Top

Journal of Cardiovascular Translational Research

Published in:

01-04-2017 | Original Article

Translational Challenges in Cardiovascular Tissue Engineering

Authors: Maximilian Y. Emmert, Emanuela S. Fioretta, Simon P. Hoerstrup

Published in: Journal of Cardiovascular Translational Research | Issue 2/2017

Abstract

Valvular heart disease and congenital heart defects represent a major cause of death around the globe. Although current therapy strategies have rapidly evolved over the decades and are nowadays safe, effective, and applicable to many affected patients, the currently used artificial prostheses are still suboptimal. They do not promote regeneration, physiological remodeling, or growth (particularly important aspects for children) as their native counterparts. This results in the continuous degeneration and subsequent failure of these prostheses which is often associated with an increased morbidity and mortality as well as the need for multiple re-interventions. To overcome this problem, the concept of tissue engineering (TE) has been repeatedly suggested as a potential technology to enable native-like cardiovascular replacements with regenerative and growth capacities, suitable for young adults and children. However, despite promising data from pre-clinical and first clinical pilot trials, the translation and clinical relevance of such TE technologies is still very limited. The reasons that currently limit broad clinical adoption are multifaceted and comprise of scientific, clinical, logistical, technical, and regulatory challenges which need to be overcome. The aim of this review is to provide an overview about the translational problems and challenges in current TE approaches. It further suggests directions and potential solutions on how these issues may be efficiently addressed in the future to accelerate clinical translation. In addition, a particular focus is put on the current regulatory guidelines and the associated challenges for these promising TE technologies.

Marelli, A. J., Mackie, A. S., Ionescu-Ittu, R., Rahme, E., & Pilote, L. (2007). Congenital heart disease in the general population: changing prevalence and age distribution. Circulation, 115(2), 163–172. doi:10.1161/CIRCULATIONAHA.106.627224.CrossRefPubMed

Nkomo, V. T., Gardin, J. M., Skelton, T. N., Gottdiener, J. S., Scott, C. G., & Enriquez-Sarano, M. Burden of valvular heart diseases: a population-based study. The Lancet, 368(9540), 1005–1011. doi:10.1016/S0140-6736(06)69208-8.

Supino, P. G., Borer, J. S., Preibisz, J., & Bornstein, A. (2006). The epidemiology of valvular heart disease: a growing public health problem. Heart Failure Clinics, 2(4), 379–393. doi:10.1016/j.hfc.2006.09.010.CrossRefPubMed

Cribier, A., Eltchaninoff, H., Bash, A., Borenstein, N., Tron, C., Bauer, F., et al. (2002). Percutaneous transcatheter implantation of an aortic valve prosthesis for calcific aortic stenosis: first human case description. Circulation, 106(24), 3006–3008.CrossRefPubMed

Fioretta, E. S., Dijkman, P. E., Emmert, M. Y., & Hoerstrup, S. P. (2016). The future of heart valve replacement: recent developments and translational challenges for heart valve tissue engineering. Journal of Tissue Engineering and Regenerative Medicine. doi:10.1002/term.2326.PubMed

Schoen, F. J., & Gotlieb, A. I. (2016). Heart valve health, disease, replacement, and repair: a 25-year cardiovascular pathology perspective. Cardiovascular Pathology, 25(4), 341–352. doi:10.1016/j.carpath.2016.05.002.CrossRefPubMed

Alexi-Meskishvilia, V., Ovroutskib, S., Ewertb, P., DaÈhnertb, I., Bergerb, F., Langeb, P. E., et al. (2000). Optimal conduit size for extracardiac Fontan operation. European Journal of Cardio-Thoracic Surgery, 18(690–695).

Yacoub, M. H., & Takkenberg, J. J. (2005). Will heart valve tissue engineering change the world? Nature Clinical Practice. Cardiovascular Medicine, 2(2), 60–61. doi:10.1038/ncpcardio0112.CrossRefPubMed

Mendelson, K., & Schoen, F. J. (2006). Heart valve tissue engineering: concepts, approaches, progress, and challenges. Annals of Biomedical Engineering, 34(12), 1799–1819. doi:10.1007/s10439-006-9163-z.CrossRefPubMedPubMedCentral

10.

Langer, R., & Vacanti, J. P. (1993). Tissue engineering. Science, 260(5110), 920–926.CrossRefPubMed

11.

Dohmen, P. M., Lembcke, A., Hotz, H., Kivelitz, D., & Konertz, W. F. (2002). Ross operation with a tissue-engineered heart valve. The Annals of Thoracic Surgery, 74(5), 1438–1442.CrossRefPubMed

12.

Dohmen, P. M., Lembcke, A., Holinski, S., Pruss, A., & Konertz, W. (2011). Ten years of clinical results with a tissue-engineered pulmonary valve. The Annals of Thoracic Surgery, 92(4), 1308–1314. doi:10.1016/j.athoracsur.2011.06.009.CrossRefPubMed

13.

Cebotari, S., Lichtenberg, A., Tudorache, I., Hilfiker, A., Mertsching, H., Leyh, R., et al. (2006). Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation, 114(1 Suppl), I132–I137. doi:10.1161/CIRCULATIONAHA.105.001065.PubMed

14.

Dohmen, P. M., Lembcke, A., Holinski, S., Kivelitz, D., Braun, J. P., Pruss, A., et al. (2007). Mid-term clinical results using a tissue-engineered pulmonary valve to reconstruct the right ventricular outflow tract during the Ross procedure. The Annals of Thoracic Surgery, 84(3), 729–736. doi:10.1016/j.athoracsur.2007.04.072.CrossRefPubMed

15.

Naito, Y., Imai, Y., Shin’oka, T., Kashiwagi, J., Aoki, M., Watanabe, M., et al. (2003). Successful clinical application of tissue-engineered graft for extracardiac Fontan operation. The Journal of Thoracic and Cardiovascular Surgery, 125(2), 419–420. doi:10.1067/mtc.2003.134.CrossRefPubMed

16.

Shinoka, T., & Breuer, C. (2008). Tissue-engineered blood vessels in pediatric cardiac surgery. Yale Journal of Biology and Medicine, 81, 161–166.PubMedPubMedCentral

17.

Bouten, C. V., Dankers, P. Y., Driessen-Mol, A., Pedron, S., Brizard, A. M., & Baaijens, F. P. (2011). Substrates for cardiovascular tissue engineering. Advanced Drug Delivery Reviews, 63(4–5), 221–241. doi:10.1016/j.addr.2011.01.007.CrossRefPubMed

18.

Fioretta, E. S., Fledderus, J. O., Burakowska-Meise, E. A., Baaijens, F. P., Verhaar, M. C., & Bouten, C. V. (2012). Polymer-based scaffold designs for in situ vascular tissue engineering: controlling recruitment and differentiation behavior of endothelial colony forming cells. Macromolecular Bioscience, 12(5), 577–590. doi:10.1002/mabi.201100315.CrossRefPubMed

19.

Dijkman, P. E., Fioretta, E. S., Frese, L., Pasqualini, F. S., & Hoerstrup, S. P. (2016). Heart valve replacements with regenerative capacity. Transfusion Medicine and Hemotherapy, 43(4), 282–290. doi:10.1159/000448181.CrossRefPubMedPubMedCentral

20.

Cheung, D. Y., Duan, B., & Butcher, J. T. (2015). Current progress in tissue engineering of heart valves: multiscale problems, multiscale solutions. Expert opinion on biological therapy. [early online].

21.

Jana, S., Tefft, B. J., Spoon, D. B., & Simari, R. D. (2014). Scaffolds for tissue engineering of cardiac valves. Acta Biomaterialia, 10(7), 2877–2893. doi:10.1016/j.actbio.2014.03.014.CrossRefPubMed

22.

Kurobe, H., Maxfield, M. W., Breuer, C. K., & Shinoka, T. (2012). Concise review: tissue-engineered vascular grafts for cardiac surgery: past, present, and future. Stem Cells Transl Med, 1(7), 566–571. doi:10.5966/sctm.2012-0044.CrossRefPubMedPubMedCentral

23.

Patterson, J. T., Gilliland, T., Maxfield, M. W., Church, S., Naito, Y., Shinoka, T., et al. (2012). Tissue-engineered vascular grafts for use in the treatment of congenital heart disease: from the bench to the clinic and back again. Regenerative Medicine, 7(3), 409–419. doi:10.2217/rme.12.12.CrossRefPubMedPubMedCentral

24.

Fioretta, E. S., Fledderus, J. O., Baaijens, F. P., & Bouten, C. V. (2012). Influence of substrate stiffness on circulating progenitor cell fate. Journal of Biomechanics, 45(5), 736–744. doi:10.1016/j.jbiomech.2011.11.013.CrossRefPubMed

25.

Tudorache, I., Horke, A., Cebotari, S., Sarikouch, S., Boethig, D., Breymann, T., et al. (2016). Decellularized aortic homografts for aortic valve and aorta ascendens replacement. European Journal of Cardio-Thoracic Surgery, 50(1), 89–97. doi:10.1093/ejcts/ezw013.CrossRefPubMedPubMedCentral

26.

Sarikouch, S., Horke, A., Tudorache, I., Beerbaum, P., Westhoff-Bleck, M., Boethig, D., et al. (2016). Decellularized fresh homografts for pulmonary valve replacement: a decade of clinical experience. European Journal of Cardio-Thoracic Surgery. doi:10.1093/ejcts/ezw050.

27.

Neumann, A., Cebotari, S., Tudorache, I., Haverich, A., & Sarikouch, S. (2013). Heart valve engineering: decellularized allograft matrices in clinical practice. Biomed Tech (Berl), 58(5), 453–456. doi:10.1515/bmt-2012-0115.CrossRef

28.

Cebotari, S., Tudorache, I., Ciubotaru, A., Boethig, D., Sarikouch, S., Goerler, A., et al. (2011). Use of fresh decellularized allografts for pulmonary valve replacement may reduce the reoperation rate in children and young adults: early report. Circulation, 124(11 Suppl), S115–S123. doi:10.1161/CIRCULATIONAHA.110.012161.CrossRefPubMed

29.

da Costa, F. D. A., Costa, A. C. B. A., Prestes, R., Domanski, A. C., Balbi, E. M., Ferreira, A. D. A., et al. (2010). The early and midterm function of decellularized aortic valve allografts. The Annals of Thoracic Surgery, 90(6), 1854–1860. doi:10.1016/j.athoracsur.2010.08.022.CrossRefPubMed

30.

Hoerstrup, S. P., Sodian, R., Daebritz, S., Wang, J., Bacha, E. A., Martin, D. P., et al. (2000). Functional living trileaflet heart valves grown in vitro. Circulation, 102(19 Suppl 3), III44–III49.PubMed

31.

Hoerstrup, S. P., Cummings Mrcs, I., Lachat, M., Schoen, F. J., Jenni, R., Leschka, S., et al. (2006). Functional growth in tissue-engineered living, vascular grafts: follow-up at 100 weeks in a large animal model. Circulation, 114(1 Suppl), I159–I166. doi:10.1161/CIRCULATIONAHA.105.001172.PubMed

32.

Shinoka, T., Ma, P. X., Shum-Tim, D., Breuer, C. K., Cusick, R. A., Zund, G., et al. (1996). Tissue-engineered heart valves. Autologous valve leaflet replacement study in a lamb model. Circulation, 94(9), II164–II168.PubMed

33.

Weber, B., Scherman, J., Emmert, M. Y., Gruenenfelder, J., Verbeek, R., Bracher, M., et al. (2011). Injectable living marrow stromal cell-based autologous tissue engineered heart valves: first experiences with a one-step intervention in primates. European Heart Journal, 32(22), 2830–2840. doi:10.1093/eurheartj/ehr059.CrossRefPubMed

34.

Driessen-Mol, A., Emmert, M. Y., Dijkman, P. E., Frese, L., Sanders, B., Weber, B., et al. (2014). Transcatheter implantation of homologous “off-the-shelf” tissue-engineered heart valves with self-repair capacity: long-term functionality and rapid in vivo remodeling in sheep. Journal of the American College of Cardiology, 63(13), 1320–1329. doi:10.1016/j.jacc.2013.09.082.CrossRefPubMed

35.

Syedain, Z., Reimer, J., Schmidt, J., Lahti, M., Berry, J., Bianco, R., et al. (2015). 6-month aortic valve implantation of an off-the-shelf tissue-engineered valve in sheep. Biomaterials, 73, 175–184. doi:10.1016/j.biomaterials.2015.09.016.CrossRefPubMed

36.

Syedain, Z., Reimer, J., Lahti, M., Berry, J., Johnson, S., & Tranquillo, R. T. (2016). Tissue engineering of acellular vascular grafts capable of somatic growth in young lambs. Nature Communications, 7, 12951. doi:10.1038/ncomms12951.CrossRefPubMedPubMedCentral

37.

Sievers, H.-H., Stierle, U., Schmidtke, C., & Bechtel, M. (2003). Decellularized pulmonary homograft (SynerGraft) for reconstruction of the right ventricular outflow tract: first clinical experience. [journal article]. Zeitschrift für Kardiologie, 92(1), 53–59. doi:10.1007/s00392-003-0883-x.CrossRefPubMed

38.

Hibino, N., McConnell, P., Shinoka, T., Malik, M., & Galantowicz, M. (2015). Preliminary experience in the use of an extracellular matrix (CorMatrix) as a tube graft: word of caution. Seminars in thoracic and cardiovascular surgery, doi:10.1053/j.semtcvs.2015.08.008.

39.

Iop, L., & Gerosa, G. (2015). Guided tissue regeneration in heart valve replacement: from preclinical research to first-in-human trials. BioMed Research International, 2015, 432901. doi:10.1155/2015/432901.CrossRefPubMedPubMedCentral

40.

Salmikangas, P., Schuessler-Lenz, M., Ruiz, S., Celis, P., Reischl, I., Menezes-Ferreira, M., et al. (2015). Marketing regulatory oversight of advanced therapy medicinal products (ATMPs) in Europe: the EMA/CAT perspective. Advances in Experimental Medicine and Biology, 871, 103–130. doi:10.1007/978-3-319-18618-4_6.CrossRefPubMed

41.

Yano, K., Watanabe, N., Tsuyuki, K., Ikawa, T., Kasanuki, H., & Yamato, M. (2015). Regulatory approval for autologous human cells and tissue products in the United States, the European Union, and Japan. Regenerative Therapy, 1, 45–56. doi:10.1016/j.reth.2014.10.001.CrossRef

42.

Sanzenbacher, R., Dwenger, A., Schuessler-Lenz, M., Cichutek, K., & Flory, E. (2007). European regulation tackles tissue engineering. Nat Biotech, 25(10), 1089–1091.CrossRef

43.

Commission Directive 2009/120/EC of 14 September 2009 amending Directive 2001/83/EC of the European Parliament and of the Council on the Community code relating to medicinal products for human use as regards advanced therapy medicinal products (2009). Official Journal of the European Union, 242, 3).

44.

Lee, M. H., Arcidiacono, J. A., Bilek, A. M., Wille, J. J., Hamill, C. A., Wonnacott, K. M., et al. (2010). Considerations for tissue-engineered and regenerative medicine product development prior to clinical trials in the United States. Tissue Engineering. Part B, Reviews, 16(1), 41–54.CrossRefPubMed

45.

Lu, L., Arbit, H. M., Herrick, J. L., Segovis, S. G., Maran, A., & Yaszemski, M. J. (2015). Tissue engineered constructs: perspectives on clinical translation. Annals of Biomedical Engineering, 43(3), 796–804. doi:10.1007/s10439-015-1280-0.CrossRefPubMedPubMedCentral

46.

Law, E. U. (2012). Proposal for a regulation of the European Parliament and of the council on medical devices. EUR-Lex, 52012PC0542, http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex:52012PC50542.

47.

Lichtenberg, A., Tudorache, I., Cebotari, S., Suprunov, M., Tudorache, G., Goerler, H., et al. (2006). Preclinical testing of tissue-engineered heart valves re-endothelialized under simulated physiological conditions. Circulation, 114(1 Suppl), I559–I565. doi:10.1161/CIRCULATIONAHA.105.001206.PubMed

48.

Baraki, H., Tudorache, I., Braun, M., Hoffler, K., Gorler, A., Lichtenberg, A., et al. (2009). Orthotopic replacement of the aortic valve with decellularized allograft in a sheep model. Biomaterials, 30(31), 6240–6246. doi:10.1016/j.biomaterials.2009.07.068.CrossRefPubMed

49.

Iop, L., Bonetti, A., Naso, F., Rizzo, S., Cagnin, S., Bianco, R., et al. (2014). Decellularized allogeneic heart valves demonstrate self-regeneration potential after a long-term preclinical evaluation. PloS One, 9(6), e99593. doi:10.1371/journal.pone.0099593.CrossRefPubMedPubMedCentral

50.

Row, S., Peng, H., Schlaich, E. M., Koenigsknecht, C., Andreadis, S. T., & Swartz, D. D. (2015). Arterial grafts exhibiting unprecedented cellular infiltration and remodeling in vivo: the role of cells in the vascular wall. Biomaterials, 50, 115–126. doi:10.1016/j.biomaterials.2015.01.045.CrossRefPubMedPubMedCentral

51.

Koobatian, M. T., Row, S., Smith Jr., R. J., Koenigsknecht, C., Andreadis, S. T., & Swartz, D. D. (2016). Successful endothelialization and remodeling of a cell-free small-diameter arterial graft in a large animal model. Biomaterials, 76, 344–358. doi:10.1016/j.biomaterials.2015.10.020.CrossRefPubMed

52.

Simon, P., Kasimir, M. T., Seebacher, G., Weigel, G., Allrich, R., Salzer-Muhar, U., et al. (2003). Early failure of the tissue engineered porcine heart valve SYNERGRAFT in pediatric patients. European Journal of Cardio-Thoracic Surgery, 23(6), 1002–1006.CrossRefPubMed

53.

Voges, I., Brasen, J. H., Entenmann, A., Scheid, M., Scheewe, J., Fischer, G., et al. (2013). Adverse results of a decellularized tissue-engineered pulmonary valve in humans assessed with magnetic resonance imaging. European Journal of Cardio-Thoracic Surgery, 44(4), e272–e279. doi:10.1093/ejcts/ezt328.CrossRefPubMed

54.

Ruffer, A., Purbojo, A., Cicha, I., Glockler, M., Potapov, S., Dittrich, S., et al. (2010). Early failure of xenogenous de-cellularised pulmonary valve conduits—a word of caution! European Journal of Cardio-Thoracic Surgery, 38(1), 78–85. doi:10.1016/j.ejcts.2010.01.044.CrossRefPubMed

55.

Woo, J. S., Fishbein, M. C., & Reemtsen, B. (2015). Histologic examination of decellularized porcine intestinal submucosa extracellular matrix (CorMatrix) in pediatric congenital heart surgery. Cardiovascular Pathology. doi:10.1016/j.carpath.2015.08.007.PubMed

56.

Watanabe, M., Shin’oka, T., Tohyama, S., Hibino, N., Konuma, T., Matsumura, G., et al. (2001). Tissue-engineered vascular autograft: inferior vena cava replacement in a dog model. Tissue Engineering, 7(4), 429–439.CrossRefPubMed

57.

Hoerstrup, S. P., Kadner, A., Melnitchouk, S., Trojan, A., Eid, K., Tracy, J., et al. (2002). Tissue engineering of functional trileaflet heart valves from human marrow stromal cells. Circulation, 106(suppl I), I-143–I-150. doi:10.1161/01.cir.0000032872.55215.05.

58.

Frese, L., Sanders, B., Beer, G. M., Weber, B., Driessen-Mol, A., Baaijens, F. P. T., et al. (2015). Adipose derived tissue engineered heart valve. Journal of Tissue Science & Engineering, 06(03). doi:10.4172/2157-7552.1000156.

59.

Sodian, R., Schaefermeier, P., Begg-Zips, S., Kuebler, W. M., Shakibaei, M., & Daebritz, S. (2010). Use of human umbilical cord blood-derived progenitor cells for tissue-engineered heart valves. Ann.Thorac.Surg., 89(3), 819–828.CrossRefPubMed

60.

Bayon, Y., Vertes, A. A., Ronfard, V., Egloff, M., Snykers, S., Salinas, G. F., et al. (2014). Translating cell-based regenerative medicines from research to successful products: challenges and solutions. Tissue Engineering. Part B, Reviews, 20(4), 246–256. doi:10.1089/ten.TEB.2013.0727.CrossRefPubMed

61.

Fioretta, E. S., Simonet, M., Smits, A. I., Baaijens, F. P., & Bouten, C. V. (2014). Differential response of endothelial and endothelial colony forming cells on electrospun scaffolds with distinct microfiber diameters. Biomacromolecules, 15(3), 821–829. doi:10.1021/bm4016418.CrossRefPubMed

62.

Nisbet, D. R., Forsythe, J. S., Shen, W., Finkelstein, D. I., & Horne, M. K. (2009). Review paper: a review of the cellular response on electrospun nanofibers for tissue engineering. Journal of Biomaterials Applications, 24(1), 7–29.CrossRefPubMed

63.

Jana, S., Tranquillo, R. T., & Lerman, A. (2016). Cells for tissue engineering of cardiac valves. Journal of Tissue Engineering and Regenerative Medicine, 10(10), 804–824. doi:10.1002/term.2010.CrossRefPubMed

64.

da Costa, F. D., Dohmen, P. M., Duarte, D., von Glenn, C., Lopes, S. V., Filho, H. H., et al. (2005). Immunological and echocardiographic evaluation of decellularized versus cryopreserved allografts during the Ross operation. European Journal of Cardio-Thoracic Surgery, 27(4), 572–578. doi:10.1016/j.ejcts.2004.12.057.CrossRefPubMed

65.

Dijkman, P. E., Driessen-Mol, A., Frese, L., Hoerstrup, S. P., & Baaijens, F. P. (2012). Decellularized homologous tissue-engineered heart valves as off-the-shelf alternatives to xeno- and homografts. Biomaterials, 33(18), 4545–4554. doi:10.1016/j.biomaterials.2012.03.015.CrossRefPubMed

66.

Syedain, Z. H., Meier, L. A., Reimer, J. M., & Tranquillo, R. T. (2013). Tubular heart valves from decellularized engineered tissue. Annals of Biomedical Engineering, 41(12), 2645–2654. doi:10.1007/s10439-013-0872-9.CrossRefPubMed

67.

Melchiorri, A. J., Hibino, N., Yi, T., Lee, Y. U., Sugiura, T., Tara, S., et al. (2015). Contrasting biofunctionalization strategies for the enhanced endothelialization of biodegradable vascular grafts. Biomacromolecules, 16(2), 437–446. doi:10.1021/bm501853s.CrossRefPubMed

68.

Tara, S., Kurobe, H., Maxfield, M. W., Rocco, K. A., Yi, T., Naito, Y., et al. (2015). Evaluation of remodeling process in small-diameter cell-free tissue-engineered arterial graft. Journal of Vascular Surgery, 62(3), 734–743. doi:10.1016/j.jvs.2014.03.011.CrossRefPubMed

69.

Talacua, H., Smits, A. I., Muylaert, D. E., van Rijswijk, J. W., Vink, A., Verhaar, M. C., et al. (2015). In situ tissue engineering of functional small-diameter blood vessels by host circulating cells only. Tissue Engineering. Part A, 21(19–20), 2583–2594. doi:10.1089/ten.TEA.2015.0066.CrossRefPubMed

70.

Ekdahl, K. N., Lambris, J. D., Elwing, H., Ricklin, D., Nilsson, P. H., Teramura, Y., et al. (2011). Innate immunity activation on biomaterial surfaces: a mechanistic model and coping strategies. Advanced Drug Delivery Reviews, 63(12), 1042–1050. doi:10.1016/j.addr.2011.06.012.CrossRefPubMedPubMedCentral

71.

Smyth, J. V., Welch, M., Carr, H. M., Dodd, P. D., Eisenberg, P. R., & Walker, M. G. (1995). Fibrinolysis profiles and platelet activation after endothelial cell seeding of prosthetic vascular grafts. Annals of Vascular Surgery, 9(6), 542–546. doi:10.1007/BF02018827.CrossRefPubMed

72.

Laube, H. R., Duwe, J., Rutsch, W., & Konertz, W. (2000). Clinical experience with autologous endothelial cell-seeded polytetrafluoroethylene coronary artery bypass grafts. The Journal of Thoracic and Cardiovascular Surgery, 120(1), 134–141. doi:10.1067/mtc.2000.106327.CrossRefPubMed

73.

Zilla, P., Fasol, R., Deutsch, M., Fischlein, T., Minar, E., Hammerle, A., et al. (1987). Endothelial cell seeding of polytetrafluoroethylene vascular grafts in humans: a preliminary report. Journal of Vascular Surgery, 6(6), 535–541. doi:10.1016/0741-5214(87)90266-7.CrossRefPubMed

74.

Herring, M. B. (1991). Endothelial cell seeding. Journal of Vascular Surgery, 13(5), 731–732. doi:10.1016/0741-5214(91)90365-2.CrossRefPubMed

75.

Shi, Z., Neoh, K. G., & Kang, E. T. (2013). In vitro endothelialization of cobalt chromium alloys with micro/nanostructures using adipose-derived stem cells. Journal of Materials Science: Materials in Medicine, 24(4), 1067–1077. doi:10.1007/s10856-013-4868-7.PubMed

76.

Kim, Y., & Liu, J. C. (2016). Protein-engineered microenvironments can promote endothelial differentiation of human mesenchymal stem cells in the absence of exogenous growth factors. Biomaterials Science, 4(12), 1761–1772. doi:10.1039/C6BM00472E.CrossRefPubMed

77.

Melchiorri, A. J., Hibino, N., & Fisher, J. P. (2013). Strategies and techniques to enhance the in situ endothelialization of small-diameter biodegradable polymeric vascular grafts. Tissue Engineering. Part B, Reviews, 19(4), 292–307. doi:10.1089/ten.TEB.2012.0577.CrossRefPubMedPubMedCentral

78.

Lin, Q., Ding, X., Qiu, F., Song, X., Fu, G., & Ji, J. (2010). In situ endothelialization of intravascular stents coated with an anti-CD34 antibody functionalized heparin-collagen multilayer. Biomaterials, 31(14), 4017–4025. doi:10.1016/j.biomaterials.2010.01.092.CrossRefPubMed

79.

Rotmans, J. I., Heyligers, J. M., Verhagen, H. J., Velema, E., Nagtegaal, M. M., de Kleijn, D. P., et al. (2005). In vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation, 112(1), 12–18. doi:10.1161/CIRCULATIONAHA.104.504407.CrossRefPubMed

80.

Lu, S., Zhang, P., Sun, X., Gong, F., Yang, S., Shen, L., et al. (2013). Synthetic ePTFE grafts coated with an anti-CD133 antibody-functionalized heparin/collagen multilayer with rapid in vivo endothelialization properties. ACS Applied Materials & Interfaces, 5(15), 7360–7369. doi:10.1021/am401706w.CrossRef

81.

Jordan, J. E., Williams, J. K., Lee, S. J., Raghavan, D., Atala, A., & Yoo, J. J. (2012). Bioengineered self-seeding heart valves. The Journal of Thoracic and Cardiovascular Surgery, 143(1), 201–208. doi:10.1016/j.jtcvs.2011.10.005.CrossRefPubMed

82.

Ravi, S., Qu, Z., & Chaikof, E. L. (2009). Polymeric materials for tissue engineering of arterial substitutes. Vascular, 17(Supplement 1), S45-S54, doi:10.2310/6670.2008.00084.

83.

Zheng, W., Wang, Z., Song, L., Zhao, Q., Zhang, J., Li, D., et al. (2012). Endothelialization and patency of RGD-functionalized vascular grafts in a rabbit carotid artery model. Biomaterials, 33(10), 2880–2891. doi:10.1016/j.biomaterials.2011.12.047.CrossRefPubMed

84.

Caiado, F., Carvalho, T., Silva, F., Castro, C., Clode, N., Dye, J. F., et al. (2011). The role of fibrin E on the modulation of endothelial progenitors adhesion, differentiation and angiogenic growth factor production and the promotion of wound healing. Biomaterials, 32(29), 7096–7105. doi:10.1016/j.biomaterials.2011.06.022.CrossRefPubMed

85.

Rodenberg, E. J., & Pavalko, F. M. (2007). Peptides derived from fibronectin type III connecting segments promote endothelial cell adhesion but not platelet adhesion: implications in tissue-engineered vascular grafts. Tissue Engineering, 13(11), 2653–2666. doi:10.1089/ten.2007.0037.CrossRefPubMed

86.

Jun, H.-W., & West, J. L. (2005). Modification of polyurethaneurea with PEG and YIGSR peptide to enhance endothelialization without platelet adhesion. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 72B(1), 131–139. doi:10.1002/jbm.b.30135.CrossRef

87.

Aubin, H., Mas-Moruno, C., Iijima, M., Schutterle, N., Steinbrink, M., Assmann, A., et al. (2016). Customized interface biofunctionalization of decellularized extracellular matrix: toward enhanced endothelialization. Tissue Engineering. Part C, Methods, 22(5), 496–508. doi:10.1089/ten.TEC.2015.0556.CrossRefPubMedPubMedCentral

88.

Liu, P., Zhao, Y., Yan, Y., Hu, Y., Yang, W., & Cai, K. (2015). Construction of extracellular microenvironment to improve surface endothelialization of NiTi alloy substrate. Mater Sci Eng C Mater Biol Appl, 55, 1–7. doi:10.1016/j.msec.2015.05.047.CrossRefPubMed

89.

Smith Jr., R. J., Koobatian, M. T., Shahini, A., Swartz, D. D., & Andreadis, S. T. (2015). Capture of endothelial cells under flow using immobilized vascular endothelial growth factor. Biomaterials, 51, 303–312. doi:10.1016/j.biomaterials.2015.02.025.CrossRefPubMedPubMedCentral

90.

Wang, H., Leinwand, L. A., & Anseth, K. S. (2014). Cardiac valve cells and their microenvironment—insights from in vitro studies. Nature Reviews. Cardiology, 11(12), 715–727. doi:10.1038/nrcardio.2014.162.CrossRefPubMedPubMedCentral

91.

Yin, Y., Zhao, X., Fang, Y., Yu, S., Zhao, J., Song, M., et al. (2010). SDF-1α involved in mobilization and recruitment of endothelial progenitor cells after arterial injury in mice. Cardiovascular Pathology, 19(4), 218–227. doi:10.1016/j.carpath.2009.04.002.CrossRefPubMed

92.

Liu, T., Liu, S., Zhang, K., Chen, J., & Huang, N. (2014). Endothelialization of implanted cardiovascular biomaterial surfaces: the development from in vitro to in vivo. Journal of Biomedical Materials Research. Part A, 102(10), 3754–3772. doi:10.1002/jbm.a.35025.CrossRefPubMed

93.

Emmert, M. Y., & Hoerstrup, S. P. (2016). Tissue engineered heart valves: moving towards clinical translation. Expert Review of Medical Devices, 13(5), 417–419. doi:10.1586/17434440.2016.1171709.CrossRefPubMed

94.

Beebe, D. J., Ingber, D. E., & den Toonder, J. (2013). Organs on chips 2013. Lab on a Chip, 13(18), 3447–3448. doi:10.1039/c3lc90080k.CrossRefPubMed

95.

Ram-Liebig, G., Bednarz, J., Stuerzebecher, B., Fahlenkamp, D., Barbagli, G., Romano, G., et al. (2015). Regulatory challenges for autologous tissue engineered products on their way from bench to bedside in Europe. Advanced Drug Delivery Reviews, 82-83, 181–191. doi:10.1016/j.addr.2014.11.009.CrossRefPubMed

96.

Hurtado-Aguilar, L. G., Mulderrig, S., Moreira, R., Hatam, N., Spillner, J., Schmitz-Rode, T., et al. (2016). Ultrasound for in vitro noninvasive, real time monitoring and evaluation of tissue-engineered heart valves. Tissue Engineering. Part C, Methods. doi:10.1089/ten.TEC.2016.0300.PubMed

97.

Ozaki, S., Herijgers, P., & Flameng, W. (2004). A new model to test the calcification characteristics of bioprosthetic heart valves. Annals of Thoracic and Cardiovascular Surgery, 10, 23–28.PubMed

98.

Taramasso, M., Emmert, M. Y., Reser, D., Guidotti, A., Cesarovic, N., Campagnol, M., et al. (2015). Pre-clinical in vitro and in vivo models for heart valve therapies. Journal of Cardiovascular Translational Research, 8(5), 319–327. doi:10.1007/s12265-015-9631-7.CrossRefPubMed

99.

Yuan, S. M., Mishaly, D., Shinfeld, A., & Raanani, E. (2008). Right ventricular outflow tract reconstruction: valved conduit of choice and clinical outcomes. Journal of Cardiovascular Medicine, 9, 327–337.CrossRefPubMed

100.

Bayon, Y., Vertes, A. A., Ronfard, V., Culme-Seymour, E., Mason, C., Stroemer, P., et al. (2015). Turning regenerative medicine breakthrough ideas and innovations into commercial products. Tissue Engineering. Part B, Reviews, 21(6), 560–571. doi:10.1089/ten.TEB.2015.0068.CrossRefPubMed

101.

de Wilde, S., Guchelaar, H. J., Herberts, C., Lowdell, M., Hildebrandt, M., Zandvliet, M., et al. (2016). Development of cell therapy medicinal products by academic institutes. Drug Discovery Today, 21(8), 1206–1212. doi:10.1016/j.drudis.2016.04.016.CrossRefPubMed

Title: Translational Challenges in Cardiovascular Tissue Engineering
Authors: Maximilian Y. Emmert
Emanuela S. Fioretta
Simon P. Hoerstrup
Publication date: 01-04-2017
Publisher: Springer US
Published in: Journal of Cardiovascular Translational Research / Issue 2/2017
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI: https://doi.org/10.1007/s12265-017-9728-2

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Translational Challenges in Cardiovascular Tissue Engineering

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2017

Utilizing the Foreign Body Response to Grow Tissue Engineered Blood Vessels in Vivo

Intravascular Ultrasound Characterization of a Tissue-Engineered Vascular Graft in an Ovine Model

Stem Cell Spheroids and Ex Vivo Niche Modeling: Rationalization and Scaling-Up

Tissue Engineering—Bridging the Gap

Cardiovascular Bio-Engineering: Current State of the Art

The Dynamics of Cardiovascular Biomarkers in non-Elite Marathon Runners

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page