Scand J Med Sci Sports 2012:

2011 22: 179–184 & 2011 John Wiley & Sons A/S
doi: 10.1111/j.1600-0838.2010.01285.x

Dynamics of viscoelastic creep during repeated stretches

E. D. Ryan1, T. J. Herda2, P. B. Costa2, A. A. Walter2, J. T. Cramer2
1
Applied Musculoskeletal and Human Physiology Laboratory, Department of Health and Human Performance, Oklahoma State
University, Stillwater, Oklahoma, USA, 2Biophysics Laboratory, Department of Health and Exercise Science, University of
Oklahoma, Norman, Oklahoma, USA
Corresponding author: Eric D. Ryan, PhD, Applied Musculoskeletal and Human Physiology Laboratory, Department of
Health and Human Performance, Oklahoma State University, 198 Colvin Recreation Center, Stillwater, Oklahoma 74078,
USA. Tel: 11 405 744-9935, Fax: 11 405 744-6507, E-mail: eric.ryan@okstate.edu
Accepted for publication 29 November 2010

The present study examined the viscoelastic creep responses
in vivo during repeated constant-torque stretches in human
skeletal muscle. Twelve healthy participants completed four
consecutive 30-s constant-torque passive stretches of the
right plantar flexor muscles. Position and surface electro-
myographic (EMG) amplitude values were quantified at
every 5-s period and the percent change in position was
quantified for each 5-s epoch relative to the total increase in
ankle joint position for each stretch. In addition, the
absolute changes in position were plotted on a logarithmic
time scale and fit with a linear regression line to examine
both the rate of increase (slope) and the overall increase in
position over the entire stretch (y-intercept). The percent
change and slope were similar (P40.05) over all four
stretches, with the majority of increases in position occur-
ring within the initial 15–20 s of each stretch (84%).
Absolute ankle joint position and the y-intercept increased
(Po0.05) following both the first and second stretch but
plateaued (P40.05) after the third stretch. In addition,
EMG amplitude values did not change (P40.05) during or
between each 30-s stretch. These data indicate that the
amount and rate of viscoelastic creep were similar during
practical durations of constant-torque stretching despite no
change in ankle joint position following three 30-s stretches.

Skeletal muscle, like most biological tissues, exhibits
properties of viscoelasticity and displays time-depen-
dent properties when held at a constant length (stress
relaxation) or force (creep) (Taylor et al., 1990;
McHugh et al., 1992; Ryan et al., 2010). Viscoelastic
tissues are classically described by mechanical models
where elasticity is modeled using linear springs
(Hookean body) and viscosity (Newtonian body) is
modeled with a hydraulic piston or dashpot (Taylor
et al., 1990). Hysteresis, stress relaxation, and creep
are properties of skeletal muscle that represent a
viscous effect (Viidik 1973; Toft et al., 1989). These
properties have been examined previously by Taylor
et al. (1990) who developed a model to characterize
the viscoelasticity of the rabbit muscle–tendon unit in
vitro. These responses were later confirmed in vivo by
McHugh et al. (1992) who examined stress relaxation
in human skeletal muscle during static stretching of
the hamstrings. Magnusson and colleagues extended
upon these findings by examining stress relaxation
during repeated static (constant-angle) stretching of
the hamstrings under long (Magnusson et al., 1995,
1996a) and shorter (Magnusson et al., 2000) practical
stretching durations.
More recent studies have suggested that constant-
torque stretching procedures may be more beneficial
than constant-angle and cyclic stretching maneuvers
at altering the passive properties of the muscle–
tendon unit (Yeh et al., 2005, 2007). For example,
Yeh et al. (2007) reported constant-torque stretching
protocols were more effective in improving range of
motion and decreasing passive stiffness in stroke
patients. Previous authors (Ryan et al., 2008a,
2009) have suggested that constant-torque stretching
protocols may induce greater work on the muscle–
tendon unit thereby resulting in greater ‘‘muscle
creep’’ and consequently translate into greater reduc-
tions in stiffness during repetitive stretching.
Although there has been a recent interest in con-
stant-torque stretching maneuvers, little is known
about the viscoelastic creep responses of the mus-
cle–tendon unit in vivo. The majority of literature
examining the time-dependent viscoelastic properties
of the muscle–tendon unit during repeated stretching
has been completed with the use of traditional
constant-angle or static stretching techniques (Mag-
nusson et al., 1995, 1996a, 2000; McHugh et al.,
1992). Very recently, Ryan et al. (2010) confirmed
and characterized viscoelastic creep during a single
30-s stretch and examined the consistency of these
responses. The authors were able to demonstrate
viscoelastic creep in vivo and found the responses to

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Ryan et al
be consistent (Ryan et al., 2010). Therefore, the
purpose of the current study was to follow-up with
work by Ryan et al. (2010) and characterize the
viscoelastic creep responses during repeated con-
stant-torque stretching exercises using stretching
durations (2 min of time under stretch) commonly
performed in athletic and clinical settings (Bandy &
Irion, 1994; Magnusson et al., 2000; Brandenburg,
2006; Behm & Kibele, 2007).
Methods
Participants
Twelve healthy participants (mean  SD: age 5 22.4  3.2
years; height 5 168.3  12.6 cm; mass 5 69.1  17.7 kg) vo-
lunteered for this investigation. This study was approved by
the University Institutional Review Board and all participants
completed an informed consent form and a pre-exercise testing
health status questionnaire. None of the participants reported
any current or ongoing neuromuscular diseases or musculo-
skeletal injuries specific to the ankle, knee, or hip joints.
Experimental design
The participants visited the laboratory on two occasions
separated by 3–5 days. The first visit was the familiarization
trial and the second visit was the experimental trial. During
the familiarization trial, each participant practiced the 30-s
stretches (i.e. creep assessments) and determined the max-
imum tolerable passive torque threshold. The maximum
tolerable torque threshold was determined during a series of
passive stretches with the dynamometer programmed in pas-
sive mode as described previously (Ryan et al., 2009, 2010).
The torque threshold was progressively increased to the point
of discomfort, but not pain, as verbally acknowledged by the
participant. This pre-determined torque threshold was used
during the experimental trial to examine creep during each of
the repreated stretches. The experimental trial included four
30-s constant-torque stretches with a 20-s rest period (Ryan et
al., 2008b) between each stretch and a maximal voluntary
Fig. 1. The absolute changes in position over each 30-s constant-torque stretch. *Position for stretch 1 was less than stretches
2–4 at all time points (Po0.05). wPosition for stretch 2 was less than stretches 3 and 4 at all time points (Po0.05). Post hoc
comparisons for each stretch indicated that for the first and fourth stretches, position at 0 s was o5–30 s, 5 s was o10–30 s, 10 s
was o15–30 s, and 20 s was less than the 25- and 30-s time periods. For the second stretch, 0 s was o5–30 s, 5 s was o10–30 s,
and 10 s was o15–30 s. For the third stretch, 0 s was o5–30 s, 5 s was o10–30 s, 10 s was o15–30 s, and 20 s was less than the
30 s. Values are mean  SEM.
180
contraction (MVC) of the plantar flexors performed following
the four stretches.
Creep measurement
Each participant was seated with restraining straps over the
pelvis, trunk, and thigh, with a leg flexion angle of 01 below the
horizontal plane (full extension), and the lateral malleolus of
the fibula aligned with the input axis of a calibrated Biodex
System 3 dynamometer (Biodex Medical Systems Inc., Shirley,
New York, USA). The foot was secured in a thick rubber heel
cup attached to a footplate with straps over the toes and
metatarsals (distal to the malleoli). The dynamometer lever
arm passively dorsiflexed the foot at an angular velocity of 51/s
from  201 of dorsiflexion until the maximal tolerable torque
threshold was met. The dynamometer held this constant
passive torque for 30 s and was then released back to  201
of dorsiflexion for 20 s. This was repeated until a total of four
stretches were completed. The participants were instructed to
remain as quiet and relaxed as possible during the 30-s period.
During each 30-s stretch, position (1) values were examined at
every 5 s (i.e. 0, 5, 15, 20, 25, and 30 s) with 500 ms epochs
using custom-written software (LabVIEW v 8.5, National
Instruments, Austin, Texas, USA; Fig. 1). Previous work
from our laboratory (Ryan et al., 2010) has demonstrated
these responses to be consistent (ICC values  0.994 and
SEM values  1.54% of the mean).
To ensure all stretches were passive, pre-amplified active
surface electrodes (EL254S, Biopac Systems, Santa Barbara,
California, USA; gain 5 350) were placed over the medial
gastrocnemius (MG), soleus (SOL), and tibialis anterior (TA)
muscles (Hermens et al., 1999; Ryan et al., 2010). Electro-
myographic (EMG) amplitude values were calculated with a
root mean square function at every 5 s with the same 500 ms
epoch as the position signal. The MG and SOL values were
then normalized to the EMG amplitude values recorded during
a MVC based on the procedures of Gajdosik et al. (2006).
Signal processing
The position (1) and EMG (mV) signals were sampled simul-
taneously at 1 kHz with a Biopac data acquisition system

(MP150WSW, Biopac Systems) during each of the 30-s con-
stant-torque stretches. All signals were stored on a personal
computer (Dell Inspiron 8200, Round Rock, Texas, USA) and
processed offline using custom-written software (LabVIEW v
8.5). The position signals were smoothed with a zero-phase
shift 100 point moving averager and all EMG signals were
filtered with a bandpass zero-phase fourth-order Butterworth
filter (10–500 Hz). All subsequent analyses were performed on
the filtered signals.
Statistical analyses
Four separate two-way [stretch (stretch 1 vs stretch 2 vs stretch
3 vs stretch 4)  time (0 vs 5 vs 10 vs 15 vs 20 vs 25 vs 30)]
repeated measures analyses of variance (ANOVAs) were used
to examine the absolute changes in position and EMG
amplitude for the MG, SOL, and TA over each 30-s stretch.
The relative changes in position were examined with a two-
way repeated measures [stretch (stretch 1 vs stretch 2 vs stretch
3 vs stretch 4)  time (0–5 vs 5–10 vs 10–15 vs 15–20 vs 20–25
vs 25–30)] ANOVA and expressed as a percentage of the total
change in position for every 5-s period (Ryan et al., 2010)
based on the recommendation of Gajdosik (2006). For example:
 
Position at 5 s  Position at 0 s
Percent change in position ¼
Total change in position
 100
In addition, the absolute changes in position were plotted
on a logarithmic time scale (log10) and fit with a linear
regression line to examine both the rate of increase in position
(slope) and the overall increase in position over the entire
stretch (y-intercept). These procedures are similar to those
described by Magnusson et al. (2000) who examined viscoe-
lastic stress relaxation. The slope and y-intercept were exam-
ined using a one-way repeated measures ANOVA (stretch 1 vs
stretch 2 vs stretch 3 vs stretch 4). Statistical analyses were
performed using PASW v 17.0 (SPSS Inc., Chicago, Illinois,
USA). Statistical significance was set at P  0.05.
Results
There was a significant interaction (P 5 0.023) for the
absolute changes in position (Fig. 1). The first and
the fourth stretch responses were identical and de-
monstrated position at 0 s was o5–30 s, 5 s was
o10–30 s, 10 s was o15–30 s, and 20 s was less than
the 25- and 30-s time periods. For the second stretch,
0 s was o5–30 s, 5 s was o10–30 s, and 10 s was
o15–30 s. For the third stretch, 0 s was o5–30 s,
5 s was o10–30 s, 10 s was o15–30 s, and 20 s was less
than the 30 s time period. In addition, at all time
points the position for stretch 1 was less than stretches
2–4, and stretch 2 was less than stretches 3–4. Overall,
these results indicated that the increases in joint angle
were similar for all four stretches over the entire 30 s;
however, the third and the fourth stretches both
started and ended at the same joint angle.
For the relative changes in position (Fig. 2), there
was no significant interaction or main effects for
stretch (P40.05); however, there was a main effect
for time (Po0.001). The 0–5-s time period was
greater than the 5–10-, 10–15-, 15–20-, 20–25-, and
Viscoelastic creep and stretching
25–30-s time periods. The 5–10-s time period was
greater than the 10–15-, 15–20-, and 25–30-s time
periods and the 10–15- and 15–20-s time periods were
greater than the 25–30-s time period. Overall, these
results indicated that the relative change in position
is similar for all four stretches.
For the logarithmic time scale variables, there was
no main effect for stretch for the slope values
(P 5 0.059; Fig. 3); however, there was a main effect
for stretch for the y-intercept values (Po0.001).
Stretch 1 was less than stretches 2–4, and stretch 2
was less than stretches 3–4. In addition, there were no
interactions or main effects (P40.05) for EMG
amplitude of the MG, SOL, and TA muscles. Over-
all, these results indicated that the rate of viscoelastic
creep was similar for all four stretches; however,
stretch 3 and 4 started and ended at the same joint
angle. The observed power values from the highest
order ANOVA was 0.791, 0.791, 0.655, and 1.000 for
the absolute changes in position, relative changes in
position, slope of the logarithmic time scale vari-
ables, and y-intercept of the logarithmic time scale
variables, respectively.
Discussion
The primary findings of the current study indicated
that four consecutive 30-s constant-torque stretches
resulted in the same viscoelastic creep response. Each
stretch demonstrated similar relative and absolute
increases in position (Figs 1 and 2) and no significant
differences between the slope values (i.e. rate of
increase) when plotted on a logarithmic time scale
(Fig. 3). However, absolute ankle position and the y-
intercept values increased following both stretch 1
and 2 and then plateaued following the third stretch
(Figs 1 and 3).
Many previous studies have examined viscoelastic
stress relaxation responses in vitro (Taylor et al.,
1990), and in vivo (McHugh et al., 1992; Magnusson
et al., 1995, 1996a, b, 2000; Fowles et al., 2000;
McNair et al., 2000; Kubo et al., 2001; Weir et al.,
2005; Gajdosik et al., 2006) during both single and
repeated constant-angle stretches. We are aware of
only two studies that have examined viscoelastic
creep responses during single constant-torque
stretches that were held for 30 s and 30 min in
duration (Yeh et al., 2007; Ryan et al., 2010) and
no studies examining these responses during repeated
stretching protocols. During single constant-angle
and constant-torque stretches, the majority of
changes in stress relaxation and creep occur within
the first 15–20 s of the stretch (McHugh et al., 1992;
McNair et al., 2000; Gajdosik et al., 2006; Ryan et
al., 2010), which are in agreement with the findings of
the present study (Fig. 2). During repetitive constant-
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Ryan et al

Fig. 2. The marginal means (collapsed across stretch) for the relative changes in position over the 30-s period expressed as a
percentage of the total increase in position per the recommendation from Gajdosik (2006). *The 0–5-s time period was greater
than (Po0.05) all other time periods. wThe 5–10-s time period was greater than the 10–15-, 15–20-, and 25–30-s periods. #The
10–15- and 15–20-s periods are greater than the 25–30-s period. Values are mean  SEM.

Fig. 3. The absolute changes in position for each stretch on a logarithmic time scale (Magnusson et al., 2000). *The y-intercept
for stretch 1 is less than stretches 2–4 (Po0.05). **The y-intercept for stretch 2 is less than stretches 3–4 (Po0.05). The
equation [y 5 (slope) x1y  intercept] of each linear regression line (stretches 1–4) includes the mean values  95% confidence
intervals for both the slope and y-intercept.

angle stretches held at the same pre-determined final
angle, relatively short durations of stretches
(3  45 s) resulted in identical stress relaxation re-
sponses (Magnusson et al., 2000). However, longer
durations of stretches have shown that the relative
stress relaxation responses to subsequent stretches
are diminished (Magnusson et al., 1995, 1996a; Weir
et al., 2005). For example, Magnusson et al. (1995,
1996a) reported on two occasions that the relative
amount of stress relaxation occurring during five
consecutive 90-s stretches decreased as additional
stretches were performed (i.e. stretch 5ostretch 1).
In addition, when these authors re-examined pre-
vious data (Magnusson et al., 2000), they found that
when plotted on a logarithmic time scale, the slope
and y-intercept values were significantly different
between the first and the third 90-s stretch and are
likely a result of an acute alternation of the muscles
resistance to stretch (i.e. passive stiffness). Interest-
ingly, the results of the current study suggested that
the viscoelastic creep response occurred at the same
relative rate for each 30-s stretch despite starting and
ending at the same ankle joint position for the third
and fourth stretch.
The differences between the findings of the current
study and those reported during repeated constant-
angle stretching protocols (Magnusson et al., 1995,
1996a, 2000) are likely attributed to the constant-
torque nature of the stretching protocol employed. It
is possible that the lack of changes in ankle joint
position following the third stretch is a result of an
acute alteration of the muscle–tendon unit that
resulted in a possible set point in ankle joint position
(Fowles et al., 2000; Ryan et al., 2009). For example,
a previous study by Ryan et al. (2009) found that
passive stiffness of the plantar flexors was reduced
following two 30-s constant-torque stretches but did
not decrease further with two additional stretches.
Further support is provided by Fowles et al. (2000)
who examined a stretching protocol that employed

182

13 constant-angle stretches at progressively increas-
ing joint angles. The authors reported that the initial
average peak passive torque increased and plateaued
from the first to the third stretch by 7.8% and
suggested a possible ‘‘ . . . set point for stretch
tolerance’’ (p. 1181). A similar increase in position
was found (7.1%) between the first and third stretch
in the current study, which may also indicate a set
point in ankle joint position. Although there was no
change in ankle position for the third and fourth and
stretch, the percent increase (Fig. 2) and rate of
change (Fig. 3) in creep did not change (P40.05)
across all stretches. It is possible that due to the
constant load that is applied to the muscle–tendon
unit by the dynamometer, the tissues will continue to
exhibit creep at the same relative rate under relatively
light loads (  50 N m) (Aritan et al., 2008) despite a
reduction in passive stiffness. However, future stu-
dies are needed to test this hypothesis and determine
if the number or intensity of the stretches (i.e. less
than the point of discomfort) alters the creep re-
sponse in subsequent stretches (Magnusson et al.,
1995; Aritan et al., 2008).
The structures and mechanisms responsible for the
viscoelastic creep response in the human muscle–
tendon unit are unclear. Many previous authors
have speculated a number of different structural
alterations contributing to the stretching-induced
decreases in passive stiffness, which include increases
in tendon compliance (Kubo et al., 2001), non-
contractile protein elongation (Gajdosik et al.,
2005), increases in fascicle length (Fowles et al.,
2000), and lengthening of the intramuscular connec-
tive tissue (Morse et al., 2008). It is possible that
many of these mechanisms may also mediate the
viscoelastic creep response. A recent study by Morse
et al. (2008) reported that 5 min of passive stretching
elicited a distal shift of the musculo-tendinous junc-
tion in the MG muscle, which was not attributed to
increases in tendon compliance or fascicle length.
The authors proposed that ‘‘ . . . connective tissue
elements within the muscle change their elastic prop-
erties when subject to repeated stretches’’ (p. 103).
Other authors (Purslow et al., 1998) have provided
further evidence suggesting that viscoelastic stress
relaxation and creep in intramusculuar connective
tissue is due to the relaxation within the collagen
fibers themselves or the fiber and proteoglycan ma-
trix. Although the precise mechanisms responsible
for the creep responses cannot be determined from
the present study, it is possible based on these
previous findings that the relaxation of intramuscular
collagen maybe responsible for the observed viscoe-
lastic creep responses. Future studies with the use
of ultrasound measurements (Morse et al., 2008) are
needed to help identify these specific structures
in vivo.
Viscoelastic creep and stretching
In theory, it is possible that the repeated constant-
torque stretching maneuvers may elicit the stretch
reflex causing activation of the plantar flexor muscles
or potentially cause a reduction in muscle activation
in subsequent stretches, which may alter the creep
response. For example, a previous study by Gajdosik
(2006) has suggested that the low-level involuntary
muscle activation may influence the viscoelastic
stress relaxation response in older participants. How-
ever, the findings of the present study demonstrated
that EMG amplitude values did not change for the
MG, SOL, and TA muscles for each 30-s stretch,
suggesting the participants did not voluntarily or
involuntarily plantarflex or dorsiflex their foot. In
addition, the mean values for the MG and SOL
muscles over all stretches were negligible with nor-
malized surface EMG responses being 1.6% of the
MVC values.
In conclusion, our findings demonstrated that
viscoelastic creep occurs at the same rate (slope)
and to the same extent (relative to the total increase)
over all four 30-s constant-torque stretches despite
no change (y-intercept and absolute position) in
ankle joint position following the third stretch. These
findings are in contrast to repetitive constant-angle
stretches held at the same final joint angle and are
likely due to the constant-torque nature of the
stretching protocol. The majority of increases in
position occurred within the first 15–20 s for all
four stretches, which is comparable with previous
studies examining both viscoelastic creep (Ryan et
al., 2010) and stress relaxation (McHugh et al., 1992;
McNair et al., 2000; Gajdosik 2006; Gajdosik et al.,
2006). Furthermore, the creep responses over all
stretches appear to be unrelated to muscle activation
as measured by surface EMG and are in agreement
with previous work by McHugh et al. (1992). From a
clinical standpoint, previous studies have suggested
that constant-torque stretching treatments appear to
be more effective reducing passive stiffness when
compared with constant-angle and cyclic stretching
modalities in hypertonic patients (Yeh et al., 2007).
However, we are aware of no studies that have
examined viscoelastic creep responses in depth dur-
ing repetitive constant-torque stretches. Future work
is necessary to determine how the number of repeti-
tions, duration, and intensity of stretches influence
the viscoelastic creep responses in an effort to pro-
vide evidence-based recommendations for clinicians
(McHugh et al., 1992; Magnusson et al., 2000; Behm
& Kibele, 2007).
Perspectives
The viscoelastic properties of stretch (e.g. stress
relaxation) have been studied extensively during
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Ryan et al
common static or constant-angle stretching maneu-
vers. Until recently, little work has been done to
examine constant-torque stretching procedures in
vivo. The results of this study demonstrate the
dynamics of viscoelastic creep during repetitive
stretches that are commonly performed in clinical
and athletic settings. From a practical standpoint, it
appears that the rate and amount of viscoelastic
creep are relatively unaffected during four 30-s
stretches in healthy recreational active college-aged
participants. In addition, the methodology used in
the current study may be used in future studies to
determine if aging, disease, or training influences the
properties of viscoelastic creep.
Key words: passive stiffness, electromyography,
constant torque, stretching.

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