A Cumulative Effect of Physical Training on Bone Strength in Males

Abstract

Weight-bearing, high-impact exercise, as opposed to nonimpact exercise, has been demonstrated to increase bone mineral density. This was traditionally demonstrated with dual energy X‐ray absorptiometry. Our objective was to assess the differences in bone properties, using quantitative ultrasound (QUS, Sunlight Omnisense™, Sunlight Medical, Ltd., Tel Aviv, Israel), in male athletes involved in a weight-bearing, impact sport (soccer, SC) or a nonimpact sport (swimming and water polo, AQ), compared with nonathletic control (C) males. A total of 266 boys and men, aged 8 - 23 years, were divided into children (11.1 ± 1.0 years; 34 SC, 34 AQ, 25 C), adolescents (14.7 ± 1.2 years; 32 SC, 31 AQ, 31 C), and young adults (19.8 ± 1.1 years; 31 SC, 24 AQ, 24 C) · Training experience varied between 1.5 years in the children to 15 years in the adults. Bone speed of sound (SOS) was measured bilaterally at the distal radius and the mid-tibia. Body fat was significantly lower in athletes compared with C. AQ were generally heavier and had a higher fat-free mass compared with SC and C, with no significant differences in height between groups. Radial SOS increased with age, but no differences were observed between activity groups or between the dominant (D) and nondominant (ND) arm. Tibial SOS also increased with age. In the children and adolescents, no differences were observed between activity groups. However, among adults, both SC and AQ had higher tibial SOS compared with C. These differences were mainly explained by differences in fat-free mass. Among young adults but not among children and adolescent males, both soccer and aquatic sports appear to be associated with higher bone SOS in the lower, but not the upper, extremities. Further studies are needed to assess possible sport-specific mechanisms which affect bone properties and to determine the minimal cumulative effect which is needed to influence bone properties.

Key words

Adolescence - boys - soccer - sport - swimming

References

• 1 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;  33 507-511
• 2 Bangsbo J. The physiology of soccer-with special reference to intense intermittent exercise.  Acta Physiol Scand Suppl. 1994;  619 1-155
• 3 Barkmann R, Kantorovich E, Singal C, Hans D, Genant H K, Heller M, Gluer C C. A new method for quantitative ultrasound measurements at multiple skeletal sites: first results of precision and fracture discrimination.  J Clin Densitom. 2000;  3 1-7
• 4 Block J E, Friedlander A L, Brooks G A, Steiger P, Stubbs H A, Genant H K. Determinants of bone density among athletes engaged in weight-bearing and non-weight-bearing activity.  J Appl Physiol. 1989;  67 1100-1105
• 5 Calbet J A, Dorado C, Diaz-Herrera P, Rodriguez-Rodriguez L P. High femoral bone mineral content and density in male football (soccer) players.  Med Sci Sports Exerc. 2001;  33 1682-1687
• 6 Daly R M, Rich P A, Klein R. Influence of high impact loading on ultrasound bone measurements in children: a cross-sectional report.  Calcif Tissue Int. 1997;  60 401-404
• 7 Duke P M, Litt I F, Gross R T. Adolescents' self-assessment of sexual maturation.  Pediatrics. 1980;  66 918-920
• 8 Duncan C S, Blimkie C J, Cowell C T, Burke S T, Briody J N, Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength.  Med Sci Sports Exerc. 2002;  34 286-294
• 9 Duppe H, Gardsell P, Johnell O, Ornstein E. Bone mineral density in female junior, senior and former football players.  Osteoporos Int. 1996;  6 437-441
• 10 Durnin J V, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years.  Br J Nutr. 1974;  32 77-97
• 11 Falk B, Bronshtein Z, Zigel L, Constantini N, Eliakim A. Higher tibial quantitative ultrasound in young female swimmers.  Br J Sports Med. 2004;  38 461-465
• 12 Falk B, Bronshtein Z, Zigel L, Constantini N W, Eliakim A. Quantitative ultrasound of the tibia and radius in prepubertal and early-pubertal female athletes.  Arch Pediatr Adolesc Med. 2003;  157 139-143
• 13 Falk B, Sadres E, Constantini N, Eliakim A, Zigel L, Foldes A J. Quantitative ultrasound (QUS) of the tibia: a sensitive tool for the detection of bone changes in growing boys.  J Pediatr Endocrinol Metab. 2000;  13 1129-1135
• 14 Foldes A J, Rimon A, Keinan D D, Popovtzer M M. Quantitative ultrasound of the tibia: a novel approach for assessment of bone status.  Bone. 1995;  17 363-367
• 15 Gluer C C, Wu C Y, Jergas M, Goldstein S A, Genant H K. Three quantitative ultrasound parameters reflect bone structure.  Calcif Tissue Int. 1994;  55 46-52
• 16 Gonnelli S, Cepollaro C, Gennari L, Montagnani A, Caffarelli C, Merlotti D, Rossi S, Cadirni A, Nuti R. Quantitative ultrasound and dual-energy X‐ray absorptiometry in the prediction of fragility fracture in men.  Osteoporos Int. 2005;  16 963-968
• 17 Hart K J, Shaw J M, Vajda E, Hegsted M, Miller S C. Swim-trained rats have greater bone mass, density, strength, and dynamics.  J Appl Physiol. 2001;  91 1663-1668
• 18 Hoshi A, Watanabe H, Chiba M, Inaba Y. Bone density and mechanical properties in femoral bone of swim loaded aged mice.  Biomed Environ Sci. 1998;  11 243-250
• 19 Jergas M, Uffmann M, Wittenberg R, Muller P, Koster O. Ultrasonic velocity measurements at weight-bearing and non-weight-bearing sites of the peripheral skeleton. The effect of physical activity in soccer players.  Rofo. 1992;  157 420-424
• 20 Karlsson M K, Magnusson H, Karlsson C, Seeman E. The duration of exercise as a regulator of bone mass.  Bone. 2001;  28 128-132
• 21 Lima F, De Falco V, Baima J, Carazzato J G, Pereira R M. Effect of impact load and active load on bone metabolism and body composition of adolescent athletes.  Med Sci Sports Exerc. 2001;  33 1318-1323
• 22 Litmanovitz I, Dolfin T, Friedland O, Arnon S, Regev R, Shainkin-Kestenbaum R, Lis M, Eliakim A. Early physical activity intervention prevents decrease of bone strength in very low birth weight infants.  Pediatrics. 2003;  112 15-19
• 23 Liu L, Maruno R, Mashimo T, Sanka K, Higuchi T, Hayashi K, Shirasaki Y, Mukai N, Saitoh S, Tokuyama K. Effects of physical training on cortical bone at midtibia assessed by peripheral QCT.  J Appl Physiol. 2003;  95 219-224
• 24 Lloyd T, Chinchilli V M, Johnson-Rollings N, Kieselhorst K, Eggli D F, Marcus R. Adult female hip bone density reflects teenage sports-exercise patterns but not teenage calcium intake.  Pediatrics. 2000;  106 40-44
• 25 Magnusson H, Linden C, Karlsson C, Obrant K J, Karlsson M K. Exercise may induce reversible low bone mass in unloaded and high bone mass in weight-loaded skeletal regions.  Osteoporos Int. 2001;  12 950-955
• 26 Institute of Medicine .Dietary Reference Intakes: Application in Dietary Assessment. Washington, DC; The National Academic Press 2000
• 27 Njeh C F, Hans D, Wu C, Kantorovich E, Sister M, Fuerst T, Genant H K. An in vitro investigation of the dependence on sample thickness of the speed of sound along the specimen.  Med Eng Phys. 1999;  21 651-659
• 28 Nordstrom A, Karlsson C, Nyquist F, Olsson T, Nordstrom P, Karlsson M. Bone loss and fracture risk after reduced physical activity.  J Bone Miner Res. 2005;  20 202-207
• 29 Rozen G S, Rennert G, Rennert H S, Diab G, Daud D, Ish-Shalom S. Calcium intake and bone mass development among Israeli adolescent girls.  J Am Coll Nutr. 2001;  20 219-224
• 30 Schonau E, Wentzlik U, Michalk D, Scheidhauer K, Klein K. Is there an increase of bone density in children?.  Lancet. 1993;  342 689-690
• 31 Schott A M, Weill-Engerer S, Hans D, Duboeuf F, Delmas P D, Meunier P J. Ultrasound discriminates patients with hip fracture equally well as dual energy X‐ray absorptiometry and independently of bone mineral density.  J Bone Miner Res. 1995;  10 243-249
• 32 Simkin A, Leichter I, Swissa A, Samueloff S. The effect of swimming activity on bone architecture in growing rats.  J Biomech. 1989;  22 845-851
• 33 Slaughter M H, Lohman T G, Boileau B A. Skinfold equations for estimation of body fatness in children and youth.  Hum Biol. 1988;  60 709-723
• 34 Soderman K, Bergstrom E, Lorentzon R, Alfredson H. Bone mass and muscle strength in young female soccer players.  Calcif Tissue Int. 2000;  67 297-303
• 35 Tanner J M. Growth at Adolescence. Oxford; Blackwell Scientific Publications 1962
• 36 Trost S G, Pate R R, Sallis J F, Freedson P S, Taylor W C, Dowda M, Sirard J. Age and gender differences in objectively measured physical activity in youth.  Med Sci Sports Exerc. 2002;  34 350-355
• 37 Vicente-Rodriguez G, Ara I, Perez-Gomez J, Serrano-Sanchez J A, Dorado C, Calbet J A. High femoral bone mineral density accretion in prepubertal soccer players.  Med Sci Sports Exerc. 2004;  36 1789-1795
• 38 Vicente-Rodriguez G, Jimenez-Ramirez J, Ara I, Serrano-Sanchez J A, Dorado C, Calbet J A. Enhanced bone mass and physical fitness in prepubescent footballers.  Bone. 2003;  33 853-859
• 39 Welch J M, Weaver C M, Turner C H. Adaptations to free-fall impact are different in the shafts and bone ends of rat forelimbs.  J Appl Physiol. 2004;  97 1859-1865
• 40 Wittich A, Mautalen C A, Oliveri M B, 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;  63 112-117