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Published in: Diabetology & Metabolic Syndrome 1/2018

Open Access 01-12-2018 | Research

Nerve conduction study of the association between glycemic variability and diabetes neuropathy

Authors: Miho Akaza, Itaru Akaza, Tadashi Kanouchi, Tetsuo Sasano, Yuki Sumi, Takanori Yokota

Published in: Diabetology & Metabolic Syndrome | Issue 1/2018

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Abstract

Background

It remains unclear whether glycemic variability is related to diabetes microvascular disease, especially diabetes peripheral neuropathy (DPN). We investigated the association between glycemic variability and DPN with type 1 or 2 diabetes.

Methods

Forty patients (23 males and 17 females; aged 34–79 years) underwent continuous glucose monitoring (CGM) and a nerve conduction study (NCS). Glycemic variability was estimated by mean amplitude of glycemic excursions (MAGE) in CGM. DPN was quantitatively evaluated by NCS in the median, tibial, sural and medial plantar nerves.

Results

MAGE had a significantly positive correlation with disease duration and low-density lipoprotein cholesterol level (r = 0.462, p = 0.003; and r = 0.40, p = 0.011, respectively), and a significantly negative correlation with BMI and medial plantar compound nerve action potential amplitude (r = − 0.39, p = 0.012; and r = − 0.32, p = 0.042, respectively). Multivariate linear regression analysis with adjustment for clinical background showed that MAGE (β = − 0.49, p= 0.007) was independently associated with a higher risk of medial plantar neuropathy.

Conclusions

Glycemic variability may be an independent risk factor for DPN.
Literature
1.
go back to reference American Diabetes Association. Standards of medical care in diabetes-2017. Diabetes Care. 2017;40(Suppl. 1):S48–56.CrossRef American Diabetes Association. Standards of medical care in diabetes-2017. Diabetes Care. 2017;40(Suppl. 1):S48–56.CrossRef
2.
go back to reference Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, Cushman WC, Genuth S, Ismail-Beigi F, Grimm RH Jr, Probstfield JL, Simons-Morton DG, Friedewald WT. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, Cushman WC, Genuth S, Ismail-Beigi F, Grimm RH Jr, Probstfield JL, Simons-Morton DG, Friedewald WT. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef
3.
go back to reference Monnier L, Colette C, Owens DR. Integrating glycaemic variability in the glycaemic disorders of type 2 diabetes: a move towards a unified glucose tetrad concept. Diabetes Metab Res Rev. 2009;25:393–402.CrossRefPubMed Monnier L, Colette C, Owens DR. Integrating glycaemic variability in the glycaemic disorders of type 2 diabetes: a move towards a unified glucose tetrad concept. Diabetes Metab Res Rev. 2009;25:393–402.CrossRefPubMed
4.
go back to reference Gorst C, Kwok CS, Aslam S, et al. Long-term glycemic variability and risk of adverse outcomes: a systematic review and meta-analysis. Diabetes Care. 2015;38:2354–69.CrossRefPubMed Gorst C, Kwok CS, Aslam S, et al. Long-term glycemic variability and risk of adverse outcomes: a systematic review and meta-analysis. Diabetes Care. 2015;38:2354–69.CrossRefPubMed
5.
go back to reference Cardoso CRL, Leite NC, Moram CBM, Salles GF. Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes: the Rio de Janeiro type 2 diabetes cohort study. Cardiovasc Diabetol. 2018;17:33.CrossRefPubMed Cardoso CRL, Leite NC, Moram CBM, Salles GF. Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes: the Rio de Janeiro type 2 diabetes cohort study. Cardiovasc Diabetol. 2018;17:33.CrossRefPubMed
6.
go back to reference Su G, Mi S, Tao H, et al. Association of glycemic variability and the presence and severity of coronary artery disease in patients with type 2 diabetes. Cardiovasc Diabetol. 2011;10:19.CrossRefPubMedPubMedCentral Su G, Mi S, Tao H, et al. Association of glycemic variability and the presence and severity of coronary artery disease in patients with type 2 diabetes. Cardiovasc Diabetol. 2011;10:19.CrossRefPubMedPubMedCentral
7.
go back to reference Carrington AL, Shaw JE, Van Schie CH, Abbott CA, Vileikyte L, Boulton AJ. Can motor nerve conduction velocity predict foot problems in diabetic subjects over a 6-year outcome period? Diabetes Care. 2010;25:2010–5.CrossRef Carrington AL, Shaw JE, Van Schie CH, Abbott CA, Vileikyte L, Boulton AJ. Can motor nerve conduction velocity predict foot problems in diabetic subjects over a 6-year outcome period? Diabetes Care. 2010;25:2010–5.CrossRef
8.
go back to reference Boulton AJ, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care. 2004;27:1458–86.CrossRefPubMed Boulton AJ, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care. 2004;27:1458–86.CrossRefPubMed
9.
go back to reference Xu F, Zhao LH, Su JB, Chen T, Wang XQ, Chen JF, Wu G, Jin Y, Wang XH. The relationship between glycemic variability and diabetic peripheral neuropathy in type 2 diabetes with well-controlled HbA1c. Diabetol Metab Syndr. 2014;6:139.CrossRefPubMedPubMedCentral Xu F, Zhao LH, Su JB, Chen T, Wang XQ, Chen JF, Wu G, Jin Y, Wang XH. The relationship between glycemic variability and diabetic peripheral neuropathy in type 2 diabetes with well-controlled HbA1c. Diabetol Metab Syndr. 2014;6:139.CrossRefPubMedPubMedCentral
10.
go back to reference Oyibo SO, Prasad YD, Jackson NJ, Jude EB, Boulton AJ. The relationship between blood glucose excursions and painful diabetic peripheral neuropathy: a pilot study. Diabet Med. 2002;19:870–3.CrossRefPubMed Oyibo SO, Prasad YD, Jackson NJ, Jude EB, Boulton AJ. The relationship between blood glucose excursions and painful diabetic peripheral neuropathy: a pilot study. Diabet Med. 2002;19:870–3.CrossRefPubMed
11.
go back to reference Committee of the Japan Diabetes Society on the Diagnostic Criteria of Diabetes Mellitus, Seino Y, Nanjo K, Tajima N, Kadowaki T, Kashiwagi A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Haneda M, Ueki K. Report of the committee on the classification and diagnostic criteria of diabetes mellitus. J Diabetes Investig. 2010;19:212–28.CrossRef Committee of the Japan Diabetes Society on the Diagnostic Criteria of Diabetes Mellitus, Seino Y, Nanjo K, Tajima N, Kadowaki T, Kashiwagi A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Haneda M, Ueki K. Report of the committee on the classification and diagnostic criteria of diabetes mellitus. J Diabetes Investig. 2010;19:212–28.CrossRef
12.
go back to reference Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, Dills D, Kampik A, Pararajasegaram R, Verdaguer JT, Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRefPubMed Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, Dills D, Kampik A, Pararajasegaram R, Verdaguer JT, Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRefPubMed
13.
go back to reference Service FJ, Molnar GD, Rosevear JW, Ackerman E, Gatewood LC, Taylor WF. Mean amplitude of glycemic excursions, a measure of diabetic instability. Diabetes. 1970;19:644–55.CrossRefPubMed Service FJ, Molnar GD, Rosevear JW, Ackerman E, Gatewood LC, Taylor WF. Mean amplitude of glycemic excursions, a measure of diabetic instability. Diabetes. 1970;19:644–55.CrossRefPubMed
14.
go back to reference Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effect of fasting plasma glucose variability on the risk of retinopathy in type 2 diabetic patients: retrospective long-term follow-up. Diabetes Res Clin Pract. 2010;89:296–302.CrossRefPubMed Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effect of fasting plasma glucose variability on the risk of retinopathy in type 2 diabetic patients: retrospective long-term follow-up. Diabetes Res Clin Pract. 2010;89:296–302.CrossRefPubMed
15.
go back to reference Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effects of fasting plasma glucose variability and time-dependent glycemic control on the long-term risk of retinopathy in type 2 diabetic patients. Diabetes Res Clin Pract. 2011;91:e40–2.CrossRefPubMed Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effects of fasting plasma glucose variability and time-dependent glycemic control on the long-term risk of retinopathy in type 2 diabetic patients. Diabetes Res Clin Pract. 2011;91:e40–2.CrossRefPubMed
16.
go back to reference Kilpatrick ES, Rigby AS, Atkin SL. A1C variability and the risk of microvascular complications in type 1 diabetes: data from the diabetes control and complications trial. Diabetes Care. 2008;31:2198–202.CrossRefPubMedPubMedCentral Kilpatrick ES, Rigby AS, Atkin SL. A1C variability and the risk of microvascular complications in type 1 diabetes: data from the diabetes control and complications trial. Diabetes Care. 2008;31:2198–202.CrossRefPubMedPubMedCentral
17.
go back to reference Lin CC, Chen CC, Chen FN, Li CI, Liu CS, Lin WY, Yang SY, Lee CC, Li TC. Risks of diabetic nephropathy with variation in hemoglobin A1c and fasting plasma glucose. Am J Med. 2013;126:1017e1–10.CrossRef Lin CC, Chen CC, Chen FN, Li CI, Liu CS, Lin WY, Yang SY, Lee CC, Li TC. Risks of diabetic nephropathy with variation in hemoglobin A1c and fasting plasma glucose. Am J Med. 2013;126:1017e1–10.CrossRef
18.
go back to reference Ceriello A, De Cosmo S, Rossi MC, et al. Variability in HbA1c, blood pressure, lipid parameters and serum uric acid, and risk of development of chronic kidney disease in type 2 diabetes. Diabetes Obes Metab. 2017;19:1570–8.CrossRefPubMed Ceriello A, De Cosmo S, Rossi MC, et al. Variability in HbA1c, blood pressure, lipid parameters and serum uric acid, and risk of development of chronic kidney disease in type 2 diabetes. Diabetes Obes Metab. 2017;19:1570–8.CrossRefPubMed
19.
go back to reference Sartore G, Chilelli NC, Burlina S, Lapolla A. Association between glucose variability as assessed by continuous glucose monitoring (CGM) and diabetic retinopathy in type 1 and type 2 diabetes. Acta Diabetol. 2013;50:437–42.CrossRefPubMed Sartore G, Chilelli NC, Burlina S, Lapolla A. Association between glucose variability as assessed by continuous glucose monitoring (CGM) and diabetic retinopathy in type 1 and type 2 diabetes. Acta Diabetol. 2013;50:437–42.CrossRefPubMed
20.
go back to reference Xu W, Zhu Y, Yang X, Deng H, Yan J, Lin S, Yang H, Chen H, Weng J. Glycemic variability is an important risk factor for cardiovascular autonomic neuropathy in newly diagnosed type 2 diabetic patients. Int J Cardiol. 2016;215:263–8.CrossRefPubMed Xu W, Zhu Y, Yang X, Deng H, Yan J, Lin S, Yang H, Chen H, Weng J. Glycemic variability is an important risk factor for cardiovascular autonomic neuropathy in newly diagnosed type 2 diabetic patients. Int J Cardiol. 2016;215:263–8.CrossRefPubMed
21.
go back to reference Jun JE, Jin SM, Baek J, Oh S, Hur KY, Lee MS, Lee MK, Kim JH. The association between glycemic variability and diabetic cardiovascular autonomic neuropathy in patients with type 2 diabetes. Cardiovasc Diabetol. 2015;14:70.CrossRefPubMedPubMedCentral Jun JE, Jin SM, Baek J, Oh S, Hur KY, Lee MS, Lee MK, Kim JH. The association between glycemic variability and diabetic cardiovascular autonomic neuropathy in patients with type 2 diabetes. Cardiovasc Diabetol. 2015;14:70.CrossRefPubMedPubMedCentral
22.
go back to reference An JY, Park MS, Kim JS, Shon YM, Lee SJ, Kim YI, Lee KS, Kim BJ. Comparison of diabetic neuropathy symptom score and medial plantar sensory nerve conduction studies in diabetic patients showing normal routine nerve conduction studies. Intern Med. 2008;47:1395–8.CrossRefPubMed An JY, Park MS, Kim JS, Shon YM, Lee SJ, Kim YI, Lee KS, Kim BJ. Comparison of diabetic neuropathy symptom score and medial plantar sensory nerve conduction studies in diabetic patients showing normal routine nerve conduction studies. Intern Med. 2008;47:1395–8.CrossRefPubMed
23.
go back to reference Nodera H, Logigian EL, Herrmann DN. Class of nerve fiber involvement in sensory neuropathies: clinical characterization and utility of the plantar nerve action potential. Muscle Nerve. 2002;26:212–7.CrossRefPubMed Nodera H, Logigian EL, Herrmann DN. Class of nerve fiber involvement in sensory neuropathies: clinical characterization and utility of the plantar nerve action potential. Muscle Nerve. 2002;26:212–7.CrossRefPubMed
24.
go back to reference Oh SJ, Melo AC, Lee DK, Cichy SW, Kim DS, Demerci M, Seo JH, Claussen GC. Large-fiber neuropathy in distal sensory neuropathy with normal routine nerve conduction. Neurology. 2001;56:1570–2.CrossRefPubMed Oh SJ, Melo AC, Lee DK, Cichy SW, Kim DS, Demerci M, Seo JH, Claussen GC. Large-fiber neuropathy in distal sensory neuropathy with normal routine nerve conduction. Neurology. 2001;56:1570–2.CrossRefPubMed
25.
go back to reference Candrilli SD, Davis KL, Kan HJ, Lucero MA, Rousculp MD. Prevalence and the associated burden of illness of symptoms of diabetic peripheral neuropathy and diabetic retinopathy. J Diabetes Complicat. 2007;21:306–14.CrossRefPubMed Candrilli SD, Davis KL, Kan HJ, Lucero MA, Rousculp MD. Prevalence and the associated burden of illness of symptoms of diabetic peripheral neuropathy and diabetic retinopathy. J Diabetes Complicat. 2007;21:306–14.CrossRefPubMed
26.
go back to reference Wang DD, Bakhotmah BA, Hu FB, Alzahrani HA. Prevalence and correlates of diabetic peripheral neuropathy in a Saudi Arabic population: a crosssectional study. PLoS ONE. 2014;9:e106935.CrossRefPubMedPubMedCentral Wang DD, Bakhotmah BA, Hu FB, Alzahrani HA. Prevalence and correlates of diabetic peripheral neuropathy in a Saudi Arabic population: a crosssectional study. PLoS ONE. 2014;9:e106935.CrossRefPubMedPubMedCentral
27.
go back to reference Won JC, Kwon HS, Kim CH, Lee JH, Park TS, Ko KS, Cha BY. Prevalence and clinical characteristics of diabetic peripheral neuropathy in hospital patients with type 2 diabetes in Korea. Diabet Med. 2012;29:e290–6.CrossRefPubMed Won JC, Kwon HS, Kim CH, Lee JH, Park TS, Ko KS, Cha BY. Prevalence and clinical characteristics of diabetic peripheral neuropathy in hospital patients with type 2 diabetes in Korea. Diabet Med. 2012;29:e290–6.CrossRefPubMed
28.
go back to reference Siegelaar SE, Holleman F, Hoekstra JB, DeVries JH. Glucose variability; does it matter? Endocr Rev. 2010;31:171–82.CrossRefPubMed Siegelaar SE, Holleman F, Hoekstra JB, DeVries JH. Glucose variability; does it matter? Endocr Rev. 2010;31:171–82.CrossRefPubMed
29.
go back to reference Araki A, Iimuro S, Sakurai T, et al. Long-term multiple risk factor interventions in Japanese elderly diabetic patients: the Japanese Elderly Diabetes Intervention Trial–study design, baseline characteristics and effects of intervention. Geriatr Gerontol Int. 2012;12(Suppl 1):7–17.CrossRefPubMed Araki A, Iimuro S, Sakurai T, et al. Long-term multiple risk factor interventions in Japanese elderly diabetic patients: the Japanese Elderly Diabetes Intervention Trial–study design, baseline characteristics and effects of intervention. Geriatr Gerontol Int. 2012;12(Suppl 1):7–17.CrossRefPubMed
30.
go back to reference Araki A. Management of elderly patients with diabetes mellitus-lessons from the J-EDIT study. Nihon Ronen Igakkai Zasshi. 2015;52:4–11. Araki A. Management of elderly patients with diabetes mellitus-lessons from the J-EDIT study. Nihon Ronen Igakkai Zasshi. 2015;52:4–11.
31.
go back to reference Jamali R, Mohseni S. Differential neuropathies in hyperglycemic and hypoglycemic diabetic rats. J Neuropathol Exp Neurol. 2006;65:1118–25.CrossRefPubMed Jamali R, Mohseni S. Differential neuropathies in hyperglycemic and hypoglycemic diabetic rats. J Neuropathol Exp Neurol. 2006;65:1118–25.CrossRefPubMed
32.
go back to reference Zhang YP, Mei S, Yang J, Rodriguez Y, Candiotti KA. Acute hypoglycemia induces painful neuropathy and the treatment of coenzyme Q10. J Diabetes Res. 2016;2016:4593052.PubMed Zhang YP, Mei S, Yang J, Rodriguez Y, Candiotti KA. Acute hypoglycemia induces painful neuropathy and the treatment of coenzyme Q10. J Diabetes Res. 2016;2016:4593052.PubMed
34.
go back to reference Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes. 2003;52:2795–804.CrossRefPubMed Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes. 2003;52:2795–804.CrossRefPubMed
35.
go back to reference Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, Colette C. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.CrossRefPubMed Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, Colette C. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.CrossRefPubMed
Metadata
Title
Nerve conduction study of the association between glycemic variability and diabetes neuropathy
Authors
Miho Akaza
Itaru Akaza
Tadashi Kanouchi
Tetsuo Sasano
Yuki Sumi
Takanori Yokota
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2018
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/s13098-018-0371-0

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