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On-line version ISSN 1806-9940
Rev Bras Med Esporte vol.11 no.6 Niterói Nov./Dec. 2005
Efectos de la actividad física en la densidad mineral ósea y en la remodelacion del tejido óseo
Eduardo Lusa Cadore; Michel Arias Brentano; Luiz Fernando Martins Kruel
School of Physical Education Rio Grande do Sul Federal University
The purpose of this article is to make a review on different sportive modalities and the power training on the bone remodeling, and to discuss the possible relationship of the bone mineral density (BMD) to the muscular power and body composition. Several studies indicate that the high impact physical activity or physical activities demanding a high power production may have a benefic effect on the BMD due to the deformation that occurs in such tissue during the activity. Some authors have been assessing the effects of the physical training on some biochemical markers of the bone remodeling, since the variation on the concentrations of these markers might indicate a bone turnover or reabsorption state. Nevertheless, the inconsistency of the results found suggests that the analysis of the effects of the physical activity on the bone remodeling through these markers must be further investigated. There are many discrepancies as to the relationship of the BMD to the muscular power and body composition, mainly to determine what factors are most associated to the BMD. The determination of what type of physical activity is the ideal to increase the bone mass peak during the adolescence or even aiming to keep it later in the adult years is quite important in order to prevent and possibly treat the osteoporosis.
Keywords: Bone health. Physical exercise. Biochemical markers. Body composition. Muscular strength.
Este artículo busca revisar los efectos de modalidades deportivas diferentes y del entrenamiento de fuerza en la remodelación del hueso y discutir las posibles relaciones entre la densidad mineral del hueso (DMO) con la fuerza muscular y la composición corporal. Los numerosos estudios indican que la actividad física de alto impacto o que exige producción alta de fuerza, pueden tener un efecto beneficioso en la DMO, debido a la deformación que ese tejido, pasa durante la actividad física. Algunos autores han estado evaluando los efectos de la educación física en algunos marcadores bioquímicos de la remodelación del hueso, desde la variación de las concentraciones de esos marcadores que puedan indicar un estado de la formación o reabsorción del hueso. Sin embargo, la inconsistencia de los resultados encontrados, sugiere que el análisis de los efectos de la actividad física en el remodelación del hueso, a través de esos marcadores, debe investigarse más. Muchas diferencias existen con respecto a la relación entre la DMO con la fuerza muscular y la composición corporal, principalmente en la determinación de cual de esos factores está más asociada con la DMO. La determinación de que tipo de actividad física es ideal para aumentar el pico de masa del hueso en la adolescencia, o incluso mantenerla después de la edad adulta, es muy importante para la prevención y el posible tratamiento de la osteoporosis.
Palabras-clave: Salud osea. Ejercicio físico. Marcadores bioquímicos. Composición corpórea. Fuerzas musculares.
The bone mineral density (BMD) results from a dynamic process of the bone tissue formation and reabsorption called remodeling. The reabsorption causes deterioration on the tissue, while its formation is responsible by the reconstruction and strengthening of the deteriorated tissue(1). This process occurs along the lifetime within a four to six months period(2).
The maintenance of the BMD is very important to prevent the osteoporosis, which is characterized by an accentuated decrease in the BMD(3), in which the bone matrix and minerals are lost due to an excessive bone reabsorption that is related to its formation(4). This process is normally associated to the aging process and is an occurrence derived from the menopause(5) that leads to a higher incidence for fractures(6). Although the bone loss is more intense in women(5,7), men also present a decrease caused by the advanced age(8).
Several studies indicate that the physical activity has a positive relationship to the BMD, and this is an important factor to its maintenance(5,9-14). Some studies have reported the effects of several sportive modalities to the BMD in athletes or physically active individuals(12,15,16). Among these studies, a few use the strength training, trying to increase the BMD in individuals submitted to that type of physical activity(7,13,14,17). In general, the same studies have shown positive results related to the BMD(8,15,17-23). Nevertheless, despite this possible benefic effect, quite large training volumes may cause a damage on the BMD, and it seems that such damage is closely related to the disturbance in the hormonal homeostasis of the organism(5,6,24).
An assessment method that has been long used to understand the physiological mechanism coming from the osteogenic effect of the physical activity is to measure some biochemical formation markers (i.e., osteoblastic secretion) concentrations and the bone reabsorption (i.e., by-products of the bone collagen) and its variations deriving from the training.
The possible variation in these concentrations might indicate an anabolism status or a bone catabolism(3).
Although the majority of studies emphasize the effect of the type of the physical exercise on the BMD, other factors seem to interfere in that variable as well, such as the muscular strength(25) and the body composition(6,19,26). In this perspective, regardless the level of the physical activity, some studies have shown that BMD in physically active output athletes or even the sedentary ones seem to pursue an association to their muscular strength developed according to the type of the physical exercise or daily activity, and their body composition(6,19,25,26).
Based on the aspects approached in the above mentioned studies, the aim of this article is to make a review on the effects of different sportive modalities and the strength training on the bone health, and also to analyze its possible benefic or harmful mechanism. It also intends to make a review on the results attained with the biochemical markers for the bone metabolism, as a method to assess the bone remodeling related to the physical exercise, and the relationship of the BMD to other components related to the health, such as the muscular power and body composition.
1. ACTION OF THE EXERCISING ON THE BONE STRUCTURE AND REMODELING
The idea that larger overload physical activities derived from the body weight as well as the strength training cause osteogenic stimuli is a consensus in the specialized literature, due to an increase in the bone-located mechanical stress(1). Nevertheless, the physiological process responsible by the response to that strength is not clearly explained.
According to Brighton et al. apud Menkes et al.(18), a possible justification for the increase in the BMD to the strength training is the bone piezoelectric effect. This is suggested by the presence of biochemical signals that seem to reflect an electric field possibly as consequence for the applied overload.
This theory is applied to any deformation or bone overload caused by a compression, tension, torsion or shear on such tissue. These mechanical actions generate differences in the bones' electrical power that actuates as an electrical field stimulating the cellular activity, and leading to the deposition of minerals at stressed spots (Lanyon, Hartman apud Menkes et al.)(18).
Nevertheless, the osteogenic effect derived from the physical activity appears to demand a high training level that is characterized by a great volume and intensity. Related to the practice of the sportive modalities, Creighton et al.(1) assert that the bone strengthening that results from the repetitive stress that occurs during long training periods cannot be sufficient to increase the BMD in non-competitive athletes. Madsen et al.(19) suggest that the higher BMD observed in athletes can be consequence of the higher physical activity level practiced during the adolescence, suggesting an increasing BMD as consequence of a long-term training. In relation to the strength training, Pruitt et al.(13) suggest that it is required that the muscular contraction responsible by the bone deformation surpass a given threshold, in order to stimulate the tissue remodeling. In fact, the BMD seems to respond to a higher training intensity both in human(3) and in animal models(27).
Related to the bone remodeling, according to Andreoli et al.(15), in the strength induction, the deformation that occurs in the structures involved can lead to an optimum formation level and to an inhibition in the reabsorption that occurs within the normal remodeling cycle.
On the other hand, Menkes et al.(18) verified that the increase in the BMD is due to the stimulation on the bone turnover, rather than to an attenuation of the reabsorption that occurs into that tissue. Andreoli et al.(15) complement this theory suggesting that at the cellular level, the remodeling process overload-induced is performed by the action of the osteocytes that actuate as mechanical receptors of the applied stress and to the releasing of a stimulating chemical factor for the proliferation of the osteoblasts at the stressed spot.
The higher osteoblast activity that are the responsible cells by the bone turnover(18), or the osteoclasts that are the responsible cells by the bone reabsorption(4) can be suggested by the increasing circulating or urinary concentrations of the substances secreted by those cells. Those substances have been used as biochemical markers for the bone remodeling, and its concentrations have been measured in athletes or individuals submitted to some method of physical training to assess an eventual effect on the bone remodeling(6,7,17,18).
Among the markers for the bone turnover, it is the specific bone alkaline phosphatase(13,18) that is secreted by the osteoblasts and hydrolyzes the phosphate esters that are probably involved in the calcification process(4), and the osteocalcin or the bone Gla protein, whose synthesis increases whenever there is a major calcification of the tissue. However, there is a discrepancy as to its use. Some researches, such as Creighton et al.(1) observed the osteocalcin as a marker for the bone turnover, while other authors have used such substance as marker of the own remodeling activity(7,13).
Among the bone reabsorption markers, it is the free deoxypyridolin (expressed due to the urinary creatinine)(7), the circulating levels of the tartrate-resistant acid phosphatase(18), the hydroxyproline (expressed due to the urinary creatinine)(13), the telopeptide of the Type I collagen cross-linking of the amino terminal (NTx)(1), or the urinary carboxy (CTx)(2), among other cross-linking of the circulating pyridinoline(3), and all these substances are by-products of the bone collagen turnover.
Those regions with major amounts of trabecular bone, as the lumbar spine, normally present a better response to the exercise, possibly due to the fact they are more metabolic active(11,13,18). On the other hand, those regions with large amounts of cortical bone, as in the case of the femur, also present a response to the increase in the BMD to the exercise(3,17,18).
Such effect of the physical activity on the BMD generally happens specifically at the spots supporting the stress(15,28,29), although Rickli and Mcmanis(14) have observed a systemic effect of the physical activity on the BMD.
Although the physical activity may positively influence the bone remodeling, the biochemical process responsible by such effect is not quite clear, and other factors may mediate the effects of the physical training on the bone health, among them it is the nutrition, the individuals' genetics, and the hormonal homeostasis(15). This can be suggested due to the existence of studies that did not succeeded in presenting an increase in the BMD upon the physical exercising(2,7).
2. THE HARMFUL EFFECT OF EXERCISING ON THE BONE HEALTH AND THE RELATED HORMONAL ASPECTS
The female sexual hormones (i.e. estrogen, progesterone) have influence on the bone metabolism due to the fact they stimulate the osteoblastic activity. This action is suggested by the existence of the estrogenic receptors in these cells (Vandershueren apud Maïmoun et al.)(5). Furthermore, the estrogen inhibits some cytokine responsible by the osteoblast proliferation(4). In a study performed by Helge and Kanstrup(10), the concentration of the progesterone was highly related to the BMD in rhythmic and artistic gymnasts (r = 0.93, p < 0.01), indicating an association of such hormone to these athletes' BMD.
Although the level of the physical activity is a positively related variable to high BMD values, according to Gremion et al.(24), the high output endurance training might lead to an early bone loss due to the effects of the sexual female hormones on the homeostasis, and a consequent secondary amenorrhea, whose clinical picture is characterized by a decreasing number of menstrual cycles(6). Such effect is similar to what happens in postmenopausal women, whose low concentration of the sexual hormones implies in an accentuated bone loss and the consequent osteoporosis(5,7).
As to athlete women, one of the causes suggested to the bone loss process upon an intense endurance training is the low substrate level to the estrogen synthesis (i.e. the body fat)(4). According to Burrows et al.(6), the bone loss in this case happens due to a caloric deficit, and an appropriate nutritional diet could avoid these hormonal disturbances on female athletes. On the other hand, Maïmoun et al.(5) suggest that such low hormonal production that causes the osteopenia is a consequence of the hypothalamic-hypophyseal-gonadal axle suppression derived from the high intensity exercising, suggesting the effect on the central and peripheral mechanisms for the hormonal inhibition.
The BMD behavior upon the low hormonal production appears to be different among some modalities presenting an uneven overload stimuli(10). Frost et al. apud Helge and Kanstrup(10) have proposed a theoretical model suggesting that the lower estrogen concentration in the organism, the higher must be the mechanical stimuli to keep a normal BMD. In fact, comparing to sedentary women, amenorrheic and oligomenorrheal long-distance female runners presented low BMD(24), and this was not verified in oligomenorrheal rhythmic and artistic gymnasts who had that variable significantly higher than the non-physically active group(10). Probably, this had occurred due to the fact that the load applied in the joints, imposed by some jumps performed by the athletes is quite big in such modality than the load imposed during the running.
Gremion et al.(24) suggest that the hormonal reposition therapy (HRT) or the use of contraceptives with estrogen content are necessary in athletes presenting clinical amenorrhea picture. In fact, those authors observed that the BMD of runners using contraceptives was significantly higher than in athletes who did not use them. On the other hand, the benefit originated by the use of contraceptives on the BMD is questioned by Burrows et al.(6), who did not find in their results any association between the use of oral contraceptives and the BMD on female runners. As to the HRT, its association to the physical activity was already proven to be effective to the maintenance(7) or increase(30,31) of the BMD in elder women. However, the HRT cost-benefit must be assessed, once its usage can also cause some damages to the health(4) that will not be discussed in the review.
Although there is a close relationship between the homeostasis of the sexual hormones and the BMD in women(6,24), this relationship in men is not quite clear. Colvard et al. apud Maïmoun et al.(5) showed that the androgen action on the bone remodeling of men is mediated by specific receptors for the hormones found into the osteoblasts.
However, Maïmoun et al.(5) observed a benefic effect of the physical training on the BMD of triathletes with low androgenic hormone concentrations. Ryan et al.(17) found no association between the circulating testosterone levels and the variation in the BMD occurred after the strength training applied in elder men. Nevertheless, according to Ryan et al.(17), the circulating testosterone levels not necessarily reflect the action of that hormone at cellular level. Maïmoun et al.(5) suggest that other factors may be determinant to the bone mass, mainly when hormonal concentrations are found within a normal physiological range.
In such sense, although there is a bone strengthening effect in the overloaded physical activities, the intense training may cause low hormonal production and its negative effects on the axial bone health mainly in women, and this fact cannot be underestimated.
3. EFFECTS ON THE BMD OF PRACTICING SOME SPORTIVE MODALITIES
The osteogenic effect caused by the practice of exercises using the body weight or a large muscular strength production as overload(19,23) have been suggested, once athletes involved in sports with such feature present higher BMD than is usually found in the population in general(1,23). There are some indicatives that these types of sports are more energetic to the bone health than lower or no overload sports(19). Nevertheless, upon the observation of such effect(1,10,12,15,19,23,28), some authors point out that the transversal feature of studies comparing individuals who have practiced several sportive modalities to less physical active individuals may present a limitation that influenced the results.
Chart 1 presents some results found in those studies assessing the effect on the BMD of practicing several sportive modalities. These results allow to suggest that some of these modalities have a stimulating effect on the bone tissue remodeling whenever it is chronically submitted to an intensity that exceeds the regular overload(15). This effect seems to be related to the overload magnitude imposed during the exercise(1), and mainly at the specific spot where the overload is imposed(15). This allows to stimulate the practice of higher overload sportive modalities caused by the body weight(1,19), or to spread the use of the muscular strength(15) as possible tools to prevent the bone loss and the consequent osteoporosis besides of other benefits that were not approached in this review.
4. STRENGTH TRAINING AND BMD
The strength training (ST) has been pointed out as one of the physical activities that results in osteogenesis(3,8,18,21,22,32-34). Nevertheless, there are several points to be discussed as to what ST method would be more effective taking into account the exercises, the intensity and the period necessary in order to attain a bone response. Besides, the differences between the individuals' characteristics are factors that may lead to the inconsistency in the results as to the effectiveness of the ST towards a favorable influence on the bone status(13). This can be verified once individuals with high BMD levels appear not to easily respond to the osteogenic stimulus to the ST(3,7). However, the bone response to the ST appears to occur both in young and in elder individuals, and both in male and female individuals(8).
The mechanism to the increase in the BMD through the ST passes by the bone deformation magnitude caused during that activity. In fact, higher training intensities related to the peak load are generally associated to higher stimuli to the increasing BMD than lower intensities(3,13,17,18,22,35). Besides, the use of higher training intensities implies in more immediate responses on the BMD(3).
Comparing to other sportive modalities, as for instance the running, an activity that is known by its osteogenic effect(5,24), practicing ST appears to present a higher stimulus to the increasing bone mass on anatomic spots where both types of physical activity result in mechanical stress, similar to what occurs in the femoral cervix(3,5,24). It can be suggested that this occurs due to the existing relationship between the BMD to the level of the muscular strength(3,15,19,25,36), the major physical valence incremented through the ST, besides the large window of the strength gain mainly in non-trained individuals(37), allowing to apply an increasing overload propitiated by this type of training.
On the other hand, the overload imposed by the running is consequence of the body weight, and thus, it is constant along the time. Although it might have a higher amount of stimuli along the running, studies have showed that the stimulus magnitude is more important than its frequency(1,6,27,33).
Other aspect that can be considered to the optimum prescription of the type of ST with the purpose to stimulate the bone turnover is the type of muscular contraction used. So, starting from the existing relationship between the muscular strength and the BMD(2,3), it is reasonable to figure it out that the eccentric ST char acterized by a major strength production than the concentric ST(38-40) would be able to promote a major osteogenic stimulus. In fact, in a study comparing the eccentric and concentric ST using the same relative load, the eccentric ST showed to be more effective in increasing the BMD(32).
Chart 2 shows a resume of the methodology, and the results found in some studies using other ST than the combination of ST and other types of physical activity methods, and with HRT, with the purpose to investigate the effects of these types of training on the BMD. The applicability of these results is very important, in order to determine the best stimulus to the bone turnover that can be useful to prevent fractures mainly in elder postmenopausal women who had more bias to the osteoporosis(5,20).
5. PHYSICAL ACTIVITY AND BIOCHEMICAL MARKERS FOR THE BONE METABOLISM
Besides the densitometry methods, some researchers have been using the analysis of some bone metabolism markers to assess the effects of the physical activity on the bone remodeling, in search for some relationship between changes found in the BMD and the variation in the blood or urinary concentrations of these markers(1,7,8,18). This method has been used as a dynamic resource to assess the exercise vs. bone health relationship(1).
Vincent and Braith(3) showed that there is a relationship between the changes in the marker concentration of the bone metabolism and the densitometric changes observed, and indeed, there is a relationship between the training intensity and the magnitude of the increase in the markers for the bone turnover. Among other studies(1,18) those authors observed a major response from the bone turnover markers at higher training intensities.
Nevertheless, besides the daily variations of some markers(17), the discrepancy in its utilization(3,7), and the different responses these markers have to similar methodologies(17,18), the results on the variation in the biochemical markers not always follow the changes that happen in the BMD along the training period(17). On the other hand, there is a possibility that it occurs an increase in the concentration of those markers, with no response on the BMD(13). Pruitt et al.(13) suggest that the increase in the bone turnover markers concentration may be an early adaptation to the increasing BMD. However, another limitation that happens in using such method is that the response of the markers might represent a mean of the total body bone remodeling, rather than the spots that suffered the major overload during the physical activity. Due to such limitations, definitive conclusions related to the influence of the strength training or different sportive modalities in the bone remodeling assessed through such method still need further studies.
Chart 3 presents some studies using the biochemical markers for the bone metabolism in order to assess the effects of the physical activity on the BMD. However, due to the apparent limitations and discrepancies observed, further studies are needed in order to attain some conclusions on the effects of the physical exercising on the bone remodeling through this method.
6. BMD, MUSCULAR STRENGTH, AND BODY COMPOSITION
Some of the studies previously mentioned in this review, among others, have searched to assess the association between the muscular strength and the body composition to the BMD, as regardless the type of the physical activity performed, it seems to be a relationship between the strength development and the body composition and BMD(3,15,19,25,36). In general, these studies show positive correlations that range related to their level, and it have appeared some discrepancies as to the nature of such associations.
According to Hugues et al.(25), if there is a relationship between the muscular strength and the BMD, possibly the magnitude of the muscular contraction has impact at the bone spots that are anatomic related to the muscles performing the contraction. These authors suggest that the body weight may be an important factor to determine the BMD due to the compression strengths applied over the bones sustaining the body overload.
On the other hand, Madsen et al.(19) suggest that the body weight composition, including the lean and fat masses, might be more important than the body weight individually, suggesting that the fat, as a substrate to the conversion of the androgen to estrogen(26) may be related to the BMD both due to hormonal factors because of their importance in regulating sexual hormones in the BMD(5,24), and to mechanical factors. Related to the lean mass, it can be related to the BMD because although they are structurally independent, both respond to the same atrophy and hypertrophy stimuli(25).
Another relevant aspect, although not very clear, is that the associations between the BMD and the body composition and/or muscular strength suffer influence of factors such as gender(36), training level(29), and hormonal homeostasis(10).
Although there is a major relationship between the lean mass and the muscular strength(37,41,42), the associations between the lean mass and BMD not necessarily reflects the relationship observed between the muscular strength and BMD(10,25,29). Hughes et al.(25) suggest that the strength would be an independent factor to the BMD, while Madsen et al.(19) suggest that this variable would be consequence of the lean mass, and this last one would be more associated to the BMD.
Despite the different points of view among some authors on which variable (strength or lean mass) is more related to the BMD(19,25), the major part of the studies mentioned in this topic have investigated and found some correlation of the BMD with the muscular strength and some variable related to the body composition (that means, lean and fat mass)(10,19,25,29), suggesting that all these variables are strongly related to the BMD, varying only the level of these associations.
It is appropriate to point out that there are studies mentioned in this review presenting very low correlation levels between the BMD, the muscular strength, and the body composition components(19,25), and therefore, it is difficult to reach a conclusion from their results.
The differences observed in the associations investigated in the previously mentioned studies appear to exist due to different assessment methodologies. Besides, other factors such as hormonal regulation, training level, and gender seem to influence the level of these associations. Thus, maybe it is necessary to conduct further studies in order to determine on which population the body composition and the muscular strength are more associated to the BMD, and if the muscular strength is a variable that is dependant or not from the lean mass in its association to the BMD. Despite the limited conclusions, high levels of BMD are generally associated to the high lean mass or muscular strength levels, and the muscular strength may have a benefic effect on the BMD.
7. CONCLUSIONS AND IMPLICATIONS
Although factors such as genetics, hormonal homeostasis and food may be determinant to the BMD(15), the level of the physical activity seems to be an important influence on this variable. Despite the physiological mechanism is not completely clarified, the osteogenic action of the physical activity seems to be mediated through the bone piezoelectric effect (Brighton et al. apud Menker et al.)(18).
Some studies have shown that individuals who practice higher overload sportive modalities provoked by the body weight or with higher utilization level of the muscular strength have a major BMD(1,5,15,16,19). The level of the bone adaptation through the exercise seems to be dependent from the overload(29), and seems to be specific for the spots that are submitted to a major stress(15,28).
In other studies, the effect of the physical activity on the BMD was investigated in individuals submitted to the ST, showing that such intervention is effective to increase the BMD in some of them(3,17), while in others, no discrepancy was observed(2). These discrepancies may occur due to different training methodologies used by researchers or even to the sampling features (that is, high initial BMD)(13). Nevertheless, although there are discussions as to which training variable would be the most important to stimulate the bone remodeling (that means, intensity, volume), high intensity ST seems to be more effective(3).
The use of the bone metabolism biochemical markers has been used by some authors as a possibly more dynamic mean to assess the effects of the physical exercise on the bone metabolism(1). The variation found in the concentrations of these markers would possibly be precursor of the changes in the BMD(3). In this event, the measurement of these concentrations become important in order to assess the optimum physical training methods aiming to attain an increase in the BMD, having in mind that higher concentrations of markers to the bone turnover may suggest an effective training not yet translated to the densitometry values (g/cm2). However, due to the differences found in the results of some trials, it is necessary to conduct further studies in order to attain a more accurate assessment of the bone remodeling through biochemical markers.
Some studies have been demonstrated a strong relationship of the BMD to variables connected to the health, such as the muscular strength(10,29) and body composition, thus suggesting that regardless the physical activity performed, individuals with major muscular strength and lean mass might pursue major BMD, although the body fat is also related to the bone mass due to hormonal factor(6,16,19).
Nevertheless, even before such relationships, their level and nature are not completely clarified, as it was shown by the heterogeneity of the results found in the studies mentioned in this review(10,19,25,29).
To determine what type of physical activity is ideal to increase the bone mass peak during the adolescence or even with the purpose to keep it in the adult age is very important to prevent and possibly treat the osteoporosis, whose incidence occurs mainly in postmenopausal women(5). Besides, the associations of the BMD to the muscular strength and body composition suggest that the prescription of a training aiming to improve these parameters may have a benefic effect on the BMD.
1. Creighton DL, Morgan AL, Boardley D, Brolinson PG. Weight-bearing exercise and markers of bone turnover in female athletes. J Appl Physiol 2001;90:565-70. [ Links ]
2. Bemben DA, Fetters NL, Bemben MG, Nabavi N, Koh ET. Musculoskeletal responses to high- and low-intensity resistance training in early postmenopausal women. Med Sci Sports Exerc 2000;32:1949-57. [ Links ]
3. Vincent KR, Braith RW. Resistance training and bone turnover in elderly men and women. Med Sci Sports Exerc 2002;34:17-23. [ Links ]
4. Ganong WF. Fisiologia Médica. 19ª rev. ed. São Paulo: McGraw Hill Companies, 1999. [ Links ]
5. Maïmoun L, Lumbroso S, Manetta J, Paris F, Leroux JL, Sultan C. Testosterone is significantly reduced in endurance athletes without impact on bone mineral density. Horm Res 2003;59:285-92. [ Links ]
6. Burrows M, Nevill AM, Bird S, Simpson D. Physiological factors associated with low bone mineral density in female endurance runners. Br J Sports Med 2003; 37:67-71. [ Links ]
7. Humphries B, Newton RU, Bronks R, Marshall S, McBride J, McBride TT, et al. Effect of exercise intensity on bone density, strength, and calcium turnover in older women. Med Sci Sports Exerc 2000;32:1043-50. [ Links ]
8. Ryan AS, Ivey FM, Hurlubut DE, Martel GF, Lemmer JT, Sorkin JD, et al. Regional bone mineral density after resistive training in young and older men and women. J Appl Physiol 2004;14:16-23. [ Links ]
9. Heinonen A, Kannus P, Sievänen H, Pasanen M, Oja P, Vuori I. Good maintenance of high-impact activity-induced bone gain by voluntary, unsupervised exercises: an 8-month follow-up a randomized controlled trial. J Bone Miner Res 1999;14:125-8. [ Links ]
10. Helge EW, Kanstrup IL. Bone density in female gymnasts: impact of muscle strength and sex hormones. Med Sci Sports Exerc 2002;34:174-80. [ Links ]
11. Kemmler W, Engelke K, Lauber D, Weineck J, Hensen J, Kalender WA. Exercise effects on fitness and bone mineral density in early postmenopausal women: 1-year EFOPS results. Med Sci Sports Exerc 2002;34:2115-23. [ Links ]
12. Mackelvie KJ, McKay HA, Khan KM, Crocker PR. Life-style risk factors for osteoporosis in Asian and Caucasian girls. Med Sci Sports Exerc 2001;33:1818-24. [ Links ]
13. Pruitt LA, Jackson RD, Bartels RL, Lehnhard HJ. Weight training effects on bone mineral density in early postmenopausal women. J Bone Miner Res 1992;7: 179-85. [ Links ]
14. Rikli RE, McManis BG. Effects of exercise on bone mineral content in postmenopausal women. Res Q Exerc Sport 1990;61:243-9. [ Links ]
15. Andreoli A, Monteleone M, Van Loan M, Promenzio L, Tarantino U, De Lorenzo A. Effects of different sports on bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc 2001;33:507-11. [ Links ]
16. Evans EM, Prior BM, Arngrimsson SA, Modlesky CM, Cureton KJ. Relation of bone mineral density and content to mineral content and density of the fat free mass. J Appl Physiol 2001;91:2166-72. [ Links ]
17. Ryan AS, Treuch MS, Rubin MA, Miller JP, Nicklas BJ, Landis DM, et al. Effects of strength training on bone mineral density: hormonal and bone turnover relationships. J Appl Physiol 1994;77:1678-84. [ Links ]
18. Menkes A, Mazel S, Redmond RA, Koffler K, Libanati CR, Gundemberg CM, et al. Strength training increases regional bone mineral density and bone remodeling in middle-aged and older men. J Appl Physiol 1993;74:2478-84. [ Links ]
19. Madsen KL, Adams WC, Van Loan MD. Effects of physical activity, body weigth and composition, and muscular strength on bone density in young women. Med Sci Sports Exerc 1998;30:114-20. [ Links ]
20. Brentano MA. Efeitos do treinamento de força e do treinamento em circuito na força e ativação muscular, no consumo máximo de oxigênio e densidade mineral óssea de mulheres pós-menopáusicas com perda óssea. Dissertação de Mestrado, UFRGS, Porto Alegre, 2004. [ Links ]
21. Jessup JV, Horne C, Vishen RK. Wheeler D. Effects of exercise on bone density, balance, and self-efficacy on older women. Biol Res for Nurs 2003;4:171-80. [ Links ]
22. Kerr D, Ackland T, Maslen B, Morton A, Prince R. Resistance training over 2 years increase bone mass in calcium-replete in postmenopausal women. J Bone Miner Res 2001;16:170-81. [ Links ]
23. Liu L, Maruno R, Mashimo T, Sanka K, Higuchi T, Hayashi K, et al. Effects of physical training on cortical bone at midtibia assessed by peripheral QCT. J Appl Physiol 2003;95:219-24. [ Links ]
24. Gremion G, Rizzoli R, Sloman D, Theintz G, Bonjour J-P. Oligo-amenorrheic long-distance runners may lose more bone in spine than in femur. Med Sci Sports Exerc 2001;33:15-21. [ Links ]
25. Hughes VA, Frontera WR, Dallal GE, Fischer EC, Evans WJ. Muscle strength and body composition: associations with bone density in older subjects. Med Sci Sports Exerc 1995;27:967-74. [ Links ]
26. Blain H, Vuillemin A, Guillemin F, Durant R, Hanesse B, De Talance N, et al. Serum leptin level is a predictor of bone mineral density in post menopausal women. J Clin Endocrinol Metabol 2002;87:1030-5. [ Links ]
27. Cullen DM, Smith RT, Akhter MP. Bone-loading response varies with strain magnitude and cycle number. J Appl Physiol 2001;91:1971-6. [ Links ]
28. Morris FL, Smith RM, Payne WR, Galloway MA, Wark JD. Compressive and shear force generated in the lombar spine of female rowers. Int J Sports Med 2000;21:518-23. [ Links ]
29. Sandström P, Jonsson P, Lorentzon R, Thorsen K. Bone mineral density and muscle strength in female ice hockey players. Int J Sports Med 2000;21:524-8. [ Links ]
30. Cussler EC, Lohman TG, Going SB, Houtkooper LB, Metcalfe LL, Flint-Wagner HG, et al. Weight lifted in strength training predicts bone change in postmenopausal women. Med Sci Sports Exerc 2003;35:10-7. [ Links ]
31. Kohrt WM, Ehsani AA, Birge SJ Jr. HRT preserves increases in bone mineral density and reductions in body fat after a supervised exercise program. J Appl Physiol 1998;84:1505-12. [ Links ]
32. Hawkins SA, Schroeder T, Wiswel RA, Jaque SV, Marcell TJ, Costa K. Eccentric muscle action increases site specific osteogenic response. Med Sci Sports Exerc 1999;31:1287-92. [ Links ]
33. Nichols DL, Sanborn CF, Love AM. Resistance training and bone mineral density in adolescent females. J Pediatr 2001;139:494-500. [ Links ]
34. Villareal DT, Binder EF, Yarasheski KE, Williams DB, Brown M, Sinacore DR, et al. Effects of exercise training added to ongoing hormone replacement therapy on bone mineral density in frail elderly women. J Am Geriatr Soc 2003;51:985-90. [ Links ]
35. Peterson SE, Peterson MD, Raymond G, Gilligan C, Checovich MM, Smith EL. Muscular strength and bone mineral density with weigth training in middle-aged women. Med Sci Sports Exerc 1991;23:499-504. [ Links ]
36. Ribom E, Ljunggren O, Piehl-Aulin K, Ljunghall S, Bratteby Lf, Smuelson G, et al. Muscle strength correlates with total body bone mineral density in young women but not in men. Scand J Med Sci Sports 2004;14: 24-9. [ Links ]
37. Kraemer WJ, Fleck SJ, Evans WJ. Strength and power training: Physiological mechanisms of adaptation. Exer Sport Sci Rev 1996;24:363-97. [ Links ]
38. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Halkjaer-Kristensen J, Dyhre-Poulsen P. Neural inhibition during maximal eccentric and concentric quadriceps contraction: effects of resistance training. J Appl Physiol 2000;89:2249-57. [ Links ]
39. Fleck SJ, Kraemer WJ. Fundamentos do treinamento de força muscular. 2ª rev. ed. Porto Alegre: ArtMed, 1997. [ Links ]
40. Hortobágyi T, Hill J, Houmard JA, Fraser DD, Lambert NJ, Israel RG. Adaptative responses to muscle lengthening and shortening in humans. J Appl Physiol 1996; 80:765-72. [ Links ]
41. Hickner RC, Mehta PM, Dyck D, Devita P, Houmard JA, Koves T, et al. Relationship between fat-to-fat-free mass ratio and decrements in the leg strength after downhill running. J Appl Physiol 2001;90:1334-41. [ Links ]
42. Roemich JN, Sinning WE. Weight loss and wrestling training: effects on nutrition, growth, maturation, body composition and strength. J Appl Physiol 1997; 82:1751-9. [ Links ]
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Received in 10/12/04. Final version received in 8/8/05. Approved in 5/9/05.
All the authors declared there is not any potential conflict of interests regarding this article.