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Bone Marrow Adipose Tissue Quantification by Imaging

  • Ebrahim Bani Hassan
  • Ali Ghasem-Zadeh
  • Mahdi Imani
  • Numan Kutaiba
  • David K. Wright
  • Tara Sepehrizadeh
  • Gustavo DuqueEmail author
Bone Marrow and Adipose Tissue (G Duque and B Lecka-Czernik, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Bone Marrow and Adipose Tissue

Abstract

Purpose of Review

The significance and roles of marrow adipose tissue (MAT) are increasingly known, and it is no more considered a passive fat storage but a tissue with significant paracrine and endocrine activities that can cause lipotoxicity and inflammation.

Recent Findings

Changes in the MAT volume and fatty acid composition appear to drive bone and hematopoietic marrow deterioration, and studying it may open new horizons to predict bone fragility and anemia development. MAT has the potential to negatively impact bone volume and strength through several mechanisms that are partially described by inflammaging and lipotoxicity terminology.

Summary

Evidence indicates paramount importance of MAT in age-associated decline of bone and red marrow structure and function. Currently, MAT measurement is being tested and validated by several techniques. However, purpose-specific adaptation of existing imaging technologies and, more importantly, development of new modalities to quantitatively measure MAT are yet to be done.

Keywords

Yellow marrow Osteosarcopenia Red marrow Hematopoietic marrow Lipotoxicity CT MRI 

Notes

Compliance with Ethical Standards

Conflict of Interest

Ebrahim Bani Hassan, Ali Ghasem-Zadeh, Mahdi Imani, Numan Kutaiba, David K Wright, Tara Sepehrizadeh, and Gustavo Duque declare no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    •• Bani Hassan E, Demontiero O, Vogrin S, Ng A, Duque G. Marrow adipose tissue in older men: association with visceral and subcutaneous fat, bone volume, metabolism, and inflammation. Calcif Tissue Int. 2018;103(2):164–74.  https://doi.org/10.1007/s00223-018-0412-6This paper provides important evidences that MAT expansion in older men coincides with bone and hematopoietic marrow atrophy. Also, this reference provides evidences that most of the inflammatory cytokines produces by MAT are not released into systemic circulation, and may gain high local concentrations and severely impact bone and marrow health. Further, this paper is one of the limited number of publications that uses single energy CT scan for assesing bone, MAT and red marrow volumes. CrossRefPubMedGoogle Scholar
  2. 2.
    Martin RB, Chow BD, Lucas PA. Bone marrow fat content in relation to bone remodeling and serum chemistry in intact and ovariectomized dogs. Calcif Tissue Int. 1990;46(3):189–94.  https://doi.org/10.1007/BF02555043.CrossRefPubMedGoogle Scholar
  3. 3.
    Schwartz RS, Shuman WP, Bradbury VL, Cain KC, Fellingham GW, Beard JC, et al. Body fat distribution in healthy young and older men. J Gerontol. 1990;45(6):M181–5.CrossRefGoogle Scholar
  4. 4.
    • Elbaz A, Wu X, Rivas D, Gimble JM, Duque G. Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro. J Cell Mol Med. 2010;14(4):982–91.  https://doi.org/10.1111/j.1582-4934.2009.00751.xThis paper provides first evidences that toxic effects of MAT-derived fatty acids on osteoblastss can be prevented by inhibiting the biosynthesis of such fatty acids, establishing a possible causality association. CrossRefPubMedGoogle Scholar
  5. 5.
    • Gunaratnam K, Vidal C, Gimble JM, Duque G. Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology. 2014;155(1):108–16.  https://doi.org/10.1210/en.2013-1712This paper provides evidences for the lipotoxicity mechanisms of action on bone. CrossRefPubMedGoogle Scholar
  6. 6.
    Gasparrini M, Rivas D, Elbaz A, Duque G. Differential expression of cytokines in subcutaneous and marrow fat of aging C57BL/6J mice. Exp Gerontol. 2009;44(9):613–8.  https://doi.org/10.1016/j.exger.2009.05.009.CrossRefPubMedGoogle Scholar
  7. 7.
    Kirkland JL, Tchkonia T, Pirtskhalava T, Han J, Karagiannides I. Adipogenesis and aging: does aging make fat go MAD? Exp Gerontol. 2002;37(6):757–67.CrossRefGoogle Scholar
  8. 8.
    Sharma RB, Alonso LC. Lipotoxicity in the pancreatic beta cell: not just survival and function, but proliferation as well? Curr Diab Rep. 2014;14(6):492.  https://doi.org/10.1007/s11892-014-0492-2.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007;56(4):1010–3.  https://doi.org/10.2337/db06-1656.CrossRefPubMedGoogle Scholar
  10. 10.
    Jung UJ, Choi M-S. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci. 2014;15(4):6184–223.  https://doi.org/10.3390/ijms15046184.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Kalupahana NS, Claycombe KJ, Moustaid-Moussa N. (n-3) Fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights. Adv Nutr. 2011;2(4):304–16.  https://doi.org/10.3945/an.111.000505.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Mohamed-Ali V, Goodrick S, Rawesh A, Katz DR, Miles JM, Yudkin JS, et al. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. J Clin Endocrinol Metab. 1997;82(12):4196–200.  https://doi.org/10.1210/jcem.82.12.4450.CrossRefPubMedGoogle Scholar
  13. 13.
    •• Bani Hassan E, Alderghaffar M, Wauquier F, Coxam V, Demontiero O, Vogrin S, et al. The effects of dietary fatty acids on bone, hematopoietic marrow and marrow adipose tissue in a murine model of senile osteoporosis. Aging (Albany NY). 2019;11(18):7938-7947. doi: 10.18632/aging.102299.  This recent publication provides important evidences that the negative asciation netween MAT vs bone and hematopoietic marrow seen in men (Ref 1), also occurs in a progeria mouse model. Importantly, it provides evidences that abbrogating lipotoxicity by provision of omega 3 fatty acids may prevent age-associated loss of bone and red marrow atrophy in this model. Google Scholar
  14. 14.
    Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17(8):1689–96.  https://doi.org/10.1017/S1368980013002115.CrossRefPubMedGoogle Scholar
  15. 15.
    Park S, Na W, Sohn C. Relationship between osteosarcopenic obesity and dietary inflammatory index in postmenopausal Korean women: 2009 to 2011 Korea National Health and Nutrition Examination Surveys. J Clin Biochem Nutr. 2018;63(3):211–6.  https://doi.org/10.3164/jcbn.18-10.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Orchard T, Yildiz V, Steck SE, Hebert JR, Ma Y, Cauley JA, et al. Dietary inflammatory index, bone mineral density, and risk of fracture in postmenopausal women: results from the women’s health initiative. J Bone Miner Res. 2017;32(5):1136–46.  https://doi.org/10.1002/jbmr.3070.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kim HS, Sohn C, Kwon M, Na W, Shivappa N, Hebert JR, et al. Positive association between dietary inflammatory index and the risk of osteoporosis: results from the KoGES_Health Examinee (HEXA) Cohort Study. Nutrients. 2018;10(12).  https://doi.org/10.3390/nu10121999.CrossRefGoogle Scholar
  18. 18.
    Stefanaki C, Pervanidou P, Boschiero D, Chrousos GP. Chronic stress and body composition disorders: implications for health and disease. Hormones (Athens). 2018;17(1):33–43.  https://doi.org/10.1007/s42000-018-0023-7.CrossRefGoogle Scholar
  19. 19.
    Bulló M, Casas-Agustench P, Amigó-Correig P, Aranceta J, Salas-Salvadó J. Inflammation, obesity and comorbidities: the role of diet. Public Health Nutr. 2007;10(10A):1164–72.  https://doi.org/10.1017/S1368980007000663.CrossRefPubMedGoogle Scholar
  20. 20.
    Bani Hassan E, Phu S, Vogrin S, Escobedo Terrones G, Pérez X, Rodriguez-Sanchez I, et al. Diagnostic value of mid-thigh and mid-calf bone, muscle, and fat mass in osteosarcopenia: a pilot study. Calcif Tissue Int. 2019.  https://doi.org/10.1007/s00223-019-00582-5.CrossRefGoogle Scholar
  21. 21.
    Coppack SW. Pro-inflammatory cytokines and adipose tissue. Proc Nutr Soc. 2001;60(3):349–56.  https://doi.org/10.1079/PNS2001110.CrossRefPubMedGoogle Scholar
  22. 22.
    Ohshima H, Bartsch H. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutat Res. 1994;305(2):253–64.  https://doi.org/10.1016/0027-5107(94)90245-3.CrossRefPubMedGoogle Scholar
  23. 23.
    Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539–45.  https://doi.org/10.1016/S0140-6736(00)04046-0.CrossRefPubMedGoogle Scholar
  24. 24.
    Karaosmanoglu AD, Blake MA, Lennerz JK. Abundant macroscopic fat in intra-abdominal lymph nodes involved in the course of a patient with chronic lymphocytic leukaemia: presentation of imaging findings with biopsy correlation. Br J Radiol. 2012;85(1012):e91–3.  https://doi.org/10.1259/bjr/20677787.CrossRefPubMedGoogle Scholar
  25. 25.
    Li G, Xu Z, Zhuang A, Chang S, Hou L, Chen Y, et al. Magnetic resonance spectroscopy-detected change in marrow adiposity is strongly correlated to postmenopausal breast cancer risk. Clin Breast Cancer. 2017;17(3):239–44.  https://doi.org/10.1016/j.clbc.2017.01.004.CrossRefPubMedGoogle Scholar
  26. 26.
    Li G, Xu Z, Fan J, Yuan W, Zhang L, Hou L, et al. To assess differential features of marrow adiposity between postmenopausal women with osteoarthritis and osteoporosis using water/fat MRI. Menopause. 2017;24(1):105–11.  https://doi.org/10.1097/gme.0000000000000732.CrossRefPubMedGoogle Scholar
  27. 27.
    Kennedy DE, Witte PL, Knight KL. Bone marrow fat and the decline of B lymphopoiesis in rabbits. Dev Comp Immunol. 2016;58:30–9.  https://doi.org/10.1016/j.dci.2015.11.003.CrossRefPubMedGoogle Scholar
  28. 28.
    Hadamitzky C, Spohr H, Debertin AS, Guddat S, Tsokos M, Pabst R. Age-dependent histoarchitectural changes in human lymph nodes: an underestimated process with clinical relevance? J Anat. 2010;216(5):556–62.  https://doi.org/10.1111/j.1469-7580.2010.01213.x.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Khandekar MJ, Cohen P, Spiegelman BM. Molecular mechanisms of cancer development in obesity. Nat Rev Cancer. 2011;11:886.  https://doi.org/10.1038/nrc3174.CrossRefPubMedGoogle Scholar
  30. 30.
    Menendez JA. Fine-tuning the lipogenic/lipolytic balance to optimize the metabolic requirements of cancer cell growth: molecular mechanisms and therapeutic perspectives. Biochim Biophys Acta. 2010;1801(3):381–91.  https://doi.org/10.1016/j.bbalip.2009.09.005.CrossRefPubMedGoogle Scholar
  31. 31.
    de Luca C, Olefsky JM. Inflammation and insulin resistance. FEBS Lett. 2008;582(1):97–105.  https://doi.org/10.1016/j.febslet.2007.11.057.CrossRefPubMedGoogle Scholar
  32. 32.
    McArdle MA, Finucane OM, Connaughton RM, McMorrow AM, Roche HM. Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Front Endocrinol (Lausanne). 2013;4:52.  https://doi.org/10.3389/fendo.2013.00052.CrossRefGoogle Scholar
  33. 33.
    Malkov S, Cawthon PM, Peters KW, Cauley JA, Murphy RA, Visser M, et al. Hip fractures risk in older men and women associated with DXA-derived measures of thigh subcutaneous fat thickness, cross-sectional muscle area, and muscle density. J Bone Miner Res. 2015;30(8):1414–21.  https://doi.org/10.1002/jbmr.2469.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Baum T, Yap SP, Karampinos DC, Nardo L, Kuo D, Burghardt AJ, et al. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine BMD and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging. 2012;35(1):117–24.  https://doi.org/10.1002/jmri.22757.CrossRefPubMedGoogle Scholar
  35. 35.
    Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, et al. Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity (Silver Spring). 2011;19(1):49–53.  https://doi.org/10.1038/oby.2010.106.CrossRefGoogle Scholar
  36. 36.
    Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res. 1971;80:147–54.CrossRefGoogle Scholar
  37. 37.
    Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM. Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr. 2009;19(2):109–24.CrossRefGoogle Scholar
  38. 38.
    Newton AL, Hanks LJ, Davis M, Casazza K. The relationships among total body fat, bone mineral content and bone marrow adipose tissue in early-pubertal girls. Bonekey Rep. 2013;2(4).  https://doi.org/10.1038/bonekey.2013.49.
  39. 39.
    Hounsfield GN. Computed medical imaging. Science. 1980;210(4465):22–8.CrossRefGoogle Scholar
  40. 40.
    Huppertz A, Lembcke A, Sariali el H, Durmus T, Schwenke C, Hamm B, et al. Low dose computed tomography for 3D planning of total hip arthroplasty: evaluation of radiation exposure and image quality. J Comput Assist Tomogr. 2015;39(5):649–56.  https://doi.org/10.1097/rct.0000000000000271.CrossRefPubMedGoogle Scholar
  41. 41.
    Pelegrino Bastos Maues NH, Fattori Alves AF, Menegatti Pavan AL, Marrone Ribeiro S, Yamashita S, Petean Trindade A, et al. Abdomen-pelvis computed tomography protocol optimization: an image quality and dose assessment. Radiat Prot Dosim. 2019;184(1):66–72.  https://doi.org/10.1093/rpd/ncy181.CrossRefGoogle Scholar
  42. 42.
    • Demontiero O, Li W, Thembani E, Duque G. Validation of noninvasive quantification of bone marrow fat volume with microCT in aging rats. Exp Gerontol. 2011;46(6):435–40.  https://doi.org/10.1016/j.exger.2011.01.001This publication is the first to histologiaclly validate single-energy CT for the measurement of MAT. CrossRefPubMedGoogle Scholar
  43. 43.
    Chowdhury B, Sjöström L, Alpsten M, Kostanty J, Kvist H, Löfgren R. A multicompartment body composition technique based on computerized tomography. Int J Obes Relat Metab Disord. 1994;18(4):219–34.PubMedGoogle Scholar
  44. 44.
    Demerath EW, Ritter KJ, Couch WA, Rogers NL, Moreno GM, Choh A, et al. Validity of a new automated software program for visceral adipose tissue estimation. Int J Obes. 2007;31(2):285–91.  https://doi.org/10.1038/sj.ijo.0803409.CrossRefGoogle Scholar
  45. 45.
    Bredella MA, Daley SM, Kalra MK, Brown JK, Miller KK, Torriani M. Marrow adipose tissue quantification of the lumbar spine by using dual-energy CT and single-voxel (1)H MR spectroscopy: a feasibility study. Radiology. 2015;277(1):230–5.  https://doi.org/10.1148/radiol.2015142876.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Uhrig M, Simons D, Kachelrieß M, Pisana F, Kuchenbecker S, Schlemmer H-P. Advanced abdominal imaging with dual energy CT is feasible without increasing radiation dose. Cancer Imaging. 2016;16(1):15.  https://doi.org/10.1186/s40644-016-0073-5.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Horowitz MC, Berry R, Holtrup B, Sebo Z, Nelson T, Fretz JA, et al. Bone marrow adipocytes. Adipocyte. 2017;6(3):193–204.CrossRefGoogle Scholar
  48. 48.
    Lareida A, Beckmann F, Schrott-Fischer A, Glueckert R, Freysinger W, Müller B. High-resolution X-ray tomography of the human inner ear: synchrotron radiation-based study of nerve fibre bundles, membranes and ganglion cells. J Microsc. 2009;234(1):95–102.CrossRefGoogle Scholar
  49. 49.
    Mizutani R, Suzuki Y. X-ray microtomography in biology. Micron. 2012;43(2-3):104–15.CrossRefGoogle Scholar
  50. 50.
    Hardouin P, Marie PJ, Rosen CJ. New insights into bone marrow adipocytes: report from the first European meeting on bone marrow adiposity (BMA 2015). Bone. 2016;93:212–5.CrossRefGoogle Scholar
  51. 51.
    Doucette CR, Horowitz MC, Berry R, MacDougald OA, Anunciado-Koza R, Koza RA, et al. A high fat diet increases bone marrow adipose tissue (MAT) but does not alter trabecular or cortical bone mass in C57BL/6J mice. J Cell Physiol. 2015;230(9):2032–7.CrossRefGoogle Scholar
  52. 52.
    Cawthorn WP, Scheller EL, Learman BS, Parlee SD, Simon BR, Mori H, et al. Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab. 2014;20(2):368–75.CrossRefGoogle Scholar
  53. 53.
    Simon BR, Learman BS, Parlee SD, Scheller EL, Mori H, Cawthorn WP, et al. Sweet taste receptor deficient mice have decreased adiposity and increased bone mass. PLoS One. 2014;9(1):e86454.CrossRefGoogle Scholar
  54. 54.
    Lecka-Czernik B, Stechschulte LA, Czernik PJ, Sherman SB, Huang S, Krings A. Marrow adipose tissue: skeletal location, sexual dimorphism, and response to sex steroid deficiency. Front Endocrinol. 2017;8:188.CrossRefGoogle Scholar
  55. 55.
    Styner M, Thompson WR, Galior K, Uzer G, Wu X, Kadari S, et al. Bone marrow fat accumulation accelerated by high fat diet is suppressed by exercise. Bone. 2014;64:39–46.CrossRefGoogle Scholar
  56. 56.
    Styner M, Pagnotti GM, McGrath C, Wu X, Sen B, Uzer G, et al. Exercise decreases marrow adipose tissue through ß-oxidation in obese running mice. J Bone Miner Res. 2017;32(8):1692–702.CrossRefGoogle Scholar
  57. 57.
    Sulston RJ, Learman BS, Zhang B, Scheller EL, Parlee SD, Simon BR, et al. Increased circulating adiponectin in response to thiazolidinediones: investigating the role of bone marrow adipose tissue. Front Endocrinol. 2016;7:128.CrossRefGoogle Scholar
  58. 58.
    Fairfield H, Falank C, Harris E, Demambro V, McDonald M, Pettitt JA, et al. The skeletal cell-derived molecule sclerostin drives bone marrow adipogenesis. J Cell Physiol. 2018;233(2):1156–67.CrossRefGoogle Scholar
  59. 59.
    Pagnotti GM, Styner M. Exercise regulation of marrow adipose tissue. Front Endocrinol. 2016;7:94.CrossRefGoogle Scholar
  60. 60.
    Johnson JT, Hansen MS, Wu I, Healy LJ, Johnson CR, Jones GM, et al. Virtual histology of transgenic mouse embryos for high-throughput phenotyping. PLoS Genet. 2006;2(4):e61.CrossRefGoogle Scholar
  61. 61.
    Bentley MD, Jorgensen SM, Lerman LO, Ritman EL, Romero JC. Visualization of three-dimensional nephron structure with microcomputed tomography. Anat Rec Adv Integr Anat Evol Biol. 2007;290(3):277–83.CrossRefGoogle Scholar
  62. 62.
    Metscher BD. X-ray microtomographic imaging of intact vertebrate embryos. Cold Spring Harb Protoc. 2011;2011(12) pdb. prot067033.CrossRefGoogle Scholar
  63. 63.
    Litzlbauer HD, Neuhaeuser C, Moell A, Greschus S, Breithecker A, Franke FE, et al. Three-dimensional imaging and morphometric analysis of alveolar tissue from microfocal X-ray-computed tomography. Am J Phys Lung Cell Mol Phys. 2006;291(3):L535–L45.Google Scholar
  64. 64.
    Ritman EL. Molecular imaging in small animals—roles for micro-CT. J Cell Biochem. 2002;87(S39):116–24.CrossRefGoogle Scholar
  65. 65.
    Henning AL, Jiang MX, Yalcin HC, Butcher JT. Quantitative three-dimensional imaging of live avian embryonic morphogenesis via micro-computed tomography. Dev Dyn. 2011;240(8):1949–57.CrossRefGoogle Scholar
  66. 66.
    Scheller EL, Troiano N, VanHoutan JN, Bouxsein MA, Fretz JA, Xi Y, et al. Use of osmium tetroxide staining with microcomputerized tomography to visualize and quantify bone marrow adipose tissue in vivo. Methods Enzymol. Elsevier. 2014;537:123–39.CrossRefGoogle Scholar
  67. 67.
    Scheller EL, Khoury B, Moller KL, Wee NK, Khandaker S, Kozloff KM, et al. Changes in skeletal integrity and marrow adiposity during high-fat diet and after weight loss. Front Endocrinol. 2016;7:102.CrossRefGoogle Scholar
  68. 68.
    Scheller EL, Cawthorn WP, Burr AA, Horowitz MC, MacDougald OA. Marrow adipose tissue: trimming the fat. Trends Endocrinol Metab. 2016;27(6):392–403.CrossRefGoogle Scholar
  69. 69.
    de Crespigny A, Bou-Reslan H, Nishimura MC, Phillips H, Carano RA, D’Arceuil HE. 3D micro-CT imaging of the postmortem brain. J Neurosci Methods. 2008;171(2):207–13.CrossRefGoogle Scholar
  70. 70.
    Hardouin P, Rharass T, Lucas S. Bone marrow adipose tissue: to be or not to be a typical adipose tissue? Front Endocrinol. 2016;7:85.CrossRefGoogle Scholar
  71. 71.
    Scheller EL, Doucette CR, Learman BS, Cawthorn WP, Khandaker S, Schell B, et al. Region-specific variation in the properties of skeletal adipocytes reveals regulated and constitutive marrow adipose tissues. Nat Commun. 2015;6:7808.CrossRefGoogle Scholar
  72. 72.
    Alecci M, Collins CM, Smith MB, Jezzard P. Radio frequency magnetic field mapping of a 3 Tesla birdcage coil: experimental and theoretical dependence on sample properties. Magn Reson Med. 2001;46(2):379–85.CrossRefGoogle Scholar
  73. 73.
    Formica D, Silvestri S. Biological effects of exposure to magnetic resonance imaging: an overview. Biomed Eng Online. 2004;3:11.  https://doi.org/10.1186/1475-925X-3-11.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Porter BA, Shields AF, Olson DO. Magnetic resonance imaging of bone marrow disorders. Radiol Clin N Am. 1986;24(2):269–89.PubMedGoogle Scholar
  75. 75.
    Baum T, Yap SP, Karampinos DC, Nardo L, Kuo D, Burghardt AJ, et al. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging. 2012;35(1):117–24.  https://doi.org/10.1002/jmri.22757.CrossRefPubMedGoogle Scholar
  76. 76.
    Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, et al. 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. 2005;236(3):945–51.  https://doi.org/10.1148/radiol.2363041425.CrossRefPubMedGoogle Scholar
  77. 77.
    Griffith JF, Yeung DK, Antonio GE, Wong SY, Kwok TC, Woo J, et al. Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation. Radiology. 2006;241(3):831–8.  https://doi.org/10.1148/radiol.2413051858.CrossRefPubMedGoogle Scholar
  78. 78.
    Moulopoulos LA, Dimopoulos MA. Magnetic resonance imaging of the bone marrow in hematologic malignancies. Blood. 1997;90(6):2127–47.CrossRefGoogle Scholar
  79. 79.
    • Karampinos DC, Ruschke S, Dieckmeyer M, Diefenbach M, Franz D, Gersing AS, et al. Quantitative MRI and spectroscopy of bone marrow. J Magn Reson Imaging. 2018;47(2):332–53.  https://doi.org/10.1002/jmri.25769This paper is one of the most recent and important publicaitons that discusses the quantitiative MRI approach towards MAT imaging. CrossRefPubMedGoogle Scholar
  80. 80.
    Pooley RA. AAPM/RSNA physics tutorial for residents: fundamental physics of MR imaging. Radiographics. 2005;25(4):1087–99.  https://doi.org/10.1148/rg.254055027.CrossRefPubMedGoogle Scholar
  81. 81.
    Shayganfar A, Khodayi M, Ebrahimian S, Tabrizi Z. Quantitative diagnosis of osteoporosis using lumbar spine signal intensity in magnetic resonance imaging. Br J Radiol. 2019;92(1097):20180774.  https://doi.org/10.1259/bjr.20180774.CrossRefPubMedGoogle Scholar
  82. 82.
    Shah LM, Hanrahan CJ. MRI of spinal bone marrow: part I, techniques and normal age-related appearances. AJR Am J Roentgenol. 2011;197(6):1298–308.  https://doi.org/10.2214/ajr.11.7005.CrossRefPubMedGoogle Scholar
  83. 83.
    Pichardo JC, Milner RJ, Bolch WE. MRI measurement of bone marrow cellularity for radiation dosimetry. J Nucl Med. 2011;52(9):1482–9.  https://doi.org/10.2967/jnumed.111.087957.CrossRefPubMedGoogle Scholar
  84. 84.
    Li X, Kuo D, Schafer AL, Porzig A, Link TM, Black D, et al. Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging. 2011;33(4):974–9.  https://doi.org/10.1002/jmri.22489.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Schick F, Bongers H, Jung WI, Skalej M, Lutz O, Claussen CD. Volume-selective proton MRS in vertebral bodies. Magn Reson Med. 1992;26(2):207–17.CrossRefGoogle Scholar
  86. 86.
    Devlin MJ. Bone marrow composition, diabetes, and fracture risk: more bad news for saturated fat. J Bone Miner Res. 2013;28(8):1718–20.  https://doi.org/10.1002/jbmr.2013.CrossRefPubMedGoogle Scholar
  87. 87.
    Yeung DK, Griffith JF, Antonio GE, Lee FK, Woo J, Leung PC. Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J Magn Reson Imaging. 2005;22(2):279–85.  https://doi.org/10.1002/jmri.20367.CrossRefPubMedGoogle Scholar
  88. 88.
    Patsch JM, Li X, Baum T, Yap SP, Karampinos DC, Schwartz AV, et al. Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res. 2013;28(8):1721–8.  https://doi.org/10.1002/jbmr.1950.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Li S, Huang B, Jiang B, Gu M, Yang X, Yin Y. Sclerostin antibody mitigates estrogen deficiency-inducted marrow lipid accumulation assessed by proton MR spectroscopy. Front Endocrinol (Lausanne). 2019;10:159.  https://doi.org/10.3389/fendo.2019.00159.CrossRefGoogle Scholar
  90. 90.
    Michalet X, Pinaud FF, Bentolila LA, Tsay JM, Doose S, Li JJ, et al. Quantum dots for live cells, in vivo imaging, and diagnostics. Science. 2005;307(5709):538–44.  https://doi.org/10.1126/science.1104274.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Zebaze R, Osima M, Bui M, Lukic M, Wang X, Ghasem-Zadeh A, et al. Adding marrow adiposity and cortical porosity to femoral neck areal bone mineral density improves the discrimination of women with nonvertebral fractures from controls. J Bone Miner Res. 2019.  https://doi.org/10.1002/jbmr.3721.CrossRefGoogle Scholar
  92. 92.
    Bjornerem A, Wang X, Bui M, Ghasem-Zadeh A, Hopper JL, Zebaze R, et al. Menopause-related appendicular bone loss is mainly cortical and results in increased cortical porosity. J Bone Miner Res. 2018;33(4):598–605.  https://doi.org/10.1002/jbmr.3333.CrossRefPubMedGoogle Scholar
  93. 93.
    Bjornerem A, Ghasem-Zadeh A, Wang X, Bui M, Walker SP, Zebaze R, et al. Irreversible deterioration of cortical and trabecular microstructure associated with breastfeeding. J Bone Miner Res. 2017;32(4):681–7.  https://doi.org/10.1002/jbmr.3018.CrossRefPubMedGoogle Scholar
  94. 94.
    Ahmed LA, Shigdel R, Joakimsen RM, Eldevik OP, Eriksen EF, Ghasem-Zadeh A, et al. Measurement of cortical porosity of the proximal femur improves identification of women with nonvertebral fragility fractures. Osteoporos Int. 2015;26(8):2137–46.  https://doi.org/10.1007/s00198-015-3118-x.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Baum T, Yap SP, Dieckmeyer M, Ruschke S, Eggers H, Kooijman H, et al. Assessment of whole spine vertebral bone marrow fat using chemical shift-encoding based water-fat MRI. J Magn Reson Imaging. 2015;42(4):1018–23.  https://doi.org/10.1002/jmri.24854.CrossRefPubMedGoogle Scholar
  96. 96.
    Gausden EB, Nwachukwu BU, Schreiber JJ, Lorich DG, Lane JM. Opportunistic use of CT imaging for osteoporosis screening and bone density assessment: a qualitative systematic review. J Bone Joint Surg Am. 2017;99(18):1580–90.  https://doi.org/10.2106/jbjs.16.00749.CrossRefPubMedGoogle Scholar
  97. 97.
    Wong AKO, Manske SL. A comparison of peripheral imaging technologies for bone and muscle quantification: a review of segmentation techniques. J Clin Densitom. 2018.  https://doi.org/10.1016/j.jocd.2018.04.001.
  98. 98.
    Al Saedi A, Bani Hassan E, Duque G. The diagnostic role of fat in osteosarcopenia. J Lab Precis Med 2019;4:7.CrossRefGoogle Scholar
  99. 99.
    •• Duque G, Li W, Adams M, Xu S, Phipps R. Effects of risedronate on bone marrow adipocytes in postmenopausal women. Osteoporos Int. 2011;22(5):1547–53.  https://doi.org/10.1007/s00198-010-1353-8Bisphosphonate therapy decreases MAT volume about 10 times more than it increases bone volume; which is the very much ignored aspect of how MAT impacts bone health. Interestingly, increased bone volumes only explain a small fraction of fracture risk decline that may be predicted by MAT decline—if reliable and affordable measurement tools are developed. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ebrahim Bani Hassan
    • 1
    • 2
  • Ali Ghasem-Zadeh
    • 1
    • 3
  • Mahdi Imani
    • 1
    • 2
  • Numan Kutaiba
    • 4
  • David K. Wright
    • 5
  • Tara Sepehrizadeh
    • 6
  • Gustavo Duque
    • 1
    • 2
    Email author
  1. 1.Australian Institute for Musculoskeletal Science (AIMSS)The University of Melbourne and Western HealthSt. AlbansAustralia
  2. 2.Department of Medicine-Western HealthThe University of MelbourneSt. AlbansAustralia
  3. 3.Department of Medicine and EndocrinologyAustin HealthMelbourneAustralia
  4. 4.Austin Health, Department of RadiologyHeidelbergAustralia
  5. 5.Department of Neuroscience, Central Clinical SchoolMonash UniversityMelbourneAustralia
  6. 6.Monash Biomedical ImagingMonash UniversityMelbourneAustralia

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