Review of high-resolution peripheral quantitative computed tomography for the assessment of bone microstructure and strength_Journal of Biomedical Engineering

Authors：

MA Jianxiong ^1,2,3 , ZHAO Jie ^2,3 , HE Weiwei ^2,3 , KUANG Mingjie ^2,3 , CHEN Hengting ^2,3 , ZHANG Lukai ^2,3 , SUN Lei ^2,3 , CUI Yuhong ¹ ,  MA Xinlong ^2,3 , WANG Ying ^2,3

1. School of Mechanical Engineering, Tianjin University, Tianjin 300072, P.R.China;
2. Orthopaedics Institute, Tianjin Hospital, Tianjin 300211, P.R.China;
3. Orthopaedics Institute, Tianjin University Tianjin Hospital, Tianjin 300211, P.R.China;

Corresponding author：

Keywords：

high-resolution peripheral quantitative computed tomography; bone microstructure; bone density; bone strength

DOI：

10.7507/1001-5515.201707068

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Trabecular microstructure is an important factor in determining bone strength and physiological function. Normal X-ray and computed tomography (CT) cannot accurately reflect the microstructure of trabecular bone. High-resolution peripheral quantitative computed tomography (HR-pQCT) is a new imaging technique in recent years. It can qualitatively and quantitatively measure the three-dimensional microstructure and volume bone mineral density of trabecular bone in vivo. It has high precision and relative low dose of radiation. This new imaging tool is helpful for us to understand the trabecular microstructure more deeply. The finite element analysis of HR-pQCT data can be used to predict the bone strength accurately. We can assess the risk of osteoporosis and fracture with three-dimensional reconstructed images and trabecular microstructure parameters. In this review, we summarize the technical flow, data parameters and clinical application of HR-pQCT in order to provide some reference for the popularization and extensive application of HR-pQCT.

Citation： MA Jianxiong, ZHAO Jie, HE Weiwei, KUANG Mingjie, CHEN Hengting, ZHANG Lukai, SUN Lei, CUI Yuhong, MA Xinlong, WANG Ying. Review of high-resolution peripheral quantitative computed tomography for the assessment of bone microstructure and strength. Journal of Biomedical Engineering, 2018, 35(3): 468-474. doi: 10.7507/1001-5515.201707068 Copy

1.	Chiba K, Osaki M. New methods for the evaluation of bone quality. Assessment of bone quality by HR-pQCT. Clin Calcium, 2017, 27(8): 1131-1137.
2.	Bonaretti S, Majumdar S, LANG T F, et al. The comparability of HR-pQCT bone measurements is improved by scanning anatomically standardized regions. Osteoporos Int, 2017, 28(7): 2115-2128.
3.	Fournie C, Pelletier S, Bacchetta J, et al. The relationship between body composition and bone quality measured with HR-pQCT in peritoneal dialysis patients. Perit Dial Int, 2017, 37(5): 548-555.
4.	Manske S L, Davison E M, Burt L A, et al. The estimation of second-generation HR-pQCT from first-generation HR-pQCT using in vivo cross-calibration. J Bone Miner Res, 2017, 32(7): 1514-1524.
5.	Pauchard Y, Ayres F J, Boyd S K. Automated quantification of three-dimensional subject motion to monitor image quality in high-resolution peripheral quantitative computed tomography. Phys Med Biol, 2011, 56(20): 6523-6543.
6.	Sode M, Burghardt A J, Pialat J B, et al. Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone, 2011, 48(6): 1291-1297.
7.	Hosseini H S, Maquer G, Zysset P K. mu CT-based trabecular anisotropy can be reproducibly computed from HR-pQCT scans using the triangulated bone surface. Bone, 2017, 97: 114-120.
8.	Kroker A, ZHU Ying, Manske S L, et al. Quantitative in vivo assessment of bone microarchitecture in the human knee using HR-pQCT. Bone, 2017, 97: 43-48.
9.	Boutroy S, Bouxsein M L, Munoz F, et al. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab, 2005, 90(12): 6508-6515.
10.	Shi Lin, Wang Defeng, Hung V W, et al. Fast and accurate 3-D registration of HR-pQCT images. IEEE Trans Inf Technol Biomed, 2010, 14(5): 1291-1297.
11.	Putman M S, Yu E W, Lin D, et al. Differences in trabecular microstructure between black and white women assessed by individual trabecular segmentation analysis of HR-pQCT images. J Bone Miner Res, 2017, 32(5): 1100-1108.
12.	Edwards M H, Paccou J, Ward K A, et al. The relationship of bone properties using high resolution peripheral quantitative computed tomography to radiographic components of hip osteoarthritis. Osteoarthritis Cartilage, 2017, 25: 1478-1483.
13.	Manske S L, Zhu Ying, Sandino C, et al. Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone, 2015, 79: 213-221.
14.	Pialat J B, Burghardt A J, Sode M, et al. 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(1): 111-118.
15.	Okazaki N, Burghardt A J, Chiba K, et al. Bone microstructure in men assessed by HR-pQCT: Associations with risk factors and differences between men with normal, low, and osteoporosis-range areal BMD. Bone reports, 2016, 5: 312-319.
16.	Stauber M, Müller R. Volumetric spatial decomposition of trabecular bone into rods and plates--a new method for local bone morphometry. Bone, 2006, 38(4): 475-484.
17.	Odgaard A, Gundersen H J. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone, 1993, 14(2): 173-182.
18.	Liu X S, Cohen A, Shane E, et al. Individual trabeculae segmentation (ITS)-based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res, 2010, 25(7): 1496-1505.
19.	Buie H R, Campbell G M, Klinck R, et al. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone, 2007, 41(4): 505-515.
20.	Valentinitsch A, Patsch J M, Deutschmann J, et al. Automated threshold-independent cortex segmentation by 3D-texture analysis of HR-pQCT scans. Bone, 2012, 51(3): 480-487.
21.	Kawalilak C E, Johnston J D, Cooper D, et al. Role of endocortical contouring methods on precision of HR-pQCT-derived cortical micro-architecture in postmenopausal women and young adults. Osteoporos Int, 2016, 27(2): 789-796.
22.	Barnabe C, Szabo E, Martin L, et al. Quantification of small joint space width, periarticular bone microstructure and erosions using high-resolution peripheral quantitative computed tomography in rheumatoid arthritis. Clin Exp Rheumatol, 2013, 31(2): 243-250.
23.	Nishiyama K K, Macdonald H M, Hanley D A, et al. Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT. Osteoporos Int, 2013, 24(5): 1733-1740.
24.	Nishiyama K K, Macdonald H M, Buie H R, et al. 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, 2010, 25(4): 882-890.
25.	Liu X S, Shane E, McMahon D J, et al. Individual trabecula segmentation (ITS)-based morphological analysis of microscale images of human tibial trabecular bone at limited spatial resolution. J Bone Miner Res, 2011, 26(9): 2184-2193.
26.	Tjong W, Kazakia G J, Burghardt A J. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys, 2012, 39(4): 1893-1903.
27.	Burghardt A J, Buie H R, Laib A, et al. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone, 2010, 47(3): 519-528.
28.	Burghardt A J, Link T M, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res, 2011, 469(8): 2179-2193.
29.	Engelke K, Stampa B, Timm W, et al. Short-term in vivo precision of BMD and parameters of trabecular architecture at the distal forearm and tibia. Osteoporos Int, 2012, 23(8): 2151-2158.
30.	Krause M, Museyko O, Breer S, et al. Accuracy of trabecular structure by HR-pQCT compared to gold standard μCT in the radius and tibia of patients with osteoporosis and long-term bisphosphonate therapy. Osteoporos Int, 2014, 25(5): 1595-1606.
31.	Nishiyama K K, Macdonald H M, Moore S A, et al. Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: An HR-pQCT study. J Bone Miner Res, 2012, 27(2): 273-282.
32.	Farr J N, Dimitri P. The impact of fat and obesity on bone microarchitecture and strength in children. Calcif Tissue Int, 2017, 100(5, SI): 500-513.
33.	Kelley J C, Crabtree N, Zemel B S. Bone density in the obese child: clinical considerations and diagnostic challenges. Calcif Tissue Int, 2017, 100(5, SI): 514-527.
34.	Nirody J A, Cheng K P, Parrish R M, et al. Spatial distribution of intracortical porosity varies across age and sex. Bone, 2015, 75: 88-95.
35.	Burt L A, Macdonald H M, Hanley D A, et al. Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch Osteoporos, 2014, 9: 183.
36.	Fuller H, Fuller R, Pereira R M. High resolution peripheral quantitative computed tomography for the assessment of morphological and mechanical bone parameters. Rev Bras Reumatol, 2015, 55(4): 352-362.
37.	Hung V W, Zhu T Y, Cheung W H, et al. Age-related differences in volumetric bone mineral density, microarchitecture, and bone strength of distal radius and tibia in Chinese women: a high-resolution pQCT reference database study. Osteoporos Int, 2015, 26(6): 1691-1703.
38.	Cheung A M, Adachi J D, Hanley D A, et al. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep, 2013, 11(2): 136-146.
39.	Macdonald H M, Nishiyama K K, Kang Jian, et al. Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-Based HR-pQCT study. J Bone Miner Res, 2011, 26(1): 50-62.
40.	Farr J N, Khosla S. Skeletal changes through the lifespan-from growth to senescence. Nat Rev Endocrinol, 2015, 11(9): 513-521.
41.	Bjornerem A, Ghasem-Zadeh A, Bui M, et al. Remodeling markers are associated with larger intracortical surface area but smaller trabecular surface area: A twin study. Bone, 2011, 49(6): 1125-1130.
42.	Burghardt A J, Kazakia G J, Sode M, et al. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res, 2010, 25(12): 2558-2571.
43.	Cheung A M, Majumdar S, Brixen K, et al. Effects of odanacatib on the radius and tibia of postmenopausal women: improvements in bone geometry, microarchitecture, and estimated bone strength. J Bone Miner Res, 2014, 29(8): 1786-1794.
44.	Bala Y, Chapurlat R, Cheung A M, et al. Risedronate slows or partly reverses cortical and trabecular microarchitectural deterioration in postmenopausal women. J Bone Miner Res, 2014, 29(2): 380-388.
45.	Rizzoli R, Laroche M, Krieg M A, et al. Strontium ranelate and alendronate have differing effects on distal tibia bone microstructure in women with osteoporosis. Rheumatol Int, 2010, 30(10): 1341-1348.
46.	Rizzoli R, Chapurlat R D, Laroche J M, et al. Effects of strontium ranelate and alendronate on bone microstructure in women with osteoporosis results of a 2-year study. Osteoporos Int, 2012, 23(1): 305-315.
47.	MacDonald H M, Nishiyama K K, Hanley D A, et al. Changes in trabecular and cortical bone microarchitecture at peripheral sites associated with 18 months of teriparatide therapy in postmenopausal women with osteoporosis. Osteoporos Int, 2011, 22(1): 357-362.
48.	Tsai J N, Uihlein A V, Burnett-Bowie S, et al. Comparative effects of teriparatide, denosumab, and combination therapy on peripheral compartmental bone density, microarchitecture, and estimated strength: the DATA-HRpQCT study. J Bone Miner Res, 2015, 30(1): 39-45.
49.	Chapurlat R D, Laroche M, Thomas T, et al. Effect of oral monthly ibandronate on bone microarchitecture in women with osteopenia-a randomized placebo-controlled trial. Osteoporos Int, 2013, 24(1): 311-320.
50.	Vilayphiou N, Boutroy S, Szulc P, et al. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res, 2011, 26(5): 965-973.
51.	Macneil J A, Boyd S K. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone, 2008, 42(6): 1203-1213.
52.	Karasik D, Demissie S, Lu D, et al. Bone strength estimated by micro-finite element analysis (μFEA) is heritable and shares genetic predisposition with areal BMD: the framingham study. J Bone Miner Res, 2017, 32(11): 2151-2156.
53.	Okazaki R. Bone architecture and strength in diabetes mellitus. Clin Calcium, 2013, 23(7): 1001-1006.
54.	Wesseling-Perry K, Bacchetta J. CKD-MBD after kidney transplantation. Pediatr Nephrol, 2011, 26(12): 2143-2151.
55.	Patsch J M, Burghardt A J, Yap S P, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res, 2013, 28(2): 313-324.
56.	Ostertag A, Collet C, Chappard C A, et al. A case-control study of fractures in men with idiopathic osteoporosis: Fractures are associated with older age and low cortical bone density. Bone, 2013, 52(1): 48-55.
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1. Chiba K, Osaki M. New methods for the evaluation of bone quality. Assessment of bone quality by HR-pQCT. Clin Calcium, 2017, 27(8): 1131-1137.
2. Bonaretti S, Majumdar S, LANG T F, et al. The comparability of HR-pQCT bone measurements is improved by scanning anatomically standardized regions. Osteoporos Int, 2017, 28(7): 2115-2128.
3. Fournie C, Pelletier S, Bacchetta J, et al. The relationship between body composition and bone quality measured with HR-pQCT in peritoneal dialysis patients. Perit Dial Int, 2017, 37(5): 548-555.
4. Manske S L, Davison E M, Burt L A, et al. The estimation of second-generation HR-pQCT from first-generation HR-pQCT using in vivo cross-calibration. J Bone Miner Res, 2017, 32(7): 1514-1524.
5. Pauchard Y, Ayres F J, Boyd S K. Automated quantification of three-dimensional subject motion to monitor image quality in high-resolution peripheral quantitative computed tomography. Phys Med Biol, 2011, 56(20): 6523-6543.
6. Sode M, Burghardt A J, Pialat J B, et al. Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone, 2011, 48(6): 1291-1297.
7. Hosseini H S, Maquer G, Zysset P K. mu CT-based trabecular anisotropy can be reproducibly computed from HR-pQCT scans using the triangulated bone surface. Bone, 2017, 97: 114-120.
8. Kroker A, ZHU Ying, Manske S L, et al. Quantitative in vivo assessment of bone microarchitecture in the human knee using HR-pQCT. Bone, 2017, 97: 43-48.
9. Boutroy S, Bouxsein M L, Munoz F, et al. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab, 2005, 90(12): 6508-6515.
10. Shi Lin, Wang Defeng, Hung V W, et al. Fast and accurate 3-D registration of HR-pQCT images. IEEE Trans Inf Technol Biomed, 2010, 14(5): 1291-1297.
11. Putman M S, Yu E W, Lin D, et al. Differences in trabecular microstructure between black and white women assessed by individual trabecular segmentation analysis of HR-pQCT images. J Bone Miner Res, 2017, 32(5): 1100-1108.
12. Edwards M H, Paccou J, Ward K A, et al. The relationship of bone properties using high resolution peripheral quantitative computed tomography to radiographic components of hip osteoarthritis. Osteoarthritis Cartilage, 2017, 25: 1478-1483.
13. Manske S L, Zhu Ying, Sandino C, et al. Human trabecular bone microarchitecture can be assessed independently of density with second generation HR-pQCT. Bone, 2015, 79: 213-221.
14. Pialat J B, Burghardt A J, Sode M, et al. 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(1): 111-118.
15. Okazaki N, Burghardt A J, Chiba K, et al. Bone microstructure in men assessed by HR-pQCT: Associations with risk factors and differences between men with normal, low, and osteoporosis-range areal BMD. Bone reports, 2016, 5: 312-319.
16. Stauber M, Müller R. Volumetric spatial decomposition of trabecular bone into rods and plates--a new method for local bone morphometry. Bone, 2006, 38(4): 475-484.
17. Odgaard A, Gundersen H J. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone, 1993, 14(2): 173-182.
18. Liu X S, Cohen A, Shane E, et al. Individual trabeculae segmentation (ITS)-based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res, 2010, 25(7): 1496-1505.
19. Buie H R, Campbell G M, Klinck R, et al. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone, 2007, 41(4): 505-515.
20. Valentinitsch A, Patsch J M, Deutschmann J, et al. Automated threshold-independent cortex segmentation by 3D-texture analysis of HR-pQCT scans. Bone, 2012, 51(3): 480-487.
21. Kawalilak C E, Johnston J D, Cooper D, et al. Role of endocortical contouring methods on precision of HR-pQCT-derived cortical micro-architecture in postmenopausal women and young adults. Osteoporos Int, 2016, 27(2): 789-796.
22. Barnabe C, Szabo E, Martin L, et al. Quantification of small joint space width, periarticular bone microstructure and erosions using high-resolution peripheral quantitative computed tomography in rheumatoid arthritis. Clin Exp Rheumatol, 2013, 31(2): 243-250.
23. Nishiyama K K, Macdonald H M, Hanley D A, et al. Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT. Osteoporos Int, 2013, 24(5): 1733-1740.
24. Nishiyama K K, Macdonald H M, Buie H R, et al. 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, 2010, 25(4): 882-890.
25. Liu X S, Shane E, McMahon D J, et al. Individual trabecula segmentation (ITS)-based morphological analysis of microscale images of human tibial trabecular bone at limited spatial resolution. J Bone Miner Res, 2011, 26(9): 2184-2193.
26. Tjong W, Kazakia G J, Burghardt A J. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys, 2012, 39(4): 1893-1903.
27. Burghardt A J, Buie H R, Laib A, et al. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone, 2010, 47(3): 519-528.
28. Burghardt A J, Link T M, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res, 2011, 469(8): 2179-2193.
29. Engelke K, Stampa B, Timm W, et al. Short-term in vivo precision of BMD and parameters of trabecular architecture at the distal forearm and tibia. Osteoporos Int, 2012, 23(8): 2151-2158.
30. Krause M, Museyko O, Breer S, et al. Accuracy of trabecular structure by HR-pQCT compared to gold standard μCT in the radius and tibia of patients with osteoporosis and long-term bisphosphonate therapy. Osteoporos Int, 2014, 25(5): 1595-1606.
31. Nishiyama K K, Macdonald H M, Moore S A, et al. Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: An HR-pQCT study. J Bone Miner Res, 2012, 27(2): 273-282.
32. Farr J N, Dimitri P. The impact of fat and obesity on bone microarchitecture and strength in children. Calcif Tissue Int, 2017, 100(5, SI): 500-513.
33. Kelley J C, Crabtree N, Zemel B S. Bone density in the obese child: clinical considerations and diagnostic challenges. Calcif Tissue Int, 2017, 100(5, SI): 514-527.
34. Nirody J A, Cheng K P, Parrish R M, et al. Spatial distribution of intracortical porosity varies across age and sex. Bone, 2015, 75: 88-95.
35. Burt L A, Macdonald H M, Hanley D A, et al. Bone microarchitecture and strength of the radius and tibia in a reference population of young adults: an HR-pQCT study. Arch Osteoporos, 2014, 9: 183.
36. Fuller H, Fuller R, Pereira R M. High resolution peripheral quantitative computed tomography for the assessment of morphological and mechanical bone parameters. Rev Bras Reumatol, 2015, 55(4): 352-362.
37. Hung V W, Zhu T Y, Cheung W H, et al. Age-related differences in volumetric bone mineral density, microarchitecture, and bone strength of distal radius and tibia in Chinese women: a high-resolution pQCT reference database study. Osteoporos Int, 2015, 26(6): 1691-1703.
38. Cheung A M, Adachi J D, Hanley D A, et al. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian Bone Strength Working Group. Curr Osteoporos Rep, 2013, 11(2): 136-146.
39. Macdonald H M, Nishiyama K K, Kang Jian, et al. Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-Based HR-pQCT study. J Bone Miner Res, 2011, 26(1): 50-62.
40. Farr J N, Khosla S. Skeletal changes through the lifespan-from growth to senescence. Nat Rev Endocrinol, 2015, 11(9): 513-521.
41. Bjornerem A, Ghasem-Zadeh A, Bui M, et al. Remodeling markers are associated with larger intracortical surface area but smaller trabecular surface area: A twin study. Bone, 2011, 49(6): 1125-1130.
42. Burghardt A J, Kazakia G J, Sode M, et al. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res, 2010, 25(12): 2558-2571.
43. Cheung A M, Majumdar S, Brixen K, et al. Effects of odanacatib on the radius and tibia of postmenopausal women: improvements in bone geometry, microarchitecture, and estimated bone strength. J Bone Miner Res, 2014, 29(8): 1786-1794.
44. Bala Y, Chapurlat R, Cheung A M, et al. Risedronate slows or partly reverses cortical and trabecular microarchitectural deterioration in postmenopausal women. J Bone Miner Res, 2014, 29(2): 380-388.
45. Rizzoli R, Laroche M, Krieg M A, et al. Strontium ranelate and alendronate have differing effects on distal tibia bone microstructure in women with osteoporosis. Rheumatol Int, 2010, 30(10): 1341-1348.
46. Rizzoli R, Chapurlat R D, Laroche J M, et al. Effects of strontium ranelate and alendronate on bone microstructure in women with osteoporosis results of a 2-year study. Osteoporos Int, 2012, 23(1): 305-315.
47. MacDonald H M, Nishiyama K K, Hanley D A, et al. Changes in trabecular and cortical bone microarchitecture at peripheral sites associated with 18 months of teriparatide therapy in postmenopausal women with osteoporosis. Osteoporos Int, 2011, 22(1): 357-362.
48. Tsai J N, Uihlein A V, Burnett-Bowie S, et al. Comparative effects of teriparatide, denosumab, and combination therapy on peripheral compartmental bone density, microarchitecture, and estimated strength: the DATA-HRpQCT study. J Bone Miner Res, 2015, 30(1): 39-45.
49. Chapurlat R D, Laroche M, Thomas T, et al. Effect of oral monthly ibandronate on bone microarchitecture in women with osteopenia-a randomized placebo-controlled trial. Osteoporos Int, 2013, 24(1): 311-320.
50. Vilayphiou N, Boutroy S, Szulc P, et al. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res, 2011, 26(5): 965-973.
51. Macneil J A, Boyd S K. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone, 2008, 42(6): 1203-1213.
52. Karasik D, Demissie S, Lu D, et al. Bone strength estimated by micro-finite element analysis (μFEA) is heritable and shares genetic predisposition with areal BMD: the framingham study. J Bone Miner Res, 2017, 32(11): 2151-2156.
53. Okazaki R. Bone architecture and strength in diabetes mellitus. Clin Calcium, 2013, 23(7): 1001-1006.
54. Wesseling-Perry K, Bacchetta J. CKD-MBD after kidney transplantation. Pediatr Nephrol, 2011, 26(12): 2143-2151.
55. Patsch J M, Burghardt A J, Yap S P, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res, 2013, 28(2): 313-324.
56. Ostertag A, Collet C, Chappard C A, et al. A case-control study of fractures in men with idiopathic osteoporosis: Fractures are associated with older age and low cortical bone density. Bone, 2013, 52(1): 48-55.
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