Full Text:   <2558>

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CLC number: R587.1

On-line Access: 2015-09-05

Received: 2015-03-18

Revision Accepted: 2015-06-09

Crosschecked: 2015-08-10

Cited: 5

Clicked: 4825

Citations:  Bibtex RefMan EndNote GB/T7714


Barbara Ruszkowska-Ciastek


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Journal of Zhejiang University SCIENCE B 2015 Vol.16 No.9 P.788-795


Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2

Author(s):  Barbara Ruszkowska-Ciastek, Alina Sokup, Tomasz Wernik, Piotr Rhone, Krzysztof Góralczyk, Kornel Bielawski, Agata Fijałkowska, Aleksandra Nowakowska, Elżbieta Rhone, Danuta Rość

Affiliation(s):  Department of Pathophysiology, Faculty of Pharmacy, Nicolaus Copernicus University in Toruń, Collegium Medicum in Bydgoszcz, Bydgoszcz PL 85-094, Poland

Corresponding email(s):   ruszkowska.basia@gmail.com

Key Words:  Diabetes, Extrinsic coagulation pathway, Angiogenesis, Glomerular filtration rate

Barbara Ruszkowska-Ciastek, Alina Sokup, Tomasz Wernik, Piotr Rhone, Krzysztof Góralczyk, Kornel Bielawski, Agata Fijałkowska, Aleksandra Nowakowska, Elżbieta Rhone, Danuta Rość. Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2[J]. Journal of Zhejiang University Science B, 2015, 16(9): 788-795.

@article{title="Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2",
author="Barbara Ruszkowska-Ciastek, Alina Sokup, Tomasz Wernik, Piotr Rhone, Krzysztof Góralczyk, Kornel Bielawski, Agata Fijałkowska, Aleksandra Nowakowska, Elżbieta Rhone, Danuta Rość",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2
%A Barbara Ruszkowska-Ciastek
%A Alina Sokup
%A Tomasz Wernik
%A Piotr Rhone
%A Krzysztof Góralczyk
%A Kornel Bielawski
%A Agata Fijałkowska
%A Aleksandra Nowakowska
%A Elżbieta Rhone
%A Danuta Rość
%J Journal of Zhejiang University SCIENCE B
%V 16
%N 9
%P 788-795
%@ 1673-1581
%D 2015
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1500066

T1 - Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2
A1 - Barbara Ruszkowska-Ciastek
A1 - Alina Sokup
A1 - Tomasz Wernik
A1 - Piotr Rhone
A1 - Krzysztof Góralczyk
A1 - Kornel Bielawski
A1 - Agata Fijałkowska
A1 - Aleksandra Nowakowska
A1 - Elżbieta Rhone
A1 - Danuta Rość
J0 - Journal of Zhejiang University Science B
VL - 16
IS - 9
SP - 788
EP - 795
%@ 1673-1581
Y1 - 2015
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1500066

Objective: diabetes, including type 1 and type 2, is associated with the hypercoagulable state. The aim of this study is to evaluate the concentration of selected hemostatic parameters and vascular endothelial growth factor-A (VEGF-A) in diabetic subjects. Methods: The study was conducted in 62 patients with diabetes. Group I consisted of 27 patients having uncontrolled diabetes with microalbuminuria and Group II included 35 well-controlled diabetic patients. The control group was made up of 25 healthy volunteers. In the citrate plasma, the concentrations of tissue factor (TF), tissue factor pathway inhibitor (TFPI), thrombin-antithrombin (TAT) complexes, and D-dimer were assayed. Serum concentrations of VEGF-A, lipid profile, creatinine, and plasma fasting glucose were measured and in the versene plasma the concentration of HbA1c was determined. Results: In the patients with uncontrolled diabetes, higher concentrations of TF, TFPI, and VEGF-A were observed, as compared with the well-controlled diabetics group and the control group. A significantly lower activity of antiplasmin was reported in patients from Group I as compared with the control group. In Group I, using the multivariate regression analysis, the glomerular filtration rate was independently associated with VEGF-A and dependently associated with total cholesterol. Conclusions: The study showed higher concentrations of TF and TFPI in the patients with uncontrolled diabetes with microalbuminuria, which is associated with rapid neutralization of the thrombin formation, since TFPI inhibits the complex of TF/VIIa/Ca2+. The manifestation of the above suggestions is the correct TAT complexes and D-dimer, which indicates a low grade of prothrombotic risk in this group of patients, but a higher risk of vascular complications.




Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Adams, M.J., Irish, A.B., Watts, G.F., et al., 2008. Hypercoagulability in chronic kidney disease is associated with coagulation activation but not endothelial function. Thromb. Res., 123(2):374-380.

[2]Alzahrani, S.H., Ajjan, R.A., 2010. Coagulation and fibrinolysis in diabetes. Diabetes Vasc. Dis. Res., 7(4):260-273.

[3]Boden, G., Vaidyula, V.R., Homko, C., et al., 2007. Circulating tissue factor procoagulant activity and thrombin generation in patients with type 2 diabetes: effects of insulin and glucose. J. Clin. Endocrinol. Metab., 92(11):4352-4358.

[4]Breitenstein, A., Tanner, F.C., Luscher, T.F., 2010. Tissue factor and cardiovascular disease: quo vadis? Circ. J., 74(1):3-12.

[5]Chu, A.J., 2011. Tissue factor, blood coagulation, and beyond: an overview. Int. J. Inflam., 2011:367284.

[6]DelGiudice, L.A., White, G.A., 2009. The role of tissue factor and tissue factor pathway inhibitor in health and disease states. J. Vet. Emerg. Crit. Care (San Antonio), 19(1):23-29.

[7]El-Hagracy, R.S., Kamal, G.M., Sabry, I.M., et al., 2010. Tissue factor, tissue factor pathway inhibitor and factor VII activity in cardiovascular complicated type 2 diabetes mellitus. Oman Med. J., 25(3):173-178.

[8]Ghafoor, F., Bano, K.A., Malik, T., et al., 2004. Microalbuminuria as an indicator of kidney function among diabetics. J. Coll. Phys. Surg. Pak., 14(11):670-672.

[9]Hess, K., Grant, P.J., 2011. Inflammation and thrombosis in diabetes. Thromb. Haemost., 105(Suppl. 1):S43-S54.

[10]Kacso, I.M., Bondor, C.I., Kacso, G., 2012. Soluble serum Klotho in diabetic nephropathy: relationship to VEGF-A. Clin. Biochem., 45(16-17):1415-1420.

[11]Kanesaki, Y., Suzuki, D., Uehara, G., et al., 2005. Vascular endothelial growth factor gene expression is correlated with glomerular neovascularization in human diabetic nephropathy. Am. J. Kidney Dis., 45(2):288-294.

[12]Kota, S.K., Meher, L.K., Jammula, S., et al., 2012. Aberrant angiogenesis: the gateway to diabetic complications. Indian J. Endocrinol. Metab., 16(6):918-930.

[13]Kowalski, J., Sliwczyńska-Rodziewicz, D., Kowalczyk, E., et al., 2011. Plasma nitric oxide and vascular endothelial growth factor levels in patients with metabolic syndrome and co-existing vascular complications. Pol. Med. J., 30(178):249-252 (in Polish).

[14]Kubisz, P., Chudy, P., Staśko, J., et al., 2010. Circulating vascular endothelial growth factor in the normo-and/or microalbuminuric patients with type 2 diabetes mellitus. Acta Diabetol., 47(2):119-124.

[15]Lizakowski, S., Zdrojewski, Z., Jagodzinski, P., et al., 2007. Plasma tissue factor and tissue factor pathway inhibitor in patients with primary glomerulonephritis. Scand. J. Urol. Nephrol., 41(3):237-242.

[16]Mahdy, R.A., Nada, W.M., Hadhoud, K.M., et al., 2010. The role of vascular endothelial growth factor in the progression of diabetic vascular complications. Eye (Lond.), 24(10):1576-1584.

[17]Malyszko, J., Malyszko, J.S., Mysliwiec, M., 2004. Endothelial cell injury markers in chronic renal failure on conservative treatment and continuous ambulatory peritoneal dialysis. Kidney Blood Press. Res., 27(2):71-77.

[18]Olokoba, A.B., Obateru, O.A., Olokoba, L.B., 2012. Type 2 diabetes mellitus: a review of current trends. Oman Med. J., 27(4):269-273.

[19]Opstad, T.B., Pettersen, A.A., Weiss, T., et al., 2010. Gender differences of polymorphisms in the TF and TFPI genes, as related to phenotypes in patients with coronary heart disease and type-2 diabetes. Thromb. J., 8(1):7.

[20]Pawlak, K., Ulazka, B., Mysliwiec, M., et al., 2012. Vascular endothelial growth factor and uPA/suPAR system in early and advanced chronic kidney disease patients: a new link between angiogenesis and hyperfibrinolysis? Transl. Res., 160(5):346-354.

[21]Ruszkowska-Ciastek, B., Sokup, A., Socha, M.W., et al., 2014. A preliminary evaluation of VEGF-A, VEGFR1 and VEGFR2 in patients with well-controlled type 2 diabetes mellitus. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 15(6):575-581.

[22]Ruszkowska-Ciastek, B., Sokup, A., Wernik, W., et al., 2015. Effect of uncontrolled hyperglycemia on levels of adhesion molecules in patients with diabetes mellitus type 2. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 16(5):355-361.

[23]Sherif, E.M., Elbarbary, N.S., Abd Al Aziz, M.M., et al., 2014. Plasma thrombin-activatable fibrinolysis inhibitor levels in children and adolescents with type 1 diabetes mellitus: possible relation to diabetic microvascular complications. Blood Coagul. Fibrinolysis, 25(5):451-457.

[24]Steffel, J., Lüscher, M.D., Tanner, F.C., 2006. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation, 113(5):722-731.

[25]Veron, D., Reidy, K.J., Bertuccio, C., et al., 2010. Overexpression of VEGF-A in podocytes of adult mice causes glomerular disease. Kidney Int., 77(11):989-999.

[26]Xu, L., Kanasaki, K., Kitada, M., et al., 2012. Diabetic angiopathy and angiogenic defects. Fibrogenesis Tissue Repair, 5(1):13.

[27]Yuan, J., Guo, Q., Qureshi, A.R., et al., 2013. Circulating vascular endothelial growth factor (VEGF) and its soluble receptor 1 (sVEGFR-1) are associated with inflammation and mortality in incident dialysis patients. Nephrol. Dial. Transplant., 28(9):2356-2363.

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