Transient cutaneous vasodilatation and hypotension after drinking in dehydrated and exercising men
1 Department of Sports Medical Sciences, Institute of Aging and Adaptation, Shinshu University Graduate School of Medicine, Matsumoto 390-8621, Japan
Abstract
We examined whether oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and decreased mean arterial pressure (MAP) in exercising subjects, and assessed the effects of hypovolaemia or hyperosmolality alone on these responses. Seven young males underwent four hydration conditions. These were two normal plasma volume (PV) trials: normal plasma osmolality (Posmol, control trial) and hyperosmolality (Posmol = +11 mosmol (kg H2O)–1); and two low PV trials: isosmolality (PV = –310 ml) and hyperosmolality (PV = –345 ml; Posmol = +9 mosmol (kg H2O)–1), attained by combined treatment with furosemide (frusemide), hypertonic saline and/or 24 h water restriction. In each trial, the subjects exercised at 60% peak aerobic power for 50 min at 30°C atmospheric temperature and 50% relative humidity. When oesophageal temperature (Toes) reached a plateau after 30 min of exercise, the subjects drank 200 ml water at 37.5°C within a minute. Before drinking, forearm vascular conductance (FVC), calculated as forearm blood flow divided by MAP, was lowered by 20–40% in hypovolaemia, hyperosmolality, or both, compared with that in the control trial, despite increased Toes. After drinking, FVC increased by 20% compared with that before drinking (P < 0.05) in both hyperosmotic trials, but it was greater in normovolaemia than in hypovolaemia (P < 0.05). However, no increases occurred in either isosmotic trial. MAP fell by 4–8 mmHg in both hyperosmotic trials (P < 0.05) after drinking, but more rapidly in normovolaemia than in hypovolaemia. PV and Posmol did not change during this period. Thus, oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and reduced MAP during exercise, and this was accelerated when PV was restored.
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Introduction
It is well known that hyperosmolality and hypovolaemia induce thirst sensation and vasopressin secretion (Robertson & Athar, 1976), and also suppress thermoregulatory responses, including cutaneous vasodilatation and sweating (Nadel et al. 1980; Fortney et al. 1984; Takamata et al. 1997, 1998). Since these responses disappear after recovery of plasma volume (PV) and/or plasma osmolality (Posmol) (Montain & Coyle, 1992), baroreflex and osmosensitive mechanisms may be involved.
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On the other hand, in dehydrated subjects, it was reported that the stimulation of oropharyngeal reflexes by drinking such a small amount of water so as not to change PV and Posmol reduces thirst sensation and plasma vasopressin secretion (Geelen et al. 1984; Takamata et al. 1995a). These responses have been thought to be a feed-forward mechanism to prevent over-hydration by drinking too much water (Arnauld & du Pont, 1982; Geelen et al. 1984; Thrasher et al. 1987). On the other hand, very few studies have been conducted to examine the reflex effects of drinking on skin blood flow in dehydrated subjects exercising in a hot environment. Since skin blood flow increased during exercise much more than at rest (Rowell, 1986), oropharyngeal stimulation due to drinking would release the hyperosmotic suppression of cutaneous vasodilatation by anticipating the recovery in PV or Posmol in a feed-forward manner. In addition, if the suppression contributes to the maintenance of MAP in dehydrated and exercising subjects, as suggested in rats at rest (Nakajima et al. 1998), the release by drinking would cause a prominent fall in mean arterial pressure (MAP).
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We hypothesised that oropharyngeal stimulation due to drinking would enhance the cutaneous vasodilatation in dehydrated subjects, resulting in a fall in MAP, while PV and Posmol remained unchanged. To test these hypotheses, we measured skin blood flow and MAP after drinking in dehydrated subjects exercising in a hot environment. The reason for conducting additional experiments in hyperosmolality or hypovolaemia alone was to assess their individual effects on the suppression of cutaneous vasodilatation, its release by drinking, and the consequent fall in MAP, if they occurred.
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Methods
Subjects
Seven healthy non-smoking males were recruited for the present study. Subjects gave their written informed consent before participating in this study, which conformed to the guidelines contained in the Declaration of Helsinki, and it was approved by the Review Board on Human Experiments, Shinshu University School of Medicine. The physical characteristics of the subjects were: 22 ± 3 (S.D.) years of age, 167 ± 4 cm height, 59.3 ± 6.0 kg body weight, and 3549 ± 461 ml peak aerobic power , and 2937 ± 189 ml PV.
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Trials
The measurements were performed in four trials. These were two normal PV trials in isosmolality (control, C trial) and hyperosmolality (NPVHOS trial), and two low PV trials in isosmolality (LPVIOS trial) and hyperosmolality (LPVHOS trial). Each trial was conducted at the same time of day separated by at least 5 days from the preceding trial to avoid any effects of circadian rhythm or thermal adaptation by exercise on the measurements. The order of the trials was randomized.
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Protocols
Subjects' meals were controlled for 2 days before each trial to control subjects' condition, such as PV and Posmol. They were given hamburgers for supper (790 kcal with 5 g salt in each burger; Mos Food Service, Tokyo) and buns as breakfast and lunch (1035 kcal with 2 g salt in each bun). Also, the subjects were asked to refrain from alcohol, caffeine and heavy exercise during this period.
In the C group, subjects reported to the laboratory at 09:00 h normally hydrated but without breakfast on the experimental day. In the NPVHOS group, they were asked to refrain from water intake for 24 h preceding the experiment, with 30 mg of a diuretic (furosemide) intake before supper on the night before the experiment. On the experimental day, they came to the laboratory at 08:00 h, received an infusion of hypertonic NaCl solution, 2.1 (1.6–2.4)% (mean (range)) and 501 (374–720) ml, through a Teflon catheter inserted into the antecubital vein, at a rate of 0.15 ml (kg body weight)–1 min–1 for 60 min to restore PV without reducing Posmol. The concentration and the infused volume of hypertonic NaCl solution were adjusted by mixing 10% and 0.9% NaCl solutions to attain the targeted values of PV and Posmol in each subject. In the LPVIOS group, the subjects were allowed to drink water ad libitum, but asked to take furosemide, and they came to the laboratory at 09:00 h. In the LPVHOS group, the subjects were asked to refrain from water intake for 24 h preceding the experiment with furosemide intake, and they came to the laboratory at 09:00 h, but received no infusion of hypertonic NaCl solution.
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After these pretreatments, subjects in all trials, clad in shorts and shoes, emptied their bladders, and entered the chamber controlled at 30 (29–31)°C (mean (range)) atmospheric temperature (Ta), and 45% (35–53) relative humidity (RH). Then, a Teflon catheter (18 gauge) was inserted into the large antecubital vein for blood sampling. The subjects sat on the contour chair of the cycle ergometer in a semirecumbent position and rested for 60 min, during which time the devices for the measurements were applied until stabilization of body fluid. Then, after baseline measurements were taken at rest for 10 min, the subjects started to exercise in a semirecumbent position at 60% (136 ± 20 W, mean ± S.D.) without fan cooling. Forearm blood flow (FBF), laser-Doppler flux on the forearm skin (CBF), sweat rate (SR), heart rate (HR), systolic (SBP) and diastolic (DBP) arterial blood pressure, oesophageal (Toes) and mean skin temperature (Tsk) were measured during this period. After confirming that the increases in FBF and Toes reached a plateau (>37.8°C), subjects were asked to drink 200 ml of tap water warmed to 37.5°C within a minute, and they then continued to exercise for a further 10 min. Subjects drank more water at 33 ± 1 min in C, 30 ± 2 min in NPVHOS, 33 ± 1 min in LPVIOS, and 31 ± 1 min in LPVHOS, after the start of exercise, with no significant differences among them.
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Measurements
PV. PV was determined by the Evans blue dye dilution method (Greenleaf et al. 1979) at least a week before the start of this study. On the day of PV measurement, subjects reported to the laboratory at 07:30 h normally hydrated, but having fasted for 10 h before the experiment. After sitting for 60 min at 28°C Ta and 50% RH, a control blood sample was taken, the dye was injected at 0.2 mg (kg body weight)–1, and blood samples were taken at 10 and 20 min after the injection.
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. was determined with graded cycle-ergometer exercise in a semirecumbent position at 25 (24–26) °C Ta and 45% RH, as described below, on the day after the PV measurement. After the electrocardiogram electrodes were applied, the subjects started pedalling at 60 cycles min–1 at an initial intensity of 0 W. The intensity was increased by 60 W every 3 min until reaching 180 W; above this intensity, it was increased by 30 W every 2 min up to 240 W, and then 15 W every 2 min until subjects were not able to maintain the rhythm. The oxygen consumption rate was calculated every 15 s from the oxygen and carbon dioxide fractions in expired gas and the expired ventilatory volume (Aeromonitor AE260; Minato, Tokyo, Japan). was determined after the three largest consecutive values at the end of exercise were averaged.
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Toes and Tsk. Toes was monitored with a thermocouple in a polyethylene tube (PE-90). The tip of the tube was advanced at a distance of one-fourth of the subject's standing height from the external nares. Tsk was determined as Tsk = 0.25Tfa + 0.43Tch + 0.32Tth (Roberts et al. 1977), where Tfa, Tch and Tth are skin surface temperature at the forearm, chest and thigh, respectively, measured with the thermocouples.
Thermoregulatory and cardiovascular responses during exercise. FBF was measured by using venous occlusion plethysmography with a mercury-in-Silastic tube strain gauge placed around the upper side of the subject's left forearm positioned above the heart level, with the hand eliminated from the circulation by inflation of an occlusion cuff to a supra-arterial pressure (280 mmHg) (Whitney, 1953). We also measured CBF on the forearm skin just beside the strain gauge (ALF21; Advance, Tokyo, Japan). SR was determined by capacitance hygrometry, calculated from the relative humidity and temperature of the air (THPB3; Shinyei, Tokyo, Japan) flowing out of a 12.56 cm2 capsule at the rate of 1.5 l min–1 on the chest at 5 cm below the left clavicle. Toes, Tsk, CBF and SR were recorded every 5 s, and FBF was recorded every 30 s at rest and during exercise. HR was recorded every 1 min from the trace of an electrocardiogram (Life Scope 8; Nihon Kohden, Tokyo, Japan). SBP and DBP were measured every 1 min from the right upper arm placed at the heart level by inflation of the cuff with a sonometric pickup of Korotkoff's sound (STBP-780; Colin, Komaki, Japan). Pulse pressure (PP) and MAP were calculated as SBP – DBP and DBP + PP/3, respectively. Forearm (FVC) and cutaneous vascular conductance (CVC) were calculated as FBF and CBF divided by MAP, and reported in units of ml min–1 100 g–1 mmHg–1 and V mmHg–1, respectively.
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Blood analyses. Eleven millilitres of blood were sampled at rest and at 5 min before and after drinking during exercise in each trial (Fig. 1). A 1 ml aliquot of blood was used to determine haematocrit (Hct (%), microcentrifuge) and haemoglobin concentration (Hb (g dl–1), cyanomethaemoglobin). The percentage changes in PV (%PV) were calculated in all trials using Hct and Hb (Greenleaf et al. 1979). The absolute values of PV at rest and during exercise in each trial were determined from%PV and the baseline value measured by the dye dilution technique. An aliquot of 3 ml was centrifuged immediately at room temperature, and the aliquots of plasma were used to determine Posmol (mosomol (kg H2O)–1, using the freezing point depression method, and one-10 osmometer; Fisk, Norwood, MA, USA). The remaining 7 ml of the aliquot was placed in a chilled tube (EDTA (2 Na) 1.5 mg ml–1) that was centrifuged at 4°C to determine plasma adrenaline ([Ad]p), noradrenaline ([NA]p) and arginine vasopressin ([AVP]p) concentrations. These samples were stored at –85°C until hormone assays were performed. [Ad]p and [NA]p were measured by HPLC (model HPLC-725CA; Toso, Tokyo, Japan). The respective intra-assay coefficients of variation for the measurements of [Ad]p and [NA]p were 2.47 and 2.83% at the levels of 274 and 280 pg ml–1, and they were 1.88 and 3.25% at the levels of 473 and 482 pg ml–1. [AVP]p was measured by radioimmunoassay (AVP-RIA Mitsubishi; Mitsubishi Kagaku Matron, Tokyo, Japan). The intra-assay coefficients of variation were 11.34, 5.21 and 8.71% at the levels of 0.92, 2.09 and 8.16 pg ml–1, respectively.
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Thermoregulatory and mean arterial pressure responses to moderate exercise in two normal plasma volume trials: isosmolality (control, thin line) and hyperosmolality (NPVHOS, thick line) in one subject. The dark columns show the time at which the subject drank 200 ml water. The upward arrows indicate the time of blood sampling. The light columns represent the periods of 3 min before and after drinking, where the values are averaged in Tables 2 and 3. Because of a transient reduction in oesophageal temperature (Toes) due to water drinking, Toes values were averaged for the fourth and fifth minutes after drinking.
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Statistics
The effects of pretreatments and drinking on blood chemicals, thermoregulatory, cardiovascular responses and hormonal concentration were tested by a two-way ANOVA for repeated measures (Tables 1- 4, Figs 2–4). Subsequent post hoc tests to determine significant differences in the various pairwise comparisons were performed by Fisher's least squares difference test. All values are presented as means ± S.E.M. except when noted. The null hypothesis was rejected at the level of P < 0.05.
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Changes in forearm skin vascular conductance after drinking are presented as the differences from the baseline for 3 min before drinking. , NPVHOS, normal plasma volume with hyperosmolality; , LPVIOS, low plasma volume with isosmolality; , LPVHOS, low plasma volume with hyperosmolality; , C, normal plasma volume with isosmolality. 0 min indicates the time at the start of drinking. #Significant difference from the baseline within each trial; significant difference from LPVHOS at the level of P < 0.05.
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Results
Figure 1 shows typical thermoregulatory and MAP responses in the C and NPVHOS trials in one subject. Before drinking, FBF, CBF and SR were reduced in NPVHOS compared with the values in C, but after drinking, they increased in NPVHOS while those in C remained unchanged. In both trials, MAP decreased after drinking for this subject, but the reduction was greater in NPVHOS than that in C.
Table 1 shows PV and Posmol at rest and during exercise. PV in the LPV trials was 250–350 ml lower than that in the normovolaemic trials at rest, and the difference was sustained during exercise (P < 0.0001). Posmol in the HOS trials was 13 mosmol (kg H2O)–1 higher than that in the isosmotic trials (P < 0.0001) at rest, and the difference was sustained during exercise. Posmol in NPVHOS was 3 mosmol (kg H2O)–1 higher than that in LPVHOS at rest and during exercise (P < 0.0001). PV and Posmol did not change after drinking in any trials.
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Table 2 shows Toes, Tsk, FVC and SR determined after averaging the values during the 10 min resting period, for 3 min before drinking and for the first 3 min after drinking, except for Toes during exercise. Toes after drinking was determined by averaging the values at the fourth and fifth minute after the end of drinking because a transient fall in Toes occurred due to slightly lower temperature of water to drink (Fig. 1).
Before drinking, FVC was 26 and 42% lower in LPVHOS (P < 0.001) and LPVIOS (P < 0.0001), respectively, than that in C. After drinking, FVC in LPVHOS tended to increase by 11% (P = 0.07) compared with the value before drinking. On the other hand, FVC in NPVHOS tended to increase by 18% after drinking (P = 0.07).
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Similarly, before drinking, SR was 13% (P < 0.05) and 31% (P < 0.0001) lower in LPVHOS and NPVHOS, respectively, than that in C, but, after drinking, it increased by 7% in LPVHOS (P < 0.05) and by 17% in NPVHOS (P < 0.05).
Toes and Tsk in the HOS trials were slightly, but significantly, higher than those in the isosmotic trials during exercise (P < 0.05), but both remained unchanged after drinking.
Table 3 shows the cardiovascular variables in the four trials at rest and during exercise. HR in the HOS trials was higher than that in the isosmotic trials during exercise. After drinking, MAP tended to decrease by 3 mmHg in LPVHOS and by 6 mmHg in NPVHOS (P = 0.10). HR and PP remained unchanged after drinking.
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Figures 2 and 3 show more detailed protocols of changes in FVC and CVC, respectively, for 10 min after drinking as differences from the value for 3 min before drinking. As shown in Fig. 2, FVC in the HOS trials increased immediately after drinking and the increase was sustained for the next 10 min, with significant differences from the baseline during this period (P < 0.05). Similarly, as shown in Fig. 3, the change in CVC after drinking in the HOS trials showed a very similar pattern to that in FVC (P < 0.05). However, the increase in FVC after drinking was higher in NPVHOS than that in LPVHOS for 10 min after the start of drinking except for the fourth and eighth minutes (P < 0.05), and that in CVC for the first 3 min (P < 0.05).
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Changes in cutaneous vascular conductance after drinking are presented as the differences from the baseline for 3 min before drinking. The abbreviations and symbols are the same as those in Fig. 2. #Significant difference from the baseline within each trial; significant difference from LPVHOS at the level of P < 0.05.
Figure 4 shows the changes in MAP after drinking in all trials. The changes in MAP were in an inverse direction to that in FVC or CVC in all the trials. MAP in NPVHOS decreased by the first minute after the start of drinking (P < 0.01), while that in LPVHOS did not decrease before the second minute (P < 0.05). The decrease in MAP in LPVHOS tended to be attenuated compared with that in NPVHOS (P = 0.09).
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Changes in mean arterial pressure after drinking are presented as the differences from the baseline for 3 min before drinking. The abbreviations and symbols are the same as those in Fig. 2. #Significant difference from the baseline within each trial at the level of P < 0.05.
Table 4 shows [Ad]p, [NA]p and [AVP]p in all trials. During exercise, [NA]p increased in all trials (P < 0.01) and the increase was the highest in LPVHOS (P < 0.01). The increase in [AVP]p was about threefold greater in the HOS trials than that in the isosmotic trials (P < 0.0001). After drinking, [NA]p increased (P < 0.0001) but [AVP]p remained unchanged in all trials.
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Discussion
In the present study, we found that oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and caused a fall in MAP in dehydrated subjects exercising in a hot environment. In addition, we found that the suppression was released more in a normovolaemic and hyperosmotic condition than in dehydration, a hypovolaemic and hyperosmotic condition. On the other hand, the suppression of cutaneous vasodilatation in a hypovolaemic and isosmotic condition was not released by drinking.
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Released hyperosmotic suppression of cutaneous vasodilatation after drinking
As shown in Fig. 2, FVC increased markedly after drinking warm water in the HOS trials. Since there were no significant changes in Posmol and PV during this period (Table 1), the increased cutaneous vasodilatation was likely to be caused by stimulating the oropharyngeal reflexes. It has been suggested that thirst sensation and AVP concentration in plasma decrease immediately after drinking in dehydrated animals (Arnauld & Pont, 1982; Thrasher et al. 1987) and humans (Geelen et al. 1984; Takamata et al. 1995); this has been suggested to occur through oropharyngeal reflexes to prevent overhydration due to excessive water intake. Moreover, Takamata et al. (1995) suggested that, in passively heated subjects with hyperosmolality, the suppression of sweating is released by oropharyngeal stimulation by drinking. The detailed mechanisms for these responses are unclear, but the signals projecting from the central osmoreceptors to the anterior hypothalamus, where the centres for thirst sensation, AVP secretion and thermoregulation are located, are likely to be suppressed by oropharyngeal stimulation caused by drinking (Geelen et al. 1984; Takamata et al. 1995).
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Although, in the present study, FVC as well as SR increased after drinking in HOS trials (Table 2), AVP concentration in plasma did not fall (Table 4), which is different from the results reported previously (Geelen et al. 1984; Takamata et al. 1995). This discrepancy suggests that the release of the suppression of thermoregulatory responses was caused through a different path from that for thirst sensation and AVP secretion. Indeed, it has been suggested that the suppression of thermoregulatory responses by hyperosmolality is caused by a direct influence of extracellular fluid osmolality on thermosensitive cells (Silva & Boulant, 1984) although not excluding the possible involvement of osmosensitive structures in the circumventricular organs, which are known to regulate body fluid and arterial pressure homeostasis (Fitzsimons, 1979), which might send the signals to suppress the thermosensitive neurone activity. Moreover, Ichinose et al. (2005) recently suggested that the sensitivity of hyperosmotic suppression of cutaneous vasodilatation during exercise is reduced after endurance training, although the sensitivity of AVP secretion in response to increased Posmol during graded exercise was reported to be enhanced in fit subjects (Freund et al. 1987) and even remained unchanged in heat-acclimatized subjects (Takamata et al. 2001). These results support the idea that the hyperosmotic suppression of thermoregulatory response and its release by oropharyngeal stimulation occurred through a different path from that for AVP secretion.
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Takamata et al. (1995) suggested that the cutaneous vasodilatation did not occur after drinking in passively heated subjects in the sitting position, whereas it did during exercise in the present study. However, Posmol was 297 mosmol (kg H2O)–1 in their study, much lower than 305–309 mosmol (kg H2O)–1 in the present study. Thus, the larger suppression of cutaneous vasodilatation with greater increase in Posmol allowed the release of hyperosmotic suppression of cutaneous vasodilatation by drinking.
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Reduction in MAP after drinking in the hyperosmotic trials
MAP decreased with increases in FVC or CVC after drinking for the HOS trials (Fig. 4). Since the ratio of skin vascular conductance to total vascular conductance increases during exercise in a hot environment, even a small increase in the conductance might easily threaten the maintenance of MAP. The cardiac output at the exercise intensity in the present study was estimated as 20 l min–1 (Nose et al. 1994), and the total skin blood flow before drinking was 7.0 l min–1 in the HOS trials, assuming that the increase in FBF represents the average increase in skin blood flow over the entire body (Johnson & Rowell, 1975). Since MAP was approximately 100 mmHg in both trials, the total vascular conductance was calculated as 0.20 l min–1 mmHg–1, of which 30% was the total vascular conductance of the skin. Assuming that the cardiac output and the vascular conductance in other parts of the body remained unchanged, the increase in the total skin vascular conductance after drinking, estimated from the increase in FVC which increased by about 20% in NPVHOS, was 6%, leading to 6 mmHg falls in MAP. This estimate was identical to the real fall in MAP for the HOS trials (Table 3, Fig. 4).
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Because FVC was calculated as FBF divided by MAP, we were not able to exclude the possible involvement of muscle vascular conductance in the increase in FVC after drinking. However, it was suggested that arterial pressure was rather increased by drinking in dogs (Thrasher et al. 1987) and in humans (Jordan et al. 2000) with enhanced muscle sympathetic nervous activity (Endo et al. 2002). Also, Schroeder et al. (2002) suggested that the orthostatic tolerance was improved by 500 ml of water intake just before the test. These results suggest that drinking induces peripheral vasoconstriction and pressor responses in a normovolaemic, normothermic and resting condition. In contrast to these results, we found in the present study that drinking induced peripheral vasodilatation and a fall in MAP in a hyperosmotic and exercising condition. Since the increase in FVC after drinking in the Hos trials showed a similar pattern to that in CVC (Figs 2 and 3), and also since [NA]p increased after drinking (Table 4), the increase in FVC was likely to be caused mainly by cutaneous vasodilatation. In other words, cutaneous vasodilatation after drinking was high enough to conceal the effects of the drinking-induced muscular vasoconstriction, if it occurred.
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Enhanced cutaneous vasodilatation after drinking in normovolaemic hyperosmolality
The release of the suppression for FVC after drinking in LPVHOS was attenuated compared with that in NPVHOS (Table 2, Fig. 3), followed by a blunted decrease in MAP (Fig. 4). This attenuation might be caused by baroreflexes stimulated by hypovolaemia.
González-Alonso et al. (1998) reported that cardiac output and FVC started to decrease by 90 and 120 min, respectively, after the start of exercise at 60% in a hot environment with no water. Nose et al. (1994) suggested in exercising humans in a hot environment that the increased skin vascular conductance reduced central venous pressure, which suppressed a further increase in skin vascular conductance in a self-limiting manner. Moreover, it was also suggested that the reduced venous return to the heart by a lower body negative-pressure manoeuvre suppressed cutaneous vasodilatation (Kellogg et al. 1993). These results suggest that the reduced venous return to the heart due to hypovolaemia in LPVHOS suppressed the cutaneous vasodilatation through arterial and/or cardiopulmonary baroreflexes, importantly, which was not influenced by drinking as in LPVIOS. Indeed, as shown in Table 3, PP before drinking was significantly lower in LPVHOS than those in NPVHOS with enhanced HR by 5 beats min–1 (Table 3), suggesting that baroreflexes were stimulated in LPVHOS.
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Role of hyperosmolality in maintaining MAP
In the present study, we found that the cutaneous vasodilatation and the fall in MAP occurred after drinking even though in LPVHOS. González-Alonso et al. (1997) reported that MAP in dehydrated subjects was as well maintained during exercise in a cold environment as that in euhydrated ones, but it decreased significantly in a hot environment, suggesting that baroreflex suppression of cutaneous vasodilatation is not sufficient to maintain MAP in hypovolaemic subjects exercising in a hot environment. Moreover, Nakajima et al. (1998) suggested, in passively heated and awake rats, that although MAP decreased with increases in rectal temperature and tail vascular conductance in isosmotic hypovolaemia, MAP was well maintained in hyperosmotic hypovolaemia by suppressing tail cutaneous vasodilatation. These results suggest that hyperosmolality compensates for the impaired function of baroreflexes to maintain MAP by suppressing cutaneous vasodilatation in dehydrated and exercising humans, although by sacrificing body temperature regulation.
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Released hyperosmotic suppression of sweating after drinking
As shown in Table 2, a prominent increase in SR after drinking occurred not only in NPVHOS, as reported previously in resting subjects (Takamata et al. 1995), but also in LPVHOS, suggesting that the increase in SR after drinking was mainly caused by the release of hyperosmotic suppression, and the effect of hypovolaemia was minimal.
Adrenaline and noradrenaline responses
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Despite the same increase in [NA]p, during exercise (Table 4), FVC and CVC were lower in NPVHOS and LPVIOS than in C, and, moreover, despite the greater increase in [NA]p, FVC in LPVHOS remained at the same level as that in NPVHOS and LPVIOS. Further, FVC and CVC were enhanced after drinking in the HOS trials while [NA]p increased after drinking in every trial. Thus, the suppression of cutaneous vasodilatation by hypovolaemia/hyperosmolality or its releases by drinking in NPVHOS and LPVHOS were not correlated with vasoconstrictor system evaluated from [NA]p, suggesting more involvement of the active vasodilator system in these phenomena (Kellogg et al. 1993).
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In summary, the dehydration-induced suppression of cutaneous vasodilatation during exercise was released by oropharyngeal stimulation due to drinking, leading to a transient fall in MAP. However, these responses were enhanced when PV was restored, suggesting that the cutaneous vasodilatation was also suppressed by unloading of baroreceptors, which were not released by oropharyngeal stimulation.
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Abstract
We examined whether oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and decreased mean arterial pressure (MAP) in exercising subjects, and assessed the effects of hypovolaemia or hyperosmolality alone on these responses. Seven young males underwent four hydration conditions. These were two normal plasma volume (PV) trials: normal plasma osmolality (Posmol, control trial) and hyperosmolality (Posmol = +11 mosmol (kg H2O)–1); and two low PV trials: isosmolality (PV = –310 ml) and hyperosmolality (PV = –345 ml; Posmol = +9 mosmol (kg H2O)–1), attained by combined treatment with furosemide (frusemide), hypertonic saline and/or 24 h water restriction. In each trial, the subjects exercised at 60% peak aerobic power for 50 min at 30°C atmospheric temperature and 50% relative humidity. When oesophageal temperature (Toes) reached a plateau after 30 min of exercise, the subjects drank 200 ml water at 37.5°C within a minute. Before drinking, forearm vascular conductance (FVC), calculated as forearm blood flow divided by MAP, was lowered by 20–40% in hypovolaemia, hyperosmolality, or both, compared with that in the control trial, despite increased Toes. After drinking, FVC increased by 20% compared with that before drinking (P < 0.05) in both hyperosmotic trials, but it was greater in normovolaemia than in hypovolaemia (P < 0.05). However, no increases occurred in either isosmotic trial. MAP fell by 4–8 mmHg in both hyperosmotic trials (P < 0.05) after drinking, but more rapidly in normovolaemia than in hypovolaemia. PV and Posmol did not change during this period. Thus, oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and reduced MAP during exercise, and this was accelerated when PV was restored.
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Introduction
It is well known that hyperosmolality and hypovolaemia induce thirst sensation and vasopressin secretion (Robertson & Athar, 1976), and also suppress thermoregulatory responses, including cutaneous vasodilatation and sweating (Nadel et al. 1980; Fortney et al. 1984; Takamata et al. 1997, 1998). Since these responses disappear after recovery of plasma volume (PV) and/or plasma osmolality (Posmol) (Montain & Coyle, 1992), baroreflex and osmosensitive mechanisms may be involved.
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On the other hand, in dehydrated subjects, it was reported that the stimulation of oropharyngeal reflexes by drinking such a small amount of water so as not to change PV and Posmol reduces thirst sensation and plasma vasopressin secretion (Geelen et al. 1984; Takamata et al. 1995a). These responses have been thought to be a feed-forward mechanism to prevent over-hydration by drinking too much water (Arnauld & du Pont, 1982; Geelen et al. 1984; Thrasher et al. 1987). On the other hand, very few studies have been conducted to examine the reflex effects of drinking on skin blood flow in dehydrated subjects exercising in a hot environment. Since skin blood flow increased during exercise much more than at rest (Rowell, 1986), oropharyngeal stimulation due to drinking would release the hyperosmotic suppression of cutaneous vasodilatation by anticipating the recovery in PV or Posmol in a feed-forward manner. In addition, if the suppression contributes to the maintenance of MAP in dehydrated and exercising subjects, as suggested in rats at rest (Nakajima et al. 1998), the release by drinking would cause a prominent fall in mean arterial pressure (MAP).
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We hypothesised that oropharyngeal stimulation due to drinking would enhance the cutaneous vasodilatation in dehydrated subjects, resulting in a fall in MAP, while PV and Posmol remained unchanged. To test these hypotheses, we measured skin blood flow and MAP after drinking in dehydrated subjects exercising in a hot environment. The reason for conducting additional experiments in hyperosmolality or hypovolaemia alone was to assess their individual effects on the suppression of cutaneous vasodilatation, its release by drinking, and the consequent fall in MAP, if they occurred.
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Methods
Subjects
Seven healthy non-smoking males were recruited for the present study. Subjects gave their written informed consent before participating in this study, which conformed to the guidelines contained in the Declaration of Helsinki, and it was approved by the Review Board on Human Experiments, Shinshu University School of Medicine. The physical characteristics of the subjects were: 22 ± 3 (S.D.) years of age, 167 ± 4 cm height, 59.3 ± 6.0 kg body weight, and 3549 ± 461 ml peak aerobic power , and 2937 ± 189 ml PV.
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Trials
The measurements were performed in four trials. These were two normal PV trials in isosmolality (control, C trial) and hyperosmolality (NPVHOS trial), and two low PV trials in isosmolality (LPVIOS trial) and hyperosmolality (LPVHOS trial). Each trial was conducted at the same time of day separated by at least 5 days from the preceding trial to avoid any effects of circadian rhythm or thermal adaptation by exercise on the measurements. The order of the trials was randomized.
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Protocols
Subjects' meals were controlled for 2 days before each trial to control subjects' condition, such as PV and Posmol. They were given hamburgers for supper (790 kcal with 5 g salt in each burger; Mos Food Service, Tokyo) and buns as breakfast and lunch (1035 kcal with 2 g salt in each bun). Also, the subjects were asked to refrain from alcohol, caffeine and heavy exercise during this period.
In the C group, subjects reported to the laboratory at 09:00 h normally hydrated but without breakfast on the experimental day. In the NPVHOS group, they were asked to refrain from water intake for 24 h preceding the experiment, with 30 mg of a diuretic (furosemide) intake before supper on the night before the experiment. On the experimental day, they came to the laboratory at 08:00 h, received an infusion of hypertonic NaCl solution, 2.1 (1.6–2.4)% (mean (range)) and 501 (374–720) ml, through a Teflon catheter inserted into the antecubital vein, at a rate of 0.15 ml (kg body weight)–1 min–1 for 60 min to restore PV without reducing Posmol. The concentration and the infused volume of hypertonic NaCl solution were adjusted by mixing 10% and 0.9% NaCl solutions to attain the targeted values of PV and Posmol in each subject. In the LPVIOS group, the subjects were allowed to drink water ad libitum, but asked to take furosemide, and they came to the laboratory at 09:00 h. In the LPVHOS group, the subjects were asked to refrain from water intake for 24 h preceding the experiment with furosemide intake, and they came to the laboratory at 09:00 h, but received no infusion of hypertonic NaCl solution.
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After these pretreatments, subjects in all trials, clad in shorts and shoes, emptied their bladders, and entered the chamber controlled at 30 (29–31)°C (mean (range)) atmospheric temperature (Ta), and 45% (35–53) relative humidity (RH). Then, a Teflon catheter (18 gauge) was inserted into the large antecubital vein for blood sampling. The subjects sat on the contour chair of the cycle ergometer in a semirecumbent position and rested for 60 min, during which time the devices for the measurements were applied until stabilization of body fluid. Then, after baseline measurements were taken at rest for 10 min, the subjects started to exercise in a semirecumbent position at 60% (136 ± 20 W, mean ± S.D.) without fan cooling. Forearm blood flow (FBF), laser-Doppler flux on the forearm skin (CBF), sweat rate (SR), heart rate (HR), systolic (SBP) and diastolic (DBP) arterial blood pressure, oesophageal (Toes) and mean skin temperature (Tsk) were measured during this period. After confirming that the increases in FBF and Toes reached a plateau (>37.8°C), subjects were asked to drink 200 ml of tap water warmed to 37.5°C within a minute, and they then continued to exercise for a further 10 min. Subjects drank more water at 33 ± 1 min in C, 30 ± 2 min in NPVHOS, 33 ± 1 min in LPVIOS, and 31 ± 1 min in LPVHOS, after the start of exercise, with no significant differences among them.
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Measurements
PV. PV was determined by the Evans blue dye dilution method (Greenleaf et al. 1979) at least a week before the start of this study. On the day of PV measurement, subjects reported to the laboratory at 07:30 h normally hydrated, but having fasted for 10 h before the experiment. After sitting for 60 min at 28°C Ta and 50% RH, a control blood sample was taken, the dye was injected at 0.2 mg (kg body weight)–1, and blood samples were taken at 10 and 20 min after the injection.
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. was determined with graded cycle-ergometer exercise in a semirecumbent position at 25 (24–26) °C Ta and 45% RH, as described below, on the day after the PV measurement. After the electrocardiogram electrodes were applied, the subjects started pedalling at 60 cycles min–1 at an initial intensity of 0 W. The intensity was increased by 60 W every 3 min until reaching 180 W; above this intensity, it was increased by 30 W every 2 min up to 240 W, and then 15 W every 2 min until subjects were not able to maintain the rhythm. The oxygen consumption rate was calculated every 15 s from the oxygen and carbon dioxide fractions in expired gas and the expired ventilatory volume (Aeromonitor AE260; Minato, Tokyo, Japan). was determined after the three largest consecutive values at the end of exercise were averaged.
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Toes and Tsk. Toes was monitored with a thermocouple in a polyethylene tube (PE-90). The tip of the tube was advanced at a distance of one-fourth of the subject's standing height from the external nares. Tsk was determined as Tsk = 0.25Tfa + 0.43Tch + 0.32Tth (Roberts et al. 1977), where Tfa, Tch and Tth are skin surface temperature at the forearm, chest and thigh, respectively, measured with the thermocouples.
Thermoregulatory and cardiovascular responses during exercise. FBF was measured by using venous occlusion plethysmography with a mercury-in-Silastic tube strain gauge placed around the upper side of the subject's left forearm positioned above the heart level, with the hand eliminated from the circulation by inflation of an occlusion cuff to a supra-arterial pressure (280 mmHg) (Whitney, 1953). We also measured CBF on the forearm skin just beside the strain gauge (ALF21; Advance, Tokyo, Japan). SR was determined by capacitance hygrometry, calculated from the relative humidity and temperature of the air (THPB3; Shinyei, Tokyo, Japan) flowing out of a 12.56 cm2 capsule at the rate of 1.5 l min–1 on the chest at 5 cm below the left clavicle. Toes, Tsk, CBF and SR were recorded every 5 s, and FBF was recorded every 30 s at rest and during exercise. HR was recorded every 1 min from the trace of an electrocardiogram (Life Scope 8; Nihon Kohden, Tokyo, Japan). SBP and DBP were measured every 1 min from the right upper arm placed at the heart level by inflation of the cuff with a sonometric pickup of Korotkoff's sound (STBP-780; Colin, Komaki, Japan). Pulse pressure (PP) and MAP were calculated as SBP – DBP and DBP + PP/3, respectively. Forearm (FVC) and cutaneous vascular conductance (CVC) were calculated as FBF and CBF divided by MAP, and reported in units of ml min–1 100 g–1 mmHg–1 and V mmHg–1, respectively.
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Blood analyses. Eleven millilitres of blood were sampled at rest and at 5 min before and after drinking during exercise in each trial (Fig. 1). A 1 ml aliquot of blood was used to determine haematocrit (Hct (%), microcentrifuge) and haemoglobin concentration (Hb (g dl–1), cyanomethaemoglobin). The percentage changes in PV (%PV) were calculated in all trials using Hct and Hb (Greenleaf et al. 1979). The absolute values of PV at rest and during exercise in each trial were determined from%PV and the baseline value measured by the dye dilution technique. An aliquot of 3 ml was centrifuged immediately at room temperature, and the aliquots of plasma were used to determine Posmol (mosomol (kg H2O)–1, using the freezing point depression method, and one-10 osmometer; Fisk, Norwood, MA, USA). The remaining 7 ml of the aliquot was placed in a chilled tube (EDTA (2 Na) 1.5 mg ml–1) that was centrifuged at 4°C to determine plasma adrenaline ([Ad]p), noradrenaline ([NA]p) and arginine vasopressin ([AVP]p) concentrations. These samples were stored at –85°C until hormone assays were performed. [Ad]p and [NA]p were measured by HPLC (model HPLC-725CA; Toso, Tokyo, Japan). The respective intra-assay coefficients of variation for the measurements of [Ad]p and [NA]p were 2.47 and 2.83% at the levels of 274 and 280 pg ml–1, and they were 1.88 and 3.25% at the levels of 473 and 482 pg ml–1. [AVP]p was measured by radioimmunoassay (AVP-RIA Mitsubishi; Mitsubishi Kagaku Matron, Tokyo, Japan). The intra-assay coefficients of variation were 11.34, 5.21 and 8.71% at the levels of 0.92, 2.09 and 8.16 pg ml–1, respectively.
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Thermoregulatory and mean arterial pressure responses to moderate exercise in two normal plasma volume trials: isosmolality (control, thin line) and hyperosmolality (NPVHOS, thick line) in one subject. The dark columns show the time at which the subject drank 200 ml water. The upward arrows indicate the time of blood sampling. The light columns represent the periods of 3 min before and after drinking, where the values are averaged in Tables 2 and 3. Because of a transient reduction in oesophageal temperature (Toes) due to water drinking, Toes values were averaged for the fourth and fifth minutes after drinking.
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Statistics
The effects of pretreatments and drinking on blood chemicals, thermoregulatory, cardiovascular responses and hormonal concentration were tested by a two-way ANOVA for repeated measures (Tables 1- 4, Figs 2–4). Subsequent post hoc tests to determine significant differences in the various pairwise comparisons were performed by Fisher's least squares difference test. All values are presented as means ± S.E.M. except when noted. The null hypothesis was rejected at the level of P < 0.05.
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Changes in forearm skin vascular conductance after drinking are presented as the differences from the baseline for 3 min before drinking. , NPVHOS, normal plasma volume with hyperosmolality; , LPVIOS, low plasma volume with isosmolality; , LPVHOS, low plasma volume with hyperosmolality; , C, normal plasma volume with isosmolality. 0 min indicates the time at the start of drinking. #Significant difference from the baseline within each trial; significant difference from LPVHOS at the level of P < 0.05.
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Results
Figure 1 shows typical thermoregulatory and MAP responses in the C and NPVHOS trials in one subject. Before drinking, FBF, CBF and SR were reduced in NPVHOS compared with the values in C, but after drinking, they increased in NPVHOS while those in C remained unchanged. In both trials, MAP decreased after drinking for this subject, but the reduction was greater in NPVHOS than that in C.
Table 1 shows PV and Posmol at rest and during exercise. PV in the LPV trials was 250–350 ml lower than that in the normovolaemic trials at rest, and the difference was sustained during exercise (P < 0.0001). Posmol in the HOS trials was 13 mosmol (kg H2O)–1 higher than that in the isosmotic trials (P < 0.0001) at rest, and the difference was sustained during exercise. Posmol in NPVHOS was 3 mosmol (kg H2O)–1 higher than that in LPVHOS at rest and during exercise (P < 0.0001). PV and Posmol did not change after drinking in any trials.
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Table 2 shows Toes, Tsk, FVC and SR determined after averaging the values during the 10 min resting period, for 3 min before drinking and for the first 3 min after drinking, except for Toes during exercise. Toes after drinking was determined by averaging the values at the fourth and fifth minute after the end of drinking because a transient fall in Toes occurred due to slightly lower temperature of water to drink (Fig. 1).
Before drinking, FVC was 26 and 42% lower in LPVHOS (P < 0.001) and LPVIOS (P < 0.0001), respectively, than that in C. After drinking, FVC in LPVHOS tended to increase by 11% (P = 0.07) compared with the value before drinking. On the other hand, FVC in NPVHOS tended to increase by 18% after drinking (P = 0.07).
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Similarly, before drinking, SR was 13% (P < 0.05) and 31% (P < 0.0001) lower in LPVHOS and NPVHOS, respectively, than that in C, but, after drinking, it increased by 7% in LPVHOS (P < 0.05) and by 17% in NPVHOS (P < 0.05).
Toes and Tsk in the HOS trials were slightly, but significantly, higher than those in the isosmotic trials during exercise (P < 0.05), but both remained unchanged after drinking.
Table 3 shows the cardiovascular variables in the four trials at rest and during exercise. HR in the HOS trials was higher than that in the isosmotic trials during exercise. After drinking, MAP tended to decrease by 3 mmHg in LPVHOS and by 6 mmHg in NPVHOS (P = 0.10). HR and PP remained unchanged after drinking.
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Figures 2 and 3 show more detailed protocols of changes in FVC and CVC, respectively, for 10 min after drinking as differences from the value for 3 min before drinking. As shown in Fig. 2, FVC in the HOS trials increased immediately after drinking and the increase was sustained for the next 10 min, with significant differences from the baseline during this period (P < 0.05). Similarly, as shown in Fig. 3, the change in CVC after drinking in the HOS trials showed a very similar pattern to that in FVC (P < 0.05). However, the increase in FVC after drinking was higher in NPVHOS than that in LPVHOS for 10 min after the start of drinking except for the fourth and eighth minutes (P < 0.05), and that in CVC for the first 3 min (P < 0.05).
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Changes in cutaneous vascular conductance after drinking are presented as the differences from the baseline for 3 min before drinking. The abbreviations and symbols are the same as those in Fig. 2. #Significant difference from the baseline within each trial; significant difference from LPVHOS at the level of P < 0.05.
Figure 4 shows the changes in MAP after drinking in all trials. The changes in MAP were in an inverse direction to that in FVC or CVC in all the trials. MAP in NPVHOS decreased by the first minute after the start of drinking (P < 0.01), while that in LPVHOS did not decrease before the second minute (P < 0.05). The decrease in MAP in LPVHOS tended to be attenuated compared with that in NPVHOS (P = 0.09).
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Changes in mean arterial pressure after drinking are presented as the differences from the baseline for 3 min before drinking. The abbreviations and symbols are the same as those in Fig. 2. #Significant difference from the baseline within each trial at the level of P < 0.05.
Table 4 shows [Ad]p, [NA]p and [AVP]p in all trials. During exercise, [NA]p increased in all trials (P < 0.01) and the increase was the highest in LPVHOS (P < 0.01). The increase in [AVP]p was about threefold greater in the HOS trials than that in the isosmotic trials (P < 0.0001). After drinking, [NA]p increased (P < 0.0001) but [AVP]p remained unchanged in all trials.
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Discussion
In the present study, we found that oropharyngeal stimulation by drinking released the dehydration-induced suppression of cutaneous vasodilatation and caused a fall in MAP in dehydrated subjects exercising in a hot environment. In addition, we found that the suppression was released more in a normovolaemic and hyperosmotic condition than in dehydration, a hypovolaemic and hyperosmotic condition. On the other hand, the suppression of cutaneous vasodilatation in a hypovolaemic and isosmotic condition was not released by drinking.
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Released hyperosmotic suppression of cutaneous vasodilatation after drinking
As shown in Fig. 2, FVC increased markedly after drinking warm water in the HOS trials. Since there were no significant changes in Posmol and PV during this period (Table 1), the increased cutaneous vasodilatation was likely to be caused by stimulating the oropharyngeal reflexes. It has been suggested that thirst sensation and AVP concentration in plasma decrease immediately after drinking in dehydrated animals (Arnauld & Pont, 1982; Thrasher et al. 1987) and humans (Geelen et al. 1984; Takamata et al. 1995); this has been suggested to occur through oropharyngeal reflexes to prevent overhydration due to excessive water intake. Moreover, Takamata et al. (1995) suggested that, in passively heated subjects with hyperosmolality, the suppression of sweating is released by oropharyngeal stimulation by drinking. The detailed mechanisms for these responses are unclear, but the signals projecting from the central osmoreceptors to the anterior hypothalamus, where the centres for thirst sensation, AVP secretion and thermoregulation are located, are likely to be suppressed by oropharyngeal stimulation caused by drinking (Geelen et al. 1984; Takamata et al. 1995).
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Although, in the present study, FVC as well as SR increased after drinking in HOS trials (Table 2), AVP concentration in plasma did not fall (Table 4), which is different from the results reported previously (Geelen et al. 1984; Takamata et al. 1995). This discrepancy suggests that the release of the suppression of thermoregulatory responses was caused through a different path from that for thirst sensation and AVP secretion. Indeed, it has been suggested that the suppression of thermoregulatory responses by hyperosmolality is caused by a direct influence of extracellular fluid osmolality on thermosensitive cells (Silva & Boulant, 1984) although not excluding the possible involvement of osmosensitive structures in the circumventricular organs, which are known to regulate body fluid and arterial pressure homeostasis (Fitzsimons, 1979), which might send the signals to suppress the thermosensitive neurone activity. Moreover, Ichinose et al. (2005) recently suggested that the sensitivity of hyperosmotic suppression of cutaneous vasodilatation during exercise is reduced after endurance training, although the sensitivity of AVP secretion in response to increased Posmol during graded exercise was reported to be enhanced in fit subjects (Freund et al. 1987) and even remained unchanged in heat-acclimatized subjects (Takamata et al. 2001). These results support the idea that the hyperosmotic suppression of thermoregulatory response and its release by oropharyngeal stimulation occurred through a different path from that for AVP secretion.
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Takamata et al. (1995) suggested that the cutaneous vasodilatation did not occur after drinking in passively heated subjects in the sitting position, whereas it did during exercise in the present study. However, Posmol was 297 mosmol (kg H2O)–1 in their study, much lower than 305–309 mosmol (kg H2O)–1 in the present study. Thus, the larger suppression of cutaneous vasodilatation with greater increase in Posmol allowed the release of hyperosmotic suppression of cutaneous vasodilatation by drinking.
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Reduction in MAP after drinking in the hyperosmotic trials
MAP decreased with increases in FVC or CVC after drinking for the HOS trials (Fig. 4). Since the ratio of skin vascular conductance to total vascular conductance increases during exercise in a hot environment, even a small increase in the conductance might easily threaten the maintenance of MAP. The cardiac output at the exercise intensity in the present study was estimated as 20 l min–1 (Nose et al. 1994), and the total skin blood flow before drinking was 7.0 l min–1 in the HOS trials, assuming that the increase in FBF represents the average increase in skin blood flow over the entire body (Johnson & Rowell, 1975). Since MAP was approximately 100 mmHg in both trials, the total vascular conductance was calculated as 0.20 l min–1 mmHg–1, of which 30% was the total vascular conductance of the skin. Assuming that the cardiac output and the vascular conductance in other parts of the body remained unchanged, the increase in the total skin vascular conductance after drinking, estimated from the increase in FVC which increased by about 20% in NPVHOS, was 6%, leading to 6 mmHg falls in MAP. This estimate was identical to the real fall in MAP for the HOS trials (Table 3, Fig. 4).
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Because FVC was calculated as FBF divided by MAP, we were not able to exclude the possible involvement of muscle vascular conductance in the increase in FVC after drinking. However, it was suggested that arterial pressure was rather increased by drinking in dogs (Thrasher et al. 1987) and in humans (Jordan et al. 2000) with enhanced muscle sympathetic nervous activity (Endo et al. 2002). Also, Schroeder et al. (2002) suggested that the orthostatic tolerance was improved by 500 ml of water intake just before the test. These results suggest that drinking induces peripheral vasoconstriction and pressor responses in a normovolaemic, normothermic and resting condition. In contrast to these results, we found in the present study that drinking induced peripheral vasodilatation and a fall in MAP in a hyperosmotic and exercising condition. Since the increase in FVC after drinking in the Hos trials showed a similar pattern to that in CVC (Figs 2 and 3), and also since [NA]p increased after drinking (Table 4), the increase in FVC was likely to be caused mainly by cutaneous vasodilatation. In other words, cutaneous vasodilatation after drinking was high enough to conceal the effects of the drinking-induced muscular vasoconstriction, if it occurred.
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Enhanced cutaneous vasodilatation after drinking in normovolaemic hyperosmolality
The release of the suppression for FVC after drinking in LPVHOS was attenuated compared with that in NPVHOS (Table 2, Fig. 3), followed by a blunted decrease in MAP (Fig. 4). This attenuation might be caused by baroreflexes stimulated by hypovolaemia.
González-Alonso et al. (1998) reported that cardiac output and FVC started to decrease by 90 and 120 min, respectively, after the start of exercise at 60% in a hot environment with no water. Nose et al. (1994) suggested in exercising humans in a hot environment that the increased skin vascular conductance reduced central venous pressure, which suppressed a further increase in skin vascular conductance in a self-limiting manner. Moreover, it was also suggested that the reduced venous return to the heart by a lower body negative-pressure manoeuvre suppressed cutaneous vasodilatation (Kellogg et al. 1993). These results suggest that the reduced venous return to the heart due to hypovolaemia in LPVHOS suppressed the cutaneous vasodilatation through arterial and/or cardiopulmonary baroreflexes, importantly, which was not influenced by drinking as in LPVIOS. Indeed, as shown in Table 3, PP before drinking was significantly lower in LPVHOS than those in NPVHOS with enhanced HR by 5 beats min–1 (Table 3), suggesting that baroreflexes were stimulated in LPVHOS.
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Role of hyperosmolality in maintaining MAP
In the present study, we found that the cutaneous vasodilatation and the fall in MAP occurred after drinking even though in LPVHOS. González-Alonso et al. (1997) reported that MAP in dehydrated subjects was as well maintained during exercise in a cold environment as that in euhydrated ones, but it decreased significantly in a hot environment, suggesting that baroreflex suppression of cutaneous vasodilatation is not sufficient to maintain MAP in hypovolaemic subjects exercising in a hot environment. Moreover, Nakajima et al. (1998) suggested, in passively heated and awake rats, that although MAP decreased with increases in rectal temperature and tail vascular conductance in isosmotic hypovolaemia, MAP was well maintained in hyperosmotic hypovolaemia by suppressing tail cutaneous vasodilatation. These results suggest that hyperosmolality compensates for the impaired function of baroreflexes to maintain MAP by suppressing cutaneous vasodilatation in dehydrated and exercising humans, although by sacrificing body temperature regulation.
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Released hyperosmotic suppression of sweating after drinking
As shown in Table 2, a prominent increase in SR after drinking occurred not only in NPVHOS, as reported previously in resting subjects (Takamata et al. 1995), but also in LPVHOS, suggesting that the increase in SR after drinking was mainly caused by the release of hyperosmotic suppression, and the effect of hypovolaemia was minimal.
Adrenaline and noradrenaline responses
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Despite the same increase in [NA]p, during exercise (Table 4), FVC and CVC were lower in NPVHOS and LPVIOS than in C, and, moreover, despite the greater increase in [NA]p, FVC in LPVHOS remained at the same level as that in NPVHOS and LPVIOS. Further, FVC and CVC were enhanced after drinking in the HOS trials while [NA]p increased after drinking in every trial. Thus, the suppression of cutaneous vasodilatation by hypovolaemia/hyperosmolality or its releases by drinking in NPVHOS and LPVHOS were not correlated with vasoconstrictor system evaluated from [NA]p, suggesting more involvement of the active vasodilator system in these phenomena (Kellogg et al. 1993).
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In summary, the dehydration-induced suppression of cutaneous vasodilatation during exercise was released by oropharyngeal stimulation due to drinking, leading to a transient fall in MAP. However, these responses were enhanced when PV was restored, suggesting that the cutaneous vasodilatation was also suppressed by unloading of baroreceptors, which were not released by oropharyngeal stimulation.
References
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