The role of diffusion tensor imaging as an objective tool for the assessment of motor function recovery after paraplegia in a naturally-occurring large animal model of spinal cord injury

Abstract

Background: Traumatic spinal cord injury (SCI) results in sensory and motor function impairment and may cause a substantial social and economic burden. For the implementation of novel treatment strategies, parallel development of objective tools evaluating spinal cord (SC) integrity during motor function recovery (MFR) is needed. Diffusion tensor imaging (DTI) enables in vivo microstructural assessment of SCI.

Methods: In the current study, temporal evolvement of DTI metrics during MFR were examined; therefore, values of fractional anisotropy (FA) and apparent diffusion coefficient (ADC) were measured in a population of 17 paraplegic dogs with naturally-occurring acute SCI showing MFR within 4 weeks after surgical decompression and compared to 6 control dogs. MRI scans were performed preoperatively and 12 weeks after MFR was observed. DTI metrics were obtained at the lesion epicentre and one SC segment cranially and caudally. Variance analyses were performed to compare values between evaluated localizations in affected dogs and controls and between time points. Correlations between DTI metrics and clinical scores at follow-up examinations were assessed.

Results: Before surgery, FA values at epicentres were higher than caudally (p = 0.0014) and control values (p = 0.0097); ADC values were lower in the epicentre compared to control values (p = 0.0035) and perilesional (p = 0.0448 cranially and p = 0.0433 caudally). In follow-up examinations, no significant differences could be found between DTI values from dogs showing MFR and control dogs. Lower ADC values at epicentres correlated with neurological deficits at follow-up examinations (r = - 0.705; p = 0.0023).

Conclusions: Findings suggest that a tendency to the return of DTI values to the physiological situation after surgical decompression accompanies MFR after SCI in paraplegic dogs. DTI may represent a useful and objective clinical tool for follow-up studies examining in vivo SC recovery in treatment studies.

Keywords: Canine; DTI; Follow-up studies; Hemilaminectomy; IVDH; Intervertebral disc herniation; MRI; SCI; Translational medicine.

Fig. 1

Flow chart illustrating the study design. DTI Diffusion tensor imaging, MFR motor function recovery, MRI magnetic resonance imaging, SC spinal cord, SCI spinal cord injury

Fig. 2

Selection of regions of interest. Sagittal and transverse T2W images and transverse colour-coded FA maps of the spinal cord of a 17.7 kg mix-breed male dog, 6.6 years-old, with acute onset of paraplegia due to an intervertebral disc herniation (IVDH) at the level of L1–2 before (a) and 12 weeks after decompressive surgery (b). The red arrow points at the epicentre of lesion in sagittal T2W images. The star in A shows the degenerated disc material compressing the SC. The white arrow in B shows the hemilaminectomy defect performed to achieve SC decompression. Colour coding of FA maps: blue depicts craniocaudal diffusion axis, green and red indicate ventrodorsal and laterolateral diffusion axis, respectively

Fig. 3

Distribution of FA values. Tukey boxplots depicting the distribution of fractional anisotropy (FA) values at each localization before (a) and 12 weeks after showing motor function recovery (b). Values at epicentres showed significant increases compared to controls and perilesional values measured caudal to the epicentre. No differences were found in the follow-up MRI examination

Fig. 4

Distribution of ADC values. Tukey boxplots depicting the distribution of apparent diffusion coefficient (ADC) values at each localization before decompressive surgery (a) and at follow-up scan 12 weeks after MFR (b). Before decompressive surgery, values gathered from the epicentre were significantly lower than that of controls. Epicentres displayed lower values than values cranially and caudally. At follow-up scans, ADC values from dogs with MFR did not differ from controls