Physical activity (PA) has been suggested to be one of the most important modifiable lifestyle factors that can improve a variety of health-related aspects throughout life. There is increasing evidence that diseases in adulthood and old age, such as osteoporosis and related fractures, could be associated with low levels of PA during growth (4,34). Regular weight-bearing exercise is one mode of activity that has been shown to consistently improve bone mass, structure, and strength during childhood and adolescence, which may reduce the risk of osteoporosis and fractures later in life if the benefits are maintained (1,18,22,26,27). However, there are also some reports that a high level of PA during the growing years may be associated with an increased fracture risk because of more exposure to trauma (11,23), particularly early in puberty when bone turnover increases but the accrual of bone mineral lags behind gains in height and weight (5,22,28). Others have reported that increased adiposity is also a risk factor for fractures during growth (16). It is therefore important to identify safe and effective exercise or PA programs that can improve musculoskeletal health and reduce the risk of fracture during growth.
Most current international PA consensus guidelines recommended that children participate in at least 60 cumulative minutes of moderate to vigorous PA per day involving a variety of activities (10,33,36). Others also recommend that children engage in muscle-strengthening and bone-strengthening activity on at least 3 d·wk−1 (36). Although there are an increasing number of reports showing that short-term interventions involving moderate-intensity PA, including school-based programs, can improve aerobic fitness (3,30) and lower the degree of adiposity (2,38), the effects of these programs on other measures of musculoskeletal health and function are limited and the findings mixed (2,15,29,31,32,39). The mixed findings in the literature might be because several different protocols for measuring muscle strength are being used. Also, the mixed findings may be because sex, maturity, age, weight, and stature are all traits that influence muscle strength (2,15,29,31,32,39). In addition, a limitation with many of these studies is that they were short term (weeks to months) and included a relatively small number of children. Whether greater benefits can be achieved by extending the duration of the intervention is not known.
With this background knowledge, we designed a population-based prospective controlled intervention study with moderate-intensity general PA for more than 2 yr to evaluate gender-specific changes in bone mass and bone size, lean body mass (as an estimate of muscle mass), muscle strength, physical performance (as an estimate of neuromuscular function), and fracture risk in prepubertal children. The positive effects of the intervention on bone mass and bone size have previously been reported (1,24). We hypothesized that the 24-month program would promote greater gains in muscle mass, strength, and function in both boys and girls relative to normoactive controls without influencing fracture risk.
Study design and participants.
We launched in Malmö, Sweden, a population-based prospective, controlled exercise intervention study, the Malmö Paediatric Osteoporosis Prevention study, which was designed to annually assess musculoskeletal development in response to a school-based PA program in children age 7–9 yr and onward. The design of the study has previously been extensively described (1,24,25,31,32,37). At baseline, the school curriculum in children assigned to the PA intervention changed from the Swedish standard of 60 min of physical education per week to 40 min·d−1; the controls continued with 60 min of physical education per week (1,24,25,37). Lessons were led by the classroom teachers and included general activities within the standard school curriculum such as ball games, running, jumping, and climbing activities. As school physical education is compulsory, all children had to participate. During the vacation periods, no additional exercise training was provided. The study was conducted according to the 2000 Declaration of Helsinki and was approved by the ethics committee of Lund University (LU 453–98; 1998–09–15). Informed written consent was obtained from parents or guardians of all participating children before study start.
For the fracture epidemiology evaluation, all children within four schools within the same geographical area in the city with similar socioeconomic background were recruited to participate in the study. One school was chosen as the intervention school, and no individualized randomization of the students was performed. The students were assigned to the different schools according to their residential address. Overall, there were 417 girls and 500 boys in the intervention school and 836 girls and 872 boys in the control schools. Because there is only one hospital in the city, virtually all fracture patients in the city attend the hospital, and all fractures could be therefore objectively verified and classified through the radiographic archives. This fracture classification system has been validated in studies during four decades (20), and previous evaluations have found that less than 3% of all fractures are missed by using this system (20). That is, because the fractures were objectively evaluated through hospital registers and not registered through questionnaires, 100% of the children in the target population were included in the fracture survey.
In a subcohort of children, repeated measurements were also performed for anthropometric, body composition (total body and regional lean mass and fat mass), muscle strength, and muscle function. All students in the four schools with school start during 2 yr were invited to participate in the measurements. All children in the subcohort were tested at baseline before the commencement of the intervention and again at the same month 2 yr later. Children with diseases or medication known to influence bone or muscle metabolism were excluded. All children, except one boy adopted from Colombia, were Caucasians. The maturity of the children was assessed by Tanner staging (14), and all children remained in Tanner stage 1 during the study as assessed by our research nurses. A total of 55 of the 61 girls and 84 of the 89 boys in the intervention school who were invited to participate in the study agreed. One girl was excluded because she was 11 months younger than all other girls, and two boys were excluded because of medical reasons. During the follow-up, two boys and five girls moved or declined further participation. In the control cohort, 64 of the 158 girls and 68 of the 169 boys who were invited to the measurements agreed to participate. One girl and one boy were excluded because of medical reasons. During the follow-up, 13 girls and 10 boys moved or declined further participation. An additional four boys had to be excluded because of technical errors of the measurements. Therefore, this report includes 49 girls and 80 boys in the intervention group and 50 girls and 53 boys in the control group with prospective measurements. Dropout analyses in this subcohort revealed that there were no differences in baseline age, height, weight, body mass index (BMI), total body or regional body composition, muscle strength, or vertical jump height (VJH) when comparing the children that completed the measurements and those who only attended the baseline measurement (data not shown). Furthermore, there were no differences in age, height, weight, or BMI when data from the grade 1 compulsory school health examination were analyzed and compared with the children who participated in the baseline measurements with those who denied (25,37). This strengthens the view that the data are generalizable.
Anthropometry and body composition.
Body weight and height were measured by standard equipment. BMI was calculated as weight / height2 (kg·m−2). Total body and regional lean and fat mass were assessed by a dual-energy x-ray absorptiometry total body scan (DPX-L version 1.3z, Lunar®). All scans were performed and analyzed by the same two research technicians. The precision, evaluated by duplicate measurements in 13 healthy children with a mean age of 10 yr, was 3.7% for total body fat mass and 1.5% for total body lean tissue mass.
Concentric isokinetic peak torque (PT) of the knee extensors and flexors at 60°·s−1 and 180°·s−1 was assessed by computerized dynamometer (Biodex System 3®; Biodex Medical Systems, Shirley, NY). Two physiotherapists performed the measurements. During the strength testing, the participants were seated with their hips flexed to 85° from the anatomical position. The axis of the knee was aligned with the Biodex axis of rotation. The participants were secured in the chair according to the standard Biodex procedure using shin, thigh, pelvic, and upper crossing torso stabilization straps. When required, a 10-cm-thick pad was used to fill the space between the participants back and the support of the chair. When the lever arm of the Biodex was longer than the lower leg of the participant, a small pad was used to adjust for the difference. All participants were instructed to place their arms across their chest during the testing. The knee was positioned at 90° of flexion and went through a 75° range of motion, stopping at 15° of flexion. Concentric isokinetic knee extension and flexion PT was tested at an angular velocity of 60°·s−1 and 180°·s−1. After two submaximal repetitions, five maximal repetitions (flexion and extension) at 60°·s−1 were performed. After 30 s of rest, 10 maximal repetitions at 180°·s−1 for both flexion and extension were performed, with the highest PT (N·m) recorded for all measurements. All subjects received both visual and verbal encouragement during the test (13). PT (N·m) at both 60°·s−1 and 180°·s−1 for extension (PTEx60 and PTEx180) and flexion (PTFl60 and PTFl180) were normalized to body weight (kg) and expressed as newton-meters per kilogram. The intraindividual test variability, evaluated as the coefficient of variation for repeated measurements in 21 children, was 6.6% for PTEx60, 12.1% for PTFl60, 12.3% for PTEx180, and 9.1% for PTFl180. Biologically unlikely values, defined as values being higher or lower than 3 SD were excluded, a method suggested by Beck et al. (1,7) and a method commonly used in pediatric studies (1,31,32). This resulted in the exclusion of eight PT values (PTEx60 for one boy in the control group and one girl in the intervention group, PTEx180 for one girl in intervention and one girl in the control group, PTFl60 for one boy in intervention and one boy and one girl in the control group, and PTFl180 for one girl in the intervention group).
Vertical jump height.
VJH, an estimation of neuromuscular performance, was used to assess neuromuscular performance. The vertical jump test was performed on an electronic mat connected to a digital timer that registered the total time in the air (product name, “Time It”; Eleiko Sport ®, Halmstad, Sweden). From these data, the height of the jump in centimeters was automatically calculated from the computer included in the standard equipment. All vertical jumps were performed from a standing position, and participants were first required to jump onto the mat with both feet and then make a maximal vertical jump. Each subject performed three vertical jumps from which the highest jump (cm) was recorded. The intraindividual test variability, evaluated as the coefficient of variation for repeated measurements in 21 children, was 5.9%.
Lifestyle and PA habits.
A questionnaire, used in previous pediatric studies (1,24,25,31,32,37), evaluated lifestyle factors including duration of organized PA, nutritional habits, menarcheal age, use of medication, and diseases. The duration of PA in school and organized PA during leisure time was registered and the sum was reported as the total duration of PA. The mean level of PA during the follow-up period was calculated as the sum of the total PA at baseline after initiation of the intervention and at follow-up divided by two.
Statistica® version 7 (StatWin®; SXR Software, Moscow, Russia) was used for statistical calculations. Data are presented as mean ± SD or mean (95% confidence interval). The rate ratio (RR) of fracture risk was estimated by Poisson distribution. In the subcohort study, the Student t-test between means and the Fisher exact test were used for gender-specific group comparisons. To evaluate the effects of the intervention on changes in body composition, muscle strength, and VJH, all data for both groups were converted into annual changes according to the following formula: ([follow-up − baseline measurement] / duration of follow-up), and data were expressed as the absolute or percentage change from baseline. ANCOVA was used to adjust for group differences in age at baseline and baseline values for PT or VJH for each specific trait and annual changes in height when comparing the annual changes. ANCOVA was also used to analyze whether there were any group-by-gender interactions. P < 0.05 was regarded as a statistically significant difference. For the fracture data, the study has 80% power to detect an RR of 1.3 at a significance level of 0.05.
In the subcohort of children with physiological measurements, there were no significant group differences at baseline in age, anthropometry, lean or fat mass, or registered lifestyle factors. However, weight-adjusted PT was higher in both girls and boys in the control group than that in the intervention group (Table 1). Girls in the control group also had a higher VJH (Table 1). Before the intervention was initiated, there were no differences in total duration of PA between the groups, whereas throughout the intervention, the children in the intervention group were more active (Table 2).
For all body composition and muscle strength measures as well as VJH, there was no group-by-gender interaction (Table 3). The annual increase in weight-adjusted PT extension at 180°·s−1 was significantly greater in both girls (P < 0.001) and boys (P < 0.01) in the intervention than that in the control group. The boys in the intervention group also had a greater annual increase in PT flexion at 180°·s−1 (P < 0.001), whereas the girls in the intervention had a greater annual increase in VJH (P < 0.05) (Table 3). These differences between groups remained when adjusting for age at baseline and baseline values for respective traits and for changes in height. All these findings also remained significant after adjusting for organized PA outside school (data not shown). Further, all these results remained unchanged if the annual change in leg lean mass was included as a covariate in the PT analysis (data not shown). For body composition, girls in the intervention group had a larger gain in total body and regional lean body mass (P ranging from <0.05 to <0.001). Unexpectedly, both boys and girls in the intervention group also experienced a greater annual increase in fat content (P ranging from <0.05 to <0.01) (Table 3).
During the study period, 84 fractures were registered in the 2625 children who were included in the fracture evaluation. There were 30 fractures in the intervention group (17.8 events/1000 person-years) and 54 fractures in the control group (16.7 events/1000 person-years), which resulted in a nonsignificant RR of 1.07 (0.66–1. 68) (Table 4). There were no group differences in the gender-specific fracture evaluation (Table 4). The fractures were the result of a slight trauma in 46 cases (55%) and moderate trauma in 26 cases (31%), and there were no information about trauma mechanism in 12 cases (14%). During the study, there were no fractures because of a high energy trauma (i.e., traffic accident or equivalent trauma). The trauma energy preceding the fractures did not differ between groups either in boys nor girls (all P > 0.1), data not shown.
This 24-month population-based, prospective, controlled, school-based exercise intervention study shows that an increase in the duration of general moderately intense physical education in the school from 60 to 200 min per week resulted in a greater gain in lean mass and VJH in girls and lower limb peak extensor muscle strength at higher velocities in both boys and girls compared with children who participated in the general Swedish PA curriculum. These findings have important public health implications because they provide evidence-based data to support the benefit of school-based physical education as an effective strategy to enhance muscle mass and/or strength in children.
There are several reasons why it is beneficial to enhance musculoskeletal strength during growth. Bone density, muscle mass, and muscle strength are all traits that play an important role in reducing the risk of several chronic musculoskeletal diseases in adulthood (4,5,17,34), and these traits are positively affected by PA (6,18,21,25–27,37). There are now a variety of short-term reports for weeks to months that include prepubertal children, which have shown that there are beneficial effects by structured exercise training program on muscle strength, particularly high intensity resistance training programs (8,15,19) We have previously reported that there were beneficial muscular effects resulting from this general moderate-intensity exercise program after 12 months of training (31,32). Consistent with these findings, we found that the beneficial effects on lower limb muscle strength in both boys and girls remained with a longer (24 months) study period.
In this study, girls but not boys in the intervention group experienced a significantly greater gain in total body and regional lean mass compared with controls. Although the reasons for these gender differences are not clear, these findings are consistent with the results observed after 12 months of training (31,32) and suggest that increasing the amount of moderate-intensity physical education in the school curriculum can improve lean mass in young girls. Interestingly, the finding that all exercise-induced gains in muscle strength remained unchanged after including annual changes in leg lean mass as a covariate implies that the increased muscle strength was most likely related to neural adaptations. Although gains in lean mass are typically associated with gains in muscle strength (12), exercise-induced strength gains in prepubertal children have been largely attributed to neural adaptations because the capacity for muscle hypertrophy is limited during this period because of the absence of sex steroids (9,29,39). Indeed, it has been suggested that strength gains in response to training during the prepubertal period are more likely to be related to changes in motor unit activation, coordination, recruitment, and/or firing frequency (9,15,29). Consistent with this notion, we found that the intervention only led to gains in PT at the highest velocity (180°·s−1) and that girls in the intervention group also experienced a greater increase in VJH than those in the control group, independent of changes in lean mass. The task of performing a vertical jump requires both motor coordination and muscle power, which both have a strong neural component.
An unexpected finding in our study was the greater annual gain in fat mass in the intervention group compared with the controls (Table 1). However, other researchers have also reported an increase in fat mass in children associated with increased physical training (31,32,35). The greater gain in fat mass in the intervention group in the present study could be explained by an increased food intake accompanying the increased training. Although we did not assess dietary habits, we have previously reported that the discrepancy in fat gain was most likely the result of other influences besides PA because there was no dose–response relationship between the duration of exercise and the gain in fat mass (24,25).
Before such school-based physical education programs can be recommended and implemented on a broader scale, it is also important to show that the program does not confer any adverse effects, such as an increase in fractures. Previous research has shown that a high level of PA in children may be associated with an increased fracture risk, particularly forearm fracture (11). In this study, we found that there were no adverse effects of the intervention on fracture risk. However, it is important to note that the study had limited statistical power; we only had sufficient numbers and power to state that there was no increase of more than 68% or a decrease of more than 34% with the intervention program.
The strength of this study is the population-based prospective controlled study design that includes both boys and girls with adequate dropout analyses that increase the ability to generalize our inferences. In addition, this was a school-based intervention that was widely available to all children, not just children with specific ability and/or specific interest in PA or sports. This is important for informing policy and public health practice. There were several study limitations, including the nonrandomized design. An individual randomization would be advantageous but was refused by the principals, teachers, parents, and children because it was neither feasible nor practical for some children to be given additional exercise during compulsory school hours whereas others were not. However, because all schools had a similar amount of regular school physical education before the study started and because there were no differences in anthropometry measures between participants and nonparticipants or between participants and dropouts, the risk of selection bias seems minimal. Another weakness is the lack of a measure of leg length. This is important because changes in limb length could influence the muscle moment arm in relation to the improvement in torque production. However, the inclusion of changes of height in the analyses at least partly compensated for any potential differences in length. Also, during the different breaks from school, the children received no intervention. This may have reduced the estimated effect of the intervention program because of possible detraining in the intervention group. Another limitation is that PA habits were assessed by questionnaire and limited to organized exercise only. Finally, it would have been advantageous to include a larger sample size in the fracture evaluation to improve the power in fracture risk calculations.
In conclusion, the findings from this study infer that a general moderately intense school-based exercise intervention program for 2 yr in prepubertal children can improve lean mass and neuromuscular performance in girls and lower limb muscle strength in both boys and girls without increasing fracture risk. These findings may have important clinical implications because the first two decades in life seem to be an important period to reduce the risk of future chronic musculoskeletal health conditions including fractures. The findings of this study also support the notion that increasing the compulsory school-based physical education is a feasible strategy to improve musculoskeletal health on a population-based level because all children can be targeted.
The authors thank the teachers and the students for their help with the study and Per Gärdsell and Christian Linden who participated in the initiation of the POP study. The results of this study do not constitute endorsement by the American College of Sports Medicine.
The authors declare that they have no competing interests.
BL carried out the statistical analysis, the interpretation of data, and the writing of the manuscript. RD was involved in the statistical analysis, the interpretation of data, and the writing of the manuscript. JÅN was involved in the statistical analysis and the interpretation of data. MD was involved in the collection of data and the writing of the manuscript. MK designed the study, collected the data, worked with the analysis and the interpretation of data, and was in charge of writing the manuscript. All authors contributed intellectually to the manuscript, and all authors have read the manuscript and approved the submission.
Financial support for this study was provided by the Swedish Research Council, the Centre for Athletic Research, the Herman Järnhardt Foundation, and the Alfred Påhlson Foundation.
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