There were also training-induced alterations in the serum biomarkers for osteoclast activity. Serum pyridinoline cross-links (PYD) were significantly lower for 2LC, 3LC, and 4LC groups compared with both the 1LC and the Con groups (Table 4). There were no significant differences in serum PYD between 2LC, 3LC, and 4LC groups. Serum OC did not differ between Con 1LC, 2LC, 3LC, or 4LC groups (Table 4).
Training-induced elevations in BMD for the left tibia and left femur were observed for the 2LC, 3LC, and 4LC groups compared with Con. In addition, the 2LC, 3LC, and 4LC groups demonstrated significantly greater bone strength parameters for both the right tibia and right femur compared with Con. Although training-induced alterations were observed for BMD, bone strength, and serum PYD for the 2LC, 3LC, and 4LCgroups compared with Con, there were no significant differences between the 2LC, the 3LC, and the 4LC groups. Taken together, the results support our hypothesis that a low amount of resistance training (i.e., two ladder climbs) was just as effective as greater volumes of resistance exercise for stimulating more BMD and enhanced bone strength during the growth period in rats.
Elevating peak bone mass during the growth period may help to prevent the onset or reduce the severity of osteoporosis (10,30). Although pharmacological treatment strategies are available to help slow or prevent the rate of bone degradation, currently there is no cure for osteoporosis. In the absence of a cure, prevention becomes of utmost importance where high-impact activities (e.g., jumping) or resistance exercise (e.g., strength training) have been advocated as effective activities to use to increase peak bone mass that could assist in reducing the risk of osteoporosis (12,26). Although numerous human studies (1,4,13,15,24,29,30) have supported the effectiveness of high-impact or resistance activities for increasing bone formation, these investigations often use cross-sectional comparisons or prospective research designs where heredity, diet, growth rate, and lean mass (to name a few) could be contributing factors for skeletal differences rather than the exercise intervention. In contrast, the use of an animal model minimizes many of the confounding variables associated with human studies. However, most of the previous animal studies investigated the impact of treadmill running (i.e., weight bearing) on the bone (9,18). The challenge of getting animals to lift a heavy mass has limited a thorough examination of the impact of resistance training on the skeletal system. To mimic resistance training, we used a modified version of a ladder climbing task for rats that was first described by Hornberger and Farrar (8). Our current observations of training-induced elevations in BMD for the tibia and femur, using a strength training model in rats, were consistent with previous animal reports on the effectiveness of incorporating exercise for stimulating bone for mation during the growth period in animals (5,6,11,17–20,23,25,28,31). Nevertheless, although physical activity has consistently been demonstrated to stimulate bone formation, as supported by both human and animal studies, the amount of exercise to maximally elevate peak bone mass during the growth period has been unresolved.
Using adult anesthetized animals and a bone loading protocol, Turner and Robling (27) hypothesized that mechanosensors within the bone can reset after a bout of exercise. As such, partitioning the exercise into multiple bouts throughout a training day would provide more stimulation for bone formation, yielding greater elevations in peak bone mass (21,27). Thus, this interrupted exercise strategy could potentially maximize BMD during the growth period. Using this premise, we made several attempts to support the enhanced effectiveness of interrupted exercise whereby bone formation could be maximally augmented. However, we observed equivalent training-induced elevations in BMD whether the resistance exercise was interrupted using various recovery times or the resistance exercise was continuous within a training day in young, growing male rats (5,6,11). Similarly, Umemura et al. (28) demonstrated equivalent osteogenic responses between an interrupted jumping protocol (2 × 10 jumps) compared with a continuous jumping protocol (1 × 20 jumps) in young female rats. Potential factors for the discrepancy between the results of Turner and Robling (27) compared with the results of Umemura et al. (28) and our findings (5,6,11) include the following: the age of the animal (i.e., adult vs young), the osteogenic stimulus (i.e., bone loading vs exercise), and the experimental protocol (i.e., anesthetized vs conscious animals). Alternatively, the inability to support the hypothesis submitted by Turner and Robling (27) led us to speculate that during the growth period there may be a threshold for bone formation.
The loading studies of Rubin and Lanyon (22,23) were among the first to demonstrate the existence of an exercise threshold whereby any additional increases in the number of load cycles failed to result in further changes in avian bone mineral content. These initial studies were performed on anesthetized animals where the advantage of using a bone loading protocol includes a quantification of load, cycles, and compressive strains. However, caution should be used in the interpretation when applied to dynamic exercise that can create unique load and strain distribution patterns. Alternatively, the use of conscious animals engaged in exercise allows for the full impact of load and compressive strains but does not allow for a quantification of the load and compressive strains imposed on the bone. Despite the limitations with use of conscious animals, our previous work and current results support the contention of an exercise threshold as originally proposed by Rubin and Lanyon (23). First, we recently reported equivalent training-induced elevations in BMD in two groups of resistance-exercised animals despite significant differences in the volume of work performed each training day between groups (20). By using the identical training protocol as described in the current investigation, we reported that young animals climbing the ladder three times per training session (with weights appended to the tail) demonstrated the same elevation in BMD as growing animals climbing the ladder six times per exercise session (with weights appended to the tail) (20). Further, we note that in all our previous studies (5,6,11,25), the average training-induced augmentation in tibia BMD from animals climbing the ladder six times per training session was approximately 9% greater than corresponding controls, similar to the elevation in the current investigation although the animals performed approximately 33%–66% less work per training bout. Next, in a previous study, we demonstrated equivalent elevations in tibia BMD with three interrupted exercise bouts (separated by 3–4 h) where growing animals engaged in two ladder climbs per session compared with six continuous ladder climbs on a given training day (6). As such, our previous study (6) lends support to our current contention regarding the effectiveness of two ladder climbs as a volume of work (using this training regimen) sufficient for maximal bone modeling during the growth period. Collectively, our current findings and previous reports (5,6,11,25) support the contention of the existence of an exercise threshold for stimulating bone formation as initially proposed by Rubin and Lanyon (22,23) who used a bone loading protocol in anesthetized animals. We now extend this presumption to conscious animals engaged in resistance training during the growth period.
Although training-induced elevations in BMD are important, the salient feature in the prevention of fractures is bone strength. The opportunity to measure bone strength with use of an animal model is a significant advantage over human studies. However, factors that can contribute to differences in bone strength between animal studies include specimen storage, bone hydration, the temperature at which the bones are broken, the site at which the bones are broken, the direction of the applied force, and so on. Thus, we recognize that interpretations of bone strength data represent relative changes compared with a corresponding Con rather than absolute changes. In the current report, when compared with control animals, we observed a training-induced average augmentation of 27%, 32%, and 28% in Fmax, EF, and bone stiffness, respectively, for the tibia. We also observed an exercise-induced average elevation of 41%, 40%, and 50% (compared with Con) in Fmax, EF, and bone stiffness, respectively, for the femur. The absence of any significant difference between 2LC, 3LC, and 4LC groups suggests equivalent training-induced elevations in bone strength. In addition, our results were consistent with previous animal reports (5,6,11,20,27,28), demonstrating that the concomitant elevations in bone strength after training are much greater than the elevations in BMD.
In the present investigation, we note that the training-induced elevations in BMD and bone strength were greater for the femur compared with the tibia. We have no objective measurements to explain the apparent bone-specific (i.e., femur vs tibia) response to our ladder climbing exercise. On the basis of subjective interpretations, we offer the following explanations. First, the vertical ladder climbs might place more mechanical stress on the femur compared with the tibia that would account for the greater BMD. Next, we determined the BMD of the entire femur and tibia without regard to geometric changes at specific bone sites. Thus, the mechanical stress of the ladder climbs might stimulate bone formation at specific skeletal sites that are distinct for the femur compared with the tibia that contribute to differences in bone strength. Irrespective of the mechanism for the apparent difference in bone-specific response, the ladder climbing training program appears to be an effective stimulus for bone adaptation where more exercise does not result in greater bone mass.
Contributing factors for an elevation in BMD would be the relative rate of bone deposition compared with bone degradation. Ostensibly, net bone formation can be attributable to an elevation in osteoblast activity, a decline in osteoclast activity, or a combination of both. Although most studies suggest that the training-induced elevation in BMD can be attributable to an increase in osteoblast activity (3,4,5,11,16,20,25,31), only a few reports, including our current results, have demonstrated a decline in osteoclast activity (6,32). We have no explanation for the apparent discrepancy, but we note that blood withdrawn during animal sacrifice only represents a snapshot at a single time point and not the sustained activity of osteoblasts and/or osteoclasts throughout the training period. In support, several studies have demonstrated training-induced elevations in BMD in the absence of any alterations in serum biomarkers (7,19). Therefore, we recognize the significant limitation of extrapolating on bone cell activity from a single serum sample taken at one time point. Despite the drawbacks and inconsistent results from previous studies (including our own), we note that the decline in osteoclast activity (as measured by serum PYD) still provides suggestive evidence of net bone formation and corroborates the training-induced elevation in BMD and bone strength.
Finally, we acknowledge several limitations in the current study. First, the epiphyseal plates in rats do not close. This would favor a bone formation response and limit an extrapolation of the results to adult humans. As in our previous reports (5,6,11,20,25), we chose to examine the growth period in rats where the findings using this animal model might be more comparable with growing humans. Next, we recognize the limitations in the use of the DXA for the assessment of BMD where the units are expressed as mass per area rather than mass per volume. Further, a DXA is unable to discriminate between cortical and trabecular bone. In addition, differences in bone size can also lead to misinterpretations with the use of the DXA (2). Nevertheless, the DXA was used to measure BMD from all animals of equivalent body weight, minimizing the potential for confounding factors related to bone size providing relative comparisons between groups. In addition, the training-induced augmentations in BMD were supported by corresponding increases in bone strength. Despite all of these limitations, to the extent that our findings in rats can be applied to humans, our results would suggest that in children, incorporating a low amount of resistance exercise would be just as effective as higher volumes of resistance training for maximal bone formation.
In summary, our results suggest that a low volume of resistance training was just as effective as higher amounts of resistance training for maximal stimulation of bone formation during the growth period. This was supported by the equivalent elevations in BMD for the 2LC, 3LC, and 4LC groups compared with Con, despite the significant difference in work performed by each resistance-trained group. Compared with the Con group, there were also training-induced alterations in bone mechanical properties and serum PYD for the 2LC, 3LC, and 4LC groups. There were no significant differences between the 2LC, the 3LC, or the 4LC groups for BMD, bone strength, or serum PYD. Therefore, our results support the contention of an exercise threshold whereby increases in work per exercise session did not yield further elevations in bone modeling.
This study was supported by a Chapman University Faculty Research Grant.
The authors do not have any conflicts of interest or professional relationships with companies or manufacturers who would benefit from the results of this study.
The results of this study do not constitute endorsement by the American College of Sports Medicine.
1. Bradney M, Pearce G, Naughton G, et al.. 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: 1814–21.
2. Carter DR, Bouxsein ML, Marcus R. New approaches for interpreting projected bone densitometry data. J Bone Miner Res
. 1992; 7 (2): 137–45.
3. Danz AM, Zittermann A, Schiedermaier U, Klein K, Hotzel D, Schonau E. The effect of a specific strength-development exercise on bone mineral density in perimenopausal and postmenopausal women. J Women’s Health
. 1998; 7: 701–9.
4. Fujimura R, Ashizawa N, Watanabe M, et al.. Effect of resistance exercise training on bone formation and resorption in young male subjects assessed by biomarkers of bone metabolism. J Bone Miner Res
. 1997; 12: 656–62.
5. Godfrey JK, Kayser BD, Gomez GV, Bennett J, Jaque SV, Sumida KD. Interrupted resistance training & BMD in growing rats. Int J Sports Med
. 2009; 30: 579–84.
6. Goettsch BM, Smith MZ, O’Brien JA, Gomez GV, Jaque SV, Sumida KD. Interrupted vs. uninterrupted training on BMD during growth. Int J Sports Med
. 2008; 29: 980–6.
7. Holy X, Zerath E. Bone mass increases in less than 4 wk of voluntary exercising in growing rats. Med Sci Sports Exerc
. 2000; 32 (9): 1562–9.
8. Hornberger TA, Farrar RP. Physiological hypertrophy of the FHL muscle following 8 weeks progressive resistance exercise in the rat. Can J Appl Physiol
. 2004; 29: 16–31.
9. Iwamoto J, Yeh JK, Aloia JF. Effect of deconditioning on cortical and cancellous bone growth in the exercised trained young rats. J Bone Miner Res
. 2000; 15 (9): 1842–9.
10. Johnston CC, Hui SL, Wiske P, Norton JA, Epstein S. Bone mass at maturity and subsequent rates of loss as determinants of osteoporosis. In: DeLuca HF, editor. Osteoporosis: Recent Advances in Pathogenesis and Treatment
. Baltimore, MD: University Park Press; 1981. p. 285–91
11. Kayser BD, Godfrey JK, Cunningham R, Piercer RA, Jaque SV, Sumida KD. Equal BMD after daily or triweekly exercise in growing rats. Int J Sports Med
. 2010; 31: 44–50.
12. Layne JE, Nelson ME. The effects of progressive resistance training on bone density: a review. Med Sci Sports Exerc
. 1999; 31 (1): 25–30.
13. Lehtonen-Veromaa M, Mottonen T, Nuotio I, Heinonen OJ, Viikari J. Influence of physical activity on ultrasound and dual-energy x-ray absorptiometry bone measurements in peripubertal girls: a cross-sectional study. Calcif Tissue Int
. 2000; 66: 248–54.
14. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem
. 1951; 193: 265–75.
15. MacKelvie KJ, Petit MA, Khan KM, Beck TJ, McKay HA. Bone mass and structure are enhanced following a 2-year randomized controlled trial of exercise in prepubertal boys. Bone
. 2004; 34: 755–64.
16. Menkes A, Mazel S, Redmond RA, 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.
17. Notomi T, Lee SJ, Okimoto N, et al.. Effects of resistance exercise training on mass, strength, and turnover of bone in growing rats. Eur J Appl Physiol
. 2000; 82: 268–74.
18. Notomi T, Okazaki Y, Okimoto N, Saitoh S, Nakamura T, Suzuki M. A comparison of resistance and aerobic training for mass, strength, and turnover of bone in growing rats. Eur J Appl Physiol
. 2000; 83 (6): 469–74.
19. Notomi T, Okimoto N, Okazaki Y, Tanaka Y, Nakamura T, Suzuki M. Effects of tower climbing exercise on bone mass, strength, and turnover in growing rats. J Bone Miner Res
. 2001; 16: 166–74.
20. Pierce RA, Cunningham RM, Shdo SM, et al.. Different training volumes yield equivalent increases in BMD. Int J Sports Med
. 2010; 31: 803–9.
21. Robling AG, Burr DB, Turner CH. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol
. 2001; 204: 3389–99.
22. Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int
. 1985; 37: 411–7.
23. Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am
. 1984; 66(3): 397–402.
24. Scerpella TA, Davenport M, Morganti CM, Kanaley JA, Johnson LM. Dose related association of impact activity and bone mineral density in pre-pubertal girls. Calcif Tissue Int
. 2003; 72: 24–31.
25. Smith MZ, Goettsch BM, O’Brien JA, Van Ramshorst RD, Jaque SV, Sumida KD. Resistance training & bone mineral density during growth. Int J Sports Med
. 2008; 29: 316–21.
26. Suominen H. Muscle training for bone strength. Aging Clin Exp Res
. 2006; 18 (2): 85–93.
27. Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sports Sci Rev
. 2003; 31 (1): 45–50.
28. Umemura Y, Sogo N, Honda A. Effects of intervals between jumps or bouts on osteogenic response to loading. J Appl Physiol
. 2002; 93: 1345–8.
29. Van Lagendonck L, Claessens AL, Vlietinck R, Derom C, Beunen G. Influence of weight-bearing exercises on bone acquisition in prepubertal monozygotic female twins: a randomized controlled prospective study. Calcif Tissue Int
. 2003; 72: 666–74.
30. Welten DC, Kemper HCG, Post BG, et al.. Weight-bearing activity during youth is a more important factor for peak bone mass than calcium intake. J Bone Miner Res
. 1994; 9: 1089–96.
31. Westerlind KC, Fluckey JD, Gordon SE, Kraemer WM, Farrell PA, Turner RT. Effect of resistance exercise training on cortical and cancellous bone in mature male rats. J Appl Physiol
. 1998; 84 (2): 459–64.
32. Yeh JK, Lui CC, Aloia JF. Effects of exercise and immobilization on bone formation and resorption in young rats. Am J Physiol
. 1993; 264: E182–9.
Keywords:©2013The American College of Sports Medicine
TIBIA; FEMUR; DXA; THREE-POINT BENDING TEST