Semin Hear 2019; 40(04): 292-299
DOI: 10.1055/s-0039-1697033
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Diabetes and Auditory-Vestibular Pathology

Saravanan Elangovan
1   Department of Audiology and Speech-Language Pathology, East Tennessee State University, Johnson City, Tennessee
,
Christopher Spankovich
2   Department of Otolaryngology and Communicative Sciences, University of Mississippi Medical Center, Jackson, Mississippi
› Author Affiliations
Further Information

Publication History

Publication Date:
09 October 2019 (online)

Abstract

The relationship between diabetes mellitus (DM) and the auditory/vestibular system has been investigated for more than a century. Most population-based investigations of hearing loss in persons with diabetes (PWD) have revealed a slow progressive, bilateral, high-frequency sensorineural hearing loss. Despite the growing research literature on the pathophysiology of DM-related hearing loss using various animal models and other human studies, knowledge of specific mechanism of the degenerative changes of the inner ear and/or auditory nerve is far from full elucidation. Recent investigations of the mechanisms underlying the association between hearing loss and DM suggest complex combined contributions of hyperglycemia, oxidative stress resulting in cochlear microangiopathy, and auditory neuropathy. An even lesser understood complication of DM is the effect on the vestibular system. Here we provide an overview of animal and human evidence of pathophysiological changes created by DM and its effects on auditory-vestibular anatomy and function.

 
  • References

  • 1 Kambayashi J, Kobayashi T, Marcus NY, DeMott JE, Thalmann I, Thalmann R. Minimal concentrations of metabolic substrates capable of supporting cochlear potentials. Hear Res 1982; 7 (01) 105-114
  • 2 Zuma e Maia FC, Lavinsky L. Distortion product otoacoustic emissions in an animal model of induced hyperinsulinemia. Int Tinnitus J 2006; 12 (02) 133-139
  • 3 Juhn SK, Youngs JN. The effect on perilymph of the alteration of serum glucose or calcium concentration. Laryngoscope 1976; 86 (02) 273-279
  • 4 Wang S, Schacht J. Insulin stimulates protein synthesis and phospholipid signaling systems but does not regulate glucose uptake in the inner ear. Hear Res 1990; 47 (1-2): 53-61
  • 5 Nageris B, Hadar T, Feinmesser M, Elidan J. Cochlear histopathologic analysis in diabetic rats. Am J Otol 1998; 19 (01) 63-65
  • 6 Liu H, Liu X, Jia L. , et al. Insulin therapy restores impaired function and expression of P-glycoprotein in blood-brain barrier of experimental diabetes. Biochem Pharmacol 2008; 75 (08) 1649-1658
  • 7 Smith TL, Raynor E, Prazma J, Buenting JE, Pillsbury HC. Insulin-dependent diabetic microangiopathy in the inner ear. Laryngoscope 1995; 105 (3, Pt 1): 236-240
  • 8 Raynor EM, Carrasco VN, Prazma J, Pillsbury HC. An assessment of cochlear hair-cell loss in insulin-dependent diabetes mellitus diabetic and noise-exposed rats. Arch Otolaryngol Head Neck Surg 1995; 121 (04) 452-456
  • 9 Wu HP, Cheng TJ, Tan CT, Guo YL, Hsu CJ. Diabetes impairs recovery from noise-induced temporary hearing loss. Laryngoscope 2009; 119 (06) 1190-1194
  • 10 Fowler PD, Jones NS. Diabetes and hearing loss. Clin Otolaryngol Allied Sci 1999; 24 (01) 3-8
  • 11 Triana RJ, Suits GW, Garrison S. , et al. Inner ear damage secondary to diabetes mellitus. I. Changes in adolescent SHR/N-cp rats. Arch Otolaryngol Head Neck Surg 1991; 117 (06) 635-640
  • 12 McQueen CT, Baxter A, Smith TL. , et al. Non-insulin-dependent diabetic microangiopathy in the inner ear. J Laryngol Otol 1999; 113 (01) 13-18
  • 13 Ishikawa T, Naito Y, Taniguchi K. Hearing impairment in WBN/Kob rats with spontaneous diabetes mellitus. Diabetologia 1995; 38 (06) 649-655
  • 14 Arteaga AA, Sandlin DS, Wang S. , et al. Diabetes-induced changes in auditory function in the T2DN rat. Association for Research in Otolaryngology-Midwinter Meeting; 2017 ; Baltimore, MD
  • 15 Nakae S, Tachibana M. The cochlea of the spontaneously diabetic mouse. II. Electron microscopic observations of non-obese diabetic mice. Arch Otorhinolaryngol 1986; 243 (05) 313-316
  • 16 Ohlemiller KK, Rice ME, Gagnon PM. Strial microvascular pathology and age-associated endocochlear potential decline in NOD congenic mice. Hear Res 2008; 244 (1-2): 85-97
  • 17 Vasilyeva ON, Frisina ST, Zhu X, Walton JP, Frisina RD. Interactions of hearing loss and diabetes mellitus in the middle age CBA/CaJ mouse model of presbycusis. Hear Res 2009; 249 (1-2): 44-53
  • 18 Fowler CG, Chiasson KB, Colman RJ, Kemnitz JW, Beasley TM, Weindruch RH. Hyperinsulinemia/diabetes, hearing, and aging in the University of Wisconsin calorie restriction monkeys. Hear Res 2015; 328: 78-86
  • 19 Frisina RD, Walton JP. Age-related structural and functional changes in the cochlear nucleus. Hear Res 2006; 216–217: 216-223
  • 20 Liu F, Xia M, Xu A. Expression of VEGF, iNOS, and eNOS is increased in cochlea of diabetic rat. Acta Otolaryngol 2008; 128 (11) 1178-1186
  • 21 Aladag I, Eyibilen A, Güven M, Atiş O, Erkorkmaz Ü. Role of oxidative stress in hearing impairment in patients with type two diabetes mellitus. J Laryngol Otol 2009; 123 (09) 957-963
  • 22 Choi SW, Benzie IF, Ma SW, Strain JJ, Hannigan BM. Acute hyperglycemia and oxidative stress: direct cause and effect?. Free Radic Biol Med 2008; 44 (07) 1217-1231
  • 23 Goodarzi MT, Varmaziar L, Navidi AA, Parivar K. Study of oxidative stress in type 2 diabetic patients and its relationship with glycated hemoglobin. Saudi Med J 2008; 29 (04) 503-506
  • 24 Henderson D, Bielefeld EC, Harris KC, Hu BH. The role of oxidative stress in noise-induced hearing loss. Ear Hear 2006; 27 (01) 1-19
  • 25 Fujita T, Yamashita D, Katsunuma S, Hasegawa S, Tanimoto H, Nibu K. Increased inner ear susceptibility to noise injury in mice with streptozotocin-induced diabetes. Diabetes 2012; 61 (11) 2980-2986
  • 26 Lee HS, Kim KR, Chung WH, Cho YS, Hong SH. Early sensorineural hearing loss in ob/ob mouse, an animal model of type 2 diabetes. Clin Exp Otorhinolaryngol 2008; 1 (04) 211-216
  • 27 Garcia-Quiroga J, Norris CH, Glade L, Bryant GM, Tachibana M, Guth PS. The relationship between kanamycin ototoxicity and glucose transport. Res Commun Chem Pathol Pharmacol 1978; 22 (03) 535-547
  • 28 Perez R, Ziv E, Freeman S, Sichel JY, Sohmer H. Vestibular end-organ impairment in an animal model of type 2 diabetes mellitus. Laryngoscope 2001; 111 (01) 110-113
  • 29 Myers SF, Tormey MC, Akl S. Morphometric analysis of horizontal canal nerves of chronically diabetic rats. Otolaryngol Head Neck Surg 1999; 120 (02) 174-179
  • 30 Myers SF, Ross MD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. II. Connective tissue and neuroepithelial pathology. Acta Otolaryngol 1987; 104 (1-2): 40-49
  • 31 Myers SF, Ross MD, Jokelainen P, Graham MD, McClatchey KD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. I. Microvascular changes. Acta Otolaryngol 1985; 100 (5-6): 351-364
  • 32 Konrad-Martin D, Austin DF, Griest S, McMillan GP, McDermott D, Fausti S. Diabetes-related changes in auditory brainstem responses. Laryngoscope 2010; 120 (01) 150-158
  • 33 Frisina ST, Mapes F, Kim S, Frisina DR, Frisina RD. Characterization of hearing loss in aged type II diabetics. Hear Res 2006; 211 (1-2): 103-113
  • 34 Anjaneyulu M, Berent-Spillson A, Russell JW. Metabotropic glutamate receptors (mGluRs) and diabetic neuropathy. Curr Drug Targets 2008; 9 (01) 85-93
  • 35 Kujawa SG, Liberman MC. Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 2009; 29 (45) 14077-14085
  • 36 Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, Creager MA. Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 1993; 88 (06) 2510-2516
  • 37 Jorgensen MB. The inner ear in diabetes mellitus. Histological studies. Arch Otolaryngol 1961; 74: 373-381
  • 38 Akinpelu OV, Ibrahim F, Waissbluth S, Daniel SJ. Histopathologic changes in the cochlea associated with diabetes mellitus--a review. Otol Neurotol 2014; 35 (05) 764-774
  • 39 Fioretto P, Mauer M. Histopathology of diabetic nephropathy. Semin Nephrol 2007; 27 (02) 195-207
  • 40 Fukushima H, Cureoglu S, Schachern PA. , et al. Cochlear changes in patients with type 1 diabetes mellitus. Otolaryngol Head Neck Surg 2005; 133 (01) 100-106
  • 41 Fukushima H, Cureoglu S, Schachern PA, Paparella MM, Harada T, Oktay MF. Effects of type 2 diabetes mellitus on cochlear structure in humans. Arch Otolaryngol Head Neck Surg 2006; 132 (09) 934-938
  • 42 Jorgensen MB. Changes of aging in the inner ear. Histological studies. Arch Otolaryngol 1961; 74: 164-170
  • 43 Kovar M. The inner ear in diabetes mellitus. ORL J Otorhinolaryngol Relat Spec 1973; 35 (01) 42-51
  • 44 Makishima K, Tanaka K. Pathological changes of the inner ear and central auditory pathway in diabetics. Ann Otol Rhinol Laryngol 1971; 80 (02) 218-228
  • 45 Rust KR, Prazma J, Triana RJ, Michaelis IV OE, Pillsbury HC. Inner ear damage secondary to diabetes mellitus. II. Changes in aging SHR/N-cp rats. Arch Otolaryngol Head Neck Surg 1992; 118 (04) 397-400
  • 46 Wackym PA, Linthicum Jr FH. Diabetes mellitus and hearing loss: clinical and histopathologic relationships. Am J Otol 1986; 7 (03) 176-182
  • 47 Edamatsu M, Kondo Y, Ando M. Multiple expression of glucose transporters in the lateral wall of the cochlear duct studied by quantitative real-time PCR assay. Neurosci Lett 2011; 490 (01) 72-77
  • 48 Rance G, Chisari D, O'Hare F. , et al. Auditory neuropathy in individuals with Type 1 diabetes. J Neurol 2014; 261 (08) 1531-1536
  • 49 Gupta S, Baweja P, Mittal S, Kumar A, Singh KD, Sharma R. Brainstem auditory evoked potential abnormalities in type 2 diabetes mellitus. N Am J Med Sci 2013; 5 (01) 60-65
  • 50 Vaughan N, James K, McDermott D, Griest S, Fausti S. Auditory brainstem response differences in diabetic and non-diabetic veterans. J Am Acad Audiol 2007; 18 (10) 863-871
  • 51 Mishra R, Sanju HK, Kumar P. Auditory temporal resolution in individuals with diabetes mellitus type 2. Int Arch Otorhinolaryngol 2016; 20 (04) 327-330
  • 52 Agrawal Y, Carey JP, Della Santina CC, Schubert MC, Minor LB. Disorders of balance and vestibular function in US adults: data from the National Health and Nutrition Examination Survey, 2001-2004. Arch Intern Med 2009; 169 (10) 938-944
  • 53 Yoda S, Cureoglu S, Yildirim-Baylan M. , et al. Association between type 1 diabetes mellitus and deposits in the semicircular canals. Otolaryngol Head Neck Surg 2011; 145 (03) 458-462
  • 54 Kocdor P, Kaya S, Erdil M, Cureoglu S, Paparella MM, Adams ME. Vascular and neuroepithelial histopathology of the saccule in humans with diabetes mellitus. Otol Neurotol 2016; 37 (05) 553-557