Effect of alpha-lipoic acid on arterial stiffness parameters in type 2 diabetes mellitus patients with cardiac autonomic neuropathy

Adeva-Andany MM, Ameneiros-Rodriguez E, Fernandez-Fernandez C, Dominguez-Montero A, Funcasta-Calderon R. Insulin resistance is associated with subclinical vascular disease in humans. World J Diabetes 10, 63–77, 2019.10.4239/wjd.v10.i2.63637973230788044 Search in Google Scholar

American Diabetes Association. Standards of medical care in diabetes-2017. Diabetes Care 40, 88–98, 2017.10.2337/dc17-er07c548197428522554 Search in Google Scholar

Ansar H, Mazloom Z, Kazemi F, Hejazi N. Effect of alpha-lipoic acid on blood glucose, insulin resistance, and glutathione peroxidase of type 2 diabetic patients. Saudi Med J 32, 584–588, 2011. Search in Google Scholar

Balcioglu AS, Muderrisoglu H. Diabetes and cardiac autonomic neuropathy: clinical manifestations, cardiovascular consequences, diagnosis and treatment. World J Diabetes 6, 80–89, 2015.10.4239/wjd.v6.i1.80431732025685280 Search in Google Scholar

Boghdadi MA, Afify HE, Sabri N, Makboul K, Elmazar M. Comparative study of vitamin B complex combined with alpha lipoic acid versus vitamin B complex in the treatment of diabetic polyneuropathy in type 2 diabetic patients. Clin Exp Pharmacol 7, 241, 2017. Search in Google Scholar

Chorepsima S, Eleftheriadou I, Tentolouris A, Moyssakis I, Protogerou A, Kokkinos A, Sfikakis PP, Tentolouris N. Pulse wave velocity and cardiac autonomic function in type 2 diabetes mellitus. BMC Endocr Disord 17, 27, 2017.10.1186/s12902-017-0178-2543853028526073 Search in Google Scholar

Colussi G, Catena C, Novello M, Bertin N, Sechi LA. Impact of omega-3 polyunsaturated fatty acids on vascular function and blood pressure: relevance for cardiovascular outcomes. Nutr Metab Cardiovasc Dis 27, 191–200, 2017.10.1016/j.numecd.2016.07.01127692558 Search in Google Scholar

Di Flaviani A, Picconi F, Di Stefano P, Giordani I, Malandrucco I, Maggio P, Palazzo P, Sgreccia F, Peraldo C, Farina F, Frajese G, Frontoni S. Impact of glycemic and blood pressure variability on surrogate measures of cardiovascular outcomes in type 2 diabetic patients. Diabetes Care 34, 1605–1609, 2011.10.2337/dc11-0034312019821610126 Search in Google Scholar

Dimitropoulos G, Tahrani AA, Stevens MJ. Cardiac autonomic neuropathy in patients with diabetes mellitus. World J Diabetes 5, 17–39, 2014.10.4239/wjd.v5.i1.17393242524567799 Search in Google Scholar

Emoto M, Nishizawa Y, Kawagishi T, Maekawa K, Hiura Y, Kanda H, Izumotani K, Shoji T, Ishimura E, Inaba M, Okuno Y, Morii H. Stiffness indexes β of the common carotid and femoral arteries are associated with insulin resistance in NIDDM. Diabetes Care 21, 1178–1182, 1998.10.2337/diacare.21.7.11789653616 Search in Google Scholar

Ewing DJ, Martyn CN, Young RJ, Clarke BF. The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 8, 491–498, 1985.10.2337/diacare.8.5.4914053936 Search in Google Scholar

Frontoni S, Di Bartolo P, Avogaro A, Bosi E, Paolisso G, Ceriello A. Glucose variability: An emerging target for the treatment of diabetes mellitus. Diabetes Res Clin Pract, 102, 86–95, 2013.10.1016/j.diabres.2013.09.00724128999 Search in Google Scholar

Golbidi S, Badran M, Laher I. Diabetes and alpha lipoic acid. Front Pharmacol 2, 69, 2011.10.3389/fphar.2011.00069 Search in Google Scholar

Gomes MB, Negrato CA. Alpha-lipoic acid as a pleiotropic compound with potential therapeutic use in diabetes and other chronic diseases. Diabetol Metab Syndr 6, 80, 2014.10.1186/1758-5996-6-80 Search in Google Scholar

Hosseini A, Abdollahi M. Diabetic neuropathy and oxidative stress. Oxid Med Cell Longer 2013, 168039, 2013.10.1155/2013/168039 Search in Google Scholar

Huikuri HV, Makikallio TH. Heart rate variability in ischemic heart disease. Auton Neurosci 90, 95–101, 2001.10.1016/S1566-0702(01)00273-9 Search in Google Scholar

Jacob S, Henriksen EJ, Schiemann AL, Simon I, Clancy DE, Tritschler HJ, Jung WI, Augustin HJ, Dietze GJ. Enhancement of glucose disposal in patients with type 2 diabetes by alpha-lipoic acid. Arzneimittel-Forsch 45, 872–874, 1995. Search in Google Scholar

Jacob S, Ruus P, Hermann R, Ritschler HJT, Maerker E, Renn W, Augustin HJ, Dietze GJ, Rett K. Oral administration of RAC-α-lipoic acid modulates insulin sensitivity in patients with type-2 diabetes mellitus: a placebo-controlled pilot trial. Free Radic Biol Med 27, 309–314, 1999.10.1016/S0891-5849(99)00089-1 Search in Google Scholar

Koumaras C, Katsiki N, Athyros VG, Karagiannis A. Metabolic syndrome and arterial stiffness: the past, the present and the future. J Cardiovasc Med (Hagerstown) 14, 687–689, 2013.10.2459/JCM.0b013e3283657c9624335882 Search in Google Scholar

La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, Nohara R, Bigger JT, Camm AJ, Schwartz PJ; ATRAMI Investigators. Autonomic tone and reflexes after myocardial infarction. Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: implications for clinical trials. Circulation 103, 2072–2077, 2001.10.1161/01.CIR.103.16.207211319197 Search in Google Scholar

Lal C, Kaur M, Jaryal AK, Deepak KK, Bhowmik D, Agarwal SK. Reduced baroreflex sensitivity, decreased heart rate variability with increased arterial stiffness in predialysis. Indian J Nephrol 27, 446–451, 2017.10.4103/ijn.IJN_63_17570440929217881 Search in Google Scholar

Lee SJ, Jeong SJ, Lee YC, Lee YH, Lee JE, Kim CH, Min KW, Cha BY. Effects of high-dose α-lipoic acid on heart rate variability of type 2 diabetes mellitus patients with cardiac autonomic neuropathy in Korea. Diabetes Metab J 41, 275–283, 2017.10.4093/dmj.2017.41.4.275558340528868825 Search in Google Scholar

Liatis S, Alexiadou K, Tsiakou A, Makrilakis K, Katsilambros N, Tentolouris N. Cardiac autonomic function correlates with arterial stiffness in the early stage of type 1 diabetes. Exp Diabetes Res 2011, 957901, 2011.10.1155/2011/957901314345421804819 Search in Google Scholar

MacFadyen RJ, Lim HS. Emergence of structural arterial stiffness in diabetes and the role of abnormalities of autonomic tone in the sequence of events. J Hum Hypertens 18, 755–756, 2004.10.1038/sj.jhh.100175515254562 Search in Google Scholar

Manrique C, Lastra G, Sowers JR. New insights into insulin action and resistance in the vasculature. Ann N Y Acad Sci 1311, 138–150, 2014.10.1111/nyas.12395398983824650277 Search in Google Scholar

Mansour AS, Yannoutsos A, Majahalme N, Agnoletti D, Safar ME, Ouerdane S, Blacher J. Aortic stiffness and cardiovascular risk in type 2 diabetes. J Hypertens 31, 1584–1592, 2013.10.1097/HJH.0b013e328361307423822928 Search in Google Scholar

Markus MRP, Rospleszcz S, Ittermann T, Baumeister SE, Schipf S, Siewert-Markus U, Lorbeer R, Storz C, Ptushkina V, Peters A, Meisinger C, Bamberg F, Nauck M, Bahls M, Volzke H, Burkhard Felix S, Bulow R, Rathmann W, Dorr M. Glucose and insulin levels are associated with arterial stiffness and concentric remodeling of the heart. Cardiovasc Diabetol 18, 145, 2019.10.1186/s12933-019-0948-4682993431684945 Search in Google Scholar

Maser RE, Mitchell BD, Vinik AI, Freeman R. The association between cardiovascular autonomic neuropathy and mortality in individuals with diabetes a meta-analysis. Diabetes Care 26, 1895–1901, 2003.10.2337/diacare.26.6.189512766130 Search in Google Scholar

Mattace-Raso FU, van den Meiracker AH, Bos WJ, van der Cammen TJ, Westerholf BE, Elias-Smale S, Reneman RS, Hoeks AP, Hofman A, Witteman JC. Arterial stiffness, cardiovagal baroreflex sensitivity and postural blood pressure changes in older adults: the Rotterdam Study. J Hypertens 25, 1421–1426, 2007.10.1097/HJH.0b013e32811d6a0717563564 Search in Google Scholar

Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419, 1985.10.1007/BF002808833899825 Search in Google Scholar

Morioka T, Mori K, Emoto M. Is stiffness parameter β useful for the evaluation of atherosclerosis? ~ Its clinical implications, limitations, and future perspectives. J Atheroscler Thromb 28, 435–453, 2021.10.5551/jat.RV17047819378833583910 Search in Google Scholar

Olsen MH, Fossum E, Hjerkinn E, Wachtell K, Hoieggen A, Nesbitt SD, Andersen UB, Phillips RA, Gaboury CL, Ibsen H, Kjeldsen SE, Julius S. Relative influence of insulin resistance vs blood pressure on vascular changes in longstanding hypertension. ICARUS, a LIFE substudy. Insulin Carotids US Scandinavia. J Hypertens 18, 75–81, 2000.10.1097/00004872-200018010-0001110678546 Search in Google Scholar

Pop Busui R, Stevens MJ, Raffel DM, White EA, Mehta M, Plunkett CD, Brown MB, Feldman EL. Effects of triple antioxidant therapy on measures of cardiovascular autonomic neuropathy and on myocardial blood flow in type 1 diabetes: a randomized controlled trial. Diabetologia 56, 1835–1844, 2013.10.1007/s00125-013-2942-9373082823740194 Search in Google Scholar

Pop-Busui R, Boulton AJM, Feldman EL, Bril V, Freeman R, Malik RA, Sosenko JM, Ziegler D. Diabetic neuropathy: a position statement by the American Diabetes Association. Diabetes Care 40, 136–154, 2017.10.2337/dc16-2042697740527999003 Search in Google Scholar

Ramamurthy S, Ronnet G. AMP-activated protein kinase (AMPK) and energy sensing in the brain. Exp Neurobiol 21, 52–60, 2012.10.5607/en.2012.21.2.52338121222792025 Search in Google Scholar

Scaramuzza A, Giani E, Redaelli F, Ungheri S, Macedoni M, Giudici V, Bosetti A, Ferrari M, Zuccotti GV. Alpha-lipoic acid and antioxidant diet help to improve endothelial dysfunction in adolescents with type 1 diabetes: A Pilot Trial. J Diabetes Res 2015, 474561, 2015.10.1155/2015/474561447838226171398 Search in Google Scholar

Sengstock DM, Vaitkevicius PV, Supiano MA. Arterial stiffness is related to insulin resistance in nondiabetic hyper-tensive older adults. J Clin Endocrinol Metab 90, 2823–2827, 2005.10.1210/jc.2004-168615728211 Search in Google Scholar

Serhiyenko VA, Serhiyenko AA. Diabetic cardiac autonomic neuropathy: Do we have any treatment perspectives? World J Diabetes 6, 245–258, 2015.10.4239/wjd.v6.i2.245436041825789106 Search in Google Scholar

Serhiyenko VA, Serhiyenko AA. Cardiac autonomic neuropathy: Risk factors, diagnosis and treatment. World J Diabetes 9, 1–24, 2018.10.4239/wjd.v9.i1.1576303629359025 Search in Google Scholar

Serhiyenko V, Serhiyenko L, Krasnyi M, Serhiyenko A. Alpha-lipoic acid: therapeutic potential in diabetic neuropathies. Curre Res Diabetes Obes J 7, 555713, 2018.10.19080/CRDOJ.2018.07.555713 Search in Google Scholar

Sessa F, Anna V, Messina G, Cibelli G, Monda V, Marsala G, Ruberto M, Biondi A, Cascio O, Bertozzi G, Pisanelli D, Maglietta F, Messina A, Mollica MP, Salerno M. Heart rate variability as predictive factor for sudden cardiac death. Aging (Albany NY), 10, 166–177, 2018.10.18632/aging.101386584285129476045 Search in Google Scholar

Shay KP, Moreau RF, Smith EJ, Smith AR, Hagen TM. Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 1790, 1149–1160, 2009.10.1016/j.bbagen.2009.07.026275629819664690 Search in Google Scholar

Sleight P, La Rovere MT, Mortara A, Pinna G, Maestri R, Leuzzi S, Bianchini B, Tavazzi L, Bernardi L. Physiology and pathophysiology of heart rate and blood pressure variability in humans: is power spectral analysis largely an index of baroreflex gain? Clin Sci 99, 103–109, 1995.10.1042/cs08801037677832 Search in Google Scholar

Soares-Miranda L, Sandercock G, Vale S, Santos R, Abreu S, Moreira C, Mota J. Metabolic syndrome, physical activity and cardiac autonomic function. Diabetes Metab Res Rev 28, 363–369, 2012.10.1002/dmrr.228122238216 Search in Google Scholar

Spallone V, Ziegler D, Freeman R, Bernardi L, Frontoni S, Pop-Busui R, Stevens M, Kempler P, Hilsted J, Tesfaye S, Low P, Valensi P; Toronto Consensus Panel on Diabetic Neuropathy. Cardiovascular autonomic neuropathy in diabetes: clinical impact, assessment, diagnosis, and management. Diabetes Metab Res Rev 27, 639–653, 2011.10.1002/dmrr.123921695768 Search in Google Scholar

Stehouwer CD, Henry RM, Ferreira I. Arterial stiffness in diabetes and the metabolic syndrome: a pathway to cardiovascular disease. Diabetologia 51, 527–539, 2008.10.1007/s00125-007-0918-318239908 Search in Google Scholar

Tandon N, Ali MK, Narayan KM. Pharmacologic prevention of microvascular and macrovascular complications in diabetes mellitus: implications of the results of recent clinical trials in type 2 diabetes. Am J Cardiovasc Drugs 12, 7–22, 2012.10.2165/11594650-000000000-0000022217193 Search in Google Scholar

TensioClinicTensioMed™ Arteriograph and TensioMed™ program. Available from: http://www.arteriograph.nl/?act=download&fid=173. Search in Google Scholar

Tesfaye S, Boulton AJM, Dyck PJ, Freeman R, Horowitz M, Kempler P, Lauria G, Malik RA, Spallone V, Vinik A, Bernardi L, Valensi P; Toronto Diabetic Neuropathy Expert Group. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 33, 2285–2293, 2010.10.2337/dc10-1303294517620876709 Search in Google Scholar

Tomiyama H, Hashimoto H, Hirayama Y, Yambe M, Yamada J, Koji Y, Shiina K, Yamamoto Y, Yamashina A. Synergistic acceleration of arterial stiffening in the presence of raised blood pressure and raised plasma glucose. Hypertension 47, 180–188, 2006.10.1161/01.HYP.0000198539.34501.1a16380535 Search in Google Scholar

Townsend RR, Wilkinson IB, Schiffrin EL, Avolio AP, Chirinos JA, Cockcroff JR, Heffernan KS, Lakatta EG, McEniery CM, Mitchell GF, Najjar SS, Nichols WW, Urbina EM, Weber T; American Heart Association Council on Hypertension. Recommendations for improving and standardizing vascular research on arterial stiffness: a scientific statement from the American Heart Association. Hypertension 66, 698–722, 2015.10.1161/HYP.0000000000000033458766126160955 Search in Google Scholar

Vallianou N, Evangelopoulos A, Koutalas P. Alpha-lipoic acid and diabetic neuropathy. Rev Diabet Stud 6, 230–236, 2009.10.1900/RDS.2009.6.230283619420043035 Search in Google Scholar

van Dijk RA, Bakker SJ, Scheffer PG, Heine RJ, Stehouwer CD. Associations of metabolic variables with arterial stiffness in type 2 diabetes mellitus: focus on insulin sensitivity and postprandial triglyceridaemia. Eur J Clin Invest 33, 307–315, 2003.10.1046/j.1365-2362.2003.01137.x12662161 Search in Google Scholar

Verrotti A, Prezioso G, Scattoni R, Chiarelli F. Autonomic neuropathy in diabetes mellitus. Front Endocrinol (Lausanne) 5, 205, 2014.10.3389/fendo.2014.00205424949225520703 Search in Google Scholar

Vinik AI, Erbas T. Diabetic autonomic neuropathy. Handb Clin Neurol 17, 279–294, 2013.10.1016/B978-0-444-53491-0.00022-524095132 Search in Google Scholar

Vinik AI, Erbas T, Casellini CM. Diabetic cardiac autonomic neuropathy, inflammation and cardiovascular disease. J Diabetes Investig 4, 4–18, 2013.10.1111/jdi.12042358088423550085 Search in Google Scholar

Vinik AI, Casellini C, Parson HK, Colberg SR, Nevoret ML. Cardiac autonomic neuropathy in diabetes: A predictor of cardiometabolic events. Front Neurosci 12, 591, 2018.10.3389/fnins.2018.00591611972430210276 Search in Google Scholar

Wang Y, Li X, Guo Y, Chan L, Guan X. Alpha-lipoic acid increases energy expenditure by enhancing adenosine monophosphate-activated protein kinase-peroxisome proliferator-activated receptor-gamma coactivator-1 alpha signaling in the skeletal muscle of aged mice. Metabolism 59, 967–976, 2010.10.1016/j.metabol.2009.10.018288250920015518 Search in Google Scholar

Yki-Jarvinen H, Westerbacka J. Insulin resistance, arterial stiffness and wave reflection. Adv Cardiol 44, 252–260, 2007.10.1159/00009674617075214 Search in Google Scholar

Ziegler D, Schatz H, Conrad F, Gries FA, Ulrich H, Reichel G. Effects of treatment with the antioxidant alpha-lipoic acid on cardiac autonomic neuropathy in NIDDM patients. A 4-month randomized controlled multicenter trial (DEKAN Study). Deutsche Kardiale Autonome Neuropathie. Diabetes Care 20, 369–373, 1997.10.2337/diacare.20.3.3699051389 Search in Google Scholar

Ziegler D, Low PA, Litchy WJ, Boulton AJ, Vinik AI, Freeman R, Samigullin R, Tritschler H, Munzel U, Maus J, Schutte K, Dyck PJ. Efficacy and safety of antioxidant treatment with α-lipoic acid over 4 years in diabetic polyneuropathy: the NATHAN 1 trial. Diabetes Care 34, 2054–2060, 2011.10.2337/dc11-0503316130121775755 Search in Google Scholar

Ziegler D, Keller J, Maier C, Pannek J; German Diabetes Association. Diabetic neuropathy. Exp Clin Endocrinol Diabetes 122, 406–415, 2014.10.1055/s-0034-136643525014092 Search in Google Scholar