Low fasting glucose is associated with enhanced thrombin generation and unfavorable fibrin clot properties in type 2 diabetic patients with high cardiovascular risk

Cardiovascular Diabetology

Volumn 14, Issue 1, 2015, Pages

  Gajos, Grzegorz ^a   Konieczynska, Malgorzata ^b   Zalewski, Jaroslaw ^a   Undas, Anetta ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^b Krakowski Szpital Specjalistyczny Im Jana Pawła II   (Poland)

Author keywords

Blood glucose; Cardiovascular diseases; Diabetes complications; Fibrin; Hypoglycemia

Indexed keywords

FIBRINOGEN; GLUCOSE; HEMOGLOBIN A1C; INSULIN; THROMBIN; FIBRIN; GLUCOSE BLOOD LEVEL;

ADULT; AGED; ARTICLE; BLOOD CLOT LYSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; DIET RESTRICTION; EUGLOBULIN LYSIS TEST; FEMALE; FIBRIN CLOT; FIBRINOLYSIS; GLUCOSE BLOOD LEVEL; HUMAN; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PERMEABILITY; RISK FACTOR; BLOOD; BLOOD CLOTTING; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; METABOLISM; MIDDLE AGED; PHYSIOLOGY;

AGED; BLOOD COAGULATION; BLOOD GLUCOSE; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; FASTING; FEMALE; FIBRIN; HUMANS; MALE; MIDDLE AGED; RISK FACTORS; THROMBIN;

EID: 84930196737     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-015-0207-2     Document Type: Article

References (41)

1. Boussageon R, Bejan-Angoulvant T, Saadatian-Elahi M, Lafont S, Bergeonneau C, Kassaï B, et al. Effect of intensive glucose lowering treatment on all cause mortality, cardiovascular death, and microvascular events in type 2 diabetes: meta-analysis of randomised controlled trials. BMJ. 2011;343:d4169.
2. Zoungas S, Patel A, Chalmers J, de Galan BE, Li Q, Billot L, et al. Severe hypoglycemia and risks of vascular events and death. N Engl J Med. 2010;63:1410-08.
3. Wright RJ, Frier BM. Vascular disease and diabetes: is hypoglycaemia an aggravating factor? Diabetes Metab Res Rev. 2008;24:353-63.
4. Gogitidze Joy N, Hedrington MS, Briscoe VJ, Tate DB, Ertl AC, Davis SN. Effects of acute hypoglycemia on inflammatory and pro-atherothrombotic biomarkers in individuals with type 1 diabetes and healthy individuals. Diabetes Care. 2010;33:1529-35.
5. Wright RJ, Newby DE, Stirling D, Ludlam CA, Macdonald IA, Frier BM. Effects of acute insulin-induced hypoglycemia on indices of inflammation: putative mechanism for aggravating vascular disease in diabetes. Diabetes Care. 2010;33:1591-7.
6. DECODE Study Group, European diabetes epidemiology group. Is the current definition for diabetes relevant to mortality risk from all causes and cardiovascular and noncardiovascular diseases? Diabetes Care. 2003;26:688-96.
7. Emerging Risk Factors Collaboration. Glycated hemoglobin measurement and prediction of cardiovascular disease. JAM. 2014;311:1225-33.
8. Rana OA, Byrne CD, Greaves K. Intensive glucose control and hypoglycaemia: a new cardiovascular risk factor? Heart. 2014;100:21-7.
9. Dunn EJ, Ariëns RA, Grant PJ. The influence of type 2 diabetes on fibrin structure and function. Diabetologia. 2005;48:1198-206.
10. Dunn EJ, Philippou H, Ariëns RA, Grant PJ. Molecular mechanisms involved in the resistance of fibrin to clot lysis by plasmin in subjects with type 2 diabetes mellitus. Diabetologia. 2006;49:1071-80.
11. Ajjan RA, Gamlen T, Standeven KF, Mughal S, Hess K, Smith KA, et al. Diabetes is associated with posttranslational modifications in plasminogen resulting in reduced plasmin generation and enzyme-specific activity. Blood. 2013;122:134-42.
12. Jax TW, Peters AJ, Plehn G, Schoebel FC. Hemostatic risk factors in patient with coronary artery disease and type 2 diabetes - a two year follow-up of 24 patients. Cardiovasc Diabetol. 2009;8:48.
13. Kuliczkowski W, Greif M, Gasior M, Kaczmarski J, Pres D, Poloński L. Effect of platelet and inflammatory system activation on outcomes in diabetic patient with ST segment elevation myocardial infarction treated with primary percutaneous coronary intervention. Kardiol Pol. 2011;69:531-7.
14. Undas A, Ariëns RAS. Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolism diseases. Arterioscler, Thromb, Vasc Biol. 2011;31:e88-99.
15. Konieczyńska M, Fil K, Bazanek M, Undas A. Prolonged duration of type 2 diabetes is associated with increased thrombin generation, prothrombotic fibrin clot phenotype and impaired fibrinolysis. Thromb Haemost. 2014;111(4):685-93.
16. Undas A. Acquired dysfibrinogenemia in atherosclerotic vascular disease. Pol Arch Med Wewn. 2011;121:310-8.
17. Ariëns RA. Fibrin(ogen) and thrombotic disease. J Thromb Haemost. 2013;Suppl 1:294-305.
18. Hutton RA, Mikhailidis D, Dormandy KM, Ginsburg J. Platelet aggregation studies during transient hypoglycaemia: a potential method for evaluating platelet function. J Clin Pathol. 1979;32:434-8.
19. Trovati M, Anfossi G, Cavalot F, Vitali S, Massucco P, Mularoni E, et al. Studies on mechanisms involved in hypoglycemia-induced platelet activation. Diabetes. 1986;35:818-25.
20. Takeda H, Kishikawa H, Shinohara M, Miyata T, Suzaki K, Fukushima H, et al. Effect of alpha 2-adrenoceptor antagonist on platelet activation during insulin-induced hypoglycaemia in type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1988;31:657-63.
21. Ibbotson SH, Catto A, Davies JA, Grant PJ. The effect of insulin-induced hypoglycaemia on factor VIII:C concentrations and thrombin activity in subjects with type 1 (insulin-dependent) diabetes. Thromb Haemost. 1995;73:243-6.
22. Fisher BM, Quin JD, Rumley A, Lennie SE, Small M, MacCuish AC, et al. Effects of acute insulin-induced hypoglycaemia on haemostasis, fibrinolysis and haemorheology in insulin-dependent diabetic patients and control subjects. Clin Sci (Lond). 1991;80:525-31.
23. Chow EYK, Iqbal A, Phoenix F, Heller SR, Ajjan R. Hypoglycaemia promotes thrombosis and inflammation for at least one week in patients with type 2 diabetes (Abstract). Diabetologia. 2013;56:S243.
24. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2011;34 Suppl 1:S62-69.
25. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care. 2010;33:2285-93.
26. Gajos G, Zalewski J, Rostoff P, Nessler J, Piwowarska W, Undas A. Reduced thrombin formation and altered fibrin clot properties induced by polyunsaturated omega-3 fatty acids on top of dual antiplatelet therapy in patients undergoing percutaneous coronary intervention (OMEGA-PCI clot). Arterioscler, Thromb, Vasc Biol. 2011;31:1696-702.
27. Undas A, Szuldrzynski K, Stepien E, Zalewski J, Godlewski J, Tracz W, et al. Reduced clot permeability and susceptibility to lysis in patients with acute coronary syndrome: effects of inflammation and oxidative stress. Atherosclerosis. 2008;196:551-8.
28. Collet JP, Mishal Z, Lesty C, Mirshahi M, Peyne J, Baumelou A, et al. Abnormal fibrin clot architecture in nephritic patients is related to hypofibrinolysis: influence of plasma biochemical modifications. Thromb Haemost. 1999;82:1482-9.
29. Mills JD, Ariens RA, Mansfield MW, Grant PJ. Altered fibrin clot structure in the healthy relatives of patients with premature coronary artery disease. Circulation. 2002;106:1938-42.
30. Meltzer ME, Doggen CJ, de Groot PG, Rosendaal FR, Lisman T. Reduced plasma fibrinolytic capacity as a potential risk factor for a first myocardial infarction in young men. Br J Haematol. 2009;145:121-12.
31. Al Dieri R, de Laat B, Hemker HC. Thrombin generation: what have we learned? Blood Rev. 2012;26:197-203.
32. Wolberg AS. Thrombin generation and fibrin clot structure. Blood Rev. 2007;21:131-42.
33. Buys AV, Van Rooy MJ, Soma P, Van Papendorp D, Lipinski B, Pretorius E. Changes in red blood cell membrane structure in type 2 diabetes: a scanning electron and atomic force microscopy study. Cardiovasc Diabetol. 2013;12:25.
34. Pretorius E. The adaptability of red blood cells. Cardiovasc Diabetol. 2013;12:63.
35. Lipinski B, Pretorius E. Novel pathway of iron-induced blood coagulation: implications for diabetes mellitus and its complications. Pol Arch Med Wewn. 2012;122:115-22.
36. Kowalska MA, Rauova L, Poncz M. Role of the platelet chemokine platelet factor 4 (PF4) in hemostasis and thrombosis. Thromb Res. 2010;125:292-6.
37. Mutch NJ, Engel R, Uitte de Willige S, Philippou H, Ariëns RA. Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. Blood. 2010;115:3980-8.
38. Amelot AA, Tagzirt M, Ducouret G, Kuen RL, Le Bonniec BF. Platelet factor 4 (CXCL4) seals blood clots by altering the structure of fibrin. J Biol Chem. 2007;282:710-20.
39. Undas A, Wiek I, Stepien E, Zmudka K, Tracz W. Hyperglycemia is associated with enhanced thrombin formation, platelet activation, and fibrin clot resistance to lysis in patients with acute coronary syndrome. Diabetes Care. 2008;31:1590-5.
40. Jörneskog G, Hansson LO, Wallen NH, Yngen M, Blombäck M. Increased plasma fibrin gel porosity in patients with Type I diabetes during continuous subcutaneous insulin infusion. J Thromb Haemost. 2003;1:1195-201.
41. Goto A, Arah OA, Goto M, Terauchi Y, Noda M. Severe hypoglycaemia and cardiovascular disease: systematic review and meta-analysis with bias analysis. BMJ. 2013;347:f4533.