the bird could sustain,
JAP 1108-2001.R2
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with the mass spectrometer during each inert gas sample collection period, and oxygen consumption and
carbon dioxide production were calculated.
Multiple inert gas measurements. The multiple inert gas elimination technique (MIGET) was
applied in the usual manner (19, 20, 29). The inert gas solution was prepared in 5% dextrose (7) and
infused for approximately 20 minutes prior to collection of the resting samples, and during the course of
the study at a rate in ml/min of approximately 10% of the bias flow rate in l •min-1 (for example an
infusion rate of 8 ml/min was matched to a bias flow of 80 L/min). This infusion rate provides excellent
signal-to noise ratio for all six inert gases at all exercise levels.
systemic arterial blood were obtained in gas-tight syringes at rest and during exercise in normoxia and
hypoxia for measurement of the steady state concentrations of the six inert gases (SF6, ethane,
cyclopropane, enflurane, ether and acetone) using a gas chromatography (Hewlett-Packard 5890A,
Wilmington, DE) (29). Solubility, retention (R, equal to the ratio of arterial to mixed venous partial
pressure) and excretions (E, equal to the ratio of mixed expired to mixed venous partial pressure) for the
inert gases were determined, corrected for body temperature, and ventilation-perfusion distributions were
.
. .
calculated using assuming a cross current lung model (19). The second moment of the Q vs. V/Q
.
. .
distribution, exclusive of intrapulmonary shunt (logSDQ. ), and the second moment of the V vs. V/Q
.
distribution, exclusive of dead space (logSDV ) were used as indicators of the degree of ventilation. .
.
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perfusion heterogeneity, i.e. the greater the logSDQ or the logSDV , the greater the V/Q heterogeneity. The
residual sum of squares (RSS) was used as an indicator of the adequacy of fit of the data to the cross
current model of the lung (19).
There was excessive loss of acetone in the expired gas samples, likely due to difficulty in heating
the mask with high bias flows while it was on the animal. Therefore we report data derived from 5 gases
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only. The effect of the elimination of acetone from the analysis is a decrease in the resolution of V/Q
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distributions at V/Q >10. Without acetone the next most soluble gas, ether, allows the distinction of lung
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units with approximately V/Q < 10 from dead space, which results in a dead space similar to
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physiological dead space determined from CO2 measurements (20). Hence, parabronchial ventilation (V
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Quadruplicate 15 ml samples of mixed expired gas and duplicate 4 ml samples of pulmonary and
JAP 1108-2001.R2
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P,
analgous to alveolar ventilation in mammals) was estimated as the product of (1-VD/VT) and the bias
.
. .
flow rate and VP includes any lung units with V/Q <10. To predict excretions without the effect of
dilution by deadspace gas (i.e. end-parabronchial values, analogous to alveolar values in mammals) we
used the equation:
E*gas = Egas/Eether
Hemodynamic measurements. Cardiac output was calculated from the mixed venous, arterial
blood and mixed expired inert gas concentrations using the Fick principle of mass balance.
Statistical Analyses. Data are presented as means ± SEM. Repeated measures analysis of
and during normoxia and hypoxia. Significance was accepted at p<0.05, two-tailed.
Results
For technical reasons, metabolic and respiratory parameters, as well as venous blood gas samples
. .
and consequently calculated cardiac output and V/Q distributions were not obtained in all birds under all
conditions. The numbers of measurements obtained under different conditions are given in Tables 1 and
2.
Metabolic and cardiorespiratory data. Metabolic, ventilatory and hemodynamic data are
.
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presented in Table 1. During normoxia, the emus ran between 1.4 and 2.0 m• sec-1and both VO2 and VCO2
.
increased over 5 fold. Hypoxia did not significantly affect VCO2 during rest although it tended to be
higher, consistent with the increased restlessness we observed in the emus during hypoxia. Both running
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speed (1.04 m/sec) and VCO2 tended to be lower in hypoxia than in normoxia but this was not significant.
Cardiac output increased significantly between rest and exercise, and between normoxia and hypoxia, but
there was no significant interaction between oxygen level and exercise. Both heart rate and increases in
calculated stroke volume contributed to increases in cardiac output.
Blood gases. Arterial and mixed-venous blood gases are reported in Table 2. Exercise in
normoxia decreased PaCO2 , increased pHa, and increased PaO2 . Increased O2 extraction in tissues during
exercise decreased mixed venous PO2 but this was not statistically significant. At rest, hypoxia caused
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variance (ANOVA) was used to statistically test changes in the dependent variables from rest, to exercise,
JAP 1108-2001.R2
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hyperventilation, as indicated by decreased PaCO2 (p=0.08). Exercise in hypoxia further increased
hyperventilation (i.e. decreased PaCO2 ) but, arterial and venous pH were not increased in hypoxic
exercise, suggesting a metabolic acidosis during hypoxia. Hematocrit decreased with successive blood
sampling during the protocol, but these changes were not significant.
Ventilation-perfusion data. Table 3 gives the average blood-gas partition coefficients for the six
. .
inert gases used to measure ventilation-perfusion (V/Q ) distributions; they are similar to those in other
. .
species. Indices of V/Q distributions determined from the MIGET are given in Table 4. The goodness of
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fit of measured retention and excretion data to those predicted for the V/Q distributions can be judged by
only 20% of the time if the appropriate model of gas exchange is used (e.g. cross-current model in a bird
and alveolar model in a mammal, cf. (19). The RSS decreases if fewer gases are used in the analysis.
Using only 5 gases to analyze the emu data (see Methods), RSS was >5 in 74% of the cases with an
alveolar model. However, RSS with a cross-current model was <2 in 100% of the data sets. Therefore,
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inert gas elimination in the emu behaves according to a cross-current, but not an alveolar model and V/Q
distributions were determined from the MIGET data using a cross-current model.
. .
Figure 1 shows representative V/Q distributions for an emu under the four conditions studied.
.
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The distributions are centered near the overall VP / Q (Table 4) and the mean of the distributions shifts to
. .
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a higher V/Q value during exercise (p<0.05) and hypoxia (p = 0.07). V/Q heterogeneity, as measured by
.
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the log-standard deviation of the Q distributions (logSDQ ) did not change with exercise or hypoxia and
shunt was less than 1% of cardiac output under all conditions (Table 4).
.
.
Parabronchial ventilation (VP ), analogous to alveolar ventilation (VA ) in mammals, can be
estimated from MIGET data as the difference between total measured ventilation and dead space
.
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ventilation predicted from the calculated V/Q distribution. In this case, VP equals the difference between
. .
. .
the total bias flow and the highest V/Q compartment we were able to distinguish, i.e. V/Q > 10 (see
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Methods). VP calculated in this way is consistent with the changes observed in PaCO2 and VCO2 (Tables 1
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and 2). In normoxia, VP increased from 2.9 ± 0.2 L/min at rest to 20.4 ± 1.7 L/min during exercise. In
.
hypoxia, VP increased to 4.0 ± 0.7 L/min at rest and was 19.8 ± 2.0 L/min in exercise. The similar levels
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the residual sum of squares (RSS). When six gases are used in the MIGET, RSS is expected to be >5
JAP 1108-2001.R2
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of VP in exercise during normoxia and hypoxia result in a decreased PaCO2 during hypoxic exercise
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because the emus were not running as fast and VCO2 was lower (see above).
. .
Changes in the overall effective parabronchial ventilation-perfusion ratio (VP/Q , Table 4)
.
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paralleled the changes in VP . In normoxia, VP/Q increased from 0.48 ± 0.04 at rest to 1.66 ± 0.16 in
. .
exercise, and in hypoxia VP/Q increased from 0.56 ± 0.04 to 1.39 ± 0.02 in exercise. There was a
significant effect of exercise and an interaction between exercise and hypoxia, but the effect of hypoxia
alone was not significant.
Figure 2 shows average retention-excretion differences (R-E) for gases with different partition
the MIGET analysis (including instrument and physiological dead space) so the R-E* values plotted
correspond to the difference between arterial and end-parabronchial tensions. R-E* provides an index of
. .
the effects of V/Q heterogeneity on gas exchange, similar to the effects of heterogeneity on the alveolararterial PO2 difference in mammals. In mammals, minimum (or ideal) value for R-E*, or the alveolararterial PO2 difference, is 0. However, R-E* can assume negative values and end-expired PO2 can exceed
arterial PO2 in birds because of cross-current gas exchange.
. .
In normoxia, exercise reduces the effects of V/Q heterogeneity on gas exchange, as evidenced by
R-E* becoming more negative for the measured data points (Fig 2. A and B, solid dots) and the values
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predicted for the best-fit V/Q distributions (Fig. 2 A and B, dashed curves). Ideal R-E* values predicted
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for a homogeneous cross-current lung with the overall measured VP/Q ratio (Fig. 3 solid curves) are less
than measured heterogeneous values for most gases. Hence, the decrease in total area between the ideal
and measured R-E* curves with exercise in normoxia (Fig. 2A vs. B) means that gas exchange
performance is improved by exercise in normoxia. The effects of exercise during hypoxia (Fig. 2 panel C
vs. D) are smaller than the effects of exercise in normoxia. This is mainly because hypoxia at rest
improves gas exchange performance (Fig. 2A vs. C), while the effects of heterogeneity during exercise
are similar during normoxia and hypoxia (Fig. 2 B vs. D).
Discussion
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coefficients under the four test conditions. Excretion values are corrected for deadspace determined by
JAP 1108-2001.R2
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During exercise, many mammals, including humans, experience reduced efficiency of pulmonary
oxygen transport, as evidenced by an increase in the alveolar arterial difference (AaDO2) for oxygen,
and in some, a reduction in PaO2 (3). The mechanism of the increased AaDO2 is related to both
ventilation-perfusion inequality and pulmonary diffusion limitation of oxygen transport. There are clearcut species differences in the relative contribution of these two factors. For example, the horse
experiences very little increase in ventilation perfusion inequality but the extent of pulmonary diffusion
limitation for oxygen combined with mechanical constraint of ventilation is sufficient to cause marked
arterial hypoxemia (24). Pigs on the other hand, experience an increase in ventilation-perfusion inequality
inequality and pulmonary diffusion limitation although the relative contributions of each to the AaDO2
varies between individuals and with aerobic capacity (11). In many species, both pulmonary diffusion
limitation for oxygen and increased ventilation-perfusion inequality are worsened by hypoxia and hypoxic
exercise (10).
In contrast, ventilation-perfusion heterogeneity in emus did not increase with exercise, or hypoxia.
. .
Table 5 summarizes available data on V/Q distribution in birds, reptiles and mammals including humans.
. .
During normoxic exercise, as previously discussed, many mammals demonstrate an increase in V/Q
.
heterogeneity with exercise, evidenced by an increase in the logSDQ . The mechanism of the increased
. .
V/Q heterogeneity during exercise is unknown, but does not appear to be related to the structure of the
mammalian lung per se since it is observed to only a minimal extent in the horse, and is present to a
similar degree in humans and reptiles.
Various mechanisms of the increase in ventilation-perfusion inequality have been proposed
including: (1) a reduced common deadspace-to-tidal volume ratio and therefore reduced admixture of the
. .
expired air, unmasking existing V/Q heterogeneity present at rest (27), (2) non-uniform pulmonary
vasoconstriction and increased pulmonary artery pressure (4), (3) interstitial edema (22,23) or (4)
ventilatory time constant inequality (27). None of these mechanisms have been investigated in exercising
birds, however the rather non-elastic structure of the avian lung may reduce the importance of those
mechanisms relying on pressure changes in the pulmonary tissue/microenvironment. In addition changes
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with exercise, but no appreciable diffusion limitation (12). Humans experience both ventilation-perfusion
JAP 1108-2001.R2
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in the admixture of expired air as suggested above may be less important in birds since the deadspacetidal volume ratio is relatively high in birds. The fact that race horses show minimal increases in
ventilation-perfusion heterogeneity with hypoxic exercise demonstrates that not all alveolar lungs are
equally susceptible to such limitations. Hence, it remains to be determined if all avian lungs are as
immune to such limitations as the emus we studied, to provide evidence for interstitial pulmonary edema
as a possible mechanism. It should be noted that the levels of exercise sustained by the animals in this
study is less than animals in the wild. Thus caution should be used when interpreting these results.
Inert gas exchange in normoxic and hypoxic exercise. In emus, we found smooth unimodal
(normoxic, not exercising) geese (20). The reasons for the differences between these two species of birds
are unknown, but may reflect differences between awake and anesthetized birds or species differences.
. .
Also, we had limited ability to detect a high V/Q mode as described for anesthetized geese because we
only used five gases in our analysis, with ether being the most soluble. As discussed in the Methods, this
. .
limits our ability to distinguish differences between V/Q ratios > 10. Intrapulmonary shunting was
minimal under all conditions as reported for geese (20)
. .
The amount of V/Q heterogeneity measured in our emus under all conditions was similar to that
.
measured for just the main mode in anesthetized geese, which had a logSDQ = 0.56 (20). However,
.
despite a constant logSDQ in all of the measurement conditions, the mean blood flow was directed to units
. .
with higher V/Q ratio during exercise in both normoxia (0.32±0.04 vs. 1.21±0.0) and hypoxia (0.35±0.06
vs. 0.98±0.06). This is because ventilation increases to a greater extent than the corresponding increases
. .
in perfusion, so the overall V/Q ratio is increased.
The effect of ventilation-perfusion heterogeneity on a gas depends on the gas solubility and can
. .
.
vary with a change in the overall VP/Q despite a constant logSDQ (28). For example, exercise in
normoxia increases the efficiency of exchange for a gas with partition coefficient =1 because R-E*
decreases is more negative, Fig. 2A vs 3II). This approach permits insights into efficiency of CO2 and O2
gas exchange but only if the dissociation curves are linear. This is approximated for CO2 and O2 in
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distributions of ventilation and perfusion and no significant change in the amount of heterogeneity under
. .
different conditions. In contrast, a bimodal V/Q distribution has been described for anesthetized
JAP 1108-2001.R2
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hypoxia, but not for O2 in normoxia. Using partition coefficients of 0.6 and 6.0 for O2 and CO2
respectively (28), Fig 2, predicts no significant change in effects of ventilation-perfusion on O2 with
exercise in hypoxia and a small decrease in the effects on CO2 . This is consistent with no change in PaO2
and a small decrease in PaCO2 in exercise versus rest in hypoxia (Table 2).
Limitations of the study. During normoxia, the emus ran between 1.4 and 2.0 m/sec. This speed
is lower than the maximal speeds reported for emus running in the wild (14 m/sec. ref. 15) or achieved by
emus in other studies (21). There was a small decrement in running speed due to surgery and anesthesia
but it cannot account for all of the differences seen between our animals and those in the wild. Running
suggest that our captive bred birds were simply not trained well enough to run faster. Before starting these
experiments, we were advised by other investigators that emus were difficult to handle and that they
would only run on a treadmill reliably when running in a flock. This was impossible on our small
treadmill. Also, one of us had prior experience with emus suggesting they would be difficult to train. On
the other hand, data had been obtained from this species during treadmill exercise, albeit with difficulty
(8). We decided the preparation was worth pursuing when we had success in running young emus on our
treadmill. However, as they grew and became large enough to study, they became difficult to handle,
difficult to keep on the treadmill even during rest, and we were not able to make them run faster. Our
emus may have had reduced aerobic capacity from their captive life style also. Our emus showed a
respiratory exchange ration R of 0.93 during normoxic exercise and 0.96 during hypoxic exercise. It has
been our experience in exercising a variety of animals that it is difficult to exercise animals at an intensity
resulting in R > 1.
Conclusion: In emus, hypoxia and running exercise increased the overall ventilation-perfusion
ratio of the lung, while ventilation-perfusion heterogeneity remained unchanged. This behavior may
provide an advantage for birds exercising in hypoxia compared to mammals. Increased metabolic needs
with exercise were met by increased cardiac output and ventilation, resulting in significantly decreased
PaCO2 in normoxia as well as in hypoxia. The combined effect of the increased overall ventilation-
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speed in two birds decreased from 1.81 to 1.67 m/sec and from1.94 to 1.67 m/sec after surgery. We
JAP 1108-2001.R2
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perfusion ratio and no increase in heterogeneity resulted in improved CO2 exchange in hypoxia and
exercise, while O2 exchange was not affected by exercise in normoxia or hypoxia.
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JAP 1108-2001.R2
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Acknowledgements: The authors thank Donna Allsopp, Nathalie Garcia, Lennard Gonzales and
Andrew Altman for their skillful assistance with the bird training and handling; and Mark Olfert, Nick
Busan, Jeff Struthers and Eric Falor for technical support. Supported by DFG, NIH HL17731, NIH MO1
RR00827 and the University of California White Mountain Research Station.
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14. Kiley, JP, Faraci, FM, and Fedde, MR. Gas exchange during exercise in hypoxic ducks. Respir
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15. Patak, A.E. and Baldwin, J. Pelvic limb musculature in the Emu Dromaius novaehollandiae (Aves:
Sturthioniformes: Dromaiidae): Adaptations to high-speed running. J. Morphol. 238: 23-27, 1998.
16. Powell, FL. Birds at altitude. Respiration in Health and Disease, Stuttgart/New York: G. Fisher,
1993, p. 352-358.
17. Powell, FL. Respiration. Sturkie's Avian Physiology, San Diego: Academic Press, 2000, p. 233-264.
18. Powell, FL and Gray, AT. Ventilation-perfusion relationships in alligators. Respir Physiol 78: 83-94,
1989.
19. Powell, FL and Wagner, PD. Measurement of continuous distributions of ventilation-perfusion in
non-alveolar lungs. Respir Physiol 48: 219-232, 1982a.
20. Powell, FL and Wagner, PD. Ventilation-perfusion inequality in avian lungs. Respir Physiol 48: 233241, 1982b.
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13. Hopkins, SR, Wang, T, and Hicks, JW. The effect of altering pulmonary blood flow on pulmonary
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21. Roberts, TJ, Kram, R, Weyand, PG, and Taylor, CR. Energetics of bipedal running. J exp Biol 201:
2745-2751, 1998.
22. Schaffartzik, W, Arcos, JP, Tsukimoto, K, Mathieu-Costello, O, and Wagner, PD. Pulmonary
interstitial edema in the pig after heavy exercise. J Appl Physiol 75: 2535-2540, 1993.
23. Schaffartzik, W, Poole, DC, Derion, T, Tsukimoto, K, Hogan, MC, Arcos, JP, Bebout, DE, and
Wagner, PD. VA/Q distributions during heavy exercise and recovery in humans: implications for
pulmonary edema. J Appl Physiol 72: 1657-1667, 1992.
24. Seaman, J, Erickson, BK, Kubo, K, Hiraga, A, Kai, M, Yamaya, Y, and Wagner, PD. Exercise
1995.
25. Shams, H and Scheid, P. Efficiency of parabronchial gas exchange in deep hypoxia: measurements in
the resting duck. Respir Physiol 77: 135-146, 1989.
26. Swan, LW. Goose of the Himalayas. Natural History 79: 68-75, 1970.
27. Tsukimoto, K, Arcos, JP, Schaffartzik, W, Wagner, PD, and West, JB. Effect of common dead space
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28. Wagner, PD. Susceptibility of different gases to ventilation-perfusion inequality. J Appl Physiol 46:
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induced ventilation/perfusion inequality in the horse. Equine Veterinary Journal 27: 104-109,
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Figure legends
Fig. 1. Fractional ventilation (filled symbols) and blood flow (open symbols) versus ventilation-perfusion
ratio in a representative emu at (A) normoxic rest (B), normoxic exercise (C) and hypoxic rest and (D)
.
exercise. LogSDQ log standard deviation of the blood flow distribution.
Fig. 2. The retention-excretion (R-E*) difference, representing arterial-end parabronchial partial pressure
and best-fit predictions occur because of experimental error.
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of inert gases as a function of partition coefficient. R-E* for the fine measured inert gases are filled
. .
symbols, (±S.E.M.); dashed curve = R-E* predicted for V/Q distribution; solid curve = R-E* predicted
. .
for homogeneous lung with same overall VP/Q ratio. Small differences between the average data points
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Table 1. Effects of exercise and hypoxia on metabolic and cardiopulmonary variables in the emu.
1
Normoxic
Exercise
(n=6)
Hypoxic
Rest
(n=5)
Hypoxic
Exercise
(n=4)
0.2083±0.0003
0
4.4±0.3
3.5±0.3
0.78±0.02
2.9±0.2
19.87±0.03
5.8±0.6
98±5
0.2067±0.0010
1.67±0.09
18.2±1.2
17.1±1.4
0.93±0.04
20.4±1.7
26.48±1.62
12.7±0.2
167±7
0.1320±0.0026
0
5.5±1.2
4.2±0.8
0.79±0.03
4.0±0.7
19.79±1.47
8.2±0.4
112±9
0.1373±0.0021
1.04±0.07
17.2
16.1±4.7
0.96±0.08
19.8±2.0
24.78±1.65
15.5±1.4
177±16
P < 0.01 rest vs. exercise, 2P < 0.01 normoxia vs. hypoxia. (n = number of measurements)
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FIO2
Running
speed (m/sec)
.
1
V
. O2 (ml/(kg • min)) 1
VCO2 (ml/(kg • min))
R.
V.P (L/min)
.
V.P/VO2
Q (L/min)1,2
Heart rate (beats/min)1
Normoxic
Rest
(n=6)
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Table 2. Effects of exercise and hypoxia on blood gases and pH in the emu.
PIO2 (torr)
PaO2 (torr ) 2
Pv-O2 (torr ) 2
PaCO2 (torr ) 1
Pv-CO2 (torr ) 2
pHa
pHv–
Hematocrit (%)
Normoxic
Exercise
(n=6)
144.2±0.4
100.8±4.1
50.6±6.8
24.7±2.2
33.2±2.7
7.51±0.04
7.45±0.03
31.5±1.7
Hypoxic
Rest
(n=5)
90.5±1.1
58.5±4.7
43.0±1.8
25.7±2.4
30.8±1.2
7.49±0.04
7.45±0.03
29.7±1.3
Hypoxic
Exercise
(n=4)
96.2±1.5
61.9±3.8
32.2±0.2
22.8±1.3
28.4±0.7
7.51±0.04
7.44±0.05
27.7±1.9
P < 0.05 rest vs. exercise, 2P < 0.05 normoxia vs. hypoxia, 3P < 0.05 interaction between exercise and
hypoxia. (n = number of birds except n=2 for mixed-venous blood in hypoxic exercise)
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1
Normoxic
Rest
(n=6)
144.5±0.5
96.6±4.8
60.1±2.1
31.5±1.6
35.0±0.9
7.44±0.02
7.42±0.02
33.6±2.1
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Table 3. Blood gas partition coefficients of inert gases in emus (n=6).
Sulfur hexafluoride
Ethane
Cyclopropane
Enflurane
Diethyl ether
Acetone
0.00267±0.00021
0.064±0.004
0.34±0.02
1.18±0.11
11.1±0.4
295±22
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Table 4. Inert gas data at rest and during exercise in normoxia and hypoxia.
.
Q. distribution, mean
.
Q
distribution,
logSD
Q
.
V
. distribution, mean .
V. distribution
logSDV
. 1,3
VP/Q
.
Intrapulmonary shunt (%Q)
Normoxic
Rest
(n=6)
0.32±0.04
0.60±0.06
0.59±0.08
1.17±0.17
0.48±0.04
0.63±0.12
Normoxic
Exercise
(n=6)
1.21±0.03
0.68±0.06
1.98±0.18
0.93±0.26
1.66±0.16
0.52±0.16
Hypoxic
Rest
(n=5)
0.35±0.06
0.63±0.07
0.66±0.68
0.77±0.18
0.56±0.04
0.96±0.41
Hypoxic
Exercise
(n=4)
0.98±0.06
0.62±0.03
1.53±0.17
0.63±0.07
1.39±0.02
0.49±0.06
1
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P < 0.05 rest vs. exercise, 2P < 0.05 normoxia vs. hypoxia, 3P < 0.05 interaction between exercise and
hypoxia. (n = number of birds)
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.
Table 5. Ventilation-Perfusion heterogeneity (logSDQ) in mammals, reptiles and birds during exercise and
hypoxia. Means ± s.e.m.
Normoxic
exercise
Hypoxic
rest
Hypoxic
exercise
Mammals
Dog (a)
Horse 1a (b)
Pig 1a (c)
Human (d)
Aerobic Athletes 1a (e)
0.33±0.01
0.42±0.04
0.45±0.03
0.54±0.04
0.39±0.02
0.69±0.04
0.54±0.05
0.67±0.02
0.30±0.01
0.37±0.02
0.48±0.05
0.62±0.9
Reptiles
Alligator (f)
Turtle (g)
Savannah Monitor Lizard 1b (h)
Tegu Lizard (i)
0.47±0.06
0.79±0.19
0.39±0.06
0.94±0.59
0.63±0.07
0.62±0.03
0.78±0.05
Birds
Geese (j)
Emu, this study
1
0.56±0.30
0.60±0.06
0.68±0.06
P < 0.05 rest vs. exercise, 2P < 0.05 normoxia vs. hypoxia, 3P < 0.05 interaction between exercise and
hypoxia.
References
(a)
(27)
(b)
(24)
(c)
(12)
(d)
(5)
(e)
(11)
(f)
(18)
(g)
(13)
(h)
(10)
(i)
(9)
(j)
(20)
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Normoxic
rest
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Figure 1
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Figure 2
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