Characterising spinal cerebrospinal fluid flow in the pig with phase-contrast magnetic resonance imaging

Madeleine Amy Bessen; Christine Diana Gayen; Ryan David Quarrington; Angela Catherine Walls; Anna Victoria Leonard; Vartan Kurtcuoglu; Claire Frances Jones

doi:10.1186/s12987-022-00401-4

Characterising spinal cerebrospinal fluid flow in the pig with phase-contrast magnetic resonance imaging

Fluids Barriers CNS. 2023 Jan 18;20(1):5. doi: 10.1186/s12987-022-00401-4.

Authors

Madeleine Amy Bessen¹, Christine Diana Gayen^{1

2}, Ryan David Quarrington^{1

3}, Angela Catherine Walls⁴, Anna Victoria Leonard², Vartan Kurtcuoglu^{5

6

7}, Claire Frances Jones^{8

9

10}

Affiliations

¹ Adelaide Spinal Research Group and Centre for Orthopaedics and Trauma Research, Adelaide Medical School, The University of Adelaide, Level 7, Adelaide Health and Medical Sciences Building, The University of Adelaide, North Terrace, Adelaide, SA, 5005, Australia.
² Translational Neuropathology Laboratory, School of Biomedicine, The University of Adelaide, Level 2, Helen Mayo North Building, The University of Adelaide, Frome Road, Adelaide, SA, 5005, Australia.
³ School of Electrical and Mechanical Engineering, The University of Adelaide, North Terrace, Adelaide, SA, 5005, Australia.
⁴ Clinical and Research Imaging Centre, South Australian Health and Medical Research Institute, National Imaging Facility, Northern Pod, SAHMRI, North Terrace, Adelaide, SA, 5000, Australia.
⁵ Institute of Physiology, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.
⁶ Zurich Center for Integrative Human Physiology, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.
⁷ Neuroscience Center Zurich, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.
⁸ Adelaide Spinal Research Group and Centre for Orthopaedics and Trauma Research, Adelaide Medical School, The University of Adelaide, Level 7, Adelaide Health and Medical Sciences Building, The University of Adelaide, North Terrace, Adelaide, SA, 5005, Australia. claire.jones@adelaide.edu.au.
⁹ School of Electrical and Mechanical Engineering, The University of Adelaide, North Terrace, Adelaide, SA, 5005, Australia. claire.jones@adelaide.edu.au.
¹⁰ Department of Orthopaedics, Royal Adelaide Hospital, Adelaide, SA, 5000, Australia. claire.jones@adelaide.edu.au.

Abstract

Background: Detecting changes in pulsatile cerebrospinal fluid (CSF) flow may assist clinical management decisions, but spinal CSF flow is relatively understudied. Traumatic spinal cord injuries (SCI) often cause spinal cord swelling and subarachnoid space (SAS) obstruction, potentially causing pulsatile CSF flow changes. Pigs are emerging as a favoured large animal SCI model; therefore, the aim of this study was to characterise CSF flow along the healthy pig spine.

Methods: Phase-contrast magnetic resonance images (PC-MRI), retrospectively cardiac gated, were acquired for fourteen laterally recumbent, anaesthetised and ventilated, female domestic pigs (22-29 kg). Axial images were obtained at C2/C3, T8/T9, T11/T12 and L1/L2. Dorsal and ventral SAS regions of interest (ROI) were manually segmented. CSF flow and velocity were determined throughout a cardiac cycle. Linear mixed-effects models, with post-hoc comparisons, were used to identify differences in peak systolic/diastolic flow, and maximum velocity (cranial/caudal), across spinal levels and dorsal/ventral SAS. Velocity wave speed from C2/C3 to L1/L2 was calculated.

Results: PC-MRI data were obtained for 11/14 animals. Pulsatile CSF flow was observed at all spinal levels. Peak systolic flow was greater at C2/C3 (dorsal: - 0.32 ± 0.14 mL/s, ventral: - 0.15 ± 0.13 mL/s) than T8/T9 dorsally (- 0.04 ± 0.03 mL/s; p < 0.001), but not different ventrally (- 0.08 ± 0.08 mL/s; p = 0.275), and no difference between thoracolumbar levels (p > 0.05). Peak diastolic flow was greater at C2/C3 (0.29 ± 0.08 mL/s) compared to T8/T9 (0.03 ± 0.03 mL/s, p < 0.001) dorsally, but not different ventrally (p = 1.000). Cranial and caudal maximum velocity at C2/C3 were greater than thoracolumbar levels dorsally (p < 0.001), and T8/T9 and L1/L2 ventrally (p = 0.022). Diastolic velocity wave speed was 1.41 ± 0.39 m/s dorsally and 1.22 ± 0.21 m/s ventrally, and systolic velocity wave speed was 1.02 ± 0.25 m/s dorsally and 0.91 ± 0.22 m/s ventrally.

Conclusions: In anaesthetised and ventilated domestic pigs, spinal CSF has lower pulsatile flow and slower velocity wave propagation, compared to humans. This study provides baseline CSF flow at spinal levels relevant for future SCI research in this animal model.

Keywords: Cerebrospinal fluid; Flow; Phase-contrast magnetic resonance imaging; Pig; Pulsatile; Spine; Velocity.

MeSH terms

Animals
Cerebrospinal Fluid / diagnostic imaging
Cerebrospinal Fluid Pressure*
Female
Humans
Magnetic Resonance Imaging* / methods
Retrospective Studies
Spinal Cord / diagnostic imaging
Sus scrofa
Swine

Abstract

MeSH terms

Grants and funding