Bone microstructure at the distal tibia provides a strength advantage to males in late puberty: An HR-pQCT study

Journal of Bone and Mineral Research

Volumn 25, Issue 6, 2010, Pages 1423-1432

  Burrows, Melonie ^a   Liu, Danmei ^a   Moore, Sarah ^a   McKay, Heather ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Bone; Bone microstructure; Bone PQCT; Bone strength; Pediatrics

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; BONE AREA; BONE CHARACTERISTICS AND FUNCTIONS; BONE DENSITY; BONE MICROSTRUCTURE; BONE STRENGTH; BONE STRUCTURE; COMPRESSION; CONTROLLED STUDY; CORTICAL BONE; CROSS-SECTIONAL STUDY; FEMALE; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HUMAN; MALE; NORMAL HUMAN; PUBERTY; QUANTITATIVE ANALYSIS; SEX DIFFERENCE; THICKNESS; TIBIA; TRABECULAR BONE;

ADOLESCENT; AGE DISTRIBUTION; FEMALE; HUMANS; MALE; PUBERTY; SEX CHARACTERISTICS; TIBIA; TOMOGRAPHY, X-RAY COMPUTED; YOUNG ADULT;

EID: 77953517358     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.091034     Document Type: Article

References (78)

1. Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA. 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. Journal of Bone Mineral Research. 1999;14:1672-9.
2. Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA. A longitudinal analysis of sex differences in bone mineral accrual in healthy 8- to 19- year-old boys and girls. Ann Hum Biol. 2003;30:160-75.
3. Forwood MR, Baxter-Jones AD, Beck TJ, Mirwald RL, Howard A, Bailey DA. Physical activity and strength of the femoral neck during the adolescent growth spurt: A longitudinal analysis. Bone. 2006;38:576-583.
4. Macdonald HM, Kontulainen SA, Petit MA, Khan KM, McKay HA. Does a novel school-based physical activity intervention benefit femoral neck bone strength in pre- and early pubertal children? Osteoporosis International. 2008;19:1445-1456.
5. Petit MA, Beck TJ, Kontulainen SA. Examining the developing bone: What do we measure and how do we do it? J Musculoskelet Neuronal Interact. 2005;5:213-224.
6. Neu CM, Manz F, Rauch F, Merkel A, Schoenau E. Bone densities and bone size at the distal radius in healthy children and adolescents: a study using peripheral quantitative computed tomography. Bone. 2001;28:227-232. (Pubitemid 32140979)
7. Macdonald H, Kontulainen S, Petit M, Janssen P, McKay H. Bone strength and its determinants in pre- and early pubertal boys and girls. Bone. 2006;39:598-608.
8. Kontulainen SA, Macdonald HM, Khan KM, McKay HA. Examining bone surfaces across puberty: a 20-month pQCT trial. J Bone Miner Res. 2005;20:1202-7.
9. Kontulainen SA, Macdonald HM, McKay HA. Change in cortical bone density and its distribution differs between boys and girls during puberty. J Clin Endocrinol Metab. 2006;91:2555-61.
10. Macdonald H, Kontulainen SA, Mackelvie-O'Brien KJ, et al. Maturity-and sex-related changes in tibial bone geometry, strength and bone-muscle strength indices during growth: a 20-month pQCT study. Bone. 2005;36:1003-1011.
11. Cooper DML, Ahamed Y, Macdonald HM, McKay HA. Characterising cortical density in the mid-tibia: intra-individual variation in adolescent girls and boys. Br J Sports Med. 2008;42:690-695.
12. Neu CM, Rauch F, Manz F, Schoenau E. Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporosis Int. 2001;12:538-47.
13. Moyer-Mileur L, Xie B, Ball S, Bainbridge C, Stadler D, Jee WS. Predictors of bone mass by peripheral quantitative computed tomography in early adolescent girls. J Clin Densitom. 2001;4:313-23.
14. Khosla S, Riggs BL, Atkinson EJ, et al. Effects of sex and age on bone microstructure at the ultra-distal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. 2006;21:124-31.
15. Cooper C, Melton LJ. Epidemiology of osteoporosis. Trends in Endocrinology and Metabolism. 1992;3:224-229.
16. Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005;90:6508-15.
17. Laib A, Ruegsegger P. Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-microm-resolution microcomputed tomography. Bone. 1999;24:35-9.
18. Laib A, Hauselmann HJ, Ruegsegger P. In vivo high resolution 3D-QCT of the human forearm. Technol Health Care. 1998;6:329-37.
19. Boutroy S, Van Rietbergen B, Sornay-Rendu E, Munoz F, Bouxsein ML, Delmas PD. Finite element analysis based on in vivo HR-pQCT images of the distal radius is associated with wrist fracture in postmenopausal women. J Bone Miner Res. 2008;23:392-9.
20. Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD. Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res. 2007;22:425-33.
21. Boyd SK. Site-Specific Variation of Bone Micro-Architecture in the Distal Radius and Tibia. Journal of Clinical Densitometry. 2008;11:424-430.
22. Kirmani S, Christen D, van Lenthe GH, et al. Bone Structure at the Distal Radius During Adolescent Growth. Journal of Bone and Mineral Research. 2009;24:1033-1042.
23. Burrows M, Liu D, McKay H. High-resolution peripheral QCT imaging of bone micro-structure in adolescents. Osteoporosis International Web first content (10.1007/s00198-009-0913-2), 2009.
24. MacKelvie KJ, McKay HA, Khan KM, Crocker PR. A school-based exercise intervention augments bone mineral accrual in early pubertal girls. Journal of Pediatrics. 2001;139:501-8.
25. Petit MA, McKay HA, MacKelvie KJ, Heinonen A, Khan KM, Beck TJ. A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. Journal of Bone Mineral Research. 2002;17:363-72.
26. MacKelvie KJ, McKay HA, Khan KM, Crocker PR. Lifestyle risk factors for osteoporosis in Asian and Caucasian girls. Medicine and Science in Sports and Exercise. 2001;33:1818-24.
27. Tanner JM. Foetus into man. Cambridge: Harvard Press; 1978.
28. Macdonald H, Kontulainen S, Petit M, Beck T, Khan K, McKay H. Does a novel school-based physical activity model benefit femoral neck bone strength in pre- and early pubertal children? Osteoporosis International. 2008;19:1445-1456.
29. Macdonald HM, Kontulainen SA, Khan KM, McKay HA. Is a School-Based Physical Activity Intervention Effective for Increasing Tibial Bone Strength in Boys and Girls? Journal of Bone and Mineral Research. 2007;22:434-446.
30. Crocker PR, Bailey DA, Faulkner RA, Kowalski KC, McGrath R. Measuring general levels of physical activity: preliminary evidence for the Physical Activity Questionnaire for Older Children. Medicine and Science in Sports and Exercise. 1997;29:1344-9.
31. Kowalski KC, Crocker PR, Faulkner RA. Validation of the physical activity questionnaire for older children. Pediatr Exerc Sci. 1997;9:174-186.
32. Barr SI. Associations of social and demographic variables with calcium intakes of high school students. Journal of the American Diet Association. 1994;94:260-6.
33. Kontulainen S, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA. Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. Journal of Musculoskeletal and Neurological Interactions. 2008;8:401-409.
34. Kontulainen S, Sievà Nen H, Kannus P, Pasanen M, Vuori I. Effect of Long-Term Impact-Loading on Mass, Size, and Estimated Strength of Humerus and Radius of Female Racquet-Sports Players: A Peripheral Quantitative Computed Tomography Study Between Young and Old Starters and Controls. Journal of Bone and Mineral Research. 2002;17:2281-2289.
35. Wetzsteon RJ, Petit MA, Macdonald HM, Hughes JM, Beck TJ, McKay HA. Bone Structure and Volumetric Bone Density in Overweight Children: A Longitudinal Study. Journal of Bone and Mineral Research. 2008;23:1946-53.
36. Carter DR, Hayes WC. Bone compressive strength: the influence of density and strain rate. Science. 1976;194:1174-6.
37. HayesWC. Biomechanics of Cortical and Trabecular Bone: Implications for Assessment of Fracture Risk. In: Mow VC, Hayes WC, eds. Basic Orthopaedic Biomechanics. New York: Raven Press Ltd; 1991: 93-142.
38. MacNeil J, Boyd SK. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. 2007;29:1096-105.
39. Weiner S, Wagner HD. The material bone: Structure-mechanical function relations. Ann Rev Mater Sci. 1998;28:271-98.
40. Martin RB. Determinants of the mechanical properties of bones. J Biomech. 1991;24 (Suppl 1): 79-88.
41. Rauch F, Schoenau E. Peripheral quantitative computed tomography of the distal radius in young subjects - new reference data and interpretation of results. J Musculoskelet Neuronal Interact. 2005;5:119-26.
42. Macdonald H, Cooper D, McKay H. Anterior-posterior bending strength at the tibial shaft increases with physical activity in boys: evidence for non-uniform geometric adaptation. Osteoporosis International. 2009;20:61-70.
43. Rauch F. Bone growth in length and width: the yin and yang of bone stability. J Musculoskelet Neuronal Interact. 2005;5:194-201.
44. Garn SM. The course of bone gain and the phases of bone loss. Orthop Clin North Am. 1972;3:503-20.
45. Ruff C. Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone. 2003;33:317-29.
46. Garn SM. The earlier gain and later loss of cortical bone. Springfield, Il: Charles C Thomas; 1970.
47. Ruff C, Holt B, Trinkaus E. Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol. 2006.
48. Augat P, Schorlemmer S. The role of cortical bone and its microstructure in bone strength. Age Ageing 2006;35:27-31.
49. Augat P, Reeb H, Claes LE. Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell. J Bone Miner Res. 1996;11:1356-63. (Pubitemid 26282537)
50. Lochmuller EM, Groll O, Kuhn V, Eckstein F. Mechanical strength of the proximal femur as predicted from geometric and densitometric bone properties at the lower limb versus the distal radius. Bone. 2002;30:207-16. (Pubitemid 34048324)
51. Seeman E. Bone quality: the material and structural basis of bone strength. Journal of Bone and Mineral Metabolism. 2008;26:1-8. (Pubitemid 350308006)
52. Wehner T, Claes L, Simon U. Internal loads in the human tibia during gait. Clinical Biomechanics. 2009;24:299-302.
53. Sasimontonkul S, Bay BK, Pavol MJ. Bone contact forces on the distal tibia during the stance phase of running. Journal of Biomechanics. 2007;40:3503-3509. (Pubitemid 47632609)
54. Burr DB, Martin RB. The effects of composition, structure and age on the torsional properties of the human radius. Journal of Biomechanics. 1983;16:603-608.
55. Schoenau E, Neu CM, Rauch F, Manz F. The development of bone strength at the proximal radius during childhood and adolescence. J Clin Endocrinol Metab. 2001;86:613-8. (Pubitemid 32207468)
56. Forwood MR, Bailey DA, Beck TJ, Mirwald RL, Baxter-Jones AD, Uusi-Rasi K. Sexual dimorphism of the femoral neck during the adolescent growth spurt: a structural analysis. Bone. 2004;35:973-81. (Pubitemid 39349229)
57. Beck TJ. Hip Structural Analysis (HSA) Scanning Procedures and Program. Baltimore, MD: Johns Hopkins University; 2001.
58. Rauch F. Bone Accrual in Children: Adding Substance to Surfaces. Pediatrics 2007;119:S137-140. (Pubitemid 46397934)
59. Högler W, Blimkie CJR, Cowell CT, et al. Sex-specific developmental changes in muscle size and bone geometry at the femoral shaft. Bone. 2008;42:982-989.
60. Gilsanz V, Kovanlikaya A, Costin G, Roe TF, Sayre J, Kaufman F. Differential effect of gender on the sizes of the bones in the axial and appendicular skeletons. J Clin Endocrinol Metab. 1997;82:1603-7. (Pubitemid 27200442)
61. Loro ML, Sayre J, Roe TF, Goran MI, Kaufman FR, Gilsanz V. Early identification of children predisposed to low peak bone mass and osteoporosis later in life. J Clin Endocrinol Metab. 2000;85:3908-18.
62. Rauch F, Schoenau E. Changes in bone density during childhood and adolescence: an approach based on bone's biological organization. J Bone Miner Res. 2001;16:597-604. (Pubitemid 32230588)
63. Sievanen H, Koskue V, Rauhio A, Kannus P, Heinonen A, Vuori I. Peripheral quantitative computed tomography in human long bones: evaluation of in vitro and in vivo precision. J Bone Miner Res. 1998;13:871-82. (Pubitemid 28224204)
64. Seeman E, Delmas PD. Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med. 2006;354:2250-61. (Pubitemid 43788139)
65. Schaffler MB, Burr DB. Stiffness of compact bone: effects of porosity and density. J Biomech. 1988;21:13-6.
66. Schoenau E, Neu CM, Rauch F, Manz F. Gender-specific pubertal changes in volumetric cortical bone mineral density at the proximal radius. Bone. 2002;31:110-113. (Pubitemid 34754435)
67. Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue microdamage. J Biomech. 1985;18:189-200. (Pubitemid 15112335)
68. McBroom R, Hayes WC, Edwards WT, Goldberg RP, White AA. Prediction of vertebral body compressive fracture using quantitative computed tomography. Journal of Bone and Joint Surgery. 1985;67:1206-1214. (Pubitemid 16222962)
69. Lotz J, Hayes WC. The use of quantitative computed tomography to estimate risk of fracture at the hip from falls. Journal of Bone and Joint Surgery. 1990;72:689-700. (Pubitemid 20236489)
70. Jarvinen TL, Kannus P, Sievanen H. Estrogen and bone-a reproductive and locomotive perspective. J Bone Miner Res. 2003;18:1921-31. (Pubitemid 37377440)
71. Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG. Changes in vertebral bone density in black girls and white girls during childhood and puberty. N Engl J Med. 1991;325:1597-600.
72. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest. 1999;104:795-804. (Pubitemid 29536365)
73. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E. Heterogeneity in the growth of the axial and appendicular skeleton in boys: implications for the pathogenesis of bone fragility in men. J Bone Miner Res. 2000;15:1871-8.
74. Gilsanz V, Skaggs DL, Kovanlikaya A, et al. Differential effect of race on the axial and appendicular skeletons of children. J Clin Endocrinol Metab. 1998;83:1420-7. (Pubitemid 28500996)
75. Hogler W, Blimkie CJ, Cowell CT, et al. A comparison of bone geometry and cortical density at the mid-femur between prepuberty and young adulthood using magnetic resonance imaging. Bone. 2003;33:771-8. (Pubitemid 37393488)
76. van der Linden J, Weinans H. Effects of microarchitecture on bone strength. Curr Osteoporosis Rep. 2007;5:56-61.
77. Kirmani S, Christen D, van Lenthe GH, et al. Bone Structure at the Distal Radius During Adolescent Growth. Journal of Bone and Mineral Research. 2010;0:1-34.
78. Khosla S, Melton LJ III, Achenbach SJ, Oberg AL, Riggs BL. Hormonal and Biochemical Determinants of Trabecular Microstructure at the Ultradistal Radius in Women and Men. J Clin Endocrinol Metab. 2006;91:885-891. (Pubitemid 43357754)