1,614
Views
13
CrossRef citations to date
0
Altmetric
Original Article

Metabolic syndrome is associated with hearing loss among a middle-aged and older Chinese population: a cross-sectional study

, , , , , , , , , , , , , , , & show all
Pages 587-595 | Received 19 Feb 2018, Accepted 20 Apr 2018, Published online: 09 May 2018

Abstract

Background: Although the association of metabolic syndrome (MetS) and hearing loss has been evaluated, findings are controversial. This study investigated this association in a Chinese population.

Methods: A cross-sectional study including a total of 18,824 middle-aged and older participants from the Dongfeng-Tongji Cohort study was conducted. Hearing loss was defined as the pure-tone average (PTA) of frequencies 0.5, 1.0, 2.0, and 4.0 kHz >25 decibels hearing level (dB HL) in the better ear and graded as mild (PTA 26–40 dB HL), moderate (PTA >40 to ≤60 dB HL), and severe (PTA >60 dB HL). MetS was defined according to the International Diabetes Foundation (IDF) criteria of 2005. Association analysis was performed by logistic regression.

Results: After adjustment for potential confounders, participants with MetS showed higher OR of hearing loss (OR, 1.11; 95% CI: 1.03–1.19). The MetS components including central obesity (OR, 1.07; 95% CI: 1.01–1.15) and hyperglycemia (OR, 1.12; 95% CI: 1.04–1.20) were also positively associated with hearing loss. Low HDL-C levels were also associated with higher OR of moderate/severe hearing loss (OR, 1.21; 95% CI: 1.07–1.36).

Conclusions: The MetS, including its components central obesity, hyperglycemia, and low HDL-C levels were positively associated with hearing loss.

    Key messages

  • Studies indicated that cardiovascular disease and diabetes might be risk factors of hearing loss. However, few efforts have been made to establish a direct relationship between metabolic syndrome and hearing loss, especially in Chinese population.

  • In the present study, a cross-sectional design using data from the Dongfeng-Tongji Cohort study was conducted to assess the association between metabolic syndrome and hearing loss.

  • The metabolic syndrome, as well as its components central obesity, hyperglycemia, and low HDL-C levels were positively associated with hearing loss.

View correction statement:
Corrigendum

Introduction

Hearing loss is a significant public health concern affecting more than 36 million people [Citation1]. Its prevalence varies substantially by age, sex, and race, and estimates exceed 30% among people aged 65 and older. In one community-based study, 46% of the participants aged 43–84 years were classified as hearing-impaired on the basis of audiometric examination [Citation2]. Hearing loss is regarded not only as a communication disorder but also as a major disease that severely impairs quality of life, which includes social withdrawal, loss of confidence, depression, and anxiety, both of which have been significantly associated with the cognitive impairment and independence of elderly people [Citation3,Citation4]. However, the pathophysiological mechanisms underlying hearing loss are complicated. Multiple risk factors contribute to hearing loss, including inflammatory processes, genetic susceptibility, and oxidative stress [Citation5,Citation6]. A relationship between hearing loss and obesity [Citation7], diabetes [Citation8], and cardiovascular disease [Citation9] has been demonstrated. Notably, several components of metabolic syndrome, such as elevated blood pressure and dislipidemia, have also been correlated with risk of hearing loss [Citation10].

The metabolic syndrome (MetS) is characterized by a clustering of cardiovascular risk factors including central obesity, elevated blood pressure, increased glucose levels, and dyslipidemia. The prevalence of MetS has been increasing rapidly all over the world. In the United states, the prevalence is estimated to be 27% (25.2% in men and 29% in women) [Citation11]; in China, the overall age-standardized prevalence of MetS was 18.2% according to International Diabetes Foundation (IDF) criteria based on the data from the China Health and Nutrition Survey conducted in 2009 [Citation12]. MetS is related to an increased risk of diabetes, cardiovascular disease, and kidney disease [Citation13,Citation14], as well as an increased risk of mortality from cardiovascular disease and all-cause mortality [Citation15]. Among five components of metabolic syndrome, the prevalence of insulin resistance and central obesity has increased during the last decade [Citation16]. Chronic inflammation, which is associated with insulin resistance and central obesity, is found to be an important factor in the pathophysiology of metabolic syndrome [Citation17]. To date, few efforts have been made to establish a direct relationship between MetS and hearing loss. A retrospective study of 181 participants who suffered from a sudden onset of hearing loss showed that MetS was an independent risk factor [Citation18]. A study of the National Health and Nutrition Examination Survey reported that metabolic syndrome was significantly associated with the hearing threshold in the US adult population (20–65 years old) [Citation19]. However, considering the higher prevalence and the deleterious effects of metabolic syndrome and hearing loss among middle-aged and older population, it is important to elucidate the relationship between the two diseases. The aim of the present study is to investigate the relationship between metabolic syndrome and hearing loss among middle-aged and older population by analyzing the data of the Dongfeng-Tongji Cohort.

Materials and methods

Study population

The Dongfeng-Tongji Cohort study was launched in 2008 among retirees of Dongfeng Motor Corporation (DMC) in Shiyan City, Hubei province [Citation20]. DMC was founded in 1969 and is one of the three largest auto manufacturers in China. After the first follow-up in 2013, we recruited a total of 38,295 retirees. Among all the participants, 19,138 participants received audiological examination, and after excluding those with missing data allowing the determination of MetS, there were 18,824 of the participants for the final analysis. The socio-demographic characteristics were similar between participants included in the present study and those excluded (shown in Supplementary Table S1). The study has been approved by the Medical Ethics Committee of the School of Public Health, Tongji Medical College, and Dongfeng General Hospital, DMC. All participants provided written informed consent.

Data collection

Baseline data were collected by trained interviewers via epidemiological questionnaire during face-to-face interviews. Information on socio-demographic factors, health status, and lifestyle factors including smoking status, alcohol consumption status, and physical activity were included in the questionnaires.

The general health examination was performed at the same time. Standing height, body weight, waist circumference, and hip circumference were measured with participants in light indoor clothing and without shoes. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. Systolic and diastolic blood pressure were measured with mercurial sphygmomanometer in one arm while the subject was seated after resting for about 10 min.

All subjects were examined in the morning after overnight fasting and 15 miniliters of fasting blood was drawn with three vacuum (ethylenediamine tetraacetic acid, EDTA) anticoagulation tubes for plasma; coagulation tube for serum. Blood glucose level was determined through Glucose Oxidase method by Abbott Aroset analyzer. Triglyceride, total cholesterol, LDL cholesterol and HDL cholesterol levels were measured by the hospital’s laboratory with ARCHITECT Ci8200 automatic analyzer (ABBOTT Laboratories. Abbott Park, IL) using the Abbott Diagnostics reagents according to the instructions of the manufacturer. Whole-blood samples obtained from the participants were immediately assayed for HbA1c level with high-performance liquid chromatography (D-10 System; BIO-Rad Laboratories, Hercules, CA).

Assessment of covariates

Based on the self-reported alcohol consumption status, participants were grouped as ex-, current, and non-alcohol consumers. As the sample size of ex-smokers (13%) and ex-alcohol consumers (6%) was small, we combined them into non-smokers and non-alcohol consumers. Other variables were dichotomized as yes or no on the basis of the responses to questions on physical activity, past history of coronary heart disease (CHD), diabetes, hypertension, the use of lipid and/or blood pressure lowering drugs, use of diabetes medication (insulin or oral hypoglycemic agent), and use of ototoxic drugs (gentamicin, streptomycin, and kanamycin).

Audiological examination

A detailed hearing-related questionnaire including family history of deafness, type of deafness, past use of ototoxic drugs, and history of occupational noise exposure was completed by trained interviewers during face-to-face interviews. Pure-tone audiometry at both ears was performed by audiologists within soundproof rooms (background noise less than 30 dB) in the quiet environment (background noise less than 40 dB). Audiological examination was performed with Micro-DSP ZD21 at the DMC-owned hospital. In order to minimize the measurement error, all audiologists used the same method ‘heard then go down 10 dB, and no-heard go up 5 dB’ and uniformed the diagnosis standards on the sound time and waiting time, the way to explain procedures to subjects, and other manipulation details to guarantee the consistency of testing method.

Pure tone air conduction hearing thresholds were obtained for both ears at frequencies of 0.5, 1.0, 2.0, and 4.0 kHz. Hearing loss was defined as the pure-tone average (PTA) of audiometric hearing thresholds at 0.5, 1.0, 2.0, and 4.0 kHz (PTA0.5–4kHz) > 25 decibels hearing level (dB HL) in the better of the two ears, defining mild hearing loss as PTA0.5–4kHz >25 to ≤40 dB HL; moderate hearing loss as PTA0.5–4kHz >40 to ≤60 dB HL; severe hearing loss as PTA0.5–4kHz >60 dB HL. In the current study the sample size of severe hearing-impaired subjects was relatively small (2.9%); we combined them into moderate hearing-impaired subjects.

Definition of metabolic syndrome

In the present study, the IDF criteria of 2005 [Citation21] was used to define MetS. These criteria are similar to the modified US National Cholesterol Education Program's Adult Treatment Panel III criteria (NCEP) [Citation17]. The IDF definition of MetS includes central obesity (waist circumference ≥90 cm in Chinese men and ≥80 cm in Chinese women) plus any 2 of the following four factors: (1) high blood pressure: systolic ≥130 mm Hg, diastolic ≥85 mm Hg, or known treatment for hypertension; (2) hypertriglyceridemia: fasting serum triglycerides ≥1.7 mmol/l; (3) low high-density lipoprotein cholesterol (HDL-C): fasting HDL-C < 1.0 mmol/l in men and <1.3 mmol/l in women; and (4) hyperglycaemia: fasting glucose level of ≥5.6 mmol/l (≥ 100 mg/dl) or known treatment for diabetes.

Data analysis

All statistical analyses were performed using SPSS 13.0 software (SPSS, Chicago, IL). Categorical variables were expressed in percentages and compared by Chi-square analysis. Continuous variables were expressed in means ± SD and compared by analysis of variation (ANOVA) unless otherwise specified. We computed multivariable adjusted odds ratios (ORs) and 95% confidence intervals (CIs) for hearing loss by multinomial logistic regression model. In multivariate model 1, adjusted variables were age, sex, smoking, alcohol consumption plus family history of deafness, use of ototoxic drugs, and history of occupational noise exposure. Multivariate model 2 additionally included the use of lipid and/or blood pressure lowering drugs, and use of diabetes medication. For associations of each MetS component with hearing loss, analyses were further adjusted for the other components of the metabolic syndrome as dichotomized variables. We further assessed the association between general obesity and hearing loss by multivariate models including potential confounders. BMI (kg/m2) was classified into thinness (<18.5), normal (18.5–24.0), overweight (24.0–28.0), and obesity (≥28.0) according to Chinese standard [Citation22]. A two-side p value of <.05 was considered to be statistically significant.

Results

A total of 18,824 individuals (8366 males and 10,458 females with an average age of 64.7 years) were included in this study, and prevalence of hearing loss was 52.3%. Characteristics of the study population according to different degrees of hearing loss are summarized in . The prevalence of MetS was higher among hearing-impaired subjects. Compared with those with normal hearing, individuals with hearing loss were more likely to be males, older, smokers, alcohol consumers, exposed to occupational noise, and had higher levels of BMI, waist circumference, systolic blood pressure, fasting glucose, and lower HDL-C. However, individuals with hearing loss had lower levels of total cholesterol and LDL-C, which was probably due to the use of lipid-lowering medication.

Table 1. General characteristics of subjects according to hearing loss degree.

General characteristics among participants with and without MetS are summarized in Supplementary Table S2. The prevalence of hearing loss was 54.9% among subjects with MetS and was significantly higher than those without MetS (50.7%).

Association between MetS and hearing loss

The association between MetS and hearing loss are presented in . As shown in this table, individuals with MetS had higher OR of hearing loss compared with individuals without MetS (OR, 1.10; 95% CI: 1.03–1.18; p = .004) after adjustment for age and sex. Further adjustment for lifestyle parameters including smoking, alcohol consumption plus family history of deafness, use of ototoxic drugs, and history of occupational noise exposure did not materially alter the association (OR, 1.11; 95% CI: 1.03–1.18; p = .004). Additional adjustment for medication history got similar results (OR, 1.11; 95% CI: 1.03–1.19; p = .004). Furthermore, MetS was also significantly associated with mild hearing loss (OR, 1.10; 95% CI: 1.02–1.18; p = .014) as well as moderate/severe hearing loss after full adjustment (OR, 1.17; 95% CI: 1.05–1.29; p = .003).

Table 2. Multivariate models of metabolic syndrome associated with hearing loss, presented as or with 95% CI.

Associations between MetS components and hearing loss

In the present study, the association between MetS components and hearing loss were also assessed (). Among all the five components, central obesity (OR, 1.08; 95% CI: 1.01–1.16; p = .017), low HDL-C levels (OR, 1.10; 95% CI: 1.02–1.19; p = .018), and hyperglycemia (OR, 1.12; 95% CI: 1.05–1.19; p = .001) were all significantly associated with hearing loss after adjustment for age and sex. Further adjustment for smoking, alcohol consumption, family history of deafness, use of ototoxic drugs, and history of occupational noise exposure got similar results. Additional adjustment for other components of MetS turned the association between low HDL-C levels and hearing loss into null, and reduced the effects of central obesity (OR, 1.07; 95% CI: 1.01–1.15; p = .029) and hyperglycaemia (OR, 1.12; 95% CI: 1.04–1.20; p = .002) on hearing loss but the positive association still remained significant. The positive association of low HDL-C levels with moderate/severe hearing loss still remained even in the full adjustment model (OR, 1.21; 95% CI: 1.07–1.36; p = .002). No significant association was observed between elevated blood pressure and hearing loss.

Table 3. Multivariate models of metabolic syndrome components associated with hearing loss, presented as or with 95% CI.

We further examined the association between BMI and hearing loss ( and Supplementary Table S3). General obesity was significantly associated with hearing loss after adjustment for age and sex (OR, 1.17; 95% CI: 1.06–1.29; p = .002). Further adjustment for smoking, alcohol consumption, family history of deafness, use of ototoxic drugs, and history of occupational noise exposure obtained similar results (OR, 1.17; 95% CI: 1.06–1.30; p = .003). Additional adjustment for metabolic syndrome components except for central obesity did not materially change the results (OR, 1.15; 95% CI: 1.03–1.28; p = .011). General obesity was also significantly associated with different degrees of hearing loss after multivariable adjustment. Additional adjustment for central obesity attenuated the positive associations to marginal significance.

Figure 1. Odds ratios (95% CI) for hearing loss and its degrees according to different groups of BMI. Within each group from left to right: thinness, normal, overweight and obesity. The adjusted covariates included age, sex, smoking, alcohol consumption, family history of deafness, use of ototoxic drugs, history of occupational noise exposure, and metabolic syndrome components except for central obesity. The reference group was normal BMI (18.5–24.0 kg/m2).

Figure 1. Odds ratios (95% CI) for hearing loss and its degrees according to different groups of BMI. Within each group from left to right: thinness, normal, overweight and obesity. The adjusted covariates included age, sex, smoking, alcohol consumption, family history of deafness, use of ototoxic drugs, history of occupational noise exposure, and metabolic syndrome components except for central obesity. The reference group was normal BMI (18.5–24.0 kg/m2).

Preceding studies suggested that stoke might be associated with hearing function and affect acoustic organ. In the present study, when we excluded individuals with past history of stroke (4.1%), the results did not materially alter (data not shown).

Stratification analysis

Stratification analysis by sex (Supplementary Table S4) and noise exposure (Supplementary Table S5) was also performed. As shown in Supplementary Table S4, hyperglycaemia was significantly associated with hearing loss in men (OR, 1.16; 95% CI: 1.04–1.28; p = 0.007). Central obesity (OR, 1.11; 95% CI: 1.01–1.22; p = .028) and low HDL-C levels (OR, 1.13; 95% CI: 1.02–1.24; p = .021) were positively associated with hearing loss prevalence in women. In Supplementary Table S5, MetS was positively associated with hearing loss among participants both with and without noise exposure after full adjustment. Hyperglycaemia was positively associated with hearing loss among participants without noise exposure (OR, 1.15; 95% CI: 1.05–1.26; p = .002). While in those with noise exposure, significant association was observed between central obesity and hearing loss (OR, 1.14; 95% CI: 1.02–1.27; p = .020).

Discussion

Aging is becoming a global health issue. Aging-associated chronic diseases such as cardiovascular disease and metabolic syndrome impair people’s health and result in multiple organ dysfunction [Citation23]. In this large cross-sectional study, we found that MetS as well as its components central obesity, hyperglycaemia, and low HDL-C levels were independently associated with higher OR of hearing loss.

Preceding studies assessing the relationship between hypertension and hearing loss differ by study design, methods, and subjects. Data from NHANES 1999–2004 showed that hypertension was associated with high prevalence of hearing loss [Citation24,Citation25]. However, the Health Professionals Follow-up Study did not find significant association between them [Citation26]. In the present study, hypertension was not significantly associated with hearing loss in multivariate-adjusted models. One potential reason is that cross-sectional studies fail to determine temporal or causative relations between a given exposure and outcome. As hearing loss has been shown to be an independent risk factor of cardiovascular disease [Citation9], it is possible that cochlear damage associated with cardiovascular disease occurred prior to the diagnoses of hypertension.

The results of the current study indicated a significant relationship between reduced levels of HDL-C and hearing loss, which was consistent with findings of preceding studies [Citation9,Citation27]. HDL-C was reported to have anti-apoptotic, anti-oxidant, anti-inflammatory, and nitric oxide-promoting effects [Citation28]. Nitric oxide, which was produced in the cochlear blood vessels, contributed to the regulation of cochlear blood flow, and its level might be related to different forms of hearing impairment [Citation29,Citation30]. Reactive oxygen species formation in the inner ear, which caused cellular death, vasoconstriction, and reduced cochlear blood flow, also played a key role in hearing loss [Citation5,Citation31].

General and central obesity were found to be significantly associated with hearing loss in the present study. However, the association turned into null after adjustment for each other, which was probably due to the strong correlation between BMI and waist circumference. Obesity was found to be associated with hearing loss in both human and animal researches [Citation32,Citation33]. Adipose tissue is considered as an endocrine organ, releasing hormones and cytokines, and affecting appetite, insulin resistance, and energy metabolism [Citation34]. Adiponectin is an adipocytokine synthesized and released by adipose tissue and presents in low concentrations in obese individuals [Citation35] and those with MetS [Citation36]. That is, adiponectin concentrations are inversely associated with BMI, waist circumference, insulin resistance, and triglyceride, and directly associated with HDL-C concentration [Citation36]. Studies have suggested that adiponectin could protect peripheral hearing function [Citation32]. Other factors affecting the relationship between obesity and hearing loss might involve obesity-related atherosclerosis of the internal auditory artery and a reduction in cochlear blood flow [Citation33]. Under conditions of obesity-related oxidative stress, a reduction in flow-mediated arterial dilation and damage resulting from the accumulation or reactive oxygen species in auditory epithelia may cause hearing loss [Citation37].

Recent studies investigating the association between diabetes and hearing loss have been limited to several small studies with inconsistent results [Citation7,Citation9,Citation25,Citation38–41]. The Kurabuchi study found glycosylated haemoglobin positively associated with hearing impairment among older Japanese [Citation41], while the Framingham study found no association between hearing loss and either diabetes or impaired glucose tolerance [Citation9]. Several biological mechanisms might explain the association between hyperglycaemia and hearing loss. Complications of diabetes, such as retinopathy, nephropathy, and peripheral neuropathy, presented pathogenic changes in the microvasculature and sensory nerves [Citation42]. These pathologic changes may plausibly involve the capillaries and sensory neurons of the inner ear. Post-mortem observations of hyperglycaemic and diabetic patients include thickening of capillaries within the striavascularis [Citation43] and demyelination of the eighth cranial nerve, one branch of which transmits auditory signals from the cochlea to the brain stem [Citation44]. Pathologic changes specific to the cochlea also include thickened walls of the vessels of the basilar membrane and greater loss of outer hair cells in the lower basal turn [Citation43]. Other vascular changes such as narrowing of the internal auditory artery were also included [Citation45]. Furthermore, elevated plasma glucose [Citation46] was associated with increased oxidative stress and preceding studies indicated that oxidative stress was involved in the pathogenesis of noise induced hearing loss [Citation47–49]. Thereby the association between hyperglycaemia and hearing loss might be partially explained by oxidative stress, which was reported to be increased in hyperglycaemic subjects [Citation46].

In addition, as aforementioned, the prevalence of hearing loss was 52.3%, 53.6%, and 51.4% among all the participants, those with noise exposure, and those without noise exposure, respectively. Prevalence of hearing loss in those with noise exposure was slightly higher than those without noise exposure. One study based on a survey among population from four provinces indicated that about 53.65% of studied population aged 60–74 years were diagnosed with hearing loss in 2015 [Citation50], similar with the prevalence of the present population, which was probably due to the different population, different age distributions, and efficient prevention strategies of occupational noise hazards in DMC.

Several strengths of the present study are needed to highlight. First, few studies investigated the association between MetS and hearing loss among Chinese population, the present study provides new evidence from different population. Second, more than 15,000 participants were included in the present study; evidence based on this large sample size are more powerful and convincible. Third, the audiological examination and ascertainment of MetS were standardized and restrict; in addition, in the multivariate model, we adjusted for several potential confounders, which assisted us to minimize the bias.

Several limitations also need to be considered. First, the cross-sectional design only allows us to assess associations; the underlying cause–effect relationship cannot be defined and still remained to be validated in prospective cohort study. Second, the population stratification might bias our results. However, the present study population is highly homogeneous by including only Chinese population. In addition, the measurement of ototoxic drugs did not involve dose or frequency in the past. Last, our analyses were restricted to the middle-aged and older population; results might not be generalized to young people directly.

In summary, there was a positive association between MetS and hearing loss in the middle- and old-aged Chinese population; the components including central obesity, hyperglycaemia, and low HDL-C levels of MetS also significantly associated with hearing loss, suggesting that MetS might be a potential risk factor of hearing loss.

Supplemental material

Xu_Han_et_al.__Supplementary_Materials.docx

Download MS Word (35.2 KB)

Acknowledgements

The authors would like to thank all study subjects for participating in the present Dongfeng-Tongji Cohort study as well as all volunteers for assisting in collecting the sample and questionnaire data. We also acknowledge all the staff for collecting the clinic data.

Disclosure statement

The authors declare that they have no conflict of interest.

Additional information

Funding

This work was supported by the grant from the National Natural Science Foundation [Grants NSFC-81522040, 81230021, and 81473051]; National Key R&D Program of China [2017YFC0907501], the Program for HUST Academic Frontier Youth Team, the 111 Project (No. B12004); the Program for Changjiang Scholars; Innovative Research Team in University of Ministry of Education of China (No. IRT1246); and China Medical Board (No. 12-113).

Reference

  • Pleis JR, Lethbridge-Cejku M. Summary health statistics for U.S. adults: National Health Interview Survey, 2005. Vital and Health Statistics Series 10, Data from the National Health Survey 2006. pp. 1–153.
  • Cruickshanks KJ, Wiley TL, Tweed TS, et al. Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study. Am J Epidemiol. 1998;148:879–886.
  • Dalton DS, Cruickshanks KJ, Klein BE, et al. The impact of hearing loss on quality of life in older adults. Gerontologist. 2003;43:661–668.
  • Strawbridge WJ, Cohen RD, Shema SJ, et al. Successful aging: predictors and associated activities. Am J Epidemiol. 1996;144:135–141.
  • Fujimoto C, Yamasoba T. Oxidative stresses and mitochondrial dysfunction in age-related hearing loss. Oxid Med Cell Longev. 2014;2014:582849.
  • Verschuur CA, Dowell A, Syddall HE, et al. Markers of inflammatory status are associated with hearing threshold in older people: findings from the Hertfordshire ageing study. Age Ageing. 2012;41:92–97.
  • Cruickshanks KJ, Nondahl DM, Dalton DS, et al. Smoking, central adiposity, and poor glycemic control increase risk of hearing impairment. J Am Geriatr Soc. 2015;63:918–924.
  • Mitchell P, Gopinath B, McMahon CM, et al. Relationship of Type 2 diabetes to the prevalence, incidence and progression of age-related hearing loss. Diabetic Med: J Br Diabetic Assoc. 2009;26:483–488.
  • Gates GA, Cobb JL, D’Agostino RB, et al. The relation of hearing in the elderly to the presence of cardiovascular disease and cardiovascular risk factors. Arch Otolaryngol – Head Neck Surg. 1993;119:156–161.
  • Evans MB, Tonini R, Shope CD, et al. Dyslipidemia and auditory function. Otol Neurotol: Official Publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology. 2006;27:609–614.
  • Ford ES, Giles WH, Mokdad AH. Increasing prevalance of the metabolic syndrome among U.S adults. Diabetes Care. 2004;27:2444–2449.
  • Xi B, He D, Hu YH, et al. Prevalence of metabolic syndrome and its influencing factors among the Chinese adults: The China Health and Nutrition Survey in 2009. Prev Med. 2013;57:867–871.
  • Fox CS, Larson MG, Leip EP, et al. Glycemic status and development of kidney disease – The Framingham Heart Study. Diabetes Care. 2005;28:2436–2440.
  • Isomaa B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24:683–689.
  • Trevisan M, Liu J, Bahsas FB, et al. Syndrome X and mortality: a population-based study. Am J Epidemiol. 1998;148:958–966.
  • Beltran-Sanchez H, Harhay MO, Harhay MM, et al. Prevalence and trends of metabolic syndrome in the adult U.S. population, 1999–2010. J Am Coll Cardiol. 2013;62:697–703.
  • Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112:2735–2752.
  • Chien CY, Tai SY, Wang LF, et al. Metabolic syndrome increases the risk of sudden sensorineural hearing loss in Taiwan: a case–control study. Otolaryngol Head Neck Surg. 2015;153:105–111.
  • Sun YS, Fang WH, Kao TW, et al. Components of metabolic syndrome as risk factors for hearing threshold shifts. PLoS One. 2015;10:e0134388.
  • Wang F, Zhu J, Yao P, et al. Cohort Profile: the Dongfeng-Tongji cohort study of retired workers. Int J Epidemiol. 2013;42:731–740.
  • Alberti KGMM, Zimmet P, Shaw J. The metabolic syndrome-a new worldwide definition. Lancet. 2005;366:1059–1062.
  • Zhou BF. Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults – study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Biomed Environ Sci. 2002;15:83–96.
  • Oh IH, Lee JH, Park DC, et al. Hearing loss as a function of aging and diabetes mellitus: a cross sectional study. PLoS One. 2014;9:e116161.
  • Agrawal Y, Platz EA, Niparko JK. Prevalence of hearing loss and differences by demographic characteristics among US adults: data from the National Health and Nutrition Examination Survey, 1999–2004. Arch Intern Med. 2008;168:1522–1530.
  • 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.
  • Shargorodsky J, Curhan SG, Eavey R, et al. A prospective study of cardiovascular risk factors and incident hearing loss in men. Laryngoscope. 2010;120:1887–1891.
  • Suzuki K, Kaneko M, Murai K. Influence of serum lipids on auditory function. Laryngoscope. 2000;110:1736–1738.
  • Luscher TF, Landmesser U, von Eckardstein A, et al. High-density lipoprotein: vascular protective effects, dysfunction, and potential as therapeutic target. Circ Res. 2014;114:171–182.
  • Brechtelsbauer PB, Nuttall AL, Miller JM. Basal nitric oxide production in regulation of cochlear blood flow. Hear Res. 1994;77:38–42.
  • Heinrich UR, Helling K. Nitric oxide – a versatile key player in cochlear function and hearing disorders. Nitric Oxide: Biol Chem/Off J Nitric Oxide Soc. 2012;27:106–116.
  • Henderson D, Bielefeld EC, Harris KC, et al. The role of oxidative stress in noise-induced hearing loss. Ear Hear. 2006;27:1–19.
  • Hwang JH, Hsu CJ, Yu WH, et al. Diet-induced obesity exacerbates auditory degeneration via hypoxia, inflammation, and apoptosis signaling pathways in CD/1 mice. PLoS One. 2013;8:e60730.
  • Lalwani AK, Katz K, Liu YH, et al. Obesity is associated with sensorineural hearing loss in adolescents. Laryngoscope. 2013;123:3178–3184.
  • Ahima RS. Adipose tissue as an endocrine organ. Obesity. 2006;14:242–249.
  • Yang WS, Lee WJ, Funahashi T, et al. Plasma adiponectin levels in overweight and obese Asians. Obes Res. 2002;10:1104–1110.
  • Huang KC, Lue BH, Yen RF, et al. Plasma adiponectin levels and metabolic factors in nondiabetic adolescents. Obes Res. 2004;12:119–124.
  • Loffredo L, Martino F, Carnevale R, et al. Obesity and hypercholesterolemia are associated with NOX2 generated oxidative stress and arterial dysfunction. J Pediatr – Us. 2012;161:1004–1009.
  • Cullen JR, Cinnamond MJ. Hearing loss in diabetics. J Laryngol Otol. 1993;107:179–182.
  • Dalton DS, Cruickshanks KJ, Klein R, et al. Association of NIDDM and hearing loss. Diabetes Care. 1998;21:1540–1544.
  • Ma FC, Gomez-Marin O, Lee DJ, et al. Diabetes and hearing impairment in Mexican American adults: a population-based study. J Laryngol Otol. 1998;112:835–839.
  • Michikawa T, Mizutari K, Saito H, et al. Glycosylated hemoglobin level is associated with hearing impairment in older Japanese: the Kurabuchi Study. J Am Geriatr Soc. 2014;62:1231–1237.
  • Ciulla TA, Amador AG, Zinman B. Diabetic retinopathy and diabetic macular edema – pathophysiology, screening, and novel therapies. Diabetes Care. 2003;26:2653–2664.
  • Fukushima H, Cureoglu S, Schachern PA, et al. Cochlear changes in patients with type 1 diabetes mellitus. Otolaryngol Head Neck Surg. 2005;133:100–106.
  • Li XY, Shi X, Wang CJ, et al. Pathological changes of the inner ear cochlea in different time windows of murine cytomegalovirus-induced hearing loss in a mouse model. Acta Oto-Laryngol. 2015;135:536–541.
  • Ikuno Y, Comi F, Tano Y. Potent retinal arteriolar traction as a possible cause of myopic foveoschisis. Am J Ophthalmol. 2005;139:462–467.
  • Ceriello A, Mercuri F, Quagliaro L, et al. Detection of nitrotyrosine in the diabetic plasma: evidence of oxidative stress. Diabetologia. 2001;44:834–838.
  • Fechter LD, Klis SFL, Shirwany NA, et al. Acrylonitrile produces transient cochlear function loss and potentiates permanent noise-induced hearing loss. Toxicol Sci. 2003;75:117–123.
  • Kaygusuz I, Ozturk A, Ustundag B, et al. Role of free oxygen radicals in noise-related hearing impairment. Hear Res. 2001;162:43–47.
  • Yamasoba T, Pourbakht A, Sakamoto T, et al. Ebselen prevents noise-induced excitotoxicity and temporary threshold shift. Neurosci Lett. 2005;380:234–238.
  • Hu XY, Zheng XY, Ma FR, et al. Prevalence of hearing disorders in China: a population-based survey in four provinces of China. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi = Chinese Journal of Otorhinolaryngology Head and Neck Surgery. 2016;51:819–825.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.