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Noll Physiological Research Center, Pennsylvania State University, University Park, Pennsylvania 16802-6900
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Ho, C. W., J. L. Beard, P. A. Farrell, C. T. Minson, and W. L. Kenney. Age, fitness, and regional blood flow during exercise
in the heat. J. Appl. Physiol. 82(4):
1126-1135, 1997.
During dynamic exercise in warm environments,
the requisite increase in skin blood flow (SkBF) is supported by an
increase in cardiac output (
c) and decreases in
splanchnic (SBF) and renal blood flows (RBF). To examine interactions
between age and fitness in determining this integrated response, 24 men, i.e., 6 younger fit (YF), 6 younger sedentary (YS), 6 older fit (OF), and 6 older sedentary (OS) rested for 50 min, then
exercised at 35 and 60% maximal
O2 consumption
(
O2 max) at
36°C ambient temperature. YF had a significantly higher
c and SkBF than any other group during exercise,
but fitness level had no significant effect on any measured variable in
the older men. At 60%
O2 max, younger subjects had significantly greater decreases in SBF and RBF than the
older men, regardless of fitness level. Total flow redirected from
these two vascular beds (
SBF + RBF) followed YF >> YS > OF > OS. A rigorous 4-wk endurance training program
increased exercise SkBF in OS, but SBF and RBF were unchanged.
Under these conditions, older men distribute c
differently to regional circulations, i.e., smaller increases in SkBF
and smaller decreases in SBF and RBF. In younger subjects, the higher
SkBF associated with a higher fitness level is a function of both a
higher c and a greater redistribution of flow from
splanchnic and renal circulations, but the attenuated splanchnic and
renal vasoconstriction in older men does not appear to change with
enhanced aerobic fitness.
skin blood flow; splanchnic blood flow; renal blood flow; cardiac
output; hyperthermia; heat stress; aging; regional circulation
INTRODUCTION DYNAMIC EXERCISE in a warm environment creates a
competition between skin and active muscle for the available cardiac
output ( It is unclear at present how these two mechanisms that lead to
augmented skin blood flow (SkBF), i.e., increased One influence known to affect regional blood flow under hyperthermic
conditions is age. Older (e.g., >60-yr-old) men and women have a
diminished cutaneous vasodilatory response than younger subjects with a
similar Therefore, the present study expands on the previous age comparison
(16) by testing subjects who differed in both age and MATERIALS AND METHODS Preliminary Procedures
c). An integrated cardiovascular response is
necessary to perfuse these two low-resistance circulations while
maintaining blood pressure homeostasis. Accompanying the increasing
c, regional distribution of c is
altered such that sympathetically mediated renal and splanchnic (i.e.,
liver, gastrointestinal tract, pancreas, and spleen) vasoconstriction
decreases blood flow to these areas. In thermally stressful
environments, renal and splanchnic flows are further reduced, with this
additional fraction of the available c redirected to
the skin to facilitate heat dissipation (26).
c
and visceral vasoconstriction, are affected by individual subject
characteristics such as maximal O2
consumption (O2 max),
exercise training, and age. It has been suggested that there
is a close linear relationship between splanchnic and renal
vasoconstriction and the intensity of the exercise, expressed as a
percentage of an individual's O2 max, a relationship
that is unaffected by the state of physical conditioning of the subject
(5, 26, 28). However, this hypothesis, supported by data compiled
across several studies, requires further investigation.
O2 max,
resulting in a lower SkBF at a given core temperature (14,
16-18). However, until recently SkBF changes with aging have
rarely been examined in the context of concomitant changes in
c, splanchnic blood flow (SBF), and renal blood flow
(RBF). When groups of older (64 ± 2 yr) and younger (26 ± 2 yr)
men with a similar
O2 max exercised in a
warm environment, the older men responded with a significantly lower
SkBF and an attenuated decrease in SBF and RBF (16). Because that study was specifically designed to match subject groups for
O2 max, it compared a
relatively sedentary group of younger men with a well-trained group of
older men. The question of interactive effects of age and fitness in
determining regional distribution of c remains
unanswered.
O2 max. In addition to
this cross-sectional comparison, we aggressively trained a subset of
four sedentary older subjects to better elucidate effects of endurance
exercise training on the distribution of c to
cutaneous, splanchnic, and renal circulations when exercise is
performed in a warm environment.
O2) attained on the cycle
(O2 peak) was
~10-15% lower than that measured during the treadmill test
(O2 max).
Subjects
Mean subject characteristics are presented by group in Table 1. All subjects were nonsmokers, and during the experiment no subject was taking medication that had the potential to impact cardiovascular or thermoregulatory function. Classified byO2 max for their
respective age group, the younger fit (YF) men were in the 99th
percentile, younger sedentary (YS) in the 45th percentile, older fit
(OF) in the 90th percentile, and older sedentary (OS) in the 30th
percentile (1).
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Experimental Procedures
Subjects arrived at the laboratory at 0730, recorded an initial nude body weight (±10 g), then drank 5 ml/kg body weight of distilled water. Catheters were inserted into two veins at least 15 cm apart in the right arm, the proximal one for infusion and the distal one for venous sampling. After instrumentation (described below) was completed, subjects entered an environmentally controlled chamber, where they initially sat at rest for 50 min, then cycled for 20 min at 35%O2 max (~ 39% O2 peak),
followed by 30 min at 60%
O2 max (~ 65% O2 peak).
Pedaling rate (60 revolutions/min) was maintained by the subjects with
the assistance of a visual feedback display. Ambient temperature was
fixed at 36°C, relative humidity was 20%, and there was no forced
air movement. After the session, subjects were again weighed to
estimate sweat loss during the experiment. No additional fluids were
consumed during the trial.
Training Study
In addition to the cross-sectional group comparisons, a subset of 4 OS subjects underwent a rigorous 4-wk endurance training regimen, after which they were retested. Subjects trained individually on a cycle ergometer, 1 h/day, 5 days/wk in the laboratory (thermoneutral ambient temperature) under the direct supervision of one of the investigators (C. W. Ho). The training protocol was intermittent, consisting of alternating bouts of pedaling with no added resistance (3-4 min) and cycling at 80%O2 peak (6-8
min) for the full hour. All subjects completed 20 such training
sessions. Physiological characteristics of the four men before and
after the training program are presented in Table
2. After training, subjects were tested at
two exercise intensities, the same absolute intensity that represented
60% of pretraining
O2 peak and 60% of
their posttraining
O2 peak.
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Measurements
Esophageal temperature (Tes) was measured at the level of the right atrium from a copper-constantan thermocouple sealed in the lumen of a pediatric feeding tube. Mean skin temperature (Tsk) was recorded as the weighted average of four uncovered thermocouples placed on the right upper arm, chest, thigh, and calf. Heart rate (HR) was continuously monitored and recorded every 2 min from a 12-lead electrocardiograph.c was measured every 10 min by using a CO2-rebreathing technique
(equilibrium plateau method) (12). The coefficient of variation for
repeated samples was 3%. Systolic (SBP) and diastolic blood pressures
(DEP) were measured by brachial auscultation, and mean arterial
pressure (MAP) was calculated as (0.33 · SBP) + (0.67 · DBP).
Splanchnic and renal blood flows.
As previously described (16), the resting extraction ratio (ER) for
indocyanine green (ICG; Becton-Dickinson) was measured in each subject
before testing by an intravenous bolus injection technique based on a
two-compartment model (7). A bolus of 0.5 mg/kg ICG was injected, and
3-ml venous samples were collected in lithium heparin tubes every 3 min
for 30 min. A separate ER was calculated for each subject from the
plasma disappearance curve of ICG (spectrophotometry; absorbence of 805 nm) with slopes determined objectively by computer. Each individual
subject's ER was used in subsequent calculations of SBF. There were no
age differences in ER, which averaged 69 ± 3% for younger subjects and 73 ± 3% for the older group. In addition to ER, plasma volume (PV) was also calculated for each subject from the extrapolated zero-time plasma concentration of dye. When no significant change in ER
is assumed (see DISCUSSION), changes
in the clearance of ICG (CICG)
reliably represent changes in SBF. In this study, by 30 min of exercise
subjects were assumed to be at steady state, and exercise was assumed
not to alter the ICG ER (28, 29). Although some error is inherent in
the use of this indicator technique with respect to the measurement of
absolute organ flow, it has proven reliable in determining relative
changes in flow from baseline within an individual (9).
During the protocol, SBF and RBF were determined by using continuous
infusions of ICG and para-amino hippurate (PAH; Merck), respectively
(16). After a priming dose of 0.10 mg/kg ICG and 8.0 mg/kg PAH, a
solution comprising 0.5 mg/ml ICG and 12 mg/ml PAH was constantly
infused at a rate of 1 ml/min.
CICG was calculated from the ICG
concentration of the infusate (mg/ml), the infusion rate (mg/min), and
the measured plasma concentration of ICG (mg/ml) by using each
individual subject's previously calculated ER. SBF was calculated from
CICG and hematocrit (Hct) as
CICG/(1 
Hct). Similarly,
RBF was calculated from the clearance of PAH
(CPAH) and Hct as
CPAH/(1 Hct), assuming a
constant ER of 0.91 (3, 8).
Plasma norepinephrine.
Venous samples were collected into chilled tubes containing EGTA and
reduced glutathione for the determination of plasma norepinephrine concentration ([NE]). Samples were extraction from
acid-washed alumina into 200 mM perchlorate and analyzed by using
high-performance liquid chromatography (model 200, BioAnalytical
Systems). Electrochemical detection used detectors set at 2 and 5 nA
with the same applied potential of 750 mV. The coefficient of variation
for [NE] determination within a sample was 4%.
Forearm blood flow.
Forearm blood flow (FBF) was measured on the left forearm via venous
occlusion plethysmography by using a mercury-in-Silastic strain gauge.
The arm was supported above heart level to promote venous drainage
between measurements, and arterial blood flow to the hand was arrested
during the FBF measurements. Each FBF determination was composed of the
average slope of four or more separate curves, with a coefficient of
variation of 5.6%. Changes in FBF were assumed to reflect changes in
forearm SkBF because underlying inactive muscle blood flow does not
change under conditions of heating or dynamic leg exercise (6, 11).
Statistics
A nonlinear curve-fitting procedure (Marquardt-Levenberg algorithm) was used to fit the two-compartment model for the single injection of ICG. Statistical comparisons of each response variable among groups were accomplished by using analysis of variance with repeated measures. Where significant group differences occurred, appropriate post hoc pairwise comparisons were performed by using Scheffé's test with a significance level of 0.05. Training effects on subject characteristics and exercise responses were assessed by using paired t-tests and one-factor analysis of variance, respectively. Group data are presented as means ± SE.RESULTS
Effects of Age
Table 3 presents resting values and exercise responses for selected physiological variables for the four groups, which differed in age and fitness level. Exercise HR was generally lower in both groups of older men, and the younger men responded with significantly higher plasma [NE] (P < 0.01) during exercise at 60%O2 max. Figure
1 depicts the group mean values of FBF,
c, SBF, and RBF at rest and at each
exercise intensity. At rest, only RBF showed a clear age difference,
with the RBF of the older men significantly lower than their younger
counterparts (P < 0.05). During
exercise, younger subjects had significantly higher FBFs than the older men and, at the higher intensity, the younger subjects decreased SBF to
a greater extent than did the older subjects
(P < 0.02). The change in each
regional blood flow from rest to exercise at 60%
O2 max is more easily
seen in Fig. 2. RBF, significantly lower at
rest in the older men, reached similar values during exercise at 60%
O2 max, resulting in a
greater (P < 0.02) reduction in RBF
in the younger subjects.
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c),
splanchnic blood flow (SBF), and renal blood flow (RBF) at rest and
during exercise at 35 and 60% maximal
O2 consumption
(O2 max).
Top, left to
right: responses of younger fit and
sedentary men; bottom, left to
right: responses of older fit and
sedentary men. A higher fitness level was associated with greater FBF
and c responses for younger men only; there were no
fitness effects on older groups of men. * Significantly different
from sedentary group of same age, P < 0.05. 
Significant age difference compared with younger group of similar fitness category, P < 0.05.
) in blood flow variables from rest to exercise at 60%
O2 max for 4 groups.
All intergroup differences are statistically significant except where
noted [not significant (NS)]. Higher FBF of younger fit
group compared with younger sedentary group was associated with a
greater increase in c and greater decreases in SBF
and RBF. Conversely, there was no such "fitness effect" in older
men.
Fitness Effects
Within each age group, there were some resting and exercise effects attributable to fitness (Table 3). At rest and at 35%O2 max, MAP was
significantly higher in the OS group compared with the OF group
(P < 0.05), an effect not seen in
the younger subjects. At 60%
O2 max, plasma
[NE] was significantly higher in the YF group than the YS
subjects (P < 0.01), but no such
difference was seen in the older men. Finally, the percentage change in
PV was less for the two sedentary groups compared with their more fit
counterparts (P < 0.05).
Interactive Effects of Age and Fitness
As mentioned above, the younger subjects had significantly higher FBFs than the older men during exercise, but a higher fitness level was associated with a higher FBF in the younger group only (Fig. 1). The greater FBF of the YF group was associated with a higherc (P < 0.05), whereas the c response of the other three
groups was similar in magnitude. In the older group, fitness level had
no significant effect on any absolute flow or change in flow measured
(Figs. 1 and 2), with the exception of change in () FBF from rest to
60% O2 max.
When SBF and RBF are treated as additive, each age-fitness group
differed significantly (P < 0.05)
from every other in terms of the total flow redirected from these two
vascular beds (SBF + RBF) (Fig. 3).
O2 max i.e., RBF + SBF. Values are means ± SE; n = 6/group. Decreased blood flow from these regions is redirected
to cutaneous circulation during exercise in a warm environment. Each
group total was significantly different from that of every other
group.
Training Study
Because there were cross-sectional differences between the YF and YS groups which were absent in the older groups (Fig. 1), four of the OS subjects underwent a rigorous endurance training regimen. Before-and-after comparisons for selected physiological variables within this group are presented in Table 4. Well-documented training effects are shown by a lowerO2
(P = 0.06), HR, MAP, and
[NE], and a higher SV (all
P < 0.05) when these subjects are exercising at the same absolute intensity, i.e., at the pretraining intensity, which corresponded to 60% of pretraining
O2 peak. After
training, older subjects exercising at 60% of the
now-higher O2 peak (the
same relative workload as before training) had a significantly higher
FBF and c. Figure 4,
similar in format to Fig. 2, shows the change in each measured flow
from rest to exercise at 60%
O2 max. The
entire additional FBF at a similar relative intensity after training
was associated with a higher c because there was no
change in the flow redistributed from renal and splanchnic beds. The
total flow redistributed away from these circulations (SBF + RBF)
was 421 ± 96 ml/min before training and 423 ± 109 ml/min after
training (P > 0.05), respectively.
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FBF, c, SBF, and RBF from rest to
exercise at 60% peak O2
consumption (O2 peak)
in a subgroup of 4 older men before (hatched bar) and after (total bar
height) 4 wk of intense aerobic training. Solid bars and white arrows,
training-induced increase in FBF and c; however,
training had no effect on splanchnic and renal vasoconstriction during
exercise at the same relative intensity.
Control of SBF and RBF
Figure 5 presents the percentage (%) of resting SBF plotted as a function of %O2 max
(A) and as a function of plasma
[NE] (B). In
A, the linear relationship between
SBF and %O2 max published by Rowell (26, 27) is shown by the solid line, whereas the
relationship predicted by combined groups of younger and older men from
the present study are shown by the dotted (y = 126 1.23x) and dashed lines
(y = 114 0.73x), respectively. Collapsing both age groups tested in the present study into one relationship yields a line remarkably similar to that suggested by Rowell (26, 27).
When %resting SBF is plotted against plasma [NE], a
surrogate measure of sympathetic nervous system (SNS) activity, the
relationship is relatively unaffected by either age or fitness (Fig.
5B).
O2 max
(A) and plasma norepinephrine
concentration ([NE]; B).
Solid line, linear relationship between SBF and
%O2 max published by
Rowell (26, 27); dotted and dashed lines, relationship predicted by
combined groups of younger and older men from present study
(y = 126 1.23x and y = 114 0.73x, respectively).
Interestingly, collapsing both age groups into 1 relationship yields a
line remarkably similar to that suggested by Rowell. These data suggest
that relationship between splanchnic vasoconstriction and relative
exercise intensity is affected by age but not by fitness level. When
same y variable is plotted against
plasma [NE], a surrogate measure of sympathetic nervous
system activity, relationship is relatively unaffected by either age or
fitness. YF, younger fit; YS, younger sedentary; OF, older fit; OS,
older sedentary.
DISCUSSION
We recently reported that exercise-induced splanchnic and renal
vasoconstriction, and the resulting redistribution of blood flow, is
influenced by chronological age (16). This paper adds the concept that
this response may be changeable by regular exercise training in
younger, but not older, subjects. The first half of this hypothesis is
supported only by cross-sectional data; however, the latter half, that
the smaller decrease in SBF and RBF during moderate-intensity exercise
in older men does not change after training, is supported by both
cross-sectional data and a brief but rigorous longitudinal training
study. As in previous reports (14, 17, 18), increases in
SkBF were lower in older exercising subjects, regardless of their
O2 max or exercise
activity.
In addition, these data provide new insights into the effects of such
individual characteristics as age and aerobic fitness on the ability to
change regional blood flow in response to the dual challenges of
exercise and heat stress. Specifically, the present data demonstrate
that control of SBF and RBF during exercise at a given relative
intensity is age dependent because chronological age had a significant
impact on this response. However, in agreement with Rowell (26, 27),
within an age group the relationship between %SBF and
%O2 max is
minimally affected by the subjects' O2 max.
Plasma Norepinephrine
The four discrete groups exercised at intensities of 35 and 60%O2 max. The former
intensity was chosen to examine exercise responses with minimal SNS
activation, the latter to allow for 30 min of steady-state exercise
with a higher level of SNS activation. Although venous [NE] provides
only a rough index of general SNS activity, the [NE] data
illustrate this effect. There was no age difference in baseline
[NE], which then increased 25-53% at the lower
intensity. At 60%
O2 max, much
larger increases in [NE] were observed, although these
increases were significantly smaller in the older men
(P < 0.05). Age differences in
[NE] reported in the literature are contradictory. At rest,
older individuals have been reported to have higher (30, 33) or similar
(10, 20) [NE]. Some of this difference appears to be
related to subject selection because older and younger men matched for
O2 max (13) or body fatness and fat distribution (22) have a similar baseline [NE]. Because our subjects sat in the 36°C environment
for 50 min (with data collected during the last 30 min), our values
should not be considered "basal" levels. At 60%
O2 max, older
men in the present study had significantly lower [NE] than
the younger men, regardless of fitness category, a relatively
consistent finding in the literature (10, 20). Our data are consistent
with the meager literature in this area in two other respects,
1) the lack of a "fitness"
effect in the older men's [NE] response to exercise (21) and (2) the similarity of
[NE] response between the YS and OF groups, which had
similar
O2 max values
(13). The relationship between regional blood flow and plasma
[NE] as a surrogate measure of SNS activity is discussed
below.
General Exercise Responses
Other group differences during exercise were, for the most part, predictable on the basis of our experimental design. Resting HR was 15% higher in each sedentary group (P > 0.05), and the HR response to exercise was blunted in the older men (P < 0.05). At rest and at 35%O2 max, MAP
was higher in the OS group. Because c and blood flow
responses were compared at relative exercise intensities, it is
possible that differences that we have attributed to
fitness may have been due to a greater hyperthermic
influence in the fit groups. That is, for fit and unfit subjects to
exercise at the same relative intensity, the group with the higher
O2 max must exercise at
a higher absolute intensity and thus a higher metabolic heat
production. Tes was not
statistically different among the four groups tested, although the
increase was largest in the YF group. We specifically chose a hot dry
environment (water vapor pressure of 8-10 mmHg) to maximize
sweating efficiency in hopes of minimizing the effects of metabolic
heat production on core temperature. A lack of age or fitness effects
on Tes when subjects exercise at
the same relative intensity was demonstrated by the classic data of
Saltin and Hermansen (31).
Tsk, on the other hand, was
generally lower in the older men at 60%
O2 max (although
significantly so only between the fit groups), something we have noted
previously and that is attributable to the lower SkBFs of older
subjects (15). Sweating rates were too variable to find statistical
differences among groups; however, the pattern of sweat loss was YF > YS = OF > OS, showing the sudorific stimulus of regular exercise. It
should be noted that it is difficult to discriminate between training
effects and effects of heat acclimation in a comparison of groups that
differ in habitual physical activity. Regular exercise in cool
environments causes physiological adaptations that are qualitatively
similar to those conferred by heat acclimation. To minimize acclimation
effects, our subjects were not tested during the warm summer months in
central Pennsylvania. The lack of statistical significance among the
groups in sweating rate offers some evidence that no large heat
acclimation effects were evident in the fit groups. PV changes during
exercise were less in the sedentary groups
(P < 0.05) with no difference due to
age, although the mechanism underlying this difference is not
discernible from the present data.
Training Effects
Because there were fitness differences in the responses of the younger subjects that were not evident in the older men (see below), we decided to actively train the OS men and retest them. Only four of these subjects were able to perform this aspect of the investigation and, due to logistical considerations, onlyO2 peak was measured
before and after training. Nonetheless, these men vigorously trained
for 4 wk with direct supervision and motivational support by one of the
investigators. The results reflect training-induced adaptations that
are consistent with other studies and that provide solid evidence of a
training effect (see Table 4). After 4 wk,
O2 peak
increased 27-28% and PV was expanded by 14%, with no changes
in either body weight or adiposity (Table 2). Resting HR was, on
average, 9 beats/min lower after training (Table 3), but there were no
training effects on any other resting variable, including
c, indicating the typical increase in
resting stroke volume as a fundamental consequence of training. And
although the O2 during
exercise at 60%
O2 peak after exercise
training was 10% higher on an absolute basis, there were no
significant posttraining differences in MAP,
Tes,
Tsk, [NE], or %PV
at the same relative intensity. In agreement with many previous
publications, the change in body weight (reflecting sweat loss) was
slightly, but not significantly, higher after training (1.14 ± 0.18 vs. 0.92 ± 0.12 kg).
c and Its Regional Distribution
c and its distribution to various organs.
Working muscle blood flow and SkBF increase to meet metabolic and
thermoregulatory demands, respectively. c increases
during exercise as a function of
O2; however, addition of an
exogenous heat source is not accompanied by a further increase in
c (24). This pattern of integrated responses is
clearly shown in Fig. 1 for each of the four groups of subjects. On the
other hand, the data in Fig. 1 and 2 also demonstrate interactive
influences of age and fitness on the magnitude of these cardiovascular
responses.
The only resting blood flow variable that was affected by age was RBF,
which was significantly (P < 0.05)
lower in both older groups both at rest and at the lower exercise
intensity. Resting RBF of the groups averaged 1,251 ± 36 (YF),
1,095 ± 82 (YS), 940 ± 68 (OF), and 927 ± 59 ml/min (OS).
That aging is associated with decreased resting RBF is well known (34)
and has been a consistent finding in our laboratory (19). Aging results
in a loss of functional glomeruli, and both blood flow and glomerular filtration rate decrease. During exercise at 35%
O2 max, the only other
variable showing an age effect was FBF, which was lower in the OF than
the YF men, but similar to that of the YS men.
Within the younger group, there was a fitness difference in the
exercise responses of FBF and c, with a
higher O2 max associated with a significantly greater exercise response of both variables. A higher
c at a
given relative workload is an indication of an enhanced training
state; however, the same could be said for absolute workload, and the
present design cannot argue against the higher c of
the YF group being an expected response to a greater absolute workload.
Nonetheless, no such effect of a higher O2 max on either
c or FBF was evident in the older group, although a slightly higher FBF was achieved by the fitter men at 60%
O2 max
(P > 0.05). However, when examined
as the change in blood flow from rest to exercise at 60%
O2 max (Fig. 2), the
difference in SkBF (FBF) between the OF and OS men achieved statistical
significance, and a graded pattern of cutaneous vasodilation emerged,
i.e., YF > YS > OF > OS. Because the 4-wk endurance training regimen also significantly increased FBF, it is apparent that training
increases FBF during exercise in the heat in older men as it does in
younger men (23). Furthermore, because the
Tes response to exercise was
similar before and after training, FBF at a given
Tes was increased. Although not
shown here, that increase was accomplished by a greater slope of the
FBF-Tes relationship rather than a
leftward shift in the Tes
threshold for onset of cutaneous vasodilation.
Figure 2 also shows that the higher FBF of the YF men compared with the
YS men was accompanied by a greater increase in c and
greater decreases in blood flow to both splanchnic and renal circulations (P < 0.05). A
comparison of the two older groups shows no such fitness effects with
respect to c, SBF, or RBF, none of which was
significantly different between the OF and OS groups. In each case, the
fitter group had only a slightly greater increase in
c and slightly greater decreases in SBF and RBF, which combined to account for the higher FBF. The c
response of the older men was somewhat different after short-term
training (see Fig. 4). Analogous to the cross-sectional group
comparison, there was greater rise in FBF after training but, unlike
the cross-sectional comparison of OF and OS exercise,
c was higher after training. The most plausible
difference between these experimental approaches lies in the PV
expansion that attends short-term exercise training. We speculate that
the training-induced expansion of PV allowed for a greater SkBF and a
greater c response to exercise, whereas the similar
PVs of the OF and OS groups did not. On the other hand, there were no
significant differences in SBF or RBF between the OF and OS men
(Fig. 2), nor were these responses changed by training (Fig. 4). Hence,
both aspects of this study suggest a lack of adaptation of splanchnic
and renal vasoconstriction to regular exercise in men in their 60s.
The primary purpose of this investigation was to determine how
individuals who differ in age and fitness accomplish such increases in
SkBF, i.e., the extent to which an increased c and
redistribution from splanchnic and renal circulations contribute to the
SkBF response. As noted by Zambraski (36), the extent to which regional vasoconstriction contributes (SBF + RBF here = 0.5 1.2 l/min, Fig. 3) is small compared with the relatively large increases in
c (range 7-13 l/min). However, the magnitude of
the range of blood flow redistribution seen here may be particularly
important in individuals with compromised left ventricular function and thus a relative inability to increase c.
Control of Regional Blood Flow During Exercise
In his books (26, 27), Rowell makes an eloquent case for the concept that differences in splanchnic and renal vascular responses among various groups of subjects differing widely inO2 max virtually
disappear when those groups are compared at the same relative exercise
intensity, i.e., the same
%O2 max. This
relationship is shown by the solid line in the upper panel of Fig. 5,
and was gleaned from data compiled from several studies (2, 24, 26)
that tested athletes, nonathletes, and patients with a low
O2 max as a consequence
of mitral stenosis. Our data support this contention. Within a
given age group, differences in
O2 max had little
effect on the
SBF-%O2 max
relationship because this relationship was similar for both groups of
younger and both groups of older men (Fig.
5A). Rowell (27) concluded that
"superimposition of heat stress on the stress of exercise caused the
only exception seen so far" in the relationship between SBF and
%O2 max. The present
data argue that age also changes the slope of this linear relationship,
with younger subjects having a steeper decline in SBF with increasing
exercise intensities (1.23 ± 0.06 vs. 0.73 ± 0.04 %/unit increase in intensity, P < 0.001), even when
%O2 max is the
independent variable. When data from all four of our subject groups are
collapsed into a single line (yielding an overall mean slope of
0.95 ± 0.07), the general relationship is very close to that
predicted by Rowell (27) (estimated slope of 0.98 for athletes,
nonathletes, and patients combined).
A unifying hypothesis for this finding is illustrated in Fig.
5B. Because the SNS controls visceral
vasoconstriction during exercise and because SNS activity may differ
with age, we decided to plot SBF vs. [NE]. With
[NE] on the abscissa, the responses of all four groups
become similar. (The only minor exception may be the YF group at the
higher intensity, which makes the relationship for that group
curvilinear. This seeming outlier may simply reflect the nonspecificity
of plasma [NE] as an indicator of SNS function.) Nonetheless, when viewed from a stimulus-response perspective, it makes
sense that this relationship might be more congruous across age groups
than a comparison of SBF vs
%O2 max.
Comment on Methodology
The method of peripheral sampling to determine CICG as a measure of SBF requires that the liver ER of ICG remain constant during changes in flow. Previous studies using hepatic catheterization have shown that ER does not change or increases slightly during exercise and/or passive heat stress, even when SBF is so low that oxygen extraction is 100% (28, 29). Any slight increase in ER of the magnitude reported with decreased SBF results in an underestimation of hepatic-SBF by only a few percentage points (29). In contrast, in conditions where SBF is increased (such as hypoxia) ER is decreased (25), indicating that, at rest and under conditions that reduce SBF, the transport maximum of glutathione S-transferase (the carrier protein for ICG) is maximal and is not flow dependent. If ER does not change significantly, i.e., during heat stress or exercise, the CICG measured in peripheral venous blood is proportional to changes in SBF.There is no evidence to suggest that liver extraction of ICG in healthy
older humans screened for cardiovascular or liver disease is affected
by SBF. Pilot testing on 34 subjects in our laboratory as well as a
previous study (35) have shown that liver ER of ICG [measured by
iv bolus technique utilizing a two-compartment model (7)] is
unaffected by age in the absence of liver dysfunction. On the other
hand, there is evidence of altered ER in patients in intensive care
with liver disease or who have a history of heavy alcoholic
consumption. In these patients (and in animal models), measured ER
values are quite low (4, 32) and
CICG is dependent on hepatic
function. Conversely, in healthy humans with high ERs,
CICG is clearly dependent on flow.
Finally, from a methodological standpoint, some studies (4, 32) have used a high bolus dose of ICG and/or high infusion concentrations, and saturation of glutathione S-transferase may be a concern. In the present protocol, the priming ICG dose (0.10 mg/kg) was well below the bolus dose used to determine ER, and the total ICG infused over the 150 min should not cause saturation of the transport protein. Thus it is reasonable to conclude that ER is relatively constant in healthy younger and older subjects even when SBF is reduced, and any slight changes in ER would not significantly alter blood flow calculations. Under those conditions, and within the present context, we have found this procedure to estimate SBF to be a reliable and repeatable method.
Summary
The purpose of this investigation was to determine how individuals who differ in age and fitness accomplish large increases in SkBF during exercise in warm environments, i.e., the extent to which an increasedc and redistribution from splanchnic and renal
circulations contribute to the SkBF response. From the present data, the higher SkBF observed in YF men (compared with their sedentary
counterparts) appears to be a function of both a higher c and a greater redistribution of flow from
splanchnic and renal circulations. During exercise at a moderate
exercise intensity, the distribution of c to regional
circulations is age specific, with older men showing smaller increases
in SkBF and smaller decreases in SBF and RBF. The attenuated splanchnic
and renal vasoconstriction in older men does not appear to change with
exercise training.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the scientific input of Drs. E. R. Buskirk, W. Channing Nicholas, and Susan M. Puhl, the technical support of Joseph L. Loomis, Douglas A. Johnson, Marlin Druckenmiller, and Fred R. Weyandt, and the statistical expertise of Dr. Janice A. Derr. Catecholamine assays were run with the assistance of Domingo Pinero in the laboratory Dr. J. L. Beard.
FOOTNOTES
Address for reprint requests: W. L. Kenney, Noll Physiological Research Center, Pennsylvania State Univ., Univ. Park, PA 16802-6900 (E-mail: w7k{at}psu.edu).
Received 23 May 1996; accepted in final form 2 December 1996.
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