Introduction
Strength training performed with vascular occlusion, also known as blood flow restriction (BFR), has been proposed as a novel method to improve strength and hypertrophy, even in a short span of time. There are some studies using strength exercises with BFR that have shown improvements in strength, muscle mass, reduction on cardiovascular preload, and preventing disuse atrophy in orthopedic restrictions (20,26,34 ).
In the BFR method, strength exercises are performed with a very small load/intensity, which represents low mechanical stress in both joint and muscular tissues. Pooling of venous blood and reduced cardiac preload seem to be the main acute vascular responses induced by this method (34 ). Moreover, acute and chronic hemodynamic changes induced by strength exercises using the BFR method have been associated with alterations in endothelial function, although mechanisms supporting these changes are not clear, especially when comparing different intensities and volumes of training (10,16 ).
Changes in endothelial function are fully dependent on the intensity of exercise ; therefore, load and volume seem to directly affect these changes in response to a strength training program (19 ). Studies have compared the effects of different strength training programs on several variables, especially comparing traditional exercises (i.e., without BFR) and BFR exercises (13,17,22,28,37 ). However, to the best of our knowledge, no studies have compared these different exercises modes performed with equalized volumes. Thus, to ensure that the differences between the protocols are only those of exercise intensity, whether BFR is or is not used, it is very important that the next studies equalize the training volumes for the protocols to be compared.
Evidence shows that hypertrophy and strength gains occurred even with intensity between 20 and 50% of 1 repetition maximum (1RM) with BFR, thus demonstrating similar adaptations to conventional training (22,26,30,37 ), but the intensity range for optimal endothelial function adaptation could not be reported yet. In this way, some studies have shown that intensity of strength exercise could impair endothelial function in sedentary subjects (5,15 ). To get overall results in neuromuscular adaptation similar to traditional strength training, a variety of molecular and metabolic mechanisms need to occur with vascular restriction training. For example, low oxygen availability induces the recruitment of a motor unit with a high threshold, even at low loads (25 ), causes cell swelling, activating muscle adaptation pathways to mTOR (24 ), and induces inhibition of myostatin (22 ) and secretion of growth hormone (GH) (35 ), among other things. However, it is necessary to conduct more studies comparing these different methods on the parameters of endothelial function. It is not known whether or not the occlusion is aggressive to the blood vessels.
Thus, the aim of this study was to evaluate and compare the acute and chronic effects of resistance training with and without partial vascular occlusion on neuromuscular adaptations and morphological and endothelial functions in young physically active adults who undergo the same training volume, but with different intensities.
Methods
Experimental Approach to the Problem
The subjects (n = 28) were randomly assigned into 2 groups: the LI-BFR group (low-load resistance training with BFR; n = 15) and the HI-RT group (high-load resistance training without BFR n = 13). Both groups performed unilateral exercise of elbow flexion and knee extension for 8 weeks, 3 times per week and the volume was equalized. The groups were assessed before and after training and the evaluators were blinded regarding the patients and the variables studied. The dependent variables were torque, muscle thickness (MT), electromyography (EMG), and endothelial function. The independent variables were the training protocols and the variable intervening volume of training, which was controlled.
Subjects
Twenty-eight male subjects (mean ± SD : age, 23.96 ± 2.67 years; body mass, 77.70 ± 11.98 kg; and height, 1.74 ± 0.05 m) were recruited. The subjects were healthy and physically active, had not practiced strength training in the past 3 months, and were nonsmokers (Table 1 ). The sample size was determined using the study by Goldfarb et al. (14 ) as a reference, in which the confidence level was 95%, the coefficient of variation was 7.98, and the standard margin of error was 5%. The individuals who used ergogenic aids or dietary resources, who had any disease that would restrict the practice of exercise , any type of metabolic disease that altered hemodynamic function, and who had any type of heart or circulatory disease were excluded. The written informed consent (IC) was read and signed by subjects and this study was approved by the Ethics and Research Committee of Methodist University—IPA, by number 364.202.
Table 1.: Sample characterization and comparison of anthropometric measurements.*†
Procedures
The subjects came to the Exercise Physiology Laboratory of the Research Center in the Methodist University—IPA, for the explanation of study protocols and for signing the IC. Then, the medical history questionnaire (PAR-Q) was filled to ensure that there were no risks to health, as well as filling out a questionnaire on the level of physical activity (IPAQ), the short version. Later, the anthropometric evaluation was based on the anatomical site markings and the technique of measuring skinfolds following the standards of the International Society for the Advancement of Kinanthropometry (ISAK), body composition was calculated using a 5-component method (27 ), and flow-mediated dilation (FMD) was performed. After that, 3 meetings were held for familiarization with exercises and machines. Subsequently, the 1 repetition maximum test (1RM) (7 ) and a number of repetitions at 60% 1RM (rep. 60% 1RM) were performed, and the 60% load was adjusted at the end of training (2 ). At another moment, the subjects performed isokinetic and isometric tests in the upper and lower limbs, the EMG signal was measured, and MT was assessed. Finally, there was an acute exercise protocol in which subjects performed the exercise protocol that was specific to the training group (LI-BFR or HI-RT) and blood sampling was performed before and after acute exercise . All procedures were performed with an interval of 72 hours. At the end of the training, the subjects underwent the same procedures.
The HI-RT performed high-intensity exercise (80% 1RM) without BFR (4 sets, 8 reps). The LI-BFR group performed low-intensity exercise (30% 1RM) with BFR. The training volume was calculated by sets × reps × load (7 ). To ensure that the volumes of training for both groups were equal, taking into account all strength training variables, the LI-BFR group also held 4 sets, but the number of repetitions in each set was calculated according to the volume of training of the HI-RT group. For this purpose, we used 4 steps: first, an average of 1RM of HI-RT for the exercise of elbow flexors and knee extensors (12.36 ± 2.42 and 64.49 ± 11.78 kg, respectively). Second, the overall mean of the 1RM was multiplied by 4 and multiplied by 8 corresponding to the number of sets and repetitions that the HI-RT group had to perform to reach the training volume (the elbow flexors volume was 395.21 and the knee extensors volume was 2065.75). Third, a mean of 30% of the 1RM of LI-BFR subjects for the exercise of elbow flexors and knee extensors was performed (4.78 ± 1.01 and 21.82 ± 5.22 kg, respectively). Finally, to obtain the number of LI-BFR repetitions, the following calculation was performed: The general volume of the HI-RT group was divided by the multiplication between the general average of the load of 30% of 1RM and 4 sets, totaling approximately 20.70 repetitions (rounded to 21) for elbow flexors and 23.64 repetitions (rounded to 23) for knee extensors. All subjects were instructed to complete the repetitions and sets. The rest time between sets for both groups was 2 minutes (occlusion was maintained during passive rest in the LI-BFR group) and execution of the movement was controlled using a metronome (every 2 by 2 seconds).
For partial occlusion determination, the subjects arrived at the Laboratory of Physiology Exercise at the Methodist University Center—IPA and were placed in the supine position to remain at absolute rest for 20 minutes. After this, the resting blood pressure was measured, and it was later used in the cuff fixing calculation for partial occlusion of the limb. In the exercise of biceps curls, the cuff was fixed in the upper arm and for occlusion, cuff was inflated to 20 mm Hg below systolic blood pressure (14 ). In knee extension exercises, occlusion occurred 3 minutes after removing the cuffs of the upper limbs. Then, the occlusion protocol was determined being 40 mm Hg above the value used to occlude the upper limb (14 ). In all cases, the cuff was fixed in the upper arm or thigh. To ensure that the methodology used for partial occlusion was reliable, an oximeter was used (Nellcor NPB 195; Mallinckrodt, Inc., St. Louis, MO, USA) after each set to ensure that the blood flow was not completely disrupted (14 ). This occlusion methodology was chosen because the partial occlusion used in this study only prevents the venous flow, whereas total occlusion prevents both the venous and arterial flow; therefore, we opted for the less aggressive methodology. If the oximeter did not detect the pulse on the finger, the cuff had pressure reduced in increments of 5–10 mm Hg until the pulse was detected. The cuff used for lower flow restriction limbs was 112 cm long and 16 cm thick, whereas for the upper limbs, we used a cuff that was 54 cm long and 14 cm thick.
Peak torque of elbow flexors and knee extensors was assessed on a Cybex NORM dynamometer (Ronkonkoma, NY, USA) in concentric (60°·s−1 ) and isometric (at 90° of elbow flexion and 60° of knee flexion; 0°: full joint extension) conditions. For knee extension, subjects were seated on the dynamometer chair (6 ), and for elbow flexion, a Scott bench was attached to a dynamometer (12 ). Warm-up consisted of 10 submaximal concentric repetitions at 120°·s−1 . Before each test, subjects performed a pre-test that simulated the test condition, except for submaximal effort. The concentric isokinetic test consisted of 5 maximal repetitions for both elbow flexion and knee extension. After 2 minutes, 3 maximal isometric contractions were performed for both muscle groups; each one sustained for 5 seconds, with a 2-minute rest interval between them. Subjects were instructed to attain physical exertion “as fast and hard as possible.” Pre- and post-training tests followed the same evaluation order and procedures. The greatest peak torque in each test provided by the HUMAC 2009 software version 12.17.0 (HUMAC, NY, USA) was used for further analysis. Intraclass correlation coefficients for isokinetic and isometric tests were 0.91.
The collection of the EMG signal activity was recorded from the biceps brachii (BB), rectus femoris (RF), and vastus lateralis (VL) muscles during maximal isometric and isokinetic strength testing. Before placing the electrodes, shaving was performed using a disposable blade, and abrasion of the skin with alcohol and cotton was performed for the removal of oils and dead cells, thereby reducing skin impedance. Bipolar electrodes (20-mm interelectrode distance) were placed at the muscle belly in the direction of muscle fibers, according to SENIAM (http://www.seniam.org ). To ensure reliability of positioning of electrodes between pre-training and post-training, an evaluation map was used for each subject for proper placement (6 ).
A raw EMG signal was obtained using a Miotool 200, 2-channel electromyograph (Miotool; Miotec, Porto Alegre, Brazil) with sampling frequency of 2,000 Hz per channel and amplified by a factor of 100. Analyses were performed using SAD32 software. The EMG signal was Butterworth-filtered using cutoff frequencies of 20 and 500 Hz for lower and upper band-pass, respectively. Then, root mean square (RMS) values were obtained from EMG data at 1-second torque plateau for the best isometric trial (isometric RMS) and from the best concentric repetition (isokinetic RMS) for both elbow flexors and knee extensors. The evaluations were conducted by experienced evaluators according to pre-established and widely used techniques.
Assessment of MT was performed using ultrasound imaging (Toshiba Model Nemio XG) being obtained in the B-mode (32 ). Before image capture, the subjects were at rest for 10 minutes in supine position, with limbs relaxed and extended. To measure MT of BB muscles and brachialis (BR) of the upper limbs and RF muscle, vastus medialis (VM), vastus lateralis (VL) and vastus intermedius (VI) of the lower limbs of each individual, a linear transducer frequency was used (7.5 MHz), which was positioned perpendicularly to the muscles evaluated. A water-soluble gel was used to promote acoustic contact with the evaluated structure and minimum pressure was applied over the transducer. All ultrasound evaluations were performed by a qualified experienced appraiser.
For the BB and BR, a measurement was used distally corresponding to 60% of the distance between the lateral epicondyle of the humerus and the acromion. The point for assessing MT of RF, VI, and VL was half the distance from the greater trochanter and the lateral epicondyle of the femur (21 ). For the VM, it was captured the image at the location corresponding to 30% of the distance between the lateral epicondyle and the greater trochanter of the femur (18 ). A dermographic pen was used for marking the points. In addition to these reference points mentioned above, for BB and VL 2 other points were used: one proximal and one distal from the said reference point (midpoint) for the evaluation of MT. The other 2 points were assessed at BB 4 cm below and above the reference point mentioned above and VL 5 cm below and above the reference. Three images of each point were saved for posterior analyses and mean thickness was calculated for future comparisons.
For the analysis of images and measurements of MT, a perpendicular line was drawn to the inner edges, top, and bottom of the fibrous sheath of each muscle evaluated in the ImageJ (version 1:37, National Institutes of Health, USA) software. For the analysis of the thickness of the VL and RF, the distance between the subcutaneous fat and aponeurosis VI was considered, as identified in the image. As for the thickness of the VI and VM, the distance from the upper-muscle aponeurosis and bone aponeurosis was considered. To ensure capture of images at the same points, the pre-training and post-training system was used for evaluation maps as described above. All images were captured and analyzed by the same evaluator.
For comparison, we used the summations of MT of the reference points of each muscle evaluated in a muscle group (average BB + BR and VL average + RF + VM + VI) with the goal of full representation of the muscle group and the aggregate MT. Intraclass correlation coefficient for MT was 0.83.
The FMD of the brachial artery in response to reactive hyperemia was measured on an ultrasound device (Toshiba model Nemio XG) as an indirect measure of endothelial function adapted to the current guidelines (36 ). Assessments occurred before and after performing each exercise protocol in a warm room (21–24° C) always in the same period of the day, after 15 minutes of rest in the supine position. A high-frequency transducer (11.0 MHz) was used with water-based gel to obtain images of the longitudinal upper and lower walls of the brachial artery, with simultaneous electrocardiographic tracing. In the period before occlusion, 5 baseline images were analyzed and the average of them was used as a basal diameter of the brachial artery value; then, a pressure cuff placed on the forearms of the subjects was inflated to 250 mm Hg and maintained for 5 minutes (9 ). After 5 minutes of occlusion, the cuff was removed and new images of the brachial artery were obtained. The entire evaluation was recorded on a DVD for later analysis in the software ImageJ.
To minimize the influence of the cardiac cycle in arterial diameter, determination of the thicknesses was always in the “R” wave of the electrocardiogram. Due to the inability to perform a scan of the arterial diameter throughout the post-closure period as proposed in the guidelines, evaluations of arterial diameters were performed in fixed periods of 60 and 75 seconds after releasing the cuff. These periods were selected because the peak dilation of the brachial artery occlusion after 5 minutes varies significantly between periods in different populations and levels of training. The highest dilation value found was used for further analysis. The FMD values were shown absolutely and as a percentage relative to the increase in the brachial artery diameter after reactive hyperemia protocol. The calculation for determining the percentage of vasodilation was as follows: Where EH is the thickness of the brachial artery after reactive hyperemia and EB is the basal thickness of the brachial artery (9,36 ). The evaluations were performed by experienced evaluators according to pre-established and widely used techniques.
Obtaining a Biological Sample
Venous blood samples were collected (10 ml) without anticoagulant to obtain serum and heparin to obtain plasma. This was done before and after acute exercise in pre- and post-training. Serum was separated by centrifugation for 10 minutes at 2,500 rpm. Shortly afterward, it was aliquoted and frozen for later analysis.
Nitrite levels were determined by the method described by Miranda (29 ). The Griess reagent was prepared by mixing equal volumes of sulfanilamide (1%) dissolved in HCl (0.5 M) and N-naphthylethylenediamine (0.1%) in distilled water. Volumes of 250 μl of plasma and 250 μl of trichloroacetic acid 10% (TCA) were added in a test tube and centrifuged at 2,500 rpm for 10 minutes in order for the sample to lose protein. By using the enzyme-linked immunosorbent assay plate, 100 µl of deproteinized sample was added to 100 µl of a saturated solution of vanadium chloride to reduce nitrate to nitrite. Then, 100 µl of Griess reagent was added, leaving the material for 30 minutes at room temperature protected from light for reading at 540 nm in enzyme-linked immunosorbent assay. A standard curve was obtained with different volumes of sodium nitrite added to 100 µl of Griess reagent.
Statistical Analyses
For calculating the sample size, the study by Goldfarb et al. (14 ) was used as reference. The calculation was performed using the WinPEPI program Version 4.0, in which confidence level will be 95%, the coefficient of variation 7.98, and a standard margin of error of 5%. Thus, each experimental group consisted of 15 volunteers accounting for a 10% sample loss.
Distributions of all variables to verify the normality by the Shapiro-Wilk test was evaluated, assuming a homogeneous normal distribution. It used analysis of variance for repeated measures with the Bonferroni post hoc test. Significantly different values were considered when p ≤ 0.05. All data were analyzed using the Statistical Package for Social Sciences (SPSS) 17.0.
Results
The 15 volunteers who started the resistance training with BFR protocol completed all sessions of training, whereas in the HI-RT group, 2 volunteers gave up due to personal problems by the second week of training, ending with a total of 13 subjects. Table 1 displays the baseline characteristics, in mean and standard deviation. Moreover, the anthropometric measures did not show significant differences before and after training and between groups.
Table 2 shows the mean of FMD and nitrite and nitrate (NOx) measures. There was a significant difference between pre-training and post-training at rest FMD in the LI-BFR group (4.44 ± 0.51 vs. 6.35 ± 2.08 mm, respectively). For NOx concentrations, there were no difference between groups; however, there were significant differences in both groups when comparing pre- and post-acute exercise (pre-training—NOx 1.1 baseline 29.95 ± 2.19 µmol·L−1 and after acute exercise 35.4 ± 4.00 µmol·L−1 ; baseline 30.7 ± 0.19 µmol·L−1 and after acute exercise 35.61 ± 2.56 µmol·L−1 , respectively, in the LI-BFR and HI-RT groups; post-training—NOx 1.2 baseline 29.97 ± 4.59 µmol·L−1 and after acute exercise 34.56 ± 3.01 µmol·L−1 ; baseline 30.04 ± 1.33 µmol·L−1 and after acute exercise 35.08 ± 4.18 µmol·L−1 , respectively, in the LI-BFR and HI-RT groups).
Table 2.: Assessment of endothelial function by flow-mediated dilation (FMD) and concentration of nitrate and nitrite (NOx).*†
Table 3 shows the torque and rep. 60% 1RM improvements and there was a rise in all parameters when comparing baseline and post-training in both groups. There were differences between groups only in isometric delta elbow flexion and isokinetic delta knee extension (isometric delta EF 3.42 ± 5.09 and 9.61 ± 7.52 N·m; isokinetic delta KE 12.78 ± 25.61 and 42.69 ± 35.68 N·m, respectively, in the LI-BFR and HI-RT groups).
Table 3.: Absolute values of muscle torque, rep. 60% 1RM (pre-training and post-training), and muscle torque delta.*†
Table 4 shows the hypertrophy and EMG results. There was an increase of MT in both groups when comparing the baseline and post-training. An increase of both isokinetic and isometric EMG of biceps of the HI-RT group was observed. The same was observed for the LI-BFR group on isokinetic and isometric EMG of VL.
Table 4.: Absolute values of hypertrophy and electromyography (EMG), pre-training and post-training.*†
Discussion
This study compared the neuromuscular and morphological adaptations after an 8-week training period with or without vascular occlusion and the same training volumes. Furthermore, exercise -related and training-related changes in endothelial function assessed by flow-mediated dilation and nitrites/nitrates concentration were reported.
Strength training with BFR is now becoming an important alternative training methodology for people who have some kind of restriction regarding high mechanical loads. For example, people with a high risk of cardiovascular events could not withstand high mechanical loads. Vascular health is a predictor of cardiovascular events and it is related to endothelial function. It is well known that exercise and hypoxia are factors that change endothelial function. Because BFR decreases oxygen delivery to muscles, this training methodology could change endothelial function. It seems important to clarify that mechanism in healthy people to better understand it so as to support future studies involving subjects with endothelial dysfunction–related diseases. Finally, to reliably compare both protocols, it is necessary to control the volume of the methods used in the study. Therefore, the only difference between groups was the intensity and the occlusion of the limb. The importance of this work is highlighted as there are few studies with controlled volume of training that evaluate all of these parameters.
The LI-BFR and HI-RT groups were homogeneous in pre-training time as shown in Table 1 . In addition, 8 weeks of training was not able to generate significant changes in body composition.
When evaluating endothelial function, at no time were significant differences shown between groups at variable FMD and NOx (Table 2 ). However, the LI-BFR group showed a significant increase in FMD and NOx after training periods when compared with the baseline. The HI-RT group showed a significant increase only in variable NOx.
Our data are innovative when analyzing the vascular response evaluated by FMD and NOx for 8 weeks of strength training. In this way, several factors have influenced FMD, such as ischemia-reperfusion mechanism. Both groups showed similar results for NOx, but FMD only increased for the LI-BFR group. In addition, FMD was similar between groups after training. The muscular contraction and relaxation during exercise could simulate the ischemia-reperfusion mechanism, but intensity of exercise is important. If there is no BFR, probably both groups would have different FMD effects, because exercise intensity has been showing a crucial role in FMD response (5 ). However, BFR caused the same effect on low-intensity training compared with high-intensity training without occlusion, because both groups have no significant differences after training.
Nitric oxide (NO) production is influenced by shear stress mechanism and its bioavailability is altered by oxidative stress (3,16 ). Because NOx concentration was equal between groups, at all moments, it seems that the same effect of FMD occurred. The BFR added to low intensity of training could be able to generate the same biomarker increases compared with high-intensity training without occlusion.
Partial vascular occlusion during exercise partially interrupts arterial influx and blocks venous return; so, we can hypothesize that shear stress could be increased. Therefore, our results could be explained by the positive relationship of shear stress and NO bioavailability causing FMD increase. Thus, the adjustment of FMD with occlusion training must be related to endothelial vasodilators but some other endothelium-independent mechanism could also be related.
It is well established that low-intensity exercise with BFR promotes strength gains and hypertrophy (22,30,33 ), even showing similar benefits when compared with high-intensity exercise without occlusion (22 ). According to Abe et al. (1 ), 2 weeks of low-intensity strength training with BFR would already be enough for approximately 22% of power increase in the leg-press exercise . In addition, there was an increase of 7–8% of the thigh hypertrophy, evaluated using magnetic resonance imaging, a result similar to a periodization of 3–4 months of high-intensity training (1 ). Furthermore, Shionahara et al. (33 ) conducted a study with untrained subjects that presented, in thighs that underwent occlusion, a 9% increase in maximum power in 2 weeks and 26% after 4 weeks of training. However, the thighs that only underwent low-intensity training received no significant gains (33 ).
In the study by Laurentino et al. (22 ), after 8 weeks of training, the sample showed an approximately 40 and 36% of 1RM increase at knee extension for occlusion and high-intensity groups, respectively. In our study, the results showed a significant increase in both groups evaluating the basal values with the results after 8 weeks of training (Table 3 ), which confirms the literature, again highlighting this study with groups equalized by volume of training, differing only in intensity and occlusion.
Another important result in our study was the significant increase in repetitions with 60% 1RM after training in both groups (Table 3 ), with no significant difference between them. Even with equal volumes of training between the 2 groups, repetitions and intensities were different, but theoretically according to Loenneke et al. (2010), the 2 groups recruited the same type of fiber. The authors explain that when oxygen availability decreases during occlusion, an increasing recruitment of motor units occurs progressively to make up for the power deficit (25 ). Moreover, there is an increase in the EMG signal during occlusion, thereby suggesting that there is an increase in the activation of fast fibers (type 2) (23 ). According to the principle of activation of motor units, when recruiting the fibers of type 2, type 1 fibers were also recruited. If the 2 groups trained recruiting type 2 fibers, even with different intensities, the type 1 fibers must have undergone some training effect, increasing resistance in the test 60% of 1RM. Thus, the results presented in this work that in repetitions with 60% 1RM can be explained by the same fiber recruitment in both groups, indicating that occlusion “decharacterizes” high-intensity and low-intensity difference as the results are similar.
Peak torque was evaluated in dynamic and isometric forms in an isokinetic dynamometer. The 2 training groups had a significant increase in peak torque both in elbow flexion and knee extension. Furthermore, the delta results were significantly higher in the HI-RT group for isometric elbow flexion and isokinetic knee extension. Low-intensity training with BFR has been shown to have similar results compared with high-intensity training. However, the delta results of this study showed significant differences between groups, and it may be related to the control of training. It seems that the equalized volume of training promoted a greater strength gain for the high-intensity group. We believe that this effect occurred because the equalized volume makes the intensity the only difference between groups, but these results can also be related to the theory proposed by Loenneke et al. (26 ).
Loenneke et al. (23 ) proposed a theory called “theoretical reverse pattern of adaptations in traditional vs. low-intensity blood flow–restricted exercise ” (reverse theory), which may explain the delta differences between groups. They proposed that the neural and hypertrophic adaptations may occur in the opposite way to conventional strength training proposed by Sale (26 ). Thus, we could hypothesize that the greater strength gains for the high-intensity training group takes place at the first 8 weeks as a result of neural adaptations. Meanwhile, the low intensity with BFR group would have hypertrophic adaptations and the strength gains may occur after 8 weeks with neural adaptations (26 ).
In this work, muscle activation (EMG signal) did not differ between the groups and these results could be explained by the same recruitment pattern of fiber type II. Muscle activation of elbow flexors increased only for the high-intensity training group. Because elbow flexors activation does not take place for the vascular occlusion group, it seems that the “reverse theory” would be confirmed. However, EMG for knee extensors showed opposed effects with the only group increasing muscle activation being the vascular occlusion group. Thus, neural adaptations could be different between upper and lower limbs. In addition, MT increased for both groups, contradicting the “reverse theory” (26 ).
Muscle thickness had baseline values that were similar between groups and showed significantly different changes after the intervention (Table 4 ). These results are in agreement with many other studies showing similar hypertrophic adaptations between high-intensity training and low-intensity vascular occlusion training (8 ). So far, the physiological mechanisms eliciting hypertrophy in strength training with BFR are not entirely clear. A variety of molecular and metabolic mechanisms for strength and hypertrophy adaptations, which will be discussed below, may explain the results of low intensity with vascular occlusion training.
The low availability of oxygen and metabolic stress during full or partial occlusion causes a progressive recruitment of motor units, which may occur to offset the deficit strength output. The activation of fast-twitch fibers (type II) after that progressive recruitment would occur due to the activation of high-threshold motor units (25 ). Furthermore, the increase of water content in the muscle cell takes place with BFR and exercise . This “swelling” would cause different intracellular signals including activation of mTOR and MAPK pathways increasing muscle adaptation (24 ).
Loenneke et al. (25 ), in their review article, note that several studies show an increased concentration of GH after training with occlusion, appearing to be related to acidity of intracellular environment. The low pH seems to cause sympathetic activation through the afferent neurons type III and IV (also sensitive to metabolite accumulation: K+ , H+ , AMP, and hypoxia) that are related to the significant increase in pituitary GH secretion (25 ).
In the same way, some researchers have been studying the acute effect of this training to clarify the mechanisms that are involved in its methodology. A study of young adult males, which evaluated the acute effect of strength training with vascular occlusion, showed an increase in GH levels compared with resting levels (35 ). The research of Pierce et al. (31 ) found that the group that underwent ischemia and exercise (20% of maximal voluntary contraction) increased GH levels approximately 9 times the baseline levels, but no significant increases were shown by the group that only performed ischemia. Abe et al. (1 ) demonstrated that GH levels are related to circulating IGF-1 increases stimulating protein synthesis. Therefore, the production of IGF-1 stimulates an activation cascade, for example, of Akt (also known as protein kinase B—PKB). The Akt promotes the activation of mTOR and GSK-3B (glycogen synthase kinase-3B) both inducing skeletal muscle hypertrophy (4 ).
A study performed at the University of Texas evaluated another protein (S6K1—ribosomal S6 Kinase1) that has a strong relationship with mTOR. The study demonstrated that training with vascular occlusion stimulates the phosphorylation of S6K1, which is the key regulator of translation initiation and protein synthesis in human skeletal muscle (11 ). In addition, the increases of cross-sectional area and strength gains with vascular occlusion training could be related to myostatin, a potent inhibitor of muscle growth. Laurentino et al. (22 ) found that physically active males can have an approximately 40% expression decrease of myostatin gene with occlusion and high-intensity training.
Finally, this study showed similar strength gains and hypertrophy of the low-intensity strength training with BFR compared with high-intensity resistance training with controlled volume of training, and few studies equalize the training volume of groups. It can be suggested that this method may be a very important tool for people who cannot undergo the mechanical stress caused by traditional strength training. In addition, endothelium-dependent function seems to change positively with vascular occlusion resistance training. Thus, in addition to strength and hypertrophy gains, this study also shows benefits related to vascular function. This demonstrates a clinical importance of low-intensity vascular occlusion training as an alternative methodology.
Practical Applications
Because of the low workloads, strength training with BFR can be an alternative training method for individuals who have some orthopedic, cardiovascular, or metabolic limitation. Future studies can test this methodology for patients who have endothelial dysfunction–related diseases, including diabetes mellitus, hypertension, and heart failure. Vascular occlusion could be an additional method for athletes to increase strength and hypertrophy gains, like individuals seeking body composition changes.
Acknowledgments
This work was funded by the Higher Education Personnel Training Coordination (CAPES) and the Foundation for Support of Research of the State of Rio Grande do Sul (FAPERGS). The authors thank the IPA Methodist University Center and Federal University of Rio Grande do Sul (Porto Alegre, Brazil). They declare that there is no conflict of interest. This work was funded by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and FAPERS (Fundação de Amparo à Pesquisa do Rio Grande do Sul).
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