Clinical Applications of Naturally Derived Biopolymer-Based Scaffolds for Regenerative Medicine

Abstract

Naturally derived polymeric biomaterials, such as collagens, silks, elastins, alginates, and fibrins are utilized in tissue engineering due to their biocompatibility, bioactivity, and tunable mechanical and degradation kinetics. The use of these natural biopolymers in biomedical applications is advantageous because they do not release cytotoxic degradation products, are often processed using environmentally-friendly aqueous-based methods, and their degradation rates within biological systems can be manipulated by modifying the starting formulation or processing conditions. For these reasons, many recent in vivo investigations and FDA-approval of new biomaterials for clinical use have utilized natural biopolymers as matrices for cell delivery and as scaffolds for cell-free support of native tissues. This review highlights biopolymer-based scaffolds used in clinical applications for the regeneration and repair of native tissues, with a focus on bone, skeletal muscle, peripheral nerve, cardiac muscle, and cornea substitutes.

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References

  1. 1.

    Abou Neel, E. A., L. Bozec, J. C. Knowles, O. Syed, V. Mudera, R. Day, and J. K. Hyun. Collagen—emerging collagen based therapies hit the patient. Adv. Drug Deliv. Rev. 65:429–456, 2013.

    CAS  PubMed  Google Scholar 

  2. 2.

    Alaminos, M., M. D. C. Sánchez-Quevedo, J. I. Muñoz-Ávila, D. Serrano, S. Medialdea, I. Carreras, and A. Campos. Construction of a complete rabbit cornea substitute using a fibrin-agarose scaffold. Investig. Ophthalmol. Vis. Sci. 47:3311–3317, 2006.

    Google Scholar 

  3. 3.

    Allen, R. A., W. Wu, M. Yao, D. Dutta, X. Duan, T. N. Bachman, H. C. Champion, D. B. Stolz, A. M. Robertson, and K. Kim. Nerve regeneration and elastin formation within poly (glycerol sebacate)-based synthetic arterial grafts one-year post-implantation in a rat model. Biomaterials 35:165–173, 2014.

    CAS  PubMed  Google Scholar 

  4. 4.

    Alluin, O., C. Wittmann, T. Marqueste, J.-F. Chabas, S. Garcia, M.-N. Lavaut, D. Guinard, F. Feron, and P. Decherchi. Functional recovery after peripheral nerve injury and implantation of a collagen guide. Biomaterials 30:363–373, 2009.

    CAS  PubMed  Google Scholar 

  5. 5.

    Almine, J. F., D. V. Bax, S. M. Mithieux, L. Nivison-Smith, J. Rnjak, A. Waterhouse, S. G. Wise, and A. S. Weiss. Elastin-based materials. Chem. Soc. Rev. 39:3371–3379, 2010.

    CAS  PubMed  Google Scholar 

  6. 6.

    Altman, G. H., F. Diaz, C. Jakuba, T. Calabro, R. L. Horan, J. Chen, H. Lu, J. Richmond, and D. L. Kaplan. Silk-based biomaterials. Biomaterials 24:401–416, 2003.

    CAS  PubMed  Google Scholar 

  7. 7.

    Amini, A. R., C. T. Laurencin, and S. P. Nukavarapu. Bone tissue engineering: recent advances and challenges. Crit. Rev. Biomed. Eng. 40:363–408, 2012.

    PubMed Central  PubMed  Google Scholar 

  8. 8.

    An, B., T. M. DesRochers, G. K. Qin, X. X. Xia, G. Thiagarajan, B. Brodsky, and D. L. Kaplan. The influence of specific binding of collagen-silk chimeras to silk biomaterials on hMSC behavior. Biomaterials 34:402–412, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  9. 9.

    Anitua, E., I. Andia, B. Ardanza, P. Nurden, and A. T. Nurden. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb. Haemost. 91:4–15, 2004.

    CAS  PubMed  Google Scholar 

  10. 10.

    Annabi, N., K. Tsang, S. M. Mithieux, M. Nikkhah, A. Ameri, A. Khademhosseini, and A. S. Weiss. Highly elastic micropatterned hydrogel for engineering functional cardiac tissue. Adv. Funct. Mater. 23:4950–4959, 2013.

    CAS  Google Scholar 

  11. 11.

    Astete, C. E., and C. M. Sabliov. Synthesis and characterization of plga nanoparticles. J. Biomater. Sci. Polym. Ed. 17:247–289, 2012.

    Google Scholar 

  12. 12.

    Athanasiou, K. A., G. G. Niederauer, and C. Agrawal. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/polyglycolic acid copolymers. Biomaterials 17:93–102, 1996.

    CAS  PubMed  Google Scholar 

  13. 13.

    Athanasiou, K. A., C. F. Zhu, D. R. Lanctot, C. M. Agrawal, and X. Wang. Fundamentals of biomechanics in tissue engineering of bone. Tissue Eng. 6:361–381, 2000.

    CAS  PubMed  Google Scholar 

  14. 14.

    Baldock, C., A. F. Oberhauser, L. Ma, D. Lammie, V. Siegler, S. M. Mithieux, Y. Tu, J. Y. Chow, F. Suleman, M. Malfois, S. Rogers, L. Guo, T. C. Irving, T. J. Wess, and A. S. Weiss. Shape of tropoelastin, the highly extensible protein that controls human tissue elasticity. Proc. Natl. Acad. Sci. USA 108:4322–4327, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  15. 15.

    Bartus, C., C. William Hanke, and E. Daro-Kaftan. A decade of experience with injectable poly-l-lactic acid: a focus on safety. Dermatol. Surg. 39:698–705, 2013.

    CAS  PubMed  Google Scholar 

  16. 16.

    Bell, E., B. Ivarsson, and C. Merrill. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. 76:1274–1278, 1979.

    PubMed Central  CAS  PubMed  Google Scholar 

  17. 17.

    Bellas, E., B. J. B. Panilaitis, D. L. Glettig, C. A. Kirker-Head, J. J. Yoo, K. G. Marra, J. P. Rubin, and D. L. Kaplan. Sustained volume retention in vivo with adipocyte and lipoaspirate seeded silk scaffolds. Biomaterials 34:2960–2968, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  18. 18.

    Beun, L. H., I. M. Storm, M. W. Werten, F. A. de Wolf, M. A. Cohen Stuart, and R. de Vries. From micelles to fibers: balancing self-assembling and random coiling domains in ph-responsive silk-collagen-like protein-based polymers. Biomacromolecules 15:3349–3357, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  19. 19.

    Bhola, M., S. Sanchez, and S. Kolhatkar. Use of an extracellular matrix membrane for root coverage: case series and review of the literature. Clin. Adv. Periodontics 3:16–21, 2013.

    Google Scholar 

  20. 20.

    Bhumiratana, S., W. L. Grayson, A. Castaneda, D. N. Rockwood, E. S. Gil, D. L. Kaplan, and G. Vunjak-Novakovic. Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds. Biomaterials 32:2812–2820, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  21. 21.

    Black, III, L. D., J. D. Meyers, J. S. Weinbaum, Y. A. Shvelidze, and R. T. Tranquillo. Cell-induced alignment augments twitch force in fibrin gel–based engineered myocardium via gap junction modification. Tissue Eng. Part A 15:3099–3108, 2009.

    PubMed Central  CAS  PubMed  Google Scholar 

  22. 22.

    Bond, E., S. Barrett, J. Pragnell, and R. Victoria. Successful treatment of nonhealing wounds with xelma®. Br. J. Nursing 18:1404–1409, 2009.

    Google Scholar 

  23. 23.

    Borrelli, M., S. Reichl, Y. Feng, M. Schargus, S. Schrader, and G. Geerling. In vitro characterization and ex vivo surgical evaluation of human hair keratin films in ocular surface reconstruction after sterilization processing. J. Mater. Sci. Mater. Med. 24:221–230, 2013.

    CAS  PubMed  Google Scholar 

  24. 24.

    Bose, S., M. Roy, and A. Bandyopadhyay. Recent advances in bone tissue engineering scaffolds. Trends Biotechnol. 30:546–554, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  25. 25.

    Boublik, J., H. Park, M. Radisic, E. Tognana, F. Chen, M. Pei, G. Vunjak-Novakovic, and L. E. Freed. Mechanical properties and remodeling of hybrid cardiac constructs made from heart cells, fibrin, and biodegradable, elastomeric knitted fabric. Tissue Eng. 11:1122–1132, 2005.

    CAS  PubMed  Google Scholar 

  26. 26.

    Burdick, J. A., R. L. Mauck, J. H. Gorman, and R. C. Gorman. Acellular biomaterials: an evolving alternative to cell-based therapies. Sci. Transl. Med. 5:176ps4, 2013.

    PubMed Central  PubMed  Google Scholar 

  27. 27.

    Buskens, E., M. J. Meijboom, H. Kooijman, and B. A. Van Hout. The use of a surgical sealant (coseal) in cardiac and vascular reconstructive surgery: an economic analysis. J. Cardiovasc. Surg. 47:161–170, 2006.

    CAS  Google Scholar 

  28. 28.

    Cannata, A., C. Taglieri, C. F. Russo, G. Bruschi, and L. Martinelli. Use of coseal in a patient with a left ventricular assist device. Ann. Thorac. Surg. 87:1956–1958, 2009.

    PubMed  Google Scholar 

  29. 29.

    Carlson, M., K. Faria, Y. Shamis, J. Leman, V. Ronfard, and J. Garlick. Epidermal stem cells are preserved during commercial-scale manufacture of a bilayered, living cellular construct (apligraf®). Tissue Eng. Part A 17:487–493, 2010.

    PubMed  Google Scholar 

  30. 30.

    Centers for Disease Control and Prevention. Heart disease fact sheet. Atlanta, GA: US Department of Health and Human Services, 2014.

  31. 31.

    Chen, J. L., Z. Yin, W. L. Shen, X. Chen, B. C. Heng, X. H. Zou, and H. W. Ouyang. Efficacy of hESC-MSCs in knitted silk-collagen scaffold for tendon tissue engineering and their roles. Biomaterials 31:9438–9451, 2010.

    CAS  PubMed  Google Scholar 

  32. 32.

    Chen, Q.-Z., H. Ishii, G. A. Thouas, A. R. Lyon, J. S. Wright, J. J. Blaker, W. Chrzanowski, A. R. Boccaccini, N. N. Ali, J. C. Knowles, and S. E. Harding. An elastomeric patch derived from poly(glycerol sebacate) for delivery of embryonic stem cells to the heart. Biomaterials 31:3885–3893, 2010.

    CAS  PubMed  Google Scholar 

  33. 33.

    Chicatun, F., C. E. Pedraza, C. E. Ghezzi, B. Marelli, M. T. Kaartinen, M. D. McKee, and S. N. Nazhat. Osteoid-mimicking dense collagen/chitosan hybrid gels. Biomacromolecules 12:2946–2956, 2011.

    CAS  PubMed  Google Scholar 

  34. 34.

    Chicatun, F., C. E. Pedraza, N. Muja, C. E. Ghezzi, M. D. McKee, and S. N. Nazhat. Effect of chitosan incorporation and scaffold geometry on chondrocyte function in dense collagen type I hydrogels. Tissue Eng. Part A 19:2553–2564, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  35. 35.

    Cho, O. H., C. Mallappa, J. M. Hernandez-Hernandez, J. A. Rivera-Perez, and A. N. Imbalzano. Contrasting roles for myod in organizing myogenic promoter structures during embryonic skeletal muscle development. Dev. Dyn. 2014. doi:10.1002/dvdy.24217.

  36. 36.

    Chow, D., M. L. Nunalee, D. W. Lim, A. J. Simnick, and A. Chilkoti. Peptide-based biopolymers in biomedicine and biotechnology. Mater. Sci. Eng. R 62:125–155, 2008.

    Google Scholar 

  37. 37.

    Choy, D. K. S., V. D. W. Nga, J. Lim, J. Lu, N. Chou, T. T. Yeo, and S.-H. Teoh. Brain tissue interaction with three-dimensional, honeycomb polycaprolactone-based scaffolds designed for cranial reconstruction following traumatic brain injury. Tissue Eng. Part A 19:2382–2389, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  38. 38.

    Christman, K. L., H. H. Fok, R. E. Sievers, Q. Fang, and R. J. Lee. Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng. 10:403–409, 2004.

    CAS  PubMed  Google Scholar 

  39. 39.

    Christman, K. L., A. J. Vardanian, Q. Fang, R. E. Sievers, H. H. Fok, and R. J. Lee. Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 44:654–660, 2004.

    CAS  PubMed  Google Scholar 

  40. 40.

    Cormio, L., A. Perrone, G. Di Fino, N. Ruocco, M. De Siati, J. de la Rosette, and G. Carrieri. Tachosil® sealed tubeless percutaneous nephrolithotomy to reduce urine leakage and bleeding: outcome of a randomized controlled study. J. Urol. 188:145–150, 2012.

    PubMed  Google Scholar 

  41. 41.

    Corona, B. T., M. A. Machingal, T. Criswell, M. Vadhavkar, A. C. Dannahower, C. Bergman, W. Zhao, and G. J. Christ. Further development of a tissue engineered muscle repair construct in vitro for enhanced functional recovery following implantation in vivo in a murine model of volumetric muscle loss injury. Tissue Eng. Part A 18:1213–1228, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  42. 42.

    Corona, B. T., C. L. Ward, H. B. Baker, T. J. Walters, and G. J. Christ. Implantation of in vitro tissue engineered muscle repair constructs and bladder acellular matrices partially restore in vivo skeletal muscle function in a rat model of volumetric muscle loss injury. Tissue Eng. Part A 20:705–715, 2013.

  43. 43.

    Corpas Ldos, S., I. Lambrichts, M. Quirynen, B. Collaert, C. Politis, L. Vrielinck, W. Martens, T. Struys, and R. Jacobs. Peri-implant bone innervation: histological findings in humans. Eur. J. Oral Implantol. 7:283–292, 2014.

    PubMed  Google Scholar 

  44. 44.

    Curran, M. P., and G. L. Plosker. Bilayered bioengineered skin substitute (apligraf®). BioDrugs 16:439–455, 2002.

    PubMed  Google Scholar 

  45. 45.

    Curren, R. D., and J. W. Harbell. Ocular safety: a silent (in vitro) success story. Altern. Lab. Anim. 30(Suppl 2):69–74, 2002.

    CAS  PubMed  Google Scholar 

  46. 46.

    Dahl, S. L. M., A. P. Kypson, J. H. Lawson, J. L. Blum, J. T. Strader, Y. Li, R. J. Manson, W. E. Tente, L. DiBernardo, M. T. Hensley, R. Carter, T. P. Williams, H. L. Prichard, M. S. Dey, K. G. Begelman, and L. E. Niklason. Readily available tissue-engineered vascular grafts. Sci. Transl. Med. 3:68ra9, 2011.

    PubMed  Google Scholar 

  47. 47.

    Dan, H., C. Vaquette, A. G. Fisher, S. M. Hamlet, Y. Xiao, D. W. Hutmacher, and S. Ivanovski. The influence of cellular source on periodontal regeneration using calcium phosphate coated polycaprolactone scaffold supported cell sheets. Biomaterials 35:113–122, 2014.

    CAS  PubMed  Google Scholar 

  48. 48.

    De la Riva, B., C. Nowak, E. Sanchez, A. Hernandez, M. Schulz-Siegmund, M. K. Pec, A. Delgado, and C. Evora. VEGF-controlled release within a bone defect from alginate/chitosan/PLA-H scaffolds. Eur. J. Pharm. Biopharm. 73:50–58, 2009.

    PubMed  Google Scholar 

  49. 49.

    De Luca, A. C., J. S. Stevens, S. L. M. Schroeder, J. B. Guilbaud, A. Saiani, S. Downes, and G. Terenghi. Immobilization of cell-binding peptides on poly-ε-caprolactone film surface to biomimic the peripheral nervous system. J. Biomed. Mater. Res. Part A 101:491–501, 2013.

    Google Scholar 

  50. 50.

    de Peppo, G. M., I. Marcos-Campos, D. J. Kahler, D. Alsalman, L. Shang, G. Vunjak-Novakovic, and D. Marolt. Engineering bone tissue substitutes from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 110:8680–8685, 2013.

    PubMed Central  PubMed  Google Scholar 

  51. 51.

    de Valence, S., J.-C. Tille, D. Mugnai, W. Mrowczynski, R. Gurny, M. Möller, and B. H. Walpoth. Long term performance of polycaprolactone vascular grafts in a rat abdominal aorta replacement model. Biomaterials 33:38–47, 2012.

    PubMed  Google Scholar 

  52. 52.

    Deal, D. N., J. W. Griffin, and M. V. Hogan. Nerve conduits for nerve repair or reconstruction. J. Am. Acad. Orthop. Surg. 20:63–68, 2012.

    PubMed  Google Scholar 

  53. 53.

    Deng, Y., X. Bi, H. Zhou, Z. You, Y. Wang, P. Gu, and X. Fan. Repair of critical-sized bone defects with anti-mir-31-expressing bone marrow stromal stem cells and poly (glycerol sebacate) scaffolds. Eur. Cells Mater. 27:13, 2014.

    CAS  Google Scholar 

  54. 54.

    Dhanraj, P. A clinical study comparing helicoll with scarlet red and opsite in the treatment of split thickness skin graft donor sites—a randomized controlled trial. Indian J. Surg. 2013. doi:10.1007/s12262-013-0850-3.

  55. 55.

    Dhawan, V., I. F. Lytle, D. E. Dow, Y.-C. Huang, and D. L. Brown. Neurotization improves contractile forces of tissue-engineered skeletal muscle. Tissue Eng. 13:2813–2821, 2007.

    CAS  PubMed  Google Scholar 

  56. 56.

    Di Martino, A., M. Sittinger, and M. V. Risbud. Chitosan: a versatile biopolymer for orthopaedic tissue-engineering. Biomaterials 26:5983–5990, 2005.

    PubMed  Google Scholar 

  57. 57.

    Diab, T., E. M. Pritchard, B. A. Uhrig, J. D. Boerckel, D. L. Kaplan, and R. E. Guldberg. A silk hydrogel-based delivery system of bone morphogenetic protein for the treatment of large bone defects. J. Mech. Behav. Biomed. Mater. 11:123–131, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  58. 58.

    Dornseifer, U., D. Lonic, T. I. Gerstung, F. Herter, A. M. Fichter, C. Holm, T. Schuster, and M. Ninkovic. The ideal split-thickness skin graft donor-site dressing: a clinical comparative trial of a modified polyurethane dressing and aquacel. Plast. Reconstr. Surg. 128:918–924, 2011.

    CAS  PubMed  Google Scholar 

  59. 59.

    Dorozhkin, S. V. Calcium orthophosphate-based biocomposites and hybrid biomaterials. J. Mater. Sci. 44:2343–2387, 2009.

    CAS  Google Scholar 

  60. 60.

    Downie, F., and R. Gannon. Opsite flexifix gentle: preventing skin breakdown in vulnerable skin. Br. J. Nurs. 22:698–700, 2013.

  61. 61.

    Driscoll, P. Tissue engineering, cell therapy, and transplantation: products, technologies, and market opportunities worldwide: 2009–2018. Tissue Eng. Cell Ther. 2010. http://www.mediligence.com/rpt/rpt-s520.htm.

  62. 62.

    Dvir, T., B. P. Timko, M. D. Brigham, S. R. Naik, S. S. Karajanagi, O. Levy, H. Jin, K. K. Parker, R. Langer, and D. S. Kohane. Nanowired three-dimensional cardiac patches. Nat. Nanotechnol. 6:720–725, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  63. 63.

    Eaglstein, W. H., and V. Falanga. Tissue engineering and the development of apligraf®, a human skin equivalent. Clin. Ther. 19:894–905, 1997.

    CAS  PubMed  Google Scholar 

  64. 64.

    Ellis, C. N. Outcomes with the use of bioprosthetic grafts to reinforce the ligation of the intersphincteric fistula tract (biolift procedure) for the management of complex anal fistulas. Dis. Colon Rectum 53:1361–1364, 2010.

    PubMed  Google Scholar 

  65. 65.

    Engelmayr, Jr., G. C., M. Cheng, C. J. Bettinger, J. T. Borenstein, R. Langer, and L. E. Freed. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat. Mater. 7:1003–1010, 2008.

    PubMed Central  CAS  PubMed  Google Scholar 

  66. 66.

    Erb, M. A., T. Claus, M. Hartrumpf, S. Bachmann, and J. M. Albes. The use of tachosil® surgical patch or fibrin glue in coronary artery surgery does not affect quality of anastomosis or provoke postoperative adhesions in pigs. Eur. J. Cardiothorac. Surg. 36:703–707, 2009.

    PubMed  Google Scholar 

  67. 67.

    Etienne, O., A. Schneider, J. A. Kluge, C. Bellemin-Laponnaz, C. Polidori, G. G. Leisk, D. L. Kaplan, J. A. Garlick, and C. Egles. Soft tissue augmentation using silk gels: an in vitro and in vivo study. J. Periodontol. 80:1852–1858, 2009.

    PubMed Central  PubMed  Google Scholar 

  68. 68.

    Fagerholm, P., N. S. Lagali, K. Merrett, W. B. Jackson, R. Munger, Y. Liu, J. W. Polarek, M. Soderqvist, and M. Griffith. A biosynthetic alternative to human donor tissue for inducing corneal regeneration: 24-month follow-up of a phase 1 clinical study. Sci. Transl. Med. 2:46ra61, 2010.

    PubMed  Google Scholar 

  69. 69.

    Fagerholm, P., N. S. Lagali, J. A. Ong, K. Merrett, W. B. Jackson, J. W. Polarek, E. J. Suuronen, Y. Liu, I. Brunette, and M. Griffith. Stable corneal regeneration four years after implantation of a cell-free recombinant human collagen scaffold. Biomaterials 35:2420–2427, 2014.

    CAS  PubMed  Google Scholar 

  70. 70.

    Falabella, A. F., L. A. Schachner, I. C. Valencia, and W. H. Eaglstein. The use of tissue-engineered skin (apligraf) to treat a newborn with epidermolysis bullosa. Arch. Dermatol. 135:1219–1222, 1999.

    CAS  PubMed  Google Scholar 

  71. 71.

    Falabella, A. F., I. C. Valencia, W. H. Eaglstein, and L. A. Schachner. Tissue-engineered skin (apligraf) in the healing of patients with epidermolysis bullosa wounds. Arch. Dermatol. 136:1225–1230, 2000.

    CAS  PubMed  Google Scholar 

  72. 72.

    Falanga, V., and M. Sabolinski. A bilayered living skin construct (apligraf®) accelerates complete closure of hard-to-heal venous ulcers. Wound Repair Regen. 7:201–207, 1999.

    CAS  PubMed  Google Scholar 

  73. 73.

    Fan, T., X. Ma, J. Zhao, Q. Wen, X. Hu, H. Yu, and W. Shi. Transplantation of tissue-engineered human corneal endothelium in cat models. Mol. Vis. 19:400–407, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  74. 74.

    Ferreira, A. M., P. Gentile, V. Chiono, and G. Ciardelli. Collagen for bone tissue regeneration. Acta Biomater. 8:3191–3200, 2012.

    CAS  PubMed  Google Scholar 

  75. 75.

    Fishman, J. M., A. Tyraskis, P. Maghsoudlou, L. Urbani, G. Totonelli, M. A. Birchall, and P. De Coppi. Skeletal muscle tissue engineering: which cell to use? Tissue Eng. Part B 19:503–515, 2013.

    CAS  Google Scholar 

  76. 76.

    Fivenson, D., and L. Scherschun. Clinical and economic impact of apligraf® for the treatment of nonhealing venous leg ulcers. Int. J. Dermatol. 42:960–965, 2003.

    CAS  PubMed  Google Scholar 

  77. 77.

    Foster, T. E., B. L. Puskas, B. R. Mandelbaum, M. B. Gerhardt, and S. A. Rodeo. Platelet-rich plasma from basic science to clinical applications. Am. J. Sports Med. 37:2259–2272, 2009.

    PubMed  Google Scholar 

  78. 78.

    Francis, N. L., P. M. Hunger, A. E. Donius, B. W. Riblett, A. Zavaliangos, U. G. K. Wegst, and M. A. Wheatley. An ice-templated, linearly aligned chitosan-alginate scaffold for neural tissue engineering. J. Biomed. Mater. Res. Part A 101:3493–3503, 2013.

    Google Scholar 

  79. 79.

    Garkavenko, O., S. Wynyard, D. Nathu, T. Quane, K. Durbin, J. Denner, and R. Elliott. The first clinical xenotransplantation trial in new zealand: efficacy and safety. Xenotransplantation 19:6, 2012.

    Google Scholar 

  80. 80.

    Gentzkow, G. D., S. D. Iwasaki, K. S. Hershon, M. Mengel, J. J. Prendergast, J. J. Ricotta, D. P. Steed, and S. Lipkin. Use of dermagraft, a cultured human dermis, to treat diabetic foot ulcers. Diabetes Care 19:350–354, 1996.

    CAS  PubMed  Google Scholar 

  81. 81.

    Geuze, R. E., L. F. Theyse, D. H. Kempen, H. A. Hazewinkel, H. Y. Kraak, F. C. Oner, W. J. Dhert, and J. Alblas. A differential effect of bone morphogenetic protein-2 and vascular endothelial growth factor release timing on osteogenesis at ectopic and orthotopic sites in a large-animal model. Tissue Eng. Part A 18:2052–2062, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  82. 82.

    Ghezzi, C. E., B. Marelli, N. Muja, N. Hirota, J. G. Martin, J. E. Barralet, A. Alessandrino, G. Freddi, and S. N. Nazhat. Mesenchymal stem cell-seeded multilayered dense collagen-silk fibroin hybrid for tissue engineering applications. Biotechnol. J. 6:1198–1207, 2011.

    CAS  PubMed  Google Scholar 

  83. 83.

    Ghezzi, C. E., B. Marelli, N. Muja, and S. N. Nazhat. Immediate production of a tubular dense collagen construct with bioinspired mechanical properties. Acta Biomater. 8:1813–1825, 2012.

    CAS  PubMed  Google Scholar 

  84. 84.

    Ghezzi, C. E., N. Muja, B. Marelli, and S. N. Nazhat. Real time responses of fibroblasts to plastically compressed fibrillar collagen hydrogels. Biomaterials 32:4761–4772, 2011.

    CAS  PubMed  Google Scholar 

  85. 85.

    Ghezzi, C. E., P. A. Risse, B. Marelli, N. Muja, J. E. Barralet, J. G. Martin, and S. N. Nazhat. An airway smooth muscle cell niche under physiological pulsatile flow culture using a tubular dense collagen construct. Biomaterials 34:1954–1966, 2013.

    CAS  PubMed  Google Scholar 

  86. 86.

    Ghezzi, C. E., J. Rnjak-Kovacina, A. S. Weiss, and D. L. Kaplan. Multifunctional silk-tropoelastin biomaterial systems. Isr. J. Chem. 53:777–786, 2013.

    CAS  Google Scholar 

  87. 87.

    Gil, E. S., B. B. Mandal, S. H. Park, J. K. Marchant, F. G. Omenetto, and D. L. Kaplan. Helicoidal multi-lamellar features of RGD-functionalized silk biomaterials for corneal tissue engineering. Biomaterials 31:8953–8963, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  88. 88.

    Gil, E. S., S. H. Park, J. Marchant, F. Omenetto, and D. L. Kaplan. Response of human corneal fibroblasts on silk film surface patterns. Macromol. Biosci. 10:664–673, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  89. 89.

    Grassl, E. D., T. R. Oegema, and R. T. Tranquillo. Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J. Biomed. Mater. Res. 60:607–612, 2002.

    CAS  PubMed  Google Scholar 

  90. 90.

    Grau, A. E., and J. A. Durán. Treatment of a large corneal perforation with a multilayer of amniotic membrane and tachosil. Cornea 31:98–100, 2012.

    PubMed  Google Scholar 

  91. 91.

    Griffith, M., R. Osborne, R. Munger, X. Xiong, C. J. Doillon, N. L. Laycock, M. Hakim, Y. Song, and M. A. Watsky. Functional human corneal equivalents constructed from cell lines. Science 286:2169–2172, 1999.

    CAS  PubMed  Google Scholar 

  92. 92.

    Griffiths, M., N. Ojeh, R. Livingstone, R. Price, and H. Navsaria. Survival of apligraf in acute human wounds. Tissue Eng. 10:1180–1195, 2004.

    CAS  PubMed  Google Scholar 

  93. 93.

    Gu, X., F. Ding, and D. F. Williams. Neural tissue engineering options for peripheral nerve regeneration. Biomaterials 35:6143–6156, 2014.

    CAS  PubMed  Google Scholar 

  94. 94.

    Guan, L., H. Ge, X. Tang, S. Su, P. Tian, N. Xiao, H. Zhang, L. Zhang, and P. Liu. Use of a silk fibroin-chitosan scaffold to construct a tissue-engineered corneal stroma. Cells Tissues Organs 198:190–197, 2013.

    CAS  PubMed  Google Scholar 

  95. 95.

    Guo, X., M. Das, J. Rumsey, M. Gonzalez, M. Stancescu, and J. Hickman. Neuromuscular junction formation between human stem-cell-derived motoneurons and rat skeletal muscle in a defined system. Tissue Eng. Part C 16:1347–1355, 2010.

    Google Scholar 

  96. 96.

    Guyer, R. D., S. G. Tromanhauser, and J. J. Regan. An economic model of one-level lumbar arthroplasty versus fusion. Spine J. Off. J. N. Am. Spine Soc. 7:558–562, 2007.

    Google Scholar 

  97. 97.

    Hall, K. K., K. M. Gattás-Asfura, and C. L. Stabler. Microencapsulation of islets within alginate/poly(ethylene glycol) gels cross-linked via staudinger ligation. Acta Biomater. 7:614–624, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  98. 98.

    Hallab, N. J. Hypersensitivity to implant debris. Degrad. Implant Mater. 2012:329–345, 2012.

    Google Scholar 

  99. 99.

    Han, J., P. Lazarovici, C. Pomerantz, X. Chen, Y. Wei, and P. I. Lelkes. Co-electrospun blends of plga, gelatin, and elastin as potential nonthrombogenic scaffolds for vascular tissue engineering. Biomacromolecules 12:399–408, 2010.

    PubMed  Google Scholar 

  100. 100.

    Hansbrough, J. F., D. W. Mozingo, G. P. Kealey, M. Davis, A. Gidner, and G. D. Gentzkow. Clinical trials of a biosynthetic temporary skin replacement, dermagraft-transitional covering, compared with cryopreserved human cadaver skin for temporary coverage of excised burn wounds. J. Burn Care Res. 18:43–51, 1997.

    CAS  Google Scholar 

  101. 101.

    Hart, C. E., A. Loewen-Rodriguez, and J. Lessem. Dermagraft: use in the treatment of chronic wounds. Adv. Wound Care 1:138–141, 2012.

    Google Scholar 

  102. 102.

    Hauser, M., A. Eicken, A. Kuehn, J. Hess, S. Fratz, P. Ewert, and H. Kaemmerer. Managing the right ventricular outflow tract for pulmonary regurgitation after tetralogy of fallot repair. Heart Asia 5:106–111, 2013.

    Google Scholar 

  103. 103.

    Hayabuchi, Y., K. Mori, T. Kitagawa, M. Sakata, and S. Kagami. Polytetrafluoroethylene graft calcification in patients with surgically repaired congenital heart disease: evaluation using multidetector-row computed tomography. Am. Heart J. 153:806.e1–806.e8, 2007.

    Google Scholar 

  104. 104.

    Herrmann, J. B., R. J. Kelly, and G. A. Higgins. Polyglycolic acid sutures: laboratory and clinical evaluation of a new absorbable suture material. Arch. Surg. 100:486–490, 1970.

    CAS  PubMed  Google Scholar 

  105. 105.

    Hoffman, A. S. Stimuli-responsive polymers: biomedical applications and challenges for clinical translation. Adv. Drug Deliv. Rev. 65:10–16, 2013.

    CAS  PubMed  Google Scholar 

  106. 106.

    Hofmann, S., M. Hilbe, R. J. Fajardo, H. Hagenmueller, K. Nuss, M. Arras, R. Mueller, B. von Rechenberg, D. L. Kaplan, H. P. Merkle, and L. Meinel. Remodeling of tissue-engineered bone structures in vivo. Eur. J. Pharm. Biopharm. 85:119–129, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  107. 107.

    Holzapfel, B. M., J. C. Reichert, J.-T. Schantz, U. Gbureck, L. Rackwitz, U. Noeth, F. Jakob, M. Rudert, J. Groll, and D. W. Hutmacher. How smart do biomaterials need to be? A translational science and clinical point of view. Adv. Drug Deliv. Rev. 65:581–603, 2013.

    CAS  PubMed  Google Scholar 

  108. 108.

    Hong, Y., A. Huber, K. Takanari, N. J. Amoroso, R. Hashizume, S. F. Badylak, and W. R. Wagner. Mechanical properties and in vivo behavior of a biodegradable synthetic polymer microfiber–extracellular matrix hydrogel biohybrid scaffold. Biomaterials 32:3387–3394, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  109. 109.

    Hu, S., R. S. Kirsner, V. Falanga, T. Phillips, and W. H. Eaglstein. Evaluation of apligraf® persistence and basement membrane restoration in donor site wounds: a pilot study. Wound Repair Regen. 14:427–433, 2006.

    PubMed  Google Scholar 

  110. 110.

    Hu, X., X. Wang, J. Rnjak, A. S. Weiss, and D. L. Kaplan. Biomaterials derived from silk-tropoelastin protein systems. Biomaterials 31:8121–8131, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  111. 111.

    Huang, A. H., and L. E. Niklason. Engineering biological-based vascular grafts using a pulsatile bioreactor. J. Vis. Exp. 2011. doi:10.3791/2646.

  112. 112.

    Ilic, D. Industry update: latest developments in the field of stem cell research and regenerative medicine compiled from publicly available information and press releases from nonacademic institutions from 1 November 2013 until 31 December 2013. Regen. Med. 9:137–143, 2014.

    CAS  Google Scholar 

  113. 113.

    Japan Tissue Engineering Company. Labcyte cornea model product page. 2014. http://www.jpte.co.jp/english/business/LabCyte/CORNEAmodel.html.

  114. 114.

    Jell, G., D. Kerjaschki, P. Revell, and N. Al-Saffar. Lymphangiogenesis in the bone-implant interface of orthopedic implants: importance and consequence. J. Biomed. Mater. Res. A 77:119–127, 2006.

    PubMed  Google Scholar 

  115. 115.

    Kaiser, D., J. Hafner, D. Mayer, L. E. French, and S. Lauchli. Alginate dressing and polyurethane film versus paraffin gauze in the treatment of split-thickness skin graft donor sites: a randomized controlled pilot study. Adv. Skin Wound Care 26:67–73, 2013.

    PubMed  Google Scholar 

  116. 116.

    Kanjickal, D., S. Lopina, M. M. Evancho-Chapman, S. Schmidt, and D. Donovan. Effects of sterilization on poly(ethylene glycol) hydrogels. J. Biomed. Mater. Res. Part A 87A:608–617, 2008.

    CAS  Google Scholar 

  117. 117.

    Karr, J. C. Retrospective comparison of diabetic foot ulcer and venous stasis ulcer healing outcome between a dermal repair scaffold (primatrix) and a bilayered living cell therapy (apligraf). Adv. Skin Wound Care 24:119–125, 2011.

    PubMed  Google Scholar 

  118. 118.

    Kawazoe, N., C. Inoue, T. Tateishi, and G. Chen. A cell leakproof PLGA-collagen hybrid scaffold for cartilage tissue engineering. Biotechnol. Prog. 26:819–826, 2010.

    CAS  PubMed  Google Scholar 

  119. 119.

    Kehoe, S., X. F. Zhang, and D. Boyd. FDA approved guidance conduits and wraps for peripheral nerve injury: a review of materials and efficacy. Injury 43:553–572, 2012.

    CAS  PubMed  Google Scholar 

  120. 120.

    Kierstan, M., and C. Bucke. The immobilization of microbial cells, subcellular organelles, and enzymes in calcium alginate gels. Biotechnol. Bioeng. 19:387–397, 1977.

    CAS  PubMed  Google Scholar 

  121. 121.

    Kim, D. M., M. Nevins, M. Camelo, P. Schupbach, S.-W. Kim, J. M. Camelo, K. Al Hezaimi, and M. L. Nevins. The feasibility of demineralized bone matrix and cancellous bone chips in conjunction with an extracellular matrix membrane for alveolar ridge preservation: a case series. Int. J. Periodontics Restor. Dent. 31:39–47, 2011.

    CAS  Google Scholar 

  122. 122.

    Kim, J., S. McBride, B. Tellis, P. Alvarez-Urena, Y.-H. Song, D. D. Dean, V. L. Sylvia, H. Elgendy, J. Ong, and J. O. Hollinger. Rapid-prototyped PLGA/beta-TCP/hydroxyapatite nanocomposite scaffolds in a rabbit femoral defect model. Biofabrication 4:025003, 2012.

    PubMed  Google Scholar 

  123. 123.

    Kirsner, R. S. The use of apligraf in acute wounds. J. Dermatol. 25:805–811, 1998.

    CAS  PubMed  Google Scholar 

  124. 124.

    Knoll, L. D. Use of porcine small intestinal submucosal graft in the surgical management of peyronie’s disease. Urology 57:753–757, 2001.

    CAS  PubMed  Google Scholar 

  125. 125.

    Ko, I. K., B.-K. Lee, S. J. Lee, K.-E. Andersson, A. Atala, and J. J. Yoo. The effect of in vitro formation of acetylcholine receptor (ACHR) clusters in engineered muscle fibers on subsequent innervation of constructs in vivo. Biomaterials 34:3246–3255, 2013.

    CAS  PubMed  Google Scholar 

  126. 126.

    Kolambkar, Y. M., K. M. Dupont, J. D. Boerckel, N. Huebsch, D. J. Mooney, D. W. Hutmacher, and R. E. Guldberg. An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials 32:65–74, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  127. 127.

    Komura, M., H. Komura, Y. Kanamori, Y. Tanaka, K. Suzuki, M. Sugiyama, S. Nakahara, H. Kawashima, A. Hatanaka, K. Hoshi, Y. Ikada, Y. Tabata, and T. Iwanaka. An animal model study for tissue-engineered trachea fabricated from a biodegradable scaffold using chondrocytes to augment repair of tracheal stenosis. J. Pediatr. Surg. 43:2141–2146, 2008.

    PubMed  Google Scholar 

  128. 128.

    Kreutziger, K. L., and C. E. Murry. Engineered human cardiac tissue. Pediatr. Cardiol. 32:334–341, 2011.

    PubMed Central  PubMed  Google Scholar 

  129. 129.

    Krishnan, L., N. Willett, and R. Guldberg. Vascularization strategies for bone regeneration. Ann. Biomed. Eng. 42:432–444, 2014.

    PubMed  Google Scholar 

  130. 130.

    Kwon, H., L. Sun, D. M. Cairns, R. S. Rainbow, R. C. Preda, D. L. Kaplan, and L. Zeng. The influence of scaffold material on chondrocytes under inflammatory conditions. Acta Biomater. 9:6563–6575, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  131. 131.

    Lawrence, B. D., J. K. Marchant, M. A. Pindrus, F. G. Omenetto, and D. L. Kaplan. Silk film biomaterials for cornea tissue engineering. Biomaterials 30:1299–1308, 2009.

    PubMed Central  CAS  PubMed  Google Scholar 

  132. 132.

    Lee, E., F. K. Kasper, and A. Mikos. Biomaterials for tissue engineering. Ann. Biomed. Eng. 42:323–337, 2014.

    PubMed Central  PubMed  Google Scholar 

  133. 133.

    Lee, K. Y., and D. J. Mooney. Alginate: properties and biomedical applications. Prog. Polym. Sci. 37:106–126, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  134. 134.

    Leslie-Barbick, J. E., J. E. Saik, D. J. Gould, M. E. Dickinson, and J. L. West. The promotion of microvasculature formation in poly(ethylene glycol) diacrylate hydrogels by an immobilized VEGF-mimetic peptide. Biomaterials 32:5782–5789, 2011.

    CAS  PubMed  Google Scholar 

  135. 135.

    Liao, I. C., F. T. Moutos, B. T. Estes, X. Zhao, and F. Guilak. Composite three-dimensional woven scaffolds with interpenetrating network hydrogels to create functional synthetic articular cartilage. Adv. Funct. Mater. 23:5833–5839, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  136. 136.

    Lin, C. C., and K. S. Anseth. Glucagon-like peptide-1 functionalized PEG hydrogels promote survival and function of encapsulated pancreatic beta-cells. Biomacromolecules 10:2460–2467, 2009.

    PubMed Central  CAS  PubMed  Google Scholar 

  137. 137.

    Lin, W., R. W. Burgess, B. Dominguez, S. L. Pfaff, J. R. Sanes, and K. F. Lee. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057–1064, 2001.

    CAS  PubMed  Google Scholar 

  138. 138.

    Liu, J., B. D. Lawrence, A. Liu, I. R. Schwab, L. A. Oliveira, and M. I. Rosenblatt. Silk fibroin as a biomaterial substrate for corneal epithelial cell sheet generation. Investig. Ophthalmol. Vis. Sci. 53:4130–4138, 2012.

    CAS  Google Scholar 

  139. 139.

    Liu, W., K. Merrett, M. Griffith, P. Fagerholm, S. Dravida, B. Heyne, J. C. Scaiano, M. A. Watsky, N. Shinozaki, N. Lagali, R. Munger, and F. Li. Recombinant human collagen for tissue engineered corneal substitutes. Biomaterials 29:1147–1158, 2008.

    CAS  PubMed  Google Scholar 

  140. 140.

    Liu, Y., N. Li, Y.-P. Qi, L. Dai, T. E. Bryan, J. Mao, D. H. Pashley, and F. R. Tay. Intrafibrillar collagen mineralization produced by biomimetic hierarchical nanoapatite assembly. Adv. Mater. 23:975–980, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  141. 141.

    Living Cell Technologies. Diabecell product page. 2014. http://www.lctglobal.com/products/diabecell.

  142. 142.

    Living Cell Technologies. Ntcell product page. 2014. http://www.lctglobal.com/products/ntcell.

  143. 143.

    Luo, H., Y. Lu, T. Wu, M. Zhang, Y. Zhang, and Y. Jin. Construction of tissue-engineered cornea composed of amniotic epithelial cells and acellular porcine cornea for treating corneal alkali burn. Biomaterials 34:6748–6759, 2013.

    CAS  PubMed  Google Scholar 

  144. 144.

    Luvizuto, E. R., S. Tangl, G. Zanoni, T. Okamoto, C. K. Sonoda, R. Gruber, and R. Okamoto. The effect of bmp-2 on the osteoconductive properties of [beta]-tricalcium phosphate in rat calvaria defects. Biomaterials 32:3855–3861, 2011.

    CAS  PubMed  Google Scholar 

  145. 145.

    Ma, H. Y., J. A. Hu, and P. X. Ma. Polymer scaffolds for small-diameter vascular tissue engineering. Adv. Funct. Mater. 20:2833–2841, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  146. 146.

    Ma, L., C. Gao, Z. Mao, J. Zhou, J. Shen, X. Hu, and C. Han. Collagen/chitosan porous scaffolds with improved biostability for skin tissue engineering. Biomaterials 24:4833–4841, 2003.

    CAS  PubMed  Google Scholar 

  147. 147.

    Machingal, M. A., B. T. Corona, T. J. Walters, V. Kesireddy, C. N. Koval, A. Dannahower, W. Zhao, J. J. Yoo, and G. J. Christ. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng. Part A 17:2291–2303, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  148. 148.

    Mackinnon, S. E., and A. L. Dellon. Clinical nerve reconstruction with a bioabsorbable polyglycolic acid tube. Plast. Reconstr. Surg. 85:419–424, 1990.

    CAS  PubMed  Google Scholar 

  149. 149.

    Maisano, F., H. K. Kjærgård, R. Bauernschmitt, A. Pavie, G. Rábago, M. Laskar, J. P. Marstein, and V. Falk. Tachosil surgical patch versus conventional haemostatic fleece material for control of bleeding in cardiovascular surgery: a randomised controlled trial. Eur. J. Cardiothorac. Surg. 36:708–714, 2009.

    PubMed  Google Scholar 

  150. 150.

    Mandal, B. B., A. Grinberg, E. S. Gil, B. Panilaitis, and D. L. Kaplan. High-strength silk protein scaffolds for bone repair. Proc. Natl. Acad. Sci. USA 109:7699–7704, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  151. 151.

    Marelli, B., C. E. Ghezzi, A. Alessandrino, J. E. Barralet, G. Freddi, and S. N. Nazhat. Silk fibroin derived polypeptide-induced biomineralization of collagen. Biomaterials 33:102–108, 2012.

    CAS  PubMed  Google Scholar 

  152. 152.

    Marelli, B., C. E. Ghezzi, J. E. Barralet, A. R. Boccaccini, and S. N. Nazhat. Three-dimensional mineralization of dense nanofibrillar collagen-bioglass hybrid scaffolds. Biomacromolecules 11:1470–1479, 2010.

    CAS  PubMed  Google Scholar 

  153. 153.

    Marelli, B., C. E. Ghezzi, J. E. Barralet, and S. N. Nazhat. Collagen gel fibrillar density dictates the extent of mineralization in vitro. Soft Matter 7:9898–9907, 2011.

    CAS  Google Scholar 

  154. 154.

    Marelli, B., C. E. Ghezzi, D. Mohn, W. J. Stark, J. E. Barralet, A. R. Boccaccini, and S. N. Nazhat. Accelerated mineralization of dense collagen-nano bioactive glass hybrid gels increases scaffold stiffness and regulates osteoblastic function. Biomaterials 32:8915–8926, 2011.

    CAS  PubMed  Google Scholar 

  155. 155.

    Marston, W. A. Dermagraft®, a bioengineered human dermal equivalent for the treatment of chronic nonhealing diabetic foot ulcer. Expert Rev. Med. Devices 1:21–31, 2004.

    CAS  PubMed  Google Scholar 

  156. 156.

    Marston, W. A., J. Hanft, P. Norwood, and R. Pollak. The efficacy and safety of dermagraft in improving the healing of chronic diabetic foot ulcers results of a prospective randomized trial. Diabetes Care 26:1701–1705, 2003.

    PubMed  Google Scholar 

  157. 157.

    Marta, G. M., F. Facciolo, L. Ladegaard, H. Dienemann, A. Csekeo, F. Rea, S. Dango, L. Spaggiari, V. Tetens, and W. Klepetko. Efficacy and safety of tachosil® versus standard treatment of air leakage after pulmonary lobectomy. Eur. J. Cardiothorac. Surg. 38:683–689, 2010.

    PubMed  Google Scholar 

  158. 158.

    Martino, M. M., F. Tortelli, M. Mochizuki, S. Traub, D. Ben-David, G. A. Kuhn, R. Müller, E. Livne, S. A. Eming, and J. A. Hubbell. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 3:100ra89, 2011.

    PubMed  Google Scholar 

  159. 159.

    Martins, A. M., G. Eng, S. G. Caridade, J. F. Mano, R. L. Reis, and G. Vunjak-Novakovic. Electrically conductive chitosan/carbon scaffolds for cardiac tissue engineering. Biomacromolecules 15:635–643, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  160. 160.

    Matsuura, K., Y. Haraguchi, T. Shimizu, and T. Okano. Cell sheet transplantation for heart tissue repair. J. Controlled Release 169:336–340, 2013.

    CAS  Google Scholar 

  161. 161.

    MatTekCorporation. Mattek corporation: In vitro tissue models, Ashland, MA. 2014. http://www.mattek.com/.

  162. 162.

    McCarty, L. P., D. D. Buss, M. W. Datta, M. Q. Freehill, and M. R. Giveans. Complications observed following labral or rotator cuff repair with use of poly-l-lactic acid implants. J. Bone Jt. Surg. 95:507–511, 2013.

    Google Scholar 

  163. 163.

    McHugh, K. J., S. L. Tao, and M. Saint-Geniez. Porous poly (ε-caprolactone) scaffolds for retinal pigment epithelium transplantation. Investig. Ophthalmol. Vis. Sci. 55:1754–1762, 2014.

    CAS  Google Scholar 

  164. 164.

    McInnes, A. Consensus statement on the use of xelma in diabetic foot ulcers. Diabetic Foot 13:148–151, 2010.

    Google Scholar 

  165. 165.

    McNamara, S. L., J. Rnjak-Kovacina, D. F. Schmidt, T. J. Lo, and D. L. Kaplan. Silk as a biocohesive sacrificial binder in the fabrication of hydroxyapatite load bearing scaffolds. Biomaterials 35:6941–6953, 2014.

    CAS  PubMed  Google Scholar 

  166. 166.

    Meek, M. F., and J. H. Coert. US food and drug administration/conformit Europe-approved absorbable nerve conduits for clinical repair of peripheral and cranial nerves. Ann. Plast. Surg. 60:110–116, 2008.

    CAS  PubMed  Google Scholar 

  167. 167.

    Meek, M. F., and J. H. Coert. Recovery of two-point discrimination function after digital nerve repair in the hand using resorbable FDA- and CE-approved nerve conduits. J. Plast. Reconstr. Aesthet. Surg. 66:1307–1315, 2013.

    PubMed  Google Scholar 

  168. 168.

    Meinel, L., S. Hofmann, V. Karageorgiou, C. Kirker-Head, J. McCool, G. Gronowicz, L. Zichner, R. Langer, G. Vunjak-Novakovic, and D. L. Kaplan. The inflammatory responses to silk films in vitro and in vivo. Biomaterials 26:147–155, 2005.

    CAS  PubMed  Google Scholar 

  169. 169.

    Mi, S. L., B. Chen, B. Wright, and C. J. Connon. Ex vivo construction of an artificial ocular surface by combination of corneal limbal epithelial cells and a compressed collagen scaffold containing keratocytes. Tissue Eng. Part A 16:2091–2100, 2010.

    CAS  PubMed  Google Scholar 

  170. 170.

    Miklas, J. W., S. S. Nunes, A. Sofla, L. A. Reis, A. Pahnke, Y. Xiao, C. Laschinger, and M. Radisic. Bioreactor for modulation of cardiac microtissue phenotype by combined static stretch and electrical stimulation. Biofabrication 6:024113, 2014.

    PubMed  Google Scholar 

  171. 171.

    Mirza, D., A. J. W. Millar, K. Sharif, H. Vilca-Melendez, M. Rela, and N. Heaton. The use of tachosil in children undergoing liver resection with or without segmental liver transplantation. Eur. J. Pediatr. Surg. 21:111–115, 2011.

    CAS  PubMed  Google Scholar 

  172. 172.

    Mithieux, S. M., S. G. Wise, and A. S. Weiss. Tropoelastin—a multifaceted naturally smart material. Adv. Drug Deliv. Rev. 65:421–428, 2013.

    CAS  PubMed  Google Scholar 

  173. 173.

    Morgan, K. Y., and L. D. Black, III. It’s all in the timing: modeling isovolumic contraction through development and disease with a dynamic dual electromechanical bioreactor system. Organogenesis 10:1, 2014.

    Google Scholar 

  174. 174.

    Morgan, K. Y., and L. D. Black, III. Mimicking isovolumic contraction with combined electromechanical stimulation improves the development of engineered cardiac constructs. Tissue Eng. Part A 20:1654–1667, 2014.

    CAS  PubMed  Google Scholar 

  175. 175.

    Morgan, K. Y., and L. D. Black, III. Creation of a bioreactor for the application of variable amplitude mechanical stimulation of fibrin gel-based engineered cardiac tissue. Methods Mol. Biol. 1181:177–187, 2014.

    PubMed  Google Scholar 

  176. 176.

    Morgan, K. Y., and L. D. Black, III. Investigation into the effects of varying frequency of mechanical stimulation in a cycle-by-cycle manner on engineered cardiac construct function. J. Tissue Eng. Regen. Med. 2014. doi:10.1002/term.1915.

  177. 177.

    Mudera, V., M. Morgan, U. Cheema, S. N. Nazhat, and R. A. Brown. Ultra-rapid engineered collagen constructs tested in an in vivo nursery site. J. Tissue Eng. Regen. Med. 1:192–198, 2007.

    CAS  PubMed  Google Scholar 

  178. 178.

    Nakamuta, J. S., M. E. Danoviz, F. L. N. Marques, L. Dos Santos, C. Becker, G. A. Gonçalves, P. F. Vassallo, I. T. Schettert, P. J. F. Tucci, and J. E. Krieger. Cell therapy attenuates cardiac dysfunction post myocardial infarction: effect of timing, routes of injection and a fibrin scaffold. PLoS ONE 4:e6005, 2009.

    PubMed Central  PubMed  Google Scholar 

  179. 179.

    Napoleone, C. P., G. Oppido, E. Angeli, and G. Gargiulo. Resternotomy in pediatric cardiac surgery: Coseal® initial experience. Interact. Cardiovasc. Thorac. Surg. 6:21–23, 2007.

    Google Scholar 

  180. 180.

    Napoleone, C. P., A. Valori, G. Crupi, S. Ocello, F. Santoro, P. Vouhé, N. Weerasena, and G. Gargiulo. An observational study of coseal® for the prevention of adhesions in pediatric cardiac surgery. Interact. Cardiovasc. Thorac. Surg. 9:978–982, 2009.

    Google Scholar 

  181. 181.

    Neal, R. A., A. Jean, H. Park, P. B. Wu, J. Hsiao, G. C. Engelmayr, Jr., R. Langer, and L. E. Freed. Three-dimensional elastomeric scaffolds designed with cardiac-mimetic structural and mechanical features. Tissue Eng. Part A 19:793–807, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  182. 182.

    Neuenschwander, P. Scaffolds for artificial heart valves and vascular structures, Eidgenössische Technische Hochschule Zürich. 2007.

  183. 183.

    Nevins, M., M. L. Nevins, M. Camelo, J. M. Camelo, P. Schupbach, and D. M. Kim. The clinical efficacy of dynamatrix extracellular membrane in augmenting keratinized tissue. Int. J. Periodontics Restor. Dent. 30:151–161, 2010.

    Google Scholar 

  184. 184.

    Nguyen, L. H., A. K. Kudva, N. L. Guckert, K. D. Linse, and K. Roy. Unique biomaterial compositions direct bone marrow stem cells into specific chondrocytic phenotypes corresponding to the various zones of articular cartilage. Biomaterials 32:1327–1338, 2011.

    CAS  PubMed  Google Scholar 

  185. 185.

    Nishio, S., K. Kosuga, K. Igaki, M. Okada, E. Kyo, T. Tsuji, E. Takeuchi, Y. Inuzuka, S. Takeda, and T. Hata. Long-term (>10 years) clinical outcomes of first-in-human biodegradable poly-l-lactic acid coronary stents Igaki-Tamai stents. Circulation 125:2343–2353, 2012.

    CAS  PubMed  Google Scholar 

  186. 186.

    O’Brien, G., K. Buckley, G. Vanwalleghem, D. Vanrenterghem, H. Dharma, R. L. Winter, and J. Douglass. A multi-centre, prospective, clinical in-market evaluation to assess the performance of opsite™ post-op visible dressings. Int. Wound J. 7:329–337, 2010.

    PubMed  Google Scholar 

  187. 187.

    Omar, A. A., A. I. D. Mavor, A. M. Jones, and S. Homer-Vanniasinkam. Treatment of venous leg ulcers with dermagraft®. Eur. J. Vasc. Endovasc. Surg. 27:666–672, 2004.

    CAS  PubMed  Google Scholar 

  188. 188.

    Ouasti, S., R. Donno, F. Cellesi, M. J. Sherratt, G. Terenghi, and N. Tirelli. Network connectivity, mechanical properties and cell adhesion for hyaluronic acid/PEG hydrogels. Biomaterials 32:6456–6470, 2011.

    CAS  PubMed  Google Scholar 

  189. 189.

    Ozcelik, B., K. D. Brown, A. Blencowe, M. Daniell, G. W. Stevens, and G. G. Qiao. Ultrathin chitosan-poly(ethylene glycol) hydrogel films for corneal tissue engineering. Acta Biomater. 9:6594–6605, 2013.

    CAS  PubMed  Google Scholar 

  190. 190.

    Parenteau-Bareil, R., R. Gauvin, and F. Berthod. Collagen-based biomaterials for tissue engineering applications. Materials 3:1863–1887, 2010.

    CAS  Google Scholar 

  191. 191.

    Park, H., B. L. Larson, M. E. Kolewe, G. Vunjak-Novakovic, and L. E. Freed. Biomimetic scaffold combined with electrical stimulation and growth factor promotes tissue engineered cardiac development. Exp. Cell Res. 321:297–306, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  192. 192.

    Partlow, B. P., C. W. Hanna, J. Rnjak-Kovacina, J. E. Moreau, M. B. Applegate, K. A. Burke, B. Marelli, A. N. Mitropoulos, F. G. Omenetto, and D. L. Kaplan. Highly tunable elastomeric silk biomaterials. Adv. Funct. Mater. 24:4615–4624, 2014.

    CAS  PubMed  Google Scholar 

  193. 193.

    Pellenc, D., H. Berry, and O. Gallet. Adsorption-induced fibronectin aggregation and fibrillogenesis. J. Colloid Interface Sci. 298:132–144, 2006.

    CAS  PubMed  Google Scholar 

  194. 194.

    Pennisi, C. P., C. G. Olesen, M. De Zee, J. Rasmussen, and V. Zachar. Uniaxial cyclic strain drives assembly and differentiation of skeletal myocytes. Tissue Eng. Part A 17:2543–2550, 2011.

    PubMed  Google Scholar 

  195. 195.

    Pocar, M., D. Passolunghi, A. Bregasi, and F. Donatelli. Tachosil® for postinfarction ventricular free wall rupture. Inter. Cardiovasc. Thorac. Surg. 14:866–867, 2012.

  196. 196.

    Pok, S., O. M. Benavides, P. A. Hallal, and J. Jacot. Use of myocardial matrix in a chitosan-based full thickness heart patch. Tissue Eng. 20:1877–1887, 2014.

  197. 197.

    Preda, R. C., G. Leisk, F. Omenetto, and D. L. Kaplan. Bioengineered silk proteins to control cell and tissue functions. Methods Mol. Biol. (Clifton, N.J.) 996:19–41, 2013.

    CAS  Google Scholar 

  198. 198.

    Pryor, II, H. I., E. O’Doherty, A. Hart, G. Owens, D. Hoganson, J. P. Vacanti, P. T. Masiakos, and C. A. Sundback. Poly(glycerol sebacate) films prevent postoperative adhesions and allow laparoscopic placement. Surgery 146:490–497, 2009.

    PubMed  Google Scholar 

  199. 199.

    Purdue, G. F., J. L. Hunt, J. M. Still, Jr., E. J. Law, D. N. Herndon, I. W. Goldfarb, W. R. Schiller, J. F. Hansbrough, W. L. Hickerson, and H. N. Himel. A multicenter clinical trial of a biosynthetic skin replacement, dermagraft-TC, compared with cryopreserved human cadaver skin for temporary coverage of excised burn wounds. J. Burn Care Res. 18:52–57, 1997.

    CAS  Google Scholar 

  200. 200.

    Qi, M., B. L. Strand, Y. Morch, I. Lacik, Y. Wang, P. Salehi, B. Barbaro, A. Gangemi, J. Kuechle, T. Romagnoli, M. A. Hansen, L. A. Rodriguez, E. Benedetti, D. Hunkeler, G. Skjak-Braek, and J. Oberholzer. Encapsulation of human islets in novel inhomogeneous alginate-Ca2+/Ba2+ microbeads: in vitro and in vivo function. Artif. Cells Blood Substit. Biotechnol. 36:403–420, 2008.

    CAS  Google Scholar 

  201. 201.

    Qiao, P., J. Wang, Q. Xie, F. Li, L. Dong, and T. Xu. Injectable calcium phosphate-alginate-chitosan microencapsulated mc3t3-e1 cell paste for bone tissue engineering in vivo. Mater. Sci. Eng. C 33:4633–4639, 2013.

    CAS  Google Scholar 

  202. 202.

    Quintessenza, J. 2011, Bicuspid vascular valve and methods for making and implanting same, Google Patents.

  203. 203.

    Rabotyagova, O. S., P. Cebe, and D. L. Kaplan. Protein-based block copolymers. Biomacromolecules 12:269–289, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  204. 204.

    Radisic, M., and K. L. Christman. Materials science and tissue engineering: repairing the heart. Mayo Clin. Proc. 88:884–898, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  205. 205.

    Rafat, M., F. Li, P. Fagerholm, N. S. Lagali, M. A. Watsky, R. Munger, T. Matsuura, and M. Griffith. PEG-stabilized carbodiimide crosslinked collagen-chitosan hydrogels for corneal tissue engineering. Biomaterials 29:3960–3972, 2008.

    CAS  PubMed  Google Scholar 

  206. 206.

    Rai, R., M. Tallawi, A. Grigore, and A. R. Boccaccini. Synthesis, properties and biomedical applications of poly(glycerol sebacate) (PGS): a review. Prog. Polym. Sci. 37:1051–1078, 2012.

    CAS  Google Scholar 

  207. 207.

    Rajan, N., J. Habermehl, M. F. Coté, C. J. Doillon, and D. Mantovani. Preparation of ready-to-use, storable and reconstituted type I collagen from rat tail tendon for tissue engineering applications. Nat. Protoc. 1:2753–2758, 2007.

    Google Scholar 

  208. 208.

    Redekop, W. K., J. McDonnell, P. Verboom, K. Lovas, and Z. Kalo. The cost effectiveness of apligraf® treatment of diabetic foot ulcers. Pharmacoeconomics 21:1171–1183, 2003.

    PubMed  Google Scholar 

  209. 209.

    Reichl, S., J. Bednarz, and C. C. Muller-Goymann. Human corneal equivalent as cell culture model for in vitro drug permeation studies. Br. J. Ophthalmol. 88:560–565, 2004.

    PubMed Central  CAS  PubMed  Google Scholar 

  210. 210.

    Richter, J. R., R. C. de Guzman, and M. E. Van Dyke. Mechanisms of hepatocyte attachment to keratin biomaterials. Biomaterials 32:7555–7561, 2011.

    CAS  PubMed  Google Scholar 

  211. 211.

    Rnjak-Kovacina, J., L. S. Wray, J. M. Golinski, and D. L. Kaplan. Arrayed hollow channels in silk-based scaffolds provide functional outcomes for engineering critically sized tissue constructs. Adv. Funct. Mater. 24:2188–2196, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  212. 212.

    Rockwood, D. N., R. C. Preda, T. Yucel, X. Wang, M. L. Lovett, and D. L. Kaplan. Materials fabrication from Bombyx mori silk fibroin. Nat. Protoc. 6:1612–1631, 2011.

    CAS  PubMed  Google Scholar 

  213. 213.

    Rouse, J. G., and M. E. Van Dyke. A review of keratin-based biomaterials for biomedical applications. Materials 3:999–1014, 2010.

    Google Scholar 

  214. 214.

    Ruberti, J. W., A. S. Roy, and C. J. Roberts. Corneal biomechanics and biomaterials. Annu. Rev. Biomed. Eng. 13:269–295, 2011.

    CAS  PubMed  Google Scholar 

  215. 215.

    Saffer, E. M., G. N. Tew, and S. R. Bhatia. Poly(lactic acid)-poly(ethylene oxide) block copolymers: new directions in self-assembly and biomedical applications. Curr. Med. Chem. 18:5676–5686, 2011.

    CAS  PubMed  Google Scholar 

  216. 216.

    Sajesh, K. M., R. Jayakumar, S. V. Nair, and K. P. Chennazhi. Biocompatible conducting chitosan/polypyrrole–alginate composite scaffold for bone tissue engineering. Int. J. Biol. Macromol. 62:465–471, 2013.

    CAS  PubMed  Google Scholar 

  217. 217.

    Samal, S. K., M. Dash, S. Van Vlierberghe, D. L. Kaplan, E. Chiellini, C. van Blitterswijk, L. Moroni, and P. Dubruel. Cationic polymers and their therapeutic potential. Chem. Soc. Rev. 41:7147–7194, 2012.

    CAS  PubMed  Google Scholar 

  218. 218.

    Sambasivan, R., R. Yao, A. Kissenpfennig, L. Van Wittenberghe, A. Paldi, B. Gayraud-Morel, H. Guenou, B. Malissen, S. Tajbakhsh, and A. Galy. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 138:3647–3656, 2011.

    CAS  PubMed  Google Scholar 

  219. 219.

    Santerre, J. P., K. Woodhouse, G. Laroche, and R. S. Labow. Understanding the biodegradation of polyurethanes: from classical implants to tissue engineering materials. Biomaterials 26:7457–7470, 2005.

    CAS  PubMed  Google Scholar 

  220. 220.

    Santos, M. I., and R. L. Reis. Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges. Macromol. Biosci. 10:12–27, 2010.

    CAS  PubMed  Google Scholar 

  221. 221.

    Sasson, L., S. Houri, A. Raucher Sternfeld, I. Cohen, O. Lenczner, E. L. Bove, L. Kapusta, and A. Tamir. Right ventricular outflow tract strategies for repair of tetralogy of fallot: effect of monocusp valve reconstruction. Eur. J. Cardiothorac. Surg. 43:743–751, 2013.

    PubMed  Google Scholar 

  222. 222.

    Schaaf, S., A. Shibamiya, M. Mewe, A. Eder, A. Stoehr, M. N. Hirt, T. Rau, W.-H. Zimmermann, L. Conradi, T. Eschenhagen, and A. Hansen. Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. Plos One 6:e26397, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  223. 223.

    Schneider, S., P. J. Feilen, F. Brunnenmeier, T. Minnemann, H. Zimmermann, U. Zimmermann, and M. M. Weber. Long-term graft function of adult rat and human islets encapsulated in novel alginate-based microcapsules after transplantation in immunocompetent diabetic mice. Diabetes 54:687–693, 2005.

    CAS  PubMed  Google Scholar 

  224. 224.

    Schonfeld, W. H., K. F. Villa, J. M. Fastenau, P. D. Mazonson, and V. Falanga. An economic assessment of apligraf®(graftskin) for the treatment of hard-to-heal venous leg ulcers. Wound Repair Regen. 8:251–257, 2000.

    CAS  PubMed  Google Scholar 

  225. 225.

    Seif-Naraghi, S. B., and K. L. Christman. Tissue engineering and the role of biomaterial scaffolds: the evolution of cardiac tissue engineering. In: Resident Stem Cells and Regenerative Therapy, edited by R. C. S. Goldenberg and A. C. C. de Carvalho. Elsevier, 2013, pp. 43–67. http://www.sciencedirect.com/science/book/9780124160125.

  226. 226.

    Seif-Naraghi, S. B., J. M. Singelyn, M. A. Salvatore, K. G. Osborn, J. J. Wang, U. Sampat, O. L. Kwan, G. M. Strachan, J. Wong, P. J. Schup-Magoffin, R. L. Braden, K. Bartels, J. A. DeQuach, M. Preul, A. M. Kinsey, A. N. DeMaria, N. Dib, and K. L. Christman. Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci. Transl. Med. 5:10, 2013.

    PubMed Central  Google Scholar 

  227. 227.

    Shachar, M., O. Tsur-Gang, T. Dvir, J. Leor, and S. Cohen. The effect of immobilized RGD peptide in alginate scaffolds on cardiac tissue engineering. Acta Biomater. 7:152–162, 2011.

    CAS  PubMed  Google Scholar 

  228. 228.

    Shafei, S., M. A. Sharifudin, M. S. Ismail, S. Ab Rahman, and A. N. Sadagatullah. A comparative study of Tualang honey spray versus film spray (opsite®) as post-long bone fracture fixation wound dressing. In: Kelantan Research Day 2013. Rural Transformation Centre (RTC), Terminal Agribisnes Negara (TEMAN), Kota Bharu. 2013. http://irep.iium.edu.my/32605/.

  229. 229.

    Shang, K., J. Rnjak-Kovacina, Y. Lin, R. Hayden, H. Tao, and D. Kaplan. Accelerated in vitro degradation of optically clear low beta-sheet silk films by enzyme mediated pretreatment. Trans. Vis. Sci. Technol. 2:2, 2013.

    Google Scholar 

  230. 230.

    Shapiro, A. M. J., C. Ricordi, B. J. Hering, H. Auchincloss, R. Lindblad, P. Robertson, A. Secchi, M. D. Brendel, T. Berney, D. C. Brennan, E. Cagliero, R. Alejandro, E. A. Ryan, B. DiMercurio, P. Morel, K. S. Polonsky, J. A. Reems, R. G. Bretzel, F. Bertuzzi, T. Froud, R. Kandaswamy, D. E. R. Sutherland, G. Eisenbarth, M. Segal, J. Preiksaitis, G. S. Korbutt, F. B. Barton, L. Viviano, V. Seyfert-Margolis, J. Bluestone, and J. R. T. Lakey. International trial of the Edmonton protocol for islet transplantation. N. Engl. J. Med. 355:1318–1330, 2006.

    CAS  PubMed  Google Scholar 

  231. 231.

    Sharifpoor, S., C. A. Simmons, R. S. Labow, and J. P. Santerre. A study of vascular smooth muscle cell function under cyclic mechanical loading in a polyurethane scaffold with optimized porosity. Acta Biomater. 6:4218–4228, 2010.

    CAS  PubMed  Google Scholar 

  232. 232.

    Sharifpoor, S., C. A. Simmons, R. S. Labow, and J. P. Santerre. Functional characterization of human coronary artery smooth muscle cells under cyclic mechanical strain in a degradable polyurethane scaffold. Biomaterials 32:4816–4829, 2011.

    CAS  PubMed  Google Scholar 

  233. 233.

    Shen, W., X. Chen, Y. Hu, Z. Yin, T. Zhu, J. Hu, J. Chen, Z. Zheng, W. Zhang, J. Ran, B. C. Heng, J. Ji, W. Chen, and H. W. Ouyang. Long-term effects of knitted silk-collagen sponge scaffold on anterior cruciate ligament reconstruction and osteoarthritis prevention. Biomaterials 35:8154–8163, 2014.

    CAS  PubMed  Google Scholar 

  234. 234.

    Shields, L. B. E., G. H. Raque, S. D. Glassman, M. Campbell, T. Vitaz, J. Harpring, and C. B. Shields. Adverse effects associated with high-dose recombinant human bone morphogenetic protein-2 use in anterior cervical spine fusion. Spine 31:542–547, 2006. doi:10.1097/01.brs.0000201424.27509.72.

    PubMed  Google Scholar 

  235. 235.

    Shimizu, T., M. Yamato, A. Kikuchi, and T. Okano. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials 24:2309–2316, 2003.

    CAS  PubMed  Google Scholar 

  236. 236.

    Shin, S. R., S. M. Jung, M. Zalabany, K. Kim, P. Zorlutuna, Sb Kim, M. Nikkhah, M. Khabiry, M. Azize, J. Kong, K-t Wan, T. Palacios, M. R. Dokmeci, H. Bae, X. Tang, and A. Khademhosseini. Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano 7:2369–2380, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  237. 237.

    Sicchieri, L. G., G. E. Crippa, P. T. de Oliveira, M. M. Beloti, and A. L. Rosa. Pore size regulates cell and tissue interactions with PLGA-cap scaffolds used for bone engineering. J. Tissue Eng. Regen. Med. 6:155–162, 2012.

    CAS  PubMed  Google Scholar 

  238. 238.

    Sierpinski, P., J. Garrett, J. Ma, P. Apel, D. Klorig, T. Smith, L. A. Koman, A. Atala, and M. Van Dyke. The use of keratin biomaterials derived from human hair for the promotion of rapid regeneration of peripheral nerves. Biomaterials 29:118–128, 2008.

    CAS  PubMed  Google Scholar 

  239. 239.

    Silva, A. K. A., M. Juenet, A. Meddahi-Pellé, and D. Letourneur. Polysaccharide-based strategies for heart tissue engineering. Carbohydr. Polym. 116:267–277, 2014.

  240. 240.

    Siti-Ismail, N., A. E. Bishop, J. M. Polak, and A. Mantalaris. The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance. Biomaterials 29:3946–3952, 2008.

    CAS  PubMed  Google Scholar 

  241. 241.

    Skulstad, H., G. Erikssen, M. E. Estensen, and H. L. Lindberg. Insufficient long term follow up and risk for aneurism in patients operated with dacron patch for coarctatio aortae. Eur. Heart J. 34:P2117, 2013.

    Google Scholar 

  242. 242.

    Sosa, H., D. Popp, G. Ouyang, and H. E. Huxley. Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys. J . 67:283–292, 1994.

    PubMed Central  CAS  PubMed  Google Scholar 

  243. 243.

    Sowjanya, J. A., J. Singh, T. Mohita, S. Sarvanan, A. Moorthi, N. Srinivasan, and N. Selvamurugan. Biocomposite scaffolds containing chitosan/alginate/nano-silica for bone tissue engineering. Colloids Surf. B 109:294–300, 2013.

    CAS  Google Scholar 

  244. 244.

    Spotnitz, W. D. Fibrin sealant: past, present, and future: a brief review. World J. Surg. 34:632–634, 2010.

    PubMed  Google Scholar 

  245. 245.

    Stavarachi, M., P. Apostol, M. Toma, D. Cimponeriu, and L. Gavrila. Spinal muscular atrophy disease: a literature review for therapeutic strategies. J. Med. Life 3:3, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  246. 246.

    Steinberg, J. S., M. Edmonds, D. P. Hurley, Jr., and W. N. King. Confirmatory data from eu study supports apligraf for the treatment of neuropathic diabetic foot ulcers. J. Am. Podiatr. Med. Assoc. 100:73–77, 2010.

    PubMed  Google Scholar 

  247. 247.

    Stoppel, W. L., J. C. White, S. D. Horava, S. R. Bhatia, and S. C. Roberts. Transport of biological molecules in surfactant-alginate composite hydrogels. Acta Biomater. 7:3988–3998, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  248. 248.

    Stoppel, W. L., J. C. White, S. D. Horava, A. C. Henry, S. C. Roberts, and S. R. Bhatia. Terminal sterilization of alginate hydrogels: efficacy and impact on mechanical properties. J. Biomed. Mater. Res. Part B 102:877–884, 2013.

  249. 249.

    Streit, M., and L. R. Braathen. Apligraf–a living human skin equivalent for the treatment of chronic wounds. Int. J. Artif. Organs 23:831–833, 2000.

    CAS  PubMed  Google Scholar 

  250. 250.

    Takata, I., T. Tosa, and I. Chibata. Screening of matrix suitable for immobilization of microbial cells. J. Solid-Phase Biochem. 2:225–236, 1977.

    CAS  Google Scholar 

  251. 251.

    Tan, C., M. Utley, C. Paschalides, J. Pilling, J. D. Robb, K. M. Harrison-Phipps, L. Lang-Lazdunski, and T. Treasure. A prospective randomized controlled study to assess the effectiveness of coseal® to seal air leaks in lung surgery. Eur. J. Cardiothorac. Surg. 40:304–308, 2011.

    PubMed  Google Scholar 

  252. 252.

    Tan, P. L. J. Company profile: tissue regeneration for diabetes and neurological diseases at living cell technologies. Regen. Med. 5:181–187, 2010.

    PubMed  Google Scholar 

  253. 253.

    Taylor, M. S., A. U. Daniels, K. P. Andriano, and J. Heller. Six bioabsorbable polymers: in vitro acute toxicity of accumulated degradation products. J. Appl. Biomater. 5:151–157, 1994.

    CAS  PubMed  Google Scholar 

  254. 254.

    Themistocleous, G. S., H. A. Katopodis, L. Khaldi, A. Papalois, C. Doillon, A. Sourla, P. N. Soucacos, and M. Koutsilieris. Implants of type I collagen gel containing mg-63 osteoblast-like cells can act as stable scaffolds stimulating the bone healing process at the sites of the surgically-produced segmental diaphyseal defects in male rabbits. In Vivo 21:69–76, 2007.

    CAS  PubMed  Google Scholar 

  255. 255.

    Tonami, K., S. Hata, K. Ojima, Y. Ono, Y. Kurihara, T. Amano, T. Sato, Y. Kawamura, H. Kurihara, and H. Sorimachi. Calpain-6 deficiency promotes skeletal muscle development and regeneration. PLoS Genet. 9:e1003668, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  256. 256.

    Trent, J. F., and R. S. Kirsner. Tissue engineered skin: apligraf, a bi-layered living skin equivalent. Int. J. Clin. Pract. 52:408–413, 1998.

    CAS  PubMed  Google Scholar 

  257. 257.

    Troncoso, R., C. Ibarra, J. M. Vicencio, E. Jaimovich, and S. Lavandero. New insights into IGF-1 signaling in the heart. Trends Endocrinol. Metab. 25:128–137, 2014.

    CAS  PubMed  Google Scholar 

  258. 258.

    Turner, N. J., T. J. Keane, and S. F. Badylak. Lessons from developmental biology for regenerative medicine. Birth Defects Res. Part C 99:149–159, 2013.

    CAS  Google Scholar 

  259. 259.

    Turrentine, M. W., R. P. McCarthy, P. Vijay, K. W. McConnell, and J. W. Brown. PTFE monocusp valve reconstruction of the right ventricular outflow tract. Ann. Thorac. Surg. 73:871–880, 2002.

    PubMed  Google Scholar 

  260. 260.

    Twardowski, R., and L. D. Black, III. Cardiac fibroblasts support endothelial cell proliferation and sprout formation but not the development of multicellular sprouts in a fibrin gel co-culture model. Ann. Biomed. Eng. 42:1074–1084, 2014.

  261. 261.

    Uebersax, L., T. Apfel, K. M. R. Nuss, R. Vogt, H. Y. Kim, L. Meinel, D. L. Kaplan, J. A. Auer, H. P. Merkle, and B. von Rechenberg. Biocompatibility and osteoconduction of macroporous silk fibroin implants in cortical defects in sheep. Eur. J. Pharm. Biopharm. 85:107–118, 2013.

    CAS  PubMed  Google Scholar 

  262. 262.

    Ungerleider, J. L., and K. L. Christman. Concise review: Injectable biomaterials for the treatment of myocardial infarction and peripheral artery disease: translational challenges and progress. Stem Cells Transl. Med. 3:1090–1099, 2014.

  263. 263.

    Van Goethem, F., E. Adriaens, N. Alepee, F. Straube, B. De Wever, M. Cappadoro, S. Catoire, E. Hansen, A. Wolf, and P. Vanparys. Prevalidation of a new in vitro reconstituted human cornea model to assess the eye irritating potential of chemicals. Toxicol. In Vitro 20:1–17, 2006.

    PubMed  Google Scholar 

  264. 264.

    Venkatesan, J., I. Bhatnagar, and S.-K. Kim. Chitosan-alginate biocomposite containing fucoidan for bone tissue engineering. Mar. Drugs 12:300–316, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  265. 265.

    Venkatesan, J., I. Bhatnagar, P. Manivasagan, K.-H. Kang, and S.-K. Kim. Alginate composites for bone tissue engineering: a review. Int. J. Biol. Macromol. 72C:269–281, 2014.

  266. 266.

    von Maltzahn, J., A. E. Jones, R. J. Parks, and M. A. Rudnicki. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc. Natl. Acad. Sci. USA 110:16474–16479, 2013.

    Google Scholar 

  267. 267.

    Vorndran, C. Recent us patents on extracellular matrix in tissue engineering and regenerative medicine. Recent Patents Regen. Med. 4:34–39, 2014.

    CAS  Google Scholar 

  268. 268.

    Vowden, K., J. McGowan, M. Pilcher, A. D’Arcy, C. Renton, V. Warner, J. Megson, and P. Vowden. Experience with the use of an amelogenin-based extracellular matrix substitute (xelma®) in the management of a variety of complex hard-to-heal chronic wounds. In: European Wound Management Association Conference Abstracts, May 2007, Glasgow, Scotland. Oral presentation #91.

  269. 269.

    Vowden, P., M. Romanelli, R. Peter, Å. Boström, A. Josefsson, and H. Stege. The effect of amelogenins (xelma™) on hard-to-heal venous leg ulcers. Wound Repair Regen. 14:240–246, 2006.

    PubMed  Google Scholar 

  270. 270.

    Wang, X., W. Wang, J. Ma, X. Guo, X. Yu, and X. Ma. Proliferation and differentiation of mouse embryonic stem cells in apa microcapsule: a model for studying the interaction between stem cells and their niche. Biotechnol. Prog. 22:791–800, 2006.

    CAS  PubMed  Google Scholar 

  271. 271.

    Wang, Y., Y. M. Kim, and R. Langer. In vivo degradation characteristics of poly(glycerol sebacate). J. Biomed. Mater. Res. Part A 66A:192–197, 2003.

    CAS  Google Scholar 

  272. 272.

    Wang, Z., Y. Cui, J. Wang, X. Yang, Y. Wu, K. Wang, X. Gao, D. Li, Y. Li, X.-L. Zheng, Y. Zhu, D. Kong, and Q. Zhao. The effect of thick fibers and large pores of electrospun poly(ε-caprolactone) vascular grafts on macrophage polarization and arterial regeneration. Biomaterials 35:5700–5710, 2014.

    CAS  PubMed  Google Scholar 

  273. 273.

    Waterhouse, A., S. G. Wise, M. K. C. Ng, and A. S. Weiss. Elastin as a nonthrombogenic biomaterial. Tissue Eng. Part B 17:93–99, 2011.

    CAS  Google Scholar 

  274. 274.

    Weber, R. A., W. C. Breidenbach, R. E. Brown, M. E. Jabaley, and D. P. Mass. A randomized prospective study of polyglycolic acid conduits for digital nerve reconstruction in humans. Plast. Reconstr. Surg. 106:1036–1045, 2000.

    CAS  PubMed  Google Scholar 

  275. 275.

    White, E. S., and A. F. Muro. Fibronectin splice variants: understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life 63:538–546, 2011.

    CAS  PubMed  Google Scholar 

  276. 276.

    Williams, C., K. P. Quinn, I. Georgakoudi, and L. D. Black III. Young developmental age cardiac extracellular matrix promotes the expansion of neonatal cardiomyocytes in vitro. Acta Biomater. 10:194–204, 2014.

    CAS  PubMed  Google Scholar 

  277. 277.

    Wilson, S. L., I. Wimpenny, M. Ahearne, S. Rauz, A. J. El Haj, and Y. Yang. Chemical and topographical effects on cell differentiation and matrix elasticity in a corneal stromal layer model. Adv. Funct. Mater. 22:3641–3649, 2012.

    CAS  Google Scholar 

  278. 278.

    Wise, A. K., J. B. Fallon, A. J. Neil, L. N. Pettingill, M. S. Geaney, S. J. Skinner, and R. K. Shepherd. Combining cell-based therapies and neural prostheses to promote neural survival. Neurotherapeutics 8:774–787, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  279. 279.

    Wolf, M. T., C. L. Dearth, S. B. Sonnenberg, E. G. Loboa, and S. F. Badylak. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv. Drug Deliv. Rev. 2014. doi:10.1016/j.addr.2014.08.011.

  280. 280.

    Wray, L. S., J. Rnjak-Kovacina, B. B. Mandal, D. F. Schmidt, E. S. Gil, and D. L. Kaplan. A silk-based scaffold platform with tunable architecture for engineering critically-sized tissue constructs. Biomaterials 33:9214–9224, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  281. 281.

    Wu, H., W. C. Xiong, and L. Mei. To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137:1017–1033, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  282. 282.

    Xin, M., E. N. Olson, and R. Bassel-Duby. Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair. Nat. Rev. Mol. Cell Biol. 14:529–541, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  283. 283.

    Xu, Z. C., W. J. Zhang, H. Li, L. Cui, L. Cen, G. D. Zhou, W. Liu, and Y. Cao. Engineering of an elastic large muscular vessel wall with pulsatile stimulation in bioreactor. Biomaterials 29:1464–1472, 2008.

    CAS  PubMed  Google Scholar 

  284. 284.

    Yamato, M., and T. Okano. Cell sheet engineering. Mater. Today 7:42–47, 2004.

    CAS  Google Scholar 

  285. 285.

    Ye, K. Y., K. E. Sullivan, and L. D. Black, III. Encapsulation of cardiomyocytes in a fibrin hydrogel for cardiac tissue engineering. J. Vis. Exp. 2011. doi:10.3791/3251.

  286. 286.

    Yin, H., C. Gong, S. Shi, X. Liu, Y. Wei, and Z. Qian. Toxicity evaluation of biodegradable and thermosensitive PEG-PCL-PEG hydrogel as a potential in situ sustained ophthalmic drug delivery system. J. Biomed. Mater. Res. B 92B:129–137, 2010.

    CAS  Google Scholar 

  287. 287.

    Yu, C.-C., J.-J. Chang, Y.-H. Lee, Y.-C. Lin, M.-H. Wu, M.-C. Yang, and C.-T. Chien. Electrospun scaffolds composing of alginate, chitosan, collagen and hydroxyapatite for applying in bone tissue engineering. Mater. Lett. 93:133–136, 2013.

    CAS  Google Scholar 

  288. 288.

    Yuvarani, I., S. S. Kumar, J. Venkatesan, S.-K. Kim, and P. N. Sudha. Preparation and characterization of curcumin coated chitosan-alginate blend for wound dressing application. J. Biomater. Tissue Eng. 2:54–60, 2012.

    CAS  Google Scholar 

  289. 289.

    Zaky, S. H., K.-W. Lee, J. Gao, A. Jensen, J. Close, Y. Wang, A. J. Almarza, and C. Sfeir. Poly (glycerol sebacate) elastomer: a novel material for mechanically loaded bone regeneration. Tissue Eng. Part A 20:45–53, 2013.

    PubMed  Google Scholar 

  290. 290.

    Zammit, P. S., F. Relaix, Y. Nagata, A. P. Ruiz, C. A. Collins, T. A. Partridge, and J. R. Beauchamp. Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119:1824–1832, 2006.

    CAS  PubMed  Google Scholar 

  291. 291.

    Zaulyanov, L., and R. S. Kirsner. A review of a bi-layered living cell treatment (apligraf®) in the treatment of venous leg ulcers and diabetic foot ulcers. Clin. Interv. Aging 2:93, 2007.

    PubMed Central  PubMed  Google Scholar 

  292. 292.

    Zhang, D., I. Y. Shadrin, J. Lam, H.-Q. Xian, H. R. Snodgrass, and N. Bursac. Tissue-engineered cardiac patch for advanced functional maturation of human esc-derived cardiomyocytes. Biomaterials 34:5813–5820, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  293. 293.

    Zhang, X., L. Zhu, H. Lv, Y. Cao, Y. Liu, Y. Xu, W. Ye, and J. Wang. Repair of rabbit femoral condyle bone defects with injectable nanohydroxyapatite/chitosan composites. J. Mater. Sci. Mater. Med. 23:1941–1949, 2012.

    CAS  PubMed  Google Scholar 

  294. 294.

    Zhou, J., J. Chen, H. Sun, X. Qiu, Y. Mou, Z. Liu, Y. Zhao, X. Li, Y. Han, C. Duan, R. Tang, C. Wang, W. Zhong, J. Liu, Y. Luo, M. M. Xing, and C. Wang. Engineering the heart: Evaluation of conductive nanomaterials for improving implant integration and cardiac function. Sci. Rep. 4:1–11, 2014.

  295. 295.

    Zimmermann, H., S. Shirley, and U. Zimmermann. Alginate-based encapsulation of cells: past, present, and future. Curr. Diab.Rep. 7:314–320, 2007.

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the NIH for support (P41 EB002520, R01 EB011620, R01 EY020856, R01 DE017207). W.L.S acknowledges funding from the Tufts University Training in Education and Critical Research Skills NIH IRACDA program (K12 GM074869).

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Correspondence to David L. Kaplan.

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Associate Editor Fei Wang oversaw the review of this article.

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Stoppel, W.L., Ghezzi, C.E., McNamara, S.L. et al. Clinical Applications of Naturally Derived Biopolymer-Based Scaffolds for Regenerative Medicine. Ann Biomed Eng 43, 657–680 (2015). https://doi.org/10.1007/s10439-014-1206-2

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Keywords

  • Biopolymers
  • Scaffolds
  • Regenerative medicine