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Role of oxidative stress in hearing impairment in patients with type two diabetes mellitus

Published online by Cambridge University Press:  09 February 2009

İ Aladag ,
A Eyibilen ,
M Güven ,
Ö Atış  and
Ü Erkokmaz
İ Aladag*
Affiliation:
Department of ORL, Faculty of Medicine, Gaziosmanpasa University, Tokat, Turkey
A Eyibilen
Affiliation:
Department of ORL, Faculty of Medicine, Gaziosmanpasa University, Tokat, Turkey
M Güven
Affiliation:
Department of ORL, Faculty of Medicine, Gaziosmanpasa University, Tokat, Turkey
Ö Atış
Affiliation:
Department of Biochemistry, Faculty of Medicine, Gaziosmanpasa University, Tokat, Turkey
Ü Erkokmaz
Affiliation:
Department of Biostatistics, Faculty of Medicine, Gaziosmanpasa University, Tokat, Turkey
*
Address for correspondence: Professor İbrahim Aladag, Gaziosmanpasa University, Medical Faculty, Department of Otorhinolaryngology, Tokat, Turkey. Fax: 90 356 213 31 79 E-mail: ibrahimal@hotmail.com
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Abstract

Objective:

Although many clinical investigations have found a relationship between hearing loss and diabetes mellitus, the pathophysiology of this effect remains controversial. To date, the mechanisms of hearing loss in diabetic patients have been explained in terms of microangiopathy, neuropathy and encephalopathy. However, many reports indicate that some diabetic complications are associated with oxidative stress related to the diabetes itself. In the present study, we hypothesised that oxidative stress may be a cause of hearing loss in diabetic patients.

Methods:

The study group comprised non-insulin dependent diabetic patients with no signs of microangiopathy or peripheral neuropathy. The control group comprised sex-, age- and body weight matched, non-diabetic subjects. Auditory function was evaluated using pure tone audiometry and tympanometry. Subjects with normal hearing and sensorineural hearing loss were included in the study, whereas subjects with conductive hearing loss were excluded. Both the study group (n = 63) and the control group (n = 37) were divided into subgroups based on the presence and absence of hearing loss. Oxidative stress was evaluated by measuring serum indicators of protein oxidation and lipid peroxidation, serum levels of nitric oxide and various non-enzymatic antioxidants, and the activity of various enzymatic antioxidants.

Results:

The non-insulin dependent diabetic patients had significantly higher serum levels of protein oxidation products, nitric oxide, enzymatic antioxidant activity (i.e. glutathione peroxidase and superoxide dismutase), compared with the control group (p < 0.05). When we compared the groups in relation to the presence of hearing loss, the nitric oxide level was significantly increased in the diabetic group with good hearing, compared with diabetic patients with hearing loss (p = 0.014). In the diabetic group, a clear, negative correlation was observed between serum levels of nitric oxide and vitamins C and E, and hearing impairment (r = −0.395, r = −0.318, r = −0.500, respectively). There was also a positive correlation between serum vitamin C concentrations and hearing levels in the control group (r = 0.417).

Conclusion:

These results suggest that oxidative stress may play an important role in hearing impairment in diabetic patients. In this process, increased protein oxidation appears to be more important than lipid peroxidation. Nitric oxide may have a protective effect on hearing, as may some nonenzymatic antioxidants such as vitamin C and E.

Keywords

Diabetes MellitusSensorineural Hearing LossOxidative Stress
Type
Main Articles
Information
The Journal of Laryngology & Otology , Volume 123 , Issue 9 , September 2009 , pp. 957 - 963
Copyright
Copyright © JLO (1984) Limited 2009

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References

1 Ravecca, F, Berrettini, S, Bruschini, L, Segnini, G, Sellari-Franceschini, S. Progressive sensorineural hearing loss: metabolic, hormonal and vascular etiology [in Italian]. Acta Otorhinolaryngol Ital 1998;18:42–50Google ScholarPubMed
2 de España, R, Biurrun, O, Lorente, J, Traserra, J. Hearing and diabetes. ORL J Otorhinolaryngol Relat Spec 1995;57:325–7CrossRefGoogle ScholarPubMed
3 Taylor, IG, Irwin, J. Some audiological aspects of diabetes mellitus. J Laryngol Otol 1978;92:99–113CrossRefGoogle ScholarPubMed
4 Cullen, JR, Cinnamond, MJ. Hearing loss in diabetics. J Laryngol Otol 1993;107:179–82CrossRefGoogle ScholarPubMed
5 Parving, A, Elberling, C, Balle, V, Parbo, J, Dejgaard, A, Parving, HH. Hearing disorders in patients with insulin-dependent diabetes mellitus. Audiology 1990;29:113–21CrossRefGoogle ScholarPubMed
6 Park, MS, Park, SW, Choi, JH. Distortion product otoacoustic emissions in diabetics with normal hearing. Scand Audiol Suppl 2001;52:148–51CrossRefGoogle Scholar
7 Di Leo, MA, Di Nardo, W, Cercone, S, Ciervo, A, Lo Monaco, M, Greco, AV et al. Cochlear dysfunction in IDDM patients with subclinical peripheral neuropathy. Diabetes Care 1997;20:824–8CrossRefGoogle ScholarPubMed
8 Lisowska, G, Namysłowski, G, Morawski, K, Strojek, K. Cochlear dysfunction and diabetic microangiopathy. Scand Audiol Suppl 2001;52:199–203CrossRefGoogle Scholar
9 Sasso, FC, Salvatore, T, Tranchino, G, Cozzolino, D, Caruso, AA, Persico, M et al. Cochlear dysfunction in type 2 diabetes: a complication independent of neuropathy and acute hyperglycemia. Metabolism 1999;48:1346–50CrossRefGoogle ScholarPubMed
10 Hunt, JV, Smith, CC, Wolff, SP. Autoxidative glycosylation and possible involvement of peroxides and free radicals in LDL modification by glucose. Diabetes 1990;39:1420–4CrossRefGoogle ScholarPubMed
11 Ramakrishna, V, Jailkhani, R. Oxidative stress in non-insulin-dependent diabetes mellitus (NIDDM) patients. Acta Diabetol 2008;45:41–6CrossRefGoogle ScholarPubMed
12 Bhatia, S, Shukla, R, Venkata Madhu, S, Kaur Gambhir, J, Madhava Prabhu, K. Antioxidant status, lipid peroxidation and nitric oxide end products in patients of type 2 diabetes mellitus with nephropathy. Clin Biochem 2003;36:557–62CrossRefGoogle ScholarPubMed
13 Baynes, JW, Thorpe, SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 1999;48:1–9CrossRefGoogle Scholar
14 Ha, H, Kim, KH. Role of oxidative stress in the development of diabetic nephropathy. Kidney Int Suppl 1995;51:18–21Google ScholarPubMed
15 Lehmann, R, Schleicher, ED. Molecular mechanism of diabetic nephropathy. Clin Chim Acta 2000;297:135–44CrossRefGoogle ScholarPubMed
16 Lowry, OH, Rosebrough, NJ, Farr, AL, Randall, RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–275CrossRefGoogle ScholarPubMed
17 Sun, Y, Oberley, LW, Li, Y. A simple method for clinical assay of superoxide dismutase. Clin Chem 1988;34:497–500CrossRefGoogle ScholarPubMed
18 Paglia, DE, Valentine, WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158–69Google ScholarPubMed
19 Esterbaur, H, Cheeseman, KH. Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 1990;186:407–421CrossRefGoogle Scholar
20 Levine, RL, Garland, D, Oliver, CN, Amici, A, Climent, I, Lenz, AG, Ahn, BW, Shaltiel, S, Stantman, ER. Determination of carbonyl content in oxidatively modified proteins. In: Packer L Glazer, A (Eds). Methods in Enzymology V 186, Oxygen Radicals in Biological Systems. New York, Academic Press 1990. pp. 464–478.Google Scholar
21 Cortas, NK, Wakid, NW. Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin Chem 1990;36:1440–1443CrossRefGoogle ScholarPubMed
22 Chisolm, TH, Willott, JF, Lister, JJ. The aging auditory system: anatomic and physiologic changes and implications for rehabilitation. Int J Audiol 2003;42:3–10CrossRefGoogle ScholarPubMed
23 Evans, P, Halliwell, B. Free radicals and hearing. Cause, consequence, and criteria. Ann N Y Acad Sci 1999;884:19–40CrossRefGoogle ScholarPubMed
24 Takumida, M, Anniko, M, Popa, R, Zhang, DM. Pharmacological models for inner ear therapy with emphasis on nitric oxide. Acta Otolaryngol 2001;121:16–20Google ScholarPubMed
25 Yamane, H, Nakai, Y, Takayama, M, Konishi, K, Iguchi, H, Nakagawa, T et al. The emergence of free radicals after acoustic trauma and strial blood flow. Acta Otolaryngol Suppl 1995;519:87–92CrossRefGoogle ScholarPubMed
26 Ohlemiller, KK, Wright, JS, Dugan, LL. Early elevation of cochlear reactive oxygen species following noise exposure. Audiol Neurootol 1999;4:229–36CrossRefGoogle ScholarPubMed
27 Hu, BH, Henderson, D, Nicotera, TM. Involvement of apoptosis in progression of cochlear lesion following exposure to intense noise. Hear Res 2002;166:62–71CrossRefGoogle ScholarPubMed
28 Gallou, G, Ruelland, A, Legras, B, Maugendre, D, Allannic, H, Cloarec, L. Plasma malondialdehyde in type 1 and type 2 diabetic patients. Clin Chim Acta 1993;214:227–34CrossRefGoogle ScholarPubMed
29 Altomare, E, Vendemiale, G, Chicco, D, Procacci, V, Cirelli, F. Increased lipid peroxidation in type 2 poorly controlled diabetic patients. Diabetes Metab 1992;18:264–71Google ScholarPubMed
30 Heistad, DD. Oxidative stress and vascular disease: 2005 Duff lecture. Arterioscler Thromb Vasc Biol 2006;26:689–95CrossRefGoogle ScholarPubMed
31 Mooradian, AD. Increased serum conjugated dienes in elderly diabetic patients. J Am Geriatr Soc 1991;39:571–4CrossRefGoogle ScholarPubMed
32 Kaji, H, Kurasaki, M, Ito, K, Saito, T, Saito, K, Niioka, T et al. Increased lipoperoxide value and glutathione peroxidase activity in blood plasma of type 2 (non-insulin-dependent) diabetic women [in English]. Klin Wochenschr 1985;63:765–8CrossRefGoogle ScholarPubMed
33 Griesmacher, A, Kindhauser, M, Andert, SE, Schreiner, W, Toma, C, Knoebl, P et al. Enhanced serum levels of thiobarbituric-acid-reactive substances in diabetes mellitus. Am J Med 1995;98:469–75CrossRefGoogle ScholarPubMed
34 Velázquez, E, Winocour, PH, Kesteven, P, Alberti, KG, Laker, MF. Relation of lipid peroxides to macrovascular disease in type 2 diabetes. Diabet Med 1991;8:752–8CrossRefGoogle ScholarPubMed
35 Miles, AM, Bohle, DS, Glassbrenner, PA, Hansert, B, Wink, DA, Grisham, MB. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J Biol Chem 1996;271:40–7CrossRefGoogle ScholarPubMed
36 Lüscher, TF, Noll, G. Endothelium dysfunction in the coronary circulation. J Cardiovasc Pharmacol 1994;24:16–26CrossRefGoogle ScholarPubMed
37 Evans, P, Halliwell, B. Free radicals and hearing. Cause, consequence, and criteria. Ann N Y Acad Sci 1999;884:19–40CrossRefGoogle ScholarPubMed
38 Seidman, MD, Shivapuja, BG, Quirk, WS. The protective effects of allopurinol and superoxide dismutase on noise-induced cochlear damage. Otolaryngol Head Neck Surg 1993;109:1052–6CrossRefGoogle ScholarPubMed
39 Elliott, TG, Cockcroft, JR, Groop, PH, Viberti, GC, Ritter, JM. Inhibition of nitric oxide synthesis in forearm vasculature of insulin-dependent diabetic patients: blunted vasoconstriction in patients with microalbuminuria. Clin Sci (Lond) 1993;85:687–93CrossRefGoogle ScholarPubMed
40 Brechtelsbauer, PB, Nuttall, AL, Miller, JM. Basal nitric oxide production in regulation of cochlear blood flow. Hear Res 1994;77:38–42CrossRefGoogle ScholarPubMed
41 Ren, T, Nuttall, AL, Miller, JM. ATP-induced cochlear blood flow changes involve the nitric oxide pathway. Hear Res 1997;112:87–94CrossRefGoogle ScholarPubMed
42 Cohen, RA. Role of nitric oxide in diabetic complications. Am J Ther 2005;12:499–502CrossRefGoogle ScholarPubMed
43 Durante, W, Sen, AK, Sunahara, FA. Impairment of endothelium-dependent relaxation in aortae from spontaneously diabetic rats. Br J Pharmacol 1988;94:463–8CrossRefGoogle ScholarPubMed
44 Mayhan, WG. Impairment of endothelium-dependent dilatation of the basilar artery during diabetes mellitus. Brain Res 1992;580:297–302CrossRefGoogle ScholarPubMed
45 Vanizor, B, Orem, A, Karahan, SC, Kiran, E, Erem, C, Aliyazicioğlu, R et al. Decreased nitric oxide end-products and its relationship with high density lipoprotein and oxidative stress in people with type 2 diabetes without complications. Diabetes Res Clin Pract 2001;54:33–9CrossRefGoogle ScholarPubMed
46 Aydin, A, Orhan, H, Sayal, A, Ozata, M, Sahin, G, Işimer, A. Oxidative stress and nitric oxide related parameters in type II diabetes mellitus: effects of glycemic control. Clin Biochem 2001;34:65–70CrossRefGoogle ScholarPubMed
47 Chiarelli, F, Cipollone, F, Romano, F, Tumini, S, Costantini, F, di Ricco, L et al. Increased circulating nitric oxide in young patients with type 1 diabetes and persistent microalbuminuria: relation to glomerular hyperfiltration. Diabetes 200l;49:1258–63CrossRefGoogle Scholar
48 Sharma, A, Kharb, S, Chugh, SN, Kakkar, R, Singh, GP. Evaluation of oxidative stress before and after control of glycemia and after vitamin E supplementation in diabetic patients. Metabolism 2000;49:160–2CrossRefGoogle ScholarPubMed
49 Matkovics, B, Varga, SI, Szabó, L, Witas, H. The effect of diabetes on the activities of the peroxide metabolism enzymes. Horm Metab Res 1982;14:77–9CrossRefGoogle ScholarPubMed
50 Rema, M, Mohan, V, Bhaskar, A, Shanmugasundaram, KR. Does oxidant stress play a role in diabetic retinopathy? Indian J Ophthalmol 1995;43:17–21Google ScholarPubMed
51 Matkovics, B, Kotormán, M, Varga, IS, Hai, DQ, Salgó, L, Novák, Z. Pro-antioxidant and rheologic studies in the blood of type 2 diabetic patients [in English]. Acta Physiol Hung 1997–8;85:107–12Google ScholarPubMed
52 Sundaram, RK, Bhaskar, A, Vijayalingam, S, Viswanathan, M, Mohan, R, Shanmugasundaram, KR. Antioxidant status and lipid peroxidation in type II diabetes mellitus with and without complications. Clin Sci (Lond) 1996;90:255–60CrossRefGoogle ScholarPubMed
53 Martín-Gallán, P, Carrascosa, A, Gussinye, M, Domínguez, C. Estimation of lipoperoxidative damage and antioxidant status in diabetic children: relationship with individual antioxidants. Free Radic Res 2005;39:933–42CrossRefGoogle ScholarPubMed
54 Peuchant, E, Brun, JL, Rigalleau, V, Dubourg, L, Thomas, MJ, Daniel, JY et al. Oxidative and antioxidative status in pregnant women with either gestational or type 1 diabetes. Clin Biochem 2004;37:293–8CrossRefGoogle ScholarPubMed
55 Ford, ES, Mokdad, AH, Giles, WH, Brown, DW. The metabolic syndrome and antioxidant concentrations: findings from the Third National Health and Nutrition Examination Survey. Diabetes 2003;52:2346–52CrossRefGoogle ScholarPubMed
56 Nakamura, M, Ozaki, M, Fuchinoue, S, Teraoka, S, Ota, K. Ascorbic acid prevents ischemia-reperfusion injury in the rat small intestine. Transpl Int 1997;10:89–95CrossRefGoogle ScholarPubMed
57 Byrka-Owczarek, K, Steplewska-Mazur, K, Krasoń, M, Bohosiewicz, J, Koszutski, T, Wojtynek, G. The evaluation of the protective action of antioxidants on small intestine of rabbits experimentally injured by ischemia and reperfusion. J Pediatr Surg 2004;39:1226–9CrossRefGoogle ScholarPubMed
58 Shimizu, MH, Araujo, M, Borges, SM, de Tolosa, EM, Seguro, AC. Influence of age and vitamin E on post-ischemic acute renal failure. Exp Gerontol 2004;39:825–30CrossRefGoogle ScholarPubMed
59 Bursell, SE, Clermont, AC, Aiello, LP, Aiello, LM, Schlossman, DK, Feener, EP et al. High-dose vitamin E supplementation normalizes retinal blood flow and creatinine clearance in patients with type 1 diabetes. Diabetes Care 1999;22:1245–51CrossRefGoogle ScholarPubMed
60 Le, T, Keithley, EM. Effects of antioxidants on the aging inner ear. Hear Res 2007;226:194–202CrossRefGoogle ScholarPubMed