Jodi N. Dowthwaite

Site-specific advantages in skeletal geometry and strength at the proximal femur and forearm in young female gymnasts☆

PURPOSE We evaluated site-specific skeletal adaptation to loading during growth, comparing radius (RAD) and femoral neck (FN) DXA scans in young female gymnasts (GYM) and non-gymnasts (NON). METHODS Subjects from an ongoing longitudinal study (8-26yr old) underwent annual DXA scans (proximal femur, forearm, total body) and anthropometry, completing maturity and physical activity questionnaires. This cross-sectional analysis used the most recent data meeting the following criteria: gynecological age ≤2.5yr post-menarche; and GYM annual mean gymnastic exposure ≥5.0h/wk in the prior year. Bone geometric and strength indices were derived from scans for 173 subjects (8-17yr old) via hip structural analysis (femoral narrow neck, NN) and similar radius formulae (1/3 and Ultradistal (UD)). Maturity was coded as M1 (Tanner I breast), M2 (pre-menarche, ≥Tanner II breast) or M3 (post-menarche). ANOVA and chi square compared descriptive data. Two factor ANCOVA adjusted for age, height, total body non-bone lean mass and percent body fat; significance was tested for main effects and interactions between gymnastic exposure and maturity. RESULTS At the distal radius, GYM means were significantly greater than NON means for all variables (p<0.05). At the proximal femur, GYM exhibited narrower periosteal and endosteal dimensions, but greater indices of cortical thickness, BMC, aBMD and section modulus, with lower buckling ratio (p<0.05). However, significant interactions between maturity and loading were detected for the following: 1) FN bone mineral content (BMC) and NN buckling ratio (GYM BMC advantages only in M1 and M3; for BMC and buckling ratio, M1 advantages were greatest); 2) 1/3 radius BMC, width, endosteal diameter, cortical cross-sectional area, and section modulus (GYM advantages primarily post-menarche); and 3) UD radius BMC and axial compressive strength (GYM advantages were larger with greater maturity, greatest post-menarche). CONCLUSIONS Maturity-specific comparisons suggested site-specific skeletal adaptation to loading during growth, with greater advantages at the radius versus the proximal femur. At the radius, GYM advantages included greater bone width, cortical cross-sectional area and cortical thickness; in contrast, at the femoral neck, GYM bone tissue cross-sectional area and cortical thickness were greater, but bone width was narrower than in NON. Future longitudinal analyses will evaluate putative maturity-specific differences.

Mechanical loading during growth is associated with plane-specific differences in vertebral geometry: A cross-sectional analysis comparing artistic gymnasts vs. non-gymnasts.

Lumbar spine geometry, density and indices of bone strength were assessed relative to menarche status, using artistic gymnastics exposure during growth as a model of mechanical loading. Paired posteroanterior (pa) and supine lateral (lat) DXA scans of L3 for 114 females (60 ex/gymnasts and 54 non-gymnasts) yielded output for comparison of paired (palat) versus standard pa and lat outcomes. BMC, areal BMD, vertebral body dimensions, bone mineral apparent density (BMAD), axial compressive strength (IBS) and a fracture risk index were evaluated, modeling vertebral body geometry as an ellipsoid cylinder. Two-factor ANCOVA tested statistical effects of gymnastic exposure, menarche status and their interaction, adjusting for age and height as appropriate. Compared to non-gymnasts, ex/gymnasts exhibited greater paBMD, paBMC, paWidth, pa Cross-sectional area (CSA), paVolume, latBMD, latBMAD, palatCSA and palatIBS (p<0.05). Non-gymnasts exhibited greater latDepth/paWidth, latBMC/paBMC, latVHeight, latArea and Fracture Risk Index. Using ellipsoid vertebral geometric models, no significant differences were detected for pa or palat BMAD. In contrast, cuboid model results (Carter et al., 1992) suggested erroneous ex/gymnast paBMAD advantages, resulting from invalid assumptions of proportional variation in linear skeletal dimensions. Gymnastic exposure was associated with shorter, wider vertebral bodies, yielding greater axial compressive strength and lower fracture risk, despite no BMAD advantage. Our results suggest the importance of plane-specific vertebral geometric adaptation to mechanical loading during growth. Paired scan output provides a more accurate assessment of this adaptation than pa or lat plane scans alone.

Agreement between pQCT- and DXA-derived indices of bone geometry, density, and theoretical strength in females of varying age, maturity, and physical activity.

Measurement of bone mass, geometry, density, and strength are critical in bone research and clinical studies. For peripheral quantitative computed tomography (pQCT), single and repeated measurements are particularly adversely affected by movement and positional variation. Dual‐energy X‐ray absorptiometry (DXA)–derived indices may alleviate these problems and provide useful alternative assessments. To evaluate this hypothesis, distal radius DXA and pQCT indices were compared in 101 healthy females aged 8.0 to 22.8 years (prepuberty to adulthood), reflecting a broad range of body sizes, physical maturity, and activity exposures. At the diaphysis, correlations were ρ = +0.74 to +0.98, with strong intermethod agreement for most indices. At the metaphysis, correlations were ρ = +0.64 to +0.97; intermethod agreement improved with modifications to the simplified geometric formulas more closely reflecting metaphyseal bone geometry. Further improvements may be possible because skeletal size and maturity‐related biases in agreement were detected. Overall, DXA‐derived indices may provide a useful assessment of bone geometry, density, and theoretical strength contingent on appropriate consideration of their limitations.

Distal Radius Strength: A Comparison of DXA-Derived vs pQCT-Measured Parameters in Adolescent Females

Although quantitative computed tomography (QCT) is considered the gold standard for in vivo densitometry, dual-energy X-ray absorptiometry (DXA) scans assess larger bone regions and are more appropriate for pediatric longitudinal studies. Unfortunately, DXA does not yield specific bone architectural output. To address this issue in healthy, postmenarcheal girls, Sievänens distal radius formulae [1996] were applied to derive indices of bone geometry, volumetric bone mineral density (vBMD), and strength from DXA data; results were compared to peripheral quantitative computed tomography (pQCT) output. Contemporaneous scans were performed on the left, distal radii of 35 gymnasts, ex-gymnasts, and nongymnasts (aged 13.3-20.4 yr, mean 16.6 yr). For 4% and 33% regions, pQCT measured cross-sectional areas (CSAs) and vBMD; comparable DXA indices were generated at ultradistal and 1/3 regions. Index of structural strength in axial compression was calculated from 4% pQCT and DXA output for comparison; 33% pQCT strength-strain index was compared to 1/3 DXA section modulus. Sievänen DXA indices were significantly, positively correlated with pQCT output (R=+0.61 to +0.98; p<0.0001). At the distal radius, in healthy postmenarcheal girls, Sievänens method yielded potentially useful DXA indices of diaphyseal cortical CSA and bone strength at both the diaphysis (section modulus) and the metaphysis (index of structural strength in axial compression).

Correcting Fan-Beam Magnification in Clinical Densitometry Scans of Growing Subjects

As children grow, body and limb girths increase. For serial densitometric measurements, growth increases the distance between the bone region of interest and X-ray source over time, thereby increasing fan-beam magnification. To isolate bone accrual from magnification error in growing subjects, we developed a correction method based on waist girth, a common anthropometric measure. This correction was applied to dual-energy X-ray absorptiometry output obtained in a cohort of premenarcheal gymnasts and nongymnasts. After correcting for magnification, results for projected area and bone mineral content (BMC) increased by 0.4-1.1% at the lumbar spine and 8-16% at the femoral neck, decreasing areal bone mineral density (aBMD) by 0.4-2.3% at both sites. The effects of magnification correction were similar in magnitude to BMC and aBMD gains previously reported in longitudinal studies of normoactive children. Because of body size differences, the effect of correction for BMC and aBMD was 10-20% greater in nongymnasts than in gymnasts, which increased the observed aBMD differential between gymnasts and nongymnasts. Fan-beam magnification distorts true changes in bone mineral measures in growing premenarcheal girls and, therefore, may obscure additional activity-related changes during growth. Our correction technique may enhance detection of skeletal adaptation, particularly in pediatric populations.

Site-specific, adult bone benefits attributed to loading during youth: A preliminary longitudinal analysis.

We examined site-specific bone development in relation to childhood and adolescent artistic gymnastics exposure, comparing up to 10years of prospectively acquired longitudinal data in 44 subjects, including 31 non-gymnasts (NON) and 13 gymnasts (GYM) who participated in gymnastics from pre-menarche to ≥1.9years post-menarche. Subjects underwent annual regional and whole-body DXA scans; indices of bone geometry and strength were calculated. Anthropometrics, physical activity, and maturity were assessed annually, coincident with DXA scans. Non-linear mixed effect models centered growth in bone outcomes at menarche and adjusted for menarcheal age, height, and non-bone fat-free mass to evaluate GYM-NON differences. A POST-QUIT variable assessed the withdrawal effect of quitting gymnastics. Curves for bone area, mass (BMC), and strength indices were higher in GYM than NON at both distal radius metaphysis and diaphysis (p<0.0001). At the femoral neck, greater GYM BMC (p<0.01), narrower GYM endosteal diameter (p<0.02), and similar periosteal width (p=0.09) yielded GYM advantages in narrow neck cortical thickness and buckling ratio (both p<0.001; lower BR indicates lower fracture risk). Lumbar spine and sub-head BMC were greater in GYM than NON (p<0.036). Following gymnastics cessation, GYM slopes increased for distal radius diaphysis parameters (p≤0.01) and for narrow neck BR (p=0.02). At the distal radius metaphysis, GYM BMC and compressive strength slopes decreased, as did slopes for lumbar spine BMC, femoral neck BMC, and narrow neck cortical thickness (p<0.02). In conclusion, advantages in bone mass, geometry, and strength at multiple skeletal sites were noted across growth and into young adulthood in girls who participated in gymnastics loading to at least 1.9years post-menarche. Following gymnastics cessation, advantages at cortical bone sites improved or stabilized, while advantages at corticocancellous sites stabilized or diminished. Additional longitudinal observation is necessary to determine whether residual loading benefits enhance lifelong skeletal strength.

Subclinical atherosclerotic risk in endurance-trained premenopausal amenorrheic women.

PURPOSE In premenopausal women, amenorrhea contributes to endothelial dysfunction. It is unknown whether this vascular functional change is associated with vascular structural change. METHODS This study examined regional and systemic vascular structure and function to gain insight into subclinical atherosclerotic risk in 10 amenorrheic athletes, 18 eumenorrheic athletes, and 15 recreationally active controls. Brachial flow-mediated dilation (FMD) and low flow mediated constriction (L-FMC) were used to measure global endothelial function. Carotid-femoral pulse wave velocity (PWV) was used to measure aortic stiffness. Doppler-ultrasound of the superficial femoral artery (SFA) was used to assess intima-media thickness (IMT) and vessel diameter as indicators of vascular remodeling. RESULTS Amenorrheic athletes had significantly lower brachial FMD adjusted for shear stimulus (6.9 ± 1.3%) compared with eumenorrheic athletes (11.0 ± 1.0%) and controls (11.0 ± 1.1%, p = 0.05). Brachial L-FMC (-1.8 ± 4.3%) and aortic PWV (5.0 ± 1.0 m/s) of amenorrheic athletes were similar to those of eumenorrheic athletes (L-FMC, -1.6 ± 4.6%; PWV, 4.6 ± 0.5 m/s) and controls (L-FMC, -1.5 ± 2.8%, p = 0.98; PWV, 5.4 ± 0.7 m/s, p = 0.15). SFA diameters were similar in amenorrheic athletes (5.7 ± 0.7 mm) and eumenorrheic athletes (5.7 ± 0.7 mm), but amenorrheic athletes had larger SFA diameters compared with controls (5.1 ± 0.6 mm, p = 0.04). In amenorrheic athletes, SFA IMT (0.31 ± 0.03 mm) was similar to that of eumenorrheic athletes (0.35 ± 0.07 mm) but significantly thinner compared to that of controls (0.38 ± 0.06, p = 0.01). CONCLUSION Vascular dysfunction in female amenorrheic athletes is not systemic. Parenthetically, amenorrhea may not prevent favorable peripheral vascular structural adaptations to habitual exercise training.

The influence of organized physical activity (including gymnastics) on young adult skeletal traits: Is maturity phase important?

We prospectively evaluated adolescent organized physical activity (PA) as a factor in adult female bone traits. Annual DXA scans accompanied semiannual records of anthropometry, maturity, and PA for 42 participants in this preliminary analysis (criteria: appropriately timed DXA scans at ~1 year premenarche [predictor] and ~5 years postmenarche [dependent variable]). Regression analysis evaluated total adolescent interscan PA and PA over 3 maturity subphases as predictors of young adult bone outcomes: 1) bone mineral content (BMC), geometry, and strength indices at nondominant distal radius and femoral neck; 2) subhead BMC; 3) lumbar spine BMC. Analyses accounted for baseline gynecological age (years pre- or postmenarche), baseline bone status, adult body size and interscan body size change. Gymnastics training was evaluated as a potentially independent predictor, but did not improve models for any outcomes (p > .07). Premenarcheal bone traits were strong predictors of most adult outcomes (semipartial r2 = .21-0.59, p ≤ .001). Adult 1/3 radius and subhead BMC were predicted by both total PA and PA 1-3 years postmenarche (p < .03). PA 3-5 years postmenarche predicted femoral narrow neck width, endosteal diameter, and buckling ratio (p < .05). Thus, participation in organized physical activity programs throughout middle and high school may reduce lifetime fracture risk in females.

Muscle function, dynamic loading, and femoral neck structure in pediatric females.

PURPOSE Muscle forces influence the development of bone mass and structure, but dynamic loading via impact exercise is considered particularly osteogenic. We hypothesized that indices of local muscle function and physical activity exposure would predict femoral neck (FN) structure in premenarcheal females. METHODS We tested this hypothesis in 76 healthy, premenarcheal girls (46 gymnasts and 30 nongymnasts). Height, weight, Tanner breast stage, and prior year nonaquatic, organized physical activity level (PAL) were recorded semiannually. Hologic dual-energy x-ray absorptiometry scans (whole body, left FN) yielded total body nonbone lean mass and bone outcomes, including narrow neck (NN) hip structural analysis data. Dynamometers assessed nondominant hand grip and left hip flexion/extension indices. Parsimonious regression models tested the following as predictors of bone outcomes: local muscle function, PAL, gymnast status, and lean mass, accounting for Tanner breast stage and height, as appropriate. RESULTS Hip flexion indices were significantly correlated with indices of FN mass, density, structure, and strength (P < 0.05). However, the entry of PAL, gymnast status, and lean mass into regression models supplanted local muscle function explanatory value. In contrast, for many variables, the significant association of gymnast status persisted after accounting for physical maturity, body size/lean mass, and PAL. For all skeletal indices except FNArea, NNwidth, NN endosteal diameter, and NN buckling ratio, gymnast status was more strongly associated with bone outcomes than PAL. CONCLUSIONS Greater activity doses and exposure to extreme dynamic loading provide independent benefits to FN structure during growth. Furthermore, weight-bearing activity and high-impact exercise exposure appear superior to local muscle force measures for prediction of FN structure.

Cross-Calibrated Dual-Energy X-Ray Absorptiometry Scanners Demonstrate Systematic Bias in Pediatric and Young Adult Females

Consistency of dual-energy X-ray absorptiometry (DXA) scan results is critical for data integrity. For pediatric subjects, the extent to which cross-calibration of DXA scanners alleviates model-to-model scanner differences is unclear. In the current study, DXA bone outcomes were compared for same-day measurements performed using different scanners, cross-calibrated to alleviate discrepancies (Hologic; Discovery A [DISCO] and QDR 4500W [QDR]). Interscanner differences were evaluated in approximately 130 females aged 8-24 yr. Scans were performed in a single session on both QDR and DISCO scanners to compare projected area, bone mineral content, and areal bone mineral density (BMD) outputs for the whole body (total, subhead, head, arm, and leg), forearm (1/3 and ultradistal radius), lumbar spine (vertebra L3 and L1-L4), and proximal femur (femoral neck). Paired t tests evaluated interscanner differences; concordance correlation coefficients (CCCs) evaluated interscanner correlations. Root mean square error coefficients of variation were compared to same-day duplicate DISCO scan root mean square error coefficients of variation for approximately 30 adult females. Deming regression equations were generated for conversion of QDR to DISCO results and vice versa. Interscanner correlations were very high (95% confidence interval for CCC > 0.90), for all outcomes except for femoral neck area and subhead area (95% confidence interval for CCC = 0.83-0.94, 0.57-073). However, QDR values were systematically lower than Discovery values (p < 0.05), except for head area, head bone mineral content, head BMD, ultradistal BMD (QDR > Discovery, p ≤ 0.05) and L1-L4 area, L3 area, and femoral neck BMD (no differences). Most Bland-Altman and Deming regression plots indicated good interscanner agreement, with little systematic variation based on bone or body size. In pediatric and young adult females, subtle but systematic differences were noted between scans obtained on DISCO and QDR scanners, despite cross-calibration, such that most outcomes are systematically higher for DISCO than for QDR. The use of conversion equations is warranted.