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ARTICLE Mouth rinsing with a carbohydrate solution does not influence cycle time trial performance in the heat1 Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by Fudan University on 05/10/15 For personal use only.
Phillip Watson, David Nichols, and Philip Cordery
Abstract: Ten endurance-trained males were recruited to examine the possible role of carbohydrate (CHO) receptors in the mouth influencing exercise performance in the heat. Volunteers completed an incremental test to exhaustion to determine peak oxygen uptake, a familiarisation trial, followed by 2 experimental trials. Trials consisted of a 1-h time trial undertaken in a climatic chamber maintained at 30 °C, 60% relative humidity. Immediately before, and at regular intervals throughout exercise, subjects ingested a bolus of water and then were provided with either a placebo (PLA) or a 6.4% glucose (CHO) solution to rinse in the mouth for 10 s before being expectorated. There was no difference in total work done between the PLA and CHO trials (758.8 ± 149.0 kJ; 762.6 ± 141.1 kJ; P = 0.951). Pacing was also similar, with no differences in power output apparent during the experimental trials (P = 0.546). Core temperature (P = 0.615), heart rate (P = 0.505), ratings of perceived exertion (P = 0.181), and perceived thermal stress (P = 0.416) were not influenced by the nature of the intervention. Blood glucose concentrations were similar during the CHO and PLA trials (P = 0.117). In contrast to the findings of several studies undertaken in temperate conditions, the present investigation failed to support role of oral sensing of CHO in influencing performance during prolonged exercise in warm conditions. Key words: sports drink, central nervous system, fatigue, dopamine, thermoregulation. Résumé : Dans cette étude, on sollicite dix hommes entraînés a` l’endurance et on analyse le rôle possible des récepteurs gustatifs qui perçoivent la saveur sucrée (« CHO ») sur la performance a` l’effort dans la chaleur. Les volontaires participent a` un test d’effort progressif jusqu’a` épuisement afin de déterminer la consommation d’oxygène de pointe, a` un essai de familiarisation, puis a` deux essais expérimentaux. Les essais consistent en des épreuves contre-la-montre de 60 minutes réalisées dans une chambre climatique maintenue a` 30 °C, 60% humidité relative. Immédiatement avant et a` intervalles réguliers au cours de l’effort, les sujets consomment un bolus d’eau, puis se rincent la bouche durant 10 s au moyen d’une solution contenant un placebo (« PLA ») ou 6,4% de CHO puis la rejettent. On n’observe pas de différence de quantité totale de travail accompli entre les deux essais (PLA : 758,8 ± 149,0 kJ comparativement a` CHO : 762,6 ± 141,1 kJ; P = 0,951). La cadence est semblable d’un groupe a` l’autre : on n’observe pas de différence apparente de la puissance produite au cours des essais expérimentaux (P = 0,546). La nature de l’intervention n’a pas d’effet sur la température centrale (P = 0,615), le rythme cardiaque (P = 0,505), la perception de l’intensité de l’effort (P = 0,181) et du stress thermique (P = 0,416). La concentration de glucose est similaire dans les deux conditions, PLA et CHO (P = 0,117). Contrairement aux résultats de plusieurs études réalisées dans des milieux tempérés, la présente étude ne confirme pas le rôle de la détection gustative de CHO dans la performance au cours d’un effort prolongé dans la chaleur. [Traduit par la Rédaction] Mots-clés : boisson pour sportif, système nerveux central, fatigue, dopamine, thermorégulation.
Introduction The capacity to perform prolonged exercise is significantly reduced when exercise is performed in a warm environment (Galloway and Maughan 1997; Parkin et al. 1999). Additionally, distance covered during a 30-min cycle time trial was also reduced when ambient temperature was increased from 23 to 32 °C (Tatterson et al. 2000). Several explanations for the progressive deterioration in performance during exercise in the heat have been proposed, including a reduction in maximal oxygen uptake and an increased physiological burden to support the skin blood flow required for heat dissipation (Sawka et al. 2012). Any reduction in the rate of heat loss will result in a more rapid rise in core temperature at a given exercise intensity. Clearly some degree of core temperature elevation during exercise is normal, with the
increase proportional to the absolute power output (Nielsen 1938), but the narrowing of the skin to ambient temperature gradient will increase the rate of heat gain at a given power output (Galloway and Maughan 1997). Studies have provided evidence that hyperthermia profoundly influences brain function during exercise, resulting in altered brain activity (Nielsen et al. 2001), reduced voluntary activation of muscle during sustained contractions (Nybo and Nielsen 2001a), and an increased perception of effort (Nybo and Nielsen 2001b). Although the exact balance between these factors remains unclear, it is clear that fatigue fundamentally occurs because of heatrelated mechanisms, rather than any pressure on substrate availability (Parkin et al. 1999), or the metabolic limitations that closely describe fatigue occurring during prolonged exercise in temperate conditions (Maughan et al. 2007). However, the rate of
Received 7 September 2013. Accepted 5 December 2013. P. Watson. School of Sport, Exercise and Health Sciences, Loughborough University, Leicestershire, LE11 3TU, UK; Department of Human Physiology and Sports Medicine, Vrije Universiteit Brussel, Brussels B-1050, Belgium. D. Nichols and P. Cordery. School of Sport, Exercise and Health Sciences, Loughborough University, Leicestershire, LE11 3TU, UK. Corresponding author: Phillip Watson (e-mail: [email protected]). 1This paper is a part of a Special Issue entitled Nutritional Triggers to Adaptation and Performance. Appl. Physiol. Nutr. Metab. 39: 1064–1069 (2014) dx.doi.org/10.1139/apnm-2013-0413
Published at www.nrcresearchpress.com/apnm on 11 December 2013.
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Watson et al.
carbohydrate (CHO) oxidation is increased when exercise is performed in warm conditions (Febbraio et al. 1994, 1996). This response appears to be caused by increased rates of muscle glycogen oxidation (+25%), and is accompanied by a reduction in exogenous CHO usage (Jentjens et al. 2002). While the rate of muscle glycogen use is increased during exercise undertaken in warm conditions, relatively high muscle glycogen concentrations have been reported at the point of fatigue (Parkin et al. 1999), suggesting that substrate availability is not limiting when exercise is undertaken in the heat (Maughan et al. 2007). Despite these observations, several studies have reported improvements in performance following the ingestion of high-CHO diets (Pitsiladis and Maughan 1999) and the use of CHO beverages before and during exercise in warm conditions (Below et al. 1995; Carter et al. 2003; Millard-Stafford et al. 2005; Watson et al. 2012). In the absence of a definitive metabolic rationale for these improvements, it is possible that these effects of CHO may reflect a central effect of CHO ingestion, mediated through CHO-sensing receptors found in the mouth or elsewhere. A link between CHO ingestion and the central nervous system (CNS) has been proposed, with the presence of glucose in the mouth found to stimulate brain activity in the hypothalamus (Liu et al. 2000). In addition, evidence from functional magnetic resonance imaging (fMRI) studies suggest that while CHO-containing and artificially sweetened beverages activate similar taste pathways within the brain, particularly regions within the frontal operculum/anterior insula (FO/AI), CHO elicits a greater response, as well as engaging areas of the brain densely populated with dopaminergic neurons (e.g., striatum, ventral tegmental area, nucleus accumbens; Frank et al. 2008). These observations may go some way to explain reports demonstrating that simply rinsing with CHO in the mouth can produce a positive effect on cycle (Beelen et al. 2009; Carter et al. 2004; Lane et al. 2013) and running (Rollo et al. 2011) time-trial performance. There is sound logic behind this response, with CHO being sensed in the mouth as feed-forward signal to the brain to prime the body for the appearance of substrate (Liu et al. 2000). This response appears to be greater following a period of fasting (Beelen et al. 2009; Lane et al. 2013), perhaps because of an enhanced signalling response when undertaken with background feelings of hunger (Haase et al. 2009). It is worth noting, however, that the magnitude of benefit gained from mouth rinsing, followed by expectorating the solution, compared with the actual ingestion of CHO is not clear; studies report improved performance following ingestion (Rollo et al. 2011), while others have found no difference between these conditions (Pottier et al. 2010). While these findings suggest that CHO availability is typically not limiting during exercise in the heat, ingestion of CHOcontaining beverages before and during exercise appears to consistently produce improvements in performance. With this in mind, it seems possible that at least some of the benefits associated with CHO ingestion during exercise in the heat may be due to the feed-forward mechanisms originating from the mouth, potentially priming the body for the forthcoming delivery of substrate and attenuating decrements in central drive that have been reported. With this in mind, the aim of the present study was to examine the effect of mouth rinsing either a placebo or CHO solution on 1-h cycle time-trial performance in the heat.
Materials and methods Subjects Ten healthy males (age, 21 ± 2 years; height, 1.79 ± 0.09 m; body mass, 74.2 ± 5.3 kg; maximal oxygen uptake, 65.1 ± 5.3 mL/(kg·min); maximal workload (Wmax), 376 ± 32 W) volunteered to participate in this study. All volunteers were experienced road cyclists who regularly took part in cycle training and competitive races, but were not familiar with exercise in warm environments at the time of the study. Volunteers were asked
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to visit the laboratory on 4 separate occasions, each separated by at least 7 days. Prior to volunteering, all participants received written information regarding the nature and purpose of the study. Following an opportunity to ask any questions, a written statement of consent was signed. The experimental protocol was approved by the Loughborough University ethical advisory committee (Ref. R12-P114). Experimental protocol All subjects completed a preliminary test, a familiarisation trial, and 2 experimental trials (placebo or CHO). Experimental trials were randomised and undertaken in a double-blind, counterbalanced, crossover manner. The preliminary trial consisted of incremental cycle exercise to volitional exhaustion on an electrically braked cycle ergometer (Lode Corival, Groningen, Holland). Starting at a workload of 95 W, the workload increased by 35 W every 3 min, with expired gas collected at the end of each stage using the Douglas bag method. Wmax was calculated from the last completed workload, plus the fraction of time spent in the final noncompleted stage multiplied by the work rate increment (Jeukendrup et al. 1996). An abbreviated time trial lasting 15 min was completed after a short recovery to allow volunteers an initial opportunity to practice pacing and control of the ergometer. The familiarisation trial followed the same format as the experimental trials; this was undertaken to allow volunteers to gain additional experience of pacing the performance test, to minimise any potential learning effect, and to ensure they were accustomed to the procedures employed during the investigation. During the familiarisation trial, the placebo beverage was provided in the same manner as the experimental trials. To help ensure that metabolic conditions were similar before each experimental trial, subjects were instructed to record dietary intake and physical activity during the day before the familiarization trial and to replicate this in the day prior to the subsequent experimental trials. No strenuous exercise or alcohol consumption was permitted in the 24 h before each trial. The evening before each experimental trial, a radio-telemetry pill (HQ Inc., Palmetto, Fla., USA) was ingested to enable to measurement of intestinal temperature; this was used as an index of core body temperature. Trials took place in the morning, following an overnight fast. Subjects were instructed to ingest 500 mL of plain water at 90 min before the scheduled start of the trial. On arrival at the laboratory, subjects first emptied their bladders and postvoid nude body mass was measured to the nearest 10 g (Adam AFW-120K, Milton Keynes, UK). A telemetry band (Polar, Kempele, Finland) was positioned to allow heart rate (HR) to be measured. Participants then rested in a seated position for 15 min in a comfortable environment (20–22 °C), before entering a climatic chamber maintained at 30.1 ± 0.2 °C, a relative humidity of 60% ± 1% and an air velocity of between 1–1.5 m/s. The subjects were seated on the cycle ergometer and performed a 5-min warm-up at 50% Wmax, followed by an opportunity to stretch. Subjects then started the time trial, where they were instructed to complete as much work as possible in a 1-h period. The initial work load was set at 75% Wmax, but volunteers were free to self-select power output via the control unit on the ergometer from the outset. Prior to each trial, volunteers were encouraged to produce a maximal effort. Contact between the researchers and the subject was limited to the mouth rinse administration, recording of perceptual measures, and collection of blood samples; no verbal encouragement was provided. Feedback during the time trial was limited to the time lapsed; power output, cadence, HR, and core temperature were all hidden from the participant. After completion of the time trial, volunteers towelled dry and nude body mass was recorded. The change in body mass, corrected for the volume of ingested fluid, was used to determine sweat losses. Published by NRC Research Press
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Beverages At the start, and after every 10 min of the time trial, subjects ingested 100 mL of plain water. Subjects were then provided with a 25-mL bolus of either a placebo (PLA; sugar-free fruit drink; Tesco Ltd, Cheshunt, UK) or a 6.4% CHO (sugar-free fruit drink with 6.4 g/L of glucose) solution. Solutions were taste-matched through the addition of a small quantity of aspartimine sweetener to the placebo beverage. The subjects were instructed to rinse the fluids around their mouths for 10 s before expectorating it into a separate container held by an investigator. Total expectorate volume was determined following each trial to confirm that no fluid had been consumed. Measures Current power output, cadence, and total work done were recorded at 10-min intervals during the time trial. Core temperature and HR were recorded at 5-min intervals while at rest and during exercise. Ratings of perceived exertion (RPE; Borg 1982) and ratings of thermal stress (using a 21-point scale ranging from unbearable cold (–10) to unbearable heat (+10)) were assessed at 15-min intervals. Capillary blood samples were drawn at end of the rest period and at 15-min intervals throughout exercise from a fingertip into duplicate heparinised capillary tubes. Blood glucose concentrations were determined using a handheld blood analysis system (EC4 +, i-Stat, Abbott Laboratories, Abbott Park, Ill., USA).
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
Fig. 1. Mean (bars) and individual (lines) total work done during the placebo (PLA) and carbohydrate (CHO) trials.
Fig. 2. Power output during the 1-h time trial during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD). Data represent the current value at each time point, rather than a mean for the preceding 10-min period.
Statistical analysis Data are presented as means ± SD unless otherwise stated. Differences in time trial performance were examined using a paired t test. Cohen’s d effect sizes (ES) for the differences in total work done were also determined. To identify differences in data collected throughout each trial, 2-way (time-by-trial) ANOVA were employed. Where a significant interaction was apparent, pairwise differences were evaluated using the Bonferroni post hoc procedure to maintain the family-wise error rate when examining differences between individual time points. Significance was accepted at P < 0.05.
Results No difference in time trial performance was apparent between treatments, with total work done of 758.8 ± 149.0 kJ and 762.6 ± 141.1 kJ recorded in the PLA and CHO trials, respectively (P = 0.820; ES = 0.03; Fig. 1). No trial order effect was apparent (P = 0.593) and none of the participant’s performance was vastly different in one trial compared with the other (Fig. 1). As the time trial required the subjects to complete as much work as possible in a 1-h period, the total work done was directly related to the power output maintained throughout this period. Mean power output in was 231 ± 41 W and 232 ± 42 W in the PLA and CHO trials, respectively (P = 0.531). Pacing during the trials was also similar, with no difference in power output (Fig. 2, P = 0.546) or pedal cadence at any time point. Exercise produced a progressive increase in core temperature during both trials (P < 0.001), with no difference apparent between the 2 conditions (P = 0.615; Fig. 3). At the end of the time trial, core temperature was 38.9 °C ± 0.5 °C in the PLA trial and 38.9 °C ± 0.4 °C in the CHO trial. HR progressively increased throughout the time trial, peaking at 181 ± 13 beats/min and 184 ± 13 beats/min at the end of the PLA and CHO trials, respectively (P = 0.505). There was no difference in total sweat loss (P = 0.322) or calculated sweat rates between the 2 trials (P = 0.280), with a mean sweat rate of 28 ± 7 mL/min in the PLA trial and 27 ± 5 mL/min during the CHO condition. The rinse solution had no effect on perceived exertion during exercise (P = 0.181; Fig. 4A). RPE was 19 ± 1 and 19 ± 1 at the end of exercise in the PLA and CHO trials, respectively, suggesting a consistent and near-maximal effort during both experimental trials. The subjects’ rating of perceived thermal stress is presented in
Fig. 3. Core temperature at rest and during exercise during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
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Fig. 4. Rating of perceived exertion (A) and thermal stress (B) during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
Fig. 5. Blood glucose concentrations at rest and during exercise during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
Fig. 4B. No difference in the subjects’ thermal stress was apparent between trials (P = 0.416). CHO mouth rinse did not significantly influence blood glucose concentrations, although there was a tendency for higher values during the CHO trial compared with the PLA trial (P = 0.117). At the end of the performance, blood glucose concentrations were 5.4 ± 0.4 mmol/L and 5.6 ± 0.3 mmol/L during the PLA and CHO trials, repectively (Fig. 5). The volume of expectorate was determined at the end of each trial, confirming that the subjects had ingested only negligible quantities of the solutions (PLA, 2 ± 2 mL; CHO, 1 ± 5 mL; P = 0.294).
strate and attenuating decrements in central drive that occurs during exercise in the heat. With this in mind, the aim of the present study was to examine the effect of mouth rinsing with either a placebo or CHO solution on 1-h cycle time trial performance in the heat. Several published studies have demonstrated improvements in cycle time trial performance in temperate conditions when a CHO-containing solution is rinsed in the mouth (Beelen et al. 2009; Carter et al. 2004; Lane et al. 2013). Magnitude of response appears to be something in the order of 1%–3% when this approach is employed following an overnight fast (Carter et al. 2004; Lane et al. 2013), but this effect appears to be reduced (Lane et al. 2013) or disappears completely (Beelen et al. 2009) when exercise is undertaken shortly after a meal. This positive response was not apparent in the present study, with no difference in total work completed between the PLA and CHO trials (P = 0.820; ES = 0.03). There was no clear pattern in the response to the rinse solution, with 3 volunteers performing better with CHO, 4 demonstrating no response (≤1% difference between trials), and 3 participants completing less work with CHO (Fig. 1). While ingestion of CHO does tend to result in greater performance gains (2%–6%) when compared with mouth rinsing and expectorating the solution (Below et al. 1995; Jeukendrup et al. 1997; Rollo et al. 2011), it has been suggested that this strategy may have some application in athletes who are prone to gastrointestinal problems as a result of pre- or during-event feeding during training and competition (Lane et al. 2013). While several studies have investigated this phenomenon, a clearly defined and plausible physiological mechanism is yet to be proposed. Sweet taste perception is mediated through activation of T1R3 and T1R2 receptors found on the tongue (Chandrashekar et al. 2006). Cranial nerves transmit sensory information from these receptors to the brain, finally reaching the primary gustatory cortex (FO/AI), a brain region responsible for the perception of taste (Ogawa 1994). Evidence from fMRI studies suggests that while CHO-containing and artificially sweetened beverages activate similar taste pathways within the brain, particularly regions within the FO/AI, CHO elicits a greater response, as well as engaging areas of the brain densely populated with dopaminergic neurons (e.g., striatum, ventral tegmental area, nucleus accumbens; Frank et al. 2008; Liu et al. 2000). Several rodent studies have reported dopamine release in the nucleus accumbens in following feeding with sucrose (Smith 2004). This response remains, even when these animals are fitted with a chronic gastric fistula, meaning that none of the ingested fluid passes on to the intestine and into the circulation (Schneider 1989). While it is important to
Discussion During exercise in temperate conditions, endurance performance largely appears to be limited by CHO availability. While there is an increased reliance on CHO as a fuel during exercise undertaken in the heat, muscle glycogen stores are not significantly depleted by exhaustive exercise. Despite this observation, several studies have reported improvements in performance after the ingestion of high-CHO diets in the days preceding an exercise bout (Pitsiladis and Maughan 1999), as well as the use of CHO supplements before and during prolonged exercise in warm conditions (Below et al. 1995; Carter et al. 2003; Millard-Stafford et al. 2005; Watson et al. 2012). In the absence of a definitive metabolic rationale for these improvements, it was hypothesised that these effects of CHO may reflect a central effect of CHO ingestion, mediated through CHO-sensing receptors found in the mouth that potentially prime the body for the forthcoming delivery of sub-
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recognise species differences in food/nutrient-seeking behaviour, these findings do highlight a clear central response to the presence of CHO within the oral cavity. Since increases in central dopaminergic activity are intrinsically linked to feelings of drive, motivation, arousal, and reward (Flagel et al. 2011; Maughan et al. 2007), and pharmacological interventions acting on this neurotransmitter system consistently increase exercise performance in warm environments (Roelands et al. 2012), perhaps this provides some plausible rationale for the benefits of mouth rinsing CHO reported by some studies. The reason for the diminished effectiveness of a CHO mouth rinse on performance in the heat remains unclear. While there is an increase in total CHO oxidation when exercise is performed in warm conditions (Febbraio et al. 1994; 1996), this response seems to be caused by an increased rate of muscle glycogen oxidation, rather than a change in exogenous CHO utilisation (Jentjens et al. 2002). In fact, Jentjens and colleagues (2002) reported lower exogenous CHO use, perhaps because of a reduction in muscle glucose uptake or decreased rates of gastric emptying and (or) intestinal absorption. Despite these observations, CHO feeding during exercise in the heat appears to increase performance by a similar magnitude to that seen when exercise of a similar intensity is undertaken in temperate environments (Below et al. 1995; Carter et al. 2003; Watson et al. 2012). Given these observations, we originally speculated that activation of CHO receptors in the mouth facilitating a central response to CHO ingestion would go some way to explaining the performance benefits observed in the heat. However, the present data suggest that the presence of heat stress may mask or override signals from CHO receptors in the mouth, thereby blunting any potential beneficial performance effect. Since volunteers were provided with water during each trial, it is possible that this practice may have limited the effectiveness of the mouth rinse intervention. Plain water was ingested at 10-min intervals immediately prior to each mouth rinse exposure. Consequently there should have been sufficient time between each water bolus to prolong the possible activation of oral receptors that result from any residual CHO remaining in the mouth. In addition, a similar fluid ingestion regimen was employed in a recent study by Lane and colleagues, and this did not appear to limit the benefits observed (Lane et al. 2013). In addition to the points discussed above, it is also possible that the protocol employed for the time trial may have masked subtle differences between trials. The setup of the trial was such that a change in intensity was only achievable through manual adjustment of the ergometer workload. Ourselves and others have employed this approach in a number of studies (Rollo et al. 2011; Roelands et al. 2012), but it should be acknowledged that this protocol may limit the chance for small subconscious fluctuations in pace to influence the outcome. To minimise this possibility, the volunteers had 2 occasions (abbreviated time trial and familiarisation trial) to practice the control of the power output. In addition, prior to all trials volunteers were encouraged to produce a maximal effort. Despite there being no significant difference in blood glucose concentration between the trials, there was a trend towards higher blood glucose concentrations in the CHO trial compared with the PLA trial (Fig. 4). Several other studies employing CHO mouth rinse interventions do not report differences in blood glucose concentrations during exercise, so the cause of this response is unclear. Given that very little CHO was ingested (
ARTICLE Mouth rinsing with a carbohydrate solution does not influence cycle time trial performance in the heat1 Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by Fudan University on 05/10/15 For personal use only.
Phillip Watson, David Nichols, and Philip Cordery
Abstract: Ten endurance-trained males were recruited to examine the possible role of carbohydrate (CHO) receptors in the mouth influencing exercise performance in the heat. Volunteers completed an incremental test to exhaustion to determine peak oxygen uptake, a familiarisation trial, followed by 2 experimental trials. Trials consisted of a 1-h time trial undertaken in a climatic chamber maintained at 30 °C, 60% relative humidity. Immediately before, and at regular intervals throughout exercise, subjects ingested a bolus of water and then were provided with either a placebo (PLA) or a 6.4% glucose (CHO) solution to rinse in the mouth for 10 s before being expectorated. There was no difference in total work done between the PLA and CHO trials (758.8 ± 149.0 kJ; 762.6 ± 141.1 kJ; P = 0.951). Pacing was also similar, with no differences in power output apparent during the experimental trials (P = 0.546). Core temperature (P = 0.615), heart rate (P = 0.505), ratings of perceived exertion (P = 0.181), and perceived thermal stress (P = 0.416) were not influenced by the nature of the intervention. Blood glucose concentrations were similar during the CHO and PLA trials (P = 0.117). In contrast to the findings of several studies undertaken in temperate conditions, the present investigation failed to support role of oral sensing of CHO in influencing performance during prolonged exercise in warm conditions. Key words: sports drink, central nervous system, fatigue, dopamine, thermoregulation. Résumé : Dans cette étude, on sollicite dix hommes entraînés a` l’endurance et on analyse le rôle possible des récepteurs gustatifs qui perçoivent la saveur sucrée (« CHO ») sur la performance a` l’effort dans la chaleur. Les volontaires participent a` un test d’effort progressif jusqu’a` épuisement afin de déterminer la consommation d’oxygène de pointe, a` un essai de familiarisation, puis a` deux essais expérimentaux. Les essais consistent en des épreuves contre-la-montre de 60 minutes réalisées dans une chambre climatique maintenue a` 30 °C, 60% humidité relative. Immédiatement avant et a` intervalles réguliers au cours de l’effort, les sujets consomment un bolus d’eau, puis se rincent la bouche durant 10 s au moyen d’une solution contenant un placebo (« PLA ») ou 6,4% de CHO puis la rejettent. On n’observe pas de différence de quantité totale de travail accompli entre les deux essais (PLA : 758,8 ± 149,0 kJ comparativement a` CHO : 762,6 ± 141,1 kJ; P = 0,951). La cadence est semblable d’un groupe a` l’autre : on n’observe pas de différence apparente de la puissance produite au cours des essais expérimentaux (P = 0,546). La nature de l’intervention n’a pas d’effet sur la température centrale (P = 0,615), le rythme cardiaque (P = 0,505), la perception de l’intensité de l’effort (P = 0,181) et du stress thermique (P = 0,416). La concentration de glucose est similaire dans les deux conditions, PLA et CHO (P = 0,117). Contrairement aux résultats de plusieurs études réalisées dans des milieux tempérés, la présente étude ne confirme pas le rôle de la détection gustative de CHO dans la performance au cours d’un effort prolongé dans la chaleur. [Traduit par la Rédaction] Mots-clés : boisson pour sportif, système nerveux central, fatigue, dopamine, thermorégulation.
Introduction The capacity to perform prolonged exercise is significantly reduced when exercise is performed in a warm environment (Galloway and Maughan 1997; Parkin et al. 1999). Additionally, distance covered during a 30-min cycle time trial was also reduced when ambient temperature was increased from 23 to 32 °C (Tatterson et al. 2000). Several explanations for the progressive deterioration in performance during exercise in the heat have been proposed, including a reduction in maximal oxygen uptake and an increased physiological burden to support the skin blood flow required for heat dissipation (Sawka et al. 2012). Any reduction in the rate of heat loss will result in a more rapid rise in core temperature at a given exercise intensity. Clearly some degree of core temperature elevation during exercise is normal, with the
increase proportional to the absolute power output (Nielsen 1938), but the narrowing of the skin to ambient temperature gradient will increase the rate of heat gain at a given power output (Galloway and Maughan 1997). Studies have provided evidence that hyperthermia profoundly influences brain function during exercise, resulting in altered brain activity (Nielsen et al. 2001), reduced voluntary activation of muscle during sustained contractions (Nybo and Nielsen 2001a), and an increased perception of effort (Nybo and Nielsen 2001b). Although the exact balance between these factors remains unclear, it is clear that fatigue fundamentally occurs because of heatrelated mechanisms, rather than any pressure on substrate availability (Parkin et al. 1999), or the metabolic limitations that closely describe fatigue occurring during prolonged exercise in temperate conditions (Maughan et al. 2007). However, the rate of
Received 7 September 2013. Accepted 5 December 2013. P. Watson. School of Sport, Exercise and Health Sciences, Loughborough University, Leicestershire, LE11 3TU, UK; Department of Human Physiology and Sports Medicine, Vrije Universiteit Brussel, Brussels B-1050, Belgium. D. Nichols and P. Cordery. School of Sport, Exercise and Health Sciences, Loughborough University, Leicestershire, LE11 3TU, UK. Corresponding author: Phillip Watson (e-mail: [email protected]). 1This paper is a part of a Special Issue entitled Nutritional Triggers to Adaptation and Performance. Appl. Physiol. Nutr. Metab. 39: 1064–1069 (2014) dx.doi.org/10.1139/apnm-2013-0413
Published at www.nrcresearchpress.com/apnm on 11 December 2013.
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Watson et al.
carbohydrate (CHO) oxidation is increased when exercise is performed in warm conditions (Febbraio et al. 1994, 1996). This response appears to be caused by increased rates of muscle glycogen oxidation (+25%), and is accompanied by a reduction in exogenous CHO usage (Jentjens et al. 2002). While the rate of muscle glycogen use is increased during exercise undertaken in warm conditions, relatively high muscle glycogen concentrations have been reported at the point of fatigue (Parkin et al. 1999), suggesting that substrate availability is not limiting when exercise is undertaken in the heat (Maughan et al. 2007). Despite these observations, several studies have reported improvements in performance following the ingestion of high-CHO diets (Pitsiladis and Maughan 1999) and the use of CHO beverages before and during exercise in warm conditions (Below et al. 1995; Carter et al. 2003; Millard-Stafford et al. 2005; Watson et al. 2012). In the absence of a definitive metabolic rationale for these improvements, it is possible that these effects of CHO may reflect a central effect of CHO ingestion, mediated through CHO-sensing receptors found in the mouth or elsewhere. A link between CHO ingestion and the central nervous system (CNS) has been proposed, with the presence of glucose in the mouth found to stimulate brain activity in the hypothalamus (Liu et al. 2000). In addition, evidence from functional magnetic resonance imaging (fMRI) studies suggest that while CHO-containing and artificially sweetened beverages activate similar taste pathways within the brain, particularly regions within the frontal operculum/anterior insula (FO/AI), CHO elicits a greater response, as well as engaging areas of the brain densely populated with dopaminergic neurons (e.g., striatum, ventral tegmental area, nucleus accumbens; Frank et al. 2008). These observations may go some way to explain reports demonstrating that simply rinsing with CHO in the mouth can produce a positive effect on cycle (Beelen et al. 2009; Carter et al. 2004; Lane et al. 2013) and running (Rollo et al. 2011) time-trial performance. There is sound logic behind this response, with CHO being sensed in the mouth as feed-forward signal to the brain to prime the body for the appearance of substrate (Liu et al. 2000). This response appears to be greater following a period of fasting (Beelen et al. 2009; Lane et al. 2013), perhaps because of an enhanced signalling response when undertaken with background feelings of hunger (Haase et al. 2009). It is worth noting, however, that the magnitude of benefit gained from mouth rinsing, followed by expectorating the solution, compared with the actual ingestion of CHO is not clear; studies report improved performance following ingestion (Rollo et al. 2011), while others have found no difference between these conditions (Pottier et al. 2010). While these findings suggest that CHO availability is typically not limiting during exercise in the heat, ingestion of CHOcontaining beverages before and during exercise appears to consistently produce improvements in performance. With this in mind, it seems possible that at least some of the benefits associated with CHO ingestion during exercise in the heat may be due to the feed-forward mechanisms originating from the mouth, potentially priming the body for the forthcoming delivery of substrate and attenuating decrements in central drive that have been reported. With this in mind, the aim of the present study was to examine the effect of mouth rinsing either a placebo or CHO solution on 1-h cycle time-trial performance in the heat.
Materials and methods Subjects Ten healthy males (age, 21 ± 2 years; height, 1.79 ± 0.09 m; body mass, 74.2 ± 5.3 kg; maximal oxygen uptake, 65.1 ± 5.3 mL/(kg·min); maximal workload (Wmax), 376 ± 32 W) volunteered to participate in this study. All volunteers were experienced road cyclists who regularly took part in cycle training and competitive races, but were not familiar with exercise in warm environments at the time of the study. Volunteers were asked
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to visit the laboratory on 4 separate occasions, each separated by at least 7 days. Prior to volunteering, all participants received written information regarding the nature and purpose of the study. Following an opportunity to ask any questions, a written statement of consent was signed. The experimental protocol was approved by the Loughborough University ethical advisory committee (Ref. R12-P114). Experimental protocol All subjects completed a preliminary test, a familiarisation trial, and 2 experimental trials (placebo or CHO). Experimental trials were randomised and undertaken in a double-blind, counterbalanced, crossover manner. The preliminary trial consisted of incremental cycle exercise to volitional exhaustion on an electrically braked cycle ergometer (Lode Corival, Groningen, Holland). Starting at a workload of 95 W, the workload increased by 35 W every 3 min, with expired gas collected at the end of each stage using the Douglas bag method. Wmax was calculated from the last completed workload, plus the fraction of time spent in the final noncompleted stage multiplied by the work rate increment (Jeukendrup et al. 1996). An abbreviated time trial lasting 15 min was completed after a short recovery to allow volunteers an initial opportunity to practice pacing and control of the ergometer. The familiarisation trial followed the same format as the experimental trials; this was undertaken to allow volunteers to gain additional experience of pacing the performance test, to minimise any potential learning effect, and to ensure they were accustomed to the procedures employed during the investigation. During the familiarisation trial, the placebo beverage was provided in the same manner as the experimental trials. To help ensure that metabolic conditions were similar before each experimental trial, subjects were instructed to record dietary intake and physical activity during the day before the familiarization trial and to replicate this in the day prior to the subsequent experimental trials. No strenuous exercise or alcohol consumption was permitted in the 24 h before each trial. The evening before each experimental trial, a radio-telemetry pill (HQ Inc., Palmetto, Fla., USA) was ingested to enable to measurement of intestinal temperature; this was used as an index of core body temperature. Trials took place in the morning, following an overnight fast. Subjects were instructed to ingest 500 mL of plain water at 90 min before the scheduled start of the trial. On arrival at the laboratory, subjects first emptied their bladders and postvoid nude body mass was measured to the nearest 10 g (Adam AFW-120K, Milton Keynes, UK). A telemetry band (Polar, Kempele, Finland) was positioned to allow heart rate (HR) to be measured. Participants then rested in a seated position for 15 min in a comfortable environment (20–22 °C), before entering a climatic chamber maintained at 30.1 ± 0.2 °C, a relative humidity of 60% ± 1% and an air velocity of between 1–1.5 m/s. The subjects were seated on the cycle ergometer and performed a 5-min warm-up at 50% Wmax, followed by an opportunity to stretch. Subjects then started the time trial, where they were instructed to complete as much work as possible in a 1-h period. The initial work load was set at 75% Wmax, but volunteers were free to self-select power output via the control unit on the ergometer from the outset. Prior to each trial, volunteers were encouraged to produce a maximal effort. Contact between the researchers and the subject was limited to the mouth rinse administration, recording of perceptual measures, and collection of blood samples; no verbal encouragement was provided. Feedback during the time trial was limited to the time lapsed; power output, cadence, HR, and core temperature were all hidden from the participant. After completion of the time trial, volunteers towelled dry and nude body mass was recorded. The change in body mass, corrected for the volume of ingested fluid, was used to determine sweat losses. Published by NRC Research Press
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Beverages At the start, and after every 10 min of the time trial, subjects ingested 100 mL of plain water. Subjects were then provided with a 25-mL bolus of either a placebo (PLA; sugar-free fruit drink; Tesco Ltd, Cheshunt, UK) or a 6.4% CHO (sugar-free fruit drink with 6.4 g/L of glucose) solution. Solutions were taste-matched through the addition of a small quantity of aspartimine sweetener to the placebo beverage. The subjects were instructed to rinse the fluids around their mouths for 10 s before expectorating it into a separate container held by an investigator. Total expectorate volume was determined following each trial to confirm that no fluid had been consumed. Measures Current power output, cadence, and total work done were recorded at 10-min intervals during the time trial. Core temperature and HR were recorded at 5-min intervals while at rest and during exercise. Ratings of perceived exertion (RPE; Borg 1982) and ratings of thermal stress (using a 21-point scale ranging from unbearable cold (–10) to unbearable heat (+10)) were assessed at 15-min intervals. Capillary blood samples were drawn at end of the rest period and at 15-min intervals throughout exercise from a fingertip into duplicate heparinised capillary tubes. Blood glucose concentrations were determined using a handheld blood analysis system (EC4 +, i-Stat, Abbott Laboratories, Abbott Park, Ill., USA).
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
Fig. 1. Mean (bars) and individual (lines) total work done during the placebo (PLA) and carbohydrate (CHO) trials.
Fig. 2. Power output during the 1-h time trial during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD). Data represent the current value at each time point, rather than a mean for the preceding 10-min period.
Statistical analysis Data are presented as means ± SD unless otherwise stated. Differences in time trial performance were examined using a paired t test. Cohen’s d effect sizes (ES) for the differences in total work done were also determined. To identify differences in data collected throughout each trial, 2-way (time-by-trial) ANOVA were employed. Where a significant interaction was apparent, pairwise differences were evaluated using the Bonferroni post hoc procedure to maintain the family-wise error rate when examining differences between individual time points. Significance was accepted at P < 0.05.
Results No difference in time trial performance was apparent between treatments, with total work done of 758.8 ± 149.0 kJ and 762.6 ± 141.1 kJ recorded in the PLA and CHO trials, respectively (P = 0.820; ES = 0.03; Fig. 1). No trial order effect was apparent (P = 0.593) and none of the participant’s performance was vastly different in one trial compared with the other (Fig. 1). As the time trial required the subjects to complete as much work as possible in a 1-h period, the total work done was directly related to the power output maintained throughout this period. Mean power output in was 231 ± 41 W and 232 ± 42 W in the PLA and CHO trials, respectively (P = 0.531). Pacing during the trials was also similar, with no difference in power output (Fig. 2, P = 0.546) or pedal cadence at any time point. Exercise produced a progressive increase in core temperature during both trials (P < 0.001), with no difference apparent between the 2 conditions (P = 0.615; Fig. 3). At the end of the time trial, core temperature was 38.9 °C ± 0.5 °C in the PLA trial and 38.9 °C ± 0.4 °C in the CHO trial. HR progressively increased throughout the time trial, peaking at 181 ± 13 beats/min and 184 ± 13 beats/min at the end of the PLA and CHO trials, respectively (P = 0.505). There was no difference in total sweat loss (P = 0.322) or calculated sweat rates between the 2 trials (P = 0.280), with a mean sweat rate of 28 ± 7 mL/min in the PLA trial and 27 ± 5 mL/min during the CHO condition. The rinse solution had no effect on perceived exertion during exercise (P = 0.181; Fig. 4A). RPE was 19 ± 1 and 19 ± 1 at the end of exercise in the PLA and CHO trials, respectively, suggesting a consistent and near-maximal effort during both experimental trials. The subjects’ rating of perceived thermal stress is presented in
Fig. 3. Core temperature at rest and during exercise during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
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Fig. 4. Rating of perceived exertion (A) and thermal stress (B) during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
Fig. 5. Blood glucose concentrations at rest and during exercise during the placebo (PLA) and carbohydrate (CHO) trials (mean ± SD).
Fig. 4B. No difference in the subjects’ thermal stress was apparent between trials (P = 0.416). CHO mouth rinse did not significantly influence blood glucose concentrations, although there was a tendency for higher values during the CHO trial compared with the PLA trial (P = 0.117). At the end of the performance, blood glucose concentrations were 5.4 ± 0.4 mmol/L and 5.6 ± 0.3 mmol/L during the PLA and CHO trials, repectively (Fig. 5). The volume of expectorate was determined at the end of each trial, confirming that the subjects had ingested only negligible quantities of the solutions (PLA, 2 ± 2 mL; CHO, 1 ± 5 mL; P = 0.294).
strate and attenuating decrements in central drive that occurs during exercise in the heat. With this in mind, the aim of the present study was to examine the effect of mouth rinsing with either a placebo or CHO solution on 1-h cycle time trial performance in the heat. Several published studies have demonstrated improvements in cycle time trial performance in temperate conditions when a CHO-containing solution is rinsed in the mouth (Beelen et al. 2009; Carter et al. 2004; Lane et al. 2013). Magnitude of response appears to be something in the order of 1%–3% when this approach is employed following an overnight fast (Carter et al. 2004; Lane et al. 2013), but this effect appears to be reduced (Lane et al. 2013) or disappears completely (Beelen et al. 2009) when exercise is undertaken shortly after a meal. This positive response was not apparent in the present study, with no difference in total work completed between the PLA and CHO trials (P = 0.820; ES = 0.03). There was no clear pattern in the response to the rinse solution, with 3 volunteers performing better with CHO, 4 demonstrating no response (≤1% difference between trials), and 3 participants completing less work with CHO (Fig. 1). While ingestion of CHO does tend to result in greater performance gains (2%–6%) when compared with mouth rinsing and expectorating the solution (Below et al. 1995; Jeukendrup et al. 1997; Rollo et al. 2011), it has been suggested that this strategy may have some application in athletes who are prone to gastrointestinal problems as a result of pre- or during-event feeding during training and competition (Lane et al. 2013). While several studies have investigated this phenomenon, a clearly defined and plausible physiological mechanism is yet to be proposed. Sweet taste perception is mediated through activation of T1R3 and T1R2 receptors found on the tongue (Chandrashekar et al. 2006). Cranial nerves transmit sensory information from these receptors to the brain, finally reaching the primary gustatory cortex (FO/AI), a brain region responsible for the perception of taste (Ogawa 1994). Evidence from fMRI studies suggests that while CHO-containing and artificially sweetened beverages activate similar taste pathways within the brain, particularly regions within the FO/AI, CHO elicits a greater response, as well as engaging areas of the brain densely populated with dopaminergic neurons (e.g., striatum, ventral tegmental area, nucleus accumbens; Frank et al. 2008; Liu et al. 2000). Several rodent studies have reported dopamine release in the nucleus accumbens in following feeding with sucrose (Smith 2004). This response remains, even when these animals are fitted with a chronic gastric fistula, meaning that none of the ingested fluid passes on to the intestine and into the circulation (Schneider 1989). While it is important to
Discussion During exercise in temperate conditions, endurance performance largely appears to be limited by CHO availability. While there is an increased reliance on CHO as a fuel during exercise undertaken in the heat, muscle glycogen stores are not significantly depleted by exhaustive exercise. Despite this observation, several studies have reported improvements in performance after the ingestion of high-CHO diets in the days preceding an exercise bout (Pitsiladis and Maughan 1999), as well as the use of CHO supplements before and during prolonged exercise in warm conditions (Below et al. 1995; Carter et al. 2003; Millard-Stafford et al. 2005; Watson et al. 2012). In the absence of a definitive metabolic rationale for these improvements, it was hypothesised that these effects of CHO may reflect a central effect of CHO ingestion, mediated through CHO-sensing receptors found in the mouth that potentially prime the body for the forthcoming delivery of sub-
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recognise species differences in food/nutrient-seeking behaviour, these findings do highlight a clear central response to the presence of CHO within the oral cavity. Since increases in central dopaminergic activity are intrinsically linked to feelings of drive, motivation, arousal, and reward (Flagel et al. 2011; Maughan et al. 2007), and pharmacological interventions acting on this neurotransmitter system consistently increase exercise performance in warm environments (Roelands et al. 2012), perhaps this provides some plausible rationale for the benefits of mouth rinsing CHO reported by some studies. The reason for the diminished effectiveness of a CHO mouth rinse on performance in the heat remains unclear. While there is an increase in total CHO oxidation when exercise is performed in warm conditions (Febbraio et al. 1994; 1996), this response seems to be caused by an increased rate of muscle glycogen oxidation, rather than a change in exogenous CHO utilisation (Jentjens et al. 2002). In fact, Jentjens and colleagues (2002) reported lower exogenous CHO use, perhaps because of a reduction in muscle glucose uptake or decreased rates of gastric emptying and (or) intestinal absorption. Despite these observations, CHO feeding during exercise in the heat appears to increase performance by a similar magnitude to that seen when exercise of a similar intensity is undertaken in temperate environments (Below et al. 1995; Carter et al. 2003; Watson et al. 2012). Given these observations, we originally speculated that activation of CHO receptors in the mouth facilitating a central response to CHO ingestion would go some way to explaining the performance benefits observed in the heat. However, the present data suggest that the presence of heat stress may mask or override signals from CHO receptors in the mouth, thereby blunting any potential beneficial performance effect. Since volunteers were provided with water during each trial, it is possible that this practice may have limited the effectiveness of the mouth rinse intervention. Plain water was ingested at 10-min intervals immediately prior to each mouth rinse exposure. Consequently there should have been sufficient time between each water bolus to prolong the possible activation of oral receptors that result from any residual CHO remaining in the mouth. In addition, a similar fluid ingestion regimen was employed in a recent study by Lane and colleagues, and this did not appear to limit the benefits observed (Lane et al. 2013). In addition to the points discussed above, it is also possible that the protocol employed for the time trial may have masked subtle differences between trials. The setup of the trial was such that a change in intensity was only achievable through manual adjustment of the ergometer workload. Ourselves and others have employed this approach in a number of studies (Rollo et al. 2011; Roelands et al. 2012), but it should be acknowledged that this protocol may limit the chance for small subconscious fluctuations in pace to influence the outcome. To minimise this possibility, the volunteers had 2 occasions (abbreviated time trial and familiarisation trial) to practice the control of the power output. In addition, prior to all trials volunteers were encouraged to produce a maximal effort. Despite there being no significant difference in blood glucose concentration between the trials, there was a trend towards higher blood glucose concentrations in the CHO trial compared with the PLA trial (Fig. 4). Several other studies employing CHO mouth rinse interventions do not report differences in blood glucose concentrations during exercise, so the cause of this response is unclear. Given that very little CHO was ingested (
