Distal radius microstructure and finite element bone strain are related to site-specific mechanical loading and areal bone mineral density in premenopausal women

Megan E Mancuso, Joshua E Johnson, Sabahat S Ahmed, Tiffiny A Butler, Karen L Troy, Megan E Mancuso, Joshua E Johnson, Sabahat S Ahmed, Tiffiny A Butler, Karen L Troy

Abstract

While weight-bearing and resistive exercise modestly increases aBMD, the precise relationship between physical activity and bone microstructure, and strain in humans is not known. Previously, we established a voluntary upper-extremity loading model that assigns a person's target force based on their subject-specific, continuum FE-estimated radius bone strain. Here, our purpose was to quantify the inter-individual variability in radius microstructure and FE-estimated strain explained by site-specific mechanical loading history, and to determine whether variability in strain is captured by aBMD, a clinically relevant measure of bone density and fracture risk. Seventy-two women aged 21-40 were included in this cross-sectional analysis. High resolution peripheral quantitative computed tomography (HRpQCT) was used to measure macro- and micro-structure in the distal radius. Mean energy equivalent strain in the distal radius was calculated from continuum finite element models generated from clinical resolution CT images of the forearm. Areal BMD was used in a nonlinear regression model to predict FE strain. Hierarchical linear regression models were used to assess the predictive capability of intrinsic (age, height) and modifiable (body mass, grip strength, physical activity) predictors. Fifty-one percent of the variability in FE bone strain was explained by its relationship with aBMD, with higher density predicting lower strains. Age and height explained up to 31.6% of the variance in microstructural parameters. Body mass explained 9.1% and 10.0% of the variance in aBMD and bone strain, respectively, with higher body mass indicative of greater density. Overall, results suggest that meaningful differences in bone structure and strain can be predicted by subject characteristics.

Keywords: Bone QCT; Bone adaptation; Finite element model; HRpQCT; Physical activity.

Figures

Fig. 1
Fig. 1
Flow diagram describing recruitment, screening, and enrollment.
Fig. 2
Fig. 2
a) Representative forearm DXA scan including ultradistal (UD), Middle (MID) and 1/3 regions, and b) distal radius HRpQCT scan (scale bar 5 mm). c) Three-dimensional continuum FE model used to estimate energy equivalent strain (ε¯) within the HRpQCT scanned region.
Fig. 3
Fig. 3
Mean energy equivalent strain within the ultradistal region matching the volume scanned with HRpQCT versus areal bone mineral density measured using DXA within the standard ultradistal site.

References

    1. Ackerman K.E., Putman M., Guereca G., Taylor A.P., Pierce L., Herzog D.B., Klibanski A., Bouxsein M., Misra M. Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone. 2012;51:680–687.
    1. Babatunde O.O., Forsyth J.J., Gidlow C.J. A meta-analysis of brief high-impact exercises for enhancing bone health in premenopausal women. Osteoporos. Int. 2012;23:109–119.
    1. Bailey R.L., Dodd K.W., Goldman J.A., Gahche J.J., Dwyer J.T., Moshfegh A.J., Sempos C.T., Picciano M.F. Estimation of total usual calcium and vitamin D intakes in the United States 1–3. J. Nutr. 2010:817–822.
    1. Baird Pat. Getting Enough Calcium? Patient Calcium Questionnaire. 2018. Available online:
    1. Balogun J.A., Akinloye A.A., Adenlola S.A. Grip strength as a function of age, height, body weight and quetelet index. Physiother. Theory Pract. 1991;7:111–119.
    1. Bass S., Pearce G., Bradney M., Hendrich E., Delmas P.D., Harding A., Seeman E. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J. Bone Miner. Res. 1998;13:500–507.
    1. Bhatia V.A., Edwards W.B., Troy K.L. Predicting surface strains at the human distal radius during an in vivo loading task - finite element model validation and application. J. Biomech. 2014;47:2759–2765.
    1. Bhatia V.A., Brent Edwards W., Johnson J.E., Troy K.L. Short-term bone formation is greatest within high strain regions of the human distal radius: a prospective pilot study. J. Biomech. Eng. 2015;137:11001-1–5.
    1. Buie H.R., Campbell G.M., Klinck R.J., MacNeil J.A., Boyd S.K. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone. 2007;41:505–515.
    1. Burghardt A.J., Kazakia G.J., Ramachandran S., Link T.M., Majumdar S. Age and gender related differences in the geometric properties and biomechanical significance of intra-cortical porosity in the distal radius and tibia. J. Bone Miner. Res. 2009;25:983–993.
    1. Burghardt A.J., Buie H.R., Laib A., Majumdar S., Boyd S.K. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. 2010;47:519–528.
    1. Burt L.A., Macdonald H.M., Hanley D.A., Boyd S.K. Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch. Osteoporos. 2014;9
    1. Cosman F., de Beur S.J., LeBoff M.S., Lewiecki E.M., Tanner B., Randall S., Lindsay R. Clinician's guide to prevention and treatment of osteoporosis. Osteoporos. Int. 2014;25:2359–2381.
    1. Courteix D., Lespessailles E., Peres S.L., Obert P., Germain P., Benhamou C.L. Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteoporos. Int. 1998;8:152–158.
    1. Court-Brown C.M., Caesar B. Epidemiology of adult fractures: a review. Injury. 2006;37:691–697.
    1. Daly R.M., Bass S.L. Lifetime sport and leisure activity participation is associated with greater bone size, quality and strength in older men. Osteoporos. Int. 2006;17:1258–1267.
    1. Dolan S.H., Williams D.P., Ainsworth B.E., Shaw J.M. Development and reproducibility of the bone loading history questionnaire. Med. Sci. Sports Exerc. 2006;38:1121–1131.
    1. Dowthwaite J.N., Dunsmore K.A., Gero N.M., Burzynski A.O., Sames C.A., Rosenbaum P.F., Scerpella T.A. Arm bone loading index predicts DXA musculoskeletal outcomes in two samples of post-menarcheal girls. J. Musculoskelet. Neuronal Interact. 2015;15:358–371.
    1. Edwards M.H., Robinson D.E., Ward K.A., Javaid M.K., Walker-Bone K., Cooper C., Dennison E.M. Cluster analysis of bone microarchitecture from high resolution peripheral quantitative computed tomography demonstrates two separate phenotypes associated with high fracture risk in men and women. Bone. 2016;88:131–137.
    1. Felson D.T., Zhang Y., Hannan M.T., Anderson J.J. Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J. Bone Miner. Res. 1993;8:567–573.
    1. Földhazy Z., Arndt A., Milgrom C., Finestone A., Ekenman I. Exercise-induced strain and strain rate in the distal radius. J. Bone Joint Surg. Br. 2005;87–b:261–266.
    1. Ghasem-Zadeh A., Burghardt A., Wang X.F., Iuliano S., Bonaretti S., Bui M., Zebaze R., Seeman E. Quantifying sex, race, and age specific differences in bone microstructure requires measurement of anatomically equivalent regions. Bone. 2017;101:206–213.
    1. Gjesdal C.G., Halse J.I., Eide G.E., Brun J.G., Tell G.S. Impact of lean mass and fat mass on bone mineral density: the Hordaland health study. Maturitas. 2008;59:191–200.
    1. Gnudi S., Sitta E., Fiumi N. Relationship between body composition and bone mineral density in women with and without osteoporosis: relative contribution of lean and fat mass. J. Bone Miner. Metab. 2007;25:326–332.
    1. Greenway K.G., Walkley J.W., Rich P.A. Relationships between self-reported lifetime physical activity, estimates of current physical fitness, and aBMD in adult premenopausal women. Arch. Osteoporos. 2015;10
    1. Hambli R. Micro-CT finite element model and experimental validation of trabecular bone damage and fracture. Bone. 2013;56:363–374.
    1. Hasegawa Y., Schneider P., Reiners C. Age, sex, and grip strength determine architectural bone parameters assessed by peripheral quantitative computed tomography (pQCT) at the human radius. J. Biomech. 2001;34:497–503.
    1. Helgason B., Perilli E., Schileo E., Taddei F., Brynjólfsson S., Viceconti M. Mathematical relationships between bone density and mechanical properties: a literature review. Clin. Biomech. 2008;23:135–146.
    1. Ho A.Y.Y., Kung A.W.C. Determinants of peak bone mineral density and bone area in young women. J. Bone Miner. Metab. 2005;23:470–475.
    1. Hsieh Y.F., Turner C.H. Effects of loading frequency on mechanically induced bone formation. J. Bone Miner. Res. 2001;16:918–924.
    1. James M.M.S., Carroll S. Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. J. Bone Miner. Metab. 2010;28:251–267.
    1. Janz K.F., Thomas D.Q., Ford M.A., Williams S.M. Top 10 research questions related to physical activity and bone health in children and adolescents. Res. Q. Exerc. Sport. 2015;86:5–12.
    1. Johnson J.E., Troy K.L. Validation of a new multiscale finite element analysis approach at the distal radius. Med. Eng. Phys. 2017;44:16–24.
    1. Kato T., Yamashita T., Mizutani S., Honda A., Matumoto M., Umemura Y. Adolescent exercise associated with long-term superior measures of bone geometry: a cross-sectional DXA and MRI study. Br. J. Sports Med. 2009;43:932–935.
    1. Kelley G.A., Kelley K.S., Kohrt W.M. Exercise and bone mineral density in premenopausal women: a meta-analysis of randomized controlled trials. Int. J. Endocrinol. 2013;2013
    1. Laib A., Hauselmann H.J., Ruegsegger P. In vivo high resolution 3D-QCT of the human forearm. Technol. Health Care. 1998;6:329–337.
    1. Lambers F.M., Kuhn G., Weigt C., Koch K.M., Schulte F.A., Müller R. Bone adaptation to cyclic loading in murine caudal vertebrae is maintained with age and directly correlated to the local micromechanical environment. J. Biomech. 2015;48:1179–1187.
    1. Lanyon L.E., Hampson W.G.J., Goodship A.E., Shah J.S. Bone deformation recorded in vivo from strain gauges attached to the human Tibial shaft. Acta Orthop. Scand. 1975;46:256–268.
    1. Lespessailles E., Hambli R., Ferrari S. Osteoporosis drug effects on cortical and trabecular bone microstructure: a review of HR-pQCT analyses. Bonekey Rep. 2016;5:1–8.
    1. Lorbergs A.L., Farthing J.P., Baxter-Jones A.D.G., Kontulainen S.A. Forearm muscle size, strength, force, and power in relation to pQCT-derived bone strength at the radius in adults. Appl. Physiol. Nutr. Metab. 2011;36:618–625.
    1. Lou Bareither M., Troy K.L., Grabiner M.D. Bone mineral density of the proximal femur is not related to dynamic joint loading during locomotion in young women. Bone. 2006;38:125–129.
    1. MacKelvie K.J., Khan K.M., McKay H.A. Is there a critical period for bone response to weight-bearing exercise in children and adolescents? A systematic review. Br. J. Sports Med. 2002;36:250–257. doi: 10.1136/bjsm.36.4.250. discussion 257.
    1. MacNeil J.A., Boyd S.K. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med. Eng. Phys. 2007;29:1096–1105.
    1. Martyn-St James M., Carroll S. Progressive high-intensity resistance training and bone mineral density changes among premenopausal women. Sports Med. 2006;36:683–704.
    1. Massy-Westropp N.M., Gill T.K., Taylor A.W., Bohannon R.W., Hill C.L. Hand grip strength: age and gender stratified normative data in a population-based study. BMC. Res. Notes. 2011;4:127.
    1. Morgan E.F., Bayraktar H.H., Keaveny T.M. Trabecular bone modulus-density relationships depend on anatomic site. J. Biomech. 2003;36:897–904.
    1. Morin S., Tsang J.F., Leslie W.D. Weight and body mass index predict bone mineral density and fractures in women aged 40 to 59 years. Osteoporos. Int. 2009;20:363–370.
    1. Nikander R., Kannus P., Rantalainen T., Uusi-Rasi K., Heinonen A., Sievänen H. Cross-sectional geometry of weight-bearing tibia in female athletes subjected to different exercise loadings. Osteoporos. Int. 2010;21:1687–1694.
    1. Nilsson M., Ohlsson C., Sundh D., Mellström D., Lorentzon M. Association of physical activity with trabecular microstructure and cortical bone at distal tibia and radius in young adult men. J. Clin. Endocrinol. Metab. 2010;95:2917–2926.
    1. Nilsson M., Ohlsson C., Mellström D., Lorentzon M. Sport-specific association between exercise loading and the density, geometry, and microstructure of weight-bearing bone in young adult men. Osteoporos. Int. 2013;24:1613–1622.
    1. Nishiyama K.K., Macdonald H.M., Buie H.R., Hanley D.A., Boyd S.K. Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J. Bone Miner. Res. 2009;25:882–890.
    1. Pasanen M., Kontulainen S., Kannus P., Haapasalo H., Sieva H. Vol. 16. 2001. Good Maintenance of Exercise-Induced Bone Gain with Decreased Training of Female Tennis and Squash Players: a Prospective 5-Year Follow-Up Study of Young and Old Starters and Controls; pp. 195–201.
    1. Pialat J.B., Burghardt A.J., Sode M., Link T.M., Majumdar S. Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone. 2012;50:111–118.
    1. Rubin C.T., Lanyon L.E. Regulation of bone formation by applied dynamic loads. J. Bone Joint Surg. 1984;66A:397–402.
    1. Rubin C.T., Lanyon L.E. Regulation of bone mass by mechanical strain magnitude. Calcif. Tissue Int. 1985;37:411–417.
    1. Rubin L.A., Hawker G.A., Peltekova V.D., Fielding L.J., Ridout R., Cole D.E. Determinants of peak bone mass: clinical and genetic analyses in a young female Canadian cohort. J. Bone Miner. Res. 1999;14:633–643.
    1. Scerpella T.A., Bernardoni B., Wang S., Rathouz P.J., Li Q., Dowthwaite J.N. Site-specific, adult bone benefits attributed to loading during youth: a preliminary longitudinal analysis. Bone. 2016;85:148–159.
    1. Schipilow J.D., Macdonald H.M., Liphardt A.M., Kan M., Boyd S.K. Bone micro-architecture, estimated bone strength, and the muscle-bone interaction in elite athletes: an HR-pQCT study. Bone. 2013;56:281–289.
    1. Sornay-Rendu E., Boutroy S., Duboeuf F., Chapurlat R.D. Bone microarchitecture assessed by HR-pQCT as predictor of fracture risk in postmenopausal women: the OFELY study. J. Bone Miner. Res. 2017;32:1243–1251.
    1. Stein E.M., Liu X.S., Nickolas T.L., Cohen A., Thomas V., McMahon D.J., Zhang C., Yin P.T., Cosman F., Nieves J., Guo X.E., Shane E. Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J. Bone Miner. Res. 2010;25:2296–2305.
    1. Troy K.L., Edwards W.B., Bhatia V.A., Lou Bareither M. In vivo loading model to examine bone adaptation in humans: a pilot study. J. Orthop. Res. 2013;31:1406–1413.
    1. Umemura Y., Ishiko T., Yamauchi T., Kurono M., Mashiko S. Five jumps per day increase bone mass and breaking force in rats. J. Bone Miner. Res. 1997;12:1480–1485.
    1. Warden S.J., Fuchs R.K., Turner C.H. Steps for targeting exercise towards the skeleton to increase bone strength. Eura. Medicophys. 2004;40:223–232.
    1. Webster D., Schulte F.A., Lambers F.M., Kuhn G., Müller R. Strain energy density gradients in bone marrow predict osteoblast and osteoclast activity: a finite element study. J. Biomech. 2015;48:866–874.
    1. Weeks B.K., Beck B.R. The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos. Int. 2008;19:1567–1577.
    1. Wong S.L. 2016. Grip Strength Reference Values for Canadians Aged 6 to 79: Canadian Health Measures Survey, 2007 to 2013.

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