J Reconstr Microsurg 2018; 34(06): 436-445
DOI: 10.1055/s-0038-1636539
Original Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Dynamic Quantitative Assessment of Motor Axon Sprouting after Direct Facial–Hypoglossal End-To-Side Neurorrhaphy in Rats

Pengfei Liu*
1   Department of Neurosurgery, XinHua Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
,
Zhang Zhang*
2   Department of Neurosurgery, Central Hospital of Wuhan, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
,
Chenlong Liao
1   Department of Neurosurgery, XinHua Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
,
Wenxiang Zhong
1   Department of Neurosurgery, XinHua Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
,
Pengyang Li
3   Aerospace School of Clinical Medicine, Peking University Health Science Center, Beijing, China
,
Wenchuan Zhang
1   Department of Neurosurgery, XinHua Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
› Author Affiliations
Further Information

Publication History

14 October 2017

18 January 2018

Publication Date:
01 April 2018 (online)

Abstract

Background End-to-side (ETS) neurorrhaphy is a promising procedure for peripheral nerve repair, yet controversies regarding the efficacy of this repair in facial nerve anastomosis for facial paralysis still exist.

Materials and Methods Thirty rats were divided into three groups: intact control group, direct facial–hypoglossal ETS neurorrhaphy, and end-to-end (ETE) neurorrhaphy. Nerve regeneration was assessed with vibrissae motor performance, electrophysiological tests, retrograde labeling, and histomorphological analysis at 4 and 8 months postoperatively.

Results Both ETS and ETE neurorrhaphies resulted in axonal regeneration and functional recovery of the recipient nerve but did not reach the level of intact controls. Significantly higher numbers of myelinated axons and labeled neurons giving regenerating fibers were found in group ETE compared with group ETS at both time points, consistent with the functional and electrophysiological recovery. Group ETS showed significantly smaller fiber diameter and thinner myelin thickness than group ETE at 4 months, but the difference became nonsignificant at 8 months. ETS neurorrhaphy had a very slight effect on the donor nerve, as determined electrophysiologically and histomorphologically. Sparsely distributed double-labeled neurons and relatively large amounts of single-labeled neurons contributing to reinnervation were found through double retrograde neuronal labeling in group ETS. Further quantitative analysis of the percentage of double-labeled neurons showed a pronounced tendency to decline from 19.8% at 4 months to 6.0% at 8 months postoperatively.

Conclusion Successful reinnervation after ETS neurorrhaphy could be achieved through both collateral sprouting and terminal sprouting, with the latter seeming to be the principal origin of motor nerve sprouting.

 
  • References

  • 1 Yetiser S, Karapinar U. Hypoglossal-facial nerve anastomosis: a meta-analytic study. Ann Otol Rhinol Laryngol 2007; 116 (07) 542-549
  • 2 Samii M, Alimohamadi M, Khouzani RK, Rashid MR, Gerganov V. Comparison of direct side-to-end and end-to-end hypoglossal-facial anastomosis for facial nerve repair. World Neurosurg 2015; 84 (02) 368-375
  • 3 Martins RS, Socolovsky M, Siqueira MG, Campero A. Hemihypoglossal-facial neurorrhaphy after mastoid dissection of the facial nerve: results in 24 patients and comparison with the classic technique. Neurosurgery 2008; 63 (02) 310-316 , discussion 317
  • 4 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
  • 5 Zhang F, Fischer KA. End-to-side neurorrhaphy. Microsurgery 2002; 22 (03) 122-127
  • 6 Tos P, Colzani G, Ciclamini D, Titolo P, Pugliese P, Artiaco S. Clinical applications of end-to-side neurorrhaphy: an update. BioMed Res Int 2014; 2014: 646128
  • 7 Xiong G, Ling L, Nakamura R, Sugiura Y. Retrograde tracing and electrophysiological findings of collateral sprouting after end-to-side neurorrhaphy. Hand Surg 2003; 8 (02) 145-150
  • 8 Bontioti E, Kanje M, Lundborg G, Dahlin LB. End-to-side nerve repair in the upper extremity of rat. J Peripher Nerv Syst 2005; 10 (01) 58-68
  • 9 Sámal F, Haninec P, Raska O, Dubovỳ P. Quantitative assessment of the ability of collateral sprouting of the motor and primary sensory neurons after the end-to-side neurorrhaphy of the rat musculocutaneous nerve with the ulnar nerve. Ann Anat 2006; 188 (04) 337-344
  • 10 Haastert K, Joswig H, Jäschke KA, Samii M, Grothe C. Nerve repair by end-to-side nerve coaptation: histologic and morphometric evaluation of axonal origin in a rat sciatic nerve model. Neurosurgery 2010; 66 (03) 567-576 , discussion 576–577
  • 11 Haninec P, Kaiser R, Dubový P. A comparison of collateral sprouting of sensory and motor axons after end-to-side neurorrhaphy with and without the perineurial window. Plast Reconstr Surg 2012; 130 (03) 609-614
  • 12 Liao C, Zhang W, Zhong W, Liu P. Facial-hypoglossal end-to-side neurorrhaphy: exploration of the source of axonal sprouting. J Reconstr Microsurg 2016; 32 (08) 599-607
  • 13 Pannucci C, Myckatyn TM, Mackinnon SE, Hayashi A. End-to-side nerve repair: review of the literature. Restor Neurol Neurosci 2007; 25 (01) 45-63
  • 14 Guntinas-Lichius O, Wewetzer K, Tomov TL. , et al. Transplantation of olfactory mucosa minimizes axonal branching and promotes the recovery of vibrissae motor performance after facial nerve repair in rats. J Neurosci 2002; 22 (16) 7121-7131
  • 15 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 (02) 391-402
  • 16 Arvidsson J. Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 1982; 211 (01) 84-92
  • 17 Berg RW, Kleinfeld D. Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 2003; 89 (01) 104-117
  • 18 Dörfl J. The innervation of the mystacial region of the white mouse: a topographical study. J Anat 1985; 142: 173-184
  • 19 Fernandez E, Lauretti L, Denaro L. , et al. Motoneurons innervating facial muscles after hypoglossal and hemihypoglossal-facial nerve anastomosis in rats. Neurol Res 2004; 26 (04) 395-400
  • 20 Wan H, Zhang L, Blanchard S. , et al. Combination of hypoglossal-facial nerve surgical reconstruction and neurotrophin-3 gene therapy for facial palsy. J Neurosurg 2013; 119 (03) 739-750
  • 21 Papalia I, Magaudda L, Righi M. , et al. Epineurial window is more efficient in attracting axons than simple coaptation in a sutureless (cyanoacrylate-bound) model of end-to-side nerve repair in the rat upper limb: functional and morphometric evidences and review of the literature. PLoS One 2016; 11 (02) e0148443
  • 22 Lauretti L, D'Ercole M, Di Masi G, Socolovsky M, Fernandez E. Facial--hypoglossal nerve end-to-side neurorrhaphy: anatomical study in rats. Acta Neurochir Suppl (Wien) 2011; 108: 221-226
  • 23 Bertelli JA, dos Santos AR, Calixto JB. Is axonal sprouting able to traverse the conjunctival layers of the peripheral nerve? A behavioral, motor, and sensory study of end-to-side nerve anastomosis. J Reconstr Microsurg 1996; 12 (08) 559-563
  • 24 Hayashi A, Pannucci C, Moradzadeh A. , et al. Axotomy or compression is required for axonal sprouting following end-to-side neurorrhaphy. Exp Neurol 2008; 211 (02) 539-550
  • 25 Kovačič U, Zele T, Tomšič M, Sketelj J, Bajrović FF. Influence of breaching the connective sheaths of the donor nerve on its myelinated sensory axons and on their sprouting into the end-to-side coapted nerve in the rat. J Neurotrauma 2012; 29 (18) 2805-2815
  • 26 Liu HF, Chen ZG, Shen HM. , et al. Efficacy of the end-to-side neurorrhaphies with epineural window and partial donor neurectomy in peripheral nerve repair: an experimental study in rats. J Reconstr Microsurg 2015; 31 (01) 31-38
  • 27 Liao WC, Chen JR, Wang YJ, Tseng GF. The efficacy of end-to-end and end-to-side nerve repair (neurorrhaphy) in the rat brachial plexus. J Anat 2009; 215 (05) 506-521
  • 28 Matsumoto M, Hirata H, Nishiyama M, Morita A, Sasaki H, Uchida A. Schwann cells can induce collateral sprouting from intact axons: experimental study of end-to-side neurorrhaphy using a Y-chamber model. J Reconstr Microsurg 1999; 15 (04) 281-286
  • 29 Hayashi A, Yanai A, Komuro Y, Nishida M, Inoue M, Seki T. Collateral sprouting occurs following end-to-side neurorrhaphy. Plast Reconstr Surg 2004; 114 (01) 129-137
  • 30 Rovak JM, Cederna PS, Macionis V, Urbanchek MS, Van Der Meulen JH, Kuzon Jr WM. Termino-lateral neurorrhaphy: the functional axonal anatomy. Microsurgery 2000; 20 (01) 6-14
  • 31 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 (07) 459-471
  • 32 Liu HF, Chen ZG, Fang TL, Arnold P, Lineaweaver WC, Zhang J. Changes of the donor nerve in end-to-side neurorrhaphies with epineurial window and partial neurectomy: a long-term evaluation in the rat model. Microsurgery 2014; 34 (02) 136-144