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The first night with phase advance decreased total sleep time, sleep efficiency, sleep onset latency, stage 2 of nonrapid eye movement (N2), and rapid eye ...
Applied Physiology, Nutrition, and Metabolism

Volume 39

An NRC Research Press Journal

2014

Une revue de NRC Research Press

www.nrcresearchpress.com

Physiologie appliquée, nutrition et métabolisme

The Canadian Society for Exercise Physiology and the Canadian Nutrition Society have chosen Applied Physiology, Nutrition, and Metabolism as their principal medium for the publication of research papers

La Société canadienne de physiologie de l’exercice et la Société canadienne de nutrition ont choisi Physiologie appliqueé, nutrition et métabolisme comme leur principal organe de publication d’articles de recherche

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ARTICLE Impact of 5-h phase advance on sleep architecture and physical performance in athletes

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Elisabeth Petit, Fabienne Mougin, Hubert Bourdin, Grégory Tio, and Emmanuel Haffen

Abstract: Travel across time zones causes jet lag and is accompanied by deleterious effects on sleep and performance in athletes. These poor performances have been evaluated in field studies but not in laboratory conditions. The purpose of this study was to evaluate, in athletes, the impact of 5-h phase advance on the architecture of sleep and physical performances (Wingate test). In a sleep laboratory, 16 male athletes (age: 22.2 ± 1.7 years, height: 178.3 ± 5.6 cm, body mass: 73.6 ± 7.9 kg) spent 1 night in baseline condition and 2 nights, 1 week apart, in phase shift condition recorded by electroencephalography to calculate sleep architecture variables. For these last 2 nights, the clock was advanced by 5 h. Core body temperature rhythm was assessed continuously. The first night with phase advance decreased total sleep time, sleep efficiency, sleep onset latency, stage 2 of nonrapid eye movement (N2), and rapid eye movement (REM) sleep compared with baseline condition, whereas the second night decreased N2 and increased slow-wave sleep and REM, thus improving the quality of sleep. After phase advance, mean power improved, which resulted in higher lactatemia. Acrophase and bathyphase of temperature occurred earlier and amplitude decreased in phase advance but the period was not modified. These results suggest that a simulated phase shift contributed to the changes in sleep architecture, but did not significantly impair physical performances in relation with early phase adjustment of temperature to the new local time. Key words: simulated jet lag, polysomnography, rectal temperature, anaerobic test. Résumé : La traversée de fuseaux horaires crée un décalage accompagné d’effets nocifs sur le sommeil et la performance des athlètes. Ces piètres performances ont été évaluées dans des études sur le terrain, mais pas dans des conditions de laboratoire. Cette étude évalue chez des athlètes l’impact d’un décalage horaire positif de 5 h sur l’architecture du sommeil et sur la performance physique (test de Wingate). Seize athlètes masculins (22,2 ± 1,7 ans, 178,3 ± 5,6 cm, 73,6 ± 7,9 kg) passent une nuit dans des conditions de base dans un laboratoire de sommeil et deux nuits, a` une semaine d’intervalle, dans une condition de décalage horaire afin de calculer par électroencéphalographie des variables de l’architecture du sommeil. Au cours des deux dernières nuits, on avance l’horloge de 5 heures. On enregistre en continu le rythme de la température centrale. Au cours de la première nuit en condition de décalage, on observe une diminution du temps total de sommeil, de l’efficacité du sommeil, de la latence d’endormissement, de mouvement oculaire non-rapide (N2) et de mouvement oculaire rapide (MOR) comparativement a` la condition de base alors qu’au cours de la deuxième nuit, on observe une diminution de N2, du sommeil lent profond et de MOR, indices d’une meilleure qualité de sommeil. À la suite du décalage horaire positif, on observe une augmentation de la puissance moyenne, d’où une plus forte lactatémie. L’acrophase et la bathyphase de la température se présentent plus hâtivement, l’amplitude diminue lors du décalage horaire positif, mais la période n’est pas modifiée. D’après ces résultats, le décalage simulé contribue aux modifications de l’architecture du sommeil, mais ne diminue pas significativement la performance physique par rapport a` l’ajustement précoce de la phase de la température en fonction de la nouvelle heure locale. [Traduit par la Rédaction] Mots-clés : décalage horaire simulé, polysomnographie, température rectale, test anaérobie.

Introduction Although athletes and coaches believe that adequate sleep is essential for peak performance, there are many situations in which sleep is disturbed prior to an athletic event (Reilly and Edwards 2007; Reilly and Waterhouse 2009). A flight across different time zones may produce disorientation, light-headedness, lack of energy, and general discomfort (Reilly et al. 2005; Waterhouse et al. 2004). The feelings associated with

jet lag can be accompanied by fatigue, loss of appetite, and mood disorders (Leatherwood and Dragoo 2012; Williams 2010). Other symptoms can occur, such as difficulty in sleeping and disturbances of circadian rhythm during the new nighttime, because of changes in light exposure (Forbes-Robertson et al. 2012; Waterhouse et al. 2002). These deleterious effects are attributed to a temporary desynchrony between the new local time and the “body clock”. Indeed, in the syndrome of jet lag, it is difficult for

Received 14 November 2013. Accepted 7 April 2014. E. Petit. University of Franche-Comte, 1, rue Goudimel, F-25000 Besançon, France; Equipe d’Accueil 481, FED 4234, Place Leclerc, F-25000 Besançon, France; UPFR Sports, 31, chemin de l’Epitaphe, F-25030 Besançon, France. F. Mougin. University of Franche-Comte, 1, rue Goudimel, F-25000 Besançon, France; UPFR Sports, 31, chemin de l’Epitaphe, F-25030 Besançon, France; EA3920 and Exercise Performance Health Innovation Platform, Hauts de Chazal, F-25030 Besançon, France. H. Bourdin. Equipe d’Accueil 481, FED 4234, Place Leclerc, F-25000 Besançon, France; Sleep Disorder Unit, 2, Clinical HIV Research Unit (CHRU), Regional University Hospital, place St Jacques, F-25030 Besançon, France. G. Tio. CIC-IT 808 INSERM, 2, CHRU, place St Jacques, F-25000 Besançon, France; Clinical Psychiatry, CHRU, Hauts de Chazal, F-25030 Besançon, France. E. Haffen. University of Franche-Comte, 1, rue Goudimel, F-25000 Besançon, France; Equipe d’Accueil 481, FED 4234, Place Leclerc, F-25000 Besançon, France; CIC-IT 808 INSERM, 2, CHRU, place St Jacques, F-25000 Besançon, France; Clinical Psychiatry, CHRU, Hauts de Chazal, F-25030 Besançon, France. Corresponding author: Elisabeth Petit (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 1230–1236 (2014) dx.doi.org/10.1139/apnm-2013-0531

Published at www.nrcresearchpress.com/apnm on 11 June 2014.

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Petit et al.

the circadian system to adjust to new external synchronizers, thus causing sleep deprivation, the extent of which depends on the direction of flight (Forbes-Robertson et al. 2012). Jet lag results from rapid transmeridian travel where time zones are crossed, such as east-to-west or west-to-east airplane travel (Forbes-Robertson et al. 2012). The severity increases with the number of time zones crossed and the fastest rate of adaptation is approximately half a day per hour of the time difference westwards, whereas it is 1 day per hour of the time difference eastwards (Jackson 2010); it is predicated upon the fact that the average human free-running period is about 24.2 h (Czeisler et al. 1999), and that individuals will therefore find it easier to adjust to a longer day than a shorter one (Forbes-Robertson et al. 2012). Until the whole range of biological rhythms adjusts to the new local time, thereby becoming resynchronized, athletic performance may be below par. Reilly and Edwards (2007) showed that the sleep–wake cycle may be normalized prior to adjustment of body temperature where resynchronization seems to coincide with disappearance of jet-lag symptoms. Only then does the performance curve return to its normal circadian rhythm. Therefore, light stimuli have been used to shift the circadian pacemaker to be aligned with a new sleep–wake schedule, resulting in an increase in subjective alertness and objective performance at required times compared with schedules (Dean et al. 2009). Ocular light can accelerate the re-entrainment of the circadian system with the new sleep–wake schedule or maintain circadian entrainment (Dean et al. 2009). The impairments of athletic performance following transmeridian flight have been documented in field studies (Bishop 2004; Edwards et al. 2000; Lagarde et al. 2001; Lemmer et al. 2002; Winter et al. 2009; Wright et al. 1983). Studies investigating the effects of a phase shift, especially in simulated laboratory conditions, are sparse and are mainly on healthy participants (Beaumont et al. 2004; Boivin and James 2002; Monk et al. 1993, 2006; Waterhouse et al. 2005b, 2005c). Specific studies on athletes are still lacking. Consequently, no compelling evidence exists demonstrating that a rapid phase advance influences athletic performances in athletes. Furthermore, no study to date has assessed polysomnography sleep structure after a simulated phase advance in athletes. Therefore, the aim of this study was to evaluate, in highly trained young participants, the impact of a 5-h phase advance on architecture of sleep, and to examine its effects on specific indices of measures of very short-term physical exercise. We hypothesized that a 5-h simulated jet lag would induce an alteration in amounts and quality of subsequent sleep and physical performance. These reduced performances may be due to phase shifts in temperature and sleep–wake rhythms.

Materials and methods Participants Twenty trained athletes were screened, of whom 16 (age: 22.2 ± 1.7 years, height: 178.3 ± 5.6 cm, body mass: 73.6 ± 7.9 kg, fat mass: 12.6% ± 3.4%) participated in the study. Only males were voluntarily recruited, to the extent that the severity of the jet-lag symptoms may be related to menstrual cycle phase in women. Disturbances of these cycles might arise from an interaction between melatonin and estrogen secretions (Waterhouse et al. 2004). Four were excluded because of reported sleep disturbances. Enrolled participants did not report any significant previous or existing health problems, including substance abuse, and they did not have any sleep-related complaints or partial sleep restriction. The participants’ selection was based on the following criteria: •

Their circadian typology, according to the Horne and Östberg “morningness–eveningness” questionnaire (Horne and Östberg 1976). All participants had an intermediate chronotype with an

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average circadian typology score of 52.88 ± 5.45. Morning or evening types were excluded. Their sleeping diary, which was completed for 1 month before experimentation: sleeping diary averaged estimated total sleep time per night to be 491.44 ± 41.12 min, estimated sleep onset latency to be 15.75 ± 12.18 min, and sleep efficiency index (total sleep time estimated/time in bed × 100) to be 94.81% ± 3.02%. All these parameters were monitored by a sleeping diary, filled by subjects for 1 month, and analyzed by an experimented technician. Finally, to be eligible for this study, the following sleep criteria were required: an amount of at least 450 min of sleep per night, a bedtime around 2230 to 2300 hours, a sleep efficiency index of at least 85%, and a sleep onset latency (SOL) of less than 20 min. To exclude subjects with sleep disorders, a habituation night has been performed with standard polysomnographic techniques before the beginning of the experimentation. All data have been scored by a doctor in sleep medicine. Data gathered during these habituation nights are not shown in this present study. Their maximal oxygen uptake (V˙O2max), measured directly during a rapidly progressive incremental exercise test (25 W every minute until exhaustion) on a cycle ergometer (Lode Excalibur; Lode B.V., Groningen, Netherlands) for 1 week prior to the experiment. The maximal power output and V˙O2max averaged 384 ± 66 W and 55.5 ± 9.1 mL·min−1·kg−1, respectively. Nevertheless, subjects were recruited based on their physical levels and regular participation in national competitions in a sport specialty in their personal practice, rather than on the results of a V˙O2max or power output test.

Ethics The study was carried out in accordance with the Declaration of Helsinki on Biomedical Studies involving human participants and was approved by the local ethics committee of Regional University Hospital of Besançon (protocol no. T/2009/06 “WINAP”). The study procedures were explained to all participants and any questions about the protocol were answered. All participants signed a written informed consent form in the presence of independent witnesses. Participants were informed about their right to withdraw from the study at any time. Protocol overview The experimental protocol is described in detail in Fig. 1. Sleep conditions The participants spent a total of 4 nights in a sleep laboratory. All patients first spent 1 habituation night (HN) in the laboratory. Then, participants were randomized to 1 of 2 orders of passage for the remaining 3 nights, namely either (i) 1 baseline night (BN) and, 1 week later,1 phase-advance night (PAN1) plus a second night with phase advance (PAN2); or (ii) PAN1 plus PAN2 and, 1 week later, a BN. The HN was used to ensure that the participants had no sleep disorders and to accustom them to sleeping in the laboratory (Agnew et al. 1966). During this night, participants were accommodated in a quiet room and slept in a comfortable, soundproofed bedroom. For the BN, as for the HN, participants arrived at the laboratory at 1900 hours and the lights were turned off from 2300 until 0700 hours. Before the PAN1, participants were instructed to arrive at the laboratory at 1400 hours for dinner, and sleep was shifted in phase-advance condition (PAC) by 5 h. They were asked to change their clocks and watches. The PAC comprised PAN1 and PAN2 during which lights were turned off from 1800 to 0200 hours the day after. Published by NRC Research Press

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Fig. 1. Experimental protocol in baseline condition (a), first night phase-advance (PAN1) condition (b), and second night phase-advance (PAN2) condition (c). EEG, electroencephalography. DAY 1 in Laboratory

DAY 2 in Laboratory

Continuous recording of core body temperature BASELINE CONDITION (BC) Standardized Diner 19:00-20:00

Polysomnography EEG acquisition Baseline night (BN)

Breakfast 07:00-08:00

Standardized morning in laboratory 08:00 - 12:00

(a)

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Control EEG

23:00-07:00

Lunch 12:00-13:00

Post-lunch rest 13:00-14:00

Wingate 15:00 (30’)

Standardized Diner 19:00-20:00

Wingate 10:00 (30’)

Standardized Diner 14:00-15:00

PHASE ADVANCE CONDITION (PAC) Standardized Diner 14:00-15:00

Polysomnography EEG acquisition Phase advance night (PAN1)

(b) 18:00-02:00

Control EEG Breakfast 02:00-03:00

Lunch 07:00-08:00

Post-lunch rest 08:00-09:00

Standardized morning in laboratory 03:00-07:00

Polysomnography EEG acquisition Second night with phase advance (PAN2)

(c) 18:00-02:00

Time in laboratory

Participants did not leave the laboratory from the evening before PAN1 night until the awakening of PAN2 night. They were monitored throughout this period by an investigator. Participants stayed awake sitting, watching television, reading books, or listening to music while being controlled by polysomnography (PSG) and under constant surveillance of a technician (to avoid micro-sleeping) from 0700 to 1200 hours in the baseline condition (BC) and from 0200 to 0700 hours in the PAC. In the latter condition, once participants woke up, they were exposed to 5 h of room light (Pharos Max, 10000 Lux; 76 cm) to stay awake. Naps and intense physical activity were prohibited during the day before each experimental night. Daily motor activity was evaluated during the 24 h before the participants came to the laboratory, and for the week between conditions, by recording movements of the nondominant wrist with an Actiwatch activity monitoring system (Actiwatch AW7, CamNtech Ltd, Cambridge, UK; Cambridge Neuro-Technology). Participants were required to abstain from prohibited substances, such as tobacco, caffeine, and alcohol the week before the experiments and on the days of the experimental sessions. These abstinences were verified by an experimenter only during the presence of athletes in laboratory. Sleep recording All nights took place in a sleep laboratory, in constant temperature (18–20 °C), noise (