Update on nerve repair by biological tubulization

Stefano Geuna; Pierluigi Tos; Paolo Titolo; Davide Ciclamini; Teresa Beningo; Bruno Battiston

doi:10.1186/1749-7221-9-3

Journal of Brachial Plexus and Peripheral Nerve Injury, Table of Contents

J Brachial Plex Peripher Nerve Inj 2014; 09(01): e16-e21
DOI: 10.1186/1749-7221-9-3

Review

Geuna et al.; licensee BioMed Central Ltd.

Update on nerve repair by biological tubulization^[*]

Stefano Geuna

¹Neuroscience Institute of the Cavalieri Ottolenghi Foundation (NICO), University of Turin, Turin 10043, Italy

²Department of Clinical and Biological Sciences, University of Turin, Turin 10043, Italy

,

Pierluigi Tos

³Department of Traumatology, Microsurgery Unit, CTO Hospital, Turin, Italy

,

Paolo Titolo

⁴UOC Traumatology–Reconstructive Microsurgery, Department of Orthopaedics and Traumatology, CTO Hospital, Torino, Italy

,

Davide Ciclamini

³Department of Traumatology, Microsurgery Unit, CTO Hospital, Turin, Italy

,

Teresa Beningo

³Department of Traumatology, Microsurgery Unit, CTO Hospital, Turin, Italy

,

Bruno Battiston

³Department of Traumatology, Microsurgery Unit, CTO Hospital, Turin, Italy

⁴UOC Traumatology–Reconstructive Microsurgery, Department of Orthopaedics and Traumatology, CTO Hospital, Torino, Italy

› Author Affiliations
Subject Editor:

Abstract

Many surgical techniques are available for bridging peripheral nerve defects. Autologous nerve grafts are the current gold standard for most clinical conditions. In selected cases, alternative types of conduits can be used. Although most efforts are today directed towards the development of artificial synthetic nerve guides, the use of non-nervous autologous tissue-based conduits (biological tubulization) can still be considered a valuable alternative to nerve autografts. In this paper we will overview the advancements in biological tubulization of nerve defects, with either mono-component or multiple-component autotransplants, with a special focus on the use of a vein segment filled with skeletal muscle fibers, a technique that has been widely investigated in our laboratory and that has already been successfully introduced in the clinical practice.

Keywords

Nerve reconstruction - Tissue engineering - Autotransplant - Tubulization - Vein - Skeletal muscle - Schwann cells

Full Text

References

References
1 Geuna S, Raimondo S, Ronchi G, Di Scipio F, Tos P, Czaja K, Fornaro M. Histology of the peripheral nerve and changes occurring during nerve regeneration. Int Rev Neurobiol 2009; 87: 27-46 19682632
2 Evans GR. Peripheral nerve injury: a review and approach to tissue engineered constructs. Anat Rec 2001; 263: 396-404 10.1002/ar.1120 11500817
3 Siemionow M, Uygur S, Ozturk C, Siemionow K. Techniques and materials for enhancement of peripheral nerve regeneration: a literature review. Microsurgery 2013; 33: 318-328 10.1002/micr.22104 23568681
4 Naff NJ, Ecklund JM. History of peripheral nerve surgery techniques. Neurosurg Clin N Am 2001; 12: 197-209 11175999
5 Millesi H. Interfascicular nerve grafting. Orthop Clin North Am 1970; 2: 419-435
6 Millesi H, Meissl G, Berger A. The interfascicular nerve-grafting of the median and ulnar nerves. J Bone Joint Surg Am 1972; 54: 727-750 4560075
7 Millesi H, Meissl G, Berger A. Further experience with interfascicular grafting of the median, ulnar, and radial nerves. J Bone Joint Surg Am 1976; 58: 209-218 767344
8 Deumens R, Bozkurt A, Meek MF, Marcus MA, Joosten EA, Weis J, Brook GA. Repairing injured peripheral nerves: bridging the gap. Prog Neurobiol 2010; 92: 245-276 10.1016/j.pneurobio.2010.10.002 20950667
9 Millesi H. Techniques for nerve grafting. Hand Clin 2000; 16: 73-91 10696578
10 Siemionow M, Brzezicki G. Current techniques and concepts in peripheral nerve repair. Int Rev Neurobiol 2009; 87: 141-172 19682637
11 Muratori L, Ronchi G, Raimondo S, Giacobini-Robecchi MG, Fornaro M, Geuna S. Can regenerated nerve fibers return to normal size? A long-term post-traumatic study of the rat median nerve crush injury model. Microsurgery 2012; 32: 383-387 10.1002/micr.21969 22434492
12 Fox IK, Brenner MJ, Johnson PJ, Hunter DA, Mackinnon SE. Axonal regeneration and motor neuron survival after microsurgical nerve reconstruction. Microsurgery 2012; 32: 552-562 10.1002/micr.22036 22806696
13 Battiston B, Raimondo S, Tos P, Gaidano V, Audisio C, Scevola A, Perroteau I, Geuna S. Tissue engineering of peripheral nerves. Int Rev Neurobiol 2009; 87: 227-249 19682640
14 Neuber G. Ein antiseptischer Dauerverband nach gründlicher Blutstillung. Arch Klin Chir 1879; 24: 314-330
15 Gluck T. Ueber neutroplastic auf dem wege de transplantation. Arch Klin Chir 1880; 25: 606-616
16 Vanlair C. De la régénération des nerfs périphériques par le procédé de la suture tubulaire. Arch Biol Paris 1882; 3: 379-496
17 Vanlair C. Nouvelles recherches expérimentales sur la régénération des nerfs. Arch Biol Paris 1885; 6: 127-235
18 Battiston B, Papalia I, Tos P, Geuna S. Peripheral nerve repair and regeneration research: a historical note. Int Rev Neurobiol 2009; 87: 1-7 19682630
19 Fields RD, Le Beau JM, Longo FM, Ellisman MH. Nerve regeneration through artificial tubular implants. Prog Neurobiol 1989; 33: 87-134 10.1016/0301-0082(89)90036-1 2678271
20 Bungner O. Ueber die degenerations un regenerationsvorgange an nerven nach verletzungen. Arch Mikrosk Anat 1891; 41: 146-178
21 Bethe A. Nwei neue methoden der ueberbruchung grossere nervenluchen. Dt Med Wschr 1916; 2: 1311-1314
22 Dustin AP. Les lesions postraumatiques des nerfs: contribution a l’histopathologie du systeme nerveux peripherique chez l’homme. Ambul Ocean 1917; 1: 71-161
23 Eden R. Sind zue ueberbruckung von nervendefekten die verfahren der tubulisation und der nervetransplantation zu empfehlen. Zentbl Chir 1917; 44: 138-140
24 Weiss P. Reunion of stumps of small nerves by tabulation instead of suture. Science 1941; 93: 67-68 10.1126/science.93.2403.67 17832859
25 Wrede L. Uberbrueckung eines nervendefektes mittels seidennaht und leben venenstueckes. Dt Med Wschr 1909; 35: 1125-1146
26 Foramitti C. Zur technik der nervennaht. Arch Klin Chir 1904; 73: 643-648
27 Gibb AG. Fascial nerve sleeve graft. J Lar Otol 1970; 84: 517-534
28 Matson D. Experiments on the bridging of gaps in several peripheral nerves of monkeys. J Neurosurg 1948; 5: 230-248 10.3171/jns.1948.5.3.0230 18857812
29 Nageotte J. Le processus de la cicatrisation des nerfs. CR Soc Biol Paris 1915; 78: 249-254
30 Platt H. On the results of bridging gaps in injured nerve trunks by autogenous fascial tubulization and autogenous nerve grafts. Br J Surg 1919; 7: 384-389 10.1002/bjs.1800072709
31 Szal GJ, Miller T. Surgical repair of the facial nerve branches: an analysis of different sheathing and suturing techniques. Arch Otolar 1975; 101: 160-165 10.1001/archotol.1975.00780320018004
32 Fullerton A. On the use of a sleeve of vein in nerve suture. Br Med J 1915; 2: 320-325 10.1136/bmj.2.2852.320 2303020 20767785
33 Chiu DT, Janecka I, Krizek TJ, Wolff M, Lovelace RE. Autogenous vein graft as a conduit for nerve regeneration. Surgery 1982; 91: 226-233 7058501
34 Risitano G, Cavallaro G, Lentini M. Autogenous vein and nerve grafts: a comparative study of nerve regeneration in the rat. J Hand Surg (Br) 1989; 14: 102-104 2926202
35 Walton RL, Brown RE, Matory Jr WE, Borah GL, Dolph JL. Autogenous vein graft repair of digital nerve defects in the finger: a retrospective clinical study. Plast Reconstr Surg 1989; 84: 944-949 10.1097/00006534-198912000-00013 2587658
36 Chiu DT, Strauch B. A prospective clinical evaluation of autogenous vein grafts used as a nerve conduit for distal sensory nerve defects of 3 cm or less. Plast Reconstr Surg 1990; 86: 928-934 10.1097/00006534-199011000-00015 2236318
37 Terzis JK, Kostas I. Vein grafts used as nerve conduits for obstetrical brachial plexus palsy reconstruction. Plast Reconstr Surg 2007; 120: 1930-1941 10.1097/01.prs.0000287391.12943.00 18090757
38 Flores LP. The use of autogenous veins for microsurgical repair of the sural nerve after nerve biopsy. Neurosurgery 2010; 66: 238-243 20489512
39 Jones RH. The use of vein grafts in the repair of the inferior alveolar nerve following surgery. Aust Dent J 2010; 55: 207-213 10.1111/j.1834-7819.2010.01215.x 20604766
40 Rinker B, Liau JY. A prospective randomized study comparing woven polyglycolic acid and autogenous vein conduits for reconstruction of digital nerve gaps. J Hand Surg [Am] 2011; 36: 775-781 10.1016/j.jhsa.2011.01.030 21489720
41 Chiu DT. Autogenous venous nerve conduits: a review. Hand Clin 1999; 15: 667-671 10563269
42 Fawcett JW, Keynes RJ. Muscle basal lamina: a new graft material for peripheral nerve repair. J Neurosurg 1986; 65: 354-363 10.3171/jns.1986.65.3.0354 3734886
43 Glasby MA, Gschmeissner SG, Hitchcock RJI, Huang CL-H, de Souza BA. A comparison of nerve regeneration through nerve and muscle grafts in rat sciatic nerve. Neuro-Orthopaedics 1986; 2: 21-28
44 Meek MF, Varejão AS, Geuna S. Use of skeletal muscle tissue in peripheral nerve repair: review of the literature. Tissue Eng 2004; 10: 1027-1036 10.1089/ten.2004.10.1027 15363160
45 Kraus H, Reisner H. Behandlungsergenisse von Verletungen pripherer Nerven mit besonderer Berücksichtigung der Schussverletzungen del Jahre 1919, 1927, und 1934. Arch Klin Chir 1940; 199: 318-336
46 Keynes RJ, Hopkins WG, Huang LH. Regeneration of mouse peripheral nerves in degenerating skeletal muscle: guidance by residual muscle fibre basement membrane. Brain Res 1984; 295: 275-281 10.1016/0006-8993(84)90976-4 6713188
47 Fawcett JW, Keynes RJ. Peripheral nerve regeneration. Annu Rev Neurosci 1990; 13: 43-60 10.1146/annurev.ne.13.030190.000355 2183684
48 Glasby MA, Fullerton AC, Lawson GM. Immediate and delayed nerve repair using freeze-thawed muscle autografts in complex nerve injuries. associated arterial injury. J Hand Surg Br 1998; 23: 354-359 9665525
49 Mountain RE, Glasby MA, Sharp JF, Murray JA. A morphological comparison of interposed freeze-thawed skeletal muscle autografts and interposed nerve autografts in the repair of the rat facial nerve. Clin Otolaryngol Allied Sci 1993; 18: 171-177 8365002
50 Fullarton AC, Glasby MA, Lawson GM. Immediate and delayed nerve repair using freeze-thawed muscle allografts. Associated long-bone fracture. J Hand Surg Br 1998; 23: 360-364 10.1016/S0266-7681(98)80058-2 9665526
51 Kong JM, Zhong SZ, Bo S, Zhu SX. Experimental study of bridging the peripheral nerve gap with skeletal muscle. Microsurgery 1986; 7: 183-189 10.1002/micr.1920070411 3796271
52 Norris RW, Glasby MA, Gattuso JM. Peripheral nerve repair in humans using muscle autografts: a new technique. J Bone Joint Surg (Br) 1988; 70: 530-533 3403592
53 Pereira JH, Bowden REM, Gattuso JM, Norris RW. Comparison of results of repair of digital nerves by denatured muscle grafts and end-to-end sutures. J Hand Surg (Br) 1991; 16: 519-523 10.1016/0266-7681(91)90107-Y 1791363
54 Pereira JH, Palande DD, Subramanian A, Narayanakumar TS, Curtis J, Turk JL. Denatured autologous muscle graft in leprosy. Lancet 1991; 338: 1239-1240 10.1016/0140-6736(91)92105-B 1682647
55 Calder JS, Norris RW. Repair of mixed peripheral nerves using muscleautografts: a preliminary communication. Br J Plast Surg 1993; 46: 557-569 10.1016/0007-1226(93)90105-K 8252261
56 Thomas M, Stirrat A, Birch R, Glasby MA. Freeze-thawed muscle grafting for painful cutaneous neuromas. J Bone Joint Surg (Br) 1994; 76: 474-486 8175858
57 Pereira JH, Bowden RE, Narayanakumar TS, Gschmeissner SE. Peripheral nerve reconstruction using denatured muscle autografts for restoring protective sensation in hands and feet of leprosy patients. Indian J Lepr 1996; 68: 83-91 8727118
58 Tang JB. Group fascicular vein grafts with interposition of nerve slices for long ulnar nerve defects: report of three cases. Microsurgery 1993; 14: 404-408 10.1002/micr.1920140611 8371689
59 Tang JB. Vein conduits with interposition of nerve tissue for peripheral nerve defects. J Reconstr Microsurg 1995; 11: 21-26 10.1055/s-2007-1006506 7714875
60 Keskin M, Akbas H, Uysal OA, Canan S, Ayyıldız M, Agar E, Kaplan S. Enhancement of nerve regeneration and orientation across a gap with a nerve graft within a vein conduit graft: a functional, stereological, and electrophysiological study. Plast Reconstr Surg 2004; 113: 1372-1379 10.1097/01.PRS.0000111596.61137.A1 15060349
61 Di Benedetto G, Zura G, Mazzucchelli R, Santinelli A, Scarpelli M, Bertani A. Nerve regeneration through a combined autologous conduit (vein plus acellular muscle grafts). Biomaterials 1998; 19: 173-181 10.1016/S0142-9612(97)00200-7 9678865
62 Couturier CA, Dauge MC, Henin D, Alnot JY, Masmejean EH. Nerve repair using a composite graft of vein and denatured skeletal muscle: morphologic analysis. J Reconstr Microsurg 2002; 18: 681-688 10.1055/s-2002-36500 12524587
63 Tos P, Battiston B, Nicolino S, Raimondo S, Fornaro M, Lee JM, Chirila L, Geuna S, Perroteau I. Comparison of fresh and predegenerated muscle-vein-combined guides for the repair of rat median nerve. Microsurgery 2007; 27: 48-55 10.1002/micr.20306 17211839
64 Brunelli G, Battiston B, Vigasio A, Brunelli G, Marocolo D. Bridging nerve defects with combined skeletal muscle and vein conduits. Microsurgery 1993; 14: 247-251 10.1002/micr.1920140407 8412634
65 Fornaro M, Tos P, Geuna S, Giacobini-Robecchi MG, Battiston B. Confocal imaging of Schwann cell migration along muscle-vein-combined grafts used to bridge nerve defects in the rat. Microsurgery 2001; 21: 143-155 10.1002/micr.1027 11494381
66 Geuna S, Raimondo S, Nicolino S, Boux E, Fornaro M, Tos P, Battiston B, Perroteau I. Schwann-cell proliferation in muscle-vein combined conduits for bridging rat sciatic nerve defects. J Reconstr Microsurg 2003; 19: 119-123 10.1055/s-2003-37818 12632312
67 Raimondo S, Nicolino S, Tos P, Battiston B, Giacobini-Robecchi MG, Perroteau I, Geuna S. Schwann cell behavior after nerve repair by means of tissue-engineered muscle-vein combined guides. J Comp Neurol 2005; 489: 249-259 10.1002/cne.20625 15984006
68 Geuna S, Nicolino S, Raimondo S, Gambarotta G, Battiston B, Tos P, Perroteau I. Nerve regeneration along bioengineered scaffolds. Microsurgery 2007; 27: 429-438 10.1002/micr.20383 17596863
69 Nicolino S, Panetto A, Raimondo S, Gambarotta G, Guzzini M, Fornaro M, Battiston B, Tos P, Geuna S, Perroteau I. Denervation and reinnervation of adult skeletal muscle modulate mRNA expression of neuregulin-1 and ErbB receptors. Microsurgery 2009; 29: 464-472 10.1002/micr.20636 19296522
70 Tos P, Battiston B, Geuna S, Giacobini-Robecchi MG, Hill MA, Lanzetta M, Owen ER. Tissue specificity in rat peripheral nerve regeneration through combined skeletal muscle and vein conduit grafts. Microsurgery 2000; 20: 65-71 10.1002/(SICI)1098-2752(2000)20:2<65::AID-MICR4>3.0.CO;2-4 10702739
71 Tos P, Calcagni M, Gigo-Benato D, Boux E, Geuna S, Battiston B. Use of muscle-vein-combined Y-chambers for repair of multiple nerve lesions: experimental results. Microsurgery 2004; 24: 459-464 10.1002/micr.20064 15378575
72 Lee JM, Tos P, Raimondo S, Fornaro M, Papalia I, Geuna S, Giacobini-Robecchi MG. Lack of topographic specificity in nerve fiber regeneration of rat forelimb mixed nerves. Neuroscience 2007; 144: 985-990 10.1016/j.neuroscience.2006.11.001 17157991
73 Battiston B, Tos P, Cushway T, Geuna S. Nerve repair by means of vein filled with muscle grafts: I: clinical results. Microsurgery 2000; 20: 32-36 10.1002/(SICI)1098-2752(2000)20:1<32::AID-MICR6>3.0.CO;2-D 10617879
74 Tos P, Battiston B, Ciclamini D, Geuna S, Artiaco S. Primary repair of crush nerve injuries by means of biological tubulization with muscle-vein-combined grafts. Microsurgery 2012; 32: 358-363 10.1002/micr.21957 22422438
75 Battiston B, Geuna S, Ferrero M, Tos P. Nerve repair by means of tubulization: literature review and personal clinical experience comparing biological and synthetic conduits for sensory nerve repair. Microsurgery 2005; 25: 258-267 10.1002/micr.20127 15934044
76 Marcoccio I, Vigasio A. Muscle-in-vein nerve guide for secondary reconstruction in digital nerve lesions. J Hand Surg [Am] 2010; 35: 1418-1426 10.1016/j.jhsa.2010.05.019 20807618
77 Ansselin AD, Fink T, Dawey DF. Peripheral nerve regeneration through nerve guides seeded with adult Schwann cells. Neuropathol Appl Neurobiol 1997; 23: 387-398 10.1111/j.1365-2990.1997.tb01313.x 9364464
78 Strauch B, Rodriguez DM, Diaz J, Yu HL, Kaplan G, Weinstein DE. Autologous Schwann cells drive regeneration through a 6-cm autogenous venous nerve conduit. J Reconstr Microsurg 2001; 17: 589-595 10.1055/s-2001-18812 11740653
79 Cheng B, Chen Z. Fabricating autologous tissue to engineer artificial nerve. Microsurgery 2002; 22: 133-137 10.1002/micr.21740 12111977
80 Zhang F, Blain B, Beck J, Zhang J, Chen Z, Chen ZW, Lineaweaver WC. Autogenous venous graft with one-stage prepared Schwann cells as a conduit for repair of long segmental nerve defects. J Reconstr Microsurg 2002; 18: 295-300 10.1055/s-2002-30186 12022035
81 Dubovy P, Svizenska I. Denervated skeletal muscle stimulates migration of Schwann cells from the distal stump of transected peripheral nerve: an in vivo study. Glia 1994; 12: 99-107 10.1002/glia.440120203 7868190
82 Nijhuis TH, Bodar CW, van Neck JW, Walbeehm ET, Siemionow M, Madajka M, Cwykiel J, Blok JH, Hovius SE. Natural conduits for bridging a 15-mm nerve defect: comparison of the vein supported by muscle and bone marrow stromal cells with a nerve autograft. J Plast Reconstr Aesthet Surg 2013; 66: 251-259 10.1016/j.bjps.2012.09.011 23063384
83 Geuna S, Borrione P, Fornaro M, Giacobini-Robecchi MG. Adult stem cells and neurogenesis: historical roots and state of the art. Anat Rec 2001; 265: 132-141 10.1002/ar.1135 11458328
84 Tohill MP, Terenghi G. Stem cell plasticity and therapy for injuries of the peripheral nervous system. Biotechnol Appl Biochem 2004; 40: 17-24 10.1042/BA20030173 15270703
85 Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci 2001; 14: 1771-1776 10.1046/j.0953-816x.2001.01814.x 11860471
86 Tomita K, Madura T, Sakai Y, Yano K, Terenghi G, Hosokawa K. Glial differentiation of human adipose-derived stem cells: implications for cell-based transplantation therapy. Neuroscience 2013; 236: 55-65 23370324
87 Wang X, Luo E, Li Y, Hu J. Schwann-like mesenchymal stem cells within vein graft facilitate facial nerve regeneration and remyelination. Brain Res 2011; 1383: 71-80 21295556
88 Pu LL, Syed SA, Reid M, Patwa H, Goldstein JM, Forman DL, Thomson JG. Effects of nerve growth factor on nerve regeneration through a vein graft across a gap. Plast Reconstr Surg 1999; 104: 1379-1385 10.1097/00006534-199910000-00021 10513921
89 Gravvanis AI, Tsoutsos DA, Tagaris GA, Papalois AE, Patralexis CG, Iconomou TG, Panayotou PN, Ioannovich JD. Beneficial effect of nerve growth factor-7S on peripheral nerve regeneration through inside-out vein grafts: an experimental study. Microsurgery 2004; 24: 408-415 10.1002/micr.20055 15378588
90 Haastert K, Grothe C. Gene therapy in peripheral nerve reconstruction approaches. Curr Gene Ther 2007; 7: 221-228 10.2174/156652307780859035 17584040
91 Tannemaat MR, Boer GJ, Eggers R, Malessy MJ, Verhaagen J. From microsurgery to nanosurgery: how viral vectors may help repair the peripheral nerve. Prog Brain Res 2009; 175: 173-186 19660656
92 Zacchigna S, Giacca M. Gene therapy perspectives for nerve repair. Int Rev Neurobiol 2009; 87: 381-392 19682649
93 Pereira Lopes FR, Lisboa BC, Frattini F, Almeida FM, Tomaz MA, Matsumoto PK, Langone F, Lora S, Melo PA, Borojevic R, Han SW, Martinez AM. Enhancement of sciatic nerve regeneration after vascular endothelial growth factor (VEGF) gene therapy. Neuropathol Appl Neurobiol 2011; 37: 600-612 10.1111/j.1365-2990.2011.01159.x 21208251
94 Moimas S, Novati F, Ronchi G, Zacchigna S, Fregnan F, Zentilin L, Papa G, Giacca M, Geuna S, Perroteau I, Arnež ZM, Raimondo S. Effect of vascular endothelial growth factor gene therapy on post-traumatic peripheral nerve regeneration and denervation-related muscle atrophy. Gene Ther 2013;
95 Raimondo S, Fornaro M, Tos P, Battiston B, Giacobini-Robecchi MG, Geuna S. Perspectives in regeneration and tissue engineering of peripheral nerves. Ann Anat 2011; 193: 334-340 10.1016/j.aanat.2011.03.001 21474294
96 Geuna S, Tos P, Battiston B. Emerging issues in peripheral nerve repair. Neural Reg Res 2012; 7: 2267-2272
97 Papalia I, Raimondo S, Ronchi G, Magaudda L, Giacobini-Robecchi MG, Geuna S. Repairing nerve gaps by vein conduits filled with lipoaspirate-derived entire adipose tissue hinders nerve regeneration. Ann Anat 2013; 195: 225-230 10.1016/j.aanat.2012.10.012 23287534

Update on nerve repair by biological tubulization[*]

Update on nerve repair by biological tubulization^[*]