Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments

Solomon Tesfaye, Andrew J M Boulton, Peter J Dyck, Roy Freeman, Michael Horowitz, Peter Kempler, Giuseppe Lauria, Rayaz A Malik, Vincenza Spallone, Aaron Vinik, Luciano Bernardi, Paul Valensi, Toronto Diabetic Neuropathy Expert Group, James W Albers, Gerard Amarenco, Henning Anderson, Joe Arezzo, Misha-Miroslav Backonja, Luciano Bernardi, Geert-Jan Biessels, Andrew J M Boulton, Vera Bril, Norman Cameron, Mary Cotter, Peter J Dyck, John England, Eva Feldman, Roy Freeman, Simona Frontoni, Jannik Hilsted, Michael Horowitz, Peter Kempler, Giuseppe Lauria, Philip Low, Rayaz Malik, Peter C O'Brien, Rodica Pop-Busui, Bruce Perkins, Gerry Rayman, James Russell, Søren Sindrup, Gordon Smith, Vincenza Spallone, Martin Stevens, Solomon Tesfaye, Paul Valensi, Tamas Varkonyi, Aristides Veves, Loretta Vileikyte, Aaron Vinik, Dan Ziegler, Doug Zochodne, Teresa Jones, Solomon Tesfaye, Andrew J M Boulton, Peter J Dyck, Roy Freeman, Michael Horowitz, Peter Kempler, Giuseppe Lauria, Rayaz A Malik, Vincenza Spallone, Aaron Vinik, Luciano Bernardi, Paul Valensi, Toronto Diabetic Neuropathy Expert Group, James W Albers, Gerard Amarenco, Henning Anderson, Joe Arezzo, Misha-Miroslav Backonja, Luciano Bernardi, Geert-Jan Biessels, Andrew J M Boulton, Vera Bril, Norman Cameron, Mary Cotter, Peter J Dyck, John England, Eva Feldman, Roy Freeman, Simona Frontoni, Jannik Hilsted, Michael Horowitz, Peter Kempler, Giuseppe Lauria, Philip Low, Rayaz Malik, Peter C O'Brien, Rodica Pop-Busui, Bruce Perkins, Gerry Rayman, James Russell, Søren Sindrup, Gordon Smith, Vincenza Spallone, Martin Stevens, Solomon Tesfaye, Paul Valensi, Tamas Varkonyi, Aristides Veves, Loretta Vileikyte, Aaron Vinik, Dan Ziegler, Doug Zochodne, Teresa Jones

Abstract

Preceding the joint meeting of the 19th annual Diabetic Neuropathy Study Group of the European Association for the Study of Diabetes (NEURODIAB) and the 8th International Symposium on Diabetic Neuropathy in Toronto, Canada, 13-18 October 2009, expert panels were convened to provide updates on classification, definitions, diagnostic criteria, and treatments of diabetic peripheral neuropathies (DPNs), autonomic neuropathy, painful DPNs, and structural alterations in DPNs.

References

    1. Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, Wilson DM, O'Brien PC, Melton LJ, 3rd, Service FJ: The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology 1993;43:817–824
    1. Llewelyn JG, Tomlinson DR, Thomas PK: Diabetic Neuropathies. In Peripheral Neuropathy. 4th ed Dyck PJ, Thomas PK: Eds. Philadelphia, Elsevier; 2005, p. 1951–1992
    1. Thomas PK: Classification, differential diagnosis and staging of diabetic peripheral neuropathy. Diabetes 1997;46(Suppl. 2):S54–S57
    1. Boulton AJ, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D: American Diabetes Association Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care 2005;28:956–962
    1. Dyck PJ, Davies JL, Wilson DM, Service FJ, Melton LJ, 3rd, O'Brien PC: Risk factors for severity of diabetic polyneuropathy: intensive longitudinal assessment of the Rochester Diabetic Neuropathy Study cohort. Diabetes Care 1999;22:1479–1486
    1. Tesfaye S, Chaturvedi N, Eaton SE, Ward JD, Manes C, Ionescu-Tirgoviste C, Witte DR, Fuller JH: EURODIAB Prospective Complications Study Group Vascular risk factors and diabetic neuropathy. N Engl J Med 2005;352:341–350
    1. Dyck PJ, Davies JL, Clark VM, Litchy WJ, Dyck PJ, Klein CJ, Rizza RA, Pach JM, Klein R, Larson TS, Melton LJ, 3rd, O'Brien PC: Modeling chronic glycemic exposure variables as correlates and predictors of microvascular complications of diabetes. Diabetes Care 2006;29:2282–2288
    1. Giannini C, Dyck PJ: Ultrastructural morphometric abnormalities of sural nerve endoneurial microvessels in diabetes mellitus. Ann Neurol 1994;36:408–415
    1. Archer AG, Watkins PJ, Thomas PK, Sharma AK, Payan J: The natural history of acute painful neuropathy in diabetes mellitus. J Neurol Neurosurg Psychiatry 1983;46:491–499
    1. Singleton JR, Smith AG, Bromberg MB: Painful sensory polyneuropathy associated with impaired glucose tolerance. Muscle Nerve 2001;24:1225–1228
    1. American Diabetes Association and American Academy of Neurology Report and recommendations of the San Antonio conference on diabetic neuropathy (Consensus Statement). Diabetes Care 1988;11:592–597
    1. England JD, Gronseth GS, Franklin G, Miller RG, Asbury AK, Carter GT, Cohen JA, Fisher MA, Howard JF, Kinsella LJ, Latov N, Lewis RA, Low PA, Sumner AJ: American Academy of Neurology, American Association of Electrodiagnostic Medicine, American Academy of Physical Medicine and Rehabilitation Distal symmetric polyneuropathy: a definition for clinical research: report of the American Academy of Neurology, the American Association of Electrodiagnostic Medicine, and the American Academy of Physical Medicine and Rehabilitation. Neurology 2005;64:199–207
    1. Apfel SC, Asbury AK, Bril V, Burns TM, Campbell JN, Chalk CH, Dyck PJ, Dyck PJ, Feldman EL, Fields HL, Grant IA, Griffin JW, Klein CJ, Lindblom U, Litchy WJ, Low PA, Melanson M, Mendell JR, Merren MD, O'Brien PC, Rendell M, Rizza RA, Service FJ, Thomas PK, Walk D, Wang AK, Wessel K, Windebank AJ, Ziegler D, Zochodne DW: Ad Hoc Panel on Endpoints for Diabetic Neuropathy Trials Positive neuropathic sensory symptoms as endpoints in diabetic neuropathy trials. J Neurol Sci 2001;189:3–5
    1. Dyck PJ, Overland CJ, Low PA, Litchy WJ, Davies JL, Dyck PJ, O'Brien PC: Cl vs. NPhys Trial Investigators Albers JW, Andersen H, Bolton CF, England JD, Klein CJ, Llewelyn JG, Mauermann ML, Russell JW, Singer W, Smith AG, Tesfaye S, Vella A: Signs and symptoms versus nerve conduction studies to diagnose diabetic sensorimotor polyneuropathy: CI vs. NPhys trial. Muscle Nerve 2010;42:157–164
    1. Dyck PJ: Detection, characterization, and staging of polyneuropathy: assessed in diabetics. Muscle Nerve 1988;11:21–32
    1. Treede RD, Jensen TS, Campbell JN, Cruccu G, Dostrovsky JO, Griffin JW, Hansson P, Hughes R, Nurmikko T, Serra J: Neuropathic pain: redefinition and a grading system for clinical and research purposes. Neurology 2008;70:1630–1635
    1. Boulton AJ, Malik RA, Arezzo JC, Sosenko JM: Diabetic somatic neuropathies. Diabetes Care 2004;27:1458–1486
    1. Cruccu G, Anand P, Attal N, Garcia-Larrea L, Haanpää M, Jørum E, Serra J, Jensen TS: EFNS guidelines on neuropathic pain assessment. Eur J Neurol 2004March;11:153–162
    1. Vinik EJ, Hayes RP, Oglesby A, Bastyr E, Barlow P, Ford-Molvik SL, Vinik AI. The development and validation of the Norfolk QOL-DN, a new measure of patients' perception of the effects of diabetes and diabetic neuropathy. Diabetes Technol Ther 2005;7:497–508
    1. Tesfaye S: Advances in the management of diabetic peripheral neuropathy. Curr Opin Support Palliat Care 2009;3:136–143
    1. Ziegler D, Nowak H, Kempler P, Vargha P, Low PA: Treatment of symptomatic diabetic polyneuropathy with the antioxidant alpha-lipoic acid: a meta-analysis. Diabet Med 2004;21:114–121
    1. Tesfaye S, Watt J, Benbow SJ, Pang KA, Miles J, MacFarlane IA: Electrical spinal-cord stimulation for painful diabetic peripheral neuropathy. Lancet 1996;348:1698–1701
    1. Jensen TS, Backonja MM, Hernández Jiménez S, Tesfaye S, Valensi P, Ziegler D: New perspectives on the management of diabetic peripheral neuropathic pain. Diab Vasc Dis Res 2006;3:108–119
    1. McQuay HJ, Tramèr M, Nye BA, Carroll D, Wiffen PJ, Moore RA: A systematic review of antidepressants in neuropathic pain. Pain 1996;68:217–227
    1. Freeman R, Durso-Decruz E, Emir B: Efficacy, safety, and tolerability of pregabalin treatment for painful diabetic peripheral neuropathy: findings from seven randomized, controlled trials across a range of doses. Diabetes Care 2008;31:1448–1454
    1. Lunn MP, Hughes RA, Wiffen PJ: Duloxetine for treating painful neuropathy or chronic pain. Cochrane Database Syst Rev 2009;7:CD007115.
    1. Selvarajah D, Gandhi R, Emery CJ, Tesfaye S: Randomized placebo-controlled double-blind clinical trial of cannabis-based medicinal product (Sativex) in painful diabetic neuropathy: depression is a major confounding factor. Diabetes Care 2010;33:128–130
    1. Baron R, Mayoral V, Leijon G, Binder A, Steigerwald I, Serpell M: 5% lidocaine medicated plaster versus pregabalin in post-herpetic neuralgia and diabetic polyneuropathy: an open-label, non-inferiority two-stage RCT study. Curr Med Res Opin 2009;25:1663–1676
    1. Low PA, Benrud-Larson LM, Sletten DM, Opfer-Gehrking TL, Weigand SD, O'Brien PC, Suarez GA, Dyck PJ: Autonomic symptoms and diabetic neuropathy: a population-based study. Diabetes Care 2004;27:2942–2947
    1. Valensi P, Pariès J, Attali JR: French Group for Research and Study of Diabetic Neuropathy Cardiac autonomic neuropathy in diabetic patients: influence of diabetes duration, obesity, and microangiopathic complications–the French multicenter study. Metabolism 2003;52:815–820
    1. Witte DR, Tesfaye S, Chaturvedi N, Eaton SE, Kempler P, Fuller JH: EURODIAB Prospective Complications Study Group Risk factors for cardiac autonomic neuropathy in type 1 diabetes mellitus. Diabetologia 2005;48:164–171
    1. Pop-Busui R, Low PA, Waberski BH, Martin CL, Albers JW, Feldman EL, Sommer C, Cleary PA, Lachin JM, Herman WH: DCCT/EDIC Research Group 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;119:2886–2893
    1. Gaede 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;353:617–622
    1. Vinik AI, Ziegler D: Diabetic cardiovascular autonomic neuropathy. Circulation 2007;115:387–397
    1. American Academy of Neurology Assessment: clinical autonomic testing report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 1996;46:873–880
    1. England JD, Gronseth GS, Franklin G, Carter GT, Kinsella LJ, Cohen JA, Asbury AK, Szigeti K, Lupski JR, Latov N, Lewis RA, Low PA, Fisher MA, Herrmann DN, Howard JF, Jr, Lauria G, Miller RG, Polydefkis M, Sumner AJ: American Academy of Neurology Practice parameter: evaluation of distal symmetric polyneuropathy: role of autonomic testing, nerve biopsy, and skin biopsy (an evidence-based review): report of the American Academy of Neurology, American Association of Neuromuscular and Electrodiagnostic Medicine, and American Academy of Physical Medicine and Rehabilitation. Neurology 2009;72:177–184
    1. Spallone V, Maiello MR, Morganti R, Mandica S, Frajese G: Usefulness of ambulatory blood pressure monitoring in predicting the presence of autonomic neuropathy in type I diabetic patients. J Hum Hypertens 2007;21:381–386
    1. Ziegler D, Zentai CP, Perz S, Rathmann W, Haastert B, Döring A, Meisinger C: KORA Study Group Prediction of mortality using measures of cardiac autonomic dysfunction in the diabetic and nondiabetic population: the MONICA/KORA Augsburg Cohort Study. Diabetes Care 2008;31:556–561
    1. Bernardi L: Clinical evaluation of arterial baroreflex activity in diabetes. Diabetes Nutr Metab 2000;13:331–340
    1. Stevens MJ, Raffel DM, Allman KC, Dayanikli F, Ficaro E, Sandford T, Wieland DM, Pfeifer MA, Schwaiger M: Cardiac sympathetic dysinnervation in diabetes: implications for enhanced cardiovascular risk. Circulation 1998;98:961–968
    1. Rayner CK, Horowitz M: Gastrointestinal motility and glycemic control in diabetes: the chicken and the egg revisited? J Clin Invest 2006;116:299–302
    1. Horowitz M, Maddox AF, Wishart JM, Harding PE, Chatterton BE, Shearman DJ: Relationships between oesophageal transit and solid and liquid gastric emptying in diabetes mellitus. Eur J Nucl Med 1991;18:229–234
    1. Jones KL, Russo A, Stevens JE, Wishart JM, Berry MK, Horowitz M: Predictors of delayed gastric emptying in diabetes. Diabetes Care 2001;24:1264–1269
    1. Horowitz M, Jones KL, Rayner CK, Read NW: ‘Gastric’ hypoglycaemia: an important concept in diabetes management. Neurogastroenterol Motil 2006;18:405–407
    1. Parkman HP, Hasler WL, Fisher RS: American Gastroenterological Association American Gastroenterological Association technical review on the diagnosis and treatment of gastroparesis. Gastroenterology 2004;127:1592–1622
    1. Malavige LS, Levy JC: Erectile dysfunction in diabetes mellitus. J Sex Med 2009;6:1232–1247
    1. Várkonyi T, Kempler P: Erectile Dysfunction. In Diabetes in Old Age. 3rd ed Sinclair A: Ed. New York, John Wiley & Sons, 2009, p. 149–164
    1. Gazzaruso C, Giordanetti S, De Amici E, Bertone G, Falcone C, Geroldi D, Fratino P, Solerte SB, Garzaniti A: Relationship between erectile dysfunction and silent myocardial ischemia in apparently uncomplicated type 2 diabetic patients. Circulation 2004;110:22–26
    1. Hamdan FB, Al-Matubsi HY: Assessment of erectile dysfunction in diabetic patients. Int J Androl 2009;32:176–185
    1. Hill SR, Fayyad AM, Jones GR: Diabetes mellitus and female lower urinary tract symptoms: a review. Neurourol Urodyn 2008;27:362–367
    1. Hunter KF, Moore KN: DM-associated bladder dysfunction in the older adult. Ger Nursing 2003;24:138–145
    1. Appell RA, Whiteside HV: DM and Other Peripheral Neuropathies Affecting Lower Urinary Tract Function. In Clinical Neuro-Urology. Krane RJ, Siroky MB: Eds. Boston, Little, Brown, 1991, p. 365–375
    1. Tentolouris N, Marinou K, Kokotis P, Karanti A, Diakoumopoulou E, Katsilambros N: Sudomotor dysfunction is associated with foot ulceration in diabetes. Diabet Med 2009;26:302–305
    1. Stewart JD, Low PA, Fealey RD: Distal small fiber neuropathy: results of tests of sweating and autonomic cardiovascular reflexes. Muscle Nerve 1992;15:661–665
    1. Liatis S, Marinou K, Tentolouris N, Pagoni S, Katsilambros N: Usefulness of a new indicator test for the diagnosis of peripheral and autonomic neuropathy in patients with diabetes mellitus. Diabet Med 2007;24:1375–1380
    1. Gibbons CH, Illigens BM, Centi J, Freeman R: QDIRT: quantitative direct and indirect test of sudomotor function. Neurology 2008;70:2299–2304
    1. Malik RA, Tesfaye S, Newrick PG, Walker D, Rajbhandari SM, Siddique I, Sharma AK, Boulton AJ, King RH, Thomas PK, Ward JD: Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia 2005;48:578–585
    1. Joint Task Force of the EFNS and the PNS. European Federation of Neurological Societies/Peripheral Nerve Society Guideline on the use of skin biopsy in the diagnosis of small fiber neuropathy. Report of a joint task force of the European Federation of Neurological Societies and the Peripheral Nerve Society. J Peripher Nerv Syst 2010;15:79–92
    1. Vlcková-Moravcová E, Bednarík J, Dusek L, Toyka KV, Sommer C: Diagnostic validity of epidermal nerve fiber densities in painful sensory neuropathies. Muscle Nerve 2008;37:50–60
    1. Nebuchennykh M, Løseth S, Lindal S, Mellgren SI: The value of skin biopsy with recording of intraepidermal nerve fiber density and quantitative sensory testing in the assessment of small fiber involvement in patients with different causes of polyneuropathy. J Neurol 2009;256:1067–1075
    1. Shun CT, Chang YC, Wu HP, Hsieh SC, Lin WM, Lin YH, Tai TY, Hsieh ST: Skin denervation in type 2 diabetes: correlations with diabetic duration and functional impairments. Brain 2004;127:1593–1605
    1. Løseth S, Stålberg E, Jorde R, Mellgren SI: Early diabetic neuropathy: thermal thresholds and intraepidermal nerve fibre density in patients with normal nerve conduction studies. J Neurol 2008;255:1197–1202
    1. Quattrini C, Tavakoli M, Jeziorska M, Kallinikos P, Tesfaye S, Finnigan J, Marshall A, Boulton AJ, Efron N, Malik RA: Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 2007;56:2148–2154
    1. Sorensen L, Molyneaux L, Yue DK: The relationship among pain, sensory loss, and small nerve fibers in diabetes. Diabetes Care 2006;29:883–887
    1. Smith AG, Russell J, Feldman EL, Goldstein J, Peltier A, Smith S, Hamwi J, Pollari D, Bixby B, Howard J, Singleton JR: Lifestyle intervention for pre-diabetic neuropathy. Diabetes Care 2006;29:1294–1299
    1. Gibbons CH, Illigens BM, Wang N, Freeman R: Quantification of sweat gland innervation: a clinical-pathologic correlation. Neurology 2009;72:1479–1486
    1. Mehra S, Tavakoli M, Kallinikos PA, Efron N, Boulton AJ, Augustine T, Malik RA: Corneal confocal microscopy detects early nerve regeneration after pancreas transplantation in patients with type 1 diabetes. Diabetes Care 2007;30:2608–2612
    1. Caselli A, Rich J, Hanane T, Uccioli L, Veves A: Role of C-nociceptive fibers in the nerve axon reflex-related vasodilation in diabetes. Neurology 2003;60:297–300
    1. Krishnan ST, Rayman G: The LDIflare: a novel test of C-fiber function demonstrates early neuropathy in type 2 diabetes. Diabetes Care 2004;27:2930–2935

Source: PubMed

3
Suscribir