Collagen nerve conduits promote enhanced axonal regeneration, Schwann cell Association, and neovascularization compared to silicone conduits

Tissue Engineering - Part A

Volumn 15, Issue 8, 2009, Pages 1975-1988

  Kemp, Stephen W P ^a   Syed, Shahbaz ^a   Walsh, Sarah K ^a   Zochodne, Douglas W ^a   Midha, Rajiv ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABERRATIONS; CELL MEMBRANES; SILICONES;

AXONAL REGENERATION; COLLAGEN NERVE CONDUITS; GAP MODEL; MYELINATION; NEOVASCULARIZATION; NERVE CONDUITS; NERVE GUIDE; NERVE GUIDE CONDUITS; PERIPHERAL NERVE REGENERATION; RAT SCIATIC NERVE; SCHWANN CELLS; SILICONE CONDUIT; TIME POINTS; VASCULARIZATION;

COLLAGEN;

COLLAGEN TYPE 1; SILICONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; MYELINATION; NEOVASCULARIZATION (PATHOLOGY); NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SCHWANN CELL; SCIATIC NERVE;

RATTUS;

ANIMALS; AXONS; COLLAGEN; DISEASE MODELS, ANIMAL; MYELIN SHEATH; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE REGENERATION; PERIPHERAL NERVES; RATS; RATS, INBRED LEW; SCHWANN CELLS; SILICONES; TISSUE ENGINEERING;

EID: 68749088467     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0338     Document Type: Article

References (64)

1. Lundborg, G. Nerve Injury and Repair: Regeneration, Reconstruction, and Cortical Remodeling. Philadelphia, PA: Elsevier, 2004.
2. Ashley, W.W., Jr., Baty, J.D., Hollander, T., Noetzel, M.J., and Park, T.S. Long-term motor outcome analysis using a motor score composite following surgical brachial plexus repair. J Neurosurg 106, 276, 2007.
3. Secer, H.I., Daneyemez, M., Tehli, O., Gonul, E., and Izci, Y. The clinical, electrophysiologic, and surgical characteristics of peripheral nerve injuries caused by gunshot wounds in adults: a 40-year experience. Surg Neurol 69, 143, 2008.
4. Kelsey, J.L., Praemer, A., Nelson, L., Felberg, A., and Rice, L.M. Upper extremity disorders. Frequency, impact, and cost. New York, NY: Churchill Livingstone, 1997.
5. Dahlin, L.B., and Lundborg, G. Experimental nerve grafting: towards future solutions of a clinical problem. J Hand Surg [Am] 23, 165, 1998.
6. Nichols, C.M., Brenner, M.J., Fox, I.K., Tung, T.H., Hunter, D.A., Rickman, S.R., and Mackinnon, S.E. Effects of motor versus sensory nerve grafts on peripheral nerve regeneration. Exp Neurol 190, 347, 2004.
7. Pfister, L.A., Papaloizos, M., Merkle, H.P., and Gander, B. Nerve conduits and growth factor delivery in peripheral nerve repair. J Peripher Nerv Syst 12, 65, 2007.
8. Willerth, S.M., and Sakiyama-Elbert, S.E. Approaches to neural tissue engineering using scaffolds for drug delivery. Adv Drug Delivery Rev 59, 325, 2007.
9. Lundborg, G., Dahlin, L.B., Danielsen, N., Gelberman, R.H., Longo, F.M., Powell, H.C., and Varon, S. Nerve regeneration in silicone chambers: influence of gap length and of distal stump components. Exp Neurol 76, 361, 1982.
10. Longo, F.M., Manthorpe, M., Skaper, S.D., Lundborg, G., and Varon, S. Neuronotrophic activities accumulate in vivo within silicone nerve regeneration chambers. Brain Res 261, 109, 1983.
11. Lundborg, G., Gelberman, R.H., Longo, F.M., Powell, H.C., and Varon, S. In vivo regeneration of cut nerves encased in silicone tubes: growth across a six-millimeter gap. J Neuro-pathol Exp Neurol 41, 412, 1982.
12. Longo, F.M., Hayman, E.G., Davis, G.E., Ruoslahti, E., Engvall, E., Manthorpe, M., and Varon, S. Neurite-promoting factors and extracellular matrix components accumulating in vivo within nerve regeneration chambers. Brain Res 309, 105, 1984.
13. Lundborg, G., Dahlin, L.B., and Danielsen, N. Ulnar nerve repair by the silicone chamber technique. Case report. Scand J Plast Reconstr Surg Hand Surg 25, 79, 1991.
14. Merle, M., Dellon, A.L., Campbell, J.N., and Chang, P.S. Complications from silicon-polymer intubulation of nerves. Microsurgery 10, 130, 1989.
15. Archibald, S.J., Krarup, C., Shefner, J., Li, S.-T., and Madison, R.D. A collagen-based nerve guide conduit for peripheral nerve repair: an electrophysiological study of nerve regeneration in rodents and nonhuman primates. J Comp Neurol 306, 685, 1991.
16. Archibald, S.J., Shefner, J., Krarup, C., and Madison, R.D. Monkey median nerve repaired by nerve graft or collagen nerve guide tube. J Neurosci 15, 4109, 1995.
17. Krarup, C., Archibald, S.J., and Madison, R.D. Factors that influence peripheral nerve regeneration: an electrophysiological study of the monkey median nerve. Ann Neurol 51, 69, 2002.
18. Stang, F., Fansa, H., Wolf, G., and Keilhoff, G. Collagen nerve conduits - assessment of biocompatibility and axonal regeneration. Biomed Mater Eng 15, 3, 2005.
19. Cheng, C., and Zochodne, D.W. In vivo proliferation, migration and phenotypic changes of Schwann cells in the presence of myelinated fibers. Neuroscience 115, 321, 2002.
20. Chen, Y.Y., McDonald, D., Cheng, C., Magnowski, B., Durand, J., and Zochodne, D.W. Axon and Schwann cell partnership during nerve regrowth. J Neuropathol Exp Neurol 64, 613, 2005.
21. Carroll, S.L., Miller, M.L., Frohnert, P.W., Kim, S.S., and Corbett, J.A. Expression of neuregulins and their putative receptors, ErbB2 and ErbB3, is induced during Wallerian degeneration. J Neurosci 17, 1642, 1997.
22. Pellegrino, R.G., and Spencer, P.S. Schwann cell mitosis in response to regenerating peripheral axons in vivo. Brain Res 341, 16, 1985.
23. Fu, S.Y., and Gordon, T. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14, 67, 1997.
24. Podhajsky, R.J., and Myers, R.R. The vascular response to nerve transection: neovascularization in the silicone nerve regeneration chamber. Brain Res 662, 88, 1994.
25. Hobson, M.I., Brown, R., Green, C.J., and Terenghi, G. Interrelationships between angiogenesis and nerve regeneration: a histochemical study. Br J Plast Surg 50, 125, 1997.
26. Hoke, A., Sun, H.S., Gordon, T., and Zochodne, D.W. Do denervated peripheral nerve trunks become ischemic? The impact of chronic denervation on vasa nervorum. Exp Neurol 172, 398, 2001.
27. Weddell, G. Axonal regeneration in cutaneous nerve plexuses. J Anat 77, 49, 1942.
28. Williams, L.R., Longo, F.M., Powell, H.C., Lundborg, G., and Varon, S. Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay. J Comp Neurol 218, 460, 1983.
29. Li, S.T., Archibald, S.J., Krarup, C., and Madison, R.D. Peripheral nerve repair with collagen conduits. Clin Mater 9, 195, 1992.
30. Bray, R.C., Fisher, A.W., and Frank, C.B. Fine vascular anatomy of adult rabbit knee ligaments. J Anat 172, 69, 1990.
31. Zochodne, D.W., and Nguyen, C. Angiogenesis at the site of neuroma formation in transected peripheral nerve. J Anat 190, 23, 1997.
32. Widmer, M.S., Gupta, P.K., Lu, L., Meszlenyi, R.K., Evans, G.R., Brandt, K., Savel, T., Gurlek, A., Patrick Jr., C.W., and Mikos, AG. Manufacture of porous biodegradable polymer conduits by an extrusion process for guided tissue regeneration. Biomaterials 19, 1945, 1998.
33. Evans, G.R., Brandt, K., Widmer, M.S., Lu, L., Meszlenyi, R.K., Gupta, P.K., Mikos, A.G., Hodges, J., Williams, J., Gurlek, A., Nabawi, A., Lohman, R., and Patrick Jr., C.E. In vivo evaluation of poly(1-lactic acid) porous conduits for peripheral nerve regeneration. Biomaterials 20, 1109, 1999.
34. Jenq, C.B., and Coggeshall, R.E. Permeable tubes increase the length of the gap that regenerating axons can span. Brain Res 408, 239, 1987.
35. Katayama, Y., Montenegro, R., Freier, T., Midha, R., Belkas, J., and Shoichet, M.S. Coil-reinforced hydrogel tubes promote nerve regeneration equivalent to that of nerve auto-grafts. Biomaterials, 27, 505, 2005.
36. Rodriguez, F.J., Gomez, N., Perego, G., and Navarro, X. Highly permeable polylactide-caprolactone nerve guides enhance peripheral nerve regeneration through long gaps. Biomaterials 20, 1489, 1999.
37. Kim, D.H., Connolly, S.E., Zhao, S., Beuerman, R.W., Voorhies, R.M., and Kline, D.G. Comparison of macropore, semipermeable, and nonpermeable collagen conduits in nerve repair. J Reconstr Microsurg 9, 415, 1993.
38. Aebischer, P., Guenard, V., Winn, S.R., Valentini, R.F., and Galletti, P.M. Blind-ended semipermeable guidance channels support peripheral nerve regeneration in the absence of a distal nerve stump. Brain Res 454, 179, 1988.
39. Longo, F.M., Skaper, S.D., Manthorpe, M., Williams, L.R., Lundborg, G., and Varon, S. Temporal changes of neuro-notrophic activities accumulating in vivo within nerve regeneration chambers. Exp Neurol 81, 756, 1983.
40. den Dunnen, W.F., Stokroos, I., Blaauw, E.H., Holwerda, A., Pennings, A.J., Robinson, P.H., and Schakenraad, J.M. Light-microscopic and electron-microscopic evaluation of short-term nerve regeneration using a biodegradable poly(DL-lactide-epsilon-caprolacton) nerve guide. J Biomed Mater Res 31, 105, 1996.
41. Chamberlain, L.J., Yannas, I.V., Arrizabalaga, A., Hsu, H.P., Norregaard, T.V., and Spector, M. Early peripheral nerve healing in collagen and silicone tube implants: myofibro-blasts and the cellular response. Biomaterials 19, 1393, 1998.
42. Chamberlain, L.J., Yannas, I.V., Hsu, H.P., and Spector, M. Connective tissue response to tubular implants for peripheral nerve regeneration: the role of myofibroblasts. J Comp Neurol 417, 415, 2000.
43. Yannas, I.V., Zhang, M., and Spilker, M.H. Standardized criterion to analyze and directly compare various materials and models for peripheral nerve regeneration. J Biomater Sci Polym Ed 18, 943, 2007.
44. Yannas, I.V. Tissue and Organ Regeneration in Adults. New York, NY: Springer, 2001.
45. Derby, A., Engleman, V.W., Frierdich, G.E., Neises, G., Rapp, S.R., and Roufa, D.G. Nerve growth factor facilitates regeneration across nerve gaps: morphological and behavioral studies in rat sciatic nerve. Exp Neurol 119, 176, 1993.
46. de Ruiter, G.C., Onyeneho, I.A., Liang, E.T., Moore, M.J., Knight, A.M., Malessy, M.J., Spinner, R.J., Lu, L., Currier, B.L., Yaszemski, M.J., and Windebank, A.J. Methods for in vitro characterization of multichannel nerve tubes. J Biomed Mater Res A 84, 643, 2008.
47. Scherer, S.S., and Salzer, J.L. Axon-Schwann cell interactions during peripheral nerve degeneration and regeneration. In: Jessen, K.R., and Richardson, W.D., eds. Glial Cell Development. Oxford, UK: Bios Scientific, 1996, 169-196.
48. Mirsky, R., and Jessen, K.R. The neurobiology of Schwann cells. Brain Pathol 9, 293, 1999.
49. Sieminski, A.L., and Gooch, K.J. Biomaterial-microvasculature interactions. Biomaterials 21, 2232, 2000.
50. Lindholm, D., Heumann, R., Meyer, M., and Thoenen, H. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature 330, 658, 1987.
51. Dickson, B.J., and Senti, K.A. Axon guidance: growth cones make an unexpected turn. Curr Biol 12, R218, 2002.
52. Moore, K., MacSween, M., and Shoichet, M. Immobilized concentration gradients of neurotrophic factors guide neurite outgrowth of primary neurons in macroporous scaffolds. Tissue Eng 12, 267, 2006.
53. Generini, S., Tuveri, M.A., Matucci, C.M., Mastinu, F., Manni, L., and Aloe, L. Topical application of nerve growth factor in human diabetic foot ulcers. A study of three cases. Exp Clin Endocrinol Diabetes 112, 542, 2004.
54. Tammela, T., Enholm, B., Alitalo, K., and Paavonen, K. The biology of vascular endothelial growth factors. Cardiovasc Res 65, 550, 2005.
55. Li, W.W., Talcott, K.E., Zhai, A.W., Kruger, E.A., and Li, V.W. The role of therapeutic angiogenesis in tissue repair and regeneration. Adv Skin Wound Care 18, 491, 2005.
56. Hobson, M.I., Green, C.J., and Terenchi, G. VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat 197, 591, 2000.
57. Carmeliet, P., and Storkebaum, E. Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin Cell Dev Biol 13, 39, 2002.
58. Xu, X., Yee, W.C., Hwang, P.Y., Yu, H., Wan, A.C., Gao, S., Boon, K.L., Mao, H.Q., Leong, K.W., and Wang, S. Peripheral nerve regeneration with sustained release of poly(pho-sphoester) microencapsulated nerve growth factor within nerve guide conduits. Biomaterials 24, 2405, 2003.
59. Dowsing, B.J., Hayes, A., Bennett, T.M., Morrison, W.A., and Messina, A. Effects of LIF dose and laminin plus fibronectin on axotomized sciatic nerves. Muscle Nerve 23, 1356, 2000.
60. Chamberlain, L.J., Yannas, I.V., Hsu, H.P., Strichartz, G.R., and Spector, M. Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen-GAG matrix in a ten-millimeter gap. J Neurosci Res 60, 666, 2000.
61. Matsumoto, K., Ohnishi, K., Kiyotani, T., Sekine, T., Ueda, H., Nakamura, T., Endo, K., and Shimizu, Y. Peripheral nerve regeneration across an 80-mm gap bridged by a poly-glycolic acid (PGA)-collagen tube filled with laminin-coated collagen fibers: a histological and electrophysiological evaluation of regenerated nerves. Brain Res 868, 315, 2000.
62. Evans, G.R., Brandt, K., Katz, S., Chauvin, P., Otto, L., Bogle, M., Wang, B., Meszlenyi, R.K., Lu, L., Mikos, A.G., and Patrick Jr., C.W. Bioactive poly(1-lactic acid) conduits seeded with Schwann cells for peripheral nerve regeneration. Biomaterials 23, 841, 2002.
63. Waitayawinyu, T., Parisi, D.M., Miller, B., Luria, S., Morton, H.J., Chin, S.H., and Trumble, T.E. A comparison of polyglycolic acid versus type 1 collagen bioabsorbable nerve conduits in a rat model: an alternative to autografting. J Hand Surg [Am] 32, 1521, 2007.
64. Chen, Y.S., Hsieh, C.L., Tsai, C.C., Chen, T.H., Cheng, W.C., Hu, C.L., and Yao, C.H. Peripheral nerve regeneration using silicone rubber chambers filled with collagen, laminin and fibronectin. Biomaterials 21, 1541, 2000.