Prevalence of diabetic peripheral neuropathy and relation to glycemic control therapies at baseline in the BARI 2D cohort

Pop‐Busui, Rodica; Lu, Jiang; Lopes, Neuza; Jones, Teresa L. Z.

doi:10.1111/j.1529-8027.2009.00200.x

Cited by 133Diabetes Management and ResearchDiabetes Treatment and ManagementPain Mechanisms and Treatments

Prevalence of diabetic peripheral neuropathy and relation to glycemic control therapies at baseline in the BARI 2D cohort

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Pop‐Busui, Rodica, Lu, Jiang, Lopes, Neuza, Jones, Teresa L. Z.·2009·Journal of the Peripheral Nervous System

DOI 10.1111/j.1529-8027.2009.00200.xPMC PMC2692660

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Abstract

Abstract We evaluated the associations between glycemic therapies and prevalence of diabetic peripheral neuropathy (DPN) at baseline among participants in the Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D) trial on medical and revascularization therapies for coronary artery disease (CAD) and on insulin‐sensitizing vs. insulin‐providing treatments for diabetes. A total of 2,368 patients with type 2 diabetes and CAD was evaluated. DPN was defined as clinical examination score >2 using the Michigan Neuropathy Screening Instrument (MNSI). DPN odds ratios across different groups of glycemic therapy were evaluated by multiple logistic regression adjusted for multiple covariates including age, sex, hemoglobin A1c (HbA1c), and diabetes duration. Fifty‐one percent of BARI 2D subjects with valid baseline characteristics and MNSI scores had DPN. After adjusting for all variables, use of insulin was significantly associated with DPN (OR = 1.57, 95% CI: 1.15–2.13). Patients on sulfonylurea (SU) or combination of SU/metformin (Met)/thiazolidinediones (TZD) had marginally higher rates of DPN than the Met/TZD group. This cross‐sectional study in a cohort of patients with type 2 diabetes and CAD showed association of insulin use with higher DPN prevalence, independent of disease duration, glycemic control, and other characteristics. The causality between a glycemic control strategy and DPN cannot be evaluated in this cross‐sectional study, but continued assessment of DPN and randomized therapies in BARI 2D trial may provide further explanations on the development of DPN.

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In type 2 diabetes mellitus, enhanced glycemic control has been demonstrated to more modestly reduce the risk of developing diabetic peripheral neuropathy by 5%-9%.
“In type 2 DM, enhanced glycemic control has been demonstrated to more modestly reduce the risk of developing, by DPN 5%–9%.14 15 32”
From Glucose time in range and peripheral neuropathy in type 2 diabetes mellitus and chronic kidney disease (2020) · cites this paper as [14]

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Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33)
(1998) · The Lancet · doi:10.1016/s0140-6736(98)07019-6 · Cited by 20,023 · see citing works
Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group.
Turner, R. C., Fox, C., Matthews, McElroy, H. H., Cull, C. A., Holman, R. R., Neil, P., Hadden, D. R., Wright, D., Manley, E., et al. (1998) · The Lancet · Cited by 8,419 · see citing works
Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34)
(1998) · The Lancet · doi:10.1016/s0140-6736(98)07037-8 · Cited by 8,247 · see citing works
Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group.
(1998) · PubMed · Cited by 4,290 · see citing works
Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study.
Ohkubo, Y., Kishikawa, H., Araki, E., Miyata, T., Isami, S., Motoyoshi, S., Kojima, Y., Furuyoshi, N., & Shichiri, M. (1995) · Diabetes Research and Clinical Practice · doi:10.1016/0168-8227(95)01064-k · Cited by 3,079 · see citing works
Diabetic Neuropathies
Boulton, A. J. M., Vinik, A. I., Arezzo, J. C., Bril, V., Feldman, E. L., Freeman, R., Malik, R. A., Maser, R. E., Sosenko, J. M., & Ziegler, D. (2005) · Diabetes Care · doi:10.2337/diacare.28.4.956 · Cited by 1,859 · see citing works
A Practical Two-Step Quantitative Clinical and Electrophysiological Assessment for the Diagnosis and Staging of Diabetic Neuropathy
Feldman, E. L., Stevens, M. J., Thomas, P. K., Brown, M. B., Canal, N., & Greene, D. A. (1994) · Diabetes Care · doi:10.2337/diacare.17.11.1281 · Cited by 1,291 · see citing works
Diabetes Mellitus and Its Degenerative Complications: A Prospective Study of 4,400 Patients Observed Between 1947 and 1973
Pirart, J. (1978) · Diabetes Care · doi:10.2337/diacare.1.3.168 · Cited by 1,290 · see citing works
Longitudinal assessment of diabetic polyneuropathy using a composite score in the Rochester Diabetic Neuropathy Study cohort
Dyck, P. J., Davies, J. L., Litchy, W. J., & O’Brien, P. C. (1997) · Neurology · doi:10.1212/wnl.49.1.229 · Cited by 381 · see citing works
Neuropathy among the diabetes control and complications trial cohort 8 years after trial completion
Martin, C. L., Albers, J., Herman, W. H., Cleary, P., Waberski, B., Greene, D. A., Stevens, M. J., & Feldman, E. L. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1549 · Cited by 350 · see citing works
The effect of intensive diabetes therapy on measures of autonomic nervous system function in the Diabetes Control and Complications Trial (DCCT)
Not Available, N. A. (1998) · Diabetologia · doi:10.1007/s001250050924 · Cited by 308 · see citing works
Diabetic Peripheral Neuropathy and Depressive Symptoms
Vileikytė, L., Leventhal, H., Gonzalez, J. S., Peyrot, M. F., Rubin, R. R., Ulbrecht, J. S., Garrow, A. P., Waterman, C. G., Cavanagh, P. R., & Boulton, A. J. M. (2005) · Diabetes Care · doi:10.2337/diacare.28.10.2378 · Cited by 286 · see citing works
Diabetic neuropathy and oxidative stress
Pop‐Busui, R., Sima, A. A. F., & Stevens, M. J. (2006) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.625 · Cited by 286 · see citing works
Self-citation
Effect of intensive diabetes treatment on nerve conduction in the diabetes control and complications trial
DCCT Research Group, B. N. (1995) · Annals of Neurology · doi:10.1002/ana.410380607 · Cited by 283 · see citing works
Endothelial inflammation in insulin resistance
SJOHOLM, A., & NYSTROM, T. (2005) · The Lancet · doi:10.1016/s0140-6736(05)70804-7 · Cited by 278 · see citing works
Endothelial inflammation in insulin resistance
Sjöholm, Å., & Nyström, T. (2005) · The Lancet · doi:10.1016/s0140-6736(05)17912-4 · Cited by 277 · see citing works
Metformin Prevents High-Glucose–Induced Endothelial Cell Death Through a Mitochondrial Permeability Transition-Dependent Process
Detaille, D., Guigas, B., Chauvin, C., Batandier, C., Fontaine, E., Wiernsperger, N., & Leverve, X. (2005) · Diabetes · doi:10.2337/diabetes.54.7.2179 · Cited by 263 · cited 2× · see citing works
“, 1990), prevention of oxidative stress-induced endothelial cell death (Detaille et al., 2005), and direct neuroprotective effects via inhibition of oxidative stress-related apoptotic cell death in primary neurons (El-Mir et al.”
Background
Effect of Metformin on Carbohydrate and Lipoprotein Metabolism in NIDDM Patients
Wu, M. ‐., Johnston, P., Sheu, W. H., Hollenbeck, C. B., Jeng, C., Goldfine, I. D., Chen, Y. D., & Reaven, G. M. (1990) · Diabetes Care · doi:10.2337/diacare.13.1.1 · Cited by 257 · see citing works
Neuroprotective Role of Antidiabetic Drug Metformin Against Apoptotic Cell Death in Primary Cortical Neurons
El‐Mir, M., Détaille, D., R-Villanueva, G., Delgado‐Esteban, M., Guigas, B., Attia, S., Fontaine, E. M., Almeida, Á., & Leverve, X. M. (2007) · Journal of Molecular Neuroscience · doi:10.1007/s12031-007-9002-1 · Cited by 243 · see citing works
[Diabetes mellitus and its degenerative complications: a prospective study of 4,400 patients observed between 1947 and 1973 (2nd part) (author's transl)].
Pirart, J. (1977) · PubMed · Cited by 220 · see citing works
Angiotensin II Regulation of Collagen Type I Expression in Cardiac Fibroblasts
Chen, K., Chen, J., Li, D., Zhang, X., & Mehta, J. L. (2004) · Hypertension · doi:10.1161/01.hyp.0000144400.49062.6b · Cited by 148 · see citing works
The Effects of Intensive Glycemic Control on Neuropathy in the VA Cooperative Study on Type II Diabetes Mellitus (VA CSDM)
Azad, N., Emanuele, N., Abraira, C., Henderson, W. G., Colwell, J. A., Levin, S. R., Nuttall, F. Q., Comstock, J. P., Sawin, C. T., Silbert, C. K., et al. (1999) · Journal of Diabetes and its Complications · doi:10.1016/s1056-8727(99)00062-8 · Cited by 127 · see citing works
Activation of cerebral peroxisome proliferator-activated receptors gamma exerts neuroprotection by inhibiting oxidative stress following pilocarpine-induced status epilepticus
Yu, X., Shao, X., Sun, H. B., Li, Y., Yang, J., Deng, Y., & Huang, Y. (2008) · Brain Research · doi:10.1016/j.brainres.2008.01.047 · Cited by 97 · see citing works
Risk Factors For Distal Symmetric Neuropathy in NIDDM: The San Luis Valley Diabetes Study
Franklin, G. M., Shetterly, S. M., Cohen, J. A., Baxter, J., & Hamman, R. F. (1994) · Diabetes Care · doi:10.2337/diacare.17.10.1172 · Cited by 97 · see citing works
C-peptide corrects endoneurial blood flow but not oxidative stress in type 1 BB/Wor rats
Stevens, M. J., Zhang, W., Li, F. Y., & Sima, A. A. F. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00048.2004 · Cited by 89 · see citing works
Correction of protein kinase C activity and macrophage migration in peripheral nerve by pioglitazone, peroxisome proliferator activated‐γ‐ligand, in insulin‐deficient diabetic rats
Yamagishi, S., Ogasawara, S., Mizukami, H., Yajima, N., Wada, R., Sugawara, A., & Yagihashi, S. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05050.x · Cited by 86 · see citing works
Neuroprotection with pioglitazone against LPS insult on dopaminergic neurons may be associated with its inhibition of NF-κB and JNK activation and suppression of COX-2 activity
Xing, B., Liu, M., & Bing, G. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2007.09.029 · Cited by 78 · see citing works
Natural Progression of Diabetic Peripheral Neuropathy in the Zenarestat Study Population
Brown, M. J., Bird, S. J., Watling, S., Kaleta, H., Hayes, L., Eckert, S., & Foyt, H. L. (2004) · Diabetes Care · doi:10.2337/diacare.27.5.1153 · Cited by 78 · see citing works
Baseline characteristics of patients with diabetes and coronary artery disease enrolled in the Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D) trial
The BARI 2D Study Group (2008) · American Heart Journal · doi:10.1016/j.ahj.2008.05.015 · Cited by 58 · see citing works
Textbook of Diabetic Neuropathy
Brown, M. J. (2004) · Annals of Internal Medicine · doi:10.7326/0003-4819-141-3-200408030-00030 · Cited by 50 · see citing works
Mitochondrial ATP-Sensitive Potassium Channel: A Novel Site for Neuroprotection
Yamauchi, T., Kashii, S., Yasuyoshi, H., Zhang, S., Honda, Y., & Akaike, A. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-0815 · Cited by 47 · see citing works
Neuroprotective effect of the new thiadiazolidinone NP00111 against oxygen-glucose deprivation in rat hippocampal slices: Implication of ERK1/2 and PPARγ receptors
Rosa, A. O., Egea, J., Martı́nez, A., et al. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.03.008 · Cited by 28 · see citing works
Risk Factors for Lower Limb Complications in Diabetic Patients
El-Shazly, M. K., Abdel-Fattah, M. M., Scorpiglione, N., Benedetti, M. M., Capani, F., Carinci, F., Carta, Q., Cavaliere, D., Feo, E. M. D., Taboga, C., et al. (1998) · Journal of Diabetes and its Complications · doi:10.1016/s1056-8727(97)00001-9 · Cited by 27 · see citing works
Increased complications in noninsulin-dependent diabetic patients treated with insulin versus oral hypoglycemic agents: a population study.
Savage, S., Estacio, R., Jeffers, B., et al. (1997) · PubMed · Cited by 25 · see citing works
Potentiating effect of the ATP-sensitive potassium channel blocker glibenclamide on complex I inhibitor neurotoxicity in vitro and in vivo
Kou, J., Klorig, D. C., & Bloomquist, J. R. (2006) · NeuroToxicology · doi:10.1016/j.neuro.2006.04.004 · Cited by 18 · see citing works

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Pop-Busui R Stevens M Cheta D Insulin and cardiovascular disease in type 2 diabetes Vascular Involvement in Diabetes 2005 653 668 Karger Basel, Bucharest, Freiburg, Paris, London, New York

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Self-citation
Prevalence and Characteristics of Painful Diabetic Neuropathy in a Large Community-Based Diabetic Population in the U.K.
Abbott, C. A., Malik, R. A., van Ross, E. R. E., Kulkarni, J., & Boulton, A. J. M. (2011) · Diabetes Care · doi:10.2337/dc11-1108 · Cited by 868 · see citing works
Mechanism of diabetic neuropathy: Where are we now and where to go?
Yagihashi, S., Mizukami, H., & Sugimoto, K. (2011) · Journal of Diabetes Investigation · doi:10.1111/j.2040-1124.2010.00070.x · Cited by 488 · see citing works
Sex differences in micro- and macro-vascular complications of diabetes mellitus
Maric-Bilkan, C. (2017) · Clinical Science · doi:10.1042/cs20160998 · Cited by 217 · see citing works
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Pop-Busui, R., Lu, J., Brooks, M. M., Albert, S., Althouse, A. D., Escobedo, J., Green, J., Palumbo, P., Perkins, B. A., Whitehouse, F., et al. (2013) · Diabetes Care · doi:10.2337/dc13-0012 · Cited by 167 · see citing works
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Mayeda, L., Katz, R., Ahmad, I., Bansal, N., Batacchi, Z., Hirsch, I. B., Robinson, N., Trence, D. L., Zelnick, L., & de Boer, I. H. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2019-000991 · Cited by 162 · see citing works
Skin Advanced Glycation End Products Glucosepane and Methylglyoxal Hydroimidazolone Are Independently Associated With Long-term Microvascular Complication Progression of Type 1 Diabetes
Genuth, S., Sun, W., Cleary, P., Gao, X., Sell, D. R., Lachin, J., The DCCT/EDIC Research Group, & Monnier, V. M. (2015) · Diabetes · doi:10.2337/db14-0215 · Cited by 146 · see citing works
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Truini, A., Spallone, V., Morganti, R., Tamburin, S., Zanette, G., Schenone, A., De Michelis, C., Tugnoli, V., Simioni, V., Manganelli, F., et al. (2018) · Pain · doi:10.1097/j.pain.0000000000001378 · Cited by 85 · see citing works

Authors: Pop‐Busui, R., Lu, J., Lopes, N., & Jones, T. L. Z.
Affiliations: University of Michigan (US)
University of Pittsburgh (US)
Universidade de São Paulo (BR)
National Institutes of Health (US)
Corresponding author: Pop‐Busui, Rodica
ORCID: Pop‐Busui, Rodica
Lu, Jiang
Lopes, Neuza
Jones, Teresa L. Z.
Venue: Journal of the Peripheral Nervous System
Publisher: Wiley
Published: 2009-03
Volume: 14
Issue: 1
Pages: 1-13
ISSN: 1085-9489 (ISSN-L)
1529-8027
DOI: 10.1111/j.1529-8027.2009.00200.x
PMC: PMC2692660
OpenAlex: W2152877006
Cited by: 133
References: 35
Citations by year: 2026: 2 · 2025: 5 · 2024: 2 · 2023: 10 · 2022: 18 · 2021: 11 · 2020: 8 · 2019: 8 · 2018: 11 · 2017: 12 · 2016: 11 · 2015: 2 · 2014: 4 · 2013: 9 · 2012: 10
FWCI: 4.86
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 17 d)
Locations: Journal of the Peripheral Nervous System (publishedVersion)
PubMed (publishedVersion)
Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
PubMed Central (acceptedVersion)
Deep Blue (University of Michigan) (submittedVersion)
Funders: National Institutes of Health (UL1TR000454)
National Heart, Lung, and Blood Institute (U01HL063804, U01HL061748, U01HL061744, U01HL061746)
National Center for Advancing Translational Sciences
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Keywords: diabetic peripheral neuropathy, glycemic control, type 2 diabetes, coronary artery disease, insulin therapy, sulfonylureas, metformin, thiazolidinediones, insulin sensitizers, BARI 2D trial, Michigan Neuropathy Screening Instrument, prevalence
MeSH terms: Adult, Aged, Coronary Artery Bypass, Coronary Artery Disease, Cross-Sectional Studies, Diabetes Mellitus, Type 2, Diabetic Neuropathies, Female, Glycated Hemoglobin, Humans, Hypoglycemic Agents, Insulin, Male, Metformin, Middle Aged, Neurologic Examination, Sulfonylurea Compounds, Cohort Studies, Prevalence, Logistic Models, Randomized Controlled Trials as Topic, Thiazolidinediones

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Prevalence of diabetic peripheral neuropathy and relation to glycemic control therapies at baseline in the BARI 2D cohort

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