Outer electrospun polycaprolactone shell induces massive foreign body reaction and impairs axonal regeneration through 3D multichannel chitosan nerve guides

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Duda, Sven ^a   Dreyer, Lutz ^b   Behrens, Peter ^b   Wienecke, Soenke ^b   Chakradeo, Tanmay ^b   Glasmacher, Birgit ^b   Haastert Talini, Kirsten ^a,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHITOSAN; POLYCAPROLACTONE; BIOMATERIAL; POLYESTER;

ADULT; ANIMAL EXPERIMENT; ARTICLE; AUTOMUTILATION; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROPHYSIOLOGICAL PROCEDURES; ELECTROSPINNING; EXTRACELLULAR SPACE; FEMALE; FOREIGN BODY REACTION; FREEZE DRYING; GIANT CELL; IN VIVO STUDY; MICROENVIRONMENT; NERVE FIBER REGENERATION; NERVE TRANSPLANTATION; NOCICEPTION; NONHUMAN; PERIPHERAL NERVE; RAT; SCANNING ELECTRON MICROSCOPY; SCIATIC NERVE; ANIMAL; CHEMICALLY INDUCED; CONVALESCENCE; DRUG EFFECTS; ELECTRODIAGNOSIS; INFLAMMATION; MOTOR ACTIVITY; MUSCLE; NERVE FIBER; NERVE REGENERATION; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; TISSUE REGENERATION; TISSUE SCAFFOLD; WISTAR RAT;

ANIMALS; AXONS; BIOCOMPATIBLE MATERIALS; CHITOSAN; ELECTRODIAGNOSIS; FEMALE; FOREIGN-BODY REACTION; GUIDED TISSUE REGENERATION; INFLAMMATION; MICROSCOPY, ELECTRON, SCANNING; MOTOR ACTIVITY; MUSCLES; NERVE REGENERATION; ORGAN SIZE; PAIN PERCEPTION; POLYESTERS; RATS, WISTAR; RECOVERY OF FUNCTION; TISSUE SCAFFOLDS;

EID: 84899995375     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/835269     Document Type: Article

References (53)

1. Noble J., Munro C. A., Prasad V. S., Midha R., Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. Journal of Trauma 1998 45 1 116 122 2-s2.0-0031810933 10.1097/00005373-199807000-00025
2. Eser F., Aktekin L., Bodur H., Atan Ç., Etiological factors of traumatic peripheral nerve injuries. Neurology India 2009 57 4 434 437 2-s2.0-70349423651 10.4103/0028-3886.55614
3. Evans G. R., Challenges to nerve regeneration. Seminars in Surgical Oncology 2000 19 312 318
4. Dornseifer U., Matiasek K., Fichter M. A., Rupp A., Henke J., Weidner N., Kovacs L., Schmahl W., Biemer E., Ninkovic M., Papadopulos N. A., Surgical therapy of peripheral nerve lesions: current status and new perspectives. Zentralblatt für Neurochirurgie 2007 68 3 101 110 2-s2.0-34548681875 10.1055/s-2007-984453
5. Daly W., Yao L., Zeugolis D., Windebank A., Pandit A., A biomaterials approach to peripheral nerve regeneration: bridging the peripheral nerve gap and enhancing functional recovery. Journal of the Royal Society Interface 2012 9 67 202 221 2-s2.0-84856571603 10.1098/rsif.2011.0438
6. Gu X., Ding F., Yang Y., Liu J., Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Progress in Neurobiology 2011 93 2 204 230 2-s2.0-78650590580 10.1016/j.pneurobio.2010.11. 002
7. Dahlin L. B., Techniques of peripheral nerve repair. Scandinavian Surgical Society 2008 97 310 316
8. Bozkurt A., Lassner F., O'Dey D., Deumens R., Böcker A., Schwendt T., Janzen C., Suschek C. V., Tolba R., Kobayashi E., Sellhaus B., Tholl S., Eummelen L., Schügner F., Olde Damink L., Weis J., Brook G. A., Pallua N., The role of microstructured and interconnected pore channels in a collagen-based nerve guide on axonal regeneration in peripheral nerves. Biomaterials 2012 33 5 1363 1375 2-s2.0-83355163219 10.1016/j.biomaterials.2011.10.069
9. Yuan Y., Zhang P., Yang Y., Wang X., Gu X., The interaction of Schwann cells with chitosan membranes and fibers in vitro. Biomaterials 2004 25 18 4273 4278 2-s2.0-1642377825 10.1016/j.biomaterials.2003.11.029
10. Hsu S. H., Kuo W. C., Chen Y. T., New nerve regeneration strategy combining laminin-coated chitosan conduits and stem cell therapy. Acta Biomaterialia 2013 9 5 6606 6615 10.1016/j.actbio.2013.01.025
11. Zhang Y.-G., Huang J.-H., Hu X.-Y., Sheng Q.-S., Zhao W., Luo Z.-J., Omentum-wrapped scaffold with longitudinally oriented micro-channels promotes axonal regeneration and motor functional recovery in rats. PLoS ONE 2011 6 12 2-s2.0-83455262548 10.1371/journal.pone.0029184 e29184
12. Haastert-Talini K., Geuna S., Dahlin L. B., Chitosan tubes of varying degrees of acetylation for bridging peripheral nerve defects. Biomaterials 2013 34 9886 9904
13. Jiang X., Lim S. H., Mao H.-Q., Chew S. Y., Current applications and future perspectives of artificial nerve conduits. Experimental Neurology 2010 223 1 86 101 2-s2.0-77950858630 10.1016/j.expneurol.2009.09.009
14. Schnell E., Klinkhammer K., Balzer S., Brook G., Klee D., Dalton P., Mey J., 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 19 3012 3025 2-s2.0-34147094231 10.1016/j.biomaterials. 2007.03.009
15. den Dunnen W. F., van der Lei B., Schakenraad J. M., Poly(DL-lactide- epsilon-caprolactone) nerve guides perform better than autologous nerve grafts. Microsurgery 1996 17 348 357
16. Meek M. F., den Dunnen W. F., Schakenraad J. M., Robinson P. H., Long-term evaluation of functional nerve recovery after reconstruction with a thin-walled biodegradable poly (DL-lactide-epsilon-caprolactone) nerve guide, using walking track analysis and electrostimulation tests. Microsurgery 1999 19 247 253
17. Kuberka M., Heschel I., Glasmacher B., Rau G., Preparation of collagen scaffolds and their applications in tissue engineering. Biomedizinische Technik 2002 47 supplement 1 485 487 2-s2.0-0036371197
18. Schoof H., Bruns L., Fischer A., Heschel I., Rau G., Dendritic ice morphology in unidirectionally solidified collagen suspensions. Journal of Crystal Growth 2000 209 1 122 129 2-s2.0-0033877110 10.1016/S0022-0248(99)00519- 9
19. Schoof H., Apel J., Heschel I., Rau G., Control of pore structure and size in freeze-dried collagen sponges. Journal of Biomedical Materials Research 2001 58 4 352 357 2-s2.0-0034958557 10.1002/jbm.1028
20. Kuberka M., Influence of seeding methods on cellular growth in 3D collagen scaffolds for Tissue Engineering. Biomedical Technologist 2004 49 634
21. Petersen A., Rau G., Glasmacher B., Reduction of primary freeze-drying time by electric field induced ice nucleus formation. Heat and Mass Transfer 2006 42 10 929 938 2-s2.0-33745698119 10.1007/s00231-006-0153-3
22. Ramakrishna S., An Introduction to Electrospinning and Nanofibers 2005 Singapore World Scientific
23. Szentivanyi A. L., Zernetsch H., Menzel H., Glasmacher B., A review of developments in electrospinning technology: new opportunities for the design of artificial tissue structures. International Journal of Artificial Organs 2011 34 10 986 997 2-s2.0-83455221760 10.5301/ijao.5000062
24. Rasband W. S., ImageJ,. U. S. National Institutes of Health, Bethesda, Md, USA. ImageJ, 1997
25. Schmitte R., Tipold A., Stein V. M., Schenk H., Flieshardt C., Grothe C., Haastert K., Genetically modified canine Schwann cells-In vitro and in vivo evaluation of their suitability for peripheral nerve tissue engineering. Journal of Neuroscience Methods 2010 186 2 202 208 2-s2.0-74149088704 10.1016/j.jneumeth.2009.11.023
26. Bozkurt A., Dunda S. E., O'Dey D. M., Brook G. A., Suschek C. V., Pallua N., Epineurial sheath tube (EST) technique: an experimental peripheral nerve repair model. Neurological Research 2011 33 10 1010 1015 2-s2.0-84555203808 10.1179/1743132811Y.0000000029
27. Dijkstra C. D., Döpp E. A., Joling P., Kraal G., The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 1985 54 3 589 599 2-s2.0-0021969667
28. Lee S., Zhang J., Heterogeneity of macrophages in injured trigeminal nerves: cytokine/chemokine expressing vs. phagocytic macrophages. Brain, Behavior, and Immunity 2012 26 891 903 2-s2.0-84859377382 10.1016/j.bbi.2012.03. 004
29. Siconolfi L. B., Seeds N. W., Mice lacking tPA, uPA, or plasminogen genes showed delayed functional recovery after sciatic nerve crush. Journal of Neuroscience 2001 21 12 4348 4355 2-s2.0-0035876289
30. Haastert-Talini K., Schaper-Rinkel J., Schmitte R., Bastian R., Mühlenhoff M., Schwarzer D., Draeger G., Su Y., Scheper T., Gerardy-Schahn R., Grothe C., In vivo evaluation of polysialic acid as part of tissue-engineered nerve transplants. Tissue Engineering A 2010 16 10 3085 3098 2-s2.0-77957662604 10.1089/ten.tea.2010.0180
31. Bervar M., Video analysis of standing-an alternative footprint analysis to assess functional loss following injury to the rat sciatic nerve. Journal of Neuroscience Methods 2000 102 2 109 116 2-s2.0-0034735725 10.1016/S0165-0270(00) 00281-8
32. Korte N., Schenk H. C., Grothe C., Tipold A., Haastert-Talini K., Evaluation of periodic electrodiagnostic measurements to monitor motor recovery after different peripheral nerve lesions in the rat. Muscle and Nerve 2011 44 1 63 73 2-s2.0-79959320074 10.1002/mus.22023
33. Bozkurt A., Tholl S., Wehner S., Tank J., Cortese M., O'Dey D. M., Deumens R., Lassner F., Schügner F., Gröger A., Smeets R., Brook G., Pallua N., Evaluation of functional nerve recovery with Visual-SSI-A novel computerized approach for the assessment of the static sciatic index (SSI). Journal of Neuroscience Methods 2008 170 1 117 122 2-s2.0-41049088823 10.1016/j.jneumeth.2008.01.006
34. Rupp A., Dornseifer U., Fischer A., Schmahl W., Rodenacker K., Jütting U., Gais P., Biemer E., Papadopulos N., Matiasek K., Electrophysiologic assessment of sciatic nerve regeneration in the rat: surrounding limb muscles feature strongly in recordings from the gastrocnemius muscle. Journal of Neuroscience Methods 2007 166 2 266 277 2-s2.0-35549010772 10.1016/j.jneumeth.2007.07.015
35. Kuntzer T., van Melle G., Regli F., Clinical and prognostic features in unilateral femoral neuropathies. Muscle & Nerve 1997 20 205 211
36. Cuddon P. A., Electrophysiology in neuromuscular disease. Veterinary Clinics of North America-Small Animal Practice 2002 32 1 31 62 2-s2.0-0036143778 10.1016/S0195-5616(03)00079-2
37. Haastert K., Joswig H., Jäschke K.-A., Samii M., Grothe C., Nerve repair by end-to-side nerve coaptation: histologic and morphometric evaluation of axonal origin in a rat sciatic nerve model. Neurosurgery 2010 66 3 567 577 2-s2.0-77649163827 10.1227/01.NEU.0000365768.78251.8C
38. Geuna S., Gigo-Benato D., de Castro Rodrigues A., On sampling and sampling errors in histomorphometry of peripheral nerve fibers. Microsurgery 2004 24 1 72 76 2-s2.0-0842332419 10.1002/micr.10199
39. Geuna S., Tos P., Battiston B., Guglielmone R., Verification of the two-dimensional disector, a method for the unbiased estimation of density and number of myelinated nerve fibers in peripheral nerves. Annals of Anatomy 2000 182 1 23 34 2-s2.0-0033968592
40. Vleggeert-Lankamp C. L. A. M., The role of evaluation methods in the assessment of peripheral nerve regeneration through synthetic conduits: a systematic review. Laboratory investigation. Journal of Neurosurgery 2007 107 6 1168 1189 2-s2.0-37149003442 10.3171/JNS-07/12/1168
41. de Medinaceli L., Freed W. J., Wyatt R. J., An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Experimental Neurology 1982 77 3 634 643 2-s2.0-0019938340
42. Chamberlain L. J., Yannas I. V., Hsu H.-P., Strichartz G., Spector M., Collagen-GAG substrate enhances the quality of nerve regeneration through collagen tubes up to level of autograft. Experimental Neurology 1998 154 2 315 329 2-s2.0-0032435262 10.1006/exnr.1998.6955
43. Anderson J. M., Rodriguez A., Chang D. T., Foreign body reaction to biomaterials. Seminars in Immunology 2008 20 2 86 100 2-s2.0-40849094515 10.1016/j.smim.2007.11.004
44. Meek M. F., den Dunnen W. F. A., Porosity of the wall of a Neurolac nerve conduit hampers nerve regeneration. Microsurgery 2009 29 6 473 478 2-s2.0-70349295210 10.1002/micr.20642
45. den Dunnen W. F., Robinson P. H., van Wessel R., Pennings A. J., van Leeuwen M. B., Schakenraad J. M., Long-term evaluation of degradation and foreign-body reaction of subcutaneously implanted poly(DL-lactide-epsilon- caprolactone). Journal of Biomedical Materials Research 1997 36 337 346
46. Hernández-Cortés P., Juan G., Cámara M., Ravassa F. O., Failed digital nerve reconstruction by foreign body reaction to Neurolac: nerve conduit. Microsurgery 2010 30 5 414 416 2-s2.0-77956837565 10.1002/micr.20730
47. Dash T. K., Konkimalla V. B., Poly- ε -caprolactone based formulations for drug delivery and tissue engineering: a review. Journal of Controlled Release 2012 158 15 33 10.1016/j.jconrel.2011.09.064
48. Vleggeert-Lankamp C. L. A. M., de Ruiter G. C. W., Wolfs J. F. C., Pêgo A. P., van den Berg R. J., Feirabend H. K. P., Malessy M. J. A., Lakke E. A. J. F., Pores in synthetic nerve conduits are beneficial to regeneration. Journal of Biomedical Materials Research A 2007 80 4 965 982 2-s2.0-33847178702 10.1002/jbm.a.30941
49. Podhajsky R. J., Myers R. R., The vascular response to nerve transection: neovascularization in the silicone nerve regeneration chamber. Brain Research 1994 662 1-2 88 94 2-s2.0-0027986878 10.1016/0006-8993(94)90799-4
50. Devor M., Schonfeld D., Seltzer Z., Wall P. D., Two modes of cutaneous reinnervation following peripheral nerve injury. Journal of Comparative Neurology 1979 185 1 211 220 2-s2.0-0018755341
51. Chamberlain L. J., Yannas I. V., Hsu H. P., Strichartz G. R., Spector M., Near-terminus axonal structure and function following rat sciatic nerve regeneration through a collagen-GAG matrix in a ten-millimeter gap. Journal of Neuroscience Research 2000 60 666 677
52. Arbuthnott E. R., Boyd I. A., Kalu K. U., Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. Journal of Physiology 1980 308 125 157 2-s2.0-0019229260
53. Aitken J. T., The effect of peripheral connexions on the maturation of regenerating. Journal of Anatomy 1949 83 1 32 43 2-s2.0-0003144383