Marine collagen scaffolds for nasal cartilage repair: Prevention of nasal septal perforations in a new orthotopic rat model using tissue engineering techniques

Tissue Engineering - Part A

Volumn 19, Issue 19-20, 2013, Pages 2201-2214

  Bermueller, Christian ^a   Schwarz, Silke ^a   Elsaesser, Alexander F ^a   Sewing, Judith ^b,c   Baur, Nina ^a   Von Bomhard, Achim ^a   Scheithauer, Marc ^a   Notbohm, Holger ^b   Rotter, Nicole ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c CRM Coastal Research and Management   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCOMPATIBILITY; BODY FLUIDS; CARTILAGE; COLLAGEN; CYTOTOXICITY; DEFECTS; RATS; REPAIR;

CARTILAGE DEFECTS; CARTILAGE REPLACEMENTS; CARTILAGE TISSUE ENGINEERING; EXTRACELLULAR MATRIX FORMATION; SCAFFOLD MATERIALS; SURGICAL PROCEDURES; THREE-DIMENSIONAL CULTURE; TISSUE-ENGINEERING TECHNIQUES;

SCAFFOLDS (BIOLOGY);

COLLAGEN TYPE 2; MARINE COLLAGEN SCAFFOLD; TISSUE SCAFFOLD; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; CYTOTOXICITY; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; JELLYFISH; NONHUMAN; NOSE CARTILAGE; NOSE SEPTUM PERFORATION; NOSE SURGERY; PRIORITY JOURNAL; RAT; RHOPILEMA ESCULENTUM; TISSUE ENGINEERING;

ANIMALIA; RATTUS;

ANIMALS; CELLS, CULTURED; CHONDROCYTES; COLLAGEN; FEMALE; MALE; NASAL CARTILAGES; NASAL SEPTAL PERFORATION; RATS; TISSUE ENGINEERING;

EID: 84883677010     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0650     Document Type: Article

References (70)

1. Rotter, N., Haisch, A., and Bucheler, M. Cartilage and bone tissue engineering for reconstructive head and neck surgery. Eur Arch Otorhinolaryngol 262, 539, 2005.
2. Mandl, E.W., Jahr, H., Koevoet, J.L., van Leeuwen, J.P., Weinans, H., Verhaar, J.A., and Van Osch, G.J. Fibroblast growth factor-2 in serum-free medium is a potent mitogen and reduces dedifferentiation of human ear chondrocytes in monolayer culture. Matrix Biol 23, 231, 2004.
3. Rotter, N., Bucheler, M., Haisch, A., Wollenberg, B., and Lang, S. Cartilage tissue engineering using resorbable scaffolds. J Tissue Eng Regen Med 1, 411, 2007.
4. Nagata, S. Modification of the stages in total reconstruction of the auricle: Part I. Grafting the three-dimensional costal cartilage framework for lobule-type microtia. Plast Reconstr Surg 93, 221, 1994.
5. Ohara, K., Nakamura, K., and Ohta, E. Chest wall deformities and thoracic scoliosis after costal cartilage graft harvesting. Plast Reconstr Surg 99, 1030, 1997.
6. Ryan, M.W., and Quinn, F.B., Jr. Advancing otolaryngology education in the new millennium. Otolaryngol Clin North Am 40, 1191, 2007.
7. Wang, J.H., Lee, B.J., and Jang, Y.J. Use of silicone sheets for dorsal augmentation in rhinoplasty for Asian noses. Acta Otolaryngol Suppl 558, 115, 2007.
8. Sevin, K., Askar, I., Saray, A., and Yormuk, E. Exposure of high-density porous polyethylene (Medpor) used for contour restoration and treatment. Br J Oral Maxillofac Surg 38, 44, 2000.
9. Stone, K.R., Rodkey, W.G., Webber, R.J., McKinney, L., and Steadman, J.R. Future directions. Collagen-based prostheses for meniscal regeneration. Clin Orthop Relat Res 252, 129, 1990.
10. Glowacki, J., and Mizuno, S. Collagen scaffolds for tissue engineering. Biopolymers 89, 338, 2008.
11. O'Brien, F.J., Harley, B., Yannas, I.V., and Gibson, L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 26, 433, 2005.
12. Wakitani, S., Kimura, T., Hirooka, A., Ochi, T., Yoneda, M., Yasui, N., Owaki, H., and Ono, K. Repair of rabbit articular surfaces with allograft chondrocytes embedded in collagen gel. J Bone Joint Surg Br 71, 74, 1989.
13. Langer, R., and Vacanti, J.P. Tissue engineering. Science 260, 920, 1993.
14. Vacanti, C.A., Langer, R., Schloo, B., and Vacanti, J.P. Synthetic polymers seeded with chondrocytes provide a template for new cartilage formation. Plast Reconstr Surg 88, 753, 1991.
15. Freed, L., Marquis, J., Nohria, A., Emmanual, J., Mikos, A., and Langer, R. Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J Biomed Mater Res A 27, 11, 1993.
16. Chia, S.H., Schumacher, B.L., Klein, T.J., Thonar, E.J., Masuda, K., Sah, R.L., and Watson, D. Tissue-engineered human nasal septal cartilage using the alginate-recoveredchondrocyte method. Laryngoscope 114, 38, 2004.
17. Liese, J., Marzahn, U., El Sayed, K., Pruss, A., Haisch, A., and Stoelzel, K. Cartilage tissue engineering of nasal septal chondrocyte- macroaggregates in human demineralized bone matrix. Cell Tissue Bank 1, 2012.
18. Kusuhara, H., Isogai, N., Enjo, M., Otani, H., Ikada, Y., Jacquet, R., Lowder, E., and Landis, W.J. Tissue engineering a model for the human ear: assessment of size, shape, morphology, and gene expression following seeding of different chondrocytes. Wound Repair Regen 17, 136, 2009.
19. Cao, Y., Vacanti, J.P., Paige, K.T., Upton, J., and Vacanti, C.A. Transplantation of chondrocytes utilizing a polymercell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast Reconstr Surg 100, 297, 1997.
20. Mafi, P., Hindocha, S., Mafi, R., and S Khan, W. Evaluation of biological protein-based collagen scaffolds in cartilage and musculoskeletal tissue engineering-A systematic review of the literature. Curr Stem Cell Res Ther 7, 302, 2012.
21. Tuli, R., Li, W.J., and Tuan, R.S. Current state of cartilage tissue engineering. Arthritis Res Ther 5, 235, 2003.
22. Song, E., Yeon Kim, S., Chun, T., Byun, H.J., and Lee, Y.M. Collagen scaffolds derived from a marine source and their biocompatibility. Biomaterials 27, 2951, 2006.
23. Lee, C.H., Singla, A., and Lee, Y. Biomedical applications of collagen. Int J Pharm 221, 1, 2001.
24. Friess, W. Collagen-biomaterial for drug delivery. Eur J Pharm Biopharm 45, 113, 1998.
25. Riesle, J., Hollander, A., Langer, R., Freed, L., and Vunjak-Novakovic, G. Collagen in tissue-engineered cartilage: Types, structure, and crosslinks. J Cell Biochem 71, 313, 1998.
26. Sano, A., Maeda, M., Nagahara, S., Ochiya, T., Honma, K., Itoh, H., Miyata, T., and Fujioka, K. Atelocollagen for protein and gene delivery. Adv Drug Deliv Rev 55, 1651, 2003.
27. Ma, L., Gao, C., Mao, Z., Zhou, J., and Shen, J. Enhanced biological stability of collagen porous scaffolds by using amino acids as novel cross-linking bridges. Biomaterials 25, 2997, 2004.
28. Murray, M.M., Rice, K., Wright, R., and Spector, M. The effect of selected growth factors on human anterior cruciate ligament cell interactions with a three-dimensional collagen-GAG scaffold. J Orthop Res 21, 238, 2003.
29. Angele, P., Abke, J., Kujat, R., Faltermeier, H., Schumann, D., Nerlich, M., Kinner, B., Englert, C., Ruszczak, Z., and Mehrl, R. Influence of different collagen species on physicochemical properties of crosslinked collagen matrices. Biomaterials 25, 2831, 2004.
30. Addad, S., Exposito, J.Y., Faye, C., Ricard-Blum, S., and Lethias, C. Isolation, characterization and biological evaluation of jellyfish collagen for use in biomedical applications. Mar Drugs 9, 967, 2011.
31. Exposito, J.Y., Valcourt, U., Cluzel, C., and Lethias, C. The fibrillar collagen family. Int J Mol Sci 11, 407, 2010.
32. In Jeong, S., Kim, S.Y., Cho, S.K., Chong, M.S., Kim, K.S., Kim, H., Lee, S.B., and Lee, Y.M. Tissue-engineered vascular grafts composed of marine collagen and PLGA fibers using pulsatile perfusion bioreactors. Biomaterials 28, 1115, 2007.
33. Hayashi, Y., Yamada, S., Yanagi Guchi, K., Koyama, Z., and Ikeda, T. Chitosan and fish collagen as biomaterials for regenerative medicine. Adv Food Nutr Res 65, 107, 2012.
34. Lin, Z., Solomon, K.L., Zhang, X., Pavlos, N.J., Abel, T., Willers, C., Dai, K., Xu, J., Zheng, Q., and Zheng, M. In vitro evaluation of natural marine sponge collagen as a scaffold for bone tissue engineering. Int J Biol Sci 7, 968, 2011.
35. Duda, G.N., Haisch, A., Endres, M., Gebert, C., Schroeder, D., Hoffmann, J.E., and Sittinger, M. Mechanical quality of tissue engineered cartilage: results after 6 and 12 weeks in vivo. J Biomed Mater Res 53, 673, 2000.
36. Homicz, M.R., Schumacher, B.L., Sah, R.L., and Watson, D. Effects of serial expansion of septal chondrocytes on tissueengineered neocartilage composition. Otolaryngol Head Neck Surg 127, 398, 2002.
37. Brittberg, M., Lindahl, A., Nilsson, A., Ohlsson, C., Isaksson, O., and Peterson, L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331, 889, 1994.
38. Kafienah, W., Jakob, M., Demarteau, O., Frazer, A., Barker, M.D., Martin, I., and Hollander, A.P. Three-dimensional tissue engineering of hyaline cartilage: comparison of adult nasal and articular chondrocytes. Tissue Eng 8, 817, 2002.
39. Malda, J.,Kreijveld,E.,Temenoff, J.S., Blitterswijk,C.A.,andRiesle, J. Expansion of human nasal chondrocytes on macroporous microcarriers enhances redifferentiation. Biomaterials 24, 5153, 2003.
40. Naumann, A., Rotter, N., Bujia, J., and Aigner, J. Tissue engineering of autologous cartilage transplants for rhinology. Am J Rhinol 12, 59, 1998.
41. Stok, K.S., Lisignoli, G., Cristino, S., Facchini, A., and Müller, R. Mechano-functional assessment of human mesenchymal stem cells grown in three-dimensional hyaluronan-based scaffolds for cartilage tissue engineering. J Biomed Mater Res A 93, 37, 2010.
42. Schwarz, S., Koerber, L., Elsaesser, A.F., Goldberg-Bockhorn, E., Seitz, A.M., Durselen, L., Ignatius, A., Walther, P., Breiter, R., and Rotter, N. Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Eng Part A 18, 2195, 2012.
43. Kim, Y.J., Sah, R.L., Doong, J.Y., and Grodzinsky, A.J. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174, 168, 1988.
44. Schwarz, S., Elsaesser, A.F., Koerber, L., Goldberg-Bockhorn, E., Seitz, A.M., Bermueller, C., Durselen, L., Ignatius, A., Breiter, R., and Rotter, N. Processed xenogenic cartilage as innovative biomatrix for cartilage tissue engineering: effects on chondrocyte differentiation and function. J Tissue Eng Regen Med, 2012.
45. Barbosa, I., Garcia, S., Barbier-Chassefiere, V., Caruelle, J.P., Martelly, I., and Papy-Garcia, D. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 13, 647, 2003.
46. Livak, K.J., and Schmittgen, T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-DDCT Method. Methods 25, 402, 2001.
47. Lin, Z., Fitzgerald, J.B., Xu, J., Willers, C., Wood, D., Grodzinsky, A.J., and Zheng, M.H. Gene expression profiles of human chondrocytes during passaged monolayer cultivation. J Orthop Res 26, 1230, 2008.
48. Ciorba, A., and Martini, A. Tissue engineering and cartilage regeneration for auricular reconstruction. Int J Pediatr Otorhinolaryngol 70, 1507, 2006.
49. Vacanti, C.A., Cima, L.G., Ratkowski, D., Upton, J., and Vacanti, J.P. Tissue engineered growth of new cartilage in the shape of a human ear using synthetic polymers seeded with chondrocytes. MRS Proc 252, 1991.
50. Han, B., Jaurequi, J., Tang, B.W., and Nimni, M.E. Proanthocyanidin: a natural crosslinking reagent for stabilizing collagen matrices. J Biomed Mater Res A 65, 118, 2003.
51. Hey, K., Lachs, C., Raxworthy, M., and Wood, E. Crosslinked fibrous collagen for use as a dermal implant: control of the cytotoxic effects of glutaraldehyde and dimethylsuberimidate. Biotechnol Appl Biochem 12, 85, 1990.
52. Kotzar, G., Freas, M., Abel, P., Fleischman, A., Roy, S., Zorman, C., Moran, J.M., and Melzak, J. Evaluation of MEMS materials of construction for implantable medical devices. Biomaterials 23, 2737, 2002.
53. Nuernberger, S., Cyran, N., Albrecht, C., Redl, H., Vécsei, V., and Marlovits, S. The influence of scaffold architecture on chondrocyte distribution and behavior in matrix-associated chondrocyte transplantation grafts. Biomaterials 32, 1032, 2011.
54. Roosa, S.M.M., Kemppainen, J.M., Moffitt, E.N., Krebsbach, P.H., and Hollister, S.J. The pore size of polycaprolactone scaffolds has limited influence on bone regeneration in an in vivo model. J Biomed Mater Res A 92, 359, 2009.
55. Zeltinger, J., Sherwood, J.K., Graham, D.A., Mü eller, R., and Griffith, L.G. Effect of pore size and void fraction on cellular adhesion, proliferation, and matrix deposition. Tissue Eng 7, 557, 2001.
56. Aigner, T., and Stove, J. Collagens-major component of the physiological cartilage matrix, major target of cartilage degeneration, major tool in cartilage repair. Adv Drug Deliv Rev 55, 1569, 2003.
57. Nehrer, S., Breinan, H.A., Ramappa, A., Young, G., Shortkroff, S., Louie, L.K., Sledge, C.B., Yannas, I.V., and Spector, M. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials 18, 769, 1997.
58. Stenhamre, H., Nannmark, U., Lindahl, A., Gatenholm, P., and Brittberg, M. Influence of pore size on the redifferentiation potential of human articular chondrocytes in poly (urethane urea) scaffolds. J Tissue Eng Regen Med 5, 578, 2011.
59. Oh, S.H., Park, I.K., Kim, J.M., and Lee, J.H. In vitro and in vivo characteristics of PCL scaffolds with pore size gradient fabricated by a centrifugation method. Biomaterials 28, 1664, 2007.
60. Jeong, C.G., and Hollister, S.J. Mechanical and biochemical assessments of three-dimensional poly (1, 8-octanediol-cocitrate) scaffold pore shape and permeability effects on in vitro chondrogenesis using primary chondrocytes. Tissue Eng Part A 16, 3759, 2010.
61. Nehrer, S., Breinan, H.A., Ramappa, A., Shortkroff, S., Young, G., Minas, T., Sledge, C.B., Yannas, I.V., and Spector, M. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro. J Biomed Mater Res 38, 95, 1997.
62. Pieper, J.S., van der Kraan, P.M., Hafmans, T., Kamp, J., Buma, P., van Susante, J.L., van den Berg, W.B., Veerkamp, J.H., and van Kuppevelt, T.H. Crosslinked type II collagen matrices: preparation, characterization, and potential for cartilage engineering. Biomaterials 23, 3183, 2002.
63. Kunisawa, J., Fukuyama, S., and Kiyono, H. Mucosa-associated lymphoid tissues in the aerodigestive tract: their shared and divergent traits and their importance to the orchestration of the mucosal immune system. Curr Mol Med 5, 557, 2005.
64. Yun, K., and Moon, H.T. Inducing chondrogenic differentiation in injectable hydrogels embedded with rabbit chondrocytes and growth factor for neocartilage formation. J Biosci Bioeng 105, 122, 2008.
65. Lattyak, B.V., Maas, C.S., and Sykes, J.M. Dorsal onlay cartilage autografts. Arch Facial Plast Surg 5, 240, 2003.
66. Anderson, J.M., and Langone, J.J. Issues and perspectives on the biocompatibility and immunotoxicity evaluation of implanted controlled release systems. J Controlled Release 57, 107, 1999.
67. Anderson, J.M., and Shive, M.S. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev 28, 5, 1997.
68. Garosi, G., and Di Paolo, N. The rabbit model in evaluating the biocompatibility in peritoneal dialysis. Nephrol Dial Transplant 16, 664, 2001.
69. International Organization of Standardization. Biological Evaluation of Medical Devices-Part 5: Tests for In Vitro Cytotoxicity; (ISO 10993-5:2009); German version EN ISO 10993-5:2009, 2009.
70. Kaiser, M.L., Karam, A.M., Sepehr, A., Wong, H., Liaw, L.L., Vokes, D.E., and Wong, B.J. Cartilage regeneration in the rabbit nasal septum. Laryngoscope 116, 1730, 2006.