Enhancement of facial nerve motoneuron regeneration through cross-face nerve grafts by adding end-to-side sensory axons

Plastic and Reconstructive Surgery

Volumn 135, Issue 2, 2015, Pages 460-471

  Placheta, Eva ^a   Wood, Matthew D ^a   Lafontaine, Christine ^a   Liu, Edward H ^a   Hendry, J Michael ^a   Angelov, Doychin N ^a   Frey, Manfred ^a   Gordon, Tessa ^a   Borschel, Gregory H ^b  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG ANALYSIS; GREEN FLUORESCENT PROTEIN; NERVE GROWTH FACTOR;

ANIMAL; BRAIN STEM; FACE MUSCLE; FACIAL EXPRESSION; FACIAL NERVE; HETEROTOPIC TRANSPLANTATION; INJURIES; INNERVATION; MANDIBULAR NERVE; MOTONEURON; MOTOR CORTEX; MUSCLE DENERVATION; MYELINATED NERVE; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE REGENERATION; PATHOLOGY; PERONEUS NERVE; PHYSIOLOGY; RAT; REPORTER GENE; RETROGRADE DEGENERATION; SECRETION (PROCESS); SENSORY NERVE CELL; SPINAL GANGLION; SPRAGUE DAWLEY RAT; SURGERY; TRANSGENIC RAT; TRANSPLANTATION; ULTRASTRUCTURE; VIBRISSA;

ANALYSIS; ANIMALS; AXONS; AXOTOMY; BRAIN STEM; FACIAL EXPRESSION; FACIAL MUSCLES; FACIAL NERVE; GANGLIA, SPINAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; INJURIES; INNERVATION; MANDIBULAR NERVE; MOTOR CORTEX; MOTOR NEURONS; MUSCLE DENERVATION; NERVE FIBERS, MYELINATED; NERVE GROWTH FACTORS; NERVE REGENERATION; PATHOLOGY; PERONEAL NERVE; PHYSIOLOGY; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RETROGRADE DEGENERATION; SECRETION; SENSORY RECEPTOR CELLS; SURGERY; TRANSPLANTATION; TRANSPLANTATION, HETEROTOPIC; ULTRASTRUCTURE; VIBRISSAE;

EID: 84964255470     PISSN: 00321052     EISSN: None     Source Type: Journal    
DOI: 10.1097/PRS.0000000000000893     Document Type: Conference Paper

References (69)

1. Valls-Solé J, Montero J. Movement disorders in patients with peripheral facial palsy. Mov Disord. 2003;18:1424-1435.
2. Beurskens CH, Heymans PG. Physiotherapy in patients with facial nerve paresis: Description of outcomes. Am J Otolaryngol. 2004;25:394-400.
3. Hadlock TA, Greenfield LJ, Wernick-Robinson M, Cheney ML. Multimodality approach to management of the paralyzed face. Laryngoscope 2006;116:1385-1389.
4. Frey M, Giovanoli P. The three-stage concept to optimize the results of microsurgical reanimation of the paralyzed face. Clin Plast Surg. 2002;29:461-482.
5. Fattah A, Borschel GH, Manktelow RT, Bezuhly M, Zuker RM. Facial palsy and reconstruction. Plast Reconstr Surg. 2012;129:340e-352e.
6. Frey M, Giovanoli P, Michaelidou M. Functional upgrading of partially recovered facial palsy by cross-face nerve grafting with distal end-to-side neurorrhaphy. Plast Reconstr Surg. 2006;117:597-608.
7. Anderl H. Cross-face nerve transplant. Clin Plast Surg. 1979;6:433-449.
8. Freilinger G. A new technique to correct facial paralysis. Plast Reconstr Surg. 1975;56:44-48.
9. Manktelow RT, Zuker RM. Muscle transplantation by fascicular territory. Plast Reconstr Surg. 1984;73:751-757.
10. Frey M, Michaelidou M, Tzou CH, et al. Three-dimensional video analysis of the paralyzed face reanimated by crossface nerve grafting and free gracilis muscle transplantation: Quantification of the functional outcome. Plast Reconstr Surg. 2008;122:1709-1722.
11. Frey M, Michaelidou M, Tzou CH, Hold A, Pona I, Placheta E. Proven and innovative operative techniques for reanimation of the paralyzed face (in German). Handchir Mikrochir Plast Chir. 2010;42:81-89.
12. Braam MJ, Nicolai JP. Axonal regeneration rate through cross-face nerve grafts. Microsurgery 1993;14:589-591.
13. 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;119:271-279.
14. Frey M, Happak W, Girsch W, Bittner RE, Gruber H. Histomorphometric studies in patients with facial palsy treated by functional muscle transplantation: New aspects for the surgical concept. Ann Plast Surg. 1991;26:370-379.
15. Terzis JK, Olivares FS. Use of mini-temporalis transposition to improve free muscle outcomes for smile. Plast Reconstr Surg. 2008;122:1723-1732.
16. Fu SY, Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol. 1997;14:67-116.
17. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: Prolonged denervation. J Neurosci. 1995;15:3886-3895.
18. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. J Neurosci. 1995;15:3876-3885.
19. Midha R, Munro CA, Chan S, Nitising A, Xu QG, Gordon T. Regeneration into protected and chronically denervated peripheral nerve stumps. Neurosurgery 2005;57:1289-1299; discussion 1289.
20. Sulaiman OA, Gordon T. Role of chronic Schwann cell denervation in poor functional recovery after nerve injuries and experimental strategies to combat it. Neurosurgery 2009;65(Suppl):A105-A114.
21. Bain JR, Hason Y, Veltri K, Fahnestock M, Quartly C. Clinical application of sensory protection of denervated muscle. J Neurosurg. 2008;109:955-961.
22. Bain JR, Veltri KL, Chamberlain D, Fahnestock M. Improved functional recovery of denervated skeletal muscle after temporary sensory nerve innervation. Neuroscience 2001;103:503-510.
23. Magill CK, Moore AM, Borschel GH, Mackinnon SE. A new model for facial nerve research: The novel transgenic Thy1-GFP rat. Arch Facial Plast Surg. 2010;12:315-320.
24. Kemp SW, Phua PD, Stanoulis KN, et al. Functional recovery following peripheral nerve injury in the transgenic Thy1-GFP rat. J Peripher Nerv Syst. 2013;18:220-231.
25. Moore AM, Borschel GH, Santosa KA, et al. A transgenic rat expressing green fluorescent protein (GFP) in peripheral nerves provides a new hindlimb model for the study of nerve injury and regeneration. J Neurosci Methods 2012;204:19-27.
26. Skouras E, Pavlov S, Bendella H, Angelov DN. Stimulation of trigeminal afferents improves motor recovery after facial nerve injury: Functional, electrophysiological and morphological proofs. Adv Anat Embryol Cell Biol. 2013;213: 1-105, vii.
27. Tomov TL, Guntinas-Lichius O, Grosheva M, et al. An example of neural plasticity evoked by putative behavioral demand and early use of vibrissal hairs after facial nerve transection. Exp Neurol. 2002;178:207-218.
28. Guntinas-Lichius O, Angelov DN, Tomov TL, Dramiga J, Neiss WF, Wewetzer K. Transplantation of olfactory ensheathing cells stimulates the collateral sprouting from axotomized adult rat facial motoneurons. Exp Neurol. 2001;172:70-80.
29. Guntinas-Lichius O, Irintchev A, Streppel M, et al. Factors limiting motor recovery after facial nerve transection in the rat: Combined structural and functional analyses. Eur J Neurosci. 2005;21:391-402.
30. Hizay A, Ozsoy U, Demirel BM, et al. Use of a Y-tube conduit after facial nerve injury reduces collateral axonal branching at the lesion site but neither reduces polyinnervation of motor endplates nor improves functional recovery. Neurosurgery 2012;70:1544-1556; discussion 1556.
31. Ozsoy U, Demirel BM, Hizay A, et al. Manual stimulation of the whisker pad after hypoglossal-facial anastomosis (HFA) using a Y-tube conduit does not improve recovery of whisking function. Exp Brain Res. 2014;232:2021-2033.
32. Sinis N, Horn F, Genchev B, et al. Electrical stimulation of paralyzed vibrissal muscles reduces endplate reinnervation and does not promote motor recovery after facial nerve repair in rats. Ann Anat. 2009;191:356-370.
33. Bischoff A, Grosheva M, Irintchev A, et al. Manual stimulation of the orbicularis oculi muscle improves eyelid closure after facial nerve injury in adult rats. Muscle Nerve 2009;39:197-205.
34. Guntinas-Lichius O, Hundeshagen G, Paling T, Angelov DN. Impact of different types of facial nerve reconstruction on the recovery of motor function: An experimental study in adult rats. Neurosurgery 2007;61:1276-1283; discussion 1283.
35. Wood MD, Kemp SW, Liu EH, Szynkaruk M, Gordon T, Borschel GH. Rat-derived processed nerve allografts support more axon regeneration in rat than human-derived processed nerve xenografts. J Biomed Mater Res A 2014;102:1085-1091.
36. Hunter DA, Moradzadeh A, Whitlock EL, et al. Binary imaging analysis for comprehensive quantitative histomorphometry of peripheral nerve. J Neurosci Methods 2007;166:116-124.
37. Gordon T, Sulaiman O, Boyd JG. Experimental strategies to promote functional recovery after peripheral nerve injuries. J Peripher Nerv Syst. 2003;8:236-250.
38. Boyd JG, Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol Neurobiol. 2003;27:277-324.
39. Höke A, Gordon T, Zochodne DW, Sulaiman OA. A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol. 2002;173:77-85.
40. Sulaiman OA, Gordon T. Effects of short-and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 2000;32:234-246.
41. Sulaiman OA, Gordon T. Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia 2002;37:206-218.
42. Sulaiman OA, Voda J, Gold BG, Gordon T. FK506 increases peripheral nerve regeneration after chronic axotomy but not after chronic Schwann cell denervation. Exp Neurol. 2002;175:127-137.
43. Boyd JG, Gordon T. A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. Eur J Neurosci. 2002;15:613-626.
44. Li H, Wigley C, Hall SM. Chronically denervated rat Schwann cells respond to GGF in vitro. Glia 1998;24:290-303.
45. Terzis JK, Konofaos P. Nerve transfers in facial palsy. Facial Plast Surg. 2008;24:177-193.
46. Terzis JK, Tzafetta K. The "babysitter" procedure: Minihypoglossal to facial nerve transfer and cross-facial nerve grafting. Plast Reconstr Surg. 2009;123:865-876.
47. Rosson GD, Redett RJ. Facial palsy: Anatomy, etiology, grading, and surgical treatment. J Reconstr Microsurg. 2008;24:379-389.
48. Kalantarian B, Rice DC, Tiangco DA, Terzis JK. Gains and losses of the XII-VII component of the "baby-sitter" procedure: A morphometric analysis. J Reconstr Microsurg. 1998;14:459-471.
49. Hadlock T, Sheahan T, Heaton J, Sundback C, Mackinnon S, Cheney M. Baiting the cross-face nerve graft with temporary hypoglossal hookup. Arch Facial Plast Surg. 2004;6:228-233.
50. Venail F, Sabatier P, Mondain M, Segniarbieux F, Leipp C, Uziel A. Outcomes and complications of direct end-to-side facial-hypoglossal nerve anastomosis according to the modified May technique. J Neurosurg. 2009;110:786-791.
51. Ladak A, Schembri P, Olson J, Udina E, Tyreman N, Gordon T. Side-to-side nerve grafts sustain chronically denervated peripheral nerve pathways during axon regeneration and result in improved functional reinnervation. Neurosurgery 2011;68:1654-1665; discussion 1665.
52. 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;110:267-275.
53. Viterbo F, Trindade JC, Hoshino K, Mazzoni Neto A. Endto-side neurorrhaphy with removal of the epineurial sheath: An experimental study in rats. Plast Reconstr Surg. 1994;94:1038-1047.
54. Viterbo F. A new method for treatment of facial palsy: The cross-face nerve transplantation with end-to-side neurorrhaphy. Rev Soc Bras Cir Plast Est Reconstr. 1993;8:29.
55. Matsuda K, Kakibuchi M, Kubo T, et al. A new model of endto-side nerve graft for multiple branch reconstruction: Endto-side cross-face nerve graft in rats. J Plast Reconstr Aesthet Surg. 2008;61:1357-1367.
56. Samii M, Koerbel A, Safavi-Abbasi S, Di Rocco F, Samii A, Gharabaghi A. Using an end-to-side interposed sural nerve graft for facial nerve reinforcement after vestibular schwannoma resection: Technical note. J Neurosurg. 2006;105:920-923.
57. Sundine MJ, Quan EE, Saglam O, et al. The use of end-toside nerve grafts to reinnervate the paralyzed orbicularis oculi muscle. Plast Reconstr Surg. 2003;111:2255-2264.
58. Isaacs JE, Cheatham S, Gagnon EB, Razavi A, McDowell CL. Reverse end-to-side neurotization in a regenerating nerve. J Reconstr Microsurg. 2008;24:489-496.
59. 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;107:821-829.
60. 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;38:466-477.
61. Kale SS, Glaus SW, Yee A, et al. Reverse end-to-side nerve transfer: From animal model to clinical use. J Hand Surg Am. 2011;36:1631-1639.e2.
62. Hadlock T, Kowaleski J, Mackinnon S, Heaton JT. A novel method of head fixation for the study of rodent facial function. Exp Neurol. 2007;205:279-282.
63. Heaton JT, Kowaleski JM, Bermejo R, Zeigler HP, Ahlgren DJ, Hadlock TA. A system for studying facial nerve function in rats through simultaneous bilateral monitoring of eyelid and whisker movements. J Neurosci Methods 2008;171:197-206.
64. Pearson KG. Neural adaptation in the generation of rhythmic behavior. Annu Rev Physiol. 2000;62:723-753.
65. Berg RW, Kleinfeld D. Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. J Neurophysiol. 2003;90:2950-2963.
66. Fee MS, Mitra PP, Kleinfeld D. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J Neurophysiol. 1997;78:1144-1149.
67. Borschel GH, Kawamura DH, Kasukurthi R, Hunter DA, Zuker RM, Woo AS. The motor nerve to the masseter muscle: An anatomic and histomorphometric study to facilitate its use in facial reanimation. J Plast Reconstr Aesthet Surg. 2012;65:363-366.
68. Manktelow RT, Tomat LR, Zuker RM, Chang M. Smile reconstruction in adults with free muscle transfer innervated by the masseter motor nerve: Effectiveness and cerebral adaptation. Plast Reconstr Surg. 2006;118:885-899.
69. Bae YC, Zuker RM, Manktelow RT, Wade S. A comparison of commissure excursion following gracilis muscle transplantation for facial paralysis using a cross-face nerve graft versus the motor nerve to the masseter nerve. Plast Reconstr Surg. 2006;117:2407-2413.