Chemosphere 102 (2014) 6–11

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Serum polychlorinated biphenyls concentrations and hearing impairment in adults Jin-Young Min a, Rokho Kim b, Kyoung-Bok Min c,⇑ a

Institute of Health and Environment, Seoul National University, Seoul, Republic of Korea World Health Organization Regional Office for the Western Pacific, Suva, Fiji c Department of Occupational and Environmental Medicine, Ajou University School of Medicine, Suwon, Republic of Korea b

h i g h l i g h t s  There is evidence on the ototoxicity of polychlorinated biphenyls(PCBs) in human.  We examined the association between serum PCB and hearing impairment in adults.  PCBs levels were positively associated with the prevalence of hearing impairment.  Environmental PCB exposures may be harmful to the maintenance of hearing function.

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Article history: Received 13 August 2013 Received in revised form 4 November 2013 Accepted 21 November 2013 Available online 21 December 2013 Keywords: Polychlorinated biphenyls Ototoxicity Hearing impairment General population

a b s t r a c t Experimental studies have suggested the potential link between exposure to polychlorinated biphenyls (PCBs) and auditory impairment, but little evidence exists to support the ototoxicity of PCBs in human. Only a few studies have implicated PCB-induced hearing loss in children. This study investigated the association between serum PCB levels and hearing impairment in US adults. We analyzed data from 1946 adults aged 20 years and older in the National Health and Nutrition Examination Survey 1999– 2004: eleven PCB congeners detected in 60–90% of the samples at greater than the limit of detection (LOD) were selected, and hearing impairment was defined as a pure-tone average of the thresholds at 0.5, 1, 2 and 4 kHz of >25 dB hearing level in better ear. The adjusted odds ratio of hearing impairment was significantly increased comparing the highest quartile (Q4) of detectable PCB range with the reference (below LOD): 5.83 (95% CI: 1.20–28.24) for 2,20 ,3,30 ,4,40 ,5-heptachlorobiphenyl (PCB-170), 7.79(95% CI: 1.81–33.44) for 2,20 ,3,4,40 ,5,50 -heptachlorobiphenyl (PCB-180), 7.46 (95% CI: 1.62–34.47) for 2,20 ,3,40 ,5,50 ,6-heptachlorobiphenyl (PCB-187), 8.59 (95% CI: 1.26–58.73) for 2,20 ,3,30 ,4,40 ,5,50 -octachlorobiphenyl (PCB-194), 11.62 (95% CI: 2.20–61.55) for 2,20 ,3,30 ,4,40 ,5,60 -octachlorobiphenyl (PCB196). Our findings suggest that specific classes of PCB levels may be associated with hearing impairment in a general sample of adults. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Polychlorinated biphenyls (PCBs) are a family of synthetic chlorinated compounds that are found in insulation, coolants, lubricants in electrical equipment and other applications. PCBs are particularly harmful due to their resistance to degradation, longer-range transport and deposition, and ability to bio-magnify throughout the food chain and bio-accumulate in fatty tissues of organisms (ATSDR, 2000).

⇑ Corresponding author. Address: Department of Occupational and Environmental Medicine, Ajou University School of Medicine, San 5, Wonchon-dong, Yeongtong-gu, Suwon 443-721, Republic of Korea. Tel.: +82 31 219 5278; fax: +82 31 241 1697. E-mail address: [email protected] (K.-B. Min). 0045-6535/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2013.11.046

Although the use of PCBs has been banned or restricted, these substances remain ubiquitous, and a large proportion of the population is exposed to background levels. Exposure to PCBs, even at low levels, is associated with a wide range of adverse health effects including disruption of the endocrine, cardiovascular, and immune systems; neurobehavioral impairment; and cancers (Loomis et al., 1997; Colborn, 2004; Carpenter, 2006). PCB-induced hearing impairment has been a matter of concern. Many of related studies have suggested the potential link between exposure to PCBs and auditory impairment in treated animals (Goldey et al., 1995; Herr et al., 1996; Crofton et al., 2000; Lasky et al., 2002; Powers et al., 2006). However, there is little evidence to support the ototoxicity of PCBs in humans. Only a few epidemiologic studies have implicated the risk of hearing impairment in children exposed

J.-Y. Min et al. / Chemosphere 102 (2014) 6–11

prenatally to PCBs or related contaminants through maternal diet (Grandjean et al., 2001; Trnovec et al., 2008, 2010). In this study we investigated whether environmental exposures to PCBs are associated with hearing impairment in adults who participated in the National Health and Nutrition Examination Survey (NHANES) 1999–2004. 2. Methods and materials 2.1. Study population The NHANES, conducted by the Centers for Disease Control and Prevention, is a nationally representative survey of the non-institutionalized civilian population in the U.S. NHANES study protocols (1999–2004) were approved by the National Center for Health Statistics Institutional Review Board. Oral and written informed consent was obtained from all participants. Serum concentrations of PCBs were measured in a random onethird subsample of subjects aged more than 12 years in the NHANES 1999–2004 survey. Audiometric measures were randomly assessed in a half the NHANES sample of adults aged 20– 69 in 2000–2004. We initially selected 2553 participants who were 20 years or older and had both serum PCBs and audiometric measure. We further excluded 607 participants who had incomplete audiometric examinations (n = 175), unilateral hearing impairment (n = 209), and missing information about hearing related variable including firearm or recreational noise exposure, longest job held, and use of ototoxic drugs (n = 154) and other variables (n = 69). Thus 1946 participants were available for this study. A few participants had missing data for certain serum PCB concentrations. Table 2 illustrates the sample size for PCB congeners. 2.2. Serum polychlorinated biphenyls concentrations Venous blood samples were collected and stored under appropriate frozen (20 °C) conditions. Serum PCB concentrations were measured by high resolution gas chromatography with isotope dilution high resolution mass spectrometry (Turner et al., 1997). Although the PCBs were reported on a whole-weight and lipid-adjusted basis, Schisterman et al. (2005) found that lipid-standardized PCB concentrations shoed a higher percent bias for the effect of PCBs on the outcomes of evaluated statistical models than were wet-weight concentrations adjusted for triglycerides and total cholesterol; therefore, our study used wet-weight concentrations (ng g1) of PCBs. A total of 34 PCBs were measured in the NHANES 1999–2004 survey; we selected PCBs for which the frequency of detection at levels above the limit of detection (LOD) was at least 60%. We also excluded PCBs with more than 90% of the frequency of detection. Because the PCBs that were more than 90% above the LOD occurred in a relatively small number of participants, few or no participants with hearing loss were in the category (reference group of logistic regression model) of PCBs below the LOD. When any of the cell counts is very small, the statistical model does not yield a meaningful result; therefore, our study excluded PCBs with more than 90% below the LOD. Eleven PCBs were thus included in the present analysis: 2,4,40 ,5-tetrachlorobiphenyl (PCB-74); 2,20 ,4,40 5-pentachlorobiphenyl (PCB-99); 2,30 ,4,40 ,5pentachlorobiphenyl (PCB-118); 2,20 ,3,4,40 ,5-hexachlorobiphenyl (PCB-138); 2,20 ,4,40 ,5,50 -hexachlorobiphenyl (PCB-153); 2,20 ,3,30 , 4,40 ,5-heptachlorobiphenyl (PCB-170); 2,20 ,3,4,40 ,5,50 -hepta chlorobiphenyl (PCB-180); 2,20 ,3,40 ,5,50 ,6-heptachlorobiphenyl (PCB-187); 2,20 ,3,30 ,4,40 ,5,50 -octachlorobiphenyl (PCB-194); 2,20 , 3,30 ,4,40 ,5,60 -octachlorobiphenyl (PCB-196); 2,20 ,3,30 ,4,40 ,50 ,60 octachlorobiphenyl (PCB-199).

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2.3. Audiometric measures and hearing impairment Audiometry measures were conducted in a dedicated, soundisolating room in the mobile examination center by trained examiners using a standardized protocol. Instrumentation for the Audiometry Component included an audiometer (Interacoustics Model AD226; Assens, Denmark) with standard headphones (TDH-39) and insert earphones (Etymotic EarTone 3A) (National Center for Health, 2005). An audiometer was calibrated with the same specifications at the start and end of the testing at each field location. Air conduction thresholds were measured for each ear at 0.5–8 kHz across an intensity range of 10 to 120. The 1 kHz frequency was tested twice in each ear as a measure of the reliability of the participant’s responses. Pure-tone audiograms with a 10 dB or greater difference between the 1 kHz test–retest thresholds were not accepted. Hearing impairment was defined as a pure-tone average (PTA) of the thresholds at 0.5, 1, 2 and 4 kHz of >25 dB hearing level (HL) in the better ear, consistent with the definition used by the World Health Organization (World Health Organization). 2.4. Demographic and hearing-related covariates The following covariates were obtained from the questionnaire information: age (20–29 years, 30–39 years, 40–49 years, 50– 59 years, and 60–69 years), sex (male or female), race/ethnicity (non-Hispanic white, non-Hispanic black, Mexican–American, or other), education (less than high school, high school diploma, or college or more), and cigarette smoking (current smoker, ex-smoker, and never smoked). The presence of hypertension was based on a self-reported physician diagnosis, current use of medication, or clinical measure (systolic blood pressure P 140 mmHg/diastolic blood pressure P 90 mmHg). Diabetes mellitus was defined as a self-reported physician diagnosis, current use of medication, or fasting blood glucose P 126 mg dL1). Thyroid disease was defined as a self-reported physician diagnosis and current use of medication. Body mass index (BMI) was calculated as dividing measured weight in kilograms by measured height in meters squared. Triglyceride and total cholesterol levels were included as continuous variables. Occupational noise exposure was calculated by the job title for the longest job held according to the Occupational Network assessment (Choi et al., 2012). Occupational noise exposure groups were divided into low (