1 Department of Sport and Movement Sciences, Faculty of Physical Education and Physiotherapy, Catholic University Leuven, Leuven, Belgium.
2 Department of Movement and Sports Sciences, Faculty of Medicine and Health Sciences, Ghent University, Ghent, Belgium.
3 Department of Physical MedicineRehabilitation, University Hospital Pellenberg, Pellenberg, Belgium.
4 Department of Rehabilitation Sciences, Faculty of Physical Education and Physiotherapy, Catholic University Leuven, Leuven, Belgium.
5 Department of Kinesiology, Faculty of Physical Education and Physiotherapy, Catholic University Leuven, Leuven, Belgium.
6 Department of Rheumatology, University Hospital Gasthuisberg, Leuven, Belgium.
Received for publication March 20, 2002; accepted for publication February 25, 2003.
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ABSTRACT |
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adolescence; bone density; densitometry, x-ray; exercise; follow-up studies; men; sports
Abbreviations: Abbreviations: BMD, bone mineral density; DXA, dual-energy x-ray absorptiometry; HH, subjects participating during adolescence and adulthood in high-impact sports; HN, subjects participating during adolescence in high-impact sports and during adulthood in nonimpact sports or no sports; NN, subjects participating during adolescence and adulthood in nonimpact sports or no sports.
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INTRODUCTION |
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Although comparison of athletes participating in different sports can give valuable information, the results must be interpreted carefully because of the cross-sectional design and the selectivity of the samples under study. However, experimental studies examining the effect of physical activity during childhood and adolescence support the hypothesis that physical activity has a beneficial influence on the skeleton during growth (1623). Furthermore, most experimental studies of adults have concluded that physical activity is beneficial for bone health (2434). Most of these experimental studies focused on women, because osteoporosis was considered primarily a womans disease. Recently, the problem was also acknowledged in men (35).
Little is known about the influence of physical activity during childhood and adolescence on adult bone mass. In some retrospective studies, a positive association of former physical activity with adult bone mass was reported (16, 3643), whereas other authors found no association (44). Only a few longitudinal prospective studies have addressed the issue of the contribution of physical activity during the growing years to adult bone mass (4548). These studies concluded that physical activity during childhood or adolescence is a determinant of peak bone mass. Whether residual benefits are maintained in later adulthood and older age still needs to be demonstrated. Because the subjects of the few longitudinal studies were rather young (aged 1829 years), this question could not be addressed.
In a previous study of the same group of men, we examined the extent to which lifetime physical activity and lifestyle parameters contribute to bone mass (49). However, that study made no distinction between weight-bearing activities and non-weight-bearing activities. Therefore, we conducted the present 27-year follow-up study to examine whether physical activity during adolescence and adulthood, with special focus on the type of physical activity (high impact vs. nonimpact), contributes to bone health in males aged 40 years. In the first part, we studied the relation between bone mineral density (BMD) and impact loading due to sports participation. It was hypothesized that impact loading is positively associated with BMD. In the second part, we addressed this question by analyzing contrasting groups with different histories of sports participation. It was hypothesized that 1) the bone status of subjects involved in high-impact sports during adolescence and adulthood is better than that of subjects involved in high-impact sports during adolescence and in nonimpact sports during adulthood, and 2) the bone status of both of these groups is better than that of subjects involved in nonimpact sports during adolescence and adulthood.
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MATERIALS AND METHODS |
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In the first part of this study, the data on these 154 men were used to study the relation between impact loading due to sports participation and BMD. In the second part, the following three groups based on sports participation during adolescence and adulthood were formed to investigate this question further: group 1participation during adolescence and adulthood in high-impact sports (HH; n = 18), group 2participation during adolescence in high-impact sports and during adulthood in nonimpact sports or no sports (HN; n = 15), and group 3participation during adolescence and adulthood in nonimpact sports or no sports (NN; n = 14) (refer to the section entitled "Sports participation (high impact vs. nonimpact)"). Subjects whose sports participation did not meet these criteria (n = 107) were not included in the second part of this study.
Informed consent was obtained from all subjects. The study was approved by the local medical committee.
Anthropometry
For all subjects, body mass was measured with a balance scale accurate to 0.1 kg. Standing height was measured with a Holtain stadiometer (Holtain Ltd., Crymych, United Kingdom) with subjects barefooted. On each occasion, one experienced anthropometrist took the anthropometric measurements. On the basis of these measurements, a mean score for body mass during adolescence (mean for ages 1318 years) and during adulthood (mean for ages 30, 35, and 40 years) was calculated. In addition, body mass index (weight (kg)/height (m)2) was determined.
Bone measurements
Dual-energy x-ray absorptiometry
When subjects were 40 years of age, BMD (g/cm2) of the lumbar spine and total body was determined by dual-energy x-ray absorptiometry (DXA) (Hologic QDR-4500A; Hologic, Inc., Bedford, Massachusetts). The in vivo precision of DXA at the University Hospital (Leuven) is approximately 1 percent for lumbar spine BMD and less than 1 percent for total body BMD.
Radiogrammetry
In 1969, when subjects were 13 years of age, DXA was not yet available. Therefore, bone was measured by radiogrammetry. With a subjects left hand in a standardized position, radiographs were taken at an exposure of 1.0 second at 30 mA and 70 kV to determine several metacarpal II bone dimensions. The radiographs were scanned and analyzed digitally. Length (L), periosteal width (D), and medullary width (d) of the metacarpal II bone were measured according to the guidelines of Dequeker (52). Several derived measurements were calculated from these basic measurements based on the formulas described by Kimura (53) and Roy et al. (54), as follows: combined cortical thickness = D d (mm), cross-sectional cortical area = (D/2)2
(d/2)2 (mm2), and metacarpal cortical index = (D d)/D.
Intraobserver reliability coefficients of 0.99, 0.98, and 0.92 were obtained for L, D, and d, respectively. A paired t test revealed a significant difference only between the two measurements of periosteal width ( p = 0.002).
Sports participation (high impact vs. nonimpact)
Sports participation was investigated by using a sports participation inventory (55). For each observation, information about the types of sports and the time spent per week (Minutes Sport Participation per week) engaged in the different sports activities was obtained for the period of the year preceding each test session.
Numbers of minutes spent participating in sports activities were calculated for adolescence and adulthood. The mean score for 6 years (ages 1318 years) was calculated to obtain time spent in sports activities during adolescence, and the mean score for the results at ages 30, 35, and 40 years was calculated to obtain time spent in sports activities during adulthood.
In addition, impact scores were calculated. As previously described by Groothausen et al. (45), activities that involve jumping actions were given a peak strain score of 3, those involving explosive actions such as turning and sprinting received a peak strain score of 2, weight-bearing activities were assigned a peak strain score of 1, and all other activities received a peak strain score of 0. First, all peak strain scores for all activities registered in 1 year were summed to obtain an impact score for that year. Furthermore, an impact score for adolescence and an impact score for adulthood were calculated by respectively summing the impact scores obtained for subjects from age 13 years to age 18 years and the impact scores obtained at ages 30, 35, and 40 years.
For the second part of the analysis, three groups were formed based on subjects sports participation during adolescence and adulthood. First, the different sports were divided according to the ground reaction forces involved. Sports whose ground reaction forces were higher than four times body weight were considered high-impact sports (e.g., basketball, volleyball, gymnastics). Sports whose ground reaction forces were between two and four times, between one and two times, and less than one time body weight were respectively considered moderate-impact sports (e.g., tennis, soccer), low-impact sports (e.g., jogging, ballroom dancing), and nonimpact sports (e.g., bicycling, swimming) (23, 45). The HH group (n = 18) comprised subjects who participated for 6 years during adolescence in high-impact sports and in medium- or high-impact sports in adulthood. Subjects who participated for 6 years during adolescence in high-impact sports but during adulthood in low- or nonimpact sports or did not participate in any sports formed the HN group (n = 15). Subjects who participated during adolescence and adulthood in only nonimpact sports or who did not participate in any sports were considered the NN group (n = 14).
Ideally, subjects who participated in only nonimpact sports or who did not participate in any sports during adolescence and participated in high-impact sports during adulthood should have formed a fourth group. Unfortunately, subjects who met these criteria were not included in our sample. This finding was not surprising, since previous studies have demonstrated that subjects not involved in sports activities during adolescence hardly participate in sports during adulthood (56).
Dietary behavior and smoking habits
Dietary information was derived from a 3-day (2 weekdays and 1 weekend day) food record at age 40 years. These dietary records were reviewed by one research dietitian. In this paper, information about only calcium and alcohol consumption is given.
Information about smoking habits was obtained by questionnaire. Those who smoked daily and subjects who had recently quit (less than 1 year ago) were considered smokers. Subjects who had never smoked and quitters (more than 1 year ago) were considered nonsmokers.
Statistical analysis
For the first part of this study, descriptive statistics for the anthropometric characteristics, impact scores, time spent participating in sports, and BMD were calculated for the 154 subjects. Pearson and Spearman correlation coefficients were calculated between BMD on the one hand and the anthropometric and sports variables on the other. Full-model regression analyses were performed with BMD as the dependent variable and body mass, impact scores during adolescence and during adulthood, and time spent participating in sports during adolescence and during adulthood as independent variables. We decided to use body mass and not body mass index as an independent variable because 1) higher correlation coefficients were found between BMD and body mass than between BMD and body mass index, and 2) impact experienced by the bones during sports activities is related to body mass.
In the second part of this study, the three groups with different impact loading histories (HH, HN, and NN) were contrasted. Descriptive statistics for the anthropometric characteristics, time spent participating in sports, nutrition, metacarpal II bone variables, and BMD were calculated for the three groups.
Analyses of variance were executed to detect differences between the three groups for the bone dimensions. Because body mass is an important determinant of BMD and because the amount of time that the subjects spent participating in sports differed between the groups, analyses of covariance were conducted by using body mass, Minutes Sport Participation per week during adolescence, and Minutes Sport Participation per week during adulthood as covariates. Doing so enabled us to detect the influence of high-impact sports on BMD by taking into account the influence of body mass and of time spent participating in sports activities.
For all statistical analyses, the SAS software package was used (version 6.12; SAS Institute, Inc., Cary, North Carolina).
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RESULTS |
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The covariance analyses for total body BMD and lumbar spine BMD with weight, Minutes Sport Participation per week during adolescence, or Minutes Sport Participation per week during adulthood as covariates confirmed the results found in the analyses of variance. After adjustment for the three covariates, results just failed to reach significance; however, when each covariate was included separately, the groups differed significantly. Thus, even after we accounted for the covariates, impact during sports participation was a significant factor and resulted in significant differences between the HH group and the HN and NN groups for lumbar spine BMD (table 4).
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DISCUSSION |
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The regression analysis (N = 154) revealed that body mass during adulthood and impact score during adulthood were significant predictors of total body BMD and of lumbar spine BMD (table 2). No other variables were significant predictors. These results indicate that type of sports participation is more important than time spent participating in sports. Body mass and impact during adulthood and not during adolescence were significant predictors of bone mass. However, since these parameters are significantly related, the results do not indicate that body mass and impact during adolescence would not influence bone mass at age 40 years (lumbar spine BMD body mass during adolescence: r = 0.30, p = 0.0002; lumbar spine BMD impact during adolescence: r = 0.15, p = 0.06).
Analysis of variance (n = 47) revealed significant differences for lumbar spine BMD between the HH (1.12 g/cm2) group and the HN (1.01 g/cm2) and NN (0.99 g/cm2) groups (F = 5.07, p = 0.01). The differences for lumbar spine BMD between the groups were of the magnitude of one standard deviation, that is, an effect size of 1, which is of biologic importance. In addition, it has previously been shown that above a spinal BMD of about 1 g/cm2 (measured by dual photon absorptiometry), vertebral fractures are rare. These fractures become increasingly common as vertebral bone mass declines below this density (58). The observed differences remained significant even after controlling for weight or time spent participating in sports activities during adolescence or during adulthood. Comparison with a fourth group comprising subjects who were not involved in sports or were involved only in nonimpact sports during adolescence and who participated in high-impact sports during adulthood would have been very interesting. However, since it has been shown that very few people exhibit this pattern of sports participation (56), an experimental study should be conducted to examine the effect of high-impact sports during adulthood. Nonetheless, conclusions would have only theoretical value because, in general, very few people demonstrate this pattern of sports participation in normal life.
The results of this study can be explained in two ways. First, it is possible that the two groups involved in impact sports during adolescence gained BMD at the lumbar spine because of this sports participation. Sustained participation by the HH group could have maintained this gain or decelerated bone loss, whereas discontinuation of activity by the HN group could have resulted in bone loss. Because peak bone mass is achieved at approximately age 2530 years (5) and thereafter bone is lost at a rate of about 0.51 percent per year at most bony sites (59), it is possible that this loss was responsible for the differences observed between the HH group and the HN and NN groups. No significant differences were found between the HN group and the NN group. It is clear that impact only during adolescence did not result in a better bone status at age 40 years. Second, another explanation could be that participating in high-impact sports during adolescence did not result in bone gain but continued participation in impact sports during adulthood resulted in maintaining BMD or decelerating bone loss at the lumbar spine. Because the spines of the subjects in the HN group and the NN group were not subjected to high strain during adulthood, bone mineral could have been lost.
Regarding the results from former studies of athletes, it is not very plausible that participation in high-impact sports for 6 years did not result in bone gain. Therefore, the first explanation is most likely more correct. Nordstrom et al. (14) found, in a study of adolescent boys, that being involved in badminton and ice hockey resulted in higher bone mass at the weight-bearing sites. McCulloch et al. (12) found comparable results for adolescent soccer athletes. Pettersson et al. (60) concluded that high-impact activity in adolescent females resulted in higher BMD values at the loaded sites.
Population-based retrospective studies and longitudinal studies have shown the importance of physical activity during growth to maximize peak bone mass at the lumbar spine (37, 46, 47). Retrospective studies of athletes resulted in contrasting findings. Khan et al. (36) and Duppe et al. (38) found, for retired ballet dancers and former football players, respectively, a relation between sports participation during childhood or adolescence and bone mass at the femur but not at the lumbar spine at older ages. On the contrary, Kirchner et al. (40) and Bass et al. (16) concluded that past participation in gymnastics may have a residual effect on adult BMD. It is important to note that these studies differed in several respects. Not only were the subjects involved in different sports, but they also differed a great deal in age (Khan et al., mean age, 51 years; Duppe et al., ages 3485 years; Kirchner et al., ages 2945 years; Bass et al., ages 1835 years). As in the study by Karlsson et al. (39) in which differences in bone mass were found only between former weight lifters younger than age 65 years and controls, it is possible that after quitting sports participation for a long period of time, the bone mass gained because of the physical activity is no longer maintained. These authors concluded that a high level of physical activity has to be continued throughout life to maintain bone mass.
In the study by Hara et al. (42), the importance of physical activity during different age periods (at ages 1315 years, at ages 1618 years, and during adulthood) was investigated. These authors concluded that subjects who participated in high-impact sports during each period had significantly higher current total body BMD and lumbar spine BMD even after the authors controlled for hours per week and types of exercise during other periods. Groothausen et al. (45), on the contrary, concluded that if strain due to physical activity occurred only during the teenage period, the influence of peak strain on lumbar spine BMD at age 27 years was not of great importance.
The present study had some limitations. Mainly, the BMD measurements were not longitudinal. No such measurements were made at the start of the study. It is possible that there was a natural selection when the study began. The boys in the high-impact group were perhaps more strongly built and therefore had a higher BMD at the beginning, which still could have been evident at age 40 years. However, the fact that the metacarpal II bone variables at age 13 years did not differ between the three groups provides some indication that no baseline differences existed. Another concern is the generalizability of the results. As mentioned in a former study (61), the subjects in this study were a subsample of the 588 boys followed longitudinally over 6 years (51). The somatic, motor, and sociocultural characteristics of this subsample did not differ significantly from the total Flemish sample at 18 years of age. Thus, it is assumed that they were representative of the sample of boys followed longitudinally through adolescence (62). Moreover, the BMD of the subjects in the present study was comparable with BMD values for men of the same age reported by other studies (6365). Since the femoral neck is also an important fracture site, this measure should be incorporated in future studies.
Based on the regression analysis and the differences found between the HH group on the one hand and the HN and NN groups on the other, it can be concluded that continued participation in high-impact sports during adulthood is necessary to maintain BMD or at least slow down the loss. The influence of participation in high-impact sports during the growing years on skeletal healthas measured by DXA and expressed as BMDin adulthood is still a matter of discussion. To resolve this question, longitudinal BMD data are required.
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ACKNOWLEDGMENTS |
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The authors thank the staff of the University Hospital Department of Rheumatology (Leuven) for the DXA measurements.
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NOTES |
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REFERENCES |
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