Comparison and characterization of multiple biomaterial conduits forperipheral nerve repair

Biomaterials

Volumn 34, Issue 34, 2013, Pages 8630-8639

  Daly, William T ^a   Knight, Andrew M ^b   Wang, Huan ^c   de Boer, Ralph ^c   Giusti, Guilherme ^c   Dadsetan, Mahrokh ^c   Spinner, Robert J ^c   Yaszemski, Michael J ^c   Windebank, Anthony J ^b  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b MAYO CLINIC ROCHESTER   (United States)

^c MAYO CLINIC   (United States)

Author keywords

Functional outcomes; Nerve conduits; Polymer; Scaffolds; Tissue engineering

Indexed keywords

ASSESSMENT TECHNIQUE; FUNCTIONAL OUTCOMES; INDEPENDENT PARAMETERS; NERVE CONDUITS; NERVE REGENERATION; POLY(CAPROLACTONE FUMARATE); POLY(LACTIC-CO-GLYCOLIC ACID); STATISTICAL DIFFERENCES;

BIOLOGICAL MATERIALS; COPOLYMERS; HYDROGELS; OPTIMIZATION; POLYETHYLENE GLYCOLS; POLYMERS; REPAIR; SCAFFOLDS; TISSUE ENGINEERING; TUBES (COMPONENTS);

SCAFFOLDS (BIOLOGY);

BIOMATERIAL; COLLAGEN; FIBRIN; MACROGOL; POLYCAPROLACTONE; POLYCAPROLACTONE FUMARATE; POLYGLACTIN; SILK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOGRAFT; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; HYDROGEL; NERVE INJURY; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; RAT; SCIATIC NERVE; STATISTICAL ANALYSIS; SURFACE PROPERTY; SURGICAL TECHNIQUE; TISSUE ENGINEERING;

ANIMALIA; RATTUS;

FUNCTIONAL OUTCOMES; NERVE CONDUITS; POLYMER; SCAFFOLDS; TISSUE ENGINEERING;

ANIMALS; BIOCOMPATIBLE MATERIALS; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; LACTIC ACID; NERVE REGENERATION; POLYESTERS; POLYGLYCOLIC ACID; PROSTHESES AND IMPLANTS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84882846369     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.07.086     Document Type: Article

References (67)

1. Pabari A., Yang S.Y., Seifalian A.M., Mosahebi A. Modern surgical management of peripheral nerve gap. JPlast Reconstr Aesthet Surg 2010, 63:1941-1948.
2. Belkas S.J., Shoichet S.M., Midha Rajiv Peripheral nerve regeneration through guidance tubes. Neurol Res 2004, 26:10.
3. Alluin O., Wittmann C., Marqueste T., Chabas J.F., Garcia S., Lavaut M.N., et al. Functional recovery after peripheral nerve injury and implantation of a collagen guide. Biomaterials 2009, 30:363-373.
4. Daly W., Yao L., Zeugolis D., Windebank A., Pandit A. Abiomaterials approach to peripheral nerve regeneration: bridging the peripheral nerve gap and enhancing functional recovery. JR Soc Interface 2012, 9:202-221.
5. Ansselin A.D., Davey D.F. Axonal regeneration through peripheral nerve grafts: the effect of proximo-distal orientation. Microsurgery 1988, 9:103-113.
6. Nichols C.M., Brenner M.J., Fox I.K., Tung T.H., Hunter D.A., Rickman S.R., et al. Effects of motor versus sensory nerve grafts on peripheral nerve regeneration. Exp Neurol 2004, 190:347-355.
7. Siemionow M., Sonmez E. Nerve allograft transplantation: a review. JReconstr Microsurg 2007, 23:511-520.
8. Karabekmez F., Duymaz A., Moran S. Early clinical outcomes with the use of decellularized nerve allograft for repair of sensory defects within the hand. Hand (New York, NY) 2009, 4:245-249.
9. Mackinnon S.E., Doolabh V.B., Novak C.B., Trulock E.P. Clinical outcome following nerve allograft transplantation. Plast Reconstr Surg 2001, 107:1419-1429.
10. Mukhatyar V., Karumbaiah L., Yeh J., Bellamkonda R. Tissue engineering strategies designed to realize the endogenous regenerative potential of peripheral nerves. Adv Mater 2009, 21:4670-4679.
11. Lundborg G., Dahlin L.B., Danielsen N., Gelberman R.H., Longo F.M., Powell H.C., et al. Nerve regeneration in silicone chambers: influence of gap length and of distal stump components. Exp Neurol 1982, 76:361-375.
12. Williams L.R., Longo F.M., Powell H.C., Lundborg G., Varon S. Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: parameters for a bioassay. JComp Neurol 1983, 218:460-470.
13. Varon S., Williams L.R. Peripheral nerve regeneration in a silicone model chamber: cellular and molecular aspects. Peripher Nerve Repair Regen 1986, 1:9-25.
14. Jenq C.-B., Coggeshall R.E. Regeneration of transected rat sciatic nerves after using isolated nerve fragments as distal inserts in silicone tubes. Exp Neurol 1986, 91:154-162.
15. Abu-Rub M.T., Billiar K.L., van Es M.H., Knight A., Rodriguez B.J., Zeugolis D.I., et al. Nano-textured self-assembled aligned collagen hydrogels promote directional neurite guidance and overcome inhibition by myelin associated glycoprotein. Soft Matter 2011, 7:2770-2781.
16. Ahmed M.R., Vairamuthu S., Shafiuzama M., Basha S.H., Jayakumar R. Microwave irradiated collagen tubes as a better matrix for peripheral nerve regeneration. Brain Res 2005, 1046:55-67.
17. Archibald S., Krarup C., Shefner J., Li S., Madison R. Acollagen-based nerve guide conduit for peripheral nerve repair: an electrophysiological study of nerve regeneration in rodents and nonhuman primates. JComp Neurol 1991, 306:685-696.
18. di Summa P.G., Kalbermatten D.F., Pralong E., Raffoul W., Kingham P.J., Terenghi G. Long-term invivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience 2011, 181:278-291.
19. Kalbermatten D., Kingham P., Mahay D., Mantovani C., Pettersson J., Raffoul W., et al. Fibrin matrix for suspension of regenerative cells in an artificial nerve conduit. JPlast Reconstr Aesthet Surg 2008, 61:669-675.
20. Pettersson J., Kalbermatten D., McGrath A., Novikova L.N. Biodegradable fibrin conduit promotes long-term regeneration after peripheral nerve injury in adult rats. JPlast Reconstr Aesthet Surg 2010, 63:1893-1899.
21. Ding F., Wu J., Yang Y., Hu W., Zhu Q., Tang X., et al. Use of tissue-engineered nerve grafts consisting of a chitosan/poly(lactic-co-glycolic acid)-based scaffold included with bone marrow mesenchymal cells for bridging 50-mm dog sciatic nerve gaps. Tissue Eng Part A 2010, 16:3779-3790.
22. Fan W., Gu J., Hu W., Deng A., Ma Y., Liu J., et al. Repairing a 35-mm-long median nerve defect with a chitosan/PGA artificial nerve graft in the human: a case study. Microsurgery 2008, 28:238-242.
23. Freier T., Montenegro R., Shan Koh H., Shoichet M.S. Chitin-based tubes for tissue engineering in the nervous system. Biomaterials 2005, 26:4624-4632.
24. Evans G.R., Brandt K., Katz S., Chauvin P., Otto L., Bogle M., et al. Bioactive poly(L-lactic acid) conduits seeded with Schwann cells for peripheral nerve regeneration. Biomaterials 2002, 23:841-848.
25. Koh H.S., Yong T., Teo W.E., Chan C.K., Puhaindran M.E., Tan T.C., et al. Invivo study of novel nanofibrous intra-luminal guidance channels to promote nerve regeneration. JNeural Eng 2010, 7:046003.
26. Ngo T.-T.B., Waggoner P.J., Romero A.A., Nelson K.D., Eberhart R.C., Smith G.M. Poly(L-Lactide) microfilaments enhance peripheral nerve regeneration across extended nerve lesions. JNeurosci Res 2003, 72:227-238.
27. de Ruiter G.C., Spinner R.J., Malessy M.J., Moore M.J., Sorenson E.J., Currier B.L., et al. Accuracy of motor axon regeneration across autograft, single-lumen, and multichannel poly(lactic-co-glycolic acid) nerve tubes. Neurosurgery 2008, 63:144-153. [discussion 53-55].
28. Yao L., Wang S., Cui W., Sherlock R., Oconnell C., Damodaran G., et al. Effect of functionalized micropatterned PLGA on guided neurite growth. Acta Biomater 2009, 5:580-588.
29. Schnell E., Klinkhammer K., Balzer S., Brook G., Klee D., Dalton P., et al. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-ε-caprolactone and a collagen/poly-ε-caprolactone blend. Biomaterials 2007, 28:3012-3025.
30. Sun M., Kingham P.J., Reid A.J., Armstrong S.J., Terenghi G., Downes S. Invitro and invivo testing of novel ultrathin PCL and PCL/PLA blend films as peripheral nerve conduit. JBiomed Mater Res 2010, 93:1470-1481.
31. Hobson M.I., Green C.J., Terenghi G. VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. JAnat 2000, 197:591-605.
32. Haastert K., Lipokatić E., Fischer M., Timmer M., Grothe C. Differentially promoted peripheral nerve regeneration by grafted Schwann cells over-expressing different FGF-2 isoforms. Neurobiol Dis 2006, 21:138-153.
33. de Boer R., Borntraeger A., Knight A.M., Hebert-Blouin M.N., Spinner R.J., Malessy M.J., et al. Short- and long-term peripheral nerve regeneration using a poly-lactic-co-glycolic-acid scaffold containing nerve growth factor and glial cell line-derived neurotrophic factor releasing microspheres. JBiomed Mater Res 2012, 100:2139-2146.
34. Deister C., Schmidt C.E. Optimizing neurotrophic factor combinations for neurite outgrowth. JNeural Eng 2006, 3:172.
35. Fine E.G., Decosterd I., Papaloizos M., Zurn A.D., Aebischer P. GDNF and NGF released by synthetic guidance channels support sciatic nerve regeneration across a long gap. Eur J Neurosci 2002, 15:589-601.
36. Kokai L.E., Bourbeau D., Weber D., McAtee J., Marra K.G. Sustained growth factor delivery promotes axonal regeneration in long gap peripheral nerve repair. Tissue Eng 2011, 17:1263-1275.
37. Itoh S., Takakuda K., Samejima H., Ohta T., Shinomiya K., Ichinose S. Synthetic collagen fibers coated with a synthetic peptide containing the YIGSR sequence of laminin to promote peripheral nerve regeneration invivo. JMater Sci Mater Med 1999, 10:129-134.
38. Itoh S. Hydroxyapatite-coated tendon chitosan tubes with adsorbed laminin peptides facilitate nerve regeneration invivo. Brain Res 2003, 993:111-123.
39. Wang W., Itoh S., Matsuda A., Aizawa T., Demura M., Ichinose S., et al. Enhanced nerve regeneration through a bilayered chitosan tube: the effect of introduction of glycine spacer into the CYIGSR sequence. JBiomed Mater Res A 2008, 85:919-928.
40. Yao L., Damodaran G., Nikolskaya N., Gorman A.M., Windebank A., Pandit A. The effect of laminin peptide gradient in enzymatically cross-linked collagen scaffolds on neurite growth. JBiomed Mater Res A 2010, 92A:484-492.
41. Guenard V., Kleitman N., Morrissey T., Bunge R., Aebischer P. Syngeneic Schwann cells derived from adult nerves seeded in semipermeable guidance channels enhance peripheral nerve regeneration. JNeurosci 1992, 12:3310-3320.
42. Hadlock T., Sundback C., Hunter D., Cheney M., Vacanti J.P. Apolymer foam conduit seeded with Schwann cells promotes guided peripheral nerve regeneration. Tissue Eng 2000, 6:119-127.
43. Kaewkhaw R., Scutt A.M., Haycock J.W. Anatomical site influences the differentiation of adipose-derived stem cells for Schwann-cell phenotype and function. Glia 2011, 59:734-749.
44. Kalbermatten D.F., Erba P., Mahay D., Wiberg M., Pierer G., Terenghi G. Schwann cell strip for peripheral nerve repair. JHand Surg Eur Vol 2008, 33:587-594.
45. Daly W.T., Yao L., Abu-rub M.T., O'Connell C., Zeugolis D.I., Windebank A.J., et al. The effect of intraluminal contact mediated guidance signals on axonal mismatch during peripheral nerve repair. Biomaterials 2012, 33:6660-6671.
46. Clements I.P., Kim Y.T., English A.W., Lu X., Chung A., Bellamkonda R.V. Thin-film enhanced nerve guidance channels for peripheral nerve repair. Biomaterials 2009, 30:3834-3846.
47. Bellamkonda R., Ranieri J.P., Bouche N., Aebischer P. Hydrogel-based three-dimensional matrix for neural cells. JBiomed Mater Res 1995, 29:663-671.
48. Crompton K.E., Goud J.D., Bellamkonda R.V., Gengenbach T.R., Finkelstein D.I., Horne M.K., et al. Polylysine-functionalised thermoresponsive chitosan hydrogel for neural tissue engineering. Biomaterials 2007, 28:441-449.
49. McGrath A.M., Novikova L.N., Novikov L.N., Wiberg M. BD PuraMatrix peptide hydrogel seeded with Schwann cells for peripheral nerve regeneration. Brain Res Bull 2010, 83:207-213.
50. de Boer R., Knight A.M., Borntraeger A., Hebert-Blouin M.N., Spinner R.J., Malessy M.J., et al. Rat sciatic nerve repair with a poly-lactic-co-glycolic acid scaffold and nerve growth factor releasing microspheres. Microsurgery 2011, 31:293-302.
51. de Ruiter G.C., Onyeneho I.A., Liang E.T., Moore M.J., Knight A.M., Malessy M.J., et al. Methods for invitro characterization of multichannel nerve tubes. JBiomed Mater Res 2008, 84:643-651.
52. Midha R. Emerging techniques for nerve repair: nerve transfers and nerve guidance tubes. Clin Neurosurg 2006, 53:185-190.
53. Wang S., Kempen D.H., Simha N.K., Lewis J.L., Windebank A.J., Yaszemski M.J., et al. Photo-cross-linked hybrid polymer networks consisting of poly(propylene fumarate) and Poly(caprolactone fumarate): controlled physical properties and regulated bone and nerve cell responses. Biomacromolecules 2008, 1229-1241.
54. Wang S., Lu L., Gruetzmacher J.A., Currier B.L., Yaszemski M.J. Synthesis and characterizations of biodegradable and crosslinkable poly(epsilon-caprolactone fumarate), poly(ethylene glycol fumarate), and their amphiphilic copolymer. Biomaterials 2006, 27:832-841.
55. Wang S., Yaszemski M.J., Knight A.M., Gruetzmacher J.A., Windebank A.J., Lu L. Photo-crosslinked poly(e-caprolactone fumarate) networks for guided peripheral nerve regeneration: material properties and preliminary biological evaluations. Acta Biomater 2009, 5:1531-1542.
56. Dadsetan M., Knight A.M., Lu L., Windebank A.J., Yaszemski M.J. Stimulation of neurite outgrowth using positively charged hydrogels. Biomaterials 2009, 30:3874-3881.
57. Chen B.K., Knight A.M., Madigan N.N., Gross L., Dadsetan M., Nesbitt J.J., et al. Comparison of polymer scaffolds in rat spinal cord: a step toward quantitative assessment of combinatorial approaches to spinal cord repair. Biomaterials 2011, 32:8077-8086.
58. Dadsetan M., Szatkowski J.P., Yaszemski M.J., Lu L. Characterization of photo-cross-linked oligo[poly(ethylene glycol) fumarate] hydrogels for cartilage tissue engineering. Biomacromolecules 2007, 8:1702-1709.
59. O'Brien P.C., Shampo M.A. Statistical considerations for performing multiple tests in a single experiment. 5. Comparing two therapies with respect to several endpoints. Mayo Clin Proc 1988, 63:1140-1143.
60. de Boer R., Borntraeger A., Knight A.M., Hébert-Blouin M.-N., Spinner R.J., Malessy M.J.A., et al. Short- and long-term peripheral nerve regeneration using a poly-lactic-co-glycolic-acid scaffold containing nerve growth factor and glial cell line-derived neurotrophic factor releasing microspheres. JBiomed Mater Res A 2012, 100A:2139-2146.
61. Shin R.H., Vathana T., Giessler G.A., Friedrich P.F., Bishop A.T., Shin A.Y. Isometric tetanic force measurement method of the tibialis anterior in the rat. Microsurgery 2008, 28:452-457.
62. de Ruiter G.C.W., Malessy M.J.A., Yaszemski M.J., Windebank A.J., Spinner R.J. Designing ideal conduits for peripheral nerve repair. Neurosurg Focus 2009, 26:E5.
63. Nectow A.R., Marra K.G., Kaplan D.L. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B Rev 2012, 18:40-50.
64. Angius D., Wang H., Spinner R.J., Gutierrez-Cotto Y., Yaszemski M.J., Windebank A.J. Asystematic review of animal models used to study nerve regeneration in tissue-engineered scaffolds. Biomaterials 2012, 33:8034-8039.
65. Knight A.M., Dadsetan M., Wang S., Nesbitt J.J., Yaszemski M.J., Windebank A.J. Development and selection of biomaterials for artificial nerve tubes. JPeripher Nerv Syst 2007, 12:45.
66. Rooney G.E., Knight A.M., Madigan N.N., Gross L., Chen B., Giraldo C.V., et al. Sustained delivery of dibutyryl cyclic adenosine monophosphate to the transected spinal cord via oligo [(polyethylene glycol) fumarate] hydrogels. Tissue Eng 2011, 17:1287-1302.
67. Kim J., Dadsetan M., Ameenuddin S., Windebank A.J., Yaszemski M.J., Lu L. Invivo biodegradation and biocompatibility of PEG/sebacic acid-based hydrogels using a cage implant system. JBiomed Mater Res 2010, 95:191-197.