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Notes
Review
A B
380 Rutherford
both trabecular and cortical bone, and it is the values: the most benefit is likely to be achieved
former that may be more informative. Dual in those with the lowest initial BMD. For this
energy computerised tomography (CT) does reason it is extremely important that the
give a true volumetric density, and trabecular control and exercise groups are matched for
bone in the vertebrae can be isolated from the BMD before intervention. (e) Principle of
cortical shell. CT is, however, expensive, not diminishing returns: individuals appear to have
widely available, and has a high radiation dose, a biological/genetic ceiling that determines the
and for these reasons is not commonly used for extent of improvement. As training progresses,
measurement of bone density. Any radio- this ceiling may be reached, and gains in BMD
graphic technique needs to have a very high will slow and eventually plateau. Many of the
accuracy and precision. Changes to bone occur intervention studies are too short for this to be
slowly, and after one year of treatment the clearly observed.
increases can be in the region of only 1–2%. In
the future, magnetic resonance imaging may Cross sectional studies
provide a valuable tool for looking at the struc- Some of the strongest evidence that exercise
ture of bone which may be more informative can increase BMD comes from studies on
about bone strength than density alone. highly athletic groups. Comparisons have been
Other non-radiographic methods for moni- made between the bone density of skeletal sites
toring the impact of treatment on bone include in diVerent types of athletes and sedentary
blood and urinary markers of bone turnover controls. Nilsson and Westlin18 measured
(for a review see Calvo et al13). Current markers femoral bone density of male athletes including
of bone formation include bone specific weight lifters, throwers, runners, soccer play-
alkaline phosphatase and osteocalcin. Bone ers, swimmers, active non-athletes, and seden-
resorption can be assessed from breakdown tary men. Bone density varied with the amount
products of type I collagen such as deoxy- and extent of loading placed on the femur, with
pyridinoline and the telopeptides. In post- the greatest density occurring in the weight
menopausal women, bone turnover, particu- lifters and lowest in the sedentary group. This
larly resorption, is very high. These markers are pattern was reflected in leg muscle strength.
used widely for monitoring antiresorptive Similar studies have been carried out in
treatment such as HRT and bisphosphonates women. Heinonen et al19 showed that bone
but have been less commonly used in exercise density of the hip and spine exhibited a
intervention trials. As these markers are stepwise pattern in female athletes, with the
susceptible to circadian, menstrual, and sea- largest in squash players followed by aerobics
sonal rhythms, care needs to be taken when participants, speed skaters, and sedentary con-
choosing sampling times. trols. The importance of impact loading was
shown by Fehling et al20 who compared
Exercise and fractures regional BMD in female athletes participating
The evidence that exercise may have a role to in impact loading sports (volleyball and
play in reducing fractures comes from both gymnastics) with that in women participating
cross sectional and longitudinal studies. Many in active loading sports (swimming) and
studies have been carried out and it is beyond sedentary controls. The impact loading groups
the scope of this review to include them all. had high BMDs at most skeletal sites whereas
Rather, key examples will be used to highlight there were no significant diVerences at any site
the eVectiveness of a particular type of exercise between the swimmers and controls (fig 2).
or eVects at specific fracture sites. There are a The criticism about such comparative stud-
number of excellent reviews on this subject in ies is that the high bone density may simply
the literature.14–17 The term exercise covers reflect a genetically determined strong
many forms of activity. These can be broadly musculoskeletal system which favours the par-
divided into endurance training, strength/ ticipation of these women in high level sports
resistance training, high impact work, walking, rather than the training itself leading to an
and aerobics/keep fit classes. Much of the
initial work aimed at improving BMD concen- Volleyball
trated on the types of endurance activity that Gymnastics
had been shown to be beneficial for cardiovas- Swimming
cular health. We are increasingly becoming 18
aware that the same type of exercise may not be 16
optimal for bone health or reduction of falls. 14
However, some of the basic principles of train- 12
% Difference
increase in BMD. An argument against this have significant eVects on bone density at the
comes from studies of asymmetric activities, spine and hip. It has been diYcult to isolate the
such as tennis, where the playing arm has a type of exercise that places suYcient strain
larger bone mass than the non-playing arm.21 magnitude and of novel distribution to alter
The diVerences observed in bone density significantly bone turnover and remodelling,
between athletes and non-athletes can be large particularly in older age groups.
(10–15%), and are often much greater than the
changes measured as a result of prospective WALKING
exercise intervention studies. There are several One of the simplest and most accessible forms
possible explanations for these observations: of exercise is walking. Unfortunately the avail-
(a) high levels of activity early in life may be able evidence suggests that this form of activity
more beneficial than activity adopted later; (b) is insuYcient to improve BMD at the spine or
the intervention studies are often of much hip. It should be noted, however, that the sub-
shorter duration than the training history of the jects included in the studies have largely been
athletes; (c) the athletes may have a genetic fairly active, ambulant, and healthy. It has yet to
advantage in that their response to training is be shown whether more inactive frail groups
greater than that of many sedentary people. would show a more positive response. A one
Not all athletic groups, however, show benefi- year study of treadmill walking at 70–85% of
cial eVects on bone and this will be discussed maximum heart rate together with calcium
below. supplementation found no eVect at the spine or
forearm in postmenopausal women26 despite
Exercise intervention significant improvements in aerobic capacity.
In order to show conclusively that exercise can In recently menopausal women, walking did
slow bone loss or cause bone accretion, it is appear to attenuate the loss of bone at the spine
necessary to perform longitudinal randomised when compared with controls. Nelson et al27
intervention studies in the population of inter- compared supervised walking and either mod-
est. Problems arise when trying to compare erate or high calcium diet on BMD of the spine
such studies as there are large variations in the and hip. The spine, but not the hip, showed a
type, intensity, and duration of the training. moderate improvement independent of cal-
Additional confounding factors include wide cium intake. A similar exercise regimen, but
diVerences in the age range of subjects, with no dietary supplementation, showed no
concurrent treatments, calcium supplementa- eVect on trabecular bone density in the spine.28
tion, and skeletal sites investigated. Precise In a seven month trial, Hatori et al29 compared
details of the exercises carried out are often walking above (high intensity) or below (low
scanty or missing. Despite these problems, we intensity) the anaerobic threshold on spine
are beginning to understand more about the BMD. The moderate intensity group showed a
types of activities that can provide benefits for similar loss of bone to the controls, whereas the
diVerent skeletal sites. As yet we are not in a high intensity group showed a small improve-
position to give definitive recommendations for ment. Although the results are encouraging, it
the optimal type of exercise for the prevention is unlikely that women would naturally adopt
of osteoporosis. Recently guidelines have been such an intense walking pace without continu-
produced for physiotherapists dealing with ous encouragement. Although walking does
patients either at risk of osteoporosis or with not appear to be particularly beneficial for bone
diagnosed osteoporosis,22 and the National health in the groups studied, it may have other
Osteoporosis Society has produced a booklet benefits that could reduce the risk of fractures
giving advice on exercises that could help pre- and should not be dismissed as an important
vent osteoporosis.23 Both publications are activity for many other aspects of health.
based on the findings of research studies.
LOW INTENSITY REPETITIVE EXERCISE
Strengthening the wrist Many studies have investigated exercise regi-
The Colle’s fracture of the wrist is one of the mens based on those recommended for train-
first injuries to show an increase after the ing of the cardiovascular system; these have
menopause. Because of its accessibility, the mainly involved some form of repetitive low
wrist is one of the sites that responds well to force activity such as general keep fit classes. In
training, as long as the regimen is tailored to one of the earliest studies, Krolner et al30 com-
load the forearm. Squeezing a tennis ball for 30 pared the eVect of an eight month varied
seconds a day for six weeks showed significant programme of walking, running, floor exer-
benefits in the non-injured forearm of women cises, and ball games on the spine and forearm
who had already sustained a Colle’s fracture.24 bone mineral content (BMC) with an age
Alternatively resisted exercise involving twist- matched non-exercising control group. The
ing, compression, and bending resulted in exercise groups had a small (3.5%), but signifi-
increases averaging 3.8%.25 More general keep cant, increase in BMC of the lumbar spine
fit and dance classes often fail to show benefits when compared with the decrease in the
at the radius simply because the exercises were control group. No eVect was seen at the
not tailored to stress that site. forearm, probably because of a lack of loading
at this site from this form of activity. The
Increasing the bone density at the spine women were postmenopausal and had previ-
and hip ously had a Colle’s fracture. Chow et al31
More challenging to the researchers has been carried out a similar training programme but
defining the optimal form of exercise that can included an additional group in which light
Downloaded from bjsm.bmjjournals.com on 15 August 2005
382 Rutherford
weights were attached to the wrists and ankles BMD of several regions on the hip: the
during the exercise classes. They measured trochanter, intratrochanteric area, and Ward’s
total body calcium and this was improved in triangle. They found no eVect at the neck of
both exercise groups when compared with femur and no eVect of low intensity (endurance)
controls, but the group performing with the strength training. Their population were all
weights showed no additional benefit. The postmenopausal and ranged in age from 40 to
measurement technique was unable to detect 70 years. Both types of exercise improved
any site specific eVect. muscle strength to a similar extent, and these
In a more complex study design, Dalsky et improvements correlated with the bone changes
al32 carried out a study in which the training at several sites in the high intensity group.
included walking, running, and stair climbing Nelson et al38 also found small, but significant,
in women aged 55–70. Calcium supplements eVects of a one year high intensity strength
were given at a dose of 1500 mg/day regardless training regimen on BMD of the spine, hip, and
of dietary intake and subjects were randomly total body in 50–70 year old women. In
divided into exercise and non-exercise groups. addition, there was a significant improvement in
In the first stage of the study, exercise was car- muscle strength, muscle mass, and balance, all
ried out for nine months. Some subjects in the of which are implicated in fall risk.
exercise group then stopped training and the As with much of the literature in this field it
others continued to train for a further 13 is diYcult to reconcile the diVerent results
months. After this second training phase, the from similar regimens in seemingly similar
exercise was stopped and subjects were fol- populations. The overall message, however, is
lowed up after a further 12 month detraining that, at least for the spine, strength training can
period. After the first study period the exercise be eVective but has no added benefit for BMD
group had a significant increase of 6% in spine over the more endurance based regimens. The
BMC. After the second phase the exercise added benefit of increased muscle strength
maintained this increase but did not improve it may, in the longer term, result in a greater
further. Those that had stopped training had eVect on fracture risk. As yet this has not been
returned to their baseline BMC. This study assessed and most of the studies only last one
highlights many aspects outlined in the general year; a much longer follow up would be
principles for training discussed above. Firstly, required to determine eVects on the incidence
within the exercise group some did not benefit of falls and fractures.
from exercise and carried on losing bone while
others had very large increases of up to 15%. HIGH IMPACT EXERCISE
This could be due to diVerent intensities of Many of the studies so far discussed have been
training, diVerences in initial BMC, or diVer- ineVective at increasing BMD at the hip. As
ences in genetic potential to respond to this is the most serious fracture site, it is
training. As with any intervention treatments, it essential that safe, aVordable, and accessible
highlights the need to monitor response and exercise is defined. One of the first studies to
not assume that every person will respond be eVective at this site was by Bassey and
positively. Secondly, it demonstrates the pla- Ramsdale39 in which they used jumping to
teau eVect in that the response was maintained impart high impact forces to the hip in
but not increased in the second training phase. premenopausal women. After six months there
Thirdly, the results show that once exercise is was a significant increase of 3.4% at the
stopped, the normal bone loss continues and greater trochanter, but no other site at the hip
the benefits are not maintained. and no change at the spine. Initially they
modified the exercise before extending it to an
STRENGTH TRAINING older age group (50–60 years) and instead of
In the 1990s attention switched to the study of jumping the women carried out heel drops.40
strength training. The rationale was based on After one year no eVect was seen at any skeletal
findings from animal studies.33 34 These investi- site and the study was then repeated using
gated in detail the type of mechanical strains that jumps.41 Again, no eVect was seen, so the older
could maximise the osteogenic response. The women were showing a diVerent response to
greatest eVects were seen when the magnitude the younger group, which may be related to the
and rate of strain was high, but required few oestrogen status of the subjects although those
repetitions, and when the strain was novel in on HRT had a similar response to non-HRT
magnitude or direction. The human equivalent users.
of this type of strain exposure is strength, as In the light of the initial encouraging findings
opposed to endurance, training. Pruitt et al35 36 of Bassey and Ramsdale39 in the premenopau-
conducted two studies on strength training, one sal women, another study incorporated jump-
in early postmenopausal women and one in ing, stepping, marching, and side stepping into
women over 65. In the first study on the younger an exercise class designed specifically for the
women, there was a significant eVect of training over 50s.42 The study involved both postmeno-
at the lumbar spine averaging 1.6%, but no pausal women and men over 50, none of whom
eVect at the hip or forearm. In the second study were on calcium or HRT. After one year there
on the older women, they compared high and were significant increases in hip, but not spine,
low intensity strength training. Despite improve- BMD. The increases were in the range
ments in strength in both exercise groups, there 1.6–2.2% depending on the site on the hip.
was no eVect on BMD at either the spine or hip Some of the subjects continued for a second
for either group. Conversely Kerr et al37 did find year in which the spine BMD increased signifi-
an eVect of high intensity strength training on cantly and the changes in hip BMD were
Downloaded from bjsm.bmjjournals.com on 15 August 2005
maintained. This type of exercise also com- eVects were not seen in the other two groups.
pletely reversed the age related loss of muscle In the follow up period, those women taking
strength, with the training group increasing HRT maintained or further increased BMD,
quadriceps strength by 10% and the matched the eVect being greater in those who exercised.
controls decreasing it by the same amount. Hip Some of the improvements were maintained in
and shoulder flexibility also improved as a those in the exercise alone group. These results
result of the training. Urinary excretion of show that, in the oestrogen replete state, older
pyridinoline and deoxypyridinoline were women show a greater response to exercise. In
measured to assess the impact of the exercise addition, exercise had additional benefits
on bone resorption. Both markers significantly which could help reduce the risk of falls.
decreased during the first six months of Further studies are required to investigate the
exercise and then returned to baseline values. interaction of exercise and other treatment
This suggests that the exercise was suppressing options such as the bisphosphonates.
osteoclastic bone resorption. Similar findings
on the response to high impact work have been Exercise and fall prevention
obtained in younger subjects.43 These studies Certain forms of exercise have been recognised
lend support to the idea of high impact work as an integral part of multifactorial interven-
being a good osteogenic stimulus at the hip. tion programmes for the reduction of falls.
Extreme caution needs to be observed, how- Despite the recognition of the importance of
ever, when recommending this form of exercise exercise, there are no specific guidelines on falls
for a frail population. High impact work would management exercises for the older person.
be contraindicated for those with impaired bal- Many of the studies that have looked at the
ance, osteoporosis/osteopenia, osteoarthritis in impact of exercise on falls have had inherent
load bearing joints, or artificial joints. Even in design faults. Many have relied on subject’s
relatively healthy older subjects, the exercises recall to document the number of falls in the
should only be introduced gradually into preceding year, and in an elderly population
classes after an initial progressive skill specific this may be very inaccurate. Others have
training period to allow soft tissue adaptation included subjects with no history of falling, and
and the requisite safe technique to be learnt. it is therefore not surprising that a reduction in
falls was not observed. Several trials have used
Exercise and HRT exercise of insuYcient intensity or duration to
Many of the studies discussed have used eVect meaningful adaptations, and often the
calcium supplementation to bring subjects up exercises are not targeted specifically at the
to the recommended daily allowance. Less well factors that increase the risk of falls. Some of
studied has been the interaction between HRT the key risk factors are poor gait, balance, mus-
and exercise. Several studies have shown that in cle strength, and confidence. In a one year
the oestrogen replete sate, the response to home based study, Campbell et al45 found a
training is greater. In the most comprehensive reduction of 20–30% in falls in women over 80.
study to date, Kohrt et al44 compared four Each subject was prescribed a particular set of
groups of women aged 60–72 years. The first home exercises by a physiotherapist and were
acted as a control, the second took HRT, the regularly contacted by phone to monitor
third exercised, and the fourth took HRT and progress and maintain motivation. Another
exercised. Variables studied were bone density successful intervention was Tai Chi,46 which
of the spine, hip, and total body, bone resulted in a halving of falls.
formation (osteocalcin), body composition, Recently a falls management exercise pro-
muscle strength, and estimated VO2MAX. The gramme47 was specifically designed to provide
exercise programme involved two months of practitioners with a framework of specific
flexibility exercises followed by nine months of tailored progressive exercise guidelines which
walking, jogging, and stair climbing/ascending. could be adapted to suit older people with a
Calcium intake was adjusted to about 1500 wide range of abilities. The activities include
mg/day. After the initial 11 months, there was a three dimensional Tai Chi based movement
six month follow up phase in which those on patterns, targeted strengthening and stretching
HRT remained on treatment. Women in exer- exercises, dynamic postural and gait training,
cise groups were encouraged to continue exer- and functional floor and standing activities to
cising but most reduced both the number of improve neuromuscular skill and confidence.
exercise sessions and intensity during this In addition to supervised classes, the subjects
phase. Both the exercise and HRT alone are also encouraged to do home based exercise
brought about increases in BMD of the total aided by an exercise booklet. The women are
body, spine, neck of femur, and Ward’s also taught how to get up from the floor after a
triangle. HRT plus exercise increased BMD at fall and are encouraged to wear hip protector
all sites measured (spine, hip, total body) and pads in the classes. The eVectiveness of this
was more eVective than HRT alone in increas- regimen in reducing falls is currently being
ing BMD at the spine and total body and more assessed in a group of frequent fallers. In addi-
eVective than exercise alone at the total body, tion to falls, the other measurement outcomes
spine, and trochanter. Serum osteocalcin was of the study include lower limb muscle strength
reduced in both groups taking HRT but in no and power, functional ability, reaction time,
other group. HRT is known to be antiresorptive balance, and bone density. Examination of the
and reduce bone turnover. Both exercise baseline data has disclosed that there can be
groups had improvements in lean tissue mass considerable lower limb asymmetry in strength
and VO2MAX and reductions in fat mass; these and power in frequent fallers; this is particu-
384
% Difference
15
10
–5
–10
Spine
Controls
Eumenorrhoeic
Amenorrhoeic
Neck of femur
Total body
Figure 3 Percentage diVerence between bone mineral
density of the spine, neck of femur, and total body for
sedentary controls and athletic groups (eumenorrhoeic and
amenorrhoeic) compared with predicted age matched data
from the Lunar database. Redrawn from Stacey et al57 and
the author’s data.
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