Advertisement

Cardiac support device (ASD) delivers bone marrow stem cells repetitively to epicardium has promising curative effects in advanced heart failure

  • Shizhong Yue
  • Muhammad Naveed
  • Wang Gang
  • Dingding Chen
  • Zhijie Wang
  • Feng Yu
  • Xiaohui Zhou
Article

Abstract

Ventricular restraint therapy is a non-transplant surgical option for the management of advanced heart failure (HF). To augment the therapeutic applications, it is hypothesized that ASD shows remarkable capabilities not only in delivering stem cells but also in dilated ventricles. Male SD rats were divided into four groups (n = 6): normal, HF, HF + ASD, and HF + ASD-BMSCs respectively. HF was developed by left anterior descending (LAD) coronary artery ligation in all groups except normal group. Post-infarcted electrocardiography (ECG) and brain natriuretic peptide (BNP) showed abnormal heart function in all model groups and HF + ASD-BMSCs group showed significant improvement as compared to other HF, HF + ASD groups on day 30. Masson’s trichrome staining was used to study the histology, and a large blue fibrotic area has been observed in HF and HF + ASD groups and quantification of fibrosis was assessed. ASD-treated rats showed normal heart rhythm, demonstrated by smooth -ST and asymmetrical T-wave. The mechanical function of the heart such as left ventricular systolic pressure (LVSP), left ventricular end-diastolic pressure (LVEDP) and heart rate was brought to normal when treated with ASD-BMSCs. This effect was more prominent than that of ASD therapy alone. In comparison to HF group, the SD rats in HF + ASD-BMBCs group showed a significant decline in BNP levels. So ASD can deliver BMSCs to the cardiomyocytes successfully and broaden the therapeutic efficacy, in comparison to the restraint device alone. An effective methodology to manage the end-stage HF has been proved.

Keywords

Heart failure Myocardial remodeling; Bone marrow stem cells ASD device Cardiac support device Ventricular restraint therapy 

Notes

Acknowledgments

This work was supported by the National Found for Fostering Talents of Basic Science (NFFTBS), [grant number J1030830]. We are grateful to Dr. Michael Deininger (Medical innovation center, University of Michigan, USA) for his encouraging and supporting role for this research. We are highly thankful to Mr. Muhammad Karim Ahmed from CRI for critically reviewing the text of this paper.

Compliance with ethical standards

Conflict of interest

All the authors declare that there is no conflict of interest. All the authors read and approved the manuscript.

References

  1. E. Alskaf, A. Tridente, A. Al-Mohammad, Tolvaptan for heart failure, systematic review and meta-analysis of trials. J. Cardiovasc. Pharmacol. 68(3), 196–203 (2016)Google Scholar
  2. J. Andrew, P. Macdonald, Latest developments in heart transplantation: a review. Clin. Ther. 37, 2234–2241 (2015)CrossRefGoogle Scholar
  3. D.D. Ascheim, A.C. Gelijns, D. Goldstein, L.A. Moye, N. Smedira, S. Lee, C.T. Klodell, A. Szady, M.K. Parides, N.O. Jeffries, Mesenchymal precursor cells as adjunctive therapy in recipients of contemporary left ventricular assist devices. Circulation 129, 2287 (2014)CrossRefGoogle Scholar
  4. P. Atluri, M.A. Acker, Diastolic ventricular support with cardiac support devices: an alternative approach to prevent adverse ventricular remodeling. Heart Fail. Rev. 18, 55–63 (2013)CrossRefGoogle Scholar
  5. D.L. Bernik, Silicon based materials for drug delivery devices and implants. Recent Pat. Nanotechnol. 1, 186 (2007)CrossRefGoogle Scholar
  6. S. Bialik, D.L. Geenen, I.E. Sasson, R. Cheng, J.W. Horner, S.M. Evans, E.M. Lord, C.J. Koch, R.N. Kitsis, Myocyte apoptosis during acute myocardial infarction in the mouse localizes to hypoxic regions but occurs independently of p53. J. Clin. Invest. 100, 1363–1372 (1997)CrossRefGoogle Scholar
  7. J.C. Bilgimol, S. Ragupathi, L. Vengadassalapathy, N.S. Senthil, K. Selvakumar, M. Ganesan, S.R. Manjunath, Stem cells: an eventual treatment option for heart diseases. World J. Stem Cells 7, 1118–1126 (2015)CrossRefGoogle Scholar
  8. K. Cheng, A. Blusztajn, D. Shen, T.S. Li, B. Sun, G. Galang, T.I. Zarembinski, G.D. Prestwich, E. Marban, R.R. Smith, L. Marban, Functional performance of human cardiosphere-derived cells delivered in an in situ polymerizable hyaluronan-gelatin hydrogel. Biomaterials 33, 5317–5324 (2012)CrossRefGoogle Scholar
  9. A. Chrastina, P. Pokreisz, J.E. Schnitzer, Experimental model of transthoracic, vascular-targeted, photodynamically induced myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 306, H270–H278 (2014)CrossRefGoogle Scholar
  10. G. Cotter, M. Metra, B.D. Weatherley, H.C. Dittrich, B.M. Massie, P. Ponikowski, D.M. Bloomfield, C.M. O’Connor, Physician-determined worsening heart failure: a novel definition for early worsening heart failure in patients hospitalized for acute heart failure – association with signs and symptoms, hospitalization duration, and 60-day outcomes. Cardiology 115, 29–36 (2010)CrossRefGoogle Scholar
  11. D. Geft, S. Schwartzenberg, O. Rogowsky, A. Finkelstein, J. Ablin, S. Mayselauslender, D. Wexler, G. Keren, J. George, Circulating Apoptotic Progenitor Cells in Patients with Congestive Heart Failure. PLoS One 3, 3238 (2008)CrossRefGoogle Scholar
  12. L. Danilowicz-Szymanowicz, J. Suchecka, A. Niemirycz-Makurat, K. Rozwadowska, G. Raczak, Autonomic predictors of hospitalization due to heart failure decompensation in patients with left ventricular systolic dysfunction. PLoS One 11, e0152372 (2016)CrossRefGoogle Scholar
  13. A.M. de Jong, I.C. van Gelder, I. Vreeswijk-Baudoin, M.V. Cannon, W.H. van Gilst, A.H. Maass, Atrial remodeling is directly related to end-diastolic left ventricular pressure in a mouse model of ventricular pressure overload. PLoS One 8, 633–641 (2013)Google Scholar
  14. P. Donndorf, G. Kundt, A. Kaminski, C. Yerebakan, A. Liebold, G. Steinhoff, A. Glass, Intramyocardial bone marrow stem cell transplantation during coronary artery bypass surgery: a meta-analysis. J. Thorac. Cardiovasc. Surg. 142, 911 (2011)CrossRefGoogle Scholar
  15. V.M. Dragojevic-Simic, S.L. Dobric, D.R. Bokonjic, Z.M. Vucinic, S.M. Sinovec, V.M. Jacevic, N.P. Dogovic, Amifostine protection against doxorubicin cardiotoxicity in rats. Anti-Cancer Drugs 15, 169–178 (2004)CrossRefGoogle Scholar
  16. S.M. Eleawa, M. Alkhateeb, S. Ghosh, F. Alhashem, A.S. Shatoor, A. Alhejaily, M.A. Khalil, Coenzyme Q10 protects against acute consequences of experimental myocardial infarction in rats. Int. J. Physiol Pathophysiol. Pharmacol. 7, 1–13 (2015)Google Scholar
  17. R. Fazan Jr., C.A. Silva, J.A. Oliveira, H.C. Salgado, N. Montano, N. Garcia-Cairasco, Evaluation of cardiovascular risk factors in the Wistar Audiogenic Rat (WAR) Strain. PLoS One 10, e0129574 (2015)CrossRefGoogle Scholar
  18. I. Fernandez-Ruiz, Stem cells: cell therapy improves outcomes in heart failure. Nat. Rev. Cardiol. 13(6), 311 (2016)Google Scholar
  19. S.A. Fisher, C. Doree, S.J. Brunskill, A. Mathur, E. Martin-Rendon, Bone marrow stem cell treatment for ischemic heart disease in patients with no option of revascularization: a systematic review and meta-analysis. PLoS One 8, e64669 (2013)CrossRefGoogle Scholar
  20. G.S. Francis, Extracardiac features of heart failure: catecholamines and hormonal changes. Cardiology 75(suppl 1), 19–29 (1988)CrossRefGoogle Scholar
  21. R.K. Ghanta, A. Rangaraj, R. Umakanthan, L. Lee, R.G. Laurence, J.A. Fox, R.M. Bolman III, L.H. Cohn, F.Y. Chen, Adjustable, physiological ventricular restraint improves left ventricular mechanics and reduces dilatation in an ovine model of chronic heart failure. Circulation 115, 1201–1210 (2007)Google Scholar
  22. L. Gullestad, T. Ueland, L.E. Vinge, A. Finsen, A. Yndestad, P. Aukrust, Inflammatory cytokines in heart failure: mediators and markers. Cardiology 122, 23–35 (2012)CrossRefGoogle Scholar
  23. O. Ishida, I. Hagino, N. Nagaya, T. Shimizu, T. Okano, Y. Sawa, H. Mori, T. Yagihara, Adipose-derived stem cell sheet transplantation therapy in a porcine model of chronic heart failure. Transl. Res. 165, 631–639 (2015)CrossRefGoogle Scholar
  24. H. Jaganathan, B. Godin, Biocompatibility assessment of Si-based nano- and micro-particles. Adv. Drug Deliv. Rev. 64, 1800–1819 (2012)CrossRefGoogle Scholar
  25. V. Jeevanantham, M. Butler, A. Saad, A. Abdel-Latif, E.K. Zuba-Surma, B. Dawn, Adult bone marrow cell therapy improves survival and induces long-term improvement in cardiac parameters: a systematic review and meta-analysis. Circulation 126, 551–568 (2012)CrossRefGoogle Scholar
  26. P. Karlström, P. Johansson, U. Dahlström, K. Boman, U. Alehagen, Can BNP-guided therapy improve health-related quality of life, and do responders to BNP-guided heart failure treatment have improved health-related quality of life? Results from the UPSTEP study. BMC Cardiovasc. Disord. 16, 1–10 (2016)CrossRefGoogle Scholar
  27. T. Kawasaki, C. Sakai, K. Harimoto, M. Yamano, S. Miki, T. Kamitani, H. Sugihara, Holter monitoring and long-term prognosis in hypertrophic cardiomyopathy. Cardiology 122, 44–54 (2012)CrossRefGoogle Scholar
  28. N.K. Khan, K.M. Goode, J.G. Cleland, A.S. Rigby, N. Freemantle, J. Eastaugh, A.L. Clark, R. de Silva, M.J. Calvert, K. Swedberg, M. Komajda, V. Mareev, F. Follath, Prevalence of ECG abnormalities in an international survey of patients with suspected or confirmed heart failure at death or discharge. Eur. J. Heart Fail. 9, 491–501 (2007)CrossRefGoogle Scholar
  29. P. Konopelski, M. Ufnal, Electrocardiography in rats: a comparison to human. Physiol. Res. 65, 717–725 (2016)Google Scholar
  30. K.J. Koomalsingh, W.R. Witschey, J.R. Mcgarvey, T. Shuto, N. Kondo, C. Xu, B.M. Jackson, J.H. Gorman 3rd, R.C. Gorman, J.J. Pilla, Optimized local infarct restraint improves left ventricular function and limits remodeling. Ann. Thorac. Surg. 95, 155–162 (2013)CrossRefGoogle Scholar
  31. Y. Kubota, S. Miyagawa, S. Fukushima, A. Saito, H. Watabe, T. Daimon, Y. Sakai, T. Akita, Y. Sawa, Impact of cardiac support device combined with slow-release prostacyclin agonist in a canine ischemic cardiomyopathy model. J. Thorac. Cardiovasc. Surg. 147, 1081–1087 (2014)CrossRefGoogle Scholar
  32. K.J. Lavine, M. Sintek, E. Novak, G. Ewald, E. Geltman, S. Joseph, J. Pfeifer, D.L. Mann, Coronary collaterals predict improved survival and allograft function in patients with coronary allograft vasculopathy. J. Heart Lung Transplant. 32, S27–S27 (2013)CrossRefGoogle Scholar
  33. J. Li, S. Umar, M. Amjedi, A. Iorga, S. Sharma, R.D. Nadadur, V. Regitz-Zagrosek, M. Eghbali, New frontiers in heart hypertrophy during pregnancy. Am. J. Cardiovasc. Dis. 2, 192–207 (2012)Google Scholar
  34. F. Limana, M.C. Capogrossi, A. Germani, The epicardium in cardiac repair: from the stem cell view. Pharmacol. Ther. 129, 82–96 (2011)CrossRefGoogle Scholar
  35. S.I. Lok, N. de Jonge, J. van Kuik, A.J. van Geffen, M.M. Huibers, P. van der Weide, E. Siera, B. Winkens, P.A. Doevendans, R.A. de Weger, P.A. da Costa Martins, MicroRNA expression in myocardial tissue and plasma of patients with end-stage heart failure during LVAD support: comparison of continuous and pulsatile devices. PLoS One 10, e0136404 (2015)CrossRefGoogle Scholar
  36. J.A. Magovern, Experimental and clinical studies with the Paracor cardiac restraint device. Semin. Thorac. Cardiovasc. Surg. 17, 364–368 (2005)CrossRefGoogle Scholar
  37. M. Malatesta, Histological and histochemical methods-theory and practice. Eur. J. Histochem. 60, 2639 (2016)Google Scholar
  38. R.E. Michler, Stem cell therapy for heart failure. Cardiol. Rev. 22, 105–116 (2014)CrossRefGoogle Scholar
  39. O. Miro, F.W. Peacock, J.J. McMurray, H. Bueno, M. Christ, A.S. Maisel, L. Cullen, M.R. Cowie, S. Di Somma, F.J. Martin Sanchez, E. Platz, J. Masip, U. Zeymer, C. Vrints, S. Price, A. Mebazaa, C. Mueller European society of cardiology-acute cardiovascular care association position paper on safe discharge of acute heart failure patients from the emergency department. Eur. Heart J. Acute Cardiovasc. Care 6(4), 311 (2016)Google Scholar
  40. M. Naveed, I.S. Mohammad, L. Xue, S. Khan, W. Gang, Y. Cao, Y. Cheng, X. Cui, C. Dingding, Y. Feng, W. Zhijie, Z. Xiaohui, The promising future of ventricular restraint therapy for the management of end-stage heart failure. Biomed Pharmacother 99, 25–32 (2018)CrossRefGoogle Scholar
  41. M. Naveed, L. Wenhua, W. Gang, I.S. Mohammad, M. Abbas, X. Liao, M. Yang, L. Zhang, X. Liu, X. Qi, Y. Chen, L. Jiadi, L. Ye, W. Zhijie, C.D. Ding, Y. Feng, Z. Xiaohui, A novel ventricular restraint device (ASD) repetitively deliver Salvia miltiorrhiza to epicardium have good curative effects in heart failure management. Biomed Pharmacother 95, 701–710 (2017)CrossRefGoogle Scholar
  42. G.H. Oliveira, S.G. Al-Kindi, H.G. Bezerra, M.A. Costa, Left ventricular restoration devices. J. Cardiovasc. Transl. Res. 7, 282–291 (2014)CrossRefGoogle Scholar
  43. A.M. Orogo, Å.B. Gustafsson, Cell death in the myocardium: my heart won’t go on. IUBMB Life 65, 651–656 (2013)CrossRefGoogle Scholar
  44. Q. Qiu, C. Li, Y. Wang, C. Xiao, Y. Li, Y. Lin, W. Wang, Plasma metabonomics study on Chinese medicine syndrome evolution of heart failure rats caused by LAD ligation. BMC Complement. Altern. Med. 14, 232 (2014)CrossRefGoogle Scholar
  45. T.L. Rasmussen, G. Raveendran, J. Zhang, D.J. Garry, Getting to the heart of myocardial stem cells and cell therapy. Circulation 123, 1771–1779 (2011)CrossRefGoogle Scholar
  46. C. Rüder, T. Haase, A. Krost, N. Langwieser, J. Peter, S. Kamann, D. Zohlnhöfer, Combinatorial G-CSF/AMD3100 treatment in cardiac repair after myocardial infarction. PLoS One 9, e104644 (2014)CrossRefGoogle Scholar
  47. S.K. Sanganalmath, R. Bolli, Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 113(2), 810 (2013)CrossRefGoogle Scholar
  48. S.K. Sanganalmath, R. Bolli, Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ. Res. 113(6), 810 (2013).Google Scholar
  49. A. Shafy, T. Fink, V. Zachar, N. Lila, A. Carpentier, J.C. Chachques, Development of cardiac support bioprostheses for ventricular restoration and myocardial regeneration. Eur. J. Cardiothorac. Surg. 43, 1211–1219 (2013)CrossRefGoogle Scholar
  50. C.C. Sheng, L. Zhou, J. Hao, Current stem cell delivery methods for myocardial repair. Biomed. Res. Int. 2013, 547902 (2013)Google Scholar
  51. R.R. Smith, E. Marbán, L. Marbán, Enhancing retention and efficacy of cardiosphere-derived cells administered after myocardial infarction using a hyaluronan-gelatin hydrogel. Biomatter 3, e24490 (2013)CrossRefGoogle Scholar
  52. R.C. Starling, M. Jessup, Worldwide clinical experience with the CorCap™ cardiac support device. J. Card. Fail. 10, S225–S233 (2004)CrossRefGoogle Scholar
  53. M.M. Sung, J.R. Dyck, Therapeutic potential of resveratrol in heart failure. Ann. N. Y. Acad. Sci. 1348, 32–45 (2015)CrossRefGoogle Scholar
  54. D.A. Taylor, M.J. Robertson, Cardiovascular translational medicine (IX) the basics of cell therapy to treat cardiovascular disease: one cell does not fit all. Rev. Esp. Cardiol. 62, 1032 (2009)CrossRefGoogle Scholar
  55. X. Tian, J. Fan, M. Yu, Y. Zhao, Y. Fang, S. Bai, W. Hou, H. Tong, Adipose stem cells promote smooth Muscle cells to secrete elastin in rat abdominal aortic aneurysm. PLoS One 9, e108105 (2014)CrossRefGoogle Scholar
  56. J.G. Travers, F.A. Kamal, J. Robbins, K.E. Yutzey, B.C. Blaxall, Cardiac fibrosis. Fibroblast Awakens 118, 1021–1040 (2016)Google Scholar
  57. B. Vrtovec, G. Poglajen, F. Haddad, Stem cell therapy in patients with heart failure. Methodist Debakey Cardiovasc. J. 9, 6 (2013)CrossRefGoogle Scholar
  58. J.F. Wenk, L. Ge, Z. Zhang, D. Mojsejenko, D.D. Potter, E.E. Tseng, J.M. Guccione, M.B. Ratcliffe, Biventricular finite element modeling of the Acorn CorCap Cardiac Support Device on a failing heart. Ann. Thorac. Surg. 95, 2022–2027 (2013)CrossRefGoogle Scholar
  59. C.W. Yancy, M. Jessup, B. Bozkurt, J. Butler, D.E. Casey, M.H. Drazner, G.C. Fonarow, S.A. Geraci, T. Horwich, J.L. Januzzi, M.R. Johnson, E.K. Kasper, W.C. Levy, F.A. Masoudi, P.E. Mcbride, J.J.V. Mcmurray, J.E. Mitchell, P.N. Peterson, B. Riegel, F. Sam, L.W. Stevenson, W.H.W. Tang, E.J. Tsai, B.L. Wilkoff, 2013 ACCF/AHA Guideline for the management of heart failure. J. Am. Coll. Cardiol. 62, e147–e239 (2013)CrossRefGoogle Scholar
  60. J. Yu, M. Li, Z. Qu, D. Yan, D. Li, Q. Ruan, SDF-1/CXCR4-mediated migration of transplanted bone marrow stromal cells toward areas of heart myocardial infarction through activation of PI3K/Akt. J. Cardiovasc. Pharmacol. 55, 496–505 (2010)Google Scholar
  61. X. Zhou, Active Hydraulic Ventricular Attaching Support System. US. (2012)Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Clinical Pharmacy, School of Basic Medicine and Clinical PharmacyChina Pharmaceutical University, School of PharmacyNanjingPeople’s Republic of China
  2. 2.Key Laboratory of Semiconductor Materials Science, Institute of SemiconductorsChinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.Department of SurgeryNanjing Shuiximen HospitalNanjingPeople’s Republic of China
  4. 4.Department of Cardiothoracic SurgeryZhongda Hospital affiliated to Southeast UniversityNanjingPeople’s Republic of China

Personalised recommendations