Techniques for Diffusion and Perfusion Assessment in Bone-Marrow MRI

Part of the Medical Radiology book series (MEDRAD)


In addition to conventional magnetic resonance imaging (MRI) approaches of bone marrow such as T 1-weighted or short-tau inversion-recovery (STIR) MRI, newer techniques are available today allowing the visual and also quantitative assessment of several microstructural and physiological tissue parameters. The most important of these new techniques are MRI of hemodynamic parameters (“perfusion MRI”) and MRI of molecular water diffusion (“diffusion MRI”). Both techniques are aimed at tissue parameters beyond proton density, relaxation properties, or fat content. They allow the (absolute) quantification of properties such as the diffusion coefficient of water molecules in tissue or hemodynamic parameters including the blood volume and the blood flow. In this chapter, the physical and physiological basics of diffusion and perfusion MRI are introduced and discussed with respect to their application in bone-marrow MRI. Non-quantitative and quantitative approaches for the analysis of diffusion-weighted images and semi-quantitative and quantitative approaches for the analysis of dynamic contrast-enhanced perfusion MRI are discussed.


Apparent Diffusion Coefficient Fractional Anisotropy Diffusion Gradient Perfusion Magnetic Resonance Imaging Diffusion Weighting 


  1. Alsop DC (1997) Phase insensitive preparation of single-shot RARE: application to diffusion imaging in humans. Magn Reson Med 38(4):527–533PubMedCrossRefGoogle Scholar
  2. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219PubMedCrossRefGoogle Scholar
  3. Basser PJ, Pierpaoli C (1998) A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 39(6):928–934PubMedCrossRefGoogle Scholar
  4. Basser PJ, Mattiello J et al (1994a) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103(3):247–254CrossRefGoogle Scholar
  5. Basser PJ, Mattiello J et al (1994b) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267CrossRefGoogle Scholar
  6. Baur A, Stabler A et al (1998) Diffusion-weighted MR imaging of bone marrow: differentiation of benign versus pathologic compression fractures. Radiology 207(2):349–356PubMedGoogle Scholar
  7. Baur A, Huber A et al (2001) Diagnostic value of increased diffusion weighting of a steady-state free precession sequence for differentiating acute benign osteoporotic fractures from pathologic vertebral compression fractures. AJNR Am J Neuroradiol 22(2):366–372PubMedGoogle Scholar
  8. Biffar A, Dietrich O et al (2010a) Diffusion and perfusion imaging of bone marrow. Eur J Radiol 76(3):323–328PubMedCrossRefGoogle Scholar
  9. Biffar A, Sourbron S et al (2010b) Combined diffusion-weighted and dynamic contrast-enhanced imaging of patients with acute osteoporotic vertebral fractures. Eur J Radiol 76(3):298–303PubMedCrossRefGoogle Scholar
  10. Biffar A, Sourbron S et al (2010c) Measurement of perfusion and permeability from dynamic contrast-enhanced MRI in normal and pathological vertebral bone marrow. Magn Reson Med 64(1):115–124PubMedCrossRefGoogle Scholar
  11. Biffar A, Baur-Melnyk A et al (2011a) Quantitative analysis of the diffusion-weighted steady-state free precession signal in vertebral bone marrow lesions. Invest Radiol 46(10):601–609PubMedCrossRefGoogle Scholar
  12. Biffar A, Schmidt GP et al (2011b) Quantitative analysis of vertebral bone marrow perfusion using dynamic contrast-enhanced MRI: initial results in osteoporotic patients with acute vertebral fracture. J Magn Reson Imaging 33(3):676–683PubMedCrossRefGoogle Scholar
  13. Brix G, Griebel J et al (2010) Tracer kinetic modelling of tumour angiogenesis based on dynamic contrast-enhanced CT and MRI measurements. Eur J Nucl Med Mol Imaging 37(Suppl 1):S30–S51PubMedCrossRefGoogle Scholar
  14. Brockstedt S, Moore JR et al (2000) High-resolution diffusion imaging using phase-corrected segmented echo-planar imaging. Magn Reson Imaging 18(6):649–657PubMedCrossRefGoogle Scholar
  15. Bruder H, Fischer H et al (1988) A new steady-state imaging sequence for simultaneous acquisition of two MR images with clearly different contrasts. Magn Reson Med 7(1):35–42PubMedCrossRefGoogle Scholar
  16. Buxton RB (1993) The diffusion sensitivity of fast steady-state free precession imaging. Magn Reson Med 29(2):235–243PubMedCrossRefGoogle Scholar
  17. Capuani S, Rossi C et al (2005) Diffusion tensor imaging to study anisotropy in a particular porous system: the trabecular bone network. Solid State Nucl Magn Reson 28(2–4):266–272PubMedCrossRefGoogle Scholar
  18. Chan WP, Liu YJ et al (2011) Relationship of idiopathic osteonecrosis of the femoral head to perfusion changes in the proximal femur by dynamic contrast-enhanced MRI. Am J Roentgenol 196(3):637–643CrossRefGoogle Scholar
  19. Chen WT, Shih TT et al (2001) Vertebral bone marrow perfusion evaluated with dynamic contrast-enhanced MR imaging: significance of aging and sex. Radiology 220(1):213–218PubMedGoogle Scholar
  20. Chen WT, Shih TT et al (2002) Blood perfusion of vertebral lesions evaluated with gadolinium-enhanced dynamic MRI: in comparison with compression fracture and metastasis. J Magn Reson Imaging 15(3):308–314PubMedCrossRefGoogle Scholar
  21. Cohen Y, Assaf Y (2002) High b-value q-space analyzed diffusion-weighted MRS and MRI in neuronal tissues––a technical review. NMR Biomed 15(7–8):516–542PubMedCrossRefGoogle Scholar
  22. Courcoutsakis N, Spanoudaki A et al (2011) Perfusion parameters analysis of the vertebral bone marrow in patients with Ph(1-) chronic myeloproliferative neoplasms (Ph(neg) MPN): a dynamic contrast-enhanced MRI (DCE-MRI) study. J Magn Reson Imaging. doi: 10.1002/jmri.22870 [Epub ahead of print]
  23. D’Agostino F, Dell’Aia P et al (2010) Differentiation of normal and neoplastic bone tissue in dynamic gadolinium-enhanced magnetic resonance imaging: validation of a semiautomated technique. Radiol Med 115(5):804–814PubMedCrossRefGoogle Scholar
  24. Deoni SC, Peters TM et al (2004) Quantitative diffusion imaging with steady-state free precession. Magn Reson Med 51(2):428–433PubMedCrossRefGoogle Scholar
  25. Dietrich O (2008) Diffusion-weighted imaging and diffusion tensor imaging. In: Reiser MF, Semmler W, Hricak H (eds) Magnetic Resonance Tomography. Springer, Heidelberg, pp. 130−152Google Scholar
  26. Dietrich O, Biffar A et al (2009) Diffusion-weighted imaging of bone marrow. Semin Musculoskelet Radiol 13(2):134–144PubMedCrossRefGoogle Scholar
  27. Dietrich O, Biffar A et al (2010) Technical aspects of MR diffusion imaging of the body. Eur J Radiol 76(3):314–322PubMedCrossRefGoogle Scholar
  28. Dietrich O, Baur-Melnyk A (2011) Diffusion-weighted MR imaging of the bone marrow and the spine. In: Taouli B (ed) Extra-cranial applications of diffusion-weighted MRI. Cambridge University Press, Cambridge, pp 144–161Google Scholar
  29. Dyke JP, Aaron RK (2010) Noninvasive methods of measuring bone blood perfusion. Ann N Y Acad Sci 1192:95–102PubMedCrossRefGoogle Scholar
  30. Erlemann R, Reiser MF et al (1989) Musculoskeletal neoplasms: static and dynamic Gd-DTPA–enhanced MR imaging. Radiology 171(3):767–773PubMedGoogle Scholar
  31. Gerdes CM, Kijowski R et al (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(5):W284–W291PubMedCrossRefGoogle Scholar
  32. Glaser C, Weckbach S et al (2008) Musculoskeletal system. In: Reiser MF, Semmler W, Hricak H (eds) Magnetic resonance tomography. Springer, Heidelberg, pp 1079–1176CrossRefGoogle Scholar
  33. Griffith JF, Yeung DK et al (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(3):945–951PubMedCrossRefGoogle Scholar
  34. Griffith JF, Yeung DK et al (2009) Reproducibility of MR perfusion and (1)H spectroscopy of bone marrow. J Magn Reson Imaging 29(6):1438–1442PubMedCrossRefGoogle Scholar
  35. Griffith JF, Yeung DK et al (2011) Prediction of bone loss in elderly female subjects by MR perfusion imaging and spectroscopy. Eur Radiol 21(6):1160–1169PubMedCrossRefGoogle Scholar
  36. Gudbjartsson H, Maier SE et al (1996) Line scan diffusion imaging. Magn Reson Med 36(4):509–519PubMedCrossRefGoogle Scholar
  37. Gyngell ML (1988) The application of steady-state free precession in rapid 2DFT NMR imaging: FAST and CE-FAST sequences. Magn Reson Imaging 6(4):415–419PubMedCrossRefGoogle Scholar
  38. Hahn EL (1950) Spin echoes. Phys Rev 80(4):580–594CrossRefGoogle Scholar
  39. Jackson A, Buckley DL et al (eds) (2005) Dynamic contrast-enhanced magnetic resonance imaging in oncology. Medical radiology––diagnostic imaging. Springer, HeidelbergGoogle Scholar
  40. Jensen JH, Helpern JA (2010) MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed 23(7):698–710PubMedCrossRefGoogle Scholar
  41. Kind T, Houtzager I et al (2010) Evaluation of model-independent deconvolution techniques to estimate blood perfusion. Conf Proc IEEE Eng Med Biol Soc 2602–2607PubMedGoogle Scholar
  42. Koh DM, Collins DJ et al (2011) Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges. AJR Am J Roentgenol 196(6):1351–1361PubMedCrossRefGoogle Scholar
  43. Korosec FR, Frayne R et al (1996) Time-resolved contrast-enhanced 3D MR angiography. Magn Reson Med 36(3):345–351PubMedCrossRefGoogle Scholar
  44. Lambregts DM, Maas M et al (2011) Whole-body diffusion-weighted magnetic resonance imaging: current evidence in oncology and potential role in colorectal cancer staging. Eur J Cancer 47(14):2107–2116PubMedCrossRefGoogle Scholar
  45. Le Bihan D (1988) Intravoxel incoherent motion imaging using steady-state free precession. Magn Reson Med 7(3):346–351PubMedCrossRefGoogle Scholar
  46. Le Bihan D, Breton E et al (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161(2):401–407PubMedGoogle Scholar
  47. Le Bihan D, Breton E et al (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168(2):497–505PubMedGoogle Scholar
  48. Le Roux P (2002) Non-CPMG Fast Spin Echo with full signal. J Magn Reson 155(2):278–292PubMedCrossRefGoogle Scholar
  49. Lee H, Price RR (1994) Diffusion imaging with the MP-RAGE sequence. J Magn Reson Imaging 4(6):837–842PubMedCrossRefGoogle Scholar
  50. Lee JH, Dyke JP et al (2009) Assessment of bone perfusion with contrast-enhanced magnetic resonance imaging. Orthop Clin North Am 40(2):249–257PubMedCrossRefGoogle Scholar
  51. Li X, Yu A et al (2012) Quantitative characterization of bone marrow edema pattern in rheumatoid arthritis using 3 Tesla MRI. J Magn Reson Imaging 35(1):211–217PubMedCrossRefGoogle Scholar
  52. Lim RP, Shapiro M et al (2008) 3D time-resolved MR angiography (MRA) of the carotid arteries with time-resolved imaging with stochastic trajectories: comparison with 3D contrast-enhanced Bolus-Chase MRA and 3D time-of-flight MRA. AJNR Am J Neuroradiol 29(10):1847–1854PubMedCrossRefGoogle Scholar
  53. Luypaert R, Boujraf S et al (2001) Diffusion and perfusion MRI: basic physics. Eur J Radiol 38(1):19–27PubMedCrossRefGoogle Scholar
  54. Ma HT, Griffith JF et al (2010) Modified brix model analysis of bone perfusion in subjects of varying bone mineral density. J Magn Reson Imaging 31(5):1169–1175PubMedCrossRefGoogle Scholar
  55. Meier P, Zierler KL (1954) On the theory of the indicator-dilution method for measurement of blood flow and volume. J Appl Physiol 6(12):731–744PubMedGoogle Scholar
  56. Merboldt KD, Hanicke W et al (1985) Self-Diffusion NMR Imaging Using Stimulated Echoes. J Magn Reson 64(3):479–486Google Scholar
  57. Merboldt KD, Bruhn H et al (1989) MRI of “diffusion” in the human brain: new results using a modified CE-FAST sequence. Magn Reson Med 9(3):423–429PubMedCrossRefGoogle Scholar
  58. Moehler TM, Hawighorst H et al (2001) Bone marrow microcirculation analysis in multiple myeloma by contrast-enhanced dynamic magnetic resonance imaging. Int J Cancer 93(6):862–868PubMedCrossRefGoogle Scholar
  59. Montazel JL, Divine M et al (2003) Normal spinal bone marrow in adults: dynamic gadolinium-enhanced MR imaging. Radiology 229(3):703–709PubMedCrossRefGoogle Scholar
  60. Norris DG (2007) Selective parity RARE imaging. Magn Reson Med 58(4):643–649PubMedCrossRefGoogle Scholar
  61. Norris DG, Bornert P et al (1992) On the application of ultra-fast RARE experiments. Magn Reson Med 27(1):142–164PubMedCrossRefGoogle Scholar
  62. Nosas-Garcia S, Moehler T et al (2005) Dynamic contrast-enhanced MRI for assessing the disease activity of multiple myeloma: a comparative study with histology and clinical markers. J Magn Reson Imaging 22(1):154–162PubMedCrossRefGoogle Scholar
  63. Oppelt A, Graumann R et al (1986) FISP—a new fast MRI sequence. Electromedica 54:15–18Google Scholar
  64. Ostergaard L (2004) Cerebral perfusion imaging by bolus tracking. Top Magn Reson Imaging 15(1):3–9PubMedCrossRefGoogle Scholar
  65. Petersen ET, Zimine I et al (2006) Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79(944):688–701PubMedCrossRefGoogle Scholar
  66. Pipe JG, Farthing VG et al (2002) Multishot diffusion-weighted FSE using PROPELLER MRI. Magn Reson Med 47(1):42–52PubMedCrossRefGoogle Scholar
  67. Rahmouni A, Montazel JL et al (2003) Bone marrow with diffuse tumor infiltration in patients with lymphoproliferative diseases: dynamic gadolinium-enhanced MR imaging. Radiology 229(3):710–717PubMedCrossRefGoogle Scholar
  68. Robson MD, Anderson AW et al (1997) Diffusion-weighted multiple shot echo planar imaging of humans without navigation. Magn Reson Med 38(1):82–88PubMedCrossRefGoogle Scholar
  69. Rossi C, Capuani S et al (2005) DTI of trabecular bone marrow. Magn Reson Imaging 23(2):245–248PubMedCrossRefGoogle Scholar
  70. Savvopoulou V, Maris TG et al (2011) Degenerative endplate changes of the lumbosacral spine: dynamic contrast-enhanced MRI profiles related to age, sex, and spinal level. J Magn Reson Imaging 33(2):382–389PubMedCrossRefGoogle Scholar
  71. Shih TT, Liu HC et al (2004) Correlation of MR lumbar spine bone marrow perfusion with bone mineral density in female subjects. Radiology 233(1):121–128PubMedCrossRefGoogle Scholar
  72. Silbernagl S, Despopoulos A (2008) Color atlas of physiology. Thieme, StuttgartGoogle Scholar
  73. Sourbron S (2010) Technical aspects of MR perfusion. Eur J Radiol 76(3):304–313PubMedCrossRefGoogle Scholar
  74. Sourbron SP, Buckley DL (2012) Tracer kinetic modelling in MRI: estimating perfusion and capillary permeability. Phys Med Biol 57(2):R1–R33PubMedCrossRefGoogle Scholar
  75. Stejskal EO, Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phy 42(1):288–292CrossRefGoogle Scholar
  76. Takahara T, Imai Y et al (2004) Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display. Radiat Med 22(4):275–282PubMedGoogle Scholar
  77. Taylor DG, Bushell MC (1985) The spatial-mapping of translational diffusion-coefficients by the NMR imaging technique. Phys Med Biol 30(4):345–349PubMedCrossRefGoogle Scholar
  78. Tokuda O, Hayashi N et al (2005) Dynamic contrast-enhanced perfusion MR imaging of diseased vertebrae: analysis of three parameters and the distribution of the time-intensity curve patterns. Skeletal Radiol 34(10):632–638PubMedCrossRefGoogle Scholar
  79. Turner R, Le Bihan D et al (1990) Echo-planar imaging of intravoxel incoherent motion. Radiology 177(2):407–414PubMedGoogle Scholar
  80. Vanel D (2004) MRI of bone metastases: the choice of the sequence. Cancer Imaging 4(1):30–35PubMedCrossRefGoogle Scholar
  81. Wu EX, Buxton RB (1990) Effect of diffusion on the steady-state magnetization with pulsed field gradients. J Magn Reson 90(2):243–253Google Scholar
  82. Wu LM, Gu HY et al (2011) Diagnostic value of whole-body magnetic resonance imaging for bone metastases: a systematic review and meta-analysis. J Magn Reson Imaging 34(1):128–135PubMedCrossRefGoogle Scholar
  83. Zierler KL (1962) Theoretical basis of indicator-dilution methods for measuring flow and volume. Circ Res 10(3):393–407CrossRefGoogle Scholar
  84. Zierler KL (1965) Equations for measuring blood flow by external monitoring of radioisotopes. Circ Res 16:309–321PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Josef Lissner Laboratory for Biomedical Imaging, Department of Clinical Radiology-Großhadern Ludwig Maximilian University (LMU) of MunichMunichGermany

Personalised recommendations