Osteoporosis International

, Volume 22, Issue 8, pp 2295–2305 | Cite as

Longitudinal changes in calcaneal quantitative ultrasound measures during childhood

  • M. LeeEmail author
  • R. W. Nahhas
  • A. C. Choh
  • E. W. Demerath
  • D. L. Duren
  • W. C. Chumlea
  • R. J. Sherwood
  • B. Towne
  • R. M. Siervogel
  • S. A. Czerwinski
Original Article



This longitudinal study examined how calcaneal quantitative ultrasound (QUS) measures change during childhood while taking into account skeletal maturation, body mass index (BMI), and physical activity. The study reported sex differences in QUS growth curves and an inverse relationship between BMI and speed of sound (SOS) measures.


The aim of this study was to examine how calcaneal QUS parameters change over time during childhood and to determine what factors influence these changes.


The study sample consisted of a total of 192 Caucasian children participating in the Fels Longitudinal Study. A total of 548 calcaneal broadband ultrasound attenuation (BUA) and SOS observations were obtained between the ages of 7.6 and 18 years. The best fitting growth curves were determined using statistical methods for linear mixed effect models.


There are significant sex differences in the pattern of change in QUS parameters (p < 0.05). The relationship between QUS measures and skeletal age is best described by a cubic growth curve in boys and a linear pattern among girls. Boys experience their most rapid growth in BUA and SOS in early and late adolescence, while girls experience constant growth throughout childhood. Adiposity levels were significantly associated with the changes in SOS among boys (p < 0.001) and girls (p < 0.01), indicating that children with higher BMI are likely to have lower SOS over time compared to children with lower BMI. For girls, physical activity levels showed positive associations with changes in QUS measures (p < 0.05).


This study documents significant sex differences in the pattern of change in QUS measures over childhood and adolescence. Our study also shows significant influences of adiposity and physical activity on the pattern of change in QUS measures during childhood.


Calcaneal quantitative ultrasound Children Longitudinal study Skeletal health 



This study was supported by National Institutes of Health grants (AR052147, HD012252). This study was presented in part at the American Society for Bone and Mineral Research Annual meeting in 2008. We are thankful for the participants in the Fels Longitudinal Study and the assistance of our research staff.

Conflicts of interest



  1. 1.
    Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak bone mass. Osteoporos Int 11:985–1009PubMedCrossRefGoogle Scholar
  2. 2.
    Specker BL (2006) Influence of rapid growth on skeletal adaptation to exercise. J Musculoskelet Neuronal Interact 6:147–153PubMedGoogle Scholar
  3. 3.
    Gluer CC, Barkmann R (2003) Quantitative ultrasound: use in the detection of fractures and in the assessment of bone composition. Curr Osteoporos Rep 1:98–104PubMedCrossRefGoogle Scholar
  4. 4.
    Gluer CC (1997) Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. The International Quantitative Ultrasound Consensus Group. J Bone Miner Res 12:1280–1288PubMedCrossRefGoogle Scholar
  5. 5.
    Baroncelli GI (2008) Quantitative ultrasound methods to assess bone mineral status in children: technical characteristics, performance, and clinical application. Pediatr Res 63:220–228PubMedCrossRefGoogle Scholar
  6. 6.
    Bauer DC, Gluer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, Black DM (1997) Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. A prospective study. Study of Osteoporotic Fractures Research Group. Arch Intern Med 157:629–634PubMedCrossRefGoogle Scholar
  7. 7.
    Marin F, Gonzalez-Macias J, Diez-Perez A, Palma S, Delgado-Rodriguez M (2006) Relationship between bone quantitative ultrasound and fractures: a meta-analysis. J Bone Miner Res 21:1126–1135PubMedCrossRefGoogle Scholar
  8. 8.
    Bauer DC, Ewing SK, Cauley JA, Ensrud KE, Cummings SR, Orwoll ES (2007) Quantitative ultrasound predicts hip and non-spine fracture in men: the MrOS study. Osteoporos Int 18:771–777PubMedCrossRefGoogle Scholar
  9. 9.
    Falcini F, Bindi G, Ermini M, Galluzzi F, Poggi G, Rossi S, Masi L, Cimaz R, Brandi ML (2000) Comparison of quantitative calcaneal ultrasound and dual energy X-ray absorptiometry in the evaluation of osteoporotic risk in children with chronic rheumatic diseases. Calcif Tissue Int 67:19–23PubMedCrossRefGoogle Scholar
  10. 10.
    Fielding KT, Nix DA, Bachrach LK (2003) Comparison of calcaneus ultrasound and dual X-ray absorptiometry in children at risk of osteopenia. J Clin Densitom 6:7–15PubMedCrossRefGoogle Scholar
  11. 11.
    Gilsanz V (1998) Bone density in children: a review of the available techniques and indications. Eur J Radiol 26:177–182PubMedCrossRefGoogle Scholar
  12. 12.
    van den Bergh JP, Noordam C, Ozyilmaz A, Hermus AR, Smals AG, Otten BJ (2000) 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 11:967–976PubMedCrossRefGoogle Scholar
  13. 13.
    Zadik Z, Price D, Diamond G (2003) Pediatric reference curves for multi-site quantitative ultrasound and its modulators. Osteoporos Int 14:857–862PubMedCrossRefGoogle Scholar
  14. 14.
    Halaba ZP, Pluskiewicz W (2004) Quantitative ultrasound in the assessment of skeletal status in children and adolescents. Ultrasound Med Biol 30:239–243PubMedCrossRefGoogle Scholar
  15. 15.
    Baroncelli GI, Federico G, Vignolo M, Valerio G, del Puente A, Maghnie M, Baserga M, Farello G, Saggese G (2006) Cross-sectional reference data for phalangeal quantitative ultrasound from early childhood to young-adulthood according to gender, age, skeletal growth, and pubertal development. Bone 39:159–173PubMedCrossRefGoogle Scholar
  16. 16.
    Gonnelli S, Caffarelli C, Hayek J, Montagnani A, Cadirni A, Franci B, Lucani B, Rossi S, Nuti R (2008) Bone ultrasonography at phalanxes in patients with Rett syndrome: a 3-year longitudinal study. Bone 42:737–742PubMedCrossRefGoogle Scholar
  17. 17.
    Kutilek S, Bayer M, Dolezalova P, Nemcova D (2006) Quantitative ultrasonometry of the calcaneus in children with juvenile idiopathic arthritis. Rheumatology 45:1273–1275PubMedCrossRefGoogle Scholar
  18. 18.
    Zadik Z, Sinai T, Borondukov E, Zung A, Yaniv I, Reifen R (2005) Longitudinal monitoring of bone accretion measured by quantitative multi-site ultrasound (QUS) of bones in patients with delayed puberty (a pilot study). Osteoporos Int 16:1036–1041PubMedCrossRefGoogle Scholar
  19. 19.
    Vignolo M, Parodi A, Mascagni A, Torrisi C, De Terlizzi F, Aicardi G (2006) Longitudinal assessment of bone quality by quantitative ultrasonography in children and adolescents. Ultrasound Med Biol 32:1003–1010PubMedCrossRefGoogle Scholar
  20. 20.
    Lappe JM, Stegman M, Davies KM, Barber S, Recker RR (2000) A prospective study of quantitative ultrasound in children and adolescents. J Clin Densitom 3:167–175PubMedCrossRefGoogle Scholar
  21. 21.
    Roche AF (1992) Growth, maturation, and body composition: the Fels Longitudinal Study, 1929–1991. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  22. 22.
    Lee M, Czerwinski SA, Choh AC, Demerath EW, Sun SS, Chumlea WC, Towne B, Siervogel RM (2006) Unique and common genetic effects between bone mineral density and calcaneal quantitative ultrasound measures: the Fels Longitudinal Study. Osteoporos Int 17:865–871PubMedCrossRefGoogle Scholar
  23. 23.
    Gluer CC, Wu CY, Jergas M, Goldstein SA, Genant HK (1994) Three quantitative ultrasound parameters reflect bone structure. Calcif Tissue Int 55:46–52PubMedCrossRefGoogle Scholar
  24. 24.
    Tavakoli MB, Evans JA (1992) The effect of bone structure on ultrasonic attenuation and velocity. Ultrasonics 30:389–395PubMedCrossRefGoogle Scholar
  25. 25.
    Roche AF, Chumlea W, Thissen D (1988) Assessing the skeletal maturity of the hand-wrist: FELS method. Thomas, SpringfieldGoogle Scholar
  26. 26.
    Lohman T, Martorell R, Roche AF (1988) Anthropometric standardization reference manual. Human Kinetics, ChampaignGoogle Scholar
  27. 27.
    Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, Mei Z, Curtin LR, Roche AF, Johnson CL (2000) CDC growth charts: United States. Adv Data 314:1–28PubMedGoogle Scholar
  28. 28.
    Baecke JAH, Burema J, Frijters JER (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36:936–942PubMedGoogle Scholar
  29. 29.
    Treuth MS, Hou N, Young DR, Maynard LM (2005) Validity and reliability of the Fels physical activity questionnaire for children. Med Sci Sports Exerc 37:488–495PubMedCrossRefGoogle Scholar
  30. 30.
    Fitzmaurice GM, Laird NM, Ware JH (2004) Applied longitudinal analysis. Wiley-Interscience, HobokenGoogle Scholar
  31. 31.
    Laird NM, Ware JH (1982) Random-effects models for longitudinal data. Biometrics 38:963–974PubMedCrossRefGoogle Scholar
  32. 32.
    Akaike H (1974) A new look at the statistical model identification. IEEE Trans 19:716–723Google Scholar
  33. 33.
    Wang Q, Nicholson PH, Timonen J, Alen M, Moilanen P, Suominen H, Cheng S (2008) Monitoring bone growth using quantitative ultrasound in comparison with DXA and pQCT. J Clin Densitom 11:295–301PubMedCrossRefGoogle Scholar
  34. 34.
    Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the university of Saskatchewan bone mineral accrual study. J Bone Miner Res 14:1672–1679PubMedCrossRefGoogle Scholar
  35. 35.
    Whiting SJ, Vatanparast H, Baxter-Jones A, Faulkner RA, Mirwald R, Bailey DA (2004) Factors that affect bone mineral accrual in the adolescent growth spurt. J Nutr 134:696S–700SPubMedGoogle Scholar
  36. 36.
    Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K (2004) Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone 35:973–981PubMedCrossRefGoogle Scholar
  37. 37.
    Gunter K, Baxter-Jones AD, Mirwald RL, Almstedt H, Fuchs RK, Durski S, Snow C (2008) Impact exercise increases BMC during growth: an 8-year longitudinal study. J Bone Miner Res 23:986–993PubMedCrossRefGoogle Scholar
  38. 38.
    Janz KF, Gilmore JM, Burns TL, Levy SM, Torner JC, Willing MC, Marshall TA (2006) Physical activity augments bone mineral accrual in young children: the Iowa Bone Development Study. J Pediatr 148:793–799PubMedCrossRefGoogle Scholar
  39. 39.
    Sundberg M, Gardsell P, Johnell O, Karlsson MK, Ornstein E, Sandstedt B, Sernbo I (2002) Physical activity increases bone size in prepubertal boys and bone mass in prepubertal girls: a combined cross-sectional and 3-year longitudinal study. Calcif Tissue Int 71:406–415PubMedCrossRefGoogle Scholar
  40. 40.
    Schonau E, Radermacher A, Wentzlik U, Klein K, Michalk D (1994) The determination of ultrasound velocity in the os calcis, thumb and patella during childhood. Eur J Pediatr 153:252–256PubMedCrossRefGoogle Scholar
  41. 41.
    Wunsche K, Wunsche B, Fahnrich H, Mentzel HJ, Vogt S, Abendroth K, Kaiser WA (2000) Ultrasound bone densitometry of the os calcis in children and adolescents. Calcif Tissue Int 67:349–355PubMedCrossRefGoogle Scholar
  42. 42.
    Halaba ZP (2008) Quantitative ultrasound measurements at hand phalanges in children and adolescents: a longitudinal study. Ultrasound Med Biol 34:1547–1553PubMedCrossRefGoogle Scholar
  43. 43.
    Jaworski M, Lebiedowski M, Lorenc RS, Trempe J (1995) Ultrasound bone measurement in pediatric subjects. Calcif Tissue Int 56:368–371PubMedCrossRefGoogle Scholar
  44. 44.
    Dib L, Arabi A, Maalouf J, Nabulsi M, El-Hajj Fuleihan G (2005) Impact of anthropometric, lifestyle, and body composition variables on ultrasound measurements in school children. Bone 36:736–742PubMedCrossRefGoogle Scholar
  45. 45.
    Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol 30:160–175PubMedCrossRefGoogle Scholar
  46. 46.
    Cameron N (2002) Assessment of maturation. In: Cameron N (ed) Human growth and development. Academic, New York, pp 363–382CrossRefGoogle Scholar
  47. 47.
    Loud KJ, Gordon CM (2006) Adolescent bone health. Arch Pediatr Adolesc Med 160:1026–1032PubMedCrossRefGoogle Scholar
  48. 48.
    Daniels SR, Khoury PR, Morrison JA (1997) The utility of body mass index as a measure of body fatness in children and adolescents: differences by race and gender. Pediatrics 99:804–807PubMedCrossRefGoogle Scholar
  49. 49.
    Prentice AM, Jebb SA (2001) Beyond body mass index. Obes Rev 2:141–147PubMedCrossRefGoogle Scholar
  50. 50.
    Demerath EW, Schubert CM, Maynard LM, Sun SS, Chumlea WC, Pickoff A, Czerwinski SA, Towne B, Siervogel RM (2006) Do changes in body mass index percentile reflect changes in body composition in children? Data from the Fels Longitudinal Study. Pediatrics 117:e487–e495PubMedCrossRefGoogle Scholar
  51. 51.
    Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS (2005) Racial differences in the tracking of childhood BMI to adulthood. Obes Res 13:928–935PubMedCrossRefGoogle Scholar
  52. 52.
    Flegal KM, Ogden CL, Yanovski JA, Freedman DS, Shepherd JA, Graubard BI, Borrud LG (2010) High adiposity and high body mass index-for-age in US children and adolescents overall and by race–ethnic group. Am J Clin Nutr 91:1020–1026PubMedCrossRefGoogle Scholar
  53. 53.
    Falk B, Braid S, Moore M, O’Leary D, Sullivan P, Klentrou P (2008) Bone properties in overweight pre- and early-pubertal boys. Pediatr Exerc Sci 20:50–61PubMedGoogle Scholar
  54. 54.
    Hasanoglu A, Bideci A, Cinaz P, Tumer L, Unal S (2000) Bone mineral density in childhood obesity. J Pediatr Endocrinol Metab 13:307–311PubMedCrossRefGoogle Scholar
  55. 55.
    Leonard MB, Shults J, Wilson BA, Tershakovec AM, Zemel BS (2004) Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 80:514–523PubMedGoogle Scholar
  56. 56.
    Goulding A, Taylor RW, Jones IE, McAuley KA, Manning PJ, Williams SM (2000) Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord 24:627–632PubMedCrossRefGoogle Scholar
  57. 57.
    Rocher E, Chappard C, Jaffre C, Benhamou CL, Courteix D (2008) Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26:73–78PubMedCrossRefGoogle Scholar
  58. 58.
    Babaroutsi E, Magkos F, Manios Y, Sidossis LS (2005) Body mass index, calcium intake, and physical activity affect calcaneal ultrasound in healthy Greek males in an age-dependent and parameter-specific manner. J Bone Miner Metab 23:157–166PubMedCrossRefGoogle Scholar
  59. 59.
    Babaroutsi E, Magkos F, Manios Y, Sidossis LS (2005) Lifestyle factors affecting heel ultrasound in Greek females across different life stages. Osteoporos Int 16:552–561PubMedCrossRefGoogle Scholar
  60. 60.
    Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM (2000) More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res 15:2011–2018PubMedCrossRefGoogle Scholar
  61. 61.
    Weiler HA, Janzen L, Green K, Grabowski J, Seshia MM, Yuen KC (2000) Percent body fat and bone mass in healthy Canadian females 10 to 19 years of age. Bone 27:203–207PubMedCrossRefGoogle Scholar
  62. 62.
    Rubin CT, Lanyon LE (1985) Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 37:411–417PubMedCrossRefGoogle Scholar
  63. 63.
    Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA (2008) A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone 43:1101–1107PubMedCrossRefGoogle Scholar
  64. 64.
    Weeks BK, Young CM, Beck BR (2008) Eight months of regular in-school jumping improves indices of bone strength in adolescent boys and girls: the POWER PE study. J Bone Miner Res 23:1002–1011PubMedCrossRefGoogle Scholar
  65. 65.
    Rowlands AV, Ingledew DK, Powell SM, Eston RG (2004) Interactive effects of habitual physical activity and calcium intake on bone density in boys and girls. J Appl Physiol 97:1203–1208PubMedCrossRefGoogle Scholar
  66. 66.
    Kriemler S, Zahner L, Puder JJ, Braun-Fahrlander C, Schindler C, Farpour-Lambert NJ, Kranzlin M, Rizzoli R (2008) Weight-bearing bones are more sensitive to physical exercise in boys than in girls during pre- and early puberty: a cross-sectional study. Osteoporos Int 19:1749–1758PubMedCrossRefGoogle Scholar
  67. 67.
    Pettinato AA, Loud KJ, Bristol SK, Feldman HA, Gordon CM (2006) Effects of nutrition, puberty, and gender on bone ultrasound measurements in adolescents and young adults. J Adolesc Health 39:828–834PubMedCrossRefGoogle Scholar
  68. 68.
    Gluer CC (2008) A new quality of bone ultrasound research. IEEE Trans Ultrason Ferroelectr Freq Control 55:1524–1528PubMedCrossRefGoogle Scholar
  69. 69.
    Guglielmi G, Adams J, Link TM (2009) Quantitative ultrasound in the assessment of skeletal status. Eur Radiol 19:1837–1848PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2010

Authors and Affiliations

  • M. Lee
    • 1
    • 2
    Email author
  • R. W. Nahhas
    • 1
  • A. C. Choh
    • 1
  • E. W. Demerath
    • 3
  • D. L. Duren
    • 1
  • W. C. Chumlea
    • 1
    • 2
  • R. J. Sherwood
    • 1
    • 2
  • B. Towne
    • 1
    • 2
  • R. M. Siervogel
    • 1
    • 2
  • S. A. Czerwinski
    • 1
  1. 1.Lifespan Health Research Center, Department of Community HealthWright State University Boonshoft School of MedicineDaytonUSA
  2. 2.Department of PediatricsWright State University Boonshoft School of MedicineDaytonUSA
  3. 3.Division of Epidemiology and Community Health, School of Public HealthUniversity of MinnesotaMinneapolisUSA

Personalised recommendations