Physical Activity in the Prevention and Amelioration of Osteoporosis in Women Interaction of Mechanical, Hormonal and Dietary Factors

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1 Sports Med 2005; 35 (9): REVIEW ARTICLE /05/ /$34.95/ Adis Data Information BV. All rights reserved. Physical Activity in the Prevention and Amelioration of Osteoporosis in Women Interaction of Mechanical, Hormonal and Dietary Factors Katarina T. Borer Division of Kinesiology, The University of Michigan, Ann Arbor, Michigan, USA Contents Abstract Mechanical Characteristics of Bones Bone Morphology Methodological and Study Design Issues Mechanical Properties of Bones Properties of Bones Contributing to the Risk of Fractures Prevention of Osteoporosis Through Accumulation of Peak Bone Mass Bone Growth: Increases in Length, Width and Mass Longitudinal Bone Growth Bone Growth in Width and Thickness Accumulation of Bone Mineral Bone Growth: Endocrine Influences Messengers that Influence Bone Cell Proliferation Messengers that Influence Bone Cell Differentiation Bone Growth: Dietary Influences The Role of Energy Availability in Bone Growth and Mass The Role of Specific Nutrients in Bone Growth and Mass The Effects of Physical Activity on Bone Growth and Modelling Accretion of Bone Mass in Children and Adolescents Accretion of Bone Mass in Young and Premenopausal Women The Influence of Hormones, Diet and Physical Activity in Prevention of Osteoporosis Through Accretion of Peak Bone Mass Prevention of Bone Loss and Amelioration of Osteoporosis Endocrine Influences Over Bone Mass After Menopause Dietary Influence Over Bone Mass After Menopause The Effects of Physical Activity on Bone Mass Maintenance After Menopause Ways to Increase the Osteogenic Effects of Exercise Conclusions Abstract Osteoporosis is a serious health problem that diminishes quality of life and levies a financial burden on those who fear and experience bone fractures. Physical activity as a way to prevent osteoporosis is based on evidence that it can regulate bone maintenance and stimulate bone formation including the accumula-

2 780 Borer tion of mineral, in addition to strengthening muscles, improving balance, and thus reducing the overall risk of falls and fractures. Currently, our understanding of how to use exercise effectively in the prevention of osteoporosis is incomplete. It is uncertain whether exercise will help accumulate more overall peak bone mass during childhood, adolescence and young adulthood. Also, the consistent effectiveness of exercise to increase bone mass, or at least arrest the loss of bone mass after menopause, is also in question. Within this framework, section 1 introduces mechanical characteristics of bones to assist the reader in understanding their responses to physical activity. Section 2 reviews hormonal, nutritional and mechanical factors necessary for the growth of bones in length, width and mineral content that produce peak bone mass in the course of childhood and adolescence using a large sample of healthy Caucasian girls and female adolescents for reference. Effectiveness of exercise is evaluated throughout using absolute changes in bone with the underlying assumption that useful exercise should produce changes that approximate or exceed the absolute magnitude of bone parameters in a healthy reference population. Physical activity increases growth in width and mineral content of bones in girls and adolescent females, particularly when it is initiated before puberty, carried out in volumes and at intensities seen in athletes, and accompanied by adequate caloric and calcium intakes. Similar increases are seen in young women following the termination of statural growth in response to athletic training, but not to more limited levels of physical activity characteristic of longitudinal training studies. After 9 12 months of regular exercise, young adult women often show very small benefits to bone health, possibly because of large subject attrition rates, inadequate exercise intensity, duration or frequency, or because at this stage of life accumulation of bone mass may be at its natural peak. The important influence of hormones as well as dietary and specific nutrient abundance on bone growth and health are emphasised, and premature bone loss associated with dietary restriction and estradiol withdrawal in exercise-induced amenorrhoea is described. In section 3, the same assessment is applied to the effects of physical activity in postmenopausal women. Studies of postmenopausal women are presented from the perspective of limitations of the capacity of the skeleton to adapt to mechanical stress of exercise due to altered hormonal status and inadequate intake of specific nutrients. After menopause, effectiveness of exercise to increase bone mineral depends heavily on adequate availability of dietary calcium. Relatively infrequent evidence that physical activity prevents bone loss or increases bone mineral after menopause may be a consequence of inadequate calcium availability or low intensity of exercise in training studies. Several studies with postmenopausal women show modest increases in bone mineral toward the norm seen in a healthy population in response to high-intensity training. Physical activities continue to stimulate increases in bone diameter throughout the lifespan. These exercise-stimulated increases in bone diameter diminish the risk of fractures by mechanically counteracting the thinning of bones and increases in bone porosity. Seven principles of bone adaptation to mechanical stress are reviewed in section 4 to suggest how exercise by human subjects could be made more effective. They posit that exercise should: (i) be dynamic, not static; (ii) exceed a threshold intensity; (iii) exceed a threshold strain frequency; (iv) be relatively

3 Physical Activity and Osteoporosis in Women 781 brief but intermittent; (v) impose an unusual loading pattern on the bones; (vi) be supported by unlimited nutrient energy; and (vii) include adequate calcium and cholecalciferol (vitamin D3) availability. ended and the involution phase has begun. Although it is likely that both of these processes contribute to bone loss and osteoporosis, [6] they are discussed separately in this article. Since the capacity for accretion of bone mass and the loss of bone mineral are critically linked, respectively, to a woman s de- velopmental and chronological age, and starting bone mass and BMD, discussion of the effectiveness of exercise is organised by chronological and devel- opmental stages using a large sample of healthy North American and North European Caucasian girls, adolescents and women for reference. In sec- tion 2, changes in bone mass, bone mineral and bone geometry during growth and skeletal accumulative phase are used to evaluate the influence of physical activity. In section 3, the same principle is used to evaluate the effects of physical activity on the bone mass in adult and postmenopausal women during the bone maintenance and later involutional phase. Absolute changes in bone are described wherever possible with the premise that useful exercise should produce changes that approximate or exceed the absolute magnitude of bone parameters seen in large numbers of healthy women. Normalisation of absolute values of BMD and bone mineral content (BMC) was performed [7] to eliminate differences generated with the use of dif- ferent equipment. In this article, presentation of absolute changes in BMD and BMC differs from most reviews and meta-analyses that rely largely on the relative measures of change such as differences in percentage change between the exercising and sedentary groups. The latter approach can be mis- leading as it leaves the impression that the relative change in the bone is independent of starting bone size and density (especially when the exercising subjects have initially lower values than the healthy reference population) and implies that the magni- tude of the effect can be multiplied by simple exten- sion of the duration of the treatment. Furthermore, Osteoporosis is a reduction in bone mineral density (BMD) 2.5 standard deviations (SDs) below the mean, and osteopenia SDs below the mean, for healthy young women at the age of attainment of peak body mass (T score). In some instances, the reference population used is standard population matched for age, sex and race (Z score). Osteopenia is a reduction in BMD SDs below the reference values (T or Z scores). Loss of BMD contributes to loss of mechanical strength and to bone fragility, and thus to predisposition for bone fractures in response to atraumatic stresses. [1] Currently in the US, bone breaks occur at a rate of 1.5 million per year and are associated with more than 17 billion dollars in healthcare costs. [2,3] Among the risk factors for osteoporosis that are not amenable to modification are genetics, sex, age, body size and ethnicity. This article examines the role of physical activity, and its interaction with dietary and hormonal factors, in prevention and amelioration of osteoporosis. In general, inactivity, lack of exposure to sex hormones, low intakes of nutrient energy, and calcium and vitamin D constitute modifiable risk factors for osteoporosis. Section 1 provides a brief overview of the mechanical properties of the bone. Development of osteoporosis is variably attributed to either inadequate accumulation of peak bone mass prior to attainment of skeletal maturity [4] or to excessive rate of bone loss during aging. [5] Assuming a constant age-associated rate of bone loss, individuals with inadequate peak bone mass reach the osteoporotic bone density earlier than the individuals who have accumulated a greater peak bone mass. Therefore, one line of intense interest focuses on whether variables such as physical activity and appropriate nutrition can stimulate greater accumulation of peak bone mass. The other area of interest is whether physical activity and appropriate nutrition can reduce or block the losses of bone mineral once the accumulative phase of bone biology has

4 782 Borer matrix. Bone cortex consists of an outer surface, periosteum and an inner surface, endosteum that envelop the endocortical bone. Periosteal and endos- teal surfaces of the bone are covered with a layer of flat lining cells, also thought to be derived from osteoblasts. Osteocytes are in contact with the lining cells on bone surface, and with neighbouring osteo- cytes through extended cell processes that allow cell-to-cell communication through gap junctions. The matrix immediately surrounding the osteocyte is not mineralised but forms lacunae and an inter- connected system of fluid-filled canalliculi. the essential role of hormones and nutrition in bone growth and maintenance and their interactions with exercise are stressed throughout. Finally, the postulated mechanisms of adaptation of mature bone to mechanical stresses that have been largely developed in animal studies serve as a framework for evaluation of the adequacy of the exercise approaches that have been used to date for prevention and amelioration of osteoporosis in women. Thus, this article differs from the others [8-11] in that it: (i) integrates the information on the effects of physical activity with that on the hormonal and dietary influences on the bone; (ii) examines these influences from a lifetime perspective; and (iii) compares the changes in bone mass and geometry influenced by exercise to bone values found in a healthy reference population. Trabecular or cancellous bone (sometimes re- ferred to as spongiosa) is located in the interior of cuboid and flat bones and in epiphyseal and metaphyseal ends of long bones at the interface between the bone and the marrow cavity. It consists 1. Mechanical Characteristics of Bones of a spongy bony latticework of struts (trabeculae) that have a lamellar structure and are shaped as A better understanding of bone morphology and plates and rods µm thick (figure 2). [13] The its mechanical properties is a useful preamble to an surface of cancellous bone merges with the endocorunderstanding of their responses to physical activity, tical surface, which in turn merges with the intracorhormones and diet. It is also useful to be cognisant tical Haversian system. The general orientation of of the limitations of the methods used to assess bone trabecular struts follows the prevailing bone stress growth, bone mass, and its mineral content especial- trajectories as they align and thicken in the direcly when the magnitude of change in the bone ap- tions that will best resist the load, an observation proximates the precision (instrument limit of resolu- made by Julius Wolff in [14,15] Because of the tion) of the method. mechanical advantage of this aspect of bone morphology, Wolff s insight has stimulated research on 1.1 Bone Morphology principles that guide adaptation of bone geometry to prevailing mechanical stresses, a topic that is briefly By structural design, mature bone can be cat- egorised into two distinct types: (i) compact or corti- cal bone; and (ii) trabecular or cancellous bone. Compact or cortical bone in the diaphyseal walls of long bones and on the surface of cuboid and flat bones, derives its strength from its geometric organisation as a Haversian system of osteons, that is concentric mineralised plates (lamellae) surround- ing central canals that provide access to blood ves- sels and nerves (figure 1). [12] Interstitial lamellae fill in the spaces between the osteons. Embedded within the concentric layers of fibrous mineralised matrix is an interconnected network of osteocytes, a cell line derived from osteoblasts. In the process of differentiation to osteocytes, osteoblasts produce a collagen outlined in section 4. Trabecular surfaces are also covered with a layer of resting cells derived from osteoblasts and surrounded by marrow components. Compact bone makes up about 80%, and trabecu- lar bone about 20% of total skeletal mass. In addition, the relative proportion of cortical and trabecu- lar components varies in individual bones. The proportion of cortical bone is highest (>90%) in the diaphyseal shafts of long bones. Radial and ulnar shafts consist of about 95% cortical and 5% trabecu- lar bone. [16] The central axial skeleton (spine) con- sists of 62 70% by volume of trabecular bone [10,17] The trabeculae account for 24% of calcium in whole thoracico-lumbar vertebrae and for 42% of calcium

5 Physical Activity and Osteoporosis in Women 783 Osteogenic layer of periosteum Fibrous layer of periosteum Outer circumferential lamellae Lacunae containing osteocytes Canaliculi Cementing line Compact bone Interstitial lamellae Haversian system Volkmann's canals Blood vessel and endosteal lining of haversian canal Endosteum Fig. 1. Structure of compact bone. Longitudinal and cross-sectional view of Haversian system in the diaphysis of a long bone shows osteocytes embedded with mineralised concentric lamellae surrounding a central canal with a blood vessel. Osteocytes interconnect through processes within a network of canaliculi. Periosteal bone apposition occurs in the osteogenic outer layer, and bone resorption occurs at the inner endosteal surface (reproduced from Ham, [12] with permission). show that immobilisation in the form of bed rest [21-28] or exposure to the hypogravity of outer space [29-32] lead to massive loss of mineral in the order of 1% per week. [22-24] What is not fully under- stood is how mechanical stimulation influences bone formation, shape, or organisation, and mineral density, and how these mechanical stimuli interact with diet and hormones. It is currently hypothesised that the interconnected network of osteocytes and of the periosteal and trabecular lining cells is mecha- nosensitive to shear stress and streaming electrical potentials generated by extracellular fluid forced through the bone canaliculi when cortical bone un- dergoes compression, bending, or torsion during mechanical loading. [33-35] In compact bone, changes in mineral mass and bone geometry can be initiated at three sites: (i) in periosteal envelope where growth of the bone in width occurs through recruitment and proliferation in the body of vertebrae in women. The corresponding values for men are 19% and 34%, respectively. [18] Since proportions of cortical and trabecular bone vary in different locations of the same bone, it is important to evaluate experimental results in terms of the measurement site. For instance, in the forearm, radius at one-third the distance from the ulnar styloid process to the olecranon has 85 90% cortical and 10 15% trabecular bone, while the distal radius is approximately 60 70% trabecular bone and 30 40% cortical bone. [19] In the hip, the ratio of cortical to trabecular bone is 57% to 43% in the proximal femur, 50% to 50% in the trochanteric region, and 75% to 25% in the neck area. [20] It has been frequently reported that mechanical loading of bones is essential for their normal growth in length and width and for their accretion of mineral in a way that increases their capacity to resist muscle forces and the pull of gravity. Numerous studies

6 784 Borer Fig. 2. Structure of trabecular bone. Spongy network of interconnected horizontal and vertical trabeculae is found in the interior of spinal vertebrae, flat and couboid bones, and at the metaphyseal ends of long bones. Trabecular bone has a large surface that makes it more responsive to remodelling. Trabeculae at the ends of long bones show orientation along stress trajectories (reproduced from Mosekilde, [13] with permission from Elsevier). of osteoblasts in sub-periosteal layer and through their deposition of bone mineral into the bone ma- Several imaging techniques are used to measure bone mass, dimensions, BMC and BMD. [38] They differ in the extent to which they can isolate densitometric and geometric properties, and changes in cortical and trabecular compartments. In addition, they differ in the amount of radiation they deliver and instrument resolution. The instrument resolution differences that contribute to precision of the measurements need to be taken into consideration especially when they approximate the magnitude of exercise effects. X-ray radiography, single-photon absorptiometry (SPA), dual-photon absorptiometry (DPA), and dual-energy x-ray absorptiometry (DXA) measure combined densitometric and geometric changes in the scan path. Radiography has been used to measure dimensions of cortical bone such as width and area of the cortex particularly in the forelimb and the hand. [39] Its resolution is poor at sites where a large mass of tissue overlays the bone, and it is accompanied by relatively large radiation exposure. SPA, DPA, DXA and ultrasound attenuation measure BMD and BMC and allow for greater precision and lower coefficients of variation. SPA precision is about 1 2.5% and DPA resolution is about 2 5%. [40-43] With these two methods, subject exposure to radiation is 3 5 mrem. [44] The instrument precision of DXA scans is approximately 1 2% at most sites. [45,46] Total body surface radia- tion exposure with DXA is <1 mrem. Because of ease of its use, high resolution, and low radiation exposure, DXA has become a method of choice and has been predominantly used to measure total body, hip and spine BMD. Similarly, because of the pre- ponderance of DXA measurements in research on the effects of exercise on bone mass, only values derived from this method of measurement have been used in figures displaying reviewed data. SPA, DPA and DXA measure areal BMD in grams of mineral content per squared bone width (BMC/W 2 = g/cm 2 ). The planar projection-type of trix; (ii) in the intracortical envelope where changes in BMC of osteons takes place; and (iii) in the endosteal envelope, the predominant site of bone removal through surface resorption of mineral as a result of osteoclast action. By virtue of its spongy geometry, trabecular bone has 8-fold greater surface area accessible to osteoclastic resorption per unit volume [36] and therefore undergoes faster remodelling and more rapid changes in bone mass than the 1.2 Methodological and Study Design Issues cortical bone. [37] The epiphyseal growth plate, on the boundary between the epiphysis and metaphysis is a areal BMD measurements have a problem in that they are affected by bone size if they do not adespecialised bone region allowing for longitudinal quately adjust for depth or thickness of bone. [47] bone growth (described in section 2.1.1). Thus the same areal BMD measurement for a small

7 Physical Activity and Osteoporosis in Women 785 and a large vertebra will misleadingly underestimate the BMD of the smaller relative to the larger bone. To overcome this drawback, algorithms have been developed to approximate the volumetric bone density from areal bone density taking into account bone porosity. Bone mineral apparent density (BMAD) is derived from areal BMD measurements per estimated total volume in g/cm3. [45,46] It is calculated as BMAD = BMC/π (W/2) 2 lengthroi (where BMC is calculated by adding the bone mineral within the projected area and expressing it as grams (g) or g/cm, W is bone width, and ROI is the scanned region of interest). Thus, large bones with the higher DXA BMD measurements, may actually have the same BMAD as smaller bones. [48] Quantitative computed tomography (QCT) can isolate densitometric and geometric properties of the bone, allows for direct measurements of volumetric BMD in mg/cm 3, and can separate measurements of cortical and trabecular volumetric BMD. However, it delivers higher radiation exposure than DXA. Its precision is 1 3%. [42,49] In addition to the wholebody QCT, a special purpose peripheral QCT (pqct) was recently developed providing opportunity for 3-dimensional bone scanning at lower cost, with lower radiation exposure than the QCT, and precision of appendicular bone shaft scans of <2%. [50] Despite these advantages, at this time too few studies on exercise and bone adaptations have used QCT or pqct methods to allow for meaning- ful integration of the results. Whole-body calcium can also be measured by neutron activation [51] and γ- ray spectroscopy, [52] and can be used to estimate volumetric BMD. Precision of γ-ray spectroscopy is 1.8%, but exposure to radiation is greater than the previous methods. [53,54] Research design also affects validity of infer- ences that can be made from research studies. The assessment of the effects of physical activity on bone geometry, BMC or BMD is made difficult by the slow rate of change in these variables, which necessitates that interventions last months or years. Approaches that circumvent the problem of engaging individuals in prolonged exercise studies are either epidemiological surveys that employ ques- tionnaires assessing retroactively levels of physical activity and/or diet on the current BMD and BMC, [55-57] or cross-sectional comparisons of the effects of different levels of physical activity or athletic training on bone width, BMC or BMD. Thus in athletics, or in lifetime amateur sports like squash and tennis, motivated individuals choose to engage in intense training routines over long periods of time. Both approaches provide very useful insights if they demonstrate site-specific changes in bone mass, size or density that can be attributed to the volume or intensity of particular physical activity. They are usually criticised for being confounded by self-selection of individuals with particular pheno- types and genetic predispositions to different sports, or different levels of physical activity, as there is no assurance that the comparison active and inactive groups were similar before engaging in different levels of physical activity. Longitudinal studies usually circumvent the self-selection bias, but they re- quire sufficient numbers of individuals representa- tive of a healthy population, and random or matched assignment of subjects to groups, which is not al- ways achieved. [40,42,58,59] Concerned about the above issues, some meta-analyses have eliminated all non- randomised studies, [11] but such rigorous exclusion criteria remove some useful information. Longitudi- nal studies also require good matching of appropriate phenotypic variables (including BMC and BMD), which again is frequently missing. Starting bone mass values often are lower, and losses of bone mass in control groups are often unexpectedly large in participants in some longitudinal studies, which would suggest self-selection of individuals who al- ready have reduced bone mass or increased rate of bone loss to studies aimed at increasing BMD. The necessity for participation in exercise training for long periods of time to achieve measurable changes in bone mass is associated with large drop- out rates and variable adherence to study protocol. The retention rate in six studies that engaged sub- jects aged years was about 65% [58-63] and in 14 studies with 50- to 70-year-old women it was about 82%. [41-43,53,59,64-72] Among those subjects who stayed in the studies, compliance with the study

8 786 Borer Ultimate load Load Ultimate load Stress a b Elastic region Deformation Strength Ultimate load failure Yield region Plastic region Slope = stiffness or rigidity Elastic region Strength Ultimate stress load failure Strain Yield region Plastic region Slope = Young's modulus Ultimate deformation Ultimate strain Fig. 3. Structural properties of the bone (a). Bone stiffness or rigidity resists permanent deformation to smaller loads in a linear dosedependent manner. This reflects the elastic structural resistance of bone to loading. Above the yield load, bone undergoes non-linear plastic deformation. At ultimate or failure load, bone breaks and undergoes ultimate deformation. Material properties of the bone (b). At lower ranges of stress, bending strength (Young s modulus of elasticity or section modulus) is a measure of bone s resistance to deformation. Yield stress is the mechanical force that causes bone deformation and structural microdamage. The area under that portion of the curve is a measure of bone brittleness and indicates the amount of energy that the bone will absorb before it reaches ultimate stress or breaking strength. protocol was about 80 83%. Such relatively high attrition rates can invalidate good initial matching of exercising and sedentary subjects. Additional problems with longitudinal studies are: (i) the volume of exercise training is usually 2- to 10-fold lower (3 5 hours/week) than the volumes customarily performed by athletes (10 35 hours/week); (ii) the duration of training is substantially shorter (4 18 months) than in athletes who often train for years; (iii) the exercise stimulus is often of low intensity and diversified over different skeletal sites rather than site-specific as in many sports; (iv) they often provide customary rather than unusual patterns of mechanical loading; (v) studies seeking correlations between habitual intakes of calcium and parameters of bone mass usually employ 3- or 4-day dietary recalls, which may be of insufficient length for accurate assessment of calcium intake; and (vi) a bias against publication of negative results (which was evaluated in some meta-analyses [8] ) may influence our ability to evaluate the effectiveness of exercise on BMC and BMD. In view of the uncertainty about the effectiveness of exercise stimuli employed, adequacy of subject numbers, and other methodological issues, this review considered both the longitudinal (randomised and non-randomised) and cross-sectional studies, including studies of athletes, as well as epidemiological studies of the effects of exercise if they showed evidence of site-specificity of adaptive changes in the bone. Instead of limiting inclusion to only longitudinal randomised trials, of which there is a limited number, and which have already mentioned limitations concerning the adequacy of exercise stimulus, the validity of exercise effects was evaluated by comparing the absolute bone values and changes induced by exercise against the bone values in the healthy reference population. In addition, whenever possible, the reader is cautioned about weaknesses of study design and execution. 1.3 Mechanical Properties of Bones Bones have been designed to provide resistance against the forces of muscle contraction during movement of body parts and against gravitational

9 Physical Activity and Osteoporosis in Women 787 Fig. 4. The contribution of bone geometry to bone strength The distribution of bone mass around its bending axis provides a measure of its resistance to bending called cross-sectional moment of inertia (CSMI). CSMI increases as the cross-sectional diameter of bone increases (reproduced from Snow-Harter and Marcus, [10] with permission). (bone shaft) reflecting the distribution of bone mass around its bending axis. [48,76,77] This bone property is the cross-sectional moment of inertia (CSMI) and is expressed in cm 4. Areal moment of inertia provides resistance against bending loads imposed on the bone shaft. Polar moment if inertia provides resistance against torsion. Thus, a distribution of bone mass further away from its bending axis conveys greater strength against bending and torsion than an equal bone mass placed closer to the bending axis (figure 4, right vs left, respectively). CSMI is estimated using an engineering formula as follows: CSMI = π (W 4 (W 2 CWT 4 ))/64 where CWT is the average bone cortical thickness at a given bone site. [45,46] Bone increases in its diameter and rigidity with advancing age (figure 5). [76,77] Increases in bone diameter generate increases in CSMI and partially offset decreases in bone strength due to reduction in cortical thickness that also occurs with advancing age. When bone cortical thickness is not measured directly, it can be estimated from BMC and width as follows: CWT = W/2 (W 2 /2) BMC/length ROI π ρ force during various forms of locomotion. Both structural and material properties contribute to mechanical resistance of bone against various forces. The chief component of structural bone properties is bone geometry, that is the overall bone size and shape, [73-75] but material bone properties also play a role. Structural properties of bone are rigidity or stiffness, bending, torsional and com- pressive strength, and toughness. These structural properties of the bone are inferred from its deformation or deflection when it is subjected to increased loading forces (figure 3a). At the lower range of loading, bone stiffness or rigidity resists permanent deformation in a linear dose-dependent manner. This reflects the elastic structural resistance of bone to loading. Above the yield load, the magnitude of the force overcomes bone stiffness and elasticity, and bone undergoes non-linear plastic deformation. At ultimate or failure load, bone breaks and undergoes ultimate deformation. Stiffness and toughness (resistance to breaks) distinguish bone from tendons, which are less stiff than the bone. On the other hand, tendons contain similar non-mineral protein components as bone and may be as tough or tougher than bone. The geometrical property that contributes to bone rigidity is the cylindrical shape of its diaphysis where ρ is the material density of bone with an assumed value of 1.05 g/cm3 and ROI is region of interest. [45,46] The final geometrical property of bone shaft that influences its strength is bone length. As bone shaft increases in length its strength de- clines. [48] The principal difference between trabecular and cortical bone is the greater porosity of trabecular bone. The porosity is assessed with measurements years Fig. 5. The change in bone diameter with age. As bone grows in width with age through periosteal apposition, its cortex thins due to more rapid endosteal bone resorption. The reduction in wall thickness, and sometimes also in bone density, is partially compensated by the greater bone strength due increased bone diameter (reproduced from van der Meulen et al., [78] with permission from Elsevier).

10 788 Borer of apparent density (bone mass divided by volume of the ROI) of trabecular bone relative to cortical bone. In human skeleton, the apparent density of trabecular bone ranges between 0.1 and 1 g/cm 3, while the apparent density of cortical bone is 1.8 g/ cm3. Trabecular bone with apparent density of 0.2 g/ cm3 has porosity relative to the density of cortical bone of approximately 90%. [77] Compared with the difference in apparent bone density, the true density of trabecular and cortical bone (that takes into account differences in porosity) is similar. [48,77] Besides the degree of porosity, the orientation of horizontal and vertical trabeculae contribute importantly to trabecular bone strength. In the young bone, thick vertical plates derive added strength from bracing with thinner horizontal trabeculae [79] (figure 2). The stress-strain curve of loaded trabecular bone dis- plays an initial linear elastic region followed by a long non-linear plateau beyond the yield stress. This plateau reflects cumulative trabecular fracture. Loss of BMC at any age leads to thinning of trabeculae and to loss of their inter-connectivity as well as to increased porosity. This affects trabecular bone strength more directly than is the case for cortical bones that gain some strength with increases in bone diameter even as their cortical walls grow thinner. A 10-fold change in apparent trabecular bone density produces a 100-fold difference in its strength and compressive modulus. [77] Material properties of the bone are determined by the relative amounts of three major bone components, mineral, water and organics as well as the geometrical arrangement of the mineral (bone porosity and trabecular orientation and thickness). Material properties of the bone are inferred from the stress-strain curve (figure 3b). It shows that at lower ranges of stress, bending strength (Young s modulus of elasticity or section modulus) provides resistance to deformation in response to applied stress. The area under this linear portion of stress-strain curve indicates the amount of energy a bone can withstand before deformation. Bone bending, torsional, or compressive strength (Z) is measured in cm 3 as follows: Z = 2 CSMI/W, where CSMI is the crosssectional moment of inertia and W is bone diameter or width. [45,46] Yield stress is the mechanical input that causes bone to deform to a level in which structural damage begins to occur. The area under that portion of the curve indicates the amount of energy that the bone will absorb before damage occurs. This area is small when the bone is brittle or fragile and large when the bone is ductile. Ultimate stress (or bone breaking strength) is the energy that produces bone failure and ultimate strain. 1.4 Properties of Bones Contributing to the Risk of Fractures Bone form represents a compromise between strength and mass and thus is not maximally de- signed to resist fracture. Presence of a marrow cavi- ty represents a trade-off between lightness necessary for cost-effective movement and bone mass needed for resistance against breaks. [80] This design can produce breaks even in young bones, for instance in young tennis or squash players, if their forearm bones are exposed to high stresses. [81-83] The vari- ables that make the greatest contribution to overall strength of a whole bone and its resistance to frac- ture are BMD and bone size. [48] BMD contributes between 50% and 80% of variance to bone breaking strength, [47,84-86] but fragility can be high in some conditions of increased bone density such as fluo- ride treatment. [87] Bone quality relates to non-miner- al components such as collagen and other proteins that give bone toughness and contribute to strength. [73] In some conditions, fragility is associat- ed with reduced bone quality without a change in BMD. Some examples are glucocorticoid treat- ment, [88] organ transplants, [89] and diabetes mellitus in the elderly. [90] Big dense bones have a higher CSMI and are stronger than small bones. Bones resist normal loads but not the loads char- acteristic of falls. The proximal femur usually resists tension in its superior part (trochanteric area) and compression in inferior part (neck), with the com- pression being much greater than the tension. [48] A sideways fall reverses the nature of the stresses, and the cancellous structure of the neck can not resist increased compression in the superior part and in- creased tension in the inferior part. [48,80] One of the

11 Physical Activity and Osteoporosis in Women 789 predicted from low rates of childhood bone growth resulting in low peak bone mass and mineral con- tent. The hazard ratio for fracture risk was almost twice as high in girls with growth rates in the lowest quartile compared with girls in the highest quartile of bone mass. [116] Studies of the effects of exercise on fracture risk revealed that small increases in BMD produce exponential reductions in the relative risk of bone fractures. [107, ] The reason for the interest in the effectiveness of exercise in the reduc- tion of bone fractures is that it can positively affect BMD, muscle mass and strength, and balance. [71] reasons for the interest in variables that will reduce risk of bone fractures is the great cost to human quality of life and for medical care after their inci- dence. [3,91-94] Fractures due to falls are facilitated by loss of BMD, sarcopenia (loss of muscle mass) and the associated loss of strength, and age-associated decline in balance. [93-98] BMD is currently the best non-invasive predictor available for bone fracture risk. [99-105] Generally, bone fractures can be predicted from mineral density as well as from the geometry and size of the bones, sometimes several decades before their incidence, although predictions are more reliable over shorter 2. Prevention of Osteoporosis Through intervals. [106,107] Individual studies and a meta-anal- Accumulation of Peak Bone Mass ysis [104] reveal that for a 1SD decline in BMD of the hip, the relative risk (RR) of fracture of any type is 1.5, RR is increased to 2.8-fold for the hip, 2.1 Bone Growth: Increases in Length, Width 2.7- to 2.8-fold for the femoral neck, 2.26-fold for and Mass the femoral trochanter, to 2-fold for the lumbar vertebrae, and 1.6- to 1.83-fold for the radial shaft This section discusses how hormonal, nutritional and distal radius. [ ] In absolute terms, a deprocesses: and mechanical variables affect three distinct crease of 0.11 g/cm 2 in the femoral neck BMD in (i) growth of bones in length; (ii) growth older women was associated with a 2.6-fold increase in width; and (iii) accumulation of bone mineral, in RR for hip fracture. [110] that collectively result in peak bone mass. The three processes of accrual of bone mass will be presented Bone fragility is also related to variables such as separately using normative data from large surveys bone geometry, [75,108,109] smaller bone size [111,112] of healthy girls and women because they display and low peak bone mass. [113,114] Faulkner et al. [108] different time courses and appear to be regulated measured the hip axis length going through the independently. The interaction of mechanical stimufemoral neck from below greater trochanter to the lation, hormones, nutrient energy and specific nutriinner pelvic brim, neck-shaft angle going through ents in the coordination of these three components the femoral neck and the length of femoral shaft, and of bone growth will be emphasised in the interpretathe femoral neck width. They found that the risk of tion of the exercise data. femoral neck and trochanteric fractures increased by 1.9- and 1.6-fold, respectively, for each SD increase Longitudinal Bone Growth in the hip axis length, and that this geometric risk Longitudinal bone growth, the diagnostic feature factor was independent of loss of BMD. Ahlborg et of statural growth, starts with cellular proliferation al. [115] measured changes in geometrical features and throughout the cartilaginous bone template. After mineral density of the distal radius over a period of the diaphyseal shafts of long bones mineralise in the 15 years in women since menopause. They found course of childhood, the longitudinal bone growth that the bone strength index decreased by only 0.7% becomes restricted to the epiphyseal growth zone per year despite a 1.9% annual loss in BMD due to (EGZ) [figure 6]. [12] EGZ consists of proliferating compensatory increases of 0.7% and 1.1% in perios- germinative cartilage cells that undergo several cyteal and medullary diameters. For each SD decline cles of cell division before they stop growing and in the strength index, risk of fracture of the radius differentiate. Differentiation entails switching from increased by 3.8-fold. Fracture risk also can be secretion of type II to type X collagen into the

12 790 Borer Periosteal bone apposition Endosteal bone resorption EGZ Fig. 6. Structural modelling of bone metaphysis during longitudinal growth. A growing bone elongates in the epiphyseal growth zone (EGZ), a band of cartilage tissue that separates trabecular bone in the epiphysis and the spongiosa of the metaphysis. The bone metaphysis changes shape during longitudinal growth through periosteal apposition and endosteal resorption (reproduced from Ham, [12] with permission). partly controlled through low pulsatility of growth hormone (GH) secretion, which at this stage of human life is predominantly nocturnal. The initiation of puberty and of the adolescent spurt in longitudinal growth are delayed by inadequate nutrient availability during childhood, and advanced by excess nutrition and childhood obesity [ ] (see section 2.2.1). Puberty and pubertal growth spurt are initiated in girls about 2 years earlier than in boys. With the onset of puberty, increased pulsatile secretion of gonadotropic hormones, luteinising hormone (LH) and follicle stimulating hormone (FSH), stimulates gonadal maturation and secretion of sex steroids. Sex steroids stimulate GH synthesis and pulsatile secretion so that the volume of GH secreted in each spontaneous pulse, and total daily GH output, are increased to a lifetime peak. [127] Joint action of increased estradiol and GH secretion increases linear growth velocity in girls to about 8 9 cm/year at its peak. [123] Sex steroids and GH each contribute approximately one-half of the longitudinal growth stimulus as children deficient in either hormone grow only half as fast. [128,129] Longitudinal growth spurt in adolescent females is closely tied to stages of puberty. Although both elongation and accelerat- ed accumulation of bone calcium start at the onset of Tanner stage 2, peak height velocity occurs at the matrix and cartilage cells undergoing hypertrophy. The hypertrophied chondrocytes next release neutral proteases that break down the cartilaginous matrix and express alkaline phosphatase that initiates mineralisation. [121] Blood vessels infiltrate hypertrophied chondrocytes through the process of angiogenesis as a preamble to chondrocyte apoptosis age of years, approximately months (death). Osteoblast progenitor cells derived from before the onset of menarche at about 12.7 marrow stromal cells arrive in the blood vessels and years. [ ] replace the chondrocyte matrix mineral with Sex differences in the growth of proportions of hydroxyapatite mineral consisting largely of calciappendicular and axial skeleton and of pelvic and um carbonate and calcium phosphate. Concentric shoulder girdles are expressed during pubertal lamellae of mineral are deposited around the blood growth. Peak longitudinal growth of legs occurs 0.6 vessels to form the Haversian system of compact to 1 year before the trunk. [133] Because girls generalbone. Beyond the EGZ, in the spongiosa, and in the ly reach puberty 2 years before boys, legs in girls do interior of cuboid and flat bones, trabeculae are not grow as long as in boys. [123] Peak velocity in formed through an interaction of osteoblastic depobone turnover coincides with peak height velocity sition of lamellae within struts and osteoclastic bone and occurs approximately 20 months prior to menarresorption. che. [134] Coincidence in the pattern of longitudinal Longitudinal growth velocity is greatest during growth and markers of bone turnover indicate that the second trimester of intra-uterine life (figure modelling of bone shape undergoes rapid changes 7). [122] The rate of longitudinal growth decelerates during increases in statural height (as illustrated in throughout childhood to an average of about 5 cm/ figure 6). After it peaks during Tanner stages 3 to 4, year between the ages of 3 and 10 years. [123] This is usually at about 12 years of age, the longitudinal

13 Physical Activity and Osteoporosis in Women 791 a Birth additional small increments through early twenties, especially in slow maturers. [140, ] They attain adult leg length between the ages of years, and peak trunk length around age 19 years. The disappearance of proliferative cartilage cells and overall reduction in bone turnover has been associated with high plasma concentrations of sex steroid hormones attained during puberty [125] and growth plate senescence manifested as reduced proliferative capacity. [145] In young women, the EGZs in the limbs close, and all longitudinal growth ceases usually before the age of 25 years. Growth velocity (cm/wk) b Prenatal Girls Boys Age (wk) Postnatal Age (y) Fig. 7. Statural growth velocity before birth and during childhood. Longitudinal growth is fastest during the prenatal period (a) and declines throughout childhood (b). Growth velocity is transiently increased during the adolescent, pubertal growth spurt before it is arrested toward the middle of the second decade of life (reproduced from Lushkey, [122] with permission). bone growth in girls rapidly decelerates during menarche, which usually occurs at Tanner stage 4 and comes to a stop sometime during Tanner stage 5. [ ] Around the age of 16 years or approximate- In adolescents experiencing growth spurt, growth ly 3 years after the onset of menarche, female ado- of bone in width needs to be considered when areal lescents come close to attaining peak stature with BMD assessment methods are used to avoid mis Bone Growth in Width and Thickness During the period of skeletal elongation, bone shape and width also change through a process sometimes called structural remodelling (figure 6). Growth of bone in width and thickness results from activation of the quiescent lining cells in the periosteal, intracortical and endosteal envelopes to proliferate and deposit mineral. During the 4 years after attainment of peak stature, bone grows in width without changes in BMD. [133] The time course of the capacity to add bone differs in the three bone surfaces. Capacity of the bone to grow in width through periosteal apposition, is apparently retained for the duration of human lifespan (figure 8b). Bone growth in width increases in women even after the age of 86 years, because at that age the rate of endosteal resorption declines relative to the rate of periosteal apposition. [146] The capacity of bone to increase in cortical thickness through endosteal apposition is confined to the period of adolescent longitudinal growth or a few years after its termination. [79] Upon cessation of endosteal growth, this bone envelope becomes a resorptive zone through the action of osteoclasts. Thus, bone cortical thickness starts declining in women between the ages of about years and perhaps earlier (figure 8a). Increases in bone width contribute to the relatively stable bone bending strength (figure 9a) and bone rigidity (fig- ure 9b) between the ages of 25 and 60 years despite the decreases in cortical thickness.

14 792 Borer Cortical thickness (mm) Width (cm) a b Age (y) Femoral shaft Ulna Radius shaft Humerus prox Humerus shaft Humerus dist Femur shaft Fig. 8. Growth of female cortical bone in thickness and in width. Cortical thickness of the femoral shaft declines in women after age 27 years, and possibly earlier (a). [147] The width of the appendicular long bones continues to increase in healthy Caucasian women between the ages of 15 and 63 years (b). [33,45,147,148] Humerus measurements are reported at three locations, proximal and distal to the shoulder joint and at the midpoint (shaft). identification of bone size differences as BMD differences. Areal measurements of BMD provide mis- leading measurements if changes in bone size are not taken into account. Volumetric BMD estimates from DXA measurements in girls during pubertal growth indicate that the accretion of bone mineral proceeds primarily through increases in bone size rather than by increases in BMD. [133] When QCT is used to measure the densities of cortical and cancellous bone in growing children, BMD in bone compartments appears unchanged, and the accrual of bone mineral is attributed to increases in bone size. [47,133,150] Accumulation of Bone Mineral Throughout human lifespan, changes in mineral density occur through the process of internal remodelling that responds to accumulated defects or microdamage in bone as well as to changes in nutritional circumstances and mechanical loading. Along with the changes in bone width, BMD changes through remodelling become the main avenue of change in bone mass once the longitudinal growth and associated bone accretion have terminated. Remodelling consists of linked cycles of resorption of mineral from Haversian osteons, or surface erosion of trabeculae, and of refilling the excavated areas with new bone material. Resorption and formation of bone result from interactions of osteoclasts and osteoblasts within segments of bone anatomy called basic multicellular unit. Remodelling is initiated through activation of lining cells and removal by several enzymes of proteins lining the surface of bone. Bone resorption is then started by multinucleated osteoclasts that attach to trabecular bone surface or to the interior of a Haversian unit (which then is known as cutting-cone). The ruffled border of the basal membrane of osteoclasts is equipped with a proton pump that produces acid that dissolves bone mineral. After a unit of bone is removed, resorption is stopped as osteoclasts become apoptotic. The resorption cavity is now populated by activated lining cells and osteoblasts that form new bone through deposition of hydroxyapatite. Each remodelling cycle is concluded when osteoblasts reline the surface of newly formed bone and become quiescent. Increases in BMD are recorded throughout the period of pubertal growth spurt. Rapid increases in BMD in girls were reported to have two peaks, one between the age of years, and the other be- tween years. [130] By the age of 12 years, girls have accumulated a little more than 83% of adult total body BMD. [151] Increases in BMD are tied to pubertal progression and slow down after the attain- ment of menarche. Within a year after attaining menarche, lumbar spine BMD in girls is at 71% of adult level. One to two years post menarche, lumbar spine BMD is at 95% of adult level, and 2 4 years post menarche it is at adult level [152,153] although it

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