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Increased Prevalence of Impaired Glucose Tolerance in Patients With Painful Sensory Neuropathy
Open accessAbstract
OBJECTIVE—To characterize a cohort of patients with neuropathy and impaired glucose tolerance (IGT) but no other identifiable cause of neuropathy. Of patients with diabetes, 10% have peripheral neuropathy at the time of their diagnosis, suggesting that axonal injury may occur early in the course of glucose intolerance. The American Diabetes Association (ADA) revised diagnostic criteria to recognize IGT (a serum glucose between 140 and 200 mg/dl in a 2-h oral glucose tolerance test [OGTT]) as a risk factor for cardiovascular disease independent of development of diabetes. RESEARCH DESIGN AND METHODS—Using revised ADA criteria for diabetes and IGT, we prospectively evaluated 107 sequential patients with idiopathic neuropathy. RESULTS—A total of 13 of the 107 patients had diabetes, whereas 36 (34%) had IGT, nearly three times the prevalence in age-matched control subjects (P < 0.01). OGTT was often elevated, whereas both fasting plasma glucose and HbA1c were normal. Comparing patients with diabetes, IGT, or normal OGTT, age and BMI were similar. However, painful sensory symptoms were more common in patients with IGT and diabetes, and family history of neuropathy was significantly more common in normoglycemic patients. Electrodiagnostic findings of axonal injury were less severe in patients with IGT and were more likely to be confined to sensory fibers than in patients with diabetes. CONCLUSIONS—Our results suggest that IGT may cause or contribute to small-fiber neuropathy, which is similar in phenotype to the painful sensory neuropathy commonly encountered in diabetes. Two-hour OGTT is more sensitive than other measures of glucose handling in screening these patients.
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“There is controversy regarding the effect of glucose dysmetabolism on small nerve fibers34,42 and symptom severity16,48,56 in FMS.”
From Pain and small fiber pathology in men with fibromyalgia syndrome (2024) · cites this paper as [42]
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In the citing paper
“Other forms of diabetic neuropathies are mononeuritis such as cranial nerve palsies or entrapment neuropathies (eg, carpal tunnel syndrome, ulnar entrapment, and peroneal entrapment, among others).632–635”
From American Association of Clinical Endocrinology Clinical Practice Guideline: Developing a Diabetes Mellitus Comprehensive Care Plan-2022 Update. (2022) · cites this paper as [635]
Experimental — accuracy not yet measuredIn the citing paper
“Finally, evidence is accumulating on increased prevalence of idiopathic polyneuropathy (eg, idiopathic sensory/painful neuropathy,73–78 and sensory/small fibre only neuropathy)73,75,78 among prediabetic individuals with IGT being more strongly related to painful than non-painful neuropathy.73,75,78”
From Prediabetes: a high-risk state for diabetes development (2012) · cites this paper as [75]
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Treatment of Diabetic Sensory Polyneuropathy
Zilliox, L. A., & Russell, J. W. (2011) · Current Treatment Options in Neurology · doi:10.1007/s11940-011-0113-1 · Cited by 105
“Neuropathic pain is also one of the most common presentations of impaired glucose regulation [9, 10].”
BackgroundCauses of neuropathy in patients referred as “idiopathic neuropathy”
Farhad, K., Traub, R., Ruzhansky, K. M., & Brannagan, T. H. (2015) · Muscle & Nerve · doi:10.1002/mus.24969 · Cited by 104
Exercise-mediated improvements in painful neuropathy associated with prediabetes in mice
Groover, A. L., Ryals, J. M., Guilford, B. L., Wilson, N. M., Christianson, J. A., & Wright, D. E. (2013) · Pain · doi:10.1016/j.pain.2013.07.052 · Cited by 102
“Although neuropathy associated with prediabetes is usually less severe than neuropathy in overt diabetic patients [51], it is still a devastating complication of the disease.”
BackgroundHoffman-Snyder, C., Smith, B. E., Ross, M. A., Hernandez, J., & Bosch, E. P. (2006) · Archives of Neurology · doi:10.1001/archneur.63.8.noc50336 · Cited by 100
“Abnormal glucose metabolism was found at nearly a 2-fold higher rate (62%) in patients with CIAP when compared with CDC–published, general age-matched population prevalence rates (33%) in adults 60 years and older.(5-11) Using the CDC rates provides a control population that supports the conclusions of previously publ…”
BackgroundMethodResultInfluentialGreen, A. Q., Krishnan, S. T. M., Finucane, F. M., & Rayman, G. A. (2009) · Diabetes Care · doi:10.2337/dc09-0101 · Cited by 99
The diagnostic yield of a standardized approach to idiopathic sensory-predominant neuropathy
Smith, A. G., & Singleton, J. R. (2004) · Archives of Internal Medicine · doi:10.1001/archinte.164.9.1021 · Cited by 95
“Other data support this association.(8,11,12) Patients with IGT carry many of the macrovascular risks of frank diabetes, and diet modification and exercise have been shown to reduce their risk of developing diabetes.”
ResultSelf-citationClassification and Diagnosis of Diabetes
GENUTH, S. M., Palmer, J. P., & Nathan, D. M. (2018) · Cited by 95
Clinical Manifestations and Current Treatment options for Diabetic Neuropathies
CASELLINI, C. M., & Vinik, A. I. (2007) · Endocrine Practice · doi:10.4158/ep.13.5.550 · Cited by 95
Diet‐induced obesity in Sprague–Dawley rats causes microvascular and neural dysfunction
Davidson, E. P., Coppey, L. J., Calcutt, N. A., Oltman, C. L., & Yorek, M. A. (2010) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.1088 · Cited by 91
“The finding that rats fed a high fat diet develop indices of neuropathy is consistent with our studies of obese Zucker rats [4,14] and also with clinical studies in which pre-diabetes and impaired glucose tolerance have been associated with an early-onset, length-dependent neuropathy that is typically sensory predomin…”
Oxidative injury and neuropathy in diabetes and impaired glucose tolerance
Russell, J. W., Berent‐Spillson, A., Vincent, A. M., Freimann, C. L., Sullivan, K. A., & Feldman, E. L. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.02.013 · Cited by 91
“In human patients, neuropathy associated with IGT presents as a distal symmetrical sensory polyneuropathy with prominent neuropathic pain, similar to early diabetic neuropathy (Singleton et al., 2001; Singleton et al., 2001; Singleton et al., 2003; Russell JW, 2006; Smith et al., 2006).”
InfluentialNoninvasive evaluation of neural impairment in subjects with impaired glucose tolerance
Putz, Z., Tabák, A. G., Tóth, N., Istenes, I., Németh, N., Gandhi, R. A., Hermányi, Z., Keresztes, K., Jermendy, G., Tesfaye, S., et al. (2009) · Diabetes Care · doi:10.2337/dc08-1406 · Cited by 90
“While observational studies have shown an increased prevalence of IGT among subjects with idiopathic neuropathy (7), there are limited data concerning the prevalence of neuropathy in IGT.”
BackgroundShi, Y., Liang, X., Zhang, H., Wu, Q., Qu, L., & Sun, Q. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2013.59 · Cited by 90
Chronic idiopathic axonal polyneuropathy: a systematic review
Zis, P., Sarrigiannis, P. G., Rao, D. G., Hewamadduma, C., & Hadjivassiliou, M. (2016) · Journal of Neurology · doi:10.1007/s00415-016-8082-7 · Cited by 89
Impaired Glycemia and Diabetic Polyneuropathy
Dyck, P. J. B., Clark, V. M., Overland, C. J., Davies, J. L., Pach, J. M., Dyck, P. J. B., Klein, C. J., Rizza, R. A., Melton, L. J., Carter, R. E., et al. (2012) · Diabetes Care · doi:10.2337/dc11-1421 · Cited by 88
Diabetic neuropathy: classification, measurement and treatment
Boulton, A. J. M. (2007) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e328014979e · Cited by 89
Smith, A. G., & Singleton, J. R. (2012) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/01.con.0000411568.34085.3e · Cited by 90
Self-citationPitcher, G. M., & Henry, J. L. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2003.10.019 · Cited by 84
Hanewinckel, R., Drenthen, J., Ligthart, S., Dehghan, A., Franco, O. H., Albert Hofman, D., Ikram, M. A., & van Doorn, P. A. (2016) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2016-314171 · Cited by 89
Davidson, E. P., Coppey, L. J., Lu, B., Arballo, V., Calcutt, N. A., Gerard, C. J., & Yorek, M. A. (2009) · Experimental Diabetes Research · doi:10.1155/2009/431980 · Cited by 81
“To address this issue we used a procedure previously used in rats to protect the pancreatic β cells from streptozotocin toxicity [29, 30].”
MethodBiology of diabetic neuropathy
Vincent, A. M., Calabek, B., Roberts, L., & Feldman, E. L. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52902-2.00034-5 · Cited by 80
Kamiya, H., Zhang, W., & Sima, A. A. F. (2006) · Diabetologia · doi:10.1007/s00125-006-0379-0 · Cited by 79
“This is also underscored by degeneration of C-fibres already under pre-diabetic conditions in both humans [47, 48] and rats [49].”
Unmyelinated fiber sensory neuropathy differs in type 1 and type 2 diabetes
Kamiya, H., Murakawa, Y., Zhang, W., & Sima, A. A. F. (2005) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.541 · Cited by 77
“This notion is supported by recent clinical data describing the frequent occurrence of painful neuropathy in patients exhibiting impaired glucose tolerance and β-cell dysfunction [3,4].”
Shankarappa, S. A., Piedras-Renterı́a, E. S., & Stubbs, E. B. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07302.x · Cited by 78
Gill, H. K., Yadav, S., Ramesh, V., & Bhatia, E. (2014) · Journal of Postgraduate Medicine · doi:10.4103/0022-3859.138750 · Cited by 78
Epidemiology of peripheral neuropathy: An Indian perspective
Das, S. K., Trivedi, S., Pandit, A., & Ganguly, G. (2017) · Annals of Indian Academy of Neurology · doi:10.4103/aian.aian_470_16 · Cited by 76
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
Pharmacological treatment of diabetic peripheral neuropathy.
Cohen, K., Shinkazh, N., Frank, J., Israel, I., & Fellner, C. (2015) · PubMed Central · Cited by 71
Electrophysiologic testing in diabetic neuropathy
Perkins, B. A., & Bril, V. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53480-4.00018-7 · Cited by 71
“Of the patients with IGT or impaired fasting glucose, 69–73%, or more than two-thirds, had abnormal NCS (Singleton et al., 2001a, b; Smith et al., 2001).”
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
“Most individuals with neuropathy associated with prediabetes have painful small-fiber sensory neuropathy, are obese, and have dyslipidemia [12, 18–21].”
BackgroundC-Peptide Reverses Nociceptive Neuropathy in Type 1 Diabetes
Kamiya, H., Zhang, W., Ekberg, K., Wahren, J., & Sima, A. A. F. (2006) · Diabetes · doi:10.2337/db06-0396 · Cited by 68
“Clinically, painful diabetic neuropathy occurs in patients with pre-diabetes (8,9) and early in the course of diabetic neuropathy in type 2 patients (42,43).”
BackgroundJoseph, E. K., & Levine, J. D. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00400-7 · Cited by 68
Metadata
- Authors
- Singleton, J. R., Smith, A. G., & Bromberg, M. B.
- Affiliations
- University of Utah (US)
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2001-08-01
- Volume
- 24
- Issue
- 8
- Pages
- 1448-1453
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2095995150
- Cited by
- 364
- References
- 32
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 9 · 2023: 7 · 2022: 12 · 2021: 7 · 2020: 21 · 2019: 9 · 2018: 17 · 2017: 20 · 2016: 14 · 2015: 22 · 2014: 28 · 2013: 25 · 2012: 21
- FWCI
- 4.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- 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
- impaired glucose tolerance, small fiber neuropathy, peripheral neuropathy, diabetes mellitus, oral glucose tolerance test, axonal injury, electrodiagnostic findings
- MeSH terms
- Adult, Aged, Arsenic, Blood Glucose, Cardiovascular Diseases, Diabetic Neuropathies, Electromyography, Glucose Tolerance Test, Glycated Hemoglobin, Humans, Lead, Mercury, Middle Aged, Neural Conduction, Neuralgia, Peripheral Nervous System Diseases, Prospective Studies, Risk Factors, Body Mass Index, Prevalence, Glucose Intolerance
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