Effects of Hypertrophy Exercise in Bone Turnover Markers and Structure in Growing Male Rats

Abstract

The benefits of exercise on bone density, structure and turnover markers are rather controversial. The present study aimed to examine the effects of hypertrophy exercise (HE) on bone. 20 male Wistar rats were randomly distributed in 2 experimental groups, one performing HE and the other untrained over 12 weeks. Plasma parameters, bone mineral content, bone mineral density (BMD), structure, and trabecular and cortical microarchitecture were measured. Femur Mg content was 12% higher (p<0.001), whereas femur length, dry weight, P content, and aminoterminal propeptides of type I procollagen were lower in the HE group (all, p<0.05). Total BMD and cortical/subcortical BMD were higher (both, p<0.01), whereas total cross-sectional and trabecular areas were lower (both, p<0.001), and cortical area and thickness were lower in the HE (both, p<0.05). Trabecular connectivity density, number, mean density of total and bone volume were higher in the HE (all, p<0.05). Cortical volume fraction and the mean density of total volume of the diaphysis were lower, whereas the cortical volume density was higher in the HE (all, p<0.05). This HE protocol may have beneficial effect on cancellous bone microarchitecture, but it induces low bone formation and is associated with hypogonadism in growing male rats. However, this type of training might be inefficient to maintain appropriate cortical thickness.

Key words

bone metabolism - bone mineral density (BMD) - training - micro-CT - pQCT

• References

• 1 Amanzadeh J, Gitomer WL, Zerwekh JE, Preisig PA, Moe OW, Pak CYC, Levi M. Effect of high protein diet on stone-forming propensity and bone loss in rats. Kidney Int 2003; 64: 2142-2149
• 2 Aparicio VA, Nebot E, Kapravelou G, Sanchez C, Porres JM, Lopez Jurado M, Aranda P. Resistance training reduces the metabolic acidosis and hepatic and renal hypertrophy caused by the consumption of a high protein diet in rats. Nutr Hosp 2011; 26: 1478-1486
• 3 Aparicio VA, Nebot E, Porres JM, Ortega FB, Heredia JM, Lopez-Jurado M, Ramirez PA. Effects of high-whey-protein intake and resistance training on renal, bone and metabolic parameters in rats. Br J Nutr 2011; 105: 836-845
• 4 Bagi CM, Berryman E, Moalli MR. Comparative bone anatomy of commonly used laboratory animals: implications for drug discovery. Comp Med 2011; 61: 76-85
• 5 Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res 1998; 13: 500-507
• 6 Bennell K, Page C, Khan K, Warmington S, Plant D, Thomas D, Palamara J, Williams D, Wark JD. Effects of resistance training on bone parameters in young and mature rats. Clin Exp Pharmacol Physiol 2000; 27: 88-94
• 7 Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 2005; 35: 779-830
• 8 Borer KT, Kelch RP. Increased serum growth hormone and somatic growth in exercising adult hamsters. Am J Physiol 1978; 234: E611-E616
• 9 Bradney M, Pearce G, Naughton G, Sullivan C, Bass S, Beck T, Carlson J, Seeman E. Moderate exercise during growth in prepubertal boys: changes in bone mass, size, volumetric density, and bone strength: a controlled prospective study. J Bone Miner Res 1998; 13: 1814-1821
• 10 Chen PS, Toribara TY, Warner H. Microdetermination of Phosphorus. Anal Chem 1956; 28: 1756-1758
• 11 Cossio-Bolanos M, Gómez-Campos R, Pilco-Quesada S, Lancho-Alonso JL, de Arruda M. Propuesta de una ecuación lineal para valorar la velocidad de crecimiento somático a partir de la masa corporal de ratas machos Wistar. Anales de la Facultad de Medicina 2012; 73: 93-100
• 12 de Salles BF, Simao R, Miranda F, Novaes Jda S, Lemos A, Willardson JM. Rest interval between sets in strength training. Sports Med 2009; 39: 765-777
• 13 European Union C. Directive on the Protection of Animals used for Scientific Purposes. In Official Journal of the European Union 2010; 33-79 L 276
• 14 Falk B, Galili Y, Zigel L, Constantini N, Eliakim A. A cumulative effect of physical training on bone strength in males. Int J Sports Med 2007; 28: 449-455
• 15 Fonseca H, Moreira-Goncalves D, Coriolano H-JA, Duarte JA. Bone quality: the determinants of bone strength and fragility. Sports Med 2014; 44: 37-53
• 16 Gönul B, Baltaci G, Koz M. Effects of run training on bone development and bone mineralization in growing mice. Biol Sport 2011; 28: 129-132
• 17 Gustavsson A, Thorsen K, Nordstrom P. A 3-year longitudinal study of the effect of physical activity on the accrual of bone mineral density in healthy adolescent males. Calcif Tissue Int 2003; 73: 108-114
• 18 Gutierrez A. Modificaciones fisiológicas inducidas por el ejercicio en adolescentes y su repercusión sobre la talla definitiva. In, Archivos de Medicina del Deporte 1989; 265-268
• 19 Hamrick MW, Skedros JG, Pennington C, McNeil PL. Increased osteogenic response to exercise in metaphyseal versus diaphyseal cortical bone. J Musculoskelet Neuronal Interact 2006; 6: 258-263
• 20 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2016 update. Int J Sports Med 2015; 36: 1121-1124
• 21 Hart KJ, Shaw JM, Vajda E, Hegsted M, Miller SC. Swim-trained rats have greater bone mass, density, strength, and dynamics. J Appl Physiol 2001; 91: 1663-1668
• 22 Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone 2006; 39: 880-885
• 23 Houston MC, Fazio S, Chilton FH, Wise DE, Jones KB, Barringer TA, Bramlet DA. Nonpharmacologic treatment of dyslipidemia. Prog Cardiovasc Dis 2009; 52: 61-94
• 24 Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS. Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol 2003; 95: 300-307
• 25 Janz KF, Gilmore JM, Levy SM, Letuchy EM, Burns TL, Beck TJ. Physical activity and femoral neck bone strength during childhood: the Iowa Bone Development Study. Bone 2007; 41: 216-222
• 26 Karcioglu ZA, Sarper RM. eds. Zinc and Copper in Medicine. Springfield: Charles C. Thomas; 1980
• 27 Karlsson MK, Magnusson H, Karlsson C, Seeman E. The duration of exercise as a regulator of bone mass. Bone 2001; 28: 128-132
• 28 Kelly DM, Jones TH. Testosterone: a metabolic hormone in health and disease. J Endocrinol 2013; 217: R25-R45
• 29 Kiiskinen A. Physical training and connective tissues in young mice – physical properties of Achilles tendons and long bones. Growth 1977; 41: 123-137
• 30 Lorentzon M, Swanson C, Andersson N, Mellstrom D, Ohlsson C. Free testosterone is a positive, whereas free estradiol is a negative, predictor of cortical bone size in young Swedish men: the GOOD study. J Bone Miner Res 2005; 20: 1334-1341
• 31 Ma H, Torvinen S, Silvennoinen M, Rinnankoski-Tuikka R, Kainulainen H, Morko J, Peng Z, Kujala UM, Rahkila P, Suominen H. Effects of diet-induced obesity and voluntary wheel running on bone properties in young male C57BL/6J mice. Calcif Tissue Int 2010; 86: 411-419
• 32 Ma H, Turpeinen T, Silvennoinen M, Torvinen S, Rinnankoski-Tuikka R, Kainulainen H, Timonen J, Kujala UM, Rahkila P, Suominen H. Effects of diet-induced obesity and voluntary wheel running on the microstructure of the murine distal femur. Nutr Metab (Lond) 2011; 8: 1
• 33 McDonald R, Hegenauer J, Saltman P. Age-related differences in the bone mineralization pattern of rats following exercise. J Gerontol 1986; 41: 445-452
• 34 Morimoto Y, Arisue K, Yamamura Y. Relationship between circadian rhythm of food intake and that of plasma corticosterone and effect of food restriction on circadian adrenocortical rhythm in the rat. Neuroendocrinology 1977; 23: 212-222
• 35 Navas FJ, Martin JF, Cordova A. Compartmental shifts of calcium and magnesium as a result of swimming and swimming training in rats. Med Sci Sports Exerc 1997; 29: 882-891
• 36 Nurzenski MK, Briffa NK, Price RI, Khoo BC, Devine A, Beck TJ, Prince RL. Geometric indices of bone strength are associated with physical activity and dietary calcium intake in healthy older women. J Bone Miner Res 2007; 22: 416-424
• 37 Pietschmann P, Skalicky M, Kneissel M, Rauner M, Hofbauer G, Stupphann D, Viidik A. Bone structure and metabolism in a rodent model of male senile osteoporosis. Exp Gerontol 2007; 42: 1099-1108
• 38 Reeves PG, Nielsen FH, Fahey Jr GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993; 123: 1939-1951
• 39 Sipos W, Rauner M, Skalicky M, Viidik A, Hofbauer G, Schett G, Redlich K, Lang S, Pietschmann P. Running has a negative effect on bone metabolism and proinflammatory status in male aged rats. Exp Gerontol 2008; 43: 578-583
• 40 Smith SM, Heer MA, Shackelford LC, Sibonga JD, Ploutz-Snyder L, Zwart SR. Benefits for bone from resistance exercise and nutrition in long-duration spaceflight: evidence from biochemistry and densitometry. J Bone Miner Res 2012; 27: 1896-1906
• 41 Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sports Medicine 2016; 46: 171-182
• 42 Vicente-Rodriguez G, Ezquerra J, Mesana MI, Fernandez-Alvira JM, Rey-Lopez JP, Casajus JA, Moreno LA. Independent and combined effect of nutrition and exercise on bone mass development. J Bone Miner Metab 2008; 26: 416-424
• 43 Williams MA, Haskell WL, Ades PA, Amsterdam EA, Bittner V, Franklin BA, Gulanick M, Laing ST, Stewart KJ. Resistance exercise in individuals with and without cardiovascular disease: 2007 update: a scientific statement from the American Heart Association Council on Clinical Cardiology and Council on Nutrition, Physical Activity, and Metabolism. Circulation 2007; 116: 572–584