Training & Testing
481
Author
K. Kubo
Affiliation
Life Science (Sports Sciences), University of Tokyo, Tokyo, Japan
Key words
▶ blood volume
●
▶ oxygen saturation
●
▶tendon
●
▶human
●
Abstract
▼
Previous studies demonstrated that treatment
involving eccentric training was effective in the
conservative management of chronic tendinosis.
However, the mechanisms for these phenomena
are unknown. The purpose of this study was to
compare changes in blood circulation of the tendons after the repeated concentric and eccentric
contractions. 11 healthy males volunteered for
this study. Subjects performed the repeated concentric (CON) and eccentric (ECC) contractions (5
sets of 10 maximal voluntary contractions) of the
Introduction
▼
accepted after revision November 14, 2014
Bibliography
DOI http://dx.doi.org/
10.1055/s-0034-1398649
Published online:
March 3, 2015
Int J Sports Med 2015; 36:
481–484 © Georg Thieme
Verlag KG Stuttgart · New York
ISSN 0172-4622
Correspondence
Dr. Keitaro Kubo
Life Science (Sports Sciences)
University of Tokyo
Komaba 3-8-1
Meguro
Tokyo
Japan 153-8902
Tel.: + 81/3/5454 6860
Fax: + 81/3/5454 4317
[email protected]
Tendon injuries from overuse are a major problem among recreational and competitive athletes. Previous studies have shown that treatment
involving eccentric training has been effective in
the conservative management of chronic tendinosis [1, 10, 19, 21]. Furthermore, nonsurgical
treatment with eccentric training reduced the
need for surgical treatment for patients with
chronic tendinosis. For example, Mafi et al. [19]
reported that after the eccentric training regimen 82 % of the patients were satisfied and had
resumed their previous activity level, compared
to 36 % of the patients who were treated with the
concentric training regimen. However, the mechanisms for the efficacy of eccentric training
involved in physiologic tendon response to
eccentric loading are unknown.
It is known that tendon injuries and disorders
have been associated with disturbances in tendon vasculature [7]. These changes within the
tendons may result in the decline of blood circulation and collagen synthesis. Therefore, the
injured tendons require ample supply of blood
for their restoration and treatment [2, 8]. On the
other hand, previous studies demonstrated that
the muscle activation level and energy cost were
plantar flexors. During and after repeated contractions, oxyhemoglobin (Oxy), deoxyhemoglobin
(Deoxy), total hemoglobin (THb), and oxygen saturation (StO2) of the Achilles tendons were measured using red laser lights. Oxy and THb increased
during and after ECC, but not CON. Deoxy
decreased during both CON and ECC. Increase in
StO2 during and after ECC was greater than that
during and after CON. These results suggested that
changes in blood circulation of the Achilles tendon
during and after repeated eccentric contractions
were more remarkable than those during and
after repeated concentric contractions.
lower for eccentric contractions than concentric
contractions, although the exerted force level
during eccentric contractions was higher than
that during concentric contractions [3, 22]. At
present, however, we cannot say for certain
whether these characteristics of eccentric contractions affect blood circulation of tendons.
Recently, we measured blood circulation (blood
volume and oxygen saturation) in human tendons using 3 red laser lights [12–15]. With this
technique, we found that changes in blood circulation of tendons were different among the different contraction modes. We reported that
blood volume of the patellar tendon did not
change after 3 months of isometric knee extension training, although it increased significantly
after dynamic training [15]. Considering these
findings, changes in blood circulation of the tendons after eccentric training would be remarkable compared to other contraction mode
regimens.
In the present study, we aimed to compare
changes in blood circulation of the tendons after
the repeated concentric and eccentric contractions. We hypothesized that increases in blood
volume and oxygen saturation of the tendon
would be greater after eccentric than after concentric contractions.
Kubo K. Effect of repeated contractions on tendon blood circulation … Int J Sports Med 2015; 36: 481–484
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Effects of Repeated Concentric and Eccentric
Contractions on Tendon Blood Circulation
482 Training & Testing
Materials and Methods
160
▼
Subjects
Each subject performed 2 tests on 2 separate days, with at least 2
but no more than 4 weeks between sessions. The order of the 2
experimental conditions was randomized for each subject. Subjects sat on a chair to acclimate themselves to the laboratory conditions for 20 min prior to the experiment. Initially, subjects lay
in a comfortable prone position on a test bench for a 15 min rest
period (baseline). The subject lay prone on a test bench and the
waist and shoulders were secured by adjustable lap belts and
held in position. The right ankle joint was set at 90 deg (with the
foot perpendicular to the tibia = 90 deg with angles more than 90
deg being in plantar flexion) with the knee joint at full extension,
and the foot was securely strapped to a foot plate connected to
the lever arm of the dynamometer (Myoret, Asics, Japan). After
that, subjects performed repeated muscle contractions, which
consisted of plantar flexion tasks with 2 different contraction
modes (concentric and eccentric exercises). Concentric exercises
(CON) consisted of forcefully plantar flexing from 70 deg to 115
deg and then relaxing while the attachment was motor-driven to
return to 70 deg. Eccentric exercises (ECC) consisted of subjects
trying forcefully to maintain plantar flexion throughout the full
range of motion while the dynamometer was motor-driven from
115 deg to 70 deg and then relaxing while the attachment was
returned passively to 115 deg. Both CON and ECC consisted of 5
sets of 10 maximal voluntary contractions of the plantar flexors
at a constant velocity of 15 deg · s − 1, and the rest period between
sets was 1 min. The exerted torque (TQ) signal was recorded for
each contraction. After repeated muscle contractions, the subject
remained relaxed in the same position for 20 min.
Blood circulation of the Achilles tendon
Throughout the experiment, we measured blood circulation (oxyhemoglobin; Oxy, deoxyhemoglobin; Deoxy, total hemoglobin;
THb, oxygen saturation; StO2) of the Achilles tendons. To measure
blood circulation of the tendon using red laser lights (BOM-L1TRSF,
Omega Wave), a probe (SF-DS, Omega Wave, Tokyo, Japan) was
positioned 30-mm proximal to the calcaneus. The position of the
probe was marked on the skin by small ink dots. These dots
ensured the same probe positioning in each test during the experimental period. This instrument uses three red laser lights (635,
650, and 690 nm), and calculates the relative tissue levels of OxyHb,
DeoxyHb, and THb. The distance between the light source and
photodetector was 5 mm. According to the findings of Kashima [5],
the measurement depth was estimated at 3–5 mm when the dis-
120
100
80
1
2
3
set
4
5
Fig. 1 The mean values of peak torque produced by each contraction of
every 10 contractions (1 set) for repeated concentric (open) and eccentric
(closed) contractions.
tance between the light source and photodetector was 5 mm. The
details of this technique and principles of this instrument have
been described elsewhere [9, 13]. Briefly, 2-point detection and
the differential calculation method were used for measuring the
blood volume and oxygen saturation only in the deep region of the
tissue (measurement depth of 3–5 mm; ●
▶ Fig. 1 of Ref [13]. The
THb and StO2 at specific depths of tissue could be measured by
changing the location of the 2 detectors. The offset value of the
blood volume was reduced, and highly sensitive measurements
were achieved using the 2-point detection method.
In the present study, the units of OxyHb, DeoxyHb, and THb
were expressed as µmol/l, although this does not represent the
actual physical volume. Tissue StO2 was calculated from OxyHb
and THb values using the following formula:
StO2 (%) = 100 * OxyHb/THb
These data were input onto a personal computer at a sampling
frequency of 10 Hz via an A/D transducer (Power Lab, AD Instruments, Australia). The mean values over a given duration (every
set during exercises for CON and ECC, every minute over a 20-min
of recovery period) were calculated using analytical software
(Chart ver. 5.4.2, AD Instruments, Australia). These data were
presented as the amount of changes from the resting level.
Comparison of the THb, and StO2 values for the Achilles tendon
between the two tests (before repeated muscle contractions)
revealed no significant differences and a coefficient of variance of
4.8 % and 4.1 % for THb and StO2 of the Achilles tendon, r­ espectively.
Statistics
Descriptive data included means ± SD. Two-way (mode × time)
ANOVA with repeated measures was used to detect significant
differences in the measured variables from the resting level. The
F ratios for main effects and interactions were considered significant at p < 0.05. When the ANOVA revealed significant main
effects for mode and time, whether or not a significant interaction between them, we returned to one-way ANOVA with
repeated measures to detect any significant changes from the
resting level. Significant differences among means at p < 0.05
were detected using a Tukey post hoc test.
Kubo K. Effect of repeated contractions on tendon blood circulation … Int J Sports Med 2015; 36: 481–484
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
Repeated muscle contractions
140
Torque (Nm)
Eleven healthy males (age: 31.3 ± 5.8 years, height: 172.4 ± 4.4 cm,
body mass: 72.5 ± 11.2 kg, mean ± SD) volunteered for this study.
Subjects were physically active, but had not participated in any
organized program of regular exercise for at least 1 year before
testing. All subjects had no known metabolic, neuromuscular, or
peripheral vessel disorders. They were fully informed of the procedures to be utilized, as well as the purpose of the study. Written informed consent was obtained from all subjects. Research
was conducted ethically according to international standards
and as required by the journal as described in Harris and Atkinson [6]. This study was approved by the Ethics Committee for
Human Experiments, Department of Life Science (Sports Sciences), University of Tokyo.
Training & Testing
5
4
ΔOxy (µmol /l)
were significant. For Deoxy, the effect of time (p < 0.001) was significant, although the effects of mode (p = 0.337) and the interaction between mode and time (p = 0.07) were not significant.
repeated
contractions
#
3
# #
#
Discussion
2
▼
1
0
–1
–2
ΔDeoxy (µmol /l)
b
c
1
0.8
0.6
0.4
0.2
0
–0.2
–0.4
–0.6
–0.8
–1
*
#
**
# # #
#
5
ΔTHb (µmol/l)
#
#
4
3
2
1
0
–1
–2
d
–3
# #
10
ΔStO2 (%)
8
#
#
#
6
4
#
2
0
*
Rest
1 set
2 set
3 set
4 set
5 set
–2
*
**
*
5
10
15
20
Duration (min)
Fig. 2 Time course changes in oxyhemoglobin (Oxy; A), deoxyhemoglobin (Deoxy; B), total hemoglobin (THb; C), and oxygen saturation
(StO2; D) of the Achilles tendon during and after repeated concentric
(open) and eccentric (closed) contractions. * significantly different from
the resting level for repeated concentric contractions # significantly different from the resting level for repeated eccentric contractions.
Results
▼
The mean values of peak torque produced by each contraction of
every 10 contractions (1 set) for CON and ECC are shown in ●
▶ Fig. 1.
The mean torque values over the 5 sets for ECC were significantly
higher than those for CON, and decreased gradually over the 5 sets
for both CON and ECC. There was no difference in the relative
decrease in the mean torque values from the first to the 5th set
between CON ( − 15.8 ± 10.5 %) and ECC ( − 15.6 ± 10.3 %) (p = 0.959).
The changes in Oxy, Deoxy, THb and StO2 of the Achilles tendons
during repeated muscle contractions and recovery period are
shown in ●
▶ Fig. 2. For Oxy and StO2, the effects of both mode
(p = 0.004 for Oxy, p = 0.02 for StO2) and time (both p < 0.001) were
significant, although the effect of the interaction between mode
and time (p = 0.076 for Oxy, p = 0.255 for StO2) was not significant.
For THb, the effects of both mode (p = 0.014) and time (p < 0.001)
as well as the interaction between mode and time (p = 0.028)
The main finding of this study was that changes in blood circulation of the Achilles tendon during and after repeated eccentric
contractions were more remarkable than those during and after
repeated concentric contractions. To our knowledge, this is the
first study to compare changes in blood circulation of the tendons under these conditions.
In the present study, the effect of contraction mode was significant for Oxy and THb, but not or Deoxy. These results implied
that inflow of blood within the Achilles tendon during and after
repeated contractions was greater for ECC than for CON, while
no difference in oxygen consumption was found between CON
and ECC. Although the reasons for the increase in inflow of blood
during and after ECC are unclear, a mechanical phenomenon
within the Achilles tendon might be involved. Elongation of the
Achilles tendon during ECC would be greater than that during
CON, since the exerted torque was significantly higher for ECC
▶ Fig. 1). Our previous study showed that blood
than for CON ( ●
volume of the tendon did not change after repeat isometric contractions with a long duration, while it increased significantly
after repeat ballistic contractions [14]. Since isokinetic exercises
(especially slower movements) were actually close to “isometric” exercise, the present result on CON agreed with our previous
finding on the repeat isometric contractions with a long duration [14]. Therefore, the increased Oxy and THb during and after
ECC was caused by an elevated perfusion pressure within the
Achilles tendon due to the repetitive stretching and returning of
the tendon. Thus, these mechanical stimuli may lead to dilation
of blood vessels and opening of the arteriovenous anastomoses
within the Achilles tendon [8].
In addition to the changes in Oxy, Deoxy, and THb, the effect of
contraction mode was significant for StO2. Although StO2 of tendon maintained higher values after both CON and ECC, this tendency was more remarkable for ECC than for CON. Since the
oxygen consumption of the tendon was considerably lower than
that of the muscle [12], the increases in StO2 due to hyperthermia, acupuncture, and hyperbaric oxygen therapy was greater
for the tendon than for the muscle [11, 16]. Therefore, the
increase in StO2 of the tendon during and after ECC as well as
various therapies may contribute to healing of tendon injuries.
Langberg et al. [18] demonstrated through the use of the microdialysis technique that collagen synthesis was increased in the
injured tendon after 12 weeks of heavy-resistance eccentric
training. Recently, we tried to clarify the changes in synthesis of
type 1 collagen in tendons by comparing the dynamics of two
biochemical markers, i. e., procollagen type 1 C-peptide and
bone-specific alkaline phosphatase [17]. In future studies it may
be possible, with this technique, to estimate type 1 collagen synthesis in human tendons during and after CON and ECC.
According to the previous studies using the color Doppler and
laser Doppler techniques [10, 21], the eccentric training for a
fixed period of time reduced the increased paratendinous capillary blood flow and neovascularisation in patients with chronic
painful Achilles tendinosis, and thus these changes would be
associated with good clinical results. However, this current study
was not able to compare the present results with these previous
Kubo K. Effect of repeated contractions on tendon blood circulation … Int J Sports Med 2015; 36: 481–484
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a
483
484 Training & Testing
Acknowledgements
▼
This study was supported by a Grant-in-Aid for Young Scientists
(A) (21680047 to K. Kubo) from the Japan Society for the Promotion of Science.
Conflict of interest: The authors have no conflict of interest to
declare.
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Kubo K. Effect of repeated contractions on tendon blood circulation … Int J Sports Med 2015; 36: 481–484
This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited.
findings, because there were differences in the measured variables
(e. g., blood flow in the previous studies and blood volume in this
study) and the status of the subjects (e. g., patients in the previous
studies and healthy in this study). In particular, regarding the used
techniques, THb and StO2 measured by red laser lights were
obtained at the depth of 3–5 mm from the skin, whereas blood
flow measured by color Doppler and laser Doppler techniques was
obtained from the vascular surrounding the tendon (paratenon).
Therefore, it may be that blood circulation within the tendons differs from that of paratenon during injured and restored phases.
In the last decade, several studies have used ultrasonography to
investigate the effects of resistance training on the mechanical
properties of human tendons [e. g., [15]. These previous findings
demonstrated that there is much greater variability in the previously reported increase in tendon stiffness, ranging between 16
and 65 %. However, little is known about the effect of eccentric
training on human tendon properties in vivo [4, 5, 20]. Among
these studies, the eccentric training regimen resulted in a small
increase [4] and no change [5, 20] in tendon stiffness. The reasons
for a slight increase in tendon stiffness after eccentric training are
unclear, but there are several possibilities. Our longitudinal study
showed that blood volume of tendon increased significantly after
12 weeks of dynamic training (tendon stiffness increased
minorly), although it did not change after isometric training (tendon stiffness increased considerably) [15]. Taking these previous
findings into account together with the present result, we may
say that the tendon extensibility (elasticity) would be preserved
due to the increase in blood volume and oxygen saturation
within the tendon during the repair process following eccentric
training. More recently, Yin et al. [23] reported that there was
increased microcirculation (THb and StO2) of the patellar tendon
after performing knee extension eccentric exercises that resulted
in a reduction in tendon stiffness. However, these discussions are
speculative and require additional data for clarification.
Attention must be drawn to the limitations of the present study.
First of all, changes in blood circulation of tendons were observed
for only 20 min after exercises. As shown in ●
▶ Fig. 2, increased
Oxy, THb, and StO2 would return to the resting level after the
recovery period (> 20 min). In addition, it is uncertain whether the
observed changes in blood circulation of tendon are reproducible
with the second set of exercise after 30–60 min. However, it is
expected that the training-induced changes (chronic effects) in
blood circulation of tendons were accumulated for a long period.
In fact, it was found that blood circulation of the tendon changed
after 6 weeks of hyperbaric oxygen therapy, although this change
disappeared after a few hours in one case [11]. Secondly, the
results of the present study were gathered from healthy subjects,
but not from patients with chronic tendinosis. In the future, it will
be necessary to investigate the effect of eccentric training for a
long period on the treatment of actual injured tendon.
In conclusion, changes in blood circulation of the Achilles tendon
during and after repeated eccentric contractions were higher
compared to those during and after repeated concentric contractions. This result could be related to the efficacy of eccentric
training on injured tendons.