Acute ex vivo changes in brain white matter diffusion tensor metrics
Autoři:
Matthew R. Walker aff001; Jidan Zhong aff002; Adam C. Waspe aff003; Thomas Looi aff003; Karolina Piorkowska aff003; James M. Drake aff001; Mojgan Hodaie aff001
Působiště autorů:
Institute of Medical Science, University of Toronto, Toronto, Ontario, Canada
aff001; Division of Brain, Imaging and Behaviour - Systems Neuroscience, Krembil Research Institute, University Health Network, Toronto, Ontario, Canada
aff002; Centre for Image Guided Innovation and Therapeutic Intervention, Hospital for Sick Children, Toronto, Ontario, Canada
aff003; Department of Medical Imaging, University of Toronto, Toronto, Ontario, Canada
aff004; Division of Neurosurgery, Hospital for Sick Children, Toronto, Ontario, Canada
aff005; Division of Neurosurgery, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada
aff006
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223211
Souhrn
Purpose
Diffusion magnetic resonance imaging and tractography has an important role in the visualization of brain white matter and assessment of tissue microstructure. There is a lack of correspondence between diffusion metrics of live tissue, ex vivo tissue, and histological findings. The objective of this study is to elucidate this connection by determining the specific diffusion alterations between live and ex vivo brain tissue. This may have an important role in the incorporation of diffusion imaging in ex vivo studies as a complement to histological sectioning as well as investigations of novel neurosurgical techniques.
Methods
This study presents a method of high angular resolution diffusion imaging and tractography of intact and non-fixed ex vivo piglet brains. Most studies involving ex vivo brain specimens have been formalin-fixed or excised from their original biological environment, processes both of which are known to affect diffusion parameters. Thus, non-fixed ex vivo tissue is used. A region-of-interest based analysis of diffusion tensor metrics are compared to in vivo subjects in a selection of major white matter bundles in order to assess the translatability of ex vivo diffusion measurements.
Results
Tractography was successfully achieved in both in vivo and ex vivo groups. No significant differences were found in tract connectivity, average streamline length, or apparent fiber density. Significantly decreased diffusivity (mean, axial, and radial; p<0.0005) in the non-fixed ex vivo group and unaltered fractional anisotropy (p>0.059) between groups were observed.
Conclusion
This study validates the extrapolation of non-fixed fractional anisotropy measurements to live tissue and the potential use of ex vivo tissue for methodological development.
Klíčová slova:
Central nervous system – Diffusion magnetic resonance imaging – Diffusion tensor imaging – Nerve fibers – Swine – Tractography – Anisotropy – corpus callosum
Zdroje
1. Roebroeck A, Miller KL, Aggarwal M. Ex vivo diffusion MRI of the human brain: Technical challenges and recent advances. NMR Biomed. John Wiley & Sons, Ltd; 2018; e3941. doi: 10.1002/nbm.3941 29863793
2. Shepherd TM, Thelwall PE, Stanisz GJ, Blackband SJ. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med. NIH Public Access; 2009;62: 26–34. doi: 10.1002/mrm.21977 19353660
3. Thelwall PE, Shepherd TM, Stanisz GJ, Blackband SJ. Effects of temperature and aldehyde fixation on tissue water diffusion properties, studied in an erythrocyte ghost tissue model. Magn Reson Med. Wiley Subscription Services, Inc., A Wiley Company; 2006;56: 282–289. doi: 10.1002/mrm.20962 16841346
4. Pfefferbaum A, Sullivan E V., Adalsteinsson E, Garrick T, Harper C. Postmortem MR imaging of formalin-fixed human brain. Neuroimage. 2004;21: 1585–1595. doi: 10.1016/j.neuroimage.2003.11.024 15050582
5. Tovi M, Ericsson A. Measurements of T1 and T2 over time in formalin-fixed human whole-brain specimens. Acta Radiol. 1992;33: 400–4. 1389643
6. Miller KL, Stagg CJ, Douaud G, Jbabdi S, Smith SM, Behrens TEJJ, et al. Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. Neuroimage. 2011;57: 167–181. doi: 10.1016/j.neuroimage.2011.03.070 21473920
7. Beaulieu C. The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed. Department of Biomedical Engineering, Faculty of Medicine, University of Alberta, Edmonton, Canada. christian.beaulieu@ualberta.ca; 2002;15: 435–455. doi: 10.1002/nbm.782 12489094
8. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage. Department of Chemistry, Washington University, St. Louis, Missouri 63110, USA. victor@wuchem.wustl.edu; 2002;17: 1429–1436. doi: 10.1006/nimg.2002.1267 12414282
9. Horsfield MA, Jones DK. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases—a review. NMR Biomed. 2002;15: 570–577. doi: 10.1002/nbm.787 12489103
10. Pagani E, Filippi M, Rocca MA, Horsfield MA. A method for obtaining tract-specific diffusion tensor MRI measurements in the presence of disease: application to patients with clinically isolated syndromes suggestive of multiple sclerosis. Neuroimage. Department of Cardiovascular Sciences, University of Leicester, UK; 2005;26: 258–265. doi: 10.1016/j.neuroimage.2005.01.008 15862226
11. Schmidt TM, Fischer R, Acar S, Lorenzen M, Heinemann A, Wedegärtner U, et al. DWI of the brain: Postmortal DWI of the brain in comparison with in vivo data. Forensic Sci Int. 2012;220: 180–183. doi: 10.1016/j.forsciint.2012.02.022 22445270
12. D’Arceuil H, de Crespigny A. The effects of brain tissue decomposition on diffusion tensor imaging and tractography. Neuroimage. NIH Public Access; 2007;36: 64–68. doi: 10.1016/j.neuroimage.2007.02.039 17433879
13. Flach PM, Schroth S, Schweitzer W, Ampanozi G, Slotboom J, Kiefer C, et al. Deep Into the Fibers! Postmortem Diffusion Tensor Imaging in Forensic Radiology. Am J Forensic Med Pathol. 2015;36: 153–161. doi: 10.1097/PAF.0000000000000177 26132433
14. Guilfoyle DN, Helpern JA, Lim KO. Diffusion tensor imaging in fixed brain tissue at 7.0 T. NMR Biomed. 2003;16: 77–81. doi: 10.1002/nbm.814 12730948
15. Sun S-W, Neil JJ, Liang H-F, He YY, Schmidt RE, Hsu CY, et al. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn Reson Med. Wiley Subscription Services, Inc., A Wiley Company; 2005;53: 1447–1451. doi: 10.1002/mrm.20488 15906292
16. Sun S-W, Neil JJ, Song S-K. Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med. Wiley Subscription Services, Inc., A Wiley Company; 2003;50: 743–748. doi: 10.1002/mrm.10605 14523960
17. Yen K, Weis J, Kreis R, Aghayev E, Jackowski C, Thali M, et al. Line-Scan Diffusion Tensor Imaging of the Posttraumatic Brain Stem: Changes with Neuropathologic Correlation. Am J Neuroradiol. 2006;38: 70–73.
18. Schmierer K, Wheeler-Kingshott CAM, Boulby PA, Scaravilli F, Altmann DR, Barker GJ, et al. Diffusion tensor imaging of post mortem multiple sclerosis brain. Neuroimage. Elsevier; 2007;35: 467–77. doi: 10.1016/j.neuroimage.2006.12.010 17258908
19. D’Arceuil HE, Westmoreland S, de Crespigny AJ. An approach to high resolution diffusion tensor imaging in fixed primate brain. Neuroimage. 2007;35: 553–565. doi: 10.1016/j.neuroimage.2006.12.028 17292630
20. Haakma W, Pedersen M, Froeling M, Uhrenholt L, Leemans A, Boel LWT. Diffusion tensor imaging of peripheral nerves in non-fixed post-mortem subjects. Forensic Sci Int. Elsevier Ireland Ltd; 2016;263: 139–146. doi: 10.1016/j.forsciint.2016.04.001 27107969
21. Madi S, Hasan KM, Narayana PA. Diffusion tensor imaging of in vivo and excised rat spinal cord at 7 T with an icosahedral encoding scheme. Magn Reson Med. 2005;53: 118–25. doi: 10.1002/mrm.20304 15690510
22. Pattany PM, Puckett WR, Klose KJ, Quencer RM, Bunge RP, Kasuboski L, et al. High-resolution diffusion-weighted MR of fresh and fixed cat spinal cords: evaluation of diffusion coefficients and anisotropy. AJNR Am J Neuroradiol. 1997;18: 1049–56. 9194432
23. Beaulieu C, Allen PS. Determinants of anisotropic water diffusion in nerves. Magn Reson Med. 1994;31: 394–400. doi: 10.1002/mrm.1910310408 8208115
24. Richardson S, Siow B, Panagiotaki E, Schneider T, Lythgoe MF, Alexander DC. Viable and fixed white matter: diffusion magnetic resonance comparisons and contrasts at physiological temperature. Magn Reson Med. 2014;72: 1151–61. doi: 10.1002/mrm.25012 24243402
25. Scheurer E, Lovblad K-O, Kreis R, Maier SE, Boesch C, Dirnhofer R, et al. Forensic application of postmortem diffusion-weighted and diffusion tensor MR imaging of the human brain in situ. AJNR Am J Neuroradiol. American Society of Neuroradiology; 2011;32: 1518–24. doi: 10.3174/ajnr.A2508 21659482
26. Bär W, Kratzer A, Mächler M, Schmid W. Postmortem stability of DNA. Forensic Sci Int. 1988;39: 59–70. doi: 10.1016/0379-0738(88)90118-1 2905319
27. Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed. John Wiley & Sons, Ltd.; 2010;23: 803–820. doi: 10.1002/nbm.1543 20886566
28. Chang H, Fitzpatrick JM. A technique for accurate magnetic resonance imaging in the presence of field inhomogeneities. IEEE Trans Med Imaging. 1992;11: 319–329. doi: 10.1109/42.158935 18222873
29. Andersson JLR, Skare S, Ashburner J. How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage. 2003;20: 870–888. doi: 10.1016/S1053-8119(03)00336-7 14568458
30. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62: 782–790. doi: 10.1016/j.neuroimage.2011.09.015 21979382
31. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23 Suppl 1: S208–19. doi: 10.1016/j.neuroimage.2004.07.051 15501092
32. Andersson JLR, Sotiropoulos SN. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage. 2016;125: 1063–1078. doi: 10.1016/j.neuroimage.2015.10.019 26481672
33. Veraart J, Sijbers J, Sunaert S, Leemans A, Jeurissen B. Weighted linear least squares estimation of diffusion MRI parameters: Strengths, limitations, and pitfalls. Neuroimage. 2013;81: 335–346. doi: 10.1016/j.neuroimage.2013.05.028 23684865
34. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. The Biophysical Society; 1994;66: 259–67. doi: 10.1016/S0006-3495(94)80775-1 8130344
35. Westin C-F, Peled S, Gudbjartsson H, Kikinis R, Jolesz F. Geometrical Diffusion Measures for MRI from Tensor Basis Analysis. Proceedings of the 5th Annual Meeting of ISMRM ‘97. 1997. p. 1742.
36. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17: 825–41. 12377157
37. Dhollander T, Raffelt D, Connelly A. Unsupervised 3-tissue response function estimation from single-shell or multi-shell diffusion MR data without a co-registered T1 image. ISMRM Workshop on Breaking the Barriers of Diffusion MRI. ISMRM Workshop on Breaking the Barriers of Diffusion MRI; 2016. p. 5.
38. Tax CM, Jeurissen B, Vos SB, Viergever MA, Leemans A. Recursive calibration of the fiber response function for spherical deconvolution of diffusion MRI data. Neuroimage. 2014;86: 67–80. doi: 10.1016/j.neuroimage.2013.07.067 23927905
39. Tournier J-D, Calamante F, Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: Non-negativity constrained super-resolved spherical deconvolution. Neuroimage. 2007;35: 1459–1472. doi: 10.1016/j.neuroimage.2007.02.016 17379540
40. Tournier J-D, Calamante F, Gadian DG, Connelly A. Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage. 2004;23: 1176–85. doi: 10.1016/j.neuroimage.2004.07.037 15528117
41. Tournier J-D, Yeh C-H, Calamante F, Cho K-H, Connelly A, Lin C-P. Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data. Neuroimage. 2008;42: 617–625. doi: 10.1016/j.neuroimage.2008.05.002 18583153
42. Tournier J-D, Calamante F, Connelly A. MRtrix: Diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol. Wiley Subscription Services, Inc., A Wiley Company; 2012;22: 53–66. doi: 10.1002/ima.22005
43. Dhollander T, Smith RE, Tournier J-D, Jeurissen B, Connelly A. Time to move on: an FOD-based DEC map to replace DTI’s trademark DEC FA. 23rd International Society of Magnetic Resonance in Medicine, At Toronto, Ontario, Canada. 2015. p. 1027.
44. Dhollander T, Raffelt D, Smith RE, Connelly A. Panchromatic sharpening of FOD-based DEC maps by structural T1 information. 23rd International Society of Magnetic Resonance in Medicine, At Toronto, Ontario, Canada. 2015. p. 566.
45. Hofer S, Frahm J. Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage. 2006;32: 989–994. doi: 10.1016/j.neuroimage.2006.05.044 16854598
46. Chen DQ, Strauss I, Hayes DJ, Davis KD, Hodaie M. Age-related changes in diffusion tensor imaging metrics of fornix subregions in healthy humans. Stereotact Funct Neurosurg. 2015;93: 151–9. doi: 10.1159/000368442 25790958
47. DeSouza DD, Hodaie M, Davis KD. Abnormal trigeminal nerve microstructure and brain white matter in idiopathic trigeminal neuralgia. Pain. 2014;155: 37–44. doi: 10.1016/j.pain.2013.08.029 23999058
48. Hui ES, Cheung MM, Chan KC, Wu EX. B-value dependence of DTI quantitation and sensitivity in detecting neural tissue changes. Neuroimage. 2010;49: 2366–2374. doi: 10.1016/j.neuroimage.2009.10.022 19837181
49. Polders DL, Leemans A, Hendrikse J, Donahue MJ, Luijten PR, Hoogduin JM. Signal to noise ratio and uncertainty in diffusion tensor imaging at 1.5, 3.0, and 7.0 Tesla. J Magn Reson Imaging. Wiley Subscription Services, Inc., A Wiley Company; 2011;33: 1456–1463. doi: 10.1002/jmri.22554 21591016
50. Kiernan JA. Histological and Histochemical Methods: Theory and Practice. 3rd ed. Oxford: Butterworth-Heinemann; 1999.
51. Le Bihan D. Diffusion and Perfusion Magnetic Resonance Imaging: Applications to Functional MRI. Le Bihan D, editor. New York: Raven Press; 1995.
52. Dyrby TB, Baaré WFC, Alexander DC, Jelsing J, Garde E, Søgaard L V. An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Mapp. Wiley Subscription Services, Inc., A Wiley Company; 2011;32: 544–563. doi: 10.1002/hbm.21043 20945352
53. Knösche TR, Anwander A, Liptrot M, Dyrby TB. Validation of tractography: Comparison with manganese tracing. Hum Brain Mapp. Wiley-Blackwell; 2015;36: 4116–34. doi: 10.1002/hbm.22902 26178765
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