Secondary Logo

Journal Logo

Effects of Five-Week Resistance Training in Hypoxia on Hormones and Muscle Strength

Yan, Bing; Lai, Xiangxun; Yi, Longyan; Wang, Yang; Hu, Yang

Journal of Strength and Conditioning Research: January 2016 - Volume 30 - Issue 1 - p 184–193
doi: 10.1519/JSC.0000000000001056
Original Research
Free

Yan, B, Lai, X, Yi, L, Wang, Y, and Hu, Y. Effects of five-week resistance training in hypoxia on hormones and muscle strength. J Strength Cond Res 30(1): 184–193, 2016—The effects of different levels of systemic hypoxia on hormonal responses, strength, and body composition to 5-week resistance training were investigated. Twenty-five male subjects were randomly assigned into 3 experimental groups that performed 10 sessions (2 sessions per week) of barbell back squat (10 repetitions, 5 sets, 70% 1 repetition maximum [RM]) under normoxia (NR, FiO2 = 21%) and hypoxia (HL, FiO2 = 16%; HH, FiO2 = 12.6%). Serum growth hormone (GH), testosterone (T), and cortisol (C) concentrations were measured before (Pre) and at 0 (T-0), 15 (T-15), 30 (T-30) minutes after exercise in the first and last training sessions. One repetition maximum, isometric knee extension, isometric leg press (LP), and body composition were evaluated before and after the protocol. In the first session, GH of HH (p < 0.01) and HL (p < 0.01) was higher than NR at T-0. In the last session, only GH of HH was higher than NR at T-0 (p ≤ 0.05); meanwhile, T/C ratio of HH was higher than NR at Pre (p < 0.01), T-0 (p < 0.01), and T-15 (p ≤ 0.05). Following the training protocol, HH showed greater (p ≤ 0.05) improvement of isometric LP strength compared with NR; lean body mass was increased in the hypoxia groups only. Moderate-intensity resistance training performed in severe hypoxia (FiO2 = 12.6%) induced greater GH responses and isometric strength gains in LP than that in NR. FiO2 of 12.6% was recommended when performing the moderate-intensity resistance training under systemic hypoxia.

Sport Science Research Center, Beijing Sport University, Beijing, China

Address correspondence to Xiangxun Lai, laibsu@163.com.

Back to Top | Article Outline

Introduction

General strength is one of the fundamental characters, which determines the sports performance and fitness. Over decades, resistance training has been intensively investigated and demonstrated the positive effects on muscular strength, power, and hypertrophy (32,40). However, developing the more effective and efficient method to maximize the strength and muscle mass gain is always the focus of coaches and scientists.

Resistance exercise elicits a milieu of acute and chronic hormonal responses critical to muscular force and power production as well as subsequent tissue growth and remodeling (20). Growth hormone (GH) and T are acutely secreted in response to resistance training and play key roles in the muscular adaptation, such as hypertrophy and strength gains. It was reported that moderate-intensity resistance training elevated the GH and T significantly (18). McCall et al. (26) showed that resistance exercise–induced GH secretion was correlated with the magnitude of muscle hypertrophy. It has been proposed that the hypothalamus-pituitary hormone (GH) secretions are stimulated by the accumulation of metabolic subproducts, such as lactate or H+, during exercises (9). Metabolic stress from performing the resistance exercise might play a key role in muscular adaptations (37). However, some studies have failed to prove any correlation between these parameters (34,38). It is important to monitor the anabolic hormones and lactate responses to understand the morphologic and physiological adaptations of muscle to resistance training (36).

In recent years, some Japanese researchers started to determine the effects of occlusion on maximizing the resistance training effects. Resistance exercise with blood flow restriction (BFR, also known as Kaatsu training) was adopted as a novel training modality to promote muscle strength and hypertrophy (2). Many studies demonstrated substantial muscle hypertrophy and strength gains effects after weeks of BFR at intensities as low as 20% of maximal effort (1). Although the exact physiological mechanisms underpin the training effects of BFR was not completely clarified, local hypoxia environment and ischemia had been identified as an important factor that enhances both acute responses (30) and chronic adaptations (1,32) to resistance exercise.

Given that the localized hypoxia induced by BFR acts as the potential contributor to the augmented effects of resistance training, it is plausible to speculate similar augmented training effects from resistance exercise in systemic hypoxic environment, termed resistance training in hypoxia (RTH) (27). Manimmanakorn et al. (24) showed that both the BFR and RTH substantially improved muscular strength relative to traditional resistance training. Some studies have reported the hormonal changes to RTH. Kon et al. showed greater increased GH after low- (19) and moderate-intensity (18) (50 and 70% of 1 repetition maximum [RM]) resistance exercises in acute systemic hypoxia (FiO2 = 13%). At the same time, serum testosterone was elevated significantly after resistance exercises in both hypoxia and normoxia (NR) without statistical differences between conditions (18). However, Ho et al. (12) reported that low-intensity (30% of 1RM) resistance training under moderate systemic hypoxia (FiO2 = 15%) did not induce greater anabolic hormonal responses in untrained male compared with the same training in NR. The inconsistent results of these studies implied that the levels of hypoxia might be related to the anabolic hormonal responses.

In addition, these studies only observed the acute hormonal responses after 1 bout resistance exercise in hypoxia. The chronic effects of training in hypoxia on hormonal responses remain unknown. If the anabolic hormone responses induced by RTH persist for long term, it would be a more effective protocol to promote hypertrophy and strength.

It is also equivocal about the muscular morphological and strength changes after RTH. In a recent study, Kon et al. (20) showed no additional muscle strength and cross-sectional area (CSA) gains after 8-week RTH (FiO2 = 0.144) compared with NR control. Meanwhile, Ho et al. (13) did not find additive effect of hypoxia (FiO2 = 0.15) on muscular strength and lean body mass (LBM) after 6-week moderate-intensity resistance training. In contrast, Nishimura et al. (30) showed greater increases in the CSA of elbow muscles after 6 weeks of 70% 1RM resistance exercises in hypoxia (FiO2 = 0.16) than the NR control. Kurobe et al. (23) reported that 8-week RTH (FiO2 = 0.127) induced greater muscle thickness in elbow extensors than the NR training. The hypoxia level would possibly affect the metabolic stress induced by RTH that turns into the morphologic and strength adaptations.

Therefore, this study investigated the effects of different levels of systemic hypoxia on hormonal responses, strength, and body composition to a 5-week moderate intensity resistance training protocol. We hypothesized that (a) RTH would cause greater acute anabolic hormone and lactate responses compared with the same exercise in NR both in the first and the last training sessions of the protocol; (b) RTH under severe hypoxia (FiO2 = 12.6%) would induce greater gains in both muscle strength and LBM compared with the NR control and RTH under mild hypoxia (FiO2 = 16%).

Back to Top | Article Outline

Methods

Experimental Approach to the Problem

All the subjects were randomly assigned into HH (n = 8), HL (n = 9), and NR groups (n = 8) who finished the same resistance training protocol under FiO2 of 12.6, 16, and 21%, respectively, in a single-blinded manner. The protocol consisted twice per week for a total of 10 training sessions. In each session, the subjects performed 5 sets of 10 repetitions barbell back squat at 70% 1RM with 1-minute interval between sets. To determine the effects of different levels of hypoxia on hormonal and lactate responses induced by RTH, blood samples were drawn during the first and the last training sessions for hormonal and lactate analyses. Muscle strength and body composition tests were performed before and after the whole training protocol to compare the effects of RTH in different levels of hypoxia on muscular performance and body composition.

Back to Top | Article Outline

Subjects

Twenty-five healthy male university students (age: 22.2 ± 2.6 years; age range: 19–26 years; height: 176.3 ± 5.0 cm; weight: 70.5 ± 10.0 kg) volunteered in this study. All the subjects were sea-level residents and had not exposed to altitude or hypoxia environment of more than 1,500 m within the 6 months before participation. All the subjects were physically active and had recreational exercise training experiences. However, none of them involved in regular strength training program within 1 year before participation. Written informed consents were obtained from all the subjects after detailed explanation of the study purpose and procedures. The study was approved by Beijing Sport University Review Board for Human Subjects.

Back to Top | Article Outline

Procedures

Systemic Hypoxic Environment

All the training sessions were performed in an instrumented hypoxia training room in the Hypoxia Training Center of Beijing Sport University. The room was ventilated by the centralized oxygen filtration system (L.O.S. LOWOXYGEN SYSTEMS GmbH, Berlin, Germany). The system circulated the whole air of the room 6 times per hour and ventilated the hypoxic air into the room. The environmental control system monitored the oxygen and CO2 concentrations continuously and adjusted the ratio of N2 (99%, produced by the system) and fresh air supplied to keep the FiO2 of the room at a stable preset value. The FiO2 for the HH and HL groups was set at 12.6 and 16%, respectively. To blind subjects to altitude, the system also ran for the NR group with normoxic airflow ventilating into the room. The system was started 4 hours before each training session to create a stable and accurate hypoxic environment.

Back to Top | Article Outline

Blood Sampling and Analyses

In both the first and the last training sessions, multiple blood samples were obtained from an antecubital vein by an intravenous catheter. The catheter was inserted before the subjects entered the training environment. The blood samples were obtained at Pre (after 15-minute rest in NR or hypoxia), and at T-0, T-15, and T-30 (immediately after, 15 and 30 minutes after exercise, respectively). The subjects stayed in the training environment until the last blood sample obtained. Serum was separated by centrifugation (5,000 rpm for 5 minutes) for the hormone analysis. Commercial test kits for GH (Access Ultrasensitive hGH assay; Beckman Coulter, Inc., Brea, CA, USA), testosterone (Access Testosterone; Beckman Coulter, Inc., Brea, CA, USA), and cortisol (Access Cortisol; Beckman Coulter, Inc., Brea, CA, USA) concentration measurement were performed on an automatic immunoassay system (Unicel DXI800; Beckman Coulter, Inc.). Quality control and calibration were carried out daily and before the tests as per the manufacturer's instruction. Lactate concentration was measured by an automatic lactate analyzer (Biosen C-line; EKF diagnostic GmbH, Barleben, Germany). Arterial oxygen saturation (SpO2) was recorded at the same time points with blood sampling using a pulse oximetry (WristOx2 3150; Nonin Medical, Inc., Minneapolis, MN, USA).

Back to Top | Article Outline

Muscle Strength Tests

All subjects were instructed to avoid alcohol, caffeine, and high-intensity exercises within 48 hours before the tests. The muscle strength tests were performed before and after the training protocol. Before the first tests, all subjects participated 2 familiarization sessions in 1 week in which the proper techniques to perform the barbell back squat and the strength tests were introduced. A week later, subjects visited the laboratory to perform the strength tests in NR condition. During the 1RM test, all the subjects finished a warm-up session at the intensity of estimated 50 and 85% 1RM for 5–10 repetitions. Then, the load was increased within 4–5 trials separated at least 3 minutes until the 1RM obtained. The subjects were instructed to descend to reach a 90° knee angle and ascend to fully extension in a controlled manner. Bilateral isometric knee extension (KE) was measured by an instrumented KE machine (F200; DAVID GmbH, Neu-Ulm, Germany) with a digital analyzing module (MC-M; DAVID GmbH, Neu-Ulm, Germany) that was able to record the peak torque during the isometric muscle contraction. The lever arms were fixed at 5 cm above the medial malleolus of both legs with a static knee angle of 120°. The rotation axis of the lever arm was aligned to the lateral femoral epicondyle. Subjects performed 3 repetitions of 3-second maximal voluntary isometric KE with a 2-minute interval between repetitions (24). After 30 minutes of rest, isometric leg press (LP) was measured by the LP module of an isokinetic system (IsoMed 2000; D&R Ferstl GmbH, Hemau, Germany). Subjects were seated in a rigid chair of the system and fixed by the strap across the shoulders, chest, and hip. Footplate was adjusted to form a knee angle of 120°. Then, the subjects performed 2 repetitions of 6-second maximal voluntary isometric LP with 2-minute interval (15). The maximal torque during the tests was used in the statistical analyses.

Back to Top | Article Outline
Resistance Training Protocol

The protocol consisted twice per week for a total of 10 training sessions. In each session, the subjects entered the training room and seated for 15 minutes to adapt the training environment. Then, after the warm-up set consisting of 10 repetitions barbell back squat at 30% 1RM, each subject performed 5 sets of 10 repetitions barbell back squat at 70% 1RM with 1-minute interval between sets. The subjects were assisted if fatigue happened during the last few repetitions. All sets should be performed to exhaustion. Training load was increased if the subjects finished all repetitions in the last set of each session in 2 consecutive sessions without assistance. To control the diurnal variations of hormone secretion, the subjects performed all the training sessions at the same time window of the day from 4:00 PM to 6:00 PM in a random order. The subjects were fasted for at least 4 hours before each training session. Besides the exercises prescribed by the study protocol, participants were instructed to continue their normal dietary, refrain from alcohol and any intense exercises during the entire participation.

Back to Top | Article Outline

Body Composition Test

After an overnight fast, LBM and percentage of body fat were measured by a dual-energy x-ray absorptiometry (Norland XR-46; Cooper Surgical, Inc., Trumbull, CT, USA) before and after the training protocol.

Back to Top | Article Outline

Statistical Analyses

All data except for the values of GH were analyzed by multifactor analysis of variance with repeated measures. If significant differences existed, a post hoc analysis test (LSD) was performed. The values of GH during the first and last training sessions were compared using Mann-Whitney U-test to examine the intergroup differences at the same time point and Wilcoxon signed rank test to examine the intragroup differences among time points. The arithmetic means of hormonal and lactate values at T-0, T-15, and T-30 were calculated to represent the postexercise values (PM) (17,18). Statistical significance was set at p ≤ 0.05. Data were expressed as mean ± SE.

Back to Top | Article Outline

Results

No significant differences existed among groups (HH, HL, and NR) on the baseline of age, height, weight, muscle strength, body fat, and LBM.

SpO2 data were shown in Table 1. At all time points during the first and the last training sessions, the SpO2 values of HH were lower than that of HL (p < 0.01) and NR (p < 0.01), meanwhile, HL was lower than NR (p < 0.01). SpO2 of the HH group at T-0 was lower (p ≤ 0.05) than the Pre value in both the first and the last training sessions.

Table 1

Table 1

Figure 1A showed variations of GH during the first and last training sessions. During the first training session, the GH concentrations of HH (1.2 ± 1.3 ng·ml−1, p ≤ 0.05) and HL (2.1 ± 1.9 ng·ml−1, p ≤ 0.05) were significantly elevated after 15-minute rest in hypoxia compared with NR (0.06 ± 0.88 ng·ml−1). The significant intergroup differences were observed at T-0, which exhibited greater elevation of GH in hypoxia training groups (HH: 10.9 ± 10.7 ng·ml−1, p < 0.01; HL: 9.3 ± 7.1 ng·ml−1, p < 0.01) than in the NR (1.1 ± 5.4 ng·ml−1) group. The PM of GH concentrations of HH, HL, and NR was significantly increased compared with Pre values.

Figure 1

Figure 1

The acute elevation of GH in hypoxia training groups at Pre during the first training session was not observed in the last training session. During the last training session, the PM of GH in HH and NR groups increased significantly compared with Pre values in contrast to no statistical changes in the HL group. The only significant intergroup difference was observed at T-0 between the HH (6.9 ± 7.2 ng·ml−1, p ≤ 0.05) and NR (1.1 ± 2.2 ng·ml−1) in the last training session.

The PM of GH concentration in all groups decreased significantly in the last training session compared with the values in the first training session (Figure 1B).

Figure 1C showed the T/C ratio changes. Neither inter- or intragroup differences of T/C ratio were observed in the first training session at all time points. During the last training session, the T/C value of HH was significantly higher than that in NR at Pre (p < 0.01), T-0 (p < 0.01), and T-15 (p ≤ 0.05), and higher than that in HL (p < 0.01) at Pre. T/C elevation was also observed at T-0 (p ≤ 0.05) in the HL group compared with Pre value.

The testosterone data were shown in Table 1. Immediately after the resistance exercise during the first training session, the testosterone concentrations were increased in all the groups compared with Pre values. However, the elevation was only observed at T-0 in the HL group during the last training session. The PM of testosterone was increased (from 3.58 ± 0.78 ng·ml−1 to 4.5 ± 0.95 ng·ml−1, p ≤ 0.05) only in the NR group following the 5-week training protocol.

The cortisol data were shown in Table 1. During the first training session, cortisol was only increased in the HL group (7.8 ± 2.9 μg·dL−1 vs. 9.0 ± 3.8 μg·dl−1, p ≤ 0.05) at T-0 compared with Pre value. However, no significant intergroup differences were identified at all time points. During the last training session, the cortisol concentrations of HH (6.8 ± 3.1 μg·dl−1, p < 0.01) and HL (9.7 ± 2.7 μg·dl−1, p ≤ 0.05) at Pre were significantly lower than the NR (12.5 ± 3.0 μg·dl−1) group. In the last training session, cortisol concentration of HH (5.8 ± 1.9 μg·dl−1) was significantly lower than the NR (10.4 ± 2.7 μg·dl−1, p < 0.01) and HL (8.7 ± 2.6 μg·dl−1, p ≤ 0.05) groups at T-0 and lower than the NR (HH: 8.8 ± 4.7 μg·dl−1 vs. NR: 13.2 ± 3.6 μg·dl−1, p ≤ 0.05) group at T-15. Meanwhile, the PM of cortisol concentrations in HH (7.9 ± 2.7 μg·dl−1, p ≤ 0.05) was also significant lower than the mean in the NR (11.3 ± 2.4 μg·dl−1) group. Statistical decrease of the PM of cortisol concentrations (first: 11.1 ± 2.4 μg·dl−1 vs. last: 7.9 ± 2.7 μg·dl−1, p ≤ 0.05) was observed during the last training session compared with the first session.

Compared with the pre values, the PM of lactate concentrations was significantly elevated in all the groups in both the first and the last training sessions. However, no intergroup differences were observed in both sessions. In the first and the last training sessions, the values of lactate concentrations were significantly elevated in all the groups compared with the respective Pre values. However, no intergroup differences were observed in both sessions. The PM value of the HL group in the last training session was significant higher than the value in the first session (p < 0.01).

Figure 2 showed the changes of muscle strength before and after the training protocol. One RM (Figure 2A; HH: from 113.8 ± 18.5 kg to 147.5 ± 24.7 kg, p < 0.01; HL: from 107.8 ± 21.0 kg to 143.6 ± 22.2 kg, p < 0.01; NR: from 110.6 ± 20.4 kg to 142.5 ± 17.0 kg, p < 0.01) and isometric KE (Figure 2B; HH: from 577.5 ± 170.7 to 656.8 N·m ± 174.4 N·m, p < 0.01; HL: from 536.0 ± 100.4 N·m to 632.3 ± 95.4 N·m, p < 0.01; NR: from 510.9 ± 130.4 N·m to 553.4 ± 119.4 N·m, p ≤ 0.05) were improved significantly following the training protocol in all groups; however, no significant difference existed among groups. Isometric LP was increased only in the HH (Figure 2C; from 4,707.4 ± 1,541.9 N·m to 6,292.0 ± 1,378.4 N·m, p < 0.01) and HL (from 4,717.9 ± 1,403.0 N·m to 6,047.5 ± 1,164.9 N·m, p < 0.01) groups following the training protocol. The percentage change of isometric LP in the HH group was significantly higher than the change in the NR group (Figure 2D; HH: 39.4 ± 29.8% vs. NR: 8.14 ± 28.5%, p ≤ 0.05).

Figure 2

Figure 2

Figure 3A showed the LBM change before and after the training protocol. The LBM was increased significantly in both the HH (from 59.5 ± 7.3 kg to 61.0 ± 7.7 kg, p ≤ 0.05) and HL (from 57.6 ± 6.5 kg to 59.3 ± 6.6 kg, p < 0.01) groups after the training protocol. There was no significantly change of LBM in the NR (from 57.9 ± 5.0 kg to 58.8 ± 4.7 kg, p > 0.05) group. The percentage of body fat (Figure 3B) was decreased (HH: from 12.0 ± 3.42% to 10.1 ± 3.14%, p < 0.01; HL: from 12.7 ± 5.6% to 10.6 ± 5.8%, p < 0.01; NR: from 9.5 ± 5.7% to 8.25 ± 5.8%, p < 0.01) in all the 3 groups following the whole training protocol.

Figure 3

Figure 3

Back to Top | Article Outline

Discussion

In this study, we demonstrated that the resistance exercise in hypoxia (HH and HL groups) induced greater acute elevation of GH compared with that in NR and the elevation could be repeated in the HH group during the last training session of a 5-week RTH program. In addition, RTH in severe hypoxia (FiO2 = 12.6%) induced greater isometric strength gains in LP than that in NR. Both hypoxia groups showed improved body composition after training. To our knowledge, it was the first study to compare the effects of chronic resistance training under different levels of hypoxia on the acute exercise-induced hormonal responses, strength, and body composition.

During RTH, the SpO2 of HH and HL groups significantly decreased (mean values of HH and HL after 15 minutes hypoxia exposure: 86.8 ± 1.8% and 93.9 ± 1.9%) and remained lower than baseline values throughout the training. Meanwhile, the SpO2 of HH remained lower than HL at all time points. In contrast, during NR training, SpO2 remained unchanged (within the range from 96.5 ± 1.6% to 98.5 ± 0.5%) and higher than hypoxia training groups throughout the training (Table 1). Previous studies reported that SpO2 decreased from baseline values to 94 (30) and 84% (17) after hypoxia inhalation with FiO2 of 16 and 13%, respectively. The SpO2 data of this study ensured that subjects' exposure to hypoxia was correctly controlled for hypoxia training groups.

The immediate decrease of SpO2 after the squat exercise in hypoxia was observed in the HH group, but not in HL and NR groups, in both the first and the last training session. Intense exercise could induce the decrease of SpO2 in both NR and hypoxia (25) due to the muscular oxygen extraction and metabolites accumulation (31). According to the oxygen dissociation curve, the lower PiO2 of the HH group makes it locate on a steeper slope than the HL and NR groups, thus the SpO2 is more sensitive to the decrease of oxygen partial pressure, such as intense exercise, in the HH than in the HL and NR groups. This might account for why the significant SpO2 decrease at T-0 was only observed in HH group in this study.

Acute elevation of GH after resistance exercise was demonstrated in both the RTH and NR groups in the first training session, meanwhile significant greater increase of GH was showed in RTH groups compared with the NR group. The results were supported by the studies that showed elevated GH after low-to-moderate intensity resistance exercises in systemic hypoxia (18,19). However, some recent studies failed to demonstrate the greater GH secretion after RTH compared with the NR control (12,20). Kon et al. reported no elevation of GH in the NR group that was in contrast to the current results. Numerous studies had demonstrated substantial GH increases after various types of resistance exercises (6). The controversy might be due to the individual variability in the GH response to resistance exercise. Raastad et al. (33) reported great individual variability (responders vs. nonresponders) existed in the GH response to the same resistance protocol. These data implied that even within a homogenous population, there might be individual differences in hormonal response (6). Further studies were definitely warranted to clarify the discrepancy of GH response to RTH.

Substantial reduction of GH response to acute resistance exercise was showed following the training protocol in this study. To our knowledge, there was no study that showed the hormonal responses to chronic resistance training program in systemic hypoxia, such as the protocol in this study. Clue could be found in the study investigating the hormonal responses to resistance training in NR. Kraemer et al. (21) reported a reduction in acute GH response to the same resistance exercise after a 10-week strength training program in untrained young males. The reduction of GH response might be due to the neuromuscular adaptation to training stimulus, which decreased the metabolic stress (21), thus reflected in the mitigated GH responses (11). Although the PM of GH in the last training session was significantly lower than the corresponding value in the first training session, the GH of HH but not HL, at T-0 was still higher than the NR group (p ≤ 0.05). The data suggested that the lower oxygen concentration in HH group could repeatedly induced higher GH compared with NR group during a 5-week RTH protocol, which translated into higher isometric strength gains in HH.

Although GH responses were greater in hypoxia groups; however, the blood lactate results did not support the GH response during both the first and the last sessions. Metabolites such as H+ accumulation during exercise are considered major stimulating factors to promote GH secretion in hypoxia (18). However, there were no differences in lactate concentrations among the 3 experimental groups in this study. It is equivocal about the acute LA responses to hypoxic exercise in the literature. Kon et al. reported greater LA responses after hypoxic resistance exercise than the NR control. In contrast, some recent studies failed to demonstrate higher LA levels after hypoxic resistance exercises (12,22). However, GH concentrations increase with severe hypoxic exposure per se (22). Thus, it seems that the hypoxic stress causes the increase of GH independently.

Acute elevation of testosterone was shown immediately after the resistance exercise in the first training session in both the RTH and NR groups without intergroup differences. This was consistent with evidence showing significant testosterone elevation after resistance exercises in both hypoxia (18) and NR (6). Because of no intergroup differences in both the first and last training session, it was postulated that hypoxic stimulus might have no significant impact on testosterone secretion. So, testosterone responses were similar among groups after squat exercise. Cortisol concentration was significantly lower in the HH than the value in the NR group in the last training session. The mechanisms underlining the decreased cortisol response in the HH group after 5-week resistance protocol remained unclear in the literature and exceeded the view of this study. However, the decrease of cortisol concentration during the last training session caused greater increase in T/C ratio. The T/C ratio has been suggested to be indicators of the anabolic/catabolic status of skeletal muscle during resistance training (10). Significant greater increase of T/C in HH group compared with HL and NR groups was observed at the end of the experimental protocol. The results suggested that the HH group was in a potential better anabolic environment at the end of the protocol, which was not observed in the beginning. It was speculated that the preferable anabolic environment in HH group was induced by the accumulation of additional hypoxia stimulus, which might partly contribute to the greater strength gains compared with the NR group in this study.

In this study, we demonstrated greater improvement of isometric LP strength in the HH group compared with the NR group (p ≤ 0.05) following the training protocol. Manimmanakorn et al. (24) reported greater improvement in maximal isometric strength after 5-week RTH (SpO2 was controlled at 80%) program compared with an NR control group. Nishimura et al. (30) observed significant increase of 1RM strength after 3-week RTH (FiO2 = 16%), whereas a significant improvement of strength in the NR training group took 6 weeks. However, discrepancy existed in the literature concerning about the effects of RTH on muscular strength adaptation. In a recent study, Ho et al. (13) failed to observe the additional elevation in isometric or isokinetic strength after 6 weeks RTH (FiO2 = 15%) compared with the NR control. Friedmann et al. (8) reported no significant increase in maximal strength and muscle hypertrophy after low-intensity RTH for 4 weeks (FiO2 = 12%). The controversy might be due to the differences in training program design and/or hypoxia levels used.

The improved isometric LP strength was only identified in hypoxia training groups, whereas no change in the NR group. The mechanisms might involve the effects of hypoxia on muscle activity. Evidence showed that breathing hypoxic gas increased the recruitment of type II fibers during cycle ergometer exercise (28). Similar recruitment pattern was also reported during BFR resistance exercises (39). In this study, it is plausible to speculate that the hypoxic environment of working muscles induced by RTH would possibly facilitate the fatigue of oxygen sensitive type I fibers and the recruitment of type II fibers (29). During sprint in hypoxia, the nitric oxide-/nitric oxide synthase-mediated vasodilation causes the blood perfusion in the exercise muscle (7) that might benefit the type II fibers to make it exhibit more endurance. It is plausible to speculate that the same mechanisms also be functional during RTH. The fomented mechanisms during RTH would possibly increase the stress on type II motor units and induce the adaptation in the form of selective hypertrophy in these motor units (14). The type II motor units contract much faster and produce much higher force than the type I units (16), which explains the elevated isometric LP strength in HH and HL groups. However, no significant difference was showed in the percent increase of isometric KE strength between 2 RTH groups and NR group. The discrepancy of LP and KE results may be due to the differences in movement patterns. The LP is a multijoint movement that is similar in the movement pattern to the squat exercise used in the training sessions, thus was prone to be more sensitive to show the training effects (3). Significant elevation of 1RM was observed in all groups following the training protocol without intergroup differences in magnitude of improvement. It was in agreement with studies showed 1RM improvement after both RTH and normoxic resistance training (13). The results of 1RM and LP were not consistent in this study. The beneficial training effects of RTH were not shown in 1RM. Barbell squat is a complex dynamic movement. The 1RM is determined by the weakest muscular strength output through the full range of motion. In contrast, the isometric LP strength is measured under the optimal joint angle. Thus, the discrepancy between the 1RM and LP might be due to the differences in muscular contraction patterns (dynamic vs. static) and the limiting factors to the maximal strength output of 1RM and LP.

The different GH responses between HH and HL groups suggested that the hypoxia levels played a role in the acute response and chronic adaptation to RTH, although the exact mechanisms were not clear. Ho et al. (13) reported that the RTH group (FiO2 = 0.15) produced no difference in isometric or isokinetic strength elevation compared with the NR control group after a total of 18 sessions of 3 sets of back squat at 10RM with 2 minutes of rest between sets. The results were in agreement with the strength changes in HL group who used the similar training protocol and hypoxia level in this study. In contrast, the HH group who performed the resistance exercises in lower oxygen level (FiO2 = 0.126) produced substantial larger improvement in LP strength compared with NR. It suggested that the levels of hypoxia might play a role in the strength adaptation to long-term RTH.

Lean body mass was significantly increased in the HH and HL groups following the training protocol, whereas no statistical elevation in the NR group. Although the direct measure of muscle mass, such as muscle CSA, was not used in this study, it was believed that the increase of LBM was due to increase of muscle CSA. Nishimura et al. (30) reported that significant increase of muscle CSA was only observed in the RTH group who finished 6 weeks of bilateral elbow resistance exercises at the intensity of 70% 1RM. Manimmanakorn et al. (24) also showed substantially greater increase in muscle CSA after RTH and BFR than RT. These observations implied that the hypoxia played a role in the muscle hypertrophic adaptation to resistance training. Greater elevation of GH was observed in the RTH groups in this study than in the NR group. Growth hormone is an important anabolic hormone in the muscle adaptation process to resistance training (35). Mediated by the IGF-1, GH could facilitate the muscle protein synthesis (MPS) by activating intramuscular signaling pathways (5), such as the mammalian target of rapamycin pathway that was able to enhance the MPS and critical to the subsequent muscle hypertrophy (4). The studies about the IGF-1 changes after RTH were scarce and equivocal in the literature, thus the role of GH in the muscle strength and size adaptation to RTH was largely unknown.

In conclusion, moderate-intensity resistance training performed in severe hypoxia (FiO2 = 12.6%) induced greater GH responses and isometric strength gains in LP than that in NR. FiO2 of 12.6% was recommended when performing the moderate-intensity resistance training under systemic hypoxia.

Back to Top | Article Outline

Practical Applications

General strength is critical to performance and fitness. Developing the more effective and efficient method to improve muscular strength is the ultimate endeavor of strength professionals and practitioners. Recent studies showed that RTH was a promising way to better improve strength and induce hypertrophy. Based on the results of this study, we recommended performing the moderate-intensity (70% 1RM) resistance training under the FiO2 of 12.6% to induce anabolic hormone responses and strength gains.

Back to Top | Article Outline

Acknowledgments

The authors appreciate the participation and contribution of the subjects. Thanks to Prof. Dr. Liwei Zhang and Ms. Jiaojiao Yu for the help in statistical methodology. This study was supported by Beijing Sport University Research Funding (Grant No. 2014SYS007) and National Natural Science Foundation of China (Grant No. 31470059). The authors have no conflict of interest to disclose. Furthermore, the results of this study do not constitute endorsement by the authors or the National Strength and Conditioning Association.

Back to Top | Article Outline

References

1. Abe T, Kearns CF, Sato Y. Muscle size and strength are increased following walk training with restricted venous blood flow from the leg muscle, Kaatsu-walk training. J Appl Physiol (1985) 100: 1460–1466, 2006.
2. Abe T, Loenneke JP, Fahs CA, Rossow LM, Thiebaud RS, Bemben MG. Exercise intensity and muscle hypertrophy in blood flow-restricted limbs and non-restricted muscles: A brief review. Clin Physiol Funct Imaging 32: 247–252, 2012.
3. Baldwin TT, Ford JK. Transfer of training: A review and directions for future research. Pers Psychol 41: 63–105, 1988.
4. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014–1019, 2001.
5. Bonaldo P, Sandri M. Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech 6: 25–39, 2013.
6. Crewther B, Keogh J, Cronin J, Cook C. Possible stimuli for strength and power adaptation: Acute hormonal responses. Sports Med 36: 215–238, 2006.
7. Faiss R, Girard O, Millet GP. Advancing hypoxic training in team sports: From intermittent hypoxic training to repeated sprint training in hypoxia. Br J Sports Med 47(suppl 1): i45–50, 2013.
8. Friedmann B, Kinscherf R, Borisch S, Richter G, Bartsch P, Billeter R. Effects of low-resistance/high-repetition strength training in hypoxia on muscle structure and gene expression. Pflugers Arch 446: 742–751, 2003.
9. Gordon SE, Kraemer WJ, Vos NH, Lynch JM, Knuttgen HG. Effect of acid-base balance on the growth hormone response to acute high-intensity cycle exercise. J Appl Physiol (1985) 76: 821–829, 1994.
10. Hakkinen K. Neuromuscular and hormonal adaptations during strength and power training. A review. J Sports Med Phys Fitness 29: 9–26, 1989.
11. Henselmans M, Schoenfeld BJ. The effect of inter-set rest intervals on resistance exercise-induced muscle hypertrophy. Sports Med 44: 1635–1643, 2014.
12. Ho JY, Huang TY, Chien YC, Chen YC, Liu SY. Effects of acute exposure to mild simulated hypoxia on hormonal responses to low-intensity resistance exercise in untrained men. Res Sports Med 22: 240–252, 2014.
13. Ho JY, Kuo TY, Liu KL, Dong XY, Tung K. Combining normobaric hypoxia with short-term resistance training has no additive beneficial effect on muscular performance and body composition. J Strength Cond Res 28: 935–941, 2014.
14. Kawada S, Ishii N. Skeletal muscle hypertrophy after chronic restriction of venous blood flow in rats. Med Sci Sports Exerc 37: 1144–1150, 2005.
15. Kawakami Y, Sale DG, MacDougall JD, Moroz JS. Bilateral deficit in plantar flexion: Relation to knee joint position, muscle activation, and reflex excitability. Eur J Appl Physiol Occup Physiol 77: 212–216, 1998.
16. Kelly AM, Rubinstein NA. Why are fetal muscles slow? Nature 288: 266–269, 1980.
17. Kon M, Ikeda T, Homma T, Akimoto T, Suzuki Y, Kawahara T. Effects of acute hypoxia on metabolic and hormonal responses to resistance exercise. Med Sci Sports Exerc 1, 2009.
18. Kon M, Ikeda T, Homma T, Akimoto T, Suzuki Y, Kawahara T. Effects of acute hypoxia on metabolic and hormonal responses to resistance exercise. Med Sci Sports Exerc 42: 1279–1285, 2010.
19. Kon M, Ikeda T, Homma T, Suzuki Y. Effects of low-intensity resistance exercise under acute systemic hypoxia on hormonal responses. J Strength Cond Res 26: 611–617, 2012.
20. Kon M, Ohiwa N, Honda A, Matsubayashi T, Ikeda T, Akimoto T, Suzuki Y, Hirano Y, Russell AP. Effects of systemic hypoxia on human muscular adaptations to resistance exercise training. Physiol Rep 2, 2014. [Epub Ahead of Print].
21. Kraemer WJ, Hakkinen K, Newton RU, Nindl BC, Volek JS, McCormick M, Gotshalk LA, Gordon SE, Fleck SJ, Campbell WW, Putukian M, Evans WJ. Effects of heavy-resistance training on hormonal response patterns in younger vs. older men. J Appl Physiol (1985) 87: 982–992, 1999.
22. Kurobe K, Huang Z, Nishiwaki M, Yamamoto M, Kanehisa H, Ogita F. Effects of resistance training under hypoxic conditions on muscle hypertrophy and strength. Clin Physiol Funct Imaging, 2014.
23. Kurobe K, Huang Z, Nishiwaki M, Yamamoto M, Kanehisa H, Ogita F. Effects of resistance training under hypoxic conditions on muscle hypertrophy and strength. Clin Physiol Funct Imaging 35: 197–202, 2015.
24. Manimmanakorn A, Hamlin MJ, Ross JJ, Taylor R, Manimmanakorn N. Effects of low-load resistance training combined with blood flow restriction or hypoxia on muscle function and performance in netball athletes. J Sci Med Sport 16: 337–342, 2013.
25. Masschelein E, Vant R, Thomis M, Hespel P. High twin resemblance for sensitivity to hypoxia. Med Sci Sports Exerc 47: 74–81, 2015.
26. McCall GE, Byrnes WC, Fleck SJ, Dickinson A, Kraemer WJ. Acute and chronic hormonal responses to resistance training designed to promote muscle hypertrophy. Can J Appl Physiol 24: 96–107, 1999.
27. McLean BD, Gore CJ, Kemp J. Application of “live low-train high” for enhancing normoxic exercise performance in team sport athletes. Sports Med 44: 1275–1287, 2014.
28. Melissa L, MacDougall JD, Tarnopolsky MA, Cipriano N, Green HJ. Skeletal muscle adaptations to training under normobaric hypoxic versus normoxic conditions. Med Sci Sports Exerc 29: 238–243, 1997.
29. Moritani T, Sherman WM, Shibata M, Matsumoto T, Shinohara M. Oxygen availability and motor unit activity in humans. Eur J Appl Physiol Occup Physiol 64: 552–556, 1992.
30. Nishimura A, Sugita M, Kato K, Fukuda A, Sudo A, Uchida A. Hypoxia increases muscle hypertrophy induced by resistance training. Int J Sports Physiol Perform 5: 497–508, 2010.
31. Oguri K, Du N, Kato Y, Miyamoto K, Masuda T, Shimizu K, Matsuoka T. Effect of moderate altitude on peripheral muscle oxygenation during leg resistance exercise in young males. J Sports Sci Med 3: 182–189, 2004.
32. Phillips SM. Physiologic and molecular bases of muscle hypertrophy and atrophy: Impact of resistance exercise on human skeletal muscle (protein and exercise dose effects). Appl Physiol Nutr Metab 34: 403–410, 2009.
33. Raastad T, Bjoro T, Hallen J. Hormonal responses to high- and moderate-intensity strength exercise. Eur J Appl Physiol 82: 121–128, 2000.
34. Raynaud J, Drouet L, Martineaud JP, Bordachar J, Coudert J, Durand J. Time course of plasma growth hormone during exercise in humans at altitude. J Appl Physiol Respir Environ Exerc Physiol 50: 229–233, 1981.
35. Schoenfeld BJ. The mechanisms of muscle hypertrophy and their application to resistance training. J Strength Cond Res 24: 2857–2872, 2010.
36. Schoenfeld BJ. Potential mechanisms for a role of metabolic stress in hypertrophic adaptations to resistance training. Sports Med 43: 179–194, 2013.
37. Scott BR, Slattery KM, Dascombe BJ. Intermittent hypoxic resistance training: Is metabolic stress the key moderator? Med Hypotheses 84: 145–149, 2015.
38. Sutton JR, Jones NL, Toews CJ. Growth hormone secretion in acid-base alterations at rest and during exercise. Clin Sci Mol Med 50: 241–247, 1976.
39. Takarada Y, Takazawa H, Sato Y, Takebayashi S, Tanaka Y, Ishii N. Effects of resistance exercise combined with moderate vascular occlusion on muscular function in humans. J Appl Physiol (1985) 88: 2097–2106, 2000.
40. Wernbom M, Augustsson J, Thomee R. The influence of frequency, intensity, volume and mode of strength training on whole muscle cross-sectional area in humans. Sports Med 37: 225–264, 2007.
Keywords:

body composition; growth hormone; testosterone; cortisol; isometric strength

Copyright © 2016 by the National Strength & Conditioning Association.