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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 26  |  Issue : 4  |  Page : 240-246

Effect of time since diagnosis of type 2 diabetes mellitus and glycemic control on distortion-product otoacoustic emissions


Department of Otorhinolaryngology, Kasturba Medical College, Mangalore, Manipal Academy of Higher Education, Karnataka, India

Date of Submission04-Jan-2020
Date of Decision03-Mar-2020
Date of Acceptance11-Mar-2020
Date of Web Publication23-Apr-2021

Correspondence Address:
Dr. Vijendra S Shenoy
Professor and Head, Department of Otorhinolaryngology, Kasturba Medical College, Mangalore, Manipal Academy of Higher Education, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/indianjotol.INDIANJOTOL_2_20

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  Abstract 


Objectives: The objective of this study is to analyze the effect of glycemic control and factors like time since the diagnosis of type 2 diabetes mellitus on hearing. Materials and Methods: Hearing of 75 type 2 diabetes mellitus patients aged 40–55 years categorized into three groups of 25 patients based on their glycemic control (HbA1c %) and also based on time since the diagnosis was assessed using pure-tone audiometry (PTA) and distortion-product otoacoustic emissions (DPOAE). Results: Of 68% of the study population showing hearing loss, 40 patients (76.92%) had sensorineural hearing loss (SNHL) and 11 patients showed mixed hearing loss. The highest incidence of SNHL was seen in patients with poor glycemic control (45%) (P = 0.01) and in those with longer duration of diabetes >10 years (50%). Maximum patients showed moderate-to-moderately severe degree of hearing loss, affecting higher frequencies (P < 0.05). Bilateral SNHL was observed in 24% of patients. The absence of DPOAE was seen statistically significantly more in patients with uncontrolled glycemic control (P = 0.008) and those with the duration of diabetes of 5–10 years, affecting mid-to-high frequencies (2 and 8 kHz) (P < 0.01). Our study showed nine patients with normal PTA thresholds with absent DPOAE's. Age showed a statistically significant correlation in DPOAE outcomes with respect to glycemic control only (P = 0.038). Patients on treatment with both insulin and oral hypoglycemic agents showed the highest incidence of hearing loss but with no significant correlation. Conclusion: Patients with poor and uncontrolled glycemic control are likely to have more hearing loss. Subclinical hearing loss due to cochlear dysfunction seen commonly in patients with diabetes can be detected earliest with the aid of otoacoustic emissions in conjunction with PTA.

Keywords: Distortion-product otoacoustic emissions, glycosylated hemoglobin, pure-tone audiometry, time since diagnosis of diabetes


How to cite this article:
Shetty D, Kamath PM, Shenoy VS, Rai T, Bhat JS. Effect of time since diagnosis of type 2 diabetes mellitus and glycemic control on distortion-product otoacoustic emissions. Indian J Otol 2020;26:240-6

How to cite this URL:
Shetty D, Kamath PM, Shenoy VS, Rai T, Bhat JS. Effect of time since diagnosis of type 2 diabetes mellitus and glycemic control on distortion-product otoacoustic emissions. Indian J Otol [serial online] 2020 [cited 2021 Dec 3];26:240-6. Available from: https://www.indianjotol.org/text.asp?2020/26/4/240/314348




  Introduction Top


Type 2 diabetes mellitus constitutes 90%–95% of individuals diagnosed with diabetes in the world (the American Diabetic Association, 2017). These patients have higher risks of developing microvascular and macrovascular complications at an earlier stage and with greater frequency as compared to type 1 diabetes mellitus. They are diagnosed frequently when complications develop among which auditory disorders are the most common, although the literature data contain conflicting evidence of correlation of hearing loss with diabetes. Previous studies show a higher frequency of sensorineural hearing loss (SNHL) in patients with diabetes as compared to the general population, explained by the documented neuropathic and microvascular complications of diabetes mellitus with precarious and complex blood supply of the inner ear.[1] Possible pathogenesis noted was diffuse thickening of the basement membrane of capillaries of stria vascularis seen in animal studies.[2] The most commonly used audiological test to evaluate the hearing is pure-tone audiometry (PTA). Most audiometric studies of hearing in patients with diabetes show mild-to-moderate high-frequency hearing loss in patients with diabetes.[3] Otoacoustic emissions (OAE) testing is a useful audiometric test for diagnosing cochlear-related hearing loss since cochlear angiopathy and outer hair cell degeneration are likely to be seen in patients with diabetes as proposed by previous studies, with the absence of OAE's signifying impaired cochlea function which can missed by PTA testing alone.[4] HbA1c (glycosylated hemoglobin) is a sensitive test to assess the glycemic status of patients with diabetes, which has been recently considered as a diagnostic test for diabetes by the WHO. It assesses glycemic status of longer duration (3 months). This study was conducted to study the changes in hearing thresholds and alteration in cochlear biomechanics in relation to time since diagnosis and glycemic control in type 2 diabetic patients for the early diagnosis thus aiding in adoption of control measures to prevent the progression of disease and provide necessary rehabilitation measures for hearing impairment.


  Materials and Methods Top


This was a cross-sectional study conducted in 75 type 2 diabetes mellitus patients of both sexes aged 40–55 years in a tertiary care hospital who attended the medicine outpatient department for routine diabetic clinics. They were categorized into three groups each of 25 patients based on their HbA1c values, namely I, II, and III with good (<6.5%), poor (6.5%–8%), and uncontrollable diabetes (>8%), respectively, and based on time since diagnosis of diabetes into three groups, namely A, B, and C with <5 years, 5–10 years, and >10 years duration, respectively. Patients with a history of comorbidities such as chronic renal failure, hypertension and other immunocompromised conditions, ear infections/ear surgeries in the past, head trauma, consumption of ototoxic drugs, occupational exposure to noise, head injury, and family history of deafness were excluded from the study. Detailed pro forma was filled for each patient, including demographic data, brief history regarding diabetes (time since diagnosis of diabetes and type of treatment), and previous medical history. Patients underwent general physical and systemic examination (to rule out any diabetic complications) and ENT examination with emphasis on otological examination. Auditory assessment in patients was done using audiometric tests, namely PTA and distortion OAE (to assess cochlear function).

Pure-tone audiometry

Audiometric testing was performed using a duly calibrated double-channel clinical audiometer, GSI 61 coupled with TDH-50P earphones to obtain air conduction thresholds, and Radioear B-71 bone vibrator to obtain bone-conduction thresholds. Pure tones that range in octave spacings from 250 and 8000 Hz both for air and bone conduction were presented to the patients using the Modified Hughson–Westlake “ascending method” procedure as recommended by ANSI 1997. Hearing thresholds levels above 25 dB were considered abnormal. The degree of hearing loss was noted based on hearing thresholds according to Goodman's classification and institutional preference. Type of hearing loss was also noted. The average thresholds for air conduction were tabulated for all patients and for each of the frequencies in both right and left ears separately.

Distortion-product otoacoustic emissions

This test was performed in all patients using a computer-based distortion product OAE (DPOAE) analyzer GSI AUDERA. Stimulus of two equal pure-tone signals were given at two different frequencies, namely f1 and f2 (f2 >f1), intensities of primary stimulus was set at 65 dB SPL (L1) and 55 dB (L2) L1 >L2. The f2/f1 ratio was maintained at 1.21 on all occasions. The f2 frequency evaluated ranged from 1 kHz to 8 kHz. DPOAE amplitudes and signal-to-noise ratio (SNR) were calculated for each of the frequencies. Absent DPOAE was considered when SNR was ≤6 dB and signal amplitudes were <−10 dB for that frequency.

Data analysis

Statistical analysis was performed using the Pearson's Chi-square test and ANOVA test. The comparison among the individual parameters was done using the post hoc Tukey test using the statistical software SPSS version. 20 (IBM Corp., USA) with the help of institution's statistician. “P” < 0.05 was considered statistically significant. The study was approved by the Institutional Ethical Committee.


  Results Top


There were 48 male (64%) and 27 female patients (36%). Their age group ranged from 40 to 55 years, with a mean age of 47.87 years. There were 25 patients each in three groups I, II, and III based on glycemic control. Mean HbA1c value was 7.38. According to time since the diagnosis of diabetes, 29 patients (38.7%), 27 (36%) patients, and 19 patients (25.3%) belonged to Groups A, B, and C, respectively. There were 50.7% of patients who were on oral hypoglycemic agents (OHAs) and insulin both, 28% on OHA's alone, 14.7% and 6.7% on insulin and dietary control, respectively.

Assessment of hearing – pure-tone audiometry outcomes

Twenty-four patients (32%) had normal hearing and 51 patients (68%) showed hearing loss. Of 51 patients, 40 patients (76.92%) had SNHL and 11 patients (14.67%) had mixed hearing loss. Bilateral hearing loss was seen in 25.34% (19 patients), of which 24% (18 patients) had sensorineural and 1.4% (1 patient) had mixed hearing loss. The right ear showed normal hearing in 50.7%, SNHL in 40%, and mixed in 7%. The left ear showed normal hearing in 52%, SNHL in 38.7%, and mixed in 9.3% [Chart 1].



There was the highest incidence of moderate (18.7% in the right ear and 17.3% in the left ear) to moderately severe degree of hearing loss (17.3% in the right ear and 20% in the left ear). Mild hearing loss was seen in 10.7% in the right ear and 6% in the left ear. Nearly 2.7% patients showed a severe degree of hearing loss in both ears. There were no cases of profound hearing loss in the study [Chart 2].



Correlation of hearing with glycemic control

Of the 24 patients with normal hearing, 54.17% of patients belonged to Group I and 50% (12 patients each) belonged to Groups II and III, respectively.

Forty-eight percent (12 patients) with SNHL in the right ear and 60% (15 patients) in the left ear belonged to Group III (uncontrolled glycemic control). Thirty-six percent (9 patients) with SNHL in the right ear and 32% (8 patients) in the left ear belonged to Group II, and 36% patients with SNHL in the right ear with 24% (6 patients) in the left ear belonged to Group I [Table 1] and [Table 2]. Mixed loss was seen in 12% (3 patients) each in right and left ears belonged to Group I and 4% (1 patient) and 8% (2 patients) belonged to Groups II and III in right and left ears, respectively [Table 1] and [Table 2].
Table 1: Comparison of Pure Tone Audiometry with Glycemic control in Right ear

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Table 2: Comparison of Pure Tone Audiometry with Glycemic control in Left ear

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Correlation of hearing with time since the diagnosis of diabetes

SNHL was seen in 47.4% and 52.6% of patients in Group C in right and left ears, respectively; 37% (right ear) and 44.4% (left ear) in Group B and 37.9% and 24.1% in Group A were seen in right and left ears, respectively. Of the 9.3% patients showing mixed hearing loss, 15.8% (3 patients each) belonged to Group C in both ears, 10.3% (right ear) and 6.9% (left ear) belonged to Group A and 3.7% and 7.4% in right and left ears, respectively, belonged to Group B [Table 3] and [Table 4].
Table 3: Right ear hearing in relation to the duration of diabetes and pure-tone audiogram

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Table 4: Left ear hearing in relation to the duration of diabetes and pure-tone audiogram

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Average air conduction thresholds

In relation to glycemic control

Average thresholds seen in both ears were the highest in Group III (40.3 dB – right ear and 40.1 dB – left ear) and least in Group I, 25.3 dB and 18.4 dB, respectively, in right and left ears.

With respect to HbA1c values, the comparison of average PTA thresholds between the three groups in each frequency (250 to 8000 Hz) and average of all PTA threshold in all frequencies was statistically significant (with P < 0.001 and 0.005, respectively).

In relation to time since the diagnosis of diabetes

Average thresholds were the highest in Group C in both ears (39.3 dB and 36.4 dB in right and left ears, respectively) and least in Group A (32.25 dB – right ear and 27.9 dB – left ear).

The comparison of average PTA thresholds between the three groups in each frequency except 8 kHz showed statistically significant values in the right ear (P < 0.05), while for left ear, it was insignificant for all frequencies and average of all PTA threshold in all frequencies showed statistically insignificant values.

Assessment of hearing – Distortion-product otoacoustic emissions

OAE was absent in 21 patients (28%) bilaterally, 19 patients unilaterally (25.3%), and 35 patients present bilaterally (46.7%). The highest incidence of bilateral absent OAE was seen in patients in Group I (40% in >8% group and 36% in 6.5%–8% group) (P = 0.008) and in patients with longer duration of diabetes of >5 years (33.3% in 5–10 years' group and 31.6% in >10 years' group). The highest incidence of bilateral positive OAE's was seen in 76% of patients in Group I and Group C (55.2% in <5 years' group) [Table 5] and [Table 6].
Table 5: Comparison of distortion-product otoacoustic emissions with glycemic control (glycosylated hemoglobin)

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Table 6: Comparison of distortion-product otoacoustic emissions with the duration of diabetes

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In our study, DPOAE amplitude was significantly reduced in patients with diabetes in Group III as compared to the other two groups with no significant correlation between the time since diagnosis of diabetes. The comparison between the average DPOAE amplitudes among the three groups showed a statistically significant difference (P < 0.05) in the mid and high frequencies 2 kHz and 8 kHz in both ears with respect to HbA1c parameter and significant difference in frequencies 2 kHz and 6 kHz only in the left ear in relation to the duration of diabetes.

The comparison between average PTA and DPOAE thresholds in all frequencies is shown in [Chart 3] and [Chart 4].



Association with other parameters

Age

The maximum number of patients with normal hearing were seen in the age group of 46–50 years and those with increased incidence of hearing loss (both sensorineural and mixed) were seen in the age group of 46–50 years and 51–55 years, with absent DPOAE seen maximum in age group of 51-55 years and 46-50 years with statistical significant association with the age parameter. DPOAE's seen maximum in the age group of 51–55 years and 46–50 years which was similar to hearing loss incidence both affecting similar age groups.

Gender

Although the higher incidence of hearing loss was seen in males (68.75%) as compared to females (66.7%), no statistically significant difference in hearing loss was seen in the comparison. The highest incidence of absent DPOAE's in both ears was seen in females with no significant difference in DPOAE results between the two genders.

Type of treatment

The highest incidence of hearing loss was in patients on both oral hypoglycemics and insulin (10.5% mixed loss in both ears and 44.7% and 63.6% showed sensorineural loss in the right and left ear, respectively). DPOAE's were maximum absent in patients on insulin and oral hypoglycemics both (36.8%) followed by those on insulin (36.4%) with statistically significant correlation (P = 0.035).


  Discussion Top


Diabetes affects the auditory system, thereby altering the inner ear functioning. Debate on the association of diabetes mellitus with hearing loss has been going on for many years. Jordao,[5] in 1857, was the first to propose the association between the two. Although varied studies have shown patients with diabetes to have hearing impairment with the incidence varying from 0% to 93%, there are few which have shown no association of hearing loss in patients with diabetes.[3]

Assessment of hearing – Pure-tone audiometry outcomes

Friedman et al. showed a 55% incidence of hearing loss in patients with diabetes similar to the results obtained in our study which showed 51 patients (68%) with abnormal hearing thresholds.[6]

Type of hearing loss

Most studies have shown an increased incidence of subclinical SNHL in patients with diabetes.[6],[7] The incidence of SNHL in diabetes quoted in the literature ranges from 0 to 93%. In our study, 40 patients (76.92%) had SNHL. Unlike most studies showing only SNHL in patients with diabetes, there were 11 patients (14.67%) who showed mixed hearing loss in our study which was similar to the study conducted by Thimmasettaiah et al. to assess hearing loss in 102 type 2 diabetic patients showed that 16% showed mixed hearing loss (reasons were not mentioned).[8] Those with mixed hearing losses in our study showed type C tympanogram in four patients, type Cs in two patients (all six patients gave a history of recent upper respiratory tract infection), and five patients showed type Ad curve (two patients had scarred drum and two showed healed perforation).

Laterality

Most studies show an increased incidence of bilateral SNHL.[1],[9] In our study, bilateral hearing loss was seen in 25.3% of patients (19 patients), of which 24% had sensorineural and 1.3% had mixed hearing loss.

Degree of hearing loss

Most audiometric studies of hearing in patients of diabetes showed a mild-to-moderate SNHL.[3],[10],[11] However, our study showed the maximum number of patients with moderate (18%) to moderately severe degree of hearing loss (18.65%).

Correlation with glycemic control

The studies on patients with diabetes by Kurien et al. and Bainbridge et al. showed that maximum patients with high-frequency SNHL had poor glycemic control.[9],[12] This was similar to the results in our study wherein the highest prevalence of hearing loss was seen in uncontrolled diabetic group (HbA1c > 8%) (SNHL in 40% [30 patients] in the right ear and 60% [15 patients] in the left ear).

Correlation with time since diagnosis

Thimmasettaiah et al. in their study found that of the 76 cases with SNHL, 79% had duration >5 years and 42% patients were diagnosed for the first time suggesting that the incidence of SNHL increases with increase in the duration of diabetes.[8] Our study showed the highest incidence of SNHL in 52.6% patients in the right ear and 47.4% patients in the left ear with duration of diabetes of >10 years and least incidence in 37.9% patients in the right ear and 24.1% patients in the left ear with <5 years duration of diabetes.

Average pure-tone thresholds

Hearing loss observed in patients with diabetes has shown to affect high frequencies as shown in previous studies;[10],[13],[14] however, Friedman et al. have showed affection of lower frequencies (500 kHz) significant.[6] Our study showed significant hearing loss in all frequencies, but the comparison of average thresholds in all frequencies showed significant losses in the higher frequencies (4 kHz and 8 kHz), the prevalence being more in patients with poor glycemic control and those with longer duration of diabetes (>10 years).

Assessment of hearing – Distortion-product otoacoustic emissions outcomes

In view of cochlear outer hair cell damage seen more frequently among patients with diabetes affecting inner ear function,[15] the assessment of cochlear functioning is essential in patients with diabetes. In our study, DPOAE was used in view of its sensitivity to identify the frequency-specific hearing losses, its loss suggesting outer hair cell damage and inner ear dysfunction. A study by Sasso et al. to assess cochlear dysfunction in patients with diabetes showed OAEs impaired in 51.8% (57 of 110) of the patients with diabetes , as compared with 4.7% in the control group (5 of 106) (P <.0001–highly significant).[15] In our study, OAE was absent in 21 patients (28%) in both ears, 19 patients in one ear (25.3%), and 35 patients present in both ears (46.7%).

In relation to glycemic control

A study by Park et al. done to assess the subclinical dysfunction of cochlea using DPOAE showed that amplitudes to be significantly lower in the group with HbA1c >6% (9.1 dB SPL), especially at 6 kHz and 8 kHz as compared to normal HbA1c group (14.4 dB SPL).[16] In our study, of 21 patients, the highest incidence of bilateral absent OAE was seen in patients with poor glycemic control (40% in >8% group and 36% in 6.5%–8% group) and highest incidence of bilateral positive OAE's was seen in 76% of patients with good glycemic control (<6.5%).

In relation to time since diagnosis

Most studies showed no correlation between DPAOE results with the duration of diabetes. However, a study by Sasso et al. showed a statistically significant difference between the patients with diabetes and normal subjects in relation to duration of diabetes as explained by the finding that those with absent DPOAE's had longer duration of diabetes (11.5 ± 4.4 vs. 7.0 ± 3.9 years with P < 0.001).[15] Our study also showed no significant correlation between the two parameters. However, a comparison among the three groups showed a significant difference in frequencies 2 kHz and 6 kHz only in the left ear with absent DPOAE's maximum in patients with duration of disease for 5–10 years.

Frequencies affected in distortion-product otoacoustic emissions

In relation to amplitudes affected, Ottaviani et al. found reduced DPOAE amplitude at all studied mean frequencies, with most significant differences observed in the mid frequencies.[17] In our study, the comparison between the average DPOAE amplitudes between the groups according to their glycemic status, a statistically significant difference (P < 0.05) was seen in mid and high frequencies 2 kHz and 8 kHz in both ears with no significant difference seen in relation to the duration of diabetes.

Association with other parameters

Age

The age group included in the study was 40–55 years, thereby ruling out the influence of presbycusis on the hearing assessment. Axelsson et al. showed that even after the correction of presbycusis, the incidence of hearing loss increased with age.[18] Harkare et al. also showed the increased incidence of hearing loss with age (the highest being in the age group of 41–55 years), although no significant association was found between SNHL and age.[10] The maximum number of patients in our study with hearing loss (both sensorineural and mixed) and with absent OAE was seen in the age group of 46–50 years and 51–55 years, however, with no statistically significant correlation.

Gender

Most studies in the literature do not show any difference in hearing losses in patients with diabetes between the sexes.[6] In our study, although a higher incidence of hearing loss was seen in males (68.75%) as compared to females (66.7%), no statistically significant difference in hearing loss was seen on the comparison, similar to study by Tay et al.[11]

Type of treatment

Studies by Axelsson et al.[18] and Wackym and Linthicum et al.[19] showed that patients with diabetes treated with insulin had better hearing as compared to those on oral medications. The type of treatment showed no statistically significant difference; however, patients on both insulin and OHAs showed the highest incidence of hearing loss (44.7% and 63.6% showing sensorineural loss in the right and left ear, respectively). The absence of OAE showed similar incidence highest in patients on combination treatment with insulin and OHAs (36.8%).


  Conclusion Top


The study clearly indicates the increased prevalence of hearing impairment in type 2 diabetic patients being more pronounced in patients with poor glycemic control and longer duration of diabetes being moderate-to-moderately severe degree with average pure tone and OAE affected for mid-to-high frequencies. Age and gender did not show any significant correlation. Patients on both OHA's and insulin showed the highest incidence of hearing loss. Our study showed few patients with normal PTA thresholds with absent DPOAE's which indicated that subclinical alterations in the cochlear function can be missed by PTA. It is important for physicians to be aware of the coexistence of hearing symptoms to incorporate the referral of patients with diabetes to otorhinolaryngologists as a routine practice to detect even subclinical hearing loss at the earliest to prevent the progression of disease and implement necessary measures for the treatment and rehabilitation of hearing impairment.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Jorgensen MB. The inner ear in diabetes mellitus. Histological studies. Arch Otolaryngol 1961;74:373-81.  Back to cited text no. 1
    
2.
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Harner SG. Hearing in adult-onset diabetes mellitus. Otolaryngol Head Neck Surg 1981;89:322-7.  Back to cited text no. 3
    
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Fukushima H, Cureoglu S, Schachern PA, Kusunoki T, Oktay MF, Fukushima N, et al. Cochlear changes in patients with type 1 diabetes mellitus. Otolaryngol Head Neck Surg 2005;133:100-6.  Back to cited text no. 4
    
5.
Jordao AM. Consideration sur uncas du diabetes. Union Medicale du Paris 1857;11:446.  Back to cited text no. 5
    
6.
Friedman SA, Schulman RH, Weiss S. Hearing and diabetic neuropathy. Arch Intern Med 1975;135:573-6.  Back to cited text no. 6
    
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Virtaniemi J, Laakso M, Nuutinen J, Karjalainen S, Vartiainen E. Hearing thresholds in insulin-dependent diabetic patients. J Laryngol Otol 1994;108:837-41.  Back to cited text no. 7
    
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Nagaraj BT, Reddy S, Ravi GC, Reddy S. A one year prospective study of hearing loss in diabetes in general population. Transl Biomed 2012;3:433.  Back to cited text no. 8
    
9.
Kurien M, Thomas K, Bhanu TS. Hearing threshold in patients with diabetes mellitus. J Laryngol Otol 1989;103:164-8.  Back to cited text no. 9
    
10.
Harkare VV, Deosthale NV, Khadakkar SP, Dhoke PR, Dhote KS, Gupta A. SNHL in Diabetics: A Prospective Study. People's J Sci Res 2014;7:38-2.  Back to cited text no. 10
    
11.
Tay HL, Ray N, Ohri R, Frootko NJ. Diabetes mellitus and hearing loss. Clin Otolaryngol Allied Sci 1995;20:130-4.  Back to cited text no. 11
    
12.
Bainbridge KE, Hoffman HJ, Cowie CC. Diabetes and hearing impairment in the United States: Audiometric evidence from the National Health and Nutrition Examination Survey, 1999 to 2004. Ann Intern Med 2008;149:1-10.  Back to cited text no. 12
    
13.
Cullen JR, Cinnamond MJ. Hearing loss in diabetics. J Laryngol Otol 1993;107:179-82.  Back to cited text no. 13
    
14.
Celik O, Yalçin S, Celebi H, Oztürk A. Hearing loss in insulin-dependent diabetes mellitus. Auris Nasus Laryn×1996;23:127-32.  Back to cited text no. 14
    
15.
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;48:1346-50.  Back to cited text no. 15
    
16.
Park MS, Park SW, Choi JH. Distortion product otoacoustic emissions in diabetics with normal hearing. Scand Audiol Suppl 2001;30:148-51.  Back to cited text no. 16
    
17.
Ottaviani F, Dozio N, Neglia CB, Riccio S, Scavini M. Absence of otoacoustic emissions in insulin-dependent diabetic patients: Is there evidence for diabetic cochleopathy? J Diabetes Complications 2002;16:338-43.  Back to cited text no. 17
    
18.
Axelsson A, Fagerberg SE. Auditory function in diabetics. Acta Otolaryngol 1968;66:49-64.  Back to cited text no. 18
    
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Wackym PA, Linthicum FH Jr., Diabetes mellitus and hearing loss: Clinical and histopathologic relationships. Am J Otol 1986;7:176-82.  Back to cited text no. 19
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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