Bone Marrow Changes in Osteoporosis

Chapter
Part of the Medical Radiology book series (MEDRAD)

Abstract

Bone research in osteoporosis has quite rightly focused on the mineralised component of bone as this is the component that is ultimately responsible for bone strength. However, the non-mineralised component of bone, i.e. the bone marrow, is many times more metabolically active and responsive than the mineralised component of bone. Despite this, the bone marrow has been relatively overlooked with regard to the pathogenesis of osteoporosis and related conditions. This has changed with magnetic resonance imaging and positron emission tomography allowing non-invasive quantification of bone marrow physiology and pathology on a large scale. Aspects of the bone marrow that can be evaluated on imaging are marrow fat content, perfusion, molecular diffusion and metabolic activity. There are many ways in which bone marrow metabolism may potentially influence bone metabolism. For example, the bone marrow forms the microenvironment of biologically relevant endosteal and trabecular bone and this bone may be responding to changes in the bone marrow. Similarly, the bone marrow contains pluripotent mesenchymal stem cells with the ability to differentiate preferentially along either haematopoetic, adipocytic or osteoblastic cell lines. Preliminary research has shown how bone loss in senile osteoporosis mass is accompanied by scalar changes in marrow fat content, marrow perfusion and marrow diffusion. Similar to the bone loss of osteoporosis, the bone marrow changes in osteoporosis represent an exaggeration of physiological age-related change. Bone marrow changes occur in synchrony rather than pre- or post-date changes in the mineralised component of bone. Whether the bone marrow is an active contributor or a passive bystander to physiological and osteoporotic bone loss remains to be seen.

Keywords

Bone Mineral Density Apparent Diffusion Coefficient Fatty Marrow Bone Marrow Change Bone Blood Flow 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

References

  1. Arnett TR (2010) Acidosis, hypoxia and bone. Arch Biochem Biophys 1(503):103–119Google Scholar
  2. Balliu E, Vilanova JC, Peláez I, Puig J, Remollo S, Barceló C, Barceló J, Pedraza S (2009) Diagnostic value of apparent diffusion coefficients to differentiate benign from malignant vertebral bone marrow lesions. Eur J Radiol 69:560–566PubMedGoogle Scholar
  3. Basu S, Houseni M, Bural G, Chamroonat W, Udupa J, Mishra S, Alavi A (2007) Magnetic resonance imaging based bone marrow segmentation for quantitative calculation of pure red marrow metabolism using 2-deoxy-2-[F-18] fluoro-d-glucose-positron emission tomography: a novel application with significant implications for combined structure-function approach. Mol Imaging Biol 9:361–365PubMedGoogle Scholar
  4. Baur A, Stabler A, Bartl R, Lamerz R, Scheidler J, Reiser M (1997) MRI gadolinium enhancement of bone marrow: age-related changes in normals and in diffuse neoplastic infiltration. Skeletal Radiol 26:414–418PubMedGoogle Scholar
  5. Bernard C, Liney G, Manton D, Turnbull L, Langton C (2008) Comparison of fat quantification methods: a phantom study at 3.0 T. J Magn Reson Imaging 27:192–197PubMedGoogle Scholar
  6. Biffar A, Baur-Melnyk A, Schmidt GP, Reiser MF, Dietrich O (2010) Multiparameter MRI assessment of normal-appearing and diseased vertebral bone marrow. Eur Radiol 20:2679–2689PubMedGoogle Scholar
  7. Blake GM, Griffith JF, Yeung DK, Leung PC, Fogelman I (2009) Effect of increasing vertebral marrow fat content on BMD measurement, T-score status and fracture risk prediction by DXA. Bone 44:495–501PubMedGoogle Scholar
  8. Bloomfield SA, Hogan HA, Delp MD (2002) Decreases in bone blood flow and bone material properties in aging Fischer-344 rats. Clin Orthop 396:248–257PubMedGoogle Scholar
  9. Blouin K, Boivin A, Tchernof A (2008) Androgens and body fat distribution. J Steroid Biochem Mol Biol 108:272–280PubMedGoogle Scholar
  10. Bolotin HH (1998) Analytic and quantitative exposition of patient-specific systematic inaccuracies inherent in planar DXA-derived in vivo BMD measurements. Med Phys 25:139–151PubMedGoogle Scholar
  11. Bolotin HH (2007) DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility and bone remodelling. Bone 41:138–154PubMedGoogle Scholar
  12. Bolotin HH, Sievansen H, Grashuis JL, Kuiper JW, Jarvinen TL (2001) Inaccuracies inherent in patient-specific dual-energy x-ray absorptiometry bone mineral density measurements: comprehensive phantom-based evaluation. J Bone Miner Res 16:417–426PubMedGoogle Scholar
  13. Bredella MA (2010) Perspective: the bone-fat connection. Skeletal Radiol 39:729–731PubMedGoogle Scholar
  14. Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Rosen CJ, Klibanski A, Miller KK (2011) Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity (Silver Spring) 19:49–53Google Scholar
  15. Bridgeman G, Brookes M (1996) Blood supply to the human femoral diaphysis in youth and senescence. J Anat 188:611–621PubMedGoogle Scholar
  16. Brookes M (1974) Approaches to non-invasive blood flow measurement in bone. Biomed Eng 9:342–347PubMedGoogle Scholar
  17. Chan JH, Peh WC, Tsui EY, Chau LF, Cheung KK, Chan KB, Yuen MK, Wong ET, Wong KP (2002) Acute vertebral body compression fractures: discrimination between benign and malignant causes using apparent diffusion coefficients. Br J Radiol 75:207–214PubMedGoogle Scholar
  18. Chen WT, Shih TT (2006) Correlation between the bone marrow blood perfusion and lipid water content on the lumbar spine in female subjects. J Magn Reson Imaging 24:176–181PubMedGoogle Scholar
  19. Chen WT, Shih TT, Chen RC, Lo SY, Chou CT, Lee JM, Tu HY (2001) Vertebral bone marrow perfusion evaluated with dynamic contrast-enhanced MR imaging: significance of aging and sex. Radiology 220:213–238PubMedGoogle Scholar
  20. Chen WT, Ting-Fang Shih T, Hu CJ, Chen RC, Tu HY (2004) Relationship between vertebral bone marrow blood perfusion and common carotid intima-media thickness in aging adults. J Magn Reson Imaging 20:811–816PubMedGoogle Scholar
  21. Coetzee M, Haag M, Kruger MC (2007) Effects of arachidonic acid, docosahexaenoic acid, prostaglandin E(2) and parathyroid hormone on osteoprotegerin and RANKL secretion by MC3T3-E1 osteoblast-like cells. J Nutr Biochem 18:54–63PubMedGoogle Scholar
  22. Collins TC, Ewing SK, Diem SJ, Taylor BC, Orwoll ES, Cummings SR, Strotmeyer ES, Osteoporotic Fractures in Men (MrOS) Study Group (2009) Peripheral arterial disease is associated with higher rates of hip bone loss and increased fracture risk in older men. Circulation 119:2305–2312PubMedGoogle Scholar
  23. Cowin SC (2002) Mechanosensation and fluid transport in living bone. J Musculoskelet Neuronal Interact 2:256–260PubMedGoogle Scholar
  24. Crepaldi G, Romanato G, Tonin P, Maggi S (2007) Osteoporosis and body composition. J Endocrinol Invest 30:42–47PubMedGoogle Scholar
  25. D’Ippolito G, Diabira S, Howard GA, Roos BA, Schiller PC (2006) Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39:513–522PubMedGoogle Scholar
  26. De Bisschop E, Luypaert R, Louis O, Osteaux M (1993) Fat fraction of lumbar bone marrow using in vivo proton nuclear magnetic resonance spectroscopy. Bone 14:133–136PubMedGoogle Scholar
  27. Demer LL, Tintut Y (2009) Mechanisms linking osteoporosis with cardiovascular calcification. Curr Osteoporos Rep 7:42–46PubMedGoogle Scholar
  28. Dennison E, Eastell R, Fall CH, Kellingray S, Wood PJ, Cooper C (1999) Determinants of bone loss in elderly men and women: a prospective population-based study. Osteoporos Int 10:384–391PubMedGoogle Scholar
  29. Duda SH, Laniado M, Schick F, Strayle M, Claussen CD (1995) Normal bone marrow in the sacrum of young adults: differences between the sexes seen on chemical-shift MR imaging. AJR Am J Roentgenol 164:935–940PubMedGoogle Scholar
  30. Dunnill MS, Anderson JA, Whitehead R (1967) Quantitative histological studies on age changes in bone. J Pathol Bacteriol 94:275–291PubMedGoogle Scholar
  31. Duque G (2008) Bone and fat connection in aging bone. Curr Opin Rheumatol 20:429–434PubMedGoogle Scholar
  32. Erly WK, Oh ES, Outwater EK (2006) The utility of in-phase/opposed-phase imaging in differentiating malignancy from acute benign compression fractures of the spine. AJNR Am J Neuroradiol 27:1183–1188PubMedGoogle Scholar
  33. Fatokun AA, Stone TW, Smith RA (2006) Hydrogen peroxide-induced oxidative stress in MC3T3-E1 cells: the effects of glutamate and protection by purines. Bone 39:542–551PubMedGoogle Scholar
  34. Gameiro CM, Romão F, Castelo-Branco C (2010) Menopause and aging: changes in the immune system—a review. Maturitas 67:316–320PubMedGoogle Scholar
  35. Gao J, Zeng S, Sun BL, Fan HM, Han LH (1987) Menstrual blood loss and hematologic indices in healthy Chinese women. J Reprod Med 32:822–826PubMedGoogle Scholar
  36. Gerdes CM, Kijowski R, Reeder SB (2007) IDEAL imaging of the musculoskeletal system: robust water fat separation for uniform fat suppression, marrow evaluation, and cartilage imaging. AJR Am J Roentgenol 189:W284–W291PubMedGoogle Scholar
  37. Gimble JM, Nuttall ME (2004) Bone and fat: old questions, new insights. Endocrine 23:183–188PubMedGoogle Scholar
  38. Griffith JF, Genant HK (2011) New imaging modalities in bone. Curr Rheumatol Rep 13:241–250PubMedGoogle Scholar
  39. Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, Lau EM, Leung PC (2005) Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 236:945–951PubMedGoogle Scholar
  40. Griffith JF, Yeung DK, Antonio GE, Wong SY, Kwok TC, Woo J, Leung PC (2006) Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation. Radiology 241:831–838PubMedGoogle Scholar
  41. Griffith JF, Yeung DK, Tsang PH, Choi KC, Kwok TC, Ahuja AT, Leung KS, Leung PC (2008) Compromised bone marrow perfusion in osteoporosis. J Bone Miner Res 23:1068–1075PubMedGoogle Scholar
  42. Griffith JF, Yeung DK, Chow SK, Leung JC, Leung PC (2009) Reproducibility of MR perfusion and (1)H spectroscopy of bone marrow. J Magn Reson Imaging 29:1438–1442PubMedGoogle Scholar
  43. Griffith JF, Engelke K, Genant HK (2010) Looking beyond bone mineral density: Imaging assessment of bone quality. Ann N Y Acad Sci 1192:45–56PubMedGoogle Scholar
  44. Griffith JF, Yeung DKW, Ma HT, Leung JSC, Kwok TCY, Leung PC (2012) Bone marrow fat content in the elderly: a reversal of trend seen in younger subjects J Magn Reson Imaging (In press)Google Scholar
  45. Hamerman D (2005) Osteoporosis and atherosclerosis: biological linkages and the emergence of dual-purpose therapies. QJM 98:467–484PubMedGoogle Scholar
  46. Hannan MT, Felson DT, Dawson-Hughes B, Tucker KL, Cupples LA, Wilson PW, Kiel DP (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham Osteoporosis Study. J Bone Miner Res 15:710–720PubMedGoogle Scholar
  47. Hartsock RJ, Smith EB, Petty CS (1965) Normal variations with aging of the amount of hematopoetic tissue in bone marrow from the anterior iliac crest. A study made from 177 cases of sudden death examined by necropsy. Am J Clin Pathol 43:326–331PubMedGoogle Scholar
  48. Hatipoglu HG, Selvi A, Ciliz D, Yuksel E (2007) Quantitative and diffusion MR imaging as a new method to assess osteoporosis. Am J Neuroradiol 28:1934–1937PubMedGoogle Scholar
  49. Herneth AM, Philipp MO, Naude J, Funovics M, Beichel RR, Bammer R, Imhof H (2002) Vertebral metastases: assessment with apparent diffusion coefficient. Radiology 225:889–894PubMedGoogle Scholar
  50. Hillengass J, Stieltjes B, Bäuerle T, McClanahan F, Heiss C, Hielscher T, Wagner-Gund B, Habetler V, Goldschmidt H, Schlemmer HP, Delorme S, Zechmann CM (2011) Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) and diffusion-weighted imaging of bone marrow in healthy individuals. Acta Radiol 1(52):324–330Google Scholar
  51. Hwang S, Panicek DM (2007) Magnetic resonance imaging of bone marrow in oncology, Part 1. Skeletal Radiol 36:913–920PubMedGoogle Scholar
  52. Ishijima H, Ishizaka H, Horikoshi H, Sakurai M (1996) Water fraction of lumbar vertebral bone marrow estimated from chemical shift misregistration on MR imaging: normal variations with age and sex. AJR Am J Roentgenol 167:355–358PubMedGoogle Scholar
  53. Jung CM, Kugel H, Schulte O, Heindel W (2000) Proton-MR spectroscopy of the spinal bone marrow. An analysis of physiological signal behavior. Radiologe 40:694–699PubMedGoogle Scholar
  54. Kahn D, Weiner GJ, Ben-Haim S, Ponto LL, Madsen MT, Bushnell DL, Watkins GL, Argenyi EA, Hichwa RD (1994) Positron emission tomographic measurement of bone marrow blood flow to the pelvis and lumbar vertebrae in young normal adults. Blood 15(83):958–963Google Scholar
  55. Kha HT, Basseri B, Shouhed D, Richardson J, Tetradis S, Hahn TJ, Parhami F (2004) Oxysterols regulate differentiation of mesenchymal stem cells: pro-bone and anti-fat. J Bone Miner Res 19:830–840PubMedGoogle Scholar
  56. Khan F, Green FC, Forsyth JS, Greene SA, Morris AD, Belch JJ (2003) Impaired microvascular function in normal children: effects of adiposity and poor glucose handling. J Physiol 551:705–711PubMedGoogle Scholar
  57. Khoo MM, Tyler PA, Saifuddin A, Padhani AR (2011) Diffusion-weighted imaging (DWI) in musculoskeletal MRI: a critical review. Skeletal Radiol 40:665–681PubMedGoogle Scholar
  58. Kugel H, Jung C, Schulte O, Heindel W (2001) Age- and sex-specific differences in the 1H-spectrum of vertebral bone marrow. J Magn Reson Imaging 13:263–268PubMedGoogle Scholar
  59. Laroche M, Ludot I, Thiechart M, Arlet J, Pieraggi M, Chiron P, Moulinier L, Cantagrel A, Puget J, Utheza G et al (1995) Study of the intraosseous vessels of the femoral head in patients with fractures of the femoral neck or osteoarthritis of the hip. Osteoporos Int 5:213–217PubMedGoogle Scholar
  60. Lau EM, Leung PC, Kwok T, Woo J, Lynn H, Orwoll E, Cummings S, Cauley J (2006) The determinants of bone mineral density in Chinese men—results from Mr. Os (Hong Kong), the first cohort study on osteoporosis in Asian men. Osteoporos Int 17:297–303PubMedGoogle Scholar
  61. Lecka-Czernik B, Moerman EJ, Grant DF, Lehmann JM, Manolagas SC, Jilka RL (2002) Divergent effects of selective peroxisome proliferator-activated receptor-gamma 2 ligands on adipocyte versus osteoblast differentiation. Endocrinology 143:2376–2384PubMedGoogle Scholar
  62. Lehnert A, Machann J, Helms G, Claussen CD, Schick F (2004) Diffusion characteristics of large molecules assessed by proton MRS on a whole-body MR system. Magn Reson Imaging 22:39–46PubMedGoogle Scholar
  63. Letechipia JE, Alessi A, Rodriguez G, Asbun J (2010) Would increased interstitial fluid flow through in situ mechanical stimulation enhance bone remodeling? Med Hypotheses 75:196–198PubMedGoogle Scholar
  64. Lichtman MA (1981) The ultrastructure of the hemopoietic environment of the marrow: a review. Exp Hematol 9:391–410PubMedGoogle Scholar
  65. Liney GP, Bernard CP, Manton DJ, Turnbull LW, Langton CM (2007) Age, gender, and skeletal variation in bone marrow composition: a preliminary study at 3.0 Tesla. J Magn Reson Imaging 26:787–793PubMedGoogle Scholar
  66. Link TM (2012) Osteoporosis imaging: state of the art and advanced imaging. Radiology 263:3–17PubMedGoogle Scholar
  67. Liu Y, Tang GY, Tang RB, Peng YF, Li W (2010) Assessment of bone marrow changes in postmenopausal women with varying bone densities: magnetic resonance spectroscopy and diffusion magnetic resonance imaging. Chin Med J (Engl) 123:1524–1527Google Scholar
  68. Maeda M, Sakuma H, Maier SE, Takeda K (2003) Quantitative assessment of diffusion abnormalities in benign and malignant vertebral compression fractures by line scan diffusion-weighted imaging. AJR Am J Roentgenol 181:1203–1209PubMedGoogle Scholar
  69. Manolagas SC, Almeida M (2007) Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 21:2605–2614PubMedGoogle Scholar
  70. Marcovitz PA, Tran HH, Franklin BA, O’Neill WW, Yerkey M, Boura J, Kleerekoper M, Dickinson CZ (2005) Usefulness of bone mineral density to predict significant coronary artery disease. Am J Cardiol 96:1059–1063PubMedGoogle Scholar
  71. McCarthy ID (2005) Fluid shifts due to microgravity and their effects on bone: a review of current knowledge. Ann Biomed Eng 33:95–103PubMedGoogle Scholar
  72. McCarthy EF (2011) Perspective: skeletal complications of space flight. Skeletal Radiol 40:661–663PubMedGoogle Scholar
  73. Mills R (1973) Self-diffusion in normal and heavy water in the range 1–45 deg. J Phy Chem 77:685–688Google Scholar
  74. Montazel JL, Divine M, Lepage E, Kobeiter H, Breil S, Rahmouni A (2003) Normal spinal bone marrow in adults: dynamic gadolinium-enhanced MR imaging. Radiology 229:703–709PubMedGoogle Scholar
  75. Müller R, Van Campenhout H, Van Damme B, Van Der Perre G, Dequeker J, Hildebrand T, Rüegsegger P (1998) Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone 23:59–66PubMedGoogle Scholar
  76. Nonomura Y, Yasumoto M, Yoshimura R, Haraguchi K, Ito S, Akashi T, Ohashi I (2001) Relationship between bone marrow cellularity and apparent diffusion coefficient. J Magn Reson Imaging 13:757–760PubMedGoogle Scholar
  77. Nordström A, Eriksson M, Stegmayr B, Gustafson Y, Nordström P (2010) Low bone mineral density is an independent risk factor for stroke and death. Cerebrovasc Dis. 29:130–136PubMedGoogle Scholar
  78. Parfitt AM (2002) Misconceptions (2): turnover is always higher in cancellous than in cortical bone. Bone 30:807–809PubMedGoogle Scholar
  79. Pfitzner J (1976) Poiseuille and his law. Anaesthesia 31:273–275PubMedGoogle Scholar
  80. Piert M, Machulla HJ, Jahn M, Stahlschmidt A, Becker GA, Zittel TT (2002) Coupling of porcine bone blood flow and metabolism in high-turnover bone disease measured by [(15)O]H(2)O and [(18)F]fluoride ion positron emission tomography. Eur J Nucl Med Mol Imaging 29:907–914PubMedGoogle Scholar
  81. Poulsen RC, Wolber FM, Moughan PJ, Kruger MC (2008) Long chain polyunsaturated fatty acids alter membrane-bound RANK-L expression and osteoprotegerin secretion by MC3T3-E1 osteoblast-like cells. Prostaglandins Other Lipid Mediat 85:42–48PubMedGoogle Scholar
  82. Poulton TB, Murphy WD, Duerk JL, Chapek CC, Feiglin DH (1993) Bone marrow reconversion in adults who are smokers: MR Imaging findings. Am J Roentgenol 161:1217–1221Google Scholar
  83. Prisby RD, Ramsey MW, Behnke BJ, Dominguez JM 2nd, Donato AJ, Allen MR, Delp MD (2007) Aging reduces skeletal blood flow, endothelium-dependent vasodilation, and NO bioavailability in rats. J Bone Miner Res 22:1280–1288PubMedGoogle Scholar
  84. Ratcliffe JF (1986) Arterial changes in the human vertebral body associated with aging. The ratios of peripheral to central arteries and arterial coiling. Spine 11:235–240PubMedGoogle Scholar
  85. Rosen CJ, Klibanski A (2009) Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 122:409–414PubMedGoogle Scholar
  86. Samuels A, Perry MJ, Gibson RL, Colley S, Tobias JH (2001) Role of endothelial nitric oxide synthase in estrogen-induced osteogenesis. Bone 29:24–29PubMedGoogle Scholar
  87. Sanada M, Taguchi A, Higashi Y, Tsuda M, Kodama I, Yoshizumi M, Ohama K (2004) Forearm endothelial function and bone mineral loss in postmenopausal women. Atherosclerosis 176:387–392PubMedGoogle Scholar
  88. Savvopoulou V, Maris TG, Vlahos L, Moulopoulos LA (2008) Differences in perfusion parameters between upper and lower lumbar vertebral segments with dynamic contrast-enhanced MRI (DCE MRI). Eur Radiol 18:1876–1883PubMedGoogle Scholar
  89. Schellinger D, Lin SC, Fertikh D et al (2000) Normal lumbar vertebrae: anatomic, age, and sex variance in subjects at proton MR spectroscopy-initial experience. Radiology 215:910–916PubMedGoogle Scholar
  90. Shen W, Chen J, Punyanitya M, Shapses S, Heshka S, Heymsfield SB (2007) MRI-measured bone marrow adipose tissue is inversely related to DXA-measured bone mineral in Caucasian women. Osteoporos Int 18:641–647PubMedGoogle Scholar
  91. Shih TT, Chang CJ, Hsu CY, Wei SY, Su KC, Chung HW (2004) Correlation of bone marrow lipid water content with bone mineral density on the lumbar spine. Spine (Phila Pa 1976) 15(29):2844–2850Google Scholar
  92. Shouhed D, Kha HT, Richardson JA, Amantea CM, Hahn TJ, Parhami F (2005) Osteogenic oxysterols inhibit the adverse effects of oxidative stress on osteogenic differentiation of marrow stromal cells. J Cell Biochem 95:1276–1283PubMedGoogle Scholar
  93. Sorenson JA (1990) Effects of nonmineral tissues on measurement of bone mineral content by dual-photon absorptiometry. Med Phys 17:905–912PubMedGoogle Scholar
  94. Steiner RM, Mitchell DG, Rao VM, Schweitzer ME (1993) Magnetic resonance imaging of diffuse bone marrow disease. Radiol Clin North Am 31:383–409PubMedGoogle Scholar
  95. Sumino H, Ichikawa S, Kasama S, Takahashi T, Sakamoto H, Kumakura H, Takayama Y, Kanda T, Murakami M, Kurabayashi M (2007) Relationship between brachial arterial endothelial function and lumbar spine bone mineral density in postmenopausal women. Circ J 71:1555–1559PubMedGoogle Scholar
  96. Tang G, Liu Y, Li W, Yao J, Li B, Li P (2007) Optimization of b value in diffusion-weighted MRI for the differential diagnosis of benign and malignant vertebral fractures. Skeletal Radiol 36:1035–1041PubMedGoogle Scholar
  97. Tang GY, Lv ZW, Tang RB, Liu Y, Peng YF, Li W, Cheng YS (2010) Evaluation of MR spectroscopy and diffusion-weighted MRI in detecting bone marrow changes in postmenopausal women with osteoporosis. Clin Radiol 65:377–381PubMedGoogle Scholar
  98. Thawait SK, Marcus MA, Morrison WB, Klufas RA, Eng J, Carrino J (2011) Research synthesis: what is the diagnostic performance of MRI to discriminate benign from malignant vertebral compression fractures? Systematic review and meta-analysis. Spine (Phila Pa 1976) [Epub ahead of print]Google Scholar
  99. Toth MJ, Tchernof A, Sites CK, Poehlman ET (2000) Menopause-related changes in body fat distribution. Ann N Y Acad Sci 904:502–506PubMedGoogle Scholar
  100. Travlos GS (2006) Normal structure, function, and histology of the bone marrow. Toxicol Pathol 34:548–565PubMedGoogle Scholar
  101. Van Dyke D, Parker H, Anger HO, McRae J, Dobson EL, Yano Y, Naets JP, Linfoot J (1971) Markedly increased bone blood flow in myelofibrosis. J Nucl Med 12:506–512PubMedGoogle Scholar
  102. Wang YX, Griffith JF (2010) Effect of menopause on lumbar disk degeneration: potential etiology. Radiology 257:318–320PubMedGoogle Scholar
  103. Wang YX, Griffith JF, Kwok AW, Leung JC, Yeung DK, Ahuja AT, Leung PC (2009) Reduced bone perfusion in proximal femur of subjects with decreased bone mineral density preferentially affects the femoral neck. Bone 45:711–715PubMedGoogle Scholar
  104. Ward R, Caruthers S, Yablon C, Blake M, DiMasi M, Eustace S (2000) Analysis of diffusion changes in posttraumatic bone marrow using navigator-corrected diffusion gradients. Am J Roentgenol 174:731–734Google Scholar
  105. Wehrli FW, Hopkins JA, Hwang SN, Song HK, Snyder PJ, Haddad JG (2000) Cross-sectional study of osteopenia with quantitative MR imaging and bone densitometry. Radiology 217:527–538PubMedGoogle Scholar
  106. Wimalawansa SJ (2010) Nitric oxide and bone. Ann N Y Acad Sci 1192:391–403PubMedGoogle Scholar
  107. Yeung DK, Wong SY, Griffith JF, Lau EM (2004) Bone marrow diffusion in osteoporosis: evaluation with quantitative MR diffusion imaging. J Magn Reson Imaging 19:222PubMedGoogle Scholar
  108. Yeung DK, Griffith JF, Antonio GE, Lee FK, Woo J, Leung PC (2005) Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J Magn Reson Imaging 22:279–285PubMedGoogle Scholar
  109. Yeung DK, Lam SL, Griffith JF, Chan AB, Chen Z, Tsang PH, Leung PC (2008) Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy. Chem Phys Lipids 151:103–109PubMedGoogle Scholar
  110. Zampa V, Cosottini M, Michelassi C, Ortori S, Bruschini L, Bartolozzi C (2002) Value of opposed-phase gradient-echo technique in distinguishing between benign and malignant vertebral lesions. Eur Radiol 12:1811–1818PubMedGoogle Scholar
  111. Zhou XJ, Leeds NE, McKinnon GC, Kumar AJ (2002) Characterization of benign and metastatic vertebral compression fractures with quantitative diffusion MR imaging. Am J Neuroradiol 23:165–170PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Imaging and Interventional RadiologyThe Chinese University of Hong KongShatin, Hong KongPeople’s Republic of China

Personalised recommendations