Role of alpha-lipoic acid in vascular function: A systematic review of human intervention studies

References

• Akbari, M., V. Ostadmohammadi, K. B. Lankarani, R. Tabrizi, F. Kolahdooz, S. R. Khatibi, and Z. Asemi. 2018. The effects of alpha-lipoic acid supplementation on glucose control and lipid profiles among patients with metabolic diseases: A systematic review and meta-analysis of randomized controlled trials. Metabolism 87:56–69. doi: 10.1016/j.metabol.2018.07.002.
   PubMed Web of Science ®Google Scholar
• Badran, M., B. Abuyassin, S. Golbidi, N. Ayas, and I. Laher. 2019. Alpha lipoic acid improves endothelial function and oxidative stress in mice exposed to chronic intermittent hypoxia. Oxidative Medicine and Cellular Longevity 2019:4093018. doi: 10.1155/2019/4093018.
   PubMed Web of Science ®Google Scholar
• Bjørklund, G., J. Aaseth, G. Crisponi, M. M. Rahman, and S. Chirumbolo. 2019. Insights on alpha lipoic and dihydrolipoic acids as promising scavengers of oxidative stress and possible chelators in mercury toxicology. Journal of Inorganic Biochemistry 195:111–9. doi: 10.1016/j.jinorgbio.2019.03.019.
   PubMed Web of Science ®Google Scholar
• Boulton, A. J., P. Kempler, A. Ametov, and D. Ziegler. 2013. Whither pathogenetic treatments for diabetic polyneuropathy? Diabetes/Metabolism Research and Reviews 29 (5):327–33. doi: 10.1002/dmrr.2397.
   PubMed Web of Science ®Google Scholar
• Buelna-Chontal, M., and C. Zazueta. 2013. Redox activation of Nrf2 & NF-κB: A double end sword? Cellular Signalling 25 (12):2548–57. doi: 10.1016/j.cellsig.2013.08.007.
   PubMed Web of Science ®Google Scholar
• Chang, J. W., E. K. Lee, T. H. Kim, W. K. Min, S. Chun, K. U. Lee, S. B. Kim, and J. S. Park. 2007. Effects of alpha-lipoic acid on the plasma levels of asymmetric dimethylarginine in diabetic end-stage renal disease patients on hemodialysis: A pilot study. American Journal of Nephrology 27 (1):70–4. doi: 10.1159/000099035.
   PubMed Web of Science ®Google Scholar
• d’Uscio, L. V., S. Milstien, D. Richardson, L. Smith, and Z. S. Katusic. 2003. Long-term vitamin C treatment increases vascular tetrahydrobiopterin levels and nitric oxide synthase activity. Circulation Research 92 (1):88–95. doi: 10.1161/01.res.0000049166.33035.62.
   PubMed Web of Science ®Google Scholar
• Deanfield, J. E., J. P. Halcox, and T. J. Rabelink. 2007. Endothelial function and dysfunction: Testing and clinical relevance. Circulation 115 (10):1285–95. doi: 10.1161/CIRCULATIONAHA.106.652859.
   PubMed Web of Science ®Google Scholar
• Derosa, G., A. D’Angelo, D. Romano, and P. Maffioli. 2016. A clinical trial about a food supplement containing α-lipoic acid on oxidative stress markers in type 2 diabetic patients. International Journal of Molecular Sciences 17 (11):1802. doi: 10.3390/ijms17111802.
   Web of Science ®Google Scholar
• Ford, I., M. A. Cotter, N. E. Cameron, and M. Greaves. 2001. The effects of treatment with [alpha]-lipoic acid or evening primrose oil on vascular hemostatic and lipid risk factors, blood flow, and peripheral nerve conduction in the streptozotocin-diabetic rat. Metabolism 50 (8):868–75. doi: 10.1053/meta.2001.24914.
   PubMed Web of Science ®Google Scholar
• Förstermann, U. 2010. Nitric oxide and oxidative stress in vascular disease. Pflugers Archiv 459 (6):923–39. doi: 10.1007/s00424-010-0808-2.
   PubMed Web of Science ®Google Scholar
• Fratantonio, D., A. Speciale, M. Molonia, R. Bashllari, M. Palumbo, A. Saija, F. Cimino, G. Monastra, and F. Virgili. 2018. Alpha-lipoic acid, but not di-hydrolipoic acid, activates Nrf2 response in primary human umbilical-vein endothelial cells and protects against TNF-α induced endothelium dysfunction. Archives of Biochemistry and Biophysics 655:18–25. doi: 10.1016/j.abb.2018.08.003.
   PubMed Web of Science ®Google Scholar
• Haghighatdoost, F., and M. Hariri. 2019. The effect of alpha-lipoic acid on inflammatory mediators: A systematic review and meta-analysis on randomized clinical trials. European Journal of Pharmacology 849:115–23. doi: 10.1016/j.ejphar.2019.01.065.
   PubMed Web of Science ®Google Scholar
• Harding, S. V., T. C. Rideout, and P. J. Jones. 2012. Evidence for using alpha-lipoic acid in reducing lipoprotein and inflammatory related atherosclerotic risk. Journal of Dietary Supplements 9 (2):116–27. doi: 10.3109/19390211.2012.683136.
   PubMedGoogle Scholar
• Heinisch, B. B., M. Francesconi, F. Mittermayer, G. Schaller, G. Gouya, M. Wolzt, and J. Pleiner. 2010. Alpha-lipoic acid improves vascular endothelial function in patients with type 2 diabetes: A placebo-controlled randomized trial. European Journal of Clinical Investigation 40 (2):148–54. doi: 10.1111/j.1365-2362.2009.02236.x.
   PubMed Web of Science ®Google Scholar
• Heitzer, T., B. Finckh, S. Albers, K. Krohn, A. Kohlschütter, and T. Meinertz. 2001. Beneficial effects of alpha-lipoic acid and ascorbic acid on endothelium-dependent, nitric oxide-mediated vasodilation in diabetic patients: Relation to parameters of oxidative stress . Free Radical Biology & Medicine 31 (1):53–61. doi: 10.1016/S0891-5849(01)00551-2.
   PubMed Web of Science ®Google Scholar
• Higgins, J. P., D. G. Altman, P. C. Gøtzsche, P. Jüni, D. Moher, A. D. Oxman, J. Savović, K. F. Schulz, L. Weeks, J. A. Sterne, and Cochrane Bias Methods Group. 2011. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. Bmj 343 (oct18 2):d5928–d5928. doi: 10.1136/bmj.d5928.
   PubMed Web of Science ®Google Scholar
• Inaba, Y., J. A. Chen, and S. R. Bergmann. 2010. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: A meta-analysis. The International Journal of Cardiovascular Imaging 26 (6):631–40. doi: 10.1007/s10554-010-9616-1.
   PubMed Web of Science ®Google Scholar
• Jin, H.-B., Y.-B. Yang, Y.-L. Song, Y-c Zhang, and Y.-R. Li. 2013. Lipoic acid attenuates the expression of adhesion molecules by increasing endothelial nitric-oxide synthase activity. Molecular Biology Reports 40 (1):377–82. doi: 10.1007/s11033-012-2071-4.
   PubMed Web of Science ®Google Scholar
• Khalili, M., M. Soltani, S. A. Moghadam, P. Dehghan, A. Azimi, and O. Abbaszadeh. 2017. Effect of alpha-lipoic acid on asymmetric dimethylarginine and disability in multiple sclerosis patients: A randomized clinical trial. Electronic Physician 9 (7):4899–905. doi: 10.19082/4899.
   PubMedGoogle Scholar
• Korkmaz, H., and O. Onalan. 2008. Evaluation of endothelial dysfunction: Flow-mediated dilation. Endothelium 15 (4):157–63. doi: 10.1080/10623320802228872.
   PubMed Web of Science ®Google Scholar
• Lai, S., L. Petramala, M. Muscaritoli, R. Cianci, S. Mazzaferro, A. P. Mitterhofer, M. Pasquali, V. D’Ambrosio, M. Carta, M. Ansuini, et al. 2020. α-lipoic acid in patients with autosomal dominant polycystic kidney disease. Nutrition 71:110594. doi: 10.1016/j.nut.2019.110594.
   PubMed Web of Science ®Google Scholar
• Lee, H. A., and D. A. Hughes. 2002. Alpha-lipoic acid modulates NF-κB activity in human monocytic cells by direct interaction with DNA. Experimental Gerontology 37 (2-3):401–10. doi: 10.1016/S0531-5565(01)00207-8.
   PubMed Web of Science ®Google Scholar
• Li, R.-J., W.-Q. Ji, J.-J. Pang, J.-L. Wang, Y.-G. Chen, and Y. Zhang. 2013. Alpha-lipoic acid ameliorates oxidative stress by increasing aldehyde dehydrogenase-2 activity in patients with acute coronary syndrome. The Tohoku Journal of Experimental Medicine 229 (1):45–51. doi: 10.1620/tjem.229.45.
   PubMed Web of Science ®Google Scholar
• Lin, K. Y., A. Ito, T. Asagami, P. S. Tsao, S. Adimoolam, M. Kimoto, H. Tsuji, G. M. Reaven, and J. P. Cooke. 2002. Impaired nitric oxide synthase pathway in diabetes mellitus: Role of asymmetric dimethylarginine and dimethylarginine dimethylaminohydrolase. Circulation 106 (8):987–92. doi: 10.1161/01.CIR.0000027109.14149.67.
   PubMed Web of Science ®Google Scholar
• Matsuzawa, Y., T. G. Kwon, R. J. Lennon, L. O. Lerman, and A. Lerman. 2015. Prognostic value of flow‐mediated vasodilation in brachial artery and fingertip artery for cardiovascular events: A systematic review and meta‐analysis. Journal of the American Heart Association 4 (11):e002270. doi: 10.1161/JAHA.115.002270.
   PubMed Web of Science ®Google Scholar
• McMackin, C. J., M. E. Widlansky, N. M. Hamburg, A. L. Huang, S. Weller, M. Holbrook, N. Gokce, T. M. Hagen, J. F. Keaney, Jr., and J. A. Vita. 2007. Effect of combined treatment with alpha-lipoic acid and acetyl-L-carnitine on vascular function and blood pressure in patients with coronary artery disease. Journal of Clinical Hypertension 9 (4):249–55. doi: 10.1111/j.1524-6175.2007.06052.x.
   PubMedGoogle Scholar
• Midaoui, A. E., and J. de Champlain. 2002. Prevention of hypertension, insulin resistance, and oxidative stress by alpha-lipoic acid. Hypertension 39 (2):303–7. doi: 10.1161/hy0202.104345.
   PubMed Web of Science ®Google Scholar
• Mohammadi, V., S. Dehghani, and G. Askari. 2017. Does alpha-lipoic acid supplement regulate blood pressure? A systematic review of randomized, double-blind placebo-controlled clinical trials. International Journal of Preventive Medicine 8 (1):33.
   Web of Science ®Google Scholar
• Muller-Delp, J. M. 2009. Ascorbic acid and tetrahydrobiopterin: looking beyond nitric oxide bioavailability. Cardiovascular Research 84 (2):178–9. doi:10.1093/cvr/cvp307. PMC: 19744948
   PubMed Web of Science ®Google Scholar
• Okudan, N., K. E. Nurullahoğlu Atalik, H. Gökbel, A. Canbilen, and I. Kara. 2011. Alpha lipoic acid treatment improved endothelium-dependent relaxation in diabetic rat aorta. Yakugaku Zasshi 131 (5):739–44. doi: 10.1248/yakushi.131.739.
   PubMed Web of Science ®Google Scholar
• Pang, L., P. Deng, Y. D. Liang, J. Y. Qian, L. C. Wu, L. L. Yang, Z. P. Yu, and Z. Zhou. 2019. Lipoic acid antagonizes paraquat-induced vascular endothelial dysfunction by suppressing mitochondrial reactive oxidative stress. Toxicology Research 8 (6):918–27. doi: 10.1039/c9tx00186g.
   Web of Science ®Google Scholar
• Pashaj, A., M. Xia, and R. Moreau. 2015. α-Lipoic acid as a triglyceride-lowering nutraceutical. Canadian Journal of Physiology and Pharmacology 93 (12):1029–41. doi: 10.1139/cjpp-2014-0480.
   PubMed Web of Science ®Google Scholar
• Rabelink, T. J., H. C. De Boer, and A. J. Van Zonneveld. 2010. Endothelial activation and circulating markers of endothelial activation in kidney disease. Nature Reviews. Nephrology 6 (7):404–14. doi: 10.1038/nrneph.2010.65.
   PubMed Web of Science ®Google Scholar
• Rahman, S. T., N. Merchant, T. Haque, J. Wahi, S. Bhaheetharan, K. C. Ferdinand, and B. V. Khan. 2012. The impact of lipoic acid on endothelial function and proteinuria in quinapril-treated diabetic patients with stage I hypertension: Results from the QUALITY study. Journal of Cardiovascular Pharmacology and Therapeutics 17 (2):139–45. doi: 10.1177/1074248411413282.
   PubMed Web of Science ®Google Scholar
• Rochette, L., S. Ghibu, C. Richard, M. Zeller, Y. Cottin, and C. Vergely. 2013. Direct and indirect antioxidant properties of α-lipoic acid and therapeutic potential . Molecular Nutrition & Food Research 57 (1):114–25. doi: 10.1002/mnfr.201200608.
   PubMed Web of Science ®Google Scholar
• Rodrigues-Krause, J., M. Krause, I. Rocha, D. Umpierre, and A. Fayh. 2019. Association of l-Arginine Supplementation with Markers of Endothelial Function in Patients with Cardiovascular or Metabolic Disorders: A Systematic Review and Meta-Analysis. Nutrients 11 (1):15 doi:10.3390/nu11010015.
   Web of Science ®Google Scholar
• Scaramuzza, A., E. Giani, F. Redaelli, S. Ungheri, M. Macedoni, V. Giudici, A. Bosetti, M. Ferrari, and G. V. Zuccotti. 2015. Alpha-lipoic acid and antioxidant diet help to improve endothelial dysfunction in adolescents with type 1 diabetes: A pilot trial. Journal of Diabetes Research 2015:1–7. doi: 10.1155/2015/474561.
   Web of Science ®Google Scholar
• Sena, C. M., E. Nunes, T. Louro, T. Proenca, R. Fernandes, M. R. Boarder, and R. M. Seica. 2008. Effects of alpha-lipoic acid on endothelial function in aged diabetic and high-fat fed rats. British Journal of Pharmacology 153 (5):894–906. doi: 10.1038/sj.bjp.0707474.
   PubMed Web of Science ®Google Scholar
• Sharman, J. E., P. Gunaruwan, W. L. Knez, M. Schmitt, S. A. Marsh, G. R. Wilson, J. R. Cockcroft, and J. S. Coombes. 2004. Alpha-lipoic acid does not acutely affect resistance and conduit artery function or oxidative stress in healthy men. British Journal of Clinical Pharmacology 58 (3):243–8. doi: 10.1111/j.1365-2125.2004.02146.x.
   PubMed Web of Science ®Google Scholar
• Shay, K. P., R. F. Moreau, E. J. Smith, A. R. Smith, and T. M. Hagen. 2009. Alpha-lipoic acid as a dietary supplement: Molecular mechanisms and therapeutic potential. Biochimica et Biophysica Acta 1790 (10):1149–60. doi: 10.1016/j.bbagen.2009.07.026.
   PubMed Web of Science ®Google Scholar
• Shen, D., L. Tian, T. Shen, H. Sun, and P. Liu. 2018. Alpha-lipoic acid protects human aortic endothelial cells against H2O2-induced injury and inhibits atherosclerosis in ovariectomized low density lipoprotein receptor knock-out mice. Cellular Physiology and Biochemistry 47 (6):2261–77. doi: 10.1159/000491537.
   PubMedGoogle Scholar
• Smith, A., F. Visioli, B. Frei, and T. Hagen. 2008. Lipoic acid significantly restores, in rats, the age-related decline in vasomotion . British Journal of Pharmacology 153 (8):1615–22. doi: 10.1038/bjp.2008.28.
   PubMed Web of Science ®Google Scholar
• Sola, S., M. Q. Mir, F. A. Cheema, N. Khan-Merchant, R. G. Menon, S. Parthasarathy, and B. V. Khan. 2005. Irbesartan and lipoic acid improve endothelial function and reduce markers of inflammation in the metabolic syndrome: Results of the Irbesartan and Lipoic Acid in Endothelial Dysfunction (ISLAND) study. Circulation 111 (3):343–8. doi: 10.1161/01.cir.0000153272.48711.b9.
   PubMed Web of Science ®Google Scholar
• Sun, H., W. Yao, Y. Tang, W. Zhuang, D. Wu, S. Huang, and H. Sheng. 2017. Urinary exosomes as a novel biomarker for evaluation of α‐lipoic acid's protective effect in early diabetic nephropathy. Journal of Clinical Laboratory Analysis 31 (6):e22129. doi: 10.1002/jcla.22129.
   Web of Science ®Google Scholar
• Sydow, K., and T. Münzel. 2003. ADMA and oxidative stress. Atherosclerosis. Supplements 4 (4):41–51. doi: 10.1016/s1567-5688(03)00033-3.
   PubMed Web of Science ®Google Scholar
• Takenouchi, Y., K. Tsuboi, K. Ohsuka, K. Nobe, K. Ohtake, Y. Okamoto, and K. Kasono. 2019. Chronic treatment with α-lipoic acid improves endothelium-dependent vasorelaxation of aortas in high-fat diet-fed mice. Biological & Pharmaceutical Bulletin 42 (9):1456–63. doi: 10.1248/bpb.b18-00800.
   PubMed Web of Science ®Google Scholar
• Tibullo, D., G. L. Volti, C. Giallongo, S. Grasso, D. Tomassoni, C. D. Anfuso, G. Lupo, F. Amenta, R. Avola, and V. Bramanti. 2017. Biochemical and clinical relevance of alpha lipoic acid: Antioxidant and anti-inflammatory activity, molecular pathways and therapeutic potential. Inflamm Res 66 (11):947–59. doi: 10.1007/s00011-017-1079-6.
   PubMed Web of Science ®Google Scholar
• Tromba, L., F. M. Perla, G. Carbotta, C. Chiesa, and L. Pacifico. 2019. Effect of alpha-lipoic acid supplementation on endothelial function and cardiovascular risk factors in overweight/obese youths: A double-blind, placebo-controlled randomized trial. Nutrients 11 (2):375. doi: 10.3390/nu11020375.
   Web of Science ®Google Scholar
• Vizzardi, E., M. Gavazzoni, P. Della Pina, I. Bonadei, V. Regazzoni, E. Sciatti, E. Trichaki, R. Raddino, and M. Metra. 2014. Noninvasive assessment of endothelial function: The classic methods and the new peripheral arterial tonometry. Journal of Investigative Medicine 62 (6):856–64. doi: 10.1097/JIM.0000000000000096.
   PubMed Web of Science ®Google Scholar
• Xiang, G. D., J. H. Pu, H. L. Sun, and L. S. Zhao. 2010. Alpha-lipoic acid improves endothelial dysfunction in patients with subclinical hypothyroidism. Experimental and Clinical Endocrinology & Diabetes 118 (09):625–9. doi: 10.1055/s-0029-1237702.
   PubMedGoogle Scholar
• Xiang, G., J. Pu, L. Yue, J. Hou, and H. Sun. 2011. α-lipoic acid can improve endothelial dysfunction in subjects with impaired fasting glucose. Metabolism 60 (4):480–5. doi: 10.1016/j.metabol.2010.04.011.
   PubMed Web of Science ®Google Scholar
• Xiang, G. D., H. L. Sun, L. S. Zhao, J. Hou, L. Yue, and L. Xu. 2008. The antioxidant alpha-lipoic acid improves endothelial dysfunction induced by acute hyperglycaemia during OGTT in impaired glucose tolerance. Clinical Endocrinology 68 (5):716–23. doi: 10.1111/j.1365-2265.2007.03099.x.
   PubMed Web of Science ®Google Scholar
• Xiang, W., L. Wang, S. Cheng, Y. Zhou, and L. Ma. 2019. Protective effects of alpha-lipoic acid on vascular oxidative stress in rats with hyperuricemia. Current Medical Science 39 (6):920–8. doi: 10.1007/s11596-019-2124-1.
   PubMed Web of Science ®Google Scholar
• Xu, Y., R. C. Arora, B. M. Hiebert, B. Lerner, A. Szwajcer, K. McDonald, C. Rigatto, P. Komenda, M. M. Sood, and N. Tangri. 2014. Non-invasive endothelial function testing and the risk of adverse outcomes: A systematic review and meta-analysis. European Heart Journal Cardiovascular Imaging 15 (7):736–46. doi: 10.1093/ehjci/jet256.
   PubMed Web of Science ®Google Scholar
• Ying, Z., N. Kherada, B. Farrar, T. Kampfrath, Y. Chung, O. Simonetti, J. Deiuliis, R. Desikan, B. Khan, F. Villamena, et al. 2010. Lipoic acid effects on established atherosclerosis. Life Sciences 86 (3-4):95–102. doi: 10.1016/j.lfs.2009.11.009.
   PubMed Web of Science ®Google Scholar
• Ying, Z., X. Xie, M. Chen, K. Yi, and S. Rajagopalan. 2015. Alpha-lipoic acid activates eNOS through activation of PI3-kinase/Akt signaling pathway. Vascular Pharmacology 64:28–35. doi: 10.1016/j.vph.2014.11.004.
   PubMed Web of Science ®Google Scholar
• Zhang, W. J., and B. Frei. 2001. alpha-lipoic acid inhibits TNF-alpha-induced NF-kappaB activation and adhesion molecule expression in human aortic endothelial cells . FASEB Journal 15 (13):2423–32. doi: 10.1096/fj.01-0260com.
   PubMed Web of Science ®Google Scholar
• Zhang, W.-J., K. E. Bird, T. S. McMillen, R. C. LeBoeuf, T. M. Hagen, and B. Frei. 2008. Dietary alpha-lipoic acid supplementation inhibits atherosclerotic lesion development in apolipoprotein E-deficient and apolipoprotein E/low-density lipoprotein receptor-deficient mice. Circulation 117 (3):421–8. doi: 10.1161/CIRCULATIONAHA.107.725275.
   PubMed Web of Science ®Google Scholar
• Ziegler, D., P. A. Low, W. J. Litchy, A. J. M. Boulton, A. I. Vinik, R. Freeman, R. Samigullin, H. Tritschler, U. Munzel, J. Maus, et al. 2011. Efficacy and safety of antioxidant treatment with α-lipoic acid over 4 years in diabetic polyneuropathy: The NATHAN 1 trial. Diabetes Care 34 (9):2054–60. doi: 10.2337/dc11-0503.
   PubMed Web of Science ®Google Scholar
• Zou, H., H. Wang, T. Liu, X. Li, X. Zhu, and Z. Wang. 2017. Protective role of α-lipoic acid in hyperuricemia-induced endothelial dysfunction. Experimental and Therapeutic Medicine 13 (6):3047–54. doi: 10.3892/etm.2017.4345.
   PubMed Web of Science ®Google Scholar