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Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea National Health and Nutrition Examination Survey (KNHANES 2010–2013)
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Research Article Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea National Health and Nutrition Examination Survey (KNHANES 2010–2013)
Gu Hyeok Kang, Jun Young Uhm, Young Gon Choi, Eun Kye Kang, Soo Young Kim, Won Oh Choo, Seong Sil Changorcid
Annals of Occupational and Environmental Medicine 2018;30:22.
DOI: https://doi.org/10.1186/s40557-018-0237-9
Published online: April 17, 2018

Xgrid.411061.3Department of Occupational & Environmental Medicine, Eulji University Hospital, 95 Dunsanseo-ro, Seo-gu, Daejeon, 35233 Republic of Korea

• Received: June 12, 2017   • Accepted: April 10, 2018

© The Author(s). 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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  • Background
    Lead and cadmium have been identified as risk factors for hearing loss in animal studies, but large-scale studies targeting the general human population are rare. This study was conducted to investigate the link between heavy metal concentrations in blood and hearing impairment, using a national population-based survey.
  • Methods
    The study participants comprised 6409 Koreans aged 20 or older, who were included in the Fifth and Sixth Korea National Health and Nutrition Examination Surveys (KNHANES 2010–2013). Hearing impairment was categorized into two types, low- and high-frequency hearing impairment, using pure tone audiometry. Low-frequency hearing impairment was defined as having a binaural average of hearing thresholds for 0.5, 1, and 2 kHz exceeding 25 dB, and high-frequency hearing impairment was defined as having a binaural average of hearing thresholds for 3, 4, and 6 kHz exceeding 25 dB. The blood levels of heavy metals (lead and cadmium) were classified into quartiles. Cross-sectional association between hearing impairment and the level of heavy metals (lead and cadmium) was examined in both sexes. Multivariate logistic regression was used to obtain adjusted odds ratios (ORs) and 95% confidence intervals (CIs).
  • Results
    Among men, the prevalence of low- and high- frequency hearing impairment was 13.9% and 46.7%, respectively, which was higher than the prevalence among women (11.8% and 27.0%, respectively). Regarding lead, the adjusted OR of high-frequency hearing impairment for the highest blood level group versus the lowest group was significant in both men (OR = 1.629, 95% CI = 1.161–2.287) and women (OR = 1.502, 95% CI = 1.027–2.196), after adjusting for age, body mass index, education, smoking, alcohol consumption, exercise, diagnosis of diabetes mellitus, hypertension, and noise exposure (occupational, loud, firearm noises). No links were found between blood lead levels and low-frequency hearing impairment, or between blood cadmium levels and low- or high-frequency hearing impairment in either sex.
  • Conclusions
    The present study findings suggest that even exposure to low-level lead is a risk factor for high-frequency hearing loss. A prospective epidemiologic study should be conducted to identify the causal relationship between human health and exposure to heavy metals, and efforts to reduce heavy metal exposure in the general population should continue.
  • Keywords:

    Keywords

    Hearing loss; Heavy metals; Lead; Cadmium; KNHANES
Hearing impairment is one of the most common health conditions, and is increasing in aging societies [1, 2]. According to the World Health Organization (WHO), 360 million people worldwide and approximately one third of the older population (65 years or older) suffer from hearing impairment [3]. In a study based on the 2010–2012 Korea National Health and Nutrition Examination Surveys (KNHANES), it was estimated that people with mild hearing impairment comprise 20.5% of the population over the age of 19 years, and 70% of the population over the age of 65 years [4]. Hearing impairment can cause social isolation due to communication problems in everyday life [5, 6], and is a serious public health issue in Korea.
Hearing impairment tends to increase rapidly with age [7]. Aside from aging, exposure to loud noise is a risk factor for hearing loss [8], and ototoxic chemicals also affect hearing ability [9–11]. Numerous studies have reported the effect of heavy metals on hearing loss. Jones et al. argued that lead is an ototoxic heavy metal and that lead exposure results in degeneration of the inner ear receptor cells and decreases the conduction function of auditory nerve cells [12]. Cadmium is reported to cause apoptosis of inner ear receptor cells and alter their arrangement, resulting in an increased hearing threshold [13, 14]. Prasher suggested multiple ototoxic effects of lead and cadmium [15]. Additionally, a limited number of epidemiologic studies have been conducted. In a study on the general population, Park et al. confirmed a link between low-level lead exposure and hearing impairment [16]. The relationship between hearing impairment and exposure to lead and cadmium was confirmed in a study by Shargorodsky et al. of American adolescents [17], and in a study of American adults by Choi et al. [18].
Heavy metals, such as lead and cadmium, are present not only in factory-manufactured products, but also in the environment within air, water, food, soil, and dust [19–21]. Industrialization has surreptitiously exposed human bodies to heavy metal [22]. Once heavy metal is absorbed into the body, it is stored in the tissues, because the human body has a limited capacity to effectively eliminate it, due to a half-life lasting several decades [23]. Consequently, the link between hearing impairment and heavy metal levels requires close examination. Currently, lead and cadmium concentration levels in Korea continue to decrease but remain higher when compared to developed countries such as the United States (US) and Canada [24]. Accordingly, the link between heavy metals and hearing impairment should be carefully monitored in Korea.
Several studies have examined the relationship between hearing impairment and heavy metals. However, the number of studies on the general population is limited and the number of epidemiologic studies conducted within the Korean population is even fewer. Accordingly, the present study was conducted to investigate the link between exposure to lead and cadmium and hearing impairment using KNHANES data.
Participants
Data from the fifth and sixth KNHANES, gathered from 2010 to 2013, was used for the analyses. The KNHANES is a multistage stratified complex design survey of a representative sample of the entire Korean population, conducted by the Korea Centers for Disease Control and Prevention. Trained interviewers and laboratory technicians conducted surveys in households, including administering questionnaires, performing health examinations, and collecting blood samples. The section for health behaviors, such as smoking and alcohol consumption, was self-administered. The total number of respondents was 33,552.
Of those, 6582 participants aged 20 years or older underwent pure tone audiometry and blood tests to assess the level of heavy metals (lead and cadmium). After excluding those with missing data, a total of 6409 participants were selected as study participants.
Hearing impairment
To examine the respondents hearing condition, pure tone audiometry was performed. Both ears were tested at 0.5, 1, 2, 3, 4, and 6 kHz, in a soundproof booth, using the Entomed SA 203. WHO defines hearing as normal if, in the better hearing ear, the average of hearing thresholds at 0.5, 1, 2, and 4 kHz is under 25 dB [25]. Until recently, this definition has been widely used as the criterion to determine an individual’s hearing condition in everyday life. However, potential hearing impairment of one ear may be neglected when the hearing threshold is under 25 dB in the other ear. To account for this, some studies have defined hearing impairment by taking the binaural average of hearing thresholds in preference to relying on the hearing ability of one ear only [26], while another study measured 2 types of hearing impairment, low- and high-frequency hearing impairment [27]. Based on information from these studies, we used the binaural pure-tone average threshold and computed two binaural averages, one across 0.5, 1, and 2 kHz and the other across 3, 4, and 6 kHz to determine the low- and high-frequency thresholds. Hearing impairment was then determined according to whether an average threshold exceeded 25 dB in the respective frequency band.
Measurement of lead and cadmium in whole blood
To measure heavy metal blood levels, blood samples were collected into standard commercial evacuated tubes coated with sodium heparin (Vacutainer). Blood lead and cadmium levels were measured via graphite furnace atomic absorption spectrometry (Perkin Elmer AAnalyst 600, Turku, Finland). For internal quality assurance, the analytical equipment was controlled with respect to the standard reference material from Whole Blood Metals Control (BIO-RAD, USA). The blood levels of each heavy metal were classified into quartiles separately for men and women, and geometric means with standard error were computed according to the quartile rank.
Other variables
In the analysis, we included factors suggested by previous studies as affecting hearing impairment. Some studies suggested that cerebro-cardiovascular risk factors, such as obesity and smoking, have a negative effect on hearing ability [28, 29], because the cochlea is vulnerable to ischemic changes [30]. On the other hand, moderate exercise and moderate alcohol consumption are reported to have a beneficial effect on hearing ability [31, 32].
Participants’ ages were grouped in 10-year intervals, starting from age 20, and participants aged 70 or higher were collectively gathered as one group. Body mass index (BMI) under 18.5 kg/m2 was classified as underweight, BMI between 18.5 and 25 kg/m2 as normal weight, and BMI over 25 kg/m2 as overweight. The education level was categorized as less than high school education; high school graduation; and more than high school education. Cigarette smoking was classified as follows: a non-smoker was defined as never having smoked more than 100 cigarettes; an ex-smoker was defined as having smoked 100 or more cigarettes but currently not smoking; and a current smoker was defined as having smoked 100 or more cigarettes and still currently smoking. Alcohol consumption was defined as: a non-drinker having never consumed alcohol, a light drinker as consuming alcohol less than twice per week or having fewer than 7 glasses (5 glasses for women) when drinking, and a heavy drinker as drinking more than twice per week or having 7 or more glasses (5 glasses for women) when drinking. Participants who performed intense physical activities 3 days or more per week and, with exercise, felt the effects of bodily exertions more than usual, or who performed intense exercises requiring heavy breathing for 30 min or more, were classified into an exercise group, and all others classified into a non-exercise group. Regarding noise exposure, participants who had been exposed to noise at their workplace over a 3-month period or exposed to loud noises such as car horns, machinery, and loud music at places other than the workplace for 5 h or more per week were classified into a noise exposure group. Those who had been exposed to firearm noise were also classified into the noise exposure group. Finally, regarding diabetes and hypertension, participants were categorized into one of two groups, respectively, depending on whether they had been diagnosed with diabetes or hypertension by a physician.
Statistical analyses
Weighted complex sampling analysis available from SPSS v.18.0 was used for data analysis. Regarding the general characteristics of participants, the mean and sample size for each variable was examined by sex. A chi-square test was performed to examine the distributions and t-tests performed to compare means. The relationship between each independent variable and hearing impairment was examined using a chi-square test. This test was conducted separately for low- and high-frequency hearing impairment and by sex. To examine sex-specific relationships between low- and high-frequency hearing impairment and heavy metal levels in blood, odds ratios (OR) were computed using complex sampling logistic regression. Statistical significance was defined as p < 0.05. In the first model, age, BMI, education, smoking, alcohol consumption, and exercise were included as adjusting variables, and in the second model, diabetes mellitus, and hypertension were additionally included as adjusting variables. The ORs in the final model were adjusted with exposures to occupational, loud, and firearm noises.
Participants’ general characteristics
Participants totaled 6409, of whom 3185 (49.6%) were men and 3224 (50.4%) were women. The mean age across all participants was 47; the mean age for men was 46, and for women, 48. Table 1 shows the general characteristics of the study participants. Regarding factors in respect of lifestyle habits, the proportions of ex-smokers and current smokers were both high in men, as well as the proportion of heavy drinkers. Regarding education levels, the proportions of those who had graduated from high school and those who had received more than high school education were significantly higher among men than women (p < 0.001). Additionally, the proportions of those exposed to occupational, loud, and firearm noises were significantly higher in men than in women.
Table 1
General characteristics of the study population
Variables Total na Male Female p-valueb
Total 6409 3185 3224
Age (years)
Mean ± SE 47.1 ± 0.3 46.3 ± 0.3 48.0 ± 0.3 < 0.001
 20–29 1025 493 532 0.002
 30–39 1081 537 544
 40–49 1415 709 706
 50–59 1454 717 737
 60–69 1232 615 617
 70–87 202 114 88
BMI (kg/m2)
Mean ± SE 23.8 ± 0.1 24.2 ± 0.1 23.5 ± 0.1 < 0.001
 Underweight 246 68 178 < 0.001
 Normal 4071 1936 2135
 Obese 2092 1181 911
Education
  ≤ Middle school 1861 751 1110 < 0.001
 High school 2365 1226 1139
  ≥ College 2183 1208 975
Smoking
 Non-smoker 3650 723 2927 < 0.001
 Ex-smoker 1176 1063 113
 Current smoker 1583 1399 184
Alcohol
 None 638 104 534 < 0.001
 Light drinker 4128 1923 2205
 Heavy drinker 1643 1158 485
Exercise
 No 4771 2271 2500 < 0.001
 Yes 1638 914 724
Current diagnosis of diabetes mellitus
 No 5980 2936 3044 0.069
 Yes 429 249 180
Current diagnosis of hypertension
 No 5237 2573 2664 0.202
 Yes 1172 612 560
Occupational noise exposure
 No 5496 2538 2958 < 0.001
 Yes 913 647 266
Loud noise exposure
 No 6267 3095 3172 0.008
 Yes 142 90 52
Firearm noise exposure
 No 4750 1642 3108 < 0.001
 Yes 1659 1543 116
SE standard error
aunweighted count, btested by chi-square test
The prevalence of low- and high-frequency hearing impairment
Tables 2 and 3 show the male and female prevalence of low- and high-frequency hearing impairment (defined, respectively, as a binaural average of hearing thresholds for 0.5, 1 and 2 kHz, and for 3, 4, and 6 kHz exceeding 25 dB), broken down for each of the variables. The prevalence of low- and high-frequency hearing impairment in men was 13.9% and 46.7%, respectively, which was higher than the prevalence in women (11.8% and 27.0%, respectively).
Table 2
Characteristics by hearing impairment in male subjects
Variables Low frequency hearing impairment High frequency hearing impairment
Normala Impaireda Rateb p-valuec Normala Impaireda Rateb p -valuec
Total 2743 442 13.9 1697 1488 46.7
Age
 20–29 486 7 1.4 < 0.001 466 27 5.5 < 0.001
 30–39 525 12 2.2 455 82 15.3
 40–49 680 29 4.1 444 265 37.4
 50–59 601 116 16.2 244 473 66
 60–69 406 209 34 84 531 86.3
 70–87 45 69 60.5 4 110 96.5
BMI (kg/m2)
 Underweight 56 12 17.6 0.086 39 29 42.6 0.610
 Normal 1650 286 14.8 1020 916 47.3
 Obese 1037 144 12.2 638 543 46
Education
  ≤ Middle school 514 237 31.6 < 0.001 159 592 78.8 < 0.001
 High school 1086 140 11.4 691 535 43.6
  ≥ College 1143 65 5.4 847 361 29.9
Smoking
 Non-smoker 664 59 8.2 < 0.001 483 240 33.2 < 0.001
 Ex-smoker 860 203 19.1 426 637 59.9
 Current smoker 1219 180 12.9 788 611 43.7
Alcohol
 None 77 27 26 < 0.001 42 62 59.6 < 0.001
 Light drinker 1613 310 16.1 914 1009 52.5
 Heavy drinker 1053 105 9.1 741 417 36
Exercise
 No 1941 330 14.5 0.093 1195 1076 47.4 0.239
 Yes 802 112 12.3 502 412 45.1
Current diagnosis of diabetes mellitus
 No 2558 378 12.9 < 0.001 1639 1297 44.2 < 0.001
 Yes 185 64 25.7 58 191 76.7
Current diagnosis of hypertension
 No 2289 284 11 < 0.001 1528 1045 40.6 < 0.001
 Yes 454 158 25.8 169 443 72.4
Occupational noise exposure
 no 2222 316 12.5 < 0.001 1413 1125 44.3 < 0.001
 yes 521 126 19.5 284 363 56.1
Loud noise exposure
 no 2667 428 13.8 0.640 1645 1450 46.8 0.386
 yes 76 14 15.6 52 38 42.2
Firearm noise exposure
 no 1425 217 13.2 0.265 884 758 46.2 0.517
 yes 1318 225 14.6 813 730 47.3
aunweighted count
bprevalence rate
ctested by chi-square test
Table 3
Characteristics by hearing impairment in female subjects
Variables Low frequency hearing impairment High frequency hearing impairment
Normala Impaireda Rateb p-valuec Normala Impaireda Rateb p-valuec
Total 2845 379 11.8 2354 870 27.0
Age
 20–29 525 7 1.3 < 0.001 519 13 2.4 < 0.001
 30–39 535 9 1.7 522 22 4
 40–49 676 30 4.2 614 92 13
 50–59 641 96 13 479 258 35
 60–69 421 196 31.8 209 408 66.1
 70–87 47 41 46.6 11 77 87.5
BMI (kg/m2)
 Underweight 167 11 6.2 < 0.001 156 22 12.4 < 0.001
 Normal 1906 229 10.7 1603 532 24.9
 Obese 772 139 15.3 595 316 34.7
Education
  ≤ Middle school 836 274 24.7 0.031 510 600 54.1 < 0.001
 High school 1058 81 7.1 938 201 17.6
  ≥ College 951 24 2.5 906 69 7.1
Smoking
 Non-smoker 2569 358 12.2 0.062 2114 813 27.8 0.004
 Ex-smoker 105 8 7.1 88 25 22.1
 Current smoker 171 13 7.1 152 32 17.4
Alcohol
 None 412 122 22.8 < 0.001 281 253 47.4 < 0.001
 Light drinker 1962 243 11 1646 559 25.4
 Heavy drinker 471 14 2.9 427 58 12
Exercise
 No 2185 315 12.6 0.006 1794 706 28.2 0.003
 Yes 660 64 8.8 560 164 22.7
Current diagnosis of diabetes mellitus
 No 2717 327 10.7 < 0.001 2272 772 25.4 < 0.001
 Yes 128 52 28.9 82 98 54.4
Current diagnosis of hypertension
 No 2444 220 8.3 < 0.001 2112 552 20.7 < 0.001
 Yes 401 159 28.4 242 318 56.8
Occupational noise exposure
 No 2610 348 11.8 0.957 2174 784 26.5 0.043
 Yes 235 31 11.7 180 86 32.3
Loud noise exposure
 No 2797 375 11.8 0.359 2318 854 26.9 0.535
 Yes 48 4 7.7 36 16 30.8
Firearm noise exposure
 no 2747 361 11.6 0.200 2288 820 26.4 < 0.001
 yes 98 18 15.5 66 50 43.1
aunweighted count
bprevalence rate
ctested by chi-square test
In men, the proportions of low- and high-frequency hearing impairment increased with age (low frequency: p < 0.001, high frequency: p < 0.001). Focusing on BMI and exercise habits, the prevalence of low-frequency hearing impairment had a lower tendency but not significantly lower in the obese group (p = 0.086) and in the exercise group (p = 0.093). Regarding education level, the prevalence of both low- and high-frequency hearing impairment decreased as the education level advanced (p < 0.001). Low- and high-frequency hearing impairment was less prevalent in the non-smoker group and in the heavy drinker group, as well as in the groups not diagnosed with diabetes and hypertension. In contrast, both low- and high-frequency hearing impairment was significantly more prevalent in the group exposed to occupational noise (p < 0.001). There was no significant difference in the groups exposed to loud and firearm noises.
In women, the proportions of low- and high-frequency hearing impairment increased with age (low frequency: p < 0.001, high frequency: p < 0.001). The prevalence of both low- and high-frequency impairment was significantly lower where BMI was lower and the education level was higher, as well as in the heavy drinker group and the groups not diagnosed with diabetes and hypertension. Exposure to loud noise did not show a significant difference, but the group exposed to occupational and firearm noise showed a significantly higher prevalence of high-frequency hearing impairment (p = 0.043, p < 0.001).
Figure 1 shows the binaural average of frequency hearing thresholds of quartile groups based on blood lead level and blood cadmium level in male and female participants (mean ± SD). The figure displays that the hearing thresholds increase as the quartile group is higher in general.
Fig. 1
Binaural average of frequency hearing thresholds by quartile of lead, cadmium. Mean ± SD
40557_2018_237_Fig1_HTML.jpg
ORs of hearing impairment according to blood lead and cadmium levels
Tables 4 and 5 show the results of multivariate logistic regression analysis conducted for male and female participants. The tables display the ORs of low- and high-frequency hearing impairment for two sets of quartile groups, based on blood lead level and blood cadmium level, respectively.
Table 4
Adjusted ORs and 95% CI of hearing impairment by quartile of lead, cadmium in male
Analyte <25th 25th to <50th 50th to <75th ≥75th
Lead
 Conc, μg/dLa 1.56 ± 0.01 2.22 ± 0.01 2.82 ± 0.01 4.22 ± 0.08
 Case/n (low frequency) 80/796 96/797 111/796 155/796
 Hearing thresholds(dB)b 10.8 ± 0.47 13.3 ± 0.56 14.8 ± 0.59 17.8 ± 0.70
 Prevalence(%)c 9.2% 12.7% 16.2% 21.7%
 Adjusted OR(95% CI)d Referent 1.153 (0.761–1.747) 1.002 (0.644–1.559) 1.049 (0.694–1.585)
 Adjusted OR(95% CI)e Referent 1.15 (0.758–1.745) 0.998 (0.640–1.555) 1.045 (0.690–1.582)
 Adjusted OR(95% CI)f Referent 1.17 (0.772–1.772) 1.028 (0.661–1.597) 1.026 (0.677–1.556)
 Case/n (high frequency) 242/796 322/797 404/796 520/796
 Hearing thresholds(dB)b 21.2 ± 0.86 27.4 ± 0.99 31.4 ± 0.99 37.9 ± 1.05
 Prevalence(%)c 28.6% 41.6% 51.3% 63.9%
 Adjusted OR(95% CI)d Referent 1.342 (0.988–1.823) 1.357 (0.972–1.894) 1.598 (1.14–2.238)
 Adjusted OR(95% CI)e Referent 1.352 (0.994–1.837) 1.365 (0.978–1.906) 1.614 (1.151–2.263)
 Adjusted OR(95% CI)f Referent 1.368 (1.006–1.859) 1.402 (1.005–1.955) 1.629 (1.161–2.287)
Cadmium
 Conc, μg/dLa 0.47 ± 0.01 0.79 ± 0.01 1.13 ± 0.01 1.88 ± 0.03
 Case/n (low frequency) 57/797 99/797 130/798 156/793
 Hearing thresholds(dB)b 10.5 ± 0.55 13.4 ± 0.53 15.3 ± 0.57 17.4 ± 0.71
 Prevalence(%)c 8.4% 12.9% 17.1% 21.1%
 Adjusted OR(95% CI)d Referent 0.857 (0.532–1.379) 0.845 (0.54–1.322) 0.924 (0.567–1.505)
 Adjusted OR(95% CI)e Referent 0.855 (0.531–1.376) 0.84 (0.537–1.313) 0.922 (0.566–1.503)
 Adjusted OR(95% CI)f Referent 0.842 (0.524–1.354) 0.83 (0.533–1.291) 0.905 (0.556–1.473)
 Case/n (high frequency) 221/797 362/797 433/798 472/793
 Hearing thresholds(dB)b 20.9 ± 1.00 29.0 ± 0.94 32.5 ± 1.02 35.3 ± 1.04
 Prevalence(%)c 27.4% 46.3% 52.3% 59.2%
 Adjusted OR(95% CI)d Referent 1.238 (0.895–1.712) 1.159 (0.828–1.623) 1.284 (0.892–1.848)
 Adjusted OR(95% CI)e Referent 1.236 (0.894–1.71) 1.163 (0.83–1.629) 1.283 (0.891–1.848)
 Adjusted OR(95% CI)f Referent 1.235 (0.891–1.711) 1.168 (0.833–1.638) 1.292 (0.896–1.865)
aConc, weighted mean ± SE
bBinaural average of hearing thresholds, weighted mean ± SE
cWeighted percentages
dAdjusted for age, BMI, education, smoking, alcohol consumption, and exercise,
eAdditional adjustment for diabetes mellitus, hypertension
fAdditional adjustment for noise exposure (Occupational, loud, Firearm noise)
Table 5
Adjusted ORs and 95% CI of hearing impairment by quartile of lead, cadmium in female
Analyte <25th 25th to <50th 50th to <75th ≥75th
Lead
 Conc, μg/dLa 1.12 ± 0.01 1.61 ± 0.01 2.11 ± 0.01 3.03 ± 0.03
 Case/n (low frequency) 63//808 82/804 101/806 133/806
 Hearing thresholds(dB)b 11.6 ± 0.53 13.0 ± 0.63 14.0 ± 0.52 17.8 ± 0.79
 Prevalence(%)c 10.9% 11.1% 12.6% 20.6%
 Adjusted OR(95% CI)d Referent 1.312 (0.755–2.279) 1.302 (0.791–2.143) 0.957 (0.563–1.626)
 Adjusted OR(95% CI)e Referent 1.288 (0.74–2.24) 1.281 (0.773–2.123) 0.93 (0.544–1.589)
 Adjusted OR(95% CI)f Referent 1.271 (0.726–2.223) 1.308 (0.784–2.183) 0.932 (0.541–1.604)
 Case/n (high frequency) 135/808 178/804 234/806 323/806
 Hearing thresholds(dB)b 16.4 ± 0.75 19.9 ± 0.87 21.4 ± 0.70 27.5 ± 1.10
 Prevalence(%)c 20.3% 24.2% 29.2% 44.7%
 Adjusted OR(95% CI)d Referent 0.937 (0.599–1.464) 1.009 (0.695–1.464) 1.488 (1.02–2.172)
 Adjusted OR(95% CI)e Referent 0.941 (0.602–1.471) 1.012 (0.698–1.467) 1.499 (1.028–2.187)
 Adjusted OR(95% CI)f Referent 0.947 (0.606–1.477) 1.013 (0.698–1.471) 1.502 (1.027–2.196)
Cadmium
 Conc, μg/dLa 0.57 ± 0.01 0.96 ± 0.01 1.36 ± 0.01 2.17 ± 0.03
 Case/n (low frequency) 42/806 89/807 110/806 138/805
 Hearing thresholds(dB)b 9.3 ± 0.45 14.2 ± 0.59 15.9 ± 0.63 16.9 ± 0.73
 Prevalence(%)c 6.2% 13.4% 17% 18.5%
 Adjusted OR(95% CI)d Referent 0.873 (0.486–1.567) 0.916 (0.523–1.603) 0.768 (0.432–1.364)
 Adjusted OR(95% CI)e Referent 0.88 (0.489–1.586) 0.92 (0.524–1.616) 0.758 (0.426–1.349)
 Adjusted OR(95% CI)f Referent 0.875 (0.488–1.57) 0.913 (0.521–1.601) 0.757 (0.427–1.343)
 Case/n (high frequency) 85/806 212/807 280/806 293/805
 Hearing thresholds(dB)b 13.5 ± 0.69 21.1 ± 0.88 25.0 ± 0.94 25.4 ± 0.90
 Prevalence(%)c 13.3% 28.4% 37.6% 38.6%
 Adjusted OR(95% CI)d Referent 1.225 (0.799–1.878) 1.302 (0.821–2.067) 1.425 (0.91–2.231)
 Adjusted OR(95% CI)e Referent 1.229 (0.799–1.89) 1.308 (0.821–2.082) 1.427 (0.908–2.244)
 Adjusted OR(95% CI)f Referent 1.248 (0.812–1.919) 1.325 (0.831–2.115) 1.426 (0.906–2.244)
aConc, weighted mean ± SE
bBinaural average of hearing thresholds, weighted mean ± SE
cWeighted percentages
dAdjusted for age, BMI, education, smoking, alcohol consumption, and exercise,
eAdditional adjustment for diabetes mellitus, hypertension
fAdditional adjustment for noise exposure (Occupational, loud, Firearm noise)
In men, the ORs of low-frequency hearing impairment were not significant for the quartile groups based on blood lead levels, with the lowest group as a reference. However, the OR of high-frequency hearing impairment for the highest quartile group compared to the lowest group was significantly high, that is, 1.598 (95% confidence interval [CI] = 1.140–2.238), after adjusting for age, BMI, education, smoking, alcohol consumption, and exercise. The outcome was the same when diabetes mellitus and hypertension were added as adjusted variables. After adjusting for exposure to occupational, loud, and firearm noises, the ORs significantly increased for all groups, compared to the lowest blood lead group as a reference. Regarding blood cadmium levels, the OR of low- or high-frequency hearing impairment was not significant for any quartile groups, with the lowest group as a reference.
As with the men, the ORs of low-frequency hearing impairment were not significant in women for any quartile groups based on blood lead levels, with the lowest group as a reference. However, the OR of high-frequency hearing impairment for the highest quartile group with the lowest as a reference was significant, that is, 1.488 (95% CI = 1.02–2.172), when adjusted for age, BMI, education, smoking, alcohol consumption, and exercise. The result was the same when diabetes mellitus, hypertension, and exposures to occupational, loud, and firearm noises were additionally included as adjusted variables. In addition, in line with findings for the men, women’s ORs for any quartile groups, based on blood cadmium level with the lowest group as a reference, were not significant in either low- or high-frequency hearing impairment.
The objective of the present study was to investigate the link between heavy metals to which the general population is generally exposed and hearing impairment. In the study, there was no difference between the sexes in respect of any link between heavy metals and hearing impairment. Regarding the relationship between blood lead level and high-frequency hearing impairment, the risk of hearing impairment significantly increased in both sexes. However, with respect to low-frequency hearing impairment, significant results were not obtained. In addition, blood cadmium level did not show a significant result in either low- or high-frequency hearing impairment in either sex.
Several previous studies have reported associations between lead and cadmium levels, and hearing impairment. In a study within the general US population, Choi et al. found that the hearing threshold of the highest quintile groups, based on blood lead and cadmium levels, was higher compared to the respective lowest group, by approximately 18.6% (95% CI = 7.4%–31.1%) and 13.8% (95% CI = 4.6%–23.8%), respectively [18]. Shargorodsky et al. reported, in a study with US adolescents, that the OR of high-frequency hearing impairment for the group with a blood lead level over 2 μg/dL was significantly higher compared to a reference group (a blood lead level under 1 μg/dL), that is, 2.22 (95% CI = 1.39–3.56), and that the OR of low-frequency hearing impairment was also significantly higher for the highest quartile group, based on urinary cadmium levels in comparison to the lowest group, that is, 3.08 (95% CI = 1.02–9.25) [17]. Park et al. conducted a study with 448 community-dwelling elderly men in eastern Massachusetts and demonstrated a link between hearing impairment and an increase in the interquartile range of the lead levels in the patella. In their study, the OR was 1.5 (95% CI = 1.1–1.9). In conclusion, evidence that lead and cadmium affect hearing ability within the general population is accumulating steadily [16].
Although previous studies have shown that heavy metals such as lead and cadmium affect hearing ability, the present study, to the best of our knowledge, is the first epidemiologic study conducted on Korean participants to examine the relationship between hearing impairment and cadmium exposure. The ototoxicity mechanism involving cadmium is suggested by only a handful of studies. In a study with rats exposed to water containing cadmium, it was shown that cadmium produces reactive oxygen species in auditory cells and causes loss of mitochondrial membrane depolarization, release of cytochrome c, activations of apoptosis and caspases, and an increase in extracellular signal-regulated kinase activation that ultimately elevates the hearing threshold [13, 14]. A study with US adolescents reported a significant relationship between urinary cadmium and low-frequency hearing impairment. In that study, hearing impairment was defined as an average of hearing thresholds for 0.5, 1, and 2 kHz exceeding 15 dB [17]. In a study with US adults, there was a significant correlation between blood cadmium levels and hearing impairment, with hearing impairment defined as the hearing thresholds for 0.5, 1, 2, and 4 kHz frequencies exceeding 25 dB in one of two ears [18]. Unlike these previous studies, no significant relationship was found between cadmium and hearing impairment in our study, due to several possible reasons. First, this study conducted a different statistical analysis. In the two previously mentioned studies, the data were not categorized by sex, and sex was included as an adjusting variable, unlike the present study. When we performed an additional analysis on the entire data set, not separating it into male and female categories, but including sex as an adjusting variable, we observed that the OR of high-frequency hearing impairment for the highest quartile group with the lowest group as a reference was significant, that is, 1.40 (95% CI = 1.07–1.82). Secondly, the differing results may be due to differences in physical responses caused by variations in ethnicity and lifestyle. Thirdly, the differing results may be due to different definitions and thresholds of hearing impairment used across these studies. Aside from these possibilities, our study and the study with US adolescents had different study participants, that is, adults versus adolescents, and differed in how cadmium was measured, namely in blood versus urinary test levels. More research is needed to study the link between cadmium and hearing impairment in the Korean population.
Regarding the link between lead and hearing impairment, many studies have reported results similar to the current study findings, unlike the case with cadmium. However, while the mechanisms through which lead influences the auditory system are not yet clearly known, chronic lead exposure is known to be toxic to the central and peripheral nervous systems. By using an auditory brainstem response test, a study has shown that lead exposure affects the conduction function of the peripheral nervous system along the auditory pathways [33]. Likewise, Jones et al. reported that lead exposure changes the axonal structure and function of the brainstem auditory nuclei [12]. An alternative hypothesis is that toxic metals affect intracellular calcium homeostasis [34] and accordingly, chronic lead exposure induces auditory hair cell death [35].
The current study findings support the case that even a low level of lead can negatively affect the hearing condition of the Korean general population and that, therefore, an effort should be made to reduce environmental lead exposure. The fourth quartile groups based on blood lead levels demonstrated a risk for poorer hearing in comparison to the first quartile groups. Currently, the Safety Standards of the Occupational Safety and Health Administration (OSHA) specifies 38.6 μg/dL for lead and 5 μg/L for cadmium as blood level thresholds. None of the 6409 participants in the present study exceeded the recommended threshold for lead, and only 6 exceeded it for cadmium. Accordingly, the current study findings suggest that the risk of hearing impairment is present even at a level below the OSHA threshold recommendation for lead. Evidence has been advanced to demonstrate that even where blood lead and cadmium levels are below the respective recommended threshold, they can still lead to chronic kidney disease, peripheral arterial disease, and hypertension [36–38]. Studies conducted in the US have already suggested the possibility of hearing impairment in adolescents and adults following lead and cadmium exposure at a level below their respective recommended thresholds [17, 18].
An advantage of the present study is that it was conducted on a representative sample of the Korean population, and the findings can be generalized to the entire Korean population. Although evidence for the link between hearing impairment and heavy metals, such as lead and cadmium, is accumulating, most studies have been limited in that they were either animal studies or based on a small sample size [12–16]. Epidemiologic studies targeting the general population, such as this study, are rare.
Limitations
There are several limitations to this study. First, participants’ past work history was not considered. Secondly, the level of noise exposure was not accurately measured and was based on self-reported data, meaning that information bias could have been present. In addition, the participants might have not accurately recalled their noise exposure history over the course of their lives. Thirdly, information pertaining to additional factors that could affect hearing ability, for example, congenital diseases, middle ear diseases, exposures to physical trauma, medication, and toxic substance history, was not included in the original KNHANES dataset. Fourthly, although the study used secondary data that was representative of the Korean population (KNHANES), it was a cross-sectional study. Hence, a causal relationship between hearing impairment and heavy metals could not be clearly identified.
To overcome these limitations in future research, work history, medical history, noise exposure, physical trauma, medication, and toxic substances should be examined and the noise level in the workplace should be measured. Additionally, a cohort study should be conducted that includes people not exposed to occupational and environmental noise.
In the Korean population, exposure to low-level lead is significantly associated with high-frequency hearing impairment in both men and women. Therefore, lead exposure should be closely monitored to protect citizens’ health.

The data of the KNHANES is opened to the public, therefore, any researcher can be obtained after request from the website https://knhanes.cdc.go.kr/knhanes/eng/index.do.

BMI

Body mass index

CI

Confidence interval

KNHANES

Korea National Health and Nutrition Examination Surveys

OR

odds ratio

OSHA

Occupational Safety and Health Administration

WHO

World Health Organization
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Figure & Data

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      Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea National Health and Nutrition Examination Survey (KNHANES 2010–2013)
      Ann Occup Environ Med. 2018;30:22  Published online April 17, 2018
      DOI: https://doi.org/10.1186/s40557-018-0237-9
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    Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea National Health and Nutrition Examination Survey (KNHANES 2010–2013)
    Image
    Fig. 1 Binaural average of frequency hearing thresholds by quartile of lead, cadmium. Mean ± SD

    Fig. 1

    Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea National Health and Nutrition Examination Survey (KNHANES 2010–2013)
    VariablesTotal naMaleFemalep-valueb
    Total640931853224
    Age (years)
    Mean ± SE47.1 ± 0.346.3 ± 0.348.0 ± 0.3< 0.001
     20–2910254935320.002
     30–391081537544
     40–491415709706
     50–591454717737
     60–691232615617
     70–8720211488
    BMI (kg/m2)
    Mean ± SE23.8 ± 0.124.2 ± 0.123.5 ± 0.1< 0.001
     Underweight24668178< 0.001
     Normal407119362135
     Obese20921181911
    Education
      ≤ Middle school18617511110< 0.001
     High school236512261139
      ≥ College21831208975
    Smoking
     Non-smoker36507232927< 0.001
     Ex-smoker11761063113
     Current smoker15831399184
    Alcohol
     None638104534< 0.001
     Light drinker412819232205
     Heavy drinker16431158485
    Exercise
     No477122712500< 0.001
     Yes1638914724
    Current diagnosis of diabetes mellitus
     No5980293630440.069
     Yes429249180
    Current diagnosis of hypertension
     No5237257326640.202
     Yes1172612560
    Occupational noise exposure
     No549625382958< 0.001
     Yes913647266
    Loud noise exposure
     No6267309531720.008
     Yes1429052
    Firearm noise exposure
     No475016423108< 0.001
     Yes16591543116
    VariablesLow frequency hearing impairmentHigh frequency hearing impairment
    NormalaImpairedaRatebp-valuecNormalaImpairedaRatebp -valuec
    Total274344213.91697148846.7
    Age
     20–2948671.4< 0.001466275.5< 0.001
     30–39525122.24558215.3
     40–49680294.144426537.4
     50–5960111616.224447366
     60–69406209348453186.3
     70–87456960.5411096.5
    BMI (kg/m2)
     Underweight561217.60.086392942.60.610
     Normal165028614.8102091647.3
     Obese103714412.263854346
    Education
      ≤ Middle school51423731.6< 0.00115959278.8< 0.001
     High school108614011.469153543.6
      ≥ College1143655.484736129.9
    Smoking
     Non-smoker664598.2< 0.00148324033.2< 0.001
     Ex-smoker86020319.142663759.9
     Current smoker121918012.978861143.7
    Alcohol
     None772726< 0.001426259.6< 0.001
     Light drinker161331016.1914100952.5
     Heavy drinker10531059.174141736
    Exercise
     No194133014.50.0931195107647.40.239
     Yes80211212.350241245.1
    Current diagnosis of diabetes mellitus
     No255837812.9< 0.0011639129744.2< 0.001
     Yes1856425.75819176.7
    Current diagnosis of hypertension
     No228928411< 0.0011528104540.6< 0.001
     Yes45415825.816944372.4
    Occupational noise exposure
     no222231612.5< 0.0011413112544.3< 0.001
     yes52112619.528436356.1
    Loud noise exposure
     no266742813.80.6401645145046.80.386
     yes761415.6523842.2
    Firearm noise exposure
     no142521713.20.26588475846.20.517
     yes131822514.681373047.3
    VariablesLow frequency hearing impairmentHigh frequency hearing impairment
    NormalaImpairedaRatebp-valuecNormalaImpairedaRatebp-valuec
    Total284537911.8235487027.0
    Age
     20–2952571.3< 0.001519132.4< 0.001
     30–3953591.7522224
     40–49676304.26149213
     50–59641961347925835
     60–6942119631.820940866.1
     70–87474146.6117787.5
    BMI (kg/m2)
     Underweight167116.2< 0.0011562212.4< 0.001
     Normal190622910.7160353224.9
     Obese77213915.359531634.7
    Education
      ≤ Middle school83627424.70.03151060054.1< 0.001
     High school1058817.193820117.6
      ≥ College951242.5906697.1
    Smoking
     Non-smoker256935812.20.062211481327.80.004
     Ex-smoker10587.1882522.1
     Current smoker171137.11523217.4
    Alcohol
     None41212222.8< 0.00128125347.4< 0.001
     Light drinker196224311164655925.4
     Heavy drinker471142.94275812
    Exercise
     No218531512.60.006179470628.20.003
     Yes660648.856016422.7
    Current diagnosis of diabetes mellitus
     No271732710.7< 0.001227277225.4< 0.001
     Yes1285228.9829854.4
    Current diagnosis of hypertension
     No24442208.3< 0.001211255220.7< 0.001
     Yes40115928.424231856.8
    Occupational noise exposure
     No261034811.80.957217478426.50.043
     Yes2353111.71808632.3
    Loud noise exposure
     No279737511.80.359231885426.90.535
     Yes4847.7361630.8
    Firearm noise exposure
     no274736111.60.200228882026.4< 0.001
     yes981815.5665043.1
    Analyte<25th25th to <50th50th to <75th≥75th
    Lead
     Conc, μg/dLa1.56 ± 0.012.22 ± 0.012.82 ± 0.014.22 ± 0.08
     Case/n (low frequency)80/79696/797111/796155/796
     Hearing thresholds(dB)b10.8 ± 0.4713.3 ± 0.5614.8 ± 0.5917.8 ± 0.70
     Prevalence(%)c9.2%12.7%16.2%21.7%
     Adjusted OR(95% CI)dReferent1.153 (0.761–1.747)1.002 (0.644–1.559)1.049 (0.694–1.585)
     Adjusted OR(95% CI)eReferent1.15 (0.758–1.745)0.998 (0.640–1.555)1.045 (0.690–1.582)
     Adjusted OR(95% CI)fReferent1.17 (0.772–1.772)1.028 (0.661–1.597)1.026 (0.677–1.556)
     Case/n (high frequency)242/796322/797404/796520/796
     Hearing thresholds(dB)b21.2 ± 0.8627.4 ± 0.9931.4 ± 0.9937.9 ± 1.05
     Prevalence(%)c28.6%41.6%51.3%63.9%
     Adjusted OR(95% CI)dReferent1.342 (0.988–1.823)1.357 (0.972–1.894)1.598 (1.14–2.238)
     Adjusted OR(95% CI)eReferent1.352 (0.994–1.837)1.365 (0.978–1.906)1.614 (1.151–2.263)
     Adjusted OR(95% CI)fReferent1.368 (1.006–1.859)1.402 (1.005–1.955)1.629 (1.161–2.287)
    Cadmium
     Conc, μg/dLa0.47 ± 0.010.79 ± 0.011.13 ± 0.011.88 ± 0.03
     Case/n (low frequency)57/79799/797130/798156/793
     Hearing thresholds(dB)b10.5 ± 0.5513.4 ± 0.5315.3 ± 0.5717.4 ± 0.71
     Prevalence(%)c8.4%12.9%17.1%21.1%
     Adjusted OR(95% CI)dReferent0.857 (0.532–1.379)0.845 (0.54–1.322)0.924 (0.567–1.505)
     Adjusted OR(95% CI)eReferent0.855 (0.531–1.376)0.84 (0.537–1.313)0.922 (0.566–1.503)
     Adjusted OR(95% CI)fReferent0.842 (0.524–1.354)0.83 (0.533–1.291)0.905 (0.556–1.473)
     Case/n (high frequency)221/797362/797433/798472/793
     Hearing thresholds(dB)b20.9 ± 1.0029.0 ± 0.9432.5 ± 1.0235.3 ± 1.04
     Prevalence(%)c27.4%46.3%52.3%59.2%
     Adjusted OR(95% CI)dReferent1.238 (0.895–1.712)1.159 (0.828–1.623)1.284 (0.892–1.848)
     Adjusted OR(95% CI)eReferent1.236 (0.894–1.71)1.163 (0.83–1.629)1.283 (0.891–1.848)
     Adjusted OR(95% CI)fReferent1.235 (0.891–1.711)1.168 (0.833–1.638)1.292 (0.896–1.865)
    Analyte<25th25th to <50th50th to <75th≥75th
    Lead
     Conc, μg/dLa1.12 ± 0.011.61 ± 0.012.11 ± 0.013.03 ± 0.03
     Case/n (low frequency)63//80882/804101/806133/806
     Hearing thresholds(dB)b11.6 ± 0.5313.0 ± 0.6314.0 ± 0.5217.8 ± 0.79
     Prevalence(%)c10.9%11.1%12.6%20.6%
     Adjusted OR(95% CI)dReferent1.312 (0.755–2.279)1.302 (0.791–2.143)0.957 (0.563–1.626)
     Adjusted OR(95% CI)eReferent1.288 (0.74–2.24)1.281 (0.773–2.123)0.93 (0.544–1.589)
     Adjusted OR(95% CI)fReferent1.271 (0.726–2.223)1.308 (0.784–2.183)0.932 (0.541–1.604)
     Case/n (high frequency)135/808178/804234/806323/806
     Hearing thresholds(dB)b16.4 ± 0.7519.9 ± 0.8721.4 ± 0.7027.5 ± 1.10
     Prevalence(%)c20.3%24.2%29.2%44.7%
     Adjusted OR(95% CI)dReferent0.937 (0.599–1.464)1.009 (0.695–1.464)1.488 (1.02–2.172)
     Adjusted OR(95% CI)eReferent0.941 (0.602–1.471)1.012 (0.698–1.467)1.499 (1.028–2.187)
     Adjusted OR(95% CI)fReferent0.947 (0.606–1.477)1.013 (0.698–1.471)1.502 (1.027–2.196)
    Cadmium
     Conc, μg/dLa0.57 ± 0.010.96 ± 0.011.36 ± 0.012.17 ± 0.03
     Case/n (low frequency)42/80689/807110/806138/805
     Hearing thresholds(dB)b9.3 ± 0.4514.2 ± 0.5915.9 ± 0.6316.9 ± 0.73
     Prevalence(%)c6.2%13.4%17%18.5%
     Adjusted OR(95% CI)dReferent0.873 (0.486–1.567)0.916 (0.523–1.603)0.768 (0.432–1.364)
     Adjusted OR(95% CI)eReferent0.88 (0.489–1.586)0.92 (0.524–1.616)0.758 (0.426–1.349)
     Adjusted OR(95% CI)fReferent0.875 (0.488–1.57)0.913 (0.521–1.601)0.757 (0.427–1.343)
     Case/n (high frequency)85/806212/807280/806293/805
     Hearing thresholds(dB)b13.5 ± 0.6921.1 ± 0.8825.0 ± 0.9425.4 ± 0.90
     Prevalence(%)c13.3%28.4%37.6%38.6%
     Adjusted OR(95% CI)dReferent1.225 (0.799–1.878)1.302 (0.821–2.067)1.425 (0.91–2.231)
     Adjusted OR(95% CI)eReferent1.229 (0.799–1.89)1.308 (0.821–2.082)1.427 (0.908–2.244)
     Adjusted OR(95% CI)fReferent1.248 (0.812–1.919)1.325 (0.831–2.115)1.426 (0.906–2.244)
    Table 1 General characteristics of the study population

    SE standard error

    aunweighted count, btested by chi-square test

    Table 2 Characteristics by hearing impairment in male subjects

    aunweighted count

    bprevalence rate

    ctested by chi-square test

    Table 3 Characteristics by hearing impairment in female subjects

    aunweighted count

    bprevalence rate

    ctested by chi-square test

    Table 4 Adjusted ORs and 95% CI of hearing impairment by quartile of lead, cadmium in male

    aConc, weighted mean ± SE

    bBinaural average of hearing thresholds, weighted mean ± SE

    cWeighted percentages

    dAdjusted for age, BMI, education, smoking, alcohol consumption, and exercise,

    eAdditional adjustment for diabetes mellitus, hypertension

    fAdditional adjustment for noise exposure (Occupational, loud, Firearm noise)

    Table 5 Adjusted ORs and 95% CI of hearing impairment by quartile of lead, cadmium in female

    aConc, weighted mean ± SE

    bBinaural average of hearing thresholds, weighted mean ± SE

    cWeighted percentages

    dAdjusted for age, BMI, education, smoking, alcohol consumption, and exercise,

    eAdditional adjustment for diabetes mellitus, hypertension

    fAdditional adjustment for noise exposure (Occupational, loud, Firearm noise)

    Table 1

    Table 2

    Table 3

    Table 4

    Table 5

    Ann Occup Environ Med : Annals of Occupational and Environmental Medicine
    © Korean Society of Occupational & Environmental Medicine.
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