Insight into the nature of the CRP-coronary event association using Mendelian randomization

International Journal of Epidemiology

Volumn 35, Issue 4, 2006, Pages 922-931

  Casas, Juan P ^a,b   Shah, Tina ^a   Cooper, Jackie ^a   Hawe, Emma ^a   McMahon, Alex D ^c   Gaffney, Dairena ^d   Packard, Christopher J ^d   O'Reily, Denis S ^d   Juhan Vague, Irene ^e   Yudkin, John S ^f   Tremoli, Elena ^g,h   Margaglione, Maurizio ⁱ   Di Minno, Giovanni ⁱ   Hamsten, Anders ^j   Kooistra, Teake ^k   Stephens, Jeffrey W ^a   Hurel, Steven J ^l   Livingstone, Shona ^a   Colhoun, Helen M ^a   Miller, George J ^m   Bautista, Leonelo E ⁿ   Meade, Tom ^b   Sattar, Naveed ^d   Humphries, Steve E ^a   Hingorani, Aroon D ^a   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d GLASGOW ROYAL INFIRMARY   (United Kingdom)

^e TIMONE HOSPITAL   (France)

^f ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^g UNIVERSITY OF MILAN   (Italy)

^h CENTRO CARDIOLOGICO MONZINO   (Italy)

ⁱ CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^j KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^k TNO   (Netherlands)

^l MIDDLESEX HOSPITAL   (United Kingdom)

^m QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

ⁿ UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

more..

Author keywords

C reactive protein; Cardiovascular disease; Genetics; Meta analysis; Polymorphism

Indexed keywords

C REACTIVE PROTEIN; PYRIMIDINE NUCLEOTIDE;

CARDIOVASCULAR DISEASE; GENETICS; POLYMORPHISM; PROTEIN;

ARTICLE; CALCULATION; CONFIDENCE INTERVAL; CONFOUNDING VARIABLE; CORONARY ARTERY DISEASE; COVARIANCE; DISEASE ASSOCIATION; EUROPE; FATALITY; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HEART INFARCTION; HEREDITY; HOMOZYGOSITY; HUMAN; OBSERVATIONAL STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RISK ASSESSMENT;

C-REACTIVE PROTEIN; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HOMOZYGOTE; HUMANS; LINKAGE DISEQUILIBRIUM; MALE; MYOCARDIAL INFARCTION; ODDS RATIO; PHENOTYPE; POLYMORPHISM, GENETIC; RISK ASSESSMENT;

EID: 33748425073     PISSN: 03005771     EISSN: 14643685     Source Type: Journal    
DOI: 10.1093/ije/dyl041     Document Type: Article

References (74)

1. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 1997;336:973-79.
2. Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 2000;342:836-43.
3. Kuller LH, Tracy RP, Shaten J, Meilahn EN. Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study. Multiple Risk Factor Intervention Trial. Am J Epidemiol 1996;144:537-47.
4. Pearson TA, Mensah GA, Alexander RW, et al. Markers of inflammation and cardiovascular disease: Application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 2003;107:499-511.
5. Pepys MB, Hirschfield GM. C-reactive protein: A critical update. J Clin Invest 2003;111:1805-12.
6. Danesh J, Whincup P, Walker M, et al. Low grade inflammation and coronary heart disease: Prospective study and updated meta-analyses. BMJ 2000;321:199-204.
7. Freeman DJ, Norrie J, Caslake MJ, Gaw A, Ford I, Lowe GD et al. West of Scotland Corollary Prevention Study. C-reactive protein is an independent predictor of risk for the development of diabetes mellitus in the West of Scotland Coronary Prevention Study. Diabetes 2002;51:1596-600.
8. Sattar N, McConnachie A, O'Reilly D, Upton MN, Greer IA, Davey Smith G et al. Inverse association between birthweight and C-reactive protein concentrations in the MIDSPAN family study. Arterioscler Thromb Vasc Biol 2004;24:583-87.
9. Balk EM, Lau J, Goudas LC, Jordan HS, Kupelnick B, Kim LU et al. Effects of statins on nonlipid serum markers associated with cardiovascular disease: A systematic review. Ann Intern Med 2003;139:670-82.
10. Sjoholm A, Nystrom T. Endothelial inflammation in insulin resistance. Lancet 2005;365:610-12.
11. Morgan TH. Heredity and Sex. New York, USA: Columbia University Press, 1913.
12. Davey Smith G, Ebrahim S. 'Mendelian randomization': Can genetic epidemiology contribute to understanding environmental determinants of disease? Int J Epidemiol 2003;32:1-22.
13. Keavney B. Genetic epidemiological studies of coronary heart disease. Int J Epidemiol 2002;31:730-36.
14. Klerk M, Verhoef P, Clarke R, Blom HJ, Kok FJ, Schouten EG et al. MTHFR 677C→T polymorphism and risk of coronary heart disease: A meta-analysis. JAMA 2002;288:2023-31.
15. Wald DS, Law M, Morris JK. Homocysteine and cardiovascular disease: evidence on causality from a meta-analysis. BMJ 2002;325:1202.
16. Casas JP, Bautista LE, Smeeth L, Sharma P, Hingorani AD. Homocysteine and stroke: Evidence on a causal link from Mendelian randomisation. Lancet 2005;365:224-32.
17. Davey Smith G, Harbord R, Milton J, Ebrahim S, Sterne JA. Does elevated plasma fibrinogen increase the risk of coronary heart disease? Evidence from a meta-analysis of genetic association studies. Arterioscler Thromb Vasc Biol 2005;25:2228-33.
18. MacGregor AJ, Gallimore JR, Spector TD, Pepys MB. Genetic effects on baseline values of C-reactive protein and serum amyloid a protein: A comparison of monozygotic and dizygotic twins. Clin Chem 2004;50:130-34.
19. Pankow JS, Folsom AR, Cushman M, Borecki IB, Hopkins PN, Eckfeldt JH et al. Familial and genetic determinants of systemic markers of inflammation: The NHLBI family heart study. Atherosclerosis 2001;154:681-89.
20. D'Aiuto F, Casas JP, Shah T, Humphries SE, Hingorani AD, Tonetti M. C-reactive protein (+1444C>T) polymorphism is associated with enhanced acute release of inflammatory markers. Atherosclerosis 2005;179:413-17.
21. Brull DJ, Serrano N, Zito F, Jones L, Montgomery HE, Rumley A et al. A polymorphism in the human CRP gene influences basal and stimulated CRP levels: Implications for the prediction and pathogenesis of coronary heart disease. Arterioscler Thromb Vasc Biol 2003;23:2063-69.
22. Miller GJ, Bauer KA, Barzegar S, Foley AJ, Mitchell JP, Cooper JA et al. The effects of quality and timing of venepuncture on markers of blood coagulation in healthy middle-aged men. Thromb Haemost 1995;73:82-86.
23. The WOSCOPS Group. Baseline risk factors and their association with outcome in the West of Scotland Coronary Prevention Study. The West of Scotland Coronary Prevention Study Group. Am J Cardiol 1997;79:756-62.
24. Meade T, Zuhrie R, Cook C, Cooper J on behalf of MRC General Practice Research Framework. Bezafibrate in men with lower extremity arterial disease: Randomised controlled trial. BMJ 2002;325:1139.
25. Juhan-Vague I, Morange PE, Aubert H, Henry M, Aillaud MF, Alessi MC et al. Plasma thrombin-activatable fibrinolysis inhibitor antigen concentration and genotype in relation to myocardial infarction in the north and south of Europe. Arterioscler Thromb Vasc Biol 2002;22:867-73.
26. Colhoun HM, Rubens MB, Underwood SR, Fuller JH. The effect of type 1 diabetes mellitus on the gender difference in coronary artery calcification. J Am Coll Cardiol 2000,36:2160-67.
27. Dhamrait SS, Stephens JW, Cooper JA, Acharya J, Mani AR, Moore K et al. Cardiovascular risk in healthy men and markers of oxidative stress in Diabetics men are associated with common variation in the gene for uncoupling protein 2. Eur Heart J 2004;25:468-75.
28. Pearson TA, Blair SN, Daniels SR, Eckel RH, Fair JM, Fortmann SP et al. AHA Guidelines for Primary Prevention of Cardiovascular Disease and Stroke: 2002 Update: Consensus Panel Guide to Comprehensive Risk Reduction for Adult Patients Without Coronary or Other Atherosclerotic Vascular Diseases. American Heart Association Science Advisory and Coordinating Committee. Circulation 2002;106:388-91.
29. Tunstall-Pedoe H, Kuulasmaa K, Amouyel P, Arveiler D, Rajakangas AM, Pajak A. Myocardial infarction and coronary deaths in the World Health Organization MONICA Project. Registration procedures, event rates, and case-fatality rates in 38 populations from 21 countries in four continents. Circulation 1994;90:583-12.
30. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959;22: 719-48.
31. DerSimonian R, Laird NM. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88.
32. Shadish WR, Haddock CK. Combining estimates of effect size. In: Cooper H, Hedges LV (eds). The Handbook of Research Synthesis. New York: Rusell Sage Foundation, 1994, pp. 261-84.
33. Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining heterogeneity and combining results from several studies in a meta-analysis. In: Egger M, Davey Smith G, Altman DG (eds). Systematic Reviews in Health Care: Meta-Analysis in Context. London: BMJ Publications, 2001, pp. 285-312.
34. Danesh J, Wheeler JG, Hirschfield GM, Eda S, Eiriksdottir G, Rumley A et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med 2004;350:1387-97.
35. Altman DG, Bland JM. Interaction revisited: The difference between two estimates. BMJ 2003;326:219.
36. Russell AI, Cunninghame Graham DS, Shepherd C, Roberton CA, Whittaker J, Meeks J et al. Polymorphism at the C-reactive protein locus influences gene expression and predisposes to systemic lupus erythematosus. Hum Mol Genet 2004;13:137-47.
37. Kovacs A, Green F, Hansson LO, Lundman P, Samnegard A, Boquist S et al. A novel common single nucleotide polymorphism in the promoter region of the C-reactive protein gene associated with the plasma concentration of C-reactive protein. Atherosclerosis 2005;178:193-98.
38. Miller DT, Zee RY, Suk Danik J, Kozlowski P, Chasman DI, Lazarus R et al. Association of common CRP gene variants with CRP levels and cardiovascular events. Ann Hum Genet 2005;69:623-38.
39. Carlson CS, Aldred SF, Lee PK, Tracy RP, Schwartz SM, Rieder M et al. Polymorphisms within the C-reactive protein (CRP) promoter region are associated with plasma CRP levels. Am J Hum Genet 2005;77:64-77.
40. Davey Smith G, Lawlor DA, Harbord R, et al. Association of C-reactive protein with blood pressure and hypertension. Life course confounding and Mendelian randomization tests of causality. Arterioscler Thromb Vasc Biol 2005;25:1051-56.
41. Woodward M, Rumley A, Lowe GD, Tunstall-Pedoe H. C-reactive protein: associations with haematological variables, cardiovascular risk factors and prevalent cardiovascular disease. Br J Haematol 2003;122:135-41.
42. Hackam DG, Anand SS. Emerging risk factors for atherosclerotic vascular disease: A critical review of the evidence. JAMA 2003;290:932-40.
43. Primatesta P, Falaschetti E, Poulter NR. Influence of hormone replacement therapy on C-reactive protein: Population-based data. J Cardiovasc Risk 2003;10:57-60.
44. Bautista LE. Inflammation, endothelial dysfunction, and the risk of high blood pressure: Epidemiologic and biological evidence. J Hum Hypertens 2003;17:223-30.
45. Saito M, Ishimitsu T, Minami J, Ono H, Ohrui M, Matsuoka H. Relations of plasma high-sensitivity C-reactive protein to traditional cardiovascular risk factors. Atherosclerosis 2003;167:73-79.
46. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. Elevated C-reactive protein levels in overweight and obese adults. JAMA 1999;282:2131-35.
47. Stewart SH, Mainous AG III, Gilbert G. Relation between alcohol consumption and C-reactive protein levels in the adult US population. J Am Board Fam Pract 2002;15:437-42.
48. Bautista LE, Smeeth L, Hingorani AD, Casas JP. Estimation of bias in non-genetic observational studies using 'Mendelian triangulation'. Ann Epidemiol 2006. In Press.
49. Davey Smith G, Harbord R, Ebrahim S. Fibrinogen, C-reactive protein and coronary heart disease: Does Mendelian randomization suggest the associations are non-causal? QJM 2004;97:163-66.
50. Zee RY, Ridker PM. Polymorphism in the human C-reactive protein (CRP) gene, plasma concentrations of CRP, and the risk of future arterial thrombosis. Atherosclerosis 2002;162:217-19.
51. KWJ Lee, J Hill, J Frohlich. C-reactive protein as a predictor of clinical outcomes in patients with coronary atherosclerosis. (Oral session young investigator award). Canadian Cardiovascular Congress, 2002.
52. Goldstein DB, Ahmadi KR, Weale ME, Wood NW. Genome scans and candidate gene approaches in the study of common diseases and variable drug responses. Trends Genet 2003;19:615-22.
53. SeattleSNPs. NHLBI Program for Genomic Applications, SeattleSNPs, Seattle, WA. (http://pga.gs.washington.edu) (Accessed May 1, 2005).
54. Szalai AJ, Wu J, Lange EM, McCrory MA, Langefeld CD, Williams A et al. Single-nucleotide polymorphisms in the C-reactive protein (CRP) gene promoter that affect transcription factor binding, alter transcriptional activity, and associate with differences in baseline serum CRP level. J Mol Med 2005;83:440-47.
55. Timpson NJ, Lawlor DA, Harbord RM, Gaunt TR, Day IN, Palmer LJ et al. C-reactive protein and its role in metabolic syndrome: Mendelian randomisation study. Lancet 2005;366: 1954-59.
56. Verma S, Kuliszewski MA, Li SH, Szmitko PE, Zucco L, Wang CH et al. C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and function: Further evidence of a mechanistic link between C-reactive protein and cardiovascular disease. Circulation 2004;109:2058-67.
57. Li SH, Szmitko PE, Weisel RD, Wang CH, Fedak PW, Li RK et al. C-reactive protein upregulates complement-inhibitory factors in endothelial cells. Circulation 2004;109:833-36.
58. Wang CH, Li SH, Weisel RD, Fedak PW, Dumont AS, Szmitko P et al. C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle. Circulation 2003;107:1783-90.
59. Verma S, Wang CH, Li SH, Dumont AS, Fedak PW, Badiwala MV et al. A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 2002;106:913-19.
60. Pasceri V, Willerson JT, Yeh ET. Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation 2000;102:2165-68.
61. Pasceri V, Cheng JS, Willerson JT, Yeh ET. Modulation of C-reactive protein-mediated monocyte chemoattractant protein-1 induction in human endothelial cells by anti-atherosclerosis drugs. Circulation 2001;103:2531-34.
62. Taylor KE, Giddings JC, van den Berg CW. C-Reactive protein-induced in vitro endothelial cell activation is an artefact caused by azide and lipopolysaccharide. Arterioscler Thromb Vasc Biol 2005;25:1225-30.
63. Lafuente N, Azcutia V, Matesanz N, Cercas E, Rodriguez-Manas L, Sanchez-Ferrer CF et al. Evidence for sodium azide as an artifact mediating the modulation of inducible nitric oxide synthase by C-reactive protein. J Cardiovasc Pharmacol 2005;45:193-96.
64. van den Berg CW, Taylor KE, Lang D. C-reactive protein-induced in vitro vasorelaxation is an artefact caused by the presence of sodium azide in commercial preparations. Arterioscler Thromb Vasc Biol 2004;24:e168-71.
65. Swafford AN Jr, Bratz IN, Knudson JD, Rogers PA, Timmerman JM, Tune JD et al. C-reactive protein does not relax vascular smooth muscle: Effects mediated by sodium azide in commercially available preparations. Am J Physiol Heart Circ Physiol 2005;288:H1786-95.
66. Clapp BR, Hirschfield GM, Storry C, Gallimore JR, Stidwill RP, Singer M et al. Inflammation and endothelial function: Direct vascular effects of human C-reactive protein on nitric oxide bioavailability. Circulation 2005;111:1530-36.
67. van den Berg CW, Taylor KE. Letter Regarding Article by Li et al, "C-Reactive Protein Upregulates Complement-Inhibitory Factors in Endothelial Cells". Circulation 2004;110:e542.
68. Liu C, Wang S, Deb A, Nath KA, Katusic ZS, McConnell JP et al. Proapoptotic, antimigratory, antiproliferative, and antiangiogenic effects of commercial C-reactive protein on various human endothelial cell types in vitro: Implications of contaminating presence of sodium azide in commercial preparation. Circ Res 2005;97:135-43.
69. Nerurkar SS, McDevitt PJ, Scott GF, Johanson KO, Willette RN, Yue TL. Lipopolysaccharide (LPS) contamination plays the real role in C-reactive protein-induced IL-6 secretion from human endothelial cells in vitro. Arterioscler Thrfsomb Vasc Biol 2005;25:e136.
70. Pepys MB, Hawkins PN, Kahan MC, Tennent GA, Gallimore JR, Graham D et al. Proinflammatory effects of bacterial recombinant human C-reactive protein are caused by contamination with bacterial products, not by C-reactive protein itself. Circ Res 2005;97:e97-103.
71. Hirschfield GM, Gallimore JR, Kahan MC, Hutchinson WL, Sabin CA, Benson GM et al. Transgenic human C-reactive protein is not proatherogenic in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 2005;102:8309-14.
72. Reifenberg K, Lehr H-A, Baskal D, Wiese E, Schaefer SC, Black S et al. Role of C-reactive protein in atherogenesis. Can the apolipoprotein E knockout mouse provide the answer? Arterioscler Thromb Vasc Biol 2005;25:1641-46.
73. Trion A, de Maat MP, Jukema JW, van der Laarse A, Maas MC, Offerman EH et al. No effect of C-reactive protein on early atherosclerosis development in apolipoprotein E*3-Leiden/human C-reactive protein transgenic mice. Arterioscler Thromb Vasc Biol 2005;25:1635-40.
74. Pepys MB. CRP or not CRP? That is the question. Arterioscler Thromb Vasc Biol 2005;25:1091-94.