Inflammation and endothelial dysfunction are associated with retinopathy: The Hoorn Study

Diabetologia

Volumn 48, Issue 7, 2005, Pages 1300-1306

  Van Hecke, M V ^a,b   Dekker, J M ^b   Nijpels, G ^a,b   Moll, A C ^a,b   Heine, R J ^a,b   Bouter, L M ^b   Polak, B C P ^a,b   Stehouwer, C D A ^a,b,c  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Endothelial dysfunction; Inflammation; Retinopathy; Type 2 diabetes

Indexed keywords

ALBUMIN; C REACTIVE PROTEIN; CREATININE; INTERCELLULAR ADHESION MOLECULE 1; TRIACYLGLYCEROL; VASCULAR CELL ADHESION MOLECULE 1; VON WILLEBRAND FACTOR;

ADULT; AGED; ALBUMIN BLOOD LEVEL; ARTICLE; BODY MASS; CELL DAMAGE; CHOLESTEROL BLOOD LEVEL; COHORT ANALYSIS; CREATININE BLOOD LEVEL; DIASTOLIC BLOOD PRESSURE; DISEASE ASSOCIATION; ENDOTHELIUM LESION; FEMALE; GLUCOSE TOLERANCE TEST; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MYDRIASIS; NON INSULIN DEPENDENT DIABETES MELLITUS; OPHTHALMOLOGY; OPHTHALMOSCOPY; PATHOGENESIS; PHYSICAL EXAMINATION; PRIORITY JOURNAL; RETINOPATHY; RISK FACTOR; SYSTOLIC BLOOD PRESSURE;

AGED; BLOOD GLUCOSE; BLOOD PRESSURE; C-REACTIVE PROTEIN; CARDIOVASCULAR DISEASES; COHORT STUDIES; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; DIABETIC RETINOPATHY; ENDOTHELIUM, VASCULAR; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; NETHERLANDS; RETINAL DISEASES; RETINAL VESSELS;

EID: 23944492556     PISSN: 0012186X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00125-005-1799-y     Document Type: Article

References (45)

1. van Leiden HA, Dekker JM, Moll AC et al (2002) Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn study. Diabetes Care 25:1320-1325
2. Nagi DK, Pettitt DJ, Bennett PH, Klein R, Knowler WC (1997) Diabetic retinopathy assessed by fundus photography in Pima Indians with impaired glucose tolerance and NIDDM. Diabet Med 14:449-456
3. Stratton IM, Kohner EM, Aldington SJ et al (2001) UKPDS 50: risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia 44:156-163
4. Stehouwer CD, Lambert J, Donker AJ, van Hinsbergh VW (1997) Endothelial dysfunction and pathogenesis of diabetic angiopathy. Cardiovasc Res 34:55-68
5. Jager A, van Hinsbergh VW, Kostense PJ et al (2000) Increased levels of soluble vascular cell adhesion molecule 1 are associated with risk of cardiovascular mortality in type 2 diabetes: the Hoorn study. Diabetes 49:485-491
6. Jager A, van Hinsbergh VW, Kostense PJ et al (1999) Von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn study. Arterioscler Thromb Vasc Biol 19:3071-3078
7. Otsuki M, Hashimoto K, Morimoto Y, Kishimoto T, Kasayama S (1997) Circulating vascular cell adhesion molecule-1 (VCAM-1) in atherosclerotic NIDDM patients. Diabetes 46:2096-2101
8. Hwang SJ, Ballantyne CM, Sharrett AR et al (1997) Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) study. Circulation 96:4219-4225
9. Kado S, Nagata N (1999) Circulating intercellular adhesion molecule-1, vascular cell adhesion molecule-1, and E-selectin in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 46:143-148
10. Jager A, van Hinsbergh VW, Kostense PJ et al (2002) C-reactive protein and soluble vascular cell adhesion molecule-1 are associated with elevated urinary albumin excretion but do not explain its link with cardiovascular risk. Arterioscler Thromb Vasc Biol 22:593-598
11. Stehouwer CD, Gall MA, Twisk JW, Knudsen E, Emeis JJ, Parving HH (2002) 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 51:1157-1165
12. Cruickshanks KJ, Ritter LL, Klein R, Moss SE (1993) The association of microalbuminuria with diabetic retinopathy. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. Ophthalmology 100:862-867
13. Wirta O, Pasternack A, Mustonen J, Laippala P, Lahde Y (1999) Retinopathy is independently related to microalbuminuria in type 2 diabetes mellitus. Clin Nephrol 51:329-334
14. Crimi S, Cipolli D, Infantone E, Infantone L, Lunetta M (1995) Microalbuminuria and severity of diabetic retinopathy in type 1 diabetic patients: association and relationship with some risk factors. Diabetes Metab 21:440-445
15. Matsumoto K, Sera Y, Ueki Y, Inukai G, Niiro E, Miyake S (2002) Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabet Med 19:822-826
16. Fasching P, Veitl M, Rohac M et al (1996) Elevated concentrations of circulating adhesion molecules and their association with microvascular complications in insulin-dependent diabetes mellitus. J Clin Endocrinol Metab 81:4313-4317
17. Koga M, Otsuki M, Kubo M, Hashimoto J, Kasayama S (1998) Relationship between circulating vascular cell adhesion molecule-1 and microvascular complications in type 2 diabetes mellitus. Diabet Med 15:661-667
18. Beks PJ, Mackaay AJ, de Neeling JN, de Vries H, Bouter LM, Heine RJ (1995) Peripheral arterial disease in relation to glycaemic level in an elderly Caucasian population: the Hoorn study. Diabetologia 38:86-96
19. World Health Organization (1999). Definition, diagnosis and classification of diabetes mellitus and its complications. Report of a WHO consultation, Part 1: diagnosis and classification of diabetes mellitus. World Health Organization, Geneva
20. Hoogeveen EK, Kostense PJ, Beks PJ et al (1998) Hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, especially in non-insulin-dependent diabetes mellitus: a population-based study. Arterioscler Thromb Vasc Biol 18:133-138
21. Aldington SJ, Kohner EM, Meuer S, Klein R, Sjolie AK (1995) Methodology for retinal photography and assessment of diabetic retinopathy: the EURODIAB IDDM complications study. Diabetologia 38:437-444
22. Becker A, van Hinsbergh VW, Jager A et al (2002) Why is soluble intercellular adhesion molecule-1 related to cardiovascular mortality? Eur J Clin Invest 32:1-8
23. Jager A, Kostense PJ, Ruhe HG et al (1999) Microalbuminuria and peripheral arterial disease are independent predictors of cardiovascular and all-cause mortality, especially among hypertensive subjects: five-year follow-up of the Hoorn study. Arterioscler Thromb Vasc Biol 19:617-624
24. Hoogeveen EK, Kostense PJ, Eysink PE et al (2000) Hyperhomocysteinemia is associated with the presence of retinopathy in type 2 diabetes mellitus: the Hoorn study. Arch Intern Med 160:2984-2990
25. Anonymous (1997) The sixth report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure. Arch Intern Med 157:2413-2446
26. Ross R (1999) Atherosclerosis - an inflammatory disease. N Engl J Med 340:115-126
27. Schalkwijk CG, Poland DC, van Dijk W et al (1999) 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 42:351-357
28. Jude EB, Douglas JT, Anderson SG, Young MJ, Boulton AJ (2002) Circulating cellular adhesion molecules ICAM-1, VCAM-1, P- and E-selectin in the prediction of cardiovascular disease in diabetes mellitus. Eur J Intern Med 13:185-189
29. van der Meer IM, de Maat MP, Bots ML et al (2002) Inflammatory mediators and cell adhesion molecules as indicators of severity of atherosclerosis: the Rotterdam Study. Arterioscler Thromb Vasc Biol 22:838-842
30. McLeod DS, Lefer DJ, Merges C, Lutty GA (1995) Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol 147:642-653
31. Bonetti PO, Lerman LO, Lerman A (2003) Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 23:168-175
32. Stehouwer CD, Fischer HR, van Kuijk AW, Polak BC, Donker AJ (1995) Endothelial dysfunction precedes development of microalbuminuria in IDDM. Diabetes 44:561-564
33. Feng D, Bursell SE, Clermont AC et al (2000) von Willebrand factor and retinal circulation in early-stage retinopathy of type 1 diabetes. Diabetes Care 23:1694-1698
34. Stehouwer CD, Zellenrath P, Polak BC et al (1992) von Willebrand factor and early diabetic retinopathy: no evidence for a relationship in patients with type 1 (insulin-dependent) diabetes mellitus and normal urinary albumin excretion. Diabetologia 35:555-559
35. Rajala U, Laakso M, Qiao Q, Keinanen-Kiukaanniemi S (1998) Prevalence of retinopathy in people with diabetes, impaired glucose tolerance, and normal glucose tolerance. Diabetes Care 21:1664-1669
36. Yu T, Mitchell P, Berry G, Li W, Wang JJ (1998) Retinopathy in older persons without diabetes and its relationship to hypertension. Arch Ophthalmol 116:83-89
37. Adamis AP (2002) Is diabetic retinopathy an inflammatory disease? Br J Ophthalmol 86:363-365
38. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW (2002) Diabetic retinopathy: more than meets the eye. Surv Ophthalmol 47(Suppl 2):S253-S262
39. Joussen AM, Poulaki V, Qin W et al (2002) Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol 160:501-509
40. Barouch FC, Miyamoto K, Allport JR et al (2000) Integrin-mediated neutrophil adhesion and retinal leukostasis in diabetes. Invest Ophthalmol Vis Sci 41:1153-1158
41. Miyamoto K, Khosrof S, Bursell SE et al (1999) Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A 96:10836-10841
42. Olson JA, Whitelaw CM, McHardy KC, Pearson DW, Forrester JV (1997) Soluble leucocyte adhesion molecules in diabetic retinopathy stimulate retinal capillary endothelial cell migration. Diabetologia 40:1166-1171
43. Kohner EM, Patel V, Rassam SM (1995) Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44:603-607
44. Blake GJ, Ridker PM (2001) Novel clinical markers of vascular wall inflammation. Circ Res 89:763-771
45. Meigs JB, Hu FB, Rifai N, Manson JE (2004) Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus. JAMA 291:1978-1986