Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue
Open accessAbstract
Chemically‐fixed nervous tissues are well‐suited for high‐resolution, time‐intensive MRI acquisitions without motion artifacts, such as those required for brain atlas projects, but the aldehyde fixatives used may significantly alter tissue MRI properties. To test this hypothesis, this study characterized the impact of common aldehyde fixatives on the MRI properties of a rat brain slice model. Rat cortical slices immersion‐fixed in 4% formaldehyde demonstrated 21% and 81% reductions in tissue T 1 and T 2 , respectively ( P < 0.001). The T 2 reduction was reversed by washing slices with phosphate‐buffered saline (PBS) for 12 h to remove free formaldehyde solution. Diffusion MRI of cortical slices analyzed with a two‐compartment analytical model of water diffusion demonstrated 88% and 30% increases in extracellular apparent diffusion coefficient (ADC EX ) and apparent restriction size, respectively, when slices were chemically‐fixed with 4% formaldehyde ( P ≤ 0.021). Further, fixation with 4% formaldehyde increased the transmembrane water exchange rate 239% ( P < 0.001), indicating increased membrane permeability. Karnovsky's and 4% glutaraldehyde fixative solutions also changed the MRI properties of cortical slices, but significant differences were noted between the different fixative treatments ( P < 0.05). The observed water relaxation and diffusion changes help better define the validity and limitations of using chemically‐fixed nervous tissue for MRI investigations. Magn Reson Med, 2009. © 2009 Wiley‐Liss, Inc.
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Fixation can alter tissue microstructure.
“Fixation can alter tissue microstructure47, 48; therefore, NODDI metrics as shown here may not be fully representative of their in vivo counterparts.”
From Neurite dispersion: a new marker of multiple sclerosis spinal cord pathology? (2017) · cites this paper as [47]
MR relaxation relies on water protons behaving differently depending on their molecular environment, and fixation does change this environment, for example by affecting membrane permeability.
“Moreover, MR relaxation relies on water protons behaving differently depending on their molecular environment, and fixation does change this environment, for example by affecting membrane permeability (Shepherd et al., 2009).”
From Can MRI measure myelin? Systematic review, qualitative assessment, and meta-analysis of studies validating microstructural imaging with myelin histology (2021) · cites this paper as Shepherd et al., 2009
Diffusion-weighted signals are affected by the effects of fixation on water diffusion.
“The same principle applies to diffusion-weighted signals, which are affected by the effects of fixation on water diffusion (Shepherd, Thelwall, Stanisz, Blackband, 2009, Sun, Neil, Liang, He, Schmidt, Hsu, Song, 2005).”
From Can MRI measure myelin? Systematic review, qualitative assessment, and meta-analysis of studies validating microstructural imaging with myelin histology (2021) · cites this paper as Shepherd, Thelwall, Stanisz, Blackband, 2009
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Cites
A formaldehyde - glutaraldehyde fixative of high osmolarity for use in electron microscopy
Karnovsky, M. J. (1965) · The Journal of Cell Biology · Cited by 5,882 · see citing works
The basis of anisotropic water diffusion in the nervous system—A technical review.
Beaulieu, C. (2002) · NMR in Biomedicine · doi:10.1002/nbm.782 · Cited by 4,653 · see citing works
Histological and Histochemical Methods - Theory and practice
Malatesta, M. (2016) · European Journal of Histochemistry · doi:10.4081/ejh.2016.2639 · Cited by 1,182 · see citing works
Fixation for Electron Microscopy
(1981) · Elsevier eBooks · doi:10.1016/b978-0-12-333920-1.x5001-0 · Cited by 597 · see citing works
An analytical model of restricted diffusion in bovine optic nerve
Stanisz, G. J., Wright, G. A., Henkelman, R. M., & Szafer, A. (1997) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910370115 · Cited by 501 · see citing works
Self-citationMa, Y., Hof, P. R., Grant, S. C., Blackband, S. J., Bennett, R., Slatest, L. A., McGuigan, M., & Benveniste, H. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.014 · Cited by 441 · see citing works
Self-citationPressure and temperature dependence of the self diffusion coefficient of water and oxygen-18 water
Harris, K. R., & Woolf, L. A. (1980) · Journal of the Chemical Society Faraday Transactions 1 Physical Chemistry in Condensed Phases · doi:10.1039/f19807600377 · Cited by 273 · see citing works
Sun, S., Neil, J. J., & Song, S. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10605 · Cited by 231 · see citing works
Fixation for Scanning Electron Microscopy
Hayat, M. A. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-333920-1.50017-3 · Cited by 200 · see citing works
Postmortem MR imaging of formalin-fixed human brain
Pfefferbaum, A., Sullivan, E. V., Elfar Adalsteinsson, A., Garrick, T. M., & Harper, C. G. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.024 · Cited by 199 · see citing works
An approach to high resolution diffusion tensor imaging in fixed primate brain
D'Arceuil, H. E., Westmoreland, S. V., & de Crespigny, A. J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.12.028 · Cited by 195 · see citing works
The effects of brain tissue decomposition on diffusion tensor imaging and tractography
D'Arceuil, H. E., & de Crespigny, A. J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.02.039 · Cited by 185 · see citing works
High-throughput morphologic phenotyping of the mouse brain with magnetic resonance histology
Johnson, G. A., Ali-Sharief, A., Badea, A., Brandenburg, J., Cofer, G. P., Fubara, B. N., Gewalt, S. L., Hedlund, L. W., & Upchurch, L. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.013 · Cited by 121 · see citing works
Measurements of T1 and T2 over time in formalin-fixed human whole-brain specimens
Tovi, M., & Ericsson, A. B. (1992) · Acta Radiologica · doi:10.1080/02841859209172021 · Cited by 120 · see citing works
Thelwall, P. E., Shepherd, T. M., Stanisz, G. J., & Blackband, S. J. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20962 · Cited by 113 · see citing works
Self-citationMaking the best of brain slices; comparing preparative methods
Lipton, P., Aitken, P. G., Dudek, F. E., Eskessen, K., Espanol, M. T., Ferchmin, P. A., Kelly, J., Kreisman, N. R., Landfield, P. W., Larkman, P. M., et al. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)00205-u · Cited by 112 · see citing works
Diffusion tensor imaging in fixed brain tissue at 7.0 T
Guilfoyle, D. N., Helpern, J. A., & Lim, K. O. (2003) · NMR in Biomedicine · doi:10.1002/nbm.814 · Cited by 103 · see citing works
Nuclear magnetic resonance characteristics of fresh and fixed tissue: the effect of elapsed time.
Thickman, D., Kundel, H. L., & Wolf, G. L. (1983) · Radiology · doi:10.1148/radiology.148.1.6856832 · Cited by 103 · see citing works
Yong-Hing, C. J., Obenaus, A., Stryker, R., Tong, K. A., & Sarty, G. E. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20578 · Cited by 102 · see citing works
Madi, S., Hasan, K. M., & Narayana, P. A. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20304 · Cited by 95 · see citing works
Measurements of T1 and T2 over Time in Formalin-Fixed Human Whole-Brain Specimens
Tovi, M., & Ericsson, A. B. (1992) · Acta Radiologica · doi:10.1177/028418519203300503 · Cited by 91 · see citing works
Preservation of extracellular space during fixation of the brain for electron microscopy
Cragg, B. G. (1980) · Tissue and Cell · doi:10.1016/0040-8166(80)90052-x · Cited by 82 · see citing works
Formalin fixed brains are useful for magnetic resonance imaging (MRI) study
Nagara, H., Inoue, T., Koga, T., Kitaguchi, T., Tateishi, J., & Goto, I. (1987) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(87)90184-5 · Cited by 75 · see citing works
Optimising Imaging Parameters for Post Mortem MR Imaging of the Human Brain
Blamire, A. M., Rowe, J., Styles, P., & McDonald, B. (1999) · Acta Radiologica · doi:10.3109/02841859909175593 · Cited by 70 · see citing works
Ex vivo evaluation of ADC values within spinal cord white matter tracts.
Schwartz, E. D., Cooper, E. T., Chin, C., Wehrli, S. L., Tessler, A. R., & Hackney, D. B. (2005) · PubMed Central · Cited by 69 · see citing works
Thelwall, P. E., Grant, S. C., Stanisz, G. J., & Blackband, S. J. (2002) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10270 · Cited by 67 · see citing works
Self-citationDiffusion MR in Biological Systems: Tissue Compartments and Exchange
Stanisz, G. J. (2003) · Israel Journal of Chemistry · doi:10.1560/e0wu-7ffh-31m6-vlyt · Cited by 62 · see citing works
Self-citationHarreveld, A. V., & Khattab, F. I. (1968) · Journal of Cell Science · doi:10.1242/jcs.3.4.579 · Cited by 62 · see citing works
Pattany, P. M., Puckett, W., Klose, K. J., Quencer, R. M., Bunge, R. P., Kasuboski, L., & Weaver, R. G. (1997) · PubMed Central · Cited by 62 · see citing works
Changes of relaxation times T1 and T2 in rat tissues after biopsy and fixation
Kamman, R. L., Go, K. G., Stomp, G. P., Hulstaert, C. E., & Berendsen, H. J. C. (1985) · Magnetic Resonance Imaging · doi:10.1016/0730-725x(85)90353-4 · Cited by 61 · see citing works
Integrated analysis of diffusion and relaxation of water in blood
Li, J. G., Stanisz, G. J., & Henkelman, R. M. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910400112 · Cited by 49 · see citing works
Self-citationReversible and irreversible effects of chemical fixation on the NMR properties of single cells
Purea, A., & WEBB, A. G. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21018 · Cited by 45 · see citing works
Preservation of hippocampal brain slices with in vivo or in vitro hypothermia
Newman, G. C., Qi, H., Hospod, F. E., & Grundmann, K. (1992) · Brain Research · doi:10.1016/0006-8993(92)90438-f · Cited by 40 · see citing works
Standard atlas space for C57BL/6J neonatal mouse brain
Lee, E., Jacobs, R. E., Dinov, I. D., Leow, A., & Toga, A. W. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0048-y · Cited by 37 · see citing works
Translational neuroscience and magnetic-resonance microscopy
Benveniste, H., & Blackband, S. J. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(06)70472-0 · Cited by 36 · see citing works
Self-citationWater diffusion measurements in perfused human hippocampal slices undergoing tonicity changes
Shepherd, T. M., Wirth, E. D., Thelwall, P. E., Chen, H., Roper, S. N., & Blackband, S. J. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10456 · Cited by 28 · see citing works
Self-citationSimultaneous diffusion MRI measurements from multiple perfused rat hippocampal slices
Shepherd, T. M., Blackband, S. J., & Wirth, E. D. (2002) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10241 · Cited by 18 · see citing works
Self-citationPostmortem Change in the Rat: A Histologic Characterization
Seaman, W. (1987) · Cited by 14 · see citing works
Connors, B. W., & Gutnick, M. J. (1984) · Springer eBooks · doi:10.1007/978-1-4684-4583-1_13 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [19]Shepherd TM Flint J Thelwall PE Stanisz GJ Blackband SJ Postmortem interval alters the water relaxation and diffusion properties of nervous tissue—implications for high resolution MRI of human autopsy samples Proceedings of the 14th Annual Meeting of ISMRM Seattle, WA, USA 2006 Abstract 139
- [22]Conners Gluck Neocortex: cellular properties and intrinsic circuitry Dingledine R Brain slices New York Plenum Press 1984 313 340
- [33]Shepherd TM Thelwall PE Stanisz GJ Blackband SJ Analytical model of water diffusion in isocortex slices Proceedings of the 12th Annual Meeting of ISMRM Kyoto, Japan 2004 Abstract 1229
- [35]Bossart EL Inglis BA Silver XS Mareci TH The effect of fixative solutions in magnetic resonance imaging Proceedings of the 7th Annual Meeting of ISMRM Philadelphia, PA, USA 1999 Abstract 1928
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Panagiotaki, E., Schneider, T., Siow, B., Hall, M. G., Lythgoe, M. F., & Alexander, D. C. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.081 · Cited by 422 · see citing works
Novikov, D. S., Kiselev, V. G., & Jespersen, S. N. (2018) · Magnetic Resonance in Medicine · doi:10.1002/mrm.27101 · Cited by 362 · see citing works
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Schmidt, R., Schmidt, H., Haybaeck, J., Loitfelder, M., Weis, S., Cavalieri, M., Seiler, S., Enzinger, C., Ropele, S., Erkinjuntti, T., et al. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0851-x · Cited by 327 · see citing works
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Grussu, F., Schneider, T., Tur, C., Yates, R. L., Tachrount, M., Ianuş, A., Yiannakas, M. C., Newcombe, J., Zhang, H., Alexander, D. C., et al. (2017) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.445 · Cited by 291 · see citing works
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Miller, K. L., Stagg, C. J., Douaud, G., Jbabdi, S., Smith, S. M., Behrens, T. E. J., Jenkinson, M., Chance, S. A., Esiri, M. M., Voets, N., et al. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.03.070 · Cited by 273 · see citing works
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Lee, J., Shmueli, K., Fukunaga, M., van Gelderen, P., Merkle, H., Silva, A. C., & Duyn, J. H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910222107 · Cited by 264 · see citing works
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Keren, N. I., Taheri, S., Vazey, E. M., Morgan, P. S., Granholm, A., Aston‐Jones, G., & Eckert, M. A. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.03.020 · Cited by 227 · see citing works
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Pichat, J., Iglesias, J. E., Yousry, T., Ourselin, S., & Modat, M. (2018) · Medical Image Analysis · doi:10.1016/j.media.2018.02.004 · Cited by 207 · see citing works
Lee, J., Shmueli, K., Kang, B., Yao, B., Fukunaga, M., van Gelderen, P., Palumbo, S., Bosetti, F., Silva, A. C., & Duyn, J. H. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.076 · Cited by 205 · see citing works
Jones, D. K., Alexander, D. C., Bowtell, R. W., Cercignani, M., Dell’Acqua, F., McHugh, D. J., Miller, K. L., Palombo, M., Parker, G. J. M., Rudrapatna, U. S., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.047 · Cited by 179 · see citing works
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Dula, A. N., Gochberg, D. F., Valentine, H. L., Valentine, W. M., & Does, M. D. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22267 · Cited by 148 · see citing works
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Pop, M., Ghugre, N. R., Ramanan, V., Morikawa, L., Stanisz, G. J., DICK, A. J., & Wright, G. A. (2013) · Physics in Medicine and Biology · doi:10.1088/0031-9155/58/15/5009 · Cited by 93 · see citing works
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Zhang, J., Jones, M. V., McMahon, M. T., Mori, S., & Calabresi, P. A. (2012) · Magnetic Resonance in Medicine · doi:10.1002/mrm.23032 · Cited by 88 · see citing works
Coras, R., Milesi, G., Zucca, I., Mastropietro, A., Scotti, A., Figini, M., Mühlebner, A., Heß, A., Graf, W., Tringali, G., et al. (2014) · Epilepsia · doi:10.1111/epi.12828 · Cited by 87 · see citing works
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Layer-specific diffusion weighted imaging in human primary visual cortex in vitro
Kleinnijenhuis, M., Zerbi, V., Küsters, B., Slump, C. H., Barth, M., & van Cappellen van Walsum, A.-M. (2013) · Cortex · doi:10.1016/j.cortex.2012.11.015 · Cited by 71 · see citing works
Berquist, R. M., Gledhill, K. M., Peterson, M. W., Doan, A. H., Baxter, G. T., Yopak, K. E., Kang, N., Walker, H. J., Hastings, P. A., & Frank, L. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034499 · Cited by 69 · see citing works
Portnoy, S., Flint, J. J., Blackband, S. J., & Stanisz, G. J. (2012) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24325 · Cited by 66 · see citing works
Self-citationNguyen, C. T., Fan, Z., Xie, Y., Dawkins, J. F., Tseliou, E., Bi, X., Sharif, B., Dharmakumar, R., Marbán, E., & Li, D. (2014) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/s12968-014-0068-y · Cited by 67 · see citing works
Origins of R 2 ∗ orientation dependence in gray and white matter
Rudko, D. A., Klassen, L. M., de Chickera, S. N., Gati, J. S., Dekaban, G. A., & Menon, R. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306516111 · Cited by 65 · see citing works
Anderson, S. W., Barry, B., Soto, J. A., Ozonoff, A., O’Brien, M. J., & Jara, H. J. (2013) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.24234 · Cited by 65 · see citing works
Postmortem T 2 * - Weighted MRI Imaging of Cortical Iron Reflects Severity of Alzheimer’s Disease
Bulk, M., Kenkhuis, B., van der Graaf, L. M., Goeman, J. J., Natté, R., & van der Weerd, L. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180317 · Cited by 64 · see citing works
Williamson, N. H., Ravin, R., Benjamini, D., Merkle, H., Falgairolle, M., O'Donovan, M. J., Blivis, D., Ide, D., Cai, T. X., Ghorashi, N. S., et al. (2019) · eLife · doi:10.7554/elife.51101 · Cited by 62 · see citing works
An open resource combining multi-contrast MRI and microscopy in the macaque brain
Howard, A. F. D., Huszár, I. N., Smart, A., Cottaar, M., Daubney, G., Hanayik, T., Khrapitchev, A. A., Mars, R. B., Mollink, J., Scott, C., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39916-1 · Cited by 62 · see citing works
Quantifying liver fibrosis through the application of texture analysis to diffusion weighted imaging
Barry, B., Buch, K. A., Soto, J. A., Jara, H. J., Nakhmani, A., & Anderson, S. W. (2013) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2013.04.006 · Cited by 62 · see citing works
Tissue magnetic susceptibility mapping as a marker of tau pathology in Alzheimer's disease
O’Callaghan, J. M., Holmes, H. E., Powell, N. M., Wells, J. A., Ismail, O., Harrison, I. F., Siow, B. M., Johnson, R. A., Ahmed, Z., Fisher, A., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.08.003 · Cited by 61 · see citing works
Merisaari, H., & Jambor, I. (2014) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25310 · Cited by 57 · see citing works
Mollink, J., van Baarsen, K. M., Dederen, P. J. W. C., Foxley, S., Miller, K. L., Jbabdi, S., Slump, C. H., Grotenhuis, J. A., Kleinnijenhuis, M., & van Walsum, A. M. V. C. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1115-7 · Cited by 56 · see citing works
Holmes, H. E., Powell, N. M., Ma, D., Ismail, O., Harrison, I. F., Wells, J. A., Colgan, N., O'Callaghan, J. M., Johnson, R. A., Murray, T. K., et al. (2017) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2017.00020 · Cited by 55 · see citing works
The Digital Brain Bank, an open access platform for post-mortem imaging datasets
Tendler, B. C., Hanayik, T., Ansorge, O., Bangerter-Christensen, S., Berns, G. S., Bertelsen, M. F., Bryant, K., Foxley, S., van den Heuvel, M. P., Howard, A. F. D., et al. (2022) · eLife · doi:10.7554/elife.73153 · Cited by 57 · see citing works
Flint, J. J., Hansen, B., Fey, M., Schmidig, D., King, M. A., Vestergaard‐Poulsen, P., & Blackband, S. J. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.031 · Cited by 52 · see citing works
Self-citationBrunet, J., Walsh, C., Wagner, W. L., Bellier, A., Werlein, C., Marussi, S., Jonigk, D. D., Verleden, S. E., Ackermann, M., Lee, P. D., et al. (2023) · Nature Protocols · doi:10.1038/s41596-023-00804-z · Cited by 51 · see citing works
Imaging White Matter in Human Brainstem
Ford, A. A., Colón-Pérez, L. M., Triplett, W. T., Gullett, J. M., Mareci, T. H., & FitzGerald, D. B. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00400 · Cited by 51 · see citing works
Jonkman, L. E., Graaf, Y. G.-D., Bulk, M., Kaai, E., Pouwels, P. J. W., Barkhof, F., Rozemüller, A. J. M., van der Weerd, L., Geurts, J. J. G., & van de Berg, W. D. J. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101698 · Cited by 44 · see citing works
Vestergaard‐Poulsen, P., Wegener, G., Hansen, B., Bjarkam, C. R., Blackband, S. J., Nielsen, N. C., & Jespersen, S. N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020653 · Cited by 51 · see citing works
Self-citationMRI artifacts in human brain tissue after prolonged formalin storage
van Duijn, S., Nabuurs, R. J. A., van Rooden, S., Maat‐Schieman, M. L. C., van Duinen, S. G., van Buchem, M. A., van der Weerd, L., & Natté, R. (2011) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22758 · Cited by 53 · see citing works
Velumian, A. A., Samoilova, M., & Fehlings, M. G. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.11.022 · Cited by 49 · see citing works
The present and the future of microstructure MRI: From a paradigm shift to normal science
Novikov, D. S. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108947 · Cited by 45 · see citing works
Wu, D., & Zhang, J. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.10.051 · Cited by 47 · see citing works
Fan, Q., Nummenmaa, A. R., Wichtmann, B. D., Witzel, T., Mekkaoui, C., Schneider, W., Wald, L. L., & Huang, S. Y. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.01.004 · Cited by 48 · see citing works
Quantitative Magnetic Resonance Imaging of Cortical Multiple Sclerosis Pathology
Tardif, C., Bedell, B. J., Eskildsen, S., Collins, D. L., & Pike, G. B. (2012) · Multiple Sclerosis International · doi:10.1155/2012/742018 · Cited by 60 · see citing works
Widjaja, E., Geibprasert, S., Mahmoodabadi, S. Z., Blaser, S. E., Brown, N. E., & Shannon, P. T. (2010) · American Journal of Neuroradiology · doi:10.3174/ajnr.a1985 · Cited by 47 · see citing works
Advanced Multicompartment Diffusion MRI Models and Their Application in Multiple Sclerosis
Lakhani, D. A., Schilling, K. G., Xu, J., & Bagnato, F. R. (2020) · American Journal of Neuroradiology · doi:10.3174/ajnr.a6484 · Cited by 46 · see citing works
Utility of texture analysis for quantifying hepatic fibrosis on proton density MRI
Yu, H., Buch, K. A., Li, B., O’Brien, M. J., Soto, J. A., Jara, H. J., & Anderson, S. W. (2015) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.24898 · Cited by 45 · see citing works
Henssen, D. J. H. A., Mollink, J., Kurt, E., van Dongen, R. T. M., Bartels, R., Gräβel, D., Kozicz, T., Axer, M., & van Walsum, A. V. C. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1767-1 · Cited by 45 · see citing works
Lundell, H., Alexander, D. C., & Dyrby, T. B. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3137 · Cited by 44 · see citing works
Formalin tissue fixation biases myelin – sensitive MRI
Seifert, A. C., Umphlett, M., Hefti, M., Fowkes, M., & Xu, J. (2019) · Magnetic Resonance in Medicine · doi:10.1002/mrm.27821 · Cited by 44 · see citing works
Combined 7-T MRI and histopathologic study of normal and dysplastic samples from patients with TLE
Garbelli, R., Zucca, I., Milesi, G., Mastropietro, A., D’Incerti, L., Tassi, L., Colombo, N., Marras, C. E., Villani, F. S., Minati, L., et al. (2011) · Neurology · doi:10.1212/wnl.0b013e318212aae1 · Cited by 42 · see citing works
Korteweg, M. A., Zwanenburg, J. J. M., Hoogduin, J. M., van den Bosch, M. A. A. J., van Diest, P. J., van Hillegersberg, R., Eijkemans, M. J. C., Mali, W. P. T. M., Luijten, P. R., & Veldhuis, W. B. (2011) · Radiology · doi:10.1148/radiol.11103535 · Cited by 41 · see citing works
Aggarwal, M., Burnsed, J. C., Martin, L. J., Northington, F. J., & Zhang, J. (2013) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24956 · Cited by 40 · see citing works
Nabuurs, R. J. A., Hegeman, I., Natté, R., van Duinen, S. G., van Buchem, M. A., van der Weerd, L., & Webb, A. G. (2011) · NMR in Biomedicine · doi:10.1002/nbm.1598 · Cited by 39 · see citing works
Bourne, R., Panagiotaki, E., Bongers, A., Sved, P. D., Watson, G., & Alexander, D. C. (2013) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25032 · Cited by 39 · see citing works
Magnetic resonance microscopy of human and porcine neurons and cellular processes
Flint, J. J., Hansen, B., Portnoy, S., Lee, C.-H., King, M. A., Fey, M., Vincent, F., Stanisz, G. J., Vestergaard‐Poulsen, P., & Blackband, S. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.050 · Cited by 37 · see citing works
Self-citationZwirner, J., Möbius, D., Bechmann, I., Arendt, T., Hoffmann, K., Jäger, C., Lobsien, D., Möbius, R., Planitzer, U., Winkler, D. F. H., et al. (2016) · Human Brain Mapping · doi:10.1002/hbm.23427 · Cited by 38 · see citing works
Chen, H., Holmes, N., Liu, J., Tetzlaff, W., & Kozłowski, P. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.065 · Cited by 38 · see citing works
Goubran, M., Rudko, D. A., Santyr, B. G., Gati, J. S., Szekeres, T., Peters, T. M., & KHAN, A. R. (2013) · Human Brain Mapping · doi:10.1002/hbm.22423 · Cited by 37 · see citing works
Bulk, M., Abdelmoula, W. M., Geut, H., Wiarda, W., Ronen, I., Dijkstra, J., & van der Weerd, L. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116808 · Cited by 37 · see citing works
Tornifoglio, B., Stone, A. J., Johnston, R. D., Shahid, S. S., Kerskens, C., & Lally, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-77675-x · Cited by 37 · see citing works
Dibb, R., Qi, Y. P., & Liu, C. (2015) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/s12968-015-0159-4 · Cited by 36 · see citing works
Fast and simplified mapping of mean axon diameter using temporal diffusion spectroscopy
Xu, J., Li, H., Li, K., Harkins, K. D., Jiang, X., Xie, J., Kang, H., Dortch, R. D., Anderson, A. W., Does, M. D., et al. (2016) · NMR in Biomedicine · doi:10.1002/nbm.3484 · Cited by 34 · see citing works
Kenkhuis, B., Jonkman, L. E., Bulk, M., Buijs, M., Boon, B. D. C., Bouwman, F. H., Geurts, J. J. G., van de Berg, W. D. J., & van der Weerd, L. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101665 · Cited by 35 · see citing works
MRI of whole rat brain perivascular network reveals role for ventricles in brain waste clearance
Magdoom, K. N., Brown, A., Rey, J., Mareci, T. H., King, M. A., & Sarntinoranont, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-44938-1 · Cited by 35 · see citing works
Schmierer, K., Thavarajah, J. R., An, S.-F., Brandner, S., Miller, D. H., & Tozer, D. (2010) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22381 · Cited by 37 · see citing works
White matter biomarkers from diffusion MRI
Nørhøj Jespersen, S. (2018) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2018.03.001 · Cited by 34 · see citing works
Hales, P. W., Burton, R. A. B., Bollensdorff, C., Mason, F. E., Bishop, M. J., Gavaghan, D. J., Kohl, P. K., & Schneider, J. E. (2010) · NMR in Biomedicine · doi:10.1002/nbm.1629 · Cited by 34 · see citing works
Anderson, S. W., Jara, H. J., Ozonoff, A., O’Brien, M. J., Hamilton, J. A., & Soto, J. A. (2011) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22807 · Cited by 33 · see citing works
- Authors
- Shepherd, T. M., Thelwall, P. E., Stanisz, G. J., & Blackband, S. J.
- Affiliations
- University of California, San Francisco (US)
- Newcastle University (GB)
- Sunnybrook Health Science Centre (CA)
- University of Florida (US)
- Corresponding author
- Shepherd, Timothy M.
- Venue
- Magnetic Resonance in Medicine
- Publisher
- Wiley
- Published
- 2009-04-07
- Volume
- 62
- Issue
- 1
- Pages
- 26-34
- ISSN
- 0740-3194 (ISSN-L)
- 1522-2594
- PMC
- PMC3188415
- OpenAlex
- W1965000453
- Cited by
- 305
- References
- 39
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 19 · 2023: 16 · 2022: 18 · 2021: 16 · 2020: 21 · 2019: 27 · 2018: 25 · 2017: 17 · 2016: 12 · 2015: 20 · 2014: 17 · 2013: 17 · 2012: 14
- FWCI
- 12.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Magnetic Resonance in Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- National Institutes of Health (RO1 NS36992, P41 RR16105)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Physical Sciences › Physics and Astronomy › Nuclear and High Energy Physics › NMR spectroscopy and applications
- Keywords
- aldehyde fixatives, formalin fixation, glutaraldehyde fixation, T1 and T2 relaxation, water diffusion, apparent diffusion coefficient, extracellular diffusion, membrane permeability, cortical slices, brain atlas
- MeSH terms
- Animals, Brain, Brain Chemistry, Cells, Cultured, Diffusion, Fixatives, Formaldehyde, Male, Sensitivity and Specificity, Water, Reproducibility of Results, Artifacts, Rats, Long-Evans, Diffusion Magnetic Resonance Imaging, Rats
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