Osteoporosis is a skeletal disease characterized by low bone mass and a resulting increase in the risk of fracture. Osteoporosis affects 44 million people in the USA, 80% of whom are women (17). This chronic disease causes 1.5 million fractures annually, 700,000 of which occur at the spine (17). More than 50% of women, whereas only 20% of men over the age of 50, will experience an osteoporosis-related fracture in their lifetime (21). One prevention technique developed in recent years is to build a high peak bone mass during growth and in young adult life. Peak bone mass is the highest bone mineral density (BMD) achieved and is an important determinant of future fracture risk. Someone who does not optimize peak bone mass development in youth is at an increased risk of developing osteoporosis, even without experiencing accelerated bone loss (17).
Resistance training is one of the most commonly prescribed forms of exercise. The clear benefits of resistance training such as muscle hypertrophy, strength, and power (11,24) are only part of the advantages because it has also been demonstrated to be effective in the prevention and treatment of osteoporosis (10,25). The so-called “lower impact” exercises such as swimming, bicycling, and walking that have been demonstrated to provide ground reaction forces varying from 0 to 2 times the body weight do not appear to be as effective at increasing bone. “Higher” impact activities, such as jumping and gymnastics, forces applied to bones can reach 6-8 times the body weight for jumping (16) and 10-15 times body weight for gymnastics, respectively (10). High-impact activities, defined as application of forces, at 4-8 times the body weight have been shown to be effective in increasing bone mass (4). Previous studies have shown loads at the hip and spine of the squat and deadlift exercises to reach 5-8 times body weight (5,6), thus supporting a critical level of force exposure that would support the efficacy of resistance training in optimizing bone health.
Because it is widely recognized that resistance training has a beneficial influence on bone health and when performed during young adult life can help to optimize peak bone mass, it is imperative to fully elucidate the ideal frequency, intensity, duration, and mode of resistance training necessary to optimize bone health. The squat and deadlift exercises were specifically included in our training program to elicit a bone response at clinically relevant sites for osteoporosis, the hip and spine. Therefore, the goal of this study was to investigate bone responses to a 24-week resistance training program in healthy young men and women.
Experimental Approach to the Problem
Recreationally active men and women between the ages of 18 and 23 performed 24 weeks of resistance training, 3 d·wk−1 at periodized intensities varying between 67 and 95% of 1RM on the multijoint exercises of bench press, squats, and deadlifts and 67-80% of 1RM for 7 additional upper and lower body assistance exercises. Volunteers completed questionnaires to assess health history, physical activity, dietary intake, and menstrual history. Baseline testing occurred 1 week before the onset of training, whereas follow-up testing was completed 3-5 days after the last training session. Dual energy X-ray absorptiometry (DXA) was used to assess BMD (g·cm−2) of the spine and hip. Changes in BMD from baseline were evaluated between men and women using an analysis of covariance (ANCOVA), controlling for body mass index (BMI). The influence of the independent variable (gender) was evaluated for possible influence on the dependent variables (change in BMD) at the various bone sites (PA spine, lateral spine, and femoral neck).
Recreationally active male (n = 12) and female (n = 12) volunteers between the ages of 18 and 23 were recruited from the student body at Loyola Marymount University. The participants meeting the study criteria volunteered by agreeing to commit to a 24-week resistance training program. Study criteria included previous experience with resistance training, no current musculoskeletal injuries limiting training, and a BMI between 18 and 30. To be able to evaluate typical changes in BMD for this young healthy population, an additional 5 men and 5 women were recruited to serve as controls. Controls were asked to continue with their normal prestudy physical activity patterns throughout the study period. This protocol was approved by the Loyola Marymount University Institutional Review Board for Human Subjects, and written informed consent was obtained before beginning any phase of the study. Four exercisers (2 men and 2 women) and 1 control (man) dropped out of the study after baseline testing. Two men and 1 woman cited scheduling difficulties between training and academic responsibilities as being too great. One woman ceased training because of the re-emergence of a previous back condition that became exacerbated by the exercise protocol. In total, 10 male and 10 female participants completed the entire training intervention, whereas 4 male and 5 female controls were tracked for the same duration. Lastly, 1 male control subject was lost to follow-up. Baseline descriptive data of the 29 subjects included in this analysis can be read in Table 1.
Height in centimeters was measured using a stadiometer (Seca Accu-Hite, Columbia, MD, USA), and weight was taken in kilograms on an electronic scale (Tanita BWB-627A, Tokyo, Japan). We calculated BMI by dividing weight in kilograms by the square root of the height in meters. At baseline, after 12 weeks of training, and after 24 weeks of training, study volunteers completed questionnaires to assess health history, physical activity, dietary intake, and menstrual history. The Aerobic Center Longitudinal Study Physical Activity Questionnaire (18) was used to assess regular physical activity. The questionnaire allows for calculation of intensity and duration of regular exercise in metabolic equivalents (MET-hours per week) by using age, body weight, hours per week of physical activity, and intensity of the activity (Table 1). This self-administered questionnaire has previously been validated with this population (9). Participants completed the rapid assessment method (RAM) questionnaire designed to evaluate daily calcium intake for the past 7 days. This questionnaire has been validated and deemed reliable for this population (7). Baseline calcium intake is given in Table 1. To allow for evaluation of seasonal variation in dietary intake, participants completed the RAM questionnaire when entering the study and at completion (Table 2). A menstrual history questionnaire was administered to female subjects to qualitatively and quantitatively describe menstrual irregularities. None of the women experienced primary amenorrhea, and all were currently menstruating regularly at baseline and follow-up. Seven of the 12 female exercisers reported using oral contraceptives for a duration between 1 and 3 years. None of the female control subjects reported oral contraceptive use.
Resistance Training Program
The training program was designed to be a contemporary, high-demand, yet realistic plan for nonathletic young adults to implement with the objective of improving bone health and lowering future risk for osteoporosis. The program was performed for 24 weeks with a frequency of 3 nonconsecutive days per week under the close supervision of a personal trainer to ensure correct technique, offer encouragement, ensure adherence, and decrease chance of injury. The training program included exercises for the upper, lower, and core musculature. Day 1 was designed to emphasize the lower body, day 2 the upper body, and day 3 a combined exercise day. The program was periodized and included a 2-week general training phase for the purposes of physical preparation, acclimatization, and technique instruction before the implementation of significant increases in intensity or load. The subsequent 10 weeks were marked by an undulating periodization program where intensity on the multijoint exercises (e.g., bench press, squats, deadlift) were increased according to the guidelines for strength and power development as put forth by the National Strength and Conditioning Association (NSCA) (1). Testing of 1 repetition maximum (1RM) occurred in week 3, 12, and 24 according to protocols set by the NSCA (1). Baseline strength was established using the 1RM test completed in week 3, after 2 weeks to acclimatize to the exercise protocol. The strength values measured during week 3 were used to set intensities throughout the program.
The program undulated on a daily basis in a noncontinuously increasing fashion. There were also heavy-, medium-, and light-intensity days where the resistance was 100, 90, and 80%, respectively, of the assigned training intensity of that day (i.e., light day would be 80% of 85% of 1RM for 6 repetitions not performed to failure). Training loads were adjusted after every 1RM test and throughout the training program using a 2 × 2 rule whereby if the participant was able to perform 2 or more repetitions over the prescribed number for 2 consecutive workouts, the load was increased on the subsequent workout. After the 12-week training period, volunteers were permitted a 3 week break for the winter holidays. A similar 2-week acclimatization, followed by 10 weeks of training, followed the break and coincided with the spring semester of classes. Specific care was taken to include exercises that would target the spine including; deadlift, squat, seated row, and standing overhead dumbbell press. The intensities varied from 67 to 95% of 1RM. Each training session lasted about 75 minutes, beginning with a 10 minute cardiovascular warm-up, followed by at least 1 warm-up set (<50% 1RM) for each multijoint exercise, then 30 minutes of resistance training as described above. Each session concluded with 10 minutes of abdominal and flexibility training. Table 2 contains a complete list of exercises in the order that they were performed each training day.
Bone Mineral Density
Dual energy X-ray absorptiometry (Hologic Explorer, Waltham, MA, USA) was used to assess BMD (g·cm−2) of the spine and left hip. All scans were performed and analyzed by the same technician. The coefficient of variation evaluating test-retest reliability of DXA scans, by this technician, at the Loyola Marymount University Human Performance Laboratory are 1.0% for BMD of the spine and hip. The spine scans allow for analysis of the first 4 lumbar vertebrae (L1-4) in the posterior-anterior (P-A) view and of L2-4 in the lateral view.
Pearson correlation coefficients were run to evaluate relationships between independent variables and BMD. Pearson correlation coefficients revealed that BMI was significantly related to BMD at the P-A and lateral spine (r = 0.388 and 0.500, respectively). Because BMI can explain 10-20% of the variation in BMD (3,19), we considered it a covariant in our analysis. All statistics were analyzed using SPSS software version 16.0 (Chicago, IL, USA). We chose an alpha level equal to or less than 0.05 to be considered statistically significant. To evaluate group differences in change in BMD between men and women, we performed a 2-tailed ANCOVA.
At baseline, male and female volunteers were similar in age, BMI, physical activity, and calcium intake (p > 0.05, Table 1). Men were significantly taller and heavier than women and although not statistically significant, both men and women reported an increase in physical activity of about 8 MET-h·wk−1 between baseline and follow-up. Calcium intakes between men and women were not different at either time point assessed nor did they change significantly over time. Exercisers included in this analysis attended 93% of all training sessions during the 24 weeks of training, demonstrating good adherence with the intervention protocol. Women and men did not differ in the attendance at training sessions. Bone mineral density values at baseline and after 24 weeks of training are displayed in Table 3. The change in BMD, after controlling for BMI, was significantly greater for men at the lateral view of the spine and the femoral neck, whereas changes at the P-A spine followed a similar trend.
We report that a 24-week resistance training program elicited a more favorable bone response in male volunteers than in female volunteers. Male exercisers were found to have an increase in BMD between 2.7 and 7.7%, whereas percent change in women ranged from −0.8 to 1.5%, depending on the bone site (Table 4). In fact, the changes experienced by women are close to the 1% of error associated with BMD measurement. Therefore, the small decrease in BMD observed in the female subjects at the P-A spine is likely a limitation of measurement error. These results raise a concern that perhaps young women do not have the ability to respond as well as men to resistance training exercise prescription in prevention of osteoporosis. Improvements seemed particularly discrepant at the lateral view of the spine but were also observed at the femoral neck, and at a nonsignificant level at the P-A spine (p = 0.061). These 2 sites are particularly high in trabecular bone, which is marked by higher surface area exposure and thus higher remodeling rates, therefore responding more rapidly to changes in lifestyle. Response may be greater in the lateral view of the spine because it is almost entirely trabecular bone and does not include the higher proportion of cortical bone of the spinous process contained in the P-A view. Although another explanation for lack of significant differences at the P-A spine is perhaps because the small sample size of this pilot study did not allow for enough power to detect more significant, real differences.
Maddalozzo and Snow (14) previously reported that 24 weeks of high-intensity resistance training resulted in a gain in BMD in the P-A view of the spine of mature men and not women. Although we used a very similar training program, including squats and deadlifts, for a parallel 24-week duration, the female volunteers in their investigation were postmenopausal and possibly lacking sufficient amounts of estrogen to experience the osteogenic benefit of resistance training. Our participants were young and experiencing normal, eumenorrheic menstrual cycles and yet still did not demonstrate a skeletal benefit from the training stimulus, whereas our men did. In a more recent report of resistance training in postmenopausal women, Maddalozzo et al. (15) reported an osteogenic benefit of squat and deadlift exercises at the spine. Therefore, it appears that these exercises (squat and deadlift) have the ability to elicit a positive impact on bone health in men and women, especially at the spine. However, the findings of Maddalozzo et al. (15) were after 1 year of training, whereas our volunteers trained for only 24 weeks. Ryan et al. (20) reported that a 24-week resistance training intervention created equal responses in BMD at the hip in men and women with the average age of 25 years, however reported no benefit to training at the spine. The training program used in this example did not include the squat and deadlift free-weight exercises but instead used pneumatic variable resistance machines that may not load the spine at high enough intensities to be osteogenic at that site.
There are several possible explanations for the lack of improvement in BMD observed in our female exercisers including hormonal differences, baseline strength, and dietary intake. Hormonal differences may be responsible for the differential sex responses. After investigating bone responses to a running program in male and female mice, Wallace et al. (22) suggested that because of hormonal differences, a longer duration and greater intensity of exercise is required for female mice to demonstrate an equal bone response to male mice.
Another possible explanation is that perhaps the men recruited in our study had greater relative strength at baseline and therefore were able to create greater strain on the bone inducing a more substantial increases in BMD in 24 weeks. In a 6-month investigation of novice and experienced rowers, Lariviere et al. (13) concluded that experienced rowers had higher power output and were able to generate greater forces on the spine than novice athletes. The experienced athletes in their investigation demonstrated a 2.5% increase in BMD at the P-A spine, whereas novice athletes did not change significantly. Although we attempted to obtain groups of equal training history, it is plausible that men in our investigation were more experienced at resistance training at baseline, particularly in the squat and deadlift exercises.
Daily calcium intake is another possible confounder that may explain our findings. Although calcium intake was not significantly different between men and women at baseline or 24 weeks, the women in our study reported an average daily calcium consumption approximately 34% below what is recommended, whereas the men reported consuming about 13% less than recommended at baseline. The male and female adequate intake level for calcium as determined by the Institute of Medicine is 1,300 mg·d−1 for ages 9-18 and is 1,000 mg·d−1 for ages 19-50 (8). Although the mean intake of calcium may be less than recommended, the SD for this variable is quite large indicating that some volunteers were considerably underconsuming, whereas others were meeting more than their needs. Both men and women in our study reported average intakes below the reported national averages of 797 ± 32.4 mg·d−1 for women and 1,025 ± 36.7 mg·d−1 for men aged 20-39 (12,26). It is uncertain whether lower calcium intakes resulted in the blunted bone response observed in female volunteers. Limited data are available that examine the interaction between calcium and exercise; however, Ward et al. (23) found that gymnasts about 10 years of age did not benefit from taking 1,250 mg of calcium carbonate above their dietary food intake of 800 mg·d−1 suggesting that in this high-impact activity, 800 mg·d−1 of calcium is sufficient for optimal bone health. Although our female subjects were not too far from an 800-mg intake (Table 2), it is rational to suspect that skeletal benefits may be derived from improved dietary intake in our female population.
Further comparison of changes in BMD experienced by our exercisers, to that of a ‘control’ population, strengthen the findings. During the same intervention period, examination of the BMD for 4 male and 5 female age-matched controls asked to maintain their normal activity level, reveal about a 1% change in BMD at any given bone site (Table 4). Therefore, even with the small sample sizes, it does not seem likely that all men of this age group are experiencing large gains in BMD, whereas women are not, suggesting that our exercise intervention elicited the results seen here. However, this suggests that although the men and women in our study did not differ by chronological age, it is possible that their skeletons are at different stages of development, allowing the male skeleton to be more responsive because men typically reach peak bone mass a few years after women (2). Regardless of whether men and women of the average age of 20 years have a different skeletal responsiveness, it is still imperative to understand and clearly define the training frequency, duration, intensity, and mode of resistance training that optimizes bone health in young men and women.
In conclusion, our results indicate that a 24-week resistance training program that includes squat and deadlift exercises is effective in increasing BMD in young healthy men, especially at the spine. Unfortunately, the same benefits were not derived by women who followed the same protocol. As epidemiological prevalence data state, women are affected by osteoporosis to a much higher extent than men; therefore, it is imperative to explore exercise interventions that can help to optimize peak bone mass during youth in avoidance of osteoporosis later in life.
A whole-body, high-intensity, periodized resistance training program targeted to impact the spine and hip including exercises such as the squat, deadlift, seated row, and overhead dumbbell press performed 3 d·wk−1, for a total of 24 weeks, improves bone health in college-aged men. After this program with intensities undulating in a periodized manner between 67 and 95% of 1RM appear to be effective for men, whereas women may not experience the same favorable improvements in bone health while following the same training protocol. Reasons explaining the differential sex response warrant further investigation.
We would graciously like to thank Campus Recreation Services at Loyola Marymount University and Dana McCaw along with every single member of the INVEST (Investigating New Variables in Exercise and Strength Training) research team especially: Noel Barragan, David Kohler, and Nicole Lopes for their assistance in analysis and management of the data.
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