Fractal lacunarity of trabecular bone and magnetic resonance imaging: New perspectives for osteoporotic fracture risk assessment

World Journal of Orthopedics

Volumn 6, Issue 2, 2015, Pages 221-235

  Zaia, Annamaria ^a  

^a INRCA   (Italy)

Author keywords

Fractal analysis; Fractal lacunarity; Fracture risk; Osteoporosis; Trabecular bone microarchitecture

Indexed keywords

EID: 84928950028     PISSN: None     EISSN: 22185836     Source Type: Journal    
DOI: 10.5312/wjo.v6.i2.221     Document Type: Review

References (98)

1. Lau EM. Preventing osteoporosis in every day life. Clin Calcium 2004; 14: 430-434 [PMID: 15577003]
2. Mirza FS, Prestwood KM. Bone health and aging: implications for menopause. Endocrinol Metab Clin North Am 2004; 33: 741-759 [PMID: 15501643 DOI: 10.1016/j.ecl.2004.07.001]
3. Ismail AA, O'Neill TW, Cooper C, Finn JD, Bhalla AK, Cannata JB, Delmas P, Falch JA, Felsch B, Hoszowski K, Johnell O, Diaz-Lopez JB, Lopez Vaz A, Marchand F, Raspe H, Reid DM, Todd C, Weber K, Woolf A, Reeve J, Silman AJ. Mortality associated with vertebral deformity in men and women: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 1998; 8: 291-297 [PMID: 9797915 DOI: 10.1007/s001980050067]
4. O'Neill TW, Felsenberg D, Varlow J, Cooper C, Kanis JA, Silman AJ. The prevalence of vertebral deformity in european men and women: the European Vertebral Osteoporosis Study. J Bone Miner Res 1996; 11: 1010-1018 [PMID: 8797123]
5. Cauley JA, Harrison SL, Cawthon PM, Ensrud KE, Danielson ME, Orwoll E, Mackey DC. Objective measures of physical activity, fractures and falls: the osteoporotic fractures in men study. J Am Geriatr Soc 2013; 61: 1080-1088 [PMID: 23855842]
6. Kiebzak GM. Age-related bone changes. Exp Gerontol 1991; 26: 171-187 [PMID: 1915689]
7. Audran M, Chappard D, Legrand E, Libouban H, Baslé MF. Bone microarchitecture and bone fragility in men: DXA and histomorphometry in humans and in the orchidectomized rat model. Calcif Tissue Int 2001; 69: 214-217 [PMID: 11730253]
8. Johnell O, Kanis J, Gullberg G. Mortality, morbidity, and assessment of fracture risk in male osteoporosis. Calcif Tissue Int 2001; 69: 182-184 [PMID: 11730245 DOI: 10.1007/s00223-001-1045-7]
9. Seeman E. Unresolved issues in osteoporosis in men. Rev Endocr Metab Disord 2001; 2: 45-64 [PMID: 11704979 DOI: 10.1023/A:1010054924085]
10. Elliot-Gibson V, Bogoch ER, Jamal SA, Beaton DE. Practice patterns in the diagnosis and treatment of osteoporosis after a fragility fracture: a systematic review. Osteoporos Int 2004; 15: 767-778 [PMID: 15258724]
11. Kanis JA, Borgstrom F, De Laet C, Johansson H, Johnell O, Jonsson B, Oden A, Zethraeus N, Pfleger B, Khaltaev N. Assessment of fracture risk. Osteoporos Int 2005; 16: 581-589 [PMID: 15616758 DOI: 10.1007/s00198-004-1780-5]
12. Solomon DH, Finkelstein JS, Katz JN, Mogun H, Avorn J. Underuse of osteoporosis medications in elderly patients with fractures. Am J Med 2003; 115: 398-400 [PMID: 14553876 DOI: 10.1016/S0002-9343(03)00357-7]
13. Lindsay R, Silverman SL, Cooper C, Hanley DA, Barton I, Broy SB, Licata A, Benhamou L, Geusens P, Flowers K, Stracke H, Seeman E. Risk of new vertebral fracture in the year following a fracture. JAMA 2001; 285: 320-323 [PMID: 11176842]
14. Hough S. Fast and slow bone losers. Relevance to the management of osteoporosis. Drugs Aging 1998; 12 Suppl 1: 1-7 [PMID: 9673860 DOI: 10.2165/00002512-199812001-00001]
15. National Osteoporosis Society. The use of quantitative ultrasound in the management of osteoporosis. 2002
16. Frost ML, Blake GM, Fogelman I. Contact quantitative ultrasound: an evaluation of precision, fracture discrimination, age-related bone loss and applicability of the WHO criteria. Osteoporos Int 1999; 10: 441-449 [PMID: 10663343 DOI: 10.1007/s001980050252]
17. Guglielmi G, Njeh CF, de Terlizzi F, De Serio DA, Scillitani A, Cammisa M, Fan B, Lu Y, Genant HK. Palangeal quantitative ultrasound, phalangeal morphometric variables, and vertebral fracture discrimination. Calcif Tissue Int 2003; 72: 469-477 [PMID: 12574870]
18. Stewart A, Felsenberg D, Eastell R, Roux C, Glüer CC, Reid DM. Relationship between risk factors and QUS in a European Population: The OPUS study. Bone 2006; 39: 609-615 [PMID: 16644296]
19. Bauer DC, Glüer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, Black DM. 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 1997; 157: 629-634 [PMID: 9080917 DOI: 10.1001/archinte.1997.00440270067006]
20. Cheng S, Tylavsky F, Carbone L. Utility of ultrasound to assess risk of fracture. J Am Geriatr Soc 1997; 45: 1382-1394 [PMID: 9361666]
21. Hans D, Wu C, Njeh CF, Zhao S, Augat P, Newitt D, Link T, Lu Y, Majumdar S, Genant HK. Ultrasound velocity of trabecular cubes reflects mainly bone density and elasticity. Calcif Tissue Int 1999; 64: 18-23 [PMID: 9868278 DOI: 10.1007/s002239900572]
22. Pinheiro MM, Castro CH, Frisoli A, Szejnfeld VL. Discriminatory ability of quantitative ultrasound measurements is similar to dual-energy X-ray absorptiometry in a Brazilian women population with osteoporotic fracture. Calcif Tissue Int 2003; 73: 555-564 [PMID: 14517710]
23. Helgason B, Perilli E, Schileo E, Taddei F, Brynjólfsson S, Viceconti M. Mathematical relationships between bone density and mechanical properties: a literature review. Clin Biomech (Bristol, Avon) 2008; 23: 135-146 [PMID: 17931759 DOI: 10.1016/j.clinbi omech.2007.08.024]
24. Seeman E. Is a change in bone mineral density a sensitive and specific surrogate of anti-fracture efficacy? Bone 2007; 41: 308-317 [PMID: 17644058]
25. Dalle Carbonare L, Giannini S. Bone microarchitecture as an important determinant of bone strength. J Endocrinol Invest 2004; 27: 99-105 [PMID: 15053252 DOI: 10.1007/BF03350919]
26. Cortet B, Dubois P, Boutry N, Bourel P, Cotten A, Marchandise X. Image analysis of the distal radius trabecular network using computed tomography. Osteoporos Int 1999; 9: 410-419 [PMID: 10550460 DOI: 10.1007/s001980050165]
27. Gordon CL, Webber CE, Adachi JD, Christoforou N. In vivo assessment of trabecular bone structure at the distal radius from high-resolution computed tomography images. Phys Med Biol 1996; 41: 495-508 [PMID: 8778828 DOI: 10.1088/0031-9155/41/3/011]
28. Feltrin GP, Macchi V, Saccavini C, Tosi E, Dus C, Fassina A, Parenti A, De Caro R. Fractal analysis of lumbar vertebral cancellous bone architecture. Clin Anat 2001; 14: 414-417 [PMID: 11754235 DOI: 10.1002/ca.1076]
29. Gregory JS, Stewart A, Undrill PE, Reid DM, Aspden RM. Identification of hip fracture patients from radiographs using Fourier analysis of the trabecular structure: a cross-sectional study. BMC Med Imaging 2004; 4: 4 [PMID: 15469614]
30. Oka K, Kumasaka S, Kashima I. Assessment of bone feature parameters from lumbar trabecular skeletal patterns using mathematical morphology image processing. J Bone Miner Metab 2002; 20: 201-208 [PMID: 12115065 DOI: 10.1007/s007740200029]
31. Majumdar S. A review of magnetic resonance (MR) imaging of trabecular bone micro-architecture: contribution to the prediction of biomechanical properties and fracture prevalence. Technol Health Care 1998; 6: 321-327 [PMID: 10100935]
32. Krug R, Burghardt AJ, Majumdar S, Link TM. High-resolution imaging techniques for the assessment of osteoporosis. Radiol Clin North Am 2010; 48: 601-621 [PMID: 20609895]
33. Wehrli FW, Leonard MB, Saha PK, Gomberg BR. Quantitative high-resolution magnetic resonance imaging reveals structural implications of renal osteodystrophy on trabecular and cortical bone. J Magn Reson Imaging 2004; 20: 83-89 [PMID: 15221812]
34. Krug R, Carballido-Gamio J, Burghardt AJ, Kazakia G, Hyun BH, Jobke B, Banerjee S, Huber M, Link TM, Majumdar S. Assessment of trabecular bone structure comparing magnetic resonance imaging at 3 Tesla with high-resolution peripheral quantitative computed tomography ex vivo and in vivo. Osteoporos Int 2008; 19: 653-661 [PMID: 17992467]
35. Majumdar S. Magnetic resonance imaging for osteoporosis. Skeletal Radiol 2008; 37: 95-97 [PMID: 18034342 DOI: 10.1007/s00256-007-0412-5]
36. Phan CM, Matsuura M, Bauer JS, Dunn TC, Newitt D, Lochmueller EM, Eckstein F, Majumdar S, Link TM. Trabecular bone structure of the calcaneus: comparison of MR imaging at 3.0 and 1.5 T with micro-CT as the standard of reference. Radiology 2006; 239: 488-496 [PMID: 16569786 DOI: 10.1148/radiol.2392050574]
37. Delmas PD, Li Z, Cooper C. Relationship between changes in bone mineral density and fracture risk reduction with antiresorptive drugs: some issues with meta-analyses. J Bone Miner Res 2004; 19: 330-337 [PMID: 14969404]
38. Krug R, Han ET, Banerjee S, Majumdar S. Fully balanced steady-state 3D-spin-echo (bSSSE) imaging at 3 Tesla. Magn Reson Med 2006; 56: 1033-1040 [PMID: 16986110]
39. Wehrli FW. Structural and functional assessment of trabecular and cortical bone by micro magnetic resonance imaging. J Magn Reson Imaging 2007; 25: 390-409 [PMID: 17260403]
40. Hipp JA, Jansujwicz A, Simmons CA, Snyder BD. Trabecular bone morphology from micro-magnetic resonance imaging. J Bone Miner Res 1996; 11: 286-297 [PMID: 8822353]
41. Wehrli FW, Gomberg BR, Saha PK, Song HK, Hwang SN, Snyder PJ. Digital topological analysis of in vivo magnetic resonance microimages of trabecular bone reveals structural implications of osteoporosis. J Bone Miner Res 2001; 16: 1520-1531 [PMID: 11499875]
42. Laib A, Newitt DC, Lu Y, Majumdar S. New model-independent measures of trabecular bone structure applied to in vivo high-resolution MR images. Osteoporos Int 2002; 13: 130-136 [PMID: 11905523 DOI: 10.1007/s001980200004]
43. Wehrli FW, Hwang SN, Ma J, Song HK, Ford JC, Haddad JG. Cancellous bone volume and structure in the forearm: noninvasive assessment with MR microimaging and image processing. Radiology 1998; 206: 347-357 [PMID: 9457185]
44. Griffith JF, Genant HK. Bone mass and architecture determination: state of the art. Best Pract Res Clin Endocrinol Metab 2008; 22: 737-764 [PMID: 19028355]
45. Ettinger B, Black DM, Mitlak BH, Knickerbocker RK, Nickelsen T, Genant HK, Christiansen C, Delmas PD, Zanchetta JR, Stakkestad J, Glüer CC, Krueger K, Cohen FJ, Eckert S, Ensrud KE, Avioli LV, Lips P, Cummings SR. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. JAMA 1999; 282: 637-645 [PMID: 10517716]
46. Chesnut CH, Majumdar S, Newitt DC, Shields A, Van Pelt J, Laschansky E, Azria M, Kriegman A, Olson M, Eriksen EF, Mindeholm L. Effects of salmon calcitonin on trabecular microarchitecture as determined by magnetic resonance imaging: results from the QUEST study. J Bone Miner Res 2005; 20: 1548-1561 [PMID: 16059627]
47. Zhang XH, Liu XS, Vasilic B, Wehrli FW, Benito M, Rajapakse CS, Snyder PJ, Guo XE. In vivo microMRI-based finite element and morphological analyses of tibial trabecular bone in eugonadal and hypogonadal men before and after testosterone treatment. J Bone Miner Res 2008; 23: 1426-1434 [PMID: 18410234]
48. Folkesson J, Goldenstein J, Carballido-Gamio J, Kazakia G, Burghardt AJ, Rodriguez A, Krug R, de Papp AE, Link TM, Majumdar S. Longitudinal evaluation of the effects of alendronate on MRI bone microarchitecture in postmenopausal osteopenic women. Bone 2011; 48: 611-621 [PMID: 21059422]
49. Damilakis J, Maris TG, Karantanas AH. An update on the assessment of osteoporosis using radiologic techniques. Eur Radiol 2007; 17: 1591-1602 [PMID: 17131124]
50. Krug R, Stehling C, Kelley DA, Majumdar S, Link TM. Imaging of the musculoskeletal system in vivo using ultra-high field magnetic resonance at 7 T. Invest Radiol 2009; 44: 613-618 [PMID: 19652609]
51. Boutry N, Cortet B, Dubois P, Marchandise X, Cotten A. Trabecular bone structure of the calcaneus: preliminary in vivo MR imaging assessment in men with osteoporosis. Radiology 2003; 227: 708-717 [PMID: 12676974 DOI: 10.1148/radiol.2273020420]
52. Cortet B, Dubois P, Boutry N, Varlet E, Cotten A, Marchandise X. Does high-resolution computed tomography image analysis of the distal radius provide information independent of bone mass? J Clin Densitom 2000; 3: 339-351 [PMID: 11175914 DOI: 10.1385/JCD:3:4:339]
53. Daubechies I. Ten Lectures on Wavelets. Society for Industrial and Applied Mathematics. Philadelphia, 1992 [DOI: 10.1137/1.9781611970104]
54. Bullmore E, Fadili J, Maxim V, Sendur L, Whitcher B, Suckling J, Brammer M, Breakspear M. Wavelets and functional magnetic resonance imaging of the human brain. Neuroimage 2004; 23 Suppl 1: S234-S249 [PMID: 15501094 DOI: 10.1016/j.neuroimag e.2004.07.012]
55. Faber TD, Yoon DC, Service SK, White SC. Fourier and wavelet analyses of dental radiographs detect trabecular changes in osteoporosis. Bone 2004; 35: 403-411 [PMID: 15268890]
56. Lee WL, Chen YC, Hsieh KS. Ultrasonic liver tissues classification by fractal feature vector based on M-band wavelet transform. IEEE Trans Med Imaging 2003; 22: 382-392 [PMID: 12760555]
57. Zaia A, Eleonori R, Maponi P, Rossi R, Murri R. Medical Imaging and Osteoporosis: Fractal's Lacunarity Analysis of Trabecular Bone in MR Images. In Tsymbal A and Cunningham P, editors. Proceedings - Eighteenth IEEE Symposium on Computer-Based Medical Systems-CBMS 2005. Los Alamitos CA: IEEE Computer Society Press, 2005: 3-8
58. Zaia A, Eleonori R, Maponi P, Rossi R, Murri R. MR imaging and osteoporosis: fractal lacunarity analysis of trabecular bone. IEEE Trans Inf Technol Biomed 2006; 10: 484-489 [PMID: 16871715]
59. Zaia A, Rossi R, Egidi N, Maponi P: Fractal's lacunarity analysis of trabecular bone in MR images. In Tavares J and Jorge N, editors. Computational Vision and Medical Image Processing, VipIMAGE 2009. London: CRC Press - Taylor and Francis Group, 2010: 95-100
60. Cross SS. Fractals in pathology. J Pathol 1997; 182: 1-8 [PMID: 9227334 DOI: 10.1002/(SICI)1096-9896(199705)182:1<1::AIDPATH808>3.0.CO;2-B]
61. Lipsitz LA, Goldberger AL. Loss of 'complexity' and aging. Potential applications of fractals and chaos theory to senescence. JAMA 1992; 267: 1806-1809 [PMID: 1482430 DOI: 10.1001/jama.1992.03480130122036]
62. Losa GA, Nonnenmacher TF. Self-similarity and fractal irregularity in pathologic tissues. Mod Pathol 1996; 9: 174-182 [PMID: 8685210]
63. Mandelbrot BB. The Fractal Geometry of Nature. New York: WH Freeman, 1982
64. Vaillancourt DE, Newell KM. Changing complexity in human behavior and physiology through aging and disease. Neurobiol Aging 2002; 23: 1-11 [PMID: 11755010 DOI: 10.1016/S0197-4580(01)00247-0]
65. Zaia A. Osteoporosis and fracture risk: new perspectives for early diagnosis and treatment assessment. In: Mattingly BE and Pillare AC, editors. Osteoporosis: Etiology, Diagnosis and Treatment. New York: Nova Science Publishers Inc, 2009: 267-290
66. Zaia A. Complexity, Chaos, and Fractality in Aging: Fractal lacunarity can measure physio/pathologic aging. J Nutr Health Aging 2009; 13 Supp 1: S217-218
67. Goldberger AL. Non-linear dynamics for clinicians: chaos theory, fractals, and complexity at the bedside. Lancet 1996; 347: 1312-1314 [PMID: 8622511 DOI: 10.1016/S0140-6736(96)90948-4]
68. Goldberger AL. Fractal variability versus pathologic periodicity: complexity loss and stereotypy in disease. Perspect Biol Med 1997; 40: 543-561 [PMID: 9269744]
69. Goldberger AL, Peng CK, Lipsitz LA. What is physiologic complexity and how does it change with aging and disease? Neurobiol Aging 2002; 23: 23-26 [PMID: 11755014 DOI: 10.1016/S0197-4580(01)00266-4]
70. Goldberger AL, Rigney DR, West BJ. Chaos and fractals in human physiology. Sci Am 1990; 262: 42-49 [PMID: 2296715 DOI: 10.1038/scientificamerican0290-42]
71. Kyriazis M. Practical applications of chaos theory to the modulation of human ageing: nature prefers chaos to regularity. Biogerontology 2003; 4: 75-90 [PMID: 12766532 DOI: 10.1023/A:1023306419861]
72. Cross SS, Start RD, Silcocks PB, Bull AD, Cotton DW, Underwood JC. Quantitation of the renal arterial tree by fractal analysis. J Pathol 1993; 170: 479-484 [PMID: 8410497 DOI: 10.1002/path.1711700412]
73. Nonnenmacher TF, Baumann G, Losa GA. Self-organization and fractal scaling patterns in biological systems. In: Menon J, editor. Trends in Biological Cybernetics. Trivandrum India, Publication Manager, Research Trends, Council of Scientific Research Integration, 1990
74. Mandelbrot BB. A Fractal's Lacunarity, and how it can be Tuned and Measured. In: Nonnenmacher TF, Losa GA, Weibel ER, editors. Fractals in Biology and Medicine. Basel: Birkhauser Press, 1993: 8-21
75. Allain C, Cloitre M. Characterizing the lacunarity of random and deterministic fractal sets. Phys Rev A 1991; 44: 3552-3558 [PMID: 9906372]
76. Prouteau S, Ducher G, Nanyan P, Lemineur G, Benhamou L, Courteix D. Fractal analysis of bone texture: a screening tool for stress fracture risk? Eur J Clin Invest 2004; 34: 137-142 [PMID: 14764077]
77. Plotnick RE, Gardner RH, Hargrove WW, Prestegaard K, Perlmutter M. Lacunarity analysis: A general technique for the analysis of spatial patterns. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 1996; 53: 5461-5468 [PMID: 9964879]
78. Gould DJ, Vadakkan TJ, Poché RA, Dickinson ME. Multifractal and lacunarity analysis of microvascular morphology and remodeling. Microcirculation 2011; 18: 136-151 [PMID: 21166933]
79. Chappard D, Legrand E, Haettich B, Chalès G, Auvinet B, Eschard JP, Hamelin JP, Baslé MF, Audran M. Fractal dimension of trabecular bone: comparison of three histomorphometric computed techniques for measuring the architectural two-dimensional complexity. J Pathol 2001; 195: 515-521 [PMID: 11745685]
80. Dougherty G, Henebry GM. Lacunarity analysis of spatial pattern in CT images of vertebral trabecular bone for assessing osteoporosis. Med Eng Phys 2002; 24: 129-138 [PMID: 11886832]
81. Chappard C, Brunet-Imbault B, Lemineur G, Giraudeau B, Basillais A, Harba R, Benhamou CL. Anisotropy changes in postmenopausal osteoporosis: characterization by a new index applied to trabecular bone radiographic images. Osteoporos Int 2005; 16: 1193-1202 [PMID: 15685395]
82. Herlidou S, Grebe R, Grados F, Leuyer N, Fardellone P, Meyer ME. Influence of age and osteoporosis on calcaneus trabecular bone structure: a preliminary in vivo MRI study by quantitative texture analysis. Magn Reson Imaging 2004; 22: 237-243 [PMID: 15010116 DOI: 10.1016/j.mri.2003.07.007]
83. Raisz LG. Clinical practice. Screening for osteoporosis. N Engl J Med 2005; 353: 164-171 [PMID: 16014886]
84. Olson AF. Osteoporosis detection: is BMD testing the future? Nurse Pract 2007; 32: 20-27; quiz 28 [PMID: 17557021]
85. Hernlund E, Svedbom A, Ivergård M, Compston J, Cooper C, Stenmark J, McCloskey EV, Jönsson B, Kanis JA. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 2013; 8: 136 [PMID: 24113837]
86. Bonnick SL. Osteoporosis in men and women. Clin Cornerstone 2006; 8: 28-39 [PMID: 17591574]
87. Fleurence RL, Iglesias CP, Johnson JM. The cost effectiveness of bisphosphonates for the prevention and treatment of osteoporosis: a structured review of the literature. Pharmacoeconomics 2007; 25: 913-933 [PMID: 17960951 DOI: 10.2165/00019053-200725110-00003]
88. Schacht E, Dukas L, Richy F. Combined therapies in osteoporosis: bisphosphonates and vitamin D-hormone analogs. J Musculoskelet Neuronal Interact 2007; 7: 174-184 [PMID: 17627088]
89. Silverman SL, Cummings SR, Watts NB. Recommendations for the clinical evaluation of agents for treatment of osteoporosis: consensus of an expert panel representing the American Society for Bone and Mineral Research (ASBMR), the International Society for Clinical Densitometry (ISCD), and the National Osteoporosis Foundation (NOF). J Bone Miner Res 2008; 23: 159-165 [PMID: 17892379]
90. Lentle B, Cheung AM, Hanley DA, Leslie WD, Lyons D, Papaioannou A, Atkinson S, Brown JP, Feldman S, Hodsman AB, Jamal AS, Josse RG, Kaiser SM, Kvern B, Morin S, Siminoski K. Osteoporosis Canada 2010 guidelines for the assessment of fracture risk. Can Assoc Radiol J 2011; 62: 243-250 [PMID: 21852066]
91. Pothuaud L, Carceller P, Hans D. Correlations between greylevel variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone 2008; 42: 775-787 [PMID: 18234577]
92. Pothuaud L, Barthe N, Krieg MA, Mehsen N, Carceller P, Hans D. Evaluation of the potential use of trabecular bone score to complement bone mineral density in the diagnosis of osteoporosis: a preliminary spine BMD-matched, case-control study. J Clin Densitom 2009; 12: 170-176 [PMID: 19181553]
93. Rabier B, Héraud A, Grand-Lenoir C, Winzenrieth R, Hans D. A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. Bone 2010; 46: 176-181 [PMID: 19747992]
94. Winzenrieth R, Dufour R, Pothuaud L, Hans D. A retrospective case-control study assessing the role of trabecular bone score in postmenopausal Caucasian women with osteopenia: analyzing the odds of vertebral fracture. Calcif Tissue Int 2010; 86: 104-109 [PMID: 19998029]
95. Cohen A, Stein EM, Recker RR, Lappe JM, Dempster DW, Zhou H, Cremers S, McMahon DJ, Nickolas TL, Müller R, Zwahlen A, Young P, Stubby J, Shane E. Teriparatide for idiopathic osteoporosis in premenopausal women: a pilot study. J Clin Endocrinol Metab 2013; 98: 1971-1981 [PMID: 23543660]
96. Burghardt AJ, Link TM, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res 2011; 469: 2179-2193 [PMID: 21344275]
97. Guglielmi G, Muscarella S, Bazzocchi A. Integrated imaging approach to osteoporosis: state-of-the-art review and update. Radiographics 2011; 31: 1343-1364 [PMID: 21918048]
98. Baum T, Dütsch Y, Müller D, Monetti R, Sidorenko I, Räth C, Rummeny EJ, Link TM, Bauer JS. Reproducibility of trabecular bone structure measurements of the distal radius at 1.5 and 3.0 T magnetic resonance imaging. J Comput Assist Tomogr 2012; 36: 623-626 [PMID: 22992616 DOI: 10.1097/RCT.0b013e31825f9aa3]