Association between diabetes mellitus and hearing impairment in American and Korean populations

Accepted Manuscript Association between diabetes mellitus and hearing impairment in American and Korean populations

Shinje Moon, Jung Hwan Park, Jae Myung Yu, Moon-Ki Choi, Hyung Joon Yoo PII: DOI: Reference:

S1056-8727(17)31606-9 doi:10.1016/j.jdiacomp.2018.04.004 JDC 7191

To appear in: Received date: Revised date: Accepted date:

29 November 2017 10 April 2018 12 April 2018

Please cite this article as: Shinje Moon, Jung Hwan Park, Jae Myung Yu, Moon-Ki Choi, Hyung Joon Yoo , Association between diabetes mellitus and hearing impairment in American and Korean populations. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Jdc(2018), doi:10.1016/ j.jdiacomp.2018.04.004

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Association between diabetes mellitus and hearing impairment in American and Korean populations

Running title: Diabetes mellitus and hearing impairment

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Shinje Moona,1,*, Jung Hwan Parkb, 1 , Jae Myung Yua, Moon-Ki Choia, Hyung Joon Yooa* Division of Endocrinology and Metabolism, Hallym University College of Medicine

b.

Department of Endocrinology and Metabolism, Hanyang University College of Medicine

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These authors contributed equally to this article

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a.

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* Co-corresponding author.

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Address for Correspondence

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Hyung Joon Yoo

Division of Endocrinology and Metabolism, Hallym University College of Medicine, 1 Singil-ro, Yeongdeungpo-gu, Seoul 07441, Korea.

or

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Tel: 82-2-829-5381, Fax: 82-2-846-4669, E-mail: [email protected]

Shinje Moon Division of Endocrinology and Metabolism, Hallym University College of Medicine, 1 Singil-ro, Yeongdeungpo-gu, Seoul 07441, Korea. Tel: 82-2-829-5381, Fax: 82-2-846-4669, E-mail: [email protected]

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Abstract Backgrounds: The association between diabetes mellitus (DM) and hearing impairment in clinical studies is controversial. The aim of this study was to evaluate ethnic- and sex-specific associations between DM and hearing impairment.

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Methods: For this cross-sectional study using National Health and Nutrition Examination Survey in the U.S. and Korea, the total number of eligible participants included was 7,081 in

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the U.S. and 15,704 in Korea. Hearing impairment was defined as a pure tone threshold level

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greater than 25 decibels. Multivariate logistic regression analysis was conducted, adjusting for age, sex, race/ethnicity, socioeconomic status, body mass index, noise exposure, smoking,

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hypertension, and dyslipidemia.

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Results: The association between DM and hearing impairment was found to be sex-specific. The multivariate adjusted OR of high-frequency impairment was 0.843 (95 % CI, 0.524-

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1.356) in American men, and 1.073 (95 % CI, 0.835-1.379) in Korean men, while the ORs in

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women from U.S. and Korea were 1.911 (95 % CI, 1.244-2.935) and 1.421 (95 % CI, 1.1031.830), respectively. A subgroup analysis of each race/ethnicity among the U.S. adults showed similar results. The age-adjusted OR of high-frequency impairment in women was

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1.896 (95% CI, 1.081-3.325) for Hispanics, 2.048 (95% CI, 1.173-3.575) for Non-Hispanic

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Whites, and 2.226 (95 % CI, 1.327-3.868) for Non-Hispanic Blacks. In contrast to highfrequency impairment, there was no significant association between low-frequency impairment and DM in both men and women among the U.S. and Korean populations. Conclusion: Our results suggest that DM is associated with hearing impairment in only women, irrespective of race/ethnicity groups. Keywords: Diabetes mellitus; Hearing impairment; National Health and Nutrition Examination Survey; NHANES

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1. Introduction Hearing impairment is a major public health concern that affects 328 million adults globally1, 2. Due to an aging society, the prevalence of hearing impairment is increasing rapidly; the figure more than doubled between 1995 and 20042, 3. The most common cause of

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hearing impairment is presbycusis, which is sensorineural hearing loss related to aging6. It is important to understand the risk factors associated with hearing impairment in order to

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develop appropriate strategies to address this growing problem. The prevalence of hearing

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impairment has been found to vary according to race and sex1, 4, 5. Risk factors for hearing impairment include male sex, a lower level of education, smoking, noise exposure, ototoxic

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drugs, genetic inheritance, neurodegenerative diseases, infection, and diverse types of injury6-

Several studies have proposed diabetes mellitus (DM) as another risk factor for hearing

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impairment11-14,. Previous studies with human tissue and animals indicated that

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microangiopathy or neuropathy of DM may result in hearing impairment by affecting vasculatures and neurons in the inner ear15-19. However, the association remains controversial in clinical studies20. While some studies have reported a positive association between type 2

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DM and hearing impairment11-13, others found no difference21,22. This discrepancy may be

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due to differences in demographic features and the method used to assess hearing impairment. Considering the variations in prevalence of hearing impairment according to race and sex 1, studies with consistent and well-established criteria for determining hearing impairment according to these factors are essential to clarify the association with DM. However, until now, there has been no race- and sex-specific study of this association. This study was therefore conducted to evaluate ethnic- and sex-specific associations between DM and hearing impairment in a large sample of American and Korean populations using data from the 1999-2012 National Health and Nutrition Examination Survey

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(NHANES) in the US and the 2010–2013 National Health and Nutrition Examination Survey in Korea (KNHANES).

2. Materials and methods

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2.1 Study Population Korean and American data were collected from KNHANES 2010-2013 and NHANES 1999-

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2012 respectively. Both surveys used a cross-sectional and nationally representative survey

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with a multistage and stratified sample design. The total number of subjects from each source was 33,552 and 71,916 respectively. Participants with incomplete data (demographic,

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anthropometric, or laboratory) or those under 19 years of age were excluded, leaving a total

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of 15,704 and 7,081 eligible participants, respectively.

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2.2 Clinical and laboratory measurements

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In the KNHANES, waist circumference was measured using a flexible tape at the narrowest point between the lowest border of the rib cage and the uppermost lateral border of the iliac crest at the end of normal expiration. Blood pressure (BP) was measured 3 times in the sitting

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position after at least 5 min of rest, and an average of the 3 recorded systolic and diastolic BP

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values was used in the analyses. After an 8 hour overnight fast, a venous blood sample was collected and transported to the Central Laboratory (NEODIN Medical Institute, Seoul, Korea). The fasting concentrations of glucose, triglycerides, and high-density lipoprotein cholesterol (HDL-C) were measured according to standard procedures using a Hitachi Automatic Analyzer 7600 (Hitachi, Tokyo, Japan). For accuracy and consistency in each survey, we followed KCDC guidelines that recommend the use of corrected blood pressure and corrected HDL-C values in the KNHANES data23. Pure tone air conduction hearing thresholds were obtained for each ear at frequencies of 500, 1000, 2000, 3000, 4000 and 6000

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Hz by trained audiometric technicians using a calibrated audiometer Model SA203 (Entomed AB, Bariumgatan, Sweden). The test was conducted in a sound-treated booth. In the NHANES, waist circumference was measured using flexible tape between the uppermost lateral border of right ilium and that of left ilium. BP was measured as for

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KNHANES. Fasting plasma concentrations of triglycerides and HDL-C were measured according to standard procedures using a Hitachi 704 analyzer (Hitachi, Tokyo, Japan) from

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1999 to 2004, a Hitachi 912 analyzer (Hitachi, Tokyo, Japan) from 2005 to 2006, and a

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Roche/Hitachi modular P chemistry analyzer (Roche Diagnostics GmbH, Mannheim, Germany) from 2007 to 2012. Fasting plasma concentrations of glucose were measured using

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a Cobas Mira Chemistry system (Roche, Basel, Switzerland) from 1999 to 2004, a Roche 911

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(Roche, Basel, Switzerland) from 2005 to 2006, and a Roche/Hitachi modular P chemistry analyzer (Roche Diagnostics GmbH, Mannheim, Germany) from 2007 to 2012. We followed CDC guidelines that recommend the use of corrected fasting plasma glucose concentration

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and corrected HDL-C values in the NHANES data from 1999 to 200524-26. Pure tone air conduction hearing threshold were obtained exactly as for the KNHANES, with the exception

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2.3 Definition

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that the audiometer used was Model AD226 (Interacoustics, Middelfart, Denmark).

Hearing impairment was defined as a pure tone threshold level greater than 25 decibels hearing level (dB HL) at 500, 1000, 2000, 3000, 4000, 6000 and 8000 Hz 2. We classified participants as having low frequency hearing impairment if the pure tone average of both ears measured at 500, 1000 or 2000 Hz exceeded 25 dB HL. Pure tone threshold impairment at 3000, 4000, 6000 or 8000 Hz were classified as high frequency. DM was defined as a fasting glucose concentration ≥ 126 mg/d, a glucose concentration ≥ 200 mg/dL in an oral 75 g 2hour glucose tolerance test, a hemoglobin A1C ≥ 6.5% or those taking medication for DM.

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2.4 Statistical analysis Demographic, medical condition, anthropometric, clinical measures, and laboratory results data are all presented as the mean or prevalence (%) with 95 % CI. The independent sample t-

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test was used to compare continuous variables and Pearson’s chi-square test was used to compare proportions according to sex and race. Data were analyzed with sampling weights to

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account for multistage and stratified sampling.

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Odds ratios (OR) for the independent association of diabetes with hearing impairment were estimated using multivariate logistic regression models, adjusting for age, sex, socioeconomic

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status, body mass index, leisure time noise exposure, occupational noise exposure, smoking,

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hypertension, and dyslipidemia. Analysis was conducted using SPSS version 21.0 software (IBM, Armonk, NY, USA). All of the tests were 2-sided, and P values <0.05 were considered

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to be statistically significant.

3. Results

Clinical characteristics of the Korean and U.S. populations are presented in Table 1. The

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prevalence of hearing impairment was significantly higher among diabetic participants than

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among non-diabetic participants in all race/ethnicity groups and age subgroups (Table 2 and S1 table). Mean pure tone thresholds (average value of both ears) are presented in relation to glycemic status in Fig. 1. Diabetic participants had significantly higher thresholds at all frequencies than non-diabetic participants, and the disparity became more pronounced at high frequencies in all race/ethnicity groups. To determine if the higher prevalence of hearing impairment in diabetic patients resulted from confounding factors, the data was subjected to multivariate logistic regression model analysis. In the analysis by sex, women but not men with DM showed a significant OR of

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high frequency hearing impairment (Fig 2). This pattern was observed across all race/ethnicity groups, and appeared with a high frequency in NHANES (S1 Fig.). In the further analysis by the age group, women aged 40-59 years with DM were significantly

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associated with high frequency hearing impairment in both the U.S. and Korea (S2 table)

4. Discussion

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Our study evaluates the association between diabetes and hearing impairment in the non-

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institutionalized U.S. population and the Korean population using large population data. The prevalence of hearing impairment was significantly higher among diabetic participants than

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among non-diabetic participants in both sexes and all racial/ethnic groups. When we

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examined hearing thresholds at specific frequencies, we observed higher thresholds at every frequency for diabetic participants compared to non-diabetic participants. This pattern was

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also seen across all groups of race/ethnicity.

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A hypothetical biological mechanism for the association between diabetes and hearing impairment has been proposed. Retinopathy, nephropathy, and peripheral neuropathy are well-established complications of DM and are associated with pathogenic changes to the

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microvasculature and sensory nerves27-30. These pathological changes may affect the

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vasculature and sensory neurons of the inner ear. Previous studies with human temporal bone and animals have shown thickening of the basement membrane of the stria vascularis on the lateral wall of the cochlea, sclerosis of the internal auditory artery, demyelination of the eighth cranial nerve, and atrophy of the spiral ganglion in diabetic patients15-19. However, DM-associated hearing impairment remains controversial, despite several population-based studies indicating that diabetes is a risk factor for hearing impairment 20-22

11-14,

. Horikawa et al. demonstrated an association between DM and hearing impairment in a

meta-analysis with 13 studies, in which the overall pooled OR of hearing impairment for

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diabetic participants was 2.15 (1.72–2.68) compared with non-diabetic participants14. However, there was significant heterogeneity between included studies. This heterogeneity may be due to differences in demographic features and the criteria used to define hearing impairment. The major strength of the present study was to demonstrate the association

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between DM and hearing impairment according to sex and race/ethnicity using a consistent definition for hearing impairment obtained by an audiometric method.

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We found strong associations between diabetes and high frequency hearing impairment for

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all races/ethnicities. This result is consistent with previous studies that described DM-related hearing impairment as progressive, sensorineural impairment with gradual onset

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predominantly affecting higher frequencies22, 31-33. This finding is similar to presbycusis, in

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which high frequency impairment is the first symptom34, 35. Previous studies have reported pathological similarity between DM-related hearing impairment and presbycusis, suggesting

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that DM may accelerate presbycusis via atherosclerotic changes15-19, 35-37.

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One of the most significant findings in the present study was the discrepancy between sexes. According to multivariate logistic regression analysis, only women demonstrated a significant association between DM and high frequency hearing impairment. This

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discrepancy of sex might partially explain the heterogenic results between previous studies.

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To the best of our knowledge, no epidemiological studies address how the sex of individuals with DM affects their predisposition to hearing impairment. The mechanism underlying the sex-specificity of this effect is also unclear. Additional studies are required to further elucidate the effect of sex on hearing impairment in individuals with DM. The present study includes several potential limitations. First, it is a cross sectional study. To clarify the causality between DM and hearing impairment, further prospective studies are needed. Second, because of the lack of data, most participants in NHANES were excluded from this study. Therefore, there might be selection bias and loss of general population

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representation. Third, the data from the US and Korean populations may not be comparable due to differences in laboratory methods. Fourth, we were unable to differentiate participants with type 1 diabetes from those with type 2 diabetes. Finally, although we investigated participants’ history of noise exposure, this information was still limited, most significantly in

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that we did not adjust for residential noise exposure.

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5. Conclusions

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This study suggests that DM was associated with hearing impairment in women only. This pattern was observed across all race/ethnicity groups. Additional studies are required to

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further investigate the effect of sex on hearing impairment in individuals with DM.

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ACCEPTED MANUSCRIPT Figure Legends Fig. 1. Weighted mean of within-person pure tone thresholds (average of both ears) by glycemic status. A. Hispanics, B. Non-Hispanic Whites, C. Non-Hispanic Blacks, D. Korean

Fig. 2. Multivariable-adjusted Odds Ratios (OR) for hearing impairment in diabetic patients

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by sex. A. Low/mid-frequency hearing impairment, B. High-frequency hearing impairment

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Adjusted for age, sex, socioeconomic status, body mass index, leisure time noise exposure,

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occupational noise exposure, smoking, hypertension, and dyslipidemia.

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KNHANES (Unweighted N = 15,704)

Diabetes mellitus (N =1,330)

Pvalue

Age (years)

48.8 (47.050.6)

46.9 (45.248.6)

60.7 (58.662.8)

<0.001

Women (%)

52.2 (50.753.7)

52.7 (51.154.3)

49.2 (45.353.1)

0.149

Tobacco use (%)

48.8 (46.651.0)

48.2 (45.850.6)

52.3 (48.556.2)

0.091

noise

35.7 (32.638.8)

35.0 (31.838-3)

39.8 (35.444.4)

0.040

Leisure time exposure (%)

noise

42.9 (39.446.5)

43.7 (40.147.5)

37.6 (33.641.6)

0.002

index,

28.6 (28.328.9)

28.0 (27.728.3)

32.5 (31.733.3)

<0.001

Hypertension (%)

43.5 (40.346.7)

37.7 (34.840.7)

79.6 (75.783.0)

<0.001

Dyslipidemia (%)

64.3 (62.266.3)

61.0 (58.863.1)

84.9 (82.587.1)

<0.001

122 (121123)

121 (120122)

130 (128132)

<0.001

71 (70-72)

72 (71-72)

69 (67-70)

<0.001

196 (194198) 143 (135151)

197 (195199) 132 (126139)

Total cholesterol, mg/dL Triglyceride, mg/dL

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Systolic blood pressure, mmHg Diastolic blood pressure, mmHg

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mass

193 (189196) 199 (170229)

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Body Kg/m2

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Data are the means or percentage with 95% confidential interval

Diabetes mellitus (N = 1,982)

Pvalue

45.0 (44.545.4)

58.7 (57.959.5)

<0.001

51.3 (50.352.2)

45.3 (42.847.8)

<0.001

44.9 (43.945.9)

51.4 (48.754.0)

<0.001

14.1 (13.315.1)

15.3 (13.217.5)

0.318

27.5 (25.929.2)

31.2 (28.434.2)

0.009

23.6 (23.523.7)

25.3 (25.025.5)

<0.001

22.8 (21.823.8)

55.1 (52.357.9)

<0.001

38.2 (37.239.2)

52.1 (49.254.9)

<0.001

117 (116117)

126 (125127)

<0.001

76 (75-76)

76 (75-76)

77 (76-77)

0.001

188 (188189) 135 (133137)

188 (188189) 129 (127132)

189 (186191) 182 (174190)

46.4 (46.046.9) 50.6 (49.850.2) 45.6 (44.646.5) 14.3 (13.415.1) 27.9 (26.329.6) 23.8 (23.723.8) 26.2 (25.227.2) 39.7 (38.740.6) 118 (117118)

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Occupational exposure (%)

Normal (N =13,722)

Total

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Normal (N =5,751)

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Total

Characteristics

0.022 <0.001

0.960 <0.001

ACCEPTED MANUSCRIPT Table 2. Prevalence of hearing impairment by glycemic status Characteristics

Normal

Diabetes mellitus

P-value

19.0 (17.1-21.0)

38.8 (35.4-42.3)

<0.001

Hispanics

10.6 (8.9-12.7)

24.2 (26.0-43.5)

<0.001

Non-Hispanic Whites

21.7 (19.3-24.3)

43.5 (38.1-49.2)

<0.001

Non-Hispanic Blacks

12.2 (10.1-14.6)

27.8 (22.5-33.8)

<0.001

19.9 (19.0-20.9)

41.7 (39.1-44.2)

52.6 (49.5-55.6)

82.6 (49.5-55.6)

<0.001

Hispanics

36.2 (33.2-39.3)

76.7 (69.3-82.7)

<0.001

Non-Hispanic Whites

58.0 (54.8-61.2)

86.2 (81.8-89.7)

<0.001

Non-Hispanic Blacks

41.4 (35.4-47.8)

78.4 (62.6-88.7)

<0.001

NHANES (U.S adults), (%)

KNHANES (Korean adults), (%)

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Low/mid frequency hearing impairment

KNHANES (Korean adults), (%)

50.7 (49.4-51.9)

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Data are the percentage with 95% confidential interval

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NHANES (U.S adults), (%)

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High frequency hearing impairment

81.1 (78.8-83.3)

<0.001

<0.001

Figure 1

Figure 2

Figure 3