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      Chronic post-traumatic intramedullary lesions in dogs, a translational model

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          Abstract

          Objectives

          Post-traumatic intramedullary myelopathies and cavitations are well described lesions following spinal cord injury (SCI) in humans and have been described in histopathological evaluations in dogs. Human intramedullary myelopathies/cavitations are associated with severe initial SCI and deterioration of clinical signs. Canine intervertebral disc extrusions share similarities with SCI in humans. In this descriptive study, magnetic resonance imaging (MRI) findings in spinal cords of dogs suffering from chronic post-traumatic myelopathies, including cavitations, are elucidated. An additional aim of the study was to compare diagnostic imaging and histopathological findings and identify similarities between human and canine chronic post-traumatic spinal cord lesions.

          Methods

          Thirty-seven dogs with thoracolumbar SCI and one or more 3Tesla MRI investigations more than 3 weeks after SCI were included. Extent of intramedullary lesions and particularly cavitations were evaluated and measured in sagittal and transverse MRI planes. These data were compared with clinical data.

          Results

          A total of 91.9% of study patients developed chronic intramedullary lesions, and 86.5% developed intramedullary cavitations. Paraplegia without deep pain perception at initial examination was significantly associated with longer chronic myelopathies/cavitations (P = 0.002/P = 0.008), and with larger maximal cross-sectional area (mCSA) of the lesions (P = 0.041/0.005). In addition, a non-ambulatory status after decompressive surgery was also associated with the development of longer intramedullary lesions/cavitations (P<0.001) and larger lesion mCSA (P<0.001/P = 0.012). All dogs with negative outcome developed myelopathies/cavitations. In the group of 21 dogs with positive outcome, 3 did not develop any myelopathies, and 5 did not develop cavitations.

          Conclusions

          Development of chronic intramedullary lesions/cavitations are common findings in canine SCI. Extensive chronic intramedullary lesions/cavitations reflect a severe initial SCI and negative clinical outcome. This supports the hypothesis that chronic spinal cord changes following SCI in humans share similarities with canine chronic spinal cord changes after spontaneous intervertebral disc extrusion.

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          Most cited references 49

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          Clinical canine spinal cord injury provides an opportunity to examine the issues in translating laboratory techniques into practical therapy.

          Review. To highlight the value of investigating the effects of putative therapeutic interventions in clinical spinal cord injury (SCI) in domestic dogs. England, UK. Many experimental interventions in laboratory rodents have been shown to ameliorate the functional deficits caused by SCI; the challenge now is to determine whether they can be translated into useful clinical techniques. Important differences between clinical SCI in human patients and that in laboratory rodents are in the size of the spinal cord and heterogeneity of injury severity. A further key issue is whether the statistical difference in outcome in the laboratory will translate into a useful difference in clinical outcome. Here, we stress the value of investigating the effects of putative therapies in clinical SCI in domestic dogs. The causes of injury, ability to categorise the severity and methods available to measure outcome are very similar between canine and human patients. Furthermore, postmortem tissue more rapidly becomes available from dogs because of their short lifespan than from human patients. The role that investigation of canine SCI might play is illustrated by our preliminary trials on intraspinal transplantation of olfactory glial cells for severe SCI. This canine translational model provides a means of 'filtering' putative treatments before human application.
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            Unraveling the riddle of syringomyelia.

             Dan Greitz (2006)
            The pathophysiology of syringomyelia development is not fully understood. Current prevailing theories suggest that increased pulse pressure in the subarachnoid space forces cerebrospinal fluid (CSF) through the spinal cord into the syrinx. It is generally accepted that the syrinx consists of CSF. The here-proposed intramedullary pulse pressure theory instead suggests that syringomyelia is caused by increased pulse pressure in the spinal cord and that the syrinx consists of extracellular fluid. A new principle is introduced implying that the distending force in the production of syringomyelia is a relative increase in pulse pressure in the spinal cord compared to that in the nearby subarachnoid space. The formation of a syrinx then occurs by the accumulation of extracellular fluid in the distended cord. A previously unrecognized mechanism for syrinx formation, the Bernoulli theorem, is also described. The Bernoulli theorem or the Venturi effect states that the regional increase in fluid velocity in a narrowed flow channel decreases fluid pressure. In Chiari I malformations, the systolic CSF pulse pressure and downward motion of the cerebellar tonsils are significantly increased. This leads to increased spinal CSF velocities and, as a consequence of the Bernoulli theorem, decreased fluid pressure in narrow regions of the spinal CSF pathways. The resulting relatively low CSF pressure in the narrowed CSF pathway causes a suction effect on the spinal cord that distends the cord during each systole. Syringomyelia develops by the accumulation of extracellular fluid in the distended cord. In posttraumatic syringomyelia, the downwards directed systolic CSF pulse pressure is transmitted and reflected into the spinal cord below and above the traumatic subarachnoid blockage, respectively. The ensuing increase in intramedullary pulse pressure distends the spinal cord and causes syringomyelia on both sides of the blockage. The here-proposed concept has the potential to unravel the riddle of syringomyelia and affords explanations to previously unanswered clinical and theoretical problems with syringomyelia. It also explains why syringomyelia associated with Chiari I malformations may develop in any part of the spinal cord including the medullary conus. Syringomyelia thus preferentially develops where the systolic CSF flow causes a suction effect on the spinal cord, i.e., at or immediately caudal to physiological or pathological encroachments of the spinal subarachnoid space.
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              Prognostic value of magnetic resonance imaging in dogs with paraplegia caused by thoracolumbar intervertebral disk extrusion: 77 cases (2000-2003).

              To determine whether magnetic resonance imaging findings in dogs with paraplegia caused by thoracolumbar intervertebral disk extrusion were predictive of clinical outcome. Retrospective case series. 77 dogs. Medical records and magnetic resonance images were reviewed; clinical outcome was classified as successful (regained ability to walk with no more than mild neurologic deficits) or unsuccessful (severe neurologic deficits persisted). The prognostic value of magnetic resonance imaging was compared with prognostic value of deep pain perception, duration of clinical signs, and rate of onset of clinical signs. 33 (43%) dogs had areas of hyperintensity of the spinal cord greater than or equal to the length of the L2 vertebral body on T2-weighted magnetic resonance images. All 44 dogs without areas of hyperintensity on T2-weighted images had a successful outcome, but only 18 of the 33 (55%) dogs with an area of hyperintensity did. Only 5 of 16 dogs with an area of hyperintensity that had also lost deep pain perception had a successful outcome. The odds ratio for an unsuccessful outcome for a dog with an area of hyperintensity (29.87) was higher than the odds ratio for a dog that had lost deep pain perception (5.24). Duration and rate of onset of clinical signs were not associated with clinical outcome. Findings suggest that results of magnetic resonance imaging can be used to predict clinical outcome in dogs with paraplegia caused by intervertebral disk extrusion.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: Project administration
                Role: Data curationRole: MethodologyRole: Resources
                Role: Data curationRole: Resources
                Role: Data curationRole: Resources
                Role: ConceptualizationRole: Project administrationRole: Supervision
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 November 2017
                2017
                : 12
                : 11
                Affiliations
                [1 ] Department of Small Animal Medicine and Surgery, University of Veterinary Medicine Hannover, Hannover, Germany
                [2 ] Department of Pathology, University of Veterinary Medicine Hannover, Hannover, Germany
                [3 ] Centre for Systems Neuroscience, University of Veterinary Medicine Hannover, Hannover, Germany
                Faculty of Animal Sciences and Food Engineering, University of São Paulo, BRAZIL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-16-46013
                10.1371/journal.pone.0187746
                5699804
                29166400
                © 2017 Alisauskaite et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 5, Tables: 7, Pages: 22
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: FOR 1103, project TI 309/4-1
                The present project was partly supported by the German Research Foundation (FOR 1103, project TI 309/4-1). It covered the MRI examination and decompressive surgery expenses of the plegic dogs. No financial support was provided to the authors of the manuscript. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.
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                Diagnostic Radiology
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