Skip to main content
Top
Published in: Neuroradiology 8/2017

01-08-2017 | Spinal Neuroradiology

Spinal cord microstructure integrating phase-sensitive inversion recovery and diffusional kurtosis imaging

Authors: V. Panara, R Navarra, P. A. Mattei, E. Piccirilli, A. R. Cotroneo, N. Papinutto, R. G. Henry, A. Uncini, M. Caulo

Published in: Neuroradiology | Issue 8/2017

Login to get access

Abstract

Purpose

The aim of this prospective study was to determine the feasibility in terms of repeatability and reproducibility of diffusional kurtosis imaging (DKI) for microstructural assessment of the normal cervical spinal cord (cSC) using a phase-sensitive inversion recovery (PSIR) sequence as the anatomical reference for accurately defining white-matter (WM) and gray-matter (GM) regions of interests (ROIs).

Methods

Thirteen young healthy subjects were enrolled to undergo DKI and PSIR sequences in the cSC. The repeatability and reproducibility of kurtosis metrics and fractional anisotropy (FA) were calculated in GM, WM, and cerebral-spinal-fluid (CSF) ROIs drawn by two independent readers on PSIR images of three different levels (C1–C4). The presence of statistically significant differences in DKI metrics for levels, ROIs (GM, WM, and CSF) repeatability, reproducibility, and inter-reader agreement was evaluated.

Results

Intra-class correlation coefficients between the two readers ranged from good to excellent (0.75 to 0.90). The inferior level consistently had the highest concordance. The lower values of scan–rescan variability for all DKI parameters were found for the inferior level. Statistically significant differences in kurtosis values were not found in the lateral white-matter bundles of the spinal cord.

Conclusion

The integration of DKI and PSIR sequences in a clinical MR acquisition to explore the regional microstructure of the cSC in healthy subjects is feasible, and the results obtainable are reproducible. Further investigation will be required to verify the possibility to translate this method to a clinical setting to study patients with SC involvement especially in the absence of MRI abnormalities on standard sequences.
Literature
2.
go back to reference Samson RS, Lévy S, Schneider T, Smith AK, Smith SA, Cohen-Adad J, Wheeler-Kingshott CA (2016) ZOOM or non-ZOOM? Assessing spinal cord diffusion tensor imaging protocols for multi-centre studies. PLoS One 11(5):1–14. doi:10.1371/journal.pone.0155557 CrossRef Samson RS, Lévy S, Schneider T, Smith AK, Smith SA, Cohen-Adad J, Wheeler-Kingshott CA (2016) ZOOM or non-ZOOM? Assessing spinal cord diffusion tensor imaging protocols for multi-centre studies. PLoS One 11(5):1–14. doi:10.​1371/​journal.​pone.​0155557 CrossRef
4.
go back to reference Raz E, Bester M, Sigmund EE, Tabesh A, Babb JS, Jaggi H, Helpern J, Mitnick RJ, Inglese M (2013) A better characterization of spinal cord damage in multiple sclerosis: a diffusional kurtosis imaging study. Am J Neuroradiol 34(9):1846–1852. doi:10.3174/ajnr.A3512 CrossRefPubMed Raz E, Bester M, Sigmund EE, Tabesh A, Babb JS, Jaggi H, Helpern J, Mitnick RJ, Inglese M (2013) A better characterization of spinal cord damage in multiple sclerosis: a diffusional kurtosis imaging study. Am J Neuroradiol 34(9):1846–1852. doi:10.​3174/​ajnr.​A3512 CrossRefPubMed
5.
go back to reference Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53(6):1432–1440. doi:10.1002/mrm.20508 CrossRefPubMed Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53(6):1432–1440. doi:10.​1002/​mrm.​20508 CrossRefPubMed
6.
go back to reference Conklin CJ, Middleton DM, Alizadeh M, Finsterbusch J, Raunig DL, Faro SH, Shah P, Krisa L, Sinko R, Delalic JZ, Mulcahey MJ, Mohamed FB (2016) Spatially selective 2D RF inner field of view (iFOV) diffusion kurtosis imaging (DKI) of the pediatric spinal cord. NeuroImage Clin 11:61–67. doi:10.1016/j.nicl.2016.01.009 CrossRefPubMedPubMedCentral Conklin CJ, Middleton DM, Alizadeh M, Finsterbusch J, Raunig DL, Faro SH, Shah P, Krisa L, Sinko R, Delalic JZ, Mulcahey MJ, Mohamed FB (2016) Spatially selective 2D RF inner field of view (iFOV) diffusion kurtosis imaging (DKI) of the pediatric spinal cord. NeuroImage Clin 11:61–67. doi:10.​1016/​j.​nicl.​2016.​01.​009 CrossRefPubMedPubMedCentral
7.
go back to reference Hori M, Tsutsumi S, Yasumoto Y, Ito M, Suzuki M, Tanaka FS, Kyogoku S, Nakamura M, Tabuchi T, Fukunaga I, Suzuki Y, Kamagata K, Masutani Y, Aoki S (2014) Cervical spondylosis: evaluation of microstructural changes in spinal cord white matter and gray matter by diffusional kurtosis imaging. Magn Reson Imaging 32(5):428–432. doi:10.1016/j.mri.2014.01.018 CrossRefPubMed Hori M, Tsutsumi S, Yasumoto Y, Ito M, Suzuki M, Tanaka FS, Kyogoku S, Nakamura M, Tabuchi T, Fukunaga I, Suzuki Y, Kamagata K, Masutani Y, Aoki S (2014) Cervical spondylosis: evaluation of microstructural changes in spinal cord white matter and gray matter by diffusional kurtosis imaging. Magn Reson Imaging 32(5):428–432. doi:10.​1016/​j.​mri.​2014.​01.​018 CrossRefPubMed
8.
go back to reference Hou P, Hasan KM, Sitton CW, Wolinsky JS, Narayana PA (2005) Phase-sensitive T1 inversion recovery imaging: a time-efficient interleaved technique for improved tissue contrast in neuroimaging. Am J Neuroradiol 26(6):1432–1438PubMed Hou P, Hasan KM, Sitton CW, Wolinsky JS, Narayana PA (2005) Phase-sensitive T1 inversion recovery imaging: a time-efficient interleaved technique for improved tissue contrast in neuroimaging. Am J Neuroradiol 26(6):1432–1438PubMed
9.
go back to reference Kearney H, Yiannakas MC, Abdel-Aziz K, Wheeler-Kingshott CA, Altmann DR, Ciccarelli O, Miller DH (2014) Improved MRI quantification of spinal cord atrophy in multiple sclerosis. J Magn Reson Imaging 39(3):617–623. doi:10.1002/jmri.24194 CrossRefPubMed Kearney H, Yiannakas MC, Abdel-Aziz K, Wheeler-Kingshott CA, Altmann DR, Ciccarelli O, Miller DH (2014) Improved MRI quantification of spinal cord atrophy in multiple sclerosis. J Magn Reson Imaging 39(3):617–623. doi:10.​1002/​jmri.​24194 CrossRefPubMed
10.
go back to reference Schraa B. (2013) T1-weighted phase sensitive inversion recovery for imaging multiple sclerosis lesions in the cervical SC. Clinical Neurology MAGNETOM Flash | 5/2013 Schraa B. (2013) T1-weighted phase sensitive inversion recovery for imaging multiple sclerosis lesions in the cervical SC. Clinical Neurology MAGNETOM Flash | 5/2013
11.
go back to reference Papinutto N, Schlaeger R, Panara V, Caverzasi E, Ahn S, Johnson KJ, Zhu AH, Stern WA, Laub G, Hauser SL, Henry RG (2015) 2D phase-sensitive inversion recovery imaging to measure in vivo spinal cord gray and white matter areas in clinically feasible acquisition times. J Magn Reson Imaging 42(3):698–708. doi:10.1002/jmri.24819 CrossRefPubMed Papinutto N, Schlaeger R, Panara V, Caverzasi E, Ahn S, Johnson KJ, Zhu AH, Stern WA, Laub G, Hauser SL, Henry RG (2015) 2D phase-sensitive inversion recovery imaging to measure in vivo spinal cord gray and white matter areas in clinically feasible acquisition times. J Magn Reson Imaging 42(3):698–708. doi:10.​1002/​jmri.​24819 CrossRefPubMed
12.
go back to reference Schlaeger R, Papinutto N, Panara V, Bevan C, Lobach IV, Bucci M, Caverzasi E, Gelfand JM, Green AJ, Jordan KM, Stern WA, von Büdingen HC, Waubant E, Zhu AH, Goodin DS, Cree BA, Hauser SL, Henry RG (2014) Spinal cord gray matter atrophy correlates with multiple sclerosis disability. Ann Neurol 76(4):568–580. doi:10.1002/ana.24241 CrossRefPubMedPubMedCentral Schlaeger R, Papinutto N, Panara V, Bevan C, Lobach IV, Bucci M, Caverzasi E, Gelfand JM, Green AJ, Jordan KM, Stern WA, von Büdingen HC, Waubant E, Zhu AH, Goodin DS, Cree BA, Hauser SL, Henry RG (2014) Spinal cord gray matter atrophy correlates with multiple sclerosis disability. Ann Neurol 76(4):568–580. doi:10.​1002/​ana.​24241 CrossRefPubMedPubMedCentral
13.
go back to reference Schlaeger R, Papinutto N, Zhu AH, Lobach IV, Bevan CJ, Bucci M, Castellano A, Gelfand JM, Graves JS, Green AJ, Jordan KM, Keshavan A, Panara V, Stern WA, von Büdingen HC, Waubant E, Goodin DS, Cree BA, Hauser SL, Henry RG (2015) Association between thoracic spinal cord gray matter atrophy and disability in multiple sclerosis. JAMA Neurol 72(8):897–904. doi:10.1001/jamaneurol.2015.0993 CrossRefPubMed Schlaeger R, Papinutto N, Zhu AH, Lobach IV, Bevan CJ, Bucci M, Castellano A, Gelfand JM, Graves JS, Green AJ, Jordan KM, Keshavan A, Panara V, Stern WA, von Büdingen HC, Waubant E, Goodin DS, Cree BA, Hauser SL, Henry RG (2015) Association between thoracic spinal cord gray matter atrophy and disability in multiple sclerosis. JAMA Neurol 72(8):897–904. doi:10.​1001/​jamaneurol.​2015.​0993 CrossRefPubMed
14.
go back to reference Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMed Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMed
20.
go back to reference Bester M, Jensen JH, Babb JS, Tabesh A, Miles L, Herbert J, Grossman RI, Inglese M (2015) Non-Gaussian diffusion MRI of gray matter is associated with cognitive impairment in multiple sclerosis. Mult Scler 21(7):935–944. doi:10.1177/1352458514556295 CrossRefPubMed Bester M, Jensen JH, Babb JS, Tabesh A, Miles L, Herbert J, Grossman RI, Inglese M (2015) Non-Gaussian diffusion MRI of gray matter is associated with cognitive impairment in multiple sclerosis. Mult Scler 21(7):935–944. doi:10.​1177/​1352458514556295​ CrossRefPubMed
21.
go back to reference Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, Castellanos FX, Jensen JH (2011) Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging 33(1):17–23. doi:10.1002/jmri.22397 CrossRefPubMedPubMedCentral Helpern JA, Adisetiyo V, Falangola MF, Hu C, Di Martino A, Williams K, Castellanos FX, Jensen JH (2011) Preliminary evidence of altered gray and white matter microstructural development in the frontal lobe of adolescents with attention-deficit hyperactivity disorder: a diffusional kurtosis imaging study. J Magn Reson Imaging 33(1):17–23. doi:10.​1002/​jmri.​22397 CrossRefPubMedPubMedCentral
23.
go back to reference Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. NeuroImage 45(1):S173–S186CrossRefPubMed Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM (2009) Bayesian analysis of neuroimaging data in FSL. NeuroImage 45(1):S173–S186CrossRefPubMed
26.
go back to reference Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, Cadotte D, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, Summers P, Tracey I (2014) The current state-of-the-art of spinal cord imaging: methods. NeuroImage 84:1070–1081. doi:10.1016/j.neuroimage.2013.04.124 CrossRefPubMed Stroman PW, Wheeler-Kingshott C, Bacon M, Schwab JM, Bosma R, Brooks J, Cadotte D, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, Summers P, Tracey I (2014) The current state-of-the-art of spinal cord imaging: methods. NeuroImage 84:1070–1081. doi:10.​1016/​j.​neuroimage.​2013.​04.​124 CrossRefPubMed
27.
go back to reference Wheeler-Kingshott CA, Stroman PW, Schwab JM, Bacon M, Bosma R, Brooks J, Cadotte DW, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, Summers P, Thompson AJ, Tracey I (2014) The current state-of-the-art of spinal cord imaging: applications. NeuroImage 84:1082–1093. doi:10.1016/j.neuroimage.2013.07.014 CrossRefPubMed Wheeler-Kingshott CA, Stroman PW, Schwab JM, Bacon M, Bosma R, Brooks J, Cadotte DW, Carlstedt T, Ciccarelli O, Cohen-Adad J, Curt A, Evangelou N, Fehlings MG, Filippi M, Kelley BJ, Kollias S, Mackay A, Porro CA, Smith S, Strittmatter SM, Summers P, Thompson AJ, Tracey I (2014) The current state-of-the-art of spinal cord imaging: applications. NeuroImage 84:1082–1093. doi:10.​1016/​j.​neuroimage.​2013.​07.​014 CrossRefPubMed
28.
go back to reference Reich DS, Smith SA, Jones CK, Zackowski KM, van Zijl PC, Calabresi PA, Mori S (2006) Quantitative characterization of the corticospinal tract at 3 Tesla. AJNR Am J Neuroradiol 27(10):2168–2178PubMedPubMedCentral Reich DS, Smith SA, Jones CK, Zackowski KM, van Zijl PC, Calabresi PA, Mori S (2006) Quantitative characterization of the corticospinal tract at 3 Tesla. AJNR Am J Neuroradiol 27(10):2168–2178PubMedPubMedCentral
29.
go back to reference Das SK, Wang JL, Bing L, Bhetuwal A, Yang HF (2016) Regional values of diffusional kurtosis estimates in the healthy brain during normal aging. Clin Neuroradiol [Epub ahead of print]. doi:10.1007/s00062-015-0490-z Das SK, Wang JL, Bing L, Bhetuwal A, Yang HF (2016) Regional values of diffusional kurtosis estimates in the healthy brain during normal aging. Clin Neuroradiol [Epub ahead of print]. doi:10.​1007/​s00062-015-0490-z
Metadata
Title
Spinal cord microstructure integrating phase-sensitive inversion recovery and diffusional kurtosis imaging
Authors
V. Panara
R Navarra
P. A. Mattei
E. Piccirilli
A. R. Cotroneo
N. Papinutto
R. G. Henry
A. Uncini
M. Caulo
Publication date
01-08-2017
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology / Issue 8/2017
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-017-1864-5

Other articles of this Issue 8/2017

Neuroradiology 8/2017 Go to the issue