Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Sign In to gain access to subscriptions and/or personal tools.
The British Journal of Diabetes & Vascular Disease
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Browne, D.
Right arrow Articles by Cummings, M.
Right arrow Search for Related Content
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

Reviews

Review: Endothelial dysfunction and pre-symptomatic atherosclerosis in type 1 diabetes — pathogenesis and identification

Duncan Browne

Department of Diabetes and Endocrinology, Queen Alexandra Hospital, Cosham, Portsmouth, PO6 3LY, UK, dbrowne{at}doctors.org.uk

Darryl Meeking

Kenneth Shaw

Michael Cummings

The vascular endothelium offers an attractive model for detecting functional abnormalities prior to structural changes in the vasculature. Demonstration of progression from endothelial dysfunction through to atherosclerosis is required. Measurements of forearm bloodflow, biochemical markers and biophysical assessments of the endothelium have been employed as research tools for investigating pre-symptomatic atherosclerosis.

However, studies examining endothelial function in type 1 diabetes have been sparse and conflicting. Differences in methodology and the study populations were potential confounding factors. Augmented vasodilatory prostanoids compensate for reduced nitric oxide bioavailability in determining endothelial function in type 1 diabetes. Hyperglycaemia appears to be the initiating event in type 1 diabetes which promotes a variety of biochemical events which are pathogenic to the endothelium.

Improved understanding of the endothelium may facilitate the development of novel diagnostic tools and interventions targeting the accelerated atherosclerosis associated with type 1 diabetes.

Key Words: type 1 diabetes • atherosclerosis • forearm • vascular endothelium • nitric oxide.

References

  • Krolewski AS, Kosinski EJ, Warram JH et al. Magnitude and determinants of coronary artery disease in juvenile-onset, insulin-dependent diabetes mellitus. Am J Cardiol 1987;59:750-5.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Kannel WB, Kannel C., Paffenberger RS Jr et al. Heart rate and cardiovascular mortality: the Framingham Study. Am Heart J 1987;13:1489-99.
  • Moorish NJ, Stevens LK, Fuller JH et al. Risk factors for macrovascular disease in diabetes mellitus: the London follow-up to the WHO Multinational Study of Vascular Disease in Diabetics. Diabetologia 1991;34:590-4.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Peppa-Patrikou M., Scordili M., Antoniou A. et al. Carotid atherosclerosis in adolescents with IDDM. Relation to urinary endothelin, albumin, free cortisol, and other factors. Diabetes Care 1998;21:1004-07.[Abstract]
  • Hadock S., Richardson M., Winocour PH et al. Intimal alterations in rabbit aortas during the first 6 months of alloxan-induced diabetes. Arterioscler Thromb Vasc Biol 1991;11:517-29.[Abstract/Free Full Text]
  • Ross R. The pathogenesis of atherosclerosis; a perspective for the 1990's. Nature 1993;362:801-09.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Calermajer DS, Sorensen KE, Gooch VM et al. Non-invasive detection of endothelial function in children and adults at risk of atherosclerosis. Lancet 1992;340:1111-15.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Behrendt D., Ganz P. Endothelial function. From vascular biology to clinical applications. Am J Cardiol 2002;90(10C):L40-8.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Storey AM, Perry CJ, Petrie JR Endothelial dysfunction in type 2 diabetes. Br J Diabetes Vasc Dis 2001;1:22-7.[Abstract/Free Full Text]
  • Moncada S., Radomski MW, Palmer RMJ. Endothelium-derived relaxing factor: identification as nitric oxide and role in the control of vascular tone and platelet function. Biochem Pharmacol 1988;37:2495-501.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Crea F., Biasucci LM, Buffon A. et al. Role of inflammation in the pathogenesis of unstable coronary artery disease. Am J Cardiol 1997;80:10-16E.
  • Loscalzo J. Nitric oxide insufficiency, platelet activation, and arterial thrombosis. Circ Res 2001;88:756-62.[Abstract/Free Full Text]
  • Diodati JG, Dakak N., Gilligan DM et al. Effect of atherosclerosis on endothelium-dependent inhibition of platelet activation in humans. Circulation 1998;98:17-24.[Abstract/Free Full Text]
  • Stehouwer CD, Lambert J., Donker AJ et al. Endothelial dysfunction and pathogenesis of diabetic angiopathy. Cardiovasc Res 1997;34:55-68.[Abstract/Free Full Text]
  • Pieper GM Enhanced, unaltered and impaired nitric oxide mediated endothelium dependent relaxation in experimental diabetes mellitus: importance of disease duration. Diabetologia 1999;42:204-13.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Benjamin N., Calver A., Collier J. et al. Measuring forearm bloodflow and interpreting the responses to drugs and mediators. Hypertension 1995; 25:918-23.[Abstract/Free Full Text]
  • Ludmer PL, Selwyn AP, Shook TI et al. Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. N Engl J Med 1986;315:1046-51.[Abstract]
  • Takase B., Akima T., Uehata A. et al. Close relation between endothelium-dependent flow mediated vasodilation in coronary and brachial artery in human. J Am Coll Cardiol 1998;31:359A.
  • Clarkson P., Celermajer DS, Donald AE et al. Impaired vascular reactivity in insulin-dependent diabetes mellitus is related to disease duration and low density lipoprotein cholesterol levels. J Am Coll Cardiol 1996;28:573-9.[Abstract]
  • Schroeder S., Enderle MD, Ossen R. et al. Noninvasive determination of endothelium-mediated vasodilation as a screening test for coronary artery disease: Pilot study to assess the predictive value in comparison with angina pectoris, exercise electrocardiography, and myocardial perfusion imaging. Am Heart J 1999;138:731-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Drexler H., Zeiher AM Progression of coronary endothelial dysfunction in men and its potential clinical significance. Basic Res Cardiol 1991;86: 223-32.
  • Chowienczyk PJ, Cockcroft JR, Ritter JM Differential inhibition by NGmonomethyl-L-arginine of vasodilator effects of acetylcholine and methacholine in human forearm vasculature. Br J Pharmacol 1993;110: 736-8.[Web of Science][Medline] [Order article via Infotrieve]
  • Chowienczyk PJ, Cockcroft JR, Ritter JM Blood flow responses to intraarterial acetylcholine in man: effects of basal flow and conduit vessel length. Clin Sci 1994;87:45-51.[Web of Science][Medline] [Order article via Infotrieve]
  • Rossi M., Lall K., Standfield N., Dornhurst A. Impaired vasoconstriction of peripheral cutaneous blood flow in type 1 diabetic patients following food ingestion. Diabetic Med 1998;15:463-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Pitkanen OP, Nuutila P., Raitakari OT et al. Coronary Flow reserve is reduced in young men with IDDM. Diabetes 1998;47:248-54.[Abstract]
  • Lehmann ED, Hopkins KD, Rawesh A. et al. Relation between number of cardiovascular risk factors/events and noninvasive Doppler ultrasound assessments of aortic compliance. Hypertension 1998;32:565-9.[Abstract/Free Full Text]
  • Nicolaides E., Jones CJH. Type 2 diabetes - implications for macrovascular mechanics and disease. Br J Diabetes Vasc Dis 2002;2:9-12.[Abstract/Free Full Text]
  • Brooks B., Molyneaux L., Yue DK Augmentation of central arterial pressure in type 1 diabetes. Diabetes Care 1999;22:1722-7.[Abstract/Free Full Text]
  • Westerbacka J., Uosukainen A., Makimattila S. et al. Insulin-induced decrease in large artery stiffness is impaired in uncomplicated type 1 diabetes mellitus. Hypertension 2000;35:1043-8.[Abstract/Free Full Text]
  • van Veen S., Chang PC Prostaglandin and nitric oxide mediate insulin-induced vasodilation in the human forearm. Cardiovasc Res 1997;34: 223-9.[Abstract/Free Full Text]
  • Bots ML, Hoes AW, Hoffman A. et al. Cross-sectionally assessed carotid intima-media thickness relates to long-term risk of stroke, coronary heart disease and death as estimated by available risk functions. J Intern Med 1999;245:269-76.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • McVeigh GF, Hamilton PK, Morgan DR Evaluation of mechanical arterial properties: clinical, experimental and therapeutic aspects. Clin Sci 2002;102:51-67.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Zureik M., Ducimetiere P., Touboul PJ et al. Common carotid intima-media thickness predicts occurrence of carotid atherosclerotic plaques: longitudinal results from the Aging Vascular Study (EVA) study. Arterioscler Thromb Vasc Biol 2000;20:1622-9.[Abstract/Free Full Text]
  • Balbarini A., Buttitta F., Limbruno U. et al. Usefulness of carotid intima-media thickness measurement and peripheral B-mode ultrasound scan in the clinical screening of patients with coronary artery disease. Angiology 2000;51:269-70.[Web of Science][Medline] [Order article via Infotrieve]
  • Effect of intensive diabetes treatment on carotid artery wall thickness in the epidemiology of diabetes interventions and complications. Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group. Diabetes 1999;48:383-90.[Abstract]
  • Huvers FC, De Leeuw PW, Alfons JHM et al. Endothelium-dependent vasodilation, plasma markers of endothelial function, and adrenergic vasoconstrictor responses in type 1 diabetes under near-normoglycaemic conditions. Diabetes 1999;47:1300-07.
  • Elhadd TA, Kennedy G., Hill A. et al. Abnormal markers of endothelial cell activation and oxidative stress in children, adolescents and young adults with type 1 diabetes with no clinical evidence of vascular disease. Diabetes Metab Res Rev 1999;15:405-11.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Hofmann MA, Kohl B., Zumbach MS et al. Hyperhomocysteinaemia and endothelial dysfunction in IDDM. Diabetes Care 1998;21:841-8.[Abstract]
  • Usui M., Matsuoka H., Miyazaki H., Ueda S., Okuda S., Imaizumi T. Endothelial dysfunction by acute hyperhomocysteinaemia: restoration by folic acid. Clin Sci 1999;96:235-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Poston L., Taylor PD Endothelium-mediated vascular function in insulin-dependent diabetes mellitus. Clin Sci 1995;88:245-55.[Web of Science][Medline] [Order article via Infotrieve]
  • Chan NN, Vallance P., Colhoun HM Nitric oxide and vascular responses in type 1 diabetes. Diabetologia 2000;43:137-47.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Johnstone MT, Creager SJ, Scales KM et al. Impaired endothelium-dependent vasodilatation in patients with insulin-dependent diabetes mellitus. Circulation 1993;88:2510-16.[Abstract/Free Full Text]
  • Williams SB, Goldfine AB, Timimi FK et al. Acute hyperglycaemia attenuates endothelium-dependent vasodilation in humans in vivo. Circulation 1998;97:1695-701.[Abstract/Free Full Text]
  • Akbari CM, Saouaf R., Barnhill DF et al. Endothelium-dependent vasodilation is impaired in both microcirculation and macrocirculation during acute hyperglycaemia. J Vasc Surg 1998;28:687-94.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Macklin AV, Viberti GC, Ritter J. Forearm blood flow in type 1 diabetics during systemic hyperglycemia. Diabetologia 1998;41:A310.
  • Avogadro A., Calo L., Piarulli F. et al. Effect of acute ketosis on the endothelial function of type 1 diabetic patients: The role of nitric oxide. Diabetes 1999;48:391-7.[Abstract]
  • Wang W., Diamond SL Does elevated nitric oxide production enhance the release of prostacyclin from shear stressed aortic endothelial cells. Biochem Biophys Res Commun 1997;233:748-51.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Cardillo C., Nambi SS, Kilcoyne CM et al. Insulin stimulates both endothelin and nitric oxide activity in the human forearm. Circulation 1999; 100:820-5.[Abstract/Free Full Text]
  • Dogra G., Rich L., Stanton K. et al. Endothelium-dependent and independent vasodilation studies at normoglycaemia in type 1 diabetes with and without microalbuminuria. Diabetologia 2001;44:593-601.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Stuhlinger MC, Tsao PS, Her JH et al. Homocysteine impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine. Circulation 2001;104:2569-75.[Abstract/Free Full Text]
  • O'Byrne SO, Forte P., Roberts J. et al. Nitric oxide synthesis and isoprostane production in subjects with type 1 diabetes and normal urinary albumin excretion. Diabetes 2000;49:857-62.[Abstract]
  • Meeking DR, Browne DL, Allard S. et al. Effects of cyclo-oxygenase inhibition on vasodilatory response to acetylcholine in patients with type 1 diabetes and nondiabetic subjects. Diabetes Care 2000;23:1840-3.[Abstract/Free Full Text]
  • Browne DL, Allard SE, Munday LJ et al. The relative contributions and synergy between vasodilatory prostanoids and nitric oxide in determining endothelial function in type 1 diabetes. Diabetes 2001;50(suppl 2):A599.
  • Tesfamariam B., Jakubowski JA, Cohen RA Contraction of diabetic rabbit aorta caused by endothelium-derived PGH2-TxA2. Am J Physiol 1989;257:H1327-33.[Web of Science][Medline] [Order article via Infotrieve]
  • Tesfamariam B., Brown ML, Deykin D., Cohen RA Elevated glucose promotes generation of endothelium-derived vasoconstrictor prostanoids in rabbit aorta. J Clin Invest 1990;85:929-32.[Web of Science][Medline] [Order article via Infotrieve]
  • Katusic ZS, Schugel J., Consentino F. et al. Endothelium dependent contractions to oxygen-derived free radicals in the canine basilar artery. Am J Physiol 1993;264:H859-64.[Web of Science][Medline] [Order article via Infotrieve]
  • Thorne S., Mullen MJ, Clarkson P. et al. Early endothelial dysfunction in adults at risk from atherosclerosis: different responses to L-arginine. J Am Coll Cardiol 1998;32:110-16.[Abstract/Free Full Text]
  • Schade DS, Eaton RP, Freidman N. et al. The intravenous, intraperitoneal and subcutaneous routes of insulin delivery in diabetic man. Diabetes 1979;28:1069-72.[Medline] [Order article via Infotrieve]
  • Wolf BA, Williamson JR, Eason RA et al. Diacylglycerol accumulation and microvascular abnormalities induced by elevated glucose levels. J Clin Invest 1991;87:31-8.[Web of Science][Medline] [Order article via Infotrieve]
  • Hawthorne GC, Bartlett K., Hetherington CS et al. The effect of high glucose on polyol pathway activity and myoinositol metabolism in cultured human endothelial cells. Diabetologia 1989;32:196-9.
  • Tesfamariam B., Palacino JJ, Weisbrod RM et al. Aldose reductase inhibition restores endothelial cell function in diabetic rabbit aorta. J Cardiovasc Pharmacol 1993;21:205-11.[Web of Science][Medline] [Order article via Infotrieve]
  • Bucula R., Tracey KJ, Cerami A. Advanced glycosylation products quench nitric oxide and mediate defective endothelium-dependent vasodilation in experimental diabetes. J Clin Invest 1991;87:432-8.[Web of Science][Medline] [Order article via Infotrieve]
  • Watts GF, Playford DA Dyslipoproteinaemia and hyperoxidative stress in the pathogenesis of endothelial dysfunction in non-insulin dependent diabetes mellitus: an hypothesis. Atherosclerosis 1998;141:17-30.[Web of Science][Medline] [Order article via Infotrieve]
  • Kugiyama K., Kerns SA, Morriset JD et al. Impairment of endothelium-dependent relaxation by lysolecithin in modified low density lipoprotein Nature 1990;344:160-2.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Laakso M., Edelmann SV, Bretchel G. et al. Impaired insulin-mediated skeletal muscle blood flow in patients with NIDDM. Diabetes 1992;41: 1076-83.[Abstract]
  • Skyrme-Jones RAP, Berry KL, O'Brien RC et al. Basal and exercise-induced skeletal muscle blood flow is augmented in type 1 diabetes mellitus. Clin Sci 2000;98:111-20.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Tooke JE Microvascular haemodynamics in diabetes mellitus. Clin Sci 1986;70:119-25.[Web of Science][Medline] [Order article via Infotrieve]
  • Parving HH, Viberti GC, Keen H. et al. Haemodynamic factors in the genesis of diabetic microangiopathy. Metabolism 1983;32:943-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Christensen NJ A reversible vascular abnormality associated with diabetic ketosis. Clin Sci 1970;39:539-48.[Web of Science][Medline] [Order article via Infotrieve]
  • Taddei S., Galetta F., Virdis A. et al. Physical activity prevents age related impairment in nitric oxide availability in elderly athletes. Circulation 2000; 101:2896-901.[Abstract/Free Full Text]
  • Pieper GM Enhanced, unaltered and impaired nitric oxide mediated endothelium dependent relaxation in experimental diabetes mellitus: importance of disease duration. Diabetologia 1999;42:204-13.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]

The British Journal of Diabetes & Vascular Disease, Vol. 3, No. 1, 27-34 (2003)
DOI: 10.1177/14746514030030010401
Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
 Therapeutic Advances in UrologyHome page
A. Aversa, R. Bruzziches, D. Francomano, M. Natali, and A. Lenzi
Testosterone and phosphodiesterase type-5 inhibitors: new strategy for preventing endothelial damage in internal and sexual medicine?
Therapeutic Advances in Urology, October 1, 2009; 1(4): 179 - 197.
[Abstract] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Browne, D.
Right arrow Articles by Cummings, M.
Right arrow Search for Related Content
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?