Strategies for preventing osteoporosis include maximizing peak bone mass early in life and slowing the rate of age-related bone loss (18). Peak bone mass is reached within the third decade of age and then starts to decline (6). Exercise is advocated as an essential strategy for obtaining an optimal peak bone mass, and the years before the age of 30 is regarded as the final opportunity for this (18). However, it is still unclear which training mode is most effective for increasing bone mass in young adult individuals (9,14,24).
Both plyometric high-impact exercises and traditional strength training promote beneficial effects on bone mass (17). In young adults, both training modes have been reported to increase bone mineral density (BMD) at the hip and lumbar spine (17,23,24), which are sites prone to osteoporotic fractures. Beneficial changes in circulating levels of bone formation markers (e.g., type 1 collagen amino-terminal propeptide [P1NP]) and bone resorption markers (e.g., type 1 collagen C breakdown products [CTX]) have also been reported (22,36). However, the training programs that appear to be most effective include a relatively high volume of training, using a combination of strength training and high-impact exercises (24,37,38). A meta-analysis concluded that training protocols combining high-impact and high-intensity strength training were most effective for regional BMD improvements at both hip and lumbar spine in young women (24). Based on the results from meta-analyses and reviews, high-impact exercises seem to be superior to strength training for increasing bone mass, although high-impact exercises alone seem to mainly induce BMD improvements at the femoral neck (9,24). Strength training, however, has the advantage over high-impact training that targeted loading at both hip and spine is easier to accomplish.
It has been suggested that high acceleration during muscle contractions is important to provide mechanical forces that are strong enough to stimulate osteogenesis (33). Maximal strength training (MST) is a training mode characterized by maximal acceleration during muscle contractions, applying high loads and few repetitions, with priority on progressive loading. Maximal strength training has been reported to effectively improve rate of force development (RFD) and maximal muscle strength, measured as 1 repetition maximum (1RM), in both healthy and diseased individuals (12,13). Improvements in 1RM have been shown to correlate with BMD attainments in postmenopausal women (8,16), whereas neuromuscular performance has been reported to robustly predict bone strength in both premenopausal and postmenopausal women (30). Rate of force development is a measure of neuromuscular performance, and RFD improvement may be advantageous for bone because it reflects the muscles' ability to generate high accelerations (1). Because of the special emphasis placed on progressive loading and rapid execution of muscle contraction, MST is likely to promote higher strain rates in bone than conventional strength training, thus potentially exerting beneficial skeletal effects.
A reduction in the level of the signaling molecule sclerostin, which is an osteocyte-specific inhibitor of osteogenesis, is one possible mechanism by which bone adapts to mechanical loading (28), as attenuated sclerostin signaling may promote bone growth (19). An inverse relationship between circulating sclerostin and physical activity levels has been demonstrated in premenopausal women (2). Whether strength training can reduce the level of circulating sclerostin in humans remains unclear.
Strength training for skeletal adaptations can be designed more simplistic than what has been previously reported (9,18,24), ideally consisting of 1 exercise only, targeting sites most susceptible to osteoporotic fractures. Hack squat exercise, with loads resting on the shoulders, will provide compressive loading through the spine and the hip, both being sites that are particularly subjected to osteoporotic fractures. Thus, the hack squat exercise may be sufficient to induce beneficial effects at relevant skeletal sites. Based on this rationale, performing MST in a hack squat exercise may be an effective intervention for improving skeletal health. Hack squat MST may therefore provide a simple, low-volume training method to increase bone mass in young adults. In the present study, we aimed to investigate the skeletal effects of a hack squat MST intervention in young adult women. We hypothesized that 12 weeks of hack squat MST in young adult women would promote increased BMD at the spine and hip, elevated serum levels of P1NP, and reduced serum levels of CTX and sclerostin. It was also hypothesized that these improvements would coincide with enhanced RFD and 1RM.
Experimental Approach to the Problem
This study was designed to investigate the effects of high-acceleration MST on bone-related parameters, along with RFD and 1RM in young adult women. Maximal oxygen consumption (V[Combining Dot Above]O2max) was measured to control for possible alterations in aerobic fitness. Participants were stratified by age and randomly allocated to a training group (TG, n = 15) and a control group (CG, n = 15) by a locally developed computer software (Unit for Applied Clinical Research, Norwegian University of Science and Technology, Trondheim, Norway). Pretesting occurred 2 weeks before the training period started. Posttesting of the TG was generally completed within 4 days after the last training session, whereas blood samples were collected approximately 48 hours after the last training session for each participant. The CG was posttested 12 weeks after pretesting.
The MST training procedure has been described previously (26). The TG underwent a 12-week MST intervention, 3 sessions per week for a total of 36 training sessions. The training was performed in a laboratory setting and supervised by an instructor at all sessions. In contrast to conventional strength training, MST focuses on high acceleration during the concentric phase, resulting in a high RFD during muscle contractions. The force/time profile of MST has been described previously (13). The training sessions consisted of 1 exercise, using the lower extremities in a squat exercise machine (IT 7006; Impulse Fitness, Shandong, China). The training session started with a warm-up including 2 sets of 8–12 repetitions at approximately 50% of the participant's training load, followed by 4 sets of 3–5 repetitions at 85–90% of 1RM, with special emphasis on maximal mobilization of force during the concentric phase of movement. The participants were encouraged to perpetuate until fatigue. To assure sufficient progression of intensity, the participants' training loads were evaluated during each training session. If they could perform more than 5 repetitions, the training load was increased by 2.5 kg. Each set was separated by 2–3 minutes of rest. The training session lasted for approximately 20 minutes. The CG was encouraged to follow exercise advises in accordance with existing recommendations from the American College of Sports Medicine on Bone Health (18). The exercise recommendations given to the CG were voluntarily followed and were solely intended as motivation for the participants and to ensure compliance.
Of 83 volunteers, 30 were randomly drawn to participate in the study (Figure 1). Inclusion criteria were female gender between 18 and 30 years of age. Subjects were excluded if they had any disease, injuries, or other conditions that made them unable to perform the physical tests or training, or if they had participated in systematic strength training of the lower extremities in the last 6 months before the study. They were also excluded if they had diseases or used medications known to affect bone metabolism. Subjects in the TG were excluded from the analyses if not fulfilling at least 80% of the planned training sessions. Participants were recruited by posters on the campuses at the Norwegian University of Science and Technology, Trondheim, Norway. The study was approved by the Regional Committee for Medical and Health Research Ethics in Central Norway. All participants reviewed and signed an informed consent form, in line with the Declaration of Helsinki.
Dual-Energy X-ray Absorptiometry
Bone mineral content (BMC) and BMD at the lumbar spine (L1–L4) and hip region were measured by dual-energy X-ray absorptiometry (DXA) applying Hologic (Discovery, S/N 83817). The coefficients of variations for BMD were 1.1% at the lumbar spine, 1.3% at the total hip, and 1.5% at the femoral neck. Whole-body scans were also included to analyze body composition and body weight. All DXA measurements were carried out by a certified technician at the Department of Endocrinology at St. Olav's Hospital, Trondheim, Norway.
Maximal strength in the lower extremities was tested by 1RM in the same hack squat machine as used in the training procedure as previously described (26). The 1RM test was executed from straight legs, down to a 90° angle between the front side of the lower leg and upper side of the thigh and up again. Several lifts were performed with increasing loads of 5 kg for each lift. One repetition maximum was determined as the highest load that was successfully lifted.
Dynamic and Isometric Rate of Force Development
Dynamic RFD and peak force (PF) were obtained in the same hack squat machine as used in the 1RM tests, using a force platform (9286AA; Kistler, Switzerland), with loads corresponding to 80% of the participant's pretest 1RM as previously described (26). Measurements were performed starting at a 90° angle at the knee joint, and participants were instructed to execute the lift as rapid as possible. Dynamic RFD was analyzed as the time difference between 10 and 90% of PF. Maximal dynamic RFD and PF were regarded as the best performance within 3 attempts.
Isometric RFD and PF were measured with the same force platform as used for the dynamic measurements. The force platform was placed underneath an adjustable, rigid bar, and the participants were instructed to place the feet in a standardized position on the force platform. The bar was placed on the participants' shoulders and fixed in a position corresponding to a 70° angle in the knee joint (0° = straight legs). Each of the positions were registered and used for the posttests. Subjects remained in this position for a few seconds until given signal to execute a lift as rapid and forceful as possible. Maximal isometric RFD and PF were regarded as the best performance within 3 attempts. Data were collected at 2,000 Hz (Bioware v3.06b). Isometric RFD was analyzed at 30, 50, 100, and 200 milliseconds. The starting point of isometric RFD was defined as the time where the baseline value was exceeded by 2.5% of the difference between baseline force and PF.
Maximal Oxygen Consumption (V[Combining Dot Above]O2max)
V[Combining Dot Above]O2max was assessed using a metabolic gas analyzer (Metamax II; Cortex, Germany), following standardized protocols, as previously described (12). The tests were performed on a treadmill, applying incrementing workloads. V[Combining Dot Above]O2max was defined as the mean of the highest oxygen consumption values measured during a 30-second interval.
International Physical Activity Questionnaire
The International Physical Activity Questionnaire (IPAQ) was used to monitor possible differences in physical activity level between the groups throughout the intervention period. The IPAQ calculates average weekly physical activity level by estimating the metabolic equivalent of task score (MET). The IPAQ accounts for the total number of minutes per week spent on low-, moderate-, and vigorous-intensity activities (3.3, 4.0, and 8.0 MET-minutes/week, respectively).
Blood samples (5 ml) were drawn in the morning following an overnight fast, by venipuncture with stasis, and collected on vacuum tubes for serum. For serum preparation, blood samples were left in room temperature for 30 minutes before being centrifuged for 10 minutes at 3,000g. Serum samples were stored at −80° C until further analyses. Serum levels of the bone formation marker P1NP were determined by radioimmunoassay (Orion Diagnostica, Espoo, Finland). The detection limit was 2 µg·L−1, and inter- and intra-assay variations were 6.5 and 7.0%, respectively. Concentration of the bone resorption marker CTX was determined by a Serum CrossLaps enzyme-linked immunosorbent assay (ELISA) (Nordic Bioscience Diagnostics A/S, Herlev, Denmark). The detection limit was 0.020 ng·ml−1, and inter- and intra-assay variations were 6.5 and 5.1%, respectively. Sclerostin in serum was analyzed by an ELISA sclerostin kit (Biomedica, Wien, Austria). The detection limit was 2.6 pmol·L−1, and inter- and intra-assay variations were 4 and 5%, respectively. Detection limits and variances were determined by the manufacturers.
This study was not adequately powered to detect bone adaptations by DXA after such a short training intervention. However, from previous observations (10,26) we expected a change of ∼25% in the bone formation marker P1NP, as an indicator of osteogenic response from training. With a power of 80% and a significance level of 5%, 12 participants in each group were required to detect such a difference. Levene's test of variances was performed on all parameters, demonstrating normally distributed data. Parametric statistics were used to detect differences within each group, using 2-tailed paired t-tests on pretest and posttest values. Differences between groups were evaluated on delta values by 2-way analysis of variance. Two-tailed tests were used in all analyses. Data are presented as arithmetic mean ± SD. In figures, data are presented as arithmetic mean and SEM. The p-values ≤ 0.05 were considered significant. All statistical analyses were made using the software programs SPSS (version 19.0) and GraphPad Prism (version 5.0).
Thirty healthy women (18–27 years of age) were included in the study. The subjects' characteristics are presented in Table 1. No significant differences were apparent in baseline characteristics between the TG and CG (Tables 1–4). Likewise, baseline values of all outcome variables were similar in the TG and CG. There was no difference between the groups in the use of oral or hormonal contraceptives. The participants were fit for their age with maximal oxygen consumption (V[Combining Dot Above]O2max) of ∼49 ml·kg−1·min−1, which indicates that the participants in both groups were physically active individuals (4). V[Combining Dot Above]O2max did not change throughout the intervention period in either of the groups, and no difference was observed between the groups in self-reported activity level throughout the intervention (Table 2). In the TG, 1 participant withdrew because of personal reasons, leaving 14 participants for statistical analyses. The subjects in the TG completed 89% of the scheduled training sessions.
Rate of Force Development and One Repetition Maximum
The TG improved dynamic RFD and PF by 81.7% (p < 0.01) and 12.6% (p < 0.001), respectively. The CG also increased dynamic RFD and PF by 27.2% (p = 0.031) and 5.8% (p < 0.01), respectively. However, dynamic RFD and PF improvements were greater in the TG compared with the CG (p = 0.043 and 0.029). In the TG, isometric RFD rose by 505.4 N·s−1 at 30 milliseconds (p ≤ 0.05), 653.2 N·s−1 at 50 milliseconds (p < 0.01), 678.5 N·s−1 at 100 milliseconds (p < 0.01), and 326.8 N·s−1 at 200 milliseconds (p = 0.034), whereas no changes appeared in the CG. At 100 milliseconds, the isometric RFD improvements in the TG differed from the observations in the CG (p = 0.031). Isometric PF improved by 8.0% in the TG (p = 0.016) and 7.0% in the CG (p = 0.036). One repetition maximum increased by 97.7% in the TG (p < 0.001) and 12.9% in the CG (p < 0.01). One repetition maximum increased more in the TG compared with the CG (p < 0.001). Results are presented in Figure 2 and Table 2.
Four of the whole-body DXA scans were excluded from the analyses because of errors in subject positioning (1 in the TG and 3 in the CG). Within the TG, body weight increased by 1.50 kg (p = 0.026) while body fat increased by 0.75 kg (p < 0.01) at the whole body and 0.35 kg (p < 0.01) at the lower extremities. Lower extremity lean mass also increased by 0.42 kg (p = 0.043) in the TG. These results were not significantly different from observations in the CG. No changes in anthropometric variables occurred in the CG. Results are presented in Table 3.
Dual-Energy X-ray Absorptiometry Bone Measurements
Following 12 weeks of MST, BMD and BMC at the lumbar spine increased by 2.2% (p < 0.01) and 3.4% (p < 0.01) in the TG, whereas no changes occurred in the CG. Lumbar spine BMD and BMC increased more in the TG than in the CG (p < 0.001 and p = 0.011, respectively). At the intertrochanteric hip and total hip, BMD improved by 1.0% (p = 0.016) and 1.0% (p < 0.01) in the TG, whereas no changes appeared in the CG. Total hip BMD also improved more in the TG than in the CG (p = 0.022). No changes occurred in whole-body BMD in neither the TG nor the CG. Results are presented in Figure 3A and Table 4.
Serum Bone Markers and Sclerostin
Serum levels of P1NP increased by 26.2% in the TG (p < 0.01), whereas no changes occurred in the CG. The elevated P1NP levels in the TG differed significantly from what was observed in the CG (p = 0.015). No changes were observed in the serum levels of CTX or sclerostin in either group. Results are presented in Figure 3B and Table 4.
This study showed that MST may be an effective intervention to increase BMD at the spine and hip in young adult women. Twelve weeks of MST also caused increased serum levels of the bone formation marker P1NP. The MST intervention also caused improvements in rapid force production and maximal strength in skeletal muscle.
In the present study, BMD increased by 2.2% at the lumbar spine and 1.0% at the total hip in the TG. These results are in line with our recent study where we observed increments in bone mass from the same training intervention in postmenopausal women with osteopenia or osteoporosis (26). The emphasis on progressive loading targeted to the spine and hip, along with high concentric acceleration, may be important contributors to the positive skeletal effects. Several studies have reported similar gains in lumbar spine BMD from strength training interventions in young adults (10,20,32), yet BMD improvements at the proximal femur have been less pronounced. Lumbar spine BMD gains of 1.2 and 2.8% have previously been reported from 5 to 8 months of strength training in young adult women (20,32). One of these studies also reported trochanter BMD to improve by 2.0% after 18 months of training (20). Both these studies applied multiple lower extremity exercises with intensities of ∼75% of 1RM (20,32) and thereby differ from the present study with respect to intensity, number of exercises, and duration of the intervention.
Compared with previous studies (20,32), we observed beneficial skeletal effects after a relatively short training period. One possible explanation for this is the emphasis on intensity monitoring and progressive loading in the MST intervention. In our study, the training load was re-evaluated every training session, ensuring a progressive loading pattern throughout the intervention, which may contribute to stimulate bone formation at an earlier stage. This may also be reflected by the 1RM improvement at the lower extremities, being 98% in the present study versus 58 and 54% in the aforementioned studies (20,32). Using few repetitions and only 1 exercise may contribute to ease the monitoring of loading progression.
Kohrt et al. (17) have defined impact-exercise as “…activities that take advantage of the body mass impacting the ground to generate gravitational loading.” A combination of high-impact exercises and strength training has been reported to be more effective for improving BMD at the hip and spine than each training mode alone (24). While high-impact exercises, primary ameliorate BMD at the hip region (24), and strength training commonly increases BMD at the lumbar spine (23). Still, one study by Kato et al. (15) reported a BMD gain of 2.4% at the lumbar spine and 2.6% at the femoral neck after 6 months of high-impact jump training (10 jumps per day, 3 days per week). Similar to our study, Kato et al. (15) applied a simple intervention consisting of only 1 exercise with few repetitions and high concentric acceleration. However, during high-impact jump training, the highest bone strain rate is mainly generated through ground reaction forces from the landing, whereas in our study, the highest bone strain rate is primarily produced by the skeletal muscles during the concentric phase of contractions (15). Moreover, squat exercise MST seems to promote similar skeletal effects as interventions using concurrent strength training and high-impact exercises (37,38), possibly because of the compressive loading through the spine and hip and the emphasis on rapid force development during contractions.
We observed a marked increase in maximal dynamic squat RFD and early-phase isometric RFD, which agrees with previous reports from MST studies (12,34) and demonstrates that MST improves neuromuscular performance. Rantalainen et al. (30) demonstrated that neuromuscular performance robustly predicts bone quality in both premenopausal and postmenopausal women, suggesting that neuromuscular outcome measures, such as RFD, are profoundly related to skeletal health. Several previous studies have demonstrated that power training, emphasizing improvements in neuromuscular performance, effectively promotes osteogenic bone adaptations (15,24,33). However, only one of these studies reported to use an intervention where PF during training was generated from skeletal muscle acceleration rather than from impact with the ground (33). It has been reported that bone strain increases when both electromyography-recorded muscle activity and ground reaction forces are high, relative to high ground reaction forces alone (5). High acceleration during the concentric phase of movement, combined with heavy loading, is postulated as essential stimuli for MST-induced RFD improvements, which also seem to be important stimuli for strain-induced osteogenesis.
We observed a 26% increase in circulating P1NP levels in the TG, whereas no significant changes occurred in CTX levels, indicating that the improvement in BMD was caused by an increase in bone formation. Several training studies have used the bone formation marker osteocalcin to identify changes in bone metabolism (22). We chose to analyze P1NP and CTX because these are acknowledged as the most precise and sensitive markers of bone metabolism and are also the most widely used bone metabolism markers clinically (35). Our findings generally agree with previous studies regarding the magnitude of increase in bone formation markers (10,20), although some have not observed such increments (15,27). It has been demonstrated that P1NP is upregulated in skeletal muscle (7) and tendon tissue (25) following exercise. However, nonskeletal origin of P1NP seems to be more apparent in men than in women (25). Circulating P1NP has also been observed to rise acutely after one single bout of exercise (31) and to sustain until 48 hours postexercise (29). In the present study, blood samples were collected at approximately 48 hours after the last training session. Thus, our results may reflect acute responses from 1 bout of MST (i.e., the last training session). If so, P1NP has probably remained elevated in the TG throughout the training period. The observation that increased P1NP coincided with BMD gain supports our assumption that the P1NP alterations reflect positive changes in bone metabolism in response to exercise.
Sclerostin levels in serum did not change after the training period. A longitudinal study recently revealed reduced circulating sclerostin levels after 8 weeks of weight-bearing activities in healthy, physically active premenopausal women (2). So far, reduced levels of sclerostin from resistance-like exercises have only been demonstrated in rodents (21). Still, 1 study demonstrated that an exercise program, consisting of concurrent endurance and resistance training, prevented weight loss–induced elevations of sclerostin in obese older adults (3). Although it might be expected that the high compressive loading applied in the present study should attenuate sclerostin levels, the duration and sample size may not have been adequate to identify such alterations.
Total body weight increased in the TG during the 12-week training period. However, the rise in body weight did not differ significantly from the CG. The slight increase in lower extremity lean mass and fat mass seems to account for most of the weight gain in the TG. Both groups consisted of physically active individuals, as reflected by relatively high aerobic capacity (4). Furthermore, the improved 1RM and dynamic RFD in the CG indicate that several of these participants chose to exploit our encouragement to follow exercise guidelines for skeletal health. One explanation for the increased fat mass could therefore be that the MST sessions, constituting a relatively low training volume, may have caused the participants in the TG to reduce their normal activity level, thus reducing total energy expenditure. Although there was no significant difference between the groups in self-reported activity level during the intervention, the CG tended to score slightly higher than the TG. However, both groups had similar V[Combining Dot Above]O2max at both baseline and follow-up, showing that the weight gain in the TG did not coincide with reduced aerobic capacity.
A weakness of this study was the relatively low sample size and the short training period. In spite of this, BMD improvements were evident. The current study did not exceed what is known as the bone remodeling transient period, which is estimated to be approximately 10 months in premenopausal women (11). Thus, we cannot exclude the possibility that the skeletal improvements observed in our study may have been blunted if the intervention was continued for longer duration. Still, the mechanostat theory proposes that stringent progressive loading, as applied in the present study, will stimulate the higher mechanostat thresholds and promote osteogenesis. Twelve weeks of training with progressive loading will allow approximately 1 bone remodeling cycle to be completed, leaving enough time to achieve an osteogenic response. Yet, the effectiveness of MST to increase BMD in young adults needs to be further explored in trials of longer duration, including a larger sample size.
The present study showed that 1 squat exercise alone, administered at a relatively low volume, was enough to promote beneficial skeletal effects in young adult women. Squat MST seemed to promote similar skeletal adaptations as training programs that have applied concurrent strength training and plyometric exercises, although with a considerable lower volume of training. Our results indicate that compressive loading through the spine, combined with maximal acceleration during the concentric phase of movement, may benefit the osteogenic response from training, resulting in evident increases in bone mass only from 4 series of 3–5 repetitions, 3 times a week. The relatively high intensity used in this intervention (85–90% of 1RM) also promotes strength gains that enable progressive loading over time, which again contributes to amplify the skeletal loading patterns during exercise. Therefore, the training loads should be re-evaluated each training session to assure that the right intensity is maintained. Squat exercise MST may be used as a simple and effective strategy for optimizing peak bone mass in young adults and thereby contribute to prevent age-related bone loss and osteoporotic fractures.
The corresponding author was funded by a PhD grant from the Liaison Committee between the Central Norway Regional Health Authority and the Norwegian University of Science and Technology. The authors thank Kari W. Slørdahl for assistance with the blood sample collection and the immunoassay procedures. The authors declare no conflict of interest.
1. Aagaard P, Suetta C, Caserotti P, Magnusson SP, Kjaer M. Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure. Scand J Med Sci Sports 20: 49–64, 2010.
2. Ardawi MS, Rouzi AA, Qari MH. Physical activity in relation to serum sclerostin, insulin-like growth Factor-1, and bone turnover markers in healthy premenopausal women: A cross-sectional and a longitudinal study. J Clin Endocrinol Metab 97: 3691–3699, 2012.
3. Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR, Qualls C, Villareal DT. Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise
training. J Bone Miner Res 27: 1215–1221, 2012.
4. Åstrand PO, Rodahl K, Dahl HA, Strømme SB. Textbook of Work Physiology. Champaign, IL: Human Kinetics, 2003.
5. Bassey EJ, Littlewood JJ, Taylor SJ. Relations between compressive axial forces in an instrumented massive femoral implant, ground reaction forces, and integrated electromyographs from vastus lateralis during various “osteogenic” exercises. J Biomech 30: 213–223, 1997.
6. Berger C, Goltzman D, Langsetmo L, Joseph L, Jackson S, Kreiger N, Tenenhouse A, Davison KS, Josse RG, Prior JC, Hanley DA. Peak bone mass
from longitudinal data: Implications for the prevalence, pathophysiology, and diagnosis of osteoporosis. J Bone Miner Res 25: 1948–1957, 2010.
7. Crameri RM, Langberg H, Teisner B, Magnusson P, Schroder HD, Olesen JL, Jensen CH, Koskinen S, Suetta C, Kjaer M. Enhanced procollagen processing in skeletal muscle
after a single bout of eccentric loading in humans. Matrix Biol 23: 259–264, 2004.
8. Cussler EC, Lohman TG, Going SB, Houtkooper LB, Metcalfe LL, Flint-Wagner HG, Harris RB, Teixeira PJ. Weight lifted in strength training predicts bone change in postmenopausal women. Med Sci Sports Exerc 35: 10–17, 2003.
9. Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA. Exercise
and bone mass in adults. Sports Med 39: 439–468, 2009.
10. Guadalupe-Grau A, Perez-Gomez J, Olmedillas H, Chavarren J, Dorado C, Santana A, Serrano-Sanchez JA, Calbet JA. Strength training combined with plyometric jumps in adults: Sex differences in fat-bone axis adaptations. J Appl Physiol (1985) 106: 1100–1111, 2009.
11. Heaney RP. The bone-remodeling transient: Implications for the interpretation of clinical studies of bone mass change. J Bone Miner Res 9: 1515–1523, 1994.
12. Hoff J, Gran A, Helgerud J. Maximal strength training improves aerobic endurance performance. Scand J Med Sci Sports 12: 288–295, 2002.
13. Hoff J, Tjonna AE, Steinshamn S, Hoydal M, Richardson RS, Helgerud J. Maximal strength training of the legs in COPD: A therapy for mechanical inefficiency. Med Sci Sports Exerc 39: 220–226, 2007.
14. Iwamoto J, Sato Y, Takeda T, Matsumoto H. Role of sport and exercise
in the maintenance of female bone health. J Bone Miner Metab 27: 530–537, 2009.
15. Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y. Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol (1985) 100: 839–843, 2006.
16. Kerr D, Morton A, Dick I, Prince R. Exercise
effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res 11: 218–225, 1996.
17. Kohrt WM, Barry DW, Schwartz RS. Muscle forces or gravity: What predominates mechanical loading on bone? Med Sci Sports Exerc 41: 2050–2055, 2009.
18. Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR. American College of Sports Medicine position stand: Physical activity and bone health. Med Sci Sports Exerc 36: 1985–1996, 2004.
19. Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J, Li Y, Feng G, Gao X, He L. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res 24: 1651–1661, 2009.
20. Lohman T, Going S, Pamenter R, Hall M, Boyden T, Houtkooper L, Ritenbaugh C, Bare L, Hill A, Aickin M. Effects of resistance training on regional and total bone mineral density in premenopausal women: A randomized prospective study. J Bone Miner Res 10: 1015–1024, 1995.
21. Macias BR, Swift JM, Nilsson MI, Hogan HA, Bouse SD, Bloomfield SA. Simulated resistance training, but not alendronate, increases cortical bone formation and suppresses sclerostin during disuse. J Appl Physiol (1985) 112: 918–925, 2012.
22. Maimoun L, Sultan C. Effects of physical activity on bone remodeling. Metabolism 60: 373–388, 2011.
23. Martyn-St James M, Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women: Evidence of discordant site-specific skeletal effects. Sports Med 36: 683–704, 2006.
24. Martyn-St James M, Carroll S. Effects of different impact exercise
modalities on bone mineral density in premenopausal women: A meta-analysis. J Bone Miner Metab 28: 251–267, 2010.
25. Miller BF, Hansen M, Olesen JL, Schwarz P, Babraj JA, Smith K, Rennie MJ, Kjaer M. Tendon collagen synthesis at rest and after exercise
in women. J Appl Physiol (1985) 102: 541–546, 2007.
26. Mosti MP, Kaehler N, Stunes AK, Hoff J, Syversen U. Maximal strength training in postmenopausal women with osteoporosis or osteopenia. J Strength Cond Res 27: 2879–2886, 2013.
27. Mullins NM, Sinning WE. Effects of resistance training and protein supplementation on bone turnover in young adult women. Nutr Metab (Lond) 2: 19, 2005.
28. Price JS, Sugiyama T, Galea GL, Meakin LB, Sunters A, Lanyon LE. Role of endocrine and paracrine factors in the adaptation of bone to mechanical loading. Curr Osteoporos Rep 9: 76–82, 2011.
29. Rantalainen T, Heinonen A, Linnamo V, Komi PV, Takala TES, Kainulainen H. Short-term bone biochemical response to a single bout of high-impact exercise
. J Sports Sci Med 8: 553–559, 2009.
30. Rantalainen T, Nikander R, Heinonen A, Multanen J, Hakkinen A, Jamsa T, Kiviranta I, Linnamo V, Komi PV, Sievanen H. Neuromuscular performance and body mass as indices of bone loading in premenopausal and postmenopausal women. Bone 46: 964–969, 2010.
31. Scott JP, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD. The role of exercise
intensity in the bone metabolic response to an acute bout of weight-bearing exercise
. J Appl Physiol (1985) 110: 423–432, 2011.
32. Snow-Harter C, Bouxsein ML, Lewis BT, Carter DR, Marcus R. Effects of resistance and endurance exercise
on bone mineral status of young women: A randomized exercise
intervention trial. J Bone Miner Res 7: 761–769, 1992.
33. Stengel SV, Kemmler W, Pintag R, Beeskow C, Weineck J, Lauber D, Kalender WA, Engelke K. Power training is more effective than strength training for maintaining bone mineral density in postmenopausal women. J Appl Physiol (1985) 99: 181–188, 2005.
34. Støren O, Helgerud J, Støa EM, Hoff J. Maximal strength training improves running economy in distance runners. Med Sci Sports Exerc 40: 1087–1092, 2008.
35. Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, Kanis JA. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med 49: 1271–1274, 2011.
36. Vincent KR, Braith RW. Resistance exercise
and bone turnover in elderly men and women. Med Sci Sports Exerc 34: 17–23, 2002.
37. Winters KM, Snow CM. Detraining reverses positive effects of exercise
on the musculoskeletal system in premenopausal women. J Bone Miner Res 15: 2495–2503, 2000.
38. Winters-Stone KM, Snow CM. Site-specific response of bone to exercise
in premenopausal women. Bone 39: 1203–1209, 2006.