EIGHT WEEKS OF INTERMITTENT HYPOXIC TRAINING IMPROVES SUBMAXIMAL PHYSIOLOGICAL VARIABLES IN HIGHLY TRAINED RUNNERS BEN A. HOLLISS,1,2 RICHARD J. BURDEN,3 ANDREW M. JONES,1
AND
CHARLES R. PEDLAR3
1
College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom; 2British Swimming National Centre, Sports Training Village, University of Bath, Bath, United Kingdom; and 3Centre for Health, Applied Sport and Exercise Science, St. Mary’s University College, Twickenham, United Kingdom ABSTRACT
Holliss, BA, Burden, RJ, Jones, AM, and Pedlar, CR. Eight weeks of intermittent hypoxic training improves submaximal physiological variables in highly trained runners. J Strength Cond Res 28(8): 2195–2203, 2014—It is unclear whether intermittent hypoxic training (IHT) results in improvements in physiological variables associated with endurance running. Twelve highly trained runners (V_ O2peak 70.0 6 3.5 ml$kg21$min21) performed incremental treadmill tests to exhaustion in normobaric normoxia and hypoxia (16.0% FIO2) to assess submaximal and maximal physiological variables and the limit of tolerance (T-Lim). Participants then completed 8 weeks of moderate to heavy intensity normoxic training (control [CONT]) or IHT (twice weekly 40 minutes runs, in combination with habitual training), in a single blinded manner, before repeating the treadmill tests. Submaximal heart rate decreased significantly more after IHT (25 6 5 b$min21; p = 0.001) than after CONT ( 21 6 5 b$min21; p = 0.021). Changes in submaximal V_ O2 were significantly different between groups (p # 0.05); decreasing in the IHT group in hypoxia (22.6 6 1.7 ml$kg21$min21; p = 0.001) and increasing in the CONT group in normoxia (+1.1 6 2.1 ml$kg21$min21; p = 0.012). There were no V_ O2peak changes within either group, and while T-Lim improved post-IHT in hypoxia (p = 0.031), there were no significant differences between groups. Intermittent hypoxic training resulted in a degree of enhanced cardiovascular fitness that was evident during submaximal, but not maximal intensity exercise. These results suggest that moderate to heavy intensity IHT provides a mean of improving the capacity for submaximal exercise and may be useful for pre-acclimatization for subsequent exercise in hypoxia, but additional research is
Address correspondence to Ben A. Holliss, [email protected]. 28(8)/2195–2203 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
required to establish its efficacy for athletic performance at sea level.
KEY WORDS normobaric, single blinded, placebo INTRODUCTION
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nder hypoxic conditions, the reduced cellular oxygen partial pressure (PO2) results in an increased activity of the “oxy-gene” hypoxiainducible factor 1 (HIF-1) (15). Several HIF-1 target genes have been identified, including those encoding erythropoietin, glucose transporters, glycolytic enzymes, and vascular endothelial growth factor (27), and there is some evidence for direct effects on mitochondrial function (20,29). As such, interventions that expose athletes to altitude or hypoxia for varying durations are commonly used. The traditional approach involving spending 20 h$d21 or more for 3 weeks or more, at physical altitude, may enhance subsequent sea level endurance performance through hematologically or non hematologically mediated improvements in O2 transport and utilization (9,18). An alternative approach is for athletes to breathe a hypoxic inspirate during some of their usual exercise training, while living in normoxia, termed intermittent hypoxic training (IHT). Although IHT does not provide a sufficient exposure required for complete acclimatization (21), there have been some noteworthy adaptations reported to date. In an early study using highly trained cyclists, Terrados et al. (30) found that 3–4 weeks of moderate and heavy intensity IHT at an altitude simulation of 2300 m resulted in significantly lower submaximal exercise blood [lactate] [BLa] and significantly enhanced capillarization, compared with a normoxic trained control group (CONT). Furthermore, cycling work capacity improved significantly more after IHT than after CONT, when tested in hypoxia. Although work capacity improved in the IHT group on average by 33% in normoxia, this was not significantly different to the 22% improvement in CONT (30). Similarly, Roels et al. (26) exposed moderately trained cyclists to 7 weeks of heavy intensity IHT at an altitude simulation of VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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;3000 m. Maximal pulmonary O2 uptake (V_ O2max) significantly increased by ;9% after IHT, compared with a mean increase of ;5% after CONT, but this between group difference was not statistically significant. Moreover, the increased V_ O2max after IHT did not correspond to a greater endurance cycling performance improvement than after CONT. Another study, by Dufour et al. (5), involved 18 moderately trained men completing 6 weeks of moderate intensity IHT or CONT, at the speed corresponding to the second ventilatory threshold, at the speed corresponding to the second ventilatory threshold (2). Despite the similar training load, the IHT group experienced a significant ;5% V_ O2max increase, which did not change in CONT group, and time to exhaustion at the V_ O2max velocity also improved significantly more after IHT (+35%) compared with CONT (+10%) (5). Given that the hypoxic doses of ,2 h$d21 in Roels et al. (26) and ,1 h$d21 in Dufour et al. (5) are too small for erythropoiesis to have occurred (24), it is likely that the V_ O2max improvements were because of nonhematological adaptations (9). The frequency of IHT sessions is important, with participants in the earlier study by Terrados et al. (30) dedicating the majority of their training to the 4–5 IHT sessions per week, compared with just 2 sessions per week in Dufour et al. (5) and Roels et al. (26). The ecological validity of the design of any such IHT intervention is paramount, in that experimental treatments aimed at enhancing athletic performance should match what is likely possible to incorporate into an athlete’s training schedule. Although participants in Roels et al. (26) were “welltrained cyclists,” with a mean baseline cycling V_ O 2 max of 66 ml$kg 21 $min 21 , and participants in Dufour et al. (5) were moderately trained runners, with a mean baseline running V_ O 2 max of ;63 ml$kg 21 $min 21 , Terrados et al. (30) are the only authors to date to have assessed the effects of IHT in highly trained athletes (international standard cyclists with a mean baseline cycling V_ O 2 max of 70 ml$kg 21 $min 21 ). Moreover, IHT participants trained in a hypobaric chamber in Terrados et al. (30), and wore face masks in Dufour et al. (5), whereas CONT participants trained in normoxic laboratories, without masks, and Roels et al. (26) did not report whether participants were blinded to the environmental treatment. A lack of blinding in these may have resulted in influential placebo or nocebo effects, which must be controlled for to ascertain the efficacy of IHT as a worthwhile intervention. The purpose of this study was to investigate cardiopulmonary physiological adaptations resulting from IHT or CONT, in highly trained endurance runners, using a single blinded research design. We hypothesized that 8 weeks of IHT would elicit greater improvements in submaximal and maximal physiological variables, and would lead to an
*CONT = control; IHT = intermittent hypoxic training. †The “IHT/CONT in Lab” sessions replaced 2 of the participants’ normal outdoors runs, thus maintaining comparable total training volumes.
Easy run (75 minutes) Intense race (15–35 minutes) or rest day Easy run (30 minutes) Intense intervals (50 minutes) IHT/CONT in laboratory (40 minutes) and threshold run (50 minutes) Intense intervals (60 minutes) IHT/CONT in laboratory (40 minutes) and easy run (30 minutes)
Friday Thursday Wednesday Tuesday Monday
TABLE 1. Typical running training week during the 8-week intervention.*†
Saturday
Sunday
Simulated Altitude Training and Endurance Running
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METHODS Experimental Approach to the Problem
After a competition phase, a group of runners completed 6 weeks of routine training to ensure stability of basic fitness, and were then randomly allocated into an IHT group (n = 9) or a CONT group (n = 9), in a single blinded manner. In weeks 1 and 10, participants completed incremental exercise tests to quantify a range of submaximal and maximal physiological variables, as well as T-Lim, in a controlled laboratory environment. In between, during weeks 2–9, participants undertook their habitual training, with 2 “anaerobic threshold” runs each week replaced by 40 minutes IHT or CONT running sessions (16 3 40-minute sessions in total over the 8 weeks) (Table 1). These anaerobic threshold runs would ordinarily be 20–60 minutes, between the speed corresponding to the lactate threshold (LTspeed) and lactate turnpoint (LTPspeed) (13,28)—see “Procedures.” Subjects
Following the approval by the University of Exeter Ethics Committee, the participating athletes were instructed as to the details of the study and then provided written informed consent. Initially, there were 18 highly trained male endurance runners who volunteered for this study. Descriptive data for the 12 participants that finished the study are detailed in Table 2. They were all part of the same training group, lived in the same accommodation, and ate in the same canteen. These participants regularly competed at a national and international level in track events ranging from 1500 to 10,000 m, as well as in a variety of cross-country races. Procedures
Incremental Step Test to Volitional Exhaustion. Tests were performed at the same time of day, on the same days of the week, in normobaric normoxia (FIO2 = 20.9%) and hypoxia (FIO2 = 16.0%, equivalent to ;2150 m), each
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separated by 1 day. Participants wore a chest harness for safety, because of the high speed running, and completed a discontinuous incremental test on a treadmill (ELG; Woodway, Waukesha, WI, USA) set at a gradient of 1% to compensate for the lack of air resistance (14); this was also the case for all the IHT and CONT training sessions. Each stage lasted 3 minutes followed by a 15-second rest interval while a capillary blood sample was taken from the earlobe for [BLa] determination (Biosen C_Line; EKF, Magdeburg, Germany). The first stage was at 10 km$h21, with subsequent increments of 1.5 km$h21 each stage. Peripheral O2 saturation (SpO2) and heart rate (HR) were quantified continuously through fingertip pulse-oximetry (BCI-Autocorr; Smiths Medical, Waukesha) and telemetry (S610i; Polar Electro, Kempele, Finland). These variables and breath-bybreath V_ O2 (Oxycon-Pro; VIASYS, Ho¨echberg, Germany) were averaged over the final 60 seconds of each stage, when rating of perceived exertion (RPE) was also recorded using the Borg 6–20 scale (3). Running economy (submaximal V_ O2, relative to body weight) was measured at 14.5 km$h21, which was below the LTspeed for all participants. The running speed that elicited 4.0 mM [Bla] and the LT (LTspeed) were derived using the Lactate-E Software (22). The LTspeed was defined as the final running velocity before the first sustained increase in [Bla] above baseline (13,28). In addition, for the purpose of setting the initial training treadmill speeds, the running speed that elicited the LTP (LTPspeed) was determined by 2 independent reviewers, defined as the final running speed before the observation of a sudden and sustained rise in [Bla], at approximately 2–5 mM [Bla] (13,28). Minimum SpO2 was calculated as the lowest 5 seconds rolling average, and V_ O2peak was calculated as the highest 30 seconds rolling average. Throughout all tests, the participants were verbally encouraged to perform maximally, and the treadmill was only stopped at volitional exhaustion, when the participant placed his feet either side of the treadmill belt or lifted his legs up and became suspended from the chest harness, at which time T-Lim was
TABLE 2. Descriptive characteristics of those participants who completed the study.*† CONT group (n = 7) Age (y) Body weight (kg) Stature (cm) V_ O2peak in normoxia V_ O2peak in hypoxia
19.3 67.3 179.0 70.7 58.3
6 6 6 6 6
0.6 6.1 7.2 3.1 3.7
IHT group (n = 5) 20.2 66.5 181.3 69.2 58.2
6 6 6 6 6
0.7 6.7 8.0 4.0 4.2
Combined groups (n = 12) 19.7 67.0 180.1 70.0 58.3
6 6 6 6 6
0.8 6.1 7.3 3.5 3.8
*CONT = control; IHT = intermittent hypoxic training. _ O2peak in normoxia was measured in the laboratory at a fraction of †Participants were split into a control (CONT) or an IHT group. V
inspired oxygen (FIO2) of 20.9%, and V_ O2peak in hypoxia was measured in the same laboratory at a FIO2 of 16.0%. Participants were successfully blinded to the environmental condition during the pre-intervention and postintervention tests and all training sessions.
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Simulated Altitude Training and Endurance Running recorded to the nearest second. Based on the investigators experience of testing these caliber of athletes, maximal [Bla] ([BLa]max) was assessed at 2 minutes postexhaustion. Environmental Control and Calibrations. Ambient FIO2 and humidity were controlled by an installed S3 Hypoxic and Humidity System (Sporting Edge UK Ltd., Basingstoke, United Kingdom), switched on during all training and testing, to allow complete participant blinding. This system was accurate to within 60.1% and was checked before and during all tests (Servomex 5200; Servomex, Crowborough, United Kingdom). During the treadmill tests, participants wore a face mask for breath-by-breath V_ O2 determination using the Oxycon-Pro, which required adapted calibrations for use in hypoxia, as previously described (12). Face masks were not worn during any of the training sessions. Intermittent Hypoxic Training and Control Sessions. Each treadmill training session lasted 40 minutes, comprising a 5-minute moderate intensity warm-up at the LTspeed, a 30-minute heavy intensity core phase at the LTPspeed, and a 5-minute moderate intensity cool down at 1.0 km$h21 slower than the LTspeed. All speeds were set according to the pretraining test in the specific FIO2 environment. Heart Rate, RPE, and [Bla] were recorded every 10 minutes during the 30-minute core phase, to relativize the exercise intensity between the IHT and CONT groups. The aim was to achieve a steady state [Bla], with a rise of ,2.0 mM from 10 to
30 minutes. Treadmill speed was adjusted within the session after any 10-minute period using the following criteria: if RPE ,13 or there was a [Bla] decrease, speed was increased by 0.5 km$h21. If RPE .17 or there was an increase in [Bla] .2.0 mM, between 10 and 30 minutes, speed was decreased by 0.5 km$h21. Participants were obstructed from viewing their exercising HR, [Bla], and treadmill speeds to minimize the chances of them guessing the training or testing FIO2. When asked, after the final supervised exercise session, 46% of participants were correct, and 54% were incorrect in their guess of which environmental FIO2 they had exercised in (50% of the IHT group and 43% of the CONT group were correct in their judgment, respectively), so the blinding was judged to have been successful. Training Monitoring. The running speeds during the final 10 minutes of each of the supervised laboratory sessions were recorded and used to assess any differences in the progression between the IHT and CONT groups over the 8week intervention. In addition, all participants wore a GPS equipped watch (Forerunner 405; Garmin Ltd., Southampton, United Kingdom) during all runs completed outside the laboratory to quantify running distances. Data were analyzed to investigate any differences in total running distances between groups. Table 1 illustrates a typical training week. Resting Hematology and Nutrition. Venous blood samples were drawn from an antecubital vein through phlebotomy during
Figure 1. Changes in submaximal variables in the intermittent hypoxic training (IHT) group (black bars) and control (CONT) group (gray bars). Data are presented as mean change values, with SD error bars. #Significant training effect within the IHT or CONT group (p # 0.05). *Significant difference between the IHT and CONT groups pretraining to posttraining (p # 0.05). V_ O2 at 14.5 km$h21 significantly decreased post-IHT in hypoxia, and increased post-CONT in normoxia. Heart rate (HR) at 14.5 km$h21 decreased significantly more so post-IHT compared with post-CONT, when tested in normoxia.
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Analyses were performed using PASW Statistics (v18.0; IBM SPSS, Portsmouth, United Kingdom), with the probability level of p # 0.05 being accepted as statistically significant. Data are reported as mean 6 SD. To assess changes pretraining to posttraining, absolute changes in each dependent variable were compared between IHT and CONT groups using repeated measures analyses of covariance with mixed measures. Pretraining values for all exercise test variables were entered as covariates, to control for any baseline differences between the IHT and CONT groups.
RESULTS Of the 18 participants who started the study, 4 dropped out due to illness (IHT group n = 3, CONT group n = 1), and 2 qualified for international competitions so chose to cease
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their involvement (IHT group n = 1, CONT group n = 1). Baseline descriptive data is detailed in Table 2 for the 12 “finishers” who completed all 16 supervised treadmill sessions within the planned 8-week period. The mean running speed during all 16 of the laboratory training sessions was significantly slower in the IHT group compared with the CONT group (15.6 6 0.8 vs. 17.1 6 0.8 km$h21, p = 0.007). There was a significant increase in the mean running speed during week 1 to week 8 when results from both groups were combined (16.1 6 1.1 to 16.9 6 1.0, km$h21, p = 0.033), but there was no difference in this running speed progression between the IHT and the CONT groups (IHT 15.2 6 0.7 to 16.0 6 0.7 vs. CONT 16.8 6 0.9 to 17.5 6 0.7 km$h21, p = 0.565). Total weekly running distances were also not different between groups (IHT 85.1 6 5.1 km vs. CONT 84.6 6 5.6 km; p = 0.776). Submaximal Variables
The changes in submaximal V_ O2 were significantly different after IHT compared with CONT, in both normoxia (p = 0.003) and hypoxia (p = 0.010) (Figure 1). During normoxic tests, submaximal V_ O2 increased in 5 of the 7 CONT participants (54.1 6 2.9 to 55.2 6 1.5 ml$kg21$min21, p = 0.012) and showed a tendency to decrease post-IHT, with submaximal V_ O2 decreasing in 4 out of the 5 IHT participants (52.0 6 3.6 to 50.5 6 2.7 ml$kg21$min21, p = 0.052). In hypoxia, submaximal V_ O2 did not change post-CONT (49.0 6 1.7 to 50.3 6 1.7 ml$kg21$min21, p = 0.296), but
Figure 2. Absolute changes in T-Lim pre-intermittent hypoxic training (IHT) to post-IHT and control (CONT); black lines represent individual participants, whereas gray bars are mean values. T-Lim in hypoxia significantly increased post-IHT. #Significant training effect within the IHT group (p # 0.05).
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Figure 3. Comparisons of the changes (D) in maximal variables between the intermittent hypoxic training (IHT) (black bars) and control (CONT) (gray bars) groups. Data are presented as mean values, with SD error bars. #Significant training effect within the IHT or CONT group (p # 0.05). *Significant difference between the IHT and CONT groups pretraining to posttraining (p # 0.05). HR = heart rate.
decreased in all 5 of the IHT participants (48.6 6 3.5 to 46.0 6 1.8 ml$kg21$min21, p = 0.001). Submaximal HR when tested in normoxia decreased significantly after both IHT (154 6 13 to 148 6 8 b$min21; p = 0.001) and CONT (160 6 10 to 159 6 7 b$min21; p = 0.021), with this difference being statistically greater after IHT (p = 0.001) (Figure 1). There were no significant submaximal HR changes within or between groups in hypoxia, and there were no significant changes within groups or differences between groups in the speed at 4.0 mM [BLa] or in submaximal SpO2 (Figure 1). Maximal Variables
T-Lim remained unaltered after both CONT and IHT in normoxic conditions. During hypoxic tests, there was a significant T-Lim improvement after IHT (25.0 6 1.9 to 25.6 6 1.1 minutes; p = 0.031), but not after CONT (23.7 6 1.7 to 23.8 6 1.9 minutes; p = 0.836). However, T-Lim changes were not statistically different between the IHT and CONT groups when tested in either normoxia (p = 0.463) or hypoxia (p = 0.214) (Figure 2). While V_ O2peak in normoxia increased to a greater extent after CONT than after IHT, HRmax in hypoxia decreased to a greater extent after IHT than after CONT, and SpO2 min in normoxia increased to a greater extent after IHT than after CONT (Figure 3), such changes were not significant within either group, in either normoxic or hypoxic test
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conditions. Similarly, while in hypoxic conditions, there was a significant decrease in [Bla]max post-IHT (13.0 6 4.1 to 11.4 6 2.1 mM; p = 0.007), but not post-CONT (11.0 6 1.9 to 10.5 6 2.3 mM; p = 0.372), and there were no significant between group differences (Figure 3). Resting Hematology
[sFe] remained above 30 mg$L21 in all participants who completed the study, and the medical team had no concerns regarding the FBC red or white blood cell differential variables, which did not significantly differ from baseline, and did not differ between groups.
DISCUSSION We investigated whether 8 weeks of IHT would elicit improvements in submaximal and maximal physiological variables and incremental running T-Lim compared with CONT. Our main findings were that (a) submaximal HR reduced more after IHT, compared with CONT; (b) submaximal V_ O2 tended to increase after CONT and to decrease after IHT; and (c) although T-Lim after IHT improved in hypoxic test conditions, there were no T-Lim changes within either group in normoxic test conditions. The greater submaximal HR reductions that we observed post-IHT (mean 24%) compared with postCONT (mean 21%) indicate a greater cardiovascular fitness gain post-IHT. In a similar manner, Vallier et al. (31) reported
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Journal of Strength and Conditioning Research that submaximal HR was on average 4% lower after highly trained triathletes performed 3 weeks of IHT. Although consistent with our results, these authors used a more extreme altitude simulation (;4000 m), hypobaric rather than normobaric hypoxia, and did not include a CONT group, so it is impossible to judge to what extent the changes were because of the hypoxia, per se, or to enhanced cardiovascular fitness after exercise training. Moreover, Terrados et al. (29) found that constant submaximal load HR was reduced significantly more after highly trained cyclists undertook 3–4 weeks of IHT (at an altitude simulation of ;2300 m) compared with CONT (mean 216 vs. 212%, respectively). In this study, 5 out of the 7 CONT participants showed submaximal V_ O2 increases, which reached statistical significance in normoxia. On the contrary, of the 5 IHT participants, submaximal V_ O2 decreased in 4 of them in normoxia, and all 5 of them in hypoxia, which reached statistical significance in hypoxia. These results in conjunction with the decreased submaximal HR indicate a lower energetic cost of exercise post-IHT and an increased energetic cost of exercise post-CONT, the latter being rather surprising, as an increase in submaximal V_ O2 would not be expected after 8 weeks of training. However, in the similarly designed study by Roels et al. (26), these authors also reported a trend for submaximal V_ O2 to decrease after IHT (n = 11, 23%, tested in hypoxia) and increase after CONT (n = 11, +2%, tested in normoxia), although these differences were not statistically significant. Furthermore, Robertson et al. (25) found that submaximal V_ O2 remained unchanged in moderately trained middle distance runners who performed 3 weeks of either IHT, or IHT while living in normobaric hypoxia (3000 m simulated altitude). This study also had a number of withdrawals, meaning that there were only 12 “finishers,” thus in a similar manner to this study, the statistical power was reduced. Finally, although the aforementioned study by Dufour et al. (5) showed impressive gains in maximal physiological variables and T-Lim after IHT (n = 9) compared with CONT (n = 9), these authors also reported no significant submaximal V_ O2 changes in either group. Given the larger sample sizes, the power of statistical analyses in Roels et al. (26) and Dufour et al. (5) would have surpassed that of this study. Together with results from Robertson et al. (25), these investigations question whether the submaximal V_ O2 changes that we observed were physiologically meaningful. Nevertheless, the attenuated submaximal HR suggests that IHT may be a useful means of improving submaximal (moderate to heavy) exercise capacity, and this area warrants additional research. It is reasonable to suggest that any reduction in the energetic cost of exercise post-IHT would likely lead to an improved T-Lim. Indeed there was a significant T-Lim increase post-IHT, when participants were tested in hypoxia. Although the measure of T-Lim in this study can only provide a surrogate estimate of athletic performance, and
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changes were not statistically different between groups, the within IHT group change shows a clear trend (Figure 2). Based on this finding, and that from another of our recent IHT investigations, whereby muscle oxidative capacity improved in active men when tested in hypoxic conditions (11), we suggest that IHT elicits adaptations within skeletal muscle that result in a degree of acclimatization to subsequent hypoxia. Although an (resting) intermittent normobaric hypoxic exposure intervention has been reported not to enhance subsequent exercise tolerance at moderate altitude (7), as far as we are aware this has not been trialled using a similarly designed IHT intervention to the present study, in highly trained athletes. Results from the similar study by Dufour et al. (5) differ to this study, as after 6 weeks’ training, T-Lim in normoxia improved in all 9 IHT participants (mean + 35%; approximate range, +5 to +63%) compared with only 5 out of 9 CONT participants (mean + 10%; approximate range, 218 to +51%). Some variability is to be expected in durationblinded time to exhaustion tests, perhaps ;15% (16), but the changes reported by Dufour et al. are considerably greater, so it is suggested that the lack of FIO2 blinding and the resulting placebo or nocebo effects, were partially responsible. These researchers found no in vitro maximal oxidative capacity improvements after IHT compared with CONT, and concluded either that the participants had reached a mitochondrial adaptation plateau, or that IHT does not improve mitochondrial content (23). In contrast, studies in untrained participants by Vogt et al. (33) and Geiser et al. (8) reported significantly greater increases in mitochondrial and capillary densities after IHT compared with CONT. Similarly, Terrados et al. (29) and Melissa et al. (20) reported significant citrate synthase activity increases in the hypoxic trained legs compared with normoxic trained legs of untrained participants (using the same absolute work rates), thus indicating enhanced mitochondrial function post-IHT. Results from these studies being largely different to results in moderately trained participants (23) indicate that baseline training status likely has an important impact on adaptive outcomes. In this study, the participants’ pre-intervention V_ O2peak of 70.0 6 3.5 ml$kg21$min21 was already high, so the scope for further maximal aerobic improvements through an 8-week intervention was likely to be limited. Nevertheless, in another investigation using single-legged exercise, Bakkman et al. (1) had 8 untrained participants to undertake IHT and CONT, at 65% of the maximal attained work rate in the specific FIO2 that each leg was to be trained in. Maximal power output improved similarly in both legs, regardless of training condition, and in contrast to Terrados et al. (29) and Melissa et al. (20), citrate synthase activity increased significantly more in the CONT leg than in the IHT leg, in which there was no such change. These authors suggested that the lower absolute work rate in the IHT leg likely caused a reduced stimulus for mitochondrial VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Simulated Altitude Training and Endurance Running biogenesis (1). Furthermore, Heinonen et al. (10) demonstrated that during submaximal exercise in normobaric hypoxia, elevated cardiac output provides adequately increased muscle blood flow to counteract reductions in arterial O2 content, thus total muscle O2 delivery remains largely unaltered. It is only during high intensity whole body exercise in hypoxia that muscle O2 delivery is significantly reduced (4). On this basis, a recent study by Faiss et al. (6) found that repeated sprint cycling performance improved significantly more so after IHT compared with CONT, when equal absolute (maximal effort) workloads were used. As such, the IHT stimulus in this study, whereby the relative training intensity was essentially “clamped,” meaning that IHT participants underwent lower absolute workloads than CONT participants, may simply not have been sufficiently intense to stress O2 delivery. So the lack of observed T-Lim gains in this study, and similarly by others that used moderate to heavy intensity training (17,25,26,30), is perhaps not all that surprising. In the case of the moderate intensity, IHT study by Dufour et al. (5), again, we suggest that the performance gains were at least in part because of placebo and nocebo effects. Moreover, these authors did not report any between group statistical analyses, meaning that the effects within the IHT and CONT group were not shown to be different. In agreement with this study, Ventura et al. (32) also reported no significant performance improvements after 6 weeks’ IHT in moderately trained cyclists. However, their IHT sessions were in addition to participants’ habitual training, and these authors suggested that the lack of performance change could have been a result of over-training (32). Reductions in submaximal HR, peak [Bla], and maximal exercise capacity are commonly observed during overtraining (19), and it is possible that a similar effect occurred in this study. Our experimental design meant that training loads were maintained consistently over the 8 weeks, so participants were not able to take additional rest when feeling fatigued, as they may have done under normal circumstances. It is therefore likely that some participants experienced accumulated fatigue by the end of the intervention, which was confirmed anecdotally by the athletes and their coach, and is evidenced by the lack of T-Lim changes, the high proportion of withdrawals due to illness, and by trends toward a post-IHT reduction in normoxic V_ O2peak and HRmax. It should be acknowledged that the discontinuous combined submaximal and maximal intensity exercise test may not have provided the most sensitive means of assessing maximal exercise capacity. Instead of using T-Lim as the sole surrogate estimate of athletic performance, future similar studies should include a range of exercise capacity tests, including extended submaximal protocols to establish whether any changes in submaximal HR or V_ O2 lead to greater aerobic exercise tolerance, and also using more ecologically valid assessments of maximal performance capacity.
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In conclusion, 8 weeks of IHT resulted in significantly lower submaximal HR and a tendency for a reduced oxygen cost of submaximal exercise. Although incremental running time to exhaustion improved in hypoxic conditions, changes in normoxic test conditions were not apparent.
PRACTICAL APPLICATIONS The results of this study do not support the use of moderate intensity IHT to enhance athletic performance at sea level. One potential use for such an IHT intervention is during pre-acclimatization for subsequent training in hypoxia, although this concept requires more direct assessment, with performance being quantified using more ecologically valid methods (e.g., competitive races). It is recommended that those professionals who supervise IHT interventions closely monitor individual athlete fatigue and well-being, and that research is carried out into the fatigue consequent to IHT in more depth, especially if equal absolute workloads are used for IHT as they would be for normoxic training. Recent literature suggests that IHT using severe or supramaximal intensity exercise may provide an additional benefit on athletic performance than normoxic training, at least for repeated sprint type activities, but these claims must be further substantiated. In particular, future research should comprise rigorously designed double-blinded assessments of the effects of whole body severe or supramaximal intensity IHT in highly trained athletes, as there is a scarcity of data in this population.
ACKNOWLEDGMENTS The academic tuition fees related to this research were in part funded by British Swimming (www.swimming.org), the English Institute of Sport (www.eis2win.co.uk), and Sporting Edge UK Ltd (www.sportingedgeuk.co.uk).
REFERENCES 1. Bakkman, L, Sahlin, K, Holmberg, HC, and Tonkonogi, M. Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol (Oxf ) 190: 243–251, 2007. 2. Beaver, WL, Wasserman, K, and Whipp, BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol (1985) 60: 2020–2027, 1986. 3. Borg, G. The borg RPE scale. In: Borg’s Perceived Exertion and Pain Scales. G. Borg, ed. Champaign, IL: Human Kinetics, 1998. pp. 29–38. 4. Calbet, JA, Radegran, G, Boushel, R, and Saltin, B. On the mechanisms that limit oxygen uptake during exercise in acute and chronic hypoxia: Role of muscle mass. J Physiol 587: 477–490, 2009. 5. Dufour, SP, Ponsot, E, Zoll, J, Doutreleau, S, Lonsdorfer-Wolf, E, Geny, B, Lampert, E, Fluck, M, Hoppeler, H, Billat, V, Mettauer, B, Richard, R, and Lonsdorfer, J. Exercise training in normobaric hypoxia in endurance runners. I. Improvement in aerobic performance capacity. J Appl Physiol (1985) 100: 1238–1248, 2006.
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Journal of Strength and Conditioning Research 6. Faiss, R, Leger, B, Vesin, JM, Fournier, PE, Eggel, Y, Deriaz, O, and Millet, GP. Significant molecular and systemic adaptations after repeated sprint training in hypoxia. PLoS One 8: e56522, 2013. 7. Faulhaber, M, Gatterer, H, Haider, T, Patterson, C, and Burtscher, M. Intermittent hypoxia does not affect endurance performance at moderate altitude in well-trained athletes. J Sports Sci 28: 513–519, 2010. 8. Geiser, J, Vogt, M, Billeter, R, Zuleger, C, Belforti, F, and Hoppeler, H. Training high–living low: Changes of aerobic performance and muscle structure with training at simulated altitude. Int J Sports Med 22: 579–585, 2001. 9. Gore, CJ and Hopkins, WG. Counterpoint: Positive effects of intermittent hypoxia (live high:train low) on exercise performance are not mediated primarily by augmented red cell volume. J Appl Physiol (1985) 99: 2055–2057, 2005. 10. Heinonen, IH, Kemppainen, J, Kaskinoro, K, Peltonen, JE, Borra, R, Lindroos, M, Oikonen, V, Nuutila, P, Knuuti, J, Boushel, R, and Kalliokoski, KK. Regulation of human skeletal muscle perfusion and its heterogeneity during exercise in moderate hypoxia. Am J Physiol Regul Integr Comp Physiol 299: R72–R79, 2010. 11. Holliss, BA, Fulford, J, Vanhatalo, A, Pedlar, CR, and Jones, AM. Influence of intermittent hypoxic training on muscle energetics and exercise tolerance. J Appl Physiol (1985) 114: 611–619, 2013. 12. Holliss, BA, Pedlar, C, Glaister, M, and Jones, A. Validity of the Ja¨eger Oxycon-ProÒ expired air analyzer in normobaric hypoxia. Presented at 16th Annual Congress of the European College of Sport Science, Liverpool, United Kingdom, 6–9 July, 2011. 13. Jones, AM. The physiology of the world record holder for the women’s marathon. Int J Sports Sci Coach 1: 101–115, 2006.
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20. Melissa, L, MacDougall, JD, Tarnopolsky, MA, Cipriano, N, and Green, HJ. Skeletal muscle adaptations to training under normobaric hypoxic versus normoxic conditions. Med Sci Sports Exerc 29: 238–243, 1997. 21. Millet, GP, Roels, B, Schmitt, L, Woorons, X, and Richalet, JP. Combining hypoxic methods for peak performance. Sports Med 40: 1–25, 2010. 22. Newell, J, Higgins, D, Madden, N, Cruickshank, J, Einbeck, J, McMillan, K, and McDonald, R. Software for calculating blood lactate endurance markers. J Sports Sci 25: 1403–1409, 2007. 23. Ponsot, E, Dufour, SP, Zoll, J, Doutrelau, S, N’Guessan, B, Geny, B, Hoppeler, H, Lampert, E, Mettauer, B, Ventura-Clapier, R, and Richard, R. Exercise training in normobaric hypoxia in endurance runners. II. Improvement of mitochondrial properties in skeletal muscle. J Appl Physiol (1985) 100: 1249–1257, 2006. 24. Rasmussen, P, Siebenmann, C, Diaz, V, and Lundby, C. Red cell volume expansion at altitude: A meta-analysis and Monte Carlo simulation. Med Sci Sports Exerc 45: 1767–1772, 2013. 25. Robertson, EY, Saunders, PU, Pyne, DB, Gore, CJ, and Anson, JM. Effectiveness of intermittent training in hypoxia combined with live high/train low. Eur J Appl Physiol 110: 379–387, 2010. 26. Roels, B, Millet, GP, Marcoux, CJ, Coste, O, Bentley, DJ, and Candau, RB. Effects of hypoxic interval training on cycling performance. Med Sci Sports Exerc 37: 138–146, 2005. 27. Semenza, GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551–578, 1999.
14. Jones, AM and Doust, JH. A 1% treadmill grade most accurately reflects the energetic cost of outdoor running. J Sports Sci 14: 321–327, 1996.
28. Smith, CG and Jones, AM. The relationship between critical velocity, maximal lactate steady-state velocity and lactate turnpoint velocity in runners. Eur J Appl Physiol 85: 19–26, 2001.
15. Kallio, PJ, Wilson, WJ, O’Brien, S, Makino, Y, and Poellinger, L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem 274: 6519–6525, 1999.
29. Terrados, N, Jansson, E, Sylven, C, and Kaijser, L. Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol (1985) 68: 2369–2372, 1990.
16. Laursen, PB, Francis, GT, Abbiss, CR, Newton, MJ, and Nosaka, K. Reliability of time-to-exhaustion versus time-trial running tests in runners. Med Sci Sports Exerc 39: 1374–1379, 2007.
30. Terrados, N, Melichna, J, Sylven, C, Jansson, E, and Kaijser, L. Effects of training at simulated altitude on performance and muscle metabolic capacity in competitive road cyclists. Eur J Appl Physiol Occup Physiol 57: 203–209, 1988.
17. Lecoultre, V, Boss, A, Tappy, L, Borrani, F, Tran, C, Schneiter, P, and Schutz, Y. Training in hypoxia fails to further enhance endurance performance and lactate clearance in well-trained men and impairs glucose metabolism during prolonged exercise. Exp Physiol 95: 315– 330, 2010. 18. Levine, BD and Stray-Gundersen, J. Point: Positive effects of intermittent hypoxia (live high:train low) on exercise performance are mediated primarily by augmented red cell volume. J Appl Physiol (1985) 99: 2053–2055, 2005. 19. Meeusen, R, Nederhof, E, Buyse, L, Roelands, B, de Schutter, G, and Piacentini, MF. Diagnosing overtraining in athletes using the twobout exercise protocol. Br J Sports Med 44: 642–648, 2010.
31. Vallier, JM, Chateau, P, and Guezennec, CY. Effects of physical training in a hypobaric chamber on the physical performance of competitive triathletes. Eur J Appl Physiol Occup Physiol 73: 471–478, 1996. 32. Ventura, N, Hoppeler, H, Seiler, R, Binggeli, A, Mullis, P, and Vogt, M. The response of trained athletes to six weeks of endurance training in hypoxia or normoxia. Int J Sports Med 24: 166–172, 2003. 33. Vogt, M, Puntschart, A, Geiser, J, Zuleger, C, Billeter, R, and Hoppeler, H. Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol (1985) 91: 173–182, 2001.
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CHARLES R. PEDLAR3
1
College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom; 2British Swimming National Centre, Sports Training Village, University of Bath, Bath, United Kingdom; and 3Centre for Health, Applied Sport and Exercise Science, St. Mary’s University College, Twickenham, United Kingdom ABSTRACT
Holliss, BA, Burden, RJ, Jones, AM, and Pedlar, CR. Eight weeks of intermittent hypoxic training improves submaximal physiological variables in highly trained runners. J Strength Cond Res 28(8): 2195–2203, 2014—It is unclear whether intermittent hypoxic training (IHT) results in improvements in physiological variables associated with endurance running. Twelve highly trained runners (V_ O2peak 70.0 6 3.5 ml$kg21$min21) performed incremental treadmill tests to exhaustion in normobaric normoxia and hypoxia (16.0% FIO2) to assess submaximal and maximal physiological variables and the limit of tolerance (T-Lim). Participants then completed 8 weeks of moderate to heavy intensity normoxic training (control [CONT]) or IHT (twice weekly 40 minutes runs, in combination with habitual training), in a single blinded manner, before repeating the treadmill tests. Submaximal heart rate decreased significantly more after IHT (25 6 5 b$min21; p = 0.001) than after CONT ( 21 6 5 b$min21; p = 0.021). Changes in submaximal V_ O2 were significantly different between groups (p # 0.05); decreasing in the IHT group in hypoxia (22.6 6 1.7 ml$kg21$min21; p = 0.001) and increasing in the CONT group in normoxia (+1.1 6 2.1 ml$kg21$min21; p = 0.012). There were no V_ O2peak changes within either group, and while T-Lim improved post-IHT in hypoxia (p = 0.031), there were no significant differences between groups. Intermittent hypoxic training resulted in a degree of enhanced cardiovascular fitness that was evident during submaximal, but not maximal intensity exercise. These results suggest that moderate to heavy intensity IHT provides a mean of improving the capacity for submaximal exercise and may be useful for pre-acclimatization for subsequent exercise in hypoxia, but additional research is
Address correspondence to Ben A. Holliss, [email protected]. 28(8)/2195–2203 Journal of Strength and Conditioning Research Ó 2014 National Strength and Conditioning Association
required to establish its efficacy for athletic performance at sea level.
KEY WORDS normobaric, single blinded, placebo INTRODUCTION
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nder hypoxic conditions, the reduced cellular oxygen partial pressure (PO2) results in an increased activity of the “oxy-gene” hypoxiainducible factor 1 (HIF-1) (15). Several HIF-1 target genes have been identified, including those encoding erythropoietin, glucose transporters, glycolytic enzymes, and vascular endothelial growth factor (27), and there is some evidence for direct effects on mitochondrial function (20,29). As such, interventions that expose athletes to altitude or hypoxia for varying durations are commonly used. The traditional approach involving spending 20 h$d21 or more for 3 weeks or more, at physical altitude, may enhance subsequent sea level endurance performance through hematologically or non hematologically mediated improvements in O2 transport and utilization (9,18). An alternative approach is for athletes to breathe a hypoxic inspirate during some of their usual exercise training, while living in normoxia, termed intermittent hypoxic training (IHT). Although IHT does not provide a sufficient exposure required for complete acclimatization (21), there have been some noteworthy adaptations reported to date. In an early study using highly trained cyclists, Terrados et al. (30) found that 3–4 weeks of moderate and heavy intensity IHT at an altitude simulation of 2300 m resulted in significantly lower submaximal exercise blood [lactate] [BLa] and significantly enhanced capillarization, compared with a normoxic trained control group (CONT). Furthermore, cycling work capacity improved significantly more after IHT than after CONT, when tested in hypoxia. Although work capacity improved in the IHT group on average by 33% in normoxia, this was not significantly different to the 22% improvement in CONT (30). Similarly, Roels et al. (26) exposed moderately trained cyclists to 7 weeks of heavy intensity IHT at an altitude simulation of VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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;3000 m. Maximal pulmonary O2 uptake (V_ O2max) significantly increased by ;9% after IHT, compared with a mean increase of ;5% after CONT, but this between group difference was not statistically significant. Moreover, the increased V_ O2max after IHT did not correspond to a greater endurance cycling performance improvement than after CONT. Another study, by Dufour et al. (5), involved 18 moderately trained men completing 6 weeks of moderate intensity IHT or CONT, at the speed corresponding to the second ventilatory threshold, at the speed corresponding to the second ventilatory threshold (2). Despite the similar training load, the IHT group experienced a significant ;5% V_ O2max increase, which did not change in CONT group, and time to exhaustion at the V_ O2max velocity also improved significantly more after IHT (+35%) compared with CONT (+10%) (5). Given that the hypoxic doses of ,2 h$d21 in Roels et al. (26) and ,1 h$d21 in Dufour et al. (5) are too small for erythropoiesis to have occurred (24), it is likely that the V_ O2max improvements were because of nonhematological adaptations (9). The frequency of IHT sessions is important, with participants in the earlier study by Terrados et al. (30) dedicating the majority of their training to the 4–5 IHT sessions per week, compared with just 2 sessions per week in Dufour et al. (5) and Roels et al. (26). The ecological validity of the design of any such IHT intervention is paramount, in that experimental treatments aimed at enhancing athletic performance should match what is likely possible to incorporate into an athlete’s training schedule. Although participants in Roels et al. (26) were “welltrained cyclists,” with a mean baseline cycling V_ O 2 max of 66 ml$kg 21 $min 21 , and participants in Dufour et al. (5) were moderately trained runners, with a mean baseline running V_ O 2 max of ;63 ml$kg 21 $min 21 , Terrados et al. (30) are the only authors to date to have assessed the effects of IHT in highly trained athletes (international standard cyclists with a mean baseline cycling V_ O 2 max of 70 ml$kg 21 $min 21 ). Moreover, IHT participants trained in a hypobaric chamber in Terrados et al. (30), and wore face masks in Dufour et al. (5), whereas CONT participants trained in normoxic laboratories, without masks, and Roels et al. (26) did not report whether participants were blinded to the environmental treatment. A lack of blinding in these may have resulted in influential placebo or nocebo effects, which must be controlled for to ascertain the efficacy of IHT as a worthwhile intervention. The purpose of this study was to investigate cardiopulmonary physiological adaptations resulting from IHT or CONT, in highly trained endurance runners, using a single blinded research design. We hypothesized that 8 weeks of IHT would elicit greater improvements in submaximal and maximal physiological variables, and would lead to an
*CONT = control; IHT = intermittent hypoxic training. †The “IHT/CONT in Lab” sessions replaced 2 of the participants’ normal outdoors runs, thus maintaining comparable total training volumes.
Easy run (75 minutes) Intense race (15–35 minutes) or rest day Easy run (30 minutes) Intense intervals (50 minutes) IHT/CONT in laboratory (40 minutes) and threshold run (50 minutes) Intense intervals (60 minutes) IHT/CONT in laboratory (40 minutes) and easy run (30 minutes)
Friday Thursday Wednesday Tuesday Monday
TABLE 1. Typical running training week during the 8-week intervention.*†
Saturday
Sunday
Simulated Altitude Training and Endurance Running
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Journal of Strength and Conditioning Research enhanced incremental exercise limit of tolerance (T-Lim), compared with CONT.
METHODS Experimental Approach to the Problem
After a competition phase, a group of runners completed 6 weeks of routine training to ensure stability of basic fitness, and were then randomly allocated into an IHT group (n = 9) or a CONT group (n = 9), in a single blinded manner. In weeks 1 and 10, participants completed incremental exercise tests to quantify a range of submaximal and maximal physiological variables, as well as T-Lim, in a controlled laboratory environment. In between, during weeks 2–9, participants undertook their habitual training, with 2 “anaerobic threshold” runs each week replaced by 40 minutes IHT or CONT running sessions (16 3 40-minute sessions in total over the 8 weeks) (Table 1). These anaerobic threshold runs would ordinarily be 20–60 minutes, between the speed corresponding to the lactate threshold (LTspeed) and lactate turnpoint (LTPspeed) (13,28)—see “Procedures.” Subjects
Following the approval by the University of Exeter Ethics Committee, the participating athletes were instructed as to the details of the study and then provided written informed consent. Initially, there were 18 highly trained male endurance runners who volunteered for this study. Descriptive data for the 12 participants that finished the study are detailed in Table 2. They were all part of the same training group, lived in the same accommodation, and ate in the same canteen. These participants regularly competed at a national and international level in track events ranging from 1500 to 10,000 m, as well as in a variety of cross-country races. Procedures
Incremental Step Test to Volitional Exhaustion. Tests were performed at the same time of day, on the same days of the week, in normobaric normoxia (FIO2 = 20.9%) and hypoxia (FIO2 = 16.0%, equivalent to ;2150 m), each
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separated by 1 day. Participants wore a chest harness for safety, because of the high speed running, and completed a discontinuous incremental test on a treadmill (ELG; Woodway, Waukesha, WI, USA) set at a gradient of 1% to compensate for the lack of air resistance (14); this was also the case for all the IHT and CONT training sessions. Each stage lasted 3 minutes followed by a 15-second rest interval while a capillary blood sample was taken from the earlobe for [BLa] determination (Biosen C_Line; EKF, Magdeburg, Germany). The first stage was at 10 km$h21, with subsequent increments of 1.5 km$h21 each stage. Peripheral O2 saturation (SpO2) and heart rate (HR) were quantified continuously through fingertip pulse-oximetry (BCI-Autocorr; Smiths Medical, Waukesha) and telemetry (S610i; Polar Electro, Kempele, Finland). These variables and breath-bybreath V_ O2 (Oxycon-Pro; VIASYS, Ho¨echberg, Germany) were averaged over the final 60 seconds of each stage, when rating of perceived exertion (RPE) was also recorded using the Borg 6–20 scale (3). Running economy (submaximal V_ O2, relative to body weight) was measured at 14.5 km$h21, which was below the LTspeed for all participants. The running speed that elicited 4.0 mM [Bla] and the LT (LTspeed) were derived using the Lactate-E Software (22). The LTspeed was defined as the final running velocity before the first sustained increase in [Bla] above baseline (13,28). In addition, for the purpose of setting the initial training treadmill speeds, the running speed that elicited the LTP (LTPspeed) was determined by 2 independent reviewers, defined as the final running speed before the observation of a sudden and sustained rise in [Bla], at approximately 2–5 mM [Bla] (13,28). Minimum SpO2 was calculated as the lowest 5 seconds rolling average, and V_ O2peak was calculated as the highest 30 seconds rolling average. Throughout all tests, the participants were verbally encouraged to perform maximally, and the treadmill was only stopped at volitional exhaustion, when the participant placed his feet either side of the treadmill belt or lifted his legs up and became suspended from the chest harness, at which time T-Lim was
TABLE 2. Descriptive characteristics of those participants who completed the study.*† CONT group (n = 7) Age (y) Body weight (kg) Stature (cm) V_ O2peak in normoxia V_ O2peak in hypoxia
19.3 67.3 179.0 70.7 58.3
6 6 6 6 6
0.6 6.1 7.2 3.1 3.7
IHT group (n = 5) 20.2 66.5 181.3 69.2 58.2
6 6 6 6 6
0.7 6.7 8.0 4.0 4.2
Combined groups (n = 12) 19.7 67.0 180.1 70.0 58.3
6 6 6 6 6
0.8 6.1 7.3 3.5 3.8
*CONT = control; IHT = intermittent hypoxic training. _ O2peak in normoxia was measured in the laboratory at a fraction of †Participants were split into a control (CONT) or an IHT group. V
inspired oxygen (FIO2) of 20.9%, and V_ O2peak in hypoxia was measured in the same laboratory at a FIO2 of 16.0%. Participants were successfully blinded to the environmental condition during the pre-intervention and postintervention tests and all training sessions.
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Simulated Altitude Training and Endurance Running recorded to the nearest second. Based on the investigators experience of testing these caliber of athletes, maximal [Bla] ([BLa]max) was assessed at 2 minutes postexhaustion. Environmental Control and Calibrations. Ambient FIO2 and humidity were controlled by an installed S3 Hypoxic and Humidity System (Sporting Edge UK Ltd., Basingstoke, United Kingdom), switched on during all training and testing, to allow complete participant blinding. This system was accurate to within 60.1% and was checked before and during all tests (Servomex 5200; Servomex, Crowborough, United Kingdom). During the treadmill tests, participants wore a face mask for breath-by-breath V_ O2 determination using the Oxycon-Pro, which required adapted calibrations for use in hypoxia, as previously described (12). Face masks were not worn during any of the training sessions. Intermittent Hypoxic Training and Control Sessions. Each treadmill training session lasted 40 minutes, comprising a 5-minute moderate intensity warm-up at the LTspeed, a 30-minute heavy intensity core phase at the LTPspeed, and a 5-minute moderate intensity cool down at 1.0 km$h21 slower than the LTspeed. All speeds were set according to the pretraining test in the specific FIO2 environment. Heart Rate, RPE, and [Bla] were recorded every 10 minutes during the 30-minute core phase, to relativize the exercise intensity between the IHT and CONT groups. The aim was to achieve a steady state [Bla], with a rise of ,2.0 mM from 10 to
30 minutes. Treadmill speed was adjusted within the session after any 10-minute period using the following criteria: if RPE ,13 or there was a [Bla] decrease, speed was increased by 0.5 km$h21. If RPE .17 or there was an increase in [Bla] .2.0 mM, between 10 and 30 minutes, speed was decreased by 0.5 km$h21. Participants were obstructed from viewing their exercising HR, [Bla], and treadmill speeds to minimize the chances of them guessing the training or testing FIO2. When asked, after the final supervised exercise session, 46% of participants were correct, and 54% were incorrect in their guess of which environmental FIO2 they had exercised in (50% of the IHT group and 43% of the CONT group were correct in their judgment, respectively), so the blinding was judged to have been successful. Training Monitoring. The running speeds during the final 10 minutes of each of the supervised laboratory sessions were recorded and used to assess any differences in the progression between the IHT and CONT groups over the 8week intervention. In addition, all participants wore a GPS equipped watch (Forerunner 405; Garmin Ltd., Southampton, United Kingdom) during all runs completed outside the laboratory to quantify running distances. Data were analyzed to investigate any differences in total running distances between groups. Table 1 illustrates a typical training week. Resting Hematology and Nutrition. Venous blood samples were drawn from an antecubital vein through phlebotomy during
Figure 1. Changes in submaximal variables in the intermittent hypoxic training (IHT) group (black bars) and control (CONT) group (gray bars). Data are presented as mean change values, with SD error bars. #Significant training effect within the IHT or CONT group (p # 0.05). *Significant difference between the IHT and CONT groups pretraining to posttraining (p # 0.05). V_ O2 at 14.5 km$h21 significantly decreased post-IHT in hypoxia, and increased post-CONT in normoxia. Heart rate (HR) at 14.5 km$h21 decreased significantly more so post-IHT compared with post-CONT, when tested in normoxia.
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Journal of Strength and Conditioning Research weeks 1, 5, and 10, to screen for illness and to ensure adequate iron stores (serum ferritin concentration ([sFe]) $30 mg$L21). Within 2 hours, samples were analyzed for full blood count (FBC) using an automated cell counter (ADVIA 120; Siemens AG, Erlangen, Germany) and [sFe] using a chemiluminescent microparticle immunoassay (ARCHITECT Ferritin Assay; Abbott Point of Care Inc., Birmingham, United Kingdom). Furthermore, to stress the importance of adequate dietary iron and other nutrient intake, all participants attended a 45-minute nutrition seminar by an experienced sports dietician during week 1. Statistical Analyses
Analyses were performed using PASW Statistics (v18.0; IBM SPSS, Portsmouth, United Kingdom), with the probability level of p # 0.05 being accepted as statistically significant. Data are reported as mean 6 SD. To assess changes pretraining to posttraining, absolute changes in each dependent variable were compared between IHT and CONT groups using repeated measures analyses of covariance with mixed measures. Pretraining values for all exercise test variables were entered as covariates, to control for any baseline differences between the IHT and CONT groups.
RESULTS Of the 18 participants who started the study, 4 dropped out due to illness (IHT group n = 3, CONT group n = 1), and 2 qualified for international competitions so chose to cease
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their involvement (IHT group n = 1, CONT group n = 1). Baseline descriptive data is detailed in Table 2 for the 12 “finishers” who completed all 16 supervised treadmill sessions within the planned 8-week period. The mean running speed during all 16 of the laboratory training sessions was significantly slower in the IHT group compared with the CONT group (15.6 6 0.8 vs. 17.1 6 0.8 km$h21, p = 0.007). There was a significant increase in the mean running speed during week 1 to week 8 when results from both groups were combined (16.1 6 1.1 to 16.9 6 1.0, km$h21, p = 0.033), but there was no difference in this running speed progression between the IHT and the CONT groups (IHT 15.2 6 0.7 to 16.0 6 0.7 vs. CONT 16.8 6 0.9 to 17.5 6 0.7 km$h21, p = 0.565). Total weekly running distances were also not different between groups (IHT 85.1 6 5.1 km vs. CONT 84.6 6 5.6 km; p = 0.776). Submaximal Variables
The changes in submaximal V_ O2 were significantly different after IHT compared with CONT, in both normoxia (p = 0.003) and hypoxia (p = 0.010) (Figure 1). During normoxic tests, submaximal V_ O2 increased in 5 of the 7 CONT participants (54.1 6 2.9 to 55.2 6 1.5 ml$kg21$min21, p = 0.012) and showed a tendency to decrease post-IHT, with submaximal V_ O2 decreasing in 4 out of the 5 IHT participants (52.0 6 3.6 to 50.5 6 2.7 ml$kg21$min21, p = 0.052). In hypoxia, submaximal V_ O2 did not change post-CONT (49.0 6 1.7 to 50.3 6 1.7 ml$kg21$min21, p = 0.296), but
Figure 2. Absolute changes in T-Lim pre-intermittent hypoxic training (IHT) to post-IHT and control (CONT); black lines represent individual participants, whereas gray bars are mean values. T-Lim in hypoxia significantly increased post-IHT. #Significant training effect within the IHT group (p # 0.05).
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Figure 3. Comparisons of the changes (D) in maximal variables between the intermittent hypoxic training (IHT) (black bars) and control (CONT) (gray bars) groups. Data are presented as mean values, with SD error bars. #Significant training effect within the IHT or CONT group (p # 0.05). *Significant difference between the IHT and CONT groups pretraining to posttraining (p # 0.05). HR = heart rate.
decreased in all 5 of the IHT participants (48.6 6 3.5 to 46.0 6 1.8 ml$kg21$min21, p = 0.001). Submaximal HR when tested in normoxia decreased significantly after both IHT (154 6 13 to 148 6 8 b$min21; p = 0.001) and CONT (160 6 10 to 159 6 7 b$min21; p = 0.021), with this difference being statistically greater after IHT (p = 0.001) (Figure 1). There were no significant submaximal HR changes within or between groups in hypoxia, and there were no significant changes within groups or differences between groups in the speed at 4.0 mM [BLa] or in submaximal SpO2 (Figure 1). Maximal Variables
T-Lim remained unaltered after both CONT and IHT in normoxic conditions. During hypoxic tests, there was a significant T-Lim improvement after IHT (25.0 6 1.9 to 25.6 6 1.1 minutes; p = 0.031), but not after CONT (23.7 6 1.7 to 23.8 6 1.9 minutes; p = 0.836). However, T-Lim changes were not statistically different between the IHT and CONT groups when tested in either normoxia (p = 0.463) or hypoxia (p = 0.214) (Figure 2). While V_ O2peak in normoxia increased to a greater extent after CONT than after IHT, HRmax in hypoxia decreased to a greater extent after IHT than after CONT, and SpO2 min in normoxia increased to a greater extent after IHT than after CONT (Figure 3), such changes were not significant within either group, in either normoxic or hypoxic test
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conditions. Similarly, while in hypoxic conditions, there was a significant decrease in [Bla]max post-IHT (13.0 6 4.1 to 11.4 6 2.1 mM; p = 0.007), but not post-CONT (11.0 6 1.9 to 10.5 6 2.3 mM; p = 0.372), and there were no significant between group differences (Figure 3). Resting Hematology
[sFe] remained above 30 mg$L21 in all participants who completed the study, and the medical team had no concerns regarding the FBC red or white blood cell differential variables, which did not significantly differ from baseline, and did not differ between groups.
DISCUSSION We investigated whether 8 weeks of IHT would elicit improvements in submaximal and maximal physiological variables and incremental running T-Lim compared with CONT. Our main findings were that (a) submaximal HR reduced more after IHT, compared with CONT; (b) submaximal V_ O2 tended to increase after CONT and to decrease after IHT; and (c) although T-Lim after IHT improved in hypoxic test conditions, there were no T-Lim changes within either group in normoxic test conditions. The greater submaximal HR reductions that we observed post-IHT (mean 24%) compared with postCONT (mean 21%) indicate a greater cardiovascular fitness gain post-IHT. In a similar manner, Vallier et al. (31) reported
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Journal of Strength and Conditioning Research that submaximal HR was on average 4% lower after highly trained triathletes performed 3 weeks of IHT. Although consistent with our results, these authors used a more extreme altitude simulation (;4000 m), hypobaric rather than normobaric hypoxia, and did not include a CONT group, so it is impossible to judge to what extent the changes were because of the hypoxia, per se, or to enhanced cardiovascular fitness after exercise training. Moreover, Terrados et al. (29) found that constant submaximal load HR was reduced significantly more after highly trained cyclists undertook 3–4 weeks of IHT (at an altitude simulation of ;2300 m) compared with CONT (mean 216 vs. 212%, respectively). In this study, 5 out of the 7 CONT participants showed submaximal V_ O2 increases, which reached statistical significance in normoxia. On the contrary, of the 5 IHT participants, submaximal V_ O2 decreased in 4 of them in normoxia, and all 5 of them in hypoxia, which reached statistical significance in hypoxia. These results in conjunction with the decreased submaximal HR indicate a lower energetic cost of exercise post-IHT and an increased energetic cost of exercise post-CONT, the latter being rather surprising, as an increase in submaximal V_ O2 would not be expected after 8 weeks of training. However, in the similarly designed study by Roels et al. (26), these authors also reported a trend for submaximal V_ O2 to decrease after IHT (n = 11, 23%, tested in hypoxia) and increase after CONT (n = 11, +2%, tested in normoxia), although these differences were not statistically significant. Furthermore, Robertson et al. (25) found that submaximal V_ O2 remained unchanged in moderately trained middle distance runners who performed 3 weeks of either IHT, or IHT while living in normobaric hypoxia (3000 m simulated altitude). This study also had a number of withdrawals, meaning that there were only 12 “finishers,” thus in a similar manner to this study, the statistical power was reduced. Finally, although the aforementioned study by Dufour et al. (5) showed impressive gains in maximal physiological variables and T-Lim after IHT (n = 9) compared with CONT (n = 9), these authors also reported no significant submaximal V_ O2 changes in either group. Given the larger sample sizes, the power of statistical analyses in Roels et al. (26) and Dufour et al. (5) would have surpassed that of this study. Together with results from Robertson et al. (25), these investigations question whether the submaximal V_ O2 changes that we observed were physiologically meaningful. Nevertheless, the attenuated submaximal HR suggests that IHT may be a useful means of improving submaximal (moderate to heavy) exercise capacity, and this area warrants additional research. It is reasonable to suggest that any reduction in the energetic cost of exercise post-IHT would likely lead to an improved T-Lim. Indeed there was a significant T-Lim increase post-IHT, when participants were tested in hypoxia. Although the measure of T-Lim in this study can only provide a surrogate estimate of athletic performance, and
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changes were not statistically different between groups, the within IHT group change shows a clear trend (Figure 2). Based on this finding, and that from another of our recent IHT investigations, whereby muscle oxidative capacity improved in active men when tested in hypoxic conditions (11), we suggest that IHT elicits adaptations within skeletal muscle that result in a degree of acclimatization to subsequent hypoxia. Although an (resting) intermittent normobaric hypoxic exposure intervention has been reported not to enhance subsequent exercise tolerance at moderate altitude (7), as far as we are aware this has not been trialled using a similarly designed IHT intervention to the present study, in highly trained athletes. Results from the similar study by Dufour et al. (5) differ to this study, as after 6 weeks’ training, T-Lim in normoxia improved in all 9 IHT participants (mean + 35%; approximate range, +5 to +63%) compared with only 5 out of 9 CONT participants (mean + 10%; approximate range, 218 to +51%). Some variability is to be expected in durationblinded time to exhaustion tests, perhaps ;15% (16), but the changes reported by Dufour et al. are considerably greater, so it is suggested that the lack of FIO2 blinding and the resulting placebo or nocebo effects, were partially responsible. These researchers found no in vitro maximal oxidative capacity improvements after IHT compared with CONT, and concluded either that the participants had reached a mitochondrial adaptation plateau, or that IHT does not improve mitochondrial content (23). In contrast, studies in untrained participants by Vogt et al. (33) and Geiser et al. (8) reported significantly greater increases in mitochondrial and capillary densities after IHT compared with CONT. Similarly, Terrados et al. (29) and Melissa et al. (20) reported significant citrate synthase activity increases in the hypoxic trained legs compared with normoxic trained legs of untrained participants (using the same absolute work rates), thus indicating enhanced mitochondrial function post-IHT. Results from these studies being largely different to results in moderately trained participants (23) indicate that baseline training status likely has an important impact on adaptive outcomes. In this study, the participants’ pre-intervention V_ O2peak of 70.0 6 3.5 ml$kg21$min21 was already high, so the scope for further maximal aerobic improvements through an 8-week intervention was likely to be limited. Nevertheless, in another investigation using single-legged exercise, Bakkman et al. (1) had 8 untrained participants to undertake IHT and CONT, at 65% of the maximal attained work rate in the specific FIO2 that each leg was to be trained in. Maximal power output improved similarly in both legs, regardless of training condition, and in contrast to Terrados et al. (29) and Melissa et al. (20), citrate synthase activity increased significantly more in the CONT leg than in the IHT leg, in which there was no such change. These authors suggested that the lower absolute work rate in the IHT leg likely caused a reduced stimulus for mitochondrial VOLUME 28 | NUMBER 8 | AUGUST 2014 |
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Simulated Altitude Training and Endurance Running biogenesis (1). Furthermore, Heinonen et al. (10) demonstrated that during submaximal exercise in normobaric hypoxia, elevated cardiac output provides adequately increased muscle blood flow to counteract reductions in arterial O2 content, thus total muscle O2 delivery remains largely unaltered. It is only during high intensity whole body exercise in hypoxia that muscle O2 delivery is significantly reduced (4). On this basis, a recent study by Faiss et al. (6) found that repeated sprint cycling performance improved significantly more so after IHT compared with CONT, when equal absolute (maximal effort) workloads were used. As such, the IHT stimulus in this study, whereby the relative training intensity was essentially “clamped,” meaning that IHT participants underwent lower absolute workloads than CONT participants, may simply not have been sufficiently intense to stress O2 delivery. So the lack of observed T-Lim gains in this study, and similarly by others that used moderate to heavy intensity training (17,25,26,30), is perhaps not all that surprising. In the case of the moderate intensity, IHT study by Dufour et al. (5), again, we suggest that the performance gains were at least in part because of placebo and nocebo effects. Moreover, these authors did not report any between group statistical analyses, meaning that the effects within the IHT and CONT group were not shown to be different. In agreement with this study, Ventura et al. (32) also reported no significant performance improvements after 6 weeks’ IHT in moderately trained cyclists. However, their IHT sessions were in addition to participants’ habitual training, and these authors suggested that the lack of performance change could have been a result of over-training (32). Reductions in submaximal HR, peak [Bla], and maximal exercise capacity are commonly observed during overtraining (19), and it is possible that a similar effect occurred in this study. Our experimental design meant that training loads were maintained consistently over the 8 weeks, so participants were not able to take additional rest when feeling fatigued, as they may have done under normal circumstances. It is therefore likely that some participants experienced accumulated fatigue by the end of the intervention, which was confirmed anecdotally by the athletes and their coach, and is evidenced by the lack of T-Lim changes, the high proportion of withdrawals due to illness, and by trends toward a post-IHT reduction in normoxic V_ O2peak and HRmax. It should be acknowledged that the discontinuous combined submaximal and maximal intensity exercise test may not have provided the most sensitive means of assessing maximal exercise capacity. Instead of using T-Lim as the sole surrogate estimate of athletic performance, future similar studies should include a range of exercise capacity tests, including extended submaximal protocols to establish whether any changes in submaximal HR or V_ O2 lead to greater aerobic exercise tolerance, and also using more ecologically valid assessments of maximal performance capacity.
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In conclusion, 8 weeks of IHT resulted in significantly lower submaximal HR and a tendency for a reduced oxygen cost of submaximal exercise. Although incremental running time to exhaustion improved in hypoxic conditions, changes in normoxic test conditions were not apparent.
PRACTICAL APPLICATIONS The results of this study do not support the use of moderate intensity IHT to enhance athletic performance at sea level. One potential use for such an IHT intervention is during pre-acclimatization for subsequent training in hypoxia, although this concept requires more direct assessment, with performance being quantified using more ecologically valid methods (e.g., competitive races). It is recommended that those professionals who supervise IHT interventions closely monitor individual athlete fatigue and well-being, and that research is carried out into the fatigue consequent to IHT in more depth, especially if equal absolute workloads are used for IHT as they would be for normoxic training. Recent literature suggests that IHT using severe or supramaximal intensity exercise may provide an additional benefit on athletic performance than normoxic training, at least for repeated sprint type activities, but these claims must be further substantiated. In particular, future research should comprise rigorously designed double-blinded assessments of the effects of whole body severe or supramaximal intensity IHT in highly trained athletes, as there is a scarcity of data in this population.
ACKNOWLEDGMENTS The academic tuition fees related to this research were in part funded by British Swimming (www.swimming.org), the English Institute of Sport (www.eis2win.co.uk), and Sporting Edge UK Ltd (www.sportingedgeuk.co.uk).
REFERENCES 1. Bakkman, L, Sahlin, K, Holmberg, HC, and Tonkonogi, M. Quantitative and qualitative adaptation of human skeletal muscle mitochondria to hypoxic compared with normoxic training at the same relative work rate. Acta Physiol (Oxf ) 190: 243–251, 2007. 2. Beaver, WL, Wasserman, K, and Whipp, BJ. A new method for detecting anaerobic threshold by gas exchange. J Appl Physiol (1985) 60: 2020–2027, 1986. 3. Borg, G. The borg RPE scale. In: Borg’s Perceived Exertion and Pain Scales. G. Borg, ed. Champaign, IL: Human Kinetics, 1998. pp. 29–38. 4. Calbet, JA, Radegran, G, Boushel, R, and Saltin, B. On the mechanisms that limit oxygen uptake during exercise in acute and chronic hypoxia: Role of muscle mass. J Physiol 587: 477–490, 2009. 5. Dufour, SP, Ponsot, E, Zoll, J, Doutreleau, S, Lonsdorfer-Wolf, E, Geny, B, Lampert, E, Fluck, M, Hoppeler, H, Billat, V, Mettauer, B, Richard, R, and Lonsdorfer, J. Exercise training in normobaric hypoxia in endurance runners. I. Improvement in aerobic performance capacity. J Appl Physiol (1985) 100: 1238–1248, 2006.
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Journal of Strength and Conditioning Research
Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
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Journal of Strength and Conditioning Research 6. Faiss, R, Leger, B, Vesin, JM, Fournier, PE, Eggel, Y, Deriaz, O, and Millet, GP. Significant molecular and systemic adaptations after repeated sprint training in hypoxia. PLoS One 8: e56522, 2013. 7. Faulhaber, M, Gatterer, H, Haider, T, Patterson, C, and Burtscher, M. Intermittent hypoxia does not affect endurance performance at moderate altitude in well-trained athletes. J Sports Sci 28: 513–519, 2010. 8. Geiser, J, Vogt, M, Billeter, R, Zuleger, C, Belforti, F, and Hoppeler, H. Training high–living low: Changes of aerobic performance and muscle structure with training at simulated altitude. Int J Sports Med 22: 579–585, 2001. 9. Gore, CJ and Hopkins, WG. Counterpoint: Positive effects of intermittent hypoxia (live high:train low) on exercise performance are not mediated primarily by augmented red cell volume. J Appl Physiol (1985) 99: 2055–2057, 2005. 10. Heinonen, IH, Kemppainen, J, Kaskinoro, K, Peltonen, JE, Borra, R, Lindroos, M, Oikonen, V, Nuutila, P, Knuuti, J, Boushel, R, and Kalliokoski, KK. Regulation of human skeletal muscle perfusion and its heterogeneity during exercise in moderate hypoxia. Am J Physiol Regul Integr Comp Physiol 299: R72–R79, 2010. 11. Holliss, BA, Fulford, J, Vanhatalo, A, Pedlar, CR, and Jones, AM. Influence of intermittent hypoxic training on muscle energetics and exercise tolerance. J Appl Physiol (1985) 114: 611–619, 2013. 12. Holliss, BA, Pedlar, C, Glaister, M, and Jones, A. Validity of the Ja¨eger Oxycon-ProÒ expired air analyzer in normobaric hypoxia. Presented at 16th Annual Congress of the European College of Sport Science, Liverpool, United Kingdom, 6–9 July, 2011. 13. Jones, AM. The physiology of the world record holder for the women’s marathon. Int J Sports Sci Coach 1: 101–115, 2006.
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20. Melissa, L, MacDougall, JD, Tarnopolsky, MA, Cipriano, N, and Green, HJ. Skeletal muscle adaptations to training under normobaric hypoxic versus normoxic conditions. Med Sci Sports Exerc 29: 238–243, 1997. 21. Millet, GP, Roels, B, Schmitt, L, Woorons, X, and Richalet, JP. Combining hypoxic methods for peak performance. Sports Med 40: 1–25, 2010. 22. Newell, J, Higgins, D, Madden, N, Cruickshank, J, Einbeck, J, McMillan, K, and McDonald, R. Software for calculating blood lactate endurance markers. J Sports Sci 25: 1403–1409, 2007. 23. Ponsot, E, Dufour, SP, Zoll, J, Doutrelau, S, N’Guessan, B, Geny, B, Hoppeler, H, Lampert, E, Mettauer, B, Ventura-Clapier, R, and Richard, R. Exercise training in normobaric hypoxia in endurance runners. II. Improvement of mitochondrial properties in skeletal muscle. J Appl Physiol (1985) 100: 1249–1257, 2006. 24. Rasmussen, P, Siebenmann, C, Diaz, V, and Lundby, C. Red cell volume expansion at altitude: A meta-analysis and Monte Carlo simulation. Med Sci Sports Exerc 45: 1767–1772, 2013. 25. Robertson, EY, Saunders, PU, Pyne, DB, Gore, CJ, and Anson, JM. Effectiveness of intermittent training in hypoxia combined with live high/train low. Eur J Appl Physiol 110: 379–387, 2010. 26. Roels, B, Millet, GP, Marcoux, CJ, Coste, O, Bentley, DJ, and Candau, RB. Effects of hypoxic interval training on cycling performance. Med Sci Sports Exerc 37: 138–146, 2005. 27. Semenza, GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551–578, 1999.
14. Jones, AM and Doust, JH. A 1% treadmill grade most accurately reflects the energetic cost of outdoor running. J Sports Sci 14: 321–327, 1996.
28. Smith, CG and Jones, AM. The relationship between critical velocity, maximal lactate steady-state velocity and lactate turnpoint velocity in runners. Eur J Appl Physiol 85: 19–26, 2001.
15. Kallio, PJ, Wilson, WJ, O’Brien, S, Makino, Y, and Poellinger, L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem 274: 6519–6525, 1999.
29. Terrados, N, Jansson, E, Sylven, C, and Kaijser, L. Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol (1985) 68: 2369–2372, 1990.
16. Laursen, PB, Francis, GT, Abbiss, CR, Newton, MJ, and Nosaka, K. Reliability of time-to-exhaustion versus time-trial running tests in runners. Med Sci Sports Exerc 39: 1374–1379, 2007.
30. Terrados, N, Melichna, J, Sylven, C, Jansson, E, and Kaijser, L. Effects of training at simulated altitude on performance and muscle metabolic capacity in competitive road cyclists. Eur J Appl Physiol Occup Physiol 57: 203–209, 1988.
17. Lecoultre, V, Boss, A, Tappy, L, Borrani, F, Tran, C, Schneiter, P, and Schutz, Y. Training in hypoxia fails to further enhance endurance performance and lactate clearance in well-trained men and impairs glucose metabolism during prolonged exercise. Exp Physiol 95: 315– 330, 2010. 18. Levine, BD and Stray-Gundersen, J. Point: Positive effects of intermittent hypoxia (live high:train low) on exercise performance are mediated primarily by augmented red cell volume. J Appl Physiol (1985) 99: 2053–2055, 2005. 19. Meeusen, R, Nederhof, E, Buyse, L, Roelands, B, de Schutter, G, and Piacentini, MF. Diagnosing overtraining in athletes using the twobout exercise protocol. Br J Sports Med 44: 642–648, 2010.
31. Vallier, JM, Chateau, P, and Guezennec, CY. Effects of physical training in a hypobaric chamber on the physical performance of competitive triathletes. Eur J Appl Physiol Occup Physiol 73: 471–478, 1996. 32. Ventura, N, Hoppeler, H, Seiler, R, Binggeli, A, Mullis, P, and Vogt, M. The response of trained athletes to six weeks of endurance training in hypoxia or normoxia. Int J Sports Med 24: 166–172, 2003. 33. Vogt, M, Puntschart, A, Geiser, J, Zuleger, C, Billeter, R, and Hoppeler, H. Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J Appl Physiol (1985) 91: 173–182, 2001.
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