274
Views
67
CrossRef citations to date
0
Altmetric
Review

Cardiac autonomic neuropathy in patients with diabetes mellitus: current perspectives

&
Pages 419-434 | Published online: 06 Oct 2017

References

  • International Diabetes Federation IDF Diabetes Atlas 7th ed Brussels IDF 2015
  • National Diabetes Information Clearinghouse DCCT and EDIC: the Diabetes Control and Complications Trial and follow-up study 2008 Available from: https://www.niddk.nih.gov/about-niddk/research-areas/diabetes/dcct-edic-diabetes-control-complications-trial-follow-up-study/Documents/DCCT-EDIC_508.pdf Accessed July 19, 2017
  • No authors listed Epidemiology of Diabetes Interventions and Complications (EDIC): design, implementation, and preliminary results of a long-term follow-up of the Diabetes Control and Complications Trial cohort Diabetes Care 1999 22 1 99 111 10333910
  • Domingueti CP Dusse LM Carvalho MG de Sousa LP Gomes KB Fernandes AP Diabetes mellitus: the linkage between oxidative stress, inflammation, hypercoagulability and vascular complications J Diabetes Complications 2016 30 4 738 745 26781070
  • Balcıoğlu AS Müderrisoğlu H Diabetes and cardiac autonomic neuropathy: clinical manifestations, cardiovascular consequences, diagnosis and treatment World J Diabetes 2015 6 1 80 91 25685280
  • Spallone V Ziegler D Freeman R Cardiovascular autonomic neuropathy in diabetes: clinical impact, assessment, diagnosis, and management Diabetes Metab Res Rev 2011 27 7 639 653 21695768
  • Stables CL Glasser RL Feldman EL Diabetic cardiac autonomic neuropathy: insights from animal models Auton Neurosci 2013 177 2 74 80 23562143
  • Freeman R Diabetic autonomic neuropathy Handb Clin Neurol 2014 126 63 79 25410215
  • Dimitropoulos G Tahrani AA Stevens MJ Cardiac autonomic neuropathy in patients with diabetes mellitus World J Diabetes 2014 5 1 17 39 24567799
  • O’Brien IA Mcfadden JP Corrall RJ The influence of autonomic neuropathy on mortality in insulin-dependent diabetes Q J Med 1991 79 290 495 502 1946930
  • Navarro X Kennedy W Aeppli D Sutherland D Neuropathy and mortality in diabetes: influence of pancreas transplantation Muscle Nerve 1996 19 8 1009 1016 8756167
  • Chen HS Hwu CM Kuo BI Abnormal cardiovascular reflex tests are predictors of mortality in type 2 diabetes mellitus Diabet Med 2001 18 4 268 273 11437856
  • Kempler P Tesfaye S Chaturvedi N Autonomic neuropathy is associated with increased cardiovascular risk factors: the EURODIAB IDDM complications study Diabet Med 2002 19 11 900 909 12421426
  • Low PA Benrud-Larson LM Sletten DM Autonomic symptoms and diabetic neuropathy: a population-based study Diabetes Care 2004 27 12 2942 2947 15562211
  • Pop-Busui R Low PA Waberski BH 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 2009 119 22 2886 2893 19470886
  • Pop-Busui R Cardiac autonomic neuropathy in diabetes: a clinical perspective Diabetes Care 2010 33 2 434 441 20103559
  • Eze C Onwuekwe I Ogunniyi A The frequency and pattern of cardiac autonomic neuropathy (CAN) in type 2 dm patients in a diabetic clinic in Enugu south-east Nigeria Niger J Med 2013 22 1 24 31 23441516
  • Tahrani AA Dubb K Raymond NT Cardiac autonomic neuropathy predicts renal function decline in patients with type 2 diabetes: a cohort study Diabetologia 2014 57 6 1249 1256 24623102
  • Lerner A Bernabé-Ortiz A Ticse R Type 2 diabetes and cardiac autonomic neuropathy screening using dynamic pupillometry Diabet Med 2015 32 11 1470 1478 25761508
  • Mendivil C Kattah W Orduz A Tique C Cárdenas J Patiño J Neuropad for the detection of cardiovascular autonomic neuropathy in patients with type 2 diabetes J Diabetes Complications 2016 30 1 93 98 26525688
  • Razanskaite-Virbickiene D Danyte E Mockeviciene G Dobrovolskiene R Verkauskiene R Zalinkevicius R Can coefficient of variation of time-domain analysis be valuable for detecting cardiovascular autonomic neuropathy in young patients with type 1 diabetes: a case control study BMC Cardiovasc Disord 2017 17 1 34 28103812
  • Menon AS Dixit A Garg MK Girish R Cardiac autonomic neuropathy in patients with type 2 diabetes mellitus at high risk for foot ulcers Indian J Endocrinol Metab 2017 21 2 282 285 28459026
  • Tahrani AA Altaf QA Piya MK Barnett AH Peripheral and autonomic neuropathy in South Asians and white Caucasians with type 2 diabetes mellitus: possible explanations for epidemiological differ-ences J Diabetes Res 2017 2017 1273789 28409160
  • Pop-Busui R Braffett BH Zinman B Cardiovascular autonomic neuropathy and cardiovascular outcomes in the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) study Diabetes Care 2017 40 1 94 100 27803120
  • Dimova R Tankova T Guergueltcheva V Risk factors for autonomic and somatic nerve dysfunction in different stages of glucose tolerance J Diabetes Complications 2017 31 3 537 543 27894750
  • Pfeifer MA Weinberg CR Cook DL Autonomic neural dysfunction in recently diagnosed diabetic subjects Diabetes Care 1984 7 5 447 453 6499637
  • Ziegler D Diabetic cardiovascular autonomic neuropathy: prognosis, diagnosis and treatment Diabetes Metab Rev 1994 10 4 339 383 7796704
  • Giacco F Brownlee M Oxidative stress and diabetic complications Circ Res 2010 107 9 1058 1070 21030723
  • No authors listed The effect of intensive diabetes therapy on measures of autonomic nervous system function in the Diabetes Control and Complications Trial (DCCT) Diabetologia 1998 41 4 416 423 9562345
  • Boulton AJ Vinik AI Arezzo JC Diabetic neuropathies: a statement by the American Diabetes Association Diabetes Care 2005 28 4 956 962 15793206
  • Witte DR Tesfaye S Chaturvedi N Risk factors for cardiac autonomic neuropathy in type 1 diabetes mellitus Diabetologia 2005 48 1 164 171 15619072
  • Chung JO Park SY Cho DH Chung DJ Chung MY Anemia, bilirubin, and cardiovascular autonomic neuropathy in patients with type 2 diabetes Medicine (Baltimore) 2017 96 15 e6586 28403090
  • Valensi P Pariès J Attali JR Cardiac autonomic neuropathy in diabetic patients: influence of diabetes duration, obesity, and microangiopathic complications – the French multicenter study Metabolism 2003 52 7 815 820 12870154
  • Maser RE Lenhard MJ Cardiovascular autonomic neuropathy due to diabetes mellitus: clinical manifestations, consequences, and treatment J Clin Endocrinol Metab 2005 90 10 5896 5903 16014401
  • Ko SH Park SA Cho JH Progression of cardiovascular autonomic dysfunction in patients with type 2 diabetes: a 7-year follow-up study Diabetes Care 2008 31 9 1832 1836 18509202
  • Huang CC Lee JJ Lin TK Diabetic retinopathy is strongly predictive of cardiovascular autonomic neuropathy in type 2 diabetes J Diabetes Res 2016 2016 6090749 26955641
  • Pop-Busui R Evans GW Gerstein HC Effects of cardiac autonomic dysfunction on mortality risk in the Action to Control Cardiovascular Risk in Diabetes (ACCORD) trial Diabetes Care 2010 33 7 1578 1584 20215456
  • Tannus LR Drummond KR Clemente EL da Matta MF Gomes MB Predictors of cardiovascular autonomic neuropathy in patients with type 1 diabetes Front Endocrinol (Lausanne) 2014 5 191 25505446
  • Charles M Fleischer J Witte DR Impact of early detection and treatment of diabetes on the 6-year prevalence of cardiac autonomic neuropathy in people with screen-detected diabetes: ADDITION-Denmark, a cluster-randomised study Diabetologia 2013 56 1 101 108 23064291
  • Abbott CA Chaturvedi N Malik RA Explanations for the lower rates of diabetic neuropathy in Indian Asians versus Europeans Diabetes Care 2010 33 6 1325 1330 20215455
  • Gæde P Oellgaard J Carstensen B Years of life gained by multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: 21 years follow-up on the Steno-2 randomised trial Diabetologia 2016 59 11 2298 2307 27531506
  • Edwards JL Vincent AM Cheng HT Feldman EL Diabetic neuropathy: mechanisms to management Pharmacol Ther 2008 120 1 1 34 18616962
  • Verrotti A Prezioso G Scattoni R Chiarelli F Autonomic neuropathy in diabetes mellitus Front Endocrinol (Lausanne) 2014 5 205 25520703
  • Soriano FG Virág L Szabó C Diabetic endothelial dysfunction: role of reactive oxygen and nitrogen species production and poly(ADP-ribose) polymerase activation J Mol Med 2001 79 8 437 448 11511974
  • Hosseini A Abdollahi M Diabetic neuropathy and oxidative stress: therapeutic perspectives Oxid Med Cell Longev 2013 2013 168039 23738033
  • Adeshara KA Diwan AG Tupe RS Diabetes and complications: cellular signaling pathways, current understanding and targeted therapies Curr Drug Targets 2016 17 11 1309 1328 26648059
  • Vinik AI Erbas T Casellini CM Diabetic cardiac autonomic neuropathy, inflammation and cardiovascular disease J Diabetes Investig 2013 4 1 4 18
  • Polydefkis M Griffin JW McArthur J New insights into diabetic polyneuropathy JAMA 2003 290 10 1371 6 12966130
  • Ziegler D Buchholz S Sohr C Nourooz-Zadeh J Roden M Oxidative stress predicts progression of peripheral and cardiac autonomic nerve dysfunction over 6 years in diabetic patients Acta Diabetol 2015 52 1 65 72 24898524
  • Jaiswal M Fingerlin TE Urbina EM Impact of glycemic control on heart rate variability in youth with type 1 diabetes: the SEARCH CVD study Diabetes Technol Ther 2013 15 12 977 983 24010960
  • Shah MS Brownlee M Molecular and cellular mechanisms of cardiovascular disorders in diabetes Circ Res 2016 118 11 1808 1829 27230643
  • Gibbons C Centi J Vernino S Freeman R Autoimmune autonomic ganglionopathy with reversible cognitive impairment Arch Neurol 2012 69 4 461 466 22158721
  • Gibbons C Freeman R Antibody titers predict clinical features of autoimmune autonomic ganglionopathy Auton Neurosci 2009 146 1–2 8 12 19144572
  • Skärstrand H Dahlin LB Lernmark A Vaziri-Sani F Neuropeptide Y autoantibodies in patients with long-term type 1 and type 2 diabetes and neuropathy J Diabetes Complications 2013 27 6 609 617 23910631
  • Stroud CR Heller SR Ward JD Hardisty CA Weetman AP Analysis of antibodies against components of the autonomic nervous system in diabetes mellitus QJM 1997 90 9 577 585 9349450
  • Granberg V Ejskjaer N Peakman M Sundkvist G Autoantibodies to autonomic nerves associated with cardiac and peripheral autonomic neuropathy Diabetes Care 2005 28 8 1959 1964 16043739
  • Ejskjaer N Arif S Dodds W Prevalence of autoantibodies to autonomic nervous tissue structures in type 1 diabetes mellitus Diabet Med 1999 16 7 544 549 10445828
  • Berntorp K Frid A Alm R Fredrikson GN Sjöberg K Ohlsson B Antibodies against gonadotropin-releasing hormone (GnRH) in patients with diabetes mellitus is associated with lower body weight and autonomic neuropathy BMC Res Notes 2013 6 329 23958111
  • Zanone MM Raviolo A Coppo E Association of autoimmunity to autonomic nervous structures with nerve function in patients with type 1 diabetes: a 16-year prospective study Diabetes Care 2014 37 4 1108 1115 24550215
  • Politi C Ciccacci C D’Amato C Novelli G Borgiani P Spallone V Recent advances in exploring the genetic susceptibility to diabetic neuropathy Diabetes Res Clin Pract 2016 120 198 208 27596057
  • Ciccacci C Morganti R Di Fusco D Common polymorphisms in MIR146a, MIR128a and MIR27a genes contribute to neuropathy susceptibility in type 2 diabetes Acta Diabetol 2014 51 4 663 671 24682535
  • Osztovits J Horváth T Littvay L Effects of genetic vs. environmental factors on cardiovascular autonomic function: a twin study Diabet Med 2011 28 10 1241 8 21679234
  • Tahrani AA Obstructive sleep apnoea in diabetes: does it matter? Diab Vasc Dis Res Epub 2017 6 1
  • Tahrani AA Ali A Raymond NT Obstructive sleep apnea and diabetic neuropathy: a novel association in patients with type 2 diabetes Am J Respir Crit Care Med 2012 186 5 434 441 22723291
  • Janovsky CC Rolim LC De Sá JR Cardiovascular autonomic neuropathy contributes to sleep apnea in young and lean type 1 diabetes mellitus patients Front Endocrinol (Lausanne) 2014 5 119 25157241
  • Stevens M Ali A Dubb K Begum S Piya M Tahrani A Obstructive sleep apnoea is associated with cardiac autonomic abnormalities in patients with type 2 diabetes Diabet Med 2014 31 37 Available from: https://insights.ovid.com/diabetic-medicine/diame/2014/03/001/obstructive-sleep-apnoea-associated-cardiac/110/00003135 Accessed September 21, 2017
  • Altaf Q Ali A Tahrani A The impact of obstructive sleep apnoea on cardiac autonomic neuropathy in patients with type 2 diabetes: a longitudinal study 2017 Available from: http://www.neurodiab2017.com/Portals/0/Docs/abstract_book.pdf Accessed August 31, 2017
  • Theilade S Lyngbaek S Hansen TW Soluble urokinase plasminogen activator receptor levels are elevated and associated with complications in patients with type 1 diabetes J Intern Med 2015 277 3 362 371 24830873
  • Chung T Prasad K Lloyd TE Peripheral neuropathy: clinical and electrophysiological considerations Neuroimaging Clin N Am 2014 24 1 49 65 24210312
  • Albers JW Pop-Busui R Diabetic neuropathy: mechanisms, emerging treatments, and subtypes Curr Neurol Neurosci Rep 2014 14 8 473 24954624
  • Vinik AI Freeman R Erbas T Diabetic autonomic neuropathy Semin Neurol 2003 23 4 365 372 15088257
  • Pop-Busui R What do we know and we do not know about cardiovascular autonomic neuropathy in diabetes J Cardiovasc Transl Res 2012 5 4 463 478 22644723
  • Hillis G Woodward M Rodgers A Resting heart rate and the risk of death and cardiovascular complications in patients with type 2 diabetes mellitus Diabetologia 2012 55 5 1283 1290 22286552
  • Vinik AI Ziegler D Diabetic cardiovascular autonomic neuropathy Circulation 2007 115 3 387 397 17242296
  • No authors listed Consensus statement on the definition of orthostatic hypotension, pure autonomic failure, and multiple system atrophy Neurology 1996 46 5 1470 8628505
  • Kuehl M Stevens MJ Cardiovascular autonomic neuropathies as complications of diabetes mellitus Nat Rev Endocrinol 2012 8 7 405 416 22371159
  • Ninkovic VM Ninkovic SM Miloradovic V Prevalence and risk factors for prolonged QT interval and QT dispersion in patients with type 2 diabetes Acta Diabetol 2016 53 5 737 744 27107571
  • Veglio M Chinaglia A Cavallo-Perin P QT interval, cardiovascular risk factors and risk of death in diabetes J Endocrinol Invest 2004 27 2 175 181 15129815
  • Sargin H Ozisik M Ozisik NC The prevalence of silent ischemia in Turkish patients with type 2 diabetes mellitus Tohoku J Exp Med 2005 205 4 351 355 15750331
  • Deluca AJ Kaplan S Aronow WS Comparison of prevalence of unrecognized myocardial infarction and of silent myocardial ischemia detected by a treadmill exercise sestamibi stress test in patients with versus without diabetes mellitus Am J Cardiol 2006 98 8 1045 1046 17027568
  • Wackers FJ Young LH Inzucchi SE Detection of silent myocardial ischemia in asymptomatic diabetic subjects: the DIAD study Diabetes Care 2004 27 8 1954 1961 15277423
  • Deluca AJ Saulle LN Aronow WS Ravipati G Weiss MB Prevalence of silent myocardial ischemia in persons with diabetes mellitus or impaired glucose tolerance and association of hemoglobin A1c with prevalence of silent myocardial ischemia Am J Cardiol 2005 95 12 1472 1474 15950575
  • Ambepityia G Kopelman PG Ingram D Swash M Mills PG Timmis AD Exertional myocardial ischemia in diabetes: a quantitative analysis of anginal perceptual threshold and the influence of autonomic function J Am Coll Cardiol 1990 15 1 72 77 2295745
  • Valensi P Sachs RN Harfouche B Predictive value of cardiac autonomic neuropathy in diabetic patients with or without silent myocardial ischemia Diabetes Care 2001 24 2 339 343 11213889
  • Töyry JP Niskanen LK Länsimies EA Partanen KP Uusitupa MI Autonomic neuropathy predicts the development of stroke in patients with non-insulin-dependent diabetes mellitus Stroke 1996 27 8 1316 1318 8711794
  • Cohen JA Estacio RO Lundgren RA Esler AL Schrier RW Diabetic autonomic neuropathy is associated with an increased incidence of strokes Auton Neurosci 2003 108 1–2 73 78 14614967
  • Ko SH Song KH Park SA Cardiovascular autonomic dysfunction predicts acute ischaemic stroke in patients with type 2 diabetes mellitus: a 7-year follow-up study Diabet Med 2008 25 10 1171 1177 19046195
  • Hayat SA Patel B Khattar RS Malik RA Diabetic cardiomyopathy: mechanisms, diagnosis and treatment Clin Sci 2004 107 6 539 557 15341511
  • Boudina S Abel ED Diabetic cardiomyopathy, causes and effects Rev Endocr Metab Disord 2010 11 1 31 39 20180026
  • Vinik AI Erbas T Diabetic autonomic neuropathy Handb Clin Neurol 2013 117 279 294 24095132
  • Oakley I Emond L Diabetic cardiac autonomic neuropathy and anesthetic management: review of the literature AANA J 2011 79 6 473 479 22400413
  • Burgos LG Ebert TJ Asiddao C Increased intraoperative cardiovascular morbidity in diabetics with autonomic neuropathy Anesthesiology 1989 70 4 591 597 2929996
  • Latson TW Ashmore TH Reinhart DJ Klein KW Giesecke AH Autonomic reflex dysfunction in patients presenting for elective surgery is associated with hypotension after anesthesia induction Anesthesiology 1994 80 2 326 337 8311315
  • Yun JS Cha SA Lim TS Cardiovascular autonomic dysfunction predicts diabetic foot ulcers in patients with type 2 diabetes without diabetic polyneuropathy Medicine (Baltimore) 2016 95 12 e3128 27015188
  • Chahal S Vohra K Syngle A Association of sudomotor function with peripheral artery disease in type 2 diabetes Neurol Sci 2017 38 1 151 156 27783183
  • Yun JS Ahn YB Song KH The association between abnormal heart rate variability and new onset of chronic kidney disease in patients with type 2 diabetes: a ten-year follow-up study Diabetes Res Clin Pract 2015 108 1 31 37 25656759
  • Forsén A Kangro M Sterner G A 14-year prospective study of autonomic nerve function in type 1 diabetic patients: association with nephropathy Diabet Med 2004 21 8 852 858 15270788
  • 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 2003 26 6 1895 1901 12766130
  • Soedamah-Muthu SS Chaturvedi N Witte DR Relationship between risk factors and mortality in type 1 diabetic patients in Europe: the EURODIAB Prospective Complications Study (PCS) Diabetes Care 2008 31 7 1360 1366 18375412
  • Ewing DJ Campbell IW Clarke BF Assessment of cardiovascular effects in diabetic autonomic neuropathy and prognostic implications Ann Intern Med 1980 92 2 Pt 2 308 311 7356219
  • Pafili K Trypsianis G Papzoglou D Maltezos E Papanas N Simplified diagnosis of cardiovascular autonomic neuropathy in type 2 diabetes using Ewing’s battery Rev Diabet Stud 2015 12 1–2 213 219 26676669
  • Ziegler D Laux G Dannehl K Assessment of cardiovascular autonomic function: age-related normal ranges and reproducibility of spectral analysis, vector analysis, and standard tests of heart rate variation and blood pressure responses Diabet Med 1992 9 2 166 175 1563252
  • Pfeifer MA Cook D Brodsky J Quantitative evaluation of cardiac parasympathetic activity in normal and diabetic man Diabetes 1982 31 4 Pt 1 339 345 7152130
  • Sandroni P Benarroch EE Low PA Pharmacological dissection of components of the Valsalva maneuver in adrenergic failure J Appl Physiol (1985) 1991 71 4 1563 1567 1757382
  • Ewing DJ Campbell IW Murray A Neilson JM Clarke BF Immediate heart-rate response to standing: simple test for autonomic neuropathy in diabetes Br Med J 1978 1 6106 145 147 620228
  • Borowik E Grabowicz W Grycewicz T Lubiński A Clinical usefulness of baroreflex sensitivity test in the detection of cardiovascular autonomic neuropathy in patients with type 2 diabetes mellitus Pol Merkur Lekarski 2015 39 233 277 280 26637091
  • Zygmunt A Stanczyk J Methods of evaluation of autonomic nervous system function Arch Med Sci 2010 6 1 11 18 22371714
  • Shrivastava S Sukla P Shrivastava P Rao N Assessment of the cardiac autonomic neuropathy among the known diabetics and age-matched controls using noninvasive cardiovascular reflex tests in a south-Indian population: a case-control study Avicenna J Med 2016 6 3 81 85 27390670
  • Turker Y Aslantas Y Aydin Y Heart rate variability and heart rate recovery in patients with type 1 diabetes mellitus Acta Cardiol 2013 68 2 145 150 23705556
  • Montano N Ruscone TG Porta A Lombardi F Pagani M Malliani A Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt Circulation 1994 90 4 1826 1831 7923668
  • La Rovere M Maestri R Pinna G Baroreflex sensitivity assessment: latest advances and strategies Eur Cardiol 2011 7 2 89 92
  • Kamińska A Tafil-Klawe M Smietanowski M Spontaneous baroreflex sensitivity in subjects with type 1 diabetes with and without cardiovascular autonomic neuropathy Endokrynol Pol 2008 59 5 398 402 18979450
  • Svačinová J Honzíková N Krtička A Tonhajzerová I Javorka K Javorka M Diagnostic significance of a mild decrease of baroreflex sensitivity with respect to heart rate in type 1 diabetes mellitus Physiol Res 2013 62 6 605 613 23869895
  • Messmer EM Schmid-Tannwald C Zapp D Kampik A In vivo confocal microscopy of corneal small fiber damage in diabetes mellitus Graefes Arch Clin Exp Ophthalmol 2010 248 9 1307 1312 20490534
  • Tavakoli M Begum P McLaughlin J Malik R Corneal confocal microscopy for the diagnosis of diabetic autonomic neuropathy Muscle Nerve 2015 52 3 363 370 25556884
  • Maddaloni E Sabatino F Del Toro R In vivo corneal confocal microscopy as a novel non-invasive tool to investigate cardiac autonomic neuropathy in type 1 diabetes Diabet Med 2014 32 2 262 266 25251450
  • Buse JB Ginsberg HN Bakris GL Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association Circulation 2007 115 1 114 126 17192512
  • Howorka K Pumprla J Haber P Koller-Strametz J Mondrzyk J Schabmann A Effects of physical training on heart rate variability in diabetic patients with various degrees of cardiovascular autonomic neuropathy Cardiovasc Res 1997 34 1 206 214 9217892
  • Soares-Miranda L Sandercock G Vale S Metabolic syndrome, physical activity and cardiac autonomic function Diabetes Metab Res Rev 2012 28 4 363 369 22238216
  • Motooka M Koike H Yokoyama T Kennedy NL Effect of dog-walking on autonomic nervous activity in senior citizens Med J Aust 2006 184 2 60 63 16411869
  • Carnethon MR Prineas RJ Temprosa M The association among autonomic nervous system function, incident diabetes, and intervention arm in the Diabetes Prevention Program Diabetes Care 2006 29 4 914 919 16567837
  • Voulgari C Pagoni S Vinik A Poirier P Exercise improves cardiac autonomic function in obesity and diabetes Metab Clin Exp 2013 62 5 609 621 23084034
  • Esposito P Mereu R De Barbieri G Trained breathing-induced oxygenation acutely reverses cardiovascular autonomic dysfunction in patients with type 2 diabetes and renal disease Acta Diabetol 2016 53 2 217 226 25956276
  • Ceriello A Esposito K Ihnat M Thorpe J Giugliano D Long-term glycemic control influences the long-lasting effect of hyperglycemia on endothelial function in type 1 diabetes J Clin Endocrinol Metab 2009 94 8 2751 2756 19491221
  • Jaiswal M Urbina EM Wadwa RP Reduced heart rate variability among youth with type 1 diabetes: the SEARCH CVD study Diabetes Care 2013 36 1 157 162 22961570
  • Azad N Emanuele NV Abraira C The effects of intensive glycemic control on neuropathy in the VA cooperative study on type II diabetes mellitus (VA CSDM) J Diabetes Complications 1999 13 5–6 307 313 10765007
  • Gæde P Vedel P Parving HH Pedersen O Intensified multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: the Steno type 2 randomised study Lancet 1999 353 9153 617 622 10030326
  • Ziegler D Schatz H Conrad F Gries FA Ulrich H Reichel G 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). Deutsche Kardiale Autonome Neuropathie Diabetes Care 1997 20 3 369 73 9051389
  • Manzella D Barbieri M Ragno E Paolisso G Chronic administration of pharmacologic doses of vitamin E improves the cardiac autonomic nervous system in patients with type 2 diabetes Am J Clin Nutr 2001 73 6 1052 1057 11382659
  • Pop-Busui R Stevens MJ Raffel DM 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 2013 56 8 1835 1844 23740194
  • Johansson BL Borg K Fernqvist-Forbes E Kernell A Odergren T Wahren J Beneficial effects of C-peptide on incipient nephropathy and neuropathy in patients with type 1 diabetes mellitus Diabet Med 2000 17 3 181 189 10784221
  • Hu X Li S Yang G Liu H Boden G Li L Efficacy and safety of aldose reductase inhibitor for the treatment of diabetic cardiovascular autonomic neuropathy: systematic review and meta-analysis PLoS One 2014 9 2 e87096 24533052
  • Johnson BF Nesto RW Pfeifer MA Cardiac abnormalities in diabetic patients with neuropathy: effects of aldose reductase inhibitor administration Diabetes Care 2004 27 2 448 454 14747227
  • Athyros VG Didangelos TP Karamitsos DT Papageorgiou AA Boudoulas H Kontopoulos AG Long-term effect of converting enzyme inhibition on circadian sympathetic and parasympathetic modulation in patients with diabetic autonomic neuropathy Acta Cardiol 1998 53 4 201 209 9842405
  • Ziegler D Low PA Freeman R Tritschler H Vinik AI Predictors of improvement and progression of diabetic polyneuropathy following treatment with α-lipoic acid for 4 years in the NATHAN 1 trial J Diabetes Complications 2016 30 2 350 356 26651260
  • Baruch L Anand I Cohen IS Ziesche S Judd D Cohn JN Augmented short- and long-term hemodynamic and hormonal effects of an angiotensin receptor blocker added to angiotensin converting enzyme inhibitor therapy in patients with heart failure Circulation 1999 99 20 2658 2664 10338459
  • Ebbehøj E Poulsen PL Hansen KW Knudsen ST Mølgaard H Mogensen CE Effects on heart rate variability of metoprolol supplementary to ongoing ACE-inhibitor treatment in type I diabetic patients with abnormal albuminuria Diabetologia 2002 45 7 965 975 12136395
  • Lampert R Ickovics JR Viscoli CJ Horwitz RI Lee FA Effects of propranolol on recovery of heart rate variability following acute myocardial infarction and relation to outcome in the Beta-Blocker Heart Attack Trial Am J Cardiol 2003 91 2 137 142 12521623
  • Shibao C Lipsitz LA Biaggioni I ASH position paper: evaluation and treatment of orthostatic hypotension J Clin Hypertens (Greenwich) 2013 15 3 147 153 23458585