Translational research in cardiovascular repair a call for a paradigm shift

Circulation Research

Volumn 122, Issue 2, 2018, Pages 310-318

  Chamuleau, Steven A J ^a,b   Van Der Naald, Mira ^a   Climent, Andreu M ^b,c   Kraaijeveld, Adriaan O ^a   Wever, Kim E ^d   Duncker, Dirk J ^e,f   Fernández Avilés, Francisco ^b,c   Bolli, Roberto ^g  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b European Society of Cardiology Working Group on Cardiovascular Regenerative and Reparative Medicine   (France)

^c HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f INTERUNIVERSITY CARDIOLOGY INSTITUTE OF THE NETHERLANDS   (Netherlands)

^g University of Louisville School of Medicine   (United States)

Author keywords

Animal experimentation; Research design; Stem cell research; Translational medical research

Indexed keywords

CARDIOVASCULAR SURGERY; CLINICAL PROTOCOL; COMMUNITY; CONFIRMATORY STUDY; EXPLORATORY RESEARCH; HUMAN; INTERNAL VALIDITY; LEAD CELL PRODUCT DEVELOPMENT; LEAD CELL PRODUCT DISCOVERY; MEDICAL RESEARCH; META ANALYSIS (TOPIC); METHODOLOGY; NONHUMAN; PARAMETERS; PRECLINICAL RESEARCH; PRECLINICAL STUDY; PRIORITY JOURNAL; PUBLISHING; QUALITY CONTROL; REGISTRATION; REPRODUCIBILITY; RESEARCH COMMUNITY; RESEARCH INTEGRITY; REVIEW; STANDARDIZATION; SYSTEMATIC REVIEW (TOPIC); TRANSLATIONAL RESEARCH; ANIMAL; CARDIOVASCULAR DISEASE; GENETICS; PATHOLOGY; PROCEDURES; REGENERATIVE MEDICINE; TRENDS;

ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; META-ANALYSIS AS TOPIC; REGENERATIVE MEDICINE; SYSTEMATIC REVIEWS AS TOPIC; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85046851665     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.311565     Document Type: Review

References (60)

1. Fernández-Avilés F, Sanz-Ruiz R, Climent AM, et al; TACTICS (Transnational Alliance for Regenerative Therapies in Cardiovascular Syndromes) Writing Group; Authors/Task Force Members. Chairpersons; Basic Research Subcommittee; Translational Research Subcommittee; Challenges of Cardiovascular Regenerative Medicine Subcommittee; Tissue Engineering Subcommittee; Delivery, Navigation, Tracking and Assessment Subcommittee; Clinical Trials Subcommittee; Regulatory and funding strategies subcommittee; Delivery, Navigation, Tracking and Assessment Subcommittee. Global position paper on cardiovascular regenerative medicine. Eur Heart J. 2017;38:2532-2546. doi: 10.1093/eurheartj/ehx248.
2. Zwetsloot PP, Végh AM, Jansen of Lorkeers SJ, van Hout GP, Currie GL, Sena ES, Gremmels H, Buikema JW, Goumans M-J, Macleod MR, Doevendans PA, Chamuleau SA, Sluijter JP. Cardiac stem cell treatment in myocardial infarction: A systematic review and meta-Analysis of preclinical studies. Circ Res. 2016;118:1223-1232.
3. Jansen of Lorkeers SJ, Eding JEC, Vesterinen HM, van der Spoel TIG, Sena ES, Duckers HJ, Doevendans PA, Macleod MR, Chamuleau SAJ. Similar effect of autologous and allogeneic cell therapy for ischemic heart disease: systematic review and meta-Analysis of large animal studies. Circ Res. 2015;116:80-86.
4. Fisher SA, Doree C, Mathur A, Martin-Rendon E. Meta-Analysis of cell therapy trials for patients with heart failure. Circ Res. 2015;116:1361-1377.
5. Bolli R, Ghafghazi S. Cell therapy needs rigorous translational studies in large animal models. J Am Coll Cardiol. 2015;66:2000-2004. doi: 10.1016/j.jacc.2015.09.002.
6. Van Hout GPJ, Jansen of Lorkeers SJ, Wever KE, Sena ES, Kouwenberg LHJ, van Solinge WW, Macleod MR, Doevendans PA, Pasterkamp G, Chamuleau SAJ, Hoefer IE. Translational failure of anti-inflammatory compounds for myocardial infarction: A meta-Analysis of large animal models. Cardiovasc Res. 2016;109:240-248.
7. Bolli R. Reflections on the irreproducibility of scientific papers. Circ Res. 2015;117:665-666. doi: 10.1161/CIRCRESAHA.115.307496.
8. Bolli R. New initiatives to improve the rigor and reproducibility of articles published in circulation research. Circ Res. 2017;121:472-479.
9. Sena E, van der Worp HB, Howells D, Macleod M. How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci. 2007;30:433-439. doi: 10.1016/j.tins.2007.06.009.
10. Ramirez FD, Motazedian P, Jung RG, Di Santo P, MacDonald ZD, Moreland R, Simard T, Clancy AA, Russo JJ, Welch VA, Wells GA, Hibbert B. Methodological rigor in preclinical cardiovascular studies: Targets to enhance reproducibility and promote research translation. Circ Res. 2017;120:1916-1926. doi: 10.1161/CIRCRESAHA.117.310628.
11. Gyöngyösi M, Wojakowski W, Lemarchand P, et al; ACCRUE Investigators. Meta-Analysis of Cell-based CaRdiac stUdiEs (ACCRUE) in patients with acute myocardial infarction based on individual patient data. Circ Res. 2015;116:1346-1360. doi: 10.1161/CIRCRESAHA.116.304346.
12. Bolli R, Ghafghazi S. Stem cells: cell therapy for cardiac repair: what is needed to move forward? Nat Rev Cardiol. 2017;14:257-258.
13. Poss KD, Wilson LG, Keating MT. Heart regeneration in zebrafish. Science. 2002;298:2188-2190. doi: 10.1126/science.1077857.
14. Golpanian S, Schulman IH, Ebert RF, Heldman AW, DiFede DL, Yang PC, Wu JC, Bolli R, Perin EC, Moyé L, Simari RD, Wolf A, Hare JM; Cardiovascular Cell Therapy Research Network. Concise review: review and perspective of cell dosage and routes of administration from preclinical and clinical studies of stem cell therapy for heart disease. Stem Cells Transl Med. 2016;5:186-191. doi: 10.5966/sctm.2015-0101.
15. Jansen of Lorkeers SJ, Gho JMIH, Koudstaal S, van Hout GPJ, Zwetsloot PPM, van Oorschot JWM, van Eeuwijk ECM, Leiner T, Hoefer IE, Goumans M-J, Doevendans PA, Sluijter JPG, Chamuleau SAJ. Xenotransplantation of human cardiomyocyte progenitor cells does not improve cardiac function in a porcine model of chronic ischemic heart failure. Results from a randomized, blinded, placebo controlled trial. PLoS One. 2015;10:e0143953.
16. Kupfer ME, Ogle BM. Advanced imaging approaches for regenerative medicine: emerging technologies for monitoring stem cell fate in vitro and in vivo. Biotechnol J. 2015;10:1515-1528. doi: 10.1002/biot.201400760.
17. Dib N, Menasche P, Bartunek JJ, et al; International Society for Cardiovascular Translational Research. Recommendations for successful training on methods of delivery of biologics for cardiac regeneration: A report of the International Society for Cardiovascular Translational Research. JACC Cardiovasc Interv. 2010;3:265-275. doi: 10.1016/j.jcin.2009.12.013.
18. van der Spoel TIG, Lee JC-T, Vrijsen K, Sluijter JPG, Cramer MJM, Doevendans PA, van Belle E, Chamuleau SAJ. Non-surgical stem cell delivery strategies and in vivo cell tracking to injured myocardium. Int J Cardiovasc Imaging. 2011;27:367-383.
19. Begley CG, Ellis LM. Drug development: raise standards for preclinical cancer research. Nature. 2012;483:531-533. doi: 10.1038/483531a.
20. Ioannidis JPA. Why most published research findings are false. PLoS Med. 2005;2:e124.
21. Patsopoulos NA, Tatsioni A, Ioannidis JP. Claims of sex differences: An empirical assessment in genetic associations. JAMA. 2007;298:880-893. doi: 10.1001/jama.298.8.880.
22. Friedman LM, Furberg CD, Demets DL. Fundamentals of Clinical Trials. New York: Springer-Verlag; 2010:1-445.
23. Dechartres A, Boutron I, Trinquart L, Charles P, Ravaud P. Single-center trials show larger treatment effects than multicenter trials: evidence from a meta-epidemiologic study. Ann Intern Med. 2011;155:39-51. doi: 10.7326/0003-4819-155-1-201107050-00006.
24. Lefer DJ, Bolli R. Development of an NIH consortium for preclinicAl AssESsment of CARdioprotective therapies (CAESAR): A paradigm shift in studies of infarct size limitation. J Cardiovasc Pharmacol Ther. 2011;16:332-339.
25. Dirnagl U, Fisher M. International, multicenter randomized preclinical trials in translational stroke research: its time to act. J Cereb Blood Flow Metab. 2012;32:933-935.
26. Jones SP, Tang XL, Guo Y, et al. The NHLBI-sponsored Consortium for preclinicAl assESsment of cARdioprotective therapies (CAESAR): A new paradigm for rigorous, accurate, and reproducible evaluation of putative infarct-sparing interventions in mice, rabbits, and pigs. Circ Res. 2015;116:572-586. doi: 10.1161/CIRCRESAHA.116.305462.
27. Howells DW, Sena ES, Macleod MR. Bringing rigour to translational medicine. Nat Rev Neurol. 2014;10:37-43.doi: 10.1038/nrneurol.2013.232.
28. Kukreja R, Tang X-L, Lefer D, et al. Administration of sildenafil at reperfusion fails to reduce infarct size: results from the CAESAR Cardioprotection Consortium (LB650). FASEB J. 2014;28:LB650.
29. Lefer D, Jones S, Steenbergen C, et al. Sodium nitrite fails to limit myocardial infarct size: results from the CAESAR Cardioprotection Consortium (LB645). FASEB J. 2014;28:LB645.
30. Hare JM, Bolli R, Cooke JP, et al; Cardiovascular Cell Therapy Research Network. Phase II clinical research design in cardiology: learning the right lessons too well: observations and recommendations from the Cardiovascular Cell Therapy Research Network (CCTRN). Circulation. 2013;127:1630-1635. doi: 10.1161/CIRCULATIONAHA.112.000779.
31. Hariharan N, Quijada P, Mohsin S, Joyo A, Samse K, Monsanto M, De La Torre A, Avitabile D, Ormachea L, McGregor MJ, Tsai EJ, Sussman MA. Nucleostemin rejuvenates cardiac progenitor cells and antagonizes myocardial aging. J Am Coll Cardiol. 2015;65:133-147.
32. van Berlo JH, Kanisicak O, Maillet M, Vagnozzi RJ, Karch J, Lin SJ, Middleton RC, Marba E, Molkentin JD. c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature. 2014;509:337-341.
33. Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov. 2004;3:711-715. doi: 10.1038/nrd1470.
34. Chalmers I, Glasziou P. Avoidable waste in the production and reporting of research evidence. Lancet. 2009;374:86-89.
35. Dwan K, Gamble C, Williamson PR, Kirkham JJ; Reporting Bias Group. Systematic review of the empirical evidence of study publication bias and outcome reporting bias-An updated review. PLoS One. 2013;8:e66844. doi: 10.1371/journal.pone.0066844.
36. Macleod MR, OCollins T, Howells DW, Donnan GA. Pooling of animal experimental data reveals influence of study design and publication bias. Stroke. 2004;35:1203-1208.
37. Hopewell S, Clarke MJ, Stewart L, Tierney J. Time to publication for results of clinical trials. Cochrane Database Syst Rev. 2007;MR000011.
38. Sena ES, van der Worp HB, Bath PM, Howells DW, Macleod MR. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol. 2010;8:e1000344. doi: 10.1371/journal. pbio.1000344.
39. Cuijpers P, van Straten A, Bohlmeijer E, Hollon SD, Andersson G. The effects of psychotherapy for adult depression are overestimated: A metaanalysis of study quality and effect size. Psychol Med. 2010;40:211-223. doi: 10.1017/S0033291709006114.
40. Dirnagl U, Lauritzen M. Fighting publication bias: introducing the negative results section. J Cereb Blood Flow Metab. 2010;30:1263-1264. doi: 10.1038/jcbfm.2010.51.
41. Chambers CD, Dienes Z, McIntosh RD, Rotshtein P, Willmes K. Registered reports: realigning incentives in scientific publishing. Cortex. 2015;66:A1-A2. doi: 10.1016/j.cortex.2015.03.022.
42. Turner S, Wright D, Maeso R, Cook A, Milne R. Publication rate for funded studies from a major UK health research funder: A cohort study. BMJ Open. 2013;3:e002521.
43. Jöni P, Altman DG, Egger M. Assessing the quality of controlled clinical trials. BMJ. 2001;323:42-46.
44. Schulz KF, Altman DG, Moher D. CONSORT 2010 Statement: updated guidelines for reporting parallel group randomised trials. BMJ. 2010;340:c332.
45. van Hout GP, Jansen of Lorkeers SJ, Wever KE, Sena ES, Kouwenberg LH, van Solinge WW, Macleod MR, Doevendans PA, Pasterkamp G, Chamuleau SA, Hoefer IE. Translational failure of anti-inflammatory compounds for myocardial infarction: A meta-Analysis of large animal models. Cardiovasc Res. 2016;109:240-248. doi: 10.1093/cvr/cvv239.
46. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. Animals. 2013;4:35-44.
47. Korevaar DA, Hooft L, ter Riet G. Systematic reviews and meta-Analyses of preclinical studies: publication bias in laboratory animal experiments. Lab Anim. 2011;45:225-230.
48. Wever KE, Hooijmans CR, Riksen NP, Sterenborg TB, Sena ES, Ritskes-Hoitinga M, Warlé MC. Determinants of the efficacy of cardiac ischemic preconditioning: A systematic review and meta-Analysis of animal studies. PLoS One. 2015;10:e0142021. doi: 10.1371/journal.pone.0142021.
49. Bromage DI, Pickard JMJ, Rossello X, Ziff OJ, Burke N, Yellon DM, Davidson SM. Remote ischaemic conditioning reduces infarct size in animal in vivo models of ischaemia-reperfusion injury: A systematic review and meta-Analysis. Cardiovasc Res. 2016;113:288-297.
50. Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLEs risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14:43. doi: 10.1186/1471-2288-14-43.
51. Macleod MR, Ebrahim S, Roberts I. Surveying the literature from animal experiments: systematic review and meta-Analysis are important contributions. BMJ. 2005;331:110. doi: 10.1136/bmj.331.7508.110-b.
52. van der Spoel TI, Jansen of Lorkeers SJ, Agostoni P, van Belle E, Gyöngyösi M, Sluijter JP, Cramer MJ, Doevendans PA, Chamuleau SA. Human relevance of pre-clinical studies in stem cell therapy: systematic review and meta-Analysis of large animal models of ischaemic heart disease. Cardiovasc Res. 2011;91:649-658. doi: 10.1093/cvr/cvr113.
53. Ross JS, Mulvey GK, Hines EM, Nissen SE, Krumholz HM. Trial publication after registration in clinicaltrials.gov: A cross-sectional analysis. PLoS Med. 2009;6:e1000144. doi: 10.1371/journal.pmed.1000144.
54. Chalmers I, Glasziou P, Godlee F. All trials must be registered and the results published. BMJ. 2013;346:f105.
55. Jansen of Lorkeers SJ, Doevendans PA, Chamuleau SA. All preclinical trials should be registered in advance in an online registry. Eur J Clin Invest. 2014;44:891-892.
56. Kimmelman J, Anderson JA. Should preclinical studies be registered? Nat Biotechnol. 2012;30:488-489. doi: 10.1038/nbt.2261.
57. Brown T. Its time for alltrials registered and reported. Cochrane Database Syst Rev. 2013;4. doi: 10.1002/14651858.ED000057.
58. Hale C, Arrowsmith J, Bayes S, Bodmer H, Garman A, Hubbard P, Perrin N, Sooben P. The Concordat to Support Research Integrity. http://www. universitiesuk.ac.uk/policy-And-Analysis/reports/Documents/2012/theconcordat-To-support-research-integrity.pdf. Accessed February 24, 2017.
59. Moylan EC, Kowalczuk MK. Why articles are retracted: A retrospective cross-sectional study of retraction notices at BioMed Central. BMJ Open. 2016;6:e012047.
60. Benedictus R, Miedema F, Ferguson MWJ. Fewer numbers, better science. Nature. 2016;538:453-455.