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A 2-yr, School-Based Resistance Exercise Pilot Program Increases Bone Accrual in Adolescent Girls

Dowthwaite, Jodi N.1; Weiss, Deena M.2; Thein-Nissenbaum, Jill3; Scerpella, Tamara A.1,4

Translational Journal of the American College of Sports Medicine: June 1, 2019 - Volume 4 - Issue 11 - p 74–83
doi: 10.1249/TJX.0000000000000086
Original Investigation
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ABSTRACT The current analysis evaluates cumulative benefits after year 2 of a school-based resistance training intervention. Adolescent girls were enrolled and measured at the beginning of sixth grade (baseline [BL]) and again at first follow-up (Y1 end) and second follow-up (year 2 end). School gym classes met alternate school days. Site 1 had standard gym classes (CON). Site 2 gym classes included 8–12 min of resistance training (INT); INT girls were categorized based on observed participation effort and time (LO, HI). Measurements included the following: 1) height and weight, 2) questionnaires to assess extracurricular exercise and diet (calcium, vitamin D), and 3) dual-energy X-ray absorptiometry (Lunar Prodigy). Whole body less head scans yielded bone mineral content (BMC) and body composition. Lumbar spine (L1–L4) and femoral neck (FN) scans yielded BMC and areal bone mineral density (BMD); radius scans yielded ultradistal and 1/3 BMD. ANCOVA compared group means for percent gains from BL to second follow-up, accounting for biological maturity, BL height, height change, interscan interval, organized activity, calcium, and vitamin D. In 62 girls (21 CON, 41 INT), intention-to-treat analyses detected INT versus CON advantages for L1–L4 BMC and BMD (4.1%, 5.6%: P < 0.05). HI effort participants (n = 19) demonstrated advantages for BMC and BMD at L1–L4 and FN (5.7% to 8.2%, P < 0.01) versus CON. Over two school years, this resistance intervention yielded lumbar spine advantages; enthusiastic participation (HI) yielded lumbar spine and FN advantages. Further work is warranted to evaluate benefit persistence after intervention cessation.

1Department of Orthopedic Surgery, SUNY Upstate Medical University, Syracuse, NY;

2University of Wisconsin School of Medicine and Public Health (UWSMPH), Madison, WI;

3Department of Family Medicine and Community Health, UWSMPH, Madison, WI; and

4Department of Orthopedics and Rehabilitation, UWSMPH, Madison, WI

Address for correspondence: Jodi N. Dowthwaite, Ph.D., Department of Orthopedic Surgery, Musculoskeletal Science Research Center, 750 E. Adams Street, Syracuse, NY 13210 (E-mail: dowthwaj@upstate.edu).

Compendium date: June 1, 2019

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INTRODUCTION

For the past two decades, investigators have attempted to define osteogenic youth exercise, with the goal of optimizing skeletal gains during growth (1–5). Skeletal gains acquired during childhood and adolescence likely persist to improve adult bone health (6–12). Certain activities, such as artistic gymnastics and soccer, have been associated with greater bone mass, geometry, and/or density at various sites (6,13–21). Many highly osteogenic activities impart high impact and/or “odd” impact loading (18,19), such that tissue strains exceed habitual levels and/or are out of the plane of “normal” movements. Accordingly, attempts to identify broadly generalizable, easily implemented osteogenic exercise regimens have focused on programs using impact as a main form of exercise. Interventions testing school-based jumping programs in pre- and peripubertal boys and girls have been associated with small to moderate advantages in bone acquisition over 7- to 20-month periods (1–5).

Our team has previously reported benefits in bone acquisition in sixth-grade girls exposed to a school-based resistance training intervention, relative to age-matched controls (22). We tested this program because of its potential generalizability and ease of administration in a group setting, using simple low-cost equipment, including resistance bands, handheld weights, and medicine balls. In addition, we were attracted to the potential for the exercise program to affect all skeletal sites, not just the weight bearing sites typically improved by jumping programs. However, after the initial 8-month intervention, significant benefits were identified only in a subsample of high effort participants who were Tanner breast stage 2 or 3 at baseline (BL) (22). We noted significantly greater gain in lumbar spine bone mineral density (BMD) in Tanner 3 girls (4%) and femoral narrow neck width (19%) in Tanner 2 girls compared with maturity-matched controls (22). We hypothesized that continued exposure to this resistance training protocol would yield significant skeletal advantages at clinically important sites, including lumbar spine, proximal femur, and distal radius. Therefore, we undertook the present analysis to evaluate skeletal benefits after a second, consecutive year of this school-based exercise intervention.

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METHODS

Study protocols were approved by our university’s Institutional Review Board, in compliance with the Code of Ethics of the World Medical Association (Declaration of Helsinki). We enrolled sixth-grade girls from a local, Midwestern, suburban school district with two geographically separated middle schools (22). Students were recruited during sixth-grade orientation at each school in late summer. The PI and other members of the research team sat at a table during each orientation session and provided verbal and written information regarding the study. Potential participants provided their contact information and were given a copy of the consent document. They were formally enrolled when they attended a BL measurement session. As study participants were minors at enrollment, they provided informed assent, accompanied by parental informed consent.

Study measurements were obtained at the beginning of sixth grade (BL), approximately 8 months later at the completion of the school year (follow-up 1 [FU1]), and again 1 yr later at the completion of the seventh-grade school year (follow-up 2 [FU2]). Subjects were assigned to the intervention or control group based on geographically determined attendance at one of two middle schools in that district; formal randomization beyond chance geographic distribution was not carried out (first school = control [CON]; second school = intervention [INT]). The two schools draw from a school district with the following racial/ethnic composition: 85% white, 4% black, 4% Hispanic, 5% Asian, and 2% mixed (23).

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Intervention

At BL, all participants were transitioning from elementary to middle school and began attending one of the two participating middle schools for the first time as sixth graders. At both schools, required gym classes met two or three times per week (alternating school days) and included traditional gym class activities like basketball, volleyball, and dodgeball. At the intervention school, the focal resistance training intervention was also incorporated at the beginning of most gym class sessions, as part of the standard regimen for all students at this school (regardless of study enrollment). Accordingly, the only extra time commitments and protocols for study participants versus nonparticipants were BL and follow-up measurement sessions. The resistance training program used exercise bands, handheld weights, medicine balls, and body weight to achieve progressive overload in all major muscle groups (see Video, Supplemental Digital Content 1, Resistance Training Intervention, http://links.lww.com/TJACSM/A38). In general, exercises focused on whole body, multiplanar, functional movements. Specific content varied day to day and included lunges, body rows, push-ups, pull-ups, planks, and other combined arm and leg resistance exercises. Occasionally, jumps/hops were included for less than 1–2 min.

The intervention activity sessions lasted 8–12 min and included two to four exercises at each of 4 stations (1 min per exercise, 40 s on, 20 s off, for each exercise). Prerecorded bells provided timing at 40 and 20 s each minute, played in conjunction with high-energy music. Progressive overload was achieved by the introduction of higher-intensity modifications of exercises as the school year progressed and by the incorporation of increasingly stiffer elastic bands and heavier handheld weights. Increases were made at student discretion under the guidance of a supervising physical education instructor and were individualized to provide a safe but challenging workout for each student. Each session was preceded by a 4- to 6-min floor warm-up, including static and dynamic activities to engage core, arm, and leg muscles. The four physical education instructors at the intervention school were well versed in this program, as each had been using it as part of the middle school curriculum for the previous 2–3 yr.

The intervention activity began approximately 1 month after physical education classes commenced in the fall and concluded with the onset of warm weather, allowing outdoor activities in the spring. Initial familiarization with techniques and equipment required 3–4 wk additional “ramp-up” time. Therefore, the intervention spanned a period of 6 months, from November 1 to May 1, minus school vacation weeks, providing 24 wk of intervention activity exposure per school year. Because gym classes at the elementary school did not incorporate resistance band exercises, and because it is unusual for young girls to perform these exercises on their own, the vast majority of participants reported that they had not engaged in formal resistance training at any point before BL measurements.

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Participants

Female study participants were recruited from an upper-Midwestern suburban school district. The total number of female students entering the sixth grade was 112 girls at the intervention school and 97 girls at the nonintervention school; we enrolled as many students from each site as were willing to participate. Ethnic/racial composition of the included sample was as follows: 88.7% white, non-Hispanic; 4.8% mixed race; 4.8% Asian; and 1.6% Hispanic. Participants ranged in age from 11.0 to 12.1 yr at BL and from 12.6 to 13.7 yr at FU2.

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Physical Maturity Assessment

In girls, the most rapid period of bone accrual occurs in the 4 yr roughly centered at menarche (24). Our rationale for maturity assessment is based on this biological foundation, as well as our previous work confirming the value of menarche as a maturational milestone for centering longitudinal studies of bone accrual (7,25). Thus, in this study, menarche date was recorded to inform assignment of maturity group based on relative bone accrual progression. Self-assessed Tanner stage is unreliable for precise pubertal staging at higher maturity levels, but for pubertal onset in girls, self-assessment and clinical assessment exhibit strong agreement (26). Accordingly, we used self-assessed Tanner stage as the basis for distinguishing between prepubertal and pubertal status (an indicator of estrogen exposure), and we used menarche as a discrete marker reflecting peak bone mineral accrual velocity. At BL and both follow-up sessions, all participants provided self-assessed Tanner breast and pubic staging, based on line drawings with short descriptions. In addition, menarche date was queried and recorded at each measurement session until menarche was achieved. On this basis, we divided participants into three biological maturity groups, as follows: PRE = premenarche at BL and FU2; PERI = premenarche at BL, postmenarche at FU2; and POST = postmenarche at BL and FU2.

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Intervention Compliance

To minimize the risk that poor compliance or attendance would confound results, our study design included, a priori, a plan to quantify intervention participation time and to record participation effort. A single member of our research team observed all intervention physical education classes over the course of the first year (year 1, from BL to FU1), documenting daily effort and participation minutes for each study participant (22). Although participation in the intervention was mandatory at the intervention school, not every student in each physical education class was enrolled in our study. Therefore, a close observation of study participants was feasible, as each physical education class contained only two to nine of our study participants.

Effort was qualitatively assessed for every intervention activity session, categorizing effort for each participant as low (=1), medium (=2), or high (=3) based on observation. Participant effort was rated as “low” for those who (a) stopped exercising when the teacher was not looking, (b) decreased exercise time by moving slowly between stations, and/or (c) exercised with low vigor. By contrast, participant effort was rated as “high” for those who (a) exercised regardless of teacher observation, (b) maximized exercise time for each station, and (c) participated with vigor. Participant effort was rated as “medium” if they fell somewhere between the two extremes or demonstrated inconsistent effort during an intervention session. For each session, individual numeric effort scores were multiplied by the number of participation minutes (effort × minutes). All effort × minutes session scores were summed to create subject-specific totals. On this basis, effort and failure to participate for any reason were incorporated into the summed effort score (e.g., absence, illness, injury, and unprepared status).

Subject-specific effort × minutes totals were used to determine a dichotomous grouping variable based on total effort during year 1: low effort (LO, current n = 22) mean = 774 effort × minutes (range, 381–1080); high effort (HI, current n = 19) mean = 1561 effort × minutes (range, 1155–1982). During year 2 (7 months directly preceding FU2), intermittent class observations were performed over the course of the school year to evaluate effort agreement with year 1, and physical education instructors were consulted to quantify intervention minutes. On the basis of this information, at FU2, all but one subject, who missed significant time due to illness, was classified in the same effort group as for FU1; therefore, effort groupings were maintained from FU1 to FU2 for statistical analyses.

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Densitometry and Other Measurements

At BL, FU1, and FU2, total body and regional dual-energy X-ray absorptiometry (DXA) scans were performed by a single technologist certified by the International Society for Clinical Densitometry, using a GE Healthcare Lunar iDXA densitometer (Madison, WI). Using enCore software (version 13.31), total body scans assessed fat mass for whole body (WB) and nonbone lean mass for WB less head (SUB). Percent body fat was calculated for WB (fat mass / total mass). Regional scans provided bone mineral content (BMC) for SUB, lumbar spine (L1–L4), and femoral neck (FN); areal BMD was evaluated for L1–L4, FN, ultradistal radius (radUD), and 1/3 radius (rad1/3) regions of interest.

To calculate values of age-specific coefficient of variation (CV), duplicate same-day scans are required; this practice is uncommon in growing children and adolescents, as it increases risks from greater radiation exposure to rapidly growing tissues. Accordingly, to evaluate quality control, we relied on CV for DXA variables calculated using duplicate scans of 30 postmenopausal females: FN BMD and total body BMC CV values were <1%, lumbar spine BMD and FN BMC CV values were <2.0%, and radius BMD CV values were <4% (22). CV values for lean and fat mass were <1%, assessed in young adult females, 18–23 yr old (WB scans only) (27).

Anthropometrics and other data were collected contemporaneous with DXA scans, as follows. Height was measured, in stocking feet, via wall-mounted stadiometer (Holtain Model 602VR, Crosswell, Pembrokeshire, UK), to the nearest 0.1 cm, and weight was measured in light clothing via electronic force plate (Leonardo Mechanograph® GRFP STD, Novatec), to the nearest 0.01 kg. Body mass index (kg·m−2) was calculated from resultant mass and height. Forearm length was measured with a ruler to the nearest 0.1 cm, from the tip of the olecranon to the tip of the ulnar styloid. A validated, pediatric, semiquantitative food frequency questionnaire was completed to assess food consumption habits (28), yielding intakes of calcium and vitamin D, including supplementation. For the present analysis, mean intakes were calculated from the results of questionnaires administered at FU1 and FU2, representing habitual intakes between BL and FU2. With assistance from parents, subjects used a calendar-based form to report hours per week of participation in nonaquatic organized activity, excluding gym class time, over the same intervals (BL to FU1, FU1 to FU2), allowing calculation of mean background organized activity dose (h·wk−1) from BL to FU2 (22). In previous research, 12-month activity means from a similar population correlated strongly with coaches’ logs (r > 0.97, P < 0.0001) (14).

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Statistical Analyses

A priori power calculations were based on cross-sectional gymnast versus nongymnast comparisons for a group of girls of similar age to the cohort studied here, at two effect size levels, derived from a longitudinal, observational study (7,29). We hypothesized that the intervention would yield benefits comparable to 50%–75% of the effect sizes observed in gymnasts versus nongymnasts. At 50% of observed gymnast advantages, 10–31 girls per group would be required to achieve at least 80% power to detect significant differences between intervention participants and controls. At 75% of observed gymnast advantages, cell sizes of 10–14 would provide at least 80% power to detect significant differences.

SPSS version 23 was used to perform statistical analyses (IBM, Armonk, NY), using alpha = 0.05. Normality of distributions was evaluated using Kolmogorov–Smirnov tests. Where appropriate, dependent variables were ln-transformed for analysis, or Kruskal–Wallis tests were used to evaluate group differences in descriptive statistics. Otherwise, ANOVA or repeated-measures (RM) ANOVA were used to assess group differences, as appropriate. For ANOVA and RM ANOVA, Levene’s test was used to evaluate equality of error variances. Intervention status was coded for comparisons as follows: control (CON), intervention (INT), low effort (LO), and high effort (HI). Intention-to-treat analyses compared results for CON versus INT; to evaluate intervention success with high compliance, we compared CON versus HI. To evaluate potential bias in maturational status, chi-square analysis was used to evaluate associations between maturity status and intervention status (INT vs CON; CON vs LO vs HI), as well as race/ethnicity and intervention status. We used Pearson correlations to assess the potential relationship between interscan interval (date difference, BL to FU2, years) and dependent variables.

To minimize potential for type 1 error through multiple testing, dependent variables were limited to the following: subhead BMC (SUB BMC), radUD BMD, rad1/3 BMD, FN BMC, FN BMD, L1–L4 BMC, and L1–L4 BMD. Both BMC and BMD were evaluated for L1–L4 and FN to allow comparison of our results in previous research (see discussion). Included covariates were as follows: maturity status, intermeasurement background organized physical activity exposure (excluding gym class), mean interscan calcium intake, natural logarithm of mean vitamin D intake, interscan interval, BL dependent variable, BL height, and interscan change in height (FU2 minus BL).

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RESULTS

Of the original 68 participants enrolled and measured at BL, 62 were measured at FU2 and form the basis of this analysis. Descriptive statistics are presented in Table 1 for the total sample (n = 62), and separately for the CON (n = 21), LO (n = 22), and HI (n = 19) groups. (The six study participants who did not return for FU2 included two CON and four INT.) As the two schools have slightly different race/ethnicity profiles for their student bodies, we tested for differences in CON versus INT profiles; among individuals returning for FU2, racial and ethnic groups were distributed evenly among control versus intervention and control versus LO versus HI groupings (chi-square P > 0.91).

TABLE 1

TABLE 1

Of the 62 participants included in the present analyses, most had not achieved menarche at BL in the fall of their sixth-grade year; by FU2, most were postmenarcheal. In terms of pubertal onset, 56/62 had entered puberty at BL (self-reported Tanner breast or pubic stage II or higher); few girls were prepubertal at BL (1 CON [6%], 3 LO [14%], and 2 HI [10%]). As described in the Methods section, to reflect maturational progression over the full study period, participants were classified in one of three groups: premenarcheal at BL and FU2 (PRE, n = 21), premenarcheal at BL, and postmenarcheal at FU2 (PERI, n = 32) or postmenarcheal at BL and FU2 (POST, n = 9).

There was no significant difference in menarche status by group (INT vs CON, chi-square P > 0.09; CON vs LO vs HI: chi-square P > 0.30). However, there was a trend for more CON to be classed as PRE or POST compared with INT (CON: PRE = 43%, PERI = 33%, POST = 24%; INT: PRE = 29%, PERI = 61%, POST = 10%); the majority of INT were classed as PERI. On this basis, we included maturity status as an independent variable in regression analyses and ANCOVA.

Table 2 shows raw data for dependent variables at BL and FU2; no GROUP differences were detected for BL dependent variables using ANOVA (P > 0.14). Likewise, from BL to FU2, no significant GROUP differences were detected for mean interscan values for physical activity level (Kruskal–Wallis P > 0.53), calcium intake or ln vitamin D intake (ANOVA P > 0.37).

TABLE 2

TABLE 2

There was a significant difference among intervention groups for interscan interval (Kruskal–Wallis P < 0.001), with both LO and HI having longer interscan intervals than CON (LO = 19.3 ± 0.7 months, HI = 19.2 ± 0.8 months, CON = 18.5 ± 0.7 months). However, this interval disparity represented only ~4% of the total interscan interval (~3 wk). In addition, from BL to FU2, no significant GROUP (LO, HI, and CON) differences (RM ANOVA P > 0.23) or group–time interactions (P > 0.12) were detected for height, weight, body mass index, or percent body fat, or for age at either time point (Kruskal–Wallis P > 0.08), suggesting that body growth was similar across the interscan interval for all groups and was not likely to have confounded the significant group differences identified in bone accrual. Nonetheless, we evaluated this potential source of bias by including interscan interval and change in height as independent variables in ANCOVA; interscan interval exerted no significant influence as a covariate in any of the models (P > 0.20).

Intervention participation was quantified for each individual during year 1. Mean participation time over the 24 wk of the intervention was 22.3 min·wk−1. Similarly, when only the HI group was considered, mean participation time was 22.1 min·wk−1. Thus, the division of participants into HI and LO effort groups (effort minutes = effort × minutes) was mainly a function of observed effort, as mean exposure time was not greater in HI than LO.

Intention-to-treat ANCOVA (INT vs CON) indicated that intervention exposure conferred site-specific advantages in gain of both BMC and BMD at L1–L4, regardless of intervention effort or participation time (effort × minutes) (P < 0.05; 5.6% and 4.1%, respectively) (Fig. 1). No covariates exerted significant individual influence (all P > 0.22).

Figure 1

Figure 1

To quantify differences in percentage gains between BL and FU2 as a function of high intervention compliance, we used ANCOVA to compare adjusted group means for HI versus CON (LO excluded). Significant, site-specific intervention advantages were observed for L1–L4 BMC, L1–L4 BMD, FN BMC, and FN BMD (P = 0.006, 0.005, 0.007, and 0.006, respectively) (Table 3). These results indicated relative advantages for HI versus CON in percent gain, ranging from 3.9% to 7.6% for these same outcomes (P < 0.008) (Fig. 2). Intervention exposure appeared to confer no advantage in radius properties at either site, with a trend for intervention disadvantage in ultradistal BMD. Height change was a significant covariate (P = 0.000), with maturity, BL height, and inter-DXA physical activity exposure playing minor supportive roles (P = 0.07, P < 0.15); other covariates were not significantly influential (P ≥ 0.21). In all dependent variable–based analyses, Levene’s test indicated equivalent error variances (all P > 0.13, except LS BMC percent difference P > 0.07).

TABLE 3

TABLE 3

Figure 2

Figure 2

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DISCUSSION

This group of predominantly white, upper-Midwestern, adolescent girls obtained significant lumbar spine BMC and BMD benefits through two consecutive school years of a resistance training program, regardless of maturity status and background physical activity. Exposure averaged only 22 min·wk−1, acquired in 1–2 sessions per week. Girls who demonstrated high intervention effort had significant advantages at both lumbar spine and FN sites, gaining 5%–8% more bone mass than controls. Importantly, intervention benefits were clear at sites that are prone to clinically devastating fragility fractures later in life (FN, lumbar spine).

Our results are similar to those of other investigative groups who have evaluated various interventions in pre-, peri-, and postpubertal girls over interventions spanning 7 to 20 months (1–5). After a school-based, 10-month controlled intervention in 9- to 10-yr-old girls, using aerobic impact and weight training, Morris et al. (4) identified differential percent gains in total body (5.5%) and FN (6.5%) BMC. However, their intervention involved 30-min sessions, three times weekly, averaging more than 4 times the weekly intervention exposure time of our protocol. It is possible that our protocol would yield even greater benefits, if comparable exposure times were achieved. Fuchs et al. (2) identified differential gains of 4.5% and 3.1% for FN and lumbar spine BMC, respectively, in a combined sample of prepubescent boys and girls who participated in a 7-month jumping intervention (100 jumps, 3 times weekly). MacDonald et al. (5) identified a 5.4% advantage in FN strength in a subset of highly compliant 9- to 11-yr-old girls who participated in 11 months of a school-based exercise program, monitored over a 16-month period. Weeks et al. (3) evaluated bone mass in peri- and postpubertal boys and girls (mean age 13.8 ± 0.4 yr) after an 8-month school-based randomized controlled trial that included 10 min of jumping, twice weekly. They identified significant gains in FN BMC, LS BMD, and LS area for girls; however, differential gains for intervention participants versus controls were not statistically significant (FN BMC, 13.9% vs 4.9%; LS BMD, 5.2% vs 1.5%; and LS area, 4.9% vs 2.0%) (3). Finally, in a group of girls who were 10 yr old at BL, MacKelvie et al. (1) identified significant advantages in lumbar spine (3.7%) and FN (4.6%) BMC gains after a high-impact, circuit-based, jumping intervention (10 min, 3 times a week) over 20 months (two school years).

Although difficult to compare based on intervention variation (type, intensity, and duration) and group composition (sex and maturity), our 19-month differential percent gains (14 months of intervention exposure) are greater than or equal to those previously reported after 7–11 months of intervention exposure (≤16 months observation). Particularly when the amount of minutes engaged in the intervention is considered, our results spanning two 7-month exposure periods are notable. Moreover, our results were accomplished using resistance bands and light handheld dumbbells, with minimal impact loading, in contrast to the previously published interventions that focused on jumping.

The group of girls included in the present analysis is not identical with the group in which we previously reported 8-month results (22). For the previous analysis, we specifically evaluated a smaller subset of the whole group, comparing HI effort participants versus controls in girls who were Tanner breast stage 2 or 3 at BL (T2 and T3, n = 48). In that subset, we identified advantages in differential gains for T3 girls at the lumbar spine (BMD, 4%) and for T2 girls at the FN (width, 19%) (P < 0.03) (22). The present analysis includes the entire group of girls who provided both BL and 19-month follow-up data (n = 62), accounting for maturational variation on the basis of menarche status progression (PRE, PERI, and POST groups). In the current analysis, the significant benefits observed in intervention subjects across the total sample (lumbar spine BMC and BMD) may be attributable to cumulative benefits of a second year of intervention exposure or to exposure during a more favorable maturity phase for adaptation, when estrogen levels were likely higher. Forty-four girls in the present analysis were postmenarche by the completion of year 2 (44/62: 71% of year 2 analysis sample), compared with only 15 girls from the previously published analysis who were postmenarcheal at the completion of year 1 (15/38: 39% of year 1 analysis sample). As noted above, we have previously provided evidence of greater intervention response at the lumbar spine in more mature (T3 vs T2) participants; a similar effect may have contributed to the significant response observed after the year 2 intervention (22). In the present analysis, maturity status was not a significant covariate in ANCOVA, likely due to collinearity with change in height, which was a highly influential covariate in both sets of analyses. Results of the present analysis do not allow us to distinguish between cumulative and/or maturity-specific intervention effects; it is likely that both factors played a role in year 2 bone acquisition. Future analyses, when all subjects are postmenarche, will address maturity-specific responses to intervention activity more effectively, using biological age as a continuous function to evaluate activity exposure timing relative to menarche (see Limitations section).

We were concerned that background physical activity participation, separate from the resistance training intervention, might confound our results. Therefore, we carefully recorded hours per week of nonintervention organized physical activity and calculated a mean value for the study interval. We have reported significant associations with both lumbar spine and FN bone outcomes in children and adolescents using mean organized activity recorded using a similar questionnaire (16,30). We are confident that entry of this organized activity variable as a covariate in ANCOVA captured the intended physical activity exposure variation, as it explained 5% of variance in fat mass in separate regression models (data not shown: negative factor, P = 0.004). However, organized physical activity did not serve as a significant covariate in either ANCOVA bone model. Thus, in our cohort of sixth- and seventh-grade girls, the focal resistance training intervention appears to have been a more influential factor in bone acquisition than background, nonintervention organized physical activity; this lack of significance may be due to lower variance in organized activity exposure and vigor in the current study than that in our previous work. Although use of accelerometers may provide a better indicator of background activity vigor than activity hours alone, short-term accelerometry may not reflect long-term patterns and is burdensome for longitudinal monitoring of study participants over multiple years (13). Use of other devices to measure bone stresses directly (e.g., strain gauges) is unlikely to be approved for use in healthy pediatric populations and would deter study participation.

There was no difference in reported calcium or vitamin D intake among groups. On the whole, girls consumed the current RDA for calcium (1300 mg·d−1) and fell below current recommendations for vitamin D intake (600 IU·d−1). With no significant difference in intakes among groups, it is unlikely that variation in vitamin D consumption confounded our results, especially as we accounted statistically for intake variation in our analyses. We cannot rule out variability in serum vitamin D, as disparate sun exposure may have contributed to more disparate serum vitamin D levels than are evident based on intake indices. It is possible that a greater intervention effect might have been observed if vitamin D intakes had been within the adequate range.

The current analysis was designed to assess the effect of a resistance training intervention over two school years. Effort was carefully observed and recorded for each girl during the first intervention year, but it was only “spot checked” during year 2 (different observer, blind to year 1 effort status). Because “spot checking” indicated consistent effort level within individuals from year to year, we did not change the categorization of LO and HI effort groups from year 1 to year 2. It is possible that some girls classed as HI effort in year 1 may have reduced effort while not observed by researchers during year 2, and conversely, some girls classed as LO effort in year 1 may have increased effort while not observed by researchers during year 2. However, this possible scenario, yielding more similar effort levels between HI and LO groups, would have been expected to reduce differences between HI and LO intervention groups; accordingly, our view is that observed significant differences between HI and LO likely provide a conservative view of benefits attributable to enthusiastic participation in this loading intervention.

The efficacy of an exercise intervention is limited by both compliance and generalizability; programs that are not easily implemented and enthusiastically completed over a sufficient term will not be successful. In the current analysis, our data suggest that approximately 50% of the intervention participants were adequately enthusiastic to derive significant benefits at both major sites of osteoporotic fracture. Future research is needed to ascertain how to motivate all participants to engage with sufficient effort to gain significant and clinically relevant benefits. The intervention studied here was performed as part of the regular, school-based physical education program. It is important to note that all intervention schoolgirls participated in these exercise sessions, as they were part of the curriculum; unfortunately, we cannot evaluate effort or benefits in these girls, as they did not enroll in the study. The sessions required only 8–12 min of participation, 2–3 d·wk−1, from November through April. Equipment includes light dumbbells and wall-mounted resistance bands, which are low in cost and easy to store and maintain. The program is safe, easy to teach, and easy to individualize in a group setting, allowing progressive resistance as strength and coordination improve. Implementation on a large scale, in a variety of schools, appears feasible but must be tested in a large study that includes schools representing a variety of racial, ethnic, and socioeconomic characteristics. Additional study, including careful assessment of maturational progression during exposure, evaluating retention of benefits after intervention cessation, is needed to assess the utility of this or similar adolescent exercise interventions in improving adult bone health.

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Limitations

As is often the case in a clinical interventional study, our study was hampered by several methodological issues. First, we successfully enrolled and studied only about 1/3 of eligible students at the study schools, minimizing representation and generalizability of results. Second, a different observer assessed intervention effort during years 1 and 2, introducing the possibility that variation in effort was underreported. Third, the current intermediate analysis uses a simplistic RM design, which does not allow for evaluation of time-varying covariates, as would be ideal for a growth analysis of this nature. We plan more sophisticated analyses when additional follow-up data have been accumulated, evaluating relevant factors that change across time (e.g., height, weight, and body composition) and accounting for biological age as a continuous variable. This strategy will improve statistical power and provide us with greater capacity to evaluate the potential influence of disparate rates of growth/maturation and uneven interscan interval on bone accrual rates; the current analysis was underpowered to completely address this concern and likely underpowered overall. Fourth, participants were assigned to the intervention by school site (geographic basis only); although it is possible that this methodology may have resulted in the systematic influence of factors such as socioeconomic status or racial/ethnic variation on variables of interest, our racial/ethnic chi-square results do not support this concern. Finally, our metric of background physical activity relies on self-reported calendar-based data, rather than accelerometric measures; as noted, we are confident that these data capture relevant variance in organized activity exposure, as they explained significant variance in follow-up fat mass, accounting for key covariates. The observed negative association with fat mass, without a significant association with bone properties, suggests that there may have been inadequate variance in osteogenic activity separate from the intervention to detect “background activity” bone benefits in the current sample.

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CONCLUSION

This study provides evidence of significant benefits in lumbar spine properties as a result of a simple school-based exercise intervention, even in participants who expended low effort. Higher levels of participation compliance were associated with significant benefits at both lumbar spine and FN. Observed benefits, the ease of participation, and the potential generalizability of the intervention make this pilot program an attractive possibility for bone-building youth exercise. Further study is necessary, including a larger randomized trial to determine whether broad implementation is feasible and yields significant benefits under more stringent conditions. Additional follow-up is needed to determine whether long-term benefits are realized.

Conception and study design: TAS. Data collection: Kristen Hendrickson and Brittney Bernardoni. Data analysis: JND. Data interpretation: JND, TAS, DMW, and JTN. Drafting: JND. Revising critically: JND, TAS, DMW, and JTN. Final approval of manuscript: JND, TAS, DMW, and JTN. Responsibility for integrity: JND, TAS, DMW, and JTN. The authors are deeply grateful to Kristen Hendrickson and Dr. Brittney Bernardoni who worked as study coordinators for the first and second year of this longitudinal study, respectively; their dedication provided meaningful data and remarkable study retention. The authors appreciate the expertise and dedication of Jessie Libber, their study DXA technologist. The results of the present study do not constitute endorsement by the American College of Sports Medicine.

The authors have no conflicts of interest to disclose. They acknowledge funding support from the UW Institute for Clinical and Translational Research (Clinical and Translational Science Award, NIH/NCATS 9U54TR000021) and from the UWHC Sports Medicine Classic Fund.

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