Possibility of leg muscle hypertrophy by ambulation in older adults: A brief review

Abstract

It is known that ambulatory exercises such as brisk walking and jogging are potent stimuli for improving aerobic capacity, but it is less understood whether ambulatory exercise can increase leg muscle size and function. The purpose of this brief review is to discuss whether or not ambulatory exercise elicits leg muscle hypertrophy in older adults. Daily ambulatory activity with moderate (>3 metabolic equivalents [METs], which is defined as the ratio of the work metabolic rate to the resting metabolic rate) intensity estimated by accelerometer is positively correlated with lower body muscle size and function in older adults. Although there is conflicting data on the effects of short-term training, it is possible that relatively long periods of walking, jogging, or intermittent running for over half a year can increase leg muscle size among older adults. In addition, slow-walk training with a combination of leg muscle blood flow restriction elicits muscle hypertrophy only in the blood flow restricted leg muscles. Competitive marathon running and regular high intensity distance running in young and middle-aged adults may not produce leg muscle hypertrophy due to insufficient recovery from the damaging running bout, although there have been no studies that have investigated the effects of running on leg muscle morphology in older subjects. It is clear that skeletal muscle hypertrophy can occur independently of exercise mode and load.

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Clinical Interventions in Aging 2013:8 369–375
Clinical Interventions in Aging
Possibility of leg muscle hypertrophy
by ambulation in older adults: a brief review
Hayao Ozaki1
Jeremy P Loenneke2
Robert S Thiebaud2
Joel M Stager3
Takashi Abe3
1Juntendo University, Inzai, Chiba,
Japan; 2Department of Health
and Exercise Science, University
of Oklahoma, Norman, OK, USA;
3Department of Kinesiology, Indiana
University, Bloomington, IN, USA
Correspondence: Takashi Abe
Depar tment of Kinesiolog y, Indiana
University, 1025 East 7th Street ,
Room 104, Bloomington, IN 47405, U SA
Tel +1 812 856 7163
Fax +1 812 855 3193
Email t12abe@gmail.com
Abstract: It is known that ambulatory exercises such as brisk walking and jogging are potent
stimuli for improving aerobic capacity, but it is less understood whether ambulatory exercise can
increase leg muscle size and function. The purpose of this brief review is to discuss whether or
not ambulatory exercise elicits leg muscle hypertrophy in older adults. Daily ambulatory activ-
ity with moderate (.3 metabolic equivalents [METs], which is defined as the ratio of the work
metabolic rate to the resting metabolic rate) intensity estimated by accelerometer is positively
correlated with lower body muscle size and function in older adults. Although there is conflicting
data on the effects of short-term training, it is possible that relatively long periods of walking,
jogging, or intermittent running for over half a year can increase leg muscle size among older
adults. In addition, slow-walk training with a combination of leg muscle blood flow restriction
elicits muscle hypertrophy only in the blood flow restricted leg muscles. Competitive marathon
running and regular high intensity distance running in young and middle-aged adults may not
produce leg muscle hypertrophy due to insufficient recovery from the damaging running bout,
although there have been no studies that have investigated the effects of running on leg muscle
morphology in older subjects. It is clear that skeletal muscle hypertrophy can occur indepen-
dently of exercise mode and load.
Keywords: aerobic exercise, muscle mass, aging, strength, sarcopenia
Introduction
Brisk walking and jogging are recommended for improving maximal oxygen uptake
(VO 2 max) in older men and women.1–3 Elite race walkers have high VO2 max values,4,5
which are similar to elite long distance and marathon runners.4 Although endurance
exercise is generally not prescribed for increasing muscle mass, some cross-sectional
studies have observed greater muscle fiber cross-sectional areas (CSA) in the leg
muscles of distance runners than that of untrained subjects.6,7 Although the previous
studies observed change in muscle fiber size resulting from running, the whole muscle
volume or CSA has not been investigated. Thus, it is unclear whether the greater muscle
fiber CSA in distance runners is due to running or if it is influenced by genetic factors.8
In addition, with cross-sectional studies it is difficult to separate the possibility that
the athletes, in many cases, also performed resistance exercise. Therefore, the effects
of endurance exercise on muscle hypertrophy and strength gain are not well known.
In general, a training intensity of more than 60% of one’s concentric one repeti-
tion maximum (1RM) is commonly considered the minimum intensity required to
achieve muscle hypertrophy.9 In recent years, however, it has been established that
myofibrillar protein synthesis is maximally stimulated following acute work matched
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Clinical Interventions in Aging 2013:8
resistance exercise at 60% of 1RM, and that increasing the
external load provided no additional stimulation in the syn-
thesis rate.10 Nevertheless, when resistance exercise is not
matched for work and is taken to volitional fatigue, even
lower exercise intensities appear capable of maximizing the
synthetic response. To illustrate, low intensity knee extension
exercise at 30% of 1RM has been demonstrated to increase
myofibrillar protein synthesis at rates that are similar to
those observed with higher intensity resistance exercise
(90% 1RM). However, the lower intensity group to failure
resulted in a more sustained synthetic response.11 Recently,
these findings have been extended to demonstrate that when
low intensity (30% of 1RM) resistance exercise to failure is
performed repeatedly, comparable increases in muscle hyper-
trophy (whole muscle and fiber level) are observed between
low and high intensities.12,13 Additionally, very low intensity
exercise training such as walking (approximately 10% of
maximum voluntary contraction) combined with blood flow
restriction (BFR) to the exercising muscles can elicit muscle
hypertrophy and strength gain in young and older adults.14,15
These increases in muscle size and strength have also been
previously observed with aerobic exercise in older women
without BFR, although the intensity used was approximately
60%–80% of the heart rate reserve.16 These results suggest
that high external loads are not a prerequisite for increasing
muscle protein synthesis, and ultimately muscle hypertrophy.
The exercise intensity to lower limb muscles during brisk
walking and jogging is approximately ∼30% of maximum
voluntary contraction.17,18 Thus, it is possible that ambula-
tion exercise with a sufficient workload may induce muscle
hypertrophy and strength gain. Therefore, the purpose of
this brief review is to discuss whether or not brisk walking
and jogging/running elicits muscle hypertrophy and strength
gain in older adults.
Daily physical activity and leg
muscle size and function
During the last decade, only a few studies have reported
the relationship between accelerometer (or pedometer)
determined physical activity and skeletal muscle size
in middle-aged and older populations. For example,
Bassey et al19 found that triceps surae muscle strength was
significantly and positively correlated (r = 0.30, P , 0.05)
with recorded amounts of daily walking when averaged
over 7 consecutive days in men aged . 65 years. Scott
et al20 reported that ambulatory activity averaged over 7
consecutive days is positively associated with both leg
strength and muscle quality in women aged 50–79 years.
The associations between ambulatory activity and both leg
strength and muscle quality were nonsignificant in men.20 In
addition, the authors reported that there was no significant
association between ambulatory activity and dual energy
X-ray absorptiometry (DXA) estimated leg lean tissue mass.
On the other hand, Park et al21 reported a significant posi-
tive correlation between DXA estimated appendicular lean
tissue mass and year averaged duration of physical activity
at .3 metabolic equivalents (METs) in women (r = 0.38,
P , 0.05) and men (r = 0.28, P , 0.05) aged 65–84 years.21
Since DXA assesses the sum of lean tissue mass, which
includes the anterior and posterior upper leg and lower
leg, site specific muscle mass cannot be determined by this
method. Recently, Abe et al22 reported that accelerometer
determined ambulatory activity, especially moderate and
vigorous intensities (.3 METs), is positively correlated
with the tibialis anterior (r = 0.34, P , 0.05), as well as
by the triceps surae muscle thickness (r = 0.41, P , 0.01),
suggesting that .3 METs of physical activity may prevent
age related loss of muscle mass in the lower leg muscles. In
addition, isometric knee flexion strength is positively cor-
related with the duration of moderate physical activity. The
results from the previous studies suggest that ambulatory
activity with moderate or vigorous intensities can improve
lower leg muscle size and function in older adults.
Short-term training studies
Walk training
A number of studies have reported the effect of walk training
on aerobic capacity and body composition;23 however, only a
few studies have observed the influence of walk training on
lower body muscle size and strength. In active young men,
a short duration (3 weeks) of regular slow-walk training did
not change dynamic leg press strength, isometric knee exten-
sion strength, or magnetic resonance imaging measured thigh
muscle CSA.14 In older women aged 76–78 years, there was
no significant change in computed tomography measured
thigh muscle CSA following 18 weeks of walk training.24
Similarly, active older men and women did not increase mag-
netic resonance imaging measured mid-thigh muscle CSA and
quadriceps muscle volume after 10 weeks of walk training.15
On the other hand, one study reported increases in ultrasound
measured muscle thickness following 6 months of walk train-
ing in sedentary or mildly to moderate active older adults.25
They found that muscle thickness increased significantly for
knee flexors and dorsi flexors, but not for the knee extensors
or plantar flexors. It is clear that the change in muscle size by
walk training may be influenced by initial physical activity
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Clinical Interventions in Aging 2013:8
levels and/or programs (intensity, duration, and frequency).
In the previous study reported by Kubo et al,25 the numbers of
steps increased by 44% from 7025 steps/day to 9915 steps/day
(average walking duration was 45 minutes/day, and frequency
was 5.4 days/week) although the authors did not report the
intensity. These results suggest a possibility that site specific
locomotor muscles, which are unable to be differentiated
from whole muscle thigh or lower leg measurements, increase
following walk training when the volume of walking is sig-
nificantly increased from baseline.
With regard to muscle strength, several studies have
observed increases in strength following walk training in
older adults. A study reported that moderate intensity (about
50% of VO2 max) continuous (8000 steps or more per day)
walking increased isometric knee extension (7%) strength
in older men and women.26 Furthermore, high intensity
interval walking (.5 sets of 3 minutes walking at approxi-
mately 40% of VO2 max followed by 3 minutes of walking
at .70% VO2 max) produced improvements in isometric
knee extension (13%) and flexion (16%) strength.26 On the
other hand, following walk training at 45% of the heart rate
reserve in older men and women, there was no change in
ether isometric knee extension or flexion strength.15 Thus,
it appears that the magnitude of improvement of the muscle
strength may be associated with exercise intensity during
walking. Participants with a low initial fitness level have a
greater potential for improving muscle strength and muscle
hypertrophy following brisk walk training.
To illustrate this, a study reported that maximum
isokinetic knee extension and flexion strength increased
by 10% following 3 months of home based walk training
(30–45 minutes, 3–4 sessions per week) in patients with
chronic heart failure.27 Similarly, patients with peripheral
arterial disease performed supervised treadmill walking
training (3 sessions per week, 12 weeks) and a significant
increase in isokinetic plantar flexion strength is observed.28
Running training
Several studies have investigated the effect of chronic run-
ning on muscle fiber size, fat free mass, and muscle strength
in young and middle-aged subjects. For instance, Dolezal
and Potteiger29 have shown that 20–45 minutes of running at
65%–85% of the maximum heart rate for 10 weeks did not
increase 1RM strength for squat or fat free mass in young
men. Additionally, Glowacki et al30 reported that 12 weeks
of running significantly increased 1RM strength for leg press
and isokinetic knee extension, but it did not change fat free
mass. Additionally, in other studies, fat free mass also did
not change with running.31,32 Thus, it appears that chronic
running does not induce an increase in fat free mass for
young subjects, although lower limb strength may improve
in some cases. Meanwhile, Trappe et al33 have investigated
the effects of 16 weeks of marathon training (∼60 km per
week) on muscle fiber size for three leg muscles in young
subjects (four men and three women). The authors reported
that type 1 and type 2A fiber size in the gastrocnemius muscle
was significantly reduced by approximately 20% following
training.33 Furthermore, the type 1 and type 2A fiber size
for the soleus muscle and type 2A fiber size for the vastus
lateralis (VL) muscle did not change after the marathon
training. The type 1 fibers of the VL were the only fibers
that significantly increased in size from marathon training.
The authors stated that muscle fiber size in the soleus did
not increase by marathon training because the “untrained”
soleus has simply adapted to normal daily activity and is in a
more conditioned state compared with the VL.34 In contrast,
other studies have observed that muscle fiber CSA in the
VL did not change significantly after chronic running.32,35–37
Thus, it is generally observed that chronic running does
not induce leg muscle hypertrophy, especially in the thigh
muscle, in young and middle-aged adults. However, there are
no investigations about the effects of running on leg muscle
morphology in older subjects. Interestingly, a previous study
reported that a single bout of aerobic exercise enhanced
the anabolic response to insulin (sensitivity of feeding) by
stimulating mixed muscle protein synthesis and producing
a positive protein balance in older adults.38 Therefore, it is
still a possibility that training induced muscle hypertrophy
from running occurs in older men and women with insulin
resistance. It should be stated, however, that although mixed
muscle protein synthesis often serves as a surrogate marker
for myofibrillar protein synthesis, differential responses have
been observed within each subfraction.11 Therefore, it may
be appropriate to measure the individual synthesis rates of
myofibrillar, mitochondrial, and sarcoplasmic proteins to
better to clarify these issues.
Differences between the effects of run training and walk
training on muscle morphology are unclear, but several pos-
sibilities exist. Hikida et al39 investigated the ultrastructural
changes in the gastrocnemius muscles before and imme-
diately after a marathon event, and found marathon race
induced muscle necrosis and also regular distance training
induced muscle necrosis. The authors suggest that the ini-
tial trauma is probably the disruption of the sarcolemma,
which results in an ionic imbalance, especially of calcium.40
The increase in calcium concentration activates a protease
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Clinical Interventions in Aging 2013:8
and breaks down the Z-lines and thin filaments.41 A recent
study showed that calcium concentrations in the VL muscles
increased immediately after a 10 km and a 20 km run, and
the calcium accumulation was positively related to running
distance and time spent running.42 Interestingly, the authors
also found that the calcium response to a 10 km run did
not significantly alter following 10 weeks of run training
(distance of ∼29 km per week, three times/week). It could
be speculated, therefore, that repeated distance running,
but not walking, caused some damage that would make it
harder to recover from the damaging exercise bout.43 This
insufficient recovery may ultimately affect the capability of
the muscle to grow.
Although it appears that chronic continuous running
does not increase fat free mass and muscle f iber size,
Krustrup et al36 have investigated the effect of 1 hour of
running versus recreational soccer training at the same
exercise time and intensity on muscle fiber size in untrained
men aged 20–43 years, and reported that only soccer training
(1 hour per day and 2.3 days per week) significantly increased
muscle fiber CSA in VL (15%), fat free mass (3%), and
maximal isometric knee extension strength (11%). For
untrained women aged 19–42 years, similar soccer training
(1 hour per day for 1.8 days per week) demonstrated signifi-
cantly increased lean mass of the leg (11%), and they tended
to exhibit increased muscle fiber CSA in VL (P = 0.09).37
These data suggest that soccer training (intermittent jogging/
running) at various intensities and motions (including lateral
movements) has the potential to promote muscle hypertrophy
and strength gain. The mechanism of muscle hypertrophy is
unclear, although it may be possible that the higher eleva-
tion in blood lactate during soccer exercise compared to
continuous running indirectly affect increases in muscle
fiber size induced by recreational soccer training.36 Recently,
Inaba et al44 reported the biomechanical factors contributing
to quickness in lateral movements and found that extension
torques of the hip, knee, and ankle joints contribute sub-
stantially to the changes in side step distances. The lateral
movement and quickness during soccer exercise may be a
crucial factor for muscle hypertrophy in the leg muscles,
especially in the quadriceps muscle. However, further stud-
ies are needed to elucidate whether intermittent running can
induce hypertrophy at the whole muscle level.
Relatively long-term training studies
Most intervention studies on running have been relatively
short-term (less than or equal to 10 weeks), but some studies
have performed walking and jogging for over half a year.
Schwartz et al45 have shown that walking and jogging, 5 days
per week for 27 weeks, did not change thigh muscle CSA in
young men, but significantly increased thigh muscle CSA (9%)
for older men. As previously mentioned, 4 months of running
reduced type 1 and type 2A fiber size (20%) of the gastrocne-
mius muscle for young men and women,31 but Coggan et al46
have demonstrated that walking and jogging, 4 days per week
for 9–12 months, significantly increased (6%–18%) type 1 and
type 2A fiber size of the gastrocnemius muscle in older men
and women. Thus, walking or jogging/running from several
weeks to 2–3 months rarely induces muscle hypertrophy, but it
is possible that relatively long periods of training for over half
a year can increase leg muscle size by approximately 1% per
month for older adults. Further studies are required to make
a final decision because only a few studies have reported that
walking and/or jogging increased muscle size.
Inuence of specic environment
Hypobaric hypoxia
The specific internal environment in the legs during
walking and jogging/running can also influence the muscle
hypertrophy and strength response. For instance, high altitude
mediated hypobaric hypoxia creates many morphological and
physiological changes. A study reported that thigh muscle
CSA decreased by 10% after sojourn at a high altitude
(Himalayas; greater than 5000 m for over 56 days), although
whether a change in physical activity occurred is not clear.
In that study, the loss of thigh muscle size is mainly due to a
decrease in myofibrillar proteins.47 Mizuno et al48 also reported
that muscle fiber size decreased by an average of 15% in the
VL and biceps brachii muscles in both active and less active
men after 75 days of altitude (greater than 5250 m) exposure.
Other studies investigated the effects of acute and chronic
hypobaric hypoxia and physical exercise on muscle protein
metabolism, and the results suggest that the large increase in
protein degradation is the underlying mechanism for the loss
of skeletal muscle mass.49,50 Contrary to chronic hypobaric
hypoxia, a recent study investigated the effects of intermittent
systemic hypoxia on high intensity (70% 1RM) resistance
training induced muscle hypertrophy in young men.51 The
researchers found that muscle hypertrophic responses are
greater in resistance exercise under hypoxia than those of
a normoxia condition. However, Friedmann et al52 reported
that resistance training with low intensity (30% 1RM) under
hypoxia did not promote muscle hypertrophy. These findings
suggest that exercise training under intermittent hypoxia can-
not lead to muscle hypertrophy with low workloads such as
walking and jogging.
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Clinical Interventions in Aging 2013:8
Blood ow restriction
As stated previously, the potential for walk training induced
muscle hypertrophy is weak and may be specific to active
locomotor muscles. Interestingly, when combined with BFR
to the exercising muscles, walk training induced muscle
hypertrophy in the lower limb muscles has been observed
in both young and older adults. An earlier study has shown
that twice daily walk training with BFR at 50 m/minute for
10 minutes of actual walking, 6 days per week for 3 weeks,
increased quadriceps muscle volume (4%) and isometric
knee extension strength (10%) in young men.14 Additionally,
Park et al53 reported an increase in muscle strength following
2 weeks of twice daily BFR walk training in young athletes.53
In older adults, 10 weeks of BFR walk training can lead
to significant improvements in thigh muscle CSA/volume
and knee joint strength.15 Recently, a study has reported
that muscle volume of the thigh and lower leg increased by
4% and 3%, respectively, in the BFR walk group following
training;54 however, gluteus maximus muscle volume and the
lumbar L4–L5 muscle CSA did not change in the BFR walk
group, although there was a trend (P = 0.07) for an increase
in iliopsoas muscle volume. Therefore, the combination of
leg muscle BFR with slow-walk training elicits muscle hyper-
trophy only in the blood flow restricted leg muscles, which
might be due to an accumulation of metabolites within the
muscle fiber and subsequent muscle cell swelling induced
from the application of BFR.55,56
Conclusion
It is an undeniable fact that brisk walking and jogging
are potent stimuli for improving maximal oxygen uptake
(VO 2 max) in older men and women. This improvement
in cardiorespiratory fitness may also be associated with
increases in muscle size and strength depending on the
intensity, duration, and environment in which walking and
jogging/ running are performed. Table 1 shows a summary
of the effects of ambulation on muscle size and strength
in older adults. Daily ambulatory activity with moderate
(.3 METs) intensity, estimated by accelerometer, is
positively correlated with lower body muscle size and
function in older adults. Although the effects of short-term
training are uncertain, it is possible that relatively long
periods of walking, jogging, and/or intermittent running
training for over half a year can increase leg muscle size in
older adults. In addition, slow-walk training in a combina-
tion with leg muscle BFR elicits muscle hypertrophy only
in the blood flow restricted leg muscles. Competitive mara-
thon running and regular high intensity distance running in
young and middle-aged adults may not produce leg muscle
hypertrophy due to insufficient recovery from the damag-
ing running bout, although there is no study investigating
the effects of running on leg muscle morphology in older
subjects. It is clear that skeletal muscle hypertrophy can
occur independently of exercise mode and its load.
Disclosure
The authors report no conflicts of interest in this work. None
of the authors had financial or personal conflict of interests
with regard to this study.
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Leg muscle hypertrophy in older adults