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In vivo visualization of pig vagus nerve ‘vagotopy’ using ultrasound

View ORCID ProfileMegan L. Settell, View ORCID ProfileMaïsha Kasole, Aaron C. Skubal, View ORCID ProfileBruce E. Knudsen, View ORCID ProfileEvan N. Nicolai, View ORCID ProfileChengwu Huang, View ORCID ProfileChenyun Zhou, View ORCID ProfileJames K. Trevathan, Aniruddha Upadhye, View ORCID ProfileChaitanya Kolluru, View ORCID ProfileAndrew J. Shoffstall, Justin C. Williams, View ORCID ProfileAaron J. Suminski, View ORCID ProfileWarren M. Grill, View ORCID ProfileNicole A. Pelot, Shigao Chen, View ORCID ProfileKip A. Ludwig
doi: https://doi.org/10.1101/2020.12.24.424256
Megan L. Settell
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
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Maïsha Kasole
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
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Aaron C. Skubal
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
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Bruce E. Knudsen
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
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Evan N. Nicolai
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
3Mayo Clinic, Mayo Clinic Graduate School of Biomedical Sciences, Rochester, MN, USA
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Chengwu Huang
4Mayo Clinic, Department of Radiology, Rochester, MN, USA
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Chenyun Zhou
4Mayo Clinic, Department of Radiology, Rochester, MN, USA
5West China Hospital of Sichuan University, Department of Ultrasound, Chengdu, Sichuan, China
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James K. Trevathan
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
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Aniruddha Upadhye
10Case Western Reserve University, Department of Biomedical Engineering, Cleveland, OH, USA
11Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA
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Chaitanya Kolluru
10Case Western Reserve University, Department of Biomedical Engineering, Cleveland, OH, USA
11Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA
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Andrew J. Shoffstall
10Case Western Reserve University, Department of Biomedical Engineering, Cleveland, OH, USA
11Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA
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Justin C. Williams
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
2University of Wisconsin-Madison, Department of Neurosurgery, Madison, WI, USA
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Aaron J. Suminski
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
2University of Wisconsin-Madison, Department of Neurosurgery, Madison, WI, USA
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Warren M. Grill
6Duke University, Department of Biomedical Engineering, Durham, NC, USA
7Duke University, Department of Electrical and Computer Engineering, Durham, NC, USA
8Duke University, Department of Neurobiology, Durham, NC, USA
9Duke University, Department of Neurosurgery, Durham, NC, USA
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Nicole A. Pelot
6Duke University, Department of Biomedical Engineering, Durham, NC, USA
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Shigao Chen
4Mayo Clinic, Department of Radiology, Rochester, MN, USA
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  • For correspondence: Kip.ludwig@wisc.edu Chen.shigao@mayo.edu
Kip A. Ludwig
1University of Wisconsin-Madison, Department of Biomedical Engineering, Madison, WI, USA
2University of Wisconsin-Madison, Department of Neurosurgery, Madison, WI, USA
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  • For correspondence: Kip.ludwig@wisc.edu Chen.shigao@mayo.edu
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Abstract

Background Placement of the clinical vagus nerve stimulating cuff is a standard surgical procedure based on anatomical landmarks, with limited patient specificity in terms of fascicular organization or vagal anatomy. As such, the therapeutic effects are generally limited by unwanted side effects of neck muscle contractions, demonstrated by previous studies to result from stimulation of 1) motor fibers near the cuff in the superior laryngeal and 2) motor fibers within the cuff projecting to the recurrent laryngeal.

Objective The use of patient-specific visualization of vagus nerve fascicular organization could better inform clinical cuff placement and improve clinical outcomes.

Methods The viability of ultrasound, with the transducer in the surgical pocket, to visualize vagus nerve fascicular organization (i.e. vagotopy) was characterized in a pig model. Ultrasound images were matched to post-mortem histology to confirm the utility of ultrasound in identifying fascicular organization.

Results High-resolution ultrasound accurately depicted the vagotopy of the pig vagus nerve intra-operatively, as confirmed via histology. The stereotypical pseudo-unipolar cell body aggregation at the nodose ganglion was identifiable, and these sensory afferent fascicular bundles were traced down the length of the vagus nerve. Additionally, the superior and recurrent laryngeal nerves were identified via ultrasound.

Conclusions Intraoperative visualization of vagotopy and surrounding nerves using ultrasound is a novel approach to optimize stimulating cuff placement, avoid unwanted activation of motor nerve fibers implicated in off-target effects, and seed patient-specific models of vagal fiber activation to improve patient outcomes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This manuscript has been revised to update several figures, and text throughout.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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In vivo visualization of pig vagus nerve ‘vagotopy’ using ultrasound
Megan L. Settell, Maïsha Kasole, Aaron C. Skubal, Bruce E. Knudsen, Evan N. Nicolai, Chengwu Huang, Chenyun Zhou, James K. Trevathan, Aniruddha Upadhye, Chaitanya Kolluru, Andrew J. Shoffstall, Justin C. Williams, Aaron J. Suminski, Warren M. Grill, Nicole A. Pelot, Shigao Chen, Kip A. Ludwig
bioRxiv 2020.12.24.424256; doi: https://doi.org/10.1101/2020.12.24.424256
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In vivo visualization of pig vagus nerve ‘vagotopy’ using ultrasound
Megan L. Settell, Maïsha Kasole, Aaron C. Skubal, Bruce E. Knudsen, Evan N. Nicolai, Chengwu Huang, Chenyun Zhou, James K. Trevathan, Aniruddha Upadhye, Chaitanya Kolluru, Andrew J. Shoffstall, Justin C. Williams, Aaron J. Suminski, Warren M. Grill, Nicole A. Pelot, Shigao Chen, Kip A. Ludwig
bioRxiv 2020.12.24.424256; doi: https://doi.org/10.1101/2020.12.24.424256

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