The effects of physical activity can be separated into five research categories: (a) cross-sectional studies, (b) intervention studies, (c) muscle mass, muscle strength and BMD, (d) cardiorespiratory fitness and BMD and (e) reproductive endocrine status and physical fitness .
Comparisons of active and sedentary populations at single points in time generally lend strong support to the notion that a positive relationship exists between activity and bone density . Athletes, tennis players and experienced runners have higher bone density than non-active controls and demonstrate specificity of bone mass accretion in relation to activity mode. Bone mineral content of the radius was higher in tennis players and swimmers, and lumbar spine density was higher only in tennis players, indicating the potential role of weight-bearing activities in bone mass accretion [35, 54].
With regard to the importance of weight bearing to the skeleton, some studies suggest that loads other than those generated by gravity, such as muscular pulling, actively stimulate bone deposition. Davee et al.  found that young women who supplemented aerobic exercise training of only 1 h per week had higher spine densities than women who were sedentary or participated in aerobic exercises only. Additionally, Orwoll et al.  reported that radial and vertebral BMD were higher among men who swam regularly than non-exercising men, suggesting that although swimming is considered a non-weight-bearing exercise activity, its contribution to BMD may occur through loads created from high intensity muscular activity. The resistance offered by the water constitutes the stimulus that increases muscular activity.
With regard to the elderly, it is important to emphasise that not only is bone density higher in physically active people, which can be very significant when trying to prevent osteoporosis by increasing peak bone mass, but also the literature suggests that increased activity may be associated with a lower rate of age-related bone loss . Thus, a comparison of older athletic women with younger athletic women who exercise at least three times a week, 8 or more months of the year, for a minimum of 3 years, showed that middle radius and lumbar spine values for the older women were similar to those of the younger athletic women. During this period, the control group formed by women older than 50 showed an annual decrease of 0.7% in spine density . Other studies have also found a relationship between muscular strength, physical fitness and body weight but not in postmenopausal women (see below).
Intervention studies investigate the effects of an imposed exercise programme on BMD. In several studies, postmenopausal women who performed callisthenics and light aerobic exercise three times a week for 30–50 min per session during 8 to 48 months [41, 69–71] showed significant changes in lumbar spine and total body calcium even in a period of less than 12 months. No significant changes in bone mineral content of the radius were observed . However, despite the fact that the majority of programmes that affect BMD in the spine and lower limbs imply exercises like walking or weight-bearing aerobic activities, differences have been observed in the wrist and in the distal part of the forearm (radius). Similarly, some studies have found that BMD was favourably affected by programmes that included muscle-conditioning exercises with weights for the upper body but not for those that used only weight-bearing activities .
Smith et al.  present some data that can help us to interpret the differential effects of exercise programmes on different areas of the skeleton. It seems logical that for a particular zone to be affected, it should be exposed to stimuli that produce a specific effect on it. These authors studied 200 women varying in age from 35 to 65, of whom 80 carried out a specific training programme and 120 served as a control group. The duration of the exercise programme was 36 months. Results demonstrated a significant decline in bone mass in the exercise group during the first year, followed by increases in radial densities over the following 24 months. However, the observed increases did not make up for the loss during the first year. The study was extended to 48 months after reporting that the data for the first year were not reliable because of problems with equipment quality control. Data for the third year showed that loss rates of the radius and ulna significantly decreased in the exercise group compared to the controls. On examination of the exercise programme, it is interesting to note that in the first year, the programme consisted of weight-bearing activities, whereas during successive years, additional emphasis was placed on upper body strength .
The site selected to show the changes is an important issue. For example, changes have not been observed in the density of the forearm of postmenopausal women after carrying out weight-bearing activities . Significant increases were shown in the calcaneus of a group of women runners after a 9-month programme . After performing a combination of bending, loading compression and torsion exercises designed to load wrist and forearm, the postmenopausal exercise group had a significant increase in forearm bone density (3.8%) after following the programme three times a week for 5 months . Another interesting aspect that emerged when studying the exercise programme, which included trunk extension exercises, was its effect on vertebral fractures. The group that carried out this programme suffered fewer fractures than the one which carried out flexions. A possible explanation is that extension exercises strengthen the back but flexion exercises do not .
Another aspect that is important for obtaining benefits from physical training is progression. To improve physical capacity, physiological overload must be maintained. Therefore, it is important to progress in training, i.e. we should increment the weight that is moved or, in this case worn, to maintain the stimulus to realise additional benefits. In this case, wearing a weighted vest would be a way to apply the training principle of progressively incrementing the physiological overload to provide a stronger stimulus than just walking. Snow et al.  found this procedure to be an effective system, and in a long-term study, the procedure prevented hip bone loss in postmenopausal women.
It has already been pointed out that weight-bearing exercise programmes are generally recommended, but certain studies indicate that resistance exercises can be more powerful for promoting bone accretion because of the different forces produced at the lumbar vertebrae level. For example, in comparing fast walking with jogging, the forces were 1 and 1.75 times body weight, respectively. On the other hand, during weight training exercises defined as non-weight-bearing activity, the load on the lumbar vertebrae can be as high as five to six times body weight .
High-impact exercises are another way to impose a higher intensity load on bone and can be utilised for stimulus progression to facilitate greater adaptation. In a randomised, controlled trial involving 98 healthy, sedentary, 35- to 45-year-old women, those who participated in 18 months of three weekly sessions of progressive high-impact training had significantly greater increases in femoral neck BMD than sedentary controls (+1.6% vs −0.2%, respectively) . Just as noted, impact intensity has been used to explain the differences found between female gymnasts and swimmers and controls after a 12-month programme. If done regularly, these type of exercises can help to reduce the risk of future fractures, as they facilitate the accretion of bone mass .
Muscle mass, muscle strength and bone mineral density
We should not forget that the skeleton is a dynamic tissue, so it is not surprising that through its connections with muscle, it exhibits changes similar to those observed in muscle. Sarcopaenia, the age-related loss of muscle, inhibits mobility, increasing the risk for developing many diseases including diabetes, arthritis, heart disease and, what it is important in the context of this review, osteoporosis . It increases the risk of weakness, functional decline, impaired gait, falls, infections, glucose intolerance and osteoporotic fractures. Sarcopaenia is linked to osteoporotic problems and for this reason has also been treated in the context of osteoporosis.
The estimated loss of bone from its peak in young adulthood to 80 years of age is comparable to the reported 35–45% decline in muscle strength during the same lifespan . Several authors have studied the relationship between BMD and muscle strength, which depends to a large extent on muscle mass. Significant correlations have been found between different parameters of muscle mass and bone density and between vertebral ash weight and psoas muscle weight in 46 routine autopsies, which suggests a relationship between the strength of a specific muscle group and the corresponding bone [1, 21, 64–66]. Some studies do not find this relationship significant. Sinaki et al. , for example, did not find significant changes in BMD of the spine after a 2-year exercise programme that entailed non-weight-bearing activities but increased the isometric strength of the back. However, this could be attributed to the fact that the type of programme used loads to improve muscular resistance but not strength, and the magnitude of the load may not have been sufficient to achieve the necessary stimulus to provoke adaptation.
The effect of muscular activity on BMD has been assumed to be site specific. However, other aspects make this statement a little more complex. Pocock et al.  evaluated pre- and post-menopausal women on the strength of biceps brachii and quadriceps group, and BMD of the spine and proximal femur. They found biceps strength but not quadriceps strength to be a predictor of BMD at the spine and three regional sites on the proximal femur. For this population, muscle strength better explained the variance in BMD than age. Snow et al. have found similar results as well [73, 74]. It can be concluded that in some cases, the relationship between strength and BMD are specific. In other cases, however, muscle groups more distal to the spine and proximal femur significantly contribute to bone density. A possible explanation of this relationship may be that arm activity is linked to the simultaneous contraction of trunk-stabilizing muscles that directly exert forces on the hip and spine. Moreover, the length of the lever arm between arm muscles and the spine is considerably greater than that between back extensors and the spine, so that when lifting the same weight, loads on axial bone generated by arm activity exceed those generated by back extensors [45, 73].
Fiatarone et al.  have shown how progressive resistance training is feasible, safe and effective in a variety of settings such as nursing homes, chronic hospitals, outpatient clinics, continuing care communities and individual homes with elderly people even of a very advanced age (nonagenarians). Several studies have shown that progressive resistance training may lead to muscle hypertrophy, whereas cardiovascular endurance training does not in general improve either muscle strength or mass. The injury rate with appropriate exercises is very low, and very few medical conditions are incompatible with its usage. The benefits observed with these programmes include improvements in muscle strength, muscle mass, gait speed, balance, stair climbing ability, overall physical activity levels, functional status, morale, depression, sleep and nutritional intake. Muscle biopsy samples indicate activation of satellite cells and myogenic precursor appearance, as well as expression of developmental myosin and insulin-like growth factor I (IGF-I), all indicative of the plasticity and remodelling of the skeletal muscle.
There is evidence that high-intensity resistance training promotes bone maintenance in older women. High intensity can be applied using several weight machines that support the spine. People can then perform exercises in a sitting position with support for the back or use free weights in which muscles need to stabilise the body to maintain posture. Maddalozzo and Snow  compared the effects of a moderate seated resistance-training programme with high-intensity standing programmes on bone mass and serum levels of IGF-I and insulin-like growth factor binding protein 3 (IGFBP3) in healthy older men and women (54.6 ± 3.2 and 52.8 ±3.3 years, respectively). High-intensity training resulted in spinal BMD gain in men (1.9%, p < 0.05) but not in women. Moderate programmes produced no changes in either gender at this site. Increases were observed in the greater trochanter in men regardless of training intensity but not in women. Both men and women in the high-intensity group improved in trochanteric BMD. Both programmes improved total body strength (37.63%) and lean body mass (men 4.1%, women 3.1%). Neither circulating serum IGF-I nor IGFBP3 was altered by either training regimen. The authors concluded that although resistance training of moderate to high intensity produced similar muscle changes in older adults, a higher magnitude is necessary to stimulate osteogenesis at the spine. However, at the spine, intensity was not sufficient to offset low levels of oestrogen in early postmenopausal women, and bone changes were not accompanied by changes in circulating serum levels of IGF-I or IGFBP3.
Tissue plasticity or the ability to regenerate after stress has been a subject of investigation in ageing humans. Fiatarone et al.  explored the effects of a 10-week progressive resistance-training programme on muscle plasticity in frail elders, aged 72–98 years. Post-muscle biopsy specimens showed an increased appearance of IGF-I and regeneration potential from baseline atrophy. The 257% increase in strength after resistance training was associated with a 141% increase in ultrastructural damage and a 491% increase in IGF-I immunofluorescence staining. Because the IGF-I receptor plays a dominant role in muscle IGF-I signalling, the authors speculated that this increase in IGF-I receptor numbers together with markers of muscle damage and regeneration may expand existing knowledge regarding the IGF-I response to exercise stress in older adults. Later, Urso et al.  assessed the impact of 10 weeks of resistance training on markers of skeletal muscle plasticity and IGF-I receptor density in a sub-sample of subjects who in an earlier study had demonstrated enhanced immuno-histochemical labelling of IGF after resistance training. The experimental subjects showed a 161 ± 93.7% increase in Z band damage after resistance training. Myofibrillar central nuclei increased 296 ±120% (p = 0.029) in the experimental subjects. Changes in the percentage of damaged Z bands were associated with alterations in the presence of central nuclei (r = 0.668, p = 0.034). Post-hoc analysis revealed that the relative pre–post percentage changes in myofibrillar Z band damage and central nuclei were not statistically different between the control and exercise groups. Exercise training increased myofibril IGF-I receptor densities in the exercise subjects (p = 0.008), with a non-significant increase in the control group. The authors remarked that the labelling patterns suggested enhanced receptor density around the Z bands, sarcolemma and mitochondrial and nuclear membranes. Furthermore, these findings suggest that the age-related down-regulation of the skeletal muscle IGF-I system may be reversed to some extent with progressive resistance training and that skeletal muscle tissue plasticity in the frail elderly is maintained at least to some extent, as exemplified by the enhancement of IGF-I receptor density and markers of tissue regeneration .
Cardiovascular fitness and bone mineral density
Some studies have found a significant relationship between cardiovascular fitness and bone density [15, 55], while others have found no differences between active groups and sedentary groups [7, 8, 18, 30, 52]. The relationship of cardiovascular fitness to BMD is probably due to the weight-bearing stimulation that activity itself provides to the skeleton.
Reproductive endocrine status and physical training
It is now recognised that despite the beneficial effects of weight-bearing exercise (and probably resistance training) on BMD, severe and excessive exercise training together with deficient nutrition attributable to eating disorders may interrupt menstrual function and lead to bone loss and increased fracture risk [12, 22, 48]. This condition has become known as the ‘female athlete triad syndrome’ and is characterised by disordered eating, amenorrhea and osteoporosis. The loss of menstrual function has been clearly associated with a consistent decrease in trabecular bone despite apparent preservation of normal cortical bone density. Fortunately, reports indicate that although serious depletion of bone mass can occur in the amenorrheic athlete, a portion of this loss is potentially reversible . It should be noted as well that in spite of often being amenorrheic, gymnasts demonstrate an exception to this rule; they typically have very dense bones. The large discrepancy in magnitude of the forces placed on the skeleton during different activities can explain the differences from other highly trained athletes, as much higher impact forces are generated in gymnastics . However, it should be emphasised that in the case of women, excessive exercise can be contraindicated, as the hypo-oestrogenism associated with athletic amenorrhoea can lead to a loss of bone mass . In the same way, it is advisable to underscore that today’s high incidence of cases of anorexia nervosa is a certain source of future problems.
To summarise, although results from cross-sectional analysis support a positive effect of exercise on BMD, results from longitudinal studies provide mixed outcomes. These results vary with the mode, duration, intensity and frequency of exercise. Most of the studies have used weight-bearing activities (walking, jogging, running, dancing) as the exercise intervention. However, when the programmes have been more intense, of longer duration or included exercises that overloaded the muscular system, a better osteogenic stimulus has been observed.