Quantitative magnetization transfer measured pool-size ratio reflects optic nerve myelin content in ex vivo mice
Xiawei Ou
Department of Radiology, Vanderbilt University Institute of Imaging Science, Nashville, Tennessee
Arkansas Children's Hospital, University of Arkansas for Medical Sciences, Little Rock, Arkansas
Search for more papers by this authorShu-Wei Sun
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorHsiao-Fang Liang
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorSheng-Kwei Song
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorCorresponding Author
Daniel F. Gochberg
Department of Radiology, Vanderbilt University Institute of Imaging Science, Nashville, Tennessee
Vanderbilt University Institute of Imaging Science, 1161 21st Avenue South, Medical Center North, AA-1105, Nashville, Tennessee 37232-2310===Search for more papers by this authorXiawei Ou
Department of Radiology, Vanderbilt University Institute of Imaging Science, Nashville, Tennessee
Arkansas Children's Hospital, University of Arkansas for Medical Sciences, Little Rock, Arkansas
Search for more papers by this authorShu-Wei Sun
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorHsiao-Fang Liang
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorSheng-Kwei Song
Department of Radiology, Washington University School of Medicine, St. Louis, Missouri
Search for more papers by this authorCorresponding Author
Daniel F. Gochberg
Department of Radiology, Vanderbilt University Institute of Imaging Science, Nashville, Tennessee
Vanderbilt University Institute of Imaging Science, 1161 21st Avenue South, Medical Center North, AA-1105, Nashville, Tennessee 37232-2310===Search for more papers by this authorAbstract
Optic nerves from mice that have undergone retinal ischemia were examined using a newly implemented quantitative magnetization transfer (qMT) technique. Previously published results indicate that the optic nerve from retinal ischemia mice suffered significant axon degeneration without detectable myelin injury at 3 days after reperfusion. At this time point, we acquired ex vivo qMT parameters from both shiverer mice (which have nearly no myelin) and control mice that have undergone retinal ischemia, and these qMT measures were compared with diffusion tensor imaging (DTI) results. Our findings suggests that the qMT estimated ratio of the pool sizes of the macromolecular and free water protons reflected the different myelin contents in the optic nerves between the shiverer and control mice. This pool size ratio was specific to myelin content only and was not significantly affected by the presence of axon injury in mouse optic nerve 3 days after retinal ischemia. Magn Reson Med 61:364–371, 2009. © 2009 Wiley-Liss, Inc.
REFERENCES
- 1 Dousset V, Grossman RI, Ramer KN, Schnall MD, Young LH, Gonzalezscarano F, Lavi E, Cohen JA. Experimental allergic encephalomyelitis and multiple sclerosis—lesion characterization with magnetization transfer imaging. Radiology 1992; 182: 483–491.
- 2 Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G. Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 2001; 56: 304–311.
- 3 Mackay A, Whittall K, Adler J, Li D, Paty D, Graeb D. In-vivo visualization of myelin water in brain by magnetic resonance. Magn Reson Med 1994; 31: 673–677.
- 4 Kim JH, Budde MD, Liang HF, Klein RS, Russell JH, Cross AH, Song SK. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol Dis 2006; 21: 626–632.
- 5 Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002; 17: 1429–1436.
- 6 Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26: 132–140.
- 7 Privat A, Jacque C, Bourre JM, Dupouey P, Baumann N. Absence of the major dense line in myelin of the mutant mouse shiverer. Neurosci Lett 1979; 12: 107–112.
- 8 Ou X, Sun SW, Liang HF, Gochberg DF, Song SK. QMT estimated pool size ratio and DTI derived radial diffusivity reflect the integrity of myelin sheath in mice. Proceedings of the International Society of Magnetic Resonance Medicine, 2007, p 317.
- 9 Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003; 20: 1714–1722.
- 10 Sun SW, Liang HF, Le TQ, Armstrong RC, Cross AH, Song SK. Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. Neuroimage 2006; 32: 1195–1204.
- 11 Wolff SD, Balaban RS. Magnetization transfer contrast (MTC) and tissue water proton relaxation in vivo. Magn Reson Med 1989; 10: 135–144.
- 12 Koenig SH, Brown RD 3rd, Spiller M, Lundbom N. Relaxometry of brain: why white matter appears bright in MRI. Magn Reson Med 1990; 14: 482–495.
- 13 Henkelman RM, Huang XM, Xiang QS, Stanisz GJ, Swanson SD, Bronskill MJ. Quantitative interpretation of magnetization transfer. Magn Reson Med 1993; 29: 759–766.
- 14 Portnoy S, Stanisz GJ. Modeling pulsed magnetization transfer. Magn Reson Med 2007; 58: 144–155.
- 15 Stanisz GJ, Webb S, Munro CA, Pun T, Midha R. MR properties of excised neural tissue following experimentally induced inflammation. Magn Reson Med 2004; 51: 473–479.
- 16 Odrobina EE, Lam TY, Pun T, Midha R, Stanisz GJ. MR properties of excised neural tissue following experimentally induced demyelination. NMR Biomed 2005; 18: 277–284.
- 17 Tozer DJ, Davies GR, Altmann DR, Miller DH, Tofts PS. Correlation of apparent myelin measures obtained in multiple sclerosis patients and controls from magnetization transfer and multicompartmental T-2 analysis. Magn Reson Med 2005; 53: 1415–1422.
- 18 Schmierer K, Scaravilli F, Altmann DR, Barker GJ, Miller DH. Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain. Ann Neurol 2004; 56: 407–415.
- 19 Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, Barker GJ, Tofts PS, Newcombe J, Cuzner ML, Ordidge RJ, McDonald WI, Miller DH. High field MRI correlates of myelin content and axonal density in multiple sclerosis—a post-mortem study of the spinal cord. J Neurol 2003; 250: 1293–1301.
- 20 Blezer EL, Bauer J, Brok HP, Nicolay K, Hart BA. Quantitative MRI-pathology correlations of brain white matter lesions developing in a non-human primate model of multiple sclerosis. NMR Biomed 2007; 20: 90–103.
- 21 Hickman SJ, Toosy AT, Jones SJ, Altmann DR, Miszkiel KA, MacManus DG, Barker GJ, Plant GT, Thompson AJ, Miller DH. Serial magnetization transfer imaging in acute optic neuritis. Brain 2004; 127(Pt 3): 692–700.
- 22 Gochberg DF, Gore JC. Quantitative magnetization transfer imaging via selective inversion recovery with short repetition times. Magn Reson Med 2007; 57(2): 437–441.
- 23 Sled JG, Pike GB. Quantitative interpretation of magnetization transfer in spoiled gradient echo MRI sequences. J Magn Reson 2000; 145: 24–36.
- 24 Edzes HT, Samulski ET. Measurement of cross-relaxation effects in proton NMR spin-lattice relaxation of water in biological systems—hydrated collagen and muscle. J Magn Reson 1978; 31: 207–229.
- 25 Gochberg DF, Gore JC. Quantitative imaging of magnetization transfer using an inversion recovery sequence. Magn Reson Med 2003; 49: 501–505.
- 26 Gochberg DF, Kennan RP, Gore JC. Quantitative studies of magnetization transfer by selective excitation and T-1 recovery. Magn Reson Med 1997; 38: 224–231.
- 27
Gochberg DF,
Kennan RP,
Robson MD,
Gore JC.
Quantitative imaging of magnetization transfer using multiple selective pulses.
Magn Reson Med
1999;
41:
1065–1072.
10.1002/(SICI)1522-2594(199905)41:5<1065::AID-MRM27>3.0.CO;2-9 CAS PubMed Web of Science® Google Scholar
- 28 Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 1996; 111: 209–219.
- 29 Horsfield MA, Jones DK. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review. NMR Biomed 2002; 15: 570–577.
- 30 Miller DH, Grossman RI, Reingold SC, McFarland HF. The role of magnetic resonance techniques in understanding and managing multiple sclerosis. Brain 1998; 121: 3–24.
- 31 Trapp BD, Bo L, Mork S, Chang A. Pathogenesis of tissue injury in MS lesions. J Neuroimmunol 1999; 98: 49–56.
- 32 Sun SW, Neil JJ, Song SK. Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med 2003; 50: 743–748.
- 33 Henkelman RM, Stanisz GJ, Kim JK, Bronskill MJ. Anisotropy of NMR properties of tissues. Magn Reson Med 1994; 32: 592–601.
- 34 Sun SW, Neil JJ, Liang HF, He YY, Schmidt RE, Hsu CY, Song SK. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn Reson Med 2005; 53: 1447–1451.
- 35 Sled JG, Levesque I, Santos AC, Francis SJ, Narayanan S, Brass SD, Arnold DL, Pike GB. Regional variations in normal brain shown by quantitative magnetization transfer imaging. Magn Reson Med 2004; 51: 299–303.
- 36 Yarnykh VL, Yuan C. Cross-relaxation imaging reveals detailed anatomy of white matter fiber tracts in the human brain. Neuroimage 2004; 23: 409–424.
- 37 Narayanan S, Francis SJ, Sled JG, Santos AC, Antel S, Levesque I, Brass S, Lapierre Y, Sappey-Marinier D, Pike GB, Arnold DL. Axonal injury in the cerebral normal-appearing white matter of patients with multiple sclerosis is related to concurrent demyelination in lesions but not to concurrent demyelination in normal-appearing white matter. Neuroimage 2006; 29: 637–642.
- 38 Beaulieu C, Allen PS. Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn Reson Med 1994; 32: 579–583.
- 39 Stanisz GJ, Henkelman RM. Diffusional anisotropy of T2 components in bovine optic nerve. Magn Reson Med 1998; 40: 405–410.
- 40
Peled S,
Cory DG,
Raymond SA,
Kirschner DA,
Jolesz FA.
Water diffusion, T(2), and compartmentation in frog sciatic nerve.
Magn Reson Med
1999;
42:
911–918.
10.1002/(SICI)1522-2594(199911)42:5<911::AID-MRM11>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- 41 Andrews TJ, Osborne MT, Does MD. Diffusion of myelin water. Magn Reson Med 2006; 56: 381–385.
- 42 Koenig SH. Cholesterol of myelin is the determinant of gray-white contrast in MRI of brain. Magn Reson Med 1991; 20: 285–291.
- 43
Stanisz GJ,
Kecojevic A,
Bronskill MJ,
Henkelman RM.
Characterizing white matter with magnetization transfer and T-2.
Magn Reson Med
1999;
42:
1128–1136.
10.1002/(SICI)1522-2594(199912)42:6<1128::AID-MRM18>3.0.CO;2-9 CAS PubMed Web of Science® Google Scholar
- 44 Bjarnason TA, Vavasour IM, Chia CL, MacKay AL. Characterization of the NMR behavior of white matter in bovine brain. Magn Reson Med 2005; 54: 1072–1081.