Effects of Age and Resistance Training on Skeletal Muscle A Review

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					                                Effects of Age and Resistance Training on Skeletal
                                Muscle: A Review
                                Jane F Hopp
                                PHYS THER. 1993; 73:361-373.

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                                    Anatomy: Central Nervous System and
                                Neuromuscular System
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                                    Therapeutic Exercise
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Clinical Perspective

Effects of Age and Resistance Training on Skeletal
Muscle: A Review

As humans age, there is a decrease in the ability of skeletal muscle to generate
force. This review describes alterations in the neuromuscular systems of humans
 and animals that may be responsible for the diminished force-generating capacity
 of older muscles. The effects of resistance training on the force-generating capacity
 of older muscles in humans and o n the neuromuscular system of humans and
 animals are then examined. The age-related decline in force-generating capacity
 may be due, in part, to a loss of motor units and to a decline in muscle mass.
 Fiber atrophy and, possibly, loss of muscle fibers contribute to the decline in mus-
 cle mass in older persons. High-intensity resistance training appears to attenuate
 the age-related decline in force-generating capacity in humans and cause fiber
 hypertrophy of old muscle fibers. Investigations of the effects of age on the neuro-
 muscular system and of the effects of resistance training o n the neuromuscular
system and thefunctional capacity of older persons are essential for the develop-
 ment of cost-effective intenentions that will increase the physical capacity of older
persons. [HoppJE Effects of age and resistance training o n skeletal muscle: a
 review. Phys Ther. 1993;  73~361-373.1 '

Key Words: Aging; Functional training and activities; Geriatrics;Muscle p d o r -
munce, general; Neurophysiologylneuroanatomy.

An increasing number of older per-                 sented. To provide a basis for under-          cross-sectional areas of the gastrocne-
sons are thought to be living at or just           standing the animal and human find-            mius and soleus muscles of men and
above a threshold of physical capaci-              ings, differences in species' life spans,      women 82 to 100 years of age were
ty.' The occurrence of any illness may             muscle fiber classification schemes,           found to be less than those of men
severely limit their functional capaci-            and exercise training protocols are            and women younger than 82 years of
ty.' Thus, it is important to under-               reviewed. Clinical implications and            age.9 In the older individuals, how-
stand the effects of age on physical               future research concerning aged mus-           ever, the declines in the cross-
capacity and how extrinsic factors (eg,            cle resistance training are discussed.         sectional areas of the gastrocnemius
exercise) may alter an older person's                                                             and soleus muscles were found to be
physical capacity. This review exarn-              Effects of Age on the                          less than the reductions in the
ines age-related alterations in the                Neuromuscular System                           amounts of torque generated by the
neuromuscular ~ y s t e m and~the
                             ~- ~                                                                 muscles.9 This discrepancy may be
effects of aged skeletal muscle resis-             Decreases in skeletal muscle mass in           due, in part, to increases in fat and
tance training on the neuromuscular                aged organisms have frequently been            connective tissue in older muscles. An
system."s2+30 Findings from both                   do~umented.9~3~-33 example, using
                                                                      For                         increase in fat infiltration in lean
animal and human studies are pre-                  ultrasonic imaging techniques, the             tissue of legs of sedentary older men
                                                                                                  has been reported.34 In rats, age-
                                                                                                  related increases in endomysiaB5 and
                                                                                                  perimysial36 connective tissue have
JF Hopp, PhD, PT, is Assistant Professor, Department of Physical Therapy, College of Associated   been found. Other alterations in the
Health Professions, and Section of Geriatric Medicine, Department of Medicine, College of Medi-
cine, University of Illinois at Chicago, 1919 W Taylor St (M/C 898), Chicago, IL 60612 (USA).
                                                                                                  neuromuscular system may also con-

This article was submitted May 4, 1992, and was accepted Febma y 2, 1993.

24 / 361                                                                              Physical Therapy /Volume 73, Number fillJune1993
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tribute to the decline in older muscle      longevity of I-at~.3~  Colonies are          Based on color, skeletal muscles are
force-generating capacity.                  housed either under barrier                  classified as either "red" or "white."
                                            @athogen-free) or nonbarrier condi-          "Red" muscles have a high capillary
In this section, alterations in the neu-    tions. There is an increased incidence       density, giving them a reddish appear-
romuscular system that may account          of infectious diseases in rats raised in     ance. "Red" muscles are considered
for the decline in an older muscle's        nonbarrier conditions as compared            to have a high capacity for aerobic
force-generating capacity will be re-       with those raised in barrier condi-          metabolism. In contrast, "white" mus-
viewed. The effects of age on motor         tions.37 It is difficult, therefore, to      cles have a low capillary density, giv-
unit size, number, and structure; skel-     determine whether decreases in phys-         ing them a pale appearance. "White"
etal muscle cross-sectional area and        ical capacity with age in nonbarrier-        muscles are considered to have a
number; and skeletal muscle anaero-         housed colonies are due to the aging         high capacity for anaerobic metabo-
bic and aerobic metabolism in rats          process or to the increased incidence        lism. This classification scheme does
and humans are discussed. Overviews         of diseases. As an example, rats raised      not characterize a muscle's contractile
of the species and muscle fiber classi-     in nonbarrier conditions are more            properties.
fication schemes often used in studies      prone to respiratory infection^?^
investiga.tingthe effects of age on the     which may influence the oxidative            Skeletal muscles are classified based
neuromuscular system are also               capacity of skeletal muscles indepen-        on their contractile characteristics by
presented.                                  dent of the effects of age.                  determining the type of myosin aden-
                                                                                         osine triphosphatase (ATPase) in the
fiperimental Models and                     In humans, the effects of age on dif-        muscles' fibers.49A histochemical
Designs                                     ferent physiological systems have            reaction for myosin ATPase is often
                                            been found to vary among systems             used to distinguish two types of mus-
Species studied. The effects of age         and individuals.14~42~6    Skeletal muscle   cle fibers: slow and fast.49
on the neuromuscular system have            can be influenced by many factors,
been studied primarily in rodents and       including heredity, nutrition, and           Peter et also attempted to utilize both
humans. The laboratory rat is an            physical activity.'4,31,47 In experimental   contractile and metabolic properties
often-used rodent model in investiga-       studies, these factors may be difficult      of a muscle to characterize its compo-
tions of the effects of age on the neu-     to control. Therefore, when reporting        sition. A muscle is classified as slow
romuscular system because rats have         findings of effects of age on the hu-        oxidative (SO), fast oxidative glyco-
a relatively short life span.37 In addi-    man neuromuscular system, detailed           lytic (FOG), or fast glycolytic (FG)
tion, maintenance costs for rats are        descriptions of the subjects (eg, chro-      based on the muscle fibers' histo-
comparatively low, permitting produc-       nological age, lifestyle, health and         chemical reaction for myosin ATPase
tion and maintenance of large colo-         nutritional status, physical activity        and their glycolytic and oxidative
nies of animals for study.37                level) should be provided in order to        enzyme activity l e ~ e l s . 5 ~ oxida-
                                            aid in the interpretation of the results.    tive muscles are considered slow-
A question that arises is, "How old is                                                   twitch, with moderate oxidative capac-
an old rat?" In many studies, the "old"     Finally, changes in skeletal muscle          ity and low glycolytic capacity. Fast
experimental group has been com-            occur over the life span of a species.4"     oxidative glycolytic muscles are con-
posed of rats that are 18 to 28 months      Thus, different age groups (young,           sidered fast-twitch,with high oxidative
of age.2.3.12316s21,3Mo
                     Some strains (eg,      adult, and old) of a species should be       capacity and moderate to high glyco-
Fischer 344 Brown Norway F1 hy-             studied when investigating the effects       lytic capacity. Fast glycolytic muscles
brid), however, have been reported          of age on the neuromuscular system.          are considered fast-twitch, with high
to survive approximately 40 months          Caution should also be used when             glycolytic capacity and low oxidative
(unpublished information, National          comparing the results of studies using       ~apacity.5~
Institute on Aging). In addition, gen-      different age groups of the same
der can affect the survival rate. For       species.                                     The classification scheme of Peter et
example, the 50% survival rate (age at                                                   al,5O however, has several limitations.
which 50% of the colony has died) of        Skeletal muscle fiber composi-               The classification scheme was devel-
the Fischer 344 Norway Brown F1             tion. In many studies investigating          oped by selecting guinea pig and
hybrid females is 190 weeks com-            the age-related changes in the neuro-        rabbit limb muscles composed pre-
pared with 140 weeks for the males          muscular system, muscles are classi-         dominantly or exclusively of one type
(unpublished information, National          fied based on their fiber type compo-        of fiber and then studying the meta-
Institute on Aging). Thus, to define a      sition. In this review, fiber-typing         bolic properties of these muscles.%In
rat as "old" requires knowledge of          nomenclature from the original arti-         contrast, many muscles in a variety of
the strain survival curve for the gen-      cles will be used when skeletal mus-         species are composed of a variety of
der st~tlied.3~8~~                          cles are referred to by their fiber          fiber types. In addition, since the de-
                                            composition.                                 velopment of the classification scheme
Housing conditions of a rat colony                                                       of Peter et al,50 incompatibility be-
will also affect general health and                                                      tween the myosin-based fiber type

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classification system and classifications     to 58 years of age (29.9k25.5 p v . 5          with increasing age.5 In the biceps
based on metabolic enzyme activity            The increase in the size of aged mo-           brachii muscle, individuals over
levels has been re~orted.5~-53  For           tor units may be due to surviving              60 years of age had approximately
example, large variations in mitochon-        axons adopting denervated muscle               half the number of motor units as
drial succinate dehydrogenase (SDH)           fibers (formation of larger or giant           compared with individuals under
enzyme activity exist in muscle fibers        motor unitsj5,"r to hypertrophy of             60 years of age.7After the age o f
stained for myosin ATPase.5'-55 Yet, the      surviving muscle fibers. If larger or          60 years, motoneuron counts in the
histochemical reaction for myosin             giant motor units d o occur in older           lumbosacral portion of human spinal
ATPase is often used to divide muscles        individuals, the degree of control             cords decreased by 50% as compared
into slow and fast categories, and then       older individuals have over their              with prior to 60 years of age.6 Thus, a
fast muscles are further subtyped into        muscles may decrease.                          factor contributing to the decline in
SO, FOG, and FG subcategories based                                                          aged human muscle force-generating
on the intensity of the SDH reaction                                         f
                                              Loss of recruitment o some o the
                                                                    f                        capacity appears to be an age-related
end-product.                                  remaining giant motor units o r firing         reduction in the number of motor
                                              of giant motor units at suboptimal             units. This decline in the number of
In another classification scheme, that        frequencies during a maximal volun-            motor units, however, appears to
of Brooke and Kaiser,5*fibers are             tary contraction (MVCj could produce           begin only after the age of 60 years.
stained for myosin ATPase following           a decline in muscle force-generating
acid or alkaline preincubations. Classi-      capacity in older persons. Vander-             There is evidence that the conduction
fication using the Brooke and Kaiser          voort and McComas6 assessed                    velocities of surviving motoneurons
method54 yields the following fiber           whether older individuals activated            slow with age.4,5The conduction
categories: type I (slow-twitch) and          their ankle plantar-flexor and dorsi-          velocities of the fastest-conducting
three subcategories of type I1 (fast-         flexor muscles optimally. The                  nerve fibers innervating the extensor
twitch), type IIa, type IIb, and type IIc.    amounts of torque produced during              digitorum brevis muscle fibers de-
Metabolically, type I fibers are often        an MVC and during application of               creased in 60- to 96-year-olds as com-
correlated with SO fibers, type IIa           supramaximal electrical stimulations           pared with 3- to 58-year-olds.5In
fibers with FOG fibers, and type IIb          superimposed on an MVC were re-                addition, marked slowing of conduc-
fibers with FG fibers. Type IIc fibers        corded. The amount of torque gener-            tion velocities in the distal regions of
are rarely identified in normal, ma-          ated during an MVC was greater in              some axons in 24- to 36-month-old
ture human mu~cles.5~ myosin
                          In                  men than in women, regardless of               rats suggests that axons undergo seg-
ATPase-stained fibers in a variety of         age. The amount of torque generated            mental demyelination.Vhis slowing
species, however, the activity levels of      during an MVC declined after 60 years          may be indicative of an age-related
oxidative and glycolytic enzymes have         of age in both men and women. Dur-             dysfunction of Schwann cells. The
been found to vary within a specific          ing an MVC, electrical stimulation of          surviving slower-conducting motoneu-
fiber type ~ategory.555~                      the motoneurons produced no addi-              rons may innervate slower-twitch
                                              tional torque in either the plantar-           muscle fibers. Because a slower-twitch
It is difficult, therefore, to draw con-      flexor or dorsiflexor muscles in the           fiber generates lower force per unit
clusions about a muscle's contractile         majority of men and women, 20 to               area of the fiber, a predominance of
properties based solely on its meta-          100 years of age.Thus, older individ-          slower-conducting motor units in
bolic properties or about a muscle's          uals appear to be able to use de-              older persons could contribute to the
metabolic properties based solely on          scending motor pathways to optimally           decreases observed in force-
its contractile properties. One reason        activate ankle plantar-flexor and dorsi-       generating capacity.
for the lack of correlation between           flexor muscles. Further investigation
contractile and metabolic classifica-         is needed to determine whether the             Effect of Age on Skeletal
tions is that metabolic features are          electrophysiological findings in the           Muscle Morphology
very mutable and reflect the type,            ankle plantar-flexor and dorsiflexor
intensity, and duration of activity of a      muscles6 are indicative of what occurs                           and
                                                                                             In rats2.~O3l3,l647 humans,",14,15
given fiber in a given muscle.5"              in other muscles.                              decreased muscle mass has been
                                                                                             attributed to decreases in the num-
Effect of Age on the Motor Unit               A decline in the number of motor                                            of
                                                                                             ber2,13.'5,47and area10~1z-15 the mus-
                                              units has been found in older hu-              cle fibers. In 24-month-old rat soleus
Campbell et a15 found that the size of        mans.5,7jxBetween the ages of 3 and            muscles, atrophy and loss of mo-
human motor units increased with              58 years, the mean number of human             toneurons were found.z In male and
increasing age. The mean amplitude            extensor digitorum brevis muscle               female Wistar rats, tibialis anterior
of extensor digitorum brevis muscle           motor units was 197558 units.5After            muscle weight decreased over 50%
single motor unit action potentials                      f
                                              60 years o age, the number of motor            between 12 and 24 months of age.13
recorded from humans 60 to 96 years           units decreased to fewer than                  In the tibialis anterior muscles of
of age (47.6k43.2 p,V) was greater            Between the ages of 60 and 96 years,           24-month-old rats, the area of "white"
than those recorded from humans 3             the number of motor units decreased            fibers and the number of "red" fibers

                                                                                  Physical Therapy /Volume
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decreased compared with the muscles          81 years of age, no gender differences        The amounts of atrophy that occur in
of 12-month-old rats.13 Similar find-        in the percentages of type I and type         old muscle fibers appear to be influ-
ings were observed in psoas major            I1 fibers were found in vastus lateralis      enced by the amount and type of
muscles from the 24-month-old male           or biceps brachii muscle biopsy sam-          muscle activity the old muscle
Wistar rats.'3                               ples for any of the age groups.14             undergoes.59
                                             There was, however, a decline in type
Fibers in both the soleus and exten-         I1 fiber area, especially type IIb fiber      In addition, in rats, the decreases in
sor digitorum longus muscles from            area, in the vastus lateralis muscle          muscle fiber numbers and in type I1
30-month-old female albino rats de-          biopsy samples from the oldest indi-          or FOG fiber percentages d o not
creased 25% to 30% as compared               viduals ( 7 8 8 1 years of age) as com-       appear to be consistent aging phe-
with fibers of muscles from 3- to            pared with fiber areas in muscle sam-                              Differences ~ ~
                                                                                           n 0 m e n a . ~ . ~ ~ , ~ 3 , ~ ~ , are seen
4-month-old rats. In both muscles,           ples from younger individuals.14The           between muscles in the same strain of
there were decreases in the percent-         biceps brachii muscle of the 78- to           rats47and in the same muscles be-
ages of FOG fibers and increases in          81-year-old individuals did not show          tween               Eddinger et a147
the percentages of SO fibers." There         any decline in fiber area with age as         proposed that fiber numbers are
were ncl differences in the percent-         compared with fiber areas in muscle           genetically determined. Thus, changes
ages of type I, IIa, or IIb fibers in        samples from younger individuals.14           in fiber number and percentages with
extensor digitorum longus muscles            In autopsied whole vastus lateralis           age may be genetically
from barrier-reared Fischer 344 male         muscles from men 19 to 37 and 70 to
rats ranging in age from 3 to 30             73 years of age, there were no differ-        The disparate findings regarding the
months.47 In contrast, the soleus and        ences between the age groups in the           effects of age on the area and percent-
diaphragm muscles from the 30-               percentages of type I and type I1 fi-         ages of fibers in vastus lateralis mus-
month-old Fischer 344 rats had a             bers or in the type I and I1 fiber ar-        cle biopsy ~ a m p l e s ~ may be due to
higher percentage of type I fibers and       eas.l5 Both the size of the muscle and        differences in the biopsy sites used in
a lower percentage of type IIa fibers        the total number of fibers in the vas-        the studies. The sizes and percentages
than did muscles from the younger            tus lateralis muscles, however, de-           of fiber types vary in different parts of
I- at^.*^ The total number of fibers per     creased with age.'5                           the muscle.GOThus, findings may vary
cross-sectional area of muscle, how-                                                       among studtes if different portions of
ever, did not change with age in ei-         The ability of aged rat and human             the vastus lateralis muscle are sam-
ther the extensor digitorum longus or        muscles to generate force would               pled. Sampling from a single area of
soleus muscles of the Fischer 344            decrease as a result of an age-related        the vastus lateralis muscle may not
I-~s.4~                                      atrophy or loss of muscle fibers. An          give findings representative of the
                                             age-related atrophy or loss of muscle         whole muscle. This could account, in
Brown found no change in the total           fibers could also result in an eventual       part, for the divergent findings re-
number of fibers in both soleus and          decrease in the size of aging motor           garding the effects of age on human
extensor digitorum longus muscles in         units (eg, the number of fibers inner-        muscle morphology in vastus lateralis
24-month-old Wistar rats as compared         vated by an axon). The decrease in            muscle biopsy samplesl2J4as com-
with 12-month-old rats.lG Fiber atro-        the size of motor units may be due to         pared with whole vastus lateralis
phy, however, was noted in the mus-          a decline in the capacity of aging            mu~cles.~5
cles after 12 months of age.16 Type I1       motoneurons to sprout nerve termi-
fiber atrophy has also been found in         nals. Denervation of fibers within the        Effect of Age on Skeletal
soleus and extensor digitorum longus         muscle, and atrophy and eventual loss         Muscle Metabolism
muscles of 28- to 36-month-old male          of the denervated muscle fibers,
Wistar rats as compared with muscles         would then occur. This hypothesis is          Muscle metabolism is one of the
in younger Wistar rats.1°                    supported by findings of reductions           factors that influence the length of
                                             in the terminal branching of mo-              time a maximal contraction or a se-
In biopsy samples from vastus latera-        toneurons and the length of the end-          ries of repeated contractions can be
lis muscles of sedentary men, 20 to          plates in the soleus muscles of 28-           maintained. The activity levels of en-
65 years of age, the percentage of           month-old female Wistar rats3 and of          zymes catalyzing skeletal muscle
type I fibers in the muscles increased       retraction of the terminal boutons            anaerobi~10,14,2~,~~~~ and aero-
with increasing age.12There were also        from the sarcolemma and destruction           bic10,14.*0,21,40<60
                                                                                                             metabolism and the
decreases in both type I and I1 fiber        of the sarcolemma infoldings in 36-           concentrations of intramuscular sub-
areas in the vastus lateralis muscle         month-old rat soleus muscles.*                strates used during anaerobic metabo-
biopsy samples from the older men                                                          liSm17-19,22,62in aged rat10,17-21,3WO
as compared with fiber areas in bi-          The conflicting findings regarding the        and humanl4~22~62    muscles have been
opsy samples from the younger                effect of age on motor unit size (in-         measured. Both the presence1O.l7-22
men.12 The decrease in fiber area in         creased5 versus decreased2J0.12-15)                                   of
                                                                                           and absen~e14~3-~.61 age-related
the older men was greatest in type I1        may be due to differences in activity         declines in enzymatic activity lev-
fibers." In men and women up to              levels among muscle groups studied.           el~~OJ4820321-~~61and intramuscular

Physical Therapy /Volume 73, Number 6/June 1993
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substrate ~oncentrationsl7-19.2~,~8~39       primarily of FG fibers) from 9- and            glycogen were found in 10- and 24-
have been reported.                          24-month-old barrier-raised male               monthald untrained barrier-raised
                                             Long-Evans rats, no differences in HK,         male Fischer 344 rats' "white" gastroc-
Decreases in glycolyti~,~0~2~                phosphorylase, and pyruvate kinase             nemius (FG fibers), "red" gastrocne-
 P-oxidation,20sl1 and citric acid cy-       (glycolytic enzymes); HAD (a                   mius (FOG and SO fibers), plantaris
~lel0~~0enzyme activity levels have          P-oxidation enzyme); and CS and                (FOG and SO fibers), and soleus (SO
been found in older rat muscles hav-         succinate dehydrogenase (citric acid           fibers) muscles3H and in 9- and 28-
ing a high percentage of slow-twitch         cycle enzymes) activity levels were            month-old untrained barrier-raised
fibers. In contrast, rat muscles com-        found.40 In 56 sedentary men, 22 to            male Long-Evans rats' soleus
posed of a high percentage of fast-          65 years of age, no differences in             muscles.39
twitch fibers appear to decrease their       phosphofructokinase, LDH, HAD, and
glycolytic capacity but increase their       CS enzyme activity levels in vastus            In summary, it appears that there is
oxidative capacity with age.10.2l Bass et    lateralis muscle biopsy samples from           little decline in anaerobic and aerobic
all0 reported that activity levels of        younger and older individuals were             metabolism in "active, community-
three glycolytic enzyrnes-triosephos-        found.61 In addition, no declines in           living" 80-year-old individuals when
phate dehydrogenase (TPDH), lactate          hexokinase, LDH, HAD, and CS en-               compared with younger individu-
dehydrogenase (LDH), and glycerol-3-         zyme activity levels were found in             als.l4,22Caution should be exercised
phosphate dehydrogenase (GPDH)-              biopsy samples of vastus lateralis and         in applying this conclusion to all
were decreased in extensor digitorum         biceps brachii muscles from 80-year-           older persons, however, until "active"
longus ("fast") and soleus ("slow")          old men and women as compared                  and "community-living" are better
muscles of 28- to 36-month-old un-           with younger men and women.14 In               defined.
trained male Wistar rats as compared         this study,l4 no differences in enzyme
with the same muscles in 3-month-old         activity levels between sexes were             The findings regarding the effect of
untrained rats. Activity levels of malate    found except for higher HK activity            age on anaerobic and aerobic metabo-
dehydrogenase and citrate synthase           levels in vastus lateralis and biceps          lism in rats' muscles appear to be
(CS) (citric acid cycle enzymes) were        brachii muscle biopsy samples from             conflicting. The disparate metabolic
only decreased in the soleus muscles         women as compared with men.                    findings in old rats' muscles can be
of the older rats.1°                                                                        attributed, in part, to differences in the
                                             Conflicting findings regarding the             ages of the rats investigated. Decreased
The activity levels of LDH and hexoki-               f
                                             effect o age o n intramuscular anaero-         enzyme activity levels and intramuscu-
nase (HK) (glycolytic enzymes) and of        bic substrate contents have also been          lar substrate concentrations were often
3 hydroxyaxyl CoA dehydrogenase              reported.17-l9,",39 Ermimil7 and Er-           reported in Wistar rats older than
(HAD) (a P-oxidation enzyme) de-             mimi and Verzar18 found that the               30 months of age.10,17-19   Witar rats
creased in the extensor digitorum            concentrations of phosphocreatine              rarely survive to 40 months of age.
longus and soleus muscles from 24-           (PC) were reduced in the rectus fem-           Thus, rats 30 months and older could
month-old untrained male Wistar rats         oris and gluteus maximus ("white")             be considered to be "very old."18 The
as compared with 3-month-old rats of         muscles and the piriformis, vastus             Wistar rats were also raised under
the same strain2l Although the activity      intermedius, and gluteus maximus               nonbarrier conditions10J7-21 and thus
level of CS decreased in the 24-             centralis ("red") muscles from 33- to          may have had respiratory diseases that
month-old rats' soleus muscles, the          37-month-old untrained Wistar rats as          might have affected their aerobic me-
CS activity level increased in the rats'     compared with the same muscles of              tabolism. When no decline in enzyme
extensor digitorum longus muscles.21         rats younger than 33 months of age.            activity levels40and intramuscular
The activity levels of acyl-CoA dehy-        In the "red" muscles, adenosine tri-           substrate ~oncentrations3~.39  were
drogenase and HAD (P-oxidation               phosphate (ATP) and adenosine di-              reported, rats younger than 28 months
enzymes) and CS, NAD-isocitrate              phosphate (ADP) concentrations were            of age were investigated. In these
dehydrogenase, and 2-oxoglutarate            also significantly reduced. l7.18 In addi-     studies,jM0 the rats were also raised
dehydrogenase (citric acid cycle en-         tion, the intracellular glycogen con-          under barrier conditions. Thus, these
zymes) were decreased in 24-month-           tent decreased by 50% in the "white"           animals3-0 would be less likely to
old untrained male Wistar rats' soleus       and "red" muscles of the old rats.l9 In        experience respiratory infections that
muscles ("red oxidative") as com-            vastus lateralis muscle biopsy samples         might affect the oxidative capacity of
pared with the soleus muscles of             from healthy men and women, 52 to              muscle, independent of age. In addi-
6-month-old untrained rats.1°                79 years of age, intracellular concen-         tion, in rats older than 30 months, the
                                             trations of ATP, ADP, adenosine                decline in metabolism may be due to
Other investigators have reported no         monophosphate (AMP), and PC de-                a decrease in physical activity rather
age-related declines in glycolyt-            creased only j% as compared with               than age. The activity of the 33- to
i~,14.~0@                   and citric
          P-oxidati0n,1~,40~~~               contents in muscle biopsy samples              37-month-old rats, for example, was
acid cy~lel4~40~60
                enzyme activity levels       from men and women approximately               described as "slow," whereas those
in rat40 and human14z61 muscles. In          40 years younger.22No differences in           rats less than 33 months of age were
epitrochlearis muscle (composed              resting concentrations of ATP, PC, and         described as "lively and active."l8

28 / 365                                                                         Physical Therapy /Volume
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Eftects of Resistance                        Maximum aerobic capacity is the                with pretraining forces.23 In the 61- to
Training on Aged Skeietal                     maximum rate at which oxygen can              80-year-old age group, however, there
Muscle                                        be used by the muscles. It does not           were no increases in forces generated
                                              describe the anaerobic capacity of an         by any of the muscle groups follow-
Exercise training is thought to attenu-       individual and therefore should not           ing isometric resistance trai11ing.~3
ate the age-related decline in human          be used when describing activities            The maximum isometric forces gener-
physical capacity.' In an attempt to          that require little oxygen (eg, high-         ated by the different muscle groups in
increase the force-generating capacity        intensity resistance training). The           the different age groups following
of aged muscles and decrease the              amount of exercise performed is               balance, flexibility, and coordination
effects of age on the neuromuscular           expressed as the number of minutes            training were less than those gener-
system, resistance training (eg,              per day times days per week times             ated by the age-matched isometric
strength training) of aged human              total weeks the exercise was                  resistance trained groups.23 The lower
muscle has been performed, with               performed.                                    isometric forces generated following
varying amounts of success repon-                                                           balance, flexibility, and coordination
ed.l2123-?,0In this section, an overview      Effect of Resistance                          training as compared with isometric
of exercise training protocols will be        Training on Aged Muscle                       resistance training may be due to a
presented. The effects of resistance          Force-Generating Capacity                     lack of training and testing specificity
training on aged human muscle force-                                                        and to a lack of any overload being
generating capacity and on aged rat          The effects of isometric and isotonic          applied to the muscles in the balance,
and hurnan neuromuscular systems             resistance training on muscle force-           flexibility, and coordination training
are then examined.                           generating capacity in healthy,                group.
                                             community-living older persons have
Exercise Training Protocols                  been inve~tigated.23-~5  Liemohn23            In contrast to Liemohn's findings,23
                                             investigated the effects of age and           KauffmanZ4   found that the isometric
To obtain a training effect in muscle,       isometric resistance training on the          force generated by a small distal
an exercise overload must be ap-             force-generating capacity of human            upper-extremity muscle (abductor
plied.62 Adaptations of muscles to           upper- and lower-extremity muscles.           digiti minimi) was unchanged with
training are related to the type, inten-     Twenty-seven healthy men, 41 to               age and that high-intensity isometric
sity, and duration of the training and       80 years of age, participated in one of       resistance training increased the
to the type of muscle being exercised.       two training programs. Each training          force-generating capacity of the mus-
The extent of training is, at least in       group performed 15 minutes of exer-           cle in both younger and older hu-
pan, a function of the pretraining           cise, 3 days a week, for 6 weeks. One         mans. Ten healthy women, 20 to
state of the muscles being used in the       training group performed three iso-           26 years of age, and 10 healthy
e~ercise.6~ Exercise training protocols      metric contractions with four different       women, 65 to 73 years of age, per-
should be described by the type,             muscle groups (forearm flexors, fore-         formed two sets of 10 maximal iso-
intensity, and amount of exercise            arm extensors, knee flexors, and knee         metric contractions of the left abduc-
performed by the                             extensors). The intensities of isomet-        tor minimi muscle, three times a
                                             ric contractions were not specified.          week for 6 weeks. Prior to isometric
Types of exercises used to increase          The second training group performed           resistance training, there was no sig-
the physical capacity of older persons       balance, flexibility, and coordination        nificant difference between the
are resistance and cardiovascular            exercises, avoiding "overload" to the         younger and older women in the
endurance training.' The intensity of        knee and forearm flexor and extensor          amount of isometric force generated
exercise can be expressed in a num-          muscles. The term "overload" was not          by their abductor digiti minimi mus-
ber of different ways. In resistance         operationally defined.23 The balance,         cles. At the end of 6 weeks of training,
training, repetition maximum (RM),           flexibility, and coordination exercises       the average gains in the amount of
which describes the maximum                  were not described.'3                         isometric force generated by abductor
amount of weight that can be moved                                                         digiti minimi muscle of younger and
through a joint's full range of motion       Prior to training, isometric forces           older women were similar (819 and
a specified number of times, is often        generated by the muscle groups were           607 g).24
used to describe the intensity of exer-      lower in the older (61-80 years) age
cise.63 Also, force, torque, or power is     groups as compared with the younger           The effects of high-intensity isometric
measured during an MVC, and the              (41-60 years) age groups.23 Following         and isotonic resistance training on t h ~
intensity of resistance training is then     isometric resistance training, forces         force-generating capacity of aged
established using a percentage of the        generated by the right and left elbow         human muscles have been compared
maximum force, torque, or power              extensors and left elbow flexors in           by Perkins and Kaiser.25 Five healthy
mea~urement.~Z    During cardiovascular      the 41- to 50-year-old age group and          men and 15 healthy women, 62 to
endurance training, the intensity of         the right knee flexors and right elbow        84 years of age @=73.6), performed
exercise is expressed as a percentage        extensors in the 51- to 60-year-old age       either isometric or isotonic resistance
of maximum aerobic capacity.l.62             group were increased as compared              exercise of the plantar flexors of the

                         73, Number 6/June 1993
Physical Therapy /Volume Downloaded from by guest on December 10, 2011                          366 / 29
ankle, the extensors of the knee, and      addition, the contrasting findings of           Two subjects, who ambulated with the
the extensors of the hip, three times a                                      studies
                                           Liemohn's23 and K a ~ f f m a n ' s ~ ~         assistance of a cane prior to training,
week for 6 weeks. The isometric            reinforce the idea that the effects of          no longer used the cane following
exercise program consisted of hold-        age and resistance training may not             training.z6One of three subjects who
ing the maximum resistance load for        be the same in different muscles. The           could not rise from a chair without
each muscle group for 6 seconds,           activity levels of muscles over a life          using their arms could d o so follow-
followed by holding one half of the        span may influence the muscles' re-             ing training.26No cardiovascular com-
maximum resistance load for another        sponses to aging and training. Thus,            plications occurred during the train-
6 seconds. During a training session,      caution must be used when generaliz-            ing sessions in any of the subjects.26
each isometric resistance load was         ing results from one muscle to other            One subject, however, had to with-
held three times per muscle group.         muscles in the body.                            draw following 4 weeks of training
The isotonic resistance training proto-                                                    because of complications related to a
col consisted of performing the            There may be a reluctance on the                previously repaired hemia.26 These
10 RM for the muscle group followed        part of some physical therapists to use         preliminary findings in a very small
by performance of one half of the          high-intensity resistance training for          samplez6suggest that high-intensity
muscle group's 10 RM each exercise         older persons, due, in part, to the             isotonic resistance training can pro-
session. New isometric and isotonic        presence of multiple chronic medical            duce an increase in muscle force-
maximum resistance training loads          conditions in these individuals or to           generating capacity in very old indi-
were established weekly. Following         concerns regarding the ability of old           viduals without negative effects. In
6 weeks of isometric and isotonic          muscles to tolerate MVCs. Recently,             addition, the increase in muscle force-
resistance training, the mean percent-     the effects of high-intensity isotonic          generating capacity in these very old
age increases in the amounts of mus-       resistance training on muscle force-            persons may be correlated with an
cle force generated were 46% (iso-         generating capacity have been investi-          increase in functional performance.
metric) and 57% (i~otonic).~5              gated in 10 "frail" older persons               This hypothesis, however, needs to be
                                           (4 men, 6 women; 902 1 years of age)            confirmed in investigations of larger
In three studies,2>25 the differences in   who were institutionalized.26The                samples of older persons, using reli-
the force-generating response of aged      individuals were ambulatory, were               able and valid functional assessment
muscle to isometric resistance train-      not acutely ill or diagnosed with un-           tests.
ing were most likely due to differ-        stable cardiovascular disease or un-
ences in exercise training intensities.    controlled chronic conditions, and              Findings of Brown27suggest that there
In younger individuals, the largest        were able to follow simple com-                 is little damage to older muscle fol-
gains in force-generating capacity         mands. No additional definition of              lowing manual resistance training.
occur when high-resistance loads are       frailty was provided. The individuals           Female Sprague-Dawley rats, 21 to
applied to muscles.62 Similar findings     trained for 8 weeks, three times a              30 months of age (50% longevity of
are seen in older m u ~ c l e s .The , ~ ~ week, performing three sets of eight
                                  ~~                                                       females of this strain was 30 months),
largest gains in force-generating ca-      repetitions. The subjects trained at            performed three sets of 10 repetitions
pacity were found when older muscle        50% of their one RM during the first            of manually resisted chin-ups twice a
groups were resistance trained using       week of training and then at 80% of             day for 3 months.27 No indicators of
maximum loads and these loads were         their one RM during weeks 2 through             damage (eg, large numbers of macro-
adjusted on a weekly basis to main-        8 of training. Regional body composi-           phages, central nuclei, loss of stria-
tain that muscle overloading through-      tion, using computed tomography                 tions) in trained palmaris longus
out the training period. Specificity of    (CT) scans of the thigh, were ob-               muscles were found in any of the
training and testing principles were       tained prior to and within 1week of             aged            A definitive conclusion
also adhered to in these st~dies.2~9~5 the completion of training. Functional                         V
                                                                                           that an M C does not cause damage
In addition, it appears that both iso-     mobility was assessed using the chair-          to older muscle, however, cannot be
metric and isotonic resistance training    stand maneuver and gait observations            drawn from Brown's study.27 It was
are capable of increasing healthy aged     at the beginning and end of training.26         not conclusively shown that MVCs of
skeletal muscle force-generating ca-                                                       the palmaris longus muscles were
pacity to an equivalent degree if both     Following training, the amount of               being performed during the manually
types of training use heavy resistance.    maximum muscle force generated by               resisted chin-ups. The amount of
                                           the older subjects significantly in-            overload being applied to the pal-
In contrast, in Liemohm's23study, in       creased (174%k31%).26      The midthigh         maris longus muscle was also not
which no increase in old muscle            muscle area, based on CT scan mea-              q~antified.~7
force-generating capacity was found,       surements, increased 9.0%k 4.5%
isometric training at unspecified in-      following training.26Habitual (eg,
tensities was performed. Thus, it is       preferred) gait speed did not change
not known whether these muscles            significantly with training, but tandem
were significantly overloaded              (not defined) gait speed significantly
throughout the training period. In         increased (48%) following training.26

                                                                                Physical Therapy/Volume
                                  Downloaded from by guest on December 10, 2011   73, Number 6lJune 1993
Effects of Aged Muscle                       during the 8 weeks of resistance train-       that performed 5 months of treadmill
Resistance Training on                       ing was due mainly to neural factors,         exercise, 30 minutes a day, 5 days a
Motorneurons                                 as evidenced by findings of a greater         week, an increase in terminal sprout-
                                             increase in the electrical activity of the    ing of the soleus motoneurons was
Moritani and deVriesZH    have attributed    muscles without any increase in the           found as compared with 26-month-old
the increase in aged muscle force-           cross-sectional areas of the muscles          untrained rats.65 In the gastrocnemius
generating capacity following resis-         following training.2nNeural factors, as       muscle, there was no difference be-
tance training to changes in neural          defined by Moritani and deVries,28            tween the 26-month-old trained and
activity. Male subjects, 18 to 26 years      were either an increase in facilitation       untrained rats in the amount of mo-
of age and 67 to 72 years of age, per-       or disinhibition within the central                                              .~~
                                                                                           toneuron terminal s p r o ~ t i n gThis
formed 20 repetitions of elbow flex-         nervous system.                               finding does not necessarily mean
ion at 66% of the muscle's 10 RM.                                                          that aged slow-twitch motor units are
The exercises were performed twice a         It appears, based on Moritani and             more capable of initiating terminal
day, three times a week, for 8 weeks.        deVries' findings,zxthat older persons        sprouting in response to exercise
Every 2 weeks, the maximal isometric         increase their muscle force-generating        than aged fast-twitch motor units.
forces generated by the elbow flexors,       capacity following moderate-intensity         Rather, the results may be due to the
the electrical activity of the biceps        (66% of 10 RM) resistance training            exercise protocol used in this study."5
brachii muscles, and the cross-              because of activation of neuromotor           During endurance training, a predom-
sectional areas of the elbow flexor          patterns that enable the older individ-       inance of slow-twitch motor units are
muscles were measured.28                     ual to coordinate his or her muscles          recruited. Thus, the effects of chronic
                                             more effectively to exert a greater           resistance exercise on motor unit
Prior to training, there were no differ-     force (eg, motor learning). One might         terminal sprouting in older individu-
ences between the younger and older          also conclude from Moritani and               als needs to be investigated. Because
men in the maximal isometric forces          deVriesl findings28 that a muscle loses       axon withdrawal has been suggested
generated by the muscles, the electri-       its ability to hypertrophy in response        as a possible cause of fiber atrophy in
cal activity of the muscles, and the         to resistance training as it ages. The        older muscles,6 an increase in termi-
cross-sectional areas of the muscles.28      lack of hypertrophy in older muscles,         nal sprouting and end-plate growth in
Followirlg training, the maximal iso-        however, may be due to an underesti-          response to chronic exercise might
metric force generated by the trained        mation on the part of the investiga-          reduce the amount of fiber atrophy
elbow flexors of the younger and                     ~ ~
                                             t o r of the~amount of resistance             and fiber loss seen in older muscle.
older men increased 30% and 20%.28           needed to be applied to the older
In the younger men, the electrical           muscles to produce hypertrophy.               Effects of Resistance
activity of the muscles and the cross-       Moritani and deVries2B also used an-          Training on Aged Skeletal
sectional areas of the muscles both          thropometric methods (skinfold and            Muscle Morphology
increased approximately           In the     girth measurements) to estimate mus-
older men, the electrical activity of        cle mass. Anthropometric methods do           Following high-intensity resistance
the muscles and the cross-sectional          not provide an accurate assessment of         training, increases in maximum force-
areas of the muscles increased ap-           hypertrophpl; thus, Moritani and              generating capacity have been associ-
proximately 20% and 2%.28                                  '~~
                                             d e v r i e ~conclusions may be               ated with muscle hypertrophy in both
                                             inaccurate.                                   healthy elderly men29 and women.30
Moritani and deVries2H concluded that                                                      Twelve men, 60 to 72 years of age,
during the first 4 weeks of training,        Moritani and deVries' findings28 are          participated 3 days a week for
the increase in tension-generating           difficult to generalize to other mus-         12 weeks in high-intensity isokinetic
capacity in younger muscles was due          cles and individuals because these            resistance training.2Wuring each
to neural factors, as evidenced by an        investigators did not normalize the           training session, subjects performed
increase in the electrical activity of the   electrical activity of the muscles.           three sets of eight repetitions of knee
muscles with no change in the cross-         When measuring electrical activity of         flexion and extension (covering a
sectional areas of the muscles during        muscles during isometric contrac-             range of motion of 90")t 80% of the
this time. During the final 4 weeks of       tions, the variables affecting the signal     muscles' one RM. Prior to and follow-
training, the increased force-               (eg, time, force, body composition)           ing the 12 weeks of training, peak
generating capacity of the younger           must be normalized with respect to            torques of the extensor and flexor
muscles appeared to be due to hyper-         their maximal measurable values for           muscles were measured, and needle
trophy, as evidenced by an increase in       the particular experimental                   biopsies of the left vastus lateralis
the cross-sectional areas of the mus-        procedure.6"                                  muscles and CT scans of the thighs
cles with little change in the electrical                                                  were performed. Biopsy samples
activity of the muscles during this          Chronic exercise appears to increase          were stained for myofibrillar ATPase,
period. In contrast, the authors con-        terminal sprouting in aged motoneu-           and muscle fibers were classified as
cluded that the increase in force-           rons.65 In soleus muscles from 26-            either type I o r 11.29
generating capacity in older muscles         month-old female Fischer 344 rats

Physical Therapy /Volume 73, Number 6June 1993
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Following 12 weeks of training, knee         intensity resistance training at 80% to        age, twice a week for 15 weeks using
extensor and flexor muscle peak              85% of one RM for 20 weeks.66 The              a 10-station circuit-training program.
torques, as measured by the isokinetic       lower type I1 fiber hypertrophy in             At each station, 20 to 30 repetitions of
dynamometer, increased 10% and               older muscles as compared with                 exercise were performed using either
18% at 60°/s and 17% and 15% at              younger muscles following high-                body weight or light weights for resis-
240"/~.~9 torques of the knee                resistance training may be due to a            tance. Knee extensor muscle exercises
extensors and flexors, as measured by        difference in training regimens (mod-          were incorporated in every second
the one-RM test, increased 107% and          erate resistance training3O versus             station. No descriptions of the exer-
227%.29The area of the quadriceps            heavy resistance training,66 12-week           cises at each station o r a definition of
femoris muscle increased 9%.29 Cross-        training period30 versus 20-week train-        the term "light weight" were given.
sectional areas of type I and type I1        ing periocF6) o r an age-related con-          Maximum force produced by the leh
fibers increased 34% and 28%.29              straint on hypertrophy. To determine           knee extensor muscles was measured,
                                             whether there is an age-related con-           and needle biopsy samples were
In another study,30 13 women, 64 to          straint on hypertrophy during resis-           taken from the left vastus lateralis
86 years of age, participated in 12          tance training, both younger and               muscle before and after training.12
weeks of moderate- to high-intensity         older subjects need to perform the
isotonic resistance training of the          same training protocols. There also                Prior to training, the average amount
quadriceps femoris, hamstring, glu-          may be a gender difference in the                  of force produced at the different
teus medius, adductor magnus, ilio-          hypertrophy response of older muscle               isokinetic angular velocities was less
psoas, and gluteus maximus muscles.          to resistance training. Following resis-           in the 56- to 65-year-old age group
Subjects in the training group exer-         tance training, the areas of both type I           than in the 29- to 39-year-old age
cised at 65% of one R during the
                        M                    and type I1 fibers increased in the                group.l2 The proportion of type I
first 5 weeks, 70% for 4 weeks, and          vastus lateralis muscle biopsy sam-                fibers was 19% greater in muscle
75% for 3 additional weeks. Training         ples.29 In vastus lateralis muscle bi-             samples obtained from the older age
sessions were conducted 3 days a             opsy samples from the older women,                 group as compared with the younger
week, and three sets of six repetitions      however, only the area of type I1                  age group.12 In the older age group,
of each exercise were performed              fibers increased.30 These differences              the cross-sectional areas of type I and
during each training session. Six            need to be investigated further.                   I1 fibers were also 29% and 38% less
women, 64 to 86 years of age, served                                                            compared with the younger age
as control subjects and received no          The finding that hypertrophy of older              group.12 Following training, type I and
active intervention. Measurements of         muscles can occur following high-                  I1 fiber cross-sectional areas increased
maximum force-generating capacity            intensity resistance e x e r ~ i s e l ~ ~ ~ 9 ~ 3 ~
                                                                                                38% and 52% in the older individuals,
for each muscle and needle biopsies          appears to contradict the findings of              whereas the increases in the fibers'
were taken from the vastus lateralis         Moritani and deVries,2* who reported               cross-sectional areas were insignifi-
muscles at the initiation and conclu-        no significant muscle hypertrophy                  cant in the younger individuals.12The
sion of the study. Fibers were stained       following moderate-intensity resis-                proportions of fiber types and the
for myofibrillar ATPase to differentiate     tance training. Differences in mea-                force-generating capacity at the differ-
type I and I1 fibers.30                      surement techniques may explain the                ent angular velocities in the younger
                                             disparity in the findings. Moritani and            and older age groups were un-
Maximum force-generating capacity            deVries2Qsed anthropometric mea-                   changed following training.12Thus,
increased 28% to 115% in all muscle          surements to estimate muscle mass, a               the magnitude of the increases in
groups following training.3O Type I1         relatively crude measure. More recent              force-generating capacity and fiber
cross-sectional fiber area in the vastus                       ~ 2 9 more
                                             s t ~ d i e s ~ ~ used ~ 3 ~ sensitive             cross-sectional area following heavy
lateralis muscle biopsy samples in-          methods (histochemical tech-                       resistance training appears to be de-
creased 20% following resistance             niquesI12,29,3O scans2') to examine
                                                               CT                               pendent on the amount of overload
training.3O No significant increases in      whether muscle hypertrophy oc-                     applied to older muscles.
the maximum force-generating capac-          curred in older subjects.
ity and type I1 cross-sectional area in                                                         In addition, only high-intensity resis-
control subjects and in type I cross-        The magnitude of the increases in                  tance training, not high-intensity car-
sectional area in either group were          force-generating capacity and fiber                diovascular endurance training, causes
f0und.3~                                     cross-sectional area appears to be                 hypertrophy and an increase in mus-
                                             dependent on the intensity of resis-               cle force-generating capacity in older
The 20% increase in the type I1 fiber        tance training. Low-resistance training            muscles.59 Maximal isometric force
cross-sectional area in healthy older        appears to result in little improve-               production, muscle mass, fiber cross-
women3O is less than the 45% in-             ment of aged muscle's maximum                      sectional area, and contractile protein
crease in type I1 fiber cross-sectional      force-generating capacity but may                  content of the vastus lateralis and
area observed in healthy younger             reverse, in part, aged muscle's atro-              biceps brachii muscles were investi-
women who performed 6 to 8 repeti-           phy.12 Aerobic exercise was per-                   gated in younger sedenta~y    men
tions per muscle group of high-              formed by 18 men, 20 to 65 years of                (28k0.1 years of age) and older sed-

                                                                                 Physical Therapy /Volume
                                   Downloaded from by guest on December 10, 2011   73, Number 64une 1993
entaty men (68k0.5 years of age) and         ages of 20 and 30 year^.^' An in-             lack of change in the proportions of
in older male swimmers (69k 1.9              creased rate of 3-methylhistidine ex-         fibers in older human m u s ~ l e s ~ ~ ~ 2 9 ~ ~ ~
years of age), runners (70k0.7 years         cretion in the urine, an index of actin       may be due to the fact that the train-
of age), and resistance-trained subjects     and myosin catabolism, was found              ing durations used (12 weeks and
(68k0.8 years of age).59                     following 12 days of resistance train-        less) were not long enough to induce
                                             ing at 60% to 70% of one-RM values            a change.
For the 12 to 17 years previous to the       of upper- and lower-extremity mus-
study, the trained older men partici-        cles in these individuals.67 Contractile      Effects of Resistance Training
pated three times a week in swim-            protein catabolism and anabolism in           on Aged Muscle Metabolism
ming (800-1,000 m each session);             older skeletal muscle following high-
running (9-12 krn); or three sets of         intensity resistance training needs to        The effect of resistance training on
10 repetitions of weight lifting using       be investigated.                              anaerobic and aerobic metabolism in
the legs, torso, shoulders, and arms.                                                      24- and 29-month-old male Wistar rats
Knee extension and elbow flexion             Although the area of fibers increased,        following 20 and 36 weeks of resis-
maximal isometric force values in            the percentages of fiber types in older       tance training was investigated by
older sedentary men were 44% and             human muscle did not change follow-           Klitgaard et al.@The activity level of
32% less than the values for younger         ing resistance training.12.29*30
                                                                            Changes        CS (an aerobic enzyme) in the soleus
sedentary men.59 The cross-sectional         in the percentages of fiber types,            and plantaris muscles of 24- and 29-
areas of the vastus lateralis and biceps     however, have been found in the               month-old resistance-trained rats was
brachii rnuscles of the older sedentary      muscles of both older rats68 and              lower than in the muscles of 24- and
men were 24% and 20% less com-               younger humans66 following resis-             29-month-old untrained rats.6Vn the
pared with those of the younger sed-         tance training. Klitgaard et a1a com-         soleus muscles of 24- and 29-month-
entary nlen.59 Mean fiber areas in           pared the effects of 36 weeks of resis-       old untrained and resistance-trained
both the vastus lateralis and biceps         tance training on soleus and plantaris        rats, there were no differences in the
brachii muscles were 24% less in the         muscle morphology in 29-month-old             activity levels of the anaerobic en-
older sedentary men compared with            male Wistar rats. Following 36 weeks          zymes TPDH and LDH.68The TPDH
the younger sedentary men.59                 of resistance training, type I and type       and LDH activity levels were higher,
                                             IIa fiber cross-sectional areas were          however, in the plantaris muscles of
Higher myosin heavy chain and myo-           larger in both soleus and plantaris           the 24- and 29-month-old resistance-
sin light chain type I contents were         muscles that were exercised as com-           trained rats as compared with the 24-
also found in the vastus lateralis and       pared with untrained control mus-             and 29-month-old untrained rats.@Rat
biceps brachii muscles of the older          cles.68 The proportion of type I fibers       plantaris muscle has a greater propor-
sedentary men as compared with the           decreased in soleus muscles from              tion of fast fibers than does rat soleus
younger sedentary rnen.59 The mus-           36-week resistance-trained rats as            rnusc1e.a Because of its fiber compo-
cles of older resistance-trained men         compared with untrained control               sition, the aged plantaris muscle may
had maximal isometric forces, muscle         rats." In the deep part of plantaris          have been activated to a greater ex-
mass, fiber cross-sectional areas, and       muscles from 36-week resistance-              tent than the aged soleus muscle
myosin heavy and light chain contents        trained rats, type IIb fiber proportions      during resistance training. This pro-
that were nearly identical to those of       increased and type I fiber proportions        posed difference in aged muscle acti-
younger sedentary men.59 In contrast,        decreased as compared with un-                vation during resistance training may
the isometric force values, muscle           trained control rats.68 Previously,           have contributed to the differences
mass, fiber cross-sectional areas, and       Klitgaard et a169 reported no age-            between aged muscles in the anaero-
myosin heavy and light chain contents        related decline in twitch and tetanic         bic enzyrne activity level following
of muscles from older runners and            tension generation in the soleus and          resistance training.68In this same
swimmers were similar to those of            plantaris muscles of 29-month-old rats                            C
                                                                                                     ATP and P concentrations
the older sedentary men.59                   that were resistance trained for              were 24% and 17% higher in the
                                             36 weeks. A decrease in proportion of         lateral gastrocnemius muscles of 29-
The hypertrophy of older muscles in          type IIb fibers and an increase in the        month-old rats following 36 weeks of
response to high-intensity resistance        proportion of type IIa fibers were            resistance training as compared with
training may be due to an increase in        found in vastus lateralis muscles from        the ATP and PC contents of the rnus-
muscle protein turnover. During              younger women who were resistance             cles of age-matched control rats.
heavy resistance strength training of                                         M
                                             trained at 80% to 85% of one R for
older muscle, there may be an in-            20 weeks.66                                   The finding that resistance training
crease in muscle fiber breakdown,                                                          increases the capacity of aged rat
with a concomitant increase in con-          When changes in fiber type percent-           muscle to generate ATP anaerobi-
tractile protein anabolism between           ages were found in muscles of both            cally68 is similar to findings in
the exercise sessions. Increased mus-        older r a t ~ 6 ~ younger women,@
                                                           and                             younger human muscles.70Increases
cle protein turnover has been demon-         the length of training was of long            in the resting concentrations of ATP,
strated in male subjects between the         duration (20 weeks o r greater). The          PC, and glycogen in mixed fiber bi-

Physical Therapy /Volume 73, Number 6lJune 1993
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opsy samples of triceps brachii mus-        Valsalva maneuvers during the exer-            applied to the muscle, number of
cle from younger men have been              cise period, as this maneuver may              repetitions performed, and frequency
reportcd following high-intensity           place strain on the individual's cardio-       of training. In many reports, the pro-
resistance training.'O Younger men          vascular system.                               tocols are poorly described, making it
who have undergone high-intensity                                                          difficult to apply the methodology in
resistance training also have higher        Future Research                                clinical practice. Thus, more system-
levels of muscle and blood lactate and                                                     atic comparisons, utilizing a variety of
a greater depletion of muscle glyco-        Although it has been demonstrated              different exercise approaches, are
gen during a session of resistance          that resistance training increases the         needed.
exercise as compared with untrained         force-generating capacity of older
men.'O Currently, one can only hy-          muscles, additional investigations             Although high-intensity training in-
pothesize that the anaerobic capacity       regarding the effects of resistance            creases force-generating capacity, little
of older human muscle following             training on aged muscles are war-              is known about its effects on func-
high-intensity resistance training will     ranted. The effects of resistance train-       tional performance. Unless investiga-
be increased.                               ing on older muscle need to be inves-          tions are conducted in which different
                                            tigated in larger samples of human             measures of functional performance
Recommendations for a                       subjects and in human muscles other            are made prior to and following resis-
Therapeutic Approach for                    than the gastrocnemius and the bi-             tance training, the validity of this
Improving Force Generation                  ceps brachii. The sample sizes of the          approach to improving the quality of
In Older Muscle                             human studies performed to date                life of older persons cannot be estab-
                                            have been small. It is unclear whether         lished. In order to establish effective
The following recommendations are           the results obtained for the gastrocne-        resistance training programs that
based on what is known to date about        mius and biceps brachii muscles can            optimally improve the physical capac-
the effects of resistance training on       be generalized to other muscles,               ity of older persons, the effect of
older muscle. To illicit the greatest       which might have ddferent structures           resistance training on the neuromus-
increase in force in older muscles,         and functions. Larger numbers of               cular system and other physiological
high-intensity resistance training is       persons 70 years of age and older              systems must continue to be
neces~ary.~~~29 The isotonic resistance     need to be studied. Longitudinal pop-          investigated.
protocol that produced the greatest         ulation studies, in addition to cross-
increases in force-generating capacity      sectional population studies, are also
and attenuated atrophy to the greatest      needed. In addition, investigations of
extent in older human muscle was            how factors such as gender, race,              High-intensity resistance training ap-
three sets of eight repetitions of exer-    culture, and nutrition influence the           pears to be the most effective proto-
cise performed at an intensity of 80%       age-related muscle alterations and the         col to date in counteracting the
of a muscle's one RM, 3 days a week         responses of aged muscles to resis-            changes in skeletal muscle morphol-
for 12 weeks.29 Isotonic resistance         tance training are needed. Studies             ogy and performance seen in many
training of older muscle can be initi-      have only investigated the effects of          older persons. Systematic investiga-
ated at an intensity of 50% to 60% of       age on muscle morphology and me-               tions, however, of the effects of age
the muscle's one RM for 1 week and          tabolism in biopsy samples obtained            on the neuromuscular system and of
then increased to 80% of the muscle's       from older persons of Caucasian                the effects of resistance training on
one RM for the remainder of the             descent,                        the neuromuscular system and the
training period.*6 Throughout the                                                          functional capacity of older persons
isotonic training period, maximum           Recently, it has been reported that            are essential for the development of
training loads need to be reestab-          fiber type proportion and muscle               cost-effective interventions that im-
lished on a regular basis. A 6-second       metabolism are also influenced by              prove the physical capacity of older
maximum isometric contraction re-           race.71Whether the findings from               persons.
peated five times a training session,       older persons of Caucasian descent
three times a week, can increase a          can be applied to older women o r
muscle's force-generating capacity and      older persons of other races and               References
mass following joint immobilization.62      cultures is not yet known. In younger          1 h t r a n d P-0. "Why exercise?" Med Sci SpvrIs
This isometric resistance training          adults, dietary carbohydrate intake            Exerc. 1992;24:153-162.
protocol may also produce similar           influences the rate and amount of              2 Gutmann E. Hanzlikova V. Motor unit in old
effects in older muscles. During high-      glycogen repletion following a session         age. Nature. 1966;209:921-922.
intensity resistance training, older        of maximal exerci~e.'~  What effect            3 Pestronk A, Drachman DB, Griffin JW. Effects
                                                                                           of aging o n nerve sprouting and regeneration.
persons should be continuously mon-         nutrition in combination with exer-            Exp Neurol 1980;70:65-82.
itored for heart rate, blood pressure,      cise has on older muscle performance           4 Gutmann E, Hanzlikova V. Fast and slow
and any signs o r symptoms of dis-          needs to be examined. Resistance               motor units in ageing. Gerontology. 1976;22:
tress. Older individuals should also        protocols havc diffcred with respect
be cautioned to avoid performing            to types of contraction studied, loads

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                               Effects of Age and Resistance Training on Skeletal
                               Muscle: A Review
                               Jane F Hopp
                               PHYS THER. 1993; 73:361-373.

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