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Prevalence of Hearing Loss in Type 2 Diabetes Mellitus
tinnitus in spells), patients with a past history Assessment of HL continuous variables between more than two
of neurological diseases (stroke, multiple Pure tone audiometry (PTA) was performed groups. ANOVA for repeated measures was used
sclerosis, dementia, or central nervous system using Maico-MA 32 diagnostic audiometer in a to find the change in PTA averages at different
infections), patients with a past history of soundproof compartment. Air conduction and frequencies. Linear regression was used to find
closed or open head injuries, patients with bone conduction audiometric thresholds at the significant predictors by taking the PTA
chronic overexposure of loud noises (90 dB for 250, 500, 1000, 2000, 4000, and 8000 Hz were average as the outcome for both the right and
8 hours a day, 5 days a week), patients unable obtained using 5 dB steps. Hearing sensitivity left ear. Bivariate logistic regression was used to
to comprehend PTA assessment, and patients for each ear was measured separately, and find the significant predictors by taking an HL in
not willing to consent or not capable to the severity of HL was assessed according any one ear as an outcome. A p-value of <0.05
consent were excluded. Demographic details to Goodman’s classification. Patients were was considered statistically significant. Data
were obtained from the subject’s clinical classified into those with mild, moderate, analysis was done using Statistical Package for
notes, followed by a clinical assessment of moderately severe, severe, or profound HL Social Sciences (version 21.0).
DSPN and an assessment of hearing using PTA. accordingly.18,19 Severity of HL in the worse ear
Ethical Approval and Registration of was considered for statistical analysis. In our R e s u lts
study, HL was defined as pure tone average A total of 200 patients with T2DM were enrolled
Study Protocol >15 dB hearing level (dBHL) in the worse in the study, and the overall prevalence of HL
The Institutional Ethics Committee of Christian ear. CSHL was defined as pure tone average
was 81%. Among them, 152 patients had
Medical College and Hospital approved the > 25 dBHL in the worse ear. Pure tone average
neuropathy, and 48 patients did not have
study protocol prior to any study-related was defined as the average of 500, 1000, and
neuropathy. The prevalence of HL was 66.7%
activities, and the protocol was registered 2000 Hz.
among patients without neuropathy, 80.9%
with the Baba Farid University of Health
among patients with mild neuropathy, and
Sciences prospectively as part of the Doctor Statistical Analysis
87.6% in patients with moderate to severe
of Medicine thesis in general medicine for
Data was collected using a structured proforma. neuropathy (p-value = 0.004). The PTA values
the first author and the principal investigator
Data entry was done in Microsoft Excel increased with an increase in the Hba1c
of the study under the supervision of the
spreadsheets. Mean, frequency, and standard levels. The flow of patients in the study is
other two authors (https://www.bfuhs.ac.in/
deviation (SD) were calculated. The Chi-squared summarized in Flowchart 1.
examination/PlanOfThesis/27-8-18/CMC-2016.
test was used to compare categorical variables
pdf). Patients were recruited in the study Baseline Profile of Patients
between the groups. An independent t-test
after they provided informed consent in a
was used to compare the continuous data The demographic, clinical, and biochemical
language comfortable to them (English, Hindi,
between two groups, and a one-way analysis profile of the patients is summarized in
or Punjabi)
of variance (ANOVA) was used to compare the Table 1. Patients with neuropathy, males, and
Sample Size
The prevalence of neuropathy in patients Flowchart 1: Flow of patients in the study
with diabetes was noted to be 50%.16 The
sample size was calculated to be n = 200
by using the formula n = Z α/2 2 *p (1-p)/d2,
where Z = α/2 is the critical value of the
normal distribution at α/2 (for our study,
the confidence level of 95%, α is 0.05 and
the critical value is 1.96), p = 50% is the
proportion and d = 7% is margin of error.
Assessment of Peripheral
Neuropathy
Distal peripheral sensory-motor neuropathy
(DSPN) among the participants of the study
was assessed using the clinical Michigan
Diabetic Neuropathy Score (MDNS). The MDNS
score is calculated based on a neurological
examination, and it is a validated tool for
diagnosis and assessment of the severity
of neuropathy in patients with DSPN, as
discussed in the study by Feldman et al.17
Based on the MDNS score, recruited patients
were divided into three groups. Group I
included patients with no neuropathy (MDNS
score of ≤6). Group II included patients with
mild neuropathy (MDNS score of 7–13). Group
III included patients with both moderate
(MDNS score of 13–30) and severe neuropathy
(MDNS score of ≥30).
older patients (p = 0.003) had a higher risk of (MDNS Grade). The prevalence of HL and CSHL tone average increased with an increase in
developing HL. increased with the increase in severity of the severity of neuropathy (p = 0.005). On
neuropathy (MDNS Grade), and the correlation univariate linear regression with PTA average
Prevalence of HL and its Association was statistically significant (p-value 0.009 and as the dependent variable, age, severity of
with Neuropathy 0.015, respectively). neuropathy (MDNS score and MDNS Class),
Figure 1A shows the prevalence of HL and and fasting plasma glucose (FPG) was found
CSHL among patients with and without Hearing Loss (HL) in Speech to have a significant positive correlation. The
neuropathy. The correlation was statistically Frequencies (Pure Tone Average) estimated glomerular filtration rate (eGFR) had
significant for HL and CSHL (p = 0.004 and The clinical pure tone average (average of 500, a negative correlation with the PTA average.
0.016). Figure 1B shows the association of HL 1000, and 2000 Hz) was found to be higher
and CSHL with the severity of the neuropathy in patients with neuropathy, and the pure Association of MDNS Score/MDNS
Class with Hearing Threshold in
Various Frequencies
Table 1: Baseline profile of patients in the study
Figure 2 shows the association of the severity
Neuropathy of neuropathy with hearing threshold values
at various frequencies in the right and left ears.
No Mild Moderate to severe p-value
In patients with neuropathy, the HL was found
(n = 48, 24%) n = 47 (23.5%) n = 105 (52.5%) to be worse at higher frequencies like 2000,
Age (years) 46 ± 9.4 49 ± 8.0 51 ± 7.6 0.001 4000, and 8000 Hz. With worsening grades of
Mean ± SD neuropathy, HL in the higher frequencies also
Gender n (%)
worsened. The correlation was statistically
significant in the higher frequencies like 2000,
Male (n =100) 27 (56.3) 21 (44.7) 52 (49.5) 0.524 4000, and 8000 Hz. The p-values were <0.001,
Female (n = 100) 21 (43.8) 26 (55.3) 53 (50.5) 0.024, and 0.020 in the left ear. In the right ear,
BMI (body mass index) 24.2 ± 3.0 25.0 ± 4.5 25.4 ± 3.2 0.183 p-values were 0.005, 0.007, and 0.028 for these
kg/m2, mean ± SD frequencies.
On comparing the MDNS score with
Duration of DM (years) 4.7 ± 4.0 6.0 ± 4.1 6.6 ± 4.9 0.067
the PTA hearing threshold, similar results
Mean ± SD
were seen. The correlation was statistically
FPG (mg/dL) 174.8 ± 55.9 183.9 ± 64.8 183.7 ± 58.5 0.660 significant for 2000, 4000, and 8000 Hz
Mean ± SD (p = 0.001, 0.001, and 0.006 in the right ear
HbA1c (%) 8.9 ± 2.7 10.3 ± 2.9 10.2 ± 2.7 0.073 and p ≤ 0.001, 0.004, and 0.022 in the left ear).
Mean ± SD
eGFR (mL/minute/1.73 m2) 100.5 ± 25.4 84.0 ± 32 79.4 ± 27.2 <0.001 Association of Hba1c with HL or PTA
Mean ± SD The severity of HL in speech frequencies (pure
Hypertension 5 (10.4) 10 (21.3) 36 (35.0) 0.004 tone average) had a significant correlation
n = 81 (40.5 %)
with HbA1c. The PTA values at 250, 500,
1000 Hz, and pure tone average increased with
Established cardiovascular 3 (6.3) 6 (12.8) 10 (9.5) 0.556
an increase in Hba1c levels, and the correlation
disease
was statistically significant (p = 0.017, 0.004,
n = 19 (9.5 %)
0.029, and 0.048, respectively). In the left ear,
Figs 1A and B: (A) Prevalence of HL and CSHL in patients with neuropathy and without neuropathy; (B) Prevalence of HL and CSHL in patients without
neuropathy (MDNS* grade 0), mild neuropathy (MDNS grade 1) and moderate to severe neuropathy (MDNS grade 2); *MDNS, Michigan Diabetic
Neuropathy Score
the PTA values at 250 Hz and PTA average Univariate and Multivariate Patients with neuropathy were more likely to
had a significant correlation with Hba1c levels Regression Analysis with HL in Any have HL, and the severity of HL increased with
(p = 0.037 and 0.012, respectively). The PTA One Ear as an Outcome an increase in the severity of the neuropathy.
values and their correlation with Hba1c levels The prevalence of CSHL was 20.8% in patients
On univariate analysis, age, gender, the
are shown in Figure 3. without neuropathy (group I), 25.5% in patients
severity of neuropathy (MDNS score and
with mild neuropathy (group II), and 33.3% in
Association of eGFR with HL MDNS grade), and the presence of neuropathy
patients with moderate to severe neuropathy
were found to have significant correlations
The mean eGFR for patient s with HL (group III). The clinical pure tone average, which
(Table 2). The prevalence of HL was higher in
and those without HL was 84.1 ± 28.3 represents the average hearing threshold in
older patients (p = 0.004) and patients with
and 91.8 ± 3.4, respectively (p = 0.145). speech frequencies, increased with increased
neuropathy (p = 0.006). The risk of developing
With worsening renal function, there was severity of neuropathy. This was suggestive
HL increased with the worsening severity of
worsening HL across all the frequencies. of worsening hearing impairment with an
neuropathy (p = 0.007). Women had some
There was an increase in the PTA threshold increase in the severity of neuropathy. It was
protection against developing HL (p = 0.033).
across various frequencies as the eGFR noted that the hearing impairment was more
On multivariate analysis with AHL in any one
decreased. At 2000 Hz, the increase in PTA in the higher frequencies, like 2000, 4000, and
ear as an outcome, age (p = 0.018), gender, and
threshold with the decrease in eGFR was 8000 Hz, among patients with T2DM, and the
MDNS score (p = 0.005) were found to have a
found to be statistically significant (p-value correlation of HL with neuropathy was more in
significant correlation.
of 0.034). However, the correlation was not the higher frequencies. Age, gender, presence
significant in the other frequencies. The of neuropathy, and severity of neuropathy were
average PTA also increased with a decrease D i s c u s s i o n associated with a significantly increased risk of
in eGFR (negative correlation); however, the Among the patients enrolled in our study developing HL.
correlation was not statistically significant with T2DM, the overall prevalence of HL was In our study, the clinical pure tone average
(p-value > 0.05). 81%, and the prevalence of CSHL was 28.5%. (average hearing threshold in 500, 1000, and
Figs 2A and B: (A) Comparison of Hearing threshold across various frequencies for patients without neuropathy, mild neuropathy, and moderate to
severe neuropathy in the right ear; (B) and left ear
Figs 3A and B: (A) Association of Hba1c with HL (PTA values) in the left ear; (B) Association of Hba1c with HL (PTA values) in the right ear
Table 2: Univariate binary logistic regression with HL as the outcome group, none of them were evaluated for HL prior
Predictors Coefficient β p-value Odds ratio 95% confidence interval to our study or underwent any treatment for HL.
Few studies showed some benefits of
Lower Upper
screening for HL among adults; however,
Age 0.06 0.004 1.062 1.019 1.107 there is no consensus regarding the high-
Gender risk groups who require screening for HL. In
Male 1 our study, it was seen that the prevalence of
CSHL was significantly higher in patients with
Female −0.802 0.033 0.448 0.214 0.938 moderate to severe neuropathy compared to
MDNS score 0.093 0.002 1.097 1.035 1.163 the prevalence of HL reported among middle-
MDNS grade 1.775 0.017 0.326 3.224 aged adults. Studies have shown that a 10 dB
0 1 increase in PTA values was associated with
52% increased odds of social isolation and
1 0.52 0.272 1.682 0.665 4.252
significant cognitive decline.26,27 Subclinical
2 1.168 0.007 3.217 1.385 7.47 HL has also been independently associated
Neuropathy with cognitive impairment and depressive
Absent 1 symptoms. Due to the gradual onset of HL,
many elderly individuals are unaware of their
Present 1.045 0.006 2.843 1.344 6.012
hearing impairment, and increasing age is
Multivariate binary logistic regression with HL as the outcome
associated with the underestimation of the
Age 0.055 0.018 1.056 1.01 1.105 severity of HL. 4 With increasing age and
Gender cognitive decline, it becomes progressively
Male 1 difficult to use hearing aids. Delays in diagnosis
can lead to an unwillingness to start treatment,
Female −1.143 0.006 0.319 0.141 0.723
poor compliance, improper maintenance
MDNS score 0.107 0.005 1.113 1.041 1.191 of the hearing aids, and poor treatment
outcomes. 28 Diagnosis and initiation of
2000 Hz) showed a significant correlation with (2000, 4000, and 8000 Hz) for patients with treatment at the right time are important
the severity of neuropathy, age, and HbA1c. As T2DM. The correlation between hearing for the acceptance of treatment, adequate
speech sounds are more densely represented threshold and neuropathy was more in compliance, and optimal treatment outcome.
in the mid frequencies, the average of 500, the higher frequencies. This suggests that Screening for HL in patients with diabetic
1000, and 2000 Hz signifies the involvement of patients with diabetic neuropathy are neuropathy who are at a higher risk of
speech frequencies. Clinical pure tone average more likely to have hearing impairment in developing HL can help in the timely diagnosis
had a significant association with MDNS the higher frequencies. The HL in higher and treatment of these patients.
score and MDNS grade. This was suggestive frequencies was more than the HL seen in American Speech-Language-Hearing
of worsening hearing impairment in speech speech frequencies. Similar results were Association recommends screening all
frequencies with an increase in the severity of seen in a study by Sugimoto et al. in which adults, and World Health Organization’s
neuropathy. The pure tone average was higher neuropathy correlated significantly with HL guidelines on integrated care for older
in older patients and patients with higher in the higher frequencies among patients people recommend screening of elderly.
HbA1c. Similar results were seen in the study by with T2DM. 20 Studies were done on diabetes As suggested by Nieman et al., although
Austin et al. and Sugimoto et al., where higher and its association with HL, and a systematic definitive recommendations have yet to
HbA1c and uncontrolled blood glucose levels review by Akinpelu et al. concluded that be developed, the appropriate clinical
correlated with HL in patients with T2DM.8,20 the severity of HL was higher in frequencies practice would be to screen any person with
Most patients with T2DM tend to develop HL among patients with T2DM.22–24 Patients with perceived HL and persons with risk factors
in the higher frequencies; however, those with HL in the higher frequencies have difficulty for developing HL. 29 Studies have suggested
poorly controlled glucose levels had significant hearing when there is background noise or that stimulation of the auditory system may
HL in the speech frequencies also. In a cross- when they are in a group which can lead to reduce age-related degeneration, and using
sectional study conducted by Sugimoto et al., social withdrawal and avoidance of social hearing aids might be beneficial in modifying
diabetic neuropathy, creatinine clearance, interactions. People with high-frequency the aging process in the auditory system. 30
and retinopathy were found to have some HL tend to have difficulty in hearing certain Hence screening of patients with moderate-
association with HL. 20 Pathophysiological consonants, like s, h, and f, which are uttered severe diabetic neuropathy who are at high
changes seen in the auditory nerve and inner at a higher frequency than vowel sounds. risk for developing HL should be considered
ear, which are similar to the changes seen in This can result in speech sounding muffled, to prevent the further worsening of quality
the peripheral nerves of patients with diabetic especially when talking on the phone, of life-related to hearing impairment.
neuropathy, might explain the association of watching TV, or trying to have a conversation Single question screening, hearing
HL with neuropathy. In our study, HL had a in background noise. handicap inventory for the elderly- screening
negative correlation with eGFR, and this was Among patients enrolled in our study with version (HHIE-S), clinical tests like whispered
consistent with other studies where patients moderate to severe neuropathy, the prevalence voice tests, finger rub tests, and hand-held
with diabetic nephropathy were found to have of CSHL was 33.3%, while studies have reported audiometers have been used for screening
a significant association with HL.20,21 that the prevalence of HL in a population of for HL in various studies. In single-question
It was noted in our study that HL was middle-aged adults is 14–20%.25 Even though screening, the patient is asked a single
more prominent in the higher frequencies the prevalence of CSHL was higher in our study screening question like “Do you have difficulty
with your hearing?” It has a sensitivity of References 17. Feldman EL, Stevens MJ, Thomas PK , et al. A
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