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Circulation. 1999;99:2239-2242

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(Circulation. 1999;99:2239-2242.)
© 1999 American Heart Association, Inc.


Clinical Investigation and Reports

Effect of Diabetes Mellitus on Formation of Coronary Collateral Vessels

Adnan Abaci, MD; Abdurrahman Oguzhan, MD; Sinan Kahraman, MD; Namik Kemal Eryol, MD; Sükrü Ünal, MD; Hüseyin Arinç, MD; Ali Ergin, MD

From the Department of Cardiology, Erciyes University School of Medicine, Kayseri, Turkey.

Correspondence to Adnan Abaci, Selanik Cad, Sinema Onay, Karsisi, Kiliç Apt 29/15, Kayseri-38010, Turkey. E-mail abacia{at}hotmail.com

Background—Although myocardial ischemia is known to be significantly related to the development of coronary collateral vessels (CCVs), there is considerable variation between patients with ischemic heart disease in the presence of collateral development. The nature of this variability is not well known. Likewise, it remains unclear whether diabetes mellitus (DM) has any effect on CCVs. The aim of this study was to evaluate the effect of DM on CCVs.

Methods and Results—Of the patients who underwent coronary angiography during the interval between March 1, 1993, and June 20, 1998, in our institution, 306 were diabetic. Those patients in whom coronary angiography is normal or severity of coronary artery stenosis is thought not to be sufficient for the development of CCVs (<75%) were excluded from the study. A total of 205 patients (mean age, 59±8 years) met the criteria for the DM group. For case-control matching, 205 consecutive nondiabetic patients (mean age, 58±9 years) who had >=1 diseased vessel with >75% stenosis were included in the control group. The CCVs were graded according to the Rentrop scoring system, and the collateral score was calculated by summing the Rentrop numbers of every patient. There was no statistical difference between patients with and without DM in clinical baseline characteristics. The mean number of diseased vessels in the DM group (1.58±0.68) was higher than that in the nondiabetic group (1.42±0.65, P=0.005). The mean collateral score was 2.41±2.20 in the DM group and 2.60±2.39 in the control group. After confounding variables were controlled for, the collateral score in the diabetic group was significantly different from that in the nondiabetic group (P=0.034).

Conclusions—Our findings suggest that CCV development is poorer in patients with than in patients without DM. Thus, we can speculate that DM is an important factor affecting CCV development.


Key Words: collateral circulation • coronary disease • diabetes mellitus




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M Fujita and K Tambara
Recent insights into human coronary collateral development
Heart, March 1, 2004; 90(3): 246 - 250.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
C. Calvi, P. Dentelli, M. Pagano, A. Rosso, M. Pegoraro, S. Giunti, G. Garbarino, G. Camussi, L. Pegoraro, and M. F. Brizzi
Angiopoietin 2 Induces Cell Cycle Arrest in Endothelial Cells: A Possible Mechanism Involved in Advanced Plaque Neovascularization
Arterioscler Thromb Vasc Biol, March 1, 2004; 24(3): 511 - 518.
[Abstract] [Full Text]


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CirculationHome page
N. E.J. West, P. N. Ruygrok, C. M.C. Disco, M. W.I. Webster, W. K. Lindeboom, W. W. O'Neill, N. F. Mercado, and P. W. Serruys
Clinical and Angiographic Predictors of Restenosis After Stent Deployment in Diabetic Patients
Circulation, February 24, 2004; 109(7): 867 - 873.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
C. J.M. Loomans, E. J.P. de Koning, F. J.T. Staal, M. B. Rookmaaker, C. Verseyden, H. C. de Boer, M. C. Verhaar, B. Braam, T. J. Rabelink, and A.-J. van Zonneveld
Endothelial Progenitor Cell Dysfunction: A Novel Concept in the Pathogenesis of Vascular Complications of Type 1 Diabetes
Diabetes, January 1, 2004; 53(1): 195 - 199.
[Abstract] [Full Text] [PDF]


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ANN INTERN MEDHome page
R. T. Hurst and R. W. Lee
Increased Incidence of Coronary Atherosclerosis in Type 2 Diabetes Mellitus: Mechanisms and Management
Ann Intern Med, November 18, 2003; 139(10): 824 - 834.
[Abstract] [Full Text] [PDF]


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Diabetes CareHome page
M. M. Graham, W. A. Ghali, P. D. Faris, P. D. Galbraith, C. M. Norris, and M. L. Knudtson
Sex Differences in the Prognostic Importance of Diabetes in Patients With Ischemic Heart Disease Undergoing Coronary Angiography
Diabetes Care, November 1, 2003; 26(11): 3142 - 3147.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
R. Tamarat, J.-S. Silvestre, M. Huijberts, J. Benessiano, T. G. Ebrahimian, M. Duriez, M.-P. Wautier, J. L. Wautier, and B. I. Levy
Blockade of advanced glycation end-product formation restores ischemia-induced angiogenesis in diabetic mice
PNAS, July 8, 2003; 100(14): 8555 - 8560.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
G. S. Werner, B. M. Richartz, S. Heinke, M. Ferrari, and H. R. Figulla
Impaired acute collateral recruitment as a possible mechanism for increased cardiac adverse events in patients with diabetes mellitus
Eur. Heart J., June 2, 2003; 24(12): 1134 - 1142.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
N. van Royen, I. Hoefer, M. Bottinger, J. Hua, S. Grundmann, M. Voskuil, C. Bode, W. Schaper, I. Buschmann, and J.J. Piek
Local Monocyte Chemoattractant Protein-1 Therapy Increases Collateral Artery Formation in Apolipoprotein E-Deficient Mice but Induces Systemic Monocytic CD11b Expression, Neointimal Formation, and Plaque Progression
Circ. Res., February 7, 2003; 92(2): 218 - 225.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
K. Hirata, T.-S. Li, M. Nishida, H. Ito, M. Matsuzaki, S. Kasaoka, and K. Hamano
Autologous bone marrow cell implantation as therapeutic angiogenesis for ischemic hindlimb in diabetic rat model
Am J Physiol Heart Circ Physiol, January 1, 2003; 284(1): H66 - H70.
[Abstract] [Full Text] [PDF]


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CirculationHome page
O. M. Tepper, R. D. Galiano, J. M. Capla, C. Kalka, P. J. Gagne, G. R. Jacobowitz, J. P. Levine, and G. C. Gurtner
Human Endothelial Progenitor Cells From Type II Diabetics Exhibit Impaired Proliferation, Adhesion, and Incorporation Into Vascular Structures
Circulation, November 26, 2002; 106(22): 2781 - 2786.
[Abstract] [Full Text] [PDF]


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British Journal of Diabetes & Vascular DiseaseHome page
S. P Marso
Review: The pathogenesis of type 2 diabetes and cardiovascular disease
The British Journal of Diabetes & Vascular Disease, September 1, 2002; 2(5): 350 - 356.
[Abstract] [PDF]


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Am. J. Pathol.Home page
F. Facchiano, A. Lentini, V. Fogliano, S. Mancarella, C. Rossi, A. Facchiano, and M. C. Capogrossi
Sugar-Induced Modification of Fibroblast Growth Factor 2 Reduces Its Angiogenic Activity in Vivo
Am. J. Pathol., August 1, 2002; 161(2): 531 - 541.
[Abstract] [Full Text] [PDF]


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Ann. Thorac. Surg.Home page
T. Krabatsch, R. Petzina, H. Hausmann, A. Koster, and R. Hetzer
Factors influencing results and outcome after transmyocardial laser revascularization
Ann. Thorac. Surg., June 1, 2002; 73(6): 1888 - 1892.
[Abstract] [Full Text] [PDF]


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CirculationHome page
E. Chou, I. Suzuma, K. J. Way, D. Opland, A. C. Clermont, K. Naruse, K. Suzuma, N. L. Bowling, C. J. Vlahos, L. P. Aiello, et al.
Decreased Cardiac Expression of Vascular Endothelial Growth Factor and Its Receptors in Insulin-Resistant and Diabetic States: A Possible Explanation for Impaired Collateral Formation in Cardiac Tissue
Circulation, January 22, 2002; 105(3): 373 - 379.
[Abstract] [Full Text] [PDF]


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HeartHome page
Z S Kyriakides, S Psychari, N Chrysomallis, M Georgiadis, E Sbarouni, and D T Kremastinos
Type II diabetes does not prevent the recruitment of collateral vessels and the normal reduction of myocardial ischaemia on repeated balloon inflations during angioplasty
Heart, January 1, 2002; 87(1): 61 - 66.
[Abstract] [Full Text] [PDF]


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Mayo Clin Proc.Home page
K. M. Detre and R. Holubkov
Coronary Revascularization on Balance: Robert L. Frye Lecture
Mayo Clin. Proc., January 1, 2002; 77(1): 72 - 82.
[Abstract] [PDF]


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J Am Coll CardiolHome page
T. Pohl, C. Seiler, M. Billinger, E. Herren, K. Wustmann, H. Mehta, S. Windecker, F. R. Eberli, and B. Meier
Frequency distribution of collateral flow and factors influencing collateral channel development: Functional collateral channel measurement in 450 patients with coronary artery disease
J. Am. Coll. Cardiol., December 1, 2001; 38(7): 1872 - 1878.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
J. L. Tuttle, R. D. Nachreiner, A. S. Bhuller, K. W. Condict, B. A. Connors, B. P. Herring, M. C. Dalsing, and J. L. Unthank
Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression
Am J Physiol Heart Circ Physiol, September 1, 2001; 281(3): H1380 - H1389.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
R. Moreno, E. Garcia, J. Zamorano, J.-L. Lopez-Sendon, and L. Sanchez-Harguindey
Acute myocardial infarcation in diabetic patients. Are we acutally doing bad?
Eur. Heart J., August 1, 2001; 22(15): 1359 - 1361.
[Abstract] [PDF]


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CirculationHome page
A. K. M. T. Zaman, S. Fujii, H. Sawa, D. Goto, N. Ishimori, K. Watano, T. Kaneko, T. Furumoto, T. Sugawara, I. Sakuma, et al.
Angiotensin-Converting Enzyme Inhibition Attenuates Hypofibrinolysis and Reduces Cardiac Perivascular Fibrosis in Genetically Obese Diabetic Mice
Circulation, June 26, 2001; 103(25): 3123 - 3128.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
N. van Royen, J. J. Piek, I. Buschmann, I. Hoefer, M. Voskuil, and W. Schaper
Stimulation of arteriogenesis; a new concept for the treatment of arterial occlusive disease
Cardiovasc Res, February 16, 2001; 49(3): 543 - 553.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
J. Waltenberger
Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications
Cardiovasc Res, February 16, 2001; 49(3): 554 - 560.
[Abstract] [Full Text] [PDF]


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Eur J Heart FailHome page
T. Melchior, C. Rask-Madsen, C. Torp-Pedersen, P. Hildebrandt, L. Kober, and G. Jensen
The impact of heart failure on prognosis of diabetic and non-diabetic patients with myocardial infarction: a 15-year follow-up study
Eur J Heart Fail, January 1, 2001; 3(1): 83 - 90.
[Abstract] [Full Text] [PDF]


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CirculationHome page
T. Matsunaga, D. C. Warltier, D. W. Weihrauch, M. Moniz, J. Tessmer, and W. M. Chilian
Ischemia-Induced Coronary Collateral Growth Is Dependent on Vascular Endothelial Growth Factor and Nitric Oxide
Circulation, December 19, 2000; 102(25): 3098 - 3103.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
S. Dimmeler and A. M. Zeiher
Endothelial Cell Apoptosis in Angiogenesis and Vessel Regression
Circ. Res., September 15, 2000; 87(6): 434 - 439.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
T. Hammoud, J.-F. Tanguay, and M. G. Bourassa
Management of coronary artery disease: therapeutic options in patients with diabetes
J. Am. Coll. Cardiol., August 1, 2000; 36(2): 355 - 365.
[Abstract] [Full Text] [PDF]


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CirculationHome page
J. Waltenberger, J. Lange, and A. Kranz
Vascular Endothelial Growth Factor-A-Induced Chemotaxis of Monocytes Is Attenuated in Patients With Diabetes Mellitus : A Potential Predictor for the Individual Capacity to Develop Collaterals
Circulation, July 11, 2000; 102(2): 185 - 190.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
T. O'Brien
Adenoviral Vectors and Gene Transfer to the Blood Vessel Wall
Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1414 - 1416.
[Full Text] [PDF]


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NEJMHome page
K. M. Detre, M. S. Lombardero, M. M. Brooks, R. M. Hardison, R. Holubkov, G. Sopko, R. L. Frye, B. R. Chaitman, and The Bypass Angioplasty Revascularization Investiga
The Effect of Previous Coronary-Artery Bypass Surgery on the Prognosis of Patients with Diabetes Who Have Acute Myocardial Infarction
N. Engl. J. Med., April 6, 2000; 342(14): 989 - 997.
[Abstract] [Full Text] [PDF]


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CirculationHome page
W. Schaper and I. Buschmann
Collateral Circulation and Diabetes
Circulation, May 4, 1999; 99(17): 2224 - 2226.
[Full Text] [PDF]