Bioreactors as engineering support to treat cardiac muscle and vascular disease.

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.

[1]  Vladimir Mironov,et al.  Perfusion Bioreactor for Vascular Tissue Engineering with Capacities for Longitudinal Stretch , 2003, The Journal of craniofacial surgery.

[2]  Niamh Plunkett,et al.  Bioreactors in tissue engineering. , 2011, Technology and health care : official journal of the European Society for Engineering and Medicine.

[3]  Milica Radisic,et al.  2 BIOMATERIAL SCAFFOLDS FOR GUIDING TISSUE ORGANIZATION , 2009 .

[4]  Thomas Eschenhagen,et al.  Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[5]  C. Vacanti,et al.  Bioengineered Three-Layered Robust and Elastic Artery Using Hemodynamically-Equivalent Pulsatile Bioreactor , 2008, Circulation.

[6]  Gordana Vunjak-Novakovic,et al.  Perfusion improves tissue architecture of engineered cardiac muscle. , 2002, Tissue engineering.

[7]  L. A. Hidalgo-Bastida,et al.  Modeling and design of optimal flow perfusion bioreactors for tissue engineering applications. , 2012, Biotechnology and bioengineering.

[8]  M. G. Taylor,et al.  Alterations with Age in the Viscoelastic Properties of Human Arterial Walls , 1966, Circulation research.

[9]  N Reichek,et al.  Echocardiographic Determination of Left Ventricular Mass in Man: Anatomic Validation of the Method , 1977, Circulation.

[10]  A. Kirschning,et al.  Fully defined in situ cross-linkable alginate and hyaluronic acid hydrogels for myocardial tissue engineering. , 2013, Biomaterials.

[11]  E Bell,et al.  A blood vessel model constructed from collagen and cultured vascular cells. , 1986, Science.

[12]  Axel Haverich,et al.  Tissue engineering of small diameter vascular grafts. , 2002, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[13]  N. Alpert,et al.  Altered Myocardial Force‐Frequency Relation in Human Heart Failure , 1992, Circulation.

[14]  Tal Dvir,et al.  Activation of the ERK1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly. , 2007, Tissue engineering.

[15]  George J Christ,et al.  Smooth muscle cell seeding of decellularized scaffolds: the importance of bioreactor preconditioning to development of a more native architecture for tissue-engineered blood vessels. , 2009, Tissue engineering. Part A.

[16]  Milica Radisic,et al.  Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Marie-Christine Herregods,et al.  Left ventricular strain and strain rate in a general population. , 2008, European heart journal.

[18]  R Langer,et al.  Functional arteries grown in vitro. , 1999, Science.

[19]  C V C Bouten,et al.  Substrates for cardiovascular tissue engineering. , 2011, Advanced drug delivery reviews.

[20]  Gordana Vunjak-Novakovic,et al.  Effects of oxygen on engineered cardiac muscle. , 2002, Biotechnology and bioengineering.

[21]  L. Field,et al.  Cardiomyocyte cell cycle regulation. , 2002, Circulation research.

[22]  Frédéric Couet,et al.  Fetal development, mechanobiology and optimal control processes can improve vascular tissue regeneration in bioreactors: an integrative review. , 2012, Medical engineering & physics.

[23]  Ryan M. Anderson,et al.  Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes , 2010, Nature.

[24]  R J Cohen,et al.  Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. , 1999, American journal of physiology. Heart and circulatory physiology.

[25]  D. Durand,et al.  Electric Stimulation of Excitable Tissue , 1999 .

[26]  Thomas Boudou,et al.  A microfabricated platform to measure and manipulate the mechanics of engineered cardiac microtissues. , 2012, Tissue engineering. Part A.

[27]  Ralf Pörtner,et al.  Bioreactor design for tissue engineering. , 2005, Journal of bioscience and bioengineering.

[28]  E. Olson,et al.  Transient Regenerative Potential of the Neonatal Mouse Heart , 2011, Science.

[29]  Mehmet Toner,et al.  An Outline of Cardiovascular Structure and Function , 2003 .

[30]  R. Shadwick,et al.  Mechanical design in arteries. , 1999, The Journal of experimental biology.

[31]  C. Breuer,et al.  Vascular tissue engineering: the next generation. , 2012, Trends in molecular medicine.

[32]  J. Leor,et al.  Cells, scaffolds, and molecules for myocardial tissue engineering. , 2005, Pharmacology & therapeutics.

[33]  Alexander M Seifalian,et al.  The use of animal models in developing the discipline of cardiovascular tissue engineering: a review. , 2004, Biomaterials.

[34]  Robert Zweigerdt,et al.  Suspension culture of human pluripotent stem cells in controlled, stirred bioreactors. , 2012, Tissue engineering. Part C, Methods.

[35]  Peter M. Vogt,et al.  Development of a Laminar Flow Bioreactor by Computational Fluid Dynamics , 2012 .

[36]  Thomas Eschenhagen,et al.  Three‐dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart muscle model system , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[37]  Jianwen Luo,et al.  Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue , 2012, Journal of tissue engineering and regenerative medicine.

[38]  Rei Ogawa,et al.  Vascular tissue engineering and vascularized 3D tissue regeneration. , 2007, Regenerative medicine.

[39]  Diego Mantovani,et al.  Bioreactors for tissue engineering: focus on mechanical constraints. A comparative review. , 2006, Tissue engineering.

[40]  P E McHugh,et al.  Endothelial cell response to biomechanical forces under simulated vascular loading conditions. , 2007, Journal of biomechanics.

[41]  E. Sparrow,et al.  Bioreactor for the reconstitution of a decellularized vascular matrix of biological origin , 2011 .

[42]  Peter W Zandstra,et al.  Engineered heart tissue model of diabetic myocardium. , 2011, Tissue engineering. Part A.

[43]  Margherita Cioffi,et al.  Potential and Bottlenecks of Bioreactors in 3D Cell Culture and Tissue Manufacturing , 2009, Advanced materials.

[44]  P. Doevendans,et al.  Transplantation of cells for cardiac repair. , 2003, Journal of the American College of Cardiology.

[45]  Kenneth R Chien,et al.  Towards regenerative therapy for cardiac disease , 2012, The Lancet.

[46]  Frédéric Couet,et al.  Design of a perfusion bioreactor specific to the regeneration of vascular tissues under mechanical stresses. , 2005, Artificial organs.

[47]  Yuichi Ueda,et al.  Novel pulse duplicating bioreactor system for tissue-engineered vascular construct. , 2004, Tissue engineering.

[48]  Joseph P Vacanti,et al.  Dynamic rotational seeding and cell culture system for vascular tube formation. , 2003, Tissue engineering.

[49]  S. Alper,et al.  Hemodynamic shear stress and its role in atherosclerosis. , 1999, JAMA.

[50]  Thomas Rau,et al.  Human Engineered Heart Tissue as a Versatile Tool in Basic Research and Preclinical Toxicology , 2011, PloS one.

[51]  F A Auger,et al.  A completely biological tissue‐engineered human blood vessel , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[52]  G. Burch [Cardiovascular diseases]. , 1956, Revista medica cubana.

[53]  G. Vunjak-Novakovic,et al.  Design of electrical stimulation bioreactors for cardiac tissue engineering , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[54]  David L Kaplan,et al.  Simple modular bioreactors for tissue engineering: a system for characterization of oxygen gradients, human mesenchymal stem cell differentiation, and prevascularization. , 2010, Tissue engineering. Part C, Methods.

[55]  Andreas Hess,et al.  Cardiac Grafting of Engineered Heart Tissue in Syngenic Rats , 2002, Circulation.

[56]  H. Mertsching,et al.  Bioreactor technology in cardiovascular tissue engineering. , 2009, Advances in biochemical engineering/biotechnology.

[57]  W. Desmet,et al.  Outcomes of patients with acute coronary syndromes who are treated with bivalirudin during PCI: An analysis from the REPLACE-2 trial , 2004 .

[58]  Nicola Elvassore,et al.  Micro-bioreactor array for controlling cellular microenvironments. , 2007, Lab on a chip.

[59]  F J Schoen,et al.  Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization. , 1999, Biotechnology and bioengineering.

[60]  Bart Meuris,et al.  Design of a new pulsatile bioreactor for tissue engineered aortic heart valve formation. , 2002, Artificial organs.

[61]  R. Nuccitelli,et al.  Endogenous ionic currents and DC electric fields in multicellular animal tissues. , 1992, Bioelectromagnetics.

[62]  Ivan Martin,et al.  Bioreactor-based roadmap for the translation of tissue engineering strategies into clinical products. , 2009, Trends in biotechnology.

[63]  Youngmee Jung,et al.  Three-dimensional electrospun poly(lactide-co-ɛ-caprolactone) for small-diameter vascular grafts. , 2012, Tissue engineering. Part A.

[64]  Gordana Vunjak-Novakovic,et al.  Perfusion seeding of channeled elastomeric scaffolds with myocytes and endothelial cells for cardiac tissue engineering , 2010, Biotechnology progress.

[65]  P. Doevendans,et al.  Stem cell therapy for ischemic heart disease. , 2003, Trends in molecular medicine.

[66]  P. Doevendans,et al.  Cardiomyocyte cell cycle activation improves cardiac function after myocardial infarction. , 2008, Cardiovascular research.

[67]  J. Vacanti,et al.  Mechanical dissociation of swine liver to produce organoid units for tissue engineering and in vitro disease modeling. , 2010, Artificial organs.

[68]  Milica Radisic,et al.  Challenges in cardiac tissue engineering. , 2010, Tissue engineering. Part B, Reviews.

[69]  Payam Akhyari,et al.  A novel miniaturized multimodal bioreactor for continuous in situ assessment of bioartificial cardiac tissue during stimulation and maturation. , 2011, Tissue engineering. Part C, Methods.

[70]  A Mantalaris,et al.  Computational modeling for the optimization of a cardiogenic 3D bioprocess of encapsulated embryonic stem cells , 2012, Biomechanics and modeling in mechanobiology.

[71]  Gerald D Buckberg,et al.  Basic science review: the helix and the heart. , 2002, The Journal of thoracic and cardiovascular surgery.

[72]  R Langer,et al.  Tissue engineering of functional cardiac muscle: molecular, structural, and electrophysiological studies. , 2001, American journal of physiology. Heart and circulatory physiology.

[73]  D. Mozaffarian,et al.  Executive summary: heart disease and stroke statistics--2012 update: a report from the American Heart Association. , 2012, Circulation.

[74]  B. Murphy,et al.  Mechanical characterization of a customized decellularized scaffold for vascular tissue engineering. , 2012, Journal of the mechanical behavior of biomedical materials.

[75]  L. Bačáková,et al.  Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery. , 2009, Physiological research.

[76]  Axel Haverich,et al.  The current status of heart transplantation and the development of "artificial heart systems". , 2009, Deutsches Arzteblatt international.

[77]  Jeffrey A. Paten,et al.  Design and performance of an optically accessible, low-volume, mechanobioreactor for long-term study of living constructs. , 2011, Tissue engineering. Part C, Methods.

[78]  M. Ruel,et al.  Cardiac Tissue Engineering , 2014, Methods in Molecular Biology.

[79]  Milica Radisic,et al.  Electrical stimulation systems for cardiac tissue engineering , 2009, Nature Protocols.

[80]  W. Zimmermann,et al.  3D engineered heart tissue for replacement therapy , 2002, Basic Research in Cardiology.

[81]  N. Fortuin,et al.  Determination of Left Ventricular Volumes by Ultrasound , 1971, Circulation.

[82]  R. Tuma,et al.  Relationship between microvascular blood velocity and pressure distribution. , 1977, The American journal of physiology.

[83]  N. Tandon,et al.  Optimization of electrical stimulation parameters for cardiac tissue engineering , 2011, Journal of tissue engineering and regenerative medicine.

[84]  S. M. Collins,et al.  Measurement of right ventricular volume using cine computed tomography. , 1987, Investigative Radiology.

[85]  Gordana Vunjak-Novakovic,et al.  Alignment and elongation of human adipose-derived stem cells in response to direct-current electrical stimulation , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[86]  Jacqueline T Johanas,et al.  Dynamic culture conditions to generate silk-based tissue-engineered vascular grafts. , 2009, Biomaterials.

[87]  J. Lüdemann,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. , 1998, Cardiovascular research.

[88]  Richard Archer,et al.  Why tissue engineering needs process engineering , 2005, Nature Biotechnology.

[89]  Michael S Kallos,et al.  New tissue dissociation protocol for scaled-up production of neural stem cells in suspension bioreactors. , 2004, Tissue engineering.

[90]  R. Sodian,et al.  Tissue engineering of small caliber vascular grafts. , 2001, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[91]  S. Louis,et al.  The Washington manual of surgery , 2013 .

[92]  Michael D Hill,et al.  Stenting versus endarterectomy for treatment of carotid-artery stenosis. , 2010, The New England journal of medicine.

[93]  Anthony Ratcliffe,et al.  Bioreactors and Bioprocessing for Tissue Engineering , 2002, Annals of the New York Academy of Sciences.

[94]  N. L'Heureux,et al.  Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. , 2009, Biomaterials.

[95]  C. Montero-Menei,et al.  Combining adult stem cells and polymeric devices for tissue engineering in infarcted myocardium. , 2012, Biomaterials.

[96]  F. O'Brien,et al.  Part 1: scaffolds and surfaces. , 2008, Technology and health care : official journal of the European Society for Engineering and Medicine.

[97]  L. Field Modulation of the Cardiomyocyte Cell Cycle in Genetically Altered Animals , 2004, Annals of the New York Academy of Sciences.

[98]  Timothy J Gardner,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). , 2004, Circulation.

[99]  D. Wendt,et al.  The role of bioreactors in tissue engineering. , 2004, Trends in biotechnology.

[100]  S R Gonda,et al.  Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. , 1999, Tissue engineering.

[101]  Artur Lichtenberg,et al.  Myocardial tissue engineering: the extracellular matrix. , 2008, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[102]  A R Boccaccini,et al.  Myocardial tissue engineering: a review , 2007, Journal of tissue engineering and regenerative medicine.

[103]  W. Zimmermann,et al.  Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. , 2000, Biotechnology and bioengineering.

[104]  Andreas Hess,et al.  Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts , 2006, Nature Medicine.

[105]  J. Patterson,et al.  Observations on the Circulation of Domestic Cattle , 1960, Circulation research.

[106]  Milica Radisic,et al.  High-density seeding of myocyte cells for cardiac tissue engineering. , 2003, Biotechnology and bioengineering.

[107]  Tal Dvir,et al.  Electric field stimulation integrated into perfusion bioreactor for cardiac tissue engineering. , 2010, Tissue engineering. Part C, Methods.

[108]  Yao Sun,et al.  Vascular endothelial growth factor (VEGF)-A: role on cardiac angiogenesis following myocardial infarction. , 2010, Microvascular research.

[109]  Elisa Figallo Advanced technologies for cardiac tissue engineering , 2008 .

[110]  S. Russell,et al.  Advanced heart failure treated with continuous-flow left ventricular assist device. , 2009, The New England journal of medicine.

[111]  A. Belker Principles of microsurgery. , 1994, The Urologic clinics of North America.

[112]  Milica Radisic,et al.  Cardiac tissue engineering using perfusion bioreactor systems , 2008, Nature Protocols.

[113]  Narutoshi Hibino,et al.  Successful application of tissue engineered vascular autografts: clinical experience. , 2003, Biomaterials.

[114]  W. P. Smotherman,et al.  Heart rate response of the rat fetus and neonate to a chemosensory stimulus , 1991, Physiology & Behavior.

[115]  Frédéric Couet,et al.  Optimization of Culture Conditions in a Bioreactor for Vascular Tissue Engineering Using a Mathematical Model of Vascular Growth and Remodeling , 2012 .

[116]  Aldo R Boccaccini,et al.  Myocardial tissue engineering. , 2008, British medical bulletin.

[117]  Chrysanthi Williams,et al.  Perfusion bioreactor for small diameter tissue-engineered arteries. , 2004, Tissue engineering.

[118]  Robert Plonsey,et al.  Electrical Stimulation of Excitable Tissue , 2000 .

[119]  D. Mozaffarian,et al.  Executive Summary: Heart Disease and Stroke Statistics—2015 Update A Report From the American Heart Association , 2011, Circulation.

[120]  R K Birla,et al.  Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle. , 2007, Tissue engineering.

[121]  Reto Luginbuehl,et al.  Tissue engineering - nanomaterials in the musculoskeletal system. , 2012, Swiss medical weekly.

[122]  Lior Gepstein,et al.  Controlling the Cellular Organization of Tissue‐Engineered Cardiac Constructs , 2004, Annals of the New York Academy of Sciences.

[123]  Farshid Guilak,et al.  Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. , 2006, Tissue engineering.

[124]  Bryan J. Pfister,et al.  Axon Stretch Growth: The Mechanotransduction of Neuronal Growth , 2011, Journal of visualized experiments : JoVE.

[125]  Rebecca Lyn Carrier Cardiac tissue engineering : bioreactor cultivation parameters , 1999 .

[126]  Smadar Cohen,et al.  Cardiac Tissue Engineering, Ex-Vivo: Design Principles in Biomaterials and Bioreactors , 2003, Heart Failure Reviews.

[127]  J. Ornato,et al.  ACC/AHA 2004 guideline update for coronary artery bypass graft surgery: summary article: 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). , 2004, Circulation.

[128]  Maria Paola Sassi,et al.  CARS and SHG microscopy to follow collagen production in living human corneal fibroblasts and mesenchymal stem cells in fibrin hydrogel 3D cultures , 2011, 1109.5907.

[129]  Stefan Wagner,et al.  Murine and human pluripotent stem cell-derived cardiac bodies form contractile myocardial tissue in vitro. , 2013, European heart journal.

[130]  M. Radisic,et al.  Pulsatile perfusion bioreactor for cardiac tissue engineering , 2008, Biotechnology progress.

[131]  M. Oz,et al.  Bridge experience with long-term implantable left ventricular assist devices. Are they an alternative to transplantation? , 1997, Circulation.

[132]  P. E. McHugh,et al.  Bioreactors for Cardiovascular Cell and Tissue Growth: A Review , 2003, Annals of Biomedical Engineering.

[133]  Lucie Germain,et al.  Mechanical properties of tissue-engineered vascular constructs produced using arterial or venous cells. , 2011, Tissue engineering. Part A.

[134]  Jeffrey T. Krawiec,et al.  Adult stem cell-based tissue engineered blood vessels: a review. , 2012, Biomaterials.

[135]  Carl E Butler,et al.  Principles of microsurgery , 2013 .

[136]  Federica Limana,et al.  Mobilized bone marrow cells repair the infarcted heart, improving function and survival , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[137]  Charles H. Thorne,et al.  Grabb and Smith's Plastic Surgery , 1991 .

[138]  W. Zimmermann,et al.  Tissue Engineering of a Differentiated Cardiac Muscle Construct , 2002, Circulation research.

[139]  P. McFetridge,et al.  Rolling the human amnion to engineer laminated vascular tissues. , 2012, Tissue engineering. Part C, Methods.

[140]  Robert Plonsey,et al.  An Outline of Cardiovascular Structure and Function , 2003 .