The Chinese skeleton: Insights into microstructure that help to explain the epidemiology of fracture

Bone Research

Volumn 2, Issue , 2014, Pages

  Cong, Elaine ^a   Walker, Marcella D ^a  

^a NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84993177746     PISSN: 20954700     EISSN: 20956231     Source Type: Journal    
DOI: 10.1038/boneres.2014.9     Document Type: Review

References (117)

1. Cooper C, Atkinson EJ, Jacobsen SJ, O'Fallon WM, Melton LJ 3rd. Population-based study of survival after osteoporotic fractures. Am J Epidemiol 1993; 137: 1001-1005.
2. Chrischilles EA, Butler CD, Davis CS, Wallace RB. A model of lifetime osteoporosis impact. Arch Intern Med 1991; 151: 2026-2032.
3. Dempster DW. Osteoporosis and the burden of osteoporosis-related fractures. Am J Manag Care 2011; 17(Suppl 6): S164-S169.
4. Kanis JA, Oden A,McCloskey EV, Johansson H,Wahl DA, Cooper C. A systematic review of hip fracture incidence and probability of fracture worldwide. Osteoporos Int 2012; 23: 2239-2256.
5. Dai K, Zhang Q, Fan T, Sen SS, Osteoporotic Hip Fracture in China Study T. Estimation of resource utilization associated with osteoporotic hip fracture and level of post-acute care in China. Curr Med Res Opin 2007; 23: 2937-2943.
6. Cooper C, Campion G, Melton LJ 3rd. Hip fractures in the elderly: a world-wide projection. Osteoporos Int 1992; 2: 285-289.
7. Koh LK, Saw SM, Lee JJ, Leong KH, Lee J,NationalWorking Committee on O. Hip fracture incidence rates in Singapore 1991-1998. Osteoporos Int 2001; 12: 311-318.
8. Cooper C, Cole ZA, Holroyd CR et al. Secular trends in the incidence of hip and other osteoporotic fractures. Osteoporos Int 2011; 22: 1277-1288.
9. Wu XP, Liao EY, Luo XH, Dai RC, Zhang H, Peng J. Age-related variation in quantitative ultrasound at the tibia and prevalence of osteoporosis in native Chinese women. Br J Radiol 2003; 76: 605-610.
10. Taylor AJ, Gary LC, Arora T et al. Clinical and demographic factors associated with fractures among older Americans. Osteoporos Int 2011; 22: 1263-1274.
11. Golden SH, Brown A, Cauley JA et al. Health disparities in endocrine disorders: biological, clinical, and nonclinical factors-an Endocrine Society scientific statement. J Clin Endocrinol Metab 2012; 97: E1579-E1639.
12. Proximity One. America's Asian Population Patterns 2012. Available at http://proximityone.com/cen2010-asian.ht.m.
13. NIH Consensus Development Panel on Osteoporosis Prevention D, Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA 2001; 285: 785-795.
14. NIH Consensus Development Panel on Osteoporosis. Osteoporosis prevention, diagnosis and therapy. J Am Med Assoc 2001; 285: 785-795.
15. Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int 2003; 14(Suppl 3): S13-S18.
16. Finkelstein JS, Lee ML, SowersMet al. Ethnic variation in bone density in premenopausal and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 2002; 87: 3057-3067.
17. Russell-Aulet M, Wang J, Thornton JC, Colt EW, Pierson RN Jr. Bone mineral density and mass in a cross-sectional study of white and Asian women. J Bone Miner Res 1993; 8: 575-582.
18. Carter DR, Bouxsein ML, Marcus R. New approaches for interpreting projected bone densitometry data. J Bone Miner Res 1992; 7: 137-145.
19. Katzman DK, Bachrach LK, Carter DR, Marcus R. Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 1991; 73: 1332-1339.
20. Barrett-Connor E, Siris ES, Wehren LE et al. Osteoporosis and fracture risk in women of different ethnic groups. J BoneMiner Res 2005; 20: 185-194.
21. Xu L, Lu A, Zhao X, Chen X, Cummings SR. Very low rates of hip fracture in Beijing, People's Republic of China the Beijing Osteoporosis Project. Am J Epidemiol 1996; 144: 901-907.
22. Lauderdale DS, Jacobsen SJ, Furner SE, Levy PS, Brody JA, Goldberg J. Hip fracture incidence among elderly Asian-American populations. Am J Epidemiol 1997; 146: 502-509.
23. Silverman SL, Madison RE. Decreased incidence of hip fracture in Hispanics, Asians, and Blacks: California Hospital Discharge Data. Am J Public Health 1988; 78: 1482-1483.
24. Ishii S, Cauley JA, Greendale GA, Danielson ME, Safaei Nili N, Karlamangla A. Ethnic differences in composite indices of femoral neck strength. Osteoporos Int 2012; 23: 1381-1390.
25. Yu N, Liu YJ, Pei Y et al. Evaluation of compressive strength index of the femoral neck in Caucasians and Chinese. Calcif Tissue Int 2010; 87: 324-332.
26. Walker MD,Liu XS, Zhou B et al. Pre-and postmenopausal differences in bone microstructure and mechanical competence in Chinese-American and white women. J Bone Miner Res 2013; 28: 1308-1318.
27. Walker MD, Liu XS, Stein E et al. Differences in bone microarchitecture between postmenopausal Chinese-American and white women. J Bone Miner Res 2011; 26: 1392-1398.
28. Liu XS, Walker MD, McMahon DJ et al. Better skeletal microstructure confers greater mechanical advantages in Chinese-American women versus white women. J Bone Miner Res 2011; 26: 1783-1792.
29. Walker MD, McMahon DJ, Udesky J, Liu G, Bilezikian JP. Application of high-resolution skeletal imaging to measurements of volumetric BMD and skeletal microarchitecture in Chinese-American and white women: explanation of a paradox. J Bone Miner Res 2009; 24: 1953-1959.
30. Wang XF, Wang Q, Ghasem-Zadeh A et al. Differences in macro-and microarchitecture of the appendicular skeleton in young Chinese and white women. J Bone Miner Res 2009; 24: 1946-1952.
31. Bow CH, Cheung E, Cheung CL et al. Ethnic difference of clinical vertebral fracture risk. Osteoporos Int 2012; 23: 879-885.
32. Golden SH, Brown A, Cauley JA et al. Health disparities in endocrine disorders: biological, clinical, and nonclinical factors-an endocrine society scientific statement. J Clin Endocrinol Metab 2012; 97: E1579-E1639.
33. Lau EM, Chan HH, Woo J et al. Normal ranges for vertebral height ratios and prevalence of vertebral fracture in Hong Kong Chinese: a comparison with American Caucasians. J Bone Miner Res 1996; 11: 1364-1368.
34. Ross PD, Fujiwara S, Huang C et al. Vertebral fracture prevalence in women in Hiroshima compared to Caucasians or Japanese in the US. Int J Epidemiol 1995; 24: 1171-1177.
35. Kung AW. Management of osteoporosis in Hong Kong. Clin Calcium 2004; 14: 108-111.
36. Tsang SW , Bow CH , Chu EY , Yeung SC , Soong CC , Kung AW. Clinical risk factor assessment had better discriminative ability than bone mineral density in identifying subjects with vertebral fracture. Osteoporos Int 2011; 22: 667-674.
37. Tsai K, Twu S, Chieng P, Yang R, Lee T. Prevalence of vertebral fractures in Chinese men and women in urban Taiwanese communities. Calcif Tissue Int 1996; 59: 249-253.
38. Melton LJ 3rd, Lane AW, Cooper C, Eastell R, O'Fallon WM, Riggs BL. Prevalence and incidence of vertebral deformities. Osteoporos Int 1993; 3: 113-119.
39. Black DM, Cummings SR, StoneK, Hudes E, Palermo L, Steiger P.Anew approach to defining normal vertebral dimensions. J Bone Miner Res 1991; 6: 883-892
40. Ling X, Cummings SR, Mingwei Q et al. Vertebral fractures in Beijing, China: the Beijing Osteoporosis Project. J BoneMiner Res 2000; 15: 2019-2025.
41. Lofthus CM, Frihagen F, Meyer HE, Nordsletten L, Melhuus K, Falch JA. Epidemiology of distal forearm fractures in Oslo, Norway. Osteoporos Int 2008; 19: 781-786.
42. Khandewal S, Chandra M, Lo JC. Clinical characteristics, bone mineral density and non-vertebral osteoporotic fracture outcomes among postmenopausal U.S. South Asian Women. Bone 2012; 51: 1025-1028.
43. Lau EM, Cooper C. Epidemiology and prevention of osteoporosis in urbanized Asian populations. Osteoporos Int 1993; 3(Suppl 1): 23-26.
44. Lau EM, Cooper C. The epidemiology of osteoporosis. The oriental perspective in a world context. Clin Orthop Relat Res 1996; (323): 65-74.
45. Lau EM, Lee JK, Suriwongpaisal P et al. The incidence of hip fracture in four Asian countries: the Asian Osteoporosis Study (AOS). Osteoporos Int 2001; 12: 239-243.
46. Lau EM, Suriwongpaisal P, Lee JK et al. Risk factors for hip fracture in Asian men and women: the Asian osteoporosis study. J Bone Miner Res 2001; 16: 572-580.
47. Chie WC, Yang RS, Liu JP, Tsai KS.High incidence rate of hip fracture in Taiwan: estimated from a nationwide health insurance database. Osteoporos Int 2004; 15: 998-1002.
48. Lau EM, Cooper C, Fung H, Lam D, Tsang KK. Hip fracture in Hong Kong over the last decade-a comparison with the UK. J Public Health Med 1999; 21: 249-250.
49. Ho SC, Bacon WE, Harris T, Looker A, Maggi S. Hip fracture rates in Hong Kong and the United States, 1988 through 1989. Am J Public Health 1993; 83: 694-697.
50. Yan L, Zhou B, Prentice A, Wang X, Golden MH. Epidemiological study of hip fracture in Shenyang, People's Republic of China. Bone 1999; 24: 151-155.
51. Bjornerem A, Bui QM, Ghasem-Zadeh A, Hopper JL, Zebaze R, Seeman E. Fracture risk and height: an association partly accounted for by cortical porosity of relatively thinner cortices. J Bone Miner Res 2013; 28: 2017-2026.
52. Woo J, Li M, Lau E. Population bone mineral density measurements for Chinese women and men in Hong Kong. Osteoporos Int 2001; 12: 289-295.
53. Xiaoge D, Eryuan L, XianpingWet al. Bone mineral density differences at the femoral neck and Ward's triangle: a comparison study on the reference data between Chinese and Caucasian women. Calcif Tissue Int 2000; 67: 195-198.
54. Walker MD, Babbar R, Opotowsky AR et al. A referent bone mineral density database for Chinese American women. Osteoporos Int 2006; 17: 878-887.
55. Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK. Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 1996; 11: 1545-1456.
56. Lau EM, Lynn H, Woo J, Melton LJ 3rd. Areal and volumetric bone density in Hong Kong Chinese: a comparison with Caucasians living in the United States. Osteoporos Int 2003; 14: 583-588.
57. Ross PD, He Y, Yates AJ et al. Body size accounts for most differences in bone density between Asian and Caucasian women. The EPIC (Early Postmenopausal Interventional Cohort) Study Group. Calcif Tissue Int 1996; 59: 339-343.
58. Nam HS, Shin MH, Zmuda JM et al. Race/ethnic differences in bone mineral densities in older men. Osteoporos Int 2010; 21: 2115-2123.
59. Bouxsein ML, Szulc P, Munoz F, Thrall E, Sornay-Rendu E, Delmas PD. Contribution of trochanteric soft tissues to fall force estimates, the factor of risk, and prediction of hip fracture risk. J Bone Miner Res 2007; 22: 825-831.
60. Majumder S, Roychowdhury A, Pal S. Effects of trochanteric soft tissue thickness and hip impact velocity on hip fracture in sideways fall through 3D finite element simulations. J Biomech 2008; 41: 2834-2842.
61. Melton LJ 3rd, Riggs BL, Keaveny TM et al. Structural determinants of vertebral fracture risk. J Bone Miner Res 2007; 22: 1885-1892.
62. Stein EM, Liu XS, Nickolas TL et al. Abnormal microarchitecture and stiffness in postmenopausal women with ankle fractures. J Clin Endocrinol Metab 2011; 96: 2041-2048.
63. 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: 392-399.
64. Cohen A, Liu XS, Stein EM et al. Bone microarchitecture and stiffness in premenopausal women with idiopathic osteoporosis. J Clin Endocrinol Metab 2009; 94: 4351-4360.
65. Faulkner KG, Cummings SR, Black D, PalermoL, Gluer CC, Genant HK. Simple measurement of femoral geometry predicts hip fracture: the study of osteoporotic fractures. J Bone Miner Res 1993; 8: 1211-1217.
66. PeacockM, Turner CH, Liu G,Manatunga AK, Timmerman L, Johnston CC Jr. Better discrimination of hip fracture using bone density, geometry and architecture. Osteoporos Int 1995; 5: 167-173.
67. Duboeuf F, Hans D, Schott AM et al. Different morphometric and densitometric parameters predict cervical and trochanteric hip fracture: the EPIDOS Study. J Bone Miner Res 1997; 12: 1895-1902.
68. Geusens P. Geometric characteristics of the proximal femur and hip fracture risk. Osteoporos Int 1996; 6(Suppl 3): 27-30.
69. Center JR,Nguyen TV, PocockNAet al. Femoral neck axis length, height loss and risk of hip fracture in males and females. Osteoporos Int 1998; 8: 75-81.
70. Cummings SR, Cauley JA, Palermo L et al. Racial differences in hip axis lengths might explain racial differences in rates of hip fracture. Study of Osteoporotic Fractures Research Group. Osteoporos Int 1994; 4: 226-229.
71. Yan L, Crabtree NJ, Reeve J et al. Does hip strength analysis explain the lower incidence of hip fracture in the People's Republic of China? Bone 2004; 34: 584-588.
72. Wang MC, Aguirre M, Bhudhikanok GS et al. Bone mass and hip axis length in healthy Asian, black, Hispanic, and white American youths. J Bone Miner Res 1997; 12: 1922-1935.
73. Wang XF, Duan Y, Beck TJ, Seeman E. Varying contributions of growth and ageing to racial and sex differences in femoral neck structure and strength in old age. Bone 2005; 36: 978-986.
74. Danielson ME, Beck TJ, Lian Y et al. Ethnic variability in bone geometry as assessed by hip structure analysis: findings from the hip strength across the menopausal transition study. J Bone Miner Res 2013; 28: 771-779.
75. Zhang F, Tan LJ, Lei SF, Deng HW. The differences of femoral neck geometric parameters: effects of age, gender and race. Osteoporos Int 2010; 21: 1205-1214.
76. Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA. The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech 1994; 27: 375-389.
77. Keaveny TM, Morgan EF, Niebur GL, Yeh OC. Biomechanics of trabecular bone. Annu Rev Biomed Eng 2001; 3: 307-333.
78. Kim HS, Al-Hassani ST. A morphological model of vertebral trabecular bone. J Biomech 2002; 35: 1101-1114.
79. van Rietbergen B, Odgaard A, Kabel J, Huiskes R. Relationships between bone morphology and bone elastic properties can be accurately quantified using high-resolution computer reconstructions. J Orthop Res 1998; 16: 23-28.
80. Walker MD, Saeed I, McMahon DJ et al. Volumetric bone mineral density at the spine and hip in Chinese American and White women. Osteoporos Int 2012; 23: 2499-2506.
81. Marshall LM, Zmuda JM, Chan BK et al. Race and ethnic variation in proximal femur structure and BMD among older men. J Bone Miner Res 2008; 23: 121-130.
82. 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: theOFELY study. J Bone Miner Res 2007; 22: 425-433.
83. 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: 6508-6515.
84. Sornay-Rendu E, Cabrera-Bravo JL, Boutroy S, Munoz F, Delmas PD. Severity of vertebral fractures is associated with alterations of cortical architecture in postmenopausal women. J Bone Miner Res 2009; 24: 737-743.
85. Kim S,Macdonald HM, Nettlefold L,McKay HA.Acomparison of bone quality at the distal radius between Asian and Caucasian adolescents and young adults: an HR-pQCT study. J Bone Miner Res 2013; 28: 2035-2042.
86. Liu XS, Stein EM, Zhou B et al. Individual trabecula segmentation (ITS)-based morphological analyses and microfinite element analysis of HRpQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J BoneMiner Res 2012; 27: 263-272.
87. Liu XS, Sajda P, Saha PK et al. Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res 2008; 23: 223-235.
88. Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res 2006; 21: 1608-1617.
89. Liu XS, Bevill G, Keaveny TM, Sajda P, Guo XE. Micromechanical analyses of vertebral trabecular bone based on individual trabeculae segmentation of plates and rods. J Biomech 2009; 42: 249-256.
90. Liu XS, Zhang XH, Sekhon KK et al. High-resolution peripheral quantitative computed tomography can assess microstructural and mechanical properties of human distal tibial bone. J Bone Miner Res 2010; 25: 746-756.
91. MacNeil JA, Boyd SK. Load distribution and the predictive power of morphological indices in the distal radius and tibia by high resolution peripheral quantitative computed tomography. Bone 2007; 41: 129-137.
92. Vico L, Zouch M, Amirouche A et al. High-resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res 2008; 23: 1741-1750.
93. Seeman E, Delmas PD. Bone quality-the material and structural basis of bone strength and fragility. N Engl J Med 2006; 354: 2250-2261.
94. Boutroy S, Walker MD, Liu XS et al. Lower cortical porosity and higher tissue mineral density in Chinese-American versus white women. J Bone Miner Res 2014; 29: 551-561.
95. Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA. Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitometry 2011; 14: 302-312.
96. Hans D, Goertzen AL, Krieg MA, Leslie WD. Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 2011; 26: 2762-2769.
97. Boutroy S, Hans D, Sornay-Rendu E, Vilayphiou N, Winzenrieth R, Chapurlat R. Trabecular bone score improves fracture risk prediction in non-osteoporotic women: the OFELY study. Osteoporos Int 2013; 24: 77-85.
98. Silva BC, Walker MD, Abraham A et al. Trabecular bone score is associated with volumetric bone density and microarchitecture as assessed by central QCT and HRpQCT in Chinese American and white women. J Clin Densitometry 2013; 16: 554-561.
99. Cheung CK, Panesar NS, Lau E, Woo J, Swaminathan R. Increased bone resorption and decreased bone formation in Chinese patients with hip fracture. Calcif Tissue Int 1995; 56: 347-349.
100. Zhao J, Xia W, Nie M et al. The levels of bone turnover markers in Chinese postmenopausal women: Peking Vertebral Fracture study. Menopause 2011; 18: 1237-1243.
101. Hu WW, Zhang Z, He JW et al. Establishing reference intervals for bone turnover markers in the healthy shanghai population and the relationship with bone mineral density in postmenopausal women. Int J Endocrinol 2013; 2013: 513925.
102. Tamaki J, Iki M, Kadowaki E et al. Biochemical markers for bone turnover predict risk of vertebral fractures in postmenopausal women over 10 years: the Japanese Population-based Osteoporosis (JPOS) Cohort Study. Osteoporos Int 2013; 24: 887-897.
103. Yan L, Prentice A, Zhou B et al. Age-and gender-related differences in bone mineral status and biochemical markers of bone metabolism in Northern Chinese men and women. Bone 2002; 30: 412-415.
104. Finkelstein JS, Sowers M, Greendale GA et al. Ethnic variation in bone turnover in pre-and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 2002; 87: 3051-3056.
105. Costa AG, Walker MD, Zhang CA et al. Circulating sclerostin levels and markers of bone turnover in Chinese-American and white women. J Clin Endocrinol Metab 2013; 98: 4736-4743.
106. Xu XJ, Shen L, Yang YP et al. Serum sclerostin levels associated with lumbar spine bone mineral density and bone turnover markers in patients with postmenopausal osteoporosis. Chin Med J 2013; 126: 2480-2484.
107. Sheng Z, Tong D, Ou Y et al. Serum sclerostin levels were positively correlated with fat mass and bone mineral density in central south Chinese postmenopausal women. Clin Endocrinol 2012; 76: 797-801.
108. Poole KE, van Bezooijen RL, Loveridge N et al. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J 2005; 19: 1842-1844.
109. van Bezooijen RL, ten Dijke P, Papapoulos SE, Lowik CW. SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev 2005; 16: 319-327.
110. Arasu A, Cawthon PM, Lui LY et al. Serum sclerostin and risk of hip fracture in older Caucasian women. J Clin Endocrinol Metab 2012; 97: 2027-2032.
111. Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R. Bone mineral acquisition in healthy Asian, Hispanic, Black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 1999; 84: 4702-4712.
112. Finkelstein JS, Brockwell SE,MehtaVet al. Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J Clin Endocrinol Metab 2008; 93: 861-868.
113. Duan Y, Wang XF, Evans A, Seeman E. Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone 2005; 36: 987-998.
114. Schousboe JT, Shepherd JA, Bilezikian JP, Baim S. Executive summary of the 2013 International Society for Clinical Densitometry Position Development Conference on bone densitometry. J Clin Densitometry 2013; 16: 455-466.
115. Cauley JA, El-Hajj Fuleihan G, Arabi A et al. Official Positions for FRAX(R) clinical regarding international differences from Joint Official Positions Development Conference of the International Society for Clinical Densitometry and International Osteoporosis Foundation on FRAX(R). J Clin Densitometry 2011; 14: 240-262.
116. Wang X, Sanyal A, CawthonPMet al. Prediction of new clinical vertebral fractures in elderly men using finite element analysis of CT scans. J Bone Miner Res 2012; 27: 808-816.
117. Lau EM, Cooper C, Wickham C, Donnan S, Barker DJ. Hip fracture in Hong Kong and Britain. Int J Epidemiol 1990; 19: 1119-1121.