Effect of silk fibroin/poly (<i>L</i>-lactic acid-co-e-caprolactone) nanofibrous scaffold on tendon-bone healing of rabbits _Chinese Journal of Reparative and Reconstructive Surgery

Authors：

CAI Jiangyu ¹ , JIANG Jia ¹ , MO Xiumei ² ,  CHEN Shiyi ¹

1. Department of Sports Medicine and Arthroscopic Surgery, Huashan Hospital, Fudan University, Shanghai, 200040, P.R.China;
2. Biomaterials and Tissue Engineering Laboratory, College of Chemistry, Chemical Engineering and Biotechnology, Donghua University, Shanghai, 201620, P.R.China;

Corresponding author：

CHEN Shiyi, Email: cshiyi@163.com

Keywords：

Anterior cruciate ligament; silk fibroin; poly(L-lactic acid-co-e-caprolactone); nanofibrous scaffold; tendon-bone healing; rabbit

DOI：

10.7507/1002-1892.201704077

Video：

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ObjectiveTo explore the effect of silk fibroin/poly(L-lactic acid-co-e-caprolactone) [SF/P(LLA-CL)] nanofibrous scaffold on tendon-bone healing of rabbits.MethodsSF/P(LLA-CL) nanofibrous scaffold was fabricated by electrospinning methods. The morphology of the scaffold was observed by scanning electron microscope (SEM). Pre-osteoblasts MC3T3-E1 cells were seeded on the scaffold and cultured for 1, 3, and 5 days. Cell adhesion and proliferation were also observed by SEM. Meanwhile, twenty-four New Zealand white rabbits were randomly divided into the autogenous tendon group (control group) and the autogenous tendon wrapped with SF/P(LLA-CL) scaffold group (experimental group), with twelve rabbits in each group. An extra-articular model was established, the effect was evaluated by histological examination and mechanical testing.ResultsThe morphology of SF/P(LLA-CL) nanofibrous scaffold was random, with a diameter of (219.4±66.5) nm. SEM showed that the MC3T3-E1 cells seeded on the scaffold were in the normal shape, growing well, and proliferating with time course. The results of histological examination showed that inflammatory cells infltrated into the graft-host bone interface at 6 weeks after operation in both groups. Besides, the width of interface showed no significant difference between groups. At 12 weeks after operation, protruding new bone tissue could be observed at the interface in the experimental group, while scar tissue but no new bone tissue could be seen at the interface in the control group. Mechanical testing showed that there was no significant difference in the failure load and the stiffness between groups at 6 weeks after operation (P>0.05). The failure load and the stiffness in the experimental group were significantly higher than those in the control group at 12 weeks after operation (P<0.05).ConclusionThe SF/P(LLA-CL) nanofibrous scaffold has good cell biocompatibility and can effectively promote tendon-bone healing, thus providing new method for modifying graft for ACL reconstruction in the clinical practice.

Citation： CAI Jiangyu, JIANG Jia, MO Xiumei, CHEN Shiyi. Effect of silk fibroin/poly (L-lactic acid-co-e-caprolactone) nanofibrous scaffold on tendon-bone healing of rabbits . Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(8): 957-962. doi: 10.7507/1002-1892.201704077 Copy

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2.	Lohmander LS, Englund PM, Dahl LL, et al. The long-term consequence of anterior cruciate ligament and meniscus injuries: osteoarthritis. Am J Sports Med, 2007, 35(10): 1756-1769.
3.	张承昊, 李棋, 唐新, 等. 促进腱-骨愈合方法的研究进展. 中国修复重建外科杂志, 2015, 29(7): 912-916.
4.	Sridhar R, Lakshminarayanan R, Madhaiyan K, et al. Electrosprayed nanoparticles and electrospun nanofibers based on natural materials: applications in tissue regeneration, drug delivery and pharmaceuticals. Chem Soc Rev, 2015, 44(3): 790-814.
5.	Claes S, Verdonk P, Forsyth R, et al. The " ligamentization” process in anterior cruciate ligament reconstruction: what happens to the human graft? A systematic review of the literature. Am J Sports Med, 2011, 39(11): 2476-2483.
6.	Atesok K, Fu FH, Wolf MR, et al. Augmentation of tendon-to-bone healing. J Bone Joint Surg (Am), 2014, 96(6): 513-521.
7.	Zhang K, Wang H, Huang C, et al. Fabrication of silk fibroin blended P(LLA-CL) nanofibrous scaffolds for tissue engineering. J Biomed Mater Res A, 2010, 93(3): 984-993.
8.	Wang CY, Zhang KH, Fan CY, et al. Aligned natural-synthetic polyblend nanofibers for peripheral nerve regeneration. Acta Biomater, 2011, 7(2): 634-643.
9.	Chen J, Yan C, Zhu M, et al. Electrospun nanofibrous SF/P(LLA-CL) membrane: a potential substratum for endothelial keratoplasty. Int J Nanomedicine, 2015, 10: 3337-3350.
10.	Wang Z, Lin M, Xie Q, et al. Electrospun silk fibroin/poly(lactide-co-epsilon-caprolactone) nanofibrous scaffolds for bone regeneration. Int J Nanomedicine, 2016, 11: 1483-1500.
11.	高林峰, 王洪复. 骨基质 Ⅰ 型胶原的增龄性改变. 中华老年医学杂志, 2001, 20(6): 465-467.
12.	Takeuchi A, Ohtsuki C, Miyazaki T, et al. Deposition of bone-like apatite on silk fiber in a solution that mimics extracellular fluid. J Biomed Mater Res A, 2003, 65(2): 283-289.
13.	Shanmugavel S, Reddy VJ, Ramakrishna S, et al. Precipitation of hydroxyapatite on electrospun polycaprolactone/aloe vera/silk fibroin nanofibrous scaffolds for bone tissue engineering. J Biomater Appl, 2014, 29(1): 46-58.
14.	Vetsch JR, Paulsen SJ, Müller R, et al. Effect of fetal bovine serum on mineralization in silk fibroin scaffolds. Acta Biomater, 2015, 13: 277-285.
15.	Midha S, Murab S, Ghosh S. Osteogenic signaling on silk-based matrices. Biomaterials, 2016, 97: 133-153.
16.	Jung SR, Song NJ, Yang DK, et al. Silk proteins stimulate osteoblast differentiation by suppressing the Notch signaling pathway in mesenchymal stem cells. Nutr Res, 2013, 33(2): 162-170.
17.	Wang H, Pieper J, Peters F, et al. Synthetic scaffold morphology controls human dermal connective tissue formation. J Biomed Mater Res A, 2005, 74(4): 523-532.
18.	Li Y, Jiang X, Zhong H, et al. Hierarchical Patterning of Cells with a Microeraser and Electrospun Nanofibers. Small, 2016, 12(9): 1230-1239.
19.	Sperling LE, Reis KP, Pozzobon LG, et al. Influence of random and oriented electrospun fibrous poly(lactic-co-glycolic acid) scaffolds on neural differentiation of mouse embryonic stem cells. J Biomed Mater Res A, 2017, 105(5): 1333-1345.
20.	Yin Z, Chen X, Chen JL, et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials, 2010, 31(8): 2163-2175.
21.	Yin Z, Chen X, Song HX, et al. Electrospun scaffolds for multiple tissues regeneration in vivo through topography dependent induction of lineage specific differentiation. Biomaterials, 2015, 44: 173-185.
22.	Zhang C, Yuan H, Liu H, et al. Well-aligned chitosan-based ultrafine fibers committed teno-lineage differentiation of human induced pluripotent stem cells for Achilles tendon regeneration. Biomaterials, 2015, 53: 716-730.

1. Spindler KP, Warren TA, Callison JC Jr, et al. Clinical outcome at a minimum of five years after reconstruction of the anterior cruciate ligament. J Bone Joint Surg (Am), 2005, 87(8): 1673-1679.
2. Lohmander LS, Englund PM, Dahl LL, et al. The long-term consequence of anterior cruciate ligament and meniscus injuries: osteoarthritis. Am J Sports Med, 2007, 35(10): 1756-1769.
3. 张承昊, 李棋, 唐新, 等. 促进腱-骨愈合方法的研究进展. 中国修复重建外科杂志, 2015, 29(7): 912-916.
4. Sridhar R, Lakshminarayanan R, Madhaiyan K, et al. Electrosprayed nanoparticles and electrospun nanofibers based on natural materials: applications in tissue regeneration, drug delivery and pharmaceuticals. Chem Soc Rev, 2015, 44(3): 790-814.
5. Claes S, Verdonk P, Forsyth R, et al. The " ligamentization” process in anterior cruciate ligament reconstruction: what happens to the human graft? A systematic review of the literature. Am J Sports Med, 2011, 39(11): 2476-2483.
6. Atesok K, Fu FH, Wolf MR, et al. Augmentation of tendon-to-bone healing. J Bone Joint Surg (Am), 2014, 96(6): 513-521.
7. Zhang K, Wang H, Huang C, et al. Fabrication of silk fibroin blended P(LLA-CL) nanofibrous scaffolds for tissue engineering. J Biomed Mater Res A, 2010, 93(3): 984-993.
8. Wang CY, Zhang KH, Fan CY, et al. Aligned natural-synthetic polyblend nanofibers for peripheral nerve regeneration. Acta Biomater, 2011, 7(2): 634-643.
9. Chen J, Yan C, Zhu M, et al. Electrospun nanofibrous SF/P(LLA-CL) membrane: a potential substratum for endothelial keratoplasty. Int J Nanomedicine, 2015, 10: 3337-3350.
10. Wang Z, Lin M, Xie Q, et al. Electrospun silk fibroin/poly(lactide-co-epsilon-caprolactone) nanofibrous scaffolds for bone regeneration. Int J Nanomedicine, 2016, 11: 1483-1500.
11. 高林峰, 王洪复. 骨基质 Ⅰ 型胶原的增龄性改变. 中华老年医学杂志, 2001, 20(6): 465-467.
12. Takeuchi A, Ohtsuki C, Miyazaki T, et al. Deposition of bone-like apatite on silk fiber in a solution that mimics extracellular fluid. J Biomed Mater Res A, 2003, 65(2): 283-289.
13. Shanmugavel S, Reddy VJ, Ramakrishna S, et al. Precipitation of hydroxyapatite on electrospun polycaprolactone/aloe vera/silk fibroin nanofibrous scaffolds for bone tissue engineering. J Biomater Appl, 2014, 29(1): 46-58.
14. Vetsch JR, Paulsen SJ, Müller R, et al. Effect of fetal bovine serum on mineralization in silk fibroin scaffolds. Acta Biomater, 2015, 13: 277-285.
15. Midha S, Murab S, Ghosh S. Osteogenic signaling on silk-based matrices. Biomaterials, 2016, 97: 133-153.
16. Jung SR, Song NJ, Yang DK, et al. Silk proteins stimulate osteoblast differentiation by suppressing the Notch signaling pathway in mesenchymal stem cells. Nutr Res, 2013, 33(2): 162-170.
17. Wang H, Pieper J, Peters F, et al. Synthetic scaffold morphology controls human dermal connective tissue formation. J Biomed Mater Res A, 2005, 74(4): 523-532.
18. Li Y, Jiang X, Zhong H, et al. Hierarchical Patterning of Cells with a Microeraser and Electrospun Nanofibers. Small, 2016, 12(9): 1230-1239.
19. Sperling LE, Reis KP, Pozzobon LG, et al. Influence of random and oriented electrospun fibrous poly(lactic-co-glycolic acid) scaffolds on neural differentiation of mouse embryonic stem cells. J Biomed Mater Res A, 2017, 105(5): 1333-1345.
20. Yin Z, Chen X, Chen JL, et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials, 2010, 31(8): 2163-2175.
21. Yin Z, Chen X, Song HX, et al. Electrospun scaffolds for multiple tissues regeneration in vivo through topography dependent induction of lineage specific differentiation. Biomaterials, 2015, 44: 173-185.
22. Zhang C, Yuan H, Liu H, et al. Well-aligned chitosan-based ultrafine fibers committed teno-lineage differentiation of human induced pluripotent stem cells for Achilles tendon regeneration. Biomaterials, 2015, 53: 716-730.

Chinese Journal of Reparative and Reconstructive Surgery

Effect of silk fibroin/poly (L-lactic acid-co-e-caprolactone) nanofibrous scaffold on tendon-bone healing of rabbits

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