ABSTRACT: The effect of strength training for 14 weeks on patella tendon

viscoelastic properties was investigated in a group of elderly individuals.

Participants were assigned to training (age [mean SD] 73.6 3.4 years;
n 7) or control (age 66.4 1.7 years; n 7) groups. Training was
performed three times per week and consisted of two series of 10 repetitions
of leg-extension and leg-press exercises at 80% of the 5-repetition maxi-
mum. Tendon elongation during an isometric knee-extension contraction
relaxation was measured using ultrasonography. Tendon stiffness was cal-
culated from the gradient of the estimated force elongation relationship and
mechanical hysteresis was calculated as the area between loading unload-
ing curves. Knee-exor coactivation, estimated from biceps femoris muscle
electromyographic activity, was unaltered (P 0.05) after the training and
control periods. No changes (P 0.05) were observed in stiffness or
hysteresis after the control period. In contrast, tendon stiffness increased
from 1376 811 to 2256 1476 N.mm1 (P 0.01) and hysteresis
decreased from 33 5 to 24 4% (P 0.05), after training. These
training-induced adaptations have implications for maximal muscle force,
rate of force development, and metabolic cost of locomotion.
Muscle Nerve 28: 74 81, 2003

STRENGTH TRAINING ALTERS THE

VISCOELASTIC PROPERTIES OF TENDONS
IN ELDERLY HUMANS
NEIL D. REEVES, MSc, MARCO V. NARICI, PhD, and CONSTANTINOS N. MAGANARIS, PhD

Centre for Biophysical and Clinical Research into Human Movement,

Manchester Metropolitan University, Alsager Campus, Hassall Road, Cheshire ST7 2HL, UK

Accepted 26 February 2003

Strength training in old age has been effective for
increasing muscle strength and size. Despite
6,1518,47
numerous reports on the adaptations of skeletal
muscles to strength training, so far no attention has
been paid to changes in tendon viscoelastic proper-
ties with regimens of increased loading in old age.
The primary role of tendons is the transmission
of contractile forces from muscle to bone, enabling
movement to occur.8 In vitro studies suggest that the
tensile stiffness of collagen tissues is reduced with
aging.43,44 Consistent with these ndings, recent in
vivo observations have shown that the tendons of
elderly humans are more compliant than those of
young adults.34 An increased stiffness of tendon and
aponeuroses by 9 57% has been reported in re-
sponse to periods of increased loading in animals
Abbreviations: BF, biceps femoris; EMG, electromyographic; MRI, mag-
netic resonance imaging; RM, repetition maximum; RMS, root mean square;
VL, vastus lateralis
Key words: elderly; hysteresis; stiffness; strength training; tendon
Correspondence to: N. Reeves; e-mail: n.reeves@mmu.ac.uk
2003 Wiley Periodicals, Inc.
and humans.26,27,52,53 An increase in tendon stiffness
is likely to result in a faster rate of force development
and reduced shortening of the in-series contractile
component.19,27 However, to our knowledge, no
studies have been performed to establish the extent
to which similar responses would occur in tendons of
elderly humans.
Tendons of the knee and ankle extensors also act
as springs that store and release elastic energy dur-
ing locomotion, thus minimizing the metabolic en-
ergy required to displace the body forward.3,9 The
energy dissipated upon tendon recoil is an indica-
tion of the internal damping of the tendon, known
as mechanical hysteresis. There is evidence from
animal and human studies that tendons performing
different physiological functions have similar values
of mechanical hysteresis.41,45 However, other studies
have shown that tendons subjected to high physio-
logical loads display a reduced mechanical hysteresis
compared with relatively low-stressed tendons.50,55,56
Consistent with these data, Kubo et al.26 found that
exercise training reduces the mechanical hysteresis
of adult human tendons. It is unknown whether
tendons of elderly humans would respond in a sim-

74 Tendon Viscoelasticity After Training MUSCLE & NERVE July 2003

ilar manner to a regimen of increased loading, but,
if they do, this adaptation might reduce the ener-
getic cost of locomotion.
To address these issues, we investigated the effect
of strength training on the viscoelastic properties of
patella tendons in elderly humans.
METHODS
Subjects. Fourteen elderly individuals provided
written informed consent to participate in this study,
which was approved by our institutional ethics com-
mittee. All subjects received medical clearance from
their general practitioners prior to undertaking the
training program. Subjects had no neurological or
musculoskeletal disorder that might prevent their
participation. None of the subjects had previously
performed any type of resistance training. Three
men and four women were assigned randomly to the
training group (age [mean SD] 73.6 3.4 years;
body mass 69.4 17.7 kg; height 162 10.7 cm)
and the remaining 7 subjects (3 men) were assigned
to the control group (age 66.4 1.7 years; body
mass 72.5 16.4 kg; height 166.2 12.1 cm).
Strength Training. Progressive isotonic resistance
training was performed three times per week for 14
weeks. All exercises were performed using Techno-
gym resistance machines (Technogym, Gambettola,
Italy) after having completed a 510-min warm-up
on a cycle ergometer at 60 65% of age-predicted
maximum heart rate.31 Specic exercises performed
for loading the patella tendon were: (1) bilateral leg-
extension for the knee-extensor muscle group; and
(2) bilateral leg-press for the hip, knee, and ankle
extensors. Other exercises performed were bilateral
calf-raise, chest-press, seated-row, abdominal-crunch,
and lower back extension. During the rst 2 weeks
of training, subjects became familiarized with the
exercises and gradually increased their work load
until they were able to lift the highest possible load
5 consecutive times (5-repetition maximum [5 RM])
for each exercise. It was believed that the 5 RM was
more appropriate for elderly individuals who were
unaccustomed to this type of strenuous exercise, as
an alternative to the 1 RM. A similar approach has
been used previously for assessing maximum
strength on the training devices in young11,14 and
elderly48 subjects. The 5 RM was determined every 2
weeks to assess any strength increases, so that the
same relative training intensity could be maintained.
All exercises were performed with the concentric
phase of the contraction lasting 2 s, followed by a
3-s eccentric phase. One specic warm-up set of 15
Tendon Viscoelasticity After Training
repetitions was performed on each exercise at an
intensity of 45% of the 5 RM. As part of the warm-up
process, two or three sets of static stretching for the
specic muscle groups were performed for each ex-
ercise. For each of the lower limb exercises, two
training sets of 10 repetitions were performed,
initially at an intensity of 60 70% of 5 RM pro-
gressing to 80% of 5 RM within 13 weeks, depend-
ing upon the subjects capabilities. According to the
formula proposed by Brzycki,7 80% of the 5 RM
corresponds to approximately 70 75% of the pre-
dicted 1 RM. The aforementioned formula has been
derived from measurements in young adults, but it
has also been used for the prediction of the 1 RM
from repetitions to fatigue in elderly individuals.48
During the sessions, all subjects wore heart-rate
monitors, and if the heart rate rose to within 15
beats per min of the age-predicted maximum, the
exercise was stopped. A recovery period of 3 min
was introduced between exercise sets. Subjects were
observed very closely during all exercises to ensure
the correct technique was performed and to provide
verbal encouragement to maintain motivation. Com-
pliance to training was very high, with only 7% of
sessions missed due to such factors as holidays or
illness.
Study Design. All subjects were tested at baseline.
Seven subjects were retested after 14 weeks of train-
ing (training group). Seven subjects continued their
usual activities and were retested after 14 weeks of
normal activity (control group).
Measurement of Maximal Knee-Extension and Flexion
Joint Moment. Maximal isometric knee-extension
and exion torque was measured at a 90 knee angle
(full extension 0), with the hip angle at 85
(supine position 0), using an isokinetic dyna-
mometer (Cybex NORM, Ronkonkoma, NY). Straps
were positioned at the hip, shoulders, and over the
right thigh to prevent any extraneous movement. All
measurements were performed on the right leg. Sub-
jects had previously visited the laboratory on at least
one occasion to become familiar with the proce-
dures involved. Signals of torque and electromyo-
graphic (EMG) activity were displayed on the screen
of a computer (Macintosh G4, Apple Computer,
Cupertino, CA), interfaced with an acquisition sys-
tem (Acknowledge, Biopac Systems, Santa Barbara,
CA) used for analog-to-digital conversion, sampling
at a frequency of 2000 Hz.
Measurement of Electromyographic Activity. The
EMG activity of the vastus lateralis (VL) muscle and
MUSCLE & NERVE July 2003 75
the long head of the biceps femoris (BF) muscle was
measured in order to assess the effect of training on
agonist and antagonist muscle actions. Two self-
adhesive AgAgCl electrodes 10 mm in diameter
(Medicotest, Rugmarken, Denmark) were placed in
a bipolar conguration with a constant interelec-
trode distance of 20 mm, at a site corresponding to
the distal one-third of the length of the muscle.58
Electrodes were placed in the midsagittal plane of
each muscle, guided by axial-plane ultrasound scan-
ning in an attempt to minimize crosstalk from adja-
cent muscles. In order to estimate the common EMG
signals between the VL and BF muscles, a cross-
correlation analysis was performed.33,54 An r-value of
0.144 was obtained, indicating the presence of neg-
ligible crosstalk (2%) between these two muscles.51
The reference electrodes were placed on the lateral
tibial condyle. Electrode placement was always pre-
ceded by shaving, skin abrasion, and cleaning with Figure 1. The biceps femoris muscle RMS EMG activity as a
function of isometric knee-exor torque. Values expressed as
an alcohol-based solution to reduce skin impedance
means, corresponding to 25%, 50%, 75%, and 100% of isometric
to below 5000 . The location of all electrodes with knee exor torque (n 6).
respect to anatomical landmarks was recorded and
also traced onto an acetate sheet to ensure identical
placement on subsequent sessions. The raw EMG and 0.4-mm gap. The patella tendon moment arm
signal was preamplied and ltered using high- and length was dened as the perpendicular distance
low-pass lters of 10 and 500 Hz, respectively between the tibiofemoral contact point and the mid-
(Biopac Systems). At the timepoint corresponding to point of the patella tendon4,24 (Fig. 2). Due to con-
the highest torque during a maximal knee-exten- straints of the available coil it was only possible to
sion, the root mean square (RMS) EMG activity of image the knee joint at full knee-extension. The
the VL and BF muscles were measured. To deter- previously reported4 ratio of the patella tendon mo-
mine maximal activation of the BF muscle when ment arm length between 0 and 90 of knee-exion
acting as an agonist, EMG activity of the BF muscle (0.994) was used to estimate the moment arm length
was measured during a maximal knee-exion at the at 90 of knee-exion for each subject.
timepoint corresponding to maximal torque. The
antagonist torque of the knee exors during a knee- Calculation of Patella Tendon Force. Patella tendon
extension contraction was calculated assuming a lin- forces were calculated from the moment equilibrium
ear EMGtorque relationship,30 from the EMG equation around the knee joint at intervals of 20% of
torque relationship of the BF muscle when acting as maximal knee joint torque. At each torque level
an agonist.23,36 This assumption was conrmed from examined, the estimated coactivation torque of the
additional tests in a subsample of elderly individuals knee exors was added to the net joint torque mea-
(Fig. 1), conrming previous reports.1 Measure- sured during knee-extension and the sum was di-
ments of EMG activity were analyzed over a 50-ms vided by the estimated tendon moment arm length.
period, and were normalized for a 1-s period.
Measurement of Patella Tendon Elongation. Elonga-
Patella Tendon Moment Arm Length Measurement. tion of the patella tendon was assessed using B-mode
The patella tendon moment arm length was mea- ultrasonography (ATL-HDI 3000, Bothell, WA) dur-
sured from sagittal-plane magnetic resonance imag- ing a maximal knee-extension contractionrelax-
ing (MRI) scans taken with a 0.2-T magnet (E-Scan, ation, using previously reported methods.35,37,38,41
Esoate Biomedica, Genoa, Italy) to allow calculation Measurements were taken after four maximal iso-
of tendon forces (Fig. 2). Scans were taken using a metric knee-extension contractions were performed
T1-weighted spin echo sequence with the following to precondition the tendon.46,57 Subjects were in-
scanning parameters: time to echo (TE), 26 ms; time structed to perform a maximal knee-extension con-
of repetition (TR), 850 ms; eld of view, 180 180 traction attempting to reach maximal torque within
mm; with a 256 192 matrix; 4-mm slice thickness, 1 s, to maintain this for 12 s, and then relax com-

76 Tendon Viscoelasticity After Training MUSCLE & NERVE July 2003


Figure 2. Typical sagittal-plane MRI scan of the knee joint in full
extension. The length of the perpendicular dashed line, CA,
illustrates the patella tendon moment arm length.
pletely upon a verbal signal. Preliminary measure-
ments demonstrated that complete relaxation from
a maximal contraction typically occurs within 500
ms. A 7.5-MHz linear-array transducer was placed
over an echo-absorptive external marker xed on
the skin with surgical tape and positioned in the
sagittal plane at the level of the patella tendon (Fig.
3). The transducer was secured by a custom-built
external xator and held in position by the experi-
menter. Ultrasound scanning was optimized for im-
age quality, while the sampling frequency remained
above 30 Hz. Ultrasound scans were recorded onto
S-VHS videotape at 50 Hz for subsequent analysis.
All measurements were synchronized with signals
captured by the acquisition system using an external
marker. The displacement of the apex of the patella
was measured with respect to the line cast on the
ultrasound image by the external marker (Fig. 3).
This displacement was assumed to represent the
elongation of the patella tendon. In trials where
movement of the line cast on the ultrasound image
by the external marker occurred during contrac-
tionrelaxation, the data obtained were omitted
from further analysis. Measurements of displace-
ment were analyzed at intervals of 20% of maximal
joint torque on both the loading and unloading
phases, using digitizing software (NIH Image, ver-
sion 1.61, National Institutes of Health, Bethesda,
MD). The mean of three measurements for each
image was used for further analysis.
Calculation of Patella Tendon Stiffness, Hysteresis, and
Rebound Resilience. Patella tendon stiffness
(N.mm1) was calculated during the loading phase,
from the gradient of the force elongation relation-
ship over the interval 60 100% of maximal force.
Tendon Viscoelasticity After Training
Force elongation data in loading unloading phases
of contraction were tted with a spline and the area
under each curve was measured using digitizing soft-
ware. The mechanical hysteresis was dened as the
area between the loading and unloading curves and
expressed as a percentage:
Mechanical hysteresis (L UnL)/L 100
where L the area under the loading curve and
UnL the area under the unloading curve. The
reciprocal of hysteresis, rebound resilience, was cal-
culated as:
Rebound resilience
100 mechanical hysteresis value
Statistical Analysis. Data were analyzed using a 2
(group: training or control) 2 (time: pre or post)
factorial analysis of variance (ANOVA) and followed
by post hoc test using the Scheffe procedure, where
necessary. Baseline differences between the two
groups were tested for all measured variables using
independent-sample Students t-tests. Changes in
5-RM strength before and after training were ana-
lyzed using Students t-tests for paired samples. Data
are presented as mean standard deviation.
RESULTS
No differences (P 0.05) were found between the
two groups at baseline on any of the measured vari-
ables. Body mass was unchanged (P 0.05) in either
group following the training and control periods.
The 5 RM for the leg-extension exercise increased
from 40.7 11.7 kg before training to 47.5 14.7 kg
after training (17% increase, P 0.01). For the
leg-press exercise, the 5 RM increased from 165
42.9 kg before training to 198.1 53.2 kg after
training (20% increase, P 0.01).
Patella tendon stiffness increased from 1375.5
811.2 N.mm1 before training to 2256.1 1475.5
N.mm1 after training (64%, P 0.01; Table 1).
Before and after both the training and control peri-
ods, the patella tendon loading unloading curves
produced an open hysteresis loop (Figs. 4 and 5).
However, the tendon returned to its original resting
position 341 109 ms after the knee-joint torque
had returned to zero, indicating that the tendon did
not exceed its elastic limit. The tendon mechanical
hysteresis decreased from 32.7 4.7% before train-
ing to 23.5 4.1% after training (P 0.05; Fig. 4).
Therefore, the tendon rebound resilience increased
MUSCLE & NERVE July 2003 77
Figure 3. Typical sagittal-plane ultrasound scans of the patella tendon in one subject at rest and maximal tendon force before (a) and after
(b) training. Arrows indicate the reference point, which shows reduced displacement at maximal tendon force after training. External
marker is indicated by the arrowhead (X).

from 67.3 4.7% before training to 76.5 4.1%
after training (P 0.05). In contrast, no changes in
stiffness, mechanical hysteresis, or rebound resil-
ience were observed after the control period (P
0.05; Table 1).
The estimated maximal tendon force increased
from 2915.5 991.7 N before training to 3484.4
1249.3 N after training (20% increase, P 0.01;
Table 1). In the control group, the estimated maxi-
mal tendon force decreased from 3374.6 1230.9 N

Table 1. Measured and estimated variables before and after the training and control periods.
Training group Control group
Pre Post Pre Post

Leg-extension 5 RM (kg) 40.7 (11.7) 47.5 (14.7)
Leg-press 5 RM (kg) 165 (42.9) 198.1 (53.2)
Stiffness (N.mm1) 1375.5 (811.2) 2256.1 (1475.5) 1167.7 (615.7) 847.9 (241)
Hysteresis (%) 32.7 (4.7) 23.5 (4.1)* 29.5 (9.5) 30.1 (4.5)
Rebound resilience (%) 67.3 (4.7) 76.5 (4.1)* 70.5 (9.5) 69.9 (4.5)
Maximum tendon force (N) 2915.5 (991.7) 3484.4 (1249.3) 3374.6 (1230.9) 2843.1 (933.5)
Coactivation (%) 33.1 (27.9) 35.6 (26.7) 34 (15) 32.6 (19.6)
VL EMG (mV.s) 5.012 (3.122) 7.322 (5.892) 0.102 (6.452) 7.542 (5.92)*

Data presented as mean (SD). EMG, electromyogram; RM, repetition maximum; VL, vastus lateralis.
*P 0.05 versus pretraining or control periods.

P 0.01 versus pretraining or control periods.

78 Tendon Viscoelasticity After Training MUSCLE & NERVE July 2003


Figure 4. Patella tendon force elongation relations before and
after strength training for 14 weeks. The arrows indicate the
loading and unloading directions. Values are means (n 7);
maximal SD values are shown in Table 1.
before to 2843.1 933.5 N after the control period
(16% decrease, P 0.01). Coactivation of the knee
exors during a maximal knee-extension did not
change signicantly after the training or control
periods (Table 1). The EMG activity of the VL mus-
cle during maximal isometric knee-extension
showed a tendency to increase following training
and decreased after the control period (Table 1).
The latter nding in the control group is consistent
with the respective change in estimated maximal
tendon force, thus indicating exertion of reduced
voluntary efforts after the control period.
of young adults.34 Strength training may, therefore,
reverse this aspect of aging to a certain extent, caus-
ing tendons in the elderly to become stiffer, as in
young adults. Indeed, the greater training-induced
increase in tendon stiffness in the present study,
compared with previous reports,26,27 may indicate a
greater responsiveness of tendons in the elderly to
levels of increased loading than in young adults.
Increased tendon stiffness after training would
increase the rate of force development by contrac-
tion.22 This may result in a faster application of
external breaking forces, which is necessary, for ex-
ample, to decelerate the body mass in response to a
perturbation in balance.2,32 The increased tendon
stiffness after training may also have implications for
the lengthtension relation of the quadriceps mus-
cle group. It has been reported that the constituent
muscles of the human quadriceps act over the as-
cending limb and the plateau region of the sarco-
mere lengthtension relation.13 These data suggest
that increased patella tendon stiffness, causing re-
duced ber shortening, would displace the average
sarcomere operating range closer to the plateau re-
gion, thus shifting the optimal angle of quadriceps
muscle force generation toward full knee-extension.
The mechanisms contributing to increased tendon
stiffness after strength training are unclear. How-
ever, increased diameter and packing density of col-
lagen brils and changes in collagen crimp structure
are likely factors, as shown by animal studies.42,57
The present nding of reduced mechanical hys-
teresis after strength training (Fig. 4), coincides with

DISCUSSION

The present study demonstrates that 14 weeks of

strength training in elderly subjects alters the vis-
coelastic properties of the human patella tendon.
Training increased patella tendon stiffness by 64%
and reduced hysteresis by 28% (Fig. 4 and Table 1).
The increased tendon stiffness after training is con-
sistent with previous reports in young adults, show-
ing an increased stiffness of tendon structures by
1557% following strength training.26,27 However,
these reports were based on measurements of apo-
neurotic length. Aponeuroses show variable elonga-
tion along their lengths and are considerably more
compliant than free tendons.29,39,40 The nding of
increased stiffness after training is also consistent
Figure 5. Patella tendon force elongation relations before and
with reports from animal studies.52,53,55,56 Prelimi- after the 14-week control period. The arrows indicate the loading
nary ndings from our laboratory suggest that ten- and unloading directions. Values expressed as means (n 7);
dons of the elderly are more compliant than tendons maximal SD values are shown in Table 1.

Tendon Viscoelasticity After Training MUSCLE & NERVE July 2003 79

in vitro animal studies showing that tendons subject
to high physiological loading levels exhibit lower
mechanical hysteresis than tendons subjected to
smaller loads.50,55,56 Results in a wider range of mam-
mals suggest that tendon mechanical hysteresis is
independent of the loading to which the tendon is
subjected under normal loading.41,45 It should be
emphasized, however, that the previously mentioned
ndings do not reect loading levels above those
usually experienced under physiological conditions.
Indeed, Kubo et al.26 found a 42% reduction in the
mechanical hysteresis of the human gastrocnemius
tendon aponeurosis after combined strength and
stretching training in young humans. However, they
failed to demonstrate any effect on mechanical hys-
teresis by strength training alone, which contrasts
with our ndings. This discrepancy suggests that the
viscous component in tendons of elderly subjects
may be more responsive to mechanical loading than
tendons of younger subjects.
The present baseline estimate of tendon mechan-
ical hysteresis of 31% is comparable with previous
values from in vitro studies (24 38%).12,21,49,50 Our
estimate, however, is higher than the average me-
chanical hysteresis value of 10% reported from
measurements on adult mammals.5,25,45 This discrep-
ancy may be accounted for, in part, by aging-induced
increases in the mechanical hysteresis of tendon.21
Moreover, our in vivo method cannot exclude fric-
tion of the tendon and the patella as they pass over
internal structures, such as the fat-pad lying poste-
rior to the patella tendon. Internal friction is likely
to oppose tendon recoil and result in overestimation
of hysteresis as compared with in vitro conditions.
Interestingly, the mechanical hysteresis value of
24% after strength training approaches previous in
vivo reports in young subjects of 19% for the human
tibialis anterior tendon,38 and 21% and 19% for
the gastrocnemius tendon aponeurosis,26,28 which
indicates adaptations toward more rebound-resilient
structures similar to those in young adults. Since the
patella tendon may store and release elastic energy
during locomotion,3 our nding of training-induced
reductions in mechanical hysteresis suggests that
knee-extensor strength training in the elderly might
lead to metabolic energy savings during locomotor
tasks, especially those involving higher speeds than
spontaneous walking speed. However, these ndings
would be of greater relevance and importance for
locomotion in tendons of the plantarexors. A pos-
sible mechanism for reduced mechanical hysteresis
following strength training may be a change in the
uid phase of the tendon, as this has been shown to
inuence the tendons time-dependent behavior in
80 Tendon Viscoelasticity After Training
the toe region.10,20 This force region has been shown
to correspond to tensile loads generated by muscle
contraction.29,35
This study was partly supported by Italian Space Agency (ASI)
funds. The authors thank Technogym (Gambettola, Italy) for
providing the resistance machines used in this study.
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