Abstract
Study design
This investigation was a cohort study that included: 36 typically developing (TD) children and 19 children with spinal cord lesions who underwent spinal cord MRI.
Objectives
To investigate diffusion tensor imaging (DTI) cervical and thoracic spinal cord changes in pediatric patients that have clinically traumatic and non-traumatic spinal cord injury (SCI) without MR (SCIWOMR) abnormalities.
Setting
Thomas Jefferson University, Temple University, Shriners Hospitals for Children all in Philadelphia, USA.
Methods
36 TD children and 19 children with spinal cord lesions that represent either a chronic traumatic acquired SCI or chronic non-traumatic SCI (≥6 months post injury), age range, 6–16 years who underwent cervical and thoracic spinal cord MRI in 2014–2017. Additionally DTI was correlated to clinical American Spinal Injury Association Impairment Scale (AIS).
Results
Both SCIWOMR and MRI positive (+) groups showed abnormal FA and RD DTI values in the adjacent MRI-normal appearing segments of cephalad and caudal spinal cord compared to TD. The FA values demonstrated perilesional abnormal DTI findings in the middle and proximal segments of the cephalad and caudal cord in the SCIWOMR AIS A/B group compared to SCIWOMR AIS C/D group.
Conclusions
We found DTI changes in children with SCIWOMR with different causes of spinal lesions. We also investigated the relationship between DTI and clinical AIS scores. This study further examined the potential diagnostic value of DTI and should be translatable to adults with spinal cord lesions.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Data availability
Raw data is available upon request assuming a data sharing agreement can be executed.
References
Pang D. Spinal cord injury without radiographic abnormality in children, 2 decades later. Neurosurgery.2004;55:1325–43.
Piatt JH. Pediatric spinal injury in the US: epidemiology and disparities. J Neurosurg—Pediatr. 2015;16:463–71.
Osenback RK, Menezes AH. Spinal cord injury without radiographic abnormality in children. Pediatr Neurosurg. 1989;15:168–75.
Pang D. Spinal cord injury without radiographic abnormality in children. In: Betz RR, Mulcahey MJ The child with a spinal cord injury. Rosemont, IL: American Academy of Orthopedic Surgeons. 1996;168–75.
Oyinbo CA. Secondary injury mechanisms in traumatic spinal cord injury: a nugget of this multiply cascade. Acta Neurobiol Exp. 2011;71:281–99.
Jones LL, Margolis RU, Tuszynski MH. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol. 2003;182:399–411.
Schultz SS. Adult stem cell application in spinal cord injury. Curr Drug Targets. 2005;6:63–73.
Knerlich-Lukoschus F, Held-Feindt J. Chemokine-ligands/receptors: multiplayers in traumatic spinal cord injury. Mediators Inflamm. 2015;2015:486758.
Cohen-Adad J, Leblond H, Delivet-Mongrain H, Martinez M, Benali H, Rossignol S. Wallerian degeneration after spinal cord lesions in cats detected with diffusion tensor imaging. Neuroimage. 2011;57:1068–76.
Schwartz ED, Duda J, Shumsky JS, Cooper ET, Gee J. Spinal cord diffusion tensor imaging and fiber tracking can identify white matter tract disruption and glial scar orientation following lateral funiculotomy. J Neurotrauma. 2005;22:1388–98.
Freund P, Schneider T, Nagy Z, Hutton C, Weiskopf N, Friston K, et al. Degeneration of the injured cervical cord is associated with remote changes in corticospinal tract integrity and upper limb impairment. PLoS ONE. 2012;7:e51729 https://doi.org/10.1371/journal.pone.0051729
David G, Seif M, Huber E, Hupp M, Rosner J, Dietz V, et al. In vivo evidence of remote neural degeneration in the lumbar enlargement after cervical injury. Neurology.2019;92:e1367–77.
Ziegler G, Grabher P, Thompson A, Altmann D, Hupp M, Ashburner J, et al. Progressive neurodegeneration following spinal cord injury: Implications for clinical trials. Neurology.2018;90:e1257–66.
Como JJ, Samia H, Nemunaitis GA, Jain V, Anderson JS, Malangoni MA, et al. The misapplication of the term spinal cord injury without radiographic abnormality (SCIWORA) in adults. J Trauma Acute Care Surg. 2012;73:1261–6.
Boese CK, Lechler P. Spinal cord injury without radiologic abnormalities in adults: a systematic review. J Trauma Acute Care Surg. 2013;75:320–30.
Shen H, Tank Y, Huang L, et al. Applications of diffusion-weighted MRI in thoracic spinal cord injury without radiographic abnormality. Int Orthop. 2007;31:375–83.
Sundberg LM, Herrera JJ, Narayana PA. In vivo longitudinal MRI and behavioral studies in experimental spinal cord injury. J Neurotrauma. 2010;27:1753–67.
Ellingson BM, Schmit BD, Kurpad SN. Lesion growth and degeneration patterns using diffusion tensor 9.4-T magnetic resonance imaging in rat spinal cord injury. J Neurosurg Spine. 2010;13:181–92.
Saksena S, Mohamed FB, Middleton DM, Krisa L, Alizadeh M, Shahrampour S. DTI Assessment of Regional White Matter Changes in the cervical and thoracic spinal cord in pediatric participants. J Neurotrauma. 2019;19:853–61.
Conklin CJ, Middleton DM, Alizadeh M, Finsterbusch J, Raunig DL, Faro SH, et al. Spatially selective 2D RF inner field of view (iFOV) diffusion kurtosis imaging (DKI) of the pediatric spinal cord. Neuroimage Clin. 2016;11:61–7.
Yucesoy K, Yuksel KZ. SCIWORA in MRI era. Clin Neurol Neurosurg. 2008;110:429–33.
Flanders A, Spettell CM, Tartaglino LM, Friedman DP, Herbison GJ. Forecasting motor recovery after cervical spinal cord injury: value of MR imaging. Radiology.1996;201:649–55.
Cohen-Adad J, El Mendili M, Lehericy S, Pradat PF, Blancho S, Rossignol S, et al. Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI. Neuroimage. 2011;55:1024–33.
Petersen JA, Wilm BJ, von Meyenburg J, Schubert M, Seifert B, Najafi Y, et al. Chronic cervical spinal cord injury: DTI correlates with clinical and electrophysiological measures. J Neurotrauma. 2012;29:1556–66.
Koskinen E, Brander A, Hakulinen U, Luoto T, Helminen M, Ylinen A, et al. Assessing the state of chronic spinal cord injury using diffusion tensor imaging. J Neurotrauma. 2013;30:1587–95.
Kirshblum SC, Burns SP, Biering-Sorensen F, Betz R, Donovan W, Graves DE, et al. International standards for neurological classification of spinal cord injury (Revised 2011). J Spinal Cord Med. 2011;34:535–46.
Saksena S, Alizadeh M, Middleton DM, Conklin CJ, Krisa L, Flanders A, et al. Characterization of spinal cord diffusion tensor imaging metrics in clinically asymptomatic pediatric subjects with incidental congenital lesions. Spinal Cord Ser Cases. 2018;4:41.
Finsterbusch J. Improving the performance of diffusion-weighted inner field-of-view echo-planar imaging based on 2D-selective radiofrequency excitations by tilting the excitation plane. J Magn Reson Imaging. 2012;35:984–92.
Middleton DM, Mohamed FB, Barakat N, Hunter LN, Shellikeri S, Finsterbusch J, et al. An investigation of motion correction algorithms for pediatric spinal cord DTI in healthy participants and individuals with spinal cord injury. Magn Reson Imaging. 2014;32:433–9.
Chang LC, Jones DK, Pierpaoli C. RESTORE: Robust estimation of tensors by outlier rejection. Magn Reson Med. 2005;53:1088–95.
Ren J, Zeng G, Ma YJ, Chen N, Chen Z, Ling F, et al. Pediatric thoracic SCIWORA after back bend during dance practice: a retrospective case series and analysis of trauma mechanisms. Childs Nerv Syst. 2017;33:1191–8.
Vedantam A, Jirjis MB, Schmit BD, Wang MC, Ulmer JL, Kurpad SN. Diffusion tensor imaging of the spinal cord: insights from animal and human studies. Neurosurgery. 2014;74:1–8.
Budde MD, Kim JH, Liang HF, Schmidt RE, Russell JH, Cross AH, et al. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn Reson Med. 2007;57:688–95.
Acknowledgements
We thank Rebecca Sinko, OTR/L, OTD for her help with participant recruitment and data collection.
Funding
NIH -RO1 NSO79635-01A1 Mulcahey and Mohamed –co-PIs.
Author information
Authors and Affiliations
Contributions
Conceived and designed the analysis: SF, SS, LK, DM, MA, AF, FM. Collected the data: SF, SS, LK, DM, MA, MJ, FM. Contributed data or analysis tools: SF, SS, MA, DM, FM. Performed the analysis: SF, SS. Wrote the paper: SF, SS, LK, DM, MA, AF, KT, MJM, FB. Other contribution: JF - designed the MR sequence.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
This study was approved by the Thomas Jefferson University institutional review board (16 F.577). We certify that all applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during the course of this research.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Faro, S.H., Saksena, S., Krisa, L. et al. DTI of chronic spinal cord injury in children without MRI abnormalities (SCIWOMR) and with pathology on MRI and comparison to severity of motor impairment. Spinal Cord 60, 457–464 (2022). https://doi.org/10.1038/s41393-022-00770-5
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41393-022-00770-5
