Skip to main content
Top
Published in: Journal of Translational Medicine 1/2017

Open Access 01-12-2017 | Research

Altered Semmes–Weinstein monofilament test results are associated with oxidative stress markers in type 2 diabetic subjects

Authors: Sergio Martinez-Hervás, Mercedes Molina Mendez, José Folgado, Carmen Tormos, Pilar Ascaso, Marta Peiró, Jose T. Real, Juan F. Ascaso

Published in: Journal of Translational Medicine | Issue 1/2017

Login to get access

Abstract

Background

Different lines of evidence suggest that oxidative stress (OS) is implicated in the pathogenesis of diabetic neuropathy. The Semmes–Weinstein monofilament (SWM) test is an efficient tool for evaluating diabetic polyneuropathy and diabetic foot. In this study, we analyzed the association between OS markers and altered SWM test results in type 2 diabetes (T2DM) patients.

Methods

Seventy T2DM patients were studied and 34 showed altered SWM results. The clinical and biochemical parameters were determined using standardized methods. Levels of oxidized glutathione (GSSG) and malondialdehyde (MDA) were measured in circulating mononuclear cells using high-performance liquid chromatography.

Results

We found that T2DM patients with altered SWM test results had significantly higher GSSG (3.53 ± 0.31 vs. 3.31 ± 0.35 mmol/ml, p < 0.05) and MDA (1.88 ± 0.16 vs. 1.75 ± 0.19 nmol/ml, p < 0.01) values compared to diabetic patients with normal SWM test outcomes. Moreover, altered SWM test results were independently related to age, glycosylated hemoglobin, and GSSG levels, but there was no association between OS markers and altered neuropathy sensitivity score (NSS) values.

Conclusions

Alteration of the glutathione system and MDA values in T2DM patients are associated with loss of proprioceptive (pressure) sensitivity, but not with symptomatic polyneuropathy (as evaluated by NSS). This finding may be important for understanding how OS affects distal symmetric polyneuropathy in diabetic patients.
Literature
1.
go back to reference England JD, Gronseth GS, Franklin G, Miller RG, Asbury AK, Carter GT, Cohen JA, Fisher MA, Howard JF, Kinsella LJ, et al. Distal symmetric polyneuropathy: a definition for clinical research: report of the American Academy of Neurology, the American Association of Electrodiagnostic Medicine, and the American Academy of Physical Medicine and Rehabilitation. Neurology. 2005;64(2):199–207.CrossRefPubMed England JD, Gronseth GS, Franklin G, Miller RG, Asbury AK, Carter GT, Cohen JA, Fisher MA, Howard JF, Kinsella LJ, et al. Distal symmetric polyneuropathy: a definition for clinical research: report of the American Academy of Neurology, the American Association of Electrodiagnostic Medicine, and the American Academy of Physical Medicine and Rehabilitation. Neurology. 2005;64(2):199–207.CrossRefPubMed
2.
3.
go back to reference Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615–25.CrossRefPubMed Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615–25.CrossRefPubMed
4.
go back to reference de Bandeira MS, da Fonseca LJ, da Guedes SG, Rabelo LA, Goulart MO, Vasconcelos SM. Oxidative stress as an underlying contributor in the development of chronic complications in diabetes mellitus. Int J Mol Sci. 2013;14(2):3265–84.CrossRefPubMedCentral de Bandeira MS, da Fonseca LJ, da Guedes SG, Rabelo LA, Goulart MO, Vasconcelos SM. Oxidative stress as an underlying contributor in the development of chronic complications in diabetes mellitus. Int J Mol Sci. 2013;14(2):3265–84.CrossRefPubMedCentral
5.
go back to reference Sugimoto K, Yasujima M, Yagihashi S. Role of advanced glycation end products in diabetic neuropathy. Curr Pharm Des. 2008;14(10):953–61.CrossRefPubMed Sugimoto K, Yasujima M, Yagihashi S. Role of advanced glycation end products in diabetic neuropathy. Curr Pharm Des. 2008;14(10):953–61.CrossRefPubMed
6.
go back to reference Aubert CE, Michel PL, Gillery P, Jaisson S, Fonfrede M, Morel F, Hartemann A, Bourron O. Association of peripheral neuropathy with circulating advanced glycation end products, soluble receptor for advanced glycation end products and other risk factors in patients with type 2 diabetes. Diabetes Metab Res Rev. 2014;30(8):679–85.CrossRefPubMed Aubert CE, Michel PL, Gillery P, Jaisson S, Fonfrede M, Morel F, Hartemann A, Bourron O. Association of peripheral neuropathy with circulating advanced glycation end products, soluble receptor for advanced glycation end products and other risk factors in patients with type 2 diabetes. Diabetes Metab Res Rev. 2014;30(8):679–85.CrossRefPubMed
7.
go back to reference Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404(6779):787–90.CrossRefPubMed Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404(6779):787–90.CrossRefPubMed
8.
go back to reference Schmeichel AM, Schmelzer JD, Low PA. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes. 2003;52(1):165–71.CrossRefPubMed Schmeichel AM, Schmelzer JD, Low PA. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes. 2003;52(1):165–71.CrossRefPubMed
9.
go back to reference Pop-Busui R, Sima A, Stevens M. Diabetic neuropathy and oxidative stress. Diabetes Metab Res Rev. 2006;22(4):257–73.CrossRefPubMed Pop-Busui R, Sima A, Stevens M. Diabetic neuropathy and oxidative stress. Diabetes Metab Res Rev. 2006;22(4):257–73.CrossRefPubMed
10.
go back to reference Vincent AM, Russell JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev. 2004;25(4):612–28.CrossRefPubMed Vincent AM, Russell JW, Low P, Feldman EL. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev. 2004;25(4):612–28.CrossRefPubMed
11.
go back to reference Obrosova IG. How does glucose generate oxidative stress in peripheral nerve? Int Rev Neurobiol. 2002;50:3–35.CrossRefPubMed Obrosova IG. How does glucose generate oxidative stress in peripheral nerve? Int Rev Neurobiol. 2002;50:3–35.CrossRefPubMed
12.
go back to reference Kasznicki J, Kosmalski M, Sliwinska A, Mrowicka M, Stanczyk M, Majsterek I, Drzewoski J. Evaluation of oxidative stress markers in pathogenesis of diabetic neuropathy. Mol Biol Rep. 2012;39(9):8669–78.CrossRefPubMedPubMedCentral Kasznicki J, Kosmalski M, Sliwinska A, Mrowicka M, Stanczyk M, Majsterek I, Drzewoski J. Evaluation of oxidative stress markers in pathogenesis of diabetic neuropathy. Mol Biol Rep. 2012;39(9):8669–78.CrossRefPubMedPubMedCentral
13.
go back to reference Merzouk S, Hichami A, Madani S, Merzouk H, Berrouiguet AY, Prost J, Moutairou K, Chabane-Sari N, Khan NA. Antioxidant status and levels of different vitamins determined by high performance liquid chromatography in diabetic subjects with multiple complications. Gen Physiol Biophys. 2003;22(1):15–27.PubMed Merzouk S, Hichami A, Madani S, Merzouk H, Berrouiguet AY, Prost J, Moutairou K, Chabane-Sari N, Khan NA. Antioxidant status and levels of different vitamins determined by high performance liquid chromatography in diabetic subjects with multiple complications. Gen Physiol Biophys. 2003;22(1):15–27.PubMed
14.
go back to reference Mendez MM, Folgado J, Tormo C, Artero A, Ascaso M, Martinez-Hervás S, Chaves FJ, Ascaso JF, Real JT. Altered glutathione system is associated with the presence of distal symmetric peripheral polyneuropathy in type 2 diabetic subjects. J Diabetes Complic. 2015;29(7):923–7.CrossRef Mendez MM, Folgado J, Tormo C, Artero A, Ascaso M, Martinez-Hervás S, Chaves FJ, Ascaso JF, Real JT. Altered glutathione system is associated with the presence of distal symmetric peripheral polyneuropathy in type 2 diabetic subjects. J Diabetes Complic. 2015;29(7):923–7.CrossRef
15.
go back to reference Standards of Medical Care in. Diabetes-2017: summary of Revisions. Diabetes Care. 2017;40(Suppl 1):S4–5. Standards of Medical Care in. Diabetes-2017: summary of Revisions. Diabetes Care. 2017;40(Suppl 1):S4–5.
16.
go back to reference Feng Y, Schlösser FJ, Sumpio BE. The Semmes Weinstein monofilament examination is a significant predictor of the risk of foot ulceration and amputation in patients with diabetes mellitus. J Vasc Surg. 2011;53(1):220–6.CrossRefPubMed Feng Y, Schlösser FJ, Sumpio BE. The Semmes Weinstein monofilament examination is a significant predictor of the risk of foot ulceration and amputation in patients with diabetes mellitus. J Vasc Surg. 2011;53(1):220–6.CrossRefPubMed
17.
go back to reference Boulton AJ. Guidelines for diagnosis and outpatient management of diabetic peripheral neuropathy. European Association for the Study of Diabetes, Neurodiab. Diabetes Metab. 1998;24(Suppl 3):55–65.PubMed Boulton AJ. Guidelines for diagnosis and outpatient management of diabetic peripheral neuropathy. European Association for the Study of Diabetes, Neurodiab. Diabetes Metab. 1998;24(Suppl 3):55–65.PubMed
18.
go back to reference Peripheral arterial disease in people with diabetes. American Diabetes Association. Comment Diabetes Care. 2004;27(8):2095. Peripheral arterial disease in people with diabetes. American Diabetes Association. Comment Diabetes Care. 2004;27(8):2095.
19.
go back to reference Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem. 1974;20(4):470–5.PubMed Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem. 1974;20(4):470–5.PubMed
20.
go back to reference Wahlefeld AW. Triglycerides: determiation after enzymatic hydrolisis. In: de Bergmeyer HU, editor. Methods of enzymatic analysis. New York: Academic Press, Inc; 1974. p. 1831–5.CrossRef Wahlefeld AW. Triglycerides: determiation after enzymatic hydrolisis. In: de Bergmeyer HU, editor. Methods of enzymatic analysis. New York: Academic Press, Inc; 1974. p. 1831–5.CrossRef
21.
go back to reference Burstein M, Scholnick HR, Morfin R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J Lipid Res. 1970;11(6):583–95.PubMed Burstein M, Scholnick HR, Morfin R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J Lipid Res. 1970;11(6):583–95.PubMed
22.
go back to reference Little RR. Glycated hemoglobin standardization–National Glycohemoglobin Standardization Program (NGSP) perspective. Clin Chem Lab Med. 2003;41(9):1191–8.CrossRefPubMed Little RR. Glycated hemoglobin standardization–National Glycohemoglobin Standardization Program (NGSP) perspective. Clin Chem Lab Med. 2003;41(9):1191–8.CrossRefPubMed
23.
go back to reference Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, Kusek JW, Van Lente F, Chronic Kidney Disease Epidemiology Collaboration. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med. 2006;145(4):247–54.CrossRefPubMed Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, Kusek JW, Van Lente F, Chronic Kidney Disease Epidemiology Collaboration. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med. 2006;145(4):247–54.CrossRefPubMed
24.
go back to reference Oltra AM, Carbonell F, Tormos C, Iradi A, Sáez GT. Antioxidant enzyme activities and the production of MDA and 8-oxo-dG in chronic lymphocytic leukemia. Free Radic Biol Med. 2001;30(11):1286–92.CrossRefPubMed Oltra AM, Carbonell F, Tormos C, Iradi A, Sáez GT. Antioxidant enzyme activities and the production of MDA and 8-oxo-dG in chronic lymphocytic leukemia. Free Radic Biol Med. 2001;30(11):1286–92.CrossRefPubMed
25.
go back to reference Navarro J, Obrador E, Pellicer JA, Aseni M, Viña J, Estrela JM. Blood glutathione as an index of radiation-induced oxidative stress in mice and humans. Free Radic Biol Med. 1997;22(7):1203–9.CrossRefPubMed Navarro J, Obrador E, Pellicer JA, Aseni M, Viña J, Estrela JM. Blood glutathione as an index of radiation-induced oxidative stress in mice and humans. Free Radic Biol Med. 1997;22(7):1203–9.CrossRefPubMed
26.
go back to reference Wong SH, Knight JA, Hopfer SM, Zaharia O, Leach CN Jr, Sunderman FW Jr. Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin Chem. 1987;33:214–20.PubMed Wong SH, Knight JA, Hopfer SM, Zaharia O, Leach CN Jr, Sunderman FW Jr. Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin Chem. 1987;33:214–20.PubMed
27.
28.
go back to reference Hayes JD, McLellan LI. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res. 1999;31(4):273–300.CrossRefPubMed Hayes JD, McLellan LI. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res. 1999;31(4):273–300.CrossRefPubMed
29.
go back to reference Iwata-Ichikawa E, Kondo Y, Miyazaki I, Asanuma M, Ogawa N. Glial cells protect neurons against oxidative stress via transcriptional up-regulation of the glutathione synthesis. J Neurochem. 1999;72(6):2334–44.CrossRefPubMed Iwata-Ichikawa E, Kondo Y, Miyazaki I, Asanuma M, Ogawa N. Glial cells protect neurons against oxidative stress via transcriptional up-regulation of the glutathione synthesis. J Neurochem. 1999;72(6):2334–44.CrossRefPubMed
30.
go back to reference Keelan J, Allen NJ, Antcliffe D, Pal S, Duchen MR. Quantitative imaging of glutathione in hippocampal neurons and glia in culture using monochlorobimane. J Neurosci Res. 2001;66(5):873–84.CrossRefPubMed Keelan J, Allen NJ, Antcliffe D, Pal S, Duchen MR. Quantitative imaging of glutathione in hippocampal neurons and glia in culture using monochlorobimane. J Neurosci Res. 2001;66(5):873–84.CrossRefPubMed
31.
go back to reference Little C, O’Brien PJ. An intracellular GSH-peroxidase with a lipid peroxide substrate. Biochem Biophys Res Commun. 1968;31(2):145–50.CrossRefPubMed Little C, O’Brien PJ. An intracellular GSH-peroxidase with a lipid peroxide substrate. Biochem Biophys Res Commun. 1968;31(2):145–50.CrossRefPubMed
32.
go back to reference El Boghdady NA, Badr GA. Evaluation of oxidative stress markers and vascular risk factors in patients with diabetic peripheral neuropathy. Cell Biochem Funct. 2012;30(4):328–34.CrossRefPubMed El Boghdady NA, Badr GA. Evaluation of oxidative stress markers and vascular risk factors in patients with diabetic peripheral neuropathy. Cell Biochem Funct. 2012;30(4):328–34.CrossRefPubMed
33.
go back to reference Ahmed FN, Naqvi FN, Shafiq F. Lipid peroxidation and serum antioxidant enzymes in patients with type 2 diabetes mellitus. Ann NY Acad Sci. 2006;1084:481–9.CrossRefPubMed Ahmed FN, Naqvi FN, Shafiq F. Lipid peroxidation and serum antioxidant enzymes in patients with type 2 diabetes mellitus. Ann NY Acad Sci. 2006;1084:481–9.CrossRefPubMed
34.
go back to reference Kesavulu MM, Giri R, Kameswara Rao B, Apparao C. Lipid peroxidation and antioxidant enzyme levels in type 2 diabetics with microvascular complications. Diabetes Metab. 2000;26(5):387–92.PubMed Kesavulu MM, Giri R, Kameswara Rao B, Apparao C. Lipid peroxidation and antioxidant enzyme levels in type 2 diabetics with microvascular complications. Diabetes Metab. 2000;26(5):387–92.PubMed
35.
go back to reference Kesavulu MM, Rao BK, Giri R, Vijaya J, Subramanyam G, Apparao C. Lipid peroxidation and antioxidant enzyme status in Type 2 diabetics with coronary heart disease. Diabetes Res Clin Pract. 2001;53(1):33–9.CrossRefPubMed Kesavulu MM, Rao BK, Giri R, Vijaya J, Subramanyam G, Apparao C. Lipid peroxidation and antioxidant enzyme status in Type 2 diabetics with coronary heart disease. Diabetes Res Clin Pract. 2001;53(1):33–9.CrossRefPubMed
36.
go back to reference Bolajoko EB, Mossanda KS, Adeniyi F, Akinosun O, Fasanmade A, Moropane M. Antioxidant and oxidative stress status in type 2 diabetes and diabetic foot. S Afr Med J. 2008;98(8):614–7.PubMed Bolajoko EB, Mossanda KS, Adeniyi F, Akinosun O, Fasanmade A, Moropane M. Antioxidant and oxidative stress status in type 2 diabetes and diabetic foot. S Afr Med J. 2008;98(8):614–7.PubMed
37.
go back to reference Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol. 2006;212(2):167–78.CrossRefPubMed Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol Appl Pharmacol. 2006;212(2):167–78.CrossRefPubMed
38.
go back to reference Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest. 2001;108(9):1341–8.CrossRefPubMedPubMedCentral Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest. 2001;108(9):1341–8.CrossRefPubMedPubMedCentral
39.
go back to reference Martínez-Blasco A, Bosch-Morell F, Trenor C, Romero FJ. Experimental diabetic neuropathy: role of oxidative stress and mechanisms involved. BioFactors. 1998;8(1–2):41–3.CrossRefPubMed Martínez-Blasco A, Bosch-Morell F, Trenor C, Romero FJ. Experimental diabetic neuropathy: role of oxidative stress and mechanisms involved. BioFactors. 1998;8(1–2):41–3.CrossRefPubMed
40.
go back to reference Pop-Busui R, Sullivan KA, Van Huysen C, Bayer L, Cao X, Towns R, Stevens MJ. Depletion of taurine in experimental diabetic neuropathy: implications for nerve metabolic, vascular, and functional deficits. Exp Neurol. 2001;168(2):259–72.CrossRefPubMed Pop-Busui R, Sullivan KA, Van Huysen C, Bayer L, Cao X, Towns R, Stevens MJ. Depletion of taurine in experimental diabetic neuropathy: implications for nerve metabolic, vascular, and functional deficits. Exp Neurol. 2001;168(2):259–72.CrossRefPubMed
41.
go back to reference van Dam PS, van Asbeck BS, Van Oirschot JF, Biessels GJ, Hamers FP, Marx JJ. Glutathione and alpha-lipoate in diabetic rats: nerve function, blood flow and oxidative state. Eur J Clin Invest. 2001;31(5):417–24.CrossRefPubMed van Dam PS, van Asbeck BS, Van Oirschot JF, Biessels GJ, Hamers FP, Marx JJ. Glutathione and alpha-lipoate in diabetic rats: nerve function, blood flow and oxidative state. Eur J Clin Invest. 2001;31(5):417–24.CrossRefPubMed
42.
go back to reference Low PA, Nickander KK, Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes. 1997;46(Suppl 2):S38–42.CrossRefPubMed Low PA, Nickander KK, Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes. 1997;46(Suppl 2):S38–42.CrossRefPubMed
43.
go back to reference Vareniuk I, Pavlov IA, Drel VR, Lyzogubov VV, Ilnytska O, Bell SR, Tibrewala J, Groves JT, Obrosova IG. Nitrosative stress and peripheral diabetic neuropathy in leptin-deficient (ob/ob) mice. Exp Neurol. 2007;205(2):425–36.CrossRefPubMed Vareniuk I, Pavlov IA, Drel VR, Lyzogubov VV, Ilnytska O, Bell SR, Tibrewala J, Groves JT, Obrosova IG. Nitrosative stress and peripheral diabetic neuropathy in leptin-deficient (ob/ob) mice. Exp Neurol. 2007;205(2):425–36.CrossRefPubMed
44.
go back to reference Kishi Y, Nickander KK, Schmelzer JD, Low PA. Gene expression of antioxidant enzymes in experimental diabetic neuropathy. J Peripher Nerv Syst. 2000;5(1):11–8.CrossRefPubMed Kishi Y, Nickander KK, Schmelzer JD, Low PA. Gene expression of antioxidant enzymes in experimental diabetic neuropathy. J Peripher Nerv Syst. 2000;5(1):11–8.CrossRefPubMed
45.
go back to reference Hamilton RT, Bhattacharya A, Walsh ME, Shi Y, Wei R, Zhang Y, Rodriguez KA, Buffenstein R, Chaudhuri AR, Van Remmen H. Elevated protein carbonylation, and misfolding in sciatic nerve from db/db and Sod1(-/-) mice: plausible link between oxidative stress and demyelination. PLoS ONE. 2013;8(6):e65725.CrossRefPubMedPubMedCentral Hamilton RT, Bhattacharya A, Walsh ME, Shi Y, Wei R, Zhang Y, Rodriguez KA, Buffenstein R, Chaudhuri AR, Van Remmen H. Elevated protein carbonylation, and misfolding in sciatic nerve from db/db and Sod1(-/-) mice: plausible link between oxidative stress and demyelination. PLoS ONE. 2013;8(6):e65725.CrossRefPubMedPubMedCentral
46.
go back to reference Russell JW, Berent-Spillson A, Vincent AM, Freimann CL, Sullivan KA, Feldman EL. Oxidative injury and neuropathy in diabetes and impaired glucose tolerance. Neurobiol Dis. 2008;30(3):420–9.CrossRefPubMedPubMedCentral Russell JW, Berent-Spillson A, Vincent AM, Freimann CL, Sullivan KA, Feldman EL. Oxidative injury and neuropathy in diabetes and impaired glucose tolerance. Neurobiol Dis. 2008;30(3):420–9.CrossRefPubMedPubMedCentral
47.
go back to reference Russell JW, Golovoy D, Vincent AM, Mahendru P, Olzmann JA, Mentzer A, Feldman EL. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 2002;16(13):1738–48.CrossRefPubMed Russell JW, Golovoy D, Vincent AM, Mahendru P, Olzmann JA, Mentzer A, Feldman EL. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 2002;16(13):1738–48.CrossRefPubMed
48.
go back to reference Kim ES, Isoda F, Kurland I, Mobbs CV. Glucose-induced metabolic memory in Schwann cells: prevention by PPAR agonists. Endocrinology. 2013;154(9):3054–66.CrossRefPubMedPubMedCentral Kim ES, Isoda F, Kurland I, Mobbs CV. Glucose-induced metabolic memory in Schwann cells: prevention by PPAR agonists. Endocrinology. 2013;154(9):3054–66.CrossRefPubMedPubMedCentral
49.
go back to reference Sampson MJ, Gopaul N, Davies IR, Hughes DA, Carrier MJ. Plasma F2 isoprostanes: direct evidence of increased free radical damage during acute hyperglycemia in type 2 diabetes. Diabetes Care. 2002;25(3):537–41.CrossRefPubMed Sampson MJ, Gopaul N, Davies IR, Hughes DA, Carrier MJ. Plasma F2 isoprostanes: direct evidence of increased free radical damage during acute hyperglycemia in type 2 diabetes. Diabetes Care. 2002;25(3):537–41.CrossRefPubMed
Metadata
Title
Altered Semmes–Weinstein monofilament test results are associated with oxidative stress markers in type 2 diabetic subjects
Authors
Sergio Martinez-Hervás
Mercedes Molina Mendez
José Folgado
Carmen Tormos
Pilar Ascaso
Marta Peiró
Jose T. Real
Juan F. Ascaso
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2017
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-017-1291-8

Other articles of this Issue 1/2017

Journal of Translational Medicine 1/2017 Go to the issue