Terminolateral Neurorrhaphy: Review of Experimental and Clinical Studies

ABSTRACT

Since the reintroduction of the terminolateral neurorrhaphy (TLN) concept by Viterbo in 1992, several published articles and abstracts have been reported in the English literature. This report was prepared to investigate the following subjects: source of current research on TLN, animal models, methods of assessment of axonal regeneration, the source of regenerating axons, sensory vs. motor collateral sprouting, effects on the donor nerve, cellular events following TLN, factors affecting axonal regeneration and, finally, end-to-side nerve repair in the human patient.

REFERENCES

• 1 Sherren J. Some points in the surgery of the peripheral nerves.  Edinburgh Med J . 1906;  20 297
• 2 Kennedy R. On the restoration of coordinated movement after nerve crossing with interchange of function of the cerebral cortical centers.  Phil Trans R Soc Lond . 1901;  194B 127
• 3 Ballance C, Ballance H A, Stewart P. Remarks on the operative treatment of chronic facial palsy of peripheral origin.  Br Med J . 1903;  2 1009
• 4 Harris L, Low V W. On the importance of accurate muscular analysis in lesions of the brachial plexus and the treatment of Erb's palsy and infantile paralysis of the upper extremity by cross-union of the nerve roots.  Br Med J . 1903;  24 1035
• 5 Petropoulos P C, Stefanko S. Experimental observations on the prevention of neuroma formation.  J Surg Res . 1961;  1 241
• 6 Viterbo F, Trindade J C, Hoshino K, Mazzoni A. Latero-terminal neurorrhaphy without removal of the epineurial sheath: experimental study in rats.  Sao Paulo Med J . 1992;  110 267
• 7 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 Estet Reconstr . 1993;  8 29
• 8 Viterbo F, Palhares A, Franciosi L F. Restoration of sensibility after removal of the sural nerve: a new application of lateral-terminal neurorrhaphy (case report).  Rev Soc Bras Cir Plast Estet Reconstr . 1993;  8 85
• 9 Viterbo F. Cross-face termino lateral neurorrhaphy: a new method of treatment of facial palsy (Abstract).  J Reconstr Microsurg . 1994;  10 109
• 10 Viterbo F, Trindade J C, Hoshino W, Mazzoni N A. Two end-to-side neurorrhaphies and nerve graft with removal of the epineurial sheath: experimental study in rats.  Br J Plast Surg . 1994;  47 75
• 11 Viterbo F, Trindade J C, Hoshino K, Mazzoni N A. End-to-side neurorrhaphy with removal of the epineurial sheath: an experimental study in rats.  Plast Reconstr Surg . 1994;  94 1038
• 12 Viterbo F, Fraciosi L F, Pathares A. Nerve grafting end-to-side neurorrhaphies connecting the phrenic nerve to the brachial plexus (letter).  Plast Reconstr Surg . 1995;  96 494
• 13 Lundborg G, Zhao Q, Kanje M. Can sensory and motor collateral sprouting be induced from intact peripheral nerve by end-to-side anastomosis?.  J Hand Surg . 1994;  19B 277
• 14 Ross D, Zuker R M, Matsuda H. End-to-side nerve coaptation for muscle reinnervation (Abstract).  J Reconstr Microsurg . 1995;  11 373
• 15 Van Vliet D, Doering L, Bain J, Veltri K. End-to-side neurorrhaphy: trauma or collateral sprouting?.  <~>(Abstract). Can J Plast Surg . 1996;  4 27
• 16 Bertelli J A, dos Santos R S A, Calixto J B. Is axonal sprouting able to transverse the conjunctival layers of the peripheral nerve?.  <~>A behavioral, motor, sensory study of end-to-side nerve anastomosis. J Reconstr Microsurg . 1996;  12 559
• 17 Al-Qattan M M, Al-Thunayan A. Variables affectig axonal regeneration following end-to-side neurorrhaphy .  1998;  51 238
• 18 Al-Qattan M M. Prevention and treatment of painful neuromas of the superficial radial nerve by the end-to-side nerve repair concept: an experimental study and preliminary clinical experience.  Microsurgery . 2000;  20 99
• 19 Giovanoli P, Koller R, Meuli-Simmen C. Functional and morphologic results after end-to-side neurorrhaphy for muscle reinnervation: experimental study in rabbits (Abstract).  J Reconstr Microsurg . 2000;  16 69
• 20 Zhang Z, Jinyan B, Soucacos P N, Beris A E. Long term observations with end-to-side neurorrhaphy to repair the main nerve trunk of the forelimb in a rabbit model (Abstract).  J Reconst Microsurg . 1999;  15 631
• 21 Zhang Z, Soucacos P N, Beris A E. Long-term evaluation of rat peripheral nerve repair with end-to-side neurorrhaphy.  J Reconstr Microsurg . 2000;  16 303
• 22 Zhang Z, Soucacos P N, Jinyan B O, Beris A E. Evaluation of collateral sprouting after end-to-side coaptation using a fluorescent double labelling technique.  Microsurgery . 1999;  19 281
• 23 Zhang Z, Soucacos P N, Jinyan B O. What extent of reinnervation can be achieved from end-to-side nerve coaptation in a rat model?.  <~>(Abstract). J Reconstr Microsurg . 1998;  14 271
• 24 Zhang Z, Jinyan B O, Soucacos P N. End-to-side neurorrhaphy: a short and long term evaluation (Abstract).  Microsurgery . 1999;  19 10
• 25 Terzis J K, Fortes W M, Liuzzi F, Noah M. End-to-side neurorrhaphy evaluation of nerve growth factor elaboration using cRNA probes (in-situ hybridization).  J Reconstr Microsurg . 1997;  13 136
• 26 Fortes W M, Noah E M, Liuzzi F J, Terzis J K. End-to-side neurorrhaphy: evaluation of axonal response and upregulation of IGF-I and IGF-II in a non-injury model.  J Reconstr Microsurg . 1999;  15 449
• 27 Caplan J, Tiangco D A, Terzis J K. Effects of IGF-II in a new end-to-side model.  J Reconstr Microsurg . 1999;  15 351
• 28 Andreopoulos E K, Skoulis T G, Liuzzi F, Terzis J K. Double-labelling technique to trace axonal sprouting after end-to-side neurorrhaphy (Abstract).  J Reconstr Microsurg . 1998;  14 591
• 29 Noah E M, Williams A, Jorgensen C. End-to-side neurorrhaphy: a histologic and morphometric study of axonal sprouting into an end-to-side nerve graft.  J Reconstr Microsurg . 1997;  13 99
• 30 Noah E M, Williams A, Fortes W, Terzis J K. A new animal model to investigate axonal sprouting after end-to-side neurorrhaphy.  J Reconstr Microsurg . 1997;  13 317
• 31 Okajima S, Terzis J K. Ultrastructure of axonal regeneration in end-to-side neurorrhaphy.  J Reconstr Microsurg . 1997;  13 605
• 32 Tarasidis G, Watanabe O, Mackinnon S E. End-to-side neurorrhaphy resulting in limited sensory axonal regeneration in a rat model.  Ann Otol Rhinol Laryngol . 1997;  106 506
• 33 Tarasidis G, Watanabe O, Mackinnon S E. End-to-side neurorrhaphy: a long-term study of neural regeneration in a rat model.  Otolaryngol Head Neck Surg . 1998;  119 337
• 34 Hu G, Murin V P, Hays A, Chiu D TW. Termino-lateral neurorrhaphy with autogenous venous nerve conduit (AVNC): histologic study (Abstract).  J Reconstr Microsurg . 1999;  15 627
• 35 Ting J, Hu G, Marin V P. End-to-side nerve anastomosis using autogenous vein nerve conduits (Abstract).  J Reconstr Microsurg . 1998;  14 591
• 36 McCallister W V, Tang P, Trumble T E. Is end-to-side neurorrhaphy effective?.  <~>A study of axonal sprouting stimulated from intact nerves. J Reconstr Microsurg . 1999;  15 597
• 37 Matloub H S, Yan J G, Sanger J R, Yousif N J. A new anastomosis method for peripheral nerve: helicoid anastomosis (Abstract).  J Reconstr Microsurg . 1997;  13 67
• 38 Yan J G, Matloub H S, Sanger S R, Zhang L L. Nerve sprouting after termino-lateral neurorrhaphy (Abstract).  J Reconstr Microsurg . 1999;  15 376
• 39 Rovak J M, Cederna P S, Macionis V. Termino-lateral neurorrhaphy: the functional axonal anatomy.  Microsurgery . 2000;  20 6
• 40 Kalliainen L K, Cederna P S, Kuzon W M. Mechanical function of muscle reinnervated by end-to-side neurorrhaphy.  Plast Reconstr Surg . 1999;  103 1919
• 41 Lohmen R, Bullock F, McNaughton T, Siemionow M. End-to-end versus end-to-side neurorrhaphy (Abstract).  J Reconstr Microsurg . 1997;  13 135
• 42 Campbell J N, Belzberg A J. Nerve fibers in the proximal end of the distal segment of a previously severed nerve in man: evidence for side-to-side nerve sprouting (Abstract).  J Reconstr Microsurg . 1997;  13 137
• 43 Chen Y G, Brushart T M. The effect of denervated muscle and Schwann cells on axon collateral sprouting.  J Hand Surg . 1998;  23A 1025
• 44 Shah M H, Kasabian A K, Karp N S. Axonal regeration through an autogenous nerve bypass: an experimental study in the rat.  Ann Plast Surg . 1997;  38 408
• 45 Kasabian A, Karp N, Margiotta M. Treatment of a neuroma-in-continuity of the peroneal nerve bypass grafts: a case report.  Ann Plast Surg . 1999;  42 449
• 46 Zhang F, Cheng C, Chin B. Results of termino-lateral neurorrhaphy to original and adjacent nerves.  Microsurgery . 1998;  18 276
• 47 Tham S KY, Morrison W A. Motor collateral sprouting through an end-to-side nerve repair.  J Hand Surg . 1998;  23A 844
• 48 Mennen U. End-to-side nerve suture in the primate (Chacma baboon).  Hand Surg . 1998;  3 1
• 49 Mennen U. End-to-side nerve suture in the human patient.  Hand Surg . 1998;  3 7
• 50 Yuksel F, Kislaoglu E, Yildirim S. End-to-side neurorrhaphy supported by transposed active nerve fibers: its functional end result in a rat model.  Eur J Plast Surg . 1998;  21 57
• 51 Yuksel F, Karacaoglu E, Guler M. Nerve regeneration through side-to-side neurorrhaphy sites in a rat model: a new concept in peripheral nerve surgery.  Plast Reconstr Surg . 1999;  104 2092
• 52 Kostakoglu N. Motor and sensory reinnervation in the hand after an end-to-side median to ulnar nerve coaptation in the forearm.  Br J Plast Surg . 1999;  52 404
• 53 Reis F A. Comparative study of axonal sprouting in nerve grafted to the vagus nerve and end-to-side neurorrhaphy. Master's thesis, Instituto de Biociencias, Universdade Estadual Paulista, Botucatu, Brazil, 1999
• 54 Millesi H. Successful application of termino-lateral coaptation in brachial plexus surgery (Abstract).  J Reconstr Microsurg . 1999;  15 626
• 55 Frey M, Giovanoli P, Girsch W. Clinical application of end-to-side nerve coaptation for sensory or motor reinnervation (Abstract).  J Hand Surg . 1999;  24B supplement 9
• 56 Cao X, Tamai M, Kizaki W. Choline acetyltransferase activity in collateral sprouting of peripheral nerve after surgical intervention: experimental study in rats.  J Reconstr Microsurg . 1999;  15 443
• 57 Matsuda H, Hata Y, Osamu I, Battal N M. End-to-side nerve coaptation: clinical applications for cross face nerve grafts (Abstract).  J Reconstr Microsurg . 1997;  13 376
• 58 Matsumoto M, Hirata H, Nishiyama M. 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;  15 281
• 59 Battal M N, Hata Y, Matsuka K. Experimental study of nerve regeneration in end-to-side nerve coaptation.  J Jpn Plast Reconstr Surg . 1995;  15 910
• 60 Battal M N, Hata Y, Matsuka K. Cross facial nerve grafting by end-to-side neurorrhaphy with or without removal of the epineurium in rats.  J Jpn Plast Reconstr Surg . 1996;  16 641
• 61 Lutz B S, Chuang D CC, Hsu J C, Wei F C. End-to-side neurorrhaphy: functional and double labelling study in rat upper limb (Abstract).  J Reconstr Microsurg . 1998;  14 590
• 62 Santamaria E, Wei F C, Chen I H, Chuang D CC. Sensory recovery on innervated radial forearm flap for hemiglossectomy reconstruction by using different recipient nerves.  Plast Reconstr Surg . 1999;  103 450
• 63 Zhao J Z, Chen Z W, Chen T Y. Nerve regeneration after termino-lateral neurorrhaphy: experimental study in rats.  J Reconstr Microsurg . 1997;  13 31
• 64 Luo Y-X. Preliminary investigation of treatment of ulnar nerve defect by end-to-side neurorrhaphy (Abstract).  Plast Reconst Surg . 1998;  102 2528
• 65 McCallister W V, Tang P, Thomas E. Axonal sprouting across end-to-side coaptation: can it be stimulated and does it work?.  <~>(Abstract). J Reconstr Microsurg . 1998;  14 591
• 66 Okajima S, Terzis J K. Ultrastructure of early axonal regeneration in an end-to-side neurorrhaphy model.  J Reconstr Microsurg . 2000;  16 313
• 67 Liu K, Chen L E, Seaber A V. Motor functional and morphological findings following end-to-side neurorrhaphy in the rat model.  J Orthop Res . 1999;  17 293
• 68 Rowen P R, Chen L, Urbaniak J R. End-to-side nerve repair: a review.  Hand Clin . 2000;  16 151
• 69 Dellon A L. Re: nerve grafting and end-to-side neurorrhaphies connecting phrenic nerve to the brachial plexus (Letter).  Plast Reconstr Surg . 1996;  98 905
• 70 Mackinnon S E. Comment on variables affecting axonal regeneration following end-to-side neurorrhaphy. In: The Year Book of Hand Surgery St. Louis: Mosby 1999: 295
• 71 May M, Sobol F M, Mester S J. Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy.  Otolaryngol Head Neck Surg . 1991;  104 818
• 72 Oberlin C, Beal D, Leechavengvongs S. Nerve transfer to biceps muscle using a part of ulnar nerve for C₅-C₆ avulsions of the brachial plexus: anatomical study and report of four cases.  J Hand Surg . 1994;  19A 232
• 73 Nath R K, Mackinnon S E. Nerve transfers in the upper extremity.  Hand Clin . 2000;  16 131
• 74 Battiston B, Lanzetta M. Reconstruction of high ulnar nerve lesions by distal double median to ulnar nerve transfer.  J Hand Surg . 1999;  24A 1185