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  Original Article Bone Geometry, Density, and Strength Indices of the Distal RadiusReflect Loading via Childhood Gymnastic Activity  Jodi N. Dowthwaite,*  ,1  Portia P. E. Flowers,  2  J  oseph A. Spadaro, 1  and Tamara A. Scerpella 1 1  Department of Orthopedic Surgery, State University of New York Upstate Medical University, Syracuse, NY;and   2  Department of Biomedical and Chemical Engineering, Syracuse University, Syracuse, NY  Abstract The distal radius bears unique forces during gymnastic activity. Its relatively simple anatomy, minimal soft tissueenvelope, and varied composition make the distal radius ideal for evaluating the effects of loading on bone proper-ties. For 56 premenarcheal gymnasts and nongymnasts, ultradistal and 1/3 distal radius DXA scans measured bonemineral content (BMC), areal bone mineral density, and projected area. Simplified geometric models were used togenerate bone mineral apparent density (BMAD), geometric indices, strength indices, and fall strength ratios. Ratiosof regional BMC vs total body fat-free mass (FFM) were calculated. Separate Tanner I and II analyses of covarianceadjusted bone parameters for age and height. Ratios were compared using maturity-matched analyses of variance. Atthe 1/3 region, periosteal width, BMC, cortical cross-sectional area, and section modulus were greater in gymnaststhan nongymnasts (  p ! 0.05); 1/3 BMAD means were equivalent. Ultradistal BMAD, BMC, and index for struc-tural strength in axial compression were higher in gymnasts than nongymnasts; ultradistal periosteal width wasonly larger in Tanner I gymnasts. Fall strength ratios and BMC/FFM ratios were greater in gymnasts (  p ! 0.05).Geometric and volumetric responses to mechanical loading are site specific during late childhood and earlyadolescence. Key Words:  Bone density; bone size; exercise; growth; gymnasts; radius. Introduction To date, most studies that evaluate the effect of mechanicalloading on bone growth have focused on areal bone mineraldensity (aBMD) and bone mineral content (BMC), ratherthan on bone geometry. When considered, bone size is oftenused solely to adjust for the confounding effects of body sizevariation upon BMC or BMD, rather than as an outcome mea-sure that varies as a function of physical activity. Fewinvestigators have attempted to evaluate bone geometry inresponse to exercise; as a result, limited evidence has beenprovided for an effect of mechanical loading on bone archi-tecture  (1 e 7) . Even fewer studies have demonstrated geomet-ric adaptation to mechanical loading during growth  (8 e 12) .Artistic gymnastics has been studied extensively as a modelfor the skeletal effects of impact loading. Because the uniqueweight-bearing function of the upper extremity in gymnasticsis infrequently duplicated by other activity, the forearm isa particularly useful site for these evaluations. Within theforearm, the radius bears the brunt of impact forces, therebyproviding a specific barometer of impact/weight-bearing ac-tivity experienced during gymnastics. In addition, the radiuscontains regions of bone that are predominantly cortical orpredominantly trabecular, allowing for comparisons of bonetissue-specific responses. Compared to the more complexanatomy of the proximal femur or lumbar spine, the structureof the radius facilitates the use of a simplified model to derivegeometric measures, bone mineral apparent density (BMAD), Received 09/05/06; Revised 10/13/06; Accepted 10/13/06.*Address correspondence to: Jodi N. Dowthwaite, PhD,Department of Orthopedic Surgery, State University of New York Upstate Medical University, 550 Harrison Street, Suite 128, Syracuse,NY 13202. E-mail: 65  Journal of Clinical Densitometry,  vol. 10, no. 1, 65 e 75, 2007   Copyright 2007 by The International Society for Clinical Densitometry1094-6950/07/10:65 e 75/$32.00DOI: 10.1016/j.jocd.2006.10.003  and indices of strength  (13) . Finally, in the distal forearm,there is negligible variation in soft tissue envelope dimen-sions; thus, variation in distance from the X-ray source andresultant fan-beam magnification error are both uniform andminimal  (14) .Many studies have identified higher aBMD in gymnaststhan nongymnasts at the forearm and other weight-bearingsites  (15 e 20) ; only one has explored the relative contribu-tions of geometry and volumetric density  (11) . Previous anal-yses by our group demonstrated significantly higher arealBMD at the forearm in premenarcheal gymnasts relative tomaturity-matched nongymnasts; these differences persistedafter adjustment for age, height, and total body fat-freemass (FFM)  (15) . We hypothesized that variation in aBMDwas due to both geometric and densitometric adaptations toimpact loading, and that the ultradistal (metaphyseal, trabec-ular bone) and 1/3 (diaphyseal, cortical bone) regions of theradius would express these adaptations differently. This studyexpands upon our prior work, reassessing scans from the es-tablished cohort to elucidate geometric, material, and strengthproperties of the ultradistal and 1/3 distal radius in preme-narcheal gymnasts and nongymnasts. Materials and Methods Subjects represent a premenarcheal subset of 56 partici-pants from an ongoing, longitudinal study of female artisticgymnasts and nongymnasts  (15) . At enrollment, all partici-pants (n 5 122) were aged 7 e 12 yr and nongymnasts wereselected to match gymnasts for age and body size. Nongym-nasts were recruited from local grade schools, whereas gym-nasts were recruited from local gymnastics clubs. Prior tostudy initiation, institutional review board approval was pro-vided for the study design, and written informed consentwas obtained from participants and their parents.Participants were included in these analyses if they re-ported self-assessed Tanner stage I (Tanner breast I and Tan-ner pubic I) or Tanner stage II (Tanner breast II and Tannerpubic II) at the time of an annual DXA scan. Non-Caucasiansubjects were excluded from analyses, as there were insuffi-cient numbers to account for racial variation. Gymnastswere included if they trained for at least 6 h/wk in the 2-yrperiod prior to measurement, based upon a previous study (16) . Following these criteria, 28 gymnasts and 28 nongym-nasts were evaluated.All subjects attended semiannual measurement sessionsand completed questionnaires, assessing anthropometry,body composition, calcium intake, and pubertal stage, as pre-viously described  (15) . At these semiannual sessions, weeklyhours of organized physical activity (including gymnastics)were recorded by interview; for most gymnasts, gymnasticstraining was recorded in daily logs. Mean values for physicalactivity and calcium intake were calculated from records forthe year prior to and including the focal DXA scan; these an-nual means were assessed as potential covariates of bone pa-rameters. Pubertal stage and body size covariates werederived from assessments at the focal DXA session.  Bone Measures Fan-beam DXA scans were performed on the distal thirdof the left forearm using a Hologic QDR 4500 W scanner(Hologic Inc., Bedford, MA) and a standardized protocol;the coefficient of variation for the machine was 1%. Datawere included for 2 regions of interest (ROI) in the distal ra-dius: the ultradistal region, composed primarily of trabecularbone, and the 1/3 region, composed primarily of cortical bone( see  Fig. 1). Hologic software (version 9.03D) was also usedto calculate non-bone, FFM, and percentage of body mass asfat (%BF) from whole body scans. Forearm length (cm) wasmeasured from the tip of the ulnar styloid to the tip of theolecranon with a ruler, by the DXA technician.Areal BMD (aBMD, g/cm 2 ), projected area of the ROI(Area ROI , cm 2 ), length of the ROI (  L  ROI , mm), and BMC of the ROI (g) were assessed for the ultradistal and 1/3 regions,separately. Ratio of regional BMC/total body FFM was calcu-lated for each ROI to evaluate regional bone mineral accumu-lation (BMC ROI ) in relation to development of total bodymuscle (total body FFM) and mechanical loading applied dur-ing gymnastics. Mean ultradistal and 1/3 region periostealwidths (mm) were calculated by dividing Area ROI  by  L  ROI , re-spectively. Results of analyses for mean periosteal width,Area ROI , and periosteal cross-sectional area (CSA) were sim-ilar; only periosteal width is reported. ABCD Fig. 1.  DXA regions of interest (ROI) for the distal radius:ultradistal, mid-distal and 1/3. ( A ) Reference line, drawn atthe distal articular surface of the ulnar aspect of the radius.( B ) Ultradistal ROI 5 15.1-mm long (10.1 e 25.2 mm fromthe articular reference line). ( C ) Mid-distal ROI. ( D ) 1/3ROI 5 20.1 e 20.2-mm long, centered at 33% of measuredulna length. 66 Dowthwaite et al.  Journal of Clinical Densitometry Volume 10, 2007   Geometric Models To derive measures of regional geometry and BMAD,models of simplified bone architecture were applied, asdescribed below. Mathematical formulae are detailed inTable 1. Ultradistal Region In children, the ultradistal region is largely comprised of trabecular bone, with a cortical shell so thin that its depth can-not be measured accurately in vivo; therefore, its assessmentis simplified even in peripheral quantitative computed tomog-raphy (pQCT) studies  (21) . As such, the ultradistal region wasmodeled as an elliptical cylinder of uniform volumetricdensity; ‘‘apparent’’ vBMD (BMAD) was calculated usingthe mean periosteal width and BMC of the ROI. To accountfor the elliptical geometry of the ultradistal radius, Sieva¨nenet al. determined that the coefficient  P  approximates thegeneral relationship between bone depth, mean periostealwidth, and p ( P 5 0.8); P is used in computations of volumeand/or CSA for this ROI  (13) . The index for structuralstrength in axial compressive loading, or IBS, was calculatedto assess ultradistal bone strength  (13) . For a more detailedaccount,  see  Table 1. 1/3 Region To derive bone architecture and strength indices, the 1/3region of the radial shaft was treated as a hollow cylinder,with all bone mineral distributed peripherally in a shell of uniform cortical thickness and vBMD. In accordance withthe narrow range of chronological age and maturationalvariation in our sample, calculations used a uniform corti-cal vBMD of 1.01 g/cm 3 ; this value has been reported asa pQCT-measured mean cortical vBMD for Tanner II girlsat the 65% region of the radial shaft  (22) . Furthermore, 1/3cortical vBMD was assumed to be uniform across activitygroups, based upon a pQCT study in which corticalvBMD did not differ between female competitive weight-lifters and controls  (3) . Thus, our simplified model of the1/3 radial shaft holds that: ‘‘periosteal width’’ is equal to‘‘periosteal depth’’; cortical vBMD is constant and equalto 1.01 g/cm 3 ; thickness of the cortical shell is uniform;and all of the bone mineral mass is distributed within thecortical shell.On this basis, we derived variables for the 1/3 region basedupon the formulae of Sieva¨nen et al.  (13) . To assess the cor-tical shell, cortical wall thickness (CWT) and cortical com-partment CSA were calculated. Intramedullary diameter wasderived to assess cortical shell position, relative to the cen-troid. To assess bone strength in response to torsion and bend-ing forces, we derived 2 related indices: section modulus (Z)and cross-sectional moment of inertia (CSMI), respectively.For a true cylinder, polar moment of inertia equals 2   CSMIand indicates torsional strength  (23) . As results are similar,we report only Z. Calculations relied upon the equations of Sieva¨nen et al. and DXA-measured values for BMC, Area ROI ,  L  ROI , and calculated mean periosteal width ( W  ) ( see  Table 1) (13) . Fall Strength Ratios To assess bone strength relative to forces generated bya low trauma fall, we calculated a ratio of bone strength vsthe product of total body weight and a moment arm(weight   forearm length)  (24,25) . These ratios are describedin the literature as ‘‘strength/weight ratios,’’ but we refer tothem as ‘‘fall strength ratios,’’ to avoid confusion  (24) . Fallstrength ratios were calculated using IBS for the ultradistalregion and Z for the 1/3 region. Statistical Analysis The cohort was divided into subgroups based upon matu-rity level (Tanner I and Tanner II) and activity status (gym-nasts and nongymnasts). Comparisons were made betweengymnasts and nongymnasts within each maturity level. Anal-yses of variance (ANOVA) were used to test for significantdifferences between activity groups in age, body size, and cal-cium intake, setting 2-tailed alpha equal to 0.05. Site-specific,between-group differences in ratios of total body FFM/BMCand fall strength ratios were also assessed by ANOVA. Forbone geometry, mass, density and strength variables, analysesof covariance (ANCOVA) were performed to adjust for ageand height. Means, standard deviations, and significancelevels (  p  values) are reported for ANOVA comparisons of subject characteristics. For ANOVA and ANCOVA results,means, 95% confidence intervals, and significance levels arereported.Separate Pearson correlations for gymnasts and nongym-nasts assessed the association between dependent variablesand age, body size, physical activity, and calcium intake.For significant correlations between outcome variables andcalcium intake or physical activity level, partial correlationswere performed to adjust for the effects of age and height.Significant correlation coefficients and  p  values are noted. Results As previously reported in this cohort, gymnasts and non-gymnasts did not differ significantly in age, height, weight,FFM, or calcium intake within either maturity group, al-though Tanner I nongymnasts exhibited higher mean %BFthan Tanner I gymnasts (Table 1)  (15) . Gymnastics participa-tion (h/wk) was significantly higher in Tanner II than Tanner Igymnasts. Based upon exclusion criteria, all gymnasts hadbeen participating in gymnastics for a minimum of 2 yr atgreater than 6 h/wk. Nongymnasts performed a wide rangeof organized physical activities, at variable doses (h/wk).All nongymnasts with at least 5.0 h/wk of weight-bearingactivity played basketball; many also participated in otheractivities, including soccer, lacrosse, and dance. Ultradistal Region Tanner I gymnasts demonstrated significantly highervalues than nongymnasts for all bone outcomes, with differ-ences persisting after ANCOVA adjustment for age andheight (Table 2; Fig. 2A). Similarly, Tanner II gymnasts exhibited higher means for all bone measures, although  Distal Radius Reflects Childhood Gymnastics 67   Journal of Clinical Densitometry Volume 10, 2007   Table 1 Geometric and Bone Strength FormulaeEstimate (units) Description Equation DefinitionsUltradistal BMAD (g/cm 3 ) BMAD, approximatestotal bone vBMDBMAD 5 BMC   L  ROI P   A 2ROI BMAD, bone mineral apparent densityBMC, bone mineral content  L  ROI , length of ROI 5 15.1 mmUltradistal IBS (g 2  /cm 4 ) IBS, incorporatesgeometry and totalbone vBMDIBS 5 BMAD 2   A C orBy algebraic reduction,IBS 5 1 P aBMD 2 P 5 0.8, approximate relation of ultradistalbone width, depth and  p  A c 5 P W  2 (approximate ultradistal CSA)aBMD, areal BMD1/3 BMAD (g/cm 3 ) BMAD, modeledas a cylinderBMAD 5 4BMC   L  ROI p  A 2ROI  A ROI , projected area of ROI  L  ROI , length of ROIBMC, as above1/3 Z (mm 3 ) Z, indexof bending strengthZ 5 BMC2 p r ½ p 2 ð  A ROI  L  ROI Þ 2   BMC r  L  ROI   Z, section modulus r , 1.01 g/cm3 (uniform cortical vBMD)1/3 CWT (mm) CWT for a hollowcylinder of uniformcortical vBMDCWT 5  R    r  orCWT 5  R   ð  R 2  ð  BMC p  r   L  ROI ÞÞ 1 = 2 Periosteal radius,  R 5 12  A ROI  L  ROI Endosteal radius,  r  5 ð  R 2  ð  BMC p  r   L  ROI ÞÞ 1 = 2 r 5 1.01 g/cm 3 1/3 Cortical CSA (mm 2 ) CSA of uniformcortical shell, resistanceto load in axialcompressionCSA 5 ð p   CWT Þð W     CWT Þ  CSA 5 cross-sectional areaCWT 5 cortical wall thickness W  5 mean periosteal width,  W  5  A ROI  L  ROI 1/3 Intramedullarydiameter (mm)Double the radiusof the endosteal cavityIntramedullary diameter 5 2 r  2 r  5 W   2CWTCWT 5 cortical wall thickness r  5 radius of the endosteal cavity W  5 mean periosteal width,  W  5  A ROI  L  ROI Fall-strength ratios For 1/3 and ultradistalregions, indicativeof strength underforce of low trauma fall1 = 3 5  Z W  t   L  FOREARM Ultradistal 5  IBS W  t   L  FOREARM  Z  5 1/3 strength indexIBS 5 ultradistal strength index W  t 5 total body mass  L  FOREARM 5 ulna length (moment arm)  J   o ur  n a l    o  f    C l    i    n i    c a l   D e n s  i    t   o m e t  r   y V  o l    u m e1   0   ,2   0   0   7 


Aug 1, 2017
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