Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging

Abstract Background Traumatic spinal cord injury (SCI) causes spinal cord swelling and occlusion of the subarachnoid space (SAS). SAS occlusion can change pulsatile cerebrospinal fluid (CSF) dynamics, which could have acute clinical management implications. This study aimed to characterise SAS occlu...

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Main Authors: Madeleine Amy Bessen, Christine Diana Gayen, Ryan L. O’Hare Doig, Ryan Michael Dorrian, Ryan David Quarrington, Adnan Mulaibrahimovic, Vartan Kurtcuoglu, Angela Catherine Walls, Anna Victoria Leonard, Claire Frances Jones
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Fluids and Barriers of the CNS
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Online Access:https://doi.org/10.1186/s12987-024-00595-9
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author Madeleine Amy Bessen
Christine Diana Gayen
Ryan L. O’Hare Doig
Ryan Michael Dorrian
Ryan David Quarrington
Adnan Mulaibrahimovic
Vartan Kurtcuoglu
Angela Catherine Walls
Anna Victoria Leonard
Claire Frances Jones
author_facet Madeleine Amy Bessen
Christine Diana Gayen
Ryan L. O’Hare Doig
Ryan Michael Dorrian
Ryan David Quarrington
Adnan Mulaibrahimovic
Vartan Kurtcuoglu
Angela Catherine Walls
Anna Victoria Leonard
Claire Frances Jones
author_sort Madeleine Amy Bessen
collection DOAJ
description Abstract Background Traumatic spinal cord injury (SCI) causes spinal cord swelling and occlusion of the subarachnoid space (SAS). SAS occlusion can change pulsatile cerebrospinal fluid (CSF) dynamics, which could have acute clinical management implications. This study aimed to characterise SAS occlusion and investigate CSF dynamics over 14 days post-SCI in the pig. Methods A thoracic contusion SCI was induced in female domestic pigs (22–29 kg) via a weight drop apparatus (N = 5, 10 cm; N = 5, 20 cm). Magnetic resonance imaging (MRI) was performed pre-SCI and 3, 7 and 14 days post-SCI. SAS occlusion length (cranial-caudal), and injury site SAS area (cross-sectional), were measured on T2-weighted MRI. CSF dynamics, specifically peak cranial/caudal mean velocity (cm/s), and the corresponding time to peak (% of cardiac cycle), were measured on cardiac gated, axial phase-contrast MRI obtained at C2/C3, T8/T9, T11/T12 and L1/L2. Linear-mixed effects models, with a significance level of α = 0.05, were developed to assess the effect of: (1) injury group and time point on SAS occlusion measures; and (2), time point and spinal level, adjusted by injury group, on CSF dynamics. Results For both injury groups, SAS occlusion length decreased from 3 to 7 days post-SCI, and 7 to 14 days post-SCI. The cross-sectional SAS area decreased after SCI, and increased to 14 days post-SCI, in both groups. At all spinal levels, peak cranial/caudal mean velocity and the time to peak caudal mean velocity decreased at day 3 post-SCI. From 3 to 14 days post-SCI, peak caudal mean velocity and the time to peak caudal mean velocity increased towards baseline values, at all spinal levels. Conclusions Spinal-level specific changes to CSF dynamics, with concurrent changes to SAS occlusion, occurred after SCI in the pig, suggesting that CSF pulsatility and craniospinal compliance were altered in the sub-acute post-traumatic period. These results suggest that PC-MRI derived CSF dynamics may provide a non-invasive method to investigate functional alterations to the spinal intrathecal space following traumatic SCI.
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spelling doaj-art-6601b2c6765145199089169fdd9297af2025-01-19T12:35:49ZengBMCFluids and Barriers of the CNS2045-81182025-01-0122111610.1186/s12987-024-00595-9Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imagingMadeleine Amy Bessen0Christine Diana Gayen1Ryan L. O’Hare Doig2Ryan Michael Dorrian3Ryan David Quarrington4Adnan Mulaibrahimovic5Vartan Kurtcuoglu6Angela Catherine Walls7Anna Victoria Leonard8Claire Frances Jones9Adelaide Spinal Research Group & Centre for Orthopaedics and Trauma Research, Faculty of Health and Medical Sciences, The University of AdelaideAdelaide Spinal Research Group & Centre for Orthopaedics and Trauma Research, Faculty of Health and Medical Sciences, The University of AdelaideAdelaide Medical School, The University of AdelaideTranslational Neuropathology Laboratory, School of Biomedicine, The University of AdelaideAdelaide Spinal Research Group & Centre for Orthopaedics and Trauma Research, Faculty of Health and Medical Sciences, The University of AdelaideAdelaide Spinal Research Group & Centre for Orthopaedics and Trauma Research, Faculty of Health and Medical Sciences, The University of AdelaideInstitute of Physiology, University of ZurichClinical and Research Imaging Centre, South Australian Health and Medical Research Institute, National Imaging FacilityTranslational Neuropathology Laboratory, School of Biomedicine, The University of AdelaideAdelaide Spinal Research Group & Centre for Orthopaedics and Trauma Research, Faculty of Health and Medical Sciences, The University of AdelaideAbstract Background Traumatic spinal cord injury (SCI) causes spinal cord swelling and occlusion of the subarachnoid space (SAS). SAS occlusion can change pulsatile cerebrospinal fluid (CSF) dynamics, which could have acute clinical management implications. This study aimed to characterise SAS occlusion and investigate CSF dynamics over 14 days post-SCI in the pig. Methods A thoracic contusion SCI was induced in female domestic pigs (22–29 kg) via a weight drop apparatus (N = 5, 10 cm; N = 5, 20 cm). Magnetic resonance imaging (MRI) was performed pre-SCI and 3, 7 and 14 days post-SCI. SAS occlusion length (cranial-caudal), and injury site SAS area (cross-sectional), were measured on T2-weighted MRI. CSF dynamics, specifically peak cranial/caudal mean velocity (cm/s), and the corresponding time to peak (% of cardiac cycle), were measured on cardiac gated, axial phase-contrast MRI obtained at C2/C3, T8/T9, T11/T12 and L1/L2. Linear-mixed effects models, with a significance level of α = 0.05, were developed to assess the effect of: (1) injury group and time point on SAS occlusion measures; and (2), time point and spinal level, adjusted by injury group, on CSF dynamics. Results For both injury groups, SAS occlusion length decreased from 3 to 7 days post-SCI, and 7 to 14 days post-SCI. The cross-sectional SAS area decreased after SCI, and increased to 14 days post-SCI, in both groups. At all spinal levels, peak cranial/caudal mean velocity and the time to peak caudal mean velocity decreased at day 3 post-SCI. From 3 to 14 days post-SCI, peak caudal mean velocity and the time to peak caudal mean velocity increased towards baseline values, at all spinal levels. Conclusions Spinal-level specific changes to CSF dynamics, with concurrent changes to SAS occlusion, occurred after SCI in the pig, suggesting that CSF pulsatility and craniospinal compliance were altered in the sub-acute post-traumatic period. These results suggest that PC-MRI derived CSF dynamics may provide a non-invasive method to investigate functional alterations to the spinal intrathecal space following traumatic SCI.https://doi.org/10.1186/s12987-024-00595-9CSFSpineFlowVelocityDynamicsPulsatile
spellingShingle Madeleine Amy Bessen
Christine Diana Gayen
Ryan L. O’Hare Doig
Ryan Michael Dorrian
Ryan David Quarrington
Adnan Mulaibrahimovic
Vartan Kurtcuoglu
Angela Catherine Walls
Anna Victoria Leonard
Claire Frances Jones
Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
Fluids and Barriers of the CNS
CSF
Spine
Flow
Velocity
Dynamics
Pulsatile
title Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
title_full Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
title_fullStr Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
title_full_unstemmed Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
title_short Cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig: an investigation using magnetic resonance imaging
title_sort cerebrospinal fluid dynamics and subarachnoid space occlusion following traumatic spinal cord injury in the pig an investigation using magnetic resonance imaging
topic CSF
Spine
Flow
Velocity
Dynamics
Pulsatile
url https://doi.org/10.1186/s12987-024-00595-9
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