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 fibers and symptom severity in FMS.
“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]
The Abstract reports that impaired glucose tolerance may contribute to small-fiber neuropathy, and the Results say conclusive proof will be difficult. This supports uncertainty about an effect on small fibers, but the paper studies patients with sensory neuropathy, not FMS; it does not establish controversy specifically in FMS. The separate symptom-severity clause has other citations. (LLM, conf=0.84)
Experimental — accuracy not yet measuredOther diabetic neuropathies include mononeuritis such as cranial nerve palsies and entrapment neuropathies.
“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]
The Results discuss sensory-predominant neuropathy in early diabetes, and the Research Design and Methods describe testing for distal neuropathy (page numbers unavailable). Neither passage identifies mononeuritis, cranial nerve palsies, or entrapment neuropathies as forms of diabetic neuropathy; searches for those terms and the named entrapments found no supporting passage in our copy. (LLM, conf=0.72)
Experimental — accuracy not yet measuredEvidence is accumulating on increased prevalence of idiopathic polyneuropathy among prediabetic individuals, with IGT being more strongly related to painful than non-painful neuropathy.
“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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“paired glucose tolerance in prediabetic state is linked to painful sensory neuropathy.(2) It has been proposed that”
BackgroundAssociated conditions in small fiber neuropathy – a large cohort study and review of the literature
de Greef, B. T. A., Hoeijmakers, J. G. J., Gorissen-Brouwers, C. M. L., Geerts, M., Faber, C. G., & Merkies, I. S. J. (2017) · European Journal of Neurology · doi:10.1111/ene.13508 · Cited by 156 · see citing works
“of the patients, adding to the underlying conditions of SFN [28,29].”
BackgroundCorneal Confocal Microscopy Detects Neuropathy in Subjects With Impaired Glucose Tolerance
Asghar, O., Petropoulos, I. N., Alam, U., Jones, W., Jeziorska, M., Marshall, A. G., Ponirakis, G., Fadavi, H., Boulton, A. J. M., Tavakoli, M., et al. (2014) · Diabetes Care · doi:10.2337/dc14-0279 · Cited by 155 · see citing works
Early diabetic neuropathy: Triggers and mechanisms
Dobretsov, M. G. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i2.175 · Cited by 153 · see citing works
Reduction of skin innervation is associated with a severe fibromyalgia phenotype
Evdokimov, D., Frank, J., Klitsch, A., Unterecker, S., Warrings, B., Serra, J., Papagianni, A., Saffer, N., Meyer zu Altenschildesche, C., Kampik, D., et al. (2019) · Annals of Neurology · doi:10.1002/ana.25565 · Cited by 152 · see citing works
“Disturbance of glucose metabolism leading to impaired glucose tolerance or diabetes mellitus has been associated with small fiber neuropathy.(43) Surprisingly, small fiber test results of 17 patients, who had an elevated HbA1c and/or elevated glucose values in the OGTT after study inclusion, did not differ from those…”
BackgroundSmith, S. M., Dworkin, R. H., Turk, D. C., Baron, R., Polydefkis, M. J., Tracey, I., Borsook, D., Edwards, R. R., Harris, R. E., Wager, T. D., et al. (2017) · Journal of Pain · doi:10.1016/j.jpain.2017.02.429 · Cited by 151 · see citing works
“biopsy detected neuropathy in individuals with impaired glucose tolerance or occult diabetes who had normal large fiber test results.(139,170,171,176) Patients with SFN followed for approximately 2.”
Palacios, T., Vitetta, L., Coulson, S., Madigan, C. D., Lam, Y. Y., Manuel, R., Briskey, D. R., Hendy, C., Kim, J.-N., Ishoey, T., et al. (2020) · Nutrients · doi:10.3390/nu12072041 · Cited by 139 · see citing works
“Prediabetes is of concern, as people with this condition are at high risk of developing T2DM and complications—particularly cardiovascular disease, nephropathy [3], and retinopathy [4,5].”
BackgroundUnderstanding the impact of painful diabetic neuropathy
Quattrini, C., & Tesfaye, S. H. (2003) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.360 · Cited by 137 · see citing works
Twigg, S. M., Kamp, M. C., Davis, T. M. E., Neylon, E. K., & Flack, J. R. (2007) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.2007.tb00998.x · Cited by 133 · see citing works
The reliability of skin biopsy with measurement of intraepidermal nerve fiber density
Smith, A. G., Howard, J. R., Kroll, R., Ramachandran, P., Hauer, P. E., Singleton, J. R., & McArthur, J. C. (2004) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2004.09.032 · Cited by 135 · see citing works
“Peripheral neuropathy with prominent small nerve injury is a common clinical problem, occurring in diabetes, prediabetes, drug and toxin exposures, and idiopathic neuropathies [1–3].”
BackgroundSelf-citationNew Insights Into Diabetic Polyneuropathy
Polydefkis, M. J. (2003) · JAMA · doi:10.1001/jama.290.10.1371 · Cited by 134 · see citing works
Freeman, R. L. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53480-4.00006-0 · Cited by 133 · see citing works
Biological and medical physics, biomedical engineering
Herman, I. P. (2014) · Cited by 136 · see citing works
Body Mass Index, Weight Gain, and Incident Urinary Incontinence in Middle-Aged Women
Townsend, M. K., Danforth, K. N., ROSNER, B. A., Curhan, G. C., Resnick, N. M., & Grodstein, F. (2007) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000270121.15510.57 · Cited by 131 · see citing works
Role of Neurologists and Diagnostic Tests on the Management of Distal Symmetric Polyneuropathy
Callaghan, B. C., Kerber, K. A., Lisabeth, L. D., Morgenstern, L. B., Longoria, R., Rodgers, A. F., Longwell, P. J., & Feldman, E. L. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.1279 · Cited by 129 · see citing works
Idiopathic neuropathy, prediabetes and the metabolic syndrome
Smith, A. G., & Singleton, J. R. (2006) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2005.11.020 · Cited by 127 · see citing works
Self-citationThe metabolic syndrome and neuropathy: Therapeutic challenges and opportunities
Callaghan, B. C., & Feldman, E. L. (2013) · Annals of Neurology · doi:10.1002/ana.23986 · Cited by 125 · see citing works
Impaired glucose tolerance and insulinopenia in the GK‐rat causes peripheral neuropathy
Murakawa, Y., Zhang, W., Pierson, C. R., Brismar, T., Östenson, C., Efendić, S., & Sima, A. A. F. (2002) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.326 · Cited by 125 · see citing works
Idiopathic neuropathy patients are at high risk for metabolic syndrome
Smith, A. G., Rose, K., & Singleton, J. R. (2008) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2008.06.005 · Cited by 121 · see citing works
“Several groups have demonstrated a 30– 45% prevalence of impaired glucose tolerance (IGT) in patients with otherwise idiopathic neuropathy [1].”
Self-citationKrishnan, S. T. M., & Rayman, G. A. (2004) · Diabetes Care · doi:10.2337/diacare.27.12.2930 · Cited by 117 · see citing works
In vivo confocal microscopy of corneal small fiber damage in diabetes mellitus
Messmer, E. S. B. M., Schmid-Tannwald, C. M., Zapp, D., & Kampik, A. (2010) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-010-1396-8 · Cited by 115 · see citing works
“Moreover, up to 40% of patients with previously diagnosed “idiopathic” neuropathy have, in fact, impaired glucose tolerance-related neuropathy, the earliest stage of diabetic neuropathy [ 2 ].”
BackgroundLü, B., Hu, J., Wen, J., Zhang, Z., Zhou, L., Li, Y., & Hu, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061053 · Cited by 111 · see citing works
“Many studies indicate that the prevalence of IGT is up to 40%– 50% in idiopathic neuropathy patients [7,8,12].”
BackgroundPathology and Quantitation of Cutaneous Innervation
Kennedy, W. R., Wendelschafer‐Crabb, G., Polydefkis, M. J., & McArthur, J. C. (2005) · Elsevier eBooks · doi:10.1016/b978-0-7216-9491-7.50037-5 · Cited by 105 · see citing works
Entrapment neuropathies in diabetes mellitus
Rota, E., & Morelli, N. (2016) · World Journal of Diabetes · doi:10.4239/wjd.v7.i17.342 · Cited by 104 · see citing works
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 104 · see citing works
“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 102 · see citing works
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 · see citing works
“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 · see citing works
“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 96 · see citing works
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 · see citing works
“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 · see citing works
Noninvasive 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 · see citing works
“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.”
BackgroundClinical 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 92 · see citing works
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 · see citing works
“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 · see citing works
“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).”
InfluentialShi, Y., Liang, X., Zhang, H., Wu, Q., Qu, L., & Sun, Q. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2013.59 · Cited by 90 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Smith, A. G., & Singleton, J. R. (2012) · CONTINUUM Lifelong Learning in Neurology · doi:10.1212/01.con.0000411568.34085.3e · Cited by 88 · see citing works
Self-citationPitcher, G. M., & Henry, J. L. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2003.10.019 · Cited by 84 · see citing works
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 84 · see citing works
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 · see citing works
“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 · see citing works
Kamiya, H., Zhang, W., & Sima, A. A. F. (2006) · Diabetologia · doi:10.1007/s00125-006-0379-0 · Cited by 79 · see citing works
“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 · see citing works
“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 76 · see citing works
Gill, H. K., Yadav, S., Ramesh, V., & Bhatia, E. (2014) · Journal of Postgraduate Medicine · doi:10.4103/0022-3859.138750 · Cited by 76 · see citing works
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 · see citing works
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 · see citing works
Pharmacological treatment of diabetic peripheral neuropathy.
Cohen, K., Shinkazh, N., Frank, J., Israel, I., & Fellner, C. (2015) · PubMed Central · Cited by 70 · see citing works
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 69 · see citing works
“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) · International Journal of Experimental Diabetes Research · doi:10.1155/2011/848307 · Cited by 66 · see citing works
“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 · see citing works
“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 · see citing works
- 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 › Neurology › Peripheral Neuropathies and Disorders
- Health Sciences › Medicine › Physiology › 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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