Age and hypohydration independently influence peripheral vascular response to heat stress
the
W. L. KENNEY, C. G. TANKERSLEY, D. L. NEWSWANGER, D. E. HYDE, S. M. PUHL, AND N. L. TURNER Laboratory for Human Performance Research, Pennsylvania State University, University Park, Pennsylvania 16802
KENNEY, W. L., C. G. TANKERSLEY, D. L. NEWSWANGER, D. E. HYDE, S. M. PUHL, AND N. L. TURNER. Age and hypohydration independently influence the peripheral vascular response to heat stress. J. Appl. Physiol. 68(5): 1902-1908,1990.-Seven
young (Y, 22-28 yr) and seven middle-aged (MA, 49-60 yr) normotensive men of similar body size, fatness, and maximal oxygen uptake (Vozmax) were exposedto a heat challenge in an environmental chamber (48°C 15% relative humidity). Tests were performed in two hydration states: hydrated (H, 25 ml water/kg body wt 1 h before the test, 2.5 h before exercise)and hypohydrated (Hypo, after 18-20 h of water deprivation). Each test began with a 90-min rest period during which the transiently increasedplasmavolume and decreasedosmolality after drinking in the H condition returned to baseline. This period was followed by 30 min of cycle exerciseat a meanintensity of 43% Vozmax and a 60-min resting recovery period with water ad libitum. Although prior drinking caused no sustained changesin plasmaosmolality, Hypo increasedplasmaosmolality by 7-10 mosmol/kg in both groups. There were no significant agedifferencesin water intake, urine output or osmolality, overall changein body weight, or sweatingrate. In the H state, the percent changein plasmavolume wasless(P < 0.01) during exercisefor the Y group (-5.9 & 0.7%) than for the MA group (-9.4 t 0.6%). Esophagealtemperature (T,,) was higher in the Hypo condition for both groupswith no age-relateddifferences. Throughout the 3-h period, mean skin temperature washigher in the Y group and significantly so (P < 0.05) in the Hypo condition. During exercise, forearm blood flow (FBF) was significantly (i.e., 50-60%) lower and mean arterial pressurewas significantly (15-20 mmHg) higher in the MA group in both hydration states, yielding an elevated forearm vascular resistance compared with the Y group. Furthermore, there was no interaction betweenageand hydration state in theseperipheral vascular responses.Estimated core-to-skin heat conductance was-50% lower in the Hypo condition but wasnot significantly different between agegroupsbecausethe higher FBF of the Y group offset their lower core-to-skin temperature gradient (thus accounting for the similar AT,, in both age groups). It was concludedthat age-relatedalterations in the peripheral circulation limit vasodilation and maintain higher arterial pressures during exercisein a warm environment. These differences are not a function of age-related differences in cardiorespiratory fitness or hydration state but appear to be a primary consequenceof the aging process. aging; skin blood flow; blood pressure;temperature regulation; body temperature; peripheral vascular resistance
is elevated, heat is typically conducted from the core to the skin for subsequent WHEN BODY TEMPERATURE 1902
via dry and evaporative heat loss. Conduction of this heat load is a function of both skin blood flow (SkBF) and the thermal gradient between core and skin (7). The ability to measure whole body SkBF in human subjects is limited, so changes in forearm blood flow (FBF) are commonly measured because increases in FBF during passive heating (2) and prolonged dynamic leg exercise in the heat (1, 11) are confined to the forearm skin. Furthermore, neurogenic control of forearm SkBF is reported to reflect that of SkBF to most of the body surface (6), and increases in forearm SkBF appear to reflect increases in whole-body SkBF in pattern and magnitude (14). Although control and magnitude of FBF under heat stress conditions has been well studied in young subjects, only recently has the role of aging in this response been given much attention. In 1936, Pickering (18) showed an attenuated hand blood flow response to body heating in older subjects, yet in the 1950’s, Hellon et al. (8,9) published contradictory results. This latter group of researchers showed that under hot conditions, FBF of men 45 yr of age was double that of men 25 yr of age (8). However, the subjects used were not well described with respect to cardiovascular fitness, activity level, body size, or acclimation state (8, 9). In the past decade, we (12, 22) and others (21) have shown that FBF is lower in older subjects at rest or during exercise in warm environments compared with younger subjects. Evidence suggests that older men and women are prone to hyperosmolar hypohydration (17). This may result from a decreased thirst sensitivity and/or a limited ability of the kidneys to concentrate urine, which might lead to enhanced free water excretion (17). Hyperosmolality secondary to water deprivation or diuretic use has been shown to decrease SkBF in baboons (23) and in humans (5). Therefore, the purpose of this investigation was to further examine the FBF response of young vs. middleaged men under conditions of adequate hydration and after water deprivation to better understand the role of aging in thermoregulatory responses. Because not controlling for prior drinking behavior leaves doubt as to just what fluid state “euhydration” signifies, we prehydrated our subjects with a volume of water equal to 2.5% of body weight before the experimental session. Because prehydration immediately bedissipation to the environment
0161-7567/90 $1.50 Copyright 0 1990 the American Physiological Society
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FBF:
AGE
AND
fore exercise may alter thermoregulatory responses because of an expansion of plasma volume, the subjects sat at rest in the environmental chamber for an additional 90 min (for a total of 2.5 h) before exercising. Without the use of a plasma expander (e.g., glycerol, albumin, dextran) “hyperhydration of an individual by ingesting large volumes of fluid before a stressful work environment [is not] possible” (21). Therefore, we tested subjects in a state of controlled hydration (not hyperhydration, because the fluid was not retained in the vascular space) and in a state of hypohydration to best compare relative effects of hypohydration in these two distinct age groups. METHODS
Subjects. Seven middle-aged (MA) and seven young (Y) men were recruited to serve as subjects for this investigation. The MA group ranged in age from 49-60 yr and the Y group from 22-28 yr. All subjects were regular exercisers, although the MA group could subjectively be characterized as more aerobically active on a regular basis; it included two competitive masters-level runners. The investigation took place between the months of September and March, and no effort was made to acclimate the subjects to heat. Before participation, verbal and written informed consents were procured from all subjects, and each subject was examined by a physician. This preliminary screening included a resting 12lead electrocardiogram, hydrodensitometric measurement of body composition, and a maximal graded exercise test on a motor-driven treadmill by use of a modified Balke protocol. None of the subjects smoked, and all were normotensive. Mean subject characteristics are presented in Table 1. Protocol. The test consisted of 3 h in an environmental chamber set at a dry-bulb (and globe) temperature of 48°C and a wet-bulb temperature of 25°C (15% relative humidity). There was no forced air movement; average air velocity was ~0.4 m/s. Subjects were clothed in shorts, cotton socks, and running shoes, and they sat throughout the test in a reclining mesh seat affixed to a cycle ergometer. Before entering the chamber, each subject was weighed nude and seated in a wheelchair for the next 30 min to minimize postural influences. Subjects were again weighed nude after the experiment. Hydration state was manipulated in randomized order before the tests. On one test day, the subject was given cool (ll-12°C) water (25 ml/kg body wt) to drink during the hour before entering the chamber. This was denoted the hydrated (H) condition; it ensured that subjects were fully hydrated, rather than hyperhydrated. This volume of water ingestion transiently increased plasma volume
1903
HYPOHYDRATION
(PV) and decreased plasma osmolality. Base-line PV and osmolality were restored by the end of the initial 90-min rest period (Fig. 1, Table 2). Furthermore, water intake minus urine output was not significantly different between H and hypohydrated (Hypo) conditions. Mean urine specific gravity remained X.010 for both groups after drinking. The other test was performed after an 18-h period of water deprivation (Hypo). For these tests, the subject consumed no liquids after 1500 h on the previous day but was allowed to eat food from a list of lowwater (~75%) foods. The only exception to this was the drinking of a small (200-ml) volume of water while the esophageal thermocouple was inserted. This procedure changed preexposure body weight by -2% and caused a sustained increase in mean plasma osmolality of 7-10 mosmols/kg. One MA subject completed only the Hypo test for reasons not significant to the study, but the statistical analysis employed allowed inclusion of his data for that condition after verification that addition of these data did not qualitatively alter the results. For the initial 90 min, the subject sat at rest on the ergometer. For the H tests, urine was collected and volume was measured at minutes 60 and 90. This 90-min period of passive heating was followed by 30 min of dynamic leg exercise at an average intensity of 43% of previously measured treadmill maximal oxygen uptake (VOW,,,). Although this may represent a high VOWrelative to peak cycle Ooz, it was believed that a similar relative intensity (as well as absolute intensity) was maintained across both groups. The final 60 min were spent at rest A 10
-1
rest, no water
contrd
-20
’
-30
I 30
0
B
8x81.
-
I ’ I 60 90 Time (mln)
rest, water
-
I 150
120
’ 180
Hypohydrated
1. Subject characteristics
TABLE
Age, Mb, Yr
%Fat
kg
&/Mb, m2/k
VO
ml - kg-’ - min-’
2
max
l/min
cant rol
-20
Y MA
Hydrated
24&l 54&2*
Values condition). value.
77&4 69k4
are means k&, body
16t2 19t2
0.025&0.001 0.026*0.001
50.3t1.2 47.8t3.7
3X5&0.24 3.24t0.14*
t SE; n. = 7 men per group (6 MA men in the H mass; AD, DuBois surface area. * P c 0.05 from Y
exer.
rest, no water
rest, water .
-
-30
I
0
n
1
30
-
I
r
!
60 90 Time (mln)
,
.
-
120
150
180
FIG. 1. Percent change in plasma volume as a function of time for Y and MA men in each hydration state. Open symbols, MA subjects; closed symbols, Y subjects. Values are means t SE.
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1904
FBF:
AGE
AND
HYPOHYDRATION
with water (11-12°C) provided ad libitum, and water consumption during the 3rd h was monitored. All tests began at 0900 h, with >l rest day between consecutive tests. Measurements. Esophageal temperature (T,,) was measured every 5 min through the first 120 min from a copper-constantan thermocouple within a sealed infant feeding catheter. Each catheter was marked at 40% of subject height and taped to the cheek at this mark to establish a uniform insertion depth. Rectal temperature (T,,) was measured every 5 min throughout the 3 h via a flexible thermistor inserted 9 cm past the anal sphincter. Mean skin temperature (Tsk) was calculated every 5 min as the weighted average of four uncovered sites: chest, upper arm, thigh, and calf (19). Heart rate was monitored continuously and recorded every 5 min from a singlelead electrocardiogram. Measured variables, chamber conditions, and pedal rpm were recorded and stored on a dedicated computer via a Keithley Series 500 data collection system. iTo was measured by the open-circuit technique at minutes 45 (rest) and 100 (exercise). FBF was measured three times within a 20-s period on entry into the chamber and every 10 min thereafter by venous occlusion plethysmography and a mercury-inSilastic strain gauge (25). The average of these three values was recorded as the FBF for that time period. The left arm was suspended away from the body just above the venostatic level, and arterial flow to the hand was occluded with a wrist tourniquet before each series of measurements. In the same arm, arterial blood pressure was measured by auscultation every 15 min. Mean arterial pressure (MAP) was calculated from systolic (SBP) and diastolic (DBP) pressures as MAP = 1/3 SBP + 2/3 DBP. Forearm vascular resistance (FVR), in units of mmHg ml-‘. 100 ml min, was calculated as the ratio of MAP to FBF. Venous samples (lo-11 ml per sample) were drawn from an antecubital vein in the contralateral arm without stasis 1 h preexposure (before drinking in the H condition), immediately on entry into the chamber, at minutes 15 and 30 and every 30 min thereafter. Urine was collected before each subject entered the chamber and at minutes 60 and 90 of the H experiments. Urine volume, osmolality, and specific gravity were determined. Percent changes in PV were determined from hematocrit (microhematocrit method) and hemoglobin (cyanmethemoglobin method) according to the method of Dill and Costill (3) with appropriate corrections for venous sampling and trapped plasma. Plasma and urine osmolality were determined by freezing-point depression by use of an osmometer (Advanced Instruments), and total protein concentration was determined by the biuret method by use of an autoanalyzer (Technicon). Plasma Na’ and K+ concentrations were determined by flame photometry (Instrument Laboratory). Overall sweating rate was determined from the change in nude weight corrected for fluid intake and output but not for respiratory water loss, which was assumed to be negligible. All provided water was carefully measured, and the volumes were recorded. To estimate core-to-skin heat conductance (k), SkBF l
l
was estimated from FBF according to the assumptions set forth by Johnson et al. (10). These assumptions include a constant skin thickness and forearm segment dimensions and a muscle blood flow of 2 ml 100 ml-‘. min? Conductance was calculated (7) in watts as k = SkBF x 64.2 (T,, - Tsk) where SkBF is in l/min, 64.2 is the specific heat of blood in We min. 1-l. ‘C--l, and (T,, - Tsk) represents the coreto-skin temperature gradient; k was then corrected for body surface area (W/m”). Statistics. Data were analyzed for age and hydration effects using multivariate analysis of variance for passive heating, exercise, and recovery periods. Subsequently, univariate analyses of variance were performed to examine age and hydration effects across time. Critical alpha level was set at 0.05. Data are presented as means t SE. RESULTS
The subject groups were well matched for body size and composition and VO zrnax relative to body weight (Table 1). Although there was no significant difference between the groups in VO 2max relative to body weight, the mean absolute VO zrnaxof the MA group was ~15% lower because of the 8-kg difference in mean weight. However, during exercise, metabolic heat production (calculated from exercise Vo2 with the assumption that 1 liter 02 = 4.9 kcal and subtraction of external work performed) was 236 t 8 (SE) W/m” for the Y group and 225 t 11 W/m” for the MA group (not significantly different). Table 2 presents plasma and urine osmolality, total protein concentration, and plasma electrolyte concentrations. These data and Fig. 1 clearly indicate that the transient increase in PV and decrease in osmolality after drinking were resolved by minute 90, i.e., before initiation TABLE 2. Plasma and urine osmolality, total plasma protein concentration, and plasma electrolyte concentrations for Y and MA men at various times during the protocol H Before drinking
After drinking
Plasma osmolality, mosmol/kg Y 281t3 276t2 MA 283t3 280t3 Total proteins, g/d1 Y 6.8&O. 1 6.7t0.2 MA 6.5~10.1 6.320.1 Na+, meq/l 139&l Y 140t2 140+2 MA 140t2 K+, meq/l Y 4.lkO.2 4.120.1 MA 4.OkO.2 4.OkO.l Urine osmolality, mosmol/kg Y 943*91 532+151 t MA 741HO5 536+102-f’
HYPO Minute
90
282t2 27922
After water deprivation
288+1p 290+2t
Minute
90
287&l? 289kZ.f
6.9&O. 1 6.3tO.l*
6.920.2 6.720.2
7.1to.1 6.6*0.1*
140,tZ 139t3
139&l 142&Z
141&Z 143&l
4.0,tO.Z 4.1t0.2
4.0,to.o 4.l_tO.l
4.2&O. 1 4.2,tO. 1
Values are means t SE. * Significantly 0.001 from before-drinking value.
995k49 868k34 lower
than
Y value;
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FBF:
AGE
AND
of exercise. The enhanced free water clearance is evidenced by the lowered urine osmolality relative to the predrinking urine sample. On the other hand, the significantly higher plasma osmolality consequent to water deprivation (compared with the before-drinking samples) was sustained throughout the 90-min rest period before exercise. Total plasma proteins were 3-7% lower (P < 0.05) for the MA group throughout the session for both conditions. There were no significant age or hydration differences in plasma Na+ or K+ concentration. Figure 2 shows the mean T,,, T,,, and T,k responses for the Y and MA subjects. T,, was artificially low in the H condition (because of the cool water consumed before the subjects entered the chamber) at time 0, but it plateaued late in the passive heating phase of the protocol. If this transient is excluded, T,, at minutes 30-90 (rest) and at minutes 90-120 (exercise) was significantly higher in the Hypo condition (P < 0.05) in both age groups. There were no significant differences in T,, caused by age. T,k was higher in the Y subjects in both hydration states but significantly higher only in the Hypo condition. Although the esophageal thermocouple was extracted after minute 120 to allow drinking, we continued to monitor T,, throughout the 3 h (Fig. 2). At the end of exercise, the T,, of the Y group continued to increase and remained above the end-exercise value for the next 20-30 min. The overshoot seen in the Y group was greater than that seen in the MA group, causing a significant (P A 39
Hypohydrated
Hydrated
39
1
38
38
1905
HYPOHYDRATION
< 0.05) age effect across hydration
states at minutes DO-
180.
Cardiovascular responses are presented in Fig. 3 and Table 3. Overall, heart rate was significantly lower for the MA subjects; however, the increase from rest to exercise was similar for both groups. When heart rate was expressed as a percentage of maximal heart rate obtained during the maximal graded exercise test, no significant age differences were seen. During exercise, but not during the preexercise rest period, the FBF of the Y group was significantly higher (P < 0.05) and the MAP was significantly lower (P c 0.01) than those of their older counterparts in both hydration states. Exercise FBF at minute 120 was significantly lower (P c 0.05) in the Hypo state for all subjects. Although there were independent effects of age and hypohydration on FBF during the exercise period, there was no statistical interaction between age and hydration state in the FBF response. In the Hypo condition, the significantly higher FBF of the Y group lasted 20 min after exercise had ceased (Fig. 3). As presented in Table 3, the lower exercise MAP of the Y group was primarily the result of a greater reduction (P c 0.01) in DBP, although SBP was also slightly lower in the Y than in the MA group (not significant). As a result of the higher pressure-lower flow of the MA group during the exercise bout, calculated FVR was -150% greater (P < 0.001) in this group than in the Y group. Changes in PV (% APV) during the exercise bout are also shown in Table 3. When water loaded, an early hemodilution was noted (see Fig. 1) followed by a return to near base-line values by the end of the resting phase. % APV during exercise was calculated using hematocrit B 20
Hypohydrated
1
36
36
1 0x81 35 0
30
60
90
120
150
0
180
I 30
I 60
I 90
I 120
I 150
I 180
0, 0
, 30
, 60
, 90
, 120
, 150
, 180
0
30
0
30
60
90
120
150
180
38
38
2
E
36
36 0
30
90
60
120
150
I
I 90
180
I 120
I 150
I 180
100
100
90
90
80
80
.
$
, 0
38
middle-aged
”
30
60
90
120
150
180
I, ! , exer
90
-
36
36
, 60
150
, 180
young w
30 4
120
middle-aged
34 60
90 time,
120 mln
150
180
0
30
60
90 time,
120
150
180
min
2. T,,, T,, and iTSk responses of Y and MA men to experimental protocol in hydrated and hypohydrated states. Values are means k SE of 7 subjects in each group (6 for MA subjects in hydrated condition). TSk of Y subjects is significantly higher in hypohydrated condition. *‘P < 0.05 between age groups.
I
FIG.
0
,
exer 30
I 60
I 90 time,
I 120
I 150
I 180
0
min
3. FBF, MAP, and FVR of Y and MA challenge. *P < 0.05 between age groups. FIG.
30
,
!
60
90 time,
men during
I
exer
120
, 150
, 180
mln
the 3-h heat
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1906 TABLE
FBF:
(Minute
H
HR, beats/min Y MA FBF, ml 100 Y MA MAP, mmHg Y MA FVR, mmHg Y MA SBP, mmHg Y MA DBP, mmHg Y MA %APV Y MA are means
0)
After
HYPOHYDRATION
90 Min
Passive
Heating
H
HYPO
69k2 58k3 ml-’ min-l 4.06t0.50 3.132056
l
TABLE
AND
3. Mean cardiovascular responsesto passive heating and exercise in the heat in Y and MA men Rest
Values
AGE
72k4 61t3
76t3 65t7
5.02t0.81 3.88t0.61
After
Exercise
H
HYPO
HYPO
7822 6523
135zk8 128t9
149k6 135t6
6.1Ok1.40
6.84t1.29 6.80t0.80
17.58t2.00 10.37k2.50”
14.59t2.07 7.32t1.18*
86k4 9o,t2
84t3 90t3
88k-2 8723
82t2 100+5-t
84k3 99*4*
2024 27k4
lltl
17t3
16-el 13&l
5*0 12k3$
11424 116t3
llOt3 121t4
11823 119k5
72k4 77t2
71t4 75t3
74rt3 72t3
-1.7k1.5 +0.2*1.0
-1.5kO.9 -1.5kO.9
l
l
88t3 90t3 100 ml 24,t3 35t6
min
l
l
ml-’
11222 116t2 77-e4 81t3
t SE. Heating
7.34t0.90
at 48”C,
15% relative
humidity.
*
6kl 16+2$
163k6 167kll
151t8 17226
42t5 66t3-f
50t5 66k3.t
-5.9t0.7 -9.4+0.6t
P < 0.05, t P < 0.01, $ P c 0.001 between
-9.5tl.O -10.4kl.O age groups.
4. Fluid consumption, urine output, weight change, and calculated sweating rate for Y and MA men H
&PO
Y
Water consumed before test, ml Water consumed during final hour, ml Urine output, ml Total weight change, kg Average sweating rate, g rns2 h-l l
Values
30 Min
are means
l
t, SE. * Significantly
MA
2,104&109 394*152
1,893+110 417*103
1,096+127 0.78kO.26 120t14 different
from
843t78 0.77kO.30 133*15 corresponding
and hemoglobin at minute 90 as a reference. During exercise (i.e., minutes 90-120), the decrease in PV was significantly less in the Y subjects (P C 0.01) in this condition. When hypohydrated, no age differences were present with respect to %APV. As previously described, k was calculated for each subject at the end of exercise from SkBF (estimated from FBF) and (T,, - ?Jk). In the H condition, k averaged 320 -+ 15 W/m” for the Y and 301 & 36 W/m” for the MA group; in the Hypo condition, k was 178 t 11 W/m” for the Y and 148 t 12 W/m” for the MA group. Within each age group, k was significantly less as a result of hypohydration (P < O.OOl), but no age differences were seen. Table 4 presents fluid volumes and overall (average for the 3 h) sweating rates for each age group by hydration state. No significant age differences were seen in weight lost over the 3 h or water consumed during the final test hour, although as expected, significantly more water was consumed in the Hypo condition. Urine output (minutes 60-90 for the H condition) averaged 1,096 t 127 ml for the Y and 843 t 78 ml for the MA group. Water balance (water in - total fluid out) was similar for each age group and each hydration state.
Y
MA
200* 1,375_+183*
200* 1,304_+94*
0* 0.59t0.20 117k12
0* 0.63t0.14 112k6
H value. DISCUSSION
We previously reported a diminished active vasodilation in older men during exercise in warm environments (12, 22). Because 1) hyperosmolality has been shown to cause similar reductions in FBF (5) independent of age and 2) older men and women may be predisposed to hyperosmolar hypohydration because of reduced thirst sensation (l7), we believed it prudent to reexamine the peripheral vascular response after better controlling drinking by the subjects. Therefore, in the present investigation we used a preexposure period of water loading to ensure adequate hydration in all subjects (H condition). Had we not done this, differences in initial hydration state (due to prior drinking, exercise, food intake, etc.) may have biased the results and precluded a true comparison with the hypohydrated condition. Drinking even large volumes of distilled water does not hyperhydrate humans (20), because the absorption and passage of the water through the various fluid compartments is rapid. The return of plasma osmolality and PV back to predrinking levels before exercise began and the large urine volumes collected made this evident. Age differences in urine osmolality, although not statistically significant, are similar to those published by Phillips et al. (17) and are significantly (P < 0.001) lower after drinking
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FBF:
AGE
AND
in both groups, which demonstrates the increased excretion of free water. In contrast, we also tested the subjects in a state of hyperosmolar hypohydration caused by 18 h of water deprivation (Hypo condition). The major finding was that age and hypohydration independently reduce the FBF response to exercise i.n a hot envi .ronment. Thus the contention that aging Per se has a role in the limited vasodilation under these conditions (12) is further supported. Another factor that may potentially limit the ability to increase blood flow to the skin is a low arterial (i.e., driving) pressure. In this study, the MA subjects maintained a higher MAP during the period in which FBF was lower, so driving pressure does not appear to be a limiting factor. A more likely explanation may lie in structural alterations in the skin vasculature, although alterations in adrenergic control or sensitivity of the skin arterioles remain possibilities. When body temperature rises, heat must be conducted from the core to the skin for dissipation. To facilitate this transfer of heat, SkBF increases via increased carof flow away from diac output and a redistribution spla nchnic vascular beds. The rate of heat transfer depends not only on SkBF but also on (T,, - Tsk) (7). In the present investigation, the Y men had a significantly higher FBF (and presumably SkBF), but they also maintained a higher Tsk and thus a lower (T,, - TJ. In the MA subjects, the higher thermal gradient between core and skin allowed for a similar k at a lower FBF. As a result, k was not significantly different between the two age groups. This accounts for the similar core temperature responses in light of the vastly different FBF values under conditions where evaporative cooling is similar between groups (evidenced by the similar body weight changes). In the Hypo condition, both FBF and (T,, - Tsk) were lower for each group, which led to a significantly lower (P < 0.001) k and a higher T,, response. The T, overshoot after cessation of exercise, seen on 1Y in the Y subjects, was an unexpected occurrence. D uring this time, FBF is still relatively higher in the Y subjects. It is possible that the Y subjects have less heat transfer away from the core during this time because FBF is dropping but Tsk remains elevated. The MA men, on the other hand, maintain their higher (T,, - Tgk) and are therefore able to move heat to the skin. Because we did not simultaneously monitor T,, during the recovery period, we have no way of knowing whether the sustained increase in T re reflects a transient increase in heat storage or an enhanced pooling of blood in the lower body. This hypothesis depends on similar heat transfer via other avenues, the greatest of which is evaporative heat loss. We assumed from the change in body weight that evaporative losses were similar through the entire 3 h; however, we have no intermediate weights or direct sweating measurements to further document this. Because ambient water vapor pressure was low, evaporative cooling was presumably high and skin wettedness was low. Further investigation into this seemingly different method of heat transfer between age groups is warranted. The lower hemoconcentration during exercise (i.e., a
HYPOHYDRATION
1907
smaller %APV) in the Y men in the H condition supports earlier findings from our laboratory. In a warm humid environment, older women lost more PV during a Z-h exercise session than did matched younger women (13). Meischer and Fortney (15) have also demonstrated a relatively larger decrease in PV in older men in a resting heat study. In the present investigation, no age differences were seen in the Hypo condition, which perhaps suggests that adequate hydration allows for less lability in PV in younger but not older subjects. The mechanisms behind this phenomenon are not clear and also deserve further study. One possibility is the greater hydrostatic pressure coupled with a lower oncotic pressure (resulting from the lower protein concentration). Differences in core temperature between older and younger subjects during a heat challenge depend on how well subjects are matched and on acclimation state. For example, when no attempt is made to match subjects on the basis of VOW,,,, older men respond to passive heating (4, 21) and exercise in the heat (24) with a greater elevation in Tes. However, these results could be explained solely on the basis of differences in cardiorespiratory capacity. Exercise studies compound the problem, because heat production is a function of absolute exercise intensity but Te, is a function of relative (i.e., Av02 max) intensity (4). When older and younger subjects are matched for Vo2max but are not experimentally acclimated, the older subjects are typically more active. This higher level of chronic activity may serve to partially acclimate the subjects, as illustrated nicely by the data of Pandolf et al. (16), where before acclimation, a group of 46-yr-old men maintained lower core temperatures than a group of VO 2,,,-matched Zl-yr-old men (differences disappeared with acclimation). In such paradigms (12) it is common for no age difference to be seen in core temperature response. Such is the case in the present study, where VO 2maxwas similar among subjects and no acclimation was performed. Conversely, when VOzrnax is similar and all subjects are rigorously heat acclimated, younger women respond to exercise in hot environments with lower core temperatures than their older counterparts (13). The picture may be further clouded by the effects of regular physical activity on PV. If the MA men tested in the present study were more active on a regular basis, initial PV may have been greater, although we did not measure absolute PV. This would argue even more against their lower FBF responses being secondary to availability of intravascular volume and in favor of a diminished response, the basis of which is within the arteriolar wall. However, it should be repeated that the sample of active MA men tested in this study is not representative of that overall population in terms of aerobic capacity. We previously reported a decreased FBF response of older men to short-term (22) and longer (12) periods of exercise in warm environments. Sagawa and colleagues (21) found similar decrements during passive heating. These findings are contrary to the higher FBFs of older men reported by Hellon and Lind (8). However, some of their “older” men were as young as 41 yr of age, and no
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1908
FBF:
AGE
AND
attempts were made to match or acclimate subjects. Furthermore, we previously reported (12) that plotting FBF vs. T,, yielded lower slopes for the older subjects with no difference in threshold of this effector response. However, no consideration was given to hydration status in that study. In summary, the attenuated FBF response to exercise during heat stress of fit MA men does not appear to be caused by hyperosmolar hypohydration or a lower driving pressure. Rather, it may be due to structural changes within the cutaneous vascular network. In this hot dry environment, the MA men managed an equivalent rate of heat conductance to the skin in the presence of lower SkBF by maintenance of a higher (T,, - TSk). The authors acknowledge the technical assistance of Marlin Druckenmiller, Fred Weyandt, and Tim Benner. The assistance of Joseph L. Loomis was greatly appreciated. This study was supported by National Institutes of Aging Grant
HYPOHYDRATION
vasodilatation 9.
Address for reprint requests: W. L. Kenney, Laboratory for Human Performance Research, 119 No11 Laboratory, Pennsylvania State University, University Park, PA 16802.
14.
15.
17.
Received 5 July 1989; accepted in final form 13 December 1989. REFERENCES
1Sl I”.
D. A., W. E. GLOVER, AND I. C. RODDIE. Vasomotor responses in the human arm during leg exercise. Circ. Res. 9: 264-
1. BLAIR,
271, 1961. 2. DETRY, J.
M., G. L. BRENGELMANN, L. B. ROWELL, AND C. WYSS. Skin and muscle components of forearm blood flow in directly heated resting man. J. Appl. Physiol. 32: 506-511, 1972. 3. DILL, D. B., AND D. L. COSTILL. Calculation of percentage changes in volumes of blood, plasma, and red blood cells in dehydration. J. Appl. Physiol. 37: 247-248, 1974. 4. DRINKWATER, B. L., AND S. M. HORVATH. aging. Med. Sci. Sports 2: 49-55, 1979. 5. FORTNEY, S. M., C. B. WENGER, J. R. BOVE,
Heat tolerance and
AND E. R. NADEL. Effect of hyperosmolality on control of blood flow and sweating. J.
Appl. Physiol. 57: 1688-1695, 1984. 6. Fox, R. H., AND 0. G. EDHOLM. Nervous control of the cutaneous circulation. Br. Med. Bull. 19: 110-114, 1963. 7. GISOLFI, C. V., AND C. B. WENGER. Temperature regulation during exercise: old concepts, new ideas. In: Exercise and Sport Sciences Reviews, edited by R. L. Terjung. Lexington, MA: Heath, 1984, vol.
12, p. 339-372. R. F., AND A. R. LIND. The influence of age on peripheral
8. HELLON,
J. Physiol.
Lond.
141: 262-
R. F., A. R. LIND, AND J. S. WEINER. The physiological reactions of men of two age groups to a hot environment. J. Physiol.
Lond. 133: 118-131,1956. J. M., G. L. BRENGELMANN, J. R. S. HALES, P. M. 10. JOHNSON, VANHOUTTE, AND C. B. WENGER. Regulation of the cutaneous circulation. Federation Proc. 45: 2841-2850, 1986. 11. JOHNSON, J. M., AND L. B. ROWELL. Forearm skin and muscle vascular responses to prolonged leg exercise. J. AppZ. Physiol. 39: 920-924,1975. 12. KENNEY, W. L. Control of heat-induced cutaneous vasodilatation in relation to age. Eur. J. Appl. Physiol. Occup. Physiol. 57: 120125, 1988. 13. KENNEY, W. L., AND R. K. ANDERSON. Responses of older and
16.
R29-AG-07004-02.
in a hot environment.
272, 1958. HELLON,
1g ’ 2.
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younger women to exercise in dry and humid heat without fluid replacement. Med. Sci. Sports Exercise 20: 155-160, 1988. KOROXENIDIS, G. T., J. T. SHEPHERD, AND R. J. MARSHALL. Cardiovascular response to acute heat stress. J. Appl. Physiol. 16: 869-872,1961. MEISCHER, E., AND S. M. FORTNEY. Effect of age on thermal and plasma volume responses to dehydration and rehydration in a hot dry environment (Abstract). Federation Proc. 46: 323, 1987. PANDOLF, K. B., B. S. CADERETTE, M. N. SAWKA, A. J. YOUNG, R. P. FRANCESCONI, AND R. R. GONZALEZ. Thermoregulatory responses of middle-aged and young men during dry-heat acclimation. J. Appl. Physiol. 65: 65-71, 1988. PHILLIPS, P. A., B. J. ROLLS, J. G. G. LEDINGHAM, M. L. FORSLING, J. J. MORTON, M. J. CROWE, AND L. WOLLNER. Reduced thirst after water deprivation in healthy elderly men. N. Engl. J. Med. 311: 753-759,1984. PICKERING, G. W. The peripheral resistance in persistent arterial hypertension. Clin. Sci. Lond. 2: 209-235, 1936. RAMANATHAN, N. L. A new weighting system for mean surface temperature of the human body. J. Appl. Physiol. 19: 531-533, 1964. RIEDESEL, M. L., D. Y. ALLEN, G. T. PEAKE, AND K. AL-QATTAN. Hyperhydration with glycerol solutions. J. Appl. Physiol. 63: 22622268,1987.
21. SAGAWA, S., K. SHIRAKI, M. K. YOUSEF, AND K. MIKI. Sweating and cardiovascular responses of aged men to heat exposure. J. GerontoZ.
43: Ml-M8,
1988.
22, TANKERSLEY, C. G., J. SMOLANDER, AND S. M. FORTNEY. Skin blood flow responses in young and older men during exercise in the heat (Abstract). Federation Proc. 46: 1440, 1987. 23. THORNTON, R. M., AND D. W. PROPPE. Attenuation of hindlimb vasodilation in heat-stressed baboons during dehydration. Am. J. 24.
Physiol. 250 (Regulatory Integrative Comp. Physiol. 19): R30-R35, 1986. WAGNER, J. A., S. ROBINSON, S. P. TZANKOFF, AND R. P. MARINO.
Heat tolerance and acclimatization to work in the heat in relation to age. J. Appl. Physiol. 33: 616-622, 1972. 25. WHITNEY, R. J. The measurement of volume changes in human limbs. J. Physiol. Lond. 121: l-27, 1953.
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the
W. L. KENNEY, C. G. TANKERSLEY, D. L. NEWSWANGER, D. E. HYDE, S. M. PUHL, AND N. L. TURNER Laboratory for Human Performance Research, Pennsylvania State University, University Park, Pennsylvania 16802
KENNEY, W. L., C. G. TANKERSLEY, D. L. NEWSWANGER, D. E. HYDE, S. M. PUHL, AND N. L. TURNER. Age and hypohydration independently influence the peripheral vascular response to heat stress. J. Appl. Physiol. 68(5): 1902-1908,1990.-Seven
young (Y, 22-28 yr) and seven middle-aged (MA, 49-60 yr) normotensive men of similar body size, fatness, and maximal oxygen uptake (Vozmax) were exposedto a heat challenge in an environmental chamber (48°C 15% relative humidity). Tests were performed in two hydration states: hydrated (H, 25 ml water/kg body wt 1 h before the test, 2.5 h before exercise)and hypohydrated (Hypo, after 18-20 h of water deprivation). Each test began with a 90-min rest period during which the transiently increasedplasmavolume and decreasedosmolality after drinking in the H condition returned to baseline. This period was followed by 30 min of cycle exerciseat a meanintensity of 43% Vozmax and a 60-min resting recovery period with water ad libitum. Although prior drinking caused no sustained changesin plasmaosmolality, Hypo increasedplasmaosmolality by 7-10 mosmol/kg in both groups. There were no significant agedifferencesin water intake, urine output or osmolality, overall changein body weight, or sweatingrate. In the H state, the percent changein plasmavolume wasless(P < 0.01) during exercisefor the Y group (-5.9 & 0.7%) than for the MA group (-9.4 t 0.6%). Esophagealtemperature (T,,) was higher in the Hypo condition for both groupswith no age-relateddifferences. Throughout the 3-h period, mean skin temperature washigher in the Y group and significantly so (P < 0.05) in the Hypo condition. During exercise, forearm blood flow (FBF) was significantly (i.e., 50-60%) lower and mean arterial pressurewas significantly (15-20 mmHg) higher in the MA group in both hydration states, yielding an elevated forearm vascular resistance compared with the Y group. Furthermore, there was no interaction betweenageand hydration state in theseperipheral vascular responses.Estimated core-to-skin heat conductance was-50% lower in the Hypo condition but wasnot significantly different between agegroupsbecausethe higher FBF of the Y group offset their lower core-to-skin temperature gradient (thus accounting for the similar AT,, in both age groups). It was concludedthat age-relatedalterations in the peripheral circulation limit vasodilation and maintain higher arterial pressures during exercisein a warm environment. These differences are not a function of age-related differences in cardiorespiratory fitness or hydration state but appear to be a primary consequenceof the aging process. aging; skin blood flow; blood pressure;temperature regulation; body temperature; peripheral vascular resistance
is elevated, heat is typically conducted from the core to the skin for subsequent WHEN BODY TEMPERATURE 1902
via dry and evaporative heat loss. Conduction of this heat load is a function of both skin blood flow (SkBF) and the thermal gradient between core and skin (7). The ability to measure whole body SkBF in human subjects is limited, so changes in forearm blood flow (FBF) are commonly measured because increases in FBF during passive heating (2) and prolonged dynamic leg exercise in the heat (1, 11) are confined to the forearm skin. Furthermore, neurogenic control of forearm SkBF is reported to reflect that of SkBF to most of the body surface (6), and increases in forearm SkBF appear to reflect increases in whole-body SkBF in pattern and magnitude (14). Although control and magnitude of FBF under heat stress conditions has been well studied in young subjects, only recently has the role of aging in this response been given much attention. In 1936, Pickering (18) showed an attenuated hand blood flow response to body heating in older subjects, yet in the 1950’s, Hellon et al. (8,9) published contradictory results. This latter group of researchers showed that under hot conditions, FBF of men 45 yr of age was double that of men 25 yr of age (8). However, the subjects used were not well described with respect to cardiovascular fitness, activity level, body size, or acclimation state (8, 9). In the past decade, we (12, 22) and others (21) have shown that FBF is lower in older subjects at rest or during exercise in warm environments compared with younger subjects. Evidence suggests that older men and women are prone to hyperosmolar hypohydration (17). This may result from a decreased thirst sensitivity and/or a limited ability of the kidneys to concentrate urine, which might lead to enhanced free water excretion (17). Hyperosmolality secondary to water deprivation or diuretic use has been shown to decrease SkBF in baboons (23) and in humans (5). Therefore, the purpose of this investigation was to further examine the FBF response of young vs. middleaged men under conditions of adequate hydration and after water deprivation to better understand the role of aging in thermoregulatory responses. Because not controlling for prior drinking behavior leaves doubt as to just what fluid state “euhydration” signifies, we prehydrated our subjects with a volume of water equal to 2.5% of body weight before the experimental session. Because prehydration immediately bedissipation to the environment
0161-7567/90 $1.50 Copyright 0 1990 the American Physiological Society
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FBF:
AGE
AND
fore exercise may alter thermoregulatory responses because of an expansion of plasma volume, the subjects sat at rest in the environmental chamber for an additional 90 min (for a total of 2.5 h) before exercising. Without the use of a plasma expander (e.g., glycerol, albumin, dextran) “hyperhydration of an individual by ingesting large volumes of fluid before a stressful work environment [is not] possible” (21). Therefore, we tested subjects in a state of controlled hydration (not hyperhydration, because the fluid was not retained in the vascular space) and in a state of hypohydration to best compare relative effects of hypohydration in these two distinct age groups. METHODS
Subjects. Seven middle-aged (MA) and seven young (Y) men were recruited to serve as subjects for this investigation. The MA group ranged in age from 49-60 yr and the Y group from 22-28 yr. All subjects were regular exercisers, although the MA group could subjectively be characterized as more aerobically active on a regular basis; it included two competitive masters-level runners. The investigation took place between the months of September and March, and no effort was made to acclimate the subjects to heat. Before participation, verbal and written informed consents were procured from all subjects, and each subject was examined by a physician. This preliminary screening included a resting 12lead electrocardiogram, hydrodensitometric measurement of body composition, and a maximal graded exercise test on a motor-driven treadmill by use of a modified Balke protocol. None of the subjects smoked, and all were normotensive. Mean subject characteristics are presented in Table 1. Protocol. The test consisted of 3 h in an environmental chamber set at a dry-bulb (and globe) temperature of 48°C and a wet-bulb temperature of 25°C (15% relative humidity). There was no forced air movement; average air velocity was ~0.4 m/s. Subjects were clothed in shorts, cotton socks, and running shoes, and they sat throughout the test in a reclining mesh seat affixed to a cycle ergometer. Before entering the chamber, each subject was weighed nude and seated in a wheelchair for the next 30 min to minimize postural influences. Subjects were again weighed nude after the experiment. Hydration state was manipulated in randomized order before the tests. On one test day, the subject was given cool (ll-12°C) water (25 ml/kg body wt) to drink during the hour before entering the chamber. This was denoted the hydrated (H) condition; it ensured that subjects were fully hydrated, rather than hyperhydrated. This volume of water ingestion transiently increased plasma volume
1903
HYPOHYDRATION
(PV) and decreased plasma osmolality. Base-line PV and osmolality were restored by the end of the initial 90-min rest period (Fig. 1, Table 2). Furthermore, water intake minus urine output was not significantly different between H and hypohydrated (Hypo) conditions. Mean urine specific gravity remained X.010 for both groups after drinking. The other test was performed after an 18-h period of water deprivation (Hypo). For these tests, the subject consumed no liquids after 1500 h on the previous day but was allowed to eat food from a list of lowwater (~75%) foods. The only exception to this was the drinking of a small (200-ml) volume of water while the esophageal thermocouple was inserted. This procedure changed preexposure body weight by -2% and caused a sustained increase in mean plasma osmolality of 7-10 mosmols/kg. One MA subject completed only the Hypo test for reasons not significant to the study, but the statistical analysis employed allowed inclusion of his data for that condition after verification that addition of these data did not qualitatively alter the results. For the initial 90 min, the subject sat at rest on the ergometer. For the H tests, urine was collected and volume was measured at minutes 60 and 90. This 90-min period of passive heating was followed by 30 min of dynamic leg exercise at an average intensity of 43% of previously measured treadmill maximal oxygen uptake (VOW,,,). Although this may represent a high VOWrelative to peak cycle Ooz, it was believed that a similar relative intensity (as well as absolute intensity) was maintained across both groups. The final 60 min were spent at rest A 10
-1
rest, no water
contrd
-20
’
-30
I 30
0
B
8x81.
-
I ’ I 60 90 Time (mln)
rest, water
-
I 150
120
’ 180
Hypohydrated
1. Subject characteristics
TABLE
Age, Mb, Yr
%Fat
kg
&/Mb, m2/k
VO
ml - kg-’ - min-’
2
max
l/min
cant rol
-20
Y MA
Hydrated
24&l 54&2*
Values condition). value.
77&4 69k4
are means k&, body
16t2 19t2
0.025&0.001 0.026*0.001
50.3t1.2 47.8t3.7
3X5&0.24 3.24t0.14*
t SE; n. = 7 men per group (6 MA men in the H mass; AD, DuBois surface area. * P c 0.05 from Y
exer.
rest, no water
rest, water .
-
-30
I
0
n
1
30
-
I
r
!
60 90 Time (mln)
,
.
-
120
150
180
FIG. 1. Percent change in plasma volume as a function of time for Y and MA men in each hydration state. Open symbols, MA subjects; closed symbols, Y subjects. Values are means t SE.
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1904
FBF:
AGE
AND
HYPOHYDRATION
with water (11-12°C) provided ad libitum, and water consumption during the 3rd h was monitored. All tests began at 0900 h, with >l rest day between consecutive tests. Measurements. Esophageal temperature (T,,) was measured every 5 min through the first 120 min from a copper-constantan thermocouple within a sealed infant feeding catheter. Each catheter was marked at 40% of subject height and taped to the cheek at this mark to establish a uniform insertion depth. Rectal temperature (T,,) was measured every 5 min throughout the 3 h via a flexible thermistor inserted 9 cm past the anal sphincter. Mean skin temperature (Tsk) was calculated every 5 min as the weighted average of four uncovered sites: chest, upper arm, thigh, and calf (19). Heart rate was monitored continuously and recorded every 5 min from a singlelead electrocardiogram. Measured variables, chamber conditions, and pedal rpm were recorded and stored on a dedicated computer via a Keithley Series 500 data collection system. iTo was measured by the open-circuit technique at minutes 45 (rest) and 100 (exercise). FBF was measured three times within a 20-s period on entry into the chamber and every 10 min thereafter by venous occlusion plethysmography and a mercury-inSilastic strain gauge (25). The average of these three values was recorded as the FBF for that time period. The left arm was suspended away from the body just above the venostatic level, and arterial flow to the hand was occluded with a wrist tourniquet before each series of measurements. In the same arm, arterial blood pressure was measured by auscultation every 15 min. Mean arterial pressure (MAP) was calculated from systolic (SBP) and diastolic (DBP) pressures as MAP = 1/3 SBP + 2/3 DBP. Forearm vascular resistance (FVR), in units of mmHg ml-‘. 100 ml min, was calculated as the ratio of MAP to FBF. Venous samples (lo-11 ml per sample) were drawn from an antecubital vein in the contralateral arm without stasis 1 h preexposure (before drinking in the H condition), immediately on entry into the chamber, at minutes 15 and 30 and every 30 min thereafter. Urine was collected before each subject entered the chamber and at minutes 60 and 90 of the H experiments. Urine volume, osmolality, and specific gravity were determined. Percent changes in PV were determined from hematocrit (microhematocrit method) and hemoglobin (cyanmethemoglobin method) according to the method of Dill and Costill (3) with appropriate corrections for venous sampling and trapped plasma. Plasma and urine osmolality were determined by freezing-point depression by use of an osmometer (Advanced Instruments), and total protein concentration was determined by the biuret method by use of an autoanalyzer (Technicon). Plasma Na’ and K+ concentrations were determined by flame photometry (Instrument Laboratory). Overall sweating rate was determined from the change in nude weight corrected for fluid intake and output but not for respiratory water loss, which was assumed to be negligible. All provided water was carefully measured, and the volumes were recorded. To estimate core-to-skin heat conductance (k), SkBF l
l
was estimated from FBF according to the assumptions set forth by Johnson et al. (10). These assumptions include a constant skin thickness and forearm segment dimensions and a muscle blood flow of 2 ml 100 ml-‘. min? Conductance was calculated (7) in watts as k = SkBF x 64.2 (T,, - Tsk) where SkBF is in l/min, 64.2 is the specific heat of blood in We min. 1-l. ‘C--l, and (T,, - Tsk) represents the coreto-skin temperature gradient; k was then corrected for body surface area (W/m”). Statistics. Data were analyzed for age and hydration effects using multivariate analysis of variance for passive heating, exercise, and recovery periods. Subsequently, univariate analyses of variance were performed to examine age and hydration effects across time. Critical alpha level was set at 0.05. Data are presented as means t SE. RESULTS
The subject groups were well matched for body size and composition and VO zrnax relative to body weight (Table 1). Although there was no significant difference between the groups in VO 2max relative to body weight, the mean absolute VO zrnaxof the MA group was ~15% lower because of the 8-kg difference in mean weight. However, during exercise, metabolic heat production (calculated from exercise Vo2 with the assumption that 1 liter 02 = 4.9 kcal and subtraction of external work performed) was 236 t 8 (SE) W/m” for the Y group and 225 t 11 W/m” for the MA group (not significantly different). Table 2 presents plasma and urine osmolality, total protein concentration, and plasma electrolyte concentrations. These data and Fig. 1 clearly indicate that the transient increase in PV and decrease in osmolality after drinking were resolved by minute 90, i.e., before initiation TABLE 2. Plasma and urine osmolality, total plasma protein concentration, and plasma electrolyte concentrations for Y and MA men at various times during the protocol H Before drinking
After drinking
Plasma osmolality, mosmol/kg Y 281t3 276t2 MA 283t3 280t3 Total proteins, g/d1 Y 6.8&O. 1 6.7t0.2 MA 6.5~10.1 6.320.1 Na+, meq/l 139&l Y 140t2 140+2 MA 140t2 K+, meq/l Y 4.lkO.2 4.120.1 MA 4.OkO.2 4.OkO.l Urine osmolality, mosmol/kg Y 943*91 532+151 t MA 741HO5 536+102-f’
HYPO Minute
90
282t2 27922
After water deprivation
288+1p 290+2t
Minute
90
287&l? 289kZ.f
6.9&O. 1 6.3tO.l*
6.920.2 6.720.2
7.1to.1 6.6*0.1*
140,tZ 139t3
139&l 142&Z
141&Z 143&l
4.0,tO.Z 4.1t0.2
4.0,to.o 4.l_tO.l
4.2&O. 1 4.2,tO. 1
Values are means t SE. * Significantly 0.001 from before-drinking value.
995k49 868k34 lower
than
Y value;
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FBF:
AGE
AND
of exercise. The enhanced free water clearance is evidenced by the lowered urine osmolality relative to the predrinking urine sample. On the other hand, the significantly higher plasma osmolality consequent to water deprivation (compared with the before-drinking samples) was sustained throughout the 90-min rest period before exercise. Total plasma proteins were 3-7% lower (P < 0.05) for the MA group throughout the session for both conditions. There were no significant age or hydration differences in plasma Na+ or K+ concentration. Figure 2 shows the mean T,,, T,,, and T,k responses for the Y and MA subjects. T,, was artificially low in the H condition (because of the cool water consumed before the subjects entered the chamber) at time 0, but it plateaued late in the passive heating phase of the protocol. If this transient is excluded, T,, at minutes 30-90 (rest) and at minutes 90-120 (exercise) was significantly higher in the Hypo condition (P < 0.05) in both age groups. There were no significant differences in T,, caused by age. T,k was higher in the Y subjects in both hydration states but significantly higher only in the Hypo condition. Although the esophageal thermocouple was extracted after minute 120 to allow drinking, we continued to monitor T,, throughout the 3 h (Fig. 2). At the end of exercise, the T,, of the Y group continued to increase and remained above the end-exercise value for the next 20-30 min. The overshoot seen in the Y group was greater than that seen in the MA group, causing a significant (P A 39
Hypohydrated
Hydrated
39
1
38
38
1905
HYPOHYDRATION
< 0.05) age effect across hydration
states at minutes DO-
180.
Cardiovascular responses are presented in Fig. 3 and Table 3. Overall, heart rate was significantly lower for the MA subjects; however, the increase from rest to exercise was similar for both groups. When heart rate was expressed as a percentage of maximal heart rate obtained during the maximal graded exercise test, no significant age differences were seen. During exercise, but not during the preexercise rest period, the FBF of the Y group was significantly higher (P < 0.05) and the MAP was significantly lower (P c 0.01) than those of their older counterparts in both hydration states. Exercise FBF at minute 120 was significantly lower (P c 0.05) in the Hypo state for all subjects. Although there were independent effects of age and hypohydration on FBF during the exercise period, there was no statistical interaction between age and hydration state in the FBF response. In the Hypo condition, the significantly higher FBF of the Y group lasted 20 min after exercise had ceased (Fig. 3). As presented in Table 3, the lower exercise MAP of the Y group was primarily the result of a greater reduction (P c 0.01) in DBP, although SBP was also slightly lower in the Y than in the MA group (not significant). As a result of the higher pressure-lower flow of the MA group during the exercise bout, calculated FVR was -150% greater (P < 0.001) in this group than in the Y group. Changes in PV (% APV) during the exercise bout are also shown in Table 3. When water loaded, an early hemodilution was noted (see Fig. 1) followed by a return to near base-line values by the end of the resting phase. % APV during exercise was calculated using hematocrit B 20
Hypohydrated
1
36
36
1 0x81 35 0
30
60
90
120
150
0
180
I 30
I 60
I 90
I 120
I 150
I 180
0, 0
, 30
, 60
, 90
, 120
, 150
, 180
0
30
0
30
60
90
120
150
180
38
38
2
E
36
36 0
30
90
60
120
150
I
I 90
180
I 120
I 150
I 180
100
100
90
90
80
80
.
$
, 0
38
middle-aged
”
30
60
90
120
150
180
I, ! , exer
90
-
36
36
, 60
150
, 180
young w
30 4
120
middle-aged
34 60
90 time,
120 mln
150
180
0
30
60
90 time,
120
150
180
min
2. T,,, T,, and iTSk responses of Y and MA men to experimental protocol in hydrated and hypohydrated states. Values are means k SE of 7 subjects in each group (6 for MA subjects in hydrated condition). TSk of Y subjects is significantly higher in hypohydrated condition. *‘P < 0.05 between age groups.
I
FIG.
0
,
exer 30
I 60
I 90 time,
I 120
I 150
I 180
0
min
3. FBF, MAP, and FVR of Y and MA challenge. *P < 0.05 between age groups. FIG.
30
,
!
60
90 time,
men during
I
exer
120
, 150
, 180
mln
the 3-h heat
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1906 TABLE
FBF:
(Minute
H
HR, beats/min Y MA FBF, ml 100 Y MA MAP, mmHg Y MA FVR, mmHg Y MA SBP, mmHg Y MA DBP, mmHg Y MA %APV Y MA are means
0)
After
HYPOHYDRATION
90 Min
Passive
Heating
H
HYPO
69k2 58k3 ml-’ min-l 4.06t0.50 3.132056
l
TABLE
AND
3. Mean cardiovascular responsesto passive heating and exercise in the heat in Y and MA men Rest
Values
AGE
72k4 61t3
76t3 65t7
5.02t0.81 3.88t0.61
After
Exercise
H
HYPO
HYPO
7822 6523
135zk8 128t9
149k6 135t6
6.1Ok1.40
6.84t1.29 6.80t0.80
17.58t2.00 10.37k2.50”
14.59t2.07 7.32t1.18*
86k4 9o,t2
84t3 90t3
88k-2 8723
82t2 100+5-t
84k3 99*4*
2024 27k4
lltl
17t3
16-el 13&l
5*0 12k3$
11424 116t3
llOt3 121t4
11823 119k5
72k4 77t2
71t4 75t3
74rt3 72t3
-1.7k1.5 +0.2*1.0
-1.5kO.9 -1.5kO.9
l
l
88t3 90t3 100 ml 24,t3 35t6
min
l
l
ml-’
11222 116t2 77-e4 81t3
t SE. Heating
7.34t0.90
at 48”C,
15% relative
humidity.
*
6kl 16+2$
163k6 167kll
151t8 17226
42t5 66t3-f
50t5 66k3.t
-5.9t0.7 -9.4+0.6t
P < 0.05, t P < 0.01, $ P c 0.001 between
-9.5tl.O -10.4kl.O age groups.
4. Fluid consumption, urine output, weight change, and calculated sweating rate for Y and MA men H
&PO
Y
Water consumed before test, ml Water consumed during final hour, ml Urine output, ml Total weight change, kg Average sweating rate, g rns2 h-l l
Values
30 Min
are means
l
t, SE. * Significantly
MA
2,104&109 394*152
1,893+110 417*103
1,096+127 0.78kO.26 120t14 different
from
843t78 0.77kO.30 133*15 corresponding
and hemoglobin at minute 90 as a reference. During exercise (i.e., minutes 90-120), the decrease in PV was significantly less in the Y subjects (P C 0.01) in this condition. When hypohydrated, no age differences were present with respect to %APV. As previously described, k was calculated for each subject at the end of exercise from SkBF (estimated from FBF) and (T,, - ?Jk). In the H condition, k averaged 320 -+ 15 W/m” for the Y and 301 & 36 W/m” for the MA group; in the Hypo condition, k was 178 t 11 W/m” for the Y and 148 t 12 W/m” for the MA group. Within each age group, k was significantly less as a result of hypohydration (P < O.OOl), but no age differences were seen. Table 4 presents fluid volumes and overall (average for the 3 h) sweating rates for each age group by hydration state. No significant age differences were seen in weight lost over the 3 h or water consumed during the final test hour, although as expected, significantly more water was consumed in the Hypo condition. Urine output (minutes 60-90 for the H condition) averaged 1,096 t 127 ml for the Y and 843 t 78 ml for the MA group. Water balance (water in - total fluid out) was similar for each age group and each hydration state.
Y
MA
200* 1,375_+183*
200* 1,304_+94*
0* 0.59t0.20 117k12
0* 0.63t0.14 112k6
H value. DISCUSSION
We previously reported a diminished active vasodilation in older men during exercise in warm environments (12, 22). Because 1) hyperosmolality has been shown to cause similar reductions in FBF (5) independent of age and 2) older men and women may be predisposed to hyperosmolar hypohydration because of reduced thirst sensation (l7), we believed it prudent to reexamine the peripheral vascular response after better controlling drinking by the subjects. Therefore, in the present investigation we used a preexposure period of water loading to ensure adequate hydration in all subjects (H condition). Had we not done this, differences in initial hydration state (due to prior drinking, exercise, food intake, etc.) may have biased the results and precluded a true comparison with the hypohydrated condition. Drinking even large volumes of distilled water does not hyperhydrate humans (20), because the absorption and passage of the water through the various fluid compartments is rapid. The return of plasma osmolality and PV back to predrinking levels before exercise began and the large urine volumes collected made this evident. Age differences in urine osmolality, although not statistically significant, are similar to those published by Phillips et al. (17) and are significantly (P < 0.001) lower after drinking
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FBF:
AGE
AND
in both groups, which demonstrates the increased excretion of free water. In contrast, we also tested the subjects in a state of hyperosmolar hypohydration caused by 18 h of water deprivation (Hypo condition). The major finding was that age and hypohydration independently reduce the FBF response to exercise i.n a hot envi .ronment. Thus the contention that aging Per se has a role in the limited vasodilation under these conditions (12) is further supported. Another factor that may potentially limit the ability to increase blood flow to the skin is a low arterial (i.e., driving) pressure. In this study, the MA subjects maintained a higher MAP during the period in which FBF was lower, so driving pressure does not appear to be a limiting factor. A more likely explanation may lie in structural alterations in the skin vasculature, although alterations in adrenergic control or sensitivity of the skin arterioles remain possibilities. When body temperature rises, heat must be conducted from the core to the skin for dissipation. To facilitate this transfer of heat, SkBF increases via increased carof flow away from diac output and a redistribution spla nchnic vascular beds. The rate of heat transfer depends not only on SkBF but also on (T,, - Tsk) (7). In the present investigation, the Y men had a significantly higher FBF (and presumably SkBF), but they also maintained a higher Tsk and thus a lower (T,, - TJ. In the MA subjects, the higher thermal gradient between core and skin allowed for a similar k at a lower FBF. As a result, k was not significantly different between the two age groups. This accounts for the similar core temperature responses in light of the vastly different FBF values under conditions where evaporative cooling is similar between groups (evidenced by the similar body weight changes). In the Hypo condition, both FBF and (T,, - Tsk) were lower for each group, which led to a significantly lower (P < 0.001) k and a higher T,, response. The T, overshoot after cessation of exercise, seen on 1Y in the Y subjects, was an unexpected occurrence. D uring this time, FBF is still relatively higher in the Y subjects. It is possible that the Y subjects have less heat transfer away from the core during this time because FBF is dropping but Tsk remains elevated. The MA men, on the other hand, maintain their higher (T,, - Tgk) and are therefore able to move heat to the skin. Because we did not simultaneously monitor T,, during the recovery period, we have no way of knowing whether the sustained increase in T re reflects a transient increase in heat storage or an enhanced pooling of blood in the lower body. This hypothesis depends on similar heat transfer via other avenues, the greatest of which is evaporative heat loss. We assumed from the change in body weight that evaporative losses were similar through the entire 3 h; however, we have no intermediate weights or direct sweating measurements to further document this. Because ambient water vapor pressure was low, evaporative cooling was presumably high and skin wettedness was low. Further investigation into this seemingly different method of heat transfer between age groups is warranted. The lower hemoconcentration during exercise (i.e., a
HYPOHYDRATION
1907
smaller %APV) in the Y men in the H condition supports earlier findings from our laboratory. In a warm humid environment, older women lost more PV during a Z-h exercise session than did matched younger women (13). Meischer and Fortney (15) have also demonstrated a relatively larger decrease in PV in older men in a resting heat study. In the present investigation, no age differences were seen in the Hypo condition, which perhaps suggests that adequate hydration allows for less lability in PV in younger but not older subjects. The mechanisms behind this phenomenon are not clear and also deserve further study. One possibility is the greater hydrostatic pressure coupled with a lower oncotic pressure (resulting from the lower protein concentration). Differences in core temperature between older and younger subjects during a heat challenge depend on how well subjects are matched and on acclimation state. For example, when no attempt is made to match subjects on the basis of VOW,,,, older men respond to passive heating (4, 21) and exercise in the heat (24) with a greater elevation in Tes. However, these results could be explained solely on the basis of differences in cardiorespiratory capacity. Exercise studies compound the problem, because heat production is a function of absolute exercise intensity but Te, is a function of relative (i.e., Av02 max) intensity (4). When older and younger subjects are matched for Vo2max but are not experimentally acclimated, the older subjects are typically more active. This higher level of chronic activity may serve to partially acclimate the subjects, as illustrated nicely by the data of Pandolf et al. (16), where before acclimation, a group of 46-yr-old men maintained lower core temperatures than a group of VO 2,,,-matched Zl-yr-old men (differences disappeared with acclimation). In such paradigms (12) it is common for no age difference to be seen in core temperature response. Such is the case in the present study, where VO 2maxwas similar among subjects and no acclimation was performed. Conversely, when VOzrnax is similar and all subjects are rigorously heat acclimated, younger women respond to exercise in hot environments with lower core temperatures than their older counterparts (13). The picture may be further clouded by the effects of regular physical activity on PV. If the MA men tested in the present study were more active on a regular basis, initial PV may have been greater, although we did not measure absolute PV. This would argue even more against their lower FBF responses being secondary to availability of intravascular volume and in favor of a diminished response, the basis of which is within the arteriolar wall. However, it should be repeated that the sample of active MA men tested in this study is not representative of that overall population in terms of aerobic capacity. We previously reported a decreased FBF response of older men to short-term (22) and longer (12) periods of exercise in warm environments. Sagawa and colleagues (21) found similar decrements during passive heating. These findings are contrary to the higher FBFs of older men reported by Hellon and Lind (8). However, some of their “older” men were as young as 41 yr of age, and no
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1908
FBF:
AGE
AND
attempts were made to match or acclimate subjects. Furthermore, we previously reported (12) that plotting FBF vs. T,, yielded lower slopes for the older subjects with no difference in threshold of this effector response. However, no consideration was given to hydration status in that study. In summary, the attenuated FBF response to exercise during heat stress of fit MA men does not appear to be caused by hyperosmolar hypohydration or a lower driving pressure. Rather, it may be due to structural changes within the cutaneous vascular network. In this hot dry environment, the MA men managed an equivalent rate of heat conductance to the skin in the presence of lower SkBF by maintenance of a higher (T,, - TSk). The authors acknowledge the technical assistance of Marlin Druckenmiller, Fred Weyandt, and Tim Benner. The assistance of Joseph L. Loomis was greatly appreciated. This study was supported by National Institutes of Aging Grant
HYPOHYDRATION
vasodilatation 9.
Address for reprint requests: W. L. Kenney, Laboratory for Human Performance Research, 119 No11 Laboratory, Pennsylvania State University, University Park, PA 16802.
14.
15.
17.
Received 5 July 1989; accepted in final form 13 December 1989. REFERENCES
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