Physical activity and bone: The importance of the various mechanical stimuli for bone mineral density. A review

Abstract

Numerous studies have reported benefits of regular physical activity on bone mineral density (BMD). The effects of physical activity on BMD are primarily linked to the mechanisms of mechanical loading, but the understanding of the precise mechanism behind the association is incomplete. The aim of this paper was to review the main findings concerning sources and types of mechanical stimuli in relation to BMD. Mechanical forces that act on bone are generated from impact with the ground (ground-reaction forces) and from skeletal muscle contractions (muscle forces or muscle-joint forces), but the relative importance of these two sources has not been elucidated. Both muscle-joint forces and gravitational forces seem to be able to induce bone adaptation independently, and there may be differences in the importance of loading sources at different skeletal sites. The nature of the stimuli is affected by the type, intensity, frequency, and duration of the activity. The activity should be dynamic, not static, and the magnitude and rate of the stimuli should be high. In accordance with this, cross-sectional studies report highest BMD in athletes of high-impact activities such as dancing, soccer, volleyball, basketball, squash, speed skating, gymnastics, hockey, and step-aerobics. Endurance activities such as orienteering, skiing, and triathlon seem to be beneficial to a lesser degree, whereas low-impact activities such as swimming and cycling are associated with lower BMD than controls. Both the intensity and frequency of the activity should be varied and increased beyond the habitual level. Duration of the activity seems to be less important, and a few loading cycles seem to be sufficient.

Full text

Norsk Epidemiologi 2011; 20 (2): 173-178 173
Physical activity and bone: The importance of the various
mechanical stimuli for bone mineral density. A review
Bente Morseth1, Nina Emaus2 and Lone Jørgensen1,2,3
1) Department of Community Medicine, University of Tromsø, Tromsø, Norway
2) Department of Health and Care Sciences, University of Tromsø, Tromsø, Norway
3) Department of Clinical Therapeutic Services, University Hospital North Norway, Tromsø, Norway
Correspondence: Bente Morseth, Department of Community Medicine, Faculty of Medicine, University of Tromsø, NO-9037 Tromsø, Norway
E-mail: bente.morseth@uit.no Telephone +47 77 64 48 16, direct line +47 77 62 31 24 Telefax +47 77 64 48 31
ABSTRACT
Numerous studies have reported benefits of regular physical activity on bone mineral density (BMD). The
effects of physical activity on BMD are primarily linked to the mechanisms of mechanical loading, but the
understanding of the precise mechanism behind the association is incomplete. The aim of this paper was to
review the main findings concerning sources and types of mechanical stimuli in relation to BMD. Mechanical
forces that act on bone are generated from impact with the ground (ground-reaction forces) and from skeletal
muscle contractions (muscle forces or muscle-joint forces), but the relative importance of these two sources
has not been elucidated. Both muscle-joint forces and gravitational forces seem to be able to induce bone ad-
aptation independently, and there may be differences in the importance of loading sources at different skeletal
sites. The nature of the stimuli is affected by the type, intensity, frequency, and duration of the activity. The
activity should be dynamic, not static, and the magnitude and rate of the stimuli should be high. In accordance
with this, cross-sectional studies report highest BMD in athletes of high-impact activities such as dancing,
soccer, volleyball, basketball, squash, speed skating, gymnastics, hockey, and step-aerobics. Endurance ac-
tivities such as orienteering, skiing, and triathlon seem to be beneficial to a lesser degree, whereas low-impact
activities such as swimming and cycling are associated with lower BMD than controls. Both the intensity and
frequency of the activity should be varied and increased beyond the habitual level. Duration of the activity
seems to be less important, and a few loading cycles seem to be sufficient.
INTRODUCTION
Osteoporotic fractures constitute a substantial health
problem, particularly in the elderly, causing more dis-
ability than most other diseases [1]. Among many risk
factors, physical inactivity has been related to a higher
risk of osteoporotic fracture [2]. Physical activity may
postpone the age-related decline in bone mineral den-
sity (BMD), and by that reduce the risk of fracture.
BMD is at present the most common single measure of
bone strength [3] and also a major predictor of fracture
risk [4-7]. The effects of physical activity on BMD are
primarily linked to the mechanisms of mechanical
loading [8-10]. Knowledge about the importance of
various types and sources of loading stimuli will have
implications for the design of physical activity pro-
grams aimed at preventing osteoporosis.
The aim of this paper was to review the literature
concerning mechanical loading in relation to BMD,
with focus on which types of stimuli and sources of
loading that are most effective.
BONE REMODELING AND MECHANICAL
LOADING
Bone is a highly dynamic tissue that adapts its mass
and architecture to the physiological and mechanical
environment [11]. Bone is constantly renewed during
adulthood, when bone mass and architecture are main-
tained by bone remodeling [12]. Remodeling involves
bone resorption and bone formation, a continuous pro-
cess of bone cells removing and replacing bone tissue,
and an imbalance in the remodeling process can cause
osteoporosis. The bone cells involved in remodeling
are osteoclasts (which remove bone) and osteoblasts
(which produce new bone), forming the "basic multi-
cellular unit" [12]. Remodeling can occur at four
surfaces; the periosteal, endocortical, trabecular, and
intracortical (Haversian) [12], although the turnover is
higher in trabecular than in cortical bone.
As early as in 1892, Wolff stated that bone tissue
accommodates to stress that is imposed on it [13], and
later research on the topic has been founded on this
contention. Several theories have been proposed to
explain the loading mechanism, and one of the most
recognized is the “Mechanostat theory” by Harold
Frost [14-16]. Frost proposed that local deformation
from mechanical loading stimulates bone cells, resul-
ting in bone adaptation, under the influence of para-
meters such as age, sex, environment, genes, nutrition,
and systemic biochemical factors [11,17]. Today, it is
generally acknowledged that loads applied to bone aff-
ect bone mass [9] and morphology (e.g. cross-sectional
area and thickness of cortical bone) [18,19] through a
mechanism called "mechanotransduction”. Mechano-

174 B. MORSETH ET AL.
transduction involves conversion of a mechanical force
into a cellular response. The process is not yet fully
understood, but seems to include osteocytes, which
detect mechanical strain and transduce the applied
strain to the cells (osteoblasts and osteoclasts) on the
surface, where bone remodeling (formation and re-
sorption) occurs [8,10,20]. Details of the cellular pro-
cesses of mechanical loading have been reviewed pre-
viously [20-22] and will not be further elaborated here.
PHYSICAL ACTIVITY AN D BMD
Data from numerous cross-sectional studies demon-
strate a positive association between BMD and phys-
ical activity [23-25]. Generally, athletes have higher
BMD than age-matched sedentary controls [26-30].
The most extensive evidence from human studies sup-
porting the effect of exercise on bone mass has been
obtained from studies of unilateral loading, as in tennis
players, where the dominant arm has thicker cortices
and up to 22% higher BMD than the non-dominant
arm [31-34].
Intervention studies in pre- and peripubertal chil-
dren confirm the findings from cross-sectional studies
that high-impact physical activity [35-37] and regular
physical activity increases BMD [38,39]. In adults, the
effect of physical activity is smaller and less consis-
tent. Findings from intervention studies in premeno-
pausal women indicate that young women who exer-
cise continue to increase bone mass compared to non-
exercising controls [40-42]. In postmenopausal women,
systematic reviews indicate that physical activity may
slow the rate of bone loss on weight-bearing sites with
an effect of approximately 1% per year [40,41]. This
finding has been confirmed in two other reviews,
which concluded that there is strong evidence of the
effect of daily walking on the femoral neck bone mass
in postmenopausal women [43,44]. The results seen in
women are also present in the few existing studies in
men [45-47].
Taken together, most results indicate that physical
activity has an effect on BMD. Nevertheless, the exact
type and amount of physical activity that may increase
BMD and reduce the risk of fracture is still uncertain
due to lack of randomized, controlled studies (particu-
larly on fracture risk), a large number of confounders
to control for, as well as an incomplete understanding
of the precise mechanism behind the association be-
tween physical activity and BMD [48,49].
WHICH TYPES OF STRAIN ARE MOST
EFFECTIVE TO INCREASE BMD?
A load that is applied to bone is called stress, defined
as force divided by area [50]. The applied load causes
a mechanical deformation of bone tissue, and this de-
formation can be measured as strain [11,51]. Strain is
the ratio of the amount of shortening (Δl) divided by
the original length (l), typically expressed as micro-
strain, 10-6 (i.e. a bone of length 500 mm experiencing
0.5 mm deformation gives a strain of 0.001 or 0.1%,
equal to 1000 microstrain) [11,20,51]. Strains may be
compressive, tensile (when the bone is stretched), or
torsional (shear) (when the bone is twisted), and in
most situations, they affect bone in a combined way
[11,50], i.e. a deformation can create 2500 microstrain
in compression on the concave side of a bending
diaphysis, while creating 2000 microstrain in tension
on the other side [51].
In humans, an in vivo study of the tibia has shown
that running produced larger strains and higher strain
rate on the tibia than walking, while bicycling produ-
ced lower strains than walking [52]. Step and leg press
did not induce larger strain or strain rate than walking.
Strain magnitude ranged from 271 to 5027 microstrain
and strain rate from 1258 to 38 164 microstrain/s. In
accordance with these findings, Burr et al. [53] showed
that strains during running were 2-3 times higher than
during walking.
Frost's mechanostat theory [54] indicates that there
is a lower and an upper strain threshold, creating a
range where strain stimuli maintains homeostasis of
the remodeling process and bone mass, called the
physiological loading zone. Below the lower threshold
(200 microstrain), called the "minimum effective strain
for remodeling", the stimuli is insufficient to maintain
formation, and resorption will be the overriding pro-
cess, resulting in bone loss. Above the upper threshold
(2000 microstrain), the "minimum effective strain for
modeling", formation is dominant, resulting in bone
gain. These thresholds may be relative to the indivi-
dual's habitual loads [11].
The mechanostat theory mainly relies on the magni-
tude of the strain [51], and animal studies support that
strain magnitude is an important driving force for bone
remodeling [55,56]. However, several animal studies
have demonstrated that dynamic, but not static strains
(strain rate = 0), induce bone formation [56-59]. In the
animal studies, jumping was more osteogenic than
running, and strain rate was higher in jumping than
running at similar strain magnitude [60,61]. Translated
to humans, this would imply that high-impact activities
are more effective than running and walking [62].
Moreover, studies of the effect of low-magnitude,
high-frequent vibrations indicate that the magnitude
may be less important than strain rate and frequency
[48,51,58,59]. An important implication of this is that
an increase in rate or frequency, not only magnitude,
may represent overload and bone formation [11,51].
Uneven distribution of the strain seems to have a
higher potential for increasing osteogenesis than the
habitual loading pattern [62-65], indicating that the
intensity and type of activity should be increased or
changed beyond the habitual level. Moreover, after a
few loading cycles, the adaptive response decreases
[56,66]. Inserting a rest period after each loading cycle
can increase the osteogenic response [55,58,67,68].
In conclusion, animal studies and a small number of

PHYSICAL ACTIVITY AND BONE HEALTH 175
studies of humans indicate that the stimuli from high-
impact activities (e.g., jumping) is more effective than
running and walking, as jumping has a higher strain
rate than running even at the same strain magnitude.
The activity should be dynamic, not static, and the
load should be increased or changed beyond the hab-
itual level. Moreover, a few loading cycles seems suf-
ficient, and a rest period after each loading cycle can
increase the osteogenic response.
WHICH SOURCES OF MECHANICAL LOADING
ARE MOST IMPORTANT TO BMD?
During physical activity, mechanical forces that act on
bone are generated mainly from two sources; loads
from impact with the ground (ground-reaction forces)
and loads from skeletal muscle contractions (muscle
forces or muscle-joint forces) [69,70]. Ground-reaction
forces are generated from contact between the body
and a surface due to gravitation, whereas muscle loads
result from muscle contractions creating a force that is
transmitted to the bone through the tendons [49]. The
relative importance of these two sources for stimula-
tion of bone is under debate and was recently the center
of attention in four symposium reviews [48,49,69,71].
In support of his mechanostat theory, Frost asserted
that ‘‘Bone strength and mass normally adapt to the
largest voluntary loads on bones. The loads come from
muscles, not body weight’’ [48]. From a theoretical
view, the magnitude of muscle loading on bone is lar-
ger than the gravitational loading, at least during sim-
ple static movements, because of differences in lever
arm length [48,49]. In a static exercise, ground-
reaction forces x lever A should equal muscle force x
lever B to maintain equilibrium at the joint. Thus, if
lever A is longer than lever B, the muscle forces must
be equally larger than ground-reaction forces [49].
However, many factors must be considered in more
complex, dynamic exercises; varying lever arm lengths,
body mass, acceleration (or deceleration), and eccentric
muscle contractions [49]. Thus, only simple loading si-
tuations are easily measurable because most movements
are complex [49]. Experimental research has shown
that peak ground-reaction forces are approximately 1.5
times body weight during walking (3.6-10.8 km/h) and
2-3 times body weight during running (5.4-21 km/h)
[72], whereas peak muscle force is 2.8-4.8 times body
weight during walking (1-5 km/h) and 5-6 times body
weight during jogging and stair walking [73]. For more
complex activities, less experimental evidence exists,
and the discussion must be based on research of asso-
ciations between disuse, loading, muscle mass, and
bone mass.
Space flight studies are particularly suitable because
astronauts are subject to weightlessness, while at the
same time, they are required to perform exercise while
being in space [49]. During long-duration spaceflight,
severe loss of both trabecular and cortical bone mass
has been observed, particularly in the lower skeleton,
despite daily exercise routines [74-76]. In paraplegic
patients, bone loss continues several years longer than
muscle loss [77]. These findings indicate that gravita-
tional loading is essential for bone homeostasis [49,78].
Papers in the field of mechanical loading during
exercise often refer to weight-bearing and weight-
supported (non-weight-bearing) activities. Kohrt et al.
[69] has suggested that the terms "impact" (ground-
reaction forces) and "no-impact" (joint-reaction forces
or muscle-joint forces) activities are better suitable to
describe the source of loading.
Impact activities generate gravitational loads on the
skeleton; thus, impact activities are weight-bearing
(e.g. jumping) [69]. However, most impact activities
also involve muscle forces [49,69], and the individual
effect of the ground-reaction forces can be difficult to
separate. Impact activities primarily involve the lower
skeleton and are often divided into high-impact and
low-impact activities.
In contrast, no-impact activities influence bone
mostly through muscle loading [49,69]. No-impact
activities can be weight-bearing (e.g. weight lifting) or
weight-supported (e.g. swimming, cycling) [49,69].
The understanding of the effects and importance of
various strains and loading sources in humans is chal-
lenging, and much of the knowledge comes from exer-
cise studies [49]. To differentiate between sources of
reaction force, it may be useful to study whether the
activity involves primarily impact/ground-reaction
loads or not.
Cross-sectional studies have typically compared
athletes in various sports and sedentary controls
[28,29,63,79-83]. As an example, Nikander et al. [29]
compared femoral neck BMD in premenopausal fe-
male athletes who competed in sports with different
types of load. Athletes competing in high-impact sports
(volleyball, hurdling, squash-playing, soccer, speed
skating, step-aerobics ) had the highest femoral neck
BMD, followed by weight-lifters, thereafter orientee-
ring and skiing athletes, while swimmers and cyclists
had BMD similar to the non-athletes [29].
Mudd et al. [79] found that swimmers and runners
had lower total and site-specific BMD than athletes in
sports such as gymnastics, track, soccer, softball and
field hockey. In another study, female runners had
highest femoral neck BMD, compared to triathletes
and cyclists, who had higher BMD than controls, while
swimmers had lower BMD than controls [80]. Similar
results have been found in other cross-sectional studies
of athletes, mostly premenopausal women [63,81-83]
and men [28] with impact activities including soccer,
dancing, volleyball, basketball, squash, speed skating,
weight lifting, and gymnastics compared to swimming
as no-impact activity and/or sedentary controls.
In conclusion, cross-sectional studies indicate that a
range of high-impact activities are associated with
higher BMD, while swimming and cycling are associ-
ated with lower BMD, than controls. Endurance ac-
tivities seem to be beneficial to a lesser degree. These
studies indicate that ground-reaction forces are impor-

176 B. MORSETH ET AL.
tant for site-specific BMD and that muscle contractions
are less important but still effective. However, causal
conclusions cannot be drawn from cross-sectional
studies.
In an intervention study, Kohrt et al. [73] compared
the effect of impact load (walking, jogging, stair
climbing) and no-impact, weight-bearing load (weight-
lifting, rowing) on BMD in postmenopausal women.
After 9 months, both types of exercise increased spine
and total hip BMD, while only the impact group
increased their femoral neck BMD [73]. Impact activi-
ties (walking, jogging, star climbing) were associated
with the highest increase in BMD, in contrast to
controls who did not increase their BMD at all [73].
Likewise, Snow-Harter et al. [42] found that in young
women, both weight-training and running produced an
increase in spine BMD, whereas only weight-training
increased muscle strength. Intervention studies indi-
cate that gravitational forces are essential for BMD of
the femoral neck, but not the spine, suggesting that
muscle contractions and ground-reaction forces could
be efficient at different skeletal sites. However, in
other studies, no-impact resistance training have been
found to increase or preserve femoral neck BMD in
postmenopausal women [84] and elderly men [85],
emphasizing the inconsistency of the findings.
Unfortunately, most studies of humans are based on
small sample sizes, and epidemiological studies of
large cohorts are difficult to implement. Recent meta-
analyses by Martyn-St James and Carroll [86-90]
studied the effect of different exercise types on BMD
in pre- and postmenopausal women. Resistance train-
ing alone increased lumbar spine BMD, but not fe-
moral neck BMD [86,87,89], whereas combining im-
pact activities with resistance training significantly
increased BMD at both sites [89,90]. In postmeno-
pausal women, low-impact exercise (jogging com-
bined with stair climbing and walking) also increased
BMD at the lumbar spine and femoral neck [90], but
not walking alone [88]. These meta-analyses suggest
that impact forces of a certain magnitude and rate, but
not resistance training, were sufficient to increase fe-
moral neck BMD, and that resistance training has
strongest effect on lumbar spine BMD.
CONCLUSION
The existing literature shows that both muscle-joint
forces and gravitational forces may be able to induce
bone adaptation independently; though in most situa-
tions these forces act together. Ground-reaction forces
of a certain magnitude and rate seem to be essential for
BMD at the hip, but not the spine, whereas resistance
training seems to have strongest effect on spine BMD.
This suggests that muscle contractions and ground-
reaction forces could act differently at different skel-
etal sites. The nature of the activity should be dy-
namic, not static, and the magnitude and rate of the
stimuli should be high, preferentially involving high-
impact activities and resistance training. Endurance
activities seem to be beneficial to a lesser degree,
whereas low-impact activities are not beneficial. Both
the intensity and frequency of the activity should be
varied and increased beyond the habitual level. Dur-
ation of the activity seems to be less important, as a
few loading cycles seem to be sufficient.
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