Are retinal microvascular abnormalities associated with large artery endothelial dysfunction and intima-media thickness? The Hoorn Study

Clinical Science

Volumn 110, Issue 5, 2006, Pages 597-604

  Van Hecke, Manon V ^a,b   Dekker, Jacqueline M ^b   Nijpels, Giel ^a,b   Stolk, Ronald P ^c   Henry, Ronald M A ^d   Heine, Robert J ^a,b   Bouter, Lex M ^b   Stehouwer, Coen D A ^b,e   Polak, Bettine C P ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d Infection and Immunology   (Netherlands)

^e MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cardiovascular event; Endothelial dysfunction; Flow mediated vasodilatation; Intima media thickness; Microvascular disorder, retina

Indexed keywords

ADULT; AGED; ARTERY ENDOTHELIUM; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL DIAMETER; BRACHIAL ARTERY; CARDIOVASCULAR RISK; CAROTID ARTERY; COMPUTER AIDED DESIGN; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF CARBOHYDRATE METABOLISM; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; EYE PHOTOGRAPHY; FEMALE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HUMAN; INTIMA; MAJOR CLINICAL STUDY; MALE; MICROANGIOPATHY; NON INSULIN DEPENDENT DIABETES MELLITUS; OPHTHALMOLOGY; OPHTHALMOSCOPY; PRIORITY JOURNAL; RETINA ARTERY; RETINA BLOOD VESSEL; RETINA INJURY; RETINA VEIN; RETINOPATHY; VASCULAR DISEASE; VASODILATATION; VEIN DILATATION;

AGED; AGED, 80 AND OVER; ANTHROPOMETRY; ARTERIOLES; BLOOD GLUCOSE; CAROTID ARTERY, COMMON; CROSS-SECTIONAL STUDIES; DIABETIC RETINOPATHY; ENDOTHELIUM, VASCULAR; HUMANS; MICROCIRCULATION; MIDDLE AGED; RETINAL ARTERY; RETINAL DISEASES; TUNICA INTIMA; TUNICA MEDIA; VASODILATION; VENULES;

EID: 33646715586     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20050270     Document Type: Article

References (52)

1. Wong, T. Y., Rosamond, W., Chang, P. P. et al. (2005) Retinopathy and risk of congestive heart failure. JAMA, J. Am. Med. Assoc. 293, 63-69
2. Klein, B. E., Klein, R., McBride, P. E. et al. (2004) Cardiovascular disease, mortality, and retinal microvascular characteristics in type 1 diabetes: Wisconsin Epidemiologic Study of Diabetic Retinopathy. Arch. Intern. Med. 164, 1917-1924
3. Jager, A., Kostense, P. J., Ruhe, H. G. 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
4. Cannon, III, R. O., Leon, M. B., Watson, R. M., Rosing, D. R. and Epstein, S. E. (1985) Chest pain and 'normal' coronary arteries-role of small coronary arteries. Am. J. Cardiol. 55, 50B-60B
5. Brush, Jr, J. E., Cannon, III, R. O., Schenke, W. H. et al. (1988) Angina due to coronary microvascular disease in hypertensive patients without left ventricular hypertrophy. N. Engl. J. Med. 319, 1302-1307
6. Egashira, K., Inou, T., Hirooka, Y., Yamada, A., Urabe, Y. and Takeshita, A. (1993) Evidence of impaired endothelium-dependent coronary vasodilatation in patients with angina pectoris and normal coronary angiograms. N. Engl. J. Med. 328, 1659-1664
7. Buchthal, S. D., den Hollander, J. A., Merz, C. N. et al. (2000) Abnormal myocardial phosphorus-31 nuclear magnetic resonance spectroscopy in women with chest pain but normal coronary angiograms. N. Engl. J. Med. 342, 829-835
8. Liu, P. P., Mak, S. and Stewart, D. J. (1999) Potential role of the microvasculature in progression of heart failure. Am. J. Cardiol. 84, 23L-26L
9. Wu, K. C., Zerhouni, E. A., Judd, R. M. et al. (1998) Prognostic significance of microvascular obstruction by magnetic resonance imaging in patients with acute myocardial infarction. Circulation 97, 765-772
10. Ijzerman, R. G., de Jongh, R. T., Beijk, M. A. et al. (2003) Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur. J. Clin. Invest. 33, 536-542
11. Wong, T. Y., Klein, R., Klein, B. E. K., Tielsch, J. M., Hubbard, L. and Nieto, F. J. (2001) Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv. Ophthalmol. 46, 59-80
12. Hubbard, L. D., Brothers, R. J., King, W. N. et al. (1999) Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the Atherosclerosis Risk in Communities Study. Ophthalmology 106, 2269-2280
13. Wong, T. Y., Klein, R., Sharrett, A. R. et al. (2004) Retinal arteriolar diameter and risk for hypertension. Ann. Intern. Med. 140, 248-255
14. Wong, T. Y., Shankar, A., Klein, R., Klein, B. E. and Hubbard, L. D. (2004) Prospective cohort study of retinal vessel diameters and risk of hypertension. Br. Med. J. 329, 79
15. Sharrett, A. R., Hubbard, L. D., Cooper, L. S. et al. (1999) Retinal arteriolar diameters and elevated blood pressure: the Atherosclerosis Risk in Communities Study. Am. J. Epidemiol. 150, 263-270
16. Chaturvedi, N., Sjoelie, A. K., Porta, M. et al. (2001) Markers of insulin resistance are strong risk factors for retinopathy incidence in type 1 diabetes. Diabetes Care 24, 284-289
17. van Leiden, H. A., Dekker, J. M., Moll, A. C. et al. (2003) Risk factors for incident retinopathy in a diabetic and nondiabetic population: The Hoorn Study. Arch. Ophthalmol 121, 245-251
18. Wong, T. Y., Klein, R., Sharrett, A. R. et al. (2002) Retinal arteriolar narrowing and risk of diabetes mellitus in middle-aged persons. JAMA, J. Am. Med. Assoc. 287, 2528-2533
19. Wong, T. Y., Duncan, B. B., Golden, S. H. et al. (2004) Associations between the metabolic syndrome and retinal microvascular signs: the Atherosclerosis Risk In Communities study. Invest. Ophthalmol. Visual Sci. 45, 2949-2954
20. Wong, T. Y., Klein, R., Couper, D. J. et al. (2001) Retinal microvascular abnormalities and incident stroke: the Atherosclerosis Risk in Communities Study. Lancet 358, 1134-1140
21. Wong, T. Y., Klein, R., Sharrett, A. R. et al. (2002) Retinal arteriolar narrowing and risk of coronary heart disease in men and women: The Atherosclerosis Risk In Communities Study. JAMA, J. Am. Med. Assoc. 287, 1153-1159
22. van Hecke, M. V., Dekker, J. M., Nijpels, G. et al. (2003) Retinopathy is associated with cardiovascular and all-cause mortality in both diabetic and nondiabetic subjects: The Hoorn Study. Diabetes Care 26, 2958
23. Klein, R., Sharrett, A. R., Klein, B. E. et al. (2000) Are retinal arteriolar abnormalities related to atherosclerosis? The Atherosclerosis Risk in Communities Study. Arterioscler., Thromb., Vasc. Biol. 20, 1644-1650
24. Wong, T. Y., Klein, R., Sharrett, A. R. et al. (2003) The prevalence and risk factors of retinal microvascular abnormalities in older persons: the Cardiovascular Health Study. Ophthalmology 110, 658-666
25. Klein, R., Sharrett, A. R., Klein, B. E. K. et al. (2002) The association of atherosclerosis, vascular risk factors, and retinopathy in adult's with diabetes: the atherosclerosis risk in communities study. Ophthalmology 109, 1225-1234
26. Klein, R., Marino, E. K., Kuller, L. H. et al. (2002) The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study. Br. J. Ophthalmol. 86, 84-90
27. Stehouwer, C. D., Henry, R. M., Dekker, J. M., Nijpels, G., Heine, R. J. and Bouter, L. M. (2004) Microalbuminuria is associated with impaired brachial artery, flow-mediated vasodilation in elderly individuals without and with diabetes: further evidence for a link between microalbuminuria and endothelial dysfunction: the Hoorn Study. Kidney Int. Suppl. S42-S44
28. Ross, R. (1999) Atherosclerosis: an inflammatory disease. N. Engl. J. Med. 340, 115-126
29. Bonetti, P. O., Lerman, L. O. and Lerman, A. (2003) Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler., Thromb., Vasc. Biol. 23, 168-175
30. Mooy, J. M., Grootenhuis, P. A., de Vries, H. et al. (1995) Prevalence and determinants of glucose intolerance in a Dutch Caucasian population. The Hoorn Study. Diabetes Care 18, 1270-1273
31. Henry, R. M., Ferreira, I., Kostense, P. J. et al. (2004) Type II diabetes is associated with impaired endothelium-dependent, flow-mediated dilation, but impaired glucose metabolism is not: The Hoorn Study. Atherosclerosis 174, 49-56
32. World Health Organization (1999) Definition, diagnosis and classification of diabetes mellitus and its complications. Report of a WHO consultation, Geneva, Switzerland
33. Parr, J. C. and Spears, G. F. (1974) Mathematic relationships between the width of a retinal artery and the widths of its branches. Am. J. Ophthalmol. 77, 478-483
34. Parr, J. C. and Spears, G. F. (1974) General caliber of the retinal arteries expressed as the equivalent width of the central retinal artery. Am. J. Ophthalmol. 77, 472-477
35. Knudtson, M. D., Lee, K. E., Hubbard, L. D., Wong, T. Y., Klein, R. and Klein, B. E. (2003) Revised formulas for summarizing retinal vessel diameters. Curr. Eye Res. 27, 143-149
36. Aldington, S. J., Kohner, E. M., Meuer, S., Klein, R. and Sjolie, A. K. (1995) Methodology for Retinal Photography and Assessment of Diabetic-Retinopathy: the Eurodiab IDDM Complications Study. Diabetologia 38, 437-444
37. Corretti, M. C., Anderson, T. J., Benjamin, E. J. et al. (2002) Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J. Am. Coll. Cardiol. 39, 257-265
38. Lambert, J., Aarsen, M., Donker, A. J. and Stehouwer, C. D. (1996) Endothelium-dependent and -independent vasodilation of large arteries in normoalbuminuric insulin-dependent diabetes mellitus. Arterioscler., Thromb., Vasc. Biol. 16, 705-711
39. Henry, R. M., Kostense, P. J., Spijkerman, A. M. et al. (2003) Arterial stiffness increases with deteriorating glucose tolerance status: the Hoorn Study. Circulation 107, 2089-2095
40. Chobanian, A. V., Bakris, G. L., Black, H. R. et al. (2003) The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA, J. Am. Med. Assoc. 289, 2560-2572
41. Beks, P. J., Mackaay, A. J., de Neeling, J. N., de Vries, H., Bouter, L. M. and Heine, R. J. (1995) Peripheral arterial disease in relation to glycaemic level in an elderly Caucasian population: the Hoorn Study. Diabetologia 38, 86-96
42. Jager, A., Kostense, P. J., Nijpels, G., Heine, R. J., Bouter, L. M. and Stehouwer, C. D. (1998) Microalbuminuria is strongly associated with NIDDM and hypertension, but not with the insulin resistance syndrome: the Hoorn Study. Diabetologia 41, 694-700
43. Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F. and Turner, R. C. (1985) Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419
44. van Hecke, M. V., Dekker, J. M., Nijpels, G. et al. (2005) Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn Study. Diabetologia 48, 1300-1306
45. Matsumoto, K., Sera, Y., Ueki, Y., Inukai, G., Niiro, E. and Miyake, S. (2002) Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabetic Med. 19, 822-826
46. van Hecke, M. V., Dekker, J. M., Stehouwer, C. D. et al. (2005) Diabetic retinopathy is associated with mortality and cardiovascular disease incidence: the EURODIAB prospective complications study. Diabetes Care 28, 1383-1389
47. Ruige, J. B., Assendelft, W. J., Dekker, J. M., Kostense, P. J., Heine, R. J. and Bouter, L. M. (1998) Insulin and risk of cardiovascular disease: a meta-analysis. Circulation 97, 996-1001
48. Muis, M. J., Bots, M. L., Bilo, H. J. et al. (2005) High cumulative insulin exposure: a risk factor of atherosclerosis in type 1 diabetes? Atherosclerosis 181, 185-192
49. Steinberg, H. O., Brechtel, G., Johnson, A., Fineberg, N. and Baron, A. D. (1994) Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J. Clin. Invest. 94, 1172-1179
50. Ikram, M. K., de Jong, F. J., Vingerling, J. R. et al. (2004) Are retinal arteriolar or venular diameters associated with markers for cardiovascular disorders? The Rotterdam Study. Invest. Ophthalmol. Visual Sci. 45, 2129-2134
51. Bhagat, K., Hingorani, A. and Vallance, P. (1997) Flow associated or flow mediated dilatation? More than just semantics. Heart 78, 7-8
52. Gokce, N., Keaney, Jr, J. F., Hunter, L. M., Watkins, M. T., Menzoian, J. O. and Vita, J. A. (2002) Risk stratification for postoperative cardiovascular events via noninvasive assessment of endothelial function: a prospective study. Circulation 105, 1567-1572