Advertisement

Delivery Modes for Cardiac Stem Cell Therapy

  • Neil Davies
  • Kyle Goetsch
  • Malebogo Ngoepe
  • Thomas Franz
  • Sandrine Lecour
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Stem cell delivery has received considerable attention as a potential therapy for myocardial infarction. However, therapeutic efficacy has been variable and modest in the clinical setting. One potential confounding factor is the poor cardiac retention and engraftment of the injected cells. The various delivery routes are considered with particular reference to their influence on engraftment. Further to that the potential of utilising injectable biomaterials as a strategy for optimizing retention is examined.

Keywords

Delivery Engraftement Biomaterials Intracoronary infusion Stem cell retention 

References

  1. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ (2004) Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110(21):3300–3305PubMedCrossRefGoogle Scholar
  2. Azene N, Fu Y, Maurer J, Kraitchman DL (2014) Tracking of stem cells in vivo for cardiovascular applications. J Cardiovasc Magn Reson 16:7PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bastings MM, Koudstaal S, Kieltyka RE, Nakano Y, Pape AC, Feyen DA et al (2014) A fast pH-switchable and self-healing supramolecular hydrogel carrier for guided, local catheter injection in the infarcted myocardium. Adv Healthc Mater 3(1):70–78PubMedCrossRefGoogle Scholar
  4. Bearzi C, Gargioli C, Baci D, Fortunato O, Shapira-Schweitzer K, Kossover O et al (2014) PlGF-MMP9-engineered iPS cells supported on a PEG-fibrinogen hydrogel scaffold possess an enhanced capacity to repair damaged myocardium. Cell Death Dis 5Google Scholar
  5. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S et al (2009) Evidence for cardiomyocyte renewal in humans. Science 324(5923):98–102PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bonios M, Terrovitis J, Chang CY, Engles JM, Higuchi T, Lautamaeki R et al (2011) Myocardial substrate and route of administration determine acute cardiac retention and lung bio-distribution of cardiosphere-derived cells. J Nucl Cardiol 18(3):443–450PubMedPubMedCentralCrossRefGoogle Scholar
  7. Boopathy AV, Che PL, Somasuntharam I, Fiore VF, Cabigas EB, Ban K et al (2014) The modulation of cardiac progenitor cell function by hydrogel-dependent Notch1 activation. Biomaterials 35(28):8103–8112PubMedPubMedCentralCrossRefGoogle Scholar
  8. Campbell NG, Suzuki K (2012) Cell Delivery routes for stem cell therapy to the heart: current and future approaches. J Cardiovasc Transl Res 5(5):713–726PubMedCrossRefGoogle Scholar
  9. Chang MY, Chang CH, Chen CH, Cheng B, Lin YD, Luo CY et al (2015) The time window for therapy with Peptide nanofibers combined with autologous bone marrow cells in pigs after acute myocardial infarction. PLoS One 10(3), e0115430PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chen CH, Wang SS, Wei EI, Chu TY, Hsieh PC (2013) Hyaluronan enhances bone marrow cell therapy for myocardial repair after infarction. Mol Ther 21(3):670–679PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chen IY, Wu JC (2013) Molecular imaging: the key to advancing cardiac stem cell therapy. Trends Cardiovasc Med 23(6):201–210PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cheng K, Blusztajn A, Shen D, Li T-S, Sun B, Galang G et al (2012) Functional performance of human cardiosphere-derived cells delivered in an in situ polymerizable hyaluronan-gelatin hydrogel. Biomaterials 33(21):5317–5324PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chenite A, Chaput C, Wang D, Combes C, Buschmann MD, Hoemann CD et al (2000) Novel injectable neutral solutions of chitosan form biodegradable gels in situ. Biomaterials 21(21):2155–2161PubMedCrossRefGoogle Scholar
  14. Christman KL, Fok HH, Sievers RE, Fang Q, Lee RJ (2004a) Fibrin glue alone and skeletal myoblasts in a fibrin scaffold preserve cardiac function after myocardial infarction. Tissue Eng 10(3–4):403–409PubMedCrossRefGoogle Scholar
  15. Christman KL, Vardanian AJ, Fang QZ, Sievers RE, Fok HH, Lee RJ (2004b) Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J Am Coll Cardiol 44(3):654–660PubMedCrossRefGoogle Scholar
  16. Clifford DM, Fisher SA, Brunskill SJ, Doree C, Mathur A, Watt S et al (2012) Stem cell treatment for acute myocardial infarction. Cochrane Database Syst Rev 2, CD006536Google Scholar
  17. Cui XJ, Xie H, Wang HJ, Guo HD, Zhang JK, Wang C et al (2010) Transplantation of mesenchymal stem cells with self-assembling polypeptide scaffolds is conducive to treating myocardial infarction in rats. Tohoku J Exp Med 222(4):281–289PubMedCrossRefGoogle Scholar
  18. Dai W, Hale SL, Kay GL, Jyrala AJ, Kloner RA (2009) Delivering stem cells to the heart in a collagen matrix reduces relocation of cells to other organs as assessed by nanoparticle technology. Regen Med 4(3):387–395PubMedPubMedCentralCrossRefGoogle Scholar
  19. Danoviz ME, Nakamuta JS, Marques FLN, dos Santos L, Alvarenga EC, dos Santos AA et al (2010) Rat adipose tissue-derived stem cells transplantation attenuates cardiac dysfunction post infarction and biopolymers enhance cell retention. PLoS One 5(8), e12077PubMedPubMedCentralCrossRefGoogle Scholar
  20. Davis ME, Hsieh PC, Takahashi T, Song Q, Zhang S, Kamm RD et al (2006) Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc Natl Acad Sci U S A 103(21):8155–8160PubMedPubMedCentralCrossRefGoogle Scholar
  21. de Jong R, Houtgraaf JH, Samiei S, Boersma E, Duckers HJ (2014) Intracoronary stem cell infusion after acute myocardial infarction: a meta-analysis and update on clinical trials. Circ Cardiovasc Interv 7(2):156–167PubMedCrossRefGoogle Scholar
  22. Dobner S, Bezuidenhout D, Govender P, Zilla P, Davies N (2009) A synthetic non-degradable polyethylene glycol hydrogel retards adverse post-infarct left ventricular remodeling. J Card Fail 15(7):629–636PubMedCrossRefGoogle Scholar
  23. Doyle B, Kemp BJ, Chareonthaitawee P, Reed C, Schmeckpeper J, Sorajja P et al (2007) Dynamic tracking during intracoronary injection of 18F-FDG-labeled progenitor cell therapy for acute myocardial infarction. J Nucl Med 48(10):1708–1714PubMedCrossRefGoogle Scholar
  24. Ehrbar M, Sala A, Lienemann P, Ranga A, Mosiewicz K, Bittermann A et al (2011) Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys J 100(2):284–293PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fisher SA, Doree C, Mathur A, Martin-Rendon E (2015) Meta-analysis of cell therapy trials for patients with heart failure. Circ Res 116(8):1361–1377PubMedCrossRefGoogle Scholar
  26. Frangogiannis NG (2006) The mechanistic basis of infarct healing. Antioxid Redox Signal 8(11–12):1907–1939PubMedCrossRefGoogle Scholar
  27. Frey N, Linke A, Suselbeck T, Muller-Ehmsen J, Vermeersch P, Schoors D et al (2014) Intracoronary delivery of injectable bioabsorbable scaffold (IK-5001) to treat left ventricular remodeling after ST-elevation myocardial infarction: a first-in-man study. Circ Cardiovasc Interv 7(6):806–812PubMedCrossRefGoogle Scholar
  28. Freyman T, Polin G, Osman H, Crary J, Lu M, Cheng L et al (2006) A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J 27(9):1114–1122PubMedCrossRefGoogle Scholar
  29. Furlani D, Ugurlucan M, Ong L, Bieback K, Pittermann E, Westien I et al (2009) Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvasc Res 77(3):370–376PubMedCrossRefGoogle Scholar
  30. George JC, Goldberg J, Joseph M, Abdulhameed N, Crist J, Das H et al (2008) Transvenous intramyocardial cellular delivery increases retention in comparison to intracoronary delivery in a porcine model of acute myocardial infarction. J Interv Cardiol 21(5):424–431PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gnecchi M, Zhang Z, Ni A, Dzau VJ (2008) Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 103(11):1204–1219PubMedPubMedCentralCrossRefGoogle Scholar
  32. Guo HD, Cui GH, Wang HJ, Tan YZ (2010) Transplantation of marrow-derived cardiac stem cells carried in designer self-assembling peptide nanofibers improves cardiac function after myocardial infarction. Biochem Biophys Res Commun 399(1):42–48PubMedCrossRefGoogle Scholar
  33. Gyongyosi M, Blanco J, Marian T, Tron L, Petnehazy O, Petrasi Z et al (2008) Serial noninvasive in vivo positron emission tomographic tracking of percutaneously intramyocardially injected autologous porcine mesenchymal stem cells modified for transgene reporter gene expression. Circ Cardiovasc Imaging 1(2):94–103PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gyongyosi M, Wojakowski W, Lemarchand P, Lunde K, Tendera M, Bartunek J et al (2015) Meta-analysis of Cell-based CaRdiac stUdiEs (ACCRUE) in patients with acute myocardial infarction based on individual patient data. Circ Res 116(8):1346–1360PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hale SL, Dai W, Dow JS, Kloner RA (2008) Mesenchymal stem cell administration at coronary artery reperfusion in the rat by two delivery routes: a quantitative assessment. Life Sci 83(13–14):511–515PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hofmann M, Wollert KC, Meyer GP, Menke A, Arseniev L, Hertenstein B et al (2005) Monitoring of bone marrow cell homing into the infarcted human myocardium. Circulation 111(17):2198–2202PubMedCrossRefGoogle Scholar
  37. Holmes JW, Borg TK, Covell JW (2005) Structure and mechanics of healing myocardial infarcts. Annu Rev Biomed Eng 7:223–253PubMedCrossRefGoogle Scholar
  38. Hong KU, Guo Y, Li QH, Cao P, Al-Maqtari T, Vajravelu BN et al (2014a) c-kit+ Cardiac stem cells alleviate post-myocardial infarction left ventricular dysfunction despite poor engraftment and negligible retention in the recipient heart. PLoS One 9(5), e96725PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hong SJ, Hou D, Brinton TJ, Johnstone B, Feng D, Rogers P et al (2014b) Intracoronary and retrograde coronary venous myocardial delivery of adipose-derived stem cells in swine infarction lead to transient myocardial trapping with predominant pulmonary redistribution. Catheter Cardiovasc Interv 83(1):E17–E25PubMedCrossRefGoogle Scholar
  40. Hou DM, Youssef EAS, Brinton TJ, Zhang P, Rogers P, Price ET et al (2005) Radiolabeled cell distribution after intramyocardial, intracoronary, and interstitial retrograde coronary venous delivery—Implications for current clinical trials. Circulation 112(9):I150–I156PubMedGoogle Scholar
  41. Ifkovits JL, Tous E, Minakawa M, Morita M, Robb JD, Koomalsingh KJ et al (2010) Injectable hydrogel properties influence infarct expansion and extent of postinfarction left ventricular remodeling in an ovine model. Proc Natl Acad Sci U S A 107(25):11507–11512PubMedPubMedCentralCrossRefGoogle Scholar
  42. Jiang XJ, Wang T, Li XY, Wu DQ, Zheng ZB, Zhang JF et al (2009) Injection of a novel synthetic hydrogel preserves left ventricle function after myocardial infarction. J Biomed Mater Res A 90(2):472–477PubMedCrossRefGoogle Scholar
  43. Kadner K, Dobner S, Franz T, Bezuidenhout D, Sirry MS, Zilla P et al (2012) The beneficial effects of deferred delivery on the efficiency of hydrogel therapy post myocardial infarction. Biomaterials 33(7):2060–2066PubMedCrossRefGoogle Scholar
  44. Kang WJ, Kang HJ, Kim HS, Chung JK, Lee MC, Lee DS (2006) Tissue distribution of 18F-FDG-labeled peripheral hematopoietic stem cells after intracoronary administration in patients with myocardial infarction. J Nucl Med 47(8):1295–1301PubMedGoogle Scholar
  45. Kharlamov AN, Duckers HJ, van Beusekom HM, Smits PC, Perin EC, Serruys PW (2013) Do we have a future with transcatheter adventitial delivery of stem cells? Int J Cardiol 165(2):217–221PubMedCrossRefGoogle Scholar
  46. Klein HM, Ghodsizad A, Marktanner R, Poll L, Voelkel T, Mohammad Hasani MR et al (2007) Intramyocardial implantation of CD133+ stem cells improved cardiac function without bypass surgery. Heart Surg Forum 10(1):E66–E69PubMedCrossRefGoogle Scholar
  47. Kraehenbuehl TP, Ferreira LS, Hayward AM, Nahrendorf M, van der Vlies AJ, Vasile E et al (2011) Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 32(4):1102–1109PubMedCrossRefGoogle Scholar
  48. Kraitchman DL, Tatsumi M, Gilson WD, Ishimori T, Kedziorek D, Walczak P et al (2005) Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 112(10):1451–1461PubMedPubMedCentralCrossRefGoogle Scholar
  49. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK et al (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25(9):1015–1024PubMedCrossRefGoogle Scholar
  50. Landa N, Miller L, Feinberg MS, Holbova R, Shachar M, Freeman I et al (2008) Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117(11):1388–1396PubMedCrossRefGoogle Scholar
  51. Lee LC, Wall ST, Klepach D, Ge L, Zhang Z, Lee RJ et al (2013) Algisyl-LVR with coronary artery bypass grafting reduces left ventricular wall stress and improves function in the failing human heart. Int J Cardiol 168(3):2022–2028PubMedPubMedCentralCrossRefGoogle Scholar
  52. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL et al (2009) Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5(1):54–63PubMedPubMedCentralCrossRefGoogle Scholar
  53. Leor J, Tuvia S, Guetta V, Manczur F, Castel D, Willenz U et al (2009) Intracoronary injection of in situ forming alginate hydrogel reverses left ventricular remodeling after myocardial infarction in Swine. J Am Coll Cardiol 54(11):1014–1023PubMedCrossRefGoogle Scholar
  54. Lepperhof V, Polchynski O, Kruttwig K, Bruggemann C, Neef K, Drey F et al (2014) Bioluminescent imaging of genetically selected induced pluripotent stem cell-derived cardiomyocytes after transplantation into infarcted heart of syngeneic recipients. PLoS One 9(9), e107363PubMedPubMedCentralCrossRefGoogle Scholar
  55. Li S-H, Lai TYY, Sun Z, Han M, Moriyama E, Wilson B et al (2009) Tracking cardiac engraftment and distribution of implanted bone marrow cells: comparing intra-aortic, intravenous, and intramyocardial delivery. J Thorac Cardiovasc Surg 137(5):1225–1233PubMedCrossRefGoogle Scholar
  56. Li X, Zhou J, Liu Z, Chen J, Lu S, Sun H et al (2014) A PNIPAAm-based thermosensitive hydrogel containing SWCNTs for stem cell transplantation in myocardial repair. Biomaterials 35(22):5679–5688PubMedCrossRefGoogle Scholar
  57. Li Y, Yao Y, Sheng Z, Yang Y, Ma G (2011) Dual-modal tracking of transplanted mesenchymal stem cells after myocardial infarction. Int J Nanomedicine 6:815–823PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lin Y-D, Yeh M-L, Yang Y-J, Tsai D-C, Chu T-Y, Shih Y-Y et al (2010) Intramyocardial peptide nanofiber injection improves postinfarction ventricular remodeling and efficacy of bone marrow cell therapy in pigs. Circulation 122(11):S132–S141PubMedCrossRefGoogle Scholar
  59. Liu J, Narsinh KH, Lan F, Wang L, Nguyen PK, Hu S et al (2012a) Early stem cell engraftment predicts late cardiac functional recovery: preclinical insights from molecular imaging. Circ Cardiovasc Imaging 5(4):481–490PubMedPubMedCentralCrossRefGoogle Scholar
  60. Liu Z, Wang H, Wang Y, Lin Q, Yao A, Cao F et al (2012b) The influence of chitosan hydrogel on stem cell engraftment, survival and homing in the ischemic myocardial microenvironment. Biomaterials 33(11):3093–3106PubMedCrossRefGoogle Scholar
  61. Lu S, Wang H, Lu W, Liu S, Lin Q, Li D et al (2010) Both the transplantation of somatic cell nuclear transfer- and fertilization-derived mouse embryonic stem cells with temperature-responsive chitosan hydrogel improve myocardial performance in infarcted rat hearts. Tissue Eng Part A 16(4):1303–1315PubMedCrossRefGoogle Scholar
  62. Lu WN, Lu SH, Wang HB, Li DX, Duan CM, Liu ZQ et al (2009) Functional improvement of infarcted heart by co-injection of embryonic stem cells with temperature-responsive chitosan hydrogel. Tissue Eng Part A 15(6):1437–1447PubMedCrossRefGoogle Scholar
  63. Luna SM, Silva SS, Gomes ME, Mano JF, Reis RL (2011) Cell adhesion and proliferation onto chitosan-based membranes treated by plasma surface modification. J Biomater Appl 26(1):101–116PubMedCrossRefGoogle Scholar
  64. Mitchell AJ, Sabondjian E, Sykes J, Deans L, Zhu W, Lu X et al (2010) Comparison of initial cell retention and clearance kinetics after subendocardial or subepicardial injections of endothelial progenitor cells in a canine myocardial infarction model. J Nucl Med 51(3):413–417PubMedCrossRefGoogle Scholar
  65. Muller-Ehmsen J, Krausgrill B, Burst V, Schenk K, Neisen UC, Fries JW et al (2006) Effective engraftment but poor mid-term persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. J Mol Cell Cardiol 41(5):876–884PubMedCrossRefGoogle Scholar
  66. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M et al (2004) Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428(6983):664–668PubMedCrossRefGoogle Scholar
  67. Nakamuta JS, Danoviz ME, Marques FLN, dos Santos L, Becker C, Goncalves GA et al (2009) Cell therapy attenuates cardiac dysfunction post myocardial infarction: effect of timing, routes of injection and a fibrin scaffold. PLoS One 4(6), e6005PubMedPubMedCentralCrossRefGoogle Scholar
  68. Nelson DM, Ma Z, Fujimoto KL, Hashizume R, Wagner WR (2011) Intra-myocardial biomaterial injection therapy in the treatment of heart failure: materials, outcomes and challenges. Acta Biomater 7(1):1–15PubMedCrossRefGoogle Scholar
  69. Opie LH, Commerford PJ, Gersh BJ, Pfeffer MA (2006) Controversies in ventricular remodelling. Lancet 367(9507):356–367PubMedCrossRefGoogle Scholar
  70. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B et al (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701–705PubMedCrossRefGoogle Scholar
  71. Padin-Iruegas ME, Misao Y, Davis ME, Segers VF, Esposito G, Tokunou T et al (2009) Cardiac progenitor cells and biotinylated insulin-like growth factor-1 nanofibers improve endogenous and exogenous myocardial regeneration after infarction. Circulation 120(10):876–887PubMedPubMedCentralCrossRefGoogle Scholar
  72. Panda NC, Zuckerman ST, Mesubi OO, Rosenbaum DS, Penn MS, Donahue JK et al (2014) Improved conduction and increased cell retention in healed MI using mesenchymal stem cells suspended in alginate hydrogel. J Interv Card Electrophysiol 41(2):117–127PubMedCrossRefGoogle Scholar
  73. Pek YS, Wan AC, Ying JY (2010) The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31(3):385–391PubMedCrossRefGoogle Scholar
  74. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT et al (2003) Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 107(18):2294–2302PubMedCrossRefGoogle Scholar
  75. Perin EC, Tian M, Marini FC 3rd, Silva GV, Zheng Y, Baimbridge F et al (2011) Imaging long-term fate of intramyocardially implanted mesenchymal stem cells in a porcine myocardial infarction model. PLoS One 6(9), e22949PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pompilio G, Steinhoff G, Liebold A, Pesce M, Alamanni F, Capogrossi MC et al (2008) Direct minimally invasive intramyocardial injection of bone marrow-derived AC133+ stem cells in patients with refractory ischemia: preliminary results. Thorac Cardiovasc Surg 56(2):71–76PubMedCrossRefGoogle Scholar
  77. Radisic M, Christman KL (2013) Materials science and tissue engineering: repairing the heart. Mayo Clin Proc 88(8):884–898PubMedPubMedCentralCrossRefGoogle Scholar
  78. Rane AA, Chuang JS, Shah A, Hu DP, Dalton ND, Gu Y et al (2011) Increased infarct wall thickness by a bio-inert material is insufficient to prevent negative left ventricular remodeling after myocardial infarction. PLoS One 6(6), e21571PubMedPubMedCentralCrossRefGoogle Scholar
  79. Ransohoff KJ, Wu JC (2010) Advances in cardiovascular molecular imaging for tracking stem cell therapy. Thromb Haemost 104(1):13–22PubMedPubMedCentralCrossRefGoogle Scholar
  80. Sanganalmath SK, Bolli R (2013) Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res 113(6):810–834PubMedPubMedCentralCrossRefGoogle Scholar
  81. Schachinger V, Aicher A, Dobert N, Rover R, Diener J, Fichtlscherer S et al (2008) Pilot trial on determinants of progenitor cell recruitment to the infarcted human myocardium. Circulation 118(14):1425–1432PubMedCrossRefGoogle Scholar
  82. Seif-Naraghi SB, Singelyn JM, Salvatore MA, Osborn KG, Wang JJ, Sampat U et al (2013) Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med 5(173):173ra25PubMedCrossRefGoogle Scholar
  83. Senyo SE, Steinhauser ML, Pizzimenti CL, Yang VK, Cai L, Wang M et al (2013) Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493(7432):433–436PubMedCrossRefGoogle Scholar
  84. Sheikh AY, Lin SA, Cao F, Cao Y, van der Bogt KE, Chu P et al (2007) Molecular imaging of bone marrow mononuclear cell homing and engraftment in ischemic myocardium. Stem Cells 25(10):2677–2684PubMedPubMedCentralCrossRefGoogle Scholar
  85. Shen D, Cheng K, Marban E (2012) Dose-dependent functional benefit of human cardiosphere transplantation in mice with acute myocardial infarction. J Cell Mol Med 16(9):2112–2116PubMedPubMedCentralCrossRefGoogle Scholar
  86. Silva SA, Sousa AL, Haddad AF, Azevedo JC, Soares VE, Peixoto CM et al (2009) Autologous bone-marrow mononuclear cell transplantation after acute myocardial infarction: comparison of two delivery techniques. Cell Transplant 18(3):343–352PubMedCrossRefGoogle Scholar
  87. Siminiak T, Fiszer D, Jerzykowska O, Grygielska B, Rozwadowska N, Kalmucki P et al (2005) Percutaneous trans-coronary-venous transplantation of autologous skeletal myoblasts in the treatment of post-infarction myocardial contractility impairment: the POZNAN trial. Eur Heart J 26(12):1188–1195PubMedCrossRefGoogle Scholar
  88. Singelyn JM, Sundaramurthy P, Johnson TD, Schup-Magoffin PJ, Hu DP, Faulk DM et al (2012) Catheter-deliverable hydrogel derived from decellularized ventricular extracellular matrix increases endogenous cardiomyocytes and preserves cardiac function post-myocardial infarction. J Am Coll Cardiol 59(8):751–763PubMedPubMedCentralCrossRefGoogle Scholar
  89. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E et al (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7):896–908PubMedCrossRefGoogle Scholar
  90. Strauer BE, Steinhoff G (2011) 10 years of intracoronary and intramyocardial bone marrow stem cell therapy of the heart: from the methodological origin to clinical practice. J Am Coll Cardiol 58(11):1095–1104PubMedCrossRefGoogle Scholar
  91. Sutton MG, Sharpe N (2000) Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101(25):2981–2988PubMedCrossRefGoogle Scholar
  92. Swijnenburg R-J, Govaert JA, van der Bogt KEA, Pearl JI, Huang M, Stein W et al (2010) Timing of bone marrow cell delivery has minimal effects on cell viability and cardiac recovery after myocardial infarction. Circ Cardiovasc Imaging 3(1):77–85PubMedCrossRefGoogle Scholar
  93. Templin C, Zweigerdt R, Schwanke K, Olmer R, Ghadri JR, Emmert MY et al (2012) Transplantation and tracking of human-induced pluripotent stem cells in a pig model of myocardial infarction: assessment of cell survival, engraftment, and distribution by hybrid single photon emission computed tomography/computed tomography of sodium iodide symporter transgene expression. Circulation 126(4):430–439PubMedCrossRefGoogle Scholar
  94. Terrovitis J, Lautamaeki R, Bonios M, Fox J, Engles JM, Yu J et al (2009) Noninvasive quantification and optimization of acute cell retention by in vivo positron emission tomography after intramyocardial cardiac-derived stem cell delivery. J Am Coll Cardiol 54(17):1619–1626PubMedPubMedCentralCrossRefGoogle Scholar
  95. Tossios P, Krausgrill B, Schmidt M, Fischer T, Halbach M, Fries JWU et al (2008) Role of balloon occlusion for mononuclear bone marrow cell deposition after intracoronary injection in pigs with reperfused myocardial infarction. Eur Heart J 29(15):1911–1921PubMedCrossRefGoogle Scholar
  96. Vulliet PR, Greeley M, Halloran SM, MacDonald KA, Kittleson MD (2004) Intra-coronary arterial injection of mesenchymal stromal cells and microinfarction in dogs. Lancet 363(9411):783–784PubMedCrossRefGoogle Scholar
  97. Wall ST, Walker JC, Healy KE, Ratcliffe MB, Guccione JM (2006) Theoretical impact of the injection of material into the myocardium: a finite element model simulation. Circulation 114(24):2627–2635PubMedCrossRefGoogle Scholar
  98. Wang H, Liu Z, Li D, Guo X, Kasper FK, Duan C et al (2012) Injectable biodegradable hydrogels for embryonic stem cell transplantation: improved cardiac remodelling and function of myocardial infarction. J Cell Mol Med 16(6):1310–1320PubMedPubMedCentralCrossRefGoogle Scholar
  99. Wang T, Jiang XJ, Tang QZ, Li XY, Lin T, Wu DQ et al (2009) Bone marrow stem cells implantation with alpha-cyclodextrin/MPEG-PCL-MPEG hydrogel improves cardiac function after myocardial infarction. Acta Biomater 5(8):2939–2944PubMedCrossRefGoogle Scholar
  100. Wenk JF, Wall ST, Peterson RC, Helgerson SL, Sabbah HN, Burger M et al (2009) A method for automatically optimizing medical devices for treating heart failure: designing polymeric injection patterns. J Biomech Eng 131(12):121011PubMedCrossRefGoogle Scholar
  101. Westrich J, Yaeger P, He C, Stewart J, Chen R, Seleznik G et al (2010) Factors affecting residence time of mesenchymal stromal cells (MSC) injected into the myocardium. Cell Transplant 19(8):937–948PubMedCrossRefGoogle Scholar
  102. Yang JJ, Liu ZQ, Zhang JM, Wang HB, Hu SY, Liu JF et al (2013) Real-time tracking of adipose tissue-derived stem cells with injectable scaffolds in the infarcted heart. Heart Vessels 28(3):385–396PubMedCrossRefGoogle Scholar
  103. Zhang G, Hu Q, Braunlin EA, Suggs LJ, Zhang J (2008) Enhancing efficacy of stem cell transplantation to the heart with a PEGylated fibrin biomatrix. Tissue Eng Part A 14(6):1025–1036PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Neil Davies
    • 1
  • Kyle Goetsch
    • 1
  • Malebogo Ngoepe
    • 2
  • Thomas Franz
    • 3
  • Sandrine Lecour
    • 4
  1. 1.Cardiovascular Research Unit, Department of Surgery, Faculty of Health SciencesUniversity of Cape TownObservatorySouth Africa
  2. 2.Department of Mechanical EngineeringUniversity of Cape TownRondeboschSouth Africa
  3. 3.Division of Biomedical Engineering, Department of Human Biology, Faculty of Health SciencesUniversity of Cape TownObservatorySouth Africa
  4. 4.Cardioprotection Group, Hatter Institute for Cardiovascular Research in Africa and MRC Inter-University Cape Heart Group, Faculty of Health SciencesUniversity of Cape TownObservatorySouth Africa

Personalised recommendations