International Journal of Audiology 2015; 54: 265–273

Original Article

Hearing impairment among adults: The impact of cardiovascular diseases and cardiovascular risk factors Venla Lohi*,†, Samuli Hannula*,†, Pasi Ohtonen‡, Martti Sorri*,† & Elina Mäki-Torkko*,§ *Institute of Clinical Medicine, Department of Otorhinolaryngology, University of Oulu, Finland, †Department of Otorhinolaryngology and Head and Neck Surgery, Oulu University Hospital, Northern Ostrobothnia Hospital District, Oulu, Finland, ‡Departments of Surgery and Anesthesiology, Oulu University Hospital, Northern Ostrobothnia Hospital District, Oulu, Finland, §Department of Clinical and Experimental Medicine/Technical Audiology, Faculty of Health Sciences, Linköping University, and Department of ENT-Head Neck Surgery, County Council of Östergötland, Linköping, Sweden

Abstract Objective: To investigate the influence of cardiovascular diseases on hearing impairment (HI) among adults. Furthermore, to seek other potential risk factors for HI, such as smoking, obesity, and socioeconomic class. Design: A cross-sectional, unscreened, populationbased, epidemiological study among adults. Study sample: The subjects (n ⫽ 850), aged 54–66 years, were randomly sampled from the population register. A questionnaire survey, an otological examination, and pure-tone audiometry were performed. Results: Cardiovascular diseases did not increase the risk for HI in a propensity-score adjusted logistic regression model: OR 1.24, 95% CI 0.79 to 1.96 for HI defined by better ear hearing level (BEHL), and OR 1.48, 95% CI 0.96 to 2.28 for HI defined by worse ear hearing level (WEHL), in the 0.5–4 kHz frequency range. Heavy smoking is a risk factor for HI among men (BEHL: OR 1.96, WEHL: OR 1.88) and women (WEHL: OR 2.4). Among men, obesity (BEHL, OR 1.85) and lower socioeconomic class (BEHL: OR 2.79, WEHL: OR 2.28) are also risk factors for HI. Conclusion: No significant association between cardiovascular disease and HI was found.

Key Words: Hearing impairment; adult; cardiovascular disease; diabetes; body mass index; smoking; socioeconomic class

Hearing impairment (HI) is a common disorder among adults and can cause many psychosocial problems (Nachtegaal et al, 2009). HI also impairs the quality of life (Gopinath et al, 2012). The aetiology of adult-onset HI is considered to be multifactorial: noise exposure, cardiovascular diseases (CVD), and related risk factors such as obesity, hypertension (HT), diabetes mellitus (DM), smoking, and socioeconomic factors have been found to be associated with HI (Agrawal et al, 2008; Fransen et al, 2008; Cruickshanks et al, 2010). The role of CVD in HI has interested researchers at least since the 1960s. Rosen et al (1962) studied hearing with pure-tone audiometry among Mabaan tribe people, a noise-free population in Sudan. The study population consisted of 541 unselected subjects, aged 10 to 90 years. None of them had hypertension (HT) or were overweight. The Mabaans retained good hearing during their life. They had better hearing thresholds generally and particularly at the higher frequencies compared to relatively healthy people in an urban environment. The authors concluded that the possible explanations could be the noise-free environment and lack of CVD. Rosen et al (1964) also

conducted a hospital-based clinical intervention study and found that patients with diet low in saturated fat had better hearing compared to patients with normal diet. There are still only few population-based studies on the influence of CVD on hearing among adults. In the Framingham cohort (n ⫽ 1662), the association between CVD events (including coronary heart disease, stroke, and intermittent claudication) and worse hearing thresholds was found in low frequencies (Gates et al, 1993). In another population-based study of Torre et al (2005), participants (n ⫽ 1501) were tested with distortion product otoacoustic emissions, and they found that history of myocardial infarct was associated with sensorineural HI among women, but not among men. HT is the main risk factor for cardiovascular disease (Mancia et al, 2007) and has been linked with HI in some previous studies. In the Framingham cohort, HT was defined as systolic blood pressure (BP) greater than 160 mmHg, diastolic BP greater than 95 mmHg, or the use of antihypertensive medication. Hypertensive men had worse hearing in high frequencies (4, 6, and 8 kHz), whereas among

Correspondence: Venla Lohi, Department of Clinical Medicine, Otorhinolaryngology, University of Oulu, PO Box 5000, FI-90014, Oulu, Finland. E-mail: [email protected] (Received 12 August 2013; accepted 3 October 2014 )

ISSN 1499-2027 print/ISSN 1708-8186 online © 2014 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society DOI: 10.3109/14992027.2014.974112

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Abbreviations ARHI BEHL BP CI CVD DM HI HL HT OR PTA WEHL SEC

Age-related hearing impairment Better ear hearing level Blood pressure Confidence interval Cardiovascular disease Diabetes mellitus Hearing impairment Hearing level Hypertension Odds ratios Pure tone average Worse ear hearing level Socioeconomic class

women, HT was associated with worse hearing at the low frequencies (0.25, 0.5, and 1 kHz) (Gates et al, 1993). Association between high BP (relative risks per 20 mmHg difference were counted) and HI was found for male subjects without otological risk factors or stroke in a longitudinal study (Brant et al, 1996). In a Swedish cohort study, high systolic BP was associated with worse hearing levels at the low frequencies (0.25, 0.5, and 1 kHz) among 79-year-old women but not among 70- or 75-year old women or men, when hearing was compared to quartiles of BP levels (Rosenhall & Sundh, 2006). In a US population (age range 20 to 69 years), HT (defined by a physician diagnosis, systolic BP level higher than 140, or diastolic BP level higher than 90 mmHg, or the use of antihypertensive medication) had association with HI only at 1 kHz (Agrawal et al, 2009). On the other hand, in a European population-based multicenter study, no significant association between HT and HI was found (HT defined by a physician diagnosis, systolic BP level higher than 140, or diastolic BP level higher than 90 mmHg, or the use of antihypertensive medication) (Fransen et al, 2008). Some other CVD markers have also been linked to HI. In the Beaver Dam Offspring study, a larger retinal vein equivalent and higher hematocrit percentage were associated with HI (Nash et al, 2011). In a Finnish study, a significant association between LDL-cholesterol level and HI was found (Pyykko et al, 1988), and in the Framingham study, an association was found between low levels of high-density lipoprotein and HI among women (Gates et al, 1993). The association between non-insulin-dependent DM and HI was investigated in the Epidemiology of Hearing Loss study, with 3571 subjects aged 43–84 years (Dalton et al, 1998). In a univariate analysis, subjects with non-insulin-dependent DM (mean age 69.6 years) were more likely to have HI than subjects without diabetes (mean age 65.1 years). However, the difference was not significant after controlling for age. In another population-based study, DM was associated with significantly increased hearing thresholds in the 0.5–8 kHz frequency range among 20–69 year-old subjects (Agrawal et al, 2009). Only few studies exist concerning stroke and HI, and stroke has been linked with sudden sensorineural hearing loss rather than agerelated HI (Lin et al, 2008). According to Gopinath et al (2009), subjects with moderate to severe hearing loss are more likely to report previous stroke but the incidence of stroke in five-year follow-up was not increased among subjects with any degree of HI. Of CVD-related risk factors, smoking has been linked to HI in many studies. In a study of one thousand 50-year-old men without

noise exposure, right-ear hearing was worse among smokers than non-smokers (Drettner et al, 1975). Rosenhall et al (1993) found a positive association between HI and smoking in older men in a Swedish cross-sectional study. In a rural Malaysian village, a dosedependent effect of smoking to HI has been found among men without noise exposure (Noorhassim & Rampal, 1998). There is also more recent evidence on smoking increasing the risk for HI (Itoh et al, 2001; Fransen et al, 2008). In a US population-based study, heavy smokers (more than 20 pack-years) had poorer hearing levels (Agrawal et al, 2009). However, an association between smoking and hearing loss has not always been found (Gates et al, 1993; Brant et al, 1996). Persons with higher education at the age of 20–69 years showed better hearing than those with lower education after adjusting for confounding factors (age, sex, race/ethnicity, education, smoking, noise exposure, DM, and HT) in a cross-sectional population-based study in the US (Agrawal et al, 2008). In a longitudinal US study, socioeconomic status has been found to be associated with HI, as those with lower status had a higher hazard ratio for a 10-year cumulative incidence of HI (Cruickshanks et al, 2010). Social class has been found to have an influence on low- and high-frequency hearing even if noise exposure and tympanic membrane pathology have been taken into account (Rudin et al, 1988). In addition, parents’ social class is suggested to have an appreciable effect on subjects’ hearing in middle age (Rosenhall & Pedersen, 1995). In studies concerning alcohol use and HI, moderate alcohol use has been found to have a protective effect on hearing (Fransen et al, 2008; Gopinath et al, 2009). In a Japanese study of metal company workers, a similar protective effect of moderate alcohol use was found, and heavy drinking did not increase the risk for HI (Itoh et al, 2001), but in a Swedish study, alcohol abuse increased the risk for HI in 70-year-old males (Rosenhall et al, 1993). We have previously reported from the sample of the present study that prevalence of HI (pure-tone average of 0.5, 1, 2, and 4 kHz frequencies 20 dB or greater in the better ear) is high (26.9%) among 55–64 year-old adults (Hannula et al, 2010). We also know that aging, gender, and otological risk factors are associated with HI in this population (Hannula et al, 2012). The hypothesized mechanism for the influence of CVD on hearing is that CVD reduces the circulation of the cochlea and causes atrophy of the stria vascularis (Schuknecht & Gacek, 1993) and based on epidemiological studies, there is also some evidence about association between CVD or related risk factors and HI. In the present study, our primary aim was to investigate the association between CVD and HI in a cross-sectional, randomly sampled, unscreened population. Furthermore, the influence of cardiovascular risk factors (HT, hypercholesterolemia, DM, smoking, and obesity), SEC, and alcohol use on HI were studied.

Methods Subjects The study subjects were randomly sampled from the population register. The subjects were recruited in conjunction with the European ARHI Project (QLRT-2001-00331), a multicenter study to investigate age-related HI. A total of 1428 letters were mailed in 2003 and 2004 to native Finnish subjects living in the city of Oulu or the surrounding areas, Northern Finland. Altogether 60% of invited subjects participated. Data on 850 subjects, aged 54–66 years, are included in the study. The proportion of men was 45.1% (383). To analyse the non-participants, a short questionnaire was sent to 400 of the 549

Cardiovascular diseases and HI among adults non-participants. After two rounds of reminder letters 246 (62%) replies were received. The proportion of men was higher among the non-responders (55.8%) than among the responders (45.1%) and the non-responders were slightly younger (mean age 57.5 years) than the responders (mean age 60.9 years). There were no marked differences in general health, smoking habits, or ear diseases between the participants and the non-participants. However, answers to the question ‘Do you have any difficulty with your hearing?’ suggested hearing difficulties among 21.5% of the non-participants and among 37.1% of the participants. A full description of the sampling is reported in our previous article (Hannula et al, 2010).

Data collection All the subjects underwent an otological examination, including pneumatic otoscopy, made by an ear, nose and throat specialist (SH or EM-T), and they completed an extensive questionnaire. Possible risk factors for HI were screened by questions about CVD, DM, smoking, alcohol use, and body weight and height. Occupational information and the profession of the study subjects were asked, to define the socioeconomic class (SEC). The whole questionnaire was checked during the interview with the study physician (SH or EM-T) to correct all possible misinterpretations of the questions. Written informed consent was obtained from all the subjects and the study was approved by the Finnish National Advisory Board on Health Care Ethics. The subjects did not receive any financial compensation for their participation. Detailed information about the subjects, methods, and data collection has been reported previously (Hannula et al, 2010).

CARDIOVASCULAR DISEASES

AND MEDICAL HISTORY

The presence of CVD, asked in the questionnaire and the self-report, was confirmed in the structured interview. The principal questions to screen CVD were: Have you ever had a heart attack? Have you ever had heart surgery? Have you ever had coronary artery catheterization? Do you suffer from intermittent claudication? Do you have other problems with your heart or circulation? Do you have other severe health problems that are not asked? Some questions were further particularized in secondary questions concerning the type and time of disease event or operation. In addition, the history of HT, hypercholesterolemia, and DM were screened in the questionnaire by self-report or the use of related medication, and confirmed in the interview. If a subject had DM, the need for insulin was verified. The study subjects were asked to report their body height and weight. Body mass index (BMI) ⱖ 30 kg/m2 was applied as a definition for obesity, as the Expert Panel on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults has stated (1998). Data concerning body weight was missing from three subjects. In analysis we applied a variable of total CVD defined as a history of any, one or more, of the following: ischemic heart disease, heart attack, atrial fibrillation, valve problem, heart insufficiency, intermittent claudication, or history of stroke. HT, hypercholesterolemia, DM, smoking, and obesity were considered as cardiovascular risk factors (Mancia et al, 2007).

SMOKING The questions concerning tobacco smoking were: Have you ever smoked regularly? If the subjects answered yes, they were asked to respond also to following questions: For how many years did you (have you) smoke(d) up to now? Approximately how many cigarettes do (did) you smoke on average? (1) Less than 5 each day, (2) 5–10

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each day, (3) 10–20 each day, (4) more than 20 each day? Approximately how many cigars or cigarellos do (did) you smoke on average each day? Approximately how much pipe tobacco (grams) do (did) you smoke each day? For data analyses, smokers were divided into three classes according to the amount of cigarettes smoked a day and a weighting factor was given accordingly: (1) less than 10 cigarettes a day (weighting factor ⫽ 0.5), (2) 10–20 cigarettes a day (weighting factor ⫽ 1), and (3) more than 20 cigarettes a day (weighting factor ⫽ 1.5). To estimate the pack-years of smoking, we multiplied the time (in years) a subject had been smoking by the weighting factor, as in the study of Fransen et al (2008). We used three categories for pack-years in the analyses: zero for non-smokers, 1–19, and ⱖ 20. Pack years could not be calculated for 16 subjects as data concerning smoking years was missing from three subjects and daily amount of cigarettes was missing from 13 subjects, including seven subjects who consumed only cigars/cigarellos or pipe tobacco. Moreover, for 21 (2.4%) subjects who reported smoking pipe and/or cigars in addition to cigarettes the classification was based only on the amount of smoked cigarettes. Fifteen of them were included in the heavy smokers group anyway (ⱖ 20 pack-years). Thus, for six subjects, the pack-years might be underestimated.

SOCIOECONOMIC CLASS SEC was defined according to the classification of socio-economic groups (Statistics Finland, 1989); (1) Self-employed persons, (2) Upper-level employees with administrative, managerial, professional, and related occupations, (3) Lower-level employees with administrative and clerical occupations, (4) Manual workers, (5) Students, (6) Pensioners, and (7) Others. The occupational information and reported profession of the subject were used to define SEC. However, if the subject was a pensioner, his or her earlier occupation was used to define the status. This decision was made because the age distribution of the subjects in the current study caused a potential risk for over-representation of pensioners. There were no students in the study population. The data needed to conclude the socioeconomic status was missing for eight subjects. In the analyses, socioeconomic class 2. (upper-level employees) was used as a referent group, because group 1 includes a wide variety of occupations, including farmers and manual workers, and group 2 (upper-level employees) represent a higher social class with more education and thus they presumably have the smallest risk for HI.

ALCOHOL

USE, NOISE EXPOSURE, AND OTOLOGICAL RISK FACTORS

The study subjects were asked for their alcohol-use habits with the following questions: Do you drink alcohol regularly (every week)? In addition subjects were asked to report the amount of consumed alcohol: One bottle of beer, 12 cl wine, or 4 cl of spirit was counted as one drink. Structured answers were (1) less than 1 drink each week, (2) 1–5 drinks each week, (3) 1–3 drinks each day or (4) more than 3 drinks each day. In the analyses, we used a dichotomized variable: those who did not consume alcohol at all or used irregularly and those who consumed alcohol regularly every week. The exposure to noise was screened in the questionnaire, including questions on occupational, leisure time, and firearm noise exposure. The question concerning occupational noise exposure was: Have you ever worked more than one year in a place where you had to raise your voice to make yourself heard by someone standing one metre away from you? ; and leisure time noise exposure: During your leisure time, are you/have you been regularly (more than once a week) exposed to intense sounds or noises (so that you have to shout to make yourself heard by someone who stands more

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than one metre away from you)? A subject was considered noiseexposed, if the subject had history of any of the following: working more than one year in a noisy environment; regular (more than once a week) leisure time noise exposure; or gunfire noise (more than 100 rounds with a light weapon and/or more than 10 rounds with a heavy weapon). Questions screening following otological diseases and risk factors were included: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital and hereditary HI, ear trauma, severe head trauma, ototoxic medication, or radiation therapy in the area of the head. For analyses, these risk factors were subdivided to (1) direct otological risk factors that have clear deteriorating effect on hearing: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital and hereditary HI, and ear trauma; and (2) to indirect otological risk factors: severe head trauma, ototoxic medication, and radiation therapy in the area of head. Subjects with direct otological risk factors were excluded from the multivariable analysis. The more specific definition of noise exposure, as well as otological risk factors, has been described previously (Hannula et al, 2012).

(ⱕ 60 vs. ⬎ 60 years), BMI (⬍ 30 vs. ⱖ 30 kg/m²), alcohol usage (regular weekly usage vs. less frequently), and HT as confounding factors. The continuous variables were classified if they acted nonlinearly. Secondly, sex and otological risk factors (separately direct and indirect otological risk factors) were added to the propensity score adjusted model to increase the precision and to see possible differences between males and females. The propensity score was classified to quintiles due to its non-linear nature. Odds ratios (OR) with 95% confidence intervals (95% CI) are presented for logistic regression models. Interaction terms in all models were calculated and found non-significant. All analyses were performed using SPSS for Windows (IBM Corp., released 2011, SPSS Statistics for Windows, Version 20.0. Armonk, USA). Two-tailed p-values are reported.

Results Of 850 study subjects, 383 (45.1%) were men and 467 (54.9%) women. The mean age of the study subjects was 60.9 years (SD 3.9). The frequencies of CVD, cardiovascular risk factors, and other factors with or without HI are presented in Tables 1 and 2.

AUDIOLOGICAL MEASUREMENTS Pure-tone air conduction thresholds (0.125, 0.25, 0.5, 1, 2, 3, 4, 6, 8 kHz) and bone conduction thresholds (0.25, 0.5, 1, 2, 4 kHz) were measured in a sound-insulated booth by a trained audiology assistant. Madsen Midimate 602 (Otometrics, Denmark) and Madsen Orbiter 922 (Otometrics, Denmark) clinical audiometers were used, and calibrated according to ISO 389-1 (1998) and ISO 389-3 (1994). Supra-aural TDH-39 earphones with MX-41/AR cushions and Radioear B-71 bone vibrators were used with both audiometers. Puretone averages (PTA) were calculated for better and worse ears (better ear hearing level, BEHL; and worse ear hearing level, WEHL) in two frequency ranges: low frequencies including 0.125, 0.25, 0.5, and 1 kHz, and middle frequencies including 0.5, 1, 2, and 4 kHz. As a definition for HI, PTA ⱖ 20 dB HL was used (Pascolini & Smith, 2009). The analyses in the present study are based on air-conduction thresholds, because the prevalence of conductive or mixed HI among all the subjects was low, 2.6%, as reported previously (Hannula et al, 2010). If an air-conduction pure-tone threshold exceeded the maximum output of the audiometer, the value of 130 dB was used in the data entry, according to the recommendation of the British Society of Audiology (1988).

Statistical methods Summary statistics are presented as mean and standard deviation (SD) unless other stated. A multivariable logistic regression model was built to detect risk factors for HI (BEHL ⱖ 20, and WEHL ⱖ 20) separately for males and females. Potential risk factors with p-value ⬍ 0.3 in a univariate model were entered one-by-one into the model and were left in the model if the adjusted p-value was ⬍ 0.05, or the variable decreased the ⫺ 2log likelihood function significantly. Also the Hosmer-Lemeshow p-values were calculated to check the goodness-of-fit of each model. A propensity score adjusted logistic regression model was built to evaluate the impact of CVD on HI (for both BEHL ⱖ 20 and WEHL ⱖ 20, separately for low and middle frequencies). First the propensity score was calculated by creating a logistic regression model for CVD with socioeconomic class, smoking (none, 1–19, and ⱖ 20 pack-years), diabetes, hypercholesterolemia, age

Cardiovascular diseases One hundred twenty-five (14.7% of the study population) reported at least one cardiovascular disease. Ischemic heart disease and history of heart attack were more prevalent in HI group, but the differences were not significant. Twenty-three subjects (2.7%) reported previous stroke. Other CVDs were rare in this population.

CARDIOVASCULAR RISK FACTORS HT was the most frequently reported cardiovascular risk factor. There were no differences in the frequencies of HT between HI and no-HI groups. History of DM was also slightly, but not significantly, more common among subjects with HI. Hypercholesterolemia was common condition in this population (20.0%) and there were no significant differences between HI and no HI groups.

Body height and weight Among men (n ⫽ 383), the mean body height was 174.9 cm (SD 6.0) and the mean body weight was 82.4 kg (SD 13.0). Among women (n ⫽ 464) the corresponding figures were 160.9 cm (SD 5.2) and 70.6 kg (SD 12.4). The mean body mass index (BMI) among study subjects was 27.1 kg/m2 (SD 4.3) and 22.7% of subjects had BMI more than 30 kg/m2. High BMI was more common among men with HI (p ⫽ 0.012 for BEHL0.5,1,2,4kHz ⱖ 20 dB and 0.048 for WEHL0.5,1,2,4kHz ⱖ 20 dB).

Smoking and alcohol use The majority of men (53.5%) but only 23.3% of women reported to be current or previous smokers (p ⬍ 0.001). Mean pack-years smoked were 9.0 (SD 15.4). Smoking was more common among subjects with HI (Table 1). One third (32.2%) of subjects reported regular alcohol use (every week), and most of them (85.5%) consumed no more than five drinks a week. Only 12 subjects (3.0% of the study population) consumed more than three drinks a day. There was no difference in alcohol consumption between HI and no HI groups not even for heavy users (more than five drinks a week, data not shown).

Cardiovascular diseases and HI among adults

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Table 1. Frequencies of reported cardiovascular diseases (CVD) and other factors for study subjects (n ⫽ 850) with or without hearing impairment (HI), with p-values for differences between HI and no HI groups. HI defined as pure-tone average of ⱖ 20 dB at the frequencies of 0.5, 1, 2, and 4 kHz in the better ear (BEHL0.5,1,2,4kHz ⱖ 20 dB). Men (n ⫽ 383)

Disease or risk factor Cardiovascular disease Total CVDa Ischemic heart disease Heart attack Atrial fibrillation Valve problem Heart insufficiency Claudication Stroke CVD risk factors Diabetes Hypertension Hypercholesterolemia Body mass index ⱖ 30 kg/m2 Smoking (pack-years)b 0 1–19 ⱖ 20 Alcohol use (every week) Socioeconomic classc Upper-level employees Self-employed persons Lower-level employees Manual workers Otological risk factorsd Direct Indirect Noise exposuree Age 54–60 years 61–66 years

HI (n ⫽ 141)

no HI (n ⫽ 242)

n (%)

n (%)

37 (26.2) 23 (16.3) 16 (11.3) 3 (2.1) 1 (0.4) 2 (1.4) 2 (1.4) 11 (7.8) 15 (10.6) 47 (33.3) 29 (20.6) 37 (26.2) 56 24 59 63

(40.3) (17.3) (41.8) (44.7)

19 9 36 76

(13.5) (6.4) (25.5) (53.9)

Women (n ⫽ 467) HI (n ⫽ 86)

no HI (n ⫽ 381)

p

n

n (%)

p

46 (19.1) 33 (13.6) 21 (8.7) 8 (3.3) 1 (0.7) 2 (0.8) 7 (2.9) 5 (2.1)

0.10 0.48 0.40 0.75 ⬎ 0.9 0.63 0.50 0.007

10 (11.6) 7 (8.1) 4 (4.7) 0 (0) 1 (1.2) 0 (0) 0 (0) 2 (2.3)

32 (8.4) 24 (6.3) 9 (2.4) 3 (0.8) 4 (1.0) 0 (0) 2 (0.5) 5 (1.3)

0.35 0.54 0.27 ⬎ 0.9 ⬎ 0.9

21 (8.7) 79 (32.6) 39 (16.1) 38 (15.7)

0.53 0.89 0.27 0.012 0.035

10 (11.6) 30 (34.9) 15 (17.4) 24 (27.9)

31 (8.1) 132 (34.6) 87 (22.8) 94 (24.7)

66 (77.6) 8 (9.4) 11 (12.9) 16 (18.6)

292 (77.7) 50 (13.3) 34 (9.0) 78 (20.5)

7 (8.1) 4 (4.7) 42 (48.8) 31 (36.0)

45 (11.8) 19 (5.0) 206 (54.1) 106 (27.8)

22 (25.6) 6 (9.4) 18 (20.9)

20 (5.2) 36 (7.0) 52 (13.6)

27 (31.4) 59 (68.6)

174 (45.7) 207 (54.3)

123 (52.6) 41 (17.5) 70 (29.9) 117 (48.3) 67 19 64 92

0.49 0.002

(27.7) (7.9) (26.4) (38.0)

16 (11.3) 22 (15.6) 122 (86.5)

15 (6.2) 24 (9.9) 198 (81.8)

46 (32.6) 95 (67.4)

106 (43.8) 136 (56.2)

0.075 0.099 0.23 0.031

⬎ 0.9 0.62 0.30 ⬎ 0.9 0.27 0.53 0.38

0.70 0.46

⬍ 0.001 0.47 0.088 0.016

aA

study subject has one or more cardiovascular disease. bData was missing for 16 smokers for calculating pack-years. according to Statistics Finland, 1989. Eight subjects were missing data to conclude their socioeconomic class. dA study subject has history of one or more of the following: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital and hereditary HI or ear trauma (direct otological risk factors) or severe head trauma, ototoxic medication or radiation therapy in the area of the head (indirect otological risk factors). eIncluding subjects exposed to occupational noise, leisure time noise or gunfire noise. d,ePreviously reported data (Hannula et al 2012). cClassification

Socioeconomic status Most of the subjects were lower-level employees or manual workers (76.8%). Among men with HI, more than half were manual workers. Among women, socioeconomic class distributions were not different between HI and no-HI groups.

p ⫽ 0.35) and the corresponding figure for WEHL0.5,1,2,4kHz ⱖ 20 dB was 1.48 (95% CI 0.96 to 2.28, p ⫽ 0.79). In analyses for lower frequency range, results were: OR for BEHL0.125,0.25,0.5,1kHz ⱖ 20 dB 0.88 (95% CI 0.36 to 2.16, p ⫽ 0.78) and for WEHL0.125,0.25,0.5,1kHz ⱖ 20 dB 1.67 (95% CI 0.58 to 1.97, p ⫽ 0.84).

Propensity score adjusted model for the impact of cardiovascular diseases

The evaluation of other risk factors

In the propensity score adjusted multivariate regression model for impact of CVD, no significant association with HI and the total CVD (a study subject has history of one or more CVD) was found. Odds ratio for BEHL0.5,1,2,4kHz ⱖ 20 dB was 1.24 (95% CI 0.79 to 1.96,

In a multivariate logistic regression model, heavy smoking was associated with HI defined by worse ear (WEHL0.5,1,2,4kHz ⱖ 20 dB) among both genders, and among men, also with better-ear defined HI (BEHL0.5,1,2,4kHz ⱖ 20 dB). In addition, lower socioeconomic

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V. Lohi et al. Table 2. Frequencies of reported cardiovascular diseases and other factors for study subjects (n ⫽ 850) with or without hearing impairment (HI), with p-values for differences between HI and no HI groups. HI defined as pure-tone average of ⱖ 20 dB at the frequencies of 0.5, 1, 2, and 4 kHz in the worse ear (WEHL0.5,1,2,4kHz ⱖ 20 dB). Men (n ⫽ 383)

Disease or risk factor Cardiovascular disease Total CVDa Ischemic heart disease Heart attack Atrial fibrillation Valve problem Heart insufficiency Claudication Stroke CVD risk factors Diabetes Hypertension Hypercholesterolemia Body mass index ⱖ 30 kg/m2 Smoking (pack-years)b 0 1–19 ⱖ 20 Alcohol use (every week) Socioeconomic classc Upper-level employees Self-employed persons Lower-level employees Manual workers Otological risk factorsd Direct Indirect Noise exposuree Age 54–60 years 61–66 years

HI (n ⫽ 206)

no HI (n ⫽ 177)

n (%)

n (%)

51 (24.8) 33 (16.0) 23 (11.2) 4 (1.9) 2 (1.0) 2 (1.1) 3 (1.5) 12 (5.8)

Women (n ⫽ 467) HI (n ⫽ 153)

no HI (n ⫽ 314)

p

n

n (%)

p

32 (18.2) 23 (13.0) 14 (17.9) 7 (4.0) 0 (0) 2 (1.0) 6 (3.4) 4 (2.3)

0.12 0.40 0.29 0.24 0.5 ⬎ 0.9 0.50 0.082

19 (12.4) 13 (8.5) 6 (3.9) 0 (0) 2 (1.3) 0 (0) 1 (0.7) 4 (2.6)

23 (7.3) 18 (5.7) 7 (2.2) 3 (1.0) 3 (1.0) 0 (0) 1 (0.3) 3 (1.0)

0.07 0.26 0.34 0.55 0.66

21 (10.2) 69 (33.5) 40 (19.4) 48 (23.3)

15 (8.5) 57 (32.2) 28 (15.8) 27 (15.3)

0.57 0.79 0.36 0.048 0.016

15 (9.8) 51 (33.3) 27 (17.6) 35 (22.9)

26 (8.3) 111 (35.4) 75 (23.9) 83 (26.4)

0.59 0.67 0.13 0.41 0.19

86 31 82 90

(43.2) (15.6) (41.2) (43.7)

93 34 47 90

(53.4) (19.5) (27.0) (50.8)

34 14 51 106

(16.5) (6.8) (24.8) (51.5)

52 14 49 62

(29.4) (7.9) (27.7) (35.0)

23 (11.2) 30 (14.6) 173 (84.0)

8 (4.5) 16 (9.0) 147 (83.1)

75 (36.4) 131 (63.6)

77 (43.5) 100 (56.5)

0.16 0.004

0.017 0.097 0.81 0.16

111 19 20 26

(74.0) (12.7) (13.3) (17.0)

247 39 25 68

(79.4) (12.5) (8.0) (21.7)

16 8 74 52

(10.5) (5.2) (48.4) (34.0)

36 15 174 85

(11.5) (4.8) (55.4) (27.1)

36 (23.5) 13 (8.5) 28 (18.3)

6 (1.9) 29 (9.2) 42 (13.4)

47 (30.7) 106 (69.3)

154 (49.0) 160 (51.0)

0.55 0.22

0.24 0.51

⬍ 0.001 0.79 0.16 ⬍ 0.001

aA

study subject has one or more cardiovascular disease. bData was missing for 16 smokers for calculating pack-years. according to Statistics Finland, 1989. Eight subjects were missing data to conclude their socioeconomic class. dA study subject has history of one or more of the following: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital and hereditary HI or ear trauma (direct otological risk factors) or severe head trauma, ototoxic medication or radiation therapy in the area of the head (indirect otological risk factors). eIncluding subjects exposed to occupational noise, leisure time noise or gunfire noise. d,ePreviously reported data (Hannula et al, 2012). cClassification

class (manual workers) and obesity were associated with HI, either defined by better or worse ear (BEHL0.5,1,2,4kHz ⱖ 20 dB, WEHL0.5,1,2,4kHz ⱖ 20 dB), but only among men. Lower socioeconomic class and HI (BEHL) were also associated among women, but this result was not significant. None of the CVD variables were associated with HI. No significant interactions were found between the variables in any of the models. Unadjusted and adjusted odds ratios for the association between HI and significant risk factors are presented in Table 3 and Table 4.

Discussion In our sample, CVDs were not associated with HI, not even at the low frequency range. Similar results with ours are reported in another

population-based study with 2049 participants where no association between CVD and HI was found (Helzner et al, 2011). In their population, clinical CVD was highly more prevalent than in our study, and in an older population (mean age 73 years), so some survival bias may occur. Also in the Beaver Dam Offspring study (n ⫽ 3285), history of clinical CVD was not associated with HI, with younger population (mean age 49 years) and small prevalence (3.4%) of clinical CVD (Nash et al, 2011). In the Framingham study, with 1662 elderly subjects (mean age 73 years), in which association was found between CVD and HI, 40 dB HL or greater was used as the definition for HI for analyses separately in low (0.25, 0.5, and 1 kHz) and high (4, 6, and 8 kHz) frequencies for both better and worse ear (Gates et al, 1993). In addition to the Framingham cohort, Friedland et al (2009) found an association between low-frequency

Cardiovascular diseases and HI among adults Table 3. Multivariate logistic regression model for hearing impairment defined as pure-tone average of ⱖ 20 dB at the frequencies of 0.5, 1, 2, and 4 kHz in the better ear (better ear hearing level, BEHL) separately for men (n ⫽ 352) and women (n ⫽ 425). Values are presented as adjusted and unadjusted odds ratios (OR) with 95% confidence interval (95% CI). Gender Men

Women

Risk factor Age 54–60 years 61–66 years Body mass index ⱖ 30 kg/m2 Socioeconomic classa Upper-level employees Self-employed persons Lower-level employees Manual workers Smoking (pack-years) 0 1–19 ⱖ 20 Age 54–60 years 61–66 years Socioeconomic classa Upper-level employees Self-employed persons Lower-level employees Manual workers

Adjusted OR

95% CI

p-value

Unadjusted OR

95% CI

1.0 1.72 1.85

1.05 to 2.80 1.05 to 3.25

0.03 0.033

1.0 1.56 1.86

0.99 to 2.45 1.10 to 3.14

1.0 1.42 1.98 2.79

0.51 to 3.96 0.97 to 4.07 1.45 to 5.39

0.50 0.062 0.002

1.0 1.62 2.01 2.77

0.60 to 4.37 1.01 to 3.98 1.48 to 5.17

1.0 1.23 1.96

0.63 to 2.41 1.17 to 3.26

0.55 0.01

1.0 1.27 2.31

0.67 to 2.43 1.41 to 3.77

1.0 2.01

1.13 to 3.59

0.018

1.0 2.09

1.17 to 3.70

1.0 2.94 2.29 3.06

0.59 to 14.64 0.67 to 7.84 0.87 to 10.82

0.19 0.19 0.082

1.0 3.11 2.35 3.25

0.63 to 15.34 0.69 to 8.01 0.93 to 11.42

Subjects with history of one or more of the following: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital or hereditary HI were excluded from the analysis. Male model: ⫺ 2log likelihood ⫽ 413.9, P (Hosmer-Lemeshow) ⫽ 0.50. Female model: ⫺ 2log likelihood ⫽ 344.3, P (HosmerLemeshow) ⫽ 0.91. aClassification according to Statistics Finland. Significant values shown with bold text.

Table 4. Multivariate logistic regression model for hearing impairment defined as pure-tone average of ⱖ 20 dB at the frequencies of 0.5, 1, 2, and 4 kHz in the worse ear (worse ear hearing level, WEHL) separately for men (n ⫽ 352) and women (n ⫽ 425). Values are presented as adjusted and unadjusted odds ratios (OR) with 95% confidence intervals (95% CI). Gender Men

Women

Risk factor Pack-years of smoking 0 1–19 ⱖ 20 Body mass index ⱖ 30 kg/m2 Socioeconomic classa Upper-level employees Self-employed persons Lower-level employees Manual workers Age 54–60 years 61–66 years Pack-years of smoking 0 1 ⫺ 19 ⱖ 20

Adjusted OR

95% CI

1.0 0.84 1.88 1.71

0.45 to 1.57 1.14 to 3.08 0.97 to 3.01

1.0 1.27 1.43 2.28

p-value

Unadjusted OR

95% CI

0.58 0.013 0.062

1.0 0.88 2.13 1.72

0.48 to 1.61 1.01 to 2.92 1.01 to 2.92

0.51 to 3.18 0.76 to 2.70 1.28 to 4.07

0.61 0.27 0.005

1.0 1.40 1.67 2.53

0.57 to 3.43 0.91 to 3.07 1.45 to 4.43

1.0 2.29

1.44 to 3.65

⬍ 0.001

1.0 2.19

1.40 to 3.44

1.0 1.41 2.40

0.72 to 2.74 1.22 to 4.71

0.32 0.011

1.0 1.23 2.27

0.64 to 2.35 1.17 to 4.39

Subjects with history of one or more of the following: chronic ear infection, otosclerosis, Ménière’s disease, sudden sensorineural HI, Herpes zoster oticus, congenital or hereditary HI were excluded from the analysis. Male model: ⫺ 2log likelihood ⫽ 479.1, P (Hosmer-Lemeshow) ⫽ 0.60. Female model: ⫺ 2log likelihood ⫽ 537.7, P (HosmerLemeshow) ⬎ 0.9. aClassification according to Statistics Finland. Significant values shown with bold text.

271

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V. Lohi et al.

HI and CVD in a cohort of 1168 audiological patients, when the associations between audiogram pattern and cardiovascular variables were analysed. It is difficult to compare the results of previous studies on association between CVD and HI, and the results are often inconsistent. The difficulties in making comparisons result mainly from varying criteria used to define HI and CVD. Differences in the sampling of the subjects and age distribution are other possible causes of the divergent results. In the study of Friedland et al (2009) the subjects had been referred to an audiological clinic, so most of them had already difficulties with hearing thus the sample was not populationbased. Furthermore, the subjects were slightly older (mean age 67.5 years) and their cardiovascular morbidity was higher than in our study population. Thus the results are rather poorly comparable to our unscreened population. However, when hearing impairment was defined as WEHL0.5,1,2,4kHz ⱖ 20 dB, a weak association for the impact of CVD was found (OR 1.48, 95% CI 0.96 to 2.28, p ⫽ 0.079). Furthermore, as seen in Tables 1 and 2, HI is more common among subjects with heart attack and ischemic heart disease, but the differences between groups were not significant. Hereby, it has to be taken into account that the numbers of each subgroup are rather small. Thus these findings might have been clearer in a larger study population with higher statistical power. These results also indicate that there might be other confounding factors that are not recognized. One possible explanation for the different results between studies could be that in the age group of our study population, clinical CVD events, such as heart attack, are still rare (Go et al, 2014). It is possible that risk factors are controlled by medication, and there might be subjects with unknown risk factors or undiagnosed CVD in the study population. On the other hand, considering the nonspecific entity of CVD, it may not be a part of CVD-hearing pathway as such. If we assume that the discovered cardiovascular risk factors lead to HI, we might have exposures or protective factors we do not recognize and are missing from the analyses. Among men, obesity was a risk factor for HI defined by BEHL and the same trend, though not significant, was detected for WEHL. In a previous study, high BMI was associated to HI among women, but not among men (Helzner et al, 2011). No association between HT and HI was found in the present study. This may be due to the fact that, in this age group in Finland, HT is actively screened in occupational health care and treated with medication. Thus, the actual BP levels among the subjects with proper medication might have been low enough not to lead to HI. The previous studies indicating association between HT and HI are not comparable because the definition of HT varies. Previously, subjects with DM have been shown to have poorer hearing when compared to subjects without DM (Tay et al, 1995). In a US population-based study, history of DM increased the risk for HI (OR 2.0, 95% CI 1.2 to 3.2) (Agrawal et al, 2009). In a Finnish population-based study concerning DM (Saaristo et al, 2008), obesity was more common (25.2% among men and 29.0% among women) than in the present study (Table 1). In the same study, prevalence of DM (16.9% among men and 11.5% among women) was higher than in the present study, and possible subjects with undiagnosed DM in the present study population could have biased our results. We found that heavy smoking increases risk for HI (WEHL0,5,1,2,4kHz ⱖ 20 dB) in both genders after multivariate adjustment. These results are in keeping with previous studies (Itoh et al, 2001; Fransen et al, 2008; Agrawal et al, 2009). In the Epidemiology of Hearing Loss study, current smokers had

increased risk of having HI (OR 1.69, 95% CI 1.31 to 2.17), and also passive smoking increased risk of having HI (Cruickshanks et al, 1998). Alcohol consumption was not a risk factor for HI. It must be emphasized that the amount of alcohol used, as well as the amount of smoking, were self-reported and possible cause for bias in this study, as the consumed amount of alcohol and tobacco might be underestimated. Lower SEC was associated with HI among men in the multivariate analysis. The same trend was detected among women for BEHL0.5,1,2,4kHz of having ⱖ 20 dB, though not significant. Socioeconomic factors are associated with health behavior and low SEC increases cardiovascular morbidity (Mackenbach et al, 2003; Power et al, 2007). Furthermore, occupational noise exposure is more common among less educated public (Gan et al, 2011). In our study, however, otological risk factors and noise exposure, as well as many other possible risk factors have been taken into account and still low SEC seems to be a risk factor for HI. This result indicates that HI and SEC are not associated via CVD and the cause for this needs further research. There might be some confounding by exposure to noise, as the duration and intensity of harmful noise is somewhat difficult to estimate. Methodologically, this was a population-based study in an unscreened population. Thus the results can be generalized to population-level, although our population represents geographically the northern part of Finland. Another strength of the current study is the fact that otological status of the subjects was investigated by specialists. In addition, clinical pure-tone audiometry was performed by trained audiologists, which increases the quality of the audiological data. However, these are cross-sectional findings and longitudinal studies are needed to investigate the cause-and-effect relationship. There are also some limitations in this study: Relatively small numbers of subjects remain in each subgroup in multivariate analysis which reduces the statistical power of the study. This could explain the fact that CVD variable did not end up in the multivariable model (Tables 3 and 4). Additionally, medical conditions, such as HT, DM, and hypercholesterolemia were reported in the questionnaire and not diagnosed by clinical measurements. However, medical records were checked when needed and the questionnaire was checked in a structured interview to increase the reliability of collected data. When analysing the non-responders, self-reported hearing problems were more common among participants (37.1%) than non-participants (21.5%). Thus there is the some possibility of over-sampling subjects with HI.

Conclusion In this population-based study, no significant association between CVD and HI was found. Lower socioeconomic class was associated with HI among men. Smoking and obesity might be preventable risk factors for HI.

Acknowledgements This study was supported by VTR funding of Oulu University Hospital and the European ARHI Project (QLRT-2001-00331). The authors would like to express their gratitude to the ARHI partners. We would also like to thank the staff of the Hearing Centre of the Oulu University Hospital and other staff who helped us to conduct the project. Declaration of interest: The authors report no conflicts of interest.

Cardiovascular diseases and HI among adults

References Agrawal Y., Platz E.A. & Niparko J.K. 2009. Risk factors for hearing loss in US adults: Data from the National Health and Nutrition Examination Survey, 1999 to 2002. Otol Neurotol, 30, 139–145. Agrawal Y., Platz E.A. & Niparko J.K. 2008. 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, 168, 1522–1530. Anonymous: Executive Summary of the Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults. 1998. Arch Intern Med, 158, 1855–1867. Brant L.J., Gordon-Salant S., Pearson J.D., Klein L.L., Morrell C.H. et al. 1996. Risk factors related to age-associated hearing loss in the speech frequencies. J Am Acad Audiol, 7, 152–160. British Society of Audiology. 1988. British Society of Audiology recommendation. Descriptors for pure-tone audiograms. Br J Audiol, 22, 123. Cruickshanks K.J., Klein R., Klein B.E., Wiley T.L., Nondahl D.M. et al. 1998. Cigarette smoking and hearing loss: The epidemiology of hearing loss study. JAMA, 279, 1715–1719. Cruickshanks K.J., Nondahl D.M., Tweed T.S., Wiley T.L., Klein B.E. et al. 2010. Education, occupation, noise exposure history and the 10-year cumulative incidence of hearing impairment in older adults. Hear Res, 264, 3–9. Dalton D.S., Cruickshanks K.J., Klein R., Klein B.E. & Wiley T.L. 1998. Association of NIDDM and hearing loss. Diabetes Care, 21, 1540–1544. Drettner B., Hedstrand H., Klockhoff I. & Svedberg A. 1975. Cardiovascular risk factors and hearing loss. A study of 1000 fifty-year-old men. Acta Otolaryngol (Stockh), 79, 366–371. Fransen E., Topsakal V., Hendrickx J.J., Van Laer L., Huyghe J.R. et al. 2008. Occupational noise, smoking, and a high body mass index are risk factors for age-related hearing impairment and moderate alcohol consumption is protective: A European population-based multicenter study. J Assoc Res Otolaryngol, 9, 264–276. Friedland D.R., Cederberg C. & Tarima S. 2009. Audiometric pattern as a predictor of cardiovascular status: Development of a model for assessment of risk. Laryngoscope, 119, 473–486. Gan W.Q., Davies H.W. & Demers P.A. 2011. Exposure to occupational noise and cardiovascular disease in the United States: The National Health and Nutrition Examination Survey 1999–2004. Occup Environ Med, 68, 183–190. Gates G.A., Cobb J.L., D Agostino R.B. & Wolf P.A. 1993. The relation of hearing in the elderly to the presence of cardiovascular disease and cardiovascular risk factors. Arch Otolaryngol Head Neck Surg, 119, 156–161. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D. et al. 2014. Heart disease and stroke statistics, 2014 update: A report from the American Heart Association. Circulation, 129, e28–e292. Gopinath B., Schneider J., Hickson L., McMahon C.M., Burlutsky G. et al. 2012. Hearing handicap, rather than measured hearing impairment, predicts poorer quality of life over 10 years in older adults. Maturitas, 72, 146–151. Gopinath B., Schneider J., Rochtchina E., Leeder S.R. & Mitchell P. 2009. Association between age-related hearing loss and stroke in an older population. Stroke, 40, 1496–1498. Hannula S., Bloigu R., Majamaa K., Sorri M. & Maki-Torkko E. 2012. Ear diseases and other risk factors for hearing impairment among adults: An epidemiological study. Int J Audiol, 51, 833–840. Hannula S., Mäki-Torkko E., Majamaa K. & Sorri M. 2010. Hearing in a 54- to 66-year-old population in northern Finland. Int J Audiol, 49, 920–927. Helzner E.P., Patel A.S., Pratt S., Sutton-Tyrrell K., Cauley J.A. et al. 2011. Hearing sensitivity in older adults: Associations with cardiovascular risk

273

factors in the health, aging and body composition study. J Am Geriatr Soc, 59, 972–979. Itoh A., Nakashima T., Arao H., Wakai K., Tamakoshi A. et al. 2001. Smoking and drinking habits as risk factors for hearing loss in the elderly: Epidemiological study of subjects undergoing routine health checks in Aichi, Japan. Public Health, 115, 192–196. Lin H.C., Chao P.Z. & Lee H.C. 2008. Sudden sensorineural hearing loss increases the risk of stroke: A 5-year follow-up study. Stroke, 39, 2744–2748. Mackenbach J.P., Bos V., Andersen O., Cardano M., Costa G. et al. 2003. Widening socioeconomic inequalities in mortality in six Western European countries. Int J Epidemiol, 32, 830–837. Mancia G., De Backer G., Dominiczak A., Cifkova R., Fagard R. et al. 2007. 2007 guidelines for the management of arterial hypertension: The Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur Heart J, 28, 1462–1536. Nachtegaal J., Smit J.H., Smits C., Bezemer P.D., van Beek J.H. et al. 2009. The association between hearing status and psychosocial health before the age of 70 years: Results from an internet-based national survey on hearing. Ear Hear, 30, 302–312. Nash S.D., Cruickshanks K.J., Klein R., Klein B.E., Nieto F.J. et al. 2011. The prevalence of hearing impairment and associated risk factors: The Beaver Dam Offspring Study. Arch Otolaryngol Head Neck Surg, 137, 432–439. Noorhassim I. & Rampal K.G. 1998. Multiplicative effect of smoking and age on hearing impairment. Am J Otolaryngol, 19, 240–243. Pascolini D. & Smith A. 2009. Hearing impairment in 2008: A compilation of available epidemiological studies. Int J Audiol, 48, 473–485. Power C., Atherton K., Strachan D.P., Shepherd P., Fuller E. et al. 2007. Life-course influences on health in British adults: Effects of socioeconomic position in childhood and adulthood. Int J Epidemiol, 36, 532–539. Pyykkö I., Koskimies K., Starck J., Pekkarinen J. & Inaba R. 1988. Evaluation of factors affecting sensory neural hearing loss. Acta Otolaryngol Suppl (Stockh), 449, 155–158. Rosen S., Bergman M., Plester D., El-Mofty A. & Satti M.H. 1962. Presbycusis study of a relatively noise-free population in the Sudan. Ann Otol Rhinol Laryngol, 71, 727–743. Rosen S., Plester D., El-Mofty A. & Rosen H.V. 1964. Relation of hearing loss to cardiovascular disease. Trans Am Acad Ophthalmol Otolaryngol, 68, 433–444. Rosenhall U. & Pedersen K.E. 1995. Presbycusis and occupational hearing loss. Occup Med, 10, 593–607. Rosenhall U., Sixt E., Sundh V. & Svanborg A. 1993. Correlations between presbycusis and extrinsic noxious factors. Audiology, 32, 234–243. Rosenhall U. & Sundh V. 2006. Age-related hearing loss and blood pressure. Noise Health, 8, 88–94. Rudin R., Rosenhall U. & Svardsudd K. 1988. Hearing capacity in samples of men from the general population. The study of men born in 1913 and 1923. Scand Audiol, 17, 3–10. Saaristo T.E., Barengo N.C., Korpi-Hyovalti E., Oksa H., Puolijoki H. et al. 2008. High prevalence of obesity, central obesity and abnormal glucose tolerance in the middle-aged Finnish population. BMC Public Health, 8, 423. Schuknecht H.F. & Gacek M.R. 1993. Cochlear pathology in presbycusis. Ann Otol Rhinol Laryngol, 102, 1–16. Tay H.L., Ray N., Ohri R. & Frootko N.J. 1995. Diabetes mellitus and hearing loss. Clin Otolaryngol Allied Sci, 20, 130–134. Torre P. 3rd, Cruickshanks K.J., Klein B.E., Klein R. & Nondahl D.M. 2005. The association between cardiovascular disease and cochlear function in older adults. J Speech Lang Hear Res, 48, 473–481.

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Hearing impairment among adults: the impact of cardiovascular diseases and cardiovascular risk factors.

To investigate the influence of cardiovascular diseases on hearing impairment (HI) among adults. Furthermore, to seek other potential risk factors for...
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