Vascular Endothelial Growth Factor Genetic Variant is Associated with In-Stent Restenosis after Percutaneous Coronary Intervention
Abstract
Background: In-stent restenosis (ISR) is an inevitable complication of percutaneous coronary intervention, with genetic factors thought to play a role in its pathogenesis. The VEGF gene can have an inhibitory effect on ISR development. Accordingly, in the present study, we investigated the role of −2549 VEGF (insertion/deletion [I/D]) variants in ISR formation.
Methods: Patients with ISR (ISR+) (n=53) and patients without ISR (ISR-) (n=67) were enrolled in this case-control study based on follow-up angiography 1 year after percutaneous coronary intervention between 2019 and 2020. The clinical characteristics of the patients were evaluated, and the frequencies of the alleles and genotypes of −2549 VEGF (I/D) variants were determined using polymerase chain reaction. The χ2 test was performed for the calculation of genotypes and alleles. A P value of less than 0.05 was considered the level of significance.
Results: This study recruited 120 individuals at a mean age of 61.43±8.91 years in the ISR+ group and 62.09±7.94 years in the ISR- group. Women and men, respectively, comprised 26.4% and 73.6% of the ISR+ group and 43.3% and 56.7% of the ISR- group. A significant association was observed between the VEGF −2549 genotype frequency and ISR. The frequency of the insertion/insertion (I/I) allele was significantly higher in the ISR+ group than in the ISR- group, while the frequency of the D/D allele was higher in the latter group.
Conclusion: Regarding ISR development, the I/I allele may be a risk allele and the D/D allele a protective allele.
1. Habib A, Finn AV. Antiproliferative Drugs for Restenosis Prevention. Interv Cardiol Clin 2016;5:321-329.
2. Gaziano TA, Opie LH, Weinstein MC. Cardiovascular disease prevention with a multidrug regimen in the developing world: a cost-effectiveness analysis. Lancet 2006;368:679-686.
3. Nakamura N, Torii S, Tsuchiya H, Nakano A, Oikawa Y, Yajima J, Nakamura S, Nakano M, Masuda N, Ohta H, Yumoto K, Natsumeda M, Ijichi T, Ikari Y, Nakazawa G. Formation of Calcified Nodule as a Cause of Early In-Stent Restenosis in Patients Undergoing Dialysis. J Am Heart Assoc 2020;9:e016595.
4. Buccheri D, Piraino D, Andolina G, Cortese B. Understanding and managing in-stent restenosis: a review of clinical data, from pathogenesis to treatment. J Thorac Dis 2016;8:E1150-E1162.
5. Alfonso F, Byrne RA, Rivero F, Kastrati A. Current treatment of in-stent restenosis. J Am Coll Cardiol 2014;63:2659-2673.
6. Kokkinidis DG, Waldo SW, Armstrong EJ. Treatment of coronary artery in-stent restenosis. Expert Rev Cardiovasc Ther 2017;15:191-202.
7. Santulli G, Wronska A, Uryu K, Diacovo TG, Gao M, Marx SO, Kitajewski J, Chilton JM, Akat KM, Tuschl T, Marks AR, Totary-Jain H. A selective microRNA-based strategy inhibits restenosis while preserving endothelial function. J Clin Invest 2014;124:4102-4114.
8. Jain M, Dhanesha N, Doddapattar P, Chorawala MR, Nayak MK, Cornelissen A, Guo L, Finn AV, Lentz SR, Chauhan AK. Smooth muscle cell-specific fibronectin-EDA mediates phenotypic switching and neointimal hyperplasia. J Clin Invest 2020;130:295-314.
9. Calvert JW, Kevil CG, Spite MR. Regulation and maintenance of vascular tone and patency in cardiovascular health and disease. Int J Vasc Med 2012;2012:396369.
10. Verschuren JJ, Trompet S, Postmus I, Sampietro ML, Heijmans BT, Houwing-Duistermaat JJ, Slagboom PE, Jukema JW. Systematic testing of literature reported genetic variation associated with coronary restenosis: results of the GENDER Study. PLoS One 2012;7:e42401.
11. Yang J, Zeng Y, Zhang C, Chen YX, Yang Z, Li Y, Leng X, Kong D, Wei XQ, Sun HF, Song CX. The prevention of restenosis in vivo with a VEGF gene and paclitaxel co-eluting stent. Biomaterials 2013;34:1635-1643.
12. Chang HK, Kim PH, Kim DW, Cho HM, Jeong MJ, Kim DH, Joung YK, Lim KS, Kim HB, Lim HC, Han DK, Hong YJ, Cho JY. Coronary stents with inducible VEGF/HGF-secreting UCB-MSCs reduced restenosis and increased re-endothelialization in a swine model. Exp Mol Med 2018;50:1-14.
13. Santulli G. microRNAs Distinctively Regulate Vascular Smooth Muscle and Endothelial Cells: Functional Implications in Angiogenesis, Atherosclerosis, and In-Stent Restenosis. Adv Exp Med Biol 2015;887:53-77.
14. Shin M, Beane TJ, Quillien A, Male I, Zhu LJ, Lawson ND. Vegfa signals through ERK to promote angiogenesis, but not artery differentiation. Development 2016;143:3796-3805.
15. Liu D, Song J, Ji X, Liu Z, Cong M, Hu B. Association of Genetic Polymorphisms on VEGFA and VEGFR2 With Risk of Coronary Heart Disease. Medicine (Baltimore) 2016;95:e3413.
16. Inoue M, Itoh H, Tanaka T, Chun TH, Doi K, Fukunaga Y, Sawada N, Yamshita J, Masatsugu K, Saito T, Sakaguchi S, Sone M, Yamahara Ki, Yurugi T, Nakao K. Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and endothelial cells through activation of peroxisome proliferator-activated receptor-gamma. Arterioscler Thromb Vasc Biol 2001;21:560-566.
17. Inoue T, Croce K, Morooka T, Sakuma M, Node K, Simon DI. Vascular inflammation and repair: implications for re-endothelialization, restenosis, and stent thrombosis. JACC Cardiovasc Interv 2011;4:1057-1066.
18. Bradshaw AC, Baker AH. Gene therapy for cardiovascular disease: perspectives and potential. Vascul Pharmacol 2013;58:174-181.
19. Osadnik T, Lekston A, Bujak K, Strzelczyk JK, Poloński L, Gąsior M. The Relationship between VEGFA and TGFB1 Polymorphisms and Target Lesion Revascularization after Elective Percutaneous Coronary Intervention. Dis Markers 2017;2017:8165219.
20. Li L, Pan Y, Dai L, Liu B, Zhang D. Association of Genetic Polymorphisms on Vascular Endothelial Growth Factor and its Receptor Genes with Susceptibility to Coronary Heart Disease. Med Sci Monit 2016;22:31-40.
21. Bagyura Z, Kiss L, Hirschberg K, Berta B, Széplaki G, Lux Á, Szelid Z, Soós P, Merkely B. Association between VEGF Gene Polymorphisms and In-Stent Restenosis after Coronary Intervention Treated with Bare Metal Stent. Dis Markers 2017;2017:9548612.
22. Osadnik T, Strzelczyk JK, Reguła R, Bujak K, Fronczek M, Gonera M, Gawlita M, Wasilewski J, Lekston A, Kurek A, Gierlotka M, Trzeciak P, Hawranek M, Ostrowska Z, Wiczkowski A, Poloński L, Gąsior M. The Relationships between Polymorphisms in Genes Encoding the Growth Factors TGF-β1, PDGFB, EGF, bFGF and VEGF-A and the Restenosis Process in Patients with Stable Coronary Artery Disease Treated with Bare Metal Stent. PLoS One 2016;11:e0150500.
23. Ohtani K, Egashira K, Hiasa K, Zhao Q, Kitamoto S, Ishibashi M, Usui M, Inoue S, Yonemitsu Y, Sueishi K, Sata M, Shibuya M, Sunagawa K. Blockade of vascular endothelial growth factor suppresses experimental restenosis after intraluminal injury by inhibiting recruitment of monocyte lineage cells. Circulation 2004;110:2444-2452.
24. Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE. Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine 2000;12:1232-1235.
25. Yang B, Cross DF, Ollerenshaw M, Millward BA, Demaine AG. Polymorphisms of the vascular endothelial growth factor and susceptibility to diabetic microvascular complications in patients with type 1 diabetes mellitus. J Diabetes Complications 2003;17:1-6.
26. Jain L, Vargo CA, Danesi R, Sissung TM, Price DK, Venzon D, Venitz J, Figg WD. The role of vascular endothelial growth factor SNPs as predictive and prognostic markers for major solid tumors. Mol Cancer Ther 2009;8:2496-2508.
27. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006;290:L209-221.
28. Bhanoori M, Arvind Babu K, Pavankumar Reddy NG, Lakshmi Rao K, Zondervan K, Deenadayal M, Kennedy S, Shivaji S. The vascular endothelial growth factor (VEGF) +405G>C 5'-untranslated region polymorphism and increased risk of endometriosis in South Indian women: a case control study. Hum Reprod 2005;20:1844-1849.
29. Brogan IJ, Khan N, Isaac K, Hutchinson JA, Pravica V, Hutchinson IV. Novel polymorphisms in the promoter and 5' UTR regions of the human vascular endothelial growth factor gene. Hum Immunol 1999;60:1245-1249.
30. Kuntz RE, Baim DS. Defining coronary restenosis. Newer clinical and angiographic paradigms. Circulation 1993;88:1310-1323.
31. Mehran R, Dangas G, Abizaid AS, Mintz GS, Lansky AJ, Satler LF, Pichard AD, Kent KM, Stone GW, Leon MB. Angiographic patterns of in-stent restenosis: classification and implications for long-term outcome. Circulation 1999;100:1872-1878.
32. Dangas GD, Claessen BE, Caixeta A, Sanidas EA, Mintz GS, Mehran R. In-stent restenosis in the drug-eluting stent era. J Am Coll Cardiol 2010;56:1897-1907.
33. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010;33 Suppl 1(Suppl 1):S62-69.
34. Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, Kitzmiller J, Knowler WC, Lebovitz H, Lernmark A, Nathan D, Palmer J, Rizza R, Saudek C, Shaw J, Steffes M, Stern M, Tuomilehto J, Zimmet P; Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 2003;26:3160-3167.
35. Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract 2014;2014:943162.
36. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C; American Heart Association; National Heart, Lung, and Blood Institute. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004;109:433-438.
37. Alberti KG, Zimmet P, Shaw J. Metabolic syndrome--a new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006;23:469-480.
38. Nesto RW. The relation of insulin resistance syndromes to risk of cardiovascular disease. Rev Cardiovasc Med 2003;4 Suppl 6:S11-18.
39. Grundy SM, Cleeman JI, Merz CN, Brewer HB Jr, Clark LT, Hunninghake DB, Pasternak RC, Smith SC Jr, Stone NJ; Coordinating Committee of the National Cholesterol Education Program. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J Am Coll Cardiol 2004;44:720-732.
40. Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, Tietz AB, Kirchmair R, Silver M, Curry C, Wecker A, Yoon YS, Heidenreich R, Hanley A, Kearney M, Tio FO, Kuenzler P, Isner JM, Losordo DW. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation 2004;110:36-45.
41. Bleda S, De Haro J, Varela C, Esparza L, De Maturana IL, Acin F. Impact of VEGF polymorphisms on the severity of peripheral artery disease in diabetic patients. Growth Factors 2012;30:277-282.
42. Nasibullin TR, Sadikova RI, Timasheva IaR, Tuktarova IA, Erdman VV, Khusainova LN, Nikolaeva IE, Mustafina OE. [Association between inflanummatory gene polymorphisms and the risk of myocardial infarction]. Genetika 2014;50:236-242.
43. Keshavarzi F, Shahrakipoor M, Teimoori B, Yaghmaei M, Narooei-Nejad M, Rasooli A, Salimi S. Association of the placental VEGF promoter polymorphisms and VEGF mRNA expression with preeclampsia. Clin Exp Hypertens 2019;41:274-279.
44. Keshavarzi F, Salimi S, Mohammadpour-Gharehbagh A, Teimoori B, Yazdi A, Farajian-Mashhadi F, Yaghmaei M, Mokhtari M. The -2549 insertion/deletion polymorphism of VEGF gene associated with uterine leiomyoma susceptibility in women from Southeastern Iran. Ginekol Pol 2017;88:115-119.
45. Kapahi R, Manjari M, Uppal MS, Singh NR, Sambyal V, Guleria K. Association of -2549 insertion/deletion polymorphism of vascular endothelial growth factor with breast cancer in North Indian patients. Genet Test Mol Biomarkers 2013;17:242-248.
46. Shukla M, Gupta R, Pandey V, Rochette J, Dhandapany PS, Tiwari PK, Amrathlal RS. VEGFA Promoter Polymorphisms rs699947 and rs35569394 Are Associated With the Risk of Anterior Cruciate Ligament Ruptures Among Indian Athletes: A Cross-sectional Study. Orthop J Sports Med 2020;8:2325967120964472.
47. Kibos A, Campeanu A, Tintoiu I. Pathophysiology of coronary artery in-stent restenosis. Acute Card Care 2007;9:111-119.
48. Buraczynska M, Ksiazek P, Baranowicz-Gaszczyk I, Jozwiak L. Association of the VEGF gene polymorphism with diabetic retinopathy in type 2 diabetes patients. Nephrol Dial Transplant 2007;22:827-832.
49. Gala-Błądzińska A, Czech J, Braun M, Skrzypa M, Gargasz K, Mazur A, Zawlik I. Association of 18bp insertion/deletion polymorphism, at −2549 position of VEGF gene, with diabetic vascular complications in type 2 diabetes mellitus. Adv Med Sci 2019;64:137-143.
50. Schulz S, Sibbing D, Braun S, Morath T, Mehilli J, Massberg S, Byrne RA, Schömig A, Kastrati A. Platelet response to clopidogrel and restenosis in patients treated predominantly with drug-eluting stents. Am Heart J 2010;160:355-3561.
51. Gurbel PA, Cummings CC, Bell CR, Alford AB, Meister AF, Serebruany VL; Plavix Reduction Of New Thrombus Occurrence (PRONTO) trial. Onset and extent of platelet inhibition by clopidogrel loading in patients undergoing elective coronary stenting: the Plavix Reduction Of New Thrombus Occurrence (PRONTO) trial. Am Heart J 2003;145:239-247.
52. Pekdemir H, Cin VG, Camsari A, Cicek D, Akkus MN, Doven O, Parmaksiz T. A comparison of 1-month and 6-month clopidogrel therapy on clinical and angiographic outcome after stent implantation. Heart Vessels 2003;18:123-129.
53. Wu X, Zhao Y, Tang C, Yin T, Du R, Tian J, Huang J, Gregersen H, Wang G. Re-Endothelialization Study on Endovascular Stents Seeded by Endothelial Cells through Up- or Downregulation of VEGF. ACS Appl Mater Interfaces 2016;8:7578-7589.
54. Chang HK, Kim PH, Kim DW, Cho HM, Jeong MJ, Kim DH, Joung YK, Lim KS, Kim HB, Lim HC, Han DK, Hong YJ, Cho JY. Coronary stents with inducible VEGF/HGF-secreting UCB-MSCs reduced restenosis and increased re-endothelialization in a swine model. Exp Mol Med 2018;50:1-14.
2. Gaziano TA, Opie LH, Weinstein MC. Cardiovascular disease prevention with a multidrug regimen in the developing world: a cost-effectiveness analysis. Lancet 2006;368:679-686.
3. Nakamura N, Torii S, Tsuchiya H, Nakano A, Oikawa Y, Yajima J, Nakamura S, Nakano M, Masuda N, Ohta H, Yumoto K, Natsumeda M, Ijichi T, Ikari Y, Nakazawa G. Formation of Calcified Nodule as a Cause of Early In-Stent Restenosis in Patients Undergoing Dialysis. J Am Heart Assoc 2020;9:e016595.
4. Buccheri D, Piraino D, Andolina G, Cortese B. Understanding and managing in-stent restenosis: a review of clinical data, from pathogenesis to treatment. J Thorac Dis 2016;8:E1150-E1162.
5. Alfonso F, Byrne RA, Rivero F, Kastrati A. Current treatment of in-stent restenosis. J Am Coll Cardiol 2014;63:2659-2673.
6. Kokkinidis DG, Waldo SW, Armstrong EJ. Treatment of coronary artery in-stent restenosis. Expert Rev Cardiovasc Ther 2017;15:191-202.
7. Santulli G, Wronska A, Uryu K, Diacovo TG, Gao M, Marx SO, Kitajewski J, Chilton JM, Akat KM, Tuschl T, Marks AR, Totary-Jain H. A selective microRNA-based strategy inhibits restenosis while preserving endothelial function. J Clin Invest 2014;124:4102-4114.
8. Jain M, Dhanesha N, Doddapattar P, Chorawala MR, Nayak MK, Cornelissen A, Guo L, Finn AV, Lentz SR, Chauhan AK. Smooth muscle cell-specific fibronectin-EDA mediates phenotypic switching and neointimal hyperplasia. J Clin Invest 2020;130:295-314.
9. Calvert JW, Kevil CG, Spite MR. Regulation and maintenance of vascular tone and patency in cardiovascular health and disease. Int J Vasc Med 2012;2012:396369.
10. Verschuren JJ, Trompet S, Postmus I, Sampietro ML, Heijmans BT, Houwing-Duistermaat JJ, Slagboom PE, Jukema JW. Systematic testing of literature reported genetic variation associated with coronary restenosis: results of the GENDER Study. PLoS One 2012;7:e42401.
11. Yang J, Zeng Y, Zhang C, Chen YX, Yang Z, Li Y, Leng X, Kong D, Wei XQ, Sun HF, Song CX. The prevention of restenosis in vivo with a VEGF gene and paclitaxel co-eluting stent. Biomaterials 2013;34:1635-1643.
12. Chang HK, Kim PH, Kim DW, Cho HM, Jeong MJ, Kim DH, Joung YK, Lim KS, Kim HB, Lim HC, Han DK, Hong YJ, Cho JY. Coronary stents with inducible VEGF/HGF-secreting UCB-MSCs reduced restenosis and increased re-endothelialization in a swine model. Exp Mol Med 2018;50:1-14.
13. Santulli G. microRNAs Distinctively Regulate Vascular Smooth Muscle and Endothelial Cells: Functional Implications in Angiogenesis, Atherosclerosis, and In-Stent Restenosis. Adv Exp Med Biol 2015;887:53-77.
14. Shin M, Beane TJ, Quillien A, Male I, Zhu LJ, Lawson ND. Vegfa signals through ERK to promote angiogenesis, but not artery differentiation. Development 2016;143:3796-3805.
15. Liu D, Song J, Ji X, Liu Z, Cong M, Hu B. Association of Genetic Polymorphisms on VEGFA and VEGFR2 With Risk of Coronary Heart Disease. Medicine (Baltimore) 2016;95:e3413.
16. Inoue M, Itoh H, Tanaka T, Chun TH, Doi K, Fukunaga Y, Sawada N, Yamshita J, Masatsugu K, Saito T, Sakaguchi S, Sone M, Yamahara Ki, Yurugi T, Nakao K. Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and endothelial cells through activation of peroxisome proliferator-activated receptor-gamma. Arterioscler Thromb Vasc Biol 2001;21:560-566.
17. Inoue T, Croce K, Morooka T, Sakuma M, Node K, Simon DI. Vascular inflammation and repair: implications for re-endothelialization, restenosis, and stent thrombosis. JACC Cardiovasc Interv 2011;4:1057-1066.
18. Bradshaw AC, Baker AH. Gene therapy for cardiovascular disease: perspectives and potential. Vascul Pharmacol 2013;58:174-181.
19. Osadnik T, Lekston A, Bujak K, Strzelczyk JK, Poloński L, Gąsior M. The Relationship between VEGFA and TGFB1 Polymorphisms and Target Lesion Revascularization after Elective Percutaneous Coronary Intervention. Dis Markers 2017;2017:8165219.
20. Li L, Pan Y, Dai L, Liu B, Zhang D. Association of Genetic Polymorphisms on Vascular Endothelial Growth Factor and its Receptor Genes with Susceptibility to Coronary Heart Disease. Med Sci Monit 2016;22:31-40.
21. Bagyura Z, Kiss L, Hirschberg K, Berta B, Széplaki G, Lux Á, Szelid Z, Soós P, Merkely B. Association between VEGF Gene Polymorphisms and In-Stent Restenosis after Coronary Intervention Treated with Bare Metal Stent. Dis Markers 2017;2017:9548612.
22. Osadnik T, Strzelczyk JK, Reguła R, Bujak K, Fronczek M, Gonera M, Gawlita M, Wasilewski J, Lekston A, Kurek A, Gierlotka M, Trzeciak P, Hawranek M, Ostrowska Z, Wiczkowski A, Poloński L, Gąsior M. The Relationships between Polymorphisms in Genes Encoding the Growth Factors TGF-β1, PDGFB, EGF, bFGF and VEGF-A and the Restenosis Process in Patients with Stable Coronary Artery Disease Treated with Bare Metal Stent. PLoS One 2016;11:e0150500.
23. Ohtani K, Egashira K, Hiasa K, Zhao Q, Kitamoto S, Ishibashi M, Usui M, Inoue S, Yonemitsu Y, Sueishi K, Sata M, Shibuya M, Sunagawa K. Blockade of vascular endothelial growth factor suppresses experimental restenosis after intraluminal injury by inhibiting recruitment of monocyte lineage cells. Circulation 2004;110:2444-2452.
24. Watson CJ, Webb NJ, Bottomley MJ, Brenchley PE. Identification of polymorphisms within the vascular endothelial growth factor (VEGF) gene: correlation with variation in VEGF protein production. Cytokine 2000;12:1232-1235.
25. Yang B, Cross DF, Ollerenshaw M, Millward BA, Demaine AG. Polymorphisms of the vascular endothelial growth factor and susceptibility to diabetic microvascular complications in patients with type 1 diabetes mellitus. J Diabetes Complications 2003;17:1-6.
26. Jain L, Vargo CA, Danesi R, Sissung TM, Price DK, Venzon D, Venitz J, Figg WD. The role of vascular endothelial growth factor SNPs as predictive and prognostic markers for major solid tumors. Mol Cancer Ther 2009;8:2496-2508.
27. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006;290:L209-221.
28. Bhanoori M, Arvind Babu K, Pavankumar Reddy NG, Lakshmi Rao K, Zondervan K, Deenadayal M, Kennedy S, Shivaji S. The vascular endothelial growth factor (VEGF) +405G>C 5'-untranslated region polymorphism and increased risk of endometriosis in South Indian women: a case control study. Hum Reprod 2005;20:1844-1849.
29. Brogan IJ, Khan N, Isaac K, Hutchinson JA, Pravica V, Hutchinson IV. Novel polymorphisms in the promoter and 5' UTR regions of the human vascular endothelial growth factor gene. Hum Immunol 1999;60:1245-1249.
30. Kuntz RE, Baim DS. Defining coronary restenosis. Newer clinical and angiographic paradigms. Circulation 1993;88:1310-1323.
31. Mehran R, Dangas G, Abizaid AS, Mintz GS, Lansky AJ, Satler LF, Pichard AD, Kent KM, Stone GW, Leon MB. Angiographic patterns of in-stent restenosis: classification and implications for long-term outcome. Circulation 1999;100:1872-1878.
32. Dangas GD, Claessen BE, Caixeta A, Sanidas EA, Mintz GS, Mehran R. In-stent restenosis in the drug-eluting stent era. J Am Coll Cardiol 2010;56:1897-1907.
33. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010;33 Suppl 1(Suppl 1):S62-69.
34. Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, Kitzmiller J, Knowler WC, Lebovitz H, Lernmark A, Nathan D, Palmer J, Rizza R, Saudek C, Shaw J, Steffes M, Stern M, Tuomilehto J, Zimmet P; Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 2003;26:3160-3167.
35. Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract 2014;2014:943162.
36. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C; American Heart Association; National Heart, Lung, and Blood Institute. Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004;109:433-438.
37. Alberti KG, Zimmet P, Shaw J. Metabolic syndrome--a new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006;23:469-480.
38. Nesto RW. The relation of insulin resistance syndromes to risk of cardiovascular disease. Rev Cardiovasc Med 2003;4 Suppl 6:S11-18.
39. Grundy SM, Cleeman JI, Merz CN, Brewer HB Jr, Clark LT, Hunninghake DB, Pasternak RC, Smith SC Jr, Stone NJ; Coordinating Committee of the National Cholesterol Education Program. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J Am Coll Cardiol 2004;44:720-732.
40. Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, Tietz AB, Kirchmair R, Silver M, Curry C, Wecker A, Yoon YS, Heidenreich R, Hanley A, Kearney M, Tio FO, Kuenzler P, Isner JM, Losordo DW. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation 2004;110:36-45.
41. Bleda S, De Haro J, Varela C, Esparza L, De Maturana IL, Acin F. Impact of VEGF polymorphisms on the severity of peripheral artery disease in diabetic patients. Growth Factors 2012;30:277-282.
42. Nasibullin TR, Sadikova RI, Timasheva IaR, Tuktarova IA, Erdman VV, Khusainova LN, Nikolaeva IE, Mustafina OE. [Association between inflanummatory gene polymorphisms and the risk of myocardial infarction]. Genetika 2014;50:236-242.
43. Keshavarzi F, Shahrakipoor M, Teimoori B, Yaghmaei M, Narooei-Nejad M, Rasooli A, Salimi S. Association of the placental VEGF promoter polymorphisms and VEGF mRNA expression with preeclampsia. Clin Exp Hypertens 2019;41:274-279.
44. Keshavarzi F, Salimi S, Mohammadpour-Gharehbagh A, Teimoori B, Yazdi A, Farajian-Mashhadi F, Yaghmaei M, Mokhtari M. The -2549 insertion/deletion polymorphism of VEGF gene associated with uterine leiomyoma susceptibility in women from Southeastern Iran. Ginekol Pol 2017;88:115-119.
45. Kapahi R, Manjari M, Uppal MS, Singh NR, Sambyal V, Guleria K. Association of -2549 insertion/deletion polymorphism of vascular endothelial growth factor with breast cancer in North Indian patients. Genet Test Mol Biomarkers 2013;17:242-248.
46. Shukla M, Gupta R, Pandey V, Rochette J, Dhandapany PS, Tiwari PK, Amrathlal RS. VEGFA Promoter Polymorphisms rs699947 and rs35569394 Are Associated With the Risk of Anterior Cruciate Ligament Ruptures Among Indian Athletes: A Cross-sectional Study. Orthop J Sports Med 2020;8:2325967120964472.
47. Kibos A, Campeanu A, Tintoiu I. Pathophysiology of coronary artery in-stent restenosis. Acute Card Care 2007;9:111-119.
48. Buraczynska M, Ksiazek P, Baranowicz-Gaszczyk I, Jozwiak L. Association of the VEGF gene polymorphism with diabetic retinopathy in type 2 diabetes patients. Nephrol Dial Transplant 2007;22:827-832.
49. Gala-Błądzińska A, Czech J, Braun M, Skrzypa M, Gargasz K, Mazur A, Zawlik I. Association of 18bp insertion/deletion polymorphism, at −2549 position of VEGF gene, with diabetic vascular complications in type 2 diabetes mellitus. Adv Med Sci 2019;64:137-143.
50. Schulz S, Sibbing D, Braun S, Morath T, Mehilli J, Massberg S, Byrne RA, Schömig A, Kastrati A. Platelet response to clopidogrel and restenosis in patients treated predominantly with drug-eluting stents. Am Heart J 2010;160:355-3561.
51. Gurbel PA, Cummings CC, Bell CR, Alford AB, Meister AF, Serebruany VL; Plavix Reduction Of New Thrombus Occurrence (PRONTO) trial. Onset and extent of platelet inhibition by clopidogrel loading in patients undergoing elective coronary stenting: the Plavix Reduction Of New Thrombus Occurrence (PRONTO) trial. Am Heart J 2003;145:239-247.
52. Pekdemir H, Cin VG, Camsari A, Cicek D, Akkus MN, Doven O, Parmaksiz T. A comparison of 1-month and 6-month clopidogrel therapy on clinical and angiographic outcome after stent implantation. Heart Vessels 2003;18:123-129.
53. Wu X, Zhao Y, Tang C, Yin T, Du R, Tian J, Huang J, Gregersen H, Wang G. Re-Endothelialization Study on Endovascular Stents Seeded by Endothelial Cells through Up- or Downregulation of VEGF. ACS Appl Mater Interfaces 2016;8:7578-7589.
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| Files | ||
| Issue | Vol 17 No 3 (2022): J Teh Univ Heart Ctr | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jthc.v17i3.10844 | |
| Keywords | ||
| Coronary restenosis Drug-eluting stent Gene variant VEGF | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Asgarbeik S, Vahidi A, Hasanzad M, Asadi M, M.Amoli M. Vascular Endothelial Growth Factor Genetic Variant is Associated with In-Stent Restenosis after Percutaneous Coronary Intervention. J Tehran Heart Cent. 2022;17(3):119-126.
