You are on page 1of 5

Available online at www.sciencedirect.

com

Journal of Science and Medicine in Sport 14 (2011) 95–99

Original paper

Blood flow restriction by low compressive force prevents disuse


muscular weakness
Atsushi Kubota a,∗ , Keishoku Sakuraba a,b , Sadao Koh c , Yuji Ogura d , Yoshifumi Tamura e
a Sportology Center, Juntendo University, Tokyo, Japan
bDepartment of Sports Medicine, School of Health and Sports Science, Juntendo University, Chiba, Japan
c Koh Orthopaedic Clinic, Saitama, Japan
d Department of Physiology, St. Marianna University School of Medicine, Kanagawa, Japan
e Department of Medicine, Metabolism and Endocrinology, School of Medicine, Juntendo University, Tokyo, Japan
Received 8 December 2009; received in revised form 9 August 2010; accepted 19 August 2010

Abstract
Repetitive blood flow restriction prevents muscular atrophy and weakness induced by chronic unloading. However, it was unclear which
external compressive force for blood flow restriction was optimal to prevent muscular dysfunction. The present study was intended to investigate
the effects of repeated muscle blood flow restriction at low pressure on muscular weakness induced by immobilization without weight bearing.
Using casts, the left ankles of 11 healthy males were immobilized for 2 weeks. Subjects were instructed to walk using crutches with no weight
bearing during the period. Subjects were divided randomly into two groups: a restriction of blood flow (RBF) group (application of external
compressive force of 50 mm Hg) and a control (CON) group (no intervention). We measured changes in the muscle strength of the knee
extensor–flexor and ankle plantar flexor. The percent changes in knee extensor torque at 60◦ /s under eccentric contraction in the RBF group
were significantly smaller than in the CON group (−12.5 ± 10.7% and −30.1 ± 10.9%, p < 0.05). The percent changes in knee flexor torque
when performing an eccentric contraction at 60◦ /s, an isometric contraction, or a concentric contraction at both 60 and 300◦ /s in the RBF
group were significantly smaller than those in the CON group (p < 0.05). In conclusion, our results show that repetitive restriction of blood
flow with 50 mm Hg cuff pressure to the lower extremity reduces muscular weakness induced by chronic unloading.
© 2010 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.

Keywords: Skeletal unloading; Muscular atrophy; Muscle strength; Immobilization; Weightlessness

1. Introduction ventive effect against muscle atrophy and weakness induced


by disuse.
Chronic unloading resulting from space flight,1–4 bed It remains unclear how blood flow restriction prevents
rest,5–9 and immobilization10–13 induces muscular atrophy muscle dysfunction induced by chronic unloading. The effect
and reduces muscle strength. It has been demonstrated that of resistance training was ameliorated when it was combined
resistance training prevents disuse muscle atrophy.14–16 We with blood flow restriction.17–20 Therefore, it is hypothesized
showed in an earlier study that repetitive blood flow restric- that the intramuscular accumulation of phosphate metabolites
tion during a 2-week immobilization and non-weight bearing and hydrogen ions influence the hypertrophic effects of con-
period prevents muscle weakness and atrophy.16 The pre- tinuous muscle contraction.21 Data obtained from our earlier
ventive effects were more pronounced than those achieved study16 suggest that blood flow restriction with 200 mm Hg
through isometric training and the results of that study suggest cuff pressure prevents disuse muscle atrophy. Based on
that blood flow restriction, like resistance training, has a pre- those results, it is hypothesized that intramuscular metabolic
changes induced by ischemia prevent muscle atrophy induced
∗ Corresponding author at: Department of Sports Medicine, School of by chronic unloading.16 Furthermore, the previous study22
Health and Sports Science, Juntendo University, Chiba, Japan. showed that the effects of resistance exercise with blood
E-mail address: akubota@juntendo.ac.jp (A. Kubota). flow restriction, even the application of lower cuff pressure

1440-2440/$ – see front matter © 2010 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jsams.2010.08.007
96 A. Kubota et al. / Journal of Science and Medicine in Sport 14 (2011) 95–99

(50 mm Hg), significantly increased muscle strength. There- sured with the second derivative plethysmograph (Fukuda
fore, it is assumed that repetitive blood flow restriction per se Denshi Co. Ltd., Tokyo) during the application of external
(without any exercise) with 50 mm Hg cuff pressure prevents compression of 50, 100, 200 and 300 mm Hg was reduced
disuse atrophy. The present study was designed to investi- to 90.0 ± 23.1, 80.9 ± 26.4, 64.2 ± 26.3, 2.6 ± 7.3%, respec-
gate the effects of repeated muscle blood flow restriction at tively (n = 8). At the end of the 2-week period, muscle strength
low pressure (50 mm Hg) on muscular weakness induced by was measured again.
immobilization and non-weight bearing. The knee extensor–flexor torque under isokinetic and iso-
metric contraction and the ankle plantar flexor torques under
isokinetic contraction were measured quantitatively using an
2. Methods apparatus that determines isokinetic muscle strength (System
3 Dynamometer; Biodex Medical Systems, Shirley, NY).
Subjects were 11 healthy untrained males without a his- To determine the knee extensor–flexor torque, subjects
tory of injuries to the lower extremities or serious medical were seated; the measured femoral region and upper part of
complaints. This study was approved by the Human Ethics the subject were constrained using 1–3 belts. The subject
Committee of Juntendo University. Prior to the experiment, extended and flexed the knee joints 3 or 5 times at an angular
the purpose of the study, contents, experimental protocol, speed of 60, 180, or 300◦ /s using a concentric contraction
possible risk involved, and management or security offered (CC60, CC180, and CC300), and at angular speeds of 60 and
if an accident occurs were fully explained to these subjects. 180◦ /s using an eccentric contraction (EC60 and EC180). Iso-
Their consent in writing was obtained. metric contractions were performed with the knee joint flexed
We investigated the effect of blood flow restriction by at an angle of 60◦ (IM). The subject continued extending or
application of external compressive forces of 50 mm Hg on flexing the knee joints for 5 s with a 10-s break between knee
muscular weakness. For each subject, we measured muscle extension and flexion. Following determination of the ankle
strength and the circumference of the lower extremity at base- plantar flexor torque, the subject lay in a supine position and
line (before intervention). The muscle strength of the lower the measurement limbs were fastened with a belt. The sub-
extremities was measured as the torque of the knee and ankle ject then extended and flexed the ankle joints three times at
joints performing an isokinetic contraction. Details of these CC60, CC120, EC60, and EC120.
measurements are described in the Measurement of muscle All data were expressed as mean ± SD. Differences in
strength section. muscle strength at each angular speed and contraction pattern,
To determine changes in the volume of thigh and leg mus- and circumference, before and after the intervention were
cles, we measured the circumference of the thigh region at statistically analyzed using a paired t-test in the RBF and
10 and 15 cm above the upper border of the patella (thigh 10 CON groups respectively. In addition, percent changes cal-
and 15) and the maximum circumference of the leg using a culated from the muscle strength and circumference before
tape while the subject was standing (n = 5 in the RBF group, and after the intervention were tested using an unpaired t-test
n = 5 in the CON group). The measurements of each region between the RBF and CON groups. All p values less than
were performed three times and the average values were used 0.05 were inferred as demonstrating a statistically significant
for analysis. difference.
For 2 weeks after all measurements, to induce muscu-
lar weakness, the left ankle joint of subjects was fixated
at the neutral position (ankle joint angle = 0◦ ) using a cast. 3. Results
Subjects were required to use crutches to move without
weight bearing. Subjects were then divided randomly into Table 1 shows the knee extensor–flexor muscle strength
two groups: subjects who received repetitive blood flow before and after 2 weeks of immobilization without weight
restriction with compressive force of 50 mm Hg (RBF group, bearing. Almost all muscle strength values had decreased
n = 5, age: 22.8 ± 0.8 year, height: 174.2 ± 5.9 cm, weight: significantly in the CON after the protocol, while several mus-
68.0 ± 3.7 kg) and subjects for whom blood flow was not cle strength values in the RBF group showed no significant
restricted (control group, CON group, n = 6, age: 22.8 ± 1.2 protection against such changes in muscle strength for both
year, height: 174.8 ± 3.9 cm, weight: 70.3 ± 5.0 kg). During the knee extensor and flexor muscles. The percent changes
the 2-week period, blood flow to the lower left extremity in knee extensor torque showed significant differences in
was restricted by compressing the proximal end of the thigh EC60 and knee flexor torques in EC60, IM, CC60, and
using a tourniquet (77 mm width, 770 mm length, MIZUHO CC300. Fig. 1 shows that the percent changes in knee extensor
Co. Ltd., Tokyo) in subjects of the RBF group. A set consisted torque at EC60 in the RBF group were significantly smaller
of 5 min of applied blood flow restriction followed by 3 min than in the CON group (−12.5 ± 10.7% and −30.1 ± 10.9%,
of rest (release of compression); each subject underwent five p = 0.025). Fig. 2 portrays that the percentage changes in
sets twice a day (morning and afternoon) for 14 days. Our pre- knee flexor torques at EC60, IM, CC60 and CC300 in the
liminary data demonstrated that compared with the control RBF group were significantly smaller than those in the CON
(before compression), the pulse wave velocity (PWV) mea- group: EC60 (−3.5 ± 4.7% and −18.9 ± 9.6%, p = 0.0095),
A. Kubota et al. / Journal of Science and Medicine in Sport 14 (2011) 95–99 97

Data are mean ± SD. EC180, 180◦ /s under eccentric contraction; EC60, 60◦ /s under eccentric contraction; IM, isometric contraction; CC60, 60◦ /s under concentric contraction; CC180, 180◦ /s under concentric
73.7 ± 18.2*
112.8 ± 24.7

121.6 ± 25.0
92.1 ± 11.6
Post
125.4 ± 24.0
87.5 ± 20.9

127.5 ± 18.2
95.7 ± 12.2
CC300 (N m)

Pre
Knee extensor–flexor torques at baseline and after a 2-week immobilization and non-weight bearing period combined with blood flow restriction (RBF) and no intervention (CON).

Fig. 1. Percent changes in knee extensor torque after a 2-week immobi-


138.4 ± 28.5*
82.9 ± 17.7

143.5 ± 28.4
99.5 ± 10.1
lization and non-weight bearing period, relative to baseline, combined with
blood flow restriction or no intervention. Data are mean ± SD. *p < 0.05.
EC180, 180◦ /s under eccentric contraction; EC60, 60◦ /s under eccentric
Post

contraction; IM, isometric contraction; CC60, 60◦ /s under concentric con-


traction; CC180, 180◦ /s under concentric contraction; CC300, 300◦ /s under
156.8 ± 28.2
99.3 ± 20.4

162.2 ± 21.4
101.0 ± 10.6
CC180 (N m)

concentric contraction.

IM (−3.7 ± 5.8% and −20.9 ± 13.7%, p = 0.029), CC60


Pre

(−6.9 ± 2.9% and −18.6 ± 11.0%, p = 0.047) and CC300


(−3.6 ± 4.6% and −15.4 ± 9.1%, p = 0.029).
172.3 ± 29.9**
105.4 ± 23.3*

195.9 ± 18.4*
123.8 ± 9.3*

All muscle strength values of the ankle plantar flexor


muscles had decreased significantly in the CON group
Post

after the protocol: EC120 (pre: 122.6 ± 27.3 N m and post:


104.1 ± 28.7 N m, p = 0.032), EC60 (pre: 133.1 ± 27.0 N m
222.5 ± 45.6
130.7 ± 30.0

234.6 ± 17.3
133.3 ± 13.7
CC60 (N m)

and post: 110.8 ± 18.5 N m, p = 0.004), CC60 (pre:


79.9 ± 18.3 N m and post: 59.5 ± 21.8 N m, p = 0.008) and
CC120 (pre: 57.2 ± 10.2 N m and post: 44.7 ± 13.7 N m,
Pre

p = 0.005). In the RBF group, the muscle strength value in


184.6 ± 26.3***
92.3 ± 17.4*

244.3 ± 20.6*
119.2 ± 17.8

CC60 had decreased significantly after the protocol (pre:


87.2 ± 15.5 N m and post: 68.0 ± 16.5 N m, p = 0.005), but
Post

RBF partially protected against such changes in muscle


strength. Specifically, the percentage change in ankle plantar
239.0 ± 38.9
117.8 ± 21.4

295.3 ± 11.6
124.0 ± 18.2

flexor torque at EC60 in the RBF group was significantly


less than that of the CON group (−0.2 ± 12.1% and
IM (N m)

−16.1 ± 6.3%, p = 0.020).


Pre

All circumferences of the lower extremities had decreased


143.5 ± 36.3**

significantly in the CON group after the protocol: thigh 10


203.3 ± 27.7*

309.9 ± 40.5
183.8 ± 27.3

(pre: 48.5 ± 2.8 cm and post: 47.2 ± 2.7 cm, p = 0.013), thigh
15 (pre: 52.6 ± 3.5 cm and post: 51.1 ± 2.9 cm, p = 0.012)
Post

and leg (pre: 38.5 ± 2.0 and post: 37.5 ± 2.1, p = 0.007).
In the RBF group, the circumferences in thigh 15 and leg
301.6 ± 92.6
177.3 ± 40.7

354.1 ± 11.2
190.1 ± 23.5
EC60 (N m)

had decreased significantly after the protocol: thigh 10 (pre:


contraction; CC300, 300◦ /s under concentric contraction.
Pre
185.7 ± 26.8**

247.2 ± 28.9**
140.6 ± 37.9*

171.4 ± 37.2
Post
255.7 ± 65.7
173.9 ± 39.7

321.3 ± 41.4
190.3 ± 22.8
EC180 (N m)

Pre

Fig. 2. Percent changes in knee flexor torque after a 2-week immobiliza-


tion and non-weight bearing period, relative to baseline, combined with
Extensor

Extensor

blood flow restriction or no intervention. Data are mean ± SD. *p < 0.05,
Flexor

Flexor

*** p < 0.001.


* p < 0.05.
** p < 0.01.

**p < 0.01. EC180, 180◦ /s under eccentric contraction; EC60, 60◦ /s under
eccentric contraction; IM, isometric contraction; CC60, 60◦ /s under con-
Table 1

Group

centric contraction; CC180, 180◦ /s under concentric contraction; CC300,


CON

RBF

300◦ /s under concentric contraction.


98 A. Kubota et al. / Journal of Science and Medicine in Sport 14 (2011) 95–99

48.2 ± 1.0 cm and post: 47.2 ± 1.2 cm, p = 0.051), thigh 15 underlying mechanisms of the effects of blood flow restric-
(pre: 52.3 ± 1.2 cm and post: 51.5 ± 1.6 cm, p = 0.045) and tion.
leg (pre: 37.5 ± 1.5 cm and post: 36.8 ± 1.6 cm, p = 0.005). In Results of this study did not clarify whether muscle
addition, the differences between the RBF and CON groups atrophy was prevented by blood flow restriction. We only
were not significant for all percent changes of circumfer- measured the respective circumferences of thigh and leg and
ences. the data suggest that the circumferences of those muscles
were significantly but similarly decreased in both groups.
Therefore, it seems that a low cuff pressure program, in con-
4. Discussion trast to the high pressure program,16,24 might not be effective
for preventing muscle atrophy induced by chronic unloading.
The main finding of this study is that repeated muscle Interestingly, muscle weakness was predominantly prevented
blood flow restriction at low pressure (50 mm Hg) mitigated in knee flexor muscles, which suggests that a muscle specific
muscular weakness induced by immobilization and non- effect can occur by blood flow restriction, thereby necessi-
weight bearing. This result suggests that mild blood flow tating direct measurement (CT or MRI) to measure muscle
restriction, achieved by 50 mm Hg cuff pressure, has a mild atrophy more precisely. In addition, it has been reported
preventive effect on muscular atrophy and weakness induced that the maximum force production is directly dependent
by chronic unloading. on muscle cross-sectional area.25 It is also generally known
We observed partial reduction of muscle weakness by that neuromuscular coordination plays an intimate role in
blood flow restriction with low cuff pressure (50 mm Hg). the expression of muscle strength. These factors might con-
Comparison with data from our previous report shows that tribute to the inconsistent results between muscle weakness
a 50 mm Hg cuff pressure program has a milder effect on and atrophy in the present study.
muscle weakness induced by chronic unloading than the
200 mm Hg cuff pressure program. Our previous study using
the same weight-bearing protocol described that less than 5. Conclusion
a 5% decrease of muscle strength was observed in the
200 mm Hg cuff pressure group, although 10–25% reduction The repetitive restriction of blood flow with 50 mm Hg
was observed in the control group.16 In the present study, cuff pressure to the lower extremity partially prevents
50 mm Hg cuff pressure had a preventive effect against the muscular weakness induced by chronic unloading. Further
knee flexor muscle strength decrease, in agreement with the investigation is necessary to clarify the underlying mecha-
results of our previous study,16 but only a slight effect was nisms of the anti-atrophic effects of blood flow restriction.
observed in the knee extensor muscle strength (Fig. 1). The
PWV data suggest that 50 mm Hg cuff pressure has a smaller
effect on arterial blood flow than 200 mm Hg cuff pressure. Practical implications
Therefore, the level of blood flow restriction might be an
important factor to prevent muscle weakness by repetitive • Blood flow restriction is a potential measures to pre-
blood flow restriction, especially in the knee extensor muscle. vent muscle atrophy and weakness induced by chronic
It remains unclear how blood flow restriction with unloading such as that which occurs as bed rest and cast
50 mm Hg cuff pressure prevents muscle weakness induced immobilization.
by chronic unloading. It has been reported that hemodynamic • Blood flow restriction may also be used as a medical treat-
responses to the blood flow restriction were less observed ment in the rehabilitation of sports injury.
in 50 mm Hg cuff pressure compared with 200 mm Hg cuff • The positive effect of blood flow restriction on the muscle
pressure.23 Because 50 mm Hg is lower than the arterial weakness depends on the external compressive force.
blood pressure, but higher than the venous blood pressure,
50 mm Hg cuff pressure might induce venous congestion in
lower extremities. This congestion might have some roles References
to diminish muscle dysfunction. It has been reported that
the accumulation of intramuscular phosphate metabolites 1. Akima H, Kawakami Y, Kubo K, et al. Effect of short-duration of
and hydrogen ions influence the hypertrophic effects of spaceflight on thigh and leg muscle volume. Med Sci Sports Exerc
2000;32(10):1743–7.
continuous muscle contraction.21 Consequently, blood flow 2. Edgerton VR, Zhou MY, Ohira Y, et al. Human fiber size and enzy-
restriction with 50 mm Hg cuff pressure might prevent mus- matic properties after 5 and 11 days of spaceflight. J Appl Physiol
cle weakness through those underlying mechanisms.21,24 In 1995;78(5):1733–9.
addition, the different effects of 50 mm Hg cuff pressure and 3. LeBlanc A, Rowe R, Schneider V, et al. Regional muscle loss after
short duration spaceflight. Aviat Space Environ Med 1995;66(12):
200 mm Hg cuff pressure programs are also explained by this
1151–4.
hypothesis because the PWV data suggest that 50 mm Hg cuff 4. Widrick JJ, Knuth ST, Norenberg KM, et al. Effect of a 17 day space-
pressure had less effect on arterial blood flow than 200 mm Hg flight on contractile properties of human soleus muscle fibres. J Physiol
cuff pressure. Further studies are necessary to clarify the 1999;516(Pt. 3):915–30.
A. Kubota et al. / Journal of Science and Medicine in Sport 14 (2011) 95–99 99

5. Berg HE, Larsson L, Tesch PA. Lower limb skeletal muscle function 16. Kubota A, Sakuraba K, Sawaki K, et al. Prevention of disuse mus-
after 6 wk of bed rest. J Appl Physiol 1997;82(1):182–8. cular weakness by restriction of blood flow. Med Sci Sports Exerc
6. Bloomfield SA. Changes in musculoskeletal structure and function 2008;40(3):529–34.
with prolonged bed rest. Med Sci Sports Exerc 1997;29(2):197– 17. Abe T, Kearns CF, Sato Y. Muscle size and strength are increased fol-
206. lowing walk training with restricted venous blood flow from the leg
7. Ferrando AA, Stuart CA, Brunder DG, et al. Magnetic resonance imag- muscle, Kaatsu-walk training. J Appl Physiol 2006;100(5):1460–6.
ing quantitation of changes in muscle volume during 7 days of strict 18. Clark BC, Fernhall B, Ploutz-Snyder LL. Adaptations in human neuro-
bed rest. Aviat Space Environ Med 1995;66(10):976–81. muscular function following prolonged unweighting. I. Skeletal muscle
8. LeBlanc AD, Schneider VS, Evans HJ, et al. Regional changes contractile properties and applied ischemia efficacy. J Appl Physiol
in muscle mass following 17 weeks of bed rest. J Appl Physiol 2006;101(1):256–63.
1992;73(5):2172–8. 19. Takarada Y, Takazawa H, Sato Y, et al. Effects of resistance exercise
9. Trappe S, Trappe T, Gallagher P, et al. Human single muscle fibre func- combined with moderate vascular occlusion on muscular function in
tion with 84 day bed-rest and resistance exercise. J Physiol 2004;557(Pt. humans. J Appl Physiol 2000;88(16):2097–106.
2):501–13. 20. Takarada Y, Tsuruta T, Ishii N. Cooperative effects of exercise
10. Booth FW. Effect of limb immobilization on skeletal muscle. J Appl and occlusive stimuli on muscular function in low-intensity resis-
Physiol 1982;52(5):1113–8. tance exercise with moderate vascular occlusion. Jpn J Physiol
11. Hortobágyi T, Dempsey L, Fraser D, et al. Changes in muscle strength, 2004;54(6):585–92.
muscle fibre size and myofibrillar gene expression after immobilization 21. Schott J, McCully K, Rutherford OM. The role of metabolites in
and retraining in humans. J Physiol 2000;524(Pt. 1):293–304. strength training. II. Short versus long isometric contractions. Eur J
12. Stevens JE, Pathare NC, Tillman SM, et al. Relative contributions Appl Physiol Occup Physiol 1995;71(4):337–41.
of muscle activation and muscle size to plantarflexor torque during 22. Sumide T, Sakuraba K, Sawaki K, et al. Effect of resistance exercise
rehabilitation after immobilization. J Orthop Res 2006;24(8):1729– training combined with relatively low vascular occlusion. J Sci Med
36. Sport 2009;12(1):107–12.
13. Yasuda N, Glorer EI, Phillips SM, et al. Sex-based differences in 23. Iida H, Kurano M, Takano H, et al. Hemodynamic and neurohumoral
skeletal muscle function and morphology with short-term limb immo- responses to the restriction of femoral blood flow by KAATSU in
bilization. J Appl Physiol 2005;99(3):1085–92. healthy subjects. Eur J Appl Physiol 2007;100(3):275–85.
14. Akima H, Kubo K, Kanehisa H, et al. Leg-press resistance training 24. Takarada Y, Takazawa H, Ishii N. Applications of vascular occlusion
during 20 days of 6 degrees head-down tilt bed rest prevents muscle diminish disuse atrophy of knee extensor muscles. Med Sci Sports Exerc
deconditioning. Eur J Appl Physiol 2000;82(1–2):30–8. 2000;32(12):2035–9.
15. Germain P, Güell A, Marini JF. Muscle strength during bedrest with 25. Schantz P, Randall-Fox E, Hutchison W, et al. Muscle fibre type distri-
and without muscle exercise as a countermeasure. Eur J Appl Physiol bution, muscle cross-sectional area and maximal voluntary strength in
Occup Physiol 1995;71(4):342–8. humans. Acta Physiol Scand 1983;117(2):219–26.

You might also like