Journal of Healthcare Engineering

Journal of Healthcare Engineering / 2013 / Article

Research Article | Open Access

Volume 4 |Article ID 313045 | https://doi.org/10.1260/2040-2295.4.3.329

Diana Massai, Giulia Cerino, Diego Gallo, Francesco Pennella, Marco A. Deriu, Andres Rodriguez, Franco M. Montevecchi, Cristina Bignardi, Alberto Audenino, Umberto Morbiducci, "Bioreactors as Engineering Support to Treat Cardiac Muscle and Vascular Disease", Journal of Healthcare Engineering, vol. 4, Article ID 313045, 42 pages, 2013. https://doi.org/10.1260/2040-2295.4.3.329

Bioreactors as Engineering Support to Treat Cardiac Muscle and Vascular Disease

Received01 Nov 2012
Accepted01 Mar 2013

Abstract

Cardiovascular disease is the leading cause of morbidity and mortality in the Western World. The inability of fully differentiated, load-bearing cardiovascular tissues to in vivo regenerate and the limitations of the current treatment therapies greatly motivate the efforts of cardiovascular tissue engineering to become an effective clinical strategy for injured heart and vessels. For the effective production of organized and functional cardiovascular engineered constructs in vitro, a suitable dynamic environment is essential, and can be achieved and maintained within bioreactors. Bioreactors are technological devices that, while monitoring and controlling the culture environment and stimulating the construct, attempt to mimic the physiological milieu. In this study, a review of the current state of the art of bioreactor solutions for cardiovascular tissue engineering is presented, with emphasis on bioreactors and biophysical stimuli adopted for investigating the mechanisms influencing cardiovascular tissue development, and for eventually generating suitable cardiovascular tissue replacements.

References

  1. V. L. Roger and A. S. Go, “Executive summary: heart disease and stroke statistics-2012 update: a report from the American Heart Association,” Circulation, vol. 125, no. 1, pp. 188–197, 2012. View at: Google Scholar
  2. L. M. Ptaszek, M. Mansour, J. N. Ruskin, and K. R. Chien, “Towards regenerative therapy for cardiac disease,” Lancet, vol. 379, no. 9819, pp. 933–942, 2012. View at: Google Scholar
  3. World Health Organization - WHO, “Fact Sheet N°317, Cardiovascular diseases,” Geneva, Switzerland. September 2011, http://www.who.int/en/, Accessed July 12, 2012. View at: Google Scholar
  4. J. Leor, Y. Amsalem, and S. Cohen, “Cells, scaffolds, and molecules for myocardial tissue engineering,” Pharmacology and Therapeutics, vol. 105, no. 2, pp. 151–163, 2005. View at: Google Scholar
  5. T. Eschenhagen, M. Didié, F. Münzel, P. Schubert, K. Schneiderbanger, and W. H. Zimmermann, “3D engineered heart tissue for replacement therapy,” Basic Research in Cardiology, vol. 97, Suppl 1, pp. 146–152, 2002. View at: Google Scholar
  6. H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “British Medical Bulletin,” British Medical Bulletin, vol. 87, pp. 31–47, 2008. View at: Google Scholar
  7. R. E. Akins, R. A. Boyce, M. L. Madonna et al., “Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells,” Tissue Engineering, vol. 5, no. 2, pp. 103–118, 1999. View at: Google Scholar
  8. H. Jawad, N. N. Ali, A. R. Lyon, Q. Z. Chen, S. E. Harding, and A. R. Boccaccini, “Myocardial tissue engineering: a review,” Journal of Tissue Engineering and Regenerative Medicine, vol. 1, no. 5, pp. 327–342, 2007. View at: Google Scholar
  9. G. Vunjak-Novakovic, N. Tandon, A. Godier et al., “Challenges in cardiac tissue engineering,” Tissue Engineering Part B Review, vol. 16, no. 2, pp. 169–187, 2010. View at: Google Scholar
  10. M. Strüber, A. L. Meyer, D. Malehsa, C. Kugler, A. R. Simon, and A. Haverich, “The current status of heart transplantation and the development of “artificial heart systems”,” Deutsches Ärzteblatt International, vol. 106, no. 28-29, pp. 471–477, 2009. View at: Google Scholar
  11. K. A. Eagle, R. A. Guyton, R. Davidoff et al., “ACC/AHA 2004 guideline update for coronary artery bypass graft surgery: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Update the 1999 Guidelines for Coronary Artery Bypass Graft Surgery),” Circulation, vol. 110, no. 14, pp. 340–437, 2004. View at: Google Scholar
  12. R. Gauvin, M. Guillemette, T. Galbraith et al., “Mechanical properties of tissue-engineered vascular constructs produced using arterial or venous cells,” Tissue Engineering Part A, vol. 17, no. 15–16, pp. 2049–2059, 2011. View at: Google Scholar
  13. T. G. Brott, R. W. Hobson 2nd, G. Howard et al., “Stenting versus endarterectomy for treatment of carotid-artery stenosis,” The New England Journal of Medicine, vol. 363, no. 1, pp. 11–23, 2010. View at: Google Scholar
  14. J. Chlupác, E. Filová, and L. Bacáková, “Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery,” Physiological Research, vol. 58, Suppl 2, pp. S119–139, 2009. View at: Google Scholar
  15. J. P. Karam, C. Muscari, and C. N. Montero-Menei, “Combining adult stem cells and polymeric devices for tissue engineering in infarcted myocardium,” Biomaterials, vol. 33, no. 23, pp. 5683–5695, 2012. View at: Google Scholar
  16. M. S. Slaughter, J. G. Rogers, C. A. Milano et al., “Advanced heart failure treated with continuous-flow left ventricular assist device,” The New England Journal of Medicine, vol. 361, no. 23, pp. 2241–2251, 2009. View at: Google Scholar
  17. M. C. Oz, M. Argenziano, K. A. Catanese et al., “Bridge experience with long-term implantable left ventricular assist devices. Are they an alternative to transplantation?” Circulation, vol. 95, no. 7, pp. 1844–1852, 1997. View at: Google Scholar
  18. G. Matsumura, N. Hibino, Y. Ikada, H. Kurosawa, and T. Shin'oka, “Successful application of tissue engineered vascular autografts: clinical experience,” Biomaterials, vol. 24, no. 13, pp. 2303–2308, 2003. View at: Google Scholar
  19. R. J. Hassink, J. D. Dowell, A. Brutel de la Rivière, P. A. Doevendans, and L. J. Field, “Stem cell therapy for ischemic heart disease,” Trends in Molecular Medicine, vol. 9, no. 10, pp. 436–441, 2003. View at: Google Scholar
  20. R. J. Hassink, A. Brutel de la Rivière, C. L. Mummery, and P. A. Doevendans, “Transplantation of cells for cardiac repair,” Journal of the American College of Cardiology, vol. 41, no. 5, pp. 711–717, 2003. View at: Google Scholar
  21. D. Orlic, J. Kajstura, S. Chimenti et al., “Mobilized bone marrow cells repair the infarcted heart, improving function and survival,” Protocol of the National Academy of Science of the United States of America, vol. 98, no. 18, pp. 10344–10349, 2001. View at: Google Scholar
  22. K. B. Pasumarthi and L. J. Field, “Cardiomyocyte cell cycle regulation,” Circulation Research, vol. 90, no. 10, pp. 1044–1054, 2002. View at: Google Scholar
  23. L. J. Field, “Modulation of the cardiomyocyte cell cycle in genetically altered animals,” Annals of the New York Academy of Science, vol. 1015, pp. 160–170, 2004. View at: Google Scholar
  24. R. J. Hassink, K. B. Pasumarthi, H. Nakajima et al., “Cardiomyocyte cell cycle activation improves cardiac function after myocardial infarction,” Cardiovascular Research, vol. 78, no. 1, pp. 18–25, 2008. View at: Google Scholar
  25. E. R. Porrello, A. I. Mahmoud, E. Simpson et al., “Transient regenerative potential of the neonatal mouse heart,” Science, vol. 331, no. 6020, pp. 1078–1080, 2011. View at: Google Scholar
  26. K. Kikuchi, J. E. Holdway, A. A. Werdich et al., “Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes,” Nature, vol. 464, no. 7288, pp. 601–605, 2010. View at: Google Scholar
  27. K. Bilodeau and D. Mantovani, “Bioreactors for tissue engineering: focus on mechanical constraints. A comparative review,” Tissue Engineering, vol. 12, no. 8, pp. 2367–2383, 2006. View at: Google Scholar
  28. F. Lyons, S. Partap, and F. J. O?Brien, “Part 1: scaffolds and surfaces,” Technology and Healthcare, vol. 16, no. 4, pp. 305–317, 2008. View at: Google Scholar
  29. W. L. Grayson, T. P. Martens, G. M. Eng, M. Radisic, and G. Vunjak-Novakovic, “Biomimetic approach to tissue engineering,” Seminars in cells and developmental biology, vol. 20, no. 6, pp. 665–673, 2009. View at: Google Scholar
  30. R. J. Egli and R. Luginbuehl, “Tissue engineering—nanomaterials in the musculoskeletal system,” Swiss Medical Weekly, vol. 142:w13647, 2012. View at: Google Scholar
  31. E. Figallo, Advanced technologies for cardiac tissue engineering [Ph.D. Dissertation], Universitá degli Studi di Padova, 2008.
  32. R. Ogawa, K. Oki, and H. Hyakusoku, “Vascular tissue engineering and vascularized 3D tissue regeneration,” Regenerative Medicine, vol. 2, no. 5, pp. 831–837, 2007. View at: Google Scholar
  33. I. Martin, D. Wendt, and M. Heberer, “The role of bioreactors in tissue engineering,” Trends Biotechnology, vol. 22, no. 2, pp. 80–86, 2004. View at: Google Scholar
  34. N. Plunkett and F. J. O'Brien, “Bioreactors in tissue engineering,” Studies in Health Technology and Information, vol. 152, pp. 214–230, 2010. View at: Google Scholar
  35. R. L. Carrier, M. Papadaki, M. Rupnick et al., “Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization,” Biotechnology and Bioengineering, vol. 64, no. 5, pp. 580–589, 1999. View at: Google Scholar
  36. R. Carrier, Cardiac tissue engineering: bioreactor cultivation parameters [Ph.D. Dissertation], Massachusetts Institute of Technology, 2000.
  37. S. A. Korossis, F. Bolland, J. N. Kearney, J. Fisher, and E. Ingham, “Bioreactors in tissue engineering,” in Nureddin Ashammakhi, Rui L Reis, Ed., vol. 2 of Topics in Tissue Engineering, Chapter 8, 2005. View at: Google Scholar
  38. K. Dumont, J. Yperman, E. Verbeken et al., “Design of a new pulsatile bioreactor for tissue engineered aortic heart valve formation,” Artificial Organs, vol. 26, no. 8, pp. 710–714, 2002. View at: Google Scholar
  39. I. Martin, T. Smith, and D. Wendt, “Bioreactor-based roadmap for the translation of tissue engineering strategies into clinical products,” Trends Biotechnology, vol. 27, no. 9, pp. 495–502, 2009. View at: Google Scholar
  40. R. Archer and D. J. Williams, “Why tissue engineering needs process engineering,” Nature Biotechnology, vol. 23, no. 11, pp. 1353–1355, 2005. View at: Google Scholar
  41. R. Pörtner, S. Nagel-Heyer, C. Goepfert, P. Adamietz, and N. M. Meenen, “Bioreactor design for tissue engineering,” Journal for Bioscience and Bioengineering, vol. 100, no. 3, pp. 235–245, 2005. View at: Google Scholar
  42. R. Olmer, A. Lange, S. Selzer et al., “Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors,” Tissue Engineering Part C Methods, vol. 18, no. 10, pp. 772–784, 2012. View at: Google Scholar
  43. C. V. Bouten, P. Y. Dankers, A. Driessen-Mol, S. Pedron, A. M. Brizard, and F. P. Baaijens, “Substrates for cardiovascular tissue engineering,” Advanced Drug Delivery Reviews, vol. 63, no. 4–5, pp. 221–241, 2011. View at: Google Scholar
  44. M. Shachar and S. Cohen, “Cardiac tissue engineering, ex-vivo: design principles in biomaterials and bioreactors,” Heart Failure Reviews, vol. 8, no. 3, pp. 271–276, 2003. View at: Google Scholar
  45. A. Ratcliffe and L. E. Niklason, “Bioreactors and bioprocessing for tissue engineering,” Annals of the NY Academy of Sciences, vol. 96, pp. 210–215, 2002. View at: Google Scholar
  46. A. Sen, M. S. Kallos, and L. A. Behie, “New tissue dissociation protocol for scaled-up production of neural stem cells in suspension bioreactors,” Tissue Engineering, vol. 10, no. 5–6, pp. 904–913, 2004. View at: Google Scholar
  47. S. Schaaf, A. Shibamiya, M. Mewe et al., “Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology,” PLoS One, vol. 6, no. 10: e26397, 2011. View at: Google Scholar
  48. K. Irani, I. Pomerantseva, A. R. Hart, C. A. Sundback, C. M. Neville, and J. P. Vacanti, “Mechanical dissociation of swine liver to produce organoid units for tissue engineering and in vitro disease modeling,” Artificial Organs, vol. 34, no. 1, pp. 75–78, 2010. View at: Google Scholar
  49. R. B. Devereux and N. Reichek, “Echocardiographic determination of left ventricular mass in man anatomic validation of the method,” Circulation, vol. 55, no. 4, pp. 613–618, 1977. View at: Google Scholar
  50. D. Schneck, “An outline of cardiovascular structure and function,” in Tissue Engineering, Bernhard Palsson, Jeffrey A. Hubbell, Robert Plonsey, and Joseph D. Bronzino, Eds., I-1-I-12, CRC Press, 2003. View at: Google Scholar
  51. N. J. Fortuin, W. P. Hood Jr, M. E. Sherman, and E. Craige, “Determination of left ventricular volumes by ultrasound,” Circulation, vol. 44, pp. 575–584, 1971. View at: Google Scholar
  52. L. T. Mahoney, W. Smith, M. P. Noel, M. Florentine, D. J. Skorton, and S. M. Collins, “Measurement of right ventricular volume using cine computer tomography,” Investigative Radiology, vol. 22, no. 6, pp. 451–455, 1987. View at: Google Scholar
  53. M. E. Klingensmith, L. Ern Chen, S. C. Glasgow, T. A. Goers, and S. J. Melby, The Washington Manual of Surgery, Wolters Kluwer Health/Lippincott Williams & Wilkins, 2008.
  54. M. A. Punchard, C. Stenson-Cox, E. D. O'cearbhaill et al., “Endothelial cell response to biomechanical forces under simulated vascular loading conditions,” Journal of Biomechanics, vol. 40, no. 14, pp. 3146–3154, 2007. View at: Google Scholar
  55. G. Konig, T. N. McAllister, N. Dusserre et al., “Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery,” Biomaterials, vol. 30, no. 8, pp. 1542–1550, 2009. View at: Google Scholar
  56. H. N. Mayrovitz, R. F. Tuma, and M. P. Wiedeman, “Relationship between microvascular blood velocity and pressure distribution,” American Journal of Physiology, vol. 232, no. 4, pp. 400–405, 1977. View at: Google Scholar
  57. A. M. Malek, S. L. Alper, and S. Izumo, “Hemodynamic shear stress and its role in atherosclerosis,” The Journal of the American Medical Association, vol. 282, no. 21, pp. 2035–2042, 1999. View at: Google Scholar
  58. T. Kuznetsova, L. Herbots, T. Richart et al., “Left ventricular strain and strain rate in a general population,” European Heart Journal, vol. 29, no. 16, pp. 2014–2023, 2014. View at: Google Scholar
  59. V. Mironov, V. Kasyanov, K. McAllister, S. Oliver, J. Sistino, and R. Markwald, “Perfusion bioreactor for vascular tissue engineering with capacities for longitudinal stretch,” Journal of Craniofacial Surgery, vol. 14, no. 3, pp. 340–347, 2003. View at: Google Scholar
  60. N. Tandon, C. Cannizzaro, P. G. Chao et al., “Electrical stimulation systems for cardiac tissue engineering,” Nature Protocols, vol. 4, no. 2, pp. 155–173, 2009. View at: Google Scholar
  61. G. D. Buckberg, “Basic science review: the helix and the heart,” Journal of Thoracic and Cardiovascular Surgery, vol. 124, no. 5, pp. 863–883, 2002. View at: Google Scholar
  62. P. Akhyari, H. Kamiya, A. Haverich, M. Karck, and A. Lichtenberg, “Myocardial tissue engineering: the extracellular matrix,” European Journal of Cardiothoracic Surgery, vol. 34, no. 2, pp. 229–241, 2008. View at: Google Scholar
  63. R. L. Carrier, M. Rupnick, R. Langer, F. J. Schoen, L. E. Freed, and G. Vunjak-Novakovic, “Effects of oxygen on engineered cardiac muscle,” Biotechnology Bioengineering, vol. 78, no. 6, pp. 617–625, 2002. View at: Google Scholar
  64. C. Holubarsch, J. Ludemann, S. Wiessner et al., “Shortening versus isometric contractions in isolated human failing and non-failing left ventricular myocardium: dependency of external work and force on muscle length, heart rate and inotropic stimulation,” Cardiovascular Research, vol. 37, no. 1, pp. 46–57, 1998. View at: Google Scholar
  65. L. A. Mulieri, G. Hasenfuss, B. Leavitt, P. D. Allen, and N. R. Alpert, “Altered myocardial force-frequency relation in human heart failure,” Circulation, vol. 85, no. 5, pp. 1743–1750, 1992. View at: Google Scholar
  66. D. M. Durand, “Electrical stimulation of excitable tissue,” in the Biomedical EngIneerIng Handbook, Joseph D. Bronzino, Ed., Chapter 17, CRC Press, 2nd edition, 2000. View at: Google Scholar
  67. R. Nuccitelli, “Endogenous ionic currents and DC electric fields in multicellular animal tissues,” Bioelectromagnetics, Suppl 1, pp. 147–157, 1992. View at: Google Scholar
  68. W. H. Zimmermann, C. Fink, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes,” Biotechnology and Bioengineering, vol. 68, no. 1, pp. 106–114, 2000. View at: Google Scholar
  69. W. H. Zimmermann, I. Melnychenko, G. Wasmeier et al., “Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts,” Nature Medicine, vol. 12, no. 4, pp. 452–458, 2006. View at: Google Scholar
  70. W. P. Smotherman, S. R. Robinson, A. E. Ronca, J. R. Alberts, and P. G. Hepper, “Heart rate response of the rat fetus and neonate to a chemosensory stimulus,” Physiology & Behaviour, vol. 50, no. 1, pp. 47–52, 1991. View at: Google Scholar
  71. WikiVet, http://en.wikivet.net/Rat_Physiology_-_WikiNormals, Accessed January 2, 2013.
  72. C. H. Mun, Y. Jung, S. H. Kim et al., “Three-dimensional electrospun poly(lactide-co-ε-caprolactone) for small-diameter vascular grafts,” Tissue Engineering Part A, vol. 18, no. 15–16, pp. 1608–1616, 2012. View at: Google Scholar
  73. R. E. Shadwick, “Mechanical design in arteries,” The Journal of Experimental Biology, vol. 202, pp. 3305–3313, 1999. View at: Google Scholar
  74. B. M. Learoyd and M. G. Taylor, “Alterations with age in the viscoelastic properties of human arterial walls,” Circulation Research, vol. 18, pp. 278–292, 1966. View at: Google Scholar
  75. D. Adams and M. McKinley, “The sheep. Anzccart Human Science,” Fact Sheet A9. July, 2009, http://www.adelaide.edu.au/ANZCCART/publications/A9_SheepFactSheet.pdf, Accessed January 3, 2013. View at: Google Scholar
  76. F. Esposito, N. Vitale, B. Crescenzi, M. Scardone, L. de Luca, and M. Cotrufo, “Short-term results of bovine internal mammary artery use in cardiovascular surgery,” Texas Heart Institute Journal, vol. 21, no. 3, pp. 193–197, 1994. View at: Google Scholar
  77. WIkiVet, http://en.wikivet.net/Bovine_Physiology_-_WikiNormals, Accessed January 2, 2013.
  78. J. T. Doyle, J. L. Patterson Jr, J. V. Warren, and D. K. Detweiler, “Observations on the circulation of domestic cattle,” Circulation Research, vol. 8, pp. 4–15, 1960. View at: Google Scholar
  79. S. T. Rashid, H. J. Salacinski, G. Hamilton, and A. M. Seifalian, “The use of animal models in developing the discipline of cardiovascular tissue engineering: a review,” Biomaterials, vol. 25, no. 9, pp. 1627–1637, 2004. View at: Google Scholar
  80. C. Fink, S. Ergün, D. Kralisch, U. Remmers, J. Weil, and T. Eschenhagen, “Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement,” Federation of American Societies for Experimental Biology Journal, vol. 14, no. 5, pp. 669–679, 2000. View at: Google Scholar
  81. D. Wendt, S. A. Riboldi, M. Cioffi, and I. Martin, “Potential and bottlenecks of bioreactors in 3D cell culture and tissue manufacturing,” Advanced Materials, vol. 21, no. 32–33, pp. 3352–3367, 2009. View at: Google Scholar
  82. L. E. Freed, F. Guilak, X. E. Guo et al., “Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling,” Tissue Engineering, vol. 12, no. 12, pp. 3285–3305, 2006. View at: Google Scholar
  83. V. Barron, E. Lyons, C. Stenson-Cox, P. E. McHugh, and A. Pandit, “Bioreactors for cardiovascular cell and tissue growth: a review,” Annals of Biomedical Engineering, vol. 31, no. 9, pp. 1017–1030, 2003. View at: Google Scholar
  84. B. A. Nasseri, I. Pomerantseva, M. R. Kaazempur-Mofrad et al., “Dynamic rotational seeding and cell culture system for vascular tube formation,” Tissue Engineering, vol. 9, no. 2, pp. 291–299, 2003. View at: Google Scholar
  85. N. Tandon, A. Marsano, C. Cannizzaro, J. Voldman, and G. Vunjak-Novakovic, “Design of electrical stimulation bioreactors for cardiac tissue engineering,” in Conference Proceedings—IEEE Engineering in Medicine and Biology Society, pp. 3594–3597, 2008. View at: Google Scholar
  86. H. Mertsching and J. Hansmann, “Bioreactor technology in cardiovascular tissue engineering,” Advances in Biochemical Engineering Biotechnology, vol. 112, pp. 29–37, 2009. View at: Google Scholar
  87. M. Gonen-Wadmany, L. Gepstein, and D. Seliktar, “Controlling the cellular organization of tissue-engineered cardiac constructs,” Annals of the NY Academy of Sciences, vol. 1015, pp. 299–311, 2004. View at: Google Scholar
  88. E. Lyons and A. Pandit, “Design of bioreactors for cardiovascular applications,” in Topics in Tissue Engineering, Nureddin Ashammakhi and Rui L. Reis, Eds., vol. Volume 2,, Chapter 7, 2005. View at: Google Scholar
  89. M. Papadaki, N. Bursac, R. Langer, J. Merok, G. Vunjak-Novakovic, and L. E. Freed, “Tissue engineering of functional cardiac muscle: molecular, structural, and electrophysiological studies,” American Journal of Physiology Heart and Circulatory Physiology, vol. 280, no. 1, pp. 168–178, 2001. View at: Google Scholar
  90. T. Eschenhagen, C. Fink, U. Remmers et al., “Three dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system,” Federation of American Societies for Experimental Biology Journal, vol. 11, pp. 683–694, 1997. View at: Google Scholar
  91. W. H. Zimmermann, K. Schneiderbanger, P. Schubert et al., “Tissue engineering of a differentiated cardiac muscle construct,” Circulation Research, vol. 90, no. 2, pp. 223–230, 2002. View at: Google Scholar
  92. R. K. Birla, Y. C. Huang, and R. G. Dennis, “Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle,” Tissue Engineering, vol. 13, no. 9, pp. 2239–2248, 2007. View at: Google Scholar
  93. R. E. Akins, R. A. Boyce, M. L. Madonna et al., “Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells,” Tissue Engineering, vol. 5, no. 2, pp. 103–118, 1999. View at: Google Scholar
  94. R. L. Carrier, M. Rupnick, R. Langer, F. Schoen, L. E. Freed, and G. Vunjak-Novakovic, “Perfusion improves tissue architecture of engineered cardiac muscle,” Tissue Engineering, vol. 8, no. 2, pp. 175–188, 2002. View at: Google Scholar
  95. M. Radisic, M. Euloth, L. Yang, R. Langer, L. E. Freed, and G. Vunjak-Novakovic, “High-density seeding of myocyte cells for cardiac tissue engineering,” Biotechnology Bioengineering, vol. 82, no. 4, pp. 403–414, 2003. View at: Google Scholar
  96. M. Radisic, H. Park, H. Shing et al., “Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds,” Proceedings of the National Academy of Science of the USA, vol. 101, no. 52, pp. 18129–18134, 2004. View at: Google Scholar
  97. N. Tandon, A. Marsano, R. Maidhof, L. Wan, H. Park, and G. Vunjak-Novakovic, “Optimization of electrical stimulation parameters for cardiac tissue engineering,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 6, pp. 115–125, 2011. View at: Google Scholar
  98. N. Tandon, B. Goh, A. Marsano et al., “Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation,” in Conference Proceedings—IEEE Engineering in Medicine and Biology Society, pp. 6517–6521, 2009. View at: Google Scholar
  99. Y. Barash, T. Dvir, P. Tandeitnik, E. Ruvinov, H. Guterman, and S. Cohen, “Electric field stimulation integrated into perfusion bioreactor for cardiac tissue engineering,” Tissue Engineering Part C Methods, vol. 16, no. 6, pp. 1417–1426, 2010. View at: Google Scholar
  100. R. Maidhof, N. Tandon, E. J. Lee et al., “Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue,” Journal of Tissue Engineering and Regenerative Medicine, vol. 6, no. 10, pp. e12–23, 2012. View at: Google Scholar
  101. A. Hansen, A. Eder, M. Bönstrup et al., “Development of a Drug Screening Platform Based on Engineered Heart Tissue,” Circulation Research, vol. 107, pp. 35–44, 2010. View at: Google Scholar
  102. G. Kensah, I. Gruh, J. Viering et al., “A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation,” Tissue Engineering Part C Methods, vol. 17, no. 4, pp. 463–473, 2011. View at: Google Scholar
  103. G. Kensah, A. Roa Lara, J. Dahlmann et al., “Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro,” European Heart Journal, 2012. View at: Google Scholar
  104. T. Boudou, W. R. Legant, A. Mu et al., “A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues,” Tissue Engineering Part A, vol. 18, no. 9–10, pp. 910–919, 2012. View at: Google Scholar
  105. T. Eschenhagen, M. Didié, J. Heubach, U. Ravens, and W. H. Zimmerman, “Cardiac tissue engineering,” Transplant Immunology, vol. 9, no. 2–4, pp. 315–321, 2002. View at: Google Scholar
  106. W. H. Zimmermann, M. Didié, G. H. Wasmeier et al., “Cardiac grafting of engineered heart tissue in syngenic rats,” Circulation, vol. 106, no. 12, Suppl 1, pp. 151–157, 2002. View at: Google Scholar
  107. N. Bursac, M. Papadaki, R. J. Cohen et al., “Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies,” American Journal of Physiology, vol. 277, no. 2, Pt 2, pp. H433–44, 1999. View at: Google Scholar
  108. M. Radisic, A. Marsano, R. Maidhof, Y. Wang, and G. Vunjak-Novakovic, “Cardiac tissue engineering using perfusion bioreactor systems,” Nature Protocols, vol. 3, no. 4, pp. 719–738, 2008. View at: Google Scholar
  109. T. Dvir, O. Levy, M. Shachar, Y. Granot, and S. Cohen, “Activation of the ERK1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly,” Tissue Engineering, vol. 13, no. 9, pp. 2185–2193, 2007. View at: Google Scholar
  110. M. A. Brown, R. K. Iyer, and M. Radisic, “Pulsatile perfusion bioreactor for cardiac tissue engineering,” Biotechnology Progress, vol. 24, no. 4, pp. 907–920, 2008. View at: Google Scholar
  111. C. Holubarsch, J. Ludemann, S. Wiessner et al., “Shortening versus isometric contractions in isolated human failing and non-failing left ventricular myocardium: dependency of external work and force on muscle length, heart rate and inotropic stimulation,” Cardiovascular Research, vol. 37, pp. 46–57, 1998. View at: Google Scholar
  112. L. A. Mulieri, G. Hasenfuss, B. Leavitt, P. D. Allen, and N. R. Alpert, “Altered myocardial force-frequency relation in human heart failure,” Circulation, vol. 85, pp. 1743–1750, 1992. View at: Google Scholar
  113. J. Dahlmann, A. Krause, L. Möller et al., “Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering,” Biomaterials, vol. 34, no. 4, pp. 940–951, 2013. View at: Google Scholar
  114. SP. Hoerstrup, G. Zünd, R. Sodian, AM. Schnell, J. Grünenfelder, and M. I. Turina, “Tissue engineering of small caliber vascular grafts,” European Journal of Cardiothoracic Surgery, vol. 20, no. 1, pp. 164–169, 2001. View at: Google Scholar
  115. H. Song, P. W. Zandstra, and M. Radisic, “Engineered heart tissue model of diabetic myocardium,” Tissue Engineering Part A, vol. 17, no. 13–14, pp. 1869–1878, 2011. View at: Google Scholar
  116. J. T. Krawiec and D. A. Vorp, “Adult stem cell-based tissue engineered blood vessels: a review,” Biomaterials, vol. 33, no. 12, pp. 3388–3400, 2012. View at: Google Scholar
  117. W. S. Sheridan, J. P. Duffy, and B. P. Murphy, “Mechanical characterization of a customized decellularized scaffold for vascular tissue engineering,” Journal of the Mechanical Behavior of Biomedical Materials, vol. 8, pp. 58–70, 2012. View at: Google Scholar
  118. K. Iwasaki, K. Kojima, S. Kodama et al., “Bioengineered threelayered robust and elastic artery using hemodynamically-equivalent pulsatile bioreactor,” Circulation, vol. 118, Suppl 14, pp. S52–S57, 2008. View at: Google Scholar
  119. M. A. Cleary, E. Geiger, C. Grady, C. Best, Y. Naito, and C. Breuer, “Vascular tissue engineering: the next generation,” Trends in Molecular Medicine, vol. 18, no. 7, pp. 394–404, 2012. View at: Google Scholar
  120. L. E. Niklason, L. Gao, W. M. Abbott et al., “Functional arteries grown in vitro,” Science, vol. 284, no. 5413, pp. 489–493, 1999. View at: Google Scholar
  121. O. E. Teebken and A. Haverich, “Tissue engineering of small-diameter vascular grafts,” European Journal of Vascular and Endovascular Surgery, vol. 23, 475:485, 2002. View at: Google Scholar
  122. L. H. Yap and C. E. Butler, “Principles of Microsurgery,” in Grabb and Smith's Plastic Surgery, Charles H. Thorne, Ed., pp. 66–72, Wolters Kluwer Health/Lippincott Williams & Wilkins, 6th edition, 2006. View at: Google Scholar
  123. T. Zhao, W. Zhao, Y. Chen, R. A. Ahokas, and Y. Sun, “Vascular endothelial growth factor (VEGF)-A: role on cardiac angiogenesis following myocardial infarction,” Microvascular Research, vol. 80, no. 2, pp. 188–194, 2010. View at: Google Scholar
  124. C. B. Weinberg and E. Bell, “A blood vessel model constructed from collagen and cultured vascular cells,” Science, vol. 231, pp. 397–400, 1986. View at: Google Scholar
  125. N. L'Heureux, S. Pâquet, R. Labbé, L. Germain, and F. Auger, “A completely biological tissue-engineered human blood vessel,” Federation of American Societies for Experimental Biology Journal, vol. 12, no. 1, pp. 47–56, 1998. View at: Google Scholar
  126. M. G. Geeslin, G. J. Caron, S. M. Kren, E. M. Sparrow, D. A. Hultman, and D. A. Taylor, “Bioreactor for the reconstitution of a decellularized vascular matrix of biological origin,” Journal of Biomedical Science and Engineering, vol. 4, pp. 435–442, 2011. View at: Google Scholar
  127. C. Williams and T. M. Wick, “Perfusion bioreactor for small diameter tissue-engineered arteries,” Tissue Engineering, vol. 10, no. 5–6, pp. 930–941, 2004. View at: Google Scholar
  128. Y. Narita, K. Hata, H. Kagami, A. Usui, M. Ueda, and Y. Ueda, “Novel pulse duplicating bioreactor system for tissue-engineered vascular construct,” Tissue Engineering, vol. 10, no. 7–8, pp. 1224–1233, 2004. View at: Google Scholar
  129. S. K. Yazdani, B. Watts, M. Machingal, Y. P. Jarajapu, M. E. Van Dyke, and G. J. Christ, “Smooth muscle cell seeding of decellularized scaffolds: the importance of bioreactor preconditioning to development of a more native architecture for tissue-engineered blood vessels,” Tissue Engineering Part A, vol. 15, no. 4, pp. 827–840, 2009. View at: Google Scholar
  130. K. Bilodeau, F. Couet, F. Boccafoschi, and D. Mantovani, “Design of a perfusion bioreactor specific to the regeneration of vascular tissues under mechanical stresses,” Artificial Organs, vol. 29, no. 11, pp. 906–912, 2005. View at: Google Scholar
  131. X. Zhang, X. Wang, V. Keshav et al., “Dynamic culture conditions to generate silk-based tissue-engineered vascular grafts,” Biomaterials, vol. 30, no. 19, pp. 3213–3223, 2009. View at: Google Scholar
  132. S. Amensag and P. S. McFetridge, “Rolling the human amnion to engineer laminated vascular tissues,” Tissue Engineering Part C Methods, vol. 18, no. 11, pp. 903–912, 2012. View at: Google Scholar
  133. F. Couet, S. Meghezi, and D. Mantovani, “Fetal development, mechanobiology and optimal control processes can improve vascular tissue regeneration in bioreactors: an integrative review,” Medical Engineering and Physics, vol. 34, no. 3, pp. 269–278, 2012. View at: Google Scholar
  134. R. Maidhof, A. Marsano, E. J. Lee, and G. Vunjak-Novakovic, “Perfusion seeding of channeled elastomeric scaffolds with myocytes and endothelial cells for cardiac tissue engineering,” Biotechnology Progress, vol. 26, no. 2, pp. 565–572, 2010. View at: Google Scholar
  135. M. Lovett, D. Rockwood, A. Baryshyan, and D. L. Kaplan, “Simple modular bioreactors for tissue engineering: a system for characterization of oxygen gradients, human mesenchymal stem cell differentiation, and prevascularization,” Tissue Engineering Part C Methods, vol. 16, no. 6, pp. 1565–1573, 2010. View at: Google Scholar
  136. J. A. Paten, R. Zareian, N. Saeidi, S. A. Melotti, and J. W. Ruberti, “Design and performance of an optically accessible, low-volume, mechanobioreactor for long-term study of living constructs,” Tissue Engineering Part C Methods, vol. 17, no. 7, pp. 775–788, 2011. View at: Google Scholar
  137. R. J. Loverde, R. E. Tolentino, and B. J. Pfister, “Axon stretch growth: the mechanotransduction of neuronal growth,” Journal of Visualized Experiments, vol. 54:2753, 2011. View at: Google Scholar
  138. L. Mortati, C. Divieto, and M. P. Sassi, “CARS and SHG microscopy to follow collagen production in living human corneal fibroblasts and mesenchymal stem cells in fibrin hydrogel 3D cultures,” Journal of Raman Spectroscopy, vol. 43, pp. 675–680, 2012. View at: Google Scholar
  139. F. Consolo, C. Bariani, A. Mantalaris, F. M. Montevecchi, A. Redaelli, and U. Morbiducci, “Computational modeling for the optimization of a cardiogenic 3D bioprocess of encapsulated embryonic stem cells,” Biomechanics and Modeling in Mechanobiology, vol. 11, no. 1–2, pp. 261–277, 2012. View at: Google Scholar
  140. L. A. Hidalgo-Bastida, S. Thirunavukkarasu, S. Griffiths, S. H. Cartmell, and S. Naire, “Modeling and design of optimal flow perfusion bioreactors for tissue engineering applications,” Biotechnology and Bioengineering, vol. 109, no. 4, pp. 1095–1099, 2012. View at: Google Scholar
  141. M. Israelowitz, B. Weyand, S. Rizvi, P. M. Vogt, and H. P. von Schroeder, “Development of a laminar flow bioreactor by computational fluid dynamics,” Journal of Healthcare Engineering, vol. 3, no. 3, pp. 455–476, 2012. View at: Google Scholar
  142. F. Couet and D. Mantovani, “Optimization of culture conditions in a bioreactor for vascular tissue engineering using a mathematical model of vascular growth and remodeling,” Cardiovascular Engineering and Technology, vol. 3, no. 2, pp. 228–236, 2012. View at: Google Scholar
  143. E. Figallo, C. Cannizzaro, S. Gerecht et al., “Microbioreactor array for controlling cellular microenvironments,” Lab on a Chip, vol. 7, no. 6, pp. 710–719, 2007. View at: Google Scholar

Copyright © 2013 Hindawi Publishing Corporation. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


More related articles

 PDF Download Citation Citation
 Order printed copiesOrder
Views602
Downloads667
Citations

Related articles

We are committed to sharing findings related to COVID-19 as quickly as possible. We will be providing unlimited waivers of publication charges for accepted research articles as well as case reports and case series related to COVID-19. Review articles are excluded from this waiver policy. Sign up here as a reviewer to help fast-track new submissions.