Agreement Between Dual-Energy X-Ray Absorptiometry and Quantitative Ultrasound to Evaluate Bone Health in Adolescents: The PRO-BONE Study

in Pediatric Exercise Science
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Purpose: The present study aims to investigate the association between dual-energy X-ray absorptiometry (DXA) and quantitative ultrasound (QUS) parameters and the intermethods agreement in active males. Methods: In this cross-sectional study, bone health (by DXA and calcaneal QUS), physical activity (by accelerometers), and anthropometrics measurements were assessed in 117 active adolescents (12–14 y old). Bivariate correlation coefficients were calculated to assess the relationships between DXA standard regions of interest and QUS parameters. Intraclass correlation coefficients and Bland–Altman plots were used to assess the level of agreement between bone mineral content regions derived from DXA and stiffness index. The measurements were z score transformed for comparison. Results: Most QUS parameters were positive and significantly correlated with DXA outcomes (stiffness index: r = .43–.52; broadband ultrasound attenuation: r = .50–.58; speed of sound: r = .25–.27) with the hip showing the highest correlations. Moreover, the present study found fair to good intraclass correlation coefficients of agreement (.60–.68) between DXA and QUS to assess bone health. The Bland–Altman analysis showed a limited percentage of outliers (3.2%–8.6%). Conclusion: QUS device could represent an acceptable alternative method to assess bone health in active adolescent males.

Torres-Costoso and Ferri-Morales are with the School of Nursing and Physiotherapy, University of Castilla-La Mancha, Toledo, Spain. Vlachopoulos, Ubago-Guisado, and Gracia-Marco are with the Children’s Health and Exercise Research Centre, Sport and Health Sciences, University of Exeter, Exeter, United Kingdom. Ubago-Guisado is also with the IGOID Research Group, University of Castilla-La Mancha, Toledo, Spain. Cavero-Redondo and Martínez-Vizcaino are with the Health and Social Research Center, University of Castilla-La Mancha, Cuenca, Spain. Martínez-Vizcaino is also with the Faculty of Health Sciences, Autonomous University of Chile, Talca, Chile. Gracia-Marco is also with the Growth, Exercise, Nutrition and Development Research Group, University of Zaragoza, Zaragoza, Spain; and PROFITH “PROmoting FITness and Health through physical activity” Research Group, Dept. of Physical Education and Sports, Faculty of Sport Sciences, University of Granada, Granada, Spain.

Address author correspondence to Ana Torres-Costoso at AnaIsabel.Torres@uclm.es.
  • 1.

    Baroncelli GI. Quantitative ultrasound methods to assess bone mineral status in children: technical characteristics, performance, and clinical application. Pediatr Res. 2008;63(3):220–8. doi:10.1203/PDR.0b013e318163a286

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Baxter-Jones ADG, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26(8):1729–39. PubMed doi:10.1002/jbmr.412

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Bilsborough JC, Greenway K, Opar D, Livingstone S, Cordy J, Coutts AJ. The accuracy and precision of DXA for assessing body composition in team sport athletes. J Sports Sci. 2014;32(19):1821–8. PubMed doi:10.1080/02640414.2014.926380

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Chong KH, Poh BK, Jamil NA, Kamaruddin NA, Deurenberg P. Radial quantitative ultrasound and dual energy x-ray absorptiometry: intermethod agreement for bone status assessment in children. BioMed Res Int. 2015;2015:232876. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Crabtree NJ, Arabi A, Bachrach LK, et al. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD pediatric official positions. J Clin Densitom. 2014;17(2):225–42. PubMed doi:10.1016/j.jocd.2014.01.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Davies JH, Evans BA, Gregory JW. Bone mass acquisition in healthy children. Arch Dis Child. 2005;90(4):373–8. PubMed doi:10.1136/adc.2004.053553

  • 7.

    Euser AM, Dekker FW, le Cessie S. A practical approach to Bland-Altman plots and variation coefficients for log transformed variables. J Clin Epidemiol. 2008;61(10):978–82. PubMed doi:10.1016/j.jclinepi.2007.11.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Gracia-Marco L, Moreno LA, Ortega FB, et al. Levels of physical activity that predict optimal bone mass in adolescents: the HELENA study. Am J Prev Med. 2011;40(6):599–607. PubMed doi:10.1016/j.amepre.2011.03.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Grampp S, Henk C, Lu Y, et al. Quantitative US of the calcaneus: cutoff levels for the distinction of healthy and osteoporotic individuals. Radiology. 2001;220(2):400–5. PubMed doi:10.1148/radiology.220.2.r01au05400

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Grampp S, Henk CB, Fuerst TP, et al. Diagnostic agreement of quantitative sonography of the calcaneus with dual X-ray absorptiometry of the spine and femur. Am J Roentgenol. 1999;173(2):329–34. doi:10.2214/ajr.173.2.10430129

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Hadji P, Hars O, Wuster C, et al. Stiffness index identifies patients with osteoporotic fractures better than ultrasound velocity or attenuation alone. Maturitas. 1999;31(3):221–6. PubMed doi:10.1016/S0378-5122(99)00003-1

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    He YQ, Fan B, Hans D, et al. Assessment of a new quantitative ultrasound calcaneus measurement: precision and discrimination of hip fractures in elderly women compared with dual X-ray absorptiometry. Osteoporos Int. 2000;11(4):354–60. PubMed doi:10.1007/s001980070125

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Jaworski M, Lebiedowski M, Lorenc RS, Trempe J. Ultrasound bone measurement in pediatric subjects. Calcif Tissue Int. 1995;56(5):368–71. PubMed doi:10.1007/BF00301604

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Langton CM, Langton DK. Comparison of bone mineral density and quantitative ultrasound of the calcaneus: site-matched correlation and discrimination of axial BMD status. Br J Radiol. 2000;73(865):31–5. doi:10.1259/bjr.73.865.10721317

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Marin F, Gonzalez-Macias J, Diez-Perez A, Palma S, Delgado-Rodriguez M. Relationship between bone quantitative ultrasound and fractures: a meta-analysis. J Bone Miner Res. 2006;21(7):1126–35. PubMed doi:10.1359/jbmr.060417

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Moayyeri A, Adams JE, Adler RA, Krieg MA, Hans D, Compston J, Lewiecki EM. Quantitative ultrasound of the heel and fracture risk assessment: an updated meta-analysis. Osteoporos Int. 2012;23(1):143–53. PubMed doi:10.1007/s00198-011-1817-5

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Moayyeri A, Kaptoge S, Dalzell N, et al. Is QUS or DXA better for predicting the 10-year absolute risk of fracture? J Bone Miner Res. 2009;24(7):1319–25. PubMed doi:10.1359/jbmr.090212

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Mughal MZ, Langton CM, Utretch G, Morrison J, Specker BL. Comparison between broad-band ultrasound attenuation of the calcaneum and total body bone mineral density in children. Acta Paediatr. 1996;85(6):663–5. PubMed doi:10.1111/j.1651-2227.1996.tb14119.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Njeh CF, Fuerst T, Hans D, Blake GM, Genant HK. Radiation exposure in bone mineral density assessment. Appl Radiat Isot. 1999;50(1):215–36. PubMed doi:10.1016/S0969-8043(98)00026-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Phillips LR, Parfitt G, Rowlands AV. Calibration of the GENEA accelerometer for assessment of physical activity intensity in children. J Sci Med Sport. 2013;16(2):124–8. PubMed doi:10.1016/j.jsams.2012.05.013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Prins SH, Jorgensen HL, Jorgensen LV, Hassager C. The role of quantitative ultrasound in the assessment of bone: a review. Clin Physiol. 1998;18(1):3–17. PubMed doi:10.1046/j.1365-2281.1998.00067.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Raum K, Grimal Q, Varga P, Barkmann R, Gluer CC, Laugier P. Ultrasound to assess bone quality. Curr Osteoporos Rep. 2014;12(2):154–62. PubMed doi:10.1007/s11914-014-0205-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Rawal J, Eleftheriou K, Skipworth J, et al. Relationship between calcaneal quantitative ultrasound and hip dual energy X-ray absorptiometry in young healthy men. Osteoporos Int. 2012;23(7):1947–56. PubMed doi:10.1007/s00198-011-1853-1

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Rizzoli R, Bianchi ML, Garabédian M, McKay HA, Moreno LA. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46(2):294–305. PubMed doi:10.1016/j.bone.2009.10.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Sandstrom L, McGuigan FE, Callreus M, Akesson KE. Peak bone mass and quantitative ultrasound bone properties in young adulthood: a study in the PEAK-25 cohort of women. J Clin Densitom. 2016;19(4):477–84. PubMed doi:10.1016/j.jocd.2016.03.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Schott AM, Weill-Engerer S, Hans D, Duboeuf F, Delmas PD, Meunier PJ. Ultrasound discriminates patients with hip fracture equally well as dual energy X-ray absorptiometry and independently of bone mineral density. J Bone Miner Res. 1995;10(2):243–9. PubMed doi:10.1002/jbmr.5650100210

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420–8. PubMed doi:10.1037/0033-2909.86.2.420

  • 28.

    Sioen I, Goemare S, Ahrens W, et al. The relationship between paediatric calcaneal quantitative ultrasound measurements and dual energy X-ray absorptiometry (DXA) and DXA with laser (DXL) as well as body composition. Int J Obes. 2011;35 Suppl1:125–30. doi:10.1038/ijo.2011.44

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Stewart A, Reid DM. Quantitative ultrasound in osteoporosis. Semin Musculoskelet Radiol. 2002;6(3):229–32. PubMed doi:10.1055/s-2002-36720

  • 30.

    Tanner JM, Whitehouse RH. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis child. 1976;51(3):170–9. PubMed doi:10.1136/adc.51.3.170

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Torres-Costoso A, Gracia-Marco L, Sanchez-Lopez M, Notario-Pacheco B, Arias-Palencia N, Martinez-Vizcaino V. Physical activity and bone health in schoolchildren: the mediating role of fitness and body fat. PLoS ONE. 2015;10(4):e0123797. PubMed doi:10.1371/journal.pone.0123797

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Trimpou P, Bosaeus I, Bengtsson BA, Landin-Wilhelmsen K. High correlation between quantitative ultrasound and DXA during 7 years of follow-up. Eur J Radiol. 2010;73(2):360–4. doi:10.1016/j.ejrad.2008.11.024

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    van den Bergh JP, Noordam C, Ozyilmaz A, Hermus AR, Smals AG, Otten BJ. Calcaneal ultrasound imaging in healthy children and adolescents: relation of the ultrasound parameters BUA and SOS to age, body weight, height, foot dimensions and pubertal stage. Osteoporos Int. 2000;11(11):967–76. PubMed doi:10.1007/s001980070036

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Vicente-Rodríguez G. How does exercise affect bone development during growth? Sports Med. 2006;36(7):561–9. doi:10.2165/00007256-200636070-00002

  • 35.

    Vicente-Rodriguez G, Ara I, Perez-Gomez J, Serrano-Sanchez JA, Dorado C, Calbet JA. High femoral bone mineral density accretion in prepubertal soccer players. Med Sci Sports Exerc. 2004;36(10):1789–95. PubMed doi:10.1249/01.MSS.0000142311.75866.D7

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Vlachopoulos D, Barker AR, Ubago-Guisado E, et al. The effect of 12-month participation in osteogenic and non-osteogenic sports on bone development in adolescent male athletes. The PRO-BONE study. J Sci Med Sport. 2018;21(4):404–409. PubMed doi:10.1016/j.jsams.2017.08.018

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Vlachopoulos D, Barker AR, Williams CA, Knapp KM, Metcalf BS, Gracia-Marco L. Effect of a program of short bouts of exercise on bone health in adolescents involved in different sports: the PRO-BONE study protocol. BMC Public Health. 2015;15:361. PubMed doi:10.1186/s12889-015-1633-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Wang Q, Nicholson PH, Timonen J, Alen M, Moilanen P, Suominen H, Cheng S. Monitoring bone growth using quantitative ultrasound in comparison with DXA and pQCT. J Clin Densitom. 2008;11(2):295–301. PubMed doi:10.1016/j.jocd.2007.10.003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Weeks BK, Hirsch R, Nogueira RC, Beck BR. Is calcaneal broadband ultrasound attenuation a valid index of dual-energy x-ray absorptiometry-derived bone mass in children? Bone Joint Res. 2016;5(11):538–43. PubMed doi:10.1302/2046-3758.511.BJR-2016-0116.R1

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Wetter AC, Economos CD. Relationship between quantitative ultrasound, anthropometry and sports participation in college aged adults. Osteoporos Int. 2004;15(10):799–806. PubMed doi:10.1007/s00198-004-1607-4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Wilkinson K, Vlachopoulos D, Klentrou P, et al. Soft tissues, areal bone mineral density and hip geometry estimates in active young boys: the PRO-BONE study. Eur J Appl Physiol. 2017;117(4):833–42. PubMed doi:10.1007/s00421-017-3568-2

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Willson T, Nelson SD, Newbold J, Nelson RE, LaFleur J. The clinical epidemiology of male osteoporosis: a review of the recent literature. Clin Epidemiol. 2015;7:65–76. PubMed

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Xu Y, Guo B, Gong J, Xu H, Bai Z. The correlation between calcaneus stiffness index calculated by QUS and total body BMD assessed by DXA in Chinese children and adolescents. J Bone Miner Metab. 2014;32(2):159–66. PubMed doi:10.1007/s00774-013-0474-5

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Yung PS, Lai YM, Tung PY, Tsui HT, Wong CK, Hung VW, Qin L. Effects of weight bearing and non-weight bearing exercises on bone properties using calcaneal quantitative ultrasound. Br J Sports Med. 2005;39(8):547–51. PubMed doi:10.1136/bjsm.2004.014621

    • Crossref
    • Search Google Scholar
    • Export Citation
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