Cardiac magnetic resonance imaging findings and the risk of cardiovascular events in patients with recent myocardial infarction or suspected or known coronary artery disease: A systematic review of prognostic studies

Journal of the American College of Cardiology

Volumn 63, Issue 11, 2014, Pages 1031-1045

  El Aidi, Hamza ^a   Adams, Arthur ^a   Moons, Karel G M ^a   Den Ruijter, Hester M ^a   Mali, Willem P Th M ^a   Doevendans, Pieter A ^a   Nagel, Eike ^b   Schalla, Simon ^c   Bots, Michiel L ^a   Leiner, Tim ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ST THOMAS HOSPITAL   (United Kingdom)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

cardiac magnetic resonance; prognosis; systematic review

Indexed keywords

ARTICLE; CARDIAC IMAGING; CARDIOVASCULAR MAGNETIC RESONANCE; CARDIOVASCULAR RISK; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART PERFUSION; HEART VENTRICLE WALL MOTION; HUMAN; PATIENT IDENTIFICATION; PRIORITY JOURNAL; PROGNOSIS; RISK ASSESSMENT; SYSTEMATIC REVIEW; BLEEDING; CONTRAST ENHANCEMENT; EDEMA; HEART DEATH; HEART MUSCLE PERFUSION; HEART TRANSPLANTATION; MORTALITY; REVIEW;

CARDIAC MAGNETIC RESONANCE; PROGNOSIS; SYSTEMATIC REVIEW;

ACUTE CORONARY SYNDROME; CARDIOVASCULAR DISEASES; CORONARY ARTERY DISEASE; CORONARY CIRCULATION; FEMALE; GADOLINIUM; HUMANS; IMAGE ENHANCEMENT; MAGNETIC RESONANCE IMAGING, CINE; MALE; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; PROGNOSIS; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY; STROKE VOLUME;

GADOLINIUM;

EID: 84896539393     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2013.11.048     Document Type: Review

References (95)

1. R. Lozano, M. Naghavi, and K. Foreman et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010 Lancet 380 2012 2095 2128
2. E.A. Hulten, S. Carbonaro, S.P. Petrillo, J.D. Mitchell, and T.C. Villines Prognostic value of cardiac computed tomography angiography: a systematic review and meta-analysis J Am Coll Cardiol 57 2011 1237 1247
3. O. Bruder, S. Schneider, and D. Nothnagel et al. EuroCMR (European Cardiovascular Magnetic Resonance) registry: results of the German pilot phase J Am Coll Cardiol 54 2009 1457 1466
4. C. Jaarsma, T. Leiner, and S.C. Bekkers et al. Diagnostic performance of noninvasive myocardial perfusion imaging using single-photon emission computed tomography, cardiac magnetic resonance, and positron emission tomography imaging for the detection of obstructive coronary artery disease: a meta-analysis J Am Coll Cardiol 59 2012 1719 1728
5. O.P. Simonetti, R.J. Kim, and D.S. Fieno et al. An improved MR imaging technique for the visualization of myocardial infarction Radiology 218 2001 215 223
6. R.C. Semelka, E. Tomei, and S. Wagner et al. Interstudy reproducibility of dimensional and functional measurements between cine magnetic resonance studies in the morphologically abnormal left ventricle Am Heart J 119 1990 1367 1373
7. J. Romero, X. Xue, W. Gonzalez, and M.J. Garcia CMR imaging assessing viability in patients with chronic ventricular dysfunction due to coronary artery disease: a meta-analysis of prospective trials J Am Coll Cardiol Img 5 2012 494 508
8. K.R. Nandalur, B.A. Dwamena, A.F. Choudhri, M.R. Nandalur, and R.C. Carlos Diagnostic performance of stress cardiac magnetic resonance imaging in the detection of coronary artery disease: a meta-analysis J Am Coll Cardiol 50 2007 1343 1353
9. R.J. Kim, E. Wu, A. Rafael, and E.L. Chen et al. The use of contrast-enhanced magnetic resonance imaging to identify reversible myocardial dysfunction N Engl J Med 343 2000 1445 1453
10. B.J. Ingui, and M.A. Rogers Searching for clinical prediction rules in MEDLINE J Am Med Inform Assoc 8 2001 391 397
11. R.C. Hendel, M.R. Patel, and C.M. Kramer et al. ACCF/ACR/SCCT/SCMR/ASNC/ NASCI/SCAI/SIR 2006 appropriateness criteria for cardiac computed tomography and cardiac magnetic resonance imaging: a report of the American College of Cardiology Foundation Quality Strategic Directions Committee Appropriateness Criteria Working Group, American College of Radiology, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, American Society of Nuclear Cardiology, North American Society for Cardiac Imaging, Society for Cardiovascular Angiography and Interventions, and Society of Interventional Radiology J Am Coll Cardiol 48 2006 1475 1497
12. D. Moher, A. Liberati, J. Tetzlaff, and D.G. Altman Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement Ann Intern Med 151 2009 264 269 W64
13. J.A. Hayden, P. Cote, and C. Bombardier Evaluation of the quality of prognosis studies in systematic reviews Ann Intern Med 144 2006 427 437
14. W. Bouwmeester, N.P. Zuithoff, and S. Mallett et al. Reporting and methods in clinical prediction research: a systematic review PLoS Med 9 2012 1 12
15. G.S. Collins, S. Mallett, O. Omar, and L.M. Yu Developing risk prediction models for type 2 diabetes: a systematic review of methodology and reporting BMC Med 9 2011 103
16. S. Lerakis, D.S. McLean, and A.V. Anadiotis et al. Prognostic value of adenosine stress cardiovascular magnetic resonance in patients with low-risk chest pain J Cardiovasc Magn Reson 11 2009 37
17. G. Hartlage, M. Janik, and A. Anadiotis et al. Prognostic value of adenosine stress cardiovascular magnetic resonance and dobutamine stress echocardiography in patients with low-risk chest pain Int J Cardiovasc Imaging 28 2012 803 812
18. S. Lerakis, M. Janik, and D.S. McLean et al. Adenosine stress magnetic resonance imaging in women with low risk chest pain: the Emory University experience Am J Med Sci 339 2010 216 220
19. J. Vogel-Claussen, J. Skrok, and D. Dombroski et al. Comprehensive adenosine stress perfusion MRI defines the etiology of chest pain in the emergency room: comparison with nuclear stress test J Magn Reson Imaging 30 2009 753 762
20. W.P. Ingkanisorn, R.Y. Kwong, and N.S. Bohme et al. Prognosis of negative adenosine stress magnetic resonance in patients presenting to an emergency department with chest pain J Am Coll Cardiol 47 2006 1427 1432
21. K.T. Ahn, Y.B. Song, and Y.H. Choe et al. Impact of transmural necrosis on left ventricular remodeling and clinical outcomes in patients undergoing primary percutaneous coronary intervention for ST-segment elevation myocardial infarction Int J Cardiovasc Imaging 29 2013 835 842
22. N. Amabile, A. Jacquier, and A. Shuhab et al. Incidence, predictors, and prognostic value of intramyocardial hemorrhage lesions in ST elevation myocardial infarction Catheter Cardiovasc Interv 79 2012 1101 1108
23. V. Bodi, O. Husser, and J. Sanchis et al. Contractile reserve and extent of transmural necrosis in the setting of myocardial stunning: comparison at cardiac MR imaging Radiology 255 2010 755 763
24. V. Bodi, J. Sanchis, and J. Nunez et al. Prognostic value of a comprehensive cardiac magnetic resonance assessment soon after a first ST-segment elevation myocardial infarction J Am Coll Cardiol Img 2 2009 835 842
25. O. Bruder, F. Breuckmann, and C. Jensen et al. Prognostic impact of contrast-enhanced CMR early after acute ST segment elevation myocardial infarction (STEMI) in a regional STEMI network: results of the "Herzinfarktverbund Essen" Herz 33 2008 136 142
26. A. Cochet, A. Lalande, and L. Lorgis et al. Prognostic value of microvascular damage determined by cardiac magnetic resonance in non ST-segment elevation myocardial infarction: comparison between first-pass and late gadolinium-enhanced images Invest Radiol 45 2010 725 732
27. A.A. Cochet, L. Lorgis, and A. Lalande et al. Major prognostic impact of persistent microvascular obstruction as assessed by contrast-enhanced cardiac magnetic resonance in reperfused acute myocardial infarction Eur Radiol 19 2009 2117 2126
28. I. Eitel, M. Nowak, and C. Stehl et al. Endothelin-1 release in acute myocardial infarction as a predictor of long-term prognosis and no-reflow assessed by contrast-enhanced magnetic resonance imaging Am Heart J 159 2010 882 890
29. I. Eitel, S. Desch, and S. de Waha et al. Long-term prognostic value of myocardial salvage assessed by cardiovascular magnetic resonance in acute reperfused myocardial infarction Heart 97 2011 2038 2045
30. I. Eitel, S. Desch, and G. Fuernau et al. Prognostic significance and determinants of myocardial salvage assessed by cardiovascular magnetic resonance in acute reperfused myocardial infarction J Am Coll Cardiol 55 2010 2470 2479
31. I. Eitel, K. Kubusch, and O. Strohm et al. Prognostic value and determinants of a hypointense infarct core in T2-weighted cardiac magnetic resonance in acute reperfused ST-elevation-myocardial infarction Circ Cardiovasc Imaging 4 2011 354 362
32. M. Grothoff, C. Elpert, and J. Hoffmann et al. Right ventricular injury in ST-elevation myocardial infarction: risk stratification by visualization of wall motion, edema, and delayed-enhancement cardiac magnetic resonance Circ Cardiovasc Imaging 5 2012 60 68
33. O. Husser, V. Bodi, and J. Sanchis et al. Head to head comparison of quantitative versus visual analysis of contrast CMR in the setting of myocardial stunning after STEMI: implications on late systolic function and patient outcome Int J Cardiovasc Imaging 26 2010 559 569
34. O. Husser, J.V. Monmeneu, and J. Sanchis et al. Cardiovascular magnetic resonance-derived intramyocardial hemorrhage after STEMI: influence on long-term prognosis, adverse left ventricular remodeling and relationship with microvascular obstruction Int J Cardiol 167 2013 2047 2054
35. C.J. Jensen, M. Jochims, P. Hunold, G.V. Sabin, T. Schlosser, and O. Bruder Right ventricular involvement in acute left ventricular myocardial infarction: prognostic implications of MRI findings AJR Am J Roentgenol 194 2010 592 598
36. G. Klug, A. Mayr, and S. Schenk et al. Prognostic value at 5 years of microvascular obstruction after acute myocardial infarction assessed by cardiovascular magnetic resonance J Cardiovasc Magn Reson 14 2012 46
37. E. Larose, J. Rodes-Cabau, and P. Pibarot et al. Predicting late myocardial recovery and outcomes in the early hours of ST-segment elevation myocardial infarction: traditional measures compared with microvascular obstruction, salvaged myocardium, and necrosis characteristics by cardiovascular magnetic resonance J Am Coll Cardiol 55 2010 2459 2469
38. J.T. Lonborg, T. Engstrom, and J.E. Moller et al. Left atrial volume and function in patients following ST elevation myocardial infarction and the association with clinical outcome: a cardiovascular magnetic resonance study Eur Heart J Cardiovasc Imaging 14 2013 118 127
39. J. Lonborg, N. Vejlstrup, and H. Kelbaek et al. Final infarct size measured by cardiovascular magnetic resonance in patients with ST elevation myocardial infarction predicts long-term clinical outcome: an observational study Eur Heart J Cardiovasc Imaging 14 2013 387 395
40. T. Miszalski-Jamka, P. Klimeczek, and M. Tomala et al. Extent of RV dysfunction and myocardial infarction assessed by CMR are independent outcome predictors early after STEMI treated with primary angioplasty J Am Coll Cardiol Img 3 2010 1237 1246
41. S. de Waha, I. Eitel, and S. Desch et al. Time-dependency, predictors and clinical impact of infarct transmurality assessed by magnetic resonance imaging in patients with ST-elevation myocardial infarction reperfused by primary coronary percutaneous intervention Clin Res Cardiol 101 2012 191 200
42. S. de Waha, S. Desch, and I. Eitel et al. Relationship and prognostic value of microvascular obstruction and infarct size in ST-elevation myocardial infarction as visualized by magnetic resonance imaging Clin Res Cardiol 101 2012 487 495
43. S. de Waha, S. Desch, and I. Eitel et al. Impact of early vs. late microvascular obstruction assessed by magnetic resonance imaging on long-term outcome after ST-elevation myocardial infarction: a comparison with traditional prognostic markers Eur Heart J 31 2010 2660 2668
44. F. Prunier, S. Brette, S. Delepine, P. Geslin, J.J. Le Jeune, and A.P. Furber Three-dimensional MRI assessment of regional wall stress after acute myocardial infarction predicts postdischarge cardiac events J Magn Reson Imaging 27 2008 516 521
45. S.V. Raman, O.P. Simonetti, and M.W. Winner 3rd et al. Cardiac magnetic resonance with edema imaging identifies myocardium at risk and predicts worse outcome in patients with non-ST-segment elevation acute coronary syndrome J Am Coll Cardiol 55 2010 2480 2488
46. E. Wu, J.T. Ortiz, and P. Tejedor et al. Infarct size by contrast enhanced cardiac magnetic resonance is a stronger predictor of outcomes than left ventricular ejection fraction or end-systolic volume index: prospective cohort study Heart 94 2008 730 736
47. K.C. Wu, E.A. Zerhouni, and R.M. Judd et al. Prognostic significance of microvascular obstruction by magnetic resonance imaging in patients with acute myocardial infarction Circulation 97 1998 765 772
48. D. Bello, A. Einhorn, and R. Kaushal et al. Cardiac magnetic resonance imaging: infarct size is an independent predictor of mortality in patients with coronary artery disease Magn Reson Imaging 29 2011 50 56
49. A.G. Bertaso, J.D. Richardson, and D.T. Wong et al. Prognostic value of adenosine stress perfusion cardiac MRI with late gadolinium enhancement in an intermediate cardiovascular risk population Int J Cardiol 167 2013 2055 2060
50. S.E. Bingham, and R. Hachamovitch Incremental prognostic significance of combined cardiac magnetic resonance imaging, adenosine stress perfusion, delayed enhancement, and left ventricular function over preimaging information for the prediction of adverse events Circulation 123 2011 1509 1518
51. V. Bodi, J. Sanchis, and M.P. Lopez-Lereu et al. Prognostic value of dipyridamole stress cardiovascular magnetic resonance imaging in patients with known or suspected coronary artery disease J Am Coll Cardiol 50 2007 1174 1179
52. V. Bodi, O. Husser, and J. Sanchis et al. Prognostic implications of dipyridamole cardiac MR imaging: a prospective multicenter registry Radiology 262 2012 91 100
53. D. Buckert, P. Dewes, T. Walcher, W. Rottbauer, and P. Bernhardt Intermediate-term prognostic value of reversible perfusion deficit diagnosed by adenosine CMR: a prospective follow-up study in a consecutive patient population J Am Coll Cardiol Img 6 2013 56 63
54. O. Catalano, G. Moro, and M. Perotti et al. Late gadolinium enhancement by cardiovascular magnetic resonance is complementary to left ventricle ejection fraction in predicting prognosis of patients with stable coronary artery disease J Cardiovasc Magn Reson 14 2012 29
55. C. Charoenpanichkit, T.M. Morgan, and C.A. Hamilton et al. Left ventricular hypertrophy influences cardiac prognosis in patients undergoing dobutamine cardiac stress testing Circ Cardiovasc Imaging 3 2010 392 397
56. B.Y. Cheong, R. Muthupillai, and J.M. Wilson et al. Prognostic significance of delayed-enhancement magnetic resonance imaging: survival of 857 patients with and without left ventricular dysfunction Circulation 120 2009 2069 2076
57. O.R. Coelho-Filho, L.F. Seabra, and F.P. Mongeon et al. Stress myocardial perfusion imaging by CMR provides strong prognostic value to cardiac events regardless of patient's sex J Am Coll Cardiol Img 4 2011 850 861
58. G. Di Bella, V. Siciliano, and G.D. Aquaro et al. Scar extent, left ventricular end-diastolic volume, and wall motion abnormalities identify high-risk patients with previous myocardial infarction: a multiparametric approach for prognostic stratification Eur Heart J 34 2013 104 111
59. R. Gebker, C. Jahnke, and R. Manka et al. The role of dobutamine stress cardiovascular magnetic resonance in the clinical management of patients with suspected and known coronary artery disease J Cardiovasc Magn Reson 13 2011 46
60. W.G. Hundley, T.M. Morgan, C.M. Neagle, C.A. Hamilton, P. Rerkpattanapipat, and K.M. Link Magnetic resonance imaging determination of cardiac prognosis Circulation 106 2002 2328 2333
61. C. Jahnke, V. Furundzija, and R. Gebker et al. Gender-based prognostic value of pharmacological cardiac magnetic resonance stress testing: head-to-head comparison of adenosine perfusion and dobutamine wall motion imaging Int J Cardiovasc Imaging 28 2012 1087 1098
62. C. Jahnke, E. Nagel, and R. Gebker et al. Prognostic value of cardiac magnetic resonance stress tests: adenosine stress perfusion and dobutamine stress wall motion imaging Circulation 115 2007 1769 1776
63. S. Kelle, A. Chiribiri, and J. Vierecke et al. Long-term prognostic value of dobutamine stress CMR J Am Coll Cardiol Img 4 2011 161 172
64. E. Larose, P. Ganz, and H.G. Reynolds et al. Right ventricular dysfunction assessed by cardiovascular magnetic resonance imaging predicts poor prognosis late after myocardial infarction J Am Coll Cardiol 49 2007 855 862
65. K.Y. Lo, K.F. Leung, C.M. Chu, K.L. Loke, C.K. Chan, and C.S. Yue Prognostic value of adenosine stress myocardial perfusion by cardiac magnetic resonance imaging in patients with known or suspected coronary artery disease QJM 104 2011 425 432
66. M. Kaminski, K. Steel, and M. Jerosch-Herold et al. Strong cardiovascular prognostic implication of quantitative left atrial contractile function assessed by cardiac magnetic resonance imaging in patients with chronic hypertension J Cardiovasc Magn Reson 13 2011 42
67. G. Korosoglou, Y. Elhmidi, and H. Steen et al. Prognostic value of high-dose dobutamine stress magnetic resonance imaging in 1,493 consecutive patients: assessment of myocardial wall motion and perfusion J Am Coll Cardiol 56 2010 1225 1234
68. G. Korosoglou, G. Gitsioudis, and A. Voss et al. Strain-encoded cardiac magnetic resonance during high-dose dobutamine stress testing for the estimation of cardiac outcomes: comparison to clinical parameters and conventional wall motion readings J Am Coll Cardiol 58 2011 1140 1149
69. R. Krittayaphong, T. Boonyasirinant, and P. Saiviroonporn et al. Prognostic significance of left ventricular mass by magnetic resonance imaging study in patients with known or suspected coronary artery disease J Hypertens 27 2009 2249 2256
70. R. Krittayaphong, V. Chaithiraphan, A. Maneesai, and S. Udompanturak Prognostic value of combined magnetic resonance myocardial perfusion imaging and late gadolinium enhancement Int J Cardiovasc Imaging 27 2011 705 714
71. R. Krittayaphong, A. Maneesai, V. Chaithiraphan, P. Saiviroonporn, O. Chaiphet, and S. Udompunturak Comparison of diagnostic and prognostic value of different electrocardiographic criteria to delayed-enhancement magnetic resonance imaging for healed myocardial infarction Am J Cardiol 103 2009 464 470
72. R. Krittayaphong, T. Boonyasirinant, and V. Chaithiraphan et al. Prognostic value of late gadolinium enhancement in hypertensive patients with known or suspected coronary artery disease Int J Cardiovasc Imaging 26 Suppl 1 2010 123 131
73. R.Y. Kwong, A.K. Chan, and K.A. Brown et al. Impact of unrecognized myocardial scar detected by cardiac magnetic resonance imaging on event-free survival in patients presenting with signs or symptoms of coronary artery disease Circulation 113 2006 2733 2743
74. R.Y. Kwong, H. Sattar, and H. Wu et al. Incidence and prognostic implication of unrecognized myocardial scar characterized by cardiac magnetic resonance in diabetic patients without clinical evidence of myocardial infarction Circulation 118 2008 1011 1020
75. K. Steel, R. Broderick, and V. Gandla et al. Complementary prognostic values of stress myocardial perfusion and late gadolinium enhancement imaging by cardiac magnetic resonance in patients with known or suspected coronary artery disease Circulation 120 2009 1390 1400
76. E.L. Wallace, T.M. Morgan, and T.F. Walsh et al. Dobutamine cardiac magnetic resonance results predict cardiac prognosis in women with known or suspected ischemic heart disease J Am Coll Cardiol Img 2 2009 299 307
77. P. Peduzzi, J. Concato, E. Kemper, T.R. Holford, and A.R. Feinstein A simulation study of the number of events per variable in logistic regression analysis J Clin Epidemiol 49 1996 1373 1379
78. R.A. Kloner, C.E. Ganote, and R.B. Jennings The "no-reflow" phenomenon after temporary coronary occlusion in the dog J Clin Invest 54 1974 1496 1508
79. M.C. Fishbein, Y.R. J, U. Lando, K. Kanmatsuse, J.C. Mercier, and W. Ganz The relationship of vascular injury and myocardial hemorrhage to necrosis after reperfusion Circulation 62 1980 1274 1279
80. J.E. Moller, G.S. Hillis, J.K. Oh, G.S. Reeder, B.J. Gersh, and P.A. Pellikka Wall motion score index and ejection fraction for risk stratification after acute myocardial infarction Am Heart J 151 2006 419 425
81. S.A. Mollema, G. Nucifora, and J.J. Bax Prognostic value of echocardiography after acute myocardial infarction Heart 95 2009 1732 1745
82. M.J. Lipinski, C.M. McVey, J.S. Berger, C.M. Kramer, and M. Salerno Prognostic value of stress cardiac magnetic resonance imaging in patients with known or suspected coronary artery disease: a systematic review and meta-analysis J Am Coll Cardiol 62 2013 826 838
83. P. Royston, D.G. Altman, and W. Sauerbrei Dichotomizing continuous predictors in multiple regression: a bad idea Stat Med 25 2006 127 141
84. M.A. Babyak What you see may not be what you get: a brief, nontechnical introduction to overfitting in regression-type models Psychosom Med 66 2004 411 421
85. R.D. Riley, P.C. Lambert, and G. Abo-Zaid Meta-analysis of individual participant data: rationale, conduct, and reporting BMJ 340 2010 c221
86. H. Hemingway, P. Philipson, and R. Chen et al. Evaluating the quality of research into a single prognostic biomarker: a systematic review and meta-analysis of 83 studies of C-reactive protein in stable coronary artery disease PLoS Med 7 2010 e1000286
87. R.D. Riley, D. Heney, and D.R. Jones et al. A systematic review of molecular and biological tumor markers in neuroblastoma Clin Cancer Res 10 Pt 1 2004 4 12
88. Collins GS. Opening up multivariable prediction models: consensus-based guidelines for transparent reporting. 2011. Available at: http://blogs.bmj.com. proxy.library.uu.nl/bmj/2011/08/03/gary-collins-opening-up-multivariable- prediction-models/. Accessed June 20, 2013.
89. H.M. Den Ruijter, S.A. Peters, and T.J. Anderson et al. Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis JAMA 308 2012 796 803
90. K.A. Fox, T.C. Clayton, and P. Damman et al. Long-term outcome of a routine versus selective invasive strategy in patients with non-ST-segment elevation acute coronary syndrome: a meta-analysis of individual patient data J Am Coll Cardiol 55 2010 2435 2445
91. L.M. McShane, D.G. Altman, W. Sauerbrei, S.E. Taube, M. Gion, and G.M. Clark REporting recommendations for tumour MARKer prognostic studies (REMARK) Br J Cancer 93 2005 387 391
92. H. Hemingway, P. Croft, and P. Perel et al. Prognosis research strategy (PROGRESS) 1: a framework for researching clinical outcomes BMJ 346 2013 e5595
93. R.D. Riley, J.A. Hayden, and E.W. Steyerberg et al. Prognosis Research Strategy (PROGRESS) 2: prognostic factor research PLoS Med 10 2013 e1001380
94. E.W. Steyerberg, K.G. Moons, and D.A. van der Windt et al. Prognosis Research Strategy (PROGRESS) 3: prognostic model research PLoS Med 10 2013 e1001381
95. A.D. Hingorani, D.A. Windt, and R.D. Riley et al. Prognosis research strategy (PROGRESS) 4: stratified medicine research BMJ 346 2013 e5793