J Reconstr Microsurg 2023; 39(06): 435-443
DOI: 10.1055/s-0042-1758186
Original Article

Supercharge End-to-Side Sensory Transfer to A Long Nerve Graft to Enhance Motor Regeneration in A Brachial Plexus Model—An Experimental Rat Study

1   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, Chang Gung University, College of Medicine, Taipei, Taiwan
2   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital; Chang Gung University and Medical College, Taipei, Taiwan
3   Freiburg University Medical Center, Freiburg, Germany
,
Teun Giesen
1   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, Chang Gung University, College of Medicine, Taipei, Taiwan
4   Faculty of Health, Medicine and Life Sciences, University of Maastricht, Maastricht, The Netherlands
,
Johnny Chuieng-Yi Lu
1   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, Chang Gung University, College of Medicine, Taipei, Taiwan
,
Tommy Nai-Jen Chang
1   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, Chang Gung University, College of Medicine, Taipei, Taiwan
,
Abraham Zavala
2   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital; Chang Gung University and Medical College, Taipei, Taiwan
,
1   Department of Plastic and Reconstructive Surgery, Chang Gung Memorial Hospital, Chang Gung University, College of Medicine, Taipei, Taiwan
› Author Affiliations
Funding The study was supported by a grant from the Ministry of Science and Technology Taiwan (MOST 107-2314-B-182A-093). None of the authors have a financial interest in any of the products, devices, or drugs mentioned in this article.

Abstract

Background Long nerve grafts will affect muscle recovery. Aim of this study is to investigate if supercharged end-to-side (SETS) sensory nerve transfer to long nerve graft can enhance functional outcomes in brachial plexus animal model.

Methods A reversed long nerve graft (20–23-mm) was interposed between C6 and musculocutaneous nerve (MCN) in 48 SD rats. The sensory nerves adjacent to the proximal and distal coaptation sites of the nerve graft were used for SETS. There were four groups with 12 rats in each: (A) nerve graft alone, (B) proximal SETS sensory transfer, (C) distal SETS sensory transfer, and (D) combined proximal and distal SETS sensory transfers. Grooming test at 4, 8, 12 and 16 weeks, and compound muscle action potentials (CMAP), biceps tetanic muscle contraction force, muscle weight and MCN axon histomorphologic analysis at 16 weeks were assessed.

Results Grooming test was significantly better in group C and D at 8 weeks (p = 0.02 and p = 0.04) and still superior at 16 weeks. There was no significant difference in CMAP, tetanic muscle contraction force, or muscle weight. The axon counts showed all experimental arms were significantly higher than the unoperated arms. Although the axon count was lowest in group C and highest in group D (p = 0.02), the nerve morphology tended to be better in group C overall.

Conclusion Distal sensory SETS transfer to a long nerve graft showed benefits of functional muscle recovery and better target nerve morphology. Proximal sensory inputs do not benefit the outcomes at all.

Note

This study was presented at the Meeting of the World Society of Reconstructive Microsurgery in Bologna, Italy (WSRM 2019).


Supplementary Material



Publication History

Received: 22 May 2022

Accepted: 17 September 2022

Article published online:
30 November 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Dellon ES, Dellon AL. The first nerve graft, Vulpian, and the nineteenth century neural regeneration controversy. J Hand Surg Am 1993; 18 (02) 369-372
  • 2 Hu CH, Chang TN, Lu JC, Laurence VG, Chuang DC. Comparison of Surgical Strategies between Proximal Nerve Graft and/or Nerve Transfer and Distal Nerve Transfer Based on Functional Restoration of Elbow Flexion: A Retrospective Review of 147 Patients. Plast Reconstr Surg 2018; 141 (01) 68e-79e
  • 3 Chuang DC, Hernon C. Minimum 4-year follow-up on contralateral C7 nerve transfers for brachial plexus injuries. J Hand Surg Am 2012; 37 (02) 270-276
  • 4 Chuang DC, Lu JC, Chang TN, Laurence VG. Comparison of Functional Results After Cross-Face Nerve Graft-, Spinal Accessory Nerve-, and Masseter Nerve-Innervated Gracilis for Facial Paralysis Reconstruction: The Chang Gung Experience. Ann Plast Surg 2018; 81 (6S, Suppl 1) S21-S29
  • 5 Sunderland S, Ray LJ. Denervation changes in mammalian striated muscle. J Neurol Neurosurg Psychiatry 1950; 13 (03) 159-177
  • 6 Jacobs JM, Laing JH, Harrison DH. Regeneration through a long nerve graft used in the correction of facial palsy. A qualitative and quantitative study. Brain 1996; 119 (Pt 1): 271-279
  • 7 Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci 1995; 15 (5 Pt 2): 3886-3895
  • 8 Kanaya F, Tajima T. Effect of electrostimulation on denervated muscle. Clin Orthop Relat Res 1992; (283) 296-301
  • 9 Doyle LM, Roberts BL. Exercise enhances axonal growth and functional recovery in the regenerating spinal cord. Neuroscience 2006; 141 (01) 321-327
  • 10 Abbas OL, Borman H, Uysal CA. et al. Adipose-Derived Stem Cells Enhance Axonal Regeneration through Cross-Facial Nerve Grafting in a Rat Model of Facial Paralysis. Plast Reconstr Surg 2016; 138 (02) 387-396
  • 11 Moore AM, Wood MD, Chenard K. et al. Controlled delivery of glial cell line-derived neurotrophic factor enhances motor nerve regeneration. J Hand Surg Am 2010; 35 (12) 2008-2017
  • 12 Yan Y, Sun HH, Hunter DA, Mackinnon SE, Johnson PJ. Efficacy of short-term FK506 administration on accelerating nerve regeneration. Neurorehabil Neural Repair 2012; 26 (06) 570-580
  • 13 Papakonstantinou KC, Kamin E, Terzis JK. Muscle preservation by prolonged sensory protection. J Reconstr Microsurg 2002; 18 (03) 173-182 , discussion 183–184
  • 14 Terzis JK, Tzafetta K. The “babysitter” procedure: minihypoglossal to facial nerve transfer and cross-facial nerve grafting. Plast Reconstr Surg 2009; 123 (03) 865-876
  • 15 Beck-Broichsitter BE, Becker ST, Lamia A, Fregnan F, Geuna S, Sinis N. Sensoric protection after median nerve injury: babysitter-procedure prevents muscular atrophy and improves neuronal recovery. BioMed Res Int 2014; 2014: 724197
  • 16 Placheta E, Wood MD, Lafontaine C. et al. Enhancement of facial nerve motoneuron regeneration through cross-face nerve grafts by adding end-to-side sensory axons. Plast Reconstr Surg 2015; 135 (02) 460-471
  • 17 Catapano J, Demsey DR, Ho ES, Zuker RM, Borschel GH. Cross-Face Nerve Grafting with Infraorbital Nerve Pathway Protection: Anatomic and Histomorphometric Feasibility Study. Plast Reconstr Surg Glob Open 2016; 4 (09) e1037
  • 18 Cobo JL, Abbate F, de Vicente JC, Cobo J, Vega JA. Searching for proprioceptors in human facial muscles. Neurosci Lett 2017; 640: 1-5
  • 19 Goodmurphy CW, Ovalle WK. Morphological study of two human facial muscles: orbicularis oculi and corrugator supercilii. Clin Anat 1999; 12 (01) 1-11
  • 20 Happak W, Liu J, Burggasser G, Flowers A, Gruber H, Freilinger G. Human facial muscles: dimensions, motor endplate distribution, and presence of muscle fibers with multiple motor endplates. Anat Rec 1997; 249 (02) 276-284
  • 21 McGrath AM, Lu JC, Chang TN, Fang F, Chuang DC. Proximal versus Distal Nerve Transfer for Biceps Reinnervation-A Comparative Study in a Rat's Brachial Plexus Injury Model. Plast Reconstr Surg Glob Open 2016; 4 (12) e1130
  • 22 Hayashi A, Moradzadeh A, Hunter DA. et al. Retrograde labeling in peripheral nerve research: it is not all black and white. J Reconstr Microsurg 2007; 23 (07) 381-389
  • 23 Popratiloff AS, Neiss WF, Skouras E, Streppel M, Guntinas-Lichius O, Angelov DN. Evaluation of muscle re-innervation employing pre- and post-axotomy injections of fluorescent retrograde tracers. Brain Res Bull 2001; 54 (01) 115-123
  • 24 Bertelli JA, Taleb M, Saadi A, Mira JC, Pecot-Dechavassine M. The rat brachial plexus and its terminal branches: an experimental model for the study of peripheral nerve regeneration. Microsurgery 1995; 16 (02) 77-85
  • 25 Terzis JK, Sweet RC, Dykes RW, Williams HB. Recovery of function in free muscle transplants using microneurovascular anastomoses. J Hand Surg Am 1978; 3 (01) 37-59
  • 26 Schindelin J, Arganda-Carreras I, Frise E. et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9 (07) 676-682
  • 27 Engelmann S, Ruewe M, Geis S. et al. Rapid and Precise Semi-Automatic Axon Quantification in Human Peripheral Nerves. Sci Rep 2020; 10 (01) 1935
  • 28 Viterbo F, Trindade JC, Hoshino K, Mazzoni Neto A. Latero-terminal neurorrhaphy without removal of the epineural sheath. Experimental study in rats. Rev Paul Med 1992; 110 (06) 267-275
  • 29 Isaacs J, Allen D, Chen LE, Nunley II J. Reverse end-to-side neurotization. J Reconstr Microsurg 2005; 21 (01) 43-48 , discussion 49–50
  • 30 Fujiwara T, Matsuda K, Kubo T. et al. Axonal supercharging technique using reverse end-to-side neurorrhaphy in peripheral nerve repair: an experimental study in the rat model. J Neurosurg 2007; 107 (04) 821-829
  • 31 Farber SJ, Glaus SW, Moore AM, Hunter DA, Mackinnon SE, Johnson PJ. Supercharge nerve transfer to enhance motor recovery: a laboratory study. J Hand Surg Am 2013; 38 (03) 466-477
  • 32 Brushart T, Kebaish F, Wolinsky R, Skolasky R, Li Z, Barker N. Sensory axons inhibit motor axon regeneration in vitro. Exp Neurol 2020; 323: 113073
  • 33 van Neerven SG, Bozkurt A, O'Dey DM. et al. Retrograde tracing and toe spreading after experimental autologous nerve transplantation and crush injury of the sciatic nerve: a descriptive methodological study. J Brachial Plex Peripher Nerve Inj 2012; 7 (01) 5
  • 34 Zavala A, Lu JCY, Chang TNJ. et al. Supercharge End-to-Side Motor Transfer to a Long Nerve Graft to Enhance Motor Regeneration: An Experimental Rat Study. Plast Reconstr Surg 2021