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O2
on blood flow dynamics at onset of forearm exercise
Department of Kinesiology, University of Waterloo, Waterloo, Ontario N2L 3G1; and Faculty of Kinesiology and Department of Physiology, University of Western Ontario, London, Ontario N6A 3K7, Canada
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Hughson, R. L., J. K. Shoemaker, M. E. Tschakovsky, and J. M. Kowalchuk. Dependence muscle of
O2
on blood flow dynamics at the onset of forearm exercise.
J. Appl. Physiol. 81(4):
1619-1626, 1996.
The hypothesis that the rate of increase in
muscle O2 uptake (O2 mus)
at the onset of exercise is influenced by muscle blood flow was tested
during forearm exercise with the arm either above or below heart level
to modify perfusion pressure. Ten young men exercised at a power of
~2.2 W, and five of these subjects also worked at 1.4 W. Blood flow
to the forearm was calculated from the product of blood velocity and
cross-sectional area obtained with Doppler techniques. Venous blood was
sampled from a deep forearm vein to determine
O2 extraction. The rate of
increase in
O2 mus
and blood flow was assessed from the mean response time (MRT), which is
the time to achieve ~63% increase from baseline to steady state. In
the arm below heart position during the 2.2-W exercise, blood flow and
O2 mus
both increased, with a MRT of ~30 s. With the arm above the heart at
this power, the MRTs for blood flow [79.8 ± 15.7 (SE)
s] and
O2 mus
(50.2 ± 4.0 s) were both significantly slower. Consistent with
these findings were the greater increases in venous plasma lactate
concentration over resting values in the above heart position (2.8 ± 0.4 mmol/l) than in the below heart position (0.9 ± 0.2 mmol/l). At the lower power, both blood flow and
O2 mus
also increased more rapidly with the arm below compared with above the
heart. These data support the hypothesis that changes in blood flow at
the onset of exercise have a direct effect on oxidative metabolism
through alterations in O2
transport.
oxygen uptake; handgrip exercise; Doppler velocimetry; echo
Doppler; human
INTRODUCTION IT HAS OFTEN BEEN CLAIMED for the onset of submaximal
exercise by human subjects that the supply of
O2 is adequate and that oxidative
phosphorylation is limited by the concentration of other regulators
such as phosphocreatine (PCr) or ADP concentration (5, 6, 14, 39).
Evidence from nuclear magnetic resonance spectroscopy has shown a time
course of change in intramuscular metabolism during dynamic calf muscle
contractions that is similar to that observed for
O2 uptake
( The rationale for suggesting that
O2 is available in excess of
metabolic demand at the onset of submaximal exercise by humans has
focused largely on the apparent rapidity of
O2 transport responses. Cardiac
output increases more rapidly than does
Information is available on the general pattern of
O2 extraction from the blood in
transitions from rest to exercise in the forearm (10) and leg (4, 29).
Only very recently (12) has the response of blood flow been measured
simultaneously with muscle metabolism at the onset of exercise. This
recent study was restricted to a single intensity of cycling exercise.
It was the purpose of our research to examine calculated muscle
METHODS A total of 10 healthy male subjects volunteered to take part in this
study after receiving full written and verbal details of the
experimental procedures and signing a consent form approved by the
Office of Human Research of the University of Waterloo, Waterloo,
Canada. The average physical characteristics were age 27.0 ± 2.5 (SE) yr, height 178 ± 2 cm, and weight 76.7 ± 2.0 kg. Their maximal voluntary isometric contraction strength was 50.4 ± 2.0 kg during handgrip exercise.
O2) during cycling exercise (5), but this is rather indirect evidence. At the onset of electrically
stimulated exercise in the dog gracilis muscle, it was shown that there
is a rapid increase in muscle blood flow and capillary recruitment
(16). Connett et al. (7) suggested that there is adequate intracellular
oxygenation throughout the transition period with increased metabolic
demand. On the contrary, in studies of isolated in situ dog
gastrocnemius muscle, it appears that
O2 plays an important role in
regulating tissue respiration (3, 15). Similarly, for exercising
humans, there have been numerous reports of altered
O2 availability to working muscles causing an alteration in O2.
For example, hypoxia (23, 26), 
-blockers (17), and supine exercise
(18) all slow the rate of O2
increase at the onset of exercise. Application of lower body negative
pressure (thereby increasing the heart-to-legs perfusion gradient)
during supine exercise (18) and as few as 4 days of cycle ergometer
training (27) have caused accelerated
O2 kinetics.
O2 at the onset of exercise
(9, 39), and there have been several reports of very rapid increases in
muscle blood flow (11, 37).
O2 (O2 mus)
and to determine the effects of altered blood flow dynamics on this
response during a transition from rest to moderate forearm exercise.
Exercise was conducted with the subjects in a supine position with the
arm raised or lowered relative to the position of the heart to achieve
different perfusion pressures. It was hypothesized that when rhythmic
handgrip exercise was initiated with the arm below the heart, the
increase in both muscle blood flow and
O2 would be faster than the
corresponding responses with the arm above the heart. That is, there is
a dependence of O2 mus
at the onset of exercise on the dynamics of
O2 delivery.
r2,
where r is the vessel radius.
Blood sampling.
A three-way stopcock was fixed to the catheter. During the second trial
of each experimental condition, 1-ml samples were collected in
heparinized syringes at 0 and 1 min of rest, then at the same times as
given above for diameter measurements. These samples were immediately
but gently agitated and stored in an ice bath. Within 1 h of
collection, all whole blood samples were analyzed for
PO2,
PCO2, hematocrit, and the plasma
concentration of lactate by selective electrodes in a blood gas-electrolyte analyzer (Nova StatProfile 9 Plus, Nova Biomedical Canada, Mississauga, ON). The analyzer was calibrated at regular intervals during the analyses. Hemoglobin concentration was calculated from the measured hematocrit by assuming a normal mean corpuscular hemoglobin of 33% of the total cell volume.
O2 saturation and content were
obtained from the output of the analysis system after application of
standard equations.
Calculated
O2 mus.
To calculate
O2 mus,
it is necessary to have a quantitative estimate of blood flow and an
estimate of O2 extraction. That is,
O2 mus
was obtained from the Fick equation as the product of FBF and
arteriovenous O2 content
difference
(a-vDO2).
Blood samples were obtained at specified times, so it was necessary to
obtain estimates of blood flow at these same times. To accomplish this,
the best fits to each of the MBV and arterial diameter measurements were obtained by a nonlinear least squares curve-fitting procedure by
using a one- or two-component exponential model, as previously described (33). Selection of the one- or two-component model was based
solely on best fit criteria. This approach produced the best estimate
of the true physiological response after recognition that some of the
between-sample point variability was probably due to random variation
caused by probe movement and muscle contraction. Values were then
calculated for blood flow at the time points corresponding to the times
of the blood samples.
The estimate of O2 extraction was
obtained by first assuming a constant arterial
O2 content (97% saturation is
commonly measured by oximetry in our laboratory), then subtracting the
measured venous O2 content to
yield
a-vDO2. It
is reasonable to assume constant arterial
O2 content under these test
conditions because the intensity of the forearm exercise placed a very
small demand on the cardiovascular system.
The time course of the calculated
O2 mus
was evaluated by the same one- or two-component exponential
curve-fitting procedure described above, and the mean response times
(MRT; time to 63% of the increase from rest to steady-state exercise)
were compared. We have elected to use either one- or two-component
models to fit the data because we were interested in obtaining the best least squares fit of the data without constraining the fit to a
preconceived model. Also, the wide range of time constants that we
observed precluded arbitrarily using a single-exponential model. MRT
has been used for many years in this area of research (22) to yield an
indicator of the overall dynamic response characteristics.
Statistical analysis.
The effect of arm position on the steady-state values, on changes from
baseline, and on the kinetics of the blood flow and O2 mus
responses were analyzed by a repeated-measures one-way analysis of
variance for each contraction rate protocol. Additional analyses were
completed with a two-way repeated-measures analysis of variance to
determine effects of arm position and time. The level of significance
for main effects and interactions was set at
P < 0.05 and significant differences
were further analyzed with Student-Newman-Keuls post hoc test. Linear
regression of the relationship between MRT for
O2 mus
and FBF was obtained by the nonparametric reduced major axis approach
as described by Anderson et al. (2). In this approach, the presence of
error in both the x- and
y-axes is acknowledged, and the slope
of the regression is obtained from
Sy /Sx,
where Sy is the standard
deviation of y-axis data and
Sx is the standard
deviation of x-axis data. All data are
presented as means ± SE.
RESULTS
O2 mus
did not differ between arm positions (Table
1). Immediately at the start of exercise,
there was a rapid increase in FBF for both the Above and Below arm
positions (Fig. 1). However, the rate of
increase was markedly more rapid in the Below compared with the Above
arm position as seen in the pattern of the response and a significant position by time interaction effect (P < 0.005, Fig. 1) and the considerably faster MRT (Table 1,
P < 0.05). The absolute increase in
FBF was not different between arm positions, nor were the final blood
flow values different.
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O2 mus;
top), forearm blood flow (FBF; middle), and
arteriovenous O2 content difference
(a-vDO2; bottom) are shown
for exercise conducted above (50° above horizontal body position;
) and below (50° below horizontal body position; 
) heart.
Values are means ± SE for 10 subjects during 2.2-W (higher power
output) forearm exercise. See RESULTS for statistical
analysis.
Over the first minute of exercise, there were no differences in estimated a-vDO2 between exercise positions Above or Below the heart (Fig. 1). Beyond 1 min, there was a systematically greater O2 extraction when the arm was Above compared with Below heart level, as indicated by a significant position by time interaction effect (Fig. 1, Table 1, P < 0.005). Calculated
O2 mus
increased more rapidly when the arm was Below the heart (MRT = 29.2 ± 2.0 s) than when it was Above (50.2 ± 4.0 s) (Table 1,
P < 0.05). There was a significant
position by time interaction effect (P < 0.0001) because the
O2 mus
was lower in the Above test early in exercise, then rose to values higher than in the Below tests later in exercise (Fig. 1). The finding
that the increase above resting values in venous plasma lactate
concentration at the end of 5 min of forearm exercise was 2.8 ± 0.4 and 0.9 ± 0.2 mmol/l for Above compared with Below exercise,
respectively (P < 0.05) is
consistent with the slower increase in
O2 in the Above heart
position.
Lower power output test.
In the subset of five subjects who also performed the lower power test,
there were no differences in resting values between the arm positions
(Table 1). There was, as in the higher power output exercise, a smaller
a-vDO2
during exercise with the arm Below compared with Above the heart (Table
1, P < 0.05). Likewise, the rate of
increase in each of the FBF and
O2 mus
values was faster for the Below position than the Above heart position
(Table 1, P < 0.05). The
changes in plasma lactate concentration were not significantly
different between arm positions, but the overall mean values for the
Below position (0.4 ± 0.1 mmol/l) and the Above position (1.2 ± 0.4 mmol/l) were consistent with the patterns of change in the
O2 mus
responses.
Dependence of
O2 mus
on FBF.
For 28 out of the 30 paired observations between the time course (MRT)
of increase in
O2 mus
and FBF at the onset of exercise, there was a tight relationship with
little variation from the line of identity (Fig.
2). Two subjects during the higher power output tests in the Above heart position had quite slow FBF responses with more typical
O2 mus
responses. Excluding these two individual data points, the overall
regression equation describing the lower and higher power output tests
in both Above and Below heart exercise was MRT 
O2 mus = 0.63 · MRT FBF + 12.3, r = 0.84. Presented on Fig. 2 are the regressions for each
of the low and high exercise intensities. Both Table 1 and Fig. 2 show
that in higher and lower power output exercise, the responses for
O2 mus
and FBF were faster in the Below than in the Above heart position. It is also clear that the responses were faster during exercise with the
lower metabolic demand.
O2 mus
is shown as a function of MRT for FBF for all test conditions. Regression equation for lower exercise intensity (Low WR) was MRT O2 mus = 1.03 · MRT FBF + 4.8, r = 0.70. For higher exercise
intensity (High WR), 2 rightmost
points were omitted from regression. Equation describing remaining data
was MRT O2 mus = 0.64 · MRT FBF + 10.5, r = 0.85. For Low WR,
n = 5, and for High WR,
n = 10, for each of Above and Below
tests.
DISCUSSION
This study has established that there is a strong dependency of
O2 mus
on the supply of O2, as dictated
in large part by the blood flow response, during the adaptive phase of
forearm exercise. The rate of increase, as measured by the MRT, for
O2 mus was in the range of values reported previously for both
arm and leg exercise using several different approaches (5, 12, 18, 19,
22). The slower kinetics in the tests with the arm Above compared with
Below the heart are consistent with observations of slower
O2 kinetics during supine
position arm cycling when the arms were above the body (19) and with
supine leg cycling where the kinetics of
O2 were ~15-20%
slower than those observed in the upright position (18).
The direct estimation of
O2 mus
yielded estimates of the time course of adaptation that were similar to
recent studies employing magnetic resonance spectroscopy (5, 24, 25,
38). In these latter studies, the time course for
O2 mus
has been inferred from measurements of the change in muscle PCr
concentrations at the onset of forearm (24, 25) and leg muscle (5, 38) exercise. In contrast with these latter studies in which the position of the forearm or the leg within the magnetic device is
dictated by the horizontal position of the large magnets, we were able to show that there is a sensitive dependence of forearm
O2
and O2 mus
on arm position Above or Below the heart. These data support the
hypothesis of this study that the kinetics of
O2 mus would be influenced by the kinetics of FBF.
O2 mus
was obtained from the Fick equation as the product of blood flow and
a-vDO2. For
this latter variable, it was necessary to sample blood from a forearm
vein and to assume the arterial content. Given the very light demand placed on the cardiorespiratory system by forearm exercise, it is
unlikely that the arterial O2
content would have been affected by the exercise. We assumed an
arterial O2 saturation of 97%
because we have measured this repeatedly by ear oximetry. Inclusion of directly measured saturation probably would not have provided any
additional precision to our estimates of
a-vDO2. The
greatest point of uncertainty in this experimental design was
measurement of venous blood O2
content (8). Although efforts were made to trace the path of the vein
back toward the belly of the forearm muscle, it is not known to what
extent surface veins might have contributed to changes in venous
O2 content, nor is it known
whether the vein was draining a representative region of the forearm
muscle. However, one can see a pattern of change that is consistent
with exercise-induced extraction of
O2, and these patterns were
consistent between Above and Below heart exercise.
Steady-state measurements.
Resting blood flow of 58-68 ml/min is equivalent to ~4-5
ml · 100 ml
tissue
1 · min1
when corrected for the forearm volume in these subjects. This is
similar to flow measurements reported previously with strain gauge and
other techniques (11, 35, 37). With an
a-vDO2 of
50-75 ml O2/l, the calculated
O2 mus
values were close to 4-5 ml/min. There were no differences in
steady-state measurements at rest between the arm Above compared with
Below positions.
The increase in
O2 mus
was five- to sevenfold during exercise. This was achieved in part by
almost doubling
a-vDO2 to
as much as 130 ml O2/l. The
a-vDO2 was
greatest in the Above position, with both the higher and lower power
output exercises having similar O2
extractions. These values are very similar to those observed by Ahlborg
and Jensen-Urstad (1) during arm-cycling exercise at powers up to 90 W. The smaller
a-vDO2
observed during forearm exercise with the arm below the heart probably
reflects the relative hyperperfusion in this position, whereas the
value of 130 ml O2/l might
indicate the greatest extraction possible during arm exercise. Support
for this hypothesis comes from the pattern of
a-vDO2
observed over the first minutes of exercise, when it appears that
inadequate flow in the Above position was not compensated for by
increased extraction such that
O2 mus
in this transient phase was reduced in the Above position compared with
Below.
In the Above heart tests, the
O2 mus
was greater at the end of exercise than that observed in the Below
tests. The cause of this is not known. It is unlikely that the power
was different because the same apparatus was used in each position. It
has been well established that, for strenuous cycling exercise (28) and repeated isometric contractions (36), the
O2 continues to increase to
levels beyond those predicted based on the metabolic cost of lower
submaximal powers. The origin of this extra
O2 is in the muscle (28), but
the specific mechanism has not been established. If the extra
O2 that we measured is
established to be the same phenomenon, the forearm exercise model might
make further research of this problem easier because it eliminates the
need for a femoral venous catheter.
Transient changes in blood flow and
O2 mus.
The changes in FBF and
O2 mus
were both well approximated by an exponential response at the onset of
exercise (see Fig. 1). This is consistent with the pattern of change
observed during whole body exercise and with small muscle mass exercise
studied by magnetic resonance spectroscopy.
Using Doppler methodology, Eriksen et al. (11) reported that blood flow
to the quadriceps muscle at the onset of supine rhythmic leg
contractions reached 80% or more of the end-exercise values within
10-15 s. This is considerably faster than our results and the
findings in previous studies of leg exercise (12, 33, 34). It appears
from the figures in the study of Leyk et al. (21) that blood flow was
still increasing at 40 s of rhythmic leg exercise. The faster
adaptation of flow in the study of Eriksen et al. (11) could be a
function of the relatively small leg movement and metabolic demand in
their exercise model.
While this paper was under review, Grassi et al. (12) reported on the
O2 mus
response at the onset of upright leg cycling at a power output 50 W
below measured ventilatory threshold. There are both notable
similarities and differences in our results. First, they found as we
did (see Fig. 2) that the time to achieve 63% of the new steady state
for blood flow [33.7 ± 9.2 (SD) s] was very similar to
the time required to reach 63% for
O2 mus (35.6 ± 8.4 s). Their 63% time was equivalent to our MRT because they added the time delay to the time constant of their monoexponential fit. Whereas the results of Grassi et al. (12) came from a single work
rate that they constrained to be below the ventilatory threshold, we
explored the responses to a range of relative exercise intensities. The
group mean values during our higher power output in the Below condition
were very similar to their group mean values just indicated. In
contrast, at the lower power output in the Below condition of our
study, the MRT for blood flow [19.3 ± 1.6 (SE) s] and
for O2 mus
(24.4 ± 2.1 s) appeared to be faster. Because both upright leg
cycling and our Below condition have the benefit of gravitational assist for muscle perfusion pressure, it is not clear why the arm
exercise had a faster response.
One notable difference between our study and that of Grassi et al. (12)
was the method and site of blood flow measurement. In applying Doppler
measurements to the arterial inflow, we have an estimate of the
delivery of O2 to the working
muscles. The femoral vein thermodilution method has normally been
applied in steady-state measurements, but Grassi et al. adapted it for
the non-steady state. One of the major limitations of this method might
be the uncertain contribution of pooled venous blood. Although one
might expect that most of this influence will occur over the first few
contractions at the higher work rate, this is not known. Cycling
exercise is performed largely by the quadriceps muscle group, but there
is a contribution, especially in trained cyclists as studied by Grassi
et al. (12), from lower leg muscles (13). Maybe the spatially separated
contributors to muscular contraction have influenced the apparent time
course of measured muscle blood flow and
O2 mus.
In any event, these two studies represent the first attempts to provide
information on the time course of the adaptive processes that are so
critical in establishing the metabolic steady state. Both studies
suggest a strong relationship between O2 supply and
O2 utilization during the major
adaptive phase.
Blood flow distribution at the onset of exercise must be dependent on a
perfusion pressure gradient and changes in vascular conductance. With
activation of the muscle pump immediately with the first
contraction/relaxation, blood flow increases rapidly (more than double
by 10 s of exercise, see Fig. 1). However, the within-muscle pattern of
distribution is not known. If the muscle pump increases flow primarily
by increasing the pressure gradient across the capillary bed in the
first seconds of exercise (32), then distribution will not be related
to the metabolic demand of individual muscle fibers. Alternatively,
metabolically induced dilation might begin with the first contraction
(8) and adjust blood flow more appropriately for the demand (31). Given
the immediate and progressive increase in
a-vDO2,
it appears that distribution was reasonably well matched to metabolic
demand. A brief consideration of the consequences of increased flow to nonexercising tissues will show that our estimates of
O2 mus might have underestimated the time course of change. Increased blood
flow through tissues that have not increased their metabolic rate would
cause an increase in venous O2
content. This would diminish the
a-vDO2
relative to the regions in which metabolic rate did increase and result
in an apparently slower response time for the overall muscle. That is,
if anything, our MRT for blood flow and
O2 mus
might be even closer than we calculated. The converse, a reduction in
blood flow to nonexercising regions within the muscle, is unlikely
because of the muscle pump effect (32) and the slow activation of
sympathetic vasoconstrictor tone. Seals et al. (30) observed almost no
change in muscle sympathetic nerve activity after 2.5 min of static
handgrip at 15% maximal voluntary contraction. Little change in
sympathetic nerve activity would be expected in the present
experiments, which required intermittent contractions for 5 min at
~10% maximal voluntary contraction.
The observation that maximum
a-vDO2
during the heavier exercise was only ~130 ml/l might reflect
inappropriate distribution with exercise, differences in
capillary-to-fiber ratios in comparison with leg muscles, a diffusion
limitation, or mixing with flow from inactive regions including the
skin. The observation of two individuals who had very slow blood flow
responses and somewhat faster
O2 mus
can be attributed to availability of different mechanisms to achieve
the same objective. They had relatively greater
a-vDO2
values early in exercise and then extracted less O2 as the blood flow increased.
Biochemical consequences.
The metabolic state in the muscle at the onset of exercise has been
investigated in several studies of exercising human muscle. Metabolic
rate can be estimated from muscle PCr breakdown by magnetic resonance
spectroscopy (5, 24, 25, 38). Recently, McCann et al. (25) observed a
time constant for PCr depletion at the onset of 1.7-W exercise to be 33 ± 7.7 (SD) s. This was similar to our observations of 29.2 s for
the 2.2-W power below the heart but somewhat slower than the 24.4 s at
1.4 W. McCann et al. (25) also observed that the time constant at a
higher power (3.6 W) was considerably slower at 53 s. The subjects in
that study were in a supine position, presumably with the arm
horizontal, so that muscle perfusion pressure would have been less than
during the arm Below heart position in the present study. This could
have accounted for slightly slower kinetics than we observed.
Alternatively, between-subject differences might have contributed
because the power in both studies was set at an absolute level without
regard to muscle mass. Furthermore, fitness might influence the
metabolic adaptation to exercise (27). The similarity of the two
estimates of oxidative metabolism by very different techniques suggests that each is capable of following the dynamic responses of metabolism at the onset of exercise.
It has been well established that a direct linear relationship exists
between the amount of PCr breakdown and the magnitude of the
O2 deficit when subjects exercised
at constant submaximal power while breathing gases with varying
inspired PO2 (23) or across a range
of exercise intensities (20). Recently, studies of dog muscle
metabolism under various steady-state conditions indicated that in the
face of a reduced arterial PO2, the
same ATP production rate could be achieved with a reduction in the
"energetic state" (a function of the sum of free concentrations of PCr, ATP, and ADP) (3, 15). In contrast with earlier biochemical studies, this model proposed by Arthur et al. (3) does not require that
intracellular PO2 reach extremely low
values before metabolic control is altered. Rather, intracellular
PO2 values such as those measured in
the working dog muscle studies of Connett et al. (7) might be low
enough to cause compensatory changes in energetic state. Application of
this hypothesis to our observations could mean that a limitation in
O2 availability at the onset of
exercise might result in slower adaptation of O2 mus
and a greater O2 deficit. This
would, in turn, cause a lower intracellular concentration of PCr and a
greater reliance on anaerobic ATP turnover during the non-steady-state
transition.
Conclusion.
A significant positive correlation was found between the rate of
increase in forearm muscle blood flow and calculated
O2 mus across a range of values achieved with two different power outputs and
arm positions. These data obtained from exercise intensities that
caused either minimal or moderate elevations of venous blood lactate
support the hypothesis that
O2 mus
can be limited at the onset of exercise by the availability of
O2. If this is true, it raises a
number of questions regarding the mechanism by which the increase in
blood flow and the patterns of blood flow distribution are regulated in
the rest-to-exercise transition and about the potential limitations due
to O2 diffusion. Furthermore, it
suggests that in future investigations of metabolic control, for
example with magnetic resonance spectroscopy, the regulation of muscle blood flow and availability of O2
are important variables that must also be considered.
ACKNOWLEDGEMENTS
The authors thank Barry Scheuermann and David Northey for assistance with blood gas analysis.
FOOTNOTES
Address for reprint requests: R. L. Hughson, Dept. of Kinesiology, Univ. of Waterloo, Waterloo, Ontario N2L 3G1, Canada (E-mail: hughson{at}cgsa.uwaterloo.ca).
Received 24 January 1996; accepted in final form 21 May 1996.
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