Essential neural anatomy for creating a clinically translatable osseointegrated neural interface for prosthetic control in sheep

Abstract

Aim: Ovine models for osseointegrated prosthetics research are well established, but do not consider neural control of advanced prostheses. The validity of interfacing technologies, such as the Osseointegrated Neural Interface (ONI), in their ability to provide communication between native nerves and advanced prosthetics is required, necessitating a stable, longitudinal large animal model for testing. The objective of this study is to provide a detailed anatomic description of the major nerves distal to the carpal and tarsal joints, informing the creation of a chronic ONI for prosthetic control in sheep.

Methods: Six pelvic and six thoracic cadaveric limbs from mature female, non-lactating sheep were utilized. Radiographs were obtained to determine average bone length, medullary canal diameter, and cortical bone thickness. Microsurgical dissection was performed to discern topographical neuroanatomy and average circumferences of the major nerves of the pelvic and thoracic limbs. Histologic analysis was performed. A surgical approach for the creation of ONI was designed.

Results: Average metacarpal and metatarsal length was 15.0 cm (± 0.0) and 19.7 cm (± 1.0), respectively. Average intramedullary canal diameter was 12.91 mm (± 3.69) for forelimbs and 12.60 mm (± 3.69) for hindlimbs. The thoracic limb nerves consisted of one dorsal and three ventral nerves, with an average circumference of 5.14 mm (± 2.00) and 5.05 mm (± 1.06), respectively. Pelvic limb nerves consisted of two dorsal and one ventral nerve with an average circumference of 6.27 mm (± 1.79) and 5.40 mm (± 0.53), respectively.

Conclusions: These anatomic data inform the surgical approach and manufacture of a sensory ONI for chronic testing in awake, freely ambulating animals for future clinical translation.

Keywords

Amputation / prosthesis / prostheses / neural interface / clinical translation / large animal / osseointegration / neuroprosthesis

References

[1] Millevolte AXT,Ness JP.Improving the selectivity of an osseointegrated neural interface: proof of concept for housing sieve electrode arrays in the medullary canal of long bones.Front Neurosci2021;15:613844 PMCID:PMC8006940

[2] Karczewski AM,Poore SO.The need to work arm in arm: calling for collaboration in delivering neuroprosthetic limb replacements.Front Neurorobot2021;15:711028 PMCID:PMC8334559

[3] Dingle AM,Novello J.Methodology for creating a chronic osseointegrated neural interface for prosthetic control in rabbits.J Neurosci Methods2020;331:108504

[4] Dingle AM,Novello J.Experimental basis for creating an osseointegrated neural interface for prosthetic control: a pilot study in rabbits.Mil Med2020;185:462-9

[5] Aman M,Festin C.Experimental testing of bionic peripheral nerve and muscle interfaces: animal model considerations.Front Neurosci2020;13:1422 PMCID:PMC7025572

[6] Clites TR,Srinivasan SS,Brånemark R.Caprine models of the agonist-antagonist myoneural interface implemented at the above- and below-knee amputation levels.Plast Reconstr Surg2019;144:p 218e-229e.

[7] Jeyapalina S,Agarwal J.A 24-month evaluation of a percutaneous osseointegrated limb-skin interface in an ovine amputation model.J Mater Sci Mater Med2017;28:179

[8] Jeyapalina S,Drew A,Bachus KN.Variation in bone response to the placement of percutaneous osseointegrated endoprostheses: a 24-month follow-up in sheep.PLoS One2019;14:e0221850 PMCID:PMC6814231

[9] Hoellwarth JS,Rozbruch SR,Coughlan A.Osseointegration for amputees: current implants, techniques, and future directions.JBJS Rev2020;8:e0043 PMCID:PMC7161721

[10] Shelton TJ,Bloebaum RD.Percutaneous osseointegrated prostheses for amputees: limb compensation in a 12-month ovine model.J Biomech2011;44:2601-6 PMCID:PMC3190641

[11] Sartoretto SC,Miguel FB,Ascoli F.Sheep as an experimental model for biomaterial implant evaluation.Acta Ortop Bras2016;24:262-6 PMCID:PMC5266658

[12] Karczewski AM,Stratchko LM,Poore SO.Clinical basis for creating an osseointegrated neural interface.Front Neurosci2022;16:828593 PMCID:PMC9039253

[13] Settell ML,Knudsen BE.Functional vagotopy in the cervical vagus nerve of the domestic pig: implications for the study of vagus nerve stimulation.J Neural Eng2020;17:026022 PMCID:PMC7306215

[14] Blanz SL,Settell ML.Spatially selective stimulation of the pig vagus nerve to modulate target effect versus side effect.J Neural Eng2023;20:016051 PMCID:PMC10339030

[15] Jeyapalina S,Bachus KN,Bloebaum RD.Radiographic evaluation of bone adaptation adjacent to percutaneous osseointegrated prostheses in a sheep model.Clin Orthop Relat Res2014;472:2966-77 PMCID:PMC4160482

[16] Duda GN,Sokiranski R,Miller R.Analysis of inter-fragmentary movement as a function of musculoskeletal loading conditions in sheep.J Biomech1998;31:201-10

[17] Grisez BT,Boukhemis KW,Lindsey BA.Osseointegrated transcutaneous device for amputees: a pilot large animal model.Adv Orthop2018;2018:4625967 PMCID:PMC6158950

[18] Schuurman SO,Weijs WA.The equine hind limb is actively stabilized during standing.J Anat2003;202:355-62 PMCID:PMC1571089

[19] Welsh PJ,Clement HM,Mason JB.Cranial Cruciate ligament desmotomies in sheep resulting in peroneus tertius injury.Case Rep Vet Med2021;2021:2628791 PMCID:PMC8324369