Efficacy of the End-to-Side Neurorrhaphies with Epineural Window and Partial Donor Neurectomy in Peripheral Nerve Repair: An Experimental Study in Rats

Abstract

Background End-to-side (ETS) neurorrhaphy was a useful tool in peripheral nerve repair and “baby-sitter” procedure. The study was designed to evaluate the long-term efficacy of ETS with epineurial window and 40% partial donor neurectomy in rats.

Materials and Methods A total of 60 Lewis rats were divided into three groups (n = 20, each group): following peroneal nerve transection, rats in Group A underwent end-to-end neurorrhaphy; rats in Group B underwent ETS neurorrhaphy of the distal peroneal nerve stump to an epineurial window on the tibial nerve; and rats in Group C underwent ETS neurorrhaphy of the distal peroneal nerve stump to the tibial nerve with 40% partial neurectomy. At 6, 12, 18, and 24 weeks after surgery, electrophysiology, muscle tension, myelinated fiber regeneration, cross-sectional area of muscular fiber, and muscle weight were analyzed.

Results Histology exhibited apparently increased number and size of myelinated fibers in peroneal nerves in Group C, compared with those in Group B. More superior recovery was demonstrated in the electrophysiology and axon regeneration of the peroneal nerves, as well as the maintenance of muscle force, wet weight, and fiber size of the anterior tibial muscles in Group C than those in Group B.

Conclusion ETS neurorrhaphy with partial donor neurectomy can achieve higher efficacy in functional and structural recovery of the recipient system. This study provides the evidence of long-term follow-up for the further investigation of ETS neurorrhaphies with different modalities in peripheral nerve repair and in “baby-sitter” procedure.

Keywords

end-to-side neurorrhaphy - epineurial window - neurectomy

• References

• 1 Zhao Q, Dahlin LB, Kanje M, Lundborg G. Specificity of muscle reinnervation following repair of the transected sciatic nerve. A comparative study of different repair techniques in the rat. J Hand Surg [Br] 1992; 17 (3) 257-261
• 2 Millesi H. Peripheral nerve surgery today: turning point or continuous development?. J Hand Surg [Br] 1990; 15 (3) 281-287
• 3 Tang P, Kilic A, Konopka G, Regalbuto R, Akelina Y, Gardner T. Histologic and functional outcomes of nerve defects treated with acellular allograft versus cabled autograft in a rat model. Microsurgery 2013; 33 (6) 460-467
• 4 Siemionow M, Uygur S, Ozturk C, Siemionow K. Techniques and materials for enhancement of peripheral nerve regeneration: a literature review. Microsurgery 2013; 33 (4) 318-328
• 5 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 (6) 267-275
• 6 Lykissas MG, Korompilias AV, Batistatou AK, Mitsionis GI, Beris AE. Can end-to-side neurorrhaphy bridge large defects? An experimental study in rats. Muscle Nerve 2007; 36 (5) 664-671
• 7 Zhang Z, Soucacos PN, Bo J , et al. Reinnervation after end-to-side nerve coaptation in a rat model. Am J Orthop 2001; 30 (5) 400-406 , discussion 407
• 8 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 (7) 459-471
• 9 Viterbo F, Amr AH, Stipp EJ, Reis FJ. End-to-side neurorrhaphy: past, present, and future. Plast Reconstr Surg 2009; 124 (6, Suppl): e351-e358
• 10 Lykissas MG. Current concepts in end-to-side neurorrhaphy. World J Orthod 2011; 2 (11) 102-106
• 11 Akeda K, Hirata H, Matsumoto M , et al. Regenerating axons emerge far proximal to the coaptation site in end-to-side nerve coaptation without a perineurial window using a T-shaped chamber. Plast Reconstr Surg 2006; 117 (4) 1194-1203 , discussion 1204–1205
• 12 Lundborg G, Zhao Q, Kanje M, Danielsen N, Kerns JM. Can sensory and motor collateral sprouting be induced from intact peripheral nerve by end-to-side anastomosis?. J Hand Surg [Br] 1994; 19 (3) 277-282
• 13 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 (8) 559-563
• 14 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
• 15 Bontioti E, Dahlin LB, Kataoka K, Kanje M. End-to-side nerve repair induces nuclear translocation of activating transcription factor 3. Scand J Plast Reconstr Surg Hand Surg 2006; 40 (6) 321-328
• 16 Brenner MJ, Dvali L, Hunter DA, Myckatyn TM, Mackinnon SE. Motor neuron regeneration through end-to-side repairs is a function of donor nerve axotomy. Plast Reconstr Surg 2007; 120 (1) 215-223
• 17 Terzis JK, Tzafetta K. The “babysitter” procedure: minihypoglossal to facial nerve transfer and cross-facial nerve grafting. Plast Reconstr Surg 2009; 123 (3) 865-876
• 18 Mersa B, Tiangco DA, Terzis JK. Efficacy of the “baby-sitter” procedure after prolonged denervation. J Reconstr Microsurg 2000; 16 (1) 27-35
• 19 Terzis JK, Tzafetta K. “Babysitter” procedure with concomitant muscle transfer in facial paralysis. Plast Reconstr Surg 2009; 124 (4) 1142-1156
• 20 Yohn DC, Miles GB, Rafuse VF, Brownstone RM. Transplanted mouse embryonic stem-cell-derived motoneurons form functional motor units and reduce muscle atrophy. J Neurosci 2008; 28 (47) 12409-12418
• 21 Yüksel F, Karacaoğlu E, Güler MM. Nerve regeneration through side-to-side neurorrhaphy sites in a rat model: a new concept in peripheral nerve surgery. Plast Reconstr Surg 1999; 104 (7) 2092-2099
• 22 Kalliainen LK, Cederna PS, Kuzon Jr WM. Mechanical function of muscle reinnervated by end-to-side neurorrhaphy. Plast Reconstr Surg 1999; 103 (7) 1919-1927
• 23 Noah EM, Williams A, Jorgenson C, Skoulis TG, Terzis JK. End-to-side neurorrhaphy: a histologic and morphometric study of axonal sprouting into an end-to-side nerve graft. J Reconstr Microsurg 1997; 13 (2) 99-106
• 24 Shah MH, Kasabian AK, Karp NS , et al. Axonal regeneration through an autogenous nerve bypass: an experimental study in the rat. Ann Plast Surg 1997; 38 (4) 408-414 , discussion 414–415
• 25 Zhao JZ, Chen ZW, Chen TY. Nerve regeneration after terminolateral neurorrhaphy: experimental study in rats. J Reconstr Microsurg 1997; 13 (1) 31-37
• 26 Zhang F, Lineaweaver WC, Ustüner T , et al. Comparison of muscle mass preservation in denervated muscle and transplanted muscle flaps after motor and sensory reinnervation and neurotization. Plast Reconstr Surg 1997; 99 (3) 803-814
• 27 Tonken HP, Zhang F, Sudekum AE , et al. Microvascular transplant of the gastrocnemius muscle in rats. Microsurgery 1993; 14 (2) 120-124
• 28 Yoshitatsu S, Matsuda K, Yano K, Hosokawa K, Tomita K. Muscle flap mass preservation by sensory reinnervation with end-to-side neurorrhaphy: an experimental study in rats. J Reconstr Microsurg 2008; 24 (7) 479-487
• 29 Jaeger MR, Braga-Silva J, Gehlen D , et al. End-to-end versus end-to-side motor and sensory neurorrhaphy in the repair of the acute muscle denervation. Ann Plast Surg 2011; 67 (4) 391-396
• 30 Oswald TM, Zhang F, Lei MP, Gerzenshtein J, Lineaweaver WC. Muscle flap mass preservation with end-to-side neurorrhaphy: an experimental study. J Reconstr Microsurg 2004; 20 (6) 483-488
• 31 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 (1) 129-137
• 32 Cao X, Shidao H, Yu J. Experimental study on the collateral sprouting after end-to-side anastomosis of nerve trunk [in Chinese]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 1997; 11 (6) 321-324
• 33 Viterbo F, Teixeira E, Hoshino K, Padovani CR. End-to-side neurorrhaphy with and without perineurium. Sao Paulo Med J 1998; 116 (5) 1808-1814
• 34 Zhang Z, Soucacos PN, Beris AE, Bo J, Ioachim E, Johnson EO. Long-term evaluation of rat peripheral nerve repair with end-to-side neurorrhaphy. J Reconstr Microsurg 2000; 16 (4) 303-311
• 35 Liu K, Chen LE, Seaber AV, Goldner RV, Urbaniak JR. Motor functional and morphological findings following end-to-side neurorrhaphy in the rat model. J Orthop Res 1999; 17 (2) 293-300
• 36 Sterne GD, Coulton GR, Brown RA, Green CJ, Terenghi G. Neurotrophin-3-enhanced nerve regeneration selectively improves recovery of muscle fibers expressing myosin heavy chains 2b. J Cell Biol 1997; 139 (3) 709-715
• 37 McCallister WV, Tang P, Smith J, Trumble TE. Axonal regeneration stimulated by the combination of nerve growth factor and ciliary neurotrophic factor in an end-to-side model. J Hand Surg Am 2001; 26 (3) 478-488
• 38 Johnson EO, Charchanti A, Soucacos PN. Nerve repair: experimental and clinical evaluation of neurotrophic factors in peripheral nerve regeneration. Injury 2008; 39 (Suppl. 03) S37-S42
• 39 Pondaag W, Gilbert A. Results of end-to-side nerve coaptation in severe obstetric brachial plexus lesions. Neurosurgery 2008; 62 (3) 656-663 , discussion 656–663
• 40 Oyamatsu H, Koga D, Igarashi M, Shibata M, Ushiki T. Morphological assessment of early axonal regeneration in end-to-side nerve coaptation models. J Plast Surg Hand Surg 2012; 46 (5) 299-307
• 41 Cederna PS, Kalliainen LK, Urbanchek MG, Rovak JM, Kuzon Jr WM. “Donor” muscle structure and function after end-to-side neurorrhaphy. Plast Reconstr Surg 2001; 107 (3) 789-796
• 42 Liu HF, Chen ZG, Fang TL , et al. 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 (2) 136-144