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EUR J ­PHYS REHABIL MED 2013;49:131-43

Role of exercise on sarcopenia in the elderly


N. MONTERO-FERNÁNDEZ 1, J. A. SERRA-REXACH 2

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Sarcopenia leads to a loss of strength, later on to a de- 1Geriatric Department, University Hospital Gregorio
creased functional status, impaired mobility, a higher Marañón, Madrid, Spain
risk of falls, and eventually an increased risk of mortal- 2Chair Geriatric Department, University Hospital Gregorio

ity. There are many factors responsible for the decline Marañón Complutense University, Madrid, Spain

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of muscle mass and muscle strength associated with
aging, although the complex, multi-factorial mecha-
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nisms driving the sarcopenic process are not clearly
understood. Physical inactivity or a decreased physical

S
activity level is a part of the underlying mechanisms arcopenia, initially defined as an age-related loss
of sarcopenia and therefore physical activity can be
seen as an important factor to reverse or modify the of muscle mass,1 is now considered a syndrome
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development of this condition. Several treatments have characterized by progressive and generalized loss of
been proposed for the treatment of this loss of muscle skeletal muscle mass and strength associated with
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and strength, but there is no doubt that exercise rep- ageing.2 It is a complex medical condition that pre-
resents the most important approach to prevent and dicts mobility, disability, leading in turn to loss of
treat sarcopenia. In this review, we describe first the
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independence, a higher risk of falls, reduced quality


conceptual distinctions between the terms sedentary
behaviour, physical activity and exercise. In addition, of life, increased health care costs and eventually an
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we review the benefits of physical activity in the eld- increased risk of mortality.3
erly population, including lower mortality and func- Even in healthy persons, muscle mass declines at
tional independence, and discuss the four categories approximately 1% per year from the peak between
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for specific recommendations for exercises (aerobic 20 and 30 years old, and accelerates from 50 years,
exercise, progressive resistance exercise, flexibility particularly in the lower extremities.
and balance). Finally we discuss the principles govern-
ing the prescription of physical activity for older peo- This decline occurs gradually in men, whereas it
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ple with sarcopenia and make some specific advices occurs sharply in women after menopause.4, 5 There
for how to engage older adults in appropriate exercise. are many factors responsible for this decline of mus-
Key words: Sarcopenia - Exercise - Motor activity - Postural cle mass and muscle strength associated with aging.
balance - Lifestyle. It seems that the anabolic potential of skeletal mus-
cle may be reduced in the elderly. Insulin resistance,
inflammation, hormonal alterations, perturbations in
“Lack of activity destroys the good condition of every muscle metabolism and decreased muscle prolifera-
human being while movement and methodical physical
or other proprietary information of the Publisher.

exercise save it and preserve it”. tion are the main changes involved. In addition to
the aging process, there have been identified several
Plato
risk factors that favor its appearance, most notably
sedentary lifestyle, female gender and some organ
Corresponding author: N. Montero-Fernández, Hospital General
Universitario Gregorio Marañón, Calle Doctor Esquerdo 46, 28007 diseases.3, 6 Overall, the most prominent cause of
Madrid, Spain. E-mail: nmonterof@yahoo.es sarcopenia is inactivity. Although it does not com-

Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 131


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
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MONTERO-FERNÁNDEZ Role of exercise on sarcopenia in the elderly

pletely revert with exercise, the absence of physical muscular strength, skeletal muscular power, speed,
activity (PA) accelerates muscle mass loss. flexibility, agility, balance, reaction time, and body
Different strategies have been tested for its treat- composition.10
ment: human growth hormone, androgens, estro- Sedentary behaviors (SB) are defined as a way
gens in women, nutritional treatment and exercise. of living or lifestyle that requires minimal PA and
Of all the therapeutics available, PA with or without that encourages inactivity through limited choices,
dietary supplementation has shown its efficacy in disincentives, and/or structural or financial barriers.8
increasing skeletal muscle mass. They include the time spent sitting or lying which
Before we provide in this review more informa- has been shown to be a modifiable risk factor of car-
tion detailing the role of exercise in sarcopenia, we diovascular disease, type 2 diabetes mellitus, obesity,
will briefly offer some definitions of terms in order some cancers, skeletal health. Moreover they have a
to avoid misunderstandings, errors and inconsisten- negative impact on some aspects of mental health,

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cies using this terminology. Casperson et al. attempt- overall mortality, disablement and frailty as well as
ed 27 years ago to provide a common framework poor quality of life, independently from physical ac-

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for researches from different fields to communicate.7 tivity levels.11 Besides that, SB affects muscle physi-
Physical activity (PA) is any bodily movement pro- ology, lead to weakness and accelerates sarcopenia.
duced by contraction of skeletal muscle that sub- But it would be feasible that these age related de-

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stantially increases energy expenditure, although the clines in muscle mass and function were also the
intensity and duration can vary substantially.8 Base- principal drivers of increased SB among aging per-
line activity is, however, the smallest increments sons.12, 13

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of body movements produced by skeletal muscle
contractions that increases energy above sedentary
Finally, lifestyle modification refers to the use of
opportunities in a person’s daily routine to increase
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behaviors (e.g., standing, slow walking, lifting very energy expenditure (e.g., manually open doors, car-
light objects, etc.).9 Consistent with this definition, ry groceries, use stairs rather than elevators, parking
individuals who do only baseline activity are not further from entrances) and substitute active for sed-
sedentary, per se, but are still considered to be inac- entary leisure time.14
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tive. PA may be measured in terms of METs (meta- The purpose of this review is to examine whether
bolic equivalents), units used to estimate the meta- the different types of exercise show to be beneficial
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bolic cost (oxygen consumption) of PA. One MET for treatment and prevention of sarcopenia among
equals the resting metabolic rate of approximately older adults.
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3.5 mL O2/kg/min, and represents the approximate


rate of oxygen consumption of a seated adult at
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rest. Moderate physical activity includes activity per- Mechanisms of sarcopenia


formed at an intensity of 3 to 6 METs (leisure cy-
cling, moderate effort swimming, playing golf walk- Muscle mass is the primary determinant of
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ing, general cleaning at home, or lawn mowing), or strength. Males are generally stronger than females
the equivalent of walking briskly at approximately primarily because they have larger muscle mass. The
5 to 8 kilometers (3 to 5 miles) per hour.10 Vigorous loss of muscle mass during the ageing process is
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physical activity includes activity performed at >6 clinically important as it leads to reduced strength
METs, such as running, rope jumping, and calisthen- and exercise capacity, both of which are required
ics (e.g., push-ups, pull-ups, sit-ups, jumping jacks). undertaking normal daily living activities. Although
Exercise is a subcategory of leisure time PA in we will all lose muscle mass as we age, individual
which planned, structured, and repetitive bodily differences in the rate of loss in muscle mass, the
movements are performed to improve or maintain age at which muscle mass starts to decline, and the
one or more components of physical fitness. Partici- individual’s peak muscle mass, determine the im-
or other proprietary information of the Publisher.

pation in exercise and the accumulation of PA have pact that sarcopenia has on functional ability.15
been shown to result in improvements in physical Several physiological mechanisms are involved in
fitness that is a set of attributes that contribute to the the cause of the syndrome including changes affect-
ability to perform physical work: cardiorespiratory ing neuromuscular transmission, muscle and tendon
endurance, skeletal muscular endurance, skeletal architecture, fiber composition, excitation-contrac-

132 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE February 2013


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
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Role of exercise on sarcopenia in the elderly MONTERO-FERNÁNDEZ

tion coupling, and metabolism.16 Throughout the described in relation to several of the factors act-
human aging process, the loss of strength in old age ing on muscle in age-related processes. The effects
is predominantly accounted for by reduced mus- of PA in elderly subjects, measurable at cell level,
cle mass and myofibrillar protein content in conse- involves beneficial outcomes on muscle anabolism,
quence of a combination of progressive fiber loss muscle energetic metabolism, oxidative stress, mus-
and fiber atrophy. The aging process is often char- cle inflammation, muscle denervation, muscle and
acterized by investigators as a selective loss of fast- tendon architecture and muscle mechanical exci-
twitch fibers in muscle.17 Some recent findings sug- tation-contraction coupling.16 Increasing PA could
gest that surviving fibers are still prone to plasticity be effective for reducing chronic inflammation in
in response to different functional demands such as elderly people with sarcopenia. On the other hand,
physical exercise; this response helps elderly muscle regular PA can thus partially correct the acceleration
to compensate to partially correct muscle size deficit of sarcopenic progression related to inactivity and

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in an attempt to maintain optimal force-generating poor nutrition.23
capacity.18 However, these factors are not common to all eld-

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Sarcopenia is also associated with increased con- erly and/or sarcopenic individuals. Within clinical
centrations of proinflamatory cytokines and acute study cohorts, a large degree of heterogeneity exists
phase reactants, and several cytokines have direct, that complicates the work of clinical and transla-

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detrimental effects on skeletal muscle leading to the tional scientists studying sarcopenia. Furthermore,
loss of myofibers and the consequent disruption of variability in lifestyle and disease conditions induces
contractile function.19 different atrophy-related mechanisms and degrees

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On the other hand, anabolic hormones such as
growth hormone, testosterone and estrogen fall with
of atrophy. Therefore, global therapeutic approach-
es are unlikely to prove equally effective in all mod-
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ageing, which causes a decrease of its trophic ef- els of sarcopenia.
fect and produces muscle atrophy. Other changes in
muscle leading to a loss of strength include infiltra-
tion into muscle by fat, which is a powerful predic- Benefits of physical activity and aging
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tor of future disability and mortality.19 This has been


designated as sarcopenic obesity or myosteatosis.20 Exercise is believed to be the most effective of all
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Clearly sarcopenia worses by disuse and a sed- interventions proposed to improve quality of life and
entary life produces greater and more rapid loss of functionality in older adults. Since the first paper of
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muscle than active life. Evidence from observational Morris in the early 1950s 24 describing the relation
and intervention studies are beginning to show that between inactivity and coronary heart disease, there
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disuse may actually be the underlying reason for has been a wealth of scientific evidence about the
muscle atrophy and weakness, rather than aging, benefits of exercise prescription for health-related
per se.21 Following some periods of disuse that oc- and quality of life benefits.25, 26 However, there is
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cur with increasing frequency in the elderly, for ex- still scepticism between elderly people, clinicians,
ample, due to illness or hospitalization, the rate of investigators and health authorities, about the role
sarcopenic muscle loss is accelerating,22 even some- of PA for disease prevention and treatment in the
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thing as benign as a reduction in daily step counts, older, particularly in frail adults. Although the pro-
can accelerate sarcopenic muscle loss, from which it motion of exercise can’t avoid the aging process, PA
is more difficult for the elderly to recover. can minimize the physiological effects of a SB and
Furthermore, poor nutrition is well-known to increase active life expectancy by limiting the de-
contribute to sarcopenia. Certain conditions have velopment and progression of chronic disease and
the strong potential to coincide with sarcopenia in disabling conditions.26
accelerating the progression of muscle atrophy in It is never too late to become physically active.
or other proprietary information of the Publisher.

older adults. Among these conditions are co-morbid For older adults, the benefits of PA, including lower
diseases common to older individuals such as can- mortality and functional independence, occur with
cer, kidney disease, organ failure, diabetes, and pe- initiation and maintenance of exercise. Even indi-
ripheral artery disease.23 viduals who were previously sedentary but initiate
The influence of PA in sarcopenic muscle can be exercise as late as age 85 demonstrate a significant

Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 133


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

MONTERO-FERNÁNDEZ Role of exercise on sarcopenia in the elderly

survival benefit in three years in comparison to indi- The patterns of change in body composition seen
viduals who were sedentary.27 in usual aging include a gradual increase in adipos-
The physiological, cardiovascular and neuromus- ity and loss of skeletal muscle and bone mass in
cular adaptive response to regularly performed ex- both men and women from 25 to approximately 65
ercise in the elderly has been repeatedly demon- years of age, after which total body weight declines.
strated to be similar to those of younger adults. These age-related changes have important clinical
Older individuals who practice exercise regularly implications as they may negatively impact metabol-
get higher VO2max and higher maximal cardiac out- ic, cardiovascular and musculoskeletal function and
put with PA when compared to matched sedentary they are independently associated with declining
controls. These improvements are lower in older performance as well as increased risk for disability
versus young people, but similar if we focus only and mortality in older persons.37, 38 Physically active
on the relative values changes. The exercise training older adults compared to sedentary have less total

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attenuates the age related loss of arterial compliance and abdominal body fat and greater muscle mass in
and preserves the endothelial function even in pre- the limbs and higher bone mineral density.39

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viously sedentary older men, in a very similar way The relative risk of developing many chronic dis-
to what occurs in younger people. Finally, even very eases (cardiovascular disease, type 2 diabetes, hy-
old individuals maintain the capability of increas- pertension, obesity and certain cancers), the preva-

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ing the synthesis rate of muscle contractile proteins lence of degenerative musculoskeletal conditions
in response to resistance exercise, as we have sug- (osteoporosis, arthritis, sarcopenia) and disability in-
gested earlier in this review.28-30 creases with advancing age.8, 25, 40 A graded relation-

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All older adults, including the oldest ones, those
with multiple morbidities, or those who are in
ship between exercise and the development of these
common chronic conditions and some geriatric syn-
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chronic care facilities, are likely to benefit from PA. dromes (cognitive impairment, frailty, disability, mo-
Participation in any amount of PA will result in some bility impairments, falls, urinary stress incontinence,
health benefit as some PA is better than none. A de- insomnia) has been observed even in the elderly
scription of the benefits of exercise and a full discus- population. The mechanisms of this preventive ex-
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sion of types of exercise and their recommendations ercise effect involve decrease body weight, mainte-
for older adults will be offered in next sections. nance of muscles and tendons strength, decrease es-
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Large observational studies suggest that regular trogens levels and LDL cholesterol, decrease blood
exercise in older populations reduces risk of all- pressure and insulin resistance and hyperinsuline-
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cause mortality for most individuals.27, 31, 32 These mia. Also PA is a main therapeutic intervention for
beneficial effects appear to be dose-dependent, the treatment and management of these chronic dis-
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even in older adults with chronic diseases.33 It oc- eases 8, 40, 25 and for their associated disability, al-
curs in despite the increasing likelihood of comor- though traditional medical approach usually do not
bidity, frailty, dependence, and ever-shortening life address disuse and deconditioning accompanying
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expectancy, remaining and even starting to be phys- these kind of diseases.


ically active increases the likelihood of living longer Exercise also reduces likelihood of falls and fall-
and functionally independent.34 Regular PA increas- related injuries.41 More than one-third of community-
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es life expectancy through its influence on chronic living older adults fall each year and approximately
diseases development and treatment and also limits 10% of falls result in serious clinical consequences.
the impact of secondary aging through restoration Falls are not only associated with morbidity and
of functional capacity in previously sedentary older mortality, but are also linked to poorer overall func-
adults. tioning and early admission to long-term care facili-
Increasing PA in old age improves quality of life, ties.42 PA reduces risk of falls and injuries from falls
psychological health and is associated with bet- 43 even in the oldest old,44 both in the community
or other proprietary information of the Publisher.

ter mental health and social integration, improves both as residential population, improving strength,
anxiety, depression and self efficacy for PA in older endurance and body mechanics.
adults.35 The relationship between neurological dis- As reviewed in several epidemiological studies 45-
orders and sarcopenia are discussed in detail in an- 47 regular practice PAS exercise is associated with
other review in this issue. decreased risk for activities of daily living disabil-

134 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE February 2013


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
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Role of exercise on sarcopenia in the elderly MONTERO-FERNÁNDEZ

ity. Decline in function and loss of independence Progressive resistance exercise (PRE)
are not an inevitable consequence of aging. Given
the high prevalence and impact of chronic health It is a form of structured PA that is generally de-
problems among older patients, evidence-based fined as exercise that requires muscles to generate
interventions to address these problems become force to move or resist weight, with the intensity
increasingly important to maximize both the quan- increasing as physical capacity improves. Structured
tity and quality of life for older adults. Additionally, PRE relies on anaerobic metabolism to meet energy
many small studies have reported the benefits of PA demands and examples of PRE activities include lift-
on physical capacity and precursors of physical dis- ing weights, working with resistance bands, doing
ability (increasing muscle strength, aerobic capacity calisthenics using body weight for resistance (such
and bone density),32 even in frail elderly persons.47, as push-ups, pull-ups, and sit-ups), climbing stairs,
48 Physically active adults are more likely to survive carrying heavy loads, and heavy gardening.49

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to age 80 or beyond and had approximately on half Several studies and systematic reviews have shown
risk of dying with disability compared to their sed- that even in the elderly, PRE increases muscle mass,
muscle power and muscle strength.47 Although ini-

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entary counterparts.48
tially these results on the improved function were
unclear, the recent systematic review by Liu and

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Types of exercise Lathman 53 has shown to be an effective interven-
tion for improving physical function in the elderly
There are four types of exercises recommended and therefore delaying disability, which is the main

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for older adults: aerobic, progressive resistance, flex-
ibility and balance training.
adverse event of sarcopenia.
Several investigations have reported that after
even short durations of PRE, protein synthesis rate
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and neuromuscular adaptive-responses among eld-
Aerobic exercise (AE) erly adults were similar to that of young subjects,
It is a form of structured PA characterized by despite a much lower pre-exercise rate.54-56
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rhythmic and repetitive movements of large mus- PRE improves modestly cardiorespiratory fitness,
cles, for sustained periods that depends primarily particularly for previously sedentary older adults,
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on the use of oxygen to meet energy demands decreases risk of fall, increases bone mineral density
through aerobic metabolism, and that is structured and tendon strength, and improves various cardi-
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and intended to generate improvements in car- ometabolic risk factors in the absence of weight loss
diorespiratory fitness, body composition, and/or (decreased LDL-cholesterol 57, 58 and triglycerides,57
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cardiometabolic health.49 Examples of aerobic ac- reductions in blood pressure,59 increases in HDL-
tivities include brisk walking, jogging, swimming, cholesterol 58 and improves glucose homeostasis
water aerobics, tennis, aerobic exercises classes, and insulin sensitivity).
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dancing and bicycle riding. PRE attenuates development of sarcopenia by


Although advancing age is accompanied by an many ways: improving muscle size and function, re-
accelerating reduction of AE capacity, that is ex- ducing balance and flexibility problems and reduc-
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acerbated by many comorbidities common to the ing also the risk of development of many sarcope-
elderly, it has long been linked to improvements nia-related comorbidities.60
in cardiovascular fitness and endurance capacity in The effectiveness and outcomes of this type of
older adults, both in healthy and diseased individu- exercise depends on some factors as intensity, train-
als. Notwithstanding that AE is believed to largely ing volume (sets by repetitions), frequency and type
decreases most of risk factors for cardiometabolic of recommended exercises (isokinetic/variable re-
diseases and attenuates chronic inflammation, with sistance/isoinertial), periods of recovery between
or other proprietary information of the Publisher.

minimal effects on muscle mass and strength, it can sets and frequency training.62 Different combination
increase the cross-sectional area of muscle fibers.50 of these variables (number of repetitions per set,
AE can also reduce body fat including intramuscular number of sets and rest between sets) originate dif-
fat which in turn improves the functional role of ferent physiological responses. Thus in general, all
muscle relative to body weight.51, 52 training programs induce certain improvements on

Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 135


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

MONTERO-FERNÁNDEZ Role of exercise on sarcopenia in the elderly

strength, hypertrophy or muscle power. However, yses 21, 64 has revealed that PRE is effective for elicit-
certain combinations will have a particular emphasis ing significant strength adaptation and increases in
on one of these manifestations. lean body mass among older adults, and that there
Volume of PRE measures the total amount of exer- is a robust dose-response relationship such that vol-
cise made and it is expressed in terms of the number ume and intensity are strongly associated with ad-
of repetitions, total kilograms raised, duration of the aptations.
session or period training. The best definition is the However, it seems evident that the realization of
total number of sets performed per unit of time. A repetitions to failure with these excessive intensi-
widely accepted definition for this is volume load ties may pose an unnecessary effort, besides being
(VL), which takes into account the total number of detrimental for health and performance, not only for
performed sets, repetitions and weight (kg) lifted these special population groups (e.g., aging, obesity,
(i.e., (total repetitions [no.] x external load [kg]); diabetes) but also for most athletes. Furthermore,

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however, since most published PRE studies for older there is little evidence that shows the superior ef-
adults do not include VL as a prescription entity, it fect of these intensities over other more lower (e.g.,

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is difficult to draw conclusions regarding the dose- 20RM-30RM) in previously untrained people.65 A re-
response relationship. cent review, which analyzes which training intensi-
Frequency is defined as the occurrence, per unit ties are correlated to strength increase in the eld-

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of time (e.g., calendar week) that a full-body PRE erly,66 concludes that intensities are higher than the
regimen is completed. Training frequency recom- low improvement in terms of maximum force but
mended is 3-5 days per week. Train less than two not necessarily in terms of functional gains.

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days a week does not produce a significant increase
in the maximal oxygen consumption. Moreover, the Flexibility exercises
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benefit  additional health training obtained above
five days a week is minimum, and the incidence of It is the ability to move a joint through a complete
injury can increase. range of motion. This limited range of motion in
Intensity is commonly defined as the percentage the hip, knee, and ankle joints may increase the risk
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of maximal ability for a given exercise (i.e., one-rep- of falls and contribute to age-related gait changes.
etition maximum [1RM]). Although this operational Although there is scant research devoted to exam-
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definition for intensity provides a more objective, ining the impact of flexibility on health outcomes,
quantifiable unit than training fatigue or rating of it is considered paramount to overall good physi-
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perceived exertion, current recommendations for cal health. Stretches can be static (assume position,
older adults still rely on a 0-to-10 RPE (perceived hold stretch, then relax); dynamic (fluid motion [e.g.,
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physical exertion) for moderate-intensity (5 to 6 out Tai-Chi]); active (balance while holding stretch, then
of 10) and vigorous-intensity (7 to 8 out of 10) PRE.8, moving [e.g., yoga]); or a combination (propriocep-
40 Alternatively, intensity of PRE may be modified tive neuromuscular facilitation).49
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based on a targeted number of repetitions, or by


increasing loading within a prescribed repetition- Balance training
maximum range (e.g., 8-12 RM).61
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Emphasis on muscle power (how fast the muscle Postural hypotension, impaired proprioception,
contracts) rather than strength alone may help pa- vision, larger postural sway, slower gait velocity and
tients retain the greatest amount of functional capac- slower correcting reflexes are the major factors that
ity as they age. Regardless of age or health status, occur with age. Balance is the exercise that helps
continual improvement requires a progressively in- maintaining stability during daily activities and other
creasing resistance as the patient becomes stronger. exercises, preventing falls. It can be static (e.g., stand
But current recommendations for older adults do on one leg) or dynamic (e.g., walk a tightrope), with
or other proprietary information of the Publisher.

not reflect the viability of progression in PRE dosage hand support as needed. Examples of balance train-
to accommodate a hierarchical muscular adaptive- ing include tandem walking, standing on heels or
response to training, in spite of a significant body toes, walking on compliant surface such as foam
of literature to support its safety and effectiveness.63 mattresses, maintaining balance on moving vehicles
Besides that, recent evidence from two meta-anal- such as bus or train, walking backward.49

136 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE February 2013


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

Role of exercise on sarcopenia in the elderly MONTERO-FERNÁNDEZ

Exercise interventions and sarcopenia and physically limited older adults to minimize the
risk of injury. Many months of activity at less than
Although there is currently no consensus recom- recommended levels is appropriate for very decon-
mendation for PA and exercise among older adults ditioned older adults as they increase activity in a
with sarcopenia, there are some recommendations stepwise manner. In addition, activity plans need to
for adults over the age 65 years for various types of be re-evaluated when there are changes in health
activity and specific guides for implementing such status.
programs. We will provide in the following section —— Muscle strengthening activities and/or balance
an overview of current and specific recommenda- training may need to precede aerobic training activi-
tions, for PA in the elderly, many of which have ties among very frail individuals.
been proven to be useful in preventing or attenuat- —— Proper warm-up and stretching are particular-
ing sarcopenia.8, 25, 40, 49, 67 ly important with careful instruction on balance and

® A
breathing. A warm-up with aerobic activity usually
General recommendations consists of short intervals of low-intensity movement

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(e.g., walking for 5 minutes).
Older adults are a varied group. Most, but not —— Sensory impairments, such as hearing loss,
all, have one or more chronic conditions that vary can make it difficult to instruct older adults. There-

H DI
in type and severity. All have experienced a loss of fore, speaking loudly and slowly, using visual aids,
physical fitness with age, some more than others. and demonstrating exercises are all techniques that
This diversity means that some older adults can run help older adults become active.

IG E
several miles, while others struggle to walk sever-
al blocks. Starting an exercise program later in life
—— Supervision, monitoring, teaching, and en-
couragement are essential, recognizing that long ad-
R M
can significantly reduce risk factors even if a person aptation periods may be needed as deconditioned
was sedentary when he or she was younger, so we elderly may develop aches and pains as they begin
should avoid ageism when we are prescribing exer- a more active lifestyle. Supervision is best when it
cise. Several areas should be emphasized in promot- comes from people familiar with the special needs
P A

ing PA in older adults:8, 25, 26, 40 of the elderly.


—— Before arranging for an exercise program, —— Finally, in the absence of contraindications,
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physicians should consider and identify specific protein intake should be about 1.5 g/kg per day
activities that a patient prefers, according to their to elicit a robust acute muscle protein synthetic re-
C ER

social preferences, cultural norms, exercise history, sponse above that seen at rest. Evidence suggests
readiness, motivation, self-discipline and short and that the elderly may need to distribute this protein
Y

long term goals and logistics. intake evenly throughout the day. Studies combining
—— An activity plan is recommended for all older protein supplements with exercise have obtained
adults. This plan should be individualized with spe- the best outcomes when supplementation is admin-
IN

cific objectives and tasks and tailored according to istered immediately after exercise. The use of pro-
chronic conditions and activity limitations, risk for tein supplements without exercise, however, has not
falls, individual abilities and fitness. had any effect on muscle mass.68
M

—— The PA prescription should be done in the


same manner as clinicians prescribe drugs for a Lifestyle modifications
disease. The plan has to define what, how, when,
where, and how often each activity will be done. Prescriptions should encourage patients to limit
For example “Take a 10-minute walk, three times sedentary activities such as television watching
a day, every day of the week. Choose a speed that and computer use, as recent studies also show that
allows you to talk but that is moderately hard work. breaking up sedentary time can be beneficial. This
or other proprietary information of the Publisher.

The distance is not important, but make sure to walk can include behaviors that result in a transition from
for the entire 10 minutes”. sitting to a standing position or from standing still to
—— The progression of activities (duration and in- beginning to walk. Useful goals include structuring
tensity) should also be individual: a conservative ap- activity into a normal daily routine, as self transpor-
proach may be necessary for the most deconditioned tation (walking, bicycling), take stairs instead eleva-

Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 137


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

MONTERO-FERNÁNDEZ Role of exercise on sarcopenia in the elderly

tors, parking further from entrances, go shopping, spread throughout the day in short time allotments.
do home tasks.25, 26, 40 Moderate-intensity aerobic activity involves a mod-
erate level of effort relative to an individual’s aerobic
Specific recommendations for exercise fitness. On a 10-point scale, where sitting is 0 and
all-out effort is 10, moderate-intensity activity is a 5
Although maintenance or increases in leisure time or 6 and produces noticeable increases in heart rate
PA is known to support preservation of function and breathing. On the same scale, vigorous-intensity
and longevity, there are also well-recognized health activity is a 7 or 8 and produces large increases in
benefits associated with structured and progressive heart rate and breathing. For example, given the het-
exercise.62 erogeneity of fitness levels in older adults, for some
The exercise prescription for elderly patients does older adults a moderate-intensity walk is a slow
not differ significantly from the prescription for walk, and for others it is a brisk walk.49

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younger adults. It is recommended that adults par- However, the guidelines emphasize that for most
ticipate in a minimum of 150 minutes of moderate health outcomes, additional benefits occur as the

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intensity or 60 minutes of vigorous PA per week. amount of PA increases through higher intensity,
Older adults with functionally limiting chronic dis- greater frequency, and/or longer duration. The
eases should be as active as their medical conditions guidelines stress that if older adults cannot do 150

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allows in order to reduce sedentary behavior.40 min of moderate-intensity aerobic activity per week
There is some public awareness of the PA guide- because of chronic conditions, they should be as
lines recommending aerobic exercise on 5 or more physically active as their abilities and conditions al-

IG E
days of the week. However, very few clinicians and
elderly people are knowledgeable about the other
low.49
On the other hand, the minimal 150 minutes of
R M
recommended components of a PA plan, and the moderate-intensity PA per week may be insufficient
prevalence of older adults performing activities to for weight loss for overweight or obese individu-
address muscle strengthening, flexibility, and bal- als. Older adults who are overweight may need the
ance is low. equivalent of 300 minutes per week of moderate-
P A

intensity PA to adequately mange weight control, in


Aerobic conjunction with an appropriate diet.8
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exercise
This recommended amount of aerobic activity
Guidelines from the AHA and the ACSM suggest to is in addition to routine activities of daily living of
C ER

promote and maintain health 30-60 minutes per day light-intensity (e.g., self care, cooking, casual walk-
of moderate-intensity aerobic activity on five days ing or shopping) or moderate-intensity activities
Y

each week, or 20-30 minutes of vigorous-intensity lasting less than 10 min in duration (e.g., walking
activity on three days each week, or some combina- around home or office, walking from the parking
tion of the two, with no more than two consecutive lot).40
IN

days between bouts.40, 49 The types of exercise in- Because an optimal effect on the mechanical and
clude any modality that does not impose excessive metabolic properties of aged muscle cannot be ob-
orthopaedic stress, activities such as brisk walking, tained by a single type of exercise, and considering
M

swimming, and recumbent cycling/stepping that are that AE is better than PRE for developing endurance
usually well tolerated by older individuals. However, capacity, it has been suggested that these types of
unless other specified by a primary care physician exercises should be combined to combat the glo-
or cardiologist, individuals may also progress to oth- bal issues of sarcopenia in the elderly population.69,
er modalities such as jogging, hiking, rowing, and 70 As an original aerobic training program for sed-
stair-climbing. Aquatic exercise and stationary cycle entary aged people, aerobic interval training (AIT;
exercise may be advantageous for those with lim- weekly exercise sessions with 4-minute repetitions
or other proprietary information of the Publisher.

ited tolerance for weight bearing activity. Sessions at a moderate aerobic intensity alternated with one-
should be a minimum of 10 minutes for intermittent minute repetitions at a sub-high aerobic intensity)
AE, and intended to reach energy expenditure goals could next be considered in sarcopenia. AIT im-
of a minimum of 100-250 kcal per session. Activi- proves aerobic capacity and maximal aerobic power
ties do not have to be done at one time but can be in sedentary aged subjects, while a sub-high aerobic

138 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE February 2013


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

Role of exercise on sarcopenia in the elderly MONTERO-FERNÁNDEZ

intensity repetitions program tends to increase the age to accommodate improvements in strength and
metabolic stimulus to resistance exercise in an aero- muscle hypertrophy. Varying the type of exercises,
bic training program.71 increasing the level of resistance; increasing by 5%
up to 40% of 1 RM for arm exercises and up to 60%
Progressive resistance exercise (PRE) of 1 RM for leg exercises, adding a second set of
exercises without increasing level of resistance and
The current guidelines also call for PRE to be per- adding a third day of resistance training during the
formed two or more nonconsecutive days per week, week are some suggestions to pertain to progres-
using a single set of 8-10 exercises for the whole sion in PRE.62
body, and at a moderate (5-6 RPE out of 10) to vig-
orous (7-8 RPE out of 10) level of effort that allows Flexibility
8-12 repetitions.8, 40

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The type of recommended exercise are muscle There are a small number of studies that have
strengthening activities that involve all the major documented the effects of flexibility exercises in

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muscle groups (legs, hips, chest, back, abdomen, older populations. There is some evidence that flex-
shoulders and arms), with a progressive weight ibility can be increased in the major joints by these
training program, stair climbing, and other strength- exercises; however, how much and what types of

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ening activities that use the major muscle groups, or flexibility exercises are most effective have not been
weight bearing calisthenics (8-10 exercise involving completely established.40 The ACSM recommenda-
the major muscle groups of 8-12 repetitions each). tions states that flexibility exercise should be done

IG E
Do not forget about providing a-2 minutes of rest
between exercises. Some PRE training examples
at least two days per week, ten minutes per day at a
moderate intensity (5-6) on a scale of 0 to 10 and in-
R M
alternating between upper and lower body work, cluding exercise for the neck, shoulder, elbow, wrist,
should be the following: hip, knee and ankle.40 Preferably, flexibility activities
—— upper body: chest press, shoulder press, tri- are performed on all days that aerobic or muscle-
ceps extension, biceps curl, lateral pull-down (up- strengthening activity is performed.
P A

per back);
—— midsection of the body: lower-back extension, Balance
O V

abdominal crunch/curl-up;
—— lower body: quadriceps extension or leg press, There are no specific recommendations regard-
C ER

leg curls (hamstrings), calf raise. ing specific frequency, intensity, or type of balance
Due to the disproportionate degree of muscle at- exercises for older adults. Preferably, older adults
Y

rophy and strength decline of the lower limb mus- at risk of falls should do balance training three or
culature during aging,4 a PRE intervention model more days a week. The exercises can increase in
for positive effects on lower-extremity strength is difficulty by progressing from holding onto a stable
IN

recommended to provide enhancement of overall support (like furniture) while doing the exercises to
functional capacity. doing them without support. Participation in Tai-Chi
The technique of this PRE prescription refers to classes also improves balance and reduces the risk
M

perform each exercise through a full range of mo- of falls.


tion, in a controlled rhythmic manner, and at a slow The ACSM guidelines recommend activities that
to moderate speed, avoiding breath-holding and include the following:40 progressively difficult pos-
straining (Valsalva manoeuvre) and emphasizing tures that gradually reduce the base of support (e.g.,
proper body mechanics throughout each exercise. two-legged stand, semitandem stand, tandem stand,
They should be repeated until the point at which it one-legged stand); dynamic movements that perturb
would be difficult to do another repetition without the centre of gravity (e.g., tandem walk, backward
or other proprietary information of the Publisher.

help. walking, sideways walking, heel walking, toe walk-


Following a familiarization period, in which very ing circle turns, standing from a sitting position,
low dosage training takes place 1-2 times per week walking on compliant surface such as foam mattress-
it may be expected that older adults with sarcopenia es, maintaining balance on moving vehicles such as
can benefit from gradual increases in training dos- bus or train); stressing postural muscle groups (e.g.,

Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 139


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

MONTERO-FERNÁNDEZ Role of exercise on sarcopenia in the elderly

heel stands, toe stands) and reducing sensory input bed based exercise should be considered as a start-
(e.g., standing with eyes closed). ing point and used by frail patients.
Older adults face multiple barriers to practice ex-
Exercise precautions ercise regularly and therefore experience difficulties
starting with a PA program and adhering to it. These
Common problems with exercise in the elderly barriers include lack of knowledge about the benefi-
are those related to comorbidity, which is a very fre- cial effects of PA, fear of falling and problems to find
quent condition in this group of age. It is not a con- and get to an exercise facility near home.75 A more
traindication by itself, but requires a careful medical structured environment with classes (e.g., yoga, pi-
evaluation before beginning the exercise program. It lates, dancing) or in a fitness center (with a trainer
is appropriate to initiate activity at modest duration or specialized equipment) may provide a variety of
and intensity with regimens that progress gradually activities that may engage the individual, but home-

® A
over extended time intervals. Particularly in these based exercise (e.g., jogging, using an exercise bike)
circumstances, it is important to limit activity to what may result in better adherence given low cost and

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a patient feels is comfortable, progressing in small convenience. Data are lacking in determining the
increments and prioritizing longer duration over optimal setting to perform exercise (e.g., outdoors
higher exercise intensity. Absolute contraindications versus indoors, home versus fitness center).76, 77 A

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are mainly cardiovascular diseases: recent heart at- systematic review of six trials evaluated the efficacy
tack, unstable angina, uncontrolled hypertension, of home-based versus hospital (center)-based exer-
acute heart failure and blocking complete AV.62, 72 cise programs in older adults.77 In the short-term,

IG E
The elderly are extensive users of both prescrip-
tion and over-the-counter medications and they
center-based programs were superior to home-
based programs in patients with peripheral vascu-
R M
tend to use them chronically. These medications can lar disease. However, in the long-term, home-based
have negative effects on performance and they can programs were superior to center-based programs
lead to increasing adverse effects. Clinicians should in terms of adherence.
be alert to elderly taking statins, beta-blockers and Health care providers are perceived as respected
P A

vasodilators drugs.73 sources of health information and should thus take


The main risks of aerobic and strength training an active role in promoting PA. However, less than
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are the risk of musculoskeletal injuries and cardio- 50% of older adults report that their physicians have
vascular risk. Patients should be advised that muscle recommended exercise. The primary care setting
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soreness is normal at first and should subside in a would appear to be a good place for health promo-
few weeks. If injury or illness interrupts an activity tion because most older adults visit their primary
Y

routine, resuming activity at a lower intensity level care provider more than once a year.40 However,
is possible once sufficient healing has occurred. Any most observational studies and randomized trials
potential risks of routine exercise do not outweigh have found conflicting results on whether usual
IN

its benefits, in the absence of a contraindication to counselling in a primary care setting is sufficient to
exercise. effect behavioral change.78, 79
General recommendations for safety, particularly
M

in the initial stages of exercise, include exercising


with one other person, carrying a cell phone to fa- Conclusions
cilitate calling for emergency help, well-lit and ven-
tilated rooms and adhering to an activity level that is In conclusion, motivating older persons to in-
comfortable and with normal breathing.74 crease their physical activity level as well as provid-
These data support the notion that supervised or ing safe access to exercise programs seems to be a
group settings may be preferable for elders, with mandatory task. Many previous authors have pro-
or other proprietary information of the Publisher.

regard to both safety and compliance. It is necessary vided data and interpretation critical to understand-
to wear proper footwear and clothing, good nutri- ing that muscle weakness, reduction in muscle mass
tion and liquid intake and adequate sleep. Exercise and reduction in PA occur during life span and lead
machines have advantages for older, especially frail, to sarcopenia and disability in some older people.
as the range of motion is easier to control. Chair and PA, which is a modifiable lifestyle behavior, can par-

140 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE February 2013


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

Role of exercise on sarcopenia in the elderly MONTERO-FERNÁNDEZ

tially reverse this muscle dysfunction in the elderly, 11. Balboa-Castillo T, Guallar-Castillon P, Leon-Munoz LM, Gra-
ciani A, Lopez-Garcia E, Rodriguez-Artalejo F. Physical activity
as well as benefit every part of the body and sub- and mortality related to obesity and functional status in older
stantially extend independent functional lifespan. adults in Spain. Am J Prev Med 2011;40:39-46.
In addition to our traditional recommendations of 12. Mayhew DL, Kim JS, Cross JM, Ferrando AA, Bamman MM.
Translational signaling responses preceding resistance training-
the health benefits of exercise in young people, we mediated myofiber hypertrophy in young and old humans. J
should stress the harms of inactivity even in the old- Appl Physiol 2009;107:1655-1662.
est adults and view the inactive elder population as 13. Chastin SF, Ferriolli E, Stephens NA, Fearon KC, Greig C. Rela-
tionship between sedentary behaviour, physical activity, mus-
abnormal and consider them at high risk of disease cle quality and body composition in healthy older adults. Age
and disabilities.80 Ageing 2012;41:114-4.
We would like to finish our review honoring Jer- 14. Moyer VA, U.S. Preventive Services Task Force. Behavioral
counseling interventions to promote a healthful diet and physi-
emy Morris, one of the first clinicians who advised cal activity for cardiovascular disease prevention in adults: U.S.
about the health benefits of exercise, remembering Preventive Services Task Force recommendation statement.

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his last investigation paper, published in 2009, some Ann Intern Med 2012;157:197-204.
15. Breen L, Phillips SM. Skeletal muscle protein metabolism in the
days before his dead at the age of 99:81 “We now elderly: interventions to counteract the “anabolic resistance” of

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know that regular physical activity of 150 minutes/ ageing. Nutr Metab 2011;8: 68.
week of moderate intensity physical activity reduces 16. Pillard F, Laoudj-Chenivesse D, Carnac G, Mercier J, Rami J,
Rivière D, Rolland Y. Physical activity and sarcopenia. Clin
the risk of numerous chronic diseases, preserves

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Geriatr Med 2011;27:449-70.
health and function (both physical and mental) into 17. Nair KS. Aging muscle. Am J Clin Nutr 2005;81:953.
old age, and extends longevity. The current chal- 18. Frontera WR, Reid KF, Phillips EM, Krivickas LS, Hughes VA,
Roubenoff R et al. Muscle fiber size and function in elderly
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sedentary societies”. IG E
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20. Visser M, Goodpaster BH, Kritchevsky SB et al. Muscle mass,
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Vol. 49 - No. 1 EUROPEAN JOURNAL OF PHYSICAL AND REHABILITATION MEDICINE 141


not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo,
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other

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