ARTICLE IN PRESS
Manual Therapy 11 (2006) 192–196
Musculoskeletal adaptations to resistance training in old age
N.D. ReevesÃ, M.V. Narici, C.N. Maganaris
Institute for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, MMU Cheshire, Alsager Campus,
Hassall Road, Alsager, Cheshire ST7 2HL, UK
Received 27 October 2005; accepted 6 April 2006
Muscle weakness experienced in old age has many detrimental consequences for activities of daily life. Given the serious problems
presented by weakness in old age, strategies to prevent or mitigate this process are of paramount importance. In recent years
resistance training has emerged as an effective method for increasing strength in the elderly. Despite this, little is known regarding
the muscular, neural and tendinous adaptations that occur with resistance training in old age. Hence, we have conducted a series of
experiments to investigate these adaptations. We have found increases in maximal isometric and concentric torque by 9–37% after
resistance training in older people (65–81 years). Associated with these strength gains were increases in agonist muscle neural drive
without any change in the co-activation of antagonist muscles. Resistance training can cause increases in muscle size and also
adaptations to the internal muscle structure. Tendons of older adults adapt to resistance training by increasing their stiffness and
Young’s modulus. In conclusion, many of the musculoskeletal factors characterizing ageing can be at least partially mitigated by
r 2006 Elsevier Ltd. All rights reserved.
Keywords: Old age; Exercise; Muscle; Tendon
Ageing is characterized by a loss of muscle size known 1999; Frontera et al., 2000). This is primarily important
as senile sarcopenia and a progressive decline in strength because the extensors of the knee and ankle are the
that accelerates after the sixth decade of life. Cross- major muscle groups responsible for locomotion and
sectional comparisons of young and older adults have will therefore impact upon many activities of daily
shown that adults 70–80 years of age are 40% weaker living. For example, the loss of leg extension power with
in terms of knee extension and plantarﬂexion torque as ageing has been shown to correlate with the decline in
compared to young adults 20–30 years of age (Roos maximal gait velocity (Rantanen and Avela, 1997). As
et al., 1999; Klein et al., 2001; Macaluso et al., 2002; maximal leg extension power (normalized to body mass)
Morse et al., 2004). Senile sarcopenia affecting various declines, the maximal attainable gait velocity also
muscle groups is evident from cross-sectional studies declines. Power (the product of joint torque and
showing that muscle size is 20% smaller in older adults velocity) declines at a faster rate than joint torque with
as compared to young adults (Klein et al., 2001; Narici ageing (Skelton et al., 1994), likely due to the fact that
et al., 2003; Morse et al., 2004). The extensor muscle not only strength (joint torque) declines with ageing but
groups, particularly the knee and ankle extensors are also the velocity of muscle shortening. Given the
most severely affected by ageing-induced declines in detrimental consequences of muscle weakness in old
strength and size (Winegard et al., 1996; Lynch et al., age described above, it is of paramount importance to
ﬁnd ways in which this ageing-induced strength decline
ÃCorresponding author. Tel.: +44 161 2475429; can be delayed or even reversed to a certain extent.
fax: +44 161 2476375. In relatively recent years resistance exercise training
E-mail address: N.Reeves@mmu.ac.uk (N.D. Reeves). has been shown as an effective method for reducing
1356-689X/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
ARTICLE IN PRESS
N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 193
ageing-induced muscle weakness (for review see Maca-
luso and De Vito, 2004). Perhaps contrary to popular
belief, strength gains can be achieved in old age and
have been observed in 70–80 year old adults following
resistance exercise training programmes (e.g. Fiatarone
et al., 1990). Many studies however, have assessed
strength only in terms of the repetition maximum on the
exercise device used for training. Whilst this will clearly
provide an important indication of any possible strength
gains occurring with exercise training, due to the speciﬁc
nature of the task it is likely to overestimate the ‘‘true’’
strength gains. Dynamometry based measurements of
isometric and dynamic torque are required to accurately
quantify any training-induced changes following ex-
ercise programmes in older adults. Furthermore, it is
important to understand the origin of any possible
strength gains with resistance training and identify the
adaptations occurring in the different motor system
components of older adults. In order to address the
above issues we have conducted a series of studies
Fig. 1. Knee extensor torque–velocity relationship pre- and post-
investigating the musculoskeletal adaptations to resis-
training. Values are means and SD. * and ** denote signiﬁcantly
tance training in older adults. (Po0:05 and Po0:01, respectively) increased torque after 14 weeks of
Nine older adults completed a 14-week resistance resistance training. Modiﬁed from the data presented in Reeves et al.
exercise training programme and nine older adults (2005).
served as non-exercising controls (aged 65–81 years).
The training programme was performed using resistance
exercise machines (Technogym, Gambettola Italy). Ex- group, there were no changes in concentric or eccentric
ercises were performed for the major muscle groups of torque, but there was a signiﬁcant decrease in isometric
the upper and lower body in order to provide a whole- torque post-intervention. The strength gains brought
body conditioning stimulus. The major muscle groups of about by resistance training may be partly attributed to
interest from an experimental perspective in the present increased agonist (knee extensor muscles) neural drive.
study were the knee extensors. This muscle group Measurements of electromyographic (EMG) activity
was studied because of its crucial role in all locomotor taken from the vastus lateralis muscle showed increases
activities. The main exercises performed to target the ranging from 28% to 38% compared to pre-training
knee extensors were the leg-press and leg-extension. A values. During voluntary contractions, muscle force and
5-repetition maximum (5RM) was established for each torque is produced not only by the agonist muscles but
exercise (the maximum load that could be raised and also by the antagonist muscles, which are co-activated.
lowered under control, 5 times only). The training load During knee extension contractions, antagonist muscle
corresponded to 80% of the 5RM and the repetition co-activation (knee ﬂexors) has been shown to be higher
maximum was tested every 2 weeks in order to maintain in the elderly compared to young adults (Macaluso
the same relative training load. Two series of 10 et al., 2002). This may be regarded as a strategy to
repetitions were performed for each exercise and maintain a higher degree of knee joint stability in the
sessions were performed three times each week for 14 elderly. However, co-activation also functions to apply
weeks. Pre- and post-intervention maximal isometric, an opposing torque to the intended direction of effort.
concentric and eccentric knee extension torque was Higher levels of antagonist muscle co-activation there-
assessed using an isokinetic dynamometer. This device fore contribute to strength deﬁcits in old age. Some
allows torque measurements to be taken in all modes of studies suggest that resistance exercise training in older
contraction whilst allowing the external angular velocity adults can reduce the level of antagonist muscle co-
to be manipulated. These measurements enable con- activation (Hakkinen et al., 1998; Hakkinen et al.,
struction of the torque–velocity relationship (Fig. 1). 2001), an independent factor that would serve to
After training, older adults signiﬁcantly increased increase strength. In our study however, the level of
maximal isometric torque by 9% and maximal con- antagonist muscle co-activation was unaltered by
centric torque by 22–37% across the angular velocities resistance training, indicating that only changes in
tested (Reeves et al., 2005). In contrast to isometric and agonist muscle activation contributed to the observed
concentric torque, resistance training did not signiﬁ- strength gains. An interesting ﬁnding is that older adults
cantly alter eccentric torque (Fig. 1). In the control did not increase eccentric torque after resistance
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194 N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196
training. Explanations for this ﬁnding may include the number has increased both in-series (increased fascicle
preservation of eccentric force with ageing and under- length) and in-parallel (pennation angle increase) and
loading of the eccentric contraction phase during have implications for maximal force production and the
training. It has been shown from both animal and operating range length range of the muscle. Pennation is
human studies that eccentric force is relatively well a strategy to allow more contractile material to be
preserved with ageing in relation to isometric and packed along the length of the muscle, so theoretically a
concentric force (Vandervoort et al., 1990; Phillips et greater number of sarcomeres in-parallel suggests that
al., 1991; Hortobagyi et al., 1995). This relative force the muscle would be able to generate a greater
preservation may reduce the adaptability of this muscle maximum force. Although an increased number of
contraction type in response to exercise training. As sarcomeres in-series suggests that the muscle may be
illustrated by the force-velocity relationship (Fig. 1), able to produce force over a greater length range as
higher forces can be generated during eccentric contrac- compared to the situation before training with fewer
tions as compared to during isometric and concentric sarcomeres in-series, in vivo this is limited by joint
contractions (Cook and McDonagh, 1995). During constraints. Resistance training programmes for older
exercise training using the constant external load devices adults can therefore not only increase gross muscle area
employed in our study, the repetition maximum is but also cause alterations to the internal muscle
limited by the concentric contraction and therefore the structure. In addition to changes in gross muscle area,
eccentric contraction phase of the same movement will changes in muscle architecture are another muscular-
be under-loaded and may partly explain the lack of based factor contributing to the strength gains observed
adaptation in this contraction type with training. after resistance training.
A number of studies have shown that skeletal muscle Whilst most attention may intuitively be focused on
can still adapt to an exercise training stimulus even in the muscular adaptations to resistance training pro-
old age (e.g. Fiatarone et al., 1990; Hakkinen et al., grammes, potential adaptations occurring in other
1998; Harridge et al., 1999). Using imaging techniques musculoskeletal structures should be considered. For
such as magnetic resonance imaging (MRI) and example, tendons are the force-transmitting structures
computed tomography (CT) enlargement of muscle connecting muscle to bone, thus allowing the effective
anatomical cross-sectional area (ACSA) by 5–17% has transformation of contractile force in the muscle to joint
been reported in the elderly after resistance training movement. Tendons are not inextensible bodies, but
programmes lasting 3 months (Brown et al., 1990; elongate when they are subjected to the tensile load
Ferri et al., 2003). Indeed data from our laboratory generated by muscle contraction (for review see Butler et
agrees with these reports as we have found increased al., 1978). The tendon’s dimensions and mechanical
ACSA of the vastus lateralis muscle by 3–10% along the properties inﬂuence the degree of deformation that will
length of the muscle following 14 weeks of resistance take place in response to the application of a given
training (Reeves et al., 2004b). These ﬁndings suggest a tensile load. Information on the modiﬁcation of tendon
certain degree of reversal to the muscle atrophy mechanical properties with changes in activity level is
experienced with ageing. Although the enlargement of scanty as compared to the information available on
muscle size with resistance training is a major factor skeletal muscle. Some inferences however, can be drawn
contributing to the observed strength gains, it is not the from in vitro experiments on isolated tissues. In vitro
sole factor. As discussed above, neural factors con- studies suggest that ageing reduces tendon stiffness,
tribute substantially to increases in strength and other causing a greater tendon elongation for any given force
muscular and tendinous factors are also involved. In applied compared to younger tendons (Tkaczuk, 1968;
most human muscles, fascicles do not lie parallel to the Noyes and Grood 1976). Indeed the ﬁndings from
length of the muscle but insert into the tendinous sheath experiments performed on humans in our laboratory
known as the aponeurosis at an angle. The internal agree with in vitro reports (Maganaris, 2001). Animal
arrangement of muscle fascicles is referred to as muscle models (Woo et al., 1980, 1981, 1982; Buchanan and
architecture. We have previously observed that Marsh, 2001) have shown that when tendons undergo
muscle architecture is altered in old age. Gastrocnemius exercise loading above that normally experienced under
muscle fascicles were found to be shorter by 10% in the habitual conditions, they respond by increasing their
elderly compared to young adults and the angle at which stiffness (i.e. they become more resistant to elongation,
the fascicles inserted into the aponeurosis, known as the shown by a steeper slope of the force-elongation curve).
pennation angle, was smaller by 13% in the elderly By using ultrasound imaging to scan tendon elongation
(Narici et al., 2003). We have recently shown in the in vivo during an isometric contraction, we investigated
vastus lateralis muscle that following 14 weeks of the inﬂuence of resistance training on the mechanical
resistance training muscle fascicle lengths increase by properties (stiffness and Young’s modulus—stiffness
9% and pennation angles increase by 30% (Reeves normalized to the tendon’s dimensions) of the patellar
et al., 2004a). These ﬁndings suggest that sarcomere tendon in older adults. After 14 weeks of resistance
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N.D. Reeves et al. / Manual Therapy 11 (2006) 192–196 195
training we found that both tendon stiffness and the factors characterizing ageing can be at least partially
normalized stiffness, Young’s modulus increased by mitigated by resistance training.
65% and 69%, respectively (Reeves et al., 2003). The
increase in the tendon Young’s modulus suggests that The support received from Technogym and funding
the stiffness increase occurred to due a change in the
provided by the Italian Space Agency is acknowledged.
material properties of the tendon. These ﬁndings
indicate a certain degree of reversal of the ageing effects
on human tendons. The modiﬁcation of tendon References
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