Key words
eccentric muscle contraction - strength training - force suppression - quadriceps
hypertrophy - muscular power
Introduction
Eccentric exercise is a popular strength training paradigm. Investigators who have
implemented eccentric training programs in healthy individuals generally report significant
hypertrophy in the active muscles [17]
[20]
[21]
[29], as well as increased maximum eccentric and isometric strength [21]
[22] following training. Results for maximum concentric strength and/or power, however,
have been mixed with some investigators reporting increases [4]
[20], but most investigators have reported unchanged maximum concentric strength and/or
power [8]
[17]
[21]
[34]. These mixed reports on maximum concentric strength and/or power improvements following
eccentric training are curious because muscle force is generally a function of muscle
excitation and cross-sectional area [13]
[15]. Furthermore, skeletal muscle hypertrophy with changes in maximum eccentric but
not concentric strength and/or power implies that improvements are contraction or
velocity-specific. Although such a unique finding could be due to adaptations that
are truly velocity-specific [36], this finding is not universal [32]. Alternatively, a suppressive effect associated with chronic eccentric training
intervention may explain the lack of improvements in maximum concentric strength and/or
power found in immediate post-training evaluations. In other words, eccentric exercise
could suppress muscle force [11] and/or alter the neural control of muscle force [7]. Depending on the eccentric training intensity and duration, improvement in maximum
concentric strength and/or power might not be fully realized until muscle tissue,
neuromuscular control and reflex sensitivity has fully recovered or adapted (i. e.,
several weeks following end of training) [2]
[6]
[37]. Measures of concentric strength and/or power performed weeks after cessation of
training may reflect fully adapted and recovered neuromuscular function. Such measures
could support and expound upon previous findings of improved concentric strength and/or
power.
Cycling provides a particularly effective model for evaluating the effects of eccentric
training on maximal concentric function. That is, eccentric cycling can serve as repetitive,
high-force, low-metabolic cost, multi-joint eccentric training modality which is known
to produce significant hypertrophy [16]
[17]
[29]. Maximal concentric cycling can also be used to assess pre- to-post changes in maximum
power [8]
[17], thus providing similar actions for training and assessment. Accordingly, our purpose
for conducting this investigation was to evaluate changes in muscle structure (rectus-femoris
(RF) and vastus-lateralis (VL) thickness and pennation angles) and muscular function
(maximum concentric cycling power, Pmax) at 1 and 8 weeks following chronic eccentric cycling training. The timing of these
measures would allow comparison with many previous studies in which pre- to post-changes
in concentric strength and/or power were measured soon after training and provide
sufficient time for recovery following chronic eccentric cycling training. We hypothesized
that eccentric cycling training would induce structural changes to the muscle, which
would be reflected in improved maximum concentric cycling power, with the largest
increases occurring 8 weeks post-training.
Methods
Participants
8 young healthy individuals (4 males and 4 females) volunteered to participate in
this investigation (participant characteristics are presented in [Table 1]). Participants were instructed to refrain from strength training during eccentric
cycling training and for the 8 weeks following the completion of the study. Experimental
procedures used in this investigation were approved by the University of Utah Institutional
Review Board and conformed to required ethical standards [18]. All participants provided written informed consent prior to engaging in experimental
procedures.
Table 1 Participant descriptive characteristics (n=8).
|
Mean±SD
|
|
age (years)
|
22±2
|
|
mass (kg)
|
69±13
|
|
height (m)
|
1.7±0.1
|
|
BMI (kg/m2)
|
23±2
|
BMI: Body mass index
Experimental design
The experimental protocol is described below and illustrated in [Fig. 1]. In this investigation, we implemented an 8-week eccentric cycling training intervention
and evaluated pre- to post-training changes in muscle structure (RF and VL thickness
and pennation angles) and maximum concentric cycling power (Pmax). 1 week before the start of the eccentric cycling training, participants reported
to the laboratory for familiarization trials of maximal concentric cycling and for
pre-training assessments of muscle structure and maximum cycling power. After these
initial visits, participants performed eccentric cycling training 2 times per week
for 8 consecutive weeks. 1 week after the final training session, participants returned
to the laboratory where muscle structure and Pmax were assessed. Participants returned to the laboratory again 8 weeks after the final
training session for the assessment of Pmax. Participants also performed familiarization trials of maximal concentric cycling
1 week before the post-training and 8 weeks post-training measurements in order to
retain any learning and to ensure that the participants were adept at the cycling
technique [30].
Fig. 1 Experimental protocol of the study. One week before the start of the eccentric cycling
training, pre-training assessments of muscle structure and maximum concentric cycling
power (Pmax) were conducted. Next, participants performed eccentric cycling training 2 times
per week for 8 consecutive weeks. One week after the final training session, muscle
structure and Pmax were assessed. Pmax was assessed again 8 weeks after the final training session.
Eccentric cycling training
Participants performed eccentric cycling training at 60 rpm on an isokinetic eccentric
cycling ergometer ([Fig. 2]) [8]
[9]. The progression of eccentric cycling training intensity and duration was modified
from our previous work [8] and is summarized in [Table 2]. Specifically, eccentric cycling power was initially set to 20% of pre-training
Pmax for 5 min and progressively increased to 55% of pre-training Pmax for 10.5 min over the 8-week training period. Participants targeted the prescribed
powers with feedback from a power meter (Schoberer Rad Messtechnik, SRM, Jülich, Germany).
During the final minute of each training session, participants were asked to report
ratings of perceived exertion for their total body exertion (RPEbody) as well their specific leg exertion (RPElegs) using a Borg 6–20 scale (Borg, 1970). Heart rate was also was assessed during the
final minute of every training session (Polar FT1, Kempele, Finland). Finally, prior
to each eccentric cycling training session participants performed a bilateral squat
movement during which they indicated the level of muscle soreness in their legs using
a visual analog scale (0–10 cm) with 10 cm representing the worst pain imaginable
[8]. A soreness value of less than 5 cm (representing moderate soreness) was used as
an indication to proceed with subsequent eccentric cycling training. This measure
was utilized to ensure that the eccentric cycling protocol was safely administered
and tolerated by the uncompensated volunteer participants.
Fig. 2 Overview of experimental setup. Schematic illustrates the eccentric cycle ergometer.
As the pedals are driven toward the participant (large white circular arrow) by the
electric motor, the participant resists by applying force to the pedals (small white
arrow). Because the magnitude of the force produced by the motor exceeds that produced
by the participant, leg extensors (black arrows on thigh) actively lengthen (eccentric
muscle action). Muscle structure and muscular function were evaluated before and after
training. Representative ultrasound images of the vastus lateralis (VL) illustrate
the assessment of muscle thickness a and pennation angle (θ) b. Representative power-pedaling rate relationship c illustrates the assessment of maximum concentric cycling power.
Table 2 Progression of eccentric cycling training intensity and duration. Note that all training
was performed at 60 rpm.
|
Weeks of Training
|
% Baseline Pmax
|
Duration (min)
|
|
1
|
20
|
5
|
|
2
|
25
|
6
|
|
3
|
30
|
7
|
|
4
|
35
|
8
|
|
5
|
40
|
9
|
|
6
|
45
|
9.5
|
|
7
|
50
|
10
|
|
8
|
55
|
10.5
|
Pmax: Maximum concentric cycling power
Muscle structure
Ultrasound imaging (LOGIQ e 2008, GE Healthcare, Wauwatosa, WI, USA) was used to examine
muscle structure of RF and VL of the right quadriceps. Participants were placed in
the supine position with knees resting comfortably in extension near the natural resting
position of 10° of flexion. Images of the RF were taken at the midpoint between the
anterior superior iliac spine and the superior border of the patella. Vastus lateralis
images were taken at the midpoint between the greater trochanter and the lateral femoral
epicondyle. Each midpoint was clearly marked on the skin to ensure proper placement
of the probe during repeated scans. Electrode gel was applied to the skin to aid acoustic
coupling and to eliminate compression or deformation of the muscle. Two-dimensional
B-mode ultrasound imaging with a 6–12 MHz linear array transducer was used to obtain
images of the RF and VL. Digitizing software (ImageJ 1.46r, National Institutes of
Health, Bethesda, MD, USA) was used to assess (1) muscle thickness as the distance
between the superficial and deep aponeuroses in the middle of the ultrasound image
at a 90° angle from the deep aponeurosis, and (2) pennation angle as the positive
angle between the deep aponeurosis and the fascicle line.
Maximum concentric cycling
Participants performed maximal concentric cycling trials (4 s) on an inertial-load
cycle ergometer which measures maximal concentric cycling power across a range of
pedaling rates (e. g., 60–180 rpm) in a single brief trial [31]. Following a 5-min cycling warm-up (~50–125 W), participants began each trial from
rest and accelerated maximally for 8 pedal revolutions with resistance provided solely
by the moment of inertia of the flywheel. Participants were instructed to remain seated
throughout each trial and were given standardized verbal encouragement. Flywheel angular
position data were low-pass filtered at 8 Hz using a 5th order spline routine [38], and velocity and acceleration were determined from the spline coefficients. Power
averaged over each complete crank revolution was calculated as rate of change in kinetic
energy, and maximum power was identified as the apex of the power-pedaling rate relationship.
Statistical analysis
Paired student’s t-tests were used to evaluate pre- to post-training changes in muscle
thickness and pennation angle. A one-way repeated measures analysis of variance (ANOVA)
and subsequent post hoc (Fisher least significant differences) analyses were used
to evaluate pre- to post-training changes in Pmax (pre-training, 1 week and 8 weeks post-training). Effect sizes (ES) were calculated for all analyses and ES magnitudes of 0.10, 0.30, and 0.50, were interpreted as small, medium, and large
effects, respectively [12]. Values are reported as mean±SEM, and alpha was set at 0.05.
Results
All participants completed the 8-week training study at 92±4% of prescribed training
intensity. Average power absorption progressed from 157±24W to 442±56W, and total
work increased from 48±8 kJ to 272±35 kJ during the 8-week training period ([Fig. 3]). Training heart rate, RPEbody, and RPElegs also increased in response to the progressive eccentric cycling training ([Fig. 3]). Participants reported low (0.6±0.2 cm) to moderate (2.5±0.9 cm) levels of muscle
soreness during the training period ([Fig. 3]).
Fig. 3 Mechanical, cardiorespiratory and perceptual responses recorded during eccentric
cycling training. Values are presented as mean±SEM.
Following eccentric cycling training RF and VL muscle thickness increased by 24±4%
(18.6±1.3 pre-training to 23.0±1.7 mm, 1 week post-training) and 13±2% (19.6±1.4 pre-training
to 22.1±1.4 mm, one week post-training), respectively, compared to pre-training values
(both P<0.01, ES=0.83; [Fig. 4]). Similarly, RF and VL pennation angles increased by 31±4% (11.6±0.7 pre-training
to 15.1±0.9°, 1 week post-training; P<0.05, ES=0.74) and 13±1% angle (15.8±1.0 pre-training to 17.8±0.6°, 1 week post-training;
P<0.05, ES=0.70), respectively, compared to pre-training values. Repeated measures ANOVA procedures
revealed a significant main effect of time on Pmax values (P<0.01). Subsequent post-hoc analyses indicated that compared to pre-training values,
Pmax increased by 5±1% from 894±120W pre-training to 941±124W at 1 week post-training
(P<0.05, ES=0.78) and by 9±2% from 894±120W pre-training to 970±128W at 8 weeks post-training
(P<0.05, ES=0.82; [Fig. 5]). Although Pmax at 8-weeks post-training vs. 1-week post-training was not statistically significant
(P=0.06, ES=0.64), the higher Pmax observed in 11 out of the 12 participants at 8 week vs. 1 week post-training provides
strong evidence for a trend of increasing Pmax.
Fig. 4 Pre- to post-training changes in vastus lateralis (VL) and rectus femoris (RF) muscle
thickness a and pennation angles b. Values are presented as mean±SEM. *P<0.05 vs. pre-training.
Fig. 5 Pre- to-post-training changes in maximum concentric cycling power a. Complete powerpedaling rate relationships b were shifted upward at 1- and 8-weeks post-training. Values are presented as mean±SEM.
SEM bars in panel b were removed for clarity. *P<0.05 vs. pre-training value. Note that, maximum power
measured at 8 weeks post-training tended to be greater than that measured at 1 week
post-training (P=0.06).
Discussion
Our main finding in this study was that 8 weeks of eccentric cycling training elicited
changes in both muscle thickness and pennation angle, and improved Pmax. Furthermore, the larger increase in Pmax measured at 8 weeks post-training suggested that sufficient recovery following chronic
eccentric cycling training might be necessary to fully detect changes in maximum concentric
power. Thus, our intervention involving short-duration high-intensity eccentric cycling
(2×/week, 5–10.5 min at 20–55% Pmax) served as a time-effective strategy for improving muscle structure and muscular
function, and our post-testing period of 8 weeks allowed sufficient time for the recovery/adaptation.
Although the gradual ramp-up protocol utilized in the current study was more aggressive
than those employed by previous investigators [8]
[29], our results suggested that our protocol can be safely administered and tolerated
by healthy individuals.
To the best of our knowledge, this is the first report of increased maximum cycling
power following eccentric cycling training in young healthy populations. Previous
investigators using similar protocols reported findings of unchanged concentric cycling
power [8]. We believe the most plausible explanation for these differences is the timing of
the post-training evaluation of muscular function. The non-significant findings reported
by previous investigators may be a reflection of suppressed muscular function due
to muscle remodeling following high-intensity eccentric exercise. Several investigators
have reported long lasting indications of remodeling with suppressed muscle force
after eccentric exercise [1]
[33]. Results from mechanistic studies indicate that a cascade of events resulting in
muscle remodeling occur in response to eccentric training [19]
[25]
[26]
[35]. These events include satellite cell activation and proliferation for mediating
muscle remodeling during the regenerative process. Furthermore, muscle remodeling
can also be initiated independent of discernible damage to the muscle [14]
[28]. Therefore, post-training measures will accurately reflect optimum muscular function
if the time course for the cascade of events that result in complete muscle remodeling
is observed in the regenerative process. Indeed, Kadi and colleagues (2004) reported
that satellite cells remained significantly elevated at 60 days of detraining following
heavy resistance training. Hence, the time course of a muscle remodeling event such
as satellite cell content modulation could explain the larger increase in maximum
concentric cycling power measured at 8 weeks post-training. The present data allow
us to speculate that previous investigations evaluating maximum concentric strength
and/or power [8]
[17] might have shown significant increases if additional post-training assessments were
performed at a later time point. Such evaluation might have provided time for full
muscular recovery, which would allow the positive consequences of eccentric cycling
training to emerge.
The results of increased RF and VL muscle thickness and pennation angles demonstrated
training-induced alterations in muscle structure. Previous investigators have reported
increases in muscle fiber cross-sectional area [29] and lean muscle mass [17] in healthy individuals following eccentric cycling training. Thus, the results from
the current investigation relating to muscle structure improvements support and unite
these previous findings. Hypertrophy after eccentric cycling training would be expected
given the high forces and powers elicited during repetitive eccentric muscle contractions
[5]. In addition, an increase in pennation angle provides variable gearing to improve
the modulation of force output for contractions against high loads [3] and can also be regarded as a strategy for attaching more contractile material along
the tendon aponeurosis [10]. Hence, the training-induced hypertrophy and concomitant increase in pennation angle
may account for muscular function improvements observed in this investigation. Because
logistical issues prevented the assessment of muscle structure at the 8-weeks post-training
time point, our present results only allow us to speculate that these muscular adaptations
were retained at the 8-weeks post-training time point. Furthermore, adaptations to
strength training have been shown to be retained for at least 31 weeks after cessation
of training in young healthy individuals [24]. Neural adaptations associated with the activation of agonistic, synergistic and
antagonistic muscles [27] could have also contributed to the improvement in maximum concentric cycling power.
A future direction for our laboratory will be to quantify and separate the contributions
of muscular and neural adaptations with more direct measures (e. g., electromyography).
An extensive review by Isner-Horobeti et al. (2013) highlighted more than 15 investigations
demonstrating that eccentric cycling training is more effective than traditional concentric
and/or strength training at improving muscular function in a variety of populations
ranging from patients with central limitations to competitive athletes [23]. Based on these previous findings, we did not include a control group in the present
study. Despite the improvements in quadriceps muscle structure and maximum cycling
power observed in this study, obtaining direct measures of muscle damage, as well
as muscular and neural adaptations, will provide a more complete description of the
repeated bout effect and the modulation of adaptations associated with chronic eccentric
cycling.
In summary, short-duration high-intensity eccentric cycling training resulted in improvements
in muscle structure, reflected in improved Pmax. These results also suggest that allowing sufficient time for recovery is important
for detecting functional gains following eccentric cycling training.
