Cited by 708Peripheral Neuropathies and DisordersPain Mechanisms and TreatmentsHereditary Neurological Disorders

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The spectrum of neuropathy in diabetes and impaired glucose tolerance

Sumner, C.J., Sheth, S., Griffin, J.W., Cornblath, D.R., Polydefkis, M.·2003·Neurology

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Abstract

OBJECTIVE: To compare the neuropathy associated with impaired glucose tolerance (IGT) and diabetes mellitus (DM) determined by oral glucose tolerance testing (OGTT). METHODS: Patients with peripheral neuropathy of unknown cause were prescribed OGTT. Duration of neuropathic symptoms, neuropathic pain, neuropathy classification, nerve conduction test results, and intraepidermal nerve fiber densities (IENFD) were compared between IGT and DM groups. RESULTS: Seventy-three patients completed OGTT; 41 (56%) had abnormal results. Of these 41 patients, 26 had IGT and 15 had DM. Patients with IGT had less severe neuropathy than patients with diabetes, as measured by sural nerve amplitudes (p = 0.056), sural nerve conduction velocities (p = 0.03), and distal leg IENFD (p = 0.01). Patients with IGT had predominantly small fiber neuropathy, compared to patients with DM (p = 0.05), who had more involvement of large nerve fibers. CONCLUSIONS: The neuropathy associated with IGT is milder than the neuropathy associated with DM. Small nerve fibers are prominently affected and may be the earliest detectable sign of neuropathy in glucose dysmetabolism. OGTT is appropriate in patients with idiopathic neuropathy.

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BackgroundInfluential
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New diagnostic tests for diabetic distal symmetric polyneuropathy
Παπάνας, Ν., & Ziegler, D. (2009) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2009.09.006 · Cited by 75
“Neuropad assesses sudomotor function, which is mediated by small fibers, and these may be impaired at a very early stage in diabetes before any largefiber injury (Malik et al., 2005; Smith et al., 2001; Sumner et al., 2003).”
Background
Prevalence of somatic small fiber neuropathy in obesity
Herman, R. M., Brower, J. B., Stoddard, D. G., Casano, A. R., Targovnik, J. H., Herman, J., & Tearse, P. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803418 · Cited by 74
Topical C itrullus colocynthis (bitter apple) extract oil in painful diabetic neuropathy: A double‐blind randomized placebo‐controlled clinical trial
Heydari, M., Homayouni, K., Hashempur, M. H., & Shams, M. (2015) · Journal of Diabetes · doi:10.1111/1753-0407.12287 · Cited by 74
Update on the management of diabetic polyneuropathies
Stevens, M. J., & Shakher, J. (2011) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s11324 · Cited by 82
“05 for diabetes vs NGT, IFG, and IGT).(7) The reported prevalence of painful DPN typically ranges from 10%–26% based on differing criteria used to diagnose neuropathic pain.”
Effects of Polyol Pathway Hyperactivity on Protein Kinase C Activity, Nociceptive Peptide Expression, and Neuronal Structure in Dorsal Root Ganglia in Diabetic Mice
Uehara, K., Yamagishi, S., Otsuki, S., Chin, S., & Yagihashi, S. (2004) · Diabetes · doi:10.2337/diabetes.53.12.3239 · Cited by 72
“There is growing evidence that an early involvement in diabetic neuropathy is small nerve fibers, conferring pain sensation and autonomic nerve function (14,15).”
Endoplasmic reticulum stress contributes to prediabetic peripheral neuropathy
Lupachyk, S., Watcho, P., Obrosov, A. A., Stavniichuk, R., & Obrosova, I. G. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.11.001 · Cited by 73
“Several groups reported a higher incidence of diabetes-like neuropathic changes in human subjects with impaired glucose tolerance (Smith et al., 2001, 2006; Sumner et al., 2003; Ziegler et al., 2009) and metabolic syndrome (Bonadonna et al.”
BackgroundInfluential
An Open-Label Study of the Lidocaine Patch 5% in Painful Idiopathic Sensory Polyneuropathy
Herrmann, D. N., Barbano, R. L., Hart-Gouleau, S., Pennella‐Vaughan, J., & Dworkin, R. H. (2005) · Pain Medicine · doi:10.1111/j.1526-4637.2005.00058.x · Cited by 71
Pain and small-fiber neuropathy in patients with hypothyroidism
Ørstavik, K., Norheim, I., & Jørum, E. (2006) · Neurology · doi:10.1212/01.wnl.0000234035.13779.4a · Cited by 70
Determinants of epidermal nerve fiber density in normal individuals
Umapathi, T., Tan, W. L., Tan, N. C., & Chan, Y. H. (2006) · Muscle & Nerve · doi:10.1002/mus.20528 · Cited by 70
Pharmacological treatment of diabetic peripheral neuropathy.
Cohen, K., Shinkazh, N., Frank, J., Israel, I., & Fellner, C. (2015) · PubMed Central · Cited by 71
Triglyceride, nonesterified fatty acids, and prediabetic neuropathy: role for oxidative–nitrosative stress
Lupachyk, S., Watcho, P., Hasanova, N., Julius, U., & Obrosova, I. G. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.01.029 · Cited by 72
Etiology of small‐fiber neuropathy
Bednařík, J., Vlčková, E., Buršová, Š., Bělobrádková, J., Dušek, L., & Sommer, C. (2009) · Journal of the Peripheral Nervous System · doi:10.1111/j.1529-8027.2009.00229.x · Cited by 69
“IGT is a well-identified condition increasing the risk of SFN (Smith et al., 2001; Sumner et al., 2003; Smith and Singleton, 2008).”
BackgroundInfluential
Diagnosis and management of sensory polyneuropathy
Gwathmey, K. G., & Pearson, K. (2019) · BMJ · doi:10.1136/bmj.l1108 · Cited by 76
Electrically Stimulated Axon Reflexes Are Diminished in Diabetic Small Fiber Neuropathies
Krämer, H. H., Schmelz, M., Birklein, F., & Bickel, A. (2004) · Diabetes · doi:10.2337/diabetes.53.3.769 · Cited by 69
“On the other hand, in patients with very early neuropathy and impaired glucose tolerance (45), skin biopsies demonstrated slightly reduced nerve fiber density but there was simultaneously an increased distal fiber branching, which counteracts fiber loss (4,46).”
Background
Phenotypic Changes in Diabetic Neuropathy Induced by a High-Fat Diet in Diabetic C57Bl/6 Mice
Guilford, B. L., Ryals, J. M., & Wright, D. E. (2011) · Experimental Diabetes Research · doi:10.1155/2011/848307 · Cited by 69
Animal Models of Diabetic Neuropathic Pain
Gao, F., & Zheng, Z. (2014) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0033-1363234 · Cited by 68
Evaluation of distal symmetric polyneuropathy: The role of laboratory and genetic testing (an evidence‐based review)
England, J. D., Gronseth, G., Franklin, G. M., Carter, G. T., Kinsella, L. J., Cohen, J. A., Asbury, A. K., Szigeti, K., Lupski, J. R., Latov, N., et al. (2008) · Muscle & Nerve · doi:10.1002/mus.21226 · Cited by 68
Self-citation
Reliability of quantitative sudomotor axon reflex testing and quantitative sensory testing in neuropathy of impaired glucose regulation
Peltier, A., Smith, A. G., Russell, J. W., Sheikh, K., Bixby, B. A., Howard, J., Goldstein, J. M., Song, Y., Wang, L., Feldman, E. L., et al. (2009) · Muscle & Nerve · doi:10.1002/mus.21210 · Cited by 70
Variables associated with corneal confocal microscopy parameters in healthy volunteers: implications for diabetic neuropathy screening
Wu, T., Ahmed, A., Bril, V., Orszag, A., Ng, E., Nwe, P., & Perkins, B. A. (2012) · Diabetic Medicine · doi:10.1111/j.1464-5491.2012.03678.x · Cited by 67
Chronic Idiopathic Axonal Polyneuropathy Is Associated With the Metabolic Syndrome
Visser, N. A., Vrancken, A. F. J. E., van der Schouw, Y. T., van den Berg, L. H., & Notermans, N. C. (2012) · Diabetes Care · doi:10.2337/dc12-0469 · Cited by 67
Diabetic Neuropathies
Llewelyn, J., Tomlinson, D. R., & Thomas, P. K. (2005) · Elsevier eBooks · doi:10.1016/b978-0-7216-9491-7.50088-0 · Cited by 67
Electrophysiological findings of peripheral neuropathy in newly diagnosed type II diabetes mellitus
Rota, E., Quadri, R., Fanti, E., Isoardo, G., Poglio, F., Tavella, A., Paolasso, I., Ciaramitaro, P., Bergamasco, B., & Cocito, D. (2005) · Journal of the Peripheral Nervous System · doi:10.1111/j.1085-9489.2005.00046.x · Cited by 67
“…glucose-tolerance test appeared the most sensitive measure to reveal abnormalities in glucose handling (Singleton et al., 2001), and it has therefore been suggested appropriate to screen patients with neuropathy of unknown cause (Novella et al., 2001; Singleton et al., 2001; Sumner et al., 2003).”
BackgroundInfluential
Nitrosative stress and peripheral diabetic neuropathy in leptin-deficient (ob/ob) mice
Vareniuk, І., Pavlov, I. A., Drel, V. R., Lyzogubov, V. V., Ilnytska, O., Bell, S. R., Tibrewala, J., Groves, J. T., & Obrosova, I. G. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.03.019 · Cited by 67
“Subjects with both Type 1 and Type 2 diabetes display clearly manifest epidermal nerve fiber loss ( Sumner et al., 2003; Pittenger et al., 2004).”
Background
Does impaired glucose metabolism cause polyneuropathy? Review of previous studies and design of a prospective controlled population‐based study
Dyck, P. J. B., Dyck, P. J. B., Klein, C. J., & Weigand, S. D. (2007) · Muscle & Nerve · doi:10.1002/mus.20846 · Cited by 65
Prediabetic Neuropathy: Does It Exist?
Παπάνας, Ν., & Ziegler, D. (2012) · Current Diabetes Reports · doi:10.1007/s11892-012-0278-3 · Cited by 70
Mechanisms of Vascular Complications in Prediabetes
Milman, S., & Crandall, J. P. (2011) · Medical Clinics of North America · doi:10.1016/j.mcna.2010.11.004 · Cited by 68
“However, the neuropathy associated with IGT is less severe than the neuropathy seen with diabetes, documented by skin nerve fiber density, nerve amplitude, and nerve velocity.(116) Manifestations of autonomic neurop-”
Attenuation of Vascular/Neural Dysfunction in Zucker Rats Treated With Enalapril or Rosuvastatin
Oltman, C. L., Davidson, E. P., Coppey, L. J., Kleinschmidt, T. L., Lund, D. D., & Yorek, M. A. (2008) · Obesity · doi:10.1038/oby.2007.19 · Cited by 63
Peripheral neuropathy is associated with insulin resistance independent of metabolic syndrome
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“Similar to previous studies, dysglycemia showed the strongest evidence supporting a pathogenic link with PN [20-22].”
Result
In Vivo Corneal Confocal Microscopy and Prediction of Future-Incident Neuropathy in Type 1 Diabetes: A Preliminary Longitudinal Analysis
Lovblom, L. E., Halpern, E. M., Wu, T., Kelly, D., Ahmed, A., Boulet, G., Orszag, A., Ng, E., Ngo, M., Bril, V., et al. (2015) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2015.02.006 · Cited by 64
Polyneuropathy with impaired glucose tolerance: Implications for diagnosis and therapy
Singleton, J. R., Smith, A. G., Russell, J. W., & Feldman, E. L. (2005) · Current Treatment Options in Neurology · doi:10.1007/s11940-005-0004-4 · Cited by 63
Increased Incidence of Carpal Tunnel Syndrome up to 10 Years Before Diagnosis of Diabetes
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An update on electrophysiological studies in neuropathy
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Incidence Rate of Prediabetes Progression to Diabetes: Modeling an Optimum Target Group for Intervention
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Small Fiber Neuropathy
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Transplantation of Neural Crest-Like Cells Derived from Induced Pluripotent Stem Cells Improves Diabetic Polyneuropathy in Mice
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“Depletion of IENFDs, representing the peripheral terminals of nociceptive fibers, appears to be an early index of DPN (48,53).”
Background
Bergapten exerts inhibitory effects on diabetes-related osteoporosis via the regulation of the PI3K/AKT, JNK/MAPK and NF-κB signaling pathways in osteoprotegerin knockout mice
Xue-ju, L., Zhu, Z., Han, S.-L., & Zhang, Z. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2794 · Cited by 60
“Constantly high blood sugar levels lead to kidney failure, cardiovascular problems and neuropathy (26,27).”
Sodium Channels, Mitochondria, and Axonal Degeneration in Peripheral Neuropathy
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Painful diabetic neuropathy
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Sensitivity and specificity of a new indicator test (Neuropad) for the diagnosis of peripheral neuropathy in type 2 diabetes patients: a comparison with clinical examination and nerve conduction study
Παπάνας, Ν., Giassakis, G., Papatheodorou, K., Papazoglou, D., Monastiriotis, C., Christakidis, D., Piperidou, H., & Maltezos, E. S. (2007) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2006.08.003 · Cited by 57

Authors: Sumner, C. J., Sheth, S., Griffin, J. W., Cornblath, D. R., & Polydefkis, M.
Affiliations: Johns Hopkins University (US)
ORCID: Sumner, C.J.
Cornblath, D.R.
Polydefkis, M.
Venue: Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2003-01-14
Volume: 60
Issue: 1
Pages: 108-111
ISSN: 0028-3878 (ISSN-L)
1526-632X
DOI: 10.1212/wnl.60.1.108
OpenAlex: W1978686107
Cited by: 708
References: 25
Citations by year: 2026: 9 · 2025: 18 · 2024: 11 · 2023: 13 · 2022: 19 · 2021: 21 · 2020: 30 · 2019: 26 · 2018: 27 · 2017: 35 · 2016: 37 · 2015: 42 · 2014: 53 · 2013: 43 · 2012: 40
FWCI: 21.43
Type: journal article
Language: en
Open access: closed
Locations: Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5k23ns041374-04)
National Institute of Neurological Disorders and Stroke (K23NS41374-01)
Topics: Health Sciences › Medicine › Clinical Neurology › Peripheral Neuropathies and Disorders
Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
Keywords: diabetic peripheral neuropathy, impaired glucose tolerance, oral glucose tolerance test, small fiber neuropathy, intraepidermal nerve fiber density, nerve conduction velocity, sural nerve, neuropathic pain, neuropathy classification
MeSH terms: Adult, Aged, Aged, 80 and over, Blood Glucose, Cell Count, Diabetic Nephropathies, Electrodiagnosis, Electromyography, Epidermis, Female, Glucose Tolerance Test, Humans, Male, Middle Aged, Nerve Fibers, Neural Conduction, Pain Measurement, Peripheral Nervous System Diseases, Sural Nerve, Cell Size

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The spectrum of neuropathy in diabetes and impaired glucose tolerance

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