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 Kluft, C.
Right arrow Articles by Jespersen, J.
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: Diabetes as a procoagulant condition

Cornelis Kluft

Gaubius Laboratory, TNO-PG, Leiden, The Netherlands, Thrombosis Institute, University of Southern Denmark, Esbjerg, Denmark, c.kluft{at}pg.tno.nl

Jorgen Jespersen

Thrombosis Institute, University of Southern Denmark, Esbjerg, Denmark

Major known effects of the metabolic derangements of diabetes in haemostasis are induction of platelet-vascular activation by hyperglycaemia, the increase in fibrinogen, modification of fibrin substrate by glucose and hypofibrinolysis related to insulin resistance. The platelet effects are specifically expressed during high shear stress and may be relevant in particular for developing of micro-angiopathy. Hypofibrinolysis, increased fibrinogen and modifications of fibrin may aggravate microthrombosis and organ damage and contribute to precipitation of coronary and cerebral infarction. In addition to specific anti-diabetic medication to reduce the haemostatic effects, specific antiplatelet and profibrinolytic treatments may be relevant for reducing further the morbidity and mortality in diabetics for both micro- and macro-angiopathy.

Key Words: diabetes • platelet • fibrinogen • hypofibrinolysis.

References

  • Bierman EL Atherogenesis in diabetes. Arterioscl Thromb 1992;12:647-55.[Free Full Text]
  • Colwell JA Treatment for the procoagulant state in type 2 diabetes. Endocrinol Metab Clin North Am 2001;30:1011-30.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Cominacini L., Fratta PA, Garbin U. et al. Elevated levels of soluble E-selectin in patients with IDDM and NIDDM; relation to metabolic control. Diabetologia 1995;38:1122-4.[Web of Science][Medline] [Order article via Infotrieve]
  • Nomura S., Shouzu A., Omoto S., Nishikawa M., Fukuhara S. Significance of chemokines and activated platelets in patients with diabetes. Clin Exp Immunol 2000;121:437-43.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Shouzu A., Nomura S., Hayakawa T. et al. Effect of sarpogrelate hydrochloride on platelet-derived microparticles and various soluble adhesion molecules in diabetes mellitus. Clin Appl Thromb Hemost 2000;6:139-43.[Abstract/Free Full Text]
  • Omoto S., Nomura S., Shouzu A. et al. Significance of platelet-derived microparticles and activated platelets in diabetic nephropathy. Nephron 1999;81:271-7.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Nomura S., Shouzu A., Omoto S. et al. Effect of cilostazol on soluble adhesion molecules and platelet-derived microparticles in patients with diabetes. Thromb Haemost 1998;80:388-92.[Web of Science][Medline] [Order article via Infotrieve]
  • Elhadd TA, Kennedy G., Hill A. et al. Abnormal markers of endothelial cell activation and oxidative stress in children, adolescent and young adults with type 1 diabetes with no clinical vascular disease. Diabetes Metab Res Rev 1999;15:405-11.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Nappo F., Esposito K., Cioffi M. et al. Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. J A Coll Cardiol 2002;39:1145-50.[CrossRef]
  • van der Planken MG, Vertessen FJ, Vertommen J., Engelen W., Berneman ZN, De Leeuw I. Platelet prothrombinase activity, a final pathway platelet procoagulant activity, is overexpressed in type 1 diabetes: no relationship with mean platelet volume or background retinopathy. Clin Appl Thromb Hemost 2000;6:65-8.[Abstract/Free Full Text]
  • Tooke JE, Shore AC, Cohen RA, Kluft C. Diabetic angiopathy: tracking down the culprits. J Diabetes Complications 1996;10:173-81.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Marfella R., Esposito K., Giunta R. et al. Circulating adhesion molecules in humans: role of hyperglycemia and hyperinsulinemia. Circulation 2000; 101:2247-51.[Abstract/Free Full Text]
  • Ajzenberg N., Denis CV, Veyradier A., Girma JP, Meyer D., Baruch D. Complete defect in vWF-cleaving protease activity associated with increased shear-induced platelet aggregation in thrombotic microangiopathy. Thromb Haemos 2002;87:808-11.[Web of Science][Medline] [Order article via Infotrieve]
  • Kharbanda RK, Walton B., Allen M. et al. Prevention of inflammation-induced endothelial dysfunction. A novel vascula-protective action of asprin. Circulation 2002;105:2600-04.[Abstract/Free Full Text]
  • Otsuki M., Saito H., Sumitani S., Kouhara H., Kurabayashi M., Kasayama S. Cilostazol represses vascular cell adhesion molecule-1 gene transcription via inhibiting NF-kappaB binding to its recognition sequence. Atherosclerosis 2001;158:121-8.[CrossRef][Medline] [Order article via Infotrieve]
  • Martin S., van den Engel NK, Vinke A., Heidenthal E., Schulte B., Kolb H. Dominant role of intercellular adhesion molecule-1 in the pathogenesis of autoimmune diabetes in non-obese diabetic mice. J Autoimmune 2001;17:109-17.[CrossRef]
  • Nishimura M., Obayashi H., Maruya E. et al. Association between type 1 diabetes age-at-onset and intercellular adhesion moleculae-1 (ICAM-1) gene polymorphism. Hum Immunol 2000;61:507-10.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Konieczkowski M., Skrinska VA Increased synthesis of thromboxane A (2) and expression of procoagulant activity by monocytes in response to arachidonic acid in diabetes mellitus. Prostaglandins Leukot Essent Fatty Acids 2001;65:133-8.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Kaplar M., Kappelmayer J., Veszpremi A., Szabo K., Udvardy M. The possible association of in vivo leukocyte-platelet heterophilic aggregate formation and the development of diabetic angiopathy. Platelets 2001;12:419-22.[CrossRef][Medline] [Order article via Infotrieve]
  • Desfaits AC, Serri O., Renier G. Normalization of plasma lipid peroxides, monocyte adhesion, and tumor necrosis factor-alpha production in NIDDM patients after gliclazide treatment. Diabetes Care 1998;21:487-93.[Abstract]
  • Cominacini L., Garbin U., Pasini AF et al. The expression of adhesion molecules on endothelial cells is inhibited by troglitazone through its antioxidant activity. Cell Adhes Commun 1999;7:223-31.[Web of Science][Medline] [Order article via Infotrieve]
  • The DAMAD Study Group. Effect of aspirin alone and aspirin plus dipyridamole in early diabetic retinopathy. A multicenter randomized controlled clinical trial. Diabetes 1989;38:491-8.[Abstract]
  • Hopper AH, Tindall H., Davies JA Administration of aspirin-dipyridamole reduces proteinuria in diabetic nephropathy. Nephrol Dial Transplant 1989;4:140-3.[Abstract/Free Full Text]
  • Rubtsova AL, Ametov AS, Strakhov VV The use of ticlid in diabetic retinopathy. Ter Arkh 1997;69:19-21.[Web of Science][Medline] [Order article via Infotrieve]
  • Esmatjes E., Maseras M., Gallego M., Coves MJ, Conget I. Effect of treatment with an inhibitor of platelet aggregation on the evaluation of background retinopathy: 2 years of follow up. Diabetes Res Clin Pract 1989; 7:285-91.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Myrup B., Rossing P., Jensen T., Gram J., Kluft C., Jespersen J. Fibrinolysis in insulin-dependent diabetic patients with and without nephropathy. Fibrinolysis Proteolysis 1996;10:331-5.
  • Bruttomesso D., Iori E., Kiwanuka E. et al. Insulin infusion normalizes fasting and post-prandial albumin and fibrinogen synthesis in type 1 diabetes mellitus. Diabet Med 2001;18:915-20.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Ceriello A., Taboga C., Giacomello R. et al. Fibrinogen plasma levels as a marker of thrombin activation in diabetes. Diabetes 1994;43:430-2.[Abstract]
  • Avellone G., di Garbo V., Crdova R. et al. Effects of heparin treatment on hemostatic abnormalities in obese non-insulin-dependent diabetic patients. Metabolism 1997;46:930-4.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Myrup B., Jensen T., Gram J., Kluft C., Jespersen J., Deckert T. No effect of unfractionated or low molecular weight heparin treatment on markers of vascular wall and hemostatic function in incipient diabetic nephropathy. Diabetes Care 1997;20:1615-19.[Abstract]
  • D'Elia JA, Weinrauch LA, Gleason RE et al. Fibrinogen and factor VII levels improve with glycemic control in patients with type 1 diabetes mellitus who have microvascular complications. Arch Intern Med 2001;161: 98-101.[Abstract/Free Full Text]
  • Maat de MPM. Effects of diet, drugs, and genes on plasma fibrinogen levels. Ann NY Acad Sci 2001;936:509-21.[Web of Science][Medline] [Order article via Infotrieve]
  • Schut NH, van Arkel EC, Hardeman MR, Bilo HJ, Michels RP, Vreeken J. Blood and plasma viscosity in diabetes: possible contribution to late organ complications? Diabetes Res 1992;19:31-5.[Web of Science][Medline] [Order article via Infotrieve]
  • Sandhagen B., Ewald U., Tuvemo T. Haemorheology in insulin-dependent diabetes is still normal five years after onset of the disease. Acta Paediatr 1997;418(suppl):21-3.
  • Richter WO, Jahn P., Jung N., Nielebock E., Tachezy H. Fibrinogen adsorption in the diabetic foot syndrome and peripheral arterial occlusive disease: first clinical experience. Ther Apher 2001;5:335-9.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Koll RA, Klinkmann J., Richter WO RheoSorb: a specific adsorber for fibrinogen elimination in clinical situations with impaired rheology. Artif Organs 2002;26:145-51.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Boeri D., Maiello M., Lorenzi M. Increased prevalence of microthromboses in retinal capillaries of diabetic individuals. Diabetes 2001;50:1432-9.[Abstract/Free Full Text]
  • Bent-Hansen L. Whole body capillary exchange of albumin. Alterations in diabetic microangiopathy. Dan Med Bull 1997;44:40-55.[Web of Science][Medline] [Order article via Infotrieve]
  • Murakami T., Egawa H., Komiyama Y., Masuda M., Murata K. Increased accumulation of nonenzymatically glycated fibrinogen in the renal cortex in rats. Thromb Res 1990;58:23-33.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Jorneskog G., Egberg N., Fagrell B. et al. Altered properties of the fibrin gel structure in patients with IDDM. Diabetologica 1996;39:1519-23.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Nair CH, Azhar A., Wilson JD, Dhall DP Studies on fibrin network structure in human plasma. Part II. Clinical application: diabetes and antidiabetic drugs. Thromb Res 1991;64:477-85.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Brownlee M., Vlassara H., Cerami A. Nonenzymatic glycosilation reduces the susceptibility of fibrin to degradation by plasmin. Diabetes 1983;32: 680-4.[Abstract]
  • Mirshahi M., Soria J., Soria C., Bertrand O., Mirshahi M., Basdevant A. Glycosilation of human fibrinogen and fibrin in vitro. Its consequences on the properties of fibrin(ogen). Thromb Res 1987;48:279-89.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Dhall DP, Nair CH Effects of gliclazide on fibrin network. J Diabetes Complications 1994;8:231-4.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Williams S., Fatah K., Ivert T., Blomback M. The effect of acetylsalicylic acid on fibrin gel lysis by tissue plasminogen activator. Blood Coagul Fibrinolysis 1995;6:718-25.[Web of Science][Medline] [Order article via Infotrieve]
  • Standeven KF, Ariens RA, Whitaker P., Ashcroft AE, Weisel JW, Grant PJ The effect of dimethylbiguanide on thrombin activity, FXIII activation, fibrin polymerization, and fibrin clot formation. Diabetes 2002;51:189-97.[Abstract/Free Full Text]
  • Kohler HP, Grant PJ The role of factor XIIIVal34Leu in cardiovascular disease. QJM 1999;92:67-72.[Free Full Text]
  • Kohler HP, Grant PJ Plasminogen-activator inhibitor type 1 and coronary artery disease. N Engl J Med 2000;342:1792-801.[Free Full Text]
  • Mansfield MW, Stickland MH, Grant PJ Plasminogen activator inhibitor-1 (PAI-1) promoter polymorphism and coronary artery disease in non-insulin-dependent diabetes. Thromb Haemost 1995;74:1032-4.[Web of Science][Medline] [Order article via Infotrieve]
  • Kluft C. Constitutive synthesis of tissue-type plasminogen activator (t-PA) and plasminogen activator inhibitor type 1 (PAI-1): conditions and therapeutic targets. Fibrinolysis 1994;8(suppl 2):1-7.[Medline] [Order article via Infotrieve]
  • Juhan-Vague I., Roul C., Alessi MC, Ardissone JP, Heim M., Vague P. Increased plasminogen activator inhibitor activity in non insulin dependent diabetic patients - relationship with plasma insulin. Thromb Haemost 1989;61:370-3.[Web of Science][Medline] [Order article via Infotrieve]
  • Juhan-Vague I., Alessi MC, Vague P. Increased plasma plasminogen activator inhibitor 1 levels. A possible link between insulin resistance and atherothrombosis. Diabetologia 1991;34:457-62.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Riese H., Vrijkotte TGM, Meijer P., Kluft C., de Geus EJC. Covariance of metabolic and hemostatic risk indicators in men and women. Fibrinolysis & Proteolysis 2001;15:9-20.[CrossRef][Web of Science]
  • Pandolfi A., Cetrullo D., Polishuck R. et al. Plasminogen activator inhibitor type 1 is increased in the arterial wall of type II diabetic subjects. Arterioscler Thromb Vasc Biol 2001;21;1378-82.[Abstract/Free Full Text]
  • Aso Y., Matsumoto S., Fujiwara Y., Tayama K., Inukai T., Takemura Y. Impaired fibrinolytic compensation for hypercoagulability in obese patients with type 2 diabetes: association with increased plasminogen activator inhibitor-1. Metabolism 2002;51:471-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Zeitler P., Thiede A., Muller HL Prospective study on plasma clotting parameters in diabetic children - no evidence for specific changes in coagulation system. Exp Clin Endocrinol Diabetes 2001;109:146-50.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Asakawa H., Tokunaga K., Kawakami F. Elevation of fibrinogen and thrombin-antithrombin III complex levels of type 2 diabetes mellitus patients with retinopathy and nephropathy. J Diabetes Complications 2000;14:121-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Carr ME Diabetes mellitus: hypercoagulable state. J Diabetes Complications 2001;15:44-54.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Gabazza EC, Takeya H., Deguchi H. et al. Protein C activation in NIDDM patients. Diabetologia 1996;39:1455-61.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Kario K., Matsuo T., Kobayashi H., Matsuo M., Sakata T., Miyata T. Activation of tissue factor-induced coagulation and endothelial cell dysfunction in non-insulin-dependent diabetic patients with microalbuminuria. Arterioscler Thromb Vasc Biol 1995;15:1114-20.[Abstract/Free Full Text]
  • Ceriello A., Taboga C., Tonutti L. et al. Post-meal coagulation activation in diabetes mellitus: the effect of acarbose. Diabetologia 1996;39:469-73.[Web of Science][Medline] [Order article via Infotrieve]
  • Grant PJ The effects of high- and medium-dose metformin therapy on cardiovascular risk factors in patients with type II diabetes. Diabetes care 1996;19:648-54.[Web of Science][Medline] [Order article via Infotrieve]
  • Gregorio F., Ambrosi F., Manfrini S. et al. Poorly controlled elderly type 2 diabetic patients: the effects of increasing sulphonylurea dosages or adding metformin. Diabet Med 1999;16:1016-24.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Anfosso F., Chomiki N., Alessi MC, Vague P., Juhan-Vague I. Plasminogen activator inhibitor-1 synthesis in the human hepatoma cell line Hep G2. Metformin inhibits the stimulating effect of insulin. J Clin Invest 1993;91: 2185-93.[Web of Science][Medline] [Order article via Infotrieve]
  • Nagi DK, Yudkin JS Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects. A study of two ethnic groups. Diabetes Care 1993;16:621-9.[Abstract]
  • Diamant M., Brussaard HE, Princen HMG et al. Glycated LDL is associated with fibrinolysis in women with type 2 diabetes. Diabetes 1999; 48(S1):A1611.
  • Ren S., Lee H., Hu L., Lu L., Shen GX Impact of diabetes-associated lipoproteins on generation of fibrinolytic regulators from vascular endothelial cells. J Clin Endocrinol Metab 2002;87:286-91.[Abstract/Free Full Text]
  • Knobl P., Schernthaner G., Schnack C. et al. Haemostatic abnormalities persist despite glycemic improvement by insulin therapy in lean type 2 diabetic patients. Thromb Haemost 1994;71:692-7.[Web of Science][Medline] [Order article via Infotrieve]
  • Avellone G., di Garbo V., Cordova R. et al. Effects of heparin treatment on hemostatic abnormalities in obese non-insulin-dependent diabetic patients. Metabolism 1997;46:930-4.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
  • Nagi DK, Yudkin JS Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects. A study of two ethnic groups. Diabetes Care 1993;16:621-9.[Abstract]
  • Grant PJ, Stickland MH, Booth NA, Prentice CR Metformin causes a reduction in basal and post-venous occlusion plasminogen activator inhibitor-1 in type 2 diabetic patients. Diabet Med 1001;8:361-5.
  • Vague P., Juhan-Vague I., Alessi MC, Badier C., Valadier J. Metformin decreases the high plasminogen activator inhibition capacity, plasma insulin and triglyceride levels in non-diabetic obese subjects. Thromb Haemost 1987;57:326-8.[Web of Science][Medline] [Order article via Infotrieve]
  • Lee AJ, MacGregor AS, Hau CM et al. The role of haematological factors in diabetic peripheral arterial disease: the Edinburgh Artery Study. Br J Haemat 1999;105:648-54.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]

The British Journal of Diabetes & Vascular Disease, Vol. 2, No. 5, 358-362 (2002)
DOI: 10.1177/14746514020020050301
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
 Am. J. Physiol. Heart Circ. Physiol.Home page
I. Lekli, G. Szabo, B. Juhasz, S. Das, M. Das, E. Varga, L. Szendrei, R. Gesztelyi, J. Varadi, I. Bak, et al.
Protective mechanisms of resveratrol against ischemia-reperfusion-induced damage in hearts obtained from Zucker obese rats: the role of GLUT-4 and endothelin
Am J Physiol Heart Circ Physiol, February 1, 2008; 294(2): H859 - H866.
[Abstract] [Full Text] [PDF]

Home page
 J. Pharmacol. Exp. Ther.Home page
S. G. Burke, C. L. Wainwright, I. Vojnovic, T. Warner, D. G. Watson, and B. L. Furman
The Effect of NCX4016 [2-Acetoxy-benzoate 2-(2-nitroxymethyl)-phenyl Ester] on the Consequences of Ischemia and Reperfusion in the Streptozotocin Diabetic Rat
J. Pharmacol. Exp. Ther., March 1, 2006; 316(3): 1107 - 1114.
[Abstract] [Full Text] [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 Kluft, C.
Right arrow Articles by Jespersen, J.
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?