Evaluation of Polycaprolactone Scaffold with Basic Fibroblast Growth Factor and Fibroblasts in an Athymic Rat Model for Anterior Cruciate Ligament Reconstruction

Tissue Engineering - Part A

Volumn 21, Issue 11-12, 2015, Pages 1859-1868

  Leong, Natalie Luanne ^a   Kabir, Nima ^a   Arshi, Armin ^a   Nazemi, Azadeh ^b   Wu, Ben ^b   Petrigliano, Frank A ^a   McAllister, David R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Engineering IV   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; CELL CULTURE; FIBROBLASTS; HISTOLOGY; LIGAMENTS; RATS; STIFFNESS; SURGERY;

ANTERIOR CRUCIATE LIGAMENT; ANTERIOR-CRUCIATE-LIGAMENT RECONSTRUCTION; BASIC FIBROBLAST GROWTH FACTOR; INFLAMMATORY REACTION; INHERENT LIMITATIONS; LIGAMENT RECONSTRUCTION; MECHANICAL EVALUATION; POLYCAPROLACTONE SCAFFOLDS;

MECHANICAL TESTING;

COLLAGEN; FIBROBLAST GROWTH FACTOR 2; POLYCAPROLACTONE; POLYESTER;

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; ANTERIOR CRUCIATE LIGAMENT RUPTURE; ARTICLE; CELL INFILTRATION; COLORIMETRY; CONTROLLED STUDY; EVALUATION STUDY; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATION; MALE; MOLECULAR WEIGHT; NONHUMAN; NUDE RAT; POSTOPERATIVE PERIOD; PREPUCE; PRIORITY JOURNAL; RAT; RAT MODEL; RIGIDITY; RODENT MODEL; TISSUE ENGINEERING; WOUND HEALING; ANIMAL; ANTERIOR CRUCIATE LIGAMENT; BIODEGRADABLE IMPLANT; CYTOLOGY; DRUG EFFECTS; FOREIGN-BODY REACTION; MATERIALS TESTING; PATHOLOGY; PROCEDURES; STAINING; SURGERY; TISSUE SCAFFOLD; TRANSPLANTATION; WEIGHT BEARING; XENOGRAFT;

RATTUS; RODENTIA;

ABSORBABLE IMPLANTS; ANIMALS; ANTERIOR CRUCIATE LIGAMENT; ANTERIOR CRUCIATE LIGAMENT RECONSTRUCTION; COLLAGEN; FIBROBLAST GROWTH FACTOR 2; FIBROBLASTS; FOREIGN-BODY REACTION; FORESKIN; HETEROGRAFTS; HUMANS; MALE; MATERIALS TESTING; POLYESTERS; RATS; RATS, NUDE; STAINING AND LABELING; TISSUE SCAFFOLDS; WEIGHT-BEARING; WOUND HEALING;

EID: 84930175441     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0366     Document Type: Article

References (66)

1. Fetto, J.F., and Marshall, J.L. The natural history and diagnosis of anterior cruciate ligament insufficiency. Clin Orthop Relat Res 29, 147, 1980.
2. Kim, Y.M., Lee, C.A., and Matava, M.J. Clinical results of arthroscopic single-bundle transtibial posterior cruciate ligament reconstruction: a systematic review. Am J Sports Med 39, 425, 2011.
3. Andersson, C., Odensten, M., and Gillquist, J. Knee function after surgical or nonsurgical treatment of acute rupture of the anterior cruciate ligament: a randomized study with a long-term follow-up period. Clin Orthop Relat Res 264, 255, 1991.
4. Klimkiewicz, J.J., Petrie, R.S., and Harner, C.D. Surgical treatment of combined injury to anterior cruciate ligament, posterior cruciate ligament, and medial structures. Clin Sports Med 19, 479, 2000.
5. Petrigliano, F.A., McAllister, D.R., and Wu, B.M. Tissue engineering for anterior cruciate ligament reconstruction: a review of current strategies. Arthroscopy 22, 441, 2006.
6. de Groot, J.H., de Vrijer, R., Pennings, A.J., Klompmaker, J., Veth, R.P., and Jansen, H.W. Use of porous polyurethanes for meniscal reconstruction and meniscal prostheses. Biomaterials 17, 163, 1996.
7. Leong, N.L., Petrigliano, F.A., and McAllister, D.R. Current tissue engineering strategies in anterior cruciate ligament reconstruction. J Biomed Mater Res A 102, 1614, 2014.
8. Duling, R.R., Dupaix, R.B., Katsube, N., and Lannutti, J. Mechanical characterization of electrospun polycaprolactone (PCL): a potential scaffold for tissue engineering. J Biomech Eng 130, 011006, 2008.
9. Shao, Z., Zhang, X., Pi, Y., Wang, X., Jia, Z., Zhu, J., Dai, L., Chen, W., Yin, L., Chen, H., Zhou, C., and Ao, Y. Polycaprolactone electrospun mesh conjugated with an MSC affinity peptide for MSC homing in vivo. Biomaterials 33, 3375, 2012.
10. Tillman, B.W., Yazdani, S.K., Lee, S.J., Geary, R.L., Atala, A., and Yoo, J.J. The in vivo stability of electrospun polycaprolactone-collagen scaffolds in vascular reconstruction. Biomaterials 30, 583, 2009.
11. Wise, S.G., Byrom, M.J., Waterhouse, A., Bannon, P.G., Weiss, A.S., and Ng, M.K. A multilayered synthetic human elastin/polycaprolactone hybrid vascular graft with tailored mechanical properties. Acta Biomater 7, 295, 2011.
12. Bölgen, N., Vargel, I., Korkusuz, P., Menceloʇlu, Y.Z., and Pişkin, E. In vivo performance of antibiotic embedded electrospun PCL membranes for prevention of abdominal adhesions. J Biomed Mater Res B Appl Biomater 81, 530, 2007.
13. Cao, H., McHugh, K., Chew, S.Y., and Anderson, J.M. The topographical effect of electrospun nanofibrous scaffolds on the in vivo and in vitro foreign body reaction. J Biomed Mater Res A 93, 1151, 2010.
14. Joshi, V.S., Lei, N.Y., Walthers, C.M., Wu, B., and Dunn, J.C. Macroporosity enhances vascularization of electrospun scaffolds. J Surg Res 183, 18, 2013.
15. Pham, Q.P., Sharma, U., and Mikos, A.G. Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 7, 2796, 2006.
16. Vaz, C.M., van Tuijl, S., Bouten, C.V., and Baaijens, F.P. Design of scaffolds for blood vessel tissue engineering using a multi-layering electrospinning technique. Acta Biomater 1, 575, 2005.
17. Petrigliano, F., Arom, G., Nazemi, A., Yeranosian, M., Wu, B., and McAllister, D. In vivo evaluation of electrospun polycaprolactone graft for anterior cruciate ligament engineering. Tissue Eng Part A 2014 [Epub ahead of print].
18. Van Eijk, F., Saris, D.B., Riesle, J., Willems, W.J., Van Blitterswijk, C.A., Verbout, A.J., and Dhert, W.J. Tissue engineering of ligaments: a comparison of bone marrow stromal cells, anterior cruciate ligament, and skin fibroblasts as cell source. Tissue Eng 10, 893, 2004.
19. Scherping, S.C., Schmidt, C.C., Georgescu, H.I., Kwoh, C.K., Evans, C.H., and Woo, S.L. Effect of growth factors on the proliferation of ligament fibroblasts from skeletally mature rabbits. Connect Tissue Res 36, 1, 1997.
20. Haddad-Weber, M., Prager, P., Kunz, M., Seefried, L., Jakob, F., Murray, M.M., Evans, C.H., Nöth, U., and Steinert, A.F. BMP12 and BMP13 gene transfer induce ligamentogenic differentiation in mesenchymal progenitor and anterior cruciate ligament cells. Cytotherapy 12, 505, 2010.
21. Petrigliano, F.A., English, C.S., Barba, D., Esmende, S., Wu, B.M., and McAllister, D.R. The effects of local bFGF release and uniaxial strain on cellular adaptation and gene expression in a 3D environment: implications for ligament tissue engineering. Tissue Eng 13, 2721, 2007.
22. Mentink, A., Hulsman, M., Groen, N., Licht, R., Dechering, K.J., van der Stok, J., Alves, H.A., Dhert, W.J., van Someren, E.P., Reinders, M.J., van Blitterswijk, C.A., and de Boer, J. Predicting the therapeutic efficacy of MSC in bone tissue engineering using the molecular marker CADM1. Biomaterials 34, 4592, 2013.
23. Rouwkema, J., Gibbs, S., Lutolf, M.P., Martin, I., Vunjak-Novakovic, G., and Malda, J. In vitro platforms for tissue engineering: implications for basic research and clinical translation. J Tissue Eng Regen Med 5, e164, 2011.
24. Yeh, W.L., Lin, S.S., Yuan, L.J., Lee, K.F., Lee, M.Y., and Ueng, S.W. Effects of hyperbaric oxygen treatment on tendon graft and tendon-bone integration in bone tunnel: biochemical and histological analysis in rabbits. J Orthop Res 25, 636, 2007.
25. Ma, J., Smietana, M.J., Kostrominova, T.Y., Wojtys, E.M., Larkin, L.M., and Arruda, E.M. Three-dimensional engineered bone-ligament-bone constructs for anterior cruciate ligament replacement. Tissue Eng Part A 18, 103, 2012.
26. Watanabe, H., Saito, K., Kokubun, K., Sasaki, H., and Yoshinari, M. Change in surface properties of zirconia and initial attachment of osteoblastlike cells with hydrophilic treatment. Dent Mater J 31, 806, 2012.
27. Kawamura, S., Ying, L., Kim, H.J., Dynybil, C., and Rodeo, S.A. Macrophages accumulate in the early phase of tendon-bone healing. J Orthop Res 23, 1425, 2005.
28. Fan, H., Liu, H., Wong, E.J., Toh, S.L., and Goh, J.C. In vivo study of anterior cruciate ligament regeneration using mesenchymal stem cells and silk scaffold. Biomaterials 29, 3324, 2008.
29. Landis, J.R., and Koch, G.G. The measurement of observer agreement for categorical data. Biometrics 33, 159, 1977.
30. Bourke, S.L., Kohn, J., and Dunn, M.G. Preliminary development of a novel resorbable synthetic polymer fiber scaffold for anterior cruciate ligament reconstruction. Tissue Eng 10, 43, 2004.
31. Fisher, M.B., Liang, R., Jung, H.J., Kim, K.E., Zamarra, G., Almarza, A.J., McMahon, P.J., and Woo, S.L. Potential of healing a transected anterior cruciate ligament with genetically modified extracellular matrix bioscaffolds in a goat model. Knee Surg Sports Traumatol Arthrosc 20, 1357, 2012.
32. Brooks, C.G., Webb, P.J., Robins, R.A., Robinson, G., Baldwin, R.W., and Festing, M.F. Studies on the immunobiology of rnu/rnu "nude" rats with congenital aplasia of the thymus. Eur J Immunol 10, 58, 1980.
33. Joshi, S.M., Mastrangelo, A.N., Magarian, E.M., Fleming, B.C., and Murray, M.M. Collagen-platelet composite enhances biomechanical and histologic healing of the porcine anterior cruciate ligament. Am J Sports Med 37, 2401, 2009.
34. Scheffler, S.U., Schmidt, T., Gangéy, I., Dustmann, M., Unterhauser, F., and Weiler, A. Fresh-frozen free-tendon allografts versus autografts in anterior cruciate ligament reconstruction: delayed remodeling and inferior mechanical function during long-term healing in sheep. Arthroscopy 24, 448, 2008.
35. Ng, G.Y., Oakes, B.W., Deacon, O.W., McLean, I.D., and Lampard, D. Biomechanics of patellar tendon autograft for reconstruction of the anterior cruciate ligament in the goat: three-year study. J Orthop Res 13, 602, 1995.
36. Bellincampi, L.D., Closkey, R.F., Prasad, R., Zawadsky, J.P., and Dunn, M.G. Viability of fibroblast-seeded ligament analogs after autogenous implantation. J Orthop Res 16, 414, 1998.
37. Tischer, T., Aryee, S., Wexel, G., Steinhauser, E., Adamczyk, C., Eichhorn, S., Milz, S., Martinek, V., Gänsbacher, B., Imhoff, A.B., and Vogt, S. Tissue engineering of the anterior cruciate ligament-sodium dodecyl sulfate-acellularized and revitalized tendons are inferior to native tendons. Tissue Eng Part A 16, 1031, 2010.
38. Leong, N., Kabir, N., Arshi, A., Nazemi, A., Wu, B., McAllister, D., and Petrigliano, F. Athymic rat model for evaluation of engineered anterior cruciate ligament grafts. J Vis Exp 2015 (In Press).
39. Packer, J.D., Bedi, A., Fox, A.J., Gasinu, S., Imhauser, C.W., Stasiak, M., Deng, X.H., and Rodeo, S.A. Effect of immediate and delayed high-strain loading on tendon-to-bone healing after anterior cruciate ligament reconstruction. J Bone Joint Surg Am 96, 770, 2014.
40. Fu, S.C., Cheng, W.H., Cheuk, Y.C., Mok, T.Y., Rolf, C.G., Yung, S.H., and Chan, K.M. Effect of graft tensioning on mechanical restoration in a rat model of anterior cruciate ligament reconstruction using free tendon graft. Knee Surg Sports Traumatol Arthrosc 21, 1226, 2013.
41. Dayan, D., Hiss, Y., Hirshberg, A., Bubis, J.J., and Wolman, M. Are the polarization colors of picrosirius red-stained collagen determined only by the diameter of the fibers? Histochemistry 93, 27, 1989.
42. Lukinmaa, P.L., and Waltimo, J. Immunohistochemical localization of types I, V, and VI collagen in human permanent teeth and periodontal ligament. J Dent Res 71, 391, 1992.
43. Byers, P.H. Inherited disorders of collagen gene structure and expression. Am J Med Genet 34, 72, 1989.
44. Dash, T.K., and Konkimalla, V.B. Poly-ε-caprolactone based formulations for drug delivery and tissue engineering: a review. J Control Release 158, 15, 2012.
45. Yoshimoto, H., Shin, Y.M., Terai, H., and Vacanti, J.P. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 24, 2077, 2003.
46. Fukasawa, M., Bryant, S.M., Nakamura, R.M., and diZerega, G.S. Modulation of fibroblast proliferation by post-surgical macrophages. J Surg Res 43, 513, 1987.
47. Chung, A.S., Hwang, H.S., Das, D., Zuk, P., McAllister, D.R., and Wu, B.M. Lamellar stack formation and degradative behaviors of hydrolytically degraded poly(ε-caprolactone) and poly(glycolide-ε-caprolactone) blended fibers. J Biomed Mater Res B Appl Biomater 100, 274, 2012.
48. Davies, G., Grant, A.G., Duke, D., and Hermon-Taylor, J. Antibody response of nude (RNU/RNU) and hairy (RNU/+) rats to circulating cell surface components from human pancreatic cancer xenografts. Br J Cancer 48, 239, 1983.
49. Angello, J.C., Pendergrass, W.R., Norwood, T.H., and Prothero, J. Proliferative potential of human fibroblasts: an inverse dependence on cell size. J Cell Physiol 132, 125, 1987.
50. Heydarkhan-Hagvall, S., Choi, C.H., Dunn, J., Heydarkhan, S., Schenke-Layland, K., MacLellan, W.R., and Beygui, R.E. Influence of systematically varied nano-scale topography on cell morphology and adhesion. Cell Commun Adhes 14, 181, 2007.
51. Dabiri, G., Tumbarello, D.A., Turner, C.E., and Van de Water, L. Hic-5 promotes the hypertrophic scar myofibroblast phenotype by regulating the TGF-beta1 autocrine loop. J Invest Dermatol 128, 2518, 2008.
52. Ho, Y.C., Mi, F.L., Sung, H.W., and Kuo, P.L. Heparin-functionalized chitosan-alginate scaffolds for controlled release of growth factor. Int J Pharm 376, 69, 2009.
53. Neidert, M.R., Lee, E.S., Oegema, T.R., and Tranquillo, R.T. Enhanced fibrin remodeling in vitro with TGF-beta1, insulin and plasmin for improved tissue-equivalents. Biomaterials 23, 3717, 2002.
54. Knapp, D.M., Helou, E.F., and Tranquillo, R.T. A fibrin or collagen gel assay for tissue cell chemotaxis: assessment of fibroblast chemotaxis to GRGDSP. Exp Cell Res 247, 543, 1999.
55. Wada, N., Bartold, P.M., and Gronthos, S. Human foreskin fibroblasts exert immunomodulatory properties by a different mechanism to bone marrow stromal/stem cells. Stem Cells Dev 20, 647, 2011.
56. Schmitt, T., Fox, P.M., Woon, C.Y., Farnebo, S.J., Bronstein, J.A., Behn, A., Pham, H., and Chang, J. Human flexor tendon tissue engineering: in vivo effects of stem cell reseeding. Plast Reconstr Surg 132, 567e, 2013.
57. Goertzen, M.J., Buitkamp, J., Clahsen, H., and Möllmann, M. Cell survival following bone-anterior cruciate ligamentbone allograft transplantation: DNA fingerprints, segregation, and collagen morphological analysis of multiple markers in the canine model. Arch Orthop Trauma Surg 117, 208, 1998.
58. Mirensky, T.L., Hibino, N., Sawh-Martinez, R.F., Yi, T., Villalona, G., Shinoka, T., and Breuer, C.K. Tissue-engineered vascular grafts: does cell seeding matter? J Pediatr Surg 45, 1299, 2010.
59. Cartmell, J.S., and Dunn, M.G. Development of cell-seeded patellar tendon allografts for anterior cruciate ligament reconstruction. Tissue Eng 10, 1065, 2004.
60. Kimura, Y., Hokugo, A., Takamoto, T., Tabata, Y., and Kurosawa, H. Regeneration of anterior cruciate ligament by biodegradable scaffold combined with local controlled release of basic fibroblast growth factor and collagen wrapping. Tissue Eng Part C Methods 14, 47, 2008.
61. Sahoo, S., Ang, L.T., Cho-Hong Goh, J., and Toh, S.L. Bioactive nanofibers for fibroblastic differentiation of mesenchymal precursor cells for ligament/tendon tissue engineering applications. Differentiation 79, 102, 2010.
62. Xie, J., Bian, H., Qi, S., Xu, Y., Tang, J., Li, T., and Liu, X. Effects of basic fibroblast growth factor on the expression of extracellular matrix and matrix metalloproteinase-1 in wound healing. Clin Exp Dermatol 33, 176, 2008.
63. Liu, G., Hu, Y.Y., Zhao, J.N., Wu, S.J., Xiong, Z., and Lu, R. Effect of type I collagen on the adhesion, proliferation, and osteoblastic gene expression of bone marrow-derived mesenchymal stem cells. Chin J Traumatol 7, 358, 2004.
64. Leong, N.L., Arshi, A., Kabir, N., Nazemi, A., Petrigliano, F.A., Wu, B.M., and McAllister, D.R. In vitro and in vivo evaluation of heparin mediated growth factor release from tissue-engineered constructs for anterior cruciate ligament reconstruction. J Orthop Res 33, 229, 2015.
65. Ishiguro, S., Akasaka, Y., Kiguchi, H., Suzuki, T., Imaizumi, R., Ishikawa, Y., Ito, K., and Ishii, T. Basic fibroblast growth factor induces down-regulation of alpha-smooth muscle actin and reduction of myofibroblast areas in open skin wounds. Wound Repair Regen 17, 617, 2009.
66. Reed, S., and Wu, B. Sustained Growth Factor Delivery in Tissue Engineering Applications. Ann Biomed Eng 42, 1528, 2014.