Body composition, strength static and isokinetic, and bone health: comparative study between active adults and amateur soccer players

Óscar M. Tavares João P. Duarte André O. Werneck Daniela C. Costa Paulo Sousa-e-Silva Diogo Martinho Leonardo G. O. Luz Pedro Morouço João Valente-dos-Santos Rui Soles-Gonçalves Jorge Conde José M. Casanova Manuel J. Coelho-e-Silva About the authors

ABSTRACT

Objective:

To compare tissue composition, total and regional bone mineral content and bone mineral density, static hand grip and knee joint isokinetic strength between amateur soccer players and Control Group.

Methods:

Cross-sectional study. Air displacement plethysmography was used to estimate body volume and, in turn, density. Body composition, bone mineral content and bone mineral density were assessed for the whole body and at standardized regions using dual energy X-ray absorptiometry. Static grip strength was assessed with an adjustable dynamometer, and peak torque derived from isokinetic strength dynamometer (concentric muscular knee actions at 60°/s). Magnitude of the differences between groups was examined using d-Cohen.

Results:

Compared to healthy active adults, soccer players showed larger values of whole body bone mineral content (+651g; d=1.60; p<0.01). In addition, differences between groups were large for whole body bone mineral density (d=1.20 to 1.90; p<0.01): lumbar spine, i.e. L1-L4 (+19.4%), upper limbs (+8.6%) and lower limbs (+16.8%). Soccer players attained larger mean values in strength test given by static hand grip protocol (+5.6kg, d=0.99; p<0.01).

Conclusion:

Soccer adequately regulates body composition and is associated better bone health parameters (bone mineral content and density at whole-body and at particular sites exposed to mechanical loadings).

Keywords:
Sports; Isokinetic dynamometer; Body composition; Muscle strength

RESUMO

Objetivo:

Comparar a composição de tecidos, o conteúdo mineral ósseo e a densidade mineral óssea totais e por regiões do corpo, a força de preensão manual estática, e força isocinética da articulação do joelho, entre um grupo de jogadores de futebol amadores e um Grupo Controle.

Métodos:

Estudo transversal utilizando pletismografia de ar deslocado para estimar o volume corporal, para subsequente cálculo da densidade corporal. A composição de tecidos, o conteúdo mineral ósseo e a densidade mineral óssea foram avaliados para o corpo todo e regiões padronizadas através da absorciometria de raios-X de dupla energia. A força de preensão manual estática foi avaliada por um dinamômetro ajustável. Os momentos máximos de força das ações musculares concêntricas para os extensores e flexores do joelho foram avaliados pela dinamometria isocinética (60°/s). Foi calculado o valor d-Cohen para apreciar a magnitude do efeito das diferenças entre grupos.

Resultados:

Os futebolistas apresentaram níveis superiores de conteúdo mineral ósseo em comparação com os adultos ativos do Grupo Controle (+651g; d=1,60; p<0,01) e obtiveram valores superiores de densidade mineral óssea (d: 1,20 a 1,90; p<0,01) para a coluna lombar, L1-L4 (+19,4%), membros superiores (+8,6%) e membros inferiores (+16,8%). Para a força de preensão (estática) a diferença foi moderada (d=0,99; p<0,01) com valores mais elevados apresentados pelo futebolistas (+5,6kg; d=0,99; p<0,01).

Conclusão:

A prática de futebol promove uma regulação adequada da composição corporal (tecidos magro e gordo) e ganhos na densidade mineral óssea, mais acentuada em partes do corpo com maior exposição aos impactos mecânicos da atividade motora.

Descritores:
Esportes; Dinamômetria isocinética; Composição corporal; Força muscular

INTRODUCTION

Physical activity corresponds to the movement produced by skeletal muscle and entails daily energy expenditure in three different contexts, namely daily living, occupational and leisure activities. Obesity and related chronic metabolic disorders have been attracting significant attention from a public health perspective.(11. Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN, Katzmarzyk PT; Lancet Physical Activity Series Working Group. Effect of physical inactivity on major non-communicable diseases worldwide: an analysis of burden of disease and life expectancy. Lancet. 2012;380(9838):219-29.,22. NCD Risk Factor Collaboration (NCD-RisC). Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016; 387(10026):1377-96. Review. Erratum in: Lancet. 2016;387(10032):1998.) Not surprisingly, the battle against obesity and physical inactivity, in particular, have led to the emergence of a preventive paradigm in behavioral medicine, which focuses on lifestyle rather than communicable diseases factors. A high value is attributed to interventions aimed to promote physical activity,(33. Dietz WH, Baur LA, Hall K, Puhl RM, Taveras EM, Uauy R, et al. Management of obesity: improvement of health-care training and systems for prevention and care. Lancet. 2015;385(9986):2521-33. Review.) and special emphasis is placed on high-intensity activities, which are more effective for body composition regulation.(44. Janssen I, Ross R. Vigorous intensity physical activity is related to the metabolic syndrome independent of the physical activity dose. Int J Epidemiol. 2012; 41(4):1132-40.)

Adiposity, especially in adult life, may lead to several metabolic disorders, which are risk factors for metabolic syndrome(55. Castanheira M, Chor D, Braga JU, Cardoso LO, Griep RH, Molina MD, et al. Predicting cardiometabolic disturbances from waist-to-height ratio: findings from the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil) baseline. Public Health Nutr. 2018;21(6):1028-35.) and cardiovascular disease-related mortality.(66. Abramowitz MK, Hall CB, Amodu A, Sharma D, Androga L, Hawkins M. Muscle mass, BMI, and mortality among adults in the United States: A population-based cohort study. PLoS One. 2018;13(4):e0194697. Erratum in: PLoS One. 2018;13(5):e0198318.) In contrast, lean mass appears to be protective against cardiovascular disease-related mortality.(66. Abramowitz MK, Hall CB, Amodu A, Sharma D, Androga L, Hawkins M. Muscle mass, BMI, and mortality among adults in the United States: A population-based cohort study. PLoS One. 2018;13(4):e0194697. Erratum in: PLoS One. 2018;13(5):e0198318.) Also, muscle mass development may partially attenuate the association between higher adiposity and cardiovascular diseases,(66. Abramowitz MK, Hall CB, Amodu A, Sharma D, Androga L, Hawkins M. Muscle mass, BMI, and mortality among adults in the United States: A population-based cohort study. PLoS One. 2018;13(4):e0194697. Erratum in: PLoS One. 2018;13(5):e0198318.) being an important component of adult health.

Moreover, bone health is another relevant issue in modern society, given the growing population aging and the resulting loss of functional autonomy, with high impact on the quality of life of older adults and significant healthcare, social and familiar implications. Researches investigating associations between functional indicators, body composition and bone health parameters are increasingly being undertaken, and emphasize the holistic view of health and quality of life.

Even during aging, women have a higher risk of fractures due to decreased periosteal apposition,(77. Duan Y, Turner CH, Kim BT, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. 2001;16(12):2267-75.) men aged over 50 years have a 27% risk of osteoporotic fracture.(88. Cooley H, Jones G. A population-based study of fracture incidence in southern Tasmania: lifetime fracture risk and evidence for geographic variations within the same country. Osteoporos Int. 2001;12(2):124-30.) Physical activity has been consistently associated with metabolic, mental and cardiovascular health benefits, regardless of age and sex, and the same holds true for bone health indicators. Increased bone mineral content (BMC) in response to muscular strength exercise is somewhat of a consensus, and mechanical load is thought to play a significant role in bone strengthening.(99. Nilsson M, Ohlsson C, Mellström D, Lorentzon M. Previous sport activity during childhood and adolescence is associated with increased cortical bone size in young adult men. J Bone Miner Res. 2009;24(1):125-33.1111. Morel J, Combe B, Francisco J, Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12(2):152-7.) However, associations between sports practice and bone health remain unclear - both from a tissue component and specific strength test (relatively to tested muscle groups and forms of manifestation of static and isokinetic forces perspective).(1212. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8(8):457-65. Review.,1313. Lau RW, Liao LR, Yu F, Teo T, Chung RC, Pang MY. The effects of whole body vibration therapy on bone mineral density and leg muscle strength in older adults: a systematic review and meta-analysis. Clin Rehabil. 2011;25(11): 975-88. Review.)

OBJECTIVE

To compare fat and lean tissue mass, mineral bone content and density, and physical fitness indicators between experienced amateur competitive soccer players and physically active young adults of similar age but not involved in officially recognized sports.

METHODS

Data collection was carried out in compliance with international ethical standards with humans,(1414. Harriss DJ, Atkinson G. Ethical Standards in Sport and Exercise Science Research: 2016 Update. Int J Sports Med. 2015;36(14):1121-4.) after approval by the Ethics Committee of the Universidade de Coimbra (CE/FCDEF-UC/00102014). All participants were informed about the aims, the protocol and procedures, and signed written informed consent. Participation was voluntary and each participant could withdraw at any time.

Sample

The sample comprised 66 male adults aged 18.5 to 29.9 years, allocated in one of two groups: healthy adults (G1, n=35) and amateur soccer players (G2, n=31). At the G1 participants had no means of transport, kept on average more than 10 thousand steps per day, had no diseases, including neuromuscular limitations, and no sports practice over the last 5 years or longer (participation in school sports was limited to one subject). The G2 was locally recruited (i.e., third national division). Soccer practice experience (years) was provided by the selected clubs and confirmed by the respective Association. Inclusion criteria for G2 were as follows: minimum of 4 years of participation in competitive soccer; at least four weekly training sessions in clubs registered at Federação Portuguesa de Futebol. The mean soccer practice experience in the G2 was 14.5±4.2 years.

Anthropometric measurements

Height was measured to the nearest 0.1cm using a stadiometer (Harpenden Stadiometer 98.603, Holtain Ltd., Crosswell, UK).

Air-displacement plethysmography

Body volume and body density were determined using a Bod Pod Body Composition System (model Bod Pod 2006, Life Measurement, Inc., Concord, USA). Body mass was determined to the nearest 0.1kg using an electronic scale connected to the Bod Pod system. Calibration was performed prior to individual test, using a 50.225L cylinder. Participants wore lycra swimsuit and a cap and were tested, sited in the chamber of the Bod Pod, motionless while the system estimated the body volume two consecutive times and, when necessary, three times, considered valid if their difference was less than 150mL. Thoracic gas volume was predicted based on body volume. Body density (body mass/body volume) was calculated and then used for the estimation of the fat tissue percentage.(1515. Siri WE. Body composition from fluid spaces and density: analysis of methods. Nutrition. 1961;9(5):480-91, discussion 480, 492.) A single and experienced investigator performed measurements.

Dual-energy X-ray absorptiometry

Body composition parameters were measured using dual-energy X-ray absorptiometry (DXA), with patients being assessed in the supine position. A Lunar (DPX-PRO/NT/MD+ DXA) machine was used for lean tissue mass (LTM), fat tissue mass (FTM), BMC and bone mineral density (BMD) quantification. An experienced technician acted in a certified clinic and performed all measurements.

Handgrip dynamometry (static strength)

Upper limb isometric strength was assessed using a mechanical dynamometer (Hand Dynamometer, Lafayette 78010, USA). Maximal handgrip strength (kg) was measured bilaterally with limbs unsupported.

Isokinetic dynamometry

Isokinetic testing (Biodex System 3, Shirley, New York, USA) of knee extensor and flexor muscles was performed in concentric mode (CON), at 60°/s-1 angular velocity. Participants were assessed in the sitting position with the lever arm aligned with the lateral epicondyle of the knee and the stabilization strap positioned over the tibiotarsal joint, 3 to 5cm distant from the lateral malleolus of the tibia. Participants were instructed to keep their hands on their shoulders throughout the test. The range of motion was defined according to maximal voluntary extension (0° to 90° knee flexion). Lever arm calibration was performed at the start of each measurement for gravity effect correction (at 30 degrees position). Participants were instructed to perform the maximum voluntary muscle contraction. One set of five consecutive maximum intensity knee extension and flexion repetitions were performed and the peak torque (PT in N.m) recorded. Warm up consisted of cycling exercise (Monark Ergomedic 894E Peak Bike, Monark AB, Varberg, Sweden) with minimal resistance (≤60rpm), three static stretching exercises (20 seconds) for the quadriceps, hamstring and adductor muscles, and three standardized extension/flexion repetitions at the test velocity. Data filtering and curves windowing were performed using AcqKnowledge software, version 4.1 (Biopac Systems, Inc., California, USA).

Statistical analysis

Descriptive statistics (range, mean, standard error of the mean, 95% confidence interval of the mean and standard deviation) were calculated for the overall sample. Data normality was tested using the Kolmogorov-Smirnov test. The effect size of intergroup comparisons was estimated using Cohen's d. Statistical analyses were performed using IBM Statistical Package for Social Science (SPSS) version 22.0 (SPSS, Inc., Chicago, Ilinois, USA) and the level of significance set at 5%.

RESULTS

Table 1 summarized descriptive statistics for anthropometry (including air displacement plethysmography), DXA whole body and regional body composition, and parameters extracted from handgrip and isokinetic dynamometry. Several variables violated the assumption of normal distribution reflecting intergroup heterogeneity.

Table 1
Descriptive statistics and test for normal distribution

Characteristics of the healthy adults (G1) and soccer players (G2) are presented in table 2. Soccer players had significantly higher body density (+0.016L/kg; d=1.22). Healthy adults displayed higher percentages of fat tissue at the different regions of interest (d=0.67 to 1.67) and lean soft tissue (d=1.39) at the lower limbs. Soccer players had significantly greater BMC (+651g; d=1.60) and BMD (lumbar L1 - L4: +0.24g/cm2; +19.4%; d=1.90; upper limbs: +0.09g/cm2; +8.6%; d=1.20; lower limbs: +0.27g/cm-2; +16.8%; d=1.90) than healthy adults as shown in figure 1. Soccer players attained better performance in the static grip strength (+ 5.6kg; d=0.99).

Table 2
Descriptive statistics by group and mean differences on anthropometry and functional variable means
Figure 1
Lumbar spine, upper and lower limb bone mineral density differences between healthy adults and adult amateur soccer players

DISCUSSION

Intrinsic (e.g., sex and age) and extrinsic (e.g., diet and physical exercise) factors have been associated with bone mass differences.(1616. Glaser DL, Kaplan FS. Osteoporosis. Definition and clinical presentation. Spine (Phila Pa 1976). 1997;22(24 Suppl):12S-6S. Review.) Extrinsic factors may be regulated according to individual health. In this study, body composition, bone health and functional parameters were compared between active healthy adults not practicing any particular sport and amateur competitive soccer players. Major findings suggest that soccer practice, which is associated with mechanical loads, promote largely whole body BMC and moderately whole body BMD increase, with more significant increments (effect size) in specific regions (lumbar spine and appendicular regions, i.e., upper and lower limbs). This is true even when the effect size of differences in forms of muscle effort is low (trivial or moderate). Also, higher fat tissue mass indices in healthy adults suggest specific sports programs may impact energy balance, and therefore the maintenance of ideal body mass, or promote improvement of bone health indicators, which persist even when sports practice is not associated with high levels of competition and relevant functional differences between sports practitioners and physically active healthy adults are lacking.

Findings of this study confirm results of previous study(1717. Wittich A, Mautalen CA, Oliveri MB, Bagur A, Somoza F, Rotemberg E. Professional football (soccer) players have a markedly greater skeletal mineral content, density and size than age- and BMI-matched controls. Calcif Tissue Int. 1998;63(2):112-7.) reporting 12% higher whole body BMD in soccer players compared to controls. However, contrary to expectations, isokinetic strength did not differ between groups. Similar isokinetic strength across individuals in this sample indicates their respective levels of physical activity was sufficient to induce quantitative and functional muscle adaptations in all cases, and suggests bone adaptations require higher levels of specific stimuli (i.e., mechanical impact).(99. Nilsson M, Ohlsson C, Mellström D, Lorentzon M. Previous sport activity during childhood and adolescence is associated with increased cortical bone size in young adult men. J Bone Miner Res. 2009;24(1):125-33.) Higher strength values in soccer players compared to healthy adults support the premise that the user-friendly handgrip test has good diagnostic capability regarding overall musculoskeletal status, and may also be used for brief assessment of undernourished groups.(1818. Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A Jr, Orlandini A, Seron P, Ahmed SH, Rosengren A, Kelishadi R, Rahman O, Swaminathan S, Iqbal R, Gupta R, Lear SA, Oguz A, Yusoff K, Zatonska K, Chifamba J, Igumbor E, Mohan V, Anjana RM, Gu H, Li W, Yusuf S; Prospective Urban Rural Epidemiology (PURE) Study investigators. Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet. 2015;386(9990):266-73.)

Bone mineral content did not differ significantly in one study comparing soccer players and runners.(1919. Milanović Z, Pantelić S, Kostić R, Trajković N, Sporiš G. Soccer vs. running training effects in young adult men: which programme is more effective in improvement of body composition? Randomized controlled trial. Biol Sport. 2015;32(4):301-5.) Nonetheless, in this study soccer players were compared with active healthy adults not necessarily involved in any specific sports practice. Being a high mechanical impact sport, soccer may be assumed to promote increased BMC and BMD from an early age.(2020. Vlachopoulos D, Barker AR, Ubago-Guisado E, Fatouros IG, Knapp KM, Williams CA, et al. Longitudinal Adaptations of Bone Mass, Geometry, and Metabolism in Adolescent Male Athletes: the PRO-BONE Study. J Bone Miner Res. 2017;32(11):2269-77.) Higher BMC and BMD values in response to soccer practice may have occurred via different pathways. Firstly, the mechanical impact associated with this particular sport must be accounted for. Secondly, soccer is played outdoors, therefore soccer players tend to have higher vitamin D levels, which is associated with higher BMC and BMD.(2121. Allison RJ, Farooq A, Cherif A, Hamilton B, Close GL, Wilson MG. Why don't serum vitamin D concentrations associate with BMD by DXA? A case of being “bound” to the wrong assay? Implications for vitamin D screening. Br J Sports Med. 2017;52(8):522-6.) Finally, given the recreational nature of soccer playing among participants of this study, their training volume was also higher, which is another factor associated with higher BMC and BMD.(2222. Agostinete RR, Maillane-Vanegas S, Lynch KR, Turi-Lynch B, Coelho-E-Silva MJ, Campos EZ, et al. The impact of training load on bone mineral density of adolescent swimmers: a structural equation modeling approach. Pediatr Exerc Sci. 2017;29(4):520-8.)

An inverse association between lean and fat tissue mass in different body segments could be observed, which can be derived from high intensity sprints, jumps, accelerations and decelerations associated with soccer practice.(2323. Carling C, Orhant E. Variation in body composition in professional soccer players: interseasonal and intraseasonal changes and the effects of exposure time and player position. J Strength Cond Res. 2010;24(5):1332-9.) Although soccer players had less lean tissue mass compared to active adults, they also had about three times less lower limb fat, suggesting a higher lean/fat tissue ratio in this group. This finding emphasizes the relevance of physical activity regimens with varying intensity, acyclic movement patterns and mechanical impact components. One study with 88 peripubertal female participants (6 to 11 years; 30 highly competitive gymnasts training 16 hours per week on average, 29 gymnasts training 1 to 5 hours per week, and 29 youth not practicing gymnastics)(2424. Burt LA, Naughton GA, Greene DA, Courteix D, Ducher G. Non-elite gymnastics participation is associated with greater bone strength, muscle size, and function in pre- and early pubertal girls. Osteoporos Int. 2012;23(4):1277-86.) and evaluating lean tissue mass, upper limb BMC and BMD, forearm bone geometry and results of three upper limb functional performance tests concluded that gymnasts with more modest training regimens achieved higher functional performance and had more favorable bone tissue geometry and resilience values, while total muscle mass and maximum forearm muscle cross-sectional area were larger in the elite gymnast group.

Results of the present study have clear practical applications. Having in mind the high incidence and prevalence of osteoporotic injuries(2525. Hernlund E, Svedbom A, Ivergård M, Compston J, Cooper C, Stenmark J, et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos. 2013;8:136. Review.,2626. Stevens JA, Rudd RA. The impact of decreasing U.S. hip fracture rates on future hip fracture estimates. Osteoporos Int. 2013;24(10):2725-8.) and the growing rates of obesity globally,(22. NCD Risk Factor Collaboration (NCD-RisC). Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016; 387(10026):1377-96. Review. Erratum in: Lancet. 2016;387(10032):1998.) sports practice may not only enhance BMC and BMD but also reduce body fat. Soccer is a largely practiced high impact, high intensity sport(2727. Mithoefer K, Williams RJ 3rd, Warren RF, Wickiewicz TL, Marx RG. High-impact athletics after knee articular cartilage repair: a prospective evaluation of the microfracture technique. Am J Sports Med. 2006;34(9):1413-8.) and, according to findings of this study, should be sufficient to enhance BMD.

This study has some limitations. The use of a cross-sectional data derived from a relatively small sample comprising exclusively male adults limit the result extrapolation to other populations. Future investigations of similar differences in younger subjects and the inclusion of female individuals, with greater body size and composition variability, are warranted and should provide a starting point for the design of programs and interventions aimed at bone health promotion during growth, maturation and development in children and youth, with increased osteoporosis prevention potential. Also, the type of exercise performed by participants in both groups was not controlled, as the only criteria adopted were the practice of soccer and being physically active.

CONCLUSION

Soccer practice, even at the recreational level, may lead to an increased bone mineral content, bone mineral density, reduced body fat and greater handgrip strength. Soccer is a good intervention alternative for achievement and maintenance of ideal body mass, with added benefits regarding lean, fat and bone tissue composition.

ACKNOWLEDGMENTS

The Centro de Investigação do Desporto e Actividade Física (Research Unit for the Study of Sport and Physical Activity, uid/dtp/04213/2019) is being funded by Fundação para a Ciência e a Tecnologia. AOW is supported by São Paulo Research Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) process: 2017/27234-2.

REFERENCES

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    NCD Risk Factor Collaboration (NCD-RisC). Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet. 2016; 387(10026):1377-96. Review. Erratum in: Lancet. 2016;387(10032):1998.
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  • 4
    Janssen I, Ross R. Vigorous intensity physical activity is related to the metabolic syndrome independent of the physical activity dose. Int J Epidemiol. 2012; 41(4):1132-40.
  • 5
    Castanheira M, Chor D, Braga JU, Cardoso LO, Griep RH, Molina MD, et al. Predicting cardiometabolic disturbances from waist-to-height ratio: findings from the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil) baseline. Public Health Nutr. 2018;21(6):1028-35.
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    Abramowitz MK, Hall CB, Amodu A, Sharma D, Androga L, Hawkins M. Muscle mass, BMI, and mortality among adults in the United States: A population-based cohort study. PLoS One. 2018;13(4):e0194697. Erratum in: PLoS One. 2018;13(5):e0198318.
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    Duan Y, Turner CH, Kim BT, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. 2001;16(12):2267-75.
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    Cooley H, Jones G. A population-based study of fracture incidence in southern Tasmania: lifetime fracture risk and evidence for geographic variations within the same country. Osteoporos Int. 2001;12(2):124-30.
  • 9
    Nilsson M, Ohlsson C, Mellström D, Lorentzon M. Previous sport activity during childhood and adolescence is associated with increased cortical bone size in young adult men. J Bone Miner Res. 2009;24(1):125-33.
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    Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng. 2006;8:455-98. Review.
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    Morel J, Combe B, Francisco J, Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12(2):152-7.
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    Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8(8):457-65. Review.
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    Lau RW, Liao LR, Yu F, Teo T, Chung RC, Pang MY. The effects of whole body vibration therapy on bone mineral density and leg muscle strength in older adults: a systematic review and meta-analysis. Clin Rehabil. 2011;25(11): 975-88. Review.
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    Harriss DJ, Atkinson G. Ethical Standards in Sport and Exercise Science Research: 2016 Update. Int J Sports Med. 2015;36(14):1121-4.
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    Siri WE. Body composition from fluid spaces and density: analysis of methods. Nutrition. 1961;9(5):480-91, discussion 480, 492.
  • 16
    Glaser DL, Kaplan FS. Osteoporosis. Definition and clinical presentation. Spine (Phila Pa 1976). 1997;22(24 Suppl):12S-6S. Review.
  • 17
    Wittich A, Mautalen CA, Oliveri MB, Bagur A, Somoza F, Rotemberg E. Professional football (soccer) players have a markedly greater skeletal mineral content, density and size than age- and BMI-matched controls. Calcif Tissue Int. 1998;63(2):112-7.
  • 18
    Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A Jr, Orlandini A, Seron P, Ahmed SH, Rosengren A, Kelishadi R, Rahman O, Swaminathan S, Iqbal R, Gupta R, Lear SA, Oguz A, Yusoff K, Zatonska K, Chifamba J, Igumbor E, Mohan V, Anjana RM, Gu H, Li W, Yusuf S; Prospective Urban Rural Epidemiology (PURE) Study investigators. Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet. 2015;386(9990):266-73.
  • 19
    Milanović Z, Pantelić S, Kostić R, Trajković N, Sporiš G. Soccer vs. running training effects in young adult men: which programme is more effective in improvement of body composition? Randomized controlled trial. Biol Sport. 2015;32(4):301-5.
  • 20
    Vlachopoulos D, Barker AR, Ubago-Guisado E, Fatouros IG, Knapp KM, Williams CA, et al. Longitudinal Adaptations of Bone Mass, Geometry, and Metabolism in Adolescent Male Athletes: the PRO-BONE Study. J Bone Miner Res. 2017;32(11):2269-77.
  • 21
    Allison RJ, Farooq A, Cherif A, Hamilton B, Close GL, Wilson MG. Why don't serum vitamin D concentrations associate with BMD by DXA? A case of being “bound” to the wrong assay? Implications for vitamin D screening. Br J Sports Med. 2017;52(8):522-6.
  • 22
    Agostinete RR, Maillane-Vanegas S, Lynch KR, Turi-Lynch B, Coelho-E-Silva MJ, Campos EZ, et al. The impact of training load on bone mineral density of adolescent swimmers: a structural equation modeling approach. Pediatr Exerc Sci. 2017;29(4):520-8.
  • 23
    Carling C, Orhant E. Variation in body composition in professional soccer players: interseasonal and intraseasonal changes and the effects of exposure time and player position. J Strength Cond Res. 2010;24(5):1332-9.
  • 24
    Burt LA, Naughton GA, Greene DA, Courteix D, Ducher G. Non-elite gymnastics participation is associated with greater bone strength, muscle size, and function in pre- and early pubertal girls. Osteoporos Int. 2012;23(4):1277-86.
  • 25
    Hernlund E, Svedbom A, Ivergård M, Compston J, Cooper C, Stenmark J, et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos. 2013;8:136. Review.
  • 26
    Stevens JA, Rudd RA. The impact of decreasing U.S. hip fracture rates on future hip fracture estimates. Osteoporos Int. 2013;24(10):2725-8.
  • 27
    Mithoefer K, Williams RJ 3rd, Warren RF, Wickiewicz TL, Marx RG. High-impact athletics after knee articular cartilage repair: a prospective evaluation of the microfracture technique. Am J Sports Med. 2006;34(9):1413-8.

Publication Dates

  • Publication in this collection
    30 May 2019
  • Date of issue
    2019

History

  • Received
    07 Feb 2018
  • Accepted
    24 June 2018
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