Hyperglycemia following recovery from hypoglycemia worsens endothelial damage and thrombosis activation in type 1 diabetes and in healthy controls

Nutrition, Metabolism and Cardiovascular Diseases

Volumn 24, Issue 2, 2014, Pages 116-123

  Ceriello, A ^a,b   Novials, A ^a,b   Ortega, E ^a,b   Pujadas, G ^a,b,c,d   La Sala, L ^a   Testa, R ^a,b,c,d   Bonfigli, A R ^c   Genovese, S ^d  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INRCA   (Italy)

^d IRCCS MULTIMEDICA   (Italy)

Author keywords

8 iso PGF2 ; Hyperglycemia; Hypoglycemia; Oxidative stress; TAT; Thrombosis; VWFAc; VWFAg

Indexed keywords

CHOLESTEROL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM LESION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; OXIDATIVE STRESS; RISK FACTOR; THROMBOSIS; YOUNG ADULT;

HYPERGLYCEMIA; HYPOGLYCEMIA; OXIDATIVE STRESS; THROMBOSIS;

ADULT; ANTITHROMBIN III; ASCORBIC ACID; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; DINOPROST; ENDOTHELIUM, VASCULAR; FEMALE; HEALTHY VOLUNTEERS; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIA; MALE; OXIDATIVE STRESS; P-SELECTIN; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN PRECURSORS; PROTHROMBIN; THROMBOSIS; VON WILLEBRAND FACTOR; YOUNG ADULT;

EID: 84894225197     PISSN: 09394753     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.numecd.2013.05.003     Document Type: Article

References (40)

1. Auer R.N. Progress review: hypoglycemic brain damage. Stroke 1986, 17:699-708.
2. Wright R.J., Frier B.M. Vascular disease and diabetes: is hypoglycaemia an aggravating factor?. Diabetes Metab Res Rev 2008, 24:353-363.
3. Vazzana N., Ranalli P., Cuccurullo C., Davì G. Diabetes mellitus and thrombosis. Thromb Res 2012, 129:371-377.
4. Hutton R.A., Mikhailidis D., Dormandy K.M., Ginsburg J. Platelet aggregation studies during transient hypoglycaemia. J Clin Pathol 1979, 32:434-438.
5. 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, 35:818-825.
6. Monnier L.H., Lachkar H., Richard J.L., Colette C., Borgel D., Orsetti A., et al. Plasma β-thromboglobulin response to insulin-induced hypoglycemia in type 1 diabetic patients. Diabetes 1984, 33:907-909.
7. Gogitidze Joy N., Hedrington M.S., Briscoe V.J., Tate D.B., Ertl A.C., Davis S.N. Effects of acute hypoglycemia on inflammatory and pro-atherothrombotic biomarkers in individuals with type 1 diabetes and healthy individuals. Diabetes Care 2010, 33:1529-1535.
8. Whincup P.H., Danesh J., Walker M., Lennon L., Thomson A., Appleby P., et al. von Willebrand factor and coronary heart disease: prospective study and meta-analysis. Eur Heart J 2002, 23:1764-1770.
9. Fisher B.M., Quin J.D., Rumley A., Lennie S.E., Small M., MacCuish A.C., et al. Effects of acute insulin induced hypoglycaemia on haemostasis, fibrinolysis, and haemorrheology in insulin-dependent diabetic patients and control subjects. Clin Sci 1991, 80:525-531.
10. Ibbotson S.H., Catto A., Davies J.A., Grant P.J. 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, 73:243-246.
11. Ceriello A., Giacomello R., Stel G., Motz E., Taboga C., Tonutti L., et al. Hyperglycemia-induced thrombin formation in diabetes. The possible role of oxidative stress. Diabetes 1995, 44:924-928.
12. Lemkes B.A., Hermanides J., Devries J.H., Holleman F., Meijers J.C., Hoekstra J.B. Hyperglycemia: a prothrombotic factor?. JThromb Haemost 2010, 8:1663-1669.
13. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010, 107:1058-1070.
14. Wang J., Alexanian A., Ying R., Kizhakekuttu T.J., Dharmashankar K., Vasquez-Vivar J., et al. Acute exposure to low glucose rapidly induces endothelial dysfunction and mitochondrial oxidative stress: role for AMP kinase. Arterioscler Thromb Vasc Biol 2012, 32:712-720.
15. Suh S.W., Gum E.T., Hamby A.M., Chan P.H., Swanson R.A. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest 2007, 117:910-918.
16. Ceriello A., Novials A., Ortega E., La Sala L., Pujadas G., Testa R., et al. Evidence that hyperglycemia after recovery from hypoglycemia worsens endothelial function and increases oxidative stress and inflammation in healthy control subjects and subjects with type 1 diabetes. Diabetes 2012, 61:2993-2997.
17. Ewing D.J., Martyn C.N., Young R.J., Clarke B.F. The value of cardiovascular autonomic function tests: 10 year experience in diabetes. Diabetes Care 1985, 8:491-498.
18. Gold A.E., MacLeod K.M., Frier B.M. Frequency of severe hypoglycemia in patients with type 1 diabetes and impaired awareness of hypoglycemia. Diabetes Care 1994, 17:697-703.
19. Amiel S.A., Tamborlane W.V., Simonson D.C., Sherwin R.S. Defective glucose counterregulation after strict glycemic control of insulin-dependent diabetes mellitus. N Engl J Med 1987, 316:1376-1383.
20. Mullan B.A., Ennis C.N., Fee H.J., Young I.S., McCance D.R. Pretreatment with intravenous ascorbic acid preserves endothelial function during acute hyperglycaemia (R1). Clin Exp Pharmacol Physiol 2005, 32:340-345.
21. Davis J.E., McDonald J.M., Jarett L. A high-performance liquid chromatography method for hemoglobin A1c. Diabetes 1978, 27:102-107.
22. Wide L., Porath J. Radioimmunoassay of proteins with the uses of sephadex-coupled antibodies. Biochim Biophys Acta 1966, 130:257-260.
23. Ceriello A., Mercuri F., Quagliaro L., Assaloni R., Motz E., Tonutti L., et al. Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia 2001, 44:834-838.
24. Smith K.A., Shepherd J., Wakil A., Kilpatrick E.S. A comparison of methods for the measurement of 8-isoPGF(2α): a marker of oxidative stress. Ann Clin Biochem 2011, 48(Pt 2):147-154.
25. Ceriello A. Hyperglycaemia and the vessel wall: the pathophysiological aspects on the atherosclerotic burden in patients with diabetes. Eur J Cardiovasc Prev Rehabil 2010, 17(Suppl. 1):S15-S19.
26. Wei M., Gibbons L.W., Mitchell T.L., Kampert J.B., Stern M.P., Blair S.N. Low fasting plasma glucose level as a predictor of cardiovascular disease and all-cause mortality. Circulation 2000, 101:2047-2052.
27. Johnston S.S., Conner C., Aagren M., Smith D.M., Bouchard J., Brett J. Evidence linking hypoglycemic events to an increased risk of acute cardiovascular events in patients with type 2 diabetes. Diabetes Care 2011, 34:1164-1170.
28. Gerstein H.C., Miller M.E., Byington R.P., Goff D.C., Bigger J.T., Buse J.B., et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 2008, 358:2545-2559. Action to Control Cardiovascular Risk in Diabetes Study Group.
29. Duckworth W., Abraira C., Moritz T., Reda D., Emanuele N., Reaven P.D., et al. Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 2009, 360:129-139. VADT Investigators.
30. Zoungas S., Patel A., Chalmers J., de Galan B.E., Li Q., Billot L., et al. Severe hypoglycemia and risks of vascular events and death. N Engl J Med 2010, 363:1410-1418. ADVANCE Collaborative Group.
31. Genuth S., Ismail-Beigi F. Clinical implications of the ACCORD trial. J Clin Endocrinol Metab 2012, 97:41-48.
32. Gruden G., Barutta F., Chaturvedi N., Schalkwijk C., Stehouwer C.D., Witte D.R., et al. Severe hypoglycemia and cardiovascular disease incidence in type 1 diabetes: the EURODIAB Prospective Complications Study. Diabetes Care 2012, 35:1598-1604.
33. Snell-Bergeon J.K., Nadeau K. Cardiovascular disease risk in young people with type 1 diabetes. J Cardiovasc Transl Res 2012, 5:446-462.
34. Giménez M., López J.J., Castell C., Conget I. Hypoglycaemia and cardiovascular disease in type 1 diabetes. Results from the Catalan National Public Health Registry on insulin pump therapy. Diabetes Res Clin Pract 2012, 96:e23-25.
35. Angiolillo D.J. The evolution of antiplatelet therapy in the treatment of acute coronary syndromes: from aspirin to the present day. Drugs 2012, 72:2087-2116.
36. Briscoe V.J., Ertl A.C., Tate D.B., Dawling S., Davis S.N. Effects of a selective serotonin reuptake inhibitor, fluoxetine, on counterregulatory responses to hypoglycemia in healthy individuals. Diabetes 2008, 57:2453-2460.
37. Briscoe V.J., Ertl A.C., Tate D.B., Davis S.N. Effects of the selective serotonin reuptake inhibitor fluoxetine on counterregulatory responses to hypoglycemia in individuals with type 1 diabetes. Diabetes 2008, 57:3315-3322.
38. Ceriello A., Ihnat M.A., Thorpe J.E. Clinical review 2: the "metabolic memory": is more than just tight glucose control necessary to prevent diabetic complications?. J Clin Endocrinol Metab 2009, 94:410-415.
39. Adler G.K., Bonyhay I., Failing H., Waring E., Dotson S., Freeman R. Antecedent hypoglycemia impairs autonomic cardiovascular function: implications for rigorous glycemic control. Diabetes 2009, 58:360-366.
40. Ceriello A., Ihnat M.A. 'Glycaemic variability': a new therapeutic challenge in diabetes and the critical care setting. Diabet Med 2010, 27:862-867.