Thermoregulatory Responses Are Attenuated after Fructose but Not Glucose Intake AKINA SUZUKI1, KAZUNOBU OKAZAKI1,2, DAIKI IMAI1,2, RYOSUKE TAKEDA1, NOOSHIN NAGHAVI1, HISAYO YOKOYAMA1,2, and TOSHIAKI MIYAGAWA1,2 1

Department of Environmental Physiology for Exercise, Osaka City University Graduate School of Medicine, Osaka, JAPAN; and 2Research Center for Urban Health and Sports, Osaka City University, Osaka, JAPAN

ABSTRACT SUZUKI, A., K. OKAZAKI, D. IMAI, R. TAKEDA, N. NAGHAVI, H. YOKOYAMA, and T. MIYAGAWA. Thermoregulatory Responses Are Attenuated after Fructose but Not Glucose Intake. Med. Sci. Sports Exerc., Vol. 46, No. 7, pp. 1452–1461, 2014. Purpose: We examined whether plasma hyperosmolality induced by oral monosaccharide intake attenuated thermoregulatory responses and whether the responses were different between fructose and glucose. Methods: Ten healthy young subjects performed three trials in a sitting position in an artificial climate chamber (ambient temperature, 28-C; relative humidity, 40%). After resting for 10 min, the subjects drank 300 mL of water alone (control), or 300 mL of water supplemented with 75 g fructose or 75 g glucose. Twenty minutes later, they were heated passively by immersing the lower legs in water at 42-C for 60 min. Plasma osmolality (Posm), sodium ([Na+]p) and insulin concentrations ([Ins]p), and percent change in plasma volume (%$PV) were measured, and esophageal temperature (Tes) thresholds for cutaneous vasodilation (THCVC) and sweating (THSR) at the forearm were determined. Results: Posm was significantly increased by fructose and glucose intake compared with water alone, although %$PV and [Na+]p were not significantly different among the three trials. [Ins]p was significantly higher after glucose intake than after fructose or water alone. THCVC and THSR were significantly higher after fructose intake than after glucose intake, which showed similar values to water intake. Conclusions: These results suggest that the Tes threshold for thermoregulation is elevated after fructose intake, indicating the attenuation of thermoregulatory responses, whereas it is not attenuated after glucose intake. These results provide a novel insight to better determine the carbohydrate component of oral rehydration fluids for preventing dehydration and/or heat disorders. Key Words: CARBOHYDRATE, OSMOLALITY, INSULIN, CUTANEOUS VASODILATION, SWEATING

APPLIED SCIENCES

A

the precise role of the carbohydrate component on thermoregulatory responses has not been well studied. Previous studies indicate that plasma osmolality (Posm) increases with increases in blood glucose concentration after intravenous glucose infusion (40,45) and oral intake of carbohydrate containing beverages (3,17). Plasma hyperosmolality induced by thermal dehydration (9) or hypertonic saline infusion (38) attenuates thermoregulatory responses by elevating the core body temperature threshold for cutaneous vasodilation and sweating. In addition, increases in Posm caused by sodium and mannitol infusion evoked excessive, similar increases in rectal temperature in exercising dogs, indicating that plasma hyperosmolality attenuates thermoregulatory responses independently of sodium concentration (21). Thus, it is possible that oral carbohydrate-induced increases in blood glucose concentration might attenuate thermoregulatory responses. In contrast, other data indicate that intravenous glucose infusion attenuated the increase in esophageal temperature (Tes) during prolonged (120–150 min) exercise under a hot condition, compared with 0.45% saline, indicating enhanced thermoregulatory responses after intravenous glucose infusion (24). In addition, rises in rectal temperature during exercise in men following water immersion-induced dehydration were lower after glucose solution intake compared with no intake during the rehydration period before exercise, although intravascular volume and Posm were similar between the trials (7). These studies indicate that increases in blood glucose concentration

dequate fluid intake is essential for athletes and for members of the general public exposed to hot environments (33). Body fluid balance can be disturbed as a result of elevated body temperatures, leading to dehydration and subsequent reductions in exercise performance and greater incidences of heat related disorders (32). Carbohydrate–electrolyte fluids are widely used as oral rehydration solutions to prevent dehydration (33). Several studies have suggested that these fluids can effectively prevent dehydration in hot environments (4) and sustain thermoregulatory responses and exercise performance (5,12). The electrolytes in the fluids, mainly sodium, replace electrolytes lost in sweat and effectively maintain body fluid volume (27). Carbohydrate oral rehydration solutions may help to maintain plasma volume and blood glucose concentration and thereby sustain exercise performance (17,34). However,

Address for correspondence: Kazunobu Okazaki, Ph.D., Department of Environmental Physiology for Exercise, Osaka City University Graduate School of Medicine, 3-3-138 Sugimoto Sumiyoshi, Osaka 558-8585, Japan; E-mail: [email protected]. Submitted for publication August 2013. Accepted for publication November 2013. 0195-9131/14/4607-1452/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2014 by the American College of Sports Medicine DOI: 10.1249/MSS.0000000000000233

1452

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

induced by oral carbohydrate intake may not attenuate thermoregulatory responses; clearly, further studies are needed to address these issues. Furthermore, commercially available carbohydrate–electrolyte fluids contain fructose as well as glucose, and other forms of carbohydrates in the fluids are absorbed as fructose, as well as glucose, in the intestine (14). However, to the best of our knowledge, no studies have yet investigated the effects of fructose on thermoregulatory responses. Accordingly, we compared the effects of glucose and fructose intakes with that of water alone on the Tes threshold for cutaneous vasodilation and sweating during passive heating in humans. We hypothesized that 1) plasma hyperosmolality induced by fructose intake elevates the Tes threshold for cutaneous vasodilation and sweating and 2) the shift of the Tes threshold for cutaneous vasodilation and sweating is attenuated with glucose compared with fructose intake. The results of this study provide novel insights into the effects of the different components of oral rehydration solutions in terms of preventing dehydration, which could have direct implications for medical support staff dealing with those individuals exercising and working in warm ambient conditions.

METHODS Subjects This study was approved by the Institutional Review Board of Osaka City University Graduate School of Medicine and conformed to the Declaration of Helsinki. Ten healthy, non-heat-acclimatized young subjects (9 males and 1 female, age = 22.8 T 3.2 yr, height = 175 T 7 cm, body weight = 64.7 T 6.7 kg, body mass index = 21.2 T 1.2 kgImj2; mean T SD) were recruited for this study. The subjects were moderately active but had not participated in any regular exercise training program before the study. All subjects were informed of the purpose and procedures of this study and gave written informed consent before participation. They were nonsmokers and normotensives and had no overt history of cardiovascular or metabolic diseases or diabetes. During the experiment, none of the subjects took medications that could influence cardiovascular or thermoregulatory function, blood volume, or blood constituents. The female subject was tested during the early follicular phase of her menstrual cycle.

All trials were performed between October and May to avoid any effects of heat acclimation in summer. Subjects performed three trials with the order counterbalanced. Each trial was performed Q1 wk apart, but all three trials were completed within 6 wk, except for the female subject who completed the study in 8 wk because of her menstrual cycle. The subjects were instructed to refrain from consuming beverages containing caffeine or alcohol and to avoid vigorous exercise for 24 h before each trial. On the day of each trial, the subjects arrived at the laboratory at 0800–0900 h after fasting

MONOSACCHARIDE INTAKE AND THERMOREGULATION

Oral Fluids The test fluids were 300 mL of water alone as a control, or 300 mL of water containing either 75 g fructose or 75 g glucose. The amounts of fructose (D(j)-fructose; 127-02765; Wako Pure Chemical Industries, Ltd., Osaka, Japan) and glucose (D(+)-glucose; 049-31165; Wako Pure Chemical Industries, Ltd.) were selected based on the amount used in an oral glucose tolerance test because these amounts are known to be safe and cause measureable increases in blood glucose and insulin concentrations. The subjects and the researchers were blinded to the test fluids, except for one researcher who prepared each fluid. We did not use flavored samples to avoid unintended effects of flavoring. Measurements Esophageal and skin temperatures. Tes was measured with the thermistor probe (LT-ST08-11; Gram Co., Saitama, Japan). The change in Tes ($Tes) was calculated as the increase in Tes from just before passive heating. Skin surface temperatures were measured at five sites using thermistors (LT-ST08-12; Gram Co.) placed on the right chest (Tchest), the upper arm (Tarm), the thigh (Tthigh), the leg (Tleg), and the forearm (Tforearm). The position of each site was marked and scaled to place the thermistors in identical positions in all three trials. Tes and skin temperature data were recorded continuously at 5-s intervals. Mean skin temperature (Tsk) was calculated as 0.3 (Tchest + Tarm) + 0.2 (Tleg + Tthigh), as previously described (29).

Medicine & Science in Sports & Exercised

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

1453

APPLIED SCIENCES

Experimental Protocol

for Q10 h. To ensure that subjects started the trials well hydrated, the subjects were instructed to drink Q300 mL of water after waking in the morning. After sitting quietly for 30 min and emptying their bladders, they were weighed in the nude. Male subjects then put on short pants, and the female subjects put on short pants and a sports bra. A thermistor probe was inserted from their naris to the distance of one-quarter of their standing height to measure Tes. While the subjects sat quietly, electrocardiogram electrodes were applied to measure heart rate, and thermistor probes were applied to measure skin temperature. The subjects then entered an artificial climatic chamber (TBR-6W2S2L2M; Espec Co., Osaka, Japan) with a mean T range ambient temperature of 28.0-C T 0.1-C and relative humidity of 40% T 1%. The devices used to measure skin blood flow (SkBF), sweat rate (SR), and arterial blood pressure were applied, and a 22-G Teflon-coated catheter (SR-DS2225; Terumo, Tokyo, Japan) was inserted into the right antecubital vein while the subjects rested in a sitting position. After 30 min and confirming all of the measurement signals were in a steady state, baseline data were measured for 10 min. The subjects then drank the allocated fluid within 2 min. Twenty minutes later, the subjects put their lower legs in water controlled at 42-C for 60 min. Blood samples (15 mL) were collected immediately before and at 20, 30, 40, 60, and 80 min after fluid intake. Nude body weight was measured again immediately after passive heating.

SkBF and SR. SkBF was measured using laser-Doppler flowmetry (LDF type ALF-21D; Advance, Tokyo, Japan) at the forearm. The laser probe was placed 1 cm away from the thermistor for Tforearm, externally avoiding superficial veins. SR was measured by the ventilated capsule method (SKN2000; Nishizawa Electronic Measuring Instruments, Nagano, Japan) at forearm. A 0.785-cm2 capsule was placed proximally to the laser probe. The air following rate of the capsule was 300–600 mLIminj1. SkBF and SR data were recorded continuously at 1-s intervals. Total sweat loss was calculated as the change in nude body weight from before to after the experiment plus the weight of the test fluid. Hemodynamic and metabolic responses. Heart rate was monitored using an electrocardiogram bedside monitor (BSM-7200; Nihon Kohden Co., Tokyo, Japan), and beat-bybeat data were recorded. Systolic and diastolic blood pressures were measured every minute using a pressure cuff (oscillometric method; Nihon Kohden Co.) applied to the left ˙ O2) and carbon arm at the level of the heart. Oxygen uptake (V ˙ dioxide excretion (VCO2) were measured using a respiratory monitor (Vmax29; Sensor Medics Co., Yorba Linda, CA) continuously. Energy expenditure was calculated as 3.9  ˙ O2 + 1.1 V ˙ CO2 (41). V Blood constituents. A 1-mL aliquot of each blood sample was transferred to a heparin-treated tube immediately after collection and used to determine the hematocrit (Hct; microcentrifuge method) and hemoglobin concentration ([Hb]; SLS-hemoglobin method; Wako, Tokyo, Japan) in triplicate. Hct values were corrected by multiplying 0.96 for trapped plasma and 0.91 for the F-cell ratio. The percent change in plasma volume from baseline (%$PV) was calculated based on Hct and [Hb] using the following equation:

APPLIED SCIENCES

Q$PV ¼ 100f½HbB =½HbA  ð1jHctA  10j2 Þ=ð1jHctB  10j2 Þj100g

where B is the baseline value and A is the value at the indicated time (13). A 4-mL aliquot of each blood sample was also transferred to another heparin-treated tube and centrifuged at 5-C for 15 min. The separated plasma sample was stored at j80-C until used to measure plasma glucose and lactate concentrations ([Glu]p and [Lac]p, respectively; immobilized enzyme method; YSI 2300 STAT PLUS; YSI Inc., Yellow Springs, OH), total protein concentration ([TP]p; refractometry; ATAGO SPR-T2; Atago Co., Tokyo, Japan), osmolality (Posm; freezing point depression method; Fiske 110 Osmometer; Fiske Associates, Norwood, MA), sodium and potassium concentrations ([Na+]p and [K+]p, respectively; flame photometry; M750; Hitachi Ltd., Tokyo, Japan), and chloride concentration ([Clj]p; coulometric titration method; Chloride Analyzer M926; Corning, Halstead, UK). The remaining blood was collected in a chilled tube containing 1.5 mgImLj1 EDTA-2Na, centrifuged, and the separated plasma was stored as above until used to measure the plasma concentrations of insulin ([Ins]p; chemiluminescent enzyme immunoassay; SRL, Tokyo, Japan), catecholamine (highperformance liquid chromatography; SRL), and antidiuretic

1454

Official Journal of the American College of Sports Medicine

hormone (ADH; double antibody radioimmunoassay; SRL). The intra-assay coefficients of variation were as follows: 1.71%, 1.11%, and 2.11% for insulin at 5.3, 56.3, and 180.5 KIUImL–1, respectively; 1.00%, 0.45%, and 0.36% for noradrenaline at 356, 990, and 3577 pgImL–1, respectively; 2.79%, 1.13%, and 2.19% for adrenaline at 136, 363, and 2279 pgImL–1, respectively; 2.40%, 3.48%, and 0.38% for dopamine at 170, 392, and 17919 pgImL–1, respectively; and 8.69%, 7.19%, and 14.08% for ADH at 3.4, 5.8, and 18.6 pgImL–1, respectively. Data Analysis Cutaneous vascular conductance (CVC) was calculated as SkBF divided by mean arterial pressure and is expressed as the percent change from baseline. The Tes threshold for cutaneous vasodilation (THCVC) and sweating (THSR) and the sensitivity of the increase in CVC and SR for a given increase in Tes were determined from a scatterplot of $Tes versus the percent change in CVC or change in SR from before passive heating in each subject by two different investigators who were blinded to the subject and trials, and averaged data are reported. The typical error values for the determination of the THCVC and THSR obtained from multiple analyses of 10 data sets by the investigators were 0.04-C and 0.02-C, or 9.6% and 5.0% as coefficient of variation, respectively. Statistics A two-way (trial  time) repeated-measures ANOVA was used to test the effects of trial (i.e., water alone, fructose, and glucose) and time. The effects of trial on THCVC and THSR and the sensitivity of the increase in CVC and SR for a given increase in Tes were tested by one-way repeated-measures ANOVA. Subsequent post hoc tests to determine significant differences in pairwise comparisons were performed using the Student–Newman–Keuls test. The Pearson’s product– moment correlation coefficient was used for correlation analysis between variables. To assess the relationship between the increase in [Ins]p and THCVC or THSR, we applied the correlation analysis on the pooled data from fructose and glucose intake trials because [Ins]p increased after both fructose and glucose intake, with a similar increase in Posm compared with water intake. The null hypothesis was rejected at P G 0.05.

RESULTS As shown in Table 1, there were no significant differences ˙ CO2 in hemodynamics among the three trials. Although V was significantly higher after fructose intake compared with water alone (P G 0.048) and at 40 to 60 min after glucose intake (P G 0.038), there were no significant differences in ˙ O2 and energy expenditure among the three trials. V Figure 1 shows the [Glu]p, [Ins]p, and Posm responses in each trial. [Glu]p increased rapidly after glucose intake and reached its highest values at 40 min. As expected, [Glu]p was significantly higher after glucose intake than after fructose or water intake throughout the experiment (P G 0.001).

http://www.acsm-msse.org

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose

66.1 63.7 65.8 105 104 105 65 63 63 186 214 197 160 196 165 0.90 1.05 0.95

T T T T T T T T T T T T T T T T T T 4.0 4.3 4.2 2 3 3 3 3 3 10 13 12 9 26 10 0.05 0.08 0.06

0 min 66.0 63.8 66.6 106 108 103 66 62 60 200 220 207 172 234 175 0.97 1.12 1.00

T T T T T T T T T T T T T T T T T T 3.8 4.9 4.2 2 3*** 2 2 3 2*** 12*** 17 8*** 10*** 34*,*** 7 0.06*** 0.10*** 0.04***

20 min 69.4 70.8 69.5 105 108 105 63 63 59 194 221 209 167 242 184 0.94 1.13 1.02

T T T T T T T T T T T T T T T T T T 4.2*** 5.5*** 4.9*** 2 4*** 3 2 4 2*** 10*** 16 9*** 9 37*,*** 8*** 0.05*** 0.10*** 0.04***

30 min 77.1 76.2 74.9 109 111 106 62 63 59 214 253 224 190 276 210 1.04 1.29 1.01

T T T T T T T T T T T T T T T T T T 4.4*** 5.9*** 4.6*** 3*** 4*** 3 2*** 4 3*** 9*** 16*** 7*** 9*** 37*,*** 9**,*** 0.05*** 0.10*** 0.04***

40 min 81.9 85.5 82.7 111 113 109 61 61 57 229 259 233 201 284 219 1.11 1.32 1.15

T T T T T T T T T T T T T T T T T T 5.4*** 6.0*** 5.0*** 3*** 4*** 3*** 3*** 3 2*** 12*** 17*** 11*** 11*** 38*,*** 11**,*** 0.06*** 0.11*** 0.05***

60 min 85.6 90.6 88.2 112 112 110 60 59 57 231 259 245 198 278 225 1.12 1.32 1.20

T T T T T T T T T T T T T T T T T T 4.6*** 6.0*** 4.9*** 4*** 4*** 4*** 3*** 3*** 2*** 15*** 14*** 13*** 14*** 33*,*** 13*** 0.08*** 0.09*** 0.06***

80 min 0.964

0.471

0.333

0.083

0.043

0.058

G0.001

G0.001

G0.001

G0.001

G0.001

Trial

G0.001

Time

Values are presented as mean T SEM for 10 subjects. *P G 0.05 compared with water. **P G 0.05 compared with fructose. ***P G 0.05 compared with 0 min. SBP, systolic blood pressure; DBP, diastolic blood pressure; V˙O2, oxygen uptake; V˙CO2, carbon dioxide excretion; P values for the effects of time and trial were assessed by two-way repeated-measures ANOVA.

Energy expenditure, kcalIminj1

V˙CO2, mLImin

j1

V˙O2, mLIminj1

DBP, mm Hg

SBP, mm Hg

Heart rate, bpm

Trial

TABLE 1. Hemodynamic and metabolic responses in each trial.

[Glu]p increased slightly after fructose intake and was significantly higher at 40 to 60 min compared with water alone (P G 0.038). [Ins]p increased after fructose and glucose intake and was significantly higher in both trials compared with water intake throughout the experiment (P G 0.016 and P G 0.001, respectively). In addition, the increase in [Ins]p was significantly higher after glucose intake than after fructose intake

Medicine & Science in Sports & Exercised

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

1455

APPLIED SCIENCES

MONOSACCHARIDE INTAKE AND THERMOREGULATION

FIGURE 1—Plasma glucose concentration ([Glu]p, A), insulin concentration ([Ins]p, B), and plasma osmolality (Posm, C) throughout the experiment. Open circles, water alone; open squares, fructose; closed squares, glucose. Values are presented as mean T SEM for 10 subjects. #P G 0.05 compared with water alone. †P G 0.05 compared with fructose. *P G 0.05 compared with 0 min.

P

0.424

G0.001

0.603

0.299

0.186

G0.001

Time  Trial

(P G 0.001) by three to four times. Posm increased similarly after fructose and glucose intake and was significantly higher in both trials compared with water intake throughout the experiment (P G 0.016), except at 80 min after fructose intake. At 30 min, Posm was significantly higher after fructose (290 T 1 mOsmIkg H2Oj1) and glucose intake (289 T 1 mOsmIkg H2Oj1) than after water intake (284 T 1 mOsmIkg H2Oj1) by 6.0 and 5.0 mOsmIkg H2Oj1, respectively. Table 2 shows the effects of fluid intake on other blood constituents. PV decreased gradually during passive heating in all three trials, although no significant differences were found among the trials. [Lac]p increased rapidly after fructose intake and was significantly higher than after glucose or water intake throughout the experiment. By contrast, [Lac]p increased at a slower rate after glucose intake and was significantly higher at 60 to 80 min compared with water intake. There were no significant differences in plasma electrolyte concentrations throughout the experiment between any trials. Plasma catecholamine concentrations increased gradually during passive heating in all trials but were not significantly different among the trials. Plasma ADH concentration increased gradually after fructose and glucose intake and reached significantly higher levels at 60 to 80 min from before intake, without significant difference between the trials. Although passive heating increased Tes, Tsk, and Tforearm in all three trials, these were not significantly different among

the three trials throughout the experiment (Table 3). Figure 2 shows the percent changes in CVC and the changes in SR in response to increased Tes during passive heating and the Tes threshold for cutaneous vasodilation and sweating. The responses showed a rightward shift after fructose intake but not after glucose intake, indicating attenuated thermoregulatory responses after fructose intake compared with water intake alone. The THCVC was significantly higher after fructose intake than after water intake (P G 0.001) or glucose intake (P G 0.001). On the other hand, the THCVC was not significantly different between glucose and water intake (P = 0.404). Similarly, the THSR was significantly higher after fructose intake compared with water alone (P = 0.023) and with glucose intake (P = 0.004). In contrast, the THSR was not significantly different between glucose intake and water alone (P = 0.422). There were no significant differences in the sensitivity of the increase in CVC (2055 T 644%I-Cj1 after water, 2206 T 641%I-Cj1 after fructose, and 2822 T 901%I-C j1 after glucose, P = 0.556) and SR for a given increase in Tes (0.99 T 0.28 mgIcm j2Iminj1I-Cj1 after water, 0.74 T 0.09 mgIcm j2 Imin j1 I-C j1 after fructose, and 0.87 T 0.12 mgIcmj2Iminj1I-Cj1 after glucose, P = 0.643). Finally, as shown in Figure 3, the THCVC and THSR after fructose and glucose intake were negatively correlated with the increase in [Ins]p from before intake at the time when the Tes threshold was found. We confirmed that the THCVC and

TABLE 2. Blood constituents in each trial. P Trial %$PV, % j1

[Lac]p, mmolIkg H2O

j1

+

[Na ]p, mEqIkg H2O

[K+]p, mEqIkg H2Oj1 j

j1

[Cl ]p, mEqIkg H2O

j1

APPLIED SCIENCES

Noradrenaline, pgImL

Adrenaline, pgImLj1

Dopamine, pgImL j1

ADH, pgImL

j1

Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose

0 min

20 min

30 min

— j0.9 T 1.1 j1.2 T 0.8 j1.4 — j3.1 T 1.0*** j1.2 T 2.8 j3.1 — j1.5 T 0.8 j0.4 T 0.8 0.2 1.2 T 0.1 1.2 T 0.1 1.3 T 0.1 1.3 , , 3.6 1.3 T 0.1 2.1 T 0.2* *** 3.0 T 0.3* *** , 1.2 T 0.1 1.2 T 0.1** 1.5 T 0.1** *** 1.7 157 T 0 157 T 1 157 T 0 157 158 T 0 158 T 0 158 T 0 158 157 T 0 157 T 1 157 T 1 156 4.7 T 0.2 4.8 T 0.2 4.8 T 0.3 4.8 4.8 T 0.2 4.5 T 0.1*** 4.4 T 0.1*** 4.4 4.7 T 0.1 4.6 T 0.2 4.5 T 0.2*** 4.6 101 T 1 99 T 1*** 99 T 1*** 99 100 T 1 100 T 1 101 T 1 100 99 T 1 99 T 1 100 T 1 100 303 T 36 319 T 36 295 T 29 284 268 T 21 307 T 28 306 T 29 290 265 T 28 300 T 34 285 T 29 272 43 T 11 31 T 6*** 36 T 7 52 39 T 7 33 T 7 36 T 8 53 45 T 9 31 T 8*** 28 T 6*** 34 7.9 T 1.1 10.0 T 1.5*** 7.7 T 1.0 8.1 7.0 T 0.8 6.8 T 0.8 9.4 T 1.1*** 11.1 6.8 T 1.0 6.8 T 1.0 8.0 T 1.7 9.3 1.32 T 0.08 1.22 T 0.02 1.31 T 0.11 1.24 1.2 T 0 1.29 T 0.08 1.56 T 0.24 1.51 1.32 T 0.12 1.42 T 0.15 1.34 T 0.07 1.5

40 min T T T T T T T T T T T T T T T T T T T T T T T T T T T

0.8 j5.8 1.8*** j3.3 0.9 j1.7 0.1 1.2 , 0.4* *** 4.0 , 0.2** *** 2.0 0 157 0 157 0 156 0.3 4.9 0.1*** 4.2 0.2 4.3 1*** 100 1 102 1 100 29 324 30 324 28 326 9*** 67 12*** 60 6*** 49 1.5 8.7 1.0*** 9.5 1.7*** 7.3 0.03 1.46 0.22 2.08 0.14 1.89

60 min T T T T T T T T T T T T T T T T T T T T T T T T T T T

0.8*** j6.0 2.7*** j3.5 1.1*** j3.7 0.1 1.1 , 0.2* *** 3.8 , , 0.2* ** *** 2.0 0 158 0 158 1 157 0.4 4.7 0.1*** 4.2 0.1*** 4.3 1 100 1*** 102 1*** 100 36 335 32*** 351 36*** 367 10*** 76 9*** 73 8 59 1.1 9.4 1.2*** 10.2 1.1 11.0 0.13 1.56 0.49*** 2.19 0.23*** 2.06

80 min T T T T T T T T T T T T T T T T T T T T T T T T T T T

0.6*** 2.3*** 1.0*** 0.1 0.2*,*** 0.2*,**,*** 0 0 1 0.3 0.2*** 0.1*** 1 1*** 1*** 32 31*** 39*** 10*** 10*** 13*** 1.3 1.3*** 1.6*** 0.19 0.40*** 0.24***

Time

Trial Time  Trial

G0.001 0.812

0.021

G0.001 G0.001

G0.001

0.298 0.235

0.298

0.011 0.14

0.273

0.013 0.348

0.034

0.008 0.942

0.567

G0.001 0.316

0.172

0.044 0.815

0.142

G0.001 0.08

0.004

Values are presented as mean T SEM for 10 subjects. %$PV, percent change in plasma volume; [Lac]p, plasma lactate concentration; [Na+ ]p, [K+ ]p, and [Cl– ]p, plasma sodium, potassium, and chloride concentrations, respectively. P values for the effects of time and trial were assessed by two-way repeated-measures ANOVA. *P G 0.05 compared with water. **P G 0.05 compared with fructose. ***P G 0.05 compared with 0 min. ADH, plasma antidiuretic hormone concentration.

1456

Official Journal of the American College of Sports Medicine

http://www.acsm-msse.org

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

TABLE 3. Esophageal and skin temperature responses in each trial. P Trial Tes,-C

Tsk,-C

Tforearm,-C

Water Fructose Glucose Water Fructose Glucose Water Fructose Glucose

0 min 36.84 36.69 36.70 33.09 33.11 33.20 32.16 32.30 32.78

T T T T T T T T T

0.10 0.09 0.05 0.24 0.22 0.21 0.39 0.27 0.23

20 min 36.71 36.60 36.59 33.13 33.16 33.26 32.02 32.08 32.71

T T T T T T T T T

0.11 0.10 0.05 0.21 0.22 0.19 0.36 0.21 0.20

30 min 36.76 36.67 36.62 34.83 34.58 34.79 32.12 32.09 32.80

T T T T T T T T T

0.09 0.09 0.05 0.29 0.28 0.30 0.37 0.24 0.23

40 min 37.11 37.03 36.95 34.75 34.56 34.94 32.16 32.50 32.95

T T T T T T T T T

0.09* 0.10* 0.05* 0.27 0.23* 0.22 0.35 0.31 0.23

60 min 37.34 37.40 37.25 34.78 34.69 35.00 32.28 33.08 32.80

T T T T T T T T T

80 min

0.11* 0.08* 0.05* 0.33* 0.32* 0.33* 0.28 0.34* 0.31

37.36 37.37 37.26 34.75 34.90 34.85 32.77 33.81 33.27

T T T T T T T T T

0.10* 0.07* 0.06* 0.37* 0.33* 0.37* 0.33* 0.34* 0.28*

Time

Trial

Time  Trial

G0.001

0.454

0.100

G0.001

0.282

0.399

G0.001

0.144

G0.001

Values are presented as mean T SEM for 10 subjects. Tes, esophageal temperature; Tsk, mean skin temperature; Tfoream, forearm temperature. P values for the effects of time and trial were assessed by two-way repeated-measures ANOVA. *P G 0.05 compared with 0 min.

THSR in each subject were lowered with a higher [Ins]p after glucose intake than fructose intake in 9 of 10 subjects.

DISCUSSION The major findings of the present study are as follows: 1) THCVC and THSR increased after fructose intake compared with water intake, indicating the attenuation of thermoregulatory responses following the fructose-induced increase in Posm; and 2) the upward shift of the THCVC and THSR was absent after glucose intake, although Posm increased in the same manner as after fructose intake. [Ins]p increased after both glucose and fructose intake, although the size of the increase was considerably smaller after fructose than glucose intake. The increased [Ins]p after glucose intake may be

associated with the absence of an upward shift of either THCVC or THSR. Effects of fructose intake on the Tes threshold for thermoregulation. It has been suggested that thermoregulatory responses are attenuated by plasma hyperosmolality induced by hypertonic saline infusion as well as by thermal dehydration (9). Takamata et al. (38) reported that intravenous infusion of hypertonic saline (2% or 3% NaCl) before passive heating by immersing the lower legs in hot water for 60 min increased the Tes threshold for cutaneous vasodilation and sweating in proportion to plasma hyperosmolality, by 0.044-C and 0.034-C, respectively, to 1 mOsmIkg H2Oj1 increase in Posm, independently of changes in PV. In the present study, the observed increase in Posm after fructose intake from water intake at the time when THCVC and THSR

MONOSACCHARIDE INTAKE AND THERMOREGULATION

Medicine & Science in Sports & Exercised

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

1457

APPLIED SCIENCES

FIGURE 2—Percent changes in cutaneous vascular conductance (%$CVC, A) and changes in SR ($SR, B) in response to changes in esophageal temperature ($Tes) during passive heating, and the esophageal temperature threshold for cutaneous vasodilation (THCVC, C) and for sweating (THSR, D). Open circles, water alone; open squares, fructose; closed squares, glucose. Values are shown as minute average for 10 subjects with the error bars (SEM) every 5 min for A and B. Values in C and D are presented as mean T SEM for 10 subjects. *P G 0.05.

APPLIED SCIENCES

FIGURE 3—The relationship between the increase in plasma insulin concentration ($[Ins]p) and esophageal temperature threshold for cutaneous vasodilation (THCVC, A) or sweating (THSR, B) after fructose (open squares) and glucose intake (closed squares). $[Ins]p was calculated as the increase in plasma insulin concentration from before intake at the time when the THCVC or THSR was found. Individual values after fructose and glucose intake are connected with a dashed line.

were observed was 5.43 mOsmIkg H2Oj1 for THCVC and 5.14 mOsmIkg H2Oj1 for THSR. The increase in Posm was smaller than the previous study; however, based on these values, an increase in THCVC and THSR with the increased Posm after fructose intake was estimated as 0.239-C and 0.175-C, respectively. The observed increases in THCVC of 0.198-C and THSR of 0.125-C showed similar, although slightly lower, values to those estimated. More importantly, it was reported that an increase in Posm induced by hypertonic saline or nonsodium osmols of mannitol infusion caused a similar excessive increase in rectal temperature during exercise in dogs, indicating that the attenuation in thermoregulation was due to increased Posm rather than the sodium concentration (21). In rats, it was found that the activity of warm-sensitive neurons was similarly suppressed by perfusion with hypertonic NaCl or mannitol solution (26). As expected, we found no significant differences in [Na+]p among the three trials, but Posm was increased by fructose and glucose intake (Table 2 and Fig. 1). Notably, there were no significant differences in %$PV among the trials, which has been reported to significantly affect thermoregulation independently of Posm (25). From these observations, we assume that the elevated THCVC and THSR after fructose intake as compared with water intake were caused, at least in part, by an increase in Posm. However, we cannot exclude the possibility that other unknown mechanisms of fructose are associated with our observations. The increased [Lac]p as a result of fructose metabolism might also explain the attenuated thermoregulatory responses following fructose intake. As shown in Table 2, [Lac]p was significantly higher after fructose intake than after water alone. It was previously reported that an increase in [Lac]p during exercise was associated with a decrease in the slope (i.e., sensitivity) of the increase in forearm CVC for a given increase in Tes, and it was suggested that muscle metaboreceptors were involved in the response (23). Regarding the effects of muscle metaboreceptors on thermoregulatory responses, another study showed that forearm CVC was decreased whereas forearm SR was increased during activation of muscle metaboreceptors

1458

Official Journal of the American College of Sports Medicine

with isometric handgrip exercise and subsequent postexercise ischemia in passively hyperthermic subjects (6). In contrast to these previous observations, in the present study, we found no significant differences among the three trials in the sensitivity of the increases in CVC and SR to a given increase in Tes. Moreover, we found increased Tes threshold both for cutaneous vasodilation and sweating with the increased [Lac]p after ˙ CO2, which would fructose intake. Fructose intake increased V be a result of compensated respiratory alkalosis to the increased ˙ O2 and EE, indicating no effect on [Lac]p, but did not increase V heat production. Therefore, the increase in [Lac]p after fructose intake in the present study might not be associated with the observed increase in Tes threshold for thermoregulation. It has been reported that the antiepilepsy drug topiramate, which is a sulfamate-substituted monosaccharide derivative of fructose, inhibits the sweating response in human, although the exact mechanism remains unknown (16). Arcas et al. (1) reported that sweat gland density in response to pilocarpine administration by iontophoresis was reduced in patients with epilepsy treated by topiramate, that the patients developed hypohidrosis, and that these symptoms disappeared after drug suppression. It is possible that fructose has similar effects as topiramate. However, there were no significant differences among trials either in local SR, or in the sensitivity of the increase in SR for a given increase in Tes, in the present study, indicating that sweat gland function was not decreased after fructose intake. Thus, in the present study, these possible mechanisms would not be associated with the observed increase in the Tes threshold for thermoregulation after fructose intake, although it is possible that other unknown mechanisms of fructose are associated with these observations. Effects of Glucose Intake on the Tes Threshold for Thermoregulation As we expected, the upward shift in the Tes threshold for cutaneous vasodilation and sweating after fructose intake was absent after glucose intake (Fig. 2), although Posm,

http://www.acsm-msse.org

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

MONOSACCHARIDE INTAKE AND THERMOREGULATION

glucose concentrations. DeFronzo (8) demonstrated that insulin stimulates the reabsorption of sodium in the kidney to reduce sodium excretion. The response in %$PV after glucose intake might be associated with the increased [Ins]p. However, we observed no significant differences in [Na+]p or %$PV among the three trials (Table 2); therefore, the possible effects of insulin on sodium and water balance and consequently on PV are unlikely to contribute to the present observations. Oral glucose intake is known to attenuate plasma catecholamine concentrations (10,11) because increased insulin concentrations modulate the release of catecholamine from the hypothalamus (31). Importantly, reductions in plasma catecholamine concentrations attributed to increases in blood glucose levels are associated with enhanced thermoregulatory responses after intravenous glucose infusion as compared with saline infusion (24), although the precise mechanism is not fully understood. In the present study, however, we found no differences in plasma catecholamine concentrations among the three trials (Table 2). Thus, changes in catecholamine concentrations associated with oral glucose intake are not involved in the attenuation of the rise in the Tes threshold for cutaneous vasodilation and sweating after glucose intake as compared with fructose intake. Limitations. We assumed, but did not prove, that endogenous insulin might improve hyperosmolality-induced impaired thermoregulatory response, and our observations were not sufficient to clarify the mechanisms. Further studies are required to prove the possible effects of endogenous insulin on thermoregulatory responses. We suggested that the elevated THCVC and THSR after fructose intake were caused by the increase in Posm. However, we found no significant correlation between the increase in Posm after fructose intake and the increase in THCVC and THSR. This may be because the increase in Posm was relatively small compared with previous studies (38) and because we only investigated one concentration of the test fluids. In addition, the wide interindividual variation in the hyperosmolalityinduced right-ward shift of the Tes threshold for thermoregulation associated with the levels of sweat sodium concentration (39) or blood volume (15) may hide the possible relationship between Posm and Tes threshold. Moreover, in the present study, the increased [Ins]p after fructose intake might also confound the possible relationship. The present observations were obtained in young, healthy individuals. The possible effects of oral carbohydrate intake on thermoregulation would be different in subjects whose thermoregulatory or metabolic function is deteriorated as in the elderly (20,22) or diabetic patients (42,43). We used lower leg immersion in hot water to increase body core temperature in the present study because we wanted to evaluate the Tes threshold for cutaneous vasodilation and sweating without the effects of changes in local skin temperature. Skin temperature at the site where CVC and SR was measured remained unchanged during passive heating until the Tes threshold was observed in all subjects (È30–40 min after oral fluid intake) as

Medicine & Science in Sports & Exercised

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

1459

APPLIED SCIENCES

plasma electrolyte concentrations, and %$PV were similar in both trials. Previous studies showed an attenuated increase in Tes during exercise after intravenous glucose infusion (24) or oral glucose intake (7) as compared with saline infusion trial or no intake trial. Thus, glucose may have some effects which enhance heat dissipative mechanisms. As shown in Figure 3, we found a significant negative linear correlation between the THCVC or THSR and the increase in [Ins]p from before intake to the time where the Tes threshold was found in pooled data from the fructose and glucose intake trials. We further confirmed that the THCVC and the THSR in each subject were lowered, with a higher [Ins]p after glucose intake than after fructose intake, in 9 of 10 subjects. These observations indicate that the increase in endogenous insulin after glucose intake may contribute to the enhanced thermoregulatory response. Insulin can reportedly cross the blood–brain barrier and activate insulin receptors in the brain, including in the hypothalamus (30). However, there are few studies examining the effects of insulin on thermoregulatory responses in humans. In rats, direct injection of insulin into the preoptic area of the hypothalamus induced a specific and dose-dependent increase in body core temperature in combination with increased thermogenesis in brown adipose tissue, which was activated by insulin receptor-expressing warmsensitive neurons (30). These results indicate that insulin modulates thermoregulatory responses via central mechanisms, although these observations in rats differ from the present results in humans. In another human study, it was suggested that insulin administration increases skin sympathetic nerve activity with a concomitant increase in cutaneous vasodilation and sweating, although these results were observed under insulin-induced hypoglycemia, which may affect the outcomes (2). In addition, Passias et al. (28) reported that hypoglycemia attenuated thermogenesis in a cold environment by showing a decreased Tes threshold for shivering during hypoglycemia compared with euglycemia. In that study, [Ins]p was clamped to the same level between trials; therefore, the effects of insulin on thermoregulation remained unclear. Coupled with the present results, the increase in endocrine insulin following glucose intake may enhance thermoregulatory responses via central mechanisms, although further studies are required to determine the mechanisms. Insulin has been reported to have vasodilatory effects in the cutaneous vasculatures (35) as well as in skeletal muscle vasculature (44), indicating that insulin may also enhance thermoregulatory responses via peripheral mechanisms. Insulin appears to induce vasodilation by facilitating the synthesis and release of nitric oxide (NO), particularly by endothelial NO synthase (eNOS) (37). However, it was reported that eNOS is stimulated by local heating but not by whole body heating (19). In addition, the inhibition of NOS did not affect the Tes threshold for cutaneous vasodilation (18) or sweating (36). Thus, the vasodilatory properties of insulin may not be associated with the present observations. It has been reported that insulin is closely related to sodium balance by altering renal sodium transport independently of

in Table 3. The present observations may be different in conditions that local skin temperature is changed. Although the concentration of both test solutions was 20%, which is higher than that of beverages commonly used to prevent dehydration and/or heat disorders, the amount of carbohydrate in the test solutions (75 g) can be taken by drinking commonly available beverages. Thus, the effects of carbohydrates on thermoregulation should be considered when determining the composition of the beverages. In conclusion, the Tes threshold for cutaneous vasodilation and sweating was elevated, indicating attenuated thermoregulatory responses, after fructose intake with increased Posm. By contrast, the upward shift of the Tes threshold was absent after glucose intake. Thus, orally ingested glucose

and fructose have different effects on thermoregulatory responses, and the carbohydrate component of oral rehydration fluids for preventing dehydration and/or heat disorders should therefore be considered. This study was supported in part by a Grant-in-Aid for Young Scientists A 23689014 and Challenging Exploratory Research 25560372 (to K. Okazaki) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The authors are very grateful to the volunteers who participated in this study. They also thank Dr. Takaaki Okumoto from their laboratory and Dr. Shinya Matsumura from the Sport Science and Medical Science, Osaka University of Health and Sport Science, for useful comments and suggestions regarding this manuscript. The authors declare that they have no conflict of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine.

APPLIED SCIENCES

REFERENCES 1. Arcas J, Ferrer T, Roche MC, Martinez-Bermejo A, Lopez-Martin V. Hypohidrosis related to the administration of topiramate to children. Epilepsia. 2001;42(10):1363–5. 2. Berne C, Fagius J. Skin nerve sympathetic activity during insulininduced hypoglycaemia. Diabetologia. 1986;29(12):855–60. 3. Carter JE, Gisolfi CV. Fluid replacement during and after exercise in the heat. Med Sci Sports Exerc. 1989;21(5):532–9. 4. Coyle EF, Montain SJ. Benefits of fluid replacement with carbohydrate during exercise. Med Sci Sports Exerc. 1992;24(9 suppl): S324–30. 5. Coyle EF, Montain SJ. Carbohydrate and fluid ingestion during exercise: are there trade-offs? Med Sci Sports Exerc. 1992;24(6): 671–8. 6. Crandall CG, Stephens DP, Johnson JM. Muscle metaboreceptor modulation of cutaneous active vasodilation. Med Sci Sports Exerc. 1998;30(4):490–6. 7. Dearborn AS, Ertl AC, Jackson CG, Barnes PR, Breckler JL, Greenleaf JE. Effect of glucose-water ingestion on exercise thermoregulation in men dehydrated after water immersion. Aviat Space Environ Med. 1999;70(1):35–41. 8. DeFronzo RA. The effect of insulin on renal sodium metabolism. A review with clinical implications. Diabetologia. 1981;21(3): 165–71. 9. Fortney SM, Wenger CB, Bove JR, Nadel ER. Effect of hyperosmolality on control of blood flow and sweating. J Appl Physiol Respir Environ Exerc Physiol. 1984;57(6):1688–95. 10. Galbo H, Christensen NJ, Holst JJ. Glucose-induced decrease in glucagon and pinephrine responses to exercise in man. J Appl Physiol Respir Environ Exerc Physiol. 1977;42(4):525–30. 11. Galbo H, Holst JJ, Christensen NJ. The effect of different diets and of insulin on the hormonal response to prolonged exercise. Acta Physiol Scand. 1979;107(1):19–32. 12. Gonzalez-Alonso J, Calbet JA, Nielsen B. Muscle blood flow is reduced with dehydration during prolonged exercise in humans. J Physiol. 1998;513( Pt 3):895–905. 13. Greenleaf JE, Convertino VA, Mangseth GR. Plasma volume during stress in man: osmolality and red cell volume. J Appl Physiol. 1979;47(5):1031–8. 14. Guyton AC, Hall JE. Textbook of Medical Physiology. Philadelphia (PA): Elsevier Inc; 2006. pp. 808–25. 15. Ichinose T, Okazaki K, Masuki S, et al. Ten-day endurance training attenuates the hyperosmotic suppression of cutaneous vasodilation during exercise but not sweating. J Appl Physiol (1985). 2005;99(1): 237–43.

1460

Official Journal of the American College of Sports Medicine

16. Incecik F, Herguner MO, Altunbasak S. Hypohidrosis and hyperthermia during topiramate treatment in children. Turk J Pediatr. 2012;54(5):515–8. 17. Kamijo Y, Ikegawa S, Okada Y, et al. Enhanced renal Na+ reabsorption by carbohydrate in beverages during restitution from thermal and exercise-induced dehydration in men. Am J Physiol Regul Integr Comp Physiol. 2012;303(8):R824–33. 18. Kellogg DL Jr, Crandall CG, Liu Y, Charkoudian N, Johnson JM. Nitric oxide and cutaneous active vasodilation during heat stress in humans. J Appl Physiol (1985). 1998;85(3):824–9. 19. Kellogg DL Jr, Zhao JL, Wu Y. Endothelial nitric oxide synthase control mechanisms in the cutaneous vasculature of humans in vivo. Am J Physiol Heart Circ Physiol. 2008;295(1):H123–9. 20. Kenney WL, Morgan AL, Farquhar WB, Brooks EM, Pierzga JM, Derr JA. Decreased active vasodilator sensitivity in aged skin. Am J Physiol. 1997;272(4 pt 2):H1609–14. 21. Kozlowski S, Greenleaf JE, Turlejska E, Nazar K. Extracellular hyperosmolality and body temperature during physical exercise in dogs. Am J Physiol. 1980;239(1):R180–3. 22. Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW. Decreased nitric oxide- and axon reflex-mediated cutaneous vasodilation with age during local heating. J Appl Physiol (1985). 2002;93(5):1644–9. 23. Mitono H, Endoh H, Okazaki K, et al. Acute hypoosmolality attenuates the suppression of cutaneous vasodilation with increased exercise intensity. J Appl Physiol (1985). 2005;99(3):902–8. 24. Mora-Rodriguez R, Gonzalez-Alonso J, Below PR, Coyle EF. Plasma catecholamines and hyperglycaemia influence thermoregulation in man during prolonged exercise in the heat. J Physiol. 1996;491 ( Pt 2):529–40. 25. Nadel ER, Fortney SM, Wenger CB. Effect of hydration state of circulatory and thermal regulations. J Appl Physiol Respir Environ Exerc Physiol. 1980;49(4):715–21. 26. Nakashima T, Hori T, Kiyohara T, Shibata M. Osmosensitivity of preoptic thermosensitive neurons in hypothalamic slices in vitro. Pflugers Arch. 1985;405(2):112–7. 27. Nose H, Mack GW, Shi XR, Nadel ER. Role of osmolality and plasma volume during rehydration in humans. J Appl Physiol (1985). 1988;65(1):325–31. 28. Passias TC, Meneilly GS, Mekjavic IB. Effect of hypoglycemia on thermoregulatory responses. J Appl Physiol (1985). 1996;80(3): 1021–32. 29. Ramanathan NL. A new weighting system for mean surface temperature of the human body. J Appl Physiol. 1964;19:531–3.

http://www.acsm-msse.org

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

30. Sanchez-Alavez M, Tabarean IV, Osborn O, et al. Insulin causes hyperthermia by direct inhibition of warm-sensitive neurons. Diabetes. 2010;59(1):43–50. 31. Sauter A, Goldstein M, Engel J, Ueta K. Effect of insulin on central catecholamines. Brain Res. 1983;260(2):330–3. 32. Sawka MN. Physiological consequences of hypohydration: exercise performance and thermoregulation. Med Sci Sports Exerc. 1992;24(6): 657–70. 33. Sawka MN, Burke LM, Eichner ER, Maughan RJ, Montain SJ, Stachenfeld NS. American College of Sports Medicine Position Stand. Exercise and fluid replacement. Med Sci Sports Exerc. 2007; 39(2):377–90. 34. Seidman DS, Ashkenazi I, Arnon R, Shapiro Y, Epstein Y. The effects of glucose polymer beverage ingestion during prolonged outdoor exercise in the heat. Med Sci Sports Exerc. 1991;23(4): 458–62. 35. Serne EH, RG IJ, Gans RO, et al. Direct evidence for insulininduced capillary recruitment in skin of healthy subjects during physiological hyperinsulinemia. Diabetes. 2002;51(5):1515–22. 36. Shastry S, Dietz NM, Halliwill JR, Reed AS, Joyner MJ. Effects of nitric oxide synthase inhibition on cutaneous vasodilation during body heating in humans. J Appl Physiol (1985). 1998;85(3): 830–4. 37. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. Insulin-mediated skeletal muscle vasodilation is nitric oxide

38.

39.

40.

41. 42.

43.

44. 45.

dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest. 1994;94(3):1172–9. Takamata A, Nagashima K, Nose H, Morimoto T. Osmoregulatory inhibition of thermally induced cutaneous vasodilation in passively heated humans. Am J Physiol. 1997;273(1 Pt 2):R197–204. Takamata A, Yoshida T, Nishida N, Morimoto T. Relationship of osmotic inhibition in thermoregulatory responses and sweat sodium concentration in humans. Am J Physiol Regul Integr Comp Physiol. 2001;280(3):R623–9. Thrasher TN, Brown CJ, Keil LC, Ramsay DJ. Thirst and vasopressin release in the dog: an osmoreceptor or sodium receptor mechanism? Am J Physiol. 1980;238(5):R333–9. Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol. 1949;109(1–2):1–9. Wick DE, Roberts SK, Basu A, et al. Delayed threshold for active cutaneous vasodilation in patients with type 2 diabetes mellitus. J Appl Physiol (1985). 2006;100(2):637–41. Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. Impaired nitric oxide-mediated vasodilation in patients with non-insulindependent diabetes mellitus. J Am Coll Cardiol. 1996;27(3):567–74. Yki-Jarvinen H, Utriainen T. Insulin-induced vasodilatation: physiology or pharmacology? Diabetologia. 1998;41(4):369–79. Zerbe RL, Robertson GL. Osmoregulation of thirst and vasopressin secretion in human subjects: effect of various solutes. Am J Physiol. 1983;244(6):E607–14.

APPLIED SCIENCES

MONOSACCHARIDE INTAKE AND THERMOREGULATION

Medicine & Science in Sports & Exercised

Copyright © 2014 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.

1461

Thermoregulatory responses are attenuated after fructose but not glucose intake.

We examined whether plasma hyperosmolality induced by oral monosaccharide intake attenuated thermoregulatory responses and whether the responses were ...
365KB Sizes 0 Downloads 0 Views