Proof of concept for multiple nerve transfers to a single target muscle

  1. Matthias Luft
  2. Johanna Klepetko
  3. Silvia Muceli
  4. Jaime Ibáñez
  5. Vlad Tereshenko
  6. Christopher Festin
  7. Gregor Laengle
  8. Olga Politikou
  9. Udo Maierhofer
  10. Dario Farina
  11. Oskar C Aszmann
  12. Konstantin Davide Bergmeister  Is a corresponding author
  1. Medical University of Vienna, Austria
  2. Chalmers University of Technology, Sweden
  3. Imperial College London, United Kingdom
  4. Karl Landsteiner University of Health Sciences, Austria

Abstract

Surgical nerve transfers are used to efficiently treat peripheral nerve injuries, neuromas, phantom limb pain or improve bionic prosthetic control. Commonly, one donor nerve is transferred to one target muscle. However, the transfer of multiple nerves onto a single target muscle may increase the number of muscle signals for myoelectric prosthetic control and facilitate the treatment of multiple neuromas. Currently, no experimental models are available for multiple nerve transfers to a common target muscle in the upper extremity. This study describes a novel experimental model to investigate the neurophysiological effects of peripheral double nerve transfers. For this purpose, we developed a forelimb model to enable tension-free transfer of one or two donor nerves in the upper extremity. Anatomic dissections were performed to design the double nerve transfer model (n=8). In 62 male Sprague-Dawley rats the ulnar nerve of the antebrachium alone (n=30) or together with the anterior interosseus nerve (n=32) was transferred to reinnervate the long head of the biceps brachii. Before neurotization, the motor branch to the biceps’ long head was transected at the motor entry point and resected up to its original branch to prevent auto-reinnervation. In all animals, coaptation of both nerves to the motor entry point could be performed tension-free. Mean duration of the procedure was 49 ± 13 min for the single nerve transfer and 78 ± 20 min for the double nerve transfer. Twelve weeks after surgery, muscle response to neurotomy, behavioral testing, retrograde labeling and structural analyses were performed to assess reinnervation. These analyses indicated that all nerves successfully reinnervated the target muscle. No aberrant reinnervation was observed by the originally innervating nerve. Our observations suggest a minimal burden for the animal with no signs of functional deficit in daily activities or auto-mutilation in both procedures. Furthermore, standard neurophysiological analyses for nerve and muscle regeneration were applicable. This newly developed nerve transfer model allows for the reliable and standardized investigation of neural and functional changes following the transfer of multiple donor nerves to one target muscle.

Data availability

Muscle mass data have been deposited in Dryad under the DOI: https://doi.org/10.5061/dryad.3j9kd51jb.Retrograde labeling data has been deposited in Dryad under the DOI: https://doi.org/10.5061/dryad.6q573n60c.

The following data sets were generated

Article and author information

Author details

  1. Matthias Luft

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9161-4125
  2. Johanna Klepetko

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Silvia Muceli

    Department of Electrical Engineering, Chalmers University of Technology, Gothenburg, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0310-1021
  4. Jaime Ibáñez

    Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Vlad Tereshenko

    Clinical Laboratory for Bionic Extremity Reconstruction, Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7761-5191
  6. Christopher Festin

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  7. Gregor Laengle

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1011-3482
  8. Olga Politikou

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  9. Udo Maierhofer

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  10. Dario Farina

    Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7883-2697
  11. Oskar C Aszmann

    Department of Plastic, Reconstructive and Aesthetic Surgery, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  12. Konstantin Davide Bergmeister

    Karl Landsteiner University of Health Sciences, St. Poelten, Austria
    For correspondence
    kbergmeister@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3910-9727

Funding

European Research Council (ERC Synergy Grant: No 810346)

  • Matthias Luft
  • Vlad Tereshenko
  • Christopher Festin
  • Gregor Laengle
  • Olga Politikou
  • Udo Maierhofer
  • Dario Farina
  • Oskar C Aszmann
  • Konstantin Davide Bergmeister

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The protocols for the experiments were approved by the ethics committee of the Medical University of Vienna and the Austrian Ministry for Research and Science (reference number BMBWF- 66.009/0413-V/3b/2019) and strictly followed the principles of laboratory animal care as recommended by the Federation of European Laboratory Animal Science Associations (FELASA).

Reviewing Editor

  1. Samantha R Santacruz, The University of Texas at Austin, United States

Publication history

  1. Received: June 16, 2021
  2. Preprint posted: July 10, 2021 (view preprint)
  3. Accepted: September 30, 2021
  4. Accepted Manuscript published: October 1, 2021 (version 1)
  5. Version of Record published: October 21, 2021 (version 2)

Copyright

© 2021, Luft et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Matthias Luft
  2. Johanna Klepetko
  3. Silvia Muceli
  4. Jaime Ibáñez
  5. Vlad Tereshenko
  6. Christopher Festin
  7. Gregor Laengle
  8. Olga Politikou
  9. Udo Maierhofer
  10. Dario Farina
  11. Oskar C Aszmann
  12. Konstantin Davide Bergmeister
(2021)
Proof of concept for multiple nerve transfers to a single target muscle
eLife 10:e71312.
https://doi.org/10.7554/eLife.71312

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