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

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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.

ABBREVIATIONS CJV = common jugular vein; CSV = cruciate sulcal vein; ECoG = electrocorticography; ID = inner diameter; IJV = internal jugular vein; IQR = interquartile range; SSS = superior sagittal sinus.

Article Information

Correspondence Thomas J. Oxley, Vascular Bionics Laboratory, Melbourne Brain Centre, Departments of Medicine and Neurology, Royal Melbourne Hospital, The University of Melbourne, Parkville, Victoria 3050, Australia. email: thomas.oxley@unimelb.edu.au.

INCLUDE WHEN CITING Published online April 28, 2017; DOI: 10.3171/2016.11.JNS161754.

Disclosures Dr. Oxley has received support of non–study-related clinical or research effort from Synchron. Dr. Mitchell has received support of non–study-related clinical or research effort from Codman Johnson & Johnson, Stryker, and Medtronic. Dr. Davis has received modest travel support from Boehringer Ingelheim, BMS, Pfizer, and Medtronic; and has received modest honoraria from Boehringer Ingelheim and Medtronic for serving on an advisory board. Drs. Oxley and Opie hold shares in SmartStent Pty, Ltd., and Synchron, Inc.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Ovine cerebral venography. A telescoping coaxial catheter system comprising a sheath and up to 3 catheters was fed over a microwire (B) to navigate the tortuous venous pathway from CJV to SSS. The CJV was exposed via cut-down at the proximal third of the neck (A). Standardized lateral (D) and superior (E) digital subtraction venogram projections were recorded in each animal to record vessel diameters and conduct surgical planning. A native radiograph (C) demonstrates the telescoping catheter system in situ with “J” curve on the leading microwire to reduce trauma. Figure is available in color online only.

  • View in gallery

    Sheep cerebral venography in relation to motor cortex. A sagittal plane MRI slice in the midline (A) demonstrates allocated fiducial points (green dots) along the course of the SSS, commencing at the torcular herophili and separated by 5-mm increments. Box and whisker plots (C) demonstrate the SSS diameters (upper) and distance from motor cortical surface (lower) at each incremental fiducial point along the SSS. Three-dimensional reconstructions of the SSS in a lateral (B) and superior (E) projection of 1 animal are shown, with the corresponding superior projection from digital subtraction venography (D). Graphical representation of the motor cortex from cortical stimulation mapping literature2 demonstrates somatotopic representation of motor function geographically across the superior frontal gyrus (F; red = hind limb, yellow = forelimb, green = head and eyes, purple = face, mouth, and tongue). Reconstruction using MRI images of the cortical surface of an individual sheep brain with superimposed SSS reconstruction demonstrates motor areas in relation to CSVs (F). Figure is available in color online only.

  • View in gallery

    Example of a complication. Before (left) and after (right) a dissection of the origin of the CSV leading to a subdural hemorrhage (arrow) in the frontal lobe bilaterally, shown on a superior projection.

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