Eur Rev Aging Phys Act (2012) 9:109–117

DOI 10.1007/s11556-012-0102-8

ACADEMIC LITERATURE REVIEW

Muscle weakness in the elderly: role of sarcopenia,

dynapenia, and possibilities for rehabilitation
Teet Seene & Priit Kaasik

Received: 22 November 2011 / Accepted: 18 April 2012 / Published online: 4 May 2012
# European Group for Research into Elderly and Physical Activity (EGREPA) 2012

Abstract Aging is a multifactorial process leading to those over the age of 80 years are sarcopenic [34, 52]. If the
changes in skeletal muscle quantity and quality, which cause loss of muscle mass is more than 5 % in 6–12 months, the
muscle weakness and disability in the aging population. term mypenia has been suggested for use [25]. Aging and
This paper discusses the reasons for muscle weakness— inactivity or disuse is associated with a decline in muscle
and its biological and physiological mechanisms—in the mass, structure, and strength [23, 77]. A sedentary lifestyle,
elderly and describes the role of sarcopenia and dynapenia, bed rest, spaceflight, and hindlimb suspension lead the
and the possibilities to modify the age-associated decline in skeletal muscle to microcirculatory disturbances, atrophy,
muscle function and decelerate the development of muscle protein loss, changes in contractile properties, and fiber-
weakness and disability. Resistance and endurance training type switching [23, 33, 63, 95]. In both young and aged
are effective measures of exercise therapy in the elderly, skeletal muscle, oxidative stress increases in response to
which improve muscle metabolism and thereby muscle unloading [84] and may have an important role in mediating
function and life quality. muscle atrophy. Unloading results in a decrease in the
number of myonuclei and an increase in the number of
Keywords Aging . Sarcopenia . Dynapenia . Muscle apoptotic myonuclei in skeletal muscle [46].
weakness . Exercise therapy Heat-shock protein 70 inhibits caspase-dependent and
caspase-independent apoptotic pathways and may function
in the regulation of muscle size via the inhibition of necrotic
Introduction muscle fiber distribution and apoptosis in aged muscle [59].
The decline in muscle mass primarily results from type II
Sarcopenia has been considered to be a minor modifiable fiber atrophy and loss in the number of muscle fibers.
risk factor for health outcomes, and it plays a significant role Increased variability in fiber size; accumulation of non-
in the etiology of disability [14, 45]. Sarcopenia is under- grouping, scattered, and angulated fibers; and the expansion
stood as an age-related loss of muscle mass, muscle of extracellular space are characteristic of muscle atrophy
strength, and physical function [23]. The term sarcopenia [8]. Beyond the loss of muscle size due to reduced fiber
has been defined as the age-related loss of muscle mass and number and myofibrillar proteins that underlie muscle
dynapenia as the age-related loss of muscle strength [13]. weakness in the elderly [13, 23], impairments in neural
The rate of muscle loss has been established to range activation have been found, as well as potential alterations
from 1 to 2 % per year past the age of 50 years, as a result of in other muscular properties that may reduce contractile
which 25 % of people under the age of 70 years and 40 % of quality defined as a reduction in involuntary force produc-
tion per unit muscle size [31, 86, 100]. The functional and
T. Seene (*) : P. Kaasik structural decline of the neuromuscular system is a recog-
Institute of Exercise Biology and Physiotherapy, nized cause of decreased strength, impaired performance of
University of Tartu,
daily activities, and loss of independence in the elderly [51].
Ülikooli Str 18,
Tartu 50090, Estonia Loss of muscle strength in older adults is weakly associated
e-mail: [email protected] with the loss of lean body mass [29]. It means that muscle
110 Eur Rev Aging Phys Act (2012) 9:109–117

weakness in older adults is more related to impairments in Regeneration capacity of sarcopenic muscle
neural activation and/or reductions in the intrinsic force-
generating capacity of skeletal muscle [51]. Aging is a physiological process that includes a gradual
Research data suggest that the number and magnitude of decrease in skeletal muscle mass, strength, and endurance
associations for low physical performance or disability are coupled with an ineffective response to tissue damage [18].
greater for low muscle strength than low muscle mass [29]. Aging and a reduced physical level are mainly responsible
At the same time, it has been shown that higher aerobic for the progressive decline in several physiological capaci-
capacity is related to an increase in the abilities of cardio- ties in the elderly [39]. Decrease in the protein synthesis rate
vascular factors in the elderly [73]. But it is still unclear is affected by the translational process occurring in older
whether aerobic exercise training is superior to resistance human skeletal muscle, whereas the transcriptional process
training or other exercise models in altering effect on the appears to be unaltered when compared with those in youn-
elderly [58]. However, it is clear that purposeful life-long ger men [69]. Skeletal muscle fibers have a remarkable
physical activity (exercise therapy) has been proven to have capacity to regenerate [5, 69], and this depends on the
a positive effect on health via many disease-specific mech- number of satellite cells under the basal lamina of fibers
anisms and seems to provide the highest health benefits and their oxidative capacity [83]. Autografting of gastroc-
[44]. nemius muscle in old rats shows that regeneration proceeds
The purpose of the present review was to analyze the at a significantly slower rate in comparison with young
reasons for aging skeletal muscle weakness and the role of animals [38]. A decrease in the number of satellite cells
sarcopenia and dynapenia in this process and to evaluate has been shown in fast-twitch muscle fibers of elderly sub-
possibilities for decelerating the development of muscle jects [98]. In sarcopenic muscle, the decrease in the satellite
weakness and disability in the aging population. We also cell pool and the length of telomeres might explain the
intend to examine the decelerative effect of exercise therapy higher prevalence of muscle injuries and delayed muscle
on the structure and function of aging skeletal muscle. regeneration [39]. Functionally heterogeneous satellite cells
with different properties may be recruited for different tasks,
for example, muscle regeneration [49, 61, 92].
Etiology of muscle weakness and disability in the elderly After severe damage, muscles in old rodents did not
regenerate as well as muscles in adults [10, 17]. The de-
Sarcopenia creased regeneration capacity of muscles is likely due to
extrinsic causes rather than an intrinsic limitation of muscles
Aging leads to changes in skeletal muscle quantity and [10, 17]. A contraction-induced muscle injury to weight-
quality, and these changes are a major cause of the increased bearing muscles in old rodents causes deficits in muscle
prevalence of disability in the aging population [23, 24, 71, mass and force [67]. It has been shown that the degradation
77]. In addition to sarcopenia, osteopenia and organopenia rate of contractile proteins in rat skeletal muscle during
are characteristic of increasing age [50] and may contribute aging increased about two times, and muscle strength and
to the development of disability. motor activity decreased at the same time [38]. Aging-
About two decades ago, sarcopenia was already defined induced sarcopenia is a result of decreased synthesis and
as the age-related loss of muscle mass [37]. Nowadays, we increased degradation of myofibrillar proteins, which leads
know that muscle mass and strength are causally linked and to the slower turnover rate of muscle proteins, particularly
that changes in mass are responsible for changes in strength contractile proteins, and this, in turn, leads to the decrease in
[29]. About three decades ago, it was shown that muscle muscle strength [23, 24, 38]. It has been shown that increas-
strength does not solely depend on muscle mass [56]. In ing dietary protein intake in combination with the use of
elderly people, the decline in muscle strength is more rapid anabolic agents attenuates muscle loss [23]. In essence,
than the concomitant loss of muscle mass [11, 19, 28, 31], sarcopenia is an imbalance between protein synthesis and
and loss of muscle mass during disuse is associated with degradation rate (Fig. 1).
loss of strength only in the range of 10 % [12, 15]. This
standpoint is also supported by the experiments where mus- Dynapenia
cle mass is gained but the age-related decline in muscle
strength is not prevented [19]. As muscle size is not the sole contributor to loss in physical
Thus, the aforementioned standpoint that the loss of activity in the elderly, it is important to evaluate all aspects
muscle strength in elderly people is weakly associated in the etiology of disability. In the literature, there are many
with the loss of lean body mass demonstrates that the descriptions for the identification of risk factors for loss in
loss of strength is more related to impairments in the physical activity among the elderly [6, 14]. The decline in
neural activation of muscle [29]. muscle strength is a result of a combination of neurologic
Eur Rev Aging Phys Act (2012) 9:109–117 111

Fig. 1 Factors supporting the

Reduction in total motor
development of loss of muscle Chronic inflammation unit number
mass and strength in the elderly Changes in hormonal
ansemble
Loss of muscle fiber
Decrease in number and size
Decrease in anabolic physical activity
and increase in catabolic
processes in muscle
Structural changes in
muscle fibers
Decrease in muscle fibre
regenerative capacity
SARCOPENIA Imbalance between rates
of muscle protein
Alterations in immune synthesis and degradation
function

Impairment of neural activation

Muscle fiber type
transformation
DYNAPENIA Exitation – contraction
uncoupling
Changes in contractile
proteins isoforms pattern
Reduction in functional reserve

Infiltration of adipocytes
into muscle fibers Decrease in vital capacity
Reduction
in muscle
Deterioration of capillary contractile
blood supply quality

and muscular factors, such as the impairment of neural mitochondrial ATP production [1]. It has been demonstrated
activation due to a reduction in descending excitatory drive that in both humans and rodents, skeletal muscle mitochon-
from supraspinal centers, suboptimal motor unit recruit- drial dysfunction occurs with age [4, 70]. The reason is a
ment, and neuromuscular transmission failure [14, 31, 86, decrease in mitochondrial DNA copy numbers, decreased
100]. Muscle atrophy, reduced contractile quality due to mRNA in genes encoding muscle mitochondrial proteins
changes in the myofibrillar machinery, and infiltration of [4], reduced oxidative enzyme activity, and a decreased
adipocytes into muscle fibers are also reasons for the de- mitochondrial protein synthesis rate [82]. Neuronal or
crease of muscle strength and physical activity [14, 19, 72, chemical mediators may also play a role in signaling
77]. Taking all these into account, Clark and Manini [13, 14] hypothalamus from the periphery to stimulate the center
described the age-related loss of muscle strength using the of sympathetic nerves signaling the paraventricular nu-
term dynapenia. cleus of the hypothalamic center [57]. It is generally
A decrease in skeletal muscle strength contractile protein known that skeletal muscle protein synthesis in humans
synthesis rate and an increase in muscle protein degradation decreases with age [3, 70, 81, 102]. Studies have shown
rate demonstrate that the contractile machinery in the elderly that the synthesis rate of MyHC and mitochondrial
is structurally and functionally damaged (Fig. 1). Such an proteins decreases, but others like sarcoplasmic proteins
integral indicator of contractile protein metabolism as their have a relatively high synthesis rate in the elderly [57].
turnover rate shows that in senescent rats, myosin heavy It has been shown that the age-related decrease in
chain (MyHC) turned over about 35 % and actin about 10 % muscle protein is not a global effect on all proteins,
more slowly than in young elderly [38, 76]. Functional but is selective for certain proteins [57]. Proteins that
rearrangements in the contractile apparatus of senescent rats have a faster turnover rate contribute more to the skel-
also show a decrease in MyHC fastest isoform relative etal muscle synthesis rate despite their small amount.
content in skeletal muscle [64]. Changes in MyHC isoform’s Proteins which constitute a major part of muscle pro-
composition in skeletal muscle may be related to slower teins but have a slow turnover rate play a smaller role
ATP splitting in the elderly because of a decrease in muscle in the synthesis rate of skeletal muscle proteins [57].
112 Eur Rev Aging Phys Act (2012) 9:109–117

Effect of unloading and reloading on muscle quantity the recovery of muscle strength and is related to the regen-
and quality in the elderly eration of muscle structures from disuse atrophy [36]. Mus-
cle metabolism can be restored faster than the full recovery
Unloading of muscle function as the cross-sectional area and myonu-
clear domain size require more time for restoration of neural
The gradual development of functional limitations over an and mechanical properties of muscle [20, 60].
extended period of time is affected by a natural age-related It has also been proposed that aging militates against the
decline in physical and biological properties, which already loss of collagen stability due to mechanical overextension
starts in midlife and increases the risk for a decline in [101], but the growth hormone is more important in
physical functioning in later life [99]. strengthening the matrix tissue than forming muscle fiber
During aging, the physical system suffers to a different hypertrophy in aged musculotendinous tissue [21]. After
extent and rate in diverse parts of the body. This results in severe damage, muscle in old rodents does not regenerate
reduced functional reserve, a decrease in vital capacity, as well as muscle in adults [17]. A contraction-induced
deterioration of the capillary blood supply, and a decrease muscle injury to weight-bearing muscles in old age causes
in muscle mass [53]. deficits in muscle mass and force [67]. The fact that an
Due to living a sedentary life in older age, inactivity can increase in muscular strength lags behind that in muscular
lead to a loss of functional health due to deficits in strength, mass shows that an increase in muscular mass contains
endurance, and flexibility [53]. “Use it or lose it” has been functionally immature muscle fibers during the recovery
shown to be a key rule for maintaining physical indepen- process following disuse atrophy [77].
dence in the elderly [68]. One of the reasons for the devel-
opment of muscle weakness in the elderly is decreased
physical activity [66]. Inactivity and aging cause a marked Effect of exercise therapy on muscle weakness
relative increase in the endo- and perimysial connective in the elderly
tissue, which results in changes in the mechanical properties
of the skeletal muscle [22]. Myofibrillar basal lamina Resistance exercise training
becomes thicker and more rigid with age, and increased
cross-linking of collagen molecules makes fibrils more re- Muscle weakness is the main factor in the dysfunction of
sistant to degradation by collagenase [30]. The muscle tissue locomotory activity and balance not only in the elderly but
response to unloading seems to more expressed than the also during the first months of a newborn’s life activity. It
connective tissue response [41, 48]. The connective struc- has been shown that an increase in muscle strength is in
tures are protected from rapid changes in tissue mass, while good agreement with the development of the baby’s con-
the muscle, which is known to act as a protein store of the trolled movements during the first 5 months of life [79].
organism, is subject to substantial and fast changes in tissue This fact in turn shows the importance of muscle strength in
mass. Despite the small changes in connective tissue mass, human everyday activity. It has been demonstrated that
important changes occur in the tissue structures during exercise programs incorporating balance training are effec-
unloading and aging [77]. tive in reducing falls in older people [90].
Unloading has been shown to decrease the protein syn- Elderly people were 59 % weaker than young, but a 6-
thesis rate in skeletal muscle by 46 % [27]. Decreased month resistance training improved muscle strength in the
muscle mass, reduction in strength, and aerobic capacity old group and was only 38 % lower than in the young group
are the typical changes in the elderly during bed rest [23]. [54]. During aging, muscle power declines more rapidly
An increase of dietary protein intake attenuates protein than strength [55]. Resistance training improves the
degradation rate during bed rest [87] and, in combination power-producing capacity of skeletal muscle fibers in the
with anabolic agents, prevents muscle loss [23, 40, 91]. elderly due to the increase of contractile velocity [96].
Resistance training is a strong stimulus for skeletal mus-
Reloading cle metabolism in the elderly, particularly for the contractile
apparatus as the fractional synthesis rate of myofibrillar
Due to the differences in the plasticity of young and old proteins in the skeletal muscle increases [64]. Compensatory
skeletal muscle, young muscle mass increases faster than hypertrophy of plantaris muscle by tenotomy of the gas-
old after reloading [88], but the recovery of muscle strength, trocnemius muscle decreased the relative content of MyHC
both in young and old, takes more time than gain of muscle IIb and IIa isoforms in old rats. Simultaneous compensatory
mass [65]. Regaining muscle strength after unloading takes hypertrophy and heavy resistance training increased the
longer in old than in the young [88]. The recovery of proportion of MyHC IIb and decreased the relative content
locomotory activity after hindlimb suspension is as fast as of MyHC IId isoform in old animals’ muscles [64]. If the
Eur Rev Aging Phys Act (2012) 9:109–117 113

intensity and volume ratio is properly regulated in heavy skeletal muscle proteins depends on the functional activity
resistance training, it may prevent the age-related decrease of the muscle [78]. The turnover rate of contractile proteins
in the relative content of MyHC IIb isoform in skeletal in skeletal muscle seems to be related to age-related changes
muscle. in the composition of the MyHC isoform [77]. Resistance
In the elderly, skeletal muscle atrophy and mitochondrial training increases the turnover rate of contractile proteins,
dysfunction coexist and maybe causally related [7]. There is but the changes in old age are relatively slower than in
convincing evidence of the existing link between muscle young age [77, 78].
mitochondrial dysfunction and insulin resistance in the el- Even if it does not cause hypertrophy of muscle fibers,
derly [2]. It has been shown that resistance training in older resistance exercise in the aging population avoids muscle
adults can increase mitochondrial capacity in skeletal mus- atrophy as the myonuclear number increases slightly as a
cle [62]. Muscle contraction induce(s) the mobilization of result of the fusion of satellite cells with damaged fibers. Via
local lipid reserves in obese skeletal muscle and promotes this or as a result of myoblasts’ fusion forming myotubes,
beta-oxidation while discouraging glucose utilization [93]. which develop into new muscle fibers, muscle functional
Resistance training helps elderly skeletal muscle preserve capacity increases. Exercise causes adaptational changes in
fat-free mass during body mass loss [9]. the contractile apparatus, primarily in newly formed fibers
Rapid recovery from resistance exercise in young age via the remodeling of myosin isoforms. A faster turnover
supports the increase in muscle strength [77], but recovery rate of contractile proteins in resistance-trained muscles
from more damaging resistance exercise is slower as a result supports the strength generation capacity of muscle fibers
of age, whereas there are no age-related differences in in elderly skeletal muscle (Fig. 2). Naturally, this process is
recovery from less damaging metabolic fatigue [26]. Recent more effective in muscle fibers with higher oxidative capac-
evidence suggests that the difference in the regenerative ity than in muscle fibers with low oxidative capacity.
capacity of skeletal muscle between young and very old rats
is only about 10 %, but regeneration of the myofibrillar Endurance exercise training
apparatus is much slower in the elderly [38].
This is obviously related to the greater amount of resis- Structural and functional rearrangements in skeletal muscle
tance exercise-induced damage in skeletal muscle as there is depend on the oxidative capacity of the fibers [78]. The integral
relatively slow repair of muscle tissue after exercise in the indicator of muscle protein metabolism, muscle protein turn-
elderly [26]. Finding possibilities to rehabilitate the loss of over, fiber recovery from exercise-induced injury, and regener-
physical function by exercise therapy in the elderly is one of ation capacity is faster in fibers with higher oxidative capacity
today’s burning issues due to an increase in elderly people in [74, 75, 80]. As a physiological process, aging also includes a
the society. gradual decrease in skeletal muscle endurance [18, 77], and this
is related to the reduction in fitness. A decrease in physical
Changes in the turnover rate of muscle proteins fitness gives theoretical background to use both endurance and
during resistance exercise training resistance exercise for health outcomes in the elderly. The
turnover of muscle protein provides a mechanism by which
Resistance exercise may modify muscle fiber structure and resistance training can change the contractile protein renewal in
metabolism and promote the release of growth factors and accordance with the needs of the contractile machinery of
other signaling molecules, such as nitric oxide, which acti- skeletal muscle [75]. As the oxidative capacity of skeletal
vates the satellite cells through the paracrine system [94]. muscle decreases in the elderly, endurance training seems to
Myosatellites, which develop further into myoblasts, con- be effective in its restoration as it stimulates mitochondrial
tain lots of ribosomes, branching granular sarcoplasmic biogenesis and improves their functional parameters [35, 47].
reticulum with widened canals, and a Golgi apparatus. A combination of endurance and resistance exercise in the
Myosatellitocytes may also contain centrioles, and this con- elderly for the purpose of increasing muscle oxidative capacity
firms that these cells are divided by mitosis [78]. Myosatel- and the contractile protein turnover rate is an effective measure
litocytes sarcoplasm close to the nucleus contains bundles of for enhancing quality of life in the elderly by improving skeletal
filaments, which may turn out to be myofilaments [97]. In muscle functional capacity and plasticity (Fig. 2). It has recently
adults and aged persons, resistance training causes muscle been shown that the individual development of muscle plastic-
hypertrophy in two ways: firstly, damaged fibers regenerate ity in the elderly makes it possible to modify the age-associated
as a result of the fusion with the satellite cells; secondly, decline even in maximal physical performance at least for some
satellite cells divide and, later, myosymplasts fuse with each time [89]. The higher aerobic capacity in trained elderly people
other and form myotubes [78]. It has been shown that is related to an increase in the abilities of the cardiovascular
contractile proteins turned over faster in type I and IIA system and, to a lesser extent, to an increase in muscle mito-
muscle fibers than in IIB fibers, and the turnover rate of chondrial concentration and capacity [73]. Here, the lesser
114 Eur Rev Aging Phys Act (2012) 9:109–117

Increase in turnover rate of myofibrillar

Increase in myofibrillar structure Hypertrophy of fast-twitch fibers
proteins
regeneration capacity

Increase in muscle strength Anabolic and anticatabolic effects on

Decrease in the fastest myosin muscle fibers
isoforms’ relative content

Structural rearrangements in fast-twitch

Improvement of muscle-nerve fibers
contact
RESISTANCE TRAINING

Qualitative remodelling of fast- Qualitative remodelling of skeletal muscle

twitch fibers

DECELERATION OF MUSCLE
WEAKNESS

Increase in muscle sarcoplasmatic Increase in turnover rate of sarcoplasmatic

structure regenerative capacity proteins

ENDURANCE TRAINING
Structural rearrangemets in type I and IIA
Transformation of the contractile
fibers
apparatus in accordance with the
increase in muscle oxidative capacity
Increase in muscle oxidative capacity
Structural rearrangements in muscle
Improvement of muscle-nerve spindles
contact
Decrease in muscle fibers O2
Increase in functional reserve
Qualitative remodelling in type I and difusion distance
IIA fibres
Increase in vital capacity
Improvement of capillary blood
supply

Fig. 2 Effect of exercise therapy on the deceleration of muscle weakness and, via this, improvement of quality of life in the elderly

extent means that regular aerobic activity provides a foundation to the development of muscle wasting and weakness in the
for an increase of muscle oxidative capacity in the elderly. At elderly, it is complicated to find one certain measure for
this point, it is useful to repeat the viewpoint of Suominen [89] rehabilitation. As lack of strength is one of the main reasons
that adequate physical performance is an essential element of a for muscle weakness, it seems to be most realistic to use
healthy and productive life among the elderly. Although factors resistance training for this purpose in the elderly. Resistance
such as health, physical function, and independence constitute training is a strong stimulus for muscle metabolism in the
components of the quality of life in the elderly, physiological elderly, particularly for the contractile machinery of muscle.
functioning is significant in determining the ability to maintain The contractile protein turnover rate provides a mechanism
independence and an active interaction with the environment by which the effect of exercise-caused changes can be
[85]. The mode of exercise plays a significant role in elderly assessed in accordance with the needs of the contractile
training. It has shown that high-intensity aerobic exercise train- apparatus. As the contractile protein turnover rate depends
ing efficiently reduced visceral fat in elderly and overweight on the oxidative capacity of muscle and muscle oxidative
adults [16]. However, with older age, managing everyday capacity decreases in the elderly, it is obvious that endur-
activities becomes less self-evident, although there are gender ance exercise stimulates an increase in the oxidative capac-
differences in physical functioning [43]. Functional limitation ity of skeletal muscle by an increase in mitochondrial
in old age is an objective measure of the consequences of biogenesis and supports faster protein turnover during resis-
disease and impairment [32]. There is increasing need in the tance training, as a result of which muscle function, and
society to encourage elderly people to follow the mot of thereby quality of life, in the elderly improves. The regen-
Kramer and Erickson [42] for successful aging to use wide- eration of skeletal muscle from the damage caused by exer-
spread participation in low-cost and low-tech exercise to further cise is faster in muscles with higher oxidative capacity.
improve their fitness and reduce the risk of disability. Using both resistance and endurance exercise in the elderly
makes it possible to modify the age-associated decline in
muscle function and decelerate the development of muscle
Summary and conclusions weakness.

Both sarcopenia and dynapenia are risk factors for health

Acknowledgments This study was supported by the funds of the
outcomes and play a significant role in the etiology of Ministry of Education and Research of Estonia, research project no.
disability in the elderly. As a complex of factors contributes TKKSB1787.
Eur Rev Aging Phys Act (2012) 9:109–117 115

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