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Original Studies |
Paavo Nurmi Center, Sport and Exercise Medicine Unit, Department of Physiology, University of Turku (M.L.-V.); Department of Medicine (M.L.-V., T.M., I.N., J.V.) and Central Laboratory (K.I., A.L.), Turku University Central Hospital, Turku, Finland
Address all correspondence and requests for reprints to: Dr. Timo Möttönen, Department of Medicine of Turku University Central Hospital, Paimio Hospital, 21540 Paimio, Finland. E-mail: timo.mottonen{at}tyks.fi
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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The 1-yr increase in BMD (adjusted for age, height, Tanner stage, BMD at baseline, and increases in height and weight) of the femoral neck was 0.037 g/cm2·yr [95% confidence interval (CI), 0.019–0.051 g/cm2·yr), and that of the greater trochanter was 0.020 g/cm2·yr (95% CI, 0.003–0.039 g/cm2·yr) greater in gymnasts than in controls. The corresponding figures for gymnasts compared with runners were 0.038 g/cm2·yr (95% CI, 0.009–0.041 g/cm2·yr) and 0.033 g/cm2·yr (95% CI, 0.006 to 0.043 g/cm2·yr). The figures for the lumbar spine did not differ significantly between study groups.
The baseline serum concentrations of formation markers and resorption marker accounted for 2.3–12.8% (P < 0.05) of the variation in the 1-yr increase in BMD at the femoral neck and lumbar spine. However, there was no significant difference between the levels of adjusted baseline bone turnover markers of the gymnasts, runners, and controls.
The present data add considerable support to the argument that high impact mechanical loading is extremely important and beneficial for the acquisition of BMD of the hip during peripubertal years. Our results indicate also that a high rate of bone turnover, reflected as elevated bone markers, is only weakly associated with the 1-yr bone gain in peripubertal girls.
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Although genetic factors may be the main determinants of bone mass and BMD, environmental factors also influence the quality and durability of bone. Several cross-sectional studies have shown that high impact weight-bearing activity is beneficial for the load-bearing sites of the skeleton (2, 3, 4, 5, 6). There are few longitudinal data on the relationship between physical activity and bone mineral acquisition in prepubertal and pubertal girls (7, 8, 9, 10, 11).
Several biochemical markers of bone formation and bone resorption have been introduced. Osteocalcin (OC) is the major noncollagenous protein of bone matrix. OC is synthesized by osteoblasts in the bone, partly incorporated into the bone matrix, and partly delivered to the circulatory system. The bone-derived alkaline phosphatase (BAP) is an enzyme localized to the membrane of osteoblasts, and it is released into the circulation. Collagen type I is the most common protein of bone matrix, accounting for more than 90% of the total mass of protein. The amino-terminal propeptide of type I procollagen (PINP) is present in the circulation before the collagen molecules are assembled into fibers (12). Type I collagen peptides are present in the mature form of collagen. In the process of bone degradation, C-terminal telopeptide of type I collagen (CTX) is released into the circulation (13).
Puberty is a time of large increases in bone mass over a relatively brief period. In females, the time of maximum bone acquisition occurs between 11–14 yr of age, a time that corresponds to pubertal stages Tanner 3–5 (14, 15). Careful evaluation of the factors associated with the increase in bone mass during this phase may be important for prevention of osteoporosis later in life.
There has been little research on the association between biochemical markers of bone formation and resorption, and physical activity, especially in children and young adults (16, 17, 18, 19, 20). Furthermore, little is known about the effects of various loading states on the formation and resorption of bone tissue or osteoblast-osteoclast activity in the growing skeleton. The aim of the present study was to evaluate the influence of physical activity on acquisition of bone mass during 1 yr with regard to biochemical markers of bone and type I collagen metabolism among peripubertal girls.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The original study group comprised 191 healthy Caucasian girls, aged 9–15 yr (66 competing gymnasts, 65 competing runners, and 60 nonathletic controls), who participated in a long-term health study. The participants were recruited from local sports clubs and schools in the city of Turku and its vicinity. Gymnasts, runners, and controls were studied to determine the difference in the impact of physical activity on the growing skeleton. Gymnastics is characterized by very high impact through repeated jumps and body contact with hard surfaces. Running, on the other hand, causes repetitive weight-bearing stress and impact loading mainly on the lower limbs. The intensity of the exercise was defined as competitive if the subject had participated regularly in competitive sports at a local, provincial, or national level for at least 1 yr. The group of the runners consisted of long distance runners and track runners. The controls were usually classmates of the athletes. Subjects in the control group did not participate in any kind of regular or organized sports activity. All participants were healthy, as assessed clinically and by questionnaire. All subjects were studied over an 8-week period from February to March 1997 and 1998.
The study protocol was approved by the joint ethics committee of Turku University and Turku University Central Hospital. The study was carried out in accordance with the Declaration of Helsinki. Written informed consent was obtained from all participants and their parents.
Anthropometry
Weight and height were recorded with subjects in minimal clothing and bare feet. Height was measured with a fixed stadiometer (Harpenden stadiometer, Holtain, Crymych, UK), and weight was measured with a regularly calibrated electronic scale (EKS Exclusive, EKS International, Sweden). The body mass index was calculated (kilograms per m2).
Bone mineral density (BMD) measurements
The BMD (grams per cm2) and the projected bone area (square centimeters) of the nondominant hip and the lumbar spine (L2–L4) were measured by dual energy x-ray absorptiometry (QDR 4500C, Hologic, Inc., Waltham, MA). All measurements were performed and analyzed by the same 3 trained radiographers. Calibration was performed daily to assure quality, using a spine phantom supplied by the manufacturer. The coefficients of variation of two consecutive measurements for 10 girls were 1.3% for the spine, 0.8% for the hip, and 0.4% for the phantom over the study period.
Assessment of puberty stage
The Tanner stage was examined and recorded by the researcher (M.L.-V.) according to the method of Tanner (21). When there were discrepancies between breast stage and pubic hair stage, greater emphasis was placed on the degree of breast development. The prepuberty group consisted of Tanner stage 1, the early puberty group consisted of Tanner stages 2–3, and the late puberty group consisted of Tanner stages 4–5.
Assessment of physical activity
The subjects completed a detailed questionnaire on their physical activity every 6 months. The competitive athletic history of the subjects and their leisure time physical activity (LTPA) during the past 6 months (weekly frequency, mean duration in minutes, and mean intensity of all bouts of physical activity) were reported retrospectively. On the basis of this information the LTPA was calculated as MET-hours per week by multiplying frequency, mean duration in minutes, and mean intensity of weekly physical activity and then dividing by 60 (22). The mean LTPA of 1 yr was calculated. The number of years of training of the athletes was also recorded.
Laboratory studies
All blood samples were obtained from the participants between 0800–0900 h after an overnight fast. The puncture site was anesthetized by local anesthetic patches (Emla, Astra USA, Inc., Sodertalje, Sweden). In menstruating subjects samples were collected during the early follicular phase of the menstrual cycle, defined as the time between the fifth and eighth days after the onset of menstrual bleeding. Blood samples were centrifuged (2100 x g, 10 min) within 2 h of venipuncture, and serum samples were stored frozen at -20 C.
Serum OC (S-OC) was measured by RIA (CIS-Bio International, Gif-sur-Yvette, France). The intra- and interassay coefficients of variation were 1.7% and 3.1% at 22 ng/mL, respectively. Serum BAP (S-BAP) was measured by immunoassay (Metra Biosystems, Mountain View, CA), and the respective intra- and interassay coefficients of variation were 2.1% and 3.2% at 70 U/L, respectively. The serum concentration of PINP (S-PINP) was measured by RIA (Orion Diagnostica, Espoo, Finland), with intra- and interassay coefficients of variation of 5.2% and 2.0% at 106 µg/L, respectively. Serum CTX (S-CTX) was measured by enzyme immunological test (Osteometer Biotech, Herlev, Denmark), and the intra- and interassay coefficients of variation were 10.3% and 4.9% at 7387 pmol/L, respectively.
Statistical analyses
Spearman’s correlation analyses, one-way ANOVAs, multivariate and regression analyses, Bonferroni tests, and nonparametric analyses were performed using version 6.12 of the SAS software (SAS Institute, Inc., Cary, NC). The normality of the variable distributions was tested using Shapiro-Wilk statistics and normality plots. The differences between exercise groups in baseline values were evaluated with one-way ANOVA followed by pairwise Bonferroni tests. In case of non-Gaussian distributions the Kruskal-Wallis test was used, followed by pairwise Wilcoxon analyses with Bonferroni correction. The homogeneity of slopes was assessed by studying the cross-product of Tanner stage and the independent bone formation or resorption marker with main effects in the model. The 1-yr changes in BMD of the femoral neck, greater trochanter, and lumbar spine were calculated to match the exact follow-up period. Multivariate analyses were applied in the adjustments of bone formation and resorption markers and 1-yr increases in BMD and in the assessment of the relationship between these markers and the 1-yr change in BMD.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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One hundred and ninety-one girls were originally evaluated. There
were 6 dropouts from the follow-up during the year, and, in addition,
30 retired from sports and were therefore excluded from the analysis.
After 1 yr of follow-up, 51 gymnasts and 50 runners who continued their
sports career and 54 controls were available (n = 155). The
absolute mean BMD values of the femoral neck, greater trochanter, and
lumbar spine by pubertal stages and study groups at baseline are
presented in Table 1
. The body weight of
the early pubertal gymnasts was significantly lower than that of the
runners, but there were no differences in stature in the late puberty
groups. Both athletic groups had significantly higher mean absolute BMD
of the femoral neck than the controls in the early pubertal subgroup.
The BMD of the femoral neck, greater trochanter, and lumbar spine of
the late pubertal gymnasts differed significantly from those in the
controls and the runners at baseline (Table 1). However, the projected
area of the lumbar spine was comparable in each study group of three
pubertal stages (data not shown).
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). The strongest correlations between
formation markers were found between S-OC and S-PINP (r =
0.539–0.893) and between S-BAP and S-PINP (r = 0.612–0.894). The
correlations between various bone markers were stronger in the late
pubertal group (r = 0.725–0.894) than in the earlier stages
(r = 0.175–0.628). Accordingly, significant differences
(P < 0.05) were noted in regression slopes between the
pubertal stages, and slopes were 1.2–2 times greater in late puberty
than in prepuberty or early puberty.
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Physical activity and 1-yr increases in BMD
The changes in BMD of the femoral neck, greater trochanter, and
lumbar spine over 1 yr among the different physical exercise groups are
illustrated in Fig. 1. Compared with the
controls, the 1-yr increase in BMD (adjusted for age, height, Tanner
stage, BMD at baseline, and 1-yr increases in height and weight) of the
femoral neck in the gymnasts was 0.037 g/cm2·yr
[95% confidence interval (CI), 0.019–0.051
g/cm2·yr], and that of the greater trochanter
was 0.020 g/cm2·yr (95% CI, 0.003–0.039
g/cm2·yr) higher. In contrast, the 1-yr
increase in the areas of the femoral neck and the lumbar spine did not
differ significantly between gymnasts and controls. The corresponding
figures compared to runners were 0.038 g/cm2·yr
(95% CI, 0.009–0.041 g/cm2·yr) and 0.033
g/cm2·yr (95% CI, 0.006–0.043
g/cm2·yr). The rates of change at the lumbar
spine did not differ significantly between the study groups.
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. The mean
rate of increase was high in the early pubertal subjects
(5.9–13.5%/yr) and then decreased in the late pubertal participants
(1.8–6.0%). The mean percent increase in the BMD of the femoral neck
was significantly greater in the prepubertal and late pubertal gymnasts
than in the runners or controls (Table 3).
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The baseline serum concentrations of OC and PINP correlated significantly with the adjusted 1-yr changes in BMD of the femoral neck and the lumbar spine (r = 0.280–0.478), but none of the biochemical markers correlated with the adjusted 1-yr change in BMD of the greater trochanter among late pubertal group.
The baseline serum formation markers accounted for 5.0–6.9% (P < 0.001) of the variation in the 1-yr increase of BMD at the femoral neck in multivariate analyses. The corresponding figures were 7.3–12.8% (P < 0.001) at the lumbar spine. In contrast, the serum resorption marker CTX accounted for only 2.3% (P < 0.05) of the variation in the 1-yr increase in BMD at the femoral neck and only 4.9% (P < 0.001) at the lumbar spine.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The influence of exercise on the femoral neck was more evident than that on the lumbar spine in both the longitudinal and cross-sectional data of our study. The 1-yr increases in adjusted BMD at the femoral neck and greater trochanter of the gymnasts were 115% and 49% larger than those of the controls; at the lumbar spine there was only a tendency toward higher BMD values in the gymnasts. In a very recent study McKay et al. (11) reported that an 8-month school-based jumping program augmented BMD at the greater trochanter, but not at the lumbar spine, in prepubertal and early pubertal children (11). In an earlier study Bass et al. reported that growth is region specific; the growth spurt was more evident at the spine than at the lower limbs during puberty. The growth of the lower limbs was more rapid than that of the trunk before puberty (23). Although the cross-sectional data regarding late pubertal gymnasts showed significantly higher BMD values of the lumbar spine than in the controls or the runners, a follow-up of only 1 yr was too short to observe any significant difference in the increase in BMD of the lumbar spine. The BMD of the lumbar spine, however, is more sensitive to the negative effect of hormonal disturbances, which are common in athletes (5, 24). In our baseline data the runners had a tendency toward higher BMD values of the femoral neck and lumbar spine than the controls, whereas the 1-yr increases in BMD were similar in the two groups. However, we did not find any negative effect of running on BMD as has been described previously in college-aged women (5, 25).
The influence of physical activity on the BMD of children has been explored in a few follow-up studies (7, 8, 9, 10, 11, 20, 26). In general, the studies have concentrated on prepubertal subjects. We chose a more extensive age span that allowed us to study the effect of sexual maturation, and therefore we adjusted analyses for the Tanner stage. Our results are in agreement with those reported by Bass et al., whose 12-month follow-up study showed an increase in BMD of the total body, lumbar spine, and legs that was 30–85% greater in gymnasts than in controls in a population of prepubertal girls (9). However, in a recent cross-sectional study, Haapasalo et al. found that the benefit of physical activity became evident during the growth spurt or Tanner stage III–IV (27). Bailey et al. (10) reported that the increase in total body bone mineral content reached its peak velocity in girls at the age of 12.5 yr (10). According to our results the mean 1-yr increase in BMD was highest (5.9–13.5%) in early pubertal girls.
In our prepubertal group the average number of training years was 5.4 for gymnasts and 3.2 for runners, and the amount of exercise was far above moderate, particularly in the group of gymnasts. Prospective studies of prepubertal children have shown that a 10- to 30-min exercise session three times per week for less than 1 yr increased BMD significantly (8, 11, 26).
In the present study the baseline projected bone area and annual increase in that bone area at the femoral neck and lumbar spine were comparable in gymnasts and controls. This fact did not explain the higher BMD values in the gymnasts than in the controls. In contrast to our results, Morris et al. reported that exercise also significantly increased the projected bone area of the femoral neck in prepubertal girls (8). Our results are in line with those reported by Nordström et al. (28), who found that exercise affected primarily the BMD and not the bone area of adolescent boys.
According to our results there were significant correlations in the serum concentrations of bone formation markers (OC, BAP, and PINP) and a bone resorption marker (CTX), which were associated with the positive response to the annual change in BMD, particularly at the lumbar spine and partly at the femoral neck of the growing skeleton. Our results stand in contrast to previous results for older subjects, in which the concentrations of bone turnover markers did not predict changes in bone mass (17, 29). Our findings disagreed also with the study by Slemenda et al. (30), who reported that low concentrations of formation and resorption markers in children predicted high BMD values.
Puberty is associated with the high values of bone turnover markers (31, 32, 33). Mora et al. found that the concentrations of biochemical markers reach a zenith at pubertal stage 2 (32). Our findings for all measured formation markers were consistent with previous results (23, 31, 32, 33). All four bone turnover markers we studied correlated significantly with the 1-yr increase in BMD at the lumbar spine, and both OC and PINP also correlated with the increase in BMD at the femoral neck. Mora et al. (33) found in their cross-sectional study of 7- to 18-yr-old subjects that serum BAP and OC correlated inversely with the material density of bone, and markers of bone resorption were related to the volume of bone. Borderie et al. (34) found that the values of the biochemical markers correlated with the change in BMD at the lumbar spine, but not at the femoral neck. This might have been due to higher biological activity of trabecular bone than that of cortical bone; the lumbar spine consists mostly of trabecular bone (35). It is likely that estradiol is the primary ovarian steroid maintaining bone health, whereas in exercising women with luteal phase abnormalities, BMD and biochemical markers of bone turnover are unaffected (36). However, in recent studies there has been no significant difference in bone turnover markers among amenorrheic and eumenorrheic athletes and controls (24, 37). In pubertal children there is a significant negative correlation between the serum concentration of estrogen and bone turnover markers (23, 31).
Biochemical markers of bone turnover have large diurnal and seasonal variation (38, 39, 40). Therefore, the sampling time is crucial for the interpretation of the results, and understandably the single measurements may be misleading. In the present study the samples were collected at the same time of the morning and at the same early follicular phase of the menstrual cycle. To avoid seasonal variation we used only samples collected in the winter.
The effect of physical activity on bone turnover markers in the growing skeleton has been poorly studied. Bass et al. reported that prepubertal gymnasts had significantly lower serum concentrations of OC and BAP than did sedentary controls (9). In our opinion this may have been due to delayed growth in regard to strenuous exercise. Our results for peripubertal girls are in line with the recent study by Nickols-Richardson et al. (20), who did not find differences in turnover markers between female gymnasts and controls aged 8–13 yr. Instead, short exercise trials have been shown to increase serum concentrations of formation markers, particularly OC (16, 19, 41). There have been several attempts to evaluate the influence of exercise on the bone turnover of adult athletes, but the results have remained conflicting (18, 42, 43, 44).
The present study is particularly important because it examines and establishes certain effects of common physical activities on health in adolescent girls. Our results confirm that participation in physical exercise remarkably affects BMD. Cross-sectional comparisons cannot establish a causal relationship between exercise and bone density, because self-selection may confound athlete-control studies. Thus, this 1-yr follow-up study is especially valuable; peripubertal female gymnasts have greater increases in BMD of both the femoral neck and the greater trochanter than runners or controls. This adds considerable support to the argument that high impact mechanical loading is indeed responsible for the differences in BMD, not selection bias. The biochemical markers reflect the status of overall skeletal health and not of a particular site as does dual energy x-ray absorptiometry. High bone turnover is associated with the high annual bone gain in peripubertal girls. High impact mechanical loading during the peripubertal years is apparently extremely important and beneficial, particularly for the acquisition of BMD of the femoral neck. An important question remains: are osteoporotic fractures in senescence reduced by increasing the magnitude of high impact exercise during peripubertal years? Therefore, it is important to conduct long-term follow-up studies to explain whether the beneficial effect of physical activity on bone accumulation is sustained.
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Footnotes |
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Received March 13, 2000.
Revised July 5, 2000.
Accepted July 11, 2000.
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References |
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BMD) (%) at the
femoral neck (FN), greater trochanter (Troch), and lumbar spine (L2–4)
in the prepubertal, early pubertal, and late pubertal gymnasts,
runners, and controls.