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BioMed Research International
Volume 2014, Article ID 543020, 10 pages
http://dx.doi.org/10.1155/2014/543020
Research Article

Hypoglossal-Facial Nerve Reconstruction Using a Y-Tube-Conduit Reduces Aberrant Synkinetic Movements of the Orbicularis Oculi and Vibrissal Muscles in Rats

1Department of Anatomy, Akdeniz University Faculty of Medicine, 07070 Antalya, Turkey
2Department of Ear Nose Throat, Akdeniz University Faculty of Medicine, 07070 Antalya, Turkey
3Anatomical Institute I, University of Cologne, 50931 Cologne, Germany

Received 23 June 2014; Revised 16 September 2014; Accepted 17 September 2014; Published 9 December 2014

Academic Editor: Stefan Rampp

Copyright © 2014 Yasemin Kaya et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. A. Bascom, B. M. Schaitkin, M. May, and S. Klein, “Facial nerve repair: a retrospective review,” Facial Plastic Surgery, vol. 16, no. 4, pp. 309–313, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Gharabaghi, S. Heckl, J. Kaminsky et al., “Hirnnervenausfälle durch ungewöhnliche Schädelbasisläsionen des Sinus cavernosus,” HNO, vol. 55, no. 4, pp. 278–280, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. O. Guntinas-Lichius, “The facial nerve in the presence of a head and neck neoplasm: assessment and outcome after surgical management,” Current Opinion in Otolaryngology and Head and Neck Surgery, vol. 12, no. 2, pp. 133–141, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Hundeshagen, Effect of Mechanical Stimulation of the Vibriseal Muscles on the Recovery of Whisking after Hypoglossal-Facial Nerve Anastomosis (HFA) in Adult Rats, Department of Anatomy Cologne: University of Cologne, 2006.
  5. S. Sood, R. Anthony, J. J. Homer, P. Van Hille, and J. D. Fenwick, “Hypoglossal-facial nerve anastomosis: assessment of clinical results and patient benefit for facial nerve palsy following acoustic neuroma excision,” Clinical Otolaryngology and Allied Sciences, vol. 25, no. 3, pp. 219–226, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Miehlke, “Reconstruction of function in vocal cord paralysis. Round table discussion,” Laryngologie, Rhinologie, Otologie, vol. 65, no. 1, pp. 1–4, 1986. View at Publisher · View at Google Scholar · View at Scopus
  7. N. J. Naff and J. M. Ecklund, “History of peripheral nerve surgery techniques,” Neurosurgery Clinics of North America, vol. 12, no. 1, pp. 197–209, 2001. View at Google Scholar · View at Scopus
  8. J. D. F. Kerrebijn and J. L. Freeman, “Facial nerve reconstruction: outcome and failures,” Journal of Otolaryngology, vol. 27, no. 4, pp. 183–186, 1998. View at Google Scholar · View at Scopus
  9. A. Bischoff, M. Grosheva, A. Irintchev et al., “Manual stimulation of the orbicularis oculi muscle improves eyelid closure after facial nerve injury in adult rats,” Muscle & Nerve, vol. 39, no. 2, pp. 197–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. O. Guntinas-Lichius, G. Hundeshagen, T. Paling et al., “Manual stimulation of facial muscles improves functional recovery after hypoglossal-facial anastomosis and interpositional nerve grafting of the facial nerve in adult rats,” Neurobiology of Disease, vol. 28, no. 1, pp. 101–112, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Hwang, S. G. Kim, and D. J. Kim, “Facial-hypoglossal nerve anastomosis using laser nerve welding,” Journal of Craniofacial Surgery, vol. 17, no. 4, pp. 687–691, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Stennert, “I. Hypoglossal facial anastomosis: Its significance for modern facial surgery. II. Combined approach in extratemporal facial nerve reconstruction,” Clinics in Plastic Surgery, vol. 6, no. 3, pp. 471–486, 1979. View at Google Scholar · View at Scopus
  13. D. N. Angelov, A. Gunkel, E. Stennert, and W. F. Neiss, “Recovery of original nerve supply after hypoglossal-facial anastomosis causes permanent motor hyperinnervation of the whisker-pad muscles in the rat,” Journal of Comparative Neurology, vol. 338, no. 2, pp. 214–224, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. Y.-S. Chen, C.-J. Hsu, T.-C. Liu, N. Yanagihara, and S. Murakami, “Histological rearrangement in the facial nerve and central nuclei following immediate and delayed hypoglossal-facial nerve anastomosis,” Acta Oto-Laryngologica, vol. 120, no. 4, pp. 551–556, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. J. H. Morris, A. R. Hudson, and G. Weddell, “A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy - II. The development of the “regenerating unit”,” Zeitschrift für Zellforschung und Mikroskopische Anatomie, vol. 124, no. 2, pp. 103–130, 1972. View at Publisher · View at Google Scholar · View at Scopus
  16. G. D. Shawe, “On the number of branches formed by regenerating nerve-fibres,” The British Journal of Surgery, vol. 42, no. 175, pp. 474–488, 1955. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Montserrat and M. Benito, “Facial synkinesis and aberrant regeneration of facial nerve,” Advances in Neurology, vol. 49, pp. 211–224, 1988. View at Google Scholar · View at Scopus
  18. A. J. Sumner, “Aberrant reinnervation,” Muscle and Nerve, vol. 13, no. 9, pp. 801–803, 1990. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Ito and M. Kudo, “Reinnervation by axon collaterals from single facial motoneurons to multiple muscle targets following axotomy in the adult guinea pig,” Acta Anatomica, vol. 151, no. 2, pp. 124–130, 1994. View at Publisher · View at Google Scholar · View at Scopus
  20. C. L. A. M. Vleggeert-Lankamp, G. C. W. de Ruiter, J. F. C. Wolfs et al., “Type grouping in skeletal muscles after experimental reinnervation: Another explanation,” European Journal of Neuroscience, vol. 21, no. 5, pp. 1249–1256, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Streppel, N. Azzolin, S. Dohm et al., “Focal application of neutralizing antibodies to soluble neurotrophic factors reduces collateral axonal branching after peripheral nerve lesion,” European Journal of Neuroscience, vol. 15, no. 8, pp. 1327–1342, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Grosheva, O. Guntinas-Lichius, S. K. Angelova et al., “Local stabilization of microtubule assembly improves recovery of facial nerve function after repair,” Experimental Neurology, vol. 209, no. 1, pp. 131–144, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. O. Guntinas-Lichius, A. Irintchev, M. Streppel et al., “Factors limiting motor recovery after facial nerve transection in the rat: combined structural and functional analyses,” European Journal of Neuroscience, vol. 21, no. 2, pp. 391–402, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Tos, B. Battiston, S. Geuna et al., “Tissue specificity in rat peripheral nerve regeneration through combined skeletal muscle and vein conduit grafts,” Microsurgery, vol. 20, no. 2, pp. 65–71, 2000. View at Google Scholar
  25. U. Ozsoy, B. M. Demirel, A. Hizay et al., “Hypoglossal-facial anastomosis (HFA) over a 10 mm gap bridged by a Y-tube-conduit enhances neurite regrowth and reduces collateral axonal branching at the lesion site,” Restorative Neurology and Neuroscience, vol. 29, no. 4, pp. 227–242, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Skouras, U. Ozsoy, L. Sarikcioglu, and D. N. Angelov, “Intrinsic and therapeutic factors determining the recovery of motor function after peripheral nerve transection,” Annals of Anatomy, vol. 193, no. 4, pp. 286–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Hizay, U. Ozsoy, B. M. Demirel 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, vol. 70, no. 6, pp. 1544–1556, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Semba, H. Szechtman, and B. R. Komisaruk, “Synchrony among rhythmical facial tremor, neocortical “alpha” waves, and thalamic non-sensory neuronal bursts in intact awake rats,” Brain Research, vol. 195, no. 2, pp. 281–298, 1980. View at Publisher · View at Google Scholar · View at Scopus
  29. R. W. Berg and D. Kleinfeld, “Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control,” Journal of Neurophysiology, vol. 89, no. 1, pp. 104–117, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Semba and B. R. Komisaruk, “Neural substrates of two different rhythmical vibrissal movements in the rat,” Neuroscience, vol. 12, no. 3, pp. 761–774, 1984. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Dorfl, “The innervation of the mystacial region of the white mouse. A topographical study,” Journal of Anatomy, vol. 142, pp. 173–184, 1985. View at Google Scholar · View at Scopus
  32. G. E. Carvell and D. J. Simons, “Biometric analyses of vibrissal tactile discrimination in the rat,” Journal of Neuroscience, vol. 10, no. 8, pp. 2638–2648, 1990. View at Google Scholar · View at Scopus
  33. D. N. Angelov, O. Guntinas-Lichius, K. Wewetzer, W. F. Neiss, and M. Streppel, “Axonal branching and recovery of coordinated muscle activity after transection of the facial nerve in adult rats,” in Advances in Anatomy Embryology and Cell Biology, F. F. Beck, B. Christ, F. Clascá et al., Eds., pp. 3–25, Springer, Berlin, Germany, 2005. View at Google Scholar
  34. A. Gruart, P. Blazquez, and J. M. Delgado-Garcia, “Kinematics of spontaneous, reflex, and conditioned eyelid movements in the alert cat,” Journal of Neurophysiology, vol. 74, no. 1, pp. 226–248, 1995. View at Google Scholar · View at Scopus
  35. A. Gruart, M. Streppel, O. Guntinas-Lichius, D. N. Angelov, W. F. Neiss, and J. M. Delgado-García, “Motoneuron adaptability to new motor tasks following two types of facial-facial anastomosis in cats,” Brain, vol. 126, no. 1, pp. 115–133, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. S. K. Koekkoek, W. L. den Ouden, G. Perry, S. M. Highstein, and C. I. de Zeeuw, “Monitoring kinetic and frequency-domain properties of eyelid responses in mice with magnetic distance measurement technique,” Journal of Neurophysiology, vol. 88, no. 4, pp. 2124–2133, 2002. View at Google Scholar · View at Scopus
  37. B. W. Quist and M. J. Z. Hartmann, “A two-dimensional force sensor in the millinewton range for measuring vibrissal contacts,” Journal of Neuroscience Methods, vol. 172, no. 2, pp. 158–167, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. R. B. Towal and M. J. Z. Hartmann, “Variability in velocity profiles during free-air whisking behavior of unrestrained rats,” Journal of Neurophysiology, vol. 100, no. 2, pp. 740–752, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Bendella, S. P. Pavlov, M. Grosheva et al., “Non-invasive stimulation of the vibrissal pad improves recovery of whisking function after simultaneous lesion of the facial and infraorbital nerves in rats,” Experimental Brain Research, vol. 212, no. 1, pp. 65–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Bermejo, M. Harvey, P. Gao, and H. P. Zeigler, “Conditioned whisking in the rat,” Somatosensory and Motor Research, vol. 13, no. 3-4, pp. 225–233, 1996. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Bermejo, D. Houben, and H. P. Zeigler, “Optoelectronic monitoring of individual whisker movements in rats,” Journal of Neuroscience Methods, vol. 83, no. 2, pp. 89–96, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Bermejo and H. P. Zeigler, “‘Real-time’ monitoring of vibrissa contacts during rodent whisking,” Somatosensory and Motor Research, vol. 17, no. 4, pp. 373–377, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Hadlock, J. Kowaleski, S. Mackinnon, and J. T. Heaton, “A novel method of head fixation for the study of rodent facial function,” Experimental Neurology, vol. 205, no. 1, pp. 279–282, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Leal-Campanario, J. A. Barradas-Bribiescas, J. M. Delgado-García, and A. Gruart, “Relative contributions of eyelid and eye-retraction motor systems to reflex and classically conditioned blink responses in the rabbit,” Journal of Applied Physiology, vol. 96, no. 4, pp. 1541–1554, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. J. M. Delgado-Garcia, C. Evinger, M. Escudero, and R. Baker, “Behavior of accessory abducens and abducens motoneurons during eye retraction and rotation in the alert cat,” Journal of Neurophysiology, vol. 64, no. 2, pp. 413–422, 1990. View at Google Scholar · View at Scopus
  46. W. F. Crandall, S. J. Goldberg, J. S. Wilson, and J. R. McClung, “Muscle units divided among retractor bulbi muscle slips and between the lateral rectus and retractor bulbi muscles in cat,” Experimental Neurology, vol. 71, no. 2, pp. 251–260, 1981. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Oda, “Extraocular muscles and their relationship to the accessory abducens nucleus in rats as studied by the horseradish peroxidase method,” Okajimas Folia Anatomica Japonica, vol. 58, no. 1, pp. 43–53, 1981. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Khanna and J. D. Porter, “Evidence for rectus extraocular muscle pulleys in rodents,” Investigative Ophthalmology and Visual Science, vol. 42, no. 9, pp. 1986–1992, 2001. View at Google Scholar · View at Scopus
  49. J. Husseman and R. P. Mehta, “Management of synkinesis,” Facial Plastic Surgery, vol. 24, no. 2, pp. 242–249, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. C. H. G. Beurskens and P. G. Heymans, “Mime therapy improves facial symmetry in people with long-term facial nerve paresis: a randomised controlled trial,” Australian Journal of Physiotherapy, vol. 52, no. 3, pp. 177–183, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. R. W. Lindsay, M. Robinson, and T. A. Hadlock, “Comprehensive facial rehabilitation improves function in people with facial paralysis: a 5-year experience at the Massachusetts eye and ear infirmary,” Physical Therapy, vol. 90, no. 3, pp. 391–397, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Borodic, M. Bartley, W. Slattery et al., “Botulinum toxin for aberrant facial nerve regeneration: double-blind, placebo-controlled trial using subjective endpoints,” Plastic and Reconstructive Surgery, vol. 116, no. 1, pp. 36–43, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. D. K. Henstrom, J. S. Malo, M. L. Cheney, and T. A. Hadlock, “Platysmectomy: an effective intervention for facial synkinesis and hypertonicity,” Archives of Facial Plastic Surgery, vol. 13, no. 4, pp. 239–243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. M. H. Hohman, L. N. Lee, and T. A. Hadlock, “Two-step highly selective neurectomy for refractory periocular synkinesis,” Laryngoscope, vol. 123, no. 6, pp. 1385–1388, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Hontanilla, C. Aubá, J. Arcocha, and O. Gorría, “Nerve regeneration through nerve autografts and cold preserved allografts using tacrolimus (FK506) in a facial paralysis model: a topographical and neurophysiological study in monkeys,” Neurosurgery, vol. 58, no. 4, pp. 768–777, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. R. N. Toledo, A. Borin, O. L. M. Cruz, P. L. Ho, J. R. G. Testa, and Y. Fukuda, “The action of topical basic fibroblast growth factor in facial nerve regeneration,” Otology and Neurotology, vol. 31, no. 3, pp. 498–505, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Wiberg, S. Vedung, and E. Stålberg, “Neuronal loss after transsection of the facial nerve: a morphological and neurophysiological study in monkeys,” Scandinavian Journal of Plastic and Reconstructive Surgery and Hand Surgery, vol. 35, no. 2, pp. 135–140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Irintchev, “Potentials and limitations of peripheral nerve injury models in rodents with particular reference to the femoral nerve,” Annals of Anatomy, vol. 193, no. 4, pp. 276–285, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Ronchi, S. Nicolino, S. Raimondo et al., “Functional and morphological assessment of a standardized crush injury of the rat median nerve,” Journal of Neuroscience Methods, vol. 179, no. 1, pp. 51–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. G. K. Frykman, P. J. McMillan, and S. Yegge, “A review of experimental methods measuring peripheral nerve regeneration in animals,” Orthopedic Clinics of North America, vol. 19, no. 1, pp. 209–219, 1988. View at Google Scholar · View at Scopus
  61. J. W. Griffin, B. Pan, M. A. Polley, P. N. Hoffman, and M. H. Farah, “Measuring nerve regeneration in the mouse,” Experimental Neurology, vol. 223, no. 1, pp. 60–71, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Brecht, V. Grinevich, T.-E. Jin, T. Margrie, and P. Osten, “Cellular mechanisms of motor control in the vibrissal system,” Pflugers Archiv European Journal of Physiology, vol. 453, no. 3, pp. 269–281, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Brecht, B. Preilowski, and M. M. Merzenich, “Functional architecture of the mystacial vibrissae,” Behavioural Brain Research, vol. 84, no. 1-2, pp. 81–97, 1997. View at Publisher · View at Google Scholar · View at Scopus
  64. R. N. S. Sachdev, T. Sato, and F. F. Ebner, “Divergent movement of adjacent whiskers,” Journal of Neurophysiology, vol. 87, no. 3, pp. 1440–1448, 2002. View at Google Scholar · View at Scopus
  65. T. Berg, L. Jonsson, and M. Engström, “Agreement between the Sunnybrook, House-Brackmann, and Yanagihara facial nerve grading systems in Bell's palsy,” Otology and Neurotology, vol. 25, no. 6, pp. 1020–1026, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. C. H. Yian, R. C. Paniello, and J. Gershon Spector, “Inhibition of motor nerve regeneration in a rabbit facial nerve model,” Laryngoscope, vol. 111, no. 5, pp. 786–791, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. J. M. Byers, K. F. Clark, and G. C. Thompson, “Effect of pulsed electromagnetic stimulation on facial nerve regeneration,” Archives of Otolaryngology: Head and Neck Surgery, vol. 124, no. 4, pp. 383–389, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. S. D. de Faria, J. R. G. Testa, A. Borin, and R. N. Toledo, “Standardization of techniques used in facial nerve section and facial movement evaluation in rats,” Revista Brasileira de Otorrinolaringologia, vol. 72, no. 3, pp. 341–347, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Hadlock, J. Kowaleski, D. Lo et al., “Functional assessments of the rodent facial nerve: a synkinesis model,” Laryngoscope, vol. 118, no. 10, pp. 1744–1749, 2008. View at Publisher · View at Google Scholar · View at Scopus