Long-term leisure-time physical activity has a positive effect on bone mass gain in girls

Abstract

The purpose of this 7-year prospective longitudinal study was to examine whether the level and consistency of leisure-time physical activity (LTPA) during adolescence affected the bone mineral content (BMC) and bone mineral density (BMD) attained at early adulthood. The study subjects were 202 Finnish girls who were 10 to 13 years of age at baseline. Bone area (BA), BMC, and BMD of the total body (TB), total femur (TF), and lumbar spine (L₂–L₄) were assessed by dual-energy X-ray absorptiometry (DXA). Scores of LTPA were obtained by questionnaire. Girls were divided into four groups: consistently low physical activity (G_LL), consistently high (G_HH), and changed from low to high (G_LH) and from high to low (G_HL) during 7 years of follow-up. At baseline, no differences were found in BA, BMC, and BMD among the groups in any of the bone sites. Compared with the G_LL group, the G_HH group had higher BMC (11.7% in the TF, p < .05) and BMD at the TB (4.5%) and the TF (12.2%, all p < .05) at age 18. Those in the G_LH group also had higher a BMC at each site (8.5% to 9.4%, p < .05) and a higher BMD in the TB (5.4%) and the TF (8.9%) than that of G_LL (all p < 0.05) at the age 18. Our results suggest that long-term leisure-time physical activity has a positive effect on bone mass gain of multiple bone sites in girls during the transition from prepuberty to early adulthood. In addition, girls whose physical activity increases during adolescence also benefit from bone mass gain. © 2010 American Society for Bone and Mineral Research

Introduction

The development of bone mass in childhood and its influence in later life are well described by several authors,1–7 and they are considered to be an area of primary importance for the prevention of osteoporosis and fracture. Cross-sectional studies have shown that about 35% of total-body and lumbar spine bone mineral content (BMC) and over 27% of femoral neck BMC are laid down during the 4 years surrounding peak height velocity (PHV).8 There is evidence that leisure-time physical activity (LTPA) has beneficial effects on bone mass accrual during childhood.9–12 Regular physical activity during the first decades of life could be one important factor affecting bone gain, but long-term studies are needed to confirm whether the benefits achieved during childhood persist into adulthood and later life.

The type and duration of physical activity have an important effect on bone development.13 Furthermore, the intensity of exercise also has an effect: weight-bearing physical activity and other activities that result in high bone strains are the most important for increasing the accrual of bone mineral density (BMD).14, 15 Valdimarsson and colleagues16 studied female soccer players with 8-years of follow-up and found that intense exercise after puberty was associated with higher BMD accrual and that decreased physical activity in both the short and long term was associated with higher BMD loss than in controls. Some longitudinal studies also indicated that moderately intense training was sufficient to increase the accrual of bone mineral in a young population.9, 17, 18 MacKelvie and colleagues9, 18 reported that only weight-bearing exercise interventions in school programs had significant effects on bone mass gain. A daily school-based exercise intervention of 40 minutes per school day was beneficial for spinal BMD and BMC in boys aged 7 to 9 years.19

Persistent participation in LTPA is a challenge if a child does not take part in communally organized sports throughout the year. It is important to know if, during puberty and the adolescent period, an increase or decrease in the level of physical activity would result in differences in bone accrual. Thus the purpose of this 7-year prospective longitudinal study was to evaluate (1) whether girls with consistently high LTPA from prepuberty through early adulthood experience benefits in terms of bone mass accrued by early adulthood and (2) whether increasing in level of LTPA from low to high from prepuberty throughout adolescence has beneficial effects on bone mass by early adulthood.

Materials and Methods

Study participants

Recruitment of the study population is presented schematically in Fig. 1. The subjects were first contacted via class teachers in grades 4 to 6 (age 9 to 13 years) in 61 schools in the city of Jyväskylä and its surroundings in central Finland (96% of all the schools in these areas). Briefly, of those eligible, 396 girls participated in the laboratory tests 1 to 8 times over a maximum period of 8 years (mean duration of total follow-up was 7.5 years, and mean age at last follow-up was 18.3 years). Of the 396 girls, 258 participated in a calcium and vitamin D intervention trial during the first 2 years,20 and 235 participated in the 7-year follow-up assessments.21 Of these, 101 girls were from the intervention group and 134 from the nonintervention group. Owing to missing physical activity questionnaires, 33 subjects (15 from the intervention group and 18 from the nonintervention group) were excluded from the final analysis; therefore, 202 girls were included in the final analysis. No intervention effects on bone mass were found; thus data were pooled in the present analysis.21, 22 The study protocol was approved by the Ethics Committee of the University of Jyväskylä, the Central Finland Health Care District, and the Finnish National Agency of Medicine. An informed consent was provided by all subjects and their parents prior to the assessments.

Figure 1. Study population flow. The subjects were recruited from the fourth to sixth grades (ages 9 to 13 years) in 61 schools in the city of Jyväskylä and its surroundings in central Finland (96% of all schools in these areas).

Physical activity assessment

LTPA level was evaluated using a self-administrated physical activity questionnaire that was a modified version of a validated questionnaire used in a previous World Health Organization (WHO) study.23, 24 The modification consisted of two additional questions asking about the frequency and duration of physical exercise. Specifically, the questionnaire asked the girls what were the first, second, and third most common sports they participated in; the duration of exercise in each session; and the number of sessions each week. The intensity of each activity was calculated on the basis of the energy expenditure per minute.25 Bone loading was based on whether the activity was weight-bearing or not. We constructed a formula to calculate the LTPA score:

• 

where frequency = times per week, 1–3 = the three physical activities, intensity index = MET (metabolic equivalent of physical activity) value according to body mass, duration = hours per session, loading = weight bearing, where non–weight bearing = 1 and weight bearing = 2. Finally, 202 girls with valid LTPA scores were included in the final analysis.

To test whether consistency or change of physical activity level during adolescence had significant effects on bone gain, girls were divided first into two groups according to the median values of their LTPA scores at screening and at the 7-year follow-up visit. Four activity groups then were formed as follows: consistently high (G_HH = 50), consistently low (G_LL = 53), and changed from high to low (G_HL = 48) or low to high (G_LH = 51).

To test whether the differences already existed at baseline, a subgroup was formed consisting of girls who had valid LTPA scores and bone assessments both at baseline and follow-up (G_HH: n = 26; G_LL: n = 31; G_HL: n = 12; G_LH: n = 16). Physical inactivity (PIA) was calculated as the sum of sitting and lying hours per day.

Physical performance

Maximum isometric strength of the left knee extensors (KE) was measured with a dynamometer of isometric muscle strength measurements (Metitur, Jyväskylä, Finland). Lower limb explosive performance capacity was evaluated by using a vertical counter movement jump test. The test was performed on a contact platform to determine the flight time of the jump.

Anthropometric measurements

All measurements were performed after overnight fasting (12 hours). Participants were weighed with light clothes and without shoes. Height was determined using a fixed wall scale measuring device to the nearest 0.1 cm. Weight was determined within 0.1 kg for each subject using an electronic scale calibrated before each measurement session. Body mass index (BMI) was calculated as weight (kg) per height squared (m²).

DXA assessment

Dual-energy X-ray absorptiometry (DXA; Prodigy, GE Lunar Corp., Madison, WI, USA, with software Version 9.3) was used to estimate bone mineral content (BMC), bone mineral density (BMD), and bone area (BA) of the total body (TB), total femur (TF), and lumbar spine (L₂–L₄). The total-body fat mass (FM) and lean tissue mass (LM) were assessed. All metal items were removed from the participants to ensure the accuracy of the measurement. The subjects were positioned in the center of the table for each scan. They were scanned using the default scan mode automatically selected by the Prodigy software. Precision of the repeated measurements expressed as the percent coefficient of variation (CV%) ranged from 0.6% to 1.2% for BMC, from 0.9% to 1.3% for BMD, and from 0.6% to 1.2% for BA of the whole body, total femur, and L₂–L₄.

pQCT assessment

A peripheral quantitative computed tomography (pQCT) device (XCT-2000, Stratec Medizintechnik, GmbH, Pforzheim, Germany) was used to scan left tibia.26, 27 A 2-mm-thick single tomographic slice was scanned with a voxel size of 0.59 mm. The left tibial shaft was scanned in the transverse plane using the manufacturer's research mode at a site 60% of the way up the tibia, based on a measurement of the lower leg length between the lateral knee joint line and the lateral malleolus. The lower leg length was measured when the subject was in a sitting position with the knee angled at 90 degrees. The distal radius was scanned at 4% of forearm length proximal to its wrist joint surface. Forearm length was measured as the distance between the ulnar styloid process and the olecranon with the elbow at 90 degrees and the forearm neutrally rotated. In addition, at 7-year follow-up, the middle shaft of the radius at 30% of forearm length proximal to the wrist joint surface was scanned. Total cross-sectional area (CSA, mm²), BMC (mg/mm), volumetric bone mineral density (vBMD, mg × cm⁻³), and cortical CSA (cCSA), cortical BMC (cBMC), cortical vBMD (cvBMD), and cortical thickness (C.Th, mm) were analyzed using the manufacturer's software package (Version 5.40) and Geanie 2.1 (Commit, Ltd., Espoo, Finland). The CV% was 1% for the CSA and less than 1% for BMC, vBMD, and C.Th.

QUS assessment

Calcaneal broadband ultrasound attenuation (BUA) of the left calcaneus was measured using a gel-coupled scanning quantitative ultrasonometer (QUS-2, Quidel Corporation, San Diego, CA, USA). QUS-2 uses point-source transducers (16 mm in diameter) with wide transmission and acceptance angles and a hemispherical contact surface.28 The short-term reproducibility with repositioning (determined on the same day by a single technician) expressed as CV% was less than 1.2%.

Statistical analysis

Data were checked for normality by Shapiro-Wilk's W test and for homogeneity by Levene's test before each analysis. Descriptive results are reported as means ± SD. Analysis of covariance with height at 7-year follow-up and Tukey post hoc tests were used to test the differences in bone variables among the LTPA groups. Analysis of variance with Tukey post hoc test or Kruskal-Wallis ANOVA with Mann-Whitney test was used to test the differences in anthropometric variables at the 7-year follow-up and in bone variables at age 11 among the LTPA groups. Statistica for Windows Version 8.0 software (StatSoft, Inc., Tulsa, OK, USA) was used to perform the statistical analyses. A p value of less than 0.05 was considered statistically significant.

Results

The physical characteristics of the girls at age 18 according to consistency of LTPA during puberty are presented in Table 1. At the end of the 84-month follow-up, there were no differences in age, body height, body weight, BMI, fat mass, bone mass, age at menarche, physical inactivity, and calcium intake among the LTPA groups. Also, 12.4% of the girls were overweight or obese according to the criteria of Cole and colleagues29 and the WHO.30 The G_HH group had a significantly higher amount of lean mass than the G_HL group (p = .012) and the G_LL group (p = .004), and the G_LH group had more lean mass than the G_HL group (p < .001) and the G_LL group (p < .001). The G_HL group had significantly smaller maximal force in knee extension than the G_HH group (p = .018) and the G_LH group (p = .009), whereas the G_HH group had better results in jumping height than the G_HL group (p = .022) and the G_LL group (p = .044). The groups differed significantly in LTPA scores, but not in PIA hours, respectively. The scores of the G_LL group stayed at a consistently low level (24.2 and 19.3) during the 7 years. The G_LH group increased its LTPA scores from 31.4 to 137.1, and the G_HL group decreased its scores from 139.2 to 22.0. The LTPA scores of G_HH group stayed at a consistently high level between the ages of 11 and 18 years (133.4 and 123.4). The most common summer LTPAs undertaken by girls (ie, the activities listed in first place) were swimming (38%), cycling (26%), and horseback riding (13%) at age 11 and cycling (35%), walking (21%), and jogging (11%) at age 18. The amount of weight-bearing exercise increased for those in the G_HH, G_LH, and and G_HL groups (p < .001, respectively, by χ² test). The G_LL group also increased its amount of weight-bearing exercise at follow-up (p < .001 by χ² test) but still had a preponderance of nonloading physical activities (63%).

Table 1. Physical Characteristics of the Girls at 84-Month Follow-up According to Consistency of LTPA During Puberty

	High-high (n = 50)	High-low (n = 48)	Low-high (n = 51)	Low-low (n = 53)	ANOVA p	Post hoc
						HH-HL	HH-LH	HH-LL	HL-LH	HL-LL	LH-LL
Values are given as mean ± SD. PIA = physical inactivity; KE = knee extension.
Age (years)	18.3 ± 1.1	18.3 ± 1.3	18.3 ± 1.1	18.5 ± 1.0	.493	N.S.
Height (cm)	166 ± 5.5	165 ± 4.9	167 ± 6.1	165 ± 6.1	.051	N.S.
Weight (kg)	60.0 ± 8.9	59.3 ± 9.5	61.4 ± 9.1	58.0 ± 8.5	.222	N.S.
BMI (kg × m^−1)	21.7 ± 2.9	21.9 ± 3.2	21.9 ± 2.6	21.3 ± 2.6	.804	N.S.
Fat mass (kg)	18.4 ± 7.4	19.6 ± 7.0	18.7 ± 6.8	18.8 ± 5.9	.659	N.S.
Lean mass (kg)	39.0 ± 3.3	36.7 ± 4.2	39.8 ± 3.9	36.4 ± 3.6	<.001	.012		.004	<.001		<.001
Bone Mass (kg)	2.5 ± 0.4	2.5 ± 0.4	2.5 ± 0.4	2.3 ± 0.4	.051	N.S.
Menarche age (years)	13.1 ± 1.2	12.8 ± 1.1	13.0 ± 1.3	12.9 ± 1.3	.534	N.S.
Maximum force KE (Nm)	404 ± 86.1	351 ± 93.1	408 ± 85.4	383 ± 87.9	<.01	.018			.009
Jumping height (cm)	23.9 ± 5.2	21.0 ± 4.0	23.4 ± 5.7	21.3 ± 3.6	<.01	.022		.044
LTPA score	123 ± 66.9	22.0 ± 13.0	137 ± 102.1	19.3 ± 13.7	<.001	<.001		<.001	<.001		<.001
PIA (h/day)	17.6 ± 3.0	17.8 ± 2.6	17.4 ± 2.9	18.1 ± 3.2	.587	N.S.
Total Ca (mg/day)	1340 ± 521	1191 ± 511	1484 ± 623	1189 ± 494	.378	N.S.

The G_HH and G_LH groups had higher values of BMC at TB, TF, and L₂–L₄ than the G_LL group (p < .05; Table 2) at age 18. The G_HL group had higher values of BMC than the G_LL group at L₂–L₄ (p < .05). All the results in Table 2 show that we had a 91% power to detect the differences between the groups for p < .05. The G_HH and G_LH groups had higher values of BMD at TB, TF, and L₂–L₄ than the G_LL group (p < .05), and the G_HL group had a higher BMD in the TB and L₂–L₄ than the G_LL group (p < .05; Table 2) at age 18. The percentage differences between the G_LL group and the other groups are given in Fig. 2. There were significant differences in BA at each bone site, but no differences in post hoc comparisons were found among the LTPA groups.

Table 2. Bone Properties of the Girls at 84-Month Follow-up According to Consistency of LTPA During Puberty

	High-high (n = 50)	High-low (n = 48)	Low-high (n = 51)	Low-low (n = 53)	ANCOVAap	Post hoc
						HH-HL	HH-LH	HH-LL	HL-LH	HL-LL	LH-LL
Values are given as original mean ± SD. a Covariate: body height at 7-year follow-up.
DXA:
Total body
BMC (kg)	2.51 ± 0.4	2.45 ± 0.4	2.53 ± 0.4	2.32 ± 0.4	<.001			.018			.002
BMD (g/cm^2)	1.17 ± 0.1	1.17 ± 0.1	1.18 ± 0.1	1.12 ± 0.1	<.001			.010		.01	.002
BA (cm^2)	2.14 ± 0.2	2.09 ± 0.2	2.15 ± 0.2	2.05 ± 0.2	<.001	N.S.
L2–L4
BMC (g)	50.6 ± 6.7	49.8 ± 7.9	50.2 ± 8.3	46.3 ± 7.7	<.001			.007		.017	.003
BMD (g/cm^2)	1.23 ± 0.1	1.22 ± 0.1	1.21 ± 0.1	1.16 ± 0.1	<.001			.020		.042	.044
BA (cm^2)	41.2 ± 3.3	40.9 ± 4.1	41.3 ± 4.3	39.8 ± 3.9	<.001	N.S.
Total femur
BMC (g)	33.4 ± 4.6	31.4 ± 3.8	32.8 ± 4.7	30.0 ± 4.9	<.001			.001			.005
BMD (g/cm^2)	1.11 ± 0.1	1.07 ± 0.1	1.10 ± 0.1	1.01 ± 0.1	<.001			<.001			.006
BA (cm^2)	30.0 ± 2.0	29.4 ± 1.9	29.8 ± 2.0	29.6 ± 2.3	<.001	N.S.
pQct:
Radius (distal)
BMC (mg/mm)	108 ± 13	107 ± 13	109 ± 12	101 ± 13	<.001			.015	.038		.004
vBMD (mg/cm^3)	347 ± 40	351 ± 40	338 ± 44	340 ± 44	.136	N.S.
CSA (mm^2)	315 ± 38	308 ± 40	327 ± 47	299 ± 36	<.001						.001
Radius (middle)
BMC (mg/mm)	94.9 ± 8.9	94.5 ± 10.6	97.7 ± 10.2	91.3 ± 11.4	<.001						.007
vBMD (mg/cm^3)	920 ± 62	939 ± 63	937 ± 58	938 ± 56	.448	N.S.
CSA (mm^2)	104 ± 13	101 ± 14	105 ± 13	98 ± 14	<.001	N.S.
cBMC (mg/mm)	84.4 ± 8.3	84.4 ± 9.5	87.7 ± 9.4	81.5 ± 10.3	<.001						.004
cvBMD (mg/cm^3)	1184 ± 22	1190 ± 10	1190 ± 20	1190 ± 18	.623	N.S.
cCSA (mm^2)	71.3 ± 7.0	71.0 ± 7.7	73.7 ± 7.8	68.6 ± 8.7	<.001						.003
C.Th (mm)	2.55 ± 0.2	2.59 ± 0.2	2.64 ± 0.2	2.54 ± 0.2	.001	N.S.
Tibial shaft
BMC (mg/mm)	367 ± 41	345 ± 40	364 ± 44	339 ± 41	<.001	.013		.001	.035		.004
vBMD (mg/cm^3)	754 ± 50	758 ± 44	766 ± 57	736 ± 52	.074
CSA (mm^2)	488 ± 57	456 ± 54	476 ± 58	462 ± 54	<.001	.004		.030
cBMC (mg/mm)	322 ± 38	304 ± 38	322 ± 42	296 ± 39	<.001	.042		.002	.029		.001
cvBMD (mg/cm^3)	1130 ± 22	1140 ± 21	1135 ± 20	1136 ± 20	.067	N.S.
cCSA (mm^2)	285 ± 34	266 ± 33	283 ± 37	260 ± 34	<.001	.010		.001	.014		.001
C.Th (mm)	4.43 ± 0.4	4.28 ± 0.4	4.49 ± 0.5	4.13 ± 0.5	.036			.004			<.002
QUS:
BUA (dB/mHz)	85.6 ± 10.1	82.0 ± 12.8	85.7 ± 12.8	80.5 ± 12.1	.013	N.S.

Figure 2. Comparison of the percentage differences in bone variables (DXA: left panel; pQCT: right panel) between the G_LL group and other groups. The vertical line (0) represents the G_LL group. The horizontal lines represent the 95% confidence interval, and the full circles represent the mean differences from the G_LL group.

Of the pQCT measurements (Table 2), at the distal radius, the G_LL group had significantly lower values of BMC than the G_HH group (p = .015) and the G_LH group (p = .004) and a significantly lower CSA than the G_LH group (p = .001). The G_HL group also had a significantly lower BMC value than the G_LH group (p = .038). At the middle radius, the G_LH group had higher values in total BMC, cBMC, and cCSA than the G_LL group (p = .007, p = .004, and p = .003). No differences were found in total vBMD and cvBMD. There were significant differences in CSA and C.Th by ANCOVA, but post hoc tests did not show differences among the groups. At the tibial shaft, the G_LL group had a significantly lower BMC, cBMC, and cCSA and thinner C.Th than the G_HH group (p = .001, p = .002, p = .001, and p = .004) and the G_LH group (p = .004, p = .001, p = .001, and p < .002). The G_LL group also had a lower total CSA than the G_HH group (p = .030). The G_HL group had a lower BMC, cBMC, and cCSA than the G_HH group (p = .013, p = .042, and p = .010) and the G_LH group (p = .035, p = .029, and p = .014). The G_HH group also had a larger total CSA than the G_HL group (p = .004). No significant differences were found for vBMD or cvBMD among the groups. In addition, no significant differences in BUA of the calcaneus were found in the post hoc comparison among the LTPA groups (Table 2).

To verify whether the differences in bone variables found after 7-year follow-up already existed at baseline, we compared those who had bone assessments at both age 11 and age 18. No differences were found in age, body height, body weight, BMI, fat mass, lean mass, bone mass, maximal knee extension force, jumping height, physical inactivity hours, and calcium intake at baseline (data not shown). No significant differences were found in any of the measured variables at any bone site among LTPA groups at baseline (Table 3). Calculation showed that we had 78% power to detect these differences at a significance level of p < .05.

Table 3. Bone Properties of the Girls at Baseline According to Consistency of LTPA

	High-high (n = 26)	High-low (n = 12)	Low-high (n = 16)	Low-low (n = 31)	ANOVA p
Values are given as mean ± SD.
DXA:
Total body
BMC (kg)	1.43 ± 0.24	1.37 ± 0.26	1.41 ± 0.27	1.34 ± 0.21	.560
BMD (g/cm^2)	0.95 ± 0.05	0.95 ± 0.06	0.94 ± 0.06	0.93 ± 0.04	.359
BA (cm^2)	1.50 ± 0.20	1.43 ± 0.21	1.49 ± 0.22	1.44 ± 0.18	.664
L2–L4
BMC (g)	24.1 ± 5.16	23.7 ± 6.54	22.8 ± 5.62	22.1 ± 5.13	.531
BMD (g/cm^2)	0.84 ± 0.09	0.82 ± 0.12	0.80 ± 0.12	0.81 ± 0.09	.589
BA (cm^2)	28.6 ± 3.60	28.4 ± 4.05	28.3 ± 3.60	27.1 ± 3.80	.525
Total femur
BMC (g)	20.5 ± 3.15	19.9 ± 3.93	20.3 ± 4.39	18.7 ± 3.22	.278
BMD (g/cm^2)	0.86 ± 0.09	0.85 ± 0.09	0.85 ± 0.12	0.80 ± 0.08	.091
BA (cm^2)	23.7 ± 2.21	23.1 ± 2.78	23.6 ± 2.46	23.5 ± 2.76	.918
pQCT:
Radius (distal)
BMC (mg/mm)	68.1 ± 9.8	65.2 ± 12.0	66.7 ± 9.8	64.2 ± 10.4	.406
vBMD (mg/cm^3)	293 ± 30	279 ± 30	300 ± 40	281 ± 28	.269
CSA (mm^2)	235 ± 38	236 ± 47	226 ± 43	231 ± 45	.899
Tibial shaft
BMC (mg/mm)	251 ± 32	238 ± 35	241 ± 34	236 ± 32	.371
vBMD (mg/cm^3)	673 ± 49	674 ± 52	664 ± 51	658 ± 56	.669
CSA (mm^2)	374 ± 51	354 ± 46	363 ± 49	361 ± 54	.655
cBMC (mg/mm)	212 ± 30	201 ± 34	200 ± 32	197 ± 31	.392
cvBMD (mg/cm^3)	1044 ± 23	1053 ± 21	1028 ± 32	1043 ± 21	.050
cCSA (mm^2)	203 ± 29	191 ± 31	194 ± 29	188 ± 28	.402
C.Th (mm)	3.53 ± 0.4	3.42 ± 0.5	3.42 ± 0.4	3.33 ± 0.4	.341
QUS:
BUA average (db/MHz)	66.8 ± 6.8	64.0 ± 7.7	64.7 ± 9.6	61.6 ± 6.2	.121

Discussion

In this study we found that girls with consistently higher LTPA than their peers from age 11 to 18 had significantly higher bone gain at various bone sites, including TB, TF, L₂–L₄, distal radius, and tibial shaft. Furthermore, girls with low LTPA at 11 years had the opportunity to improve bone accrual by increasing their physical activity level during puberty.

The outcomes of exercise intervention studies vary depending on the pubertal maturity level of the cohort at the beginning of the intervention. Studies with pre- or early-pubertal children have reported significant increases in lumbar spine and femoral neck BMD,11, 17, 31 but no significant differences in total-body and lumbar spine BMD and BMC have been found in postpubertal girls.32 In our previous report based on cross-sectional analyses, we also found that Tanner stage I appears to be a more sensitive period for exercise to provide a beneficial effect on bone development than Tanner stage II.13 Until recently, there were only a few prospective longitudinal studies that addressed the influence of childhood LTPA on bone measurements assessed in adulthood. Baxter-Jones and colleagues33 reported that active adolescent females had 9% and 10% more adjusted BMC at the total hip and FN than their peers when they were 23 to 30 years of age at follow-up. This result is consistent with ours, where the G_HH group had 12% and the G_LH group had 11% more BMC at the TF than the G_LL group. Gunter and colleagues34 found that a short-term high-impact exercise intervention performed in early childhood was still beneficial after 8 years. On the other hand, Alwis and colleagues35 reported that a 2-year school-based moderately intense exercise program was not beneficial for structural changes in the FN in Swedish girls from age 8 to 10 years. In contrast, another research group found a significant association between the natural log of MET (metabolic equivalent of physical activity) scores and BMD at the FN36 but not for BMD of the spine. The osteogenic effects of exercise seem to be region-specific and load-dependent, but it is evident that in comparing active and inactive populations, physical activity can increase or maintain bone health.37 Our study emphasizes the benefit of consistency in LTPA from prepuberty to early adulthood, as well as comparing those who changed their level of physical activity.

We found that girls in the G_LH group started to increase their level of LTPA around menarche and about half a year after PHV. A previous study also showed that onset of menarche is a critical time at which most girls started to change their behavior patterns.38 Our study is partly in agreement with some previous studies and supports the idea that exercise during the pre- and early-pubertal years has the greatest impact on bone accrual.6, 11 It is estimated that about 26% of adult whole-body bone mineral is accrued during the 2 years around peak growth and about 36% accrual over the 4 years surrounding PHV.8, 39 Thus, maximizing bone accrual during childhood and adolescence is critical for optimizing peak bone mass.40 Our study also indicates that increasing LTPA from a lower level to a higher level will benefit bone gain during adolescence, even if the increase in physical activity begins at the onset of menarche, especially for the femur. Our results provide additional evidence that exercise-intervention strategies to maximize bone accrual should target not only prepubertal girls but also those who have already entered puberty. Whether this finding transfers to males needs to be investigated.

Not only the intensity of exercise but also the type has an impact on bone. Weight-bearing physical activities with high bone strains have been shown to be the most important for increasing the accrual of BMD, and gains are more pronounced at the loaded bone sites.14, 15, 39, 41 In our study, the most common types of physical activity were non-weight-bearing physical activities (ie, cycling, swimming, and horseback riding) at the beginning of the study when girls were 11 years of age. When girls were 18 years of age, walking and jogging were the most common physical activities, in addition to cycling. We found that 68% of the total sample participated in a non-weight-bearing physical activity at age 11 but only 36% by age 18. In the G_LL group, non-weight-bearing activities still were more common at the end of the study; therefore, this may be one explanation of our results, namely, that the lower level of weight-bearing exercise contributed to the significantly lower values in BMC and BMD as well as C.Th compared with the other groups (G_HH and G_LH).

Some studies in children have shown no association between calcium intake and BMC.42 Rowlands and colleagues reported that in 8- to 11-year-old children, dietary calcium intake should be 700 to 800 mg/day, and participation in vigorous activity is needed for a positive impact on bone indices.43 In our study, the participants increased their calcium intake from 868 to 1163 mg/day by the end of follow-up. No group differences were found in calcium intake among the LTPA groups at either time point, nor was there an effect of calcium supplementation.21 Thus physical activity is quantitatively a more important factor in terms of affecting bone than calcium intake,37 and the differences in BMC and BMD found among the LTPA groups are most likely due to patterns of LTPA.

The limitations of our study include the use of a questionnaire to assess LTPA. While questionnaires have been reported to be the most feasible methods to estimate PA in large populations,44 overreporting of PA by questionnaires45 may not reflect the actual level of PA. Accelerometers or heart rate monitors may provide more accurate estimates of physical activity, but these methods were not feasible to use during a 7-year follow-up study. Our study21 and a recent study by Kurtze and colleagues have shown that a PA questionnaire can be reproducible and provide useful measure of LTPA.46 In Finland, winter time PA is dominant, and the LTPA scores are higher than those reported for the summer.

Our sample had 12.4% of the participants classified as overweight/obese using the system of Cole and colleagues.29 This is equivalent to the prevalence of overweight/obesity (11%) published by the Finnish national report for female students (15 to 24 years of age).47 Only one of our participants met the requirements for the obese category; thus the results of our study are applicable to females who are normal or overweight.

In conclusion, our results indicate that long-term LTPA has a positive effect on peak bone mass gain of multiple bone sites in girls from the ages of 11 to 18 years. We also found that increasing physical activity from a low level during puberty promotes bone accrual at multiple bone sites. Encouraging girls to exercise regularly, especially in weight-bearing activity, during the postmenarcheal years is important for bone health.

Disclosures

All the authors state that they have no conflicts of interest. The study sponsors played no role in the design, methods, data management, or analysis nor in the decision to publish. None of the authors has a financial or personal-interest affiliation with the sponsors of this research.

Acknowledgements

We would like to thank the participants and the whole research staff and especially Mrs Shu Mei Cheng, Mrs Heli Vertamo, Ms Sirpa Mäkinen, and Mr Erkki Helkala for their valuable work and technical assistance on this project. This study was supported by grants from the Academy of Finland, Finnish Ministry of Education, University of Jyväskylä, and Juho Vainion Foundation.