Effects of triple antioxidant therapy on measures of cardiovascular autonomic neuropathy and on myocardial blood flow in type 1 diabetes: A randomised controlled trial

Diabetologia

Volumn 56, Issue 8, 2013, Pages 1835-1844

  Pop Busui, R ^a   Stevens, M J ^b   Raffel, D M ^c   White, E A ^a   Mehta, M ^a   Plunkett, C D ^a   Brown, M B ^c   Feldman, E L ^c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Antioxidant therapy; Cardiovascular autonomic neuropathy; Myocardial blood flow; Randomised trial

Indexed keywords

ALLOPURINOL; ANTIOXIDANT; HEMOGLOBIN A1C; ISOPROSTANE DERIVATIVE; LIVER ENZYME; NICOTINAMIDE; PLACEBO; THIOCTIC ACID;

ADULT; ARTICLE; AUTONOMIC NEUROPATHY; BLOOD TOXICITY; BLURRED VISION; CARDIOVASCULAR AUTONOMIC NEUROPATHY; CARDIOVASCULAR DISEASE; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; CORONARY FLOW RESERVE; DEPRESSION; DIABETIC NEUROPATHY; DIABETIC PATIENT; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG ERUPTION; DRUG HYPERSENSITIVITY; EAR DISEASE; EPIDERMIS; FEMALE; GASTROINTESTINAL SYMPTOM; GYNECOLOGIC DISEASE; HEART MUSCLE BLOOD FLOW; HUMAN; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; ISCHEMIC HEART DISEASE; MALE; MUSCULOSKELETAL DISEASE; NERVE FIBER; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROTOXICITY; NOSE DISEASE; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PARALLEL DESIGN; PATIENT COMPLIANCE; PERIPHERAL NEUROPATHY; PHARMACIST; PRIORITY JOURNAL; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; RESPIRATORY TRACT DISEASE; SIDE EFFECT; SKIN NERVE; SYMPTOM; THROAT DISEASE; TREATMENT RESPONSE; UROGENITAL TRACT DISEASE; VIRUS INFECTION;

ADOLESCENT; ADULT; AGED; ALLOPURINOL; ANTIOXIDANTS; DIABETES MELLITUS, TYPE 1; DIABETIC NEUROPATHIES; FEMALE; HUMANS; MALE; MIDDLE AGED; MYOCARDIUM; NIACINAMIDE; REGIONAL BLOOD FLOW; YOUNG ADULT;

EID: 84879967614     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-013-2942-9     Document Type: Article

References (43)

1. Nathan DM, Cleary PA, Backlund JY et al (2005) Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353:2643-2653
2. Pop-Busui R (2010) Cardiac autonomic neuropathy in diabetes: a clinical perspective. Diabetes Care 33:434-441
3. Pop-Busui R, Kirkwood I, Schmid H et al (2004) Sympathetic dysfunction in type 1 diabetes: association with impaired myocardial blood flow reserve and diastolic dysfunction. J Am Coll Cardiol 44:2368-2374
4. Taskiran M, Rasmussen V, Rasmussen B et al (2004) Left ventricular dysfunction in normotensive type 1 diabetic patients: the impact of autonomic neuropathy. Diabet Med 21:524-530
5. Pennathur S, Heinecke JW (2007) Mechanisms for oxidative stress in diabetic cardiovascular disease. Antioxid Redox Signal 9:955-969
6. Edwards JL, Vincent AM, Cheng HT, Feldman EL (2008) Diabetic neuropathy: mechanisms to management. Pharmacol Ther 120:1-34
7. Hur J, Sullivan KA, Schuyler AD et al (2010) Literature-based discovery of diabetes- and ROS-related targets. BMC Med Genomics 3:49
8. Hoeldtke RD, Bryner KD, VanDyke K (2011) Oxidative stress and autonomic nerve function in early type 1 diabetes. Clin Auton Res 21:19-28
9. Ziegler D, Gries F (1997) Alpha-lipoic acid in the treatment of diabetic peripheral and cardiac autonomic neuropathy. Diabetes 46:S62-S66
10. Klein R, Klein BE, Moss SE, Cruickshanks KJ (1998) The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XVII. The 14-year incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophthalmology 105:1801-1815
11. Raffel DM, Wieland DM (2001) Assessment of cardiac sympathetic nerve integrity with positron emission tomography. Nucl Med Biol 28:541-559
12. Stevens MJ, Raffel DM, Allman KC, Schwaiger M, Wieland DM (1999) Regression and progression of cardiac sympathetic dysinnervation complicating diabetes: an assessment by C-11 hydroxyephedrine and positron emission tomography. Metabolism 48:92-101
13. Pop-Busui R, Low PA, Waberski BH et al (2009) Effects of prior intensive insulin therapy on cardiac autonomic nervous system function in type 1 diabetes mellitus: the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications study (DCCT/EDIC). Circulation 119:2886-2893
14. Stevens MJ, Dayanikli F, Raffel DM et al (1998) Scintigraphic assessment of regionalized defects in myocardial sympathetic innervation and blood flow regulation in diabetic patients with autonomic neuropathy. J Am Coll Cardiol 31:1575-1584
15. Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene DA (1994) A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 17:1281-1289
16. DCCT (1995) Effect of intensive diabetes treatment on nerve conduction in the Diabetes Control and Complications Trial. Ann Neurol 38:869-880
17. Polydefkis M, Hauer P, Griffin JW, McArthur JC (2001) Skin biopsy as a tool to assess distal small fiber innervation in diabetic neuropathy. Diabetes Technol Ther 3:23-28
18. Liu W, Morrow JD, Yin H (2009) Quantification of F2-isoprostanes as a reliable index of oxidative stress in vivo using gas chromatography-mass spectrometry (GC-MS) method. Free Radic Biol Med 47:1101-1107
19. Stevens MJ, Raffel DM, Allman KC et al (1998) Cardiac sympathetic dysinnervation in diabetes: implications for enhanced cardiovascular risk. Circulation 98:961-968
20. Vickers AJ, Altman DG (2001) Statistics notes: analysing controlled trials with baseline and follow up measurements. BMJ 323:1123-1124
21. Obrosova IG, Fathallah L, Stevens MJ (2001) Taurine counteracts oxidative stress and nerve growth factor deficit in early experimental diabetic neuropathy. Exp Neurol 172:211-219
22. Stevens MJ, Obrosova I, Cao X, Van Huysen C, Greene DA (2000) Effects of DL-alpha-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes 49:1006-1015
23. Feldman EL (2003) Oxidative stress and diabetic neuropathy: a new understanding of an old problem. J Clin Invest 111:431-433
24. Kellogg AP, Wiggin T, Larkin D, Hayes J, Stevens M, Pop-Busui R (2007) Protective effects of cyclooxygenase-2 gene inactivation against peripheral nerve dysfunction and intraepidermal nerve fiber loss in experimental diabetes. Diabetes 56:2997-3005
25. Vincent AM, Perrone L, Sullivan KA et al (2007) Receptor for advanced glycation end products activation injures primary sensory neurons via oxidative stress. Endocrinology 148:548-558
26. Inkster ME, Cotter MA, Cameron NE (2007) Treatment with the xanthine oxidase inhibitor, allopurinol, improves nerve and vascular function in diabetic rats. Eur J Pharmacol 561:63-71
27. Rajesh M, Mukhopadhyay P, Batkai S et al (2009) Xanthine oxidase inhibitor allopurinol attenuates the development of diabetic cardiomyopathy. J Cell Mol Med 13:2330-2341
28. Stevens MJ, Li F, Drel VR et al (2007) Nicotinamide reverses neurological and neurovascular deficits in streptozotocin diabetic rats. J Pharmacol Exp Ther 320:458-464
29. Negi G, Kumar A, Kaundal RK, Gulati A, Sharma SS (2010) Functional and biochemical evidence indicating beneficial effect of melatonin and nicotinamide alone and in combination in experimental diabetic neuropathy. Neuropharmacology 58:585-592
30. Vincent AM, Stevens MJ, Backus C, McLean LL, Feldman EL (2005) Cell culture modeling to test therapies against hyperglycemia-mediated oxidative stress and injury. Antioxid Redox Signal 7:1494-1506
31. Tankova T, Cherninkova S, Koev D (2005) Treatment for diabetic mononeuropathy with alpha-lipoic acid. Int J Clin Pract 59:645-650
32. Golbidi S, Badran M, Laher I (2011) Diabetes and alpha lipoic acid. Front Pharmacol 2:69
33. Ziegler D, Schatz H, Conrad F et al (1997) Effects of treatment with the antioxidant α-lipoic acid on cardiac autonomic neuropathy in NIDDM patients. A 4-month randomized controlled multicenter trial (DEKAN Study). Diabetes Care 20:369-373
34. Ziegler D, Reljanovic M, Mehnert H, Gries FA (1999) Alpha-lipoic acid in the treatment of diabetic polyneuropathy in Germany: current evidence from clinical trials. Exp Clin Endocrinol Diabetes 107:421-430
35. Ametov AS, Barinov A, Dyck PJ et al (2003) The sensory symptoms of diabetic polyneuropathy are improved with alpha-lipoic acid: the SYDNEY trial. Diabetes Care 26:770-776
36. Ziegler D, Ametov A, Barinov A et al (2006) Oral treatment with alpha-lipoic acid improves symptomatic diabetic polyneuropathy: the SYDNEY 2 trial. Diabetes Care 29:2365-2370
37. Ziegler D, Low PA, Litchy WJ et al (2011) Efficacy and safety of antioxidant treatment with alpha-lipoic acid over 4 years in diabetic polyneuropathy: the NATHAN 1 trial. Diabetes Care 34:2054-2060
38. Huang EA, Gitelman SE (2008) The effect of oral alpha-lipoic acid on oxidative stress in adolescents with type 1 diabetes mellitus. Pediatr Diabetes 9:69-73
39. Bertolotto F, Massone A (2012) Combination of alpha lipoic acid and superoxide dismutase leads to physiological and symptomatic improvements in diabetic neuropathy. Drugs R D 12:29-34
40. Ruhnau KJ, Meissner HP, Finn JR et al (1999) Effects of 3-week oral treatment with the antioxidant thioctic acid (alpha-lipoic acid) in symptomatic diabetic polyneuropathy. Diabet Med 16:1040-1043
41. Mooradian AD, Haas MJ (2011) Glucose-induced endoplasmic reticulum stress is independent of oxidative stress: a mechanistic explanation for the failure of antioxidant therapy in diabetes. Free Radic Biol Med 50:1140-1143
42. George J, Carr E, Davies J, Belch JJ, Struthers A (2006) High-dose allopurinol improves endothelial function by profoundly reducing vascular oxidative stress and not by lowering uric acid. Circulation 114:2508-2516
43. Sorrentino SA, Besler C, Rohrer L et al (2010) Endothelial-vasoprotective effects of high-density lipoprotein are impaired in patients with type 2 diabetes mellitus but are improved after extended-release niacin therapy. Circulation 121:110-122 Diseases Diseases