Diffusion-Weighted Imaging of Bone Marrow

ABSTRACT

In diffusion-weighted magnetic resonance imaging (DWI-MRI), the observed MRI signal intensity is attenuated by the self-diffusion of water molecules. DWI can provide information about the microscopic structure and organization of biological tissue and thus can depict various pathological changes of organs or tissues. DWI has been successfully used for the characterization of bone marrow alterations or lesions, and in particular for the differentiation of benign and malignant vertebral compression fractures. In this review article, the basics of DWI are introduced, and several pulse sequences that have been used for DWI of the bone marrow are described. Subsequently, an extensive overview about diffusion studies of the bone marrow and in particular of DWI of vertebral compression fractures is provided.

KEYWORDS

Diffusion-weighted magnetic resonance imaging - bone marrow - vertebral compression fractures - pulse sequences

REFERENCES

• 1 Karaarslan E, Arslan A. Diffusion weighted MR imaging in non-infarct lesions of the brain.  Eur J Radiol. 2008;  65(3) 402-416
• 2 Provenzale J M, Mukundan S, Barboriak D P. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response.  Radiology. 2006;  239(3) 632-649
• 3 Cartes-Zumelzu F W, Stavrou I, Castillo M, Eisenhuber E, Knosp E, Thurnher M M. Diffusion-weighted imaging in the assessment of brain abscesses therapy.  AJNR Am J Neuroradiol. 2004;  25(8) 1310-1317
• 4 Horsfield M A, Jones D K. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review.  NMR Biomed. 2002;  15(7-8) 570-577
• 5 Schaefer P W, Copen W A, Lev M H, Gonzalez R G. Diffusion-weighted imaging in acute stroke.  Magn Reson Imaging Clin N Am. 2006;  14(2) 141-168
• 6 Davis D P, Robertson T, Imbesi S G. Diffusion-weighted magnetic resonance imaging versus computed tomography in the diagnosis of acute ischemic stroke.  J Emerg Med. 2006;  31(3) 269-277
• 7 Parikh T, Drew S J, Lee V S et al.. Focal liver lesion detection and characterization with diffusion-weighted MR imaging: comparison with standard breath-hold T2-weighted imaging.  Radiology. 2008;  246(3) 812-822
• 8 Zech C J, Herrmann K A, Dietrich O, Horger W, Reiser M F, Schoenberg S O. Black-blood diffusion-weighted EPI acquisition of the liver with parallel imaging: comparison with a standard T2-weighted sequence for detection of focal liver lesions.  Invest Radiol. 2008;  43(4) 261-266
• 9 Zhang J, Tehrani Y M, Wang L, Ishill N M, Schwartz L H, Hricak H. Renal masses: characterization with diffusion-weighted MR imaging—a preliminary experience.  Radiology. 2008;  247(2) 458-464
• 10 Cova M, Squillaci E, Stacul F et al.. Diffusion-weighted MRI in the evaluation of renal lesions: preliminary results.  Br J Radiol. 2004;  77(922) 851-857
• 11 Nagata S, Nishimura H, Uchida M et al.. Diffusion-weighted imaging of soft tissue tumors: usefulness of the apparent diffusion coefficient for differential diagnosis.  Radiat Med. 2008;  26(5) 287-295
• 12 Dietrich O, Raya J G, Sommer J, Deimling M, Reiser M F, Baur-Melnyk A. A comparative evaluation of a RARE-based single-shot pulse sequence for diffusion-weighted MRI of musculoskeletal soft-tissue tumors.  Eur Radiol. 2005;  15(4) 772-783
• 13 Takahara T, Imai Y, Yamashita T, Yasuda S, Nasu S, Van Cauteren M. Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display.  Radiat Med. 2004;  22(4) 275-282
• 14 Kwee T C, Takahara T, Ochiai R, Nievelstein R A, Luijten P R. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potential applications in oncology.  Eur Radiol. 2008;  18(9) 1937-1952
• 15 Raya J G, Dietrich O, Reiser M F, Baur-Melnyk A. Methods and applications of diffusion imaging of vertebral bone marrow.  J Magn Reson Imaging. 2006;  24(6) 1207-1220
• 16 Baur A, Stäbler A, Brüning R et al.. Diffusion-weighted MR imaging of bone marrow: differentiation of benign versus pathologic compression fractures.  Radiology. 1998;  207(2) 349-356
• 17 Karchevsky M, Babb J S, Schweitzer M E. Can diffusion-weighted imaging be used to differentiate benign from pathologic fractures? A meta-analysis.  Skeletal Radiol. 2008;  37(9) 791-795
• 18 Raya J G, Dietrich O, Reiser M F, Baur-Melnyk A. Techniques for diffusion-weighted imaging of bone marrow.  Eur J Radiol. 2005;  55(1) 64-73
• 19 Hahn E L. Spin echoes.  Phys Rev. 1950;  80 580-594
• 20 Stejskal E O, Tanner J E. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient.  J Chem Phys. 1965;  42 288-292
• 21 Xing D, Papadakis N G, Huang C L, Lee V M, Carpenter T A, Hall L D. Optimised diffusion-weighting for measurement of apparent diffusion coefficient (ADC) in human brain.  Magn Reson Imaging. 1997;  15(7) 771-784
• 22 Trouard T P, Sabharwal Y, Altbach M I, Gmitro A F. Analysis and comparison of motion-correction techniques in diffusion-weighted imaging.  J Magn Reson Imaging. 1996;  6(6) 925-935
• 23 Norris D G. Implications of bulk motion for diffusion-weighted imaging experiments: effects, mechanisms, and solutions.  J Magn Reson Imaging. 2001;  13(4) 486-495
• 24 Basser P J, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging.  Biophys J. 1994;  66(1) 259-267
• 25 Basser P J, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI.  J Magn Reson B. 1996;  111(3) 209-219
• 26 Basser P J, Pierpaoli C. A simplified method to measure the diffusion tensor from seven MR images.  Magn Reson Med. 1998;  39(6) 928-934
• 27 Merboldt K D, Hänicke W, Frahm J. Self-diffusion NMR imaging using stimulated echoes.  J Magn Reson. 1985;  64 479-486
• 28 Taylor D G, Bushell M C. The spatial mapping of translational diffusion coefficients by the NMR imaging technique.  Phys Med Biol. 1985;  30(4) 345-349
• 29 Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders.  Radiology. 1986;  161(2) 401-407
• 30 Ordidge R J, Helpern J A, Qing Z X, Knight R A, Nagesh V. Correction of motional artifacts in diffusion-weighted MR images using navigator echoes.  Magn Reson Imaging. 1994;  12(3) 455-460
• 31 Anderson A W, Gore J C. Analysis and correction of motion artifacts in diffusion weighted imaging.  Magn Reson Med. 1994;  32(3) 379-387
• 32 Dietrich O, Heiland S, Benner T, Sartor K. Reducing motion artefacts in diffusion-weighted MRI of the brain: efficacy of navigator echo correction and pulse triggering.  Neuroradiology. 2000;  42(2) 85-91
• 33 Gmitro A F, Alexander A L. Use of a projection reconstruction method to decrease motion sensitivity in diffusion-weighted MRI.  Magn Reson Med. 1993;  29(6) 835-838
• 34 Dietrich O, Herlihy A, Dannels W R et al.. Diffusion-weighted imaging of the spine using radial k-space trajectories.  MAGMA. 2001;  12 23-31
• 35 Gudbjartsson H, Maier S E, Mulkern R V, Mórocz I A, Patz S, Jolesz F A. Line scan diffusion imaging.  Magn Reson Med. 1996;  36(4) 509-519
• 36 Turner R, Le Bihan D, Maier J, Vavrek R, Hedges L K, Pekar J. Echo-planar imaging of intravoxel incoherent motion.  Radiology. 1990;  177(2) 407-414
• 37 Jaermann T, Pruessmann K P, Valavanis A, Kollias S, Boesiger P. Influence of SENSE on image properties in high-resolution single-shot echo-planar DTI.  Magn Reson Med. 2006;  55(2) 335-342
• 38 Norris D G, Börnert P, Reese T, Leibfritz D. On the application of ultra-fast RARE experiments.  Magn Reson Med. 1992;  27(1) 142-164
• 39 Schick F. SPLICE: sub-second diffusion-sensitive MR imaging using a modified fast spin-echo acquisition mode.  Magn Reson Med. 1997;  38(4) 638-644
• 40 Alsop D C. Phase insensitive preparation of single-shot RARE: application to diffusion imaging in humans.  Magn Reson Med. 1997;  38(4) 527-533
• 41 Pipe J G, Farthing V G, Forbes K P. Multishot diffusion-weighted FSE using PROPELLER MRI.  Magn Reson Med. 2002;  47(1) 42-52 , (Erratum in: Magn Reson Med 2002;47:621)
• 42 Gyngell M L. The application of steady-state free precession in rapid 2DFT NMR imaging: FAST and CE-FAST sequences.  Magn Reson Imaging. 1988;  6(4) 415-419
• 43 Bruder H, Fischer H, Graumann R, Deimling M. A new steady-state imaging sequence for simultaneous acquisition of two MR images with clearly different contrasts.  Magn Reson Med. 1988;  7(1) 35-42
• 44 Le Bihan D. Intravoxel incoherent motion imaging using steady-state free precession.  Magn Reson Med. 1988;  7(3) 346-351
• 45 Merboldt K D, Bruhn H, Frahm J, Gyngell M L, Hänicke W, Deimling M. MRI of “diffusion” in the human brain: new results using a modified CE-FAST sequence.  Magn Reson Med. 1989;  9(3) 423-429
• 46 Kaiser R, Bartholdi E, Ernst R R. Diffusion and field-gradient effects in NMR Fourier spectroscopy.  J Chem Phys. 1974;  60 2966-2979
• 47 Wu E X, Buxton R B. Effect of diffusion on the steady-state magnetization with pulsed field gradients.  J Magn Reson. 1990;  90 243-253
• 48 Miller K L, Hargreaves B A, Gold G E, Pauly J M. Steady-state diffusion-weighted imaging of in vivo knee cartilage.  Magn Reson Med. 2004;  51(2) 394-398
• 49 Castillo M, Arbelaez A, Smith J K, Fisher L L. Diffusion-weighted MR imaging offers no advantage over routine noncontrast MR imaging in the detection of vertebral metastases.  AJNR Am J Neuroradiol. 2000;  21(5) 948-953
• 50 Hackländer T, Scharwächter C, Golz R, Mertens H. Value of diffusion-weighted imaging for diagnosing vertebral metastases due to prostate cancer in comparison to other primary tumors.  Rofo. 2006;  178 416-424
• 51 Byun W M, Jang H W, Kim S W, Jang S H, Ahn S H, Ahn M W. Diffusion-weighted magnetic resonance imaging of sacral insufficiency fractures: comparison with metastases of the sacrum.  Spine. 2007;  32(26) E820-E824
• 52 Park S W, Lee J H, Ehara S et al.. Single shot fast spin echo diffusion-weighted MR imaging of the spine: is it useful in differentiating malignant metastatic tumor infiltration from benign fracture edema?.  Clin Imaging. 2004;  28(2) 102-108
• 53 Abanoz R, Hakyemez B, Parlak M. Diffusion-weighted imaging of acute vertebral compression: differential diagnosis of benign versus malignant pathologic fractures.  Tani Girisim Radyol. 2003;  9(2) 176-183
• 54 Baur A, Huber A, Dürr H R et al.. Differentiation of benign osteoporotic and neoplastic vertebral compression fractures with a diffusion-weighted, steady-state free precession sequence.  Rofo. 2002;  174 70-75
• 55 Byun W M, Shin S O, Chang Y, Lee S J, Finsterbusch J, Frahm J. Diffusion-weighted MR imaging of metastatic disease of the spine: assessment of response to therapy.  AJNR Am J Neuroradiol. 2002;  23(6) 906-912
• 56 Yasumoto M, Nonomura Y, Yoshimura R et al.. MR detection of iliac bone marrow involvement by malignant lymphoma with various MR sequences including diffusion-weighted echo-planar imaging.  Skeletal Radiol. 2002;  31(5) 263-269
• 57 Spuentrup E, Buecker A, Adam G, van Vaals J J, Guenther R W. Diffusion-weighted MR imaging for differentiation of benign fracture edema and tumor infiltration of the vertebral body.  AJR Am J Roentgenol. 2001;  176(2) 351-358
• 58 Baur A, Huber A, Ertl-Wagner B et al.. 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. 2001;  22(2) 366-372
• 59 Yeung D K, Wong S Y, Griffith J F, Lau E M. Bone marrow diffusion in osteoporosis: evaluation with quantitative MR diffusion imaging.  J Magn Reson Imaging. 2004;  19(2) 222-228
• 60 Balliu E, Vilanova J C, Peláez I et al.. Diagnostic value of apparent diffusion coefficients to differentiate benign from malignant vertebral bone marrow lesions.  Eur J Radiol. 2008;  , February 12 (Epub ahead of print)
• 61 Gašperšič N, Sersa I, Jevtic V, Tomsic M, Praprotnik S. Monitoring ankylosing spondylitis therapy by dynamic contrast-enhanced and diffusion-weighted magnetic resonance imaging.  Skeletal Radiol. 2008;  37(2) 123-131
• 62 Sugimoto T, Tanigawa N, Ikeda K et al.. Diffusion-weighted imaging for predicting new compression fractures following percutaneous vertebroplasty.  Acta Radiol. 2008;  49(4) 419-426
• 63 Tang G, Liu Y, Li W, Yao J, Li B, Li P. Optimization of b value in diffusion-weighted MRI for the differential diagnosis of benign and malignant vertebral fractures.  Skeletal Radiol. 2007;  36(11) 1035-1041
• 64 Hatipoglu H G, Selvi A, Ciliz D, Yuksel E. Quantitative and diffusion MR imaging as a new method to assess osteoporosis.  AJNR Am J Neuroradiol. 2007;  28(10) 1934-1937
• 65 Raya J G, Dietrich O, Birkenmaier C, Sommer J, Reiser M F, Baur-Melnyk A. Feasibility of a RARE-based sequence for quantitative diffusion-weighted MRI of the spine.  Eur Radiol. 2007;  17(11) 2872-2879
• 66 Oner A Y, Tali T, Celikyay F, Celik A, Le Roux P. Diffusion-weighted imaging of the spine with a non-Carr-Purcell-Meiboom-Gill single-shot fast spin-echo sequence: initial experience.  AJNR Am J Neuroradiol. 2007;  28(3) 575-580
• 67 Griffith J F, Yeung D K, Antonio G E et al.. Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation.  Radiology. 2006;  241(3) 831-838
• 68 Pui M H, Mitha A, Rae W I, Corr P. Diffusion-weighted magnetic resonance imaging of spinal infection and malignancy.  J Neuroimaging. 2005;  15(2) 164-170
• 69 Ballon D, Watts R, Dyke J P et al.. Imaging therapeutic response in human bone marrow using rapid whole-body MRI.  Magn Reson Med. 2004;  52(6) 1234-1238
• 70 Maeda M, Sakuma H, Maier S E, Takeda K. Quantitative assessment of diffusion abnormalities in benign and malignant vertebral compression fractures by line scan diffusion-weighted imaging.  AJR Am J Roentgenol. 2003;  181(5) 1203-1209
• 71 Bammer R, Herneth A M, Maier S E et al.. Line scan diffusion imaging of the spine.  AJNR Am J Neuroradiol. 2003;  24(1) 5-12
• 72 Herneth A M, Philipp M O, Naude J et al.. Vertebral metastases: assessment with apparent diffusion coefficient.  Radiology. 2002;  225(3) 889-894
• 73 Chan J H, Peh W C, Tsui E Y et al.. Acute vertebral body compression fractures: discrimination between benign and malignant causes using apparent diffusion coefficients.  Br J Radiol. 2002;  75(891) 207-214
• 74 Zhou X J, Leeds N E, McKinnon G C, Kumar A J. Characterization of benign and metastatic vertebral compression fractures with quantitative diffusion MR imaging.  AJNR Am J Neuroradiol. 2002;  23(1) 165-170
• 75 Herneth A M, Naude J, Philipp M, Beichel R, Trattnig S, Imhof H. The value of diffusion-weighted MRT in assessing the bone marrow changes in vertebral metastases.  Radiologe. 2000;  40(8) 731-736
• 76 Le Bihan D, Breton E, Lallemand D, Aubin M L, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging.  Radiology. 1988;  168(2) 497-505
• 77 Moon W J, Lee M H, Chung E C. Diffusion-weighted imaging with sensitivity encoding (SENSE) for detecting cranial bone marrow metastases: comparison with T1-weighted images.  Korean J Radiol. 2007;  8(3) 185-191
• 78 Ragin A B, Wu Y, Storey P et al.. Bone marrow diffusion measures correlate with dementia severity in HIV patients.  AJNR Am J Neuroradiol. 2006;  27(3) 589-592
• 79 Nonomura Y, Yasumoto M, Yoshimura R et al.. Relationship between bone marrow cellularity and apparent diffusion coefficient.  J Magn Reson Imaging. 2001;  13(5) 757-760
• 80 Ballon D, Dyke J, Schwartz L H et al.. Bone marrow segmentation in leukemia using diffusion and T (2) weighted echo planar magnetic resonance imaging.  NMR Biomed. 2000;  13(6) 321-328
• 81 Ward R, Caruthers S, Yablon C, Blake M, DiMasi M, Eustace S. Analysis of diffusion changes in posttraumatic bone marrow using navigator-corrected diffusion gradients.  AJR Am J Roentgenol. 2000;  174(3) 731-734
• 82 Mürtz P, Krautmacher C, Träber F, Gieseke J, Schild H H, Willinek W A. Diffusion-weighted whole-body MR imaging with background body signal suppression: a feasibility study at 3.0 Tesla.  Eur Radiol. 2007;  17(12) 3031-3037
• 83 Koh D M, Takahara T, Imai Y, Collins D J. Practical aspects of assessing tumors using clinical diffusion-weighted imaging in the body.  Magn Reson Med Sci. 2007;  6(4) 211-224