High-sensitivity C-reactive protein and cardiovascular disease: A resolute belief or an elusive link?

Journal of the American College of Cardiology

Volumn 62, Issue 5, 2013, Pages 397-408

  Yousuf, Omair ^a   Mohanty, Bibhu D ^b   Martin, Seth S ^a   Joshi, Parag H ^a   Blaha, Michael J ^a   Nasir, Khurram ^a,c,d,e   Blumenthal, Roger S ^a   Budoff, Matthew J ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c HARBOR UCLA MEDICAL CENTER   (United States)

^d MIAMI CANCER INSTITUTE   (United States)

^e FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

atherosclerosis; cardiovascular disease; coronary heart disease; CRP; hsCRP; inflammation; prevention; statins

Indexed keywords

ATORVASTATIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CANAKINUMAB; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HIGH SENSITIVITY C REACTIVE PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; METHOTREXATE; MEVINOLIN; PLACEBO; PRAVASTATIN; ROSUVASTATIN; UNCLASSIFIED DRUG;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CLINICAL DECISION MAKING; CLINICAL PRACTICE; DISEASE ASSOCIATION; DISEASE MARKER; ENZYME INHIBITION; FRAMINGHAM RISK SCORE; GENETIC ASSOCIATION; HUMAN; ISCHEMIC HEART DISEASE; MONOCYTE; NONHUMAN; PATIENT CODING; PHENOTYPE; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REFERENCE VALUE; REYNOLDS RISK SCORE; RISK ASSESSMENT; SCREENING TEST; SEX DIFFERENCE; TREATMENT PLANNING; TREATMENT RESPONSE;

EID: 84880606957     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2013.05.016     Document Type: Review

References (98)

1. M.B. Pepys, and G.M. Hirschfield C-reactive protein: a critical update J Clin Invest 111 2003 1805 1812
2. P. Libby Inflammation in atherosclerosis Nature 420 2002 868 874
3. J. Danesh, R. Collins, P. Appleby, and R. Peto Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies JAMA 279 1998 1477 1482
4. J.K. Pai, T. Pischon, and J. Ma Inflammatory markers and the risk of coronary heart disease in men and women N Engl J Med 351 2004 2599 2610
5. P. Greenland, M.D. Knoll, and J. Stamler Major risk factors as antecedents of fatal and nonfatal coronary heart disease events JAMA 290 2003 891 897
6. U.N. Khot, M.B. Khot, and C.T. Bajzer Prevalence of conventional risk factors in patients with coronary heart disease JAMA 290 2003 898 904
7. S.C. Smith Jr. Current and future directions of cardiovascular risk prediction Am J Cardiol 97 2006 28A 32A
8. W.S. Tillett, and T. Francis Serological reactions in pneumonia with a non-protein somatic fraction of Pneumococcus J Exp Med 52 1930 561 571
9. L.H. Kuller, R.P. Tracy, J. Shaten, and E.N. Meilahn Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study. Multiple Risk Factor Intervention Trial Am J Epidemiol 144 1996 537 547
10. D.M. Vigushin, M.B. Pepys, and P.N. Hawkins Metabolic and scintigraphic studies of radioiodinated human C-reactive protein in health and disease J Clin Invest 91 1993 1351 1357
11. G.D. Norata, P. Marchesi, and V.K. Pulakazhi Venu Deficiency of the long pentraxin PTX3 promotes vascular inflammation and atherosclerosis Circulation 120 2009 699 708
12. Y.X. Zhang, W.J. Cliff, G.I. Schoefl, and G. Higgins Coronary C-reactive protein distribution: its relation to development of atherosclerosis Atherosclerosis 145 1999 375 379
13. P. Libby, M. Nahrendorf, M.J. Pittet, and F.K. Swirski Diversity of denizens of the atherosclerotic plaque: not all monocytes are created equal Circulation 117 2008 3168 3170
14. R. Kones Primary prevention of coronary heart disease: integration of new data, evolving views, revised goals, and role of rosuvastatin in management. A comprehensive survey Drug Des Devel Ther 5 2011 325 380
15. H. Guan, P. Wang, R. Hui, M.L. Edin, D.C. Zeldin, and D.W. Wang Adeno-associated virus-mediated human C-reactive protein gene delivery causes endothelial dysfunction and hypertension in rats Clin Chem 55 2009 274 284
16. I. Jialal, S. Verma, and S. Devaraj Inhibition of endothelial nitric oxide synthase by C-reactive protein: clinical relevance Clin Chem 55 2009 206 208
17. S.U. Eisenhardt, J. Habersberger, and A. Murphy Dissociation of pentameric to monomeric C-reactive protein on activated platelets localizes inflammation to atherosclerotic plaques Circ Res 105 2009 128 137
18. S.R. Ji, L. Ma, and C.J. Bai Monomeric C-reactive protein activates endothelial cells via interaction with lipid raft microdomains FASEB J 23 2009 1806 1816
19. S. Kinlay Low-density lipoprotein-dependent and -independent effects of cholesterol-lowering therapies on C-reactive protein: a meta-analysis J Am Coll Cardiol 49 2007 2003 2009
20. S.E. Nissen, E.M. Tuzcu, and P. Schoenhagen Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease N Engl J Med 352 2005 29 38
21. P.M. Ridker, C.P. Cannon, and D. Morrow C-reactive protein levels and outcomes after statin therapy N Engl J Med 352 2005 20 28
22. P.M. Ridker, N. Rifai, and M.A. Pfeffer Inflammation, pravastatin, and the risk of coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events (CARE) Investigators Circulation 98 1998 839 844
23. J.G. Robinson, B. Smith, N. Maheshwari, and H. Schrott Pleiotropic effects of statins: benefit beyond cholesterol reduction? A meta-regression analysis J Am Coll Cardiol 46 2005 1855 1862
24. A.D. Hingorani, R. Sofat, and R.W. Morris Is it important to measure or reduce C-reactive protein in people at risk of cardiovascular disease? Eur Heart J 33 2012 2258 2264
25. A. Trion, M.P. de Maat, and J.W. Jukema No effect of C-reactive protein on early atherosclerosis development in apolipoprotein Eâ̂ - 3-Leiden/human C-reactive protein transgenic mice Arterioscler Thromb Vasc Biol 25 2005 1635 1640
26. G.A. Tennent, W.L. Hutchinson, and M.C. Kahan Transgenic human CRP is not pro-atherogenic, pro-atherothrombotic or pro-inflammatory in apoE-/- mice Atherosclerosis 196 2008 248 255
27. B.R. Clapp, G.M. Hirschfield, and C. Storry Inflammation and endothelial function: direct vascular effects of human C-reactive protein on nitric oxide bioavailability Circulation 111 2005 1530 1536
28. M.B. Pepys, P.N. Hawkins, and M.C. Kahan Proinflammatory effects of bacterial recombinant human C-reactive protein are caused by contamination with bacterial products, not by C-reactive protein itself Circ Res 97 2005 e97 103
29. G.M. Hirschfield, J.R. Gallimore, and M.C. Kahan Transgenic human C-reactive protein is not proatherogenic in apolipoprotein E-deficient mice Proc Natl Acad Sci U S A 102 2005 8309 8314
30. T. Koike, S. Kitajima, and Y. Yu Human C-reactive protein does not promote atherosclerosis in transgenic rabbits Circulation 120 2009 2088 2094
31. P. Elliott, J.C. Chambers, and W. Zhang Genetic loci associated with C-reactive protein levels and risk of coronary heart disease JAMA 302 2009 37 48
32. J. Zacho, A. Tybjaerg-Hansen, J.S. Jensen, P. Grande, H. Sillesen, and B.G. Nordestgaard Genetically elevated C-reactive protein and ischemic vascular disease N Engl J Med 359 2008 1897 1908
33. F. Wensley, P. Gao, and S. Burgess Association between C reactive protein and coronary heart disease: Mendelian randomisation analysis based on individual participant data BMJ 342 2011 d548
34. A. Dehghan, J. Dupuis, and M. Barbalic Meta-analysis of genome-wide association studies in >80,000 subjects identifies multiple loci for C-reactive protein levels Circulation 123 2011 731 738
35. P.R. Kamstrup, A. Tybjaerg-Hansen, R. Steffensen, and B.G. Nordestgaard Genetically elevated lipoprotein(a) and increased risk of myocardial infarction JAMA 301 2009 2331 2339
36. J.C. Cohen, E. Boerwinkle, T.H. Mosley Jr., and H.H. Hobbs Sequence variations in PCSK9, low LDL, and protection against coronary heart disease N Engl J Med 354 2006 1264 1272
37. K. Musunuru, B.G. Kral, and R.S. Blumenthal The use of high-sensitivity assays for C-reactive protein in clinical practice Nat Clin Pract Cardiovasc Med 5 2008 621 635
38. P.M. Ridker, M. Cushman, M.J. Stampfer, R.P. Tracy, and C.H. Hennekens Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men N Engl J Med 336 1997 973 979
39. P.M. Ridker, N. Rifai, L. Rose, J.E. Buring, and N.R. Cook Comparison of C-reactive protein and low-density lipoprotein cholesterol levels in the prediction of first cardiovascular events N Engl J Med 347 2002 1557 1565
40. D.I. Buckley, R. Fu, M. Freeman, K. Rogers, and M. Helfand C-reactive protein as a risk factor for coronary heart disease: a systematic review and meta-analyses for the U.S. Preventive Services Task Force Ann Intern Med 151 2009 483 495
41. U.S. Preventive Services Task Force Using nontraditional risk factors in coronary heart disease risk assessment: U.S. Preventive Services Task Force recommendation statement Ann Intern Med 151 2009 474 482
42. J. Danesh, J.G. Wheeler, and G.M. Hirschfield C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease N Engl J Med 350 2004 1387 1397
43. R. Kones Rosuvastatin, inflammation, C-reactive protein, JUPITER, and primary prevention of cardiovascular disease - a perspective Drug Des Devel Ther 4 2010 383 413
44. S. Woloshin, and L.M. Schwartz Distribution of C-reactive protein values in the United States N Engl J Med 352 2005 1611 1613
45. S. Kaptoge, E. Di Angelantonio, and L. Pennells C-reactive protein, fibrinogen, and cardiovascular disease prediction N Engl J Med 367 2012 1310 1320
46. J.K. Bower, M. Lazo, S.P. Juraschek, and E. Selvin Within-person variability in high-sensitivity C-reactive protein Arch Intern Med 172 2012 1519 1521
47. E.M. DeGoma, B. French, R.L. Dunbar, M.A. Allison, E.R. Mohler 3rd, and M.J. Budoff Intraindividual variability of C-reactive protein: the Multi-Ethnic Study of Atherosclerosis Atherosclerosis 224 2012 274 279
48. S. Kaptoge, E. Di Angelantonio, and G. Lowe C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis Lancet 375 2010 132 140
49. N.K. Gupta, J.A. de Lemos, C.R. Ayers, S.M. Abdullah, D.K. McGuire, and A. Khera The relationship between C-reactive protein and atherosclerosis differs on the basis of body mass index: the Dallas Heart Study J Am Coll Cardiol 60 2012 1148 1155
50. M.J. Blaha, J.J. Rivera, and M.J. Budoff Association between obesity, high-sensitivity C-reactive protein ≥2 mg/L, and subclinical atherosclerosis: implications of JUPITER from the Multi-Ethnic Study of Atherosclerosis Arterioscler Thromb Vasc Biol 31 2011 1430 1438
51. P.M. Ridker, E. Danielson, and F.A. Fonseca Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein N Engl J Med 359 2008 2195 2207
52. R. Detrano, A.D. Guerci, and J.J. Carr Coronary calcium as a predictor of coronary events in four racial or ethnic groups N Engl J Med 358 2008 1336 1345
53. R. Blankstein, M.J. Budoff, and L.J. Shaw Predictors of coronary heart disease events among asymptomatic persons with low low-density lipoprotein cholesterol: MESA (Multi-Ethnic Study of Atherosclerosis) J Am Coll Cardiol 58 2011 364 374
54. Y. Arad, K.J. Goodman, M. Roth, D. Newstein, and A.D. Guerci Coronary calcification, coronary disease risk factors, C-reactive protein, and atherosclerotic cardiovascular disease events: the St. Francis Heart Study J Am Coll Cardiol 46 2005 158 165
55. J.A. de Lemos, M.A. Blazing, and S.D. Wiviott Early intensive vs a delayed conservative simvastatin strategy in patients with acute coronary syndromes: phase Z of the A to Z trial JAMA 292 2004 1307 1316
56. S. Mohlenkamp, N. Lehmann, and S. Moebus Quantification of coronary atherosclerosis and inflammation to predict coronary events and all-cause mortality J Am Coll Cardiol 57 2011 1455 1464
57. R. Park, R. Detrano, and M. Xiang Combined use of computed tomography coronary calcium scores and C-reactive protein levels in predicting cardiovascular events in nondiabetic individuals Circulation 106 2002 2073 2077
58. G.C. Brooks, M.J. Blaha, and R.S. Blumenthal Relation of C-reactive protein to abdominal adiposity Am J Cardiol 106 2010 56 61
59. C.E. Ndumele, K. Nasir, R.D. Conceicao, J.A. Carvalho, R.S. Blumenthal, and R.D. Santos Hepatic steatosis, obesity, and the metabolic syndrome are independently and additively associated with increased systemic inflammation Arterioscler Thromb Vasc Biol 31 2011 1927 1932
60. M.A. Albert, R.J. Glynn, and P.M. Ridker Alcohol consumption and plasma concentration of C-reactive protein Circulation 107 2003 443 447
61. P.M. Ridker, J.E. Buring, N. Rifai, and N.R. Cook Development and validation of improved algorithms for the assessment of global cardiovascular risk in women: the Reynolds risk score JAMA 297 2007 611 619
62. B. Zethelius, L. Berglund, and J. Sundstrom Use of multiple biomarkers to improve the prediction of death from cardiovascular causes N Engl J Med 358 2008 2107 2116
63. I.M. van der Meer, M.P. de Maat, A.J. Kiliaan, D.A. van der Kuip, A. Hofman, and J.C. Witteman The value of C-reactive protein in cardiovascular risk prediction: the Rotterdam Study Arch Intern Med 163 2003 1323 1328
64. M.G. Shlipak, L.F. Fried, and M. Cushman Cardiovascular mortality risk in chronic kidney disease: comparison of traditional and novel risk factors JAMA 293 2005 1737 1745
65. P.W. Wilson, B.H. Nam, M. Pencina, R.B. D'Agostino Sr., E.J. Benjamin, and C.J. O'Donnell C-reactive protein and risk of cardiovascular disease in men and women from the Framingham Heart Study Arch Intern Med 165 2005 2473 2478
66. M.K. Rutter, J.B. Meigs, L.M. Sullivan, R.B. D'Agostino Sr., and P.W. Wilson C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study Circulation 110 2004 380 385
67. W. Koenig, H. Lowel, J. Baumert, and C. Meisinger C-reactive protein modulates risk prediction based on the Framingham score: implications for future risk assessment: results from a large cohort study in southern Germany Circulation 109 2004 1349 1353
68. D.M. Lloyd-Jones, K. Liu, L. Tian, and P. Greenland Narrative review: assessment of C-reactive protein in risk prediction for cardiovascular disease Ann Intern Med 145 2006 35 42
69. A.R. Folsom, L.E. Chambless, and C.M. Ballantyne An assessment of incremental coronary risk prediction using C-reactive protein and other novel risk markers: the Atherosclerosis Risk in Communities Study Arch Intern Med 166 2006 1368 1373
70. O. Melander, C. Newton-Cheh, and P. Almgren Novel and conventional biomarkers for prediction of incident cardiovascular events in the community JAMA 302 2009 49 57
71. J. Yeboah, R.L. McClelland, and T.S. Polonsky Comparison of novel risk markers for improvement in cardiovascular risk assessment in intermediate-risk individuals JAMA 308 2012 788 795
72. M. Kavousi, S. Elias-Smale, and J.H. Rutten Evaluation of newer risk markers for coronary heart disease risk classification: a cohort study Ann Intern Med 156 2012 438 444
73. A.P. DeFilippis, M.J. Blaha, and C.E. Ndumele The association of Framingham and Reynolds risk scores with incidence and progression of coronary artery calcification in MESA (Multi-Ethnic Study of Atherosclerosis) J Am Coll Cardiol 58 2011 2076 2083
74. P.M. Ridker, N.P. Paynter, N. Rifai, J.M. Gaziano, and N.R. Cook C-reactive protein and parental history improve global cardiovascular risk prediction: the Reynolds risk score for men Circulation 118 2008 2243 2251
75. N.R. Cook, J.E. Buring, and P.M. Ridker The effect of including C-reactive protein in cardiovascular risk prediction models for women Ann Intern Med 145 2006 21 29
76. P.W. Wilson, M. Pencina, P. Jacques, J. Selhub, R. D'Agostino Sr., and C.J. O'Donnell C-reactive protein and reclassification of cardiovascular risk in the Framingham Heart Study Circ Cardiovasc Qual Outcomes 1 2008 92 97
77. P.M. Ridker, N. Rifai, and M. Clearfield Measurement of C-reactive protein for the targeting of statin therapy in the primary prevention of acute coronary events N Engl J Med 344 2001 1959 1965
78. N. Sattar, H.M. Murray, and A. McConnachie C-reactive protein and prediction of coronary heart disease and global vascular events in the Prospective Study of Pravastatin in the Elderly at Risk (PROSPER) Circulation 115 2007 981 989
79. E.Y. Yang, V. Nambi, and Z. Tang Clinical implications of JUPITER (Justification for the Use of Statins in Prevention: an Intervention Trial Evaluating Rosuvastatin) in a U.S. population: insights from the ARIC (Atherosclerosis Risk in Communities) study J Am Coll Cardiol 54 2009 2388 2395
80. S. Kaul, R.P. Morrissey, and G.A. Diamond By Jove! What is a clinician to make of JUPITER? Arch Intern Med 170 2010 1073 1077
81. M. de Lorgeril, P. Salen, and J. Abramson Cholesterol lowering, cardiovascular diseases, and the rosuvastatin-JUPITER controversy: a critical reappraisal Arch Intern Med 170 2010 1032 1036
82. P.M. Ridker, and R.J. Glynn The JUPITER trial: responding to the critics Am J Cardiol 106 2010 1351 1356
83. T.J. Wang Assessing the role of circulating, genetic, and imaging biomarkers in cardiovascular risk prediction Circulation 123 2011 551 565
84. Heart Protection Study Collaborative Group C-reactive protein concentration and the vascular benefits of statin therapy: an analysis of 20,536 patients in the Heart Protection Study Lancet 377 2011 469 476
85. P.M. Ridker, J. MacFadyen, P. Libby, and R.J. Glynn Relation of baseline high-sensitivity C-reactive protein level to cardiovascular outcomes with rosuvastatin in the Justification for Use of Statins in Prevention: an Intervention Trial Evaluating Rosuvastatin (JUPITER) Am J Cardiol 106 2010 204 209
86. P.S. Sever, N.R. Poulter, and C.L. Chang Evaluation of C-reactive protein prior to and on-treatment as a predictor of benefit from atorvastatin: observations from the Anglo-Scandinavian Cardiac Outcomes Trial Eur Heart J 33 2012 486 494
87. D.A. Morrow, J.A. de Lemos, and M.S. Sabatine Clinical relevance of C-reactive protein during follow-up of patients with acute coronary syndromes in the Aggrastat-to-Zocor trial Circulation 114 2006 281 288
88. S. van Wissen, M.D. Trip, T.J. Smilde, J. de Graaf, A.F. Stalenhoef, and J.J. Kastelein Differential hs-CRP reduction in patients with familial hypercholesterolemia treated with aggressive or conventional statin therapy Atherosclerosis 165 2002 361 366
89. M.A. Hlatky, P. Greenland, and D.K. Arnett Criteria for evaluation of novel markers of cardiovascular risk: a scientific statement from the American Heart Association Circulation 119 2009 2408 2416
90. M.J. Blaha, M.J. Budoff, and A.P. DeFilippis Associations between C-reactive protein, coronary artery calcium, and cardiovascular events: implications for the JUPITER population from MESA, a population-based cohort study Lancet 378 2011 684 692
91. N.K. Choudhry, A.R. Patrick, R.J. Glynn, and J. Avorn The cost-effectiveness of C-reactive protein testing and rosuvastatin treatment for patients with normal cholesterol levels J Am Coll Cardiol 57 2011 784 791
92. K.K. Lee, L.E. Cipriano, D.K. Owens, A.S. Go, and M.A. Hlatky Cost-effectiveness of using high-sensitivity C-reactive protein to identify intermediate- and low-cardiovascular-risk individuals for statin therapy Circulation 122 2010 1478 1487
93. P.M. Ridker Testing the inflammatory hypothesis of atherothrombosis: scientific rationale for the Cardiovascular Inflammation Reduction Trial (CIRT) J Thromb Haemost 7 Suppl 1 2009 332 339
94. P.M. Ridker, T. Thuren, A. Zalewski, and P. Libby Interleukin-1beta inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-Inflammatory Thrombosis Outcomes Study (CANTOS) Am Heart J 162 2011 597 605
95. J. Genest, R. McPherson, and J. Frohlich 2009 Canadian Cardiovascular Society/Canadian guidelines for the diagnosis and treatment of dyslipidemia and prevention of cardiovascular disease in the adult - 2009 recommendations Can J Cardiol 25 2009 567 579
96. P. Greenland, J.S. Alpert, and G.A. Beller 2010 ACCF/AHA guideline for assessment of cardiovascular risk in asymptomatic adults: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines J Am Coll Cardiol 56 2010 e50 103
97. G. Mancia, S. Laurent, and E. Agabiti-Rosei Reappraisal of European guidelines on hypertension management: a European Society of Hypertension Task Force document J Hypertens 27 2009 2121 2158
98. J. Perk, G. De Backer, and H. Gohlke European guidelines on cardiovascular disease prevention in clinical practice (version 2012). The Fifth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts). Developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR) Eur Heart J 33 2012 1635 1701