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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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).

Manabu Mochizuki, Nobuo Sasaki, HIROYUKI OGAWA … (2005)

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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Magnetic resonance imaging in dogs with neurologic impairment due to acute thoracic and lumbar intervertebral disk herniation.

J M Levine, G T Fosgate, A. Chen … (2016)

Magnetic resonance imaging (MRI) is a correlate to physical examination in various myelopathies and a predictor of functional outcome. To describe associations among MRI features, neurological dysfunction before MRI, and functional outcome in dogs with disk herniation. One hundred and fifty-nine dogs with acute thoracolumbar disk herniation. Retrospective case series. Signalment, initial neurological function as assessed by a modified Frankel score (MFS), and ambulatory outcome at hospital discharge and >3 months (long-term) follow-up were recorded from medical records and telephone interview of owners. Associations were estimated between these parameters and MRI signal and morphometric data. Dogs with intramedullary T2W hyperintensity had more severe pre-MRI MFS (median 2, range 0-4) and lower ambulatory proportion at long-term follow-up (0.76) than those dogs lacking hyperintensity (median MFS 3, range 0-5; ambulatory proportion, 0.93) (P=.001 and .013, respectively). Each unit of T2W length ratio was associated with a 1.9 times lower odds of long-term ambulation when adjusted for pre-MRI MFS (95% confidence interval 1.0-3.52, P=.05). Dogs with a compressive length ratio >1.31 (which was the median ratio within this population) had more severe pre-MRI MFS (median 3, range 0-5) compared with those with ratios < or =1.31 (median MFS 3, range 0-4; P=.006). MRI features were associated with initial injury severity in dogs with thoracolumbar disk herniation. Based on results of this study, the T2W length ratio and presence of T2W intramedullary hyperintensity appear to be predictive of long-term ambulatory status.

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Author and article information

Contributors

Neringa Alisauskaite: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Ingo Spitzbarth: Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: Writing – original draft

Wolfgang Baumgärtner: Role: Data curationRole: InvestigationRole: Project administration

Peter Dziallas: Role: Data curationRole: MethodologyRole: Resources

Sabine Kramer: Role: Data curationRole: Resources

Ricarda Dening: Role: Data curationRole: Resources

Veronika Maria Stein: Role: ConceptualizationRole: Project administrationRole: Supervision

Andrea Tipold: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – review & editing

Carlos E. Ambrósio: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 22 November 2017

Publication date Collection: 2017

Volume: 12

Issue: 11

Electronic Location Identifier: e0187746

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.

* E-mail: neringavet@ 123456gmail.com

Article

Publisher ID: PONE-D-16-46013

DOI: 10.1371/journal.pone.0187746

PMC ID: 5699804

PubMed ID: 29166400

SO-VID: 3db3ec0c-ba71-4026-bf71-22b89edd32d8

License:

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.

History

Date received : 20 November 2016

Date accepted : 25 October 2017

Page count

Figures: 5, Tables: 7, Pages: 22

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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Data Availability All relevant data are within the paper and its Supporting Information files.

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

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Abstract

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Most cited references 49

Unraveling the riddle of syringomyelia.

Prognostic value of magnetic resonance imaging in dogs with paraplegia caused by thoracolumbar intervertebral disk extrusion: 77 cases (2000-2003).

Magnetic resonance imaging in dogs with neurologic impairment due to acute thoracic and lumbar intervertebral disk herniation.

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