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Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 2568569, 12 pages
https://doi.org/10.1155/2018/2568569
Review Article

Vascular Endothelial Dysfunction in Inflammatory Bowel Diseases: Pharmacological and Nonpharmacological Targets

1Department of Precision Medicine, University of Campania “Luigi Vanvitelli”, Via Pansini 5, 80131 Naples, Italy
2Department of Medicine and Surgery, University of Salerno, Via Salvador Allende, 84081 Baronissi, Salerno, Italy

Correspondence should be addressed to Alessandro Federico; ti.ainapmacinu@ociredef.ordnassela

Received 22 December 2017; Accepted 14 March 2018; Published 12 April 2018

Academic Editor: Saeid Golbidi

Copyright © 2018 Antonietta Gerarda Gravina et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Zanoli, S. Rastelli, G. Inserra, and P. Castellino, “Arterial structure and function in inflammatory bowel disease,” World Journal of Gastroenterology, vol. 21, no. 40, pp. 11304–11311, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Tian, Z. Wang, and J. Zhang, “Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies,” Oxidative Medicine and Cellular Longevity, vol. 2017, 18 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Corridoni, K. O. Arseneau, and F. Cominelli, “Inflammatory bowel disease,” Immunology Letters, vol. 161, no. 2, pp. 231–235, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Levy, Y. Rizwan, L. Thibault et al., “Altered lipid profile, lipoprotein composition, and oxidant and antioxidant status in pediatric Crohn disease,” The American Journal of Clinical Nutrition, vol. 71, no. 3, pp. 807–815, 2000. View at Publisher · View at Google Scholar
  5. A. J. Yarur, A. R. Deshpande, D. M. Pechman, L. Tamariz, M. T. Abreu, and D. A. Sussman, “Inflammatory bowel disease is associated with an increased incidence of cardiovascular events,” The American Journal of Gastroenterology, vol. 106, no. 4, pp. 741–747, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. S. D. Dorn and R. S. Sandler, “Inflammatory bowel disease is not a risk factor for cardiovascular disease mortality: results from a systematic review and meta-analysis,” The American Journal of Gastroenterology, vol. 102, no. 3, pp. 662–667, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. A. D. Booth, S. Wallace, C. M. McEniery et al., “Inflammation and arterial stiffness in systemic vasculitis: a model of vascular inflammation,” Arthritis and Rheumatism, vol. 50, no. 2, pp. 581–588, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. K. M. Mäki-Petäjä, F. C. Hall, A. D. Booth et al., “Rheumatoid arthritis is associated with increased aortic pulsewave velocity, which is reduced by anti-tumor necrosis factor-alpha therapy,” Circulation, vol. 114, no. 11, pp. 1185–1192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. J. Roman, R. B. Devereux, J. E. Schwartz et al., “Arterial stiffness in chronic inflammatory diseases,” Hypertension, vol. 46, no. 1, pp. 194–199, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Mancia, R. Fagard, K. Narkiewicz et al., “2013 Practice guidelines for the management of arterial hypertension of the European Society of Hypertension (ESH) and the European Society of Cardiology (ESC),” Journal of Hypertension, vol. 31, no. 10, pp. 1925–1938, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Laurent, J. Cockcroft, L. Van Bortel et al., “Expert consensus document on arterial stiffness: methodological issues and clinical applications,” European Heart Journal, vol. 27, no. 21, pp. 2588–2605, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Pietri, G. Vyssoulis, C. Vlachopoulos et al., “Relationship between low-grade inflammation and arterial stiffness in patients with essential hypertension,” Journal of Hypertension, vol. 24, no. 11, pp. 2231–2238, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Yasmin, C. McEniery, S. Wallace, I. Mackenzie, J. Cockcroft, and I. Wilkinson, “C-reactive protein is associated with arterial stiffness in apparently healthy individuals,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 5, pp. 969–974, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. S. McDonnell, M. Morgan, and C. Lynch, “Role of matrix metalloproteinases in normal and disease processes,” Biochemical Society Transactions, vol. 27, no. 4, pp. 734–740, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Zanoli, M. Cannavò, S. Rastelli et al., “Arterial stiffness is increased in patients with inflammatory bowel disease,” Journal of Hypertension, vol. 30, no. 9, pp. 1775–1781, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. R. A. Akdoğan, M. E. Durakoğlugil, S. A. Kocaman et al., “Increased pulse wave velocity and carotid intima-media thickness in patients with ulcerative colitis,” Digestive Diseases and Sciences, vol. 58, no. 8, pp. 2293–2300, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Korkmaz, F. Sahin, S. H. Ipekci, T. Temel, and L. Kebapcilar, “Increased pulse wave velocity and relationship with inflammation, insulin, and insulin resistance in inflammatory bowel disease,” European Journal of Gastroenterology & Hepatology, vol. 26, no. 7, pp. 725–732, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Aytac, D. Buyuktas, B. Baysal et al., “Visual evoked potentials and pulse wave velocity in inflammatory bowel disease,” The Turkish Journal of Gastroenterology, vol. 26, no. 1, pp. 15–19, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Zanoli, S. Rastelli, G. Inserra et al., “Increased arterial stiffness in inflammatory bowel diseases is dependent upon inflammation and reduced by immunomodulatory drugs,” Atherosclerosis, vol. 234, no. 2, pp. 346–351, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Cibor, R. Domagala-Rodacka, T. Rodacki, A. Jurczyszyn, T. Mach, and D. Owczarek, “Endothelial dysfunction in inflammatory bowel diseases: pathogenesis, assessment and implications,” World Journal of Gastroenterology, vol. 22, no. 3, pp. 1067–1077, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Deanfield, A. Donald, C. Ferri et al., “Endothelial function and dysfunction. Part I: methodological issues for assessment in the different vascular beds,” Journal of Hypertension, vol. 23, no. 1, pp. 7–17, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Steyers III and F. Miller Jr, “Endothelial dysfunction in chronic inflammatory diseases,” International Journal of Molecular Sciences, vol. 15, no. 7, pp. 11324–11349, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. Ciccone, E. Bilianou, A. Balbarini et al., “Task force on,” Journal of Cardiovascular Medicine, vol. 14, no. 10, pp. 757–766, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Lerman and A. M. Zeiher, “Endothelial function: cardiac events,” Circulation, vol. 111, no. 3, pp. 363–368, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Schinzari, A. Armuzzi, B. De Pascalis et al., “Tumor necrosis factor-α antagonism improves endothelial dysfunction in patients with Crohn’s disease,” Clinical Pharmacology & Therapeutics, vol. 83, no. 1, pp. 70–76, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Garolla, R. D’Incà, D. Checchin et al., “Reduced endothelial progenitor cell number and function in inflammatory bowel disease: a possible link to the pathogenesis,” The American Journal of Gastroenterology, vol. 104, no. 10, pp. 2500–2507, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Scaldaferri, S. Lancellotti, M. Pizzoferrato, and R. De Cristofaro, “Haemostatic system in inflammatory bowel diseases: new players in gut inflammation,” World Journal of Gastroenterology, vol. 17, no. 5, pp. 594–608, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Deban, C. Correale, S. Vetrano, A. Malesci, and S. Danese, “Multiple pathogenic roles of microvasculature in inflammatory bowel disease: a jack of all trades,” The American Journal of Pathology, vol. 172, no. 6, pp. 1457–1466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. I. F. Charo and R. M. Ransohoff, “The many roles of chemokines and chemokine receptors in inflammation,” The New England Journal of Medicine, vol. 354, no. 6, pp. 610–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. S. D’Alessio, C. Tacconi, C. Fiocchi, and S. Danese, “Advances in therapeutic interventions targeting the vascular and lymphatic endothelium in inflammatory bowel disease,” Current Opinion in Gastroenterology, vol. 29, no. 6, pp. 608–613, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. O. A. Hatoum, H. Miura, and D. G. Binion, “The vascular contribution in the pathogenesis of inflammatory bowel disease,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 285, no. 5, pp. H1791–H1796, 2003. View at Publisher · View at Google Scholar
  32. S. Danese, S. Semeraro, M. Marini et al., “Adhesion molecules in inflammatory bowel disease: therapeutic implications for gut inflammation,” Digestive and Liver Disease, vol. 37, no. 11, pp. 811–818, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Danese, “Role of the vascular and lymphatic endothelium in the pathogenesis of inflammatory bowel disease: ‘brothers in arms’,” Gut, vol. 60, no. 7, pp. 998–1008, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Briskin, D. Winsor-Hines, A. Shyjan et al., “Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue,” The American Journal of Pathology, vol. 151, no. 1, pp. 97–110, 1997. View at Google Scholar
  35. V. Lelio Burgio, S. Fais, M. Boirivant, A. Perrone, and F. Pallone, “Peripheral monocyte and naive T-cell recruitment and activation in Crohn’s disease,” Gastroenterology, vol. 109, no. 4, pp. 1029–1038, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. W. E. Cromer, J. M. Mathis, D. N. Granger, G. V. Chaitanya, and J. S. Alexander, “Role of the endothelium in inflammatory bowel diseases,” World Journal of Gastroenterology, vol. 17, no. 5, pp. 578–593, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. C. H. Wang, S. H. Li, R. D. Weisel et al., “C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle,” Circulation, vol. 107, no. 13, pp. 1783–1790, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Pasceri, J. T. Willerson, and E. T. H. Yeh, “Direct proinflammatory effect of C-reactive protein on human endothelial cells,” Circulation, vol. 102, no. 18, pp. 2165–2168, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. S. K. Venugopal, S. Devaraj, and I. Jialal, “Macrophage conditioned medium induces the expression of C-reactive protein in human aortic endothelial cells,” The American Journal of Pathology, vol. 166, no. 4, pp. 1265–1271, 2005. View at Publisher · View at Google Scholar
  40. B. R. Clapp, G. M. Hirschfield, C. Storry et al., “Inflammation and endothelial function: direct vascular effects of human C-reactive protein on nitric oxide bioavailability,” Circulation, vol. 111, no. 12, pp. 1530–1536, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Roifman, Y. C. Sun, J. P. Fedwick et al., “Evidence of endothelial dysfunction in patients with inflammatory bowel disease,” Clinical Gastroenterology and Hepatology, vol. 7, no. 2, pp. 175–182, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Danese, F. Scaldaferri, S. Vetrano et al., “Critical role of the CD40 CD40-ligand pathway in regulating mucosal inflammation-driven angiogenesis in inflammatory bowel disease,” Gut, vol. 56, no. 9, pp. 1248–1256, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. H. Liu, Y. Ding, C. C. Gao, L. S. Li, Y. X. Wang, and J. D. Xu, “Functional macrophages and gastrointestinal disorders,” World Journal of Gastroenterology, vol. 24, no. 11, pp. 1181–1195, 2018. View at Publisher · View at Google Scholar
  44. I. Kullo, J. Seward, K. Bailey et al., “C-reactive protein is related to arterial wave reflection and stiffness in asymptomatic subjects from the community,” American Journal of Hypertension, vol. 18, no. 8, pp. 1123–1129, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. J. A. Vita, J. F. Keaney Jr, M. G. Larson et al., “Brachial artery vasodilator function and systemic inflammation in the Framingham Offspring Study,” Circulation, vol. 110, no. 23, pp. 3604–3609, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Floege and M. Ketteler, “Vascular calcification in patients with endstage renal disease,” Nephrology, Dialysis, Transplantation, vol. 19, Supplement_5, pp. V59–v66, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. I. E. Koutroubakis, G. Tsiolakidou, K. Karmiris, and E. A. Kouroumalis, “Role of angiogenesis in inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 12, no. 6, pp. 515–523, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Bielli, M. G. Scioli, D. Mazzaglia, E. Doldo, and A. Orlandi, “Antioxidants and vascular health,” Life Sciences, vol. 143, pp. 209–216, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Horowitz, D. G. Binion, V. M. Nelson et al., “Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 292, no. 5, pp. G1323–G1336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Magro, J. B. Soares, and D. Fernandes, “Venous thrombosis and prothrombotic factors in inflammatory bowel disease,” World Journal of Gastroenterology, vol. 20, no. 17, pp. 4857–4872, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Sibal, S. C Agarwal, P. D Home, and R. H Boger, “The role of asymmetric dimethylarginine [ADMA] in endothelial dysfunction and cardiovascular disease,” Current Cardiology Reviews, vol. 6, no. 2, pp. 82–90, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. R. H. Boger, R. Maas, F. Schulze, and E. Schwedhelm, “Asymmetric dimethylarginine [ADMA] as a prospective marker of cardiovascular disease and mortality--an update on patient populations with a wide range of cardiovascular risk,” Pharmacological Research, vol. 60, no. 6, pp. 481–487, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Kleinbongard, G. Heusch, and R. Schulz, “TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure,” Pharmacology & Therapeutics, vol. 127, no. 3, pp. 295–314, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Picchi, X. Gao, S. Belmadani et al., “Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome,” Circulation Research, vol. 99, no. 1, pp. 69–77, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. L. Kalinowski and T. Malinski, “Endothelial NADH/NADPH-dependent enzymatic sources of superoxide production: relationship to endothelial dysfunction,” Acta Biochimica Polonica, vol. 51, no. 2, pp. 459–469, 2004. View at Google Scholar
  56. S. Kundu, P. Ghosh, S. Datta, A. Ghosh, S. Chattopadhyay, and M. Chatterjee, “Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis,” Free Radical Research, vol. 46, no. 12, pp. 1482–1489, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. M. S. Wolin, “Interactions of oxidants with vascular signaling systems,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 6, pp. 1430–1442, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Biniecka, A. Kennedy, C. T. Ng et al., “Successful tumour necrosis factor [TNF] blocking therapy suppresses oxidative stress and hypoxia-induced mitochondrial mutagenesis in inflammatory arthritis,” Arthritis Research & Therapy, vol. 13, no. 4, p. R121, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Lancellotti, V. De Filippis, N. Pozzi et al., “Formation of methionine sulfoxide by peroxynitrite at position 1606 of von Willebrand factor inhibits its cleavage by ADAMTS-13: a new prothrombotic mechanism in diseases associated with oxidative stress,” Free Radical Biology & Medicine, vol. 48, no. 3, pp. 446–456, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. M. M. Ciccone, M. Principi, E. Ierardi et al., “Inflammatory bowel disease, liver diseases and endothelial function: is there a linkage?” Journal of Cardiovascular Medicine, vol. 16, no. 1, pp. 11–21, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Desreumaux, G. Huet, F. Zerimech et al., “Acute inflammatory intestinal vascular lesions and in situ abnormalities of the plasminogen activation system in Crohn’s disease,” European Journal of Gastroenterology & Hepatology, vol. 11, no. 10, pp. 1113–1120, 1999. View at Publisher · View at Google Scholar
  62. M. Principi, M. Mastrolonardo, P. Scicchitano et al., “Endothelial function and cardiovascular risk in active inflammatory bowel diseases,” Journal of Crohn’s and Colitis, vol. 7, no. 10, pp. e427–e433, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. E. Theocharidou, T. D. Gossios, T. Griva et al., “Is there an association between inflammatory bowel diseases and carotid intima-media thickness? Preliminary data,” Angiology, vol. 65, no. 6, pp. 543–550, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. S. I. van Leuven, R. Hezemans, J. H. Levels et al., “Enhanced atherogenesis and altered high density lipoprotein in patients with Crohn’s disease,” Journal of Lipid Research, vol. 48, no. 12, pp. 2640–2646, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Papa, A. Santoliquido, S. Danese et al., “Increased carotid intima–media thickness in patients with inflammatory bowel disease,” Alimentary Pharmacology & Therapeutics, vol. 22, no. 9, pp. 839–846, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. N. Dagli, O. K. Poyrazoglu, A. Ferda Dagli et al., “Is inflammatory bowel disease a risk factor for early atherosclerosis?” Angiology, vol. 61, no. 2, pp. 198–204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Maharshak, Y. Arbel, N. M. Bornstein et al., “Inflammatory bowel disease is not associated with increased intimal media thickening,” The American Journal of Gastroenterology, vol. 102, no. 5, pp. 1050–1055, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Broide, A. Schopan, M. Zaretsky, N. A. Kimchi, M. Shapiro, and E. Scapa, “Intima media thickness of the common carotid artery is not significantly higher in Crohn’s disease patients compared to healthy population,” Digestive Diseases and Sciences, vol. 56, no. 1, pp. 197–202, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Di Sabatino, R. Ciccocioppo, E. Armellini et al., “Serum bFGF and VEGF correlate respectively with bowel wall thickness and intramural blood flow in Crohn’s disease,” Inflammatory Bowel Diseases, vol. 10, no. 5, pp. 573–577, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. W. B. Song, Y. H. Lv, Z. S. Zhang et al., “Soluble intercellular adhesion molecule-1, D-lactate and diamine oxidase in patients with inflammatory bowel disease,” World Journal of Gastroenterology, vol. 15, no. 31, pp. 3916–3919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Magro, F. Araujo, P. Pereira, E. Meireles, M. Diniz-Ribeiro, and F. T. Velosom, “Soluble selectins, sICAM, sVCAM, and angiogenic proteins in different activity groups of patients with inflammatory bowel disease,” Digestive Diseases and Sciences, vol. 49, no. 7/8, pp. 1265–1274, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. G. Murdaca, B. M. Colombo, P. Cagnati, R. Gulli, F. Spano, and F. Puppo, “Endothelial dysfunction in rheumatic autoimmune diseases,” Atherosclerosis, vol. 224, no. 2, pp. 309–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Prati, C. Demougeot, X. Guillot, M. Godfrin-Valnet, and D. Wendling, “Endothelial dysfunction in joint disease,” Joint, Bone, Spine, vol. 81, no. 5, pp. 386–391, 2014. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Davignon and P. Ganz, “Role of endothelial dysfunction in atherosclerosis,” Circulation, vol. 109, 23_Supplement_1, pp. III-27–III-32, 2004. View at Publisher · View at Google Scholar
  75. C. Rungoe, S. Basit, M. F. Ranthe, J. Wohlfahrt, E. Langholz, and T. Jess, “Risk of ischaemic heart disease in patients with inflammatory bowel disease: a nationwide Danish cohort study,” Gut, vol. 62, no. 5, pp. 689–694, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. T. Jess, M. Gamborg, P. Munkholm, and T. I. A. Sørensen, “Overall and causespecific mortality in ulcerative colitis: meta-analysis of population based inception cohort studies,” The American Journal of Gastroenterology, vol. 102, no. 3, pp. 609–617, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Bewtra, L. M. Kaiser, T. TenHave, and J. D. Lewis, “Crohn’s disease and ulcerative colitis are associated with elevated standardized mortality ratios: a meta-analysis,” Inflammatory Bowel Diseases, vol. 19, no. 3, pp. 599–613, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Ozturk, A. K. Guler, M. Cakir et al., “Pulse wave velocity, intima media thickness, and flow-mediated dilatation in patients with normotensive normoglycemic inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 21, no. 6, pp. 1314–1320, 2015. View at Publisher · View at Google Scholar · View at Scopus
  79. M. M. Ciccone, V. Miniello, R. Marchioli et al., “Morphological and functional vascular changes induced by childhood obesity,” European Journal of Cardiovascular Prevention and Rehabilitation, vol. 18, no. 6, pp. 831–835, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. Z. Caliskan, N. Keles, H. S. Gokturk et al., “Is activation in inflammatory bowel diseases associated with further impairment of coronary microcirculation?” International Journal of Cardiology, vol. 223, pp. 176–181, 2016. View at Publisher · View at Google Scholar · View at Scopus
  81. O. A. Hatoum and D. G. Binion, “The vasculature and inflammatory bowel disease: contribution to pathogenesis and clinical pathology,” Inflammatory Bowel Diseases, vol. 11, no. 3, pp. 304–313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Kaptoge, S. R. K. Seshasai, P. Gao et al., “Inflammatory cytokines and risk of coronary heart disease: new prospective study and updated metaanalysis,” European Heart Journal, vol. 35, no. 9, pp. 578–589, 2014. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Van Doornum, G. McColl, A. Jenkins, D. J. Green, and I. P. Wicks, “Screening for atherosclerosis in patients with rheumatoid arthritis: comparison of two in vivo tests of vascular function,” Arthritis and Rheumatism, vol. 48, no. 1, pp. 72–80, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. M. M. Ciccone, G. De Pergola, M. T. Porcelli et al., “Increased carotid IMT in overweight and obese women affected by Hashimoto’s thyroiditis: an adiposity and autoimmune linkage?” BMC Cardiovascular Disorders, vol. 10, no. 1, p. 22, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. S. L. Kristensen, O. Ahlehoff, J. Lindhardsen et al., “Prognosis after first-time myocardial infarction in patients with inflammatory bowel disease according to disease activity: nationwide cohort study,” Circulation Cardiovascular Quality and Outcomes, vol. 7, no. 6, pp. 857–862, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Principi, L. Montenegro, G. Losurdo et al., “Endothelial function and cardiovascular risk in patients with inflammatory bowel disease in remission phase,” Scandinavian Journal of Gastroenterology, vol. 51, no. 2, pp. 253–255, 2015. View at Publisher · View at Google Scholar · View at Scopus
  87. F. M. Ruemmele, G. Veres, K. L. Kolho et al., “Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn’s disease,” Journal of Crohn’s & Colitis, vol. 8, no. 10, pp. 1179–1207, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Singh, H. Singh, E. V. Loftus Jr, and D. S. Pardi, “Risk of cerebrovascular accidents and ischemic heart disease in patients with inflammatory bowel disease: a systematic review and meta-analysis,” Clinical Gastroenterology and Hepatology, vol. 12, no. 3, pp. 382–393.e1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Fumery, C. Xiaocang, L. Dauchet, C. Gower-Rousseau, L. Peyrin-Biroulet, and J. F. Colombel, “Thromboembolic events and cardiovascular mortality in inflammatory bowel diseases: a meta-analysis of observational studies,” Journal of Crohn’s & Colitis, vol. 8, no. 6, pp. 469–479, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. D. Szpak, A. Grochowalski, R. Chrząszcz, E. Florek, W. Jawień, and A. Undas, “Tobacco smoke exposure and endothelial dysfunction in patients with advanced coronary artery disease,” Polish Archives of Internal Medicine, vol. 123, no. 9, pp. 474–481, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Ray and M. V. Autieri, “Regulation of pro- and anti-atherogenic cytokines,” Cytokine, 2017. View at Publisher · View at Google Scholar · View at Scopus
  92. P. Wang, Z. F. Ba, and I. H. Chaudry, “Administration of tumor necrosis factor-alpha in vivo depresses endothelium-dependent relaxation,” American Journal of Physiology-Heart and Circulatory Physiology, vol. 266, no. 6, pp. H2535–H2541, 1994. View at Publisher · View at Google Scholar
  93. K. Kotani, M. Miyamoto, and H. Ando, “The effect of treatments for rheumatoid arthritis on endothelial dysfunction evaluated by flow-mediated vasodilation in patients with rheumatoid arthritis,” Current Vascular Pharmacology, vol. 15, no. 1, pp. 10–18, 2017. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Danese, M. Sans, F. Scaldaferri et al., “TNF-alpha blockade down-regulates the CD40/CD40L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infliximab in Crohn’s disease,” Journal of Immunology, vol. 176, no. 4, pp. 2617–2624, 2006. View at Publisher · View at Google Scholar
  95. J. M. Lü, P. H. Lin, Q. Yao, and C. Chen, “Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems,” Journal of Cellular and Molecular Medicine, vol. 14, no. 4, pp. 840–860, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. K. Tran and A. C. Chan, “R,R,R-α-tocopherol potentiates prostacyclin release in human endothelial cells. Evidence for structural specificity of the tocopherol molecule,” Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, vol. 1043, no. 2, pp. 189–197, 1990. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Brigelius-Flohé and M. G. Traber, “Vitamin E: function and metabolism,” The FASEB Journal, vol. 13, no. 10, pp. 1145–1155, 1999. View at Publisher · View at Google Scholar
  98. J. Armour, K. Tyml, D. Lidington, and J. X. Wilson, “Ascorbate prevents microvascular dysfunction in the skeletal muscle of the septic rat,” Journal of Applied Physiology, vol. 90, no. 3, pp. 795–803, 2001. View at Publisher · View at Google Scholar
  99. J. M. May and F. E. Harrison, “Role of vitamin C in the function of the vascular endothelium,” Antioxidants & Redox Signaling, vol. 19, no. 17, pp. 2068–2083, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. T. Heitzer, H. Just, and T. Münzel, “Antioxidant vitamin C improves endothelial dysfunction in chronic smokers,” Circulation, vol. 94, no. 1, pp. 6–9, 1996. View at Publisher · View at Google Scholar · View at Scopus
  101. H. Amagase, B. Sun, and C. Borek, “Lycium barbarum [goji] juice improves in vivo antioxidant biomarkers in serum of healthy adults,” Nutrition Research, vol. 29, no. 1, pp. 19–25, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. X. M. Li, Y. L. Ma, and X. J. Liu, “Effect of the Lycium barbarum polysaccharides on age-related oxidative stress in aged mice,” Journal of Ethnopharmacology, vol. 111, no. 3, pp. 504–511, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. A. Keshavarzian, G. Morgan, S. Sedghi, J. H. Gordon, and M. Doria, “Role of reactive oxygen metabolites in experimental colitis,” Gut, vol. 31, no. 7, pp. 786–790, 1990. View at Publisher · View at Google Scholar
  104. B. Xia, C. S. Deng, D. J. Chen, Y. Zhou, and J. Q. Xiao, “Role of copper zinc superoxide dismutase in the short-term treatment of acetic acid-induced colitis in rats,” Acta Gastroenterologica Latinoamericana, vol. 26, no. 4, pp. 227–230, 1996. View at Google Scholar
  105. J. Seguí, F. Gil, M. Gironella et al., “Down-regulation of endothelial adhesion molecules and leukocyte adhesion by treatment with superoxide dismutase is beneficial in chronic immune experimental colitis,” Inflammatory Bowel Diseases, vol. 11, no. 10, pp. 872–882, 2005. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Seguí, M. Gironella, M. Sans et al., “Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine,” Journal of Leukocyte Biology, vol. 76, no. 3, pp. 537–544, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. N. Martins, L. Barros, C. Santos-Buelga, S. Silva, M. Henriques, and I. C. F. R. Ferreira, “Decoction, infusion and hydroalcoholic extract of cultivated thyme: antioxidant and antibacterial activities, and phenolic characterisation,” Food Chemistry, vol. 167, pp. 131–137, 2015. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Nickavar and N. Esbati, “Evaluation of the antioxidant capacity and phenolic content of three thymus species,” Journal of Acupuncture and Meridian Studies, vol. 5, no. 3, pp. 119–125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. T. Murase, S. Haramizu, A. Shimotoyodome, I. Tokimitsu, and T. Hase, “Green tea extract improves running endurance in mice by stimulating lipid utilization during exercise,” American Journal of Physiology Regulatory, Integrative and Comparative Physiology, vol. 290, no. 6, pp. R1550–R1556, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. Q.-Y. Lu, Y. Jin, J. T. Mao et al., “Green tea inhibits cycolooxygenase-2 in non-small cell lung cancer cells through the induction of annexin-1,” Biochemical and Biophysical Research Communications, vol. 427, no. 4, pp. 725–730, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. K. M. Kim, S. B. Chun, M. S. Koo et al., “Differential regulation of NO availability from macrophages and endothelial cells by the garlic component S-allyl cysteine,” Free Radical Biology & Medicine, vol. 30, no. 7, pp. 747–756, 2001. View at Publisher · View at Google Scholar · View at Scopus
  112. S. D. Rodrigues, K. C. França, F. T. Dallin et al., “N-acetylcysteine as a potential strategy to attenuate the oxidative stress induced by uremic serum in the vascular system,” Life Sciences, vol. 121, pp. 110–116, 2015. View at Publisher · View at Google Scholar · View at Scopus
  113. M. Sasaki, D. Ostanin, J. W. Elrod et al., “TNF-α-induced endothelial cell adhesion molecule expression is cytochromeP-450 monooxygenase dependent,” American Journal of Physiology Cell Physiology, vol. 284, no. 2, pp. C422–C428, 2003. View at Publisher · View at Google Scholar
  114. G. S. Ribas, C. R. Vargas, and M. Wajner, “L-Carnitine supplementation as a potential antioxidant therapy for inherited neurometabolic disorders,” Gene, vol. 533, no. 2, pp. 469–476, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. M. A. Stasi, M. G. Scioli, G. Arcuri et al., “Propionyl-L-carnitine improves postischemic blood flow recovery and arteriogenetic revascularization and reduces endothelial NADPH-oxidase 4-mediated superoxide production,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 3, pp. 426–435, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. G. D’Argenio, G. Mazzone, C. Tuccillo et al., “Apple polyphenols extract (APE) improves colon damage in a rat model of colitis,” Digestive and Liver Disease, vol. 44, no. 7, pp. 555–562, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. D. G. Binion, J. Heidemann, M. S. Li, V. M. Nelson, M. F. Otterson, and P. Rafiee, “Vascular cell adhesion molecule-1 expression in human intestinal microvascular endothelial cells is regulated by PI 3-kinase/Akt/MAPK/NF-kappaB: inhibitory role of curcumin,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 297, no. 2, pp. G259–G268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  118. W. J. Zhang and B. Frei, “Alpha-lipoic acid inhibits TNF-alpha-induced NF-kappaB activation and adhesion molecule expression in human aortic endothelial cells,” The FASEB Journal, vol. 15, no. 13, pp. 2423–2432, 2001. View at Publisher · View at Google Scholar · View at Scopus
  119. K. M. Sakthivel and C. Guruvayoorappan, “Amentoflavone inhibits iNOS, COX-2 expression and modulates cytokine profile, NF-κB signal transduction pathways in rats with ulcerative colitis,” International Immunopharmacology, vol. 17, no. 3, pp. 907–916, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. B. J. Geerling, A. Badart-Smook, R. W. Stockbrügger, and R. J. Brummer, “Comprehensive nutritional status in recently diagnosed patients with inflammatory bowel disease compared with population controls,” European Journal of Clinical Nutrition, vol. 54, no. 6, pp. 514–521, 2000. View at Publisher · View at Google Scholar · View at Scopus
  121. J. Jahnsen, J. A. Falch, P. Mowinckel, and E. Aadland, “Body composition in patients with inflammatory bowel disease: a population-based study,” The American Journal of Gastroenterology, vol. 98, no. 7, pp. 1556–1562, 2003. View at Publisher · View at Google Scholar
  122. P. Ruisi, J. N. Makaryus, M. Ruisi, and A. N. Makaryus, “Inflammatory bowel disease as a risk factor for premature coronary artery disease,” Journal of Clinical Medicine Research, vol. 7, no. 4, pp. 257–261, 2015. View at Publisher · View at Google Scholar