Cross-sectional associations of C-reactive protein with vascular risk factors and vascular complications in the DCCT/EDIC cohort

Journal of Diabetes and its Complications

Volumn 22, Issue 3, 2008, Pages 153-163

  Jenkins, Alicia J ^a,b,c   Rothen, Michelle ^a   Klein, Richard L ^a   Moller, Karina ^a   Eldridge, Leslie ^a   Zheng, Deyi ^a   Durazo Arvizu, Ramon ^a   McGee, Daniel ^a   Lackland, Daniel ^a   Thorpe, Suzanne R ^d   Garvey, W Timothy ^a   Lyons, Timothy J ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

C Reactive protein; Complications; Inflammation; Type 1 diabetes

Indexed keywords

ACETYLSALICYLIC ACID; C REACTIVE PROTEIN; HEMOGLOBIN A1C; LOW DENSITY LIPOPROTEIN; ORAL CONTRACEPTIVE AGENT;

ADULT; ARTICLE; BODY MASS; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; FEMALE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; NEPHELOMETRY; PARTICLE SIZE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RISK FACTOR; SYSTOLIC BLOOD PRESSURE; VASCULAR DISEASE; WAIST HIP RATIO;

ADULT; C-REACTIVE PROTEIN; COHORT STUDIES; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; HYPERTENSION; LIPIDS; MALE; RISK FACTORS; SEX CHARACTERISTICS;

EID: 42149105264     PISSN: 10568727     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdiacomp.2007.02.003     Document Type: Article

References (74)

1. Albert C.M., Ma J., Rifai N., Stampfer M.J., and Ridker P.M. Prospective study of C-reactive protein, homocysteine, and plasma lipid levels as predictors of sudden cardiac death. Circulation 105 22 (2002) 2595-2599
2. American Diabetes Association. Diabetes complications. Diabetes 1996: Vital Statistics (1996), American Diabetes Association, Alexandria, VA 29-44
3. Araki A., and Sako Y. Determination of free and total homocysteine in human plasma by high-performance liquid chromatography with fluorescence detection. Journal of Chromatography 422 (1987) 43-52
4. Atabek M.E., Pirgon O., Kurtoglu S., and Imamoglu H. Evidence for an association between type 1 diabetes and premature carotid atherosclerosis in childhood. Pediatric Cardiology 27 4 (2006) 428-433
5. Bhakdi S., Torzewski M., Klouche M., and Hemmes M. Complement and atherogenesis: Binding of CRP to degraded, nonoxidized LDL enhances complement activation. Arteriosclerosis, Thrombosis, and Vascular Biology 19 10 (1999) 2348-2354
6. Colhoun H.M., Schalkwijk C., Rubens M.B., and Stehouwer C.D. C-Reactive protein in type 1 diabetes and its relationship to coronary artery calcification. Diabetes Care 25 10 (2002) 1813-1817
7. Costacou T., Zgibor J.C., Evans R.W., Otvos J., Lopes-Virella M.F., Tracy R.P., and Orchard T.J. The prospective association between adiponectin and coronary artery disease among individuals with type 1 diabetes. The Pittsburgh Epidemiology of Diabetes Complications Study. Diabetologia 48 (2005) 41-48
8. Devaraj S., Glaser N., Griffen S., Wang-Polagruto J., Miguelino E., and Jialal I. Increased monocytic activity and biomarkers of inflammation in patients with type 1 diabetes. Diabetes 55 3 (2006) 774-779
9. Epidemiology of Diabetes Interventions and Complications (EDIC). Design, implementation, and preliminary results of a long-term follow-up of the Diabetes Control and Complications Trial cohort. Diabetes Care 22 (1999) 99-111
10. Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group. Effect of intensive diabetes treatment on carotid artery wall thickness in the Epidemiology of Diabetes Interventions and Complications. Diabetes 48 (1999) 383-390
11. Erlandsen E.J., and Randers E. Reference interval for serum C-reactive protein in healthy blood donors using the Dade Behring N Latex CRP mono assay. Scandinavian Journal of Clinical and Laboratory Investigation 60 (2000) 37-43
12. Ford E.S. Body mass index, diabetes, and C-reactive protein among U.S. adults. Diabetes Care 22 (1999) 1971-1977
13. Ford E.S., and Giles W.H. Serum C-reactive protein and fibrinogen concentrations and self-reported angina pectoris and myocardial infarction (findings from the National Health and Nutrition Examination Survey III). Journal of Clinical Epidemiology 53 (2000) 95-102
14. Freeman D.J., Norrie J., Caslake M.J., Gaw A., Ford I., Lowe G.D., O'Reilly D.S., Packard C.J., Sattar N., and West of Scotland Coronary Prevention Study. C-Reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes 51 5 (2002) 1596-1600
15. Fyfe A.I., Rothenberg L.S., DeBeer F.C., Cantor R.M., Rotter J.I., and Lusis A.J. Association between serum amyloid A proteins and coronary artery disease: Evidence from two distinct arteriosclerotic processes. Circulation 96 (1997) 2914-2919
16. Garvey W.T., Kwon S., Zheng D., Shaughnessy S., Wallace P., Hutto A., Pugh K., Jenkins A.J., Klein R.L., and Liao Y. Effects of insulin resistance and type 2 diabetes on lipoprotein subclass particle size and concentration determined by nuclear magnetic resonance. Diabetes 52 2 (2003) 453-462
17. Giese M., Lackland D., Basile J., and Egan B. 2003 update on the Hypertension Initiative of South Carolina. Bringing South Carolina from "worst to first" in cardiovascular health. Journal of the South Carolina Medical Association 99 6 (2003) 157-161
18. Gunn M., Stephens J.C., Thompson J.R., Rathbone B.J., and Samani N.J. Significant association of sera positive Helicobacter pylori strains with risk of premature myocardial infarction. Heart 84 3 (2000) 267-271
19. Gunczler P., Lanes R., Soros A., Verdu L., Ramon Y., Guevara B., and Beer N. Coronary artery calcification, serum lipids, lipoproteins, and peripheral inflammatory markers in adolescents and young adults with type 1 diabetes. Journal of Pediatrics 149 3 (2006) 320-323
20. Hayaishi-Okano R., Yamasaki Y., Katakami N., Ohtoshi K., Gorogawa S., Kuroda A., Matshuisa M., Kosugi K., Nishikawa N., Kajimoto Y., and Hori M. Elevated C-reactive protein associates with early-stage carotid atherosclerosis in young subjects with type 1 diabetes. Diabetes Care 25 8 (2002) 1432-1438
21. Heliovaara M.K., Teppo A.M., Karonen S.L., Tuominen J.A., and Ebeling P. Improved glycaemia in type 1 diabetes results in decreased levels of soluble adhesion molecules with no change in serum adiponectin or most acute phase proteins. Experimental and Clinical Endocrinology & Diabetes 114 6 (2006) 295-300
22. Hotamisligil G.S., Arner P., Caro J.F., Atkinson R.L., and Spiegelman B.M. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. Journal of Clinical Investigation 95 (1995) 2409-2415
23. Ikeda U., Ito T., and Shimada K. Statins and C-reactive protein. Lancet 353 (1999) 1274-1275
24. Jenkins A.J., Lyons T.J., Zheng D., Otvos J.D., Lackland D.T., McGee D., Garvey W.T., Klein R.L., and DCC/EDIC Research Group. Serum lipoproteins in the Diabetes Control and Complications Trial/Epidemiology of Diabetes Intervention and Complications cohort: Associations with gender and glycemia. Diabetes Care 26 3 (2003) 810-818
25. Jenkins A.J., Best J.D., Klein R.L., and Lyons T.J. Lipoproteins, glycoxidation and diabetic angiopathy. Diabetes/Metabolism Research and Reviews 20 5 (2004) 349-368
26. Kannel W.B., and McGee D.L. Diabetes and cardiovascular disease. The Framingham Study. Journal of the American Medical Association 241 (1979) 2035-2038
27. Kilpatrick E.S., Keevil B.G., Jagger C., Spooner R.J., and Small M. Determinants of raised C-reactive protein concentration in type 1 diabetes. Quarterly Journal of Medicine 93 (2000) 231-236
28. Klein R.L., Hunter S.J., Jenkins A.J., Zheng D., Semler A.J., Clore J., Garvey W.T., and DCCT/ECIC Study Group. Fibrinogen is a marker for nephropathy and peripheral vascular disease in type 1 diabetes: Studies of plasma fibrinogen and fibrinogen gene polymorphism in the DCCT/EDIC cohort. Diabetes Care 26 5 (2003) 1439-1448
29. Koenig W. Fibrin(ogen) in cardiovascular disease: An update. Thrombosis and Haemostasis 89 4 (2003) 601-609
30. Koenig W., Sund M., Frohlich M., Fischer H.G., Lowel H., Doring A., Hutchinson W.L., and Pepys M.B. C-Reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: Results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation 99 2 (1992) 237-242
31. Ladeia A.M., Stefanelli E., Ladeia-Frota C., Moreira A., Hiltner A., and Adan L. Association between elevated serum C-reactive protein and triglyceride levels in young subjects with type 1 diabetes. Diabetes Care 29 2 (2006) 424-426
32. Lee W.Y., Park J.S., Noh S.Y., Rhee E.J., Sung K.C., Kim B.S., Kang J.H., Kim S.W., Lee M.H., and Park J.R. C-Reactive protein concentrations are related to insulin resistance and metabolic syndrome as defined by the ATP III report. International Journal of Cardiology 97 1 (2004) 101-106
33. Loesche W.J. Periodontal infection a risk factor for cardiovascular disease. Postgraduate Medicine 107 (2001) 17-20
34. Loukovaara S., Immonen I., Koistinen R., Hiilesmaa V., and Kaaja R. Inflammatory markers and retinopathy in pregnancies complicated with type I diabetes. Eye 19 4 (2005) 422-430
35. Mackness B., Hine D., McElduff P., and Mackness M. High C-reactive protein and low paraoxonase1 in diabetes as risk factors for coronary heart disease. Atherosclerosis 186 2 (2006) 396-401
36. Mangge H., Schauenstein K., Stroedter L., Griesl A., Maerz W., and Borkenstein M. Low grade inflammation in juvenile obesity and type 1 diabetes associated with early signs of atherosclerosis. Experimental and Clinical Endocrinology & Diabetes 112 7 (2004) 378-382
37. McMillan D.E. Increased levels of acute phase serum proteins in diabetes. Metabolism 38 (1989) 1042-1046
38. Mendall M.A., Patel P., Ballam L., Strachan D., and Northfield T.C. CRP and its relation to cardiovascular risk factors: A population based cross sectional study. British Medical Journal 312 (1996) 1061-1065
39. Nakagomi A., Freedman S.B., and Geezy C.L. Interferon-γ and lipopolysaccharide potentiate monocyte tissue factor induction by c-reactive protein: Relationship with age, sex, and hormone replacement. Circulation 101 (2000) 1785-1791
40. Olson J.C., Erbey J.R., Forrest K.Y., Williams K., Becker D.J., and Orchard T.J. Glycemia (or, in women, estimated glucose disposal rate) predict lower extremity arterial disease events in type 1 diabetes. Metabolism 51 2 (2002) 248-254
41. Olson J.C., Erbey J.R., Williams K.V., Becker D.J., Edmundowicz D., Kelsey S.F., Tyrrell K.S., and Orchard T.J. Subclinical atherosclerosis and estimated glucose disposal rate as predictors of mortality in type 1 diabetes. Annals of Epidemiology 12 5 (2002) 331-337
42. Orchard T.J., Chang Y.F., Ferrell R.E., Petro N., and Ellis D.E. Nephropathy in type 1 diabetes: A manifestation of insulin resistance and multiple genetic susceptibilities? Further evidence from the Pittsburgh Epidemiology of Diabetes Complication Study. Kidney International 62 3 (2002) 963-970
43. Orchard T.J., Olson J.C., Erbey J.R., Williams K., Forrest K.Y., Smithline Kinder L., Ellis D., and Becker D.J. Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year follow-up data from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care 26 5 (2003) 1374-1379
44. Picardi A., Valorani M.G., Vespasiani Gentilucci U., Manfrini S., Ciofini O., Cappa M., Guglielmi C., and Pozzilli P. Raised C-reactive protein levels in patients with recent onset type 1 diabetes. Diabetes/Metabolism Research and Reviews (2006, Jul 11) (electronic publication ahead of print)
45. Purnell J.Q., Hokanson J.E., Marcovina S.M., Steffes M.W., Cleary P.A., and Brunzell J.D. Effect of excessive weight gain with intensive therapy of type 1 diabetes on lipid levels and blood pressure: Results from the DCCT. Diabetes Control and Complications Trial. Journal of the American Medical Association 280 2 (1998) 140-146
46. Purnell J.Q., Dev R.K., Steffes M.W., Cleary P.A., Palmer J.P., Hirsch I.B., Hokanson J.E., and Brunzell J.D. Relationship of family history of type 2 diabetes, hypoglycemia, and autoantibodies to weight gain and lipids with intensive and conventional therapy in the Diabetes Control and Complications Trial. Diabetes 52 10 (2003) 2623-2629
47. Pyorala K. Diabetes and heart disease. In: Mogensen C.E., and Standl E. (Eds). Prevention and treatment of the diabetic late complications (1989), Walter de Gruyter, New York 151-168
48. Ridker P.M. Inflammation, atherosclerosis, and cardiovascular risk: An epidemiologic view. Blood Coagulation & Fibrinolysis (1999) S9-S12
49. Ridker P.M., Cushman M., Stamfer M.J., Tracy R.P., and Hennekens C.H. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. New England Journal of Medicine 336 (1997) 973-979
50. Ridker P.M., Cushman M., Stampfer M.J., Tracy R.P., and Hennekens C.H. Plasma concentration of C-reactive protein and risk of developing peripheral vascular disease. Circulation 97 (1998) 425-428
51. Ridker P.M., Hennekens C.H., Buring J.E., and Rifai N. C-Reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. New England Journal of Medicine 342 (2000) 836-843
52. Rohde L.E.P., Hennekens C.H., and Ridker P.M. Survey of C-reactive protein and cardiovascular risk factors in apparently healthy men. American Journal of Cardiology 84 (1999) 1018-1022
53. Rojas R., Gomez-Perez F.J., Mehta R., Franco A., Olaiz G., and Rull J.A. The metabolic syndrome: A concept hard to define. Archives of Medical Research 36 3 (2005) 223-231
54. Saraheimo M., Teppo A.M., Forsblom C., Fagerudd J., and Groop P.H. Diabetic nephropathy is associated with low-grade inflammation in Type 1 diabetic patients. Diabetologia 46 10 (2003) 1402-1407
55. Schalkwijk C.G., Poland D.C.W., van Dijk W., Kok A., Emeis J.J., Dräger A.M., Doni A., van Hinsbergh V.W.M., and Stehouwer C.D.A. Plasma concentration of C-reactive protein is increased in Type I diabetic patients without clinical macroangiopathy and correlates with markers of endothelial dysfunction: Evidence for chronic inflammation. Diabetologia 42 (1999) 351-357
56. Schaumberg D.A., Glynn R.J., Jenkins A.J., Lyons T.J., Rifai N., Manson J.E., Ridker P.M., and Nathan D.M. Effect of intensive glycemic control on levels of markers of inflammation in type 1 diabetes mellitus in the Diabetes Control and Complications Trial. Circulation 111 19 (2005) 2446-2453
57. Scholin A., Siegbahn A., Lind L., Berne C., Sundkvist G., Bjork E., Karlsson F.A., and Diabetes Incidence Study in Sweden group. CRP and IL-6 concentrations are associated with poor glycemic control despite preserved beta-cell function during the first year after diagnosis of type 1 diabetes. Diabetes/Metabolism Research and Reviews 20 3 (2004) 205-210
58. Schram M.T., Chaturvedi N., Schalkwijk C.G., Fuller J.H., Stehouwer C.D., and EURODIAB Prospective Complications Study Group. Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes - the EURODIAB Prospective Complications Study. Diabetologia 48 2 (2005) 370-378
59. Shimada K., Mokuno H., Watanabe Y., Sawano M., Daida H., and Yamaguchi H. High prevalence of seropositivity for antibodies to Chlamydia-specific lipopolysaccharide in patients with acute coronary syndrome. Journal of Cardiovascular Risk 7 (2000) 209-213
60. Skrivarhaug T., Bangstad H.J., Stene L.C., Sandvik L., Hanssen K.F., and Joner G. Low risk of overt nephropathy after 24 yr of childhood-onset type 1 diabetes mellitus (T1DM) in Norway. Pediatric Diabetes 7 5 (2006) 239-246
61. Stehouwer C.D., Gall M.A., Twisk J.W., Knudsen E., Emeis J.J., and Parving H.H. Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: Progressive, interrelated, and independently associated with risk of death. Diabetes 51 4 (2002) 1157-1165
62. Strandberg T.E., and Tiluis R.S. C-Reactive protein, cardiovascular disease, and mortality in a prospective study in the elderly. Arteriosclerosis, Thrombosis, and Vascular Biology 20 (2000) 1057-1060
63. Streja D., Cressey P., and Rabkin S.W. Associations between inflammatory markers, traditional risk factors, and complications in patients with type 2 diabetes mellitus. Journal of Diabetes and its Complications 17 3 (2003) 120-127
64. Sundell J., Ronnemaa T., Laine H., Raitakari O.T., Luotolahti M., Nuutila P., and Knuuti J. High-sensitivity C-reactive protein and impaired coronary vasoreactivity in young men with uncomplicated type 1 diabetes. Diabetologia 47 11 (2004) 1888-1894
65. Superko H.R. New aspects of risk factors for the development of atherosclerosis, including small dense lipoprotein, homocyst(e)ine, and lipoprotein (a). Current Opinion in Cardiology 10 (1995) 347-354
66. Targher G., Bertolini L., Zoppini G., Zenari L., and Falezza G. Increased plasma markers of inflammation and endothelial dysfunction and their association with microvascular complications in Type 1 diabetic patients without clinically manifest macroangiopathy. Diabetic Medicine 22 8 (2005) 999-1004
67. The Diabetes Care and Complications Trial (DCCT) Research Group. Feasibility of centralized measurements of glycated hemoglobin in the Diabetes Control and Complications Trial: A multicenter study. Clinical Chemistry 33 (1987) 2267-2271
68. The Diabetes Care and Complications Trial (DCCT). The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New England Journal of Medicine 329 (1993) 977-986
69. The Diabetes Control and Complications Trial (DCCT) Research Group. The effect of intensive diabetes treatment on the progression of diabetic retinopathy in insulin-dependent diabetes mellitus: The Diabetes Control and Complications Trial. Archives of Ophthalmology 113 (1995) 36-51
70. Tracy R.P., Psaty B.M., Macy E., Bovill E.G., Cushman M., Cornell E.S., and Kuller L.H. Lifetime smoking exposure affects the association of C-reactive protein with cardiovascular disease risk factors and subclinical disease in healthy elderly subjects. Arteriosclerosis, Thrombosis, and Vascular Biology (1997) 2167-2176
71. van Hecke M.V., Dekker J.M., Nijpels G., Moll A.C., Heine R.J., Bouter L.M., Polak B.C., and Stehouwer C.D. Inflammation and endothelial dysfunction are associated with retinopathy: The Hoorn Study. Diabetologia 48 7 (2005) 1300-1306
72. Visser M., Bouter L.M., McQuillan G.M., Wener M.H., and Harris T.B. Elevated C-reactive protein levels in overweight and obese adults. Journal of the American Medical Association 282 22 (1999) 2131-2135
73. Whicher J., Biasucci L., and Rifai N. Inflammation, the acute phase response and atherosclerosis. Clinical Chemistry and Laboratory Medicine 37 (1999) 495-503
74. Williams K.V., Erbey J.R., Becker D., Arslanian S., and Orchard T.J. Can clinical factors estimate insulin resistance in type 1 diabetes?. Diabetes 49 4 (2000) 626-632