Osteoporosis is a chronic disease with the highest prevalence among postmenopausal women. These patients suffer increased fracture risk because of reduced bone mineral density (BMD) and impaired bone quality (23). Osteopenia refers to a condition where BMD values are between 1 and 2.5 SD below the average BMD of young women, whereas in osteoporosis, the BMD is 2.5 SD or more below the average. Sarcopenia refers to the skeletal muscle atrophy and weakness that often accompany aging. Osteoporosis and sarcopenia are both major contributors to the frailty syndrome, an age-related loss of physiological function that is most pronounced in women (9). Frailty leads to falls, and >90% of hip fractures among older adults are caused by falls from standing heights (9), causing disability and increased mortality (23).
Current guidelines recommend strength training and weight-bearing exercises for preventing bone loss and maintaining bone mass in patients with osteoporosis (16). Strength training has been shown to maintain, or improve BMD in postmenopausal women, and strength training at high intensities seems to be most effective (10). Strength training has also been shown to promote increased levels of bone formation markers, for example, type 1 collagen amino-terminal propeptide (P1NP), and reduced levels of bone resorption markers, like, type 1 collagen C breakdown products (CTX) in the blood (19). However, what type of strength training is most efficient for improving skeletal health is not settled.
A positive association between maximal muscle strength, measured as 1-repetition maximum (1RM) and bone mass has previously been reported (5,15). Strength training programs emphasizing improvements in the 1RM seem to be effective for improving BMD and bone mineral content (BMC) in postmenopausal women (15,18). Power training, focusing on high-speed contractions, was in 1 study reported to be more effective than conventional strength training for reducing bone loss in postmenopausal women (24). Another study showed that neuromuscular performance robustly predicted bone strength in postmenopausal women (22). The latter finding suggests that rate of force development (RFD) capacity may also be important for skeletal adaptations from training. The RFD is considered as a fundamental part of muscular mechanical function and physical capacity (1). Lower extremity RFD is also associated with improved reaction speed and subsequent fall prevention (4). Altogether, these findings suggest that strength training interventions that improve both the 1RM and RFD are likely to be effective for promoting skeletal health in postmenopausal women.
Maximal strength training (MST) is characterized by high loads and few repetitions, with special emphasis on fast mobilization of force in the concentric part of movement. The MST has previously been shown to improve lower extremity 1RM and RFD in elderly and diseased individuals (12,14,27). Because patients with reduced bone mass may benefit from both 1RM and RFD improvements, the MST may be an advantageous training method for these patients. Furthermore, the emphasis on high acceleration during muscle contraction may induce higher bone strains than conventional strength training, possibly ameliorating the osteogenic responses from training as previously suggested (24). The MST implemented in a squat exercise, with load resting on the shoulders, will induce an axial loading targeting the hip and spine, which are both sites prone to bone loss.
To our knowledge, no studies have so far applied interventions combining heavy loads with high concentric acceleration as in MST, promoting both 1RM and RFD improvements. Most previous studies have also used training programs with a high volume of exercises, which may undermine compliance to the training program. Because the efficacy regarding squat exercise MST in patients with reduced bone mass is not yet known, this study aimed to examine this in patients with osteoporosis or osteopenia. We hypothesized that 12 weeks of squat exercise MST would improve 1RM and RFD in postmenopausal women with osteoporosis or osteopenia and that this would coincide with improvements in BMD, BMC, and serum levels of bone metabolism markers.
Experimental Approach to the Problem
This study was designed to investigate the effects of squat exercise MST on 1RM, RFD, and bone-related parameters in patients with osteoporosis or osteopenia. Peak oxygen consumption (V[Combining Dot Above]O2peak) was measured to control for possible changes in activity levels and concomitant alterations in aerobic fitness. Twenty-one patients with osteoporosis or osteopenia volunteered to participate in the study. For each participant, measurements were obtained within 14 days before entry and 5 days after finishing the study. The participants were stratified by BMD T score and randomly allocated to a training group (TG, n = 10) and a control group (CG, n = 11).
The TG followed a training program consisting of supervised MST for 12 weeks, comprising 3 sessions each week for a total number of 36 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 (12). The training sessions consisted of 1 exercise, using the lower extremities in a squat exercise machine (Impulse Fitness IT 7006, Shandong, China). The exercise was executed from straight legs, down to a 90° angle in the knee joint and up again (Figure 1). 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 part of movement. The participants were encouraged to perpetuate until fatigue. To assure sufficient progression of intensity, the participants' training loads were evaluated each training session. If the participants could perform >5 repetitions, the training load was increased by 2.5 kg. Each set was separated by 2–3 minutes of rest. The CG was encouraged to follow current exercise guidelines for osteoporotic patients (16).
The participants were recruited via their general practitioner, via advertisement in newspapers or from the outpatient clinic at the hospital. Women who were at least 2 years postmenopausal, <75 years, and had a BMD T score between −1.5 and −4.0 at the lumbar spine, femoral neck, or total hip were eligible for inclusion. Exclusion criteria were fractures during the last 2 years, use of glucocorticoids or treatment for osteoporosis, other than calcium and vitamin D. Women were also excluded if they had any condition that precluded them from taking part in the exercise testing procedures or failed to participate in at least 80% of the planned training sessions. The participants’ V[Combining Dot Above]O2peak indicated that they were normally fit for their age (∼30 ml·min−1·kg−1, Table 2). None of the participants had been doing strength training during the last year before inclusion. All the participants received calcium and vitamin D supplements during the intervention period. The study was approved by the regional medical ethics committee of central Norway. All the participants reviewed and signed an informed consent form, in accordance with the Declaration of Helsinki.
Maximal Strength and Rate of Force Development
Maximal strength was obtained as 1RM, using the same squat exercise machine and execution as described in the experimental approach. Several lifts were performed with increasing loads of 5 kg for each lift. The 1RM was determined as the highest load that was successfully lifted. The RFD and peak force (PF) were obtained in the squat machine with loads corresponding to 80% of the participant's pretest 1RM, using a force platform (9286AA, Kistler, Switzerland). Measurements were performed starting at a 90° angle at the knee joint, and the participants were instructed to execute the lift as rapid as possible. Maximal voluntary RFD and PF were regarded as the best performance within 3 attempts. Data were collected at 2,000 Hz (Bioware v3.06b, Kistler), and RFD analyzed as the time difference between 10 and 90% of the PF. The 1RM and RFD testing procedures have been described previously (27). The participants were encouraged to maximal effort. All the tests were performed during midday, and the participants were instructed to meet hydrated and prepared to the testing.
Dual X-ray Absorptiometry
The BMC and BMD at the lumbar spine (L1–L4), femoral neck, and total hip were measured by dual X-ray absorptiometry (DXA) applying Hologic (Discovery, S/N 83,817). The coefficient of variation was 1.1% at the lumbar spine and 1.5% at the femoral neck. All DXA measurements were carried out by a certified technician at the Department of Endocrinology at St. Olav's Hospital, Trondheim, Norway.
Vitamin D and Markers of Bone Metabolism
Twenty-five-OH vitamin D in the serum was determined at baseline by a Roche Cobas e601 immunology analyzer (Roche Diagnostics, Holliston, MA, USA), using standardized procedures. 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 interassay and intraassay variations were 6.5 and 7.0%, respectively. The concentration of the bone resorption marker CTX was determined by a Serum CrossLaps enzyme-linked immunosorbent assay (Nordic Bioscience Diagnostics, Herlev, Denmark). The detection limit was 0.020 (ng·ml−1), and interassay and intraassay variations were 6.5 and 5.1%, respectively. Blood samples were collected in the morning, after an overnight fast, and the serum samples were stored at −80° C until analyses.
The treadmill tests were performed to control for possible changes in the aerobic capacity among the participants during the intervention. Peak oxygen consumption (V[Combining Dot Above]O2peak) was attained using a metabolic gas analyzer (Metamax II, Cortex, Leipzig, Germany) during an incremented workload protocol as previously described (20,28). The V[Combining Dot Above]O2peak was defined as the mean of the highest oxygen consumption values during an interval of 30 seconds. Peak heart rate (HRpeak) was assessed with a heart rate monitor (Polar Electro, Kempele, Finland). Concentration of lactate in blood ([La−]b) was determined in blood samples drawn from the fingertip within 1 minute after the maximal treadmill test, and analyzed with an YSI 1500 Sport Lactate Analyzer (Yellow Springs Instrument Co., Yellow Springs, OH, USA). The treadmill testing procedures have been described previously (20,28).
This study was not adequately powered to detect bone adaptations from such a short training intervention. However, the 1RM and RFD were regarded as the primary outcome variables. From previous observations (20,27), we expected a change of approximately 50 kg (SD ∼25 kg) in 1RM, and approximately 1,500 N·s−1 (SD ∼1,000 N·s−1) in RFD. With a power of 80% and a significance level of 5%, 8 participants in each group were enough to detect such differences. Nonparametric statistics were used because of the relatively low number of subjects. All variables were compared between pretest and posttest to detect possible changes within each group. To avoid multiple testing, between groups, comparisons were limited to delta values from pretest and posttest on each variable. To detect differences within each group, Wilcoxon signed rank test (paired test) was applied, whereas the Mann-Whitney U test (unpaired test) was used to calculate differences between the groups. To compare the results with other studies, data are presented as arithmetic mean ± SD. In figures, data are presented as arithmetic mean and standard error (SE). Changes were considered to be significant at p ≤ 0.05. All statistical analyses were made using software program SPSS (version 19.0) and GraphPad Prism (version 5.0).
Twenty-one women were included. In the TG, 1 participant withdrew, and 1 was excluded because of not obtaining the required amount of training. In the CG, 3 participants withdrew. Eight women in each group completed the study. At baseline, the TG and CG differed in the half squat 1RM and RFD. Because the subjects were stratified by the BMD T score, and as the intention of this study was to investigate changes in strength and bone parameters in the groups throughout the intervention period, the initial differences were regarded as acceptable. The TG completed 87% of the planned training sessions. No adverse events occurred during the training period. Participants' characteristics are presented in Table 1.
The TG improved 1RM and dynamic RFD in the squat machine by 154 ± 75% (p = 0.012) and 52 ± 46% (p = 0.018), respectively. The 1RM improvements were significantly greater than in the CG (p = 0.001). Peak force improved by 6.4 ± 4.6% (p = 0.028), within the TG. No changes appeared in endurance capacity parameters (V[Combining Dot Above]O2, maximal treadmill workload and time to exhaustion). The results are presented in Figure 2A and Table 2.
The BMC at the lumbar spine increased by 2.9 ± 2.8% (p = 0.012) from baseline in the TG (Figure 2B). This change was significantly higher than in the CG (p = 0.028). The BMC at the femoral neck increased by 4.9 ± 5.6% (p = 0.043) within the TG. Bone area increased by 2.4 ± 2.0% (p = 0.012) at the lumbar spine, and 5.2 ± 5.1% (p = 0.036) at the femoral neck. No changes occurred in the CG. The results are presented in Table 3.
Vitamin D and Bone Markers in Serum
None of the participants had vitamin D deficiency (TG; 80.7 ± 29.2 nmol·L−1, CG; 99.5 ± 16.5 nmol·L−1). No significant changes occurred in the serum levels of P1NP and CTX; however, the ratio of P1NP/CTX increased in the TG (Figure 2C), although not significantly (21.5 ± 40.5%, p = 0.093). The results are presented in Table 3.
In line with the hypothesis, 12 weeks of squat exercise MST improved 1RM, RFD, and BMC in postmenopausal women with osteoporosis or osteopenia. Because patients with reduced bone mass are likely to benefit from 1RM and RFD improvements, and especially BMC attainments, our data suggest that MST has a potential in the prevention and treatment of osteoporosis.
Previous studies have demonstrated a positive association between 1RM and BMD (5,15). The MST has been reported to effectively improve 1RM in the elderly and diseased individuals (12,14,27). In this study, 12 weeks of squat exercise MST improved half squat 1RM by 154% in the TG. This improvement surpasses findings from previous studies that have applied lower extremity training interventions (15,18,21). Kerr et al. (15) found an improved leg press 1RM of 95% after 1 year of resistance training at an intensity of 8 repetitions maximum in postmenopausal women. Nelson et al. (21) reported that leg press 1RM improved by 35.2% after 12 months of strength training at approximately 80% of 1RM in postmenopausal women. Both studies applied several tests for measuring lower extremity 1RM (e.g., leg curl, leg extension, and leg press) (15,21,25). Among these tests, the seated leg press was most comparable with what was used in this study. Comparison of 1RM training response between this study and the studies by Kerr et al. (15) and Nelson et al. (21) is difficult because 1RM changes are exercise specific. Also, the baseline values of lower extremity 1RM were lower in our study than in the study by Kerr et al. (15) and Nelson et al. (21). Still, when compared with previous findings in postmenopausal women, the squat exercise MST used in this study seems to effectively improve 1RM in postmenopausal women with osteoporosis or osteopenia.
A relationship between neuromuscular function and bone quality has previously been reported (22). The RFD is considered as a functional measure of neuromuscular performance (1), and may thus be an important outcome variable regarding strength training and skeletal health. To our knowledge, this study is the first to emphasize training induced RFD adaptations in relation to skeletal health. In this study, the RFD improved by 52% in the TG. These findings line up with previous reports concerning RFD improvements after MST in elderly individuals (12,14,27). The RFD improvements from MST are likely a result of the special emphasis on high acceleration in the concentric phase (2). A previous study demonstrated that power training using rapid execution of muscle contractions, prevented bone loss to a greater extent than conventional strength training in postmenopausal women (24). However, the latter study did not measure possible changes in RFD after the training period (24). The strain from external loads, combined with the reaction force caused by skeletal muscle acceleration may induce sufficient bone strains to effectively stimulate osteogenesis (3,26), and RFD could be a significant outcome measure also in this regard. These 2 factors are difficult to differentiate; however, 1 study reported that the bone strain during axial loading was greater when electromyography-derived muscle activity was high (3). Thus, the high axial strains, combined with the rapid execution of muscle contraction, are likely to be important contributors to the improved RFD and the skeletal effects in this study.
During the training period, the TG improved BMC by 2.9 and 4.9% at the lumbar spine and femoral neck, respectively. These improvements were most likely an effect of training, rather than a result of the calcium and vitamin D supplements, as none of the participants suffered from vitamin D deficiency. In previous exercise studies, increases in BMD have been reported more often than BMC improvements (10,15,18,21). One study observed an improved BMD by 4.5% at the femoral neck and 3.6% at the lumbar spine after 12 months of strength training with multiple exercises (21). Another study reported that 1 year of resistance training improved BMD by 0.43% at the lumbar spine and maintained BMD at the femoral neck in early postmenopausal women (18), which is a lower bone response than observed by others (15,21). The latter study did not report whether progressive loadings were applied during the training period (18). The absence of progressive loading throughout the intervention may cause the overall training intensity to be lower than intended. Also, both aforementioned studies included multiple exercises in the training interventions, making it hard to distinguish which of the exercises that were most effective for gaining bone mass at the different sites (18). Altogether, the squat exercise MST intervention seems to have been efficient because we attain bone responses after a relatively short training period with 1 single exercise.
The improvement of BMC rather than BMD in this study may be explained by the automatic edge detection of the DXA software, as previously argued (6). When the bone mass is low, BMC improvements can induce more effective edge detection, which may cause a larger bone area to be measured. Because BMD is BMC divided by bone area, the result is that although BMC increases, the BMD remains unchanged (11). The BMC baseline values are lower in our participants compared with that in previous investigations (15,18,21), which could cause underestimation of the bone area, measured by DXA at baseline. The BMC changes in this study coincided with an increased bone area, which agrees with this suggestion. Because the edge detection becomes more accurate as BMC increases (6), the posttest measurements of bone area in this study are likely to be most correct. If the DXA measurements are recalculated with the bone area fixed to posttest values, the BMD improvements at the lumbar spine are in line with the findings of Nelson et al. (21) with an improvement of 2.4%.
We observed a 21.5% increase in the serum P1NP/CTX ratio in the TG, although not significantly. This increase is similar to that in previous reports (17,25), and it suggests a positive effect of the MST intervention on bone formation. In comparison; Vincent and Braith (25) reported a 39% increase in osteocalcin (OC) levels, and a 61% improved ratio of OC/pyridinoline crosslinks after 6 months of heavy strength training in elderly women and men (25). This coincided with an increased BMD at the femoral neck (25). Another study found reduced serum levels of OC after 9 months of strength training in postmenopausal women, which may have been caused by an overall reduction in bone turnover rate (17). In the latter study, the BMD increased by 1.5% at the lumbar spine, which demonstrates that bone mass may increase after exercise without corresponding increase in serum markers of bone formation. Also, circulating levels may not reflect the local production of bone metabolism markers.
The present findings are in line with the mechanostat theory of bone by Frost (7), which suggests that weight-bearing bones adapt to the amount of mechanical loading they are exposed to. Frost suggests that the skeletal demands from mechanical loading are sensed by a control mechanism where different thresholds of loading regulate bone metabolism in favor of bone formation or resorption (8,13). Although bones may respond to high frequencies of small loading stimuli (e.g., 20–60 Hz), an osteogenic response is more likely to appear when applying high loads and few loading cycles, because of triggering of the higher mechanostat thresholds (8). In context of the Frost hypothesis, the skeletal effects obtained in our study were probably because of reaching a favorable mechanical threshold, thereby promoting bone formation.
A weakness of this study is the low number of participants, and the short training period. However, based on previous studies from our institution (12,14,27), this study was adequately powered to assess the effectiveness of this training program on the main outcome variables, 1RM and RFD. Furthermore, the initial differences in 1RM and RFD between the TG and CG may be regarded as unfavorable. However, the groups were only compared by delta values for potential changes throughout the intervention period. Thus, the baseline differences were regarded as acceptable.
In conclusion, this study demonstrates that squat exercise MST, applying only one exercise, improves 1RM, RFD, and BMC in patients with osteoporosis and osteopenia. Because patients with low bone mass are likely to benefit from 1RM and RFD improvements, and these changes coincided with skeletal adaptations, MST may be established as a simple and beneficial training method for postmenopausal women with osteoporosis or osteopenia.
Strength training programs for promoting skeletal health should be made simple and effective. Here, we argue that 1RM and RFD are important covariables for skeletal health. Furthermore, we have used a training intervention that is both simple and efficient for improving 1RM and RFD. Our data show that MST in a squat machine exercise alone, targeting sites prone to bone loss and executed at a relatively low volume, is sufficient to induce beneficial effects on 1RM, RFD, and BMC in women with low bone mass. The MST intervention in this study applied high-intensity (85–90% of 1RM) and high axial loading which is in accordance with current guidelines (16). The MST also emphasizes rapid execution of concentric movements, which are suggested to ameliorate bone responses (24), and assumed to be the main stimulus for RFD improvements. However, because high loads compromise movement velocity, it is the rapid execution rather than the actual velocity of movement that is important. It should be noted that our findings may not translate to patients with more severe osteoporosis (i.e., T score <−4.0 and previous fractures) than the participants in this study. Because these patients are more prone to experience fractures, caution must be exerted when giving recommendations concerning exercise.
The authors thank Kari W. Slørdahl for assistance with the immunoassay procedures, and Ellen Gjerlow for assistance with the DXA measurements. This project was funded by the Liaison Committee between the Central Norway Regional Health Authority and the Norwegian University of Science and Technology. The authors declare no conflict of interest. M.P. Mosti and N. Kaehler have contributed equally to the work.
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