Sports Mad.

19 (2): 103· 122,1995

REVIEW ARTICLE oI I 2· I642/95/0CIY2-D IO3/SI 0,00/0
© Ads International Umited. All rights reserved.

Exercise and Bone Mineral Density

Philip D. Chilibeck, Digby G. Sale and Colin E. Webber
Departments of Kinesiology and Nuclear Medicine, McMaster University,
Hamilton, Ontario, Canada

Contents
Summary .. ... . ... . . . . . . . . . 103
1. Animal Studies . . . . . . . . . . . . . . . 104
1.1 Physical Changes in Stressed Bone . 104
1.2 Mechanical Changes in Stressed Bone 105
1.3 Optimal Strain Characteristics for Bone Formation . 105
2. Human Studies . . . . . . . . 106
2.1 Cross-Sectional Studies. . . . . . . . . . . . . , . . 106
2.2 Longitudinal Studies . . . . . . . . . . . . . . . . . 109
3. Effects of Loading on the Remodelling Cycle of Bone 113
3,1 Quiescence to Activation . 113
3.2 Resorption 114
3.3 Reversal . . , . . . . . . . . 114
3.4 Formation . . . . . . . . . . 114
3.5 Modifications of the Remodelling Cycle with Loading 114
4. Mechanisms for Transformation of Mechanical Stimuli to Biomechanical Signals for
New Bone Formation .. . . . . . . .... . 115
4.1 Prostaglandin Release . . . . . . . . . . 115
4.2 Piezoelectric and Streaming Potentials 116
4.3 Bone Blood Flow . . . . . . . . . . . . . 117
4.4 Bone Formation in Response to Microdamage . 117
4.5 Hormonally Mediated Mechanisms 117
5. Conclusions , . . . . . . . . . . . . . . . . . . , . . . . 118

Summary A decrease in physical activity may lead to an increased loss of bone and an
increase in the incidence of osteoporotic fractures. Studies have demonstrated
increases in bone formation in animals and increases in bone mineral density in
humans. Studies of animals show that bone has enhanced physical and mechan-
ical properties following periods of increased stress. Strains which are high in
rate and magnitude, and of abnormal distribution, but not necessarily long in
duration, are best for inducing new bone formation, resulting in the strengthening
of bone by increased density. Cross-sectional studies show that athletes, espe-
cially those who are strength-trained, have greater bone mineral densities than
non athletes, and that strength, muscle mass and maximal oxygen uptake correlate
with bone density. Longitudinal training studies indicate that strength training
and high impact endurance training increase bone density.
Strain induction, the deformation that occurs in bone under loading, may cause
a greater level of formation and an inhibition of resorption within the normal
104 Chilibeck et al.

remodelling cycle of bone, or it may cause direct activation of osteoblastic bone

formation from the quiescent state.
Various mechanisms have been proposed for the transformation of mechanical
strain into biochemical stimuli to enhance bone formation. These include prosta-
glandin release, piezoelectric and streaming potentials, increased bone blood
flow, microdamage and hormonally mediated mechanisms. These mechanisms
may act on their own or in concert, depending on the loading situation and the
characteristics of the bone.

Osteoporosis is an increasing problem in to-
day's society, with the incidence of osteoporotic
fractures increasing faster than can be explained by
the increase in age of the population.[l] Although
numerous factors affect bone mineral density
(BMD), which is highly correlated with bone
strength,[2,3] an increasingly sedentary lifestyle is
blamed for the decreasing bone density of our pop-
ulation.[l] BMD is higher in young[4] and elderly[5]
women, and in middle-aged men[6] and women[7,8]
who engage in greater amounts of physical activity.
A less physically active lifestyle has also been as-
sociated with an increased incidence of osteo-
porotic fracture.l 9 ] Exercise has, therefore, been
recommended as a treatment for increasing bone
density after menopause,[IO] and as a preventative
measure before menopause since substantial tra-
becular bone loss may occur premenopausallyJll.14]
(Trabecular bone is relatively porous with a high
mineral turnover rate, and is found mainly in the
axial skeleton; cortical bone is more dense with a
low mineral turnover rate, and is found mainly in
the appendicular skeleton.)
Exercise along with estrogen supplementation
after menopause[15] and an adequate level of calcium
in the diet[16] seems to be the best combination for
preventing or treating osteoporosis, although there
is some debate about estrogen supplementation
(unopposed by progestogen supplementation) and
an increased risk of breast cancer, thought to be
caused by the estrogen-without-progestogen sup-
plementation. [17]
The purpose of this review is to identify the
physical and mechanical changes that occur in
bone as a result of exercise stress, to review which
exercise regimens are most effective in increasing
bone density, and to review the possible mechanisms
by which strain is detected and transformed into a
biochemical signal to activate bone formation.
The first part of this review will examine studies
using animal models which show how the physical
and mechanical properties of bone change with ex-
ercise, and which strain regimens are most effec-
tive in forming new bone. Conclusions from these
studies will then be compared with cross-sectional
and longitudinal studies involving humans. The
third part of this review will discuss the normal
bone remodelling cycle and how it may be affected
by mechanical loading. The final part will review
proposed mechanisms by which strain is detected
and transformed into biochemical signals for new
bone formation.
1. Animal Studies
1.1 Physical Changes in Stressed Bone
When different species of animals undergo
treadmill exercise training,[18] have artificial exter-
nalloads applied to bone through implants[19-2 11 or
have increased loads imposed on radii (by the re-
moval of ulnae[22]), increases in new bone forma-
tion on loaded bone surfaces are evident on post-
humous examination. Tetracyline, injected into
exercising animals, allows labelling of areas of
mineral deposition and new bone formation. The
periosteum, which is the thick fibrous membrane
covering the entire bone surface, usually shows the
greatest increase in bone formation following load-
ing due to the muscular attachments which induce
greater strains. [221 The endosteum, the layer of cells

© Adis International limited. All rights reserved. Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density
lining the inner surface of bone, gives rise to
smaller amounts of new bone in response to load-
ing. Total volume, and the dry, ash, calcium and
fat-free weights of stressed bone are greater fol-
lowing exercise training.l 18 ,23]
1.2 Mechanical Changes in Stressed Bone
The mechanical strength of bone can be deter-
mined from bending tests and the development of
stress-strain or load-deformation curves,l24] Stress
is defined as the load per unit area developed on a
bone surface due to externally applied loads. Strain
is defined as the deformation that occurs in re-
sponse to this loading. The resulting stress-strain
curve is an illustration of deformation because of
loading. Strength of bone (in terms of energy stor-
age) is defined as the area under this curve.
Bending tests have shown that bone taken from
exercised animals is stronger, in that there is more
energy stored and higher maximal loads are
reached before breaking,l23] The force that bone is
able to resist at yield (bending) and ultimate
(breaking) points is' higher in exercised than in con-
trol animals.[18] Thus, loading regimens result in
increased bone formation, and enhanced structural
and mechanical properties.
1.3 Optimal Strain Characteristics for
Bone Formation
7.3. 7 Strain Magnitude
Using implanted strain gauges in rooster ulnae,
it has been shown that a greater amount of bone
formation occurs when bone is subjected to pro-
gressively greater magnitudes of strain, through
external, artificial loading.l 21 ] This results in a
stronger bone.
Frost[25] proposed a theory in which a minimum
effective strain is necessary for bone formation to
occur. Once this strain is detected by bone cells new
bone is formed, strengthening the bone and reduc-
ing the strain response to a given stress. The newly
reduced strain is then ineffective as a stimulus and
bone formation ceases. Thus, a feedback mecha-
nism is present in bone to reduce strain levels.[26]
© Adis International Limited. All rights reserved.
105
This feedback mechanism is evident in in vivo
studies in which pigs have the ulna from one limb
removed, resulting in increased strain (measured
by implanted strain gauges) in the remaining radius
during functional 10ading.[27] New bone is laid
down in the radius, making it stronger and reduc-
ing the strain. The newly reduced strain is no
longer effective in stimulating bone formation and
formation ceases, through the feedback mecha-
nism. A minimum effective strain is needed, as
shown in loading experiments on long bones,
where new bone only forms on the compression
side of the bone (where strain is greatest), and little
or no bone forms on the tensile side (where there
is less strain).[22,28]
Further evidence of increased bone formation
resulting from higher strain magnitudes is shown
in studies which demonstrate that, given a fixed
level of stress, immature bone shows greater in-
creases in formation than mature bone. [29] Imma-
ture bone is much more compliant, resulting in
greater strain magnitudes than those which occur
in stiffer mature bone.[30]
7.3.2 Strain Rate
By applying intermittent loads to sheep radius,
in vivo through implants, it was found that most
bone is formed in response to the highest physio-
logical strain rates PO] and that strains of high mag-
nitude are inadequate in stimulating new bone for-
mation unless imposed at high strain rates.[22]
Substantial changes in bone are observed after only
6 weeks, with 1 hour of artificial loading per day.
High strain rates applied over a short period of time
are, therefore, effective in stimulating new bone
formation.
7.3.3 Strain Distribution
When strain distribution is altered in sheep ra-
dius by removal of the ulna, new bone is deposited
to compensate for the structural loss.[22] After 50
weeks, strain levels are actually lower than normal,
suggesting that peak strain levels are less respon-
sible for stimulating the adaptive response than are
the changes in strain distribution. Bone formation
can be stimulated by submaximal strains if strain
distribution is abnormal.
Sports Med. 19 (2) 1995
106
1.3.4 Static Versus Dynamic Strain
It has been shown that continuously applied
stress (static strain) is ineffective in stimulating
bone formation, whereas intermittent loading (dy-
namic strain) is effective. When remodelling activ-
ity in turkey ulnae was assessed under conditions
of disuse and disuse interrupted by short daily pe-
riods of either static or dynamic compressive loads
of similar magnitude, nonloaded and statically
loaded bone demonstrated losses in bone, while dy-
namically loaded bone showed increases in forma-
tion.l 31 ] Similar results were found in the rabbit
tibia, which did not respond to continuous stress[32]
but showed new bone formation following inter-
mittent loading. Stress must be dynamic in nature
in order for bone formation to be stimulated.
1.3.5 Strain Cycles
By altering the number of strain cycles imposed
on rooster ulnae in situ, and keeping strain magni-
tude and rate constant, it was found that only a
small number of loading cycles per day was re-
quired for gains in bone mineral content (BMC).[33]
When mathematical modelling relating bone den-
sity to daily stress histories was applied to running
studies, it was found that stress magnitude had a
greater influence on bone mass than did the number
ofloading cycles.[34] If strains are dynamic, high in
magnitUde, high in rate and of abnormal distribu-
tion, a substantial bone formation response can be
achieved after remarkably few loading cycles.
1.3.6 Implications for Designing Exercise
Programmes to Increase Bone Mass
From the results of these studies, exercise regi-
mens designed to increase bone mass and strength
should involve loads of high magnitude and rate,
should be dynamic in nature and involve varied and
diverse patterns of stress. Relatively few cycles of
loading per day would be required, so the exercise
would not have to be long in duration.
Weight training offers loading of high magni-
tude and varied patterns of stress, through lifting
exercises with strain distributions which are differ-
ent from those encountered in normal daily activi-
ties. Disadvantages are that loads are more static in
nature and are applied at relatively low rates. Run-
© Adis Intemational Limited. All rights reseNed.
Chilibeck et al.
ning or aerobic dance programmes involve dy-
namic, high impact loading at high strain rates.
Disadvantages are that peak strain magnitudes are
not particularly high and strain distribution is not
altered to a great degree. The advantages of one
exercise programme over another are still very un-
clear. Human exercise studies, discussed in section
2, have generated mixed results.
2. Human Studies
The following review of cross-sectional and
longitudinal studies is not comprehensive. Instead,
studies with the largest sample sizes and fewest
limitations in methodology have been included.
2.1 Cross-Sectional Studies
2. 1. 1 Athletic Groups
Cross-sectional studies of athletic groups show
that strength-trained athletes have higher BMD
than do endurance trained athletes and nonathletes.
This has been confirmed for young male and fe-
male athletes: BMDs of the lumbar spine, femoral
neck, distal radius, distal femur, patella, proximal
tibia and calcaneus were found to be approximately
9 to 26% higher in young female weightlifters than
in endurance athletes and control individuals.[35-37]
Young and middle-aged weight-trained males sim-
ilarly have greater femoral and spinal BMDs than
do runners, swimmers[38] and control individu-
als. [39-41]
Elite male junior weightlifters (mean age 17.4
years) were found to have 13 to 30% greater spine
and femoral neck BMD than in age-matched non-
weightlifters and adults (20- to 39-year-old men),[42]
indicating that bone mass may be increased rela-
tively early in life with few years of training (2 to
3 years of training for participants in this study). A
retrospective study of young male world-class
powerlifters found that lumbar vertebral BMD was
highly correlated (r = 0.82) with the total poundage
lifted over the past training year.l43 ] The vertebral
BMC of the powerlifters was 36% higher than in
age-matched non-weightlifters. Mathematical mod-
elling found that the loads on the lumbar spine
during maximal dead lifts exceeded those found at
Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density
the maximal ultimate strength of experimentally
tested vertebrae. Thus, the heavy loading of bone
is associated with an elevated BMC, inferring a
bone formation response to high strain magni-
tudes. Weight training may stimulate bone forma-
tion through the direct action of muscle pulling on
bone or the increased effect of gravity acting on
bone when heavy weights are supported by the
skeleton.
BMD is also elevated in athletes who sustain
high impact loads (landing from heights) in train-
ing and competition. Slemenda and Johnston[44]
found that figure skaters had 5.6% greater total
body BMD and 8 to 14% greater trunk, legs and
pelvis BMD compared with control individuals.
Nichols et aI.l45] found 8% higher lumbar spine and
femoral neck BMD in gymnasts than in control
individuals; 27 weeks of gymnastic training during
a school year resulted in a further significant 1.3%
increase in lumbar spine BMD.
Studies of endurance athletes show that young
female runners have lumbar BMD similar to that
of nonrunners[lI.36,37] but slightly higher BMD at
the distal femur and proximal tibia,[36] whereas
older male and female life-long runners have
greater BMC in the lumbar spine.l46,47]
Several studies have demonstrated that ex-
tremely high run training loads may have a detri-
mental effect on bone. It was found that lumbar
BMD was significantly reduced in young male
runners with a training mileage averaging 92krn
per week, compared with nonrunners.[48] It was
hypothesised that the high weekly mileage of this
running group may have resulted in lowered tes-
tosterone and higher cortisol levels, having a cata-
bolic effect on bone. A hormonal mechanism may
be responsible for reduced BMD in female endur-
ance athletes who engage in a high volume of train-
ing,[49.51] where estradiol and prolactin levels fall.
Grimston et al. [52] showed that a group of female run-
ners with low BMD, running more than 50 kmIweek,
had an altered calciotropic hormone response to a
calcium load administered before a treadmill run.
They had an increased parathyroid hormone re-
sponse (which increases bone resorption) and a
© Adis International Umited. All rights reserved.
107
decreased calcitonin response (which inhibits bone
resorption) ; this is opposite to changes seen in non-
runners and in a group of runners with normal BMD.
There may be a threshold level of exercise that
stimulates bone formation, with higher levels hav-
ing a reducing effect. It was found that male run-
ners (20 to 45 years of age) who run 24 to 32
kmIweek had significantly greater lower leg BMD
than those running 8 to 16 kmlweek and non-
runners;[53] however, with a training mileage greater
than 32 kmlweek, BMD tended to decrease. These
results indicate that a running mileage of 20 to 30
kmlweek may positively affect bone, but greater
amounts of training may have detrimental effects,
with altered hormone responses overriding the
load-induced stimulus for bone formation.
Proponents of impact-loading endurance-type
training hypothesise that the best stimulus for bone
formation is the effect of gravity plus increased
bodyweight upon bone, instead of muscle pull. A
finding that contradicts this theory is that male
swimmers, who were not engaged in any other type
of training (i.e. weight training), were found to
have greater lumbar spine and radial BMD than
nonexercising males.l 54] Swimming is a non-
weightbearing activity, so higher bone densities
would have to be attributed to the effects of muscle
pull. However, Grimston et aLl55] found that chil-
dren engaged in sports that involve impact loading
of greater than 3 times body weight (running, gym-
nastics and dance) had greater BMD of the femoral
neck than swimmers, and that swimmers had BMD
values within the normal population range. This
would favour an effect of gravity on increasing
bone mass.
While studies of athletic groups favour strength
over endurance training for improving BMD,
cross-sectional studies must be interpreted with
caution. The weight trainers used in most studies
are from highly selected groups, and therefore not
very suitable for comparison with normal popula-
tions. It has been suggested that genetics could ac-
count for up to 80% of the variability in bone den-
sity.[56] Individuals with genetically favourable
muscle and bone strength would be more likely to
Sports Med. 19 (2) 1995
108
participate in weight training at an elite level. This
is most evident in the study of elite male junior
weightlifters by Conroy et al.,l42] who found spinal
and femoral neck BMOs that were 33% and 24%
higher than in age-matched non-weighlifting indi-
viduals, respectively. Here the weightlifters had an
average of only 2.7 years of training experience.
This difference is much greater than the gains seen
in the most successful longitudinal studies, which
demonstrate increases in bone mass of only a few
per cent per year.[57,58]
Anabolic steroid usage by weight trainers could
be a confounding variable, as this may increase
bone mass l59 ] independently of the effects of
weight training. The studies of Colleti et aLl40] and
Karlsson et aLl41] included individuals who admit-
ted to steroid usage, while Nilsson and Westlin[38]
and Block et al.[39] did not screen study participants
for steroid use. Heinrich et aLl37] screened their fe-
male study participants for steroid and oral contra-
ceptive use, while Conroy et al.[42) screened for
steroid use by questionnaire and urinalysis. An-
other confounding variable is body mass differ-
ences between weight trainers and non-weight
trainers, since heavier individuals tend to have
higher BMO.[l2.60) Weightlifters in the studies of
Heinreich et aLl37] and Nilsson and Westlin[38] had
significantly higher body mass, and those in the
study of Block et aLl39] had a significantly higher
body mass index than their non-weight training
counterparts. Heinonen et al,l36) adjusted their re-
sults for body mass, and still found that female
weightlifters had higher BMO than non-weight-
lifters. These confounding factors should be con-
sidered when interpreting the results of studies
favouring strength over endurance training.
2. 1.2 Strength, Lean Body Mass,
Muscle Mass, Maximal Oxygen Uptake
and Bone Mineral Density
To eliminate the potential bias of using highly
selected groups, several investigators have looked
at the relationship between muscle strength, mus-
cle mass or maximal oxygen uptake and BMO in
normal populations. If strength training builds
bone through local effects, there should be a rela-
© Adis Interno~onollimited . All rights reserved.
Chilibeck et al.
tionship between the strength of a muscle and the
bone to which it is attached.
Moderate, but significant, correlations are
found between hip adductor or quadriceps strength
and hip BMO (r =0.24 to 0.55) in young (20 to 30
years of age) females[61 ,62) and middle-aged (28 to
51 years of age) males,[6] back extensor strength
and spine BMO (r =0.34 to 0.58) in middle-aged
males,[6) old males (61 to 84 years of age)l63] and
females (48 to 50 years of age),l64] and grip strength
and radius BMO (r =0.37 to 0.47) in old males and
females[63] and young females,l62]
The strength of some muscle groups correlates
with densities of bone far from their sites of attach-
ment. Biceps and grip strength are 2 of the best
predictors (r =0.37 to 0.45) of lumbar spine BMO
in 01d[63) and young[62.65] females and middle-aged
males.[6] It is possible that biceps and forearm
strength are good indicators of overall strength, or
that arm activity is linked to the simultaneous con-
traction of trunk stabilising muscles that exert
forces on the spine. Also, the length of the lever
arm between arm muscles and the spine is greater
than that between the back extensors and the spine,
so that loads on the spine generated by arm activity
are greater than those generated by back extensors.
Arm strength may therefore be an indicator of spine
bone strength. The lack of strong correlations be-
tween many strength measures and bone densities
may be because strength is not only dependent on
the size of the muscle that attaches to bone, but also
on the neural drive to the muscle.[66] This weakens
the relationship between strength and bone.
Total body BMO correlates with lean body mass
in men, but not women once fat mass has been
taken into account.[67,68] In either case, when BMO
is expressed in relation to height (BMO/height),
the relationship between BMO and lean body mass
disappears. It has been argued that lean body mass-
BMD relationships are artifacts attributable to the
use of areal density measurements,l68]
Studies which have measured the size of spe-
cific muscles have found good correlations with
the density of the bones to which they are attached.
The weight of the left psoas muscle, obtained from
Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density 109

Table I. Longitudinal strength training and bone mineral density

Reference Gender, age (years) No. Method Training Significant bone results
Gleeson et al.(74) F, 30-40 E 34 DPA 3 days/week 0.8% increase in lumbar spine BMD
(pre-menopausal) C 38 12 months (significant compared with 0.5%
8 exercises control decrease)
2 sets/20 reps
60% of 1 RM
Menkes et al. [58) M,59±2.0 E 11 DEXA 3 days/week 3.8% increase in femoral neck BMD;
C 7 16 weeks 2.0% increase in lumbar spine BMD
13 exercises
1-2 sets/15 reps
Pruitt et al. (75) F,53.6±2.0 E17 DPA 3 days/week 1.6% increase in lumbar spine BMD
(post-menopausal) C 9 9 months (significant compared with 3.6%
11 exercises control decrease)
1 setl10-15 reps
60-80% of 1 RM
Rockwell et alF61 F,40±1.6 E10 DEXA 2 days/week 3.96% decrease in lumbar spine BMD
(pre-menopausal) C 7 months
8 exercises
2 sets/12 reps
70% of 1 RM
Ryan et al. In) M,61 (range 51-71) E21 DEXA 3 days/week 2.8% increase in femoral neck BMD
C 16 16 weeks
14 exercises
2 sets/15 reps
Snow-Harter et a1F8) F, 20±0.7 E 12 DEXA 3 days/week 1.2% increase in lumbar spine BMD
C 8 8 months
14 exercises
3 sets/8-12 reps
70-85% of 1 RM
Abbreviations: BMD =bone mineral density; C =control group; DEXA =dual energy x-ray absorptiometry; DPA =dual photon absorptiometry;
E = exercise group; F =females; M = males; reps = repetitions; RM =repetition maximum.

47 cadavers, correlates well (r = 0.72) with the ash
weight of the third lumbar vertebra.l 69 ) Leg lean
muscle mass and leg BMD, measured by dual en-
ergy x-ray absorptiometry (DEXA) in young fe-
males, are significantly correlated (r = 0.59)PO)
Spine and hip BMD correlates with paraspinous
muscle area (r = 0.33 to 0.55), obtained by com-
puted tomography)39) Thus, muscle size tends to
be a better indicator of BMD than strength.
When maximal oxygen uptake, an indicator of
aerobic power, is measured, significant correla-
tions have been found with lumbar spine BMD in
males (r = 0.41)[63) and females (r = 0.54)[63J and
with femoral neck BMD (r = 0.6) in females.[7))
However, other studies have failed to show such
correlations in postmenopausal women.l 72 ,73)
From these findings it is difficult to draw con-
clusions on which type of training is more benefi-
cial in increasing BMD. The results of longitudinal
studies have also been equivocal, as discussed in
section 2.2.
2.2 Longitudinal Studies
2.2. 1 Strength Training Studies
Six recent training studies have employed
whole-body strength training in an attempt to in-
crease BMD, with the hypothesis that training may
have effects either systemically, through the direct
attachment of muscle on bone, or through stabilis-
ing musculature used during different lifts (see ta-
ble I). These studies demonstrate positive effects
on bone except for the study of Rockwell et aJ.l76)
The studies in females failed to induce significant
gains in hip bone mass. The proximal femur, hav-
ing a higher percentage of cortical bone (which is
less metabolically active than trabecular bone)

© Adis International Limited. All rights reserved. Sports Med. 19 (2) 1995
110
than the lumbar spine, may require longer training
durations to produce changes.
The decrease in lumbar BMD found by Rock-
well et aP76] after a programme of weight training
in middle-aged women is difficult to explain.
These authors did not offer an explanation, but con-
ceded limitations such as the small number of study
participants who were self-selected into training
and control groups. It was also noted that the larg-
est decrease occurred over the first 4.5 months of
the 9-month training programme, and it was sug-
gested that in the first several months the effects of
such a programme serve to establish a new basal
state of bone turnover. Several further months may
be needed to evaluate the ultimate effects of this
kind of exercise on bone.
A problem with most of these studies is the
small number of participants used and the precision
of measurements needed to detect the small
changes in bone density. The precision of a meas-
urement affects the sample size needed to identify
a treatment effect with a given statistical power and
a-level.[79] Precision of bone measurements is of-
ten expressed as a coefficient of variation, obtained
by taking duplicate measures on a group of individ-
uals .[79,80] Taking into account the coefficients of
variation from duplicate measures for spine and hip
BMD with dual photon absorptiometry (DPA) and
DEXA,179,81-83] larger sample sizes are needed to
detect small BMD changes, especially those of the
hip,l79] Future studies will have to involve larger
sample sizes to determine whether or not small
changes seen in bone are significant. However, sev-
eral conclusions and recommendations can be
drawn from these studies.
• Males tended to show greater increases in bone
mass with training than females, despite the rel-
atively short duration of training and low inten-
sity used in the 2 studies of males.l 58 ,77]
• A training frequency of 3 days/week at intensi-
ties greater than 60% of 1 repetition maximum
tend to result in greater increases in BMD. Too
Iowan intensity may not result in sufficient peak
strain magnitudes to stimulate bone formation.
© Adis International Limited. All rights reserved.
Chilibeck et al.
• Training of 8 to 12 months duration results in
much smaller increases in BMD than expected
from cross-sectional comparisons of resistance-
trained and sedentary individuals. A training du-
ration of greater than 1 year may be needed
before physiologically significant gains in bone
mass are noticed. The bone remodelling cycle
lasts from 4 to 6 months; it is therefore recom-
mended that training studies be continued for at
least 1 year to ensure that the training effect is
measured over an equilibrium period. 157 ]
To determine if muscle may have direct effects
on bone, through tension caused by its attachment,
several studies have investigated the effects of
training specific muscle groups on the density of
the bones on which they pull. These have involved
either training of the back or forearm:
Training of the Back
Training for 1 year l84 ] and 2 years,[85] using back
extensions, situps or leg-lift exercises, failed to
change DPA-measured lumbar spine BMD in post-
menopausal women. Exercises were done at home
without supervision and, therefore, compliance
may have been low. The study by Sinaki et aLl85]
failed to screen participants for estrogen use; this
may have confounded their results. The DPA meas-
urements may not have been sufficiently precise I81 ,82]
to demonstrate any small treatment effects.
Training of the Forearm
Training of 77 elderly women resulted in sig-
nificant increases (3.4%) in single photon ab-
sorptiometry (SPA)-measured forearm BMD, fol-
lowing 6 weeks of forearm exercise (tennis ball
squeezing) for 30 seconds a day.l86] Six months of
detraining resulted in a 2.6% decrease in BMD.
Thus, small amounts of training are effective on the
forearm if carried out at sufficient strain magni-
tudes. The detraining results give evidence of the
dynamic nature of bone. When forearms of 14 el-
derly women were loaded in tension, bending,
compression and torsion (ensuring abnormal strain
distributions) at high strain rates, 3 times a week
for 5 months, BMD (measured by Compton scat-
tering) increased 3.8%.1 87 ] The Compton scattering
method measures bone volume as well as mass,
Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density
Table II. Longitudinal endurance training and bone mass in postmenopausal females
Reference No. Method
Dalsky et al.[72J E 17 DPA
C 18
Grove & LondereeI90J E10 DPA
C 5
Krolner et al. 191J E 13 DPA
C 14
Smith et al. 192J E80 SPA
C62
Abbreviations: BMC = bone mineral content; BMD = bone mineral density; C = control group; DEXA = dual energy x-ray absorptiometry;
DPA =dual photon absorptiometry; E =exercise group; SPA =single photon absorptiometry.
allowing bone density to be expressed in actual
units of density (g/cm3) rather than the 'areal' den-
sity units (g/cm2) employed by other techniques
(SPA, DPA, DEXA). A limitation of the former
is that marrow as well as mineral mass is mea-
sured; therefore, bone mineral density cannot be
measured.
Site-specific training appears to be effective in
increasing forearm BMD, whereas whole-body
strength training is more effective in increasing
lumbar BMD. This suggests that stabilising con-
tractions of trunk musculature or the effects of
gravitational loading are more effective than spe-
cific exercises that involve muscle attached to the
spine.
2.2.2 Endurance Training Studies
Endurance training may be beneficial in in-
creasing bone mass or density, by imposing
stresses through repetitive impact loading. Lack of
weightbearing, imposed by long term bed rest, re-
sults in marked loss of bone.l 88 ,89] If bed rest was
interspersed by 3 hours of standing per day, bone
loss was slowed; cycling or sitting had no effect. [88]
Gravity is therefore an important factor in stressing
© Adis International Limited. All rights reserved.
111
Training Sign~icant bone results
50-60 min/day 5.2-6.1 % increase in lumbar spine BMD (control
3 times/week group decrease of 1.4%)
9-22 months
Walking, jogging, stair
climbing, cycling, rowing,
bench press
20 min/day Exercise groups maintained BMD; control group
3 days/week had a significant decrease in lumbar spine BMD
12 months (6.1%)
High and low impact aerobics
60 min/day 3.5% increase in lumbar spine BMC (control group
2 times/week decrease of 2.7%)
8 months
Walking, running and
calisthenics
45 min/day Decrease in ulna and radial BMD and BMC (0.04
3 times/week and 0.65%) was significantly less than the control
4 years group decrease (1 .38 and 1.67%)
Aerobic dance with light upper
body weights
bone and maintaining bone balance. Enhancing this
effect through high impact loading may allow bone
balance to become more positive. Studies of mainly
early postmenopausal women have demonstrated
positive effects on bone, with a variety of endur-
ance-type impact loading exercises (table II).
Dalsky et aU 72 ] conducted the only well con-
trolled study, as others failed to minimise exercise
and nonexercise group differences in dietary in-
take,[90,92] estrogen supplementation[90,91] and even
menopausal status.l 91 ] It is difficult to derive an
exercise prescription from results of these studies
because of the wide differences in exercises used,
but it does appear that endurance impact-loading
exercise performed for durations ranging from 20
to 60 minutes per day, 2 to 3 days/week is just as
effective as weight training (table I) for increasing
bone mass. Future studies will have to involve
better control in screening of appropriate study
participants and strict adherence to one type of ex-
ercise, to determine which mode of exercise is most
effective.
Load bearing and/or impact loading may not be
a necessary feature of endurance training for a ben-
Sports Med. 19 (2) 1995
112 Chilibeck et al.

Table III. Walking interventions and bone mass in postmenopausal females

Reference No. Method Training Significant bone results
Cavanaugh & Cann l951 E 8 CT 15-40 min/day No difference between exercises and control
C 9 3 days/week group in changes of trabecular bone density
12 months of the lumbar spine
Walking at 60-85% of age-predicted
maximum heart rate
Hatori et al. 1961 E21 DEXA 30 min/day Lumbar spine BMD increased significantly
C 12 3 days/week only in the group walking above the
7 months anaerobic threshold (1.1% increase)
12 participants walked at intensities
> anaerobic threshold;
9 at intensities < anaerobic threshold
Martin & Notelovitz(97) E36 DPA 30-45 min/day No changes in lumbar spine BMD
C 19 3 days/week
12 months
Treadmill walking at 70-85%
maximal heart rate
Nelson et a1. (98) E 18 CT 50 min/day Trabecular bone density of the lumbar spine
C 18 4 days/week increased 0.5% in exercise group; decreased
12 months 7% in the control group
Walking at 75-80% maximum heart
rate with weighted belts
Abbreviations: C = control group; CT = computed tomography; DEXA = dual energy x-ray absorptiometry; BMD = bone mineral density;
E = exercise group.

eficial effect on bone. Bloomfield et al.[93] reported
a 3.6% increase in lumbar spine BMD but no change
in femoral BMD in postmenopausal women fol-
lowing 8 months of cycling training done for 30
min/day, 3 days/week.
For elderly individuals who have low fitness
levels or pre-existing fractures, low risk, low impact
or stable weightbearing activities are recom-
mended,[94] as they may help to strengthen or pro-
tect bone through increased muscle strength. Several
walking interventions have been performed with
postmenopausal women, with mixed results (table
III). Two studies have shown small positive gains
in bone mass, whereas 2 others showed no change.
The 2 studies showing positive gains had study par-
ticipants walking with weighted belts[98] and others
walking above their anaerobic thresholds,f96] It
therefore seems that walking has to be done at a
brisk pace or with the addition of loads (i.e., hand-
held weights) to result in any positive effects on
bone. Once again, the number of participants in-
volved in these studies may have been too small to
demonstrate small treatment effects with sufficient
precision.
2.2.3 Studies of Strength Versus
Endurance Training
In an attempt to find which type of training is
most effective, several investigators have formed 2
training groups within one study, each group per-
forming endurance, strength, or endurance com-
bined with strength exercises. Studies involving
post-menopausal women who either trained aero-
bically or combined aerobic and strength training,
30 to 45 minutes a day, 3 times/week for 10 to 12
months, showed small increases in upper thigh and
trunk calcium bone index (as measured by neutron
activation analysis)[99] and in SPA-measured distal
radius BMD,[IOO] but no change in DPA-measured
hip and spine BMD[IOI] when compared with con-
trol groups. Differences between training groups
were not found; however, various factors confound
the results of these studies. Compliance in the study
of Peterson et al,fIOl] is suspect, as weight training
was done unsupervised at home. Rikli et aLl 100] did
not screen out estrogen usage among their study

© Adis International Limited. All rights reseNed. Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density
participants, and the neutron activation analysis
technique. used by Chow et aI.l 99 l lacks sufficient
precision, due to the problem of site relocation
when part-body measurements are performed.l 102l
By combining strength and endurance training
on the same day, strength development may be im-
peded;[I03] therefore, the high muscle force levels
associated with strength training alone would not
be achieved, resulting in reduced high magnitude
loading of bone.
The only well controlled study which has com-
pared strength and endurance training in groups of
individuals with similar baseline characteristics is
that of Snow-Harter et alp 8l Young women were
randomly divided into 3 groups: those who trained
by running at least 3 times/week for 8 months,
those who weight trained 3 times/week for 8
months, and a control group which maintained
baseline activity patterns. The endurance trained
and strength trained groups showed similar signif-
icant increases in DEXA-measured lumbar spine
BMD of 1.6% and 1.3%, respectively, whereas that
of the control group did not change. It appears that
strength and endurance training are equally effec-
tive in stimulating increases in bone mass, al-
though the groups used in this study were relatively
small (10 runners and 12 weight trainers), again
raising the question of precision of measurements
needed to observe small treatment effects. More
studies, with larger sample sizes, are needed to
confirm these results.
In general, longitudinal studies show increases
in bone with exercise, but not nearly as much as
suggested by cross-sectional studies of athletes.
Future studies will have to involve better controls,
longer durations of training and larger groups of
participants, and should be directed at finding an
optimal exercise prescription for bone mass gains.
In studies performed with humans a final ques-
tion is, To what degree does BMD, by itself, deter-
mine bone strength? Although bone strength is
highly correlated to BMD,[2.3] other factors such as
bone size (cross-sectional area), shape (amount of
bone distributed away from the neutral axis of the
bone) and length, number of cement lines and col-
© Adis International Umited. All rights reserved.
113
lagen orientation contribute significantly to the
strength of boneP4.104] Future studies should take
these factors into account when determining the
effects of interventions on bone strength.
3. Effects of Loading on the
Remodelling Cycle of Bone
Bone is continually turning over (remodelling),
with specialised cells causing bone resorption (os-
teoclasts) and bone formation (osteoblasts). This
rate of turnover is determined by hormonal and
local factors. Parathyroid hormone is released in
response to a low serum calcium level and stimu-
lates the resorption of calcium from bone,l105] Cal-
citonin has the opposite effect, inhibiting osteo-
clastic resorption.l 105 ] Estrogen increases bone
formation by stimulating osteoblastic activity,
while an adequate level of calcitriol (vitamin D) is
necessary for proper calcification of bone.[106]
Local factors affecting rate of turnover involve
mechanical loading, which has beneficial effects
on bone formation. Lanyon[107] hypothesised that
any functional level of bone mass results from the
balance between mechanical drive towards forma-
tion and net hormonal drive towards resorption.
The remodelling cycle is made up of 5 stages -
quiescence, activation, resorption, reversal and
formation[ 108 l- and usually takes 4 to 6 months to
complete in the normal adult.l l09l Mechanical load-
ing can increase net bone formation by affecting
the various stages of this cycle.
3.1 Quiescence to Activation
Osteoclast activation is mainly under hormonal
(parathyroid hormone) influence. Activation in-
volves the recruitment of osteoclast precursors
(haematopoietic stem cells) from bone marrow.l 108 ]
These precursor cells are mononuclear and display
phagocytotic recognition of bone mineral
particles. [110] Once attached to the surface of bone,
they fuse to form multinucleated osteoclasts.l lll ]
Sports Med. 19 (2) 1995
114
3.2 Resorption
Once activated on the surface of bone, osteo-
clasts dissolve mineral while mononuclear cells,
which fail to fuse, digest collagen, forming a char-
acteristic cavity within the bone surface.[108]
3.3 Reversal
At a certain depth, resorption is halted, possibly
due to signals from osteocytes (bone cells within
the matrix, derived from osteoblasts) or lining
cells. [I II] Reversal involves the possible release of
a coupling factor (human skeletal growth fac-
tor),[112] which stimulates recruitment and prolifer-
ation of preosteoblasts from the bone marrow.
3.4 Formation
Osteoblasts secrete alkaline phosphatase, type I
collagen and bone Gla-protein (osteocalcin). [m-
ILS] Secreted collagen monomers polymerise,
forming collagen fibres. [105] Bone Gla-protein is
required for binding of calcium into calcium salts
called hydroxylapatite,[1I6] while alkaline phos-
phatase induces collagen fibres to deposit hydrox-
ylapatite.l 105 ] Serum alkaline phosphatase and
bone Gla-protein levels are often used as measures
of bone formation.[ll7] The cavity formed by re-
sorption is gradually filled by formation, and bone
then returns to the quiescent stage. Osteoblasts ei-
ther disappear, settle into the bone matrix and be-
come osteocytes or flatten out and become lining
cells, losing their ability to synthesise collagen.l 108]
3.5 Modifications of the Remodelling
Cycle with Loading
Frost[25] proposed that bone has a 'set-point' for
responses based on the amount of strain detected.
When bone experiences less than normal loads
(e.g. during immobilisation or weightlessness), the
decreased strain is detected and signals are sent out
to increase bone resorption. When bone is over-
loaded, the increased strain results in signals for
increased bone formation, and bone mass in-
creases. With increased loads, one of two situations
may arise: (i) the remodelling cycle may be shifted
© Adis International Limited, All rights reserved,
Chilibeck et a/.
in favour of formation, with either depression of
osteoclasts or enhanced stimulation of osteoblasts;
and (ii) bone formation may be activated from the
quiescent stage without intervening resorption.
Studies of animals and humans demonstrate that
the remodelling cycle is shifted in favour of forma-
tion: dogs subjected to loading exercise for 2 years
(by wearing weighted jackets),[1I8] and middle-
aged women or men who underwent 2 to 9 months
of muscular endurance,[1I9] strength[58] or weight-
bearing aerobicl 79 ] training, showed elevated se-
rum alkaline phosphatase and bone Gla-protein
levels (markers of osteoblastic activity and bone
formation). Cross-sectional studies show weight-
lifters to have higher serum bone Gla-protein levels
than non-weightlifters.l 120,12l] The use of serum al-
kaline phosphatase levels has been criticised since
they correlate poorly with bone formation rates as
determined by tetracycline labelling.l122] Serum
levels of alkaline phosphatase could be difficult to
interpret because multiple isoenzymes exist, de-
rived from the small intestine, kidneys and other
sources.[l23,124]
In response to loading, bone may be trans-
formed directly from the quiescent stage to forma-
tion. Osteocytes are probably the cells most suited
for detection of strain changes, since they are lo-
cated throughout the entire bone matrix, in a three-
dimensional interconnecting network.lI25 ] Os-
teocytes have gap junctions with osteoblasts and
lining cells, and may be involved in transmitting
proliferating or differentiation factors or other reg-
ulatory proteins to these cells.[126] Both in vitro and
in vivo studies have shown that within hours fol-
lowing strain, ribonucleic acid (RNA) or deoxyri-
bonucleic acid (DNA) synthesis (evidenced by in-
corporation of radiolabelled thymidine or uridine)
is increased in osteocytes and osteoblasts, indicat-
ing that protein synthesis and cell proliferation are
activated without preceding resorption.l 125-133 ]
Proteins synthesised by osteocytes could include
proliferation or differentiation factors which could
have direct effects on osteoblasts or lining cells,
when released. 1126] Osteoblasts show an increase in
the production of collagenous and noncollagenous
Sports Med, 19 (2) 1995
Exercise and Bone Mineral Density
proteins, [129.130.132) including osteonectin which is
involved in the induction of calcium phosphate de-
position on type I collagen.[l29.132) The immediate
increases in DNA and RNA activity in osteocytes
and osteoblasts indicate that formation may be di-
rectly activated in response to loading, bypassing
the other stages in the remodelling cycle.
4. Mechanisms for Transformation of
Mechanical Stimuli to Biochemical
Signals for New Bone Formation
A number of mechanisms have been proposed
for the transformation of mechanical stimuli into
biochemical signals for bone formation. These in-
clude prostaglandin release, piezoelectric and
streaming potentials, increased bone blood flow,
microdamage and hormonally mediated mecha-
nisms. It is possible that more than one mechanism
is involved, depending on the loading situation.
4.1 Prostaglandin Release
Prostaglandin release is implicated as a neces-
sary stage in bone formation with loading. When
external in vivo loading was imposed on rooster
ulnae with half the roosters receiving indometha-
cin (a prostaglandin inhibitor), the indomethacin
group had a significantly lower amount of acti-
vated osteoblasts than the regular loaded group,
when examined posthumously.ll3l) Since loading
was short term (1 day), prostaglandin release is
implicated in the early response of bone formation
to loading.
Prostaglandins of the E series administered to
rats[133) and dogS[134) for 30 days resulted in in-
creased mineral apposition rates, increased trabec-
ular and cortical bone formation (as evidenced by
fluorescent labelling upon sacrifice) and increased
serum levels of bone Gla-protein and alkaline
phosphatase, indicating osteoblast activation and
bone formation. Furthermore, prostaglandin E2
(PGE2; dinoprostone) added to rat bone tissue cul-
ture increases radiolabelled thymidine incorpora-
tion into DNA and radio labelled proline incorpo-
ration into collagen over a time period of 96
hours.l l35 ) These results mirror the effects of load-
© Adis International Limited. All rights reserved.
115
ing, and indirectly imply that PGE2 could be a me-
diator of bone formation with loading.
Following physical deformation of in vitro cul-
tured bone cells, PGE2, cyclic adenine monophos-
phate (cAMP) and radiolabelled thymidine incor-
poration into DNA all increase, but are blocked
when indomethacin is administered.[126.136) When
PGE 2 is added to cultures without deformation, the
stress-induced rise in cAMP and radiolabelled
thymidine incorporation is mimicked.[l36) This in-
dicates that PGE 2 may act to increase DNA levels
though cAMP regulation, when bones are subject
to strain. PGE 2 may act to enhance adenylate cy-
clase activity or inhibit phosphodiesterase activity,
to increase cAMP levels. cAMP may then act as a
second messenger to increase DN A levels and bone
cell proliferation.
Stress-induced increases in PGE2 and cAMP are
abolished when anti phospholipid antibodies are
administered to bone cell cultures.[l37) Anti-
phospholipid antibodies inhibit the reaction be-
tween cell membrane phospholipids and phos-
pholipase A2. It is proposed that when exposed to
phospholipase A2, membrane phospholipids re-
lease arachidonic acid which is a precursor to PGE2
synthesis. Addition of arachidonic acid or PGE2 to
the cultures in the presence of anti phospholipid an-
tibodies stimulate cAMP formation.
From these results, a mechanism is proposed for
PGE 2-mediated transformation of strain into bone
formation) 137) Strain causes stretching of bone cell
membranes. This may either cause membrane
phospholipid exposure to phopholipase A2 or in-
creased calcium influx, which could increase the
activity of membrane phospholipase A2. This
could cause the release of arachidonic acid from
membrane phospholipid, which then acts as a pre-
cursor for PGE 2 synthesis. PGE 2 activates adenyl-
ate cyclase or inhibits phophodiesterase, resulting
in increased intracellular levels of cAMP. cAMP
would then act as a second messenger to increase
DNA or RNA synthesis, resulting in bone cell dif-
ferentiation and proliferation, and the formation of
new bone.
Sports Med. 19 (2) 1995
116
While prostaglandin release is implicated as a
necessary stage in the formation of bone, some
studies have paradoxically found that prostaglan-
dins added to bone tissue in organ culture actually
stimulate osteoclastsJl38,139] One explanation in-
volves the osteoblastic control of osteoclasts.
It is hypothesised that osteoblasts can either in-
hibit osteoclasts, through prostaglandin releaser 140]
or stimulate osteoclasts through mineral expo-
sure. [III] When prostaglandins reach bone from an
external source (as occurs with prostaglandin addi-
tion to organ cultures), homeostasis is disturbed
and osteoblasts stimulate osteoclasts in an attempt
to preserve homeostasis.[l 40I
4.2 Piezoelectric and Streaming Potentials
Organic crystals, which lack a centre of sym-
metry, display the generation of an electrical po-
tential (separation of opposite charges) when de-
formed. 1141 ] Bone may be a piezoelectric substance,
since collagen and hydroxylapatite exist in a crys-
talline state, and the production of electrical poten-
tials upon the application of loads may be a mech-
anism which stimulates new bone formation.
Upon the application of stress to long bones in
vitro electrical fields are observed, with the com-
pression side of the bone displaying a negative
charge and the tensile side a positive charge.l142.144]
The amplitude of electrical potentials are depend-
ent on the rate and magnitude of strain.[142] When
strain gauges and electrodes are implanted in sheep
radius to record strain and electrical potentials in
vivo, strain magnitude and strain rate are related to
the amplitude of recorded electrical potentials dur-
ing fast locomotionJl45]
The piezoelectric effect (electric polarisation in
a substance resulting from application of mechan-
ical stress) is maximal with shear stresses and min-
imal when compressive or tensile stress is im-
posed.[I44] Shearing forces acting on collagen fibres
may cause them to slide past one another, resulting
in distortion of cross-linking bonds (most likely
hydrogen bonds) and production of electrical
charge separation. Electrical charge separation
may also occur with the bending of hyaluronic
© Adis International Limited. All rights reserved.
Chilibeck et al.
acid, a mucopolysaccharide, found in the ground
substance of boneJl46] Alternatively, charge sepa-
ration could result from bending at the junction of
collagen and hydroxylapatite (calcium salt) crys-
tals. When hydroxylapatite is removed from bone,
electrical potentials are greatly reducedJ I46 1
Most studies involving piezoelectric effects
have used dry bone. When bone exists in a physi-
ologically moist condition, fully hydrated collagen
may lose its piezoelectric property due to the struc-
tured water it contains, making the collagen mole-
cule more symmetricaJ.l147] Electrical charge sepa-
ration within stressed bone may be due to
'streaming potentials'. This occurs when strain
causes the movement of ions in a liquid, within
bone canals, past ions of opposite charge which
remain in a fixed position. Ions of one sign are
attracted to the channel walls, leaving the current
rich in ions of the opposite signJ147,148] When stud-
ies are performed in physiologically moist condi-
tions, in which the ionic composition of the fluid
forced through the bone under stress is changed, a
change in the voltage measured across the bone is
produced, indicating that streaming potentials
cause electrical charge separation.l 148] Streaming
potentials are affected by the velocity of fluid flow.
In experiments in which the viscosity of fluid flow-
ing through bone under stress is altered (resulting
in decreased velocity), the observed electrical po-
tential is reducedJl48] These 2 studies show that
electrical potentials are most likely to be due to
streaming potentials instead of a piezoelectric ef-
fect. Thus, streaming potentials appear to be the
dominant mechanism by which electric fields are
produced across stressed bone.
In vivo studies in which electrical stimulation is
applied to bone result in bone formation. When
electrical potentials were generated in dog femur
by the implantation of battery packs, bone forma-
tion was observed to occur around the negative
electrodeJl46] When mechanical stress or electrical
stimulation was applied to canine teeth in vivo,
straining intensity for osteoblasts was increased.
Following mechanical loading or electrical stimu-
lation, osteoblastic production of cAMP, cyclic
Sports Med. 19 (2) 1995
Exercise and Bone Mineral Density 117

guanosine monophosphate and PGE z were in- bone, and results in an increased surface area for
creased, indirectly implying that electrical poten- diffusion, allowing a greater amount of nutrients to
tial generation in response to stress may be involved be delivered to bone cells (osteocytes) responsible
in osteoblastic activation and bone formation. 1149] for release of growth and proliferative factors.l 153 ]
Several mechanisms are proposed by which
electrical potential generation in stressed bone may 4.4 Bone Formation in Response to
cause formation of new bone. Based on the obser- Microdamage
vation that a negative charge usually occurs on the
With repetitive loading, microcracks may ap-
bone surface under compressive strain, and that
pear within bone.l 154] Osteons (central canals
this surface usually shows the greatest amount of
within bone, surrounded by concentric lamellae)
new bone formation, it is proposed that free posi-
arrest and trap microcracks produced by cyclic
tively charged calcium ions may be attracted to
loading. The changes produced within the canal
the negatively charged surface and deposited
wall adjacent to the crack initiate the production of
there.l 143 ] Another proposed mechanism is that os-
a new secondary osteon (stimulation of remodell-
teocytes, which influence proliferation and differ-
ing). Osteoclasts remove damaged material so os-
entiation of osteoblasts and lining cells, through
teoblasts can deposit matrix and mineral along the
interconnections, may depend on nourishment,
paths of imposed stress,r155] The repair of damage
through fluid flow, to be activated. Osteocytes are
by secondary osteons may lead to the formation of
situated far from blood vessels within bone and are
new cortical bone. 1154] When damage is gradual ,
usually undernourished. Deformations, causing al-
bone mass increases. With a high rate of damage
ternating electrical signals, may act to pump fluid,
(from continuous repetitions), bone formation may
full of ions and charged molecules, through bone
not keep up and fracture may occur. When military
and allow delivery of nutrients to osteocytes.1 146]
recruits were subjected to 14 weeks of strenuous
Strain-induced flow of charged fluid may cause re-
training (8 hours a day, 6 days/week), BMD of the
orientation of proteoglycans.l 150] The core proteins
distal tibia increased by 7.5% (as measured by
of proteoglycans are either attached to, or penetrate
Compton scattering) with almost one-half of the
cell membranes. Reorientation of proteoglycans
recruits suffering stress fractures,r156] lending sup-
may alter membrane permeability, leading to al-
port to this proposed mechanism.
tered influx of ions, such as calcium. Calcium may
The major argument against the microdamage
activate enzymes, such as phospholipase A2, re-
theory is that functional adaptation can be pro-
sulting in the cascade of phospholipid release of
duced in bone in which strain magnitudes and cy-
arachidonic acid, PGE z production, increased ade-
cles are too low to produce microdamage. 1157 ] New
nylate synthase activity and increased cAMP pro-
bone formation via microdamage repair may take
duction, which could then act as a second messen-
place only at moderately high strains, and may act
ger to increase DNA or RNA content, resulting in
together with other bone forming mechanisms to
proliferation and differentiation of the bone
lay down new bone.
cell.l 149 ]
4.5 Hormonally Mediated Mechanisms
4.3 Bone Blood Flow
Although local strain related factors are most
Increased bone blood flow with exercise I151 ,152] likely to influence new bone formation, there is
is proposed as a mechanism by which bone forma- some evidence that altered hormone levels, as a
tion may increase. A significant correlation is result of heavy resistance exercise training, may
found between bone blood flow and endosteal new affect bone formation.
bone formation .[153] Increased blood flow could be Various weight training protocols result in in-
in response to increased metabolic demand within creased endogenous testosterone production, as

© Adis International Limited. All rights reseNed. Sports Med. 19 (2) 1995
118
measured from blood serum samples.[158) Human
osteoblast cells in vitro show increased levels of
radiolabelled thymidine incorporation into DNA
when dihydrotestosterone is added to the me-
dium.l 59) Osteoblasts may have androgen receptors
and may respond to resistance training-induced
testosterone increases by increasing the rate of
proliferation and formation of new bone.
In a cross-sectional study, weight-trained males
had greater levels of serum calcitriol (vitamin D)
than did control individuals.[l20) The endocrine
system may undergo some sort of modification in
response to resistance training. stimulates osteo-
blastic production of bone-Gla protein,[159) which
is required for the binding of calcium to hydroxyl-
apatite within bone,l"6) resulting in bone forma-
tion. Osteoblasts may have as well as testosterone
receptors, and may respond to exercised-induced
increases in these indices by laying down new
bone.
An argument against a systemic mechanism
arises when looking at cross-sectional unilateral
limb studies. The playing arm of tennis players has
significantly greater bone mineral than the non-
playing arm,[160,161] and this difference is greater
than the difference between dominant and non-
dominant arms in normal populations,[162] suggest-
ing that strain acts through local effects.
5. Conclusions
Studies of animals demonstrate that bone mass
and strength is substantially increased with exer-
cise; increases tend to be more pronounced in
young animals. On the other hand, exercise train-
ing studies in humans show rather small changes
in BMD. The strain characteristics which result in
optimal bone formation in animals imply that both
strength and high impact endurance-type training
may be effective in enhancing bone mass. Cross-
sectional studies of athletes favour strength over
endurance type training; however, selection of spe-
cific elite groups, and higher body mass and steroid
usage in weightlifters may bias these findings. In
normal populations, strength and muscle mass tend
to have better correlations with bone mass than
© Adis International Limited. All rights reseNed.
Chilibeck et al.
does aerobic fitness. Longitudinal studies involv-
ing resistance or endurance training have resulted
in similar gains in bone mass, but less than would
be expected from the results of cross-sectional
studies. Longer training studies with larger sample
sizes are needed to detect small changes expected
in bone, and for the formulation of an optimal ex-
ercise prescription. Prostaglandin release, piezo-
electric and streaming potentials, increased bone
blood flow, microdamage and increased hormone
release are some of the proposed mechanisms for
the induction of signals for new bone formation,
following alterations in strain.
References
I. Martin AD, Silverthorn KG, Houstyon CS, et at. Trends in frac-
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