Skip to main content
Erschienen in: Clinical Autonomic Research 1/2011

01.02.2011 | Review Article

Oxidative stress and autonomic nerve function in early type 1 diabetes

verfasst von: Robert Daniel Hoeldtke, Kimberly D. Bryner, Knox VanDyke

Erschienen in: Clinical Autonomic Research | Ausgabe 1/2011

Einloggen, um Zugang zu erhalten

Abstract

Introduction

The biochemical mechanisms by which hyperglycemia causes microvascular disease and neuropathy are poorly understood. Experimental studies have established that oxidative stress is present in diabetic rodents with neuropathy, and that antioxidant therapy is protective. Oxidative stress is also present in human diabetes, but its clinical importance is uncertain.

Material and methods

We examined several biochemical measures of oxidative stress in 37 patients with recent-onset (less than 2 years) type 1 diabetes annually in a 3-year longitudinal study. We also performed a comprehensive annual evaluation of somatosensory and autonomic nerve function. A total of 41 control subjects were studied.

Results

Malondialdehyde excretion, a measure of lipid peroxidation, was 1.5l ± .1 μmol/g creatinine in the control subjects, but 2.43 ± . 3 in the diabetic patients in year one, 2.39 ± .2 in year two and 1.92 ± .15 in year three, which was different from controls across all years; p < .005. Serum NOx (nitrate and nitric) was 34.0 ± 4.9 μmol/L in the controls, but 52.4 ± 5 in the diabetics in year one, 50.0 ± 5.1 in year two, and 49.0 ± 5.2 in year three, which was different from controls; p < .01. We measured sudomotor function and observed that the poorly controlled diabetic patients had relatively increased sweating above the waist and relatively decreased sweating below the waist, a typical pattern for sympathetic nerve injury. The ratio of sweating above to sweating below the waist was .385 ± .04 in controls, 0.70 ± .14 in diabetic patients in year one, .51 ± .14 in year two and .496 ± .12 in year three (different from controls; p < .01 across all years). Urinary MDA correlated negatively with total sweat (r = −39, p < .01); NOx also correlated negatively with total sweat (r = −.34, p < .025). Abnormalities in the processing of renin (the renin/prorenin ratio), a test of renal sympathetic neurons, was also documented in early type 1 diabetes.

Conclusions

Oxidative stress and excessive serum NOx are associated with sympathetic dysfunction in early type 1 diabetes.
Literatur
1.
Zurück zum Zitat Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M (2007) Oxidative DNA damage and augmentation of poly (ADP-ribose) polymerase/nuclear factor-kappa b signaling in patients with type 2 diabetes and microangiopathy. Int J Biochem and Cell Biol 39:1673–1684CrossRef Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M (2007) Oxidative DNA damage and augmentation of poly (ADP-ribose) polymerase/nuclear factor-kappa b signaling in patients with type 2 diabetes and microangiopathy. Int J Biochem and Cell Biol 39:1673–1684CrossRef
2.
Zurück zum Zitat Ames BN, Cathcart R, Schwiers E, Hochstein P (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA 78:6858–6862CrossRefPubMed Ames BN, Cathcart R, Schwiers E, Hochstein P (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: A hypothesis. Proc Natl Acad Sci USA 78:6858–6862CrossRefPubMed
3.
Zurück zum Zitat Bennett T, Hosking DJ, Hampton JR (1975) Cardiovascular control in diabetes mellitus. Br J Med 2:585–587CrossRef Bennett T, Hosking DJ, Hampton JR (1975) Cardiovascular control in diabetes mellitus. Br J Med 2:585–587CrossRef
4.
Zurück zum Zitat Chiarelli F, Cipollone F, Romano F, Tumini S, Costantini F, DiRicco L, Pomilio M, Pierdomenico SD, Marini M, Cuccurullo F, Mezzeti A (2002) Increased circulating nitric oxide in young patients with type I diabetes and persistent microalbuminuria. Diabetes 49:1258–1263CrossRef Chiarelli F, Cipollone F, Romano F, Tumini S, Costantini F, DiRicco L, Pomilio M, Pierdomenico SD, Marini M, Cuccurullo F, Mezzeti A (2002) Increased circulating nitric oxide in young patients with type I diabetes and persistent microalbuminuria. Diabetes 49:1258–1263CrossRef
5.
Zurück zum Zitat Coppey LJ, Gellet JS, Davidson EP, Dunlap JA, Lund DD, Yorek MA (2001) Effect of anti oxidant treatment on streptozotocin-induced diabetic rats on endoneurial blood flow, nerve conduction velocity, and vascular reactivity of epineural arterioles of the sciatic nerve. Diabetes 50:1927–1937CrossRefPubMed Coppey LJ, Gellet JS, Davidson EP, Dunlap JA, Lund DD, Yorek MA (2001) Effect of anti oxidant treatment on streptozotocin-induced diabetic rats on endoneurial blood flow, nerve conduction velocity, and vascular reactivity of epineural arterioles of the sciatic nerve. Diabetes 50:1927–1937CrossRefPubMed
6.
Zurück zum Zitat Davi G, Ciabattoni G, Consoli A, Mezzetti A, Falco A, Santarone S, Pennese E, Vitacolonna E, Bucciarelli T, Costantini F, Capani F, Patrono C (1999) In vivo formation of 8-iso-prostaglandin F2 and platelet activation in diabetes mellitus: effects of improved metabolic control and vitamin E supplementation. Circulation 99:224–229PubMed Davi G, Ciabattoni G, Consoli A, Mezzetti A, Falco A, Santarone S, Pennese E, Vitacolonna E, Bucciarelli T, Costantini F, Capani F, Patrono C (1999) In vivo formation of 8-iso-prostaglandin F2 and platelet activation in diabetes mellitus: effects of improved metabolic control and vitamin E supplementation. Circulation 99:224–229PubMed
7.
Zurück zum Zitat DeRosa MA, Cryer PE (2004) Hypoglycemia and the sympathoadrenal system: neurogenic symptoms are largely the result of sympathetic neural rather than adrenomedulary activation. Am J Phys Endocr Metab 287:E32–E41CrossRef DeRosa MA, Cryer PE (2004) Hypoglycemia and the sympathoadrenal system: neurogenic symptoms are largely the result of sympathetic neural rather than adrenomedulary activation. Am J Phys Endocr Metab 287:E32–E41CrossRef
8.
Zurück zum Zitat Dhiman M, Estrada-Franco JG, Pando JM, Ramirez-Aguilar FJ, Spratt H, Vazquez-Corzo S, Perez-Molina G, Gallegos-Sandova R, Moreno R, Garg NJ (2009) Increased myeloperoxidase activity and proteín nitration are indicators of inflammation in patients with Chagas’ disease. Clin Vaccine Immunol 16:660–666CrossRefPubMed Dhiman M, Estrada-Franco JG, Pando JM, Ramirez-Aguilar FJ, Spratt H, Vazquez-Corzo S, Perez-Molina G, Gallegos-Sandova R, Moreno R, Garg NJ (2009) Increased myeloperoxidase activity and proteín nitration are indicators of inflammation in patients with Chagas’ disease. Clin Vaccine Immunol 16:660–666CrossRefPubMed
9.
Zurück zum Zitat Drel VR, Lupachyk S, Shevalye H, Vareniuk I, Xu W, Zhang J, Delamere NA, Shahidullah M, Slusher B, Obrosova IG (2010) New therapeutic and biomarker discovery for peripheral diabetic neuropathy: PARP inhibitor, nitrotyrosine, and tumor necrosis factor-alpha. Endocrinology 151:1–9CrossRef Drel VR, Lupachyk S, Shevalye H, Vareniuk I, Xu W, Zhang J, Delamere NA, Shahidullah M, Slusher B, Obrosova IG (2010) New therapeutic and biomarker discovery for peripheral diabetic neuropathy: PARP inhibitor, nitrotyrosine, and tumor necrosis factor-alpha. Endocrinology 151:1–9CrossRef
10.
Zurück zum Zitat Feldman E (2003) Oxidative stress and diabetic neuropathy: a new understanding of an old problem. J Clin Invest 111:431–433PubMed Feldman E (2003) Oxidative stress and diabetic neuropathy: a new understanding of an old problem. J Clin Invest 111:431–433PubMed
11.
Zurück zum Zitat Giustarini D, Dalle-Donne I, Tsikas D, Rossi R (2009) Oxidative stress and human diseases: origin, link, measurement, mechanisms, and biomarkers. Crit Rev Clin Lab Sci 46:241–281CrossRefPubMed Giustarini D, Dalle-Donne I, Tsikas D, Rossi R (2009) Oxidative stress and human diseases: origin, link, measurement, mechanisms, and biomarkers. Crit Rev Clin Lab Sci 46:241–281CrossRefPubMed
12.
Zurück zum Zitat Goss DE, Trafford JC, Roberts VC, Flynn MD, Edmonds ME, Watkins PJ (1989) Raised ankle/brachial pressure index in insulin-treated diabetic patients. Diabetes Med 6:576–578CrossRef Goss DE, Trafford JC, Roberts VC, Flynn MD, Edmonds ME, Watkins PJ (1989) Raised ankle/brachial pressure index in insulin-treated diabetic patients. Diabetes Med 6:576–578CrossRef
13.
Zurück zum Zitat Grandenetti A, Chow DC, Sletten DM, Oyama JK, Theriault AG, Schatz IJ, Low PA (2007) Impaired glucose tolerance is associated with postganglionic sudomotor impairment. Clin Auton Res 17:231–233CrossRef Grandenetti A, Chow DC, Sletten DM, Oyama JK, Theriault AG, Schatz IJ, Low PA (2007) Impaired glucose tolerance is associated with postganglionic sudomotor impairment. Clin Auton Res 17:231–233CrossRef
14.
Zurück zum Zitat Hensley K, Maidt ML, Yu Z, San H, Merkeshery WR, Floyd RA (1998) Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer’s brain indicates region specific accumulation. J Neurosci 18:8126–8132PubMed Hensley K, Maidt ML, Yu Z, San H, Merkeshery WR, Floyd RA (1998) Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer’s brain indicates region specific accumulation. J Neurosci 18:8126–8132PubMed
15.
Zurück zum Zitat Hoeldtke RD (2006) Oxidative stress in type I diabetes: a clinical perspective. In: Opara E (ed) Nutrition and diabetes: pathophysiology and treatment. Taylor and Francis, Boca Raton, pp 319–344 Hoeldtke RD (2006) Oxidative stress in type I diabetes: a clinical perspective. In: Opara E (ed) Nutrition and diabetes: pathophysiology and treatment. Taylor and Francis, Boca Raton, pp 319–344
16.
Zurück zum Zitat Hoeldtke RD, Bryner KD, Corum LL, Hobbs GR, VanDyke K (2009) Lipid peroxidation in early type I diabetes mellitus is unassociated with oxidative damage to DNA. Metab Clin Exp 58:731–734PubMed Hoeldtke RD, Bryner KD, Corum LL, Hobbs GR, VanDyke K (2009) Lipid peroxidation in early type I diabetes mellitus is unassociated with oxidative damage to DNA. Metab Clin Exp 58:731–734PubMed
17.
Zurück zum Zitat Hoeldtke RD, Bryner KD, Hoeldtke ME, Christie I, Ganzer G, Hobbs G, Riggs J (2006) Sympathetic sudomotor disturbance in early type I diabetes mellitus is linked to lipid peroxidation. Metabolism Clin Exp 55:1524–1531 Hoeldtke RD, Bryner KD, Hoeldtke ME, Christie I, Ganzer G, Hobbs G, Riggs J (2006) Sympathetic sudomotor disturbance in early type I diabetes mellitus is linked to lipid peroxidation. Metabolism Clin Exp 55:1524–1531
18.
Zurück zum Zitat Hoeldtke RD, Bryner KD, Horvath GG, Phares RW, Broy LF, Hobbs GR (2001) Redistribution of sudomotor responses is an early sign of sympathetic dysfunction in Type I diabetes. Diabetes 50:436–443CrossRefPubMed Hoeldtke RD, Bryner KD, Horvath GG, Phares RW, Broy LF, Hobbs GR (2001) Redistribution of sudomotor responses is an early sign of sympathetic dysfunction in Type I diabetes. Diabetes 50:436–443CrossRefPubMed
19.
Zurück zum Zitat Hoeldtke RD, Bryner KD, McNeill DR, Hobbs GR, Riggs JE, Warehime SS, Christie I, Ganser G, VanDyke K (2002) Nitrosative stress, uric acid and peripheral nerve function in Early type I diabetes. Diabetes 51:2817–2825CrossRefPubMed Hoeldtke RD, Bryner KD, McNeill DR, Hobbs GR, Riggs JE, Warehime SS, Christie I, Ganser G, VanDyke K (2002) Nitrosative stress, uric acid and peripheral nerve function in Early type I diabetes. Diabetes 51:2817–2825CrossRefPubMed
20.
Zurück zum Zitat Klandorf H, Rathore DS, Iqbal M, Shi X, VanDyke K (2001) Accelerated tissue aging and increased oxidative stress in broiler chickens fed allopurinol. Comp Biochem Physiol Toxicol Pharmacol 129:93–104CrossRef Klandorf H, Rathore DS, Iqbal M, Shi X, VanDyke K (2001) Accelerated tissue aging and increased oxidative stress in broiler chickens fed allopurinol. Comp Biochem Physiol Toxicol Pharmacol 129:93–104CrossRef
21.
Zurück zum Zitat Kosugi H, Kojima T, Kikugawa K (1993) Characteristics of the thiobarbituric acid reactivity of human urine as a possible consequence of lipid peroxidation. Lipids 28:337–343CrossRefPubMed Kosugi H, Kojima T, Kikugawa K (1993) Characteristics of the thiobarbituric acid reactivity of human urine as a possible consequence of lipid peroxidation. Lipids 28:337–343CrossRefPubMed
22.
Zurück zum Zitat Maejima K, Nakano S, Himeno M, Tsuda S, Makiishi H, Ito T, Nakagawa A, Kigoshi T, Ishibashi T, Nishio M, Uchida K (2001) Increased basal levels of plasma nitric oxide in Type 2 diabetic subjects. Relationship to microvascular complications. J Diabetes Complicat 15:135–143CrossRefPubMed Maejima K, Nakano S, Himeno M, Tsuda S, Makiishi H, Ito T, Nakagawa A, Kigoshi T, Ishibashi T, Nishio M, Uchida K (2001) Increased basal levels of plasma nitric oxide in Type 2 diabetic subjects. Relationship to microvascular complications. J Diabetes Complicat 15:135–143CrossRefPubMed
23.
Zurück zum Zitat Marnett LJ, Wright TL, Crews BC, Tannenbaum SR, Morrow JD (2000) Regulation of prostaglandin biosynthesis by nitric oxide is revealed by targeted deletion of inducible nitric-oxide synthase. J Biol Chem 275:13427–13430CrossRefPubMed Marnett LJ, Wright TL, Crews BC, Tannenbaum SR, Morrow JD (2000) Regulation of prostaglandin biosynthesis by nitric oxide is revealed by targeted deletion of inducible nitric-oxide synthase. J Biol Chem 275:13427–13430CrossRefPubMed
24.
Zurück zum Zitat Marra G, Cotroneo P, Pitocco D, Manto A, DiLeo MA, Ruotolo V, Caputo S, Giardna B, Ghirlandu G, Santini SA (2002) Early increase of oxidative stress and reduced antioxidant defenses in patients with uncomplicated type I diabetes: a case for gender difference. Diabetes Care 25:370–375CrossRefPubMed Marra G, Cotroneo P, Pitocco D, Manto A, DiLeo MA, Ruotolo V, Caputo S, Giardna B, Ghirlandu G, Santini SA (2002) Early increase of oxidative stress and reduced antioxidant defenses in patients with uncomplicated type I diabetes: a case for gender difference. Diabetes Care 25:370–375CrossRefPubMed
25.
Zurück zum Zitat Martinet W, Knaapen MWM, DeMeyer G, Herman AG, Kockx MM (2002) Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation 106:927–932CrossRefPubMed Martinet W, Knaapen MWM, DeMeyer G, Herman AG, Kockx MM (2002) Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation 106:927–932CrossRefPubMed
26.
Zurück zum Zitat Nishikawa T, Edelstein D, Brownlee MA (2000) Missing link: a single unifying mechanism for diabetic complications. Kidney Int 58(Suppl 77):S26–S30CrossRef Nishikawa T, Edelstein D, Brownlee MA (2000) Missing link: a single unifying mechanism for diabetic complications. Kidney Int 58(Suppl 77):S26–S30CrossRef
27.
Zurück zum Zitat Obrosova IG (2008) Diabetes and the peripheral nerve (2009). Biochem Biophys Acta 1792:931–940PubMed Obrosova IG (2008) Diabetes and the peripheral nerve (2009). Biochem Biophys Acta 1792:931–940PubMed
28.
Zurück zum Zitat O’Bryne S, Forte P, Roberts LJ II, Morrow JD, Johnston A, Anggard E, Leslie RDG, Benjamin N (2000) Nitric oxide synthesis and isoprostane production in subjects with type 1 diabetes and normal urinary albumin excretion. Diabetes 49:857–862CrossRef O’Bryne S, Forte P, Roberts LJ II, Morrow JD, Johnston A, Anggard E, Leslie RDG, Benjamin N (2000) Nitric oxide synthesis and isoprostane production in subjects with type 1 diabetes and normal urinary albumin excretion. Diabetes 49:857–862CrossRef
29.
Zurück zum Zitat Pitocco D, DiStasio E, Romitelli F, Zaccardi F, Tavazzi B, Manto A, Caputo S, Musella T, Zuppi C, Santini SA, Ghirlanda G (2008) Hypouricemia linked to overproduction of nitric oxide is an early marker of oxidative stress in female subjects with type I diabetes. Diabetes Metab Res Rev 24:318–323CrossRefPubMed Pitocco D, DiStasio E, Romitelli F, Zaccardi F, Tavazzi B, Manto A, Caputo S, Musella T, Zuppi C, Santini SA, Ghirlanda G (2008) Hypouricemia linked to overproduction of nitric oxide is an early marker of oxidative stress in female subjects with type I diabetes. Diabetes Metab Res Rev 24:318–323CrossRefPubMed
30.
Zurück zum Zitat Safinowski M, Wilhelm B, Reimer T, Weise A, Thome N, Hanel H, Forst T, Pfutzner A (2009) Determination of nitrotyrosine concentrations in plasma samples of diabetes mellitus patients by four different immunoassays leads to contradictive results and disqualifies the majority of the tests. Clin Chem Lab Med 47:483–488CrossRefPubMed Safinowski M, Wilhelm B, Reimer T, Weise A, Thome N, Hanel H, Forst T, Pfutzner A (2009) Determination of nitrotyrosine concentrations in plasma samples of diabetes mellitus patients by four different immunoassays leads to contradictive results and disqualifies the majority of the tests. Clin Chem Lab Med 47:483–488CrossRefPubMed
31.
Zurück zum Zitat Santos CXC, Anjos EI, Augusto O (1999) Uric acid oxidation by peroxynitrite: multiple reactions, free radical formation, and amplification of lipid peroxidation. Arch Biochem Biophys 372:285–294CrossRefPubMed Santos CXC, Anjos EI, Augusto O (1999) Uric acid oxidation by peroxynitrite: multiple reactions, free radical formation, and amplification of lipid peroxidation. Arch Biochem Biophys 372:285–294CrossRefPubMed
32.
Zurück zum Zitat Shelley WB, Florence R (1960) Compensatory hyperhidrosis after sympathectomy. New Engl J Med 263:1056–1058CrossRef Shelley WB, Florence R (1960) Compensatory hyperhidrosis after sympathectomy. New Engl J Med 263:1056–1058CrossRef
33.
Zurück zum Zitat Shishehbor MH, Aviles RJ, Brennan ML, Fu X, Goormastic M, Pearce GL, Gokce KeaneyJF, Penn MS, Sprecher DL, Vita JA, Hazen SL (2003) Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 289:1675–1680CrossRefPubMed Shishehbor MH, Aviles RJ, Brennan ML, Fu X, Goormastic M, Pearce GL, Gokce KeaneyJF, Penn MS, Sprecher DL, Vita JA, Hazen SL (2003) Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 289:1675–1680CrossRefPubMed
34.
Zurück zum Zitat Suto T, Losonczy G, Qiu C, Hill C, Samsell L, Ruby J, Charon N, Venuto R, Baylis C (1995) Acute changes in urinary excretion of nitrite + nitrate do not necessarily predict renal vascular NO production. Kidney Int 48:1272–1277CrossRefPubMed Suto T, Losonczy G, Qiu C, Hill C, Samsell L, Ruby J, Charon N, Venuto R, Baylis C (1995) Acute changes in urinary excretion of nitrite + nitrate do not necessarily predict renal vascular NO production. Kidney Int 48:1272–1277CrossRefPubMed
35.
Zurück zum Zitat Tesfaye S, Malik R, Harris N, Jakubowski JJ, Mody C, Rennie IG, Ward JD (1996) Arteriovenous shunting and proliferating new vessels in acute painful neuropathy of rapid glycemic control (insulin neuritis). Diabetologia 39:329–335CrossRefPubMed Tesfaye S, Malik R, Harris N, Jakubowski JJ, Mody C, Rennie IG, Ward JD (1996) Arteriovenous shunting and proliferating new vessels in acute painful neuropathy of rapid glycemic control (insulin neuritis). Diabetologia 39:329–335CrossRefPubMed
36.
Zurück zum Zitat Thum T, Fraccarollo D, Schultheiss M, Froese S, Galuppo P, Widder JD, Tsikas D, Ertl G, Bauersachs J (2007) Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56:666–674CrossRefPubMed Thum T, Fraccarollo D, Schultheiss M, Froese S, Galuppo P, Widder JD, Tsikas D, Ertl G, Bauersachs J (2007) Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56:666–674CrossRefPubMed
37.
Zurück zum Zitat Tuncayengin A, Biri H, Onaran M, Seni I, Tucayengin O, Polat F, Erbas D, Bozkirli I (2003) Cavernosal tissue nitrite, nitrate, malondialdehyde and glutathione levels in diabetic and on diabetic erectile function. Int J Androl 26:250–254CrossRefPubMed Tuncayengin A, Biri H, Onaran M, Seni I, Tucayengin O, Polat F, Erbas D, Bozkirli I (2003) Cavernosal tissue nitrite, nitrate, malondialdehyde and glutathione levels in diabetic and on diabetic erectile function. Int J Androl 26:250–254CrossRefPubMed
38.
Zurück zum Zitat Vincent AM, Russell JW, Low P, Feldman EL (2004) Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25:612–628CrossRefPubMed Vincent AM, Russell JW, Low P, Feldman EL (2004) Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25:612–628CrossRefPubMed
39.
Zurück zum Zitat Vinik AI, Erbas T, Park TS, Stansberry KB, Scanelli JA, Pittenger GL (2001) Dermal neurovascular dysfunction in type 2 diabetes. Diabetes Care 24:1468–1475CrossRefPubMed Vinik AI, Erbas T, Park TS, Stansberry KB, Scanelli JA, Pittenger GL (2001) Dermal neurovascular dysfunction in type 2 diabetes. Diabetes Care 24:1468–1475CrossRefPubMed
40.
Zurück zum Zitat Vinik AI, Maser RE, Mitchell BD, Freeman R (2003) Diabetic autonomic neuropathy. Diabetes Care 26:1553–1579CrossRefPubMed Vinik AI, Maser RE, Mitchell BD, Freeman R (2003) Diabetic autonomic neuropathy. Diabetes Care 26:1553–1579CrossRefPubMed
41.
Zurück zum Zitat Waring WS, McKnight JA, Webb DJ, Maxwell SR (2006) Uric acid restores endothelial function in patients with type I diabetes and regular smokers. Diabetes 55:3127–3132CrossRefPubMed Waring WS, McKnight JA, Webb DJ, Maxwell SR (2006) Uric acid restores endothelial function in patients with type I diabetes and regular smokers. Diabetes 55:3127–3132CrossRefPubMed
42.
Zurück zum Zitat Watkins PJ (1992) Clinical observations and experiments in diabetic neuropathy. Diabetologia 35:2–11CrossRefPubMed Watkins PJ (1992) Clinical observations and experiments in diabetic neuropathy. Diabetologia 35:2–11CrossRefPubMed
43.
Zurück zum Zitat Zeballos GA, Bernstein RD, Thompson CI, Forfia PR, Seyedi N, Shen W, Kaminsi PM, Wolin MS, Hintze TH (1995) Pharmacodynamics of plasma nitrate/nitrite as an indication of nitric oxide formation in conscious dogs. Circulation 91:2982–2988 Zeballos GA, Bernstein RD, Thompson CI, Forfia PR, Seyedi N, Shen W, Kaminsi PM, Wolin MS, Hintze TH (1995) Pharmacodynamics of plasma nitrate/nitrite as an indication of nitric oxide formation in conscious dogs. Circulation 91:2982–2988
Metadaten
Titel
Oxidative stress and autonomic nerve function in early type 1 diabetes
verfasst von
Robert Daniel Hoeldtke
Kimberly D. Bryner
Knox VanDyke
Publikationsdatum
01.02.2011
Verlag
Springer-Verlag
Erschienen in
Clinical Autonomic Research / Ausgabe 1/2011
Print ISSN: 0959-9851
Elektronische ISSN: 1619-1560
DOI
https://doi.org/10.1007/s10286-010-0084-4

Weitere Artikel der Ausgabe 1/2011

Clinical Autonomic Research 1/2011 Zur Ausgabe