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The influence of ice slushy on voluntary contraction force following exercise-induced hyperthermia Catriona A. Burdon, Christopher S. Easthope, Nathan A. Johnson, Phillip G. Chapman, and Helen O’Connor

Abstract: This study aimed to investigate the effect of exercise-induced hyperthermia on central fatigue and force decline in exercised and nonexercised muscles and whether ingestion of ice slushy (ICE) ameliorates fatigue. Eight participants (5 males, 3 females) completed 45 s maximal voluntary isometric contractions (MVIC) with elbow flexors and knee extensors at baseline and following an exercise-induced rectal temperature (Trec) of 39.3 ± 0.2 °C. Percutaneous electrical muscle stimulation was superimposed at 15, 30 and 44 s during MVICs to assess muscle activation. To increase Trec to 39.3 °C, participants cycled at 60% maximum power output for 42 ± 11 min in 40 °C and 50% relative humidity. Immediately prior to each MVIC, participants consumed 50 g of ICE (–1 °C) or thermoneutral drink (38 °C, CON) made from 7.4% carbohydrate beverage. Participants consumed water (19 °C) during exercise to prevent hypohydration. Voluntary muscle force production and activation in both muscle groups were unchanged at Trec 39.3 °C with ICE (knee extensors: 209 ± 152 N) versus CON (knee extensors: 255 ± 157 N, p = 0.19). At Trec 39.3 °C, quadriceps mean force (232 ± 151 N) decreased versus baseline (302 ± 180 N, p < 0.001) and mean voluntary activation was also decreased (by 15% ± 11%, p < 0.001). Elbow flexor mean force decreased from 179 ± 67 N to 148 ± 65 N when Trec was increased to 39.3 °C (p < 0.001) but mean voluntary activation was not reduced at 39.3 °C (5% ± 25%, p = 0.79). After exercise-induced hyperthermia, ICE had no effect on voluntary activation or force production; however, both were reduced from baseline in the exercised muscle group. Peripheral fatigue was greater than the central component and limited the ability of an intervention designed to alter central fatigue. Key words: beverage temperature, muscle activation, thermoregulation, central fatigue. Résumé : Cette étude analyse l’effet de l’hyperthermie de l’effort sur la fatigue centrale et la diminution de la force des muscles sollicités ou non par l’effort et vérifie si l’ingestion de barbotine (« ICE ») influence positivement la fatigue. Huit participants (5 hommes, 3 femmes) effectuent volontairement durant 45 s des contractions isométriques maximales (« MVIC ») des fléchisseurs des coudes et des extenseurs des genoux dans une condition de base et après l’atteinte au moyen de l’exercice physique d’une température rectale (Trec) de 39,3 ± 0,2 °C. Pour évaluer l’activation musculaire, on applique aux muscles en contraction une électromyostimulation percutanée a` la 15e, 30e et 44e seconde des MVIC. Pour atteindre une Trec de 39,3 °C, les participants pédalent durant 42 ± 11 min a` 60 % de la puissance maximale développée dans un local a` 40 °C et 50 % humidité relative. Immédiatement avant chaque MVIC, les participants consomment 50 g de ICE (–1 °C) ou une boisson thermoneutre (38 °C, « CON ») renfermant 7,4 % de sucre. Pour prévenir l’hypohydratation durant l’exercice physique, les participants boivent de l’eau (19 °C). L’activation et la production volontaires de force par les deux groupes musculaires ne varient pas a` une Trec de 39,3 °C dans la condition ICE (extenseurs du genou : 209 ± 152 N) comparativement a` CON (extenseurs du genou : 255 ± 157 N, p = 0,19). À la Trec de 39,3 °C, la force moyenne du quadriceps (232 ± 151 N) diminue par rapport aux valeurs de base (302 ± 180 N, p < 0,001); l’activation volontaire moyenne diminue aussi (de 15 ± 11 %, p < 0,001). La force moyenne des fléchisseurs du coude diminue de 179 ± 67 N a` 148 ± 65 N quand la Trec est de 39,3 °C (p < 0,001), mais l’activation volontaire moyenne n’est pas plus faible a` 39,3 °C (5 ± 25 %, p = 0,79). En condition d’hyperthermie suscitée par l’effort, l’activation et la production volontaires de la force ne sont pas modifiées par ICE, mais les valeurs de ces deux variables des muscles sollicités diminuent comparativement aux valeurs de base. La fatigue périphérique est plus grande que la fatigue centrale et nuit a` la capacité d’intervention conçue pour altérer la fatigue centrale. [Traduit par la Rédaction] Mots-clés : température de la boisson, activation musculaire, thermorégulation, fatigue centrale.

Introduction It is well established that exercise in the heat augments the rise in core body temperature and contributes to the early onset of fatigue (Maughan and Shirreffs 2004). An elevated core temperature may contribute to central fatigue or fatigue that is due to increased cardiovascular and thermal strain (Nybo 2008; Thompson 2006). Consumption of cold beverages has been dem-

onstrated to be an effective strategy to lower core body temperature and improve endurance (Mundel et al. 2006; Wimer et al. 1997). Recent evidence suggests that the benefit of cold fluid consumption may partly reflect an independent sensory-mediated effect because of increased pleasantness and stimulation of brain regions associated with pleasure (Guest et al. 2007). Cold receptor stimulants including menthol and cold beverages have been in-

Received 21 August 2013. Accepted 24 December 2013. C.A. Burdon, N.A. Johnson, and H. O’Connor. Exercise and Sport Science, University of Sydney, 75 East St., Lidcombe 2141, NSW, Australia. C.S. Easthope. Exercise and Sport Science, University of Sydney, 75 East St., Lidcombe 2141, NSW, Australia; LAMHESS, EA 6309, Université de Nice Sophia Antipolis and Université de Toulon, France. P.G. Chapman. Exercise Science, Australian Catholic University, 25 Barker Rd., Strathfield, NSW, Australia. Corresponding author: Catriona A. Burdon (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 781–786 (2014) dx.doi.org/10.1139/apnm-2013-0394

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vestigated as strategies to combat fatigue during endurance exercise in the heat (Burdon et al. 2010; Gillis et al. 2010; Mundel and Jones 2010; Siegel et al. 2011). These strategies have been shown to be effective for improving performance via their effect on altering thermal sensation and decreasing participants’ rating of perceived exertion independent of any change in core body temperature. For example, in a cycling time to exhaustion test in the heat, endurance time was improved with menthol mouthwash versus a placebo (Mundel and Jones 2010). Reduction in voluntary activation and torque has been observed during brief muscular work such as maximal voluntary isometric contractions (MVIC) when core temperature is elevated (Nybo and Nielsen 2001; Périard et al. 2011). This suggests a reduction in central drive, which has been argued to protect against further elevation in core temperature from continued heat production (Marino, 2004). Recently, it was observed that ingestion of ⬃100 g of ice slushy following an ⬃42-min run to exhaustion led to a small but statistically significant improvement in sustained MVIC (Siegel et al. 2011). Given that this result was demonstrated in a nonexercised muscle group, the findings were interpreted as a reduction in central fatigue because of sensory mechanisms from the mouth/throat region positively influencing perception of thermal state and (or) activation of reward centres in the brain. Whether this benefit translates to active muscle is yet to be determined. This is particularly relevant given the mixed findings regarding voluntary activation of nonexercised (inactive) and exercise-fatigued (active) muscles when core temperature is elevated. Some studies have observed reduced voluntary activation of both the exercised and nonexercised muscle (Nybo and Nielsen 2001; Périard et al. 2011), while others have observed this reduction in the exercise-fatigued muscles and not in nonexercised muscles (Saboisky et al. 2003; Thomas et al. 2006; Todd et al. 2005; White et al. 2002). To delineate central fatigue from peripheral factors during voluntary muscular work requires external stimulation (superimposed twitch) to recruit and fire motor units. The techniques most often used to achieve this are percutaneous muscle stimulation, transcranial magnetic stimulation and nerve stimulation. Therefore, the aim of this study was to measure the effect of a cold versus thermoneutral oral stimulus on MVIC force production at an elevated core body temperature. To determine the central and peripheral contributors to fatigue, superimposed percutaneous electrical muscle stimulation was added. In addition, to further uncouple central factors from potential confounding of cycling exercise-induced peripheral fatigue, MVIC were measured in both active (knee extensors) and inactive (elbow flexors) muscle groups. We hypothesised that a cold stimulus in the form of ice slushy (ICE) would reduce central fatigue and improve voluntary force production and activation in both exercise-fatigued and nonexercised muscle groups when compared with a thermoneutral control beverage (CON). This would suggest that input to the brain regarding thermal sensation has a significant role in the reduction in central activation when hyperthermic.

Materials and methods Eight healthy, active adults (5 males, 3 females) who regularly partook in endurance-type activities, including cycling and running, completed the study (age 25 ± 3 years, weight 65 ± 8 kg, peak oxygen consumption (V˙O2peak) 56 ± 10 mL·kg−1·min−1). On the first visit, participants completed a health screening and were excluded if they had any musculoskeletal injury or recent heat illness. The study was approved by the University of Sydney Human Research Ethics Committee and participants gave informed written consent according to Declaration of Helsinki guidelines. Before each visit to the laboratory, subjects were requested to refrain from strenuous exercise and replicate dietary intake for 24 h.

Appl. Physiol. Nutr. Metab. Vol. 39, 2014

Preliminary visit Participants presented to the laboratory and were measured for body mass (in light clothing) to 0.01 kg using an electric floor scale (Mettler ID 1, Albstadt, Germany). For measurement of force, participants lay supine on a reclined custom-built adjustable chair and to prevent erroneous movement were secured at the waist and chest with the hips and knees flexed at 90°. The ankle was strapped to a force transducer (XTran Load Cell S1W, Applied Measurement, Sydney, Australia) to determine quadriceps MVIC. For elbow flexor MVICs the upper arm was strapped to the chair and wrist attached to a force transducer at a 90° elbow angle. Equipment constraints required all leg extensor contractions to be performed with the left leg and all elbow flexor contractions with the right arm. All participants were right handed. For percutaneous electrical muscle stimulation, 2 oval carbon rubber electrodes (8 × 13 cm for quadriceps, 4 × 8 cm for biceps brachii) were placed proximally and distally over the quadriceps and biceps brachii and connected to a high-voltage stimulator (Digitimer Stimulator DS7, Welwyn Garden City, England). Electrodes were placed according to anthropological landmarks and situated over probable motor points (Allen et al. 1995; Botter et al. 2011; Place et al. 2010) to ensure maximal recruitment. Electrodes were traced with indelible marker to prevent loss of congruency over trials. To determine stimulus intensity, amperage was progressively increased until limited by participant tolerance and terminated by request, or when force elicited >75% of MVIC (Davies et al. 1982). After rest, participants were familiarised with the 45-s MVIC protocol. Prior to the experimental trials, peak aerobic capacity was measured during a continuous incremental test on a cycle ergometer (Lode Excalibur, Groningen, Netherlands). The test consisted of an incremental increase in power (30 W·min−1) until volitional fatigue. Maximal effort was defined as having a heart rate within 10% of predicted maximum (based on 220 bpm – age). Oxygen consumption (V˙O2) was measured with Douglas Bags and expired air was collected for no less than 30 s prior to fatigue. Expired air was analysed with Servomex Pm1111E and Ir1507 sensors (Servomex, Crowborough, UK) to determine percent of oxygen and carbon dioxide. Gas analysers were calibrated using a gas with known oxygen and carbon dioxide composition. Gas volume was measured with a dry gas meter (Harvard, UK) allowing V˙O2 to be calculated using indirect calorimetry equations. Power output for subsequent tests was calculated as 60% of the maximum power attained. Experimental design Participants attended 3 sessions: a preliminary (described above) and 2 experimental trials in which either ice slushy (–1 °C, ICE) was given to elicit a cold oral stimulus or a thermoneutral beverage (38 °C, CON) was given as the control oral stimulus. The experimental trials were performed in a randomised counterbalanced order. Each trial was separated by a minimum of 7 and no more than 21 days. Female participants were tested during the same phase of their monthly menstrual cycle (Janse de Jonge et al. 2001). Prior to presenting at the laboratory, participants were instructed to refrain from alcohol and caffeine intake and strenuous physical activity (no more than 30-min walk) for 24 h. Participants were additionally instructed to consume 30 mL·kg–1 of body mass in the 24 h prior to presenting at the laboratory and 2 h prior to consume a meal and an additional 300 mL of fluid. They were asked to record the meal and replicate it for both visits. Participants commenced each trial at the same time of day to reduce the effect of circadian rhythm on body temperature. Upon arrival at the laboratory, participants self-inserted a rectal probe to 10 cm and were weighed. Participants completed a sustained 45-s MVIC of the knee extensors and elbow flexors at 2 rectal temperatures (Trec): baseline (⬃37–37.5 °C) and elevated Published by NRC Research Press

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Burdon et al.

(39–39.5 °C). To elevate Trec participants cycled on an upright ergometer (Lode Excalibur, Groningen, Netherlands) at 60% of their predetermined maximal power output in a climate chamber (40 °C, 50% relative humidity (RH)). Power output was lowered throughout the trial as dictated by the change in Trec and increasing perceived exertion (Borg 1973). Knee extensors were selected as the exercise fatigued (active) muscle and elbow flexors as the nonexercised (inactive) muscle group. Participants first performed the 45-s MVIC with the exercise-fatigued knee extensors at 1 min after cycling ceased to minimise any recovery. The MVIC of the elbow flexors immediately followed. Participants were provided fluid (19 °C water) to improve comfort while exercising in the heat and reduce hypohydration measured via weight change halfway during exercise. At baseline and at the elevated Trec, body mass was measured and a 45-s MVIC was performed. Immediately (30 s) before every MVIC, participants ingested 50 g of ICE or CON as a commercially available 7.4% carbohydrate-electrolyte sports drink (Powerade Isotonic, CocaCola Amatil, Australia). This was heated to 38 °C in CON by a thermostatic water bath (E-5A, Julabo, Germany) and frozen as slushy in ICE using a commercial “slush” machine (Iceotonic, Essential Slush, Australia). Beverage temperature was checked prior to consumption using an electronic thermometer (Thermistor 400 series, Cole Parmer, Ill., USA). Power output, total fluid consumption, beverage composition and carbohydrate consumption was matched between trials. Heart rate (S410, Polar Electro, Kempele, Finland) and Trec were continuously monitored (Thermistor 400 series). Skin temperature was recorded every minute using 4 skin thermistors (DS1921H-F5 ibutton, Maxim, USA) placed on the left side (upper chest, midhumerus, mid-calf and mid-thigh) and were combined to give a ˉ sk): T ˉ sk = 0.3 Tchest + 0.3 Tarm + 0.2 Tthigh + mean skin temperature (T 0.2 Tleg (Ramanathan 1964). The 45-s MVIC was performed on the custom-built chair and participants were secured at the waist and chest to prevent extraneous movement. The chair was reclined to enhance ventricular filling pressure and reduce the effects of transient hypotension following exercise-induced hyperthermia during all MVICs. To maximise voluntary activation and enhance motivation, standardised verbal encouragement and a visual display of force production on a computer monitor were provided as feedback during all contractions (Gandevia 2001). The protocol involved a superimposed 100-ms tetanus at 100 Hz using 2 electrodes placed proximally and distally over the muscle as previously described. Data was prerecorded for 10 s before contraction-onset (0 s) to collect stable baseline force output because of limb mass. Superimposed tetanii were given during the contraction at 15, 30 and 44 s and 5 s after contraction end. This method of stimulation has been demonstrated to activate a substantial portion of muscle (Bigland-Ritchie et al. 1978; Davies et al. 1982) and detect a reduction in central nervous system drive during isometric knee extension (Miller et al. 1999). The strain gauge force signals were pre-amplified, sent through an A/D board and sampled at 1000 Hz by data acquisition hardware and software (Labview, National Instruments, Austin, Tex., USA). Pre-analysis, a 50 Hz notch filter was applied to eliminate mains noise. All data was subsequently filtered using a 5th order Butterworth filter with a cut off frequency of 7 Hz to eliminate high frequency variation but preserve trace landmarks. Peak voluntary force was determined as the highest voluntarily produced force during the contraction. Mean contraction force was calculated as the average from when participants reached an initial peak or plateau until force dropped to