Effect of Continuous and Intermittent Blood Flow Restriction Deep-squat Training on Thigh Muscle Activation and Fatigue Levels in Male Handball Players

Abstract

Background: We aimed to investigate acute changes before and after low-intensity continuous and intermittent blood flow restriction deep-squat exercises on the thigh muscle activation characteristics and fatigue level under suitable individual arterial occlusion pressure (AOP) to provide a theoretical basis and practical reference for athletes undergoing blood flow restriction training.

Methods: Twelve elite male handball players were recruited. Continuous (Program 1) and intermittent (Program 2) blood flow restriction deep-squat exercises were performed with 30% one-repetition maximum intensity. Program 1 does not include decompression during the intervals, while Program 2 contains decompression during each interval. Electromyography (EMG) was performed before and after two blood flow restriction training programs in each period. EMG signals of the quadriceps femoris, posterior femoral muscles, and gluteus maximus, including the root mean square (RMS) and normalized RMS and median frequency (MF) values of each muscle under maximum voluntary contraction (MVC) before and after exercise were calculated.

Results: The RMS value under MVC (RMS_MVC) of the rectus femoris, vastus medialis, vastus lateralis, gluteus maximus decreased after continuous and intermittent blood flow restriction training programs, and those of the biceps femoris and semitendinosus increased; rectus femoris changed significantly after continuous exercise (P<0.01). RMS_MVC values of the biceps femoris and semitendinosus changed significantly after intermittent exercise (P<0.01). The RMS values of the vastus lateralis, biceps femoris, and semitendinosus were significantly increased after continuous and intermittent blood flow restriction training (P<0.05). The gluteus maximus RMS value significantly decreased after cuff binding (P<0.05); The MF values of rectus femoris, vastus medialis, vastus lateralis, and gluteus maximus decreased significantly after continuous blood flow restriction training (P<0.05).

Conclusion: Continuous blood flow restriction deep-squat training under 50%AOP is more effective than the intermittent training in removing pressure on the thigh muscle group. In the third and fourth sets of exercise, all muscle groups showed a significant increase except the medial femoral muscle. However, this may also cause fatigue that may be harder to eliminate than that after intermittent training. 

Background

Resistance training can effectively promote muscle hypertrophy and increase strength in athletes [1]. Reducing intensity in training combined with blood flow restriction can cause the same adaptation effect [2–5]. Low-intensity blood flow restriction training, also known as blood flow restriction (BFR) training, can induce an increase in muscle volume and strength, and its force gain effect is similar to that of traditional high-intensity resistance training [6–8]. At the same time, blood flow restriction training can promote muscle activation to ensure a total power output similar to traditional training [9–11]. In addition, blood flow restriction training can enhance neural activation and promote the mobilization of type II motor units [12]. Therefore, the neuromuscular response generated by external pressure stimulation is also one of the main causes of muscle hypertrophy. Shinohara et al. concluded that the neuromuscular activity level generated by low-intensity blood flow restriction training is equivalent to that generated by traditional high-intensity resistance training, and both can promote the mobilization of type II motor units [13]. However, whether neuromuscular factors play a key role in blood flow restriction training induced muscular adaptation is unclear.

In studies on muscle hypertrophy induced by blood flow restriction training, different selection methods of external pressure resulted in different understandings of its physiological mechanism. Moore and Pierce used arbitrary, subjective pressure values to implement the blood flow restriction training program [14, 15], while Abe and Yasuda calculated external blood limit pressure based on brachial artery resting systolic pressure and applied it to their experimental design [16, 17]. Loenneke et al. pointed out that neither of the above two methods represents an effective strategy for controlling the blood pressure limit of the lower limbs [18]. Different girths experience different degrees of blood flow restriction under the same pressure condition and then produce completely different training stress responses. Laurentino et al. studied the pressure required to complete vascular occlusion in the upper thigh under static condition [19]. Therefore, the relative pressure calculated using the individual specific percentage of arterial occlusion pressure (%AOP) deserves widespread application and promotion.

In studies exploring the instantaneous changes in muscle activation caused by different external pressure stimuli before and after compression resistance training, the exercises were mainly single joint movements such as elbow flexion of the upper limb and isokinetic knee extension of the lower limb. Loenneke et al. found that knee stretching with 40–50%AOP to limit blood pressure may change the flesh instant response of the quadriceps femoris and improve the muscle activation level, while higher pressure does not cause these changes [20]. In the field of multi-joint sports, Li Zhiyuan et al. concluded that the application of 50% AOP can significantly improve the optimal activation degree of the quadriceps femoris and posterior femoris muscle groups of male handball players at the same time, resulting in the best training effect [21].

However, the effects of continuous and intermittent compression exercises on thigh muscle activation and fatigue during weight-bearing squats under the same external adaptive stress conditions have not been thoroughly investigated. Therefore, this study aimed to investigate the characteristics of the instantaneous changes in muscle group activation and fatigue of the lower limbs of male handball athletes before and after squat training with two modes of continuous pressure and depressure intervals under 50% AOP stimulation. This study provides a theoretical basis and reference for the scientific selection and rational utilization of the interval mode in blood flow restriction training. In this study, it was assumed that the activation of the anterior and posterior thigh muscle groups increased significantly during both continuous and intermittent pressure training programs. In contrast, the activation degree of the anterior thigh muscle group decreased, and that of the posterior thigh muscle group increased after pressure removal. However, continuous training leads to transient fatigue reactions in the anterior thigh muscle group.

Methods

MVC test and root mean square (RMS) value collection

After placing the surface electrodes, the electrode wires were connected to test the thigh muscles’ MVC, and the corresponding muscle surface EMG signals were recorded. Specific testing methods are outlined in the EMG manual [25] (Fig. 4). We collected and recorded surface EMG values, which were used as RMS values under MVC (RMS_MVC) after processing.

Surface EMG data collection and processing

Before each squatting test, the camera and Waveplus wireless EMG acquisition system were set up. After the subjects began to move, the acquisition system was turned on to collect the EMG data. All EMG signals from 1 to 4 sets of exercise were selected according to the synchronous video of the experiment. The original EMG data were cleaned, filtered, smoothed, and their amplitude standardized using the matching analysis software of the Emgserver instrument, and the selected index was the RMS amplitude. The range of muscle exertion was selected from the original EMG, and the mean RMS was determined. The EMG RMS of each muscle obtained during MVC testing was defined as 100%MVC. The standardized EMG data processing system automatically divided the EMG RMS value obtained in each set by the EMG of maximum voluntary contraction (EMG_MVC) value for standardized processing; the RMS standardized processing unit is %.

Results

Discussion

Analysis of the change characteristics of the thigh muscle groups’ maximum activation before and after the compression squat exercise

The results in Table 2 show that the RMS_MVC values of the rectus femoris, vastus medialis, and vastus lateralis decreased after compression removal. The RMS_MVC values of the rectus femoris changed significantly after continuous compression (P < 0.05), while those of the vastus medialis and vastus lateralis showed no significant change (P > 0.05). Most previous studies showed that after the implementation of blood flow restriction training, the maximum activation of active muscles restricted by blood flow had a downward trend. Loenneke et al. [18] performed compression and non-compression one-knee stretching exercises with the quadriceps as the main active muscle group in 16 healthy adult males and found that the MVC value of the quadriceps muscle decreased after the compression and non-compression leg exercises. Umbel et al. [26] found that the MVC value of centripetal contraction decreased by 9.8%, and the MVC value of centrifugal contraction decreased by 3.4% after 24 h of unilateral compression knee stretching exercise and returned to normal after 96 h, which may be related to delayed onset muscle soreness. Fatela et al. [27] performed compression knee stretching exercises with different blood pressure limits in 14 adult males and found that the vastus medialis and vastus lateralis’ RMS_MVC values decreased significantly after exercise under 60 and 80% BFR relative blood pressure limits. This study found that compared with knee stretch exercise, the pressurized squats exercise can lead to reduced quadriceps activation; additionally, compared with the intermittent exercise continuous pressurized squats exercise it led to more reduction, which may be linked to activity of the muscle cell metabolites caused by excessive accumulation of acidosis.

In addition, the results in Table 2 also showed that the RMS_MVC values of the biceps femoralis and semitendinosus increased after the compression squatting program, and there was a significant change after the interval training. However, the RMS_MVC value of the gluteus maximus decreased and significantly changed after continuous pressure interval exercise. The results showed that the RMS_MVC of the posterior thigh muscle showed an increasing trend after compression squat exercises. Yasuda et al. [28] also found that the activation contribution rate of the triceps brachii as an antagonistic muscle increased from 40–60% after 30%-1RM multi-joint compression bench press exercise, suggesting that compression exercise can improve the maximum independent activation rate of antagonistic muscles and thus effectively develop the strength of antagonistic muscle group compared with non-compression multi-joint exercise. The results also showed that RMS_MVC values of the biceps femoralis and semitendinosus increased significantly after blood flow restriction training. This indicated that blood flow restriction training can provide an optimal acidic environment to activate fast muscle fibers in the posterior thigh muscle group and induce more muscle fibers to activate.

Analysis of changes in the activation degree of thigh muscle groups before and after compression squat exercises

Many studies have confirmed that the RMS value of active muscles increases during low-intensity compression exercises. After the exercises, the RMS values of the anterior and posterior thigh muscle groups were higher than those before compression exercises. During continuous compression exercises, vastus lateralis, biceps femoralis, and semitendinosus were significantly improved. After the compression band was removed, the RMS values of the anterior and posterior thigh muscle groups decreased compared with the RMS values of the period before the compression at the end of the implementation of the compression program but were higher than the RMS values before compression.

The above results show that after the implementation of the compression program, the activation of the thigh’s anterior and posterior muscle groups increased. It is mainly caused by the acidic environment resulting from the accumulation of metabolites in the muscle, which can generate more type II muscle fibers, thus increasing the average amplitude of the electromyographic signal on the surface [29]. Fatela et al. [27] also found that rectus femoris and vastus medialis activation changed with external blood pressure limitation during compression knee stretching exercises. Acute external pressure stimulation increased the RMS values of the rectus femoris and vastus medialis; nevertheless, the vastus medioris and rectus femoris responded differently to different external pressure stimulations. Vastus medialis activation was significantly increased in 60 and 80% BFR external pressure restriction conditions before blood flow restriction training (post-1) compared to pre-2. The activity of the rectus femoris increased significantly only under 80% RFR, suggesting that higher blood pressure restriction can induce a reflex increase in vastus medialis and rectus femoris activation. The results also showed that the vastus lateralis, biceps femoralis, and semitendinosus had similar characteristics of change before and after compression with continuous and intermittent practice under constant external pressure limits and that the vastus lateralis, biceps femoralis, and semitendinosus, interval exercises significantly increased vastus medialis activation. In addition, the results in Table 3 show that the activation of the gluteus maximus was significantly reduced after bandaging. It was comparable to that after bandaging at the end of the treatment and did not return to pre-compression levels after intermittent depressurization. Sun et al. [30] concluded that low-intensity compression and hard pull exercises can increase the activation degree of the distal muscles with limited blood flow and the proximal muscles with no limited synergistic function. This study showed that low-intensity compression squats reduced the activation of the gluteus maximus, suggesting that different compression exercises had different effects on the activation of unrestricted proximal coordination muscles.

Analysis of changes in fatigue degree of thigh muscle groups before and after compression squat exercises

Indicators reflecting muscle fatigue are usually expressed by the MF, and the decrease in the MF value is strongly correlated with the decrease in the swing rate of the muscle bridge [31]. Place et al. [32] confirmed that the degree of intramuscular acidity and the reduction of Ca²⁺ absorption by the sarcoplasmic reticulum are the main factors affecting the decline in muscle contraction function. The results in Table 4 show that the MF values of the rectus femoris, vastus medialis, and vastus lateralis decreased before the end of compression training in both continuous compression mode and intermittent compression mode, and there were significant differences after continuous compression mode. It is suggested that the primary muscle in the front group of the thigh is the main force-generating muscle group, which leads to excessive accumulation of metabolites such as lactic acid in the muscle during the weight-bearing exercise in the continuous pressure mode. This results in acidity changes, reduced Ca²⁺ absorption by the sarcoplasmic reticulum, and ultimately, accelerated muscle fatigue.

After a short rest of 1 min after decompression, the MF values of the three muscles in the front thigh group have recovered to the pre-compression level. This indicates that the functional decline of the muscle caused by the two programs at 50% AOP level is temporary, and it can be restored to the level before compression after a short rest with decompression. In addition, Pierce et al. [15] pointed out that 60%AOP of continuous compression knee extension exercise can cause a significant reduction in the vastus lateralis and rectus femoris’ MF values. Neto et al. [33] also performed a set of 80%1RM high-intensity compression squats with 60%AOP blood pressure limitation, and the results showed that the MF values of the vastus medialis and vastus lateralis decreased by 18.5 and 18.2%, respectively. Previous studies have shown that blood flow restriction training induces fatigue mainly by stimulating protein synthesis of the Akt/mTOR signaling pathway, and the decrease in MF values is sensitive to biochemical changes in type II muscle fibers [34].

Combined with the above results, it can be concluded that neuromuscular fatigue is affected by the intermittent mode and the external pressure-limiting intensity. A higher pressure-limiting intensity will cause greater fatigue and slower recovery speed. In addition, Table 4 shows that the MF values of the biceps femoralis and semitendinosus increased before pressure removal at the end of pressure training in both modes and returned to the level before pressure removal 1 min later. This also suggests that both continuous and intermittent modes of load-bearing compression squat exercise can largely promote the activation of the posterior thigh muscle group, ensure that the neuromuscular component is at a suitable level of excitement, ensure the high synchronization of motor neuron discharge, and then promotes the reflex improvement of contraction force. In addition, the two modes of weight-bearing compression exercise had different effects on muscle fatigue in the unrestricted area. The gluteus maximus MF decreased significantly after continuous compression exercise but recovered shortly after decompression, while intermittent compression exercise had less effect on the gluteus maximus MF. It does not cause fatigue in the gluteus maximus.

Analysis of the change characteristics of the activation degree of lower limb muscle groups in each set of compressive weight-bearing squat exercises

As shown in Fig. 2, anterior thigh muscle group activation was higher during all four sets of compression squats than before the experiment, suggesting that the rectus femoris, vastus medialis, and vastus lateralis were activated to varying degrees during each set of compression. The acidic environment created after the application of pressure stimulation can attract more fast muscle fibers to participate in the activity so that the discharge frequency of fast muscle motor units gradually increases. The RMS value of the rectus femoris in the third and fourth sets was significantly higher than that in the initial set. Vastus medialis RMS values were significantly higher in the second set of continuous mode practice and the third set of intermittent mode practice than at the initial stage (P < 0.05), and the vastus lateralis values were significantly higher in the fourth set of both modes of practice than at the initial stage (P < 0.05). Counts et al. [35] found that the degree of activation of the biceps brachii during an elbow flexion exercise was not affected by external limit blood pressure. High-and low-limit blood pressure had similar adaptive effects on muscle hypertrophy, strength, endurance, and other aspects, but high-limit blood pressure would produce higher discomfort. In addition, Dandel et al. [36] found that adding BFR to interval of high-intensity elbow flexion training could not promote the activation of the biceps brachii and cause muscle hypertrophy. It has been suggested that blood flow restriction during low-intensity squat exercises can promote muscle activation and cause a hypertrophic response. The results of this study, similarly to previous studies, showed that continuous and intermittent exercises of the upper and lower extremities with moderate intensity blood pressure limitation could effectively improve the activation degree of the prime muscle and reduce discomfort.

Figure 2 shows that biceps femoralis and semitendinosus activation was significantly higher in the third and fourth sets than at the beginning of the weight-bearing exercises. However, activation of the gluteus maximus increased in the first set. Activation in the second, third, and fourth sets gradually declined, indicating that both continuous and intermittent blood flow restriction training will not only improve the thigh before the group of the original dynamic degree of muscle activation, but also improve the state of no pressure and rarely participate in and mobilization of the stocks after the muscle group, such as antagonist muscle activation degree. This can improve the thigh muscle group compared to flexion and extension and help prevent sports injuries. In addition, Abe et al. used 20% 1RM for compression squats, believing that, due to the low training intensity and the unrestricted position of the gluteus maximus, such load would not cause gluteus maximus hypertrophy [37]. However, there may be synergies between the thigh and buttocks in squat exercises. This study showed that the gluteus maximus was complementary, and its activation increased significantly when the anterior thigh group was relatively low during pressure exercise. In the second, third, and fourth exercise sets, the activity of the anterior thigh muscles gradually increased, while the activity of the gluteus maximus gradually decreased. This may be because the gluteus maximus extends the hip while the quadriceps muscle mainly extends the knee. The two muscles may be complementary in function to some extent as the adjacent active muscles of the important lower limb motor chain and the gluteus maximus may recruit more motion units to supplement the quadriceps deficit. This demonstrates that 50% AOP compression during weight-bearing squat training can induce more significant muscle group activation in the front and back of the legs, while gluteus maximus stimulation was not significant for hip extension. The authors believe that the main reason is that the compression site mainly plays a major role in lower limb blood flow occlusion but has little effect on the gluteal muscle. At the same time, lightweight squatting exercises may not significantly affect the gluteus maximus, and further extensive hip extension or increased weight-bearing strength to 85% or more may induce greater gluteus maximus activation.

Conclusions

In 50% AOP compression squats under 30% 1RM, the acute activation of thigh muscle groups was different between continuous compression interval training and decompression interval training. The degree of of thigh muscle groups activation induced was greater in continuous compression interval training than in decompression interval training. RMS values of all muscle groups except the vastus medialis increased significantly after training in the third and fourth sets, but fatigue also occurred. In contrast, although the intermittent mode of pressure removal produces fatigue, recovery is faster. Therefore, the use of a continuous pressure training mode is recommended for trained athletes and an intermittent pressure training mode for beginners.

Abbreviations

1RM, one-repetition maximum; %AOP, percentage of arterial occlusion pressure; ANOVA, analysis of variance; BFR, blood flow restriction; EMG, electromyography; MF, median frequency: MVC, maximum voluntary contraction; RMS, root mean square; RMS_MVC, RMS value under MVC.

Declarations

Ethics approval and consent to participate

The study was approved by Fuzhou University Human Research Ethics Committee (LLWYH20200269) and all aspects of the study were conducted in agreement with the Declaration of Helsinki. All of the participants were fully informed about the purpose and experimental procedures of the study. Informed consent was obtained prior written from each participant. The participants were informed that all data collected would be processed anonymously.

Consent for publication

All participants were informed about the experimental nature of the study and gave their written informed consent for the publication of relevant data.

Availability of data and materials

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

No funding was linked to the undertaking of this research.

Authors' contributions

YW, ZL, and TC conceived and designed research. TC and ZL conducted experiments and facilitated the data collection. YW undertook the data analysis and drafted the manuscript. YW completed the writing of the manuscript. YW, ZL, and TC reviewed and provided comments on the manuscript. All authors read and approved the final manuscript.

Acknowledgments

The authors would like to acknowledge and thank all the participants for their time and contribution to the present study.

References

1. Hatfield DL, Kraemer WJ, Volek JS, Nindl BC, Caldwell LK, Vingren JL, et al. Hormonal stress responses of growth hormone and insulin-like growth factor-I in highly resistance trained women and men. Growth Horm IGF Res. 2021;59:101407.
2. Centner C, Wiegel P, Gollhofer A, König D. Effects of Blood flow restriction training on muscular strength and hypertrophy in older individuals: A systematic review and meta-analysis. Sports Med. 2019;49:95–108.
3. Sheng JJ, Wei WZ, Sun K, Zhao ZG. Physiological load and effect on muscle hypertrophy of slow downhill walking with Kaatsu. China Sport Science and Technology. 2019;55:13–19. (in Chinese)
4. Patterson SD, Hughes L, Warmington S, Burr J, Scott BR, Owens J, et al. Blood flow restriction exercise: Considerations of methodology, application, and safety. Front Physiol. 2019;10:533.
5. Shen L, Li J, Chen Y, Lu Z, Lyu W. L-carnitine's role in Kaatsu training-induced neuromuscular fatigue. Biomed Pharmacother. 2020;125:109899.
6. Ogawa H, Nakajima T, Shibasaki I, Nasuno T, Kaneda H, Katayanagi S, et al. Low-intensity resistance training with moderate blood flow restriction appears safe and increases skeletal muscle strength and size in cardiovascular surgery patients: A pilot study. J Clin Med. 2021;10:547.
7. Wilk M, Krzysztofik M, Gepfert M, Poprzecki S, Gołaś A, Maszczyk A. Technical and training related aspects of resistance training using blood flow restriction in competitive sport - A review. J Hum Kinet. 2018;65:249–60.
8. Benito PJ, Cupeiro R, Ramos-Campo DJ, Alcaraz PE, Rubio-Arias JÁ. A systematic review with meta-analysis of the effect of resistance training on whole-body muscle growth in healthy adult males. Int J Environ Res Public Health. 2020;17:E1285.
9. Chen NJ. The effect of 6-week hypobaric resistance training on muscle recruitment and PAP in sprint athletes. Beijing: Beijing Sport University; 2018 (in Chinese)
10. Wilk M, Trybulski R, Krzysztofik M, Wojdala G, Campos Y, Zajac A, et al. Acute effects of different blood flow restriction protocols on bar velocity during the squat exercise. Front Physiol. 2021;12:652896.
11. Fahs CA, Loenneke JP, Thiebaud RS, Rossow LM, Kim D, Abe T, et al. Muscular adaptations to fatiguing exercise with and without blood flow restriction. Clin Physiol Funct Imaging. 2015;35:167–76.
12. Yoshiaki Sato, Naokata Ishii, Toshiaki Nakajima. Kaatsu training theoretical and practical prespectives. Tokyo: kodansha; 2008. (in Japanese)
13. Shinohara M, Kouzaki M, Yoshihisa T, Fukunaga T. Efficacy of tourniquet ischemia for strength training with low resistance. Eur J Appl Physiol Occup Physiol. 1998;77:189–91.
14. Moore DR, Burgomaster KA, Schofield LM, Gibala MJ, Sale DG, Phillips SM. Neuromuscular adaptations in human muscle following low intensity resistance training with vascular occlusion. Eur J Appl Physiol. 2004;92:399–406.
15. Pierce JR, Clark BC, Ploutz-Snyder LL, Kanaley JA. Growth hormone and muscle function responses to skeletal muscle ischemia. J Appl Physiol (1985). 2006;101:1588-95.
16. Abe T, Fujita S, Nakajima T, Sakamaki M, Ozaki H, Ogasawara R, et al. Effects of low-intensity cycle training with restricted leg blood flow on thigh muscle volume and VO2MAX in young men. J Sports Sci Med. 2010;9:452–8.
17. Yasuda T, Fujita T, Miyagi Y, Kubota Y, Sato Y, Nakajima T, et al. Electromyographic responses of arm and chest muscle during bench press exercise with and without Kaatsu. Int J Kaatsu Training Res. 2006;2:15–18.
18. Loenneke JP, Fahs CA, Rossow LM, Sherk VD, Thiebaud RS, Abe T, et al. Effects of cuff width on arterial occlusion: implications for blood flow restricted exercise. Eur J Appl Physiol. 2012;112:2903–12.
19. Laurentino G, Ugrinowitsch C, Aihara AY, Fernandes AR, Parcell AC, Ricard M, et al. Effects of strength training and vascular occlusion. Int J Sports Med. 2008;29:664–7.
20. Loenneke JP, Kim D, Fahs CA, Thiebaud RS, Abe T, Larson RD, et al. Effects of exercise with and without different degrees of blood flow restriction on torque and muscle activation. Muscle Nerve. 2015;51:713–21.
21. Li ZY, Yu SK, Li JP, Li YZ. Effect of different arterial occlusion pressure and intermittent mode on Kaatsu-loaded deepï¼࿽squat exercise on the characteristics of thigh muscle activation. Chin J App Physiol. 2021;37:300–304. (in Chinese)
22. Hiraizumi Y, Nakajima T, Imanishi T, Sato Y. Muscle and muscle enhancement training: Kaatsu training. Jpn J Rehabil Med. 2017;54:768–775. (in Japanese)
23. Yan Q, Liao T, Zhang YJ. Digital-based performance training: Concepts, advances and applications. China Sport Science. 2018;38:3–16. (in Chinese)
24. Jovanović M, Flanagan EP. 2014. Researched applications of velocity based strength training. J Aust Strength Cond. 2014;22:58–69.
25. Konrad P. The ABC of EMG: A Practical Introduction to Kinesiological Electromyography. Version 1.0. USA: Noraxon INC; 1998.
26. Umbel JD, Hoffman RL, Dearth DJ, Chleboun GS, Manini TM, Clark BC. Delayed-onset muscle soreness induced by low-load blood flow-restricted exercise. Eur J Appl Physiol. 2009;107:687–95.
27. Fatela P, Reis JF, Mendonca GV, Avela J, Mil-Homens P. Acute effects of exercise under different levels of blood-flow restriction on muscle activation and fatigue. Eur J Appl Physiol. 2016;116:985–95.
28. Yasuda T, Brechue WF, Fujita T, Shirakawa J, Sato Y, Abe T. Muscle activation during low-intensity muscle contractions with restricted blood flow. J Sports Sci. 2009;27:479–89.
29. 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). 2000;88:2097 – 106.
30. Sun K, Wei WZ, Zhao ZG. The difference of muscle activity between the blood flow restricted part and the unrestricted part in low-intensity Kaatsu training on lower limbs. China Sport Science and Technology. 2019;55:14–19. (in Chinese)
31. Eberstein A, Beattie B. Simultaneous measurement of muscle conduction velocity and EMG power spectrum changes during fatigue. Muscle Nerve. 1985;8:768–73.
32. Place N, Bruton JD, Westerblad H. Mechanisms of fatigue induced by isometric contractions in exercising humans and in mouse isolated single muscle fibres. Clin Exp Pharmacol Physiol. 2009;36:334–9.
33. Neto GR, Santos HH, Sousa JB, Júnior AT, Araújo JP, Aniceto RR, et al. Effects of high-intensity blood flow restriction exercise on muscle fatigue. J Hum Kinet. 2014;41:163–72.
34. Loenneke JP, Wilson GJ, Wilson JM. A mechanistic approach to blood flow occlusion. Int J Sports Med. 2010;31:1–4.
35. Counts BR, Dankel SJ, Barnett BE, Kim D, Mouser JG, Allen KM, et al. Influence of relative blood flow restriction pressure on muscle activation and muscle adaptation. Muscle Nerve. 2016;53:438–45.
36. Dankel SJ, Buckner SL, Jessee MB, Mattocks KT, Mouser JG, Counts BR, et al. Can blood flow restriction augment muscle activation during high-load training. Clin Physiol Funct Imaging. 2018;38:291–5.
37. Abe T, Yasuda T, Midorikawa T, Sato Y. Skeletal muscle size and circulating IGF-1 are increased after two weeks of twice daily “Kaatsu” resistance training. Int J Kaatsu Training Res. 2005;1:6–12.