An ovine model of cerebral catheter venography for implantation of an endovascular neural interface

Thomas James Oxley, Nicholas Lachlan Opie, Gil Simon Rind, Kishan Liyanage, Sam Emmanuel John, Stephen Ronayne, Alan James McDonald, Anthony Dornom, Timothy John Haynes Lovell, Peter John Mitchell, Iwan Bennett, Sebastien Bauquier, Leon Norris Warne, Chris Steward, David Bruce Grayden, Patricia Desmond, Stephen M. Davis, Terence John O'Brien, Clive N. May

Research output: Contribution to journalArticleResearchpeer-review

7 Citations (Scopus)

Abstract

OBJECTIVE Neural interface technology may enable the development of novel therapies to treat neurological conditions, including motor prostheses for spinal cord injury. Intracranial neural interfaces currently require a craniotomy to achieve implantation and may result in chronic tissue inflammation. Novel approaches are required that achieve less invasive implantation methods while maintaining high spatial resolution. An endovascular stent electrode array avoids direct brain trauma and is able to record electrocorticography in local cortical tissue from within the venous vasculature. The motor area in sheep runs in a parasagittal plane immediately adjacent to the superior sagittal sinus (SSS). The authors aimed to develop a sheep model of cerebral venography that would enable validation of an endovascular neural interface. METHODS Cerebral catheter venography was performed in 39 consecutive sheep. Contrast-enhanced MRI of the brain was performed on 13 animals. Multiple telescoping coaxial catheter systems were assessed to determine the largest wide-bore delivery catheter that could be delivered into the anterior SSS. Measurements of SSS diameter and distance from the motor area were taken. The location of the motor area was determined in relation to lateral and superior projections of digital subtraction venography images and confirmed on MRI. RESULTS The venous pathway from the common jugular vein (7.4 mm) to the anterior SSS (1.2 mm) was technically challenging to selectively catheterize. The SSS coursed immediately adjacent to the motor cortex (< 1 mm) for a length of 40 mm, or the anterior half of the SSS. Attempted access with 5-Fr and 6-Fr delivery catheters was associated with longer procedure times and higher complication rates. A 4-Fr catheter (internal lumen diameter 1.1 mm) was successful in accessing the SSS in 100% of cases with no associated complications. Complications included procedure-related venous dissection in two major areas: the torcular herophili, and the anterior formation of the SSS. The bifurcation of the cruciate sulcal veins with the SSS was a reliable predictor of the commencement of the motor area. CONCLUSIONS The ovine model for cerebral catheter venography has generalizability to the human cerebral venous system in relation to motor cortex location. This novel model may facilitate the development of the novel field of endovascular neural interfaces that may include preclinical investigations for cortical recording applications such as paralysis and epilepsy, as well as other potential applications in neuromodulation.

Original languageEnglish
Pages (from-to)1020-1027
Number of pages8
JournalJournal of Neurosurgery
Volume128
Issue number4
DOIs
Publication statusPublished - 1 Apr 2018
Externally publishedYes

Keywords

  • Brain-machine interface
  • Catheter
  • Cerebral venography
  • Motor cortex
  • Neural interface
  • Ovine
  • Sheep
  • Vascular disorders

Cite this

Oxley, T. J., Opie, N. L., Rind, G. S., Liyanage, K., John, S. E., Ronayne, S., ... May, C. N. (2018). An ovine model of cerebral catheter venography for implantation of an endovascular neural interface. Journal of Neurosurgery, 128(4), 1020-1027. https://doi.org/10.3171/2016.11.JNS161754
Oxley, Thomas James ; Opie, Nicholas Lachlan ; Rind, Gil Simon ; Liyanage, Kishan ; John, Sam Emmanuel ; Ronayne, Stephen ; McDonald, Alan James ; Dornom, Anthony ; Lovell, Timothy John Haynes ; Mitchell, Peter John ; Bennett, Iwan ; Bauquier, Sebastien ; Warne, Leon Norris ; Steward, Chris ; Grayden, David Bruce ; Desmond, Patricia ; Davis, Stephen M. ; O'Brien, Terence John ; May, Clive N. / An ovine model of cerebral catheter venography for implantation of an endovascular neural interface. In: Journal of Neurosurgery. 2018 ; Vol. 128, No. 4. pp. 1020-1027.
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title = "An ovine model of cerebral catheter venography for implantation of an endovascular neural interface",
abstract = "OBJECTIVE Neural interface technology may enable the development of novel therapies to treat neurological conditions, including motor prostheses for spinal cord injury. Intracranial neural interfaces currently require a craniotomy to achieve implantation and may result in chronic tissue inflammation. Novel approaches are required that achieve less invasive implantation methods while maintaining high spatial resolution. An endovascular stent electrode array avoids direct brain trauma and is able to record electrocorticography in local cortical tissue from within the venous vasculature. The motor area in sheep runs in a parasagittal plane immediately adjacent to the superior sagittal sinus (SSS). The authors aimed to develop a sheep model of cerebral venography that would enable validation of an endovascular neural interface. METHODS Cerebral catheter venography was performed in 39 consecutive sheep. Contrast-enhanced MRI of the brain was performed on 13 animals. Multiple telescoping coaxial catheter systems were assessed to determine the largest wide-bore delivery catheter that could be delivered into the anterior SSS. Measurements of SSS diameter and distance from the motor area were taken. The location of the motor area was determined in relation to lateral and superior projections of digital subtraction venography images and confirmed on MRI. RESULTS The venous pathway from the common jugular vein (7.4 mm) to the anterior SSS (1.2 mm) was technically challenging to selectively catheterize. The SSS coursed immediately adjacent to the motor cortex (< 1 mm) for a length of 40 mm, or the anterior half of the SSS. Attempted access with 5-Fr and 6-Fr delivery catheters was associated with longer procedure times and higher complication rates. A 4-Fr catheter (internal lumen diameter 1.1 mm) was successful in accessing the SSS in 100{\%} of cases with no associated complications. Complications included procedure-related venous dissection in two major areas: the torcular herophili, and the anterior formation of the SSS. The bifurcation of the cruciate sulcal veins with the SSS was a reliable predictor of the commencement of the motor area. CONCLUSIONS The ovine model for cerebral catheter venography has generalizability to the human cerebral venous system in relation to motor cortex location. This novel model may facilitate the development of the novel field of endovascular neural interfaces that may include preclinical investigations for cortical recording applications such as paralysis and epilepsy, as well as other potential applications in neuromodulation.",
keywords = "Brain-machine interface, Catheter, Cerebral venography, Motor cortex, Neural interface, Ovine, Sheep, Vascular disorders",
author = "Oxley, {Thomas James} and Opie, {Nicholas Lachlan} and Rind, {Gil Simon} and Kishan Liyanage and John, {Sam Emmanuel} and Stephen Ronayne and McDonald, {Alan James} and Anthony Dornom and Lovell, {Timothy John Haynes} and Mitchell, {Peter John} and Iwan Bennett and Sebastien Bauquier and Warne, {Leon Norris} and Chris Steward and Grayden, {David Bruce} and Patricia Desmond and Davis, {Stephen M.} and O'Brien, {Terence John} and May, {Clive N.}",
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Oxley, TJ, Opie, NL, Rind, GS, Liyanage, K, John, SE, Ronayne, S, McDonald, AJ, Dornom, A, Lovell, TJH, Mitchell, PJ, Bennett, I, Bauquier, S, Warne, LN, Steward, C, Grayden, DB, Desmond, P, Davis, SM, O'Brien, TJ & May, CN 2018, 'An ovine model of cerebral catheter venography for implantation of an endovascular neural interface', Journal of Neurosurgery, vol. 128, no. 4, pp. 1020-1027. https://doi.org/10.3171/2016.11.JNS161754

An ovine model of cerebral catheter venography for implantation of an endovascular neural interface. / Oxley, Thomas James; Opie, Nicholas Lachlan; Rind, Gil Simon; Liyanage, Kishan; John, Sam Emmanuel; Ronayne, Stephen; McDonald, Alan James; Dornom, Anthony; Lovell, Timothy John Haynes; Mitchell, Peter John; Bennett, Iwan; Bauquier, Sebastien; Warne, Leon Norris; Steward, Chris; Grayden, David Bruce; Desmond, Patricia; Davis, Stephen M.; O'Brien, Terence John; May, Clive N.

In: Journal of Neurosurgery, Vol. 128, No. 4, 01.04.2018, p. 1020-1027.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - An ovine model of cerebral catheter venography for implantation of an endovascular neural interface

AU - Oxley, Thomas James

AU - Opie, Nicholas Lachlan

AU - Rind, Gil Simon

AU - Liyanage, Kishan

AU - John, Sam Emmanuel

AU - Ronayne, Stephen

AU - McDonald, Alan James

AU - Dornom, Anthony

AU - Lovell, Timothy John Haynes

AU - Mitchell, Peter John

AU - Bennett, Iwan

AU - Bauquier, Sebastien

AU - Warne, Leon Norris

AU - Steward, Chris

AU - Grayden, David Bruce

AU - Desmond, Patricia

AU - Davis, Stephen M.

AU - O'Brien, Terence John

AU - May, Clive N.

PY - 2018/4/1

Y1 - 2018/4/1

N2 - OBJECTIVE Neural interface technology may enable the development of novel therapies to treat neurological conditions, including motor prostheses for spinal cord injury. Intracranial neural interfaces currently require a craniotomy to achieve implantation and may result in chronic tissue inflammation. Novel approaches are required that achieve less invasive implantation methods while maintaining high spatial resolution. An endovascular stent electrode array avoids direct brain trauma and is able to record electrocorticography in local cortical tissue from within the venous vasculature. The motor area in sheep runs in a parasagittal plane immediately adjacent to the superior sagittal sinus (SSS). The authors aimed to develop a sheep model of cerebral venography that would enable validation of an endovascular neural interface. METHODS Cerebral catheter venography was performed in 39 consecutive sheep. Contrast-enhanced MRI of the brain was performed on 13 animals. Multiple telescoping coaxial catheter systems were assessed to determine the largest wide-bore delivery catheter that could be delivered into the anterior SSS. Measurements of SSS diameter and distance from the motor area were taken. The location of the motor area was determined in relation to lateral and superior projections of digital subtraction venography images and confirmed on MRI. RESULTS The venous pathway from the common jugular vein (7.4 mm) to the anterior SSS (1.2 mm) was technically challenging to selectively catheterize. The SSS coursed immediately adjacent to the motor cortex (< 1 mm) for a length of 40 mm, or the anterior half of the SSS. Attempted access with 5-Fr and 6-Fr delivery catheters was associated with longer procedure times and higher complication rates. A 4-Fr catheter (internal lumen diameter 1.1 mm) was successful in accessing the SSS in 100% of cases with no associated complications. Complications included procedure-related venous dissection in two major areas: the torcular herophili, and the anterior formation of the SSS. The bifurcation of the cruciate sulcal veins with the SSS was a reliable predictor of the commencement of the motor area. CONCLUSIONS The ovine model for cerebral catheter venography has generalizability to the human cerebral venous system in relation to motor cortex location. This novel model may facilitate the development of the novel field of endovascular neural interfaces that may include preclinical investigations for cortical recording applications such as paralysis and epilepsy, as well as other potential applications in neuromodulation.

AB - OBJECTIVE Neural interface technology may enable the development of novel therapies to treat neurological conditions, including motor prostheses for spinal cord injury. Intracranial neural interfaces currently require a craniotomy to achieve implantation and may result in chronic tissue inflammation. Novel approaches are required that achieve less invasive implantation methods while maintaining high spatial resolution. An endovascular stent electrode array avoids direct brain trauma and is able to record electrocorticography in local cortical tissue from within the venous vasculature. The motor area in sheep runs in a parasagittal plane immediately adjacent to the superior sagittal sinus (SSS). The authors aimed to develop a sheep model of cerebral venography that would enable validation of an endovascular neural interface. METHODS Cerebral catheter venography was performed in 39 consecutive sheep. Contrast-enhanced MRI of the brain was performed on 13 animals. Multiple telescoping coaxial catheter systems were assessed to determine the largest wide-bore delivery catheter that could be delivered into the anterior SSS. Measurements of SSS diameter and distance from the motor area were taken. The location of the motor area was determined in relation to lateral and superior projections of digital subtraction venography images and confirmed on MRI. RESULTS The venous pathway from the common jugular vein (7.4 mm) to the anterior SSS (1.2 mm) was technically challenging to selectively catheterize. The SSS coursed immediately adjacent to the motor cortex (< 1 mm) for a length of 40 mm, or the anterior half of the SSS. Attempted access with 5-Fr and 6-Fr delivery catheters was associated with longer procedure times and higher complication rates. A 4-Fr catheter (internal lumen diameter 1.1 mm) was successful in accessing the SSS in 100% of cases with no associated complications. Complications included procedure-related venous dissection in two major areas: the torcular herophili, and the anterior formation of the SSS. The bifurcation of the cruciate sulcal veins with the SSS was a reliable predictor of the commencement of the motor area. CONCLUSIONS The ovine model for cerebral catheter venography has generalizability to the human cerebral venous system in relation to motor cortex location. This novel model may facilitate the development of the novel field of endovascular neural interfaces that may include preclinical investigations for cortical recording applications such as paralysis and epilepsy, as well as other potential applications in neuromodulation.

KW - Brain-machine interface

KW - Catheter

KW - Cerebral venography

KW - Motor cortex

KW - Neural interface

KW - Ovine

KW - Sheep

KW - Vascular disorders

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