Display options
Share it on

Acta Diabetol. 2021 Jul 02; doi: 10.1007/s00592-021-01767-x. Epub 2021 Jul 02.

Redefining distal symmetrical polyneuropathy features in type 1 diabetes: a systematic review.

Acta diabetologica

Eleonora Galosi, Xiaoli Hu, Nivatha Michael, Jens Randel Nyengaard, Andrea Truini, Páll Karlsson

Affiliations

  1. Department of Human Neuroscience, Sapienza University, Rome, Italy. [email protected].
  2. Core Center for Molecular Morphology, Section for Stereology and Microscopy, Aarhus University, Aarhus, Denmark.
  3. Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
  4. Department of Pathology, Aarhus University Hospital, Aarhus, Denmark.
  5. Department of Human Neuroscience, Sapienza University, Rome, Italy.
  6. Department of Clinical Medicine, Danish Pain Research Center, Aarhus University, Aarhus, Denmark.

PMID: 34213655 DOI: 10.1007/s00592-021-01767-x

Abstract

Diabetic neuropathy is among the most frequent complications of both type 1 (T1DM) and type 2 diabetes (T2DM) and commonly manifests as a distal symmetrical polyneuropathy (DSPN). Despite evidence that T1DM- and T2DM-related DSPN are separate entities, most of our knowledge on diabetic DSPN derives from studies focused on type 2 diabetes. This systematic review provides an overview of current evidence on DSPN in T1DM, including its epidemiological, pathophysiological and clinical features, along with principal diagnostic tests findings. This review included 182 clinical and preclinical studies. The results indicate that DSPN is a less frequent complication in T1DM compared with T2DM and that distinctive pathophysiological mechanisms underlie T1DM-related DSPN development, with hyperglycemia as a major determinant. T1DM-related DSPN more frequently manifests with non-painful than painful symptoms, with lower neuropathic pain prevalence compared with T2DM-associated DSPN. The overt clinical picture seems characterized by a higher prevalence of large fiber-related clinical signs (e.g., ankle reflexes reduction and vibration hypoesthesia) and to a lesser extent small fiber damage (e.g., thermal or pinprick hypoesthesia). These findings as a whole suggest that large fibers impairment plays a dominant role in the clinical picture of symptomatic T1DM-related DSPN. Nevertheless, small fiber diagnostic testing shows high diagnostic accuracy in detecting early nerve damage and may be an appropriate diagnostic tool for disease monitoring and screening.

Keywords: Distal symmetrical polyneuropathy; Neuropathic pain; Neuropathy; Type 1 diabetes

References

  1. Federation ID (2019) IDF Diabetes Atlas. 9th edition. IDF https://diabetesatlas.org/https://diabetesatlas.org/key-messages.html - PubMed
  2. Boulton AJ (2007) Diabetic neuropathy: classification, measurement and treatment. Curr Opin Endocrinol Diabetes Obes 14(2):141–145 - PubMed
  3. Gylfadottir SS et al (2019) Painful and non-painful diabetic polyneuropathy: clinical characteristics and diagnostic issues. J Diabetes Investig 10(5):1148–1157 - PubMed
  4. Mobasseri M et al (2020) Prevalence and incidence of type 1 diabetes in the world: a systematic review and meta-analysis. Health Promot Perspect 10(2):98–115 - PubMed
  5. Rodríguez-Gutiérrez R, Montori VM (2016) Glycemic control for patients with type 2 diabetes mellitus: our evolving faith in the face of evidence. Circ Cardiovasc Qual Outcomes 9(5):504–512 - PubMed
  6. Callaghan BC et al (2012) Enhanced glucose control for preventing and treating diabetic neuropathy. Cochrane Database Syst Rev 6(6):Cd007543 - PubMed
  7. Dyck PJ et al (2011) Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev 27(7):620–628 - PubMed
  8. Tesfaye S et al (2010) Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 33(10):2285–2293 - PubMed
  9. Pop-Busui R et al (2017) Diabetic neuropathy: a position statement by the american diabetes association. Diabetes Care 40(1):136–154 - PubMed
  10. Galosi E et al (2021) Differential involvement of myelinated and unmyelinated nerve fibers in painful diabetic polyneuropathy. Muscle Nerve 63(1):68–74 - PubMed
  11. Itani M et al (2020) Small and large fiber sensory polyneuropathy in type 2 diabetes: Influence of diagnostic criteria on neuropathy subtypes. J Peripher Nerv Syst 26(1):55–66 - PubMed
  12. Peltier A, Goutman SA, Callaghan BC (2014) Painful diabetic neuropathy. Bmj 348:g1799 - PubMed
  13. Callaghan BC, Hur J, Feldman EL (2012) Diabetic neuropathy: one disease or two? Curr Opin Neurol 25(5):536–541 - PubMed
  14. Moghtaderi A, Bakhshipour A, Rashidi H (2006) Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg 108(5):477–481 - PubMed
  15. Weintrob N et al (2007) Bedside neuropathy disability score compared to quantitative sensory testing for measurement of diabetic neuropathy in children, adolescents, and young adults with type 1 diabetes. J Diabetes Complic 21(1):13–19 - PubMed
  16. Meijer JW et al (2002) Symptom scoring systems to diagnose distal polyneuropathy in diabetes: the diabetic neuropathy symptom score. Diabet Med 19(11):962–965 - PubMed
  17. Report and recommendations of the San Antonio conference on diabetic neuropathy (1988) Consensus statement. Diabetes, 37(7): 1000–1004 - PubMed
  18. Adamska A et al (2019) An increased skin microvessel density is associated with neurovascular complications in type 1 diabetes mellitus. Diab Vasc Dis Res 16(6):513–522 - PubMed
  19. Truini A et al (2018) A cross-sectional study investigating frequency and features of definitely diagnosed diabetic painful polyneuropathy. Pain 159(12):2658–2666 - PubMed
  20. Cristian AB, Remus PA (2018) Diabetic neuropathy prevalence and its associated risk factors in two representative groups of type 1 and type 2 diabetes mellitus patients from Bihor county. Maedica (Bucur) 13(3):229–234 - PubMed
  21. Pan Q et al (2018) Prevalence of and risk factors for peripheral neuropathy in Chinese patients with diabetes: a multicenter cross-sectional study. Front Endocrinol (Lausanne) 9:617 - PubMed
  22. Falkowski B et al (2020) Novel biochemical markers of neurovascular complications in type 1 diabetes patients. J Clin Med 9(1):198 - PubMed
  23. Cardinez N et al (2019) Sex differences in neuropathy & neuropathic pain: a brief report from the phase 2 Canadian study of longevity in type 1 diabetes. J Diabetes Complic 33(12):107397 - PubMed
  24. González-Clemente JM et al (2005) Diabetic neuropathy is associated with activation of the TNF-alpha system in subjects with type 1 diabetes mellitus. Clin Endocrinol (Oxf) 63(5):525–529 - PubMed
  25. Ziegler D et al (2018) Painful and painless neuropathies are distinct and largely undiagnosed entities in subjects participating in an educational initiative (PROTECT study). Diabetes Res Clin Pract 139:147–154 - PubMed
  26. Barbosa M et al (2019) Prevalence and determinants of painful and painless neuropathy in type 1 diabetes mellitus. Front Endocrinol (Lausanne) 10:402 - PubMed
  27. Pop A et al (2016) Insulin resistance is associated with all chronic complications in type 1 diabetes. J Diabetes 8(2):220–228 - PubMed
  28. Chistyakov DA et al (2001) Polymorphisms in the Mn-SOD and EC-SOD genes and their relationship to diabetic neuropathy in type 1 diabetes mellitus. BMC Med Genet 2:4 - PubMed
  29. Van Acker K et al (2009) Prevalence and impact on quality of life of peripheral neuropathy with or without neuropathic pain in type 1 and type 2 diabetic patients attending hospital outpatients clinics. Diabetes Metab 35(3):206–213 - PubMed
  30. Jaiswal M et al (2013) Peripheral neuropathy in adolescents and young adults with type 1 and type 2 diabetes from the SEARCH for diabetes in youth follow-up cohort: a pilot study. Diabetes Care 36(12):3903–3908 - PubMed
  31. Young MJ et al (1993) A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 36(2):150–154 - PubMed
  32. Kwai NC et al (2016) Association between glycemic variability and peripheral nerve dysfunction in type 1 diabetes. Muscle Nerve 54(5):967–969 - PubMed
  33. Obrosova IG et al (2005) Role for nitrosative stress in diabetic neuropathy: evidence from studies with a peroxynitrite decomposition catalyst. Faseb J 19(3):401–403 - PubMed
  34. Drel VR et al (2007) A peroxynitrite decomposition catalyst counteracts sensory neuropathy in streptozotocin-diabetic mice. Eur J Pharmacol 569(1–2):48–58 - PubMed
  35. Araszkiewicz A et al (2011) Increased accumulation of skin advanced glycation end products is associated with microvascular complications in type 1 diabetes. Diabetes Technol Ther 13(8):837–842 - PubMed
  36. Rajaobelina K et al (2017) Progression of skin autofluorescence of AGEs over 4 years in patients with type 1 diabetes. Diabetes Metab Res Rev 33(7):e2917 - PubMed
  37. Elbarbary NS et al (2018) Role of neopterin as a biochemical marker for peripheral neuropathy in pediatric patients with type 1 diabetes: Relation to nerve conduction studies. Int Immunopharmacol 59:68–75 - PubMed
  38. Ortmann KL, Chattopadhyay M (2014) Decrease in neuroimmune activation by HSV-mediated gene transfer of TNFα soluble receptor alleviates pain in rats with diabetic neuropathy. Brain Behav Immun 41:144–151 - PubMed
  39. El-Samahy MH et al (2017) Expression of CD4(+) CD28(null) T lymphocytes in children and adolescents with type 1 diabetes mellitus: relation to microvascular complications, aortic elastic properties, and carotid intima media thickness. Pediatr Diabetes 18(8):785–793 - PubMed
  40. Sherif EM et al (2019) Soluble urokinase plasminogen activator receptor in type 1 diabetic children, relation to vascular complications. J Diabetes Complic 33(9):628–633 - PubMed
  41. Ponirakis G et al (2019) Hypertension contributes to neuropathy in patients with type 1 diabetes. Am J Hypertens 32(8):796–803 - PubMed
  42. Louraki M et al (2016) The prevalence of early subclinical somatic neuropathy in children and adolescents with Type 1 diabetes mellitus and its association with the persistence of autoantibodies to glutamic acid decarboxylase (GAD) and islet antigen-2 (IA-2). Diabetes Res Clin Pract 117:82–90 - PubMed
  43. Thakur V et al (2016) Viral vector mediated continuous expression of interleukin-10 in DRG alleviates pain in type 1 diabetic animals. Mol Cell Neurosci 72:46–53 - PubMed
  44. Sun Q et al (2019) Downregulation of glucose-6-phosphate dehydrogenase contributes to diabetic neuropathic pain through upregulation of toll-like receptor 4 in rats. Mol Pain 15:1744806919838659 - PubMed
  45. Wang X et al (2018) Sigma 1 receptor mediated HMGB1 expression in spinal cord is involved in the development of diabetic neuropathic pain. Neurosci Lett 668:164–168 - PubMed
  46. Méndez-Lara KA et al (2018) Administration of CORM-2 inhibits diabetic neuropathy but does not reduce dyslipidemia in diabetic mice. PLoS One 13(10):e0204841 - PubMed
  47. Akamine T et al (2018) Accumulation of sorbitol in the sciatic nerve modulates circadian properties of diabetes-induced neuropathic pain hypersensitivity in a diabetic mouse model. Biochem Biophys Res Commun 503(1):181–187 - PubMed
  48. Bouhassira D, Letanoux M, Hartemann A (2013) Chronic pain with neuropathic characteristics in diabetic patients: a french cross-sectional study. PLoS One 8(9):e74195 - PubMed
  49. Abbott CA et al (2011) Prevalence and characteristics of painful diabetic neuropathy in a large community-based diabetic population in the U.K. Diabetes Care 34(10):2220–4 - PubMed
  50. Ghaemi N et al (2018) Peripheral neuropathy in children and adolescents with insulin-dependent diabetes mellitus. Iran J Child Neurol 12(2):83–90 - PubMed
  51. Kästenbauer T et al (2004) The prevalence of symptoms of sensorimotor and autonomic neuropathy in type 1 and type 2 diabetic subjects. J Diabetes Complic 18(1):27–31 - PubMed
  52. Hyllienmark L et al (2009) Abnormal cold perception in the lower limbs: a sensitive indicator for detection of polyneuropathy in patients with type 1 diabetes mellitus. Diabetes Res Clin Pract 85(3):298–303 - PubMed
  53. Walter-Höliner I et al (2018) High prevalence and incidence of diabetic peripheral neuropathy in children and adolescents with type 1 diabetes mellitus: results from a 5-year prospective cohort study. Pediatr Neurol 80:51–60 - PubMed
  54. Hajas G, Kissova V, Tirpakova A (2016) A 10-yr follow-up study for the detection of peripheral neuropathy in young patients with type 1 diabetes. Pediatr Diabetes 17(8):632–641 - PubMed
  55. Barkai L et al (1998) Peripheral sensory nerve dysfunction in children and adolescents with type 1 diabetes mellitus. Diabet Med 15(3):228–233 - PubMed
  56. Abad F et al (2002) Subclinical pain and thermal sensory dysfunction in children and adolescents with type 1 diabetes mellitus. Diabet Med 19(10):827–831 - PubMed
  57. Maser RE et al (1991) Measuring subclinical neuropathy: does it relate to clinical neuropathy? Pittsburgh epidemiology of diabetes complications study-V. J Diabet Complic 5(1):6–12 - PubMed
  58. Meh D, Denislic M (1998) Subclinical neuropathy in type I diabetic children. Electroencephalogr Clin Neurophysiol 109(3):274–280 - PubMed
  59. Karsidag S et al (2005) The electrophysiological findings of subclinical neuropathy in patients with recently diagnosed type 1 diabetes mellitus. Diabetes Res Clin Pract 67(3):211–219 - PubMed
  60. Abuelwafaa N et al (2019) Electrophysiological characterization of neuropathy complicating type 1 diabetes mellitus. J Diabetes Res 2019:2435261 - PubMed
  61. Höliner I et al (2013) Validity of the neurological examination in diagnosing diabetic peripheral neuropathy. Pediatr Neurol 49(3):171–177 - PubMed
  62. Nery Ferreira BE, Silva IN, de Oliveira JT (2005) High prevalence of diabetic polyneuropathy in a group of Brazilian children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 18(11):1087–94 - PubMed
  63. Shalitin S et al (2002) Bedside scoring procedure for the diagnosis of diabetic peripheral neuropathy in young patients with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 15(5):613–620 - PubMed
  64. Azmi S et al (2017) Small-fibre neuropathy in men with type 1 diabetes and erectile dysfunction: a cross-sectional study. Diabetologia 60(6):1094–1101 - PubMed
  65. Løseth S et al (2010) Polyneuropathy in type 1 and type 2 diabetes: comparison of nerve conduction studies, thermal perception thresholds and intraepidermal nerve fibre densities. Diabetes Metab Res Rev 26(2):100–106 - PubMed
  66. Toopchizadeh V et al (2016) Electrophysiologic pattern and prevalence of subclinical peripheral neuropathy in children and adolescents with type I diabetes mellitus in Iran. Saudi Med J 37(3):299–303 - PubMed
  67. Suljic E, Drnda S (2019) Type of diabetes mellitus has influence on electrophysiological parameters. Acta Inform Med 27(2):108–113 - PubMed
  68. Peltier AC et al (2013) Evaluation of dermal myelinated nerve fibers in diabetes mellitus. J Peripher Nerv Syst 18(2):162–167 - PubMed
  69. Toth C et al (2014) Motor unit number estimations are smaller in children with type 1 diabetes mellitus: a case-cohort study. Muscle Nerve 50(4):593–598 - PubMed
  70. Picconi F et al (2018) Association between early neuroretinal dysfunction and peripheral motor unit loss in patients with type 1 diabetes mellitus. J Diabetes Res 2018:9763507 - PubMed
  71. Lauria G et al (2010) 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. Eur J Neurol 17(7):903–12 - PubMed
  72. Azmi S et al (2019) Early nerve fibre regeneration in individuals with type 1 diabetes after simultaneous pancreas and kidney transplantation. Diabetologia 62(8):1478–1487 - PubMed
  73. Khoshnoodi M, Truelove S, Polydefkis M (2019) Effect of diabetes type on long-term outcome of epidermal axon regeneration. Ann Clin Transl Neurol 6(10):2088–2096 - PubMed
  74. Løseth S et al (2016) Small and large fiber neuropathy in those with type 1 and type 2 diabetes: a 5-year follow-up study. J Peripher Nerv Syst 21(1):15–21 - PubMed
  75. Ahmed A et al (2012) Detection of diabetic sensorimotor polyneuropathy by corneal confocal microscopy in type 1 diabetes: a concurrent validity study. Diabetes Care 35(4):821–828 - PubMed
  76. Ostrovski I et al (2015) Reproducibility of in vivo corneal confocal microscopy using an automated analysis program for detection of diabetic sensorimotor polyneuropathy. PLoS One 10(11):e0142309 - PubMed
  77. Pritchard N et al (2015) Corneal confocal microscopy predicts 4-year incident peripheral neuropathy in type 1 diabetes. Diabetes Care 38(4):671–675 - PubMed
  78. Chen X et al (2015) Small nerve fiber quantification in the diagnosis of diabetic sensorimotor polyneuropathy: comparing corneal confocal microscopy with intraepidermal nerve fiber density. Diabetes Care 38(6):1138–1144 - PubMed
  79. Alam U et al (2017) Diagnostic utility of corneal confocal microscopy and intra-epidermal nerve fibre density in diabetic neuropathy. PLoS One 12(7):e0180175 - PubMed
  80. Chen X et al (2018) Corneal nerve fractal dimension: a novel corneal nerve metric for the diagnosis of diabetic sensorimotor polyneuropathy. Invest Ophthalmol Vis Sci 59(2):1113–1118 - PubMed
  81. Lovblom LE et al (2015) In vivo corneal confocal microscopy and prediction of future-incident neuropathy in type 1 diabetes: a preliminary longitudinal analysis. Can J Diabetes 39(5):390–397 - PubMed
  82. Lewis EJH et al (2017) Effect of omega-3 supplementation on neuropathy in type 1 diabetes: A 12-month pilot trial. Neurology 88(24):2294–2301 - PubMed
  83. Tavakoli M et al (2013) Corneal confocal microscopy detects early nerve regeneration in diabetic neuropathy after simultaneous pancreas and kidney transplantation. Diabetes 62(1):254–260 - PubMed
  84. Blankenburg M et al (2012) Childhood diabetic neuropathy: functional impairment and non-invasive screening assessment. Diabet Med 29(11):1425–1432 - PubMed
  85. Gibbons CH et al (2013) The evolving natural history of neurophysiologic function in patients with well-controlled diabetes. J Peripher Nerv Syst 18(2):153–161 - PubMed
  86. Maser RE et al (1989) Measuring diabetic neuropathy. Assessment and comparison of clinical examination and quantitative sensory testing. Diabetes Care 12(4):270–275 - PubMed
  87. Navarro X, Kennedy WR, Fries TJ (1989) Small nerve fiber dysfunction in diabetic neuropathy. Muscle Nerve 12(6):498–507 - PubMed
  88. Navarro X, Kennedy WR (1991) Evaluation of thermal and pain sensitivity in type I diabetic patients. J Neurol Neurosurg Psychiatry 54(1):60–64 - PubMed
  89. Louraki M et al (2014) Reproducibility of vibration perception threshold values in children and adolescents with type 1 diabetes mellitus and associated factors. Prim Care Diabetes 8(2):147–157 - PubMed
  90. Feldman EL et al (2017) New horizons in diabetic neuropathy: mechanisms, bioenergetics, and pain. Neuron 93(6):1296–1313 - PubMed
  91. Rosenberger DC et al (2020) Challenges of neuropathic pain: focus on diabetic neuropathy. J Neural Transm (Vienna) 127(4):589–624 - PubMed
  92. Selvarajah D et al (2019) Diabetic peripheral neuropathy: advances in diagnosis and strategies for screening and early intervention. Lancet Diabetes Endocrinol 7(12):938–948 - PubMed
  93. Bonhof GJ et al (2019) Emerging biomarkers, tools, and treatments for diabetic polyneuropathy. Endocr Rev 40(1):153–192 - PubMed
  94. Finnerup NB et al (2015) Pharmacotherapy for neuropathic pain in adults: a systematic review and meta-analysis. Lancet Neurol 14(2):162–173 - PubMed
  95. Callaghan BC et al (2012) Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 11(6):521–534 - PubMed
  96. Hicks CW, Selvin E (2019) Epidemiology of peripheral neuropathy and lower extremity disease in diabetes. Curr Diab Rep 19(10):86 - PubMed
  97. Liu X et al (2019) The risk factors for diabetic peripheral neuropathy: a meta-analysis. PLoS One 14(2):e0212574 - PubMed
  98. Tesfaye S et al (2005) Vascular risk factors and diabetic neuropathy. N Engl J Med 352(4):341–350 - PubMed
  99. Wang N et al (2016) Glycated albumin indicates peripheral diabetic neuropathy. Acta Diabetol 53(6):973–979 - PubMed
  100. Jarmuzewska EA, Ghidoni A, Mangoni AA (2007) Hypertension and sensorimotor peripheral neuropathy in type 2 diabetes. Eur Neurol 57(2):91–95 - PubMed
  101. Partanen J et al (1995) Natural history of peripheral neuropathy in patients with non-insulin-dependent diabetes mellitus. N Engl J Med 333(2):89–94 - PubMed
  102. Adler AI et al (1997) Risk factors for diabetic peripheral sensory neuropathy. results of the seattle prospective diabetic foot study. Diabetes Care 20(7):1162–1167 - PubMed
  103. Feldman EL et al (2019) Diabetic neuropathy. Nat Rev Dis Primers 5(1):41 - PubMed
  104. Ekberg K, Johansson BL (2008) Effect of C-peptide on diabetic neuropathy in patients with type 1 diabetes. Exp Diabetes Res 2008:457912 - PubMed
  105. von Hehn CA, Baron R, Woolf CJ (2012) Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73(4):638–652 - PubMed
  106. Ved N et al (2018) Diabetes-induced microvascular complications at the level of the spinal cord: a contributing factor in diabetic neuropathic pain. J Physiol 596(16):3675–3693 - PubMed
  107. Themistocleous AC et al (2016) The Pain in Neuropathy Study (PiNS): a cross-sectional observational study determining the somatosensory phenotype of painful and painless diabetic neuropathy. Pain 157(5):1132–1145 - PubMed
  108. Raputova J et al (2017) Sensory phenotype and risk factors for painful diabetic neuropathy: a cross-sectional observational study. Pain 158(12):2340–2353 - PubMed
  109. Feldman EL, Stevens MJ (1994) Clinical testing in diabetic peripheral neuropathy. Can J Neurol Sci 21(4):S3-7 - PubMed
  110. Petropoulos IN et al (2013) Corneal nerve loss detected with corneal confocal microscopy is symmetrical and related to the severity of diabetic polyneuropathy. Diabetes Care 36(11):3646–3651 - PubMed
  111. Ziegler D, Mayer P, Gries FA (1988) Evaluation of thermal, pain, and vibration sensation thresholds in newly diagnosed type 1 diabetic patients. J Neurol Neurosurg Psychiatry 51(11):1420–1424 - PubMed
  112. Breiner A et al (2014) Does the prevailing hypothesis that small-fiber dysfunction precedes large-fiber dysfunction apply to type 1 diabetic patients? Diabetes Care 37(5):1418–1424 - PubMed
  113. Ziegler D et al (1988) Assessment of small and large fiber function in long-term type 1 (insulin-dependent) diabetic patients with and without painful neuropathy. Pain 34(1):1–10 - PubMed
  114. Zhang X et al (2017) Clinical characteristics and risk factors of diabetic peripheral neuropathy of type 1 diabetes mellitus patients. Diabetes Res Clin Pract 129:97–104 - PubMed
  115. Sveen KA et al (2013) Small- and large-fiber neuropathy after 40 years of type 1 diabetes: associations with glycemic control and advanced protein glycation: the Oslo Study. Diabetes Care 36(11):3712–3717 - PubMed

Publication Types