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    Original Research

    Quantitative Measurement of Brain Perfusion with Intravoxel Incoherent Motion MR Imaging

    Published Online:Dec 1 2012https://doi.org/10.1148/radiol.12120584

    Abstract

    The results of this study validate the use of intravoxel incoherent motion MR imaging to measure perfusion in the human brain and demonstrate that perfusion fraction, pseudodiffusion coefficient, and blood flow–related perfusion fraction change gradually under hypercapnia and hyperoxygenation in the full brain and in smaller regions of interest.

    Purpose

    To evaluate the sensitivity of the perfusion parameters derived from Intravoxel Incoherent Motion (IVIM) MR imaging to hypercapnia-induced vasodilatation and hyperoxygenation-induced vasoconstriction in the human brain.

    Materials and Methods

    This study was approved by the local ethics committee and informed consent was obtained from all participants. Images were acquired with a standard pulsed-gradient spin-echo sequence (Stejskal-Tanner) in a clinical 3-T system by using 16 b values ranging from 0 to 900 sec/mm2. Seven healthy volunteers were examined while they inhaled four different gas mixtures known to modify brain perfusion (pure oxygen, ambient air, 5% CO2 in ambient air, and 8% CO2 in ambient air). Diffusion coefficient (D), pseudodiffusion coefficient (D*), perfusion fraction (f), and blood flow–related parameter (fD*) maps were calculated on the basis of the IVIM biexponential model, and the parametric maps were compared among the four different gas mixtures. Paired, one-tailed Student t tests were performed to assess for statistically significant differences.

    Results

    Signal decay curves were biexponential in the brain parenchyma of all volunteers. When compared with inhaled ambient air, the IVIM perfusion parameters D*, f, and fD* increased as the concentration of inhaled CO2 was increased (for the entire brain, P = .01 for f, D*, and fD* for CO2 5%; P = .02 for f, and P = .01 for D* and fD* for CO2 8%), and a trend toward a reduction was observed when participants inhaled pure oxygen (although P > .05). D remained globally stable.

    Conclusion

    The IVIM perfusion parameters were reactive to hyperoxygenation-induced vasoconstriction and hypercapnia-induced vasodilatation. Accordingly, IVIM imaging was found to be a valid and promising method to quantify brain perfusion in humans.

    © RSNA, 2012

    References

    • 1 Krogh A. The anatomy and physiology of capillaries. New Haven, Conn: Yale University Press, 1922. Google Scholar
    • 2 Kety SS, Schmidt CF. The nitrous oxide method for the quantitative determination of cerebral blood flow in man: theory, procedure and normal values. J Clin Invest 1948;27(4):476–483. Crossref, Medline, Google Scholar
    • 3 Villringer A, Rosen BR, Belliveau JWet al.. Dynamic imaging with lanthanide chelates in normal brain: contrast due to magnetic susceptibility effects. Magn Reson Med 1988;6(2):164–174. Crossref, Medline, Google Scholar
    • 4 Dixon WT, Du LN, Faul DD, Gado M, Rossnick S. Projection angiograms of blood labeled by adiabatic fast passage. Magn Reson Med 1986;3(3):454–462. Crossref, Medline, Google Scholar
    • 5 Calamante F, Gadian DG, Connelly A. Quantification of perfusion using bolus tracking magnetic resonance imaging in stroke: assumptions, limitations, and potential implications for clinical use. Stroke 2002;33(4):1146–1151. Crossref, Medline, Google Scholar
    • 6 Knutsson L, Ståhlberg F, Wirestam R. Absolute quantification of perfusion using dynamic susceptibility contrast MRI: pitfalls and possibilities. MAGMA 2010;23(1):1–21. Crossref, Medline, Google Scholar
    • 7 Petersen ET, Zimine I, Ho YC, Golay X. Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 2006;79(944):688–701. Crossref, Medline, Google Scholar
    • 8 Paulson ES, Schmainda KM. Comparison of dynamic susceptibility-weighted contrast-enhanced MR methods: recommendations for measuring relative cerebral blood volume in brain tumors. Radiology 2008;249(2):601–613. Link, Google Scholar
    • 9 Le Bihan D. Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology 2008;249(3):748–752. Link, Google Scholar
    • 10 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. Link, Google Scholar
    • 11 Maier SE, Sun Y, Mulkern RV. Diffusion imaging of brain tumors. NMR Biomed 2010;23(7):849–864. Crossref, Medline, Google Scholar
    • 12 Mikulis DJ, Roberts TP. Neuro MR: protocols. J Magn Reson Imaging 2007;26(4):838–847. Crossref, Medline, Google Scholar
    • 13 Roberts TP, Mikulis D. Neuro MR: principles. J Magn Reson Imaging 2007;26(4):823–837. Crossref, Medline, Google Scholar
    • 14 Schellinger PD, Jansen O, Fiebach JBet al.. Feasibility and practicality of MR imaging of stroke in the management of hyperacute cerebral ischemia. AJNR Am J Neuroradiol 2000;21(7):1184–1189. Medline, Google Scholar
    • 15 Hagmann P, Kurant M, Gigandet Xet al.. Mapping human whole-brain structural networks with diffusion MRI. PLoS ONE 2007;2(7):e597. Crossref, Medline, Google Scholar
    • 16 Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T. MR tractography: a review of its clinical applications. Magn Reson Med Sci 2009;8(4):165–174. Crossref, Medline, Google Scholar
    • 17 Bammer R, Holdsworth SJ, Veldhuis WB, Skare ST. New methods in diffusion-weighted and diffusion tensor imaging. Magn Reson Imaging Clin N Am 2009;17(2):175–204. Crossref, Medline, Google Scholar
    • 18 Pekar J, Moonen CT, van Zijl PC. On the precision of diffusion/perfusion imaging by gradient sensitization. Magn Reson Med 1992;23(1):122–129. Crossref, Medline, Google Scholar
    • 19 Ito H, Kanno I, Iida Het al.. Arterial fraction of cerebral blood volume in humans measured by positron emission tomography. Ann Nucl Med 2001;15(2):111–116. Crossref, Medline, Google Scholar
    • 20 Kim T, Kim SG. Quantification of cerebral arterial blood volume and cerebral blood flow using MRI with modulation of tissue and vessel (MOTIVE) signals. Magn Reson Med 2005;54(2):333–342. Crossref, Medline, Google Scholar
    • 21 Koh DM, Collins DJ, Orton MR. Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges. AJR Am J Roentgenol 2011;196(6):1351–1361. Crossref, Medline, Google Scholar
    • 22 Luciani A, Vignaud A, Cavet Met al.. Liver cirrhosis: intravoxel incoherent motion MR imaging—pilot study. Radiology 2008;249(3):891–899. Link, Google Scholar
    • 23 Callot V, Bennett E, Decking UK, Balaban RS, Wen H. In vivo study of microcirculation in canine myocardium using the IVIM method. Magn Reson Med 2003;50(3):531–540. Crossref, Medline, Google Scholar
    • 24 Lemke A, Laun FB, Klauss Met al.. Differentiation of pancreas carcinoma from healthy pancreatic tissue using multiple b-values: comparison of apparent diffusion coefficient and intravoxel incoherent motion derived parameters. Invest Radiol 2009;44(12):769–775. Crossref, Medline, Google Scholar
    • 25 Sigmund EE, Cho GY, Kim Set al.. Intravoxel incoherent motion imaging of tumor microenvironment in locally advanced breast cancer. Magn Reson Med 2011;65(5):1437–1447. Crossref, Medline, Google Scholar
    • 26 Thoeny HC, Binser T, Roth B, Kessler TM, Vermathen P. Noninvasive assessment of acute ureteral obstruction with diffusion-weighted MR imaging: a prospective study. Radiology 2009;252(3):721–728. Link, Google Scholar
    • 27 Karampinos DC, King KF, Sutton BP, Georgiadis JG. Intravoxel partially coherent motion technique: characterization of the anisotropy of skeletal muscle microvasculature. J Magn Reson Imaging 2010;31(4):942–953. Crossref, Medline, Google Scholar
    • 28 Riches SF, Hawtin K, Charles-Edwards EM, de Souza NM. Diffusion-weighted imaging of the prostate and rectal wall: comparison of biexponential and monoexponential modelled diffusion and associated perfusion coefficients. NMR Biomed 2009;22(3):318–325. Crossref, Medline, Google Scholar
    • 29 Henkelman RM, Neil JJ, Xiang QS. A quantitative interpretation of IVIM measurements of vascular perfusion in the rat brain. Magn Reson Med 1994;32(4):464–469. Crossref, Medline, Google Scholar
    • 30 Le Bihan D, Moonen CT, van Zijl PC, Pekar J, DesPres D. Measuring random microscopic motion of water in tissues with MR imaging: a cat brain study. J Comput Assist Tomogr 1991;15(1):19–25. Crossref, Medline, Google Scholar
    • 31 Neil JJ, Bosch CS, Ackerman JJ. An evaluation of the sensitivity of the intravoxel incoherent motion (IVIM) method of blood flow measurement to changes in cerebral blood flow. Magn Reson Med 1994;32(1):60–65. Crossref, Medline, Google Scholar
    • 32 Chenevert TL, Pipe JG, Williams DM, Brunberg JA. Quantitative measurement of tissue perfusion and diffusion in vivo. Magn Reson Med 1991;17(1):197–212. Crossref, Medline, Google Scholar
    • 33 Turner R, Le Bihan D, Maier J, Vavrek R, Hedges LK, Pekar J. Echo-planar imaging of intravoxel incoherent motion. Radiology 1990;177(2):407–414. Link, Google Scholar
    • 34 Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 1988;168(2):497–505. Link, Google Scholar
    • 35 Wirestam R, Brockstedt S, Lindgren Aet al.. The perfusion fraction in volunteers and in patients with ischaemic stroke. Acta Radiol 1997;38(6):961–964. Crossref, Medline, Google Scholar
    • 36 Song AW, Fichtenholtz H, Woldorff M. BOLD signal compartmentalization based on the apparent diffusion coefficient. Magn Reson Imaging 2002;20(7):521–525. Crossref, Medline, Google Scholar
    • 37 Kim T, Kim SG. Quantification of cerebral arterial blood volume using arterial spin labeling with intravoxel incoherent motion-sensitive gradients. Magn Reson Med 2006;55(5):1047–1057. Crossref, Medline, Google Scholar
    • 38 Stejskal EO, Tanner JE. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 1965;42(1):288–292. Crossref, Google Scholar
    • 39 Kety SS, Schmidt CF. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J Clin Invest 1948;27(4):484–492. Crossref, Medline, Google Scholar
    • 40 Parker SM, Gibson GJ. Evaluation of a transcutaneous carbon dioxide monitor (“TOSCA”) in adult patients in routine respiratory practice. Respir Med 2007;101(2):261–264. Crossref, Medline, Google Scholar
    • 41 Smith SM, Jenkinson M, Woolrich MWet al.. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004;23(Suppl 1):S208–S219. Crossref, Medline, Google Scholar
    • 42 Seber GA, Wild CJ. Nonlinear regression. Hoboken, NJ: Wiley-Interscience, 2003. Google Scholar
    • 43 Le Bihan D, Turner R, MacFall JR. Effects of intravoxel incoherent motions (IVIM) in steady-state free precession (SSFP) imaging: application to diffusion imaging. Magn Reson Med 1989;10(3):324-337. Crossref, Medline, Google Scholar
    • 44 Piechnik SK, Evans J, Bary LH, Wise RG, Jezzard P. Functional changes in CSF volume estimated using measurement of water T2 relaxation. Magn Reson Med 2009;61(3):579–586. Crossref, Medline, Google Scholar
    • 45 Jin T, Kim SG. Change of the cerebrospinal fluid volume during brain activation investigated by T(1rho)-weighted fMRI. Neuroimage 2010;51(4):1378–1383. Crossref, Medline, Google Scholar
    • 46 Ho YC, Petersen ET, Zimine I, Golay X. Similarities and differences in arterial responses to hypercapnia and visual stimulation. J Cereb Blood Flow Metab 2011;31(2):560–571. Crossref, Medline, Google Scholar
    • 47 Hutchinson EB, Stefanovic B, Koretsky AP, Silva AC. Spatial flow-volume dissociation of the cerebral microcirculatory response to mild hypercapnia. Neuroimage 2006;32(2):520–530. Crossref, Medline, Google Scholar
    • 48 Ito H, Kanno I, Fukuda H. Human cerebral circulation: positron emission tomography studies. Ann Nucl Med 2005;19(2):65–74. Crossref, Medline, Google Scholar
    • 49 Leontiev O, Buxton RB. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 2007;35(1):175–184. Crossref, Medline, Google Scholar
    • 50 Piechnik SK, Chiarelli PA, Jezzard P. Modelling vascular reactivity to investigate the basis of the relationship between cerebral blood volume and flow under CO2 manipulation. Neuroimage 2008;39(1):107–118. Crossref, Medline, Google Scholar
    • 51 Le Bihan D, Turner R. The capillary network: a link between IVIM and classical perfusion. Magn Reson Med 1992;27(1):171–178. Crossref, Medline, Google Scholar

    Article History

    Received March 10, 2012; revision requested May 8; revision received May 24; accepted June 6; final version accepted June 18.
    Published online: Dec 2012
    Published in print: Dec 2012