Abstract
This study investigated the effects of endurance running training on the bones of growing rats. Thirty-two male Wistar rats (7 weeks old) were assigned to a sedentary control group (CON, n = 10), a continuous endurance running group (CEN, n = 10), or an intermittent endurance running group (IEN, n = 12). After an 8-week training period, both exercise groups had significantly less body weight (BW) gain but higher aerobic capacity, shown by increased muscle citrate synthase (CS) activity. Bone area (BA), areal bone mineral density (aBMD), and bone mineral content (BMC) were measured by dual-energy Xray absorptiometry (DXA) in the total femur and sections of femora. Except for showing a significantly higher aBMD in total femora, the CON group was only slightly and nonsignificantly higher in other DXA measurements. In tissue weight measurements, the CON group showed a nonsignificantly higher tissue dry weight (P = 0.146), but a significantly lower tissue water content ratio (WCR, %) as compared to the exercise group. Despite having nonsignificantly lower long bone cross-sectional parameters, both exercise groups showed significantly better biomaterial properties, as measured by a three-point bending test. In extrinsic analysis, femora of the two exercise groups showed no difference in bending load and stiffness, but were significantly higher in post-yield bending energy and total ultimate bending energy (P < 0.05). Similar phenomena were revealed in tissue-level measurements; the CEN and IEN groups were significantly higher in ultimate toughness and post-yield toughness (P < 0.05). Higher post-yield energy shown by two exercise groups implied a change in bone matrix organization. In conclusion, this study demonstrated that two endurance treadmill training modes benefit bone, with subjects showing better tissue biomaterial properties without significantly increasing aBMD, BMC, or bone dimension. Further study would be valuable to investigate the effects of endurance running on other components of bone, such as organization of bone matrix and its relationship with bone biomaterial properties.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Iwamoto J, Takeda T, Sato Y (2005) Effect of treadmill exercise on bone mass in female rats. Exp Anim 54:1–6
Notomi T, Okazaki Y, Okimoto N, Saitoh S, Nakamura T, Suzuki M (2000) A comparison of resistance and aerobic training for mass, strength and turnover of bone in growing rats. Eur J Appl Physiol 83:469–474
Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S (1997) Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res 12:1480–1485
Welch JM, Weaver CM, Turner CH (2004) Adaptations to free-fall impact are different in the shafts and bone ends of rat forelimbs. J Appl Physiol 97:1859–1865
Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS (2003) Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol 95:300–307
Huang TH, Yang RS, Hsieh SS, Liu SH (2002) Effects of caffeine and exercise on the development of bone: a densitometric and histomorphometric study in young Wistar rats. Bone (NY) 30: 293–299
Jurimae T, Soot T, Jurimae J (2005) Relationships of anthropometrical parameters and body composition with bone mineral content or density in young women with different levels of physical activity. J Physiol Anthropol Appl Hum Sci 24:579–587
Soot T, Jurimae T, Jurimae J, Gapeyeva H, Paasuke M (2005) Relationship between leg bone mineral values and muscle strength in women with different physical activity. J Bone Miner Metab 23: 401–406
Frost HM (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9
Webb AA, Gowribai K, Muir GD (2003) Fischer (F-344) rats have different morphology, sensorimotor and locomotor abilities compared to Lewis, Long-Evans, Sprague-Dawley and Wistar rats. Behav Brain Res 144:143–156
Puustjarvi K, Nieminen J, Rasanen T, Hyttinen M, Helminen HJ, Kroger H, Huuskonen J, Alhava E, Kovanen V (1999) Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 14:321–329
Skedros JG, Dayton MR, Sybrowsky CL, Bloebaum RD, Bachus KN (2006) The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone. J Exp Biol 209:3025–3042
Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319–336
Wang X, Bank RA, TeKoppele JM, Agrawal CM (2001) The role of collagen in determining bone mechanical properties. J Orthop Res 19:1021–1026
Lin YS, Jan MS, Tsai TJ, Chen HI (1995) Immunomodulatory effects of acute exercise bout in sedentary and trained rats. Med Sci Sports Exerc 27:73–78
Zonderland ML, Bar PR, Reijneveld JC, Spruijt BM, Keizer HA, Glatz JFC (1999) Different metabolic adaptation of heart and skeletal muscles to moderate-intensity treadmill training in the rat. Eur J Appl Physiol Occup Physiol 79:391–396
Shepherd D, Garland PB (1969) Citrate synthase from rat liver. Methods Enzymol 13:11–16
Honda A, Umemura Y, Nagasawa S (2001) Effect of high-impact and low-repetition training on bones in ovariectomized rats. J Bone Miner Res 16:1688–1693
Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone (NY) 14:595–608
Sakamoto K, Grunewald KK (1987) Beneficial effects of exercise on growth of rats during intermittent fasting. J Nutr 117:390–395
Nordsletten L, Kaastad TS, Skjeldal S, Kirkeby OJ, Reikeras O, Ekeland A (1993) Training increases the in vivo strength of the lower leg: an experimental study in the rat. J Bone Miner Res 8:1089–1095
Bourrin S, Palle S, Pupier R, Vico L, Alexandre C (1995) Effect of physical training on bone adaptation in three zones of the rat tibia. J Bone Miner Res 10:1745–1752
Hagihara Y, Fukuda S, Goto S, Iida H, Yamazaki M, Moriya H (2005) How many days per week should rats undergo running exercise to increase BMD? J Bone Miner Metab 23:289–294
Iwamoto J, Shimamura C, Takeda T, Abe H, Ichimura S, Sato Y, Toyama Y (2004) Effects of treadmill exercise on bone mass, bone metabolism, and calciotropic hormones in young growing rats. J Bone Miner Metab 22:26–31
Wheeler DL, Graves JE, Miller GJ, Vander Griend RE, Wronski TJ, Powers SK, Park HM (1995) Effects of running on the torsional strength, morphometry, and bone mass of the rat skeleton. Med Sci Sports Exerc 27:520–529
Yeh JK, Liu CC, Aloia JF (1993) Effects of exercise and immobilization on bone formation and resorption in young rats. Am J Physiol 264:E182–E189
Davicco MJ, Horcajada-Molteni MN, Gaumet-Meunier N, Lebecque P, Coxam V, Barlet JP (1999) Endurance training and bone metabolism in middle-aged rats. Mech Ageing Dev 109: 83–96
Joo YI, Sone T, Fukunaga M, Lim SG, Onodera S (2003) Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone (NY) 33:485–493
Kiuchi A, Arai Y, Katsuta S (1998) Detraining effects on bone mass in young male rats. Int J Sports Med 19:245–249
Banu MJ, Orhii PB, Mejia W, McCarter RJ, Mosekilde L, Thomsen JS, Kalu DN (1999) Analysis of the effects of growth hormone, voluntary exercise, and food restriction on diaphyseal bone in female F344 rats. Bone (NY) 25:469–480
Mosekilde L, Thomsen JS, Orhii PB, McCarter RJ, Mejia W, Kalu DN (1999) Additive effect of voluntary exercise and growth hormone treatment on bone strength assessed at four different skeletal sites in an aged rat model. Bone (NY) 24:71–80
Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. Br Med J 312:1254–1259
Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA 288:1889–1897
Felson DT, Zhang YQ, Hannan MT, Anderson JJ (1993) Effects of weight and body-mass index on bone-mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573
Mazess RB (1998) Body weight predicts bone density better than resorption markers. Arch Intern Med 158:298, 300
Rico H, Revilla M, Hernandez ER, Villa LF, Alvarez del Buergo M, Lopez Alonso A (1991) Age-and weight-related changes in total body bone mineral in men. Miner Electrolyte Metab 17: 321–323
Siemon NJ, Moodie EW (1973) Body weight as a criterion in judging bone mineral adequacy. Nature (Lond) 243:541–543
Marotti G, Muglia MA, Palumbo C (1994) Structure and function of lamellar bone. Clin Rheumatol 13(suppl 1):63–68
Currey JD (1979) Changes in the impact energy absorption of bone with age. J Biomech 12:459–469
Currey JD (1988) The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biomech 21:131–139
Boskey AL, Wright TM, Blank RD (1999) Collagen and bone strength. J Bone Miner Res 14:330–335
Burr DB (2002) The contribution of the organic matrix to bone’s material properties. Bone (NY) 31:8–11
Nyman JS, Roy A, Shen X, Acuna RL, Tyler JH, Wang X (2006) The influence of water removal on the strength and toughness of cortical bone. J Biomech 39:931–938
Wang X, Shen X, Li X, Agrawal CM (2002) Age-related changes in the collagen network and toughness of bone. Bone (NY) 31: 1–7
Kopp J, Bonnet M, Renou JP (1989) Effect of collagen crosslinking on collagen-water interactions (a DSC investigation). Matrix 9:443–450
Wallace JD, Cuneo RC, Lundberg PA, Rosen T, Jorgensen JO, Longobardi S, Keay N, Sacca L, Christiansen JS, Bengtsson BA, Sonksen PH (2000) Responses of markers of bone and collagen turnover to exercise, growth hormone (GH) administration, and GH withdrawal in trained adult males. J Clin Endocrinol Metab 85:124–133
Welsh L, Rutherford OM, James I, Crowley C, Comer M, Wolman R (1997) The acute effects of exercise on bone turnover. Int J Sports Med 18:247–251
Zittermann A, Sabatschus O, Jantzen S, Platen P, Danz A, Stehle P (2002) Evidence for an acute rise of intestinal calcium absorption in response to aerobic exercise. Eur J Nutr 41:189–196
Fahey TD, Baldwin KM, Brooks GA (2005) Exercise Physiology: Human Bioenergetics and Its Applications. McGraw-Hill, New York
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Huang, TH., Chang, FL., Lin, SC. et al. Endurance treadmill running training benefits the biomaterial quality of bone in growing male Wistar rats. J Bone Miner Metab 26, 350–357 (2008). https://doi.org/10.1007/s00774-007-0831-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00774-007-0831-3