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The Influence of Aging and Sex On Skeletal Muscle Mass and Strength
The Influence of Aging and Sex On Skeletal Muscle Mass and Strength
strength
Timothy J. Doherty
discussion, mainly comprising males. Two recent high Reductions in skeletal muscle fiber size
quality studies, however, have overcome many of these and number
failings. Gallagher et al. [12] measured arm skeletal In attempts to understand the underlying cause of age-
muscle mass, leg skeletal muscle mass and total related atrophy, numerous studies have assessed muscle
appendicular skeletal muscle mass using dual-energy morphology from tissue obtained using muscle biopsy.
X-ray absorptiometry in a sample of 148 women and 136 The majority of these studies have been undertaken on
men between 20 and 90 years of age. After adjusting for the vastus lateralis muscle and the overall conclusion is
height, body weight and age, men had larger total reasonably consistent: average type II ®ber size is
appendicular skeletal muscle mass than women. More- diminished with age while the size of type I ®bers is
over, men exhibited larger age-related decreases in total much less affected [1±3,16±18]. While reductions in type
appendicular skeletal muscle mass, in comparison to II area range from 20±50%, type I ®ber area losses range
women (14.8% versus 10.8% respectively). Similarly, from 1±25%. The variability noted in these studies relates
Janssen et al. [13 .] used whole body magnetic resonance to sampling variability, potential sampling bias with
imaging to determine skeletal muscle mass in a sample muscle biopsy, and the undoubted inherent variability
of 268 men and 200 women between 18 and 88 years of in both the older and younger control populations.
age. Again, men had signi®cantly greater skeletal muscle
mass than women with greater losses of skeletal muscle The above reductions in ®ber size, however, are
mass with aging. The mechanisms leading to greater considered moderate in comparison with the reductions
losses of muscle mass with aging in men as compared in muscle mass, and therefore reductions in muscle ®ber
with women are unknown but have been postulated to number have been proposed. Lexell et al. [18], using
relate to hormonal factors including growth hormone, whole muscle cross-sections from the vastus lateralis
insulin-like growth factor, and androgens [13 .]. While muscle obtained post mortem, reported that by the ninth
greater losses of muscle mass occur with aging in men, it decade approximately 50% fewer type I and type II
has been suggested that sarcopenia is a greater public ®bers were present than in tissue from 20-year-olds. The
health problem for women since they live longer and fact that similar losses of muscle ®bers were present for
have higher rates of disability [5 . .]. type I and II ®bers stood in contrast to earlier work from
samples obtained with muscle biopsy. Further analysis
Age-associated loss of muscle mass appears inevitable determined that the cross-sectional area of the vastus
and is likely the most signi®cant contributing factor to lateralis, at least, is mainly determined by the total
the decline in muscle strength [4,5 . .]. While all men and number of ®bers and, to a lesser extent, by the size or
women experience some degree of sarcopenia, this is number of type II ®bers [16,17].
variable and on a continuum. However, as per the typical
clinical de®nition for osteoporosis, it is possible to Electrophysiologic studies have demonstrated similar
dichotomize this continuous process by establishing a dramatic losses of whole functioning motor units in
lower limit of normal, such as 2 SD below the mean proximal and distal muscles in the upper and lower
appendicular muscle mass for healthy young adults. For extremities, in the order of 50% for the thenar and
example, Baumgartner et al. [14], in the New Mexico biceps/brachialis muscle groups [19±21]. These ®ndings,
Elder Survey, measured appendicular muscle mass by taken together with histologic changes consistent with a
dual-energy X-ray absorptiometry in 883 randomly chronic neurodegenerative process, point toward age-
selected elderly Hispanic and white men and women. associated losses of anterior horn cells as an important
Sarcopenia was de®ned as losses greater than 2 SD contributing factor to reduced muscle ®ber number and
below the mean for young healthy controls. The muscle mass [1,3].
prevalence of sarcopenia ranged from 13±24% in persons
aged 65±70 years and was over 50% for those older than There is a paucity of data on the effect of sex on changes
80 years. In this study the prevalence was higher for men in muscle ®ber number and area. In general, similar
over age 75 (58%) than for women (45%). In a similar losses of type I and type II ®ber area have been reported.
study, the prevalence based on total skeletal mass Essen-Gustavsson and Borges [22], however, reported
determined by dual-energy X-ray absorptiometry was more signi®cant decline for older women in type 1 (men
10% for men and 8% for women between 60 and 69 15%, women 25%) and type II ®ber area (men 19%,
years, and 40% and 18% respectively for men and women 45%) for the vastus lateralis muscle. Aniansson et
women over 80 years [15]. As these prevalance rates are al. [23] similarly reported smaller mean type I and type
relative to sex-speci®c younger control populations they II ®ber areas in older women than in older men.
suggest greater declines in muscle mass for men than
women. Nevertheless, substantial declines occur for both Age-related changes in muscle strength
sexes and are directly related to increasing disability with Starting at approximately 30 years of age, in the absence
advancing age. of training, strength declines at a rate of about 10±15%
Skeletal muscle mass and strength Doherty 505
per decade. Since typical activities of daily living require Many of the studies that have examined age-related
minimal to moderate muscular contractile efforts, this changes in strength have studied small numbers of
gradual loss of strength does not become functionally subjects, employed cross-sectional designs, and in many
signi®cant until beyond 55±60 years of age for most men cases studied only men, or inappropriately combined
and women. Beyond about the sixth decade, the rate of men and women in their analysis. To examine the
force loss may accelerate, but eventually levels off in the in¯uence of sex on age-related changes in strength,
seventh and eighth decades, such that men and women selected older and more recent high quality studies will
in this age group have about 50% of the strength of be reviewed.
younger adults. In the absence of disease, further losses
in the subsequent decades may be no greater than 10%. Cross-sectional studies
This level of strength often approaches that necessary to Vandervoort and McComas [32] examined young,
carry out the basic tasks of daily living, but leaves little or middle aged and elderly men and women. Maximal
no safety factor for dealing with concomitant illness or voluntary and electrically evoked maximal twitch forces
for leisure activities requiring higher levels of function were determined for both the plantar¯exor and dorsi-
[1,3,4,5 .,23]. ¯exor muscles. As illustrated in Fig. 1, men were
stronger than women at all ages and aging was associated
Age-related decreases in strength have been well with substantial declines in force. These changes were
documented in numerous studies. A variety of limb similar for men and women and the declines were similar
muscles have been examined in cross-sectional studies for both evoked and voluntary contractions. Interest-
during isometric and dynamic conditions in young, ingly, when the values for subjects in the youngest and
middle-aged, and older men and women. In general, middle-aged (40±52 years) groups were compared, the
these studies suggest that reductions in isometric and voluntary torques were similar, with only dorsi¯exion in
dynamic voluntary and electrically evoked contractile men showing a signi®cant decline. In an attempt to
strength become substantial by the seventh decade of determine the extent to which reduced central drive may
life, and may accelerate thereafter. Healthy men and contribute to reduced volitional torque production, the
women in their seventh and eighth decades demonstrate twitch interpolation technique was used. An important
average reductions of 20±40% in maximal isometric ®nding of this study was that most older men and
strength in comparison to young controls (Table 1). In women were able to maximally activate the lower motor
general, similar reductions have been reported for both neuron pool for maximal force production. Thus, the
men and women in both upper and lower limb muscles. reduced volitional forces with aging, and the lower forces
There is some indication that greater losses are present across all ages in women, were attributed to decreased
at higher contractile velocities during dynamic contrac- muscle mass as opposed to the inability to adequately
tions and that eccentric force production may be better recruit the available contractile tissue [1,3]. Reductions
preserved than concentric [28,29,31]. in muscle cross-sectional area were less than the
Figure 1. Age-related changes in muscle strength There has been interest in the extent to which aging
effects concentric and eccentric force production. Both
(a) Vandervoort et al. [29], and Poulin et al. [28] reported
Maximal 50 losses of eccentric strength with aging, but such losses
voluntary were signi®cantly less than those reported for the
contraction 40 concentric testing condition. A larger, more recent study
(Nm) of subjects drawn from the Baltimore Longitudinal
30 Study of Aging is in contrast to these ®ndings, in that
similar losses were found for concentric and eccentric
20
knee extensor torque with no signi®cant effect of sex.
10
Regression analysis did however reveal that age ex-
plained losses in concentric torque better than eccentric
0 [30].
20 – 32 40 – 52 60 – 69 70 –79 80 –100
Age (years) Longitudinal studies
Relatively few longitudinal studies of skeletal muscle
(b)
strength and aging have been undertaken. In one study,
Maximal 200
the extent of strength decline over time was greater
voluntary
contraction when studied longitudinally, suggesting the potential for
(Nm) underestimation of age-related strength loss from cross-
sectional studies [34]. Earlier longitudinal studies have
100 reported a decline [34], no change [35] or gains [36,37]
over variable time periods in differing muscle groups.
Bassey and Harries [34] reported a 12% loss in grip
strength for men over a 4-year period and a 19% loss for
women. Alternatively, similar losses of 25±35% were
0
20 – 32 40 – 52 60 – 69 70 –79 80 –100 reported for men and women over an 11-year period for
Age (years) knee extensors [38].
age-related decreases in strength appear to occur for men stronger than similar ®bers from older women, even after
and women. adjusting for size. These important ®ndings provide
direct evidence for differences in muscle quality in older
Age-related changes in muscle quality men and women. The mechanism underlying such sex-
Recent work has highlighted the importance of expres- related differences with aging remains in question.
sing age-related strength losses relative to muscle mass. However, hormonal factors may play a role. It has been
Thus, the term `muscle quality' has been coined, which, demonstrated that speci®c force is similar in men and
otherwise known as speci®c tension, refers to the premenopausal women, whereas there was a dramatic
strength per unit muscle mass and is considered a better decline in speci®c force around the time of menopause;
indicator of muscle function than strength alone [5 . .]. the latter, however, was diminished in women using
hormone replacement therapy [43].
Some interesting sex differences in muscle quality with
aging have been suggested in a number of cross- Conclusion
sectional studies. Some reports have found no difference Aging is associated with signi®cant decreases in strength
in muscle quality when comparing young and older in men and women and, while women may show
women, but many have reported an age-associated somewhat earlier losses in strength, the overall reduc-
decline in muscle quality in men. In a recent compre- tions are reasonably similar. Decline in the quantity and
hensive study, Lynch et al. [30] set out to determine perhaps quality of muscle mass is the most important
differences in muscle quality between arm and leg contributing factor to age-related reductions in strength.
muscles across the life span. Reliable measures were On average, men tend to be stronger than women at all
used for measurement of both concentric and eccentric ages, however, the majority of these differences are
strength as well as muscle mass. The major ®ndings accounted for by differences in muscle mass. Recent
of this study were as follows: (1) age-associated differ- evidence, however, suggests that differences may exist
ences in arm muscle quality were greater in men than in muscle quality when comparing men and women and
women; whereas leg muscle quality declined similarly. that these differences may relate to altered muscle ®ber
(2) Muscle quality for the arm was higher than for the leg contractile function in men and women. The impact of
across all age groups for men and women. (3) The physical activity, hormonal and nutritional in¯uences on
decline in leg muscle quality was greater than the such sex related differences are the topic of considerable
decline in arm muscle quality for women, whereas for ongoing study.
men they declined at the same rate. These age-related
losses in muscle quality are potentially related, among
other factors, to changes in neural drive, altered muscle References and recommended reading
pennation and increases in connective tissue. With Papers of particular interest, published within the annual period of review, have
been highlighted as:
regard to this latter point, Kent-Braun et al. [41 .] recently . of special interest
.. of outstanding interest
reported twofold to threefold increases in intramuscular
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The first study to examine the relationship between strength and size at the whole
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